ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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1.
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Gern L, Rais O, 1996. Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). J Med Entomol 33: 189–192.
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Dolan MC, Schulze TL, Jordan RA, Dietrich G, Schulze CJ, Hojgaard A, Ullmann AJ, Sackal C, Zeidner NS, Piesman J, 2011. Elimination of Borrelia burgdorferi and Anaplasma phagocytophilum in rodent reservoirs and Ixodes scapularis ticks using a doxycycline hyclate-laden bait. Am J Trop Med Hyg 85: 1114–1120.
-
14.
Dolan MC, Maupin GO, Schneider BS, Denatale C, Hamon N, Cole C, Zeidner NS, Stafford KC, 2004. Control of immature Ixodes scapularis (Acari: Ixodidae) on rodent reservoirs of Borrelia burgdorferi in a residential community of southeastern Connecticut. J Med Entomol 41: 1043–1054.
-
15.
Mather TN, Ribeiro JMC, Moore SI, Spielman A, 1988. Reducing transmission of Lyme disease spirochetes in a suburban setting. Ann N Y Acad Sci 539: 402–403.
-
16.
Mather TN, Ribeiro JM, Spielman A, 1987. Lyme disease and babesiosis: Acaricide focused on potentially infected ticks. Am J Trop Med Hyg 36: 609–614.
-
17.
Pelletier J, Rocheleau J-P, Aenishaenslin C, Masson GD, Lindsay LR, Ogden NH, Bouchard C, Leighton PA, 2022. Fluralaner baits reduce the infestation of Peromyscus spp. mice (Rodentia: Cricetidae) by Ixodes scapularis (Acari: Ixodidae) larvae and nymphs in a natural environment. J Med Entomol 59: 2080–2089.
-
18.
Poche DM, Franckowiak G, Clarke T, Tseveenjav B, Polyakova L, Poche RM, 2021. Efficacy of low-dose fipronil bait against blacklegged tick (Ixodes scapularis) larvae feeding on white-footed mice (Peromyscus leucopus) under simulated field conditions. Parasit Vectors 14: 459.
-
19.
Schulze TL, Jordan RA, Schulze CJ, Healy SP, Jahn MB, Piesman J, 2007. Integrated use of 4-poster passive topical treatment devices for deer, targeted acaricide applications, and Maxforce TMS bait boxes to rapidly suppress populations of Ixodes scapularis (Acari: Ixodidae) in a residential landscape. J Med Entomol 44: 830–839.
-
20.
Stafford KC, Williams SC, van Oosterwijk JG, Linske MA, Zatechka S, Richer LM, Molaei G, Przybyszewski C, Wikel SK, 2020. Field evaluation of a novel oral reservoir-targeted vaccine against Borrelia burgdorferi utilizing an inactivated whole-cell bacterial antigen expression vehicle. Exp Appl Acarol 80: 257–268.
-
21.
Richer LM, Brisson D, Melo R, Ostfeld RS, Zeidner N, Gomes-Solecki M, 2014. Reservoir targeted vaccine against Borrelia burgdorferi: A new strategy to prevent Lyme disease transmission. J Infect Dis 209: 1972–1980.
-
22.
Voordouw MJ, Tupper H, Önder Ö, Devevey G, Graves CJ, Kemps BD, Brisson D, 2013. Reductions in human Lyme disease risk due to the effects of oral vaccination on tick-to-mouse and mouse-to-tick transmission. Vector Borne Zoonotic Dis 13: 203–214.
-
23.
Daniels TJ, Fish D, Falco RC, 1991. Evaluation of host-targeted acaricide for reducing risk of Lyme disease in southern New York state. J Med Entomol 28: 537–543.
-
24.
Hinckley AF, Niesobecki SA, Connally NP, Hook SA, Biggerstaff BJ, Horiuchi KA, Hojgaard A, Mead PS, Meek JI, 2021. Prevention of Lyme and other tickborne diseases using a rodent-targeted approach: A randomized controlled trial in Connecticut. Zoonoses Public Health 68: 578–587.
-
25.
