SciELO - Scientific Electronic Library Online

vol.53 número3La infección por Leishmania (L.) amazonensis afecta parámetros reproductivos y fetales en ratones hembrasCaracterísticas clínicas y microbiológicas de infecciones del torrente sanguíneo en pacientes adultos neutropénicos índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados




  • No hay articulos citadosCitado por SciELO

Links relacionados


Revista argentina de microbiología

versión impresa ISSN 0325-7541versión On-line ISSN 1851-7617

Rev. argent. microbiol. vol.53 no.3 Ciudad Autónoma de Buenos Aires set. 2021



First report of pathogenic Leptospira spp. in Tadaridabrasiliensis bats (family Molossidae) and Eptesicus furinalis (family Vespertilionidae) of Argentina. New host species in this country?

Primer reporte de Leptospira spp. patógena en murciélagos Tadaridabrasiliensis (familia: Molossidae) y Eptesicusfurinalis (familia: Vespertilionidae) en Argentina. ¿Nuevas especies hospedadoras en el país?

Vanina Saraullo1 

Sylvia GruneLoffler1 

Florencia Pastorino1 

Olivia Watanabe1 

Maria Laura Alonso1 

Micaela Hamer1 

Cecilia Moreira1 

Mara Martinez1 

Gustavo Martinez1 

Bibiana Brihuega1 

1 Laboratory of Leptospirosis, Institute of Pathobiology, National Institute of Agricultural Technology (INTA), Nicolás Repetto and Reseros w/n, Hurlingham, Buenos Aires, Argentina b National Research Council of Argentina (CONICET), Godoy Cruz 2290, Buenos Aires, Argentina c Urban Zoonoses Division, Ministry of Health of the Buenos Aires Province, Italia N° 324 Avellaneda, Buenos Aires, Argentina


Leptospirosis is an endemic disease caused byLeptospiraspp., a bacterium that affects animals and humans. In recent years, the number of reports of leptospirosis in wild animals has increased, which highlights the need to study the infectious agents in these animals. In this study, a duplex PCR for the detection of leptospiral DNA was performed on 50 kidney samples from bats, and a MAT (Microscopic Agglutination Test) for serological detection of anti-leptospiral antibodies was applied to 47 serum samples from bats from different regions of Buenos Aires Province, Argentina.

DNA was extracted using Chelex-100 and duplex PCR was performed by targeting the detection of genessecYandflaB, of pathogenicLeptospiraspp. Of the 50 kidney samples, 3 were positive forEumopssp. andTadaridabrasiliensisby duplex PCR. Of the 47 serum samples, 12 were positive for different serovars:Leptospira interrogansserovars Icterohaemorrhagiae, Cynopteri and Bataviae, andLeptospira borgpeterseniiserovar Ballum. This is the first report of the detection of pathogenic leptospires by serology in bats belonging to theT. brasiliensisandEptesicus furinalisspecies in Argentina. In addition, this is the first report of the detection of pathogenic leptospiral DNA by PCR inT. brasiliensisspecies. The detection ofLeptospiraspp. in these wild animals shows that they may play an important role as wildlife reservoirs of leptospires.

Keywords: Bats Leptospira spp. PCR Serology Wildlife.


La leptospirosis es una enfermedad endémica causada porLeptospiraspp., una bacteria que afecta a animales y a humanos. En los últimos años, el número de reportes de leptospirosis en animales silvestres ha aumentado, lo que resalta la necesidad de analizar los agentes infecciosos en estos animales. En este estudio, se aplicó una reacción en cadena de la polimerasa (PCR) dúplex para la identificación del ADN leptospiral en 50 muestras de riñones de murciélagos y la prueba de aglutinación microscópica (MAT) para la detección serológica de anticuerpos antileptospira en 47 muestras de suero de murciélagos de diferentes regiones de la provincia de Buenos Aires, Argentina. El ADN fue extraído usando Chelex-100 y la PCR dúplex estuvo dirigida a la detección de los genessecYyflaBdeLeptospiraspp. patógena. De las 50 muestras de riñón, tres resultaron positivas por PCR dúplex paraEumopssp. yTadaridabrasiliensis. De las 47 muestras de suero, 12 fueron positivas a diferentes serovares:LeptospirainterrogansserovaresIcterohaemorrhagiae, Cynopteri y Bataviae, yLeptospiraborgpeterseniiserovarBallum. Este es el primer reporte de detección de leptospiras patógenas por serología en murciélagos pertenecientes a las especiesT. brasiliensisyEptesicusfurinalisen Argentina. Además, también es el primero en la localización de ADN leptospiral por PCR en la especieT. brasiliensis.La identificación deLeptospiraspp. en estos animales silvestres muestra que pueden desempeñar un papel importante como reservorios de leptospiras en la fauna silvestre.

