Quantifying and predicting meat and meat products quality attributes using electromagnetic waves: An overview

Meat Science 95 (2013) 879–896

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Quantifying and predicting meat and meat products quality attributes using electromagnetic waves: An overview Jean-Louis Damez ⁎, Sylvie Clerjon INRA, UR370 Qualité des Produits Animaux, F-63122 Saint Genès Champanelle, France

a r t i c l e

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Article history: Received 11 February 2013 Received in revised form 11 April 2013 Accepted 12 April 2013 Keywords: Meat quality NMR X-ray Microwave Fluorescence Infrared

a b s t r a c t The meat industry needs reliable meat quality information throughout the production process in order to guarantee high-quality meat products for consumers. Besides laboratory researches, food scientists often try to adapt their tools to industrial conditions and easy handling devices useable on-line and in slaughterhouses already exist. This paper overviews the recently developed approaches and latest research efforts related to assessing the quality of different meat products by electromagnetic waves and examines the potential for their deployment. The main meat quality traits that can be assessed using electromagnetic waves are sensory characteristics, chemical composition, physicochemical properties, health-protecting properties, nutritional characteristics and safety. A wide range of techniques, from low frequency, high frequency impedance measurement, microwaves, NMR, IR and UV light, to X-ray interaction, involves a wide range of physical interactions between the electromagnetic wave and the sample. Some of these techniques are now in a period of transition between experimental and applied utilization and several sensors and instruments are reviewed. © 2013 Elsevier Ltd. All rights reserved.

1. Introduction Consumers and manufacturers are increasingly seeking products of certified quality (Verbeke, 2011). The meat industry is no exception to this expectation (Grunert, 2006; Verbeke et al., 2010). Furthermore, the meat sector, particularly the beef sector, has to contend with a major challenge due to the broad-ranging variability of the raw material, which ultimately translates into high variability in product quality and low process control over the commercialized end product. The meat industry needs reliable meat quality information throughout the production process in order to guarantee high-quality meat products for consumers. To meet this demand, many studies have recently been performed in research laboratories, sometimes leading to systems for analyzing, assessing and certifying product quality. Among the techniques used, those based on physical methods of analysis predominate, with analysis and characterization systems that often rely on electromagnetic waves. The widespread use of electromagnetic waves for meat quality assessment is due to their practicality and their ability to explore the material. Depending on the frequency or the wavelength used, electromagnetic waves are more or less likely to be reflected in the meat or be transmitted and absorbed, offering the possibility to objectively quantify quality factors through physical measurements. The targeted quality factors are characterized from the review and analysis of the reflected and

⁎ Corresponding author. E-mail address: [email protected] (J.-L. Damez). 0309-1740/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.meatsci.2013.04.037

transmitted waves after sometimes sophisticated computation, now facilitated by the power of modern computers. The main meat quality traits that can be assessed are sensory characteristics, chemical composition, physicochemical properties, health-protecting properties, nutritional characteristics and safety (Damez & Clerjon, 2012). The electromagnetic waves used range from low frequency, high frequency, microwaves, NMR, to IR, UV light and X-ray. The dielectrical properties of meat are to a large extent dependent on the state of the cell membranes, and also on molecular composition, the presence of ions, electrical charges on proteins and pH variations that lead to a complex dielectric spectrum (Fig. 1). Some of the techniques involved are of particular interest as they can explore the material without requiring any contact, but unfortunately they are often costly and difficult to use on the production line. The purpose of this paper is to provide a non-exhaustive overview of recent approaches and the latest research in electromagnetic methods developed for evaluating the quality of different meat products, and to examine the possibility of their deployment. These techniques are now making their way out of the laboratory. In addition, several sensors and devices are reviewed. 2. Low frequency assessment Low frequencies have long been used to characterize the properties of biological tissue and to assess meat quality, thus they are used in a broad range of applications. The technique is known as bioimpedance and at first glance seems easy to use as generally only a low frequency

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Fig. 1. Schematic representation of the electromagnetic spectrum (in logarithm scale) of the different effects that contribute to effective loss factor (adapted from Castro-Giraldez et al., 2010) where I represent the ionic losses, MW means Maxwell–Wagner effect, db and dfw are respectively related to the dipolar losses of bound water and free water, a and e are respectively related to the atomic losses and the electronic losses.

generator, a couple of electrodes and a view meter are needed (Fig. 2). At low frequencies the cell membrane is non-conducting, and intracellular fluid (ICF) acts as an internal electrolyte and gives rise to a capacitance when an alternating electric current is induced. When an electric current passes through tissue, it passes through the extracellular fluid (ECF) or through both the ECF and ICF compartments. Both these compartments can be considered as purely resistive. The current pathway is generally represented as two parallel branches: one through the ECF and the other through the capacitive membrane and the ICF compartment. The extracellular pathway is considered to be purely resistive, whereas the intracellular pathway including the capacitive effect of the cell membrane is an impedance (i.e. complex), with a resistive part (real) and a capacitive part (imaginary), resulting in the magnitude of the intracellular impedance being frequency dependent (Damez & Clerjon, 2007; Damez, Clerjon, Abouelkaram, & Lepetit, 2007). Spectral analysis of the magnitude gives details of membrane integrity, and the state of ECF and ICF and the interaction between them.

2010). The structural organization and composition of meat makes it a highly anisotropic dielectric material, i.e. impedance varies according to whether the current runs parallel or perpendicular to muscle fiber

2.1. Meat tenderness Meat-tenderizing biochemical processes occur during aging, with endogenous proteases causing structural changes, fragmentation of myofibrils and degradation of the cytoskeleton (Hopkins & Thompson, 2002; Ouali et al., 2006). Bioimpedance has proven particularly successful in assessing age-related meat tenderness and could be used for prediction of meat tenderness (Lepetit, Sale, Favier, & Dalle, 2002). More recently, Hopkins and Wang (2012) reported that this technology could be used to screen meat into tender or tough categories at 1 day post-mortem, but found no signifiant correlation with 5-day shear force. However, Byrne, Troy, and Buckely (2000) reported that there is no relationship between electrical conductivity and shear force values assessed with Warner–Bratzler shear force, arguing that the amount of connective tissue inducing meat toughness cannot be assessed by a straightforward electrical measurements. Electrical impedance-based techniques for measuring tenderness therefore focus more on exploiting the potential of measuring the state of muscle fiber and age-related shifts in its anisotropy (Castro-Giraldez, Botella, Toldra, & Fito,

Fig. 2. A handled device for impedance measurement with two electrodes (LF-STAR; Matthäus, Nobitz, Germany).

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(Damez, Clerjon, Abouekaram, & Lepetit, 2008a; Damez, Clerjon, Abouelkaram, & Lepetit, 2008b). As meat ages, it tends to lose anisotropy, and studies and new instruments exist that are capable of identifying this phenomenon and thus characterizing this myofibril profile-related anisotropy (Lepetit et al., 2007). 2.2. Fat content Many studies conducted since the 1980s have attempted to use electrical properties to estimate fat content in animal carcasses and meat (Slanger & Marchello, 1994). As fat is an electrical insulator, it influences tissue impedance. Preliminary investigations have been made in pork by Swantek, Crenshaw, Marchello, and Lukaski (1992) and in beef and pork by Marchello, Slanger, and Carlson (1999). Slanger and Marchello (1994) measured the electrical conductivity of bovine carcasses and obtained remarkable results with a simple electric conductivity measurement immediately after slaughter giving fat content with remarkable accuracy (R2 = 0.95). This can be explained by the fact that no membrane or extracellular compartment modifications occur immediately after slaughter, and the measurements are made at a stable temperature. Measurements of fat content after rigor mortis are not consistent, as impedance in this case is also influenced by membrane state as mentioned in the paragraph above. A patented electrical impedance system has been developed (Madsen, Rasmussen, Boggaard, & Nielsen, 1999) for measuring fat content in muscle. This portable apparatus uses electrodes inserted in the muscle and fat content is estimated via measurements made at several frequencies. 2.3. Salt content Sodium chloride is widely used in the meat industry as an inhibitor of microbial spoilage flora, as a taste exhauster and because it improves technological meat quality such as water holding capacity (WHC). However, excessive salt consumption is linked to cardiovascular disease and a reduction of salt content in brined products is therefore recommended by public health policies (WHO, 2007). Recent studies have shown that electrical impedance is a viable salt measurement in fish (Chevalier, Ossart, & Ghommidh, 2006). In this study, three circular probes with different electrode geometries were concurrently tested and impedance measurements were performed with a system developed by Fogale Nanotech (Nimes, France), sodium chloride content was determined by ISO 1841-2 potentiometric method. The authors conclude that the circular geometry of the probe is very important, the probe with higher interior electrode providing the most efficient prediction model for salt content (R2 = 0.89). A similar study was undertaken on minced meat (Labrador et al., 2010) and other food products by (Masot et al., 2010), with a circular coaxial needle probe, and prediction models compared with those obtained from a voltametric electronic tongue. The authors concluded that the good accuracy and precision in prediction of chloride (p1 = 0.985; NR = 0.388) offer the possibility of developing portable devices to be used at any point of the processing step. This sensor is very smart, but the associated electronic equipment (frequency response analyzer) and PC software must be integrated in a portable apparatus for on line utilization. 2.4. Pale soft exudative (PSE) and dark firm dry (DFD) meats These two quality defects are associated with membrane modifications and changes in the extracellular medium. They are therefore bound to affect electrical properties. A major quality problem in pork is preventing the production of pale soft exudative (PSE) meat whose pH decreases rapidly, they are highly exudative, and so are unsuitable for processing. In beef, one quality problem is dark firm dry (DFD) meat with high pH and high susceptibility to spoiling. The difficulty in detecting PSE meats during the development of rigor mortis arises because, as this phenomenon occurs, parameters such as pH and temperature evolve

