Ultrasonics in food processing – Food quality assurance and food safety

Trends in Food Science & Technology 26 (2012) 88e98

Review

Ultrasonics in food processing e Food quality assurance and food safety Jayani Chandrapalaa, Christine Oliverb, Sandra Kentishc and Muthupandian Ashokkumara,* a

School of Chemistry, University of Melbourne, Melbourne, VIC 3010, Australia (Tel.: D61 3 83447090; fax: D61 3 93475180; e-mail: [email protected]) b CSIRO Division of Food and Nutritional Sciences, 671 Sneydes Road, Werribee, VIC 3030, Australia c Department of Chemical and Biomolecular Engineering, University of Melbourne, VIC 3010, Australia In recent years, ultrasound technology has been used as an alternative processing option to conventional thermal approaches. Ultrasonication can pasteurize and preserve foods by inactivating many enzymes and microorganisms at mild temperature conditions, which can improve food quality in addition to guaranteeing stability and safety of foods. In addition, the changes to the physical properties of ultrasound, such as scattering and attenuation caused by food materials have been used in food quality assurance applications.

Ultrasound as a physical toolefood quality assurance Ultrasound has been used as a “scanning and imaging” tool in the medical field. The key concept of this application is the scattering and reflection of sound waves similar to light waves. In this application, low power/intensity, high frequency acoustic pulses are sent from a transducer. The * Corresponding author. 0924-2244/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.tifs.2012.01.010

reflected and scattered intensities of the acoustic pulses are then received by either the same transducer or a 2nd transducer, which can be used to construct the image of an object under investigation. A similar approach has been used in food quality assurance where scattered, transmitted and reflected acoustic pulses are used. Quality assurance is crucial for monitoring food processes and evaluating the final food products to ensure they are safe for consumption and meet consumer expectations with regard to organoleptic attributes and consistent quality. Low intensity, high frequency ultrasound used for detection purposes is typically <1 W/cm2 and >100 kHz. It is increasingly being used in the food industry where it can provide a rapid, accurate, inexpensive, simple and non-destructive method to assess and to monitor the properties of foods on-line during process operations (Berm
udez-Aguirre, Mobbs, & Barbosa-C
anovas, 2011; McClements, 1997). The structures and compositions of foods are an important determinant of their overall quality and cost. A plethora of studies have demonstrated the potential of ultrasound as an analytical tool for characterizing various properties of a range of foods. Examples include the composition of meat, meat products and fish (Benedito, Carcel, Rossello, & Mulet, 2001; Ghaedian, Coupland, Decker, & McClements, 1998; M€orlein, Rosner, Brand, Jenderka, & Wicke, 2005), sugar and alcohol content of beverages (Krause, Sch€ock, Hussein, & Becker, 2011), deterioration of edible oil during frying (Benedito, Mulet, Velasco, & Dobarganes, 2002), solid content of semi-crystalline fats (Coupland, 2004), mechanical properties of cheeses (Cho & Irudayaraj, 2003), sugar content of melon (Mizrach, Galili, Rosenhouse, & Teitel, 1991), solid fat index (McClements, 1997), fat droplet size distribution in homogenized milk (Miles, Shore, & Langley, 1990), variation in particle size distribution during instability of food emulsions (e.g. caused by sedimentation/creaming/shear) (Gan, Palla, & Hutchins, 2006), the size and shape of gas cells in bread (Elmehdi, Page, & Scanlon, 2003), and the volume fraction of some components in foods, such as fruit juices, syrups, and alcoholic beverages (Coupland, 2004). This application of ultrasound relies on there being a significant change in the acoustic properties (velocity, attenuation, impedance) of a food as its composition or structure varies. The larger the magnitude of the change, the more accurately the composition/structure can be determined.

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

Ghaedian et al. (1998) measured the ultrasonic velocity (at 4 MHz) of Atlantic cod fillets having various moisture contents between 78 and 82%. The ultrasonic velocity decreased linearly over the range 1575e1595 m/s with increasing moisture content, estimated to
1% weight. In a recent study, Camara and Laux (2010) showed that an ultrasonic (at 10 MHz) shear reflectivity method could distinguish between two honeys with a moisture content difference of <0.2% over the range 15e20% moisture. This technique also provided information on the honey microstructure as the temperature at which the vitreous plateau began could be related to relaxation times. The authors proposed the application of this technique for honey quality control. The advantage of this technique is that it is highly sensitive, non-destructive, requires little information about the honey and can potentially be applied directly to glass jars of honey with closed lids. Making use of the variation in ultrasound velocity (at 1 MHz) with temperature, Benedito, Carcel, Rossello et al. (2001) determined the chemical composition of fermented sausages containing various protein (221%), moisture (776%) and fat (290%) contents at two temperatures, 4 and 25  C. A variance of 85.4% for protein, 98.7% for moisture and 99.6% for fat was achieved. In another study, Ni~ noles, Mulet, Ventanas, and Benedito (2010) demonstrated the feasibility of using ultrasonic measurements (at 1 MHz) to characterize the melting behaviour of fat in Iberian dry-cured hams, and subsequently their related sensory attributes. Ultrasonic velocity strongly correlated (R2 ¼ 0.99) with the percentage of melted fat, demonstrating an increase of 5.4 m/s for a 1% increase in melted fat (% melted fat > 60%). Ultrasound is regarded as a useful tool to characterize tissue and evaluate animal carcasses. M€ orlein et al. (2005) classified animal carcasses based on intramuscular fat content by spectral analysis of ultrasound echo signals (at w3.5 MHz). In pigs, backfat thickness and longissimus muscle depth has been predicted using ultrasound scanning (at 3 MHz), as a prediction of meat yield (Cisneros et al., 1996). In poultry, breast muscle thickness, as determined by ultrasonography (at 7 MHz), was shown to be a reliable measurement of meatiness (Kleczek, Wawro, WilkiewiczWawro, Makowski, & Konstantynowicz, 2009). Ultrasound images (at 3e7.5 MHz) and body measurements of live animals have been employed to predict carcass traits of ducks (Farhat, 2009), sheep (Emenheiser, Greiner, Lewis, & Notter, 2010), cattle (Stelzleni et al., 2002) and catfish (Bosworth, Holland, & Brazil, 2001). The baking industry relies on the control of dough/batter
properties to achieve food quality and consistency. Alava et al. (2007) showed that ultrasonic measurements (velocity, attenuation) (at w100 kHz) could be successfully used to assess flour quality. The ultrasound parameters correlated with the rheological properties of doughs prepared from flours of a range of quality, showing that ultrasound may be a suitable measurement method to discriminate

89

types of flour for different applications. Other researchers found that acoustic impedance (frequency not provided) of cake batter provided a direct measurement of the gas
content in the batter (G
omez, Oliete, Garc
ıa-Alvarez, Ronda, & Salazar, 2008). The measurement was highly sensitive to incorporation of small amounts of air and provided improved correlation to the quality, with respect to physical properties, of the resulting cakes than conventional methods. Several researchers have shown the potential of ultrasonic techniques to characterize the structure of breadcrumb. By combining the results of both the attenuation and the velocity of the sound at 54 kHz, information on the porosity and the cell size and shape could be obtained (Elmehdi et al., 2003). Lagrain, Boeckx, Wilderjans, Delcour, and Lauriks (2006) employed non-contact ultrasonic techniques to characterize the porous structure of breadcrumb, and the phase velocity and attenuation measurements confirmed structural differences between two different bread types for a broad frequency range (40 kHz up to 1 MHz). Furthermore, non-contact ultrasound permitted estimation of flow resistance, open porosity and tortuosity of different crumb grain features. Crispness is a distinctive textural characteristic that signifies freshness and high quality in dry crisp and fried foods. Povey and Harden (1981) measured crispness of biscuits using the ultrasonic pulse echo technique (at 1.5 MHz) and found a good correlation (R2 ¼ 0.80e0.95) between the crispness from sensory measurement and the velocity of longitudinal sound. In the study of Antonova, Mallikarjunan, and Duncan (2003), mechanical and ultrasonic techniques were used to determine crispness in breaded fried chicken nuggets under different storage conditions. A pair of dry-coupling 250 kHz ultrasonic transducers was used to perform the ultrasonic transmission through the fried chicken nuggets. The ultrasonic velocity had high correlation with sensory crispness, indicating that sensory crispness could be reasonably well predicted by the ultrasonic velocity. One of the most promising applications of ultrasound in the food industry is as an on-line/in-line sensor to measure the properties of food materials during processing. By acquiring ultrasonic measurements in real time, composition can be adjusted, and/or process parameters modified, to optimize product quality. This on-line capability has been demonstrated, for example, by Choi, McCarthy, and McCarthy (2002), where ultrasonic velocimetry (UDV) measurements (at 5 MHz) were successfully used to determine the flow rate of tomato juice and corn syrup in pipes. As another example, ultrasonic pulsed echo Doppler-pressure differences (UVP-PD) (using four ultrasonic transducers, 24 MHz), in combination with in-line rheological measurements, was applied to successfully determine the concentration of solids in various highly concentrated, bimodal and polydisperse model and industrial food suspensions (tomato, vegetable and pasta sauces, seafood chowder, strawberry yoghurt, cheese sauce with vegetables) (Wiklund & Stading, 2008).

