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Volume 19, Number 5—May 2013

Letter

Reindeer Warble Fly–associated Human Myiasis, Scandinavia

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Technical Appendicies

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To the Editor: We report migratory myiasis that occurred during 1991–2012 caused by the reindeer warble fly, Hypoderma tarandi (Technical Appendix Figures 1, 2 [PDF - 328 KB - 2 pages]), in 7 tourists to reindeer habitats of northern Scandinavia. We also report 2 additional women (patients 8 and 9), independent of each other, who were asymptomatic but sought medical care in August 2012 after finding 30–60 parasite eggs in scalp hair 3 days after hiking in Kebnekaise and Jämtland Mountains (northern Sweden), respectively.

Patients 1–7 (Table) had enlarged regional lymph nodes and migratory dermal swelling of the head and upper face. Rounded cutaneous swelling of 2–5 cm occurred 1 at a time, persisted for 1–3 days, and reappeared after 2–34 days.

In mid-January 2009, 4 months after initial symptoms, patient 1 felt a sudden pain in his left eye; 10 days later, an ophthalmologist discovered an intraocular larva (Technical Appendix Figure 3 [PDF - 328 KB - 2 pages]). Patient 3 had a swelling on his forehead, which reappeared 2× before his right eyelid swelled; the day after the eyelid swelling disappeared, vision decreased in his right eye. Patients 1, 3, and 7 underwent eye surgery; 1 living larva was extracted from each patient. Patients 3 and 7 lost vision in the affected eye.

For 5 patients, ivermectin was administered orally (≈200–350 µg/kg body weight), on 3–5 occasions in relation to the swellings. Patients 8 and 9 also each received 1 dose of ivermectin; they remained asymptomatic. Patient 3 received the first dose on day 5 after the living larva was extracted because of a new swelling. Swelling recurred on 3 occasions 2 weeks–1.5 months after surgery. In patient 7, swelling reappeared on several occasion 10–30 days after eye surgery, indicating that retrieval of 1 larva does not exclude concomitant occult infestations. This probably was also the case for patient 2, who had a swelling on his upper forehead when pain developed at the root of his nose, where a new swelling appeared 4 days later.

The 3 larvae removed from patients 1, 3, and 7 were identified as H. tarandi, 2 by morphology and 1 by molecular-specific amplification and sequencing (1). Antibodies against hypodermin C, an enzyme released by the larva during migration in host tissues, were detected in 5 of the symptomatic patients (2,3).

H. tarandi eggs take 4–7 days to hatch, depending on the temperature of the hair layer (4); thus, patients 8 and 9 were treated soon after oviposition and were seronegative. Newly hatched H. tarandi larvae can easily dry, so their chance of survival is higher when they are close to scalp skin. Eggs from patient 2 were initially misidentified as head lice eggs but were eventually identified as H. tarandi by T.G. Jaenson (Uppsala). Published photographs of the H. tarandi eggs alongside the eggs of head lice (5) helped identify H. tarandi eggs in patients 8 and 9. According to those patients, H. tarandi eggs could not be removed from the hair with a lice comb. The H. tarandi fly is well adapted to sub-Arctic climate; nearly all reindeer were found to be infested in some districts of northern Finland and Norway (6). Reindeer habitats attract tourists, mostly during summer. H. tarandi is mainly active on warm summer days; warm weather perhaps does not encourage persons to cover their heads, which may predispose for oviposition. Also, persons moving around probably attract more flies than do those staying still, and strong wind, rain, and temperatures <10°C–12°C are thought to inhibit the warble fly’s flight activity and oviposition (7).

Awareness of human infestation by H. tarandi warble flies increased in Sweden and Norway after news media in Sweden described patient 2 (5; http://www.lakartidningen.se/engine.php?articleId=14643). This publication helped in the recognition of symptoms and in shortening diagnostic delay in patients 3–6, 8, and 9. Of the 3 cases for which diagnosis was not delayed, patients 4 and 5 were children of a physician who read our publication and recognized the symptoms; patient 6, herself a physician, also read the article (5). Increased awareness, rather than increased incidence, explains the emergence of new cases. Nine of 12 cases of proven H. tarandi myiasis found in the literature occurred in persons who had ophthalmomyiasis interna (3,8,9); migratory dermal swellings, the clinical signature of hypodermosis, have been reported only in 1 case (10). Such swellings occurred in all the patients reported here, suggesting that clinicians overlooked this finding, possibly because of the overtaking severity of eye complications and the reporting of most previous cases by ophthalmologists (3,8,9). Persons who seek care for migratory dermal swellings during August–December should be asked about recent travel to reindeer habitats.

