CASE NOTES


ULCERATIVE BALANITIS IN RAMS – ‘AN ENIGMATIC DISEASE OF UNKNOWN AETIOLOGY’

Bruce Watt1, Petrea Wait2 and Shaun Slattery3

1Central Tablelands Local Land Services, Bathurst NSW

2South East Local Land Services, Cooma NSW

3North West Local Land Services, Narrabri NSW

Paper presented at the Australian Sheep Veterinarian’s Conference, Dubbo, NSW, 9-11 September 2016
Posted Flock & Herd November 2016

INTRODUCTION

In November 1958, Gunnedah (NSW) private practitioner, Dr Phil Knight, reported that 14 of 20, two-tooth Border Leicester rams, joined to a mob of merino ewes 3.5 weeks previously, were found to have ulcerative and necrotic balanitis.1 

A few months later, in mid-April 1959, a sheep producer reported to Dubbo (NSW) Veterinary Inspector, Dr Doug Mumford that, of a mob of 49 18 month old Border Leicester rams, recently purchased then joined to 2300 aged Merino ewes, five had developed ‘sheath rot.’  On inspecting the rams, Mumford found a total of 15 affected rams and noted that ‘the condition was not one of simple sheath rot.’ He described a range of lesions in the rams, from paraphimosis to, most commonly, a deep blood clot filled ulcer, involving part or all of the glans of the penis.2 Both Knight and Mumford considered that disease was initiated by trauma. 

Whilst the aetiological hypotheses of Knight and Mumford have not been supported, little else has changed in nearly 60 years. Ulcerative balanitis (balanoposthitis and vulvitis, knob rot or peetstersiekte) is a disease that commonly but not exclusively affects young British breed (especially Border Leicester) rams, during and after joining, but remains an ‘enigmatic disease of unknown aetiology.’3

Figure 1. Ulcerative balanitis in white Suffolk rams (photograph Bruce Watt)

CASE REPORTS

Case 1 Walgett

In April 2012, 27 young Border Leicester rams (2 ½ years old) were presented for examination after a number were observed to be unable to retract their penises.

The rams were purchased from two different studs, with rams from both studs affected.  The majority of rams had been joined for four weeks before clinical signs developed.  Several rams were joined for the final four days, and a further several rams had not been joined at all.   The rams had been joined to a mob of 850 mixed age merino ewes.  

On examination, two rams were severely affected with very swollen and inflamed penises, which were unable to be retracted into the sheath (paraphimosis).  The penises had secondary bacterial infections, myiasis and a pungent odour.  There was also traumatic damage.  One ram urinated out of the side of the shaft instead of the glans.  There was blood present in the urine.

Five rams were selected for closer inspection of the penis.  One of the rams inspected did not have any lesions.  In two rams the penis could not be exteriorised for examination.  The other two rams had acute lesions.  The lesions consisted of inflammation and a focal area of ulceration of the glans and acute mild haemorrhage, and were quite painful.  On exteriorisation of the penis the ram seemed uncomfortable and kicked out.

Three of the rams were noticeably coughing and sneezing although this could be within the norm for a mob of Border Leicester rams.

The 27 rams were re-examined four weeks later.  

The two rams with paraphimosis at the initial visit had not recovered and were culled.

Again unusual difficulty was encountered in exteriorising the penises, with only 5 of the 23 remaindering rams successfully exteriorised for examination.  No adhesions were observed that account for this difficulty.  No pain was shown during palpation of the sheath in any ram.

Of the five rams examined, one was normal, in 2 rams the glands penis was congested but there were no other lesions, 1 ram had a small 10mm blood clot and 1 ram had a 5mm cauliflower lesions.

The owner reported that the rams were showing homosexual activity as mustered, with no signs of pain.

The owner elected to recommence joining (and sourced an additional 25 older rams to add to the ram mob).  The owner observed the joined rams and ewes for a week and reported that most rams and mountings were normal, with only two rams observed to show some reluctance during mounting.

