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Systematic review of emerging and innovative technologies for meat tenderisation
Accepted Manuscript Systematic review of emerging and innovative technologies for meat tenderisation
R.D. Warner, C. McDonnell, A.E.D. Bekhit, J. Claus, R. Vaskoska, A. Sikes, F.R. Dunshea, M. Ha PII: DOI: Reference:
S0309-1740(17)30169-9 doi: 10.1016/j.meatsci.2017.04.241 MESC 7264
To appear in:
Meat Science
Received date: Revised date: Accepted date:
10 February 2017 19 April 2017 28 April 2017
Please cite this article as: R.D. Warner, C. McDonnell, A.E.D. Bekhit, J. Claus, R. Vaskoska, A. Sikes, F.R. Dunshea, M. Ha , Systematic review of emerging and innovative technologies for meat tenderisation, Meat Science (2017), doi: 10.1016/ j.meatsci.2017.04.241
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ACCEPTED MANUSCRIPT Systematic review of emerging and innovative technologies for meat tenderisation R.D. Warnera*, C. McDonnellb, A.E.D Bekhitc, J. Clausd, R. Vaskoskaa, A. Sikes,e F.R. Dunsheaa, M. Haa a
Faculty of Veterinary and Agricultural Science, University of Melbourne, Parkville,
Food Quality and Sensory Science Department, Teagasc Food Research Centre, Ashtown,
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b
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Victoria, 3010, Australia.
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Dublin 15, Ireland.
Department of Food Science, University of Otago, Dunedin, 9054, New Zealand.
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Department of Animal Sciences, University of Wisconsin, 5306, USA.
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CSIRO Food and Nutrition, 39 Kessels Road, Coopers Plains, Queensland 4108, Australia.
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c
*
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Corresponding author: [email protected]
Keywords: pulsed electric field; high pressure processing; tenderness, texture; meta-analysis;
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ultrasound; shock wave; shockwave; smartstretch
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ACCEPTED MANUSCRIPT List of acronyms PSF = peak shear force. Note: wherever possible, the units used are Newtons, but some authors give peak shear force in kg. PSF (N) = PSF (kg) x 9.8. Where possible, we have converted the units to Newtons.
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PEF = pulsed electric field
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SW = shockwave
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HPP = high pressure processing
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US = ultrasound
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ACCEPTED MANUSCRIPT ABSTRACT Consumers are the final step in the meat supply chain and meeting consumer expectations of quality and tenderness are important for satisfaction and repeat purchase. High pressure processing, shockwaves, ultrasound, pulsed electric field and muscle stretching can be applied to pre- and post-rigor meat for tenderisation. These non-thermal and thermal
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innovative technologies can be used with varying levels of success to cause physical
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disruption to muscle structure, enhanced proteolysis and ageing and muscle protein
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denaturation and solubilisation resulting in changes to texture and juiciness. Results of a meta-analysis are used to compare the effects of these technologies on meat tenderisation. In
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a range of desired textures for meat products.
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the future, a combination of new and innovative technologies will be ideally suited to deliver
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1. INTRODUCTION
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Consumers are the final step in the meat supply chain and meeting their expectations is an important part of their satisfaction (Font-I-Furnois & Guerrero, 2014) and therefore long-term viability of the meat industry.
Consumer experience, perception and in-mouth sensory
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appreciation of meat derives from the traits ‘texture, juiciness and flavour’ and these
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characteristics are highly related to the overall experience of quality, intention to purchase, repeat purchase and willingness to pay (Font-I-Furnois & Guerrero, 2014; Lyford et al., 2010). In some countries with established quality assurance systems, the producer, processor and retailer are paid more for assuring quality and tenderness, an example being the Meat Standards Australia grading system for beef (Acil Allen Consulting, 2016).
Meat quality traits, particularly tenderness, depend on intrinsic and extrinsic factors. These factors include (i) pre-slaughter factors such as species, genotype, nutrition and age of the
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ACCEPTED MANUSCRIPT animal (many of which affect fatness and weight of the carcass), pre-slaughter stress and (ii) post-slaughter factors such as electrical stimulation and hanging of the carcass, ageing of the meat and packaging and conditions during storage and excellent reviews are available on these topics (Young, Hopkins, & Pethick, 2005; Purchas, 2007; Channon, D’Souza, Dunshea, 2016a; Channon, Hamilton, D’Souza, & Dunshea, 2016b; Hocquette et al., 2014; McMillin,
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2008; Strydom & Rosenvold, 2014; Thompson et al., 2006). Traditionally, meat tenderness is
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improved post-mortem through ageing of meat allowing proteolysis to proceed in an
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anaerobic environment, electrical stimulation of red meat carcasses in order to prevent coldshortening, application of stretching techniques such as tenderstretch, and moisture infusion
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(Channon et al., 2016b). The application of each of these techniques has had varying success and application. Furthermore, the modern production of efficient, fast-growing, lean beef,
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lamb, pork and poultry carcasses has resulted in modifications which have generally resulted in a reduction in tenderness and eating quality (Dunshea, D’Souza, & Channon, 2016). One
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opportunity is to overcome the reduced tenderness through the application of novel and
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emerging post-mortem processing technologies. The other opportunity is to develop application of technologies that will accelerate tenderisation, enabling production of tender
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meat at 24 hrs post-mortem.
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New developments in technology have led to the emergence of thermal and non-thermal innovative processing methods for improved microbiological safety, reduced nutritional loss, increased efficiency and modified texture. By manipulating processing parameters, including temperature, atmosphere, time of application (pre- or post-rigor) and pressure, the structural changes of meat during processing are influenced, with a resulting impact on texture and tenderness (Bryony & Yang, 2012). Increases in temperature are associated with high temperature high pressure processing (HPP) (called adiabatic heating) and can also be generated during the application of technologies such as pulsed electric field (PEF), 4
ACCEPTED MANUSCRIPT ultrasound (US) and shockwave, thus a consideration of the effects of heating on muscle structure and proteins is required. The relevance and importance of any incident or applied thermal treatments in determining meat texture is included in the present analysis in order to understand the underlying mechanisms, including the contribution of muscle structure and proteins to the changes in texture with the application of innovative and emerging
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technologies. Note that HPP is not considered an emerging technology, as it was first applied
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to meat in the 1970’s (Mcfarlane, 1973) but the way it is presently being developed and used
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is novel. This paper examines some technologies that can be applied to improve meat
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tenderness and are being investigated for adoption by the meat processing industry.
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2. OVERVIEW OF THE INFLUENCING FACTORS FOR MEAT TENDERNESS
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Tenderness is a multi-parameter sensory attribute and together with juiciness of meat, defines
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a large part of the mouth-feel (Lawless and Heymann, 2010), with texture, juiciness, and flavor together forming the consumers' perception of "overall quality." Meat, and in fact any food, is processed in the mouth (Chen and Engelen, 2012) and the sensory/thermo-
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mechanical material properties are significant for the "mouth-feel" and the taste and release Thus although this review focuses on technologies for
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of aroma, fat, and moisture.
"tenderization," the implicit effects of tenderness on the consumers' perception of overall quality, being both flavor, juiciness, and tenderness, are also important.
A brief overview of meat tenderness, muscle biochemical changes post-mortem, changes in muscle during heating, methods to measure tenderness and some traditional technologies for tenderisation are presented in order to understand how different technologies may affect muscle structure. The effects of heat on the changes in texture of meat depend on water-
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ACCEPTED MANUSCRIPT holding capacity, protein denaturation, solubilisation and gelation, determining the force required to shear the meat (in the mouth), and are described below.
It is important to understand how different technologies may have their effect on texture, sensory tenderness, water-holding capacity and muscle structure, as this assists in
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understanding where technologies used in combination may have additive, interactive or
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multiplying effects.
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2.1 Main determinants of meat tenderness
Tenderness is an important meat quality trait and the biological, structural and physiological
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mechanisms underlying meat tenderness have been extensively investigated (Dransfield &
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Jones, 1980; Harper, 1999; Huff-Lonergan, Zhang, & Lonergan, 2010, Koohmaraie, 1988; Tornberg, 1996). Essentially, meat tenderness is determined by intrinsic factors, such as the amount and solubility of connective tissue (Purslow, 1994), sarcomere shortening during
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rigor development (Marsh & Leet, 1966) and post-mortem proteolysis of myofibrillar and myofibrillar-associated proteins by calpains (Koohmaraie & Geesink, 2006) and cathepsins
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(Ertbjerg, Henckel, Karlsson, Larsen, & Moller, 1999). Post-mortem energy metabolism also affects meat tenderness (Thompson et al., 2006;
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Tornberg, 1996) principally through the effect on the post-mortem structure of the muscle and protein degradation, as discussed below. In addition, external factors, for example, the balance between myofibrillar denaturation, shrinkage in the structure and associated water loss and toughening and solubilisation/gelation of proteins during thermal treatments and heating are known to affect tenderness of meat (Purslow, Oiseth, Hughes, & Warner, 2016; Tornberg, 2005). Interactions occur between the influencing factors, which can be difficult to separate (Harper, 1999) and each of these is influenced to a greater or lesser degree by genotype and the pre- or post-slaughter environment (Warner et al., 2010). Examples of 6
ACCEPTED MANUSCRIPT animal and management factors known to detrimentally affect tenderness, predominantly through influencing muscle protease activity, include the callipyge gene in sheep, a tenderness gene prevalent in the Bos indicus population of cattle and the use of hormonal growth promotants and beta-agonists (Lean & Dunshea, 2014; Warner, Greenwood, Pethick, & Ferguson, 2010; Watson, 2008). The successful application of innovative processing
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technologies for meat tenderisation can be highly dependent on the on-farm management and
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the state of the animal and muscle at time of application.
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2.2 Post-mortem energy metabolism and application of technologies to pre-rigor meat The process of rigor mortis is one of the recognizable signs of death as a result of the
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chemical changes in the muscles, causing the musculature to lose extensibility and become
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stiff. Once an animal is slaughtered, oxygen and blood circulation cease and the muscles are forced to switch to anaerobic metabolism and glycolysis to maintain the generation of ATP. Synthesis of ATP in the muscle is initially by creatine phosphate (CP) but later by
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glycogenolysis and glycolysis. CP usually drops to low levels within 1–2 h post-mortem. When CP levels start to decline, ATP levels also decline, inorganic phosphate increases in the cell, and lactate accumulates concomitantly with increasing hydrogen ion (H+)
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concentration. Once ATP reaches low levels, the extensibility of the muscles starts to
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approach 0% of its original, the pH approaches the final pH, and lactic acid reaches its final concentration of 5–6 mmol g -1 of tissue (in a well-fed, rested animal; Warner, 2016). The decline in the muscle pH post-mortem leads to an increase in intracellular calcium concentration due to altered functions of the sarcoplasmic reticulum and calcium pump leading to rigor development when the ATP production declines. For a detailed account of the biochemical changes in post-mortem meat, see Ferguson and Gerrard (2014) and Warner (2016).
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ACCEPTED MANUSCRIPT Post-mortem energy metabolism in muscle and in particular, glycolysis and rigor onset, are important for determining sarcomere length and the occurrence of shortening-induced toughening (Thompson et al., 2006), protease activity and tenderisation during ageing and myofibrillar spacing which can determine muscle water-holding capacity and tenderness (Hughes et al., 2014). The pre-rigor metabolism and availability of substrate, combined with
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muscle temperature, in any muscle in a carcass will determine the shortening occurring at
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rigor and thus the post-rigor sarcomere length (Koohmaraie & Geesink, 2006). Sarcomere shortening can be due to low temperatures pre-rigor (and consequent cold toughening) or
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high temperatures pre-rigor (and associated heat-toughening) and influences the myofibrillar,
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the connective tissue and also the proteolytic contributions to meat tenderness (Warner et al., 2010). Thus it is evident that control of energy metabolism post-mortem is important for
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producing tender meat.
Meat tenderness varies not only with the rate of glycolysis and rigor onset post-slaughter, but
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also with the extent of glycolysis, classically identified through the ultimate pH (pHu) achieved in a muscle. The relationship between meat pHu and tenderness is quadratic, with a peak in toughness at pHu 6.1 (Purchas & Aungsupakorn, 1993). The improved tenderness as
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ultimate pH increases above 6.1 appears to be largely attributable to improvements in water-
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holding capacity and consequent decreases in cooking losses, and to the greater activity of proteases at pH values close to neutrality (Yu & Lee, 1986). Muscle metabolism pre-rigor in any muscle of a carcass can vary significantly with genetics, nutrition, pre-slaughter stress, muscle fibre type, post-slaughter electrical stimulation and chilling of the carcass (Channon, Payne, & Warner, 2000; Gardner, Kennedy, Milton, & Pethick, 1999; Simmons et al., 2006; Thompson et al., 2006; to name a few good reviews on these topics). Control of meat quality through control of post-mortem metabolism (pH and temperature) is difficult to achieve under commercial conditions and variable responses are 8
ACCEPTED MANUSCRIPT usually due to animal and carcass characteristics rather than processing conditions (Simmons et al., 2006). But if technologies applied to pre-rigor meat are able to; (1) arrest or control the rate of glycolysis, through influencing the glycolytic enzymes, or (2) accelerate the breakdown of membranes and release of proteases, or of ions which activate proteases, they have definite potential for having significant effects on meat tenderisation. This is the
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principal used for applying electrical stimulation to beef and sheep carcasses. It was
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discovered in the 1970’s as a method to accelerate the rate of glycolysis and prevent
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sarcomere shortening due to cold temperatures (Chrystall & Devine, 1978; Davey, Gilbert, & Carse, 1975; Locker, Davey, Nottingham, Haughey, & Law, 1975). The opposite problem
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sometimes now occurs where glycolysis is too rapid in beef carcasses post-mortem, due to electrical stimulation. This causes sarcomere shortening due to high temperatures as the
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muscle enters rigor, protein denaturation and enzyme inactivation during ageing (Gutzke, Franks, Hopkins, & Warner, 2014; Kim, Warner, & Rosenvold, 2014; Warner, Thompson,
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Polkinghorne, Gutzke, & Kearney, 2014).
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2.3 Changes in the texture and structure of meat during heating
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Each piece of meat has a multi-scale, or hierarchical, nature in its’ physical properties, with aspects of the scale being of differential importance in contribution to texture.
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contribution to texture depends on the inherent hierarchical structure of the muscle, including the connective tissue proteins, structural proteins within the muscle cell and degradation or disruption of these proteins. In addition, meat tissue consists of numerous molecules which fragment, denature, interact and solubilise at different temperature and time scales.
The effect of heat resulting from processing technologies, or applied for the preparation of ready-to-eat meals in order to prepare meat for consumption, is also of importance for meat 9
ACCEPTED MANUSCRIPT tenderness. At temperatures as low as 35-40oC, proteins can start to denature, causing shrinkage in the structure, the texture and water loss, with higher temperatures causing more severe effects. Thus any heating arising as a result of the application of a technology needs to be considered, due to consequences for the later sensorial texture subsequent to meal preparation and cooking. This has effects on both meat texture and water-holding capacity,
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and important implications for sensory acceptability.
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Objective measurements of peak shear force (PSF) and subjective sensory evaluations have
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identified two to three phases of changes in toughness/ tenderness (measured by PSF), shrinkage and water loss as a function of temperature. These three phases are summarised in
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Table 1 and are;
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Phase 1 – From 35 to 62oC Transverse shrinkage,
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Water loss,
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Toughening, particularly from 40 to 50-53oC.
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Phase 2 – from 50 to 60-65 oC, a transition phase, which overlaps phase 1 and phase 3, Both transverse and longitudinal shrinkage can occur,
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Sometimes a phase of tenderisation or a plateau is observed.
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Phase 3 - From 60 °C to 80 °C, -
Longitudinal shrinkage,
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Increased water loss,
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Toughening usually occurs, although some observe no change.
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ACCEPTED MANUSCRIPT In spite of the potential and actual variability in experimental heating conditions, species and muscles studied, the studies shown in Table 1 show a consistency of response in showing two to three phases, with the two main phases being toughening and water loss in response to an increase in temperature. Concomitant with the texture changes, heat induces transversal and longitudinal shrinkage of meat, which result in water loss as shown in Table 1 and Figure 1.
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Juiciness is a result of the inherent moisture and fat content of the meat and the release of
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fluids from the muscle structure during oral processing.
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2.4 Measurements of texture and tenderness
In-mouth sensory tenderness is generally correlated to instrumental measures of texture
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(Font-I-Furnois & Guerrero, 2014). Measurements of peak shear force shows a very good correlation to sensory tenderness scores, as shown in Figure 2A (Perry, Thompson, Hwang,
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Butchers, & Egan, 2001). A threshold of peak shear force (PSF) = 40 N (4.1 kg) for sensory
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acceptability of beef tenderness has been established (Huffman, Miller, Hoover, Wu, Brittin, & Ramsey, 1996; Rodas-González, Huerta-Leidenz, Jerez-Timaue, & Miller, 2009). Figure
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2B shows that beef steaks scored by people, in both the home and in a restaurant, as extremely tender, had an instrumentally measured mean PSF of 3.7-4.0 kg. A threshold, for
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acceptability of tenderness, of 40N is used in subsequent discussions in this review.
2.5 Some traditional methods to improve meat tenderness Traditionally, ageing of meat for a period of time post-mortem in an anaerobic environment allows proteolysis to proceed and flavour and tenderness to develop (Koohmaraie & Geesink, 2006). Electrical stimulation applied to sheep, beef and more recently venison carcasses induces rapid glycolysis (see above), preventing sarcomere shortening (cold-shortening) as
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ACCEPTED MANUSCRIPT well as likely disrupting muscle tissue, accelerating proteolysis and resulting in more tender meat (Hopkins, 2014). Tenderstretch, or other stretching techniques discussed in a later section, not only prevent sarcomere shortening but likely also result in muscle disruption and tenderisation (Hopkins, 2014). Moisture infusion can reliably induce improved tenderness in meat as well as juiciness (Channon et al., 2016b). Each of these procedures has met with
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some success, with all of these techniques still being used today. But each technique has
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limitations including, inherent problems for application on-line in modern plants, requirement
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for extensive storage periods influencing efficiency of inventory control or unacceptability for the modern consumer. Thus the need for new and alternative technologies which address
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these deficiencies are required.
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Under the appropriate pressure, temperature and time post-mortem conditions, HPP has been shown to induce tenderisation in meat (see below). Apart from a high energy requirement and the initial capital outlay, which create an impact on the cost of technologies and thus
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industry feasibility, thermal processing during HPP application to meat can lead to undesirable side effects such as nutritional loss or flavour issues (Knorr, Ade-Omowaye, & Heinz, 2002). In addition, HPP application to meat, with associated heating, results in a
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‘cooked’ appearance to the meat. Thus there has been strong industry interest to develop and
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use non-thermal treatments in food processing, such as ultrasonics, shock wave, pulsed electric field and pre-rigor stretching. These technologies, including HPP, are discussed below.
3. HIGH-PRESSURE PROCESSING (HPP)
High pressure processing (HPP) is a technique in which a pressure is applied statically to a product, at or above 100 MPa by means of a liquid transmitter (Simonin, Duranton, & de 12
ACCEPTED MANUSCRIPT Lamballerie, 2012). The pressure is isostatically and uniformly transmitted to the product (Norton & Sun, 2008). In theory, this pressure is transmitted almost instantaneously to the product, and is not dependent on the size and shape of the product, however, in commercial HPP processes, it does take time for the pressure to build up. HPP of food products, and of meat, has generally focussed on extending the shelf-life and improving food safety. The
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application of HPP for meat tenderisation was demonstrated a number of years ago (Bouton,
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Ford, Harris, Macfarlane, & O'Shea, 1977; Bouton, Harris, Macfarlane, & O'Shea, 1977a),
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but its implementation in industry has been slow. HPP can also either be applied to pre- or post-rigor meat. Excellent reviews are available on this topic (Buckow, Sikes, & Tume,
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2012; Guillou, Lerasle, Simonin, & Federighi, 2017; Ma & Ledward, 2013).
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The textural outcome of applying HPP to meat depends on the pressure applied, the temperature, the time, the muscle and the time post-mortem, with the consequent results
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varying from toughening to significant tenderisation. These variations are described below.
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Importantly, during application of high pressure, adiabatic heating occurs which is equivalent
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to 3oC per 100 MPa (Table 2).
As shown in Hughes et al. (2014), there is a change in the colour of meat, as a consequence
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of the application of HPP. When HPP is applied at 10oC, pressures above 100 MPa result in subtle to obvious changes in the visual appearance, as the pressure increases. For this reason, HPP tends to be considered as a viable option for ready-to-eat food, but not for the ‘fresh food’ shelves, limiting its commercial application.
There is an R&D opportunity to
investigate the retention of fresh meat colour in HPP-treated muscle foods.
3.1 Mode of action
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ACCEPTED MANUSCRIPT HPP influences both the structure and function of proteins (Lee, Kim, Lee, Hong, & Yamamoto, 2007) and is known to modify only non-covalent bonds, thus not affecting small flavour molecules or vitamins. In contrast, heat affects hydrogen and covalent bonds, and thus results in both unfolding and irreversible denaturation of proteins. HPP can either be applied at ambient or low temperatures, or at high temperatures, with differential effects on
Whereas pressure favours dissociation and
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the aggregate remains stable after cooling.
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meat proteins and texture. Temperature denatured protein has a tendency to aggregate and
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unfolding of proteins, with refolding and re-association once the pressure is removed (Smeller, 2002). The diagram in Figure 3 shows that in comparing the structures of pressure-
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and heat-denatured proteins, there are three phases for protein structure being native, intermediate/unfolded and intermediate/aggregated.
The diagram also shows that above
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40oC, the aggregated state is more stable than the intermediate and also that the intermediate and unfolded states cannot form an aggregate if the pressure is above 200 MPa (Smeller,
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2002). Alternatively, Sun & Holley (2010) have stated that the changes in proteins are
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usually reversible below 300 MPa, but irreversible above 300 MPa. Meat tenderisation is often associated with increases in protein solubility and HPP treatment appears to induce
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tenderisation through increasing protein solubility as a result of depolymerisation of proteins
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under pressure (Sun & Holley, 2010).
Under HPP treatment, noncovalent interactions between proteins are destabilized and a small degree of unfolding occurs, with subsequent formation of hydrophobic and disulphide bonds after pressure release (Sun & Holley 2010). When pressure is applied at ambient temperature, there appears to be little to no change to the connective tissue (background toughness) because collagen, the main protein, is stabilised by hydrogen bonds (Gekko & Koga, 1983). When pressure is applied at high temperatures (especially 60-70oC), collagen in connective
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ACCEPTED MANUSCRIPT tissue denatures and unfolds and may contribute to the increased tenderisation observed (Ma and Ledward, 2004). The increased hardness or toughness of post-rigor meat subjected to HPP at ambient temperatures may also be due to a greater integrity in the myofibrillar structure (Jung, de Lamballerie-Anton, & Ghoul, 2000a; 2000b).
Generally, the HPP
treatment of fresh meat at high temperatures results in greater tenderness after cooking,
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whereas similar meat without HPP treatment becomes tougher after cooking. The increase in
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tenderness of high temperature-HPP is variously attributed to accelerated proteolysis (Ma &
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Ledward, 2004), increased fracturing of myofibrillar proteins and muscle structure due to greater stability of collagen (Sikes, Tornberg, & Tume, 2010), increased protein
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solubilisation (Sun & Holley 2010), reduced water loss from the myofibrillar structure (Hughes, Oiseth, Purslow, & Warner, 2014), or combinations of these, depending on the
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3.2 Application to pre-rigor meat
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conditions applied.
