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Abanico veterinario

On-line version ISSN 2448-6132Print version ISSN 2007-428X

Abanico vet vol.11  Tepic Jan./Dec. 2021  Epub Oct 11, 2021

https://doi.org/10.21929/abavet2021.23 

Literature Review

Frequency of Leptospira spp serovars reported in horses: a literature review

Oscar Toriz-Suarez1 
http://orcid.org/0000-0003-1016-9267

Juan Pérez-Rivero*  2 
http://orcid.org/0000-0003-1078-6695

Antonio Herrera-Barragán2 
http://orcid.org/0000-0003-1492-2228

Jorge Torres-Barranca2 

German Lombardero-Goldaracena2 
http://orcid.org/0000-0002-7151-6405

1Maestría en Ciencias Agropecuarias Universidad Autónoma Metropolitana Unidad Xochimilco;

2Departamento de Producción Agrícola y Animal. Universidad Autónoma Metropolitana Unidad Xochimilco. Calzada del hueso 1100, Coyoacán CDMX, CP. 04960.


Abstract:

Equine leptospirosis has been associated with abortions, renal failure and uveitis, which constitutes a health and economic problem. However, it is generally asymptomatic, which makes this disease of little interest in equines in comparison with other domestic and wild species. At present, the real epidemiological situation of leptospirosis in equines is unknown; just as the disease develops in these animals. A search of scientific literature was carried out; with the objective of knowing which are the serovars of genus leptospira reported in equines from 2010 to 2020. In the literature review, 21 articles were selected, in which it was identified that Leptospira bratislava, is the most frequently reported (11.43%, IC 95%: 6-19.1%) is in contact with equines, followed by Leptospira icterohaemorrhagiae (9.52%, IC 95%: 4.6-16.8%).

Keywords: host; Infection; uveitis; zoonosis

Resumen:

La leptospirosis equina ha sido asociada con abortos, insuficiencia renal y uveítis, lo cual constituye un problema de salud y económico, sin embargo, de manera general es asintomática, lo cual provoca que dicha enfermedad sea de poco interés en equinos en comparación con otras especies domésticas y silvestres. En la actualidad la situación epidemiológica real de leptospirosis en equinos se desconoce; al igual que la enfermedad se desarrolla en estos animales. Se realizó una búsqueda de literatura científica; con el objetivo de conocer cuáles son las serovariedades del género leptospira reportadas en equinos desde 2010 a 2020. En la revisión de literatura se seleccionaron 21 artículos, en los cuales se identificó que Leptospira bratislava, es la que se reportó con mayor frecuencia (11.43%, IC95%: 6-19.1%), seguida por Leptospira icterohaemorrhagiae (9.52%, IC95%: 4.6-16.8%).

Palabras clave: hospedero; Infección; uveítis; zoonosis

INTRODUCTION

Leptospirosis described in 1886 by the German physician Adolph Weil, is currently one of the most widely distributed infectious diseases worldwide, bacteria of the genus Leptospira spp (Adler and de la Peña, 2010).

The frequency of leptospirosis is usually associated with bad hygiene, so its presence is more frequent in regions where activities such as agriculture, the manufacture of products of animal origin, forestry, livestock, mining, etc (Torres et al., 2016).

This disease has relevance for public and animal health, due to the participation of natural and accidental hosts, which are important for maintenance. Rodents are considered the main hosts, in addition to bovines, horses, pigs, sheep, goats, dogs and cats; as well as wild mammals (Andersen et al., 2016). Some of these meet the function of carriers, which may be able to eliminate bacteria by urine as sick individuals do, without presenting detectable clinical signs (Wood et al., 2018; Ellis, 2014; Moral et al., 2014).

In equines, leptospirosis is commonly associated with genitourinary and ophthalmic diseases in which damage to placenta and fetus, kidneys and eyes can be appreciated. In general, the clinical picture is mild or subclinical; however, in the acute way, depression, jaundice, pyrexia, while in severe infections are observed abortions, neonatal diseases or the birth of a healthy pony with antibodies against this bacterium. In some cases, perinatal mortality is presented, as well as respiratory disorders and recurrent uveitis (ERU) or iridocyclitis (Divers, et al., 2019; Arent and Kedzierska-Mięszkowska, 2013; Verma et al.,2010).

Equines are infected when consuming water contaminated with leptospira; as well as any other species when in contact with urine or other fluids of infected animals. These bacteria have the ability to enter the body through mucous membranes, skin abrasions and transplacental route, so that later they can lodge mainly in the renal tubules of animals, where they are colonizing the kidney (Khalili et al., 2019).