Palabras clave: Murciélagos Leptospira spp; PCR Serología Animales silvestres


Leptospirosis is a zoonotic disease caused by pathogenic strains of the genusLeptospiraspp. Currently, the genus comprises 35 species34with more than 300 serovars according to the composition of their lipopolysaccharide (LPS)21.

Recent reports show that leptospirosis has a global effect in terms of risk on human health27,36. In humans, the disease may vary from a flu-state to severe multiorgan involvement. In livestock animals, the disease can cause large economic losses due to reproductive failures, mainly in cattle production.

Transmission may occur by direct or indirect contact with urine or water contaminated with strains of pathogenic leptospires. Urine infected with leptospires is spread through the environment by reservoir hosts (mainly rodents), wild animals or domestic animals that can participate in the complex epidemiological cycle of leptospirosis as reservoirs and carrier hosts5,21,22.

Since the 1940s, most EID (Emerging Infectious Diseases) events have originated in wildlife, and of all EIDs zoonoses from wildlife represent the most significant ones, as they imply a growing threat to global health16. Zoonotic pathogens have been identified in carnivores, rodents, primates, bats and other wild animals39and their incidence has continued to increase16.

Due to their abundance and broad spatial distribution, bats have been involved in numerous EID events, and are increasingly recognized as important reservoir hosts for bacteria, rickettsiae and viruses (alphaviruses, flaviviruses, rhabdoviruses and arenaviruses)8,23,28. However, the role of bats as hosts of bacterial zoonotic agents is almost unknown.

In many regions of Latin America, people live in precarious neighborhoods establishing ideal ecological conditions for the transmission of zoonotic diseases, mainly from synanthropic animals such as rodents and bats. In this context, bats have been postulated as possible sources of leptospiral infection11,40.

Leptospira interrogans, a typical rodent-borneLeptospiraspecies has been detected in frugivorous and insectivorous bats, and therefore, the transmission between rodents and bats has been suggested19,25. Thus, indirect transmission ofLeptospiraspp. to humans may also occur through bat-borne pathogenic strains and other animal-associated leptospires, in particular rodents that reside or forage under bat roosts25,33.

However, direct transmission has not been evidenced38. Currently, Argentina has few data of leptospirosis in bats, although there is existing evidence of the important role that these animals play in the transmission of different zoonotic diseases.

The aim of this work was to detect leptospiral DNA by PCR and anti-Leptospira antibodies by serology in bats from Argentina.

Materials and methods

Sampling area

Bats, dead and stored at 4-5°C, were received at the Urban Zoonoses Laboratory of the Ministry of Health of Avellaneda (Buenos Aires Province, Argentina) and Pasteur Zoonosis Institute (Buenos Aires City, Argentina).

A total of 50 animals (collected between 2015 and 2018) were used in this study: 44 samples belonged to the family Molossidae and 6 samples belonged to the family Vespertilionidae (Table 1). In each case, both kidneys were extracted with sterile dissection forceps and scissors, placed in a dry sterile Eppendorf tube and preserved at −20°C. These samples were collected from different locations of Buenos Aires Province (Fig. 1, supplementary material), and were received in the Laboratory of Leptospirosis, OIE Reference Center, located at the Institute of Pathobiology (National Institute of Agricultural Technology, Castelar-INTA Buenos Aires, Argentina) for their processing. In addition, 47 serum samples (collected between 2012 and 2013) were submitted to detect anti-Leptospira antibodies.

Sex/age group: both samples young, female. Collection site (year): San Nicolás and Morón, B.A. (2017).

Molecular detection using duplex PCR

DNA was extracted from the kidney samples using 150μl of 5% solution of Chelex-100®15(Biorad USA). Incubation was performed at 56°C for 20min and 100°C for 8min. Later, the samples were centrifuged at 10000rpm for 5s and 100μl of the supernatant was collected in 1.5ml tubes and stored at −20°C until use.