The application of HPP, at 100-225 MPa and 10-35oC, to pre-rigor meat has consistently been shown to improve the tenderness of beef, lamb, poultry and pork. There has also been a
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patent developed by Hormel foods on this process, for pork (Smit, Summerfield, & Cannon,
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2010). The tenderisation associated with HPP of pre-rigor meat is proposed to be a result of either accelerated or arrested glycolysis (Sikes & Warner, 2016).
Accelerated glycolysis, as measured by pH drop in muscles post-pressurisation (Macfarlane, 1973), is most likely a result of release of calcium during the application of pressure, and this is associated with severe contraction resulting in massive disruption to the myofibrillar structure and very tender meat (Bouton et al., 1977a; Kennick & Elgasim, 1981; Kennick, Elgasim, Holmes, & Meyer, 1980; Macfarlane, 1973). Where HPP was applied to pre-rigor
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ACCEPTED MANUSCRIPT meat and the result was accelerated glycolysis, the increase in tenderness is usually quite large (in the range of 30-80% improvement) across different muscles and species. Bouton et al. (1977a) applied HPP to pre-rigor beef semitendinosus (103 MPa, 35C, 4 min) and if the muscle was not restrained prior to HPP application, the PSF reduced from 188 N in the control to 38 N, a significant change from a highly unacceptable texture to a desirable and
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acceptable product. A PSF = 40 N has previously been reported to be the threshold for
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consumer panel assessment of acceptability of beef tenderness (see previous section). If the
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muscle was restrained prior to HPP application, the resulting PSF was 71 N and much tougher than the HPP-treated non-restrained muscle (Bouton, Harris, et al., 1977a), providing
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evidence that severe shortening causes major disruption and tenderisation.
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Arrested glycolysis during HPP treatment of pre-rigor meat is proposed to arise from the denaturation of glycolytic enzymes during the application of pressure, resulting in a higher
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ultimate pH in the muscle (Smit et al., 2010). Partial inhibition of glycolysis as a result of
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application of HPP to pre-rigor meat has only been demonstrated by Smit et al. (2010) and Souza et al. (2011). Souza et al. (2011) applied HPP to pre-rigor pork carcasses (215 MPa,
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33°C, 15 s) and measured the change in texture for the longissimus, psoas major, triceps brachii and semimembranosus muscles. Although HPP treatment significantly increased
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(P<0.01 for al muscles)the ultimate pH compared to the control in the longissimus (6.26 vs 5.78, respectively), semimembranosus (6.48 vs 6.01) and triceps brachii (6.35 vs 6.08) (P<0.01 for al muscles), a significant (P=0.03) decrease in PSF was only seen for the semimembranosus, (21 vs 25 N; Souza et al., 2011). These results demonstrate the difficulty in inducing reliable tenderisation across all muscles, through the application of HPP to prerigor meat. It is well-known that there is considerable variation between muscles and carcasses in the stage of rigor, and thus muscle pH and sarcomere length at any defined time point in the pre-rigor period. Furthermore, if HPP applied to pre-rigor meat is successful in 16
ACCEPTED MANUSCRIPT arresting glycolysis and results in a higher muscle pH, the curvilinear relationship between muscle pH and tenderness predicts that elevated muscle pH may increase meat toughness (Purchas, 1990). Elevated muscle pH can result in shorter sarcomere length and depending on the level of elevated pH, either higher or lower proteolysis (Purchas, 1990), thus varying
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effects of muscle pH on meat tenderness are observed.
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3.3 Application to post-rigor meat at a low temperature
The application of HPP to post-rigor meat at low or ambient temperatures has shown quite
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variable effects on texture and tenderness, depending on the time, temperature and pressure
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used. Application of high pressure at ambient or low temperature (0-25oC) usually results either in no change in tenderness, or an increase in toughness in beef, pork, lamb, alligator
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and poultry meat (Gimenez et al., 2015; Jung 2000a; 2000b; Duranton et al., 2012; Kim et al., 2007; Grossi et al., 2014; Hong et al., 2005; Hong et al., 2012; Kruk et al., 2011;
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Macfarlane et al., 1981; Ma and Ledward 2004; Zamri et al., 2006; McArdle et al., 2011;
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McArdle et al., 2013). Only five out of 17 references in the review by Sikes and Warner (2016) showed any evidence for tenderisation of meat when HPP is applied at ambient or low
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temperatures. In these five studies, the tenderisation was highly dependent on the muscle, pressure, temperature and time applied. The change in PSF values in beef longissimus
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thoracis et lumborum was from about 58 to 38 N (estimated from graph) when HPP was applied at 100 MPa for 10 min, with no tenderisation evident for higher pressures of 200-300 MPa (Schenková et al., 2007). Ichinoseki, Nishiumi, and Suzuki (2006) showed a reduction in PSF values from 58 to 45 N when HPP was applied at 100-500 MPa, at 8oC for 10 min.
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ACCEPTED MANUSCRIPT 3.4 Application to post-rigor meat at a high temperature Application of high pressure at higher than ambient temperatures (>25oC), generally results in tenderisation. Generally, optimum tenderisation is evident for HPP applied at 100-200 MPa and at temperatures of 60-70°C (Ma & Ledward, 2004; McArdle, Marcos, Mullen, & Kerry, 2013; Rusman, Gerelt, Tamamoto, & Nishiumi, 2007). Across the thirteen studies
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reviewed by Sikes and Warner (2016), all studies showed tenderisation of 30-80%, through
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measurements of hardness or PSF, when the pressure applied was in the range 150-400 MPa
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and the temperature was above 50-60oC for beef, lamb, pork and chicken, across a range of muscles (Bouton et al., 1977a; Bouton et al., 1977b; Ratcliff et al., 1977; Bouton et al., 1980;
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Beilken et al., 1990; Ma & Ledward 2004; Rusman et al., 2007; Sikes et al., 2010; McArdle et al., 2011; McArdle et al., 2013; Sikes & Tume 2014). Pressures above 400 MPa resulted in
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toughening of meat (Ma & Ledward, 2004; McArdle et al., 2013; Zamri, Ledward, & Frazier, 2006), while HPP treatment at 200 MPa for 20 min of beef sternomandibularis,
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50 N (estimated from graphs).
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semimembranosus and biceps femoris reduced the PSF from about 110-130 N down to about
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3.5 Considerations for the future
The application of HPP to meat is no longer seen as an alternative process to conventional
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pasteurisation but as a technology to create new meat-based products. However, pressureinduced changes affecting the colour quality are significant for fresh red meat and need to be considered when evaluating marketability and consumer preferences of new products. High pressure applied at low or ambient temperatures is a commercially viable process but necessitates processing of muscle in the pre-rigor state to achieve tenderisation. This process would reduce the aging time compared to current protocols and as moderate pressures are needed, there is no impact on colour quality. The improved tenderness and yield of post-rigor
18
ACCEPTED MANUSCRIPT meat when HPP is applied at higher temperatures also has potential as a commercial process but would be limited to a specific market, such as the food service industry, due to the impact on colour stability. High pressure processing is unlikely to totally replace traditional meat processing methods but could be used in combination with, or to complement, current
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methods or to discover niche applications and markets.
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4. SHOCKWAVES
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Shockwaves, or hydrodynamic pressure processing, involve the application of high pressure waves up to 1 GPa in fractions of a millisecond (Bolumar, Enneking, Toepfl, & Heinz, 2013)
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which propagates through a fluid (typically water). The shockwaves can be generated by
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piezoelectric, electromagnetic, electro-thermal or electro-detonation methods (Bolumar et al., 2013). The two methods that have been trialled for meat tenderisation are; (a) chemical, by
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detonating explosives underwater, first described by Long (1993) and shown to tenderise beef
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meat (Solomon et al., 1997) and (b) electrical discharge underwater, which was first described by Long (2000) and shown to tenderise poultry meat by Claus et al. (2001b, 2001a). The electrical discharge system can either be via discharging a high voltage arc
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across a gap between two electrodes in water (Long & Ayers, 2001) or via a sparker system
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(Bowker et al., 2011). Details of the principles of the design of the equipment, various configurations for both chemical detonation and electrical discharge and the effects on meat have been described previously (Solomon et al., 1997; 2006; Bolumar et al., 2013; Claus, 2017). During the application of explosive-based shockwaves, the pressure wave of ~100 MPa results in a small increase in temperature of 2-3oC (Table 2). There appears to be no increase in temperature when electrically-generated shockwaves are applied (Table 2).
4.1 Mode of action 19
ACCEPTED MANUSCRIPT The principle of hydrodynamic shockwaves is that they travel through water and also anything that is an acoustical match with water (Claus et al., 2001b). Thus, as meat is 75% water, it is an acoustical match for water and when shockwaves are applied to muscle, the shockwave reflects off any object that is not an acoustical match (Solomon et al., 1997), resulting in ultrastructural damage to the muscle (Zuckerman et al., 2013) and proteolytic
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enzyme release (Bowker et al., 2008).
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There are some indications that shockwaves disrupt the collagen fibril network of the endomysium (Zuckerman et al., 2013). Previous research has shown that detonation
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shockwaves applied to beef longissimus cause fragmentation in the I-band and that the jagged edges of thin filaments next to the Z-line imply physical disruption of myofibrillar proteins
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rather than proteolysis (Zuckerman and Solomon 1998). Others have also shown physical disruption to the muscle fibres and tissues, particularly to the myofibrils and the Z-line (Claus
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et al., 2002; Bolumar et al., 2014). The degradation of troponin-T (TnT) to a 30 kD protein is
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widely used as an indicator of tenderisation due to proteolysis (Huff-Lonergan et al., 1996). Bowker et al. (2008) used SDS-PAGE and Western blotting to show that shockwave
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treatment increased the tenderisation of beef longissimus and enhanced the accumulation of 30kD TnT degradation products, indicating enhanced proteolysis. Bolumar et al. (2014) did
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not show any effect of shockwave treatment of beef longissimus on myofibrillar proteins but as Western blotting was not used, the sensitivity of their assay may have been compromised.
4.2 Explosive shockwaves The early work on the application of a detonation (100 g of explosives) shockwave to beef muscle showed a major effect on the texture of very tough beef, the result being very tender
20
ACCEPTED MANUSCRIPT meat in most cases (Solomon et al., 1997). The muscles tested varied in connective tissue content as well as protease activity and the PSF value was reduced from 78-129 N in controls to 28-57 N in treated muscles, a 55-66% reduction (Solomon et al., 1997). Detonation shockwaves applied to beef semimembranosus after 7 days ageing resulted in a reduction in PSF by >20 N, from 62 to 39 N (Zuckerman et al., 2013). This is a significant reduction, as it
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was induced in a muscle that had already undergone ageing and also is known to be tough
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due to low protease activity, high amounts of connective tissue and relatively short sarcomere
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length (Rhee et al., 2004). Furthermore, after 21 days of ageing post-treatment, shockwavetreated semimembranosus was still more tender than controls (Zuckerman et al., 2013). In
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contrast, turkey pectoralis (a muscle with low connective tissue) treated with electrical shockwave at 3 days post-mortem showed very little tenderisation, although the muscle was
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already very tender prior to treatment (Claus et al., 2001b). The structural myofibrillar and collagen (connective tissue) proteins are largely responsible for the toughness of meat. The
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most well-documented effect of shockwave tenderization is on physically breaking the
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myofilaments, thus in the case of the semimembranosus in the experiment of (Zuckerman et al. (2013), shockwave appeared to achieve a similar tenderising effect to high protease
turkey pectoralis
in Claus et al. (2011b), shockwave does not induce any further
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tenderisation.
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activity. When the meat is already tender when the shockwave is applied, as in the case of
Previously, application of a detonation shockwave to pork loin has shown small levels of meat tenderisation, as measured by PSF (32.4 N, 26.9 N; P<0.01), although a trained panel could not pick up any differences in tenderness (Moeller et al., 1999). The largest effects of detonation shockwaves on tenderisation have been seen in lamb longissimus (57-60 N for control and 19-43 N for shock-waved muscles) (Solomon et al., 1998), beef longissimus, semimembranosus, biceps femoris, semitendinosus (see above; Solomon et al., 1997) and 21
ACCEPTED MANUSCRIPT poultry pectoralis (60 N for control and 43 N for treated) (Meek et al., 2000). The biggest reduction in toughness with detonation shockwaves is seen with the highest amount of charge [for comparisons, see (Solomon et al., 1997; Meek et al., 2000)] and does vary with both muscle and species. As discussed above, low to zero levels of tenderisation have been seen for pork longissimus and turkey pectoralis as a result of detonation shockwaves (Moeller et
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al., 1999; Bowker et al., 2010), most likely because the muscles being treated were not
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considered tough. In the case of turkey pectoralis, the control samples had a PSF of 25 N and
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after detonation shockwaves, the PSF was 29 N, and not different to control (Bowker et al., 2010). A PSF of 25 N is very tender and acceptable to consumers.
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4.3 Electrical shockwaves
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Recent research using commercial units/prototypes has shown promise for tenderising, beef, pork and poultry (turkey chicken) using electrical discharge shockwaves. Applying electrical
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discharge shockwaves to hot- or cold-boned poultry pectoralis has been shown to result in
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tenderisation by 10-20 N (Claus et al., 2001b; 2001a). Pork semimembranosus and semitendinosus showed no change in tenderness in response to 2 pulses of electrical discharge shockwave from a commercial prototype (Bolumar et al., 2013). In contrast, using
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the same unit, beef ST and LL showed reductions in PSF from 84 to 63 N and 48 to 39 N,
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respectively (Bolumar et al., 2013). The reason for the difference between species is unclear, as the pork muscles were not particularly tender (43 N for SM; 70 N for ST). For electrical shockwaves, the reductions in toughness are generally about 10-30% across beef, pork, turkey and chicken (Bolumar et al., 2013) and have not shown the dramatic tenderisation as seen for detonation shockwaves. For electrical shockwaves, increased tenderisation results from repeating the pulses and increasing the energy setting (Bowker et al., 2011; Bolumar et al., 2013). Due to concerns with the use of explosives, the technology for tenderising meat using shockwaves now centres around electrical discharge. The use of electrical discharge to 22
ACCEPTED MANUSCRIPT apply the shockwaves allows continuous operation, rather than a ‘batch’ system, which is a characteristic of the shockwave systems utilising detonation. Recent research testing industrial-scale equipment for applying electrical shockwaves has shown no effect on pork semimembranosus and semitendinosus tenderness and a moderate reduction in beef longissimus and semitendinosus (84 to 63 N for longissimus and 48 to 39 N for
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semitendinosus) (Bolumar et al., 2013).
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4.4 Future
Although creating hydrodynamic shockwave by the detonation of explosives in water has
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demonstrated significant tenderization, attempts to commercialize a system based on explosives has encountered technological challenges that have not been overcome.
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Application of explosive shockwaves requires that the meat is vacuum packaged, as the meat needs to be immersed in the same water that the shockwave is produced. When the explosive
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is detonated, a very high percentage of the bags have previously been shown to fail, exposing
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the meat to the processing water, including unknown combustion components, as well as elemental metal released from the shockwave electrodes. Additional problems include the
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safety issues associated with using explosives, lack of durability of the system and the
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predicted very high infrastructure and equipment costs to build the system.
Electrical-based generation of a hydrodynamic shockwave generating system is an emerging technology that is based on the well-established principle that shockwaves can tenderise meat.
Unlike the explosive-based approach, with electrical-based systems it is entirely
feasible to expose the meat to shockwaves multiple times, for additional tenderization. Two somewhat similar electrical-based systems are being developed (Claus, 2002; Bolumar et al., 2014), both with high chances of commercialization. The main difference between the systems is that the system described by Claus (2002) physically separates the meat from the 23
ACCEPTED MANUSCRIPT shockwave processing water. This eliminates any issues associated with the meat absorbing the processing water. In the system described by Bolumar et al. (2014), the meat is exposed to the processing water.
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5. PULSED ELECTRIC FIELD (PEF)
Pulsed electric field (PEF) is one of the novel non-thermal technologies being investigated by
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the food industry to improve the food safety, modify food texture and improve the extraction
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of bioactive compounds. The technology is regarded as an efficient green technology due the short time processing time, fossil fuel-free technology and generates no waste compared to
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traditional processing options. PEF is a treatment of food involving generation of an electrical
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field between two electrodes using direct current voltage pulses for periods of time ranging from microseconds to milliseconds. The theory behind PEF and its applications in food plants
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and biomaterial processing have been examined in depth in several books and review papers
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(Arroyo & Lyng, 2017; Donsi, Ferrari, & Pataro, 2010; Puertolas, Luengo, Alvarez, & Raso, 2012; Raso-Pueyo & Heinz, 2006; Toepfl, Heinz, & Knorr, 2006; Vorobiev & Lebovka, 2008). The potential of PEF to improve food qualities has been investigated (Fryer &
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Versteeg, 2008; Luengo, Álvarez, & Raso, 2013; Wiktor, Schulz, Voigt, Witrowa-Rajchert,
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& Knorr, 2015) and the use of PEF as a post-mortem treatment to enhance qualities of muscle food has only recently been investigated.
Although referred to as a ‘non- thermal’
technology, the application of PEF to food can result in a temperature rise of 5-30oC (O'Dowd, Arimi, Noci, Cronin, & Lyng, 2013) (Table 2) and is called a mild “ohmic” heating (O'Dowd et al., 2013).
Because PEF is an emerging technology in food processing, the amount of research on the potential of PEF in meat is limited in comparison with processing of other food types. 24
ACCEPTED MANUSCRIPT However, recent studies on the effect of PEF on different beef muscle types have shown promising results. As tenderness is arguably the most important attribute of meat, most of the research in this field has focussed on the effect of PEF treatment on meat tenderisation.
5.1 Mode of action
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Cellular membranes become more permeable due to electroporation as a result of the
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application of PEF to biological tissues. Pre- or post-rigor meat treated with PEF prior to
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ageing likely results in membrane damage, which would potentially result in; (i) calcium release from cellular organelles thus activating the calcium-dependent proteases, calpains (ii)
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release of cathepsins from lysosomes, (iii) accelerated glycolysis in pre-rigor meat as a result of the calcium release, all of which could enhance tenderisation. As indicated by Bekhit, van
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de Ven, Suwandy, Fahri, and Hopkins (2014b), a post-treatment aging step is required to overcome the lack of immediate effect for PEF treatment on beef tenderness found by
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O'Dowd et al. (2013) or after short aging period of 2 days (Arroyo, Lascorz, et al., 2015).
5.2 Application to post-rigor (cold-boned) meat
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Application of different strengths of PEF treatment has shown intriguing results. The
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application of a low field strength PEF treatment (1.4 KV.cm-1, 10 Hz) with 300 or 600 pulses of 20 μs each to 48 h post-mortem beef longissimus lumborum at different stages of ageing did not result in a significant change in PSF (88N to 74N) (Arroyo et al., 2015). Further aging times for 10, 18 and 26 days post-treatment tended to indicate lower PSF in PEF treatment samples compared with the non-treated controls at P < 0.1. High intensity PEF (10 kV.cm-1, 90 Hz) applied to cold-boned (24 h post-mortem) longissimus lumborum resulted in a reduction of ~25 N (57 N to 35 N) in 21 day aged meat (Suwandy, Carne, van de Ven, Bekhit, & Hopkins, 2015c, 2015d). The effect of PEF on tenderisation varies with 25
ACCEPTED MANUSCRIPT the treatment intensity, i.e. the voltage and frequency of the applied PEF. Application of 5 kV.cm-1 at 90 Hz or 10 kV.cm-1 at 20 Hz PEF to cold-boned (24 h post-mortem) beef longissimus lumborum produced the greatest tenderisation (PSF reduced from 61-64 N to 4950 N after 21 days of ageing) relative to 5 kV.cm-1 at 20 or 50 Hz PEF (Bekhit, van de Ven, Suwandy, Fahri, & Hopkins, 2014b; Suwandy, Carne, van de Ven, Bekhit, & Hopkins,
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2015a). In addition, when the high intensity PEF (10 kV.cm-1, 90 Hz) is repeatedly applied,
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the PSF value decreased by an average of 2.5 N with each application (61 N to 51 N)
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(Suwandy et al., 2015d). Interestingly, proteolysis analysis using SDS-PAGE and Western blotting indicated that, while degradation of troponin-T and desmin were associated with a
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reduction in PSF of meat cuts treated once with PEF, the absence of degradation of these two proteins in samples treated with PEF two and three times suggested another mechanism, such
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as physical disruption of myofibrils, is involved in the tenderisation process (Suwandy et al., 2015d). Although PEF is theoretically a non-thermal technique, high intensity PEF treatment
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of meat has been shown to induce heating in meat samples, as demonstrated in various
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studies (Bekhit, van de Ven, et al., 2014b; Suwandy et al., 2015c; 2015d). The muscle temperature was elevated by 12.6-16.2oC after PEF of cold-boned beef longissimus cuts
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Suwandy et al., 2015d. This elevated temperature may contribute to an increase in myofibrillar protein and enzyme denaturation, likely explaining the absence of troponin-T
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and desmin degradation in meat samples subjected to repeated PEF treatment (Suwandy et al., 2015d).
It is well-known that muscle types differ in morphology, fibre type composition, intrinsic myofibrillar proteomic composition and metabolic properties, resulting in differing meat qualities (Tornberg, 2005). The effect of PEF treatment in different muscle types was examined under different PEF intensities, and repetition of treatment coupled with varying
26
ACCEPTED MANUSCRIPT ageing durations. A difference in PSF reduction was observed between beef cold-boned longissimus lumborum and semimembranosus muscles treated with different PEF voltages and frequencies (Bekhit et al., 2014b; O'Dowd, Arimi, Noci, Cronin, & Lyng, 2013; Suwandy et al., 2015a) that reflected signficant effects for the muscle and the processing conditions. Differences in the amount of heat generated between beef longissimus and
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semimembranosus due to PEF treatment may explain the differences between the muscles in
This also suggests that meat composition and
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Suwandy et al., 2015a; 2015b, 2015d).
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PSF reduction and proteolysis post-treatment (Bekhit et al., 2014b; Bekhit et al., 2016;
probably muscle fibre type play a role in the variation in tenderisation response to PEF
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between muscles.
5.3 Application to pre-rigor (hot-boned) meat
The effect of PEF on meat qualities of hot-boned muscles has also recently been examined
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and has been found to have differential effects on different muscles. Application of PEF at 510 kV.cm-1 tended to cause an increase in the toughness of the longissimus lumborum with increasing PEF frequency (20, 50, 90 Hz) whereas the semimembranosus tended to show a
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decrease in PSF (by about 25 N at each time point) with an increase in PEF frequency
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(Bekhit, Suwandy, Carne, van de Ven, & Hopkins, 2016a; Suwandy, Carne, van de Ven, Bekhit, & Hopkins, 2015b). The authors also showed an increase in the toughness (increased from 60 to 74 N) of hot-boned beef longissimus lumborum with repeated high strength PEF treatment (10 kV.cm-1 and 90 Hz) whereas the semimembranosus was more tender after repeated PEF treatment. The effect of PEF on the water holding capacity of beef was found to differ between the two muscle types (Bekhit et al., 2016a; Suwandy et al., 2015b), which may have contributed to the differences in tenderisation. Changes in the micro-environment at the cellular level can affect the activity of calpains (Huff-Lonergan & Lonergan, 2005). For 27
ACCEPTED MANUSCRIPT example, an increase in ionic strength that can be expected with electroporation of the cells ,after US application, and the moisture available to sustain the released ionic components, would both affect calpain activity.
