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Meat Quality and Rigor Mortis Development in Broiler Chickens with Gas- Induced Anoxia and Postmortem Electrical Stimulation1 A. R. SAMS2 and C. S. DZUIK Department of Poultry Science, Texas A&M University System, College Station, Texas 77843-2472 ABSTRACT This study was conducted to evaluate the lower pH values at 1 h postmortem. The Ar + ES treatment combined rigor-accelerating effects of postmortem electri- had a greater R-value than the ES treatment, which was cal stimulation (ES) and argon-induced anoxia (Ar) of greater than either the Ar or 1-h controls, which, in turn, broiler chickens. One hundred broilers were processed were not different from each other. The ES treatment had in the following treatments: untreated controls, ES, Ar, the lowest L* value, and ES, Ar, and Ar + ES produced or Ar with ES (Ar + ES). Breast ﬁllets were harvested at signiﬁcantly higher a* values than the 1-h controls. For 1 h postmortem for all treatments or at 1 and 6 h postmor- the IQF ﬁllets, the ES and Ar + ES treatments were not tem for the control carcasses. Fillets were sampled for pH different in shear value but were lower than Ar, which and ratio of inosine to adenosine (R-value) and were then was lower than the 1-h controls. The same was true for individually quick frozen (IQF) or aged on ice (AOI) until the AOI ﬁllets except that the ES and the Ar treatments 24 h postmortem. Color was measured in the AOI ﬁllets were not different. These results indicated that although at 24 h postmortem. All ﬁllets were then cooked and ES and Ar had rigor-accelerating and tenderizing effects, evaluated for Allo-Kramer shear value. ES seemed to be more effective than Ar; there was little The Ar treatment accelerated the normal pH decline, enhancement when Ar was added to the ES treatment whereas the ES and Ar + ES treatments yielded even and ﬁllets were deboned at 1 h postmortem. (Key words: argon, electrical stimulation, rigor mortis, stunning, tenderness) 1999 Poultry Science 78:1472–1476 INTRODUCTION a larger blood loss from birds treated with CO2 compared with birds treated with traditional electrical stunning. The poultry industry currently uses electrical stunning Mohan Raj et al. (1990a,b) suggested that birds could be to immobilize birds for killing. Fletcher (1993) reported stunned in their transport crates, thus eliminating the that when birds are rendered unconscious by electricity, stress associated with uncrating and shackling. A prob- it allows for ease of neck cutting. Bilgili (1992) compared lem associated with stunning in coops is the increasing U.S. and European-type stunning systems and stated that O2 concentrations in the stunning tank after repetitive European stunning systems use higher amperage than batches. If this occurs, the birds will not be sufﬁciently those in the U. S. High stunning amperages are required stunned and will regain consciousness rapidly between to achieve an irreversible state of unconsciousness; there- the gas chamber and kill machine. To reduce this type of fore such amperages are required in Europe because they problem, Mohan Raj et al. (1990a) suggested that birds are presumed to be more humane. However, although should be killed in their transport coops as opposed to stunning with high electrical currents provides irrevers- stunned only. ible unconsciousness, it also increases the occurrence of In addition to minimizing stress and decreasing down- carcass damage (Gregory and Wilkens, 1993). It is because graded carcasses, Ar-induced anoxia (Ar) has been re- of this carcass damage problem that new methods of ported to produce a more advanced state of rigor mortis poultry immobilization have been researched. development by exhibiting a rapid decrease in pH. Mohan Gas stunning has been extensively studied as an alter- Raj et al. (1992) reported that this decrease in pH is caused native to electrical stunning. Kotula et al. (1957) observed by anoxic convulsions (wing ﬂapping) during death that accelerates the postmortem utilization of adenosine tri- Received for publication December 14, 1998. phosphate (ATP) by the muscles. Furthermore, birds Accepted for publication May 25, 1999. 1 This research was supported by Praxair, Inc.; grant 999902-147 from the Texas Higher Education Coordinating Board Advanced Technology Development Program; and a grant from the Texas Agricultural Experi- Abbreviation Key: AOI = aged on ice; Ar = argon-induced anoxia; ment Station Research Enhancement Program. Ar + ES = argon-induced anoxia with electrical stimulation; ATP = 2 To whom correspondence should be addressed: asams@poultry. adenosine triphosphate; ES = electrical stimulation; IQF = individually tamu.edu quick frozen; R-value = ratio of inosine to adenosine. 