90

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

Low intensity ultrasound (at 1 MHz) has been used successfully to monitor different stages of the cheese manufacturing process (Benedito, Carcel, Gonzalez, & Mulet, 2002). The ultrasonic parameters (attenuation, velocity) were used to determine the optimal renneting time, by relating ultrasonic variables to enzyme activity in milk during coagulation, and to indicate the maturation degree of cheeses. In a similar manner, the propagation of ultrasound waves (at 1 MHz) through tofu has been used to monitor the development of tofu texture during gelation, allowing the assessment of the quality of tofu during its manufacture (Ting, Kuo, Lien, & Sheng, 2009). Recently, Telis-Romero, V
aquiro, Bon, and Benedito (2011) proposed a method to estimate the fat and moisture content of fresh and blended cheeses from measurements of acoustic velocity at 1 MHz and various temperatures ranging from 3 to 29  C. Since the ultrasonic measurements could be performed during the cooling process, subsequent to curdling, this approach has potential use as a food quality control tool to detect process anomalies during production of cheese on-line. Characterizing the fermentation process is essential to control and improve the quality of the final product during the manufacture of alcoholic drinks and bread. In a recent study, Skaf, Nassar, Lefebvre, and Nongaillard (2009) designed a non-destructive acoustic sensor suitable to monitor the kinetics of bread dough fermentation by ultrasound (w4146 kHz). The device was also sensitive to the influence of the technological parameters of temperature and nature of the ingredients. Such an approach has potential as an effective on-line monitoring and quality control technique in dough fermentation that may also be applicable to processes that involve other complex viscoelastic media. Resa, Elvira, de Espinosa, Gonz
alez, and Barcenilla (2009) assessed the potential of on-line ultrasonic velocity measurements (at 1, 2 and 4 MHz) to monitor alcoholic fermentation and the contributions of gas production, microorganism growth, polysaccharide hydrolysis and monosaccharide catabolism in synthetic broths (glucose, fructose, sucrose) and natural media (wort, must). In a recent study, Sch} ock and Becker (2010) established a polynomial approach to simultaneously determine the sugar and ethanol concentration in industrial fermentation fluids based on measurement of acoustic velocity using the pulse echo method (centre frequency w2 MHz). It also offers the possibility to reach high accuracy (0.22% deviation) with minimal experimental effort and low cost. Aboonajmi et al. (2010) applied an ultrasonic technique as a non-destructive and non-invasive means of evaluating the quality of commercial poultry eggs during different storage conditions, by calculating the ultrasound phase velocity (at 150 kHz) within the egg material. The decrease in mean value of the phase velocity during storage correlated with the change in well-known quality parameters of eggs determined by conventional destructive techniques used to measure egg freshness. The results showed the potential of ultrasound phase velocity to recognize

differences between fresh and aged eggs up to 3 weeks after the eggs were laid. Low intensity ultrasound (50 or 100 kHz) has been used to assess the quality of various fruits and vegetables, including apples (Kim, Lee, Kim, & Cho, 2009), tomatoes (Mizrach, 2007), carrots (Nielsen, Martens, & Kaack, 1998), avocadoes, mangoes and melons (Mizrach, 2000), according to ripeness/texture/firmness. This was achieved by evaluating ultrasound parameters (velocity, attenuation) in relation to the physical characteristics (texture/firmness, total soluble solids, dry weight, and acidity) of the produce. Microbial quality control is an important stage of the production chain for many food products in which biological contamination would have adverse effects on food quality. Acoustic streaming induced by ultrasound in a liquid is affected by the microbial activity, and thus, bacteria that alter the physicochemical parameters of a liquid (e.g. viscosity, elasticity) can be detected through the use of ultrasonic waves (Elvira et al., 2006). Elvira et al. (2006) designed an 8-channel non-invasive ultrasonic device suitable for monitoring microbiological contamination of aseptically packaged milk. The amplitude and time-of-flight measurements at 800 kHz constituted a signature of the presence of a microorganism, with similar trace behaviours for bacteria originating from the same family. They showed that ultrasonic detection could occur even prior to the occurrence of physicochemical changes. Foreign bodies (e.g. glass, metal, plastic), suspended particles (e.g. microorganisms) or internal structural defects (e.g. holes, cracks) in foods are a hazard and quality assurance issue for many food manufacturers. Typical foreign body detection methods used by the food industry include optical inspection, metal detection, and X-rays. Many of these techniques suffer from limitations in the range of foreign bodies that they can detect. Ultrasound is a promising alternative, due to its ability to detect changes in acoustic impedance (Z ) between different regions within a given volume. Low intensity ultrasound-based techniques are able to detect and identify foreign bodies in a range of food products, including cheese (Benedito, Carcel, Gisbert, & Mulet, 2001), poultry (Correia, Mittal, & Basir, 2008), bottled beverages (Zhao, Basir, & Mittal, 2003), and yogurt, fruit juices and tomato ketchup (Knorr, Zenker, Heinz, & Lee, 2004). Knorr et al. (2004) used ultrasonic signals in a time-frequency analysis to detect and identify standard foreign materials, as well as raw material contaminants (kernels imbedded in cherry flesh), in various food products. Hæggstr}om and Luukkala (2001) detected a variety of foreign materials (bone, stone, wood, glass, plastic) in plastic-packaged cheeses using a piezoelectric transducer operating at a frequency of 5 MHz. Experiments were conducted in a water tank with pulse echo mode. The sensitive, non-destructive approach was feasible for use in homogenous products to a probe depth of 20e75 mm. Ultrasonic pulse compression (UPC) is used to detect foreign objects in contained foods,

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

consistency of some liquids, and discrepancies in liquid levels in polymer-based beverage bottles (Berm
udezAguirre et al., 2011).

