Content uploaded by Flora Davies-Bolorunduro
Author content
All content in this area was uploaded by Flora Davies-Bolorunduro on Jun 30, 2020
Content may be subject to copyright.
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
Prevalence of Rifampicin Resistance among Presumptive Pulmonary
Tuberculosis Patients within Lagos and its Environs in South-Western Nigeria
Davies-Bolorunduro O.F.
1*
, Nduaga S.J.
1
, Abiodun A.T
1
., Amuda, B.O., Osuolale,
K.A.
2
, Atoe K. and Cadmus S.
1,3
.
1
Center for Tuberculosis Research (CTBR), Department of Microbiology, Nigerian Institute
of Medical Research (NIMR), Yaba, Lagos State.
2
Monitoring and Evaluation Unit (Biostatistics), Nigerian Institute of Medical Research
(NIMR), Yaba, Lagos State.
3
Department of Veterinary Public Health & Preventive Medicine, University of Ibadan,
Ibadan, Oyo State, Nigeria.
Corresponding author: of.davies-bolorunduro@nimr.gov.ng, bizdave1@gmail.com:
+2348068964292
Abstract: Drug resistance (DR) is a major global health concern and currently implicated in fuelling the
burden of multi-drug resistant tuberculosis (MDR-TB) in Nigeria. Overall, DR poses serious public health
threat to TB control programmes particularly in TB endemic countries with limited resources. However,
early and rapid detection of rifampicin resistance (RR), a surrogate marker for MDR-TB is important to
reduce treatment period and transmission; with the overall goal of reducing the burden of the disease. The
study successfully determined the prevalence of RR Mycobacterium tuberculosis (MTB) among
presumptive pulmonary TB patients in Lagos and its environs. A retrospective study involving 1,453 TB
patients was conducted using data extracted from the clinical register of presumptive TB patients screened
for MTB and RR-TB using Xpert MTB/RIF assay at the Centre for Tuberculosis Research, Nigerian
Institute of Medical Research (NIMR) between January, 2018 and August, 2019. The data was analysed
using Statistical Package for Social Sciences (SPSS) version 23. Result shows that the overall prevalence
of TB was 15.3% (222/1453). MTB infection was detected in 79 locations out of which eight had a high
prevalence (15.7%-26.1%) of the disease. Notably, from the patients, RR-TB was 5.9% (13/222) among all
TB confirmed cases, with four (30.8%) being females and those infected ranging from 22 to 75 years
(34.85±15.01) years; with one person (male) being co-infected with HIV. This study highlights the
prevalence of 5.9% rifampicin-resistance among pulmonary TB patients in the urban and peri-urban areas
of Lagos, South-Western Nigeria.
Keywords: Prevalence, Rifampicin-resistance, Mycobacterium tuberculosis, GeneXpert.
INTRODUCTION
he emergence and transmission of
multidrug-resistant tuberculosis
(MDR-TB) has over the years posed
a great challenge to global health; thereby
complicating diagnosis, treatment and
control of TB (WHO/IUATLD, 2008). The
Global TB Report of 2016 estimated newly
diagnosed and previously treated TB cases
with MDR-TB at 3.9% and 21%
respectively. In 2015, approximately
580,000 TB cases were resistant to at least
rifampicin (RR-TB) globally and 480,000 of
the population were resistant to both
rifampicin and isoniazid (MDR-TB) with
250,000 deaths occurring due to MDR-
TB/RR-TB in the same year. (WHO, 2015).
On the average, 4.1% of newly diagnosed
and 19% previously treated TB patients are
estimated to be infected with MDR-TB
worldwide in 2017 (WHO, 2017). Treatment
of TB (Self-medication) without proper
diagnosis and drug susceptibility testing
which is a common practice in developing
countries has increased the transmission of
drug resistant (DR) strains (Arega et al.,
2019). Drug resistant-TB is a major cause of
concern globally, and currently implicated in
fuelling the burden of TB in Nigeria.
Overall, this poses serious public health
threat to TB control programmes particularly
in TB endemic countries with limited
resources. The low sensitivity and time-
consuming nature of conventional diagnostic
techniques such as direct microscopy and
culture increase the need for more efficient
diagnostic methods (Onyedum, 2017).
Although culture and drug susceptibility
testing are gold standards for diagnosis, they
are time consuming.
