Clinical course and pathogenicity of a Mycobacterium avium subsp. paratuberculosis isolate from scimitar oryx (Oryx dammah) in experimentally infected rabbits

  • Edith MALDONADO-CASTRO Faculty of Veterinary Medicine and Zootechnics, National Autonomous University of Mexico, University Av. 3000, Coyoacan, 04510, Mexico City, Mexico. http://orcid.org/0000-0002-3793-4646
  • Ana L. HERNÁNDEZ-REYES Faculty of Veterinary Medicine and Zootechnics, National Autonomous University of Mexico, University Av. 3000, Coyoacan, 04510, Mexico City, Mexico. https://orcid.org/0000-0002-8159-9902
  • Beatriz ARELLANO-REYNOSO Faculty of Veterinary Medicine and Zootechnics, National Autonomous University of Mexico, University Av. 3000, Coyoacan, 04510, Mexico City, Mexico. https://orcid.org/0000-0002-3067-2719
  • Carlos G. GUTIÉRREZ Faculty of Veterinary Medicine and Zootechnics, National Autonomous University of Mexico, University Av. 3000, Coyoacan, 04510, Mexico City, Mexico. https://orcid.org/0000-0002-6098-3913
  • Marta ALONSO-HEARN Department of Animal Health, NEIKER, Basque Research and Technology Alliance (BRTA). Technology Park of Bizkaia, Parcela 812, Berreaga 1, 48160 Derio, Bizkaia, Spain. https://orcid.org/0000-0001-5979-347X
  • Gilberto CHÁVEZ-GRIS Faculty of Veterinary Medicine and Zootechnics, National Autonomous University of Mexico, University Av. 3000, Coyoacan, 04510, Mexico City, Mexico. http://orcid.org/0000-0003-1123-1878
Keywords: bacteriological culture, granulomatous lesions, IS900 PCR, real-time F57 PCR, ruminants, experimental infection

Abstract

Aim of study: To evaluate the infectivity of a MAP type C of a scimitar oryx (Oryx dammah) - included in an international conservation list - that showed clinical signs and granulomatous enteritis associated with paratuberculosis in rabbits (Oryctolagus cuniculus) using molecular, bacteriological and pathological methodologies.

Area of study: The study was made in Tequisquiapan, Queretaro, CEIEPAA, FMVZ, UNAM, Mexico.

Material and methods: Three 6-week-old female New Zealand rabbits were orally infected for 3 consecutive days with 109 CFU of the MAP isolate. Blood and fecal samples were collected every 2 weeks for a total period of 28 weeks. IS900 PCR in blood and F57 real-time PCR in the feces were performed every 2 weeks and pathological analysis and bacteriological culture from tissue were made 28 weeks post infection.

Main results: MAP was detected by IS900 PCR in the blood of two of the three animals after 2 weeks of infection and again by F57 real-time PCR in the feces of the three infected rabbits. Infection with the MAP isolates in feces at 22 and 28 weeks post infection in one rabbit and isolate of vermiform appendix resulted in the development of granulomatous lesions in the three rabbits. The lesions were diffuse intermediate in one animal and multifocal in the other two rabbits.

Research highlights: Overall, these results demonstrated the infectivity of a MAP isolate from the scimitar oryx in rabbits.

Downloads

Download data is not yet available.

References

Alowanou GG, Adenilé AD, Akouèdegni GC, Bossou AC, Zinsou FT, Akakpo GCA, et al., 2021. A comparison of Mini-FLOTAC and McMaster techniques in detecting gastrointestinal parasites in West Africa dwarf sheep and goats and crossbreed rabbits. J Appl Anim Res 49: 30-38. https://doi.org/10.1080/09712119.2021.1876703

Arrazuria R, Molina E, Mateo-Abad M, Arostegui I, Garrido JM, Juste RA, et al., 2015. Effect of various dietary regimens on oral challenge with Mycobacterium avium subsp. paratuberculosis in a rabbit model. Res Vet Sci 101: 80-83. https://doi.org/10.1016/j.rvsc.2015.06.006

Arrazuria R, Molina E, Garrido JM, Pérez V, Juste RA, Elguezabal N, 2016. Vaccination sequence effects on immunological response and tissue bacterial burden in paratuberculosis infection in a rabbit model. Vet Res 47: 1-11. https://doi.org/10.1186/s13567-016-0360-y

