bovine adenoviruses infections

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Pathology

Lung from an animal experimentally infected with an adenovirus with large red areas of consolidation in the middle and caudal lobes.

NADC, ARS-USDA

Histopathology

Histopathology observed in a calf with a natural adenovirus infection. Note the intranuclear inclusions in a blood vessel epithelial cell (A) and in the epithelial cells of the bronchiole (B).

NADC, ARS-USDA

Identity

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Preferred Scientific Name

bovine adenoviruses infections

International Common Names

English: adenovirus infection in ruminants

Pathogen/s

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bovine adenoviruses

Overview

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Rowe et al. (1953) isolated a new virus from cultures of human adenoids. The currently accepted name, "adenovirus", was proposed for this group of viruses by Enders et al. (1956). The family Adenoviridae now comprises a well-defined group of viruses with wide distribution in nature. Adenovirus types are defined based on the species of origin of the virus and quantitative neutralization assays with antisera prepared in non-host species. The family Adenoviridae is currently divided into three genera, Mastadenovirus,Aviadenovirus, and Atadenovirus (Benkö et al., 2000).

Klein et al. (1959) reported the first isolation of a bovine adenovirus (BAdV). Bovine adenoviruses have been isolated from healthy cattle, but more often, the isolations are associated with some form of clinical disease. The preponderance of isolations from cattle with clinical disease is because this is the type sample submitted to diagnostic laboratories. Most adenovirus infections in cattle involve either the respiratory or gastrointestinal tracts. In addition there have been reports of adenovirus associated with conjunctivitis, keratoconjunctivitis, and weak calf syndrome. Currently the International Committee on Taxonomy of Viruses recognizes 10 types in cattle (Benkö et al., 2000). Strain Rus is being evaluated as a potential new type (Zakharchuk et al., 1993). The table shows prototype strains and origin.

SerotypeStrainReferenceBAdV-1No. 10Klein et al., 1959BAdV-2No. 19Klein et al., 1960BAdV-3WBR 1Darbyshire et al., 1965aBAdV-4THT/62Bartha and Áldásy, 1966BAdV-5B4/65Bartha and Áldásy, 1966BAdV-6671130Rondhuis, 1968BAdV-7FukuroiInaba et al., 1968BAdV-8Misk/67Bartha et al., 1970(BAdV-9)Sofia 4/67Guenov et al., 1970BAdV-1078-5371Horner et al., 1989(BAdV-11)RusZakharchuk et al., 1993

BAdVs were originally divided into two groups based on cultural and antigenic characteristics by Bartha (1969). Subgroup 1 contained BAdV 1, 2, and 3 with similarities to human and other mammalian adenoviruses. Subgroup 2 contained the atypical BAdV 4, 5, 6, 7, and 8 that could not replicate in kidney epithelial cells, produced noticeably different nuclear inclusion bodies, and lacked the common complement-fixing antigen found in members of the genus Mastadenovirus. Division was further supported after genomic analysis demonstrated marked differences in the two groups. The subgroup 1 BAdVs (BAdV-1 through -3 and -9) are members of the genus Mastadenovirus and the subgroup 2 BAdVs (BAdV-4 through -8) have been recently assigned to a proposed new Atadenovirus genus within the family Adenoviridae (Benkö and Harrach 1998; Benkö et al, 2000). BAdV 10 does not fit clearly into either genus (Maitz et al., 1998) but, based on genomic analysis, has been assigned to the genus Atadenovirus for now (Benkö et al., 2000).

Host Animals

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Animal name	Context	Life stage
Bos indicus (zebu)
Bos taurus (cattle)	Domesticated host; Experimental settings	Cattle & Buffaloes\|All Stages
Capra hircus (goats)
Ovis aries (sheep)	Domesticated host; Experimental settings	Sheep & Goats\|All Stages

Hosts/Species Affected

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Adenoviruses are generally confined to one host species or closely related species and are classified on the basis of species of origin and antigenic reactivity. Because bovine adenoviruses or closely related antigenic viruses have been isolated from a variety of other ruminant species (Belák and Palfi, 1974; Davies and Humphreys, 1977; Baber and Candy, 1981; Boros et al., 1985), the potential for infection across species exists among adenovirus isolates from ruminants.

Systems Affected

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digestive diseases of large ruminants
digestive diseases of small ruminants
multisystemic diseases of large ruminants
nervous system diseases of large ruminants
respiratory diseases of large ruminants
respiratory diseases of small ruminants

Distribution

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Bovine adenoviruses are found worldwide as indicated by either serology or virus isolation. Antibodies to adenoviruses have been demonstrated in sera in virtually every cattle population tested. Serum-virus neutralization tests have been used to detect adenovirus type-specific antibodies, and complement fixation and agar gel immunodiffusion tests have been used to detect the adenovirus group-specific antibody in serological surveys.

