Research | Volume 38, Article 203, 23 Feb 2021 | 10.11604/pamj.2021.38.203.19034

Prevalence of rifampicin resistance tuberculosis among HIV/TB coinfected patients in Benue State, Nigeria

Francis Enenche Ejeh, Ann Undiandeye, Kenneth Okon, Kazeen Haruna Moshood

Corresponding author: Francis Enenche Ejeh, Department of Veterinary Microbiology, University of Maiduguri, Maiduguri, Nigeria

Received: 05 May 2019 - Accepted: 19 Jan 2020 - Published: 23 Feb 2021

Domain: Infectious diseases epidemiology

Keywords: Microbiology, drug resistance, infection control

©Francis Enenche Ejeh et al. Pan African Medical Journal (ISSN: 1937-8688). This is an Open Access article distributed under the terms of the Creative Commons Attribution International 4.0 License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Cite this article: Francis Enenche Ejeh et al. Prevalence of rifampicin resistance tuberculosis among HIV/TB coinfected patients in Benue State, Nigeria. Pan African Medical Journal. 2021;38:203. [doi: 10.11604/pamj.2021.38.203.19034]

Available online at: https://www.panafrican-med-journal.com/content/article/38/203/full

Home | Volume 38 | Article number 203

Research

Prevalence of rifampicin resistance tuberculosis among HIV/TB coinfected patients in Benue State, Nigeria

Prevalence of rifampicin resistance tuberculosis among HIV/TB coinfected patients in Benue State, Nigeria

Francis Enenche Ejeh1,&, Ann Undiandeye2, Kenneth Okon3, Kazeem Haruna Moshood 4

 

1Department of Veterinary Microbiology, University of Maiduguri, Maiduguri, Nigeria, 2Federal Medical Center, Yola, Adamawa State, Nigeria, 3Department of Medical Microbiology, Federal Medical Centre, Makurdi, Nigeria, 4Department of Veterinary Microbiology, Ahmadu Bello University, Zaria, Nigeria

 

 

&Corresponding author
Francis Enenche Ejeh, Department of Veterinary Microbiology, University of Maiduguri, Maiduguri, Nigeria

 

 

Abstract

Introduction: the emergence of HIV/TB co-infection has changed the global health landscape globally, particularly in sub-Saharan Africa and Asia with high prevalence rate. It has further worsened and compound patient diagnosis, treatment/management approach and infection control. Rifampicin resistance TB (RR-TB) is a good indicator of treatment failure and infection control in the community. This study determines the prevalence of RR-TB among HIV/TB coinfected patients in Benue state, Nigeria.

 

Methods: the case-control study was carried out at Federal Medical Centre, Makurdi and General Hospital, Otupko, between January 2017 and February 2018. One thousand and ten suspected tuberculosis and HIV patients were enrolled in the study, diagnosed according to WHO guidelines. Sputum samples were collected and then analyzed by acid-fast bacilli smear test and GeneXpert MTB/RIF assay.

 

Results: overall prevalence of tuberculosis by acid-fast test was 74 (7.3%), 171 (16.93%) by GeneXpert assay and 2.18% by RR-TB test respectively. Significant difference was observed between the detection technique and demographic variables, high prevalence among urban patient compared to rural (8.85%vs 5.40%; Χ²= 4.38; P = 0.036) and ethnic background of the patients (Χ²= 23.21; P = 0.000) by acid fast test. With GeneXpert, high prevalence recorded among patient within age-group15-45years (Χ²= 8.01; P = 0.046) and ethnic group (Χ²= 6.30; P = 0.044). The occurrence of HIV/TB coinfection was less associated with Idoma ethnic group (COR; 0.440; 95% C.I; 0.246 0.786).

 

Conclusion: The relatively high prevalence of HIV/TB co-infection and RR-TB is a tremendous public health threat, considering society's attendant implication. Further surveillance studies are needed to evaluate the situation in Benue state better.

