Meat Science 100 (2015) 134–138
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The relationship between pre-harvest stress and the carcass characteristics of beef heifers that qualified for kosher designation N.S. Hayes, C.A. Schwartz, K.J. Phelps, P. Borowicz, K.R. Maddock-Carlin, R.J. Maddock ⁎ Department of Animal Sciences, North Dakota State University, Fargo, ND 58108, USA
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Article history: Received 19 September 2013 Received in revised form 26 September 2014 Accepted 30 September 2014 Available online xxxx Keywords: Kosher Stress Beef Tenderness Color
a b s t r a c t Differences in pre-harvest stress measurements and carcass characteristics between kosher and not-qualified-askosher cattle were evaluated. Finished heifers (n = 157) were slaughtered by a shochet while held in an upright position using Glatt slaughter procedures. Stress measurements were collected prior to slaughter. Carcass data were collected, and 3.8-cm thick samples were taken from the loin at the 13th rib. Steaks from each sample were evaluated for mechanical tenderness and simulated retail display. Cattle with shorter times from gate to exsanguination and lower vocalization scores were more likely (P b 0.01) to qualify as kosher. Kosher carcasses had larger (P = 0.02) ribeye areas and higher (P b 0.0001) Warner–Bratzler shear values. At each day of simulated retail display, kosher steaks had lower (P b 0.05) L*, a*, and b* values. These data suggest that body composition and pre-harvest stress affect the likelihood of a beef animal qualifying as kosher and quality differences exist between kosher and non-kosher steaks. Published by Elsevier Ltd.
1. Introduction
2. Materials and methods
Kosher food based on biblical origins grew into a $200 billion food industry in 2009 (Regenstein & Regenstein, 2012). The kosher slaughter process is performed by a trained religious slaughter man with no stunning of the animal prior to exsanguination. However, this procedure alone does not make an animal acceptable for kosher consumption. Internal organs, specifically the lungs, must be inspected for any defects. Lungs have been inspected since biblical times as a guard against disease. Pneumonia and other respiratory illnesses are among the most common causes of lung leisons today (Schneider, Tait, Busby, & Reecy, 2009). Lung adhesions are of primary concern and may result in an animal failing to qualify as kosher. We hypothesize that there are differences between cattle that qualify as kosher and those that do not, that pre-slaughter stress may affect carcass and meat quality of steers and heifers kosher slaughtered, and there may be differences in carcass and meat quality between kosher-qualified cattle and nonkosher-qualified cattle. The objective of this study was to determine if there are differences in pre-slaughter stress measurements and carcass characteristics between carcasses that qualified for kosher versus those that did not qualify as kosher.
2.1. Data collection
⁎ Corresponding author at: PO Box 6050, Department 7630, NDSU, Fargo, ND 581086050, USA. Tel.: +1 701 231 8975; fax: +1 701 231 7590. E-mail address: [email protected] (R.J. Maddock).
http://dx.doi.org/10.1016/j.meatsci.2014.09.145 0309-1740/Published by Elsevier Ltd.
Trained university personnel observed kosher beef slaughter of steers and heifers of mostly Angus genetics sourced from North Dakota and Minnesota, USA (n = 162) at a commercial abattoir in New Rockford, ND during three slaughter days in consecutive months (January through March). Slaughter facilities are typical of a modern beef slaughter facility, with cattle moving from lairage pens onto a v-belt restrainer that moved the cattle to the bleeding gate. All cattle were held in an upright position and the head restrained by a hydraulic device that presented the throat to the trained rabbi for bleeding. A single rabbi performed all of the bleeding, and all animal were presented for “Glatt” kosher slaughter. Pre-slaughter stress measurements recorded included number of animals per lairage pen, chute score, vocalization score, number of times electrical prods used, and time from entering the v-belt to exsanguination (GtE). Chute scores (1 = calm, no movement; 2 = slightly restless; 3 = squirming, occasionally shaking the chute; 4 = continuous, very vigorous movement and shaking of the chute; 5 = rearing, twisting of the body and struggling violently) were adapted from Grandin (1993) and Grandin (2010) and recorded in the holding chute prior to entering the v-belt restrainer. Vocalization scores (0 = no vocalization, 1 = low intensity, singular vocalization; 2 = mild intensity, one to two vocalizations; 3 = high intensity, two or more vocalizations) were observed on the v-belt restrainer. Time from exsanguination to insensibility (EtU) was recorded. Insensibility
N.S. Hayes et al. / Meat Science 100 (2015) 134–138
was defined by lack of corneal reflex. Approximately 30 s after exsanguination, a 2-mL blood sample was collected and analyzed immediately for blood lactate concentration using a Lactate Pro Meter (Arkray, USA Inc., Edina, MN). Hot carcass weight (HCW) was recorded, and carcasses were transported in refrigerated trailers to the North Dakota Natural Beef processing facility in Fargo, ND. The kosher data indicating if a carcass qualified for kosher, with all carcasses qualified for kosher designated as “Glatt,” or were not kosher were obtained from North Dakota Natural Beef after the slaughter process was completed. The trained rabbis inspected the internal organs, and especially the lungs and carcasses for evidence of defects that would prevent the carcass from being classified as kosher. To inspect the lungs, a small hand-held air pump was used to inflate the lungs which were then evaluated for the lungs ability to hold air. If the lungs did not hold air, the carcass would not qualify as kosher. After a 24-h chill, 12th rib fat (BF), rib eye area (REA), kidney pelvic and heart fat percentage (KPH), final yield grade (FYG), marbling score (Marb), as well as the presence of beef quality defects were measured by trained university personnel. At the same time, an approximately 3.8-cm thick sample was obtained from the loin at the 13th rib, placed in a labeled bag inside a cooler, and transported immediately to the North Dakota State University's meats laboratory. Upon arrival, a subsample of loin (~2 g) was removed and frozen at − 10 °C for up to 60 d for later analysis of sarcomere length and troponin-T degradation. Two steaks (2.54-cm and 1.25-cm thick) were cut from the remaining sample, vacuum packaged (Cryovac® vacuum packager, Duncan, SC) and aged at 4 °C for 14 d and 7 d respectively until further processing and analyses. It is important to note that the steak samples had not been subjected to “koshering” that is, the samples had not been salted or soaked.
