- Email: [email protected]
Improving appearance and microbiologic quality of broiler carcasses with an allostatic modulator
Improving appearance and microbiologic quality of broiler carcasses with an allostatic modulator M. E. Rubio-Garc´ıa,∗ M. S. Rubio-Lozano,† E. Ponce-Alquicira,‡ C. Rosario-Cortes,§ G. M. Nava,# and M. P. Casta˜ neda-Serrano∗,1 ∗
ABSTRACT An important priority of poultry producers is to guarantee animal welfare during animal production; however, broilers are exposed to unavoidable chronic stress (also known as allostasis) when they are captured, caged, and transported to the processing plant. This antemortem management causes allostatic load, animal injuries, and poor carcass quality. The aim of the present study was to evaluate the effects of an allostatic modulator (AM) on antemortem stress by measuring the appearance and microbiological quality of broiler carcasses. The AM consisted of a liquid formula containing ascorbic acid, acetyl salicylic acid, and electrolytes, administered orally 48 h before shipment to the processing plant. A total of 600 chickens (49-days-old) were used under a factorial arrangement 2 × 2 × 2 [2 commercial hybrid lines, 2 feed withdrawal
programs (10 and 16 h), and 2 water treatments (control and AM)]. Each treatment included 25 chickens per pen and was carried out in triplicate. The broilers were shipped, slaughtered, and processed in a commercial processing plant where carcass defects (bruises and broken bones caused by antemortem management), crop pH, and carcass bacterial counts were evaluated in all experimental groups. Broilers under AM treatment showed a reduction in carcass defects (P = 0.015), crop pH (P = 0.0001), coliforms counts (P = 0.014), and total aerobic mesophilic bacteria (P = 0.0001) when compared to the control treatment. The present study indicates that the AM can be used to improve carcass quality in broilers. Our study provides a novel and economic alternative to reduce the allostatic load in broilers.
Key words: allostatic load, broilers, carcass quality, stress, welfare 2015 Poultry Science 94:1957–1963 http://dx.doi.org/10.3382/ps/pev144
INTRODUCTION The need to produce more food in the shortest possible time has led to a change in poultry production practices. In current production systems, an imperative priority of farmers is to provide animal welfare; however, poultry are exposed to numerous and chronic stressors in the farms (McFarlane et al., 1989; Ak¸sit et al., 2006; Estevez, 2007; Jayalakshmi et al., 2009; ˇ Kun et al., 2009; Skrbi´ c et al., 2009). These chronic stressors trigger an active process in which broilers undergo a strong physiological response to preserve its body homeostasis. The accumulation of these stressors is known as allostasis, and the group of physiological C 2015 Poultry Science Association Inc. Received July 15, 2014. Accepted April 20, 2015. 1 Corresponding author: [email protected]
responses to deal with these stressors is defined as allostatic load (Seyle and Fortier, 1950; Minton, 1994; Korte et al., 2005; Stewart, 2006; Herring and Gawlik, 2007; Romero et al., 2009). In broilers, a severe allostatic load is caused by the antemortem management; consisting of feed withdrawal (FW), chicken capture, caging, transport, lairage time, and slaughter process. These stressors have a negative and economically significant impact on carcass defects (Bilgili, 1992; Kannan et al., 1997; Savenije et al., 2002; McNeal et al., 2003; Vecerek et al., 2006; Whiting et al., 2007). Experimentally, we have estimated that the economic losses caused by carcass defects during the antemortem management are about $0.19 (in United States dollars) per carcass (unpublished data). Water-soluble additives have been used as alternatives to reduce the allostatic load in broilers. Most of them contain either ascorbic acid (AA), acetyl salicylic acid (ASA), sodium bicarbonate, or
1957
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
Center for Teaching, Research, and Poultry Extension (CEIEPAv), School of Veterinary Medicine, National Autonomous University of Mexico, FMVZ-UNAM, M´exico, D.F. C.P. 13209; † Center for Teaching and Research in Production and Animal Health, FMVZ-UNAM, M´exico, D.F. C.P. 04510; ‡ Biotechnology Department, Autonomous Metropolitan University, Iztapalapa, M´exico City, M´exico, D.F. C.P. 09340; § Medicine and Poultry Husbandry Department, FMVZ-UNAM. M´exico City, M´exico, D.F. C.P. 04510; and # Department of Research and Graduate Studies in Food Science, School of Chemistry, University Autonomous of Queretaro, M´exico, C.P. 04510
RUBIO-GARC´IA ET AL.
1958
were randomly taken from the 3 experimental replicates and placed in properly identified treatment cages. During transportation to the processing plant, cages were placed in an equitable manner for all treatments in different sections (edges and middle of the platform) of the truck. The flock was sent to the processing plant at 6:36 am Central Daylight Time with a local temperature of 8◦ C and 68.7% RH. Animals arrived at 7:08 am Central Daylight Time with a local temperature of 9.5◦ C and 69.6% RH and the lairage time was 68 min prior to slaughtering; the birds were electrically stunned using 25 V, 0.02 amp, and 400 Hz, which caused a state of unconsciousness before death by decapitation.
Antemortem Evaluations MATERIALS AND METHODS The study was performed in the Poultry Research Center, Universidad Nacional Aut´ onoma de M´exico (UNAM). The average annual temperature is 16◦ C. All experimental procedures were approved by the Institutional Sub-Committee for the Care and Use of Experimental Animals of Graduate Health Sciences and Animal Production–UNAM.
At the arrival to the processing plant, time of transport, lairage, number of dead birds on arrival, and panting birds were recorded. During the stunning and decapitation processes, the number of flapping birds and head lifting were counted as indicators of animal welfare as suggested by the Welfare of Chickens Kept for Meat Production (The European Commission, 2000).
Crop pH Measurements Experimental Design A total of six hundred 1-day-old broilers (males and females) were housed in a conventional open-sided unit with clean wood shavings beds, brooders, manual feeders, and bell waterers. The broilers were raised from 1 to 49 d age and provided with feed and water ad libitum. Mortality during this period was 5% (total of 30 chickens). The chickens belonged to 2 commercial hybrid lines: Cobb 500 (defined as L1) and Ross 308 (defined as L2). The animals were subjected to 2 different FW programs (10 and 16 h), and 2 water treatments: tap-water without AM (i.e., control (CON) group] and tap-water supplemented with AM (i.e., AM group). Thus, the experimental arrangement consisted of 8 treatments with 3 replicates of 25 birds each, under a factorial arrangement 2 × 2 × 2. The AM formulation consisted of a combination of 50 mg AA, 62.5 mg ASA, and 251 μEq Na+ , K+ , and Cl− per L drinking water. The AM treatment was provided ad libitum, 48 h before the chickens were sent to a commercial processing plant located 10 km from the experimental farm.
Animal Transportation and Sacrifice Animals were manually captured by the feet (5 birds/hand), placed in a plastic poultry transport cage (97-cm length × 57-cm width × 27-cm height) to a final density of 10 broilers/cage and sent to the commercial processing plant. To avoid biases during transportation and processing of the animals, 10 chickens/treatment
After de-feathering, crop pH was measured in 30 birds/treatment selected at random. Briefly, the crop pH was measured by introducing a portable pH meter through a vertical incision (∼1 cm) made on the proximal side of crop. Before measurements, the pH meter was calibrated using a buffer solution at pH 7.0 as indicated by the manufacturer (Digital Pocket pH meter, Model 501, Mannix Testing and Measurement, Taiwan).
