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mycobacteriosis in fish

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mycobacteriosis in fish

Summary

  • Last modified
  • 20 March 2018
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • mycobacteriosis in fish
  • Overview
  • The discovery of the tubercle bacillus by Robert Koch in 1882 stands as the most important contribution to the study of tuberculosis in any host. Before the end of the eighteenth century, piscine mycobacteria had been d...

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Pictures

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PictureTitleCaptionCopyright
Subcutaneous granuloma in Siamese fighting fish infected with Mycobacterium. x 130 (haematoxylin and eosin (H & E) stain).
TitleSubcutaneous granuloma
CaptionSubcutaneous granuloma in Siamese fighting fish infected with Mycobacterium. x 130 (haematoxylin and eosin (H & E) stain).
CopyrightS. Chinabut
Subcutaneous granuloma in Siamese fighting fish infected with Mycobacterium. x 130 (haematoxylin and eosin (H & E) stain).
Subcutaneous granulomaSubcutaneous granuloma in Siamese fighting fish infected with Mycobacterium. x 130 (haematoxylin and eosin (H & E) stain).S. Chinabut
Tubercle granuloma in snakehead fish infected with Mycobacterium: (a) gills x 130, (b) muscles x 250 and (c) brain x 500 (H & E stain).
TitleTubercle granuloma
CaptionTubercle granuloma in snakehead fish infected with Mycobacterium: (a) gills x 130, (b) muscles x 250 and (c) brain x 500 (H & E stain).
CopyrightS. Chinabut
Tubercle granuloma in snakehead fish infected with Mycobacterium: (a) gills x 130, (b) muscles x 250 and (c) brain x 500 (H & E stain).
Tubercle granulomaTubercle granuloma in snakehead fish infected with Mycobacterium: (a) gills x 130, (b) muscles x 250 and (c) brain x 500 (H & E stain).S. Chinabut
Macrophage with lipofuscin in the cytoplasm accumulating at the edge of the granuloma to form a melanomacrophage centre in an infected fish. x 500 (H & E stain).
TitleMacrophage with lipofuscin in the cytoplasm
CaptionMacrophage with lipofuscin in the cytoplasm accumulating at the edge of the granuloma to form a melanomacrophage centre in an infected fish. x 500 (H & E stain).
CopyrightS. Chinabut
Macrophage with lipofuscin in the cytoplasm accumulating at the edge of the granuloma to form a melanomacrophage centre in an infected fish. x 500 (H & E stain).
Macrophage with lipofuscin in the cytoplasmMacrophage with lipofuscin in the cytoplasm accumulating at the edge of the granuloma to form a melanomacrophage centre in an infected fish. x 500 (H & E stain).S. Chinabut
Isolation procedure for mycobacteria (Thoen and Schliesser, 1984). NaOH, sodium hydroxide.
TitleIsolation procedure for mycobacteria
CaptionIsolation procedure for mycobacteria (Thoen and Schliesser, 1984). NaOH, sodium hydroxide.
CopyrightS. Chinabut
Isolation procedure for mycobacteria (Thoen and Schliesser, 1984). NaOH, sodium hydroxide.
Isolation procedure for mycobacteriaIsolation procedure for mycobacteria (Thoen and Schliesser, 1984). NaOH, sodium hydroxide.S. Chinabut

Identity

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Preferred Scientific Name

  • mycobacteriosis in fish

International Common Names

  • English: focal tuberculosis in fish; mycobacterial infection of fish; mycobactériose; mycobacteriosis; mycobacteriosis of fish; mycobacterium infection of fish; piscine mycobacteriosis; piscine tubercle; tuberculosis in fish
  • Spanish: micobacteriosis; tuberculosis pisciaria

Local Common Names

  • Germany: mycobacteriose
  • Italy: micobatteriosi
  • Japan: mikobakuteria-sho
  • Korea, Republic of: U Kal Jhal Jung
  • Netherlands: mycobacteriose
  • Thailand: wan na rok pla

Overview

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The discovery of the tubercle bacillus by Robert Koch in 1882 stands as the most important contribution to the study of tuberculosis in any host. Before the end of the eighteenth century, piscine mycobacteria had been described by a group of French scientists (Bataillon et al., 1897). They reported that Mycobacterium piscium (a name which is now obsolete; Van Duijn, 1981) was a pathogen of diseased carp, Cyprinus carpio. Since that time, much research on mycobacterial diseases in fish has been carried out.

