Oil uptake by beef during pan frying: Impact on fatty acid composition

Meat Science 91 (2012) 79–87

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Oil uptake by beef during pan frying: Impact on fatty acid composition S. Clerjon a,⁎, A. Kondjoyan a, J.M. Bonny a, S. Portanguen a, C. Chevarin a, A. Thomas b, D. Bauchart b a b

INRA, UR370 Qualité des Produits Animaux, F-63122 Saint-Genès-Champanelle, France INRA, UR1213 Unité de Recherches sur les Herbivores, F-63122 Saint-Genès-Champanelle, France

a r t i c l e

i n f o

Article history: Received 14 September 2011 Received in revised form 19 December 2011 Accepted 20 December 2011 Keywords: Meat Frying process MRI Diffusion Weighted Imaging Fatty acid composition Thermal modeling

a b s t r a c t Fat entering food during frying needs to be monitored to control the nutritional properties of the products: fat penetration and fatty acid (FA) composition. The large difference between the apparent diffusion coefficients of lipids and meat fibers allows the use of diffusion-weighted magnetic resonance imaging (DWI) to measure oil uptake profiles. This method, in association with analysis of FAs by gas–liquid chromatography, predicts nutritional changes. Beef samples from finishing cows given control feed or high FA supplemented feed were fried in olive oil at 130 °C and 180 °C. Frying oil penetration was quantified by computing oil signal profiles from 3D DWI. Oil penetration was deeper at 180 °C (5 mm) than at 130 °C (2.5 mm), consistent with oil penetration processes. Oil penetration evaluated with DWI was correlated (R² = 0.82) with biochemical analysis of FA composition. These results highlight the predominance of oil uptake over animal feed effects in the first millimeters of in-plane fried meat. © 2012 Elsevier Ltd. All rights reserved.

1. Introduction The public image of meat, which is linked to that of lipids, is relatively unfavorable, meat often being judged too fatty and too rich in pro-atherogenous fatty acids (FAs). The effects of breeding conditions and meat technological processes have been analyzed with a view to improving and securing qualities associated with lipids in beef for human consumption. Some authors have demonstrated the impact of rearing factors linked to animals (e.g. breed, age, sex and emotional stress) and their feeding conditions (dietary lipids and antioxidant supplements) on FA deposition and composition in muscles at slaughter (Habeanu, Durand, Gobert, & Bauchart, 2008) and of technological factors (maturation, packaging and storage) of the produced meats on lipoperoxidation (Gobert et al., 2010). In Europe, meat cuts from highest market value muscles are often grilled or pan-fried. Oil is most often used for pan frying, and can be taken up by the meat. Most studies dealing with oil uptake and its effect on human health concern the significant contribution of deepfat fried food to the consumption of saturated FAs, which are considered as a major factor increasing the risk of health disorders such as coronary heart diseases, cancer, diabetes and hypertension (Saguy & Dana, 2003). Frying is also related to the formation of some toxic compounds in food, such as acrylamide in carbohydrate foods (Taeymans et al., 2005), heterocyclic amines in meat products (Skog, Johansson, & Jagerstad, 1998), and oxidized FAs (Kalogeropoulos, Salta, Chiou, & Andrikopoulos, 2007). Some constituents of oil such as trans FAs or degradation

⁎ Corresponding author. Tel.: + 33 4 73 62 45 93; fax: + 33 4 73 62 40 89. E-mail address: [email protected] (S. Clerjon). 0309-1740/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2011.12.009

compounds may also be harmful (Paul & Mittal, 1997; Saguy & Dana, 2003; Singh & Tyagi, 2001). Some studies have focused on the effect of frying on the FA profile in animal products. In a recent study, it was shown that the FA profile of flesh from king salmon was modified by deep-fat frying, but remained unchanged with pan frying performed without adding oil in the pan (Larsen, Queck, & Eyres, 2010). However, comparison with previous studies was difficult owing to potential differences in salmon species and cooking parameters. The effect of pan frying in various culinary fats has been reported to increase the FA content of pork meat (Haak, Sioen, Raes, Van Camp, & De Smet, 2007): the FA composition of the pan-fried meat tended to change and become similar to that of the culinary fat used. This effect was more marked when meat was pan-fried in olive oil; this oil being very rich in monounsaturated fatty acids, it has a higher viscosity compared with the other seed oils commonly used (Kalogeropoulos et al., 2007), leading to a stronger adherence of oil on meat at the end of the frying process. Librelotto et al. (2008) reported effect of pan frying in olive oil on restructured lowfat or walnut-added beef steaks, final FAs content being dependent on the initial FAs profile. However, the penetration depth of oil in meat remained unknown and global fat uptake in meat is generally measured for enrobed or coated products (Akinbode, Ngadi, & Raghavan, 2009; Eyas Ahamed, Anjaneyulu, Sathu, & Kondaiah, 2007; Perlo, Bonato, Teira, Fabre, & Kueider, 2006). Repeatable measurements are difficult due to the difficult frying procedure standardization. This is not surprising considering the complexity of the transfer phenomena responsible for oil uptake during food frying. Most work on oil uptake mechanisms deals with the deep-fat frying of carbohydrate products such as french fries or sliced potatoes (Achir, Vitrac, & Trystram, 2010; Dana & Saguy, 2006; Mellema, 2003). Marked evaporation of water occurs during deep-fat frying, leading to crust formation at the surface of products, and forming

