Enteropathogens associated with enterocoliti in foals: Epidemiological, clinical aspects and diagnostic methods

Authors

DOI:

https://doi.org/10.33448/rsd-v10i4.14008

Keywords:

Enteritis; Enteropathogens; Equine; Enteric disorders.

Abstract

Enterocolitis is among the conditions that most affect foals in horse breeding systems worldwide. It is estimated that up to 80% of foals in the first six months of life are affected by at least one episode of diarrhea, mostly mild and transient episodes, however, the costs of treatment and the mortality rate that this condition can generate are impacting for breeders and owners. The aim of this review is to describe the epidemiological, clinical and diagnostic methods of the main bacterial, viral and parasitic enteropathogens involved in episodes of diarrhea in foals from birth to 8 months of age. Articles available on the Mendeley, MEDLINE, pubMed and SciELO platforms were used. Among the main enteropathogens causing diarrhea in foals, we can highlight infections caused by Salmonella spp., Escherichia coli, Rhodococcus equi, Clostridium perfringens, Clostridium difficile, Lawsonia intracellularis, Rotavirus, Coronavirus and helminths. The identification of high-risk foals and the implementation of therapeutic protocols based on complementary tests and identification of the etiological agent are of great importance for the success in the treatment, control and implementation of prophylaxis methods in the breeding systems.

References

Almeida, J. M., Nader, R. G. M. & Mallet, A. C. T. (2021) T. Intestinal microbiota in the first thousand days of life and its relation to dysbiosis. Research, Society and Development, 10(2), e35910212687.

Arroyo, L. G., Stampfli, H. R. & Weese, J. S. (2006) Potential role of Clostridium difficile as a cause of duodenitis-proximal jejunitis in horses. Journal of Medical Microbiology, 55(5), 605-608.

Bailey, K. E., Gilkerson, J. R. & Browning, G. F. (2013) Equine rotaviruses- Current understanding and continuing challenges. Veterinary Microbiology, 167(1-2), 135-144.

Barrelet, A. (2011). How to diagnose: Lawsonia. Proceedings of the 50th British Equine Veterinary Association Congress - Liverpool, United Kingdom.

Baums, C. G., Schotte, U., Amtsberg, G. & Goethe, R. (2004) Diagnostic multiplex PCR for toxin genotyping of Clostridium perfringens isolates. Veterinary Microbiology, 100(1-2) 11-16.

Baverud, V. (2002) Clostridium difficile infections in animals with special reference to the horse. A review. Veterinary Quarterly, 24(4), 203-219.

Baverud, V., Gustafsson, A., Franklin, A., Aspán, A. & Gunnarsson, A. (2003) Clostridium difficile: prevalence in horses and environment, and antimicrobial susceptibility. Equine Veterinary Journal, 35(5), 465-471.

Baverud, V. (2004) Clostridium difficile diarrhea: infection control in horses. Veterinary Clinics: Equine Practice, 20(3), 615-630.

Beau, I., Cotte-Laffitte, J., Géniteau-Legendre, M., Estes, M. K. & Servin, A. L. (2007) An NSP4-dependant mechanism by which rotavirus impairs lactase enzymatic activity in brush border of human enterocyte-like Caco-2 cells. Cellular Microbiology, 9(9), 2254–2266.

Bihr, T. P (2003). Protein-losing enteropathy caused by Lawsonia intracellularis in a weanling foal. The Canadian Veterinary Journal, 44(1), 65.

Bora, D. P., Barman, N. N., Bhattacharyya, D. K. & Dutta, L. J. (2011) Faecal excretion of rotavirus by naturally infected pregnant sows in organized pig farms-a potent source of infection to newborns. Indian Journal of Animal Sciences, 81(6), 575.

Bowman, D. D. G. (2010) Parasitologia veterinária.. Saunders.

Brockmeier, S. L., Loving, C. L., Nicholson, T. L. & Palmer, M. V. (2008) Coinfection of pigs with porcine respiratory coronavirus and Bordetella bronchiseptica. Veterinary Microbiology, 128(2008), 36–47.

Cohen, N. D. (1994) Causes of and farm management factors associated with disease and death in foals. Journal of the American Veterinary Medical Association, 204(10), 1644-1651.

