Seroprevalence and risk factors for brucellosis and leptospirosis in swine from rural communities of Argentina

Seroprevalencia y factores de riesgo de brucelosis y leptospirosis en cerdos en comunidades rurales de Argentina

Objectives. To determine the seroprevalence of brucellosis and leptospirosis in pigs reared on small-scale farms in rural areas of the district of Tandil, Buenos Aires Province, Argentina; to analyse the associated risk factors; to describe the prevalent Leptospira spp. serogroups; and to determine the spatial distribution of both diseases. Materials and methods. A total of 340 serum samples were obtained. Buffer Plate Agglutination Test, Rose Bengal Test, and Fluorescence Polarisation Assay were used to detect antibodies against Brucella spp. Microscopic Agglutination Test was applied for serological diagnosis of leptospirosis. Statistical methods were used to evaluate the factors associated with the infections. Results. Seroprevalence of 0% and 22.6% was observed for brucellosis and leptospirosis, respectively. The most prevalent Leptospira serogroups identified were Canicola, Ballum, Icterohaemorrhagiae and Pomona. The main risk factors associated with leptospirosis infection were farms with a higher number of pigs and the presence of horses and wild boars near or within the farms. The use of milling by-products of cereal grains as animal feed and the presence of weaning cages were also associated. A relevant spatial cluster of seropositivity to Leptospira spp. was identified in a low-altitude area. Conclusions. Our results suggest that brucellosis is probably controlled, but Leptospira spp. are present in the farming systems under study. Knowledge of brucellosis and leptospirosis seroprevalence, spatial distribution and associated risk factors can be useful for the prevention and control of endemic zoonotic diseases in the region.

1. Ministerio de Agricultura, Ganadería y Pesca. Anuario 2019 Porcinos. Subsecretaría de ganadería y producción animal: Argentina; 2019. https://www.magyp.gob.ar/sitio/areas/porcinos/estadistica/_archivos/000005-Anuario/190000-Anuario%202019.pdf
2. SENASA. Informe estadístico de producción porcina. Servicio Nacional de Sanidad y Calidad Agroalimentaria: Argentina; 2014. http://www.senasa.gob.ar/cadena-animal/porcinos/informacion/informes-y-estadisticas
3. Samartino L. Zoonosis En Los Sistemas De Producción Animal De Las Áreas Urbanas y Periurbanas De América Latina. Livestock Information and Policita Breanh, AGAL; 2001. https://www.fao.org/Ag/againfo/resources/en/publications/sector_discuss/PP_Nr2_Final.pdf
4. Dibarbora M, Cappuccio JA, Aznar MN, Bessone FA, Piscitelli H, Pereda A, Pérez D. Serological detection of Brucella suis, influenza virus and Aujeszky's disease virus in backyard and small swine holders in Argentina. Rev Argent Microbiol. 2017; 49(2):158-165. https://doi.org/10.1016/j.ram.2016.09.010
5. SENASA. Guía de recomendaciones para la tenencia y producción familiar de cerdos. Programa de enfermedades de los Porcinos. Servicio Nacional de Sanidad y Calidad Agroalimentaria: Argentina; 2015. http://www.senasa.gob.ar/sites/default/files/manual_cerdos-version_2_0.pdf
6. Lovera R, Fernández MS, Jacob J, Lucero N, Morici G, Brihuega B, et al. Intrinsic and extrinsic factors related to pathogen infection in wild small mammals in intensive milk cattle and swine production systems. PLoS Negl Trop Dis. 2017; 11(6):e0005722. https://doi.org/10.1371/journal.pntd.0005722
7. Hartskeerl RA, Collares-Pereira M, Ellis WA. Emergence, control and re-emerging leptospirosis: dynamics of infection in the changing world. Clin Microbiol Infect. 2011; 17(4):494–501. https://doi.org/10.1111/j.1469-0691.2011.03474.x
