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Black-Light Detects White-Nose Syndrome in Bats


Wing from dead eastern pipestrelle (Pipistrellus subflavus) bat shows points of orange-yellow fluorescence when exposed to UV light. From Turner and others, 2014, Figure 1E, page 569.

U.S. Geological Survey (USGS) scientists and collaborators discovered that long-wave ultraviolet (UV) light directed at the wings of bats with white-nose syndrome (WNS) produced points of distinctive orange-yellow fluorescence. The orange-yellow glow corresponds directly with microscopic skin lesions that define the current "gold standard" for diagnosing WNS. White-nose syndrome, a fungal disease caused by the fungus Pseudogymnoascus destructans (Pd), has killed millions of bats in North America since it was first diagnosed in New York in 2007. This application of UV light is the first screening method for WNS that can provide immediate 'on-site' information regarding WNS in bats.
WNS cannot be reliably identified with visual inspection and the only way to confirm presence of disease has been to euthanize the bats and send them to a laboratory for testing. In an effort to evaluate UV light as a non-fatal WNS screening method, 168 bats submitted for diagnostic testing from 2009 through spring 2012 had their wings examined with both UV light and microscopically to determine if they had WNS. Comparing the results of histology and UV light showed that 98.8-percent of bats with orange-yellow wing fluorescence (80) under UV light were confirmed positive for WNS microscopically, and 100-percent of the 88 bats that were fluorescent negative were also microscopically negative. Ultraviolet light was then used to target areas of fluorescence for biopsy and these 4mm samples contained microscopic erosions diagnostic for WNS.

Wing biopsies guided by UV fluorescence were then used in the field to evaluate WNS status in 62 bats during capture-and-release as they were leaving hibernacula in the Czech Republic during 2012. Of 22 biopsies that were taken from points of fluorescence on the wing, 95.5-percent were also microscopically positive for WNS. The 40 biopsies from non-fluorescent areas of wing were all negative for WNS.

Combining research from two continents demonstrates that this UV screening tool for WNS has broad geographic and species applicability with great reliability and minimal harm to bats. The use of UV fluorescence will help wildlife managers and researchers more quickly track the spread of this disease with an 'on-site' screening tool and it will be particularly helpful for use in populations of endangered bats that are federally protected. This WNS screening tool can also provide a way to look at the dynamics and intensity of infection over time in live bats and could be used to evaluate the potential response of bats to medical treatment.

Funding for this work was provided by the USGS Wildlife: Terrestrial and Endangered Resources Program and the Contaminant Biology Program.

Reference
Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white-nose syndrome: Journal of Wildlife Diseases, 2014, v. 50, no. 3, p. 566-573, doi:10.7589/2014-03-058.

More Information
For more information contact Carol Meteyer, USGS Contaminant Biology Program
White-Nose Syndrome (WNS), USGS National Wildlife Health Center

This article was featured as an article in the USGS GeoHealth Newsletter, Vol. 11, No. 1, 2014
Abstract
Definitive diagnosis of the bat disease white-nose syndrome (WNS) requires histologic analysis to identify the cutaneous erosions caused by the fungal pathogen Pseudogymnoascus [formerly Geomyces] destructans (Pd). Gross visual inspection does not distinguish bats with or without WNS, and no nonlethal, on-site, preliminary screening methods are available for WNS in bats. We demonstrate that long-wave ultraviolet (UV) light (wavelength 366–385 nm) elicits a distinct orange–yellow fluorescence in bat-wing membranes (skin) that corresponds directly with the fungal cupping erosions in histologic sections of skin that are the current gold standard for diagnosis of WNS. Between March 2009 and April 2012, wing membranes from 168 North American bat carcasses submitted to the US Geological Survey National Wildlife Health Center were examined with the use of both UV light and histology. Comparison of these techniques showed that 98.8% of the bats with foci of orange–yellow wing fluorescence (n = 80) were WNS-positive based on histologic diagnosis; bat wings that did not fluoresce under UV light (n = 88) were all histologically negative for WNS lesions. Punch biopsy samples as small as 3 mm taken from areas of wing with UV fluorescence were effective for identifying lesions diagnostic for WNS by histopathology. In a nonlethal biopsy-based study of 62 bats sampled (4-mm diameter) in hibernacula of the Czech Republic during 2012, 95.5% of fluorescent (n = 22) and 100% of nonfluorescent (n = 40) wing samples were confirmed by histopathology to be WNS positive and negative, respectively. This evidence supports use of long-wave UV light as a nonlethal and field-applicable method to screen bats for lesions indicative of WNS. Further, UV fluorescence can be used to guide targeted, nonlethal biopsy sampling for follow-up molecular testing, fungal culture analysis, and histologic confirmation of WNS.