Collins, A., Love, R. J., Pozo, J., Smith, S. H. & McOrist, S. (2000) Studies on the ex vivo survival of Lawsonia intracellularis. Journal of Swine Health and Production, 8(5), 211-215.

Delmée, M. (2001) Laboratory diagnosis of Clostridium difficile disease. Clinical Microbiology and Infection, 7(8), 411-416.

Deprez, P., Chiers, K., Gebhart, C. J., Ducatelle, R., Lefère, L., Vanschandevijl, K. & Loon, G. V. (2005) Lawsonia intracellularis infection in a 12-monthold colt in Belgium. The Veterinary Record, 157(24), 774.

Diab, S. S., Kinde, H., Moore, J., Shahriar, M. F., Odani, J., Anthenill, L., Songer, G. & Uzal, F. A. (2012) Pathology of Clostridium perfringens type C enterotoxemia in horses. Veterinary Pathology, 49(2), 255-263.

Diab, S. S., Songer, G., & Uzal, F. A. (2013) Clostridium difficile infection in horses: a review. Veterinary Microbiology, 167(1-2), 42-49.

Dwyer, R. M. (1993) Rotaviral diarrhea. Veterinary Clinics of North America: Equine Practice, 9(2), 311-319

Fabiani, J. V. & Nielsen, L. M. K. (2016) Dynamics of Parascaris and Strongylus spp. parasites in untreated juvenile horses. Veterinary Parasitology, 230, 62-66.

Frazer, M. L. (2008) Lawsonia intracellularis infection in horses: 2005–2007. Journal of Veterinary Internal Medicine, 22(5), 1243-1248.

Frederick, J., Giguère, S. & Sanchez, L. C. (2009). Infectious agents detected in the feces of diarrheic foals: a retrospective study of 233 cases (2003–2008). Journal of Veterinary Internal Medicine, 23(6), 1254-1260.

Gabardo, M. P., Sato, J. P. H., Resende, T. P. & Guedes, R. M. C. (2015). Equine proliferative enteropathy on a Brazilian farm. Pesquisa Veterinária Brasileira, 35(5), 443-447.

Giannitti, F., Diab, S., Mete, A., Stanton, J. B., Fielding, L., Crossley, B., Sverlow, K., Fish, S., Mapes, S., Scott, L. & Pusterla, N. (2015) Necrotizing enteritis and hyperammonemic encephalopathy associated with equine coronavirus infection in equids. Veterinary Pathology, 52(6), 1148-1156.

Gibert, M., Jolivet-Renaud, C. & Popoff, M. R. (1997) Beta2 toxin, a novel toxin produced by Clostridium perfringens. Gene, 203(1), 65-73.

Giguère, S., Cohen, N. D., Chaffin, M. K., Slovis, N. M., Hondalus, M. K., Hines, S. A. & Prescott, J. F. (2011). Diagnosis, Treatment, Control, and Prevention of Infections Caused by Rhodococcus equi in Foals. Journal of Veterinary Internal Medicine, 25(6), 1209-1220.

Guimarães‐Ladeira, C. V., Palhares, M. S., Oliveira, J. S. V., Ramirez, M. A. & Guedes, R. M. C. (2009) Faecal shedding and serological cross‐sectional study of Lawsonia intracellularis in horses in the state of Minas Gerais, Brazil. Equine Veterinary Journal, 41(6), 593-596.

Gohari, M. I., Parreira, V. R., Nowell, V. J., Nicholson, V. M., Oliphant, K. & Prescott, J. F. (2015) A novel pore-forming toxin in type A Clostridium perfringens is associated with both fatal canine hemorrhagic gastroenteritis and fatal foal necrotizing enterocolitis. PloS one, 10(4), e0122684.

Gohari, M. I., Parreira, V. R., Timoney, J. F., Fallon, L., Slovis, N. & Prescott, J. F. (2016) NetF-positive Clostridium perfringens in neonatal foal necrotising enteritis in Kentucky. Veterinary Record, 178(9), 216-216.

Gohari, M. I., Unterer, S., Whitehead, A. E. & Prescott, J. F. (2020) NetF-producing Clostridium perfringens and its associated diseases in dogs and foals. Journal of Veterinary Diagnostic Investigation, 32(2), 230-238.

Gray, J. T. & Fedorka-Cray, P. J. (2001) Survival and infectivity of Salmonella choleraesuis in swine feces. Journal of Food Protection, 64(7), 945-949.