Distribution Table

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

Last updated: 10 Jan 2020

Continent/Country/Region	Distribution	Reference	Notes
Africa
Congo, Democratic Republic of the	Present	Eyanga et al. (1989)
Egypt	Present	Hafez and Krauss (1979)
Morocco	Present	Mahin et al. (1985)
Nigeria	Present	Obi and Taylor (1984)
Somalia	Present	Mani et al. (1978) CABI (Undated)
Togo	Present	Espinasse et al. (1980)
Zambia	Present	Ghirotti et al. (1991)
Zimbabwe	Present	Baber and Condy (1981)
Asia
Iran	Present	Afshar (1969)
Japan	Present	CABI (Undated a)	Present based on regional distribution.
-Honshu	Present, Widespread	Tanaka et al. (1968) CABI (Undated)
South Korea	Present	Cho et al. (1985) CABI (Undated)
Syria	Present	Giangaspero et al. (1992)
Turkey	Present, Widespread	Burgu and Akca (1982) Burgu and Toker (1985) Yonguç et al. (1988) CABI (Undated)
Europe
Austria	Present	Burki et al. (1978) Coulibaly (1990) Pernthaner et al. (1990) Peinhopf et al. (1996)
Belgium	Present	Mammerickx et al. (1989)
Bulgaria	Present, Widespread	Haralambiev and Azev (1969)
Croatia	Present	Župančić et al. (1984) Sabirović et al. (1987) Sabirović (1988)
Czechoslovakia	Present	Krpata (1978) Novak (1982)
Denmark	Present	Uttenthal et al. (1996) Tegtmeier et al. (1999)
Finland	Present	Sihvonen and Tuomi (1978)
Germany	Present, Widespread	Mayr et al. (1970) Kretzschmar (1973)
Hungary	Present, Widespread	Bartha et al. (1970) Bartha et al. (1984) Rusvai and Fodor (1998) Endre (1999) CABI (Undated)
Ireland	Present	Timoney (1971)
Italy	Present, Widespread	Cancellotti et al. (1976)
Netherlands	Present	Rondhuis (1968) Opdenbosch et al. (1986)
Norway	Present	Saxegaard and Bratberg (1971)
Poland	Present, Widespread	Buczek and Wrzolek-Lobocka (1977) Majewska et al. (1978)
Romania	Present	Istrate et al. (1983)
Russia	Present	CABI (Undated a)	Present based on regional distribution.
-Central Russia	Present	Shichkina et al. (1971) Kis (1977) Frolov (1984)
-Southern Russia	Present	Zhumabaev et al. (1993) CABI (Undated)
Switzerland	Present	Läuchli et al. (1990)
United Kingdom	Present, Widespread	Phillip and Sands (1972) CABI (Undated)
North America
Canada	Present	CABI (Undated a)	Present based on regional distribution.
-Ontario	Present	Bulmer et al. (1975) Thompson et al. (1981)
-Quebec	Present	Key and Derbyshire (1984) Richer et al. (1988)
-Saskatchewan	Present	Orr (1984)
Cuba	Present	Nuñez and Castell (1985)
Mexico	Present	Suzan et al. (1983) Ramírez R. and Trigo (1986)
United States	Present	CABI (Undated a)	Present based on regional distribution.
-Alabama	Present	Rossi et al. (1973)
-California	Present	Bibrack and McKercher (1971) Lehmkuhl et al. (1999)
-Idaho	Present	Stauber et al. (1976) Stauber et al. (1986)
-Iowa	Present	Lehmkuhl et al. (1975) Lehmkuhl and Gough (1977) CABI (Undated)
-Maryland	Present	Mohanty and Lillie (1970)
-Minnesota	Present	Reed et al. (1978) Baker et al. (1986) Baker et al. (1986a)
-Oregon	Present	Mattson (1973) Mattson et al. (1977) Mattson et al. (1988)
-Pennsylvania	Present	Welch and Dellers (1973)
-South Dakota	Present	Reed et al. (1978) Kirkbride (1992)
-Tennessee	Present	Lehmkuhl et al. (1998)
-Washington	Present	Stauber et al. (1986)
Oceania
Australia	Present	CABI (Undated a)	Present based on regional distribution.
-Queensland	Present	Wilcox (1969) Wilcox (1970) CABI (Undated)
New Zealand	Present	Thompson (1977) Horner et al. (1980)
South America
Argentina	Present	Carrillo et al. (1986)