5.4 Future
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The limited research on the effect of PEF in muscle foods has indicated some potential for the
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application of PEF for tenderisation as a post-mortem technology to improve meat qualities.
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Optimum processing parameters appears to differ for the various muscles. More research is required to evaluate the impact of PEF on commercially important muscles other than those
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already studied. Thus the variable effect on meat texture between different muscles needs to be resolved and further research is required to understand the mechanism by which PEF
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affects muscle structure. In addition, it appears that the design and application of different intensities and repetitions of PEF treatment in order to achieve desirable sensory attributes in
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different meat cuts needs further consideration.
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6. ULTRASONICS (US)
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Power ultrasound (US) is a non-thermal technology based on sound energy. As the sound wave travels between high (compression) and low (rarefaction) pressure, microscopic gas bubbles oscillate and grow in size. The process will continue until the bubble implodes, resulting in a phenomenon known as cavitation (Tiwari, 2015). The efficiency of cavitation is dependent on several factors. Predominantly, the frequency of the sound wave will determine whether cavitation occurs and if it is stable and transient cavitation (Tiwari, 2015). At frequencies of 18-100 kHz, microscopic gas bubbles have approximately 25 µs to grow during the rarefactional cycle, leading to less frequent but more violent cavitation (Crum, 28
ACCEPTED MANUSCRIPT 1995). Excellent reviews are available in Misra et al. (2017) and in Alarcon-Rojo et al. (2015).
6.1 Mode of action It has been suggested that tenderisation of post-rigor meat using ultrasound is by one or a
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combination of; (a) physical disruption of the tissue caused by cavitation (Jayasooriya et al.,
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2004), (b) release and activation of enzymes (Roncales et al., 1993) and/or by (c) altering the
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metabolism in pre-rigor meat by the release of calcium (Got et al., 1999). Ultrasound application has some potential for improving the texture of post-rigor meat. However, for this
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to be a commercial viability, the acoustic conditions need to be thoroughly investigated in
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order to optimise the conditions for tenderisation.
Along with bubble implosion, other mechanical actions which occur during US application
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can induce physical and chemical changes in a medium. Pressure fluctuations are known to
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squeeze and release a medium, which in combination with bubble oscillations can cause agitation and micro-stirring. The implosion of the bubble can cause a micro-jet, which if
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directed at a solid surface, can induce physical disruption. In the case of meat, this has been shown to disrupt myofibrils (Got et al., 1999). Moreover, the action of cavitation may split
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molecules, resulting in free radical formation and accelerated chemical reactions (Crum, 1995). Therefore, care must be taken to optimise US studies for tenderisation while limiting oxidation. As many factors affect the efficiency of cavitation such as parameters of the medium (viscosity, dissolved gas, temperature), vessel (geometry, material) and acoustics (frequency, intensity, amplitude, treatment time), optimisation and measurement of the acoustic field are important. Several authors have discussed these factors in more detail (Crum, 1995; Raso et al., 1999; Tiwari, 2015).
29
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Although it has been suggested that US could possibly fragment collagen, damage cell membranes, affect protease activity and disrupt meat structure (Misra et al., 2017), further work is required to fully understand and optimise the penetration depth of US in meat. As demonstrated by McDonnell et al. (2014), US (20 kHz, 19 W cm-2, 40 min) caused an
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increase in denatured myosin on the surface of pork LTL (<2 mm depth) during ultrasonic
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salting. Myosin denaturation was attributed to the US treatment as the salt concentration was
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low (5.7% w w-1 NaCl) and myosin peaks were evident in differential scanning calorimetry (DSC) graphs for all other samples, including control samples, which had been treated with This indicates that the actions of US may be strongest at the surface of meat.
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salt.
Furthermore, studies indicate that frequency, intensity and treatment time play an important
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role in US efficiency. Importantly, temperature increases of 15-30oC can occur when ultrasound is applied to meat, depending on the experimental set-up (Jayasooriya, Torley,
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D’Arcy, & Bhandari, 2007) (Table 2). The rise in temperature is attributed to the conversion
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of ultrasonic energy into heat (Jayasooriya, Torley, D’Arcy, et al., 2007).
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6.2 Low intensity US applied to post-rigor meat
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It is difficult to conclude on the effect of US on meat texture due to variation in the US parameters and results of studies. It has been suggested that intensities below 10 W cm-2 do not have a tenderising effect on meat (Alvez et al., 2013). This has been been corroborated by other studies, predominantly using ultrasonic baths whereby the intensity is low due to a large emmitting surface at the base of the bath. Lyng et al. (1997) treated beef Longissimus thoracis et lumborum (LTL), Semimembranosus (SM) and Biceps femoris (BF) in an ultrasonic bath (30-47 kHz, 0.29-0.62 W cm-2, 5-90 min) and found no effect on peak load bite force tenderometry, collagen solubility and SDS page of myobribrillar proteins. 30
ACCEPTED MANUSCRIPT However, other authors found a significant decrease in shear force when treating beef in US baths at 25.9 kHz, 1000 W US bath, 2- 16 min (Smith et al., 1991) and 40 kHz, 1500 W, 1060 min (Chang et al., 2015). One theory for inconsistent results could be that samples are analysed too soon after treatment such that US may disrupt the microstructure, thereby affecting proteolysis and changing the texture over the ageing period. In a study which
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applied US (45 kHz, 2 W cm-2, 120 s) to beef SM and assessed the changes at various stages
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of post-mortem (24, 48, 72 and 96 h), microsctructural changes were evident in the 24 h post-
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mortem samples suggesting that sonication can accelerate the post-mortem process (Stadnik et al., 2008). The sonicated sample differed from the control such that there was swelling of
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the A-band and fragmentation of the z-lines (Stadnik et al., 2008). Such changes in the microstructure could be beneficial for tenderisation if applied to pre-rigor meat. This was an
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interesting approach as it demonstrated that the effect of US on meat may differ depending on the post-mortem time it is applied. Lyng et al. (1997) also applied US to beef at 24 or 72 h
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post-mortem stating that the aim of the 24 h treatment was to enhance early proteolytic
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activity, while at 72 h post-mortem, the myofibrillar proteins may be more susceptible to US disruption due to weakening by proteases. However, no positive effects of US on
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tenderisation were found (Lyng et al., 1997). The post-mortem time chosen for US application in a study depends on the initial hypotheses. However, the majority of authors
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standardise the application of US to meat at 24 h post-mortem (Sikes et al., 2014; Jayasooriya et al., 2007; Stadnik et al., 2008), as this ensures that the ultimate pH has been reached, thus reducing variability in tenderisation response.
6.3 Application to pre-rigor meat Considering that several studies suggest an effect of US on meat microstructure (Got et al., 1999; Stadnik et al., 2008) and enzyme activity (Xiong et al., 2012; Roncales et al., 1993), 31
ACCEPTED MANUSCRIPT there is certainly interest in applying the technology to pre-rigor meat and thus assess the effect of US on rigor-onset and the action of the proteases over the ageing time. In a study assessing the effect of US (2.6 MHz, 10 W cm-2, 30 s) on pre-rigor beef SM (day 0, pH 6.2), microstructural analysis revealed stretching of sarcomeres, z-line disruption and a slight delay in rigor onset, however, no effect the ageing rate or ultimate tenderness was observed (Got et
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al., 1999). Similarly, Sike et al. (2014) reported that high frequency US (2 MHz, 48 kPa
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acoustic pressure, 5 min) applied to beef sternomandiburlaris resulted in a tendency towards
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increased exhaustion factor (P = 0.073), suggesting increased glycolytic activity, but this was not evident in the final tenderness of the product. In two separate studies which applied high
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intensity low frequency US (20 kHz, 62 W cm-2, 15 s) to pre-rigor beef (Lyng et al., 1998a) and lamb (Lyng et al.,1998b), there was no effect on bite force tenderometry, sensory texture,
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collagen solubility or myofibrillar proteins assessed by SDS-PAGE. Although these studies found no ultimate improvement in meat tenderness the studies of Got et al. (1999) and Sike et
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al. (2014) indicate that frequencies above 2 MHz may cause ultrastructural changes in the
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meat matrix which warrants further research.
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6.4 High intensity US applied to post-rigor meat
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It has been suggested that US could be applied to manipulate proteolytic enzyme activity in order to increase tenderness (Xiong et al., 2012; Chang et al., 2012), in which case an assessment of meat tenderness during the ageing process following US treatment is of interest. However, as with all US studies, the experimental parameters must be optimised. For example, in a study assessing the effect of US (40 kHz, 1500 W, 10-60 min) on beef semitendinosus (ST) muscles, only 10 min of treatment significantly affected the activity of β- galactosidase and β-glucuronidase enzymes (Chang et al., 2012). Moreover, the level of enzyme in the sonicated samples was lower than the control which is undesirable given that 32
ACCEPTED MANUSCRIPT β-galactosidase and β-glucuronidase play a role in collagen degradation. Although other proteolytic enzymes are key to post-mortem tenderisation, the study of Chang et al. (2012) indicates that when US parameters are optimised, increased enzymatic activity may be evident. This warrants further research on the effect of US on the activity of other proteolytic enzymes such as calpains and cathepsins. However, it must be noted that cavitation may
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disrupt the cell membrane leading to release of enzymes from the cytosol early on in US
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treatment and that cavitation itself may damage enzyme activity (Chang et al., 2012; Got et
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al., 1999).
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Although high intensity US (20 kHz, 56-62 W cm-2, up to 3 min) has been shown to increase protease activity in cell plasma in lamb liver, the increase in activity was not sustained and
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ultimately, there was no difference compared to conventional ageing (Roncales et al., 1993). Got et al. (1999) sonicated (2.6 MHz, 10 W cm-2, 15 s) post-rigor beef SM and reported that
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there was only an increase in tenderness at 6 days post-treatment with no final improvement
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after 14 days storage. It is concluded by the authors that the US treatment conditions used in this study are not sufficient to induce textural changes in meat. Likewise, in another study
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which applied relatively high frequency US treatment (600 kHz, 48 kPa and 65 kPa acoustic pressure, 10 min) to beef LTL muscles, no effect on tenderness over storage of 7 days was
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found (Sikes et al., 2014). The approach of Jayasooriya et al. (2007) was valuable in that a study was firstly conducted to assess the length of treatment time required to tenderise meat with the given apparatus and experimental set-up. It was found that when beef muscles (LTL and ST) were sonicated (24 kHz, 12 W cm-2) for up to 240 s, the WBS force decreased as a function of US treatment time. Certainly, in studies which applied shorter US treatment times (20 kHz, 63 W cm-2, 15 s) to beef, there were no tenderising effects (Lyng et al., 1998a; 1998b).
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6.5 Future Fundamental studies should be conducted to further elucidate the effect of US on meat (microstructure, enzyme activity, final tenderness) and to optimise process parameters (frequency, intensity, treatment time) for improved efficiency and penetration into the meat
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matrix. As both ultrasonics and meat science are complex, it is imperative that US studies
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report measurements of the acoustic field and details of the experimental set-up as this will
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reduce the difficulty in replicating experiments and allow the field of ultrasonics to evolve. This is especially important in the case of studies which assess the application of US for meat
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tenderisation as there is a high level of variability in the findings.
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7. SMARTSTRETCH™/SMARTSHAPE™ AND PIVAC® The development of methods such as ‘tenderstretch’, ‘tendercut’ (Sorheim & Hildrum, 2002)
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and ‘super stretch’ (Kim, Kerr, Geesink, & Warner, 2014; Warner, Kerr, Kim, & Geesink,
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2014) were to ‘stretch’ muscles and prevent toughening during rigor development. However, these methods were applied to the whole carcass, leading to stretching in only a selected
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number of muscles in the carcass during hanging. Recent developments of PiVac® (Sorheim & Hildrum, 2002) and Smartstretch™ (Taylor, Toohey, van de Ven, & Hopkins, 2012b;
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2013b; Toohey, Van de Ven, Thompson, Geesink, & Hopkins, 2012a; 2012b; 2012c) involve not only stretching, but also shaping. These technologies are applied to hot-boned muscle and have shown significant improvements in meat tenderness.
7.1 Mode of action It is well established the degree of muscle contraction which occurs during rigor mortis is correlated to tenderness of meat (Locker, 1960). Thus the application of stretching to muscle 34
ACCEPTED MANUSCRIPT is well-known to produce more tender meat, mainly through the pre-rigor prevention of muscle shortening. An excellent review of Smartstretch and PiVac is provided in Taylor and Hopkins (2011).
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7.2 PiVac®
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PiVac involves an initial wrapping technique which is applied via stretching of an extendable elastic sleeve by pressure inside a packaging chamber. Following insertion of muscles into
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the packaging chamber, the pressure is released, which results in the elastic sleeve preventing
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muscle contraction through restriction in expansion in the diameter of the cut. PiVac® applied to hot-boned beef muscles chilled at different temperatures showed an increase in
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sarcomere length (Hildrum, Andersen, Nilsen, & Wahlgren, 2000; O'Sullivan, Korzeniowska, White, & Troy, 2003) and allowed rapid chilling of hot-boned M. longissimus without
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compromising tenderness (Hildrum, Nilsen, & Wahlgren, 2002). Moreover, when PiVac®
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was compared to low-voltage and high-voltage electrical stimulation of hot-boned beef M. longissimus, the PSF value was lower for PiVac® (45 N) compared to other treatments (~90
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N) following 14 days of ageing and this was also confirmed by a trained sensory panel
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(O’Sullivan et al., 2003). 7.3 Smartstretch™
Recent developments of Smartstretch™ combine both stretching and shaping and are applied to meat removed from the carcass. Unlike tenderstretch and tendercut, in which some muscles are restricted from stretching in intact carcasses, these new technologies are applied to hot-boned muscle and have been shown to significantly improve meat tenderness. Similar to PiVac®, a more recent stretching and shaping technique named Smartstretch™ was
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ACCEPTED MANUSCRIPT developed and patented (SmartstretchTM/SmartshapeTM) to increase tenderness of hot-boned meat cuts (Pitt & Daly, 2010). Smartstretch™ employs a flexible sleeve placed in an airtight chamber and when meat inserted into the flexible sleeve is compressed, it prevents any expansion in the diameter of the product by forces perpendicular to muscle fibres. Pre-rigor beef longissimus lumborum and gluteus medius showed a reduction of 12-14 N in PSF with
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the application of SmartstretchTM treatment and the application to sheep semimembranosus
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caused significant tenderisation with a reduction in PSF of 22-49 N (Taylor et al., 2012b;
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2013b; Toohey et al., 2012a; 2012b; 2012c). Interestingly, SmartstretchTM treatment of both beef and sheep meat resulted in juicier non-aged meat cuts (Toohey et al., 2012a; 2012c) and
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stretching has been shown to increase the water-holding capacity of meat (Warner, Kerr, et al., 2014). These results demonstrate potential improvement of eating qualities of hot-boned
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primals by SmartstretchTM in accelerated meat production.
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7.4 Combining stretching with other technologies Application of PiVac® and Smartstretch™ treatments to hot-boned primals offers advantages
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over whole carcass stretching such as a reduction in chiller space and energy requirements, accelerating meat processing and increasing control over serving portion size and shape
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control for consumers.
Increasingly, research into improving eating quality of meat is
exploring the combinatory effect of more than one tenderising method. Several studies have investigated the potential of a combination of electrical stimulation and ageing coupled with muscle tenderstretching and PiVac® and reported mixed results on different meat cuts (Sørheim and Hildrum 2002; Troy 2006). More recently, a study of Toohey et al. (2013a) showed that medium voltage electrical stimulation neither improved nor inhibited the tenderising effect of SmartstretchTM in sheep M. semimembranosus. It is noteworthy that the
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ACCEPTED MANUSCRIPT degree of muscle contraction varies with muscle types (Locker 1960), reflecting underlying differences in glycolysis, temperature and pH of meat at the time of rigor. It is therefore important for research on meat stretching and shaping to be performed in targeted primals in
7.5 Future
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The number of studies on meat qualities following application
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order to ensure consistent end-results in commercial settings.
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of PiVac® and SmartstretchTM are limited compared to other technologies. Even more limited are fundamental studies examining molecular changes in meat under stretching and
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shaping. Variations in sarcomere length, in PSF and thus in the level of tenderisation between different muscles in response to SmartstretchTM (Toohey et al., 2012b) are not well
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understood. Adoption of SmartstretchTM and PiVac® in commercial settings has been limited for various reasons, including a relatively small number of hot boning plants, cost
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in integrating SmartstretchTM and PiVac® machines into existing production
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chains and training of operating staff, and inconsistent tenderness of primals that vary in size. Other challenges of SmartstretchTM and PiVac® prototype machines are their speed of
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operation and the labour intensiveness required for their operation (Sorheim & Hildrum, 2002). Thus further investigation to address these issues is warranted
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for successful implementation of these technologies.
8. COMPARISON OF TENDERISATION BETWEEN VARIOUS TECHNOLOGIES
It is quite difficult to compare the tenderisation outcome from a technology, across studies, when the conditions of applying a technology for meat tenderisation include different species,
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ACCEPTED MANUSCRIPT different muscles, varying time applied post-mortem and widely varying conditions of application. Therefore, a meta-analytical approach was used to unify the published literature.
8.1 Meta-analysis of the effects of technologies on peak shear force (PSF)
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Meta-analysis is an appropriate statistical methodology to use where sufficient data is available from different studies. Thus data was collected from a number of studies for all the
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aforementioned technologies, namely PEF, HPP, SW, PEF, US and tenderstretch/Pivac.
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Studies were only included where there was PSF data, sufficient detail was given in terms of variation (SE, SED or SD), muscles, number of animals and samples were provided and an
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appropriate control was included. The change in PSF in response to the application of a
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technology was then expressed relative to the control and the variation was standardised to a standard error. A summary of the analysis follows and greater detail will be provided in a paper by Warner and the other co-authors on this paper (yet to be published) but the approach
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was very similar to that utilised by Lean et al. (2014). Table 3 shows the number of studies included as well as the number of treatments/tests within each study, the species and muscles included and the source references. In the case of data where there was distinct groupings of
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treatment, and sufficient data was available for each grouping, the data were initially
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analysed across all the studies, and was then partitioned into the separate sub-groupings. Thus, PEF was separated into the application to pre- or post- rigor meat and shockwave was separated into electrical and explosive. In the case of HPP, sufficient data was available to analyse the effect of species, as well as pre- vs post-rigor. In addition, the conditions of HPP widely varied in pressure and temperature and there was insufficient data available for pork or poultry to analyse the combined effects. In the case of beef and lamb, sufficient data was available to analyse the combined effects of pressure and temperature and these data are presented below. 38
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All the technologies investigated had significant and positive effects on tenderness, as measured by the change in PSF from the control (Tables 4 and 5 and Figures 4, 5 and 6). Overall, PEF resulted in a reduction in PSF of 4.4 N (data not shown), but when split into two groups of pre- and post-rigor application, there was no effect of pre-rigor application of PEF
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(P>0.05) whereas the application of PEF to post-rigor meat resulted in a reduction of 7.1 N
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(P<0.05) in PSF. In the case of the technology shock-wave, the only technology which is
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approved for use commercially is electrical shockwave, and overall the reduction in PSF across all studies was 7.5 N. This compares to a much larger reduction in PSF with explosive
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shockwave of 17.7 N. The reduction in PSF with ultrasound was 6.0 N and was similar to that achieved with PEF applied to pre-rigor meat and electrical SW. Excluding HPP,
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Smartstretch applied to pre-rigor meat achieved the greatest improvement in tenderness of 10.8 N. Overall, HPP applied to meat resulted in the largest reduction in PSF, of 43.5 N.
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Further analysis was conducted of the HPP data and this showed an effect of species
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(P<0.001) and also time of application (P<0.001). The greatest effect of HPP on shear force was on beef and sheep meat followed by pork and chicken (predicted change in PSF; 29.7,
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14.0, 9.9, 8.5 N respectively) (Figure 5). Pre-rigor meat showed a much greater decrease in shear force in response to HPP, relative to post-rigor meat (predicted change in PSF; 26.3, 4.7
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N respectively) (Figure 5). Further meta-analysis of the effect of different high pressure and temperature combinations applied to beef and sheepmeat showed an interaction between pressure and temperature (P<0.001) (Table 5 and Figure 6). The greatest positive change in PSF was observed at low pressures (100-150 MPa) combined with intermediate (35-45 oC), high (50-60 oC) and very high (68-80 oC) temperatures. Intermediate pressures (200-400 MPa) had only small positive effects on PSF. High pressures (520-600 MPa) generally had little effect on PSF except at low (10-30 oC) temperatures there was a clear toughening effect.
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It is worth noting that PEF, US, non-thermal HPP and SW are applied at ambient temperature and are called ‘non-thermal’ as they have an effect on the microbial load at ambient or sub thermal temperatures (Cullen, Tiwari, & Valdramidis, 2011). However, these technologies generate heat and can increase the temperature, by up to 30oC, of treated samples, under
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certain conditions (see Table 2). In addition, Smart-stretch/PiVac are applied to ‘hot’ pre-
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rigor muscles (30-40oC). Thus generation of heat during technology application (see Table 2)
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or warm muscle conditions during application to pre-rigor meat means that phase 1 of the three heating stages associated with changes in texture and water loss mentioned in section
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2.3, are of relevance. Where the application of thermal high pressure processing is concerned,
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all three phases are relevant.
It should be noted that it is well-known that different muscles in the carcass vary widely in
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their tenderness, depending on anatomical location and function which relates to sarcomere
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length, collagen content and cross-linking and protease content and post-mortem activity. For example, amongst eleven major muscles in the beef carcass, the sensory and PSF
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tenderness ranges from very tender in the psoas major (sensory tenderness =7.4 out of 10 points; PSF = 28.9 N) to tough in the supraspinatus (sensory tenderness = 4.1 out of 10
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points; PSF = 48.5 N; Rhee et al., 2004). Thus although many studies included the longissmus and for chicken and turkey only the pectoralis major was tested, other studies included a range of muscles (Table 3). 8.2 Comparison of the effects of growth promoting technologies on meat texture Previously, a meta-analysis was conducted to determine the effects of metabolic modifiers on the tenderness of beef meat. From a meta-analysis of 22 studies, hormonal growth promotants (HGP’s) significantly increased the PSF (toughness) of beef longissimus by 2.6 N 40
ACCEPTED MANUSCRIPT (Watson, 2008). Thus, in the MSA model for predicting eating quality, the meat from HGPtreated cattle has a 5-point reduction in the consumer- derived meat quality score (MQ4) applied, to adjust for this effect. Since some of the processing effects and animal effects on meat quality are additive, HGP-treated meat has to be aged for longer to reach the same degree of tenderisation as meat from untreated cattle. Meta-analysis of data has shown that
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the application of the beta-agonists zilpaterol and ractopamine to cattle causes increased PSF
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of beef longissimus by 8.2 and 2.0 N, respectively (across 47 and 17 studies respectively)
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(Lean & Dunshea, 2014). If ractopamine and zilpaterol were to be registered for use in Australia, reductions in the predicted MQ4 score would need to be included in the MSA
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model for predicting eating quality. In other markets, the benefits in efficiencies and carcass yield from along the value chain from using HGP’s and beta-agonists will need to be offset
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against any negative effects on consumer perceptions of eating quality. Figure 4 shows metaanalysis results comparing changes in PSF in response to application of metabolic modifiers
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(HGP, ractopamine, zilpaterol) to beef cattle. It is evident that the technologies applied post-
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slaughter generally increase the PSF by at least 6-7 N, whereas the application of HGP’s and of zilpaterol only result in a reduction in PSF of 2-2.6 N, ractopamine causing a reduction in
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PSF of 8.4N. This suggests that the application and optimisation of post-slaughter
modifiers.
