Skin Lesions in European Hibernating Bats Associated with Geomyces destructans, the Etiologic Agent of White-Nose Syndrome

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Abstract

White-nose syndrome (WNS) has claimed the lives of millions of hibernating insectivorous bats in North America. Its etiologic agent, the psychrophilic fungus Geomyces destructans, causes skin lesions that are the hallmark of the disease. The fungal infection is characterized by a white powdery growth on muzzle, ears and wing membranes. While WNS may threaten some species of North American bats with regional extinction, infection in hibernating bats in Europe seems not to be associated with significant mortality. We performed histopathological investigations on biopsy samples of 11 hibernating European bats, originating from 4 different countries, colonized by G. destructans. One additional bat was euthanized to allow thorough examination of multiple strips of its wing membranes. Molecular analyses of touch imprints, swabs and skin samples confirmed that fungal structures were G. destructans. Additionally, archived field notes on hibernacula monitoring data in the Harz Mountains, Germany, over an 11-year period (2000-2011) revealed multiple capture-recapture events of 8 banded bats repeatedly displaying characteristic fungal colonization. Skin lesions of G. destructans-affected hibernating European bats are intriguingly similar to the epidermal lesions described in North American bats. Nevertheless, deep invasion of fungal hyphae into the dermal connective tissue with resulting ulceration like in North American bats was not observed in the biopsy samples of European bats; all lesions found were restricted to the layers of the epidermis and its adnexae. Two bats had mild epidermal cupping erosions as described for North American bats. The possible mechanisms for any difference in outcomes of G. destructans infection in European and North American bats still need to be elucidated. © 2013 Wibbelt et al.

Figures

  • Table 1. Details on bat samples regarding bat species, origin, collection date, sampled tissue, histology result and accession numbers for ITS gene sequences.
  • Figure 1. Emaciated Myotis myotis from a hibernaculum in France covered by Geomyces destructans. 1A: Old laceration of the left wing identified on the day of collection. 1B: Bat with improved body condition after some weeks of rehabilitation. 1C+D: Wing membranes after cleaning with notable depigmentation. doi:10.1371/journal.pone.0074105.g001
  • Figure 2. Biopsy of uropatagial membrane of Myotis myotis with acute inflammatory response against Geomyces destructans. 2A (sample HU 1): Dissection microscope image of punch biopsy with distinct circular lesions (arrows), where G. destructans had sloughed off during preparation. 2B: Histological cross section of 2A with multiple well-demarcated intraepidermal microabscesses (arrows). Hematoxylin-eosin staining. Inset: Hyphae of G. destructans invading the microabscesses (arrow heads). PAS staining. doi:10.1371/journal.pone.0074105.g002
  • Figure 3. Geomyces destructans colonization of superficial epidermis occasionally associated with epidermal pustules. 3A: A representative wing biopsy punch (GE 7). 3B (wing punch GE 1): Small epidermal cluster of G. destructans hyphae (encircled). 3C (sample NL 1): Wing membrane of euthanized bat with cupping erosion and densely packed hyphae of G. destructans restricted to the epidermis. 3D (sample NL 1): Fungal hyphae (arrows) invasion into intraepidermal pustules (star). PAS staining. doi:10.1371/journal.pone.0074105.g003
  • Figure 4. Skin of the muzzle of a Geomyces destructans infected Myotis daubentonii (sample NL 1). 4A: Multiple hair follicles with intraluminal colonization of G. destructans hyphae. 4B: Wall of a hair follicle replaced by marked growth of G. destructans hyphae. 4C+D: Cutaneous epithelium of one nare severely colonized by G. destructans with mild localized suppurative inflammation limited to the epithelial layer. PAS staining. doi:10.1371/journal.pone.0074105.g004
  • Table 2. Retrospective data on capture/recapture of banded Myotis myotis with visible fungal colonization.
  • Figure 5. Development of Geomyces destructans colonization over 3 weeks’ time on naturally infected bats. 5A+B: Two banded Myotis myotis with mild facial fungal patches on 5th February 2011. 5C: Recapture of these bats on 26th February 2011 with marked fungal colonization over most of the glabrous skin parts and the snout. doi:10.1371/journal.pone.0074105.g005

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Wibbelt, G., Puechmaille, S. J., Ohlendorf, B., Mühldorfer, K., Bosch, T., Görföl, T., … Forget, F. (2013). Skin Lesions in European Hibernating Bats Associated with Geomyces destructans, the Etiologic Agent of White-Nose Syndrome. PLoS ONE, 8(9). https://doi.org/10.1371/journal.pone.0074105

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