Von Betegh first reported mycobacteriosis in marine fish in 1910. Mycobacterium marinum was isolated and described in 1926 by Aronson as the cause of tuberculosis-like lesions in the liver, spleen and kidney of tropical coral fish kept in the Philadelphia aquarium. This organism was initially thought to infect only marine fish, but it has since been isolated from freshwater species and human beings (Barrow and Hewitt, 1971; Van Duijn, 1981). Mycobacterium fortuitum was another acid-fast bacillus repeatedly found from diseased neon tetra, Parocheirodon innesi, in 1953, although the taxonomic identification of the species was later described by Ross and Brancato (1959).

Many acid-fast bacteria have been recorded as the aetiological agents causing mycobacteriosis in fish. However, some of them were synonymous with either M. marinum, M. fortuitum or Mycobacterium chelonei and some species names were not considered valid by the International Working Group on Mycobacterial Taxonomy. These included M. piscium, Mycobacterium salmoniphilum, Mycobacterium anabanti and M. platypoecilus (Thoen and Schliesser, 1984; Dalsgaard et al, 1992). M. gordonae and M. triplex have also been reported to infect fish (Bozzeta et al, 1995; Herbst et al, 2001). Rhodes et al. (2001, 2003) isolated M. shottsii from striped bass during the mycobacteriosis outbreak in Chesapeake Bay, USA.

[Based upon material originally published in Woo PTK, Bruno DW, eds., 1999. Fish diseases and disorders, Vol. 3 Viral, bacterial and fungal infections. Wallingford, UK: CABI Publishing.]

Hosts/Species Affected

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Some 167 species of both freshwater and saltwater fish have been reported as hosts for this disease, and it has been described from a wide variety of aquarium fish (Aronson, 1926; Besse, 1949; Nigrelli and Vogel, 1963; Giavenni et al., 1980) and food fish (Alexander, 1913; Johnstone, 1913; Sutherland, 1922; Wood and Ordal, 1958; Hublou et al., 1959; Parisot and Wood, 1960; Lawhavinit et al., 1988; Chinabut et al., 1990; Hatai et al., 1993). Mycobacteriosis was reported in the freshwater prawn. Macrobrachium rosenbergii (Brook et al., 1986) and is widespread in all penaeids (Lightner, 1996). As mycobacteriosis is a subacute to chronic disease, it seems likely that fish maintained in aquaria will show a higher incidence of this disease than cultured or wild species, because aquarium fish are often kept for long periods of time compared with fish raised for commercial purposes.

Wild stocks of fish have been reported to suffer from mycobacteriosis, including cod, Gadus morhua (Alexander, 1913); halibut, Hippoglossus hippoglossus (Sutherland, 1922); striped bass, Morone saxatilis (Aronson, 1926); North-East Atlantic mackerel, Scomber scombrus (MacKenzie, 1988); and yellow perch, Perca flavescens (Daoust et al., 1989). In intensive fish culture systems, mycobacteriosis was first documented in the salmon industry of the Pacific North-West (Parisot, 1958; Wood and Ordal, 1958). Mycobacterial disease has also been recorded from pejerrey, Odonthestes bonariensis (Lawhavinit et al., 1988; Hatai et al., 1993) and snakehead fish, Channa striatus (Chinabut et al., 1990), which are both cultured in ponds.

The incidence of mycobacteriosis in aquarium fish has been reported to vary from 10 to 22% (Wolke and Stroud, 1978; Santacana et al., 1982). The prevalence of infected fish in natural populations varies from 10 to 100% (Abernethy and Lund, 1978; Sakanari et al., 1983; Hedrick et al., 1987, Lawhavinit et al., 1988; MacKenzie, 1988). There appears to be no bias towards the sex of the fish in the prevalence of mycobacteriosis, but the severity of the infection is apparently related to age (Abernethy and Lund, 1978; MacKenzie,1988).

Disease outbreaks in cultured fish appear to be related to management factors, such as, the quality and quantity of nutrient and water supplied and the stocking density. Poor management results in abnormal stress and a reduction in the normal resistance of the host.

Distribution

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Mycobacterium is ubiquitous in the water and sediment, and so mycobacteriosis in fish populations continues to be documented worldwide, and no country can claim that this long-recognized bacterial fish disease has been eradicated as a cause of illness and death. Since many fish live in close contact with soil and water during their entire lives, these environments should be considered potential sources of infection.