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technologies would likely overcome any toughness induced by the use of metabolic
Other animal factors known to increase red meat toughness include the callipyge gene in sheep (Cockett et al., 1993; Duckett, Snowder, & Cockett, 2000), the Carwell sire in sheep (Jopson et al., 2001; Nichol et al., 1998) and a toughness gene prevalent in bos indicus cattle (Cafe et al., 2010; Cafe et al., 2011), to name a few. Previously, electrical stimulation has been found to have little to no effect on the tenderness of the leg, forequarter and loin
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ACCEPTED MANUSCRIPT muscles of callipyge sheep (Kerth, Cain, Jackson, Ramsey, & Miller, 1999; Solomon, Carpenter, Snowder, & Cockett, 1998) although detonation/explosive shockwaves resulted in significant tenderisation of callipyge loin muscles (Solomon et al., 1998). The modern production of lean beef, sheep, pork and poultry carcasses has been achieved through the use of genetics in combination with nutrition and metabolic modifiers and this has generally
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resulted in reductions in eating quality (Dunshea et al., 2016). The opportunity is to
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processing technologies, such as those described above.
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overcome some of the reduction in eating quality through the application of post-mortem
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8.3 Possible combinations of technologies
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Exogenous proteases have been shown to be capable of hydrolysing meat proteins, thus facilitating tenderization of meat and has recently been comprehensively reviewed by Bekhit, Hopkins, Geesink, Bekhit, and Franks (2014a). The proteases can be extracted or generated
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from plant, marine, fungal or microbial sources and each protease shows varying levels of proteolytic acitivty against collagen and myofibrillar proteins. Actinidin is an extract from kiwifruit showing particular promise as it exhibits a more controlled tenderization action
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through hydrolysis of myofibril proteins, which may offer an advantage in reducing the
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mushy texture and off flavour observed in meat treated with other proteases. It is likely there will be developments in new proteases for meat tenderisation and they show potential for being combined with some of the technologies discussed above.
Certainly, there is scope for further research on the interactions and possible synergistic effects of emerging technologies combined with enzymes for meat tenderisation, particularly to add value to high connective tissue muscles. An understanding of the mechanisms of how each technology induces tenderisation assists in determining the ideal combination of 42
ACCEPTED MANUSCRIPT technologies for a particular cut of meat or market. For example, the target for low connective tissue muscles, destined for a local market, might be accelerating the proteolytic process in order to reduce the ageing period required. All of the technologies discussed above show some promise for delivering accelerated tenderisation as each has been shown to have some effect on proteolysis or muscle structure. In contrast, high connective tissue
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muscles are more likely to require an intervention technology which influences collagen as
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well as myofibrillar structure. When high pressure processing is applied at high
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temperatures, there appears to be some changes to connective tissue with may contribute to the positive outcomes for texture. Exogenous enzyme added to meat cuts also cause
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degradation in collagen and connective tissue. Thus high temperature-HPP, or exogenous enzymes, applied alone or in combination, are possible solutions for delivering accelerated
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tenderisation in high connective tissue cuts, thus warranting further investigation.
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9. SUMMARY
High pressure processing, shockwave processing, ultrasound, pulsed electric field and
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SmartstretchTM/PiVacTM can be used to increase the tenderness, predominantly through physical disruption to muscle structure, enhanced proteolysis and ageing and muscle protein
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denaturation and solubilisation depending on the technology.
A number of studies have been conducted on the ideal conditions for tenderisation from the application of high pressure processing. The meta-analysis on the available studies shows the ideal conditions are 20-150 MPa and ≥ 35 oC. Subjecting meat to high pressures (520-600 MPa), can result in toughening, particularly when applied at low or ambient temperatures. Meat subjected to HPP pre-rigor shows double the amount of tenderisation relative to the application of HPP to post-rigor meat, although it is recognised pre-rigor application of HPP 43
ACCEPTED MANUSCRIPT is logistically more difficult. There are species differences in the tenderisation response to HPP with the order of tenderisation response to HPP being beef > sheep meat > pork=poultry and beef showing double the tenderisation response relative to sheep meat. Likely the differences between species are due to variation in the initial tenderness, and rate of tenderisation, with beef generally being tougher, and requiring a longer ageing period relative
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to meat from the other species.
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The research on generating shockwaves using explosives has shown significant tenderisation outcomes. The application of shockwaves using electricity and of PEF, for meat
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tenderisation, are only very recent. Using the data on PSF from the available studies in the literature, as well as some unpublished data, showed that the application of electrical
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shockwaves, PEF and ultrasound to cold-boned meat produced a similar reduction in PSF of 6-7 N. Across all available studies, the application of smartstretch and high pressure
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processing, but not PEF, resulted in significant tenderisation when applied to pre-rigor meat.
There is potential for tenderisation technologies to be used to ameliorate the toughness in
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meat resulting from genetic and production practices. Furthermore the application of tenderisation technologies to pre- and post-rigor muscles, including muscles traditionally
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considered to be quite tough, should deliver real benefits to an industry that prides itself on quality, and is also often for quality. The optimum application of these new and innovative technologies for tenderisation will need to be adjusted for different muscles in the carcass, different markets (food service, fresh product, export markets) and also target demographics.
Previous research shows that in some countries, the consumer will be willing to pay for assured tenderness. This will likely drive the interest in, and adoption of, these emerging
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ACCEPTED MANUSCRIPT technologies for tenderisation. The implementation of these technologies in industry will be dependent on operators willingness to innovate, the capital and operating cost of the technologies and the cost-benefit.
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10. Acknowledgements Funding provided by Meat and Livestock Australia in project V.RMH.0044 is gratefully
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PT
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D
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CE
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ACCEPTED MANUSCRIPT Suwandy, V., Carne, A., van de Ven, R., Bekhit, A. E.-D. A., & Hopkins, D. L. (2015c). Effect of pulsed electric field treatment on the eating and keeping qualities of coldboned beef loins: impact of initial pH and fibre orientation. Food and Bioprocess Technology, 8(6), 1355-1365. Suwandy, V., Carne, A., van de Ven, R., Bekhit, A. E.-D. A., & Hopkins, D. L. (2015d).
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ACCEPTED MANUSCRIPT Table 1: Description of changes in texture, shrinkage in muscle fibre and water loss over three temperature ranges being up to 62 oC (phase 1), 50-65 oC (phase 2, transition) and above 60 oC (phase 3).
Phase 2 – Transition between phase 1 and 3- 50-65 oC 50-65 oC 1, 2;
Toughening; 44 to 72
Tenderisation; 72 to
N1
55N1
35-55 oC; 20 to 49 N9
55-65 oC; 69-118 N9
Shrinkage in
Transverse; 35- 62 oC4
muscle fibre,
40-60 oC; 3-16%10
D
direction and
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volume (%)
60-80 oC 1, 2, 3
NU
SC
RI
40-53 oC 1, 2, 3
MA
Texture
Phase 3 – Above 60 oC
PT
Phase 1- up to 62 oC
Toughening; 55 to 90N1
70-80 oC; 137-157 N9 Longitudinal; 65- 90oC4
65 oC; 20%10
70-95 oC; 28-46%10
50-56 oC; 22-28%5
58-62 oC; 34-35%5
64-70 oC – 38-41%5
during heating
40-55 oC; 2-5%6
60 oC; 9%6
70-80 oC; 16-33%6
45-55 oC; 5-10%7
65 oC; 18-23%7
75-85 oC; 23-35%7
55-60 oC; 15-20%8
65 oC; 24%8
75-105 oC; 30-43%8
65 oC; 20%10
70-95 oC; 28-44%10
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Water loss (%)
40-60 oC; 3-16%10
1
(Christensen, Purslow, & Larsen, 2000); 2 (Davey & Gilbert, 1974); 3 (Martens, Stabursvik,
& Martens, 1982); 4 (Bendall & Restall, 1983; Hearne, Penfield, & Goertz, 1978; Hostetler & Landmann, 1968; Palka & Daun, 1999; Purslow et al., 2016; Tornberg, 2005); 5 (Berhe, Engelsen, Hviid, & Lametsch, 2014); 6 (Tornberg, 2005); 7 (Martens et al., 1982); 8 (Purslow
71
ACCEPTED MANUSCRIPT et al., 2016); 9 (Bouton, Harris, & Ratcliff, 1981); 10 Bouton et al 1976 (Bouton, Harris, &
AC
CE
PT E
D
MA
NU
SC
RI
PT
Shorthose, 1976)
72
ACCEPTED MANUSCRIPT
Table 2: Description of the technologies high pressure processing, hydrodynamic shock wave, pulsed electric field, ultrasound, stretching including tenderstretch, smartstretch and PiVac, including first patent claiming tenderisation, first trial on meat, and the associated increase in
T P
I R
temperature of the product during application of the technology.
Description
tenderisation
High pressure processing,
100-600 MPa,
(McKenna, 2009)
Hydrostatic
High
wave)
D E
PT
E C
pressure, Detonation,
hydrodynamic
C S U
First Patent claiming First trial on meat for Increase
(Long, 1993)
C A
(shock electrically generated
M
temperature
during
application to meat (oC)*
N A
tenderisation
in
(Macfarlane, 1973)
3oC /100 MPa from adiabatic heating (US food and Drug Administration, 2014)
(Solomon, Long, & Detonation; 2-3oC* Eastridge, 1997b)
(Solomon, Sharma, & Patel, 2010) Electrical; negligible (Jim Claus, unpublished results).
Pulsed electric field
Electric pulses
(Long, 2000)
(O'Dowd
et
al., 5-30oC*
73
ACCEPTED MANUSCRIPT 2013) Ultrasound
Low
(O'Dowd et al., 2013)
high (Guberman & Holt, (Dickens, Lyon, & 15-30oC*
or
frequency
1970)
(Jayasooriya, Torley, D’Arcy, et al.,
Wilson, 1991)
T P
2007) Tenderstretch
Stretch
pre-rigor (Stouffer, Buege, & (Hostetle.Rl,
muscles
on
the Gillis, 1971)
Smartstretch
Stretch
Fitzhugh, 1970) hot-boned (Pitt & Daly, 2010)
pre-rigor muscles PiVac
C S U
Landmann, Link, &
carcass
I R
negligible
Stretch
N A
(Simmons
et
al., negligible
2006)
D E
hot-boned (Meixner,
pre-rigor muscles
2004)
T P E
M
2001, (Sorheim & Hildrum, negligible 2002)
C C
*
Temperature rise depends on experimental parameters and conditions of application
A
Table 3: Summary of studies, total number of individual results tests within studies, species and muscles tested and source references. Where the pectoralis major muscle is specified, this refers to chicken or turkey only. This muscle was not included in any studies on pork, beef or sheep meat. Hence any effects of technologies on chicken or turkey meat refer specifically to the pectoralis major.
74
ACCEPTED MANUSCRIPT
Technology No. of – description of studie samples s included PEF – Pre-rigor
4
No. of resu lts within studies 114
Species
Muscles
References
Beef; Turkey
pectoralis major; longissimus; semimembranosus
Arroyo, Eslami, et al. (2015); (Arroyo, Lascorz, et al., 2015); Bekhit, Suwandy, Carne, van de Ven, and Hopkins (2016b); Suwandy, Carne, van de Ven, Bekhit, and Hopkins (2015b); Suwandy, Carne, van de Ven, Bekhit, and Hopkins (2015d) Arroyo, Eslami, et al. (2015); Bekhit, van de Ven, et al. (2014b); Bekhit et al. (2016b); Faridnia, Bekhit, Niven, and Oey (2014); Faridnia et al. (2015); Suwandy et al. (2015b); Suwandy, Carne, van de Ven, Bekhit, and Hopkins (2015a); Suwandy et al. (2015d) Bolumar, Bindrich, Toepfl, Toldra, and Heinz (2014); Bowker, Schaefer, Grapperhaus, and Solomon (2011); Claus et al. (2001b); James Claus (unpublished data)
PEF – Post-rigor
8
146
Beef
longissimus; semitendinosus; semimembranosus
Shock wave – Electrical
4
4
Shock wave Explosive
17
64
Beef; Turkey and Chicken; Pork Beef; Pork; Turkey and Chicken; Sheepmeat
Longissimus; pectoralis major; semitendinosus; semimembranosus; gluteus medius; adductor longissimus; adductor; pectoralis major; biceps femoris; semitendinosus; semimembranosus
D E
T P
I R
C S U
M
T P E
C C
A SmartStretch
6
12
Beef; Sheepmeat
N A
longissimus; gluteus medius; semimembranosus
Bowker, Callahan, and Solomon (2010); Bowker, Fahrenholz, Paroczay, Eastridge, and Solomon (2008); Bowker, Liu, et al. (2010); Callahan, Berry, Solomon, and Liu (2006); Claus et al. (2001a); Liu et al. (2006); Marriott, Wang, Solomon, and Moody (2001); Meek et al. (2000); Moeller et al. (1999); Schilling et al. (2002); Schilling, Marriott, Wang, and Solomon (2003); Solomon et al. (2008); Solomon, Long, and Eastridge (1997a); Spanier, Berry, and Solomon (2000); Zuckerman, Berry, Eastridge, and Solomon (2002); Zuckerman, Bowker, Eastridge, and Solomon (2013); Zuckerman and Solomon (1998) Taylor, Toohey, van de Ven, and Hopkins (2012a, 2013a); Toohey et al. (2012a); Toohey, van de Ven, Thompson, Geesink, and Hopkins (2012c, 2012b, 2013)
75
ACCEPTED MANUSCRIPT Technology No. of – description of studie samples s included Ultrasound
HPP – Pre-rigor
HPP – Post-rigor
6
5
18
No. of resu lts within studies 55
30
186
Species
Muscles
References
Beef; Sheepmeat; Chicken
longissimus lumborum; semitendinosus; semimembranosus; sternomandibularis; pectoralis major semitendinosus; psoas major; pectoralis minor; longissimus lumborum; biceps femoris; adductor; semimembranosus; glutius medius; triceps brachii longissimus lumborum; biceps femoris; semitendinosus; semimembranosus; pectoralis major; pectoralis profundus; psoas major; adductor; gluteus medius
Jayasooriya, Torley, D'Arcy, and Bhandari (2007); Lyng, Allen, and McKenna (1998b); Pohlman, Dikeman, and Zayas (1997); Pohlman, Dikeman, Zayas, and Unruh (1997); Sikes, Mawson, Stark, and Warner (2014); Stadnik and Dolatowski (2011); (Xiong, Zhang, Zhang, & Wu, 2012) Bouton, Ford, Harris, Macfarlane, and Oshea (1977); Bouton, Harris, and Macfarlane (1980); Bouton, Harris, Macfarlane, and O'shea (1977b); Macfarlane (1973); Souza et al. (2011)
Beef; Sheepmeat; Pork
Beef; Sheepmeat; Pork; poultry
A
C C
T P E
D E
T P
I R
C S U
M
N A
Beilken, Macfarlane, and Jones (1990); Bouton, Ford, Harris, Macfarlane, and Oshea (1977); Bouton et al. (1980); Bouton, Harris, et al. (1977b); (Del Olmo, Morales, Avila, Calzada, & Nunez, 2010); Duranton, Simonin, Cheret, Guillou, and de Lamballerie (2012); Hong, Shim, Choi, and Min (2008); Jung, De Lamballerie-Anton, and Ghoul (2000c); Jung, Ghoul, and de Lamballerie-Anton (2000a); Ma and Ledward (2004); Macfarlane (1973); Macfarlane and Mckenzie (1986); Macfarlane, Mckenzie, and Turner (1986); Macfarlane, Mckenzie, Turner, and Jones (1981); McArdle, Marcos, Kerry, and Mullen (2011); McArdle et al. (2013); Park, Ryu, Hong, and Min (2006); Ratcliff et al. (1977); Sikes and Tume (2014).
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ACCEPTED MANUSCRIPT Table 4: Results of meta-analysis of the effect of technologies on the change in objective meat tenderness measurement, defined as peak shear force (N). The meat was variously from beef, sheep, pork and poultry and a range of muscles (see text and Table 3). The technologies included are pulsed electric field (PEF; applied to pre-rigor or post-rigor meat), shockwave (applied to post-rigor meat; electrical or explosive), SmartstretchTM (applied to pre-rigor
PT
meat), ultrasound (applied to pre-rigor meat) and high pressure processing (HPP; applied to
RI
pre-rigor or post-rigor meat). The ‘Effect’ is the effect of application of a technology on the
SC
peak shear force (N) relative to untreated meat. The SED is the standard error of the
NU
difference in PSF across all studies.
SED
MA
Effect
PEF Pre-rigor
0.52ns
-
Post-rigor
7.10***
interval
-0.76, 1.88
1.110
4.88, 9.28
0.444
6.67, 8.41
17.71***
2.145
12.91, 22.57
10.76***
3.537
3.203, 18.31
6.03***
1.388
3.246, 8.80
- Pre-rigor
82.30***
10.759
60.64, 104.14
- Post-rigor1
36.82***
4.306
28.33, 45.31
Shockwave Electrical
-
Explosive
Ultrasound
AC
SmartstretchTM
7.54***
CE
-
D
0.630
PT E
-
95% confidence
HPP
1
Treatments tested were across the range of pressures (HPP) 20-600 MPa and across the
temperatures 10-80 oC
77
ACCEPTED MANUSCRIPT *** P<0.001; ns not significant, P>0.05.
Table 5: Results of meta-analysis of the predicted change in peak shear force (N) as a result of the application of high pressure processing, relative to untreated controls. The data was grouped into three pressure ranges (Low, 20-150 MPa; Medium, 200-400 MPa; High, 520-
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600 MPa) and four temperature ranges (low, 10-30 oC; intermediate, 35-45 oC; high 50-60 oC;
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very high, 68-80 oC). Pressure, P<0.001; Temperature, :P<0.001, Pressure x Temperature,
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P<0.001. Average SED = 2.051.
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Temperature Ranges (oC)
35-45
50-60
68-80
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57.81
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10-30 Pressure Range (MPa) -5.61
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ACCEPTED MANUSCRIPT LIST OF FIGURES – Please note, two new figures have been inserted into the revised manuscript. These new figures are figures 2 and 3 below. Figure 1: Effect of heating bovine cold-shortened semitendinosus muscle blocks, for one hour in a water bath at temperatures 40, 50, 55, 60, 65, 70, 80, 90, 95 oC (±0.5 oC), on cook loss
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(%; LSD=1.6), length decrease (%; LSD=2.1), area decrease (%; LSD=4.4), volume decrease
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(%;LSD=2.4) and peak shear force (kg; LSD=0.86). Adapted from (Bouton et al., 1976).
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Figure 2: (A) Relationship between peak shear force (kg) and sensory tenderness scores in bovine longissimus thoracis et lumborum, predicted from peak shear force in 1-day aged (■)
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and peak shear force in 14-day aged (♦) meat. From Perry et al. (2001). (B) Relationship between peak shear force values (kg) and sensory tenderness ratings of bovine longissimus
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steaks by consumers at home and at a restaurant. No consumers at home gave a 1 rating. a,b,c,d Means in a dining environment with different superscripts are different (P < .05). From
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Huffman et al. (1996).
Figure 3: Example of a pressure-phase diagram, showing a suggested extended phase
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diagram for the protein myoglobin. The diagram includes both the denaturation and aggregation phenomena, and therefore contains several metastable phases. The metastable
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phases are indicated in parentheses. N, native; D, denatured; A, aggregated; I, intermediate. From Smeller (2002).
Figure 4: Results of meta-analyses of the predicted change in peak shear force (N) in response to applications of ractopamine, zilpaterol and hormonal growth promotants (HGP) to beef cattle and the post-mortem application to various species (beef, sheepmeat, pork and poultry),to pre-rigor meat of smartstretch (Smartstetch), and to post-rigor meat of pulsed electric field (PEF-post-rigor), electrical shock wave (SW-electrical), ultrasound and to both 79
ACCEPTED MANUSCRIPT pre- and post-rigor meat of HPP (see Table 3, 4 and5 for sources, data and SED’s). The mean effect is shown and the vertical bar is the least significant difference (2 x SED).
Figure 5: Meta-analyses of the change in Warner-Bratzler peak shear force (N) of meat in response to applications of high pressure processing to different species (Species; beef,
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chicken, lamb and poultry) and different times post-mortem (pre-rigor vs post-rigor) (see
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Table 3, 4 and 5 for sources, data and SED’s). Species, P<0.001, average SED = 1.045; Time
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post-mortem, P<0.001, average SED=0.6413. The mean effect is shown and the vertical bar
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is the least significant difference (2 x SED).
Figure 6: The predicted change in peak shear force (N), relative to untreated controls, as a
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result of the application of high pressure processing. The data was grouped into three pressure ranges (Low, 20-150 MPa; Medium, 200-400 MPa; High, 520-600 MPa) and four
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temperature ranges (low, 10-30 oC; Intermediate, 35-45 oC; high 50-60 oC; very high, 68-80
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Average SED = 2.051.
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oC). Pressure, P<0.001; Temperature, :P<0.0001, Pressure x Temperature, P<0.001.
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R.D. Warner, C. McDonnell, A.E.D. Bekhit, J. Claus, R. Vaskoska, A. Sikes, F.R. Dunshea, M. Ha PII: DOI: Reference:
S0309-1740(17)30169-9 doi: 10.1016/j.meatsci.2017.04.241 MESC 7264
To appear in:
Meat Science
Received date: Revised date: Accepted date:
10 February 2017 19 April 2017 28 April 2017
Please cite this article as: R.D. Warner, C. McDonnell, A.E.D. Bekhit, J. Claus, R. Vaskoska, A. Sikes, F.R. Dunshea, M. Ha , Systematic review of emerging and innovative technologies for meat tenderisation, Meat Science (2017), doi: 10.1016/ j.meatsci.2017.04.241
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Systematic review of emerging and innovative technologies for meat tenderisation R.D. Warnera*, C. McDonnellb, A.E.D Bekhitc, J. Clausd, R. Vaskoskaa, A. Sikes,e F.R. Dunsheaa, M. Haa a
Faculty of Veterinary and Agricultural Science, University of Melbourne, Parkville,
Food Quality and Sensory Science Department, Teagasc Food Research Centre, Ashtown,
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b
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Victoria, 3010, Australia.
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Dublin 15, Ireland.
Department of Food Science, University of Otago, Dunedin, 9054, New Zealand.
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Department of Animal Sciences, University of Wisconsin, 5306, USA.
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CSIRO Food and Nutrition, 39 Kessels Road, Coopers Plains, Queensland 4108, Australia.
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c
*
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Corresponding author: [email protected]
Keywords: pulsed electric field; high pressure processing; tenderness, texture; meta-analysis;
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ultrasound; shock wave; shockwave; smartstretch
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ACCEPTED MANUSCRIPT List of acronyms PSF = peak shear force. Note: wherever possible, the units used are Newtons, but some authors give peak shear force in kg. PSF (N) = PSF (kg) x 9.8. Where possible, we have converted the units to Newtons.
