Salmonella spp. in non-edible animal products intended for the preparation of feed (meal) for industrial poultry feed




Salmonelosis; One Health; Food Safety; Food Technology; Non-edible by-products.


Non-edible by-products of animal origin are slaughter waste from slaughter animals that after processing give rise to animal meal which in turn is used as ingredients in the preparation of animal feed such as farm animals. Although this practice has its advantages in reducing environmental impact and meeting the nutritional needs of animals, it can serve as a vehicle for microorganisms such as Salmonella spp. Since food can play an important role in the dissemination of pathogens in the poultry production chain through feeding, the objective of the present study was to investigate the presence of Salmonella spp. samples of non-edible flours of animal origin used in the formulation of feed and also of feed produced from these by-products in slaughterhouses received from Bahia and Pernambuco states, Brazil and that are used in the industrial poultry farms of these States. Out of 649 samples of animal origin flours and feed were analyzed, of which 110 (16.9%) presented Salmonella spp. Statistical analysis, through descriptive analysis and Pearson’s chi-squase association test (X2) showed an association between the presence of Salmonella spp. and the different  types of inedible foods analyzed (p<0.05).This contamination in the analyzed samples indicates failure in the microbiological control during and/or after processing of animal origin flours, making them the sources of pathogen dissemination in the poultry chain.


Abebe, E., Gugsa, G., & Ahmed, M. (2020). Review on major food-borne zoonotic bacterial pathogens. Journal of tropical medicine, 2020. 10.1155/2020/4674235.

Ahmed. S., Dávila, J. D., Allen, A., Haklay, M., Tacoli, C., & Fèvre, E. M. (2019). Does urbanization make emergence of zoonosis more likely? Evidence, myths and gaps. Environment and urbanization, 31(2), 443-460. 10.1177/0956247819866124.

Boari, C. A; Alves, M. P; Tebaldi, V. M. R.; Savian, T. V., & Piccoli, R. H. (2009). Formação de biofilme em aço inoxidável por Aeromonas hydrophila e Staphylococcus aureus usando leite e diferentes condições de cultivo. Ciência e Tecnologia de Alimentos, 299(4), 886-895.

Brasil (2008) Ministério da Agricultura, Pecuária e Abastecimento. Regulamento Técnico da Inspeção Higiênico Sanitária e Tecnológica do Processamento de Resíduos de Animais e o Modelo de Documento de Transporte de Resíduos Animais. Instrução Normativa nº 34, de 28 de maio de 2008. Retrieved december 21, 2018. from

Brasil (2020) Ministério da Agricultura, Pecuária e Abastecimento. Secretaria de Defesa Agropecuária. Departamento de Inspeção de Produtos de Origem Animal. Regulamento da Inspeção Industrial e Sanitária de Produtos de Origem Animal. Decreto nº. 10.468, de 18 de agosto de 2020. Retrieved november 18, 2020. From

Byrd, A. L., Belkaid, Y., & Segre, J. A. (2018). The human skin microbiome. Nature Reviews Microbiology, 16(3), 143-155. 10.1038/nrmicro.2017.157.

Cebrián, G., Condón, S., & Mañas, P. (2017). Physiology of the inactivation of vegetative bacteria by thermal treatments: mode of action, influence of environmental factors and inactivation kinetics. Foods, 6(12), 107. 10.3390/foods6120107.

Chen, H. M., Wang, Y., Su, L. H., & Chiu, C. H. (2013). Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatrics & Neonatology. 54, 147-152. 10.1016/j.pedneo.2013.01.010.

Cox, N. A., Frye, J. G., McMahon, W., Jackson, C. R., Richardson, J., Cosby, D. E., Mead, G., & Doyle, M. P. (2015). “Salmonella”, Compendium of Methods for the Microbiological Examination of Foods. Washington: American Public Health Association.