Hornbostel VL, Ostfeld RS, Benjamin MA, 2005. Effectiveness of Metarhizium anisopliae (Deuteromycetes) against Ixodes scapularis (Acari: Ixodidae) engorging on Peromnyscus leucopus. J Vector Ecol 30: 91–101.
-
26.
Mandli JT, 2021. New Frontiers in Integrated Tick Management: Harnessing Environmental and Molecular Technologies to Reduce the Threat of Tick-Borne Disease. Madison, Wisconsin: The University of Wisconsin, Madison.
-
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Ostfeld RS, et al., 2023. Effects of neighborhood-scale acaricidal treatments on infection prevalence of blacklegged ticks (Ixodes scapularis) with three zoonotic pathogens. Pathogens 12: 172.
-
28.
Stafford KC, 1991. Effectiveness of host-targeted permethrin in the control of Ixodes dammini (Acari: Ixodidae). J Med Entomol 28: 611–617.
-
29.
Tsao JI, Wootton JT, Bunikis J, Luna MG, Fish D, Barbour AG, 2004. An ecological approach to preventing human infection: Vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc Natl Acad Sci USA 101: 18159–18164.
-
30.
Goethert HK, Mather TN, Buchthal J, Telford SR III, 2021. Retrotransposon-based blood meal analysis of nymphal deer ticks demonstrates spatiotemporal diversity of Borrelia burgdorferi and Babesia microti reservoirs. Appl Environ Microbiol 87: e02370-20.
-
31.
Goethert HK, Telford SR III, 2022. Limited capacity of deer to serve as zooprophylactic hosts for Borrelia burgdorferi in the northeastern United States. Appl Environ Microbiol 88: e0004222.
-
32.
Goethert HK, Telford SR III, 2022. Host contributions to the force of Borrelia burgdorferi and Babesia microti transmission differ at edges of and within a small habitat patch. Appl Environ Microbiol 88: e0239121.
-
33.
Goethert HK, Mather TN, Johnson RW, Telford SR III, 2021. Incrimination of shrews as a reservoir for Powassan virus. Commun Biol 4: 1319.
-
34.
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Tokarz R, Tagliafierro T, Cucura DM, Rochlin I, Sameroff S, Lipkin WI, 2017. Detection of Anaplasma phagocytophilum, Babesia microti, Borrelia burgdorferi, Borrelia miyamotoi, and Powassan virus in ticks by a multiplex real-time reverse transcription-PCR assay. mSphere 2: e00151-17.
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Minor Hosts Have a Major Impact on the Enzootic Transmission of Borrelia burgdorferi
Heidi Goethert
heidi.goethert@tufts.edu
Heidi Goethert
Cummings School of Veterinary Medicine at Tufts University, Grafton, Massachusetts;
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Alanna O’Callahan
Alanna O’Callahan
Cummings School of Veterinary Medicine at Tufts University, Grafton, Massachusetts;
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Richard Johnson
Richard Johnson
Martha’s Vineyard Tick-borne Illness Reduction Initiative, West Tisbury, Massachusetts
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Patrick Roden-Reynolds
Patrick Roden-Reynolds
Martha’s Vineyard Tick-borne Illness Reduction Initiative, West Tisbury, Massachusetts
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Sam Telford III
Sam Telford III
Cummings School of Veterinary Medicine at Tufts University, Grafton, Massachusetts;
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ABSTRACT.
In the northeast United States, subadult deer ticks feeding on white-footed mice are thought to drive the force of transmission of Borrelia burgdorferi (B. burgdorferi), the agent of Lyme disease. However, control measures targeting mice have produced inconsistent results, suggesting that other animals are significant contributors to enzootic transmission. Such contributions have previously been difficult to quantify. We used a retrotransposon-based host blood meal assay to measure the relative contribution of hosts to enzootic B. burgdorferi transmission at two insular sites in Massachusetts. Over 6 years, we identified mice and deer as the most common larval hosts at our Nantucket Island site. Infected nymphal ticks were derived mainly from mice (35%) and shrews (31%), despite shrews having fed only 12% of larvae. Deer were identified in 19% of the infected nymphs, despite their known reservoir incompetence. Shrews were consistently the most important host in our Martha’s Vineyard site and were identified as the source of 41% of nymphs overall and 39% of the infected nymphs. Sciurids were variable contributors, feeding from 4% to 42% of the larval ticks each year, and contributed no infected nymphs in 2020 and as many as 83% in 2023. We conclude that host contributions to feeding larval ticks change over time and within sites and that shrews may be more influential than mice at some sites. Shrews, sciurids, and even deer may contribute to B. burgdorferi maintenance. Hosts that apparently feed a minor proportion of ticks can have a major impact on the force of B. burgdorferi transmission.
