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Bovine Tuberculosis in Rwanda: Prevalence and Economic
Impact Evaluation by Meat Inspection at Société d’Abattoir
de Nyabugogo-Nyabugogo Abattoir, Kigali
Gervais Habarugira*1, Joseph Rukelibuga2, Mark Nanyingi3, 5
Borden Mushonga4
1School of Animal Sciences and Veterinary Medicine, College of Agriculture, Animal Sciences and
Veterinary Sciences, University of Rwanda, Nyagatare, Rwanda.
2US-Centre for Disease Control and Prevention (CDC), Kigali, Rwanda.
3Department of Public Health, Pharmacology and Toxicology, University of Nairobi Nairobi, Kenya.
4Department of Livestock and Pasture Science, Faculty of Science and Agriculture, University of Fort Hare,
South Africa.
5Kenya Medical Research Institute, United States Centres for Disease Control and Prevention, Kenya
Corresponding Author: Gervais Habarugira gervaish@gmail.com
*
Presented at the Inaugural Regional conference on Zoonotic Diseases in Eastern
Africa, Naivasha, Kenya on Tuesday, March 10th, 2015
 Etiology: TB in humans is primarily caused by
Mycobacterium tuberculosis (M. tb), it represents
the greatest burden of infectious diseases second
to AIDS worldwide.
 Global incidence estimates : 8.7 million cases
of & 1.4 million deaths/3,833 daily (WHO 2011)
 Burden: 17 million Disability Adjusted Life
Years (DALY), social impact underestimated.
 Drug resistance: 480,000 people with MDR-TB
 Rwanda prevalence estimates: human TB due
to (M. tb) 0.08% in 2008 (MOH 2008).
INTRODUCTION: GLOBAL ZOONOTIC TB BURDEN
(WHO Annual TB report, 2011, WHO TB Factsheet 2014)
 Pathogen host and species jump : Cattle is the
main host of Mycobacterium bovis (M. bovis) and
leads to latent infection in immunocompromised
humans (LTBI)(Gortázar et al. 2008, Cicero et al. 2009)
 Global Burden: >128 countries reported M. bovis
clinical disease in cattle population, ≈ 50 million
cattle at risk globally (Michel et al. 2002, Chantal 2001).
 Transmission: Consumption of infected animal
products (milk) or inhalation of droplets.
 Zoonotic Challenges: Human-livestock-wildlife
interactions, HIV, high prevalence of b TB,
Pasteurization failures of milk, drug resistance
(PZA)
ZOONOTIC POTENTIAL OF MYCOBACTERIUM BOVIS
(CDC TB Factsheet, Cosivi et al.1998)
 To determine the prevalence of bTB by evaluating the presence of
granulomatous lesions in cattle at SABAN Abattoir, Kigali
 To identify different mycobacteria species that are responsible for
lesions resembling tuberculosis
 Evaluate the economic impact of bTB to the beef industry in
Rwanda.
RESEARCH QUESTION
 Lack of surveillance and Diagnosis in Rwanda : Underreporting and
underestimation of human TB caused by M. bovis.
 Lack of Prevalence data: on national-wide bovine tuberculosis in
cattle, All forms of human TB estimated at 91.3/10,000 pop/yr.
RESEARCH OBJECTIVES
MATERIALS AND METHODS
 Geographical Study Area: The study was carried out at SABAN-Nyabugogo abattoir in Kigali
on slaughtered animals from four Provinces (East, North, South and West) and Kigali city
(Jan-Nov 2009)
 Cross-sectional design: A stratified cluster sampling proportional to the size of the cattle
population
STUDY DESIGN : PATHOLOGY & LAB ANALYSIS
Lab analysis: Microbiological laboratory of Higher Institute of Agriculture and Animal
Husbandry (ISAE)
RESULTS: PATHOLOGICAL TUBERCULOUS LESIONS
ORGAN CONDEMNED COUNT PERCENTAGE (%)
Head 65 43.9
Lungs 19 12.8
Liver 50 33.8
Intestine 8 5.4
Kidney 2 1.3
Abomasum 1 0.6
Whole carcass 3 2.0
Total 148 100
 Overall prevalence of gross tuberculous lesions = 0.9%
RESULTS: PATHOLOGICAL TUBERCULOUS LESIONS
Liver and Mediastinal Lymphnodes with caseous necrotic tubercles
 The overall postmortem prevalence of M. bovis using culture was
estimated to be 0.5% (0.587*148/16753)
RESULTS:PREVALENCE OF BTB ACCORDING TO SEX
Slaughtered cattle
according to sex
Count Organ condemned Occurrence
(%)
Males 10 051 61 0.6
Females 6 702 87 1.4
Total 16 753 148 1.9
Females higher prevalence attributed to: (p < 0.05, n = 16 753)
Husbandry stress caused by poor housing and extended confinement
Higher vulnerability to infection due Lactation and gestation.