In later, bacteria are eliminated by urine, polluting rivers, lakes and other water sources that are used for activities aimed at trade, agriculture, livestock, included for the consumption of the human being, in this way the infection is facilitated in humans and animals (Pulido et al., 2014). In certain occasions some products, fabrics and fluids of these animals can act as a source of infection.

Hamond et al. (2013), it proposes another non-conventional path of disease transmission, through sexual contagion, because it found the presence of DNA, from Leptospira spp in equine semen, in 50% of evaluated samples and frequency of 60% for Leptospira bratislava and Leptospira Copenhageni. It is worth mentioning that, although exposure to leptospira is common, the development of equine disease occurs at rare occasions (Malalana, 2019).

At present it is not accurately known whether the conditions in the horse kidney alter the physiological functions of the bacteria and, therefore, affect their survival, generate reduction of their pathogenesis, or if there are differences in infection between males and females (Hamond et al., 2012a). However, through histopathological studies in young horses’ kidneys, the formation of petechiae and lymphocytic infiltration in the proximal tubules and glomeruli has been observed. It has also been reported that Pomona serovar, in these organs causes fever and acute renal failure (Verma et al., 2010).

The objective of this literature review was to know the frequency of leptospirosis in equines reported in the literature of the last 10 years.

METHODOLOGY

A review was carried out in web search browsers as PubMed, Science Direct, SciELO, from the scientific literature peer-reviewed and published in the last 10 years (2010-2020), the keywords used were frequency, equines, Leptospira spp, leptospirosis, infection, diagnosis, uveitis and combination of these.

Reports of serovariety, country and continent were obtained from the articles consulted; based on this, the overall frequency of positive animals and the frequency of serovars were calculated.

Then the EpiInfo 7® program was used to analyze the data, know the frequencies and 95% of confidence intervals (95% CI) of the information obtained from the scientific peer- reviewed articles (CDC, 2016).

RESULTS

In a representative sample of 21 papers, where any serovar of leptospira was detected at 7218 horses (Table 1). In these, 40 serovarieties were found (Table 2), being Leptospira bratislava the most frequently reported with 11.43% (IC 95%: 6-19.1%), followed by Leptospira icterohaemorrhagiae with 9.52%, (IC 95%: 4.6-16.8% ; which suggests that these serovarieties reported are the ones that are in contact with equines.

Table 2 Frequency of different species of leptospira reported in equines in 2010 to 2020 

Leptospira Frequency % % Accumulated 95% confidence interval
arborea 1 0.95 0.95 0.02 5.19
australis 4 3.81 4.76 1.05 9.47
autumnalis 5 4.76 9.52 1.56 10.76
ballum 2 1.90 11.43 0.23 6.71
bataviae 1 0.95 12.38 0.02 5.19
bataviae (sv. swart) 1 0.95 13.33 0.02 5.19
bratislava 12 11.43 24.76 6.05 19.11
bratislava jez-bratislava 1 0.95 25.71 0.02 5.19
butembo 1 0.95 26.67 0.02 5.19
canicola 6 5.71 32.38 2.13 12.02
celledoni 1 0.95 33.33 0.02 5.19
copenhageni 6 5.71 39.05 2.13 12.02
copenhageni y australis 1 0.95 40.00 0.02 5.19
cynopteri 1 0.95 40.95 0.02 5.19
djasiman 3 2.86 43.81 0.59 8.12
grippothyphosa (sv. duyster) 1 0.95 44.76 0.02 5.19
grippotyphosa 7 6.67 51.43 2.72 13.25
grippotyphosa moska V 1 0.95 52.38 0.02 5.19
hardjo 4 3.81 56.19 1.05 9.47
hardjo bovis 1 0.95 57.14 0.02 5.19
hardjo prajitno 3 2.86 60.00 0.59 8.12
hardjobovis/wolffi 1 0.95 60.95 0.02 5.19
hardjoprajitno H89 1 0.95 61.90 0.02 5.19
hebdomadis 2 1.90 63.81 0.23 6.71
icterohaemorrhagiae 10 9.52 73.33 4.66 16.82
javanica 1 0.95 74.29 0.02 5.19
panama 2 1.90 76.19 0.23 6.71
patoc 1 0.95 77.14 0.02 5.19
poi 1 0.95 78.10 0.02 5.19
pomona 9 8.57 86.67 3.99 15.65
portland-vere sinaloa 1 0.95 87.62 0.02 5.19
pyrogenes 1 0.95 88.57 0.02 5.19
sentot 1 0.95 89.52 0.02 5.19
seramanga 1 0.95 90.48 0.02 5.19
serjoe 2 1.90 92.38 0.23 6.71
tarassovi 3 2.86 95.24 0.59 8.12
tarassovi perepelitsin 1 0.95 96.19 0.02 5.19
topaz 1 0.95 97.14 0.02% 5.19
wolffi 2 1.90 99.05 0.23% 6.71
zanoni 1 0.95 100 0.02% 5.19

