Lee
Berger and Rick Speare
School of Public
Health and Tropical Medicine
James Cook University
Townsville 4811
Australia.
The range of bacteria reported as causing disease in amphibians is small. Bacterial septicaemia appears to be the only bacterial disease associated with significant mortality in wild amphibians, and it can cause significant disease in captivity. Infection with non-haemolytic group B Streptococcus and chlamydia have caused outbreaks in captive amphibians. Other bacteria have caused sporadic cases of disease with no epidemics reported. Another group of bacteria can be carried by amphibians with minimal effect and are potentially capable of causing infections in humans (zoonotic diseases). Salmonella and Leptospira are in this category and are a potential risk to humans, livestock and domestic pets.
Bacterial septicaemia
Bacterial septicaemia is infection of the blood stream by bacteria with accompanying signs of disease.
There are many well-described accounts of large epidemics of bacterial septicaemia in captive amphibians. These are often caused by A. hydrophila and other gram negative bacteria or combinations of bacteria, including Pseudomonas spp., Proteus spp., Flavobacterium indologenes and F. meningosepticum (Hubbard, 1981; Taylor et al., 1993; Olson et al., 1992; Anver and Pond, 1984). A syndrome attributed to bacterial septicaemia was called “red leg” due to haemorrhages and erythema on hindlimb skin (Emerson and Norris, 1905). This descriptive term appears to have been misinterpreted by some zoologists and the general public to mean that any frog with reddening of the skin of the hind legs has “red leg” and hence bacterial septicaemia (Berger 2001).
In captive amphibians outbreaks
of bacterial septicaemia have high mortality rates. Clinical signs include pale skin, petechiation, haemorrhagic cutaneous
ulcers, lethargy, anorexia, oedema, haemorrhages in internal organs, ascites
and pale livers. On histology, there may be degenerative myopathy and multiple
foci of coagulative necrosis with clumps of bacteria. Variable results were
obtained from transmission experiments - the disease usually required
inoculation of the bacteria, or bath exposure and stress (Glorioso et al 1974; Dusi
1949; Somsiri et al 1997). A.
hydrophila and many of the other bacteria causing infections in captive
amphibians can be isolated from healthy animals and from the environment (Carr et al 1976; Hird et al 1981)
suggesting that disease occurs secondary to stresses caused by poor husbandry
such as overcrowding, dirty conditions, trauma, temperature changes, and also
after transport (Hubbard 1981; Glorioso et
al 1974).
These bacteria can also
be cultured from cases of viral disease particularly when frogs are collected
dead, and symptoms of “red leg” are similar to those caused by
iridoviruses (Cunningham et al 1996a). Some
mass die-offs in the wild have also been attributed to bacteria due to their
presence in dying animals, but these diagnoses are dubious due to a lack of
histopathological confirmation and since other agents, particularly viruses and
the amphibian chytrid, were not looked for. Bacteria were implicated in
die-offs in Alytes obstetricans in the Pyrenean mountains in Spain (Marquez et
al 1995), in R. muscosa in California
(Bradford 1991) and in B. boreas boreas
in Colorado (Carey 1993). An epidemic among tadpoles of Rana sylvatica in Rhode Island, USA was reported to be caused by A. hydrophila (Nyman 1986). Usually, deaths due to Aeromonas or Pseudomonas are secondary to environmental stressors or in captive
conditions, poor management practices.
Non-haemolytic group
B Streptococcus
A non-haemolytic group B Streptococcus caused an outbreak killing 80% of about 100000 farmed bull frogs (R. catesbiana) in Brazil (Amborski et al 1983). Septicaemia, necrotising splenitis and hepatitis with haemorrhages occurred in frogs. The outbreak was associated with overcrowding and stress. Mortality due to a similar streptococcus occurred in bullfrogs, R. catesbiana, being raised for consumption in Uruguay (Mazzoni 2001).
Chlamydia
Chlamydia is a degenerate bacteria which lives intracellularly within the amphibian host. Outbreaks of chlamydiosis in captive amphibians resulted in fulminant, multisystemic infections with pyogranulomatus inflammation. Chlamydial infections have been reported in captive amphibians, causing moderate to high mortality rates in various species including Xenopus laevis in the USA, and Ceratobatrachus guentheri in Canada (Honeyman et al 1992; Howerth 1984; Newcomer et al 1982; Wilcke et al 1983). In these cases, the chlamydial species was either unknown or assumed to be C. psittaci. Recently, C. pneumoniae has been identified as the cause of disease in a wild frog, Myxophyes iteratus with chronic pneumonia in Australia (Berger et al 1999) and in a captive colony of Xenopus tropicalis in USA (Reed et al 2000). C. pneumoniae is an important human pathogen that had previously been found only in humans, koalas and a horse (Storey et al 1993).
