Documente Academic
Documente Profesional
Documente Cultură
S. Chinabut
Aquatic Animal Health Research Institute, Department of Fisheries, Kasetsart
University Campus, Jatujak 10900, Bangkok, Thailand.
MYCOBACTERIOSIS
History
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, Myco-
bacterium salmoniphilum and Mycobacterium anabanti (Thoen and
Schliesser, 1984).
Clinical signs
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
Mycobacteriosis and Nocardiosis 321
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 (Fig. 9.1) and
internal organs (Fig. 9.2.) and consist of nodular structures with characteristic
Fig. 9.1. Subcutaneous granuloma in Siamese fighting fish infected with Mycobacterium. × 130
(haematoxylin and eosin (H & E) stain).
322 S. Chinabut
(a)
(b)
Fig. 9.2. (and Opposite) Tubercle granuloma in snakehead fish infected with Mycobacterium: (a)
gills × 130, (b) muscles × 250 and (c) brain × 500 (H & E stain).
Mycobacteriosis and Nocardiosis 323
(c)
focal granulomas. These are composed of centrally located epithelioid cells and
macrophages. The size of the granulomas vary from 80 to 500 µm (Sakanari et
al., 1983). The condition of mycobacteriosis can be divided into subacute and
chronic forms (Wolke and Stroud, 1978). In the subacute form, there is a diffuse
distribution of reticuloendothelial cells and macrophages (Fig. 9.3), 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
324 S. Chinabut
Fig. 9.3. Macrophage with lipofuscin in the cytoplasm accumulating at the edge of the
granuloma to form a melanomacrophage centre in an infected fish. × 500 (H & E stain).
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).
Media References
Bacto–Lowenstein medium (BLM) Anderson et al., 1987
Shamsudin et al., 1990
Dubos agar Abernethy and Lund, 1978
Dorset’s egg agar MacKenzie, 1988
Dubos blood agar Giavenni et al., 1980
Harold’s egg medium Wolke and Stroud, 1978
International Union against
Tuberculosis Medium (IUTM) medium Giavenni et al., 1980
Lowenstein–Jensen medium MacKenzie, 1988
MacConkey agar Shively et al., 1981
Arakawa and Fryer, 1984
Middlebrook 7H10 agar Giavenni et al., 1980
Mycobacteria 7H11 agar MacKenzie, 1988
Ogawa egg medium Shamsudin et al., 1990
Petrignani’s medium Hedrick et al., 1987
Petroff egg agar Giavenni et al., 1980
Potassium-tellurite agar Arakawa and Fryer, 1984
Diagnostic methods
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 µm 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.
A specific diagnosis of mycobacterial infection requires the isolation and
identification of the organisms from skin lesions, spleen or kidney. The pro-
cedures for isolating mycobacteria are the same as those used for other bacteria.
Specimens must be treated to kill contaminants, as indicated in Fig. 9.4.
Enzyme-linked immunosorbent assays (ELISAs) have been developed for
detecting mycobacterial antigens in exotic animals (Thoen et al., 1980) but not
fish.
Fig. 9.4. Isolation procedure for mycobacteria (Thoen and Schliesser, 1984). NaOH, sodium
hydroxide.
Public health
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).
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).
NOCARDIOSIS
Nocardiosis is a disease of both salt-water and freshwater fish caused by
actinomycetes of the genus Nocardia. Cases of piscine Nocardia are not as
widely reported as mycobacteriosis in fish. Some nocardial infections in fish
may be misinterpreted as mycobacterial disease, as they both result in similar
clinical signs and gross pathology. Nocardia asteroides, described by Eppinger
in 1891, is considered the type species of the genus (Gordon and Mihm, 1962).
Nocardia farcinica had been formerly regarded as the type species, but this was
changed due to the absence of an authentic strain in any culture collection and
the paucity of references to N. farcinica in the literature. The first case of fish
nocardiosis caused by N. asteroides was reported in neon tetra, Hyphessobrycon
innesi (Valdez and Conroy, 1962).