Prolonged contact with humans infected with TB during milking (Imtiaz et
al. 2008; Skuce, Allen & McDowell 2011).
RESULTS:PREVALENCE OF BTB ACCORDING TO AGE
Age differentials and prevalence attributed to:
Prolonged overall exposure increases exponentially with age.
Possibility of vertical transmission of infection(in-utero)
The macroscopic lesions appear at advanced stages of infection
(Awah-Ndukum et al.2012)
Slaughtered cattle
according to age
Number Organ condemned Occurrence
(%)
Less than 2 years 11 966 72 0.6
Over 2 years 4 787 76 1.6
Total 16 753 148 0.9
 Prevalence of test positives increased significantly with cattle age (p<0.001)
LABORATORY FINDINGS: MICROSCOPY
Cultures
(-)
Cultures
(+)
Total Percentage
(%)
Kinyoun(-) 8 2 10 27.8
Kinyoun(+) 5 21 26 72.2
Total 13 23 36 100
Percentage(%) 36.1 63.9 100 -
 The overall postmortem prevalence of M. bovis using culture was estimated to be
0.5% (0.587*148/16753)
 36 samples microscopically examined, 26 (72.2%) were positive to Kinyoun staining.
LABORATORY FINDINGS: BACTERIOLOGY
Condemned
organ
Positives
Cultures
Positive Results
Mycobacterium
bovis
Results for
atypical
mycobacteria
Number Percent
(%)
Number Percent
(%)
Lymphnodes 19 17 89.5 2 10.5
Lung 2 2 100 0 0
Liver 2 2 100 0 0
Total 23 21 91.3 2 8.7
 Mycobacterium bovis was present in 91.3% (n=36) of the samples vs.
8.7% (n=36) for atypical mycobacteria
ECONOMIC AND PUBLIC HEALTH IMAPCTS
 A total of 1 683.5 kg of meat was condemned and the loss was
estimated to 3 030 300Frw (USD 4810) based on the prevailing
meat market prices.
 Malnutrition: RDAI (6g of animal protein) translates into loss of
animal proteins for 345 persons per year.
 Value chain impacts: Decreases livestock productivity may be
economically devastating for the dairy sector. Milk yields and draft
power can be significantly reduced, with direct effects on the
livelihoods of poor livestock holders (WAHID 2012)
 Public health impacts at crossroads with opportunistic HIV/AIDS
infections.
 The prevalence of bTB in Rwanda is significant and requires continued
implementation of surveillance and control measures.
 Routine meat inspection protocols utilised in Rwandan abattoirs are able to detect
0.9% of bTB lesions at the gross level.
 A comparative sensitivity of tests: The sensitivity of Kinyoun staining compared to
culture was 91.3%, while the specificity was 61.5%.
 The molecular and epidemiological analysis of the M. bovis in Rwanda is necessary
to determine the clonal lineages from different provinces.
 Risk factor analysis for comparing with prevalence of cattle interdermal test positives
of cases.
 Studies are needed to assess the risk of zoonotic TB among populations in regions
where socio-cultural and economic factors increase the risk posed by this zoonosis.
DISCUSSION AND CONCLUSION
Habarugira et al., 2014
 Evaluation of Molecular diagnostics: Polymerase chain reaction for higher
sensisitivity and specificity of bTb genetic diversity detection.
 Molecular epidemiology: Determination of the Rwanda population structure and
description of the epidemiological units?
 The spoligotypes naming according to the M. bovis Spoligotype Database website
(www.mbovis.org ).
1. Ministry of Health 2009, Annual Report 2009
2. Cosivi O et al., 1998, Zoonotic tuberculosis due to Mycobacterium
bovis in developing countries. Emerging Infectious Diseases 4: 59-70
3. Gortázar C et al., 2008 : The Role of Wild Ungulates as Disease
Reservoirs in the Last Iberian Lynx Strongholds. PLoS ONE
4. Michel, A.L., 2002, ‘Implications of tuberculosis in African wildlife and
livestock’, Annals of the New York Academy of Sciences.
5. OIE, 2009, Manual of diagnostic tests and vaccines for terrestrial
animals: Bovine tuberculosis.
REFERENCES(SELECTED)
 University of Rwanda for providing funding for the research
 Dr. Anselme Achille Shyaka through his unconditional support, we
were able to overcome the difficult times that we had during this
study.
 Dr. Louis Fischer for his advice and support, both materially and
morally.
 Technicians of Saban Nyabugogo abattoir and laboratories of ISAE
Busogo who assisted respectively in samples collection and
laboratory analysis.
 The organizers of RCZEA and Audience for Kind Attention!