 

 

Introduction    Down

Mycobacterium tuberculosis (M. tuberculosis) is a member of the group Mycobacterium tuberculosis complex (MTBC), the causative agent of tuberculosis (TB) in humans and animals [1-3]. TB and HIV comorbidity of high mortality rate in Sub-Saharan Africa. .The emergence of drug-resistant TB, such as multidrug-resistant (MDR) and extensively drug-resistant (XDR) TB, is the hindering factors militating against the effective control of TB worldwide [4]. The World Health Organization recommends continuous surveillance and documentation of TB and rifampicin resistance tuberculosis (RR-TB) prevalence among high-risk populations. TB is ranked above HIV/AIDS as the leading cause of death, rendering it an alarming public health issue globally. Globally, about 9 million new cases and 1.5 million deaths have resulted from TB annually [4]. The majority of new TB cases and TB elicited fatalities occur in developing countries, such as Nigeria [5, 6]. The emergence of HIV/AIDS pandemic is a major contributing factor in the global increase of TB incidence [7], particularly among more impoverished populations. Nigeria has an estimated national adult HIV prevalence of 3.6% [8], with 3.3 million people living with HIV and represent the second-highest burden of HIV in Africa. Benue State is at high risk for TB burden in Nigeria due to its high prevalence of HIV/AIDS (12.7%) state [8]. Additionally, it has been reported that there is a strong relationship between drug resistance TB and HIV/AIDS in Nigeria [9, 10].

Nigeria ranked fourth among twenty-two high TB burden countries with 586,000 (345,000 -890,000) incidence cases and 100,000 (56,000 -155,000) HIV positive incident TB cases [6]. Nigeria not only has a surprisingly high death rate (44/100,00) of TB affecting HIV positive individuals, but it is also the country with the highest death rate (97/100,000) for individuals negative for HIV [6]. TB has become an epidemic that has extended itself into every part of Nigeria. In Kano, northwest Nigeria, 14.7% prevalence was reported among patients attending infectious disease hospital [11]. HIV/TB co-infection prevalence of 17.2% in Southeast Nigeria [12] and 24.8% in Calabar, the Niger Delta region [13]. Benue State has a high TB burden attributed to a high HIV/AIDS [14]. Anigilage et [15] reported a 19.8% prevalence of TB among HIV infected children in Benue State, while Nwadioha et al. [16] reported 21.5% prevalence of TB among patients in Makurdi Benue State.

The gold standard for diagnosing TB is the detection of Mycobacterium tuberculosis by culture and biochemical identification. However, this method is time-consuming, requiring special laboratory and expertise [4]. GeneXpert MTB/RIF assay´s development and its endorsement by the World Health Organization (WHO) to implement national TB programs in developing countries has dramatically reduced TB diagnostic period and improved TB treatment and management [17-19]. The GeneXpert is an automated technology that rapidly and simultaneously processes sputum specimen and detects MTBC and rifampicin resistance mutation in the rpoB gene. This assay was approved and recommended for TB diagnosis by WHO especially suspected HIV/TB comorbidity globally [20, 21]. There is the paucity of information on the prevalence of TB and RR-TB in Benue State. Rifampicin resistance-TB provides adequate information on patients' adherence to TB regimen and template for effective infection control. Therefore, the study determines the prevalence of tuberculosis and RR-TB among HIV positive patients in Benue State, Nigeria.

 

 

Methods Up    Down

Study setting: this descriptive case-control study was conducted at the DOTS of FMC, Makurdi and the General hospital, Otupko. The study spanned between January 2017 and February 2018. The study participants comprised 332 HIV seropositive and 678 HIV seronegative patients. The study was approved by the Research and Ethics Committee of the Federal Medical Center, Makurdi and the Health Research Ethics Committee, Benue State University Teaching Hospital, Makurdi, Nigeria. The study questionnaire and consent form were administered to patients willing to participate in the study after a verbal briefing on the study's public health importance. The questionnaire's information includes age, gender, ethnic background, residential location, TB, and HIV status.