Food safety (microbial and enzyme inactivation) The food industry has typically relied on heat to inactivate microorganisms and enzymes as a means of food preservation, despite the thermal treatment inactivates enzymes, kills vegetative microorganisms and destroys some spores, and causes loss of the nutritional and organoleptic properties of food products. The main mechanism responsible for the ultrasonic deactivation effect is the physical forces generated by acoustic cavitation. The asymmetric collapse of a cavitation bubble leads to a liquid jet rushing through the centre of the collapsing bubble. The speed of this microjet is a few hundred metres per second. Due to this high speed jet, pitting on solid surfaces has been observed. Microorganisms may have hydrophobic surfaces, which will promote the collapse of the cavitation bubbles on the surface leading to severe damage to the cell wall. Similarly, the microstreaming can lead to the erosion of cell walls, resulting in the inactivation of the microorganisms. In addition to the cavitation effects discussed above, the bactericidal effect of ultrasound in liquid foods is also attributed to intracellular cavitation (Hughes & Nyborg, 1962), which disrupts the structural and functional components up to the point of cell lysis. The effects of localized heating, free radical production causing DNA damage, and microstreaming, which causes thinning of cell membranes, are crucial in the inactivation (Berm
udez-Aguirre et al., 2011). Resistance of the different microorganisms to ultrasound varies widely. In addition, many process and treatment parameters affect ultrasound output and consequently its effect on microorganisms in liquid media. Critical processing factors include the properties of the medium, treatment parameters and ultrasound parameters. It has been suggested that the interactions between these parameters are highly complex. Earnshaw (1998) cites research that suggests large cells, such as yeast (520 mm), are more susceptible to the effects of cavitation, due to having a larger surface area than smaller sized cells. In general, spores of bacteria (e.g. Bacillus and Clostridium spp.) are more resistant to cavitational effects than vegetative cells, which are in growth phase. Fungi are generally more resistant than vegetative microorganisms, aerobes more resistant than anaerobes, and cocci typically more resistant than bacilli, due to the relationship of cell surface and volume. The bactericidal efficiency of ultrasound on Gram-positive versus Gram-negative bacteria is controversial. Some studies report Gram-positive bacteria to be more resistant to cavitation than Gram-negative bacteria (Villamiel & de Jong, 2000), while others found no significant differences in their resistance to inactivation by ultrasound (Scherba, Weigel, & O’Brien, 1991).

91

Intense ultrasound power and long contact times are required to inactivate microorganisms when ultrasound (at ambient conditions) is applied alone, especially for microbial inactivation in real food systems. For instance, the decimal reduction time value (D value) of vegetative Staphylococcus aureus treated with ultrasound (150 W, 20 kHz) took 187 min at w14  C when the microorganism was suspended in UHT milk (Ord
o~nez, Aguilera, Garcia, & Sanz, 1987). In contrast, when suspended in phosphate buffer the D value was 5 fold lower, being 36.5 min at 11  C. The differences in amount of inactivation achieved between buffers and foods have been attributed to several factors, such as aw, pH, viscosity, and food composition (Bermudez-Aguirre, Mawson, Versteeg, Narbosa-Canovas, 2009). The rate at which ultrasound (85 W/cm2, 24 kHz, 100 mm amplitude, pulsing at 80%) inactivated Escherichia coli and Listeria monocytogenes in whole and skim milk compared to phosphate buffer was recently reported by Gera and Doores (2011). Among the milk components tested, lactose was found to exert a maximum protective effect on the bacteria. The results suggested that either stabilization of the bacterial membrane and proteins by lactose, or accumulation of compatible solutes in the presence of lactose, possibly resulted in the observed increase in resistance of the bacteria to sonication. Berm
udez-Aguirre and Barbosa-C
anovas (2008) found that an increase in butter fat content of milk (fat-free, 1%, 2% and whole milk) increased the resistance of Listeria innocua against ultrasound (400 W, 24 kHz) performed at 63  C for 30 min. It was possible that the bacteria adhered to the surface of the newly formed milk fat globules and were protected either by the rough surface of the fat globules or by concealment within the globules that were disturbed with ultrasound, providing a protective fat layer against the heat and cavitation generated with the sonication. Current research to enhance microbial inactivation in food by ultrasound is focused on either exploring the selection of ultrasound processing variables to increase cavitation phenomenon and the energetics of bubble collapse, or combining ultrasound with other preservation factors (Knorr et al., 2004). Studies suggest that osmosonication may be a potential alternative to thermal stabilization processes for producing high quality juice concentrates. Osmosonication describes the combination of ultrasound treatment of a medium and its subsequent storage at high osmotic pressure. Wong, Vaillant-Barka, and Chaves-Olarte (2010) showed that osmosonication enhanced membrane damage and viability loss of Salmonella spp. in orange juice. Sonication of orange juice (50 W, 20 kHz, 25  C), combined with its subsequent concentration and storage (48 h) at high osmotic pressure (10.9 MPa) reduced Salmonella spp. by 5 log. Moreover, sonication did not affect the key physicochemical and functional attributes of the juice. However, the most effective sonication approaches to inactivate microbes for industrial purposes is the combination of ultrasound with heat (thermosonication, TS), pressure

92

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

(manosonication, MS), or heat and pressure (manothermosonication, MTS). Several studies have shown an additive or even synergistic effect of TS, MS and MTS compared to the individual treatments alone (Knorr et al., 2004). For example, Czank, Simmer, and Hartmann (2010) found TS treatment was considerably more effective (E. coli D45  C ¼ 1.74 min, D50  C ¼ 0.89 min; Saccharomyces epidermidis D45  C ¼ 2.08 min, D50  C ¼ 0.94 min) than ultrasound (150 W, 20 kHz) treatment alone (E. coli D4  C ¼ 5.94, S. epidermidis D4  C ¼ 16.01 min) for inactivation of E. coli and S. epidermidis in human milk. The enhanced lethality of microorganisms by TS, MS and MTS is generally ascribed to a greater mechanical disruption of cells, increasing their susceptibility to the effects of cavitation. The advantage is a decrease in the process temperatures and/or times required to achieve microbial inactivation. For example, Lee, Zhou, Liang, Feng, and Martin (2009) compared the effect of sonication, TS, MS and MTS (20 kHz, 124 mm amplitude) at 40, 47, 54, and 61  C and 100, 300, 400, and 500 kPa, on inactivation of E. coli in phosphate buffer (0.01 M, pH 7). They showed that the combination of lethal factors (heat and/or sonication, with and without pressurization) significantly shortened the treatment time necessary to achieve a 5 log reduction. The inactivation rates of E. coli by TS and MTS were significantly higher than those by sonication and MS. Thermosonication is considered to increase the lethality values of conventional pasteurization and sterilization treatments of liquid foods. Reports have indicated that TS treatments also lower maximum processing temperatures by 25e50%. Furthermore, the reduction in temperature and/or process time is expected to improve retention of the nutritional and organoleptic quality of food (Ord
o~ nez et al., 1987). Ugarte-Romero, Feng, Martin, Cadwallader, and Robinson (2006) found combined ultrasound (20 kHz, 0.46 W/mL, up to 20 min) and heat was effective for inactivation of E. coli in apple cider, especially at sub-lethal temperatures (40, 45 and 50  C), compared to thermal treatment alone. Moreover, the quality parameters of the cider were not considerably affected by ultrasound treatment. Similar findings were reported for thermosonicated (20 kHz, 40100% amplitude, pulsed 5 s on and 5 s off for 210 min) orange juice with minimal (Tiwari, Muthukumarappan, O’Donnell, & Cullen, 2008a) or even enhanced (Zenker, Heinz, & Knorr, 2003) (19.3 kHz, 45 and 55 mm amplitude) effect on juice quality. The quality of thermosonicated (20 kHz, 40100% amplitude, pulsed 5 s on and 5 s off for 210 min) strawberry (Tiwari, O’Donnell, Patras, & Cullen, 2008b) juices also remained largely unaltered. In another study, TS (400 W, 24 kHz, 63  C, 30 min) was reported to be a viable option for pasteurization of milk (Berm
udez-Aguirre & BarbosaC
anovas, 2010). Additionally, the TS treated milk improved the quality, shelf-life and yield (20.6%) of a cheese produced downstream (Berm
udez-Aguirre & Barbosa-C
anovas, 2010). Berm
udez-Aguirre et al. (2009) compared conventional batch pasteurization (63  C, 030 min) with TS (400 W,

