The lagomorph-infecting Treponema paraluisleporidarum is a close relative of the human syphilis-bacterium Treponema pallidum. There is a paucity of information on the epidemiology of hare syphilis and its relationship to the rabbit- and human-infecting treponemes that cause syphilis. In our study, we tested 734 serum samples from European brown hares (Lepus europaeus) collected between 2007 and 2019 in the federal state of Lower Saxony, Germany, for the presence of antibodies against T. paraluisleporidarum. Since T. paraluisleporidarum cross-reacts with T. pallidum antigen, we used a commercially available T. pallidum-particle agglutination (TP-PA) assay to test for the presence of antibodies. A high seropositivity (n = 405/734) was detected. An additional 233 serum samples were retested using a fluorescent treponemal antibody absorption test to confirm the results of the TP-PA assay. Our results show that infection is widespread in Lower Saxony and suggest a horizontal (sexual) transmission mode since adult hares show significantly higher seropositivity than subadults (odds ratio: 0.03 [95% CI 0.02-0.05], p < .0001). No difference was detected based on gender (odds ratio: 0.79 [95% Cl 0.58-1.07], p = .1283). Further studies are warranted to genetically characterize the T. paraluisleporidarum strains that infect wild hares.

Georg August University Goettingen Germany

German Primate Center Goettingen Germany

Masaryk University Brno Czech Republic

University of Veterinary Medicine Hannover Foundation Hannover Germany

Zobrazit více v PubMed

Baker-Zander, S. A., & Lukehart, S. A. (1984). Antigenic cross-reactivity between Treponema pallidum and other pathogenic members of the family Spirochaetaceae. Infection and Immunity, 46, 116-121. https://doi.org/10.1128/iai.46.1.116-121.1984

Broekhuizen, S., & Masskamp, F. (1979). Age determination in the European hare (Lepus europaeus Pallas) in the Netherlands. Zeitschrift für Säugetierkunde, 44, 162-175.

Cameron, A. R., & Baldock, F. C. (1998). Two-stage sampling in surveys to substantiate freedom from disease. Preventive Veterinary Medicine, 34, 19-30. https://doi.org/10.1016/s0167-5877(97)00073-1

Chambers, L. C., Srinivasan, S., Lukehart, S. A., Ocbamichael, N., Morgan, J. L., Lowens, M. S., … Manhart, L. E. (2019). Primary syphilis in the male urethra: A case report. Clinical Infectious Diseases, 68(7), 1231-1234. https://doi.org/10.1093/cid/ciy771

Cunliffe-Beamer, T. L., & Fox, R. R. (1981). Venereal spirochetosis of rabbits: Epizootiology. Laboratory Animal Science, 31(4), 372-378.

DiGiacomo, R. F., Lukehart, S. A., Talburt, C. D., Baker-Zander, S. A., Giddens, W. E. Jr, Condon, J., & Brown, C. W. (1985). Chronicity of infection with Treponema paraluis-cuniculi in New Zealand white rabbits. Genitourinary Medicine, 61(3), 156-164. https://doi.org/10.1136/sti.61.3.156

Froberg, M. K., Fitzgerald, T. J., Hamilton, T. R., Hamilton, B., & Zarabi, M. (1993). Pathology of congenital syphilis in rabbits. Infection and Immunity, 61, 4743-4749. https://doi.org/10.1128/IAI.61.11.4743-4749.1993

Horvath, I., Kemenes, F., & Molnar, L. (1979). Isolation of pathogenic treponemes from hare. Experientia, 35, 320-321. https://doi.org/10.1007/bf01964325

Jakšić, B. (1957). Bruceloza i sifilis zečeva (Brucellose et syphilis du lievre). Veterinarski Glasnik, 4, 423-428.

