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Volume 19, Number 9—September 2013

Letter

Alaria alata Infection in European Mink

Suggested citation for this article

To the Editor. Alariosis is a reemerging zoonotic disease caused by infection with larval stages of trematodes of the genus Alaria. The trematodes are found in wildlife that inhabit wetlands, and these animals may serve as possible reservoirs for these organisms that cause human infection (1). The main sources for human infection are suids and frogs (1). In humans, the clinical features of alariosis caused by infections with the North American species of Alaria vary from mild and asymptomatic to moderate with respiratory or cutaneous signs (2) or neuroretinitis (3), to severe-to-lethal anaphylactic shock caused by larva migrans (4,5). The genus Alaria has 7 species; only A. alata is found naturally in Europe (6), a species which has not thus far been shown to be responsible for human infections.

A. alata infection is common in its typical definitive host (red fox, Vulpes vulpes) and in certain paratenic hosts (wild boar, Sus scrofa) (1). However, the role of other paratenic hosts is poorly known. Among these, mustelids are reported to harbor mesocercariae of A. alata trematodes (7). The pathogenic effect of A. alata infection has been poorly studied, because most lesions described were in humans infected with other species of Alaria. Except for 2 experimental studies that described gross lesions produced by A. alata trematodes (6,8), to our knowledge, no data have been published concerning lesions produced by natural infection in nonhuman hosts. Our report provides a detailed description of the lesions, shown by microscopy, which suggests the pathogenic mechanisms.

One adult female European mink (Mustela lutreola) was found dead during standard surveillance operations in which box traps were used; this trapping was part of biodiversity and ecology studies in the central part of the Danube delta in Romania (45°08′N, 29°19′E) in March 2010. The corpse was deep-frozen and analyzed after 3 months in the laboratory. During necropsy, multiple, well-defined, whitish nodules were observed in most muscular and subcutaneous tissues (Figure, panel A), with no evident preferential localization. We collected samples from these tissues for artificial digestion (9,10) and histologic examination, using the routine paraffin-embedding protocol and the following staining methods: hematoxylin-eosin, Masson trichrome, and Gordon and Sweet.

Artificial digestion released parasites (6 larvae/5 gm tissue) with typical larval trematode structures (Figure, panel B). By microscopy, we observed that morphologic features of these larvae were consistent with A. alata mesocercariae (6). Histopathologic examination confirmed the presence of parasitic forms in muscle sections (Figure, panel C). The mesocercariae were located in the connective fibrous tissue of the perimysium or between the muscle fibers. The typical structure of muscle fibers was altered around the larvae, with inflammatory cell reactions, represented mainly by lymphocytes, macrophages, and plasma cells (Figure, panel D). In other areas, the inflammatory reaction around the parasite was minimal or absent (Figure, panel E). In certain histologic sections, the damaged muscular tissue was replaced by granulation tissue in various stages of development (Figure, panel F). The maturity of the granulation tissue differed substantially, depending on the muscular areas examined. Some lesions were found in adult connective tissue, formed by mature collagen scar fibers (type I collagen) and few inflammatory cells, whereas other lesions had reticulin fibers (type III collagen) with numerous inflammatory cells. The lesions of the subcutaneous connective tissue consisted of an inflammatory reaction (panniculitis). The inflammation was characterized by a low number of mononuclear leukocytes and fibrinous exudate and fibroplasia.

The polyphasic nature of muscle and subcutaneous lesions produced by A. alata infection in its paratenic host appears to be caused by mesocercarial migration. This view is sustained by the presence of mononuclear cells that it infiltrates and by the appearance of the granulomatous tissue in various stages of maturation, which leads to muscle and subcutaneous fibroplasia. The reparatory nature of the lesions suggests that the inflammation is probably the result of direct tissue damage rather than an immune reaction targeted toward the parasitic antigens. This assumption could explain the local absence of inflammatory reaction around the parasites. The lack of inflammation was previously observed also with A. americana infection of humans (4). The structure of all mesocercariae observed by microscopy suggested that they were alive and active before the mink carcass was frozen. Because no mesocercariae were surrounded by adult connective tissue or by granulomatous inflammation, together with the multiple presences of migratory routes, the continuous mobility of the parasites through the host’s tissues was strongly suggested.

