Using citizen science to describe the prevalence and distribution of tick bite and exposure to tick-borne diseases in the United States

PLoS ONE

Volumn 13, Issue 7, 2018, Pages

  Nieto, Nathan C ^a   Tanner Porter, W ^a   Wachara, Julie C ^a   Lowrey, Thomas J ^a   Martin, Luke ^b   Motyka, Peter J ^a   Salkeld, Daniel J ^b  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASMA PHAGOCYTOPHILUM; ARTICLE; BABESIA MICROTI; BORRELIA; BORRELIA BURGDORFERI; BORRELIA MIYAMOTOI; CONTROLLED STUDY; GEOGRAPHIC DISTRIBUTION; HUMAN; INFORMATION PROCESSING; MAJOR CLINICAL STUDY; NONHUMAN; NORTH AMERICA; PREVALENCE; SCIENCE; SCIENTIST; SOCIAL PARTICIPATION; TICK; TICK BITE; TICK BORNE DISEASE; UNITED STATES; ANIMAL; CLASSIFICATION; GEOGRAPHY; HEALTH SURVEY; MIXED INFECTION; SPATIAL ANALYSIS; TRANSMISSION;

ANIMALS; COINFECTION; GEOGRAPHY; HUMANS; POPULATION SURVEILLANCE; PREVALENCE; SPATIAL ANALYSIS; TICK BITES; TICK-BORNE DISEASES; TICKS; UNITED STATES;

EID: 85049725715     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0199644     Document Type: Article

References (49)