T
5188
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
Therefore, newer and more rapid methods of
diagnosis of rifampicin resistance (RR)
using molecular techniques such as Gene-
Xpert assay has been adopted for use
(Prasad et al., 2018). This is important to
reduce treatment period and transmission;
consequently decreasing the burden of the
disease.
The World Health Organisation (WHO)
endorsed the Xpert MTB/RIF assay, which
is a rapid and automated molecular system
that detects both M. tuberculosis DNA and
rifampicin-resistance (RR) associated
mutations simultaneously. Research
recognized that RR can be a surrogate
marker for MDR-TB in more than 90% of
the cases (Riordan et al., 2008). Hence,
WHO recommends that RR-TB patients
should be treated like patients with MDR-
TB (WHO, 2016). Initially, this method was
indicated for patients with TB/HIV co-
infection, presumptive MDR-TB and
paediatric TB patients (WHO, 2011).
However, three years after its
implementation, it was recommended for all
TB suspected patients (WHO, 2016).
Notably till date, there are few reports of
RR-TB prevalence study among pulmonary
TB patients in Nigeria. Recent studies by
Audu et al. (2017) reported RR-TB
prevalence of 12.1% in all TB diagnosed
patients in Nassarawa State while Adejumo
et al. (2018) reported a higher prevalence of
22.5% among newly diagnosed TB patients
in Lagos State.
Lagos State had a population of 17.5 million
in 2006 and this grew to 24.0 million in
2016 (Lagos State
Government, 2016). Despite its status as a
sub-national entity, its demography is as
important
as that of a country, for example a Local
Government Area (LGA) in the State
has more population than a country such as
Botswana (Lagos State
Government, 2016; UNDP, 2020). Due to
this huge population, transmission of RR-TB
poses more serious public health concerns
particularly within the densely populated
settings in the city and the adjoining towns.
Given the epidemiological dynamics and
risk factors involved in the spread of
RR/MDR-TB, there is the need to
understand the level of prevalence of RR-TB
in such settings in order to improve effective
monitoring of patients’ treatment as a
preventive measure to check the emergence
of DR-TB. This study therefore determined
the prevalence of RR Mycobacterium
tuberculosis (MTB) among presumptive
pulmonary TB patients in Lagos and its
environs and the associated risk factors.
MATERIALS AND METHODS
Study design
A retrospective review of presumptive TB
register of patients screened for MTB and
RR-TB using Xpert MTB/RIF assay at the
Center for Tuberculosis Research
Laboratory, NIMR was conducted between
January, 2018 and August, 2019. The study
population was presumptive TB patients
(patients with clinical signs and symptoms
suggestive of TB) who reported at the DOTS
centers during the period of study.
Laboratory investigation and data
collection
A single sputum sample per patient for age
greater than six years and a gastric aspirate
sample in case of children less than this age
group were used in the study for the
diagnosis of all presumptive TB patients
using Xpert MTB/RIF assay. Samples were
collected a wide mouth, dry and sterile
container, given to patients. Samples were
processed by GeneXpert MTB/ RIF assay.
Sample processing including dilution,
decontamination and GeneXpert MTB/RIF
assay were carried out as earlier reported
(Adejumo et al., 2018) following the
manufacturer’s instructions. Patients’ with
incomplete data set e.g., age, gender, Xpert
MTB/RIF results, HIV status, sample type,
and location were excluded from the study.
Data analysis
Statistical Package for Social Sciences
(SPSS) IBM version 23 was used for data
analysis. Measured variables were presented
using descriptive statistics such as
percentages, mean and standard deviation.
5189
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
Categorical variables were compared using
chi-squared test. Mycobacterium
tuberculosis (MTB) detection and rifampicin
resistance were the outcome variables.
Adjusted odds ratio of associated factors of
the outcome variable (age, gender, HIV
status) were determined. Confidence interval
was estimated at 95% level of significance
and p <0.05 was considered significant for
all statistical tests.
Ethical Consideration
Ethical approval for the study was obtained
from the Institutional Review Board (IRB)
of the Nigerian Institute of Medical
Research (IRB/19/053: 09/10/2019).
Confidentiality of information was
maintained by de-identifying data retrieved
from the registers.
RESULTS
Overall, 1723 presumptive TB patients
submitted samples for TB diagnosis,
however 1453 (84.3%) had complete data
and were included in the study. Out of 1453
patients, 707 (48.6%) were males while 746
(51.3%) were females.
Figure 1. Map of Nigeria showing Lagos State and the affected areas in Lagos State and
its environs (Geographical Information System, GIS).