24 kHz, 63  C, 030 min) inactivation of L. innocua and mesophilic bacteria in raw whole milk. Thermal pasteurization resulted in 0.69 log and 5.5 log reductions for 10 and 30 min treatments, respectively. With a combination of ultrasound (60, 90 or 100% of 400 W) and heat (63  C) a 5 log reduction was achieved after just 10 min, and a synergistic rather than additive effect was observed. Furthermore, the thermosonicated milk had improved whiteness and similar physicochemical properties compared to the conventionally pasteurized milk. In the case of watermelon juice, however, TS (24 kHz, 24.4, 42.7 and 61 mm amplitude, 210 min, 2545  C) significantly decreased the ascorbic acid, lycopene and total phenolic content at increasing amplitude levels and maximum processing time (Rawson et al., 2011). For example, the retention of total phenolic content was 83%, 63%, 41% at 45  C, 61 mm for respective processing times of 2, 6 and 10 min. Similarly, G
omez-L
opez, Orsolani, Mart
ınez-Y
epez, and Tapia (2010) found that the ascorbic acid content of Ca fortified orange juice decreased with sonication (20 kHz, 89.25 mm amplitude, 10  C, up to 10 min) in a time-dependent manner. Thus, optimization of the TS conditions is essential to ensure microbial food safety without compromising the quality of the food. In addition to liquid foods, TS treatments have also been investigated for microbial inactivation on solid food surfaces. Cabeza, Ord
o~nez, Cambero, de la Hoz, and Garc
ıa (2004) reported that combined ultrasound (24 kHz, 400 W) and heat (5258  C) enhanced the killing rate of a Salmonella enterica strain on intact egg shells, compared to heat treatment alone. The treatment process yielded a product that not only reduced the salmonellae to a safe level but had negligible damage to the thermolabile egg components. Haughton et al. (2010) found that Campylobacter jejuni was more susceptible to TS (24 kHz, 53  C) than to sonication or thermal treatment alone, with respective mean inactivation of 4.7, 3.2 and 1.5 log10 colony forming units per mL. However, the effectiveness of sonication and TS generally decreased when similar treatments were applied to inoculated poultry products (Haughton et al., 2010). In recent studies, TS has been combined with other emerging technologies for improved microbial inactivation. In particular, several studies have reported the beneficial effect of combining TS with pulsed electric field (PEF). For instance, Noci, Walkling-Ribeiro, Cronin, Morgan, and Lyng (2009) reported on the inactivation of L. innocua in low-fat UHT milk pre-heated to 55  C (>60 s) by combined TS (24 kHz, 400 W, 80 s) and PEF (40 kV cm1). Cell death number by TS-PEF was similar to that achieved by conventional pasteurization. In addition, the TS treatment substantially decreased the severity of the temperature/time exposure over thermal treatment alone. Similar findings were reported by Walkling-Ribeiro, Noci, Cronin, Lyng, and Morgan (2009) for TS-PEF treatment (30 kHz, 55  C, 10 min) of orange juice. The potential for selective inactivation of microorganisms by TS offers promise for pasteurization of fermented

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

foods (e.g. yogurt) whilst retaining the viability of probiotic cultures contained within the products (Knorr et al., 2004). For instance, Zenker et al. (2003) studied the effects of TS (20 kHz, 4860  C) versus heat treatment alone (5668  C) on the inactivation of Lactobacillus acidophilus and E. coli in phosphate buffer (pH 7) in a batch-type reactor. Thermosonication at 60  C resulted in an almost 6 log reduction in E. coli within 2 min compared to a 2 log reduction for ultrasound (28  C) or heat treatment (60  C) alone. A comparison of the improved effectiveness of TS over heat treatment alone on inactivation of the microorganisms revealed that L. acidophilus was more resistant to TS than E. coli. Additionally, a continuous flow treatment system was shown to afford at least a 1.7 fold (E. coli) to 1.4 fold (L. acidophilus) reduction of the process time, or approximate 1.07 fold (E. coli) to 1.03 fold (L. acidophilus) reduction in process temperature, in several liquid foods, such as fruit juices and milk (Zenker et al., 2003). Despite its benefits, the effectiveness of TS decreases with increasing temperature. Ugarte-Romero, Feng, and Martin (2007) reported an upper limit temperature of 65  C for enhanced inactivation of L. monocytogenes by TS (1000 W, 22.3 kHz), whereas at sub-lethal temperatures, an increase in volumetric acoustic energy density (0.49, 0.85 and 1.43 W/mL) increased the rate of inactivation of both Shigella boydii and L. monocytgenes. Guerrero, L
opez-Malo, and Alzamora (2001) reported a synergistic effect between ultrasound (20 kHz, 71110 mm amplitude) and heat (35 and 45  C) on inactivation of Saccharomyces cerevisiae in Sabouraud broth at pH 3 and 5.6. However, this was only observed at sub-lethal temperatures (<55  C), where the rate of yeast inactivation increased exponentially with increase in ultrasonic wave amplitude (Guerrero et al., 2001) (Fig. 1). The decrease in effectiveness of TS at increasing temperature is due to a reduction in the cavitation effect as a result of the increase in vapour pressure and the decrease in liquid surface tension (Villamiel & de Jong, 2000). However, this effect can be overcome by MS or MTS. Manosonication/manothermosonication, the simultaneous application of ultrasound under pressure (up to 600 kPa), enables cavitation to be maintained at temperatures above boiling point, substantially increasing the efficiency of microbial inactivation by ultrasound. Whilst there are numerous literature reports on the antimicrobial action of MS/MTS in model systems, few studies have been conducted on real food systems. Huang, Mittal, and Griffiths (2006) reported a combination of high hydrostatic pressure (HHP) (2  24 cycles at 138 MPa) and ultrasound (34.6 W, 20 kHz, 55  C, 5 min) resulted in the greatest inactivation (3.2 log cycle reduction) of Salmonella enteritidis in liquid whole egg, over PEF, HHP, and ultrasound alone, and various combinations thereof, although no synergy was observed. Arroyo, Cebri
an, Pag
an, and Cond
on (2011) investigated several environmental factors and process parameters with respect to inactivation of

93

Fig. 1. Survival curves of Saccharomyces cerevisiae during ultrasonic treatments in Sabouroud broth at pH 5.6. Wave amplitude: 71.4 (A); 83.3 (-); 95.2 (); and 107.1 (C) mm (pH 5.6): (a) 35  C; (b) 45  C; and (c) 55  C. Error bars represent standard deviations. Predicted values using first order model, d. (No: initial number of yeast cells and N: survival yeast count, CFU/ml) (Guerrero et al., 2001).

Cronobacter sakazakii with MS in buffer and various food products. Although cell resistance to MS (450 W, 20 kHz, 117 mm amplitude, 200 kPa, 35  C) was higher when the cells were treated in food products, the D values were always < 2.5 fold higher than those for treatment in citrate-phosphate buffer, pH 7.

94

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

The efficacy of MS is not significantly influenced by environmental factors. Thus, the advantage of MS over heat for bacterial inactivation increases as the protective effects of environmental factors on microbial heat resistance increases (Arroyo et al., 2011). It is also recognized that the lethality is scarcely modified by an increase in temperature unless lethal temperatures are reached. For most vegetative cells the lethal effect of MTS is additive, whilst a synergistic effect on spore-forming bacteria, including Bacillus coagulans, Bacillus cereus, Bacillus sterothermophilus, Bacillus subtilis, Enterococcus faecia, Sacillus cerevisiae and Aeromonas hydrophilia, has been observed (Pag
an, Ma~ nas, Alvarez, & Cond
on, 1999; Raso, Pag
an, Cond
on, & Sala, 1998). For instance, treatment of B. subtilis spores to MTS (200 kHz, 117 mm amplitude, 300 kPa) at 55 and 70  C resulted in only 20% spore survival, whereas there was 100% survival by heat alone at comparable temperatures (Raso et al., 1998). The authors also found that MTS (300 kPa) at 112  C increased the lethality of B. coagulans, B. cereus and B. sterothermophilus by 10 fold compared to non-pressurized controls. The increased sensitivity of bacterial spores to MS and MTS was confirmed by comparative visualization of the effects of ultrasound, MS and MTS on the physical structure of spores, using phase contrast microscopy (Raso et al., 1998). Whilst the heat only treated cells maintained full integrity, the MS treated cells were completely broken and the MTS cells were moderately disrupted. These results confirmed that ultrasound inactivates microbial cells through envelope breakdown. The advantage of MTS is that, in contrast to heat, the damage to the cells is irreversible (Pag
an et al., 1999). This is due to intense vibration and cavitation experienced by cells exposed to MTS, which causes violent shaking of the cells. Thermo-resistant enzymes, such as lipases and proteases that withstand UHT treatment, can reduce the quality and shelf-life of heat-treated milk and other dairy products. However, such enzymes have been efficiently inactivated at 10 fold the rate of thermal treatment alone, by MTS (20 kHz, 145 mm amplitude and 650 kPa for protease, 117 mm amplitude and 450 kPa for lipase, 109140  C) treatment (Vercet, Lopez, & Burgos, 1997). Other literature examples of enzymes inactivated by MTS include horseradish peroxidase & soybean LOX (L
opez et al., 1994), tomato pectic enzymes (Raviyan, Zhang, & Feng, 2005), polyphenol oxidase (PPO), lipase and protease (Raso & BarbosaC
anovas, 2003). MTS is a potential alternative to heat treatment in processing of milk and other beverages of neutral pH and liquid eggs. The main limitation of MTS could be its impact on the nutritional and physicochemical properties of the food. For instance, Caminiti et al. (2011) investigated the impact of selected combinations of non-thermal processing technologies on the quality of an apple and cranberry juice blend. Sensory analysis showed that UV þ PEF and high intensity light pulsing þ PEF combinations did not impact on odour and flavour of the juice, while combinations that

