Economic impact of caprine and ovine brucellosis in Mymensingh district, Bangladesh

Background Brucellosis is one of the ancient re-emerging zoonotic diseases which play a significant economic impact on public health and livestock sector. Many studies were carried out on the epidemiology of the disease recently but economic importance was not focused on those studies. This study was conducted to determine the true prevalence and economic impact of caprine and ovine brucellosis in Mymensingh district, Bangladesh. Methods A cross-sectional epidemiologic study covering all upazilas of Mymensingh district, Bangladesh was conducted during the period from January to December, 2016. The data related to age, sex, abortion record and reproduction disorders were also collected on the sampling day using a questionnaire. Blood samples (n=2593) were collected from randomly selected native goat and sheep where Rose Bengal Test, Rapid Brucella AB test kit and MAb-ELISA (Monoclonal antibody based blocking Enzyme-Linked Immunosorbent Assay) were used to identify the positive reactors. brucellosis was estimated to be 1.6% whereas it was found to be 1.56% and 1.64 % in goats and sheep respectively. The prevalence data was incorporated to the economic model to quantify the financial loss due to brucellosis. The total losses attributed to the disease was 48436400 taka (605455 US$) annually in the district whereas 46462900 taka (580786.25 US$) and 1973500 taka (24668.75 US$) in goat and sheep respectively. The study concluded that brucellosis silently constitutes economic loss to the economy of the country and the producers due to insufficient knowledge and inadequate diagnostic facilities, lack of awareness and an effective prevention and control strategy.


Introduction
Brucellosis is enlisted as the second leading zoonotic infection followed by rabies by the Office International des Epizooties and classifies risk group III in laboratory biosafety manual of the World Health Organization. This disease is considered to be an occupational disease that mainly affects slaughter-house workers, butchers, livestock producers, shepherds, farmers, veterinarians, and laboratory technicians (Behzadi and Mogheiseh, 2011;Rahman et al., 2012).
Brucellosis causes severe economic losses as result of stormy abortions in small ruminants or reproductive failure, sterility and reduced milk production rates as well as lost trade by denying exportation of sheep to international markets and reduces the Foreign Exchange Earnings (FEE). As a result the disease adds to the burden shouldered by the farmers in developing world (McDermott, 2013; Angara and Ali, 2014). Female goats were considered to be potential source of infections and infected excreted materials are the causes of transmission through contacts following abortion or full-term parturition. Mammary gland may also infected in sheep and goats resulting mastitis, characterized by multinodular firmness with watery, clotted milk commonly observed feature of caprine brucellosis compared with bovine brucellosis (Cutler et al., 2005). Goats may responsible for prolong excretion of organisms in milk but less in sheep (Poester et al., 2013). It has been reported that intermittent shedding usually observed when infected goats survive as persistent reservoir after one abortion or parturition (ECSCAHAW, 2001). Brucella ovis is also an important cause of orchitis and epididymitis in sheep but it is not recognized as a cause of natural infection in goats (Jacques, 1998). Disease transmission chance potentially increases when keeping sheep in contact with goats or get together in parturition or at night as ovine animal's behavior and it is also a risk factor for brucellosis (Coelhoa et al., 2013). In relation to age and sex, adults were more positive than young and female were more susceptible than male (3.8%) (Gani et al., 2016). In field, a lot of undiagnosed abortion, stillbirth and retained placenta cases are observed due to inadequate diagnostic facilities and thought to be down to brucellosis which could have a significant impact on the development of livestock in Bangladesh (Rahman et al., 2011b).Important factors that contribute to the spread of brucellosis in goat and sheep are existing farming system and practices, farm sanitation, livestock movement, mixing and trading of animals, and sharing of grazing grounds and watering points (Kabagambe et al., 2001;Kadohira, 1997;Omer, 2000 (BBS, 1986). During the last 12 years, sheep population increased 2.5 times, with annual growth rate of 5% (BBS, 2008). Considering the socioeconomic and climatic condition of Bangladesh, rearing of Black Bengal goat is more suitable than other breeds and recognized as best goat breed including fourth largest goat repository in the world (Report KIB, 2018). Each year 127,000 metric ton representing 25% of total red meat in Bangladesh is produced from goat. Mutton export has been started from 2013-14 (Annual report 2016-2017, DLS).
In this circumstance, brucellosis may be able to impair the growing economic market. Food and Agriculture Organization of the United Nations (FAO) and the Organization of Animal Health (OIE) considered brucellosis as a barrier to trade of animals and animal products as well as public health implications (WHO, 1997;Fitcht, 2003).
This study was conducted to determine the prevalence and economic impact of caprine and ovine brucellosis in Mymensingh district, Bangladesh.

Material and Methods Ethical Approval
All essential procedures of sample collections were performed maintaining the human consent and animal welfare.

