LETTERS and mixture, locally known as over, a successful control program 6. Radomyos B, Wongsaroj T, Wilairatana . Other methods of fi sh prepa- against chronic intestinal parasitoses P, Radomyos P, Praevanich R, Meesom- boon V, et al. Opisthorchiasis and intes- ration were (boiled), ginataan could serve as a paradigm for local tinal fl uke infections in northern Thai- (stewed in ), and sinugba health system development of effec- land. Southeast Asian J Trop Med Public (charcoal-grilled). All echinostome- tive control measures for other en- Health. 1998;29:123–7. infected patients had a history of hav- demic diseases. 7. Belizario VY, de Leon WU, Bersabe MJ, Baird JK, Bangs MJ. A focus of human in- ing eaten snails, kuhol and kiambu-ay, fection by Haplorchis taichui (Trematoda: prepared raw with coconut milk and Acknowledgments Heterophyidae) in the southern Philip- lime juice (kinilaw), especially when pines. J Parasitol. 2004;90:1165–9. We express sincere gratitude for the found in greater abundance during the support, cooperation, and assistance pro- rainy season. Address for correspondence: Vicente Y. vided by the Local Government Unit/Ru- Human echinostome infection re- Belizario, Jr., National Institutes of Health and ral Health Unit of Santa Monica, Surigao sults from ingestion of metacercariae College of Public Health, University of the del Norte, Provincial Health Offi ce, DOH- that encyst in secondary intermedi- Manila, Pedro Gil, Ermita, Manila, PHT Surigao del Norte, V.L. Makabali ate hosts, usually freshwater snails, the Philippines; email: [email protected] Memorial General Hospital, and the gen- tadpoles, or fi sh. E. malayanum uses erous residents of Santa Monica. various species of gastropod mollusks for primary and secondary intermedi- ate developmental stages (2–5). Cer- Vicente Y. Belizario,*† tain species of fi sh may also serve Giovanni G. Geronilla,*† as secondary intermediate hosts (2). Marilyn Benedith M. Anastacio,*† Several mollusks that may serve as Winifreda U. de Leon,† primary and secondary intermedi- Adriano P. Suba-an,‡ Zoonotic Pathogens ate hosts have been identifi ed in the Arlene C. Sebastian,§ in Philippines, including Lymnaea (Bul- and Michael J. Bangs¶ lastra) cumingiana, Radix quadrasi, *National Institutes of Health, Manila, the scapularis, and Physastra hungerfordiana for E. Philippines; †University of the Philippines Michigan malayanum, and Pila luzonica for E. Manila, Manila, the Philippines; ‡Health ilocanum (6,7). Development, Caraga Region, Butuan City, To the Editor: Ixodes scapularis, To our knowledge, this is the fi rst the Philippines; §Rural Health Unit, Santa the black-legged , is the predomi- report of E. malayanum infections in Monica, the Philippines; and ¶Navy Region nant vector of reportable human vec- the southern Philippines. Local eating Northwest, Silverdale, Washington, USA torborne disease in the United States. habits are a strong factor in echino- It transmits agents that cause Lyme stome infections. The general lack of References borreliosis, human , and awareness by health staff and the com- human . I. scapularis–borne munity was a big factor in the poor 1. World Health Organization. Bench aids disease is becoming more frequent as for the diagnosis of intestinal parasites. this tick expands its range from tick- identifi cation of the disease. Clinical Geneva: the Organization; 1994. Plate 3. and laboratory staff and healthcare 2. Monzon RB, Kitikoon V, Thammapalerd endemic foci in the northeastern and providers need training about echino- N, Temcharoen P, Sornmani S, Viyanant upper midwestern United States. stome infections and other intestinal V. Ecological observations on Lymnaea Despite Michigan’s proximity to (Bullastra) cumingiana. Southeast Asian J large tick-endemic areas (Wisconsin foodborne trematode infections. Simi- Trop Med Public Health. 1993;24:563–9. lar environmental, sanitary, and eating 3. Garrison PE. A new intestinal trematode and Minnesota to the west and Indiana practices in the region suggest that the of man. Philippine Journal of Science. to the south), active and passive sur- same parasitoses should be considered 1908;B3:385–93. veillance data indicated that the only 4. Waikagul J. Intestinal fl uke infections in populations of I. scapularis estab- to be widespread in the area. Redirect- Southeast Asia. Southeast Asian J Trop ing vital resources of the local health Med Public Health. 1991;22(Suppl): lished in the state before 2002 were in and government units of the Caraga 158–62. Menominee County in the Upper Pen- region to the periphery and building 5. Radomyos P, Radomyos B, Tangtrongchitr insula (1,2). However, wildlife sam- A. Multi-infection with helminths in adults pling and tick dragging in 2002–2003 local capacity will help empower au- from northeast Thailand as determined by thorities to provide public health ser- post-treatment fecal examination of adult suggested that I. scapularis had begun vices in rural areas, strengthen public worms. Trop Med Parasitol. 1994;45: to invade southwestern Michigan (3), health programs, and further develop 133–5. with nearby populations in northwest- public health infrastructure. More- ern Indiana (4) as the putative source.