From 21 articles analyzed, it was reported that Brazil is the country where more studies have been carried out on equine leptospirosis during the last decade, with 47.62% (IC 95 %: 25.71-70.22%) as shown in Table 3.

Table 3 Frequency of reports by country with equine leptospirosis during 2010 -2020 

Country/continent Frequency % % Acumulated 95% confidence interval
Germany/Europe 1 4.76 4.76 0.12 23.82
Brazil/America 10 47.62 52.38 25.71 70.22
Chile/ America 1 4.76 57.14 0.12 23.82
Colombia/ America 2 9.52 66.67 1.17 30.38
Iran/Asia 1 4.76 71.43 0.12 23.82
Italy/Europe 1 4.76 76.19 0.12 23.82
Mexico/America 1 4.76 80.95 0.12 23.82
Northwest England and North of Wales /Europe 1 4.76 85.71 0.12 23.82
Poland /Europe 1 4.76 90.48 0.12 23.82
South Africa /Africa 1 4.76 95.24 0.12 23.82
Southern Ethiopia /Africa 1 4.76 100.00 0.12 23.82
Total 21 100 100

In Table 4, the serovar reported in the literature consulted in equines are shown during the last ten years.

Table 4 Frequency by country of leptospira infections in equines 2010 to 2020 

Author Country /continent Serovariety found Leptospira: Reported frequency (%) % positive animals 95% confidence intervalal 95%
Ali, 2012 Irán/Asia pomona 38.9 39.18
grippotyphosa 32.7 35-43.6
icterohaemorrhagiae 15.1
canicola 10.4
hardjo 1.7
ballum 1.04
Alves et al., 2016 Brasil/América patoc 35.7
butembo 32.1 28.0
sentot 14.3 20.1-37.5
Arent y Kedzierska-Mięszkowska, 2013 Polonia/Europa grippotyphosa 11.7
serjoe 4.5
bratislava 4.0
poi 3.7
pomona 3.6
icterohaemorrhagiae 2.9
celledoni 0.9
cynopteri 0.9 39.0
ballum 0.6 35.3-43.0
hebdomadis 0.6
bataviae 0.5
hardjo 0.4
zanoni 0.4
autumnalis 0.4
canicola 0.3
australis 0.3
Bedoya et al., 2013 Colombia/América bratislava 53.3
hardjo bovis 28.5
icterohaemorrhagiae hardjo prajitno 26.3 5.1 66.70
grippotyphosa 2.8 51.5-79.0
pomona 2.6
Hamond et al., 2012b Brasil/América copenhageni 43.7 71.4
icterohaemorrhagiae 27.8 62.7-78.8
Hamond et al., 2013 Brasil/América bratislava 30.0 60
copenhageni 30.0 31.3-83.2
Hamond et al., 2014a Brasil/América australis 54.4 47.8
icterohaemorrhagiae 43.6 39.5-56.1
Hamond et al., 2015 Brasil/América australis 46.4 44.7
pomona 70.5 38.0-51.5
Malalana et al., 2019 Noroeste de Inglaterra y norte de Gales/Europa bratislava 19.4 51.4
copenhageni y Australis 6.9 40.0-62.6
autumnalis 8.3
Martins et al., 2017 Brasil/América australis 69.2 48.1
icterohaemorrhagiae 30.8 35.4-61.1
Méndez et al., 2013 México/América hardjoprajitno H89 12.0 71
wolffi 12.0 50.8-85.0
tarassovi perepelitsin 41.0
grippotyphosa moska V 4.0
bratislava jez-bratislava 8.0
portland-vere sinaloa 8.0
hardjo prajitno 29.0
icterohaemorrhagiae 12.0
pomona 42.0
Peixoto Ribeiro et al., 2018 Brasil/América serjoe 5.9 32.7
seramanga 5.3 30.5-35.0
djasiman 3.9
grippotyphosa 3.9
icterohaemorrhagiae 3.6
autumnalis 2.6
Pinna et al., 2014 Brasil/América bratislava 62.3 44.9
Copenhageni 37.7 41.0-48.9
Pikalo et al., 2016 Alemania/Europa icterohaemorrhagiae 11.1 17.20
bratislava 9.6 13.4-21.8
grippotyphosa 1.9
Rey et al., 2015 Colombia/América pomona 41.5
grippotyphosa 24.5
canicola 16.0
javanica 23.4
hardjo prajitno 10.5
tarassovi 7.4
hebdomadis 7.4
wolffi 2.1
bratislava 1.1
icterohaemorrhagiae 40.4
Troncoso et al., 2013 Chile/América autumnalis 54.5
bratislava 52.7 65.5
canicola 20.0 52.2-76.6
copenhageni 12.7
hardjo 7.3
Siqueira et al., 2019 Brasil/América autumnalis 2.3
bratislava 54.5
canicola 4.5
grippothyphosa (sv. duyster) 2.27 8.0
hardjobovis/wolffi 22.7 6.6-9.7
copenhageni 2.3
panama 2.3
pomona 4.5
bataviae (sv. swart) 4.5
Simbizi et al., 2016 Sudáfrica/África bratislava 32.9
djasiman 25.8 85.0
arborea 11.0 82.1-87.6
tarassovi 7.7
De Oliveira et al., 2014 Brasil/América panama 6.2
pyrogenes 3.5 7.40
grippotyphosa 3.5 4.8-11.3
Tsegay et al., 2016 Sur de Etiopia/África bratislava 34.3
djasiman 9.8 44.0
topaz 6.0 39.3-48.8
pomona 5.3
Vera et al., 2019 Italia/Europa bratislava 41.8
canicola 63.6
tarassovi 28.4 67.2
copenhageni 17.9 58.8-74.5
pomona 10.4
hardjo 2.2

