pulmonary adenomatosis
Index
- Pictures
- Identity
- Pathogen/s
- Overview
- Host Animals
- Hosts/Species Affected
- Systems Affected
- Distribution
- Distribution Table
- Pathology
- Diagnosis
- List of Symptoms/Signs
- Disease Course
- Epidemiology
- Impact: Economic
- Zoonoses and Food Safety
- Disease Treatment
- Prevention and Control
- References
- Distribution Maps
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Top of pagePreferred Scientific Name
- pulmonary adenomatosis
International Common Names
- English: ovine pulmonary adenomatosis; ovine pulmonary carcinoma, adenomatosis in sheep and goats; pulmonary adenocarcinoma in sheep and goats; sheep pulmonary adenomatosis
Local Common Names
- South Africa: jaagsiekte
- USA: ovine pulmonary carcinoma
English acronym
- OPA
- OPC
- SPA
Overview
Top of pageSheep pulmonary adenomatosis (SPA) is a contagious disease of sheep produced by a tumour of type II alveolar and Clara cells in the lungs. The disease has been occasionally recorded naturally in goats and mouflon. SPA is also known as jaagsiekte and ovine pulmonary carcinoma. The term jaagsiekte was used in South Africa where the first cases were described and it is derived from two Afrikaner words: "jaag" drive and "siekte" = disease. The term ovine pulmonary carcinoma is preferred in the USA.
SPA is caused by a type B/D exogenous retrovirus, known as jaagsiekte sheep retrovirus (JSRV); its oncogenic mechanisms are not known. SPA is widely distributed throughout several continents, except Australia and New Zealand. No accurate figures about the economic importance of the disease are available, because there are no pre-clinical diagnostic tests. The prevalence of the disease has been evaluated only by post-mortem examination in diagnostic laboratories or of lungs at the abattoir. In spite of these difficulties, in some countries such as South Africa, Scotland (UK), Peru and Spain the disease appears to be widespread and causes a high number of deaths, mainly in young adult sheep. Meat production is generally affected.
Hosts/Species Affected
Top of pageSPA is diagnosed mainly in young adult sheep but is (rarely) found in goats (Banerjee and Gupta, 1979, Sriraman et al., 1982, Metin et al., 1988), and wild mouflon, Ovis musimon (Nieddu et al., 1987). In countries where the disease is endemic, SPA may be more common in certain areas or breeds and also during the winter (Dungal et al., 1938; Tustin, 1969; Hunter and Munro, 1983). Any management condition that tends to keep animals housed for a long time promotes the spread of disease.
Distribution
Top of pageThe earliest known report of sheep pulmonary adenomatosis (SPA) comes from South Africa. In 1825, a letter by AP Aucamp reported a contagious respiratory disease known as "jaagziekte", which caused an elevated number of deaths with no recovery of affected animals. In the ensuing years, further reports confirmed the contagious and neoplastic nature of the disease and described other affected flocks, not only in South Africa, but also in several European countries (Tustin, 1969).
The history of the disease in Iceland deserves special mention. Nowadays this country is free of SPA but a very important epizootic causing a large number of deaths happened in the 1930s. The disease was imported from Germany in 1933 and introduced to an Icelandic farm called Deildartunga by a 1-year-old Karakul ram with no clinical signs of SPA. This ram was used to serve ewes and was kept in separate accommodation with one ewe and her lamb throughout the winter. The disease was noticed in the ram in the spring when the animals were released on the mountains. This ram did not return. In the following years, new cases appeared in the flock and in many others around the island, eventually killing between 50-80% of the animals in the affected flocks (Dungal et al., 1938). The high mortality probably was due to the particular sheep management system in Iceland. In this system, sheep are housed through the winter (1-4 months). At other times of the year, usually in September, sheep from different farms are concentrated at the heads of the valleys, where they spend several days before returning to their original farms. SPA was eradicated in 1952 following a very restrictive policy of sanitary control by killing all animals coming from flocks that showed any animal with clinical signs of the disease.