Case 2 Caloola 

Seven two-tooth White Suffolk rams purchased mid-March 2014, were joined 1 April 2014 and removed from the ewes (mature merinos) on 13 May.  The manager noticed that five of seven rams presented with balanoposthitis. One ram died from the condition and the manager elected to euthanise 3 rams with paraphimosis and necrotic balanitis. One ram retained its penis within its sheath but the entire shaft of the penis was necrotic.  Trueperella pyogenes isolated from all cases. No attempt was made to isolate mycoplasmas or viruses. 

Samples from two cases were submitted for histopathology. Both were similar with extensive areas of thrombosis, haemorrhages and necrosis of the penile gland mucosa. Sub mucosal tissues revealed extensive fibro vascular proliferation. There were masses of bacteria present in all sections. There were no significant changes in the testes and epididymides.

Figure 2. Severe necrotic balanoposthitis in a White Suffolk ram (photograph Bruce Watt)

Case 3 Newbridge

On the 21 October 2014, five of 23 (22%) mixed age Dorset rams were examined with ulcerous lesions 2-3 cm diameter on the external prepuce. The rams had been removed from the ewes in June 2014. The rams were running on a clover dominant pasture. No organisms were isolated on standard culture. Isolation of viruses or mycoplasmas was not attempted. The rams responded slowly to treatment with broad spectrum antibiotics and by flushing the prepuce with dilute chlorhexidine (Hibitane weekly, chlorhexidine acetate 2% w/v, Zoetis). The only concurrent disease noted was one case of epididymitis that was ovine brucellosis negative on serology. The ewes were not examined for concurrent vulvitis or vulvovaginitis. 

Case 4 Cowra

On 7 May 2015, two weeks after a six week joining, 20 mixed age Poll Dorset rams were examined with a range of reproductive tract problems. Three had balanoposthitis (15%). Of the 20 rams examined, the three with balanoposthitis had a firm meaty enlargement of the penis and/or prepuce. These swellings were 3-4 cm diameter and 7-8 cm in length, located cranial to the testicles and were painful on palpation. 

Swabs were taken from three rams for bacteriological examination (but not for mycoplasmal or viral isolation). Trueperella pyogenes was isolated from one case and Histophilus ovis (now somni) was isolated from another. The swabs were culture negative for Brucella ovis (as were blood tests).

The most severely affected ram died despite antibiotic treatment (procaine penicillin), while two other rams were subsequently culled for scrotal abnormalities.

One ram had a scrotal hernia and one had a small fibrosed testicle. The rams were negative for ovine brucellosis. The ewes were not examined for vulvovaginitis.

Case 5 Bombala

On 13 May 2016, after rams were removed from the ewes post-mating, five 1.5 year old and one 3.5 year old Border Leicester rams presented with severe necrotic balanoposthitis from a total of 30 rams (20%). Four of 6 of the affected rams were from the same stud.

Lesions ranged from moderate inflammation of the penis and prepuce with an ulcerated lesion on the tip of the penis (n =2 to full prolapse of the penis with severe inflammation and necrosis of the penis (n = 2).

Histophilus somni and Trueperella pyogenes were isolated, and Ureaplasma diversum DNA was detected. 

The rams were treated with intramuscular long acting oxytetracycline injection (Oxytet LA 1 ml/10 kg) and Prednoderm® ointment was also applied to the lesions every 3rd day. Ten days later the owner advised that all the rams were improving with reduced inflammation, drying of the ulcers and no more discharge. The two with prolapse were still prolapsed. About 1 month after this the owner advised that 5 out of six rams appeared to have recovered but the most severely affected ram was still prolapsed.

No other concurrent disease was noted in the rams and the ewes were not examined for vulvitis or vulvovaginitis.