8. Schneider M, Jancloes M, Buss D, Aldighieri S, Bertherat E, Najera P, et al. Leptospirosis: A Silent Epidemic Disease. Int J Environ Res Public Health. 2013; 10(12):7229–7234. https://doi.org/10.3390/ijerph10127229
9. Dean AS, Crump L, Greter H, Schelling E, Zinsstag J. Global Burden of Human Brucellosis: A Systematic Review of Disease Frequency. Carabin H, editor. PLoS Negl Trop Dis. 2012; 6(10):e1865. https://doi.org/10.1371/journal.pntd.0001865
10. Lounes N, Cherfa M-A, Le Carrou G, Bouyoucef A, Jay M, Garin-Bastuji B, et al. Human Brucellosis in Maghreb: Existence of a Lineage Related to Socio-Historical Connections with Europe. PLoS One. 2014; 9(12):e115319. https://doi.org/10.1371/journal.pone.0115319
11. McDermott JJ, Grace D, Zinsstag J. Economics of brucellosis impact and control in low-income countries. Rev Sci Tech. 2013; 32(1):249–261. https://doi.org/10.20506/rst.32.1.2197
12. Olsen SC, Palmer MV. Advancement of Knowledge of Brucella Over the Past 50 Years. Vet Pathol. 2014; 51(6):1076–1089. https://doi.org/10.1177/0300985814540545
13. Lucero NE, Ayala SM, Escobar GI, Jacob NR. Brucella isolated in humans and animals in Latin America from 1968 to 2006. Epidemiol Infect. 2008; 136(4):496–503. https://doi.org/10.1017/S0950268807008795
14. Ministerio de Salud de la Nación (MSAL). Dirección de Epidemiología. Boletín epidemiológico Nacional. N°631. Ministerio de Salud de la Nación: Argentina; 2022. https://bancos.salud.gob.ar/sites/default/files/2022-12/BEN_631_SE_49.pdf
15. Olsen SC, Tatum FM. Swine brucellosis: current perspectives. Vet Med (Auckl). 2017; 8:1-12. https://doi.org/10.2147/VMRR.S91360
16. Heymann DL. Control of communicable diseases manual. No. Ed. 19. American Public Health Association. Washington DC, USA; 2008.
17. https://www.cabdirect.org/cabdirect/abstract/20103167361
18. WHO. Report of the Second Meeting of the Leptospirosis Burden Epidemiology Reference Group. Geneva, Switzerland: World Health Organization; 2011. https://apps.who.int/iris/bitstream/handle/10665/44588/9789241501521_eng.pdf
19. WHO. Human leptospirosis: guidance for diagnosis, surveillance and control. Geneva, Switzerland:.World Health Organization; 2003. http://www.who.int/iris/handle/10665/42667
20. Sykes JE, Reagan KL, Nally JE, Galloway RL, Haake DA. Role of Diagnostics in Epidemiology, Management, Surveillance, and Control of Leptospirosis. Pathogens. 2022; 11(4):395. https://doi.org/10.3390/pathogens11040395
21. Tagliabue S, Figarolli BM, D’Incau M, Foschi G, Gennero MS, Giordani R, Natala A, Papa P, Ponti N, Scaltrito D, Spadari L, Vesco G & Ruocco L. Serological surveillance of Leptospirosis in Italy: Two-year national data (2010–2011). Vet Ital. 2016; 52:129-138. https://doi.org/10.12834/VetIt.58.169.2
22. Hartmann K, Egberink H, Pennisi MG, Lloret A, Addie D, Belák S, et al. Leptospira species infection in cats: ABCD guidelines on prevention and management. J Feline Med Surg. 2013; 15(7):576-581. https://doi.org/10.1177/1098612X13489217
23. Azócar-Aedo L, Monti G, Jara R. Leptospira spp. in Domestic Cats from Different Environments: Prevalence of Antibodies and Risk Factors Associated with the Seropositivity. Animals. 2014; 4(4):612–626. https://doi.org/10.3390/ani4040612
24. Kakita T, Kuba Y, Kyan H, Okano S, Morita M, Koizumi N. Molecular and serological epidemiology of Leptospira infection in cats in Okinawa Island, Japan. Sci Rep. 2021; 11(1):10365. https://doi.org/10.1038/s41598-021-89872-3
25. Mori M, Bakinahe R, Vannoorenberghe P, Maris J, De Jong E, Tignon M, et al. Reproductive Disorders and Leptospirosis: A Case Study in a Mixed-Species Farm (Cattle and Swine). Vet Sci. 2017; 4(4):64. https://doi.org/10.3390/vetsci4040064
