brucellosis (Brucella ovis)

Identity

Preferred Scientific Name

• brucellosis (Brucella ovis)

International Common Names

• English: Brucella ovis ram epididymitis; brucellosis in sheep; epididymitis of rams; epididymitis, orchitis, in sheep, goats, and pigs; orchitis; ovine contagious epididymitis; ovine epididymitis; ovine epididymitis (Brucella ovis); seminal vesiculitis, adenitis, in large animals

Pathogen/s

Overview

Ovine contagious epididymitis is a chronic disease that affects the reproductive tract of rams, causing reduced fertility (Burgess, 1982). The causative agent was isolated in the early fifties in New Zealand and Australia (McFarlane et al., 1952; Simmons and Hall, 1953), and the organism was named Brucella ovis in 1956 (Buddle, 1956). The micro-organism causes a transmissible disease unique to sheep in which the major symptom is epididymitis in rams and occasionally abortion in ewes. The disease in rams causes economic loss to the sheep industry of many countries mainly due to low fertility rates. Humans are not affected by B. ovis.

Ovine epididymitis (Brucella ovis) is on the list of diseases notifiable to the World Organisation for Animal Health (OIE). For further information on this disease from OIE, see the website: www.oie.int.

Host Animals

Hosts/Species Affected

Natural infection is almost exclusively associated with sheep. Cattle, goats and deer are susceptible to B. ovis in artificial transmission experiments but, of these, natural cases have been reported only in deer (Rider, 2001).

Systems Affected

Distribution

Brucella ovis infection is usually found in countries with an intensive sheep farming sector. Disease has been reported in Latin American, North American, South American and European countries as well as Australia, New Zealand and South Africa, but may occur in most sheep-raising countries, with the apparent exception of the United Kingdom.

For current information on disease incidence, see OIE's WAHID Interface.

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

Lesions in male animals are largely in the epididymis, tunica vaginalis and testis varying from a slight enlargement of the epididymis, either unilateral or bilateral, to large indurations. Spermatoceles containing partially inspissated spermatic fluid may be found in the epididymis and fibrous atrophy can occur in the testis. The tunica vaginalis is often thickened and fibrous, and can have extensive adhesions. There are generally no clinical signs in the ewe although occasionally infection causes abortion or the birth of weak or stillborn lambs, associated with a placentitis.

Diagnosis

The diagnosis of Brucella ovis infection in rams is complicated by the fact that infected rams retain a degree of sexual activity and fertility although the total concentration and number of normal living spermatozoa are significantly reduced (Cameron and Lauerman, 1976; Blasco, 1990). Palpation of the testicles may give a presumptive diagnosis but epididymitis is not unique to infection with B. ovis. Semen or vaginal smears can be examined following staining by Stamp’s method and characteristic coccobacilli should be demonstrated in many infected animals. Examination of stained smears of suspect tissues (ram genital tract, inguinal lymph nodes, placentas, and abomasal content and lung of fetuses) may also allow a rapid presumptive diagnosis. However, other bacteria with similar morphology or staining characteristics can also be present in such samples and microscopy results should always be confirmed by culture of the microorganism.

Isolation of the agent from a diseased animal unequivocally establishes the infection but because excretion of the organism may be intermittent, infected rams may test culture negative (Hughes and Claxton, 1968). Nevertheless, the most common sites from which B. ovis can be isolated at necropsy are the epididymis and accessory sexual glands (Worthington et al., 1985). Recovery of B. ovis from dead lambs is most frequent from the lungs, abomasum contents, and the spleen (Burgess, 1982).