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PEF = pulsed electric field
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SW = shockwave
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HPP = high pressure processing
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US = ultrasound
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ACCEPTED MANUSCRIPT ABSTRACT Consumers are the final step in the meat supply chain and meeting consumer expectations of quality and tenderness are important for satisfaction and repeat purchase. High pressure processing, shockwaves, ultrasound, pulsed electric field and muscle stretching can be applied to pre- and post-rigor meat for tenderisation. These non-thermal and thermal
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innovative technologies can be used with varying levels of success to cause physical
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disruption to muscle structure, enhanced proteolysis and ageing and muscle protein
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denaturation and solubilisation resulting in changes to texture and juiciness. Results of a meta-analysis are used to compare the effects of these technologies on meat tenderisation. In
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a range of desired textures for meat products.
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the future, a combination of new and innovative technologies will be ideally suited to deliver
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1. INTRODUCTION
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Consumers are the final step in the meat supply chain and meeting their expectations is an important part of their satisfaction (Font-I-Furnois & Guerrero, 2014) and therefore long-term viability of the meat industry.
Consumer experience, perception and in-mouth sensory
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appreciation of meat derives from the traits ‘texture, juiciness and flavour’ and these
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characteristics are highly related to the overall experience of quality, intention to purchase, repeat purchase and willingness to pay (Font-I-Furnois & Guerrero, 2014; Lyford et al., 2010). In some countries with established quality assurance systems, the producer, processor and retailer are paid more for assuring quality and tenderness, an example being the Meat Standards Australia grading system for beef (Acil Allen Consulting, 2016).
Meat quality traits, particularly tenderness, depend on intrinsic and extrinsic factors. These factors include (i) pre-slaughter factors such as species, genotype, nutrition and age of the
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ACCEPTED MANUSCRIPT animal (many of which affect fatness and weight of the carcass), pre-slaughter stress and (ii) post-slaughter factors such as electrical stimulation and hanging of the carcass, ageing of the meat and packaging and conditions during storage and excellent reviews are available on these topics (Young, Hopkins, & Pethick, 2005; Purchas, 2007; Channon, D’Souza, Dunshea, 2016a; Channon, Hamilton, D’Souza, & Dunshea, 2016b; Hocquette et al., 2014; McMillin,
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2008; Strydom & Rosenvold, 2014; Thompson et al., 2006). Traditionally, meat tenderness is
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improved post-mortem through ageing of meat allowing proteolysis to proceed in an
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anaerobic environment, electrical stimulation of red meat carcasses in order to prevent coldshortening, application of stretching techniques such as tenderstretch, and moisture infusion
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(Channon et al., 2016b). The application of each of these techniques has had varying success and application. Furthermore, the modern production of efficient, fast-growing, lean beef,
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lamb, pork and poultry carcasses has resulted in modifications which have generally resulted in a reduction in tenderness and eating quality (Dunshea, D’Souza, & Channon, 2016). One
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opportunity is to overcome the reduced tenderness through the application of novel and
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emerging post-mortem processing technologies. The other opportunity is to develop application of technologies that will accelerate tenderisation, enabling production of tender
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meat at 24 hrs post-mortem.
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New developments in technology have led to the emergence of thermal and non-thermal innovative processing methods for improved microbiological safety, reduced nutritional loss, increased efficiency and modified texture. By manipulating processing parameters, including temperature, atmosphere, time of application (pre- or post-rigor) and pressure, the structural changes of meat during processing are influenced, with a resulting impact on texture and tenderness (Bryony & Yang, 2012). Increases in temperature are associated with high temperature high pressure processing (HPP) (called adiabatic heating) and can also be generated during the application of technologies such as pulsed electric field (PEF), 4
ACCEPTED MANUSCRIPT ultrasound (US) and shockwave, thus a consideration of the effects of heating on muscle structure and proteins is required. The relevance and importance of any incident or applied thermal treatments in determining meat texture is included in the present analysis in order to understand the underlying mechanisms, including the contribution of muscle structure and proteins to the changes in texture with the application of innovative and emerging
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technologies. Note that HPP is not considered an emerging technology, as it was first applied
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to meat in the 1970’s (Mcfarlane, 1973) but the way it is presently being developed and used
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is novel. This paper examines some technologies that can be applied to improve meat
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tenderness and are being investigated for adoption by the meat processing industry.
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2. OVERVIEW OF THE INFLUENCING FACTORS FOR MEAT TENDERNESS
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Tenderness is a multi-parameter sensory attribute and together with juiciness of meat, defines
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a large part of the mouth-feel (Lawless and Heymann, 2010), with texture, juiciness, and flavor together forming the consumers' perception of "overall quality." Meat, and in fact any food, is processed in the mouth (Chen and Engelen, 2012) and the sensory/thermo-
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mechanical material properties are significant for the "mouth-feel" and the taste and release Thus although this review focuses on technologies for
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of aroma, fat, and moisture.
"tenderization," the implicit effects of tenderness on the consumers' perception of overall quality, being both flavor, juiciness, and tenderness, are also important.
A brief overview of meat tenderness, muscle biochemical changes post-mortem, changes in muscle during heating, methods to measure tenderness and some traditional technologies for tenderisation are presented in order to understand how different technologies may affect muscle structure. The effects of heat on the changes in texture of meat depend on water-
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ACCEPTED MANUSCRIPT holding capacity, protein denaturation, solubilisation and gelation, determining the force required to shear the meat (in the mouth), and are described below.
It is important to understand how different technologies may have their effect on texture, sensory tenderness, water-holding capacity and muscle structure, as this assists in
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understanding where technologies used in combination may have additive, interactive or
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multiplying effects.
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2.1 Main determinants of meat tenderness
Tenderness is an important meat quality trait and the biological, structural and physiological
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mechanisms underlying meat tenderness have been extensively investigated (Dransfield &
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Jones, 1980; Harper, 1999; Huff-Lonergan, Zhang, & Lonergan, 2010, Koohmaraie, 1988; Tornberg, 1996). Essentially, meat tenderness is determined by intrinsic factors, such as the amount and solubility of connective tissue (Purslow, 1994), sarcomere shortening during
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rigor development (Marsh & Leet, 1966) and post-mortem proteolysis of myofibrillar and myofibrillar-associated proteins by calpains (Koohmaraie & Geesink, 2006) and cathepsins
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(Ertbjerg, Henckel, Karlsson, Larsen, & Moller, 1999). Post-mortem energy metabolism also affects meat tenderness (Thompson et al., 2006;
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Tornberg, 1996) principally through the effect on the post-mortem structure of the muscle and protein degradation, as discussed below. In addition, external factors, for example, the balance between myofibrillar denaturation, shrinkage in the structure and associated water loss and toughening and solubilisation/gelation of proteins during thermal treatments and heating are known to affect tenderness of meat (Purslow, Oiseth, Hughes, & Warner, 2016; Tornberg, 2005). Interactions occur between the influencing factors, which can be difficult to separate (Harper, 1999) and each of these is influenced to a greater or lesser degree by genotype and the pre- or post-slaughter environment (Warner et al., 2010). Examples of 6
ACCEPTED MANUSCRIPT animal and management factors known to detrimentally affect tenderness, predominantly through influencing muscle protease activity, include the callipyge gene in sheep, a tenderness gene prevalent in the Bos indicus population of cattle and the use of hormonal growth promotants and beta-agonists (Lean & Dunshea, 2014; Warner, Greenwood, Pethick, & Ferguson, 2010; Watson, 2008). The successful application of innovative processing
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technologies for meat tenderisation can be highly dependent on the on-farm management and
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the state of the animal and muscle at time of application.
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2.2 Post-mortem energy metabolism and application of technologies to pre-rigor meat The process of rigor mortis is one of the recognizable signs of death as a result of the
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chemical changes in the muscles, causing the musculature to lose extensibility and become
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stiff. Once an animal is slaughtered, oxygen and blood circulation cease and the muscles are forced to switch to anaerobic metabolism and glycolysis to maintain the generation of ATP. Synthesis of ATP in the muscle is initially by creatine phosphate (CP) but later by
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glycogenolysis and glycolysis. CP usually drops to low levels within 1–2 h post-mortem. When CP levels start to decline, ATP levels also decline, inorganic phosphate increases in the cell, and lactate accumulates concomitantly with increasing hydrogen ion (H+)
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concentration. Once ATP reaches low levels, the extensibility of the muscles starts to
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approach 0% of its original, the pH approaches the final pH, and lactic acid reaches its final concentration of 5–6 mmol g -1 of tissue (in a well-fed, rested animal; Warner, 2016). The decline in the muscle pH post-mortem leads to an increase in intracellular calcium concentration due to altered functions of the sarcoplasmic reticulum and calcium pump leading to rigor development when the ATP production declines. For a detailed account of the biochemical changes in post-mortem meat, see Ferguson and Gerrard (2014) and Warner (2016).
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ACCEPTED MANUSCRIPT Post-mortem energy metabolism in muscle and in particular, glycolysis and rigor onset, are important for determining sarcomere length and the occurrence of shortening-induced toughening (Thompson et al., 2006), protease activity and tenderisation during ageing and myofibrillar spacing which can determine muscle water-holding capacity and tenderness (Hughes et al., 2014). The pre-rigor metabolism and availability of substrate, combined with
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muscle temperature, in any muscle in a carcass will determine the shortening occurring at
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rigor and thus the post-rigor sarcomere length (Koohmaraie & Geesink, 2006). Sarcomere shortening can be due to low temperatures pre-rigor (and consequent cold toughening) or
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high temperatures pre-rigor (and associated heat-toughening) and influences the myofibrillar,
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the connective tissue and also the proteolytic contributions to meat tenderness (Warner et al., 2010). Thus it is evident that control of energy metabolism post-mortem is important for
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producing tender meat.
Meat tenderness varies not only with the rate of glycolysis and rigor onset post-slaughter, but
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also with the extent of glycolysis, classically identified through the ultimate pH (pHu) achieved in a muscle. The relationship between meat pHu and tenderness is quadratic, with a peak in toughness at pHu 6.1 (Purchas & Aungsupakorn, 1993). The improved tenderness as
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ultimate pH increases above 6.1 appears to be largely attributable to improvements in water-
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holding capacity and consequent decreases in cooking losses, and to the greater activity of proteases at pH values close to neutrality (Yu & Lee, 1986). Muscle metabolism pre-rigor in any muscle of a carcass can vary significantly with genetics, nutrition, pre-slaughter stress, muscle fibre type, post-slaughter electrical stimulation and chilling of the carcass (Channon, Payne, & Warner, 2000; Gardner, Kennedy, Milton, & Pethick, 1999; Simmons et al., 2006; Thompson et al., 2006; to name a few good reviews on these topics). Control of meat quality through control of post-mortem metabolism (pH and temperature) is difficult to achieve under commercial conditions and variable responses are 8
ACCEPTED MANUSCRIPT usually due to animal and carcass characteristics rather than processing conditions (Simmons et al., 2006). But if technologies applied to pre-rigor meat are able to; (1) arrest or control the rate of glycolysis, through influencing the glycolytic enzymes, or (2) accelerate the breakdown of membranes and release of proteases, or of ions which activate proteases, they have definite potential for having significant effects on meat tenderisation. This is the
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principal used for applying electrical stimulation to beef and sheep carcasses. It was
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discovered in the 1970’s as a method to accelerate the rate of glycolysis and prevent
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sarcomere shortening due to cold temperatures (Chrystall & Devine, 1978; Davey, Gilbert, & Carse, 1975; Locker, Davey, Nottingham, Haughey, & Law, 1975). The opposite problem
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sometimes now occurs where glycolysis is too rapid in beef carcasses post-mortem, due to electrical stimulation. This causes sarcomere shortening due to high temperatures as the
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muscle enters rigor, protein denaturation and enzyme inactivation during ageing (Gutzke, Franks, Hopkins, & Warner, 2014; Kim, Warner, & Rosenvold, 2014; Warner, Thompson,
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Polkinghorne, Gutzke, & Kearney, 2014).
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2.3 Changes in the texture and structure of meat during heating
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Each piece of meat has a multi-scale, or hierarchical, nature in its’ physical properties, with aspects of the scale being of differential importance in contribution to texture.
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contribution to texture depends on the inherent hierarchical structure of the muscle, including the connective tissue proteins, structural proteins within the muscle cell and degradation or disruption of these proteins. In addition, meat tissue consists of numerous molecules which fragment, denature, interact and solubilise at different temperature and time scales.
The effect of heat resulting from processing technologies, or applied for the preparation of ready-to-eat meals in order to prepare meat for consumption, is also of importance for meat 9
ACCEPTED MANUSCRIPT tenderness. At temperatures as low as 35-40oC, proteins can start to denature, causing shrinkage in the structure, the texture and water loss, with higher temperatures causing more severe effects. Thus any heating arising as a result of the application of a technology needs to be considered, due to consequences for the later sensorial texture subsequent to meal preparation and cooking. This has effects on both meat texture and water-holding capacity,
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and important implications for sensory acceptability.
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Objective measurements of peak shear force (PSF) and subjective sensory evaluations have
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identified two to three phases of changes in toughness/ tenderness (measured by PSF), shrinkage and water loss as a function of temperature. These three phases are summarised in
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Table 1 and are;
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Phase 1 – From 35 to 62oC Transverse shrinkage,
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Water loss,
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Toughening, particularly from 40 to 50-53oC.
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Phase 2 – from 50 to 60-65 oC, a transition phase, which overlaps phase 1 and phase 3, Both transverse and longitudinal shrinkage can occur,
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Sometimes a phase of tenderisation or a plateau is observed.
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Phase 3 - From 60 °C to 80 °C, -
Longitudinal shrinkage,
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Increased water loss,
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Toughening usually occurs, although some observe no change.
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ACCEPTED MANUSCRIPT In spite of the potential and actual variability in experimental heating conditions, species and muscles studied, the studies shown in Table 1 show a consistency of response in showing two to three phases, with the two main phases being toughening and water loss in response to an increase in temperature. Concomitant with the texture changes, heat induces transversal and longitudinal shrinkage of meat, which result in water loss as shown in Table 1 and Figure 1.
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Juiciness is a result of the inherent moisture and fat content of the meat and the release of
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fluids from the muscle structure during oral processing.
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2.4 Measurements of texture and tenderness
In-mouth sensory tenderness is generally correlated to instrumental measures of texture
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(Font-I-Furnois & Guerrero, 2014). Measurements of peak shear force shows a very good correlation to sensory tenderness scores, as shown in Figure 2A (Perry, Thompson, Hwang,
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Butchers, & Egan, 2001). A threshold of peak shear force (PSF) = 40 N (4.1 kg) for sensory
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acceptability of beef tenderness has been established (Huffman, Miller, Hoover, Wu, Brittin, & Ramsey, 1996; Rodas-González, Huerta-Leidenz, Jerez-Timaue, & Miller, 2009). Figure
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2B shows that beef steaks scored by people, in both the home and in a restaurant, as extremely tender, had an instrumentally measured mean PSF of 3.7-4.0 kg. A threshold, for
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acceptability of tenderness, of 40N is used in subsequent discussions in this review.
2.5 Some traditional methods to improve meat tenderness Traditionally, ageing of meat for a period of time post-mortem in an anaerobic environment allows proteolysis to proceed and flavour and tenderness to develop (Koohmaraie & Geesink, 2006). Electrical stimulation applied to sheep, beef and more recently venison carcasses induces rapid glycolysis (see above), preventing sarcomere shortening (cold-shortening) as
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ACCEPTED MANUSCRIPT well as likely disrupting muscle tissue, accelerating proteolysis and resulting in more tender meat (Hopkins, 2014). Tenderstretch, or other stretching techniques discussed in a later section, not only prevent sarcomere shortening but likely also result in muscle disruption and tenderisation (Hopkins, 2014). Moisture infusion can reliably induce improved tenderness in meat as well as juiciness (Channon et al., 2016b). Each of these procedures has met with
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some success, with all of these techniques still being used today. But each technique has
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limitations including, inherent problems for application on-line in modern plants, requirement
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for extensive storage periods influencing efficiency of inventory control or unacceptability for the modern consumer. Thus the need for new and alternative technologies which address
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these deficiencies are required.
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Under the appropriate pressure, temperature and time post-mortem conditions, HPP has been shown to induce tenderisation in meat (see below). Apart from a high energy requirement and the initial capital outlay, which create an impact on the cost of technologies and thus
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industry feasibility, thermal processing during HPP application to meat can lead to undesirable side effects such as nutritional loss or flavour issues (Knorr, Ade-Omowaye, & Heinz, 2002). In addition, HPP application to meat, with associated heating, results in a
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‘cooked’ appearance to the meat. Thus there has been strong industry interest to develop and
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use non-thermal treatments in food processing, such as ultrasonics, shock wave, pulsed electric field and pre-rigor stretching. These technologies, including HPP, are discussed below.
3. HIGH-PRESSURE PROCESSING (HPP)
High pressure processing (HPP) is a technique in which a pressure is applied statically to a product, at or above 100 MPa by means of a liquid transmitter (Simonin, Duranton, & de 12
ACCEPTED MANUSCRIPT Lamballerie, 2012). The pressure is isostatically and uniformly transmitted to the product (Norton & Sun, 2008). In theory, this pressure is transmitted almost instantaneously to the product, and is not dependent on the size and shape of the product, however, in commercial HPP processes, it does take time for the pressure to build up. HPP of food products, and of meat, has generally focussed on extending the shelf-life and improving food safety. The
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application of HPP for meat tenderisation was demonstrated a number of years ago (Bouton,
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Ford, Harris, Macfarlane, & O'Shea, 1977; Bouton, Harris, Macfarlane, & O'Shea, 1977a),
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but its implementation in industry has been slow. HPP can also either be applied to pre- or post-rigor meat. Excellent reviews are available on this topic (Buckow, Sikes, & Tume,
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2012; Guillou, Lerasle, Simonin, & Federighi, 2017; Ma & Ledward, 2013).
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The textural outcome of applying HPP to meat depends on the pressure applied, the temperature, the time, the muscle and the time post-mortem, with the consequent results
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varying from toughening to significant tenderisation. These variations are described below.
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Importantly, during application of high pressure, adiabatic heating occurs which is equivalent
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to 3oC per 100 MPa (Table 2).
As shown in Hughes et al. (2014), there is a change in the colour of meat, as a consequence
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of the application of HPP. When HPP is applied at 10oC, pressures above 100 MPa result in subtle to obvious changes in the visual appearance, as the pressure increases. For this reason, HPP tends to be considered as a viable option for ready-to-eat food, but not for the ‘fresh food’ shelves, limiting its commercial application.
There is an R&D opportunity to
investigate the retention of fresh meat colour in HPP-treated muscle foods.
3.1 Mode of action
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ACCEPTED MANUSCRIPT HPP influences both the structure and function of proteins (Lee, Kim, Lee, Hong, & Yamamoto, 2007) and is known to modify only non-covalent bonds, thus not affecting small flavour molecules or vitamins. In contrast, heat affects hydrogen and covalent bonds, and thus results in both unfolding and irreversible denaturation of proteins. HPP can either be applied at ambient or low temperatures, or at high temperatures, with differential effects on
Whereas pressure favours dissociation and
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the aggregate remains stable after cooling.
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meat proteins and texture. Temperature denatured protein has a tendency to aggregate and
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unfolding of proteins, with refolding and re-association once the pressure is removed (Smeller, 2002). The diagram in Figure 3 shows that in comparing the structures of pressure-
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and heat-denatured proteins, there are three phases for protein structure being native, intermediate/unfolded and intermediate/aggregated.
The diagram also shows that above
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40oC, the aggregated state is more stable than the intermediate and also that the intermediate and unfolded states cannot form an aggregate if the pressure is above 200 MPa (Smeller,
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2002). Alternatively, Sun & Holley (2010) have stated that the changes in proteins are
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usually reversible below 300 MPa, but irreversible above 300 MPa. Meat tenderisation is often associated with increases in protein solubility and HPP treatment appears to induce
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tenderisation through increasing protein solubility as a result of depolymerisation of proteins
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under pressure (Sun & Holley, 2010).
Under HPP treatment, noncovalent interactions between proteins are destabilized and a small degree of unfolding occurs, with subsequent formation of hydrophobic and disulphide bonds after pressure release (Sun & Holley 2010). When pressure is applied at ambient temperature, there appears to be little to no change to the connective tissue (background toughness) because collagen, the main protein, is stabilised by hydrogen bonds (Gekko & Koga, 1983). When pressure is applied at high temperatures (especially 60-70oC), collagen in connective
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ACCEPTED MANUSCRIPT tissue denatures and unfolds and may contribute to the increased tenderisation observed (Ma and Ledward, 2004). The increased hardness or toughness of post-rigor meat subjected to HPP at ambient temperatures may also be due to a greater integrity in the myofibrillar structure (Jung, de Lamballerie-Anton, & Ghoul, 2000a; 2000b).
Generally, the HPP
treatment of fresh meat at high temperatures results in greater tenderness after cooking,
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whereas similar meat without HPP treatment becomes tougher after cooking. The increase in
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tenderness of high temperature-HPP is variously attributed to accelerated proteolysis (Ma &
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Ledward, 2004), increased fracturing of myofibrillar proteins and muscle structure due to greater stability of collagen (Sikes, Tornberg, & Tume, 2010), increased protein
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solubilisation (Sun & Holley 2010), reduced water loss from the myofibrillar structure (Hughes, Oiseth, Purslow, & Warner, 2014), or combinations of these, depending on the
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3.2 Application to pre-rigor meat
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conditions applied.
The application of HPP, at 100-225 MPa and 10-35oC, to pre-rigor meat has consistently been shown to improve the tenderness of beef, lamb, poultry and pork. There has also been a
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patent developed by Hormel foods on this process, for pork (Smit, Summerfield, & Cannon,
AC
2010). The tenderisation associated with HPP of pre-rigor meat is proposed to be a result of either accelerated or arrested glycolysis (Sikes & Warner, 2016).
Accelerated glycolysis, as measured by pH drop in muscles post-pressurisation (Macfarlane, 1973), is most likely a result of release of calcium during the application of pressure, and this is associated with severe contraction resulting in massive disruption to the myofibrillar structure and very tender meat (Bouton et al., 1977a; Kennick & Elgasim, 1981; Kennick, Elgasim, Holmes, & Meyer, 1980; Macfarlane, 1973). Where HPP was applied to pre-rigor
15
ACCEPTED MANUSCRIPT meat and the result was accelerated glycolysis, the increase in tenderness is usually quite large (in the range of 30-80% improvement) across different muscles and species. Bouton et al. (1977a) applied HPP to pre-rigor beef semitendinosus (103 MPa, 35C, 4 min) and if the muscle was not restrained prior to HPP application, the PSF reduced from 188 N in the control to 38 N, a significant change from a highly unacceptable texture to a desirable and
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acceptable product. A PSF = 40 N has previously been reported to be the threshold for
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consumer panel assessment of acceptability of beef tenderness (see previous section). If the
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muscle was restrained prior to HPP application, the resulting PSF was 71 N and much tougher than the HPP-treated non-restrained muscle (Bouton, Harris, et al., 1977a), providing
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evidence that severe shortening causes major disruption and tenderisation.
