Serological and Molecular evidence of pathogenic Leptospira species in cattle from slaughterhouses in Veracruz State, Mexico

• Jose Luis Ochoa-Valencia Universidad Veracruzana, Facultad de Medicina Veterinaria y Zootecnia, región Veracruz. Veracruz, México
• Anabel Cruz-Romero Universidad Veracruzana, Facultad de Medicina Veterinaria y Zootecnia, región Veracruz. Veracruz, México
• Sokani Sánchez-Montes Universidad Veracruzana, Facultad de Ciencias Biológicas y Agropecuarias, región Tuxpan. Veracruz, México -Universidad Nacional Autónoma de México, Facultad de Medicina, Centro de Medicina Tropical, Unidad de Investigación en Medicina Experimental. Ciudad de México, México
• Sandra Cecilia Esparza-González Universidad Autónoma de Coahuila, Facultad de Odontología, Laboratorio de Cultivo Celular, Unidad Saltillo. Saltillo, México
• Dora Romero-Salas Universidad Veracruzana, Facultad de Medicina Veterinaria y Zootecnia, región Veracruz. Veracruz, México
• Belisario Domínguez-Mancera Universidad Veracruzana, Facultad de Medicina Veterinaria y Zootecnia, región Veracruz. Veracruz, México
• Jose Rodrigo Ramos-Vázquez Universidad Veracruzana, Facultad de Medicina Veterinaria y Zootecnia, región Veracruz. Veracruz, México
• Ingeborg Becker Universidad Nacional Autónoma de México, Facultad de Medicina, Centro de Medicina Tropical, Unidad de Investigación en Medicina Experimental. Ciudad de México, México
• Marco Torres-Castro Universidad Autónoma de Yucatán, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi”, Laboratorio de Enfermedades Emergentes y Reemergentes.Yucatán, México

DOI: https://doi.org/10.52973/rcfcv-e33201

Keywords: Leptospirosis, cattle, sentinel units, Leptospira interrogans

Abstract

Cattle raising is the most important livestock activity in Mexico, highlighting the fact that the Country is eight place worldwide in the production of bovine meat. However, cattle can be affected by leptospirosis (a bacterial disease caused by 17 species of spirochetes of the genus Leptospira), which cause reproductive problems that translate into great economic losses. Additionally, these zoonotic agents can cause a rapidly evolving febrile condition in humans, which can be solved after the first week of symptoms or could progress to develop a severe late-phase manifestations. Despite the great impact of these agents on the economy and Public Health, epidemiological surveillance against the infectious disease that cause is not present in municipal slaughterhouses (MS). Therefore, the aim of this study was to identify, using serological and molecular methods, the circulating Leptospira species in three MS in Veracruz State. The frequency of anti-Leptospira antibodies was 67.5%. Additionally, five sequences were recovered that were 99% similar to L. interrogans. This work represents the first national effort for the evaluation of MS as sentinel units, that allow establishing the diversity of species of the genus Leptospira that circulate in cattle and establishing intervention measures for workers risk mitigation, who come into contact with the fluids and organs of infected animals.

References

AJAYI, O.L.; ANTIA, R.E.; AWOYOMI, O.J.; OLADIPO, T.M.; ADEBOWALE, O.O. Cultural, histochemical, and immunohistochemical detection of pathogenic Leptospira species in the kidneys of cattle slaughtered in two abattoirs in Southwest Nigeria. J. Immunoass. Immunochem. 41(3): 337–353. 2020. https://doi.org/jqrv.

ALINAITWE, L.; KANKYA, C.; ALLAN, K. J.; RODRIGUEZ-CAMPOS, S.; TORGERSON, P.; DREYFUS, A. Bovine leptospirosis in abattoirs in Uganda: Molecular detection and risk of exposure among workers. Zoon. Publ. Health. 66(6): 636–646. 2019. https://doi.org/jqrw.

AMATREDJO, A.; CAMPBELL, R.S., TRUEMAN, K.F. A study of nephritis of beef cattle in North Queensland. Austr. Vet. J. 52(9): 398–402. 1976. https://doi.org/d4nnvv.

AZIZI, S.; TAJBAKHSH, E.; HAJIMIRZAEI, M.R.; GHOLAMI – VARNAMKHAST, M.; SADEGHIAN, H.; ORYAN, A. Evaluation of ‘white-spotted kidneys’ associated with leptospirosis by polymerase chain reaction based LipL32 gene in slaughtered cows. J. South Afric. Vet. Assoc. 83(1): 69. 2012. https://doi.org/jqrx.