2.2. Warner–Bratzler shear force (WBSF) After aging for 14 d in darkness at 4 °C, the 2.54-cm steaks were frozen at − 20 °C until analysis for tenderness by WBSF. All samples from the three collection periods were evaluated on the same day. Prior to cooking and shear force measurements, steaks were thawed overnight in a 4 °C-cooler and then allowed to come to room temperature (approximately 18 °C) before being weighed. A copper-constantan thermocouple was inserted (Omega Engineering Inc., Stamford, CT) into the geometric center of the steak. Steaks were cooked on clamshellstyle grills (George Foreman grill Model No. GRP99, Columbia, MO) to an internal temperature of 71 °C and then removed from the grill and allowed to cool to room temperature (approximately 21 °C). Steaks were weighed again, and cook loss was calculated by dividing cooked weight by raw weight and subtracting the total from 100. Six, 1.27-cm cores were taken from each steak parallel to the muscle fibers and sheared once perpendicular to the muscle fibers for measurement of tenderness using a Warner–Bratzler shear force machine (G-R Manufacturing, Manhattan, KS) (AMSA, 1995).
2.3. Display life After aging for 7 d in darkness, the 1.25-cm steaks were removed from vacuum packaging, individually placed in white foam trays with absorbent pads (4S Trays, Pactiv, Lake Forest, IL), overwrapped with clear cellophane, and placed in a 4 °C cooler under continuous fluorescent light (Sylvania, 32-watt, T-8 Cool White, Sylvania, Danvers, MA). L*, a*, and b* color were measured at three locations on the steak surface, with the values being averaged for each day, on each steak every 24 h for 10 d using a Minolta colorimeter using a D65 illuminant and calibrated using a white calibration tile (Konica Minolta, Toyko, Japan). Steaks were randomly moved daily to mimic movement found in a retail case and to account for slight variations in light intensity.
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2.4. Myofibril extraction and sarcomere length Myofibrils were extracted using the method of Weaver, Bowker, and Gerrard (2009) from a subset of loin samples that were frozen 24-h post-mortem (n = 53) equally representing carcasses that qualified for kosher and those that did not. Briefly, an approximately 1 g sample was removed from the freezer, minced, and homogenized using a blender (Waring Laboratory Science, Torrington, CT) in 5 volumes of ice-cold rigor buffer [75 mM KCl, 10 mM imidazole, 2 mM MgCl2, 2 mM ethylenediaminetetraacetic acid (EDTA), 1 mM NaN3; pH 7.2; with 0.1 mM phenylethyl sulfonyl fluoride (PMSF)] using a Kinematica PT 10/35 Polytron homogenizer with PTA-10S generator (Brinkmann, Westbury, NY). After centrifugation at 20,000 ×g and 4 °C for 30 min, myofibrils were washed several times with rigor buffer and then resuspended in 5 volumes of rigor buffer and 5 volumes of glycerol and stored at −20 °C for approximately 2 months until further processing. To estimate sarcomere length, myofibrils were fixed on slides with 3% (v/v) formaldehyde in rigor buffer, mounted in media [75 mM KCl, 10 mM Tris (pH 8.5), 2 mM MgCl2, 2 mM EDTA, 1 mM NaN3, 1 mg/mL p-phenylenediamine, 75% (v/v) glycerol], and sealed under coverslips (Weaver, Bowker, & Gerrard, 2008). Five different microscopic field images were captured for each slide using the Zeiss Axio Imager M2 upright microscope equipped with high resolution AxioCamMRc3 camera and the A-Plan100x 1.25 oil Ph3 objective (Carl Zeiss Microscopy, LLC; Thornwood, NY). The first 20 myofibrils observed that were positioned in a straight-line orientation and at least 5 full sarcomeres in length were measured using Image-Pro Plus 5.0 software (Media Cybernetics, Bethesda, MD). The average sarcomere length for each slide (loin sample) was recorded. 2.5. Whole muscle protein extraction, SDS-PAGE electrophoresis, and troponin-T immunoblotting Whole muscle protein was extracted from frozen 24-h subset (n = 53) of loin subsamples as described by Huff-Lonergan, Mitsuhashi, Parrish, and Robson (1996). Briefly, 0.5 g of muscle tissue was minced and then homogenized in 5 mL of extraction buffer [10 mM sodium phosphate, pH 7.0; 2% (w/v) sodium dodecyl sulfate (SDS)] with a serrated pestle attached to a mechanical homogenizer (Eberbach Corporation, Ann Arbor, MI) at room temperature until well ground. The homogenate was clarified by centrifugation (1500 ×g) for 15 min at room temperature. The protein concentration of each cleared extract was determined using DC Protein Assay Reagents (BioRad Laboratories, Hercules, CA) based on Lowry, Rosebrough, Farr, and Randall (1951). Protein extracts were diluted with water to a final concentration of Table 1 Least squares means and standard errors for pre-harvest characteristics of heifers that qualified and did not qualify as kosher. Trait
Non-kosher (n = 85)
SEM
Kosher (n = 72)
SEM
P-value
Animal number/pen Chute scorea Blood lactate, mmol/L GtEb, s EtUc, s Vocalization scored EPe
10.6 2.97 7.48 53.7 78.1 1.09 1.03
0.35 0.15 0.60 1.92 2.75 0.15 0.16
10.3 2.85 7.78 46.5 83.2 0.47 0.92
0.37 0.16 0.63 1.99 2.88 0.16 0.17
0.53 0.60 0.73 0.01 0.20 0.01 0.64
a Chute score where 1 = calm, no movement; 2 = slightly restless; 3 = squirming, occasionally shaking the chute; 4 = continuous, very vigorous movement and shaking of the chute; and 5 = rearing, twisting of the body and struggling violently. b Gate to exsanguination, time from gate (v-belt) to exsanguination. c Exsanguination to insensibility, time from exsanguination to insensibility as defined by lack of corneal reflex. d Vocalization score where 0 = no vocalization; 1 = low intensity, singular vocalization; 2 = mild intensity, one to two vocalizations; and 3 = high intensity, two or more vocalizations. e Number of times the electrical prod was used.
