Advertisement

Correlation between number of human cases of myiasis caused by the reindeer warble fly (Hypoderma tarandi) and weather conditions during summer in northern Scandinavia

  • Kjetil ÅsbakkEmail author
  • Jörgen Landehag
  • Andreas Skogen
  • Arne C. Nilssen
Original Paper
  • 32 Downloads

Abstract

The reindeer warble fly (Hypoderma tarandi) causes myiasis in reindeer and caribou (Rangifer tarandus and subspecies) and aberrant hosts such as humans. Of 22 human cases reported 1982–2016, 16 were children and 18 were residents in or visited northern parts of Norway or Sweden. Of a series of 39 new human cases in Norway 2011–2016 (reported 2017), 32 were children, 32 were resident in Finnmark (northernmost county of Norway), one was a visitor to Finnmark (most likely infested there), 17 were infested in 2012 and 10 in 2013. There are to our knowledge no human cases reported from Finland, although the H. tarandi infestation level in reindeer is high in the reindeer husbandry area of the country and many people live there. Consequently, the differences in geographical distribution and in distribution between children and adults, and between years, relative to where Rangifer and H. tarandi live, strongly indicate the presence of important identifiable drivers affecting the number and distribution. Meteorological data for June–August 2011–2016 from five meteorological stations in Finnmark applied in statistical analyses demonstrated that low proportion of days suitable for H. tarandi flying in July–August, combined with low proportion of days with rain in August, resulted in high number of cases in the particularly cold summer 2012. In contrast, in the particularly warm summer 2013, high proportion of days suitable for H. tarandi flying during July–August gave a high number of cases, and particularly high mean temperature in June tended in the same direction.

Keywords

Hypoderma tarandi Rangifer tarandus Reindeer Myiasis Human Children Temperature Rain 

