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Relationship Between Pre-Slaughter Factors and Major Causes of Carcass Condemnation in a Broiler Slaughterhouse under Federal Inspection

ABSTRACT

This study aimed to investigate the relationship between pre-slaughter factors and major causes of total or partial carcass condemnation in a broiler slaughterhouse under federal inspection. Data on total and partial carcass condemnations between 2018 and 2020 were collected from 10 broiler farms supplying a slaughterhouse located in northern Paraná State, Brazil. The total sample comprised 2,562,642 birds. The pre-slaughter factors analyzed were age at slaughter, stocking density, weight at slaughter, feed conversion, and mortality.Associations between causes of condemnation and pre-slaughter factors were analyzed using a generalized linear model with negative binomial distribution, a generalized linear model with quasi-Poisson distribution, and a generalized linear mixed model with Poisson distribution. Total carcass condemnations were mostly due to repugnant appearance (48.67%) and arthritis (26.56%), whereas partial carcass condemnations were mainly due to arthritis (31.02%), bruising (27.97%), and myopathies (15.18%). Mean age and stocking density were the pre-slaughter factors that most contributed to increasing total and partial condemnation rates, indicating that reducing stocking density and age at slaughter might be important strategies for minimizing economic losses associated with carcass condemnation.

Keywords:
Arthritis; Carcass; Myopathy; Quality

INTRODUCTION

Chicken meat is widely consumed worldwide because of its high nutritional quality, easy accessibility, and reduced religious restrictions. In Brazil, per capita consumption reaches an average of 42.84 kg and chicken meat production holds great economic importance. In 2019, the country produced 13.245 million tonnes of chicken meat and had an export volume of 4.214 million tonnes, ranking as the world’s second largest producer and largest exporter (ABPA, 2021).

The quality of chicken meat produced in Brazil is guaranteed by the Federal Inspection Service, responsible fordeciding whether carcasses are suitable for human consumption through criteria defined and established by the Regulatory Requirements for Industrial and Sanitary Inspection of Products of Animal Origin (RIISPOA) (BRASIL, 2017Brasil. Ministério da Agricultura Pecuária e Abastecimento. 1998. Decreto n° 9.013, de 29 de março de 2017. Regulamenta a Lei n° 1.283, de dezembro de 1950, e a Lei n°7.889, de 23 de novembro de 1989, que dispõem sobre a inspeção industrial e sanitário de produtos de origem animal. Diário Oficial da República Federativa do Brasil, Brasília,DF; 2017.). Inspection includes ante- and post-mortem steps aimed at identifying animal carcasses that pose a risk to human health. In case of any abnormality, the carcass may be condemned as a whole or in part.

Total condemnation of poultry carcasses is mainly due to repugnant appearance, colibacillosis, contamination, airsacculitis, dehydration, and cachexia (Muchon et al., 2019Muchon JL, Garcia RG, Gandra ERS, Assunção ASA, Komiyama CM, Caldara FR, et al. Origin of broiler carcass condemnations. Revista Brasileira de Zootecnia 2019;48:e.20180249.; Souza et al., 2019Souza WF, Granjeiro MDB, Procópio DP. Analysis of the economic loss and the main causes of total condemnation of poultry carcasses under brazilian federal inspection between 2013 and 2017. Archives of Veterinary Science 2019;24(4):36-49.), whereas the major causes of partial condemnation include dermatosis, contamination, cellulitis, airsacculitis, and bruising/fracture (Mu-chon et al., 2019).Causes of condemnation are multifactorial.They may be related to production systems (type of farm, feed management, stocking density), intrinsic to the animal itself (strain, sex, age at slaughter), or associated with problems occurring during slaughter, such as contamination and excessive scalding.

Carcass condemnation represents an important cause of economic lossin the poultry sector. Therefore, it is important to investigate the factors associated with carcass condemnation in order to mitigate losses and support the development of strategies to minimize future occurrences.

In view of the above, this study aimed to assess the relationship between pre-slaughter factors and the major causes of total and partial carcass condemnation of broiler chickens in a commercial slaughterhouse under federal inspection.

MATERIAL AND METHODS

Data collection

Data were collected from a commercial slaughter-house located in northern Paraná State, Brazil. The slaughterhouse is licensed with the Brazilian Ministry of Agriculture, Livestock, and Food Supply (MAPA) and supervised by the Federal Inspection Service. The plant has a slaughter capacity of 220,000 birds per day.Data were collected from 10 chicken farms supplying the slaughterhouse from February 2018 to May 2020, totaling 110 batches and 2,562,642 birds.

