LETTERS and vinegar mixture, locally known as over, a successful control program 6. Radomyos B, Wongsaroj T, Wilairatana kinilaw. 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 tinola (boiled), ginataan could serve as a paradigm for local tinal fl uke infections in northern Thai- (stewed in coconut milk), 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- Philippines 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 Ixodes 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 tick, 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 anaplasmosis, and awareness by health staff and the com- human babesiosis. 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. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 7, July 2007 1131 LETTERS Because we suspected these in- 1 nymphal I. scapularis and 2 adult B. burgdorferi infection in vading ticks were bringing zoonotic Dermacentor 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 Babesia 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 Borrelia 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 Babesia microti) 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 Borrelia burgdorferi, 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 Lyme disease 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.
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