As with B. abortus and B. melitensis, serological tests are essential for the diagnosis of B. ovis. The most efficient and commonly used tests are the complement fixation test (CFT), the double agar gel immunodiffusion (AGID) test and the indirect enzyme-Iinked immunosorbent assay (I-ELISA). While the only test prescribed by the OIE and the European Union (EU) for international trade is the CFT, the AGID test is simpler to perform and has been shown to have similar sensitivity to CFT. Disadvantages of the CFT include technical complexity, anti-complementary activity of some sera, the difficulty of performing it with haemolysed sera, and the prozone phenomena. In contrast the simplicity and easy interpretation of AGID make it useful for routine use in nonspecialised laboratories. Studies have shown that I-ELISA may be more sensitive and specific than either of these tests (Marin et al., 1989, Ris et al., 1984, Spencer & Burgess, 1984; Worthington et al., 1984; Worthington et al., 1985) but further standardisation and validation is required.

Differential molecular assays such as the Bruceladder multiplex PCR or SNP typing (Gopaul et al., 2008; Lopez-Goni et al., 2008) and specific PCR tests (Xavier et al., 2010) are now available that can readily identify B. ovis following growth of suspect colonies. There are however still limited reports of the application of PCR directly to field material (Xavier et al., 2010; Costa et al., 2016). Multiplex PCRs that discriminate from other common bacterial causes of ovine epididymitis have also been reported (Saunders et al., 2007; Moustacas et al., 2013). Although the limited data available to date suggests that B. ovis is a genetically conserved species, tools such as multilocus sequence typing and multilocus variable number of tandem repeat typing (Whatmore et al., 2006; Whatmore et al., 2007; Whatmore et al., 2016) may prove increasingly useful to understand both global and local epidemiology and to track the transmission and spread of strains (Dorneles et al., 2014). B. ovis whole genome sequences are now available (Tsolis, 2009) and it is likely that whole genome sequencing will be an increasingly important epidemiological tool in the future.

List of Symptoms/Signs

Disease Course

Blasco, (1990) extensively reviewed the pathogenesis, pathology and histology of Brucella ovis infection. Briefly: as with other Brucella infections there is a period of generalized infection (Enright, 1990). After infection, the bacteria remain in the lymph nodes close to the entry site for 2-3 weeks. This is followed by a bacteraemic stage that may last up to 2 months. The organism infects the reticuloendothelial system and various organs (Biberstein et al., 1964). Although the bacteria can be isolated from several tissues they usually localize in the epididymis causing an epididymitis. However, not all infected rams develop a palpable epididymitis. Lower fertility and seminal degeneration almost always precede the appearance of lesions. In most cases there is a unilateral epididymitis affecting the tail of the epididymis. Sometimes the body and the head of the epididymis are also affected (Blasco, 1990). Following localization in the epididymis there is perivascular oedema and the infiltration of lymphocytes and monocytes into the peritubular tissue. Eventually the epithelial cells are destroyed, either by bacterial products or by extravasation of spermatozoa. This leads to formation of spermatic granulomas that block the epididymis (Jubb et al., 1985).

Testicular atrophy is characteristic for chronic infection. This affects semen quality, breeding efficiency and capacity. The affected testicle appears firm but on the cut surface granulomas and calcification may be apparent (Blasco, 1990). During the bacteraemic stage B. ovis can cause chronic interstitial nephritis resulting in permanent shedding of B. ovis in the urine (FAO/WHO, 1986).

Only ewes exposed to infection at early or mid-pregnancy develop infection that may lead to abortion. In pregnant sheep, B. ovis may cause placental necrosis and abortion 23-80 days post infection (Enright, 1990). For abortion to occur there has to be a sufficient accumulation of bacteria and exudate to cause necrosis of the placenta and separation from the caruncles. Thus, the primary effect of infection in ewes is a placentitis that interferes with normal foetal nutrition resulting in the death of lambs and abortion, or in birth of lambs with low birth weight (FAO/WHO, 1986). Dead foetuses are usually oedematous. Calcified plaques on the soles of the hooves are characteristic of abortion due to B. ovis infection (Enright 1990).

