bovine parainfluenza 3 infection

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Caption

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Symptoms

Calf with enzootic pneumonia.

©Paul R. Greenough

Infected lung cells

Bovine fetal lung cells infected with BPIV3. Cells were fixed 72 hours post-infection and stained with hematoxylin/eosin. Note the multinuclear cell (synctium) at the centre of the picture.

S. van Drusen Littel-van den Hurk

BPIV3 antigen

Detection of BPIV3 antigen by indirect immunofluorescence. Bovine fetal lung cells were fixed 72 hours post-infection and stained with anti-fusion protein monoclonal antibody and anti-species lgG linked to fluoresceine. Note the fluorescence in the cytoplasm of infected cells.

S. van Drusen Littel-van den Hurk

Infected BPIV3 lung tissue

Immunohistological staining of lung tissue of a calf infected with BPIV3. Tissue sections were fixed and stained with rabbit antibodies to BPIV3 and avidin-biotin immunoperoxidase complex using diamonobezidine, and counterstained with hematoxylin. Note presence of BPIV3 antigen (red colour) in broncheolar epithelium.

D. Haines/WCVM, Saskatoon, Canada.

Pathology - fibrinous pneumonia

Bovine lung with fibrinous pneumonia caused by Pasteurella haemolytica and bovine parainfluenzavirus 3, affecting the cranial lobe, the middle lobe and the cranio-ventral portions of the caudal lobes of the lungs.

©Paul R. Greenough

Identity

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Preferred Scientific Name

bovine parainfluenza 3 infection

International Common Names

English: bovine respiratory disease; bovine respiratory disease caused by BPIV 3; enzootic pneumonia of calves; parainfluenza virus, pi-3, infection in sheep and goats; shipping fever; shipping fever of cattle; undifferentiated respiratory disease of cattle
Chinese: xin fu nian liu gan bing du

Pathogen/s

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bovine parainfluenzavirus 3

Overview

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Bovine parainfluenza virus 3 (BPIV3) is an important pathogen that causes acute upper and lower respiratory tract infections in calves (Bryson et al., 1978). The virus was isolated for the first time in 1959 from mucus of a calf with respiratory disease and was identified as a myxovirus (Reisinger et al., 1959). Since that time, BPIV3 has been frequently associated with outbreaks of respiratory disease in dairy and beef calves in many countries (Betts et al., 1964; Tsai and Thomson, 1975; Allan et al., 1978; Bryson et al., 1978, 1979a, b). Subsequently, pneumonia typical of field cases was reproduced experimentally by infecting calves with BPIV3 (Tsai and Thomson, 1975; Bryson et al., 1979a, b). In the acute phase of the pneumonia, virus replication was observed within epithelial cells of the respiratory tract and within alveolar macrophages, and loss of cilia and ciliated cells in bronchi and broncheoli and necrosis of bronchiolar epithelium was noted (Tsai and Thomson, 1975; Bryson et al., 1983).

Although an infection with BPIV3 may cause pathology in the respiratory tract of young cattle, this is often subclinical and generally not associated with a recognizable clinical syndrome. The true impact of a BPIV3 infection is that, by causing damage to cells of the respiratory tract, it can impair pulmonary clearance from the lung and predispose calves to secondary infections by other pathogens. As such, BPIV3 is associated with respiratory disease, a major cause of morbidity and mortality in dairy and veal calves (enzootic pneumonia) and feedlot calves (shipping fever pneumonia) that results in substantial economic losses (Thomson, 1980; Yates, 1980; Ghram et al., 1989; Anon., 1992; Radostits et al., 2000a,b). Factors associated with the etiology of bovine respiratory disease are viruses (BPIV3, bovine herpesvirus 1, bovine viral diarrhoea virus, bovine respiratory syncytial virus), bacteria (Mannheimia [Pasteurella] haemolytica, Pasteurella multocida and Haemophilus somnus [Histophilus somni]), stress, and management practices (Yates, 1980; Rebhun et al., 1995; Otter and Farrer, 1997; Radostits et al., 2000a,b). Frequently, more than one infectious agent is involved and together they may act in synergy (Rosenquist et al., 1970; Irwin et al., 1979; Yates, 1980; Ghram et al., 1989).

BPIV3 is an enveloped, non-segmented, negative-sense, single-stranded RNA virus classified in the genus Respirovirus in the Paramyxoviridae family, order Mononegavirales (King et al., 2012).