The pre-slaughter factors analyzed were age at slaughter (days), weight at slaughter (kg), total mortality (calculated as the sum of mortality at the farm and during transport) (%), feed conversion, and stocking density (birds/m2), as described in Table 1.

Slaughtering was performed according to the standard procedures of the slaughterhouse. The steps were as follows: electric stunning, bleeding, scalding, plucking, evisceration, and chiller cooling.

Data on total and partial carcass condemnation were collected from broiler farms in accordance with MAPA regulatory criteria and Decree No. 9,013 of 2017 (BRASIL, 2017Brasil. Ministério da Agricultura Pecuária e Abastecimento. 1998. Decreto n° 9.013, de 29 de março de 2017. Regulamenta a Lei n° 1.283, de dezembro de 1950, e a Lei n°7.889, de 23 de novembro de 1989, que dispõem sobre a inspeção industrial e sanitário de produtos de origem animal. Diário Oficial da República Federativa do Brasil, Brasília,DF; 2017.). The causes of carcass condemnation were classified as abscess, airsacculitis, arthritis, repugnant appearance, cachexia, cellulitis, colibacillosis, contamination, bruising, dermatosis, dehydration, excessive scalding, delayed evisceration, fracture, poor bleeding, myopathy, salmonellosis, salpingitis, septicemia, andascitic syndrome.

Table 1
Pre-slaughter factors of broiler chickens from 10 commercial farms supplying a slaughterhouse under federal inspection in Paraná State, Brazil, between February 2018 and May 2020.

Data analysis

Total and partial carcass condemnation data were subjected to descriptive analysis. Results are presented as frequencies (percentages), calculated from the ratio of the number of condemnations for a specific cause to the total number of condemnations.

A generalized linear model with negative binomial distribution, a generalized linear model with quasi-Poisson distribution, and a generalized linear mixed model with Poisson distribution (Faraway, 2016Faraway JJ. Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. 2nd ed. New York: Chapman and Hall/CRC; 2016.) were used to assess associations between causes of carcass condemnation and the pre-slaughter factors described in Table 1. Analyses were performed using RStudio software version 1.1.456 (R Core Team, 2018).The regression coefficient of each pre-slaughter factor was calculated to measure its strength of association with the response variable (cause of condemnation).

RESULTS AND DISCUSSION

Of the 2,562,642 slaughtered birds, 13,604 were fully condemned (0.53%) and 252,918 were partially condemned (9.87%). Similar results were described by Jaguezeski et al. (2020Jaguezeski AM, Engelmann AM, Machado INR, Batti BPB. The effect of four commercial broiler hybrids and the season on occurrence of broiler condemnations in the abattoirs. Ciência Rural 2020;10(10):1-8.), who analyzed data from a slaughterhouse in western Paraná State from April 2015 to March 2016. The authors found that 0.41% of birds were fully condemned and 12.81% were partially condemned.

Of all condemnations (n = 266,522), 5.1% were total and 94.9% were partial. Partially condemned carcasses can still be used for human consumption, minimizing economic losses. Oliveira et al. (2016Oliveira AA, Andrade MA, Armendaris PM, Bueno PHS. Principais causas de condenação ao abate de aves em matadouros frigoríficos registrados no serviço brasileiro de inspeção federal entre 2006 e 2011. Ciência Animal Brasileira 2016;17(1):79-89.) assessed 1,612,647,133 carcasses condemned from 2006 to 2011 in Brazil and found that 85% were partially condemned and 15% were fully condemned.

As shown in Figure 1, the major causes of total condemnation were repugnant appearance, with 6,622 cases (48.67%), followed by arthritis, with 3,615 cases (26.56%), ascites, with 895 cases (6.84%), cachexia, with 781 cases (5.74%), excessive scalding, with 733 cases (5.39%), and poor bleeding, with 642 cases (4.72%).

Repugnant appearance was also the major cause of total condemnation in a study by Souza et al. (2019Souza WF, Granjeiro MDB, Procópio DP. Analysis of the economic loss and the main causes of total condemnation of poultry carcasses under brazilian federal inspection between 2013 and 2017. Archives of Veterinary Science 2019;24(4):36-49.), carried out from 2013 to 2017 in Brazil. Any change in carcass color, odor, or appearance, stemming from diseases, technopathies, or quality defects, can lead to condemnation for repugnant appearance (BRASIL, 2017Brasil. Ministério da Agricultura Pecuária e Abastecimento. 1998. Decreto n° 9.013, de 29 de março de 2017. Regulamenta a Lei n° 1.283, de dezembro de 1950, e a Lei n°7.889, de 23 de novembro de 1989, que dispõem sobre a inspeção industrial e sanitário de produtos de origem animal. Diário Oficial da República Federativa do Brasil, Brasília,DF; 2017.). Given the diversity of the causes of repugnant appearance, it is difficult to control this factor.