In intensive fishculture systems, mycobacteriosis was first documented in the salmon industry of the northwest Pacific (Parisot, 1958; Wood and Ordal, 1958).

Distribution Table

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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/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Sea Areas

Atlantic, NortheastPresentMacKenzie, 1988
Pacific, NorthwestPresent Not invasive Kent et al., 2001

Asia

IsraelPresent Not invasive Diamant et al., 2000; Ucko et al., 2002
JapanPresentHatai et al., 1993; Kusuda and Kawai, 1998
MalaysiaPresent Not invasive Anderson et al., 1987; Shamsudin et al., 1990
ThailandPresent Not invasive Chinabut et al., 1990; Somsiri et al., 1993; Somsiri and Alexandra, 1994

Africa

South AfricaPresent Not invasive Bragg et al., 1990; Mouton et al., 2001

North America

CanadaPresentPresent based on regional distribution.
-AlbertaPresent Not invasive Daoust et al., 1989
-British ColumbiaPresent Not invasive Brocklebank et al., 2003
USAPresentPresent based on regional distribution.
-ArizonaPresent Not invasive Mohney et al., 1998
-CaliforniaPresent Not invasive Sakanari et al., 1983; Hedrick et al., 1987
-FloridaPresent Not invasive Herbst et al., 2001
-MarylandPresent Not invasive Vogelbein et al., 1999; Heckert et al., 2001
-MontanaPresent Not invasive Peterson, 2000
-New YorkPresent Not invasive Ross and Brancato, 1959
-OregonPresent Not invasive Kent et al., 2001
-VirginiaPresent Not invasive Hughes and Smith, 2002; Kaattari et al., 2002; Rhodes et al., 2004
-WashingtonPresent Not invasive Abernethy and Lund, 1978; Raymond et al., 2000

South America

BrazilPresentPresent based on regional distribution.
-Sao PauloPresentRanzani-Paiva et al., 2004
VenezuelaPresent Not invasive Clavijo et al., 1999; Conroy and Conroy, 1999

Europe

Czech RepublicPresent Not invasive Navrátil et al., 2000; Lescenko et al., 2003
DenmarkPresentDalsgaard et al., 1992
FrancePresent Not invasive Bataillon et al., 1897; Kent et al., 2002; Abalain-Colloc et al., 2003
ItalyPresent Not invasive Greco and Bozzetta, 1997; Prearo et al., 2004
PortugalPresent Not invasive Santos et al., 2003
SpainPresent Not invasive Gómez et al., 1996; Gómez, 2001

Oceania

AustraliaPresent Not invasive Bruno et al., 1998; Tappin, 2000

Pathology

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Gross Pathology

The gross signs of infection include an enlargement and softening of spleen, kidney and liver. Sometimes a number of greyish-white nodules are seen peppered throughout these organs. In severe cases, almost all the visceral organs are swollen and fused by whitish membranes around the mesenteries, and fluid accumulates in the peritoneal cavity.

Histopathology

Mycobacteriosis lesions in fish are normally localized in the skin and internal organs and consist of nodular structures with characteristic focal granulomas. These are composed of centrally located epithelioid cells and macrophages. The sizes of the granulomas vary from 80 to 500 mm (Sakanari et al., 1983). The condition of mycobacteriosis can be divided into sub acute and chronic forms (Wolke and Stroud, 1978). In the sub acute form, there is a diffuse distribution of reticuloendothelial cells and macrophages, with large caseous necrotic areas. Acid-fast bacilli are found scattered among the reticuloendothelial cells and within the cytoplasm of phagocytic macrophages. The chronic proliferative form is characterized by the production of both hard and soft granulomas. Soft granulomas have four distinguishable layers. In the centre is an area of caseous necrosis, with or without nuclear debris, surrounded by a layer of spindle-shaped epithelioid cells. The third layer contains highly eosinophilic, flattened, epithelioid cells. The outermost layer is composed of fine fibrous connective tissue encircling to form a thin capsule. Hard granulomas are composed of epithelioid cells encapsulated by fibrous connective tissue. The layer of epithelioid cells closest to the zone of caseation and fibrous capsule may not be seen in all granulomas. Noga et al. (1989) have indicated that cells participating in the chronic inflammatory response to mycobacteria may not be derived from mononuclear phagocytes. As the true classification of these cells is now uncertain, they proposed the name chronic inflammatory foci (CIF), instead of tubercle granuloma.

