Avian Tuberculosis in Waterfowl, Lagomorphs and Ferrets (with notes on Hedgehogs)

Disease Summary

Alternative Names (Synonyms)

• Avian TB
• Mycobacteriosis
• Tuberculosis
• TB

Disease Type

Infectious/Non-Infectious Agent associated with the Disease

• Mycobacteria of the Mycobacterium-intracellulare avium complex . (Species included within the complex which affect birds and common synonyms: MAIC, Mycobacterium avium complex (MAC), MAI Complex, Mycobacterium avium- Mycobacterium intracellulare Complex, Mycobacterium avium, Avian tubercle bacillus; Mycobacterium intracellulare; Battey bacillus Nocardia intracellularis, Mycobacterium intracellularis)
• Mycobacterium avium (serotypes 1, 2 and 3) are the major causes of disease in birds (B15).

Infective "Taxa"

• Mycobacterium avium-intracellulare complex

Non-infective agents

Physical agents

References

Disease Author

Major References / Reviews

Code and Title List

Lagomorphs:
J2.37.w3, J42.26.w1, J212.1.w1, P3.2006b.w4

Ferrets:
B627.14.w14
J4.204.w2, J42.123.w1, J212.18.w2, J215.23.w1, J238.132.w2

Other References

Code and Title List

Hedgehogs:
J3.114.w7
J10.43.w1
J21.22.w2

Detailed Clinical and Pathological Characteristics

General

Clinical Characteristics

• Clinical signs are not pathognomonic.
• Usually loss of condition leading to eventual emaciation, with wasting of the pectoral muscles very evident (prominent sternum or keel).
• Weakness, lameness, diarrhoea and deterioration of the plumage may be noted, including retarded moult.
• Abdominal distention (usually due to ascites) in advanced disease.
• Rarely, skin lesions - abscess or nodular growth near eyes, sides of face, base of the bill, wing joints or on legs.
• Clinical signs of tuberculosis are rarely described in wild waterfowl.

(B10.26.w10, B11.39.w7, B13.46.w1, B14, B15, B36.8.w8, B37.x.w1, P4.1992.w1)

• Non-specific signs - weight loss (64%) lethargy (50%), soiling of the perineum (39%), anorexia (32%); other signs less commonly (e.g. lameness in 14%), pale mucous membranes; in three nonpregnant females, lactation (11%). (J2.37.w3)
• Clinical pathology:
  • Abnormal complete blood cell counts seen in 91% of affected rabbits at some stage of the illness: heterophilia (most common), leucocytosis, monocytosis (29% of samples), anaemia (38% of rabbits - normocytic normochromic nonregenerative or macrocytic hypochromic regenerative), nucleated red blood cells in peripheral blood smears in six rabbits, metamyelocytes in one rabbit. Gneerally, rabbits exhibeted more than one haematological abnormality. (J2.37.w3)
  • In about half of tests, hypoalbuminaemia and/or hyperglobulinaemia. Less often hypercholesterolaemia and azotaemia. Elevated alkaline phosphatase in one individual with osteomyelitis. (J2.37.w3)

In Oryctolagus cuniculus domesticus - Domestic rabbit. 

• Illness in two rabbits (Belgian hare and Dutch breeds); one (Dutch breed) with observed weight loss. (J42.26.w1)
• Deaths of rabbits reported. (J212.1.w1)
• Chronic (one year when first seen) nasal discharge and violent sneezing. (P3.2006b.w4)
  • A large mass was visible on endoscopic examination of the nasal passages. (P3.2006b.w4)

• In a pet ferret, intermittent anorexia, diarrhoea and vomiting over a period of six weeks, continuing through another three weeks of supportive care. (J4.204.w2)
• In a six-year-old neutered male ferret with concurrent lymphoma, weight loss. (J212.18.w2)
• In ferrets experimentally infected by the oral route, initial weight loss in the first four weeks post infection, but then weight was regained. (J42.123.w1)

Incubation

• In Brachylagus idahoensis - Pygmy rabbit: earliest age of onset of clinical signs 10.5 months, average age at onset 28.5 months. (J2.37.w3)

• In one pet ferret, clinical signs resumed eight months after initial resection of a jejunal lesion. (J4.204.w2)
• In experimentally infected ferrets, signs (weight loss) were seen in the first four weeks after infection. (J42.123.w1)

Mortality / Morbidity

• In Brachylagus idahoensis - Pygmy rabbit: in captive pygmy rabbits, this has been the most common cause of death - 28 deaths (28% of the adult captive population) compared with 18 deaths of adults from other causes, June 2002 - September 2004. (J2.37.w3)
• Reported very rarely as a spontaneous disease in individual Oryctolagus cuniculus domesticus - Domestic rabbit. (J212.1.w1, P3.2006b.w4)
  • On one farm, 20 adult rabbits and about 40 kits died over a short period. Infection was confirmed in the single rabbit necropsied. (J212.1.w1)

• Reported most commonly in the past from laboratory ferrets in Europe (including UK), also from farms in New Zealand. (B627.14.w14)
• A six-year-old neutered male ferret with concurrent lymphoma was euthanised. (J212.18.w1)
• This is more common in [pet] ferrets than is Mammalian Tuberculosis. (B660.41.w41)

Pathology

• Emaciated. Prominent sternum (keel). Sometimes large volumes of ascitic fluid.
• Multiple nodules, yellow, white or grey, may be less than 1mm or up to several centimeters in diameter, solid to soft or crumbly in texture. Centre usually caseous in older lesions. Occur most frequently in the liver, but also commonly in the intestines, spleen and less frequently the lung, and may be found in other organs.
• Liver and spleen may also be enlarged and fragile, with tan-to-green translucent appearance due to amyloid deposition. Occasionally liver and spleen may be large, pale and firm (B36.8.w8).
• Pericarditis and airsacculitis may be noted. "grape-like" clusters of tubercles have been described on the serous membranes of the thorax (B48.10.w10).
• Endocarditis, aortic arteritis, skeletal and skin lesions have been noted infrequently.
• Amyloidosis may be found, developing secondary to the chronic infection (B39.w1).