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a barrier to moisture and fat transfer (Adedeji & Ngadi, 2009). Surface phenomena involving adhesion and drainage forces (thickness, viscosity and surface tension of the oil layer carried on the product surface during removal) play a major role in oil penetration during food cooling. The complexity of these processes, which are not yet fully understood, has led to unreliable predictions in the literature. For example, it has generally been claimed that potatoes fried at lower temperature have a higher oil content than those fried at higher temperature (Kita, Lisińska, & Gołubowska, 2007; Pedreschi, Cocio, Moyano, & Troncoso, 2008). However, this phenomenon depends on the frying oil and on the frying time and in some other studies higher frying temperature increased or had no effect on the oil content of French fries (Dana & Saguy, 2006). Processes involved in oil uptake during pan frying are even more complex because they involve marked variations in oil temperature, spreading of the oil layer, which mixes with the meat juice, and meat flipping in the pan (Ou & Mittal, 2007). Hence it is very difficult to reproduce a given pan frying treatment accurately. In addition, even if the treatment is considered repeatable, oil temperature and meat surface temperature remain unknown, limiting the scope of the study and hindering the transposition of results to other frying conditions. MRI has no equal for non-destructively depicting intrinsic intramuscular fat distribution. With MRI it is possible to measure fat distribution before and after frying and thus to compute fat uptake during the process. In addition, 3D resolutions can be adapted to the anisotropy of penetration, with a higher resolution in the penetration direction. In the literature, fat imaging in muscle is based on diffusion-weighted imaging. It makes use of the large difference between the apparent diffusion coefficients of myofibers and of intramuscular fat and oil. Using a sufficiently large factor of diffusion attenuates the water signal, allowing detection of fat only. MRI has been used to study fat location in muscle, e.g. by Laurent, Bonny, and Renou (2000), who presented T1-weighted and chemical-shift selective inversion-recovery (CSSIR) imaging of fat in bovine semitendinosus muscle, and lipid evolution and migration during food processing, e.g. during cheese ripening (Mahdjoub, Molegnana, Seurin, & Briguet, 2003) and chocolate processing (Walter & Cornillon, 2002). MRI has also been used to study oil uptake in Japanese tempura after frying, which was quantified by T1weighted, T2-weighted and proton density-weighted magnetic resonance imaging (Horigane, Motoi, Irie, & Yoshida, 2003). Here we studied the lipid uptake during frying in olive oil applied to one face of beef samples under controlled, constant oil temperature conditions, the objective being to evaluate how the frying process changed the intrinsic FA composition and the total lipid content of the product. After the heat treatment, beef cuts were cooled in ambient air to mimic real practice. Temperature gradients were accurately measured in beef cuts during the frying and cooling periods. A fat diffusion-weighted imaging (DWI) method in muscle was developed to characterize oil penetration with an original approach in which spatial resolution was maximized in the direction of oil penetration in samples. In parallel with DWI, samples were sliced for GLC FA analysis.

2.2. Slaughter and sample preparation Normand cows were slaughtered at the experimental abattoir of the INRA Research Centre of Theix (France). For this study, 150 g samples of the longissimus thoracis (LT) muscle were removed from the carcase of two animals (one from the C group, one from the LEP group) and refrigerated at +4 °C for 24 h. They were aged at + 4 °C for 12 days under vacuum-packed conditions, and then frozen and stored at − 20 °C. At the beginning of each experiment the frozen meat samples were cut into cylinders (height 50 mm, diameter 30 mm), which were thawed in a water bath first at +10 °C for 3 h and then at +25 °C (for MRI acquisitions) for 2 h. Each beef sample was inserted into a cylindrical PVC sample holder open at one end. The meat surface exposed to the air was covered with Parafilm® to prevent oxidation by oxygen. The MRI image was acquired and the raw sample was removed from the PVC holder for the heat treatment. After frying, it was placed back in the PVC sample holder for MRI in the fried state. Finally, four slices were taken from each sample, with a slicer set at 2 mm, for biochemical analysis. Slices 2 mm thick were taken from the fried surface (0 to 2 mm, 2 to 4 mm, 4 to 6 mm and 21 to 23 mm). Table 1 lists the nine samples by diet and thermal treatments. A technical failure prevented us from obtaining MRI results for the B20 fried sample. However, this sample was normally fried and so was kept for FA analysis. 2.3. Thermal treatment A special device was built to immerse only one tip of the meat cylinder described above in an oil bath, all its other faces being thermally isolated by PTFE® (Fig. 1). The device was equipped with six needle thermocouples of diameter 1 mm. Five of these thermocouple needles were inserted through one of the PTFE® walls to reach the meat cylinder axis at different distances from the heated surface to measure the temperature gradient along the meat cylinder. These needle thermocouples (t2 to t6) were located 2, 4, 6, 10 and 20 mm from the heated surface. They were angled up at 30° from the horizontal plane to prevent direct contact with oil for those located near the surface of meat, and to reduce effects of heat conduction through the metal of the needle. Accuracy of the positioning of these five thermocouples was about ±1 mm. Thermocouple t1 was located as close as possible to the surface of the meat. To ensure repeatability of this position, the thermocouple was driven into the meat sample from the cylinder face opposite the one to be heated. The thermocouple needle was driven in until the experimenter could feel the point of the needle under his finger placed on the surface to be heated. This procedure ensured that the thermocouple was kept constantly at 0.7 mm (half length of the needle point) ±0.5 mm from the surface, at the risk of some undesired heat exchange by conduction along the needle. The device and the sample were held on an adjustable column to allow full control over the length (2 mm) of the meat cylinder immersed in the oil bath. The olive oil was purchased from a local retailer (brand “Bouton d'or”, Intermarché, France). A volume of 280 ml of oil was pre-heated in a cylindrical glass bath to the desired temperature (130 °C or

2. Materials and methods 2.1. Animals and diets Normand cull cows (48 to 60 months old, live weight 649 kg) were given, for a finishing period of 100 days, either (i) a basic diet based on concentrate (70%) and straw (30%) (diet C) or (ii) the same diet supplemented, per kg diet DM, with 40 g of lipids from extruded linseed (n-3 polyunsaturated FA source), associated antioxidants such as 155 IU of vitamin E (INZO, Château-Thierry, France) and 7 g of a mixture of plant extracts rich in polyphenols (Phytosynthèse, Riom, France) (diet LEP) (for details, see Gobert et al., 2010).

