Mycoplasma bovis infections

Pictures

Picture	Title	Caption	Copyright
Title Symptoms of natural infection Caption Calf naturally infected with M. bovis showing respiratory distress. Copyright R.A.J. Nicholas	Symptoms of natural infection	Calf naturally infected with M. bovis showing respiratory distress.	R.A.J. Nicholas
Title Symptoms of experimental infection Caption Calf experimentally infected with M. bovis showing respiratory distress. Copyright R.A.J. Nicholas	Symptoms of experimental infection	Calf experimentally infected with M. bovis showing respiratory distress.	R.A.J. Nicholas
Title Symptoms of experimental infection Caption Calf experimentally infected with M. bovis by aerosol route showing arthritis. Note grossly swollen joint (arrowed). Copyright R.A.J. Nicholas	Symptoms of experimental infection	Calf experimentally infected with M. bovis by aerosol route showing arthritis. Note grossly swollen joint (arrowed).	R.A.J. Nicholas
Title Lung pathology Caption Lung of calf experimentally infected with M. bovis. Note areas of typical pulmonary consolidation caused by M. bovis (arrowed). Copyright R.A.J. Nicholas	Lung pathology	Lung of calf experimentally infected with M. bovis. Note areas of typical pulmonary consolidation caused by M. bovis (arrowed).	R.A.J. Nicholas
Title Lung pathology Caption Lung of calf experimentally infected with M. bovis. Note areas of typical pulmonary consolidation caused by M. bovis (arrowed) Copyright R.A.J. Nicholas	Lung pathology	Lung of calf experimentally infected with M. bovis. Note areas of typical pulmonary consolidation caused by M. bovis (arrowed)	R.A.J. Nicholas
Title Joint pathology Caption Arthritic joint from calf experimentally infected with M. bovis. Note fibrin plugs in the arthritic joint (arrowed). Copyright R.A.J. Nicholas	Joint pathology	Arthritic joint from calf experimentally infected with M. bovis. Note fibrin plugs in the arthritic joint (arrowed).	R.A.J. Nicholas

Identity

Preferred Scientific Name

• Mycoplasma bovis infections

International Common Names

• English: bovine mycoplasma conjunctivitis; bovine mycoplasmal arthritis; bovine mycoplasmal conjunctivitis; bovine mycoplasmal polyarthritis; calf pneumonia; endemic pneumonia in calves; enzootic calf pneumonia; infectious bovine keratoconjunctivitis, moraxella bovis, pinkeye; keratoconjunctivitis; mastitis; mycoplasma abortion in cattle; Mycoplasma bovis arthritis; Mycoplasma bovis infertility; Mycoplasma bovis keratoconjunctivitis; Mycoplasma bovis pneumonia; mycoplasma bovis pneumonia, arthritis, tenosynovitis, in calves and cows; Mycoplasma bovis reproductive disease; Mycoplasma bovis tenosynovitis; mycoplasmal abortion in cattle; mycoplasmal mastitis in cattle; otitis media, externa, interna, middle and inner ear infections; pink eye; pinkeye

Pathogen/s

Overview

Arguably the most important mycoplasma of animals because of the range of diseases and economic losses it causes, M. bovis was first isolated in 1961 from a case of severe mastitis in cattle in the USA. It then appears to have spread via animal movements to many countries, Israel (1964), Spain (1967), Australia (1970), France (1974), Britain (1975), Czechoslovakia (1975), Germany (1977), Denmark (1981), Switzerland (1983), Morocco (1988), South Korea (1989), Brazil (1989), Northern Ireland (1993), Republic of Ireland  (1994), Chile (2000), South Africa (2005), the Czech Republic (2007) and China (2008) (Nicholas, 2011). Most European countries are thought to be affected and M. bovis has been reported in Africa and Asia.

