chicken anaemia

Identity

Top of page

Preferred Scientific Name

chicken anaemia

International Common Names

English: anemia dermatitis syndrome; avian anemia virus infection; avian infectious anaemia; avian infectious anemia; chicken anemia; chicken anemia agent, circovirus, avian infectious anemia virus, caa; chicken anemia virus infection; chicken infectious anaemia; chicken infectious anemia; hemorrhagic aplastic anemia syndrome; infectious chicken anaemia; infectious chicken anemia

Local Common Names

Sweden: blue wing disease

English acronym

CAV

Pathogen/s

Top of page

chicken anaemia virus

Overview

Top of page

Chicken anaemia, chicken infectious anaemia and blue wing disease all describe an immunosuppressive syndrome in poultry caused by chicken anaemia virus (CAV). The virus was first isolated in Japan by Yuasa et al. (1979). Reviews on CAV include Coombes and Crawford (1996), McNulty (1991), Schat and van Santen (2008) and Schat (2009).

CAV is a small and particularly hardy virus that belongs to the Gyrovirus genus of the family Circoviridae. A human virus has recently been assigned to the Gyrovirus genus (Sauvage et al., 2011). The Circoviridae also includes porcine circovirus (PCV) and psittacine beak and feather disease virus (PBFDV) which are members of the Circovirus genus and are morphologically and antigenically distinct from CAV (Meehan et al., 1992; Studdert, 1993).

CAV has been isolated in a significant number of countries and is considered to have a worldwide distribution including commercial poultry and in specific pathogen free (SPF) flocks (Fadly et al., 1994; O’Rourke et al., 1994). CAV may be transmitted vertically from parent to the chick causing a clinically apparent immunosuppressive disease (McNulty, 1991; McNulty et al., 1991) and horizontally from chicken to chicken resulting in an inapparent infection if transmission occurs after a few weeks of life.

Vertical transmission results in acute disease with clinical signs at 10-14 days of age with mortality peaks of 5-10% usual, but up to 60% mortality has been documented (Yuasa et al., 1979; Taniguchi et al., 1982; McNulty et al., 1991). Disease signs include weakness, depression, anorexia and stunting. Anaemia may be seen on non-feathered areas such as the combs and wattles, and skin lesions are also characteristic, especially on the wings (Yuasa et al., 1979; Engström et al., 1988; McNulty, 1991). The disease appears to inhibit blood cell production, probably by affecting stem cell development, hence anaemia, with lowered white cell and platelet counts. Lymphoid tissues are also affected.

Vertical transmission appears to be of particular importance in intensive operations if breeding birds become infected. The breeders transmit CAV to the chicks and the developing chick develops signs within 2 weeks of hatching. Disease in the resultant chicks is severe. Vertical spread can be controlled by vaccination of the breeding hens with common vaccination regimes being controlled exposure to the wild-type virus. Such vaccination protocols control vertical transmission but increase the probability of horizontal transmission.

Horizontal transmission occurring after a few weeks of age does not result in overt signs but studies on CAV-antibody positive and CAV-antibody negative flocks have indicated that the economic impact is still quite substantial but inapparent.

Host Animals

Top of page

Animal name	Context	Life stage	System
Gallus	Domesticated host	Poultry: Day-old chick\|Poultry/Young poultry\|Poultry/Mature female
Gallus gallus domesticus (chickens)	Domesticated host	Poultry: Day-old chick\|Poultry/Young poultry\|Poultry/Mature female

Hosts/Species Affected

Top of page

CAV is a pathogen of domestic fowl; however, antibody to CAV has also been found in quail but not duck, pigeon or crow (Farkas et al., 1999). It is unlikely that CAV infects other avian species. In the laboratory CAV can only be grown in a limited number of transformed chicken cell lines (Yuasa, 1983, McNulty, 1991; Coombes and Crawford, 1998) and has not been successfully grown in other cell lines, suggesting that CAV is species-specific. At this stage there is no evidence of infection of humans or other animal species and hence no health implications for humans or other species.

Similarly, there is no evidence of insect vectors, other animal carriers or environmental reservoirs of the virus. Fomites (i.e. inanimate objects), dust (due to the stability of the virus) and worker movements may play a role in transmission.

There do not appear to be any predisposing host factors to infection other than lack of maternal antibody to CAV. Non-immune poultry become infected and poultry that have previously been exposed to CAV (i.e. possessing CAV antibodies) do not become infected. However, the age of the bird has a marked effect on the development of clinical signs. With vertical transmission the hatched chicks develop signs from about 10 to 14 days of age with mortality rates up to 60%. Birds infected horizontally after about 14 days old do not exhibit clinical signs but production may be affected.