Evaluation of Microbial Quality in Carcasses To simulate crop rupture and the subsequent carcass microbial contamination, carcasses with crop incisions (n = 30/treatment) were subject to manual evisceration. Subsequently, 10 of the eviscerated carcasses/treatment were randomly selected for evaluation of the microbial quality. Briefly, the selected carcasses were placed in individual, sterile plastic bags and rinsed with 100 mL sterile PBS with manual shaking for 1 min. Then, the carcasses were removed from the plastic bag and the rinsing solution was kept at 4◦ C (Northcutt et al., 2007; Demirok et al., 2013). At the arrival to the laboratory, these rinsing solutions were subject to 10-fold serial dilutions and spread on aerobic mesophilic plates (RIDA count total), and total coliforms plates (RIDA count coliform) following manufacturer’s instructions (R-Biofarm AG, Darmstadt, Germany). These plates were incubated for 48 h at 37◦ C. After incubation, cfu were counted to determine the microbial load on the carcasses.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
electrolyte-balanced solutions (Gross, 1988; Stilborn et al., 1988; McKee and Harrison, 1995; McKee et al., 1997; Zulkifli et al., 2000; Borges et al., 2003, 2004; ¨ Khassaf et al., 2003; Tyler and Cummins, 2003; Ozaslan et al., 2004; Candelario-Jalil et al., 2006; Olanrewaju et al., 2007; Rohleder, 2008). Also, in the field, poultry veterinarians have observed that the combined use of AA, ASA, Cl, Na, and K, defined as an allostatic modulator (AM), is an effective and inexpensive treatment that reduces antemortem stress in broilers; however, its beneficial effects has not been evaluated systematically. The aim of the present study was to evaluate the effect of an AM on antemortem stress by measuring the appearance and microbiological quality of broiler carcasses.
IMPROVING QUALITY OF BROILER CARCASSES
Evaluation of Carcass Defects All carcasses (n = 57 to 73 per treatment) were subject to a systematic inspection by an experienced individual to classify and quantify visual defects (unilateral and bilateral bruises, scratches, and broken bones caused by antemortem management) based on parameters established in the Poultry Grading Manual (USDA, 1998). The presence or absence of defects in each carcass was recorded to estimate its frequency. Also, the total number of carcass condemnations was estimated as describe by Bilgili (2001).
Results of crop pH measurements and bacterial counts were subjected to ANOVA testing using a 2 × 2 × 2 factorial arrangement to determine 2- and 3-way interactions among AM, commercial line, and FW program. Also, a post-hoc Tukey test was performed using STATISTIX 9.0, Analytical Software (Tallahassee, FL, United States). Before the statistical analysis, the cfu counts were logarithmically transformed to achieve homogeneity of variance and were expressed as log10 cfu/mL. Results from the antemortem evaluations and frequency of defects were subject to factorial analysis of correspondence using XLSTAT 2012 v. 2.01 (Addinsoft SARL, New York, United States).
gies to reduce crop pH as a prevention method for pathogen colonization. It has been shown that a reduction by 0.3 and 1.0 pH unit in crop pH inhibits colonization by Salmonella enterica (S. enterica) (Byrd et al., 2001; Hinton Jr. et al., 2002; Avila et al., 2003; Smith and Berrang, 2006). Moreover, a reduction by 0.9 pH units in crop pH, decreased by half the total number of S. enterica colonizing the crop and ∼25% the number of crops positive to S. enterica recovery (Byrd et al., 2001). In the present study, broilers treated with the AM showed a reduced (P = 0.0001) crop pH when compared to CON treatments. Overall, chickens in the CON treatment had crop pH values varying between 5.09 and 4.88. In contrast, birds under AM treatments showed pH values between 4.52 and 4.12. Interestingly, under the present study conditions, there were not differences (P = 0.7960) in the crop pH between 10 and 16 h of FW programs in CON or AM treatments (Figure 1-A), suggesting that crop pH does not change
RESULTS AND DISCUSSION The present study was conducted to evaluate the usefulness of an AM to reduce negative effects caused by the antemortem stress in broilers. To accomplish this objective, an experiment was performed with 2 FW programs to assess its effects under conventional (10 h) and prolonged fasting stress (16 h). Broilers treated with the AM showed a reduction in crop pH, improved carcass-microbiological quality, and reduced carcass-processing defects (bruises on legs, backs, pygostyles, breasts, necks, wings; scratches; broken bones; and total condemnations) with no effect on animal welfare parameters (dead birds on arrival, panting birds, flapping birds, and head lifting birds) in both commercial hybrid lines used in the present study.
Crop pH Measurements Crop pH is one of the most important factors influencing crop bacterial populations (Hinton Jr. et al., 2000a,b, 2002; Avila et al., 2003; Smith and Berrang, 2006). Broilers under FW programs experience a reduction in lactate and short chain fatty acid production in their crops; this situation leads to an increase in crop pH (by 0.5 to 1.0 pH unit) favoring the survival and colonization of microbial pathogens (Hinton Jr. et al., 2000a,b; Northcutt, 2001; Avila et al., 2003; Rostango, 2009). Thus, it is important to design strate-
Figure 1. Water supplemented with an allostatic modulator (AM) reduces crop pH independent of the feed withdraw program or commercial hybrid line used in the experiments. Depicted values correspond to mean values. Thirty broiler crops per treatment were used for the analysis. A) Crop pH reduction using two different feed withdrawal programs. B) Crop pH reduction using 2 different commercial hybrid lines. Treatments consisted of tap-water treated with (AM) or without (CON) an AM. The AM and control (CON) treatments were provided ad libitum, 48 h before the chickens were sent to a commercial processing plant. Different letters within treatments indicate significantly different means (P = 0.0001) according to ANOVA factorial design, Tukey test.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
Statistical Analysis
1959
RUBIO-GARC´IA ET AL.
1960
to the CON group (Table 1). Similar effects on carcass contamination have been reported by Byrd et al. (2001) and Avila et al. (2003) with the use an acidifier in drinking water. Interestingly, we also observed that the AM treatment, in animals under conventional (10 h) and prolonged (16 h) FW programs, showed a significant reduction in coliforms and mesophiles (P = 0.003 and P = 0.0004; respectively) counts on carcasses, independently of the chicken genetic background (P > 0.86; Table 1). To the best of our knowledge, this is one of the first reports indicating that the supplementation with a combination of AA, ASA, Na+ , K+ , and Cl− in drinking water decreases bacterial loads in chicken carcass. Taken together, our results indicate that the AM treatment could be a useful tool to improve bacterial carcass quality.