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Arrested glycolysis during HPP treatment of pre-rigor meat is proposed to arise from the denaturation of glycolytic enzymes during the application of pressure, resulting in a higher
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ultimate pH in the muscle (Smit et al., 2010). Partial inhibition of glycolysis as a result of
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application of HPP to pre-rigor meat has only been demonstrated by Smit et al. (2010) and Souza et al. (2011). Souza et al. (2011) applied HPP to pre-rigor pork carcasses (215 MPa,
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33°C, 15 s) and measured the change in texture for the longissimus, psoas major, triceps brachii and semimembranosus muscles. Although HPP treatment significantly increased
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(P<0.01 for al muscles)the ultimate pH compared to the control in the longissimus (6.26 vs 5.78, respectively), semimembranosus (6.48 vs 6.01) and triceps brachii (6.35 vs 6.08) (P<0.01 for al muscles), a significant (P=0.03) decrease in PSF was only seen for the semimembranosus, (21 vs 25 N; Souza et al., 2011). These results demonstrate the difficulty in inducing reliable tenderisation across all muscles, through the application of HPP to prerigor meat. It is well-known that there is considerable variation between muscles and carcasses in the stage of rigor, and thus muscle pH and sarcomere length at any defined time point in the pre-rigor period. Furthermore, if HPP applied to pre-rigor meat is successful in 16
ACCEPTED MANUSCRIPT arresting glycolysis and results in a higher muscle pH, the curvilinear relationship between muscle pH and tenderness predicts that elevated muscle pH may increase meat toughness (Purchas, 1990). Elevated muscle pH can result in shorter sarcomere length and depending on the level of elevated pH, either higher or lower proteolysis (Purchas, 1990), thus varying
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effects of muscle pH on meat tenderness are observed.
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3.3 Application to post-rigor meat at a low temperature
The application of HPP to post-rigor meat at low or ambient temperatures has shown quite
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variable effects on texture and tenderness, depending on the time, temperature and pressure
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used. Application of high pressure at ambient or low temperature (0-25oC) usually results either in no change in tenderness, or an increase in toughness in beef, pork, lamb, alligator
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and poultry meat (Gimenez et al., 2015; Jung 2000a; 2000b; Duranton et al., 2012; Kim et al., 2007; Grossi et al., 2014; Hong et al., 2005; Hong et al., 2012; Kruk et al., 2011;
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Macfarlane et al., 1981; Ma and Ledward 2004; Zamri et al., 2006; McArdle et al., 2011;
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McArdle et al., 2013). Only five out of 17 references in the review by Sikes and Warner (2016) showed any evidence for tenderisation of meat when HPP is applied at ambient or low
CE
temperatures. In these five studies, the tenderisation was highly dependent on the muscle, pressure, temperature and time applied. The change in PSF values in beef longissimus
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thoracis et lumborum was from about 58 to 38 N (estimated from graph) when HPP was applied at 100 MPa for 10 min, with no tenderisation evident for higher pressures of 200-300 MPa (Schenková et al., 2007). Ichinoseki, Nishiumi, and Suzuki (2006) showed a reduction in PSF values from 58 to 45 N when HPP was applied at 100-500 MPa, at 8oC for 10 min.
17
ACCEPTED MANUSCRIPT 3.4 Application to post-rigor meat at a high temperature Application of high pressure at higher than ambient temperatures (>25oC), generally results in tenderisation. Generally, optimum tenderisation is evident for HPP applied at 100-200 MPa and at temperatures of 60-70°C (Ma & Ledward, 2004; McArdle, Marcos, Mullen, & Kerry, 2013; Rusman, Gerelt, Tamamoto, & Nishiumi, 2007). Across the thirteen studies
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reviewed by Sikes and Warner (2016), all studies showed tenderisation of 30-80%, through
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measurements of hardness or PSF, when the pressure applied was in the range 150-400 MPa
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and the temperature was above 50-60oC for beef, lamb, pork and chicken, across a range of muscles (Bouton et al., 1977a; Bouton et al., 1977b; Ratcliff et al., 1977; Bouton et al., 1980;
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Beilken et al., 1990; Ma & Ledward 2004; Rusman et al., 2007; Sikes et al., 2010; McArdle et al., 2011; McArdle et al., 2013; Sikes & Tume 2014). Pressures above 400 MPa resulted in
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toughening of meat (Ma & Ledward, 2004; McArdle et al., 2013; Zamri, Ledward, & Frazier, 2006), while HPP treatment at 200 MPa for 20 min of beef sternomandibularis,
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50 N (estimated from graphs).
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semimembranosus and biceps femoris reduced the PSF from about 110-130 N down to about
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3.5 Considerations for the future
The application of HPP to meat is no longer seen as an alternative process to conventional
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pasteurisation but as a technology to create new meat-based products. However, pressureinduced changes affecting the colour quality are significant for fresh red meat and need to be considered when evaluating marketability and consumer preferences of new products. High pressure applied at low or ambient temperatures is a commercially viable process but necessitates processing of muscle in the pre-rigor state to achieve tenderisation. This process would reduce the aging time compared to current protocols and as moderate pressures are needed, there is no impact on colour quality. The improved tenderness and yield of post-rigor
18
ACCEPTED MANUSCRIPT meat when HPP is applied at higher temperatures also has potential as a commercial process but would be limited to a specific market, such as the food service industry, due to the impact on colour stability. High pressure processing is unlikely to totally replace traditional meat processing methods but could be used in combination with, or to complement, current
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methods or to discover niche applications and markets.
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4. SHOCKWAVES
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Shockwaves, or hydrodynamic pressure processing, involve the application of high pressure waves up to 1 GPa in fractions of a millisecond (Bolumar, Enneking, Toepfl, & Heinz, 2013)
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which propagates through a fluid (typically water). The shockwaves can be generated by
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piezoelectric, electromagnetic, electro-thermal or electro-detonation methods (Bolumar et al., 2013). The two methods that have been trialled for meat tenderisation are; (a) chemical, by
D
detonating explosives underwater, first described by Long (1993) and shown to tenderise beef
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meat (Solomon et al., 1997) and (b) electrical discharge underwater, which was first described by Long (2000) and shown to tenderise poultry meat by Claus et al. (2001b, 2001a). The electrical discharge system can either be via discharging a high voltage arc
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across a gap between two electrodes in water (Long & Ayers, 2001) or via a sparker system
AC
(Bowker et al., 2011). Details of the principles of the design of the equipment, various configurations for both chemical detonation and electrical discharge and the effects on meat have been described previously (Solomon et al., 1997; 2006; Bolumar et al., 2013; Claus, 2017). During the application of explosive-based shockwaves, the pressure wave of ~100 MPa results in a small increase in temperature of 2-3oC (Table 2). There appears to be no increase in temperature when electrically-generated shockwaves are applied (Table 2).
4.1 Mode of action 19
ACCEPTED MANUSCRIPT The principle of hydrodynamic shockwaves is that they travel through water and also anything that is an acoustical match with water (Claus et al., 2001b). Thus, as meat is 75% water, it is an acoustical match for water and when shockwaves are applied to muscle, the shockwave reflects off any object that is not an acoustical match (Solomon et al., 1997), resulting in ultrastructural damage to the muscle (Zuckerman et al., 2013) and proteolytic
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enzyme release (Bowker et al., 2008).
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There are some indications that shockwaves disrupt the collagen fibril network of the endomysium (Zuckerman et al., 2013). Previous research has shown that detonation
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shockwaves applied to beef longissimus cause fragmentation in the I-band and that the jagged edges of thin filaments next to the Z-line imply physical disruption of myofibrillar proteins
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rather than proteolysis (Zuckerman and Solomon 1998). Others have also shown physical disruption to the muscle fibres and tissues, particularly to the myofibrils and the Z-line (Claus
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et al., 2002; Bolumar et al., 2014). The degradation of troponin-T (TnT) to a 30 kD protein is
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widely used as an indicator of tenderisation due to proteolysis (Huff-Lonergan et al., 1996). Bowker et al. (2008) used SDS-PAGE and Western blotting to show that shockwave
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treatment increased the tenderisation of beef longissimus and enhanced the accumulation of 30kD TnT degradation products, indicating enhanced proteolysis. Bolumar et al. (2014) did
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not show any effect of shockwave treatment of beef longissimus on myofibrillar proteins but as Western blotting was not used, the sensitivity of their assay may have been compromised.
4.2 Explosive shockwaves The early work on the application of a detonation (100 g of explosives) shockwave to beef muscle showed a major effect on the texture of very tough beef, the result being very tender
20
ACCEPTED MANUSCRIPT meat in most cases (Solomon et al., 1997). The muscles tested varied in connective tissue content as well as protease activity and the PSF value was reduced from 78-129 N in controls to 28-57 N in treated muscles, a 55-66% reduction (Solomon et al., 1997). Detonation shockwaves applied to beef semimembranosus after 7 days ageing resulted in a reduction in PSF by >20 N, from 62 to 39 N (Zuckerman et al., 2013). This is a significant reduction, as it
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was induced in a muscle that had already undergone ageing and also is known to be tough
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due to low protease activity, high amounts of connective tissue and relatively short sarcomere
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length (Rhee et al., 2004). Furthermore, after 21 days of ageing post-treatment, shockwavetreated semimembranosus was still more tender than controls (Zuckerman et al., 2013). In
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contrast, turkey pectoralis (a muscle with low connective tissue) treated with electrical shockwave at 3 days post-mortem showed very little tenderisation, although the muscle was
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already very tender prior to treatment (Claus et al., 2001b). The structural myofibrillar and collagen (connective tissue) proteins are largely responsible for the toughness of meat. The
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most well-documented effect of shockwave tenderization is on physically breaking the
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myofilaments, thus in the case of the semimembranosus in the experiment of (Zuckerman et al. (2013), shockwave appeared to achieve a similar tenderising effect to high protease
turkey pectoralis
in Claus et al. (2011b), shockwave does not induce any further
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tenderisation.
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activity. When the meat is already tender when the shockwave is applied, as in the case of
Previously, application of a detonation shockwave to pork loin has shown small levels of meat tenderisation, as measured by PSF (32.4 N, 26.9 N; P<0.01), although a trained panel could not pick up any differences in tenderness (Moeller et al., 1999). The largest effects of detonation shockwaves on tenderisation have been seen in lamb longissimus (57-60 N for control and 19-43 N for shock-waved muscles) (Solomon et al., 1998), beef longissimus, semimembranosus, biceps femoris, semitendinosus (see above; Solomon et al., 1997) and 21
ACCEPTED MANUSCRIPT poultry pectoralis (60 N for control and 43 N for treated) (Meek et al., 2000). The biggest reduction in toughness with detonation shockwaves is seen with the highest amount of charge [for comparisons, see (Solomon et al., 1997; Meek et al., 2000)] and does vary with both muscle and species. As discussed above, low to zero levels of tenderisation have been seen for pork longissimus and turkey pectoralis as a result of detonation shockwaves (Moeller et
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al., 1999; Bowker et al., 2010), most likely because the muscles being treated were not
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considered tough. In the case of turkey pectoralis, the control samples had a PSF of 25 N and
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after detonation shockwaves, the PSF was 29 N, and not different to control (Bowker et al., 2010). A PSF of 25 N is very tender and acceptable to consumers.
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4.3 Electrical shockwaves
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Recent research using commercial units/prototypes has shown promise for tenderising, beef, pork and poultry (turkey chicken) using electrical discharge shockwaves. Applying electrical
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discharge shockwaves to hot- or cold-boned poultry pectoralis has been shown to result in
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tenderisation by 10-20 N (Claus et al., 2001b; 2001a). Pork semimembranosus and semitendinosus showed no change in tenderness in response to 2 pulses of electrical discharge shockwave from a commercial prototype (Bolumar et al., 2013). In contrast, using
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the same unit, beef ST and LL showed reductions in PSF from 84 to 63 N and 48 to 39 N,
AC
respectively (Bolumar et al., 2013). The reason for the difference between species is unclear, as the pork muscles were not particularly tender (43 N for SM; 70 N for ST). For electrical shockwaves, the reductions in toughness are generally about 10-30% across beef, pork, turkey and chicken (Bolumar et al., 2013) and have not shown the dramatic tenderisation as seen for detonation shockwaves. For electrical shockwaves, increased tenderisation results from repeating the pulses and increasing the energy setting (Bowker et al., 2011; Bolumar et al., 2013). Due to concerns with the use of explosives, the technology for tenderising meat using shockwaves now centres around electrical discharge. The use of electrical discharge to 22
ACCEPTED MANUSCRIPT apply the shockwaves allows continuous operation, rather than a ‘batch’ system, which is a characteristic of the shockwave systems utilising detonation. Recent research testing industrial-scale equipment for applying electrical shockwaves has shown no effect on pork semimembranosus and semitendinosus tenderness and a moderate reduction in beef longissimus and semitendinosus (84 to 63 N for longissimus and 48 to 39 N for
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semitendinosus) (Bolumar et al., 2013).
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4.4 Future
Although creating hydrodynamic shockwave by the detonation of explosives in water has
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demonstrated significant tenderization, attempts to commercialize a system based on explosives has encountered technological challenges that have not been overcome.
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Application of explosive shockwaves requires that the meat is vacuum packaged, as the meat needs to be immersed in the same water that the shockwave is produced. When the explosive
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is detonated, a very high percentage of the bags have previously been shown to fail, exposing
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the meat to the processing water, including unknown combustion components, as well as elemental metal released from the shockwave electrodes. Additional problems include the
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safety issues associated with using explosives, lack of durability of the system and the
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predicted very high infrastructure and equipment costs to build the system.
Electrical-based generation of a hydrodynamic shockwave generating system is an emerging technology that is based on the well-established principle that shockwaves can tenderise meat.
Unlike the explosive-based approach, with electrical-based systems it is entirely
feasible to expose the meat to shockwaves multiple times, for additional tenderization. Two somewhat similar electrical-based systems are being developed (Claus, 2002; Bolumar et al., 2014), both with high chances of commercialization. The main difference between the systems is that the system described by Claus (2002) physically separates the meat from the 23
ACCEPTED MANUSCRIPT shockwave processing water. This eliminates any issues associated with the meat absorbing the processing water. In the system described by Bolumar et al. (2014), the meat is exposed to the processing water.
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5. PULSED ELECTRIC FIELD (PEF)
Pulsed electric field (PEF) is one of the novel non-thermal technologies being investigated by
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the food industry to improve the food safety, modify food texture and improve the extraction
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of bioactive compounds. The technology is regarded as an efficient green technology due the short time processing time, fossil fuel-free technology and generates no waste compared to
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traditional processing options. PEF is a treatment of food involving generation of an electrical
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field between two electrodes using direct current voltage pulses for periods of time ranging from microseconds to milliseconds. The theory behind PEF and its applications in food plants
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and biomaterial processing have been examined in depth in several books and review papers
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(Arroyo & Lyng, 2017; Donsi, Ferrari, & Pataro, 2010; Puertolas, Luengo, Alvarez, & Raso, 2012; Raso-Pueyo & Heinz, 2006; Toepfl, Heinz, & Knorr, 2006; Vorobiev & Lebovka, 2008). The potential of PEF to improve food qualities has been investigated (Fryer &
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Versteeg, 2008; Luengo, Álvarez, & Raso, 2013; Wiktor, Schulz, Voigt, Witrowa-Rajchert,
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& Knorr, 2015) and the use of PEF as a post-mortem treatment to enhance qualities of muscle food has only recently been investigated.
Although referred to as a ‘non- thermal’
technology, the application of PEF to food can result in a temperature rise of 5-30oC (O'Dowd, Arimi, Noci, Cronin, & Lyng, 2013) (Table 2) and is called a mild “ohmic” heating (O'Dowd et al., 2013).
Because PEF is an emerging technology in food processing, the amount of research on the potential of PEF in meat is limited in comparison with processing of other food types. 24
ACCEPTED MANUSCRIPT However, recent studies on the effect of PEF on different beef muscle types have shown promising results. As tenderness is arguably the most important attribute of meat, most of the research in this field has focussed on the effect of PEF treatment on meat tenderisation.
5.1 Mode of action
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Cellular membranes become more permeable due to electroporation as a result of the
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application of PEF to biological tissues. Pre- or post-rigor meat treated with PEF prior to
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ageing likely results in membrane damage, which would potentially result in; (i) calcium release from cellular organelles thus activating the calcium-dependent proteases, calpains (ii)
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release of cathepsins from lysosomes, (iii) accelerated glycolysis in pre-rigor meat as a result of the calcium release, all of which could enhance tenderisation. As indicated by Bekhit, van
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de Ven, Suwandy, Fahri, and Hopkins (2014b), a post-treatment aging step is required to overcome the lack of immediate effect for PEF treatment on beef tenderness found by
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O'Dowd et al. (2013) or after short aging period of 2 days (Arroyo, Lascorz, et al., 2015).
5.2 Application to post-rigor (cold-boned) meat
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Application of different strengths of PEF treatment has shown intriguing results. The
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application of a low field strength PEF treatment (1.4 KV.cm-1, 10 Hz) with 300 or 600 pulses of 20 μs each to 48 h post-mortem beef longissimus lumborum at different stages of ageing did not result in a significant change in PSF (88N to 74N) (Arroyo et al., 2015). Further aging times for 10, 18 and 26 days post-treatment tended to indicate lower PSF in PEF treatment samples compared with the non-treated controls at P < 0.1. High intensity PEF (10 kV.cm-1, 90 Hz) applied to cold-boned (24 h post-mortem) longissimus lumborum resulted in a reduction of ~25 N (57 N to 35 N) in 21 day aged meat (Suwandy, Carne, van de Ven, Bekhit, & Hopkins, 2015c, 2015d). The effect of PEF on tenderisation varies with 25
ACCEPTED MANUSCRIPT the treatment intensity, i.e. the voltage and frequency of the applied PEF. Application of 5 kV.cm-1 at 90 Hz or 10 kV.cm-1 at 20 Hz PEF to cold-boned (24 h post-mortem) beef longissimus lumborum produced the greatest tenderisation (PSF reduced from 61-64 N to 4950 N after 21 days of ageing) relative to 5 kV.cm-1 at 20 or 50 Hz PEF (Bekhit, van de Ven, Suwandy, Fahri, & Hopkins, 2014b; Suwandy, Carne, van de Ven, Bekhit, & Hopkins,
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2015a). In addition, when the high intensity PEF (10 kV.cm-1, 90 Hz) is repeatedly applied,
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the PSF value decreased by an average of 2.5 N with each application (61 N to 51 N)
SC
(Suwandy et al., 2015d). Interestingly, proteolysis analysis using SDS-PAGE and Western blotting indicated that, while degradation of troponin-T and desmin were associated with a
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reduction in PSF of meat cuts treated once with PEF, the absence of degradation of these two proteins in samples treated with PEF two and three times suggested another mechanism, such
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as physical disruption of myofibrils, is involved in the tenderisation process (Suwandy et al., 2015d). Although PEF is theoretically a non-thermal technique, high intensity PEF treatment
D
of meat has been shown to induce heating in meat samples, as demonstrated in various
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studies (Bekhit, van de Ven, et al., 2014b; Suwandy et al., 2015c; 2015d). The muscle temperature was elevated by 12.6-16.2oC after PEF of cold-boned beef longissimus cuts
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Suwandy et al., 2015d. This elevated temperature may contribute to an increase in myofibrillar protein and enzyme denaturation, likely explaining the absence of troponin-T
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and desmin degradation in meat samples subjected to repeated PEF treatment (Suwandy et al., 2015d).
It is well-known that muscle types differ in morphology, fibre type composition, intrinsic myofibrillar proteomic composition and metabolic properties, resulting in differing meat qualities (Tornberg, 2005). The effect of PEF treatment in different muscle types was examined under different PEF intensities, and repetition of treatment coupled with varying
26
ACCEPTED MANUSCRIPT ageing durations. A difference in PSF reduction was observed between beef cold-boned longissimus lumborum and semimembranosus muscles treated with different PEF voltages and frequencies (Bekhit et al., 2014b; O'Dowd, Arimi, Noci, Cronin, & Lyng, 2013; Suwandy et al., 2015a) that reflected signficant effects for the muscle and the processing conditions. Differences in the amount of heat generated between beef longissimus and
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semimembranosus due to PEF treatment may explain the differences between the muscles in
This also suggests that meat composition and
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Suwandy et al., 2015a; 2015b, 2015d).
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PSF reduction and proteolysis post-treatment (Bekhit et al., 2014b; Bekhit et al., 2016;
probably muscle fibre type play a role in the variation in tenderisation response to PEF
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between muscles.
5.3 Application to pre-rigor (hot-boned) meat
The effect of PEF on meat qualities of hot-boned muscles has also recently been examined
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and has been found to have differential effects on different muscles. Application of PEF at 510 kV.cm-1 tended to cause an increase in the toughness of the longissimus lumborum with increasing PEF frequency (20, 50, 90 Hz) whereas the semimembranosus tended to show a
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decrease in PSF (by about 25 N at each time point) with an increase in PEF frequency
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(Bekhit, Suwandy, Carne, van de Ven, & Hopkins, 2016a; Suwandy, Carne, van de Ven, Bekhit, & Hopkins, 2015b). The authors also showed an increase in the toughness (increased from 60 to 74 N) of hot-boned beef longissimus lumborum with repeated high strength PEF treatment (10 kV.cm-1 and 90 Hz) whereas the semimembranosus was more tender after repeated PEF treatment. The effect of PEF on the water holding capacity of beef was found to differ between the two muscle types (Bekhit et al., 2016a; Suwandy et al., 2015b), which may have contributed to the differences in tenderisation. Changes in the micro-environment at the cellular level can affect the activity of calpains (Huff-Lonergan & Lonergan, 2005). For 27
ACCEPTED MANUSCRIPT example, an increase in ionic strength that can be expected with electroporation of the cells ,after US application, and the moisture available to sustain the released ionic components, would both affect calpain activity.
5.4 Future
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The limited research on the effect of PEF in muscle foods has indicated some potential for the
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application of PEF for tenderisation as a post-mortem technology to improve meat qualities.
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Optimum processing parameters appears to differ for the various muscles. More research is required to evaluate the impact of PEF on commercially important muscles other than those
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already studied. Thus the variable effect on meat texture between different muscles needs to be resolved and further research is required to understand the mechanism by which PEF
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affects muscle structure. In addition, it appears that the design and application of different intensities and repetitions of PEF treatment in order to achieve desirable sensory attributes in
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different meat cuts needs further consideration.
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6. ULTRASONICS (US)
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Power ultrasound (US) is a non-thermal technology based on sound energy. As the sound wave travels between high (compression) and low (rarefaction) pressure, microscopic gas bubbles oscillate and grow in size. The process will continue until the bubble implodes, resulting in a phenomenon known as cavitation (Tiwari, 2015). The efficiency of cavitation is dependent on several factors. Predominantly, the frequency of the sound wave will determine whether cavitation occurs and if it is stable and transient cavitation (Tiwari, 2015). At frequencies of 18-100 kHz, microscopic gas bubbles have approximately 25 µs to grow during the rarefactional cycle, leading to less frequent but more violent cavitation (Crum, 28
ACCEPTED MANUSCRIPT 1995). Excellent reviews are available in Misra et al. (2017) and in Alarcon-Rojo et al. (2015).
6.1 Mode of action It has been suggested that tenderisation of post-rigor meat using ultrasound is by one or a
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combination of; (a) physical disruption of the tissue caused by cavitation (Jayasooriya et al.,
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2004), (b) release and activation of enzymes (Roncales et al., 1993) and/or by (c) altering the
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metabolism in pre-rigor meat by the release of calcium (Got et al., 1999). Ultrasound application has some potential for improving the texture of post-rigor meat. However, for this
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to be a commercial viability, the acoustic conditions need to be thoroughly investigated in
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order to optimise the conditions for tenderisation.
