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Ticks infected via co-feeding transmission can transmit Lyme borreliosis to vertebrate hosts

. 2017 Jul 10 ; 7 (1) : 5006. [epub] 20170710

Language English Country England, Great Britain Media electronic

Document type Comparative Study, Journal Article, Research Support, Non-U.S. Gov't

Links

PubMed 28694446
PubMed Central PMC5503982
DOI 10.1038/s41598-017-05231-1
PII: 10.1038/s41598-017-05231-1
Knihovny.cz E-resources

Vector-borne pathogens establish systemic infections in host tissues to maximize transmission to arthropod vectors. Co-feeding transmission occurs when the pathogen is transferred between infected and naive vectors that feed in close spatiotemporal proximity on a host that has not yet developed a systemic infection. Borrelia afzelii is a tick-borne spirochete bacterium that causes Lyme borreliosis (LB) and is capable of co-feeding transmission. Whether ticks that acquire LB pathogens via co-feeding are actually infectious to vertebrate hosts has never been tested. We created nymphs that had been experimentally infected as larvae with B. afzelii via co-feeding or systemic transmission, and compared their performance over one complete LB life cycle. Co-feeding nymphs had a spirochete load that was 26 times lower than systemic nymphs but both nymphs were highly infectious to mice (i.e., probability of nymph-to-host transmission of B. afzelii was ~100%). The mode of transmission had no effect on the other infection phenotypes of the LB life cycle. Ticks that acquire B. afzelii via co-feeding transmission are highly infectious to rodents, and the resulting rodent infection is highly infectious to larval ticks. This is the first study to show that B. afzelii can use co-feeding transmission to complete its life cycle.

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Voordouw MJ. Co-feeding transmission in Lyme disease pathogens. Parasitology. 2015;142:290–302. doi: 10.1017/S0031182014001486. PubMed DOI PMC

Randolph SE, Gern L, Nuttall PA. Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitol. Today. 1996;12:472–479. doi: 10.1016/S0169-4758(96)10072-7. PubMed DOI

Randolph SE. Transmission of tick-borne pathogens between co-feeding ticks: Milan Labuda’s enduring paradigm. Ticks Tick Borne Dis. 2011;2:179–182. doi: 10.1016/j.ttbdis.2011.07.004. PubMed DOI

Jones LD, Davies CR, Steele GM, Nuttall PA. A novel mode of arbovirus transmission involving a nonviremic host. Science. 1987;237:775–777. doi: 10.1126/science.3616608. PubMed DOI

Mead DG, Ramberg FB, Besselsen DG, Mare CJ. Transmission of vesicular stomatitis virus from infected to noninfected black flies co-feeding on nonviremic deer mice. Science. 2000;287:485–487. doi: 10.1126/science.287.5452.485. PubMed DOI

Higgs S, Schneider BS, Vanlandingham DL, Klingler KA, Gould EA. Nonviremic transmission of West Nile virus. Proc. Natl. Acad. Sci. USA. 2005;102:8871–8874. doi: 10.1073/pnas.0503835102. PubMed DOI PMC

Karpathy SE, Allerdice MEJ, Sheth M, Dasch GA, Levin ML. Co-Feeding transmission of the Ehrlichia muris-like agent to mice (Mus musculus) Vector-Borne Zoonot. 2016;16:145–150. doi: 10.1089/vbz.2015.1878. PubMed DOI PMC

Levin ML, Fish D. Immunity reduces reservoir host competence of Peromyscus leucopus for Ehrlichia phagocytophila. Infect. Immun. 2000;68:1514–1518. doi: 10.1128/IAI.68.3.1514-1518.2000. PubMed DOI PMC

Kurtenbach K, et al. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat. Rev. Microbiol. 2006;4:660–669. doi: 10.1038/nrmicro1475. PubMed DOI

Tsao, J. Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles. Vet. Res. (Paris) 40 (2009). PubMed PMC

Radolf JD, Caimano MJ, Stevenson B, Hu LT. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat. Rev. Microbiol. 2012;10:87–99. PubMed PMC

Stanek G, Reiter M. The expanding Lyme Borrelia complex-clinical significance of genomic species? Clin. Microbiol. Infec. 2011;17:487–493. doi: 10.1111/j.1469-0691.2011.03492.x. PubMed DOI