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Because we suspected these in- 1 nymphal I. scapularis and 2 adult B. burgdorferi infection in vading were bringing zoonotic variabilis from tick-en- I. scapularis has been reported in pathogens into southwestern Michi- demic sites. Of the adult I. scapularis, Michigan (1–3,8). To our knowledge, gan, we assessed pathogen preva- 17 (60.7%) were positive for B. burg- ours is the fi rst report of A. phago- lence within the state’s invading and dorferi, 4 (14.3%) were positive for A. cytophilum and odocoilei in endemic I. scapularis populations. phagocytophilum, and 2 (7.1%) were ticks in Michigan; they are present in Over a 1.5-week period in April–May positive for Babesia odocoilei (Table). both the endemic and recently invaded 2006, we collected adult I. scapularis We also collected 91 adult and 10 populations. Similar infection rates for by drag sampling at 3 recently invaded nymphal I. scapularis and 5 adult D. these pathogens have been reported in sites in southwestern Michigan and 2 variabilis from newly invaded sites. I. scapularis from Indiana (9). B. burg- tick-endemic sites in Menominee Of the adult I. scapularis, 43 (47.3%) dorferi and A. phagocytophilum are County. We targeted adult I. scapular- were positive for B. burgdorferi, 1 human pathogens; Babesia odocoilei, is in the spring because this life stage (1.1%) was positive for A. phagocy- an intraerythrocytic protozoan para- has had 2 chances of becoming infect- tophilum, and 4 (4.4%) were positive site maintained in transmission cycles ed and because the adult questing peak for Babesia odocoilei. All 4 Babesia in white-tailed deer, is not known to be in Michigan is greater in spring than odocoilei–positive ticks were co-in- pathogenic to humans (7). Several oth- fall (2,3). fected with B. burgdorferi (this rate of er and Babesia species (i.e., All collected ticks were bisected co-infection was signifi cantly greater B. lonestari, B. miyamotoi-like spiro- aseptically, and total DNA was ex- than random expectation; p = 0.046, chetes, and ) from US tracted from half after overnight lysis by Fisher exact test). ticks were not detected in our sample. (DNeasy Tissue Kit; QIAGEN, Va- Within the tick-endemic area, I. scapularis nymphs, which are epi- lencia, CA, USA). We used 3 PCRs comparison with prior survey data (8) demiologically important (10), were to assay for , indicated that the B. burgdorferi infec- not the focus of our sampling. How- B. lonestari, and B. miyamotoi (5); tion rate in adult ticks increased from ever, several were collected, including Anaplasma phagocytophilum (6); and 31.3% in 1992 to 60.7% in the present some infected with B. burgdorferi, A. Babesia spp., including Babesia survey (p<0.001, by Fisher exact test). phagocytophilum, or both (Table). microti and Babesia odocoilei (7). A similar increasing trend was evident These data imply a risk for Lyme Borrelia-positive and Babesia-posi- in the invasion area, where prevalence borreliosis and human anaplasmosis tive amplicons were purifi ed and increased from 37.0% in 2002–2003 in areas endemic for and recently in- sequenced for species identifi cation. (at a collection site 5 km south of our vaded by I. scapularis. For example, Tick densities were highest over- southernmost site; [3]) to 47.3% in incidence in the tick-en- all at tick-endemic Menominee Coun- 2006. This latter trend was only mar- demic zone has increased signifi cantly ty sites; in southwestern Michigan, ginally statistically signifi cant due to over the past 10 years (from 0.33 to they were highest at those sites closest small sample size and the short pe- 1.53 cases per 10,000 persons dur- to the putative source of the Indiana riod between surveys (p = 0.046, by ing 1997–2006; r2 = 0.56, p = 0.01). invasion. We collected 28 adult and 1-tailed Fisher exact test). Incidence in the invasion zone has

Table. Prevalence of 3 pathogens in Ixodes scapularis ticks from 2 Michigan field sites, spring 2006* No. ticks infected or co-infected (%) No. Borrelia Anaplasma Babesia B. burgdorferi and B. burgdorferi and Site Life stage Ix. scapularis burgdorferi phagocytophilum odocoilei A. phagocytophilum B. odocoilei E-1 A 16 9 (56.3) 1 (6.3) 1 (6.3) 1 (6.3) 0 E-2 A 12 8 (66.7) 3 (25.0) 1 (8.3) 1 (8.3) 1 (8.3) N 1 1 (100.0) 0 0 0 0 I-1 A 4 2 (50.0) 0 0 0 0 N 2 0 1 (50.0) 0 0 0 I-2 A 18 9 (50.0) 0 1 (5.6) 0 1 (5.6) N 8 2 (25.0) 1 (12.5) 0 1 (12.5) 0 I-3 A 69 32 (46.4) 1 (1.4) 3 (4.3) 0 3 (4.3) All endemic sites A 28 17 (60.7) 4 (14.3) 2 (7.1) 2† (7.1) 1† (3.6) N 1 1 (100) 0 0 0 0 All invaded sites A 91 43 (47.3) 1 (1.1) 4 (4.4) 0 4‡ (4.4) N 10 2 (20.0) 2 (20.0) 0 1† (10.0) 0 *E, endemic site; A, adult: N, nymph; I, invaded site. †Nonsignificant level of co-infection; p = 0.378–0.640, by Fisher exact test. ‡Significant level of co-infection; p = 0.046, by Fisher exact test.