Histopathology:

• Recent lesions: mass of histocytic cells with variable numbers of lymphocytes. Later centre of lesion becomes an amorphous eosinophilic mass, with surrounding epithelioid cells and giant cells, with an outer layer of fibrous tissue in older lesions (less fibrosis usual in waterfowl than in some other bird species).

(J7.11.w2, J8.17.w1, B10.26.w10, B11.39.w7, B14, B15, B36.8.w8, B37.x.w1, B48.10.w10).

Unusual presentations of the disease:

• An unusual form of the disease has been described which resembled Amyloidosis, with ascites, an enlarged, pale, firm liver and spleen, sometimes with multiple 1-2 mm foci in the liver, and sometimes hydropericardium. Large amounts of pale amorphous eosinophilic material replaced the normal tissue and inflammatory cells including lymphocytes and large phagocytic cells were found within this (B15).
• Polycystic liver lesions with a greatly enlarged liver have also been reported as an unusual form of the disease (J5.33.w1).

Gross pathology:

• Granulomas in a variety of tissues. These were generally yellow, slightly firmer than normal fat and up to several millimetres in diameter.
• Note: 
  • There was no correlation between the number/size of lesions detected at necropsy and the clinical state (degree of debilitation) of the animal. For example, pulmonary disease was rarely diagnosed in life but gross lesions were found in the lungs of 18 rabbits. (J2.37.w3)
• No granuloma formation in one wild-caught (captive 17 months) Idaho pygmy rabbit. (J2.37.w3)

Histopathology:

• Granulomas detected in 19 tissues. (J2.37.w3)
• Present in liver and kidney in more than 50%. Pulmonary lesions in 27 rabbits. Lesions were "granulomatous inflammation, discrete granulomas, and areas of necrosis. Inflammation was predominantly comprised of macrophages with fewer neutrophils, lymphocytes and plasma cells, sometimes organised into discrete granulomas oriented around foci of caseous necrosis." There were occasional Langhans-type multinucleate giant cells at the margin of necrotic areas and inflammation. With Fite's acid-fast stain, acid-fast bacilli were detected in low to moderate numbers in necrotic foci and were sometimes seen in the cytoplasm of multinucleate cells or macrophages. (J2.37.w3)
• No histologically detectable granuloma formation in one wild-caught (captive 17 months) Idaho pygmy rabbit, but necropsy tissues were positive for Mycobacterium avium. (J2.37.w3)

In Oryctolagus cuniculus domesticus - Domestic rabbit

Gross pathology

• Lungs: numerous small caseous tubercles. (J42.26.w1)
• Liver: numerous small caseous tubercles. (J42.26.w1)
• GIT: Small tuberculous nodules throughout the small intestine, reaching the size of a small pea in the duodenum. In the caudal jejunum, large ulcers. In the large intestine, "about half a dozen of the little pouches which are normally present were greatly dilated and covered externally with copious tufts of villous growth. Internally the mucous membrane lining these dilatations was ulcerated, and some of them contained an incarcerated faecal pellet." Vermiform appendix mottled and containing caseous patches, most visible from the serosal side. (J42.26.w1)
• Lymph nodes: mesenteric lymph nodes contained superficial caseous foci.(J42.26.w1)
• Spleen: Single small caseous focus.(J42.26.w1)
• Kidneys: whitish tubercles projecting prominently from the serosal surface. (J42.26.w1)

In one rabbit (Dutch breed):

• Joints: Right stifle, elbow and tibio-tarsal joint and left hock joint. Synovial membrane yellow, swollen, protruding between the tendons. (J42.26.w1)
• Lymph nodes: Enlarged popliteal and right axillary lymph nodes but no obvious lesions.

In one adult rabbit examined following deaths of 20 adults and 40 kits on a farm:

• General: cachexia, severe muscle atrophy. (J212.1.w1)
• Lungs: in the parencyma and on the serosal surface, white nodules. (J212.1.w1)
• Liver: in the parencyma and on the serosal surface, white nodules. (J212.1.w1)
• Kidney: in the parencyma and on the serosal surface, white nodules. (J212.1.w1)
• Mesentry: white nodules. (J212.1.w1)
• Intestines: in all layers, white nodules. (J212.1.w1)
• CNS: 
  • In the cerebrum, white nodules, one 1 mm diameter, the other 3 mm diameter with a localised area of haemorrhage nearby in the leptomeninges. (J212.1.w1)
  • In the medulla oblongata, a 1 mm nodule. (J212.1.w1)

Histopathology

In one rabbit (Belgian hare breed): (J42.26.w1)

• "Tubercle bacilli were fairly numerous in the lungs and kidneys." (J42.26.w1)
  • Bacilli cultured from kidney lesions and confirmed as Mycobacterium avium. (J42.26.w1)

In one rabbit (Dutch breed):

• Joints: In the swollen synovial membranes, small numbers of bacilli. (J42.26.w1)
  • Bacilli cultured from the affected knee joint and confirmed as Mycobacterium avium. (J42.26.w1)

In one adult rabbit examined following deaths of 20 adults and 40 kits on a farm:

• Lung, liver, kidney, intestine: multiple granulomas, generally with central caseous necrosis (sometimes with slight calcification) surrounded by variable zones of infiltrating lymphocytes, epithelioid macrophages, and multinucleated giant cells, with proliferating fibrous connective tissue around the lesions. (J212.1.w1)
• CNS: 
  • In the cerebrum, two granulomatous lesions, focal, with central necrosis, slight mineralisation of the larger lesions, and numerous lymphocytes. The necrotic zone was encircled by a thin zone of epithelioid macrophages and lymphocytes and there were also small collections of lymphocytes and epithelioid macrophages in the affected gyrus, lymphocytic perivascular cuffs of several vessels, and in the adjacent leptomeninges, focal thickening with epithelioid macrophages and lymphocytes. (J212.1.w1)
  • In the medulla oblongata, a granuloma with central caseous necrosis and numerous lymphocytes, encircled by a thin zone of epithelioid macrophages; lymphocytic perivascular cuffs were present around nearby vessels. (J212.1.w1)
• Acid-fast bacilli demonstrated by auramine-stain in cerebrum, medulla oblongata, lung, liver, kidney, and intestinal lesions. (J212.1.w1)

In a pet rabbit with respiratory signs (violent sneezing):

• Mass in nasal passageways was sown on histopathology (following aggressive debridement) to be granulomatous, with acid-fast oragnisms. (P3.2006b.w4)
• Mycobacterium avium complex cultured. (P3.2006b.w4)

Gross pathology

In a pet ferret: (J4.204.w2)

• GIT: 
  • Initial lesion removed at surgery: 1 cm constricting band in the jejunum. (J4.204.w2)
  • Pyloric mass, 1 cm diameter, projecting into the gastric lumen, eight months later. At necropsy two weeks after that was resected, thickened pylorus. (J4.204.w2)

In a six-year-old neutered male ferret with concurrent lymphoma. (J212.18.w2)

• GIT: Stomach wall thickened (2 mm thick) causing the mucosa to form folds. (J212.18.w2)
• Hepatic: multiple tan 0.5-1.0 cm masses. (J212.18.w2)
• Mesenteric lymph nodes: enlarged to twice normal size; no obvious cortex-medulla boundary. (J212.18.w2) 

In ferrets experimentally infected by the oral route, no gross lesions. (J42.123.w1)

Histopathology

In a pet ferret: (J4.204.w2)

• GIT: pylorus: submucosa and lamina propria, sheets of macrophages present. Jejunum and stomach, severe granulomatous inflammation. (J4.204.w2)
• Lymph nodes: mesenteric, severe granulomatous inflammation. (J4.204.w2)
• Hepatic: small granulomas present. (J4.204.w2)
• Splenic: small granulomas present. (J4.204.w2)
• Acid-fast staining: acid fast bacilli detected. (J4.204.w2)

In a six-year-old neutered male ferret with concurrent lymphoma. (J212.18.w2)

• GIT: Stomach wall normal mural architecture obliterated by mixed neoplastic lymphocytes (30-50 um diameter round cells with marked anocytosis, large, oval irregular nuclei, moderate eosinophilic cytoplasm, moderate mitotic figures) and granulomatous inflammation (macrophages with abundant, lightly eosinophilic cytoplasm, containing numerous acid-fast bacilli). (J212.18.w2)
• Hepatic: mixed neoplastic lymphocytes and granulomatous inflammation (macrophages with abundant, lightly eosinophilic cytoplasm, containing numerous acid-fast bacilli). (J212.18.w2)
• Mesenteric lymph nodes: mixed neoplastic lymphocytes and granulomatous inflammation (macrophages with abundant, lightly eosinophilic cytoplasm, containing numerous acid-fast bacilli). (J212.18.w2)
• Renal: in the cortex and pelvis, a few small aggregates of macrophages, containing acid-fast bacilli. (J212.18.w1)
• Pulmonary: In alveolar macrophages, acid-fast bacilli present. (J212.18.w2)
• PCR: positive for Mycobacterium avium; negative for Mycobacterium bovis and for Mycobacterium avium subsp. paratuberculosis. (J212.18.w2)

In ferrets experimentally infected by the oral route: (J42.123.w1)

• Mesenteric lymph node: In 1/9 ferrets, microscopic lesions but no detectable acid-fast bacilli with Ziehl-Neelsen staining in any of the ferrets (in contrast to those infected with Mycobacterium bovis, in which 9/9  had microscopic lesions and AFB were found in 8/9). (J42.123.w1)

Human Health Considerations

• In addition to immunocompromise, individuals with existing lung pathology are more susceptible. (P24.334.w4)
• Transmission to humans is by ingestion or inhalation. (P24.327.w4)
  • Human infection may occur by kissing of, or close contact with, infected birds, such that sufficient numbers of infective organisms are inhaled or ingested. (P24.334.w4)
• In males over 40 years old, pulmonary chronic cavity tuberculosis may be seen, in children, cervical lympadenitis. Systemic lymphogenic disease can occur. (B12.22.w13)
• Infections in humans tend to be progressive, refractory to treatment and are often fatal. (B12.22.w13, B47)
  • Cervical lymphadenopathy in children may be treated by surgical excision of the affected lymph node. (B12.22.w13)

Disease has been reported in either the wild or in captivity in:

