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Public health
Original research
Test negative case–control study of COVID-19 vaccine effectiveness for symptomatic SARS-CoV-2 infection among healthcare workers: Zambia, 2021–2022
  1. Oliver Mweso1,2,
  2. John Simwanza1,3,
  3. Warren Malambo4,
  4. Dabwitso Banda3,
  5. Sombo Fwoloshi5,
  6. Nyambe Sinyange3,
  7. Young M Yoo6,
  8. Leora R Feldstein6,
  9. Muzala Kapina3,
  10. Lloyd B Mulenga7,8,
  11. Mazyanga Mazaba Liwewe3,
  12. Kunda Musonda3,
  13. Nathan Kapata3,
  14. Francis Dien Mwansa5,
  15. Simon Agolory4,
  16. Patricia Bobo5,
  17. Jonas Hines4,
  18. Roma Chilengi3
  1. 1Zambia Field Epidemiology Training Program, Lusaka, Zambia
  2. 2Ministry of Health, Lusaka, Zambia
  3. 3Zambia National Public Health Institute, Lusaka, Zambia
  4. 4US Centers for Disease Control and Prevention, Lusaka, Zambia
  5. 5Zambia Ministry of Health, Lusaka, Zambia
  6. 6US Centers for Disease Control and Prevention, Atlanta, USA
  7. 7Levy Mwanawasa Medical University and University Teaching Hospitals, Lusaka, Zambia
  8. 8Ministry of Health, Government of the Republic of Zambia, Lusaka, Zambia
  1. Correspondence to Dr Oliver Mweso; oli.mweso{at}yahoo.com

Abstract

Objectives The study aim was to evaluate vaccine effectiveness (VE) of COVID-19 vaccines in preventing symptomatic COVID-19 among healthcare workers (HCWs) in Zambia. We sought to answer the question, ‘What is the vaccine effectiveness of a complete schedule of the SARS-CoV-2 vaccine in preventing symptomatic COVID-19 among HCWs in Zambia?’

Design/setting We conducted a test-negative case–control study among HCWs across different levels of health facilities in Zambia offering point of care testing for COVID-19 from May 2021 to March 2022.

Participants 1767 participants entered the study and completed it. Cases were HCWs with laboratory-confirmed SARS-CoV-2 and controls were HCWs who tested SARS-CoV-2 negative. Consented HCWs with documented history of vaccination for COVID-19 (vaccinated HCWs only) were included in the study. HCWs with unknown test results and unknown vaccination status, were excluded.

Primary and secondary outcome measures The primary outcome was VE among symptomatic HCWs. Secondary outcomes were VE by: SARS-CoV-2 variant strains based on the predominant variant circulating in Zambia (Delta during May 2021 to November 2021 and Omicron during December 2021 to March 2022), duration since vaccination and vaccine product.

Results We recruited 1145 symptomatic HCWs. The median age was 30 years (IQR: 26–38) and 789 (68.9%) were women. Two hundred and eighty-two (24.6%) were fully vaccinated. The median time to full vaccination was 102 days (IQR: 56–144). VE against symptomatic SARS-CoV-2 infection was 72.7% (95% CI: 61.9% to 80.7%) for fully vaccinated participants. VE was 79.4% (95% CI: 58.2% to 90.7%) during the Delta period and 37.5% (95% CI: −7.0% to 63.3%) during the Omicron period.

Conclusions COVID-19 vaccines were effective in reducing symptomatic SARS-CoV-2 among Zambian HCWs when the Delta variant was circulating but not when Omicron was circulating. This could be related to immune evasive characteristics and/or waning immunity. These findings support accelerating COVID-19 booster dosing with bivalent vaccines as part of the vaccination programme to reduce COVID-19 in Zambia.

  • COVID-19
  • epidemiology
  • public health
  • respiratory medicine (see thoracic medicine)
  • case-control studies
  • epidemiologic studies

Data availability statement

No data are available. No additional data available.

http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/bmjopen-2023-072144

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    Strengths and limitations of this study

    • The study design used in this study has been well described in influenza vaccine evaluation, and it can be used in post-introduction vaccine evaluation for SARS-CoV-2.

    • All health facilities, private and public, in Zambia were eligible for participation in the study hence there was no selection bias to easily accessible public health facilities.

    • Healthcare worker of any job classification in any department were eligible for enrolment, regardless of exposure to patients or vaccination status (as long as status was known).

