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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

Published online by Cambridge University Press:  26 September 2019

Soanandrasana Rahelinirina ,
Mark H. Moseley Open the ORCID record for Mark H. Moseley [Opens in a new window] ,
Kathryn J. Allan ,
Emmanuel Ramanohizakandrainy ,
Sati Ravaoarinoro ,
Minoarisoa Rajerison ,
Vincent Rakotoharinome  and
Sandra Telfer
Soanandrasana Rahelinirina
Affiliation:
Plague Unit, Institut Pasteur de Madagascar, 101 Antananarivo, Madagascar
Mark H. Moseley*
Affiliation:
School of Biological Sciences, University of Aberdeen, Aberdeen, AB24 2TZ, UK
Kathryn J. Allan
Affiliation:
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, University Avenue, Glasgow, G12 8QQ, UK
Emmanuel Ramanohizakandrainy
Affiliation:
University of Antananarivo, BP 566, Ankatso, 101 Antananarivo, Madagascar
Sati Ravaoarinoro
Affiliation:
University of Antananarivo, BP 566, Ankatso, 101 Antananarivo, Madagascar
Minoarisoa Rajerison
Affiliation:
Plague Unit, Institut Pasteur de Madagascar, 101 Antananarivo, Madagascar
Vincent Rakotoharinome
Affiliation:
Ministere de l'Agriculture et de l'Elevage, BP 1453, Analakely, Antananarivo, Madagascar
Sandra Telfer
Affiliation:
School of Biological Sciences, University of Aberdeen, Aberdeen, AB24 2TZ, UK
*
Author for correspondence: Mark H. Moseley, E-mail: mark.moseley@abdn.ac.uk
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Abstract

In developing countries, estimates of the prevalence and diversity of Leptospira infections in livestock, an important but neglected zoonotic pathogen and cause of livestock productivity loss, are lacking. In Madagascar, abattoir sampling of cattle and pigs demonstrated a prevalence of infection of 20% in cattle and 5% in pigs by real-time PCR. In cattle, amplification and sequencing of the Leptospira-specific lfb1 gene revealed novel genotypes, mixed infections of two or more Leptospira species and evidence for potential transmission between small mammals and cattle. Sequencing of the secY gene demonstrated genetic similarities between Leptospira detected in Madagascar and, as yet, uncultured Leptospira strains identified in Tanzania, Reunion and Brazil. Detection of Leptospira DNA in the same animal was more likely in urine samples or pooled samples from four kidney lobes relative to samples collected from a single kidney lobe, suggesting an effect of sampling method on detection. In pigs, no molecular typing of positive samples was possible. Further research into the epidemiology of livestock leptospirosis in developing countries is needed to inform efforts to reduce human infections and to improve livestock productivity.

Keywords

AfricaMadagascarpathogenspilloverspirochaeteTanzaniaveterinaryzoonosis
Type
Research Article
Information
Parasitology , Volume 146 , Special Issue 14: BSP 2018 Autumn Symposium , December 2019 , pp. 1707 - 1713
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Copyright
Copyright © Cambridge University Press 2019 

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Footnotes

*

These first authors contributed equally to this article.