BROWN, P.D.; MCKENZIE, M.; PINNOCK, M.; MCGROWDER, D. Environmental risk factors associated with leptospirosis among butchers and their associates in Jamaica. The Intern. J. Occupat. Environm. Med. 2(1): 47–57. 2011.

CABRAL-PIRES, B.; BERZIN-GRAPIGLIA, J.; MOREIRA, L.; JAEGER, L. H.; CARVALHO-COSTA, F. A.; LILENBAUM, W. Occurrence of uterine carriers for Leptospira interrogans on slaughtered cows. Microb. Pathog. 114: 163–165. 2018. https://doi.org/gc52vg.

COLÍN-ORTIZ, J.; PÉREZ-SERNA, J.; CABALLERO-SERVÍN, A.; GARCÍA-ROMERO, J.; IBARRA-LÓPEZ, L.; CUELLAR-ESPINOZA, J.; BERNAL-VÉLEZ, C. Seroprevalencia a leptospiras en grupos de riesgo de Guadalajara, Jalisco. Enferm. Infecc. Microbiol. 24(2): 134–137. 2004.

CAMPOS-HERNANDEZ, E.; GUTIERREZ, I.; DIAZ, R. Serologic frequency of bovine leptosirosis in the Cd. Altamirano, Guerrero State, Mexico abattoir. Vet. Mex. 26(3): 175–182.1995.

COSTA, F.; HAGAN, J.E.; CALCAGNO, J.; KANE, M.; TORGERSON, P.; MARTINEZ-SILVEIRA, M.S.; STEIN, C.; ABELA-RIDDER, B.; KO, A.I. Global Morbidity and Mortality of Leptospirosis: A Systematic Review. Plos Neglect. Trop. Dis. 9(9): e0003898. 2015. https://doi.org/b7sd.

DOGONYARO, B.B.; VAN HEERDEN, H.; POTTS, A.D.; KOLO, B.F.; LOTTER, C.; KATSANDE, C.; FASINA, F.O.; KO, A.I.; WUNDER, E.A. JR.; ADESIYUN, A.A. Seroepidemiology of Leptospira infection in slaughtered cattle in Gauteng Province, South Africa. Trop. Anim. Health Prod. 52(6): 3789–3798. 2020. https://doi.org/jqr3.

ELLIS, W.A. Animal leptospirosis. Current Topics Microbiol. Immunol. 387: 99–137. 2015. https://doi.org/jqr4.

ELLIS, W.A.; NEILL, S.D.; O’BRIEN, J.J.; CASSELLS, J.A.; HANNA, J. Bovine leptospirosis: microbiological and serological findings in normal fetuses removed from the uteri after slaughter. The Vet. Rec. 110(9): 192–194. 1982. https://doi.org/c547rj.

ELLIS, W.A.; SONGER, J.G.; MONTGOMERY, J.; CASSELLS, J.A. Prevalence of Leptospira interrogans serovar Hardjo in the genital and urinary tracts of non-pregnant cattle. The Vet. Rec. 118(1): 11–13. 1986. https://doi.org/bhhff7.

ELLIS, W.A.; THIERMANN, A.B.; MONTGOMERY, J.; HANDSAKER, A.; WINTER, P.J.; MARSHALL, R.B. Restriction endonuclease analysis of Leptospira interrogans serovar Hardjo isolates from cattle. Res. Vet. Sci. 44(3): 375–379. 1988. https://doi.org/jqr5.

FANG, F.; COLLINS-EMERSON, J.M.; CULLUM, A.; HEUER, C.; WILSON, P. R.; BENSCHOP, J. Shedding and seroprevalence of pathogenic Leptospira spp. in sheep and cattle at a New Zealand Abattoir. Zoon. Public. Health. 62(4): 258–268. 2015. https://doi.org/f68kb5.

FANG, F.; COLLINS-EMERSON, J.M.; HEUER, C.; HILL, F.I.; TISDALL, D.J.; WILSON, P.R.; BENSCHOP, J. Interlaboratory and between-specimen comparisons of diagnostic tests for leptospirosis in sheep and cattle. J. Vet. Diag. Invest. Offic. Publicat. Ame. Assoc. Vet. Lab. Diagnost. 26(6): 734–747. 2014. https://doi.org/jqr6.

FERESU, S.B. Isolation of Leptospira interrogans from kidneys of Zimbabwe beef cattle. The Vet. Rec. 130(20): 446–448. 1992. https://doi.org/d8r78r.

FERESU, S.B.; BOLIN, C.A.; KORVER, H. A new leptospiral serovar, ngavi, in the Tarassovi serogroup isolated from Zimbabwe oxen. Intern. J. Systemat. Bacteriol. 48 (1): 207–213. 1992. https://doi.org/fw6zwf.