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Table 2 Least squares means and standard errors for carcass characteristics of beef heifers that qualified and did not qualify as kosher.
the 30-kDa degradation Bandof a whole muscle protein extract control sample run on every gel.
Trait
Non-kosher (n = 85)
SEM
Kosher (n = 72)
SEM
P-value
2.6. Statistical analysis
HCWa, kg BFb (12th rib), cm REAc, cmb KPHd, % FYGe Marbf
336.8 1.17 78.8 2.00 2.55 454
8.15 0.10 1.87 0.01 0.13 18
354.8 1.14 84.7 2.00 2.38 413
6.96 0.08 1.61 0.01 0.12 15
0.10 0.82 0.02 0.18 0.33 0.09
Data indicating if a carcass qualified as Glatt kosher or not were obtained from North Dakota Natural Beef. Carcasses were designated as either kosher or non-kosher. Data were analyzed using PROC GLM procedures of SAS (Version 9.2, SAS Institute Inc., Cary, NC) with kosher as the source of variation in the model, with slaughter day used as a covariate, and least squares means were separated using the pdiff option of SAS. Color measurements were analyzed as repeated measures using kosher versus non-kosher as the sourced of variation and day as the repeated measure.
a
Hot carcass weight. Backfat. c Ribeye area. d Kidney, pelvic, and heart fat. e Final USDA yield grade, determined from components. f Marbling score where 300 = slight, 400 = small, 500 = modest, and 600 = moderate. b
3. Results and discussion 3.1. Pre-harvest stress measurements
0.64 μg/μL. One volume of each extract was combined with 0.5 volumes sample/buffer tracking dye solution [3 mM ethylenediamine tetraacetic acid (EDTA), 3% (w/v) SDS, 30 mM Tris, pH 8.0; 30% (v/v) glycerol, 0.003% (w/v) pyronine Y) (Wang, 1982) and 0.1 volumes of 2mercaptoethanol for a final protein concentration of 0.4 μg/μL. Gel samples were heated to 60 °C for 15 min and then frozen at − 80 °C for up to 10 d until electrophoresis. Individual sample protein extracts were loaded (3.2 μg protein) onto 1.5 mm thick mini polyacrylamide gels (5% stacking and 15% resolving with a 37.5:1 acrylamide:bis crosslinking and separated by electrophoresis in a running buffer [25 mM Tris, 0.19 M glycine, 1.7 mM EDTA, 0.1% (w/v) SDS] for 3.5 h at a constant voltage of 150. After electrophoresis, proteins were transferred onto polyvinylidene fluoride membranes (Immobilon-P, 0.45 μm pore size; Millipore Corporation, Billerica, MA) in a transfer buffer [25 mM Tris, 0.19 M glycine, 1.7 mM EDTA, 15% (v/v) methanol] using a wet tank transfer system with cooling at 90 V for 1.5 h. Membranes were incubated at room temperature in a blocking solution of 5% (w/v) nonfat dry milk in phosphate buffered saline (PBS)-Tween [80 mM sodium phosphate, dibasic; 20 mM sodium phosphate, monobasic, 100 mM sodium chloride, 0.1% (v/v) polyoxyethylene sorbitan monolaurate (Tween 20)]. After blocking, membranes were incubated overnight at 4 °C with mouse monoclonal anti-rabbit TnT antibody (clone JLT-12, Sigma T 6277, St. Louis, MO) diluted 1:45,000 in PBS-Tween. Blots were washed in PBS-Tween and then probed with goat anti-mouse IgG peroxidase conjugate (Sigma A 2554) diluted 1:45,000 in wash buffer for 1 h at room temperature. Blots were washed with the PBS-Tween solution, and ECL Prime Western Blotting Detection Reagents (GE Healthcare Biosciences, Piscataway, NJ) were used to detect immunoreactive bands. A molecular weight marker was used to estimate the molecular weights of the immunoreactive bands. Chemiluminescence was photo-documented and measured with an Alpha Innotech FluorChem FC2 image analysis system with supporting AlphaEaseFC software (Protein Simple, Santa Clara, CA) using 1-D multi analysis with horizontal baseline and a band width sample of ~60% of the total band width. All band intensities were normalized (band area value/control area value) to the intensity of
Least squares means and standard errors calculated for pre-harvest stress measurements of beef heifers are presented in Table 1. Number of animals per pen, chute score, EtU, and number of times electrical prods were used did not differ between those cattle that qualified for kosher and those that did not (P N 0.10). Grandin and Regenstein (1994) found that most cattle lose consciousness 5 to 60 s after kosher exsanguination; however, these findings of time to insensibility are consistent with Blackmoore (1984) and Daly, Kallweit, and Ellendorf (1988) who state that it may take over a minute for the animal to lose consciousness. In the present study, we used blood lactate as a potential objective indicator of stress during the slaughter process while chute score, GtE, and vocalization scores were used as subjective scores to try and better evaluate stress at the time of slaughter. Apple et al. (1995) measured blood lactate levels in lambs subjected to stress and found that as stress level increased, blood lactate levels were higher from blood collected after stunning and exsanguination. The handling stress levels in this plant were relatively high compared to other kosher plants and conventional plants. When both kosher and non-kosher groups are combined, over half the cattle vocalized. Data collected in two other kosher plants with upright restraint indicated that 99% to 98% of the cattle remained silent (Grandin and Regenstein, 1994). Additional data from 22 conventional plants indicated that on average, only 3% of the cattle vocalized and all the others were silent (Grandin, 2000), and the worst plant had a 17% vocalization score. Electric prod use also occurred on almost 100% of the cattle in the plant studied. Six plants, which had a V conveyor restrainer, used the electric prod on an average of 39% of the cattle (Grandin, 1998). Cattle were scored as either electric prodded or not electric prodded. The lactate levels were also higher than those in Gruber et al. (2010). There is a possibility that high levels of handling stress may have contributed to lengthening the time required for the animals to become insensible. Blood lactate level did not differ (P = 0.73) between kosher and non-kosher qualified cattle. Cattle that qualified for kosher were less vocal (P b 0.01) and took less time from entering the gate to exsanguination (P = 0.01). Grandin (1998) observed 112 cattle through six different plants and found that cattle vocalize after adverse events such as
