Pathogenesis of domestic pigs submitted to mycobacterial sensitizations previous to experimental infection with Mycobacterium bovis

Keywords: Tuberculosis, swine, pathogenicity, histopathology, infectious disease, humoral response

Abstract

Aim of study: To demonstrate the virulence of a Mycobacterium bovis local pig isolate in order to contribute to a better understanding of the pathological and immunological consequences of M. bovis infection in previous sensitized animals.

Area of study: Buenos Aires, Argentina

Material and methods: One group of ten pigs received two oral doses of killed M. bovis suspension and a comparative intradermal tuberculin test (CIT) (multiple sensitized) and then was infected with the M. bovis strain. Another group only received the CIT (single sensitized) and the infective dose. Humoral immune response was followed monthly, and gross pathology, histopathological and bacteriological analysis were performed at necropsy 100 days after infection.

Main results: M. bovis oral infection induced lesions and allowed bacterial growth in most of the animals. Previous sensitization with killed M. bovis suspension slightly raised the intensity of the response, as the multiple sensitized group showed higher lesion scores and humoral response.

Research highlights: Although the differences in lesion scores were not statistically significant, oral route infection after sensitization can modify the course of infections towards a fast development of lesions with a higher fibrotic component suggestive of increased resistance to infection in the right conditions.

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References

Aranaz AL, De Juan N, Montero C, Sanchez M, Galka C, Delso J et al,, 2004. Bovine tuberculosis (Mycobacterium bovis) in wildlife in Spain. J Clinic Microbiol 42: 2602-2608. https://doi.org/10.1128/JCM.42.6.2602-2608.2004

Arrieta-Villegas CT, Peralvarez E, Vidal Z, Puighibet X, Moll A, Canturri IA et al,, 2018. Efficacy of parenteral vaccination against tuberculosis with heat-inactivated Mycobacterium bovis in experimentally challenged goats. PloS one 13: e0196948. https://doi.org/10.1371/journal.pone.0196948

Bailey SS, Crawshaw TR, Smith NH, Palgrave CJ, 2013. Mycobacterium bovis infection in domestic pigs in Great Britain. Vet J 198: 391-397. https://doi.org/10.1016/j.tvjl.2013.08.035

Ballesteros C, Garrido JM, Vicente J, Romero B, Galindo RC, Minguijon E et al,, 2009. First data on Eurasian wild boar response to oral immunization with BCG and challenge with a Mycobacterium bovis field strain. Vaccine 27: 6662-6668. https://doi.org/10.1016/j.vaccine.2009.08.095

Barandiaran S, Martínez Vivot M, Moras EV, Cataldi AA, Zumárraga MJ, 2011. Mycobacterium bovis in swine: spoligotyping of isolates from Argentina. Vet Med Int 2011: 979647-979647. https://doi.org/10.4061/2011/979647

Barandiaran S, Martinez Vivot M, Perez AM, Cataldi AA; Zumarraga MJ, 2015a. Bovine tuberculosis in domestic pigs: Genotyping and distribution of isolates in Argentina. Res Vet Sci 103: 44-50. https://doi.org/10.1016/j.rvsc.2015.09.013

Barandiaran S, Perez AM, Gioffre AK, Martinez Vivot M, Cataldi AA, Zumarraga MJ, 2015b. Tuberculosis in swine co-infected with Mycobacterium avium subsp. hominissuis and Mycobacterium bovis in a cluster from Argentina. Epidemiol Infect 143: 966-974. https://doi.org/10.1017/S095026881400332X

Barandiaran S, Marfil MJ, Capobianco G, Perez Aguirreburualde MS, Zumarraga MJ, Eirin ME, et al., 2021. Epidemiology of pig tuberculosis in Argentina. Front Vet Sci 8: 693082. https://doi.org/10.3389/fvets.2021.693082

Beltran-Beck B, de la Fuente J, Garrido JM, Aranaz A, Sevilla I, Villar M, et al., 2014. Oral vaccination with heat inactivated Mycobacterium bovis activates the complement system to protect against tuberculosis. PloS one 9: e98048. https://doi.org/10.1371/journal.pone.0098048

Bollo E, Ferroglio E, Dini V, Mignone W, Biolatti B; Rossi L, 2000. Detection of Mycobacterium tuberculosis complex in lymph nodes of wild boar (Sus scrofa) by a target-amplified test system. J Vet Med B 47: 337-342. https://doi.org/10.1046/j.1439-0450.2000.00354.x

Buddle BM, Parlane NA, Wedlock DN, Heiser A, 2013. Overview of vaccination trials for control of tuberculosis in cattle, wildlife and humans. Transbound Emerg Dis 60(S1): 136-146. https://doi.org/10.1111/tbed.12092