Systems Affected

Top of page

blood and circulatory system diseases of poultry
multisystemic diseases of poultry

Distribution

Top of page

Antibodies to CAV and the virus itself have been isolated in a significant number of countries/states/regions. Results have generally been reported in the scientific literature and hence will not represent the totality of CAV infections worldwide. In fact, CAV is now recognised as being of worldwide distribution and is usually found when looked for. It is easier to detect antibody to CAV in birds but the definitive result is isolation of the virus. Growth of CAV in cell culture presents many difficulties hence many reports of CAV are based on antibody evidence. CAV has been found in commercial domestic fowl, in SPF flocks and in village chickens (Fadly et al., 1994; O’Rourke et al., 1994).

Distribution Table

Top of page

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 10 Jan 2020

Continent/Country/Region	Distribution	Reference	Notes
Africa
Egypt	Present	Zaki and El-Sanousi (1994)
South Africa	Present	Wicht and Maharaj (1993)
Asia
China	Present	Xiao Xin Li et al. (1994) Zhou WenPing et al. (1997)
-Shandong	Present	Chen JiangLi et al. (1999)
India	Present	Bhatt et al. (2011)
-Tamil Nadu	Present	Venugopalan et al. (1994)
Iran	Present	Aghakhan et al. (1994)
Israel	Present	Malkinson et al. (1990)
Japan	Present	Yuasa et al. (1979)
Malaysia	Present	Rozanah et al. (1995)
Saudi Arabia	Present	Al-Ankari et al. (1996)
South Korea	Present	Seong HwanWoo et al. (1996)
Taiwan	Present	Lu et al. (1993)
Thailand	Present	Tantaswasdi et al. (1996)
Europe
Bosnia and Herzegovina	Present	Ragland et al. (1998)
Croatia	Present	Novak et al. (1996) Ragland et al. (1998)
Denmark	Present	Jørgensen et al. (1994) Jørgensen et al. (1995)
Finland	Present	Rikula (1994)
France	Present	Drouin et al. (1992)
Germany	Present, Widespread	Bülow (1988)
Hungary	Present, Widespread	Farkas et al. (1991) Farkas et al. (1992) Drén et al. (1996)
Italy	Present	Anon (1997)
Netherlands	Present, Widespread	Steenhuisen et al. (1994)
Slovakia	Present	Jantošović et al. (1992)
Slovenia	Present	Ragland et al. (1998)
Sweden	Present	Engström (1999)
Switzerland	Present	Hoop et al. (1992)
United Kingdom	Present, Widespread	McNulty et al. (1988) Chettle et al. (1989)
North America
United States	Present, Widespread	Lucio et al. (1990)
-Arkansas	Present	Rozypal et al. (1997)
-Georgia	Present, Widespread	Goodwin et al. (1989)
Oceania
Australia	Present	CABI (Undated)	Present based on regional distribution.
-New South Wales	Present, Widespread	Firth and Imai (1990) Connor et al. (1991)
New Zealand	Present	Stanislawek (1992) Stanislawek and Howell (1994)
South America
Bolivia	Present	Buscaglia et al. (1994)
Brazil	Present, Widespread	Brentano et al. (1991)
Chile	Present	Toro et al. (1994)
Venezuela	Present	Urdaneta V. et al. (1998)

Pathology

Top of page

The characteristic histopathological findings in CAV-infected chicks include a change from a red colour to a yellow colour to a white colour in the bone marrow and intense atrophy of the lymphoid organs, including the thymus, bursa of Fabricius, and to a lesser extent, the spleen, with a depletion of lymphocytes, followed by hyperplasia of reticular cells. This results in a severely immunocompromised state that increases the chicks' susceptibility to secondary bacterial infections and ultimately shortens life expectancy (Taniguchi et al., 1982). Haemorrhages throughout the skeletal muscle and subcutaneous tissue are also a common finding (Yuasa et al., 1979; Taniguchi et al., 1982, 1983; Engström et al., 1988). These characteristic features are usually observed in the second week of infection (McNulty, 1991).

CAV infection is characterised by severe aplasia of the bone marrow with haematopoietic cells reduced severely or replaced almost completely by adipose tissue, giving the bone marrow a watery texture and its characteristic yellow colour (Taniguchi et al., 1982). The changes occurring in the bone marrow cause a severe anaemia.

Diagnosis

Top of page

Typical signs of weakness, depression, anorexia and stunting combined with obvious anaemia characterised by pale comb and wattles, eyelids and legs and a pale carcass. Skin lesions, commonly on the wings, are also observed.

A pale watery bone marrow, watery blood with a decreased haematocrit (red and white cells and platelets are reduced) is evident. Haematocrit values of 27% (normal range 32-37.5%) and below are commonly used to identify infected chicks (Yuasa and Imai, 1986) with values as low as 10% being recorded (Taniguchi et al., 1982).

From 16 days post-infection, recovering birds will exhibit juvenile forms of erythrocytes, thrombocytes and granulocytes in the blood, characterised by an increase of 30% or more of immature blood cells (Taniguchi et al., 1983).