• A wide variety of waterfowl, also many other bird species.
• Captive Canada geese Branta canadensis and Ross's geese Anser rossii, also mute swans Cygnus olor and tundra swans Cygnus columbianus, green-winged (common) teal Anas crecca, wild northern shoveler Anas clypeata, wood duck Aix sponsa (B15).
• Domestic geese and ducks in Europe (J18.39.w1).
• Wild mallard Anas platyrhynchos, redhead Aythya americana and gadwall Anas strepera in USA (J5.33.w1).
• White-headed tree duck (white-faced whistling-duck) Dendrocygna viduata and garganey Anas querquedula (J5.20.w4).
• Hooded merganser Lophodytes cucullatus in Japan (J5.40.w2).
• Northern pintail Anas acuta, cinnamon teal Anas cyanoptera in a collection in the UK (J3.140.w3).
• Wild green-winged (common) teal Anas crecca, redhead Aythya americana, northern pintail Anas acuta, mallard Anas platyrhynchos, northern shoveler Anas clypeata, whistling (tundra) swan Cygnus columbianus (J4.99.w1).
• Red-breasted merganser Mergus serrator in a collection in the UK (J7.5.w1).
• African yellow billed duck Anas undulata, New Zealand scaup Aythya novaeseelandiae in a collection in the UK (J7.6.w1).
• Wild Eurasian wigeon Anas penelope and common shelduck Tadorna tadorna in the UK (J7.9.w1).
• Wild common pochard Aythya ferina in the UK (J7.11.w2).
• Wild common eiders Somateria mollisima in the UK (J7.12.w2).
• Dark-bellied brent goose Branta bernicla on the Wash, UK (J7.25.w1).
• Seaducks, particularly sawbills (Mergus spp.) in a collection in the UK (J7.30.w2).
• Shelducks and sheldgeese in a collection in the UK (J7.30.w4).
• Brazilian teal Amazonetta brasiliensis, maned goose (duck) Chenonetta jubata, mandarin Aix galericulata , Carolina (wood duck) Aix sponsa, pygmy goose Nettapus spp., comb duck Sarkidornis melanotos, Hartlaub's duck Pteronetta hartlaubii, white-winged wood duck Cairina scutulata, muscovy duck Cairina moschata, spur-winged goose Plectropterus gambensis, ringed teal Callonetta leucophrys in a collection in the UK (J7.32.w1).
• Spotted whistling duck Dendrocygna guttata, Eyton's whistling-duck Dendrocygna eytoni, wandering whistling-duck Dendrocygna arcuata, fulvous whistling-duck Dendrocygna bicolor, Cuban whistling-duck Dendrocygna arborea, Javan (lesser) whistling-duck Dendrocygna javanica, white-faced whistling-duck Dendrocygna viduata, red-billed whistling-duck Dendrocygna autumnalis in a collection in the UK (J7.33.w2).
• North American ruddy duck Oxyura jamaicensis, white-headed duck Oxyura leucocephala, maccoa duck Oxyura maccoa, blackheaded duck Heteronetta atricapilla, white-backed duck Thalassornis leuconotus in a collection in the UK (J7.33.w3).
• Adult true or northern geese (Branta spp. and Anser spp.): swan goose Anser cygnoides, bean goose Anser fabalis, pink-footed goose Anser brachyrhynchus, greater white-fronted goose Anser albifrons, lesser white-fronted goose Anser erythropus, greylag goose Anser anser, bar-headed goose Anser indicus, emperor goose Anser canagicus, snow goose Anser caerulescens, Ross's goose Anser rossii, Canada goose Branta canadensis, barnacle goose Branta leucopis, brent goose Branta bernicla, red-breasted goose Branta ruficollis; noted particularly in lesser whitefronted geese Anser erythropus, Canada geese Branta canadensis, and rarely in emperor geese Branta canagicus and greylag geese Anser anser, also reported in juvenile barnacle goose Branta leucopsis and red-breasted goose Branta ruficollis (J7.34.w1).
• All swan species in a collection in the UK: Bewick's swan Cygnus columbianus bewicki, black swan Cygnus atratus, black-necked swan Cygnus melanocorypha, Coscoroba swan Coscoroba coscoroba, mute swan Cygnus olor, trumpeter swan Cygnus buccinator, whistling swan Cygnus columbianus columbianus, whooper swan Cygnus cygnus (J7.43.w1).
• Wild mute swan Cygnus olor and Bewick's swan Cygnus columbianus in the UK (J7.43.w2)
• White-winged wood ducks Cairina scutulata at a collection in the UK (J7.43.w3).
• Wild waterfowl in British Columbia, Canada (J14.19.w1).
• Wild mute swan Cygnus olor in the UK (J36.41.w1)
• Wild mute swan Cygnus olor in the UK (J36.44.w1).
• Free-living mute swan Cygnus olor, Bewick's swan Cygnus columbianus, ping-footed goose Anser brachyrhynchus, greylag goose Anser anser, Canada goose Branta canadensis, brent goose Branta bernicla, northern pintail Anas acuta, common teal Anas crecca, mallard Anas platyrhynchos, gadwall Anas strepera, Eurasian wigeon Anas penelope, Common pochard Aythya ferina, tufted duck Aythya fuligula in the UK, mainly associated with sites with captive waterfowl (P16.1993.w1).
• Mute swan Cygnus olor, whistling and Bewicks' (tundra) swans Cygnus columbianus, trumpeter swans Cygnus buccinator, whooper swan Cygnus cygnus, barnacle goose Branta leucopsis (Th2).
• Common eider Somateria mollissima, Australian grey teal Querquedula gibberifrons (Grey teal Anas gracilis), Eurasian wigeon Anas penelope, common shelduck Tadorna tadorna, tufted duck Aythya fuligula, American wigeon Anas americana, trumpeter swan Cygnus buccinator, (American) green-winged teal Anas crecca, red-headed duck Aythya americana, mallard Anas platyrhynchos, (northern) shoveler Anas clypeata, whistling swan Cygnus columbianus columbianus (B48.10.w10).

