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Evaluating the effectiveness of an integrated tick management approach on multiple pathogen infection in Ixodes scapularis questing nymphs and larvae parasitizing white-footed mice

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Abstract

We investigated the effectiveness of integrated tick management (ITM) approaches in reducing the burden of infection with Borrelia burgdorferi, Babesia microti, and Anaplasma phagocytophilum in Ixodes scapularis. We found a 52% reduction in encountering a questing nymph in the Metarhizium anisopliae (Met52) and fipronil rodent bait box treatment combination as well as a 51% reduction in the combined white-tailed deer (Odocoileus virginianus) removal, Met52, and fipronil rodent bait box treatment compared to the control treatment. The Met52 and fipronil rodent bait box treatment combination reduced the encounter potential with a questing nymph infected with any pathogen by 53%. Compared to the control treatment, the odds of collecting a parasitizing I. scapularis infected with any pathogen from a white-footed mouse (Peromyscus leucopus) was reduced by 90% in the combined deer removal, Met52, and fipronil rodent bait box treatment and by 93% in the Met52 and fipronil rodent bait box treatment combination. Our study highlights the utility of these ITM measures in reducing both the abundance of juvenile I. scapularis and infection with the aforementioned pathogens.

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References

  • Barbour AG, Maupin GO, Teltow GJ, Carter CJ, Piesman J (1996) Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like illness. J Infect Dis 173:403–409

    Article  CAS  Google Scholar 

  • Bharadwaj A, Stafford KC III (2010) Evaluation of Metarhizium anisopliae strain F52 (Hypocreales: Clavicipitaceae) for control of Ixodes scapularis (Acari: Ixodidae). J Med Entomol 47:862–867

    Article  Google Scholar 

  • Bloemer SR, Mount GA, Morris TA, Zimmerman RH, Barnard DR, Snoddy EL (1990) Management of lone star ticks (Acari: Ixodidae) in recreational areas with acaricide applications, vegetative management, and exclusion of white-tailed deer. J Med Entomol 27:543–550

    Article  CAS  Google Scholar 

  • Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP (1982) Lyme disease-a tick-borne spirochetosis? Science 216:1317–1319

    Article  CAS  Google Scholar 

  • Dennis DT, Nekomoto TS, Victor JC, Paul WS, Piesman J (1998) Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the United States. J Med Entomol 35:629–638

    Article  CAS  Google Scholar 

  • Dolan MC, Maupin GO, Schneider BS, Dentale C, Hamon N, Cole C, Zeidner NS, Stafford KC III (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

    Article  CAS  Google Scholar 

  • Diuk-Wasser MA, Liu Y, Steeves TK, Folsom-O’Keefe C, Dardick KR, Lepore T, Bent SJ, Usmani-Brown S, Telford SR III, Fish D, Krause PJ (2014) Monitoring human babesiosis emergence through vector surveillance, New England, USA. Emerg Infect Dis 20:225

    Article  Google Scholar 

  • Diuk-Wasser MA, Vannier E, Krause PJ (2016) Coinfection by Ixodes tick-borne pathogens: Ecological, epidemiological, and clinical consequences. Trends Parasitol 32:30–42

    Article  Google Scholar 

  • Eisen RJ, Eisen L, Beard CB (2016) County-scale distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental United States. J Med Entomol 53:349–386

    Article  Google Scholar 

  • Eisen RJ, Kugeler KJ, Eisen L, Beard CB, Paddock CD (2017) Tick-borne zoonoses in the United States: persistent and emerging threats to human health. ILAR J 58:319–335

    Article  CAS  Google Scholar 

  • Eisen RJ, Eisen L (2018) The blacklegged tick, Ixodes scapularis: an increasing public health concern. Trends Parasitol 34:295–309

    Article  Google Scholar 

  • Gazumyan A, Schwartz JJ, Liveris D, Schwartz I (1994) Sequence analysis of the ribosomal RNA operon of the Lyme disease spirochete, Borrelia burgdorferi Gene 146:57–65

    Article  CAS  Google Scholar 

  • Gray EB, Herwaldt BL (2019) Babesiosis surveillance – United States, 2011–2015. MMWR Surveil Summ 68:1–11

