Unexpected intracranial location of a Cephenemyia stimulator larva in a roe deer, Capreolus capreolus, revealed by computed tomography

  1. Luis E. Fidalgo
  2. Ana M. López-Beceiro
  3. Carlos Martínez-Carrasco
  4. Noelia Caparrós-Fontarosa
  5. Antonio Sánchez
  6. Mónica Vila
  7. Daniel Barreiro
  8. Mathieu Sarasa
  9. Jesús M. Pérez
Journal:
Galemys: Boletín informativo de la Sociedad Española para la conservación y estudio de los mamíferos

ISSN: 1137-8700

Year of publication: 2021

Volume: 33

Volume: 1

Pages: 13-19

Type: Article

DOI: 10.7325/GALEMYS.2021.A2 DIALNET GOOGLE SCHOLAR lock_openDialnet editor

More publications in: Galemys: Boletín informativo de la Sociedad Española para la conservación y estudio de los mamíferos

Abstract

In this study we describe the finding of a Cephenemyia stimulator larva in the brain of a roe deer (Capreolus capreolus) after performing a computed tomography (CT) scan of its head. Despite this anatomical location of oestrid larvae could be relatively frequent in other genera, such as Oestrus, to our knowledge, this is the first reported case involving the genus Cephenemyia. Concretely, a second-instar C. stimulator larva was found in the basis of the cranium. The location of a macroscopic hemorrhagic lesion involving the brain parenchyma peripheral to the location of the larva suggests that tissue colonization occurred before the animal was hunted. Since no detectable alterations or damage to the cranial bones were observed, we suggest a possible larval migration route drilling the skull bones. Finally, we propose the use of the term “neuromyiasis” to be referred to the invasion of the central nervous system by dipteran larvae, particularly oestrids.