The Paramyxoviridae contains important pathogens of humans (measles virus, human respiratory syncytial virus, human parainfluenza virus 3 and mumps), and livestock and poultry (bovine parainfluenza virus 3, bovine respiratory syncytial virus, rinderpest virus and Newcastle disease virus; Murphy, 1996), as well as the virus of canine distemper.

Host Animals

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Animal name	Context	Life stage
Bos indicus (zebu)	Domesticated host	Cattle & Buffaloes: Calf
Bos taurus (cattle)	Domesticated host	Cattle & Buffaloes: Calf
Bubalus bubalis (Asian water buffalo)	Domesticated host
Capra hircus (goats)
Ovis aries (sheep)

Hosts/Species Affected

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Parainfluenza viruses generally have a narrow host range (Murphy, 1996). The natural host for BPIV3 is cattle. Based on serology, antibodies to PIV3 have been found in humans, cattle, sheep, goats, water buffalo, deer, dogs, cats, monkeys, guineapigs, pigs, and rats (Tehteh and Goyal, 1988; Maglione and Rosati, 1988; Ulbrich, 1991; Fenner et al., 1993; Aguirre et al., 1995). Although there is a serological relationship, it is not clear whether BPIV3 infects all of these species under natural circumstances or whether there are species-specific virus strains. Human PIV3 (HPIV3) is serologically and antigenically different from BPIV3 (Andrewes et al., 1978; Klippmark et al., 1990). BPIV3 can infect humans, sheep, goats, and bisons, but is probably not pathogenic in these species (Rodger, 1989; Zarnke and Erickson, 1990; Bechmann, 1997). Vaccines using BPIV3 have been used to vaccinate humans and sheep and were found to be safe (Karron et al., 1995). It is not known if PIV3 viruses of other species can infect cattle. PIV3 can cause a mild undifferentiated pneumonia in sheep and goats, and surveys have shown that PIV3 infections are widespread and are associated with respiratory disease of economical importance (Martin, 1996; Watt, 1996). Infections in sheep and goats causing disease are probably caused by species-specific PIV3 isolates.

Systems Affected

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respiratory diseases of large ruminants

Distribution

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Reports on serological surveys and virus isolations demonstrate that BPIV3 has a worldwide geographical distribution. Seroprevalence is generally high and varies from 50 to 90% (Fenner et al., 1993; Martin, 1996; Radostits et al., 2000a,b).

The complete genome analyses of the representative BPIV3 isolates from Australia and North America indicated that BPIV3 falls into two distinct genotypes, BPIV3 genotype A (BPIV-3a) and BPIV3 genotype B (BPIV-3b) (Horwood et al., 2008). Four isolates, which were only detected in China, were proposed as genotype C (Zhu et al., 2011).