DISCUSSION

Knowing the true value of the Leptospira spp frequency from the revised articles is very complicated, there was a confidence interval from there to be able to locate 95% with a range of values among which the real value of this agent frequency in the equine population (Molina, 2013). In this study, 40 serovars of Leptospira spp in horses were identified. Although Leptospira bratislava has been the most commonly reported in the equine literature in the last 10 years (Pinna et al., 2014), Leptospira pomona is the one considered to be the specific agent for equidae, since when the individual develops the disease, high titers of antibodies against the latter can be found (Divers et al., 2019).

In the serological studies in equines, there is identified that there is variation in the frequency of infection by Leptospira (Hamond et al., 2014b); which can be submitted on the four continents reported in the study sample. The most reported infections in the literature in equines of the last 10 years were caused by Leptospira icterohaemorrahagiae, Leptospira pomona, Leptospira bratislava, Leptospira copenhageni and Leptospira grippotyphosa. These data were obtained in accordance with the analyzed papers, derived from studies, both clinical, serological and ecology of the disease, which has allowed knowing the interface between animal-human environment and its importance for the concept of a one single health (Jaeger et al., 2019). On the other hand, Bertelloni et al. (2019) mention that environmental characteristics, such as wetlands, ponds and channels present at the center of Italy, associated with the presence of domestic and wild animals (the latter as reservoirs of leptospiras) enhance the dissemination of this disease, and they are reported frequencies in pigs of 19.74% and bovines of 13.03%. It is known that leptospira are transmitted efficiently through water, being able to survive for long periods in humid environments (Lourerio et al., 2013). For its part, Verma et al., 2019 showed the existence of the interaction between the pathogen and domestic and wild animals, through water settlements, as well as the bacterium presence in kidneys of wild animals. It has been suggested that the adaptation of serovar to the host, as well as, the nearby coexistence with cattle with horses can influence the frequency of exposure (Lowe,2010). Pinna et al. (2014) demonstrate that Leptospira bratislava is adapted to equines, since this has been associated with reproductive problems in mares. However, Leptospira bratislava and Leptospira muenchen, have been associated with cases of infections in pigs, horses, bovines and dogs, and managed to identify similar strains in wild animals (Arent et al., 2016).

Witkswski et al. (2016) mention that Leptospira grippotyphosa and Leptospira pomona are associated with cases of recurrent uveitis in equines. Hashimoto et al. (2007) evaluated the prevalence of leptospirosis in equines without apparent clinical synology, and used weight loss and depression as inclusion criteria, with which they obtained 66.88% of overall frequency; of this value, antibodies represented 23.36% against Leptospira icterohaemorrhagiae and 13.14% by Leptospira grippotyphosa. While Hamond et al. (2012b) found 89.5 seroprevalence in asymptomatic horses.