Table 1 Samples by thermal treatment and animal feed. Sample name

Frying temperature (°C)

Animal diet

B12 B13 B14 B15 B16 B17 B18 B19 B20

180 180 180 130 130 130 130 130 130

LEP LEP LEP LEP LEP LEP C C C

S. Clerjon et al. / Meat Science 91 (2012) 79–87

Fixation

81

t1 PTFE® t6

meat

t5

65 mm

t4 t2 t3

30° t7

Data acquisition system Olive oil

Heating plate with magnetic stirrer Fig. 1. Experimental heating device.

180 °C) and then stirred and maintained at this temperature throughout the experiment using a hot-plate. When the desired oil temperature was reached, the sample was immersed in the hot oil for 6 min. Temperature measurements were recorded throughout the experiment by a data logger (TC-08 thermocouple data logger, Pico Technology, United Kingdom) connected to a PC computer. At the end of the frying treatment, the sample was left to cool in the PTFE® holder for 20 min until the meat temperature reached 40 °C. The meat was removed from the PTFE® holder and placed in the PVC holder with the surface exposed to air again covered by Parafilm®, and a magnetic resonance image of the fried product was captured. 2.4. Thermal modeling The knowledge of meat temperature in the area where crust forms is crucial to analyzing frying results. However, interpreting temperature recordings is always very difficult owing to the high gradients near the meat surface during frying. Very small differences in temperature locations due to either small variations in initial sensor positioning or sensor movement during experiments cause very marked differences in the recording of meat temperature. Simple thermal simulations were performed to help in interpreting the temperature recordings in meat samples very close to their heated surface. Heat conduction in the meat cylinder was simulated in 3D with Comsol Multiphysics software 3.4. The boundary condition on the heated surfaces (bottom meat surface and 2 mm height of the cylindrical surface perpendicular to this heated surface) was assumed to be purely convective and was described by Newton's law, while an adiabatic condition was assumed for the remainder of the cylinder. Thermal properties of the meat were assumed to be very close to those of raw meat (thermal conductivity 0.45 W m K − 1, density 1060 kg m − 3, thermal capacity 3200 J kg K − 1) until crust began to form. When crust was formed, thermal conductivity was 0.1 W m K− 1. This value has been measured by us in the meat. It was also determined as the effective thermal conductivity of the crust during the deep-fat frying of potatoes (Ziaiifar, Heyd, & Courtois, 2009). The same thermal conductivity value found on the two products despite their difference of composition could be explained by similar porosities and gas content in the potato crust and in the meat crust. In crust, product density and specific heat vary also but their

values are not known for temperature higher than 100–110 °C (SosaMorales, Orzuna-Espíritu, & Vélez-Ruiz, 2006) and were considered in first approximation to be those of the raw meat. Globally Evolution of thermal properties during crust formation remains poorly known. 2.5. Magnetic resonance imaging MRI experiments were performed at 400 MHz on an Avance DRX400 system (Bruker, GmbH, Ettlingen, Germany) equipped with an actively shielded gradient coil for microimaging. Beef samples were placed in a 32-mm diameter birdcage radiofrequency coil used for both excitation and signal reception. A diffusion-weighted Spin Echo sequence was used at a b value of 3500 s/mm². The b factor quantifies the influence of the gradients on the images; the higher b is, the stronger is the signal attenuation for a given apparent diffusion coefficient. Fat imaging in muscle makes use here of the large difference between the apparent diffusion coefficients of myofibers and of intramuscular fat and oil. Using a sufficiently large factor of diffusion attenuates the intensity of the water signal, allowing the detection of fat only. Muscle fibers and olive oil apparent diffusion coefficients and signal-to-noise ratio being known, all the sequence parameters were adjusted to obtain a sufficient contrast at the resolution needed for monitoring oil penetration. Voxel volumes were 100×500×500 μm3, the higher resolution (100 μm) corresponding to the axial direction of the sample (i.e. the oil penetration direction). The other acquisition parameters were: repetition time 500 ms, echo time 16.6 ms and number of average 8. Using this protocol, each acquisition lasted 4 h 35 min, at a constant temperature of 25 °C. 2.6. Image analysis From the NMR 3D images of 64 × 320 × 64 matrix size, a dedicated software developed under Matlab (Version 2010a, MathWorks Inc., Natick, USA) computed the fat signal profiles in the direction of frying oil penetration. For each raw and fried sample, 798 profiles of size 320 among the 64 × 64 available were created from a cylinder coaxial to the sample, but with a smaller diameter (16 mm) to delete errors due to the vicinity of the sample side boundaries.

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A flatness correction was applied as the face of the sample under test was not always perfectly planar. To make this correction, for each profile, the edge of the sample was considered corresponding to the position of the first voxel with a signal intensity above a given threshold.

under conditions described by Scislowski, Durand, Gruffat, and Bauchart (2004). Total LCFAs were quantified using C19:0 as internal standard. Identification and calculation of the response coefficient of each individual LCFA was achieved using the quantitative mix C4-C24 FAME (Supelco, Bellafonte, USA).

