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Bovine Tuberculosis: Abattoir Prevalence, Species Identification and Its Economic Impact Assessment of Assam and Meghalaya

Acheenta Gohain Barua Himangshu Raj Chandrani Goswami Pranita Konwar Jyoti Pawan Chutia
Vol 8(8), 204-213
DOI- http://dx.doi.org/10.5455/ijlr.20180209095048

To determine the prevalence of tuberculous lesions, species identification of the organism and associated direct economic losses due to the condemnation of organs/tissues of slaughtered cattle and buffaloes in Assam and Meghalaya, India. Over three years (September 2014 to October 2017), a total of 6053 carcasses (4985 cattle and 1068 buffalo) has been examined for tuberculous like lesions. Species identification was confirmed by biochemical test (viz. Nitrate reduction test, Pyrazinamidase test and Niacin detection test) and PCR targeting oxyR gene. Based on post-mortem examination the overall period prevalence was found to be 12.89%. Direct economic losses associated with the condemnation of 1742.94 Kg of meat/organs due to tuberculous lesions was valued as 339253.80 ($ 5241.46). Our results indicate that bovine tuberculosis caused by M. bovis is prevalent in Assam and Meghalaya and accounts for high economic losses due to the condemnation of edible organs/meat only.


Keywords : Bovine Tuberculosis Economic Loss Meat Condemnation Mycobacterium bovis North East India

Bovine tuberculosis (BTB) caused by Mycobacterium bovis, is endemic in many developing countries with a negative impact on animal productivity as well as public health due to its zoonotic nature (Michel et al., 2010; Torgerson and Torgerson, 2010). Bovine tuberculosis is a disease of zoonotic and economic significance worldwide especially in developing countries resulting in losses of human live, productive time on the part of farmers, and a huge sum of money from the condemnation of carcasses at slaughter (Ejeh et al., 2014). Farmers, slaughterhouse workers, animal keepers at the zoo as well as veterinary professionals are at high risk to the exposure of BTB infection through contact with infected livestock or their carcasses (Hambolu et al., 2013; Elmonir and Ramadan, 2016). BTB has impact on economic loss due to the decrease in milk yield and from the increased condemnation of meat and edible organs (de la Rua-Domenech et al., 2006).

Diagnosis of tuberculosis in cattle is mainly through tuberculin testing, culture and molecular genotyping (Brosch et al., 2002; Warren et al., 2006). Culture is the gold standard, however, in resource poor regions like North East (NE) India, monitoring of BTB by bacteriological study and IFN-γ assay are always not feasible because assays are costly and time consuming. Also, there is lack of organised slaughter house and routine post-mortem (PM) examination. However, meat inspection is an applicable tool for the detection of BTB in slaughtered animals in developing countries which provides useful insight into the prevalence of BTB and plays important role in both quality assurance and control (Youssef and Ahmed, 2014). There is also a paucity of information on the prevalence of bovine tuberculosis in NE India. In many slaughter houses in this region, the localized tuberculous lesions were trimmed and the remaining parts of the carcass were passed fit for human consumption and captive wild animal in zoo. Unfortunately, there is no official bovine slaughter house in Assam and Meghalaya. The objective of this study is to determine the prevalence of tuberculous lesions, species identification of the organism and associated direct economic losses due to the condemnation of organs/tissues of slaughtered cattle and buffaloes in Assam and Meghalaya in India.

Materials and Methods

Study Area

Different slaughter houses in Byrnihut, Killing, Umsning, Shillong, Jowai areas of Meghalaya and six mile, Hatigaon, Kharupetia, Nagaon, Morigaon, Borpeta, Dhuburi and Laluk areas of Assam were selected for the study (Fig. 1). More than 20000 animals were slaughtered annually in these unorganised abattoirs which served more than 5 million consumers and captive wildlife species. This study was carried out over 3 years from September 2014 to October 2017 and different abattoirs were visited several times by authors during this period for active survey.