The disease severity varies with the serovar and the affected animal, when the disease is presented subclinically, animal deterioration is not apparent; however, when the presence of the disease is chronic, the physical and productive deterioration of animals are evident (Ellis, 2015).

Leptospira pomona kennewicki is considered as responsible for most clinical presentations in American horses, is associated with placenta diseases and fetus, kidneys and eyes ((Divers et al., 2019); however, clinical presentation can result in abortion or in a sick colt. This can be due to the gestational mare stage and at the time it was infected with the bacteria, as well as its immunological state (Bernard, 1993). From the clinical point of view, a study conducted in Sweden showed that there is no significant association between the presence of clinical signs of disease and positive titles to Leptospira bratislava or Leptospira Icterohaemorrhagiae with exception with the association between respiratory problems and fatigue with the Leptospira Bratislava (Båverud et al., 2009). . Such is the case of Rocha (2004) in which, by obtaining samples of horse kidneys, isolations and serological typing were achieved, where it determined the presence of Leptospira australis and Leptospira pomona strains, these two strains are the ones that have been most reported in Portuguese horses.

It has been associated with the frequency of infection with Leptospira spp to environmental conditions, including seasonal variations, as an example has to be Leptospira icterohaemorrhagie are presented more frequently between months of October and December, this attributed to the rodents usually invade the stables and houses at the end of summer and autumn. On the other hand, the increase in frequency Leptospira bratislava is presented between April and June and October to December ( Båverud et al., 2009).

Leptospirosis is a neglected zoonosis with a worldwide distribution, affects many species of mammals, including livestock, causing clinical signs of acute character in animals of all ages and productive stages, which significantly affects animal production. The annual incidence of this zoonosis in humans is not well determined due to sub-notification; it is estimated as an example in Uruguay, which is 15 per 100,000 inhabitants. Human disease seems to be associated with infected animals, as well as with rains and floods in endemic regions (Zarantonelli et al., 2018).

CONCLUSIONS

In general, the literature consulted allowed knowing the disease frequency and serovars found on horses. Exposure to different serovars may be related to the region in which equines are found, as well as the presence of one or more specific hosts for these serovars which act as a reservoir so that infection is presented. Horses are infected when they consume contaminated water with some leptospira species. While exposure to these agents is common in horses, systemic disease is rare, equines can be asymptomatic or present different clinical signs. Frequently reported leptospira species that can infect horses are, Leptospira bratislava, (11.43%, IC 95%: 6-19.1%) and with Leptospira icterohaemorrhagiae (9.52%, IC 95%: 4.6-16.8%). It is necessary to consider in future studies, the investigation of animal leptospirosis impact in public, animal and environmental health, in order to implement geographically specific prevention and control programs of this disease.

Declaration of interest conflicts

There is no kind of conflict of interest

Acknowledgment

The National Council for Science and Technology (CONACYT) of Mexico by the scholarship granted to OTS to carry out master's studies in agricultural science at the Autonomous University Metropolitan Unity Xochimilco.

REFERENCES

Adler B, De la Peña Moctezuma A. 2010. Leptospira and leptospirosis. Veterinary Microbiology. 140(3-4):287-296. http://doi.org/10.1016/j.vetmic.2009.03.012 [ Links ]

Alves JRA, Oliveira KDS, Costa DF, Fernandez LG, Higino SSS, Alves CJ, Santos CSA, Batista AS. 2016. Epidemiological characterization of leptospirosis in horses in the state of Pernambuco, northeastern Brazil. Arquivos do Instituto Biológico. 86:1-5. http://doi.org/10.1590/1808-214 1657001032014 [ Links ]

Ali H, Saeid S. 2012. Seroprevalence of leptospiral infection in horses, donkeys and mules in east Azerbaijan province. African Journal of Microbiology Research. 6(20):4384-4387. http://doi.org/10.5897/AJMRx11.034 [ Links ]

Andersen, REU, Pipper PMC. 2016. Jensen, Global patterns of leptospira prevalence in vertebrate reservoir hosts. Journal of Wildlife Diseases. 52(3):468-477. http://doi.org/10.7589/2014-10-245 [ Links ]

Arent Z, Kedzierska-Mięszkowska S. 2013. Seroprevalence study of leptospirosis in horses in northern Poland. VetRecord. 172:269. https://doi.org/10.1136/vr.101239 [ Links ]

Arent Z, Frizzell C, Gilmore C, Allen A, Ellis WA. 2016. Leptospira interrogans serovars Bratislava and Muenchen animal infections: Implications for epidemiology and control. Veterinary Microbiology. 190: 19-26. https://doi.org/10.1016/j.vetmic.2016.05.004 [ Links ]