1. Nelson CA, Saha S, Kugeler KJ, Delorey MJ, Shankar MB, Hinckley AF, et al. Incidence of clinician-diagnosed Lyme Disease, United States, 2005–2010. Emerg Infect Dis. 2015; 21: 1625–1631. https://doi.org/10.3201/eid2109.150417 PMID: 26291194
2. Kilpatrick AM, Dobson ADM, Levi T, Salkeld DJ, Swei A, Ginsberg HS, et al. Lyme disease ecology in a changing world: consensus, uncertainty and critical gaps for improving control. Philos Trans R Soc Lond B Biol Sci. 2017; 372:20160117. https://doi.org/10.1098/rstb.2016.0117 PMID: 28438910
3. Eisen RJ, Kugeler KJ, Eisen L, Beard CB, Paddock CD. Tick-borne zoonoses in the United States: persistent and emerging threats to human health. ILAR J. 2017; https://doi.org/10.1093/ilar/ilx005
4. Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Maleev VV, et al. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis. 2011; 17: 1816–1823. https://doi.org/10.3201/eid1710.101474 PMID: 22000350
5. Krause PJ, Narasimhan S, Wormser GP, Rollend L, Fikrig E, Lepore T, et al. Human Borrelia miyamotoi infection in the United States. N Engl J Med. 2013; 368: 291–293. http://dx.doi.org/10.1056/ NEJMc1215469
6. Krause PJ, Fish D, Narasimhan S, Barbour AG. Borrelia miyamotoi infection in nature and in humans. Clin Microbiol Infect. 2015; 21: 631–639. https://doi.org/10.1016/j.cmi.2015.02.006 PMID: 25700888
7. Pritt BS, Mead PS, Johnson DKH, Neitzel DF, Respicio-Kingry LB, Davis JP, et al. Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: a descriptive study. Lancet Infect Dis. 2016; 16:556–564. https://doi.org/10.1016/S1473-3099(15)00464-8 PMID: 26856777
8. Childs JE, Paddock CD. The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu Rev Entomol. 2003; 48: 307–337. https://doi.org/10.1146/annurev.ento.48.091801.112728 PMID: 12414740
9. Mani RJ, Reichard MV, Morton RJ, Kocan KM, Clinkenbeard KD. Biology of Francisella tularensis subspecies holarctica live vaccine strain in the tick vector Dermacentor variabilis. PLOS One. 2012; 7: e35441. https://doi.org/10.1371/journal.pone.0035441 PMID: 22530023
10. Mani RJ, Metcalf JA, Clinkenbeard KD. Amblyomma americanum as a bridging vector for human infection with Francisella tularensis. PLOS One. 2015; 10(6):e0130513. https://doi.org/10.1371/journal.pone.0130513 PMID: 26121137
11. Foley JE, Nieto NC. Tularemia. Vet Microbiol. 2010; 140: 332–338. https://doi.org/10.1016/j.vetmic.2009.07.017 PMID: 19713053
12. Eisen RJ, Eisen L, Beard CB. County-scale distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental United States. J Med Entomol. 2016; 53: 349–386. https://doi.org/10.1093/jme/tjv237 PMID: 26783367
13. Salkeld DJ, Nieto NC, Carbajales-Dale P, Carbajales-Dale M, Cinkovich SS, Lambin EF. Disease risk and landscape attributes of tick-borne Borrelia pathogens in the San Francisco Bay Area, California. PLOS One, 2015; 10(8):e0134812. https://doi.org/10.1371/journal.pone.0134812 PMID: 26288371
14. Hai VV, Almeras L, Socolovschi C, Raoult D, Parola P, Pages F. Monitoring human tick-borne disease risk and tick bite exposure in Europe: available tools and promising future methods. Ticks Tick Borne Dis 2014; 5: 607–619. https://doi.org/10.1016/j.ttbdis.2014.07.022 PMID: 25178542
15. Eisen L, Eisen RJ. Critical evaluation of the linkage between tick-based risk measures and the occurrence of Lyme disease cases. J Med Entomol 2016; 53: 1050–1062.
16. Lane RS, Steinlein DB, Mun J. Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest. J Med Entomol. 2004; 41: 239–248. https://doi.org/10.1603/0022-2585-41.2.239 PMID: 15061284
17. Freifeld CC, Chunara R, Mekaru SR, Chan EH, Kass-Hout T, Ayala Iacucci A, et al. Participatory epidemiology: use of mobile phones for community-based health reporting. PLOS medicine. 2010; 7(12): e1000376. https://doi.org/10.1371/journal.pmed.1000376 PMID: 21151888.