Pathology

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Gross lesions in cattle are limited primarily to the respiratory and gastrointestinal tracts and consist of atelectasis and consolidation of the lungs and erosions, ulcerations and haemorrhage in the intestinal tract. Bronchiolar, mediastinal, and mesenteric lymph nodes are usually enlarged. Depending on adenovirus serotype, either epithelial or epithelial and vascular endothelial cells are the primary targets for viral cytopathology. Microscopically the basic lesion is bronchiolitis with necrosis and sloughing early and hyperplasia later in the course of the infection. Amphophilic, intranuclear inclusions are seen in swollen cells in the respiratory epithelium and sloughed in the lumen. Where the gastrointestinal tract is involved, the basic lesions are fibrinonecrotic plaques overlying foci of haemorrhage and necrosis. Amphophilic intranuclear inclusions are seen in enterocytes as well as in vascular endothelial cells.

Diagnosis

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Because adenoviruses can be isolated from apparently healthy cattle, isolation of adenoviruses from clinically sick calves does not necessarily mean that the isolated adenovirus type plays an aetiological role in the clinical disease. For adenovirus to be considered as the aetiologic agent in a particular disease, the antibody titre should be low at the onset of the infection and result in at least a four-fold increase in neutralizing antibodies to the virus type in question, either characteristic intranuclear inclusion bodies should be observed in tissues showing gross lesions or presence of viral antigen must be demonstrated by immunohistochemical methods, and finally, virus must be isolated from tissues showing gross lesions at the height of the clinical disease.

Adenovirus infection can be diagnosed morphometrically, serologically, and by virus isolation. Rapid presumptive diagnosis can be made either by observation of characteristic virus morphology in intranuclear inclusions by transmission electron microscopy or by immunofluorescent or immunohistochemical labeling of adenovirus antigens in tissues with gross lesions. Serotype-specific diagnosis, while not important to the treatment of clinical disease, is important in the development of a database from which to evaluate the role of each viral serotype in disease production. For a serotype to be considered as the aetiologic agent in a clinical syndrome, it must be isolated from many cases with similar clinical syndromes and be capable of reproducing the disease experimentally.

Because of the number of types of adenoviruses infecting cattle, virus isolation is necessary to definitively identify the virus. Virus can be isolated from nasal secretions, tracheal fluids, intestinal contents and tissue homogenates. Adenoviruses are best-propagated in homologous cell cultures. Low passage bovine fetal cornea, lung, and turbinate cell cultures, are preferred for virus isolation, because these cells will support replication of all known BAdV types. A permanent heteroploid embryonic calf thyroid cell culture has been developed that allows replication of all bovine adenoviruses although at a somewhat lower titre than those obtained on primary calf testicles (Benkö et al., 1989). Primary adenovirus isolation may require sub-passage of the cultures before viral-induced cytopathic effect appears.

Serologic confirmation of adenovirus infection can be done by demonstrating the presence of adenovirus group-specific antigen by immunofluorescent, immunohistochemical, and complement fixation tests, and by enzyme-linked immunosorbent assay. Reciprocal cross-neutralization tests detect type-specific antigens and further distinguish serotypes. Caution must be exercised when interpreting serum-virus neutralization test results because of demonstrated cross neutralization both among and between adenoviruses isolated from different ruminant species. Molecular characterization of adenovirus using DNA hybridization, restriction endonuclease digestion patterns and polymerase chain reaction has been used for virus identification and classification (Benkö et al., 1988; Benkö et al., 1995; Matiz et al., 1998). Phylogenetic analysis based on the adenovirus protease, hexon and DNA polymerase gene nucleic acid sequences filed with GenBank should make it possible to precisely compare newly isolated adenovirus (Benkö et al., 2000).