Båverud V, Gunnarsson A, Engvall EO, Franzén P, Egenvall A. 2009. Leptospira seroprevalence and associations between seropositivity, clinical disease and host factors in horses. Acta Veterinaria Scandinavica. 51(1):15. http://doi.org/10.1186/1751-0147-51-15 [ Links ]

Bedoya RMA, Jaimes SJ, Molina SL. 2013. Prevalencia de lepstospira spp. en equinos de la vereda Guatiguara del municipio de Piedecuesta Santander. REDVET. 14(11B): 1-6. https://www.redalyc.org/pdf/636/63632393019.pdfLinks ]

Bernard WV. 1993. Leptospirosis. The Veterinary clinics of North America. Equine practice. 9(2):435-444. https://doi.org/10.1016/s0749-0739(17)30410-8 [ Links ]

Bertelloni F, Cilia G, Turchi B, Pinzauti P, Cerri D, Fratini F. 2019. Epidemiology of leptospirosis in North-Central Italy: Fifteen years of serological data (2002-2016). Comparative Immunology, Microbiology and Infectious Diseases. 65:14-22. https://doi.org/10.1016/j.cimid.2019.04.001 [ Links ]

CDC. 2016. Centers for Disease Control and Prevention EpiInfo7 User Guide. https://www.cdc.gov/epiinfo/pdfs/UserGuide/EI7Full.pdfLinks ]

De Oliveira Filho RB, Malta KC, Oliveira JMB, Assis Santana VL, Harrop MHV, Stipp DT, Pinheiro JW. 2014. Epidemiological Analysis of Leptospira spp. Infection in Equids from the Brejo Paraibano Microregion of Brazil. Journal of Equine Veterinary Science. 34(3):407-414. https://doi.org/10.1016/j.jevs.2013.08.001 [ Links ]

Divers TJ, Chang YF, Irby NL, Smith JL, Carter CN. 2019. Leptospirosis: An important infectious disease in North American horses. Equine Veterinary Journal. 51(3):287-292. https://doi.org/10.1111/evj.13069 [ Links ]

Ellis WA. 2014. Animal Leptospirosis. Leptospira and Leptospirosis. 99-137. https://doi.org/10.1007/978-3-662-45059-8_6 [ Links ]

Ellis WA. 2015. Animal leptospirosis. Curr Top Microbiol Immunol. 387:99-137. https://doi.org/10.1007/978-3-662-45059-8_6 [ Links ]

Hashimoto VY, Gonçalves DD, da Silva FG, de Oliveira RC, Alves LA, Reichmann P, de Freitas JC. 2007. Occurrence of antibodies against Leptospira spp. in horses of the urban area of Londrina, Paraná. Revista do Instituto de Medicina Tropical de São Paulo. 49(5):327-330. https://doi.org/10.1590/S0036-46652007000500010 [ Links ]

Hamond C, Martins G, Lilenbaum W, Madeiros MA. 2012a. PCR detection of leptospiral carriers among seronegative horses. VetRecord. 171:105-6. https://doi.org/10.1136/vr.e5022 [ Links ]

Hamond C, Martins G, Lilenbaum W. 2012b. Subclinical leptospirosis may impair athletic performance in racing horses. Tropical Animal Health and Production. 44(8):1927-1930. https://doi.org/10.1007/s11250-012-0158-5 [ Links ]

Hamond C, Martins G, Medeiros MA, Lilenbaum W. 2013. Presence of leptospiral DNA in semen suggests venereal transmission in Horses. Journal of Equine Veterinary Science. 33(12):1157-1159. https://doi.org/10.1016/j.jevs.2013.03.185 [ Links ]

Hamond C, Martins G, Bremont S, Medeiros MA, Bourhy P, Lilenbaum W. 2014a. Predominance of Leptospira interrogans serovar Bratislava DNA in vaginal fluid of mares suggests sexual transmission of leptospirosis. Animal Reproduction Science. 151(3-4):275-279. https://doi.org/10.1016/j.anireprosci.2014.10.019 [ Links ]

Hamond C, Pinna A, Martins G, Lilenbaum W. 2014b. The role of leptospirosis in reproductive disorders in horses. Tropical animal health and production. 46(1):1-10. https://doi.org/10.1007/s11250-013-0459-3 [ Links ]