Notes

Acknowledgements

Thanks to Frøydis Strand and Ørjan Garfjell (UiT The Arctic University of Norway) for figure preparation, and to John-André Henden (UiT) for input related to meteorological data information.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Ågren E, Chirico J (2005) Reindeer warble fly larvae (Hypoderma tarandi) in a moose (Alces alces) in Sweden. Acta Vet Scand 46:101–103Google Scholar
  2. Anderson JR, Nilssen AC (1996) Trapping oestrid parasites of reindeer: The response of Cephenemyia trompe and Hypoderma tarandi to baited traps. Med Vet Entomol 10:337–346CrossRefGoogle Scholar
  3. Anisimov OA et al. (2007) Polar regions (Arctic and Antarctic). In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (Eds.) Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, pp. 653–685.Google Scholar
  4. Åsbakk K, Kumpula J, Oksanen A, Laaksonen S (2014) Infestation by Hypoderma tarandi in reindeer calves from northern Finland - prevalence and risk factors. Vet Parasitol 200:172–178CrossRefGoogle Scholar
  5. Bangsø J, Thøgersen KF, Nejsum P, Stensvold CR (2016) The first case of Hypoderma tarandi-associated human myiasis in Greenland. Ugeskr Laeger 178:V10150796Google Scholar
  6. Bergman AM (1919) Über die Oestriden des Renntieres (About the Oestrids of Reindeer). Zeitschrift für Infektionskrankheiten, Haustiere 20:65–116Google Scholar
  7. Chirico J, Stenkula S, Eriksson B, Gjötterberg M, Ingemansson S-O, Pehrson-Palmqvist G, Stenkula E (1987) Renkorm, en styngflugelarv, orsak till tre fall av human myiasis (Reindeer warble fly larvae causing three cases of human myiasis). Läkartidningen 84:2007–2008Google Scholar
  8. Colwell DD, Hall MJR, Scholl PJ (2006) The oestrid flies: biology, host-parasite relationships, impact and management. CABI Pub, Wallingford, UKCrossRefGoogle Scholar
  9. eKlima (2016) Norwegian Meteorological Institute’s weather- and climate data from historical data to real-time observations. https://met.no/Klimadata+fra+eKlima.9UFRvY1M.ips. Accessed 3 May 2017
  10. Faber TE, Hendrikx WML (2006) Oral myiasis in a child by the reindeer warble fly larva Hypoderma tarandi. Med Vet Entomol 20:345–346CrossRefGoogle Scholar
  11. Folstad I, Nilssen AC, Halvorsen O, Andersen J (1991) Parasite avoidance: the cause of post-calving migrations in Rangifer? Can J Zool 69:2423–2429CrossRefGoogle Scholar
  12. Gjötterberg M, Ingemansson SO (1988) Intraocular infestation by the reindeer warble fly larva: an unusual indication for acute vitrectomy. Br J Ophthalmol 72:420–426CrossRefGoogle Scholar
  13. Gryseels B, Mertens DAE, Mehl R (1991) An imported case of ophthalmomyiasis interna posterior in the Netherlands caused by a larva of the reindeer warble fly. J Infect Dis 163:931–932CrossRefGoogle Scholar
  14. Jansen JJ (1970) Hypodermatid larvae (Diptera: Hypodermatidae) from musk ox, Ovibus moschatus. Ent Ber Amst 30:222–224Google Scholar
  15. Kan B, Åsbakk K, Fossen K, Nilssen A, Panadero R, Otranto D (2013) Reindeer warble fly-associated human myiasis, Scandinavia. Emerg Infect Dis 19:830–832.  https://doi.org/10.3201/eid1905.130145 CrossRefGoogle Scholar
  16. Kan B, Åsen C, Åsbakk K, Jaenson TG (2010) Misstänkta lusägg i pojkes hår avslöjade farlig parasit (Suspected lice eggs in boy's hair revealed dangerous parasite). Läkartidningen 107:1694–1697Google Scholar
  17. Kan B, Otranto D, Fossen K, Åsbakk K (2012) Dermal swellings and ocular injury after exposure to reindeer. N Engl J Med 367:2456–2457CrossRefGoogle Scholar
  18. Karter AJ, Folstad I, Anderson JR (1992) Abiotic factors influencing embryonic development, egg hatching, and larval orientation in the reindeer warble fly, Hypoderma tarandi. Med Vet Entomol 6:355–362CrossRefGoogle Scholar
  19. Kearney MS, Nilssen AC, Lyslo A, Syrdalen P, Dannevig L (1991) Ophthalmomyiasis caused by the reindeer warble fly. J Clin Pathol 44:276–284CrossRefGoogle Scholar
  20. Lagacé-Wiens PRS, Dookeran R, Skinner S, Leicht R, Colwell DD, Galloway TD (2008) Human ophthalmomyiasis interna caused by Hypoderma tarandi, northern Canada. Emerg Infect Dis 14:64–66CrossRefGoogle Scholar
  21. Landbruksdirektoratet (2017) Fakta om reindrift. Forskjeller i flyttemønster (Facts about reindeer husbandry. Differences in migration routes). https://www.slf.dep.no/no/reindriften/fakta-om-reindrift/forskjeller-i-flyttemonster. Accessed 15 May 2017