Guttmann, P. M., Viscardi, V., Barroso, D. A. & Guedes, R. M. C. (2014) Equine Proliferative Enteropathy Caused by Lawsonia intracellularis in a Foal in Brazil. Journal of Equine Veterinary Science, 34(5), 701-703.

Halaihel, N., Liévin, V., Alvarado, F. & Vasseur, M. (2000) Rotavirus infection impairs intestinal brush-border membrane Na+-solute cotransport activities in young rabbits. American Journal Physiology- Gastrointestinal and Liver Physiology, 279(3), G587–G596.

Harris, R., Sankar, K., Small, J. A., Suepaul, R., Stewart-Johnson, A. & Adesiyun, A. (2012) Prevalence and characteristics of enteric pathogens detected in diarrhoeic and non-diarrhoeic foals in Trinidad. Veterinary Medicine International, 2012.

Hazlett, M. J., Kircanski, J., Slavic, D. & Prescott, J. F. (2011) Beta 2 toxigenic Clostridium perfringens type A colitis in a three-day-old foal. Journal of Veterinary Diagnostic Investigation, 23(2), 373-376.

Heidmann, P., Madigan, J.E. & Watson, J.L. (2006). Rhodococcus equi pneumonia: clinical findings, diagnosis, treatment and prevention. Clinical Techniques in Equine Practice, 5(3), 203-210.

Higgins, W. P., Gillespie, J. H., Schiff, E. I., Pennow, N. N., Tanneberger, M. J. (1987). Infectivity and immunity studies in foals with cell culturepropagated equine rotaviruses. In: Equine Infectious Diseases V: Proceedings of the Fifth International Conference, Lexington, Kentucky, 241–247.

Hines, M. T. (2014) Rhodococcus equi. In: Sellon, D.C., Long, M. (2a ed.) Equine Infectious Diseases (pp. 287- 302). Missouri: Elsevier Health Sciences.

Hernandez, J. A., Long, M. T., Traub-Dargats, J. L. & Besser, T. E. (2014) Salmonellosis. In: Sellon, D.C.; Long, M. (2ed.) Equine Infectious Diseases (pp. 321-333) Missouri : Elsevier Health Sciences.

Holland, R. E., Schimidt, A., Sriranganathan, N., Grimes, S. D., Wilson, R. A., Brown, C. M. & Walker, R. D. (1996). Caracterization of Escherichia coli isolated from foals. Veterinary Microbiology, 48, 243-255.

Horin, P., Sabakova, K., Futas, J., Vychodilova, L. & Necesankova, M. (2010). Immunity‐related gene single nucleotide polymorphisms associated with Rhodococcus equi infection in foals. International Journal of Immunogenetics, 37(2), 67-71.

Imagawa, H., Kato, T., Tsunemitsu, H., Tanaka, H., Sato, S., & Higuchi, t. (2005) Field study of inactivated equine rotavirus vaccine. Journal of Equine Science, 16(2), 35-44, 2005.

Knoop, F. C., Owens, M. & Crocker, C. (1993) Clostridium difficile: clinical disease and diagnosis. Clinical Microbiology Reviews, 6(3), 251-265.

Kolk J. H. V. & Kroeze, E. J. B. V. (2013). Infection disease of the horse. London: Manson.

Lavoie, J. P., Drolet, R., Parsons, D., Leguillette, R., Sauvageau, R., Shapiro, J., Houle, L., Hallé, G. & Gebhart, C. J. (2000) Equine proliferative enteropathy: a cause of weight loss, colic, diarrhoea and hypoproteinaemia in foals on three breeding farms in Canada. Equine Veterinary Journal, 32(5), 418-425.

Lawson, G. H. K. & Gebhart, C. J. (2000) Proliferative enteropathy. Journal of Comparative Pathology, 122(2-3), 77-100.

Lester, G. D. (2001) Infectious diarrhea in foals. In: Proceedings of the Annual Convention of the AAEP. 41, 468-471.

Lucena, R. B. Fighera, R. A. & Barros, C. S. L. (2012). Foal mortality associated with Strongyloides westeri parasitism. Pesquisa Veterinária Brasileira, 32(5), 401-404.

Macêdo, N. R. Al-Ghamdi, G., Gebhart, C. J. & Guedes, R. M. C. (2008) Enteropatia proliferativa em equinos. Ciência Rural, 38(3), 889-897.