2.7. Lipid and fatty acid analysis

3. Results and discussion

Four beef slices (2 mm thick corresponding to 1 g) taken from the frying surface (0 to 2 mm) up to 23 mm depth (2 to 4 mm, 4 to 6 mm and 21 to 23 mm) were frozen and ground into a fine powder in liquid nitrogen with a mixer mill (Retch MM 301, Germany) and finally stored at −80 °C for lipid analysis. Total lipids were extracted by the method of Folch, Lees, and Sloane Stanley (1957) by mixing 1 g of beef powder with chloroform/methanol (2:1, vol/vol) at 20,000 rpm, and assayed gravimetrically. Long-chain FAs (LCFAs) were extracted from total lipids and transmethylated at room temperature for 2 × 20 min with sodium methylate (1 M) followed by boron trifluoride in methanol (BF3-methanol 14%, vol/vol). LCFA analysis was conducted by gas–liquid chromatography (GLC) using the Peri 2100-model chromatograph (Perichrom Society, Saulx-lesChartreux, France) fitted with a CP-Sil 88 glass capillary column (Varian, USA) (length 100 m, Øi 0.25 mm) with H2 as carrier gas,

3.1. Meat near-surface temperatures and crust formation

A

Temperatures recorded during the 180 °C frying at respective depths of 0.7 mm, 2 mm and 4 mm from the surface of the meat are represented in Fig. 2A–C. Fig. 2D shows the temperature recorded 0.7 mm from the surface of the sample for a 130 °C frying. The recorded temperatures exceeded 100 °C only in the case of cooking at 180 °C, and only after 135 s of treatment for the thermocouple located 0.7 mm from the surface, and at the end of the treatment (after 313 s of cooking) for the thermocouple located 2 mm from the surface. At 180 °C, no constant temperature period was observed for the thermocouple located 0.7 mm from the surface, whereas such periods occurred after 184 s of treatment for the thermocouple at depth 2 mm and after 230 s for the thermocouple at depth 4 mm. These thresholds, where the temperature remained equal to boiling

B

180°C, surface and 0.7mm

180°C, 2mm

110

150

100 90

110 90 70 Simulation, surface 50

Temperature (°C)

Temperature (°C)

130

Simulation, 0.7mm

Simulation, 1.2mm

30

Experiment, 0.7mm

80 70 60 50 40 30

Simulation, 2mm

20

Experiment, 2mm

10

10 0

100

200

300

400

0

100

D 120

180°C, 4mm

110 100

110

90

100

80

Temperature (°C)

Temperature (°C)

C

200

300

400

Time (s)

Time (s)

70 60 50 40 30

Simulation, 4mm

20

Experiment, 4mm

130°C, surface

90 80 70 60 50 40 30

Simulation, surface

20

Experiment, 0.7mm

10

10 0

100

200

Time (s)

300

400

0

100

200

300

400

Time (s)

Fig. 2. (A, B, C) simulated and measured temperature profiles at several depths from the meat surface during frying at 180 °C, (D) simulated and measured temperature profiles at 0.7 mm depth during 130 °C frying. Error bars on measurements correspond to the standard deviation calculated on three independent experiments. Simulations were carried out by introducing in the model values of the convective transfer coefficient between 190 and 250 Wm− 2 K− 1. The simulated temperature kinetics at depths 2 mm and 4 mm from the meat surface, respectively in panels B and C, are not represented for temperatures higher than 100 °C because evaporation occurs at this boiling temperature, which is not taken into account by the model. Simulated temperature profiles at surface (Fig. 2D) are represented with a full line up to 100 °C (no evaporation) and with a dashed line above 100 °C for the same reason.

S. Clerjon et al. / Meat Science 91 (2012) 79–87

temperature, between 97 °C (laboratory located at an altitude of 800 m) and 100 °C, corresponded to the evaporation threshold, i.e. to periods during which the energy delivered to the product was completely consumed in the evaporation of water from the meat. During the frying at 130 °C, the temperature measured 0.7 mm beneath the surface of the product never reached 97 °C even at the end of treatment. In Fig. 2, error bars correspond to the standard deviation measured on three independent experiments. Maximum standard deviations were between 15 °C and 20 °C for thermocouples located 2 and 4 mm deep and varied depending on the time of cooking and the vicinity of evaporation thresholds. These variations corresponded to gradients simulated for a displacement of 1 mm of the probes from their initial positions (respectively at 2 and 4 mm from the surface, Table 2). For these two probes, the variance recorded in the three experiments could therefore be due to a positioning error, or a subsequent probe displacement, of the order of a millimeter. However, the variance in the recorded temperature for the probe located at 0.7 mm from the surface was only about 10 °C, owing to a better positioning of this thermocouple, with an error of about ±0.5 mm (Table 2). The simulated kinetics of temperature (value of the convective transfer coefficient between 190 and 250 Wm − 2 K − 1) are compared with the experimental kinetics in Fig. 2A–D. It shall be remembered that modeling approach followed in this paper remains very simple and is just used to assess the effect of a variation of thermocouple position on the measured temperature kinetics. Oil migration which tends to heat the product or water evaporation and steam migration through the crust which tend to cool the near-surface of the product are not taken into account in the model. As evaporation was not taken into account in the model, the kinetics simulated at depths 2 mm and 4 mm are represented only until the temperature reaches boiling point. In this case the simulated values are very close to the experimental ones. Kinetics simulated on the surface of meat, at depths 0.7 mm and 1.2 mm, are compared in Fig. 2A with experimental kinetics obtained at depth 0.7 mm for a frying at 180 °C. Kinetics simulated at depths 0.7 mm and 1.2 mm significantly overestimate the experimental values. In this case, the overestimation is not predominantly related to the thermocouple positioning error but arises because the model ignores the formation and migration of steam to the surface of the sample, with an additional error from the thermal conduction through the needle guiding the thermocouple; this phenomena overwhelming the gain of heat due to hot oil migration into the product. Overall, these results show that the experimental heating device and the positioning of thermocouples allowed the frying of one side of the sample at a constant oil temperature and the measurement of the temperature kinetics in the meat at precise locations near the surface of the sample. When the oil temperature was 180 °C, a crust formed very quickly on the surface of the sample, of thickness approximately 0.7 mm after 135–140 seconds of cooking, and 2 mm after 6 min. Evaporation then occurred to a much greater depth, at least 4 mm. When the oil temperature was 130 °C, crust formation