Hedgehogs:

• Acid-fast bacilli identified as Mycobacterium avium type 2 were isolated from the mesenteric lymph nodes of one of five apparently healthy wild adult hedgehogs (Erinaceus europaeus - West European Hedgehog) from the Berkshire Downs, UK. (J21.22.w2)
• Acid-fast bacilli (not typed) were isolated from hedgehogs (Erinaceus europaeus - West European Hedgehog) found near a sawmill in the UK. (J3.128.w2)
• Mycobacterium avium was cultured from lymph nodes of a hedgehog (Erinaceus europaeus - West European Hedgehog) in New Zealand with enlarged jejunal and colonic lymph nodes. (J10.43.w1)

Lagomorphs:

In Brachylagus idahoensis - Pygmy rabbit 

• Disseminated mycobacteriosis diagnosed in 28 captive pygmy rabbits; this was the most common cause of death (28% of the adult captive population) compared with 18 deaths of adults from other causes, June 2002 - September 2004. (J2.37.w3)
• Spontaneous disease due to Mycobacterium avium has been diagnosed rarely in Oryctolagus cuniculus domesticus - Domestic rabbit. (J212.1.w1)
• On one farm, 20 adult rabbits and about 40 kits died over a short period. Infection was confirmed in the single rabbit necropsied. (J212.1.w1)

In Oryctolagus cuniculus domesticus - Domestic rabbit

• Spontaneous infection reported for the first time in two rabbits in 1913. (J42.26.w1)
• Spontaneous infection reported occasionally, for example confirmed in the one rabbit examined post mortem after 20 adults and 40 kits died on one farm, J212.1.w1)
• Seen causing respiratory signs associated with a large mass in the nasal passages of a pet rabbit. (P3.2006b.w4)

Ferrets

• In a pet ferret. (J4.204.w2)
• In a ferret in a zoo in France (pulmonary infection). (B627.14.w14)
• In research ferrets obtained from dealers. (B627.14.w14)
• In a six-year-old neutered male ferret with concurrent lymphoma in the USA. (J212.18.w1)
• A study of 21,481 feral ferrets from wildlife areas of New Zealand, 2004-2008 detected 175 isolates of Mycobacterium avium complex. (J238.132.w2)

Further information on Host species has only been incorporated for species groups for which a full Wildpro "Health and Management" module has been completed (i.e. for which a comprehensive literature review has been undertaken). Host species with further information available are listed below:

Host Species List

• Aix galericulata - Mandarin duck
• Aix sponsa - Wood duck
• Amazonetta brasiliensis - Brazilian teal
• Anas acuta - Northern pintail
• Anas americana - American wigeon
• Anas clypeata - Northern shoveler
• Anas crecca - Common teal
• Anas gracilis - Grey teal
• Anas penelope - Eurasian wigeon
• Anas platyrhynchos - Mallard
• Anas strepera - Gadwall
• Anas undulata - Yellow-billed duck
• Anser albifrons - Greater white-fronted goose
• Anser anser - Grey-lag goose
• Anser brachyrhynchus - Pink-footed goose
• Anser caerulescens - Snow goose
• Anser canagica - Emperor goose
• Anser cygnoides - Swan goose
• Anser erythropus - Lesser white-fronted goose
• Anser fabalis - Bean goose
• Anser indicus - Bar-headed goose
• Anser rossii - Ross's goose
• Aythya americana - Redhead
• Aythya ferina - Common pochard
• Aythya fuligula - Tufted duck
• Aythya novaeseelandiae - New Zealand scaup
• Branta bernicla - Brent goose
• Branta canadensis - Canada goose
• Branta leucopsis - Barnacle goose
• Branta ruficollis - Red-breasted goose
• Cairina moschata - Muscovy duck
• Cairina scutulata - White-winged duck
• Callonetta leucophrys - Ringed teal
• Chenonetta jubata - Maned duck
• Coscoroba coscoroba - Coscoroba swan
• Cygnus atratus - Black swan
• Cygnus buccinator - Trumpeter swan
• Cygnus columbianus - Tundra swan
• Cygnus cygnus - Whooper swan
• Cygnus melanocorypha - Black-necked swan
• Cygnus olor - Mute swan
• Dendrocygna arborea - West Indian whistling-duck
• Dendrocygna arcuata - Wandering whistling-duck
• Dendrocygna autumnalis - Black-bellied whistling-duck
• Dendrocygna bicolor - Fulvous whistling-duck
• Dendrocygna eytoni - Plumed whistling-duck
• Dendrocygna guttata - Spotted whistling-duck
• Dendrocygna javanica - Lesser whistling-duck
• Dendrocygna viduata - White-faced whistling-duck
• Heteronetta atricapilla - Black-headed duck
• Mergus serrator - Red-breasted merganser
• Oxyura jamaicensis - Ruddy duck
• Oxyura leucocephala - White-headed duck
• Oxyura maccoa - Maccoa duck
• Plectropterus gambensis - Spur-winged goose
• Pteronetta hartlaubii - Hartlaub's duck
• Sarkidornis melanotos - Comb duck
• Somateria mollissima - Common eider
• Tadorna tadorna - Common shelduck
• Thalassornis leuconotus - White-backed duck

MAMMALS:

• Brachylagus idahoensis - Pygmy rabbit
• Erinaceus europaeus - West European Hedgehog
• Mustela putorius furo - Ferret
• Oryctolagus cuniculus domesticus - Domestic rabbit

Disease has been specifically reported in Free-ranging populations of:

• A wide variety of species of waterfowl, also many other bird species.
• Wild green-winged (common) teal Anas crecca, redhead Aythya americana, northern pintail Anas acuta, mallard Anas platyrhynchos, northern shoveler Anas clypeata, whistling (tundra) swan Cygnus columbianus (J4.99.w1).
• Wild mallard Anas platyrhynchos, redhead Aythya americana and gadwall Anas strepera in USA (J5.33.w1).
• Wild Eurasian wigeon Anas penelope and common shelduck Tadorna tadorna in the UK (J7.9.w1).
• Wild common pochard Aythya ferina in the UK (J7.11.w2).
• Dark-bellied brent goose Branta bernicla on the Wash, UK (J7.25.w1).
• Wild mute swan Cygnus olor and Bewick's swan Cygnus columbianus in the UK (J7.43.w2)
• Wild waterfowl in British Columbia, Canada (J14.19.w1).
• Wild mute swan Cygnus olor in the UK (J36.41.w1)
• Wild mute swan Cygnus olor in the UK (J36.44.w1).
• Free-living mute swan Cygnus olor, Bewick's swan Cygnus columbianus, pink-footed goose Anser brachyrhynchos, greylag goose Anser anser, Canada goose Branta canadensis, brent goose Branta bernicla, northern pintail Anas acuta, common teal Anas crecca, mallard Anas platyrhynchos, gadwall Anas strepera, Eurasian wigeon Anas penelope, Common pochard Aythya ferina, tufted duck Aythya fuligula in the UK, mainly associated with sites with captive waterfowl (P16.1993.w1).
• Common eider Somateria mollissima, Eurasian wigeon Anas penelope, common shelduck Tadorna tadorna, tufted duck Aythya fuligula, American wigeon Anas americana, trumpeter swan Cygnus buccinator, (American) green-winged teal Anas crecca, red-headed duck Aythya americana, mallard Anas platyrhynchos, (northern) shoveler Anas clypeata, whistling swan Cygnus columbianus columbianus (B48.10.w10).

Hedgehogs:

• Acid-fast bacilli identified as Mycobacterium avium type 2 were isolated from the mesenteric lymph nodes of one of five apparently healthy wild adult hedgehogs (Erinaceus europaeus - West European Hedgehog) from the Berkshire Downs, UK. (J21.22.w2)
• Acid-fast bacilli (not typed) were isolated from a hedgehog (Erinaceus europaeus - West European Hedgehog) found near a sawmill in the UK. (J3.128.w2)
• Mycobacterium avium was cultured from lymph nodes of a hedgehog (Erinaceus europaeus - West European Hedgehog) in New Zealand with enlarged jejunal and colonic lymph nodes. (J10.43.w1)

Ferrets

• A study of 21,481 feral ferrets from wildlife areas of New Zealand, 2004-2008 detected 175 isolates of Mycobacterium avium complex. (J238.132.w2)

Further information on Host species has only been incorporated for species groups for which a full Wildpro "Health and Management" module has been completed (i.e. for which a comprehensive literature review has been undertaken). Host species with further information available are listed below:

Host Species List

• Anas acuta - Northern pintail
• Anas americana - American wigeon
• Anas clypeata - Northern shoveler
• Anas crecca - Common teal
• Anas penelope - Eurasian wigeon
• Anas platyrhynchos - Mallard
• Anas strepera - Gadwall
• Anser anser - Grey-lag goose
• Anser brachyrhynchus - Pink-footed goose
• Aythya americana - Redhead
• Aythya ferina - Common pochard
• Aythya fuligula - Tufted duck
• Branta bernicla - Brent goose
• Branta canadensis - Canada goose
• Cygnus buccinator - Trumpeter swan
• Cygnus columbianus - Tundra swan
• Cygnus olor - Mute swan
• Somateria mollissima - Common eider
• Tadorna tadorna - Common shelduck

MAMMALS:

• Erinaceus europaeus - West European Hedgehog
• Mustela putorius furo - Ferret

General Information on Environmental Factors/Events and Seasonality

• The Mycobacterium avium-intracellulare complex associated with Avian Tuberculosis of birds contains organisms of the air-freshwater interface, which are found most commonly in temperate regions, and survive best out of sunlight. Shady conditions and completely enclosed houses, by protecting the bacteria from sunlight, may enhance survival and thereby increase contamination (J7.32.w1, J44.72.w1, P3.1990-1991.w1).
• Bacteria of the Mycobacterium avium-intracellulare complex associated with Avian Tuberculosis of birds can survive for at least four years and possibly up to seven years in the environment. Sites on which waterfowl have been maintained for many years may have high levels of contamination, due to excretion of bacilli by infected birds over time (B32.7.w43, B14, P3.1990-1991.w1, P16.1993.w1).
• For wild waterfowl, exposure to the bacterium in wastewater and sewage contaminated sites may be higher in autumn and winter, when they may be attracted since warm water discharges keep water ice-free and hunting is often not allowed at such sites (B36.7.w7).
• Deaths may occur more frequently in females in summer and in males in winter. This is probably related to differences in energy expenditure, body condition and physiological changes: females reach a low body condition in summer, associated with egg laying and incubation, while males tend to reach their lowest body weight in winter. (J7.32.w1, J7.43.w3, J44.72.w1, P3.1990-1991.w1).
• Species from very hot and very cold environments may appear more susceptible when maintained in temperate areas due to increased stress from inappropriate climate. Additionally, they may have a lower natural immunity to bacteria of the Mycobacterium avium-intracellulare complex associated with Avian Tuberculosis of birds, due to less exposure to the organism in their natural environment (J44.72.w1, P3.1990-1991.w1).
• In Brachylagus idahoensis - Pygmy rabbit, disease was thought to be associated with soil provided in enclosures for burrowing. (J2.37.w3)

Regions / Countries where the Infectious Agent or Disease has been recorded

• Worldwide, but most commonly reported from the North Temperate Zone. Variation in occurrence e.g. across Canada and Australia (Th2, B32.7.w3).
  • In Brachylagus idahoensis - Pygmy rabbit: North America. (J2.37.w3)
• In the USA (in a ferret with concurrent lymphoma). (J212.18.w1)
• In the past, laboratory ferrets in Europe (including UK), also from farms in New Zealand. (B627.14.w14)
• In a ferret in a zoo in France (pulmonary infection). (B627.14.w14)

Regions / Countries where the Infectious Agent or Disease has been recorded in Free-ranging populations

• Worldwide, but most commonly reported from the North Temperate Zone (Th2, B32.7.w3).