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, Widespread	Jetteur et al. (1988)
Egypt	Present, Widespread	Wassel et al. (1996)
Mali	Present, Widespread	Maiga and Sarr (1992)
Nigeria	Present, Widespread	Ibu et al. (1996)
South Africa	Present, Widespread	CABI (Undated)	Original citation: Odendaal et al. (1997)
Tunisia	Present, Widespread	Ghram and Minocha (1990)
Asia
China	Present, Widespread	Zhu YuanMao et al. (2011) Wen YongJun et al. (2012) Wang HaiYong et al. (2014)
India	Present, Localized	Singh (1991)
Indonesia	Present, Widespread	Itoh et al. (1989)
Iran	Present	Ezzi et al. (2013) Farzinpour et al. (2014)
Japan	Present, Widespread	Komoda et al. (1988) Kadoi et al. (1998)
Saudi Arabia	Present	Mahmoud and Allam (2013)
South Korea	Present, Widespread	Kim et al. (1988)
Syria	Present, Widespread	Tabbaa (1989) Giangaspero et al. (1992)
Taiwan	Present, Widespread	Liao et al. (1992)
Thailand	Present, Widespread	Virakul et al. (1997)
Turkey	Present, Widespread	Öztürk and Yavru (1988) Öztürk and Duman (1992) Özdarendeli et al. (1997)
Europe
Albania	Present, Widespread	Ikonomi et al. (1988)
Austria	Present, Widespread	Coulibaly (1990)
Belarus	Present, Localized	Muzychin and Letetskii (1988)
Belgium	Present	Pardon et al. (2011)
Bulgaria	Present, Localized	Kosarov et al. (1998)
Croatia	Present, Localized	Ledinek and Šilak (1995)
Czechia	Present, Localized	Trávníček (1999)
Denmark	Present, Widespread	Tegtmeier et al. (1999)
Federal Republic of Yugoslavia	Present, Localized	Vinković and Čač (1990)
France	Present, Widespread	Penn (1990)
Germany	Present, Widespread	Senf et al. (1988)
Greece	Present, Widespread	Kakamoukas et al. (1989)
Hungary	Present, Widespread	Rusvai and Fodor (1998) Miklós et al. (1999)
Ireland	Present, Widespread	Healy et al. (1993)
Italy	Present, Widespread	Maglione and Rosati (1988) Moriconi and Gnaccarini (1991)
Lithuania	Present	Kęstaitienė et al. (2009)
Netherlands	Present, Widespread	Verhoeff and Nieuwstadt (1984)
Norway	Present	Gulliksen et al. (2009)
Poland	Present, Widespread	Klimentowski et al. (1995)
Romania	Present, Widespread	Cambir and Coman (1991)
Russia	Present	CABI (Undated a) Zhumabaev and Belousova (1992) Masimov (1994)	Present based on regional distribution.
-Russia (Europe)	Present, Widespread	Zhumabaev and Belousova (1992) Masimov (1994)
-Southern Russia	Present, Widespread	Zhumabaev and Belousova (1992)
Serbia and Montenegro	Present, Localized	Lazić et al. (1995)
Slovakia	Present, Widespread	Kováč et al. (1995)
Spain	Present, Widespread	Catalán et al. (1994)
Switzerland	Present, Widespread	Läuchli et al. (1990)
Ukraine	Present, Widespread	Stetsenko et al. (1992)
United Kingdom	Present, Widespread	Stott et al. (1980)
North America
Canada	Present, Widespread	Ettinger and Feldman (2000) CABI (Undated)
-Alberta	Present, Widespread	Durham and Hassard (1990)
-Ontario	Present, Widespread	Martin and Bohac (1986) Martin et al. (1989)
-Saskatchewan	Present, Widespread	Durham and Hassard (1990) Donkersgoed et al. (1993)
Mexico	Present, Widespread	Melgarejo et al. (1991)
United States	Present, Widespread	Fulton et al. (2000) CABI (Undated)
Oceania
Australia	Present, Widespread	Dunn et al. (1998)
New Zealand	Present, Widespread	Motha et al. (1997) Motha and Hansen (1998)
South America
Argentina	Present, Widespread	Ruiz et al. (1989) Fulton et al. (2000) Maidana et al. (2012)
Brazil	Present, Widespread	Pizzol et al. (1989)
Chile	Present, Widespread	Riedemann et al. (1996)
Colombia	Present	Betancur Hurtado et al. (2010)
Peru	Present	Solís G. et al. (2010)

Pathology

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Pneumonia caused by BPIV3 by itself is usually subclinical. Necropsy findings in the apical and cardiac lobes consist of areas of atelectasis and emphysema. In the later stages of infection, dark red-coloured consolidations on apical and cardiac lobes are observed. Bronchointerstitial pneumonia is observed histologically. Generally, an acute inflammation of the nasal mucosa is accompanied by mucopurulent exudate. Microscopically, there are lesions consisting of bronchiolitis, bronchial and bronchiolar hyperplasia, alveolar epithelialization, and giant cell or syncytial formation (Radostits et al., 2000a).

Diagnosis

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The clinical signs of BPIV3 infection in calves or cattle are generally not specific enough to lead to a definitive diagnosis. Therefore, a diagnosis of a BPIV3 infection is based on recovery of the virus from animal samples or on demonstration of an increase in BPIV3 antibody titres in paired serum samples in the laboratory. Samples obtained via tracheal wash, nasopharyngeal swab, or necropsy specimens from infected calves are inoculated in cell culture. Virus is allowed to replicate in cell culture and identified by immunological staining using BPIV3-specific antibodies (Haanes et al., 1997). A direct analysis for BPIV3 can be performed on specimens taken from the respiratory tract, including specimens collected from fatal cases followed by an identification of viral antigens using immunological detection (Gardner et al., 1971; Haines et al., 1992). Alternatively, virus can be assayed by screening for viral RNA in nasal secretions by reverse transcription followed by PCR and immunodetection (Karron et al., 1994). In general, BPIV3 is only detected during the first 7-8 days after infection and is often absent in specimens taken during secondary bacterial infections. Serological diagnosis of BPIV3 antibodies in paired serum samples by complement fixation (CF), haemagglutination inhibition (HI), virus neutralization (VN), or ELISA can establish the occurrence of a virus infection (Assaf et al., 1983; Trybala et al., 1989; van Donkersgoed et al., 1991; Graham et al., 1999).

