Meat Quality of Broiler Chickens Processed Using Electrical and Controlled Atmosphere Stunning Systems

Broiler Chicken Meat Quality: Electrical vs. Controlled Atmosphere Stunning

Abstract

Consumer concerns about animal welfare have led to the exploration of controlled atmosphere stunning (CAS) as an alternative to electrical stunning (ES) in poultry processing.
The study evaluates the impact of commercially applied CAS and ES on broiler meat quality, using current U.S. parameters.
Three trials were conducted in a commercial broiler processing facility with separate processing lines for ES and CAS.
Measurements included blood glucose concentrations, visible wing damage, breast fillet pH, color, and drip loss.
Blood glucose was higher post-stunning in CAS birds compared to ES birds (P < 0.0001).
CAS carcasses had more visible wing damage (P < 0.0001).
Breast fillet pH was lower, L* (lightness) was higher, and a* (redness) was lower at deboning for CAS fillets (P < 0.0001, P = 0.0005, P = 0.0303).
Drip loss did not differ significantly between CAS and ES fillets (P = 0.0859).
Increased wing damage in CAS carcasses suggests a need for equipment adjustments.
Differences in breast fillet attributes at deboning were minimal and not present at 24 hours.

Introduction

Broiler meat consumption in the U.S. increased by 13.9% from 2011 to 2020 (USDA, 2021).
Broiler production in the U.S. increased by 20% during the same period (USDA, 2021).
Consumer preference for humanely raised animal products is increasing (Alonso et al., 2020).
Stunning is a common practice to render broilers unconscious before slaughter (Berg and Raj, 2015).
Electrical water-bath stunning (ES) is the most common method in the U.S. (approximately 95% of commercial broiler production).
Research indicates distress for birds during ES (Boyd, 1994; Erasmus et al., 2010).
Shackling and live handling can increase stress responses in birds (Kannan et al., 1997; Bedanova et al., 2007).
Pre-stun shock, caused by premature contact with the ionized water-bath, is a concern with ES.
Smaller broilers may miss the electrical water bath, leading to conscious neck cuts (Heath et al., 1981).
ES under U.S. parameters (low voltage-high frequency, 12−38 V, >400 Hz) may allow recovery of consciousness if the neck cut is not completed promptly (Gibson et al., 2016).
U.S. ES has less impact on meat quality compared to CAS (Kang and Sams, 1999).
CAS is gaining popularity due to perceived animal welfare benefits and potential improvements in meat quality.
In Europe, ES parameters are legally enforced with higher current and voltage, which can negatively impact meat quality due to muscle hemorrhaging (Sirri et al., 2017).
CAS uses a gradual, multiphasic change in atmosphere, often with increasing carbon dioxide concentrations.
CAS is considered advantageous for animal welfare due to reduced human-to-bird contact and no live shackling.
Exposure to carbon dioxide during CAS can cause adverse physical reactions for 60 to 90 seconds (McKeegan et al. 2006).
CAS systems can cost upwards of $1.5 million USD for initial capital costs (FCEC, 2012).
Physical response to stressors impacts poultry meat quality, resulting in metabolic changes in the muscle (Santonicola et al., 2017).
Some studies show improved meat quality with CAS, including less carcass damage and rapid initial pH decline (Raj et al., 1990; Raj et al., 1997).
Other studies have found less carcass damage with ES under U.S. parameters compared to CAS (Kang and Sams, 1999).
Rapid initial pH decline in CAS-stunned broilers has been associated with pale, soft, exudative (PSE) meat (Solomon et al., 1998).
Variations in gas concentrations (Xu et al., 2011) and equipment parameters can lead to conflicting results.
Limited research exists comparing meat quality of broiler breast fillets using U.S. ES or CAS as commercially applied.
This study investigates the effect of ES or CAS on meat quality by evaluating changes in circulating glucose concentrations, visible wing damage, and breast fillet pH, color, and drip loss.