General Information on Investigation / Diagnosis

• Typical pathological lesions (caseous nodules). Numerous acid-fast bacilli seen on Ziehl-Neelsen stained smears of lesions allows presumptive diagnosis.
• Acid-fast organisms are present within the large phagocytic cells in the form resembling amyloidosis.
• N.B. Culture and/or identification (standard techniques or molecular techniques) is required for definitive diagnosis of the organism as bacteria of the Mycobacterium avium-intracellulare complex.

(J8.17.w1, B10.26.w10, B11.39.w7, B14, B15, B32.7.w3, B36.8.w8, B37.x.w1)

In live birds:

• Diagnosis is difficult.
• The tuberculin test and agglutination tests are useful for diagnosis of infected chicken flocks but less useful for exotic birds. The tuberculin test appears unreliable in ducks and the skin sensitivity response may be 'switched off' in waterfowl with advanced tuberculosis. An agglutination test, which can be carried out on whole blood or serum, was found to be quick and easy to perform, but some false negatives (particularly with blood samples collected into EDTA) and false positives were noted (J6.22.w3, B32.7.w3).
• An ELISA has been developed which is sensitive, specific and capable of detecting the disease at an early stage, but this is not currently commercially available (J6.22.w3, P4.1993.w4).
• Haematological changes - anaemia, leucocytosis (high white blood cell count), monocytosis, heterophilia and hyperfibrogenaemia - are seen relatively late in the course of the disease, but may be useful for the detection of individual cases. Early cases may show moderate elevations in white cell counts and heterophilia (J6.19.w1, J6.22.w3).
• Faeces can be tested for acid-fast bacilli with Ziehl-Neelsen stain or by culture, but the absence of organisms does not confirm a negative diagnosis. Positive findings may indicate the disease but are not in themselves diagnostic.
• A new technique involving sample processing with a zwitterionic detergent followed by PCR analysis showed high sensitivity but appeared to have a relatively low specificity. This may be a useful screening test for use on faecal samples to identify birds on which further tests should be performed (J2.30.w1).
• N.B. Bacteria of the Mycobacterium avium-intracellulare complex associated with Avian Tuberculosis may be isolated from birds without evident clinical disease or lesions i.e. having infection without disease (J6.22.w3).
• Laparoscopy may be used in particularly valuable individual birds to see liver surface lesions.

(B11.39.w7, B14, B15, B37.x.w1).

• Physical examination. (J2.37.w3)
• Radiographs of thorax and skeleton. See: Imaging in Lagomorph Diagnosis and Treatment
  • Note: lesions did not change over the course of the disease (one to three months). (J2.37.w3)
• Acid-fast stains on prepared cytological samples - aspirates or impression smears - from masses.
• Haematology and serum biochemistry. 
• Antibody assays on serum or plasma: immunoblot. (J2.37.w3)
• Note: mycobacteria were detected by faecal culture in only one individual, although 11 had intestinal granulomas. (J2.37.w3)
• Sometimes positive by mycobacterial culture of urine or blood. In three animals, culture-positive urine or blood samples developed two to 10 weeks after onset of antibiotic treatment (in previously culture-negative individuals). (J2.37.w3)
• See: Clinical Pathology of Lagomorphs

In Oryctolagus cuniculus domesticus - Domestic rabbit

• Necropsy findings of multiple small granulomas, acid fast bacilli detected, and the organism grown in culture. Identity as Mycobacterium avium serovar 2 confirmed following animal inoculations. (J212.1.w1)
• In a pet rabbit with chronic respiratory signs:
  • Endoscopic examination of the nasal passages, followed by CT scan to determine the extent of the mass seen endoscopically. (P3.2006b.w4)
    • See: Imaging in Lagomorph Diagnosis and Treatment
  • Histopathology (of debrided tissue): granulomatous inflammatory mass in the nasal passages, containing acid-fast organisms. (P3.2006b.w4)
  • Repeated culture of Mycobacterium avium complex. (P3.2006b.w4)
    • See: Clinical Pathology of Lagomorphs

• Consider Mycobacterium avium (and other mycobacteria) as possible causes of illness in ferrets showing lethargy, weight loss and diarrhoea. (J215.23.w1)
• Ziehl-Neelsen staining: detection of acid fast bacilli. (J4.204.w2, J212.18.w1)
• Culture of Mycobacterium avium from spleen and liver following necropsy. (J4.204.w2)
• PCR: positive for Mycobacterium avium; negative for Mycobacterium bovis and for Mycobacterium avium subsp. paratuberculosis. (J212.18.w1)

• Environmental Assessment
• History & Documentation
• Physical Examination of Mammals
• Necropsy of Mammals
• Imaging in Lagomorph Diagnosis and Treatment
• Imaging in Ferret Diagnosis and Treatment
• Clinical Pathology of Lagomorphs
• Clinical Pathology of Ferrets
• Physical Examination of Birds - General
• Necropsy of Birds - General
• Treatment and Care - General
• Chapter 2 - B36 Field Manual of Wildlife Diseases - Specimen Collection and Preservation
• Chapter 3 - B36 Field Manual of Wildlife Diseases - Specimen shipment
• Appendix A - B36 Field Manual of Wildlife Diseases - Sample specimen history form

Similar Diseases (Differential Diagnosis)

• Aspergillosis (Aspergillosis) (caseous nodules), neoplasia (Neoplasias) (B15), yersiniosis (Yersiniosis) (B14).
• Amyloidosis (Amyloidosis) (for the form of avian tuberculosis characterised by ascites, diffuse liver enlargement (pale and firm), sometimes enlarged spleen (pale and firm) (B15).

