epizootic ulcerative syndrome
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- epizootic ulcerative syndrome
Other Scientific Names
- mycotic granulamotoses
- red spot disease
International Common Names
- English: Aphanomyces invadans infection
OverviewTop of page
Epizootic ulcerative syndrome (EUS) is a disease of freshwater and brackishwater fish that has other synonyms such as mycotic granulomatosis (MG), red spot disease (RSD) and ulcerative mycosis (UM). More than 100 species of fish species with a wide geographic distribution have been reported to be affected by EUS. EUS outbreaks occur only when a number of causal factors combine.
The causative agent of this disease is the fungus, Aphanomyces invadans. There are a number of sufficient causes that lead to exposure of the dermis to fungal spore germination. In the early stages, red spots or small haemorrhagic lesions are found on the body surface. Intermediate stage lesions become small ulcers. Advanced stage lesions expand into large necrotic open ulcers resulting in death.
Positive diagnosis of EUS is made by the presence of mycotic granulomas in histological section and isolation of Aphanomyces invadans from infected fish. Quarantine and health certification practice for the movement of live fish between countries or regions are effective means of preventing the spread of EUS to new areas. For areas where EUS is endemic, prevention programmes should include eradication, exclusion, management, surveillance and treatment.
Outbreaks of EUS have continued to occur periodically in all target countries. The immunity of fish surviving EUS infections should be the subject of interest because records from many countries showed that the severity of EUS outbreak after the first few years tends to decrease (Mohan and Shankar, 1994; Bondad-Reantaso et al., 1992). The serious implications for the development of vaccines against EUS should be deliberated because there was a report on the strong reaction between the sera from immunized fish with the spores and mycelium of pathogenic strains of Aphanomyces and the extracts of pathogenic strains of Aphanomyces (Thompson et al., 1997).
Hosts/Species AffectedTop of page
The disease called mycotic granulomatosis was first found in ponds raising goldfish (Carassius auratus) (Miyazaki and Egusa, 1972), and ayu (Plecoglossus altivelis) in various regions in Japan in 1971 (Egusa and Masuda, 1971). Wild species such as the formosan snakehead (Channa maculata), Japanese trident goby (Tridentiger obscurus) and black mullet (Mugil cephalus) were also affected by the disease at that time (Miyazaki and Egusa, 1973a,b,c). Later, the causative agent of mycotic granulomtosis was identified as Aphanomyces piscicida by Hatai (1980). In the following year, 1972, red spot disease (RSD) was first reported in estuarine fish from the Burnett River, Queensland, Australia (McKenzie and Hall, 1976; Rodgers and Burke, 1981). Lately, outbreaks of RSD have been reported in many species of estuarine and freshwater fish in New South Wales (Callinan et al., 1989), North Territory (Humphrey and Langdon, 1986; Pearce, 1990) and Western Australia (D. Pass, personal communication). Sea mullet (Mugil cephalus), sand whiting (Sillago ciliata), yellow fin bream (Acanthopagrus australis) and barramundi (Lates calcarifer) were some of the economically important estuarine species affected. Outbreaks of RSD have occurred in farmed silver perch (Bidyanus bidyanus) which is a freshwater species of Southern Australia (Rodgers and Burke, 1981).