Detection of CAV is most readily achieved by polymerase chain reaction- (PCR) based tests (Schat and Santen, 2008). These have been used not only to detect CAV in experimental work and in the field (Cardona et al., 2000; Hailemariam et al., 2008) but also to test for CAV contamination in poultry vaccines (Amer et al., 2011; Hermann et al., 2012). Antibodies to CAV can be detected by ELISA (Todd et al., 1999); commercial ELISA tests are available.

List of Symptoms/Signs

Top of page

Sign	Life Stages	Type
Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed	Poultry:Day-old chick,Poultry:Young poultry	Sign
General Signs / Cyanosis, blue skin or membranes	Poultry:Day-old chick,Poultry:Young poultry	Diagnosis
General Signs / Generalized weakness, paresis, paralysis	Poultry:Day-old chick,Poultry:Young poultry	Sign
General Signs / Increased mortality in flocks of birds	Poultry:Day-old chick,Poultry:Young poultry	Sign
General Signs / Lack of growth or weight gain, retarded, stunted growth	Poultry:Day-old chick,Poultry:Young poultry	Diagnosis
General Signs / Pale comb and or wattles in birds	Poultry:Day-old chick,Poultry:Young poultry	Diagnosis
General Signs / Pale mucous membranes or skin, anemia	Poultry:Day-old chick,Poultry:Young poultry	Diagnosis
General Signs / Petechiae or ecchymoses, bruises, ecchymosis	Poultry:Day-old chick,Poultry:Young poultry	Diagnosis
General Signs / Sudden death, found dead	Poultry:Day-old chick,Poultry:Young poultry	Sign
General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift		Sign
General Signs / Weight loss		Sign
Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless	Poultry:Day-old chick,Poultry:Young poultry	Sign

Disease Course

Top of page

Typical signs observed at the onset of clinical disease (10-14 days post-hatching) include weakness, depression, anorexia and stunting. Anaemia is noticeable on the non-feathered areas such as the comb and wattles, eyelids and legs and the carcass appears quite pale.

Clinically infected birds fail to thrive and may be runted/stunted. CAV infection reduces the effectiveness of the immune system and birds may become adventitiously infected with secondary bacterial pathogens. Mortality peaks in the third week of life.

There is no specific treatment for infected birds but culling of birds is appropriate.

Horizontally infected birds do not exhibit any signs and the only evidence of infection may be a drop in production parameters; however, very careful analysis is required to demonstrate such a decrease.

Epidemiology

Top of page

Isolates of CAV do not differ significantly in pathogenicity and all produce anaemia in 100% of inoculated 1-day-old chicks (Yuasa and Imai, 1986; McNulty et al., 1989, 1990; Brentano et al., 1991; Connor et al., 1991). CAV isolates appear to be antigenically similar suggesting that there is one serotype of CAV worldwide (McNulty et al., 1990; Connor et al., 1991) but it is possible to distinguish CAV isolates using restriction endonuclease analysis of amplified DNA (Todd et al., 1992) or other DNA analytical techniques.

CAV can be transmitted vertically from the parent to the chick (McNulty, 1991; McNulty et al., 1991) and horizontally from chicken to chicken, resulting in clinical and subclinical infections, respectively. Vertical infection occurs when breeder flocks with no previous exposure to CAV become infected as they come into egg production. After hatching the virus causes a disease that is acute at onset with clinical signs appearing at 10-14 days of age. Mortality peaks within the third week of life, usually from 5% to 10% but spikes up to 60% have been recorded (Yuasa et al., 1979; Taniguchi et al., 1982; McNulty et al., 1991). Chicks hatching from eggs over a 3-6 week period are affected. After this time the breeder flocks develop sufficient CAV antibody to stop transmitting the virus through the egg (McNulty, 1991), instead maternal antibody to CAV is transmitted and chicks are protected during the first critical weeks of life. Thus vaccination of breeders provides good protection from clinical CAV infection.

Horizontal infections occur in older chickens lacking maternal antibody to CAV. Virus is excreted by a small number of vertically infected hatch mates and acquired via the faecal-oral route or may be introduced via an external source such as on workers' boots or clothing. CAV is particularly hardy and survives in poultry houses for a considerable period of time. Clinical signs do not develop but the growth and health of the birds may be affected (McNulty et al., 1991).

Seasonal variations in the incidence of subclinical/horizontal CAV infection have been reported in Denmark, possibly due to better cleanout between flocks and hence virus inactivation (Jörgensen et al., 1994; 1995a; 1995b).

Impact: Economic

Top of page

The economic impact of CAV infection is twofold, related to the mode of infection. Vertical transmission results in clinical signs, reduced production with mortality of 5-10%, with spikes up to 60%. Vaccination of breeding birds is cost effective but specific dollar figures regarding losses and costs of vaccination are not available. Such figures could be calculated for individual commercial operations based on mortality figures of 5-10%. It should be remembered that CAV infection also interferes with the effectiveness of vaccination programs for other avian pathogens with concomitant increases in other diseases, e.g. IBDV. These factors would also need to be considered when calculating the economic importance and impact of CAV infection.