Microbiological Quality
Broilers are exposed to unavoidable allostasis when they are captured, caged, and transported to the processing plant. This antemortem stress causes animal injuries and poor carcass quality. To reduce these losses, water soluble additives (mainly based on AA and ASA) have been used to reduce the allostatic load in broilers (Gross, 1988; Stilborn et al., 1988; McKee and Harri¨ son, 1995; McKee et al., 1997; Ozaslan et al., 2004). Although the mechanisms of action of AA and ASA have not been fully elucidated, its combined use has been associated with a reduction of nociception and systemic inflammatory responses (Rokyta et al., 2003;
Feed-withdraw programs longer than 12 h increase bacteria counts on the carcass surface (Hinton Jr. et al., 2000a,b, Northcutt, 2001; Avila et al., 2003;). Thus, it is expected that the reduction in crop pH by the AM treatment, also generates a reduction in bacterial loads on broiler carcasses. As anticipated, carcass coliform counts in the AM treatments were reduced (P = 0.014) when compared to the CON groups (Table 1). Likewise, we observed that carcass mesophilic counts were also reduced (P = 0.0001) in the AM treatment compared
Carcass-Processing Defects
Table 1. Means of microbial counts on broiler carcasses of finishing broilers from 2 commercial hybrid lines treated with or without an allostatic modulator (AM)1 under conventional and prolonged feed withdraw (FW) programs. ufc/mL log10 Groups L1 L1 L1 L1 L2 L2 L2 L2
10 10 16 16 10 10 16 16
CON AM CON AM CON AM CON AM
P-values
HL L1 L1 L1 L1 L2 L2 L2 L2
FW 10 10 16 16 10 10 16 16 AM FW HL AM∗FW AM∗HL FW∗HL AM∗FW∗HL Pooled SEM n (per group)
AM CON AM CON AM CON AM CON AM
Coliforms a
Total mesophiles
6.66 6.19b 6.20b 5.28c 6.32a 6.21b 6.03c 5.87c
7.05a,b 6.62c 6.77b 6.56c 7.11a 6.72b 6.66b 6.50c
0.014 0.003 0.868 0.449 0.091 0.256 0.542 0.2319 10
0.0001 0.0004 0.990 0.107 0.737 0.221 0.998 0.0966 10
a–c Different letters within columns indicate significantly different means (P < 0.05) according to ANOVA factorial design, Tukey test. 1 On d 47, broilers received drinking water supplemented with an AM [containing 50 mg ascorbic acid, 62.5 mg acetyl salicylic acid, and 251 μ Eq Na+ , K+ and Cl− per L water]; 10 = conventional program; 16 = prolonged program; HL = Hybrid lines; AM treatment = water supplemented with the AM; CON treatment = water without AM.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
between conventional (10 h) and prolonged fasting stress (16 h). Moreover, similar effects on pH (P = 0.9528) were observed (Figure 1-B) in both genetic backgrounds (L1 and L2). These results indicate that the AM reduces crop pH independently of the FW program and chicken genetic background. Remarkably, to the best of our knowledge, none of the ingredients (AA, ASA, Na+ , K+ , and Cl− ) of the AM, alone or in combination, have been previously associated with a capacity to reduce crop pH. This effect could be attributed to the capability of the AM to reduce the pH of the drinking water. To verify this idea, we measured the pH of tap water treated with the AM and observed a reduction of 2.0 pH units compared to untreated water (pH 5.7 and 7.7, respectively). Altogether this indicates that the AM treatment could be an important tool to reduce crop pH during FW programs and possible prevention of pathogen colonization.
IMPROVING QUALITY OF BROILER CARCASSES
1961
Candelario-Jalil et al., 2006). Thus, it was expected that the AM treatment lowered the allostatic load in broilers with a subsequent improvement in carcass quality. To determine the relationship between treatment effects and the amount of carcass defects, a factorial analysis of correspondence was carried out. For this analysis, a data matrix was constructed using treatment descriptors (AM vs. CON) and the observed unilateral and bilateral defects: bruises on legs, backs, pygostyles, breasts, necks, wings; skin scratches; broken bones; and total condemnations. This analysis revealed a strong association (inertia = 0.738) between treatments and carcass defects (P = 0.015; Figure 2). The factorial analysis of correspondence explained 57.66% of the variance within 2 axes, showing that the frequency of each carcass defect could be directly associated with the use of AM and the time of FW. Specifically, on this map, the distances between treatments and carcass defects reflect the level of statistical association. Thus, it is observed that the treatments positions on the map-land in different map-quadrants, indicating a weak association. Also, it is perceived that unilateral broken and bruised wings, and bruises on the back are strongly associated with CON treatments under 10 h FW. Moreover, bilateral bruises on the wings are strongly associated with 16 h FW in the CON group (Figure 2). These results indicate that the treatment with AM had a weak sta-
tistical association with carcass defects, indicating that water supplementation of AM could be useful to decrease carcass-processing defects.
Antemortem Evaluation In the present study, we also evaluated if AM treatment had an effect on animal welfare parameters. To accomplish this goal, the numbers of dead birds on arrival, panting birds, flapping birds, and head-lifting birds were estimated. We observed no effects (P ≥ 0.05, inertia 0.086; data not shown) on these animal welfare parameters in both commercial hybrid lines used; indicating that the AM could be safely used in poultry production.
CONCLUSIONS The present study reveals that the supplementation of an AM in drinking water effectively reduces crop pH, improves carcass-microbiological quality, and reduces carcass-processing defects in broiler chickens. All together this indicates that the use of an AM is a novel and inexpensive alternative to reduce the allostatic load in broilers.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
Figure 2. Association of water treatments with carcass defects. Factorial correspondence analysis, explaining 57.66% of the variation within two axes (inertia = 0.738). Treatments consisted of tap water treated with an allostatic modulator (AM) or without [control (CON)] an AM. The AM and CON treatment were provided ad libitum, 48 h before the chickens (n = 57 to 73 per treatment) were sent to a commercial processing plant. Analyses were performed using 2 commercial hybrid lines (L1 and L2) treated with (AM) or without (CON) an AM under conventional (10 h) and prolonged (16 h) feed withdraw programs.
RUBIO-GARC´IA ET AL.
1962
ACKNOWLEDGMENTS This study was supported by a grant from Alta Tecnolog´ıa Industrial para la Salud Animal, Project UNAM- Alta Tecnolog´ıa Industrial para la Salud Animal Number 17549-1590-15-XI-05. The authors acknowledge the help provided by the students and staff of the Centro de Ense˜ nanza, Investigaci´ on y Extensi´ on en Producci´ on Av´ıcola, UNAM, during the execution of the study. Also, we thank H´ector Escalona from Universidad Aut´ onoma Metropolitana, Iztapalapa, M´exico for his kind advice in statistical analysis.
REFERENCES
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
¨ ¨ Ak¸sit, M., S. Yal¸cın, S. Ozkan, K. Metin, and D. Ozdemir. 2006. Effects of temperature during rearing and crating on stress parameters and meat quality of broilers. Poult. Sci. 85: 1867–1874. Avila, L. A. F., C. W. Canal, C. T. P. Salle, and H. L. Moraes. 2003. Effect of acidified drinking water on the recovery of Salmonella enteritidis from broiler crops. Rev. Bras. Cienc. Avic. 5:183–188. Bilgili, S. F. 1992. Electrical stunning of broilers–Basic concepts and carcass quality implications: A review. J. Appl. Poult. Res. 1:135– 146. Bilgili, S. F. 2001. Poultry meat inspection and grading. Pages 54– 58 in Poultry Meat Processing. Alan R. Sams, ed. Department of Poultry Science. Texas A&M University. CRC Press, Boca Raton, FL, United States. Borges, S. A., A. V. Fischer-da Silva, J. Ariki, D. M. Hooge, and K. R. Cummings. 2003. Dietary electrolyte balance for broiler chickens exposed to thermoneutral or heat-stress environments. Poult. Sci. 82:428–435. Borges, S. A., A. V. Fischer-da Silva, A. Majorka, D. M. Hooge, and K. R. Cummings. 2004. Physiological responses of broiler chickens to heat stress and dietary electrolyte balance (sodium plus potassium minus chloride, milliequivalents per kilogram). Poult. Sci. 83:1551–1558. Byrd, J. A., B. M. Hargis, D. J. Caldwell, R. H. Bailey, K. L. Herron, J. L. McReynolds, R. L. Brewer, R. C. Anderson, K. M. Bischoff, T. R. Callaway, and L. F. Kubena. 2001. Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on salmonella and campylobacter contamination of broilers. Poult. Sci. 80:278–283. Candelario-Jalil, E., R. S. Akundi, H. S. Bhatia, K. Lieb, K. Appel, E. Mu˜ noz, M. H¨ ull, and B. L. Fiebich. 2006. Ascorbic acid enhances the inhibitory effect of aspirin on neuronal cyclooxygenase-2-mediated prostaglandin E2 production. J. Neuroimmunol. 174:39–51. Demirok, E., G. Veluz, W. V. Stuyvenberg, M. P. Casta˜ neda, A. Byrd, and C. Z. Alvarado. 2013. Quality and safety of broiler meat in various chilling systems. Poult. Sci. 92: 1117–1126. Estevez, I. 2007. Density allowances for broilers: Where to set the limits? Poult. Sci. 86:1265–1272. Gross, W. B. 1988. Effect of environmental stress on the responses of ascorbic-acid-treated chickens to Escherichia coli challenge infection. Avian Dis. 32:432–436. Herring, G., and D. E. Gawlik. 2007. The role of stress proteins in the study of allostatic overload in birds: use and applicability to current studies in avian ecology. Scientific World J. 7: 1596–1602. Hinton, Jr. A., R. J. Buhr, and K. D. Ingram. 2000a. Physical, chemical, and microbiological changes in the crop of broiler chickens subjected to incremental feed withdrawal. Poult. Sci. 79:212–218. Hinton, Jr. A., R. J. Buhr, and K. D. Ingram. 2000b. Reduction of Salmonella in the crop of broiler chickens subjected to feed withdrawal. Poult. Sci. 79:1566–1570. Hinton, Jr. A, R. J. Buhr, and K. D. Ingram. 2002. Carbohydratenased cocktails that decrease the population of Salmonella and
