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The Effect of Blood Removal on Oxidation and Shelf Life of Broiler Breast Meat

C. Z. Alvarado^*,1, M. P. Richards, S. F. O’Keefe and H. Wang

^* Department of Animal and Food Sciences, Box 42141, Texas Tech University, Lubbock, TX 79409; Department of Animal Sciences, University of Wisconsin-Madison, 53706; and Department of Food Science and Technology, Virginia Tech, Blacksburg 24061

¹ Corresponding author: christine.alvarado{at}ttu.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Blood components, especially hemoglobin, are powerful promoters of lipid oxidation and may decrease the shelf life of meat products. Therefore, this study examined different slaughter techniques to determine their effects on pH (24 h), color (L*a*b* values at 24 h), lipid oxidation, residual hemoglobin concentration (24 h), and sensory evaluation (d 1 and 4 postmortem; PM) in broiler breast fillets. The treatments included 1) CO₂ slaughter and not bled, 2) no stunning and bled, 3) electrical stunning (ES) and bled, 4) CO₂ stunning and bled, and 5) ES and decapitation. The birds were conventionally processed, and analyses were performed at 24 h PM except residual hemoglobin for which the samples were frozen (–80 ° C) until analyses ( < 2 mo). There were no significant differences in pH or b* values at 24 h PM among any of the treatments. L* values were significantly higher, indicating lighter fillets in the ES and decapitated birds compared with the darker fillets from the CO₂ stunned and bled birds. The CO₂ slaughter and not bled birds had significantly higher a* values, indicating more red color, when compared with the ES and bled and decapitated birds. There were no significant differences in the residual hemoglobin contents in the broiler breast muscle when comparing all of the treatments except CO₂ slaughter and not bled, which was significantly (around 15%) greater. Overall TBA-reactive substances (TBARS; raw, cooked at 24 h, and cooked at 72 h PM) indicated that ES and bled birds had the lowest TBARS when compared with the remaining treatments. Consumer panels detected increased aroma (chicken meaty and warmed-over aromas) and flavor (chicken meaty and warmed-over flavors) in not bled samples at 24 h PM. By 72 h PM, however, there were no significant differences in aroma or flavor. Therefore, different slaughter and bleeding method may affect color and sensory properties of the broiler breast fillets, and the ES and decapitation method had the most favorable results for sensory quality.

Key Words: decapitation • meat quality • hemoglobin • stunning • lipid oxidation

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
According to the 1958 Humane Method of Slaughter Act, all processors of food animals must render USDA-inspected animals insensible to pain before exsanguination. Even though this act excludes poultry, electrical stunning (ES) is still widely used in turkey and broiler processing to comply with the Poultry Inspection Regulations of 1984. This regulation states that poultry will be slaughtered in a manner resulting in thorough bleeding of the carcass and it must be ensured breathing has ceased prior to entrance of the carcasses into the scalder.

The industry justifications for ES systems are to rapidly immobilize the bird, reduce struggle associated with slaughter, increase uniformity of heart beat in the broiler, and improve the bleed-out rate. Electrical stunning has always been an inexpensive, safe, and convenient method of slaughter (Bilgili, 1992; Fletcher, 1993). High voltage (~120 mA) ES is most commonly used in the European Union (EU) and has been associated with a higher incidence of carcass damage, such as red wing tips, broken bones, and hemorrhages (Gregory and Wilkins, 1989). High voltage ES can cause approximately 90% heart fibrillation resulting in inefficient bleeding, severe muscle contractions causing increased hemorrhaging, and even death before exsanguination, which can lead to poor carcass and meat quality. However, this high-voltage method is usually favored in the EU because it can lower the risk of a bird regaining consciousness during the slaughter process.

Low-voltage (~13 to 15 mA) ES is most often used in the United States and can decrease carcass quality damage and hemorrhaging associated with high-voltage ES; however, a bird can regain consciousness if not slaughtered within approximately 2 min of stunning. Low voltage ES has been shown to negatively affect early blood loss but does not affect total blood loss after the 90- to 120-s exsanguination period (Gregory, 1993; Papinaho and Fletcher, 1995). Even though ES can decrease the rate of pH decline early PM, ES has been shown to have little effect on breast muscle pH and R-values, after the 4 to 6 h PM aging period (Papinaho and Fletcher, 1996; Alvarado and Sams, 2000).

