Tracking trends and analyzing new and reemerging infectious disease issues around the world

117 Pages·1999·2.47 MB·English

(cid:1)(cid:2)(cid:3)(cid:4)(cid:5)(cid:6)(cid:7)(cid:8)(cid:9)(cid:10)(cid:2)(cid:11)(cid:7)(cid:12)(cid:13)(cid:9)(cid:3)(cid:7)(cid:12)(cid:9)(cid:3)(cid:7)(cid:3)(cid:14)(cid:15)(cid:16)(cid:6)(cid:7)(cid:8)(cid:9)(cid:7)(cid:11)(cid:17)(cid:9)(cid:3)(cid:7)(cid:12)(cid:9)(cid:2)(cid:11)(cid:11)(cid:18)(cid:11)(cid:2)(cid:8)(cid:6)(cid:7)(cid:8)
(cid:6)(cid:7)(cid:19)(cid:11)(cid:4)(cid:10)(cid:6)(cid:20)(cid:21)(cid:13)(cid:9)(cid:12)(cid:6)(cid:13)(cid:11)(cid:3)(cid:13)(cid:11)(cid:9)(cid:6)(cid:13)(cid:13)(cid:21)(cid:11)(cid:13)(cid:9)(cid:3)(cid:2)(cid:20)(cid:21)(cid:7)(cid:12)(cid:9)(cid:10)(cid:22)(cid:11)(cid:9)(cid:17)(cid:20)(cid:2)(cid:14)(cid:12)
(cid:23)(cid:9)(cid:24)(cid:11)(cid:11)(cid:2)(cid:25)(cid:2)(cid:11)(cid:26)(cid:6)(cid:11)(cid:17)(cid:11)(cid:12)(cid:9)(cid:27)(cid:20)(cid:21)(cid:2)(cid:7)(cid:3)(cid:14)(cid:9)(cid:24)(cid:21)(cid:28)(cid:14)(cid:6)(cid:13)(cid:22)(cid:11)(cid:12)(cid:9)(cid:28)(cid:15)(cid:9)(cid:10)(cid:22)(cid:11)(cid:9)(cid:29)(cid:3)(cid:10)(cid:6)(cid:20)(cid:7)(cid:3)(cid:14)(cid:9)(cid:30)(cid:11)(cid:7)(cid:10)(cid:11)(cid:2)(cid:9)(cid:19)(cid:20)(cid:2)(cid:9)(cid:31)(cid:7)(cid:19)(cid:11)(cid:4)(cid:10)(cid:6)(cid:20)(cid:21)(cid:13)(cid:9) (cid:6)(cid:13)(cid:11)(cid:3)(cid:13)(cid:11)(cid:13) !(cid:20)(cid:14)"(cid:9)#$(cid:9)(cid:29)(cid:20)"(cid:9)%$(cid:9)(cid:29)(cid:20)(cid:26)& (cid:11)(cid:4)(cid:9)’(((
(cid:23)(cid:18)(cid:24)(cid:22)(cid:6)(cid:28)(cid:6)(cid:3)(cid:7)(cid:13) (cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9))(cid:2)(cid:24)(cid:22)(cid:3)(cid:7)(cid:9)!(cid:3)(cid:4)(cid:4)(cid:6)(cid:7)(cid:11)(cid:13)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:9)(cid:23)(cid:7)(cid:10)(cid:6)(cid:18)(cid:6)(cid:4)(cid:2)(cid:20)(cid:28)(cid:6)(cid:3)(cid:14)(cid:9)*(cid:11)(cid:13)(cid:6)(cid:13)(cid:10)(cid:3)(cid:7)(cid:4)(cid:11)
(cid:1)(cid:2)(cid:1)
(cid:1)(cid:2)(cid:3)(cid:4)(cid:5)(cid:6)(cid:7)(cid:2)(cid:8)(cid:6)(cid:9)(cid:10)(cid:11)(cid:9)(cid:12)(cid:2)(cid:4)(cid:13)(cid:6)(cid:12)(cid:9)(cid:4)(cid:8)(cid:1)(cid:9)(cid:12)(cid:14)(cid:7)(cid:4)(cid:8)(cid:9)(cid:15)(cid:2)(cid:5)(cid:16)(cid:17)(cid:18)(cid:2)(cid:15)
(cid:1)(cid:2)(cid:3)(cid:4)(cid:2)(cid:5)(cid:6)(cid:7)(cid:8)(cid:9)(cid:5)(cid:7)(cid:10)(cid:11)(cid:6)(cid:2)(cid:12)(cid:6)(cid:2)(cid:7)(cid:1)(cid:9)(cid:3)(cid:4)(cid:5)(cid:9)(cid:13)
(cid:12)(cid:3)(cid:10)(cid:7)(cid:14)(cid:5)(cid:2)(cid:15)(cid:2)(cid:3)(cid:4)(cid:11)(cid:9)(cid:3)
Volume 5, Number 6
November–December 1999
Perspectives
Emerging Infectious Diseases and Amphibian P. Daszak et al.