The overall prevalence of TB in the study
area was 15.3% with 222 of the 1453
patients being positive for M. tuberculosis.
Out of the 222 MTB-positive patients, 136
(61.3%) were male while 86 (38.7%) were
females. There was however significant
relationship between TB and gender (Score
test: χ
2
(1) = 16.752, p < 0.001). The odds of
detecting TB were 0.55 times lower for
gender (OR 0.547, CI 0.408– 0.733, p <
0.001). The ages of the adult population
infected ranged between 16 to 85 years with
a prevalence of 99.1%. There was however
no significant relationship between TB and
age (Score test: χ2 (1) = 2.981, p > 0.05).
The odds of detecting TB were 0.99 times
lower for age as a predictor variable (OR
0.992, CI 0.983 – 1.001, p > 0.05).
Importantly, the HIV prevalence of the study
population was 29.9% while the prevalence
of HIV among the study population infected
with MTB was 19.4%.
5190
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
There was significant association between
HIV status and TB (Score test: χ
2
(2) =
34.042, p < 0.001). The odds of detecting
TB were 1.33 times higher for HIV status as
a predictor variable (OR 1.329, CI 0.929 –
1.902, p < 0.01). A prevalence of 13/222
(5.9%) was recorded for RR-TB patients
was recorded among the earlier confirmed
TB cases (Table 1). Out of the 13 cases, 4
(30.8%) were females while 9 (69.2%) were
males. The ages of the affected population
ranged between 22 to 75 years
(34.85±15.01) while one person (male) was
HIV positive.
Table 1. Prevalence of TB and Rifampicin Resistance among the Sample Population
X-pert MTB/RIF Assay Number
(n)
Percentage (%) LR Test OR for TB
Detected
95% CI
for OR
MTB DETECTED
(Gender)
Male 136 61.3 χ
2
(1)
=16.752, p <
0.001
0.547 0.408 –
0.733
Female 86 38.7
Total 222 100
MTB NOT DETECTED
(Gender)
Male 571 46.4
Female
659
53.5
Total 1231 100
MTB DETECTED
(HIV Status)
N 130 58.6
P 43 19.4 χ
2
(2) =
34.042, p <
0.001
1.329
0.929 –
1.902
U 49 22.1
Total 222 100
MTB NOT DETECTED
(HIV Status)
N 559 45.4
P 392 31.8
U 280 22.7
Total 1231 100
MTB DETECTED (Age
Group)
0
-
15
2
0.9
16-85 220 99.1 χ2(1) = 2.981
p > 0.05
0.992 0.983 –
1.001
Total
222
100
MTB NOT DETECTED
(Age Group)
0
-
15
117
9.5
16-85 1112 90.3
Total 1229 99.8
MTB DETECTED
(Rifampicin Resistance)
Positive 13 5.9
Indeterminate 2 0.01
Negative
207
93.2
Total 222 100
Key: N- Negative, P-Positive, U- Unknown
5191
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
MTB infection was detected in 79 locations out of which 8 locations had a high prevalence
(15.7% - 26.1%) of the disease. The prevalence of MTB was highest within the sample
population who reside in Ibafo (26.1%) followed by residents of Yaba (22.7%) (Figure 2).
However, RR-TB was detected in 12 locations and the prevalence of RR-TB was highest
within the sample population who reside Surulere, recording the highest prevalence at
15.38%. (Figure 3).