Calcification in the caseous necrotic centre occurs in more chronic infections (Majeed et al., 1981; Van Duijn, 1981; Anderson et al., 1987). Melanization and vacuolation may be found surrounding the cutaneous granulomas (Noga et al., 1990). Such granulomas are all of the soft tubercle type, occurring in the stratum spongiosum of the dermis (Anderson et al., 1987). Melanomacrophage centres were found close to the granulomas in the spleen and kidney of infected fish. The presence of giant cells is not typical in piscine mycobacteriosis (Wolke and Stroud, 1978; Anderson et al., 1987). However, they may be found at the early stage of the granulomatous formation (Timur and Roberts, 1977).

At the early stages in the development of the disease, the spleen, kidney and liver are the primary target organs for infection. In severe cases, a number of granulomas spread to almost all the visceral organs and some of them fuse to form a large granuloma enclosed by loose connective tissue (Giavenni et al., 1980). Acid-fast bacilli have been seen occasionally in the caseous necrotic centre and in the cytoplasm of the surrounding epithelioid cells and macrophages. These bacilli may also be found free within the swim-bladder lumen or within the cytoplasm of sloughed epithelial cells (Anderson et al., 1987).

Diagnosis

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Diagnosis of mycobacteriosis depends on clinical and histological signs and identification of the bacterial pathogen. Mycobacteriosis in fish is normally localized in the skin and internal organs and appears as nodular structures with a typical granulomatous pattern. Smears from scrapings of the cut surface of spleen and kidney tissues should be made and stained with the Kinyoun modification of the Ziehl-Neelsen stain. The smears should be air-dried. The stained slides are examined with an ordinary light microscope for the presence of acid-fast bacilli, which appear as coccoidal or bacillary rods, 1-3 mm in length. Fluorescing dyes, such as auramine or rhodamine, are recommended with either blue or ultraviolet and a microscope equipped with special filters. Acid-fast bacilli are seen as short, yellow-fluorescing rods. An immunocytochemical method using the avidin-biotin complex (ABC) was recommended by Gomez et al. (1993) to demonstrate the small number of mycobacteria in the section of affected tissues. More recently, Puttinaowarat et al. (2000) described the detection and identification of M. marinum in formalin fixed fish samples by immunohistochemistry using a monoclonal antibody as a specific probe.

A specific diagnosis of mycobacterial infection requires the isolation and identification of the organisms from skin lesions, spleen or kidney. The procedures for isolating mycobacteria are the same as those used for other bacteria. Specimens must be treated to kill contaminants.

Enzyme-linked immunosorbent assays (ELISAs) have been developed for detecting mycobacterial antigens in exotic animals (Thoen et al., 1980). Monoclonal antibodies to aquatic Mycobacterium have been developed to be used in ELISA for diagnosis of mycobacteriosis (Adams et al., 1995; 1996; Puttinaowarat et al., 2000). Blackwell (1998) also reported the use of monoclonal antibodies against M. marinum to identify the pathogen by ELISA and western blot. Serology is not only useful for diagnosis, but is also used in taxonomy (Tsang et al., 1984; Arakawa et al., 1986).

Clinical Diagnosis

Piscine mycobacteriosis is a slowly developing chronic disease, which may take 2 or more years for the number of organisms to grow to readily detectable numbers (Ashburner, 1977). Most species of fish may manifest few or no external signs of disease. However, in advanced stages, emaciation, cachexia, exophthalmia, lordosis, haemorrhagic and dermal ulcerative lesions or loss of scales may be observed. Other signs of infection can be seen in the gills, which are paler than normal and show thickened areas on some filaments. Small lesions may be observed around the mouth and vent. Changes in cutaneous pigmentation include a fading of normal colour in aquarium fish (Snieszko, 1978) and a bright coloration in salmonids (Ross, 1970). Affected fish generally exhibit lethargic behaviour, floating impassively on the surface of the water, with concurrent loss of appetite.

Infected crustaceans show various clinical signs including melanised lesions in muscle, ovary, gill and heart as well as raised melanised lesions in/on the cuticle (Lightner, 1996).