Duplex PCR was performed using primers G1:G2 (G1: 5′-CTGAATCGCTGTATAAAAGT-3′; 5′-G2:GCAAAACAAATGGTCGGAAG-3′), and B64I-B64II (B64I: 5′-CTGAATTCTCATCTCAACTC-3′ and B64II: 5′-GCAGAAATCAGATGGACGAT-3′) (modified from Gravekamp et al., 1993)13which amplify a fragment of 285bp and 563bp fromsecYandflaBrespectively13. The PCR reaction was carried out according to Grune et al. (2015)15. Amplification products were analyzed by electrophoresis in 2% agarose gel stained with ethidium bromide, followed by exposure to UV light (Uvi Tec transilluminator BTS-20.M). Amplicon sizes were estimated using a 100bp ladder (Embiotec, Buenos Aires, Argentina).

Microscopic Agglutination Test (MAT)

The serum samples from 47 bats were tested against a panel of 23 serovars ofLeptospiraspp. by MAT. The panel was composed by the following serovar-reference strains: Australis-Ballico; Autumnalis-Akiyami A; Castellonis-Castellon III; Bataviae-Swart; Canicola-Hond Utrecht IV; Celledoni-Celledoni; Cynopteri-3522C; Djasiman-Djasiman; Grippotyphosa-Mosvka V; Hebdomadis-Hebdomadis; Icterohaemorrhagiae-RGA; Javanica-Veldrat Batavia 46; Louisiana-LSU 1945; Manhao-Manhao; Mini-Sari; Panam-CZ 214K; Pomona-Pomona; Pyrogenes-Salinem; Ranarum-ICF; Sarmin-Sarmin; Wolffi-Wolffi 3705; Shermani-LT 821 and Tarassovi-Perepelicin.

Initial serum dilution in phosphate buffered saline (PBS buffer) was 1:25.


Duplex PCR was performed on 50 samples and a positive result was observed in 3 of them. We observed the amplification of a 285bp fragment without amplification of the negative control. DNA integrity of negative samples was controlled by electrophoresis in 1% agarose gel and PCR for the 16S rRNA gene (data not shown).

The morphological analysis of the bats coincides with the taxonomic codes published in Barquez et al., and showed that the positive specimens belonged to theEumops(1 animal) andTadaridabrasiliensis(2 animals), both from family Molossidae (Table 1).

Of the 47 serum samples tested by MAT, only 12 were positive forL. interrogansserovar-reference strains: Icterohaemorrhagiae-RGA, Bataviae-Swart, Castellonis-Castellon III, Cynopteri-3522 with titers greater than or equal to 1:25 (Table 2).

The morphological analysis of the bats showed that the 9 positive specimens belonged to speciesEptesicus furinalis(family Vespertilionidae), and 3 toT. brasiliensis(family Molossidae).


Different research works have estimated that 60% of the emerging pathogens that affect humans are zoonotic, and that 70% of them originate in wildlife16. This demonstrates the importance of wild animals in several epidemiological cycles of pathogens included in human and domestic animal diseases.

In the last years, the expansion of urban areas, the increase in population density, the worldwide trips and traffic of wild fauna are some of the causes for the rise in contact between wild animals and humans36. Many wild animals carry leptospires, which they can spread into the environment by their elimination in the urine37.

In Argentina, pathogenic strains ofLeptospiraspp. were isolated and identified by molecular genotyping (MLVA) from wild boars (Sus scrofa)6, rodents (Rattus norvegicus,Rattus rattus)14, arboreal squirrels (Callosciuruserythraeus)12, gray foxes (Lycalopex griseus)32, skunks (Conepatuschinga)31, weasels (Didelphys albiventris)5, and armadillos (Chaetophractusvillosus)1; strains of serovar Icterohaemorrhagiae have been repeatedly isolated from these wild animals1,2.

Within the wild animals, bats (Chiroptera) have been implicated in numerous emerging infectious disease events and are increasingly being recognized as important reservoir hosts for rickettsiae, bacteria and viruses8,23,28.

In several Latin American countries, the presence of pathogenic leptospiral DNA in bats has been detected by PCR. Mexico reported leptospiral DNA ofLeptospira noguchiiandLeptospira weiliiin bats11, being the first country to detect species of pathogenic leptospires in flying mammals in North America. Peru reportedL. interrogans,Leptospira borgpetersenii,Leptospira kirschneriand the intermediate speciesLeptospirafainei7,25(view Fig. 2, supplementary material).