For 3 patients with ophthalmomyiasis reported here, ophthalmologists initially had difficulty establishing a diagnosis, raising the possibility that some cases of “idiopathic” uveitis from H. tarandi–endemic areas may be caused by H. tarandi. Ophthalmomyiasis should be considered in cases of unilateral uveitis, lens subluxation, and suspicion of intraocular foreign body (3,8,9). Eosinophilia might be absent and should not be used to guide treatment.

Boris KanComments to Author , Kjetil Åsbakk, Kristian Fossen, Arne Nilssen, Rosario Panadero, and Domenico Otranto
Author affiliations: Karolinska University Hospital, Stockholm, Sweden (B. Kan); Norwegian School of Veterinary Science, Tromsø, Norway (K. Åsbakk); University Hospital of Northern Norway, Tromsø, Norway (K. Fossen); Tromsø University Museum, Tromsø (A. Nilssen); Universidad de Santiago de Compostela, Lugo, Spain (R. Panadero); Università degli Studi di Bari, Valenzano, Italy (D. Otranto)

References

  1. Otranto D, Colwell DD, Traversa D, Stevens JR. Species identification of Hypoderma affecting domestic and wild ruminants by morphological and molecular characterization. Med Vet Entomol. 2003;17:31625. DOIPubMed
  2. Asbakk K, Oksanen A, Nieminen M, Haugerud RE, Nilssen AC. Dynamics of antibodies against hypodermin C in reindeer infested with the reindeer warble fly, Hypoderma tarandi. Vet Parasitol. 2005;129:32332. DOIPubMed
  3. Lagacé-Wiens PR, Dookeran R, Skinner S, Leicht R, Colwell DD, Galloway TD. Human ophthalmomyiasis interna caused by Hypoderma tarandi, northern Canada. Emerg Infect Dis. 2008;14:646. DOIPubMed
  4. Karter AJ, Folstad I, Anderson JR. Abiotic factors influencing embryonic development, egg hatching, and larval orientation in the reindeer warble fly, Hypoderma tarandi. Med Vet Entomol. 1992;6:35562. DOIPubMed
  5. Kan B, Åsen C, Åsbakk K, Jaenson TG. Suspected lice eggs in the hair of a boy revealed dangerous parasite [in Swedish]. Lakartidningen. 2010;107:16947 .PubMed
  6. Folstad I, Nilssen AC, Halvorsen O, Andersen J. Why do male reindeer (Rangifer t. tarandus) have higher abundance of second and third instar larvae of Hypoderma tarandi than females? Oikos. 1989;55:8792. DOI
  7. Anderson JR, Nilssen AC. Trapping oestrid parasites of reindeer: the response of Cephenemyia trompe and Hypoderma tarandi to baited traps. Med Vet Entomol. 1996;10:33746. DOIPubMed
  8. Syrdalen P, Stenkula S. Ophthalmomyiasis interna posterior. Graefes Arch Clin Exp Ophthalmol. 1987;225:1036. DOIPubMed
  9. Gjötterberg M, Ingemansson SO. Intraocular infestation by the reindeer warble fly larva: an unusual indication for acute vitrectomy. Br J Ophthalmol. 1988;72:4203. DOIPubMed
  10. Chirico J, Stenkula S, Eriksson B, Gjötterberg M, Ingemansson SO, Pehrson-Palmqvist G, Reindeer warble fly larva as a cause of 3 cases of human myiasis [in Swedish]. Lakartidningen. 1987;84:22078 .PubMed

Table

Technical Appendix

Suggested citation for this article: Kan B, Åsbakk K, Fossen K, Nilssen A, Panadero R, Otranto D. Reindeer warble fly–associated human myiasis, Scandinavia [letter]. Emerg Infect Dis [Internet]. 2013 May [date cited]. http://dx.doi.org/10.3201/eid1905.130145

DOI: 10.3201/eid1905.130145

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Table of Contents – Volume 19, Number 5—May 2013

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Boris Kan, Infectious Diseases Unit, Karolinska University Hospital; 171, 76 Stockholm; Sweden

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