    Article  Google Scholar 

  • Jacobson R, McCall J, Hunter J III, Alva R, Irwin J, Eschner A, Jeannin P, Boeckh A (2004) The ability of fipronil to prevent transmission of Borrelia burgdorferi, the causative agent of Lyme disease to dogs. J Appl Res Vet Med 2:39–45

    CAS  Google Scholar 

  • Jordan RA, Schulze TL (2019) Ability of two commercially available host-targeted technologies to reduce abundance of Ixodes scapularis (Acari: Ixodidae) in a residential landscape. J Med Entomol 56:1095–1101

    Article  Google Scholar 

  • Kilpatrick HJ, LaBonte AM, Stafford KC III (2014) The relationship between deer density, tick abundance, and human cases of Lyme disease in a residential community. J Med Entomol 51:777–784

    Article  Google Scholar 

  • Kugeler KJ, Jordan RA, Schulze TL, Griffith KS, Mead PS (2016) Will culling white-tailed deer prevent Lyme disease? Zoonoses Public Health 63:337–345

    Article  CAS  Google Scholar 

  • Lee X, Coyle DR, Johnson DKH, Murphy MW, McGeehin MA, Murphy RJ, Ragga KF, Paskewitz SM (2014) Prevalence of Borrelia burgdorferi and Anaplasma phagocytophilum in Ixodes scapularis (Acari: Ixodidae) nymphs collected in managed red pine forests in Wisconsin. J Med Entomol 51:694–701

    Article  Google Scholar 

  • Little EAH, Anderson JF, Stafford KC III, Eisen L, Eisen RJ, Molaei G (2019) Predicting spatiotemporal patterns of Lyme disease incidence from passively collected surveillance data for Borrelia burgdorferi sensu lato-infected Ixodes scapularis ticks. Ticks Tick Borne Dis.https://doi.org/10.1016/j.ttbdis.2019.04.010

    Article  PubMed  Google Scholar 

  • Little EAH, Molaei G (2019) Passive tick surveillance: Exploring spatiotemporal associations of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae), Babesia microti (Piroplasmida: Babesiidae), and Anaplasma phagocytophilum (Rickettsiales: Anaplasmataceae) infection in Ixodes scapularis (Acari: Ixodidae). Vector Borne Zoonotic Dis.https://doi.org/10.1089/vbz.2019.2509

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR (2006) Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerg Infect Dis 12:468–474

    Article  Google Scholar 

  • Pancholi P, Kolbert CP, Mitchell PD, Reed KD, Dumler JS, Bakken JS, Telford SR III, Persing DH (1995) Ixodes dammini as a potential vector of human granulocytic ehrlichiosis. J Infect Dis 172:1007–1012

    Article  CAS  Google Scholar 

  • Piesman J, Spielman A (1979) Host-associations and seasonal abundance of immature Ixodes dammini in southeastern Massachusetts. Ann Entomol Soc Am 72:829–832

    Article  Google Scholar 

  • Persing D, Telford SR III, Spielman A, Barthold S (1990) Detection of Borrelia burgdorferi infection in Ixodes dammini ticks with the polymerase chain reaction. J Clin Microbiol 28:566–572

    Article  CAS  Google Scholar 

  • Persing D, Mathiesen D, Marshall W, Telford SR III, Spielman A, Thomford JW, Conrad PA (1992) Detection of Babesia microti by polymerase chain reaction. J Clin Microbiol 30:2097–2103

    Article  CAS  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. http://www.R-project.org/

  • Rand PW, Lubelczyk C, Holman MS, LaCombe EH, Smith RP III (2004) Abundance of Ixodes scapularis (Acari: Ixodidae) after the complete removal of deer from an isolated island, endemic for Lyme disease. J Med Entomol 41:779–784

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schulze TL, Jordan RA, Williams M, Dolan MC (2017) Evaluation of the SELECT tick control system (TCS), a host-targeted bait box, to reduce exposure to Ixodes scapularis (Acari: Ixodidae) in a Lyme disease endemic area of New Jersey. J Med Entomol 54:1019–1024

    Article  Google Scholar 

  • Schwartz AM, Hinckley AF, Mead PS, Hook SA, Kugeler KJ (2017) Surveillance for Lyme disease–United States, 2008-2015. MMWR Surveill Summ 66:1–12

