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Brucellosis- A Prominent Bacterial Zoonosis and Strategies for Prevention and Control – A Review

Vijay Sharma Subha Ganguly
Vol 7(8), 18-29
DOI- http://dx.doi.org/10.5455/ijlr.20170605022440

Brucellosis is a major bacterial zoonosis of global, economic and public health significance. The disease has also been reported in recent years from wild and marine mammals and birds. The presence of brucellosis in wild animals, with a potential for continuous transfer to domestic animals and from them to humans is another epidemiological issue. In cattle, B. abortus causes abortion, stillbirth and weak calves with abortions usually occurring during the third trimester of gestation. In goats, B. melitensis can cause abortion, retained placenta, orchitis and epididymitis. Abortions usually occur during the fourth month of gestation in goats. Clinical manifestations of disease in man are weakness, fever, profuse sweating especially in night, loss of weight, generalized body ache etc. Swelling in testes and burning micturition due to orchitis and urethritis, respectively, are also peculiar symptoms of disease in man.


Keywords : Animals Brucellosis Bacterial Zoonosis Epidemiology Human

Introduction

Brucellosis is a global zoonotic disease associated with significant morbidity that can lead to increased rates of spontaneous abortion in livestock and in humans. Brucellosis is also called Bang’s disease, contagious abortion, infectious abortion, undulant fever, malta fever and Mediterranean fever. The disease is widely distributed throughout the developing world, considered to be a serious problem in at least 86 countries (WHO, 1996). In India, brucellosis costs around Rs. 350 million annually in terms of food, animals and man-day’s losses (Kunen, 1994), and Rs. 240 million annually due to cattle and buffalo brucellosis (Schwabe, 1984). Dairy cattle, sheep, goat and swine are the main species involved among the domestic animals.

Brucella has always been of zoonotic importance all though the history and clinical conditions synonymous with brucellosis have been described since the time of Roman Empire (Godfroid et al., 2005). Cocco-like forms resembling Brucella havebeen detected in carbonized cheese from the Roman era (Capasso, 2002). But, it was in 1887, when Sir David Bruce isolated the organism from the spleen of a British soldier who died from the Mediterranean fever in Malta and named it as Micrococcus melitensis. Later, it was renamed Brucella melitensis in the honor of Sir David Bruce (Godfroid et al., 2005). There are six recognized species for genus Brucella– B. melitensis, B. abortus, B. suis, B. canis, B. ovis and B. neotomae; and two provisional species B. pinnipediaeand B. cetaceae (Table1). This taxonomic classification is mainly based on the difference in host preference and pathogenicity which can be attributed to various proteomes, as exemplified by specific outer-membrane protein markers (Pappas et al., 2005).

Table 1: Taxonomic Classification of Genus Brucella

Species Biotype Animal Hosts
B. melitensis 1-3 Goats, sheep
B. abortus 1-6,9 Cows, Camels, Yaks, buffaloes
B. suis 1-5 Pigs ( biotypes 1-3), wild hares (biotype 2), caribou and reindeer (biotype 4), rodents (biotype 5)
B. canis Canines
B. ovis Sheep
B. neotomae Rodents (Desert wood rat)
B. pinnipediae & B. cetaceae (provisional) Minke whales, dolphins, porpoises (pinnipediae), seals (cetaceae)

Among all species of BrucellaB. melitensis is considered to be the most pathogenic to humans (Benkirane, 2006) causing maximum number (up to 90%) of human cases (Corbel, 1972; 1973; 1997) followed by B. abortus and B. suis. Brucellosis is an occupational direct anthropozoonosis. Public health significance of brucellosis is not only because of its status as one of the world’s major zoonoses but also because it causes a serious reduction in availability of quality food, especially the animal proteins. It also poses a serious threat to livestock economy by causing abortion, loss of offspring, infertility and reduction in milk yield. Most cases in humans are caused by contact with infected animals or animal products, such as unpasteurized milk and cheese prepared from infected unpasteurized milk (Papaps et al., 2005).