DistributionTop of page
Since 1971-1972 the disease gradually spread to many countries in the Asia-Pacific region. Catfish cultured in the Mekong delta, Vietnam were reported to be infected by EUS in 1973 (Roberts et al., 1994) but this information was not supported by histopathological confirmation. In 1975, there was a report on an EUS outbreak in some freshwater fish in Papua New Guinea. By the year 1980 it had spread to Malaysia and Thailand. In 1982-1983, a severe EUS outbreak in Thailand affecting snakehead (Channa striata), Puntius sp. and many species of rice field fish was recorded (Tonguthai, 1985). The outbreak was also reported in East Kalimantan, Indonesia, in 1982 and 1984, causing serious mortality on wild species such as snakehead, catfish, sand goby, Puntius sp. and kissing gouramy in natural water resources (Roberts et al., 1994). Cambodia, Laos and Myanmar also suffered from EUS in 1984. The first confirmed EUS outbreak of some freshwater fish in Laguna de Bay, Philippines, was recorded in 1985-1986. As early as 1987, Puntius sp. and snakehead in a western province of Sri Lanka were infected by EUS. After the severe flooding in 1988, the first EUS outbreak was reported in Bangladesh. Indian major carps seem to be the main species affected. In the same year, EUS occurred in northeast India and spread throughout the whole country, then to Nepal in the following year (Roberts et al., 1994). By 1996 it was confirmed that EUS had spread to the upper part of the Indus River in Pakistan (Kanchanakhan, 1996).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Afghanistan||No information available||OIE, 2009|
|Armenia||Disease never reported||OIE, 2009|
|Azerbaijan||Disease never reported||OIE, 2009|
|Bahrain||Disease never reported||OIE, 2009|
|Bhutan||No information available||OIE, 2009|
|Cambodia||No information available||NULL||OIE, 2009|
|China||Disease never reported||OIE, 2009|
|-Hong Kong||Disease never reported||OIE, 2009|
|India||No information available||OIE, 2009|
|Indonesia||Disease never reported||NULL||Roberts et al., 1994; OIE, 2009|
|Iran||No information available||OIE, 2009|
|Iraq||Absent, reported but not confirmed||OIE, 2009|
|Israel||Disease never reported||OIE, 2009|
|Japan||Disease not reported||20020904||Egusa and Masuda , 1971; OIE, 2009|
|Jordan||No information available||OIE, 2009|
|Kazakhstan||Disease not reported||OIE, 2009|
|Korea, Republic of||No information available||OIE, 2009|
|Kuwait||Disease not reported||OIE, 2009|
|Kyrgyzstan||Disease not reported||OIE, 2009|
|Laos||No information available||NULL||OIE, 2009|
|Lebanon||No information available||OIE, 2009|
|Malaysia||Disease not reported||1986||OIE, 2009|
|Mongolia||No information available||OIE, 2009|
|Myanmar||No information available||NULL||OIE, 2009|
|Nepal||No information available||NULL||Roberts et al., 1994; OIE, 2009|
|Oman||No information available||OIE, 2009|
|Pakistan||No information available||NULL||Kanchanakhan, 1996; OIE, 2009|
|Philippines||No information available||NULL||OIE, 2009|
|Qatar||No information available||OIE, 2009|
|Saudi Arabia||No information available||OIE, 2009|
|Singapore||Disease never reported||OIE, 2009|
|Sri Lanka||No information available||NULL||OIE, 2009|
|Syria||No information available||OIE, 2009|
|Tajikistan||No information available||OIE, 2009|
|Thailand||No information available||NULL||Tonguthai , 1985; OIE, 2009|
|Turkey||No information available||OIE, 2009|
|United Arab Emirates||No information available||OIE, 2009|
|Vietnam||No information available||NULL||Roberts et al., 1994; OIE, 2009|
|Yemen||No information available||OIE, 2009|
|Algeria||No information available||OIE, 2009|
|Angola||No information available||OIE, 2009|
|Benin||No information available||OIE, 2009|
|Botswana||Disease not reported||OIE, 2009|
|Burkina Faso||No information available||OIE, 2009|
|Chad||No information available||OIE, 2009|
|Congo||No information available||OIE, 2009|
|Djibouti||No information available||OIE, 2009|
|Egypt||No information available||OIE, 2009|
|Eritrea||No information available||OIE, 2009|
|Ethiopia||No information available||OIE, 2009|
|Gambia||No information available||OIE, 2009|
|Ghana||No information available||OIE, 2009|
|Guinea||No information available||OIE, 2009|
|Guinea-Bissau||No information available||OIE, 2009|
|Kenya||No information available||OIE, 2009|
|Lesotho||Disease never reported||OIE, 2009|
|Madagascar||No information available||OIE, 2009|