Due to changes in their habitat and expansion of urban areas, the distribution of these animals has changed and has increased contact between humans and these animals. However, little is known about the role of bats as hosts for bacterial zoonotic diseases8.

With regard to the serological techniques, the MAT is widely used to detect antibodies against leptospires, as it is considered the gold standard test for the OIE (World Organization for Animal Health). Positive serology has been reported in Argentina from wild animals such as the large hairy armadillo (C. villosus)17, the water buffalo (Bubalus bubalis)18and the nutria (Myocastor coypus)24.

The presence of anti-Leptospira antibodies in bats in some countries of Latin America such as Trinidad and Tobago, Grenada and Brazil, has been detected with titers varying from 1:100 to 1:1600 against different serovars ofLeptospiraspp9,26,35,40(Fig. 2, supplementary material). As in many other diseases, the presence of seroreactivity does neither imply clinical disease in these animals nor a role as maintenance hosts of this pathogen, but rather evidences that these bats have been in contact with leptospires in their environment.

Currently, there is scant information in Argentina ofLeptospiraspp. in bats. The only available report is from Ramirez29, who reported the presence of leptospiral DNA in kidney samples from bats of suburban areas (northern region of Argentina), in individuals belonging toMolossus rufus(Black mastiff bat) andEumopspatagonicus(Patagonian dwarf bonneted bat), both from family Molossidae, andMyotis albescens(Silver-tipped myotis) family Verspertilionidae.

In this work, we report the first detection of leptospiral DNA of pathogenic leptospira inT. brasiliensis,a bat species from Argentina belonging to family Molossidae.

Furthermore, we also report the first serological detection in Argentina inT. brasiliensisandE. furinalis(family Vespertilionidae). We found antibodies against leptospiral serovars Icterohaemorrhagiae, Ballum, Cynopteri and Bataviae (Table 2). This finding constitutes a milestone in the leptospiral research in our country as there have been no serological data in bats to the present date. Furthermore, this is the first report inE. furinalisspecies in South America, and the first report in bats of urban areas from the central region of our country.

It is interesting to highlight that these serovars are usually associated with other animal hosts, such as rodents (Icterohaemorrhagiae)1, canines (Icterohaemorrhagiae and Castellon)1, weasels (Didelphys albiventris) (Bataviae)1and pigs (Castellon, Icterohaemorrhagieae)2. In many regions, cattle are infected byLeptospira borgpeterseniiserovar Hardjobovis (serovar usually associated with bovines) and serovars Pomona and Grippotyphosa2. The high diversity of serovars found in domestic and wild animals such as bats, reveals the high-genetic diversity of this genus. This is congruent with Lei et al.20, who proposed that leptospires found in bats are structured by geography rather than by the phylogenetic relationships of their hosts.

T. brasiliensisandE. furinalisare widely distributed in South America. WhileTadaridaspp. is known to be distributed from western Venezuela, Colombia, Ecuador, Peru, Bolivia, Paraguay, southern Brazil, Chile and Argentina30,Eptesicusspp. has a wide distribution in the neotropical region except the western slope of the Andes Mountains in Peru, Bolivia and Chile3,10. In ArgentinaT. braziliensishas been sighted throughout the country, except in Chaco, Corrientes and Tierra del Fuego Provinces. In addition,E. furinalisis distributed from the north of Argentina to La Pampa Province4.

The Urban Zoonosis Laboratory in the province of Buenos Aires received 513 animals from family Molossidae and 76 from family Vespertilionidae between 2015 and 2018, which shows the need to continue studying these families of bats in Argentina. These finding of leptospires in the speciesT. brasiliensisandE. furinalisis of great importance, since they are two of the most frequently seen species and of which there are numerous records within these bats circulating in the country3.

We also highlight that the isolation and genomic studies of the leptospires circulating in the sampling areas are necessary tools for the identification and confirmation that these pathogenic strains could be circulating among different wildlife species knowing that the distribution of these wild animals is important from an ecological approach, but even more so from an epidemiological point of view since it allows us to understand the distribution of many zoonotic agents, including the agentLeptospiraspp.

Conflict of interest

The authors declare that they have no conflicts of interest.


