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Amphibian: A Case Definition and Diagnostic Criteria for Batrachochytrium salamandrivorans Chytridiomycosis

June 2016
Herpetological Review 47(2):207

Authors:

C. LeAnn White

United States Geological Survey

Maria Forzan

University of Wyoming

Allan Pessier

Washington State University

Matthew C Allender

University of Illinois, Urbana-Champaign

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Comparison of Bd and Bsal-type chytridiomycosis. Notophthalmus viridescens. Hematoxylin and eosin stain 1000×. Bd-type chytridiomycosis (A) is proliferative with epidermal hyperplasia and hyperkeratosis and numerous chytrid thalli in superficial keratinocytes (arrows). The keratinocytes are arranged in distinct layers with intact nuclei (N). In contrast, Bsal-type chytridiomycosis (B) has almost full-thickness necrosis of keratinocytes with myriad chytrid thalli (arrows) that frequently have internal septa (colonial thalli). Note the loss of distinct layers of keratinocytes. At the periphery of this area of necrosis, a remaining keratinocyte has two intracytoplasmic chytrid thalli that marginate the nucleus (circle).

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Herpetological Review 47(2), 2016

AMPHIBIAN AND REPTILE DISEASES 207

AMPHIBIAN AND REPTILE DISEASES

Herpetological Review, 2016, 47(2), 207–209.

Amphibian: A Case Denition and Diagnostic Criteria for

Batrachochytrium salamandrivorans Chytridiomycosis

A newly described chytrid fungus, Batrachochytrium sala-

mandrivorans (Bsal), has caused several die-offs in salaman-

ders in Europe (Martel et al. 2013; Cunningham et al. 2015).

This pathogen is similar to the species B. dendobatidis (Bd) that

has caused massive amphibian population declines globally. As

the United States is home to the world’s most diverse salaman-

der assemblage, the United States Fish and Wildlife Service has

sought to increase protection of native salamander populations

via an interim rule under the Lacey Act (18 USC 42- USFWS

2016). This rule, effective 28 January 2016, limits international

and interstate movement of 20 genera of salamanders. Concur-

rent with this work, a U.S. Bsal Task Force (Grant et al. 2016)

was formed to help prevent and manage cases that might oc-

cur in North America. The diagnostics committee of this Task

Force developed the following Bsal case definition to promote

standardized communication of results and consistent national

reporting of this invasive pathogen among multiple diagnostic

laboratories in order to provide reliable information to wildlife

managers.

Case definitions typically include field, gross, histopatholo-

gy, laboratory, and epidemiologic criteria for assigning an indi-

vidual to a specific disease or condition. The diagnostic criteria

including field signs, gross pathology and histopathology have

been established from Bsal cases in free-ranging salamanders

in Europe and North American species examined during exper-

imental infection trials (Martel et al. 2013; A. P. Pessier, unpubl.

data). As an emerging pathogen some aspects of Bsal ecology,

including variation in species susceptibility and field signs for

North American species, are unknown. The case definition,

therefore, errs on the side of specificity over sensitivity by re-

quiring both histopathologic and laboratory confirmation to be

considered a confirmed Bsal case. However, we also included

a category for reporting the presence of the Bsal fungus in the

absence of corroborating evidence of disease (i.e., histopathol-

ogy) since consistent reporting of this information will be use-

ful for examining pathogen spread in new geographic locations

and susceptibility in new host species.

The case definition presented here represents the current

knowledge of Bsal infection in amphibians and is intended to

provide background information on this new pathogen and the

clinical and histopathogical presentation of the disease. Criteria

for diagnoses are provided and should be used for determining

disease presence. However, it should be noted that since this

disease has not been found in free-ranging North American am-

phibian species, variation in its presentation for these new pop-

ulations is unknown, and the definitions proposed below may

evolve with geographical, environmental, and host expansion.

