Ahead of Print -Lyme Disease, Virginia, USA, 2000–2011 - Volume 20, Number 10—October 2014 - Emerging Infectious Disease journal - CDC

full-text ►

Ahead of Print -Lyme Disease, Virginia, USA, 2000–2011 - Volume 20, Number 10—October 2014 - Emerging Infectious Disease journal - CDC

Volume 20, Number 10—October 2014

Research

Lyme Disease, Virginia, USA, 2000–2011

On This Page

• Methods
• Results
• Discussion
• Suggested Citation

Figures

• Figure 1
• Figure 2
• Figure 3
• Figure 4
• Figure 5

Tables

• Table

R. Jory Brinkerhoff , Will F. Gilliam, and David Gaines

Author affiliations: University of Richmond, Richmond, Virginia, USA (R.J. Brinkerhoff, W.F. Gilliam);University of KwaZulu-Natal, Pietermaritzburg, South Africa (R.J. Brinkerhoff); Virginia Department of Health, Richmond (D. Gaines)

Suggested citation for this article

Abstract

Lyme disease, caused by the bacterium Borrelia burgdorferi and transmitted in the eastern United States by the black-legged tick (Ixodes scapularis), is increasing in incidence and expanding geographically. Recent environmental modeling based on extensive field collections of host-seeking I. scapularis ticks predicted a coastal distribution of ticks in mid-Atlantic states and an elevational limit of 510 m. However, human Lyme disease cases are increasing most dramatically at higher elevations in Virginia, a state where Lyme disease is rapidly emerging. Our goal was to explore the apparent incongruity, during 2000–2011, between human Lyme disease data and predicted and observed I. scapularis distribution. We found significantly higher densities of infected ticks at our highest elevation site than at lower elevation sites. We also found that I. scapularis ticks in Virginia are more closely related to northern than to southern tick populations. Clinicians and epidemiologists should be vigilant in light of the changing spatial distributions of risk.

Lyme disease (LD), caused by the bacterium Borrelia burgdorferi and transmitted in the eastern United States by the black-legged tick (Ixodes scapularis), is the most common vector-transmitted disease in North America (1). Maintained in an enzootic cycle comprising competent vertebrate reservoir host species, B. burgdorferi is transmitted to humans by the bite of an I. scapularis nymph or adult that acquired infection during a blood feeding as a nymph or larva (2). Although the principal reservoir host for this pathogen, the white-footed deer mouse, Peromyscus leucopus, is wildly distributed throughout North America, LD is generally confined to 2 geographic foci in the eastern United States: 1 in the upper Midwest and 1 in the Northeast (2–5). Densities of host-seeking I. scapularis nymphs correlate significantly with cases of human LD (3), but this species has been reported throughout much of eastern North America (6–9). Nationally, LD incidence increased during 1992–2002, but overall numbers of confirmed cases have since remained relatively stable (1,10).

In some locations, LD incidence recently has increased dramatically; in Virginia, the number of confirmed cases nearly tripled from 2006 to 2007 (http://www.vdh.virginia.gov/epidemiology/surveillance/surveillancedata/index.htm) to ≈12.4 cases per 100,000 residents, well above the 1998–2006 average of 2.2 per 100,000 (1). A 1990 report of LD cases in Virginia noted that the disease was rare in the early 1980s but apparently increased in incidence and geographic distribution through the late 1980s, leading the authors to conclude that the disease was expanding southward (11). Before 2006, most studies of I. scapularis ticks in Virginia focused on the eastern and southeastern parts of the state and found that densities of I. scapularisticks declined, as did their rate of infection with B. burgdorferi, with distance from the coast (12,13). Several early surveys for I. scapularis ticks in Virginia’s neighboring states of North Carolina and Maryland also found them to be most abundant on the Coastal Plain but absent or less common in the Piedmont and Appalachian Mountains. During 1983–1987, Apperson et al. surveyed 1,629 hunter-killed deer from the Coastal Plain, Piedmont, and Appalachian Mountain regions of North Carolina and found I. scapularis ticks only on deer from the Coastal Plain (14). Amerasinghe et al. surveyed 1,281, and 922 hunter-killed deer in 1989 and 1991, respectively, at sites from the Coastal Plain to the Appalachian Mountains of Maryland and found I. scapularis ticks on 59%–70% of deer on the Coastal Plain, fewer on deer in the Piedmont Region, and on only 1%–5% of deer in the Appalachian Mountains (15,16).