History

History of brucellosis in India dates back to 1897 when Wright and Smith (1897) reported serological evidence of the disease in invalidated soldiers from India. But, the first investigation of contagious abortion in livestock associated with brucellosis was conducted by the Imperial Veterinary Research Institute, Mukteshwar (Anon, 1918). However, the credit of first extensive and systematic study of brucellosis goes to Polding (1948) who conducted a nationwide survey and observed considerable variation in incidence of brucellosis in different regions of India.Brucellosis is a contagious disease of livestock with significant economic impact. It is also a zoonotic disease, highly infectious for humans causing a disease called undulant fever or Malta fever. Brucellosis is a zoonosis present probably, even in Roman Era as the bone lesions suggestive of brucellosis are described in that time mummies (Capasso, 2002).

Epidemiology

Pattern of Distribution

Animal brucellosis is endemic worldwide and bovine brucellosis, caused by B. abortus, remains the most widespread form in animals (Corbel, 1997). Human brucellosis is mainly caused by four species – B. melitensis, B. abortus, B. suis and B. canis. Among these, B. melitensis remains the principal cause of human brucellosis worldwide and may account for up to 90% of all brucellosis cases with B. melitensis biotype 1 predominating in India (Mantur et al., 2006) and Spain (Colmenero et al., 1996), type 2 in northwestern Greece and type 3 in Turkey (Bodur et al., 2003). The infective dose of B. melitensis is low (10 organisms) (Boral et al., 2008). Brucellosis in wild life is of greater concern as spillage of infection has been reported in industrialized countries (Davis, 1990). Cross-infection between species further adds to the complexity of the disease.

Host Range

Though extremely rare, occasionally human-to-human transmission takes place through tissue transplantation or sexual contact (Mantur et al., 1996). Also contact with vaginal discharge, urine, feces and blood of infected animals through broken skin and mucous membrane of conjunctiva and inhalation of the organism can cause the disease. Brucellosis is an occupational hazard for livestock owners, abattoir workers, dairy workers, shepherds, farmers, veterinarians, para-veterinarians and laboratory workers. Brucellosis has been shown to be one of the most common laboratory acquired infections (Noviello et al., 2004). With the increase in global tourism, brucellosis is emerging as a common imported disease in the developed world (Memish and Balky, 2004).

Transmission

Most cases in humans are caused by contact with infected animals or animal products, such as unpasteurized milk and cheese prepared from infected unpasteurized milk (Papaps et al., 2005). Consumption of unpasteurized milk and their products especially soft cheese, yoghurts and ice-cream (Eckman, 1975), undercooked traditional delicacies such as liver (Malik, 1997) and spleen (Elbeltagy, 2001) are mainly responsible for human brucellosis. Camel milk is considered to be the most important source of infection in Middle East countries and Mongolia (Mantur and Amarnath, 2008).

Disease management strategies for brucellosis involve vaccination, testing and slaughter/segregation. For various reasons, test and slaughter policy is difficult to implement in India. B. abortus S-19 and B. melitensis Rev-1 vaccines are two most widely used immunoprophylactic biologicals in cattle and small ruminants, respectively. Once a policy of vaccination is adopted in an area, it will be necessary to develop procedures that can differentiate vaccination and infection status of animals. So far progress in this area of study is meager. Use of novel proteins as vaccine antigens have been investigated by many workers. Besides, accidental exposure to live vaccine strains can cause avoidable problems for animal handlers and professionals.

Risk Factors

  1. Consumption of unpasteurized milk and their products especially soft cheese, yoghurts and ice-cream (Eckman, 1975), undercooked traditional delicacies such as liver (Malik, 1997) and spleen (Elbeltagy, 2001) are mainly responsible for human brucellosis.
  2. Camel milk is considered to be the most important source of infection in Middle East countries and Mongolia (Mantur and Amarnath, 2008).
  3. Though extremely rare, occasionally human-to-human transmission takes place through tissue transplantation or sexual contact (Mantur et al., 1996).
  4. Also contact with vaginal discharge, urine, feces and blood of infected animals through broken skin and mucous membrane of conjunctiva and inhalation of the organism can cause the disease. Brucellosis is an occupational hazard for livestock owners, abattoir workers, dairy workers, shepherds, farmers, veterinarians, para-veterinarians and laboratory workers.
  5. Brucellosis has been shown to be one of the most common laboratory acquired infections (Noviello et al., 2004). With the increase in global tourism, brucellosis is emerging as a common imported disease in the developed world (Memish and Balky, 2004).

