Effect of Stunning Current Frequency on Carcass Downgrading
and Meat Quality of Turkey1
V. Sante,*,†,2 G. Le Pottier,† T. Astruc,* M. Mouchoniere,† and X. Fernandez*
*INRA, Meat Research Centre, F-63122 Saint Genes Champanelle, France, and †CIDEF F-35310 Mordelles, France
ABSTRACT The objective of this study was to determine the effect of frequency of a 150 mA water-bath stunning current on turkey hen carcass and meat qualities.
Fifty turkey hens were subjected to water-bath stunning
with alternating current of various frequencies: 50 Hz (n
= 12), 300 Hz (n = 14), 480 Hz (n = 12), and 600 Hz (n =
12); the duration of stunning was 4 s for each bird. Carcass
defects such as engorged wing veins, red wing tips, and
hemorrhages were recorded. Turkey meat quality traits
(M. Pectoralis major) were assessed based on rigor mortis
development, color, drip loss, cooking loss, tenderness,
and cooking yield of cured products. The data showed
that frequencies of 480 Hz and 600 Hz are associated
with an increased rate of postmortem pH decline (during
bleeding). This effect is most likely due to the occurrence
of vigorous wing flapping during the first 3 min poststunning. Under the experimental conditions of the present
work, the increase in rate of pH decline after stunning at
480 and 600 Hz did not induce carcass and meat quality
defects. However, before any recommendation is given,
the influence of stunning frequency on turkey meat quality needs to be evaluated under industrial conditions.
(Key words: electrical stunning, current frequency, carcass defects, rigor mortis development, meat quality)
2000 Poultry Science 79:1208–1214
INTRODUCTION
The main concerns of the French turkey processing
companies associated with electrical stunning are animal welfare and a possibility of carcass downgrading
and inferior meat quality. In France, all turkey processing plants use water-bath electrical stunning systems. A recent survey of five French processors showed
that electrical stunning conditions were not standardized in terms of intensity, waveform, or frequency
(Santé et al., 1996).
Although the intensity of turkey stunning was recommended to be 150 mA (Gregory and Wilkins, 1989), the
effect of other electrical parameters such as waveform
and frequency have not been elucidated. Recently, Mouchoniere et al. (1999) studied the effect of current frequency on physical recovery of turkeys after stunning.
Their data suggested that the duration of unconsciousness was reduced as the frequency of stunning increased
from 50 to 600 Hz.
It was also reported that the intensity of 150 mA reduces the incidence of convulsions and hemorrhages
Received for publication August 30, 1999.
Accepted for publication March 22, 2000.
1
This study is part of a project financed by Comité Interprofessionnel
de la Dinde Française (CIDEF, Mordelles 35310), Office Interprofessionnel de la Viande et de l’Aviculture (OFIVAL, Paris 75012) and
Institut National de la Recherche Agronomique (INRA, Paris 75007).
2
To whom correspondence should be addressed: vero@clermont.
inra.fr.
in birds (Gregory and Wilkins, 1989). Such intensity
combined with a frequency of 50 Hz is the frequency
delivered by most of stunners used in France. This
method often causes cardiac arrest and killing of the
birds, which, in turn, often results in significant reduction of bleeding efficiency (Mouchonière et al., 1999).
The incidence of cardiac arrest is reduced by increasing
the frequency of the stunning current (Wilkins et al.,
1998; Mouchonière et al., 1999). On the other hand, the
efficiency and duration of stunning-induced unconsciousness decreased with the electrical current of 150
mA to 600 Hz (Mouchonière et al., 1999, and unpublished data preparation). If such a system is utilized,
the occurrence of wing flapping may increase when
compared with a 50-Hz stunning system. This increase
could have a detrimental effect on meat quality because
an intense wing flapping early postmortem may result
in an accelerated rate of pH decline while the carcass
temperature is higher than 41 to 42 C, thus leading
to protein denaturation and a pale, soft, exudative-like
condition (Sante et al., 1995).
This study was carried out to evaluate the effect of
various current frequencies during water-bath stunning
on the incidence of turkey hen carcass defects, such as
engorged veins, red wing tips, and meat quality such
as color, drip loss, tenderness, cooking loss and cooking
yield of the cured product.
