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Background:
Review

Isoniazid Preventive Therapy for Prevention of Tuberculosis among People Living with HIV in Ethiopia: A Systematic Review of Implementation and Impacts

by
Dawit Getachew Assefa
1,2,*,
Eden Dagnachew Zeleke
1,3,
Delayehu Bekele
1,4,
Dawit A. Ejigu
5,
Wondwosen Molla
6,
Tigist Tekle Woldesenbet
7,
Amdehiwot Aynalem
8,
Mesfin Abebe
6,
Andualem Mebratu
6 and
Tsegahun Manyazewal
1
1
Center for Innovative Drug Development and Therapeutic Trials for Africa (CDT-Africa), College of Health Sciences, Addis Ababa University, Addis Ababa P.O. Box 3880, Ethiopia
2
Department of Nursing, College of Medicine and Health Sciences, Dilla University, Dilla P.O. Box 419, Ethiopia
3
Department of Midwifery, College of Health Science, Bule-Hora University, Bule-Hora P.O. Box 144, Ethiopia
4
Department of Obstetrics and Gynecology, Saint Paul’s Hospital Millennium Medical College, Addis Ababa P.O. Box 3880, Ethiopia
5
Department of Pharmacology, Saint Paul’s Hospital Millennium Medical College, Addis Ababa P.O. Box 3880, Ethiopia
6
Department of Midwifery, College of Medicine and Health Sciences, Dilla University, Dilla P.O. Box 419, Ethiopia
7
Department of Public Health, School of Graduate Studies, Pharma College, Hawassa P.O. Box 5, Ethiopia
8
School of Nursing, College of Medicine and Health Sciences, Hawassa University, Hawassa P.O. Box 1560, Ethiopia
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2023, 20(1), 621; https://doi.org/10.3390/ijerph20010621
Submission received: 13 October 2022 / Revised: 12 December 2022 / Accepted: 13 December 2022 / Published: 29 December 2022
(This article belongs to the Special Issue Sustainability: Challenges for Healthcare)
Browse Figure
Review Reports Versions Notes

Abstract

:
Background: Tuberculosis (TB) is a major cause of morbidity and mortality in people living with HIV (PLWHIV). Isoniazid preventive therapy (IPT) prevents TB in PLWHIV, but estimates of its effects and actual implementation vary across countries. We reviewed studies that examined the impact of IPT on PLHIV and the factors influencing its implementation in Ethiopia. Methods: We searched PubMed/MEDLINE, Embase, and the Cochrane Central Register of Clinical Controlled Trials from their inception to 1 April 2021 for studies of any design that examined the impact of IPT on PLHIV and the factors influencing its implementation. The protocol was registered in PROSPERO, ID: CRD42021256579. Result: Of the initial 546 studies identified, 13 of which enrolled 12,426 participants, 15,640 PLHIV and 62 HIV clinical care providers were included. PLHIV who were on IPT, independently or simultaneously with ART, were less likely to develop TB than those without IPT. IPT interventions had a significant association with improved CD4 count and reduced all-cause mortality. IPT was less effective in people with advanced HIV infection. The major factors influencing IPT implementation and uptake were stock-outs, fear of developing isoniazid-resistant TB, patient’s refusal and non-adherence, and improper counseling and low commitment of HIV clinical care providers. Conclusion: IPT alone or in combination with ART significantly reduces the incidence of TB and mortality in PLHIV in Ethiopia than those without IPT. More research on safety is needed, especially on women with HIV who receive a combination of IPT and ART. Additionally, studies need to be conducted to investigate the efficacy and safety of the new TPT (3 months combination of isoniazid and rifapentine) in children and people living with HIV.