SPA has been recognised in many other countries throughout the world and, with the exception of Australia and New Zealand, is present in all continents with a varying degree of significance (see list of countries).
Distribution Table
Top of pageThe 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.
Last updated: 10 Jan 2020Continent/Country/Region | Distribution | Last Reported | Origin | First Reported | Invasive | Reference | Notes |
---|---|---|---|---|---|---|---|
Africa |
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Algeria | Absent, No presence record(s) | ||||||
Botswana | Absent, No presence record(s) | ||||||
Burundi | Absent, No presence record(s) | ||||||
Cabo Verde | Absent, No presence record(s) | ||||||
Central African Republic | Absent, No presence record(s) | ||||||
Congo, Democratic Republic of the | Absent, No presence record(s) | ||||||
Côte d'Ivoire | Absent, No presence record(s) | ||||||
Djibouti | Absent, No presence record(s) | ||||||
Egypt | Absent, No presence record(s) | ||||||
Eritrea | Absent, No presence record(s) | ||||||
Eswatini | Absent, No presence record(s) | ||||||
Ethiopia | Absent, No presence record(s) | ||||||
Ghana | Absent, No presence record(s) | ||||||
Guinea | Absent, No presence record(s) | ||||||
Lesotho | Absent, No presence record(s) | ||||||
Libya | Absent, No presence record(s) | ||||||
Madagascar | Absent, No presence record(s) | ||||||
Mauritius | Absent, No presence record(s) | ||||||
Namibia | Present | 2003 | |||||
Nigeria | Absent, No presence record(s) | ||||||
São Tomé and Príncipe | Absent, No presence record(s) | ||||||
Seychelles | Absent, No presence record(s) | ||||||
South Africa | Present | ||||||
Sudan | Absent, No presence record(s) | ||||||
Togo | Absent, No presence record(s) | ||||||
Tunisia | Absent, No presence record(s) | ||||||
Uganda | Absent, No presence record(s) | ||||||
Zimbabwe | Present | 1994 | |||||
Asia |
|||||||
Bahrain | Absent, No presence record(s) | ||||||
Bhutan | Absent, No presence record(s) | ||||||
Brunei | Absent, No presence record(s) | ||||||
China | Present | ||||||
-Xinjiang | Present | ||||||
Georgia | Absent, No presence record(s) | ||||||
Hong Kong | Absent, No presence record(s) | ||||||
India | Absent, No presence record(s) | ||||||
-Andaman and Nicobar Islands | Present | ||||||
-Punjab | Present | ||||||
-Rajasthan | Present | ||||||
-Uttar Pradesh | Present | ||||||
-West Bengal | Present | ||||||
Indonesia | Absent, No presence record(s) | ||||||
Iran | Absent, No presence record(s) | ||||||
Israel | Present | ||||||
Japan | Absent, No presence record(s) | ||||||
Jordan | Absent, No presence record(s) | ||||||
Kazakhstan | Absent, No presence record(s) | ||||||
Kuwait | Absent, No presence record(s) | ||||||
Lebanon | Absent, No presence record(s) | ||||||
Malaysia | |||||||
-Peninsular Malaysia | Present | 2003 | |||||
-Sabah | Absent, No presence record(s) | ||||||
-Sarawak | Absent, No presence record(s) | ||||||
Mongolia | Absent, No presence record(s) | ||||||
Myanmar | Absent, No presence record(s) | ||||||
Nepal | Absent, No presence record(s) | ||||||
North Korea | Absent, No presence record(s) | ||||||
Oman | Absent, No presence record(s) | ||||||
Philippines | Absent, No presence record(s) | ||||||
Saudi Arabia | Absent, No presence record(s) | ||||||
Singapore | Absent, No presence record(s) | ||||||
South Korea | Absent, No presence record(s) | ||||||
Sri Lanka | Absent, No presence record(s) | ||||||
Syria | Absent, No presence record(s) | ||||||
Taiwan | Absent, No presence record(s) | ||||||
Thailand | Absent, No presence record(s) | ||||||
Turkmenistan | Absent, No presence record(s) | ||||||
Uzbekistan | Absent, No presence record(s) | ||||||