 

 

 

Fig. 1: Maps of Assam and Meghalaya, the two north eastern states of India. (Map is not to scale)

 

Sample Size Determination

The total number of carcasses for the study was calculated based on the formula given by Thrusfield (2007).

Where N is the required sample size, Z is the Z-score at different confidence interval, P is the expected prevalence and D is the desired absolute precision.

A 10% expected prevalence with 99% confidence interval and 1% desired absolute precision was used to determine the sample size required for the study. Hence, substituting these values the required sample size was determined to be 5972 carcasses. But to increase the precision of our estimates, the total numbers of animals included in the present study were 6,053. The sample units were selected using simple random sampling method from those animals brought for slaughter on the day of PM examination.

Post-Mortem Inspection and Prevalence Estimation

All animal carcasses were inspected by qualified, well-trained veterinarians. Mainly necrotic calcified, proliferative granulomatous nodules, milliary nodules were selected as tuberculous like lesions (Fig. 2). Visual examination, palpation and knife incision were performed for PM examination. Lymph nodes and organs including lungs, liver, kidneys, spleens, intestines, uterus and mammary glands were examined for the presence of tuberculous like lesions. The suspected lesions were collected into a clean, sterile container to avoid contamination and transported through ice box to the laboratory. Prevalence was estimated as per Elmonir et al. (2015):

A B

Fig. 2: Tuberculous lesions cattle carcass A) Lung; B) Liver

Culture and Species Specification

The lesion samples were further confirmed by Ziehl-Neelsen staining for detection of acid fast bacteria and subsequently, culture was done in Lowenstein-Jensen (LJ) media (one incorporating glycerol and the other pyruvate) (Fig. 3).

A B
Fig. 3: a) Ziehl-Neelsen staining for detection of Acid fast bacteria from suspected organ samples collected from abattoir. b) Culture of M. Bovis in Lowenstein-Jensen media (supplemented with pyruvate).

Species specification was done according to Barua et al. (2017). Briefly, culture positive isolates were further subjected for the different biochemical test (viz. nitrate reduction test, pyrazinamidase test and niacin detection test) and PCR targeting oxyR gene. PCR was performed with forward primer oxyRMTB-12F (5́-TGGCCGGGCTTCGCGCGT-3́) for both the species; however the reverse primers were different. In one reaction, reverse primer oxyRMT1R (5́-GCACGACGGTGGCCAGGCA-3́) specific for M. tuberculosis while, in another reaction primer oxyRMB2R (5́-TGCACGACGGTGGCCAGGTA-3́) specific for M. bovis were used, which amplify a product size of 280 base pair (Barua et al., 2017).

Economic Losses Estimation

Direct economic losses due to the condemnation of muscle or organs with tuberculous lesions were estimated based on total weight loss of meat in kilogram (kg) and average market price per kg. During the study period, butchers and slaughterhouse personnel were interviewed for data of the average weight and market price for edible (muscles, lungs, heart, liver, kidney and spleen) and non-edible (intestine, uterus) organs/tissues of cattle and buffaloes carcasses. The average meat yield for the whole carcass of cattle and buffaloes was 237 kg (178-296 kg). The average price for 1 kg of meat was Rs/-220.00. The average weight for lung (with heart attached) and liver was around 1.8 Kg and marketed price for liver was Rs. 220.00 and lung was Rs. 180.00 per Kg. The price of intestine was Rs. 100.00 per unit and that of uterus was Rs. 50.00. Indirect annual economic loss (IAEL) was estimated based on annual average slaughter in the abattoirs of these regions (AAS), average price of 1Kg condemned meat/organ (AP) and prevalence rate (P), i.e. IAEL=AAS×AP×P (Kwaghe et al., 2015).

Results and Discussion

In this study, the overall prevalence of tuberculous lesions (Fig. 2) among all the slaughtered animals in different abattoirs in these regions during the period from March 2014 to April 2017 was 12.89% (Table 1). The overall prevalence rate of BTB in slaughtered cattle and buffaloes was 13.09% and 11.89% respectively. The yearly prevalence rate was recorded as 12.41%, 13.35% and 12.58% during 2014-15, 2015-16 and 2016-17 respectively (Table 1).