List of Symptoms/Signs

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Sign	Life Stages	Type
Digestive Signs / Abdominal distention		Sign
Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed	Cattle & Buffaloes\|All Stages	Sign
Digestive Signs / Bloody stools, faeces, haematochezia	Cattle & Buffaloes\|All Stages	Sign
Digestive Signs / Diarrhoea	Cattle & Buffaloes\|All Stages	Sign
Digestive Signs / Dysphagia, difficulty swallowing	Cattle & Buffaloes\|All Stages	Sign
Digestive Signs / Melena or occult blood in faeces, stools		Sign
Digestive Signs / Mucous, mucoid stools, faeces	Cattle & Buffaloes\|All Stages	Sign
General Signs / Dehydration		Sign
General Signs / Fever, pyrexia, hyperthermia	Cattle & Buffaloes\|All Stages	Sign
General Signs / Generalized weakness, paresis, paralysis	Cattle & Buffaloes\|All Stages	Sign
General Signs / Inability to stand, downer, prostration		Sign
General Signs / Intraocular mass, swelling interior of eye	Cattle & Buffaloes\|All Stages	Sign
General Signs / Lack of growth or weight gain, retarded, stunted growth	Cattle & Buffaloes\|All Stages	Sign
General Signs / Lymphadenopathy, swelling, mass or enlarged lymph nodes	Cattle & Buffaloes\|All Stages	Sign
General Signs / Reluctant to move, refusal to move	Cattle & Buffaloes\|All Stages	Sign
General Signs / Sudden death, found dead		Sign
General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift	Cattle & Buffaloes\|All Stages	Sign
Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless	Cattle & Buffaloes\|All Stages	Sign
Ophthalmology Signs / Conjunctival, scleral, redness	Cattle & Buffaloes\|All Stages	Sign
Ophthalmology Signs / Lacrimation, tearing, serous ocular discharge, watery eyes	Cattle & Buffaloes\|All Stages	Sign
Ophthalmology Signs / Purulent discharge from eye	Cattle & Buffaloes\|All Stages	Sign
Pain / Discomfort Signs / Pain, chest, thorax, ribs, sternum	Cattle & Buffaloes\|All Stages	Sign
Pain / Discomfort Signs / Pain, kidney, ureters, on palpation	Cattle & Buffaloes\|All Stages	Sign
Pain / Discomfort Signs / Pain, pharynx, larynx, trachea	Cattle & Buffaloes\|All Stages	Sign
Reproductive Signs / Abortion or weak newborns, stillbirth	Cattle & Buffaloes\|Cow	Sign
Reproductive Signs / Vaginal or cervical ulcers, vesicles, erosions, tears, papules, pustules	Cattle & Buffaloes\|Cow; Cattle & Buffaloes\|Heifer	Sign
Respiratory Signs / Abnormal breathing sounds of the upper airway, airflow obstruction, stertor, snoring	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Abnormal lung or pleural sounds, rales, crackles, wheezes, friction rubs	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Change in voice, vocal strength	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Coughing, coughs	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Decreased respiratory rate	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Decreased, muffled, lung sounds, absent respiratory sounds	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Dull areas on percussion of chest, thorax	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Haemoptysis coughing up blood	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Mucoid nasal discharge, serous, watery	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Nasal mucosal ulcers, vesicles, erosions, cuts, tears, papules, pustules	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Purulent nasal discharge	Cattle & Buffaloes\|All Stages	Sign
Respiratory Signs / Sneezing, sneeze	Cattle & Buffaloes\|All Stages	Sign

Disease Course

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Adenoviruses infections are frequently inapparent, but may also result in self-limiting disease. Multiple attributes involving host, viral, and husbandry practices influence disease production. Host factors include age and immune status, viral factors include serotype and, possibly, strain of the infecting adenovirus, and husbandry factors include practices causing stress. Infections with currently recognized bovine adenovirus types are usually associated with either pneumonitis or pneumonitis with enteritis (pneumoenteritis). Pneumonitis is usually more prominent and consistent than is enteritis. Clinical disease produced by inoculation of calves with field isolates does not mimic that seen naturally, indicating that the clinical signs and lesions observed naturally result from other superimposed factors such as secondary bacteria and immunosuppression.

Infection most frequently occurs in calves of 2 weeks to 4 months old but animals of any age can be infected. Colostral antibodies will only protect against the homologous adenovirus types, and infection can occur as antibody wanes. Under natural conditions, the incubation period is probably 5 to 10 days. The serological response to adenovirus infection develops about 7 days after the onset of illness and maximum titres are attained after 3 to 4 weeks. Adenovirus antibody titres decrease little over the life of the animal. Infection by heterologous adenovirus serotypes can result in an anamnestic response for any prior infecting adenoviruses. Fever (39.5 to 41.0°C) usually develops 3 to 5 days after infection, lasting for 2 to 5 days. Respiratory and enteric symptoms usually occur following the onset of the febrile response. Respiratory symptoms include serous excretions (purulent with secondary bacterial infections) from the nose and eyes. Coughing often occurs and can be elicited with exercise or by grasping the trachea. Rapid respiration, anorexia and listlessness are frequent clinical signs. Enteric symptoms may include excessive salivation and loose stools to profuse diarrhoea. With BAdV-10 infection, minimal clinical signs followed by sudden death within 12 to 48 h is common. The prominent clinical sign with BAdV-10 may be severe diarrhoea containing blood and fibrin clots. With uncomplicated infections, clinical improvement is seen after 7 to 9 days.