Epidemiology

Brucella ovis is the least pathogenic of all the Brucella species that infect domestic animals. It almost exclusively infects sheep and affects mainly rams, although male goats experimentally inoculated with B. ovis develop lesions similar to those observed in rams (Blasco, 1990). Whereas in practice the source of infection is contaminated semen excreted by infected rams, not every infected ram excretes B. ovis in the semen (Burgess, 1982). Passive venereal transmission is the main route of spread for B. ovis infection (Buddle, 1955; Hartley et al., 1955). However, passive venereal transmission requires both an infected and non-infected ram to mate with the same ewe in one oestrus cycle. Rams may become infected at the post-abortion oestrus, as B. ovis could be found for 10 days in the vaginal discharge following abortion (Hughes, 1972). Although venereal transmission is the most important route of exposure (Jubb et al., 1985), demonstration of infection in 4-month-old rams (Burgess et al., 1982) casts doubt whether age susceptibility to B. ovis infection exists (Blasco, 1990). It has been suggested that sodomy is responsible for the spread of infection amongst young rams (Burgess, 1982). Transmission, however, may also occur when healthy rams are housed in pens where previously infected rams were kept (Clapp et al., 1962). Furthermore, since rams often sniff the genital organs of other rams infection via the nasopharynx is also possible (FAO/WHO, 1986). Under experimental conditions sheep can be infected with B. ovis via several routes (Muhammed et al., 1975; Simmons and Hall, 1953; Blasco, 1990).

Susceptibility to B. ovis may vary between breeds of rams (Cameron et al., 1971; Blasco, 1990). Rams are more susceptible to infection than ewes. Ewes also rarely become actively infected or transmit the disease during abortion to another ewe although they usually develop complement fixation titres. Since only a few infected ewes abort or have dead or weak lambs it would appear that ewes are relatively resistant to infection (Buddle, 1955; Hartley et al., 1955; Clapp et al., 1962; Haughey et al., 1967). It is generally accepted that the role of an infected ewe in congenital transmission of the disease is negligible (Blasco, 1990).

Impact: Economic

Outbreaks of Brucella ovis infections may cause significant economic loss in countries where the sheep industry plays a role in the national economy. The main economic problems arise from reduced numbers of lambs born, a high percentage (20%) of barren ewes, and a high percentage of lambs born alive that die within six weeks of birth. Furthermore, prolonging of the lambing season due to disease interference with the normal breeding scheme is of significant economic importance. Lamb yield may drop in infected flocks from 100% to 25% (FAO/WHO, 1986).

Zoonoses and Food Safety

There are no confirmed reports of human infections with B. ovis and, unlike many Brucella, this species is not considered zoonotic.

Disease Treatment

Treatment of Brucella ovis ram epididymitis with antibiotics is very expensive and not very effective. The effect of the treatment is of a short duration, with not all the shedders being cured and the fertility of some animals remaining impaired (Dargatz et al., 1990; Hajtós et al., 1994). Thus, antibiotic therapy is not endorsed except when rams with high breeding quality are infected (Blasco, 1990).

Prevention and Control

Disease prevention can be achieved by eradicating B. ovis from all the rams in a flock. However, since seronegative and clinically normal rams may be latent excretors of B. ovis, detection of all infected rams may not be simple. Vaccination of both rams and ewes is probably the most economical and practical means for medium-term control of B. ovis in areas with a high incidence of infection. The best available vaccine against B. ovis infection in rams is the live Brucella melitensis strain Rev 1 (Plommet, 1991; Ridler and West, 2011). A dose of 10⁹ CFU given subcutaneously induces good protection in 3-5- and 13-month-old rams. However, because Rev 1 vaccination elicits an immune response that may interfere with the serological diagnosis, the use of conjunctival vaccination is suggested (Blasco, 1990; Plommet, 1991). The B. abortus RB51 live vaccine has not proven successful against B. ovis in sheep (Jiménez de Bagüés et al., 1995) and no alternative vaccines are currently available.

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