Bibliographic References

  • Arias M.S., Pajares G., Díez-Baños N., Pérez-Creo A., Prieto A., Díez-Baños P. & Morrondo P. 2016. Cephenemyiosis, an emergent myiasis in roe deer (Capreolus capreolus) from northwestern Spain. Parasitology Research, 115: 4605-4610. DOI: 10.1007/s00436-016-5251-7
  • Arias M.S., Pajares G., Paz-Silva A., Díez-Baños N., Suárez J.L., Díez-Baños P., Sánchez-Andrade R. & Morrondo P. 2014. Antigen characterization from second instars of oestrid bot flies for the detection of anti-Cephenemyia stimulator antibodies by ELISA in roe deer (Capreolus capreolus). Medical and Veterinary Entomology, 28 Suppl. 1: 83-89. DOI: 10.1111/ mve.12080
  • Bernard J. & Biesemans W. 1975. A propos des oestrides parasites du cheuvreuil en Belgique. Bulletin Annuelle de la Societé Royale Belge d’Entomologie, 111: 71-95.
  • Blickle R.L. 1956. Notes on the life history of Cephenomyia phobifer Clark (Diptera). Entomological News, 67: 13-14.
  • Brooks J.W. 2016. Postmorten changes in animal carcasses and estimation of the postmortem interval. Veterinary Pathology, 53: 929-940. DOI: 10.1177/0300985816629720
  • Calero-Bernal R. & Habela M.A. 2013. First report of Cephenemyia stimulator (Diptera, Oestridae) parasitizing roe deer (Capreolus capreolus) in Extremadura (Spain). Galemys, Spanish Journal of Mammalogy, 25: 29-34. DOI: 10.7325/Galemys.2013.A03
  • Colwell D.D. 2006. Life cycle strategies. Pp. 67-77. In: D.D. Colwell, M.J.R. Hall & P.J. Scholl (eds). The Oestrid Flies: Biology, Host-parasite Relationships, Impact and Management. CABI Publishing, Wallingford.
  • Colwell D.D., Hall M.J.R. & Scholl P.J. 2006. A synopsis of the biology, hosts, distribution, disease significance and management of the genera. Pp. 220-305. In: D.D. Colwell, M.J.R. Hall & P.J. Scholl (eds). The Oestrid Flies: Biology, Host-parasite Relationships, Impact and Management. CABI Publishing, Wallingford.
  • Cook J.R. Jr., Levesque D.C. & Nuehring L.P. 1985. Intracranial cuterebral myiasis causing acute lateralizing meningoencephalitis in two cats. Journal of the American Animal Hospital Association, 21: 279-284.
  • de la Fuente A.M. 2014. Análisis morfológico y molecular de especies de la subfamilia Oestrinae (Diptera, Oestridae). Master Thesis, University of Jaén, Spain, 69 pp.
  • Drozdz J. 1961. Cephenomyinae (Diptera: Oestridae) of cervids in Poland. Wiadomosci Parazytologiczne, 8: 381-382.
  • Dudzinski W. 1970. Studies on Cephenemyia stimulator (Clark) (Diptera, Oestridae), the parasite of European roe deer, Capreolus capreolus (L.). I. Biology. Acta Parasitologica Polonica, 18: 555-572.
  • Dunn L.H. 1934. Prevalence and importance of the tropical warble fly Dermatobia hominis Linn. in Panama. Journal of Parasitology, 20: 219-226.
  • Fidalgo L.E., López-Beceiro A.M., Vila-Pastor M., Martínez-Carrasco C., Barreiro-Vázquez J.D. & Pérez J.M. 2015. Use of computed tomography as a noninvasive method for diagnosing cephenemyiosis in roe deer (Capreolus capreolus). Medical and Veterinary Entomology, 29: 110-113. DOI: 10.1111/mve.12087
  • Glass E.N., Cornetta A.M., de Lahunta A., Center S.A. & Kent M. 1998. Clinical and clinicopathologic features in 11 cats with Cuterebra larvae myiasis in the central nervous system. Journal of Veterinary Internal Medicine, 12: 365-368. DOI: 10.1111/j.1939- 1676.1998.tb02136.x
  • Hadlow W.J., Ward J.K. & Krinsky W.L. 1977. Intracranial myiasis by Hypoderma bovis (Linnaeus) in a horse. Cornell Veterinary, 67: 272-281.
  • Jögisalu I. 2010. Roe deer nose botfly (Cephenemyia stimulator Clark, 1815) (Diptera: Oestridae) larvae and helminths impact on the European roe deer (Capreolus capreolus Linnaeus, 1758). Master Thesis. University of Tartu, Estonia, 48 pp.
  • Kalelioglu M., Aktürk G., Aktürk F. et al. 1989. Intracerebral myiasis from Hypoderma bovis larva in a child. Case report. Journal of Neurosurgery, 71: 929- 931. DOI: 10.3171/jns.1989.71.6.0929
  • Király I. & Egri B. 2004. Naso-pharyngeal bot infestation of the roe deer population of Tolna county. Magyar Allatorvosok Lapja, 126: 433-438.
  • Kutzer E. 2000. The treatment of oestrinosis and hypodermosis in red deer (Cervus elaphus hippelaphus) and roe deer (Capreolus c. capreolus) by means of ivermectin (Ivomec (R)). Berliner und Munchener Tierarztliche Wochenschrift, 113: 149-151.
  • López-Beceiro A.M., Martínez-Carrasco C., Pérez J.M., Colins B. & Fidalgo, L.E. 2015. Prevalencia de Cephenemyia stimulator en Galicia. 33èmes Rencontres du GEEFSM, Balme, Italy.
  • Maes S. & Boulard C. 2001. Deer myiasis in France. Pp. 181-186. En: M. Good et al. (eds.). Mange and myiasis of livestock. COST Action 833.
  • Nickel E.A., Danner G. & Stubbe I. 1986. Morphologische und metrische untersuchungen an larven I von Cephenemyia stimulator (Diptera, Oestridae). Angewandte Parasitologie, 27: 187-192.
  • Nilssen A.C., Isomursu M. & Oksanen A. 2008. The moose throat bot fly Cephenemyia ulrichii larvae (Diptera: Oestridae) found developing in roe deer (Capreolus capreolus) for the first time. Acta Veterinaria Scandinavica, 50: 14. DOI: 10.1186/1751-0147-50-14
  • Notario A. & Castresana L. 2001. Contribution to the knowledge of Cephenemyia stimulator Clark, 1815 (Diptera, Oestridae) in Spain. Folia Venatoria, 30-31: 325-326.
  • Olander H.J. 1967. The migration of Hypoderma lineatum in the brain of a horse. A case report and review. Veterinary Pathology, 4: 477-483.
  • Rivosecchi L., Zanin E., Cavallini C. & De Paoli C. 1978. Infestation of roe deer by Cephenemyia stimulator (Clark) (Diptera, Oestridae) in Trent province. Parassitologia, 20: 143-152.
  • Rossi M.A. & Zucoloto S. 1973. Fatal cerebral myiasis caused by the tropical warble fly, Dermatobia hominis. American Journal of Tropical Medicine and Hygiene, 22: 267-269. DOI: 10.4269/ajtmh.1973.22.267
  • Salaba O., Vadlejch J., Petrtyl M., Valek P., Kudrnacova M., Jankovska I., Bartak M. et al. 2013. Cephenemyia stimulator and Hypoderma diana infection of roe deer in the Czech Republic over an 8-year period. Parasitology Research, 112: 1661-1666. DOI: 10.1007/s00436-013-3322-6
  • Sartin E.A., Hendrix C.M., Dillehay D.L. & Nicholls B. 1986. Cerebral cuterebrosis in a dog. Journal of the American Veterinary Medicine Association, 189: 1338-1339.
  • Stéen M., Faber W.E. & Oksanen A. 1998. Disease and genetical investigations of Fennoscandian Cervids - a review. Alces, 34: 287-310.
  • Sugár L. 1974. The occurence of nasal throat bot flies (Oestridae) in wild ruminants in Hungary. Parasitologia Hungarica, 7: 181-189.
  • Truett G.E., Heeger P., Mynatt R.L., Truett A.A., Walker, J.A. & Warman M.L. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques: 29, 52-54. DOI: 10.2144/00291bm09
  • Ullrich H. 1938. Zur biologie der Rachenbremsen unseres einheimischer Wildes, Genus Cephenomyia Latreille und Genus Pharyngomyia Schiner. Verhandlungen VII Kongress Entomologie, III: 2149-2162.
  • Zhang D.X. & Hewitt G.M. 1997. Assessment of the universality and utility of a set of conserved mitochondrial COI primers in insects. Insect Molecular Biology, 6: 143-150. DOI: 10.1111/j.1365- 2583.1997.tb00082.x
  • Zumpt F. 1965. Myiasis in man and animals in the Old World. Butterworths, London. 267 pp.