References

Allan, KJ, Halliday, JEB, Moseley, M, Carter, RW, Ahmed, A, Goris, MGA, Hartskeerl, RA, Keyyu, J, Kibona, T, Maro, VP, Maze, MJ, Mmbaga, BT, Tarimo, R, Crump, JA and Cleaveland, S (2018) Assessment of animal hosts of pathogenic Leptospira in northern Tanzania. PLoS Neglected Tropical Diseases 12, e0006444.Google Scholar
Andersson, M, Scherman, K and Råberg, L (2013) Multiple-strain infections of Borrelia afzelii: a role for within-host interactions in the maintenance of antigenic diversity? The American Naturalist 181, 545–554.Google Scholar
Bulach, DM, Zuerner, RL, Wilson, P, Seemann, T, McGrath, A, Cullen, PA, Davis, J, Johnson, M, Kuczek, E, Alt, DP, Peterson-Burch, B, Coppel, RL, Rood, JI, Davies, JK and Adler, B (2006) Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proceedings of the National Academy of Sciences of the United States of America 103, 14560–14565.Google Scholar
Costa, F, Hagan, JE, Calcagno, J, Kane, M, Torgerson, P, Martinez-silveira, MS, Stein, C, Abela-ridder, B and Ko, AI (2015) Global morbidity and mortality of leptospirosis: a systematic review. PLoS Neglected Tropical Diseases 9, e0003898.Google Scholar
Dietrich, M, Wilkinson, DA, Soarimalala, V, Goodman, SM, Dellagi, K and Tortosa, P (2014) Diversification of an emerging pathogen in a biodiversity hotspot: Leptospira in endemic small mammals of Madagascar. Molecular Ecology 23, 2783–2796.Google Scholar
Guedes, IB, de Araújo, SAA, de Souza, GO, de Souza Silva, SO, Taniwaki, SA, Cortez, A, Brandão, PE and Heinemann, MB (2019) Circulating Leptospira species identified in cattle of the Brazilian Amazon. Acta Tropica 191, 212–216.Google Scholar
Guernier, V, Lagadec, E, Cordonin, C, Le Minter, G, Gomard, Y, Pagès, F, Jaffar-Bandjee, M-C, Michault, A, Tortosa, P and Dellagi, K (2016) Human leptospirosis on Reunion Island, Indian Ocean: are rodents the (Only) ones to blame? PLOS Neglected Tropical Diseases 10, e0004733.Google Scholar
Halliday, J, Daborn, C, Auty, H, Mtema, Z, Lembo, T, Bronsvoort, BMD, Handel, I, Knobel, D, Hampson, K and Cleaveland, S (2012) Bringing together emerging and endemic zoonoses surveillance: shared challenges and a common solution. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 2872–2880.Google Scholar
Hamond, C, Pestana, CP, Medeiros, MA and Lilenbaum, W (2015) Genotyping of Leptospira directly in urine samples of cattle demonstrates a diversity of species and strains in Brazil. Epidemiology and Infection 144, 72–75.Google Scholar
ILRI (2012) Mapping of Poverty and Likely Zoonoses Hotspots. Zoonoses Report 4. Report to Department for International Development, UK. International Livestock Research Institute, Nairobi, Kenya.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Llanes, A, Restrepo, CM and Rajeev, S (2016) Whole genome sequencing allows better understanding of the evolutionary history of Leptospira interrogans serovar hardjo. PLoS ONE 11, 1–12.Google Scholar
Marshall, RB and Chereshsky, A (1996) Vaccination of dairy cattle against leptospirosis as a means of preventing human infections. Surveillance 23, 27–28.Google Scholar
Maudlin, I, Eisler, MC and Welburn, SC (2009) Neglected and endemic zoonoses. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 2777–2787.Google Scholar
Merien, F, Portnoi, D, Bourhy, P, Charavay, F, Berlioz-Arthaud, A and Baranton, G (2005) A rapid and quantitative method for the detection of Leptospira species in human leptospirosis. FEMS Microbiology Letters 249, 139–147.Google Scholar
Mgode, GF, Machang'u, RS, Mhamphi, GG, Katakweba, A, Mulungu, LS, Durnez, L, Leirs, H, Hartskeerl, RA and Belmain, SR (2015) Leptospira serovars for diagnosis of leptospirosis in humans and animals in Africa: common Leptospira isolates and reservoir hosts. PLoS Neglected Tropical Diseases 9, e0004251.Google Scholar
Moseley, M, Rahelinirina, S, Rajerison, M, Garin, B, Piertney, S and Telfer, S (2018) Mixed Leptospira infections in a diverse reservoir host community, Madagascar, 2013–2015. Emerging Infectious Diseases 24, 1137–1139.Google Scholar
Pagès, F, Kuli, B, Moiton, M-PP, Goarant, C and Jaffar-Bandjee, M-CC (2015) Leptospirosis after a stay in Madagascar. Journal of Travel Medicine 22, 136–139.Google Scholar
Picardeau, M (2017) Virulence of the zoonotic agent of leptospirosis: still terra incognita? Nature Reviews Microbiology 15, 297–307.Google Scholar
Rahelinirina, S, Léon, A, Harstskeerl, RA, Sertour, N, Ahmed, A, Raharimanana, C, Ferquel, E, Garnier, M, Chartier, L, Duplantier, J-M-M, Rahalison, L, Cornet, M and Harstkeerl, RA (2010) First isolation and direct evidence for the existence of large small-mammal reservoirs of Leptospira sp. in Madagascar. PLoS ONE 5, e14111.Google Scholar
Ratsitorahina, M, Rahelinirina, S, Michault, A, Rajerison, M, Rajatonirina, S and Richard, V (2015) Has Madagascar lost its exceptional leptospirosis free-like Status? PLoS ONE 10, e0122683.Google Scholar
Smythe, LD, Smith, IL, Smith, GA, Dohnt, MF, Symonds, ML, Barnett, LJ and McKay, DB (2002) A quantitative PCR (TaqMan) assay for pathogenic Leptospira spp. BMC Infectious Diseases 2, 13.Google Scholar
Sonada, RB, de Azevedo, SS, Soto, FRM, da Costa, DF, de Morais, ZM, de Souza, GO, Gonçales, AP, Miraglia, F and Vasconcellos, SA (2018) Efficacy of leptospiral commercial vaccines on the protection against an autochtonous strain recovered in Brazil. Brazilian Journal of Microbiology 49, 347–350.Google Scholar
Taylor, LH, Latham, SM and Woolhouse, MEJ (2001) Risk factors for human disease emergence. Philosophical Transactions of the Royal Society B: Biological Sciences 356, 983–989.Google Scholar
Thornley, CN, Baker, MG, Weinstein, P and Maas, EW (2002) Changing epidemiology of human leptospirosis in New Zealand. Epidemiology and Infection 128, 29–36.Google Scholar
Victoria, B, Ahmed, A, Zuerner, RL, Ahmed, N, Bulach, DM, Quinteiro, J, Harstkeerl, RA and Hartskeerl, RA (2008) Conservation of the S10-spc-a locus within otherwise highly plastic genomes provides phylogenetic insight into the genus Leptospira. PLoS ONE 3, e2752.Google Scholar
Woolhouse, ME and Gowtage-Sequeria, S (2005) Host range and emerging and reemerging pathogens emerging infectious diseases. Emerging Infectious Diseases 11, 1842–1847.Google Scholar
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