Sputum sample collection: each patient was asked to provide two sputum samples after giving consent to participate in the study. The first sputum sample was collected upon enrollment, and the second was collected the following morning. A physician did not induce sputum collections. The first sputum sample was tested with GeneXpert MTB/RIF, while the second sample was subjected to AFB smear microscopy. These procedures were carried out at the TB unit of the Microbiology Department at the FMC, Makurdi and the General Hospital, Otukpo.

Microscopic examination of sputum samples: conventional Ziehl-Neelsen (ZN) was performed to investigate the presence of acid-fast bacilli (AFB). Slides showing pink/red coloured acid-fast bacilli were recorded as positive. The procedure was done according to a previous report [22].

GeneXpert MTB/RIF PCR test: GeneXpert MTB/RIF PCR tests were carried out according to manufacturer´s instructions. Sample reagent was added to untreated sputum at a 2:1 ratio. The mixture was manually agitated twice during a 15minute incubation period at room temperature. 2 ml of the mixture were transferred into a test cartridge with a sterile pipette. The cartridge was then loaded into the GeneXpert machine. GeneXpert MTB/RIF PCR test results were received through computer software and subsequently printed for filing at the end of the real-time PCR assay.

Statistical analysis: data obtained were analyzed using the Chi-square test; logistic regression analysis was used to clarify the predictors for HIV/TB co-infection and rifampicin resistance. P values were two-tailed, with P < 0.05 being considered statistically significant. Statistical analyses were performed using SPSS 20.0 (SPSS Inc. Chicago, IL, USA).

Ethical approval: the permission (BSUTH/MKD/HREC2013B/2017/0011) to conduct this study was obtained from the Health Research Ethics Committee, Benue State University Teaching Hospital, Makurdi, Nigeria. There is no way to trace patients' identities from the results generated in this study.

 

 

Results Up    Down

The overall prevalence of tuberculosis by Smear microscopy (AFB) was 7.33% (73/1010). The prevalence among age groups was not significantly different (Χ² = 4.316; P = 0.229). However, patients within the age of 15 -34 had the highest prevalence (9.33%) of TB than other age groups. Patients from urban areas had significantly (Χ² = 4.38; P = 0.036) higher prevalence of TB than patients from rural areas (8.85% vs 5.40%). There was significant (Χ²= 23.21; P = 0.000) difference between ethnic groups in the study areas. Tiv (11.08%) and other (15.25%) ethnic groups had a higher prevalence of TB than patients from the Idoma ethnic group (3.91%). Patients who were diagnosed at FMC, Makurdi had significantly (Χ² = 22.30; P = 0.000) higher prevalence of TB than patients who visited General hospital, Otukpo (12.04% vs 4.15%) (Table 1).

Overall prevalence of TB in the study population by GeneXpert assay was 16.93% (171/1010). Of these, patients within the age bracket 15 -34 (18.42%) and 35 -54 had higher prevalence of TB than those within 0 -14 (10.25%) and 55 years and above (9.87%). The difference in TB prevalence among the age groups was significant (Χ² = 8.01%; P = 0.046). Patients from urban areas had a higher TB prevalence (17.70%) by GeneXpert assay than patients from rural areas. However, the difference was not statistically significant (Χ² = 0.54; P = 0.464). the Idoma and Tiv (16.24% and 16.16%) had about the same TB prevalence; Other ethnic groups had the highest prevalence (28.81%). Also, the difference in TB prevalence among the different ethnic groups in the study population was statistically significant (Χ² = 6.30; P = 0.044) (Table 1).

Both crude and adjusted odds ratio were higher for HIV/TB coinfected patients within the age bracket 35 -54 (COR 1.963, 95% CI 0.796 -4.842; AOR 2.154, 95% CI 0.865 -5.366) than other age groups. The Idoma ethnic group had significantly (P = 0.006) lower crude odds ratio (COR 0.440, 95% CI 0.246 -0.786) for HIV/TB co-infection than Tiv and other ethnic groups. Patients diagnosed at FMC, Makurdi had a higher crude and adjusted odds ratio for HIV/TB co-infection than patients who visited General hospital, Otukpo (Table 2).