A total of 1692 suspected organ and tissue samples were collected from 780 carcasses. In the year 2014-2015 out of 816 cattle carcasses were screened, where 106 carcasses were suspected for BTB based on PM examination. However, during Ziehl-Neelsen staining and culture by Lowenstein-Jensen (LJ) media 108 carcasses revealed positive TB lesions. It was found that lymph nodes and lungs contributed highest tuberculous lesions with a percentage of 39.01% and 29.49% respectively followed by liver (22.39%), muscle (7.62%), intestine (1.06%) and uterus (0.41%) (Table 1). All the culture isolates were found to be M. bovis based on biochemical tests and PCR assay (Fig. 3& Fig. 4).

 

 

 

Table 1: Year-wise distribution of screening of cattle and buffaloes carcasses for tuberculous lesions

Study period Organs Total carcasses screened Animal suspected (Prevalence) TB lesions
Cattle Buffalo Cattle Buffalo Cattle Buffalo
2014-2015 Muscle 816 296 106 (12.99%) 32 (10.81%) 21 8
Liver 73 26
Lung 108 29
Lymph nodes 96 51
Intestine 3 2
Uterus 2 2
Total (2014-15) 303 118
2015-2016 Muscle 2173 463 298 (13.71%) 54 (11.66%) 34 17
Liver 86 53
Lung 124 63
Lymph nodes 169 96
Intestine 4 4
Uterus 2 1
Total (2015-2016) 419 234
2016-2017 Muscle 1996 309 249 (12.47%) 41 (13.27%) 38 11
Liver 102 39
Lung 110 65
Lymph nodes 164 84
Intestine 4 1
Uterus 0 0
Total (2016-2017) 418 200
Total (2014-2017) species wise 4985 1068 653 (13.09%) 127 (11.89%) 1140 552
Overall (2014-2017) 6053 780 (12.89%) 1692

Fig. 4: Agarose gel electrophoresis image showing presence of oxyR (280bp) gene in M. bovis (L1 and L3) but absent in M. tuberculosis (L2 and L4). Lane M indicates 100bp

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

  M    L1     L2    L3   L4

   

The overall weight losses of organs in Kg from all the slaughtered carcasses were 1195.08 and 547.86 in cattle and buffaloes respectively (Table 2). A total of Rs. 233313.60 ($ 3604.69) in cattle and Rs. 105940.00 ($ 1636.77) in buffaloes was lost due to condemnation of organs affected by tuberculous lesions Based on an oral interview with the slaughter house workers, it was estimated that annually an average of 29200 animals were slaughtered in these abattoirs. The indirect economic loss was calculated considering prevalence rate of 12.89% and the average price of Rs. 220.00 per Kg condemned meat/organ. Indirect annual economic loss (IAEL) was found to be Rs. 963600.00 ($ 14887.60) due to the condemnation of meat.

Table 2: Economic loss due to the condemnation of various organs

Study period Organs Total weight (Kg) Total Loss ( )
Cattle Buffalo Cattle Buffalo
2014-2015 Muscle 15.96 6.08 3511.2 1337.6
Liver 131.4 46.8 28908 10296
Lung 194.4 52.2 34992 9396
Lymph nodes 0 0 0 0
Intestine 9 6 900 600
Uterus 3 3 150 150
Total (2014-15)   353.76 114.08 68461.2 21779.6
2015-2016 Muscle 25.84 12.92 5684.8 2842.4
Liver 154.8 95.4 34056 20988
Lung 223.2 113.4 40176 20412
Lymph nodes 0 0 0 0
Intestine 12 12 1200 1200
Uterus 3 1.5 150 75
Total (2016-2017)   418.84 235.22 81266.8 45517.4
2016-2017 Muscle 28.88 8.36 6353.6 1839.2
Liver 183.6 70.2 40392 15444
Lung 198 117 35640 21060
Lymph nodes 0 0 0 0
Intestine 12 3 1200 300
Uterus 0 0 0 0
Total (2016-2017) 422.48 198.56 83585.6 38643.2
Total (2014-2017) 1195.08 547.86 233313.6 105940
Species wise
Overall (2014-2017) 1742.94 339253.6