19
965
11
16 16
10
88
53
23 23
70 73
98
44
21.60%
17%
26.10%
21.70%
15.70%
21.90%
16.30%
22.70%
0.00%
5.00%
10.00%
15.00%
20.00%
25.00%
30.00%
0
20
40
60
80
100
120
BARIGA EBUTTE
METTA
IBAFO IJESHA IKORODU MUSHIN SURULERE YABA
MTB DETECTED
TOTAL
PREVALENCE (%)
7.69% 7.69% 7.69% 7.69% 7.69% 7.69% 7.69% 7.69%
15.38%
7.69%
7.69% 7.69%
0.00%
2.00%
4.00%
6.00%
8.00%
10.00%
12.00%
14.00%
16.00%
18.00%
0
0.5
1
1.5
2
2.5
SATELLITE
TOWN
IKATE AKUTE LAGOS
ISLAND
EGBE IYANA IPAJA BERGER MUSHIN SURULERE EBUTTE
METTA
YABA IWAYA
Mtb and Rif Resistance Dectected Prevelence (%)
Figure 2. Prevalence of MTB per Location/Residence of Sample Population
*
Locations with MTB detection less than 5 cases were excluded
Figure 3. Prevalence of MTB and Rif Resistance per Location/Residence of Sample
Population
5192
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
DISCUSSION
Drug-resistant TB continues to pose a
serious public health challenge not only in
Nigeria but globally despite various TB
control programmes and available anti-
tuberculosis drugs. Hence there is a need for
rapid laboratory TB diagnosis to enable
early commencement of treatment so as to
limit transmission (Atashi et al., 2017). This
study was designed to determine the
prevalence of M. tuberculosis and rifampicin
resistance in new cases of TB in a TB
reference laboratory in Lagos. Findings from
this study reveal that 15.3% of the patients
were positive for TB. This was higher than
the 15.1% prevalence reported in a study
conducted in Ethiopia (Arega et al 2019) but
lower than those reported in previous studies
conducted in Southern and Northern (Egbe
et al., 2016; Adejumo et al., 2018; Ikuabe
and Ebuenyi, 2018). The variations in
prevalence may be attributed to differences
such as study design, sample size as well as
methodology adopted. In this study, the
highest TB prevalence was in Ibafo (26.1%)
(Figure 2). Ibafo is a major surburb in Ogun
State, South-Western Nigeria. Many people
who work in Lagos live in the communities
in the outskirts of the city. This is of concern
because of ease of transmission through
daily commuting in confined mass transit
vehicles. Also, DR could be easily acquired
in such settings given the overcrowdiness
and congested living structure that could
facilitate transmission of the disease from
infected to healthy people resulting from
delayed treatment of those who have
developed DR. In this study, more males
(61.3%) were infected than females (38.7%).
Similar trend has also been reported in
previous studies in Nigeria and other African
countries (Nyamogoba et al., 2012; Egbe et
al. 2016; Fadeyi et al 2017; Arega et al
2019).
The prevalence of HIV and TB co-infection
in this study was 19.4%. Our result is higher
than previous reports of 12.0% in Southern
Nigeria (Onipede et al 1999), 10.0% in
Northern Nigeria (Iliyasu and Babashami,
2000), 11.6% in Jamaica (Akpaka et al.
2006) and 11.4 % in Ethiopia (Tadesse and
Tadesse, 2013). These strong relationship
between HIV and TB infection has since
been established from previous reports. The
treatment of both diseases using drug
cocktails is typically fraught with challenges
that can lead to treatment failure and thus
development of drug resistance. The
breakdown of immune system and other
gastrointestinal opportunistic infections from
malabsorption, may also lead to reduced
absorption of anti-TB medications, which
may further contribute to drug resistance,
especially rifampicin (Audu et al., 2017).
Resistance to rifampicin is usually a marker
for MDR-TB, hence almost 90% of
rifampicin-resistant strains are also resistant
to isoniazid (Atashi et al., 2017). In this
study, the overall prevalence of RR-TB was
5.9% among the TB confirmed cases. This is
higher than the 4.2% reported by Fadeyi et
al. (2017) in a study conducted in North-
Western Nigeria and 2.2% reported by
Idigbe et al. (1998). The higher prevalence
in this study may be due to study setting.
This is because the Center for Tuberculosis
Research is a National TB reference
laboratory where most presumptive DR-TB
patients are referred from other hospitals in
Lagos State for Xpert MTB/RIF test. In this
study, the prevalence of RR-TB was higher
in males (69.2%) than females (30.8%). This
is similar to previous reports in Nigeria and
South Africa (Coovadia et al., 2013;
Adejumo et al., 2018). This may be
attributed to lifestyle, social habits as well as
level of exposure to infection. Surulere had
the highest prevalence of RR-TB at 15.38%
(2/13) (Figure 3). Its dense population which
was estimated at 64,554/ Sq Km
in 2016 (Lagos State Government, 2016) is
higher than that of Lagos
State, Nigeria and Sub-Saharan Africa. This
could impact negatively on the person-to-
person air exchange necessary for
transmission due to crowding and limited
ventilation hence increasing rate of
transmission (Barun-Mathema et al., 2017).
5193
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
CONCLUSION
Drug resistance is a major cause of public
health concern apparently fuelling the TB
burden in Nigeria. Drug resistance could be
easily acquired due to living in an
environment with high prevalence of drug
resistance disease. The findings in this study
emphasized the importance of drug
susceptibility testing in TB management.