FERESU, S.B.; KORVER, H.; RIQUELME, N.; BARANTON, G.; BOLIN, C.A. Two new leptospiral serovars in the Hebdomadis serogroup isolated from Zimbabwe cattle. Intern. J. Systemat. Bacteriol. 46(3): 694–698. 1996. https://doi.org/b74f7b.

GAMAGE, C.D.; KOIZUMI, N.; PERERA, A.K.; MUTO, M.; NWAFOR-OKOLI, C.; RANASINGHE, S.; KULARATNE, S.A.; RAJAPAKSE, R.P.; KANDA, K.; LEE, R.B.; OBAYASHI, Y.; OHNISHI, M.; TAMASHIRO, H. Carrier status of leptospirosis among cattle in Sri Lanka: a zoonotic threat to public health. Transbound. Emerg. Dis. 61(1): 91–96. 2014. https://doi.org/f5npb8.

GONZALEZ, H.E.; CROWELL, W.A.; CAUDLE, A.B.; THOMPSON, F.N. Morphometric studies of the bovine uterus: microscopic lesions and retrospective reproductive history. Ame. J. Vet. Res. 46(12): 2588–2595. 1985.

GRÉGOIRE, N.; HIGGINS, R.; ROBINSON, Y. Isolation of leptospires from nephritic kidneys of beef cattle at slaughter. Ame. J. Vet. Res. 48(3): 370–371. 1987.

GUEDES, I.B.; ARAÚJO, S.; DE SOUZA, G.O.; DE SOUZA-SILVA, S.O.; TANIWAKI, S.A.; CORTEZ, A.; BRANDÃO, P.E.; HEINEMANN, M.B. Circulating Leptospira species identified in cattle of the Brazilian Amazon. Acta Trop. 191: 212–216. 2019. https://doi.org/jqr7.

HAAKE, D.A.; LEVETT, P.N. Leptospirosis in humans. Curr. Trop. Microbiol. Immunol. 387: 65–97. 2015. https://doi.org/bmhq.

HORTON, K.C.; WASFY, M.; SAMAHA, H.; ABDEL-RAHMAN, B.; SAFWAT, S.; ABDEL-FADEEL, M.; MOHAREB, E.; DUEGER, E. Serosurvey for zoonotic viral and bacterial pathogens among slaughtered livestock in Egypt. Vect. Borne Zoon. Dis. 14(9): 633–639. 2014. https://doi.org/f6hq5c.

HORNSBY, R.L.; ALT, D.P.; NALLY, J.E. Isolation and propagation of leptospires at 37 degrees C directly from the mammalian host. Sci. Rep. 10:9620. 2020. https://doi.org/jqsb.

KINGSCOTE, B.F. Leptospira interrogans serovar Hardjo Infection in Cattle in the South Okanagan District of British Columbia. The Canada. Vet. J. = La Revue Vet. Canada. 26(10): 328–332. 1985.

KORBA, A.A.; LOUNICI, H.; KAINIU, M.; VINCENT, A.T.; MARIET, J.F.; VEYRIER, F.J.; GOARANT, C.; PICARDEAU, M. Leptospira ainlahdjerensis sp. nov., Leptospira ainazelensis sp. nov., Leptospira abararensis sp. nov. and Leptospira chreensis sp. nov., four new species isolated from water sources in Algeria. Intern. J. System. Evolut. Microbiol. 71(12): 005148. 2021. https://doi.org/jqsc.

LOUREIRO, A.P.; JAEGER, L.H.; DI AZEVEDO, M.; MIRAGLIA, F.; MORENO, L.Z.; MORENO, A.M.; PESTANA, C.P.; CARVALHO-COSTA, F.A.; MEDEIROS, M.A.; LILENBAUM, W. Molecular epidemiology of Leptospira noguchii reveals important insights into a One Health context. Transboun. Emerg. Dis. 67(1): 276–283. 2020. https://doi.org/jqsd.

LOUREIRO, A.P.; PESTANA, C.; MEDEIROS, M.A.; LILENBAUM, W. High frequency of leptospiral vaginal carriers among slaughtered cows. Anim. Reprod. Sci. 178: 50–54. 2017. https://doi.org/f9v84z.

MILLER, D.A.; WILSON, M.A.; BERAN, G.W. The effect of storage time on isolation of Leptospira interrogans from bovine kidneys. Journal of veterinary diagnostic investigation: J. Vet. Diagn. Invest. Offic. Publ. Ame. Assoc. Vet. Lab. 2(1): 63–65. 1990. https://doi.org/bptqxr.