1132 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 7, July 2007 LETTERS been much lower (mean 0.03 cases Sarah A. Hamer,* Lyme borreliosis agents Borrelia burg- per 10,000 persons over same period) Pamela L. Roy,* dorferi in North America and Borrelia af- zelii in Europe. Microbiology. 2004;150: but appears to be increasing. Further Graham J. Hickling,† 1741–55. increases in tick population size, in- Edward D. Walker,* 6. Zeidner NS, Burkot TR, Massung R, fection, and co-infection can be ex- Erik S. Foster,‡ Nicholson WL, Dolan MC, Rutherford pected as the invasion continues (9). Christina C. Barber,* JS, et al. Transmission of the agent of hu- man granulocytic by Ixodes Thus, medical practitioners in south- and Jean I. Tsao* spinipalpis ticks: evidence of an enzootic western Michigan should be aware of *Michigan State University, East Lansing, cycle of dual infection with Borrelia burg- the changing increasing risk for tick- Michigan, USA; †University of Tennessee, dorferi in northern Colorado. J Infect Dis. 2000;182:616–9. borne diseases and consider disease Knoxville, Tennessee, USA; and ‡Michigan 7. Armstrong PM, Katavolos P, Caporale resulting from these pathogens during Department of Community Health, East DA, Smith RP, Spielman A, Telford S III. diagnosis. Lansing, Michigan, USA Diversity of Babesia infecting deer ticks (Ixodes dammini). Am J Trop Med Hyg. References 1998;58:739–42. Acknowledgments 8. Walker ED, Smith TW, DeWitt J, Beaudo DC, McLean RG. Prevalence of Borrelia We thank M. Rosen, K. Boatman, 1. Walker ED, Stobierski MG, Poplar ML, burgdorferi in host-seeking ticks (, and G. Hamer for fi eld and laboratory as- Smith TW, Murphy AJ, Smith PC, et al. ) from a Lyme disease endemic Geographic distribution of ticks (Acari: sistance; H. Goethert and S. Telford III for area in northern Michigan. J Med Ento- Ixodidae) in Michigan, with emphasis on mol. 1994;31:524–8. providing positive control Babesia microti Ixodes scapularis and Borrelia burgdor- 9. Steiner FE, Pinger RR, Vann CN, Abley and Babesia odocoilei DNA; the private feri. J Med Entomol. 1998;35:872–82. MJ, Sullivan B, Grindle N, et al. Detection landowners in Menominee County for 2. Strand MR, Walker ED, Merritt RW. of Anaplasma phagocytophilum and Ba- Field studies on Ixodes dammini in the their cooperation; and the Michigan De- besia odocoilei DNA in Ixodes scapularis Upper Peninsula of Michigan. Vector (Acari: Ixodidae) collected in Indiana. J partment of Natural Resources for access Control Bulletin of North Central States. Med Entomol. 2006;43:437–42. to fi eld sites. 1992;1:11–8. 10. Stafford KC III, Cartter ML, Magnarelli 3. Foster E. Ixodes scapularis (Acari: Ix- LA, Ertel SH, Mshar PA. Temporal cor- This study was supported by the De- odidae) and Borrelia burgdorferi in south- relations between tick abundance and partment of Fisheries and Wildlife, Michi- west Michigan: population ecology and prevalence of ticks infected with Borrelia verifi cation of a geographic risk model gan State University; cooperative agree- burgdorferi and increasing incidence of [master’s thesis]. East Lansing (MI): ment no. CI00171-01 from the Centers for Lyme disease. J Clin Microbiol. 1998;36: Michigan State University; 2004. 1240–4. Disease Control and Prevention (graduate 4. Pinger RR, Timmons L, Karris K. Spread assistantship to S.A.H.), and grant 4T35 of Ixodes scapularis (Acari: Ixodidae) in RR017491-04 from the National Institutes Indiana: collections of adults in 1991– Address for correspondence: Sarah A. Hamer, of Health (fellowship to C.C.B.). 1994 and description of a Borrelia burg- Department of Fisheries and Wildlife, Michigan dorferi–infected population. J Med Ento- State University, 13 Natural Resources Bldg, mol. 1996;33:852–5. The opinions expressed by authors contribut- 5. Bunikis J, Garpmo U, Tsao J, Berglund East Lansing, MI 48824, USA; email: hamer@ ing to this journal do not necessarily refl ect the J, Fish D, Barbour AG. Sequence typing msu.edu opinions of the Centers for Disease Control and reveals extensive strain diversity of the Prevention or the institutions with which the au- thors are affi liated.

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