Consequently, proactive measures are
therefore urgently needed to address the
issues of prompt diagnosis and early
commencement of treatment to reduce the
spread of DR-TB in the community. In
conclusion, we therefore advocate for the
institution of routine TB surveillance
through the use of rapid diagnostic tools
such as Gene Xpert for early detection and
effective treatment management. Since
prevalence of RR-TB indicative of a major
public health challenge, we advocate for
improved and prompt diagnosis, as well as
effective monitoring of patients’ treatment to
prevent further emergence and spread of
drug resistant tuberculosis in the country.
REFERENCES
Adejumo O.A, Olusola-Faleye B., Adepoju
V, Bowale A., Adesola V, Falana A,
Owuna H, Otemuyiwa K., Oladega
S. and Adegboye O. (2018).
Prevalence of rifampicin resistant
tuberculosis and associated factors
among presumptive tuberculosis
patients in a secondary referral
hospital in Lagos Nigeria. African
Health Sciences, 18(3): 472-478.
Akpaka, P. E. Tulloch-Reid, M., Justiz-
Vaillant, A. and Smikle, M. F.
(2006). Prevalence of human
immunodeficiency virus infection in
patients with pulmonary tuberculosis
at the National Chest Hospital in
Jamaica, Rev Panam Salud Publ, 19:
38–43.
Arega B., Menbere F. and Getachew Y.
(2019). Prevalence of rifampicin
resistant Mycobacterium tuberculosis
among presumptive tuberculosis
patients in selected governmental
hospitals in Addis Ababa, Ethiopia.
BMC Infectious Diseases, 19:307.
https://doi.org/10.1186/s12879-019-
3943-1
Atashi, S., Izadi, B., Jalilian, S., Madani,
S.H., Farahani, A. and Mohajeri, P.
(2017). Evaluation of GeneXpert
MTB/RIF for determination of
rifampicin resistance among new
tuberculosis cases in west and
northwest Iran. New Microbes and
New Infections, 19:117-120.
Audu E.S, Gambo M.S, Yakubu A.A.
(2017). Rifampicin resistant
Mycobacterium tuberculosis in
Nasarawa State, Nigeria. Niger J
Basic Clin Sci., 14:21–5.
Barun Mathema, Jason R Andrews, Ted
Cohen, Martien W Borgdorff, Marcel
Behr, Judith R Glynn, Roxana
Rustomjee, Benjamin J Silk, Robin
Wood, Drivers of Tuberculosis
Transmission, The Journal of
Infectious Diseases, 216:(6) 644–
653, https://doi.org/10.1093/infdis/ji
x354
Boehme C.C, Nabeta P., Hillemann D.,
Nicol M.P., Shenai S., Krapp F. et al.
(2010). Rapid molecular detection of
tuberculosis and rifampin resistance.
N Engl J Med., 363:1005-1015
Coovadia Y.M., Mahomed S., Pillay M.,
Werner L., Mlisana K. (2013).
Rifampicin Mono Resistance in
Mycobacterium tuberculosis in
Kwazulu Natal, South Africa: A
significant phenomenon in high
prevalence TB/HIV Region. PLos
One.,8:77712.
Dereje A.G., Yoseph C.M., Adugua N.G.,
Gizachew T.A, Melaku T.D, Kassu
D.T. (2015). Xpert MTB/RIF assay
for diagnosis of pulmonary
tuberculosis in sputum specimens in
Remote healthcare facilities. BMC
Microbiol.,15: 220. doi:
10.1186/s12866-015-0566-6
5194
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
Egbe K, Ike A.C., Aleruchi C. (2016).
Prevalence of tuberculosis and
rifampicin resistance among patients
seeking medical care in Nasarawa
State, North Central Nigeria. Science
Journal of Public Health.4:3, 214-
218. doi:
10.11648/j.sjph.20160403.18
Fadeyi A., Desalu O.O, Ugwuoke C.,
Opanwa O.A, Nwabuisi C., Salami
A.K. (2017). Prevalence of
rifampicin-resistant tuberculosis
among patients previously treated for
pulmonary tuberculosis in North-
Western, Nigeria. Nig Med J,
58:161-6
Gyar, S. D., Dauda, E. and Reuben, C. R.
(2014). Prevalence of tuberculosis in
HIV/AIDS patients in Lafia, central
Nigeria. Int J Curr Microbiol Appl
Sc, 3: 831-838.