There are several alternative methods to ES including gas stunning using CO₂, cervical dislocation, and even no stunning because ES is not required by law before slaughter of poultry. Gas (CO₂) stunning is an alternative method used by the European Economic Commission because it can quickly render the bird unconscious. Normally a mixture of gases is used in gas stunning including CO₂ (30 to 55%) and the inert filler Ar (Mojan Raj and Gregory, 1990). Carbon dioxide has a unique property in that it reduces the pH of the cerebrospinal fluid of the bird, which results in an anesthetic response, whereas Ar simply displaces air and leads to anoxia (Eisele et al., 1967). Stunning broilers with Ar or CO₂ did decrease carcass defects and poor quality meat when compared with ES (Mojan Raj et al., 1992). Further studies by Hirschler and Sams (1993) have indicated that CO₂ stunning reduces the incidence of carcass defects, specifically, broken clavicles and hemorrhages in the breast, thigh, and shoulder when compared with ES. Also, this method of stunning has been shown to accelerate rigor development as indicated by a more rapid pH decline early PM and, therefore, can reduce the need for aging (Mojan Raj, 1994). This accelerated rigor development could be explained by the increased anoxic convulsion (increased wing flapping) observed in CO₂ stunned bird, which causes increased utilization of adenosine triphosphate (ATP) by the muscles, compared with in the ES-stunned bird (Mojan Raj et al., 1992). In contrast, Kang and Sams (1999) reported that a recoverable stun did not accelerate rigor mortis development in broilers. Studies have indicated that even though the ES birds bleed out more efficiently within 60 s, there is no difference between ES and CO₂ stunning with regard to bleed-out efficiency after the 90-s exsanguination period.

After being stunned, general slaughter procedures are used to exsanguinate the broiler. Generally, this includes a bilateral or a unilateral neck cut to severe the carotid artery and jugular vein. However, recent research has focused on a new method of slaughter, decapitation. Decapitation is an acceptable means of killing chickens as described by the American Veterinary Medical Association (1993). Decapitation after low-voltage ES can be an alternative to high-voltage stunning used in the EU, which can cause meat quality problems such as hemorrhaging. Decapitation can cause a higher pH at 24 h postmortem and has no effect on color, water-holding capacity, or tenderness when compared with other methods (McNeal and Fletcher, 2003). Studies have shown that decapitation can be used successfully as an alternative to conventional ES method based on ensuring an irreversible loss of consciousness while not negatively affecting carcass and meat quality (McNeal et al., 2003; McNeal and Fletcher 2003).

Hemoglobin and myoglobin are important factors in determining meat quality. Bruises, hemorrhages, and poor bleeding efficiency can negatively affect color of the meat and skin; are considered to be major quality defects; and can cause undesirable discoloration and short shelf life (Griffiths and Nairn, 1984). Residual blood in the carcass is often associated with a meaty flavor and decreased shelf life. There are 2 main heme proteins, hemoglobin and myoglobin. Generally, myoglobin is relatively unimportant in connection with broiler breast meat quality. Studies by Nishida and Nishida (1985) and Kranen et al. (1999) reported that there was no detectable myoglobin in chicken breast muscle and that hemoglobin was the only detectable heme pigment found in chicken breast muscle. Therefore, blood content in the breast muscle of broilers is hemoglobin, and excessive hemorrhaging of blood into broiler breast muscle caused by different stunning and slaughter techniques can increase hemoglobin content. This increased hemoglobin content in the muscle can decrease shelf life and can cause increased oxidation.

There are several methods of rendering the bird unconscious (no stun, gas, ES, decapitation) before slaughter that are being currently used or researched as alternatives, and these methods can affect hemorrhaging and blood loss. Therefore, the objectives of this study were to 1) compare current and alternative slaughter method with regard to pH and color and 2) to determine residual hemoglobin in the breast muscle and relate this hemoglobin to oxidation, sensory properties, and shelf life of broiler breast meat.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
A total of 140 broilers were raised to 42 d of age on litter lined floor pens, fed according to the NRC guidelines for broilers (1994), and allowed access to water ad libitum. Feed was withdrawn from the broilers 12 h before processing, but the birds were allowed access to water until 2 h before transportation to the processing facility. The broilers were conventionally processed in a pilot processing facility, and the following treatments were applied: 1) CO₂ slaughter (70% Ar and 30% CO₂) and not bled; 2) no stunning and bled; 3) ES (Model SF-7000, Simmons Engineering Corp., Dallas, GA) in a 1% saline bath, 13 mA, 7 s, 500 Hz, DC and bled using a unilateral neck cut; 4) CO₂ stun (70% Ar and 30% CO₂) and bled using a unilateral neck cut; and 5) ES in a 1% saline bath, 13 mA, 7 s, 500 Hz, DC and decapitation (McNeal et al., 2003). The exsanguinated birds were allowed to bleed for 90 s. All birds were conventionally scalded (61 ° C, 45 s), picked in a rotary drum picker for 25 s, and manually eviscerated. The broiler carcasses were allowed to chill in an agitated chill bath for a total of 1.25 h (15 min in a prechiller at 12 ° C and 60 min in a chiller at 4 ° C).