Current Scenario of the Infection in Human and Animals

Brucellosis results in huge economic losses and social burden on the society especially in the developing countries and it is one of the most common occupational anthropozoonoses present world-wide. Due to the slow onset and absence of pathognomonic signs and symptoms, it is usually diagnosed quite late and by the time the animal herd is already infected. Important animal species of genus Brucella viz. Brucella abortus associated with cattle and B. melitensis associated with sheep and goat (Corbel, 1997). In humans, 90 percent cases of brucellosis are said to be associated with B. melitensis (Benkirane, 2006).

Prevalence of brucellosis poses a direct public health implications and act as a potential barrier to international trade of animals and animal products (WHO, 1997). Some recent reports regarding Brucella infection involving marine mammal and birds have given a new orientation to the epidemiology of brucellosis. Although, dairy cattle, sheep, goats and swine are major reservoirs of the disease and horses, camels and wild animals can also suffer occasionally. Brucellosis management remained a difficult task as control programmes require vaccination of animals besides other drastic measures. However, the difficulty in differentiating between vaccinated and infected animals has posed a serious limitation in interpretation of results during vaccination campaigns (OIE, 2008 a,b; 2009 a,b).

Although the disease is eradicated in bovines (B. abortus) in many developed countries like Australia, Canada, Cyprus, Denmark, Finland, Netherlands, New Zealand, Norway, Sweden and United Kingdom, it is still present in Mediterranean countries of Europe, Northern and Eastern Africa, near East countries, India, Central Asia, Mexico, Central and South America (Seleem et al.,2010). As reported by Schwabe (1984), in India, there have been annual losses of Rs. 240 millions due to bovine brucellosis alone. As far as eradication of B. melitensis from small ruminants is concerned, no country has yet been able to achieve it (Seleem et al., 2004). As mentioned, the disease is present in India, in both livestock (Renukaradhya, 2002; Rashid et al., 2008; Boral et al., 2009) as well as humans (Agasthya et al., 2007; Smith and Kadri, 2005). Moreover, >70 percent of Indian population is rural which is constantly exposed to the infected animals resulting in continuous transmission of disease to humans (Park, 2009). Therefore, the presence of disease in farmers, veterinarians and other occupationally exposed groups can never be questioned. Although, in past few studies, involving humans and animals had been performed in Jammu region, the status of disease in border areas of Jammu is largely unknown, thus the present study was aimed to evaluate the prevalence of brucellosis in goats and human beings along with their epidemiological features in and around border areas of Jammu. The study also compared the various serological tests viz., RBPT, STAT and I-ELISA, as they are routinely used tests in the diagnosis of brucellosis; however, no single test in itself is fully satisfactory and each test is associated with certain disadvantages (MacMillan, 1990; Nielsen, 2002). Also, due to the lack of reliability of tests, the seroprevalence has been calculated individually for each test.

Public Health Significance

Brucellosis is major health problem in Mediterranean, Middle East, India, Latin America, Africa, parts of Mexico and parts of Asia (Refai, 2002). Syria has the highest annual incidence worldwide with an alarming 1603 human cases per million per year (Boral et al., 2008, 2009). Rate of human infection is high in Peru, Kuwait and Saudi Arabia as compared to sub-Saharan Africa, where the rate is relatively low, possibly due to under reporting and low levels of surveillance (McGill, 2003).