Hamond C, Pestana CP, Rocha-de-Souza CM, Cunha LER, Brandão FZ, Medeiros MA, Lilenbaum W. 2015. Presence of leptospires on genital tract of mares with reproductive problems. Veterinary Microbiology. 179(3-4):264-269. https://doi.org/10.1016/j.vetmic.2015.06.014 [ Links ]

Jaeger L, Pestana C, Correia L, Carvalho-Costa F, Medeiros M, Lilenbaum W. 2019. Novel MLST Sequence Types of pathogenic Leptospira spp.: opening the black box of animal leptospirosis in Brazil. Acta Tropica. https://doi.org/10.1016/j.actatropica.2019.05.025 [ Links ]

Khalili M, Sakhaee E, Amiri FB, Safat AA, Afshar D, Esmaeili S. 2019. Serological evidence of leptospirosis in Iran; A systematic review and meta-analysis. Microbial Pathogenesis. https://doi.org/10.1016/j.micpath.2019.103833 [ Links ]

Loureiro A P, Hamond C, Lilenbaum W. 2013. Leptospirosis in horses. Veterinary Record. 172(18):479-480. https://doi.org/10.1136/vr.f2824 [ Links ]

Lowe RC. 2010. Equine uveitis: a UK perspective. Equine veterinary journal. Supplement. (37):46-49. https://doi.org/10.1111/j.2042-3306.2010.tb05634.x [ Links ]

Malalana F. 2019. Leptospirosis in horses: A European perspective. Equine Veterinary Journal. 51(3):285-286. https://doi.org/10.1111/evj.13022 [ Links ]

Martins G, Loureiro AP, Libonati H, Lilenbaum W. 2017. Humoral response in naturally exposed horses after leptospiral vaccination. Journal of Equine Veterinary Science. 57:24-28. https://doi.org/10.1016/j.jevs.2017.06.005 [ Links ]

Méndez C, Benavides A, Esquivel A, Aldama A, Torres J, Gavaldon D, Meléndez P, Moles LP. 2013. Pesquisa serológica de Leptospira en roedores silvestres, bovinos, equinos y caninos en el noreste de México. Revista de Salud Animal. 35(1):25-32. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0253-570X2013000100004Links ]

Molina AM. 2013. El significado de los intervalos de confianza. Rev Pediatr Aten Primaria; 15(57):91-94. https://www.redalyc.org/pdf/3666/366638747016.pdfLinks ]

Moral M, Laplume H, Sardi F, Samartino L, Vanasco B, San Juan J, Casas N. 2014. Enfermedades infecciosas leptospirosis. Ministerio de Salud de la Nación. http://www.msal.gob.ar/images/stories/bes/graficos/0000000489cnt-guia-medica-leptospirosis.pdf consultado el 14/08/2018 [ Links ]

Peixoto Ribeiro TM, Correia L, Hofstaetter Spohr KA, Aguiar DM, Martins G, de Sá Jayme V. 2018. Risk factors associated with seroreactivity against Leptospira spp. in horses from Brazilian Amazon. Journal of Equine Veterinary Science. 68:59-62. . https://doi.org/10.1016/j.jevs.2018.05.197 [ Links ]

Pikalo J, Sattler T, Eichinger M, Loitsch A, Sun H, Schmoll F, Schusser GF. 2016. Vorkommen von antikörpern gegen leptospiren bei pferden im mitteldeutschen raum [Occurrance of antibodies against Leptospira in horses in Middle Germany]. Berliner und Munchener tierarztliche Wochenschrift. 129(5-6):202-208. https://www.vetline.de/system/files/frei/BMW_2016_05_06_0202_onl300.pdfLinks ]

Pulido VA, Carreño BG, Mercado RM, Ramírez BP. 2014. Situación epidemiológica de la leptospirosis humana en centro américa, sur américa y el caribe. Universitas Scientiarum. 19(3):246-264. https://wwww.redalyc.org/articulo.oa?id=499/49931030006Links ]

Pinna A, Martins G, Hamond C, Medeiros MA, de Souza GN, Lilenbaum W. 2014. Potential differences between Leptospira serovars, host-adapted (Bratislava) and incidental (Copenhageni), in determining reproductive disorders in embryo transfer recipient mares in Brazil. The Veterinary Record. 174(21):531. https://doi.org/10.1136/vr.101444 [ Links ]

Rey Riaño LA, Pineda RNF, Góngora OA, Parra AJL, Patiño BRE. 2015. Nota serológica a Leptospira spp. En equinos aparentemente sanos en municipios del Meta y Guaviare, Colombia. Revista Lasallista de Investigación. 12(1):154-161. https://www.redalyc.org/articulo.oa?id=695/69542290015Links ]