Although I. scapularis ticks exist in the southeastern United States (6–9), they are most easily detected by drag sampling, a method used as a proxy for risk to tick exposure (5), in areas associated with highest LD incidence, i.e., the Northeast (New Jersey through Massachusetts) and upper Midwest (Wisconsin and Minnesota) (3,5,17). The difference in apparent abundance of I. scapularis ticks and risk for LD between the northern and southeastern United States has been the subject of much discussion and debate (18) and might be related, either through behavioral or physiologic mechanisms, to genetic differences between I. scapularis populations in these regions (7,19–22). Population genetic structure of I. scapularis ticks has shown that dynamic range shifts are likely to have occurred in recent evolutionary history (19–22) and that 2 distinct lineages within this species can be identified; a relatively genetically uniform “American clade” exists in the northern United States (although this lineage has also been detected in the South), and a genetically diverse “southern clade,” members of which have been found only in the South (20). Although other nomenclatures have been proposed for these 2 lineages (e.g., clades A and B for northern and southern lineages, respectively [19]), we follow the terminology established by Norris et al.: “American” describes the widely distributed yet less diverse clade and “southern” describes the geographically restricted yet more diverse mtDNA clade of I. scapularis ticks (20).

Range expansion of I. scapularis ticks over relatively short periods has been observed (23,24). Moreover, recent environmental modeling, based on extensive field collections of host-seeking I. scapularis ticks, suggests that this species suggests that the range of this species is expanding widely and its occurrence in a given area depends on the lack of abiotic drivers, vapor pressure deficit and elevation (5,25). In Virginia, studies found that I. scapularisticks were concentrated in in northern sites; very few ticks were reported in other parts of the state (5,17,25). In contrast, human LD cases at inland, higher-elevation locations have increased in recent years in Virginia (http://www.vdh.virginia.gov/epidemiology/surveillance/surveillancedata/index.htm). The incongruity between human case and vector abundance datasets might be explained by recent (i.e., since 2007) spatial and/or numerical expansion of I. scapularis populations. We hypothesized that density ofB. burgdorferi–infected ticks would be highest in counties associated with high incidence of human disease if epidemiologic data represent cases in tick-endemic areas. In contrast, low numbers of infected ticks in areas of high human disease might indicate either misdiagnosis or allochthonous exposure.

Dr Brinkerhoff is an assistant professor at the University of Richmond and holds an honorary senior lectureship in the School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa. His research focuses on the ecology, evolution, and epidemiology of bacterial pathogens transmitted by arthropod vectors.

Acknowledgments

We thank M. Massaro, R. Kelly, and L. Spicer for assistance with sample collection and processing of laboratory samples. We also thank 2 anonymous reviewers for their thoughtful comments on an earlier draft of this manuscript.

Funding for this project was provided by a Thomas F. and Kate Miller Jeffress Memorial Trust Award (J-1036) to R.J.B. and a summer research fellowship to W.F.G. provided through the University of Richmond School of Arts and Sciences.