ACKNOWLEDGEMENTS

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Bovine tuberculosis prevalence and economic impact in Rwanda

  • 1. Bovine Tuberculosis in Rwanda: Prevalence and Economic Impact Evaluation by Meat Inspection at Société d’Abattoir de Nyabugogo-Nyabugogo Abattoir, Kigali Gervais Habarugira*1, Joseph Rukelibuga2, Mark Nanyingi3, 5 Borden Mushonga4 1School of Animal Sciences and Veterinary Medicine, College of Agriculture, Animal Sciences and Veterinary Sciences, University of Rwanda, Nyagatare, Rwanda. 2US-Centre for Disease Control and Prevention (CDC), Kigali, Rwanda. 3Department of Public Health, Pharmacology and Toxicology, University of Nairobi Nairobi, Kenya. 4Department of Livestock and Pasture Science, Faculty of Science and Agriculture, University of Fort Hare, South Africa. 5Kenya Medical Research Institute, United States Centres for Disease Control and Prevention, Kenya Corresponding Author: Gervais Habarugira gervaish@gmail.com * Presented at the Inaugural Regional conference on Zoonotic Diseases in Eastern Africa, Naivasha, Kenya on Tuesday, March 10th, 2015
  • 2.  Etiology: TB in humans is primarily caused by Mycobacterium tuberculosis (M. tb), it represents the greatest burden of infectious diseases second to AIDS worldwide.  Global incidence estimates : 8.7 million cases of & 1.4 million deaths/3,833 daily (WHO 2011)  Burden: 17 million Disability Adjusted Life Years (DALY), social impact underestimated.  Drug resistance: 480,000 people with MDR-TB  Rwanda prevalence estimates: human TB due to (M. tb) 0.08% in 2008 (MOH 2008). INTRODUCTION: GLOBAL ZOONOTIC TB BURDEN (WHO Annual TB report, 2011, WHO TB Factsheet 2014)
  • 3.  Pathogen host and species jump : Cattle is the main host of Mycobacterium bovis (M. bovis) and leads to latent infection in immunocompromised humans (LTBI)(Gortázar et al. 2008, Cicero et al. 2009)  Global Burden: >128 countries reported M. bovis clinical disease in cattle population, ≈ 50 million cattle at risk globally (Michel et al. 2002, Chantal 2001).  Transmission: Consumption of infected animal products (milk) or inhalation of droplets.  Zoonotic Challenges: Human-livestock-wildlife interactions, HIV, high prevalence of b TB, Pasteurization failures of milk, drug resistance (PZA) ZOONOTIC POTENTIAL OF MYCOBACTERIUM BOVIS (CDC TB Factsheet, Cosivi et al.1998)
  • 4.  To determine the prevalence of bTB by evaluating the presence of granulomatous lesions in cattle at SABAN Abattoir, Kigali  To identify different mycobacteria species that are responsible for lesions resembling tuberculosis  Evaluate the economic impact of bTB to the beef industry in Rwanda. RESEARCH QUESTION  Lack of surveillance and Diagnosis in Rwanda : Underreporting and underestimation of human TB caused by M. bovis.  Lack of Prevalence data: on national-wide bovine tuberculosis in cattle, All forms of human TB estimated at 91.3/10,000 pop/yr. RESEARCH OBJECTIVES
  • 5. MATERIALS AND METHODS  Geographical Study Area: The study was carried out at SABAN-Nyabugogo abattoir in Kigali on slaughtered animals from four Provinces (East, North, South and West) and Kigali city (Jan-Nov 2009)  Cross-sectional design: A stratified cluster sampling proportional to the size of the cattle population
  • 6. STUDY DESIGN : PATHOLOGY & LAB ANALYSIS Lab analysis: Microbiological laboratory of Higher Institute of Agriculture and Animal Husbandry (ISAE)
  • 7. RESULTS: PATHOLOGICAL TUBERCULOUS LESIONS ORGAN CONDEMNED COUNT PERCENTAGE (%) Head 65 43.9 Lungs 19 12.8 Liver 50 33.8 Intestine 8 5.4 Kidney 2 1.3 Abomasum 1 0.6 Whole carcass 3 2.0 Total 148 100  Overall prevalence of gross tuberculous lesions = 0.9%
  • 8. RESULTS: PATHOLOGICAL TUBERCULOUS LESIONS Liver and Mediastinal Lymphnodes with caseous necrotic tubercles  The overall postmortem prevalence of M. bovis using culture was estimated to be 0.5% (0.587*148/16753)
  • 9. RESULTS:PREVALENCE OF BTB ACCORDING TO SEX Slaughtered cattle according to sex Count Organ condemned Occurrence (%) Males 10 051 61 0.6 Females 6 702 87 1.4 Total 16 753 148 1.9 Females higher prevalence attributed to: (p < 0.05, n = 16 753) Husbandry stress caused by poor housing and extended confinement Higher vulnerability to infection due Lactation and gestation. Prolonged contact with humans infected with TB during milking (Imtiaz et al. 2008; Skuce, Allen & McDowell 2011).