Rocha T. 2004. Microbiological and serological study of leptospirosis in horses at slaughter: first isolations Research in Veterinary Science. 76(3):199- 202. https://doi.org/10.1016/j.rvsc.2003.12.003 [ Links ]

Simbizi V, Saulez MN, Potts A, Lötter C, Gummow B. 2016. A study of leptospirosis in South African horses and associated risk factors. Preventive Veterinary Medicine. 134: 6-15. https://doi.org/10.1016/j.prevetmed.2016.09.019 [ Links ]

Siqueira CC, Fraga DBM, Chagas-Junior AD, Athanazio DA, Silva MMN, Cerqueira RB, Ayres MCC. 2019. Seroprevalence and risk factors associated with equine leptospirosis in the metropolitan region of Salvador and Recôncavo Baiano region, Bahia state (NE Brazil). Tropical Animal Health and Production. 52:31-39. https://doi.org/10.1007/s11250- 019-01956-5 [ Links ]

Torres CM, Hernández BS, Agudelo FP, Arroyave SE, Zaval CJ. Puerto FI. 2016. Revisión actual de la epidemiologia de la leptospirosis. Revista Médica del Instituto Mexicano del Seguro Social. 54(5):620-5. https://www.medigraphic.com/pdfs/imss/im- 2016/im165k.pdfLinks ]

Troncoso TI, Toro BJ, Guzmán CA, Fuentealba OJ, Fischer WC. 2013. Evaluación serológica de Leptospira interrogans en equinos pertenecientes a un centro ecuestre de la provincia de Linares, Chile. Revista CES Medicina Veterinaria y Zootecnia. 8(2):101-107. http://www.scielo.org.co/pdf/cmvz/v8n2/v8n2a10.pdfLinks ]

Tsegay K, Potts AD, Aklilu N, Lddototter C, Gummow B. 2016. Circulating serovars of Leptospira in cart horses of central and southern Ethiopia and associated risk factors. Preventive Veterinary Medicine. 125(1): 106-115. http://dx.doi.org/10.1016/j.prevetmed.2016.01.009 [ Links ]

Vera E, Taddei S, Cavirani S, Schiavi J, Angelone M, Cabassi CS, Schiano E, Quintavalla F. 2019. Leptospira Seroprevalence in bardigiano horses in northern Italy. Animals: an open access journal from MDPI. 10(1):23. https://doi.org/10.3390/ani10010023 [ Links ]

Verma A, Kumar P, Babb K, Timoney J F, Stevenson B. 2010. Cross-Reactivity of Antibodies against Leptospiral Recurrent Uveitis-Associated Proteins A and B (LruA and LruB) with Eye Proteins. PLOS Neglected Tropical Diseases. 4(8):778. https://doi.org/10.1371/journal.pntd.0000778 [ Links ]

Verma A, Beigel B, Smola CC, Kitts-Morgan S, Kish D, Nader P, Goss R. 2019. Evidence of Leptospiral Presence in the Cumberland Gap Region. PLOS Neglected Tropical Diseases. 13(12): e0007990. https://doi.org/10.1371/journal.pntd.0007990 [ Links ]

Witkowski L, Cywinska A, Paschalis-Trela K, Crisman M, Kita J. 2016. Multiple etiologies of equine recurrent uveitis - A natural model for human autoimmune uveitis: A brief review. Comparative Immunology, Microbiology and Infectious Diseases. 44:14- 20. https://doi.org/10.1016/j.cimid.2015.11.004 [ Links ]

Wood PL, Steinman M, Erol E, Carter C, Christmann U, Verma A. 2018. Lipidomic analysis of immune activation in equine leptospirosis and Leptospira-vaccinated horses. PLOS ONE. 13(2). https://doi.org/10.1371/journal.pone.0193424 [ Links ]

Zarantonelli L, Suanes A, Meny P, Buroni F, Nieves C, Salaberry X, Briano C, Ashfield N, Silveira S, Dutra F, Easton C, Fraga M, Giannitti F, Hamond C, Macias- Rioseco M, Menendez C, Mortola A, Picardeau M, Quintero J, Rios C, Rodríguez V, Romero A, Varela G, Rivero R, Schelotto F, Riet-Correa F, Buschiazzo A. 2018. Isolation of pathogenic Leptospira strains from naturally infected cattle in Uruguay reveals high serovar diversity, and uncovers a relevant risk for human https://doi.org/10.1371/journal.pntd.0006694. [ Links ]

Code: e2020-91.

Received: November 19, 2020; Accepted: April 27, 2021

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