Burdz TV, Wolfe J, Kabani A, 2003. Evaluation of sputum decontamination methods for Mycobacterium tuberculosis using viable colony counts and flow cytometry. Diagn Microbiol Infect Dis 47: 503-509. https://doi.org/10.1016/S0732-8893(03)00138-X

Cano-Terriza D, Risalde MA, Rodriguez-Hernandez P, Napp S, Fernandez-Morente M, Moreno I, et al., 2018. Epidemiological surveillance of Mycobacterium tuberculosis complex in extensively raised pigs in the south of Spain. Prevent Vet Med 159: 87-91. https://doi.org/10.1016/j.prevetmed.2018.08.015

Cardoso-Toset F, Luque I, Amarilla SP, Gomez-Gascon L, Fernandez L, Huerta B et al., 2015. Evaluation of rapid methods for diagnosis of tuberculosis in slaughtered free-range pigs. Vet J 204: 232-234. https://doi.org/10.1016/j.tvjl.2015.01.022

Corner LA, 2006. The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: how to assess the risk. Vet Microbiol 112: 303-312. https://doi.org/10.1016/j.vetmic.2005.11.015

Corner LA, Barrett RH, Lepper AW, Lewis V, Pearson CW, 1981. A survey of mycobacteriosis of feral pigs in the Northern Territory. Austral Vet J 57: 537-542. https://doi.org/10.1111/j.1751-0813.1981.tb00428.x

Cuerda MM, Alonso RD, Griffa MN, Colombatti Olivieri N, Mon MA, Romano ML et al., 2019. Development and validation of an enzyme-linked inmunosorbent assay (ELISA) for the diagnosis of porcine tuberculosis. IABIMO, UE INTA-CONICET, Castelar, Buenos Aires, Argentina.

Di Marco V, Mazzone P, Capucchio MT, Boniotti MB, Aronica V, Russo M, et al., 2012. Epidemiological significance of the domestic black pig (Sus scrofa) in maintenance of bovine tuberculosis in Sicily. J Clin Microbiol 50: 1209-1218. https://doi.org/10.1128/JCM.06544-11

Diez-Delgado I, Rodriguez O, Boadella M, Garrido JM, Sevilla IA, Bezos J, et al., 2017. Parenteral vaccination with heat-inactivated Mycobacterium bovis reduces the prevalence of tuberculosis-compatible lesions in farmed wild boar. Transbound Emerg Dis 64: e18-e21. https://doi.org/10.1111/tbed.12526

Garrido JM, Sevilla IA, Beltran-Beck B, Minguijon E, Ballesteros C, Galindo RC, et al., 2011. Protection against tuberculosis in Eurasian wild boar vaccinated with heat-inactivated Mycobacterium bovis. PloS one 6: e24905. https://doi.org/10.1371/journal.pone.0024905

Gortazar C, Vicente J, Gavier-Widen D, 2003. Pathology of bovine tuberculosis in the European wild boar (Sus scrofa). The Vet Record 152: 779-780. https://doi.org/10.1136/vr.152.25.779

Gortazar C, Vicente J, Samper S, Garrido JM, Fernandez-De-Mera IG, Gavin P, et al., 2005. Molecular characterization of Mycobacterium tuberculosis complex isolates from wild ungulates in south-central Spain. Vet Res 36: 43-52. https://doi.org/10.1051/vetres:2004051

Griffa N, Moyano RD, Canal AM, Traveria GE, Santangelo MP, Alonso N, Romano MI, 2020. Development and diagnostic validation of an ELISA based on an antigenic mixture for the detection of bovine tuberculosis. Vet J 256: 105426. https://doi.org/10.1016/j.tvjl.2020.105426

Hermans PW, Schuitema AR, Van Soolingen D, Verstynen CP, Bik EM, Thole JE, et al., 1990. Specific detection of Mycobacterium tuberculosis complex strains by polymerase chain reaction. J Clin Microbiol 28: 1204-1213. https://doi.org/10.1128/jcm.28.6.1204-1213.1990

Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S et al., 1997. Simultaneous detection and strain differentiation of r diagnosis and epidemiology. J Clin Microbiol 35: 907-914. https://doi.org/10.1128/jcm.35.4.907-914.1997

Martín-Hernando MP, Höfle U, Vicente J, Ruiz-Fons F, Vidal D, Barral M, et al., 2007. Lesions associated with Mycobacterium tuberculosis complex infection in the European wild boar. Tuberculosis (Edinb) 87: 360-367. https://doi.org/10.1016/j.tube.2007.02.003