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rapidly and with sequential metabolic modifications, affecting structure and therefore electrical properties (Bendall & Swatland, 1988). Most of the studies in this field have focused on the early detection of quality defects, i.e. 45 min to 1 h after slaughter. However, results show that electrical measurements do not permit the early detection of DFD (Forrest et al., 2000; Garrido, Bañón, Pedauyé, & Laencina, 1994). Guerrero et al. (2004) noted that PSE meats are better detected by low frequency impedance methods once their final pH has been reached. More recently, Castro-Giraldez et al. (2010) pointed out that the use of certain precise frequencies (140 Hz, 500 Hz and 300 kHz) in the low frequency range are more reliable at 24 h after slaughtering to detect meat quality defects in porcine muscle during post-mortem period. Two indexes were proposed, one utilizing the measurement of dielectric constant at two frequencies (140 Hz and 300 kHz), the other analyzing the integrity of cells membranes from a normalized subtraction of the conductivity at 300 kHz and 1 kHz. 2.5. Methods and apparatus The most elementary and commonly used method is to use two electrodes to induce a current flow (I) and a voltage (V) between these two electrodes, making it possible to deduce an electrical impedance by applying Ohm's law, V = ZI. The impedance (Z) is a complex function of alternating current frequency f, e.g. Z = Zreal + iZimag, where Zreal is the real part (resistive), Zimag the imaginary part (capacitive) and i = (−1)1/2. Unfortunately in this bipolar system, electrode polarization can produce a systematic error in the voltage measured between the two electrodes caused by parasitic capacitive impedances occurring at the interface of the two electrode-sample ohmic contacts (Damez et al., 2007). This capacitive gap contact reflects the dielectric quality of the samples (Hwang, Kirkpatrick, Mason, & Garboczi, 1997). It has been shown elsewhere that this effect, often interpreted as parasitic effect mainly at low frequency, could be used to control meat aging state because it reflects the conductive quality of ECF (Damez et al., 2008a). One way to eliminate this electrode-sample contact effect is not to induce a current flow in the measuring circuit. This can be achieved by the tetrapolar measurement method in which a current is applied by two injection electrodes and voltage is measured via two separate measurement electrodes (Hopkins & Wang, 2012; Swantek et al., 1992). Another way is to use several aligned, regularly spaced electrodes and take bipolar measurements between each pair of electrodes. With homogenous samples the impedance per unit length is termed lineic impedance, so that as the distance increases the impedance also increases (Damez et al., 2008a). Lineic impedance can therefore be calculated from the slope of the impedance plot. The contact impedance between the material and the sensing electrodes is the intercept corresponding to null distance between the electrodes. The advantage of this technique is that a multitude of impedance measurements can be obtained by a single application of the sensing electrodes with the determination of the contact effects. Normalized methods are frequently used in order to avoid dispersion in measurement caused by influence factors (such as temperature). The ratio of impedances at two frequencies (1 kHz/100 kHz) was used by Lepetit et al. (2002) who argued that the anisotropy of impedance in meat almost disappears at higher frequency. A similar ratio has been evaluated, ranging from π/2 to 1 (Damez et al., 2007) for an anisotropic to isotropic structural meat state (e.g., due to the disruption of the insulating myofibril membranes of the sarcoplasmic reticulum during aging, or freezing). An index of anisotropy could be used advantageously for assessing meat aging (Gomez-Sanchez, RistizabalBotero, Barragan-Arango, & Felice, 2009) and circular multi-electrode sensors based on this method have been patented (Damez, Clerjon, Abouelkaram, & Lepetit, 2006; Lepetit et al., 2007)(Fig. 3). On the other hand, the anisotropic structure of meat can be considered as a major difficulty for taking impedance measurements (Lepetit et al., 2002) and therefore for on-line control. A smart method of avoiding this difficulty is to make simultaneous measurements with tetrapolar

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Fig. 3. A multidirectional sensor for impedance measurement (Lepetit et al., 2007).

electrodes in many directions (Damez et al., 2008b) or by using a sensor to provide, intrinsically, the radial distribution of electric fields as is done when using a coaxial probe (Masot et al., 2010). Madsen et al. (1999) applied a technique with tetrapolar electrodes with a judicious choice of frequencies and patented an intramuscular fat sensor. Yang et al. (in press) developed a low-cost portable apparatus with four electrodes to distinguish meat illegally injected with water from normal fresh meat.

3. Microwaves Microwaves and electromagnetic sensors offer a non-invasive solution, but are not widely used in the meat industry. The relevant quality attributes that can be assessed with them are related to structure, composition (particularly water content), water state and water distribution in the product, and particularly water content profiles (Clerjon & Damez, 2009). In the high frequency range the dielectric properties of meat are closely correlated with water state and water content. Dielectric relaxation spectroscopy determines the response of the molecular motion of polar molecules in the sample to a weak external alternating electric field. As the frequency of the electric field is increased, it reaches a frequency called the relaxation frequency when the polar molecule can no longer rotate with the electric field. Dielectric properties change significantly around this relaxation frequency (Clerjon, Daudin, & Damez, 2003). The rare industrial applications currently using microwave are based either on cavity, antenna or probe measurements. A specific method using transmission–reflection measurements should be highlighted. The basic configuration of this method uses two antennas, one transmitting and one receiving, the meat streaming on a conveyor belt between the two non-contacting antennas (Nyfors, 2000). Applications of microwave sensors in other sectors of the food industry could be adapted for the meat industry, particularly for measuring water content. Work has been carried out over the last two decades by the US Department of Agriculture on water content, water state and density of grain and seed (Nelson & Trabelsi, 2008), and meat (Nelson & Trabelsi, 2012; Trabelsi & Nelson, 2009). The information presented is helpful to those considering applications of dielectric properties for sensing quality attributes of agricultural products and for those considering microwave or radio-frequency dielectric heating applications as well.

The addition of water is a classic method of fraud in the food industry and Kent and Anderson (1996) focused on water state in food products and particularly meat products. Dielectric spectroscopy gives information on the chemical relationship of compounds with their surroundings, thus water content, state and water activity (aw) have been studied using spectroscopic techniques (Castro-Giráldez, Aristoy, Toldrá, & Fito, 2010; Clerjon et al., 2003). The microwave transmission/reflection technique is also used to measure the presence and quantity of other compounds in food products, such as salt content (Shiinoki, Motouri, & Ito, 1998), parasites (Nelson, Bartley, & Lawrence, 1997) and foreign bodies, for example, bone in meat cuts (Damez & Clerjon, 2000). Regarding seafood quality evaluation a German company SEQUID (Sequid GmbH, Bremen, Germany) has developed a microwave sensor based on the time domain reflectometry (TDR) method and multivariate analysis (Mike et al., 2007) for the classification of fish according to flesh quality. TDR can be also applied to recognize fresh meat quality parameters (Dreyß, Klaus, & Lücker, 2010). On the basis of this apparatus the same company, in collaboration with the Spanish research institute CENTA/IRTA (Fulladosa et al., 2013), developed a handheld TDR device, the RFQ Scan 3.0, to measure salt and water content and water activity in Serrano Ham (Schimmer, Schönfeld, Duran Montgé, & Fulladosa, 2011). The applications listed above use coaxial probe methods. Because of their axial symmetry such coaxial sensors do not exploit the anisotropic properties of dielectric fibers. The material under test is exposed to the electromagnetic field in all directions and therefore there is no potential for directional measurement. The components from muscle to sarcomere filaments are elongated and roughly parallel, forming bundles of connective tissue and myofibers with very different intrinsic dielectric properties (Epstein & Foster, 1983; Gabriel, Lau, & Gabriel, 1996), conferring strong anisotropic dielectric behavior. This anisotropic trait is still under study leading to a new method and apparatus for assessing meat aging and freshness that will soon be used on-line (Clerjon & Damez, 2007, 2009; Kent, Peymann, Gabriel, & Knight, 2002). 4. Nuclear magnetic resonance (NMR) NMR is based on the emission and absorption of energy in the radiofrequency range of the electromagnetic spectrum. All nuclei that contain odd numbers of protons or neutrons can be observed with NMR. The most commonly measured nuclei are 1H and 13C, although nuclei from the isotopes of many other elements can be observed (23Na, 31P, etc.). NMR aligns magnetic moments with an applied constant magnetic field and disturbs this alignment using an orthogonal alternating radiofrequency magnetic field. This disturbance induces a resonant phenomenon which is used in NMR measurements and magnetic resonance imaging (MRI). Both NMR and MRI remain expensive techniques, but they are increasingly used in food research applications. Although we are still far from introducing industrial NMR sensors on production lines, some new devices have appeared (Bruker, 2012) and are opening the way for time domain NMR experiments outside the laboratory (Capitani, Brilli, Mannina, Proietti, & Loreto, 2009). In what follows we distinguish between NMR experiments and MRI experiments, the latter involving spatial coding to obtain images and then local information. 4.1. NMR spectroscopy Descriptions of NMR experiments often differ between publications. Fear not! Many studies on meat and fish products are based on the same principles. Basically, two kinds of NMR are performed: (i) time domain NMR and (ii) spectroscopic NMR (signal versus frequency). The time domain NMR gives relaxation times: longitudinal relaxation time T1 and transversal relaxation time T2 (more widely used). Spectroscopic