Badia-Bringué BG, Canive M, Casais R, Blanco VC, Amado J, Iglesias N, et al., 2022. Evaluation of a droplet digital PCR assay for quantification of Mycobacterium avium subsp. paratuberculosis DNA in whole-blood and fecal samples from MAP-infected Holstein cattle. Front Vet Sci 9: 1-13. https://doi.org/10.3389/fvets.2022.944189

Balseiro A, Perez V, Juste RA, 2019. Chronic regional intestinal inflammatory disease: A trans-species slow infection? Comp Immunol Microbiol Infect Dis 62: 88-100. https://doi.org/10.1016/j.cimid.2018.12.001

Beard PM, Rhind SM, Buxton D, Daniels MJ, Henderson D, Piral A, et al., 2001a. Natural paratuberculosis infection in rabbits in Scotland. J Comp Pathol 124: 290-299. https://doi.org/10.1053/jcpa.2001.0466

Beard PM, Stevenson K, Pirie A, Rudge K, Buxton D, Rhind SM, et al., 2001b. Experimental paratuberculosis in calves following inoculation with a rabbit isolate of Mycobacterium avium subsp. paratuberculosis. J Clin Microbiol 39: 3080-3084. https://doi.org/10.1128/JCM.39.9.3080-3084.2001

Begg DJ, Whittington RJ, 2008. Experimental animal infection models for Johne's disease, an infectious enteropathy caused by Mycobacterium avium subsp. paratuberculosis. Vet J 176: 2: 129-145. https://doi.org/10.1016/j.tvjl.2007.02.022

Cooney MA, JL Steele, Steinberg H, Talaat AM, 2014. A murine oral model for Mycobacterium avium subsp. paratuberculosis infection and immunomodulation with Lactobacillus casei ATCC 334. Front Cell Infect Microbiol 4: 1-10. https://doi.org/10.3389/fcimb.2014.00011

Daniels MJ, Ball N, Hutchings MR, Greig A, 2001. The grazing response of cattle to pasture contaminated with rabbit faeces and the implications for the transmission of paratuberculosis. Vet J 161: 306-313. https://doi.org/10.1053/tvjl.2000.0550

Daniels MJ, Henserson D, Greig A, Stevenson K, Sharp JM, Hutchings MR, 2003. The potential role of wild rabbits Oryctolagus cuniculus in the epidemiology of paratuberculosis in domestic ruminants. Epidemiol Infect 130: 553-559. https://doi.org/10.1017/S0950268803008471

DOF, 2015. NORMA Oficial Mexicana NOM 033 SAG/ZOO/2014 métodos para dar muerte a los animales domésticos y silvestres. Diario Oficial de la Federación (México) 26/08/2015.

Favila-Humara LC, Chávez-Gris G, Carrillo-Casas EM, Hernández-Castro R, 2010. Mycobacterium avium subsp. paratuberculosis detection in individual and bulk tank milk samples from bovine herds and caprine flocks. Foodborne Pathog Dis 7. https://doi.org/10.1089/fpd.2009.0374

Garrido JM, Cortabarria N, Oguiza JA, Aduriz G, Juste RA, 2000. Use of a PCR method on fecal samples for diagnosis of sheep paratuberculosis. Vet Microbiol 77: 379-386. https://doi.org/10.1016/S0378-1135(00)00323-0

Ghosh P, Shippy DC, Talaat AM, 2015. Superior protection elicited by live-attenuated vaccines in the murine model of paratuberculosis. Vaccine 33: 7262-7270. https://doi.org/10.1016/j.vaccine.2015.10.116

Greig A, Stevenson K, Henderson D, Pérez V, Hughes V, Pavlik I, et al., 1999. Epidemiological study of paratuberculosis in wild rabbits in Scotland. J Clin Microbiol 37: 1746-1751. https://doi.org/10.1128/JCM.37.6.1746-1751.1999

Hernández-Reyes AL, Chávez-Gris G, Maldonado-Castro E, Alcaraz-Sosa LE, Díaz-Negrete MT, 2022. First identification of Mycobacterium avium subsp. paratuberculosis in wild ruminants in a zoo in Mexico. Vet World 15: 655-661. https://doi.org/10.14202/vetworld.2022.655-661

Jorge M, Alito A, Bernardelli A, Canal A, Cataldi A, Cicuta M, et al., 2005. Diagnostic manual of mycobacteria of veterinary importance. A. AA de V. de L. of Diagnosis. Santa Fe, ed. AA de V. de L. of Diagnosis. Santa Fe, Argentin.

