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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Date
2015-07
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Addis Abeba Universty
Abstract
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.
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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
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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
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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.
Description
Keywords
bovine/cattle, bovine tuberculosis, cough, households, human TB, lineage, North Gondar /Wollo, risk, skin test, Spoligotyp, tuberculosis, typing, Ethiopia