Figure 1
Most frequent causes of total carcass commendations (%) of broilers (n= 13,604) from 110 batches of a slaughterhouse under federal inspection in Paraná State, Brazil, between 2018 and 2020.

Arthritis, the second largest cause of total carcass condemnation, is a growing concern in the global poultry industry because it leads to economic losses and poses a risk to public health. The disease not only affects slaughterhouses but may also impair animal performance or lead to death, given that affected broilers cannot feed or drink water properly, being predisposed to other diseases (Assunção et al., 2018Assunção TRS, Palka APG, Pavoni DP. Reovirose aviária:um panorama. Revista de Educação Continuada em Medicina Veterinária e Zootecnia do CRMV-SP 2018;16(2):48-59.). Arthritis is difficult to control, as there are numerous infectious agents capable of causing the disease and individual and environmental factors that may contribute to disease onset, such as high weight gain, inadequate bed management, inadequate ventilation, high thermal amplitude, and severe winter conditions (Sellers, 2017Sellers HS. Current limitations in control of viral arthritis and tenosynovitis caused by avian reoviruses in commercial poultry. Veterinary Microbiology 2017; 206:152-6.; Marcon et al., 2019Marcon AV, Oliveira GF, Caldara FR, Garcia RG, Martins RA, Marcon A, et al. Bacteriological and Histopathological Evaluation of Articulations of Chickens Diagnosed with Arthritis. Brazilian Journal of Poultry Science 2019;21(2):1-4.).

The third cause of total condemnation was ascites (6.84%). Similar results were obtained by de Muchon et al. (2019Muchon JL, Garcia RG, Gandra ERS, Assunção ASA, Komiyama CM, Caldara FR, et al. Origin of broiler carcass condemnations. Revista Brasileira de Zootecnia 2019;48:e.20180249.), who found that the condition was responsible for 6.83% of condemnations between 2004 and 2014 in a slaughterhouse in Grande Dourados, Mato Grosso do Sul State. Genetic and environmental factors, such as strain (heavy broilers with metabolic overload), high thermal amplitude, and low temperatures contribute to ascites development, as they lead to hypoxia (Jaenisch et al., 2001Jaenisch FRF, Ávila VS, Mazzuco H, Rosa OS, Fiorentin L. Síndrome da hipertensão pulmonar:a ascite em frangos de corte [circular técnica]. Concórdia: Embrapa; 2001. p.1-16.; Rosário et al., 2004Rosário MF, Silva MAN, Coelho AAD. Savino VJM. Síndrome ascítica em frangos de corte: uma revisão sobre a fisiologia, avaliação e perspectivas. Ciência Rural 2004;34(6):1987-96.).

The following three causes of total condemnations had similar frequencies, namely cachexia (5.74%), excessive scalding (5.39%), and poor bleeding (4.72%). Carcasses affected by cachexia exhibit intense loss of muscle and fat (Rabaiolli et al., 2016Rabaiolli JF, Vicensi JB, Calasans MWM, Corazza J, Tedesco DC, Klein J, et al. Avaliação microbiológica de carcaças de frangos caquéticos. Anais da 3ª Semana do conhecimento, Universidade e Comunidade em Transformação; 2016. Passo Fundo: UFP; 2016. p.1-3.), caused by inadequate feed supply or diseases that affect organism functioning (BRASIL, 2017Brasil. Ministério da Agricultura Pecuária e Abastecimento. 1998. Decreto n° 9.013, de 29 de março de 2017. Regulamenta a Lei n° 1.283, de dezembro de 1950, e a Lei n°7.889, de 23 de novembro de 1989, que dispõem sobre a inspeção industrial e sanitário de produtos de origem animal. Diário Oficial da República Federativa do Brasil, Brasília,DF; 2017.). Excessive scalding produces multiple lesions resulting from high scalding time/temperature (BRASIL, 1998). Inadequate or incomplete bleeding is identified by reddish areas on chicken skin (Freitas, 2015Freitas LS. Causas de condenações post-mortem de frangos [monografia]. Porto Alegre (RS): Universidade Federal do Rio Grande do Sul; 2015.). Souza et al. (2019Souza WF, Granjeiro MDB, Procópio DP. Analysis of the economic loss and the main causes of total condemnation of poultry carcasses under brazilian federal inspection between 2013 and 2017. Archives of Veterinary Science 2019;24(4):36-49.) found that excessive scalding, cachexia, and poor bleeding were responsible for 9.77%, 6.63%, and 4.30%, respectively, of total condemnations in a slaughterhouse in Paraná State.