Horizontal transmission does not lead to clinical signs or death but production is significantly affected. Horizontal infections are hidden as the worldwide distribution of CAV and the non-evident nature of horizontal infections makes analysis difficult. Vaccination of all birds to control horizontal transmission is a significant impost but in situations where clinical CAV exists, it may be a very useful control mechanism, i.e. complete eradication of CAV from flocks may have substantial economic benefits.

Economic Impact of CAV on Commercial Broiler Production in the UK

	Clinical Infection	Subclinical Infection
Net Income	17.3-19.6% lower	13.0% lower
Average Bird Weight	3.3-3.5% lower	2.5% lower
Mortality	2.0-2.5% higher	Not Determined

(from McIlroy et al., 1992; McNulty et al., 1991 - see also Coombes and Crawford, 1996).

Zoonoses and Food Safety

Top of page

CAV appears to be restricted to poultry and there is no current evidence of CAV being able to infect or replicate in any other species. As such, CAV is not considered a zoonosis and there are no direct food safety implications.

Vertical CAV infection leads to immunosuppression of the infected chick, reducing the effectiveness of vaccination programs and increasing the likelihood of a pool of adventitious infections in the flock. As such, clinical CAV infection may reduce the overall health of a flock and increase the chances of other diseases in the flock that may have human and food safety implications.

Disease Treatment

Top of page

CAV is a virus and as such there is no antibiotic therapy available or other specific treatment. Treatment of symptoms could be employed but in commercial situations culling is the more likely approach. Control of infection by vaccination or other measures is the only means available to limit spread of CAV infections.

Prevention and Control

Top of page

Farm-Level Control

CAV is a particularly hardy virus and difficult to eradicate from the housing environment. It is resistant to high temperatures and many commonly used disinfectants. The use of rigorous cleaning out methods combined with hypochlorite, iodoform or formalin is recommended. Virus is excreted in faeces so scrupulous attention to clothing and footwear is required by personnel and control of dusts may be important.

National and International Control Policy

Quarantine may be an effective approach but is beset with difficulties due to the resistance of CAV to inactivation and its persistence in the environment.

Immunization and Vaccines

The only viable veterinary measure is vaccination either through exposure of breeders to the wild-type virus (Controlled Exposure) or with an attenuated vaccine. Vaccination of broilers would be dependent on economic factors and the demonstration of production losses associated with vertical transmission.

Vaccination strategies are based on the vaccination of breeders to prevent vertical transmission and horizontal transmission of CAV to chicks (Schat and van Santen, 2008).

Controlled exposure of breeders has the advantage of being cheap but may increase the degree of horizontal CAV infection with concomitant and hidden reduction in production of older birds.

Live attenuated CAV vaccines are commercially available for vaccination of breeders from a young age e.g. six weeks, and up to six weeks prior to lay. Vaccination later than this could result in inadequate antibody levels in the breeders, putting progeny at risk. The live vaccines should be administered according to each manufacturer’s instructions, as recommended routes vary.

References

Top of page

Aghakhan SM; Abshar N; Fereidouni SRN; Marunesi C; Khodashenas M, 1994. Studies on avian viral infections in Iran. Archives de l'Institut Razi, No. 44/45:1-10; 14 ref.

Al-Ankari AS; Awaad MHH; El-Shazly MO; Al-Ramadan MA, 1996. Chicken anaemia virus outbreak in chickens in Saudi Arabia. Veterinary Medical Journal Giza, 44(3):557-562; 11 ref.

Amer HM; Elzahed HM; Elabiare EA; Badawy AA; Yousef AA, 2011. An optimized polymerase chain reaction assay to identify avian virus vaccine contamination with Chicken anemia virus. Journal of Veterinary Diagnostic Investigation, 23(1):34-40. http://vdi.sagepub.com/content/23/1/34.full

Anon., 1997. XXXV Meeting of the Italian Society of Avian Diseases - Immunosuppressive factors in poultry husbandry, Forli, Italy, 10-11 October 1996. Selezione Veterinaria, 8-9:537-858.

Bhatt P; Shukla SK; Mahendran M; Dhama K; Chawak MM; Kataria JM, 2011. Prevalence of chicken infectious anaemia virus (CIAV) in commercial poultry flocks of Northern India: a serological survey. Transboundary and Emerging Diseases, 58(5):458-460. http://onlinelibrary.wiley.com/doi/10.1111/j.1865-1682.2011.01215.x/abstract

Brentano L; Mores N; Wentz I; Chandratilleke D; Schat KA, 1991. Isolation and identification of chicken infectious anemia virus in Brazil. Avian Diseases, 35(4):793-800; 23 ref.

Buchholz U; Bülow Vvon, 1994. Characterization of chicken anaemia virus (CAV) proteins. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 366-375; [4th Symposium of the World Veterinary Poultry Association]; 21 ref.

Buscaglia C; Crosetti CF; Nervi P, 1994. Identification of chicken infectious anaemia, isolation of the virus and reproduction of the disease in Argentina. Avian Pathology, 23(2):297-304; 14 ref.