Differential Diagnosis

DNA-based methods have been employed to classify and diagnose the mycobacteria infection. Polymerase chain reaction (PCR) is one of the most popular methods with various DNA targets including 16s rDNA, internal transcribed spacer (ITS) rDNA, hsp65 gene, and super oxide dismutase gene (Knibb et al., 1993; Zolog and Philippi-Schulz, 1994; Talaat et al., 1997; Puttinaowarat et al., 2002; Ucko et al., 2002; Whipps et al., 2003). In situ hybridization is a useful method to identify the pathogen in the achieved samples (Arnoldi et al., 1992; McNicol and Farquharson, 1997). Physicochemical methods have also been reported. Pyrolysis mass spectrometry (PyMS), one such approach, is a versatile method for mycobacteria identification and characterization as it is a rapid and accurate method requiring little samples (Sisson et al., 1992; Freeman et al., 1993; Puttinaowarat et al., 1999).


List of Standard Diagnostic Tests and the Range of Results.



MethodScreeningPresumptiveConfirmatory
Clinical signs++-
Bacteriology++++++
Histopathology+++++
Antibodies-based methods+++++++
DNA probes- in situ hybridisation-++++
PCR-++++++

- the method is presently unavailable or unsuitable; + the method has application in some situation but cost, accuracy or other factors severely limits; ++ the method is a standard method with good diagnostic sensitivity and specificity; +++ the method is the recommended method for reasons of availability, specificity and sensitivity.

List of Symptoms/Signs

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SignLife StagesType
Finfish / Build up of bloody fluids - Body Cavity and Muscle Aquatic:Adult Sign
Finfish / Cessation of feeding - Behavioural Signs Aquatic:Adult Sign
Finfish / Cysts - Gills Aquatic:Adult Sign
Finfish / Cysts (clumps of white spheres) - Body Cavity and Muscle Aquatic:Adult Sign
Finfish / Fish swimming near surface - Behavioural Signs Aquatic:Adult Sign
Finfish / Generalised lethargy - Behavioural Signs Aquatic:Adult Sign
Finfish / Haemorrhagic lesions - Skin and Fins Aquatic:Adult Sign
Finfish / Paleness - Gills Aquatic:Adult Sign
Finfish / Scale loss - Skin and Fins Aquatic:Adult Sign
Finfish / Skin erosion - Skin and Fins Aquatic:Adult Sign
Finfish / Swelling - Organs Aquatic:Adult Sign
Finfish / White-grey patches (necrosis / tissue damage) - Organs Aquatic:Adult Sign

Disease Course

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The condition of mycobacteriosis can be divided into sub acute and chronic forms (Wolke and Stroud, 1978). The chronic proliferative form is characterized by the production of both hard and soft granulomas.

At the early stages in the development of the disease, the spleen, kidney and liver are the primary target organs for infection. In severe cases, a number of granulomas spread to almost all the visceral organs and some of them fuse to form a large granuloma enclosed by loose connective tissue (Giavenni et al., 1980).

Epidemiology

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Fish may be infected by ingesting feed and water contaminated with faecal material, urine or exudates from diseased animals that contain mycobacteria (Ross and Johnson, 1962). Dos Santos et al. (2003) suggested the contaminated inlet water was one of the most plausible sources of infection occurring in the fish farm. The sources and modes of transmission of mycobacterial infections in fish may be related to the infection of invertebrates, such as arthropods (Beerwerth et al., 1979), freshwater snails (Michelson, 1961) or freshwater prawns (Brook et al., 1986). The entry of mycobacteria through skin and gill lesions caused by injury or parasitic infection should also be considered. After the organisms enter the body they may cause skin lesions or spread to other organs through the circulatory or lymphatic system. Malnutrition was also suggested to be a cause of the mycobacterial infection (Belas et al., 1995).

Some scientists have tried to prove that Mycobacterium tuberculosis excreted from human patients may transform to cause disease in cold-blooded animals. However, it is now clear that such transformations do not occur (Thoen and Schliesser, 1984).

The observation of mycobacteria in the piscine ova and tubercle granulomas in the ovary wall suggests that transovarian transmission is a definite possibility. Johnstone (1913) reported that the ova of infected fish were small and markedly undeveloped and contained numerous acid-fast bacteria. A report from an Australian fish hatchery has provided the evidence that Mycobacterium can be introduced by eggs and transmitted to the F1 generation (Ashburner, 1977). However, this observation does not confirm that ovarian transmission takes place, as the egg surface may be contaminated by peritoneal fluid containing mycobacteria (Conroy, 1964a). Recently, Chinabut et al. (1994) confirmed the transmission of mycobacteria in Siamese fighting fish, Betta splendens, via transovarian passage. Acid-fast bacteria were found in the ova of diseased female Siamese fighting fish, using the fluorochrome technique.