Abbreviation Key: ATP = adenosine 5′-triphosphate; CrP = creatine phosphate.
1208
TURKEY STUNNING AND MEAT QUALITIES
MATERIALS AND METHODS
Animal and Stunning Procedure
Fifty turkey hens (12-wk-old, 6 to 8 kg live weight)
from the BUT 9 line were individually subjected to water-bath stunning with an alternating current of various
frequencies: 50 Hz (n = 12), 300 Hz (n = 14), 480 Hz (n
= 12), and 600 Hz (n = 12). The birds were processed
during 5 experimental days. The order of frequency
treatment was changed every day. After an overnight
feed withdrawal, turkeys were individually shackled,
the head and the upper neck were plunged into a waterbath, and an isolated constant current (150 mA)3 was
applied for 4 s between the water and the shackle. Unilateral neck cutting was manually performed 10 s after
the end of the stun, and bleeding lasted for 3 min. Carcasses were cooled 20 min after slaughter in a cold room
at 2 C for 24 h. Breast muscle was harvested from the
carcass at 24 h postmortem.
Carcass Defects
At 24 h postmortem, the following carcass gross-appearance defects were recorded: engorged wing veins,
hemorrhagic wing veins, red wingtips, and hemorrhage
in shoulders and elbows. Each defect was scored on a
subjective three-point scale: 0 = absence of the defect,
0.5 = mild presence of the defect, and 1 = strong presence
of the defect.
Meat Quality
Measurements of pH and Temperature. A 2-g sample was taken from the left breast muscle and homogenized in 18 mL of 5 mM iodoacetate buffer at different
times (3 min, 20 min, 1 h, 2 h, 5 h, and 24 h) postmortem.
The pH of the homogenate was measured 10 min after
sampling with a portable pH meter combined with a
glass electrode.4 Temperature of the breast muscle was
also monitored at the time of sample collection.
Determination of Glycogen and Lactate. To obtain
reference values for resting glycogen levels in M. Pectoralis major or superficialis, samples were taken from
five birds randomly chosen from each frequency group
(20 birds total). The samples were taken immediately
before stunning while the birds were shackled (1 to 2 s
before electrical stunning). These samples (about 1 g)
were collected using a shot biopsy device5 according to
the procedure described by Talmant et al. (1989). Two
3
The constant current stunner used in the present study was designed
and provided by the Silsoe Research Institute, Silsoe, Bedford, MK45
4HS England.
4
Schott Gerate, CG822, Bioblock, 67403 Illkirch, France.
5
Shot Biopsy Device (Talmant et al., 1989).
6
Gilson Medical Electronics, 95400 Villiers-le-Bel, France.
7
Microsorb, Rainin Instruments Co., Walnut Creek, CA 94598.
8
Aldrich Chemical Co., 38297 Saint Quentin Fallavier, France.
9
Chromameter-CR300, Minolta, 78420 Guyancourt, France.
1209
grams of left breast muscle were excised at 3 min, 20
min, 1 h, 2 h, 5 h, and 24 h postmortem. Muscle samples
were frozen in liquid nitrogen and freeze-dried prior
to analysis. About 200 mg freeze-dried muscle tissue
was homogenized in 10 mL 0.5 M perchloric acid. Glycogen, glucose, and glucose-6-phosphate were simultaneously determined from the homogenate, according to
Dalrymple and Hamm (1973), after hydrolysis of glycogen with amyloglucosidase. Lactate was determined in
the supernatant resulting from the centrifugation of the
homogenate (20 min at 2,500 g), according to Bergmeyer
(1974). Concentrations were expressed as micromoles
per gram tissue, assuming a moisture content of 75%.