Table 2 Maximum gradient value and average gradient value in meat by distance of the sensor from the surface determined by simulations over 360 s. The second column gives the frying time at which the maximum gradient is reached. Distance from surface (mm)

Time corresponding to maximum gradient

Maximum gradient (°C/mm)

Average gradient (°C/mm)

0.7 1.2 2 4 6 10 20

6 18 34 78 148 360 360

42.8 29.4 22.3 17.1 11.5 6.4 1.3

18.1 16.5 14.7 13.7 9.7 4.0 0.4

83

on the sample surface began after 120 seconds of cooking at the earliest. Its thickness never reached 0.7 mm even at the end of treatment. The conclusions of the analysis of temperature were supported by visual observations, which showed that at 180 °C the change in meat color was evenly distributed at the meat surface and that the thickness of the crust was between 1 and 2 mm after 6 min of cooking. At 130 °C, the crust was unevenly distributed at the meat surface and its thickness was only 0.2 to 0.5 mm. 3.2. Lipids And Fatty Acid Composition Data from the gravimetric quantification of total lipids after their extraction by organic solvents, and their total FA content and composition determined by GLC analysis in 2 mm-thick beef slices (each averaging 1 g) are given in Table 3. They clearly show the importance of temperature in the capacity of the frying olive oil to impregnate lipids of LT muscle. Four depths in beef samples were studied, corresponding, relative to the contact with the frying oil, to 0–2 mm, 2–4 mm, 4–6 mm and finally 21–23 mm (control slice not accessible by the frying oil). Thus the comparison of lipid and FA data from the first three beef slices (0–6 mm) with those of the 21–23 mm slice enabled us to determine the level and degree of penetration of the olive oil, dominated by oleic acid (C18:1n-9 cis, 71% of total FAs) in the beef LT tissue (Table 3). Thus at 130 °C, oleic acid level in beef samples from the control group was highest in the 0–2 mm slice compared with that in the control 21–23 mm slice (50.6 vs. 39.2%). The same effect was noted, though to a lesser extent, with C18:2n-6 also supplied by olive oil (8% of total FAs, respectively). This qualitative impact on beef FA composition was associated with a 31% and 24% increase in total lipids and total FA concentrations in the beef samples respectively (Table 3). Such preferential increase of oleic acid level in meat was previously reported in restructured beef steaks pan fried for 5 min at 170 °C in olive oil (Librelotto et al., 2008). On the other hand, FA composition was less strongly modified (2–4 mm slice) or remained unmodified (4–6 mm slice), showing the relatively low impact in depth of the oil bath heated at 130 °C (Table 3). The same study at 130 °C with a beef sample from the LEP diet group confirmed the observations reported for beef samples from the control group. The higher proportion of C18:3n-3 in beef slices could be explained by the enrichment of the LT muscle with C18:3n-3 from the linseed supplement given to the cull cows compared with the control group (Habeanu et al., 2008). At 180 °C, impacts of the olive oil bath on beef lipids and their FAs were far more pronounced (both in intensity and in depth) than at 130 °C (Table 3). The effects were maximal at the level 0–2 mm, the total FA content being 3.3 times higher than that at 130 °C. In addition, effects of the olive oil bath were still marked in slices at 2–4 mm (+130%) and 4–6 mm (+72%). Analysis of FA composition clearly showed a higher level of oleic acid (C18:1n-9 from olive oil) in beef lipids in 180 °C compared with that in 130 °C noted in slices 0–2 mm (66.1 vs. 58.9% total FAs), 2–4 mm (58.2 vs. 48.6%) and 4–6 mm (49.3 vs. 44.8%) (Table 3). Thus these data confirmed the easier penetration of olive oil in beef samples with increasing temperature of the oil bath. By modifying both the level and composition of FAs in beef lipids, oil frying can have differing impact on the nutritional value of beef lipids. Frying with olive oil, favoring the incorporation of oleic acid at the expense of saturated FAs, with no effect on polyunsaturated FAs (PUFAs) (Table 3) would enhance the health value of beef FAs for consumers as mentioned earlier by Librelotto et al. (2008). By contrast, vegetable oils subjected to hydrogenation for use in frying (e.g. hydrogenated palm or rapeseed oil) may have an adverse effect on the nutritional and health value of meats by increasing the risk of incorporation of saturated FAs and trans monounsaturated FAs (MUFAs), which are abundant in such modified oils and have been linked to systemic inflammation in heart failure (Mozaffarian et al.,

84 Table 3 Distribution of individual fatty acids (% total fatty acids) and total lipid and fatty acid contents (g/100 g fried tissue) of beef slices taken from the fried surface (0–2 mm) up to 23 mm depth (2–4 mm, 4–6 mm and 21–3 mm) from samples of longissimus thoracis muscle of cull cows given the basal diet (control) or the same diet supplemented with linseed and antioxidants (vitamin E + PERP), fried at 130 °C or 180 °C for 6 min in an olive oil bath. Control group

