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Iranian Journal of Veterinary Research logoLink to Iranian Journal of Veterinary Research
. 2022;23(3):189–195. doi: 10.22099/IJVR.2022.42574.6184

Seroprevalence to common infectious abortifacient and infertility causing agents in the dairy herds of India

T Naveena 1, L N Sarangi 2, S K Rana 3,*, A Prasad 4, T S Prabha 5, D Jhansi 6, N M Ponnanna 2, G K Sharma 7
PMCID: PMC9681985  PMID: 36425611

Abstract

Background:

Information on the prevalence of infectious agents in dairy farms forms the basis for formulating a suitable control strategy; especially in endemic situations.

Aims:

A cross-sectional study was undertaken to determine the prevalence of six economically important bovine diseases, causing reproductive disorders including bovine abortion in organized dairy herds in India.

Methods:

A total of 1,075 animals (cattle and buffaloes) from 09 dairy farms were screened by ELISA tests.

Results:

Bovine viral diarrhoea (BVD) was the most prevalent (56.5%) disease followed by infectious bovine rhinotracheitis (IBR) (45.4%). Prevalence of Q-fever (5.4%) and neosporosis (6.1%) were less on the farms. Although 16.3% of the samples turned positive for brucellosis, the contribution of calf-hood vaccination (B. abortus S19 vaccine) to the prevalence of antibodies cannot be ruled out. The overall prevalence of bovine anaplasmosis, known to cause sporadic abortions in dairy herds, was 34.1% in the 9 farms with a prevalence of less than 20% in 5 farms. Infection of multiple abortifacient (seroprevalence to more than two pathogens) was recorded in 56.8% of animals. A very strong association was observed between BVD and brucellosis (Odds ratio 14.2; P<0.001). Further, a positive association was also seen between seroprevalence of IBR and anaplasmosis, and neosporosis and Q fever (P<0.05).

Conclusion:

Viral diseases were found to be more common in the dairy herds than bacterial and protozoan diseases. Increased susceptibility of IBR seropositive cows to other bacterial and viral infections was observed.

Key Words: Abortion, Bovine viral diarrhoea, Brucellosis, Infectious bovine rhinotracheitis, Neosporosis

Introduction

Infectious bovine abortions and infertility are serious economic concerns of dairy farms. Production loss, increased breeding interval, decreased output to nutritional inputs, and increase in treatment and maintenance costs associated with abortions, and infertility impact dairy farm economics (Njiro et al., 2011 ▶; Sahlu, 2015 ▶). The estimated cost of abortions in the USA averages between $ 500-$ 900, approximately $ 165 in Argentina, and around $ 89 per animal in India (Campero et al., 2003 ▶; De Vries, 2006 ▶; Deka et al., 2018 ▶).

Bovine diseases, including infectious bovine rhinotracheitis (IBR) caused by bovine alphaherpesvirus-1 (BoHV-1), bovine viral diarrhoea (BVD) by the BVD virus (BVDV), bovine brucellosis by Brucella spp., Q fever (coxiellosis) by Coxiella spp., leptospirosis, listeriosis, and neosporosis by Leptospira, Listeria and Neospora canninum, respectively constitute the major causes of infectious abortions and infertilities in dairy herds (Anderson, 2007 ▶; Barkallah et al., 2014 ▶; Dubey et al., 2015 ▶; Derdour et al., 2017 ▶; Noaman and Nabinejad, 2020 ▶; Gelalcha et al., 2021 ▶; Sarangi et al., 2021 ▶). Bovine anaplasmosis, one of the most prevalent tick-borne disease of the tropics and sub-tropics, is also known to cause sporadic abortions in dairy herds (Aubry and Geale, 2011 ▶).

While a number of studies have dwelled on the epidemiology, prevalence, and impact of each of the diseases (Shome et al., 2019 ▶; Sarangi et al., 2021 ▶), reports are scarce on the association of multiple diseases in a herd. It has been reported that infection with one agent makes the animal susceptible or resistant to other infectious agents by modulating the host immune response (Candela et al., 2009 ▶). In tropics and sub-tropics such as India where most of the infectious diseases are endemic, the association of the diseases may significantly impact infertility and abortion in dairy herds. This study estimates the burden of major infectious agents known to cause abortion and infertility in some of the large to medium dairy farms located in various parts of India, and attempts to determine the likelihood of association between the pathogens.