included MTS (750 W, 20 kHz, 5 bar, 43  C) adversely affected those attributes. However, research data on sensory aspects of MTS treated foods is limited and therefore general conclusions cannot be drawn. A plethora of literature studies have demonstrated the potential of ultrasound to inactivate food enzymes. Most of these enzymes have been studied in model systems, whereas investigations in real food systems are limited (Table 1). General trends that were observed from all these studies were that thermolabile enzymes were more sensitive to ultrasonication than heat-resistant enzymes. Furthermore, the stabilization mechanism that operates during heat treatment does not protect enzymes against MTS treatments (unlike that which occurs to microorganisms). Molecular size and structure are thought to play a role in the sensitivity of enzymes to MTS, with large and less globular enzymes displaying more sensitivity (Vercet, Burgos, Crelier, & Lopez-Buesa, 2001). It is important to appreciate that the effects of ultrasound on enzyme activity include inactivation and activation. According to the literature, inactivation of monomeric enzymes generally involves either defragmentation of the enzyme or formation into aggregates (Mawson, Gamage, Terefe, & Knoerzer, 2011), whereas polymeric enzymes tend to fragment into monomeric subunits, during ultrasonication. Inactivation of enzymes by ultrasound is primarily attributed to cavitation phenomenon. Indeed, the cavitation effects generated by bubble collapse (mechanical, thermal, chemical) may be sufficient to cause irreversible destruction and deactivation of enzymes (Mawson et al., 2011). In addition, the extreme agitation created by microstreaming could disrupt Van der Waals interactions and hydrogen bonds in the polypeptide, causing protein denaturation (Tian, Wan, Wang, & Kang, 2004). Most likely more than one mechanism is operative. For instance, free radical mediated deactivation of lipoxygenase (LOX) by MTS has been suggested (Lopez & Burgos, 1995) and possibly protein denaturation. Splitting of the heme group from peroxidase by MTS was reported to inactivate the enzyme (L
opez et al., 1994), whereas the inactivation of trypsin has been partly attributed to the large interfacial area created by ultrasound, which disrupts hydrophobic interactions and hydrogen bonds (Tian et al., 2004). Generally, ultrasonication in combination with other treatments is more effective in enhancing the enzyme inactivation efficacy. In particular, simultaneous application of low intensity ultrasound and mild heat (TS) and/or pressure (MS, MTS) is reported to increase the effectiveness of inactivation of various enzymes in food. Nevertheless, the sensitivity can vary between enzymes. For instance, a synergistic effect of combined ultrasound (20 kHz, 65 mm amplitude) and heat (5075  C) on inactivation of pectin methylesterase (PME) and polygalacturonase (PG) in tomato juice was reported by Terefe et al. (2009). Thermosonication increased the inactivation rate of PME by 1.5e6 fold and that of PG by 2.3e4 fold over 6075  C,

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

95

Table 1. Select literature examples of application of ultrasound to inactivate enzymes in real food systems. LOX [ lipoxygenase; MTS [ manothermosonication; PG [ polygalacturonase; PME [ pectin methylesterase; PPO [ polyphenol oxidase; TS [ thermosonication. Target enzyme

Food matrix

Approach

Comments

Reference

PPO

Guava juice

Ultrasound/ carbonation

Cheng, Soh, Liew, & The, 2007

Peroxidase

Watercress

TS

Peroxidase

Seedless guava

TS

Peroxidase PPO

Fresh-cut ‘Fuji’ apple

Ultrasound/ ascorbic acid

PG PME

Tomato juice

TS

LOX

Soy flour suspension

Ultrasound

PME

Orange juice

Ultrasound

PME

Orange juice

MTS

PG PME

Tomato paste

MTS

PG PME

Tomato juice

TS

Sonication (35 kHz, 30 min) increased PPO activity (18 U) in guava juice, compared to juice without ultrasound treatment (10 U). The activity of PPO was further increased (20.1 U) by combining sonication with carbonation, where the carbonated juice without ultrasound had a PPO activity of 11 U. Ultrasound (20 kHz at 50% power) at temperatures gt; 85  C at comparable blanching times, led to higher enzyme inactivation over heat blanching alone. Application of ultrasound (20 kHz) at high temperatures (8095  C) promoted enzyme inactivation at a higher rate compared to hot water blanching alone, at comparable temperatures. Combined ultrasound (40 kHz) and ascorbic acid (1%) treatment had a synergistic inhibitory effects on monophenolase, diphenolase and peroxidase, during storage (10  C, 012 d), whereas the individual treatments had inverse and limited inhibitory effects on the enzymes. Combined ultrasound and heat (20 kHz, 65 mm, 6075  C) had a synergistic effect on the inactivation rates of both PME (by 1.5e6 times) and PG (by 2.3e4 times), with the highest increase corresponding to the lowest temperature. LOX inactivation was influenced by exposure time, pH and amplitude of ultrasound, with pH being the most important factor. Sonication (20 kHz, 22  C, 3 h) at pH >5 had no effect on LOX activity, but 7085% of LOX was inactivated by sonication at pH 4 and 5, respectively. LOX activity also decreased with an increase in wave frequency (40 and 50 kHz) when pH  5, Above pH 5, an increase in frequency did not affect LOX activity after exposure time of 1 h. Ultrasound (20 kHz) at various acoustic density levels (0.42, 0.47, 0.61, 0.79 and 1.05 W/ml) and treatment times (0, 2, 4, 6, 8 and 10 min) were investigated at < 45  C. The highest PME inactivation was 62% for sonication at 1.05 W/ml and 10 min. Combined ultrasound (20 kHz, 117 mm), heat (72  C) and pressure (200 kPa) increased the enzyme inactivation rate 25 times in citrate buffer (5 mM, pH 3.5) and >400 times in orange juice, over heat treatment alone. MTS (20 kHz, 2 kg pressure, 117 mm, 70  C, 1 min) completely deactivated PME, whereas heat alone at comparable temperature/ time decreased the initial PME activity by 38%. Furthermore, MTS decreased the total PG activity by 62%, whereas heat alone at comparable temperature/time had no affect. TS treatments (24 kHz, at 25, 50 and 75 mm at 60, 65 and 70  C) were compared to heat only treatments. TS at 60, 65 and 70  C for 41.8, 11.7 and 4.3 min exposure, respectively, decreased PME activity by 90%. Heat alone at 60, 65 and 70  C required 90.1, 23.5 and 3.5 min, respectively to inactivate PME by 90%.