The Study Area
Mymensingh is 5 th largest districts of Bangladesh situated in the north. It is also the largest district of Dhaka division. The Geo position of Mymensingh district is between 24˚02'31'' to 25˚25'56'' North latitudes and between 89˚39' to 91˚15'35' east longitude. The total population is 51,10,272 and population density is 1163/Sq. Km. Currently, Mymensingh district has thirteen upazilas (sub district) containing approximately 2700 Villages where total goat and sheep population is estimated to be 775,249 and 25,591 respectively (Annual report 2016-17, District Livestock Office, Mymensingh, DLS).

Study design and sample size estimation
A cross-sectional study was conducted covering all upazilas of Mymensingh district, Bangladesh during the period from January to December, 2016. Random blood samples were collected from native breeds of female goat and sheep (above one year) and transferred to the Laboratory of Veterinary Medicine, Bangladesh Agricultural University, Mymensingh for serum separation and serological tests. About 5 ml blood was collected from jugular vein of each of the selected goat (n=1847) and sheep (n=746) in separate sterilized test tubes and kept in refrigerator overnight. Then the serum was centrifuged at 2500 rpm for 8-10 min to obtain clear sera free from blood cells. Finally, sera were transferred into a sterilized eppendorf tube and stored at −20°C until used.

Serological tests
Rose Bengal test (RBT) as described by Alton et al. (1988) and Rapid Brucella AB test kit (chromatographic Immunoassay) were performed as per manufacturer instruction to determine the presence of antibodies against Brucella antigens. RBT positive sera were screened by MAb-ELISA (MAb based blocking Enzyme-Linked Immunosorbent Assay, Bru Alert®, TRPVB, CAHS, Tamil Nadu Veterinary and Animal Science University, Chennai) according to the protocol and reading was performed by automated ELISA reader.

Interpretation
All degree of agglutination was considered as positive reaction. In case of brucella AB test kit the presence of two purple color bands within the result window means positive. The prevalence of brucellosis in each Upazila was used for estimating the weighted average of brucellosis in the District (Angara et al., 2016).

Sources of data
Data were collected from both secondary and primary sources. The secondary data were obtained from different sources such as Department of Livestock services Under the Ministry of Fisheries and Livestock (2016-17), record from own upazila veterinary hospital, relevant studies, text books and web sites. The primary data were collected by conducting an epidemiological and economic survey during the period from January to December 2016. A questionnaire was used to collect the economic data and the health status, age, sex and history of abortion and different reproductive disorder for each goat (n=112) and sheep (n=67) from randomly selected herds (goat=370, sheep=141) containing 3-5 or more small ruminants throughout the district.

The economic model
The simple model was used to estimate the total economic losses in the district is given bellow: TEL = MT+MD ……(1) (Angara et al., 2016). Where as TEL=Total Economic Loss, MT (Economic Loss due to mortality) = Number of goats and sheep died due to dystocia/abortion followed by metritis × average price of mature animal……………(2) MD = Economic Loss due to morbidity, MD = BL+CL+LRB+CVI+OC………… (3) Where as BL (value of body weight loss) = (Number of seropositive animals × cost of body weight loss per animal CL (value of calves lost) = (Number of mature female × prevalence rate of seropositive aborted animals) × average price of weaning kid……………(4) LRB (Losses due to repeat breeding) = Number of seropositive repeat breeders × cost of repeat breeding per animal …………………(5) CVI (Cost of veterinary intervention) = Number of seropositive aborted animals(include retained placenta+ mastitis + metritis + dystocia) × cost of Veterinary intervention per animal……….(6) OC (value of opportunity cost) = It is applicable for the surviving infected goats and sheep which included (i) Cost on higher feeding and rearing inputs for weight loss (ii) Decreased milk production which leads to malnutrition of kids and loss in longer rearing-time due to late maturity of young stock, anestrous iii) Cost on permanent infertility or disability (iv)Loss in extra service due to repeat breeding, kidding interval (v) Increased cost on management for transport to veterinary hospital for treatment. These costs were difficult to quantify properly due to absence of suitable data and records. Including other records lacking mentioned above especially estimates on cost of feeding and rearing, were assumed approximately as 15 percent of the total cost of animal, i.e. Taka 1200 per infected surviving animal, i.e. Oc = (Total infected animalstotal mortality) × 15% of total cost of animal (Singh et al., 2008) ……(7) Annual losses per head= Total Economic losses / number of goats and sheep population….. (8) Annual losses per mature female = Total Economic losses / number of mature female goats and sheep………… (9) Annual losses per seropositive female = Total Economic losses / number of seropositive female.
The parameters used to estimate the economic loss in the model Most of the necessary data and parameters were obtained from the field survey. Other necessary parameters were estimated from the secondary information or some probable values adapted according to current situation.
In this study, the economic data, information about the effect of the disease on productivity parameters and epidemiological parameters were acquired from the field survey. The secondary information of reproductive and productive parameters were obtained from the Livestock Census

Result
The prevalence of caprine and ovine brucellosis in the upazilas of Mymensingh district: The prevalence rate of caprine and ovine brucellosis was estimated to be 1.6% whereas it was found to be 1.56% and 1.65 % in goats and sheep respectively.
The highest prevalence were observed in Muktagachha 3.16% followed by Mymensingh sardar 2.31% in goat and 3.77 % in Mymensingh sadar followed by 3.33% in Nandail in Sheep respectively ( Table 1).