C. LEANN WHITE

USGS-National Wildlife Health Center, Madison, Wisconsin 53711, USA

MARÍA J. FORZÁN

Canadian Wildlife Health Cooperative, Atlantic Veterinary College,

University of Prince Edward Island, Charlottetown,

Prince Edward Island C1A4P3, Canada

ALLAN P. PESSIER

Institute for Conservation Research, San Diego Zoo Global,

San Diego, California 92112, USA

MATTHEW C. ALLENDER

Wildlife Epidemiology Lab, Department of Veterinary Clinical Medicine,

University of Illinois, Urbana, Illinois 61802, USA

JENNIFER R. BALLARD

US Fish and Wildlife Service, Wildlife Health Oce,

Natural Resource Program Center, National Wildlife Refuge System,

Fort Collins, Colorado 80525, USA

ALESSANDRO CATENAZZI

Department of Zoology, Southern Illinois University Carbondale,

Carbondale, Illinois 62901, USA

HEATHER FENTON

Southeastern Cooperative Wildlife Disease Study, College of

Veterinary Medicine, Department of Population Health,

University of Georgia, Athens, Georgia 30602, USA

AN MARTEL

FRANK PASMANS

Department of Pathology, Bacteriology and Avian Diseases,

Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium

DEBRA L. MILLER

Center for Wildlife Health, University of Tennessee, Knoxville,

Tennessee 37996, USA

ROBERT J. OSSIBOFF

Department of Population Medicine and Diagnostic Sciences,

Cornell University, Ithaca, New York 14853, USA

KATHERINE L. D. RICHGELS

USGS-National Wildlife Health Center, Madison, Wisconsin 53711, USA

University of Wisconsin-Madison, School of Veterinary Medicine,

Department of Pathobiological Sciences, Madison, Wisconsin 53706, USA

JACOB L. KERBY*

Department of Biology, University of South Dakota, Vermillion,

South Dakota 57069, USA

*Corresponding author; e-mail: Jacob.Kerby@usd.edu

Herpetological Review 47(2), 2016

208 AMPHIBIAN AND REPTILE DISEASES

CHytrid Fun gus in tHe order rHiZoPHydiaLes, genus

Batrachochytrium , sPeCies sal amandrivoran s

I. Individual, Place, and Time

Individual.—Post-metamorphic amphibians (especially

salamanders) are known to be susceptible. Although larval Fire

Salamanders (Salamandra salamandra) are not susceptible

(Van Rooij et al. 2015), larval susceptibility in other species is

unknown. There is increased index of suspicion for mortality

events involving multiple salamander species (and notably not

involving co-occurring frog species), or North American spe-

cies with laboratory confirmed susceptibility to Bsal chytrid-

iomycosis, specifically Notophthalmus viridescens (Eastern

Newt), Taricha granulosa (Rough-skinned Newt).

Place.—There are currently no specific restrictions for

where Bsal can occur.

Time.—There are currently no specific restrictions for when

Bsal can occur.

II. Diagnostic Description

Field observations.—A clinically compatible case includes

amphibians with skin ulcers and lethargy, leading to a typically

high mortality rate. Weak or erratic swimming may also occur.

Gross necropsy observations.—On post-mortem examina-

tion, clinically compatible cases may present with subtle to

severe skin ulcers or erosions; some cases will have no lesions

visible on gross post-mortem examination. In addition to Bsal

infection, biologists, veterinarians, and diagnosticians are re-

minded to consider differentials for ulcerative or erosive lesions

in amphibians such as viral, bacterial, parasitic or other fungal

infections as well as lesions due to trauma or environmental

conditions (Green 2001). Lesions due to Bsal infection may oc-

cur at any site on the head, body, limbs, or tail of infected in-

dividuals. Chytridiomycosis is not known to be associated with

internal gross lesions (Martel et al. 2013). Although clinical com-

patibility may raise the index of suspicion for a positive diag-

nosis, its presence is not required for diagnostic categorization.

Histopathology.—Histopathological evidence most sugges-

tive of Bsal infection in the epidermis of salamanders is multi-

focal epidermal necrosis with loss of distinction between layers

of keratinocytes associated with myriad intracellular and extra-

cellular chytrid-type fungal thalli (Fig. 1) (Martel et al. 2013; A.

P. Pessier, unpubl. data). Thalli have a diameter of 6.9–17.2 μm

(average 12.2 ± 1.9 μm, N = 50). Lesions multifocally have areas

of erosion or ulceration. In early lesions and at the periphery of

older lesions, chytrid thalli may be observed within keratino-

cyte cytoplasm with margination of cell nuclei.

Necrotizing lesions most suspicious for Bsal (Bsal-type

chytridiomycosis) can be contrasted with those typical of Bd

infection (Bd-type chytridiomycosis) in which the epidermis

is predominantly hyperplastic and hyperkeratotic with many

superficial intracytoplasmic chytrid-type fungal thalli (Fig. 1).

However, there is overlap in these infection patterns.

General histologic features of chytrid (Batrachochytrium

spp.) fungal thalli are 5–20 μm diameter, round to slightly oval

organisms, that may contain 2–3 μm basophilic spores (zoo-

spores) or a discharge tube (giving a flask-like appearance)

(Berger et al. 2005). However, developing thalli or empty thalli

(those that have already discharged zoospores) often predomi-

nate. A highly characteristic feature of chytrid thalli are colonial

thalli that have internal septa. Colonial thalli are most easily

observed when empty or with stains that highlight fungal cell

walls (e.g., Grocott’s methenamine silver or periodic acid-

Schiff). Features of chytrid thalli that are more consistent with

Bsal over than Bd are numerous colonial thalli (compared to

infrequent) with multiple internal septa (rather than single).