Materials and Methods

Ethical considerations

In this study, serum samples submitted as part of routine brucellosis screening program and stored in the repository of NDDB R&D laboratory, Hyderabad were used. These serum samples were collected by the organized herds as per the standard protocol. The present study does not come under the category of experimental research on animals; therefore, formal ethical approval is not required.

Study design

A cross-sectional serosurvey was conducted on 09 intensive dairy farms located in different parts of India. The demographic detail of the farms is provided in Table 1. The dairy farms practiced modern farming procedures such as barn feeding, machine milking, artificial insemination, authorized entry, and exit procedures. Serum samples from the respective dairy herds were collected from June 2019 to December 2019 and submitted to the laboratory for the routine screening of bovine brucellosis. After the screening tests, the left-over serum samples were maintained in the laboratory at -20°C. For the current study, each farm was considered as an epidemiological unit and the sample size for a farm was determined with the expected prevalence of disease set at 50%, precision-5%, and confidence level-95%. Calves aged below one year were excluded from the study to exclude the influence of maternal antibodies in the study results. Samples from each farm were selected at random. The calculation of sample size and randomized selection was performed using the online tool - Epitools Epidemiological Calculators (Sergeant, 2007). A total of 1075 serum samples were screened in the study. The farm-wise description viz., location of the farm, various breeds maintained in the farm, herd size, and the number of samples screened, is given in Table 1.

Table 1.

Demographic details of the farms included in the study

Farm No. Location (State) Species Breeds Herd size Sample size
Farm 1 Maharashtra Cattle Gir, Sahiwal 72 59
Farm 2 Maharashtra Cattle and buffalo Jersey and Pandharpuri 116 91
Farm 3 Maharashtra Cattle HF, HF cross breed, Jersey cross-breeds 180 89
Farm 4 Gujarat Cattle Gir 100 74
Farm 5 Gujarat Cattle Gir, Kankrej, Red Sindhi, Sahiwal, HF, HF cross breeds, Jersey, Jersey cross breeds 345 178
Farm 6 Andhra Pradesh Cattle HF cross-breed 427 206
Farm 7 Telangana Cattle HF cross-breed 817 212
Farm 8 Madhya Pradesh Cattle Gir, Sahiwal, Malvi, HF cross-breeds 163 73
Farm 9 Punjab Cattle HF and Jersey 124 93
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HF: Holstein Friesen

Sample analysis

Commercial ELISA kits for the detection of antibodies to BoHV-1, BVDV, Brucella spp., Coxiella burnetii, Neospora caninum, and Anaplasma marginale were used for the seroprevalence determination of IBR, BVD, brucellosis, Q fever, and anaplsamosis, respectively. IBR seroprevalence in Farm 7 was determined using an additional companion IBR-gE ELISA kit for differentiating vaccinated and infected animals as the farm had been vaccinated with an inactivated marker (gE deleted) vaccine. The test performance and result interpretations were done as per the instructions of the kit manufacturer. The list of kits, the criterion for result interpretation (cut-off), reported sensitivity, and specificity are provided in Table 2.

Table 2.

Details of the bovine ELISA kits used in this study and the cut-off values used for determination of the sample status

Disease Test method Test kit Target antigen Cut-off value Sensitivity
(%)		 Specificity
(%)		 Reference
Infectious bovine rhinotracheitis Blocking ELISA IBR gB antibody test kit (IDEXX) gB protein of BoHV-1 Blocking % <45% = Negative, ≥45 to <55% = Suspect, ≥55% = Positive 97.4 99.8 Validation report IDEXX
Blocking ELISA IBR gE antibody test kit (IDEXX) gE protein of BoHV-1 Sample/Negative (S/N) >0.70 = Negative, ≤0.70 to >60 = Suspect, ≤0.6 = Positive 97 99.8 Validation report IDEXX
Bovine viral diarrhoea Competitive ELISA Bovine BVDV Ab kit (Prionics) P80 Percentage inhibition <50% = Negative, ≥50% = Positive 97.9 99.2
Brucellosis Indirect ELISA Brucella abortus antibody test kit (IDEXX) Inactivated antigen Sample/Positive (S/P) % <80 = Negative, >80 = Positive 64.5 97.3
Q-fever Indirect ELISA Q-fever antibody test kit (IDEXX) Phase I & II Sample/Positive (S/P) <30 = Negative, ≥30% and <40% = Suspect, ≥40% = Positive 98.6 97.1
Anaplasmosis Competitive ELISA Anaplasma Antibody test kit (VMRD) MSP5 protein Inhibition % <30% = Negative, ≥30% = Positive 96 95.2
Neosporosis Indirect ELISA Neospora caninum antibody test kit (IDEXX) Sonicate lysate of tachyzoites Sample/Positive (S/P) <30 = Negative, ≥30 and <40 = Suspect, ≥40 = Positive 100 93.3
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Statistical analysis