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NMR provides peaks (at given frequencies) corresponding to certain molecules of the sample under test. Both time domain and spectroscopic NMR can be performed not only for protons but also for other nuclei containing odd numbers of protons or neutrons. Since the measurement of T2 is much more common, in the following 1H NMR means T2 measurement. Several T2 can be measured in meat products revealing the water distribution which describes the different (more or less bounded) states of water in the product. Basically, a long T2 corresponds to a fraction of free water. NMR acquisition can be done at low or high field (LF or HF, respectively), depending on the static magnetic field of the experimental device. Some of the authors cited below used the magic angle spinning (MAS) method. The MAS is a physical technique used to improve NMR spectra resolution (by rotating the sample). More information on this technique applied to foodstuffs is given by Valentini et al. (2011). Several reviews dealing with NMR and meat science have been published over the last decade. The most complete are those of Renou, Bielicki, Bonny, Donnat, and Foucat (2003) and Bertram and Andersen (2004) on applications of 1H NMR and MRI and 1H, 13C and 31P NMR spectroscopy to meat. Others are devoted to NMR applications for fish (Bekirogglu, 2010; Erikson, Standal, Aursand, Veliyulin, & Aursand, 2012) or else cover all food applications in general (Bertocchi & Paci, 2008). 4.1.1. 1H NMR to study water In a comparative spectroscopic study, Brondum et al. (2000) demonstrated that 1H NMR is a better spectroscopic method for assessing water holding capacity (WHC), intra muscular fat (IMF) and total water content in porcine muscles than visual, fluorescent and near infrared (NIR) reflectance spectrophotometry. As water protons are easily visible with 1H NMR, this technique is obviously especially useful for studying water in food products. The parameters linked to meat and fish products are numerous: water content, WHC, water distribution (i.e. water state), water mobility, etc. All of them have been investigated extensively by the Danish Aarhus University. The final quality of porcine meat depends on WHC and this attribute must be understood and controlled, 1H NMR is a good candidate for performing this assessment (Bertram, 2004; Bertram & Andersen, 2007; Bertram, Jian Zhi, Rommereim, Wind, & Andersen, 2004; Straadt, Aaslyng, & Bertram, 2011). As explained above, water mobility and water distribution are other important attributes of final meat that can be measured by 1H NMR (Bertram, Purslow, & Andersen, 2002; Gudjónsdóttir, Arason, & Rustad, 2011; Moller, Gunvig, & Bertram, 2010; Tornberg, Wahlgren, Brondum, & Engelsen, 2000). In all these papers, the authors identify several transverse relaxation times and correlate them with various process or quality parameters. Also, 1H NMR measurement and water distribution in meat during aging have been dealt with briefly in a review (Pearce, Rosenvold, Andersen, & Hopkins, 2011). It is worthwhile to note that these studies were mainly carried out with laboratory bench top machines, and there is still a big step to access such results in an industrial online configuration. Sometimes, 1H NMR is simply applied to the measurement of total moisture content (Pereira & Colnago, 2012). Here, care must be taken to consider the total water content by measuring all the transverse relaxations. 4.1.2. 1H NMR for studying structure Since 1H NMR can identify variations in water–protein interactions and then in protein states, it is a potential tool for studying structure. For instance, it has been shown that NMR parameters are highly sensitive to differences in the muscle structure of farmed and wild cod and to the effect of brine injection, brining, and rigor tension on the muscle (Gudjonsdottir et al., 2010). In porcine meat, 1H NMR T2 relaxation demonstrated a significant effect of fresh meat quality (PSE versus DFD) on water distribution in frozen–thawed meat (Bertram, Andersen, & Andersen, 2007). During the heating of porcine meat, shrinkage reduces myofibrillar spacing and water mobility as measured by 1H NMR T2 (Christensen, Bertram, Aaslyng, & Christensen, 2011). Herrero et al. (2009) present an interesting NMR study on meat batter cold-set

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gelation. The measurement of 1H NMR T1 and T2 relaxation times in association with the apparent diffusion coefficient (this parameter requires spatial gradients in addition to a NMR spectrometer) informs on pore size, water mobility (inside pores) and water translational motion, all of which are related to cold-set gelation. Structure being linked to tenderness, a study with sheep meat investigated the relationship between shear force and NMR relaxation measurements and demonstrated a moderate relationship of R = 0.78 (Pearce et al., 2008). Further researches are necessary to confirm if NMR is a suitable technology for online measurement of meat tenderness (Pearce et al., 2011). 4.1.3.

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P NMR P NMR is mainly applied to post mortem evaluation in meat and fish muscle. 31P NMR is used in the prediction of fish freshness (Chiba et al., 1991), of WHC in rabbit muscle, in association with 1H MAS and NMR (Bertram et al., 2004). Significant effects of stunning method on changes of the various phosphorus metabolites in the muscle post mortem have been observed by 31P-NMR spectroscopy by Bertram, Stodkilde-Jorgensen, Karlsson, and Andersen (2002). 31P NMR is also a tool used to monitor added phosphorous compounds in brined muscle food, either to obtain better understanding of the role of these compounds in WHC (Johnsen, Jorgensen, Birkeland, Skipnes, & Skara, 2009) or to control polyphosphate additives in meat products (Hrynczyszyn, Jastrzebska, & Szyk, 2010). Applications of 31P NMR spectroscopy in foodstuffs, especially in meat and fish products, are overviewed by Spyros and Dais (2009). 31

4.1.4. 23Na NMR and salt issues Better understanding of the role of Na+ and Cl− ions is necessary to achieve safe salt reduction. Foucat, Donnat, and Renou (2003) studied the “free” and “bound” fraction of each ion in pork meat and smoked salmon using 23Na and 35Cl NMR spectroscopy. These authors capitalized on the quadripolar characteristic of these two nuclei to perform single and multi quanta filtering and then identify the state of ions. The absolute quantification based on this technique was described later by the same INRA team (Mouaddab, Foucat, Donnat, Renou, & Bonny, 2007). More classically, 23Na NMR is performed to quantify salt content in meat and fish products. For instance, in association with 23Na MRI, it is a rapid and reliable alternative for optimizing and understanding industrial salting processes in the fish industry (Erikson, Veliyulin, Singstad, & Aursand, 2004). 4.1.5. NMR combined with other technologies It is often useful to combine NMR characterization with other biophysical methods, mainly optical approaches, as it provides complementary information. For instance, Brondum, Byrne, Bak, Bertelsen, and Engelsen (2000) combined LF 1H NMR, visible (VIS) and near infrared (NIR) reflectance, Raman scattering, and fluorescence emission, to detect warmedodor flavor (WOF) in porcine meat from animals with different levels of pre-slaughter stress. VIS reflectance and LF 1H NMR provide complementary information to detect WOF, among other parameters, because LF 1H NMR measures the entire volume of the sample, thus reducing surface effects. As highlighted by Brondum and al., this method has the potential for use in rapid on-line industrial situations to predict the sensory quality of cooked meats. Fourier transform infrared (FT-IR) micro-spectroscopy and LF 1H NMR T2 relaxation measurements were used to study the changes in protein secondary structure and water distribution, e.g. relationship between myofibrillar-entrapped water and intramolecular antiparallel β-sheets and α-helical structures, in porcine meat for several conditions of aging, salting and heating (Bertram, Kohler, Bocker, Ofstad, & Andersen, 2006; Wu, Bertram, Bocker, Ofstad, & Kohler, 2007; Wu et al., 2006). This combination is of particular interest because LF 1H NMR T2 relaxation measurements provide water distribution while FT-IR is the best tool for determining the secondary structural changes of proteins in meat products. Another solution for explaining water distribution measured by LF 1H NMR is the use of atomic force microscopy