Vietnam | Absent, No presence record(s) | ||||||
Europe |
|||||||
Andorra | Present | CAB Abstracts Data Mining | |||||
Austria | Absent, No presence record(s) | ||||||
Belarus | Absent, No presence record(s) | ||||||
Bosnia and Herzegovina | Absent, No presence record(s) | ||||||
Bulgaria | Absent, No presence record(s) | ||||||
Croatia | Absent, No presence record(s) | ||||||
Cyprus | Present | 1993 | |||||
Czechia | Present | 1995 | |||||
Denmark | Present | 2000 | |||||
Estonia | Absent, No presence record(s) | ||||||
Finland | Absent, No presence record(s) | ||||||
France | Present | ||||||
Germany | Present | CAB Abstracts Data Mining | |||||
Greece | Present | 2003 | |||||
Hungary | Present | 1970 | |||||
Ireland | Present | ||||||
Isle of Man | Absent, No presence record(s) | ||||||
Jersey | Absent, No presence record(s) | ||||||
Latvia | Absent, No presence record(s) | ||||||
Liechtenstein | Absent, No presence record(s) | ||||||
Lithuania | Absent, No presence record(s) | ||||||
Luxembourg | Absent, No presence record(s) | ||||||
Malta | Absent, No presence record(s) | ||||||
Moldova | Absent, No presence record(s) | ||||||
North Macedonia | Absent, No presence record(s) | ||||||
Norway | Absent, No presence record(s) | ||||||
Poland | Absent, No presence record(s) | ||||||
Portugal | Present | ||||||
Romania | Absent, No presence record(s) | ||||||
Russia | Present | ||||||
-Central Russia | Present | ||||||
-Southern Russia | Present | ||||||
Serbia and Montenegro | Absent, No presence record(s) | ||||||
Slovakia | Absent, No presence record(s) | ||||||
Slovenia | Absent, No presence record(s) | ||||||
Sweden | Absent, No presence record(s) | ||||||
Switzerland | Present | ||||||
United Kingdom | Present | ||||||
North America |
|||||||
Barbados | Absent, No presence record(s) | ||||||
Belize | Absent, No presence record(s) | ||||||
Bermuda | Absent, No presence record(s) | ||||||
British Virgin Islands | Absent, No presence record(s) | ||||||
Canada | Present | ||||||
Cayman Islands | Absent, No presence record(s) | ||||||
Costa Rica | Absent, No presence record(s) | ||||||
Cuba | Absent, No presence record(s) | ||||||
Curaçao | Absent, No presence record(s) | ||||||
Dominica | Absent, No presence record(s) | ||||||
Dominican Republic | Absent, No presence record(s) | ||||||
El Salvador | Absent, No presence record(s) | ||||||
Guadeloupe | Absent, No presence record(s) | ||||||
Guatemala | Absent, No presence record(s) | ||||||
Haiti | Absent, No presence record(s) | ||||||
Honduras | Absent, No presence record(s) | ||||||
Jamaica | Absent, No presence record(s) | ||||||
Mexico | Absent, No presence record(s) | ||||||
Nicaragua | Absent, No presence record(s) | ||||||
Panama | Absent, No presence record(s) | ||||||
Saint Vincent and the Grenadines | Absent, No presence record(s) | ||||||
Trinidad and Tobago | Absent, No presence record(s) | ||||||
United States | Present | ||||||
-Colorado | Present | ||||||
-Minnesota | Present | ||||||
-Wyoming | Present | ||||||
Oceania |
|||||||
Australia | Absent, No presence record(s) | ||||||
French Polynesia | Absent, No presence record(s) | ||||||
New Caledonia | Absent, No presence record(s) | ||||||
New Zealand | Absent, No presence record(s) | ||||||
Samoa | Absent, No presence record(s) | ||||||
Vanuatu | Absent, No presence record(s) | ||||||
South America |
|||||||
Argentina | Present | ||||||
Brazil | |||||||
-Mato Grosso do Sul | Present | ||||||
Chile | Present | ||||||
Colombia | Absent, No presence record(s) | ||||||
Ecuador | Absent, No presence record(s) | ||||||
Falkland Islands | Absent, No presence record(s) | ||||||
French Guiana | Absent, No presence record(s) | ||||||
Guyana | Absent, No presence record(s) | ||||||