Campylobacter in the crop of broiler chickens subjected to feed withdrawal. Poult. Sci. 81:780–784. Jayalakshmi, T., R. Kumararaj, T. Sivakumar, and T. V. Thanga. 2009. Carcass characteristics of commercial broilers reared under varying stocking densities. Tamilnadu J. Vet. Anim. Sci. 5:132– 135. Kannan, G., J. L. Heath, C. J. Wabeck, M. Souza, J. C. Howe, and J. A. Mench. 1997. Effects of crating and transport on stress on meat quality characteristics in broilers. Poult. Sci. 76: 523–529. Khassaf, M., A. McArdle, C. Esanu, A. Vasilaki, F. McArdle, R. D. Griffiths, D. A. Brodie, and M. J. Jackson. 2003. Effect of vitamin C suplements on antioxidant defence and stress protein in human lymphocytes and skeletal muscle. J. Physiol. 549:645–652. Korte, S. M., J. M. Koolhaas, J. C. Wingfield, and B. S. McEwen. 2005. The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade-off in health and disease. Neurosci. Biobehav. Rev. 29:3–38. doi:10.1016 /j.neubiorev.2004.08.009 Kun, Z., A. N. Uluocak, and M. Karaman. 2009. The influence of some factors on carcass defects during fattening period in broilers. Arch. Zootec. 58:117–120. McFarlane, J. M., S. E. Curtis, R. D. Shanks, and S. G. Carmer. 1989. Multiple concurrent stressors in chicks. 1. Effect on weight gain, feed intake and behavior. Poult. Sci. 68:501–509. McKee, J. S., and P. C. Harrison. 1995. Effects of supplemental ascorbic acid on the performance of broiler chickens exposed to multiple concurrent stressors. Poult. Sci. 74:1772–1785. McKee, J. S., P. C. Harrison, and G. L. Riskowski. 1997. Effects of supplemental ascorbic acid on the energy conversion of broiler chicks during heat stress and feed withdrawal. Poult. Sci. 76:1278– 1286. McNeal, W. D., D. L. Fletcher, and R. J. Buhr. 2003. Effects of stunning and decapitation on broiler activity during bleeding, blood loss, carcass and breast meat quality. Poult. Sci. 82:163– 168. Minton, J. E. 1994. Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. J Anim. Sci. 72:1891–1898. Northcutt, J. K. 2001. Preslaugther factors affecting poultry meat quality. Pages 5–18 in Poultry Meat Processing. Alan R. Sams, ed. Department of Poultry Science, Texas A&M University, CRC Press, Boca Raton, FL, United States. Northcutt, J., D. Smith, K. D. Ingram, A. Hinton, Jr., and M. Musgrove. 2007. Recovery of bacteria from broiler carcasses after spray washing with acidified electrolyzed water or sodium hypochlorite solutions. Poult. Sci. 86:2239–2244. Olanrewaju, H. A., J. P. Thaxton, W. A. Dozier, III, and S. L. Branton. 2007. Electrolyte diets, stress, and acid-base balance in broiler chickens. Poult. Sci. 486:1363–1371. ¨ Ozaslan, M., T. Aytekin, I. H. Kilic, A. I. Bozkurt, E. G¨ uld¨ ur, B. Cengiz, and C. Bagci. 2004. The effect of vitamin C supplementation on leukocyte counts and exercise performance. J. Exerc. Physiol. Online. 7:101–105. Rohleder, N. 2008. Preventing acute stress-induced inflammatory disinhibition by aspirin: What does it tell us about the mechanism? Brain Behav. Immun. 22:148–149. Rokyta, R., V. Holecek, I. Pek´ arkova, J. Krejcov´ a, J. Racek, L. Trefil, and A. Yamamotov´ a. 2003. Free radicals after painful stimulation are influenced by antioxidants and analgesics. Neuro Endocrinol Lett. 24:304–309. Romero, L. M., M. J. Dickens, and N. E. Cyr. 2009. The reactive scope model–A new model integrating homeostasis, allostasis and stress. Horm. Behav. 55:375–389. Rostango, M. H. 2009. Can stress in farm animals increase food safety risk?. Foodborne Pathog. Dis. 6:767–776. doi.10.1089/fpd.2009.0315 Savenije, B., E. Laambooij, M. A. Gerritzen, K. Venema, and J. Korf. 2002. Effects of feed deprivation and transport on preslaughter blood metabolites, early postmortem muscle metabolites, and meat quality. Poult. Sci. 81:699–708. Seyle, H., and C. Fortier. 1950. Adaptive reaction to stress. Proc. 29th Annual Meeting of the Association for Research in Nervous and Mental Disease. Baltimore, MD, United States.
IMPROVING QUALITY OF BROILER CARCASSES ˇ Skrbi´ c, Z., Z. Pavlovski, and M. Luki´c. 2009. Stocking density–Factor of production performance, quality and broiler welfare. Biotech. Anim. Husb. 25:359–372. Smith, D. P., and M. E. Berrang. 2006. Prevalence and numbers of bacteria in broiler crop and gizzard contents. Poult. Sci. 85:144– 147. Stewart, J. A. 2006. The detrimental effects of allostasis: Allostatic load as a measure of cumulative stress. J. Physiol. Anthropol. 25:133–145. Stilborn, H. L., G. C. Harris, Jr., W. G. Bottje, and P. W. Waldroup. 1988. Ascorbic acid and acetylsalicylic acid (aspirin) in the diet of broilers maintained under heat stress conditions. Poult. Sci. 67:1183–1187. The European Commission. 2000. The Welfare of Chickens Kept for Meat Production (Broilers). Report of the Scientific Committee on Animal Health and Animal Welfare. http://ec.europa.eu/food/fs/sc/scah/out39 en.pdf
1963
Tyler, P. J., and K. A. Cummins. 2003. Effect of dietary ascorbyl-2phosphate on immune function after transport to a feeding facility. J. Dairy. Sci. 86:622–629. USDA. 1998. Poultry Grading Manual. Agriculture Handbook No. 31. USDA Agricultural Marketing Services, Washington, DC. Vecerek, V., S. Grbalova, E. Voslarova, B. Janackova, and M. Malena. 2006. Effects of travel distance and the season of the year on death rates of broilers transported to poultry processing plants. Poult. Sci. 85:1881–1884. Whiting, T. L., M. E. Drain, and D. P. Rasali. 2007. Warm weather transport of broiler chickens in Manitoba. II. Truck management factors associated with death loss in transit to slaughter. Can. Vet. J. 48:148–154. Zulkifli, I., M. T. Che Norma, C. H. Chong, and T. C. Loh. 2000. Heterophil to lymphocyte ratio and tonic immobility reactions to preslaughter handling in broiler chickens treated with ascorbic acid. Poult. Sci. 79:402–406. Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
ABSTRACT An important priority of poultry producers is to guarantee animal welfare during animal production; however, broilers are exposed to unavoidable chronic stress (also known as allostasis) when they are captured, caged, and transported to the processing plant. This antemortem management causes allostatic load, animal injuries, and poor carcass quality. The aim of the present study was to evaluate the effects of an allostatic modulator (AM) on antemortem stress by measuring the appearance and microbiological quality of broiler carcasses. The AM consisted of a liquid formula containing ascorbic acid, acetyl salicylic acid, and electrolytes, administered orally 48 h before shipment to the processing plant. A total of 600 chickens (49-days-old) were used under a factorial arrangement 2 × 2 × 2 [2 commercial hybrid lines, 2 feed withdrawal
programs (10 and 16 h), and 2 water treatments (control and AM)]. Each treatment included 25 chickens per pen and was carried out in triplicate. The broilers were shipped, slaughtered, and processed in a commercial processing plant where carcass defects (bruises and broken bones caused by antemortem management), crop pH, and carcass bacterial counts were evaluated in all experimental groups. Broilers under AM treatment showed a reduction in carcass defects (P = 0.015), crop pH (P = 0.0001), coliforms counts (P = 0.014), and total aerobic mesophilic bacteria (P = 0.0001) when compared to the control treatment. The present study indicates that the AM can be used to improve carcass quality in broilers. Our study provides a novel and economic alternative to reduce the allostatic load in broilers.