The overall prevalence of rifampicin resistance tuberculosis in the study population was 2.18%. However, not statistically significant, crude and adjusted odds ratio indicated that HIV patients were less likely to have rifampicin resistance tuberculosis than non-HIV patients (COR 0.578, 95% CI 0.247 -1.351; AOR 0.642, 95% CI 0.245 -1.681). Patients within the age group 15 -34 and 35 -54 were twice as likely to have rifampicin resistance tuberculosis (Table 3). Also, the adjusted odds ratio indicated that patients diagnosed at FMC, Makurdi, were twice as likely to have rifampicin resistance tuberculosis than those diagnosed at the General hospital, Otukpo (Table 3).

 

 

Discussion Up    Down

The overall prevalence of TB of 7.33% by smear microscopy and 16.93% by GeneXpert MTB/RIF affirmed the findings that GeneXpert high sensitivity and specificity in detecting TB infection in the clinical specimen as documented in other studies [20, 23-25]. The prevalence reported in this study was consistent with previous studies [17, 18, 26]. The high sensitivity and specificity of GeneXpert assay in detection of TB infection collaborated with a study among HIV/TB co-infection and RR-TB conducted in South Africa with a prevalence of 17.3% Lawn et al. [27]. Similarly, Habte et al. [28] report GeneXpert MTB/RIF detection rate of (35.9%) cases of TB compared to 12.8% by smear microscopy and stated that GeneXpert helped in household contact tracing [28].

There was no significant difference in TB prevalence between HIV positive and HIV negative patients in this present study. In contrast, Babatunde et al. [12] reported a higher prevalence of TB among HIV negative patients than in HIV positive patients. A study conducted in Ethiopia reported a significantly higher prevalence of TB among HIV positive than HIV negative patients [29]. A significant difference was observed with the age group comparing the patients' detection methods and demographic variables and detection methods. There was a high HIV/TB prevalence within 15 -34years and 35 to 54 years. This result was consistent with the findings of previous reports in Nigeria [14, 30]. The high prevalence of TB and HIV/TB co-infection among these age groups may be due to the high cases of HIV [8, 31-33]. Additionally, Ojiezeh et al. [14] reported a high prevalence of HIV/TB co-infection among sexually active, productive/childbearing persons aged 34-44. Primarily due to social-cultural practices that were predisposing them to this infection. The patients' residential location varies with TB prevalence and detection methods. The prevalence of TB was significantly high among patients in urban areas than those in rural areas, attributable to the variances in population density and access to healthcare facilities for proper diagnosis [34]. Prasad et al. [35] stated that two factors are responsible for a higher prevalence of TB in urban areas than in rural areas. Firstly, a high proportion of urban residents in low and middle-income countries live in dismal conditions that consist of overcrowding, poor-quality housing, and lack of water sanitation and secure tenure. Secondly, there is abundant inequality in health care access and quality in some urban areas.

We observed that the prevalence of TB was significantly different among ethnic groups in Benue State. The Idoma ethnic group had a lower TB prevalence than Tiv and other ethnic groups, as indicated by both smear microscopy and GeneXpert. Also, the Idoma ethnic group had a significantly lower risk of acquiring HIV/TB co-infection. The differences in the prevalence and risk of TB and HIV/TB co-infection among different ethnic groups in Benue State could be attributed to differences in socio-cultural practice that predispose them to infection. This observation coincided with a similar study conducted in Ethiopia in which the ethnic Afar population had a relatively low TB prevalence than other ethnic groups [29]. The relatively high prevalence of TB among the Tiv and other ethnic groups was worrisome for reasons stemming from TB transmission and poor ventilation, and overcrowding. The Tiv ethnic group´s observed prevalence might be primarily to their occupational activities as they are an agrarian community known for their large family sizes. Every member contributes to the upkeep and arduous labour of maintaining the family farm. The communal lifestyle, residing within a densely populated household with poor ventilation, facilitates TB transmission [36, 37]. There was high HIV among the Tiv ethnic group [38], hence the high HIV associated TB [39]. Among the other ethnic groups, the Hausa are the majority. The Hausa ethnic group lives in densely populated urban poor areas in Benue State. Their practice of polygamy characterizes large family sizes that lead to overcrowding and poor nutrition [40].