Stanek G, Wormser GP, Gray J, Strle F. Lyme borreliosis. Lancet. 2012;379:461–473. doi: 10.1016/S0140-6736(11)60103-7. PubMed DOI

Gern L, Rais O. Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae) J. Med. Entomol. 1996;33:189–192. doi: 10.1093/jmedent/33.1.189. PubMed DOI

Patrican LA. Acquisition of Lyme disease spirochetes by cofeeding Ixodes scapularis ticks. The American journal of tropical medicine and hygiene. 1997;57:589–593. doi: 10.4269/ajtmh.1997.57.589. PubMed DOI

Piesman J, Happ CM. The efficacy of co-feeding as a means of maintaining Borrelia burgdorferi: a North American model system. J. Vector Ecol. 2001;26:216–220. PubMed

Sato Y, Nakao M. Transmission of the Lyme disease spirochete, Borrelia garinii, between infected and uninfected immature Ixodes persulcatus during cofeeding on mice. J. Parasitol. 1997;83:547–550. doi: 10.2307/3284432. PubMed DOI

Richter D, Allgower R, Matuschka FR. Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii. Emerg. Infect. Dis. 2003;9:895–896. doi: 10.3201/eid0907.030342. PubMed DOI PMC

Tonetti N, Voordouw MJ, Durand J, Monnier S, Gern L. Genetic variation in transmission success of the Lyme borreliosis pathogen Borrelia afzelii. Ticks Tick Borne Dis. 2015;6:334–343. doi: 10.1016/j.ttbdis.2015.02.007. PubMed DOI

Jacquet M, Durand J, Rais O, Voordouw MJ. Cross-reactive acquired immunity influences transmission success of the Lyme disease pathogen. Borrelia afzelii. Infect. Genet. Evol. 2015;36:131–140. doi: 10.1016/j.meegid.2015.09.012. PubMed DOI

Heylen D, Matthysen E, Fonville M, Sprong H. Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes rinicus ticks. Environ. Microbiol. 2014;16:2859–2868. doi: 10.1111/1462-2920.12304. PubMed DOI

States, S. L., Huang, C. I., Davis, S., Tufts, D. M. & Diuk-Wasser, M. A. Co-feeding transmission facilitates strain coexistence in Borrelia burgdorferi, the Lyme disease agent. Epidemics (2016). PubMed PMC

Hu CM, et al. Early detection of Borrelia burgdorferi sensu lato infection in Balb/c mice by co-feeding Ixodes ricinus ticks. Int. J. Med. Microbiol. 2003;293:421–426. doi: 10.1078/1438-4221-00285. PubMed DOI

Randolph SE, Gern L. Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii. Emerg. Infect. Dis. 2003;9:893–894. doi: 10.3201/eid0907.030116. PubMed DOI PMC

Harrison A, Bennett N. The importance of the aggregation of ticks on small mammal hosts for the establishment and persistence of tick-borne pathogens: an investigation using the R-0 model. Parasitology. 2012;139:1605–1613. doi: 10.1017/S0031182012000893. PubMed DOI

Harrison A, Montgomery WI, Bown KJ. Investigating the persistence of tick-borne pathogens via the R-0 model. Parasitology. 2011;138:896–905. doi: 10.1017/S0031182011000400. PubMed DOI

Hartemink NA, Randolph SE, Davis SA, Heesterbeek JAP. The basic reproduction number for complex disease systems: Defining R-0 for tick-borne infections. Am. Nat. 2008;171:743–754. doi: 10.1086/587530. PubMed DOI

Pérez D, Kneubühler Y, Rais O, Jouda F, Gern L. Borrelia afzelii ospC genotype diversity in Ixodes ricinus questing ticks and ticks from rodents in two Lyme borreliosis endemic areas: Contribution of co-feeding ticks. Ticks Tick Borne Dis. 2011;2:137–142. doi: 10.1016/j.ttbdis.2011.06.003. PubMed DOI

Jacquet M, Durand J, Rais O, Voordouw MJ. Strain-specific antibodies reduce co-feeding transmission of the Lyme disease pathogen. Borrelia afzelii. Environ. Microbiol. 2016;18:833–845. doi: 10.1111/1462-2920.13065. PubMed DOI