Magdesian, K. G. (2006) Gastrointestinal Disease. In: Paradis, M. R. Equine Neonatal Medicine- A Case Based Approach (pp. 191- 229). Philidelphia: Saunders.

Magdesian, K. G. & Leutenegger, C. M. (2011) Real-time PCR and typing of Clostridium difficile isolates colonizing mare–foal pairs. The Veterinary Journal, 190(1), 119-123.

Magdesian, K. G., Dwyer, R. M. & Arguedas, M. G. (2014) Viral Diarrhea. In: Sellon, D.C. & Long, M. (2Ed.), Equine Infectious Diseases (pp. 198-203). Missouri: Elsevier Health Sciences.

Mallicote, M., House, A. M. & Sanchez, L. C. (2012) A review of foal diarrhea from birth to weaning. Equine Veterinary Education, 24(4), 206-214.

Martins, I.V. F., Pereira, M. J. S., Grisi, L., & Scott, F. B. (2005). Seasonal abundance of equine strongyles (Nematoda: Strongylidae) in the State of Rio de Janeiro, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 57(1), 43-47.

McClintock, S. A. & Collins, A. M. (2004) Lawsonia intracellularis proliferative enteropathy in a weanling foal in Australia. Australian Veterinary Journal, 82(12), 750-752.

McCracken, J. L. (2015) Screening for Rhodococcus equi Pneumonia. In: Sprayberry, K.A; Robinson, N.E (7ed.), Robinson’s Current Therapy in Equine Medicine (pp. 79-131). Missouri: Saunders.

Nemoto, M., Tsunemitsu, H., Murase, H., Nambo, Y., Sato, S., Orita, Y., Imagawa, H., Bannai, H., Tsujimura, K., Yamanaka, T., Matsumura, T. & Kondo, T. (2012). Antibody response in vaccinated pregnant mares to recent G3BP [12] and G14P [12] equine rotaviruses. Acta Veterinaria Scandinavica, 54(1), 1-5.

Nielsen, M. K. (2017). Internal Parasite Screening and Control. In: Sprayberry, K.A & Robinson, N.E. (7ed.), Robinson’s current Therapy in equine medicine (pp. 336-340). Missouri: Saunders.

Olivo, G., Lucas, T. M., Borges, A. S., Silva, R. O. S., Lobato, F. C. F., Siqueira, A. K., Leite, D. S., Brandão, P. E., Gregori, F., Oliveira-Filho, J. P., Takai, S. & Ribeiro, M. G. (2016). Enteric Pathogens and Coinfections in Foals with and without Diarrhea. BioMed research international, 2016.

Parreño, V., Marcoppido, G., Vega, C., Garaicoechea, L., Rodriguez, D., Saif, L., & Fernández, F. (2010). Milk supplemented with immune colostrum: Protection against rotavirus diarrhea and modulatory effect on the systemic and mucosal antibody responses in calves experimentally challenged with bovine rotavirus. Veterinary immunology and immunopathology, 136(1-2), 12-27.

Payment, P. & Morin, E. (1990) Minimal infective dose of the OSU strain of porcine rotavirus. Archives of Virology, 112(3-4), 277-282.

Pereira, A. S., Shitsuka, D. M., Parreira, F.J. & Shitsuka, R. (2018). Metodologia da pesquisa científica, 1º Edição UBA/NTE/UFSM, Universidade Federal de Santa Maria.

Petit, L., Gibert, M., & Popoff, M. R. (1999). Clostridium perfringens: toxinotype and genotype. Trends in microbiology, 7(3), 104-110.

Preis, I. S., Silva, R. O., Pires, P. S., Lobato, F. C., Palhares, M. S., Maranhão, R. P., & Ecco, R. (2012). Enteritis associated with Clostridium difficile and opportunistic candidiasis in a foal. Brazilian Journal of Veterinary Pathology, 5(1), 7-11.

Pusterla, N; Gebhart, C. (2009) Enteropatia proliferativa equina causada por Lawsonia intracellularis. Educação Veterinária Equina, 21(8), 415-419.

Pusterla, N., Byrne, B. A., Hodzic, E., Mapes, S., Jang, S. S., & Magdesian, K. G. (2010a). Use of quantitative real-time PCR for the detection of Salmonella spp. in fecal samples from horses at a veterinary teaching hospital. The Veterinary Journal, 186(2), 252-255.

