Bovine campylobacteriosis is an infection caused by the bacteria of the genus Campylobacter. These organisms are connected with number of disease conditions in cattle, especially related to reducing fertility in breeding cows and heifers, and diarrhea in the young animals. Moreover, these pathogens  having  zoonotic  importance can cause diarrhea in humans, and are considered to be the primary cause of foodborne gastroenteritis in developed countries. These pathogens are connected with commonly occurring zoonoses in the European countries (EFSA and ECDC, 2018). The poultry is considered  to  be  the  main source  of  human  infection. However, Campylobacter is also highly prevalent in ruminant species throughout the world. Therefore, there is a growing concern of transmission of these pathogens from ruminant animals to humans. The cattle are the second most important reservoir animals next to the broilers for Campylobacter jejuni infection in humans, and sheep are the main source of Campylobacter coli infections in humans (Sheppard et al., 2008; Roux et al., 2013).

Bovine genital campylobacteriosis (BGC) is a venereal disease of cattle (OIE, 2021a) caused by Campylobacter fetus Subsp. venerealis and C. jejuni are the most important species associated with the abortion and decreased fertility in cattle causing reduce calf crop percentage, late calving, or abortions/stillbirth (Seid, 2019; Irons et al., 2020). This disease has been included in the list of notifiable diseases of the World Organization for Animal Health (OIE), and is significant for the international trade of animals or animal products (OIE, 2021a). This disease has impact on socio-economic and zoonotic implications. A number of countries have successfully eradicated this disease; however, in many countries in the world especially in low and middle income countries (LMICs), this disease is still endemic (McDermott et al., 2013). In fact, this disease is more prevalent in the territories where the natural breeding program is usually practiced in cattle compared to the developed countries (More et al., 2017). However, the economic burden of this disease may vary due to affected animal type and husbandry pattern including the capacity of the national animal health services in different geographical locations (Mshelia et al., 2010). The loss related with the disease is directed to the elimination of non-productive animals by culling to enhance the profitability of a dairy farm (Seid, 2019). However, due to resource constraints, the control programs could not even be implemented in the low resource settings.

Because of limited active surveillance in Bangladesh, the actual burden of bovine campylobacteriosis is still unknown. However, the country is routinely notifying on the presence of BGC in cattle as per standards set by the OIE (2021b). A cross-sectional survey was conducted between July-December, 2020 in two districts (Dhaka and Mymensingh) of Bangladesh with an aim to estimate the prevalence, isolation, identification, and further characterization of Campylobacter spp. in farmed cattle. The study established an overall prevalence of Campylobacter spp. in dairy cattle 30.9% (Hoque et al., 2021). Above 15% of cattle of the national herd are crossbred high yielding stock in Bangladesh (Hamid et al., 2017), however, 100% crossbred cattle are being reared in the urban settings of Dhaka city corporation (DCC) area due to higher demand for cow’s milk and meat (DLS, 2020b). 

Since the indigenous cattle breed is less productive and unable to fulfill the country’s demand of milk and meat, to mitigate such nascent demand, artificial insemination  (AI)   using   exotic   breed   (predominantly Holstein Friesian) targeted to enhance productivity of indigenous cattle has been adopted since the last decades (NDDP, 2016). For this reason, the number of crossbred animal populations is increasing steadily in Bangladesh, and ensures reorganization to the high density of cattle population as 145 large ruminants in km² area (WB, 2018). This change enhances the likelihood of the emergence of cattle adapted Campylobacter species like C. jejuni strains (Mourkas et al., 2020). The economic burden of Campylobacter spp. is mostly associated with livestock production losses in female cattle, viz. milk production (Akhtar et al., 1993), abortion (Silveira et al., 2018), infertility/decreased pregnancy (Silveira et al., 2018; Michi et al., 2016) along with other pertinent losses like the cost for veterinary health care facilities, cleaning and disinfection cost, and restocking cost (Seid, 2019). Infection is usually not measured until a reduced calving rate is noticed in a herd, while financial losses will be incurred over time (van Bergen et al., 2005). Bulls infected with C. fetus Sub.sp. venerealis do not associate  with any clinical manifestations, deteriorate semen quality or even breeding capability (Seid, 2019; Clark, 1971; Skirrow, 1994), or gross genital anomalies (Bier et al., 1977). This disease is transmitted mostly by natural service; however, infection may also be transmitted by the semen of infected bulls during artificial insemination (AI) or by contaminated equipment (Modolo et al., 2000). Assessment of these losses is essential for the countries where a large number of livestock are kept (Azami and Zinsstag, 2018).