- Supplemental Materials (PDF 128.60 KB)
Author Notes
Financial support: This work was supported by
Data availability: Data from this study have been deposited at Open Science Framework and are available for download at https://osf.io/asfw6/?view_only=f6e23295c7484a76b46350e90da1b66b.
Current contact information: Heidi Goethert, Alanna O’Callahan, and Sam Telford III, Cummings School of Veterinary Medicine, Grafton, MA, E-mails: heidi.goethert@tufts.edu, alanna.o_callahan@tufts.edu, and sam.telford@tufts.edu. Richard Johnson and Patrick Roden-Reynolds, Martha’s Vineyard Tick-borne Illness Reduction Initiative, Edgartown, MA, E-mails: rwilcoxjohnson@yahoo.com and biologist@dukescounty.org.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Kugeler KJ, Schwartz AM, Delorey MJ, Mead PS, Hinckley AF, 2021. Estimating the frequency of Lyme disease diagnoses, United States, 2010–2018. Emerg Infect Dis 27: 616–619.
-
2.
Rollend L, Fish D, Childs JE, 2013. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: A summary of the literature and recent observations. Ticks Tick Borne Dis 4: 46–51.
-
3.
Gern L, Rais O, 1996. Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). J Med Entomol 33: 189–192.
-
4.
Brunner JL, LoGiudice K, Ostfeld RS, 2008. Estimating reservoir competence of Borrelia burgdorferi; hosts: Prevalence and infectivity, sensitivity, and specificity. J Med Entomol 45: 139–147.
-
5.
Mather TN, Wilson ML, Moore SI, Ribeiro JMC, Spielman A, 1989. Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). Am J Epidemiol 130: 143–150.
-
6.
Telford SR III, Mather TN, Moore SI, Wilson ML, Spielman A, 1988. Incompetence of deer as reservoirs of the Lyme disease spirochete. Am J Trop Med Hyg 39: 105–109.
-
7.
Levine JF, Wilson ML, Spielman A, 1985. Mice as reservoirs of the Lyme disease spirochete. Am J Trop Med Hyg 34: 355–360.
-
8.
Spielman A, Wilson ML, Levine JF, Piesman J, 1985. Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Ann Rev Ent 30: 439–460.
-
9.
Donahue J, Piesman J, Spielman A, 1987. Reservoir competence of white-footed mice for Lyme disease spirochetes. Am J Trop Med Hyg 36: 92–96.
-
10.
Anderson JF, Johnson RC, Magnarelli LA, Hyde FW, 1986. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infect Immun 51: 394–396.
-
11.
Brisson D, Dykhuizen DE, Ostfeld RS, 2008. Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proc Biol Sci 275: 227–235.
-
12.
McLean RG, Ubico SR, Cooksey LM, 1993. Experimental infection of the eastern chipmunk (Tamias striatus) with the Lyme disease spirochete (Borrelia burgdorferi). J Wildl Dis 29: 527–532.
-
13.
Dolan MC, Schulze TL, Jordan RA, Dietrich G, Schulze CJ, Hojgaard A, Ullmann AJ, Sackal C, Zeidner NS, Piesman J, 2011. Elimination of Borrelia burgdorferi and Anaplasma phagocytophilum in rodent reservoirs and Ixodes scapularis ticks using a doxycycline hyclate-laden bait. Am J Trop Med Hyg 85: 1114–1120.
-
14.