Because of the multifactorial aetiology of bovine respiratory disease (shipping fever), the high incidence of subclinical BPIV3 infections and the use of modified live virus BPIV3 vaccines, detecting the virus, viral antigens or viral nucleic acid does not prove disease causation. Therefore, the test results should be interpreted after taking into consideration the overall clinical condition of the herd and the individual animal (MacLachlan and Dubovi, 2011).

List of Symptoms/Signs

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Sign	Life Stages	Type
Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed	Cattle & Buffaloes:Calf	Sign
General Signs / Exercise intolerance, tires easily	Cattle & Buffaloes:Calf	Sign
General Signs / Fever, pyrexia, hyperthermia	Cattle & Buffaloes:Calf	Sign
Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless	Cattle & Buffaloes:Calf	Sign
Ophthalmology Signs / Lacrimation, tearing, serous ocular discharge, watery eyes		Sign
Pain / Discomfort Signs / Pain, pharynx, larynx, trachea	Cattle & Buffaloes:Calf	Sign
Reproductive Signs / Abortion or weak newborns, stillbirth	Cattle & Buffaloes:Calf,Cattle & Buffaloes:Heifer,Cattle & Buffaloes:Cow	Sign
Respiratory Signs / Abnormal breathing sounds of the upper airway, airflow obstruction, stertor, snoring	Cattle & Buffaloes:Calf	Sign
Respiratory Signs / Abnormal lung or pleural sounds, rales, crackles, wheezes, friction rubs	Cattle & Buffaloes:Calf	Sign
Respiratory Signs / Coughing, coughs	Cattle & Buffaloes:Calf	Sign
Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping		Sign
Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea	Cattle & Buffaloes:Calf	Sign
Respiratory Signs / Mucoid nasal discharge, serous, watery	Cattle & Buffaloes:Calf	Sign
Respiratory Signs / Nasal mucosal ulcers, vesicles, erosions, cuts, tears, papules, pustules		Sign

Disease Course

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Young cattle usually become susceptible to BPIV3 infection when maternal antibody levels are dropping. The clinical signs of a BPIV3 infection include fever of 40-41.7°C, depression, anorexia, nasal and ocular serous discharge, increased respiratory rate (40-80/min) tracheal rales, and occasional rales in the lower parts of the lung. Recovery from acute infection is usually within 7-10 days (Bryson et al., 1979a, b). Fatal cases due to BPIV3 infection by itself are rare. A BPIV3 infection can cause lesions in the ciliated epithelial lining of the respiratory tract and BPIV3 can infect alveolar macrophages and hence impair the defence mechanisms against respiratory pathogens (Liggitt et al., 1985; Slauson et al., 1987; Brown and Ananaba, 1988; Basaraba et al., 1993). Therefore, in most cases of a moderate to severe (including fatal) pneumonia, a BPIV3 infection is usually accompanied by bacterial infection. The most common bacteria encountered in complicated pneumonia are Mannheimia [Pasteurella] haemolytica, Pasteurella multocida and Haemophilus somnus [Histophilus somni] (Otter and Farrer, 1997; Radostits et al., 2000a, b).

Although it has been reported that BPIV3 may infect foetuses and cause abortions in cattle, it is not considered a common cause of abortion (Dunne et al., 1973; Swift and Trueblood, 1974).

Epidemiology

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The prevalence of BPIV3-specific antibodies in dairy and beef cattle is high and the virus is commonly isolated from calves with respiratory disease (Potgieter, 1977; Thomson, 1980; Fulton et al., 1982; Key and Derbyshire, 1984; Martin and Bohac, 1986; Radostits et al., 2000a,b). A BPIV3 infection of calves is generally subclinical in the absence of other pathogens and adverse environmental and management factors (Rebhun et al., 1995; Radostits et al., 2000a,b). An uncomplicated respiratory infection caused by BPIV3 is characterized by clinical signs for 3-5 days followed by a complete recovery (Fenner et al., 1993). Usually, housed dairy calves and nursing beef calves become infected with BPIV3 when they are 1-5 months old. Beef calves often become infected within 2 weeks when they enter a feedlot. Following BPIV3 infection, virus can be isolated for 1-2 weeks from individual calves and can persist for several weeks in the group. By interference with the pulmonary clearance system the virus is capable of predisposing infected young calves to more severe pneumonia (enzootic pneumonia and shipping fever pneumonia) when they are subsequently exposed to bacterial pathogens such as Mannheimia [Pasteurella] haemolytica (Radostits et al., 2000a,b). A combined infection with BPIV3 and BHV-1 causes more severe disease in calves than either virus by itself, and antibody responses are delayed and lower in calves infected with both viruses (Ghram et al., 1989).