1. Introduction

Tuberculosis (TB) remains one of the top 10 causes of death globally and the primary cause of death from a single infectious agent [1]. In 2021, there were 10.6 million TB cases globally and 1.4 million deaths among HIV-negative people, and an additional 187,000 deaths among HIV-positive people [1]. Most people who acquired TB in 2021 were in the regions of South-East Asia (45%), Africa (23%), and the Western Pacific (18%) [1]. In Africa, a widespread scale-up of antiretroviral therapy (ART) strongly declines the incidence of TB [2]. Ethiopia is one of the top 14 triple burden countries for TB, TB/HIV, and MDR-TB [1]. An estimated incidence of all forms of TB in Ethiopia, in 2019, was 140/100,000 population, with 111,039 TB cases notified [1]. TB remains one of the major causes of morbidity and mortality in the country [3].
To prevent and reduce the incidence of TB in people living with HIV (PLHIV), the World Health Organization (WHO) recommended the use of isoniazid preventive therapy (IPT) as a mainstay of the “Three I’s” approach [4]. Per the WHO recommendation, IPT is administered at a daily dose of a maximum of 300 mg daily for 6–9 months in adults and adolescents and 5 mg/kg for children [5,6]. This chemoprophylaxis reduces the risk of an early episode of TB occurrence in people with latent infection or those exposed to infection, and reduces recurrent episodes of TB [5,6]. For patients with latent TB, IPT can be beneficial, with the potential to reduce TB infection irrespective of HIV status [5,6] and protecting communities from [7,8,9]. However, the emergence of drug resistance secondary to IPT administration is a potential risk that is understudied [5].
In Ethiopia, the National TB guideline recommends that IPT should be provided to all HIV-infected individuals who are unlikely to have active TB irrespective of CD4 count, ART status, pregnancy status, or history of treatment for a prior episode of TB before three years. Patients should be supported at home level either by local health extension workers or a family supporter to ensure daily administration of IPT. Patients should be given a one-month supply of isoniazid for six months, with a monthly scheduled follow-up integrated with other treatment services. IPT should also be administered for asymptomatic children under five who were exposed to TB within the past year. However, the current evidence regarding the effects and actual implementation of IPT in Ethiopia remains unclear. This systematic review was, therefore, conducted to examine the outcomes of IPT in PLHIV and factors influencing its implementation in Ethiopia.

2. Methods

The protocol for this systematic review and meta-analysis was registered at the International Prospective Register of Systematic Reviews (PROSPERO) database, ID: CRD42021256579. The Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA 2020) guidelines were followed to choose studies to be included in this review.

2.1. Eligibility Critria Studies

Criteria included studies of any design that examined the impact of IPT on PLHIV and the factors influencing its implementation in Ethiopia, published in English language until 1 April 2021.

2.2. Participants

  • Patients with HIV,
  • Man or woman of any age,
  • ART naïve or experienced on their time of enrollment.

2.3. Types of Interventions

2.3.1. For Intervention Studies

  • Intervention group: isoniazid 300 mg daily for 6–9 months in adults and adolescents and 5 mg/kg for children.
  • Comparison group: inactive placebo, ART only, or no preventive treatment.

2.3.2. For Non-Intervention Studies

  • Effectiveness, barriers, or opportunities implementing IPT program in Ethiopia based on experiences from PLHIV or HIV clinical service providers.

2.4. Outcome Measures

2.4.1. Primary Outcome Measure

  • Incidence of definite or probable TB. Definite TB was defined by a microbiological, chest X-ray, or histological identification of TB.

2.4.2. Secondary Outcome Measures

  • Incidence of death.
  • Factors associated with TB incidence.
  • Incidence of adverse drug reactions leading treatment discontinuation.
  • Barriers to implementation of IPT.

2.5. Search Strategy

A computerized systematic search method was used to search for articles from online databases PubMed/MEDLINE, Embase, and Cochrane Central Register of Clinical controlled Trials (CENTRAL) databases from inception to 1 April 2021. The search was based on the Cochrane Handbook for Systematic Reviews of Interventions [10], with a combination of the words (tuberculosis) AND (isoniazid preventive therapy) considered the major search term (Table 1).

2.6. Study Selection

The Cochrane Handbook for Systematic Reviews of Interventions [11] was followed. To import the research articles from the electronic databases and remove duplicates, ENDNOTE software version X7 was used. Two authors independently reviewed the results of the literature search and obtained full-text copies of all potentially relevant studies. Disagreements were resolved through discussion. When clarification was necessary, the trial authors were contacted for further information. The screening and selection process was reported in a PRISMA flow chart (Figure 1).

