Summary
Background
Tuberculosis remains an important clinical and public health issue in South Africa, which has one of the highest tuberculosis burdens in the world. We aimed to estimate the burden of bacteriologically confirmed pulmonary tuberculosis among people aged 15 years or older in South Africa.
Methods
This multistage, cluster-based, cross-sectional survey included eligible residents (age ≥15 years, who had slept in a house for ≥10 nights in the preceding 2 weeks) in 110 clusters nationally (cluster size of 500 people; selected by probability proportional-to-population size sampling). Participants completed face-to-face symptom questionnaires (for cough, weight loss, fever, and night sweats) and manually read digital chest X-ray screening. Screening was recorded as positive if participants had at least one symptom or an abnormal chest X-ray suggestive of tuberculosis, or a combination thereof. Sputum samples from participants who were screen-positive were tested by the Xpert MTB/RIF Ultra assay (first sample) and Mycobacteria Growth Indicator Tube culture (second sample), with optional HIV testing. Participants with a positive Mycobacterium tuberculosis complex culture were considered positive for bacteriologically confirmed pulmonary tuberculosis; when culture was not positive, participants with a positive Xpert MTB/RIF Ultra result with an abnormal chest X-ray suggestive of active tuberculosis and without current or previous tuberculosis were considered positive for bacteriologically confirmed pulmonary tuberculosis.
Findings
Between Aug 15, 2017, and July 28, 2019, 68 771 people were enumerated from 110 clusters, with 53 250 eligible to participate in the survey, of whom 35 191 (66·1%) participated. 9066 (25·8%) of 35 191 participants were screen-positive and 234 (0·7%) were identified as having bacteriologically confirmed pulmonary tuberculosis. Overall, the estimated prevalence of bacteriologically confirmed pulmonary tuberculosis was 852 cases (95% CI 679–1026) per 100 000 population; the prevalence was highest in people aged 35–44 years (1107 cases [95% CI 703–1511] per 100 000 population) and those aged 65 years or older (1104 cases [680–1528] per 100 000 population). The estimated prevalence was approximately 1·6 times higher in men than in women (1094 cases [95% CI 835–1352] per 100 000 population vs 675 cases [494–855] per 100 000 population). 135 (57·7%) of 234 participants with tuberculosis screened positive by chest X-ray only, 16 (6·8%) by symptoms only, and 82 (35·9%) by both. 55 (28·8%) of 191 participants with tuberculosis with known HIV status were HIV-positive.
Interpretation
Pulmonary tuberculosis prevalence in this survey was high, especially in men. Despite the ongoing burden of HIV, many participants with tuberculosis in this survey did not have HIV. As more than half of the participants with tuberculosis had an abnormal chest X-ray without symptoms, prioritising chest X-ray screening could substantially increase case finding.
Funding
Global Fund, Bill & Melinda Gates Foundation, USAID.
Introduction
National strategic plan for HIV, TB and STIs 2017–2022.
South Africa was among the first countries to adopt and implement rapid molecular diagnosis with Xpert MTB/RIF assay technology.
TB GeneXpert.
Furthermore, there are activities in the country to increase awareness about tuberculosis transmission and symptoms to drive screening and testing and improve case finding through various programmes, such as the Cheka Impilo and Welcome Back campaigns.
The national wellness campaign: Cheka Impilo.
,
DOH/PEPFAR best practices meeting: HIV patient linkage and return to care.
There is now a clear, consistent, and sustained downward trend in tuberculosis case notifications in South Africa, which is partly explained by high antiretroviral therapy (ART) coverage, with 62·3% of people living with HIV receiving ART in 2017.
- Simbayi LC
- Zuma K
- Zungu N
- et al.
,
Global tuberculosis report 2018.
However, the tuberculosis burden remains high, with an incidence estimated by WHO of 322 cases (95% CI 230–428) per 100 000 population in 2017, which placed South Africa as having one of the highest tuberculosis and tuberculosis and HIV co-infection burdens in the world.
Global tuberculosis report 2018.
Evidence before this study
South Africa is one of the 30 countries with high tuberculosis burden that, in 2020, collectively contributed to 86% of the estimated incident cases worldwide. The 2020 global tuberculosis report showed a large difference in the modelled estimates of the disease burden reported by WHO compared with the number of notified tuberculosis cases started on treatment. We searched PubMed for original research articles on national tuberculosis prevalence surveys in South Africa published in English between Jan 1, 2000, and Dec 31, 2020, using the terms ((“South Africa” AND (“2000/01/01”[PDat] : “2020/12/31”[PDat]))) AND (“tuberculosis prevalence” AND (“2000/01/01”[PDat] : “2020/12/31”[PDat])). We found no national-level population-based studies.