26. Lau CL, Smythe LD, Craig SB, Weinstein P. Climate change, flooding, urbanisation and leptospirosis: fuelling the fire? Trans R Soc Trop Med Hyg. 2010; 104(10):631–638. https://doi.org/10.1016/j.trstmh.2010.07.002
27. Costa F, Hagan J, Calcagno J, Kane M, Torgerson P, Martinez-Silveira M. Global Morbidity and Mortality of Leptospirosis: A Systematic Review. PLoS Negl Trop Dis. 2015; 9(9). https://doi.org/10.1371/journal.pntd.0003898
28. Levett P, Haake D. Leptospira Species (Leptospirosis). Infectious Diseases and Their Etiologic Agents. 2015; 3:240,7. https://elsevierjapan.com/Portals/0/images/pdf/Chapter%20240.pdf
29. Ellis WA. Animal Leptospirosis. Curr Top Microbiol Immunol. 2014. https://doi.org/10.1007/978-3-662-45059-8_6
30. Valença RMB, Mota RA, Castro V, Anderlini GA, Pinheiro Júnior JW, Brandespim DF, et al. Prevalence and risk factors associated with Leptospira spp. infection in technified swine farms in the state of Alagoas, Brazil. Risk factors associated with Leptospira spp. in swine farms. Transbound Emerg Dis. 2012; 60(1):79–86. https://doi.org/10.1111/j.1865-1682.2012.01320.x
31. Ospina-Pinto MC, Rincón-Pardo M, Soler-Tovar D, Hernández-Rodríguez P. Alteration of the Reproductive Indicators by the Presence of Leptospira spp. in Sows of Swine Farms. Acta Sci Vet. 2019; 47(1). https://doi.org/10.22456/1679-9216.89894
32. Haake DA, Levett PN. Leptospirosis in Humans. Curr Top Microbiol Immunol. 2014; 387:65–97. https://doi.org/10.1007/978-3-662-45059-8_5
33. Moyo S, Swanepoel FJC. Multifunctionality of livestock in developing communities. The role of livestock in developing communities: Enhancing multifunctionality. 2010. https://books.google.com.ar/books?hl=es&lr=&id=a5ddEAAAQBAJ&oi=fnd&pg=PA1&dq=Moyo
34. Office International des Epizooties. OIE. Brucellosis (infection with B. abortus, B. melitensis and B. suis). In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. France, 2019; pp. 355–398. Available from: https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/A_summry.htm
35. Gutiérrez SE, Lützelschwab CM, Díaz AG, Estein SM. Fluorescence Polarization Assay for the Diagnosis of Anti-Brucella abortus Antibodies in Cattle Serum: Adaptation for its Use in Microplates and Comparison with Conventional Agglutination Tests. J Vet Sci Med Diagn. 2014; 3(3). http://dx.doi.org/10.4172/2325-9590.1000140
36. Nicola A, Elena S. Manual de diagnóstico serológico de la brucelosis bovina. Servicio de Sanidad y Calidad Agroalimentaria (SENASA), Argentina. 2019; https://www.argentina.gob.ar/sites/default/files/manual_tecnicas_serologicas-2019-v4_brucelosis.pdf
37. Office International des Epizooties (OIE). Leptospirosis. In Oie Terrestrial Manual; OIE: Paris, France; 2014. https://www.woah.org/app/uploads/2021/03/a-bsc-jan2015.pdf
38. Ward MP, Carpenter TE. Analysis of time–space clustering in veterinary epidemiology. Prev Vet Med. 2000; 43(4):225–237. https://doi.org/10.1016/S0167-5877(99)00111-7
39. Bence AR, Moran MC, Cacciato CS, Soto J, Gutierrez SE, Estein SM. Identification of a small-scale pig farm infected with Brucella suis linked to a clinical case of human brucellosis in Buenos Aires province, Argentina. FAVE Secc Cienc Vet. 2021; 20(1):34–40. https://doi.org/10.14409/favecv.v20i1.10055
40. Petrakovsky MJ, Tinao J, Esteves MJ. Leptospirosis porcina: prevalencia serológica en establecimientos productores de la República Argentina. Rev MVZ Córdoba. 2013; 18(1):3282–3287. https://doi.org/10.21897/rmvz.189