Key words: allostatic load, broilers, carcass quality, stress, welfare 2015 Poultry Science 94:1957–1963 http://dx.doi.org/10.3382/ps/pev144
INTRODUCTION The need to produce more food in the shortest possible time has led to a change in poultry production practices. In current production systems, an imperative priority of farmers is to provide animal welfare; however, poultry are exposed to numerous and chronic stressors in the farms (McFarlane et al., 1989; Ak¸sit et al., 2006; Estevez, 2007; Jayalakshmi et al., 2009; ˇ Kun et al., 2009; Skrbi´ c et al., 2009). These chronic stressors trigger an active process in which broilers undergo a strong physiological response to preserve its body homeostasis. The accumulation of these stressors is known as allostasis, and the group of physiological C 2015 Poultry Science Association Inc. Received July 15, 2014. Accepted April 20, 2015. 1 Corresponding author: [email protected]
responses to deal with these stressors is defined as allostatic load (Seyle and Fortier, 1950; Minton, 1994; Korte et al., 2005; Stewart, 2006; Herring and Gawlik, 2007; Romero et al., 2009). In broilers, a severe allostatic load is caused by the antemortem management; consisting of feed withdrawal (FW), chicken capture, caging, transport, lairage time, and slaughter process. These stressors have a negative and economically significant impact on carcass defects (Bilgili, 1992; Kannan et al., 1997; Savenije et al., 2002; McNeal et al., 2003; Vecerek et al., 2006; Whiting et al., 2007). Experimentally, we have estimated that the economic losses caused by carcass defects during the antemortem management are about $0.19 (in United States dollars) per carcass (unpublished data). Water-soluble additives have been used as alternatives to reduce the allostatic load in broilers. Most of them contain either ascorbic acid (AA), acetyl salicylic acid (ASA), sodium bicarbonate, or
1957
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
Center for Teaching, Research, and Poultry Extension (CEIEPAv), School of Veterinary Medicine, National Autonomous University of Mexico, FMVZ-UNAM, M´exico, D.F. C.P. 13209; † Center for Teaching and Research in Production and Animal Health, FMVZ-UNAM, M´exico, D.F. C.P. 04510; ‡ Biotechnology Department, Autonomous Metropolitan University, Iztapalapa, M´exico City, M´exico, D.F. C.P. 09340; § Medicine and Poultry Husbandry Department, FMVZ-UNAM. M´exico City, M´exico, D.F. C.P. 04510; and # Department of Research and Graduate Studies in Food Science, School of Chemistry, University Autonomous of Queretaro, M´exico, C.P. 04510
RUBIO-GARC´IA ET AL.
1958
were randomly taken from the 3 experimental replicates and placed in properly identified treatment cages. During transportation to the processing plant, cages were placed in an equitable manner for all treatments in different sections (edges and middle of the platform) of the truck. The flock was sent to the processing plant at 6:36 am Central Daylight Time with a local temperature of 8◦ C and 68.7% RH. Animals arrived at 7:08 am Central Daylight Time with a local temperature of 9.5◦ C and 69.6% RH and the lairage time was 68 min prior to slaughtering; the birds were electrically stunned using 25 V, 0.02 amp, and 400 Hz, which caused a state of unconsciousness before death by decapitation.
Antemortem Evaluations MATERIALS AND METHODS The study was performed in the Poultry Research Center, Universidad Nacional Aut´ onoma de M´exico (UNAM). The average annual temperature is 16◦ C. All experimental procedures were approved by the Institutional Sub-Committee for the Care and Use of Experimental Animals of Graduate Health Sciences and Animal Production–UNAM.
At the arrival to the processing plant, time of transport, lairage, number of dead birds on arrival, and panting birds were recorded. During the stunning and decapitation processes, the number of flapping birds and head lifting were counted as indicators of animal welfare as suggested by the Welfare of Chickens Kept for Meat Production (The European Commission, 2000).
Crop pH Measurements Experimental Design A total of six hundred 1-day-old broilers (males and females) were housed in a conventional open-sided unit with clean wood shavings beds, brooders, manual feeders, and bell waterers. The broilers were raised from 1 to 49 d age and provided with feed and water ad libitum. Mortality during this period was 5% (total of 30 chickens). The chickens belonged to 2 commercial hybrid lines: Cobb 500 (defined as L1) and Ross 308 (defined as L2). The animals were subjected to 2 different FW programs (10 and 16 h), and 2 water treatments: tap-water without AM (i.e., control (CON) group] and tap-water supplemented with AM (i.e., AM group). Thus, the experimental arrangement consisted of 8 treatments with 3 replicates of 25 birds each, under a factorial arrangement 2 × 2 × 2. The AM formulation consisted of a combination of 50 mg AA, 62.5 mg ASA, and 251 μEq Na+ , K+ , and Cl− per L drinking water. The AM treatment was provided ad libitum, 48 h before the chickens were sent to a commercial processing plant located 10 km from the experimental farm.
Animal Transportation and Sacrifice Animals were manually captured by the feet (5 birds/hand), placed in a plastic poultry transport cage (97-cm length × 57-cm width × 27-cm height) to a final density of 10 broilers/cage and sent to the commercial processing plant. To avoid biases during transportation and processing of the animals, 10 chickens/treatment
After de-feathering, crop pH was measured in 30 birds/treatment selected at random. Briefly, the crop pH was measured by introducing a portable pH meter through a vertical incision (∼1 cm) made on the proximal side of crop. Before measurements, the pH meter was calibrated using a buffer solution at pH 7.0 as indicated by the manufacturer (Digital Pocket pH meter, Model 501, Mannix Testing and Measurement, Taiwan).