|Malawi||No information available||OIE, 2009|
|Mali||No information available||OIE, 2009|
|Mauritius||No information available||OIE, 2009|
|Morocco||No information available||OIE, 2009|
|Mozambique||Disease not reported||OIE, 2009|
|Nigeria||No information available||OIE, 2009|
|Senegal||No information available||OIE, 2009|
|South Africa||No information available||OIE, 2009|
|Sudan||Disease never reported||OIE, 2009|
|Swaziland||No information available||OIE, 2009|
|Tanzania||No information available||OIE, 2009|
|Togo||No information available||OIE, 2009|
|Tunisia||Disease not reported||OIE, 2009|
|Uganda||No information available||OIE, 2009|
|Zambia||No information available||OIE, 2009|
|Zimbabwe||No information available||OIE, 2009|
|Canada||Disease never reported||OIE, 2009|
|Greenland||Disease never reported||OIE, 2009|
|Mexico||Disease not reported||OIE, 2009|
|USA||Disease not reported||2004||OIE, 2009|
Central America and Caribbean
|Belize||Disease never reported||OIE, 2009|
|Costa Rica||Disease never reported||OIE, 2009|
|Cuba||Disease never reported||OIE, 2009|
|El Salvador||No information available||OIE, 2009|
|Guadeloupe||No information available||OIE, 2009|
|Guatemala||Disease never reported||OIE, 2009|
|Haiti||No information available||OIE, 2009|
|Honduras||No information available||OIE, 2009|
|Jamaica||No information available||OIE, 2009|
|Martinique||No information available||OIE, 2009|
|Nicaragua||Disease never reported||OIE, 2009|
|Panama||No information available||OIE, 2009|
|Argentina||Disease never reported||OIE, 2009|
|Bolivia||No information available||OIE, 2009|
|Brazil||Disease never reported||OIE, 2009|
|Chile||Disease never reported||OIE, 2009|
|Colombia||Disease never reported||OIE, 2009|
|Ecuador||No information available||OIE, 2009|
|French Guiana||Disease not reported||OIE, 2009|
|Peru||No information available||OIE, 2009|
|Uruguay||No information available||OIE, 2009|
|Venezuela||No information available||OIE, 2009|
|Albania||No information available||OIE, 2009|
|Austria||No information available||OIE, 2009|
|Belarus||Disease not reported||OIE, 2009|
|Belgium||No information available||OIE, 2009|
|Bulgaria||No information available||OIE, 2009|
|Croatia||Disease never reported||OIE, 2009|
|Cyprus||Disease never reported||OIE, 2009|
|Czech Republic||Disease never reported||OIE, 2009|
|Denmark||Disease never reported||OIE, 2009|
|Estonia||No information available||OIE, 2009|
|Finland||Disease never reported||OIE, 2009|
|France||Disease not reported||OIE, 2009|
|Germany||Disease never reported||OIE, 2009|
|Greece||No information available||OIE, 2009|
|Hungary||Disease never reported||OIE, 2009|
|Iceland||Disease never reported||OIE, 2009|
|Ireland||Disease not reported||OIE, 2009|
|Italy||No information available||OIE, 2009|
|Latvia||Disease never reported||OIE, 2009|
|Liechtenstein||No information available||OIE, 2009|
|Lithuania||Disease never reported||OIE, 2009|
|Luxembourg||No information available||OIE, 2009|
|Macedonia||No information available||OIE, 2009|
|Malta||No information available||OIE, 2009|
|Montenegro||No information available||OIE, 2009|
|Netherlands||Disease never reported||OIE, 2009|
|Norway||Disease never reported||OIE, 2009|
|Poland||No information available||OIE, 2009|
|Portugal||Disease not reported||OIE, 2009|
|Romania||No information available||OIE, 2009|
|Russian Federation||No information available||OIE, 2009|
|Serbia||No information available||OIE, 2009|
|Slovakia||Disease not reported||OIE, 2009|
|Slovenia||Disease never reported||OIE, 2009|
|Spain||Disease never reported||OIE, 2009|
|Sweden||Disease never reported||OIE, 2009|
|Switzerland||Disease never reported||OIE, 2009|
|UK||Disease never reported||OIE, 2009|
|Ukraine||Disease not reported||OIE, 2009|
|-Australian Northern Territory||Present||Humphrey and Langdon, 1986; Pearce, 1990|
|-New South Wales||Present||Callinan et al., 1989|
|-Queensland||Present||McKenzie and Hall , 1976; Rodgers and Burke, 1981|
|-South Australia||Present||Rodgers and Burke, 1981|
|French Polynesia||Disease never reported||OIE, 2009|
|New Caledonia||Disease not reported||OIE, 2009|
|New Zealand||Disease never reported||OIE, 2009|
|Papua New Guinea||Present|
PathologyTop of page
Based on the investigation of the pathogenic organisms found from EUS-infected samples, a wide range of aetiologies have been attributed to EUS, such as bacteria, fungi, parasites and viruses.