BPIV3 is transmitted by direct contact between animals and by aerosol infection.

Impact: Economic

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The economic impact of BPIV3 by itself is not known. BPIV3 is one of the factors associated with enzootic pneumonia in housed dairy calves, veal calves and beef calves in crowded calving grounds, and bovine respiratory disease (BRD, shipping fever) in feedlot cattle. BRD has been reported to cause 31% of cattle deaths in the USA and enzootic pneumonia can be responsible for up to 30% of all dead calves in dairy herds is and the single largest cause of death in veal calf farms (van Donkersgoed et al., 1993; Vogel and Parrott, 1994; Radostits et al., 2000b). The economic losses for the beef industry in the USA due to death, treatment, decreased animal performance, and labour have been estimated at US $624 million per year (Anon., 1992). Morbidity rates for enzootic pneumonia in dairy cattle and BRD in beef cattle are 80-100% (van Donkersgoed et al., 1993; Vogel and Parrott, 1994; Radostits et al., 2000a,b).

One report by Senf et al. (1988) indicates the economic impact of BPIV3 infection. BPIV3 was isolated from 202 lung samples of calves with a respiratory disease complex over a 5-year period on 131 premises, and immunization with a BPIV3 vaccine reduced economic losses and disease.

Zoonoses and Food Safety

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BPIV3 is closely related to human PIV3 and can infect humans. However, a relatively high dose of BPIV3 is required for the infection of humans (Collins et al., 1996). Therefore, infection by consumption of BPIV3-contaminated meat from cattle, (particularly from the respiratory organs) is unlikely. BPIV3 does not survive in properly cooked meat. In addition, a live BPIV3 candidate vaccine for humans has been tested and was found to be safe and induce immunity in children (Karron et al., 1995; Collins et al., 1996). Nevertheless, a period of 3-4 weeks disease-free before slaughter of cattle is recommended for livestock previously infected with BPIV3.

Disease Treatment

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Treatment of BPIV3- infected calves with alpha-interferon has been reported (Kishko and Mukvich, 1998).

Treatment must take into consideration the frequent secondary bacterial pneumonia following a BPIV3 infection. Sick animals should be isolated from healthy ones and, in consultation with a veterinarian, treated with antibiotics to prevent secondary infections.

Prevention and Control

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Disease prevention and control is based on good husbandry, management strategies to decrease stress, and appropriate vaccination (Ballásh and Kudron, 1993; Elze and Selbitz, 1993; Rebhun et al., 1995; Radostits et al., 2000a,b). Many guidelines that address these factors are available for local situations from government institutions.

Enzootic Pneumonia

With respect to enzootic pneumonia, the animal population at risk for development of pneumonia are housed dairy and veal calves and to a lesser extent beef calves of 2 weeks and older (Radostits et al., 2000b).

Steps to prevent and control pneumonia include the following:

Make sure that calves drink adequate colostrum containing a high level of antibodies to BPIV3 (and other respiratory disease-causing infectious agents; Hofmann et al., 1991; Barringer and Rosenberg, 1995).

Ensure that calves are fed and housed well.

Group and house calves by size and age, and avoid overcrowding.

Isolate newly purchased calves for a few weeks.

Follow an all-in, all-out procedure; clean and disinfect pens, and leave pens empty for a few days between groups.

Keep sick calves separated from healthy ones, and treat them with antibiotics in consultation with a veterinarian.

Obtain a diagnosis of the causative agent.

Keep health records on calves.

Vaccinate calves against respiratory diseases with a vaccine including BPIV3 when passive antibodies have decreased, which usually occurs at 4 months and give a booster at 6 months, followed by yearly booster immunizations (Rebhun et al., 1995).