Mycobacteria
Mycobacterial infection of amphibians has been reported only in captivity and occurs mainly in immuno-compromised animals. Mortality rates are usually low. Natural resistance to mycobacteria, which are ubiquitous in aquatic environments, is higher than in homeotherms (Reichenbach-Klinke and Elkan 1965). Mycobacterium marinum was experimentally shown to cause a chronic granulomatous non-lethal disease in immunocompetent leopard frogs (R. pipiens) whereas frogs immunocompromised with hydrocortisone developed an acute lethal disease (Ramakrishnan et al 1997). Infections may primarily involve skin, respiratory tract or intestines. Frogs have been found with single large tumour-like masses or with disseminated nodules throughout internal organs. Organs such as liver, spleen, kidney or testes may become almost completely destroyed by the infection before the animal dies, usually with cachexia (Reichenbach-Klinke and Elkan 1965). Early granulomas are composed of mostly epithelioid macrophages, which may progress to form encapsulated foci with dry caseous centres. Granulomas typically contain large numbers of acid-fast bacilli.
Salmonella are members of the large bacterial family Enterobactericae, are usually
found in the intestinal tract of clinically normal animals, are excreted in
faeces, and can cause serious disease in humans and domestic animals.
Salmonellae are a significant cause of “food poisoning”, causing
gasterenteritis and more serious diseases. Contamination can occur at any point
in the processing of food. For humans salmonellosis is a notifiable disease due
to its potential severity, but also because it is a marker of the
microbiological safety of the human food chain. Water borne infections can
occur, but are unusual (Taylor et al 2000).
Amphibians may carry
pathogenic Salmonella species, but
rarely are frogs reported to be showing signs of disease (Reichenbach-Klinke
and Elkan 1965; Anver and Pond 1984). Prevalence of salmonellas isolated in
surveys from clinically normal amphibians is generally greater than 10% and
sometimes as high as 60% particularly if intestinal contents are sampled at
several sites (Sharma et al 1974). Salmonella are generally not of significance
to the amphibian host, but may infect humans and other animals. In Australia, Salmonella were isolated from 12.7%
(19/150) of B. marinus collected from
the wild and 9 serotypes were identified. All nine had previously been isolated
in Australia from humans and livestock (O'Shea et al 1990). An outbreak of gastroenteritis in humans
near Rockhampton was thought to have possibly arisen from green tree frogs (Litoria caerulea) contaminating drinking
water in rainwater tanks (Taylor et al 2000). Sharma et al (1974) found high
concentrations of bacteria in intestinal contents of toads and suggested that
amphibians may be good reservoirs of salmonellae with a high potential to
contaminate the environment. Some strains of salmonellae are cosmopolitan while
others are not found in Australia, but could be imported.
Table 3. Prevalence of salmonellas in clinically normal amphibians.
|
Country |
Amphibian host |
Prevalence |
Reference |
Europe |
|
|
|
|
Canary Islands |
Rana perezei
|
60% |
Monzon Moreno et al 1995 |
Australia |
|
|
|
|
North Queensland |
Bufo marinus
|
12.7% (19/150) |
O’Shea et al 1990 |
|
|
Litoria caerulea
|
One isolate |
Taylor et al 2000 |
Asia |
|
|
|
|
India |
Bufo spp. |
7% (40/570) |
Sahib Singh et al 1979 |
|
|
Bufo spp. |
36.7% (121/329) |
Sharma et al 1974; Sharma 1979 |
Central America |
|
|
|
|
Trinidad, Grenada |
Bufo marinus
Hyla minuta |
41.6% (25/60) 50% (1/2) |
Everard et al 1979 |
South America |
|
|
|
|
Surinam |
Bufo marinus
|
55.5% (15/27) |
Bool et al 1958 |
Leptospira
Leptospira are spirochaetal bacteria that usually invade the kidney of vertebrates and are excreted in the urine. Humans and domestic animals are susceptible to various strains of Leptospira usually from the species Leptospira interrogans. Serious acute and chronic disease occasionally with death can result. Workers in the banana industry in North Queensland have high rates of infection with leptospirosis, but the reason for this has yet to be determined (Smythe et al 1997). Serovars Zanoni and Australis are the most prevalent in banana workers.
Little detailed work has been done on the occurrence of Leptospira in amphibians, and on the significance of amphibians as reservoir hosts for leptospirosis in humans and domestic animals. The most comprehensive studies appear to have been done on Barbados. A series of papers reported that toads (Bufo marinus) and frogs (Eleutherodactylus johnstonei) could act as reservoirs for serovars of Leptospira pathogenic to humans (Gravekamp et al 1991; Everard et al 1990; Everard et al 1988). In addition, a new serovar, bajan, within the Autumnalis serogroup was identified. Prevalences of Leptospira isolated from both species of amphibians was about 4%, but serological evidence of past infection was much higher (>21%). Toads and frogs on Barbados were potentially significant sources of environmental contamination for human infections. A new serovar “C3” was isolated from a clinically normal toad (Bufo marinus) in the Philippines (Babudieri et al 1973). Experimentally this isolate was pathogenic to mammals. No studies appear to have been done on leptospires in amphibians in Australia.
Updated 16 February, 2003
Rick Speare