  • 10. RESULTS:PREVALENCE OF BTB ACCORDING TO AGE Age differentials and prevalence attributed to: Prolonged overall exposure increases exponentially with age. Possibility of vertical transmission of infection(in-utero) The macroscopic lesions appear at advanced stages of infection (Awah-Ndukum et al.2012) Slaughtered cattle according to age Number Organ condemned Occurrence (%) Less than 2 years 11 966 72 0.6 Over 2 years 4 787 76 1.6 Total 16 753 148 0.9  Prevalence of test positives increased significantly with cattle age (p<0.001)
  • 11. LABORATORY FINDINGS: MICROSCOPY Cultures (-) Cultures (+) Total Percentage (%) Kinyoun(-) 8 2 10 27.8 Kinyoun(+) 5 21 26 72.2 Total 13 23 36 100 Percentage(%) 36.1 63.9 100 -  The overall postmortem prevalence of M. bovis using culture was estimated to be 0.5% (0.587*148/16753)  36 samples microscopically examined, 26 (72.2%) were positive to Kinyoun staining.
  • 12. LABORATORY FINDINGS: BACTERIOLOGY Condemned organ Positives Cultures Positive Results Mycobacterium bovis Results for atypical mycobacteria Number Percent (%) Number Percent (%) Lymphnodes 19 17 89.5 2 10.5 Lung 2 2 100 0 0 Liver 2 2 100 0 0 Total 23 21 91.3 2 8.7  Mycobacterium bovis was present in 91.3% (n=36) of the samples vs. 8.7% (n=36) for atypical mycobacteria
  • 13. ECONOMIC AND PUBLIC HEALTH IMAPCTS  A total of 1 683.5 kg of meat was condemned and the loss was estimated to 3 030 300Frw (USD 4810) based on the prevailing meat market prices.  Malnutrition: RDAI (6g of animal protein) translates into loss of animal proteins for 345 persons per year.  Value chain impacts: Decreases livestock productivity may be economically devastating for the dairy sector. Milk yields and draft power can be significantly reduced, with direct effects on the livelihoods of poor livestock holders (WAHID 2012)  Public health impacts at crossroads with opportunistic HIV/AIDS infections.
  • 14.  The prevalence of bTB in Rwanda is significant and requires continued implementation of surveillance and control measures.  Routine meat inspection protocols utilised in Rwandan abattoirs are able to detect 0.9% of bTB lesions at the gross level.  A comparative sensitivity of tests: The sensitivity of Kinyoun staining compared to culture was 91.3%, while the specificity was 61.5%.  The molecular and epidemiological analysis of the M. bovis in Rwanda is necessary to determine the clonal lineages from different provinces.  Risk factor analysis for comparing with prevalence of cattle interdermal test positives of cases.  Studies are needed to assess the risk of zoonotic TB among populations in regions where socio-cultural and economic factors increase the risk posed by this zoonosis. DISCUSSION AND CONCLUSION
  • 15. Habarugira et al., 2014  Evaluation of Molecular diagnostics: Polymerase chain reaction for higher sensisitivity and specificity of bTb genetic diversity detection.  Molecular epidemiology: Determination of the Rwanda population structure and description of the epidemiological units?  The spoligotypes naming according to the M. bovis Spoligotype Database website (www.mbovis.org ).
  • 16. 1. Ministry of Health 2009, Annual Report 2009 2. Cosivi O et al., 1998, Zoonotic tuberculosis due to Mycobacterium bovis in developing countries. Emerging Infectious Diseases 4: 59-70 3. Gortázar C et al., 2008 : The Role of Wild Ungulates as Disease Reservoirs in the Last Iberian Lynx Strongholds. PLoS ONE 4. Michel, A.L., 2002, ‘Implications of tuberculosis in African wildlife and livestock’, Annals of the New York Academy of Sciences. 5. OIE, 2009, Manual of diagnostic tests and vaccines for terrestrial animals: Bovine tuberculosis. REFERENCES(SELECTED)
  • 17.  University of Rwanda for providing funding for the research  Dr. Anselme Achille Shyaka through his unconditional support, we were able to overcome the difficult times that we had during this study.  Dr. Louis Fischer for his advice and support, both materially and morally.  Technicians of Saban Nyabugogo abattoir and laboratories of ISAE Busogo who assisted respectively in samples collection and laboratory analysis.  The organizers of RCZEA and Audience for Kind Attention! ACKNOWLEDGEMENTS