Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae
Abstract Background Ixodes ricinus constitutes the main European vector tick for the Lyme borreliosis pathogen Borrelia burgdorferi (sensu lato), the relapsing fever borrelia Borrelia miyamotoi, as well as Anaplasma phagocytophilum and several Rickettsia species. Under laboratory conditions, a trans...
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| Format: | Article |
| Language: | English |
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BMC
2020-04-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13071-020-04049-7 |
| _version_ | 1819070474196353024 |
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| author | Daniela Hauck Daniela Jordan Andrea Springer Bettina Schunack Stefan Pachnicke Volker Fingerle Christina Strube |
| author_facet | Daniela Hauck Daniela Jordan Andrea Springer Bettina Schunack Stefan Pachnicke Volker Fingerle Christina Strube |
| author_sort | Daniela Hauck |
| collection | DOAJ |
| description | Abstract Background Ixodes ricinus constitutes the main European vector tick for the Lyme borreliosis pathogen Borrelia burgdorferi (sensu lato), the relapsing fever borrelia Borrelia miyamotoi, as well as Anaplasma phagocytophilum and several Rickettsia species. Under laboratory conditions, a transovarial transmission to the next tick generation is described for Rickettsia spp. and Borrelia spp., especially regarding B. miyamotoi, whereas the efficiency of transovarial transfer under field conditions is largely unstudied. Methods In order to better estimate the potential infection risk by tick larvae for humans and animals, 1500 I. ricinus larvae from 50 collected “nests” (larvae adhering to the flag in a clumped manner) were individually examined for Borrelia, Rickettsia and A. phagocytophilum DNA using quantitative real-time PCR (qPCR). Results Thirty-nine of 50 nests each (78.0%, 95% CI: 64.0–88.5%) were positive for Borrelia spp. and Rickettsia spp. DNA, and in three nests (6.0%, 95% CI: 1.3–16.5%) A. phagocytophilum DNA was detected. Overall, DNA from at least one pathogen could be detected in 90.0% (45/50, 95% CI: 78.2–96.7%) of the nests. Of the 1500 larvae, 137 were positive for Borrelia spp. DNA (9.1%, 95% CI: 7.7–10.7%), 341 for Rickettsia spp. DNA (22.7%, 95% CI: 20.6–24.9%) and three for A. phagocytophilum DNA (0.2%, 95% CI: 0–0.6%). Quantity of Borrelia spp. and Anaplasma spp. DNA in positive larvae was low, with 2.7 × 100 Borrelia 5S-23S gene copies and 2.4 × 101 A. phagocytophilum msp2/p44 gene copies detected on average, while Rickettsia-positive samples contained on average 5.4 × 102 gltA gene copies. Coinfections were found in 66.0% (33/50, 95% CI: 51.2–78.8%) of the nests and 8.6% (38/443, 95% CI: 6.1–11.6%) of positive larvae. In fact, larvae had a significantly higher probability of being infected with Borrelia spp. or Rickettsia spp. when both pathogens were present in the nest. Conclusions This study provides evidence for transovarial transmission of Rickettsia spp. and Borrelia spp. in I. ricinus under field conditions, possibly facilitating pathogen persistence in the ecosystem and reducing the dependence on the presence of suitable reservoir hosts. Further studies are needed to prove transovarial transmission and to explain the surprisingly high proportion of nests containing Rickettsia and/or Borrelia DNA-positive larvae compared to infection rates in adult ticks commonly reported in other studies. |
| first_indexed | 2024-12-21T17:06:30Z |
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| id | doaj.art-751b2e770c674157b59bf17e6e5f7767 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-12-21T17:06:30Z |
| publishDate | 2020-04-01 |
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| series | Parasites & Vectors |