41. Hashimoto VY, Garcia JL, Spohr KAH, Silva FG da, Alves LA, Freitas JC de. Prevalência de anticorpos contra Leptospira spp. em bovinos, caninos, equinos, ovinos e suínos do município de Jaguapitã, estado do Paraná, Brasil. Arq Inst Biol (Sao Paulo). 2010; 77(3):521–524. https://doi.org/10.1590/1808-1657v77p5212010
42. Cruz-Romero A, Alvarado-Esquivel C, Romero-Salas D, Alvarado-Félix ÁO, Sánchez-Montes S, Hernández-Tinoco J, et al. Seroepidemiology of Leptospira infection in backyard pigs in Durango State, Mexico. Eur J Microbiol Immunol. 2018; 1–4. https://doi.org/10.1556/1886.2018.00009
43. Carreño LA, Salas D, Beltrán KB, Carreño LA, Salas D, Beltrán KB. Prevalencia de Leptospirosis en Colombia: revisión sistemática de literatura. Rev. Salud Pública. 2017; 19(2):204–209. https://doi.org/10.15446/rsap.v19n2.54235
44. Ospina-Pinto MC, Hernández-Rodríguez P. Identification of Leptospira spp. in the animal-environment interface (swine-water) in pig production cycle. Trop Anim Health Prod. 2021; 53(1). https://doi.org/10.1007/s11250-021-02567-9
45. Smythe LD, Tiengrim S, Peacock SJ, Wuthiekanun V, Suputtamongkol Y, Day NP, et al. The Microscopic Agglutination Test (MAT) is an unreliable predictor of infecting Leptospira serovar in Thailand. Am J Trop Med Hyg. 2009; 81(4):695. https://doi.org/10.4269/ajtmh.2009.09-0252
46. Hamond C, Martins G, Lawson-Ferreira R, Medeiros MA, Lilenbaum W. The role of horses in the transmission of leptospirosis in an urban tropical area. Epidemiol Infect. 2012; 141(1):33–35. https://doi.org/10.1017/S0950268812000416
47. Rodríguez-Torrens HC. Los equinos, al actuar como reservorios de Leptospira, pueden ser un riesgo al humano. Rev Arch Med Camagüye. 2019; 23(3):293-295. http://revistaamc.sld.cu/index.php/amc/issue/view/168
48. Merino ML, Carpinetti BN. Feral pig Sus scrofa population estimates in Bahía Samborombón conservation area, Buenos Aires province, Argentina. Mastozool Neotrop. J. Neotrop. Mammal. 2003; 10(2):269-275. https://mn.sarem.org.ar/article/feral-pig-sus-scrofa-population-estimates-in-bahia-samborombon-conservation-area-buenos-aires-province-argentina/
49. Meng XJ, Lindsay DS, Sriranganathan N. Wild boars as sources for infectious diseases in livestock and humans. Philos Trans R Soc Lond B Biol Sci. 2009; 364(1530):2697–2707. https://doi.org/10.1098/rstb.2009.0086
50. Petrakovsky J, Carpinetti B, Antonuci A. Prevalencia Serológica de Leptospira spp. en Cerdos Silvestres (Sus scrofa) en Bahía de Samborombón, provincia de Buenos Aires, República Argentina, en el Periodo 2013-2015. Salud y Tecnología Veterinaria. 2016; 3(1):23. https://doi.org/10.20453/stv.v3i1.2759
51. Brihuega B, Grune Loffler S, Samartino LE, Romero G, Auteri C, Martinez, M. First isolation of Leptospira borgpetersenii from fetuses of Wild boars (Sus scrofa). Electronic Journal of Biology. 2017; 13(1):63-56. https://ejbio.imedpub.com/first-isolation-of-leptospira-borgpetersenii-from-fetuses-ofwild-boars-sus-scrofa.php?aid=18235
52. Cilia G, Bertelloni F, Piredda I, Ponti MN, Turchi B, Cantile C, et al. Presence of pathogenic Leptospira spp. in the reproductive system and fetuses of wild boars (Sus scrofa) in Italy. PLoS Negl Trop Dis. 2020; 14(12):e0008982. https://doi.org/10.1371/journal.pntd.0008982
53. Santos CVB dos, Mathias LA, Feitosa PJ da S, Oliveira JMB, Pinheiro Júnior JW, Brandespim DF. Risk factors associated with leptospirosis in swine in state of Pernambuco, Brazil. Arq Inst Biol (Sao Paulo). 2019; 86. https://doi.org/10.1590/1808-1657000632017
54. Silva JA, Scialfa EA, Tringler M, Rodríguez MG, Tisnés A, Linares S, et al. Seroprevalence of human leptospirosis in a rural community from Tandil, Argentina. Assessment of risk factors and spatial analysis. Rev Argent Microbiol. 2022; 55(1):49-59. https://doi.org/10.1016/j.ram.2022.02.007