There are limited reports available from India and many epidemiological and public health aspects of BTB remain largely unknown (Baqir et al., 2014; Neeraja et al., 2014a, b; Verma et al., 2014a,b). Thakur et al. (2010) recorded 14.31 to 34.42% prevalence rate of BTB in India. In another surveillance study in Assam and Meghalaya, Barua et al. (2017) recorded 16.58 to 19.59% prevalence of BTB based on gamma interferon (IFN-γ) assay and single intradermal comparative tuberculin test (SICTT).  Based on slaughter house surveillance the prevalence rate of bovine TB in Ri-Bhoi district of Meghalaya was 15% (Barua et al., 2016). The overall prevalence of tuberculous lesions among all slaughtered bovines in these abattoirs was approximately 12.89%. The prevalence in this study was higher than Egypt (0.21-0.6%) (Ramadan et al., 2012; Youssef and Ahmed, 2014) and African countries as 9% in Chad (Milian et al., 2000), 6.1% in Ethiopia (Aylate et al., 2013) and 1.9% in Nigeria (Ejeh et al., 2014). However, lower prevalence (0.052%) was detected by Shitaye et al. (2006) in ten years’ surveillance study in Ethiopia.  From all the slaughtered carcasses, the predominant organs showing tuberculous lesions were the lungs and its associated lymph nodes. This finding was inconsistent with many studies (Shitaye et al., 2006; Aylate et al., 2013; Youssef and Ahmed, 2014; Barua et al., 2016). Furthermore, it was recorded that the prevalence of pulmonary tuberculous lesions was higher in cattle than buffalo’s carcasses, which agreed with findings of Youssef and Ahmed (2014). The variation of BTB prevalence in this study with the previously reported studies in other developing countries might be attributed to many factors that include animal husbandry measures (production system, ventilation, hygienic conditions, etc.), animal breeds, grazing habits, climatic changes and national regulations for BTB combating (such as, comparative tuberculin test and slaughter policy). In NE India, dairy cattle and buffaloes are usually raised by semi-intensive production where animals kept indoors in large numbers.

Majority of reports on economic impact due to TB were from African countries. Comparatively lower economic losses were recorded in Rwanda ($ 4810) by Habarugira et al. (2014), in Nigeria ($ 18200) by Ejeh et al. (2014) and in Ghana ($ 18693.1) by Atawalna et al. (2016). In Nigeria, Kwaghe et al. (2015) recorded direct loss of $ 24209.396 and indirect loss of $ 1723691.6. The variation in economic losses might be due to the variation of BTB prevalence rate, the economic situation of the country as well as market price and demand for meat.

Conclusion

Based on these findings, it is highly recommended to strengthen surveillance and control measures against BTB in livestock of the study area. Strict measures and interventions should be taken towards preventing unauthorized slaughtering. PM examination measures and awareness programme regarding knowledge of occupational zoonoses and risks factors might be helpful to diminish the incidence of BTB.

Acknowledgements

Authors are thankful to Indian Council of Agricultural Research, New Delhi for funding the project “Outreach project on zoonotic diseases” and Director of Research (Veterinary), Assam Agricultural University for providing necessary facilities to carry out research work.

Conflict of Interest

The authors declare no conflict of interest.