2.7. Data Extraction and Management

The title and abstract were produced from the electronic search and were independently screened by two authors based on studies and the selection criteria. The information collected were study characteristics, including study design, study setting, age and number of participants enrolled, interventions, study title, journal, year of publication, publication status, follow-up period, funding of the trial or sources of support, baseline characteristics of study subjects, incidence of TB, factors associated with IPT, and IPT implementation barriers. One author independently extracted data, and these were cross-checked by another author. Missing data were requested from the authors whenever necessary.

3. Result

A total of 546 studies through the databases were searched, of which, 16 full-text studies were assessed further for eligibility and 13 of them fulfilled the inclusion criteria for further analysis (Table 2).

3.1. Characteristics of Included Studies

In this review, 13 studies that enrolled a total of 15,640 PLHIV and 62 health professionals working on HIV care were included (Table 2). Many of the patients were aged greater than 14 years [12,13,14,15,16] and female [12,13,14,15,17,18]. The CD4 count was > 200 cell count/μL in most of the participants in one study [13] and less than 199 cells/mm3 in another study [14], and most of the patients were in HIV stage III followed by stage II [13,14,19].

3.2. Incidence of TB

Among PLHIV, the incidence of TB after administration of IPT independently or simultaneously with ART shows a significant reduction in the incidence of TB as compared to patients who were on ‘ART only’ and ‘No intervention’ [12,13,15,16,17,18,19,20,21]. Simultaneous administration of both IPT and ART reduced the incidence of TB by 80% [12], 93.7% [13], and 65% [14], respectively. Completion of IPT showed a significant protective effect against the occurrence of active TB for 3 years when compared to IPT non-exposed patients [13]. IPT was associated with a significant change in CD4 count [15,19,20] and reduced all-cause mortality [14,17,19,20].

3.3. Factors Associated with TB Incidence among PLWHIV Who Took IPT

The risk of developing TB or dying was significantly higher in PLHIV on WHO stage III and above at baseline [12,13,14,16,17,18,22], male [12,13,14,22], with a CD4 count of less than a 350 cell count/μL and those with opportunistic infections [15,16,17,18,21,22], children with delayed motor development [21] who did not take cotrimoxazole preventive therapy [18,21,22], use anti-pain [22], and have a hemoglobin level less than 10 mg/dL [16,21,22]. The risk of TB infection and death was lower in those who held good body weight [14,18,21,22] and referred to the hospital from other health facilities [14]. In some of the studies, the effects of age [14,21] and baseline CD4 count had a suboptimal effect on TB incidence or death [14].