Brucellosis in India: Correlation between Human and Animal Incidences

  1. Reddy et al. (2014) surveyed a total of 252 serum samples were collected from the goats of Karnataka and subjected to 5 different serological tests, i.e., Rose Bengal Plate Test (RBPT), Standard Tube Agglutination Test (STAT), 2-mercaptoethanol test (2-MET), Indirect ELISA (I-ELISA) and Dot-ELISA to detect the brucella antibodies and found the sero-prevalence in goats was 5.15% by RBPT, 6.34% by STAT, 1.98% by 2-MET, 9.52% by I-ELISA and 7.14% by Dot-ELISA.
  2. Suryawanshi et al. (2014) study the prevalence of brucellosis in sheep and goats, a total of 181 and 164 serum samples were collected from apparently healthy sheep and goats respectively of different age and sex from four districts of Maharashtra. All the samples were screened for brucella antibodies by employing RBPT test. An overall prevalence of 7.32% and17.68% was observed in goats and sheep respectively.
  3. Sadhu et al.(2015) surveyed Banaskatha district of north Gujarat and screened 1000 serum samples (485 from sheep and 515 from goats) using RBPT, STAT and I-ELISA. The overall sero-prevalence recorded was 11.30%, 11.10% and 8.80% by RBPT, STAT and I-ELISA respectively. The sero-prevalence of brucellosis was found to be higher in sheep than goats.
  4. Sharma et al. (2015) screened 160 serum samples from small ruminants (sheep-90 and goat- 70) to determine the sero-prevalence of brucellosis in and around Jammu, J&K, which were tested by RBPT, STAT and I-ELISA and recorded an overall sero-prevalence of 3.33%, 2.85% in sheep and goat respectively.
  5. Mangalgi et al. (2015) screened a total of 12,054 human serum samples in with history of fever, low backache, joint pain and arthritis using RBPT, STAT and 2-ME. The study was conducted between November 2008 and December 2013 in Karad, Maharashtra. Seroprevalence of brucellosis was found to be 1.75% (218) with RBPT. Significant SAT (>160) and 2-ME (>80) titres were seen in 212 and 198 individuals respectively.
  6. Sharma et al. (2016) screened 121 human serum samples collected from veterinarians, livestock handlers and PUO Patients to determine the seroprevalence of brucellosis in humans in different geographical locations of Jammu region which were tested by RBPT, STAT and I-ELISA and recorded overall seroprevalence was 4.96%.
  7. A study was conducted by Sharma et al. (2017a, b) to determine the prevalence of Brucellosis in goats in and around border areas of Jammu, J&K, India using different serological tests. A total of 350 serum samples from goats and 75 sera samples from human patients were tested by RBPT, STAT and I-ELISA. Overall seroprevalence of 1.14% and 1.33% was recorded in goats and human respectively. Higher prevalence rates in 6-9 yr age group in goats (1.42%, 2.85% and 8.57%) and 36-50 yr age groups in human male patients were obtained by RBPT, STAT and I-ELISA, respectively. Goats of unorganized sector observed higher prevalence compared to organized sector, whereas sex-wise the does had higher prevalence than bucks (Tables 1 – 5).

Table 1: Age-wise sero-prevalence of brucellosis in goats in and around border areas of Jammu, J&K

Age Group (yr) No. of Animals RBPT +ve (%) STAT +ve (%) I-ELISA +ve (%)
1-2 100 2 (2.0) 3 (3.0) 6 (6.0)
3-5 180 3 (1.66) 7 (3.88) 8 (4.44)
6-9 70 1 (1.42) 2 (2.85) 6 (8.57)

Table 2: Sex-wise sero-prevalence of brucellosis in goats in and around border areas of Jammu, J&K

Species (No. of Samples) Sex (No. of Samples) RBPT +ve (%) STAT +ve (%) I-ELISA +ve (%)
Goat

(350)

Male (150) 1 (0.66) 4 (2.66) 8 (5.33)
Female (200) 5 (2.50) 8 (4.0) 12 (6.0)

Table 3: Sero-prevalence of brucellosis in goats in different rearing system in and around border areas of Jammu, J&K

Sector (No. of Samples) RBPT +ve (%) STAT +ve (%) I-ELISA +ve (%)
Organized (60) 1 (1.66) 2 (3.33) 2 (3.33)
Unorganized (290) 5 (1.72) 10 (3.44) 18 (6.20)

Table 4: Age-wise sero-prevalence of brucellosis in humans in and around border areas of Jammu, J&K

Age Group No. of Persons RBPT +ve (%) STAT +ve (%) I-ELISA +ve (%)
20-35 20 0 (0.0) 0 (0.0) 0 (0.0)
36-50 30 1 (3.33) 0 (0.0) 3 (10.0)
51-65 25 1 (4.0) 1 (4.0) 1 (4.0)

Table 5: Sex-wise sero-prevalence of brucellosis in humans in and around border areas of Jammu, J&K

Sex (No. of samples) RBPT +ve (%) STAT +ve (%) I-ELISA +ve (%)
Male (60) 2 (3.33) 1 (1.66) 4 (6.66)
Female (15)