Its prevalence is almost certainly under reported, as Pasteurella (Mannheimia), and Haemophilus (Histophilus) species are invariably isolated from calf pneumonia and are easier to detect. In arthritis and mastitis where M. bovis is a primary and uncomplicated cause, it is often overlooked as few laboratories routinely monitor for mycoplasmas. However, unlike these 'conventional' bacteria, the occurrence of M. bovis in a herd is always linked to cases of disease, in particular mastitis, arthritis and/or pneumonia (Pfützner and Sachse, 1996). M. bovis has also been linked to endometritis, salpingitis, oophoritis, abortion and seminovesiculitis which have all been reproduced experimentally (Ruhnke, 1994). Otitis media and meningitis resulting in neurological signs and permanent head tilt has also been reported (Gosselin et al., 2012) and reproduced experimentally (Maunsell et al., 2012). An unusual case of toxic epidermal necrolysis was associated with M. bovis in calves (Senturk et al., 2012).  

While M. bovis infections have always been difficult to treat, there is now considerable evidence that many strains are resistant to chemotherapy (Ayling et al., 2000; Gerchman et al., 2009).

The genome of M. bovis type strain is 1,003,404 base pairs and has a G+C content of 29.3% (Wise et al., 2011); whereas the Hubei-1 isolate was slightly smaller at 953,114 base pairs (Li et al., 2011).

Host Animals

Hosts/Species Affected

M. bovis is highly adapted to cattle but occasional isolations are made in buffaloes and small ruminants. Pneumonia and mastitis have been experimentally reproduced in sheep (Pfützner and Sachse, 1996). Very rare isolations have been made from chickens (Ongor et al., 2008); and man in immunocompromised patients (Pitcher and Nicholas, 2005).

Systems Affected

Distribution

M. bovis is an important cause of respiratory disease and mastitis in cattle throughout the world, often reported as emerging (Gille et al., 2018).

Distribution Table

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.

Pathology

Pulmonary lesions in naturally infected calves comprise exudative bronchopneumonia and extensive foci of coagulative necrosis surrounded by inflammatory cells. In studies involving experimental infections of gnotobiotic calves with M. bovis, significant pneumonia was induced involving up to 30% of the lung surface and was of sufficient severity to cause clinical respiratory disease in some calves (Thomas et al., 1986). Distinctive areas of coagulative necrosis were prominent within the lesions. More chronic infections are often associated with a chronic lymphocytic ‘cuffing’ pneumonia where there is marked hyperplasia of peribronchial lymphoid tissue causing stenosis of airway lumina and compression and collapse of adjacent pulmonary pyrenchyma. M. bovis antigen is mainly detected at the periphery of the areas of coagulative necrosis, in necrotic exudates and in close association with infiltrating macrophages and neutrophils (Rodríguez et al., 1996). More recently chronic caseonecrotic bronchopneumonia with multiple dry and crumbly foci of caseous necrosis, which resembles bovine tuberculosis, has been recognised in the USA and Europe (Nicholas, 2011).

In severe cases of mastitis, one or more quarters are tense and swollen but neither hot nor painful and on section consists of yellow greenish tissue with a purulent exudate replacing milk secretion. Affected animals usually show no signs of illness although mild respiratory symptoms and slight malaise may be seen; this absence of systemic disease is also an indication of mycoplasma mastitis.

M. bovis-induced arthritis usually affects the dithrodal joints which are grossly swollen and hot to the touch. At necropsy, the synovial capsule is turbid and thickened and a viscous opaque synovial fluid is present in excessive amounts. This is associated with distension of the tendon sheaths. Large fibrin deposits on the membranes and within the joints, sometimes forming large pads, are also seen (Stipkovits et al., 2001).

It has been reported that Mycoplasma species including M. bovis have the ability to form biofilms (McAuliffe et al., 2006). Whether the formation of biofilms has a role in the pathology of the disease is not known, however it is likely to provide the organism with some protection against the hosts immune response and antibiotic treatments, it will also facilitate longer survival in the environment than previously thought.

Diagnosis

Clinical signs are not characteristic for M. bovis so laboratory diagnosis is necessary for identification. Samples of choice are listed in the table below. The mycoplasma grows well in a variety of media producing 'centred' colonies within 3-5 days (Nicholas and Baker, 1998). In an appropriate medium (such as Eaton’s) M. bovis produces films and spots and gives an orange colour to the broth. Other biochemical characteristics are shown in a table under the 'Pathogen Characteristics' of M. bovis. Growth inhibition, film inhibition, fluorescent antibody or metabolic inhibition tests can be used to identify the mycoplasma using hyperimmune rabbit serum.

