Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary
Abstract Background Borrelia miyamotoi, the newly discovered human pathogenic relapsing fever spirochete, and Borrelia burgdorferi sensu lato are maintained in natural rodent populations. The aim of this study was to investigate the natural cycle of B. miyamotoi and B. burgdorferi s.l. in a forest h...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2015-06-01
|
| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13071-015-0922-2 |
| _version_ | 1797811855747448832 |
|---|---|
| author | Sándor Szekeres Elena Claudia Coipan Krisztina Rigó Gábor Majoros Setareh Jahfari Hein Sprong Gábor Földvári |
| author_facet | Sándor Szekeres Elena Claudia Coipan Krisztina Rigó Gábor Majoros Setareh Jahfari Hein Sprong Gábor Földvári |
| author_sort | Sándor Szekeres |
| collection | DOAJ |
| description | Abstract Background Borrelia miyamotoi, the newly discovered human pathogenic relapsing fever spirochete, and Borrelia burgdorferi sensu lato are maintained in natural rodent populations. The aim of this study was to investigate the natural cycle of B. miyamotoi and B. burgdorferi s.l. in a forest habitat with intensive hunting, forestry work and recreational activity in Southern Hungary. Methods We collected rodents with modified Sherman-traps during 2010–2013 and questing ticks with flagging in 2012. Small mammals were euthanized, tissue samples were collected and all ectoparasites were removed and stored. Samples were screened for pathogens with multiplex quantitative real-time polymerase chain reaction (qPCR) targeting a part of flagellin gene, then analysed with conventional PCRs and sequencing. Results 177 spleen and 348 skin samples of six rodent species were individually analysed. Prevalence in rodent tissue samples was 0.2 % (skin) and 0.5 % (spleen) for B. miyamotoi and 6.6 % (skin) and 2.2 % (spleen) for B. burgdorferi s.l. Relapsing fever spirochetes were detected in Apodemus flavicollis males, B. burgdorferi s.l. in Apodemus spp. and Myodes glareolus samples. Borrelia miyamotoi was detected in one questing Ixodes ricinus nymph and B. burgdorferi s.l in nymphs and adults. In the ticks removed from rodents DNA amplification of both pathogens was successful from I. ricinus larvae (B. miyamotoi 5.6 %, B. burgdorferi s.l. 11.1 %) and one out of five nymphs while from Ixodes acuminatus larvae, and nymph only B. burgdorferi s.l. DNA was amplified. Sequencing revealed B. lusitaniae in a questing I. ricinus nymph and altogether 17 B. afzelii were identified in other samples. Two Dermacentor marginatus engorged larva pools originating from uninfected hosts were also infected with B. afzelii. Conclusions This is the first report of B. miyamotoi occurrence in a natural population of A. flavicollis as well as in Hungary. We provide new data about circulation of B. burgdorferi s.l. in rodent and tick communities including the role of I. acuminatus ticks in the endophilic pathogen cycle. Our results highlight the possible risk of infection with relapsing fever and Lyme borreliosis spirochetes in forest habitats especially in the high-risk groups of hunters, forestry workers and hikers. |
| first_indexed | 2024-03-13T07:28:55Z |
| format | Article |
| id | doaj.art-e72f156ccf14408f81032a7c13cac44d |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-03-13T07:28:55Z |
| publishDate | 2015-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-e72f156ccf14408f81032a7c13cac44d2023-06-04T11:13:05ZengBMCParasites & Vectors1756-33052015-06-01811810.1186/s13071-015-0922-2Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in HungarySándor Szekeres0Elena Claudia Coipan1Krisztina Rigó2Gábor Majoros3Setareh Jahfari4Hein Sprong5Gábor Földvári6Department of Parasitology and Zoology, Faculty of Veterinary Science, Szent István UniversityLaboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and EnvironmentDepartment of Parasitology and Zoology, Faculty of Veterinary Science, Szent István UniversityDepartment of Parasitology and Zoology, Faculty of Veterinary Science, Szent István UniversityLaboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and EnvironmentLaboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and EnvironmentDepartment of Parasitology and Zoology, Faculty of Veterinary Science, Szent István UniversityAbstract Background Borrelia miyamotoi, the newly discovered