332 S. Chinabut
Pathology
Nocardiosis is a systemic chronic granulomatous disease of fish caused by
several species of the bacterium Nocardia. Severe emaciation, inactivity and
skin discoloration are the clinical signs of this disease. In advanced stages,
cachexia, ascites, dermal ulceration, focal necrotic areas within skeletal muscle
and pale areas in the swollen kidney, spleen, heart and liver may be observed
(Kubota et al., 1968). The appearance of small nodules on the gills of infected
yellowtails has been reported (Kusuda et al., 1974).
Histopathological examinations of infected organs have revealed character-
istic granulomas, each with a centre of necrotic material, a peripheral cellular
zone of numerous histiocytes, lymphocytes and a few multinucleated giant cells,
all of which are partially circumscribed by a fibrous capsule. Engelhardt (1987)
noted that colonies of weakly acid-fast bacteria were present within and at the
periphery of several granulomas. Hsu et al. (1987) observed numerous
disseminated abscesses, encapsulated by granulation tissue, in the pleura and
viscera of infected Formosa snakehead fish.
Diagnostic methods
As already mentioned, nocardiosis may be misdiagnosed as mycobacteriosis,
because of the similarity between the clinical signs and gross pathology
associated with the two diseases. Positive differentiation can only be made by
isolation and identification of the causative agent. In addition, histological
sections of the infected organs should be examined. Nocardioform bacteria can
grow on similar kinds of media to mycobacteria. After 24 h of growth on nutrient
agar, typical colonies of Nocardia are seen. These are raised, folded, granular or
powdery, 1–4 mm in diameter, yellow or tan, and with aerial mycelium around
the edges (Engelhardt, 1987). Nocardial granulomas without the epithelioid cells
in the earliest stages of development are easily confused with piscine
mycobacteriosis. Furthermore, while acid-fast organisms are present in the
Nocardia lesion, they only show a positive reaction for Nocardia with Fite–
Faraco acid-fast stain. Morphologically, Nocardia appear filamentous, branched
and beaded and are 5–50 µm long, while mycobacteria are usually 1–3 µm in
length (Wolke and Stroud, 1978).
Production of
Catalase v +
H2 S – +
Indole . –
Oxidase – –
Nitrate reduction + +
Degradation of
Casein – –
Gelatin – –
Hypoxanthine (weak) – +
Starch . +
Tyrosine (weak) – +
Urea (weak) + –
Xanthine – –
Utilization of
Adonitol – –
Arabinose – –
Cellobiose – –
Dextrin v –
Dulcitol v –
Fructose + +
Glucose + +
Glycerol + v
Glycogen – –
Inositol – –
Inulin – –
Lactose – –
Maltose v –
Mannose + v
Rhamnose v –
Salicin – –
Sodium acetate + +
Sodium benzoate – –
Sodium citrate – +
Sodium lactate + +
Sodium malate + +
Mycobacteriosis and Nocardiosis 335
Sodium malonate – v
Sodium propionate + +
Sodium pyruvate + +
Sodium tartrate – v
Sorbitol – –
Starch – –
Trehalose v –
Xylose – –
v, variable result; ., not determined; H2S, hydrogen sulphide.
REFERENCES
Abernethy, C.S. and Lund, J.E. (1978) Mycobacteriosis in mountain whitefish
(Prosopium williamsoni) from the Yakima River, Washington. Journal of Wildlife
Diseases 14, 333–336.
Alexander, D.M. (1913) A review of piscine tubercle, with a description of an acid-fast
bacillus found in the cod. Transactions of the Liverpool Biology Society 27, 219–
226.
336 S. Chinabut
Anderson, I.G., Shariff, M. and Shamsudin, M.N. (1987) Ornamental fish myco-
bacteriosis in Malaysia. Kajian Veterinar 19(1), 61–70.
Arakawa, C.K. and Fryer, J.L. (1984) Isolation and characterization of a new subspecies
of Mycobacterium chelonei infections for salmonid fish. Helgolander Meeres-
untersuchungen 37, 329–342.
Aronson, J.D. (1926) Spontaneous tuberculosis in salt water fish. Journal of Infectious
Diseases 39, 315–320.