Several species of parasitic protozoans (Chilodonella sp., Costia sp., Epistylis sp., Glossatella sp., Ichthyophthirius sp., Scyphidia sp., Trichodina spp.), myxosporeans (Henneguya sp. and Thelohania sp.), monogeneans and crustaceans (Lernaea sp.) have been recorded from diseased fish (Callinan et al., 1997; Reungprach et al., 1983). Nevertheless, there is no evidence to confirm that these parasites are the causative agent of the disease. Parasitic infections possibly induce stress in fish, thus predisposing them to infection (Subasinghe, 1993).
Aeromonas hydrophila, A. sobria, Pseudomonas spp. and Vibrio spp. are the species of bacteria isolated from the internal organs of EUS-infected fish (Burke and Rodgers, 1981; Llobrera and Gacutan, 1987; Tonguthai, 1985). Among these bacteria, A. hydrophila is the most commonly isolated species from the advanced stages of infected fish. It is usually not isolated from the early stage of the disease. On the other hand, A. hydrophila is known to be part of the normal microflora of fish and aquatic environments and is recognised as an opportunistic pathogen.
A number of birnaviruses, reoviruses and rhabdoviruses have been isolated from diseased snakehead and other susceptible species. These viruses most probably represent adventitious infections unrelated to EUS because of their heterogeneous nature, together with a low and non-consistent level of recovery from epizootics of disease. Therefore, the role of viruses in the aetiology of this disease remains unproven (Kanchanakarn, 1996; Roberts et al., 1994).
At least two species of fungi have been isolated from EUS-infected fish, namely, Achlya sp. which was isolated from the superficial area of the lesions (Pittchayangkula and Bodhalamik, 1983; Subasinghe et al., 1990) and Aphanomyces sp. which is normally isolated from the muscle area near the lesions (Egusa, 1992, Fraser et al., 1992; Hatai et al., 1994; Roberts et al., 1993). Recently, it has been shown that all Aphanomyces identified from EUS samples not only are the same species but also a single clonal lineage (Lilley et al., 1997). Therefore, it is confirmed that the fundamental aetiological agent of EUS is an oomycete fungus, Aphanomyces invaderis (Willoughby et al., 1995). However, the valid taxonomic name according to the International Code of Botanical Nomenclature (ICBN) of this species is A. invadans (Lilley et al., 1998). This specific pathogenic fungus showed the ability to invade the skin of EUS-infected fish (Kiryu et al., 2003). Isolation of this particular fungus is difficult as it is slow growing and most of the hyphae in the muscle are dead except for the tips that are penetrating deeper into the muscle tissue (Roberts et al., 1993)
Pathogenicity of the Fungus
After success in isolating the slow growing fungus, Aphanomyces invadans, from EUS-infected fish in various countries (Egusa, 1992; Fraser et al., 1992; Willoughby et al., 1995), pathogenicity studies were conducted. Intramuscular injection of spore suspensions into some susceptible fish species (barbs and snakehead) demonstrated a severe necrotising myogranulomatous condition at the injected site similar to the pathological feature of fish naturally infected with EUS. At the later stages, the fungus rapidly invaded the other internal organs, causing death to the host. The diameter of the hyphae of the fungus in lesions was always larger and the walls thicker than in cultured specimens (Roberts et al., 1993). Co-habitation transmission experiments with EUS-infected fish were successful (Balasuriya et al., 1990; Cruz-Lacierda and Shariff, 1995).The exposure of healthy Atlantic menhaden to suspension of zoospores of A. invadans demonstrated the germination and penetration of the germ tube through the epithelium layer of the experimental fish (Kiryu et al., 2003).
Lesions in all EUS-infected fish are similar, except that in snakehead chronic lesions can develop. This is because snakehead survive longer and the lesions are able to develop to a very advanced stage; other species die before this stage is reached.
Grossly the lesions are generally small red erosions on the body, head and fins. In the advanced stage, deep haemorrhaged ulcers spread through the whole body. Fungal mycelium is commonly found on top of the ulcerative lesions. The internal organs in the early stage of infection show only minimal inflammatory response. It is important to note that diseased fish with not too advanced lesions, kept in better water quality conditions, often recover and undergo a healing process leaving dark scars at the sites of infection.