Jacquet M, Margos G, Fingerle V, Voordouw MJ. Comparison of the lifetime host-to-tick transmission between two strains of the Lyme disease pathogen Borrelia afzelii. Parasit. Vectors. 2016;9:645. doi: 10.1186/s13071-016-1929-z. PubMed DOI PMC

Rego ROM, Bestor A, Stefka J, Rosa PA. Population bottlenecks during the infectious cycle of the Lyme disease spirochete Borrelia burgdorferi. PLOS ONE. 2014;9:e101009. doi: 10.1371/journal.pone.0101009. PubMed DOI PMC

Durand, J. et al. Multistrain infections with Lyme borreliosis pathogens in the tick vector. Appl. Environ. Microbiol. 83 (2017). PubMed PMC

Tschirren B, et al. Polymorphisms at the innate immune receptor TLR2 are associated with Borrelia infection in a wild rodent population. P. Roy. Soc. B-Biol. Sci. 2013;280:20130364. doi: 10.1098/rspb.2013.0364. PubMed DOI PMC

Randolph SE, Miklisova D, Lysy J, Rogers DJ, Labuda M. Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology. 1999;118:177–186. doi: 10.1017/S0031182098003643. PubMed DOI

Humair PF, Rais O, Gern L. Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology. 1999;118:33–42. doi: 10.1017/S0031182098003564. PubMed DOI

Kern A, et al. Tick saliva represses innate immunity and cutaneous inflammation in a murine model of Lyme disease. Vector-Borne Zoonot. 2011;11:1343–1350. doi: 10.1089/vbz.2010.0197. PubMed DOI

Jacquet, M. et al. The abundance of the Lyme disease pathogen Borrelia afzelii declines over time in the tick vector Ixodes ricinus. Parasit. Vectors 10, 257 (2017). PubMed PMC

Rosa R, Pugliese A, Norman R, Hudson PJ. Thresholds for disease persistence in models for tick-borne infections including non-viraemic transmission, extended feeding and tick aggregation. J. Theor. Biol. 2003;224:359–376. doi: 10.1016/S0022-5193(03)00173-5. PubMed DOI

Ogden NH, et al. Vector seasonality, host infection dynamics and fitness of pathogens transmitted by the tick Ixodes scapularis. Parasitology. 2007;134:209–227. doi: 10.1017/S0031182006001417. PubMed DOI

Richter D, Allgower R, Matuschka FR. Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii. Emerg. Infect. Dis. 2002;8:1421–1425. doi: 10.3201/eid0812.010519. PubMed DOI PMC

Ogden NH, Nuttall PA, Randolph SE. Natural Lyme disease cycles maintained via sheep by cofeeding ticks. Parasitology. 1997;115:591–599. doi: 10.1017/S0031182097001868. PubMed DOI

Kimura K, et al. Detection of Lyme disease spirochetes in the skin of naturally infected wild sika deer (Cervus nippon yesoensis) by PCR. Appl. Environ. Microbiol. 1995;61:1641–1642. PubMed PMC

Heylen, D. et al. Inefficient co-feeding transmission of Borrelia afzelii in two common European songbirds. Scientific Reports7, 39596 (2017). PubMed PMC

Rynkiewicz EC, et al. Closely-related Borrelia burgdorferi (sensu stricto) strains exhibit similar fitness in single infections and asymmetric competition in multiple infections. Parasit. Vectors. 2017;10:64. doi: 10.1186/s13071-016-1964-9. PubMed DOI PMC

Wang IN, et al. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics. 1999;151:15–30. PubMed PMC

Qiu WG, Dykhuizen DE, Acosta MS, Luft BJ. Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the northeastern United States. Genetics. 2002;160:833–849. PubMed PMC

Brisson D, Dykhuizen DE. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics. 2004;168:713–722. doi: 10.1534/genetics.104.028738. PubMed DOI PMC

Durand J, et al. Cross-immunity and community structure of a multiple-strain pathogen in the tick vector. Appl. Environ. Microbiol. 2015;81:7740–7752. doi: 10.1128/AEM.02296-15. PubMed DOI PMC

Walter KS, Carpi G, Evans BR, Caccone A, Diuk-Wasser MA. Vectors as epidemiological sentinels: patterns of within-tick Borrelia burgdorferi diversity. PLOS Pathog. 2016;12:e1005759. doi: 10.1371/journal.ppat.1005759. PubMed DOI PMC

