Epidemiological Study on the role of Cattle in the Occurrence of Pulmonary Tuberculosis in Humans in Rural Communities of Amhara Region, Ethiopia

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Addis Abeba Universty


Introduction: Tuberculosis is a major global public health problem resulting in considerable morbidity and mortality. According to 2012 World Health Organization report, an estimated 8.6 million people developed tuberculosis and1.3 million died from the disease (including 320 000 deaths among Human Immunodeficiency Virus (HIV) positive people). Ethiopia is one of the highest tuberculosis burden countries in the world, which ranks 8th amongst the 22 high tuberculosis burden countries. In Ethiopia, it was also estimated that about 41% of tuberculosis cases were HIV positive. The transmission of Mycobacterium tuberculosis from humans to humans is well known globally; however, little is known about the transmission of Mycobacterium tuberculosis complex species between humans and animals, in particular cattle. Bovine tuberculosis is endemic in Ethiopia. Intimacy of cattle and humans in rural farming communities may transmit Mycobacterium bovis to humans. However, there is little information about the possible transmission of tuberculosis between humans and cattle in Ethiopia. The contribution of Mycobacterium tuberculosis to bovine reactivity is also unknown. Although bovine tuberculosis is a known zoonosis, it is mainly a disease of cattle. Humans could be infected by consuming raw milk and, to some extent, by inhaling droplet nuclei. Cattle owned by tuberculosis patients revealed higher bovine tuberculosis tuberculin skin test result and this might be due to the possible infection of cattle with Mycobacterium tuberculosis. The causative agent responsible for the infection in both populations could be identified using molecular techniques. This research work aimed to investigate the role of cattle in the occurrence of pulmonary tuberculosis in humans at a rural community in Ethiopia. Methods: The study used both cross-sectional and case-control designs in Northeast and Northwest parts of the Amhara Region. A cross-sectional study was employed to determine the presence of bovine tuberculosis among cattle owned by presumptive pulmonary tuberculosis cases. A comparative cross-sectional study was conducted on 124 cattle owned by households with confirmed pulmonary tuberculosis and 381cattle owned by households without tuberculosis to determine the likelihood of bovine tuberculosis among livestock’s in the two groups. A casecontrol study was conducted on 35 households with at least one pulmonary tuberculosis case and 105 households without tuberculosis to determine the risk of bovine tuberculosis in humans. XIX Besides, laboratory based deletion typing and spoligotyping that was carried out for Mycobacterium tuberculosis isolated from acid fast bacilli confirmed pulmonary tuberculosis patients. A comparative cervical intradermal tuberculin skin test was conducted on all the study subjects (cattle) using bovine and avian purified protein derivatives as an antigen. Based on the skin test reaction measurement, the cattle were categorized as negative, doubtful and positive, if the measured difference between the bovine and avian injection site is below 1, 1- 4 and >4, or <1, 1-2 and >2, respectively. All sputum samples collected from presumptive tuberculosis cases as well as tuberculosis confirmed human patients were cultured on Lowenstein-Jensen medium (tubes containing glycerol and sodium pyruvate) and polymerase chain reaction, deletion typing, spoligotyping and single nucleotide polymorphism were performed for positive culture findings to identify the Mycobacterium tuberculosis strains involved for human tuberculosis infection. Closed questionnaires and forms were used to collect the required data. Results: Of the 124 sputum samples collected from presumptive tuberculosis cases 4/124 (3.2%) were culture positive. Polymerase Chain Reaction using region of difference-9 as a marker has confirmed that 2/4 (50%) were found to be Mycobacterium tuberculosis while the rest were atypical Mycobacterial species. Of the 381 cattle tested 5/381 (1.31%) were found to be tuberculin positive (prevalence of 1.31% with 95% CI: 0.2.0, 2.5) and 10/381 (2.63%) (Prevalence of 2.63% with 95% CI: 1.0, 4.2) were positive for the test according