Table 3 Least squares means and standard errors for tenderness measurements of beef heifers that qualified and did not qualify as kosher. Variable a
WBSF , N Sarcomere length, μm Troponin-T, 41-kDa bandb Troponin-T, 30-kDa bandb a b
n
Non-kosher
SEM
n
Kosher
SEM
P-value
83 27 27 27
33.07 1.92 4.67 0.26
0.34 0.03 0.42 0.04
77 26 26 26
41.97 1.84 6.12 0.07
0.33 0.03 10.43 0.04
b0.0001 0.09 0.02 b0.01
Warner–Bratzler shear force. Units are relative to the 30-kDa band control loin sample which was set to 1.0.
N.S. Hayes et al. / Meat Science 100 (2015) 134–138
Fig. 1. Minolta L*color score values of beef loin steaks from cattle that either qualified (Glatt) or did not qualify as kosher.
electrical prodding, slipping, or excessive pressure in a powered restraining device. Grandin (1980) also found that short term acute stress results in a buildup of lactic acid in the blood. Further, animals that are inverted prior to exsanguination have higher blood cortisol levels as well as greater vocalization scores (Dunn, 1990), suggesting that vocalization may be used as an indicator of stress level. 3.2. Carcass measurements Carcass characteristics of beef heifers are presented in Table 2. The BF, KPH, and FYG were not different (P N 0.15) between kosher and non-kosher cattle, although non-kosher cattle tended (P = 0.09) to have higher marbling scores. Daniel, Held, Brake, Wulf, and Epperson (2006) found that lambs with severe lung lesions have lower average daily gain (ADG) and higher average marbling scores than those with normal lungs. This suggests that ruminants with lung health issues may spend more time in the finishing phase, allowing for an increase in intramuscular fat. Kosher-qualified cattle had larger REA (P = 0.02) and tended (P = 0.10) to have heavier HCW than those that did not qualify. Reinhardt, Busby, and Corah (2009) reported that more excitable cattle, as measured by chute score, had a lower HCW which corresponds to these findings. Cattle with increased numbers of lung lesions also have decreased HCW and REA (Reinhardt et al., 2009; Schneider et al., 2009) suggesting that cattle with health issues in the feedlot may not reach full genetic potential for growth. Overall, these data suggest that there may be a phenotypical difference between cattle that qualify for kosher and that that do not, with kosher cattle being larger, more muscular, and having less marbling in the longissimus at the 12th rib. 3.3. Beef tenderness measurements Least squares means and standard errors for tenderness measurements of beef heifers are presented in Table 3. Loin steaks from kosher
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Fig. 3. Minolta b* color score values of beef loin steaks from cattle that either qualified (Glatt) or did not qualify as kosher.
carcasses were less tender than those from non-kosher carcasses (P b 0.0001). Longissimus muscle from kosher-qualified cattle tended (P = 0.09) to have shorter sarcomere lengths than those from nonkosher-qualified cattle. Shorter sarcomere length usually indicates lower meat tenderness (Aberle, Forrest, Gerrard, & Mills, 2001) which agrees with our findings. Moreover, cattle with calmer temperaments possess longer sarcomeres than those with excitable temperaments (King et al., 2006; Gruber et al., 2010. 3.4. Display life color score measurements Daily L*, a*, and b* color values of beef loin steaks aged in vacuum packages for 7 d and then over-wrapped in cellophane and displayed under fluorescent lighting for 10 d are shown in Figs. 1, 2, and 3. On each individual day kosher steaks had lower (P b 0.05) L*, a* and b* values. Also for each day, L*, a*, and b* values differed (P b 0.05) from the previous day. However the interaction of kosher “grade” and time was not significant. Wulf, O'Connor, Tatum, and Smith (1997) found that steaks displaying a higher L*,a* and b* value (lighter, more red, more yellow) are more tender, which is supported by the findings of this research. In addition, Breidenstein, Cooper, Cassens, Evans, and Bray (1968) and Wulf et al. (1997) found that steaks with higher marbling scores also have higher color scores. 4. Conclusion In summary, cattle that qualified as kosher had calmer temperaments and were able to move through the abattoir more quickly when compared with cattle that did not qualify, mostly due to lung adhesions. In addition, cattle that qualified as kosher were heavier muscled and larger, as evident by the larger REA and heavier HCW. Factors of carcass type and temperament could be useful selection tools for cattle buyers looking to purchase cattle for the kosher market. This may also help reduce the percentage of cattle purchased by kosher buyers that do not qualify for kosher. Lastly, we found that kosher steaks are less tender than non-kosher steaks. Further research is needed to understand the relationship between kosher grade and tenderness and the possibility of producing a more tender kosher product. References
Fig. 2. Minolta a* color score values of beef loin steaks from cattle that either qualified (Glatt) or did not qualify as kosher.