 

References

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  12. Hambolu D, Freeman J and Taddese HB. 2013. Predictors of Bovine TB Risk Behaviour amongst Meat Handlers in Nigeria: A Cross-Sectional Study Guided by the Health Belief Model. PLoS One. 8: e56091.
  13. Kwaghe AV, Ameh AJ, Ambali AG, Kudi AC and Kachalla MG. 2015. Prevalence and Economic Losses from Bovine Tuberculosis in Maiduguri, Borno State, Nigeria. International Journal of Life Sciences. 4: 283–287.
  14. Michel AL, Muller B and van Helden PD. 2010. Mycobacterium bovis at the animal-human interface: A problem, or not? Veterinary Microbiology. 140: 371–381.
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  19. Shitaye JE, Getahun B, Alemayehu T, Skoric M, Treml F, Fictum P et al. 2006. A prevalence study of bovine tuberculosis by using abattoir meat inspection and tuberculin skin testing data, histopathological and IS6110 PCR examination of tissues with tuberculosis lesions in cattle in Europia. Veterinarni Medicina. 51: 512–522.
  20. Thakur A, Sharma M, Katoch VC, Dhar P and Katoch RC. 2010. A study on the prevalence of bovine tuberculosis in farmed dairy cattle in Himachal Pradesh. Veterinary World. 3: 408–414.
  21. Thrusfield 2007. Veterinary epidemiology. 3rd Edn. Blackwell Science, Oxford, UK, pp. 165–190.
  22. Torgerson PR and Torgerson DJ. 2010. Public health and bovine tuberculosis: what’s all the fuss about? Trends in Microbiology. 18: 67–72.
  23. Verma AK, Tiwari R, Chakraborty S, Neha, Saminathan M, Dhama K, et al. 2014a. Insights into bovine tuberculosis (bTB), various approaches for its diagnosis, control and its publicBovine tuberculosis (BTB) caused by Mycobacterium bovis, is endemic in many developing countries with a negative impact on animal productivity as well as public health due to its zoonotic nature (Michel et al., 2010; Torgerson and Torgerson, 2010). Bovine tuberculosis is a disease of zoonotic and economic significance worldwide especially in developing countries resulting in losses of human live, productive time on the part of farmers, and a huge sum of money from the condemnation of carcasses at slaughter (Ejeh et al., 2014). Farmers, slaughterhouse workers, animal keepers at the zoo as well as veterinary professionals are at high risk to the exposure of BTB infection through contact with infected livestock or their carcasses (Hambolu et al., 2013; Elmonir and Ramadan, 2016). BTB has impact on economic loss due to the decrease in milk yield and from the increased condemnation of meat and edible organs (de la Rua-Domenech et al., 2006).

    Diagnosis of tuberculosis in cattle is mainly through tuberculin testing, culture and molecular genotyping (Brosch et al., 2002; Warren et al., 2006). Culture is the gold standard, however, in resource poor regions like North East (NE) India, monitoring of BTB by bacteriological study and IFN-γ assay are always not feasible because assays are costly and time consuming. Also, there is lack of organised slaughter house and routine post-mortem (PM) examination. However, meat inspection is an applicable tool for the detection of BTB in slaughtered animals in developing countries which provides useful insight into the prevalence of BTB and plays important role in both quality assurance and control (Youssef and Ahmed, 2014). There is also a paucity of information on the prevalence of bovine tuberculosis in NE India. In many slaughter houses in this region, the localized tuberculous lesions were trimmed and the remaining parts of the carcass were passed fit for human consumption and captive wild animal in zoo. Unfortunately, there is no official bovine slaughter house in Assam and Meghalaya. The objective of this study is to determine the prevalence of tuberculous lesions, species identification of the organism and associated direct economic losses due to the condemnation of organs/tissues of slaughtered cattle and buffaloes in Assam and Meghalaya in India.

    Materials and Methods

    Study Area

    Different slaughter houses in Byrnihut, Killing, Umsning, Shillong, Jowai areas of Meghalaya and six mile, Hatigaon, Kharupetia, Nagaon, Morigaon, Borpeta, Dhuburi and Laluk areas of Assam were selected for the study (Fig. 1). More than 20000 animals were slaughtered annually in these unorganised abattoirs which served more than 5 million consumers and captive wildlife species. This study was carried out over 3 years from September 2014 to October 2017 and different abattoirs were visited several times by authors during this period for active survey.

     

     

     

    Fig. 1: Maps of Assam and Meghalaya, the two north eastern states of India. (Map is not to scale)

     

    Sample Size Determination

    The total number of carcasses for the study was calculated based on the formula given by Thrusfield (2007).