Diagnostic Approach

The most reliable diagnosis of brucellosis is bacteriological isolation and identification of Brucella spp. (Alton et al., 1975a, b, 1988, Cetinkaya et al., 1999). However, bacteriological examination is a time consuming and tedious process and puts the laboratory personnel under great risk to infection. Sometimes, attempts at isolation of Brucella even from known positive cases do not yield reliable results (Ray, 1979). Due to these problems, recourse to serological tests is taken. A number of serological tests are employed to detect antibodies against Brucellaorganism for diagnosing the disease, viz., Rose Bengal Plate Test (RBPT), Standard Tube Agglutination Test (STAT), Complement Fixation Test (CFT), Milk Ring Test (MRT), Enzyme Linked Immunosorbent Assay (ELISA) etc (Sharma et al., 2017a.b). RBPT test was proved useful as a herd screening test due to its high sensitivity (MacMillan, 1990), but can also give false negative results in certain circumstances. The STAT has been widely used serological test for brucellosis diagnosis in herds. However, there is often no complete agreement between the results of the STAT and other tests (MacMillan, 1990) and STAT titer may wane in chronic infections to negative levels (Dohoo et al., 1986).

The CFT, despite its high sensitivity and specificity (Alton et al., 1975a, b, 1988), cannot be adopted as a routine test due to its difficult technical procedures leading to considerable variations in performing the test (MacMillan, 1990). ELISA has been found to be of same or higher sensitivity and specificity than RBPT and CFT (Blasco et al., 1994), with an advantage of ease of performance and adaptation to automation. Because of varying sensitivities and/or specificities of individual tests, it has been advised to use a battery of serological tests for diagnosis of brucellosis (Sharma et al., 2017a.b).

Disease Prevention and Control

  1. Disease management strategies for brucellosis involve vaccination, testing and slaughter/segregation. For various reasons, test and slaughter policy is difficult to implement in India. B. abortus S-19 and B. melitensis Rev-1 vaccines are two most widely used immunoprophylactic biologicals in cattle and small ruminants, respectively.
  2. Once a policy of vaccination is adopted in an area, it will be necessary to develop procedures that can differentiate vaccination and infection status of animals. So far progress in this area of study is meager.
  3. Use of novel proteins as vaccine antigens have been investigated by many workers. Besides, accidental exposure to live vaccine strains can cause avoidable problems for animal handlers and professionals,
  4. Therefore, it is essential to develop diagnostic tests and vaccines based on the antigens, which will allow differentiation between vaccinated and infected animals and which would be safe for handlers. Outer membrane protein antigens of Brucella have shown some promise in this regard.
  5. The work clothes of animal attendants should be reserved for this purpose and retained on the premises. They should be disinfected after use either by heat treatment (boiling or steaming), by fumigation with formaldehyde or by soaking in a disinfectant solution of appropriate concentration (iodophor, phenolic soap, chloramine or hypochlorite). Particular attention should be given to the disinfection of footwear to ensure that infection is not transferred outside the premises or into the house or tent. Ideally, operatives should have access to full washing or showering facilities. As a minimum, the hands should be rinsed in a 1% chloramine solution (or other approved disinfectant), washed in soap and water and then treated with an emollient cream. Any superficial injuries such as cuts or scratches should be treated with an antiseptic, e.g. tincture of iodine, and covered with a bandage or self-adhesive dressing (Corbel, 2006).
  6. Farm sanitation can be achieved by disposal of aborted fetuses, placentae and contaminated litter in leak-proof containers by incineration. Deep burial in freshly slaked lime at sites away from water courses is an acceptable alternative. Any area in which an abortion or infected parturition has occurred should be washed down with an approved disinfectant (hypochlorite, iodophor or phenolic disinfectant at recommended working strength). Farm implements used for handling contaminated material should be disinfected after use by immersion in a suitable disinfectant (iodophor, phenolic soap or dilute caustic soda) (Corbel, 2006).

Conclusion

Brucellosis in India is very common but often a neglected disease (Renukaradhya et al., 2002). Brucellosis due to B. melitensis is widespread in India and major cause of abortion in small ruminants imposing economic loss due to an adverse effect on total animal protein supplies and severe hazard to human health (Abeer et al., 2003). Sheep brucellosis can be divided into classical brucellosis and ram epididymitis. Ram epididymitis is caused by non-zoonotic agent B. ovis, while classical brucellosis constitutes a major public health threat equal to goat brucellosis (Acha and Szyfres, 2003). There are about 500,000 new human cases of brucellosis reported annually worldwide making it most common zoonosis (Saleem et al., 2004, 2010).

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