Ashburner, L.D. (1977) Mycobacteriosis in hatchery-confined chinook salmon
(Oncorhynchus tshawytscba Walbaum) in Australia. Journal of Fish Biology 10,
523–528.
Austin, B. and Austin, D.A. (1987) Bacterial Fish Pathogens: Disease in Farmed and
Wild Fish. Ellis Horwood Ltd, Chichester, pp. 61–67.
Backman, S., Ferguson, H.W., Prescott, J.F. and Wilcock, B.P. (1990) Progressive
panopthalmitis in chinook salmon, Oncorhynchus tshawytscba (Walbaum): a case
report. Journal of Fish Diseases 13, 345–353.
Barrow, G.P.I. and Hewitt, M. (1971) Skin infections with Mycobacterium maximum
from a tropical fish tank. British Medical Journal 2, 505–506.
Bartos, J.M. and Sommer, C.V. (1981) In vivo cell mediated immune response to M.
tuberculosis and M. salmoniphilum in rainbow trout (Salmo gairdneri). Develop-
mental and Comparative Immununology 5, 75–83.
Bataillon, E., Dubard, L. and Terre, L. (1897) Un nouveau type de tuberculose. Comptes
rendus des Séances de la Société de Biologie 49, 446–449.
Beaman, B.L., Moring, S.E. and Ioneda, T. (1988) Effect of growth stage on mycolic
acid structure in cell walls of Nocardia asteroides GUH-2. Journal of Bacteriology
170, 1137–1142.
Beerwerth, W., Eysing, B. and Kessel, U. (1979) Mycobacteria in arthropods of different
biotypes. Zentralblatt für Bakteriologie, Parasitenkunde, Infections-Krankheiten
und Hygine. I. Originale 244, 50–57.
Besse, P. (1949) Epizootie a bacilles acido-resistants chez les poissons exotiques.
Bulletin de l’Academie Veterinaire de France 23, 151–154.
Blacklock, Z.M. and Dawson, D.J. (1979) Atypical mycobacteria causing non-
pulmonary disease in Queenland. Pathology 11, 283–288.
Bovornkitti, S., Pushpakorn, R., Nana, A. and Charoenratanakul, S. (1991) Dissertation
of reported cases of nontuberculous mycobacteriosis in Thailand. (English
abstract.) Siriraj Hospital Gazette 43, 392–396.
Brook, J.A., Nakagawa, L.K. and Shimojo, R.J. (1986) Infection of a cultured freshwater
prawn, Macrobrachium rosenbergii de Man (Crustacea: Decapoda), by Myco-
bacterium spp., Runyon Group II. Journal of Fish Diseases 9, 319–324.
Brown, J., Kelm, M. and Bryan, L.E. (1977) Infection of the skin by Mycobacterium
marinum. Report of five cases. Canandian Medical Association Journal 177, 912–914.
Campbell, G. and MacKelvie, R.M. (1968) Infection of brook trout (Salvelinus
fontinalis) by nocardiae. Journal of the Fisheries Research Board of Canada 25,
423–425.
Chakrabarty, A.N. and Dastidar, S.G. (1991) Reported isolation of chemoautotrophic
nocardioform bacteria from fish epizootic ulcerative syndrome. Indian Journal of
Experimental Biology 29, 623–627.
Chinabut, S., Limsuwan, C. and Chanratchakool, P. (1990) Mycobacteriosis in the
snakehead, Channa striatus (Fowler). Journal of Fish Diseases 13, 513–535.
Chinabut, S., Kanayati, Y. and Pungkachonboon, T. (1994) Study of transovarian
transmission of mycobacteria in Betta splendens Regan. In: Chou, L.M., Munro,
A.D., Lam, T.J., Chen, T.W., Cheong, L.K.K., Ding, J.K., Hooi, K.K., Khoo, H.W.,
Mycobacteriosis and Nocardiosis 337
Phang, V.P.E., Shim, K.F. and Tan, C.H. (eds) Proceedings of the Third Asian
Fisheries Forum. Asian Fisheries Society, Manila, Philippines. pp. 339–341.
Conroy, D.A. (1964a) Notes on the incidence of piscine tuberculosis in Argentina.