Dolan MC, Maupin GO, Schneider BS, Denatale C, Hamon N, Cole C, Zeidner NS, Stafford KC, 2004. Control of immature Ixodes scapularis (Acari: Ixodidae) on rodent reservoirs of Borrelia burgdorferi in a residential community of southeastern Connecticut. J Med Entomol 41: 1043–1054.
-
15.
Mather TN, Ribeiro JMC, Moore SI, Spielman A, 1988. Reducing transmission of Lyme disease spirochetes in a suburban setting. Ann N Y Acad Sci 539: 402–403.
-
16.
Mather TN, Ribeiro JM, Spielman A, 1987. Lyme disease and babesiosis: Acaricide focused on potentially infected ticks. Am J Trop Med Hyg 36: 609–614.
-
17.
Pelletier J, Rocheleau J-P, Aenishaenslin C, Masson GD, Lindsay LR, Ogden NH, Bouchard C, Leighton PA, 2022. Fluralaner baits reduce the infestation of Peromyscus spp. mice (Rodentia: Cricetidae) by Ixodes scapularis (Acari: Ixodidae) larvae and nymphs in a natural environment. J Med Entomol 59: 2080–2089.
-
18.
Poche DM, Franckowiak G, Clarke T, Tseveenjav B, Polyakova L, Poche RM, 2021. Efficacy of low-dose fipronil bait against blacklegged tick (Ixodes scapularis) larvae feeding on white-footed mice (Peromyscus leucopus) under simulated field conditions. Parasit Vectors 14: 459.
-
19.
Schulze TL, Jordan RA, Schulze CJ, Healy SP, Jahn MB, Piesman J, 2007. Integrated use of 4-poster passive topical treatment devices for deer, targeted acaricide applications, and Maxforce TMS bait boxes to rapidly suppress populations of Ixodes scapularis (Acari: Ixodidae) in a residential landscape. J Med Entomol 44: 830–839.
-
20.
Stafford KC, Williams SC, van Oosterwijk JG, Linske MA, Zatechka S, Richer LM, Molaei G, Przybyszewski C, Wikel SK, 2020. Field evaluation of a novel oral reservoir-targeted vaccine against Borrelia burgdorferi utilizing an inactivated whole-cell bacterial antigen expression vehicle. Exp Appl Acarol 80: 257–268.
-
21.
Richer LM, Brisson D, Melo R, Ostfeld RS, Zeidner N, Gomes-Solecki M, 2014. Reservoir targeted vaccine against Borrelia burgdorferi: A new strategy to prevent Lyme disease transmission. J Infect Dis 209: 1972–1980.
-
22.
Voordouw MJ, Tupper H, Önder Ö, Devevey G, Graves CJ, Kemps BD, Brisson D, 2013. Reductions in human Lyme disease risk due to the effects of oral vaccination on tick-to-mouse and mouse-to-tick transmission. Vector Borne Zoonotic Dis 13: 203–214.
-
23.
Daniels TJ, Fish D, Falco RC, 1991. Evaluation of host-targeted acaricide for reducing risk of Lyme disease in southern New York state. J Med Entomol 28: 537–543.
-
24.
Hinckley AF, Niesobecki SA, Connally NP, Hook SA, Biggerstaff BJ, Horiuchi KA, Hojgaard A, Mead PS, Meek JI, 2021. Prevention of Lyme and other tickborne diseases using a rodent-targeted approach: A randomized controlled trial in Connecticut. Zoonoses Public Health 68: 578–587.
-
25.
Hornbostel VL, Ostfeld RS, Benjamin MA, 2005. Effectiveness of Metarhizium anisopliae (Deuteromycetes) against Ixodes scapularis (Acari: Ixodidae) engorging on Peromnyscus leucopus. J Vector Ecol 30: 91–101.
-
26.
Mandli JT, 2021. New Frontiers in Integrated Tick Management: Harnessing Environmental and Molecular Technologies to Reduce the Threat of Tick-Borne Disease. Madison, Wisconsin: The University of Wisconsin, Madison.
-
27.
Ostfeld RS, et al., 2023. Effects of neighborhood-scale acaricidal treatments on infection prevalence of blacklegged ticks (Ixodes scapularis) with three zoonotic pathogens. Pathogens 12: 172.