Judge J, Kyriazakis I, Greig A, Davidson RS, Hutchings MR, 2006. Routes of intraspecies transmission of Mycobacterium avium subsp. paratuberculosis in rabbits (Oryctolagus cuniculus): a field study. Appl Environ Microbiol 72: 398-403. https://doi.org/10.1128/AEM.72.1.398-403.2006

Maio E, Carta T, Balseiro A, Sevilla IA, Romano A, Ortiz JA, et al., 2011. Paratuberculosis in european wild rabbits from the Iberian peninsula. Res Vet Sci 91: 212-218. https://doi.org/10.1016/j.rvsc.2010.12.014

Mokresh AH, Czuprynski CJ, Butler DG, 1989. A rabbit model for study of Mycobacterium paratuberculosis infection. Infect Immun 57: 3798-3807. https://doi.org/10.1128/iai.57.12.3798-3807.1989

Mokresh AH, Butler DG, 1990. Granulomatous enteritis following oral inoculation of newborn rabbits with Mycobacterium paratuberculosis of bovine origin. Can J Vet Res 54: 313-319.

Pigoli C, Garbarino C, Ricchi M, Bonacina E, Gibelli L, Grieco V, et al., 2020. Paratuberculosis in captive scimitar-horned oryxes (Oryx dammah). Animals 1-11. https://doi.org/10.3390/ani10111949

Raizman EA, Wells SJ, Jordan PA, Delgiudice GD, Bey RR, 2005. Mycobacterium avium subsp. paratuberculosis from free-ranging deer and rabbits surrounding Minnesota dairy herds. Can J Vet Res: 32-38.

Ratnamohan TN, Spencer TL, 1986. A technique for the purification of Mycobacterium paratuberculosis from the ileal mucosa of infected cattle. Aust Vet J 63: 185-187. https://doi.org/10.1111/j.1751-0813.1986.tb02970.x

Roupie V, Viart S, Leroy B, Romano M, Trinchero N, Govaerts M, et al., 2012. Immunogenicity of eight Mycobacterium avium subsp. paratuberculosis specific antigens in DNA vaccinated and Map infected mice. Vet Immunol Immunopathol 145: 74-85. https://doi.org/10.1016/j.vetimm.2011.10.012

Singh PK, Singh SV, Kumar H, Sohal JS, Singh AV, 2010. Diagnostic application of IS900 PCR using blood as a source sample for the detection of Mycobacterium avium subspecies paratuberculosis in early and subclinical cases of caprine paratuberculosis. Vet Med Int 2010: 748621. https://doi.org/10.4061/2010/748621

Talaat A, Chia W, Murray E, 2020. Experimental small animal models of paratuberculosis, 2nd ed; Berh M et al. (eds). CAB Int Publ, Boston, USA.

Vaughan JA, Lenghaus C, Stewart DJ, Tizard ML, Michalski WP, 2005. Development of a Johne's disease infection model in laboratory rabbits following oral administration of Mycobacterium avium subspecies paratuberculosis. Vet Microbiol 105: 207-213. https://doi.org/10.1016/j.vetmic.2004.10.019

Whittington R, Donat K, Weber MF, Kelton D, Nielsen SS, Eisenberg S, et al., 2019. Control of paratuberculosis : who, why and how. A review of 48 countries. BMC Vet Res 4: 1-29. https://doi.org/10.1186/s12917-019-1943-4

Published
2023-09-27
How to Cite
MALDONADO-CASTRO, E., HERNÁNDEZ-REYES, A. L., ARELLANO-REYNOSO, B., GUTIÉRREZ, C. G., ALONSO-HEARN, M., & CHÁVEZ-GRIS, G. (2023). Clinical course and pathogenicity of a Mycobacterium avium subsp. paratuberculosis isolate from scimitar oryx (Oryx dammah) in experimentally infected rabbits. Spanish Journal of Agricultural Research, 21(4), e05SC01. https://doi.org/10.5424/sjar/2023214-19896
Section
Animal health and welfare