Deen, J., Von Seidlein, L., Andersen, F., Elle, N., White, N. J., & Lubell, Y. (2012). Community-acquired bacterial bloodstream infections in developing countries in south and southeast Asia: a systematic review. The Lancet infectious diseases. 12, 480-487.

De Freitas Neto, O. C.; Penha Filho, R. A. C., Barrow, P., & Berchieri Junior, A. (2010). Sources of human non-typhoid salmonellosis: a review. Brazilian Journal of Poultry Science. 12 (1), 01-11.

De Jong, H. K., Parry, C. M., Van, Der Poll, T., & Wiersinga, W. J. (2012). Host–pathogen interaction in invasive salmonellosis. PLOS Pathogens. 8 (10), e1002933. Retrieved Juy 7, 2021, from

Ebling, P. D., Ribeiro, A.M.L., Trevizan, L., da Silva, I. C. M. & Kessler, A. D. M. & Rubin, L. L. (2013). Effect of different dietary concentrations of amino acids on the performance of two different broiler strains. Brazilian Journal of Poultry Science, 15, 339-346.

Edmonds-Wilson, S. L., Nurinova; N. I.; Zapka, C. A., Fierer, N., & Wilson, M. (2015). Review of human hand microbiome research. Journal of dermatological science, 80(1), 3-12.

Ehuwa, O., Jaiswal, A. K., & Jaiswal, S. (2021). Salmonella, Food Safety and Food Handling Practices. Foods, 10(5), 907. 10.3390/foods10050907.

Eng, S. K., Pusparajah, P., Ab Mutalib, N. S., Ser, H. L., Chan, K. G., & Lee, L. H. (2015). Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Frontiers in Life Science, 8(3), 284-293. 10.1080/21553769.2015.1051243.

Finn, S., Condell, O., McClure, P., Amézquita, A., & Fanning, S. (2013). Mechanisms of survival, responses and sources of Salmonella in low-moisture environments. Frontiers in microbiology, 4, 331.doi:10.3389/fmicb.2013.00331.

Fornefeld, E., Schierstaedt, J., Jechalke, S., Grosch, R. Smalla, K., & Schikora, A. (2017). Interaction between Salmonella and plants: potential hosts and vectors for human infection. Current Topics in Salmonella and Salmonellosis, 171-191. 10.5772/67061.

Franke-Whittle, I. H.& Insam, H. (2013) Treatment alternatives of slaughterhouse wastes, and their effect on the inactivation of different pathogens: A review. Critical reviews in microbiology. 39 (2), 139-151.

Friedman, C. R., Torigian, C., Shillam, P. J., Hoffman, R. E., Heltze, D., Beebe, J. L., Malcolm, G., DeWitt, W. E. Hutwagner, L., & Griffin, P. M. (1998). An outbreak of salmonellosis among children attending a reptile exhibit at a zoo. The Journal of pediatrics. 132: 802-807. 10.1016/S0022-3476(98)70307-5.

Gal-Mor, O., Boyle, E. C., & Grassl, G.A. (2014). Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Frontiers in microbiology, 5: 391.10.3389/fmicb.2014.00391.

Gandolfi, C. S., & Ramos, M. I. L. (2002) Salmonella sp. em farinhas de origem animal utilizadas na elaboração de rações para aves. Revista Higiene Alimentar, 16 (102/103), 112-116.

Garcia, B. C. B., Dimasupil, M. A. Z., Vital, P. G., Widmer, K. W., & Rivera, W. L. (2015). Fecal contamination in irrigation water and microbial quality of vegetable primary production in urban farms of Metro Manila, Philippines. Journal of Environmental Science and Health, Part B, 50(10), 734-743. 10.1080/03601234.2015.1048107.

Ha, J. S., Seo, K. W., Kim, Y. B., Kang, M. S., Song, C. S., & Lee, Y. J. (2018). Prevalence and characterization of Salmonella in two integrated broiler operations in Korea. Irish veterinary journal, 71(1), 1-9. 10.1186/s13620-018-0114-4.