    Article  Google Scholar 

  • Sikes RS (2016) 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mamm 97:663–688

    Article  Google Scholar 

  • Spielman A (1976) Human babesiosis on Nantucket Island: transmission by nymphal Ixodes ticks. Am J Trop Med Hyg 25:784–787

    Article  CAS  Google Scholar 

  • Spielman A, Etkind P, Piesman J, Ruebush IITK, Juranek DD, Jacobs MS (1981) Reservoir hosts of human babesiosis on Nantucket Island. Am J Trop Med Hyg 30:560–565

    Article  CAS  Google Scholar 

  • Stafford KC III, Allan SA (2010) Field applications of entomopathogenic fungi Beauveria bassiana and Metarhizium anispliae F52 (Hyporcreales: Clavicipitaceae) for the control of Ixodes scapularis (Acari: Ixodidae). J Med Entomol 47:1107–1115

    Article  Google Scholar 

  • Stafford KC III, DeNicola AJ, Kilpatrick HJ (2003) Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with reduction of white-tailed deer. J Med Entomol 40:642–652

    Article  Google Scholar 

  • Steiner FE, Pinger RR, Vann CN, Abley MJ, Sullivan B, Grindle N, Clay K, Fuqua C (2006) Detection of Anaplasma phagocytophilum and Babesia odocoilei DNA in Ixodes scapularis (Acari: Ixodidae) collected in Indiana. J Med Entomol 43:437–442

    Article  CAS  Google Scholar 

  • Telford SR III, Dawson JE, Katavolos P, Warner CK, Kolbert CP, Persing DH (1996) Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle. Proc Natl Acad Sci USA 93:6209–6214

    Article  CAS  Google Scholar 

  • Williams SC, DeNicola AJ, Almendinger T, Maddock J (2013) Evaluation of organized hunting as a management technique for overabundant white-tailed deer in suburban landscapes. Wildl Soc Bull 37:137–145

    Article  Google Scholar 

  • Williams SC, Stafford KC III, Molaei G, Linske MA (2018a) Integrated control of nymphal Ixodes scapularis: Effectiveness of white-tailed deer reduction, the entomopathogenic fungus Metarhizium anisopliae, and fipronil-based rodent bait boxes. Vector Borne Zoonotic Dis 18:55–64

    Article  Google Scholar 

  • Williams SC, Little EAH, Stafford KC III, Molaei G, Linske MA (2018b) Integrated control of juvenile Ixodes scapularis parasitizing Peromyscus leucopus in residential settings in Connecticut, United States. Ticks Tick Borne Dis 9:1310–1316

    Article  Google Scholar 

  • Zimmerman G (2007) Review on safety of the entomopathogenic fungus Metarhizium anisopliae Biocontrol Sci Technol 17:879–920

    Article  Google Scholar 

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Acknowledgements

We are grateful to Redding Town Staff and elected officials, specifically Natalie Ketchum, Julia Pemberton, and Doug Hartline for their support and assistance as well as all the collaborating homeowners in Town for allowing us access to their properties. We thank Michael Short, Heidi Stuber, Elizabeth Alves, Laura Hayes, Saryn Kunajukr, and Alex Diaz of The Connecticut Agricultural Experiment Station as well as seasonal research assistants Mark Morris, Stephanie Shea, Heather Whiles, Adam Misiorski, Kelsey Schwenk, Jarrod Bridge, Pronoma Srivastava, and Magalí Bazzano for their technical assistance. Met52 was kindly made available by Novozymes Biological, Inc. This research was funded by a Cooperative Agreement between the Centers for Disease Control and Prevention and The Connecticut Agricultural Experiment Station (Award # 5 U01 CK000182-01). The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

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Correspondence to Goudarz Molaei.

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Little, E.A.H., Williams, S.C., Stafford, K.C. et al. Evaluating the effectiveness of an integrated tick management approach on multiple pathogen infection in Ixodes scapularis questing nymphs and larvae parasitizing white-footed mice. Exp Appl Acarol 80, 127–136 (2020). https://doi.org/10.1007/s10493-019-00452-7

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