Patients who attended the FMC of Makurdi had a higher prevalence of TB than those who attended the General Hospital of Otukpo. We also observed that patient who visited the FMC of Makurdi had a higher risk of HIV/TB co-infection. The high prevalence of TB and high risk of HIV/TB co-infection among patients who attended the FMC, Makurdi can be explained by the FMC's role as a referral centre. Therefore, it receives more positive cases of TB and HIV/TB co-infection than the General Hospital, Otukpo. Furthermore, literacy levels and work experience are essential in the performance of TB diagnostic testing. The FMC has a higher pay rate and a greater number of laboratory staff than the Benue State Ministry of Health. There are more qualified and educated personnel at the FMC of Makurdi than at the Otukpo General Hospital.

In this study, we reported a prevalence of 2.2% rifampicin resistance among HIV and non-HIV positive TB patients who attended TB clinics in both the FMC of Makurdi and the General Hospital of Otukpo. The results obtained in this study were lower than previous studies in Southwest Nigeria (5.5%) [41]. In another research study conducted in three Nigerian cities, 23% prevalence and 11% rifampicin resistance were reported among failed and new treatment cases. A higher prevalence of rifampicin resistance was also reported in Ethiopia [42, 43]. The prevalence of rifampicin resistance reported in this study was consistent with WHO's estimated prevalence of 2.2% [7]. The low prevalence of rifampicin resistance observed in this study compared with other research in Nigeria and Ethiopia may be due to differences in sample size, location and other factors that are not considered in this study. Moreover, Mulu et al. [43] explained that variation in the rate of rifampicin resistance among different authors could be due to differences in the risk for HIV acquisition, exposure to anti-TB drugs and national TB control programs.

In this study, we observed that gender, HIV status, age and residence in urban versus rural areas were not significant factors that could influence rifampicin resistance. This finding agreed with the report of Masenga et al. [44]. Masenga et al. [44] explained that both males and females had equal exposure to rifampicin resistance causative factors. A similar trend was reported among previously treated and new cases of TB in Ethiopia [43].

 

 

Conclusion Up    Down

The relatively high prevalence of HIV/TB co-infection is of public health concern, considering the consequential impact on the community, as high prevalence was observed among the sexually active age groups. The RR-TB prevalence of 2.2 % is an indicator of the emerging TB patient treatment failure trend, which could further worsen the infection control strategy. Future studies are needed for better understanding of the TB epidemiology and infection control intervention.

What is known about this topic

  • The prevalence of tuberculosis in Benue State is high because of the high burden of HIV/AIDS;
  • There is poor tuberculosis treatment outcome due to HIV/AIDS and TB comorbidity;
  • Tuberculosis treatment and diagnostic centres are located in each senatorial district in Benue state, but there is the paucity of published data on the prevalence of tuberculosis and rifampicin-resistant tuberculosis.

What this study adds

  • The overall prevalence of tuberculosis in the study area was 7.33% and 16.93% by acid-fast microscopy and GenXpert MTB/RIF;
  • The prevalence of TB was higher among patients from urban areas than from rural dwelers (8.85% vs 4.28%);
  • The prevalence of rifampicn resistant tuberculosis among the study population was 2.18%.

 

 

Competing interests Up    Down

The authors declare no competing interests.

 

 

Authors´ contributions Up    Down

All authors read and approved the final version of this manuscript and equally contributed to its content.

 

 

Acknowledgments Up    Down

We are most grateful to the technical staff of the Department of Microbiology and Research Unit, Federal Medical Centre, Makurdi and General Hospital, Otukpo, for their kind support during the conduct of this study.