3.4. Barriers in the Implementation of IPT

A significant number of HIV clinical care providers reported that several barriers hinder IPT coverage and its effective implementation, including isoniazid stock-outs, fear of developing isoniazid resistance, patient’s refusal and non-adherence, and improper counseling and low commitment of HIV clinical care providers [23]. Lack of patient empowerment and proper counseling on IPT, weak patient/healthcare provider communication, information gaps, low commitments from health administrators and other stakeholders to effectively run the IPT program, and underlying mental health issues resulting in missed or irregular patient adherence to IPT were also reported as barriers for effective implementation of IPT in Ethiopia [24]. Additionally, clinician impressions that ruling out active TB among HIV patients is difficult was found to be a significant barrier to IPT uptake [25].
Table
Table 2. Characteristics of included studies.
Table 2. Characteristics of included studies.
S. NoStudy IDDesignSettingAgeFollow UpSubjectsPatient Important Outcome
1.Mindachew et al., 2014 [24]QualitativeHospitalN/AN/A12 heath professionalbarriersLack of patient empowerment and proper counseling on IPT, weak patient/healthcare provider relationship, lack of patient information, low reinforcement by health officials and stakeholders to strengthen IPT uptake and adherence forgetfulness, patient IPT non-adherence, and non-disclosure of HIV zero-status.
2.Yirdaw et al., 2014 [12]Retrospective cohortHospitals (n = 5)Mean (30 years)2 years5407 patientsIPT before ARTaHR = 0.18, 95% CI = 0.08–0.42
IPT before ART’HR = 0.25, 95% CI = 0.11–0.59
IPT and ARTaHR = 0.20,95% CI = 0.10–0.42
IPT and ARTHR = 0.36; 95% CI = 0.17–0.74
IPT onlyHR = 0.24, 95% CI = 0.13–0.44
IPT after ARTHR = 0.19, 95% CI = 0.11–0.34
TB incidence295
3.Assebe et al., 2015 [17]Retrospective cohort studyHospitalN/AMean 24.1 months588Overall TB incidence49
IPT 294No IPT 294Overall TB incidence3.78 cases per 100 PY (95% CI: 2.85, 4.99 cases per 100 PY)
Incidence of TB among IPT Plus ART2.22 cases per 100 PY (95% CI: 1.29, 3.82 cases per 100 PY)
Incidence of TB among ART alone5.06 cases per 100 PY (95% CI: 3.65, 7.02 cases per100 PY)
Incidence of TB among IPT Plus ARTaHR 2.02 (95% CI: 1.04–3.92)
4.Nigusse et al., 2015 [16]Retrospective follow up studyHospitalMedian 38 (IQR: 31.2–42)5 years480Overall TB incidence70
Overall TB incidence3.59 per 100 PY
TB incidence among IPTaHR = 0.49, 95% CI = 0.26–0.94
5.Ayele, 2015 [14]Retrospective cohort studyHospitalRange 15–99 years839 days1922 (374 received IPT)Overall TB incidence258
Incidence of TB/death among IPT plus ARTHR = 0.35; 95% CI (0.16, 0.77)
Incidence of TB/death among ART aloneHR = 1.22; 95% CI (0.45, 3.28)
Incidence of TB/death among IPT plus ARTaHR = 0.40; 95% CI (0.18, 0.87)
Incidence of TB among IPT plus ART5.20 per 100 PYs
Incidence of TB among ART alone8.05 per 100 PYs
6.Alemu et al., 2016 [21]Retrospective cohort studyHospitals (n = 2),
Health centers (n = 6)		Median (IQR)
6 (3.5–9.00) years		N/A645Overall TB incidence79
Overall TB incidence4.2: 95% CI (3.4, 5.3) PY
7.Teklay et al., 2016 [23]Qualitative studyHospitals (n = 11)Mean (±SD)
30 (±6) years		N/A50 health providersBarriersIsoniazid stock out
Fear of creating isoniazid resistance
Problems in patient acceptance
Lack of commitment of health managers
8.Abossie et al., 2017 [15]Hospital-based retrospective studyHospitalMean (±SD)
31.27 (+12.0)		 271Incidence of TB among IPT Plus ART12 (8.7%)
IPT 138No IPT 133Incidence of TB among ART alone37 (27.8%)
Incidence of TB among IPT Plus ARTRR 0.31 (95% CI 0.122, 0.49)
9.Semu et al., 2017 [13]Retrospective cohortPublic health institutionsMean (±SD)
34.9 (±9.1) years		5 years2524 patientsTB Incidence Rate among IPT0.21/100 PY
TB-incidence Rate among at IPT completionaIRR 0.037 (95% CI, 0.016–0.072)
overall TB incidence6.7/100 PY
TB incidence277
Incidence of TB among IPT-with-HAART0.42/100 PY
Incidence of TB among IPT-with-HAARTaIRR = 0.063 (95% CI 0.035–0.104)
Incidence of TB among alone HAART7.83 cases/100 PY
10.Tiruneh et al., 2019 [18]Retrospective cohort studyHospital and health centerMean (±SD)
33 years (±9) years		Median 26 months600
IPT 200No IPT 400Overall TB Incidence 53 (8.8%)
Overall TB Incidence57 cases per 100 PY
Incidence of TB among IPT group1.98 per 100 PY
Incidence of TB among non-IPT group4.52 per 100 PY
Incidence of TB among IPT groupaHR 0.45, 95% CI 0.219–0.920
Incidence of TB among IPT groupHR 0.397, 95% CI 0.203–0.774
11.Gebremariam et al., 2020 [20]Retrospective cohort studyHospitals (n = 2)N/A5 years968 patientsIncidence of TB among ART plus IPT8 (0.5 cases/100 PY)
IPT 484No IPT 484Incidence of TB among ART plus IPT aHR 0.17; 95% CI 0.08–0.35
Incidence of TB among ART alone49 (3 cases/100 PY)
Deaths on ART plus IPT12 (0.5 cases/100 PYs)
Deaths on ART alone 35 (2.1 cases/100 PYs)
Death reduction among ART plus IPTaHR 0.48; 95% CI 0.24–0.97
12.Atey et al., 2020 [19]Retrospective Cohort StudyHospitals (n = 5)N/AN/A1863 Incidence of TB among IPT Plus ART28
IPT 621No IPT 1242Incidence of TB among ART alone272
Overall incidence300
Incidence rate of mortality among IPT Plus ART 440 per 100,000 PYs
Incidence rate of mortality among ART alone1490 per 100,000 PYs
13.Legese et al., 2020 [22]Institutional based cross-sectionalHospitalMean (±SD) 37.94 (±12.15)6 months372 (231 on IPT)Overall incidence of TB among IPT group13 (3.5%)

