Sero-Prevalence, Epidemiology, and Public Health Significance of Small Ruminant Brucellosis

Brucellosis is a widespread zoonosis mainly transmitted from cattle, sheep, goats, pigs, and camels through direct contact with blood, placenta fetuses, or uterine secretion or through consumption of the contaminated raw animal product (especially unpasteurized milk and soft cheeses) in endemic areas. Therefore, the objective of this paper are to explain the Current Epidemiological Aspects of Brucellosis and the Importance of Small ruminant Brucellosis for Public Health and briefly illustrate the Economic Importance of Small ruminant Brucellosis. Sources of infection include aborted fetuses, fetal membranes, vaginal discharges and milk from infected sheep and goat. Brucellosis is caused by facultative, intracellular and Gram- negative bacteria called Brucella. Small ruminant brucellosis is caused by B. ovis (for sheep) and B. melitensis (mainly for goats), the latter one is the most virulent species of the Brucella genus. The disease in naturally infected sheep and goats is characterized by abortion in the last trimester of pregnancy, stillbirth and birth of weak offspring in females, and acute orchitis and epididymitis in males. Brucellosis occurs worldwide in domestic animals such as cattle, sheep, goats, camels and pigs and creates a high economic problem for both the intensive and extensive livestock production system in the tropics and a threat to public health. Diagnostic tests fall into two categories: those that demonstrate the presence of the organisms and those that detect an immune response to its antigens. As a general rule, treatment of infected livestock is not attempted because of the high treatment failure rate, cost, and potential problems related to maintaining infected animals in the face of ongoing eradication programs. To control the disease in human, prevention of the disease in reservoir host is important, so test and slaughter followed by proper disposal of seropositive animals to decrease the incidence of infection and effective vaccination and hygienic practices would reduce the disease spreading in/from endemic regions and to lessen the economic and zoonotic effects of brucellosis, the government, public health officials, and veterinarians must collaborate.

Ethiopia has the largest livestock population in Africa, with 65 million cattle, 40 million sheep, 51 million goats, 8 million camels and 49 million chickens [1]. Small ruminants, which account for more than half of the domesticated ruminants in the world, are an important component of the farming systems in most developing countries [2]. A recent estimate indicates that there are about 40 million sheep and 51 million goats in the country. The Ethiopian livestock population is almost entirely composed of indigenous animals. Recent estimates for sheep are 99.6% and 0.3% for local breeds and hybrids respectively. Nearly all goats (99.9%) are indigenous breeds [1]. Despite the importance of small ruminants in the livelihoods of producers, the current productivity of goats and sheep in developing countries remains low, mainly due to under-feeding, poor management systems, and diseases [3]. Brucellosis is caused by facultative, intracellular and Gram-negative bacteria called Brucella [4]. Nine Brucella species are currently recognized, seven of them that affect terrestrial animals are: B. abortus, B. melitensis, B. suis, B. ovis, B. canis, B. neotomae, and B. microti [5] and two that affect marine mammals are: B. ceti and B. pinnipedialis [6].

Brucellosis is an infectious bacterial disease caused by members of the genus Brucella, and that characterized by late abortion, retained foetal membranes, and to a lesser extent, orchitis and infection of the accessory sex glands in males and impaired fertility. The disease primarily affects cattle, buffalo, bison, pigs, goats, sheep, dogs, elk, and camels and occasionally horses [7]. It is essentially a disease of sexually mature animals, the predilection sites being the reproductive tracts of males and female. However, if such an animal becomes pregnant the production of simple carbohydrate eryhritol in the fetus and its membranes cases enormous multiplication of bacteria in the uterus and this are likely to end in abortion [8]. Animals become infected by ingesting contaminated pastures, feedstuffs and water or licking infected placentae, foeti or the genitalia of infected female animals soon after abortion or delivery. Brucella abortus, Brucella melitensis, Brucella suis and Brucella canis can all cause human brucellosis, whereas Brucella ovis and Brucella neotomae have not been reported to cause disease in humans [9].