As a part of prevention and control activities, routine screening in breeding bulls of artificial insemination (AI) has been implemented at a limited scale. However, inadequate testing facilities have underestimated the true burden of bovine campylobacteriosis in low resource settings like Bangladesh (Michi et al., 2016).  Bangladesh has 24.2 million cattle, 1.5 million buffaloes, and 26.0 million goats. The contribution of livestock to the national economy was estimated as 1.43% for the year 2019-2020 and it is increasing at 3.04% annually. The country has fulfilled the demand of meat recently, and efforts are underway to optimize milk production (DLS, 2020b).  So, the impact of the disease would also affect the suitability of meat production and food security.

Several studies have been conducted in different geographical locations of the world which have marginally estimated economic losses of bovine campylobacteriosis (Silveira et al., 2018; Jimenez et al., 2011; Hum et al., 1994), however, such study is yet to be conducted in Bangladesh. This is the first report to estimate the economic impact of Campylobacter in farmed cattle of Bangladesh. The objective of this study was to estimate economic losses incurred due to this disease in two study districts (Dhaka and Mymensingh) as promising cattle rearing areas. The finding of this study will help in formulating a strategic document towards taking prevention and control initiatives on bovine Campylobacter in farmed cattle as a proof-based decision-making option.

Ethical approval and informed consents

The research was approved by the Animal Welfare and Experimentation Ethical Committee (AWEEC) of Bangladesh Agricultural University (AWEEC/BAU/2019/45). The participants were adequately informed on the study. A verbal consent was obtained during field observation data collection as some of the participants could not read and write.

Study area and population

The study was carried out in two districts: Dhaka (23° 47′ 24″ N, 90° 18′ 0″ E), and Mymensingh (24° 38′ 3″ N, 90° 16′ 4″ E) of Bangladesh (Figure 1). Dhaka district is located in Dhaka division in the central part of the country, whereas, Mymenisngh district is located in Mymensingh division in the northern part of the country. These two districts are considered as part of the favorable cattle rearing zone of Bangladesh with more than 1 million heads of cattle (DLS, 2020a), of which approximately 15% are crossbred (Hamid et al., 2017). These crossbred cattle population was used as a study population for this economic loss assessment model.

Data used for economic loss assessment

The economic loss analysis used the data of different parameters collected  from  different  sources,  that  is,  primary  and  secondary (Figure 2). The list of questions and its corresponding data requirement for estimation of economic loss of Campylobacter in farmed cattle of selected districts (Dhaka and Mymensingh) of Bangladesh conducted between July - December 2020 were utilizedinitially in the process of data collection.

Secondary data

The study utilized the secondary data from multiple sources, viz: secondary data/published data from the peer review journal articles (n=8) and government document/unpublished data (n=2) from the government offices (Table 1).

Primary data

A field survey (face-to-face interview) was conducted with different stakeholders (farmers/ cattle handlers/farm manger) (n=75) from study districts (Table 2). A pre-tested semi-structured questionnaire was utilized for the field survey to gather data on body weight (cow and heifer), milk production/cow/day, price of a calf, a cow, price of milk/liter, price of beef/kg, treatment cost of a suspected Campylobacter infected animal (infertility/abortion/repeat breeding), restocking cost if required, where infertility, repeat breeding, or abortion in cow/heifers are present.