4. Discussion

In this study, IPT shows a significant reduction in the risk of TB and dying as compared to that of ART only and non-intervention. It also shows an effect on the improvement of CD4 count. Several studies conducted elsewhere also reported that IPT reduces the incidence of TB [26,27,28,29,30]. Recent studies reported that IPT is effective in the reduction in TB disease on pregnant women living with HIV and with their CD4 count ≤ 350 cells/μL [31,32]. In West Africa, the early initiation of ART and 6 months of IPT showed a significant reduction in HIV-related illness by 44% and the risk of mortality from any cause by 35% as compared to the risks with deferred initiation of ART and no IPT [33]. There were several factors, such as being male, low baseline CD4 count, and hemoglobin level less than 10 mg/dl, that negatively influenced the effectiveness of IPT. In agreement with our finding, a study from Malawi reported that male PLHIV had low adherence to IPT as compared to female [34]. This might be a reason for the difference in the effectiveness of IPT between male and female patients. Additionally, the protective effect of INH was more extreme in contacts exposed to drug-sensitive tuberculosis (adjusted hazard ratio, 0.30; 95% confidence interval, 0.18–0.48) and to multidrug-resistant tuberculosis (adjusted hazard ratio, 0.19; 95% confidence interval, 0.05–0.66) compared with those exposed to mono-INH-resistant tuberculosis (adjusted hazard ratio, 0.80; 95% confidence interval, 0.23–2.80) [35].
Implementation of the IPT program in Ethiopia is facing several challenges, including stock-out that may question sustainability of the program and may provoke drug resistance. In concurrence to our finding, studies from India reported the lack of awareness on the role and way of taking IPT, risk perception among patients’ parents, cumbersome screening process, isoniazid stock-outs, inadequate knowledge among healthcare providers, and poor programmatic monitoring as main barriers to IPT implementation [36,37]. Adequate supply and availability of isoniazid at the health facilities, preparing unambiguous treatment guideline, contact tracing, provision of IPT for children, community-based intervention, and provision of adequate training for health care providers on IPT enhanced the reduction in TB incidence and patient’s adherence to IPT [38,39,40,41]. Thus, for effective implementation and outcomes of IPT program in Ethiopia, there is a need to enhance patient adherence and effectiveness of IPT through effective communication, build the capacity of the healthcare providers through training and motivation packages, sustainably increase isoniazid supply, and strengthen program partnership and collaboration.

5. Conclusions

IPT alone or in combination with ART significantly reduces the incidence of TB and mortality in PLHIV in Ethiopia than those without IPT. More research on safety is needed, especially on women with HIV who receive a combination of IPT and ART. Additionally, studies need to be conducted to investigate the efficacy and safety of the new TPT (3-month combination of isoniazid and rifapentine) in children and people living with HIV.

Author Contributions

D.G.A., E.D.Z. and W.M. developed the protocol, reviewed the reference list, extracted data, and conducted the analyses. D.G.A., E.D.Z., W.M., D.A.E., D.B., T.T.W., A.A., M.A., A.M. and T.M. assessed the quality of the data and reviewed the analysis. DGA developed the draft manuscript and T.M. critically reviewed it. All authors have read and agreed to the published version of the manuscript.