Bülow Vvon, 1988. Unsatisfactory sensitivity and specificity of indirect immunofluorescence tests for the presence or absence of antibodies to chicken anaemia agent (CAA) in sera of SPF and broiler breeder chickens. Journal of Veterinary Medicine, B (Infectious Diseases, Immunology, Food Hygiene, Veterinary Public Health), 35(8):594-600; 19 ref.

Cardona CJ; Oswald WB; Schat KA, 2000. Distribution of chicken anaemia virus in the reproductive tissues of specific-pathogen-free chickens. Journal of General Virology, 81(8):2067-2075.

Chandratilleke D; O'Connell P; Schat KA, 1991. Characterization of proteins of chicken infectious anemia virus with monoclonal antibodies. Avian Diseases, 35(4):854-862; 22 ref.

Chen JL; Xin JQ; Song XL; Zhou FH; Wang ZX; Zhang LB, 1999. Restriction fragment length polymorphism analysis of Shandong isolates of chicken anaemia virus. Chinese Journal of Veterinary Science and Technology, 29(1):18-20.

Chettle NJ; Eddy RK; Wyeth PJ; Lister SA, 1989. An outbreak of disease due to chicken anaemia agent in broiler chickens in England. Veterinary Record, 124(9):211-215; 28 ref.

Claessens JAJ; Schrier CC; Mockett APA; Jagt EHJM; Sondermeijer PJA, 1991. Molecular cloning and sequence analysis of the genome of chicken anaemia agent. Journal of General Virology, 72(8):2003-2006; 13 ref.

Connor TJ; McNeilly F; Firth GA; McNulty MS, 1991. Biological characterisation of Australian isolates of chicken anaemia agent. Australian Veterinary Journal, 68(6):199-201; 21 ref.

Coombes AL; Crawford GR, 1996. Chicken anaemia virus: a short review. World's Poultry Science Journal, 52(3):267-277; 56 ref.

Coombes AL; Crawford GR, 1998. Recommended storage and resuscitation conditions for the MDCC-MSB1 cell line. Avian Diseases, 42(1):168-172; 7 ref.

Douglas AJ; Phenix K; Mawhinney KA; Todd D; Mackie DP; Curran WL, 1995. Identification of a 24 kDa protein expressed by chicken anaemia virus. Journal of General Virology, 76(7):1557-1562; 21 ref.

Drén C; Farkas T; Németh I, 1996. Serological survey on the prevalence of chicken anaemia virus infection in Hungarian chicken flocks. Veterinary Microbiology, 50(1/2):7-16; 32 ref.

Drouin P; Picault JP; Plassiart G; Cherel Y; Toquin D; Toux TY; Guittet M; Bennejean G; Wyers M, 1992. Blue wing disease in chickens: first report in France. Recueil de Médecine Vétérinaire, 168(5):331-339; 49 ref.

Engström BE, 1999. Prevalence of antibody to chicken anaemia virus (CAV) in Swedish chicken breeding flocks correlated to outbreaks of blue wing disease (BWD) in their progeny. Acta Veterinaria Scandinavica, 40(2):97-107; 44 ref.

Engström BE; Fossum O; Luthman M, 1988. Blue wing disease of chickens: experimental infection with a Swedish isolate of chicken anaemia agent and an avian reovirus. Avian Pathology, 17(1):33-50; 19 ref.

Fadly AM; Motta JV; Witter RL; Nordgren RM, 1994. Epidemiology of chicken anemia virus in specific-pathogen-free chicken breeder flocks. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 447-455; [4th Symposium of the World Veterinary Poultry Association]; 14 ref.

Farkas T; Drén C; Németh I; Dobos-Kovács M; Povazsán J; Sághy E, 1992. Isolation of chicken anaemia virus from broiler chickens. Acta Veterinaria Hungarica, 40(3):207-223; [6 pl.]; 36 ref.

Farkas T; Maeda K; Sugiura H; Kai K; Hirai K; Otsuki K; Hayashi T, 1999. A serological survey of chickens, Japanese quail, pigeons, ducks and crows for antibodies to chicken anaemia virus (CAV) in Japan. Magyar állatorvosok Lapja, 121(8):456-458; [Article originally appeared in Avian Pathology (1998), vol. 27, no. 3, pp. 316-320 (En)].

Farkas T; Povazsán J; Dobos-Kovács M; Sághy E; Németh I; Drén C, 1991. Isolation of chicken anaemia virus from broiler chickens in Hungary. Magyar állatorvosok Lapja, 46(11):661-668; 34 ref.

Firth GA; Imai K, 1990. Isolation of chicken anaemia agent from Australian poultry. Australian Veterinary Journal, 67(8):301-302; 11 ref.

Goodwin MA; Brown J; Miller SI; Smeltzer MA; Steffens WL; Waltman WD, 1989. Infectious anemia caused by a parvovirus-like virus in Georgia broilers. Avian Diseases, 33(3):438-445; 31 ref.

