Surveillance and outbreak report Human myiasis caused by the reindeer warble fly, Hypoderma tarandi, case series from Norway, 2011 to 2016 J Landehag ¹ , A Skogen ¹ , K Åsbakk ² , B Kan ³ 1. Department of Paediatrics, Finnmark Hospital Trust, Hammerfest, Norway 2. UiT The Arctic University of Norway, Department of Arctic and Marine Biology, Tromsø, Norway 3. Unit of Infectious Diseases, Department of Medicine, Karolinska Institutet, Stockholm, Sweden Correspondence: Kjetil Åsbakk ([email protected]) Citation style for this article: Landehag J, Skogen A, Åsbakk K, Kan B. Human myiasis caused by the reindeer warble fly, Hypoderma tarandi, case series from Norway, 2011 to 2016. Euro Surveill. 2017;22(29):pii=30576. DOI: http://dx.doi.org/10.2807/1560-7917.ES.2017.22.29.30576 Article submitted on 01 September 2016 / accepted on 14 December 2016 / published on 20 July 2017 Hypoderma tarandi causes myiasis in reindeer and northern hemisphere regions (Alaska, Canada, Nordic caribou (Rangifer tarandus spp.) in most northern countries in Europe including Greenland (self-govern- hemisphere regions where these animals live. We ing territory of Denmark) and Russia) where these ani- report a series of 39 human myiasis cases caused by mals live [5]. H. tarandi in Norway from 2011 to 2016. Thirty-two were residents of Finnmark, the northernmost county Most of the 24 human cases of myiasis caused by H. of Norway, one a visitor to Finnmark, and six lived in tarandi reported in Norway and other countries in the other counties of Norway where reindeer live. Clinical literature from 1982 to 2016 [6-17] developed oph- manifestations involved migratory dermal swellings thalmomyiasis interna (OMI), a condition where the of the face and head, enlargement of regional lymph larva has invaded the eye globe, often leading to vis- nodes, and periorbital oedema, with or without eosin- ual impairment. Most of them were visitors to north- ophilia. Most cases of human myiasis are seen in tropi- ern parts of Norway and Sweden. Two cases were cal and subtropical countries, and in tourists returning from Nunavut (northern Canada) [13] and one from from such areas. Our findings demonstrate that myia- Greenland [17]. Here we present clinical and epidemi- sis caused by H. tarandi is more common than previ- ological features from a large case series of an addi- ously thought. Healthcare professionals in regions tional 39 consecutive human cases of myiasis caused where there is a likelihood of human infestation with by H. tarandi, mostly in children in northern Norway, H. tarandi (regions populated by reindeer), or treat- from 2011 to 2016. ing returning travellers, should be aware of the con- dition. All clinicians are advised to obtain a detailed Methods travel history when assessing patients with migratory dermal swellings. On clinical suspicion, ivermectin Recruitment of cases and setting should be given to prevent larval invasion of the eye Patients with suspected myiasis (transitional dermal (ophthalmomyiasis). Since H. tarandi oviposits on hair, swellings of the face or head, history of residence in or we suggest wearing a hat as a prevention measure. visit to a reindeer-inhabited area in summer or autumn) were recruited from August 2011 to October 2016. Introduction Most were recruited by the Department of Paediatrics, Myiasis is the condition where fly larvae have infested Finnmark Hospital Trust (Hammerfest, Finnmark) and a mammal and feed on its tissues. Cutaneous myiasis by primary care physicians in Finnmark, the remainder can be subdivided into furuncular, migratory (creep- by primary care physicians in other counties of Norway. ing) and wound myiasis [1,2]. Cutaneous myiasis, the A blood sample was taken for serological assaying. most common form in humans, is endemic in poor Diagnosis was based on clinical manifestations, serol- populations of many tropical and subtropical countries ogy and other findings. Data regarding baseline char- [3,4]. In Europe, myiasis is a relatively common travel- acteristics (age, sex, occupation, residence and clinical associated skin condition [1,2]. Migratory myiasis in history) were collected, and consent to publish case humans is caused by Gasterophilus and Hypoderma details was obtained from each patient. The patients flies (order Diptera, family Oestridae) [5]. Hypoderma were diagnosed and managed consecutively as they tarandi causes myiasis in reindeer and caribou in most were recruited. www.eurosurveillance.org 1 Figure 1 Figure 2 Serum samples from an 8-year-old child with myiasis Myiasis cases caused by Hypoderma tarandi, by year, caused by Hypoderma tarandi infestation, Norway, 2013 children and adults, Norway, 2011–2016 (n = 39) 110 18 Negative control Children 16 Adults 90 October Positive control 14 70 November 12 r 50 e 10 b m u 8 30 N ELISA percentage 6 10 4 -10 2 1/50 1/100 1/200 1/400 1/800 1/1,600 1/3,200 1/6,400 0 2011 2012 2013 2014 2015 2016 Serum dilution Year Symptom onset: October 2013. Serum samples assayed (ELISA) for antibodies (IgG) against Hypodermin C. First sample (October The children ranged in age from 3 to 12 years, and the adults from 2013) giving suspicion of myiasis, second sample (14 days later in 20 to 66 years. 