Population Declines......................................735
Development of Orphan Vaccines: J. Lang and
An Industry Perspective...............................749 S.C. Wood
Synopsis
Antimicrobial Resistance with G.V. Doern et al.
Streptococcus pneumoniae in the
United States, 1997–98.................................757
Research
Epidemiologic Studies of Cyclospora C. Bern et al.
Cover: Amanda Hyatt. Frogs, Glorious
Frogs (1999). Reprinted with cayetanensis in Guatemala .........................766
permission of the artist, Geelong,
Australia. Serologic Evidence of Human Monocytic A. Keysary et al.
and Granulocytic Ehrlichiosis in Israel.......775
Letters
Supplementing Tuberculosis Surveillance D.S. Yokoe et al.
with Automated Data from
Swine as a Potential Reservoir
Health Maintenance Organizations ............779
of Shiga Toxin-Producing
Escherichia coli O157:H7 in
Using Automated Pharmacy Records G.S. Subramanyan
Japan .................................833
to Assess the Management et al.
M. Nakazawa et. al
of Tuberculosis..............................................788
Hospitalizations for Rotavirus
Gastroenteritis in Gipuzkoa
Hantavirus Reservoir Hosts Associated G. Calderón
(Basque Country), Spain ...834
with Peridomestic Habitats
G. Cilla et al.
in Argentina..................................................792
Israeli Spotted Fever Rickettsia
(Rickettsia conorii Complex) Dispatches
Associated with Human
Disease in Portugal............835
Large, Persistent Epidemic of Adenovirus K.M. McNeill et al.
F. Bacellar et al.
Type 4-Associated Acute Respiratory
Disease in U.S. Army Trainees ....................798
The opinions expressed by authors
contributing to this journal do not
necessarily reflect the opinions of the Changes in Antimicrobial Resistance among M.A. Davis et al.
Centers for Disease Control and Salmonella enterica Serovar Typhimurium
Prevention or the institutions with Isolates from Humans and Cattle in the
which the authors are affiliated.
Northwestern United States, 1982–1997....802
Volume 5, Number 6
November–December 1999
Letters Dispatches
Avoiding Misdiagnosis of Toxic Shock Syndrome in the U.S.: R.A. Hajjeh et al.
Malaria: A Novel Automated Surveillance Update, 1979-1996..................807
Method Allows Specific
Diagnosis, even in the absence New Rickettsiae in Ticks Collected in E. Rydkina et al.
of Clinical Suspicion ..........836 Territories of the Former Soviet Union ......811
T. Hänscheid et al.
The First Reported Case Computer-Generated Dot Maps as S.B. Eng et al.
of Aerococcus Bacteremia an Epidemiologic Tool: Investigating
in a Patient with an Outbreak of Toxoplasmosis.....................815
HIV Infection.....................838
J.H. Razeq et al. HIV Infection as a Risk Factor J.T. Baer et al.
ew
for Shigellosis................................................820
Proficiency in Detecting
Vancomycin Resistance in
Enterococci among Dengue Seroconversion among Israeli I. Potasman et al.
Clinical Laboratories in Travelers to Tropical Countries...................824
Santiago, Chile...................839
J.A. Labarca et al. Effectiveness of Pneumococcal Polysaccharide A.E. Fiore et al.
Vaccine for Preschool-Age Children
Food-Related Illness and Death
with Chronic Disease ...................................828
in the United States ..........840
C. Hedberg
Commentary
Food-Related Illness and Death
in the United States—Reply to
Dr. Hedberg........................841 Stimulating the Development B. Schwartz and
P.S. Mead et al. of Orphan (and Other) Vaccines..................832 N.R. Rabinovich
Specimen Collection for
Electron Microscopy ..........842
J.A. Marshall and M.G. Catton
News and Notes
Upcoming Keystone
Symposia...........................843 The journal is distributed electronically and in hard copy and is available at no charge.
Applied Epidemiology YES, I would like to receive Emerging Infectious Diseases.