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(Bertram, Meyer, Wu, Zhou, & Andersen, 2008). This very high resolution microscopy also gives information on the microstructure of myofibrillar proteins. Optical methods are not the only ones that can be associated with NMR. Farag, Duggan, Morgan, Cronin, and Lyng (2009) presented the first study reporting the integrated use of 1H NMR, solid-phase micro extraction gas chromatography mass spectrometry (SPME-GC–MS), and multivariate statistics for the analysis of microbial metabolism in beef meat. While SPME-GC–MS detects mainly the end products of metabolism, the use of NMR also allows study of the evolution of intermediate compounds (Ercolini et al., 2011). 4.1.6. NMR for meat tracing and tracking To enhance consumer confidence in food, we need a traceability system providing information on the origin, processing, retailing and final destination of foodstuffs (Schwaegele & Andree, 2009). NMR is a candidate for fulfilling these tracing and tracking functions. For instance, it is well known that grazing can lead to the introduction of dioxins in beef and that it accumulates in the fatty tissues of cattle. Abernathy and Maxwell (2006) proposed a 1H NMR approach to detect dioxin in beef meat. A recent study demonstrated that 1H NMR based metabolomic fingerprinting is a useful tool, in combination with chemometric analysis, for distinguishing the origins of raw beef samples (Jung et al., 2010). A similar study, but associating 1H, 2H and 13C NMR with chemometric analysis, also demonstrated the possibility of discriminating beef meat origin, but not beef feeding (Renou et al., 2004). A study on porcine meat stemming from novel pig crossings showed that 1H NMR frozen exudates and meat extracts revealed differences in metabolite profile as a function of the breeds studied (Straadt et al., 2011). Another original study associating 1 H NMR with magic angle spinning and 13C NMR also dealt with authentication and breed discrimination in lamb meat (Sacco, Brescia, Buccolieri, & Jambrenghi, 2005). The 1H NMR plasma metabolite profile of pork is also correlated with pre-slaughter stress, and then with WHC (Bertram, Oksbjerg, & Young, 2010). Fish products have not been forgotten. The suitability of 1H NMR for identifying certain bioactive compounds in cod has been demonstrated (Martinez et al., 2005). These compounds allow the correct classification of 80% of samples, according to their processing condition (i.e. not frozen, frozen, frozen thawed, fresh unprocessed, boiled fried), using a probabilistic neural network procedure. 4.1.7. NMR and fat issues The measurement of the in vivo intramuscular fat content (IMF) of longissimus muscle of pig is of interest for breeders when selecting IMF content. A comparison between ultrasound and 1H NMR concluded that NMR is less reliable, but provides a quantification of fat composition in addition to fat content (Ville et al., 1997). Concerning foodstuffs, 1 H NMR offers a rapid, easily usable and solvent-free alternative method to extraction methods. Toussaint et al. (2002) demonstrated its reliability on previously dried fish flesh. The real advantage of NMR methods relating to fat is that, beyond total fat content, NMR gives information on fat composition by quantifying conjugated linoleic acids in beef samples (Maria, Colnago, Forato, & Bouchard, 2010), and by quantifying acid chain composition in pork meat (Siciliano et al., 2013) and in irradiated chicken meat (Stefanova, Vasilev, & Vassilev, 2011). 4.2. Magnetic resonance imaging (MRI) When looking into the food applications of MRI, we can find a wide range of issues treated by a wide range of MRI solutions. Indeed, this paramagnetic technique can be used to observe several nuclei as well as several physical properties such as diffusion, mobility, binding state, etc. using varied contrasts. This means that the image obtained depends on the method chosen to contrast it, by adjusting relaxation times, diffusion, chemical shift, etc. The overview presented below deals with fat, salt and muscle structure issues, mechanical properties and the cooking process.

4.2.1. MRI and the cooking process Cooking is a general process which transforms raw meat material into food, with the heating of the muscle matrix influencing the qualities of cooked meat. Since cooking is applied more and more frequently in standardized and industrial conditions, it makes sense to model certain key mechanisms which determine these qualities in order to optimize the process. To achieve this, several authors have monitored cooking under MRI (Shaarani, Nott, & Hall, 2006). An original experimental approach has been developed based on the quantitative, local, dynamic and in situ analysis of meat during cooking (Bouhrara et al., 2011). This approach is not based on any reductionist hypothesis by studying an intact sample at the scale of the consumed food, or on the simplifying assumption of taking into account the spatial variations of temperature in the sample. Rather it is based on original developments in high-field nuclear magnetic resonance imaging and on image processing in order to map deformation and water content (Bouhrara & Bonny, 2012; Bouhrara, Lehallier, Clerjon, Damez, & Bonny, 2012). Fig. 4 gives an overview of all the quantitative parametric maps (deformation, temperature and water content) obtained during the heating of a bovine biceps femoris muscle. The results mainly show increased deformation with temperature in several phases whose characteristics depend on the muscle composition, and a decrease in the water content with temperature (Bouhrara, Clerjon, Damez, Kondjoyan, & Bonny, 2012). Monitoring a cooking process also involves temperature control. MRI thermometry is a well known technique, but is not discussed here because it does fall within the field of product quality measurements. 4.2.2. MRI and the viscoelastic properties Mechanical properties are of great interest in meat and fish products, from raw material to final product. A new investigation method, magnetic resonance elastography (MRE) based on using MRI to track a mechanical wave in the product, has emerged from biomedical research (Manduca et al., 2001). It is being used increasingly in food science as it is a non destructive method of obtaining viscoelastic properties locally (Gruwel, Latta, Matwiy, & Tomanek, 2010). This method is in competition with another transient shear wave propagation imaging technique, that of supersonic shear imaging (Bercoff, Tanter, & Fink, 2004) performed on heated bovine muscle (Sapin-de Brosses, Gennisson, Pernot, Fink, & Tanter, 2010) which has also emerged from biomedical research. 4.2.3. MRI and fat issues The fat content and its distribution through the muscle are important factors in meat palatability. Fat contributes not only to the texture and juiciness but also to the taste and smell of the final product (Dransfield, 2008). MRI has been investigated as a method for imaging the distribution of muscle and fat with a T1 weighted spin echo sequence to increase the contrasts between muscle and fat tissues. This method has been applied in samples of fish (Brix, Apablaza, Baker, Taxt, & Grüner, 2009; Toussaint et al., 2005) with a T1 weighted spin echo sequence to increase the contrasts between muscle and fat tissues and meat (Davenel et al., 2012). The T1 weighting technique combines the benefits of speed, contrast, and image clarity in images highlighting the fat distribution (Tingle, Pope, Baumgartner, & Sarafis, 1995). Lipids present in foods must also be controlled to improve the nutritional value of processed products. An original approach based on diffusion-weighted MRI for imaging the distribution of fat in meat has been developed at INRA (Clerjon & Bonny, 2011; Clerjon et al., 2012). This technique relies on the considerable difference between the apparent diffusion coefficients of protons in water molecules and lipids: the more protons are mobile (water molecule protons in muscle fibers), the more their signal is attenuated. It is therefore possible to cancel the water signal and specifically image lipids. This high-resolution imaging has been applied to lipid imaging in fried meat. It allowed the determination of the profile of oil uptake with a precision of 0.1 mm, ten times greater than with biochemical analysis (Fig. 5). Another paper studied oil uptake in Japanese tempura after frying, quantified by

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Fig. 4. For a 5 cm biceps femoris bovine muscle sample, at four average temperatures in the sample. (A) Temperature maps obtained by numerical simulation, (B) corresponding T2*-weighted MR images (DIs). (C) Corresponding representations of deformation as a function of direction and magnitude calculated by nonlinear optimal registration from two consecutive DIs. (D) Corresponding proton density maps.

T1-weighted, T2-weighted and proton density-weighted MRI (Horigane, Motoi, Irie, & Yoshida, 2003). 4.2.4. MRI and salt issues As explained above, 23Na is a nucleus that gives signal in NMR experiments; 23Na MRI is therefore feasible. However, the absolute sensitivity of 23Na is almost 10 times lower than 1H sensitivity, making the use of 23 Na MRI a challenge for food scientists. However, several teams have performed salt content mapping in meat and fish products in order to optimize salting processes and, of course, reduce salt content in food. Initially, “imaging” was a one-dimensional 23Na MRI experiment allowing the extraction of sodium profiles in pork meat during brining (Guiheneuf, Gibbs, & Hall, 1997). Later 23Na MRI was used for the 2D control and optimization of brining in fish and meat. The structure affects the salt diffusion and distribution. Those have been investigated with 23Na MRI, in salmon and cod, with the structure observed by 1H NMR and optical microscopy (Aursand, Erikson, & Veliyulin, 2010; Aursand et al., 2009; Erikson et al., 2004; Gallart-Jornet et al., 2007; Veliyulin & Aursand, 2007). In brief, the higher the density of the raw material structure, the lower the salt diffusion. Fat content is also a barrier to salt diffusion. Imaging fat distribution on the same sample during the same experiment using 1H MRI and imaging salt distribution using 23 Na MRI demonstrates this barrier effect (Renou, Bonny, Foucat, & Traore, 2007; Veliyulin, Aursand, Erikson, & Balcom, 2009). The control of salt and water diffusion in meat during brine curing is another important application using 23Na magnetic resonance imaging (MRI) and 23Na NMR relaxometry for porcine (Renou, Benderbous, Bielicki, Foucat, & Donnat, 1994; Vestergaard, Risum, & dler-Nissen, 2005) and bovine (Bertram, Holdsworth, Whittaker, & Andersen, 2005) meat. Hansen, van der Berg, Ringgaard, Stodkilde-Jorgensen, and Karlsson (2008) showed that the diffusion coefficient increases during curing, suggesting microstructural changes in the meat. The diffusion behavior