Pusterla, N., Jackson, R., Mapes, S. M., Noland, J., Stenbom, R. M., & Gebhart, C. (2010b). Lawsonia intracellularis: Humoral immune response and fecal shedding in weanling foals following intra-rectal administration of frozen–thawed or lyophilized avirulent live vaccine. The Veterinary Journal, 186(1), 110-112.

Pusterla, N., Wattanaphansak, S., Mapes, S., Collier, J., Hill, J., Difrancesco, M., & Gebhart, C. (2010c). Oral infection of weanling foals with an equine isolate of Lawsonia intracellularis, agent of equine proliferative enteropathy. Journal of Veterinary Internal Medicine, 24(3), 622-627.

Pusterla, N., Mapes, S., & Gebhart, C. (2012). Further investigation of exposure to Lawsonia intracellularis in wild and feral animals captured on horse properties with equine proliferative enteropathy. The Veterinary Journal, 194(2), 253-255.

Pusterla, N. & Gebhart, C. (2013) Lawsonia intracellularis infection and proliferative enteropathy in foals. Veterinary Microbiology, 167(1-2), 34-41.

Pusterla, N., Vin, R., Leutenegger, C., Mittel, L. D., & Divers, T. J. (2016). Equine coronavirus: An emerging enteric virus of adult horses. Equine veterinary education, 28(4), 216-223.

Pusterla, N., Vin, R., Leutenegger, C., Mittel, L. D. & Diver, T. J. (2017) Equine coronavirus infection. In: Emerging and Re-emerging Infectious Diseases of Livestock. Springer, 121-132.

Reinemeyer, C.R (2008). Parasite control recommendation for horses during the first year of life. Proceedings of the American Association of Equine Practitioners Texas, USA, 143-154.

Reuss, S. M., Chaffin, M. K., & Cohen, N. D. (2009). Extrapulmonary disorders associated with Rhodococcus equi infection in foals: 150 cases (1987–2007). Journal of the American Veterinary Medical Association, 235(7), 855-863.

Ribas, L. D. M., Moraes, C. M., Lins, L. A., Flores, E. F., & Nogueira, C. E. W. (2009). Fatores de risco associados a doenças respiratórias em potros Puro Sangue Inglês do nascimento ao sexto mês de vida. Ciência Rural, 39(6), 1789-1794.

Rood, J. I., Adams, V., Lacey, J., Lyras, D., McClane, B. A., Melville, S. B., & Van Immerseel, F. (2018). Expansion of the Clostridium perfringens toxin-based typing scheme. Anaerobe, 53, 5-10.

Sampieri, F., Hinchcliff, K. W., & Toribio, R. E. (2006). Tetracycline therapy of Lawsonia intracellularis enteropathy in foals. Equine veterinary journal, 38(1), 89-92.

Schumacher, J., Schumacher, J., Rolsma, M., Brock, K. V., & Gebhart, C. J. (2000). Surgical and medical treatment of an Arabian filly with proliferative enteropathy caused by Lawsonia intracellularis. Journal of Veterinary Internal Medicine, 14(6), 630-632.

Silva, R. O. S., Moreira, F. M., Rezende, J. V., Pires, P. S., Maranhão, R. D. P. A., Palhares, M .S., & Lobato, F. C. F. (2012). First confirmed case of Clostridium difficile-associated diarrhea in foals in Brazil. Ciência Rural, 42(3), 498-500.

Silva, R. O. S., Neves, M. S., Ribeiro, M. G., Palhares, M. S., Maranhão, R. D. P. A., & Lobato, F. C. F. (2014). Evaluation of three enzyme immunoassays for diagnosis of Clostridium difficile–associated diarrhea in foals. Journal of Equine Veterinary Science, 34(8), 1032-1035.

Smith, D. E. & Lawson, G. K. (2001) Lawsonia intracellularis: getting inside the pathogenesis of proliferative enteropathy. Veterinary Microbiology, 82, 331-345

Slovis, N. M (2009). Foal Diarrhea: Diagnosis and treatment. In: Proceedings of the 11th International Congress of World Equine Veterinary Association - Guarujá, SP, Brasil.