1472 COMBINED METHODS OF ACCELERATING RIGOR MORTIS 1473 killed with Ar produced the lowest incidence of broken Birds from all treatments were placed on shackles and bones compared with the CO2 and electrically stunned killed by allowing them to bleed for 90 s through a unilat- treatments (Mohan Raj et al., 1990b). Birds exposed to eral neck cut severing the carotid artery and the jugular Ar exhibited a rapid decrease in muscle pH, indicating vein. The ES and Ar + ES treatments were then immedi- advanced rigor mortis development that allowed the ately electrically stimulated (450 V, 750 mA, AC, 60 Hz, breast ﬁllets to be removed 2 to 3 h postmortem without 2 s on/1 s off for 5 pulses) by placing their necks in a adversely affecting the texture of the meat (Mohan Raj et charged 1% NaCl bath with the shackle-line as the al., 1991; Mohan Raj and Nute, 1995). Filleting broiler ground. All birds were then scalded at 63 C for 25 s, breast meat at an early postmortem time would constitute picked in a rotary drum picker4 (25 s), manually eviscer- less aging than the 4 to 6 h currently required with electri- ated, prechilled (10 to 13 C for 15 min), and chilled in cal stunning (Stewart et al., 1984). ice-slush (1 to 2 C for 30 min). Both breast ﬁllets from all Electrical stimulation (ES) has also been proposed to carcasses, except the 6-h controls, were harvested imme- accelerate rigor mortis development and reduce the aging diately after chilling (at 1 h postmortem) using the method time before deboning. Li et al. (1993) and Sams (1999) described by Hamm (1981). reviewed the mechanisms and commercial implementa- The caudal tip (4 cm) of each left ﬁllet was removed tion of ES in poultry processing. Basically, electricity is for analysis of the ratio of inosine to adenosine (R-value) pulsed through a carcass immediately after death to in- and pH analysis. The tip and remaining ﬁllet were placed duce muscle contraction and thereby accelerate ATP utili- in separate labeled plastic bags and individually quick zation. Sams (1999) stated that ES can be delivered to frozen (IQF) by placing them in liquid N2. The IQF condi- carcasses in a poultry processing plant at commercial tions were included to evaluate what may be the worst killing line speeds and that the short time needed allows possible tenderness situation because the IQF process will the ES system to be easily implemented into existing kill/ prevent any aging that will occur after deboning and the bleed areas of the processing plant. early postmortem freezing may induce cold shortening Treating broiler chickens with Ar and postmortem ES (Locker, 1985). The caudal tips (4 cm) were removed from have each been researched thoroughly, and both have right-side ﬁllets at 1 h postmortem for moisture analysis the potential of a great impact on efﬁciency and meat using the press method described by Urbin et al. (1962). quality. However, there has been no research conducted This tip and the remaining right-side ﬁllet were placed on any possible interaction between Ar stunning and in separate labeled plastic bags and aged on ice (AOI) at postmortem ES, despite reports that both have the effect 1 to 3 C until 24 h postmortem. Color of the remaining of accelerating rigor mortis development. Therefore, the right-side ﬁllet portion was measured at 24 h postmortem purpose of this study was to evaluate any combined effect and then frozen. The ﬁllets from both sides of the 6-h these techniques may have on the meat quality of early- control carcasses were excised at 6 h postmortem, tips harvested broiler breast ﬁllets. were removed, and ﬁllets and tips were handled with the same procedure (including color) as described for their MATERIALS AND METHODS respective 1-h counterparts. The 6-h control left-side ﬁllets In each of two trials, 50 broilers at 7 wk of age were and tips were bagged, placed in liquid N2, and stored at obtained from a local poultry processor and housed for 2 −75 C until analyzed. d prior to slaughter at the Texas A&M University Poultry Both AOI and IQF ﬁllets were baked from the frozen Center and fed a commercial diet that met NRC recom- state to an internal temperature of 77 C as monitored mendations. Feed (but not water) was withdrawn 10 h with a probe thermometer5. The ﬁllets were then cooled before processing. Ten birds were processed in each