Course ...............................843
Please print your name and
International Conference business address in the box and
on Nosocomial and return by fax to 404-639-3075 or
Health Care-Associated mail to
Infections...........................844 EID Editor
CDC/NCID/MS D61
Towards a Healthy
1600 Clifton Road, NE
Europe for the
Atlanta, GA 30333
Year 2010...........................844
Erratum.............................844 Moving? Please give us your new address (in the box) and
ICEID 2000 .......................845 print the number of your old mailing label here__________
Journal Web Page .............846
PPPPPeeeeerrrrrssssspppppeeeeeccccctttttiiiiivvvvveeeeesssss
Emerging Infectious Diseases and
Amphibian Population Declines
PPPPPeeeeettttteeeeerrrrr DDDDDaaaaassssszzzzzaaaaakkkkk,,,,,***** LLLLLeeeeeeeeee BBBBBeeeeerrrrrgggggeeeeerrrrr,,,,,†††††‡‡‡‡‡ AAAAAnnnnndddddrrrrreeeeewwwww AAAAA..... CCCCCuuuuunnnnnnnnnniiiiinnnnnggggghhhhhaaaaammmmm,,,,,§§§§§
AAAAAllllleeeeexxxxx DDDDD..... HHHHHyyyyyaaaaatttttttttt,,,,,††††† DDDDD..... EEEEEaaaaarrrrrlllll GGGGGrrrrreeeeeeeeeennnnn,,,,,¶¶¶¶¶ aaaaannnnnddddd RRRRRiiiiiccccckkkkk SSSSSpppppeeeeeaaaaarrrrreeeee‡‡‡‡‡
*Institute of Ecology, University of Georgia, Athens, Georgia, USA;
†Australian Animal Health Laboratory, Commonwealth Scientific Industrial
Research Organization, Geelong, Victoria, Australia; ‡School of Public
Health and Tropical Medicine, James Cook University, Townsville,
Queensland, Australia; §Institute of Zoology, Zoological Society of London,
London, United Kingdom; and ¶National Wildlife Health Center, U.S.
Geological Survey, Madison, Wisconsin, USA
We review recent research on the pathology, ecology, and biogeography of two
emerging infectious wildlife diseases, chytridiomycosis and ranaviral disease, in the
context of host-parasite population biology. We examine the role of these diseases in
the global decline of amphibian populations and propose hypotheses for the origins and
impact of these panzootics. Finally, we discuss emerging infectious diseases as a
global threat to wildlife populations.
Emerging infectious diseases have been (12-19). While some declines are clearly due to
reported increasingly as causes of death in free- habitat destruction, others are not associated
living wild animals (1). These diseases are a with obvious environmental factors. Causal
particular threat to wildlife species whose hypotheses include the introduction of predators
population, habitat, or range has been dimin- or competitors, increased ultraviolet (UV-B)
ished or artificially manipulated to promote irradiation, acid precipitation, adverse weather
species survival (e.g., captive breeding, translo- patterns, environmental pollution, infectious
cation, and release programs) (2-4). An early disease, or a combination of these. Transdermal
example of an emerging disease panzootic was water uptake and gaseous exchange and a
the introduction of rinderpest in African domestic biphasic life cycle are important aspects of
cattle in 1889 (5). More recently, epizootics and amphibian biology. These factors led to the
panzootics of wildlife have been increasingly hypothesis that amphibians act as sentinels for
reported in terrestrial (1) and marine (6) habitats global environmental degradation (12,18). How-
and are probably underreported (1,4,7-9). Recent ever, this role has yet to be demonstrated, and
advances in theoretical and experimental host- many causal factors may be present (12,19,20).
parasite ecology have demonstrated a major role Of particular concern are population declines
for infectious agents in the population biology of in ecologically pristine areas, such as the montane
wild animals (10,11). We discuss recent data on tropical rain forests of Australia and Central
two newly emerging infectious diseases of America, where human impact from agriculture,
amphibians and, by reference to host-parasite deforestation, or pollution is thought to be
ecology, propose hypotheses to explain their negligible. Here, long-term data demonstrate
origin and impact. recent and catastrophic amphibian population
declines, often resulting in the complete loss of
Amphibian Population Declines amphibian species (local extinction of multiple
Global declines in amphibian population are species) from large swaths of habitat (20-25).