We thank M. Ayelen Lutz, PhD, in Natural Sciences, Argentine Bat Conservation Program (ABCP) for her valuable input as well as for her logistical support. We are also grateful for the sponsorship of the National Institute of Agricultural Technology (INTA), National Animal Health Program PNSA 1115052. Vanina Saraullo has a CONICET Doctoral Scholarship.


1 Asociación Argentina de Veterinarios de Laboratorios de Diagnóstico (AAVLD). Comisión Científica Permanente de Leptospirosis de la República Argentina Informe sobre Leptospirosis en la República Argentina. Serie enfermedades Transmisibles. [ Links ]

2 Asociación Argentina de Veterinarios de Laboratorios de Diagnóstico (AAVLD). Comisión Científica de Leptospirosis.Informe sobre Leptospirosis, (2016), [ Links ]

3 Barquez R., M. Mares, J. Braun. The bats of Argentina. Spec Publ Mus Texas Tech Univ, 42 (1999), pp. 117-123 [ Links ]

R.M. Barquez, M.M. Diaz, M.E. Montani, M.J. Pérez. [ Links ]

Nueva guía de los murciélagos de Argentina. Publicación Especial N° 3 PCMA (Programa de Conservación de los Murciélagos de Argentina), Tucumán, Argentina. [ Links ]

(2020), pp. 80-122 [ Links ]

B. Brihuega, M. Paván, F. Cairó, A. Venzano, C. Auteri, D. Funes, G. Romero, L. Samartino. [ Links ]

Leptospira patógena en riñón deDidelphysalbiventris(comadreja). [ Links ]

Rev Argent Microbiol, 39 (2007), pp. 1-19 [ Links ]

B. Brihuega, S. Grune, L. Samartino, G. Romero, C. Auteri, M. Martinez. [ Links ]

First isolation ofLeptospira borgpeterseniifrom fetuses of wild boars (Sus scrofa). [ Links ]

eJBIO, 13 (2017), pp. 63-66 [ Links ]

J. Bunnell, C. Hice, D. Watts, V. Montrueil, R. Tesh, J. Vinetz. [ Links ]

Detection of pathogenicLeptospiraspp infections among mammals captured in the Peruvian Amazon basin region. [ Links ]

Am J Trop Med Hyg, 63 (2000), pp. 255-258 [ Links ]

C. Calisher, J. Childs, H. Field, K. Holmes, T. Schountz. [ Links ]

Bats: important reservoir hosts of emerging viruses. [ Links ]

Clin Microbiol Rev, 19 (2006), pp. 531-545 [ Links ]

C. Everard, G. Fraser Chanpong, L. Bhagwandin, M. Race, A. James. [ Links ]

Leptospires in wildlife from Trinidad and Grenada. [ Links ]

J Wildl Dis, 19 (1983), pp. 192-199 [ Links ]| Medline [ Links ]

E.M. González. [ Links ]

Guía de campo de mamíferos de Uruguay. Introducción al estudio de los mamíferos. Vida Silvestre, Sociedad Uruguaya para la Conservación de la Naturaleza, Montevideo. [ Links ]

G. González, S. Sánchez Montes, D. Romero Salas, P. Colunga Salas, R. Gutiérrez Molina, L. León Paniagua, A. Cruz Romero. [ Links ]

Detection of pathogenicLeptospiraspecies associated with phyllostomid bats (Mammalia: Chiroptera) from Veracruz Mexico. [ Links ]

TransboundEmerg Dis, 65 (2017), pp. 773-781 [ Links ]| Medline [ Links ]

A. Gozzi, M. Guichón, V. Benitez, G. Romero, C. Auteri, B. Brihuega. [ Links ]

First isolation ofLeptospira interrogansfrom the arboreal squirrelCallosciurusserythraeusintroduced in Argentina. [ Links ]

Wildlife Biol, 19 (2013), pp. 483-489 [ Links ]

C. Gravekamp, H. Van de Kemp, M. Franzen, D. Carrington, G. Schoone, G. Van Eys, C. Everard, R. Hartskeerl, W. Terpstra. [ Links ]

Detection of seven species of pathogenic leptospires by PCR using two sets of primers. [ Links ]

J Gen Microbiol, 139 (1993), pp. 1691-1700 [ Links ]| Medline [ Links ]