LEP group (linseed + vit E + PERP)

LEP Group (linseed + vit E + PERP) Frying temperature

130 °C

130 °C

180 °C Beef slice depth

0–2 mm

2–4 mm

4–6 mm

21–23 mm

0–2 mm

2–4 mm

4–6 mm

21–23 mm

0–2 mm

2–4 mm

4–6 mm

21–23 mm (% total fatty acids)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD)

Mean

(SD) C16:0 C18:0 C18:1n-9 C18:2n-6 C18:3n-3 Total CLAs Total saturated FAs Total cis MUFAs Total trans MUFAs Total MUFAs Total cis n − 6 PUFAs Total trans n − 6 PUFAs Total n − 6 PUFAs Total n − 3 PUFAs Total PUFAs Total fatty acids (g/100 g fried tissue) Total lipids (g/100 g fried tissue)

19.1 9.7 50.6 5.5 0.7 0.2 32.1 56.4 1.3 56.4 7.7 0.4 8.0 1.6 9.8 3.62 4.46

(1.48) (1.15) (5.00) (0.52) (0.10) (0.06) (3.54) (4.42) (0.32) (4.42) (0.57) (0.29) (0.75) (0.42) (0.69) (0.35) (0.1)9

23.2 12.3 42.6 4.3 0.5 0.2 39.8 49.3 1.9 49.3 6.8 0.5 7.3 1.3 8.8 3.54 4.13

(0.54) (0.76) (1.55) (0.62) (0.06) (0.03) (1.84) (1.37) (0.14) (1.37) (0.69) (0.07) (0.63) (0.11) (0.70) (0.41) (0.26)

24.2 12.8 40.0 4.2 0.5 0.2 41.6 47.1 2.0 47.1 6.9 0.5 7.4 1.3 9.0 3.23 4.06

(0.40) (0.62) (1.44) (0.63) (0.05) (0.01) (0.34) (1.52) (0.17) (1.52) (0.10) (0.08) (1.05) (0.15) (1.20) (0.53) (1.55)

24.9 13.3 39.2 3.7 0.4 0.2 43.4 46.2 2.4 46.2 5.9 0.6 6.5 1.1 7.8 2.91 3.40

(0.83) (0.65) (1.12) (0.55) (0.04) (0.03) (1.79) (1.51) (0.35) (1.51) (0.82) (0.12) (0.86) (0.14) (0.97) (0.56) (0.65)

16.7 7.9 58.9 4.2 0.9 0.2 27.1 64.0 1.1 64.0 5.0 0.5 5.6 1.8 7.6 6.79 7.24

(0.04) (0.12) (0.26) (0.13) (0.09) (0.01) (0.10) (0.27) (0.09) (0.27) (0.07) (0.03) (0.04) (0.35) (0.38) (1.37) (1.46)

20.2 10.6 48.6 3.8 1.0 0.4 34.4 54.9 1.6 54.9 5.0 0.6 5.6 2.8 8.8 4.18 5.13

(0.80) (0.78) (2.04) (0.85) (0.09) (0.06) (2.63) (1.99) (0.35) (1.99) (0.83) (0.18) (0.65) (0.31) (0.90) (0.29) (0.59)

22.0 11.9 44.8 3.2 1.0 0.5 38.0 51.4 1.9 51.4 4.5 0.8 5.3 2.6 8.4 3.83 4.59

(1.43) (0.95) (3.75) (0.78) (0.09) (0.18) (3.89) (3.42) (0.43) (3.42) (0.91) (0.12) (0.79) (0.20) (0.81) (0.52) (0.36)

23.4 14.7 40.5 1.8 0.7 0.7 43.3 47.2 3.0 47.2 2.6 1.3 3.3 1.6 6.2 6.56 6.84

(0.13) (1.18) (0.68) (0.62) (0.15) (0.01) (1.92) (0.87) (0.62) (0.87) (1.04) (0.06) (0.98) (0.7) (1.73) (1.17) (3.84)

13.9 6.4 66.1 4.3 0.7 0.1 22.3 70.3 0.8 70.3 4.8 0.3 5.1 1.3 6.5 13.73 14.87

(1.13) (0.80) (3.31) (0.31) (0.05) (0.05) (2.8) (3.00) (0.22) (3.00) (0.27) (0.13) (0.19) (0.08) (0.13) (1.14) (1.47)

17.1 8.4 58.2 3.6 0.7 0.3 28.5 63.5 1.3 63.5 4.2 0.6 4.8 1.5 6.6 9.63 10.54

(1.59) (1.45) (4.72) (0.38) (0.01) (0.06) (4.35) (4.53) (0.37) (4.53) (0.34) (0.14) (0.27) (0.07) (0.24) (1.04) (1.59)

21.0 10.7 49.3 2.9 0.8 0.4 35.6 55.6 1.8 55.6 3.8 0.7 4.5 1.8 6.7 6.57 7.76

(0.97) (1.12) (2.73) (0.20) (0.03) (0.02) (2.89) (2.86) (0.30) (2.86) (0.19) (0.18) (0.37) (0.12) (0.49) (0.38) (0.05)

23.8 13.9 41.3 1.9 0.7 0.6 42.6 48.0 3.0 48.0 2.7 1.2 3.9 1.6 6.1 6.82 7.98

(0.12) (1.15) (0.21) (0.77) (0.21) (0.09) (1.82) (0.44) (0.45) (0.44) (1.14) (0.22) (0.97) (0.12) (1.77) (3.54) (4.23)

oil

frying face

320 pixels, 32 mm

intramuscular fat

raw

fried (130 C)

Fig. 3. Central longitudinal slice of a raw (top) and fried (130 °C) (bottom) beef sample. Oil at the frying surface and intramuscular fat in the sample appear as a hyper signal. Each image consists of a 64 × 320 matrix corresponding to a field of view of 32 mm by 32 mm. For each raw and fried sample, images were obtained for 64 adjacent slices.

