Infectious disease can have a deleterious effect on the ability of bulls to serve cows. The ability of bulls to serve has a significant impact on conception rates and therefore income in cow-calf herds. This report details a case of balanitis in a commercial beef herd and the diagnostic tests performed in an attempt to determine the presence of bovine herpesvirus 1 and Ureaplasma spp. The balanitis presented as unwillingness of bulls to serve.
During November 2016 a request for assistance was received from a local veterinary practitioner regarding a case of penile lesions in bulls.
The producer had purchased bulls from two different studs (Stud A and Stud B) that arrived on the property during August and September 2016.
Three Angus bulls (A1, A2 and A3) arrived from Stud A on 31 August 2016. Three Angus bulls (B1, B2 and B3) arrived from Stud B on 28 September 2016. All six bulls were put in a single paddock on 28 September 2016 in isolation from other stock on the property.
There were already a number of bulls on the property. Three bulls (Older Bull, Old Hereford Bull and Old Angus Bull) were joined along with the recently purchased Angus bulls to three mobs of cattle as described below:
On 14 November 2016 a private vet inspected bulls A1, A2, B1 and B3 and found lesions and pus on the penises of all non-working bulls at which time a request was made for assistance from the Braidwood district veterinarian.
The producer routinely observed all mobs of cattle every 2-3 days during the joining period. No bulls had been vaccinated for pestivirus or vibriosis by the producer.
The district veterinarian examined six out of the eight bulls on 23 November 2016. The findings are detailed below:
A1 – mild generalized balanitis (Figure 1)
A2 – mild generalized balanitis
B1 – mild generalized balanitis
B2 – moderate generalized balanitis
B3 – severe generalized balanitis with accumulation of purulent material
Older Bull – would not exteriorize penis
Old Angus Bull – moderate generalized balanitis with sloughing of skin from an ulcerative lesion at the tip of the penis
Old Hereford Bull – would not exteriorize penis
Blood samples and penile swabs were collected from all recently purchased bulls.
The property was revisited on 24 November 2016 for the purpose of sedating and examining Old Hereford Bull. Old Hereford Bull had been observed joining cows up until the day before examination. Old Hereford Bull had a healing ulcerative lesion at the tip of the penis and unruptured vesicles around the base of the penis. He also had a wart on the ventral aspect of penis (Figures 2, 3, and 4).
The property was visited a third time on 15 December 2016 for the purpose of collecting blood samples from the five introduced bulls and Old Hereford Bull.
All bulls were eventually treated with oxytetracycline and tolfenamic acid. Once removed none of the bulls were rejoined to mobs of cows during the current joining period.
All five introduced bulls tested negative for antibody on pestivirus antibody AGID test (0/5).
Bulls A1, B1, B2, and B3 had ureaplasma-like DNA detected from the penile swabs, while there was no ureaplasma-like DNA detected from the penile swab from bull A2 (4/5).
All blood samples were positive on bovine herpesvirus 1 (BHV-1) antibody enzyme-linked immunosorbent assay (ELISA) (6/6).
Pooled penile swabs from introduced bulls and an individual swab from Old Hereford Bull were negative for BHV-1 and bovine herpesvirus 5 (BHV-5) on real time polymerase chain reaction (qPCR) (0/2 tests, 0/6 bulls).
Results of the BHV-1 virus neutralisation test (VNT) on the samples taken in November and December are shown in Table 1.
|Bull ID||23/24 Nov 2016||15 Dec 2016|
|A1||Titre 256||Titre 128|
|A2||Titre 64||Titre 64|
|B1||Titre 512||Titre >=512|
|B2||Titre 256||Titre 128|
|B3||Titre 512||Titre 256|
|Old Hereford Bull||Titre >=128||Titre >=128|
Concerned about a poor outcome at pregnancy testing, the producer extended the joining period in the all three mobs to 12 weeks. All three mobs were pregnancy tested manually in April 2017 by the producer. The producer did not keep specific records on each of the three mobs, but there were only 3-4 open cows per mob at pregnancy diagnosis. The empty cows were culled.
The presence of Ureaplasma diversum was recently confirmed in the Australian cattle population.1 It has been associated with balanoposthitis in bulls, as well as seminal vesiculitis and abnormalities in sperm morphology. However, infection is frequently asymptomatic.2 In cows it is associated with endometritis, salpingitis, and spontaneous abortion. It is also associated with pneumonia, keratoconjunctivitis, and mastitis.3 In the study that confirmed U. diversum in Australia, 14 of the 66 sampled bulls tested positive for the bacterium (21%) using a combination of culture and PCR.1 Of the 39 bulls with genital lesions, 12 tested positive for U. diversum (31%), while 2 of the 27 bulls without lesions tested positive for U. diversum (7.4%).1 Other studies into U. diversum have found a similar relationship.4 These findings suggest that U. diversum may play a role in some cases of balanitis in Australia, although it can be present in bulls that present clinically normal.