of to room temperature and sheared using an Instron Uni- the following ﬁve treatments: unstunned controls with versal Testing Machine6 with a 10 blade Allo-Kramer breast ﬁllets deboned at 1 and 6 h postmortem and ES, shear-compression cell as described by Sams (1990.) Each Ar, and Ar + ES all with ﬁllets deboned at 1 h postmortem. left-side ﬁllet tip (IQF) was divided and used for R-value The 6 h control was included to provide a point of com- and pH. The left half of each left-side ﬁllet tip was used parison with current U.S. industry standards for aging to measure the ratios of the absorbance at 250 nm to the time prior to deboning (4 to 6 h). The Ar- and Ar + ES- absorbance at 260 nm (R-value) (Khan and Frey, 1971). treatment birds were placed in a wooden box (inside The right-side portion of the left-side IQF ﬁllet tip was dimensions: 1.2 m long, 0.9 m wide, and 0.6 m tall with used to determine postmortem pH using the iodoacetate a gas inlet at one end and a Y-shaped manifold along method (Jeacocke, 1977; Sams and Janky, 1986). The color the length of the chamber’s bottom) with <2% O2 (air measurements L* and a* were made using a portable displaced by Ar) for 2.5 min until dead. The O2 concentra- Minolta Chroma Meter7. One color measurement per ﬁllet tion in the box was measured with an O2 meter3. was taken at 24 h postmortem on each right-side (AOI) ﬁllet. The measurement was taken on the external surface 3 Model OXOR II, Barcarach, Pittsburgh, PA 15238. of the muscle at a point under the feather tract away from 4 Model SP-30-SS, Brower, Houghton, IA 52631. apparent lightening caused by scalding. 5 Traceable digital thermometer, Control Company, Friendswood, The data in this completely randomized design were TX 77546. 6 Model 1011, Instron Corp., Canton, MA 02021. subjected to ANOVA using treatment system (1-h control, 7 Model CR-200, Minolta Corp., Ramsey, NJ 07446. 1-h Ar, 1-h ES, 1-h Ar + ES, 6-h control) as the main effect 1474 SAMS AND DZUIK TABLE 1. Shear values (kg/g), R-values, pH, and L* and a* values for breast ﬁllets deboned at 1 or 6 h postmortem from carcasses that had received no treatment or received electrical stimulation (ES) and/or been killed with argon (Ar) and then individually quick frozen (IQF) or aged on ice (AOI) Shear values Postmortem Treatment deboning time IQF AOI R-value1 PH1 L*2 a*2 Control 1 18.79a 11.94a 0.92d 6.29a 54.86ab 4.44c ES 1 10.43c 8.74bc 1.12c 5.93c 53.27b 5.19ab Ar 1 14.57b 9.63b 0.97d 6.12b 55.09ab 5.11b Ar + ES 1 9.48c 7.51c 1.23b 5.84c 54.35ab 5.74a 6-h Control 6 6.25d 4.60d 1.38a 5.67d 55.82a 5.22ab Pooled SEM 0.64 0.35 0.02 0.03 0.43 0.09 Means (n = 18 per mean) within a column with no common superscript differ (P ≤ 0.05). a–d 1 At deboning time. 2 Measured at 24 h postmortem. and the residual mean square as the error term (SAS same trend of accelerated pH decline has been observed at Institute, 1985). Signiﬁcance of differences among treat- 20 min postmortem in Ar-killed broilers (Mohan Raj et ment means was tested with Duncan’s multiple range al., 1991; Poole and Fletcher, 1995) and turkeys (Raj, 1994). test (SAS Institute, 1985). Because there was no signiﬁcant These results were also consistent with previously ob- interaction between trial and treatment, the data from the served signiﬁcant decreases in pH in ES-treated broilers two trials were pooled. (Thompson et al., 1987; Lyon et al., 1989; Sams et al., 1989; Walker et al., 1994) and in ES-treated turkeys (Maki and RESULTS AND DISCUSSION Froning, 1987). The ES treatment signiﬁcantly improved the effectiveness of the Ar treatment at accelerating pH R-value estimates the ATP depletion in the muscle by decline, but Ar did not provide a similar enhancement measuring the ratio of inosine to adenosine (Khan and to the ES treatment. Because the 6-h controls have a more Frey, 1971). As aging time increases and rigor mortis advanced state of rigor mortis development, this treat- develops, ATP decreases and R-value increases. The ES ment produced a signiﬁcantly lower pH than the other treatment produced a greater R-value at 1 h postmortem treatments. than the Ar or controls at 1 h (Table 1), which indicated In both the AOI and IQF ﬁllets, the Ar treatment pro- an increased rate of postmortem metabolism, but not to duced signiﬁcantly lower shear values than the 1 h con- the extent of the Ar + ES treatment. The present study trols (Table 1). The present study followed the same agreed with other studies on postmortem R-values trends as those observed by Mohan Raj et al. (1991, 1992) changes with high