to a cutoff value > 4mms and > 2mms, respectively. About 67% (6/9) of the individuals who owned bovine tuberculosis positive cattle had the habit of drinking raw milk. Of the 10 positive cattle, five of them resided in lowland (Kola) areas (1300-1500 meters above sea level). However, none of the owners of tuberculin positive cattle were found to be tuberculosis positive. Using >2mm as a cutoff value for the diagnosis of bovine tuberculosis, the study revealed that an overall apparent prevalence of 23.6% and individual cattle apparent prevalence of 8.7% for bovine tuberculosis in the study area with an odds of nearly three times (AOR= 2.90, 95% CI: 1.50, 5.54) higher bovine tuberculosis among cattle owned by households with tuberculosis. The findings indicated that 49.3% and 61.4% were having the habit of drinking raw milk and eating XX uncooked meat, respectively. More than three fourth of the study subjects did not know the benefit of boiling milk. About 70.7% knew there is chance of disease transmission from animals to humans. Of the total respondents participated in a case - control study, 78.6% did not isolate their sick cattle and 87.1% kept the sick cattle with them. Among the TB cases, 31.4% reported sharing the living room with their cattle as compared to only 9% of controls. It was also disclosed that 42.9%, 37.1% and 14.3% of the cases shared utensils, gave their urine to cattle and urinate on a cattle feed, respectively, as compared to 36.2%, 27.6% and 4.8% of the controls. Based on >2mms as a cutoff value bovine tuberculosis was recorded in 48.6% of the cases and 15.2% of controls, more than 8 times higher for cases (AOR=8.32, 95% CI; 2.82, 24.60). In total, 70 acid fast bacilli positive sputum samples were collected in the study areas. The age of subjects ranged from 18 to 63 years with a mean age of 35.7 + 13.24 years. Of the total 70 acid fast bacilli positive sputum samples, 50/70 (71.4%) were culture positive, from which 37.1 and 31.5% had the habit of drinking unboiled milk and eating uncooked meat, respectively. Using deletion typing all the isolates were identified as Mycobacterium tuberculosis. Spoligotyping revealed 94% (47/50) interpretable patterns and three lineages namely; East- Africa-Indian (57.4%), Euro-American-African (38.3%) and Ethiopian (lineage-7) 2/50 (4.3%). Lineage 7 was registered only in North Wollo Zone. In this study 8 clusters (with cluster size ranging from 2 to 8), 8 unique and 10 new patterns were recorded. Shared International Types (SIT) (21, 25, 26, 35, 53, 109, 149 and 289) were found as clusters among which SIT 25 (7) and SIT 289 (8) were the predominant ones. Conclusion: About 3.2% (4/124) of sputum samples collected from individuals with chronic cough were culture positive, of whom 50% (2/4) were found to be Mycobacterium tuberculosis by polymerase chain reaction. The findings indicate that bovine tuberculosis is a threat in Ethiopia and implicated possible transmission of tuberculosis between humans and cattle where human pulmonary tuberculosis cases could serve as a possible source of Mycobacterium tuberculosis infection to cattle. House sharing was found as a contributing factor in bovine XXI tuberculosis test reaction. Therefore, mechanisms should be developed to create awareness. Separate houses for cattle should be constructed to minimize the risk of cross infections and further study regarding the possible infection of cattle with Mycobacterium tuberculosis thus recommended. Similarly, households with bovine tuberculosis had a higher chance of getting pulmonary tuberculosis. It is, therefore, necessary to investigate whether the pathogen responsible is Mycobacterium tuberculosis or Mycobacterium bovis and appropriate measures should be taken to prevent spread of tuberculosis in both humans and livestock. This study also revealed that 3 Mycobacterium tuberculosis lineages, namely; the ancient, intermediate and modern were identified. Besides, considerable clustering, which indicates current tuberculosis transmission was also reported in the study areas. Key words: bovine/cattle, bovine tuberculosis, cough, households, human TB, lineage, North Gondar /Wollo, risk, skin test, Spoligotyp, tuberculosis, typing, Ethiopia.



bovine/cattle, bovine tuberculosis, cough, households, human TB, lineage, North Gondar /Wollo, risk, skin test, Spoligotyp, tuberculosis, typing, Ethiopia