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Meat Science journal homepage: www.elsevier.com/locate/meatsci
The relationship between pre-harvest stress and the carcass characteristics of beef heifers that qualified for kosher designation N.S. Hayes, C.A. Schwartz, K.J. Phelps, P. Borowicz, K.R. Maddock-Carlin, R.J. Maddock ⁎ Department of Animal Sciences, North Dakota State University, Fargo, ND 58108, USA
a r t i c l e
i n f o
Article history: Received 19 September 2013 Received in revised form 26 September 2014 Accepted 30 September 2014 Available online xxxx Keywords: Kosher Stress Beef Tenderness Color
a b s t r a c t Differences in pre-harvest stress measurements and carcass characteristics between kosher and not-qualified-askosher cattle were evaluated. Finished heifers (n = 157) were slaughtered by a shochet while held in an upright position using Glatt slaughter procedures. Stress measurements were collected prior to slaughter. Carcass data were collected, and 3.8-cm thick samples were taken from the loin at the 13th rib. Steaks from each sample were evaluated for mechanical tenderness and simulated retail display. Cattle with shorter times from gate to exsanguination and lower vocalization scores were more likely (P b 0.01) to qualify as kosher. Kosher carcasses had larger (P = 0.02) ribeye areas and higher (P b 0.0001) Warner–Bratzler shear values. At each day of simulated retail display, kosher steaks had lower (P b 0.05) L*, a*, and b* values. These data suggest that body composition and pre-harvest stress affect the likelihood of a beef animal qualifying as kosher and quality differences exist between kosher and non-kosher steaks. Published by Elsevier Ltd.
1. Introduction
2. Materials and methods
Kosher food based on biblical origins grew into a $200 billion food industry in 2009 (Regenstein & Regenstein, 2012). The kosher slaughter process is performed by a trained religious slaughter man with no stunning of the animal prior to exsanguination. However, this procedure alone does not make an animal acceptable for kosher consumption. Internal organs, specifically the lungs, must be inspected for any defects. Lungs have been inspected since biblical times as a guard against disease. Pneumonia and other respiratory illnesses are among the most common causes of lung leisons today (Schneider, Tait, Busby, & Reecy, 2009). Lung adhesions are of primary concern and may result in an animal failing to qualify as kosher. We hypothesize that there are differences between cattle that qualify as kosher and those that do not, that pre-slaughter stress may affect carcass and meat quality of steers and heifers kosher slaughtered, and there may be differences in carcass and meat quality between kosher-qualified cattle and nonkosher-qualified cattle. The objective of this study was to determine if there are differences in pre-slaughter stress measurements and carcass characteristics between carcasses that qualified for kosher versus those that did not qualify as kosher.
2.1. Data collection
⁎ Corresponding author at: PO Box 6050, Department 7630, NDSU, Fargo, ND 581086050, USA. Tel.: +1 701 231 8975; fax: +1 701 231 7590. E-mail address: [email protected] (R.J. Maddock).
http://dx.doi.org/10.1016/j.meatsci.2014.09.145 0309-1740/Published by Elsevier Ltd.
Trained university personnel observed kosher beef slaughter of steers and heifers of mostly Angus genetics sourced from North Dakota and Minnesota, USA (n = 162) at a commercial abattoir in New Rockford, ND during three slaughter days in consecutive months (January through March). Slaughter facilities are typical of a modern beef slaughter facility, with cattle moving from lairage pens onto a v-belt restrainer that moved the cattle to the bleeding gate. All cattle were held in an upright position and the head restrained by a hydraulic device that presented the throat to the trained rabbi for bleeding. A single rabbi performed all of the bleeding, and all animal were presented for “Glatt” kosher slaughter. Pre-slaughter stress measurements recorded included number of animals per lairage pen, chute score, vocalization score, number of times electrical prods used, and time from entering the v-belt to exsanguination (GtE). Chute scores (1 = calm, no movement; 2 = slightly restless; 3 = squirming, occasionally shaking the chute; 4 = continuous, very vigorous movement and shaking of the chute; 5 = rearing, twisting of the body and struggling violently) were adapted from Grandin (1993) and Grandin (2010) and recorded in the holding chute prior to entering the v-belt restrainer. Vocalization scores (0 = no vocalization, 1 = low intensity, singular vocalization; 2 = mild intensity, one to two vocalizations; 3 = high intensity, two or more vocalizations) were observed on the v-belt restrainer. Time from exsanguination to insensibility (EtU) was recorded. Insensibility
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was defined by lack of corneal reflex. Approximately 30 s after exsanguination, a 2-mL blood sample was collected and analyzed immediately for blood lactate concentration using a Lactate Pro Meter (Arkray, USA Inc., Edina, MN). Hot carcass weight (HCW) was recorded, and carcasses were transported in refrigerated trailers to the North Dakota Natural Beef processing facility in Fargo, ND. The kosher data indicating if a carcass qualified for kosher, with all carcasses qualified for kosher designated as “Glatt,” or were not kosher were obtained from North Dakota Natural Beef after the slaughter process was completed. The trained rabbis inspected the internal organs, and especially the lungs and carcasses for evidence of defects that would prevent the carcass from being classified as kosher. To inspect the lungs, a small hand-held air pump was used to inflate the lungs which were then evaluated for the lungs ability to hold air. If the lungs did not hold air, the carcass would not qualify as kosher. After a 24-h chill, 12th rib fat (BF), rib eye area (REA), kidney pelvic and heart fat percentage (KPH), final yield grade (FYG), marbling score (Marb), as well as the presence of beef quality defects were measured by trained university personnel. At the same time, an approximately 3.8-cm thick sample was obtained from the loin at the 13th rib, placed in a labeled bag inside a cooler, and transported immediately to the North Dakota State University's meats laboratory. Upon arrival, a subsample of loin (~2 g) was removed and frozen at − 10 °C for up to 60 d for later analysis of sarcomere length and troponin-T degradation. Two steaks (2.54-cm and 1.25-cm thick) were cut from the remaining sample, vacuum packaged (Cryovac® vacuum packager, Duncan, SC) and aged at 4 °C for 14 d and 7 d respectively until further processing and analyses. It is important to note that the steak samples had not been subjected to “koshering” that is, the samples had not been salted or soaked.