MILLER, D.A.; WILSON, M.A.; BERAN, G.W. Survey to estimate prevalence of Leptospira interrogans infection in mature cattle in the United States. Ame. J. Vet. Res. 52(11): 1761–1765. 1991.

MILNER, A.R.; WILKS, C.R.; MORGAN, I.R.; ROSEN, N.E. Leptospira serogroup Hebdomadis infection as an Australian zoonosis. Austr. Vet. J. 56(2): 70–73. 1980. https://doi.org/dggsr7.

MYERS, D.M.; JELAMBI, F. Isolation and identification of Leptospira Hardjo from cattle in Argentina. Trop. Geograf. Med. 27(1): 63–70. 1975.

NALLY, J.E.; HORNSBY, R.L.; ALT, D.P.; BAYLES, D.; WILSON-WELDER, J.H.; PALMQUIST, D.E.; BAUER, N.E. Isolation and characterization of pathogenic leptospires associated with cattle. Vet. Microbiol. 218: 25–30. 2018. https://doi.org/gdmqn8.

NGBEDE, E.O.; RAJI, M.A.; KWANASHIE, C.N.; OKOLOCHA, E.C.; GUGONG, V.T.; HAMBOLU, S.E. Serological prevalence of leptospirosis in cattle slaughtered in the Zango abattoir in Zaria, Kaduna State, Nigeria. Vet. Ital. 48(2): 179–184. 2012.

NODA, A.; RODRÍGUEZ, I. DNA isolation by Chelex-100: an efficient approach to consider in leptospirosis early stages. J. Coast. Life Med. 2(6): 501–504. 2018. https://doi.org/jqsf.

ORGANIZACIÓN MUNDIAL DE SANIDAD ANIMAL (OIE). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (mammals, birds and bees). 8th. Ed. Volume 3. Chapter 3.1.12. Leptospirosis. 2018. On Line: https://bit.ly/3FFkbgs. 03/07/2022.

PICARDEAU, M. Virulence of the zoonotic agent of leptospirosis: still terra incognita?. Nat. Rev. Microbiol. 15 (5): 297–307. 2017. https://doi.org/fjb7.

PINNA, M.H.; MARTINS, G.; LOUREIRO, A.P.; LILENBAUM, W. Detection of bovine carriers of Leptospira by serological, bacteriological, and molecular tools. Trop. Anim. Health Prod. 50(4): 883–888. 2018. https://doi.org/gdbjg5.

PINTO, P.S.; PESTANA, C.; MEDEIROS, M.A.; LILENBAUM, W. Plurality of Leptospira strains on slaughtered animals suggest a broader concept of adaptability of leptospires to cattle. Acta Trop. 172: 156–159. 2017. https://doi.org/gbjw27.

PRESCOTT, J.F.; MILLER, R.B.; NICHOLSON, V.M. Isolation of Leptospira hardjo from kidneys of Ontario cattle at slaughter. Can. J. Vet. Res. = Revue Canada. Res. Vet. 51(2): 229–231. 1987.

RAHELINIRINA, S.; MOSELEY, M.H.; ALLAN, K.J.; RAMANOHIZAKANDRAINY, E.; RAVAOARINORO, S.; RAJERISON, M.; RAKOTOHARINOME, V.; TELFER, S. Leptospira in livestock in Madagascar: uncultured strains, mixed infections and small mammal-livestock transmission highlight challenges in controlling and diagnosing leptospirosis in the developing world. Parasitol. 146(14): 1707–1713. 2019. https://doi.org/jqsg.

RAJEEV, S.; ILHA, M.; WOLDEMESKEL, M.; BERGHAUS, R.D.; PENCE, M.E. Detection of asymptomatic renal Leptospira infection in abattoir slaughtered cattle in southeastern Georgia, United States. SAGE Open Med. 30(2): 1–5. 2014. https://doi.org/jqsh.

SHAFIGHI, T.; ABDOLLAHPOUR, G.; SALEHI, T.Z.; TADJBAKHSH, H. Serological and bacteriological study of leptospirosis in slaughtered cattle in north of Iran (Rasht). Afric. J. Microbiol. Res. 4(20): 2118–2121. 2010.

SHAFIGHI, T.; ZAHRAEI-SALEHI, T.; ABDOLLAHPOUR, G.; ASADPOUR, L.; AKBAREIN, H.; SALEHZADEH, A. Molecular detection of Leptospira spp. in the urine of cattle in northern Iran. Iran.J. Vet. Res. 15(4): 402–405. 2014.