    • No genomic sequencing was done to determine lineage, hence we could only associate vaccine effectiveness to the predominant variant in the country at the time of the study.

    • Additionally, self-reported vaccination status could have resulted in misclassification of the exposure because of social desirability bias for being vaccinated; however, we encouraged participants to report data from their vaccination card and verified vaccination status of some participants in the national COVID-19 vaccine registry in Zambia.

    Introduction

    COVID-19 vaccines have demonstrated good real-world effectiveness at reducing SARS-CoV-2 infections and preventing hospitalisations, and mortality in the western world.1 2 However, variants continue to emerge with immune evading capabilities; for example, the Omicron variants can escape neutralisation with vaccine-induced antibodies.3 However, little evidence of vaccine effectiveness (VE) has been reported from countries in Africa, where SARS-CoV-2 epidemiology has varied compared with other regions of the world.1 2

    A limited number of studies have been done on COVID-19 vaccines in countries in Africa. The Ad26.COV2.S vaccine was associated with lower hospitalisations and mortality during the Beta and Delta variant waves in South Africa,4 and additional evidence demonstrated effectiveness of this vaccine against COVID-19 hospitalisations during the Omicron variant wave.5 In Zambia, full receipt of a primary COVID-19 vaccine was associated with lower SARS-CoV-2 infections and symptomatic illness during an outbreak in a prison when Omicron was the dominant variant,6 and receipt of ≥1 vaccine dose was associated with lower progression to in-hospital mortality.7

    The Ministry of Health in Zambia used a nine-pronged approach to control and prevent the outbreak of COVID-19 from spreading further. This was after inclusion of the COVID-19 vaccination strategy. The strategies included: (1) surveillance and case finding; (2) case management; (3) infection prevention and control; (4) risk communication and community engagement; (5) laboratory diagnosis; (6) logistics and supply chain management; (7) appropriate, competent and adequate workforce; (8) routine essential health services; and (9) COVID-19 vaccination.8 The COVID-19 vaccination programme was approved in Zambia on the 24 March 2021. The vaccines were administered cautiously and in a phased-up manner and on a pilot and voluntary basis. Healthcare workers (HCWs) were prioritised to receive vaccines expeditiously; the police, security, teachers, traditional leaders, clergy and immigration 0fficers as well, as these are essential to maintaining core societal functions. Others included marketers, traders, including bus and truck drivers involved in cross border business, in view of the environment they work in. Those older than 65 years old including those with chronic illnesses were also prioritised as they were at greatest risk of severe illness and death. There was no mandatory vaccination.8

    Vaccines first became available in Zambia in mid-April 2021 and over 8.2 million (75.6%) of eligible persons have been fully vaccinated through 31 October 2022.9 ChAdOx1-S COVID-19 vaccine was the first vaccine product available in Zambia and by late 2021, Ad26.COV2.S, mRNA-127, BNT162b2 and Sinopharm BBIBP-CorV were available in the country. An additional vaccine dose (ie, ‘booster’) after completing a primary vaccine series became available in Zambia in January 2022.

    HCWs are at elevated risk of contracting SARS-CoV-2 during their interactions with patients with potential SARS-CoV-2 infection.10 A key component of controlling the pandemic and protecting the Zambian HCW is deployment of a safe and effective COVID-19 vaccine. However, vaccination rates among HCWs in countries in Africa have been low; for instance, through November 2021, the WHO estimated only 1.3 million (27%) of HCWs in Africa had been fully vaccinated.11 In Zambia, administrative data estimated much higher coverage, with 237 318 (99%) HCWs having been fully vaccinated through August 2022. Among a convenience sample of HCWs in Zambia, estimated coverage was 90%.12 Understanding VE from countries in Africa is important since most studies have been conducted in other regions of the world. We sought to measure VE among HCWs in Zambia.