Along with bubble implosion, other mechanical actions which occur during US application
D
can induce physical and chemical changes in a medium. Pressure fluctuations are known to
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squeeze and release a medium, which in combination with bubble oscillations can cause agitation and micro-stirring. The implosion of the bubble can cause a micro-jet, which if
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directed at a solid surface, can induce physical disruption. In the case of meat, this has been shown to disrupt myofibrils (Got et al., 1999). Moreover, the action of cavitation may split
AC
molecules, resulting in free radical formation and accelerated chemical reactions (Crum, 1995). Therefore, care must be taken to optimise US studies for tenderisation while limiting oxidation. As many factors affect the efficiency of cavitation such as parameters of the medium (viscosity, dissolved gas, temperature), vessel (geometry, material) and acoustics (frequency, intensity, amplitude, treatment time), optimisation and measurement of the acoustic field are important. Several authors have discussed these factors in more detail (Crum, 1995; Raso et al., 1999; Tiwari, 2015).
29
ACCEPTED MANUSCRIPT
Although it has been suggested that US could possibly fragment collagen, damage cell membranes, affect protease activity and disrupt meat structure (Misra et al., 2017), further work is required to fully understand and optimise the penetration depth of US in meat. As demonstrated by McDonnell et al. (2014), US (20 kHz, 19 W cm-2, 40 min) caused an
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increase in denatured myosin on the surface of pork LTL (<2 mm depth) during ultrasonic
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salting. Myosin denaturation was attributed to the US treatment as the salt concentration was
SC
low (5.7% w w-1 NaCl) and myosin peaks were evident in differential scanning calorimetry (DSC) graphs for all other samples, including control samples, which had been treated with This indicates that the actions of US may be strongest at the surface of meat.
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salt.
Furthermore, studies indicate that frequency, intensity and treatment time play an important
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role in US efficiency. Importantly, temperature increases of 15-30oC can occur when ultrasound is applied to meat, depending on the experimental set-up (Jayasooriya, Torley,
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D’Arcy, & Bhandari, 2007) (Table 2). The rise in temperature is attributed to the conversion
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of ultrasonic energy into heat (Jayasooriya, Torley, D’Arcy, et al., 2007).
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6.2 Low intensity US applied to post-rigor meat
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It is difficult to conclude on the effect of US on meat texture due to variation in the US parameters and results of studies. It has been suggested that intensities below 10 W cm-2 do not have a tenderising effect on meat (Alvez et al., 2013). This has been been corroborated by other studies, predominantly using ultrasonic baths whereby the intensity is low due to a large emmitting surface at the base of the bath. Lyng et al. (1997) treated beef Longissimus thoracis et lumborum (LTL), Semimembranosus (SM) and Biceps femoris (BF) in an ultrasonic bath (30-47 kHz, 0.29-0.62 W cm-2, 5-90 min) and found no effect on peak load bite force tenderometry, collagen solubility and SDS page of myobribrillar proteins. 30
ACCEPTED MANUSCRIPT However, other authors found a significant decrease in shear force when treating beef in US baths at 25.9 kHz, 1000 W US bath, 2- 16 min (Smith et al., 1991) and 40 kHz, 1500 W, 1060 min (Chang et al., 2015). One theory for inconsistent results could be that samples are analysed too soon after treatment such that US may disrupt the microstructure, thereby affecting proteolysis and changing the texture over the ageing period. In a study which
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applied US (45 kHz, 2 W cm-2, 120 s) to beef SM and assessed the changes at various stages
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of post-mortem (24, 48, 72 and 96 h), microsctructural changes were evident in the 24 h post-
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mortem samples suggesting that sonication can accelerate the post-mortem process (Stadnik et al., 2008). The sonicated sample differed from the control such that there was swelling of
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the A-band and fragmentation of the z-lines (Stadnik et al., 2008). Such changes in the microstructure could be beneficial for tenderisation if applied to pre-rigor meat. This was an
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interesting approach as it demonstrated that the effect of US on meat may differ depending on the post-mortem time it is applied. Lyng et al. (1997) also applied US to beef at 24 or 72 h
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post-mortem stating that the aim of the 24 h treatment was to enhance early proteolytic
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activity, while at 72 h post-mortem, the myofibrillar proteins may be more susceptible to US disruption due to weakening by proteases. However, no positive effects of US on
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tenderisation were found (Lyng et al., 1997). The post-mortem time chosen for US application in a study depends on the initial hypotheses. However, the majority of authors
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standardise the application of US to meat at 24 h post-mortem (Sikes et al., 2014; Jayasooriya et al., 2007; Stadnik et al., 2008), as this ensures that the ultimate pH has been reached, thus reducing variability in tenderisation response.
6.3 Application to pre-rigor meat Considering that several studies suggest an effect of US on meat microstructure (Got et al., 1999; Stadnik et al., 2008) and enzyme activity (Xiong et al., 2012; Roncales et al., 1993), 31
ACCEPTED MANUSCRIPT there is certainly interest in applying the technology to pre-rigor meat and thus assess the effect of US on rigor-onset and the action of the proteases over the ageing time. In a study assessing the effect of US (2.6 MHz, 10 W cm-2, 30 s) on pre-rigor beef SM (day 0, pH 6.2), microstructural analysis revealed stretching of sarcomeres, z-line disruption and a slight delay in rigor onset, however, no effect the ageing rate or ultimate tenderness was observed (Got et
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al., 1999). Similarly, Sike et al. (2014) reported that high frequency US (2 MHz, 48 kPa
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acoustic pressure, 5 min) applied to beef sternomandiburlaris resulted in a tendency towards
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increased exhaustion factor (P = 0.073), suggesting increased glycolytic activity, but this was not evident in the final tenderness of the product. In two separate studies which applied high
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intensity low frequency US (20 kHz, 62 W cm-2, 15 s) to pre-rigor beef (Lyng et al., 1998a) and lamb (Lyng et al.,1998b), there was no effect on bite force tenderometry, sensory texture,
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collagen solubility or myofibrillar proteins assessed by SDS-PAGE. Although these studies found no ultimate improvement in meat tenderness the studies of Got et al. (1999) and Sike et
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al. (2014) indicate that frequencies above 2 MHz may cause ultrastructural changes in the
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meat matrix which warrants further research.
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6.4 High intensity US applied to post-rigor meat
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It has been suggested that US could be applied to manipulate proteolytic enzyme activity in order to increase tenderness (Xiong et al., 2012; Chang et al., 2012), in which case an assessment of meat tenderness during the ageing process following US treatment is of interest. However, as with all US studies, the experimental parameters must be optimised. For example, in a study assessing the effect of US (40 kHz, 1500 W, 10-60 min) on beef semitendinosus (ST) muscles, only 10 min of treatment significantly affected the activity of β- galactosidase and β-glucuronidase enzymes (Chang et al., 2012). Moreover, the level of enzyme in the sonicated samples was lower than the control which is undesirable given that 32
ACCEPTED MANUSCRIPT β-galactosidase and β-glucuronidase play a role in collagen degradation. Although other proteolytic enzymes are key to post-mortem tenderisation, the study of Chang et al. (2012) indicates that when US parameters are optimised, increased enzymatic activity may be evident. This warrants further research on the effect of US on the activity of other proteolytic enzymes such as calpains and cathepsins. However, it must be noted that cavitation may
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disrupt the cell membrane leading to release of enzymes from the cytosol early on in US
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treatment and that cavitation itself may damage enzyme activity (Chang et al., 2012; Got et
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al., 1999).
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Although high intensity US (20 kHz, 56-62 W cm-2, up to 3 min) has been shown to increase protease activity in cell plasma in lamb liver, the increase in activity was not sustained and
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ultimately, there was no difference compared to conventional ageing (Roncales et al., 1993). Got et al. (1999) sonicated (2.6 MHz, 10 W cm-2, 15 s) post-rigor beef SM and reported that
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there was only an increase in tenderness at 6 days post-treatment with no final improvement
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after 14 days storage. It is concluded by the authors that the US treatment conditions used in this study are not sufficient to induce textural changes in meat. Likewise, in another study
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which applied relatively high frequency US treatment (600 kHz, 48 kPa and 65 kPa acoustic pressure, 10 min) to beef LTL muscles, no effect on tenderness over storage of 7 days was
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found (Sikes et al., 2014). The approach of Jayasooriya et al. (2007) was valuable in that a study was firstly conducted to assess the length of treatment time required to tenderise meat with the given apparatus and experimental set-up. It was found that when beef muscles (LTL and ST) were sonicated (24 kHz, 12 W cm-2) for up to 240 s, the WBS force decreased as a function of US treatment time. Certainly, in studies which applied shorter US treatment times (20 kHz, 63 W cm-2, 15 s) to beef, there were no tenderising effects (Lyng et al., 1998a; 1998b).
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6.5 Future Fundamental studies should be conducted to further elucidate the effect of US on meat (microstructure, enzyme activity, final tenderness) and to optimise process parameters (frequency, intensity, treatment time) for improved efficiency and penetration into the meat
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matrix. As both ultrasonics and meat science are complex, it is imperative that US studies
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report measurements of the acoustic field and details of the experimental set-up as this will
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reduce the difficulty in replicating experiments and allow the field of ultrasonics to evolve. This is especially important in the case of studies which assess the application of US for meat
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tenderisation as there is a high level of variability in the findings.
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7. SMARTSTRETCH™/SMARTSHAPE™ AND PIVAC® The development of methods such as ‘tenderstretch’, ‘tendercut’ (Sorheim & Hildrum, 2002)
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and ‘super stretch’ (Kim, Kerr, Geesink, & Warner, 2014; Warner, Kerr, Kim, & Geesink,
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2014) were to ‘stretch’ muscles and prevent toughening during rigor development. However, these methods were applied to the whole carcass, leading to stretching in only a selected
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number of muscles in the carcass during hanging. Recent developments of PiVac® (Sorheim & Hildrum, 2002) and Smartstretch™ (Taylor, Toohey, van de Ven, & Hopkins, 2012b;
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2013b; Toohey, Van de Ven, Thompson, Geesink, & Hopkins, 2012a; 2012b; 2012c) involve not only stretching, but also shaping. These technologies are applied to hot-boned muscle and have shown significant improvements in meat tenderness.
7.1 Mode of action It is well established the degree of muscle contraction which occurs during rigor mortis is correlated to tenderness of meat (Locker, 1960). Thus the application of stretching to muscle 34
ACCEPTED MANUSCRIPT is well-known to produce more tender meat, mainly through the pre-rigor prevention of muscle shortening. An excellent review of Smartstretch and PiVac is provided in Taylor and Hopkins (2011).
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7.2 PiVac®
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PiVac involves an initial wrapping technique which is applied via stretching of an extendable elastic sleeve by pressure inside a packaging chamber. Following insertion of muscles into
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the packaging chamber, the pressure is released, which results in the elastic sleeve preventing
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muscle contraction through restriction in expansion in the diameter of the cut. PiVac® applied to hot-boned beef muscles chilled at different temperatures showed an increase in
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sarcomere length (Hildrum, Andersen, Nilsen, & Wahlgren, 2000; O'Sullivan, Korzeniowska, White, & Troy, 2003) and allowed rapid chilling of hot-boned M. longissimus without
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compromising tenderness (Hildrum, Nilsen, & Wahlgren, 2002). Moreover, when PiVac®
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was compared to low-voltage and high-voltage electrical stimulation of hot-boned beef M. longissimus, the PSF value was lower for PiVac® (45 N) compared to other treatments (~90
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N) following 14 days of ageing and this was also confirmed by a trained sensory panel
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(O’Sullivan et al., 2003). 7.3 Smartstretch™
Recent developments of Smartstretch™ combine both stretching and shaping and are applied to meat removed from the carcass. Unlike tenderstretch and tendercut, in which some muscles are restricted from stretching in intact carcasses, these new technologies are applied to hot-boned muscle and have been shown to significantly improve meat tenderness. Similar to PiVac®, a more recent stretching and shaping technique named Smartstretch™ was
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ACCEPTED MANUSCRIPT developed and patented (SmartstretchTM/SmartshapeTM) to increase tenderness of hot-boned meat cuts (Pitt & Daly, 2010). Smartstretch™ employs a flexible sleeve placed in an airtight chamber and when meat inserted into the flexible sleeve is compressed, it prevents any expansion in the diameter of the product by forces perpendicular to muscle fibres. Pre-rigor beef longissimus lumborum and gluteus medius showed a reduction of 12-14 N in PSF with
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the application of SmartstretchTM treatment and the application to sheep semimembranosus
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caused significant tenderisation with a reduction in PSF of 22-49 N (Taylor et al., 2012b;
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2013b; Toohey et al., 2012a; 2012b; 2012c). Interestingly, SmartstretchTM treatment of both beef and sheep meat resulted in juicier non-aged meat cuts (Toohey et al., 2012a; 2012c) and
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stretching has been shown to increase the water-holding capacity of meat (Warner, Kerr, et al., 2014). These results demonstrate potential improvement of eating qualities of hot-boned
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primals by SmartstretchTM in accelerated meat production.
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7.4 Combining stretching with other technologies Application of PiVac® and Smartstretch™ treatments to hot-boned primals offers advantages
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over whole carcass stretching such as a reduction in chiller space and energy requirements, accelerating meat processing and increasing control over serving portion size and shape
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control for consumers.
Increasingly, research into improving eating quality of meat is
exploring the combinatory effect of more than one tenderising method. Several studies have investigated the potential of a combination of electrical stimulation and ageing coupled with muscle tenderstretching and PiVac® and reported mixed results on different meat cuts (Sørheim and Hildrum 2002; Troy 2006). More recently, a study of Toohey et al. (2013a) showed that medium voltage electrical stimulation neither improved nor inhibited the tenderising effect of SmartstretchTM in sheep M. semimembranosus. It is noteworthy that the
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ACCEPTED MANUSCRIPT degree of muscle contraction varies with muscle types (Locker 1960), reflecting underlying differences in glycolysis, temperature and pH of meat at the time of rigor. It is therefore important for research on meat stretching and shaping to be performed in targeted primals in
7.5 Future
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The number of studies on meat qualities following application
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order to ensure consistent end-results in commercial settings.
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of PiVac® and SmartstretchTM are limited compared to other technologies. Even more limited are fundamental studies examining molecular changes in meat under stretching and
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shaping. Variations in sarcomere length, in PSF and thus in the level of tenderisation between different muscles in response to SmartstretchTM (Toohey et al., 2012b) are not well
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understood. Adoption of SmartstretchTM and PiVac® in commercial settings has been limited for various reasons, including a relatively small number of hot boning plants, cost
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in integrating SmartstretchTM and PiVac® machines into existing production
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chains and training of operating staff, and inconsistent tenderness of primals that vary in size. Other challenges of SmartstretchTM and PiVac® prototype machines are their speed of
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operation and the labour intensiveness required for their operation (Sorheim & Hildrum, 2002). Thus further investigation to address these issues is warranted
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for successful implementation of these technologies.
8. COMPARISON OF TENDERISATION BETWEEN VARIOUS TECHNOLOGIES
It is quite difficult to compare the tenderisation outcome from a technology, across studies, when the conditions of applying a technology for meat tenderisation include different species,
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ACCEPTED MANUSCRIPT different muscles, varying time applied post-mortem and widely varying conditions of application. Therefore, a meta-analytical approach was used to unify the published literature.
8.1 Meta-analysis of the effects of technologies on peak shear force (PSF)
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Meta-analysis is an appropriate statistical methodology to use where sufficient data is available from different studies. Thus data was collected from a number of studies for all the
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aforementioned technologies, namely PEF, HPP, SW, PEF, US and tenderstretch/Pivac.
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Studies were only included where there was PSF data, sufficient detail was given in terms of variation (SE, SED or SD), muscles, number of animals and samples were provided and an
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appropriate control was included. The change in PSF in response to the application of a
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technology was then expressed relative to the control and the variation was standardised to a standard error. A summary of the analysis follows and greater detail will be provided in a paper by Warner and the other co-authors on this paper (yet to be published) but the approach
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was very similar to that utilised by Lean et al. (2014). Table 3 shows the number of studies included as well as the number of treatments/tests within each study, the species and muscles included and the source references. In the case of data where there was distinct groupings of
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treatment, and sufficient data was available for each grouping, the data were initially
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analysed across all the studies, and was then partitioned into the separate sub-groupings. Thus, PEF was separated into the application to pre- or post- rigor meat and shockwave was separated into electrical and explosive. In the case of HPP, sufficient data was available to analyse the effect of species, as well as pre- vs post-rigor. In addition, the conditions of HPP widely varied in pressure and temperature and there was insufficient data available for pork or poultry to analyse the combined effects. In the case of beef and lamb, sufficient data was available to analyse the combined effects of pressure and temperature and these data are presented below. 38
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All the technologies investigated had significant and positive effects on tenderness, as measured by the change in PSF from the control (Tables 4 and 5 and Figures 4, 5 and 6). Overall, PEF resulted in a reduction in PSF of 4.4 N (data not shown), but when split into two groups of pre- and post-rigor application, there was no effect of pre-rigor application of PEF
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(P>0.05) whereas the application of PEF to post-rigor meat resulted in a reduction of 7.1 N
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(P<0.05) in PSF. In the case of the technology shock-wave, the only technology which is
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approved for use commercially is electrical shockwave, and overall the reduction in PSF across all studies was 7.5 N. This compares to a much larger reduction in PSF with explosive
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shockwave of 17.7 N. The reduction in PSF with ultrasound was 6.0 N and was similar to that achieved with PEF applied to pre-rigor meat and electrical SW. Excluding HPP,
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Smartstretch applied to pre-rigor meat achieved the greatest improvement in tenderness of 10.8 N. Overall, HPP applied to meat resulted in the largest reduction in PSF, of 43.5 N.
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Further analysis was conducted of the HPP data and this showed an effect of species
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(P<0.001) and also time of application (P<0.001). The greatest effect of HPP on shear force was on beef and sheep meat followed by pork and chicken (predicted change in PSF; 29.7,
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14.0, 9.9, 8.5 N respectively) (Figure 5). Pre-rigor meat showed a much greater decrease in shear force in response to HPP, relative to post-rigor meat (predicted change in PSF; 26.3, 4.7
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N respectively) (Figure 5). Further meta-analysis of the effect of different high pressure and temperature combinations applied to beef and sheepmeat showed an interaction between pressure and temperature (P<0.001) (Table 5 and Figure 6). The greatest positive change in PSF was observed at low pressures (100-150 MPa) combined with intermediate (35-45 oC), high (50-60 oC) and very high (68-80 oC) temperatures. Intermediate pressures (200-400 MPa) had only small positive effects on PSF. High pressures (520-600 MPa) generally had little effect on PSF except at low (10-30 oC) temperatures there was a clear toughening effect.
39
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It is worth noting that PEF, US, non-thermal HPP and SW are applied at ambient temperature and are called ‘non-thermal’ as they have an effect on the microbial load at ambient or sub thermal temperatures (Cullen, Tiwari, & Valdramidis, 2011). However, these technologies generate heat and can increase the temperature, by up to 30oC, of treated samples, under
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certain conditions (see Table 2). In addition, Smart-stretch/PiVac are applied to ‘hot’ pre-
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rigor muscles (30-40oC). Thus generation of heat during technology application (see Table 2)
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or warm muscle conditions during application to pre-rigor meat means that phase 1 of the three heating stages associated with changes in texture and water loss mentioned in section
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2.3, are of relevance. Where the application of thermal high pressure processing is concerned,
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all three phases are relevant.
It should be noted that it is well-known that different muscles in the carcass vary widely in
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their tenderness, depending on anatomical location and function which relates to sarcomere
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length, collagen content and cross-linking and protease content and post-mortem activity. For example, amongst eleven major muscles in the beef carcass, the sensory and PSF
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tenderness ranges from very tender in the psoas major (sensory tenderness =7.4 out of 10 points; PSF = 28.9 N) to tough in the supraspinatus (sensory tenderness = 4.1 out of 10
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points; PSF = 48.5 N; Rhee et al., 2004). Thus although many studies included the longissmus and for chicken and turkey only the pectoralis major was tested, other studies included a range of muscles (Table 3). 8.2 Comparison of the effects of growth promoting technologies on meat texture Previously, a meta-analysis was conducted to determine the effects of metabolic modifiers on the tenderness of beef meat. From a meta-analysis of 22 studies, hormonal growth promotants (HGP’s) significantly increased the PSF (toughness) of beef longissimus by 2.6 N 40
ACCEPTED MANUSCRIPT (Watson, 2008). Thus, in the MSA model for predicting eating quality, the meat from HGPtreated cattle has a 5-point reduction in the consumer- derived meat quality score (MQ4) applied, to adjust for this effect. Since some of the processing effects and animal effects on meat quality are additive, HGP-treated meat has to be aged for longer to reach the same degree of tenderisation as meat from untreated cattle. Meta-analysis of data has shown that
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the application of the beta-agonists zilpaterol and ractopamine to cattle causes increased PSF
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of beef longissimus by 8.2 and 2.0 N, respectively (across 47 and 17 studies respectively)
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(Lean & Dunshea, 2014). If ractopamine and zilpaterol were to be registered for use in Australia, reductions in the predicted MQ4 score would need to be included in the MSA
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model for predicting eating quality. In other markets, the benefits in efficiencies and carcass yield from along the value chain from using HGP’s and beta-agonists will need to be offset
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against any negative effects on consumer perceptions of eating quality. Figure 4 shows metaanalysis results comparing changes in PSF in response to application of metabolic modifiers
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(HGP, ractopamine, zilpaterol) to beef cattle. It is evident that the technologies applied post-
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slaughter generally increase the PSF by at least 6-7 N, whereas the application of HGP’s and of zilpaterol only result in a reduction in PSF of 2-2.6 N, ractopamine causing a reduction in
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PSF of 8.4N. This suggests that the application and optimisation of post-slaughter
modifiers.
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technologies would likely overcome any toughness induced by the use of metabolic
Other animal factors known to increase red meat toughness include the callipyge gene in sheep (Cockett et al., 1993; Duckett, Snowder, & Cockett, 2000), the Carwell sire in sheep (Jopson et al., 2001; Nichol et al., 1998) and a toughness gene prevalent in bos indicus cattle (Cafe et al., 2010; Cafe et al., 2011), to name a few. Previously, electrical stimulation has been found to have little to no effect on the tenderness of the leg, forequarter and loin
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ACCEPTED MANUSCRIPT muscles of callipyge sheep (Kerth, Cain, Jackson, Ramsey, & Miller, 1999; Solomon, Carpenter, Snowder, & Cockett, 1998) although detonation/explosive shockwaves resulted in significant tenderisation of callipyge loin muscles (Solomon et al., 1998). The modern production of lean beef, sheep, pork and poultry carcasses has been achieved through the use of genetics in combination with nutrition and metabolic modifiers and this has generally
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resulted in reductions in eating quality (Dunshea et al., 2016). The opportunity is to
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processing technologies, such as those described above.