-
28.
Stafford KC, 1991. Effectiveness of host-targeted permethrin in the control of Ixodes dammini (Acari: Ixodidae). J Med Entomol 28: 611–617.
-
29.
Tsao JI, Wootton JT, Bunikis J, Luna MG, Fish D, Barbour AG, 2004. An ecological approach to preventing human infection: Vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc Natl Acad Sci USA 101: 18159–18164.
-
30.
Goethert HK, Mather TN, Buchthal J, Telford SR III, 2021. Retrotransposon-based blood meal analysis of nymphal deer ticks demonstrates spatiotemporal diversity of Borrelia burgdorferi and Babesia microti reservoirs. Appl Environ Microbiol 87: e02370-20.
-
31.
Goethert HK, Telford SR III, 2022. Limited capacity of deer to serve as zooprophylactic hosts for Borrelia burgdorferi in the northeastern United States. Appl Environ Microbiol 88: e0004222.
-
32.
Goethert HK, Telford SR III, 2022. Host contributions to the force of Borrelia burgdorferi and Babesia microti transmission differ at edges of and within a small habitat patch. Appl Environ Microbiol 88: e0239121.
-
33.
Goethert HK, Mather TN, Johnson RW, Telford SR III, 2021. Incrimination of shrews as a reservoir for Powassan virus. Commun Biol 4: 1319.
-
34.
Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, Warman ML, 2000. Preparation of PCR quality mouse genomic DNA with hot sodium hydroxide and Tris (HotSHOT). Biotechniques 29: 52–54.
-
35.
Tokarz R, Tagliafierro T, Cucura DM, Rochlin I, Sameroff S, Lipkin WI, 2017. Detection of Anaplasma phagocytophilum, Babesia microti, Borrelia burgdorferi, Borrelia miyamotoi, and Powassan virus in ticks by a multiplex real-time reverse transcription-PCR assay. mSphere 2: e00151-17.
-
36.
Goethert HK, 2021. Protocol for Bloodmeal Identification in Ticks Using Retrotransposon-Targeted Real Time PCR. Available at: https://doi.org/10.21203/rs.3.pex-1736/v1. Accessed December 17, 2021.
-
37.
Hammer Ø, Harper DAT, Ryan PD, 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4: 9.
-
38.
Tahir D, Meyer L, Fourie J, Jongejan F, Mather T, Choumet V, Blagburn B, Straubinger RK, Varloud M, 2020. Interrupted blood feeding in ticks: Causes and consequences. Microorganisms 8: 910.
-
39.
Backus LH, Perez AML, Foley JE, 2021. Effect of temperature on host preference in two lineages of the brown dog tick, Rhipicephalus sanguineus. Am J Trop Med Hyg 104: 2305–2311.
-
40.
Ginsberg HS, Hickling GJ, Pang G, Tsao J, Fitzgerald M, Ross B, Rulison EL, Burke RL, 2022. Selective host attachment by Ixodes scapularis (Acari: Ixodidae): Tick-lizard associations in the southeastern United States. J Med Entomol 59: 267–272.
-
41.
James AM, Oliver JH, 1990. Feeding and host preference of immature Ixodes dammini, I. scapularis, and I. pacificus (Acari: Ixodidae). J Med Entomol 27: 324–330.
-
42.
Slowik TJ, Lane RS, 2009. Feeding preferences of the immature stages of three western North American Ixodid ticks (Acari) for avian, reptilian, or rodent hosts. J Med Entomol 46: 115–122.
-
43.
Main AJ, Carey AB, Carey MG, Goodwin RH, 1982. Immature Ixodes dammini (Acari: Ixodidae) on small animals in Connecticut, USA. J Med Entomol 19: 655–664.
-
44.
Schmidt KA, Ostfeld RS, Schauber EM, 1999. Infestation of Peromyscus leucopus and Tamias striatus by Ixodes scapularis (Acari: Ixodidae) in relation to the abundance of hosts and parasites. J Med Entomol 36: 749–757.
-
45.
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