Phosphorylated Compounds. Muscle perchloric
acid extracts, adjusted to pH 7.5 with 2.5 M KCO3, were
used for HPLC determination of adenosine 5′-triphosphate (ATP) and related compounds. Separation and
quantification of creatine phosphate (CrP), ATP, adenosine 5′-monophosphate, inosine 5′-monophosphate, and
creatine were carried out with an HPLC system6 comprising a type-117 dual-wavelength detector and type306 pumps. Samples were injected automatically by using a type-231 injector and were diluted 10 times with
eluent just before injection with a type-401 dilutor. Metabolites were detected at 212 nm and 254 nm. Chromatograms were processed and calculated using a Gilson
715 HPLC-system controller.6 Elution was carried out
under isocratic conditions by using ion-pair liquid chromatography and a reverse-phase C18 column7 guarded
with a C18 precolumn (Microsorb, 4.6 × 15 mm, 5 µm
ODS7), with a flow rate of 1 ml/min. The eluent was
100 mM potassium dihydrogenphosphate (pH = 6.4)
with 0.05% tetrabutyl ammonium hydroxide8 as the ion
pair agent and 3% acetonitrile.
Drip Loss
Right breast muscle was harvested at 24 h postmortem
and sliced in 1.5-cm depth scallops. For each bird, two
scallops were weighed at 24 h, placed in a tray, wrapped
in an oxygen permeable film, and kept for 3 d at +2 C.
The scallops were then weighed, and the drip loss was
expressed as the percentage of initial weight.
Color
Color was measured on the same scallops as those
used for drip determination. Trichromatic coordinates
(L*, a*, b*) were measured at 24 h and 96 h using a
Minolta chromameter CR 300.9
Cooking Loss
For each breast muscle sample, two scallops were
vacuum-packed in polyethylene bags and cooked in a
water bath at 85 C for 15 min (end point temperature
of 75 C). Samples were weighed before cooking, cooked,
drained, and reweighed. Cooking loss was expressed
as the percentage of weight before cooking.
1210
SANTE ET AL.
TABLE 1. Influence of stunning frequency (150 mA, 4 s) on hemorrhage scores in elbow
and shoulders and on engorged wing veins score1
Engorged wing vein
score
Hemorrhage score
Elbow
50
300
480
600
Hz
Hz
Hz
Hz
Shoulder
Right
Left
Right
Left
Right
Left
0
0
0
0.1
0.1
0.1
0
0.2
0
0.1
0.3
0
0
0
0
0
0.4
0.3
0.3
0.3
0.4
0.4
0.2
0.2
1
Each defect was scored on a subjective three-point scale: 0 = absence of the defect, 0.5 = mild presence of
the defect, and 1 = strong presence of the defect.
Tenderness
After cooking, the scallops were cut into pieces (3 ×
1 × 1 cm) parallel to the fiber axis. Rheological measurements of myofibrillar strength were performed at room
temperature using an Instron,10 according to Lepetit et
al. (1986). Samples were compressed perpendicular to
the fiber axis in a cell equipped with lateral walls so
that free deformations of the samples were maintained
parallel to the fiber axis. Cooked meat samples were
compressed at a rate of 50 mmⴢmin−1, up to a compression ratio of 0.20. The maximum stresses (σ) reached at
0.20 and the strain were determined from the stressstrain curves and were expressed as Nⴢcm−2.
Cooking Yield of Cured Product
In France, processing of poultry meat by curing and
cooking is increasing. In order to evaluate the ability of
the meat to be processed by curing or cooking, the Napole yield (Naveau et al., 1985) was determined. One
hundred gram samples of trimmed breast muscle were
cut into cube pieces of 1 cm per side and were placed
in a beaker. Twenty grams of 136 g/L nitrited salt was
added according to Naveau et al. (1985). The cured meat
was covered with a 200-g steel weight and cooked for
10 min in boiling water. Dripping was allowed for 2.5
h, and the yield was calculated as the weight of cured
cooked meat divided by 100 (expressed as %).
Statistical Analysis
Analyses of variance were performed using the GLM
procedure of SAS威 (SAS Institute, 1989), to test the influence of current frequency on various meat quality
attributes. The model included the effects of biopsy sampling, day, and frequency. When a significant effect of
frequency was noted (P < 0.05), means were compared
using Duncan’s multiple-range test.
