Ovine brucellosis is caused by the bacterium Brucella ovis and is a major cause of epididymitis and reduced fertility in rams. Signs observed in infected flocks may include reduced lambing percentage, extended lambing period, and occasional abortions or birth of weak lambs, leading to reduced flock productivity.
The infected ram is the primary source of infection and perpetuates the disease in a flock6. The organism is excreted in semen. Transmission between rams occurs directly via homosexual activity, and indirectly via venereal infection from a ewe which has been mated by an infected ram followed by a clean ram in the same heat cycle5. Routes of infection include oral, preputial and conjunctival. Although ewes are more resistant to infection, the organism has been isolated from the placenta, vaginal discharges and milk of some ewes4.
Ovine brucellosis has been reported in most of the major sheep-producing regions of the world6. It occurs in all breeds. Treatment of infected rams has been successful in early experimental infections but is not considered worthwhile in practice as the damage to the reproductive organs is often permanent5.
Eradication of the disease involves either culling and replacing the entire ram flock, or identification of infected animals via a serum Complement Fixation Test (CFT) and their removal for slaughter as soon as possible after blood results are known. The CFT has a high sensitivity (>98%) and a very high specificity (100%)7
In some cases producers choose to live with the endemic infection but implement strategies to reduce its impact such as using additional rams at joining, or extending the joining period.
This case discusses some practical issues around an eradication program for ovine brucellosis in a Dorper stud.
The enterprise consisted of 250 Dorper rams (160 seven month old ram lambs and 90 mixed age rams) and 2,500 ewes running on typical NSW Western Division rangeland. Rams were joined twice a year, December - February inclusive and again in May for 10 weeks. At this time, the mixed age rams were running with the ewes so testing of the mixed age mob was delayed until end Feb.
Historically the producer tested annually for ovine brucellosis and had found no evidence of infection for several years leading up to this case. However in the latter part of 2010 and during 2011, testing had been neglected due to pressure of other activities within the enterprise. The owner confirmed finding several rams (also dorper) from his neighbour on his property several months before. In addition, he confirmed that his boundary fencing in some parts were not as secure as he would have wished.
In January 2012, the owner noted that many of his best ram lambs had enlarged scrotums. Ovine brucellosis was confirmed by necropsy (Figures 1 & 2), bacterial culture and serological testing (CFT).
Drought-breaking rains occurred in the summer of 2011-2012 for the first time in many years. There was abundant feed and surface water, and stock were constantly troubled by biting insects. Riding/mounting was consistently being observed as a behaviour. This was especially noticeable when rams were yarded. Riding/mounting occurred in all age groups and continued even when rams were being walked to and from the yards. This behaviour contrasted markedly with ram behaviour during the 2013 season, when riding/mounting was observed to be much less. The reasons for the almost continuous display of sexual behaviour during 2012 season are unknown. It may have been due to the abundance of biting insects and/or green feed as this was the obvious difference between the 2011/12 and other seasons but no evidence of this could be found in the literature.
A veterinarian experienced with ovine brucellosis in Dorpers advised one of the authors that "if you test the conventional way with dorpers (viz re-test at four week intervals) the disease will run away from you"3. The producer agreed to blood test all rams using CFT, as frequently as possible, and remove positives as soon as possible after identification. Testing was undertaken 16 times from 17th Jan 2012 until 30th August 2012, and 184 positive of the 250 rams were identified and culled over this period.
The disease prevalence varied from a peak at the start of testing until test six (Figure 3), when all rams were seronegative.
During this test period until test six, the mean testing interval was 9.8 days (Figure 4). The testing interval then increased to a mean of 14 days over the remainder of the program. This period coincided with a stubborn 'tail' of seropositive animals at each test until test 14.
Owner compliance with immediate removal of identified reactors was identified as a problem, when the data were being analysed. One positive ram was not removed after test 1, was absent at test 2 and retested again at test 3, after which it was finally removed. Two rams positive at test 8 were not removed until they were retested and found positive a second time, at test 9. Another ram found to be positive at test 4 was not removed until it was retested and found positive again at test 5. A deficiency in mustering was also identified, with one mob of negatives not being presented at the next available test. Reading and/or recording and/or transcribing ear tag numbers was also identified as a weakness during data analysis eg on two occasions two rams were recorded with the same tag number at the same test. Again, this was not recognised at the time of testing.
Successful eradication of ovine brucellosis using a test-and-cull program requires immediate removal of test-positive animals. The data indicated that removal of positives was not always complete. This was simply human error. Leaving infected rams together with seronegative animals were opportunities lost. It was only when these positives were detected at subsequent tests, were they removed. Meanwhile, infected rams were free to spread infection throughout the remainder of the mob.
The interval between tests fluctuated despite efforts to test as frequently as possible. The original plan was to retest if possible, every one to two weeks. Test frequency was best (ie shortest) at the beginning of the program but lengthened from test seven onwards. This was due to management difficulties on the property. In hindsight more emphasis could have been put on the necessity to test at weekly intervals, especially considering the rate at which the disease was being spread by promiscuous sexual behaviour amongst the rams.
Testicular palpation was not practised, as it was considered that the CFT test has both high sensitivity and specificity and most animals will seroconvert within 2 weeks1,6. The period between seroconversion (two weeks) and shedding of the organism (3 weeks) needs to be exploited in rapidly spreading infections, with testing every seven days recommended1. In addition, ovine brucellosis eradication is best achieved during the non breeding season, or from about May onwards1.
There is little mention of an increased test frequency in the literature even under rapid spreading conditions, other than the following statement from 1964 "Only when the rate of transmission was accelerated by mating and the proportion of incubating infections became high, was the testing procedure in any way inadequate"8.
The Dorper is an early-maturing breed with epididymal sperm concentrations of ram lambs rising markedly after an age of four and a half months2. Dorpers also have high libido2. The combination of being both precocious and promiscuous can lead to a very rapid spread of the infection. If eradication is attempted during the breeding season, as it was in this case, it warrants a high frequency of testing and accurate removal of positives.
Sixteen serological tests over a period of eight and a half months were required to achieve provisional eradication of B.ovis from the property. Errors in recording, delays in removal of positive rams, inaccurate mustering and decreased test frequency combined together with a rapidly spreading disease through incessant sexual behaviour, lengthened the eradication time considerably and reduced the number of rams by 74%. It is estimated that the time from diagnosis to disease eradication was lengthened by a factor of 2-3.
It is interesting to note that the conventional testing frequency for ovine brucellosis eradication has not changed over many decades. In the meantime, the 'breed mix' of sheep has changed considerably in NSW. This case highlights the need for the 'one size fits all' ovine brucellosis eradication protocol of test interval, to be adjusted to account for breed differences and/or rate of spread. Alarmingly it also highlights the unexpected high rate of recording and compliance errors which may have otherwise gone unnoticed, if the data had not been reviewed. Accurate tag reading, tag transcription, proper identification of positive animals, complete mustering and an appropriate testing interval, are fundamental to an effective eradication program. Owners should record the tag number of every ram removed following each test, with that list to be reviewed weekly by the veterinarian. The inventory of all rams presented for testing should be compared with schedules from previous tests to identify problems with straying or mustering.
In the 18 months since the final seropositive test in early August 2012, several tests on different mobs on this property have confirmed their OB free status. This has been achieved by the owner being scrupulous about biosecurity in all stock purchases, significant expenditure on improved fencing and 'unexplained' strays found are immediately quarantined tested and not released until proved negative.