64 pixels, 32 mm

Preliminary experiments showed that there was no significant difference in signal intensity, for a given b-value, between olive oil and intramuscular fat. These preliminary results are consistent with the literature (Ababneh et al., 2009). Hence our MRI method cannot discriminate between intrinsic intramuscular fat and that derived from oil. Oil penetrating during frying must therefore be quantified by comparison of raw and fried state images for each sample. Fig. 3 shows two MRI images of a raw (top) and fried (bottom) beef sample. There is an increase in the signal in the vicinity of the frying surface. This example demonstrates the ability of DWI to image lipids—oil as well as intramuscular fat—with a voxel size of 100 × 500 × 500 μm 3, 100 μm corresponding to the axial direction of the sample, i.e. the oil penetration direction. Following the image analysis process described in II.6., average profiles of fat on the entire raw and fried (130 °C and 180 °C) samples were extracted. The average profile of oil taken during frying was calculated by computing differences between fried and raw average profiles (fried profile corrected from raw profile). Fig. 4 shows the effect of frying with the presentation of these three profiles (raw, fried and oil taken up). The average raw profile was roughly constant, while the fried one presented a maximum near the frying surface. These profiles showed an oil penetration to a depth of nearly 4 mm.

3.3. NMR imaging

2004) and endothelial dysfunction (Lopez-Garcia et al., 2005). Production of trans MUFAs can occur during the cooking treatment itself at high temperatures (130 °C and 180 °C) from unsaturated FAs derived from either the frying oil or the meat itself. In our study, trans MUFA levels (% of total FAs) did not increase in beef slices in contact with the frying olive oil (0–6 mm) compared with the 21–23 mm slice, but were lower than in the 21–23 mm slice, indicating that no trans MUFAs were generated during the cooking process. The generation of peroxidized products from meat PUFAs during oil frying cannot be excluded, as reported earlier for various cooking treatments (Badiani et al., 2002, 2004). The effects of the time/temperature couple on lipoperoxidation in cooked meats have been analyzed by measuring the intensity of fluorescence (Gatellier & Santé-Lhoutellier, 2010). This method used with the same beef samples as in our study (LT muscles from cull cows given the control diet or the linseed diet enriched in 18:3n-3) showed an increase with time (from 30 to 300 s) of lipoperoxidation in all meats cooked at temperatures higher than 100 °C (123–207 °C), but for a set time, no difference in production of lipoperoxides was found between the two diets (Gatellier & SantéLhoutellier, 2010). Hence in our frying conditions (130 °C, and more likely at 180 °C for 6 min), such lipoperoxide production could occur to a degree that remains to be determined.

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Diet

S. Clerjon et al. / Meat Science 91 (2012) 79–87

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200 Raw samples 180 Fried samples 160

NMR fat signal (a.u.)

Fried samples corrected from raw samples 140 120 100 80 60 40 20 0 0

2

4

6

8

10

12

14

16

18

20

Depth in sample (mm) Fig. 4. Effect of frying. Mean profile of all raw samples (…), fried samples (130 °C and 180 °C together) ( almost 4 mm.

180°C: oil uptake 130°C: oil uptake

200

100

180°C: sample temperature 130°C: sample temperature

80

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0 0

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250 NMR signal profile Acid oleic content (biochemical analyse)

200

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Acid oleic content (g/100g of tissue)

120

). These profiles show an oil penetration to a depth of

during treatments at 180 °C. At such high temperature, water is vaporized during frying to a crust depth of 4 mm. During cooling there is condensation of water, creating a depression that leads to migration of the adhering oil film from the surface toward the center of the meat sample (Ufheil & Escher, 1996). However, MRI measurements showed that oil penetration, albeit limited, occurred in areas where the temperature of the product was always below 100 °C. We note that the temperature reached with our experimental protocol was higher than usual during home frying because oil temperature was controlled and maintained during the process in the laboratory, whereas in real home frying oil temperature decreases sharply when the meat is put in the pan on the oil. This discrepancy may cause an overevaluation of oil penetration in our experiments at both 180 °C and 130 °C. Oil penetration evaluated here through MRI profiles was correlated with FA analysis by GLC. For each sample, we compared the MRI profile of oil uptake with the quantity of oleic acid (C18:1n 9 cis) in the four slices taken from each sample. Fig. 6 presents this comparison for the B13 sample after a 180 °C frying process. It highlights the close correlation, despite a discrepancy for the deepest slice (21–23 mm), and the high resolution of DWI. This comparison was made for the three beef samples from cows in the control group (fried at 130 °C) and of the LEP diet group (fried at

Difference of NMR fat signal between fried and raw samples (a.u.)

250

Experimental sample tenperature (°°C)

Difference of NMR fat signal between fried and raw samples (a.u.)