For the diagnosis of brucellosis, the organism may be recovered from a variety of materials which usually depends on the presenting clinical signs [10].  As a general rule, treatment of infected livestock is not attempted because of the high treatment failure rate, cost, and potential problems related to maintaining infected animals in the face of ongoing eradication programs [11]. To control the disease in human, prevention of the disease in reservoir host is important, so test and slaughter followed by proper disposal of seropositive animals to decrease the incidence of infection and effective vaccination and hygienic practices would reduce the disease spreading in/from endemic regions [12].Office International des Epizooties (OIE)  sketch brucellosis as the second most important zoonotic disease in the world, accounting for the annual occurrence of more than 500,000 human cases [13].The distribution of B. melitensis is more restricted than that of B. abortus and its primary area of occurrence is in the Mediterranean region including southern Europe. Infection is also present in West and Central Asia, Mexico and countries in South America and countries in Africa.[14]. As a result, the goals of this paper are to: Explain the Current Epidemiological Aspects of Brucellosis and the Importance of Small ruminant Brucellosis for Public Health. Briefly illustrate the Economic and Importance of Small ruminant Brucellosis. Show the seroprevalencen status of small ruminant brucellosis in different geographical areas of Ethiopia.

Etiology

Brucella species are facultative intracellular gram-negative cocco-bacilli, non-spore-forming and non-capsulated. Although Brucella species are described as non-motile, they carry all the genes except the chemotactic system, necessary to assemble a functional flagellum. Nine Brucella species are currently recognized, (Table1) seven of them that affect terrestrial animals are: B. abortus, B. melitensis, B. suis, B. ovis, B. canis, B. neotomae, and B. microti [5] and two that affect marine mammals are: B. ceti and B. pinnipedialis [6]. The first three species are called classical Brucella and within these species, seven biovars are recognized for B. abortus, three for B. melitensis and five for B. suis [15].

Table 1: Brucella species and their hosts

Source: [16].

Epidemiology 

The geographical distribution of brucellosis is constantly changing, with new foci emerging or reemerging. Brucellosis is a disease of worldwide distribution occurring in domestic as well as wild animals. It has been reported wherever animals are raised all over the world [17]. Although some of the industrialized countries in Europe and America have achieved the eradication of brucellosis in domestic animals through intensive control and eradication schemes, the disease is still a serious problem in developing countries [18-19]. B. melitensis is the most virulent species of the Brucella genus and the ones isolated most frequently in small ruminants in the Mediterranean, the Middle East and Latin America [20]. Brucellosis is a barrier to trade in animals and animal products and causes significant losses from abortion, as well as being a serious zoonosis [21].           

Modes of transmission

The primary route of infection is through ingestion of contaminated feed and water, inhalation during overcrowding, contact through intact skin and conjunctiva, lambs may be infected while in the uterus or by suckling infected milk of their mother. Venereal transmissions by the infected ram to susceptible ewes appear to be rare. Transmission may occur by artificial insemination [22]. Sources of infection include aborted fetuses, fetal membranes, vaginal discharges and milk from infected sheep and goat. Studies indicate that 70-90

Host factors  

It is widely accepted that susceptibility increases with sexual development and pregnancy [24]. Brucella melitensis infection causes disease only in adult (sexually mature) females and males. Young animals may be infected but do not show any clinical sign and generally show only a weak and transient serological response ([22]. In B. melitensis infection males of sheep and goat are less susceptible than females. Brucella ovis has a great affinity for the reproductive tract of the male than the female [25]

Pathogen risk factor

Brucella is intracellular bacteria, hence has protection from the innate host defense and from therapeutics, moreover in quiescent state does not cause formation of humeral antibodies [24]. Brucella survives for up to 4 months in milk, urine, water and damp soil under proper environmental condition [25]. Disinfectants like caustic soda, formalin 2%, and Lysol 1

Bacteriological methods 

Isolation of the organism is considered the gold standard diagnostic method for brucellosis since it is specific and allows bio typing of the isolate, which is relevant under an epidemiological point of view Al Dahouk). However, in spite of its high specificity, culture of Brucella spp. is challenging. Brucella spp. is a fastidious bacterium and requires rich media for primary cultures. Furthermore, its isolation requires a large of viable bacteria in clinical samples, proper storage and quick delivery to the diagnostic laboratory [32].