The major causes of partial condemnation were arthritis (31.02%, n = 78,454), followed by bruising (27.97%, n = 70,749), myopathy (15.18%, n = 38,403), fracture (11.11%, n = 28,088), and cellulitis (9.00%, n = 22,761)(Figure 2). Muchon et al. (2019Muchon JL, Garcia RG, Gandra ERS, Assunção ASA, Komiyama CM, Caldara FR, et al. Origin of broiler carcass condemnations. Revista Brasileira de Zootecnia 2019;48:e.20180249.) classified the causes of condemnation recordedin a Brazilian slaughterhouse into two groups: (i) pre-fasting condemnation rates, associated with the poultryfarm, and (ii) post-fasting condemnation rates, associated with the slaughterhouse. In the first category, the major causes for partial condemnation were dermatosis (40.23%), airsacculitis(27.75%), and cellulitis (29.69%), whereas, in the second category, the major causes were contamination (76.90%) and bruising/fracture (22.70%). Our results agree with these findings, given that cellulitis, bruising, and fracture were among the main causes of partial condemnation. According to Paschoal et al. (2012Paschoal EC, Otutumi LK, Silveira AP. Major reasons for condemnation in broiler slaughter in a slaughterhouse located in the northwest of Paraná, Brazil. Arquivo de Ciências Veterinárias e Zoologia da UNIPAR 2012;15(2):93-7.), bruising/fracture (54.38%) and cellulitis (13.66%) were the main causes of partial condemnation between January 2011 and October 2012 in a slaughterhouse in northwestern Paraná State.

Figure 2
Most frequent causes of partial carcass commendations (%) of broilers (n=252,918) from 110 batches of a slaughterhouse under federal inspection in Paraná State, Brazil, between 2018 and 2020.

Candido et al. (2021Candido MJS, Zanini SF, Ferreira MF, Araujo FAC, TeixeirA APM, Cipriano R.C, et al. Principais causas de condenações de carcaça de frango no Espírito Santo, Brazil. Semina - Ciências Agrárias 2021;42(3):112-4.) assessed slaughterhouses under federal inspection in Espírito Santo State and found that bruising was the major cause of partial condemnation. The authors also reported an increase in the occurrence of condemnation for myopathy, from 1.05% in 2018 to 4.77% in 2019. Myopathies are associated with rapid growth, a frequent occurrence in modern broilers, explaining the high frequency of these conditions in the majority of slaughterhouses in Brazil (Zanetti et al., 2018Zanetti MA, Tedesco D, Schneider T, Teixeira STF, Daroit L, Pilotto F, et al. Economic losses associated with Wooden Breast and White Striping in broilers. Semina - Ciências Agrárias 2018;39(2):887-92.).

Correlations between pre-slaughter factors (mean age, stocking density, mean body weight, feed conversion, and mortality) and the major causes of total condemnation are described in Table 2. Broiler age was correlated positively with cachexia and negatively with ascites, indicating that older age may increase condemnation for cachexia and decrease that for ascites. According to Duarte & Santana (2019Duarte PM, Santana VTP. Isolamento de Enterobactérias a partir de frangos de corte necropsiados: relato de caso. Colloquium Vitae 2019;11(3):79-84.), older animals are more susceptible to certain diseases and infections, which might be associated with condemnation for cachexia, given that the condition is caused by diseases such as colibacillosis (Duarte & Santana, 2019) and Marek’s disease (Tambiev et al., 2021). The decrease in condemnation for ascites with increasing age (p<0.05) might be due to the fact that ascites occurs mainly in birds aged 8 to 21 days. As affected birds grow older, they are more likely to be discarded as refuse or may even die as a result of the disease (Jaenisch et al., 2001Jaenisch FRF, Ávila VS, Mazzuco H, Rosa OS, Fiorentin L. Síndrome da hipertensão pulmonar:a ascite em frangos de corte [circular técnica]. Concórdia: Embrapa; 2001. p.1-16.; Rosário et al., 2004Rosário MF, Silva MAN, Coelho AAD. Savino VJM. Síndrome ascítica em frangos de corte: uma revisão sobre a fisiologia, avaliação e perspectivas. Ciência Rural 2004;34(6):1987-96.).

Table 2
Relationships between pre-slaughter factors and major causes of total carcass condemnation of broilers from 110 batches of a slaughterhouse under federal inspection in Paraná State, Brazil, between 2018 and 2020.