Although data on the pathologic changes caused by Alaria spp. in general, and A. alata parasites in particular, are scarce, the migration pattern and the lesions seem to be dependent on the particular parasite and host species. The reparatory nature of the lesions suggests that the inflammation is the result of direct tissue damage rather than an immune reaction targeted toward the parasitic antigens.

Flaviu Tăbăran, Attila David SándorComments to Author , Mihai Marinov, Cornel Cătoi, and Andrei Daniel Mihalca
Author affiliations: University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, Cluj-Napoca, Romania (F. Tăbăran, A.D. Sándor, C. Cătoi, A.D. Mihalca); Danube Delta National Institute for Research and Development, Tulcea, Romania (M. Marinov)

Acknowledgment

The research was conducted with the support of Unitatea Executivă pentru Finanțarea Învățământului Superior, a Cercetării, Dezvoltării și Inovării grant PCE236/2011.

References

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  2. Kramer MH, Eberhard ML, Blankenberg TA. Respiratory symptoms and subcutaneous granuloma caused by mesocercariae: a case report. Am J Trop Med Hyg. 1996;55:4478 .PubMed
  3. McDonald HR, Kazacos KR, Schatz H, Johnson RN. Two cases of intraocular infection with Alaria mesocercaria (Trematoda). Am J Ophthalmol. 1994;117:44755 .PubMed
  4. Fernandes BJ, Cooper JD, Cullen JB, Freeman RS, Ritchie AC, Scott AA, Systemic infection with Alaria americana (Trematoda). Can Med Assoc J. 1976;115:11114 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1878919/.PubMed
  5. Freeman RS, Stuart PF, Cullen SJ, Ritchie AC, Mildon A, Fernandes BJ, Fatal human infection with mesocercariae of the trematode Alaria americana. Am J Trop Med Hyg. 1976;25:8037 .PubMed
  6. Skrjabin KI, editor. Trematodes of animals and man; essentials of trematodology, vol. XVIII. Jerusalem (Israel): Program for Scientific Translations; 1965. p. 327–43.
  7. Anisimova EI. Study on the European mink Mustela lutreola helminthocenoses in connection with the American mink M. vison expansion in the Belarus: story of the study and review of the results. Helminthologia. 2004;41:1936 http://www.saske.sk/pau/helminthologia/2004_4/Anisimova193.pdf.
  8. Odening K. The “Duncker’s muscle fluke” can be transmitted experimentally to monkeys [in German]. Monatsh Veterinarmed. 1961;16:3959.
  9. Gamble HR, Bessonov AS, Cuperlovic K, Gajadhar AA, van Knapen F, Noeckler K. International Commission on Trichinellosis: recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Vet Parasitol. 2000;93:39340. DOIPubMed
  10. Portier J, Jouet D, Ferté H, Gibout O, Heckmann A, Boireau P, New data in France on the trematode Alaria alata (Goeze, 1792) obtained during Trichinella inspections. Parasite. 2011;18:2715. DOIPubMed

Figure

Suggested citation for this article: Tăbăran F, Sándor AD, Marinov M, Cătoi C, Mihalca AD. Alaria alata infection in European mink [letter]. Emerg Infect Dis [Internet]. 2013 Sep [date cited]. http://dx.doi.org/10.3201/eid1909.130081

DOI: 10.3201/eid1909.130081

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Table of Contents – Volume 19, Number 9—September 2013

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Attila D. Sándor, Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Calea Mănăştur 3-5, RO-400372, Cluj, Romania

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