Serological methods 

Serological tests are crucial for laboratory diagnosis of brucellosis since most of control and eradication programs rely on these methods. Inactivated whole bacteria or purified fractions (i.e., lipopolysaccharide or membrane proteins) are used as antigens for detecting antibodies generated by the host during the infection. Antibodies against smooth Brucella species (e.g., B. abortus, B. melitensis, and B. suis) cross react with antigen preparations from B. abortus, whereas antibodies against rough Brucella species (e.g., B. ovis and B. canis) cross react with antigen preparations from B. ovis [31].  Although several serological methods are currently available, these tests can be classified as screening tests [31].

Enzyme linked immunosorbent assay

Enzyme linked immunosorbent assay (ELISA) has become popular as a standard assay for the diagnosis of brucellosis, serologically. It measures IgG, IgA and IgM antibodies and this allows a better interpretation of the clinical situation. The diagnosis of brucellosis is based on the detection of antibodies against the smooth LPS. Detection of IgG antibodies is more sensitive than detection of IgM antibodies for diagnosing cases of brucellosis but specificity is comparable [33]. Compared to the conventional agglutination methods, ELISA is more sensitive in acute and chronic cases of brucellosis and it offers a significant diagnostic advantage in the diagnosis of brucellosis in endemic areas [34, 35]. The indirect ELISA (i-ELISA) has been used for serologic diagnosis of brucellosis in sheep, goats and pigs. It has also been used for diagnosis using serum or milk from cattle [36]. O ELISA-i has been usually used for smooth LPS Brucella spp., and it is sensitive and specific for B. abortus or B. melitensis, but it is not capable of differentiating antibodies induced by the vaccine strains S19 or Rev1[37]. Sensitivity of i-ELISA varies from 96 to 100% and its specificity from 93.8% and 100% [38]. The competitive ELISA (c-ELISA) with smooth Brucella LPS as antigen is used for detection of anti-Brucella in serum samples from cattle, sheep, goats, and pigs. This test is capable of differentiating vaccine antibody response from actual infections, and its sensitivity varies from 92 to 100%, whereas the specificity ranges from 90 and 99% [39].

Rose Bengal plate test 

Rose Bengal plate test [RBT] is an agglutination test that is based on reactivity of antibodies against smooth lipopolysaccharide (LPS). As sensitivity is high, false negative results are rarely encountered. To increase specificity, the test may be applied to a serial dilution (1:2 through 1:64) of the serum samples [40]. The present World Health Organization (WHO) guidelines recommend the confirmation of the RBT by other assays such as serum agglutination tests [40].

Treatments

Due to intracellular localization of Brucella and its ability to adapt to the environmental conditions encountered in its replicative niche e.g., macrophage [15]. treatment failure and relapse rates are high and depend on the drug combination and patient compliance. The optimal treatment for brucellosis is a combination regimen using two antibiotics since monotherapies with single antibiotics have been associated with high relapse rates [42)]. The combination of Doxycycline with Streptomycin (DS) is currently the best therapeutic option with less side effects and less relapses, especially in cases of acute and localized forms of brucellosis [43].

Public Health and Economic Impact of Small Ruminant Brucellosis

Public health impact

Human brucellosis is widely distributed all over the world. It is considered by the FAO, the WHO and the OIE as one of the widest spread zonooses in the world [44]. Almost all human cases of brucellosis are acquired from animals, in particular goats and sheep. In humans, ovine/caprine brucellosis caused by B. melitensis is the most important clinically apparent disease and remains one of the most common zoonotic diseases worldwide, with more than 500,000 human cases reported annually [43, 45]. The disease is primarily an occupational risk in exposed professions, i.e., veterinarians, farmers, laboratory technicians, abattoir workers, and others who work with animals and their products. Inhalation is often responsible for a significant percentage of cases in abattoir employees. Contamination of skin wounds may be a problem for persons working in slaughterhouses or meat packing plants or for veterinarians [12].