However, these two species cannot be definitively distinguished

histologically at this time.

III. Laboratory Criteria for Diagnosis

Current molecular methods for verification of Bsal via poly-

merase chain reactions (PCR) are provided by Martel et al. (2013)

and via quantitative PCR by Blooi et al. (2013). Methods for cul-

turing Bsal are available in Martel et al. (2013).

Fig. 1. Comparison of Bd and Bsal-type chytridiomycosis. Notophthalmus viridescens. Hematoxylin and eosin stain 1000×. Bd-type chy-

tridiomycosis (A) is proliferative with epidermal hyperplasia and hyperkeratosis and numerous chytrid thalli in superficial keratinocytes

(arrows). The keratinocytes are arranged in distinct layers with intact nuclei (N). In contrast, Bsal-type chytridiomycosis (B) has almost

full-thickness necrosis of keratinocytes with myriad chytrid thalli (arrows) that frequently have internal septa (colonial thalli). Note the loss

of distinct layers of keratinocytes. At the periphery of this area of necrosis, a remaining keratinocyte has two intracytoplasmic chytrid thalli

that marginate the nucleus (circle).

Herpetological Review 47(2), 2016

AMPHIBIAN AND REPTILE DISEASES 209

Case CLassiFiCation

Below we provide criteria for three diagnostic categories of

Bsal based on diagnostic criteria. PCR and culturing methods al-

low for confirmation of the presence of Bsal but do not necessar-

ily indicate infection or the presence of disease. Histopathology

can provide support for chytridiomycosis in the salamander, but

as some histopathological findings such as necrosis and ulcer-

ation in the absence of chytrid fungi are non-specific and can be

caused by a wide variety of pathogens and environmental con-

ditions (Green 2001), a definitive diagnosis must include both

identification of the pathogen and demonstration of disease in

the salamander.

Bsal present.—Positive Bsal PCR or Bsal culture from skin

tissue of an animal for which compatible gross lesions were not

observed and for which histopathology was either not done or

was not consistent with Bsal histopathology (lacking epidermal

necrosis associated with chytrid zoosporangia).

Positive Bsal PCR or Bsal culture from a sample (e.g., swab

from individual or environmental sample) for which gross pa-

thology was not observed or recorded and for which histopathol-

ogy was not done or was not consistent with Bsal histopathology

(lacking epidermal necrosis associated with chytrid zoosporan-

gia).

Further verification (via additional samples or alternative

methodology) of a Bsal positive sample in a new area of detec-

tion is highly recommended.

Suspect Bsal chytridiomycosis.—Histopathology consistent

with Bsal infection (epidermal necrosis associated with chytrid

zoosporangia) in the absence of corroborating Bsal PCR or Bsal

fungal culture (either negative results or specimen unsuitable for

analysis).

Further verification (via additional diagnostics such as PCR

or culture) of a Bsal suspect sample is necessary for a definitive

diagnosis.

Confirmed Bsal chytridiomycosis.—Histopathology con-

sistent with Bsal infection (epidermal necrosis associated with

chytrid zoosporangia) and positive Bsal PCR or Bsal culture from

skin samples

Histopathology consistent with chytridiomycosis AND posi-

tive Bsal PCR or Bsal culture and Bd PCR or culture negative.

If Bd is also detected, further investigation into the cause of

the disease is highly recommended.

Conclusion.—As with all emerging diseases there are limited

data and many knowledge gaps for Bsal. This case definition pro-

vides guidelines for reporting Bsal chytridiomycosis. Any diag-

nosis of Bsal should be reported immediately to a regional, state,

or federal wildlife agency. This case definition will be updated as

further information is reported and a current version will be lo-

cated at www.salamanderfungus.org.

Acknowledgments.—We thank Julie Ellis, Michael Garner, Deb-

orah Iwanowicz, James Lewis, Steven Lloyd, Jeffrey Lorch, Laura

Sprague, Craig Stephen, Tom Waltzek, John Wood, and Julia Lank-

ton for reviewing drafts of this document. Authors and reviewers are

members of the Bsal Diagnostics Committee of the U.S. Bsal Task

Force. This group was initiated at a meeting hosted by USGS Powell

Center for Analysis and Synthesis, which was supported by the USGS

Ecosystems mission area. The findings and conclusions in this article

are those of the authors and do not necessarily represent the views

of the U.S. Fish and Wildlife Service. Use of trade, product, or firm

names is for descriptive purposes only and does not imply endorse-

ment by the U.S. government.