Nonparametric ANOVA of carcass defects data was
carried out using the NPAR1WAY procedure of SAS,威
10
Instron, 78284, Guyancourt, France.
and the Wilcoxon scores were recorded. Because there
were no significant trial by treatment interactions, the
data from the six trials were pooled for analysis and presentation.
RESULTS AND DISCUSSION
Effect of Biopsy Sampling
To our knowledge, our experiment was the first to
use the shot biopsy device on turkeys. The sampling
was performed 1 to 2 s before electrical stunning in
order to minimize the likely influences on muscle physiology and postmortem metabolism. Under such conditions, it is unlikely that this procedure had any relevant
welfare implication. Because it was not known whether
the sampling procedure would affect the rate of postmortem metabolism, only 20 birds (five per frequency
treatment) were sampled. The biopsy sampling enhanced the rate of postmortem ATP, CrP and glycogen
breakdown, and lactate accumulation; however, this effect was not significant for every sampling time (Figure
1). In addition, the pH of breast muscle at 5 h postmortem was lowered 0.15 pH unit, and the cooking yield
of cured product was 4 points less in biopsied birds.
None of the other traits under study were significantly
affected by the biopsy procedure.
Carcass Appearance
The effect of slaughter on carcass quality is of prime
importance to the processor. Aside from bruising, the
main causes of downgrading (red skin, blood spots,
blood splash, red wingtips, and ruptured blood vessels
in breast muscle) are associated with poor stunning or
bleeding conditions. The present study revealed that
the incidence and severity of carcass defects were not
influenced by the stunning frequency. Neither hemorrhage in shoulder or elbow nor red wing tips were observed. The main carcass defect noted was the presence
of some engorged veins at the current frequency of 50 or
300 Hz (Table 1). However, the effect was not significant.
The low incidence of carcass defects could be explained, to a large extent, because our experiment was
carried out under laboratory conditions. Indeed, the
TURKEY STUNNING AND MEAT QUALITIES
1211
FIGURE 1. Effect of biopsy sampling on postmortem evolution of glycogen, lactate, ATP and creatine phosphate in turkey Pectoralis muscle
(vertical bars show the SEM). a) At 3 min postmortem, glycogen concentrations differed significantly (P < 0.05) in breast muscle between biopsied
and nonbiopsied birds. b) At 5 h postmortem, lactate concentrations differed significantly (P < 0.05) in breast muscle between biopsied and
nonbiopsied birds. c) At 30 min postmortem, ATP concentrations differed significantly (P < 0.05) in breast muscle between biopsied and nonbiopsied
birds. d) At 30 min, 2 and 5 h postmortem, creatine phosphate concentrations differed significantly (P < 0.05) in breast muscle between biopsied
and nonbiopsied birds.
birds were gently handled compared with commercial
conditions. Therefore, any knock-out effect of wing
flapping between birds was avoided. Previous research
has shown that wing flapping prior to electrical stunning can influence the prevalence of such carcass defects
as red wingtips (Gregory et al., 1989). Recently, Hillebrand et al. (1996), studying different stunning methods
in broiler chicken (electrical whole body and head only
stunning), suggested that the variation in the level of
hemorrhages between trials could be partly explained
by different physiological conditions of birds at slaughter induced by housing, climate, catching, and transportation.
Meat Quality
The pH decline according to stunning frequency is
shown on Figure 2. During the first 3 min, the rate of
pH decline was higher after stunning at 480 and 600
Hz, compared with 50 Hz and 300 Hz. Two patterns of
pH decline were observed: a slow pH decline group
FIGURE 2. Effect of stunning frequency (50, 300, 480, and 600 Hz)
on postmortem pH in turkey breast muscle (vertical bars show the SEM).
1212
SANTE ET AL.
TABLE 2. Mean (± SEM) of in vivo glycogen and lactate
concentrations (µmol/g fresh muscle) in turkey breast muscle1
Glycogen
Lactate
50 Hz
300 Hz
480 Hz
600 Hz
49.1 ± 4.8
9.2 ± 1.2
54.1 ± 2.5
6.8 ± 1.0
54.4 ± 2.7
7.2 ± 1.0
54.4 ± 2.6
7.8 ± 2.8
1
The four treatment groups did not show significant variation in
prestunning glycogen and lactate concentrations.
after stunning at 50 and 300 Hz and a fast pH decline
group after stunning at 480 and 600 Hz. After 5 h postmortem the differences in pH were no longer statistically significant. One hour postmortem, the temperature
was 34 to 35 C in all carcasses, regardless of the stunning frequency.