Goodwin MA; Steffens WL; Davis JF; Brown J; Latimer KS; Dickson TG, 1991. Diagnoses of infections by the so-called chick anemia agent: anaemia and direct transmission electron microscopic detection of virus. Avian Diseases, 35(4):869-871; 25 ref.

Goryo M; Suwa T; Matsumoto S; Umemura T; Itakura C, 1987. Serial propagation and purification of chicken anaemia agent in MDCC-MSB1 cell line. Avian Pathology, 16(1):149-163; [7 fig.]; 18 ref.

Hermann J; Koski D; Taylor S; Gatewood D, 2012. Evaluation of the analytical sensitivity of a polymerase chain reaction assay for the detection of chicken infectious anemia virus in avian vaccines. Biologicals, 40(4):266-269. http://www.sciencedirect.com/science/journal/10451056

Hoop RK; Guscetti F; Keller B, 1992. An outbreak of infectious anaemia among broilers in Switzerland. Schweizer Archiv für Tierheilkunde, 134(10):485-489; 32 ref.

Jantosovic J; Konrád V; Kusev J; Skardová I; Varga G; Vrabec V, 1992. Infectious anaemia in chickens. Veterinárství, 42(10):374-375.

Jeurissen SHM; Janse ME; Roozelaar DJ van; Koch G; Boer GF de, 1992. Susceptibility of thymocytes for infection by chicken anaemia virus is related to pre- and post-hatching developments. Developmental Immunology, 2:123-129.

Jörgensen PH; Otte L; Bisgaard M; Nielsen OL, 1995. Seasonal variation in the incidence of subclinical horizontally transmitted infection with chicken anemia virus in Danish broilers and broiler breeders. Archiv für Geflügelkunde, 59(3):165-168; 11 ref.

Jörgensen PH; Otte L; Nielsen OL; Bisgaard M, 1994. Investigations of the epidemiology and economical impact of chicken anaemia virus infection in Danish broilers and broiler breeders. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 438-446; [4th Symposium of the World Veterinary Poultry Association]; 15 ref.

Jörgensen PH; Otte L; Nielsen OL; Bisgaard M, 1995. Influence of subclinical virus infections and other factors on broiler flock performance. British Poultry Science, 36(3):455-463; 11 ref.

Kato A; Fujino M; Nakamura T; Ishihama A; Otaki Y, 1995. Gene organization of chicken anemia virus. Virology (New York), 209(2):480-488; 28 ref.

Koch G; Roozelaar DJvan; Verschueren CAJ; Eb AJvan der; Noteborn HM, 1995. Immunogenic and protective properties of chicken anaemia virus proteins expressed by baculovirus. Vaccine, 13(8):763-770; 37 ref.

Koch G; Roozelaar DJvan; Verschueren CAJ; Eb AJvan der; Noteborn MHM, 1994. The formation of neutralising epitopes of chicken anaemia virus requires the synthesis of its proteins VP1 and VP2 in the same cell. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 498-506; [4th Symposium of the World Veterinary Poultry Association]; 29 ref.

Li XX; Xu WY; Tang GY, 1994. Isolation and identification of the chicken anemia virus and serological survey in China. In: Kaleta EF, ed. Proceedings, International Symposium on Infectious Bursal Disease and Chicken Infectious Anaemia, Rauischholzhausen, Germany, 21-24 June 1994, 429-433.

Lu YS; Tsai HJ; Kwang MJ; Tseng CS, 1993. Chicken infectious anemia in Taiwan: virus isolation and antibody survey. Journal of the Chinese Society of Veterinary Science, 19(3):137-146; 30 ref.

Lucio B; Schat KA; Shivaprasad HL, 1990. Identification of the chicken anemia agent, reproduction of the disease, and serological survey in the United States. Avian Diseases, 34(1):146-153; 19 ref.

Lucio B; Schat KA; Taylor S, 1991. Direct binding of protein A, protein G, and anti-IgG conjugates to chicken infectious anemia virus. Avian Diseases, 35(1): 180-185.

Malkinson M; Davidson I; Weisman J, 1990. Serological survey of antibodies to chicken anemia agent in domestic poultry in Israel. Israel Journal of Veterinary Medicine, 45(3):188-189; [14th Symposium of Veterinary Medicine, Koret School, Israel, 26-28 June, 1988.].

McNulty MS, 1991. Chicken anaemia agent: a review. Avian Pathology, 20(2):187-203; 72 ref.

McNulty MS; Connor TJ; McNeilly F; Kirkpatrick KS; McFerran JB, 1988. A serological survey of domestic poultry in the United Kingdom for antibody to chicken anaemia agent. Avian Pathology, 17(2):315-324; [1 pl.]; 10 ref.

McNulty MS; Connor TJ; McNeilly F; McLoughlin MF; Kirkpatrick KS, 1990. Preliminary characterisation of isolates of chicken anaemia agent from the United Kingdom. Avian Pathology, 19(1):67-73; 13 ref.