Paraguay | Absent, No presence record(s) | ||||||
Peru | Present | ||||||
Venezuela | Absent, No presence record(s) |
Pathology
Top of pagePost-mortem examination of the sheep affected by SPA shows that lesions are confined mainly to the lungs. They are considerably enlarged and heavier than normal due to infiltration by areas of tumour which may vary from small discrete nodules, measuring only 0.5-2 cm, to extensive tumours involving the entire ventral half of the diaphragmatic and other lobes. Usually tumour tissue is present in both lungs although the extent on either side does vary. The lesions can be segregated into two general types:
Classical SPA
Tumours are solid, grey or light purple with a shiny translucent sheen and often separated from adjacent normal lung by a narrow emphysematous zone. The presence of frothy white fluid in the respiratory passages is a prominent feature and is obvious even in lesions as small as a few millimetres. In advanced cases, this fluid flows out of the trachea when it is cut or pendant. Histological examination of SPA lesions shows areas of lung where cuboidal or columnar cells replace the normal thin alveolar cells. Sometimes these abnormal cells form papilliform growths that project into the alveoli. Intrabronchiolar proliferation also may be present. The histological picture is classified as a bronchioloalveolar cell carcinoma. A third type of change consists of nodules of loose connective tissue in a mucopolysaccharide substance. Accumulations of large macrophage cells occur in the lung tissue around the tumours (Wandera, 1971; Sharp and Angus, 1990).
Atypical SPA
Tumours comprise solitary or aggregated hard white nodules, which have a dry cut surface and show clear demarcation from surrounding tissues. The presence of excess fluid is not a prominent feature. The histological appearance of these tumours is essentially the same as classical SPA but with an exaggerated inflammatory response (mostly lymphocytes and plasma cells) and fibrosis (De las Heras et al.,1992; Garcia Goti et al., 2000).
Pleurisy may be evident over the surface of the tumour and in some cases abscesses or gangrenous tissue are present in the adenomatous tissue.
Adult sheep, that on post-mortem examination appear to have died from acute pasteurellosis should have their lungs examined carefully, as lesions of SPA may be masked by the acute reaction to the Pasteurellae.
The tumour rarely metastasises beyond the mediastinal lymph nodes but extrathoracic tumour metastases can be found in some cases (Nobel et al., 1969).
Ultrastructural studies have shown that the cells forming the alveolar lesion are type II alveolar cells and those in the bronchiolar tumours, the cells of Clara (Nisbet et al., 1971; Perk et al., 1971).
Diagnosis
Top of pageClinical detection of a case of classical SPA should be based on the presence, in a single mature sheep of an afebrile wasting disease, with marked respiratory signs. A useful aid to diagnosis is to raise the hindquarters and lower the head of the sheep, which causes mucoid fluid, sometimes copious in amount, to run from the nostrils. This is the key clinical sign to differentiate SPA from other sheep lung diseases that can show respiratory distress but never the emission of such amount and type of fluid. Large tumours are unmistakable in appearance at necropsy but confirmatory histology may be necessary where the amount of adenomatous tissue is small or secondary bacterial pneumonia has developed. Where tumours are not obvious, at least 1-2 samples for histological examination should be taken from each lobe. The transformed epithelial cells are the major sites of virus replication and JSRV antigens can be revealed by immunohistochemical techniques (Palmarini et al., 1995).