Histopathological observation of early stage lesions reveal acute spongiosis with loss of epithelial cells. Degenerative changes are observed in the dermis, with hyperaemia, haemorrhages and inflammatory cells infiltrating between the fibres of the dermis. Inflammatory exudate and haemorrhages are also found in the hypodermis. Sarcolysis with haemorrhages and inflammatory exudate are obvious in the more advanced stage. The fungal hyphae are enclosed by a well developed epithelioid cell layer. Mycotic granulation of these non-septate fungal hyphae spreads through the infected muscle and other internal organs in the very late stages. In the advanced stage, there are no muscle fibres in the granuloma tissues. They are replaced by fibrosis, inflammatory cells and newly developing capillaries (Chinabut et al., 1995; Chinabut and Roberts, 1999). This distinct feature of the typical mycotic granulomas in the lesions of EUS-infected fish provides important histopathological information which can be used to distinguish EUS from other fish ulcerative diseases.
DiagnosisTop of page
EUS is associated with mass mortality of susceptible fish in areas that are initially affected. However, evidence from EUS-endemic areas shows that it can also occur at low intensity, with fish often recovering towards the end of the cool season. Gross pathology of EUS infected fish is similar to other cutaneous ulcerative syndromes of freshwater and estuarine fishes and it is therefore important not to rely on clinical signs as a means of diagnosis. Outbreaks in estuarine fish have been recorded only in water with salinity less than 2 ppt. The gross appearance of lesions varies between species, habitat and stage of lesion development (Callinan et al., 1989, Viswanath et al., 1997, Chinabut and Roberts, 1999). The most distinctive EUS lesion is the open dermal ulcer. This is often most conspicuous in snakehead which is often used as an "indicator species" of EUS in an area.
Rapid muscle squash
A provisional diagnosis of EUS can be made by demonstrating aseptate fungal hyphae (12-30 µm in diameter) in a squash preparation of skeletal muscle taken from beneath the surface of an ulcer.
Confirmatory diagnosis requires histopathological demonstration of typical for necrotizing mycotic granulomas using haematoxylin and eosin stain (H&E) and a general fungus stain such as Periodic Acid Schiff (PAS), Grocott's or Uvitex.
Fungus culture and characterization
Isolation and identification of Aphanomyces invadans from infected fish are reported by Fraser et al. (1992) and Willoughby and Roberts (1994). Moderate, pale, raised, dermal lesions are most suitable for fungal isolation. Remove the scales around the lesion and sear the underlying skin with a red-hot spatula to sterilize the surface. Using a sterile scalpel blade and sterile, fine pointed forceps, cut through skin underlying the seared area and then by cutting horizontally and reflecting superficial tissues, expose underlying muscle. Ensure the instruments do not contact the contaminated external surface and otherwise contaminate the underlying muscle. Using aseptic techniques, carefully excise pieces of affected muscle, approximately 2 mm3, and place them in a Petri dish containing Czapex Dox agar with penicillin G (100 units mL-1) and oxolinic acid (100 mg mL-1). Seal plates and incubate at room temperature, examining daily. Repeatedly transfer emerging hyphal tips on to fresh plates of Czapex Dox agar until cultures are free of contamination.
Lesions located on the body or tail of fish less than 20 cm in length can be sampled by cutting the fish in two using a sterile scalpel, slicing a cross-section through the fish at the edge of the lesion. Flame the scalpel until red-hot and use this to sterilize the exposed surface of the muscle. Use a small-bladed sterile scalpel to cut out a circular block of muscle (2-4 mm3) from beneath the lesion and place it in a Petri dish of GP medium (3 g L-1 glucose, 1g L-1 peptone, 0.128 g L-1 MgSO4.7H2O, 0.014 g L-1 KH2PO4, 0.029 g L-1 CaCl2.2H2O, 2.4 mg L-1 FeCl3.6H2O, 1.8 mg L-1 MnCl2.4H2O, 3.9 mg L-1 CuSO4.5H2O, 0.4 mg L-1 ZnSO4.7H2O) with 100 units mL-1 penicillin-K and 10 mg mL-1 oxolinic acid. Instruments should not contact the contaminated external surface of the fish. Incubate inoculated media at approximately 25°C and examine under a microscope (preferably an inverted microscope) within 12 hours. Repeatedly transfer emerging hyphal tips to plates of GP medium with 12 g L-1 technical agar, 100 units mL-1 penicillin-K and 10 mg mL-1 streptomycin sulfate until pure cultures are obtained. They may be maintained at 10°C on GP agar and subcultured at intervals of no greater than 7 days.