Progressive Fish Culturist 26, 89–90.
Conroy, D.A. (1964b) Nocardiosis as a disease of tropical fish. Veterinary Record 76,
676.
Cruz, J.C. (1938) Mycobacterium fortuitum um Novo Bacilo Acidoresistente Patogenico
para o Homen. Acta Medical Rio de Janeiro 1, 297.
Daoust, P.Y., Larson, B.E. and Johnson, G.R. (1989) Mycobacteriosis in yellow perch
(Perca flavescens) from two lakes in Alberta. Journal of Wildlife Diseases 25, 31–
37.
Dulin, M.P. (1979) A review of tuberculosis (mycobacteriosis) in fish. Veterinary
Medicine and Small Animal Clinician 74, 731–735.
Engelhardt, J.A. (1987) Abdominal swelling in a gourami. Laboratory Animals 13–14.
Eppinger, H. (1891) Uber eine neue pathogene Cladothrix und eine durch sie
hervorgerufene pseudotuberculosis. Beitrage zur Pathologischen Anatomie und
Allgemeinon Pathologie 9, 287–328.
Ghittino, P. (1972) The principal aspects of bacterial fish diseases in Italy. Symposium of
the Zoological Society London 30, 25–28.
Giavenni, R., Finazzi, M., Poli, G. and Grimaldi, C.N.R. (1980) Tuberculosis in marine
tropical fishes in an aquarium. Journal of Wildlife Diseases 16, 161–167.
Gomez, S., Bernabe, A., Gomez, M.A., Navarro, J.A. and Sanchez, J. (1993) Fish
mycobacteriosis: morphopathological and immunocytochemical aspects. Journal
of Fish Diseases 16, 137–141.
Goodfellow, M. (1971) Numerical taxonomy of some nocardioform bacteria. Journal of
General Microbiology 69, 33–80.
Goodfellow, M. and Orchard, V.A. (1974) Antibiotic sensitivity of some nocardioform
bacteria and its values as a criterion for taxonomy. Journal of General Microbiology
83, 375–387.
Gordon, R.E. (1966) Some strains in search of a genus, Corynebacterium, Myco-
bacterium, Nocardia or what? Journal of General Microbiology 40, 329–343.
Gordon, R.E. and Mihm, J.M. (1962) The type species of the genus Nocardia. Journal of
General Microbiology 27, 1–10.
Hatai, K., Lawhavinit, O., Kubota, S.S., Toda, K. and Suzuki, N. (1988) Pathogenicity of
Mycobacterium sp. isolated from pejerrey, Odonthestes bonariensis. Fish
Pathology 23, 155–159.
Hatai, K. Lawhavinit, O., Toda, K. and Sugou, Y. (1993) Mycobacterium infection in
pejerrey, Odonthestes bonariensis Cuvier & Valenciennes. Journal of Fish Diseases
16, 397–402.
Hedrick, R.P., McDowell, T. and Groff, J. (1987) Mycobacteriosis in cultured striped
bass from California. Journal of Wildlife Diseases 23, 391–395.
Hsu, F.S., Chu, H.M. and Weng, C.N. (1987) An enzootic of nocardiosis in fish. The
Memoirs of Parasitology in Fish Disease 2, 16–21.
Hublou, W.L., Wallis, J., McKee, T.B., Law, D.K., Sinnhuber, R.O. and Yu, T.C. (1959)
Development of the Oregon pellet diet. Research Briefs, Fish Committee/Oregon 7,
28–56.
Huminer, D., Pitlik, S.D., Block, C., Kaufman L., Amit S. and Rosenfeld, J.R. (1986).
Aquarium-borne Mycobacterium marinum skin infection. Archives of Dermatology
122, 698–703.
Johnstone, J. (1913) Diseased conditions of fishes. Report of the Lancashire Sea Fish
Laboratory 21, 20–25.
338 S. Chinabut
Koch, R. (1882) Die Aetiologie der Tuberculose. Berliner Klinische Wochenschrift 19,
221–230.