Added value of this study
This study refined the national estimate of the burden of pulmonary tuberculosis in South Africa and identified population groups in whom tuberculosis was underdiagnosed or under-reported. The survey found a high burden of tuberculosis, with a bimodal peak driven by HIV and recurrence of tuberculosis. Key diagnostic and reporting gaps were identified in young people (age 15–24 years), men, and older adults (age 65 years or older). Chest X-ray was identified as a key screening tool for increasing tuberculosis detection because many people with tuberculosis identified by chest X-ray did not report symptoms. In addition, as this was one of the first countries to use both Mycobacteria Growth Indicator Tube culture and Xpert MTB/RIF Ultra in a national tuberculosis prevalence survey, this study provided new insights into the use of Xpert MTB/RIF Ultra, resulting in a more nuanced case definition.
Implications of all the available evidence
The South African national tuberculosis control programme can develop more targeted interventions to address key gaps for greater impact in addressing the tuberculosis burden and consider adapting the current screening algorithm to include chest X-rays, to identify tuberculosis in those who are asymptomatic (ie, subclinical tuberculosis) or do not report typical symptoms. Future research should examine the effect of Mycobacterium tuberculosis infection in people who do not report symptoms on the overall burden of tuberculosis. Although Xpert MTB/RIF Ultra is a highly useful tool in tuberculosis prevalence surveys, it should be used in conjunction with culture because of the high false-positivity and low positive predictive value in active case finding (in screening populations with low prevalence of disease compared with those who present to health-care facilities). Therefore, an appropriate case definition considering all these factors is fundamental, with consideration of the different context from clinical settings.
We aimed to estimate the prevalence of bacteriologically confirmed pulmonary tuberculosis among people aged 15 years or older in South Africa and improve the understanding of tuberculosis epidemiology for evidence-based control efforts.
Methods
Study design and participants
Tuberculosis prevalence surveys: a handbook.
We included 110 clusters, which were proportionally divided by population size across three strata in South Africa’s nine provinces based on tuberculosis prevalence (low, medium, high) from 2013 notification data.
Global tuberculosis report 2014.
Within each stratum, clusters were selected by means of multistage probability proportional-to-population size sampling, which was applied at provincial, district, and then subdistrict levels (figure 1). In each cluster, people aged 15 years or older who had slept in a house for at least 10 nights in the preceding 2 weeks were eligible to participate. No areas of the country were excluded from the sampling frame.
Figure 1South African national tuberculosis prevalence survey map
Black lines delineate provinces. The three strata are based on 2013 notification data. Stratum 1 (low tuberculosis prevalence) accounted for 38 clusters (Gauteng and Limpopo), stratum 2 (medium prevalence) had 29 clusters (KwaZulu-Natal, Mpumalanga, and Free State), and stratum 3 (high prevalence) had 44 clusters (Northern Cape, Western Cape, North West, and Eastern Cape). Data source: Human Sciences Research Council, 2020.
The survey protocol was approved by the South African Medical Research Council Research Ethics Committee in January, 2017 (EC001 2/2012), with annual renewal until completion. Individual written informed consent or assent and parent or guardian consent for participants younger than 18 years was obtained at survey enrolment. As tuberculosis is a notifiable disease in South Africa, participants also consented to give identifiers (names, address, telephone number) to facilitate follow-up of sputum sample results. These details were kept confidential by survey staff. Participation was voluntary, and participants received in-kind reimbursement to the value of US$5 (50 South African Rand) for time spent on survey activities.
Medical officers made medical referrals to the nearest health facility whenever indicated on the basis of the clinical picture or chest X-ray findings. Bacteriologically positive results (and identifiers) were sent to the national tuberculosis control programme through the tuberculosis coordinator of each cluster for follow-up and treatment initiation.
Procedures
National tuberculosis management guidelines, South Africa.
). Participants then had digital chest X-ray screening, unless they declined or a chest X-ray could not be done because of disability or pregnancy. Chest X-rays were read on site by a medical officer and were classified as normal, abnormal suggestive of tuberculosis, or abnormal not suggestive of tuberculosis. Participants with any screening symptoms or a chest X-ray classified as abnormal suggestive of tuberculosis, or a combination thereof, and those who did not report symptoms and had no chest X-ray, were asked to provide two sputum samples for laboratory testing. The first sample was taken immediately and the second was taken 1 h later. Participants who provided sputum samples were offered an optional HIV test (dried blood spot) in addition to optional self-reported HIV status collected during the interview. Those who accepted HIV testing received a barcoded voucher to retrieve the HIV test result at a designated clinic in the cluster with the necessary pretest and post-test counselling.