of NaCl in regions of meat with connective tissue/fat is distinctive from regions with pure myofilament tissue. The greater shrinkage in the direction across muscle fibers suggests that the curing induced shrinkage of the transverse structures rather than reduction in longitudinal structures. Quantitative 23Na MRI has, however, always been problematic due to the well-known partial salt invisibility phenomenon caused by the extremely short relaxation compounds of the sodium bound to macromolecules. It has been demonstrated that the SPRITE MRI sequence provides better quantification of sodium than a classic spin echo MRI sequence (Veliyulin, Egelandsdal, Marica, & Balcom, 2009). In order to assess bound Na + ions, the double quanta 23Na MRI has been investigated in resin model samples (Mouaddab et al., 2007). This technique uses the quadripolar interaction between the bound Na+ ions and macromolecules and it is promising for mapping salt in food products as a function of its bonding strength. Another solution for better quantification in salt mapping is to take into account RF field heterogeneities and developments are in progress in this direction at INRA. Lastly, biomedical studies often seek 23Na signal enhancement by using smart sequences (Heiler et al., 2011; Wetterling et al., 2012). These new approaches are based on either chemical shift imaging, or on the use of ultra short time-to-echo (TE) sequences intended to overcome the rapid signal decrease due to the short relaxation times of sodium. Although these technique are difficult to implement and need complicated post treatments, food scientists should use them to improve their 23Na MRI and thus better control the salting processes. 4.2.5. MRI and muscle structure issues MRI can be applied in several ways to provide structural information on muscle. Diffusion tensor imaging (DTI) is based on the measurement of diffusion coefficients in at least 6 directions. DTI is known for depicting fiber organization in muscle (Basser, Mattiello, & Lebihan, 1994). This DTI has been applied to bovine muscle proving its ability to

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Fig. 5. Transversal slices of a raw (top) and fried (bottom) bovine meat at 130 °C. We can observe intramuscular fat and oil that have penetrate several millimeters into the fried sample. From these images, the average profile was extracted of oil penetration after a 130 °C and a 180 °C frying process. Temperature profiles measured in the samples during the frying process are also shown. Oil penetration is higher at 180 °C (~5 mm) than at 130 °C (~2.5 mm).

analyze intra voxel fiber orientation and distribution (Bonny & Renou, 2002). More recently, Damez, et al. (2012) investigated the ability of DTI to acquire intra voxel structural information such as fiber type and diameter, arguing that diffusion-weighted intensity attenuation, able to exhibit hindered and restricted diffusion, permits to gain access to structural information. Pérez-Palacios et al. (2011) showed that the feeding background of the Iberian pig can be elucidated by MRI anatomical images associated with computational muscle-driven texture feature analysis. Moreover, susceptibility-weighted images can be used to study muscle structure (Bonny, Laurent, & Renou, 2001; Laurent, Bonny, & Renou, 2000) as connective tissue presents contrasted magnetic susceptibility. Finally, it is worthwhile noting that MRI developments for meat science applications are often published in non food journals, contributing to the improvement of MRI not only for food science but also for the biomedical area. 5. X-ray assessment Since the introduction of the Kartridg Pak Anyl Ray Fat Analyzer (Kartridg Pak Co., Model 316-4A, Davenport, IA, U.S.A.) in the 70s, based on low X-ray energy absorption (Gordon, 1973), useful new X-ray technology has mainly been derived from medical applications progressively introduced in the meat industry. X-ray micro-computed tomography (μCT) is a useful tool mainly because it is a noninvasive method of imaging under normal environmental conditions and does not require any sample preparation procedure. The degree of X-ray absorption is determined by the component densities of the product. The resolution of a few microns allows showing detailed internal structures of products to be seen with the advantage of 3-D models (Adedeji & Ngadi, 2009). In order to investigate variations in the fatty acid composition of the fat-fraction, and variations of density

in the meat-fraction, X-ray phase-contrast tomography measurements were carried out using a grating interferometric set-up at the ID19 beamline at the European Synchrotron Radiation Facility (ESRF) in Grenoble, France (Jensen et al., 2011). The method has been demonstrated in a set-up using a conventional X-ray tube (Donath et al., 2010), paving the way for use in an abattoir environment. Further work is needed before the technique can be used online on conveyor belt production lines, but a proposal has already been made for a grating-based interferometry scanning system (Kottler, Pfeiffer, Bunk, Grünzweig, & David, 2007). CT was used with an appropriate calibration equation to non-destructively analyze entire hams in a commercial type dry-curing process (Håseth, Sørheim, Høy, & Egelandsdal, 2012; Santos-Garcés, Muñoz, Gou, Sala, & Fulladosa, 2012) and more recently Picouet, Gou, Fulladosa, Santos-Garcés, and Arnau (2013) have developed a simplified methodology based on a unidirectional diffusion model and CT measurements for assessing salt diffusion during ham salting. One accurate tool for analyzing body composition in different species is dual-energy X-ray absorptiometry (DXA). The principle of DXA is to couple two absorption measurements, one at low X-ray energies (e.g., 62 keV) dependent on both fat content and sample density, the other at higher energies (e.g., 120 keV) mainly dependent on density. Coupling and subtracting one from the other gives the fat content with great accuracy. Therefore DXA provides reliable information about mass and percentage of lean tissue and fat, especially in sheep (Hunter et al., 2011; Pearce et al., 2009) and in pig (Kremer, Fernandez-Figares, Foerster, & Scholz, 2012; Marcoux, Faucitano, & Pomar, 2005), giving bone mineral content and bone mineral density (Kremer et al., 2012; Ryan, Lynch, & O'Doherty, 2011). Widespread online utilization is not far off, as acquisition with the DXA apparatus is becoming increasingly rapid. FOSS (Hilleroed, Denmark) developed an on-line DXA system to measure fat content at production speed (up to 22 tons/h) that can also detect foreign bodies (Fig. 6a). Recently, an online X-ray system has been introduced for beef and pork trim analysis for fat/lean ratio, and bone detection and batch control (SensorX by Marel hf, Iceland)(Fig. 6b). Because DXA gives information only about carcass composition and tissue content, coupling it with a non destructive imaging technique like MRI seems very promising (Kremer et al., 2012). 6. Infrared spectroscopy Infrared (IR) spectroscopy is based on the principle that the chemical bonds in organic molecules absorb or emit infrared light when their vibrational state changes. Large changes in vibrational state are observed in the near IR part of the spectrum (NIR), and sometimes up to the visible, while primary vibrations are produced in the mid IR region. A major challenge in applying IR spectroscopy to animal production is sample presentation (Rinnan, Berg, & Engelsen, 2009), since transmission is inappropriate for opaque solids. Interrogation of NIR datasets by increasingly powerful and sophisticated chemometric techniques continues to improve calibration robustness and accuracy. A recent review describes the applications of near infrared spectroscopy in muscle food analysis from 2005 to 2010 and presents the advantages of NIR spectroscopy in terms of operating speed and possible implementation of in-line, on-line or at-line process monitoring (Weeranantanaphan, Downey, Allen, & Sun, 2011). Several IR spectroscopy techniques exist. The main differences are the bandwidth and the optically measured parameters (transmission, reflection, diffusion, scattering, etc.). Treatment also differs according to the use or not of Fourier Transformation (FT-IR spectroscopy) before exploiting the spectra. The review below deals with both NIR and FT-IR. At the laboratory scale, food scientists explore IR spectroscopy to answer several kinds of questions. The quantification and qualification of fat in meat and fish products can be done by IR spectroscopy. Ziadi, Maldague, Saucier, Duchesne, and Gosselin (2012) developed a new method using VIS and NIR light transmission to evaluate the quality of beef meat based on marbling detection. They demonstrated that by

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Fig. 6. X-ray industrial apparatus. a: Dual source X-ray analyzer MeatMaster from FOSS, b: SensorX system from MAREL.