2.2. Warner–Bratzler shear force (WBSF) After aging for 14 d in darkness at 4 °C, the 2.54-cm steaks were frozen at − 20 °C until analysis for tenderness by WBSF. All samples from the three collection periods were evaluated on the same day. Prior to cooking and shear force measurements, steaks were thawed overnight in a 4 °C-cooler and then allowed to come to room temperature (approximately 18 °C) before being weighed. A copper-constantan thermocouple was inserted (Omega Engineering Inc., Stamford, CT) into the geometric center of the steak. Steaks were cooked on clamshellstyle grills (George Foreman grill Model No. GRP99, Columbia, MO) to an internal temperature of 71 °C and then removed from the grill and allowed to cool to room temperature (approximately 21 °C). Steaks were weighed again, and cook loss was calculated by dividing cooked weight by raw weight and subtracting the total from 100. Six, 1.27-cm cores were taken from each steak parallel to the muscle fibers and sheared once perpendicular to the muscle fibers for measurement of tenderness using a Warner–Bratzler shear force machine (G-R Manufacturing, Manhattan, KS) (AMSA, 1995).
2.3. Display life After aging for 7 d in darkness, the 1.25-cm steaks were removed from vacuum packaging, individually placed in white foam trays with absorbent pads (4S Trays, Pactiv, Lake Forest, IL), overwrapped with clear cellophane, and placed in a 4 °C cooler under continuous fluorescent light (Sylvania, 32-watt, T-8 Cool White, Sylvania, Danvers, MA). L*, a*, and b* color were measured at three locations on the steak surface, with the values being averaged for each day, on each steak every 24 h for 10 d using a Minolta colorimeter using a D65 illuminant and calibrated using a white calibration tile (Konica Minolta, Toyko, Japan). Steaks were randomly moved daily to mimic movement found in a retail case and to account for slight variations in light intensity.
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2.4. Myofibril extraction and sarcomere length Myofibrils were extracted using the method of Weaver, Bowker, and Gerrard (2009) from a subset of loin samples that were frozen 24-h post-mortem (n = 53) equally representing carcasses that qualified for kosher and those that did not. Briefly, an approximately 1 g sample was removed from the freezer, minced, and homogenized using a blender (Waring Laboratory Science, Torrington, CT) in 5 volumes of ice-cold rigor buffer [75 mM KCl, 10 mM imidazole, 2 mM MgCl2, 2 mM ethylenediaminetetraacetic acid (EDTA), 1 mM NaN3; pH 7.2; with 0.1 mM phenylethyl sulfonyl fluoride (PMSF)] using a Kinematica PT 10/35 Polytron homogenizer with PTA-10S generator (Brinkmann, Westbury, NY). After centrifugation at 20,000 ×g and 4 °C for 30 min, myofibrils were washed several times with rigor buffer and then resuspended in 5 volumes of rigor buffer and 5 volumes of glycerol and stored at −20 °C for approximately 2 months until further processing. To estimate sarcomere length, myofibrils were fixed on slides with 3% (v/v) formaldehyde in rigor buffer, mounted in media [75 mM KCl, 10 mM Tris (pH 8.5), 2 mM MgCl2, 2 mM EDTA, 1 mM NaN3, 1 mg/mL p-phenylenediamine, 75% (v/v) glycerol], and sealed under coverslips (Weaver, Bowker, & Gerrard, 2008). Five different microscopic field images were captured for each slide using the Zeiss Axio Imager M2 upright microscope equipped with high resolution AxioCamMRc3 camera and the A-Plan100x 1.25 oil Ph3 objective (Carl Zeiss Microscopy, LLC; Thornwood, NY). The first 20 myofibrils observed that were positioned in a straight-line orientation and at least 5 full sarcomeres in length were measured using Image-Pro Plus 5.0 software (Media Cybernetics, Bethesda, MD). The average sarcomere length for each slide (loin sample) was recorded. 2.5. Whole muscle protein extraction, SDS-PAGE electrophoresis, and troponin-T immunoblotting Whole muscle protein was extracted from frozen 24-h subset (n = 53) of loin subsamples as described by Huff-Lonergan, Mitsuhashi, Parrish, and Robson (1996). Briefly, 0.5 g of muscle tissue was minced and then homogenized in 5 mL of extraction buffer [10 mM sodium phosphate, pH 7.0; 2% (w/v) sodium dodecyl sulfate (SDS)] with a serrated pestle attached to a mechanical homogenizer (Eberbach Corporation, Ann Arbor, MI) at room temperature until well ground. The homogenate was clarified by centrifugation (1500 ×g) for 15 min at room temperature. The protein concentration of each cleared extract was determined using DC Protein Assay Reagents (BioRad Laboratories, Hercules, CA) based on Lowry, Rosebrough, Farr, and Randall (1951). Protein extracts were diluted with water to a final concentration of Table 1 Least squares means and standard errors for pre-harvest characteristics of heifers that qualified and did not qualify as kosher. Trait
Non-kosher (n = 85)
SEM
Kosher (n = 72)
SEM
P-value
Animal number/pen Chute scorea Blood lactate, mmol/L GtEb, s EtUc, s Vocalization scored EPe
10.6 2.97 7.48 53.7 78.1 1.09 1.03
0.35 0.15 0.60 1.92 2.75 0.15 0.16
10.3 2.85 7.78 46.5 83.2 0.47 0.92
0.37 0.16 0.63 1.99 2.88 0.16 0.17
0.53 0.60 0.73 0.01 0.20 0.01 0.64
a Chute score where 1 = calm, no movement; 2 = slightly restless; 3 = squirming, occasionally shaking the chute; 4 = continuous, very vigorous movement and shaking of the chute; and 5 = rearing, twisting of the body and struggling violently. b Gate to exsanguination, time from gate (v-belt) to exsanguination. c Exsanguination to insensibility, time from exsanguination to insensibility as defined by lack of corneal reflex. d Vocalization score where 0 = no vocalization; 1 = low intensity, singular vocalization; 2 = mild intensity, one to two vocalizations; and 3 = high intensity, two or more vocalizations. e Number of times the electrical prod was used.