Prestunning glycogen levels of Pectoralis muscle
were, on average, 53 µmol/g and did not differ among
the four treatment groups (Table 2). The average
prestunning concentration of glycogen was used as a
reference point for a rough calculation of the relative
variation in glycogen level postmortem. After bleeding,
the glycogen stores were reduced to 40 to 50% (480 and
600 Hz) and to 15 to 25% (50 to 300 Hz), compared with
the average prestunning value (Figure 3). At the same
time, lactate accumulation in the breast muscle was
nearly 70 and 50 µmoles, respectively (Figure 4).
The ATP levels at 3 min postmortem were significantly lower after 480 and 600 Hz stunning than after
50 and 300 Hz stunning (Figure 5). At 20 min, the rate
of ATP decline was not affected by stunning frequency.
Similar results were observed for creatine phosphate
levels; they were significantly higher after 50 Hz than
after 480 to 600 Hz stunning, with the levels recorded
after 300 Hz stunning being intermediate. The rapid
postmortem depletion of CrP after 480 and 600 Hz is
FIGURE 3. Effect of stunning frequency (50, 300, 480, and 600 Hz)
on postmortem glycogen level in turkey breast muscle (vertical bars
show the SEM). From 3 min to 5 h postmortem, glycogen concentrations
differed significantly (P < 0.05) between 50 to 300 Hz and 480 to 600
Hz stunning frequencies.
most likely due to the mobilization of this energy source
for muscular contraction associated with wing flapping.
The greater pH decline and glycogen depletion, occurring during the first 3 min after stunning at 480 and
600 Hz, is most likely due to struggle and wing flapping
during bleeding. Indeed, Mouchonière et al. (1999), using the same experimental conditions, showed that the
incidence of cardiac arrest at stunning was 100 and 60%
after 50 and 300 Hz, respectively. After stunning at 480
and 600 Hz, however, cardiac arrests were not observed,
and most birds exhibited wing flapping during bleeding. These results are consistent with the findings reported by Northcutt et al. (1998), who compared electrical stunning with no stunning. A significantly lower pH
value was found when the birds were not immobilized
by stunning before neck cutting. Differences in initial
pH values for broiler were shown by Craig and Fletcher
(1997), who compared a high current stunning to a low
voltage stunning. In the first treatment, the intensity
delivered (125 mA) combined to a frequency of 50 Hz
was associated with efficient stunning. Consequently,
the initial pH was higher than for the low voltage stunning. Increased stunning current intensity or voltage
gave similar results (Ali et al., 1995), providing that the
current intensity (or voltage) induced unconsciousness.
Trichromatic coordinates were not affected by stunning frequency (Table 3). A higher a*/b* ratio was found
for the 480 Hz group, but no clear relationship between
a/b and stunning frequency could be concluded. Stunning frequency did not affect the time-related changes
in color during the 4 d following slaughter. These results
are consistent with the results of Northcutt et al. (1998),
who reported no significant difference in turkey meat
color associated with the stunning methods. Several researchers have also reported color changes in turkey
FIGURE 4. Effect of stunning frequency (50, 300, 480, and 600 Hz)
on postmortem lactate in turkey breast muscle (vertical bars shown the
SEM). From 3 min to 5 h postmortem, lactate concentrations differed
significantly (P < 0.05) between 50 to 300 Hz and 480 to 600 Hz stunning frequencies.