At present, there are no laboratory tests to support a clinical diagnosis of SPA in the live animal. JSRV has been associated exclusively with both classical and atypical forms of SPA but antibodies to this virus have not been detected in the sera of affected sheep, even with highly sensitive assays such as immunoblotting (Ortín et al., 1998).
Sequencing of JSRV and SERVs has led to the development of PCR that can detect the exogenous virus in a background of genomic DNA and endogenous sequences (Palmarini et al., 1997). Using this sensitive procedure, JSRV has been detected in the blood of unaffected in-contact sheep from flocks with SPA, as well as experimentally infected lambs. This finding suggests that infected animals can be identified during the pre-clinical stages and may offer a new way to diagnose SPA.
List of Symptoms/Signs
Top of pageSign | Life Stages | Type |
---|---|---|
General Signs / Exercise intolerance, tires easily | Sheep and Goats|Breeding male; Sheep and Goats|Gimmer; Sheep and Goats|Hogget; Sheep and Goats|Mature female | Sign |
General Signs / Generalized weakness, paresis, paralysis | Sign | |
General Signs / Reluctant to move, refusal to move | Sign | |
General Signs / Sudden death, found dead | Sign | |
General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift | Sheep and Goats|Breeding male; Sheep and Goats|Gimmer; Sheep and Goats|Hogget; Sheep and Goats|Mature female | Diagnosis |
General Signs / Weight loss | Sheep and Goats|Breeding male; Sheep and Goats|Gimmer; Sheep and Goats|Hogget; Sheep and Goats|Mature female | Diagnosis |
Respiratory Signs / Abnormal breathing sounds of the upper airway, airflow obstruction, stertor, snoring | Sign | |
Respiratory Signs / Abnormal lung or pleural sounds, rales, crackles, wheezes, friction rubs | Sheep and Goats|Breeding male; Sheep and Goats|Gimmer; Sheep and Goats|Hogget; Sheep and Goats|Mature female | Sign |
Respiratory Signs / Coughing, coughs | Sign | |
Respiratory Signs / Dull areas on percussion of chest, thorax | Sign | |
Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping | Sheep and Goats|Breeding male; Sheep and Goats|Gimmer; Sheep and Goats|Hogget; Sheep and Goats|Mature female | Sign |
Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea | Sheep and Goats|Breeding male; Sheep and Goats|Gimmer; Sheep and Goats|Hogget; Sheep and Goats|Mature female | Sign |
Respiratory Signs / Mucoid nasal discharge, serous, watery | Sheep and Goats|Breeding male; Sheep and Goats|Gimmer; Sheep and Goats|Hogget; Sheep and Goats|Mature female | Diagnosis |
Respiratory Signs / Purulent nasal discharge | Sign |
Disease Course
Top of pageIn naturally infected sheep, the incubation period appears to be long, so that the disease is not usually seen until sheep are about 2-4 years old. However, tumours have been seen exceptionally in lambs as young as 2 months and in a sheep as old as 11 years of age (Hunter and Munro, 1983; Sharp and Angus, 1990). Clinical signs of the disease only appear when the tumours are sufficiently large to interfere with normal lung function resulting in respiratory embarrassment, which is most obvious following exercise. Abattoir studies have revealed small SPA lesions in clinically normal animals (De las Heras et al., 1992). Experimentally, tumour formation occurs 5-12 months after the intra-tracheal inoculation of tumour tissue or lung fluid extracts containing JRSV into lambs several months old (Wandera, 1971; Martin et al., 1976; Herring et al., 1983). However, when neonatal lambs are inoculated with these extracts or virions from the infectious molecular clone, the tumours can be reproduced in several weeks (Sharp et al., 1983, Palmarini et al., 1999).