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using NIR light in transmission mode, it is possible to detect the fat not only on the surface, as in traditional methods, but also under the surface. Moreover, by combining the analysis of the two sides of the meat sample, it is possible to estimate volumetric marbling which is not accessible by visual methods commonly proposed in computer imaging. The fat content in fish has often been studied with NIR transmittance spectroscopy (Nortvedt, Torrissen, & Tuene, 1998; Solberg & Fredriksen, 2001; Wold & Isaksson, 1997; Wold, Jakobsen, & Krane, 1996). Due to the relatively small size of fish, it is possible to work in transmittance giving global information on the whole fish and not only on the surface area. The fatty acid composition of pork fat determines its processing quality and NIR spectroscopy provides information on fatty acid composition. FTIR spectroscopic methods were evaluated on pork back and breast fat, directly on fat slices and fat extracts. The results showed the validity of infrared spectroscopy for estimating SFA (saturated fatty acids), MUFA (monounsaturated fatty acids), PUFA (polyunsaturated fatty acids), C16:0, C18:0, C18:1 and C18:2 contents in fat extracts (Ripoche & Guillard, 2001). Sánchez-Alonso, Carmona, and Careche (2012) associated NIR with Raman spectroscopy to obtain the free fatty acid composition and oxidation state in hake filets during frozen storage. NIR spectroscopy can be used directly on the surface of food to produce biochemically interpretable “fingerprints.” FT-IR is used to measure biochemical changes within the meat substrate, enhancing and accelerating the detection of microbial spoilage. FT-IR measurements can be taken directly from the meat surface using attenuated total reflectance. Quantitative interpretation of FT-IR spectra is possible using advanced chemometric methods and allowing estimates of bacterial loads to be rapidly calculated directly from the meat surface (Ammor, Argyri, & Nychas, 2009; Ellis, Broadhurst, Kell, Rowland, & Goodacre, 2002). The same kind of approach is used for detecting changes in the flesh of Atlantic salmon related to the numbers of bacteria present (Tito, Rodemann, & Powell, 2012). More generally, NIR spectroscopy has been used to evaluate the freshness of fish (Nilsen, Esaiassen, Heia, & Sigernes, 2002), pork meat (Chen, Cai, Wan, & Zhao, 2011) and chicken breast (Grau et al., 2011) during storage. The structure of meat and fish products contributes to their final quality. Scattering coefficients depend on meat structural properties such as sarcomere length and collagen concentration. Structural properties are key factors in determining beef tenderness. Spatially resolved diffuse reflectance used to give the scattering coefficients of beef samples was measured with a fiber optical probe in the VIS-NIR bandwidth (450–950 nm). Indeed, scattering coefficients were associated with a higher cooked Warner–Bratzler shear (WBS) (Xia, Berg, Lee, & Yao, 2007). Myofiber diameter was also successfully studied in brined pork with FT-IR microspectroscopy (Bocker, Ofstad, Bertram, Egelandsdal, & Kohler, 2006). More generally, NIR spectroscopy (NIRS) is a suitable tool for obtaining structural information in fish (Isaksson, Swensen, Taylord, Fjaera, & Skjervold, 2001) and meat (Liu et al., 2003). To conclude on structure measurements, it is noteworthy that H.J. Swatland conducted much work in the 90s on the development of optical probes to assess meat and meat product quality. He is one of the rare meat scientists to have explored the capacity of polarized light. Muscle is highly anisotropic due to fiber arrangements, and polarized light gives different information according to the angle between light polarization and meat fibers. For instance, NIR birefringence, measured by a polarized NIR (800 nm) light beam can be used to obtain structural information in pork meat related to cold shortening and pH-related paleness (Swatland, 1995). Besides structural considerations, water is obviously another important factor in meat and fish. NIR spectroscopy was for instance applied to predict drip loss in pork samples. The results indicate that NIRS enables the classification of pork longissimus muscles with a higher or lower water-holding capacity, thus a drip loss lower than 5% or higher than 7% (Geesink et al., 2003). Moisture content prediction in smoked

salmon is a way of controlling the salting process (Huang, Cavinato, Mayes, Bledsoe, & Rasco, 2002). Identification and authentication are other applications for which NIR spectroscopy is a valuable tool. For example, NIRS analysis was used to predict the proximate chemical composition and identify the rearing system of European sea bass (Xiccato, Trocino, Tulli, & Tibaldi, 2004). This spectroscopy was also used to identify (beef, pork, lamb and chicken) and authenticate different homogenized meat muscle species. The models (principal component analysis (PCA) and dummy partial least-squares regression (PLS)) correctly classified more than 80% of the meat sample muscles according to the muscle species (Cozzolino & Murray, 2004). It can be used to reliably discriminate between wild and farmed sea bass, achieving the same classification performance as classification methods that use chemical properties and morphometric traits (Ottavian et al., 2012). Halal verification purposes are increasingly taken into account. In this way, FTIR spectroscopy can be used for the detection and quantification of pork in beef meatballs (Rohman, Sismindari, Erwanto, & Che Man, 2011). Lastly, it is a solution for evaluating metal pollutants in fish (Abdel-Gawad, Ibrahim, Ammar, & Ibrahim, 2012). Several recent reports have dealt with the thermal denaturation of gel and films from meat and fish proteins studied with NIR spectroscopy, as this technique gives information on the primary structure of proteins. FTIR spectroscopy of acid soluble collagen and gelatin from skins and bones of Nile perch showed that conversion of collagen to gelatin leads to loss in the triple helical structure and a decrease in molecular order (Muyonga, Cole, & Duodu, 2004). Gelatin derived from beef, pork and fish skin sources was used to manufacture films. In addition, FTIR spectroscopy was utilized to assess the composition of various gelatin sources to determine differences in composition of these sources and ultimately, in overall functionality. FTIR spectra showed that plasticizer and gelatin were well mixed and interacted well together (Nur Hanani, Roos, & Kerry, 2012). Surimi is an appreciated fish-meat gel and VIS-NIRS can be used to optimize its heat treatment (Uddin, Okazaki, Ahmad, Fukuda, & Tanaka, 2006). Regulatory considerations can be satisfied, for example, for the discrimination of frozen-thawed fish (Uddin et al., 2005) or the differentiation between Duroc and Iberian pork (del Moral et al., 2009). Folkestad et al. (2008) described a device for rapid and non-invasive measurements of fat and pigment concentrations in live and slaughtered Atlantic salmon by visible and near infrared (VIS/NIRS) spectroscopy measurements of live/whole fish and filet. On-line devices also mean measurements on the slaughterline, with the main application making use of the capacity of NIRS for the early prediction of drip loss in pork. The results demonstrate that NIR measurements (900–1800 nm) acquired during a 6 min period starting only 30 min post exsanguination through a fiber optic probe in combination with multivariate data analysis can be used for predicting drip loss 24 h after slaughter (Forrest et al., 2000). Ortiz, Sarabia, Garcia-Rey, and de Castro (2006) validated NIRS as a tool for the on-line classification of 117 dry-cured ham samples according to their pastiness, color, crusting, marbling and ring color, with the samples being scanned by a remote reflectance fiber optic probe, helping to choose the risks of false non-compliance (α) and false compliance (β) for each sensorial variable according to the needs of the decision-maker. If both probabilities are equal, that is α = β, the values reachable are 8.0, 6.4, 5.2, 2.3 and 0.4% for marbling, crusting, ring color, color and pastiness, respectively. A recent study (Prado, Fernandez-Ibanez, Gonzalez, & Soldado, 2011) investigated the potential of on-site portable NIRS instrumentation-based models to predict three microbiological parameters to establish if pork meat is acceptable or not for consumption. This methodology makes possible the on-site prediction of the microbiological status of pork meat. Finally, NIR spectroscopy is a suitable non-destructive method for the on-line monitoring and control of the drying process in fermented sausages by measuring superficial water activity and moisture content (Collell, Gou, Arnau, Muñoz, & Comaposada, 2012).

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NIRS sensors are already being marketed and are used in food science. The i-LAB TA hand held spectrometer from IR to visible can be used for contact measurements on flat surfaces (Optoprim, 2013b). The Corona Plus is a compact industrial VIS-NIR reflection/transmission spectrometer from Carl Zeiss (Zeiss, 2013) designed for use under industrial conditions, even in harsh environments. These systems can be used for the online measurement of various optical properties in quality assurance at every stage of the production process across a wide range of industries. Shimamoto, Hiratsuka, Hasegawa, Sato, and Kawano (2003) demonstrated the rapid and non-destructive determination of fat content in frozen skipjack using a portable near infrared spectrophotometer, the FT 20 (Fantec Research Institute, Kosai, Japan), initially developed for fruit quality assessment. Besides commercial IR sensors, work is being performed on a very inexpensive single frequency infrared sensor for non-destructive fish fat detection (Buniyamin et al., 2011). A sensor in a smartphone? Pugner, Knobbe, Gruger, and Schenk (2012) from the Fraunhofer Institute, realized a near infrared spectrometer that could measure water, sugar, starch, fat and protein content in food products. The system employs NIR technology that can penetrate several centimeters below the outer surface of foodstuffs by shining a broadbandwidth light on the item to be tested — for instance a piece of meat. The resulting spectrum indicates what amounts of which substances are present in the foodstuff. The really novel thing about this spectrometer is its size (15 × 10 × 14 mm) and its few milliwatts of power consumption that has the potential to be implemented in a smartphone! 7. NIR hyperspectral imaging Spatially resolved NIRS involves acquisition of an NIR spectrum for each pixel of a micro or macroscopic image. Chemometric analysis determines which parts of the spectra contain discriminate information for a given parameter and a 2D representation at the chosen wavelength provides contrasted images according to the target parameter. Kirschner, Ofstad, Skarpeid, Host, and Kohler (2004) presented the results of a Fourier transform infrared (FT-IR) microspectroscopic study using conventional FT-IR microscopy and FT-IR imaging to detect the denaturation process during heating of myofibrillar and connective tissue proteins (raw, 45, 60, and 70 °C) spatially resolved in bovine muscle. The infrared spectra of both compounds revealed that the major spectral changes involved an increase in the β-sheet structure and a decrease in the α-helix structure. These changes appeared to be much more pronounced for the myofibers than for the connective tissue. These conformational changes could be correlated to the denaturation of the major meat proteins, such as myosin, actin, and collagen. The thermal denaturation of proteins from collagen, elastin, and myofibers from skeletal muscle have been studied and characterized, for the first time by an INRA team at the Synchrotron Soleil in Saclay, France, taking into account the metabolic and contractile fiber types in situ (Astruc et al., 2012). The secondary structure of proteins was investigated by synchrotron radiation FT-IR microspectroscopy. Whatever the target protein components, increasing temperature resulted in a decrease in the α-helix secondary structure and an increase in the β-sheet structure. The hyperspectral imaging (resolution of 0.58 mm/pixel) technique (890–1750 nm) used in tandem with multivariate analyses was investigated to identify and authenticate different red meat species (pork, lamb and beef). The results clearly showed that the combination of hyperspectral imaging, multivariate analysis and image processing has great potential as an objective and rapid method for identifying and authenticating these species (Kamruzzaman, Barbin, ElMasry, Sun, & Allen, 2012). Other applications of hyperspectral NIR imaging include the determination of contents such as oleic acid, total unsaturated fatty acid and fat content in raw beef (Kobayashi, Mori, Nishino, Toyota, & Nakauchi, 2012), and the color distribution in salmon filet (Wu, Sun, & He, 2012).