References

1. Bacon RM, Kugeler KJ, Mead PS. Surveillance for LD—United States, 1992–2006. MMWR Surveill Summ. 2008;57:1–9 .PubMed
2. Barbour AG, Fish D. The biological and social phenomenon of LD. Science. 1993;260:1610–6. DOIPubMed
3. Pepin KM, Eisen RJ, Mead PS, Piesman J, Fish D, Hoen AG, Geographic variation in the relationship between human LD incidence and density of infected host–seeking Ixodes scapularis nymphs in the eastern United States. Am J Trop Med Hyg. 2012;86:1062–71. DOIPubMed
4. Centers for Disease Control and Prevention. LD incidence rates by state, 2002–2011 [cited 2013 May 7].http://www.cdc.gov/lyme/stats/chartstables/incidencebystate.html
5. Diuk-Wasser MA, Hoen AG, Cislo P, Brinkerhoff R, Hamer SA, Rowland M, Human risk of infection with Borrelia burgdorferi, the LD agent, in eastern United States. Am J Trop Med Hyg. 2012;86:320–7. DOIPubMed
6. Goddard J. Ecological studies of adult Ixodes scapularis in central Mississippi: questing activity in relation to time of year, vegetation type, and meteorologic conditions. J Med Entomol. 1992;29:501–6 .PubMed
7. Rich SM, Caporale DA, Telford SR, Kocher TD, Hartl DL, Spielman A. Disctribution of the Ixodes ricinus–like ticks of eastern North America. Proc Natl Acad Sci U S A. 1995;92:6284–8. DOIPubMed
8. Durden LA, Oliver JH Jr, Banks CW, Vogel GN. Parasitism of lizards by immature stages of the blacklegged tick, Ixodes scapularis (Acari, Ixodidae).Exp Appl Acarol. 2002;26:257–66. DOIPubMed
9. Goddard J, Piesman J. New records of immature Ixodes scapularis from Mississippi. J Vector Ecol. 2006;31:421–2. DOIPubMed
10. Centers for Disease Control and Prevention. Incidence by state, 2005–2010 [cited 2012 Jul 1].http://www.cdc.gov/lyme/stats/chartstables/incidencebystate.html
11. Heimberger T, Jenkins S, Russell H, Duma R. Epidemiology of LD in Virginia. Am J Med Sci. 1990;300:283–7. DOIPubMed
12. Casteel M, Sonenshine D. Abundance of adult Ixodes scapularis and infection with Borrelia burgdorferi in eastern Virginia. Va J Sci.1996;47:293–300.
13. Sonenshine DE, Ratzlaff RE, Troyer J, Demmerle S, Demmerle ER, Austin WE, Borrelia burgdorferi in eastern Virginia: comparison between a coastal and inland locality. Am J Trop Med Hyg. 1995;53:123–33 .PubMed
14. Apperson CS, Levine JF, Nicholson WL. Geographic occurrence of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) infesting white-tailed deer in North Carolina. J Wildl Dis. 1990;26:550–3. DOIPubMed
15. Amerasinghe FP, Breisch NL, Azad AF, Gimpel WF, Greko M, Neidhardt MK, Distribution, density and LD spirochete infection in Ixodes dammini(Acari: Ixodidae) on white-tailed deer in Maryland. J Med Entomol. 1992;29:54–61 .PubMed
16. Amerasinghe FP, Breisch NL, Neidhardt K, Pagac B, Scott TW. Increasing density and Borrelia burgdorferi infection of deer-infesting Ixodes dammini (Acari:Ixodidae) in Maryland. J Med Entomol. 1993;30:858–64 .PubMed
17. Diuk-Wasser MA, Hoen AG, Cortinas R, Yaremych-Hamer S, Tsao J, Kitron U, Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. J Med Entomol. 2006;43:166–76. DOIPubMed
18. Stromdahl EY, Hickling GJ. Beyond Lyme: aetiology of tick-borne human diseases with emphasis on the south-eastern United States. Zoonoses Public Health. 2012;59(Suppl. 2):48–64. DOIPubMed
19. Qiu WG, Dykhuizen DE, Acosta MS, Luf BJ. Geographic uniformity of the LD spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the northeastern United States. Genetics. 2002;160:833–49 .PubMed
20. Norris DE, Klompen JSH, Keirans JE, Black WIC. Population genetics of Ixodes scapularis (Acari: Ixodidae) based on mitochondrial 16S and 12S genes. J Med Entomol. 1996;33:78–89 .PubMed
21. Van Zee J, Black WC, Levin M, Goddard J, Smith J, Piesman J. High SNP density in the black-legged tick, Ixodes scapularis, the principal vector of LD spirochetes. Ticks Tick Borne Dis. 2013;4:63–71.
22. Humphrey PT, Caporale DA, Brisson D. Uncoordinated phylogeography of Borrelia burgdorferi and its tick vector Ixodes scapularis. Evolution.2010;64:2653–63. DOIPubMed
23. Hamer SA, Tsao JI, Walker ED, Hickling GJ. Invasion of the LD vector Ixodes scapularis: implications for Borrelia burgdorferi endemicity.EcoHealth. 2010;7:47–63. DOIPubMed
24. Lee X, Hardy K, Johnson DH, Paskewitz SM. Hunter-killed deer surveillance to assess changes in the prevalence and distribution of Ixodes scapularis (Acari:Ixodiae) in Wisconsin. J Med Entomol. 2013;50:632–9. DOIPubMed
25. Diuk-Wasser MA, Vourc’h G, Cislo P, Hoen AG, Melton F, Hamer SA, Field and climate-based model for predicting the density of host-seeking nymphal Ixodes scapularis, an important vector of tick-borne diseases agents in the eastern United States. Glob Ecol Biogeogr. 2010;19:504–14.
26. Centers for Disease Control and Prevention. Recommendations for test performance and interpretation from the Second National Conference on Serologic Diagnosis of LD. MMWR Morb Mortal Wkly Rep. 1995;44:590–1 .PubMed
27. Engstrom SM, Shoop E, Johnson RC. Immunoblot interpretation criteria for serodiagnosis of early LD. J Clin Microbiol. 1995;33:419–27.PubMed
28. ESRI. ESRI demographic updates: 2012/2017, and ESRI white paper. ESRI. 2012; http://www.esri.com/library/whitepapers/pdfs/demographic-update-methodology-2012.pdf
29. Falco RC, Fish D. A comparison of methods for sampling the deer tick, Ixodes dammini, in a LD-endemic area. Exp Appl Acarol. 1992;14:165–73.DOIPubMed
30. Sonenshine DE. Ticks of Virginia (Acari, Metastigmata). Insects of Virginia series, no. 13. Blacksburg (VA): Virginia Polytechnic Institute and State University Press. 1979. 35 pp.
31. Brinkerhoff RJ, Collinge SK, Bai Y, Ray C. Are carnivores universally good sentinels of plague? Vector Borne Zoonotic Dis. 2009;9:491–7.DOIPubMed
32. Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agentsBorrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology. 2004;150:1741–55. DOIPubMed
33. Trout RT, Steelman CD, Szalanski AL. Population genetics and phylogeography of Ixodes scapularis from canines and deer in Arkansas. Southwest Entomologist. 2009;34:273–87. DOI
34. Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C content biases. Mol Biol Evol. 1992;9:678–87 .PubMed
35. Rosen ME, Hamer SA, Gerhardt RR, Jones CJ, Muller LI, Scott MC, Borrelia burgdorferi not detected in widespread Ixodes scapularis (Acari: Ixodidae) collected from white-tailed deer in Tennessee. J Med Entomol. 2012;49:1473–80. DOIPubMed
36. Oliver JH Jr, Cummins GA, Joiner MS. Ixodes scapularis (Acari: Ixodidae) parasitizing lizards from the southeastern USA. J Parasitol.1993;79:684–9. DOIPubMed
37. Oliver JH Jr, Owsley MR, Hutcheson HJ, James AM, Chen C, Irby WS, Conspecificity of the ticks Ixodes scapularis and I. dammini (Acari: Ixodidae).J Med Entomol. 1993;30:54–63 .PubMed
38. Spielman A, Levine JF, Wilson ML. Vectorial capacity of North American Ixodes ticks. Yale J Biol Med. 1984;57:507–13 .PubMed
39. Estrada-Peña A. Increasing habitat suitability in the United States for the tick that transmits LD: a remote sensing approach. Environ Health Perspect. 2002;110:635–40. DOIPubMed
40. Lantos PM, Brinkerhoff RJ, Wormser GP, Clemen R. Empiric antibiotic treatment of erythema migrans–like skin lesions as a function of geography: a clinical and cost effectiveness modeling study. Vector Borne Zoonotic Dis. 2013;13:877–83. DOIPubMed