    Methods

    We conducted a test-negative case–control COVID-19 VE study among HCWs from May 2021 to March 2022 in Zambia. HCW participants were identified through review of routine SARS-CoV-2 testing data in Zambia from May 2021 through March 2022. Data on relative variant genome frequency by region from GISAID (Global Initiative on Sharing Avian Influenza Data) were used to define the SARS-CoV-2 variant that was circulating during each wave.13

    District health officers provided line lists to the study team of HCWs in their districts who were recently symptomatic and tested for COVID-19-like illness. Additionally, the study team members inspected national testing data for HCWs who tested for SARS-CoV-2 by PCR or rapid antigen tests. Trained data collectors contacted HCWs by phone or in-person at health facilities to invite them to complete the study questionnaire. Potential HCW participants were contacted up to six times. Data collectors administered a standardised questionnaire that included information on demographics, medical history (including COVID-19 vaccination status and self-reported prior SARS-CoV-2 infection) and COVID-19 preventive measures (like mask use and hand hygiene). COVID-19 vaccination status was collected from self-report, with review of written documentation (ie, vaccine cards) when available. Additionally, a subset of participants’ vaccination status was verified in the national register if key variables (vaccine type, dose dates) were not available during the interview. All participants provided informed consent. This study was approved by the Zambia National Health Research Authority (see protocol- online supplemental file 2). The activity was reviewed by US Centers for Disease Control and Prevention (CDC) and was conducted consistent with applicable federal law and CDC policy. (See eg, 45 C.F.R. part 46.102(l),2 21 C.F.R. part 56; 42 U.S.C. §241(d); 5 U.S.C. §552a; 44 U.S.C.3501 et seq.)

    HCWs included all paid and unpaid persons serving in healthcare settings who had the potential for direct or indirect exposure to patients or infectious materials. HCW roles/cadres in this study included: nurses (nurse practitioners, general nurses, mid-wives, registered nurses), allied health staff (HCWs distinct from optometry, dentistry, nursing, medicine, clinical psychology and pharmacy, eg, anaesthesiologist assistant, perfusionist, radiographers), clinicians (HCWs in clinical practice of optometry, dentistry, medicine, ie, resident physicians, medical licentiates, clinical officers, clinical students), administrative staff (managers and administrators, clerks, office orderlies, human resource personnel, accounts staff, secretaries), non-clinical workers (cleaners, chaplain, food handlers/cafeteria staff) and other (any classification outside the mentioned categories, eg, community health workers, health science students). Cases were HCWs with symptomatic laboratory-confirmed SARS-CoV-2 infection; controls were HCWs with COVID-19-like illness (CLI) who tested SARS-CoV-2 negative. (CLI was defined as any acute illness characterised by fever, chills, cough, dyspnoea, myalgia, chills, rigours, headache, anosmia, ageusia, sore throat, coryza/rhinorrhoea, congestion, fatigue, general weakness, anorexia, nausea, vomiting, diarrhoea or altered mental status).14 15

    Patient and public involvement

    Patients (HCWs) were not involved in the setting of research priorities, defining research questions and outcome measures, providing input into study design and conduct, dissemination of results and evaluation of studies.

    Full vaccination was defined as having received the first dose of a one-dose vaccine or second dose of a two-dose vaccine ≥14 days before SARS-CoV-2 testing. Partial vaccination was defined as having received only the first dose of a two-dose vaccine ≥14 days before SARS-CoV-2 testing or receiving the second dose ≤13 days before testing. HCWs were deemed to have an indeterminate vaccination status if they received their first dose 0–13 days before testing and unknown vaccination status if the product type or dose dates of COVID-19 vaccine were unknown.

    Categorical demographic characteristics of participants by case/control status were compared using a two-sided Pearson χ2 test to assess for statistical significance. Age, described as a continuous variable, was compared between cases and controls using Wilcoxon rank-sum test as it was not normally distributed. Mixed-effects logistic regression was used to compare the odds of being partially or fully vaccinated against COVID-19 among symptomatic SARS-CoV-2 cases versus controls, adjusting for sex, age, number of comorbidities and province (random-effects term). VE was calculated as 1 minus the adjusted OR multiplied by 100. VE by vaccination status for participants whose vaccination status was unknown were excluded from the analyses as the sample sizes were inadequate for meaningful analyses. Additionally, we did a stratified analyses based on the predominant strain circulating in Zambia (Delta from May to November 2021, Omicron from December 2021 to March 2022) and vaccine type (only for ChAdOx1-S and Ad26.COV2.S vaccines because other vaccine types had small sample sizes).