Materials and Methods

The experiment was conducted at a commercial processing plant in the Southeast U.S. using small birds (approximately 2.04 kg live weight).
Three separate trials were performed on different days in May, July, and October, using different flocks.
For Trials 1 and 3, different flocks were used for ES and CAS treatments. For Trial 2, the same flock was used for both stunning types.
All birds were of the same genetic line, but age may have differed slightly.
Birds were held in lairage outdoors under covered pole barns with fans and misters.
Ambient temperatures ranged from 19°C to 27°C in Trial 1, 26°C to 32°C in Trial 2, and 14°C to 21°C in Trial 3.
Birds were assigned to ES or CAS treatments on separate operational lines.
For ES, birds were removed from transport crates, shackled, electrically stunned at 20 mA/bird for 12 seconds, mechanically neck cut, bled for 90 seconds, hard scalded at 54°C for 180 seconds, then defeathered for 210 seconds.
For CAS, birds were stunned in transport crates by exposure to increasing CO2 concentrations within 5 phases from 20% to 85% over 5 minutes, with O2 added to achieve 21% during the first 90 seconds.
Following CAS, carcasses were shackled, mechanically neck cut, bled for 90 seconds, hard scalded at 54°C for 180 seconds, then defeathered for 210 seconds.
Following defeathering, carcasses continued through evisceration, immersion chilling, and deboning for both treatments.

Glucose Concentrations

Circulating blood glucose concentrations were evaluated at lairage, immediately pre-stunning (Trial 3 only), and post-stunning.
Pre-stunning was evaluated in Trial 3 due to tipping and shackling prior to ES.
At lairage, 30, 30, and 15 blood samples per stunning method were collected for Trials 1, 2, and 3, respectively.
Immediately pre-stunning in Trial 3, 30 blood samples per stunning method were collected.
Post-stunning, 30 blood samples per stunning method were collected for all trials.
At lairage, broilers were cervically dislocated, decapitated, and blood samples were collected.
For ES pre-stunning, broilers were removed from the shackle line before the electrical waterbath.
For CAS pre-stunning, broilers were removed from their transportation tray prior to gas exposure.
For ES post-stunning, broilers were removed from shackles after mechanical neck-cutting and blood was collected.
For CAS post-stunning, carcasses were cervically dislocated, then decapitated for blood collection.
Glucose concentrations (mg/dL) were evaluated with a handheld EvencarePro glucose reader.

Visible Wing Damage

Carcasses were evaluated for visible wing damage on the shackle line after defeathering.
Wing damage was defined as any visible damage, including dislocation, broken bones, or skin tearing.
A single investigator counted damaged wings using a handheld tally counter over 5 minutes of operation.
A second investigator counted empty shackles within the same 5 minutes.
Total numbers of shackles observed was calculated based on a line speed of 150 birds per minute for ES and 175 birds per minute for CAS.
Each stunning line was evaluated for 13 repetitions of 5 minutes each, totaling 65 minutes.
A total of 18,222 wings were evaluated for the ES line and 22,312 for the CAS line.

Meat Quality Attributes

For each of 3 trials, 30 breast butterflies were removed from each processing line at deboning (n = 30 butterflies per treatment per trial, N = 180).
The right fillet was evaluated for pH with a piercing probe.
The left fillet was weighed (g) and color was measured in triplicate for Lab* values at debone (Konica Minolta Chroma Meter CR-400).
The left fillet was sealed in a ziptop bag and placed on ice for subsequent evaluation.
Fillet pH, color, and drip loss were subsequently evaluated at 24 hours post-deboning.
Drip loss percentage was determined by subtracting the weight of the fillet 24 hours post-debone from the initial weight of the fillet at debone, then multiplying by 100.

Statistical Analysis

A completely randomized design with 2 treatments (ES or CAS) was used.
Glucose data were analyzed using the General Linear Model (GLM) procedure with treatment and sample time as main effects.
For meat quality analysis, the main effect of treatment was evaluated at deboning and 24 hours post-deboning for pH, color (CIE Lab*), and drip loss data by 1-way ANOVA.
Means were separated by Tukey’s HSD with significance determined as P ≤ 0.05.
Visible wing damage data were analyzed using Chi-Square.
All analyses were conducted using the SAS OnDemand for Academics software.