perhaps one of the most pressing and enigmatic These declines include the disappearance and
environmental problems of the late 20th century presumed extinction of the recently discovered
golden toad (Bufo periglenes) of Costa Rica (23)
Address for correspondence: Peter Daszak, Institute of Ecology,
and as many as seven Australian amphibian
University of Georgia, Ecology Building, Athens, GA 30602,
USA; fax: [phone]; e-mail: [email protected]. species, including two species of gastric-brooding
Vol. 5, No. 6, November–December 1999 777773333355555 Emerging Infectious Diseases
PPPPPeeeeerrrrrssssspppppeeeeeccccctttttiiiiivvvvveeeeesssss
frog (Rheobatrachus spp.) (20). These data, along (26-31) have repeatedly found two diseases as the
with recent findings of amphibian mass deaths in causes of amphibian mass deaths globally
these areas, suggest that such local extinctions are (Table 1): chytridiomycosis in the rain forests of
not normal population fluctuations or Australia and Central and South America and
metapopulation dynamics. some parts of North America (28-32) and
Investigations in Australia, the United iridoviral infections in the United Kingdom, the
Kingdom, and North and Central America United States, and Canada (26,27,33-36). Both
Table 1. Mass deaths caused by chytridiomycosis and ranaviral disease in wild populations of amphibians
Locality and date
of mass deaths Species affected and impacta References
Chytridiomycosis E. & S. Australia Multiple montane rain forest and temperate 28-30
(1993-1999)b species. Mass deaths, local extinctions,
population declines. Near-extinction
of Taudactylus acutirostris. Hypothesized
link with global extinction of two species
of gastric brooding frog (Rheobatrachus spp.).
W. Australia Multiple species, predominantly the western 29,31
(1998-1999)c green (or motorbike) frog (Litoria moorei).
Mass deaths, population declines.
Costa Rica Multiple montane rain forest species. 20,23,
and Panama Mass deaths, local extinctions, population 28,29
(1994-99) declines. Hypothesized link with global
extinction of golden toad, Bufo periglenes.
Ecuador (1999) Montane rain forest Atelopus species, Telmatobius 29
niger, and Gastrothecus pseustes. Unknown impact.
Arizona Leopard frog (Rana yavapiensis & 29
(1996-1997) R. chiricahuensis). Mass deaths.
S. Arizona (1999) Leopard frog (Rana sp.). Mass deaths. 31,32
Colorado (1999) Boreal toad (Bufo boreas). Mass deaths. d
Colorado (1970s) Leopard frog (Rana pipiens). Mass deaths. 32d
Sierra Nevada, Yosemite toad (Bufo canorus). Mass deaths. 32e
California (1970s)
Ranaviral disease United Kingdom Common frog (Rana temporaria). Mass deaths, 5,16,26,
(1992-1999f) possibly population declines. 33,34
Arizona (1995) Sonoran tiger salamander (Ambystoma tigrinum 27
stebbinsi). Mass deaths in this endangered species.
N. Dakota (1998) Tiger salamander (A. tigrinum). 35
Mass deaths.
Maine (1998) Tiger salamander (A. maculatum). 35
Mass deaths.
Utah (1998) Tiger salamander (A. tigrinum). Mass deaths. 35
Saskatchewan, Tiger salamander (A. tigrinum diaboli). Mass deaths. 36
Canada (1997)
aMass deaths did not occur in all cases of wild amphibians infected by chytridiomycosis. Bufo americanus from Maryland and
Acris crepitans from Illinois have been found infected with chytridiomycosis without observed deaths (37,38). In Australia,
chytridiomycosis has been reported from small numbers of amphibians without evidence of clinical signs or deaths in both upland
and lowland species (R. Speare, L. Berger, unpubl. obs.).
bRetrospective studies have identified chytridiomycosis as the cause of death in wild frogs in five Australian states from as early
as 1989 (29).
cThis recent outbreak was more than 2,000 km from the closest recorded chytridiomycosis-linked amphibian die-offs (31). It is
thought that chytridiomycosis may now be enzootic in many areas of Australia, but still in the process of spreading to naïve
populations. A role for chytridiomycosis in other recent W. Australian declines is suspected due to similarities in the pattern of
declines and presence of the Batrachochytrium carcasses from W. Australia since 1992.
dD.E. Green, unpubl. obs.
eD.E. Green, unpubl. obs. Historically collected specimens recently examined histologically revealed chytridiomycosis as a
contributing factor to the cause of death in 2 of 12 animals.
fA.A. Cunningham, unpubl. obs.
Emerging Infectious Diseases 777773333366666 Vol. 5, No. 6, November–December 1999
PPPPPeeeeerrrrrssssspppppeeeeeccccctttttiiiiivvvvveeeeesssss
diseases have been classified as emerging (1).
The parasitic infection recently implicated as the
cause of amphibian deformities in North
America has not been associated with mass
deaths or population declines (31).
Chytridiomycosis—an Emerging
Panzootic Fungal Disease of Amphibians
Chytridiomycosis is a fungal disease first
described in 1998 from moribund and dead adult
amphibians collected at sites of mass deaths in
Australia and Panama from 1993 to 1998 (28).