The mechanisms of oncogenesis by JSRV are unknown and can only be speculated. The natural course of the disease suggests a very long incubation period, which would be compatible with oncogenenesis by retroviruses that lack oncogenes and induce tumours by insertional mutagenesis. This hypothesis is supported by the absence of recognisable oncogenes in the sequence of JSRV (York et al., 1992). However, the rapid induction of tumour in neonatal lambs is more characteristic of the tumours induced by acute transforming retroviruses that encode oncogenes. Other factors, such as viral dose and the age of the inoculated lamb, may be important and may account for the different types of disease response (Palmarini et al., 1997). JSRV establishes a disseminated infection in SPA-affected sheep (Palmarini et al., 1996b) and can be detected in lymphoid tissue before the onset of neoplasia (Holland et al., 1999). The dissemination of the virus is less intense in atypical SPA than in classical SPA (see types of lesions of SPA described in Pathology section) and in this form the number of tumour infiltrating cells and fibrosis is more intense, suggesting that in some animals the response to the virus is different (Garcia Goti et al., 2000). Although little is know about this area, the interaction between the JSRV and host immune system may be important in the pathogenesis of the disease.
Epidemiology
Top of pageSPA has been recognised for many years to be naturally and experimentally transmissible by the respiratory route. It is probable that an infected sheep, even before it develops obvious respiratory signs, excretes virus-containing droplets as it breathes. Later, as the disease progresses, it will discharge quantities of infective respiratory fluid, especially during feeding when the head is lowered. This causes the sheep to snuffle and doubtless creates an aerosol of infected droplets. Close confinement of a flock obviously increases the probability of transmission so that housing with trough feeding and watering may allow the infection to spread.
SPA is generally introduced into flocks by the acquisition of infected sheep. Losses from classical SPA can be high when the disease is first introduced. During the epidemic of SPA in Iceland the estimated time from the introduction of the disease and the appearance of the first clinical cases in other sheep was between 6 and 8 months (Dungal et al., 1938). All of the existing epidemiological information has been based on clinical diagnosis and pathology, and the extent of infection by jaagsiekte retrovirus (JSRV) in affected flocks is unknown.
Impact: Economic
Top of pageThere are no data available in terms of the real cost of SPA but there is some information about the percentage of animals that have died of the disease and of animals that show SPA-associated lesions at slaughterhouses. In endemic areas such as South Africa or Scotland the percentage of sheep killed by SPA is about 2-4% annually (Tustin, 1969; Hunter and Munro, 1983). However, in countries or farms where the disease has been recently introduced, the mortality, depending on management conditions, could reach 30-80% in the first two years (Dungal et al., 1938; Shirlaw, 1959; Enchev et al., 1958). Where the prevalence has been estimated as a proportion of the number of sheep slaughtered, the percentages can be as low as 0.1-0.2% in Chile or Germany (Schultz et al., 1965), 0.5-0.6% in India (Banerjee and Gupta, 1979), 0.6-1.7% in Perú (Ellis et al., 1993), 0.4-1.6% in Spain (De las Heras et al., 1992) or 0.7% in Italy (Cerretto and Deiana, 1967).
Zoonoses and Food Safety
Top of pageA protein related antigenically to JSRV has been demonstrated in approximately 30% of three forms of human primary pulmonary carcinoma and not in other tumours or diseases (De las Heras et al., 1997). This observation supports the view that the antigen in the human tumours may be a retrovirus protein and that a retrovirus may be associated with the neoplastic process in some tumours or represent reactivation/upregulation of an endogenous retrovirus. Although there is no epidemiological evidence to implicate JSRV as a cause of disease in man, recent demonstration of a receptor for JSRV on human cells warrants a cautious reappraisal of any potential zoonotic role.
Disease Treatment
Top of pageNo method of treatment is recognised or advised. Once the disease is detected there is no possibility of cure. Antimicrobial therapy only reduces the intensity of clinical signs for a short time.