human pathogenic relapsing fever spirochete, and Borrelia burgdorferi sensu lato are maintained in natural rodent populations. The aim of this study was to investigate the natural cycle of B. miyamotoi and B. burgdorferi s.l. in a forest habitat with intensive hunting, forestry work and recreational activity in Southern Hungary. Methods We collected rodents with modified Sherman-traps during 2010–2013 and questing ticks with flagging in 2012. Small mammals were euthanized, tissue samples were collected and all ectoparasites were removed and stored. Samples were screened for pathogens with multiplex quantitative real-time polymerase chain reaction (qPCR) targeting a part of flagellin gene, then analysed with conventional PCRs and sequencing. Results 177 spleen and 348 skin samples of six rodent species were individually analysed. Prevalence in rodent tissue samples was 0.2 % (skin) and 0.5 % (spleen) for B. miyamotoi and 6.6 % (skin) and 2.2 % (spleen) for B. burgdorferi s.l. Relapsing fever spirochetes were detected in Apodemus flavicollis males, B. burgdorferi s.l. in Apodemus spp. and Myodes glareolus samples. Borrelia miyamotoi was detected in one questing Ixodes ricinus nymph and B. burgdorferi s.l in nymphs and adults. In the ticks removed from rodents DNA amplification of both pathogens was successful from I. ricinus larvae (B. miyamotoi 5.6 %, B. burgdorferi s.l. 11.1 %) and one out of five nymphs while from Ixodes acuminatus larvae, and nymph only B. burgdorferi s.l. DNA was amplified. Sequencing revealed B. lusitaniae in a questing I. ricinus nymph and altogether 17 B. afzelii were identified in other samples. Two Dermacentor marginatus engorged larva pools originating from uninfected hosts were also infected with B. afzelii. Conclusions This is the first report of B. miyamotoi occurrence in a natural population of A. flavicollis as well as in Hungary. We provide new data about circulation of B. burgdorferi s.l. in rodent and tick communities including the role of I. acuminatus ticks in the endophilic pathogen cycle. Our results highlight the possible risk of infection with relapsing fever and Lyme borreliosis spirochetes in forest habitats especially in the high-risk groups of hunters, forestry workers and hikers.https://doi.org/10.1186/s13071-015-0922-2Borrelia miyamotoiBorrelia burgdorferi sensu latoTicksIxodes acuminatusRodentsApodemus flavicollis |
| spellingShingle | Sándor Szekeres Elena Claudia Coipan Krisztina Rigó Gábor Majoros Setareh Jahfari Hein Sprong Gábor Földvári Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary Parasites & Vectors Borrelia miyamotoi Borrelia burgdorferi sensu lato Ticks Ixodes acuminatus Rodents Apodemus flavicollis |
| title | Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary |
| title_full | Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary |
| title_fullStr | Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary |
| title_full_unstemmed | Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary |
| title_short | Eco-epidemiology of Borrelia miyamotoi and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary |
| title_sort | eco epidemiology of borrelia miyamotoi and lyme borreliosis spirochetes in a popular hunting and recreational forest area in hungary |
| topic | Borrelia miyamotoi Borrelia burgdorferi sensu lato Ticks Ixodes acuminatus Rodents Apodemus flavicollis |
| url | https://doi.org/10.1186/s13071-015-0922-2 |
| work_keys_str_mv | AT sandorszekeres ecoepidemiologyofborreliamiyamotoiandlymeborreliosisspirochetesinapopularhuntingandrecreationalforestareainhungary AT elenaclaudiacoipan ecoepidemiologyofborreliamiyamotoiandlymeborreliosisspirochetesinapopularhuntingandrecreationalforestareainhungary AT krisztinarigo ecoepidemiologyofborreliamiyamotoiandlymeborreliosisspirochetesinapopularhuntingandrecreationalforestareainhungary AT gabormajoros ecoepidemiologyofborreliamiyamotoiandlymeborreliosisspirochetesinapopularhuntingandrecreationalforestareainhungary AT setarehjahfari ecoepidemiologyofborreliamiyamotoiandlymeborreliosisspirochetesinapopularhuntingandrecreationalforestareainhungary AT heinsprong ecoepidemiologyofborreliamiyamotoiandlymeborreliosisspirochetesinapopularhuntingandrecreationalforestareainhungary AT gaborfoldvari ecoepidemiologyofborreliamiyamotoiandlymeborreliosisspirochetesinapopularhuntingandrecreationalforestareainhungary |