Here, long-term ecologic study sites reported
catastrophic amphibian population declines in
Big Tableland, Queensland (39,40), and Fortuna
and Cerro Pando, Panama (24,25,28). No
significant pathogens were found on routine
parasitologic, bacteriologic, mycologic, or viro-
logic examinations of tissue samples (28). Fresh
skin smears and histologic sections of the
epidermis, however, consistently contained large
numbers of developing and mature sporangia of
a new genus of chytrid fungus (phylum
Chytridiomycota) (Figures 1, 2). Sporangia were
also present within the keratinized mouthparts,
but not the epidermis, of sympatric tadpoles
(tadpoles lack epidermal keratin) (28,29). No
significant morphologic differences between
chytrids infecting Australian and Central Ameri-
can amphibians were found by transmission
electron microscopy, and the pathogen was
identified as a member of the order Chytridiales
by analysis of zoospore ultrastructure and 18s
rDNA sequence data (28). Chytrids are ubiquitous
Figure 1a: Ventral abdominal skin of Bufo haematiticus from
fungi that develop without hyphae and are found western Panama. The superficial keratinized layer of epidermis
in aquatic habitats and moist soil, where they (stratum corneum) contains numerous intracellular spherical-
to-ovoid sporangia (spore-containing bodies) of Batrachochytrium
degrade cellulose, chitin, and keratin (41).
sp. The mature sporangia (sp, arrows) are 12-20 µm (n = 25) in
Parasitic chytrids mainly infect plants, algae,
diameter and have refractile walls 0.5-2.0 µm thick. Most
protists, and invertebrates (41); the amphibian sporangia are empty, having discharged all zoospores, but a few
pathogen is the only example of a chytrid sporangia contain two to nine zoospores. This stratum corneum
is markedly thickened adjacent to groups of parasitized cells and
parasitizing vertebrates (28).
in some cases, the superficial layer has become detached. No
Clinical signs of amphibian chytridiomycosis
chytrids are present in the stratum spinosum, stratum basale,
include abnormal posture, lethargy, and loss of dermis, dermal glands, and blood vessels. Note the absence of
righting reflex. Gross lesions, which are usually hyphae and lack of an inflammatory cell response in the deeper
layers of epidermis and the dermis. Hematoxylin and eosin
not apparent, consist of abnormal epidermal
stain. Bar = 35 µm. 1b. Ventral skin of upper hind limb of
sloughing and (more rarely) epidermal ulcer-
Atelopus varius from western Panama. Two sporangia
ation; hemorrhages in the skin, muscle, or eye; containing numerous zoospores are visible within cells of the
hyperemia of digital and ventrum skin, and stratum corneum. Each flask-shaped sporangium has a single
characteristic discharge tube (arrow) at the skin surface. Exiting
congestion of viscera (29). Diagnosis is by
zoospores are visible in the discharge tubes of both sporangia.
identification of characteristic intracellular
Hyperkeratosis is minimal in this acute infection. Tissues were
flask-shaped sporangia and septate thalli within fixed in neutral-buffered 10% formalin, paraffin-embedded,
the epidermis (Figures 1, 2). sectioned at 6 µm thick and stained with hematoxylin and eosin.
Bar = 35 µm.
Vol. 5, No. 6, November–December 1999 777773333377777 Emerging Infectious Diseases
PPPPPeeeeerrrrrssssspppppeeeeeccccctttttiiiiivvvvveeeeesssss
captive Central American (T.Y. James, D.
Porter, J.E. Longcore, pers. comm.) amphibians
belong to the genus Batrachochytrium, are
probably conspecific, and form a distinct
monophyletic clade within the Chytridiales.
Emergence of Chytridiomycosis
Retrospective histologic surveys of museum
specimens of montane, riparian anurans from
protected sites in Central America and
Australia, conducted 1 to 10 years before the
population declines, showed no evidence of
chytrid infection, which suggests that
chytridiomycosis has recently emerged on two
continents (28). The relatively synchronous
Figure 2. Scanning electron micrograph of digital discovery of chytridiomycosis in Australia and
skin of a wild frog (Litoria lesueuri, from Queensland,
Central America in association with amphibian
Australia) that died of cutaneous chytridiomycosis.
population declines is striking. The data suggest
Many cells within this area of the superficial layer of
that Batrachochytrium 1) may be endemic to
the epidermis contain mature sporangia, and
these regions and the amphibian deaths and
unopened discharge tubes are visible protruding
through infected cells. The skin was fixed in 2.5% declines attributed to it have only recently been
glutaraldehyde, postfixed in 1% osmium tetroxide, discovered; 2) may be endemic and has recently
dehydrated, critical-point-dried, sputter coated with become pathogenic (e.g., through an increase in
gold, and examined with a JEOL JSM 840 scanning the organism’s prevalence or virulence, or a
electron microscope at 5 kV. All specimens are from decrease in the host’s defenses), or 3) may have
animals that were naturally infected and died due to
been introduced recently into these geographic
chytridiomycosis in montane rain forest regions of
regions and is now parasitizing novel host species.