18. Laaksonen M, Sajanti E, Sormunen JJ, Penttinen R, Hanninen J, Ruohomaki K, et al. Crowdsourcing-based nationwide tick collection reveals the distribution of Ixodes ricinus and I. persulcatus and associated pathogens in Finland. Emerg Microbes Infect 2017; 6: e31. https://doi.org/10.1038/emi.2017.17PMID: 28487561
19. Palmer JRB, Oltra A, Collantes F, Delgado JA, Lucientes J, Delacour S, et al. Citizen science provides a reliable and scaleable tool to track disease-carrying mosquitoes. Nature Comm 2017; 8: 916. https://doi.org/10.1038/s41467-017-00914-9 PMID: 29066710
20. Meentemeyer RK, Dorning MA, Vogler JB, Schmidt D, Garbelotto M. Citizen science helps predict risk of emerging infectious disease. Front Ecol Environ. 2015; 13: 189–194, https://doi.org/10.1890/140299
21. Gasmi S, Ogden NH, Leighton PA, Lindsay LR, Thivierge K. Analysis of the human population bitten by Ixodes scapularis ticks in Quebec, Canada: increasing risk of Lyme disease. Ticks Tick Borne Dis 2016; 7: 1075–1081. https://doi.org/10.1016/j.ttbdis.2016.09.006 PMID: 27650641
22. Ripoche M, Gasmi S, Adam-Poupart A, Koffi JK, Lindsay L. R., Ludwig A., et al. Passive tick surveillance provides an accurate early signal of emerging Lyme Disease risk and human cases in Southern Canada. J Med Entomol. 2018; tjy030, https://doi.org/10.1093/jme/tjy030
23. Xu G, Mather TN, Hollingsworth CS, Rich SM Passive surveillance of Ixodes scapularis (Say), their biting activity, and associated pathogens in Massachusetts. Vector-Borne Zoon Dis. 2016; 16: 520–527. https://doi.org/10.1089/vbz.2015.1912 PMID: 27248292
24. Hall JL, Alpers K, Bown KJ, Martin SJ, Birtles RJ. Use of mass-participation outdoor events to assess human exposure to tickborne pathogens. Emerg Infect Dis. 2017; 23: 463–467. https://doi.org/10.3201/eid2303.161397 PMID: 28221107
25. Furman DP, Loomis EC. The ticks of California (Acari: Ixodida). Bull California Insect Survey 1984; 25: 1–239.
26. Sonenshine D.E., 1979. Ticks of Virginia (Acari, Metastigmata). Insects of Virginia No. 13. Virginia Polytechnic Institute and State University, Blacksburg Va.
27. Dergousoff SJ, Chilton NB. Differentiation of three species of ixodid tick, Dermacentor andersoni, D. variabilis and D. albipictus, by PCR-based approaches using markers in ribosomal DNA. Mol Cell Probes 2007; 21: 343–348. https://doi.org/10.1016/j.mcp.2007.04.003 PMID: 17544620
28. Dergousoff SJ, Galloway TD, Lindsay LR, Curry PS, Chilton NB. Range expansion of Dermacentor variabilis and Dermacentor andersoni (Acari: Ixodidae) near their northern distributional limits. J Med Entomol. 2013; 50: 510–520. http://dx.doi.org/10.1603/ME12193 PMID: 23802445
29. James AM, Freier JE, Keirans JE, Durden LA, Mertins JW, Schlater JL. Distribution, seasonality, and hosts of the Rocky Mountain wood tick in the United States. J Med Entomol. 2006; 43: 17–24. PMID: 16506443
30. James AM, Burdett C, McCool MJ, Fox A, Riggs P. The geographic distribution and ecological preferences of the American dog tick, Dermacentor variabilis (Say), in the U.S.A, Med Vet Entomol. 2015; 29: 178–188. https://doi.org/10.1111/mve.12099 PMID: 25684582
31. Drazenovich N, Foley J, Brown RN. Use of real-time quantitative PCR targeting the msp2 protein gene to identify cryptic Anaplasma phagocytophilum infections in wildlife and domestic animals. Vector Borne Zoonotic Dis. 2006; 6: 83–90. https://doi.org/10.1089/vbz.2006.6.83 PMID: 16584330
32. Teal AE, Habura A, Ennis J, Keithly JS, Madison-Antenucci S. A new real-time PCR assay for improved detection of the parasite Babesia microti. J Clin Microbiol. 2012; 50: 903–908 https://doi.org/10.1128/JCM.05848-11 PMID: 22170915
33. Barbour AG, Bunikis J, Travinsky B, Hoen AG, Diuk-Wasser MA, Fish D, et al. Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. Am J Trop Med Hyg. 2009; 81: 1120–1131. https://doi.org/10.4269/ajtmh.2009.09-0208 PMID: 19996447
34. Springer YP, Jarnevich CS, Barnett DT, Monaghan AJ, Eisen RJ. Modeling the present and future geographic distribution of the Lone Star Tick, Amblyomma americanum (Ixodida: Ixodidae), in the continental United States. Am J Trop Med Hyg. 2015; 93: 875–890. https://doi.org/10.4269/ajtmh.15-0330PMID: 26217042