INTRODUCTION
White-nose syndrome (WNS) is caused by the psychrophilic fungus Pseudogymnoascus[formerly Geomyces] destructans (Pd) (Lorch et al. 2011; Minnis and Lindner 2013). Mortality from Pd infection has been confirmed for six species of North American bats, including little brown myotis (Myotis lucifugus), northern myotis (Myotis septentrionalis), Indiana myotis (Myotis sodalis), Eastern small-footed myotis (Myotis leibii), tricolored bat (Perimyotis subflavus), and big brown bat (Eptesicus fuscus) (Turner et al. 2011). Pd has also been isolated from bats in Europe (Puechmaille et al. 2011a), with documentation of characteristic invasive lesions diagnostic for WNS (Pikula et al. 2012); unusual mortality has not been reported among European bats infected by Pd (Martínková et al. 2010; Puechmaille et al. 2011b; Sachanowicz et al. 2014).

White-nose syndrome is the first invasive cutaneous ascomycosis reported in mammals. Currently, histopathology is required to diagnose WNS (Meteyer et al. 2009). To collect an adequate sample of wing membrane (skin) to conduct a thorough histopathologic analysis, euthanasia is typically required. A rapid, field-applicable, and nonlethal technique to identify presumptive WNS would reduce the need to euthanize bats to obtain a diagnosis. Such a technique would additionally serve to enhance ability to expand diagnostic activities to assess the presence of disease in new species and additional regions of the world, and to screen bats rapidly to determine efficacy of potential mitigation strategies.

Since the historic observation in 1925 that typical fungal dermatophyte infections fluoresce under long-wave ultraviolet (UV) light, this technique has been used as aid for diagnosing keratinaceous fungal infections, including ringworm in domestic animals (Koeing and Schneckenburger 1994) and tinea capitis in humans (Margarot and Deveze 1925). Applying this technique to wing membranes of bats with suspect WNS, long-wave (366–385 nm) UV light was shown to be a rapid, reliable, and field-applicable diagnostic tool for preliminary identification of WNS in bat-wing membranes and an accurate guide for targeted, nonlethal biopsy sampling for subsequent histologic confirmation.


Figure 1.Long-wave ultraviolet (UV) and white-light illumination of lesions associated with white-nose syndrome. All photographs are from bats of the US; blurring in photos of live bats in C, D, and F is due to animal movement during long exposure. (A) Camera in cave, mounted on tripod directed at platform constructed to transilluminate bat wings with UV light (photo by Craig Stihler with permission). (B) Points of orange–yellow fluorescence (arrows) detected on a roosting Indiana myotis (Myotis sodalis) following surface illumination with a field-portable 9-watt 368-nm fluorescent UV light (photo by Tina Cheng with permission). (C) Wing from live little brown myotis (Myotis lucifugus) lit from above in cave with white light shows dispersed pattern of fungal growth. (D) White-light transillumination of wing from the live bat in C shows no obvious pattern of fungal infection or wing damage. (E) Wing from dead tricolored bat (Perimyotis subflavus) lit from above with hand-held 51 LED 385-nm UV flashlight shows points of orange–yellow fluorescence. (F) Transillumination of wing from live bat in C with the use of a field-portable 9-watt 368-nm fluorescent UV light. The pattern of orange–yellow fluorescence follows the distribution of surface fungal growth seen in C.


Figure 2.Ultraviolet fluorescence in wings of live bats (main images) and periodic acid–Schiff stained histologic sections (insets) of bat-wing skin with lesions diagnostic of white-nose syndrome; blurring in photos is due to animal movement during long exposure. (A) Black circle outlines an approximately 1-cm2 area of wing from a little brown myotis (Myotis lucifugus), Pennsylvania, USA with foci of fluorescence (white arrow). Inset shows the histologic section of this 1-cm2 area of tissue with densely packed fungal hyphae in cupping erosions (arrowheads). (B) Black circle outlines a 1-cm2 area of wing from a little brown myotis, Pennsylvania, with a single fluorescent dot (white arrow). Inset shows the only fungal cupping erosion (arrowhead) found in the histologic section from this labeled area of wing membrane. (C) Black circles outline foci of fluorescence on the wing skin of a greater mouse-eared myotis (M. myotis) from the Czech Republic (white arrow). Inset (scale bar  =  50 µm) shows the histologic section from a 4-mm biopsy sample taken from an area of fluorescence with densely packed fungal hyphae in cupping erosion (arrowhead).


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BatsRule!: Black-Light Detects White-Nose Syndrome in Bats
Black-Light Detects White-Nose Syndrome in Bats
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