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Table 2 Least squares means and standard errors for carcass characteristics of beef heifers that qualified and did not qualify as kosher.
the 30-kDa degradation Bandof a whole muscle protein extract control sample run on every gel.
Trait
Non-kosher (n = 85)
SEM
Kosher (n = 72)
SEM
P-value
2.6. Statistical analysis
HCWa, kg BFb (12th rib), cm REAc, cmb KPHd, % FYGe Marbf
336.8 1.17 78.8 2.00 2.55 454
8.15 0.10 1.87 0.01 0.13 18
354.8 1.14 84.7 2.00 2.38 413
6.96 0.08 1.61 0.01 0.12 15
0.10 0.82 0.02 0.18 0.33 0.09
Data indicating if a carcass qualified as Glatt kosher or not were obtained from North Dakota Natural Beef. Carcasses were designated as either kosher or non-kosher. Data were analyzed using PROC GLM procedures of SAS (Version 9.2, SAS Institute Inc., Cary, NC) with kosher as the source of variation in the model, with slaughter day used as a covariate, and least squares means were separated using the pdiff option of SAS. Color measurements were analyzed as repeated measures using kosher versus non-kosher as the sourced of variation and day as the repeated measure.
a
Hot carcass weight. Backfat. c Ribeye area. d Kidney, pelvic, and heart fat. e Final USDA yield grade, determined from components. f Marbling score where 300 = slight, 400 = small, 500 = modest, and 600 = moderate. b
3. Results and discussion 3.1. Pre-harvest stress measurements
0.64 μg/μL. One volume of each extract was combined with 0.5 volumes sample/buffer tracking dye solution [3 mM ethylenediamine tetraacetic acid (EDTA), 3% (w/v) SDS, 30 mM Tris, pH 8.0; 30% (v/v) glycerol, 0.003% (w/v) pyronine Y) (Wang, 1982) and 0.1 volumes of 2mercaptoethanol for a final protein concentration of 0.4 μg/μL. Gel samples were heated to 60 °C for 15 min and then frozen at − 80 °C for up to 10 d until electrophoresis. Individual sample protein extracts were loaded (3.2 μg protein) onto 1.5 mm thick mini polyacrylamide gels (5% stacking and 15% resolving with a 37.5:1 acrylamide:bis crosslinking and separated by electrophoresis in a running buffer [25 mM Tris, 0.19 M glycine, 1.7 mM EDTA, 0.1% (w/v) SDS] for 3.5 h at a constant voltage of 150. After electrophoresis, proteins were transferred onto polyvinylidene fluoride membranes (Immobilon-P, 0.45 μm pore size; Millipore Corporation, Billerica, MA) in a transfer buffer [25 mM Tris, 0.19 M glycine, 1.7 mM EDTA, 15% (v/v) methanol] using a wet tank transfer system with cooling at 90 V for 1.5 h. Membranes were incubated at room temperature in a blocking solution of 5% (w/v) nonfat dry milk in phosphate buffered saline (PBS)-Tween [80 mM sodium phosphate, dibasic; 20 mM sodium phosphate, monobasic, 100 mM sodium chloride, 0.1% (v/v) polyoxyethylene sorbitan monolaurate (Tween 20)]. After blocking, membranes were incubated overnight at 4 °C with mouse monoclonal anti-rabbit TnT antibody (clone JLT-12, Sigma T 6277, St. Louis, MO) diluted 1:45,000 in PBS-Tween. Blots were washed in PBS-Tween and then probed with goat anti-mouse IgG peroxidase conjugate (Sigma A 2554) diluted 1:45,000 in wash buffer for 1 h at room temperature. Blots were washed with the PBS-Tween solution, and ECL Prime Western Blotting Detection Reagents (GE Healthcare Biosciences, Piscataway, NJ) were used to detect immunoreactive bands. A molecular weight marker was used to estimate the molecular weights of the immunoreactive bands. Chemiluminescence was photo-documented and measured with an Alpha Innotech FluorChem FC2 image analysis system with supporting AlphaEaseFC software (Protein Simple, Santa Clara, CA) using 1-D multi analysis with horizontal baseline and a band width sample of ~60% of the total band width. All band intensities were normalized (band area value/control area value) to the intensity of
Least squares means and standard errors calculated for pre-harvest stress measurements of beef heifers are presented in Table 1. Number of animals per pen, chute score, EtU, and number of times electrical prods were used did not differ between those cattle that qualified for kosher and those that did not (P N 0.10). Grandin and Regenstein (1994) found that most cattle lose consciousness 5 to 60 s after kosher exsanguination; however, these findings of time to insensibility are consistent with Blackmoore (1984) and Daly, Kallweit, and Ellendorf (1988) who state that it may take over a minute for the animal to lose consciousness. In the present study, we used blood lactate as a potential objective indicator of stress during the slaughter process while chute score, GtE, and vocalization scores were used as subjective scores to try and better evaluate stress at the time of slaughter. Apple et al. (1995) measured blood lactate levels in lambs subjected to stress and found that as stress level increased, blood lactate levels were higher from blood collected after stunning and exsanguination. The handling stress levels in this plant were relatively high compared to other kosher plants and conventional plants. When both kosher and non-kosher groups are combined, over half the cattle vocalized. Data collected in two other kosher plants with upright restraint indicated that 99% to 98% of the cattle remained silent (Grandin and Regenstein, 1994). Additional data from 22 conventional plants indicated that on average, only 3% of the cattle vocalized and all the others were silent (Grandin, 2000), and the worst plant had a 17% vocalization score. Electric prod use also occurred on almost 100% of the cattle in the plant studied. Six plants, which had a V conveyor restrainer, used the electric prod on an average of 39% of the cattle (Grandin, 1998). Cattle were scored as either electric prodded or not electric prodded. The lactate levels were also higher than those in Gruber et al. (2010). There is a possibility that high levels of handling stress may have contributed to lengthening the time required for the animals to become insensible. Blood lactate level did not differ (P = 0.73) between kosher and non-kosher qualified cattle. Cattle that qualified for kosher were less vocal (P b 0.01) and took less time from entering the gate to exsanguination (P = 0.01). Grandin (1998) observed 112 cattle through six different plants and found that cattle vocalize after adverse events such as