• (J2.37.w3)

• Atypical Mycobacterial Infection in Ferrets
• Mammalian Tuberculosis (with special reference to Badgers, Hedgehogs, Elephants, Bears, Lagomorphs and Ferrets)

Other causes of weight loss, anorexia and diarrhoea. (J215.23.w1)

• e.g. Salmonellosis (with special reference to Waterfowl, Hedgehogs, Elephants, Bears, Lagomorphs and Ferrets)
• (Intestinal/abdominal) Lymphoma in Ferrets

Specific Medical Treatment

• Bacteria of the Mycobacterium avium-intracellulare complex associated with Avian Tuberculosis of birds are highly resistant to antituberculous drugs.
• The simultaneous use of multiple drugs in combination e.g. 1) isoniazid 30mg/kg, ethambutol 30 mg/kg, rifampicin (rifampin) 45 mg/kg (B32.7.w3); 2) rifabutin (56 mg/kg daily), azithromycin (43 mg/kg daily) or clarithromycin (85 mg/kg daily), ciprofloxacin or enrofloxacin (15 mg/kg twice daily, and amikacin (15 mg/kg twice daily), over a period of several months has been used in psittacines and may be effective. Problems with toxicity may be of concern (J29.6.w1).
• Treatment is not normally attempted as infected birds are a source of infection for others, but might be considered for a particularly valuable individual.

(B10.26.w10, B11.39.w7, B13.46.w1, B15, B32.7.w3, B37.x.w1)

• Azithromycin 50 mg/kg orally every 24 hours, plus rifabutin 25 mg/kg orally every 12 hours. (J2.37.w3)
  • Ethambutol may be added (45 mg/kg orally every 12 hours) to form a triple combination therapy; this triple combination did not produce any adverse effects in more than six months of treatment of one pygmy rabbit. (J2.37.w3)
• NSAID and/or vitamin E may be given to relieve tissue inflammation/discomfort. (J2.37.w3)
• Gamma-interferon might be a useful adjunct therapy to try. (J2.37.w3)
• Granulocyte-macrophage colony-stimulating factor might be synergistic with azithromycin (as shown in mice). (J2.37.w3)

In Oryctolagus cuniculus domesticus - Domestic rabbit

• In a pet rabbit with a mass in the nasal passages, aggressive debridement followed by rifampin 75 mg/kg orally every 12 hours, azithromycin 50 ,g/kg orally every 24 hours and ciprofloxacin 10 mg/kg orally every 12 hours appeared effective for about eight months. Later (due to change of sensitivity as indicated by a sensitivity panel), clarithromycin 50 mg/kg orally every 24 hours, rifabutin 25 mg/kg orally every 12 hours and ethambutol 45 mg/kg orally every 12 hours. (P3.2006b.w4)

• Treatment and Care - General

General Nursing and Surgical Techniques

• In a pet ferret with a jejunal constriction, surgical excision of the affected area and end-to-end anastomosis (mycobacterial infection was not diagnosed at that time). (J4.204.w2)
  • Eight months later, a further 1 cm diameter raised mass was resected from the pylorus. (J4.204.w2)

• Treatment and Care - General

• Laparotomy in Ferrets (Techniques)

Preventative Measures

• No commercial vaccines are available.
• A vaccine has been being developed and is presently being trialled at The Wildfowl and Wetlands Trust.

(Th2, J7.40.w3, B11.39.w7, V.w4).

WATERFOWL

• Preventative Medicine for Mammals

• Preventative Medicine for Birds

Environmental and Population Control Measures

WATERFOWL

• Good hygiene, removal and incineration of build-ups of droppings and organic matter
• Turning of soil and removal of shading vegetation will increase bacterial decay due to sunlight.
• Removal of topsoil, liming and replacement of clean soil could be used to decontaminate an area, but even this may not be effective.
• The use of wastewater to maintain or create wetlands for wild waterfowl should be carefully thought out with the risks of introducing mycobacteria into the environment assessed. The use of wastewater for either captive or free-living waterfowl should be avoided unless testing and/or treatment can assure the water is free of Mycobacterium bacilli.

(B11.39.w7, B36.8.w8, B37.x.w1, P4.1992.w1)

• House in non-soil pens, if possible, or sterilise the soil before putting it in the pens. (J2.37.w3)

• Keep stocking densities low.
• Ensure birds are well fed and avoid stress.
• Avoid contact between wild and captive birds.

(B11.39.w7, B37.x.w1)

• Particularly sensitive species should be maintained in a separate pen with a clean water supply and extra care to reduce stress by e.g. minimising disturbance, keeping stocking densities low and social groups appropriate, with access to heated winter accommodation if appropriate (J7.43.w3).

• Birds entering a collection should be quarantined, preferably for 60 days, and screened for tuberculosis.
• Foster-hens for rearing ducklings should be tuberculin tested.
• Birds know to be infected should be euthanased. Individuals of high conservation value could be maintained in isolation.
• Destruction of flocks know to be infected has been used in poultry.

(J8.17.w1, B10.26.w10, B11.39.w7, B13.46.w1, B15, B32.7.w3, B36.8.w8, B37.x.w1, P4.1992.w1).

• Prevent access of carrier birds to enclosures holding pygmy rabbits(J2.37.w3)

• Preventative Medicine for Mammals

• Preventative Medicine for Birds
• Environmental and Population Management
• Treatment and Care - Euthanasia
• Chapter 4 - B36 Field Manual of Wildlife Diseases - Disease Control Operations
• Chapter 5 - B36 Field Manual of Wildlife Diseases - Euthanasia