Evaluation of Microbial Quality in Carcasses To simulate crop rupture and the subsequent carcass microbial contamination, carcasses with crop incisions (n = 30/treatment) were subject to manual evisceration. Subsequently, 10 of the eviscerated carcasses/treatment were randomly selected for evaluation of the microbial quality. Briefly, the selected carcasses were placed in individual, sterile plastic bags and rinsed with 100 mL sterile PBS with manual shaking for 1 min. Then, the carcasses were removed from the plastic bag and the rinsing solution was kept at 4◦ C (Northcutt et al., 2007; Demirok et al., 2013). At the arrival to the laboratory, these rinsing solutions were subject to 10-fold serial dilutions and spread on aerobic mesophilic plates (RIDA count total), and total coliforms plates (RIDA count coliform) following manufacturer’s instructions (R-Biofarm AG, Darmstadt, Germany). These plates were incubated for 48 h at 37◦ C. After incubation, cfu were counted to determine the microbial load on the carcasses.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
electrolyte-balanced solutions (Gross, 1988; Stilborn et al., 1988; McKee and Harrison, 1995; McKee et al., 1997; Zulkifli et al., 2000; Borges et al., 2003, 2004; ¨ Khassaf et al., 2003; Tyler and Cummins, 2003; Ozaslan et al., 2004; Candelario-Jalil et al., 2006; Olanrewaju et al., 2007; Rohleder, 2008). Also, in the field, poultry veterinarians have observed that the combined use of AA, ASA, Cl, Na, and K, defined as an allostatic modulator (AM), is an effective and inexpensive treatment that reduces antemortem stress in broilers; however, its beneficial effects has not been evaluated systematically. The aim of the present study was to evaluate the effect of an AM on antemortem stress by measuring the appearance and microbiological quality of broiler carcasses.
IMPROVING QUALITY OF BROILER CARCASSES
Evaluation of Carcass Defects All carcasses (n = 57 to 73 per treatment) were subject to a systematic inspection by an experienced individual to classify and quantify visual defects (unilateral and bilateral bruises, scratches, and broken bones caused by antemortem management) based on parameters established in the Poultry Grading Manual (USDA, 1998). The presence or absence of defects in each carcass was recorded to estimate its frequency. Also, the total number of carcass condemnations was estimated as describe by Bilgili (2001).
Results of crop pH measurements and bacterial counts were subjected to ANOVA testing using a 2 × 2 × 2 factorial arrangement to determine 2- and 3-way interactions among AM, commercial line, and FW program. Also, a post-hoc Tukey test was performed using STATISTIX 9.0, Analytical Software (Tallahassee, FL, United States). Before the statistical analysis, the cfu counts were logarithmically transformed to achieve homogeneity of variance and were expressed as log10 cfu/mL. Results from the antemortem evaluations and frequency of defects were subject to factorial analysis of correspondence using XLSTAT 2012 v. 2.01 (Addinsoft SARL, New York, United States).
gies to reduce crop pH as a prevention method for pathogen colonization. It has been shown that a reduction by 0.3 and 1.0 pH unit in crop pH inhibits colonization by Salmonella enterica (S. enterica) (Byrd et al., 2001; Hinton Jr. et al., 2002; Avila et al., 2003; Smith and Berrang, 2006). Moreover, a reduction by 0.9 pH units in crop pH, decreased by half the total number of S. enterica colonizing the crop and ∼25% the number of crops positive to S. enterica recovery (Byrd et al., 2001). In the present study, broilers treated with the AM showed a reduced (P = 0.0001) crop pH when compared to CON treatments. Overall, chickens in the CON treatment had crop pH values varying between 5.09 and 4.88. In contrast, birds under AM treatments showed pH values between 4.52 and 4.12. Interestingly, under the present study conditions, there were not differences (P = 0.7960) in the crop pH between 10 and 16 h of FW programs in CON or AM treatments (Figure 1-A), suggesting that crop pH does not change
RESULTS AND DISCUSSION The present study was conducted to evaluate the usefulness of an AM to reduce negative effects caused by the antemortem stress in broilers. To accomplish this objective, an experiment was performed with 2 FW programs to assess its effects under conventional (10 h) and prolonged fasting stress (16 h). Broilers treated with the AM showed a reduction in crop pH, improved carcass-microbiological quality, and reduced carcass-processing defects (bruises on legs, backs, pygostyles, breasts, necks, wings; scratches; broken bones; and total condemnations) with no effect on animal welfare parameters (dead birds on arrival, panting birds, flapping birds, and head lifting birds) in both commercial hybrid lines used in the present study.
Crop pH Measurements Crop pH is one of the most important factors influencing crop bacterial populations (Hinton Jr. et al., 2000a,b, 2002; Avila et al., 2003; Smith and Berrang, 2006). Broilers under FW programs experience a reduction in lactate and short chain fatty acid production in their crops; this situation leads to an increase in crop pH (by 0.5 to 1.0 pH unit) favoring the survival and colonization of microbial pathogens (Hinton Jr. et al., 2000a,b; Northcutt, 2001; Avila et al., 2003; Rostango, 2009). Thus, it is important to design strate-
Figure 1. Water supplemented with an allostatic modulator (AM) reduces crop pH independent of the feed withdraw program or commercial hybrid line used in the experiments. Depicted values correspond to mean values. Thirty broiler crops per treatment were used for the analysis. A) Crop pH reduction using two different feed withdrawal programs. B) Crop pH reduction using 2 different commercial hybrid lines. Treatments consisted of tap-water treated with (AM) or without (CON) an AM. The AM and control (CON) treatments were provided ad libitum, 48 h before the chickens were sent to a commercial processing plant. Different letters within treatments indicate significantly different means (P = 0.0001) according to ANOVA factorial design, Tukey test.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
Statistical Analysis
1959
RUBIO-GARC´IA ET AL.
1960
to the CON group (Table 1). Similar effects on carcass contamination have been reported by Byrd et al. (2001) and Avila et al. (2003) with the use an acidifier in drinking water. Interestingly, we also observed that the AM treatment, in animals under conventional (10 h) and prolonged (16 h) FW programs, showed a significant reduction in coliforms and mesophiles (P = 0.003 and P = 0.0004; respectively) counts on carcasses, independently of the chicken genetic background (P > 0.86; Table 1). To the best of our knowledge, this is one of the first reports indicating that the supplementation with a combination of AA, ASA, Na+ , K+ , and Cl− in drinking water decreases bacterial loads in chicken carcass. Taken together, our results indicate that the AM treatment could be a useful tool to improve bacterial carcass quality.