Results and Discussion

Glucose Concentrations

Glucose concentrations differed by trial and treatment.
Trial 1 had significantly higher overall mean glucose concentrations (343 mg/dL) than Trials 2 and 3 (298 and 284 mg/dL, respectively).
Differences in baseline blood glucose concentrations between trials were expected due to different flocks and times of the year.
Broiler management, transport, and feed withdrawal times were similar, but variations in grower management styles, distance to the processing plant, and length of feed withdrawal could impact glucose levels.
No significant differences in circulating glucose concentrations at lairage (272 and 284 mg/dL, respectively; P = 0.2646) or immediately pre-stunning (283 and 274 mg/dL, respectively; P = 0.6425) between ES and CAS treatments.
Blood glucose concentrations post-stunning were significantly higher (P < 0.0001) in broilers following CAS (418 mg/dL) compared to ES broilers (259 mg/dL).
No significant differences in blood glucose between sample locations for ES. Blood glucose concentration significantly increased from 274 to 418 mg/dL following stunning for CAS broilers (P < 0.0001).
Blood glucose increased during the CAS process.
Pinto et al. (2016) found higher glucose in broilers following ES compared to CAS, possibly due to the use of high voltage / low frequency parameters (220 V AC, 60 Hz) in their ES.
Xu et al. (2018) found no significant difference in blood glucose when comparing common mixtures of CO2, O2, and N2, possibly due to differences in the CAS method.
The current study used a commercial, 5-phase atmosphere stunner under production conditions, while previous work used a non-commercial chamber.
All 3 trials, whether the same flock was utilized or not, had significantly higher blood glucose concentrations in broilers stunned by CAS at the post-stunning location in comparison to ES broilers and also a significant increase when comparing lairage and pre-stun with post-stun on the CAS line.
Limited data are available regarding blood glucose concentrations from broilers stunned by either ES using U.S. parameters or CAS under commercial conditions.
Lack of restraint during CAS may contribute to increased glucose due to physical movement during the stunning process (Webster and Fletcher, 2004).
Physical movement during an acute stress response rapidly releases glucose from muscle tissue storage (Verberne et al., 2016).
McKeegan et al. (2007) confirmed that various concentrations of CO2 used with CAS induced strong respiratory responses, such as gasping, panting, and neck stretching, whereas later phases of increased carbon dioxide induced convulsions and vigorous wing flapping.
A visual respiratory response is typically observed during the induction phase of CAS where CO2 is first introduced to the birds and is the only phase where birds are conscious. A physical response to stressors increases the circulation of glucose within the blood.
Possible sources of stressors during the conscious induction phase of CAS include the sudden exposure to CO2, mucosal membrane irritation from carbonic acid production during respiration, and dyspnea (Anton et al., 1992; McKeegan et al. 2006).
Physical movements observed prior to loss of consciousness or loss of posture include stretching of the neck, gasping, and occasionally flapping of the wings (Abeyesinghe et al., 2007; McKeegan et al., 2007).
Unconscious movement has also been observed during later phases of CAS, such as clonic or tonic convulsions and/or flapping (Lambooij et al., 1999; Gerritzen et al., 2013).
Identifying the precise timepoint when the glucose increase occurred could be beneficial to determine whether this increase in blood glucose occurs before or after loss of consciousness therefore indicating whether increased blood glucose during CAS is relevant to animal welfare.

Visible Wing Damage

Visible wing damage was significantly higher (P < 0.0001) for broilers stunned by CAS (3.6%) compared to ES (2.2%).
Variations in equipment on separate lines could contribute to wing damage.
Carcasses from each treatment group were evaluated on separate lines following defeathering and were therefore processed using different equipment.
Distinguishing the type of damage that occurred to wings for either stun method will help determine at what point on each stunning line this damage occurred.
CAS broilers had a high occurrence of broken wing tips.
Excess wing flapping during CAS can result in wing damage (Lambooij et al., 1999; McKeegan et al., 2007; Gerritzen et al. 2013).
Further research, closely categorizing wing damage before and after stunning in an experimental setting would be beneficial.
Increased wing damage on the CAS line would lead to a reduction in yield and final weight of product available for sale.