In this study, we calculated the losses relating to Campylobacter in farmed crossbred cattle for the study districts (Dhaka and Mymensingh) during July - December 2020. The study did not cover the indigenous cattle (Zebu) as these are reared mostly in the households. Fifteen percent (15%) crossbred animal displayed in the national herd (Hamid et al., 2017) was used for estimation numbers of crossbred cattle in two studied districts. However, 100% crossbred cattle being reared in the Dhaka city corporation area (DLS, 2020a) was taken under this study. In summary, 51,402 heads of crossbred cattle in Dhaka district, and 138,540 heads of crossbred cattle in Mymensingh district were confirmed (Table 3). The proportion of different categories of cattle, viz; milking cows, pregnant cows/ heifers was confirmed from a previous study (Islam et al., 2020) (Table 1). The data on prevalence rate of Campylobacter spp. with its probability distribution of an earlier research (Hoque et al., 2021) was generalized in the estimated whole crossbred cattle population of two districts. Thus, a total number of infected animals was obtained (Table 4). The losses reported in published articles in production  parameters  were  used in the estimated infected animals of two study districts (Table 1). Finally, losses in livestock goods and the relevant costs were then converted into monetary figures (BDT: Bangladesh Taka) considering the market price for a single year.

Dprg: the cost for decreased pregnancy, [Dpg= Number of positive mature cows/heifers (Dhaka: 7,942, Mymensingh: 21,391)   x 50% non-pregnant cows/heifers x 20% infertility x cost for 1 month old calf (BDT 30,000)].

Ab: Cost for abortion in dairy cows, [Ab= Number of positive cows/heifers (Dhaka: 7,942, Mymensingh: 21,391)   x 50% pregnant cows/ heifers x 20% gestation loss x cost for 1 month old calf (BDT 30,000)].

Oth: other costs, [Oth= applicable cost for veterinary health care in infected animals + cleaning/sanitation cost + restocking cost after adjustment with the carcass value (if needed)]. here, cost for veterinary health care = BDT 500/animal × 40% infected animal (total infected cows/heifers-Dhaka:7,942, Mymensingh:21,391) (20% decrease pregnancy + 20% abortion);  Cleaning and sanitation cost: BDT 200/animal × 20% abortion  (total infected cows/heifers-Dhaka: 7,942, Mymensingh: 21,391);  Restocking cost = 40% (20%  abortion and 20% infertility) cases (buying value of a new cow/heifer BDT 180,000 - carcass value of the present stock, 200 kg meat x BDT 600 =120,000)= BDT 60,000.

Data management and statistical analysis

Data collected via stakeholder interview from farms (n=75), include weight of a mature cow/heifer (≥ 3  years,  average  milk  production  (liter/cow/day), price of an one-month-old cow/bull calf, price of a mature cow/heifer (≥3 years), price of a 1 L of milk, treatment cost of a Campylobacter infected cattle, restocking cost of a cow/heifer with infertility or abortion produced in the probability distribution functions (most likely, lowest value, highest value) using ModelRisk (VOSE, 2019) and presented in Table 4. The data were obtained and recorded in a Microsoft Excel® worksheet. Proportion, percentage, and 95% confidence interval (CI) were calculated using an Excel data analysis tool pack for estimating the financial impact of different parameters (decreased milk production, infertility/ decreased pregnancy, abortion in dairy cows and other pertinent costs).

Number of Campylobacter infected animals

Connected to the total number of crossbred farmed cattle, the number of mature cows/heifers (≥3 years old) were calculated as 94,926 (50% of total crossbred cattle population) of which 29,332 (95% CI: 25,630-33,324) cows  and  heifers  were  predicted  to   be   positive  with Campylobacter spp. (Table 5). The list of the variable inputs captured through field interview data collection includes prices of live animals and livestock products used in economic loss estimation is shown in Table 4.

Decreased milk production

An amount of BDT 395.25 million (95% CI: 345.36-446.34) was estimated to be financial loss due to decreased milk production in two study districts. However, among the two districts, Mymensingh emerged as the top position with a financial loss of BDT 288.25 million (Table 6).

Decreased pregnancy and abortion in dairy cows

These two parameters were measured as an equal economic loss (BDT 87.99 million in each parameter) in two studied districts. However, Mymensingh district was captured with higher economic loss (BDT 64.17 million in each parameter) than Dhaka district (BDT 23.82 million in each parameter) (Table 6).