Microbiological Quality
Broilers are exposed to unavoidable allostasis when they are captured, caged, and transported to the processing plant. This antemortem stress causes animal injuries and poor carcass quality. To reduce these losses, water soluble additives (mainly based on AA and ASA) have been used to reduce the allostatic load in broilers (Gross, 1988; Stilborn et al., 1988; McKee and Harri¨ son, 1995; McKee et al., 1997; Ozaslan et al., 2004). Although the mechanisms of action of AA and ASA have not been fully elucidated, its combined use has been associated with a reduction of nociception and systemic inflammatory responses (Rokyta et al., 2003;
Feed-withdraw programs longer than 12 h increase bacteria counts on the carcass surface (Hinton Jr. et al., 2000a,b, Northcutt, 2001; Avila et al., 2003;). Thus, it is expected that the reduction in crop pH by the AM treatment, also generates a reduction in bacterial loads on broiler carcasses. As anticipated, carcass coliform counts in the AM treatments were reduced (P = 0.014) when compared to the CON groups (Table 1). Likewise, we observed that carcass mesophilic counts were also reduced (P = 0.0001) in the AM treatment compared
Carcass-Processing Defects
Table 1. Means of microbial counts on broiler carcasses of finishing broilers from 2 commercial hybrid lines treated with or without an allostatic modulator (AM)1 under conventional and prolonged feed withdraw (FW) programs. ufc/mL log10 Groups L1 L1 L1 L1 L2 L2 L2 L2
10 10 16 16 10 10 16 16
CON AM CON AM CON AM CON AM
P-values
HL L1 L1 L1 L1 L2 L2 L2 L2
FW 10 10 16 16 10 10 16 16 AM FW HL AM∗FW AM∗HL FW∗HL AM∗FW∗HL Pooled SEM n (per group)
AM CON AM CON AM CON AM CON AM
Coliforms a
Total mesophiles
6.66 6.19b 6.20b 5.28c 6.32a 6.21b 6.03c 5.87c
7.05a,b 6.62c 6.77b 6.56c 7.11a 6.72b 6.66b 6.50c
0.014 0.003 0.868 0.449 0.091 0.256 0.542 0.2319 10
0.0001 0.0004 0.990 0.107 0.737 0.221 0.998 0.0966 10
a–c Different letters within columns indicate significantly different means (P < 0.05) according to ANOVA factorial design, Tukey test. 1 On d 47, broilers received drinking water supplemented with an AM [containing 50 mg ascorbic acid, 62.5 mg acetyl salicylic acid, and 251 μ Eq Na+ , K+ and Cl− per L water]; 10 = conventional program; 16 = prolonged program; HL = Hybrid lines; AM treatment = water supplemented with the AM; CON treatment = water without AM.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
between conventional (10 h) and prolonged fasting stress (16 h). Moreover, similar effects on pH (P = 0.9528) were observed (Figure 1-B) in both genetic backgrounds (L1 and L2). These results indicate that the AM reduces crop pH independently of the FW program and chicken genetic background. Remarkably, to the best of our knowledge, none of the ingredients (AA, ASA, Na+ , K+ , and Cl− ) of the AM, alone or in combination, have been previously associated with a capacity to reduce crop pH. This effect could be attributed to the capability of the AM to reduce the pH of the drinking water. To verify this idea, we measured the pH of tap water treated with the AM and observed a reduction of 2.0 pH units compared to untreated water (pH 5.7 and 7.7, respectively). Altogether this indicates that the AM treatment could be an important tool to reduce crop pH during FW programs and possible prevention of pathogen colonization.
IMPROVING QUALITY OF BROILER CARCASSES
1961
Candelario-Jalil et al., 2006). Thus, it was expected that the AM treatment lowered the allostatic load in broilers with a subsequent improvement in carcass quality. To determine the relationship between treatment effects and the amount of carcass defects, a factorial analysis of correspondence was carried out. For this analysis, a data matrix was constructed using treatment descriptors (AM vs. CON) and the observed unilateral and bilateral defects: bruises on legs, backs, pygostyles, breasts, necks, wings; skin scratches; broken bones; and total condemnations. This analysis revealed a strong association (inertia = 0.738) between treatments and carcass defects (P = 0.015; Figure 2). The factorial analysis of correspondence explained 57.66% of the variance within 2 axes, showing that the frequency of each carcass defect could be directly associated with the use of AM and the time of FW. Specifically, on this map, the distances between treatments and carcass defects reflect the level of statistical association. Thus, it is observed that the treatments positions on the map-land in different map-quadrants, indicating a weak association. Also, it is perceived that unilateral broken and bruised wings, and bruises on the back are strongly associated with CON treatments under 10 h FW. Moreover, bilateral bruises on the wings are strongly associated with 16 h FW in the CON group (Figure 2). These results indicate that the treatment with AM had a weak sta-
tistical association with carcass defects, indicating that water supplementation of AM could be useful to decrease carcass-processing defects.
Antemortem Evaluation In the present study, we also evaluated if AM treatment had an effect on animal welfare parameters. To accomplish this goal, the numbers of dead birds on arrival, panting birds, flapping birds, and head-lifting birds were estimated. We observed no effects (P ≥ 0.05, inertia 0.086; data not shown) on these animal welfare parameters in both commercial hybrid lines used; indicating that the AM could be safely used in poultry production.
CONCLUSIONS The present study reveals that the supplementation of an AM in drinking water effectively reduces crop pH, improves carcass-microbiological quality, and reduces carcass-processing defects in broiler chickens. All together this indicates that the use of an AM is a novel and inexpensive alternative to reduce the allostatic load in broilers.
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
Figure 2. Association of water treatments with carcass defects. Factorial correspondence analysis, explaining 57.66% of the variation within two axes (inertia = 0.738). Treatments consisted of tap water treated with an allostatic modulator (AM) or without [control (CON)] an AM. The AM and CON treatment were provided ad libitum, 48 h before the chickens (n = 57 to 73 per treatment) were sent to a commercial processing plant. Analyses were performed using 2 commercial hybrid lines (L1 and L2) treated with (AM) or without (CON) an AM under conventional (10 h) and prolonged (16 h) feed withdraw programs.
RUBIO-GARC´IA ET AL.
1962
ACKNOWLEDGMENTS This study was supported by a grant from Alta Tecnolog´ıa Industrial para la Salud Animal, Project UNAM- Alta Tecnolog´ıa Industrial para la Salud Animal Number 17549-1590-15-XI-05. The authors acknowledge the help provided by the students and staff of the Centro de Ense˜ nanza, Investigaci´ on y Extensi´ on en Producci´ on Av´ıcola, UNAM, during the execution of the study. Also, we thank H´ector Escalona from Universidad Aut´ onoma Metropolitana, Iztapalapa, M´exico for his kind advice in statistical analysis.
REFERENCES
Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015