Figures

• Figure 1. Locations of 4 field sites at which ticks were sampled, Virginia, May-July 2011. Circles indicate sampling areas. LE, Lesesne State Forest; AB, Appomattox-Buckingham State Forest; GR, University of Richmond–owned field site; CR, Crawfords...
• Figure 2. Progressive geographic spread of human Lyme disease across Virginia, 2001–2011. Data were reported by the Virginia Department of Health http://www.vdh.virginia.gov/epidemiology/surveillance/surveillancedata/index.htm. Cases per 100,000 population were calculated by county or...
• Figure 3. Variation in estimated prevalence of Borrelia burgdorferi infection in Ixodes scapularis nymphs at 4 field sites in Virginia. Sites are arranged west to east from left to right. LE,...
• Figure 4. Maximum-likelihood phylogenetic reconstruction of Ixodes scapularis lineages based on 16S rRNA gene sequences using Tamura 3-parameter model (35). All samples beginning with IS were collected during this study; reference......
• Figure 5. Centroids of annual incidence, by county, Virginia, 2000–2011. The size of each circle represents the annual number of cases reported by the Virginia Department of Health and is proportional...

Table

• Table. Average density of host-seeking Ixodes scapularis nymphs, average prevalence of Borrelia burgdorferi–infected nymphs, and average annual LD incidence in 5 counties, Virginia

Suggested citation for this article: Brinkerhoff RJ, Gilliam WF, Gaines D. Lyme disease, Virginia, USA, 2000–2011. Emerg Infect Dis [Internet]. 2014 Oct [date cited]. http://dx.doi.org/10.3201/eid2010.130782

DOI: 10.3201/eid2010.130782

The reference has no authors. Please proof carefully. (in reference 6 "Goddard J. Ecological studies of, 1992").

Medline indexes "Va J Sci" but cannot find a listing for reference 12 "Casteel, Sonenshine, 1996". Please check the reference for accuracy.

Medline indexes "Glob Ecol Biogeogr" but cannot find a listing for reference 25 "Diuk-Wasser, Vourc’h, Cislo, Hoen, Melton, Hamer, et al., 2010". Please check the reference for accuracy.

Medline cannot find the journal "Southwest Entomologist" (in reference 33 "Trout, Steelman, Szalanski, 2009"). Please check the journal name.