McNulty MS; Connor TJ; McNeilly F; Spackman D, 1989. Chicken anemia agent in the United States: isolation of the virus and detection of antibody in broiler breeder flocks. Avian Diseases, 33(4):691-694; 17 ref.

McNulty MS; McIlroy SG; Bruce DW; Todd D, 1991. Economic effects of subclinical chicken anaemia agent infection in broiler chickens. Avian Diseases, 35:263-268.

Meehan BM; Todd D; Creelan JL; Earle JAP; Hoey EM; McNulty MS, 1992. Characterization of viral DNAs from cells infected with chicken anaemia agent: sequence analysis of the cloned replicative form and transfection capabilities of cloned genome fragments. Archives of Virology, 124(3-4):301-319; 39 ref.

Noteborn MHM; Boer GFde; Roozelaar DJvan; Karreman C; Kranenburg O; Vos JG; Jeurissen SHM; Hoeben RC; Zantema A; Koch G; Ormondt Hvan; Eb AJvan der, 1991. Characterization of cloned chicken anemia virus DNA that contains all elements for the infectious replication cycle. Journal of Virology, 65(6):3131-3139; 52 ref.

Noteborn MHM; Koch G, 1995. Chicken anaemia virus infection: molecular basis of pathogenicity. Avian Pathology, 24(1):11-31; 113 ref.

Noteborn MHM; Koch G; Eb AJvan der, 1994. The molecular biology of chicken anemia virus, an introduction. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 341-348; [4th Symposium of the World Veterinary Poultry Association]; 38 ref.

Noteborn MHM; Todd D; Verschueren CAJ; Gauw HWFMde; Curran WL; Veldkamp S; Douglas AJ; McNulty MS; Eb AJvan der; Koch G, 1994. A single chicken anemia virus protein induces apoptosis. Journal of Virology, 68(1):346-351; 38 ref.

Novak R; Mazija H; Ragland WL, 1996. Chicken anaemia virus in broilers and their parents in Croatia. Veterinarska Stanica, 27(6):323-325; 11 ref.

O'Rourke D; Michalski WP; Bagust TJ, 1994. Chicken anaemia virus antibody ELISA reactions: practical experiences and problems in high-security SPF poultry flocks. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 456-464; [4th Symposium of the World Veterinary Poultry Association]; 12 ref.

Otaki Y; Tajima M; Saito K; Nomura Y, 1988. Immune response of chicks inoculated with chicken anemia agent alone or in combination with Marek's disease virus or turkey herpesvirus. Japanese Journal of Veterinary Science, 50(5):1040-1047; 20 ref.

Ragland WL; Mazija H; Cvelic-Cabrilo V; Savic V; Novak R; Pogacnik M, 1998. Immune suppression [to Newcastle disease immunization] of commercial broilers in Croatia, Slovenia, and Bosnia and Herzegovina from 1981 to 1991. Avian Pathology, 27(2):200-204; 24 ref.

Rikula U, 1994. Vaccination of poultry in Finland. Suomen Eläinlääkärilehti, 100(12):709-713; 5 ref.

Rozanah AS; Aini I; Al-Ajeeli KS; Jalila A; Salim NB, 1995. Detection of chicken anaemia virus in flocks of commercial chicken in Malaysia. Jurnal Veterinar Malaysia, 7(2):77-79; 10 ref.

Rozypal TL; Skeeles JK; Dash JK; Anderson EJ; Beasley JN, 1997. Identification and partial characterization of Arkansas isolates of chicken anemia virus. Avian Diseases, 41(3):610-616; 19 ref.

Sauvage V; Cheval J; Foulongne V; Gouilh MA; Pariente K; Manuguerra JC; Richardson J; Dereure O; Lecuit M; Burguiere A; Caro V; Eloit M, 2011. Identification of the first human gyrovirus, a virus related to chicken anemia virus. Journal of Virology, 85:7948-7950.

Schat KA, 1994. Influence of infection with infectious bursal disease virus or chicken infectious anaemia virus on the avian immune system. International symposium on Infectious Bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994, 17-21; [4th Symposium of the World Veterinary Poultry Association]; 34 ref.

Schat KA, 2009. Chicken anemia virus. Current Topics in Microbiology and Immunology, 331:151-183.

Schat KA; Santen VNvan, 2008. .

Seong HwanWoo; Song ChangSeon; Kim JaiHong; Kim SunJung, 1996. Detection of chicken infectious anaemia virus by a polymerase chain reaction and immunoperoxidase staining with a monoclonal antibody. RDA Journal of Agricultural Science, Veterinary, 38(2):699-706; 39 ref.

Stanislawek WL, 1992. Chicken anaemia agent (CAA)- a New Zealand perspective. Publication - Veterinary Continuing Education, Massey University, No. 147:41-48; [Proceedings Solvay chicken health course, Massey University, 1992]; 11 ref.

Stanislawek WL; Howell J, 1994. Isolation of chicken anaemia virus from broiler chickens in New Zealand. New Zealand Veterinary Journal, 42(2):58-62; 14 ref.