BHV is associated with several syndromes, including infectious bovine rhinotracheitis (IBR), encephalitis in calves, infectious pustular vulvovaginitis (IPV) in cows, and infectious pustular balanoposthitis in bulls. Two genotypes of BHV have been implicated in cases of venereal disease, BHV-1 and more recently BHV-5.5 The acute primary infection with active virus excretion is short-lived. However, these viruses produce a latent infection where the virus lies dormant in neural cells and becomes reactivated during periods of stress. During a recent study of infectious reproductive disease in dairy bulls, one of 11 bulls (9.1%) with penile lesions post-mating tested positive for BHV-1 compared to six out of 107 bulls without lesions post-mating (5.6%).6 Another investigation into beef herds in southern Australia found that herd-level seroprevalence to BHV-1 was higher in herds determined or suspected to be affected with atypical balanitis (average 51.8%, range 5.8-97.8%) compared to non-affected herds (35.0%, range 5.8-84.0%).7 However, in four herds selected for closer investigation, antibodies to BHV-1 were not found in a herd with an outbreak of balanitis during the study. Further, while antibodies to BHV-1 were found in the other three herds and lesions consistent with BHV infection were observed in all four herds, neither BHV-1 nor BHV-5 were identified by PCR in any of the 201 penile swabs collected from bulls at various points in the study.7
The definitive cause of the balanitis observed in this case remains elusive, though U. diversum and BHV could both be playing a role. Further, it is impossible to know from the history and diagnostic testing if the pathogens were endemic in the herd or introduced via the newly-purchased bulls. The VNT BHV-1 titres were high but stable, which does not indicate an infection a long time ago nor does it indicate a very recent active infection (P. Kirkland, personal communications). With a recent active infection, a rising titre would be expected at the time of the second sample collection. An infection in the distant past would be expected to yield low titres as VNT titres to BHV-1 decline relatively quickly (P. Kirkland, personal communications).
It is reasonable to assume that balanitis is under-diagnosed in the Australian beef cattle herd. The producer who reported this case diligently observed the bulls during joining. Many producers in the Braidwood district have reported less frequent observation, and absentee landholders are likely to have a limited opportunity to observe bulls during joining. Therefore, many cases of balanitis that lead the bulls to cease serving cows may not be detected until pregnancy testing, or post calving. At the time of detection of poor herd reproductive performance any lesions on the bulls in question would be expected to have healed. As U. diversum PCR and BHV serology can both be positive in clinically normal bulls, a positive result on both tests would not be sufficient to confirm balanitis as the cause of poor reproductive performance in a cow herd. The likely under detection of this syndrome highlights the importance of observing bulls successfully joining cows during joining.
It is difficult to advise this producer on the best course of action to control future balanitis outbreaks. In a recent study of 24 beef herds in southern Australia, using BHV ELISA, all herds had evidence of exposure to BHV, and 75% of the 1,221 cattle tested had evidence of exposure to BHV.7 Given the ubiquity of BHV it is impossible to say that BHV was a contributor to the balanitis. U. diversum is transmitted via coitus, contaminated semen, artificial insemination using fresh and frozen semen, direct contact and congenital infection during passage through the birth canal.2,4 It is shed from semen, preputial and vaginal mucus, conjunctival secretions and milk.2 Therefore, it seems unlikely that the producer could eliminate the U. diversum from his herd. No antibiotic treatment regimen has been documented to consistently eliminate U. diversum contamination in semen2, and therefore even if the producer were able to eliminate it he could very likely introduce it via new bulls or through the use of contaminated semen.
Further research into balanitis in Australian cattle is needed. To date studies have focused on BHV or U. diversum, but no study has attempted to investigate the two pathogens simultaneously. One hypothesis is that the papules caused by BHV infection are vulnerable to secondary infection with U. diversum, and coinfection is much more likely to lead a bull to become unwilling to join. By the time bulls are observed unwilling to join, the acute BHV infection could have been cleared by the immune response, and as a result, serological evidence of past exposure in the absence of pathogen detection would be a plausible outcome. In addition, in the study that failed to detect BHV-1 or BHV-5, one third of samples were positive on a universal herpesvirus PCR. Sequencing of a portion of the positive samples demonstrated the presence of BHV-6.7 BHV-6, also referred to as Bovine Lymphotropic Herpesvirus (BLHV), has been subject to limited investigation.7 Unlike BHV-1 and BHV-5, BHV-6 is a gammaherpesvirus.7 Viruses in this family are specific to lymphocytes and the latent phase is in lymphoid tissue.7 The role of BHV-6 in cases of balanitis is unknown and it could very well have no association with any pathology.
Thank you to the private veterinarian for referring this case. The insight and expertise from Peter Kirkland both during investigation and write-up were much appreciated. The extensive diagnostic work up in this case was made possible by funding from the NSW DPI district surveillance fund.