Other relevant costs

In this category, the restocking cost was captured as the highest loss parameter (BDT 703.89 million, 95% CI: 615.12-794.98) in two study districts. Considering the number of  cattle population, Mymensigh district was weighed with the greater economic burden (BDT 513.38 million) than Dhaka district (BDT 190.61 million). Other parameters like veterinary health care (BDT 5.87 million) and cleaning disinfection cost (BDT 1.18 million) were evaluated as substantial loss parameters under the other relevant costs category.

The annual economic loss due to decreased milk production, infertility as a result of decreased pregnancy, abortion in dairy cows with other relevant costs (veterinary health care, cleaning and, disinfection and restocking cost (if applicable) is presented in Table 6. The total financial loss from  this  disease  was  assessed as BDT 1282.3 million (95% CI: 1120.4-1448.0 million) (Equiv. USD 14.1 million, 95% CI: 13.2-17.0 million) in farmed crossbred cattle of two study districts.

The pivotal economic loss was estimated in other cost categories (BDT 711.03 million, 95% CI: 621.27 -802.92 million), of which restocking cost is the key contributor in this category (BDT 703.9 million, 95% CI: 615.1-794.9 million) followed by decreased milk production, and abortion in dairy cows or infertility respectively (Figure 3). However, decreased milk production was established to be the second position with an annual financial loss of BDT 395.3 million (95% CI: 345.4- 446.3 million) followed by infertility due to decreased pregnancy or abortion in dairy cows (Table 6 and Figure 3). The financial impact of Campylobacter in farmed cattle was found to be higher in each loss parameter at Mymensingh than Dhaka district (Figure 4).

The study has investigated highest Campylobacter loss associated with restocking cost for farming cattle followed by decrease milk production, abortion/infertility in dairy heifers/cows. This finding is apparently coherent with another research was conducted in Argentina as the disease accounts for a 10% decrease in the calving rate in the infected herds with an annual financial loss of USD 165 million (Jimenez et al., 2011). Another study in the United States confirmed the cost of abortion in dairy cattle that was evaluated yearly at around USD 555 per animal (De Vries, 2006), and a theoretical lessening of 20% for abortion in a farm composed of 1,000 pregnant cows that measured an  economic  loss  of  USD 111,000 (Silveira et al., 2018). A few studies have confirmed the distribution of repeat breeding of around 11% (Asaduzzaman et al., 2016; Hasib et al., 2020), and abortion of < 10% in crossbred cows (Parvez et al., 2020; Alam et al., 2014) in different locations of Bangladesh. These reproductive problems are associated with substantial economic cost due to treatment (veterinary health care facilities) and replacement of the diseased animals that have had a direct impact to the livelihoods of marginal dairy farmers in Bangladesh (Talukder et al., 2005). The restocking cost was found as a paramount financial loss as farmers’ attempt to overcome the productivity  loss  related  to infertility as a result of repeat breeding or abortion by selling their current stocks and purchasing of new reproductive animals.

According   to   the  Department  of  Livestock  Services (DLS), Bangladesh, the country’s total milk production was 9.40 million metric tonnes in 2018 against 15.02 million  metric  tonnes  that has demonstrated that 63% of demand was satisfied through its own production (DLS, 2018). However, in the same year, Bangladesh imported 0.11 million tonnes of powdered milk to lessen the production gap (BBS, 2018). Bangladesh is now self-reliant in meat production after various measures were taken by the government to boost the country’s livestock sector (BBS, 2018). The impact of bovine campylobacteriosis will reduce milk production directly and indirectly, will widen the gap between demand and supply of animal origin food, and ensure further dependency on imported powdered milk. It is imperative to recognize this in the dairy industry of Bangladesh for mitigating this shortfall that has a positive impact on income of the marginalized dairy farmers. Nevertheless, the diseases, like bovine campylobacteriosis, may impede this possibility via decreased production including their zoonotic transmission.