S. GruneLoffler, M. Pavan, B. Vanasco, L. Samartino, O. Suarez, C. Auteri, G. Romero, B. Brihuega. [ Links ]

Genotypes of pathogenicLeptospiraspp. isolated from rodents in Argentina. [ Links ]

Mem Inst Oswaldo Cruz, 109 (2014), pp. 163-167 [ Links ]| Medline [ Links ]

S. Grune Loffler. [ Links ]

Isolation and genotypic characterization of leptospires from wild animals in three Argentine ecoregions using the Multiple-Locus Variable-number tandem repeat analysis technique (MLVA): Coincidence with genotypes from production animals. [ Links ]

K. Jones, N. Patel, M. Levy, A. Storeygard, D. Balk, J. Gittleman, P. Daszak. [ Links ]

Global trends in emerging infectious diseases. [ Links ]

Nature, (2008), pp. 990-993 [ Links ]

M. Kin, B. Brihuega, M. Fort, F. Delgado, D. Bedotti, E.B. Casanave. [ Links ]

Presence of antibodies againstLeptospiraserovars inChaetophractusvillosus(Mammalia, Dasypodidae). La Pampa Province, Argentina. [ Links ]

Rev Argent Microbiol, 47 (2015), pp. 41-46 [ Links ] | Medline [ Links ]

J. Konrad, L. Campero, G. Caspe, B. Brihuega, G. Draghi, D. Moore, G. Crudeli, M. Venturini, C. Campero. [ Links ]

Detection of antibodies againstBrucella abortus,Leptospiraspp. andApicomplexaprotozoa in water buffaloes in the Northeast of Argentina. [ Links ]

Trop Anim Health Prod, 45 (2013), pp. 1751-1756 [ Links ]| Medline [ Links ]

E. Lagadec, Y. Gomard, V. Guernier, M. Dietrich, H. Pascalis, S. Temmam, B. Ramasindrazana, S. Goodman, P. Tortosa, K. Dellagi. [ Links ]

PathogenicLeptospiraspp. in bats Madagascar and Union of the Comoros. [ Links ]

Emerg Infect Dis, 18 (2012), pp. 1696-1698 [ Links ]| Medline [ Links ]

B.R. Lei, K.J. Olival. [ Links ]

Contrasting patterns in mammal-bacteria coevolution: Bartonella and Leptospira in bats and rodents. [ Links ]

PLoSNeglTropDis, 8 (2014), pp. 27-38 [ Links ]

P. Levett. [ Links ]

Leptospirosis. [ Links ]

Clin Microbiol Rev, 14 (2001), pp. 296-326 [ Links ]| Medline [ Links ]

P. Levett. [ Links ]

Leptospirosis: a forgotten zoonosis?. [ Links ]

Clin Appl Immunol Rev, (2004), pp. 435-448 [ Links ]

J. Mackenzie, H. Field, K.J. Guyatt. [ Links ]

Managing emerging diseases borne by fruit bats (flying foxes), with particular reference to henipaviruses and Australian bat lyssavirus. [ Links ]

J ApplMicrobiol, (2003), pp. 9459-9469 [ Links ]

P. Martino, N. Stanchi, M. Silvestrini, B. Brihuega, L. Samartino, E. Parrado. [ Links ]

Seroprevalence for selected pathogens of zoonotic importance in wild nutria (Myocastor coypus). [ Links ]

Eur J Wildl Res, 60 (2014), pp. 551-554 [ Links ]

M.A. Matthias, M.M. Díaz, K.J. Campos, M. Calderon, M.R. Willig, V. Pacheco, E. Gotuzzo, R.H. Gilman, J.M. Vinetz. [ Links ]

Diversity of bat-associatedLeptospirain the Peruvian Amazon inferred by Bayesian phylogenetic analysis of 16S ribosomal DNA sequences. [ Links ]

Am J Trop Med Hyg, 73 (2005), pp. 964-974 [ Links ]

F.Q. Mayer, E.M. Dos Reis, A.V. Bezerra, C. Cerva, J. Rosa, S.P. Cibulski, R.O. Rodrigues. [ Links ]

PathogenicLeptospiraspp. in bats: molecular investigation in Southern Brazil. [ Links ]

Comp Immunol Microbiol Infect Dis, 52 (2017), pp. 14-18 [ Links ] | Medline [ Links ]

M.A. Mwachui, L. Crump, R. Hartskeerl, J. Zinsstag, J. Hattendorf. [ Links ]