voltage ES-treated broilers (Thompson and Mohan Raj and Gregory (1991), in which Ar with et al., 1987; Lyon et al., 1989; Sams et al., 1989; Walker residual O2 of < 2% produced ﬁllets deboned at 2 h post- et al., 1994). Although the Ar treatment alone did not mortem that were more tender than those from electri- accelerate ATP depletion, it seemed to enhance the rigor- cally stunned birds deboned at 2 h postmortem. The same accelerating effectiveness of the ES by signiﬁcantly in- trends were also observed in turkeys treated with Ar creasing the R-value for the Ar + ES treatment over the ES (Raj, 1994). High voltage ES has also been previously treatment alone. The Ar treatment produced signiﬁcantly demonstrated to reduce signiﬁcantly shear values in lower R-values compared with the ES and Ar + ES treat- broiler breast ﬁllets harvested at 1 h postmortem (Thomp- ments and was not signiﬁcantly different from the 1-h son et al., 1987; Sams et al., 1989). In the AOI ﬁllets, the controls, which indicated that the Ar treatment did not ES treatment produced signiﬁcantly lower shear values accelerate rigor mortis development as indicated by post- from the 1-h controls, but was not signiﬁcantly different mortem ATP depletion. This result differs from that of when compared with both of the Ar-containing treat- Mohan Raj et al. (1990c) who reported Ar killing acceler- ments. In the IQF ﬁllets, the shear value of the ES treat- ated postmortem metabolism and rigor mortis develop- ment was signiﬁcantly lower than that of the Ar ment as indicated by pH decline. This discrepancy may treatment, suggesting that the ES was more effective than be because the two studies used different parameters to Ar at reducing toughness. Although ES improved the estimate rigor mortis development. Because the R-value tenderizing effectiveness of the Ar treatment (as indicated for all 1-h treatments was signiﬁcantly lower than that of by a signiﬁcantly lower shear value for the Ar + ES treat- the 6-h control, rigor mortis development had not com- ment than the Ar treatment) for both the IQF and AOI pleted in the muscles of any of the 1-h treatments. ﬁllets, Ar provided no similar beneﬁt to the ES treatment As muscle cells develop rigor mortis, the concentration (no signiﬁcant difference between ES and Ar + ES treat- of lactic acid accumulates, and the pH decreases (Lawrie, ments). Because the ES improved the Ar but the Ar did 1991). The ES-containing treatments were not signiﬁ- not improve the ES, it may be inferred that the effects of cantly different from each other with respect to pH and the pulsing, regular, tonic contractions of the ES domi- produced lower pH values than the Ar treatment, which nated over the random, twitching convulsions from the was signiﬁcantly lower than the 1-h controls (Table 1). The Ar-induced anoxia. In both the AOI and IQF treatments, COMBINED METHODS OF ACCELERATING RIGOR MORTIS 1475 the 6-h controls produced signiﬁcantly lower shear values Fletcher, D. L., 1993. Stunning of broilers. Broiler Ind. 56:40–46. when compared with the other treatments. These lower Froning, G. W., and T. G. Uijttenboogaart, 1988. Effect of post- mortem electrical stimulation on color, texture, pH, and cook- values are due to the 6-h controls having a more advanced ing losses of hot and cold deboned chicken broiler breast state of rigor mortis development when deboned. Ac- meat. Poultry Sci. 67:1536–1544. cording to the tenderness threshold reported by Lyon Gregory, N. G., and L. J. Wilkins, 1993. Causes of downgrading. and Lyon (1990), the only treatment in the present study Broiler Ind. 56:42–45. that produced a “very tender” to “moderately tender” Hamm, D., 1981. Unconventional meat harvesting. Poultry Sci. 60(Suppl. 1):1666. cooked breast ﬁllet was the 6-h control from the AOI Jeacocke, R. E., 1977. Continuous measurements of the pH (hy- ﬁllets. The 6-h control from the IQF ﬁllets and the 1-h drogen ion concentration) of beef muscle in intact beef car- AOI ES and Ar + ES treatments produced cooked breast casses. J. Food Technol. 