    We did a sensitivity analysis excluding unvaccinated participants who reported prior SARS-CoV-2 infection to account for potential misclassification of immunity status. Although the study procedures emphasised recruiting only symptomatic HCWs, data collectors relied on data sources that sometimes did not always contain information about clinical course to identify HCWs for recruitment (ie, line lists of HCWs who recently tested for SARS-CoV-2 within a given district and laboratory test results spreadsheets). Thus, some HCWs who were contacted and interviewed reported having asymptomatic SARS-CoV-2 infections only; we therefore conducted a secondary analysis including all HCW participants regardless of symptom status (online supplemental appendix).

    Results

    Between May 2021 and March 2022, 1919 HCWs were approached for study participation, of whom 1767 (92.1%) consented to participate and had test dates since May 2021 (43 refused participation, 1 participant with unknown test result and 108 had test dates before May 2021). Of the total number of HCWs, 1145 (64.8%) had CLI (figure 1).

    Figure 1
    Figure 1

    Recruitment flow diagram for the healthcare worker COVID-19 vaccine effectiveness study in Zambia, May 2021 to March 2022. HCWs, healthcare workers.

    The median age of symptomatic HCWs was 30 years (IQR: 26–38), and 789 (68.9%) were women (table 1). Most participants (67.4%) were from Lusaka province, in which the capital city is located, and allied HCWs comprised the largest (40.0%) HCW cadre (table 1). The overall prevalence of any chronic comorbidities was 14.7%; hypertension (6.4%) and HIV (3.6%) were the most commonly reported comorbidities. One hundred and sixty-seven HCWs (14.6%) reported prior SARS-CoV-2 infections. Twenty-one (1.8%) HCWs had been hospitalised for their illness and none had died.

    View this table:
    Table 1

    Demographic characteristics of symptomatic participants by case/control status for the healthcare worker COVID-19 vaccine effectiveness study in Zambia, May 2021 to March 2022

    Of the 1145 symptomatic HCWs, 130 (11.4%) were partially vaccinated while 282 (24.6%) were fully vaccinated. There were two distinct waves of recruitment in this study that corresponded with the periods of Delta variant predominance and Omicron variant predominance in Zambia (figure 2). Full vaccination coverage was highest among allied HCWs (27.9%) and lowest among clinicians (19.0%) (table 2). Vaccine coverage increased with time (figure 3). Only 6 (0.5%) had reported receiving an additional dose (ie, booster) beyond the primary series. The median time since full vaccination was 102 days (IQR: 56–144); this was 46 days (IQR: 25–80) during the Delta predominant period and 111 days (IQR: 69–154) during the Omicron predominant period. Among symptomatic HCWs, there were 509 (44.5%) cases (ie, tested SARS-CoV-2 positive) and 636 (55.5%) controls. Sixty-two (12.2%) HCWs with SARS-CoV-2 (cases) were fully vaccinated, compared with 220 (34.6%) HCWs with CLI but who were SARS-CoV-2 test negative (p=0.001). Few, 21, HCWs were hospitalised but those with COVID-19 (cases) were more likely to be admitted (3.7% vs 0.3%, p<0.01; table 1) than those with a negative SARS-CoV-2 test (controls).

    View this table:
    Table 2

    Vaccination coverage among symptomatic healthcare workers in the healthcare worker COVID-19 vaccine effectiveness study in Zambia, May 2021 to March 2022

    Figure 2
    Figure 2

    Weekly number of cases (positive) and controls (negative) among healthcare workers in Zambia, May 2021 to March 2022. *Incidence of SARS-CoV-2 testing by PCR and Rapid Antigen tests. ~Positive: refers to a positives SARS-Cov-2 test result by PCR or Rapid Antigen test; Negative: refers to a negative SARS-Cov-2 test result by PCR or Rapid Antigen test.

    Figure 3
    Figure 3

    Vaccine coverage by month for the healthcare worker COVID-19 vaccine effectiveness study in Zambia, May 2021 to March 2022.