with the highest increase corresponding to the lowest temperature (Terefe et al., 2009). Wu, Gamage, Vilkhu, Simons, and Mawson (2008) also found a beneficial effect of TS (24 kHz, 6065  C) on rate of inactivation of PME in tomato juice compared to thermal treatment alone. However, at 70  C, ultrasound was not effective, and this was attributed to impairment of cavitation at this temperature (Wu et al., 2008). Ercan and Soysal (2011) showed that TS (23 kHz, 6367  C, 20150 s) at different power levels (1575%, corresponding to 315 mm amplitude) caused partial to full inactivation of tomato peroxidase at a much

Cruz, Vieira, & Silva, 2006 Ganjloo et al., 2008

Jang & Moon, 2011

Terefe et al., 2009

Thakur & Nelson, 1997

Tiwari, Muthukumarappan, O’Donnell, & Cullen, 2009 Vercet, Lopez, & Burgos, 1999

Vercet, Oria, Marquina, Crelier, & Lopez-buesa, 2002

Wu et al., 2008

faster rate than heat alone. An increase in power increased the enzyme inactivation rate. Thermosonication at 50% power (i.e. 10 mm amplitude) for 150 s and 75% power (i.e. 15 mm amplitude) for 90 s fully inactivated the enzyme (Ercan & Soysal, 2011). Ganjloo, Rahman, Bakar, Osman, and Bimakr (2008) compared ultrasonic blanching (20 kHz, 25% power, 8095  C) with hot water blanching and found the combined treatment provided a more rapid and effective inactivation of seedless guava peroxidase at comparable temperature and time. Similarly, TS (150 W, 20 kHz, 120 mm amplitude, 30e75.5  C, 40.2e102.3 s) was

96

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

reported to be more effective at inactivating milk enzymes (alkaline phosphatase, lactoperoxidase and g-glutamyltranspeptidase) than heat alone. The extent of inactivation, however, was both enzyme and media specific (Villamiel & de Jong, 2000). The demand for food safety is projected to rise 8.1% annually. The major trends, reacting to consumers’ needs in the future, are towards the use of procedures that deliver food products that are less ‘heavily’ preserved, higher quality, more convenient, more ‘natural’, freer from additives, nutritionally healthier, and still with high assurance of microbiological safety. Ultrasound is a non-destructive targeted technique without introducing preservatives. Conclusion Scattered, transmitted and reflected acoustic pulses are used in food quality assurance. Enzymatic inactivation for quality preservation is a requisite for stabilization of some food materials. The chemical (free radical production, hot spots) and physical forces (micro-streaming) generated by acoustic cavitation promotes severe damage to the cell wall, resulting in the inactivation of the microorganisms. In addition to the cavitation effects, the bactericidal effect of ultrasound in liquid foods is also attributed to intracellular cavitation, which disrupts the structural and functional components up to the point of cell lysis. Ultrasound can be considered as a viable technology in quality assurance purposes and food safety. References

Alava, J. M., Sahi, S. S., Garc
ıa- Alvarez, J., Tur
o, A., Ch
avez, J. A., Garc
ıa, M. J., et al. (2007). Use of ultrasound for the determination of flour quality. Ultrasonics, 46, 270e276. Aboonajmi, M., Akram, A., Nishizu, T., Kondo, N., Setarehdan, S. K., & Rajabipour, A. (2010). An ultrasound based technique for the determination of poultry egg quality. Research Agriculture Engineering, 56(1), 26e32. Antonova, I., Mallikarjunan, P., & Duncan, S. E. (2003). Correlating objective measurements of crispness in breaded fried chicken nuggets with sensory crispness. Journal of Food Science, 68, 1308e1315. Arroyo, C., Cebri
an, G., Pag
an, R., & Cond
on, S. (2011). Inactivation of Cronobacter sakazakii by ultrasonic waves under pressure in buffer and foods. International Journal of Food Microbiology, 144, 446e454. Benedito, J., Carcel, J. A., Gisbert, M., & Mulet, A. (2001). Quality control of cheese maturation and defects using ultrasonics. Journal of Food Science, 66(1), 100e104. Benedito, J., Carcel, J. A., Gonzalez, R., & Mulet, A. (2002). Application of low intensity ultrasonics to cheese manufacturing processes. Ultrasonics, 40, 19e23. Benedito, J., Carcel, J. A., Rossello, C., & Mulet, A. (2001). Composition assessment of raw meat mixtures using ultrasonics. Meat Science, 57, 365e370. Benedito, J., Mulet, A., Velasco, J., & Dobarganes, M. C. (2002). Ultrasonic assessment of oil quality during frying. Journal of Agricultural & Food Chemistry, 50, 4531e4536. Berm
udez-Aguirre, D., & Barbosa-C
anovas, G. V. (2008). Study of butter fat content in milk on the inactivation of Listeria innocua

ATCC 51742 by thermo-sonication. Innovative Food Science Emerging Technology, 9, 176e185. Berm
udez-Aguirre, D., & Barbosa-C
anovas, G. V. (2010). Processing of soft Hispanic cheese (“Queso Fresco”) using thermo-sonicated milk: a study of physicochemical characteristics and storage life. Journal of Food Science, 75(9), S548eS558. Berm
udez-Aguirre, D., Mobbs, T., & Barbosa-C
anovas, G. V. (2011). Ultrasound applications in food processing. In H. Feng, G. V. Barbosa-C
anovas, & J. Weiss (Eds.), Ultrasound technologies for food and bioprocessing (pp. 65e105). USA: Springer. Bermudez-Aguirre, D., Mawson, R., Versteeg, K., & NarbosaCanovas, G. V. (2009). Composition properties, physicochemical characteristics and shelf life of whole milk after thermal and thermosonication treatments. Journal of Food Quality, 32, 283e302. Bosworth, B. G., Holland, M., & Brazil, B. L. (2001). Evaluation of ultrasound imagery and body shape to predict carcass and fillet yield in farm-raised catfish. Journal of Animal Science, 79, 1483e1490. ~ez, J. A., Cambero, M. I., de la Hoz, L., & Cabeza, M. C., Ord
on Garc
ıa, M. L. (2004). Effect of thermoultrasonication on Salmonella enterica serovar Enteritidis in distilled water and intact egg shells. Journal of Food Protection, 67(9), 1886e1891. Camara, V. C., & Laux, D. (2010). Moisture content in honey determination with a shear ultrasonic reflectometer. Journal of Food Engineering, 96, 93e96. Caminiti, I. M., Noci, F., Mu~ noz, A., Whyte, P., Morgan, D. J., Cronin, D. A., et al. (2011). Impact of selected combinations of non-thermal processing technologies on the quality of an apple and cranberry juice blend. Food Chemistry, 124, 1387e1392. Cheng, L. H., Soh, C. Y., Liew, S. C., & The, F. F. (2007). Effects of sonication and carbonation on guava juice quality. Food Chemistry, 104(4), 1396e1401. Cho, B. K., & Irudayaraj, J. M. K. (2003). A noncontact ultrasound approach for mechanical property determination of cheeses. Journal of Food Science, 68(7), 2243e2247. Choi, Y. J., McCarthy, K. L., & McCarthy, M. J. (2002). Tomographic techniques for measuring fluid flow properties. Journal of Food Science, 67(7), 2718e2724. Cisneros, F., Ellis, M., Miller, K. D., Novakofski, J., Wilson, E. R., & McKeith, F. K. (1996). Comparison of transverse and longitudinal real-time ultrasound scans for prediction of lean cut yields and fat-free lean content in live pigs. Journal of Animal Science, 74, 2566e2576. Correia, L. R., Mittal, G. S., & Basir, O. A. (2008). Ultrasonic detection of bone fragment in mechanically deboned chicken breasts. Innovative Food Science Emerging Technology, 9, 109e115. Coupland, J. N. (2004). Low intensity ultrasound. Food Research International, 37, 537e543. Cruz, R. M. S., Vieira, M. C., & Silva, C. L. M. (2006). Effect of heat and thermosonication treatments on peroxidase inactivation kinetics in watercress (Nasturtium officinale). Journal of Food Engineering, 72(1), 8e15. Czank, C., Simmer, K., & Hartmann, P. E. (2010). Simultaneous pasteurization and homogenization of human milk by combining heat and ultrasound: effect on milk quality. Journal of Dairy Research, 77, 183e189. Earnshaw, R. G. (1998). Ultrasound: a new opportunity for food preservation. In M. J. W. Povey, & T. J. Mason (Eds.), Ultrasound in food processing (pp. 183e192). London: Blackie Academic & Professional. Elmehdi, H. M., Page, J. H., & Scanlon, M. G. (2003). Using ultrasound to investigate the cellular structure of bread crumb. Journal of Cereal Science, 38, 33e42. Elvira, L., Sampedro, L., de Espinosa, F. M., Matesanz, J., G
omezUllate, Y., Resa, P., et al. (2006). Eight-channel ultrasonic device for non-invasive quality evaluation in packed milk. Ultrasonics, 45, 92e99.