The fungus can be identified to genus by inducing sporogenesis and demonstrating typical asexual characteristics of Aphanomyces as described in Lilley et al. (1998). A. invadans is characteristically slow growing in culture and fails to grow at 37°C on GPY agar (GP broth with 0.5 g L-1 yeast extract and 12 g L-1 technical agar). Confirmation that the isolate is A. invadans can be made by injecting a 0.1 ml suspension of 100+ motile spores intramuscularly in EUS susceptible fish at 20°C, and demonstrating histologically growth of aseptate hyphae 12-30 µm in diameter in muscle of fish sampled after 7 days, and typical mycotic granulomas in muscle of fish sample after 14 days.
EpidemiologyTop of page
Cutaneous ulcerative disease, named epizootic ulcerative syndrome (EUS), has been a seasonal disease of freshwater and brackishwater fish in Asia, Australia and the United States of America since 1971. Earlier outbreaks of mycotic granulomatosis (MG) in Japan, red spot disease (RSD) in Australia and ulcerative mycosis (UM) in the United States of America are now known to be the same as EUS (Kiryu et al., 2003). EUS commonly occurs during periods of low temperature and after periods of heavy rainfall (Bondad-Reantaso et al., 1992). These conditions favour sporulation of the Aphanomyces pathogen (Lumanlan-Mayo et al., 1997) and low temperature has been shown to delay the inflammatory response of fish to fungal infection (Chinabut et al., 1995; Catap and Munday, 1998). It has been defined as "a seasonal epizootic condition of freshwater and estuarine warm water fish of complex infectious aetiology characterized by the presence of invasive Aphanomyces infection and necrotising ulcerative lesions typically leading to a granulomatous response" (Roberts et al., 1994). Recent studies suggest that a complex infectious aetiology is not necessarily involved in all cases of EUS (Callinan, 1997, Kiryu et al., 2003); and one species of invasive fungus, Aphanomyces invadans, is involved in the outbreaks. Region wide, over 100 species have been confirmed affected by histological diagnosis in Asia (Lilley et al., 1998), but some important cultured species, including Chinese carps, milkfish and tilapia, have been shown to be resistant.
ReferencesTop of page
Balasuriya KSW; Kulathilake M; Subasinghe RP, 1990. Preliminary investigations into the experimental transmission of ulcerative diseases syndrome in fish in Sri lanka. In: Hirano R, Hanyo I, eds. The 2nd Fisheries Forum. Manila, Philippines: Asian Fisheries Society, 659-662.
Blazer VS; Vogelbein WK; Densmore CL; May EB; Lilley JH; Zwerner DE, 1999. Aphanomyces as a cause of ulcerative skin lesions of menhaden from Chesapeake Bay tributaries. Journal of Aquatic Animal Health, 11(4):340-349.
Bondad-Reantaso MG; Lumanlan SC; Natividad JM; Phillips MJ, 1992. Environmental monitoring of the epizootic ulcerative syndrome (EUS) in fish from Munoz, Nueva Ecija in the Philippines. In: Shariff M, Subasinghe RP, Arthur JR, eds. Diseases in Asian Aquaculture 1. Manila, The Philippines: Fish Health Section, Asian Fisheries Society, 475-490.
Bruno DW; Wood BP, 1999. Saprolegnia and other Oomycetes. In: Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections [ed. by Woo, P. T. K.\Bruno, D. W.]. Wallingford, UK: CAB International, 599-659.
Burke JB; Rodgers LJ, 1981. Identification on pathogenic bacteria associated with the occurrence of “red spot” in sea mullet, Mugil cephalus L., in southeastern Queensland. J. Fish Dis., 4:153-159.
Callinan RB, 1986. Diseases of native Australian fishes. Diseases of Australian fish and shellfish. Proceedings of the first Australian workshop on diseases of fish and shellfish, Benalla, Victoria, Australia, 27-30 May 1985., 102-117.