Naranjo V, Gortazar C, Vicente J, de la Fuente J, 2008. Evidence of the role of European wild boar as a reservoir of Mycobacterium tuberculosis complex. Vet Microbiol 127: 1-9. https://doi.org/10.1016/j.vetmic.2007.10.002

Neill SD, Skuce RA, Pollock JM, 2005. Tuberculosis-New light from an old window. J Appl Microbiol 98: 1261-1269. https://doi.org/10.1111/j.1365-2672.2005.02599.x

Nol P, Wehtje ME, R. A. Bowen, S. Robbe-Austerman, T. C. Thacker, K. Lantz, et al., 2020. Effects of inactivated Mycobacterium bovis vaccination on Molokai-origin wild pigs experimentally infected with virulent M. bovis. Pathogens 9(3): 199. https://doi.org/10.3390/pathogens9030199

Nugent G, Yockney IJ, Whitford EJ, 2011. Intraspecific transmission of Mycobacterium bovis among penned feral pigs in New Zealand. J Wildlife Dis 47: 364-372. https://doi.org/10.7589/0090-3558-47.2.364

Nugent G, Whitford J, Yockney IJ, Cross ML, 2012. Reduced spillover transmission of Mycobacterium bovis to feral pigs (Sus scofa) following population control of brushtail possums (Trichosurus vulpecula). Epidemiol Infect 140: 1036-1047. https://doi.org/10.1017/S0950268811001579

Nugent G, Gortazar C, Knowlesn G, 2015. The epidemiology of Mycobacterium bovis in wild deer and feral pigs and their roles in the establishment and spread of bovine tuberculosis in New Zealand wildlife. N Zeal Vet J 63(S1): 54-67. https://doi.org/10.1080/00480169.2014.963792

Palmer MV, Waters WR, 2006. Advances in bovine tuberculosis diagnosis and pathogenesis: what policy makers need to know. Vet Microbiol 112: 181-190. https://doi.org/10.1016/j.vetmic.2005.11.028

Pesciaroli M, Alvarez J, Boniotti MB, Cagiola M, Di Marco V, Marianelli C, et al., 2014. Tuberculosis in domestic animal species. Res Vet Sci 97(S): S78-85. https://doi.org/10.1016/j.rvsc.2014.05.015

Santos N, Correia-Neves M, Ghebremichael S, Kallenius G, Svenson SB, Almeida V, 2009. Epidemiology of Mycobacterium bovis infection in wild boar (Sus scrofa) from Portugal. Journal of wildlife diseases, 45, 1048-1061. https://doi.org/10.7589/0090-3558-45.4.1048

SENASA, 2012. Plan nacional de control y erradicación de la tuberculosis bovina http://www.senasa.gob.ar/normativas/resolucion-128-2012-senasa-servicio-nacional-desanidad-y-calidad-agroalimentaria

Smith NH, 2012. The global distribution and phylogeography of Mycobacterium bovis clonal complexes. Infection, genetics and evolution. J Mol Epidemiol Evol Genet Infect Dis 12: 857-865. https://doi.org/10.1016/j.meegid.2011.09.007

Smith NH, Kremer K, Inwald J, Dale J, Driscoll JR, Gordon SV, et al., 2006. Ecotypes of the Mycobacterium tuberculosis complex. J Theor Biol 239: 220-225. https://doi.org/10.1016/j.jtbi.2005.08.036

Torres PM, 2016. Situación de la tuberculosis bovina en la Republica Argentina. SENASA, https://www.senasa.gob.ar/normativas/resolucion-128-2012-senasa-servicio-nacional-de-sanidad-y-calidad-agroalimentaria.

Zumarraga MJ, Arriaga C, Barandiaran S, Cobos-Marin L, de Waard J, Estrada-Garcia I, et al., 2013. Understanding the relationship between Mycobacterium bovis spoligotypes from cattle in Latin American countries. Res Vet Sci 94: 9-21. https://doi.org/10.1016/j.rvsc.2012.07.012

Published
2022-01-26
How to Cite
CuerdaM. X., ColombattiM. A., GravisacoM. J., MarfilM. J., BarandiaranS., SevillaI. A., GarridoJ. M., MoyanoR. D., ZumarragaM. J., RomanoM. I., JusteR. A., & SantangeloM. de la P. (2022). Pathogenesis of domestic pigs submitted to mycobacterial sensitizations previous to experimental infection with Mycobacterium bovis. Spanish Journal of Agricultural Research, 20(1), e0502. https://doi.org/10.5424/sjar/2022201-18479
Section
Animal health and welfare