Immunogenetics and cellular immunology of bacterial infectious disease

Boshoven, M.

Laumen, L.

Mulder, M.

Pronk, M.

Roelfsema, J.

Verheijden, M.

Visser, L.G.

Wegdam-Blans, M.

Leiden University Scholary Publications

Migratory myiasis in a European traveller due to Hypoderma larvaeVerheijden, M.; Laumen, L.; Mulder, M.; Boshoven, M.; Roelfsema, J.; Pronk, M.; ... ; Wegdam-Blans, M.CitationVerheijden, M., Laumen, L., Mulder, M., Boshoven, M., Roelfsema, J., Pronk, M., … Wegdam-Blans, M. (2022). Migratory myiasis in a European traveller due to Hypoderma larvae. JournalOf Travel Medicine. doi:10.1093/jtm/taac023 Version: Publisher's VersionLicense: Creative Commons CC BY 4.0 licenseDownloaded from: https://hdl.handle.net/1887/3303602 Note: To cite this publication please use the final published version (if applicable).© The Author(s) 2022. Published by Oxford University Press on behalf of International Society of Travel Medicine.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permitsunrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.Journal of Travel Medicine, 2022, 1–3https://doi.org/10.1093/jtm/taac023Clinical PearlsClinical PearlsMigratory myiasis in a European traveller dueto Hypoderma larvaeMichelle Verheijden, MD1,*, Luc Laumen, MD2,3, Marlies Mulder, MD4,5,Michel Boshoven, BSc4, Jeroen Roelfsema, PhD6, Marjolijn Pronk, MD7,Leo G. Visser, MD, PhD8, and Marjolijn Wegdam-Blans, MD, PhD41Department of Family Medicine, University of Maastricht, Maastricht, P.O. Box 616, 6200 MD Maastricht, TheNetherlands, 2Department of Dermatology, Maastricht University Medical Centre+, Maastricht, P.O. Box 616, 6200 MDMaastricht, The Netherlands, 3Department of Dermatology, Catharina Ziekenhuis, Eindhoven, P.O. Box 1350, 5602 ZAEindhoven, The Netherlands, 4Department of Medical Microbiology, Stichting PAMM, Veldhoven, 5504 DL Veldhoven, TheNetherlands, 5Department of Medical Microbiology, Maastricht University Medical Centre+, P.O. Box 5800, 6202 AZMaastricht, The Netherlands, 6National Institute for Public Health and the Environment (RIVM), Centre for InfectiousDisease Control, P.O. Box 1, 3720 BA Bilthoven, The Netherlands, 7Department of Internal Medicine, CatharinaZiekenhuis, P.O. Box 1350, 5602 ZA Eindhoven, The Netherlands and 8Department of Infectious Diseases, LeidenUniversity Medical Center, P.O. Box 9600, 2300 RC Leiden, The Netherlands*To whom correspondence should be addressed. Michelle J.H. Verheijden, Department of Family Medicine, Care and Public Health Research Institute(CAPHRI), School of Health Professions Educations (SHE), Maastricht University, Maastricht, P.O. Box 616, 6200 MD Maastricht, The Netherlands.Tel: + (31) 625053180. Email: m.verheijden@.maastrichtuniversity.nl.Submitted 22 December 2021; Revised 3 February 2022; Editorial Decision 6 February 2022; Accepted 6 February 2022A 28-year old otherwise healthy Dutch male presented at theemergency department with fatigue, joint complaints and migra-tory subcutaneous swellings on back, and legs. Moreover, hereported a parasite coming out of the epidermis of his back. Threemonths previously, he returned from travelling across SouthAmerica, South and Southeastern Asia and the Caucasus.At presentation, routine haematological and biochemicalinvestigations were normal, except for high levels of eosinophils(>10∗109/l) and an increased erythrocyte sedimentation rate(highest 76 mm/h). Microscopic examination of faces, routinePCRs and serological tests for ascariasis, fascioliasis, filariasis,paragonimiasis, schistosomiasis, strongyloidiasis, toxocariasisand trichinellosis were negative.Due to migratory swellings, a Gnathostoma spinigerum infes-tation was suspected and he was treated with albendazole.However, after 2 weeks of treatment, two thick nodules on thepatient’s right flank appeared. A white, oval-shaped, 7 mm para-site was surgically removed from one of the nodules (Figure 1A).In addition, serological tests for gnathostomiasis returned neg-ative. Therefore, this diagnosis was rejected and albendazoletreatment was ceased.Finally, molecular examination revealed the diagnosis: H.sinense (S1). Further sequencing of mitochondrial targets,however, revealed a large number of mismatches between thespecimen and the closest matching Hypderma sp, H. sinense andH. lineatum (S2). Therefore, the specimen could not be assignedto a particular species. Also, the patients’ extensive travel history(across 24 countries) did not help to distinguish between H.sinense and H. lineatum, since H. lineatum is endemic in largeparts of Asia and northern Mexico, and H. sinense is endemicto Western Himalaya. The patient was treated with