SHIOKAWA, K.; WELCOME, S.; KENIG, M.; LIM, B.; RAJEEV, S. Epidemiology of Leptospira infection in livestock species in Saint Kitts. Trop. Anim. Health Prod. 51(6): 1645–1650. 2019. https://doi.org/jqsj.

SKILBECK, N.W.; FORSYTH, W.M.; DOHNT, M. Bovine leptospirosis: microbiological and histological findings in cattle at slaughter. Austr. Vet. J. 65(3): 73–75. 1988. https://doi.org/d8f8tr.

SWAI, E.S.; SCHOONMAN, L. A survey of zoonotic diseases in trade cattle slaughtered at Tanga city abattoir: a cause of Public Health concern. Asian Pacif. J. Trop. Biomed. 2(1): 55–60. 2012. https://doi.org/dp8xzj.

TAGHADOSI, V.; HOSSEINZADEH, S.; SHEKARFOROUSH, S.S.; SAMIEI, A. Prevalence of renal lesions in slaughtered cattle in Shiraz, Iran, and detection of Leptospira in them by nested PCR-RFLP. Trop. Anim. Health Prod. 48(8): 1691–1696. 2016. https://doi.org/f9fhtv.

THIBEAUX, R.; GIRAULT, D.; BIERQUE, E.; SOUPÉ-GILBERT, M.E.; RETTINGER, A.; DOUYÈRE, A.; MEYER, M.; IRAOLA, G.; PICARDEAU, M.; GOARANT, C. Biodiversity of Environmental Leptospira: Improving Identification and Revisiting the Diagnosis. Front. Microbiol. 9: 816. 2018. https://doi.org/gdjk3z.

THIERMANN, A.B. Bovine leptospirosis: bacteriologic versus serologic diagnosis of cows at slaughter. Am. J. Vet. Res. 44(12): 2244–2245. 1983.

TREML, F.; NESNALOVÁ, E. Leptospiróza jatecného skotu--sérologické a bakteriologické vysetrení [Leptospirosis in slaughter cattle serologic and bacterial study]. Vet. Med. 40(10): 305–309. 1995.

UZAL, F.A.; DOBRENOV, B.; SMYTHE, L.; NORRIS, M.; DOHNT, M.; SYMONDS, M.; O’BOYLE, D.; SCHOUTEN, F.; KELLY, W.R. A study of “white spotted kidneys” in cattle. Vet. Microbiol. 86(4): 369–375. 2002. https://doi.org/fs8j2p.

VINCENT, A.T.; SCHIETTEKATTE, O.; GOARANT, C.; NEELA, V. K.; BERNET, E.; THIBEAUX, R.; ISMAIL, N.; MOHD-KHALID, M.; AMRAN, F.; MASUZAWA, T.; NAKAO, R.; AMARA-KORBA, A.; BOURHY, P.; VEYRIER, F.J.; PICARDEAU, M. Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics. PLoS Negl Trop Dis. 13(5): e0007270. 2019. https://doi.org/ghg4zf.

VITAL-BRAZIL, J.M.; BALASSIANO, I.T.; OLIVEIRA, F.S.; COSTA, A.D.; HILLEN, L.; PEREIRA, M.M. Multiplex PCR-based detection of Leptospira in environmental water samples obtained from a slum settlement. Mem. Inst. Oswaldo Cruz. 105(3): 353–355. 2010. https://doi.org/dn8bfp.

GANGULA, R.S., PRABHU, M.M., STANLEY, W. Weil syndrome causing autoimmune haemolytic anaemia. Natl. Med. J. India. 32(2): 88–89. 2019. https://doi.org/jqsk.

BAL, A.E., GRAVEKAMP, C., HARTSKEERL, R.A., DE MEZA-BREWSTER, J., KORVER, H.; TERPSTRA, W.J. Detection of leptospires in urine by PCR for early diagnosis of leptospirosis. J. Clin. Microbiol. 32(8): 1894–1898. 1994. https://doi.org/jqsm.

NARKKUL, U.; THAIPADUNGPANIT, J.; SRILOHASIN, P.; SINGKHAIMUK, P.; THONGDEE, M.; CHAIWATTANARUNGRUENGPAISAN, S.; KRAIROJANANAN, P.; PAN-NGUM, W. Optimization of Culture Protocols to Isolate Leptospira spp. from Environmental Water, Field Investigation, and Identification of Factors Associated with the Presence of Leptospira spp. in the Environment. Trop. Med. Infect. Dis. 5(2): 94. 2020. https://doi.org/jqsn.