Epidemiology

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The respiratory and enteric tracts are the primary targets for adenovirus infection. Infection with adenovirus usually results in cell lysis and virus shedding, but some cells accumulate virus particles in the nucleus without lysis establishing persistent infections. Respiratory and faecal shedding usually last for about 10 days and, where the kidney is involved, virus can be excreted for over 10 weeks in urine (Aldásy et al., 1965). With persistent infection, lysis of fragile infected cells produces virus-shedding resulting in infection of susceptible animals that come in contact with the virus.

Adenovirus infection is common in younger animals. Maternal antibodies provide protection from infection by homologous BAdV types. As specific maternal antibodies wane, calves can become infected if that particular adenovirus type is present in the calf’s environment. Depending on maternal antibody level, virus exposure can result in either a subclinical infection followed by an active antibody response or if the antibody level is high enough, virus replication can be prevented. The incidence of infection with a serotype appears to be high within a geographic area for a period of time and then may virtually disappear from a region when herd immunity reaches a certain level. Because of the number of adenovirus types and the lack of cross protection, newly introduced adenovirus types may emerge as the predominant infecting type.

Impact: Economic

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Adenoviruses contribute to clinical disease and economic loss in cattle but have not been extensively evaluated to determine their precise role. Economic loss is difficult to assess because clinical signs and gross lesions produced by adenovirus infections are similar to those produced by many other respiratory and enteric infections. Experimental infections and serological studies can clarify the epidemiological significance of the recognized serotypes of adenoviruses isolated from cattle. Isolation of adenoviruses from sick cattle provides circumstantial evidence that adenoviruses are aetiological agents of the observed clinical disease. As with other viruses, adenovirus infection and seroconversion can occur in the absence of clinical disease when maternal antibodies decline and virus is circulating in the herd. An exception to this may be BAdV 10, which has only been isolated from samples collected at postmortem from multiple aged cattle (Adair et al., 1996).

Zoonoses and Food Safety

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Because adenoviruses are usually confined to one host species or closely related species, the zoonotic and food safety threat is very low. To date there are no documented cases of clinical disease in humans caused by bovine adenoviruses.

Disease Treatment

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When economically feasible, cattle can be treated to provide relief from clinical signs associated with adenoviral infection. Left untreated however, the uncomplicated clinical disease will run its course in seven to 10 days. Because secondary bacterial infections such as Mannheimia haemolytica, Pasteurella multocida and Haemophilus somnus are common in cattle, antibiotics are often used as part of the treatment. Where clinical signs are detected early and treated there are few long-term effects.

Prevention and Control

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Maternal antibodies provide protection against homologous virus type, thus it is important for calves to get colostrum to provide early protection from adenoviruses that might be in the calve’s environment. As calves loose maternal antibodies, they develop post-infection immunity to the prevalent adenovirus types in their environment. Husbandry conditions where calves are weaned at a young age (stressed) and mixed with calves with varying immune status and unknown adenovirus carrier status should be avoided when possible. Calves weaned at 5 to 6 months of age generally have a decreased susceptibility to adenovirus-induced disease.

Both modified live and inactivated adenovirus vaccines have been developed and evaluated for use in cattle (Bartha, 1967; Tribe et al., 1969; Bartha, 1974; Bartha, 1975; Haralambiev, 1975; Khristov et al., 1976; Baczynski et al., 1977; Morzaria et al., 1979; Bergamaschi et al., 1981; Becker et al., 1982; Litvinov et al., 1983; Zygraich and Delforge, 1983; Mattson et al., 1987; Pavlov et al., 1987; Wrzolek-Lobocka, 1988b; Belousova, 1989; Nurgaziev and Belousova, 1989; Wrzolek-Lobocka et al., 1990; Deptula et al., 1991; Belousova et al., 1993). It has been difficult to attenuate live vaccines to the point where clinical disease is no longer produced following vaccination. ß-propriolactone- or formalin-inactivated adenoviruses however, elicit excellent antibody response providing immunity to homologous adenovirus. The value of subunit vaccines for bovine adenoviruses has not been fully evaluated (York and Thorsen, 1992). Where vaccines are available for prevailing bovine adenovirus serotypes, they should be administered when maternal antibodies have waned, but 2 to 3 weeks before calves from different places are assembled under stressful conditions.

Bovine adenovirus vaccines are available in Europe and Japan, but there are no commercial adenovirus vaccines available in the USA. Most vaccines are formulated in combination with other agents. Two to 4 doses of vaccine administered subcutaneously or intramuscularly are recommended to provide proper protection. Vaccination has not eliminated infection entirely, but has resulted in the reduction in disease incidence and treatment costs.

References

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