Figure 3. Deep blood clot filled ulcer in a Border Leicester ram (Photo courtesy Petrea Waite)

DISCUSSION

Balanitis or balanoposthitis is occasionally encountered, especially in young rams, usually associated with joining. In Australia the condition was first described in young Border Leicester rams 1 2 4 but has subsequently been seen in a range of breeds. Grieg 5 considered that there were four main entities; venereal orf infection, pizzle rot caused by a diphtheritic organism (and in particular Corynebacterium renale), a mycoplasma-associated balanitis and vulvitis and finally a condition of unknown aetiology.

Orf infection (scabby mouth) is common in Australian sheep and especially lambs. While the usual manifestations are lesions around the lips and mouth, feet and occasionally the udder in ewes, proliferative orf lesions can occur on the perineal area of lambs. However, the authors are not aware of any reports of orf virus causing balanoposthitis/ vulvovaginitis in mature sheep in Australia.

Corynebacterium renale (in association with a high protein diet) is a well-known cause of posthitis (pizzle rot) in wethers and was considered by Grieg to also be a cause of balanoposthitis in rams. Filmer (1938) in ‘notes on field investigations’ into ‘pizzle rot’, mentions that rams are ‘not uncommonly affected’ and that it can be a serious disease in rams if the preputial cavity is invaded. However, this was before the role of C. renale had been elucidated so it is possible that this latter disease in rams was not associated with C. renale.6  Loste et al described an outbreak of ulcerative posthitis affecting 76 of 80 Rasa Aragonesa rams in Spain associated with a high legume diet. C. renale was isolated from the lesions which were confined to the prepuce without observed concurrent vulvovaginitis in the ewes.7 The authors are not aware of any reports of C. renale being isolated from cases of ulcerative balanitis in rams in Australia.

Mycoplasma spp have been implicated in ulcerative balanitis and vulvitis in South Africa, having been reported in Dorper sheep since 1979. Kidanemariam et al (2005) considered that the disease was multifactorial but included a probable synergism between Arcanobacterium pyogenes (now Trueperella pyogenes) and Mycoplasma mycoides subspecies mycoides (large colony variant). Young rams were more often affected than older rams and lesions were confined to the glans of the penis and lips of the vulva in ewes.8  Pritchard et al (2008) were unable to isolate any Mycoplasma spp in their investigation of three outbreaks of ulcerative balanitis and vulvitis in commercial sheep flocks in the  UK, despite an ‘in-depth investigation.’  Of interest they were unable to isolate any of the other organisms usually associated with ovine balanoposthitis and vulvovaginitis either.3

Australian investigators have also failed to find organisms that can be regarded as causing the balanoposthitis and vulvovaginitis outbreaks reported since Knight and Mumford. Numerous infectious agents have been recovered from cases of balanoposthitis in rams and (to a lesser extent) vulvovaginitis in ewes. Webb and Chick (1976) investigated the condition but were unable to incriminate any organisms. Eamens (1978) consistently isolated haemolytic, lactose fermenting corynebacteria (consistent with Trueperella pyogenes) from cases of ulcerative balanitis detected in the first 8 weeks of joining but not after 12 weeks.9

El-Arabi et al (2014), reporting on clinical and bacteriological findings of balanoposthitis and vulvitis in Scottish sheep, isolated a range of bacteria that differed between affected ewes (n = 21) and rams (n = 8). They confirmed Corynebacterium spp (but not C. renale) and Staphylococcus spp from 31% of the ewe swabs, and organisms possibly T. pyogenes from 13%, whereas in rams the predominant isolates were Streptococcus spp (26%) and Mannheimia haemolytica (19%), with T. pyogenes and Staphylococcus spp in 11%. These authors reported good responses in moderately affected rams to intramuscular long acting oxytetracycline, topical chlorhexidine disinfection and debridement followed by topical chlortetracycline powder.10

While the authors are not aware of any viruses that have been isolated from ulcerative balanitis, Pritchard et al detected ovine herpesvirus type 2 (OHV-2) DNA in the blood of two acutely affected ewes, the vulval ulcers of one and from the penis of an affected ram, using PCR technology.  However, they remark that OHV-2 is ubiquitous in sheep flocks in the UK and they were unable to satisfy themselves of a causal relationship between OHV-2 and vulvovaginitis in sheep.8 A herpesvirus has been isolated as the cause of an outbreak of vulvovaginitis in goats in New Zealand.10

In the cases we report, Trueperella pyogenes was isolated on several occasions (as might be expected) and Histophilus somni was also isolated. Ureaplasma diversum DNA was detected in the Bombala case.  