¨ ¨ Ak¸sit, M., S. Yal¸cın, S. Ozkan, K. Metin, and D. Ozdemir. 2006. Effects of temperature during rearing and crating on stress parameters and meat quality of broilers. Poult. Sci. 85: 1867–1874. Avila, L. A. F., C. W. Canal, C. T. P. Salle, and H. L. Moraes. 2003. Effect of acidified drinking water on the recovery of Salmonella enteritidis from broiler crops. Rev. Bras. Cienc. Avic. 5:183–188. Bilgili, S. F. 1992. Electrical stunning of broilers–Basic concepts and carcass quality implications: A review. J. Appl. Poult. Res. 1:135– 146. Bilgili, S. F. 2001. Poultry meat inspection and grading. Pages 54– 58 in Poultry Meat Processing. Alan R. Sams, ed. Department of Poultry Science. Texas A&M University. CRC Press, Boca Raton, FL, United States. Borges, S. A., A. V. Fischer-da Silva, J. Ariki, D. M. Hooge, and K. R. Cummings. 2003. Dietary electrolyte balance for broiler chickens exposed to thermoneutral or heat-stress environments. Poult. Sci. 82:428–435. Borges, S. A., A. V. Fischer-da Silva, A. Majorka, D. M. Hooge, and K. R. Cummings. 2004. Physiological responses of broiler chickens to heat stress and dietary electrolyte balance (sodium plus potassium minus chloride, milliequivalents per kilogram). Poult. Sci. 83:1551–1558. Byrd, J. A., B. M. Hargis, D. J. Caldwell, R. H. Bailey, K. L. Herron, J. L. McReynolds, R. L. Brewer, R. C. Anderson, K. M. Bischoff, T. R. Callaway, and L. F. Kubena. 2001. Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on salmonella and campylobacter contamination of broilers. Poult. Sci. 80:278–283. Candelario-Jalil, E., R. S. Akundi, H. S. Bhatia, K. Lieb, K. Appel, E. Mu˜ noz, M. H¨ ull, and B. L. Fiebich. 2006. Ascorbic acid enhances the inhibitory effect of aspirin on neuronal cyclooxygenase-2-mediated prostaglandin E2 production. J. Neuroimmunol. 174:39–51. Demirok, E., G. Veluz, W. V. Stuyvenberg, M. P. Casta˜ neda, A. Byrd, and C. Z. Alvarado. 2013. Quality and safety of broiler meat in various chilling systems. Poult. Sci. 92: 1117–1126. Estevez, I. 2007. Density allowances for broilers: Where to set the limits? Poult. Sci. 86:1265–1272. Gross, W. B. 1988. Effect of environmental stress on the responses of ascorbic-acid-treated chickens to Escherichia coli challenge infection. Avian Dis. 32:432–436. Herring, G., and D. E. Gawlik. 2007. The role of stress proteins in the study of allostatic overload in birds: use and applicability to current studies in avian ecology. Scientific World J. 7: 1596–1602. Hinton, Jr. A., R. J. Buhr, and K. D. Ingram. 2000a. Physical, chemical, and microbiological changes in the crop of broiler chickens subjected to incremental feed withdrawal. Poult. Sci. 79:212–218. Hinton, Jr. A., R. J. Buhr, and K. D. Ingram. 2000b. Reduction of Salmonella in the crop of broiler chickens subjected to feed withdrawal. Poult. Sci. 79:1566–1570. Hinton, Jr. A, R. J. Buhr, and K. D. Ingram. 2002. Carbohydratenased cocktails that decrease the population of Salmonella and
Campylobacter in the crop of broiler chickens subjected to feed withdrawal. Poult. Sci. 81:780–784. Jayalakshmi, T., R. Kumararaj, T. Sivakumar, and T. V. Thanga. 2009. Carcass characteristics of commercial broilers reared under varying stocking densities. Tamilnadu J. Vet. Anim. Sci. 5:132– 135. Kannan, G., J. L. Heath, C. J. Wabeck, M. Souza, J. C. Howe, and J. A. Mench. 1997. Effects of crating and transport on stress on meat quality characteristics in broilers. Poult. Sci. 76: 523–529. Khassaf, M., A. McArdle, C. Esanu, A. Vasilaki, F. McArdle, R. D. Griffiths, D. A. Brodie, and M. J. Jackson. 2003. Effect of vitamin C suplements on antioxidant defence and stress protein in human lymphocytes and skeletal muscle. J. Physiol. 549:645–652. Korte, S. M., J. M. Koolhaas, J. C. Wingfield, and B. S. McEwen. 2005. The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade-off in health and disease. Neurosci. Biobehav. Rev. 29:3–38. doi:10.1016 /j.neubiorev.2004.08.009 Kun, Z., A. N. Uluocak, and M. Karaman. 2009. The influence of some factors on carcass defects during fattening period in broilers. Arch. Zootec. 58:117–120. McFarlane, J. M., S. E. Curtis, R. D. Shanks, and S. G. Carmer. 1989. Multiple concurrent stressors in chicks. 1. Effect on weight gain, feed intake and behavior. Poult. Sci. 68:501–509. McKee, J. S., and P. C. Harrison. 1995. Effects of supplemental ascorbic acid on the performance of broiler chickens exposed to multiple concurrent stressors. Poult. Sci. 74:1772–1785. McKee, J. S., P. C. Harrison, and G. L. Riskowski. 1997. Effects of supplemental ascorbic acid on the energy conversion of broiler chicks during heat stress and feed withdrawal. Poult. Sci. 76:1278– 1286. McNeal, W. D., D. L. Fletcher, and R. J. Buhr. 2003. Effects of stunning and decapitation on broiler activity during bleeding, blood loss, carcass and breast meat quality. Poult. Sci. 82:163– 168. Minton, J. E. 1994. Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. J Anim. Sci. 72:1891–1898. Northcutt, J. K. 2001. Preslaugther factors affecting poultry meat quality. Pages 5–18 in Poultry Meat Processing. Alan R. Sams, ed. Department of Poultry Science, Texas A&M University, CRC Press, Boca Raton, FL, United States. Northcutt, J., D. Smith, K. D. Ingram, A. Hinton, Jr., and M. Musgrove. 2007. Recovery of bacteria from broiler carcasses after spray washing with acidified electrolyzed water or sodium hypochlorite solutions. Poult. Sci. 86:2239–2244. Olanrewaju, H. A., J. P. Thaxton, W. A. Dozier, III, and S. L. Branton. 2007. Electrolyte diets, stress, and acid-base balance in broiler chickens. Poult. Sci. 486:1363–1371. ¨ Ozaslan, M., T. Aytekin, I. H. Kilic, A. I. Bozkurt, E. G¨ uld¨ ur, B. Cengiz, and C. Bagci. 2004. The effect of vitamin C supplementation on leukocyte counts and exercise performance. J. Exerc. Physiol. Online. 7:101–105. Rohleder, N. 2008. Preventing acute stress-induced inflammatory disinhibition by aspirin: What does it tell us about the mechanism? Brain Behav. Immun. 22:148–149. Rokyta, R., V. Holecek, I. Pek´ arkova, J. Krejcov´ a, J. Racek, L. Trefil, and A. Yamamotov´ a. 2003. Free radicals after painful stimulation are influenced by antioxidants and analgesics. Neuro Endocrinol Lett. 24:304–309. Romero, L. M., M. J. Dickens, and N. E. Cyr. 2009. The reactive scope model–A new model integrating homeostasis, allostasis and stress. Horm. Behav. 55:375–389. Rostango, M. H. 2009. Can stress in farm animals increase food safety risk?. Foodborne Pathog. Dis. 6:767–776. doi.10.1089/fpd.2009.0315 Savenije, B., E. Laambooij, M. A. Gerritzen, K. Venema, and J. Korf. 2002. Effects of feed deprivation and transport on preslaughter blood metabolites, early postmortem muscle metabolites, and meat quality. Poult. Sci. 81:699–708. Seyle, H., and C. Fortier. 1950. Adaptive reaction to stress. Proc. 29th Annual Meeting of the Association for Research in Nervous and Mental Disease. Baltimore, MD, United States.
IMPROVING QUALITY OF BROILER CARCASSES ˇ Skrbi´ c, Z., Z. Pavlovski, and M. Luki´c. 2009. Stocking density–Factor of production performance, quality and broiler welfare. Biotech. Anim. Husb. 25:359–372. Smith, D. P., and M. E. Berrang. 2006. Prevalence and numbers of bacteria in broiler crop and gizzard contents. Poult. Sci. 85:144– 147. Stewart, J. A. 2006. The detrimental effects of allostasis: Allostatic load as a measure of cumulative stress. J. Physiol. Anthropol. 25:133–145. Stilborn, H. L., G. C. Harris, Jr., W. G. Bottje, and P. W. Waldroup. 1988. Ascorbic acid and acetylsalicylic acid (aspirin) in the diet of broilers maintained under heat stress conditions. Poult. Sci. 67:1183–1187. The European Commission. 2000. The Welfare of Chickens Kept for Meat Production (Broilers). Report of the Scientific Committee on Animal Health and Animal Welfare. http://ec.europa.eu/food/fs/sc/scah/out39 en.pdf
1963
Tyler, P. J., and K. A. Cummins. 2003. Effect of dietary ascorbyl-2phosphate on immune function after transport to a feeding facility. J. Dairy. Sci. 86:622–629. USDA. 1998. Poultry Grading Manual. Agriculture Handbook No. 31. USDA Agricultural Marketing Services, Washington, DC. Vecerek, V., S. Grbalova, E. Voslarova, B. Janackova, and M. Malena. 2006. Effects of travel distance and the season of the year on death rates of broilers transported to poultry processing plants. Poult. Sci. 85:1881–1884. Whiting, T. L., M. E. Drain, and D. P. Rasali. 2007. Warm weather transport of broiler chickens in Manitoba. II. Truck management factors associated with death loss in transit to slaughter. Can. Vet. J. 48:148–154. Zulkifli, I., M. T. Che Norma, C. H. Chong, and T. C. Loh. 2000. Heterophil to lymphocyte ratio and tonic immobility reactions to preslaughter handling in broiler chickens treated with ascorbic acid. Poult. Sci. 79:402–406. Downloaded from http://ps.oxfordjournals.org/ at Northeastern University Libraries on November 14, 2015