  22. Landehag J, Skogen A, Åsbakk K, Kan B (2017) Human myiasis caused by the reindeer warble fly, Hypoderma tarandi, case series from Norway, 2011–2016. Euro Surveill.  https://doi.org/10.2807/1560-7917.ES.2017.22.29.30576 Google Scholar
  23. Mook R (1994) The climate way north. In: Møller JJ, Reymert PK, Steinlien Ø (eds) Earth Science. University of Tromsø, Trømsø museum, Tromsø, Norway, pp 17–25Google Scholar
  24. Nelson WA, Weintraub J (1972) Hypoderma lineatum (De Vill.) (Diptera: Oestridae): Invasion of the bovine skin by newly hatched larvae. J Parasitol 58:614–624CrossRefGoogle Scholar
  25. Nilssen AC (1997) Effect of temperature on pupal development and eclosion dates in the reindeer oestrids Hypoderma tarandi and Cephenemyia trompe (Diptera: Oestridae). Environ Entomol 26:296–306CrossRefGoogle Scholar
  26. Nilssen AC, Anderson JR (1995a) Flight capacity of the reindeer warble fly, Hypoderma tarandi (L), and the reindeer nose bot fly, Cephenemyia trompe (Modeer) (Diptera, Oestridae). Can J Zool-Revue Canadienne de Zoologie 73:1228–1238CrossRefGoogle Scholar
  27. Nilssen AC, Anderson JR (1995b) The mating sites of the reindeer nose bot fly: not a practical target for control. Rangifer 15:55–61CrossRefGoogle Scholar
  28. Nilssen AC, Gjershaug JO (1988) Reindeer warble fly larvae found in red deer. Rangifer 8:35–37CrossRefGoogle Scholar
  29. Nilssen AC, Haugerud RE (1994) The timing and departure rate of larvae of the warble fly Hypoderma (=Oedemagena) tarandi (L.) and the nose bot fly Cephenemyia trompe (Modeer) (Diptera: Oestridae) from reindeer. Rangifer 14:113–122CrossRefGoogle Scholar
  30. Nilssen AC, Haugerud RE (1995) Epizootiology of the reindeer nose bot fly, Cephenemyia trompe (Modeer) (Diptera, Oestridae), in Reindeer, Rangifer tarandus (L), in Norway. Can J Zool 73:1024–1036CrossRefGoogle Scholar
  31. Paine R (1994) Herds of the tundra: A portrait of Sami reindeer pastoralism. Smithsonian Institution Press, Washington and LondonGoogle Scholar
  32. Rukke BA, Cholidis S, Johnsen A, Ottesen P (2014) Confirming Hypoderma tarandi (Diptera: Oestridae) human ophthalmomyiasis by larval DNA barcoding. Acta Parasitol 59:301–304.  https://doi.org/10.2478/s11686-014-0242-2 CrossRefGoogle Scholar
  33. Samuelsson F, Nejsum P, Raundrup K, Hansen TVA, Kapel CMO (2013) Warble infestations by Hypoderma tarandi (Diptera; Oestridae) recorded for the first time in West Greenland muskoxen. Int J Parasitol: Parasites and Wildlife 2:214–216Google Scholar
  34. Sigurdarson S, Haugerud RE (2004) “Wild reindeer” in Iceland. In: Ulvevadet B, Klokov K, Eds. Family-based reindeer herding and hunting economies, and the status of management of wild reindeer/caribou populations. Tromsø: Centre for Sami Studies, University of Tromsø, 159-162.Google Scholar
  35. Skjenneberg S, Slagsvold L (1968) Reindriften og dens naturgrunnlag (The reindeer husbandry and its natural resource base). Universitetsforlaget, Oslo/Bergen/TromsøGoogle Scholar
  36. Syrdalen P, Nitter T, Mehl R (1982) Ophthalmomyiasis interna posterior: report of case caused by the reindeer warble fly larva and review of previous reported cases. Brit J Ophthalmol 66:589–593CrossRefGoogle Scholar
  37. Syrdalen P, Stenkula S (1987) Ophthalmomyiasis interna posterior. Graefes Arch Clin Exp Ophthalmol 225:103–106CrossRefGoogle Scholar
  38. Tyler NJC et al (2007) Saami reindeer pastoralism under climate change: Applying a generalized framework for vulnerability studies to a sub-arctic social-ecological system. Global Environ Chang 17:191–206.  https://doi.org/10.1016/j.gloenvcha.2006.06.001 CrossRefGoogle Scholar
  39. Weintraub J (1961) Inducing mating and oviposition of the warble flies Hypoderma bovis (L.) and H. lineatum (De Vill.) (Diptera: Oestridae) in captivity. Can Entomol 149-156  https://doi.org/10.4039/Ent93149-2 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Arctic and Marine BiologyUiT – The Arctic University of NorwayTromsøNorway
  2. 2.Department of PaediatricsFinnmark Hospital TrustHammerfestNorway
  3. 3.UiT – The Arctic University of NorwayTromsøNorway

Personalised recommendations