We note that the maximum did not correspond to the sample surface but to a point almost 1 mm inside the fried meat. Two hypotheses can be proposed to explain this difference. The choice of the threshold during the image analysis (Part II.6) is of course a first crucial point. Voxels at the air-sample interface can be more or less partially filled with fatty material and so produce a greater or smaller signal. The choice of the threshold determines whether or not these interface voxels are taken into account. The second hypothesis is more physical and concerns the crust porosity: the presence of air cavities in the first millimeter could explain signal loss. The next results concerned the effect of frying temperature. We note in Fig. 5 that oil penetration was greater, in both depth and quantity, during beef frying at 180 °C than at 130 °C: 4 mm at 180 °C and 3 mm at 130 °C with a fat signal intensity almost 2.5 times higher at 180 °C. This result was consistent with the temperature applied to the sample (red and green lines) and oil penetration processes. Analysis of temperature gradients showed that temperature exceeded 100 °C for a 4 mm depth in a 180 °C treatment. During the 130 °C frying process, the temperature exceeded 100 °C only on the surface of the product. These values were consistent with the crust developments observed visually. They explain why cooking oil can penetrate heavily

) and oil take-up (

Sample depth (mm)

Sample depth (mm) Fig. 5. Mean profiles of oil uptake at 130 °C ( ) and 180 °C (―) and simulated temperature inside the samples after 6 min of frying at 130 °C ( ) and 180 °C ( ).

Fig. 6. Comparison for the B13 sample after a 180 °C frying process between the MRI profile and the quantity of oleic acid (C18-1n-9 cis) measured with GLC in the four slices from this sample.

S. Clerjon et al. / Meat Science 91 (2012) 79–87

150 y = 0,02x-12,76 R² = 0,82

100 50 0 -50

0

1000 2000 3000 4000 5000 6000 7000 8000 9000 10000

Acid Oleic content (mg/100g of tissue) Fig. 7. Correlation, for all sample types (supplemented and fried at 180 °C, supplemented and fried at 130 °C and control and fried at 130 °C), for the four slices, between DWI and GLC for oil content.

130 °C and 180 °C) and the correlation (R² = .82) between DWI and GLC for oil content is given in Fig. 7. This excellent correlation validates the ability of DWI to evaluate the quantity of oil uptake during oil frying. While the difference between fried and raw profiles gives the oil uptake profiles, which are closely correlated with the oleic acid content, the fried profiles alone give the total fat content directly. The average profile of fat distribution was also compared with the total FA content determined by GLC analysis on supplemented beef samples fried at 130 °C and 180 °C (Fig. 8). These representations show the close correspondence between MRI profiles and FA content by GLC analysis. The hatched area, which marks the non-fried sample end, could not be exploited: because of the flatness correction (see description in II.6.), these “back end” parts of the profiles are to some extent truncated and so cannot be meaningfully averaged in. This comparison was made for all types of studied beef samples together and the correlation between DWI and GLC for total lipid (R² = .70) validates the ability of DWI to evaluate total lipid content profile in meat products. 4. Conclusion

180

NMR fat signal (a.u.)

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DWI of lipids appears very promising, especially in food sciences, where sample movement and timing of data acquisition are not problematic. With this technique, the greater the resolution is, the lower the diffusion coefficient is, and the less sensitive the method is to movement and to susceptibility artifacts. High resolution clearly makes the method particularly useful. In addition, combining DWI and gas–liquid chromatography analyses makes use of two complementary techniques that allow high-resolution lipid localization and

yield data for the quantification and distribution of individual FAs in beef lipids. This study shows that the DWI is well-suited to micro-imaging intramuscular fat and frying oil in muscle tissues. A 100 μm high resolution in the direction of oil penetration gives precise information on variations in fat content and its distribution in meat according to values of cooking parameters. Collated MRI data, measurements of temperature gradients and biochemical FA analyses of cooked samples show alteration of meat FAs with flat frying. Careful monitoring of this operation can ensure that the benefits of animal feed supplementation are safeguarded. More generally, the tools used for combined MRI measurements and characterization of surface transfers should help to gain a fuller understanding of and predict the variation in the toxico-nutritional qualities of foods of animal origin undergoing frying treatments. Our results emphasize that for pan-fried meat, cooking oil composition has a preponderant effect on the quantity and composition of FAs in the first millimeters beneath the surface. In addition to efforts on feed composition for meat cattle to improve the nutritional value of fatty acids deposited in their muscle tissues, nutritional improvement requires cooking at 130 °C rather than 180 °C (for the same treatment time) to limit penetration of oil into the meat, and using an oil with favorable nutritional qualities. This is particularly true when the cut is thin, such as in steaks. Besides its geometry, the highly anisotropic organization of meat, with parallel fibers and fascicles, may also affect oil penetration. The high resolution of oil uptake profiles obtained with DWI makes this technique a promising tool for future research in this direction. Moreover, a fat reference (area with pure oil on the MR images) could be use to perform fat content quantification in addition to the penetration depth measurement. Another interesting follow-up of this study will be to focus on the effect of antioxidants added to the animal diet (here vitamin E combined with polyphenols provided by several plant extracts) on the prevention of oil peroxidation during the frying process. Our results suggest that such antioxidant supplements in the animal diets will help to preserve oleic acid and other unsaturated FAs (especially linoleic acid) in the olive oil from thermal denaturing. This preservation needs to be quantified to fully evaluate the added value of such dietary antioxidants on the final nutritional profile of fried meats. Acknowledgements Diffusion-weighted MRI was performed at the Platform for Magnetic Resonance in Biological Systems in the INRA Centre, Theix, ClermontFerrand. This study was part of the Lipivimus project, funded by the French National Research Agency. The authors gratefully thank Christiane Legay for her excellent technical assistance in meat lipid and fatty acid preparations. 350

20 180°C fried supplemented samples

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16 250

14 12

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8 6

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Fig. 8. Mean profile of oil uptake at 130 °C and 180 °C and total fatty acid content obtained by biochemical analysis.

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NMR fat signal of uptaken oil (a.u.)

200

NMR fat signal (a.u.)

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