Many effective BPIV3 vaccines are available; modified-live vaccines for intra-nasal and intra-muscular administration and killed products for intra-muscular use (van Donkersgoed et al., 1991; Fulton et al., 1995; Hermülheim and Wittkowski, 1995). Intra-nasal BPIV3-containing products elicit a fast local immune response.

Bovine Respiratory Disease

With respect to BRD (shipping fever) in feedlot cattle, the animals at risk for development of pneumonia are beef calves during the first weeks after arrival (Martin and Bohac, 1986; Martin et al., 1989; Radostits et al., 2000a). The cause of disease is multifactorial and greatly affected by management practices and degree of stress. Generally calves arriving in feedlots seroconvert to several respiratory viruses including BPIV3 within the first month (Fulton et al., 2000; Radostits et al., 2000a).

Risk factors associated with disease include increased mixing of calves from different origins, month of purchase, duration of transport, and weather conditions at arrival (Radostits et al., 2000a). To reduce stress and disease associated with transport and entering into a feedlot, a program of preconditioning and preimmunization is undertaken in which calves are dehorned, castrated and vaccinated before weaning by the cow-calf producer. Immunization of the calves with a vaccine containing BPIV3 is recommended during preconditioning and at arrival at the feedlot. Many modified-live and killed BPIV3 vaccines are available usually combined with other viral and bacterial products. Sick animals should be isolated from healthy calves and treated with appropriate antibiotics to prevent bacterial disease, in consultation with a veterinarian.

The efficacy of the current vaccines, irrespective of the formulation, is fair in dairy cattle, but with the different management issues confronting the feedlot industry, the control of UF/BRDC is complicated using the vaccination approach (Elankumaran, 2013). There are conflicting reports on the efficacy of the intranasal vaccine formulations in comparison with parenteral live attenuated vaccines (Ellis, 2010). Both types of vaccine are capable of inducing local and systemic protective antibody responses, but the duration and magnitude of response may depend on the status of local and systemic antibody levels at the time of vaccination. Maternal antibodies inhibit the development of active immunity against BPIV3 (Marshall and Frank, 1975; Adair et al., 2000; Fulton et al., 2004).

Contradictory data have been described with respect to the benefit of the use of alpha-interferon for prevention or reduction of disease caused by BPIV3 (Bryson et al., 1989; Kishko and Mukvich, 1998).

References

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Betancur Hurtado C, Orrego Uribe A, González Tous M, 2010. Seroepidemiological study of parainfluenza 3 virus in bovines with reproductive failure, from Monteria-Colombia. (Estudio seroepidemiológico del virus de parainfluenza 3 en bovinos del municipio de Montería (Colombia) con trastornos reproductivos.). Revista de Medicina Veterinaria. 63-70. http://publicaciones.lasalle.edu.co/images/openacces/Revistas/veterinaria/MV20/estudio_seroepidemiologico.pdf

CABI, Undated. Compendium record. Wallingford, UK: CABI

CABI, Undated a. CABI Compendium: Status inferred from regional distribution. Wallingford, UK: CABI

CABI, Undated b. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

Cambir S, Coman I, 1991. Simultaneous administration of inactivated tribacterial vaccine (Salmonella, Escherichia coli and Pasteurella) with the triviral vaccine (PI3, BVD and IBR) in calves aged from 1 to 30 days. (Aplicarea simultană a vaccinului tribacterian inactivat (Salmonella, E. coli și Pasteurella) și vaccinul triviral (PI3, BVD și IBR) la viței în vîrstă de 1-30 zile.). Lucrările Institutului de Cercetări Veterinare și Biopreparate 'Pasteur'. 55-59.

Catalán O, Terreu M, Pérez Calahorra M, Alamán C, 1994. Evaluation of the efficacy and economic impact of a vaccination programme with a tetravalent vaccine against bovine respiratory disease. (Evaluación de eficacia e impacto económico de un programa vacunal con una vacuna tetravalente en la profilaxis del síndrome respiratorio bovino.). Medicina Veterinaria. 11 (4), 220-225.

Coulibaly S, 1990. Serological studies on the occurrence of antibodies against viral pathogens in cattle in Austria. (Serologische Untersuchungen über das Auftreten von Antikörpern gegen virale Krankheitserreger beim Rind in Österreich.). Wiener Tierärztliche Monatsschrift. 77 (7), 245.

Donkersgoed J van, Ribble C S, Boyer L G, Townsend H G G, 1993. Epidemiological study of enzootic pneumonia in dairy calves in Saskatchewan. Canadian Journal of Veterinary Research. 57 (4), 247-254.