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overcome some of the reduction in eating quality through the application of post-mortem
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8.3 Possible combinations of technologies
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Exogenous proteases have been shown to be capable of hydrolysing meat proteins, thus facilitating tenderization of meat and has recently been comprehensively reviewed by Bekhit, Hopkins, Geesink, Bekhit, and Franks (2014a). The proteases can be extracted or generated
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from plant, marine, fungal or microbial sources and each protease shows varying levels of proteolytic acitivty against collagen and myofibrillar proteins. Actinidin is an extract from kiwifruit showing particular promise as it exhibits a more controlled tenderization action
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through hydrolysis of myofibril proteins, which may offer an advantage in reducing the
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mushy texture and off flavour observed in meat treated with other proteases. It is likely there will be developments in new proteases for meat tenderisation and they show potential for being combined with some of the technologies discussed above.
Certainly, there is scope for further research on the interactions and possible synergistic effects of emerging technologies combined with enzymes for meat tenderisation, particularly to add value to high connective tissue muscles. An understanding of the mechanisms of how each technology induces tenderisation assists in determining the ideal combination of 42
ACCEPTED MANUSCRIPT technologies for a particular cut of meat or market. For example, the target for low connective tissue muscles, destined for a local market, might be accelerating the proteolytic process in order to reduce the ageing period required. All of the technologies discussed above show some promise for delivering accelerated tenderisation as each has been shown to have some effect on proteolysis or muscle structure. In contrast, high connective tissue
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muscles are more likely to require an intervention technology which influences collagen as
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well as myofibrillar structure. When high pressure processing is applied at high
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temperatures, there appears to be some changes to connective tissue with may contribute to the positive outcomes for texture. Exogenous enzyme added to meat cuts also cause
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degradation in collagen and connective tissue. Thus high temperature-HPP, or exogenous enzymes, applied alone or in combination, are possible solutions for delivering accelerated
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tenderisation in high connective tissue cuts, thus warranting further investigation.
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9. SUMMARY
High pressure processing, shockwave processing, ultrasound, pulsed electric field and
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SmartstretchTM/PiVacTM can be used to increase the tenderness, predominantly through physical disruption to muscle structure, enhanced proteolysis and ageing and muscle protein
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denaturation and solubilisation depending on the technology.
A number of studies have been conducted on the ideal conditions for tenderisation from the application of high pressure processing. The meta-analysis on the available studies shows the ideal conditions are 20-150 MPa and ≥ 35 oC. Subjecting meat to high pressures (520-600 MPa), can result in toughening, particularly when applied at low or ambient temperatures. Meat subjected to HPP pre-rigor shows double the amount of tenderisation relative to the application of HPP to post-rigor meat, although it is recognised pre-rigor application of HPP 43
ACCEPTED MANUSCRIPT is logistically more difficult. There are species differences in the tenderisation response to HPP with the order of tenderisation response to HPP being beef > sheep meat > pork=poultry and beef showing double the tenderisation response relative to sheep meat. Likely the differences between species are due to variation in the initial tenderness, and rate of tenderisation, with beef generally being tougher, and requiring a longer ageing period relative
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to meat from the other species.
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The research on generating shockwaves using explosives has shown significant tenderisation outcomes. The application of shockwaves using electricity and of PEF, for meat
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tenderisation, are only very recent. Using the data on PSF from the available studies in the literature, as well as some unpublished data, showed that the application of electrical
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shockwaves, PEF and ultrasound to cold-boned meat produced a similar reduction in PSF of 6-7 N. Across all available studies, the application of smartstretch and high pressure
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processing, but not PEF, resulted in significant tenderisation when applied to pre-rigor meat.
There is potential for tenderisation technologies to be used to ameliorate the toughness in
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meat resulting from genetic and production practices. Furthermore the application of tenderisation technologies to pre- and post-rigor muscles, including muscles traditionally
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considered to be quite tough, should deliver real benefits to an industry that prides itself on quality, and is also often for quality. The optimum application of these new and innovative technologies for tenderisation will need to be adjusted for different muscles in the carcass, different markets (food service, fresh product, export markets) and also target demographics.
Previous research shows that in some countries, the consumer will be willing to pay for assured tenderness. This will likely drive the interest in, and adoption of, these emerging
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ACCEPTED MANUSCRIPT technologies for tenderisation. The implementation of these technologies in industry will be dependent on operators willingness to innovate, the capital and operating cost of the technologies and the cost-benefit.
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10. Acknowledgements Funding provided by Meat and Livestock Australia in project V.RMH.0044 is gratefully
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acknowledged. 11. REFERENCES
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Acil Allen Consulting (2016). Independent performance review of Meat and Livestock Australia and the MLA donor company. Sydney Australia. Website
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http://www.acilallen.com.au/cms_files/ACILAllen_MLAPerfomance_2016.pdf,
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Alarcon-Rojo, A.D., Janacua, H., Rodriguez, J.C., Paniwnyk, L., Mason, T.J. (2015) Power
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ultrasound in meat processing. Meat Science, 107, 86-93. Alvez, Ld.L., Cichoski, A.J., Barin, J.S., Rampelotto, C., & Durante, E.C. (2013). O
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ultrassom no amaciamento de carnes. Ciência Rural, 43, 1522-1528. Arroyo, C., & Lyng, J. G. (2017). Electroprocessing of meat and meat products. In
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Cummins, E. J., & Lyng, J. G. (Eds.), Emerging Technologies in Meat Processing (pp. 103-130): John Wiley & Sons, Ltd., Chichester, West Sussex, UK. Arroyo, C., Eslami, S., Brunton, N. P., Arimi, J. M., Noci, F., & Lyng, J. G. (2015). An assessment of the impact of pulsed electric fields processing factors on oxidation, color, texture, and sensory attributes of turkey breast meat. Poultry Science, 94(5), 1088-1095. doi: 10.3382/ps/pev097 Arroyo, C., Lascorz, D., O'Dowd, L., Noci, F., Arimi, J., & Lyng, J. G. (2015). Effect of 45
ACCEPTED MANUSCRIPT pulsed electric field treatments at various stages during conditioning on quality attributes of beef longissimus thoracis et lumborum muscle. Meat Science, 99, 52-59. doi: 10.1016/j.meatsci.2014.08.004 Beilken, S. L., Macfarlane, J. J., & Jones, P. N. (1990). Effect of high-pressure during heattreatment on the Warner-Bratzler shear force values of selected beef muscles. Journal
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of Food Science, 55(1), 15-19. doi: DOI 10.1111/j.1365-2621.1990.tb06006.x
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Bekhit, A. E. D. A., Suwandy, V., Carne, A., van de Ven, R. V., & Hopkins, D. L. (2016b).
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Effect of repeated pulsed electric field treatment on the quality of hot-boned beef loins and topsides. Meat Science, 111, 139-146. doi: 10.1016/j.meatsci.2015.09.001
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Bekhit, A. E. D., Hopkins, D. L., Geesink, G., Bekhit, A. A., & Franks, P. (2014a). Exogenous proteases for meat tenderization. Critical Reviews in Food Science and
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Nutrition, 54(1012-1031).
Bekhit, A. E. D., van de Ven, R., Suwandy, V., Fahri, F., & Hopkins, D. L. (2014b). Effect
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of pulsed electric field treatment on cold-boned muscles of different potential
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tenderness. Food and Bioprocess Technology, 7(11), 3136-3146. doi: 10.1007/s11947-014-1324-8
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Bekhit, A. E. D. A., Suwandy, V., Carne, A., van de Ven, R., & Hopkins, D. L. (2016a). Effect of repeated pulsed electric field treatment on the quality of hot-boned beef loins
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ACCEPTED MANUSCRIPT Table 1: Description of changes in texture, shrinkage in muscle fibre and water loss over three temperature ranges being up to 62 oC (phase 1), 50-65 oC (phase 2, transition) and above 60 oC (phase 3).
Phase 2 – Transition between phase 1 and 3- 50-65 oC 50-65 oC 1, 2;
Toughening; 44 to 72
Tenderisation; 72 to
N1
55N1
35-55 oC; 20 to 49 N9
55-65 oC; 69-118 N9
Shrinkage in
Transverse; 35- 62 oC4
muscle fibre,
40-60 oC; 3-16%10
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direction and
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volume (%)
60-80 oC 1, 2, 3
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40-53 oC 1, 2, 3
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Texture
Phase 3 – Above 60 oC
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Phase 1- up to 62 oC
Toughening; 55 to 90N1
70-80 oC; 137-157 N9 Longitudinal; 65- 90oC4
65 oC; 20%10
70-95 oC; 28-46%10
50-56 oC; 22-28%5
58-62 oC; 34-35%5
64-70 oC – 38-41%5
during heating
40-55 oC; 2-5%6
60 oC; 9%6
70-80 oC; 16-33%6
45-55 oC; 5-10%7
65 oC; 18-23%7
75-85 oC; 23-35%7
55-60 oC; 15-20%8
65 oC; 24%8
75-105 oC; 30-43%8
65 oC; 20%10
70-95 oC; 28-44%10
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Water loss (%)
40-60 oC; 3-16%10
1
(Christensen, Purslow, & Larsen, 2000); 2 (Davey & Gilbert, 1974); 3 (Martens, Stabursvik,
& Martens, 1982); 4 (Bendall & Restall, 1983; Hearne, Penfield, & Goertz, 1978; Hostetler & Landmann, 1968; Palka & Daun, 1999; Purslow et al., 2016; Tornberg, 2005); 5 (Berhe, Engelsen, Hviid, & Lametsch, 2014); 6 (Tornberg, 2005); 7 (Martens et al., 1982); 8 (Purslow
71
ACCEPTED MANUSCRIPT et al., 2016); 9 (Bouton, Harris, & Ratcliff, 1981); 10 Bouton et al 1976 (Bouton, Harris, &
AC
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D
MA
NU
SC
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PT
Shorthose, 1976)
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Table 2: Description of the technologies high pressure processing, hydrodynamic shock wave, pulsed electric field, ultrasound, stretching including tenderstretch, smartstretch and PiVac, including first patent claiming tenderisation, first trial on meat, and the associated increase in
T P
I R
temperature of the product during application of the technology.
Description
tenderisation
High pressure processing,
100-600 MPa,
(McKenna, 2009)
Hydrostatic
High
wave)
D E
PT
E C
pressure, Detonation,
hydrodynamic
C S U
First Patent claiming First trial on meat for Increase
(Long, 1993)
C A
(shock electrically generated
M
temperature
during
application to meat (oC)*
N A
tenderisation
in
(Macfarlane, 1973)
3oC /100 MPa from adiabatic heating (US food and Drug Administration, 2014)
(Solomon, Long, & Detonation; 2-3oC* Eastridge, 1997b)
(Solomon, Sharma, & Patel, 2010) Electrical; negligible (Jim Claus, unpublished results).
Pulsed electric field
Electric pulses
(Long, 2000)
(O'Dowd
et
al., 5-30oC*
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ACCEPTED MANUSCRIPT 2013) Ultrasound
Low
(O'Dowd et al., 2013)
high (Guberman & Holt, (Dickens, Lyon, & 15-30oC*
or
frequency
1970)
(Jayasooriya, Torley, D’Arcy, et al.,
Wilson, 1991)
T P
2007) Tenderstretch
Stretch
pre-rigor (Stouffer, Buege, & (Hostetle.Rl,
muscles
on
the Gillis, 1971)
Smartstretch
Stretch
Fitzhugh, 1970) hot-boned (Pitt & Daly, 2010)
pre-rigor muscles PiVac
C S U
Landmann, Link, &
carcass
I R
negligible
Stretch
N A
(Simmons
et
al., negligible
2006)
D E
hot-boned (Meixner,
pre-rigor muscles
2004)
T P E
M
2001, (Sorheim & Hildrum, negligible 2002)
C C
*
Temperature rise depends on experimental parameters and conditions of application
A
Table 3: Summary of studies, total number of individual results tests within studies, species and muscles tested and source references. Where the pectoralis major muscle is specified, this refers to chicken or turkey only. This muscle was not included in any studies on pork, beef or sheep meat. Hence any effects of technologies on chicken or turkey meat refer specifically to the pectoralis major.
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Technology No. of – description of studie samples s included PEF – Pre-rigor
4
No. of resu lts within studies 114
Species
Muscles
References
Beef; Turkey
pectoralis major; longissimus; semimembranosus
Arroyo, Eslami, et al. (2015); (Arroyo, Lascorz, et al., 2015); Bekhit, Suwandy, Carne, van de Ven, and Hopkins (2016b); Suwandy, Carne, van de Ven, Bekhit, and Hopkins (2015b); Suwandy, Carne, van de Ven, Bekhit, and Hopkins (2015d) Arroyo, Eslami, et al. (2015); Bekhit, van de Ven, et al. (2014b); Bekhit et al. (2016b); Faridnia, Bekhit, Niven, and Oey (2014); Faridnia et al. (2015); Suwandy et al. (2015b); Suwandy, Carne, van de Ven, Bekhit, and Hopkins (2015a); Suwandy et al. (2015d) Bolumar, Bindrich, Toepfl, Toldra, and Heinz (2014); Bowker, Schaefer, Grapperhaus, and Solomon (2011); Claus et al. (2001b); James Claus (unpublished data)
PEF – Post-rigor
8
146
Beef
longissimus; semitendinosus; semimembranosus
Shock wave – Electrical
4
4
Shock wave Explosive
17
64
Beef; Turkey and Chicken; Pork Beef; Pork; Turkey and Chicken; Sheepmeat
Longissimus; pectoralis major; semitendinosus; semimembranosus; gluteus medius; adductor longissimus; adductor; pectoralis major; biceps femoris; semitendinosus; semimembranosus
D E
T P
I R
C S U
M
T P E
C C
A SmartStretch
6
12
Beef; Sheepmeat
N A
longissimus; gluteus medius; semimembranosus
Bowker, Callahan, and Solomon (2010); Bowker, Fahrenholz, Paroczay, Eastridge, and Solomon (2008); Bowker, Liu, et al. (2010); Callahan, Berry, Solomon, and Liu (2006); Claus et al. (2001a); Liu et al. (2006); Marriott, Wang, Solomon, and Moody (2001); Meek et al. (2000); Moeller et al. (1999); Schilling et al. (2002); Schilling, Marriott, Wang, and Solomon (2003); Solomon et al. (2008); Solomon, Long, and Eastridge (1997a); Spanier, Berry, and Solomon (2000); Zuckerman, Berry, Eastridge, and Solomon (2002); Zuckerman, Bowker, Eastridge, and Solomon (2013); Zuckerman and Solomon (1998) Taylor, Toohey, van de Ven, and Hopkins (2012a, 2013a); Toohey et al. (2012a); Toohey, van de Ven, Thompson, Geesink, and Hopkins (2012c, 2012b, 2013)
75
ACCEPTED MANUSCRIPT Technology No. of – description of studie samples s included Ultrasound
HPP – Pre-rigor
HPP – Post-rigor
6
5
18
No. of resu lts within studies 55
30
186
Species
Muscles
References
Beef; Sheepmeat; Chicken
longissimus lumborum; semitendinosus; semimembranosus; sternomandibularis; pectoralis major semitendinosus; psoas major; pectoralis minor; longissimus lumborum; biceps femoris; adductor; semimembranosus; glutius medius; triceps brachii longissimus lumborum; biceps femoris; semitendinosus; semimembranosus; pectoralis major; pectoralis profundus; psoas major; adductor; gluteus medius
Jayasooriya, Torley, D'Arcy, and Bhandari (2007); Lyng, Allen, and McKenna (1998b); Pohlman, Dikeman, and Zayas (1997); Pohlman, Dikeman, Zayas, and Unruh (1997); Sikes, Mawson, Stark, and Warner (2014); Stadnik and Dolatowski (2011); (Xiong, Zhang, Zhang, & Wu, 2012) Bouton, Ford, Harris, Macfarlane, and Oshea (1977); Bouton, Harris, and Macfarlane (1980); Bouton, Harris, Macfarlane, and O'shea (1977b); Macfarlane (1973); Souza et al. (2011)
Beef; Sheepmeat; Pork
Beef; Sheepmeat; Pork; poultry
A
C C
T P E
D E
T P
I R
C S U
M
N A
Beilken, Macfarlane, and Jones (1990); Bouton, Ford, Harris, Macfarlane, and Oshea (1977); Bouton et al. (1980); Bouton, Harris, et al. (1977b); (Del Olmo, Morales, Avila, Calzada, & Nunez, 2010); Duranton, Simonin, Cheret, Guillou, and de Lamballerie (2012); Hong, Shim, Choi, and Min (2008); Jung, De Lamballerie-Anton, and Ghoul (2000c); Jung, Ghoul, and de Lamballerie-Anton (2000a); Ma and Ledward (2004); Macfarlane (1973); Macfarlane and Mckenzie (1986); Macfarlane, Mckenzie, and Turner (1986); Macfarlane, Mckenzie, Turner, and Jones (1981); McArdle, Marcos, Kerry, and Mullen (2011); McArdle et al. (2013); Park, Ryu, Hong, and Min (2006); Ratcliff et al. (1977); Sikes and Tume (2014).
76
ACCEPTED MANUSCRIPT Table 4: Results of meta-analysis of the effect of technologies on the change in objective meat tenderness measurement, defined as peak shear force (N). The meat was variously from beef, sheep, pork and poultry and a range of muscles (see text and Table 3). The technologies included are pulsed electric field (PEF; applied to pre-rigor or post-rigor meat), shockwave (applied to post-rigor meat; electrical or explosive), SmartstretchTM (applied to pre-rigor
PT
meat), ultrasound (applied to pre-rigor meat) and high pressure processing (HPP; applied to
RI
pre-rigor or post-rigor meat). The ‘Effect’ is the effect of application of a technology on the
SC
peak shear force (N) relative to untreated meat. The SED is the standard error of the
NU
difference in PSF across all studies.
SED
MA
Effect
PEF Pre-rigor
0.52ns
-
Post-rigor
7.10***
interval
-0.76, 1.88
1.110
4.88, 9.28
0.444
6.67, 8.41
17.71***
2.145
12.91, 22.57
10.76***
3.537
3.203, 18.31
6.03***
1.388
3.246, 8.80
- Pre-rigor
82.30***
10.759
60.64, 104.14
- Post-rigor1
36.82***
4.306
28.33, 45.31
Shockwave Electrical
-
Explosive
Ultrasound
AC
SmartstretchTM
7.54***
CE
-
D
0.630
PT E
-
95% confidence
HPP
1
Treatments tested were across the range of pressures (HPP) 20-600 MPa and across the
temperatures 10-80 oC
77
ACCEPTED MANUSCRIPT *** P<0.001; ns not significant, P>0.05.
Table 5: Results of meta-analysis of the predicted change in peak shear force (N) as a result of the application of high pressure processing, relative to untreated controls. The data was grouped into three pressure ranges (Low, 20-150 MPa; Medium, 200-400 MPa; High, 520-
PT
600 MPa) and four temperature ranges (low, 10-30 oC; intermediate, 35-45 oC; high 50-60 oC;
RI
very high, 68-80 oC). Pressure, P<0.001; Temperature, :P<0.001, Pressure x Temperature,
SC
P<0.001. Average SED = 2.051.
NU
Temperature Ranges (oC)
35-45
50-60
68-80
53.1
57.81
110.3
MA
10-30 Pressure Range (MPa) -5.61
200-400
3.54
-1.3
4.13
-1.76
520-600
-27.93
13.46
3.12
-2.87
AC
CE
PT E
D
20-150
78
ACCEPTED MANUSCRIPT LIST OF FIGURES – Please note, two new figures have been inserted into the revised manuscript. These new figures are figures 2 and 3 below. Figure 1: Effect of heating bovine cold-shortened semitendinosus muscle blocks, for one hour in a water bath at temperatures 40, 50, 55, 60, 65, 70, 80, 90, 95 oC (±0.5 oC), on cook loss
PT
(%; LSD=1.6), length decrease (%; LSD=2.1), area decrease (%; LSD=4.4), volume decrease
RI
(%;LSD=2.4) and peak shear force (kg; LSD=0.86). Adapted from (Bouton et al., 1976).
SC
Figure 2: (A) Relationship between peak shear force (kg) and sensory tenderness scores in bovine longissimus thoracis et lumborum, predicted from peak shear force in 1-day aged (■)
NU
and peak shear force in 14-day aged (♦) meat. From Perry et al. (2001). (B) Relationship between peak shear force values (kg) and sensory tenderness ratings of bovine longissimus
MA
steaks by consumers at home and at a restaurant. No consumers at home gave a 1 rating. a,b,c,d Means in a dining environment with different superscripts are different (P < .05). From
PT E
D
Huffman et al. (1996).
Figure 3: Example of a pressure-phase diagram, showing a suggested extended phase
CE
diagram for the protein myoglobin. The diagram includes both the denaturation and aggregation phenomena, and therefore contains several metastable phases. The metastable
AC
phases are indicated in parentheses. N, native; D, denatured; A, aggregated; I, intermediate. From Smeller (2002).
Figure 4: Results of meta-analyses of the predicted change in peak shear force (N) in response to applications of ractopamine, zilpaterol and hormonal growth promotants (HGP) to beef cattle and the post-mortem application to various species (beef, sheepmeat, pork and poultry),to pre-rigor meat of smartstretch (Smartstetch), and to post-rigor meat of pulsed electric field (PEF-post-rigor), electrical shock wave (SW-electrical), ultrasound and to both 79
ACCEPTED MANUSCRIPT pre- and post-rigor meat of HPP (see Table 3, 4 and5 for sources, data and SED’s). The mean effect is shown and the vertical bar is the least significant difference (2 x SED).
Figure 5: Meta-analyses of the change in Warner-Bratzler peak shear force (N) of meat in response to applications of high pressure processing to different species (Species; beef,
PT
chicken, lamb and poultry) and different times post-mortem (pre-rigor vs post-rigor) (see
RI
Table 3, 4 and 5 for sources, data and SED’s). Species, P<0.001, average SED = 1.045; Time
SC
post-mortem, P<0.001, average SED=0.6413. The mean effect is shown and the vertical bar
NU
is the least significant difference (2 x SED).
Figure 6: The predicted change in peak shear force (N), relative to untreated controls, as a
MA
result of the application of high pressure processing. The data was grouped into three pressure ranges (Low, 20-150 MPa; Medium, 200-400 MPa; High, 520-600 MPa) and four
D
temperature ranges (low, 10-30 oC; Intermediate, 35-45 oC; high 50-60 oC; very high, 68-80
AC
CE
Average SED = 2.051.
PT E
oC). Pressure, P<0.001; Temperature, :P<0.0001, Pressure x Temperature, P<0.001.
80
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
Figure 1:
81
ACCEPTED MANUSCRIPT
NU
SC
RI
PT
(A)
AC
CE
PT E
D
MA
(B)
Figure 2:
82
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
Figure 3:
83
D
PT E
CE
AC
Figure 4: -10 0
-5
PT
RI
SC
NU
MA
Change in peak shear force (N)
ACCEPTED MANUSCRIPT
20
15
10
5
84
ACCEPTED MANUSCRIPT
30 25 20 15 10
PT
5 0 -5
RI
Change in peak shear force (N)
35
-10 Lamb
Pork
Prerigor
SC
Chicken
Postrigor
NU
Beef
AC
CE
PT E
D
MA
Figure 5:
85
ACCEPTED MANUSCRIPT
Legend: Change in peak shear force (N) from high pressure processing (HPP) application [HPP value minus non-HPP (control) value] -20-0
0-20
20-40
40-60
60-80
80-100
100-120
RI SC
Change in peak shear force (N)
PT
-40--20
120 100
60
NU
80
80 68
60 40
MA
20 0
-20 20
200
400
45 35 30
Temperature (oC)
10 520
600
Pressure (MPa)
CE AC
Figure 6:
PT E
D
-40
150
50
86