    Where N is the required sample size, Z is the Z-score at different confidence interval, P is the expected prevalence and D is the desired absolute precision.

    A 10% expected prevalence with 99% confidence interval and 1% desired absolute precision was used to determine the sample size required for the study. Hence, substituting these values the required sample size was determined to be 5972 carcasses. But to increase the precision of our estimates, the total numbers of animals included in the present study were 6,053. The sample units were selected using simple random sampling method from those animals brought for slaughter on the day of PM examination.

    Post-Mortem Inspection and Prevalence Estimation

    All animal carcasses were inspected by qualified, well-trained veterinarians. Mainly necrotic calcified, proliferative granulomatous nodules, milliary nodules were selected as tuberculous like lesions (Fig. 2). Visual examination, palpation and knife incision were performed for PM examination. Lymph nodes and organs including lungs, liver, kidneys, spleens, intestines, uterus and mammary glands were examined for the presence of tuberculous like lesions. The suspected lesions were collected into a clean, sterile container to avoid contamination and transported through ice box to the laboratory. Prevalence was estimated as per Elmonir et al. (2015):

    A B

    Fig. 2: Tuberculous lesions cattle carcass A) Lung; B) Liver

    Culture and Species Specification

    The lesion samples were further confirmed by Ziehl-Neelsen staining for detection of acid fast bacteria and subsequently, culture was done in Lowenstein-Jensen (LJ) media (one incorporating glycerol and the other pyruvate) (Fig. 3).

    A B
    Fig. 3: a) Ziehl-Neelsen staining for detection of Acid fast bacteria from suspected organ samples collected from abattoir. b) Culture of M. Bovis in Lowenstein-Jensen media (supplemented with pyruvate).

    Species specification was done according to Barua et al. (2017). Briefly, culture positive isolates were further subjected for the different biochemical test (viz. nitrate reduction test, pyrazinamidase test and niacin detection test) and PCR targeting oxyR gene. PCR was performed with forward primer oxyRMTB-12F (5́-TGGCCGGGCTTCGCGCGT-3́) for both the species; however the reverse primers were different. In one reaction, reverse primer oxyRMT1R (5́-GCACGACGGTGGCCAGGCA-3́) specific for M. tuberculosis while, in another reaction primer oxyRMB2R (5́-TGCACGACGGTGGCCAGGTA-3́) specific for M. bovis were used, which amplify a product size of 280 base pair (Barua et al., 2017).

    Economic Losses Estimation

    Direct economic losses due to the condemnation of muscle or organs with tuberculous lesions were estimated based on total weight loss of meat in kilogram (kg) and average market price per kg. During the study period, butchers and slaughterhouse personnel were interviewed for data of the average weight and market price for edible (muscles, lungs, heart, liver, kidney and spleen) and non-edible (intestine, uterus) organs/tissues of cattle and buffaloes carcasses. The average meat yield for the whole carcass of cattle and buffaloes was 237 kg (178-296 kg). The average price for 1 kg of meat was Rs/-220.00. The average weight for lung (with heart attached) and liver was around 1.8 Kg and marketed price for liver was Rs. 220.00 and lung was Rs. 180.00 per Kg. The price of intestine was Rs. 100.00 per unit and that of uterus was Rs. 50.00. Indirect annual economic loss (IAEL) was estimated based on annual average slaughter in the abattoirs of these regions (AAS), average price of 1Kg condemned meat/organ (AP) and prevalence rate (P), i.e. IAEL=AAS×AP×P (Kwaghe et al., 2015).

    Results and Discussion

    In this study, the overall prevalence of tuberculous lesions (Fig. 2) among all the slaughtered animals in different abattoirs in these regions during the period from March 2014 to April 2017 was 12.89% (Table 1). The overall prevalence rate of BTB in slaughtered cattle and buffaloes was 13.09% and 11.89% respectively. The yearly prevalence rate was recorded as 12.41%, 13.35% and 12.58% during 2014-15, 2015-16 and 2016-17 respectively (Table 1).