    Adjusted VE against symptomatic SARS-CoV-2 was 72.7% (95% CI: 61.9% to 80.7%) for fully vaccinated HCWs and 23.1% (95% CI: −14.7% to 48.5%) for partially vaccinated (table 3). VE during the Delta predominant period was 79.4% (95% CI: 58.2% to 90.7%) and the Omicron predominant period was 37.5% (95% CI: −7.0% to 63.3%) for fully vaccinated HCWs. VE for ChAdOx1-S vaccine was 87.0% (95% CI: 74.4% to 93.7%) and for Ad26.COV2.S vaccine was 68.2% (95% CI: 48.0% to 80.8%) for fully vaccinated HCWs. A similar pattern of VE was observed when the outcome variable was any SARS-CoV-2 infection (online supplemental appendix table 1). After excluding unvaccinated HCWs who reported a prior SARS-CoV-2 infection, VE against symptomatic SARS-CoV-2 was 69.9% (95% CI: 57.5% to 78.9%) for fully vaccinated participants over the complete study period (online supplemental appendix table 2). Among 19 persons with COVID-19 (ie, cases) who were hospitalised, none (0.0%) were fully vaccinated, 2 (10.5%) were partially vaccinated, 1 (5.3%) had an indeterminate vaccination status and 16 (84.2%) were unvaccinated.

    View this table:
    Table 3

    SARS-CoV-2 vaccine effectiveness estimates for symptomatic SARS-CoV-2 infection in the healthcare worker COVID-19 vaccine effectiveness study in Zambia, May 2021 to March 2022

    Discussion

    COVID-19 vaccines were effective at preventing symptomatic SARS-CoV-2 among HCWs in Zambia during the period when the Delta variant was dominant in the country. The VE estimate decreased when the Omicron variant became predominant, which could be related to waning immunity and/or immune evasive mutations in the virus.16–18 In a US-based study, VE after receipt of both two and three doses was lower during the Omicron-predominant than during the Delta-predominant period at all time points evaluated. During both periods, VE after receipt of a third dose was higher than that after a second dose; however, VE waned with increasing time since vaccination.17 These findings of increasing VE following additional vaccine doses have been evidenced in other studies done in the western world.16 19 That most vaccinated HCWs in this study had only received the complete primary vaccine series could point to the need to increase booster vaccination coverage in Zambia, as an additional vaccine dose has been shown to strengthen immunity against SARS-CoV-2 variants.19 Moreover, most HCWs in this study had not been vaccinated at all (although recent progress in Zambia points to improving coverage). Perceptions about vaccine safety and efficacy were the strongest predictors of vaccine acceptance for adult COVID-19 vaccination20; bad perceptions potentially explaining the low vaccination rates. Perception of COVID-19 disease severity as well were especially strong predictors of vaccine uptake,20 and bad perceptions likely leading to poor uptake. Although many people in Zambia have likely had SARS-CoV-2 infection (potentially offering some immunity), vaccination offers additional protection after natural infection.21–24 The findings in this study provide important evidence about VE in Africa. Few countries in Africa have reported on COVID-19 VE, which is an important question considering the sizeable financial and human resources going toward increasing vaccine coverage on the continent.

    Omicron variant caused a large wave in December 2021 to February 2022. The findings from our study suggest that vaccination might not have reduced symptomatic infections during this period, although data from Zambia indicate vaccination protected people against severe disease during this wave.25 Our findings that vaccination was not associated with lower odds of symptomatic COVID-19 during the Omicron period, contrasts with findings from a COVID-19 outbreak in a prison in Zambia in December 2021.6 In that study, full vaccination was associated with 72.9% effectiveness for symptomatic COVID-19. Timing of vaccine receipt could account for this difference, as the median time since full vaccination was 102 days in this current study compared with much more recent vaccination (ie, <2 months) in the other study (Simwanza et al). The longer time since vaccination among HCWs could reflect that this group was prioritised for vaccination at the outset of the national campaign given their elevated risk of exposure to the virus. Beyond waning immunity, the Omicron variant of SARS-CoV-2 has mutations that enable it to evade prior immunity, both vaccine-induced and natural immunity.26–28 Furthermore, it has been similarly observed in other study findings that Ad26.COV2.S vaccines (majorly administered in the Omicron variant predominant period in our study) have diminished effect against the Omicron variant.19 Our findings are consistent with current understanding of immunity against SARS-CoV-2.19 26–28

    HCWs with COVID-19 had a higher proportion of hospitalisation than controls, consistent with relatively greater severity of SARS-CoV-2 infection compared with some other respiratory viruses that can cause CLI. Our findings of more hospitalisation among HCWs with COVID-19 who were not fully vaccinated further emphasises the importance of vaccines in strengthening immunity against severe disease.25

    Since this study was done, Zambia has made substantial strides in increasing full vaccination coverage among eligible persons (aged ≥12 years). By the end of October 2022, Zambia had fully vaccinated ~76% of persons aged ≥12 years.9 This is a major achievement considering that just 5% persons were fully vaccinated in October 2021. However, booster vaccine coverage among Zambians remains low (36%), highlighting the need for ongoing COVID-19 vaccination efforts in the country.