High stocking density was associated (p<0.05) with increased condemnation for repugnant appearance and ascites as well as withoverall total condemnation. Stocking density is a crucial factor in the poultry industry; excessively high densities may affect animal health, yield (Bilal et al., 2021Bilal RM, Hassan F, Farag MR, Nasir TA, Ragni M, Mahgoub HAM, Alagawany M. Thermal stress and high stocking densities in poultry farms:Potential effects and mitigation strategies. Journal of Thermal Biology 2021;11-2.), biochemical parameters, reproductive performance (Ying et al., 2021Ying S, Dai Z, Xi Y, Li M, Yan J, YU J, et al. Metabolomic evaluation of sérum metabolites of geese reared at different stocking densities. British Poultry Science 2021;62(2):304-9.), condemnation rates, and mortality (Bergeron et al., 2020Bergeron S, Pouliot E, Doyon M. Commercial poultry production stocking density influence on bird health and performance indicators. Animals 2020;10(8):1-8.), thereby leading to economic losses. It is difficult to establishthe optimal stocking density, given that this quantitative measure depends on qualitative factors, such as environmental and sanitary conditions. Ascitic syndrome is directly related to hypoxia, and several factors may reduce oxygen availability, including respiratory problems and poor air quality (Jaenisch et al., 2001Jaenisch FRF, Ávila VS, Mazzuco H, Rosa OS, Fiorentin L. Síndrome da hipertensão pulmonar:a ascite em frangos de corte [circular técnica]. Concórdia: Embrapa; 2001. p.1-16.; Rosário et al., 2004Rosário MF, Silva MAN, Coelho AAD. Savino VJM. Síndrome ascítica em frangos de corte: uma revisão sobre a fisiologia, avaliação e perspectivas. Ciência Rural 2004;34(6):1987-96.; Biswas, 2019Biswas A. Pulmonary hypertension syndrome in broiler chickens:a review. Veterinarski Arhiv Zagrebe 2019;89(5):723-34.) stemming from high stocking densities.

High body weight was also associated with increased condemnation (p<0.05) for ascites (Table 2), probably related to excessive oxygen expenditure by metabolic overload resulting from weight gain (Jaenisch et al., 2001Jaenisch FRF, Ávila VS, Mazzuco H, Rosa OS, Fiorentin L. Síndrome da hipertensão pulmonar:a ascite em frangos de corte [circular técnica]. Concórdia: Embrapa; 2001. p.1-16.; Rosário et al., 2004Rosário MF, Silva MAN, Coelho AAD. Savino VJM. Síndrome ascítica em frangos de corte: uma revisão sobre a fisiologia, avaliação e perspectivas. Ciência Rural 2004;34(6):1987-96.; Biswas, 2019Biswas A. Pulmonary hypertension syndrome in broiler chickens:a review. Veterinarski Arhiv Zagrebe 2019;89(5):723-34.). Contrary to the expected, feed conversion was positively associated (p<0.05) with condemnation for ascites. Hasani et al. (2017Hasani A, Bouyeh M, Rahati M, Seidavi A, Makovicky P, Laudadio V, et al. Which is the best alternative for ascites syndrome prevention in broiler chickens? Effect of feed form and rearing temperature conditions. Journal of Applied Animal Research 2017;46(1):392-6.) and Das & Deka (2019Das S, Deka P. Ascites syndrome (Water belly) in broilers and its management. Journal of Entomology and Zoology Studies 2019;7(6):388-90.) described ascitic syndrome as a serious disease of fast-growing chickens. Several factors can contribute to the development of the syndrome, namely sex, thermal amplitude, time of year, climate, respiratory problems, and air quality, which were not addressed in this study.

Mortality was associated with condemnation for poor bleeding (Table 2). It is hypothesized that blood loss might be impaired in unhealthy or stressed animals during bleeding procedures at the slaughterhouse.

Table 3 shows the correlations between pre-slaughter factors (mean age, stocking density, mean body weight, feed conversion, and mortality) and major causes of partial condemnation. Age was associated with increased condemnation for arthritis (p<0.05). In fact, according to Kieronczyk et al. (2017Kieronczyk B, Rawski M, Jozefiak D, Swiatkiewicz S. Infectious and non-infectious factors associated with leg disorders in poultry - a review. Annals of Animal Science 2017;17(3):645-69.), aging has a major impact on skeleton development and joint problems in chickens.

Table 3
Relationships between pre-slaughter factors and major causes of partial carcass condemnation of broilers from 110 batches of a slaughterhouse under federal inspection in Paraná State, Brazil, between 2018 and 2020.