Knauf, S., Dahlmann, F., Batamuzi, E. K., Frischmann, S., & Liu, H. (2015). Validation of serological tests for the detection of antibodies against Treponema pallidum in nonhuman primates. PLoS Neglected Tropical Diseases, 9, e0003637. https://doi.org/10.1371/journal.pntd.0003637

Lumeij, J. T. (2011). Widespread treponemal infections of hare populations (Lepus europaeus) in the Netherlands. European Journal of Wildlife Research, 57, 183-186. https://doi.org/10.1007/s10344-010-0428-3

Lumeij, J. T., de Koning, J., Bosma, R. B., van der Sluis, J. J., & Schellekens, J. F. (1994). Treponemal infections in hares in the Netherlands. Journal of Clinical Microbiology, 32, 543-546. https://doi.org/10.1128/JCM.32.2.543-546.1994

Lumeij, J. T., Mikalová, L., & Šmajs, D. (2013). Is there a difference between hare syphilis and rabbit syphilis? Cross infection experiments between rabbits and hares. Veterinary Microbiology, 164, 190-194. https://doi.org/10.1016/j.vetmic.2013.02.001

Mörner, T. (1999). Monitoring diseases in wildlife - a review of diseases in the orders lagomorpha and rodentia in Sweden. Verh ber Erkrg Zootiere, 39, 255-262.

Nováková, M., Najt, D., Mikalová, L., Kostková, M., Vrbová, E., Strouhal, M., … Šmajs, D. (2019). First report of hare treponematosis seroprevalence of European brown hares (Lepus europaeus) in the Czech Republic: Seroprevalence negatively correlates with altitude of sampling areas. BMC Veterinary Research, 15, 350. https://doi.org/10.1186/s12917-019-2086-3

Posautz, A., Leidinger, E., Knauer, F., Hoffmann, D., Suchentrunk, F., Walzer, C., & Kübber-Heiss, A. (2014). Seroprevalence of Treponema sp. in European brown hares (Lepus europaeus) in Austria and Germany. Wiener Tierärztliche Monatsschrift, 101, 281-285.

Šmajs, D., Zobaníková, M., Strouhal, M., Čejková, D., Dugan-Rocha, S., Pospíšilová, P., … Weinstock, G. M. (2011). Complete genome sequence of Treponema paraluiscuniculi, strain Cuniculi A: The loss of infectivity to humans is associated with genome decay. PLoS ONE, 6, e20415. https://doi.org/10.1371/journal.pone.0020415

Small, J. D., & Newman, B. (1972). Venereal spirochetosis of rabbits (rabbit syphilis) due to Treponema cuniculi: A clinical, serological, and histopathological study. Laboratory Animal Science, 22, 77-89.

Strauss, E., Ronnenberg, K., Klages, I., & Graeber, R. (2016). Wildlife survey in Lower Saxony 1991-2016 - A base tool for description of biodiversity of our cultural landscape. Verhandlungen der Gesellschaft für Ökologie, 46, 363-364.

Strouhal, M., Smajs, D., Matejkova, P., Sodergren, E., Amin, A. G., Howell, J. K., … Weinstock, G. M. (2007). Genome differences between Treponema pallidum subsp. pallidum strain Nichols and T. paraluiscuniculi strain Cuniculi A. Infection and Immunity, 75, 5859-5866. https://doi.org/10.1128/IAI.00709-07

Suchentrunk, F., Willing, R., & Hartl, G. B. (1991). On eye lens weights and other age criteria of the Brown hare (Lepus europaeus Pallas, 1778). Zeitschrift für Säugetierkunde, 56, 365-374.

Verin, R., Pestelli, M., & Poli, A. (2012). Treponemal infection in free-ranging European brown hares (Lepus europaeus) in central Italy: Serology and epidemiology. Journal of Wildlife Diseases, 48, 1079-1082. https://doi.org/10.7589/2011-03-069

The hare syphilis agent is related to, but distinct from, the treponeme causing rabbit syphilis

High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs

Penicillin Treatment Failure in Rabbit Syphilis Due to the Persistence of Treponemes (Treponema paraluisleporidarum Ecovar Cuniculus) in the Focus of Infection

Zobrazit více v PubMed

RefSeq
NC_015714.1