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98 Emenheiser, J. C., Greiner, S. P., Lewis, R. M., & Notter, D. R. (2010). Validation of live animal ultrasonic measurements of body composition in market lambs. Journal of Animal Science, 88, 2932e2939. Ercan, S.S¸, & Soysal, C ¸ (2011). Effect of ultrasound and temperature on tomato peroxidase. Ultrasonics Sonochemistry, 18, 689e695. Farhat, A. (2009). Carcass characteristics of Pekin ducks selected for greater breast muscle thickness using ultrasound scanning in response to dietary protein. Research Journal of Agricultural &. Biological Science, 5, 731e739.
G
omez, M., Oliete, B., Garc
ıa-Alvarez, J., Ronda, F., & Salazar, J. (2008). Characterization of cake batters by ultrasound measurements. Journal of Food Engineering, 89, 408e413. G
omez-L
opez, V. M., Orsolani, L., Mart
ınez-Y
epez, A., & Tapia, M. S. (2010). Microbiological and sensory quality of sonicated calciumadded orange juice. LWT e Food Science Technology, 43, 808e813. Gan, T. H., Palla, P., & Hutchins, D. A. (2006). Non-contact ultrasonic quality measurements of food products. Journal of Food Engineering, 77, 239e247. Ganjloo, A., Rahman, R. A., Bakar, J., Osman, A., & Bimakr, M. (2008). Feasibility of high-intensity ultrasonic blanching combined with heating for peroxidase inactivation of seedless guava (Psidium guajava L.). In “Proceedings of the 18th National Congress in Food Technology”, Mashhad, Iran. Gera, N., & Doores, S. (2011). Kinetics and mechanism of bacterial inactivation by ultrasound waves and sonoprotective effect of milk components. Journal of Food Science, 76(2), M111eM119. Ghaedian, R., Coupland, J., Decker, E. A., & McClements, D. J. (1998). Ultrasonic determination of fish composition. Journal of Food Engineering, 35, 323e337. Guerrero, S., L
opez-Malo, A., & Alzamora, S. M. (2001). Effect of ultrasound on the survival of Saccharomyces cerevisiae: influence of temperature, pH and amplitude. Innovative Food Science Emerging Technology, 2, 31e39. Hæggstr} om, E., & Luukkala, M. (2001). Ultrasound detection and identification of foreign bodies in food products. Food Control, 12(1), 37e45. Haughton, P. N., Lyng, J. G., Morgan, D. J., Cronin, D. A., Noci, F., Fanning, S., et al. (2010). An evaluation of the potential of highintensity ultrasound for improving the microbial safety of poultry. Food and bioprocess technology. doi:10.1007/s11947-010-0372y. Huang, E., Mittal, G. S., & Griffiths, M. W. (2006). Inactivation of Salmonella enteritidis in liquid whole egg using combination treatments of pulsed electric field, high pressure, and ultrasound. Biosystem Engineering, 94(3), 403e413. Hughes, D. E., & Nyborg, W. L. (1962). Cell disruption by ultrasound. Science, 138, 108e114. Jang, J.-H., & Moon, K.-D. (2011). Inhibition of polyphenol oxidase and peroxidase activities on fresh-cut apple by simultaneous treatment of ultrasound and ascorbic acid. Food Chemistry, 124, 444e449. Kim, K. eB., Lee, S., Kim, M. eS., & Cho, B. eK. (2009). Determination of apple firmness by nondestructive ultrasonic measurement. Postharvest Biological Technology, 52, 44e48. Kleczek, K., Wawro, K., Wilkiewicz-Wawro, E., Makowski, W., & Konstantynowicz, K. (2009). Relationships between breast muscle thickness measured by ultrasonography and meatiness and fatness in broiler chickens. Archiv Tierzucht, 52, 538e545. Knorr, D., Zenker, M., Heinz, V., & Lee, D. eU. (2004). Applications and potential of ultrasonics in food processing. Trend Food Science Technology, 15, 261e266. Krause, D., Sch€ ock, T., Hussein, M. A., & Becker, T. (2011). Ultrasonic characterization of aqueous solutions with varying sugar and ethanol content using multivariate regression methods. Journal of Chemometrics, 25, 216e223. L
opez, P., Sala, F. J., de la Fuente, J. L., Cond
on, S., Raso, J., & Burgos, J. (1994). Inactivation of peroxidase, lipoxygenase, and

97

polyphenol oxidase by manothermosonication. Journal of Agricultural & Food Chemistry, 42, 252e256. Lagrain, B., Boeckx, L., Wilderjans, E., Delcour, J. A., & Lauriks, W. (2006). Non-contact ultrasound characterization of bread crumb: application of the Biot-Allard model. Food Research International, 39, 1067e1075. Lee, H., Zhou, B., Liang, W., Feng, H., & Martin, S. E. (2009). Inactivation of Escherichia coli cells with sonication, manosonication, thermosonication, and manothermosonication: microbial responses and kinetics modeling. Journal of Food Engineering, 93, 354e364. Lopez, P., & Burgos, J. (1995). Lipoxygenase inactivation by manothermosonication: effects of sonication physical parameters, pH, KCl, sugars, glycerol, and enzyme concentration. Journal of Agricultural & Food Chemistry, 43, 620e625. M€ orlein, D., Rosner, F., Brand, S., Jenderka, K. eV., & Wicke, M. (2005). Non-destructive estimation of the intramuscular fat content of the longissimus muscle of pigs by means of spectral analysis of ultrasound echo signals. Meat Science, 69, 187e199. Mawson, R., Gamage, M., Terefe, M. S., & Knoerzer, K. (2011). Ultrasound in enzyme activation and inactivation. In H. Feng, G. V. Barbosa-C
anovas, & J. Weiss (Eds.), Ultrasound technologies for food and bioprocessing (pp. 369e404). USA: Springer. McClements, D. J. (1997). Ultrasonic characterization of foods and drinks: principles, methods, and applications. Critical Reviews in Food Science & Nutrition, 37(1), 1e46. Miles, C. A., Shore, D., & Langley, K. R. (1990). Attenuation of ultrasound in milks and creams. Ultrasonics, 28(6), 394e400. Mizrach, A. (2000). Determination of avocado and mango fruit properties by ultrasonic technique. Ultrasonics, 38, 717e722. Mizrach, A. (2007). Nondestructive ultrasonic monitoring of tomato quality during shelf-life storage. Postharvest Biological Technology, 46, 271e274. Mizrach, A., Galili, N., Rosenhouse, G., & Teitel, D. C. (1991). Acoustical mechanical and quality parameters of winter grown melon tissue. Transactions of the ASAE, 34, 2135e2138. Ni~ noles, L., Mulet, A., Ventanas, S., & Benedito, J. (2010). Ultrasonic assessment of the melting behaviour in fat from Iberian dry-cured hams. Meat Science, 85, 26e32. Nielsen, M., Martens, H. J., & Kaack, K. (1998). Low frequency ultrasonics for texture measurements in carrots (Daucus carota L.) in relation to water loss and storage. Postharvest Biological Technology, 14, 297e308. Noci, F., Walkling-Ribeiro, M., Cronin, D. A., Morgan, D. J., & Lyng, J. G. (2009). Effect of thermosonication, pulsed electric field and their combination on inactivation of Listeria innocua in milk. International Dairy Journal, 19, 30e35. ~ ez, J. A., Aguilera, M. A., Garcia, M. L., & Sanz, B. (1987). Ord
on Effect of combined ultrasonic and heat treatment (thermoultrasonication) on the survival of a strain of Staphylococcus aureus. Journal of Dairy Research, 54, 61e67. Pag
an, R., Ma~ nas, P., Alvarez, I., & Cond
on, S. (1999). Resistance of Listeria monocytogemes to ultrasonic waves under pressure at sublethal (manosonication) and lethal (manothermosonication) temperatures. Food Microbiology, 16, 139e148. Povey, M. J. W., & Harden, C. A. (1981). An application of the ultrasonic pulse echo technique to the measurement of the crispness of biscuits. Journal of Fd Technology, 16, 167e175. Raso, J., & Barbosa-C
anovas, G. V. (2003). Nonthermal preservation of foods using combined processing techniques. Critical Reviews of Food Science &. Nutrition, 43(3), 265e285. Raso, J., Pag
an, R., Cond
on, S., & Sala, F. J. (1998). Influence of temperature on the lethality of ultrasound. Applied Environmental Microbiology, 64, 465e471. Raviyan, P., Zhang, Z., & Feng, H. (2005). Ultrasonication for tomato pectinmethylesterse inactivation: effect of cavitation intensity and temperature on inactivation. Journal of Food Engineering, 70, 189e196.