Stocking density was associated with increased (p<0.05) partial condemnation for abscess, arthritis, bruising, dermatosis, fracture, and ascites. High stocking densities are associated with animal welfare problems (Avilés-Esquivel et al., 2018Avilés-Esquivel DF, Montero MA, Zurita-Vásquez H, Barros-Rodríguez M. Animal welfare and poultry productivity, a short review. Tropical and Subtropical Agroecosystems 2018;21(1):114-23.), which may culminate in bed compaction, increased microbial load, and increased humidity, factors associated with the onset of arthritis, dermatosis, and ascites. It is also noteworthy that arthritis was the major cause of partial condemnation (Figure 2). Therefore, it is important to reduce stocking density to improve animal welfare and minimize losses caused by condemnation (Bergeron et al., 2020Bergeron S, Pouliot E, Doyon M. Commercial poultry production stocking density influence on bird health and performance indicators. Animals 2020;10(8):1-8.).

Mean body weight did not influence (p>0.05) partial condemnation rates. However, worstfeed conversion led to a reduction (p<0.05) in partial condemnation for arthritis, contamination, bruising, and myopathy. Arthritis is an inflammatory process that leads to reduced feed intake, thereby affecting feed conversion, even when related parameters, such as weight gain, are low (Assunção et al., 2018Assunção TRS, Palka APG, Pavoni DP. Reovirose aviária:um panorama. Revista de Educação Continuada em Medicina Veterinária e Zootecnia do CRMV-SP 2018;16(2):48-59.). Genetic selection for improved feed conversion might be associated with the occurrence of diseases, quality defects (Zanetti et al., 2018Zanetti MA, Tedesco D, Schneider T, Teixeira STF, Daroit L, Pilotto F, et al. Economic losses associated with Wooden Breast and White Striping in broilers. Semina - Ciências Agrárias 2018;39(2):887-92.; Granquist et al., 2019Granquist EG, Vasdal G,Jong IC, Moe RO. Lameness and its relationship with health and production measures in broiler chickens. The International Journal of Animal Biosciences 2019;13(10):2365-72.), and rapid growth (Soglia et al., 2018Soglia F, Mazzoni M, Petracci M. Spotlight on avian pathology:current growth-related breast meat abnormalities in broilers. Avian Pathology 2018;489(1):1-3.; Zanetti et al., 2018), particularly in high-yielding strains (Assis et al., 2019Assis BV, Sabino LFS, Silva L, Fontes RA. Prevalência de miopatia dorsal e miopatia peitoral profunda no abate de frangos em um abatedouro frigorífico localizado em Minas Gerais. Anais do Fórum Acadêmico da Faculdade Vértice; 2019; Matipó, MG. Brasil. p.1-4.), thereby explaining the reduction in condemnation for contamination, bruising, and myopathies.

Total mortality was positively associated (p<0.05) with partial condemnation for contamination, myopathy, and ascites. Total mortality is multifactorial. Cadmus et al. (2019Cadmus KJ, Mete A, Harris M, Anderson D, Davison S, Sato Y, et al. Causes of mortality in backyard poultry in eight states in the United States. Journal of Veterinary Diagnostic Investigation 2019;31(3):318-26.) observed that the major causes of mortality in chickens in the United States of America from 2015 to 2017 were neoplastic and lymphoproliferative diseases, followed by infectious and non-infectious diseases. Thofner et al. (2019Thofner ICN, Poulsen LL, Bisgaard M, Christensen H, Olsen RH, Christensen JP. Longitudinal study on causes of mortality in danish broiler breeders. Avian Diseases 2019;63(3):400-10.), in analyzing four batches in Denmark, found that 55% of birds were killed by infectious diseases, 41% by non-infectious diseases, and 4% by unknown causes. Furthermore, the authors observed a peak in mortality at 40-49 weeks of age. Brochu et al. (2019Brochu NM, Guerin MT, Varga C, Lillie BN, Brash ML, Susta L. A two-year prospective study of small poultry flocks in Ontario, Canadá, part 2:causes of mobidity and mortality. Journal of Veterinary Diagnostic Investigation 2019;31(3):336-42.) described that the major cause of mortality over a 2-year period (October 2015 to September 2017) in Ontario was infectious diseases, mainly respiratory diseases and Marek’s disease. It is possible that birds from farms with high mortality rates may be carriers of infectious or non-infectious diseases, which would explain the increase in condemnation for contamination.

Of the pre-slaughter factors assessed here, stocking density was associated with the largest number of condemnation causes, including repugnant appearance (first cause of total condemnation), arthritis (second cause of total condemnation), bruising, and fracture (second and fourth cause of total condemnation, respectively), demonstrating the importance of controlling this parameter to minimize economic lossesin poultry production.