Prevention and Control
Top of pageControl should be based on regular inspection of adult sheep in affected flocks. Any animal showing weight loss or signs of respiratory disease should be isolated and veterinary advice sought. Prompt culling of any suspicious animal is advisable, as well as the offspring of affected ewes, which frequently develop SPA. While these methods are unlikely to eradicate SPA from a flock in which the disease is endemic, reduction in the prevalence of infection may be obtained.
Embryo transfer has been reported as one way to obtain animals free of SPA, based on clinical and pathological evidence (Parker et al., 1998). It would be worthwhile to re-evaluate this approach with the more sensitive PCR techniques to confirm that the offspring were free of JSRV infection.
References
Top of pageAdamesteanu C; Rusu M; Baba I; Vesa S, 1969. Pulmonary adenomatosis in sheep in Romania. Revista de zootehnie medicina si veterinara, 19:54-60.
Aucamp VP, 1825. Cape Archives, GR 12/4.
Aynaud M, 1926. Origin verminouse du cancer pulmonaire de la brebis. Comptes rendus des scances de la Societe de Biologie, 95:1540-1542.
Banerjee M; Gupta PP, 1979. Note on Maedi and Jaagziekte in sheep and goats in Ludbiana area of Punjab. Indian Journal of Animal Science, 49:1102-1105.
Basset B; Sheehan P, 1989. Outbreak of sheep pulmonary adenomatosis in the Irish Republic. Veterinary Record, 124:46-47.
Carrara O; Gasparini G, 1959. Atti della Societa Italiana di Scence Veterinaria, 13:450.
Cerretto F; Deiana L, 1967. Adenomatosi polmonare enzootica degli ovini (jaagsiekte) in Sardegna. Atti della Societa Italiana di Scence Veterinaria, 21:606-611.
Christodoulous T; Tarlatis K, 1952. Chronic glandular pneumonia in the sheep (jaagsiekte). Deltion tes Hellenikes Kten. Hetaireias, 2:199-208.
Cuba-Caparo A, 1945. Boletin de la Escuela Nacional de Ciencias Veterinarias, 1:27.
Cuba-Caparo A; de la Vega E; Copaira M, 1961. Pulmonary adenomatosis of sheep metastasizing bronchiolar tumours. American Journal of Veterinary Research, 22:673-682.
Cutlip RC; Young S, 1982. Sheep pulmonary adenomatosis (Jaagsiekte) in the United States. American Journal of Veterinary Research, 43:2108-2113.
Cvjetanovic J; Martinic M, 1962. Epizooticna plucna adenomatoza 0vaca pao (jaagziekte) n Jugoslaviji. Veterinarski Archiv, 32:77-92.
Damodaran S, 1960. Ovine pulmonary adenomatosis (Jaagsiekte). Indian Veterinary Journal, 37:127-138.
De las Heras M; Calafat JJ; Jaime JM; García de Jalon JA; Ferrer LM; García Goti M; Minguijon E, 1992. Sheep pulmonary adenomatasis (jaagsiekte) in slaughtered sheep. Variation in pathological characteristics. Medicina Veterinaria, 9:52-52.
De las Heras M; Palamarini M; Larsson E; Haselton P; Wagner M; Minguijón E; Egan J; Dewar P; Ortín A; Gimenez Más JA; Gonzalez L; Dalziel R; Sharp JM, 1997. Human bronhioloalveolar carcinoma contains a protein related antigenically to jaagsiekte sheep retrovirus capsid. Meeting on Retroviruses. New York, USA: Cold Spring Harbour.
Drimeier D; Moojen V; Faccini GS; de Oliveira RT, 1998. Ciencia Rural, 28:147-150.
Dualde D, 1963. Estudio general y causistico de la adenomatosis pulmonar ovina en España. Proceedings of the 17th World Veterinary Congress, 1:347-355.
Dungal N; Gislason G; Taylor EL, 1938. Epizootic adenomatosis in the lung of sheep-comparisons with jaagsiekte, verminous pneumonia and progressive pneumonia. Journal of Comparative Pathology and Therapeutics, 51:46-68.