 

 

Tables Up    Down

Table 1: comparative detection of tuberculosis by smear microscopy and GeneXpert in Benue State

Table 2: HIV/TB coinfection among patients who attended DOTS Centers in Makurdi and Otukpo, Benue State

Table 3: rate of detection of rifampicin resistance among different populations in Benue State

 

 

References Up    Down

  1. Gagneux S, Small PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis. 2007 May;7(5):328-37. PubMed | Google Scholar

  2. Ejeh EF, Akinseye VO, Igwe D, Adesokan HK, Cadmus SI. Molecular characterization of Mycobacterium bovis in slaughtered cattle in North-Central Nigeria and the public health implications. Afr J Med Med Sci. 2014 Dec;43 Suppl:97-104. PubMed | Google Scholar

  3. Thoen CO, Barletta RG. Pathogenesis of tuberculosis caused by Mycobacterium bovis. Zoonotic Tuberc. Mycobacterium bovis Other Pathog. Mycobact. 3rd Ed. 2014. Google Scholar

  4. WHO. Global tuberculosis report 2014.

  5. Anderson L, Dean A, Falzon D, Floyd K, Baena I, Gilpin C, et al. WHO Global tuberculosis report 2015.

  6. World Health Organization. Global tuberculosis report 2013. Google Scholar

  7. WHO WHO. Global tuberculosis control: WHO report 2011. 2011.

  8. FMOH. National HIV Sero-prevalence Sentinel Survey: Technical report of the Federal Ministry of haelth, Nigeria. Niger Fed Minist Heal Dep Public Heal Natl AIDS/STI Control Program 2010.

  9. Dinic L, Akande P, Idigbe EO, Ani A, Onwujekwe D, Agbaji O et al. Genetic determinants of drug-resistant tuberculosis among HIV-infected patients in Nigeria. J Clin Microbiol. 2012 Sep;50(9):2905-2909. PubMed | Google Scholar

  10. Mesfin YM, Hailemariam D, Biadglign S, Kibret KT. Association between HIV/AIDS and multidrug resistance tuberculosis: A systematic review and meta-analysis. PLoS One. 2014 Jan 8;9(1):e82235. PubMed | Google Scholar

  11. TS, Imam OT. Retrospective study of pulmonary tuberculosis (PTB) prevalence among patients attending in infectious disease hospital. Bayero J Pure Appl Sci 2008;1(1):10-5. Google Scholar

  12. Babatunde OI, Christiandolus EO, Bismarck EC, Emmanuel OI, Chike AC, Gabriel EI. Five years retrospective cohort analysis of treatment outcomes of TB-HIV patients at a PEPFAR/DOTS centre in South Eastern Nigeria. Afr Health Sci. 2016;16(3). Google Scholar

  13. Kooffreh M, Offor J, Ekerette E, Udom U. Prevalence of tuberculosis in Calabar, Nigeria: A case study of patients attending the outpatients Department of Dr. Lawrence Henshaw Memorial Hospital, Calabar. Saudi J Heal Sci. 2016;5(3):130-133. Google Scholar

  14. Ojiezeh TI, Ogundipe OO, Adefosoye VA. A retrospective study on incidence of pulmonary tuberculosis and human immunodeficiency virus co-infection among patients attending National Tuberculosis and Leprosy Control Programme, Owo centre. Pan Afr Med J 2015. Google Scholar

  15. Anígilájé EA, Aderibigbe SA, Adeoti AO, Nweke NO. Tuberculosis, before and after antiretroviral therapy among HIV-infected children in Nigeria: What are the risk factors? PLoS One. 2016 May 27;11(5):e0156177. PubMed | Google Scholar

  16. Nwadioha SI, Nwokedi EOP, Ezema GC, Eronini NC, Anikwe A, Audu F et al. Drug Resistant Mycobacterium tuberculosis in Benue, Nigeria. Microbiol Res J Int. 2014; 4(9):988-995. Google Scholar

  17. Kaur R, Kachroo K, Sharma J, Vatturi S, Dang A. Diagnostic accuracy of xpert test in tuberculosis detection: A systematic review and meta-analysis. J Glob Infect Dis. Jan-Mar 2016;8(1):32-40. PubMed | Google Scholar