CONCLUSION

Total condemnation was mainly due to repugnant appearance (48.67%) and arthritis (26.56%), and partial condemnation was mainly caused by arthritis (31.02%), bruising (27.97%), and myopathy (15.18%). Broiler age and stocking density were the pre-slaughter factors that most contributed to total and partial condemnations. Thus, a reduction in stocking density and age at slaughter might reduce economic losses associated with condemnation.

REFERENCES

  • ABPA - Associação Brasileira de Proteína Animal. Relatórios ABPA. São Paulo; 2021 [cited 2022 Dec 19]. Available from: http://abpa-br.com.br/setores/avicultura/publicacoes/relatorios-anuais
    » http://abpa-br.com.br/setores/avicultura/publicacoes/relatorios-anuais
  • Assis BV, Sabino LFS, Silva L, Fontes RA. Prevalência de miopatia dorsal e miopatia peitoral profunda no abate de frangos em um abatedouro frigorífico localizado em Minas Gerais. Anais do Fórum Acadêmico da Faculdade Vértice; 2019; Matipó, MG. Brasil. p.1-4.
  • Assunção TRS, Palka APG, Pavoni DP. Reovirose aviária:um panorama. Revista de Educação Continuada em Medicina Veterinária e Zootecnia do CRMV-SP 2018;16(2):48-59.
  • Avilés-Esquivel DF, Montero MA, Zurita-Vásquez H, Barros-Rodríguez M. Animal welfare and poultry productivity, a short review. Tropical and Subtropical Agroecosystems 2018;21(1):114-23.
  • Bergeron S, Pouliot E, Doyon M. Commercial poultry production stocking density influence on bird health and performance indicators. Animals 2020;10(8):1-8.
  • Bilal RM, Hassan F, Farag MR, Nasir TA, Ragni M, Mahgoub HAM, Alagawany M. Thermal stress and high stocking densities in poultry farms:Potential effects and mitigation strategies. Journal of Thermal Biology 2021;11-2.
  • Biswas A. Pulmonary hypertension syndrome in broiler chickens:a review. Veterinarski Arhiv Zagrebe 2019;89(5):723-34.
  • Brasil. Ministério da Agricultura Pecuária e Abastecimento. 1998. Decreto n° 9.013, de 29 de março de 2017. Regulamenta a Lei n° 1.283, de dezembro de 1950, e a Lei n°7.889, de 23 de novembro de 1989, que dispõem sobre a inspeção industrial e sanitário de produtos de origem animal. Diário Oficial da República Federativa do Brasil, Brasília,DF; 2017.
  • Brasil. Ministério da Agricultura Pecuária e Abastecimento 1998. Portaria n°210, de 10 de novembro de 1998. Aprova o Regulamento Técnico da Inspeção Tecnológia e Higiênico-Sanitária de Carne de Aves. Diário Oficial da República Federativa do Brasil, Brasília,DF; 1998.
  • Brochu NM, Guerin MT, Varga C, Lillie BN, Brash ML, Susta L. A two-year prospective study of small poultry flocks in Ontario, Canadá, part 2:causes of mobidity and mortality. Journal of Veterinary Diagnostic Investigation 2019;31(3):336-42.
  • Cadmus KJ, Mete A, Harris M, Anderson D, Davison S, Sato Y, et al. Causes of mortality in backyard poultry in eight states in the United States. Journal of Veterinary Diagnostic Investigation 2019;31(3):318-26.
  • Candido MJS, Zanini SF, Ferreira MF, Araujo FAC, TeixeirA APM, Cipriano R.C, et al. Principais causas de condenações de carcaça de frango no Espírito Santo, Brazil. Semina - Ciências Agrárias 2021;42(3):112-4.
  • Das S, Deka P. Ascites syndrome (Water belly) in broilers and its management. Journal of Entomology and Zoology Studies 2019;7(6):388-90.
  • Duarte PM, Santana VTP. Isolamento de Enterobactérias a partir de frangos de corte necropsiados: relato de caso. Colloquium Vitae 2019;11(3):79-84.
  • Faraway JJ. Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. 2nd ed. New York: Chapman and Hall/CRC; 2016.
  • Freitas LS. Causas de condenações post-mortem de frangos [monografia]. Porto Alegre (RS): Universidade Federal do Rio Grande do Sul; 2015.
  • Granquist EG, Vasdal G,Jong IC, Moe RO. Lameness and its relationship with health and production measures in broiler chickens. The International Journal of Animal Biosciences 2019;13(10):2365-72.