Samples of choice for diseases caused by M. bovis

*bronchial alveolar lavage

A rapid and sensitive sandwich ELISA for M. bovis was described by Ball and Findlay (1998). Immunobinding assays were described for M. bovis which had similar sensitivities and specificities to the culture method but were simpler and more rapid (Poumarat et al., 1999). M. bovis can be easily outgrown by opportunistic mycoplasmas such as M. bovirhinis and acholeplasmas; occasionally, antigenic variability of strains may make serological tests unreliable (Ayling et al., 1997). For these situations, polymerase chain reaction (PCR) tests are very convenient. Early PCRs, based on 16S rRNA genes, also amplified M. agalactiae DNA (Pfützner and Sachse, 1996; Ayling et al., 1997) but PCR developed based on the uvrC gene are more specific (Frey et al., 1999). PCRs have been used to detect M. bovis directly in milk and nasal samples (Hotzel et al., 1996). R-T PCR’s provide a quick and sensitive specific diagnostic test (Sachse et al., 2010), but other tests that can detect multiple mycoplasma infections can be advantageous and these include the PCR/DGGE method (McAuliffe et al., 2005) and microarray technology (Schnee et al., 2012).   

Serological detection of M. bovis antibody is often a more reliable diagnostic method as antibody levels detected by ELISA remain high for many months. This is particularly true where antibiotics have been used extensively on the herd, which severely hampers isolation; M. bovis is also difficult to isolate from chronically affected cattle (Nicholas, 1997). The presence of specific antibodies would also indicate that the infection is invasive. While a number of serological tests including indirect haemagglutination and film inhibition have been reported, these have been mostly superseded by the indirect ELISA using whole cell or chemically treated antigens (Nicholas et al., 2000); a commercial test is also available from BioX (Belgium). An ELISA method has been used successfully to select M. bovis-free cattle following depopulation as a result of BSE in Ireland (O’Farrell et al., 2001); its use in maintaining M. bovis-free herds by testing newly bought-in animals before introduction to the herd should also be seriously considered.

The isolation of M. bovis from lungs is not always possible because of ongoing antibiotic treatment, poor lung condition or gross bacterial contamination. In these cases, immunohistochemical techniques preferably using monoclonal antibodies may be valuable to localise mycoplasma antigens in the affected tissue (Adegboye et al., 1995).

List of Symptoms/Signs

Disease Course

A clinical study of endemic pneumonia caused predominantly by M. bovis showed that nearly half of dairy calves were shedding mycoplasma at 5 days of age and by 4 weeks this reached over 90% (Stipkovits et al., 2000). Clinical disease in calves, including up to 10% mortality as a result of severe serofibrinous pneumonia, is maximal at 10-15 days. Surviving calves show very poor weight gain and remain retarded; other signs included fever, depression, hyperpnoea, dysnpnoea, nasal discharge, mild to continuous coughing and loss of appetite. While Pasteurella multocida is often isolated, the rate does not always increase over time. In the UK, calf pneumonia usually begins in November and peaks around January before declining, but deaths continue to occur in some herds in the spring at pasture representing relapses because of unresolved lung lesions (Nicholas et al., 2001a).

In M. bovis-induced mastitis, clinical signs vary from subclinical to very severe and from acute to chronic. Usually with overt disease, there is a sharp reduction in milk production, swelling and firmness of the mammary glands; the condition is usually refractory to antibiotics (Ross, 1993). In an infected herd, mastitis usually affects more than 20% of cows independently of the stage of lactation with even dry cows developing the disease. The main symptoms include a great alteration in milk consistency (watery to purulent), a rapid decrease of milk yields down to a few millilitres within 3-5 days, and quick spread of the infection from one udder quarter to the others leading to agalactia. The overall number of cells in the milk increases dramatically and after a further few weeks the affected quarters become atrophic. M. bovis mastitis is characterised by the failure of cows to recover from the disease during the continuing lactation period and from the often complete lack of response to antibiotic treatment. On recovery, milk production rarely resumes normal output.