Vectors

There are many vectors of mycobacteriosis pathogens, including crustaceans and molluscs.

Impact Summary

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CategoryImpact
Animal/plant collections Negative
Animal/plant products Negative
Crop production Negative
Fisheries / aquaculture Negative
Human health Negative
Livestock production Negative
Rare/protected species Negative
Trade/international relations Negative

Impact: Economic

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Parisot and Wood (1960) reported that infections in some wild fish populations might be as high as 15%, whereas Smith (1996) reported that infections in fish populations in intensive culture may reach 100%. Giavenni and Finazzi (1980) examined approximately 300 marine and freshwater tropical fish for mycobacteriosis and found that the mortality rate amongst these fish was between 5-10%. Striped bass (Morone saxatilis) raised in California, USA were infected with Mycobacetium marinum resulting in 50% losses of 900 yearlings and most of those survivors remained with a chronic condition (Hedrick et al., 1987).

Snakehead (Channa striatus), a valuable freshwater farmed fish in Thailand, can have a mortality rate for this disease as high as 20%. Fish infected with mycobacteriosis, particularly food fish, are of no market value as they are unfit for human consumption. Smith (1996) reported that companies raising striped bass in the USA have condemned several million dollars worth of fish over the past few years due to mycobacterial infections. Colorni (1992) also described mycobacteriosis outbreaks in cultured sea bass (Dicentrarchus labrax) in Israel, and reported a 100% prevalence of Mycobacterium infection with mortality over 50%.

Mycobacterisis is rather common in the ornamental fish industry as a number of ornamental fish species are reported as being susceptible to the disease (Nigrelli and Vogel, 1963). For instance, Siamese fighting fish (Betta splendens), an economically important fish for export from Thailand, is one species particularly susceptible to Mycobacterium infections (Adams et al., 1995). The mortality could be higher than 30% during the disease outbreak.

Zoonoses and Food Safety

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An important aspect of fish mycobacteriosis is that some of the causative mycobacteria also cause skin disease in humans. Human infection with M. marinum and M. fortuitum has been widely reported. Mycobacterium marinum infections in humans have been known since 1951 and have been described in some temperate and tropical countries, such as Sweden, the Netherlands, Belgium, the UK (Pattyn, 1984), Canada (Brown et al., 1977), the USA (Mollohan and Romer, 1961) and Thailand (Bovornkitti et al., 1991). These outbreaks were associated with cutaneous abrasions and exposure to swimming pool water contaminated with M. marinum. Allergic dermatopathies have also been reported on the skin of aquarists handling water in which affected fish have been reared (Barrow and Hewitt, 1971; Giavenni et al., 1980; Huminer et al., 1986; Kullavanijaya et al., 1993). It has been recently reported that Mycobacterium fortuitum and M. chelonae were isolated from frozen fish destined for human consumption (Mediel et al., 2000). This report suggests a potential hazard for transmission of the bacterium via this route.

The rapidly growing M. fortuitum has been cultured from patients with pulmonary disease and local abscesses (Cruz, 1938). Mycobacterium chelonei has been isolated from heterograph heart-valve transplants, and lesions have also been found in synovial fluid and muscle (Blacklock and Dawson, 1979; Thoen and Schliesser, 1984).

References

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Abalain-Colloc ML, Guillerm D, Saläun M, Gouriou S, Vincent V, Picard B, 2003. Mycobacterium szulgai isolated from a patient, a tropical fish and aquarium water. European Journal of Clinical Microbiology & Infectious Diseases, 22(12):768-769.

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Adams A, Thompson KD, McEwan H, Chen SC, Richards RH, 1996. Development of monoclonal antibodies to Mycobacterium spp. isolated from chevron snakeheads and Siamese fightingfish. Journal of Aquatic Animal Health, 8(3):208-215.

Adams A, Thompson KD, Morris D, Farias C, Chen ShiChu, 1995. Development and use of monoclonal antibody probes for immunohistochemistry, ELISA and IFAT to detect bacterial and parasitic fish pathogens. Fish & Shellfish Immunology, 5(8):537-547.

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Anderson IG, Shariff M, Shamsudin MN, 1987. Ornamental fish mycobacteriosis in Malaysia. Kajian Veterinar, 19(1):61-70.