Funding

This review did not receive specific funding. T.M. was supported in part by the Fogarty International Center and National Institute of Allergy and Infectious Diseases of the US National Institutes of Health under Award Number D43TW009127.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki. The Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA 2020) guidelines were followed to choose studies to be included in this review.

Informed Consent Statement

Not applicable.

Data Availability Statement

All relevant data are within the manuscript.

Acknowledgments

We would like to express our gratitude to the Center for Innovative Drug Development and Therapeutic Trials for Africa (CDT-Africa), College of Health Sciences, Addis Ababa University, for supporting the study.

Conflicts of Interest

We declare that they have no competing interest.

Abbreviations

ARTAnti-Retroviral Therapy
aHRAdjusted Hazard Ratio
aIRRAdjusted incidence rate ratio
CENTRALCochrane Center for Clinical Trial
CIConfidence Interval
IPTIsoniazid Preventive Therapy
HAARTHighly active antiretroviral therapy
HRHazard Ratio
HIVHuman Immune Virus
IRIncidence ratio
PLWHIVPeople Living with Human Immunodeficiency Virus
PYPerson per Year
SDStandard Deviation
TBTuberculosis
TSTTuberculin Skin Test
PRISMAPreferred Reporting Items for Systematic Reviews and Meta-Analyses
WHOWorld Health Organization

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Ijerph 20 00621 g001 550
Figure 1. PRISMA study flow diagram.
Figure 1. PRISMA study flow diagram.
Ijerph 20 00621 g001
Table
Table 1. Search term for MEDLINE.
Table 1. Search term for MEDLINE.
SearchMost Reset Queries
#1Search HIV infections[MeSH] OR HIV[TW] OR HIV-1*[MeSH] OR HIV-2*[TW] OR HIV-1[TW] OR HIV-2[TW] OR HIV infec* [TW] OR Human immunodeficiency virus [TW] OR Human immune-deficiency virus [TW] OR ((Human immune* [TW]) AND (deficiency virus [TW])) OR Acquired immune deficiency syndrome [TW] OR AIDS [MeSH] OR ((acquired immune* [TW]) AND (deficiency syndrome [TW])) OR sexual transmitted diseases, viral [MeSH: No Exp]
#2Search Tuberculosis [MeSH] OR TB [MeSH]
#3Search preventive therapy [MeSH] OR Chemoprevention [MeSH] OR Prophylaxis [MeSH]
#4Search #1 AND #2 AND #3
#5Search #1 AND #2 AND #3 Limits: Publication date from 1980 to 2021
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MDPI and ACS Style

Assefa, D.G.; Zeleke, E.D.; Bekele, D.; Ejigu, D.A.; Molla, W.; Woldesenbet, T.T.; Aynalem, A.; Abebe, M.; Mebratu, A.; Manyazewal, T. Isoniazid Preventive Therapy for Prevention of Tuberculosis among People Living with HIV in Ethiopia: A Systematic Review of Implementation and Impacts. Int. J. Environ. Res. Public Health 2023, 20, 621. https://doi.org/10.3390/ijerph20010621

AMA Style

Assefa DG, Zeleke ED, Bekele D, Ejigu DA, Molla W, Woldesenbet TT, Aynalem A, Abebe M, Mebratu A, Manyazewal T. Isoniazid Preventive Therapy for Prevention of Tuberculosis among People Living with HIV in Ethiopia: A Systematic Review of Implementation and Impacts. International Journal of Environmental Research and Public Health. 2023; 20(1):621. https://doi.org/10.3390/ijerph20010621

Chicago/Turabian Style

Assefa, Dawit Getachew, Eden Dagnachew Zeleke, Delayehu Bekele, Dawit A. Ejigu, Wondwosen Molla, Tigist Tekle Woldesenbet, Amdehiwot Aynalem, Mesfin Abebe, Andualem Mebratu, and Tsegahun Manyazewal. 2023. "Isoniazid Preventive Therapy for Prevention of Tuberculosis among People Living with HIV in Ethiopia: A Systematic Review of Implementation and Impacts" International Journal of Environmental Research and Public Health 20, no. 1: 621. https://doi.org/10.3390/ijerph20010621

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