35. Easton ER, Keirans JE, Gresbrink RA, Clifford CM. The distribution in Oregon of Ixodes pacificus, Dermacentor andersoni, and Dermacentor occidentalis with a note on Dermacentor variabilis (Acarina: Ixodidae). J Med Entomol, 1977; 13:501–506. https://doi.org/10.1093/jmedent/13.4-5.501 PMID: 845890
36. Hamer SA, Bernard AB, Donovan RM, Hartel JA, Wrangham RW, Otali E, et al. Coincident tick infestations in the nostrils of wild chimpanzees and a human in Uganda. Am J Trop Med Hyg. 2013; 89: 924–927. https://doi.org/10.4269/ajtmh.13-0081 PMCID: PMC3820337 PMID: 24080634
37. Forrester JD, Brett M., Matthias J, Stanek D, Springs CB, Marsden-Haug N, et al. Epidemiology of Lyme disease in low-incidence states. Ticks Tick Borne Dis. 2015; 6, 721–723. https://doi.org/10.1016/j.ttbdis.2015.06.005 PMID: 26103924
38. Scott JD, Fernando K, Banerjee SN, Durden LA, Bryne SK, Banerjee M, et al. Birds disperse ixodid (Acari: Ixodidae) and Borrelia burgdorferi-infected ticks in Canada. J Med Entomol. 2001; 38: 493–500. https://doi.org/10.1603/0022-2585-38.4.493 PMID: 11476328
39. Scott JD, Durden LA. First record of Amblyomma rotundatum tick (Acari:Ixodidae) #parasitizing a bird collected in Canada. Syst Appl Acarol. 2015; 20: 151–161.
40. Herwaldt BL, Montgomery S, Woodhall D, Bosserman E. Babesiosis Surveillance– 18 States, 2011. Morb Mortal Wkly Rep. 2012; 61: 505–509.
41. Walter KS, Pepin KM, Webb CT, Gaff HD, Krause PJ, Pitzer VE, et al. Invasion of two tick-borne diseases across New England: harnessing human surveillance data to capture underlying ecological invasion processes. Proc Biol Sci. 2016; 283(1832):20160834. https://doi.org/10.1098/rspb.2016.0834PMID: 27252022
42. Kjemtrup AM, Wainwright K, Miller M, Penzhorn BL, Carreno RA. Babesia conradae, sp. Nov., a small canine Babesia identified in California. Vet Parasitol. 2006; 138: 103–111. https://doi.org/10.1016/j.vetpar.2006.01.044 PMID: 16524663
43. Conrad PA, Kjemtrup AM, Carreno RA, Thomford J, Wainwright K, Eberhard M, et al. Description of Babesia duncani n. sp. (Apicomplexa: Babesiidae) from humans and its differentiation from other piroplasms. Int J Parasit. 2006; 36: 779–789.
44. Dahlgren FS, Mandel EJ, Krebs JW, Massung RF, McQuiston JH. Increasing incidence of Ehrlichia chaffeensis and Anaplasma phagocytophilum in the United States, 2000–2007. Am J Trop Med Hyg. 2011; 85: 124–131. https://doi.org/10.4269/ajtmh.2011.10-0613 PMID: 21734137
45. Padgett K, Bonilla D, Kjemtrup A, Vilcins I-M, Yoshimizu MH, Hui L, et al. Large scale spatial risk and comparative prevalence of Borrelia miyamotoi and Borrelia burgdorferi sensu lato in Ixodes pacificus. PLOS ONE, 2014; 9(10): e110853. https://doi.org/10.1371/journal.pone.0110853 PMID: 25333277
46. Nieto NC, Salkeld DJ. Epidemiology and genetic diversity of Anaplasma phagocytophilum in the San Francisco Bay area, California. Am J Trop Med Hyg. 2016; 95: 50–54. https://doi.org/10.4269/ajtmh.15-0707 PMID: 27139447
47. Lane RS, Brown RN, Piesman J, Peavey CA. Vector competence of Ixodes pacificus and Dermacentor occidentalis (Acari: Ixodidae) for various isolates of Lyme disease spirochetes. J Med Entomol. 1994; 31: 417–424. PMID: 8057316
48. Stromdahl EY, Nadolny RM, Hickling GJ, Hamer SA, Ogden NH, Casal C, et al. Amblyomma americanum (Acari: Ixodidae) ticks are not vectors of the Lyme Disease agent, Borrelia burgdorferi (Spiro-cheatales: Spirochaetaceae): a review of the evidence. J Med Entomol. 2018; https://doi.org/10.1093/jme/tjx250 PMID: 29394366
49. Shock BC, Moncayo A, Cohen S, Mitchell EA, Williamson PC, Lopez G, et al. Diversity of piroplasms detected in blood-fed and questing ticks from several states in the United States. Ticks Tick Borne Dis. 2014; 5: 373–80. https://doi.org/10.1016/j.ttbdis.2014.01.003 PMID: 24709338