Statistical analysis of data was performed using the online tool (Epitools Epidemiological Calculators: https://epitools.ausvet.com.au/). The true prevalence of the disease was determined based on the sensitivity and specificity of the test kit as reported previously (Greiner and Gardner, 2000). The confidence limit of true prevalence was determined using Blaker’s interval as described previously (Reiczigel et al., 2010 ▶).

The likelihood of association between the seroprevalence of two diseases was calculated as the Odds-ratio using the online MedCalc® statistical software. Samples whose results were inconclusive in ELISA tests were considered negative for the calculation of Odds-ratio.

Results

The majority of the 1075 animals (85.6%) showed antibodies in sera to one or more of the pathogens causing the respective diseases. Only 155 (14.4%) animals were negative for all the diseases investigated in this study. Seropositivity to more than two diseases was recorded in 611 animals (56.8%). None of the animals were positive for all the six pathogens. Six animals showed seropositivity to five pathogens, while 42 animals to 4 pathogens. The results indicated the high prevalence of multiple infections in the dairy herds. The study recorded 65 different combinations of results (Supplementary Table 1 (ST1)).

The overall prevalence observed for Q fever, neosporosis, brucellosis, anaplasmosis, IBR, and BVD in this study was 5.4%, 6.1%, 16.3%, 34.1%, 45.4%, and 56.5%, respectively (Table 3). There was wide variation in the prevalence of the diseases among the different farms (Table 3).

Table 3.

Seroprevalence of the diseases across farms, species and cattle breed-types

Variable Description No of samples True prevalence (95% confidence interval)
Infectious bovine rhinotracheitis Bovine viral diarrhea Brucellosis Q fever Anaplasmosis Neosporosis
Farm Farm 1 59 83.5 (71.4-91.6) 76.0 (63.2-85.6) 0 (0-10.2) 0 (0-6.37) 95.1 (84.2-100) 0 (0-2.2)
Farm 2 91 72.2 (61.8-80.8) 17.3 (10.6-26.6) 18.8 (9.5-32.7) 0 (0-4.98) 1.8 (0-9.5) 77.6 (67.4-85.2)
Farm 3 89 0 (0-4.1) 54.7 (44.1-65.0) 0 (0-8.3) 0 (0-3.34) 100 (95.8-100) 2.1 (0-10.5)
Farm 4 74 98.5 (91.1-100) 2.0 (0-8.8) 0 (0-3.6) 6.8 (1.8-16.0) 100 (99.0-100) 0 (0-2.5)
Farm 5 178 43.1 (35.9-50.7) 57.0 (49.5-64.3) 0 (0-0) 7.0 (3.3-12.4) 0.7 (0-5.5) 6.4 (1.9-12.5)
Farm 6 206 30.3 (24.3-37.0) 31.2 (25.1-38.0) 0 (0-0) 7.1 (3.6-12.1) 18.5 (12.9-25.3) 0 (0-0)
Farm 7 212 49.3 (42.5-56.2) 100 (97.3-100) 81.9 (71.0-92.6) 9.8 (5.9-15.1) 16.3 (11.0-22.7) 0 (0-2.8)
Farm 8 73 73.1 (61.5-82.5) 34.5 (24.3-46.2) 0 (0-7.5) 7.0 (1.9-16.3) 74.3 (62.0-84.1) 4.3 (0-14.2)
Farm 9 93 4.2 (1.5-10.6) 100 (94.4-100) 6.1 (0.5-17.3) 3.7 (0-10.9) 13.4 (6.5-23.2) 0 (0-2.2)
Species Buffalo 71 89.6 (79.7-95.7) 3.5 (0.7-11.2) 0 (0-7.9) 0 (0-7.1) 3.8 (0-13.5) 78.8 (67.3-87.0)
Cattle 1004 42.3 (39.2-45.5) 60.2 (57.0-63.3) 17.5 (14.3-21.2) 5.7 (4.1-7.7) 36.2 (33.0-39.5) 0.9 (0-2.9)
Cattle breed-type Crossbred 615 36.9 (33.1-40.9) 63.0 (59.0-66.8) 25.6 (21.0-30.9) 6.3 (4.2-8.9) 26.7 (22.9-30.8) 0.2 (0-2.7)
Exotic 145 7.6 (4.2-13.2) 88.7 (82.0-93.4) 18.0 (10.4-28.6) 1.3 (0-6.1) 20.3 (13.5-28.5) 8.1 (2.9-15.2)
Indigenous 244 76.5 (70.6-81.7) 36.3 (30.4-42.7) 0 (0-0.4) 7.2 (4.0-11.8) 69.7 (63.0-75.8) 0 (0-2.6)
Grand Total 1075 45.4 (42.4-48.5) 56.5 (53.4-59.5) 16.3 (13.2-19.7) 5.4 (3.9-7.3) 34.1 (31.0-37.7) 6.1 (4.1-8.4)
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As detailed in Table 4, the Odds ratio (OR) reveals a positive association between BVD and brucellosis (OR=14.2), IBR and Q fever (OR=2.2), IBR and neosporosis (OR=2.2), IBR and anaplasmosis (OR=1.8), brucellosis and Q fever (OR=1.3), IBR and brucellosis (OR=1.3), IBR and BVD (OR=1.1), and BVD and Q fever (OR=1.7).