12:375–386. ﬁllets that would be classiﬁed as “slightly tender” ac- Khan, A. W., and A. R. Frey, 1971. A simple method for follow- cording to Lyon and Lyon (1990). ing rigor mortis development in beef and poultry meat. Can. Inst. Food Technol. J. 4:139–142. The L* value represents the lightness of the ﬁllet, and Kotula, A. W., E. E. Drewniak, and L. L. Davis, 1957. Effect of the a* value represents the redness of the ﬁllet. The ES carbon dioxide immobilization on the bleeding of chickens. and both Ar-containing treatments were not signiﬁcantly Poultry Sci. 36:585–589. different in 24-h L* values from the controls deboned at Lawrie, R., 1991. Pages 58–212 in: Meat Science, 5th ed. Pergam- 1 h postmortem (Table 1). Even though the ES L* value mon Press, Elmsford, NY. Li, Y., T. J. Siebenmorgen, and C. L. Grifﬁn, 1993. Electrical was signiﬁcantly lower than that for the 6-h control (indi- stimulation in poultry: A review and evaluation. Poultry Sci. cating darker meat), it cannot be inferred to be solely an 72:7–22. effect of the ES because the ﬁllets were also deboned at Locker, R. H., 1985. Cold-induced toughness of meat. Pages different postmortem times. The results of the present 1–44 in: Advances in Meat Research, Volume 1, Electrical study are consistent with those of Maki and Froning Stimulation. A. M. Pearson and T. R. Dutson, ed. West- port, CT. (1987) and Froning and Uijttenboogaart (1988), that ES Lyon, C. E., C. E. Davis, J. A. Dickens, C. M. Papa, and J. O. signiﬁcantly decreased the L* value and increased the a* Reagan, 1989. Effects of electrical stimulation on the post- value. The Ar + ES treatment produced the highest a* mortem biochemical changes and texture of broiler pectoralis value, indicating a redder ﬁllet when compared with the muscle. Poultry Sci. 68:249–257. Ar and the 1-h controls. The ES treatment was not signiﬁ- Lyon, C. E., and B. G. Lyon, 1990. The relationship of objective shear values and sensory tests to changes in tenderness of cantly different from the Ar treatment but produced a broiler breast meat. Poultry Sci. 69:1420–1427. signiﬁcantly higher a* value compared with the 1-h Maki, A., and G. W. Froning, 1987. Effect of post-mortem electri- controls. cal stimulation on quality of turkey meat. Poultry Sci. The trends in the present study for L* values for the 66:1155–1157. Ar-containing treatments did not agree with the results Mohan Raj, A. M., and N. G. Gregory, 1991. Effect of argon stunning, rapid chilling and early ﬁlleting on texture of of Mohan Raj et al. (1990c) who reported that L* values broiler breast meat. Br. Poult. Sci. 32:741–746. for Ar-treated broilers were signiﬁcantly lower than the Mohan Raj, A. M., N. G. Gregory, and S. D. Austin, 1990a. CO2 treatment and the controls. However, those authors Investigation into the batch stunning/killing of chickens us- also reported that Ar-treated broilers produced the high- ing carbon dioxide or argon-induced hypoxia. Res. Vet. Sci. est a* value when compared with the electrically stunned 49:364–366. controls. This result was consistent with the a* values of Mohan Raj, A. M., N. G. Gregory, and S. D. Austin, 1990b. Prevalence of broken bones in broilers killed by different the present study. Despite the statistical signiﬁcance of the stunning methods. Vet. Rec. 127:285–287. color mean differences, the magnitude of the differences Mohan Raj, A. M., T. C. Grey, A. R. Audsely, and N. G. Gregory, makes questionable their perception by consumers and, 1990c. Effect of electrical and gaseous stunning on the carcass therefore, their utility. Small differences in breast ﬁllet and meat quality of broilers. Br. Poult. Sci. 31:725–773. color may not be perceived by the consumer. However, Mohan Raj, A. M., T. C. Grey, and N. G. Gregory, 1991. Effect of early ﬁlleting on the texture of breast muscle of broilers consumers may be able to see color differences in ﬁllets stunned with argon-induced anoxia. Br. Poult. Sci. 32:319– that are not uniform in color where they are packaged to- 325. gether. Mohan Raj, A. B., and G. R. Nute, 1995. Effect of stunning In conclusion, these results indicate that ES is generally method and ﬁlleting time on sensory proﬁle of turkey breast more effective than Ar at accelerating rigor mortis devel- meat. Br. Poult. Sci. 36:221–227. Mohan Raj, A. M., G. R. Nute, S. B. Wotton, and A. Baker, 1992. opment. Also, although Ar produced some indication that Sensory evaluation of breast ﬁllets from argon-stunned and it enhanced the effectiveness of the ES treatment in accel- electrically-stimulated broiler carcasses processed under erating postmortem metabolism, this enhanced effect did commercial conditions. Br. Poult. Sci. 33:963–971. not manifest itself as a reduction in shear value. This Poole, G. H., and D. L. Fletcher, 1995. A comparison of argon, ﬁnding suggests that there is little tenderness advantage carbon dioxide, and nitrogen in a broiler killing system. Poul- try Sci. 74:1218–1223. in combining killing by Ar and postmortem ES. Raj, A.B.M., 1994. 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