After being chilled, the carcasses were stored in a 4 ° C cooler overnight and deboned at 24 h postmortem (PM). The left breast fillets were analyzed for pH (24 h PM) using a pH meter (Model 240, IQ Scientific Instruments Inc., San Diego, CA) and a piercing probe (pH 26-SS, IQ Scientific Instruments, Inc.). Color values (L*a*b*; 24 h PM) were measured with a colorimeter (Choma Meter Model CR-200, Minolta Corp., NJ) on the medial surface of each fillet by averaging 3 readings. We also analyzed lipid oxidation [TBA-reactive substances (TBARS) in raw meat on d 1 PM and in cooked meat on d 1 and 4 PM], sensory evaluation (d 1 and 4 PM), and shelf life by aerobic plate count (APC; 3M Petrifilm Aerobic Plate Count, 3M Microbiology Products, St. Paul, MN) on d 1 and 6 PM. The samples used for APC were stored in an overwrap tray package in a 4 ° C cooler until analyses (d 1 and 6 PM). The APC were plated according to standard procedures used with Petrifilm (3M Microbiology Products) plates.

The TBARS were measured using a modification of the Spanier and Traylor (1991) procedure as described by O’Keefe and Wang (2006). This is an extraction procedure in which homogenized muscle is allowed to react to TBA reagent, and the chromagen is extracted using pyridine-butanol for absorbance measurement (spectrophotometer, Model 21D, Milton Roy, Rochester, NY) at 532 nm.

Sensory evaluation was carried out on freshly cooked and cooked-then-stored (3 d at 4 ° C) breast muscle. At d 0, samples were used for immediate sensory evaluation or were individually packaged in plastic bags and stored in a home refrigerator held at 4 ° C. A total of 12 panelists (equal males and females, ages 21 to 46 yr) were trained to use a 15-point unstructured line scale (where 1 = least and 15 = most) for quantitative descriptive analysis of chicken aroma, chicken flavor, warmed-over aroma, and warmed-over flavor. Three training sessions were used to familiarize panelists with the scale when they were given fresh and warmed-over chicken breast samples. Samples were provided at room temperature, and unsalted crackers and water were also provided.

The right breast fillets were used to determine hemoglobin content. Tissue was minced (4-mm die) and homogenized in 80 mM KCl, 10 mM TRIS, and 1 mM EDTA, pH 8.0 (1:9 weight of muscle:volume of buffer; Kranen et al., 1999). Homogenate was filtered through cheesecloth and centrifuged at 105,000 x g. The supernatant was then passed through Whatman no. 1 filter paper, and heme protein content was measured using sodium dithionite reduction and bubbling with CO before we recorded the absorbance peak between 440 and 400 nm (Brown, 1961). Bovine hemoglobin was used as a standard. Values were expressed as micromoles of hemoglobin per kilogram of tissue.

The GLM procedure of the SAS software (SAS Institute, 2004) was used to analyze the data, and the means were separated using Duncan’s multiple-range test. Sensory testing and statistical evaluation were conducted according to ASTM procedures. The heme content was analyzed in a randomized, complete block, split-plot design.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
The decline of pH is related to accumulation of lactic acid within the muscle and ATP depletion caused by PM glycolysis (Lawrie, 1991). The pH can be an indicator of the quality of meat. Generally, a low pH at 24 h PM can indicate poor meat quality (Swatland, 1993; Fernandez et al., 1994). This poor quality meat can be pale, have lower water-holding capacity with increased purge and tenderness problems, and have a soft texture in the uncooked meat. The pH results from this experiment are indicated in Table 1. There were no significant differences in pH among the treatments, indicating that type of stunning may not affect pH at 24 h PM. Previous reports have indicated that some ES procedures delay PM glycolysis because of decreased struggling by broilers and turkeys (Lee et al., 1979; Thomson et al., 1986; Kim et al., 1988; Murphy et al., 1988). Fillets from stunned bird have been shown to have higher pH, ATP, and creatine phosphate levels and lower lactate levels early PM when compared with fillets from controls that were not stunned. Stunning also has been reported to minimize perimortem struggle, which decreases the utilization of glycogen by 50%, therefore resulting in a higher muscle pH early PM (de Fremery and Lineweaver, 1962). However, Papinaho et al. (1995) reported that ES does not directly affect the PM biochemistry of breast muscles. These studies also indicated that by 24 h PM, there were no significant differences in pH values between stunned and nonstunned birds. According to McNeal and others (2003) there were no significant differences between decapitated and ES birds at 24 h PM. Therefore, the stunning and bleeding method used in this study did not affect pH at 24 h PM.