Panama and Australia. Bar = 5 µm.
The pattern of amphibian deaths and
Photo courtesy of L. Berger, reprinted with permission from
A. Campbell (29). population declines associated with
chytridiomycosis is characteristic of an intro-
Its occurrence solely in keratinized tissue duced virulent pathogen dispersing through a
suggests that the chytrid uses amphibian naïve population (7,10,39). In Australia, a
keratin as a nutrient. A hyperkeratotic and distinct geographic and temporal progression in
hyperplastic response of the epidermis to population declines has occurred (20), moving
infection (restricted to the stratum corneum and northward at a mean rate of 100 km per year
stratum granulosum) usually coincides with the (39). In Central America, a progression from
immediate location of chytrid developmental northern Costa Rica to western Panama
stages. Inflammatory cell response is negligible. occurred from 1996 to 1998 (24,25). The uneven
An isolate cultured from captive dendrobatid progression of declines in Australia (40) may
frogs has recently been used to fulfil Koch’s reflect gaps in surveillance. Small-scale irregu-
postulates as a fatal pathogen of frogs and has larities, however, characterize the epidemiology
been described as a new genus and species, of many pandemics (43,44), within which
Batrachochytrium dendrobatidis (42). Three individual epidemics progress at different rates
mechanisms by which chytridiomycosis causes in different areas. In amphibian populations,
death have been proposed (28): 1) epidermal unevenness may be due to differences in ecologic
hyperplasia impairs essential cutaneous respira- factors (e.g., population density, habitat, age
tion or osmoregulation; 2) a fungal toxin is structure); differences among pathogen strains;
absorbed systemically (although a lack of clinical stochastic factors, such as the time of
signs in infected larvae suggests otherwise); and introduction; or a combination of these factors.
3) these factors are combined (28,37). In Australia and Central America, population
Comparison of histologic, ultrastructural, declines have been catastrophic, occurring over a
and 18s rDNA sequence data indicates that the few months, with dramatic population loss and
chytrids found in wild Australian (28) and high rates of adult deaths (20,24,25,28,39,40,45).
Emerging Infectious Diseases 777773333388888 Vol. 5, No. 6, November–December 1999
PPPPPeeeeerrrrrssssspppppeeeeeccccctttttiiiiivvvvveeeeesssss
Such high depopulation rates are characteristic The occurrence of chytridiomycosis in free-
of introduced virulent pathogens (10). Con- living North American amphibians (Table 1)
versely, in coevolved host-pathogen relation- suggests a less obvious pattern of dissemination
ships, a degree of herd immunity to the pathogen than in Central America and Australia. This
and lower virulence (infectivity and death rates) irregularity may be due to a paucity of data, the
are normally observed. The low host specificity of pathogen’s being enzootic to the United States,
amphibian chytridiomycosis (more than 30 or the pathogen’s introduction a number of years
species of wild amphibians from seven families in before. Historical reports of declines in the
Central America and Australia [28,29]) also United States include postmetamorphic death
suggests that the disease was not enzootic in syndrome, which progressed in waves through
those montane rain-forest populations. Ability to populations of amphibians, causing 90% to 100%
infect a range of host species is a characteristic of death rates in recently metamorphosed animals
many invading pathogens (10) and is less and low death rates in larvae (50). Recent reports
common in endemic microparasites that have of chytridiomycosis-linked die-offs in Bufo boreas
coevolved with their hosts. markedly resemble these previous die-offs. This
The most parsimonious hypothesis for the observation and the finding that chytridiomycosis
origin of chytridiomycosis panzootics in Austra- caused similar die-offs (of B. canorus and
lia and Central America is the introduction of R. pipiens) in the 1970s (Table 1) (32), support
disease into populations of previously unexposed the last of the above hypotheses. In the United
amphibians. Introduction of pathogens, termed States an amphibian pathogen (histologically
pathogen pollution (1), is increasingly recog- very similar to Batrachochytrium but identified
nized as a significant threat to global biodiversity as Basidiobolus ranarum) has been described in
(1,6,46) and forms an integral part of human wild Wyoming toads (Bufo hemiophrys baxteri)
history (10,47). There are precedents for the (51) and captive dwarf African clawed frogs
introduction of fungal pathogens (including (Hymenochirus curtipes) (52). As the latter
chytrid parasites) that cause high death rates species was widely introduced in ornamental
(41,48). Mechanisms by which wildlife patho- garden ponds throughout the United States in
gens can be introduced are common; for example, the late 1980s, it may be involved in the
a consequence of the increasing mobility of dissemination of Batrachochytrium.