ivermectin(12 mg orally once time daily) in three courses of 3 days withseveral weeks in between. The patients’ condition improved andhis blood screen returned to normal.Hypoderma sp. (warble flies), belonging to the Oestridae fam-ily, usually cause subcutaneous myiasis in cattle and are generallyfound in the Northern Hemisphere. Hypoderma sinense was firstdiscovered by Pleske in 1926, but soon synonymized with H.lineatum. The adult flies look very similar and their life cycleis identical (Figure 1B), although they differ in the host theyparasitize.1,2The diagnostic process was challenging due to the large num-ber of possible parasitic infestations characterized by migratory(sub)cutaneous swelling(s). These infestations include fasciolia-sis, gnathostomiasis, loaiasis, dirofilariasis, mansolelliasis, parag-onimiasis and toxocariasis. However, fascioliasis, paragonimiasisDownloaded from https://academic.oup.com/jtm/advance-article/doi/10.1093/jtm/taac023/6534727 by Universiteit Leiden / LUMC user on 21 July 20222 Journal of Travel MedicineFigure 1. (a) Surgically removed larva removed from a subcutaneous swelling in the patient’s abdomen. (b) Life cycle of the Hypodermasinense/Hypoderma lineatum parasite. The adult flies look very similar and their life cycle is identical, but they differ in the host they parasitize:yaks (H. sinense) or (domesticated) cattle (H. lineatum)and mansolelliasis are characterized by nodular subcutaneousswelling; loaiasis is only seen at the African continent and G.spinigerum larvae cannot mature in humans larger than 3 mm.Sparganosis and dirofilariasis could also be added as possible dif-ferential diagnosis typically presenting with subcutaneous migra-tory swelling(s). However, these infestations were not included inour initial possible differential diagnosis.Case reports of human infestations with Hypoderma sp., suchas H. lineatum and H. sinense are rare, especially in Europe.In 2014, a case report was published, describing a farmer, whohad never travelled outside Italy with an infestation by H.lineatum, confirmed by molecular analysis.3 Puente et al. (2010)reported on a European with an H. sinense infestation, presentingwith abdominal pain and, inflammation of the right groin andtesticular region after traveling to northern India.4 Furthermore,a comment was published (2012) about an H. sinense infestationof a German tourist who had developed swellings and pain aftertraveling to Tibet.5Supplementary dataSupplementary data is available at JTMEDI online.AcknowledgementsWe would like to thank L. Wammes and L. van Lieshout fromthe parasitology laboratory at Leiden University Medical Centerand the Swiss Tropical and Public Health institute for performingDownloaded from https://academic.oup.com/jtm/advance-article/doi/10.1093/jtm/taac023/6534727 by Universiteit Leiden / LUMC user on 21 July 2022Journal of Travel Medicine 3parasitological serological tests. Also, we would like to thankthe Rijksinstituut voor Volksgezondheid en Milieu (RIVM) fortheir contribution in the diagnosis by performing DNA sequenceanalysis.FundingThe authors have declared no sources of funding.Conflict of interestThe authors declare that they have no conflict of interest.Patient consentWritten informed consent was obtained from the patient for thepublication of the case report.References1. McGraw TA, Turiansky GW. Cutaneous myiasis. J Am Acad Derma-tol 2008; 58:907–26. https://doi.org/10.1016/j.jaad.2008.03.014.2. Otranto D, Colwell DD, Pape T. Hypoderma sinense: solving acentury-old enigma. Med Vet Entomol 2005; 19:315–21. https://doi.org/10.1111/j.1365-2915.2005.00576.x.3. Rappelli P, Varcasia A, Vargiu A, Scala A. Case report: first reportof autochthonous human cutaneous myiasis caused by Hypodermalineatum in Europe. Am J Trop Med Hyg 2018; 99:618–9. https://doi.org/10.4269/ajtmh.18-0100.4. Puente S, Otranto D, Panadero R et al. First diagnosis of an importedhuman myiasis caused by Hypoderma sinense (Diptera: Oestridae),detected in a European traveler returning from India. J Travel Med2010; 17:419–23. https://doi.org/10.1111/j.1708-8305.2010.00464.x.5. Biodiversity Science. A Very Unpleasant Souvenir. Accessed at https://dna-barcoding.blogspot.com/2012/08/a-very-unpleasant-souvenir-dna.html, January 16, 2021.Downloaded from https://academic.oup.com/jtm/advance-article/doi/10.1093/jtm/taac023/6534727 by Universiteit Leiden / LUMC user on 21 July 2022

Migratory myiasis in a European traveller due to Hypoderma larvae

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Migratory myiasis in a European traveller due to Hypoderma larvae

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