Steenhuisen W; Jagt HJM; Schrier CC, 1994. The use of live attenuated CAV vaccine in breeder flocks in the Netherlands. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 482-497; [4th Symposium of the World Veterinary Poultry Association]; 4 ref.

Studdert MJ, 1993. Circoviridae: new viruses of pigs, parrots and chickens. Australian Veterinary Journal, 70(4):121-122; 13 ref.

Taniguchi T; Yuasa N; Maeda M; Horiuchi T, 1982. Haematopathological changes in dead and moribund chicks induced by chicken anaemia agent. National Institute of Animal Health Quarterly (Japan), 22:61-69.

Taniguchi T; Yuasa N; Maeda M; Horiuchi T, 1983. Chronological observations on hemato-pathological changes in chicks inoculated with chicken anemia agent. National Institute of Animal Health Quarterly, Japan, 23(1):1-12; 13 ref.

Tantaswasdi U; Sirivan P; Chaisingha A, 1996. Virological and serological studies of chicken anaemia virus in Thailand. Journal of the Thai Veterinary Medical Association, 47(3/4):45-56; 23 ref.

Todd D; Douglas AJ; Phenix KV; Curran WL; Mackie DP; McNulty MS, 1994. Characterisation of chicken anaemia virus. International symposium on infectious bursal disease and chicken infectious anaemia, Rauischholzhausen, Germany, 21-24 June, 1994., 349-363; [4th Symposium of the World Veterinary Poultry Association].

Todd D; Mawhinney KA; Graham DA; Scott ANJ, 1999. Development of a blocking enzyme-linked immunosorbent assay for the serological diagnosis of chicken anaemia virus. Journal of Virological Methods, 82(2):177-184; 17 ref.

Todd D; Mawhinney KA; McNulty MS, 1992. Detection and differentiation of chicken anemia virus isolates by using the polymerase chain reaction. Journal of Clinical Microbiology, 30(7):1661-1666; 17 ref.

Todd D; Niagro FD; Ritchie BW; Curran W; Allan GM; Lukert PD; Latimer KS; Steffens WL; McNulty MS, 1991. Comparison of three animal viruses with circular single-stranded DNA genomes. Archives of Virology, 117(1-2):129-135; 17 ref.

Toro H; McNulty MS; Hidalgo H; Rosende S; Connor TJ, 1994. Detection of chicken anemia virus antibodies in four poultry operations in Chile. Preventive Veterinary Medicine, 21(1):103-106; 12 ref.

Urdaneta VSH; Andrade VLF; Parra O, 1998. Detection of anaemia and serum antibodies to chicken anaemia virus in broilers in the towns of Mara and La Canada de Urdaneta, Zulia State, Venezuela. Revista Cientifica, Facultad de Ciencias Veterinarias, Universidad del Zulia, 8(3):265-272; 31 ref.

Venugopalan AT; Elankumaran S; Raj GD; Manohar BM; Thangavelu A; Ravikumar G; Koteeswaran A; Raj AS, 1994. Isolation of chicken anaemia virus in Tamil Nadu. Indian Veterinary Journal, 71(4):411-412; 8 ref.

Wicht JV; Maharaj SB, 1993. Chicken anaemia agent in South Africa. Veterinary Record, 133(6):147-148; 1 ref.

Yuasa N, 1983. Propagation and infectivity titration of the Gifu-1 strain of chicken anemia agent in a cell line (MDCC-MSB1) derived from Marek's disease lymphoma. National Institute of Animal Health Quarterly, Japan, 23(1):13-20; 18 ref.

Yuasa N; Imai K, 1986. Pathogenicity and antigenicity of eleven isolates of chicken anaemia agent (CAA). Avian Pathology, 15(4):639-645; 11 ref.

Yuasa N; Taniguchi T; Yoshida I, 1979. Isolation and some characteristics of an agent inducing anaemia in chicks. Avian Diseases, 23(2):366-385.

Yuasa N; Yoguchi T; Furuta K; Yoshida I, 1980. Maternal antibody and its effects on the susceptibility of chickens to chicken anaemia agent. Avian Diseases, 24(1):202-209.

Zaki MM; El-Sanousi AA, 1994. Chicken anaemia agent in Egypt: I. A serological survey of antibody against chicken anaemia agent in some commercial chicken flocks using indirect immunofluorescent technique. Veterinary Medical Journal Giza, 42(3):53-58; 16 ref.

Zerihun Hailemariam; Omar AR; Mohd Hair-Bejo; Giap TanChing, 2008. Detection and characterization of chicken anemia virus from commercial broiler breeder chickens. Virology Journal, 5(128):(27 October 2008). http://www.virologyj.com/content/5/1/128

Zhou WP; Shen B; Yang B; Han SP; Wei L; Xiao BZ; Zhou J, 1997. Isolation and identification of chicken infectious anaemia virus in China. Avian Diseases, 41(2):361-364.