Strandh, M. & Raberg, L. Within-host competition between Borrelia afzelii ospC strains in wild hosts as revealed by massively parallel amplicon sequencing. Philos. T. Roy. Soc. B370 (2015). PubMed PMC

Derdakova M, et al. Interaction and transmission of two Borrelia burgdorferi sensu stricto strains in a tick-rodent maintenance system. Appl. Environ. Microbiol. 2004;70:6783–6788. doi: 10.1128/AEM.70.11.6783-6788.2004. PubMed DOI PMC

Durand, J., Jacquet, M., Rais, O., Gern, L. & Voordouw, M. J. Fitness estimates from experimental infections predict the long-term strain structure of a vector-borne pathogen in the field. Scientific Reports 7, 1851 (2017). PubMed PMC

Cook MJ. Lyme borreliosis: a review of data on transmission time after tick attachment. International Journal of General Medicine. 2015;8:1–8. PubMed PMC

Ohnishi J, Piesman J, de Silva AM. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc. Natl. Acad. Sci. USA. 2001;98:670–675. doi: 10.1073/pnas.98.2.670. PubMed DOI PMC

Piesman J, Schneider BS, Zeidner NS. Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J. Clin. Microbiol. 2001;39:4145–4148. doi: 10.1128/JCM.39.11.4145-4148.2001. PubMed DOI PMC

Piesman J, Schneider BS. Dynamic changes in Lyme disease spirochetes during transmission by nymphal ticks. Experimental and Applied Acarology. 2002;28:141–145. doi: 10.1023/A:1025351727785. PubMed DOI

Fazzino L, Tilly K, Dulebohn DP, Rosa PA. Long term survival of Borrelia burgdorferi lacking hibernation promotion factor homolog in the unfed tick vector. Infect. Immun. 2015;83:4800–4810. doi: 10.1128/IAI.00925-15. PubMed DOI PMC

Piesman J, Oliver JR, Sinsky RJ. Growth kinetics of the Lyme disease spirochete (Borrelia burgdorferi) in vector ticks (Ixodes dammini) The American journal of tropical medicine and hygiene. 1990;42:352–357. doi: 10.4269/ajtmh.1990.42.352. PubMed DOI

de Silva AM, Fikrig E. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am. J. Trop. Med. Hyg. 1995;53:397–404. doi: 10.4269/ajtmh.1995.53.397. PubMed DOI

Zhu Z. Histological observations on Borrelia burgdorferi growth in naturally infected female Ixodes ricinus. Acarologia. 1998;39:11–22.

Dunham-Ems SM, et al. Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J. Clin. Invest. 2009;119:3652–3665. doi: 10.1172/JCI39401. PubMed DOI PMC

Crippa M, Rais O, Gern L. Investigations on the mode and dynamics of transmission and infectivity of Borrelia burgdorferi sensu stricto and Borrelia afzelii in Ixodes ricinus ticks. Vector Borne and Zoonotic Diseases. 2002;2:3–9. doi: 10.1089/153036602760260724. PubMed DOI

Kahl O, et al. Risk of infection with Borrelia burgdorferi sensu lato for a host in relation to the duration of nymphal Ixodes ricinus feeding and the method of tick removal. Zbl. Bakt.-Int. J. Med. M. 1998;287:41–52. doi: 10.1016/S0934-8840(98)80142-4. PubMed DOI

Piesman J, Mather TN, Sinsky RJ, Spielman A. Duration of tick attachment and Borrelia burgdorferi transmission. J. Clin. Microbiol. 1987;25:557–558. PubMed PMC

Hovius JWR, van Dam AP, Fikrig E. Tick-host-pathogen interactions in Lyme borreliosis. Trends Parasitol. 2007;23:434–438. doi: 10.1016/j.pt.2007.07.001. PubMed DOI

Keesing F, et al. Hosts as ecological traps for the vector of Lyme disease. P. Roy. Soc. B-Biol. Sci. 2009;267:3911–3919. doi: 10.1098/rspb.2009.1159. PubMed DOI PMC

Schwaiger M, Peter O, Cassinotti P. Routine diagnosis of Borrelia burgdorferi (sensu lato) infections using a real-time PCR assay. Clin. Microbiol. Infec. 2001;7:461–469. doi: 10.1046/j.1198-743x.2001.00282.x. PubMed DOI

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