Redness is indicated by a* value (Table 1). The results from this study indicate that the CO₂ slaughter and not bled treatment had significantly higher a* values (indicating more redness) when compared with the ES and decapitation treatments. The CO₂ not bled slaughter treatment was expected to have a more red appearance because of the lack of bleed out. Electrical stun and ES decapitation treatments had lower a* values compared with the other treatments but were not significantly different. Previous reports have indicated no difference in a* value between the ES and decapitation methods (McNeal and Fletcher, 2003; McNeal et al., 2003)

Blood content in breast muscle from birds subjected to different slaughter treatments can be estimated by measuring the hemoglobin content in aqueous tissue extracts. There was no significant difference in hemoglobin content among treatments in which a bleeding step was used (Table 2). Mean hemoglobin content ranged from 8.37 to 8.72 µmol/kg of tissue in the bled groups, which was 13 to 17% lower in extracts from chicken breast muscle of bled bird compared with not bled birds. This finding indicated that bleeding removed little blood from the breast muscle. Three to 4 capillaries surround each muscle fiber (Mathieu-Costello, 1993), which might explain why there is poor blood removal from muscle after bleeding. When the neck is cut to bleed, the blood pressure drops rapidly so that there is not enough driving force to empty the numerous capillary beds in the muscle. This observation has been noted in previous research and indicates that hemoglobin content in the breast muscle of not bled, stun and bled, electrocuted and bled, and decapitated and halal killed chickens is 0.36, 0.19, 0.22, 0.17, and 0.17 mg/g of soft tissue, respectively (Griffiths et al., 1985).

Lipid oxidation is a major cause of quality deterioration in foods. Inefficient and improper bleeding may cause more blood (hemoglobin) to be retained in the breast meat. This retained hemoglobin could cause increased oxidation to occur directly, causing rancidity and reduced shelf life. Therefore, we measured TBARS in raw broiler fillets (d 1 PM) and cooked broiler fillets (d 1 and 4 PM) as an indicator of lipid oxidation. The results from the TBARS analysis are in Table 3. In raw breast muscle (d 1 PM), TBARS from CO₂ slaughter not bled samples were significantly greater than in ES, CO₂ stun, and decapitation samples. This finding could be partly explained by the fact that hemoglobin content was approximately 15% greater in extracts from not bled treatments compared with bled treatments (Table 2). When we compared the different bleeding treatments, ES and CO₂ stunning methods had lower incidence of lipid oxidation compared with the no stun treatment and were slightly lower than in decapitated birds.

Electrical stunning with bleeding decreased lipid oxidation more effectively than other stunning with bleeding methods, yet hemoglobin content was not lower in samples from ES-treated birds (Tables 2 and 3). It is possible that rupture of blood vessels and erythrocytes in the filets decreased when low-voltage ES was used compared with other stunning methods. Previously it has been shown that bleeding decreases lipid oxidation in intact but not in minced mackerel dark muscle compared with controls that are not bled (Richards and Hultin, 2002). This finding is attributed to increased rupture of blood vessels in the intact tissue from not bled fish because blood pressure is not released without a bleeding step. Mincing dark of muscle from bled and not bled fish, however, probably removed the effect of pressure-mediated blood vessel rupture because the mechanical action of mincing induces rupture, regardless of treatment. Slaughtering is a stressful period, and blood vessel rupture in chicken filets could be variable due to the stunning regimen used. When tissue extracts are prepared for hemoglobin analysis, the tissue is disintegrated so that hemoglobin from ruptured and not ruptured blood vessels will be measured equally. This procedure may explain why ES decreased lipid oxidation more effectively than other stunning methods yet hemoglobin content was not lower in samples from ES-treated birds.

Data for total aerobic plate counts (Table 4) show that the CO₂ no bleed treatment had significantly more bacteria than the other treatments, which were not different from each other at d 0 and 5. The increase in bacteria could have been due to more readily accessible nutrients available for bacterial growth in the not bled treatment. The CO₂ not bled treatment also had the greatest increase in APC between d 0 and 5.

	ACKNOWLEDGMENTS

 
This project was supported in part by the College of Agricultural and Life Sciences, University of Wisconsin-Madison, Hatch project WIS04904 and USDA project S-292.

Received for publication May 22, 2006. Accepted for publication September 18, 2006.

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