Arakawa CK, Fryer JL, 1984. Isolation and characterization of a new subspecies of Mycobacterium chelonei infectious for salmonid fish. Helgoländer Meeresuntersuchungen, 37(1/4):329-342.

Arakawa CK, Fryer JL, Sanders JE, 1986. Serology of Mycobacterium chelonei isolated from salmonid fish. Journal of Fish Diseases, 9(3):269-271.

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Aronson JD, 1926. Spontaneous tuberculosis in salt water fish. Journal of Infectious Diseases, 39:315-320.

Ashburner LD, 1977. Mycobacteriosis in hatchery-confined chinook salmon (Oncorhynchus tshawytscua Walbaum) in Australia. Journal of Fish Biology, 10(6):523-528; [2 pl.].

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Barrow GPI, Hewitt M, 1971. Skin infections with Mycobacterium maximum from a tropical fish tank. British Medical Journal, 2:505-506.

Bartos JM, Sommer CV, 1981. In vivo cell mediated immune response to M. tuberculosis and M. salmoniphilum in rainbow trout (Salmo gairdneri). Developmental and Comparative Immunology, 5(1):75-83.

Bataillon E, Dubard L, Terre L, 1897. Un nouveau type de tuberculose. Comptes rendus des Séances de la Société de Biologie, 49:446-449.

Bataillon E, Moeller A, Terre L, 1902. Uber die Identitat des Bacillus des Karpfens und des Bacillus des Blinddsschleuche. Zentralblatt für Tuberkulose, 3:467-468.

Beerwerth W, Eysing B, Kessel U, 1979. Mycobacteria in arthropods of different biotypes. Zentralblatt für Bakteriologie, Parasitenkunde, Infections-Krankheiten und Hygine. I. Originale, 244:50-57.

Belas R, Faloon P, Hannaford A, 1995. Potential applications of molecular biology to the study of fish mycobacteriosis. Annual Review of Fish Diseases, 5:133-173.

Besse P, 1949. Epizootie a bacilles acido-resistants chez les poissons exotiques. Bulletin de l’Academie Veterinaire de France, 23:151-154.

Blacklock ZM, Dawson DJ, 1979. Atypical mycobacteria causing nonpulmonary disease in Queenland. Pathology, 11:283-288.

Blackwell V, 1998. Zoonotic tuberculosis. Fish Veterinary Journal, No. 2:57-60; [presented at the winter meeting of the Fish Veterinary Society, Royal College of Veterinary Surgeons, London, 28 November 1997.].

Boos S, Schmidt H, Ritter G, Manz D, 1995. Efficacy of oral rifampicin against mycobacteriosis of ornamental fish. Berliner und Münchener Tierärztliche Wochenschrift, 108(7):253-255; 6 ref.

Boudinot P, Blanco M, Kinkelin Pde, Benmansour A, 1998. Combined DNA immunization with the glycoprotein gene of viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific response in rainbow trout. Virology (New York), 249(2):297-306.

Bovornkitti S, Pushpakorn R, Nana A, Charoenratanakul S, 1991. Dissertation of reported cases of nontuberculous mycobacteriosis in Thailand. (English abstract.) Siriraj Hospital Gazette, 43:392-396.

Bozzetta E, Prearo M, Penati V, Pungkachonboon T, Ghittino C, 1995. Isolation and typing of mycobacteria in cultured tropical fish. Bulletin Society Italy Pathology Ittica, 7:13-21.

Bragg RR, Huchzermeyer HFAK, Hanisch MAM, 1990. Mycobacterium fortuitum isolated from three species of fish in South Africa. Onderstepoort Journal of Veterinary Research, 57(1):101-102.

Brocklebank J, Raverty S, Robinson J, 2003. Mycobacteriosis in Atlantic salmon farmed in British Columbia. Canadian Veterinary Journal, 44(6):486-489.

Brook JA, Nakagawa LK, Shimojo RJ, 1986. Infection of a cultured freshwater prawn, Macrobrachium rosenbergii de Man (Crustacea: Decapoda), by Mycobacterium spp., Runyon Group II. Journal of Fish Diseases, 9:319-324.

Brown J, Kelm M, Bryan LE, 1977. Infection of the skin by Mycobacterium marinum. Report of five cases. Canadian Medical Association Journal, 177:912-914.

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