Slovis, N. M (2011). Infection gastrintestinal disorders. Proceedings of the 12th International Congress of World Equine Veterinary Association, Hiderabad, India.

Slovis, N. M., Elam, J., Estrada, M., & Leutenegger, C. M. (2014). Infectious agents associated with diarrhoea in neonatal foals in central K entucky: A comprehensive molecular study. Equine Veterinary Journal, 46(3), 311-316.

Tillotson, K., Traub-Dargatz, J. L., Dickinson, C. E., Ellis, R. P., Morley, P. S., Hyatt, D. R., Magnuson, R., Riddle, T., Bolte, D. & Salman, M. D. (2002). Population-based study of fecal shedding of Clostridium perfringens in broodmares and foals. Journal of the American Veterinary Medical Association, 220(3), 342-348.

Traub-Dargatz, J. L. & Besser, T. E (2007). Samonellosis. In: Sellon, D.C. & Long, M.T.(Ed.), Equine Infectious Diseases (pp. 331-345). Missouri: Saunders.

Uzal, F. A., Vidal, J. E., McClane, B. A., & Gurjar, A. A. (2010). Clostridium perfringens toxins involved in mammalian veterinary diseases. The Open Toxinology Journal, 2, 24.

Uzal, F. A. & Diab, S. S. (2015) Gastritis, enteritis, and colitis in horses. Veterinary Clinics: Equine Practice, 31(2), 337-358.

Vlasova, A. N., Deol, P., Sircar, S., Ghosh, S., Jacab, S., Bányai, K., Dhama, K., Amimo, J. O., Saif, L. J. & Malik, Y. S. (2020) Animal Rotaviruses. In: Animal-Origin Viral Zoonoses (pp. 163-202). Springer: Singapore.

Ward, M. P., Alinovi, C. A., Couëtil, L. L., & Wu, C. C. (2005). Evaluation of a PCR to detect Salmonella in fecal samples of horses admitted to a veterinary teaching hospital. Journal of veterinary diagnostic investigation, 17(2), 118-123.

Weese, J. S., Staempfli, H. R., & Prescott, J. F. (2000). Survival of Clostridium difficile and its toxins in equine feces: implications for diagnostic test selection and interpretation. Journal of Veterinary Diagnostic Investigation, 12(4), 332-336.

Weese, J. S., Staempfli, H. R., & Prescott, J. F. (2001). A prospective study of the roles of Clostridium difficile and enterotoxigenic Clostridium perfringens in equine diarrhoea. Equine Veterinary Journal, 33(4), 403-409.

Weese, J. S. (2007) Enteric Clostridial Infections. In: Sellon, D.C. & LONG, M.T. Equine Infections Diseases. Saint Louis: Elsevier Saunders, cap 44, 362- 367.

Weese, J. S. (2008). The Gastrointestinal system. In: McAuliffe, S.B. & SLOVIS, N.M. Color atlas of diseases and disorders of the foal (pp. 79-131) Philadelphia: Saunders.

Weese, J. S. (2020) Clostridium (Clostridioides) difficile in animals. Journal of Veterinary Diagnostic Investigation, 32(2), 213-221.

Wilson, J. H., & Gebhart, C. J. (2008) Lawsonia proliferative enteropathy in foals: clinical features and piglet parallels. In: Proceedings of the AAEP Summer Meetings: Focus on the First Year of Life, Texas. 214-226.

Würsch, K., Hüssy, D., Koch, C., & Oevermann, A. (2006). Lawsonia intracellularis proliferative enteropathy in a filly. Journal of Veterinary Medicine Series A, 53(1), 17-21.

Zimmel, D. (2008) Neonatal Foal Diarrhea. In: Annual Convention of the American Association Equine Practitioners: Focus Meeting- First Year of Life, Texas, USA. 207-213.

Published

03/04/2021

How to Cite

SOUZA, R. P. de .; MOUSQUER, M. A. .; MÜLLER, V. .; CURCIO, B. da R. .; NOGUEIRA, C. E. W. . Enteropathogens associated with enterocoliti in foals: Epidemiological, clinical aspects and diagnostic methods. Research, Society and Development, [S. l.], v. 10, n. 4, p. e14710414008, 2021. DOI: 10.33448/rsd-v10i4.14008. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/14008. Acesso em: 14 apr. 2021.

Issue

Section

Agrarian and Biological Sciences