Pathology Case of the Month - Little brown and northern long-eared bats

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Case History: Three little brown bats (Myotis lucifugus) and two northern long-eared bats (Myotis septentrionalis) were found dead at the entrance of an underground mine in St. Louis, Minnesota in February 2016.

The mine is used as a hibernaculum, and fewer bats had been observed in some areas. In 2016 and in previous years, bats had been reported to emerge early from hibernation and succumb to the cold.

Gross Findings: Two of the three little brown bats and one of the northern long-eared bats exhibited on their patagium, in variable intensity and distribution, areas of light brown pallor ranging from 1 mm to 2 cm in diameter (Fig. 1A). In some bats, the patagium was brittle. Diffuse or pinpoint orange fluorescence was found on all bats (Fig. 1B).

A bat with wings out-stretched and a bats wing under UV light appears blue with orange fluorescence.

Figure 1. Little brown bat (Myotis lucifugus) from an experimental infection trial with similar gross lesions as observed in this case. (A) Variably sized areas of depigmentation are widely distributed on the patagium. (B) Under UV light, large areas of the patagium fluoresce orange.

Histopathological Findings: Multifocally, there are numerous variably-sized cup-shaped epidermal erosions and ulcers which are filled with strongly PAS-positive, parallel walled, up to 3 µm wide, occasionally septate and branching fungal hyphae (Fig. 2A, 2B, 2D). Fungal hyphae often invade hair follicles (Fig. 2C). Small numbers of crescent shaped, 2.5 x 6 µm conidia with a basophilic centrum are present (Fig. 2D).

Photomicrographs from a wing roll of a little brown bat showing structures in purple with arrows pointing to features.

Figure 2. Photomicrographs from a wing roll of a little brown bat (Myotis lucifugus). PAS. (A) At low magnification, PAS-positive foci are easily detectable. (B) Multifocal cup-shaped ulcers (thick arrow) of the epidermis are scattered over the wing membrane surface. Inflammatory response is lacking. (C) Fungal hyphae are infiltrating the hair follicles (thin arrow). (D) Curved arthroconidia (asterisk) with a basophilic centrum are typical for P. destructans.

Morphologic Diagnosis/es: Epidermal erosion and ulceration, moderate, subacute to chronic, multifocal with intralesional fungal hyphae consistent with Pseudogymnoascus destructans

Disease: White-nose syndrome (WNS)

Etiology: Pseudogymnoascus destructans (Pd)

Gross findings: Bats are often found in winter or early spring with a delicate or thick white film covering the muzzle, ears, and wings, though this is often not apparent at the time of necropsy. Wing lesions typical of WNS consist of 1-3 mm diameter white foci with pinpoint black centers, variably sized areas of depigmentation, tearing, and/or desiccation of the patagium.

Diagnosis: Characteristically, infected skin fluoresces pale orange under UV light. Confirmation of WNS requires typical histological lesions with simultaneous verification of the presence of Pd by fungal culture or molecular techniques (PCR). Case definitions for WNS are available from the interagency White-nose Syndrome Response Team.

Distribution: After being introduced in North America in 2006 near Albany, New York, white-nose syndrome has spread leading to major mortality events among several species of cave-hibernating bats (view the WNS occurrence map). Pseudogymnoascus destructans is reported in Europe and Asia, where lesions consistent with WNS are also found, but the fungus is thought to have established a host-pathogen equilibrium without being associated with significant die-offs of bats in Europe and Asia.

Host range: Nearly all hibernating bats can be infected, but different susceptibilities are observed. Highly susceptible species include the little brown bat (Myotis lucifugus), the tri-colored bat (Perimyotis subflavus), and the northern long-eared bat (Myotis septentrionalis).

Transmission: Pseudogymnoascus destructans is a psychrophilic fungus and grows in caves or mines, which insectivorous bats use as hibernacula as a winter survival strategy. Such hibernacula constitute an environmental reservoir, where Pd can persist through summer and can infect bats the following season. In turn, infected bats carry the fungus and distribute Pd within these underground sites. It is also possible for Pd spores to contaminate clothing and equipment used at these locations.

Pathogenesis: Pseudogymnoascus destructans invades the skin surface of bats during hibernation, leading to altered behaviors, physiological disruption, and finally death. Infected hibernating bats exhibit energy-intensive behavior such as more frequent arousals from torpor or emerging early from hibernation, when insect prey is scarce. Damaged skin barriers lead to other systemic abnormalities including increased loss of water, dehydration, acidosis, and/or hyperkalemia.

Public health concerns: None known.

Wildlife population impacts: White-nose syndrome is known to have caused significant declines in several bat species of North America, with local extirpation of susceptible populations and some species at risk for extinction.

Management: Management of WNS is difficult, since P. destructans can persist in underground environments at bat hibernacula. This leads to a seasonal disease transmission dynamic and complicates effort to control the disease. Slowing down the rates of transmission and mortality in bats in subsequent years could theoretically be achieved by reducing the amount of Pd in the environment in years following the first detection. Decontamination of clothing and equipment used inside caves and limiting access to where bats roost are advised to reduce the potential for human-assisted dispersal and to improve bat survival. Research is underway to investigate potential treatment options, including vaccination.

References:

Ballmann AE, Torkelson MR, Bohuski EA, Russell RE, Blehert DS. 2017. Dispersal hazards of Pseudogymnoascus destructans by bats and human activity at hibernacula in summer. J Wildlife Dis 53(4):725-735.

Farina LL, Lankton JS. 2018. Chiroptera. In: Pathology of Wildlife and Zoo Animals, Terio KA, McAloose D, St. Leger J, editors. Academic Press, pp. 607-633

Turner GG, Meteyer CU, Barton H, Gumbs JF, Reeder DM, Overton B, Bandouchova H, Bartonicka T, Martinkova N, Pikcula J, Zukal J, Blehert DS. 2014. Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white-nose syndrome. J Wildlife Dis 50(3):566-573

Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, Shearn-Bochsler V, Thomas NJ, Gargas A, Behr MJ. 2009. Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Invest 21:411-414

Verant ML, Bohuski EA, Richgels KLD, Olival KJ, Epstein JH, Blehert DS. 2018. Determinants of Pseudogymnoascus destructans within bat hibernacula: Implications for surveillance and management of white-nose syndrome. J Appl Ecol. 55:820–829.

Zukal J, Bandouchova H, Brichta J, Cmokova A, Jaron KS, Kolarik M, Kovacova V, Kubátová A, Nováková A, Orlov O and Pikula J. 2016. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Reports 6:19829-19842

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