Dunn SE, Godwin J, Hoare RJT, Kirkland PD, Walker SB, Coverdale DA, Gibson JA, 1998. Diseases of feedlot cattle in Eastern Australia. [World Buitrics Congress Proceedings], 1 [ed. by Caple W]. Sydney, Australia: 159-164.

Durham P J K, Hassard L E, 1990. Prevalence of antibodies to infectious bovine rhinotracheitis, parainfluenza 3, bovine respiratory syncytial, and bovine viral diarrhea viruses in cattle in Saskachewan and Alberta. Canadian Veterinary Journal. 31 (12), 815-820.

Ezzi A A, Hatami A, Bakhshesh M, Shoukri M R, Gharaghozloyan M, 2013. Serological study of bovine herpesvirus type 1 and parainfluenza type 3 in cow farms of qazvin province based on different ages and seasons. Archives of Razi Institute. 68 (1), 53-57. http://www.archrazi.com/browse.php?a_id=367&sid=1&slc_lang=en

Farzinpour M, Pourjafar M, Badiei K, Ghane M, Zare K, 2014. Detection of antibodies and risk factors for infection with bovine herpesvirus-1 and parainfluenza virus-3 in dairy Holstein farms. Online Journal of Veterinary Research. 18 (2), 82-90. http://users.comcen.com.au/˜journals/bovineholsteinabs2014.htm

Fulton R W, Purdy C W, Confer A W, Saliki J T, Loan R W, Briggs R E, Burge L J, 2000. Bovine viral diarrhea viral infections in feeder calves with respiratory disease: interactions with Pasteurella spp., parainfluenza-3 virus, and bovine respiratory syncytial virus. Canadian Journal of Veterinary Research. 64 (3), 151-159.

Ghram A, Minocha H C, 1990. Neutralizing antibodies to bovine herpesvirus-1 (BHV-1) and bovine parainfluenza (PI-3) viruses in cattle in Tunisia. Archives de l'Institut Pasteur de Tunis. 67 (1/2), 25-31.

Giangaspero M, Vacirca G, Vanopdenbosch E, Blondeel H, 1992. Epidemiological survey on virus diseases of cattle in north west Syria. Tropicultura. 10 (2), 55-57.

Gulliksen S M, Jor E, Lie K I, Løken T, Ǻkerstedt J, Østerǻs O, 2009. Respiratory infections in Norwegian dairy calves. Journal of Dairy Science. 92 (10), 5139-5146. http://jds.fass.org/cgi/content/abstract/92/10/5139 DOI:10.3168/jds.2009-2224

Healy A M, Monaghan M L, Bassett H F, Gunn H M, Markey B K, Collins J D, 1993. Morbidity and mortality in a large Irish feedlot: microbiological and serological findings in cattle with acute respiratory disease. British Veterinary Journal. 149 (6), 549-560. DOI:10.1016/S0007-1935(05)80039-9

Ibu J, Obi T U, Aba-Adulugba E, 1996. Serological evidence of parainfluenza type 3 virus infection of cattle in Plateau State [Nigeria]. Nigerian Veterinary Journal. 1 (1), 100-102.

Ikonomi R, Melonashi V, Joti K, Canaj Z, 1988. Trivalent vaccine for calves against respiratory infections caused by parainfluenza, 3, IBR and adenoviruses. (Vaksinë trivalente kundër infeksioneve respiratore të vicave të shkaktura nga viruset PI-3, IBR dhe adeno.). Buletini i Shkencave Zooteknike e Veterinare. 6 (1), 59-67.

Itoh O, Sugimori T, Ogata M, Noda M, Inaba Y, Saepulloh M, Jusa E R, Noor M A R, 1989. Serological survey of some bovine disease viruses among Indonesian cattle. Annual Report of the National Veterinary Assay Laboratory. 29-31.

Jetteur P, Eyanga E, Makumbu S, 1988. Serological survey of rinderpest, IBR IPV, bovine respiratory syncytial, parainfluenza 3 and bovine virus diarrhoea viruses in cattle in Shaba and West Zaire. (Enquête sérologique concernant les virus bovipestique, IBR-IPV, RSB, PI3 et BVD-MD sur des bovins du Shaba et de l'Oest du Zaïre.). Revue d'Élevage et de Médecine Vétérinaire des Pays Tropicaux. 41 (2), 121-124.