Number of animal losses including economic losses
The number of aborted goat and sheep were estimated at 5891 and 177 where 344 (.09%) and 33 (0.27%) were died respectively as a result of complication of abortion followed by endometritis. The economic loss was estimated at 2752000 taka in goat and 264000 taka in sheep according to equation (2).

Body Weight Loss
The number of seropositive goats were estimated to be { (6918 ×Pb) ×Pk} = 8301600 taka and for 306 sheep = 367200 taka according to equation (3)

Number of kids lost
Kid lost due to brucellosis as a result of abortion in goats and sheep are estimated at yearly 11782 and 354 where the cost was 17673000 taka in goats and 531000 taka in sheep according to equation (4).

Number of repeat breeders and economic loss
Repeat breeding as a result of brucellosis was computed to be 1640 goats and 108 sheep and the cost was 2706000 taka and 178200 taka respectively according to equation (5).

Veterinary intervention
Veterinary intervention was applied in this study in term of diagnosis and treatment. Here the aborted goats and sheep followed by retained placenta and endometritis were estimated to be 4743 goats and 163 sheep and the cost was calculated at 5928750 taka and 2503200 taka respectively. In case of mastitis 441 goats and 37 sheep were computed where 1212750 taka and 101750 taka were estimated respectively as economic loss according to equation (6).

Opportunity cost
The opportunity cost was computed to be 7888800 taka in goats and 327600 taka in sheep according to equation (7).

Calculation of total annual economic losses attributable to the disease in goats and sheep
Total loss attributed to the disease was 46462900 Tk in goat and 1973500 Tk in sheep according to equation (1).

Discussion
In the present study, a large number of small ruminants serum samples were collected randomly using cross-sectional survey from 13 upazila of Mymensingh district and screened with Rose Bengal Test (RBT), Brucella AB kit test and MAb based blocking Enzyme-Linked Immunosorbent Assay (MAb-ELISA). Rose Bengal reagent is highly recommended because of its simplicity and very low cost. In small ruminants, it is highly specific (100%, Diaz,  in the absence of vaccination. The prevalence of caprine and ovine brucellosis was estimated to be 1.6% whereas it was found to be 1.56% and 1.64 % in goats and sheep respectively. The highest prevalence was observed in Muktagachha 3.16% followed by Mymensingh sadar 2.31% in goat and 3.77 % in Mymensingh sadar followed by 3.33% in Nandail in Sheep (Table:1 Table 2).
Brucellosis is not fatal in animals but mostly affects fertility. Deaths are rare except in the fetus (Saxena et al, 2018) and death usually occur in adults due to complication of abortion followed by secondary infections. The mortality rate of the disease was very low in this study and it was 0.0007% of total economic losses and 0.09% and 0.27% of goat and sheep were died respectively in this study. In morbidity rate, the highest economic loss was attributed to kid loss which was computed 17673000 (17.673 million) taka (38.6%) in goat and 531000 (.531million) taka (26.90%) in sheep annually in Mymensingh district.
The economic impact of brucellosis varies from country to country and from region to region. In this study, the total losses attributed to the disease was 48436400 (48.4364 million) taka annually whereas 46462900 (46.4629 million) taka and 1973500 (1.9735 million) taka in goat and sheep respectively in Mymensingh district and was far less that reported at Uttar Pradesh, India which was estimated to the tune of Rs. 44.02 crore due to brucellosis in small ruminants (Rs. 4.97 crore in sheep and 39.05 crore in goats) in the annual economic loss (Sinha et al., 2016). This might be happened due to the difference of area and population as known Uttar Pradesh is much bigger in area and population than the district of Mymensingh. The cost of annual losses per head of goat US $ 0 .74 and sheep US $ 0.96 in this study i.e., below 1US$ were almost similar to US $ 0.7 per sheep and US $ 0.5 per goat reported in India (Singh et al., 2015).

Conclusions
The study concluded that brucellosis silently constitutes economic loss to the economy of the country and the producers, due to insufficient knowledge and inadequate diagnostic facilities, lack of awareness and an effective prevention control strategy. Serological test might be a means for identification of brucellosis across the country and measures could have taken to establish a program for control and prevention through proper diagnosis, culling of infected animal from flock by slaughtering or initiate vaccination.