Harvey, R. R., Friedman, C. R., Crim, S. M., Judd, M., Barrett, K. A., Tolar, B., Folster, J. P., Griffin, P. M., & Brown, A. C. (2017) Epidemiology of Salmonella enterica serotype Dublin infections among humans, United States, 1968–2013. Emerging infectious diseases, 23(9), 1493. 10.3201/eid2309.170136.

Hoelzer, K., Switt, A. I. M., & Wiedmann, M. (2011) Animal contact as a source of human non-typhoidal salmonellosis. Veterinary research, 42(1), 1-28. Retrieved October 26, 2021, from

Hohmann, E. L. (2001). Nontyphoidal salmonellosis. Clinical Infectious Diseases, 32 (2), 263-269. 10.1086/318457.

Issenhuth-Jeanjean, S., Roggentin, P., Mikoleit, M., Guibourdenche, M., De Pinna, E., Nair, S., & Weill, F. X. (2014). Supplement 2008–2010 (no. 48) to the White–Kauffmann–Le Minor scheme. Research in microbiology, 165 (7), 526-530. 10.1016/j.resmic.2014.07.004.

Jones, F.T. (2011). A review of practical Salmonella control measures in animal feed. Journal of Applied Poultry Research, 20(1), 102-113. 10.3382/japr.2010-00281.

Kagirita, A. A., Baguma, A., Owalla, T. J., Bazira, J., & Majalija, S. (2017). Molecular Characterization of Salmonella from Human and Animal Origins in Uganda. International journal of bacteriology. 2017. 10.1155/2017/4604789.

Leiva, A., Granados-Chinchilla, F., Redondo-Solano, M., Arrieta-González, M., Pineda-Salazar, E., & Molina, A. (2018). Characterization of the animal by-product meal industry in Costa Rica: Manufacturing practices through the production chain and food safety. Poultry science, 97(6), 2159-2169. 10.3382/ps/pey058.

Li, S., He, Y., Mann, D. A., & Deng, X. (2021). Global spread of Salmonella Enteritidis via centralized sourcing and international trade of poultry breeding stocks. Nature communications, 12(1), 1-12. 10.1038/s41467-021-25319-7.

Liu, H., Whitehouse, C. A., & Li, B. (2018a). Presence and persistence of Salmonella in water: the impact on microbial quality of water and food safety. Frontiers in Public Health, 6, 159.

Liu, S., Tang, J., Tadapaneni, R. K., Yang, R., & Zhu, M. J. (2018b). Exponentially increased thermal resistance of Salmonella spp. and Enterococcus faecium at reduced water activity. Appl. Environ. Microbiol. 84 (8), e02742-17. 10.1128/AEM.02742-17.

Loureiro, K. D. C., Haese, D., Kill, J. L., Pires, A. F., Fernandes, D. R., Colnago, G. L., Lucas, W., & Gama, G. O. (2017). Ingredients derived from the slaughter of bovines in dog food. Ciência Rural, 47: 06, e20150778.10.1590/0103-8478cr20150778.

Malav, O. P., Birla, R., Virk, K. S., Sandhu, H. S., Mehta, N., Kumar, P., & Wagh, R.V. (2018). Safe Disposal of Slaughter House Waste. Safe Disposal of Slaughter House Waste. Appro Poult Dairy & Vet Sci. 2(4). APDV.000542. 10.31031/APDV.2018.02.000542.

Meeker, D. L. (2009). North American Rendering: processing high quality protein and fats for feed. Revista Brasileira de Zootecnia, 38, SPE, 432-440.

Neitzke, D. C., Roza, C. R., Weber, F. H. (2017). Segurança dos alimentos: contaminação por Salmonella spp. no abate de suínos. Brazilian Journal of Food Technology, 20, e2015063. 10.1590/1981-6723.6315.