2011 cases were diagnosed retrospectively in 2013. November 2013) confirming seropositivity. (Merck KGaA, Darmstadt, Germany) in washing buffer After the first three cases were diagnosed in early (0.05 M Tris-HCL, pH 7.4, containing 150 mM NaCl and November 2012 (symptom onset September–November 1% Triton X-100), 30 min at 37 °C). Following this, the 2012), we sent a letter about H. tarandi myiasis in early wells were incubated (30 min, 37 °C) with test sam- December 2012 to inform primary care physicians in ples serially twofold diluted (1:50–1:6.400) in washing Finnmark, and the Departments of Paediatrics and buffer. Antibodies were detected using horseradish Ophthalmology at the University Hospital of North peroxidase (HRP)-conjugated rabbit anti-human IgG Norway (UNN), Trømsø. News media, such as NRK (DAKO, Glostrup, Denmark). The wells were washed x4 Sápmi (a Sami-language television broadcasting ser- between each incubation step. O-phenylenediamine vice for Norway, Finland and Sweden), promoted infor- (OPD, Dako) served as substrate. Colour development mation about the disease in December 2012. Other was stopped (1M H2SO4, after 30 min) and read as news media in Norway, Finland and Sweden also OD at 492 nm (OD492). The positive control used was informed the public in 2013, and authors of this paper serum from a 10-year-old child who had had a H. tarandi and others described the condition at medical meet- larva removed from an eye [16] (collected in December ings (Norway and Sweden) and reindeer husbandry after the summer of infestation). The negative control conferences (Norway and Finland). One of the adult used was serum from a 50-year-old adult with no his- cases, who visited Finnmark to hunt in August 2012, tory of H. tarandi infestation. The controls were run in was from a county in southern Norway where there are every plate. Each OD492-reading was expressed as an no reindeer (symptom onset September 2012, sought ELISA percentage relative to the 1/50-dilution reading medical attention after receiving information via for the positive (100%) and the negative (0%) control media). Similarly, two children in Finnmark, with myia- [19]. Identification of seropositives was by comparison sis symptom onset in September and November 2011, with the corresponding negative-control dilution series respectively, received information via media, and were in the same plate. Five additional sera from adults with shown to be seropositive and diagnosed more than a no history of H. tarandi myiasis were assayed, and the year after symptom onset. dilution curves (1:50–1:6.400) for all were practically identical to the negative control curve. Each of the neg- Laboratory testing ative control dilutions gave an ELISA percentage within Serum was assayed (ELISA) for antibodies (IgG) the range 5 to minus 5 and followed the negative con- against Hypodermin C (HyC, a collagenolytic enzyme trol graph (Figure 1). secreted by Hypoderma spp. larvae during migration in the host), essentially as described for sera from rein- Seropositivity or seronegativity was identified by com- deer [18]. Briefly, 96-well microtitre plate wells (Nunc parison with the dilution curve for the negative control. PolySorp, Nunc, Roskilde, Denmark) were coated (0.5 For test sera, if the 1/50-dilution ELISA percentage was µg/ml of HyC in 0.1 M sodium carbonate buffer, pH 9.6, in the 10–30% range, the serum was considered sus- 1 hour at 37 °C) and blocked (5% skimmed milk powder pect, and seropositivity was confirmed or disproved 2 www.eurosurveillance.org Figure 3 one dose of ivermectin [15]. One child no longer had Month of symptom onset for myiasis cases caused by symptoms on presentation and received no treatment. Hypoderma tarandi, Norway, 2011–2016 (n = 35) Of the 39 cases, 17 were infested in 2012, 15 of the 17 in Finnmark. Aside from the myiasis symptoms, all cases 10 presented with good general health. Table 1 summarises the clinical characteristics. Figure 8 3 shows the time of symptom onset for 35 of the 39 cases. r 6 e b In 35 of the 39 cases, seropositivity was confirmed by m the serum collected at the first medical evaluation. In Nu 4 four cases, the serology result for the first serum sam- ple (collected in August in one case, in October in three cases) was suspect, and seropositivity was confirmed 2 by a new sample collected ≥ 2 weeks after the first. Another three cases had symptoms during autumn/ 0 winter, and serum collected at the first medical evalu- July ation (in February, May and June, respectively) con- August October firmed seropositivity.