    A total of 1692 suspected organ and tissue samples were collected from 780 carcasses. In the year 2014-2015 out of 816 cattle carcasses were screened, where 106 carcasses were suspected for BTB based on PM examination. However, during Ziehl-Neelsen staining and culture by Lowenstein-Jensen (LJ) media 108 carcasses revealed positive TB lesions. It was found that lymph nodes and lungs contributed highest tuberculous lesions with a percentage of 39.01% and 29.49% respectively followed by liver (22.39%), muscle (7.62%), intestine (1.06%) and uterus (0.41%) (Table 1). All the culture isolates were found to be M. bovis based on biochemical tests and PCR assay (Fig. 3& Fig. 4).

     

     

     

    Table 1: Year-wise distribution of screening of cattle and buffaloes carcasses for tuberculous lesions

    Study period Organs Total carcasses screened Animal suspected (Prevalence) TB lesions
    Cattle Buffalo Cattle Buffalo Cattle Buffalo
    2014-2015 Muscle 816 296 106 (12.99%) 32 (10.81%) 21 8
    Liver 73 26
    Lung 108 29
    Lymph nodes 96 51
    Intestine 3 2
    Uterus 2 2
    Total (2014-15) 303 118
    2015-2016 Muscle 2173 463 298 (13.71%) 54 (11.66%) 34 17
    Liver 86 53
    Lung 124 63
    Lymph nodes 169 96
    Intestine 4 4
    Uterus 2 1
    Total (2015-2016) 419 234
    2016-2017 Muscle 1996 309 249 (12.47%) 41 (13.27%) 38 11
    Liver 102 39
    Lung 110 65
    Lymph nodes 164 84
    Intestine 4 1
    Uterus 0 0
    Total (2016-2017) 418 200
    Total (2014-2017) species wise 4985 1068 653 (13.09%) 127 (11.89%) 1140 552
    Overall (2014-2017) 6053 780 (12.89%) 1692

    Fig. 4: Agarose gel electrophoresis image showing presence of oxyR (280bp) gene in M. bovis (L1 and L3) but absent in M. tuberculosis (L2 and L4). Lane M indicates 100bp

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

      M    L1     L2    L3   L4

       

    The overall weight losses of organs in Kg from all the slaughtered carcasses were 1195.08 and 547.86 in cattle and buffaloes respectively (Table 2). A total of Rs. 233313.60 ($ 3604.69) in cattle and Rs. 105940.00 ($ 1636.77) in buffaloes was lost due to condemnation of organs affected by tuberculous lesions Based on an oral interview with the slaughter house workers, it was estimated that annually an average of 29200 animals were slaughtered in these abattoirs. The indirect economic loss was calculated considering prevalence rate of 12.89% and the average price of Rs. 220.00 per Kg condemned meat/organ. Indirect annual economic loss (IAEL) was found to be Rs. 963600.00 ($ 14887.60) due to the condemnation of meat.

    Table 2: Economic loss due to the condemnation of various organs

    Study period Organs Total weight (Kg) Total Loss ( )
    Cattle Buffalo Cattle Buffalo
    2014-2015 Muscle 15.96 6.08 3511.2 1337.6
    Liver 131.4 46.8 28908 10296
    Lung 194.4 52.2 34992 9396
    Lymph nodes 0 0 0 0
    Intestine 9 6 900 600
    Uterus 3 3 150 150
    Total (2014-15)   353.76 114.08 68461.2 21779.6
    2015-2016 Muscle 25.84 12.92 5684.8 2842.4
    Liver 154.8 95.4 34056 20988
    Lung 223.2 113.4 40176 20412
    Lymph nodes 0 0 0 0
    Intestine 12 12 1200 1200
    Uterus 3 1.5 150 75
    Total (2016-2017)   418.84 235.22 81266.8 45517.4
    2016-2017 Muscle 28.88 8.36 6353.6 1839.2
    Liver 183.6 70.2 40392 15444
    Lung 198 117 35640 21060
    Lymph nodes 0 0 0 0
    Intestine 12 3 1200 300
    Uterus 0 0 0 0
    Total (2016-2017) 422.48 198.56 83585.6 38643.2
    Total (2014-2017) 1195.08 547.86 233313.6 105940
    Species wise
    Overall (2014-2017) 1742.94 339253.6