Callinan RB, 1997. Pathogenesis of red spot disease (epizootic ulcerative syndrome) in estuarine fish in eastern Australia and the Philippines. PhD Thesis. Queensland, Australia: University of Queensland, 232pp.
Callinan RB; Chinabut S; Kanchanakhan S; Lilley JH; Phillips MJ, 1997. Epizootic ulcerative syndrome (EUS) of fishes in Pakistan. A report of the finding of a mission to Pakistan on 9-19 March 1997.
Callinan RB; Paclibare JO; Bondad-Reantaso MG; Chin JC; Gogolewski RP, 1995. Aphanomyces species associated with epizootic ulcerative syndrome (EUS) in the Philippines and red spot disease (RSD) in Australia: preliminary comparative studies. Diseases of Aquatic Organisms, 21(3):233-238.
Catap ES; Munday BL, 1998. Effects of variations of water temperature and dietary lipids on the expression of experimental epizootic ulcerative syndrome (EUS) in sand whiting, Sillago ciliata. Gyobyo Kenkyu = Fish Pathology, 33(4):327-335.
Catap ES; Munday BL, 1998. Haematological and non-specific immune responses in glucan-stimulated sand whiting, Sillago ciliate Cuvier, with experimentally-induced epizootic ulcerative syndrome. Poster presented at the 5th Asian Fisheries Forum, Chiang Mai, Thailand. Asian Fisheries Society and Aquatic Resources Research Institute, Chulalongkorn University.
Chinabut S; Roberts RJ, 1999. Pathology and Histopathology of Epizootic Ulcerative Syndrome (EUS). Bangkok, Thailand: Aquatic Animal Health Research Institute, Department of Fisheries, Royal Thai Government, 33 pp.
Chinabut S; Roberts RJ; Willoughby GR; Pearson MD, 1995. Histopathology of snakehead, Channa striatus (Bloch), experimentally infected with the specific Aphanomyces fungus associated with epizootic ulcerative syndrome (EUS) at different temperatures. Journal of Fish Diseases, 18(1):41-47.
Cruz-Lacierda ER; Shariff M, 1995. Experimental transmission of epizootic ulcerative syndrome (EUS) in snakehead, Ophicephalus striatus. In: Shariff M, Arthur JR, Subasinghe RP, eds. Diseases in Asian Aquaculture II. Manila, Philippines: Fish Health Section, Asian Fisheries Society, 327-336.
Dykstra MJ; Noga EJ; Levine JF; Moye DW, 1986. Characterization of the Aphanomyces species involved with ulcerative mycosis (UM) in menhaden. Mycologia, 78:664-672.
Egusa S, 1992. Mycotic granulomatosis. In: Balkema AA, ed. Infectious diseases of fish. Rotterdam, Netherlands: Brookfield Publisher, 392-396.
Egusa S; Masuda N, 1971. A new fungal disease of Plecoglossus altivelis. Fish Pathol., 6:41-46.
Hatai K, 1980. Studies on Pathogenic Agents of Saprolegniasis in Fresh Water Fishes. Special Report of the Nagasaki Prefecture Institute of Fisheries No. 8, Nagasaki, 95 pp.
Humphrey JD; Langdon JS, 1986. Report on ulcerative disease in Northern Territory Fish. Internal Report. Australian Fish Health Reference Laboratory, Benalla, 13 pp.
Hunter RE, 1975. Water moulds of the river Great Ouse and its tributaries. Transactions of the British Mycological Society, 45:519-531.
Kanchanakhan S, 1996. Epizootic ulcerative syndrome (EUS): a new look at the old story. AAHRI Newsletter, 5:2-3.
Kiryu Y; Shields JD; Vogelbein WK; Kator H; Blazer VS, 2003. Infectivity and pathogenicity of the oomycete Aphanomyces invadans in Atlantic menhaden Brevoortia tyrannus. Diseases of Aquatic Organisms, 54(2):135-146.
Lilley JH; Callinan RB; Chinabut S; Kanchanakhan S; MacRae IH; Phillips MJ, 1998. Epizootic ulcerative syndrome (EUS) technical handbook. Bangkok, Thailand: Aquatic Animal Health Research Institute.
Lilley JH; Chinabut S, 2000. DNA-based studies on Aphanomyces invadans, the fungal pathogen of epizootic ulcerative syndrome (EUS). FAO Fisheries Technical Paper, No. 395:83-87.
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