Arthritis associated with M. bovis infection may be a sequel to either the respiratory or mastitic form of the disease (Pfützner, 1990). There is lameness, swelling of joints, slight elevation of temperature, failure of antibiotic treatment, and if severe, reduced consumption of feed and debilitation. This condition often arises within 2-3 weeks of housing and also following transportation of calves over long distances. The initial signs are reluctance to stand and a stiff gait. Many cases are mild and the animal usually recovers; in more severe cases, lameness becomes more pronounced within 1-4 days and the animal is reluctant to stand. The affected limb is either stiff or held stiffly at the affected joint. If the animal is walking, the limb may be dragged or thrown outwards to minimise articular action.

Genital disease caused by M. bovis is indistinguishable from common fertility disorders and is normally found in only a small number of individuals (Pfützner and Sachse, 1996).

Epidemiology

M. bovis is not ubiquitous, but is widespread within the bovine population of enzootically infected areas. Infected, but clinically healthy calves and young cattle, shed the mycoplasma via the respiratory tract, thereby acting as the reservoir of infection (Pfützner, 1990). The appearance of M. bovis on some farms has been associated with increased severity of respiratory disease and increased mortality (Nicholas, 1997).

The infection is usually brought in to M. bovis-free herds by clinically healthy calves or young cattle shedding the mycoplasma and once established in a multi-age site is very difficult to eradicate. Cattle get infected via the teat canal, the respiratory tract and genital tract; artificial insemination with infected semen is another common route (Pfützner, 1990).

In a study of calves in the Netherlands, Laak et al. (1992a, 1992b) found M. bovis in 20% of pneumonic lungs from fattening herds but not in dairy herds and in only 3% of healthy calves. Following its introduction into Ireland in 1994, M. bovis has been consistently isolated from 13-23% of pneumonic lungs (Byrne et al., 2001). In Britain, about 20-25% of pneumonic herds contain antibodies to M. bovis (Nicholas et al., 2001). In France, serological screening for M. bovis in suckling beef cattle in seven counties revealed that over 80% of herds contained at least one infected animal although the number of seropositive cattle was generally low (15%) (Le Grand et al., 2001). The low ELISA titres obtained in the study suggested a less active infection process within the adult population. In Poland, Bednarek et al. (2012) found nearly 81% of 361 herds had positive M. bovis titres.

Impact: Economic

M. bovis is an important pathogen of cattle causing disease with significant detrimental impacts on animal welfare and the farming economy (Nicholas and Ayling, 2003). The real economic cost of the disease has not been determined; a detailed analysis of all cost factors such as mortality, veterinary costs, treatment, milk loss, added housing/feed costs through lack of weight gain would yield a more complete appreciation of the full economic burden. There are no official restrictions on animal movement within the European Union; however, some countries importing cattle are increasingly aware of the risks of importing infected cattle and are requesting that cattle are tested and shown to be free of M. bovis (Calcutt et al., 2018).

In the UK, it is estimated that up to 1.9 million cattle are affected annually by respiratory disease, with a consequent loss in performance of £54 million to the cattle industry (Reeve-Johnson, 1999). Furthermore, approximately 157,000 calves die annually as a result of pneumonia and related illnesses, which would have a potential market value of £99 million. Across Europe with approximately 84.5 million cattle in 1995 this translated as total losses of 576 million ECU. It is likely that M. bovis is responsible for at least a quarter to a third of these losses, although this is certainly an underestimate as few countries report mycoplasma diseases (Nicholas et al., 2000). In the USA, losses caused by M. bovis as a result of loss of weight gain and carcass value have been estimated at $32 million per year (Rosengarten and Citti, 1999).

The losses due to bovine mastitis caused by M. bovis may be higher than that for respiratory disease. In the USA losses have been estimated at $108 million per year with infection rates of up to 70% of a herd (Rosengarten and Citti, 1999). A survey of bulk milk tank samples in New York State over 9 years reported that about 2.3% contained M. bovis; similar results have been reported in Iowa where culling rates of infected cows of 30-70% are not uncommon. In eastern Canada, 52% of dairy herds are affected with M. bovis mastitis resulting in culling rates of close to 33% and average milk production losses of 6.4 kg per cow each day (Rosengarten and Citti, 1999).

No data are available for losses due to M. bovis arthritis or reproductive disease.