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Nov 2013
J CLIN MICROBIOL

Chytridiomycosis is a lethal fungal disease contributing to declines and extinctions of amphibian species worldwide. The currently used molecular screening tests for chytridiomycosis fail to detect the recently described species Batrachochytrium salamandrivorans. In this study, we present a duplex real-time PCR that allows the simultaneous detection of B. salamandrivorans and Batrachochytrium dendrobatidis. With B. dendrobatidis- and B. salamandrivorans-specific primers and probes, detection of the two pathogens in amphibian samples is possible, with a detection limit of 0.1 genomic equivalent of zoospores of both pathogens per PCR. The developed real-time PCR shows high degrees of specificity and sensitivity, high linear correlations (r2 > 0.995), and high amplification efficiencies (>94%) for B. dendrobatidis and B. salamandrivorans. In conclusion, the described duplex real-time PCR can be used to detect DNA of B. dendrobatidis and B. salamandrivorans with highly reproducible and reliable results.

Life cycle stages of Batrachochytrium dendrobatidis (Longcore), the amphibian chytrid.

Article

Full-text available

Jan 2006

An overview of the morphology and life cycle of Batrachochytrium dendrobatidis, the cause of chytridiomycosis of amphibians, is presented. We used a range of methods to examine stages of the life cycle in culture and in frog skin, and to assess ultrastructural pathology in the skin of 2 frogs. Methods included light microscopy, transmission electron microscopy with conventional methods as well as high pressure freezing and freeze substitution, and scanning electron microscopy with critical point drying as well as examination of bulk-frozen and freeze-fractured material. Although chytridiomycosis is an emerging disease, B. dendrobatidis has adaptations that suggest it has long been evolved to live within cells in the dynamic tissue of the stratified epidermis. Sporangia developed at a rate that coincided with the maturation of the cell, and fungal discharge tubes usually opened onto the distal surface of epidermal cells of the stratum corneum. A zone of condensed, fibrillar, host cytoplasm surrounded some sporangia. Hyperkeratosis may be due to (1) a hyperplastic response that leads to an increased turnover of epidermal cells, and (2) premature keratinization and death of infected cells.

Injurious Wildlife Species; Listing salamanders due to risk of salamander chytrid fungus

Jan 2016
1534-1556

u.s. FisH and wiLdLiFe serviCe. 2016. Injurious Wildlife Species; Listing salamanders due to risk of salamander chytrid fungus. Federal Register 81(8):1534-1556.

Powers, k. L. d. riCHgeLs, r. e. russeLL, B. r. sCHmidt, a. sPitZen-van der sLuiJs, m. k. watry, d. C. woodHams, and C. L. wHite. 2016. Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States-Developing research, monitoring, and management strategies

15325-15329

E H C Grant
. J Canessa
J R Adams
L Ballard
C J Berger
J Briggs
. J Coleman
. C Gray
Harris
B Harris
. P Hossack
J Huyvaert
Lips
H I Lovich
J Mccallum
. H Olson

grant, e. H. C., e. mutHs, r. a. katZ, s. Canessa, m. J. adams, J. r. BaLLard, L. Berger, C. J. Briggs, J. CoLeman, m. J. gray, m. C. Harris, r. n. Harris, B. HossaCk, k. P. Huyvaert, J. e. koLBy, k. r. LiPs, r. e. LoviCH, H. i. mCCaLLum, J. r. mendeLson, iii, P. nanJaPPa, d. H. oLson, J. g. Powers, k. L. d. riCHgeLs, r. e. russeLL, B. r. sCHmidt, a. sPitZen-van der sLuiJs, m. k. watry, d. C. woodHams, and C. L. wHite. 2016. Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States-Developing research, monitoring, and management strategies: U.S. Geological Survey Open-File Report 2015-1233, 16 pp., http://dx.doi.org/10.3133/ofr20151233. green, d. e. 2001. Pathology of amphibians. In K. M. Wright and B. R. Whitaker (eds.), Amphibian Medicine and Captive Husbandry, pp. 401-485. Krieger Publishing Company, Malabar, Florida. marteL, a, a. sPitZen-van der sLuiJs, m. BLooi, w. Bert, r. duCateLLe, m. C. FisHer, a. woeLtJes, w. Bosman, k. CHiers, F. Bossuyt, and F. Pasmans. 2013. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc. Nat. Acad. Sci. 110(38):15325-15329.