Huang W.L, Chen H.Y, Kuo Y.M, Jou R.
(2009). Performance assessment of
the GenoType MTBDRplus test and
DNA sequencing in detection of
multidrug-resistant Mycobacterium
tuberculosis. J Clin Microbiol.,
47(8): 2520-4.
Ibrahim, K. O. O. Akanni, and U. J. Ijah,
(2004). The prevalence of
tuberculosis in HIV patients in
Minna metropolis, Nig J Microbiol,
vol. 18: 212-216.
Idigbe O, Sofola T, Akinosho R,
Onwujekwe D, Odiah F. (1998).
Initial drug resistance tuberculosis
amongst HIV seropositive and sero-
negative prison inmates in Lagos,
Nigeria. Int Conf AIDS, 12:137.
Ikuabe P.O. and Ebuenyi I.D., (2018).
Prevalence of rifampicin resistance
by automated Genexpert rifampicin
assay in patients with pulmonary
tuberculosis in Yenagoa, Nigeria.
The Pan African Medical Journal;
28:204
Iliyasu, Z. and Babashani, M. (2009).
Prevalence and Predictors of TB
coinfection Among HIV seropositive
patients attending Aminu Kano
Teaching Hospital, Northern Nigeria,
J. Epid,. 2: 81-87.
Lagos State Government. (2016). Abstract
of Local Government Statistics.
<https://mepb.lagosstate.gov.ng/wp-
content/uploads/sites/29/2017/01/AB
STRACT
-OF-LOCAL-GOVERNMENT-
STATISTICS-2016.pdf
Narasimooloo R, and Ross A. (2012). Delay
in commencing treatment for MDR
TB at a specialised TB treatment
centre in KwaZulu-Natal. S Afr Med
J., 102:360- 362.
Nyamogoba, H. D. N., Mbuthia, G., Kikuvi,
G. Mpoke, S. and Waiyaki P. G.
(2012). A high tuberculosis and
human immunodeficiency virus co-
infection rate and clinical
significance of non-tuberculous
mycobacteria in Western Kenya, Afr
J Health Sc, Vol. 21: 147-154.
Onipede, A. O. , Idigbe, O., Ako-Nai, A. K.,
Omojola, O., Oyelese, A. O.,
Aboderin, A. O., Komolafe, A. O.
and Wemambu, S. N. C. (1999).
Seroprevalence of HIV antibodies in
TB patients in Ile-Ife, Afr Med J, 76:
127-132.
Onyedum CC, Alobu I, Ukwaja KN (2017)
Prevalence of drug-resistant
tuberculosis in Nigeria: A systematic
review and meta-analysis. PLoS
ONE 12(7): e0180996.
https://doi.org/10.1371/journal.pone.
0180996
Prasad, R., Gupta, N., & Banka, A. (2018).
Multidrug-resistant
tuberculosis/rifampicin-resistant
tuberculosis: Principles of
management. Lung India : official
organ of Indian Chest Society, 35(1),
78–81.
https://doi.org/10.4103/lungindia.lun
gindia_98_17.
Tadesse, S. and Tadesse, T. (2013). HIV co-
infection among tuberculosis patients
in Dabat, northwest Ethiopia, J Infect
Dis Immun, 5:29-32.
5195
Nigerian Journal of Microbiology 2020
Available online at www.nsmjournal.org
Davies-Bolorunduro et al., 2020 Nigerian Journal of Microbiology, 34(1): - 5188 - 5196
United Nations Development Programme
(UNDP) 2020. Retrieved 2020-06-
14, from
<http://hdr.undp.org/en/countries/pro
files/BWA>
VanRie A, Page-Ship L, Scott L, Sanne I,
Stevens W. (2010). Xpert MTB/ RIF
for point-of-care diagnosis of
tuberculosis in high HIV burden,
resource-limited countries; Hype or
hope. Expert Rev Mol Diagn., 10:
937-946.
World Health Organization Global
Tuberculosis Report (2016).
WHO/HTM/2016.13. Geneva:
WHO. Available from
www.who.int/tb/publications/
global_report/en/
WHO. Global Tuberculosis Report (2017).
Available from www.who.int
WHO/IUATLD. Global Project on Anti-
tuberculosis Drug Resistance
Surveillance. (2008). Anti-
Tuberculosis Drug Resistance in the
World. Geneva: WHO
5196