  18. Durovni B, Saraceni V, van den Hof S, Trajman A, Cordeiro-Santos M, Cavalcante S et al. Impact of replacing smear microscopy with Xpert MTB/RIF for diagnosing tuberculosis in Brazil: a stepped-wedge cluster-randomized trial. PLoS Med. 2014 Dec 9;11(12):e1001766. PubMed | Google Scholar

  19. World Health Organization. Xpert MTB/RIF implementation manual. Technical and operational "how-to" practical considerations. 2014. Google Scholar

  20. Zeka AN, Tasbakan S, Cavusoglu C. Evaluation of the GeneXpert MTB/RIF assay for rapid diagnosis of tuberculosis and detection of rifampin resistance in pulmonary and extrapulmonary specimens. J Clin Microbiol. 2011 Dec;49(12):4138-41. PubMed | Google Scholar

  21. Iram S, Zeenat A, Hussain S, Yusuf NW, Aslam M. Rapid diagnosis of tuberculosis using Xpert MTB/RIF assay -report from a developing country. Pak J Med Sci. Jan-Feb 2015;31(1):105-10. PubMed | Google Scholar

  22. Whittier S, Olivier K, Gilligan P, Knowles M, Della-Latta P, Besser-Weik J et al. Proficiency testing of clinical microbiology laboratories using modified decontamination procedures for detection of nontuberculous mycobacteria in sputum samples from cystic fibrosis patients. J Clin Microbiol. 1997 Oct;35(10):2706-8. PubMed | Google Scholar

  23. Pinyopornpanish K, Chaiwarith R, Pantip C, Keawvichit R, Wongworapat K, Khamnoi P et al. Comparison of Xpert MTB/RIF Assay and the Conventional Sputum Microscopy in Detecting Mycobacterium tuberculosis in Northern Thailand. Tuberc Res Treat. 2015;2015:571782. PubMed | Google Scholar

  24. Luetkemeyer AF, Firnhaber C, Kendall MA, Wu X, Mazurek GH, Benator DA et al. Evaluation of Xpert MTB/RIF Versus AFB Smear and Culture to Identify Pulmonary Tuberculosis in Patients with Suspected Tuberculosis from Low and Higher Prevalence Settings. Clin Infect Dis. 2016 May 1;62(9):1081-8. PubMed | Google Scholar

  25. Ejeh EF, Undiandeye A, Akinseye VO, Okon KO, Kazeem HM, Kudi CA, et al. Diagnostic performance of GeneXpert and Ziehl-Neelson microscopy in the detection of tuberculosis in Benue State, Nigeria. Alexandria J Med 2018;54(4):529-33. Google Scholar

  26. Lombardi G, Di Gregori V, Girometti N, Tadolini M, Bisognin F, Dal Monte P. Diagnosis of smear-negative tuberculosis is greatly improved by Xpert MTB/RIF. PLoS One. 2017 Apr 21;12(4):e0176186. PubMed | Google Scholar

  27. Lawn SD, Harries AD, Meintjes G, Getahun H, Havlir D V, Wood R. Reducing deaths from tuberculosis in antiretroviral treatment programmes in sub-Saharan Africa. AIDS. 2012 Nov 13;26(17):2121-33. PubMed | Google Scholar

  28. Habte D, Melese M, Hiruy N, Gashu Z, Jerene D, Moges F et al. The additional yield of GeneXpert MTB/RIF test in the diagnosis of pulmonary tuberculosis among household contacts of smear positive TB cases. Int J Infect Dis. 2016 Aug;49:179-84. PubMed | Google Scholar

  29. Belay M, Bjune G, Abebe F. Prevalence of tuberculosis, HIV, and TB-HIV co-infection among pulmonary tuberculosis suspects in a predominantly pastoralist area, northeast Ethiopia. Glob Health Action. 2015;8(1):10.3402/gha.v8.27949. PubMed | Google Scholar

  30. Ofoegbu OS, Odume BB. Treatment outcome of tuberculosis patients at national hospital Abuja Nigeria: A five year retrospective study. South African Fam Pract. 2015; 57(1):50-56. Google Scholar

  31. Bashorun A, Nguku P, Kawu I, Ngige E, Ogundiran A, Sabitu K et al. A description of HIV prevalence trends in Nigeria from 2001 to 2010: what is the progress, where is the problem? Pan Afr Med J. 2014;18(Suppl 1):3. PubMed | Google Scholar

  32. Idoko J, Naamara W, Azeez A, Al E. United Nations General Assembly Country Progress Report: Nigeria. UNGASS Spec Sess Rep 2010.

