Meat Quality and Rigor Mortis Development in Broiler Chickens with

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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.
    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 =
    To whom correspondence should be addressed: asams@poultry.            adenosine triphosphate; ES = electrical stimulation; IQF = individually                                                                  quick frozen; R-value = ratio of inosine to adenosine.

                                 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
                                                                   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
   Model OXOR II, Barcarach, Pittsburgh, PA 15238.                 of the muscle at a point under the feather tract away from
   Model SP-30-SS, Brower, Houghton, IA 52631.                     apparent lightening caused by scalding.
   Traceable digital thermometer, Control Company, Friendswood,      The data in this completely randomized design were
TX 77546.
   Model 1011, Instron Corp., Canton, MA 02021.                    subjected to ANOVA using treatment system (1-h control,
   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
              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).
                 At deboning time.
                 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. Effect of stunning method, carcase chilling
                                                                          temperature and filleting time on the texture of turkey breast
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