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An interactance measurement, where the light was transmitted into the meat and then back scattered to the surface combined with X-ray computed tomography (CT), was used to measure salt and fat distribution, without contact, in salted and smoked salmon filets (Segtnan et al., 2009). Since CT responses for salt are affected by fat content, to investigate this phenomenon, the research team calculated the predicted fat content with the NIR interactance measurements and added this fat information in the CT modeling process. The combination of three X-ray energy levels (80, 110, and 130 kV) gave the best CT calibrations for NaCl, with the average prediction errors (root mean square error of cross-validation (RMSECV)), RMSECV = 0.40% NaCl and R = 0.92. Adding fat predictions based on NIR interactance imaging further improved the NaCl prediction performance, giving RMSECV = 0.34% NaCl and R = 0.95. It was also found that NIR interactance imaging alone was able to predict NaCl contents locally in salted salmon filets with RMSECV = 0.56% and R = 0.86. A review dealing with the applications of VIS/NIR imaging spectroscopy for the inspection of fish and fish products such as finding blood, melanin spots and nematodes, determining filet composition, determining freshness and detecting a frozen/thawed cycle has been published recently (Mathiassen, Misimi, Bondo, Veliyulin, & Ostvik, 2011). The authors observe that the online (i.e. those with demonstrable industrial-scale speed and cost) imaging technologies are to a limited degree capable of measuring all properties of interest, and that the offline technologies have less limitations and greater capabilities to inspect fish products with respect to fat, protein, water, salt, freshness and anatomy. Although it is much more complicated to develop an on-line imaging system than simple on-line spectrometers, some teams have taken up this challenge, motivated by the wide range of potential applications in food science. An on-line NIR system based on non-contact transflectance measurements for multi-spectral imaging was developed for industrial R&D projects to study the effect of different drying processes on water content and distribution in dried salted fish (Wold et al., 2006). The non-contact approach facilitates efficient and non-complicated on-line systems. Multi-spectral imaging allows robust and representative sampling when the chemical composition is unevenly distributed in the samples. The 760–1040 nm NIR region is well suited for the estimation of water, fat and protein, thus opening the way for many potential applications for foods and other bio-materials. Wu, Shi, et al. (2012) and Wu, Sun, et al. (2012) proposed the rapid prediction of moisture content of dehydrated prawns using an online hyperspectral imaging (380–1100 nm) system. Moreover, a commercial sensor exists and was applied in a recent study. The complete system consisting of a conveyor belt, an NIR imaging scanner (QV500, Tomra Sorting Solutions, Asker, Norway, Fig. 7), a flow weigher and grader and a host computer with synchronizing software and a sorting algorithm was developed and tested for the on-line sorting of meat trimmings into categories. Some inaccuracies emerged relating to on-line fat measurements due to inhomogeneous meat trimmings, leading to the systematic under-estimation of the fat percentage in low-fat categories and the over-estimation in high-fat categories (2 percentage points) (Måge, Wold, Bjerke, & Segtnan, 2013). These biases can be reduced by e.g. improving on-line fat measurement technology. 8. Raman spectroscopy Raman spectroscopy, in which the decay of vibration is observed after strong excitation of the sample (mainly with a laser), is a variant of mid-IR (FT-IR) spectroscopy. In contrast to IR spectroscopy which mainly highlights primary protein structures, Raman spectroscopy mainly points out modifications in secondary protein structures such as α-helix and β-sheets and is known to be a rich source of information on amino acid residues (Overman & Thomas, 1999). Smaller portions of sample are required, compared with FT-IR, and instrumentation can be less expensive and portable. Raman spectroscopy is relatively insensitive to water and hence does not suffer from water interference, so Raman spectroscopy requires little pretreatment of the sample without e.g. cryo-sectioning and

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snap drying often needed with FT-IR analysis. Raman spectroscopy is a promising technique for assessing the quality of meat and fish and a review of its applications in this area is available (Herrero, 2008). Below, we highlight the main recent applications of this technique. For instance, Raman spectroscopy is a valuable tool for measuring the structural changes of hake filets induced by freezing and frozen storage (Careche, Herrero, Rodriguez-Casado, Del Mazo, & Carmona, 1999). Raman spectroscopy was used successfully to study the in situ protein structure in raw and salted surimi from Pacific whiting, and in gels formed by setting (32 °C), cooking (86 °C) and setting followed by cooking. This approach presents the advantage of studying the nature of protein interactions and conformational changes directly in surimi, without producing artifacts which may occur during the sample preparation (Bouraoui, Nakai, & Li-Chan, 1997). Raman spectroscopy also reveals protein and water structural changes in fish surimi during gelation (Sánchez-González et al., 2008). The synergies between Raman and FT-IR are the subject of an interesting paper (Bocker et al., 2007). The correlation patterns between FT-IR and Raman microspectroscopic data obtained from pork muscle tissue, improve the interpretation and band assignment of the spectral features observed. Pork muscle tissue was subjected to different processing factors, including aging, salting, and heat treatment. Multiblock principal component analysis was utilized for data analysis. The results showed that both FT-IR and Raman spectra were useful to assess heat treatment and then variation in salt content. Thermal treatment and salt addition were again at the center of a Raman spectroscopy study (Herrero, Carmona, Lopez-Lopez, & Jimenez-Colmenero, 2008) in which Raman spectroscopy, texture, proximate composition, and water binding analysis were carried out to evaluate the effect of thermal treatment and/or salt addition to meat batter. Raman spectroscopy analysis revealed a significant decrease in α-helix content accompanied by an increase in β-sheets resulting from heating. Raman spectroscopy is a potential tool for determining beef sensory qualities. Indeed, the Raman method can predict texture and tenderness, which are the predominant factors for determining the overall acceptability in the Western world (Beattie, Bell, Farmer, Moss, & Desmond, 2004). A laboratory method has also been developed to evaluate and predict tenderness, juiciness and chewiness of fresh, uncooked pork loins (Wang, Lonergan, & Yu, 2012). Still in the field of meat sensory attributes, a preliminary investigation by (Schmidt, Scheier, & Hopkins, 2013) using Raman spectra to assess the relationship between shear force and cooking loss in sheep meat has been reported. The results are promising and show the suitability of Raman spectroscopy to predict tenderness and cooking loss. Illegal fish drugs used in aquaculture have raised serious concerns due to their negative effects on public health and the environment. In a recent study, surface-enhanced Raman spectroscopy was successfully applied to analyze prohibited aquaculture drugs including enrofloxacin, furazolidone and green malachite (Zhang et al., 2012). Fish gelatin can be used as an additional source of gelatin, especially for religious and social reasons. The manufacture of fish gelatin does reduce processing waste material and result in added-value products. FT-Raman spectroscopy confirmed the role of amino acids, hydrophobic amino acids and α-helix content in providing a high strength gelatin (Badii & Howell, 2006). Animal fats and oils have been analyzed with Raman spectroscopy. The results show that FT-Raman spectra not only provide information on the degree of unsaturation, but also on the balance between the amounts of SFA, MUFA, and PUFA. The scattering intensities near different Raman shifts (3013, 1663, and 1264 cm−1) show high correlations with the fatty acid profile determined by gas chromatography, proving the suitability of FT-Raman spectroscopy for fat qualification (Baeten, Hourant, Morales, & Aparicio, 1998; Hourant, Baeten, Morales, Meurens, & Aparicio, 2000). More recently, the same kind of study has been performed on pork meat (Olsen, Rukke, Flåtten, & Isaksson, 2007).