Given that this disease is uncommon, sporadic and is of unknown aetiology, its management poses challenges.  The behaviour of the disease suggests that an infectious agent is involved in initiating the disease and bacteria such as Trueperella pyogenes and Histophilus somni may exacerbate it. The causal agent may be harboured in the rams and introduced to a property with newly acquired rams but may also be harboured in the ewes, with outbreaks most often occurring in young (and perhaps therefore naïve) rams.

An owner is most likely to observe paraphimosis during or immediately after joining. Immediate examination and treatment of the ram team is then recommended. Given that concurrent vulvitis or vulvovaginitis is likely, examination of the ewe flock may be warranted with treatment of the worst affected cases.

Fortunately, many cases respond to treatment by first principles, with broad spectrum antibiotics, antiseptic irrigation and gentle debridement. In some cases however, the damage to the penis is so severe that euthanasia should be considered.  

This disease can affect a high proportion of the ram team and has the potential to disrupt joining.  Where it is detected early in the joining period the disruption may be managed by using alternative rams or delaying the full joining period until the rams are healed.  In the latter case there may be substantial losses associated with management of the extended and delayed lambing.  Where the problem is not detected during joining a low pregnancy rate may result.  There is the possibility that this may be responsible for a portion of the unexplained low fertility events in the Australian flock.

ACKNOWLEDGEMENTS

The authors would like to thanks Dr Graeme Eamens for his advice and constructive comments. His contribution is greatly appreciated. 

REFERENCES

  1. Knight PR (1958). Ulceration of the galea glandis in Border Leicester Rams During Service. Aust vet J. 42:440
  2. Mumford DH (1959). An Unusual Case of Traumatic Balanitis in Border Leicester Rams. Veterinary Inspector 26
  3. Pritchard GC, Scholes SFE, Foster AP, Mitchell ESE, Lawes J, Ibata G and Banks M (2008). Ulcerative vulvitis and balanitis in sheep flocks. Veterinary Record 163, 86-89
  4. Webb RF and Chick BF (1976). Balanitis and Vulvo-vaginitis in Sheep. Aust. Vet J. 52: 241-242
  5. Greig A (2007). Ulcerative balanitis and vulvitis, in Aitken (ed) Diseases of Sheep, 4th edition, pp 143-145
  6. Filmer JF (1938). Ovine Posthitis and Balano-Posthitis (“Pizzle Rot”): Some Notes on Field Investigations. Aust vet J 14, 47-52
  7. Loste A, Ramos JJ, Garcia LM, Ferrer M and Verde MT. High Prevalence of Ulcerative Posthitis in Rasa Aragonesa Rams Associated with a Legume-Rich Diet (2005). J. Vet. Med A. 52, 176-179
  8. Kindanemariam A, Gouws J, van Vuuren M and Gummow B (2005). Ulcerative balanitis and vulvitis of Dorper sheep in South Africa: a study of its aetiology and clinical features. J S Afr vet Ass, 76(4): 197-203
  9. Eamens GJ (1978). Ulcerative balanitis and balanoposthitis in Border Leicester ram – laboratory aspects. NSW Veterinary Proceedings, 14: 25-26
  10. El-Arabi A, Taylor DJ, Logue DN, Benothman M and Abuargob O (2014). Clinical and bacteriological findings of balanoposthitis and vulvitis in Scottish sheep. J Vet Adv, 4(4): 481-487
  11. Horner GW, Hunter R and Day AM (1982). An outbreak of vulvovaginitis in goats caused by caprine herpesvirus. New Zealand Veterinary Journal, 30: 150-152

 


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