Kubota, S., Kariya, T., Nakamura, Y. and Kira, K. (1968) Nocardial infection in cultured
yellowtails (Seriola quinqueradiata and S. purpurascens). II. Histological study.
Fish Pathology 3, 24–33.
Kudo, T., Hatai, K. and Seino, A. (1988) Nocardia seriolae sp. nov. causing nocardiosis
of cultured fish. International Journal of Systematic Bacteriology 38, 173–178.
Kullavanijaya, P., Sirimachan, S. and Bhuddhavudhikrai, P. (1993) Mycobacterium
marinum cutaneous infections acquired from occupations and hobbies. Inter-
national Journal of Dermatology 32, 504–507.
Kusuda, R. (1975) Nocardial infection in cultured yellowtails. In: Proceedings of the
Third US–Japan Meeting on Aquaculture. Special Publication of Fishery Agency,
Japanese Government and Japan Sea Regional Fisheries Research Laboratory,
Nijata, Japan, pp. 63–66.
Kusuda, R. and Kawahara, E. (1987) Direct and indirect fluorescent antibody identifi-
cation of yellowtail pathogens. Bulletin of the Society of Scientific Fisheries 53,
389–394.
Kusuda, R. and Nakagawa, A. (1978) Nocardial infection of cultured yellowtail. Fish
Pathology 13, 25–31.
Kusuda, R. and Taki, H. (1973) Studies on a nocardial infection of cultured yellowtail. I.
Morphological and biochemical characteristics of Nocardia isolated from diseased
fishes. Bulletin of the Japanese Society of Scientific Fisheries 39, 937–943.
Kusuda, R., Taki, H. and Takeuchi, T. (1974) Studies on a Nocardia infection of cultured
yellowtail II. Characteristics of Nocardia kampachi isolated from a gill-tuberculosis
of yellowtail. Bulletin of the Japanese Society of Scientific Fisheries 40, 369–373.
Kusuda, R., Kimura, Y. and Hamaguchi, M. (1989) Changes in peripheral and peritoneal
leucocytes in yellowtail, Seriola quinqueradiata immunized with Nocardia
kampachi. Bulletin of the Japanese Society of Scientific Fisheries 55, 1183–
1188.
Lansdell, W., Dixon, B., Smith, N. and Benjamin, L. (1993) Isolation of several Myco-
bacterium species from fish. Journal of Aquatic Animal Health 5, 73–76.
Lawhavinit, O., Hatai, K., Kubota, S.S., Toda, K. and Suzuki, N. (1988) Occurrence of
Mycobacterium infection from pond-cultured pejerry, Odonthestes bonariensis
C&V, in Japan. Bulletin of Nippon Veterinary and Zootechnical College 37, 28–34.
Lechevalier, M.P., Horan, A.C. and Lechevalier, H. (1971) Lipid composition in the
classification of nocardiae and mycobacteria. Journal of Bacteriology 105, 313–
318.
MacKenzie, K. (1988) Presumptive mycobacteriosis in North-East Atlantic mackerel,
Scomber scombrus L. Journal of Fish Biology 32, 263–275.
Majeed, S.K., Gopinath, C. and Jolly, D.W. (1981) Pathology of spontaneous tuber-
culosis and pseudotuberculosis in fish. Journal of Fish Diseases 4, 507–512.
Michelson, E.H. (1961) An acid-fast pathogen of freshwater snails. Journal of Tropical
Medicine and Hygiene 10, 423–433.
Mollohan, C.S. and Romer, M.S. (1961) Public health significance of swimming pool
granuloma. American Journal of Public Health 51, 883–891.
Nigrelli, R.F. and Vogel, H. (1963) Spontaneous tuberculosis in fishes and in other cold-
blooded vertebrates with special reference to Mycobacterium fortuitum Cruz from
fish and human lesions. Zoologica 48(9), 131–143.
Noga, E.J., Dykstra, M.J. and Wright, J.F. (1989) Chronic inflammatory cells with
epithelial cell characteristics in teleost fishes. Veterinary Pathology 26, 429–437.
Noga, E.J., Wright, J.F. and Pasarell, L. (1990) Some unusual features of myco-
Mycobacteriosis and Nocardiosis 339