Table 3 Least squares means and standard errors for tenderness measurements of beef heifers that qualified and did not qualify as kosher. Variable a
WBSF , N Sarcomere length, μm Troponin-T, 41-kDa bandb Troponin-T, 30-kDa bandb a b
n
Non-kosher
SEM
n
Kosher
SEM
P-value
83 27 27 27
33.07 1.92 4.67 0.26
0.34 0.03 0.42 0.04
77 26 26 26
41.97 1.84 6.12 0.07
0.33 0.03 10.43 0.04
b0.0001 0.09 0.02 b0.01
Warner–Bratzler shear force. Units are relative to the 30-kDa band control loin sample which was set to 1.0.
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Fig. 1. Minolta L*color score values of beef loin steaks from cattle that either qualified (Glatt) or did not qualify as kosher.
electrical prodding, slipping, or excessive pressure in a powered restraining device. Grandin (1980) also found that short term acute stress results in a buildup of lactic acid in the blood. Further, animals that are inverted prior to exsanguination have higher blood cortisol levels as well as greater vocalization scores (Dunn, 1990), suggesting that vocalization may be used as an indicator of stress level. 3.2. Carcass measurements Carcass characteristics of beef heifers are presented in Table 2. The BF, KPH, and FYG were not different (P N 0.15) between kosher and non-kosher cattle, although non-kosher cattle tended (P = 0.09) to have higher marbling scores. Daniel, Held, Brake, Wulf, and Epperson (2006) found that lambs with severe lung lesions have lower average daily gain (ADG) and higher average marbling scores than those with normal lungs. This suggests that ruminants with lung health issues may spend more time in the finishing phase, allowing for an increase in intramuscular fat. Kosher-qualified cattle had larger REA (P = 0.02) and tended (P = 0.10) to have heavier HCW than those that did not qualify. Reinhardt, Busby, and Corah (2009) reported that more excitable cattle, as measured by chute score, had a lower HCW which corresponds to these findings. Cattle with increased numbers of lung lesions also have decreased HCW and REA (Reinhardt et al., 2009; Schneider et al., 2009) suggesting that cattle with health issues in the feedlot may not reach full genetic potential for growth. Overall, these data suggest that there may be a phenotypical difference between cattle that qualify for kosher and that that do not, with kosher cattle being larger, more muscular, and having less marbling in the longissimus at the 12th rib. 3.3. Beef tenderness measurements Least squares means and standard errors for tenderness measurements of beef heifers are presented in Table 3. Loin steaks from kosher
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Fig. 3. Minolta b* color score values of beef loin steaks from cattle that either qualified (Glatt) or did not qualify as kosher.
carcasses were less tender than those from non-kosher carcasses (P b 0.0001). Longissimus muscle from kosher-qualified cattle tended (P = 0.09) to have shorter sarcomere lengths than those from nonkosher-qualified cattle. Shorter sarcomere length usually indicates lower meat tenderness (Aberle, Forrest, Gerrard, & Mills, 2001) which agrees with our findings. Moreover, cattle with calmer temperaments possess longer sarcomeres than those with excitable temperaments (King et al., 2006; Gruber et al., 2010. 3.4. Display life color score measurements Daily L*, a*, and b* color values of beef loin steaks aged in vacuum packages for 7 d and then over-wrapped in cellophane and displayed under fluorescent lighting for 10 d are shown in Figs. 1, 2, and 3. On each individual day kosher steaks had lower (P b 0.05) L*, a* and b* values. Also for each day, L*, a*, and b* values differed (P b 0.05) from the previous day. However the interaction of kosher “grade” and time was not significant. Wulf, O'Connor, Tatum, and Smith (1997) found that steaks displaying a higher L*,a* and b* value (lighter, more red, more yellow) are more tender, which is supported by the findings of this research. In addition, Breidenstein, Cooper, Cassens, Evans, and Bray (1968) and Wulf et al. (1997) found that steaks with higher marbling scores also have higher color scores. 4. Conclusion In summary, cattle that qualified as kosher had calmer temperaments and were able to move through the abattoir more quickly when compared with cattle that did not qualify, mostly due to lung adhesions. In addition, cattle that qualified as kosher were heavier muscled and larger, as evident by the larger REA and heavier HCW. Factors of carcass type and temperament could be useful selection tools for cattle buyers looking to purchase cattle for the kosher market. This may also help reduce the percentage of cattle purchased by kosher buyers that do not qualify for kosher. Lastly, we found that kosher steaks are less tender than non-kosher steaks. Further research is needed to understand the relationship between kosher grade and tenderness and the possibility of producing a more tender kosher product. References
Fig. 2. Minolta a* color score values of beef loin steaks from cattle that either qualified (Glatt) or did not qualify as kosher.
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