1213
TURKEY STUNNING AND MEAT QUALITIES
TABLE 3. Influence of stunning frequency (150 mA, 4 s) on meat quality attributes (m ± SEM)
Stunning current frequencies
50 Hz
Lightness L* 24 h
Redness a* 24 h
Yellowness b* 24 h
Ratio a*/b* 24 h
Lightness L* 96 h
Redness a* 96 h
Yellowness b* 96 h
Ratio a*/b* 96 h
Drip loss (%)
Cook loss (%)
Cooking yield of
cured product (%)
Myofibrillar strength
N/cm2
51.4
5.4
2.7
2.1
51.4
4.7
5.7
0.8
1.25
21.2
±
±
±
±
±
±
±
±
±
±
300 Hz
0.4
0.2
0.2
0.2b
0.3
0.3bc
0.3
0.03b
0.1
0.4c
52.2
4.5
2.5
2.0
52.0
4.3
5.5
0.8
1.3
21.7
±
±
±
±
±
±
±
±
±
±
480 Hz
0.6
0.3
0.3
0.2b
0.5
0.4c
0.2
0.07b
0.1
0.4bc
51.8
5.3
2.1
2.9
51.4
5.6
5.4
1.0
1.2
23.4
±
±
±
±
±
±
±
±
±
±
600 Hz
0.6
0.2
0.2
0.4a
0.5
0.2a
0.2
0.05a
0.1
0.6a
53.0
5.1
2.5
2.2
52.4
5.4
5.7
1.0
1.1
23.1
±
±
±
±
±
±
±
±
±
±
0.9
0.3
0.3
0.2ab
0.7
0.2ab
0.2
0.05a
0.1
0.6ab
96.2 ± 0.1
94.6 ± 1.2
95.7 ± 1.1
96.3 ± 1.6
26.0 ± 0.6
24.3 ± 0.5
25.8 ± 0.8
25.5 ± 0.4
Means within a row without a common superscript differ significantly (P < 0.05).
a–c
FIGURE 5. Effect of stunning frequency (50, 300, 480, and 600 Hz) on postmortem creatine phosphate (a), ATP (b), IMP (c), and creatine (d) in
turkey breast muscle (vertical bars show the SEM). a) From 3 min to 1 h postmortem, creatine phosphate concentrations differed significantly (P
< 0.05) between stunning frequencies of 50 Hz and 300 to 480 to 600 Hz. b) From 3 min to 5 h postmortem, ATP concentrations differed significantly
(P < 0.05) between stunning frequencies of 50 to 300 Hz and 480 to 600 Hz. c) From 3 min to 1 h postmortem, IMP concentrations differed
significantly (P < 0.05) between stunning frequencies of 50 to 300 Hz and 480 to 600 Hz.
1214
SANTE ET AL.
breast meat that underwent an accelerated rate of postmortem glycolysis (Froning et al., 1978; McKee and
Sams, 1997; Pietrzak et al., 1997; Sosnicki et al., 1998).
In our study, the differences in the rate of postmortem
pH decline between the stunning treatments were not
large enough to induce significant changes in color.
Meat quality attributes are presented in Table 3. Significant differences between treatments were found for
the a*/b* ratio at 24 h postmortem and redness (a*) at
96 h postmortem, but there were no clear relationships
between those items and stunning frequency. In contrast, cook losses were higher for the 480 and 600 Hz
stunning frequencies, which is consistent with the early
pH values being lower for these two treatments. At 96
h postmortem, the a*/b* ratio was higher for the 480
and 600 Hz stunning frequencies. This effect is difficult
to explain. Indeed, the a*/b* ratio and pH are usually
positively correlated (Santé et al., 1996). In that case,
the a*/b* ratio was higher in the birds showing the
lower pH values.
Our study showed that stunning frequency affects the
early rate of postmortem pH decline during bleeding
(the initial pH within the first 3 min), and this effect is
most likely due to wing flapping during this period.
Under the conditions of the present work, the increase
in rate of pH decline after stunning at 480 and 600 Hz
was not sufficient to cause considerable carcass and
meat quality defects. However, the chilling conditions
were efficient because muscle temperature was lowered
to 35 C within 1 h postmortem compared with some
slaughter plants where the same temperature is reached
at 2 h postmortem (unpublished results). This rapid
cooling probably contributed to the reduction of possible negative effects of the rapid postmortem pH decline.
The influence of stunning frequency on turkey meat
quality needs to be evaluated under industrial conditions before any recommendation is given.
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