Eber A, 1899. Z. Tiermed, 3:161.
Enchev S; Tomov T; Ivano I, 1958. Pulmonary adenomatosis of sheep in Bulgaria. Izvestia Institute Patologiya na Zhivotnite, Sofia, 6:365-367.
Equiluz C; De Aluja AS, 1981. Neumonía intersticial progresiva (Maedi) y adenomatosis pulmonar en vísceras de óvidos decomisados. Vetrinaria México, 12:235-237.
Geisel O, 1975. Zur Morphologie der spontanen Lungadenomatose des Schafes. Zentralblat für Veterinä Medizin. B. 22:535-543.
Hecht SJ; Sharp JM; Demartini JC, 1996. Retroviral aetiopathogenesis of ovine pulmonary carcinoma: a critical appraisal. British Veterinary Journal, 152(4):395-409; 4 pp. of ref.
Herring AJ; Sharp JM; Scott FMM; Angus KW, 1983. Further evidence for a retrovirus as the aetiological agent of sheep pulmonary adenomatosis (Jaagsiekte). Veterinary Microbiology, 8:237-249.
Hunter AR; Munro R, 1983. The diagnosis, occurrence and distribution of sheep pulmonary adenomatosis in Scotland 1975 to 1981. British Veterinary Journal, 139:153-164.
Jakob W; Krauze H, 1965. Zum Auftreten der enzootischen lung adenomatose in Schafbestanden- Moneastschef fur Veterinarmedizin, 60:217-223.
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McFadyean J, 1938. Jaagsiekte. Journal of Comparative Pathology and Therapeutics, 51:78-84.
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Distribution References
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CABI, Undated. Compendium record. Wallingford, UK: CABI
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Christodoulous T, Tarlatis K, 1952. Chronic glandular pneumonia in the sheep (jaagsiekte). In: Deltion tes Hellenikes Kten. Hetaireias, 2 199-208.
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Geisel O, 1975. (Zur Morphologie der spontanen Lungadenomatose des Schafes). In: Zentralblat für Veterinä Medizin. B. 22 535-543.
Jakob W, Krauze H, 1965. (Zum Auftreten der enzootischen lung adenomatose in Schafbestanden-Moneastschef fur Veterinarmedizin)., 60 217-223.
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Madeira AC, 1949. (Adenocarcinoma em focos multiples do pulmao em um ovino). In: Revista de medicina veterinaria, 44 Lisboa, 95-100.
Marsh H, 1966. Progressive pneumonia of sheep in the United States and its relation to disease of the Jaagsiekte complex. [Proceedings Third Quadrennial Conference on Cancer: Lung tumours in animals, Perugia, Italy], [ed. by Sereril L]. 285-294.
McFadyean J, 1938. (Jaagsiekte). In: Journal of Comparative Pathology and Therapeutics, 51 78-84.
Moraillon P, Yalcin N, 1967. (Adenomatose pulmonaire des ovins en France). [Proceedings of the 18th World Veterinary Congress], 1 323-324.
Nobel TA, 1958. Pulmonary adenomatosis (jaagsiekte) in sheep with special reference to its occurrence in Israel. In: Refuah Veterinarith, 15 101-198.
OIE Handistatus, 2005. World Animal Health Publication and Handistatus II (dataset for 2004)., Paris, France: Office International des Epizooties.
OIE, 1998. World Animal Health in 1997., 1-2 Paris, France: Office International des Epizooties.
Schultz L, Somoza A, Weiland F, 1965. (Zum auftreten und zum tumour charakter der enzootischen lungadenomatose des schafes vergleichende unter suchungenin Chile und in der Bundesrepublik Deutschland). In: Deutsche tieraertliche Wochenschrift, 72 458-461.
Stevenson RG, Rehmutulla AJ, Thomsom RG, 1980. Pulmonary adenomatosis (Jaagsiekte) in sheep in Canada. In: Canadian Veterinary Journal, 21 267-268.
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