Environmental and behavioural determinants of Leptopirosis transmission: a systematic review. [ Links ]

PLoSNeglTropDis, 9 (2015), pp. 2-15 [ Links ]

S.H. Newman, H.E. Field, C.E. De Jong, J.H. Epstein. [ Links ]

Investigating the role of bats in emerging zoonoses: balancing ecology, conservation and public health interests. [ Links ]

FAO animal production and health manual, (2012), pp. 1-8 [ Links ]

N.N. Ramirez, E.A. Alegre, R.M. Ruiz, M.B. De Biasio, C.E. Bastiani. [ Links ]

Detección de leptospiras patógenas en tejido renal de murciélagos de Corrientes, Argentina. [ Links ]

Rev Vet, 25 (2014), pp. 16-20 [ Links ]

N.B. Simmons. [ Links ]

Mammal species of the world: a taxonomic and geographic reference. [ Links ]

The John Hopkins University Press, (2005), pp. 312-529 [ Links ]

E. Scialfa, B. Brihuega, A. Venzano, W.E. Morris, J. Bolpe, M. Schettino. [ Links ]

First isolation ofLeptospira interrogansfromLycalopex griseus(South American Gray Fox) in Argentina shows new MLVA Genotype. [ Links ]

J Wildl Dis, 49 (2013), pp. 168-172 [ Links ]| Medline [ Links ]

E. Scialfa, B. Brihuega, W.E. Morris, M. Recavarren, S. Quintana, S. Grune, G. Romero, J. Bolpe. [ Links ]

First isolation ofLeptospira interrogansfromConepatuschingain Argentina. [ Links ]

Afr J Microbiol Res, 1 (2012), pp. 1-5 [ Links ]

L.D. Smythe, H.E. Field, L.J. Barnett, C.S. Smith, M.F. Dohnt, M.L. Symonds, M.R. Moore, P.F. Rolfe. [ Links ]

Leptospiral antibodies in flying foxes in Australia. [ Links ]

J Wildl Dis, 38 (2002), pp. 182-186 [ Links ]

R. Thibeaux, G. Iraola, I. Ferrés, E. Bierque, D. Girault, M.E. Soupé Gilbert, M. Picardeau, C. Goarant. [ Links ]

Deciphering the unexplored Leptospira diversity from soils uncovers genomic evolution to virulence. [ Links ]

MicrobGenom, 4 (2018), pp. 1-10 [ Links ]

F.B. Thirsa, A. Spichler, E.G. Berardis, A.C. Husch, M. Fernandes, M. Martos, E.S. Mouriz, D.R. Veiga, J.M. Vinetz. [ Links ]

The contribution of bats to leptospirosis transmission in São Paulo city Brazil. [ Links ]

Am J Trop Med Hyg, 82 (2010), pp. 315-317 [ Links ]

P.R. Torgerson, J.E. Hagan, F. Costa, J. Calcagno, M. Kane, M.S. Martinez Silveira, M.G. Goris, C. Stein, A.I. Ko, B. Abela Ridder. [ Links ]

Global burden of Leptospirosis: estimated in terms of disability adjusted life years. [ Links ]

PLoSNeglTropDis, 9 (2015), pp. 1-14 [ Links ]

L.S. Ullman, H. Langoni. [ Links ]

Interactions between environment, wild animals and human leptospirosis. [ Links ]

J Venom Anim Toxins Incl, 2 (2011), pp. 119-129 [ Links ]

N.A. Vashi, P. Reddy, D.B. Wayne, B. Sabin. [ Links ]

Bat-associated leptospirosis. [ Links ]

J Gen Intern Med, 25 (2010), pp. 162-164 [ Links ]| Medline [ Links ]

M.E. Woolhouse, S. GowtageSequeria. [ Links ]

Host range and emerging and reemerging pathogens. [ Links ]

Emerg Infect Dis, 12 (2005), pp. 1842-1847 [ Links ]

C.B. Zetun, J.L. Hoffmann, R.C. Silva, L.C. Souza, H. Langoni. [ Links ]

Leptospiraspp. andToxoplasma gondiiantibodies in vampire bats (Desmodusrotundus) in Botucaturegión, Brazil. [ Links ]

J Venom Anim Toxins Inc Trop, 15 (2009), pp. 547-552 [ Links ]

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License