Economic significance impact

Brucellosis results in an obstacle to trade of animals, animal products and animal movement. It causes economic losses because of abortion or breeding failure in the affected animal population, diminished milk production and in human brucellosis result in reduced work capacity through the sickness of the affected people [46]. Brucellosis also presents a significant impediment to the economic potential of the large population of small ruminants. Since small ruminants and their products are an important export commodity, detaining seropositive animals in quarantine has a negative economic impact [47].

Control and Prevention

As the ultimate source of human brucellosis is direct or indirect exposure to infected animals or their products, prevention must be based on elimination of such contact. The obvious way to do this-elimination of the disease from animals is often beyond the financial and human resources of many developing countries. The technical and social difficulties involved in eradicating B. melitensis from small ruminants have even taxed the resources of some developed countries. In many situations, there is little alternative but to attempt to minimize the impact of the disease and to reduce the risk of infection by personal hygiene, adoption of safe working practices, protection of the environment and food hygiene. prophylaxis currently plays little part in the prevention of human disease [25].

Prevention and control of brucellosis can be adopted realistically through an understanding of local and regional variations in animal husbandry practices, social customs, infrastructures and epidemiological patterns of the disease [48]. The common approaches used to control brucellosis includes quarantine of imported stoke and decide for or against immunization of the negative animals [22]. Eradication by test and slaughter principles are based on the magnitude of disease prevalence and economic status at countries and handling hygienic disposal of aborted fetuses, fetal membrane and discharges with subsequent disinfection of contaminated area [25]. 

In endemic areas, all placentas and dead fetuses should be buried as a routine practice. The need to test and cull, introduced and resident animals likely to be carriers is recommended, but difficult to be effective because of the inaccuracy of the tests [22]. The experience from all over the world, that vaccination is in most situations the only practical method of control of brucellosis in sheep and goats. Immunization with effective vaccines helps to get the infection under control, limit its spread, prevent human infections and reduce economic losses [49].

Prevalence Status of Small Ruminant Brucellosis 

The pastoral and agro-pastoral production system represent approximately 45-55% of the cattle, 75% of the small ruminants, 20% of the equines and 100% of the camels of the total national livestock population. The main mobile pastoralists in Ethiopia are the Somalis (Somali region) in the east, the Afars (Afar region) in the northeast, the Borena Oromos (Oromiya region) in the south and south-east and the Southern Omo people (SNNPS region) in the south and partly in the Gambela and Benishangul regions and around the Dire Dawa Administration. Despite the large size of the regional livestock population, its economic contribution to the regional and national economy is not significant, mostly due to natural and human limitations [50]. Most of the studies which conducted on brucellosis were entirely based on estimation of seroprevalence of the disease. A sero-surveillance study carried out in small ruminants in different regions clearly demonstrated that the disease exists in Ethiopia. According to the current sero-surveillance findings of the disease in the country, low infection rate was recorded at Bahir Dar Town of Amhara Regional State [52]. and the highest was reported at Tellalak District of Afar Regional State [53] (Table 2).

Table 2: Sero-Prevalence of small ruminant brucellosis in different pastoral and agro pastoral area of Ethiopia.

Brucellosis is worldwide and has a high prevalence in different areas of Ethiopia. Brucellosis affects both animals and humans, has a very high economic and public health impact. Its impact on public health is very well related to the infected animal species from which human transmission occurs. The disease is transmitted from infected animals to human beings through several routes. It is a special hazard to occupational groups. It causes considerable losses in small ruminants as a result of abortion and a reduction in milkyield. The following suggestions were made in light of the information provided in the conclusion: A national plan should be in place to manage the brucellosis control mechanism in small ruminants. A new vaccination against brucellosis in sheep and goats should be created using unrefined strains that do not have the vaccine's drawbacks. To lessen the economic and zoonotic effects of brucellosis, the government, public health officials, and veterinarians must collaborate.