Table 4.

The likelihood of association (Odds ratio) between the diseases

Disease combination Test results combinations Odds ratio (95% CI) P-value
Positive-Positive Positive-Negative Negative-Positive Negative-Negative
IBR Brucellosis 69 408 68 530 1.3 (0.9-1.9) 0.131
IBR BVD 274 203 324 274 1.1 (0.9-1.4) 0.285
IBR Anaplasmosis 207 270 180 418 1.8 (1.4-2.3) <0.001
IBR Q fever 54 423 33 565 2.2 (1.4-3.4) 0.0007
IBR Neosporosis 83 394 53 545 2.2 (1.5-3.1) <0.001
BVD Brucellosis 128 470 9 468 14.2 (7.1-28.2) <0.001
BVD Anaplasmosis 192 406 195 282 0.7 (0.5-0.9) 0.003
BVD Q fever 58 540 29 448 1.7 (1.0-2.6) 0.032
BVD Neosporosis 55 543 81 396 0.5 (0.3-0.7) 0.0002
Brucellosis Anaplasmosis 32 105 355 583 0.5 (0.3-0.8) 0.0011
Brucellosis Q fever 14 123 73 865 1.3 (0.7-2.5) 0.330
Brucellosis Neosporosis 14 123 122 816 0.8 (0.4-1.4) 0.36
Q fever Neosporosis 10 77 126 862 0.9 (0.4-1.8) 0.735
Q fever Anaplasmosis 27 60 360 628 0.8 (0.4-1.3) 0.315
Neosporosis Anaplasmosis 30 106 357 582 0.5 (0.3-0.7) 0.0004
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Discussion

Brucellosis, leptospirosis, Q fever, bovine genital campylobacteriosis, anaplasmosis, listeriosis, IBR, BVD, neosporosis, and trichomonosis are the common infectious diseases causing bovine abortions (Morris et al., 2018 ▶). In addition to abortion, most of these diseases are also linked to other reproductive complications in dairy herds viz., infertility, retention of foetal membrane, repeat breeding, anoestrus, endometritis, and pyometra (Sahlu, 2015 ▶). The present study estimated the prevalence of major abortion and infertility causing agents in the modern dairy herds located in different parts of India. The study was limited to the major diseases for which serological assays are routinely used for diagnosis. The study also investigated the concomitant seroprevalence of IBR, BVD, Brucellosis, Q fever, anaplasmosis, and neosporosis in the dairy herds.