humans is the global translocation of wildlife,
plants, soil, and ballast water (1,4,49,50). Chytridiomycosis as the
Freshwater fish and amphibians are also Cause of Population Declines
transported globally. In Australia, chytridiomycosis- The ability of a pathogen to cause local
infected cane toads (Bufo marinus), a recently population declines resulting in local host
introduced species, have been found (29), and in extinction requires a mechanism of persistence
North America, bullfrogs (Rana catesbeiana) at low host densities. In epidemiologic models,
and other species of amphibians have been highly virulent parasites rapidly suppress the
translocated or introduced widely. Some host population density below a threshold value
authors have suggested that tourists or fieldworkers required to maintain transmission, resulting in
surveying amphibian populations may have the pathogen’s extinction and recovery of the
facilitated the dissemination of Batrachochytrium host population (7,10). Microparasites such as
(19), although this has not been demonstrated. Batrachochytrium, with their relatively short
Batrachochytrium may have coevolved with some duration of infection and high death rates, have
amphibians (e.g., lowland) species, populations of an increased threshold population density and
which remain unaffected. Recent disturbances of are usually less able to persist. Many parasites
rain forest habitats may have introduced this have evolved life history strategies for persis-
parasite into naïve populations in Central America tence (10) and the presence of reservoir hosts
and Australia, leading to mass deaths. This range may augment the impact of other introduced
of disease outcomes parallels many diseases of wildlife diseases on host populations (46). The
humans, e.g., measles and smallpox, which aclinical presence of Batrachochytrium in the
produce a range of effects on persons in disease- keratinized mouthparts of amphibian larvae
endemic regions and cause massive deaths when implicates this life-cycle stage as a reservoir host
introduced into naïve populations (48). for the pathogen. This form of infection may
Vol. 5, No. 6, November–December 1999 777773333399999 Emerging Infectious Diseases
PPPPPeeeeerrrrrssssspppppeeeeeccccctttttiiiiivvvvveeeeesssss
enable Batrachochytrium to persist in reduced well known (42). Furthermore, the ability to
amphibian populations (Figure 3). In both develop and reproduce saprophytically is
Australia and Central America, chytrid infection common to many other fungal (54) (including
was observed in larval mouthparts months after chytrid [41]) and bacterial (55) pathogens. An
initial adult deaths: the larvae of many tropical epidemiologic model of a host-parasite system for
amphibian species survive 12 to 18 months—and pathogens that can reproduce saprophytically
some temperate species as long as 3 years— clearly shows a lowering of the host threshold
before metamorphosing. Examples of larval infection population, allowing the pathogen to drive the
enhancing pathogen-mediated population declines host to extinction (55). Development of
and leading to host population extinctions have Batrachochytrium for even short periods outside
been reported for invertebrates (53). its amphibian host may greatly increase its
Persistence may be further enhanced by impact and accelerate population declines. Long-
saprophytic development (Figure 3). term presence as a saprophyte may explain the
Batrachochytrium can be cultured in vitro on lack of recolonization of streams from which
tryptone agar without the addition of keratin or amphibians have been extirpated in both
its derivatives (37,42), and it will grow for at least Australia (29) and Central America (24,25).
one generation on cleaned epidermal keratin or The impact of chytridiomycosis may be
on amphibians that have died of the infection enhanced by the ecologic characteristics of
(42). Batrachochytrium may survive and certain host species. In Australia,
reproduce as a saprophytic organism in the chytridiomycosis-linked deaths have occurred in
environment, at least for short periods. Keratin both declining and nondeclining species (28,29).
(from decaying carcasses, shed skin, and other Species with declining populations belong to a
sources) is widely distributed in the environ- similar ecologic guild: regionally endemic rain
ment, and chytrids that use this substrate are forest specialists with low fecundity that
Figure 3. Diagrammatic representation of the range of disease outcomes in populations of amphibians affected
by a Batrachochytrium-like pathogen. Factors that hypothetically predispose some amphibian populations to
declines are illustrated. In this model, host ecologic traits (left side of pyramid) and parasite biologic traits
(right side of pyramid) combine to produce declines in a specific group of amphibian species that have low
fecundity, are stream-breeding habitat specialists, and occur in montane regions. These characteristics
predispose them to population declines after introduction of a waterborne pathogen with a low preferred
developmental temperature and ability to persist at low host population densities.1
1Note that the relative number of mass deaths decreases with increasing impact on population.