Bovine campylobacteriosis are not the diseases that get more attention in LMICs like many other economically important infectious diseases such as foot and mouth disease (FMD) and peste des pettits ruminants (PPR); however, the burden of bovine campylobacteriosis has not yet been appraised in most countries. The key stakeholders are not conscious of the actual burden of this disease in cattle including its significant public health implications. Highlighting key dairy health impacts through production loss, risk of zoonotic transmission, international trade embargo, and animal welfare issues should be important to assist the researchers and planners in considering the priority options (Wells et al., 1998). Undoubtedly, the most important change to the natural host position of C. jejuni has taken place in recent times resulting in cattle-specific pathogen found to have originated through intensive livestock farming (Thépault et al., 2017; Sheppard et al., 2013; Morley et al., 2015).

Bovine campylobacteriosis, notably C. jejuni has been recognized for decades, as they are estimated to be the primary reproductive diseases of cattle. To improve livestock production in terms of keeping sustainable economic output, a collective action between cattle farmers, government bodies, dairy industry, and academia needs to focus on further exploration of this disease in the area of diagnosis, treatment, prevention and control measurements (Michi et al., 2016). The highest prevalence of BCG has been confirmed in the LMICs where natural breeding program in cattle is mostly practiced (Mshelia et al., 2010).

To lessen the above financial burden of bovine campylobacteriosis, it is commendable to bring about all farmed female reproductive cattle under artificial insemination (AI) program to prevent venereal transmission of Campylobacter. However, breeding bulls under the AI program should be periodically tested on presence of Campylobacter through government support and culling of the positive animal to be ensured (Seid, 2019; Bondurant, 2005; Truyers et al., 2014; Cobo et al., 2004) along with vaccination of all bulls, cows, and heifers (Seid, 2019) is  also  needed.  However,  breeding bulls carrying Campylobacter can be treated using frequent antimicrobial preputial washes and may need additional injectable antimicrobials (Revell, 1998; Taylor, 2002) where scarcity of resources is an advent. Regular screening and segregation of infected animal from the herd is needed at primary stage, and test and culling would be implemented in the final stage after adjustment of adequate financing under farmers’ compensation scheme.

Good farm management is the prerequisite for fecal transmission of C. coli and C. jejuni that includes good cleanliness and hygienic practices in cattle farms, along with proper slurry management through composting or biogas plants (Hoque et al., 2021). Good practice of composting will reduce Campylobacter (and other important zoonotic pathogens such as Salmonella and Escherichia coli) within 5 days due to the high-temperature generation (>50°C) (Hutchison et al., 2005) would be beneficial to reduce the load of Campylobacter in the farm environment and to minimize the reinfection in cattle. 

The study has few limitations as it did not cover indirect losses incurred by bovine campylobacteriosis, including all categories of animals at the farm level; also, this study focused only on two districts of Bangladesh that failed to capture the actual burden. The model that has been established in this study is comparatively simple, including all potential direct losses associated with the reproduction of crossbred farming cattle for the first time in Bangladesh. Additionally, the outputs of this study could be utilized for other cattle-dominant districts of Bangladesh. Therefore, a future greater survey including all direct and indirect losses of Campylobacter considering animal situation (behavior, physical conditions, etc.) during the follow-up of the illness is intended and recommended.

The study confirms a variety of financial losses on livestock productivity related to bovine campylobacteriosis infection in crossbred farmed cattle based on the animal level prevalence and recommends an urgent need for resorting to control approaches that is fit-for-purpose in low resource settings in supporting and sustaining the livelihoods and food security for marginal dairy farmers.

The authors have not declared any conflict of interests.

The authors are grateful to dairy farmers/farm attendants, animal    traders/broker,   veterinarians/paraprofessionals for their assistance during field survey data collection. The authors are indebted to Mr. Syful Islam, Scientific Officer, Agricultural Economics Division, Bangladesh Institute of Nuclear Agriculture (BINA), Mymensingh, Bangladesh for reviewing the manuscript. The study was funded by Krishi Gobeshona Foundation (KGF Project ID: TF-45-L/17), Bangladesh.