98

J. Chandrapala et al. / Trends in Food Science & Technology 26 (2012) 88e98

Rawson, A., Tiwari, B. K., Patras, A., Brunton, N., Brennan, C., Cullen, P. J., et al. (2011). Effect of thermosonication on bioactive compounds in watermelon juice. Food Research International, 44(5), 1168e1173. Resa, P., Elvira, L., de Espinosa, F. M., Gonz
alez, R., & Barcenilla, J. (2009). On-line ultrasonic velocity monitoring of alcoholic fermentation kinetics. Bioprocessing Biosystem Engineering, 32, 321e331. Sch} ock, T., & Becker, T. (2010). Sensor array for the combined analysis of wateresugareethanol mixtures in yeast fermentations by ultrasound. Food Control, 21(4), 362e369. Scherba, G., Weigel, R. M., & O’Brien, W. D. (1991). Quantitative assessment of the germicidal efficacy of ultrasonic energy. Applied Environmental Microbiology, 57, 2079e2084. Skaf, A., Nassar, G., Lefebvre, F., & Nongaillard, B. (2009). A new acoustic technique to monitor bread dough during the fermentation phase. Journal of Food Engineering, 93, 365e378. Stelzleni, A. M., Perkins, T. L., Brown Jr., A. H., Pohlman, F. W., Johnson, Z. B., & Sandelin, B. A. (2002). Genetic parameter estimates of yearling live animal ultrasonic measurements in Brangus cattle. Journal of Animal Science, 80, 3150e3153. Telis-Romero, J., V
aquiro, H. A., Bon, J., & Benedito, J. (2011). Ultrasonic assessment of fresh cheese composition. Journal of Food Engineering, 103, 137e146. Terefe, N. S., Gamage, M., Vilkhu, K., Simons, L., Mawson, R., & Versteeg, C. (2009). The kinetics of inactivation of pectin methylesterase and polygalacturonase in tomato juice by thermosonication. Food Chemistry, 117, 20e27. Thakur, B. R., & Nelson, P. E. (1997). Inactivation of lipoxygenase in whole soy flour suspension by ultrasonic cavitation. Nahrung, 41, 299e301. Tian, Z. M., Wan, M. X., Wang, S. P., & Kang, J. Q. (2004). Effects of ultrasound and additives on the function and structure of trypsin. Ultrasonics Sonochemistry, 11(6), 399e404. Ting, C. eH., Kuo, F. eJ., Lien, C. eC., & Sheng, C. eT. (2009). Use of ultrasound for characterising the gelation process in heat induced CaSO4 · 2H2O tofu curd. Journal of Food Engineering, 93, 101e107. Tiwari, B. K., Muthukumarappan, K., O’Donnell, C. P., & Cullen, P. J. (2008a). Colour degradation and quality parameters of sonicated orange juice using response surface methodology. LWT e Food Science Technology, 41, 1876e1883. Tiwari, B. K., Muthukumarappan, K., O’Donnell, C. P., & Cullen, P. J. (2009). Inactivation kinetics of pectin methylesterase and cloud retention in sonicated orange juice. Innovative Food Science Emerging Technology, 10, 166e171. Tiwari, B. K., O’Donnell, C. P., Patras, A., & Cullen, P. J. (2008b). Anthocyanin and ascorbic acid degradation in sonicated strawberry juice. Journal of Agricultural & Food Chemistry, 56, 10071e10077.

Ugarte-Romero, E., Feng, H., & Martin, S. E. (2007). Inactivation of Shigella boydii 18 IDPH and Listeria monocytogenes Scott A with power ultrasound at different acoustic energy densities and temperatures. Journal of Food Science, 72(4), M103eM107. Ugarte-Romero, E., Feng, H., Martin, S. E., Cadwallader, K. R., & Robinson, S. J. (2006). Inactivation of Escherichia coli with power ultrasound in apple cider. Journal of Food Science, 71(2), E102eE108. Vercet, A., Burgos, J., Crelier, S., & Lopez-Buesa, P. (2001). Inactivation of proteases and lipases by ultrasound. Innovative Food Science Emerging Technology, 2, 139e150. Vercet, A., Lopez, P., & Burgos, J. (1997). Inactivation of heat-resistant lipase and protease from Pseudomonas fluorescens by manothermosonication. Journal of Dairy Science, 80, 29e36. Vercet, A., Lopez, P., & Burgos, J. (1999). Inactivation of heat-resistant pectinmethylestease from orange by manothermosonication. Journal of Agricultural & Food Chemistry, 47, 432e437. Vercet, A., Oria, R., Marquina, P., Crelier, S., & Lopez-buesa, P. (2002). Rheological properties of yoghurt made with milk submitted to manothermosonication. Journal of Agricultural & Food Chemistry, 50, 6165e6171. Villamiel, M., & de Jong, P. (2000). Inactivation of Pseudomonas fluorescens and Streptococcus thermophilus in TrypticaseÒ soy broth and total bacteria in milk by continuous-flow ultrasonic treatment and conventional heating. Journal of Food Engineering, 45, 171e179. Walkling-Ribeiro, M., Noci, F., Cronin, D. A., Lyng, J. G., & Morgan, D. J. (2009). Shelf life and sensory evaluation of orange juice after exposure to thermosonication and pulsed electric fields. Food Bioproduction Processing, 87, 102e107. Wiklund, J., & Stading, M. (2008). Application of in-line ultrasound Doppler-based UVPePD rheometry method to concentrated model and industrial suspensions. Flow Measurement and Instrumentation, 19, 171e179. Wong, E., Vaillant-Barka, F., & Chaves-Olarte, E. (2010). Synergistic effect of sonication and high osmotic pressure enhances membrane damage and viability loss of Salmonella in orange juice. Food Research International. doi:10.016/ j.foodres.2010.07.037. Wu, J., Gamage, T. V., Vilkhu, K. S., Simons, L. K., & Mawson, R. (2008). Effect of thermosonication on quality improvement of tomato juice. Innovative Food Science Emerging Technology, 9, 186e195. Zenker, M., Heinz, V., & Knorr, D. (2003). Application of ultrasoundassisted thermal processing for preservation and quality retention of liquid foods. Journal of Food Protection, 66(9), 1642e1649. Zhao, B., Basir, O. A., & Mittal, G. S. (2003). Detection of metal, glass and plastic pieces in bottled beverages using ultrasound. Food Research International, 36, 513e521.