Emerging Infectious Diseases 777774444400000 Vol. 5, No. 6, November–December 1999
PPPPPeeeeerrrrrssssspppppeeeeeccccctttttiiiiivvvvveeeeesssss
reproduce in streams and live at high altitudes may have allowed chytridiomycosis to cause
(22). These characteristics, which are largely substantial deaths (57). Further work is required
shared by declining Central American amphib- to test this hypothesis, since a drier climate
ians (24,25), are predictors of increased impact would also predict a lower overall impact from
from chytridiomycosis. Species that reproduce in chytridiomycosis—a disease transmitted by
streams are probably more susceptible to a flagellated, waterborne zoospores. The evidence
waterborne pathogen than terrestrial breeders. suggests that cofactors are not required for
Low fecundity (56) and habitat specialization chytridiomycosis to cause amphibian mass
indicate a reduced ability to recover from deaths. Chytridiomycosis is highly pathogenic to
population declines caused by stochastic events, captive-bred amphibians exposed in captivity
including disease introduction. Laurance, where control animals remained healthy (28,42).
McDonald, and Speare (39) suggested that the Further experimental infections using extremely
relation between high-altitude populations and small inocula (100 zoospores) also proved fatal (29).
declines may be due to a pathogen with a lower Some deaths among wild amphibians have
preferred developmental temperature. Prelimi- been attributed to immunosuppression, predis-
nary data on cultured Batrachochytrium are posing them to infectious disease (13,32). In the
consistent with this hypothesis: it develops most chytridiomycosis-related deaths, chytridiomycosis
rapidly at 23oC in culture, with slower growth at was consistently found as the cause of death, and
28oC and reversible cessation of growth at 29oC the range of opportunistic infections expected to
(42). The growth rate of Batrachochytrium in the occur in immunocompromised animals was not
skin (and therefore virulence) and the survival of found (28,29). An increase in UV-B irradiation
zoospores outside the host (and therefore may influence amphibian declines (58), but in
transmission rate) are likely to be lower in the subtropical regions of Australia and Central
amphibians from the warmer lowland regions. America, data demonstrate no significant
The ability of the pathogen to survive increase in UV irradiation (29,59). Even so, the
saprophytically in the environment and for the potentional effect of increased irradiation on
disease to persist may also be enhanced in the montane riparian rain forest amphibians is
cooler montane regions. These laboratory data uncertain, since these animals lay eggs under
may explain why chytridiomycosis has been rocks or in sand banks and adults are rarely
associated with population declines in North exposed to direct sunlight (24,29). Furthermore,
American amphibians in montane localities in these regions, the species most likely to be
(31,32) and after periods of cool weather at many affected by UV increases (arboreal amphibians,
U.S. and Australian sites (29,31). which bask or lay exposed eggs) are not in decline
(20). Despite extensive research, chemical
Potential Environmental Cofactors in the pollution (20,25), habitat destruction (22), or
Emergence of Chytridiomycosis climate change (57) have not, so far, been
Multiple factors (host, pathogen, environ- causally linked either to the Australian declines
mental) may be involved in chytridiomycosis or to those at Central American sites other than
emergence. Some authors have hypothesized Monteverde. No other possible cofactors, such as
that infectious disease is only the proximate sympatric pathogens, have been found.
cause of declines and that environmental factors
such as increased UV-B, chemical pollution, Emerging Viral Diseases of Amphibians
climate change, or stress may have predisposed Iridoviruses have been implicated as the
amphibian populations to opportunistic patho- cause of amphibian mass deaths worldwide, with
gens (13,32,57). Recent work at Monteverde, novel iridoviruses of amphibians recently identi-
Costa Rica, suggests that atmospheric warming, fied from a number of regions (Tables 1, 2). The
with a resultant elevation of the average altitude Iridoviridae encompass five recognized genera:
of the base of the orographic cloud bank and an Iridovirus, Chloriridovirus, Ranavirus,
increase in dry periods, is causally linked to Lymphocystivirus, and goldfish virus 1-like
amphibian declines at this site (57). Although no viruses (71). Of these, the genus Ranavirus
pathologic studies of amphibians were under- contains pathogens of fish, amphibians, and
taken, overcrowding during periods of drought reptiles (Table 2; Figure 4).
Vol. 5, No. 6, November–December 1999 777774444411111 Emerging Infectious Diseases