Disease Treatment

Pfützner (1990) stated that diseases due to M. bovis were resistant to any therapy. In spite of this, antibiotics are widely used to reduce secondary bacterial infections, but often they are ineffective for the treatment of the core mycoplasma infections. Many in vitro studies have compared the susceptibility of M. bovis to a range of antibiotics (see Table). While it is clear that antibiotics which are ineffective in vitro are unlikely to be effective in vivo, those with strong activities in vitro will not necessarily perform well in the field for reasons which are unclear (Ayling et al., 2000). Recent evidence suggests that M. bovis strains are becoming resistant to antibiotics traditionally used for treatment of mycoplasma infections; in particular oxytetracyclines, tilmicosin and spectinomycin (Nicholas et al., 2000). Some in vitro resistance to the fluoroquinolones has also been reported (Gerchman et al., 2009). Some of the new triamalides are licensed for use in treating mycoplasma respiratory disease in cattle, and are reported to be effective in the field, but in vitro test results are not always consistent with that finding (Godinho et al., 2005).    

Some success against M. bovis pneumonia and arthritis in calves was reported by Stipkovits et al. (2001) using valnemulin added to the milk from 4 days of age for 3 weeks. Animals in the treated group had fewer clinical signs and reduced clinical scores though the number of animals with nasal discharge was similar. In spite of the continuous chemotherapy, animals required a considerable number of individual treatments.

Effectiveness of antibiotics against field strains of M. bovis (minimum inhibitory concentrations µg/ml*)

=or<1 µg/ml = mycoplasmas susceptible

2-4 µg/ml = show intermediate susceptibility

>8 µg/ml = mycoplasmas resistant

(Laak et al., 1992a, 1992b)

Prevention and Control

The inability of chemotherapy to control M. bovis infections has focused attention on vaccination. Surprisingly there are no currently available vaccines although a quadrivalent inactivated vaccine containing respiratory syncytial virus, parainfluenza type 3 and 2 mycoplasmas, M. dispar and M. bovis, showed some evidence of protection against natural infection of respiratory disease (Howard et al., 1987). A vaccine prepared with formalin-inactivated strains of M. bovis and Pasteurella haemolytica taken from the target herd reduced losses from pneumonia and cost of treatment in newly introduced feedlot calves (Urbaneck et al., 2000). More recently a saponised-inactivated vaccine was shown to be safe, highly immunogenic and protective against a strong experimental challenge of virulent M. bovis (Nicholas et al., 2001). However, attempts to vaccinate against M. bovis arthritis were less successful against experimental infection although high levels of antibody were detected before challenge (Poumarat et al., 1999). Experimental vaccines against mastitis have not been successful and indeed may make the condition worse (Ross, 1993).

Mastitis caused by M. bovis responds poorly to antibiotics therefore it is best to segregate or cull carrier cows then instigate rigid sanitation procedures to prevent transmission from infected to non-infected cows (Pfützner, 1990). Identification of infected cows in the early stages of mastitis may be detected conveniently using an indirect ELISA for specific antibody in the milk; moreover the test can identify the infected quarter of an individual cow (Byrne et al., 2000). Punyapornwithaya et al. (2012) stated that most mastitic herds cleared mastitis within 1 month, with more than 50% of the herds culling diseased cows; however culling was not associated with hastened clearance and may not be an essential control practice if other good milking time hygiene and practices are observed. 

The prophylactic use of antibiotics is generally undesirable but its use may be justified when calves are introduced to a site with a history of M. bovis infection in which high levels of mortality have been sustained. Nagatomo et al. (1996) treated one group of introduced calves with leucomycin prior to the development of clinical signs. Untreated groups of calves showed mortality rates of 41% and 17% while all the calves in the treated group survived, although coughing and nasal discharges were evident. Interestingly, while M. bovis antibodies were detected in non-treated groups after two months following introduction, antibody development was significantly delayed until over eight months in the antibiotic-treated groups.This provides further evidence that antibody responses are rarely protective.

Control of calf pneumonia should include measures to reduce environmental stress and to ensure adequate housing with good circulation of air. Wherever possible consideration should be given to ‘all in, all out’ practices to prevent older animals infecting younger ones. If this is not possible, separation of calves from the adults is advisable at the earliest possible opportunity where endemic disease exists and where husbandry allows this.

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