  • Hasani A, Bouyeh M, Rahati M, Seidavi A, Makovicky P, Laudadio V, et al. Which is the best alternative for ascites syndrome prevention in broiler chickens? Effect of feed form and rearing temperature conditions. Journal of Applied Animal Research 2017;46(1):392-6.
  • Jaenisch FRF, Ávila VS, Mazzuco H, Rosa OS, Fiorentin L. Síndrome da hipertensão pulmonar:a ascite em frangos de corte [circular técnica]. Concórdia: Embrapa; 2001. p.1-16.
  • Jaguezeski AM, Engelmann AM, Machado INR, Batti BPB. The effect of four commercial broiler hybrids and the season on occurrence of broiler condemnations in the abattoirs. Ciência Rural 2020;10(10):1-8.
  • Kieronczyk B, Rawski M, Jozefiak D, Swiatkiewicz S. Infectious and non-infectious factors associated with leg disorders in poultry - a review. Annals of Animal Science 2017;17(3):645-69.
  • Marcon AV, Oliveira GF, Caldara FR, Garcia RG, Martins RA, Marcon A, et al. Bacteriological and Histopathological Evaluation of Articulations of Chickens Diagnosed with Arthritis. Brazilian Journal of Poultry Science 2019;21(2):1-4.
  • Muchon JL, Garcia RG, Gandra ERS, Assunção ASA, Komiyama CM, Caldara FR, et al. Origin of broiler carcass condemnations. Revista Brasileira de Zootecnia 2019;48:e.20180249.
  • Oliveira AA, Andrade MA, Armendaris PM, Bueno PHS. Principais causas de condenação ao abate de aves em matadouros frigoríficos registrados no serviço brasileiro de inspeção federal entre 2006 e 2011. Ciência Animal Brasileira 2016;17(1):79-89.
  • Paschoal EC, Otutumi LK, Silveira AP. Major reasons for condemnation in broiler slaughter in a slaughterhouse located in the northwest of Paraná, Brazil. Arquivo de Ciências Veterinárias e Zoologia da UNIPAR 2012;15(2):93-7.
  • R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018.
  • Rabaiolli JF, Vicensi JB, Calasans MWM, Corazza J, Tedesco DC, Klein J, et al. Avaliação microbiológica de carcaças de frangos caquéticos. Anais da 3ª Semana do conhecimento, Universidade e Comunidade em Transformação; 2016. Passo Fundo: UFP; 2016. p.1-3.
  • Rosário MF, Silva MAN, Coelho AAD. Savino VJM. Síndrome ascítica em frangos de corte: uma revisão sobre a fisiologia, avaliação e perspectivas. Ciência Rural 2004;34(6):1987-96.
  • Sellers HS. Current limitations in control of viral arthritis and tenosynovitis caused by avian reoviruses in commercial poultry. Veterinary Microbiology 2017; 206:152-6.
  • Soglia F, Mazzoni M, Petracci M. Spotlight on avian pathology:current growth-related breast meat abnormalities in broilers. Avian Pathology 2018;489(1):1-3.
  • Souza WF, Granjeiro MDB, Procópio DP. Analysis of the economic loss and the main causes of total condemnation of poultry carcasses under brazilian federal inspection between 2013 and 2017. Archives of Veterinary Science 2019;24(4):36-49.
  • Tambiev T, Tazayan A, Fedorov V, Gak Y, Derezina T, Avetisyan D. Features of the manifestation of marek's disease in poultry farms of the Rostov region, Russian Federation. Proceedings of the Conference DonAGRO: International Research Conference on Challenges and Advances in Farming, Food Manufacturing, Agricultural Research and Education; 2020 Jun 17-19; Rajon (RU): Persianovskiy: Don State Agrarian University; 2021. p.601-610.
  • Thofner ICN, Poulsen LL, Bisgaard M, Christensen H, Olsen RH, Christensen JP. Longitudinal study on causes of mortality in danish broiler breeders. Avian Diseases 2019;63(3):400-10.
  • Ying S, Dai Z, Xi Y, Li M, Yan J, YU J, et al. Metabolomic evaluation of sérum metabolites of geese reared at different stocking densities. British Poultry Science 2021;62(2):304-9.
  • Zanetti MA, Tedesco D, Schneider T, Teixeira STF, Daroit L, Pilotto F, et al. Economic losses associated with Wooden Breast and White Striping in broilers. Semina - Ciências Agrárias 2018;39(2):887-92.

Publication Dates

  • Publication in this collection
    06 Jan 2023
  • Date of issue
    2023

History

  • Received
    27 Apr 2022
  • Accepted
    18 Oct 2022
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