  33. National Agency for the Control of AIDS. Federal Republic of Nigeria: GLOBAL AIDS RESPONSE Country Progress Report. Fed Repub Niger Glob Aids Response Ctry Prog Rep Niger GARPR 2014 Niger 2014.

  34. Abubakar I, Crofts JP, Gelb D, Story A, Andrews N, Watson JM. Investigating urban-rural disparities in tuberculosis treatment outcome in England and Wales. Epidemiol Infect. 2008 Jan;136(1):122-7. PubMed | Google Scholar

  35. Prasad A, Ross A, Rosenberg P, Dye C. A world of cities and the end of TB. Trans R Soc Trop Med Hyg. 2016 Mar;110(3):151-2. PubMed | Google Scholar

  36. Omideyi AK. Family size and productivity of rural households in Nigeria. Janasamkhya. 1988 Jun;6(1):29-48. PubMed | Google Scholar

  37. Agada M, Igbokwe E. Influence of Food Culture and Practices on Household Food Security in North Central Nigeria. J Food Secur. 2016;4(2):36-41. Google Scholar

  38. Gberindyer J-A, Agbecha A, Shindi J, Useh N. Human immunodeficiency virus infection among male prison inmates in Birnin Kebbi, Nigeria. Environ Dis. 2017;1(2):27-31. Google Scholar

  39. Mekonnen D, Derbie A, Desalegn E. TB/HIV co-infections and associated factors among patients on directly observed treatment short course in Northeastern Ethiopia: A 4 years retrospective study. BMC Res Notes. 2015;8:666. PubMed | Google Scholar

  40. Ahidjo a, Yusuph H, Tahir A. Radiographic Features of Pulmonary Tuberculosis Among Hiv Patients in Maiduguri, Nigeria. Ann Afr Med. 2005;4(1):7-9. Google Scholar

  41. Daniel O, Osman E. Prevalence and risk factors associated with drug resistant TB in South West, Nigeria. Asian Pac J Trop Med. 2011 Feb;4(2):148-51. PubMed | Google Scholar

  42. Adane K, Ameni G, Bekele S, Abebe M, Aseffa A. Prevalence and drug resistance profile of Mycobacterium tuberculosis isolated from pulmonary tuberculosis patients attending two public hospitals in East Gojjam zone, northwest Ethiopia Infectious Disease epidemiology. BMC Public Health. 2015 Jun 20;15:572. PubMed | Google Scholar

  43. Mulu W, Abera B, Yimer M, Hailu T, Ayele H, Abate D. Rifampicin-resistance pattern of Mycobacterium tuberculosis and associated factors among presumptive tuberculosis patients referred to Debre Markos Referral Hospital, Ethiopia: a cross-sectional study. BMC Res Notes. 2017 Jan 3;10(1):8. PubMed | Google Scholar

  44. Masenga SK, Mubila H, Hamooya BM. Rifampicin resistance in mycobacterium tuberculosis patients using GeneXpert at Livingstone Central Hospital for the year 2015: a cross sectional explorative study. BMC Infect Dis. 2017 Sep 22;17(1):640. PubMed | Google Scholar

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Research

Prevalence of rifampicin resistance tuberculosis among HIV/TB coinfected patients in Benue State, Nigeria

Research

Prevalence of rifampicin resistance tuberculosis among HIV/TB coinfected patients in Benue State, Nigeria

Research

Prevalence of rifampicin resistance tuberculosis among HIV/TB coinfected patients in Benue State, Nigeria