    Our study had strengths and limitations. The study design used in this study has been well described in influenza vaccine evaluation, and it can be used in post-introduction vaccine evaluation for SARS-CoV-2. All health facilities, private and public, in Zambia were eligible for participation in the study hence there was no selection bias to easily accessible public health facilities. HCW of any job classification in any department were eligible for enrolment, regardless of exposure to patients or vaccination status (as long as status was known). Many participants were partially vaccinated and the sample size for fully vaccinated HCWs was small, resulting in wide CIs for our primary objective of assessing full vaccination. No genomic sequencing was done to determine lineage, hence we could only associate VE to the predominant variant in the country at the time of the study.3 Additionally, self-reported vaccination status could have resulted in misclassification of the exposure because of social desirability bias for being vaccinated; however, we encouraged participants to report data from their vaccination card and verified vaccination status of some participants in the national COVID-19 vaccine registry in Zambia. Because so few participants had a booster dose, we could not assess VE for this vaccination status.

    COVID-19 vaccination protected HCWs from symptomatic SARS-CoV-2 infections in Zambia during the Delta wave. Considering ongoing need for COVID-19 vaccine delivery in Zambia, where possible, COVID-19 vaccination could be integrated into other healthcare services to improve efficiency in under-resourced health systems like in Zambia.29 Examples of existing platforms include vaccination in HIV care clinics supported by the US President’s Emergency Plan for AIDS Relief, routine antenatal care services, for inpatients prior to discharge from the hospital, or into Expanded Programme on Immunisation programmes such as mass measles or polio vaccination campaigns. New SARS-CoV-2 variants are predicted to emerge,27 30 and thus having an ongoing ability to conduct VE studies in Zambia will be useful. Platforms like severe acute respiratory infection surveillance can provide this information, since studies like this are resource intensive.31 In addition, there is need to conduct immunological studies to ascertain that COVID-19 vaccines induce appropriate immune responses in Zambia, alongside clinical evaluation of outcomes as was done in this study. These findings support the acceleration of COVID-19 vaccination programmes in Zambia to reach high coverage, especially for booster vaccine doses in people who have finished their primary series months ago.

    Data availability statement

    No data are available. No additional data available.

    Ethics statements

    Patient consent for publication

    Ethics approval

    This study involves human participants and was approved by Zambia National Health Research Authority, Reference number: NHREB0001/20/05/2021. Participants gave informed consent to participate in the study before taking part.

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    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    Footnotes

    • Contributors OM led the study and each process of the study development, that is, protocol for the study, implementation of the study, designing data collection tools, monitoring data collection for the whole study, writing the statistical analysis plan, cleaning and analysing the data (preliminary analysis) and drafting and revising the paper and its submission. JS was co-lead and shared these tasks with OM. DB assisted in developing the protocol for this study. SF assisted in developing the protocol for this study, implementing the study, designing data collection tools and monitoring data collection for the whole study. WM developed the protocol for this study, implemented the study, designed data collection tools, monitored data collection for the whole study, wrote the statistical analysis plan, cleaned and provided technical expertise on the data analysis, drafting and revising the manuscript. MML provided guidance in developing the protocol for this study and its implementation. NS initiated the collaborative project, provided guidance in developing the protocol for this study and its implementation. JH initiated the collaborative project, developed the protocol for this study, implemented the study, designed data collection tools, monitored data collection for the whole study, wrote the statistical analysis plan, cleaned and analysed the data (preliminary analysis) and drafted and revised the paper. OM is guarantor. LRF and YMY did a comprehensive analysis of the data. MK analysed the data and revised the paper. LBM initiated the collaborative project, analysed the data and revised the paper. KM analysed the data and revised the paper. NK analysed the data and revised the paper. FDM analysed the data and revised the paper. SA analysed the data and revised the paper. PB analysed the data and revised the paper. RC initiated the collaborative project, analysed the data and revised the paper.

    • Funding This evaluation has been supported in part by the President's Emergency Plan for AIDS Relief (PEPFAR) through the Centers for Disease Control and Prevention (CDC). Grant number/CoAg ID number: GH002234.

    • Competing interests None declared.

    • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.