In the present study, BVD was the most prevalent disease with an overall prevalence of 56.5%. BVD is endemic in India and has been reported in various parts of the country (Sood et al., 2007 ▶; Kumar et al., 2018 ▶) with prevalence varying widely among the herds (2 to 100%). The mean of BVD seroprevalence is reported at 49.2% with a wide variation among herds in the world (Scharnböck et al., 2018 ▶). The variation is attributed to the differences in management practices, and known risk factors influencing prevalence viz., artificial insemination, sex, herd demographic structure, herd size, frequency of purchase, and trading activities (Scharnböck et al., 2018 ▶). Control of BVD infection in dairy farms is important to prevent direct losses due to the disease, as well as reduce the use of antibiotics and other reactive measures for resolving other infections resulting from the immunosuppressive effect of the virus (Yarnall and Thrusfield, 2017 ▶). While vaccination for the prophylaxis of BVD is not available in India, the effectiveness of the vaccines currently available elsewhere in the world for the control of HoBi-like pestivirus (HoBiPev) infection is questionable (Bauermann et al., 2013 ▶). Studies to determine the evaluation of vaccine effectiveness and also the development of novel, efficacious vaccines will herald the prevention of this economically important bovine infectious disease. Adoption of strict screening of new-born calves and newly introduced animals for the persistent infection of BVDV and their prompt removal from the herd has been proven as an effective strategy in mitigating disease transmission and incidence.

Seroprevalence of IBR has been reported from almost all parts of India albeit at a varied rate (Renukaradhya et al., 1996 ▶; Trangadia et al., 2012 ▶; Das et al., 2014 ▶). Cattle with a history of abortion, metritis, repeat breeding, and retention of the placenta have been shown to have higher seropositivity (Patil et al., 2017 ▶; Sibhat et al., 2018 ▶). In our study, IBR is the second most prevalent disease (45.4%). Only one of the 9 farms studied was found to be free from IBR. Among the seropositive herds, the prevalence showed wide variation (from 4.2% to 98.5%). Only one of the farms (Farm 2) housed both cattle and buffaloes, and the prevalence of IBR in buffaloes was very high (89.6%) on this farm than in cattle (10%). This difference was statistically significant (P<0.001), and we reckon, warrants further investigation. A pilot study on the effectiveness of the inactivated IBR marker (gE deleted) vaccine recently reported a significant reduction in disease incidence, and abortion rates (Sarangi et al., 2020a ▶). In light of the high prevalence of IBR in the dairy herds, it may be prudent to adopt preventive vaccination of the respective herds routinely with the IBR marker vaccine to bring down the disease burden over time.

Bovine brucellosis is a major cause of contagious abortion in cattle. The disease is endemic in India and a nationwide survey has reported a seroprevalence of 8.4% in individual animals (Shome et al., 2019 ▶). A drastic increase in the prevalence rates has been reported in endemic herds (Lucchese et al., 2016 ▶; Sarangi et al., 2021 ▶). The overall prevalence of the disease in the current study is 16.3%. Six out of the nine farms in the study were free from brucellosis. High prevalence was recorded on two farms. However, both farms practiced calf-hood vaccination against brucellosis with live attenuated S19 vaccine. Although antibody response elicited by the B. abortus S19 vaccines usually wane below detection levels by one-year post-vaccination, the persistence of antibodies for a longer period extending up to 4.5 years has also been recorded (Simpson et al., 2018 ▶). Therefore, the possibility of vaccine-induced antibodies in Brucella seropositive animals could not be ruled out. Effective vaccination-based prophylaxis of brucellosis, therefore, necessitates the development of marker vaccines and companion diagnostic tests for differentiating infected and vaccinated animals (DIVA). Routine screening of the farms at periodic interval need to be undertaken and good managemental practices should be adopted in addition to the calf-hood vaccination to prevent the introduction of the disease to the farms as well as to reduce the incidence of the disease in the infected farms.

Q fever or coxiellosis is a zoonotic disease of public health concern caused by Coxiella burnetii. The disease is endemic in more than 51 countries and has been reported in India (Vaidya et al., 2010 ▶; Porter et al., 2011 ▶; Pradeep et al., 2017 ▶). In this study, the individual animal level true prevalence was 5.4% which is lower than reported previously in India and elsewhere (Anastacio et al., 2016 ▶; Kesavamurthy et al., 2020 ▶).