Breast Fillet Quality

Color

At debone, L* and a* were significantly different between stunning methods (P = 0.0005, P = 0.0303).
Breast fillets from ES birds had lower L* and higher a* values (53.15, 2.31) than CAS breast fillets (54.65, 1.96).
No difference in yellowness (b*) at debone.
At 24 hours post-debone, no differences were detected for L, a, or b* values between treatments (P = 0.0859, P = 0.2102, P = 0.1415).
Color/visual aspect is a main factor in guiding consumer product preference (Kennedy et al., 2005; Wideman et al., 2016).
The differences in L* and a* at debone were minimal and most likely not applicable to impact quality from a consumer standpoint.
Fillet color was not influenced by stunning methods.
Van Laack et al. (2000) found pale meat is determined by a L* value higher than 60. Neither L* values for ES or CAS stunned broiler breast fillets in this study were found to be higher than 60 initially or 24 h post-debone.
Raj et al. (1997) similarly found no significant differences between ES and CAS methods when analyzing breast fillet color 24 h post-debone.
Pinto et al. (2012) found that fillets were lighter and less red for gas killing in comparison to ES broilers but did not evaluate fillets at 24 h post-debone.
Gas killing (CAS-simulated) birds were exposed to 10% initial CO2 with a gradual increase to 30%, while time of exposure was defined as either observed cessation of breathing (gas killing) or loss of consciousness (gas stunning).
Lightness is inversely correlated to pH in poultry meat (Allen et al., 1998; Fletcher et al., 2000) because the myofibrillar proteins in poultry meat tightly bind to water when the pH is above the isoelectric point.
Higher pH results in more light to be readily absorbed by the muscle, hence, a darker appearance (Cornforth et al., 1994).
The higher L* value in breast meat from CAS broilers observed in the current study may be related to the higher levels of circulating glucose observed.
High circulating glucose is correlated to rapid-onset post-mortem glycolytic activity, which increases initial lactic acid levels post-mortem, and therefore may be a factor in the decreased pH values at debone (Fletcher et al., 2000).

pH

Initial breast fillet pH was significantly higher for ES broilers (5.92) compared to CAS broilers (5.81).
The pH value no longer differed between stunning types when evaluated 24 hours post-debone.
Initial values of lower pH in breast fillets from the CAS treatment align with the trends of lighter breast fillets and higher glucose concentrations post-stunning.
Decreased glucose availability within muscle tissue, due to the physiological demand in response to higher circulating concentrations, will result in early onset rigor mortis from glycolysis (Sandercock et al., 2001).
Salwani et al. (2016) found broilers stunned by CAS had increased activity of pyruvate kinases, indicating an increased use of glycolysis (Uyeda, 2013).
Early onset rigor induced by the increased glycolytic activity during CAS could explain initial pH differences at debone.
The ultimate pH would likely not be affected by this, since this increased glycolytic activity was only observed during stunning, which could also explain the lack of significant differences at 24 h post-debone.

Drip Loss

Drip loss did not differ between breast fillets from broilers stunned by CAS or ES (CAS = 4.83, ES = 4.84; P = 0.0859).
Typically, higher drip loss is associated with lighter colored meat and lower pH (Woelfel et al., 2002).
Our initial pH and L* values were observed to be lower for CAS than ES, those differences were minor and did not differ 24 h post-mortem. Therefore, there was no downstream impact observed for drip loss.

Conclusions

There was a clear increase in circulating blood glucose as a consequence of CAS, however, it is unknown whether this is an important factor for animal welfare or product quality.
Determining when glucose increases during CAS will allow for a better understanding of the effect of CO₂ exposure on broilers and could possibly lead to improved stunning parameters.
The occurrence of wing damage for CAS carcasses was demonstrated to be a critical issue under the conditions used in this commercial processing facility and should be evaluated in depth by categorizing damage by type, as well as evaluating the occurrence of damage before defeathering to isolate the timeframe in which the damage is occurring.
Breast fillet meat quality had significant but minor differences at debone between broilers stunned with either ES or CAS. Color, pH, and drip loss were not different at 24 h post-deboning indicating acceptability of breast fillet quality with use of either stunning system for consumers.