| spelling | doaj.art-751b2e770c674157b59bf17e6e5f77672022-12-21T18:56:30ZengBMCParasites & Vectors1756-33052020-04-0113111110.1186/s13071-020-04049-7Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvaeDaniela Hauck0Daniela Jordan1Andrea Springer2Bettina Schunack3Stefan Pachnicke4Volker Fingerle5Christina Strube6Institute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine HannoverInstitute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine HannoverInstitute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine HannoverBayer Animal Health GmbHBayer Vital GmbHNational Reference Centre for BorreliaInstitute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine HannoverAbstract Background Ixodes ricinus constitutes the main European vector tick for the Lyme borreliosis pathogen Borrelia burgdorferi (sensu lato), the relapsing fever borrelia Borrelia miyamotoi, as well as Anaplasma phagocytophilum and several Rickettsia species. Under laboratory conditions, a transovarial transmission to the next tick generation is described for Rickettsia spp. and Borrelia spp., especially regarding B. miyamotoi, whereas the efficiency of transovarial transfer under field conditions is largely unstudied. Methods In order to better estimate the potential infection risk by tick larvae for humans and animals, 1500 I. ricinus larvae from 50 collected “nests” (larvae adhering to the flag in a clumped manner) were individually examined for Borrelia, Rickettsia and A. phagocytophilum DNA using quantitative real-time PCR (qPCR). Results Thirty-nine of 50 nests each (78.0%, 95% CI: 64.0–88.5%) were positive for Borrelia spp. and Rickettsia spp. DNA, and in three nests (6.0%, 95% CI: 1.3–16.5%) A. phagocytophilum DNA was detected. Overall, DNA from at least one pathogen could be detected in 90.0% (45/50, 95% CI: 78.2–96.7%) of the nests. Of the 1500 larvae, 137 were positive for Borrelia spp. DNA (9.1%, 95% CI: 7.7–10.7%), 341 for Rickettsia spp. DNA (22.7%, 95% CI: 20.6–24.9%) and three for A. phagocytophilum DNA (0.2%, 95% CI: 0–0.6%). Quantity of Borrelia spp. and Anaplasma spp. DNA in positive larvae was low, with 2.7 × 100 Borrelia 5S-23S gene copies and 2.4 × 101 A. phagocytophilum msp2/p44 gene copies detected on average, while Rickettsia-positive samples contained on average 5.4 × 102 gltA gene copies. Coinfections were found in 66.0% (33/50, 95% CI: 51.2–78.8%) of the nests and 8.6% (38/443, 95% CI: 6.1–11.6%) of positive larvae. In fact, larvae had a significantly higher probability of being infected with Borrelia spp. or Rickettsia spp. when both pathogens were present in the nest. Conclusions This study provides evidence for transovarial transmission of Rickettsia spp. and Borrelia spp. in I. ricinus under field conditions, possibly facilitating pathogen persistence in the ecosystem and reducing the dependence on the presence of suitable reservoir hosts. Further studies are needed to prove transovarial transmission and to explain the surprisingly high proportion of nests containing Rickettsia and/or Borrelia DNA-positive larvae compared to infection rates in adult ticks commonly reported in other studies.http://link.springer.com/article/10.1186/s13071-020-04049-7Borrelia burgdorferi (sensu lato)Borrelia miyamotoiRickettsialesAnaplasma phagocytophilumTicksTick-borne diseases |
| spellingShingle | Daniela Hauck Daniela Jordan Andrea Springer Bettina Schunack Stefan Pachnicke Volker Fingerle Christina Strube Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae Parasites & Vectors Borrelia burgdorferi (sensu lato) Borrelia miyamotoi Rickettsiales Anaplasma phagocytophilum Ticks Tick-borne diseases |
| title | Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae |
| title_full | Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae |
| title_fullStr | Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae |
| title_full_unstemmed | Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae |
| title_short | Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae |
| title_sort | transovarial transmission of borrelia spp rickettsia spp and anaplasma phagocytophilum in ixodes ricinus under field conditions extrapolated from dna detection in questing larvae |
| topic | Borrelia burgdorferi (sensu lato) Borrelia miyamotoi Rickettsiales Anaplasma phagocytophilum Ticks Tick-borne diseases |
| url | http://link.springer.com/article/10.1186/s13071-020-04049-7 |
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