    There are limited reports available from India and many epidemiological and public health aspects of BTB remain largely unknown (Baqir et al., 2014; Neeraja et al., 2014a, b; Verma et al., 2014a,b). Thakur et al. (2010) recorded 14.31 to 34.42% prevalence rate of BTB in India. In another surveillance study in Assam and Meghalaya, Barua et al. (2017) recorded 16.58 to 19.59% prevalence of BTB based on gamma interferon (IFN-γ) assay and single intradermal comparative tuberculin test (SICTT).  Based on slaughter house surveillance the prevalence rate of bovine TB in Ri-Bhoi district of Meghalaya was 15% (Barua et al., 2016). The overall prevalence of tuberculous lesions among all slaughtered bovines in these abattoirs was approximately 12.89%. The prevalence in this study was higher than Egypt (0.21-0.6%) (Ramadan et al., 2012; Youssef and Ahmed, 2014) and African countries as 9% in Chad (Milian et al., 2000), 6.1% in Ethiopia (Aylate et al., 2013) and 1.9% in Nigeria (Ejeh et al., 2014). However, lower prevalence (0.052%) was detected by Shitaye et al. (2006) in ten years’ surveillance study in Ethiopia.  From all the slaughtered carcasses, the predominant organs showing tuberculous lesions were the lungs and its associated lymph nodes. This finding was inconsistent with many studies (Shitaye et al., 2006; Aylate et al., 2013; Youssef and Ahmed, 2014; Barua et al., 2016). Furthermore, it was recorded that the prevalence of pulmonary tuberculous lesions was higher in cattle than buffalo’s carcasses, which agreed with findings of Youssef and Ahmed (2014). The variation of BTB prevalence in this study with the previously reported studies in other developing countries might be attributed to many factors that include animal husbandry measures (production system, ventilation, hygienic conditions, etc.), animal breeds, grazing habits, climatic changes and national regulations for BTB combating (such as, comparative tuberculin test and slaughter policy). In NE India, dairy cattle and buffaloes are usually raised by semi-intensive production where animals kept indoors in large numbers.

    Majority of reports on economic impact due to TB were from African countries. Comparatively lower economic losses were recorded in Rwanda ($ 4810) by Habarugira et al. (2014), in Nigeria ($ 18200) by Ejeh et al. (2014) and in Ghana ($ 18693.1) by Atawalna et al. (2016). In Nigeria, Kwaghe et al. (2015) recorded direct loss of $ 24209.396 and indirect loss of $ 1723691.6. The variation in economic losses might be due to the variation of BTB prevalence rate, the economic situation of the country as well as market price and demand for meat.

    Conclusion

    Based on these findings, it is highly recommended to strengthen surveillance and control measures against BTB in livestock of the study area. Strict measures and interventions should be taken towards preventing unauthorized slaughtering. PM examination measures and awareness programme regarding knowledge of occupational zoonoses and risks factors might be helpful to diminish the incidence of BTB.

    Acknowledgements

    Authors are thankful to Indian Council of Agricultural Research, New Delhi for funding the project “Outreach project on zoonotic diseases” and Director of Research (Veterinary), Assam Agricultural University for providing necessary facilities to carry out research work.

    Conflict of Interest

    The authors declare no conflict of interest.

     

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    health concerns: An update. Asian Journal of Animal and Veterinary Advances. 9: 323–344.

  24. Verma AK, Dhama K, Chakraborty S, Kumar A, Tiwari R, Rahal A. et al. 2014b. Strategies for combating and eradicating important infectious diseases of animals with particular reference to India: Present and future perspectives. Asian Journal of Animal and Veterinary Advances. 9: 77–106.
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