A portable Raman sensor system based on a miniaturized optical bench incorporating an excitation light source provided by a 671 nm microsystem diode laser has been developed for rapid (less than 10 s) pork meat spoilage identification (Sowoidnich, Schmidt, Kronfeldt, & Schwagele, 2012). The backscattered Raman radiation from the sample is analyzed by a custom-designed miniature spectrometer with a resolution of 8 cm−1 fiber-optically coupled to the sensor head. The complex spectra were analyzed by a PCA multivariate statistical tool to determine the spectral changes occurring during the storage period. A distinction between fresh and spoiled meat was found in the time slot of 7–8 days after slaughter. Moreover, polarized Raman spectra were measured on oriented cuts of pork and turkey with the previous device. Fresh meat slices were stored at 5 °C and measured for a consecutive time period of 10 days. Measurements were performed using a laser beam oriented perpendicularly to the long axis of the muscle fibers. In this arrangement, the fibers were aligned either parallel or perpendicular to the polarization direction of the laser source. The principal components analysis (PCA) method was used to determine a clear separation of the meat samples for fresh meat according to the orientation (parallel or perpendicular) using the first two principal components. During the storage period, this separation subsequently vanished due to the aging process and due to an increase in the microbial spoilage of the meat surface. Furthermore, specific changes of conformation-sensitive Raman bands were recognized, notably a decrease of the intensities of α-helical protein conformation (Al Ebrahim, Sowoidnich, Schmidt, & Kronfeldt, 2011). A recent study compared FT-IR and Raman spectroscopy for spoilage determination and demonstrated for the first time that Raman spectroscopy as well as FT-IR spectroscopy can be used reliably and accurately for the rapid assessment of meat spoilage (Argyri et al., 2013). These methods, before being applied within the meat industries, need however appropriate prediction models and databases. 9. UV–visible fluorescence Fluorescence spectroscopy involves using a beam of light, usually UV light, that excites the electrons in the molecules of certain compounds and causes them to emit lower-energy light. The specie (a molecule or atom) is first excited by absorbing a photon of light from its ground electronic state to one of the various vibrational states in the excited electronic state. Collisions with other molecules cause the excited molecule to lose vibrational energy until it reaches the lowest vibrational state of the excited electronic state. The molecule then drops back down to one of the various vibrational levels of its ground electronic state, emitting a photon in the process. As molecules can drop down into any of several vibrational levels in the ground state, the photons emitted will have different energies and thus frequencies. Therefore analyzing the different frequencies of light emitted in fluorescent spectroscopy, along with their relative intensities, makes it possible to determine the structure of the different vibrational levels. Tryptophan is an important intrinsic fluorescent probe that can be used to assess the nature of the tryptophan microenvironment in muscle. Proteins that lack tryptophan can be attached to an extrinsic fluorophore probe. For opaque samples such as meat products, front face fluorescence is used, and since these products contain tryptophan, this technique has been used in meat and muscle science to investigate sample structure without using extrinsic fluorophore probes. A recent paper has provided an overview of fluorescence spectroscopy measurement for the quality assessment of food systems (Karoui & Blecker, 2011). Lastly, it is worthwhile noting that fluorescence is a selective method, as the species excited depend on the excitation wavelength. Muscle tissues are oriented structures, often resulting in the anisotropy of their physical properties. A project managed at INRA has been launched to study the optical anisotropy of muscle using polarized spectrometric measurements, and to detect modifications of this anisotropy resulting from structural changes caused by meat processing. Steady-

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Fig. 7. QVision 500 Analyzer from TOMRA Sorting Solutions, Norway.

state measurements of front-face fluorescence anisotropy for different muscle tissues have been carried-out to investigate optical properties (Luc, Clerjon, Peyrin, & Lepetit, 2008) (Fig. 8). It has been observed that fluorescence anisotropy decreases post mortem, showing structural changes in tissues (Clerjon, Peyrin, & Lepetit, 2011). These studies also concerned post mortem structural modifications associated with the main processes involved in transforming muscle into food: cold shortening of the muscle (Luc, Clerjon, Peyrin, Lepetit, & Culioli, 2008), grinding and heating. Optical anisotropy is highly correlated with structure and its measurement could be used for structural evaluation, which is an important issue in food quality. This method is adaptable to other foods in the food-processing industry provided that they contain fluorescent compounds oriented preferentially (e.g., in vegetable fibers). Another application of fluorescence spectroscopy is the determination of the heterocyclic aromatic amines (HAA) in grilled meat (Sahar, Portanguen, Kondjoyan, & Dufour, 2010), since these components are naturally fluorescent. An original device coupling fluorescence detection and X-ray technology has been developed for detecting poultry meat eating quality. It can greatly increase the capacity for assessing the quality of poultry meat and perform fast and non-destructive testing (Zhao, Liu, Zhan, Shen, & Tu, 2011). Solid sample autofluorescence spectroscopy appears to be well suited for nondestructive determination of lipid oxidation level in minced poultry meat, and the method was used successfully to distinguish between rancid and fresh meat (Wold & Mielnik, 2000). Microbial spoilage on meat can be detected by fluorescence since tryptophan and NADPH (nicotinamide adenine dinucleotide phosphate-oxidase) fluorescence changes with

the growth of microorganisms. It appears that the intrinsic fluorescence spectra of aromatic-amino-acids + nucleic-acids (excitation: 250 nm, emission: 280–480 nm), tryptophan residues (excitation: 290 nm, emission: 305–400 nm) of proteins and NADH (excitation: 336 nm, emission: 360–600 nm), recorded on cod, mackerel, salmon and whiting filets at 1, 5, 8 and 13 days storage, can be considered as fingerprints that may allow discrimination between fresh and aged fish filets (Dufour, Francia, & Kane, 2003). This application of fluorescence spectroscopy has been successfully investigated on the surface of pork meat stored aerobically at 15 °C for 3 days (Oto et al., 2013). To the same end, a portable Y-type fiberoptic fluorescence spectroscopy measurement system was positively evaluated on fish (Wu, Hsiao, Chu, Hu, & Chen, 2012). Based on the autofluorescence of hydroxyproline, the quantification of connective tissue in ground beef has been successfully investigated (Wold, Lundby, & Egelandsdal, 1999). A rapid method based on front-face fluorescence spectroscopy was developed to monitor the texture of meat emulsions and frankfurters (Allais, Viaud, Pierre, & Dufour, 2004). Mercury and selenium contents were determined by fluorescence spectroscopy to evaluate human exposure to these elements through fish consumption in Spain and Portugal (Cabanero, Carvalho, Madrid, Batoreu, & Camara, 2005). A German team opened up new perspectives in food quality monitoring by developing miniaturized hardware concepts for carrying out fluorescence and Raman spectroscopic measurements using a compact and light handheld device as well as concepts for the use and integration of such a device in the logistic chain (Jordan et al., 2009). The device can be used to obtain characteristic changes in the quality and constitution of meat and how it changes over time. Another team concentrates

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which is rapid, ease to use, versatile and inexpensive, is one of the most powerful analytical techniques available to the animal production industries from feed manufacture to final product evaluation. The muscle is organized in sets of fiber bundles more or less aligned depending on type and functionality of the muscle. Looking to an index of anisotropy (such as impedances along/across the fiber direction) gives a valuable state of the meat structure. Biophysical meat properties in using an index of anisotropy could be assessed with polarized electromagnetic waves either visible, IR, UV, optical bands, microwave with horn antennae as well as conductivity. If a quality factor other then structural is to be assessed, a coaxial sensor is nevertheless required. Among the techniques overviewed, there is always an answer for each of the numerous quality issues in meat science. Moreover their combined use provides synergies and offers to the meat industry the promise of the perfect sensor for meat quality assessment! References Fig. 8. Experimental set-up to determine fluorescence anisotropy. The vector E gives the direction of the exciting light polarization. The sample rotates varying the angle γ between the meat fibers and the exciting light polarization direction. Observation of the emitted fluorescence intensity is done either parallel (I//) or perpendicular (I⊥) to the exciting light polarization direction.

its efforts on miniaturizing fluorescence devices for on-line measurements (Aït-Kaddour, Boubellouta, & Chevallier, 2011). Although desk spectrofluorimeters are often used for laboratory studies, a portable commercial sensor, the FLUO SENS Integrated (ESE, GmbH), is used for mobile measurement and online process monitoring (Optoprim, 2013a). As for the NIR band, fluorescence imaging can give localized information valuable for meat quality control. For instance, Kulmyrzaev et al. (2012) demonstrated the promising potential of a custom-designed fluorescence imager combined with multivariate statistical tools to discriminate different bovine muscles in relation to animal age, muscle type, and chemical and mechanical properties. 10. Conclusion Numerous studies have been carried out for many years to characterize meat tissues by means of their electrical properties, different types of meat tissues exhibiting different conductivity parameters depending on their structure and their composition. Spectral impedance measurements observed with increasing frequencies are mainly attributed to changes in membrane conductivity and ion and charged molecules mobility. X-ray beams at different energy levels have been developed for decades in medicine and other areas, making it possible to discriminate, fat bone and lean meat according to the energy absorption measured. Companies provide complete solutions using X-ray for meat trimming scanning, for fat assessment and/or foreign body detection. NMR and MRI are suitable tools for non destructive measurement of food properties with spectroscopic and relaxation based methodologies. MRI permits in situ multiparametric approach that must also be applied for the control and optimization of food processes. NMR and MRI require very often heavy laboratory apparatus, but efficient NMR portable devices are nowadays on the market and could be shortly used in meat industry. As a wavelength point of view, optical spectroscopy covers nearinfrared (NIR), infrared (IR), visible, and ultra-violet (UV) (including fluorescence). Because optical radiations propagate well in the air, optical spectroscopy can be used without contact. The interaction between the optical radiation and the sample under test can be assessed by measuring either the reflected, transmitted, scattered or diffused light, or several of these parameters. Optical instrumentation is quite inexpensive and easy to miniaturize allowing the development of portable devices suitable for industrial applications. Among optical spectroscopies, IR spectroscopy,

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