Osowski, G. V., Baron, L. F., Coldebella, A., Fonseca, F. N., Mota, S. C. A., Degenhardt, R., Duarte, S. C. (2019). Comparative study of egg contamination with Salmonella Heidelberg and Salmonella Typhimurium. Brazilian Journal of Veterinary Research and Animal Science, 56(1), e150479-e150479. doi 10.11606/issn.1678-4456.bjvras.2019.150479.

Reij, M. W., & Den Aantrekker, E. D.; ILSI Europe Risk Analysis in Microbiology Task Force (2004). Recontamination as a source of pathogens in processed foods. International Journal of Food Microbiology. 91(1),1-11. 10.1016/S0168-1605(03)00295-2.

Sapkota, A. R., Kinney, E.L., George, A., Hulet, R. M., Cruz-Cano, R., Schwab, K. J., & Joseph, S. W. (2014). Lower prevalence of antibiotic-resistant Salmonella on large-scale US conventional poultry farms that transitioned to organic practices. Science of the Total Environment, 476, 387-392. 10.1016/j.scitotenv.2013.12.005.

Shah, M. K., Bradshaw, R., Nyarko, E., Handy, E. T., East, C., Millner, P. D., Bergholz, T. M., & Sharma, M. (2019) Salmonella enterica in soils amended with heat-treated poultry pellets survived longer than bacteria in unamended soils and more readily transferred to and persisted on spinach. Applied and environmental microbiology, 85(10), e00334-19. 10.1128/AEM.00334-19.

Steenackers, H., Hermans, K., Vanderleyden, J., & De Keersmaecker, S. C. (2012). Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Research International, 45(2), 502-53. 10.1016/j.foodres.2011.01.038.

Thyagarajan, D., Barathi, M., & Sakthivadivu, R. (2013) Scope of poultry waste utilization. IOSR Journal of Agriculture and Veterinary Sciences. 6(5), 29-35.

Touchan, F., Hall, J. D., & Lee, R.V. (2009). Typhoid fever during pregnancy: case report and review. Obstetric medicine. 2(4), 161-163. 10.1258/om.2009.090020.

Ulrich, N., Nagler, K., Laue, M., Cockell, C. S., Setlow, P., & Moeller, R. (2018). Experimental studies addressing the longevity of Bacillus subtilis spores–The first data from a 500-year experiment. PloS one, 13(12), e0208425. 10.1371/journal.pone.0208425.

Vasconcelos, R. H., Teixeira, R. S. D. C., Silva, I. N. G. D., Lopes, E. D. S., Maciel, W. C. (2018). Feral pigeons (Columba livia) as potential reservoirs of Salmonella sp. and Escherichia coli. Arquivos do Instituto Biológico. 85: 1-6, e0412017. 10.1590/1808-1657000412017.

Wain, J., Hendriksen, R. S., Mikoleit, M. L., Keddy, K. H., Ochiai, R. L. (2015). Typhoid fever. The Lancet. 385,1136-1145. 10.1016/ S0140-6736(13)62708-7

Wang, H., Wang, H., Xing, T., Wu, N., Xu, X., & Zhou, G. (2016). Removal of Salmonella biofilm formed under meat processing environment by surfactant in combination with bio-enzyme. LWT-Food Science and Technology, 66, 298-304. 10.1016/j.lwt.2015.10.049.




How to Cite

COSTA, W. L. R.; SANTOS, E. T. S. R. dos .; LEAL NETO, A. F.; SILVA, R. A. R. da .; RODGERS, M. de S. M. .; FERNANDES, L. M. B. .; NASCIMENTO, E. R. do . Salmonella spp. in non-edible animal products intended for the preparation of feed (meal) for industrial poultry feed. Research, Society and Development, [S. l.], v. 11, n. 3, p. e16311326310, 2022. DOI: 10.33448/rsd-v11i3.26310. Disponível em: Acesso em: 16 jul. 2024.



Health Sciences