The overall prevalence of anaplasmosis was 34.1% which is also lower than previous reports from India (Sarangi et al., 2020b ▶; and references therein). Although all the 9 farms showed prevalence, the extent varied greatly from 0.7 to 100%. While four farms showed a high prevalence (74-100%), the rest showed a prevalence of less than 20% (Table 3). This wide variation could be due to managemental practices adopted by the farm especially the use of acaricides. Enzootic stability is an epidemiological concept proposed for vector-borne diseases which suggest that in highly endemic farms the possibility of severe clinical disease is rare (Oliveira et al., 2011 ▶). The Majority of the farms in this study, however, show low prevalence or enzootic instability (less than 20%), and hence adult cattle may be prone to severe clinical disease and mortality. Intensive tick control measures may be adopted on these farms to prevent disease outbreaks.

Seroprevalence to bovine neosporosis caused by the protozoan, Neospora caninum was 6.1%; lower than the previous reports from India and elsewhere (Mainar Jamie et al., 1996 ▶; Meenakshi et al., 2007 ▶; Nasir et al., 2011 ▶; Sengupta et al., 2013 ▶). Bovine neosporosis is mostly transmitted by feed and pasture contaminated with dog faeces (Haddad et al., 2005). Therefore, the prevalence of this disease is higher in conventional farms and smallholder cows where open grazing is the norm (Sengupta et al., 2013 ▶). Expectedly, the disease was absent in five of the studied farms, while the prevalence was low in the others (2.1-6.3%). Further reduction in the disease prevalence would be possible by screening at regular intervals and prompt removal of the repeat breeders. Surprisingly, the prevalence of neosporosis in farm 2 was high (77.6%). Both cattle and buffaloes of the farm showed high prevalence. The reasons for high prevalence while not obvious require further investigation.

Out of the 1075 animals, 611 (56.8%) were serologically positive for two or more pathogens. Multiple infections of cattle have been reported previously (Moshkelani et al., 2011 ▶; Yang et al., 2012 ▶; Lucchese et al., 2016 ▶; Sarangi et al., 2021 ▶). IBR and BVD are known to cause immunosuppression in the host and render increased susceptibility to other bacterial and viral infections (Hutching et al., 1990 ▶; Wellenberg et al., 2002 ▶). Epidemiological studies have also reported a positive association between these two viruses (Nikbakht et al., 2015 ▶; Noaman and Nabinejad, 2020 ▶). In this study, a very strong association was observed between the seropositivity of BVD with brucellosis. The Odds of BVD seropositive cows for brucellosis was 14.2 with a statistically significant (P<0.001) likelihood of association (Table 4). The Odds ratios of more than one were also recorded for IBR and other diseases viz., Q fever, neosporosis, brucellosis, BVD, and anaplasmosis (Table 4). The results suggest increased susceptibility of IBR seropositive cows to other bacterial and viral infections. BoHV-1 is known to impair host immune responses viz., the phagocytic function of macrophages and monocytes, reduced antibody-dependent cellular cytotoxicity function, poor T cell stimulation (Biswas et al., 2013 ▶; Jones, 2019 ▶), and hence rendering the IBR seropositive animals prone to secondary infections.

In the present study, viral diseases were more common in the dairy herds compared to bacterial and protozoan diseases with BVD, the most prevalent pathogen followed by IBR. Multiple infections were observed in a significant proportion of the animals in the dairy herds. While a strong association was observed between the seroprevalence of BVD and brucellosis, a positive association was observed between the seropositivity of IBR and other diseases. Preventive vaccination, stringent biosecurity measures, and animal health management practices should be adopted to reduce the incidence of the diseases, thereby improving productivity.

Conflict of interest

The authors declare that there are no conflicts of interest in this article.

Supporting Online Material

Refer to web version on PubMed Central® (PMC) for Supplementary Material.
ijvr-23-189-s1.pdf (57.8KB, pdf)

Acknowledgment

The authors are grateful for the management of the National Dairy Development Board (NDDB), for providing the necessary funding and facilities for the work.

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