Tuberculosis prevalence surveys: a handbook.
Specimen processing followed the manufacturers’ instructions and standard operating procedures. For each batch of samples processed for culture, an H37Rv strain was included as a positive control and a non-inoculated Mycobacterial Growth Indicator Tube (MGIT) was used as a negative control. The culture positivity rate of smear-positive samples was 95%, as determined by routine samples processed by the laboratory, and the survey samples’ contamination rate was 5·4%; both indicators were within acceptable limits.
Tuberculosis prevalence surveys: a handbook.
Xpert MTB/RIF Ultra results were recorded as positive, negative, trace, or invalid. If the test was unsuccessful, the specimen was retested for a final result. For this survey, an Xpert MTB/RIF Ultra trace result was considered negative for Mycobacterium tuberculosis complex. At the time of survey design, there were minimal data regarding trace results, except for Dorman and colleagues’
- Dorman SE
- Schumacher SG
- Alland D
- et al.
publication, which showed reduced specificity of Xpert MTB/RIF Ultra among those with trace results. In addition, trace results were not being reported as positive for M tuberculosis in the national tuberculosis programme, with which we aligned the survey results. Culture results were reported as positive, negative, or contaminated.
Dried blood spot samples were tested for HIV using a multiassay algorithm. Genscreen Ultra HIV Ag/Ab (BioRad, Hercules, CA, USA) was used as the screening assay. Specimens that showed a negative result were reported as negative, whereas those that showed a positive result were confirmed using the Murex HIV Ag/Ab Combination assay (Diasorin, Saluggia, Italy). Genscreen HIV-1 Western Blot assay (BioRad) was used in cases of discrepant results.
All chest X-rays classified by medical officers as abnormal suggestive of tuberculosis or abnormal not suggestive of tuberculosis, and 20% of those classified as normal, were read by an offsite radiologist as soon as possible. Discrepant readings were communicated to the medical officers, and sputum samples were collected where indicated if the survey team were still in that cluster and could easily access that participant again; otherwise the feedback guided future readings.
- Dorman SE
- Schumacher SG
- Alland D
- et al.
were also considered as positive for bacteriologically confirmed pulmonary tuberculosis. HIV status was based on the dried blood spot result or on self-reported status.
- Harris PA
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- et al.
,
- Harris PA
- Taylor R
- Thielke R
- Payne J
- Gonzalez N
- Conde JG
Centralised chest X-ray and laboratory data were captured directly onto REDCap. All data were backed up and linked into the central survey database. Data were cleaned throughout implementation, with final cleaning occurring before database lock.
Statistical analysis
The sample size of 55 000 people with a cluster size of 500 was based on the assumptions of smear-positive tuberculosis prevalence estimated at 300 cases per 100 000 population (prevalence was assumed to be less than notification at the time of study design, given that disease duration is short in a population with high HIV prevalence), relative precision of 20%, design effect of 1·44, and a participation rate of 85%.
Tuberculosis prevalence surveys: a handbook.
,
- Floyd S
- Sismanidis C
- Yamada N
- et al.
Specifically, cluster-level analysis and three individual-level logistic regression models were used. The model that was restricted to participants with multiple missing value imputation for individuals with missing outcome (the outcome variable that was imputed was tuberculosis status; ie, survey case, yes or no) and inverse probability weighting to represent all eligible individuals provided the single best estimate of tuberculosis prevalence at the population level. To avoid collinearity, and based on the number of observed survey cases, a finite number of the most important statistically independent variables was identified. The final imputation model to generate 25 datasets was defined using the following variables: stratum, age group, cough for longer than 2 weeks, past history of tuberculosis, HIV status, race, and sex (appendix pp 1–2). Survey prevalence was extrapolated to estimate prevalence for all forms of tuberculosis and for all ages in South Africa using WHO standard methodologies,
Tuberculosis prevalence surveys: a handbook.
and extrapolation was based on the proportion of the population that was younger than 15 years (29%), as per 2018 UN population estimates,
The world population prospects: 2015 revision.
the rate ratio of child to adult tuberculosis (0·6), and the proportion of notified tuberculosis cases that were extrapulmonary tuberculosis (9·7%), as reported by the national tuberculosis control programme for 2018.
Global tuberculosis report 2018.
As an approximate indicator of case detection,
the prevalence to case notification ratio was calculated by comparing prevalence rates with tuberculosis case notification rates of new and relapsed tuberculosis cases for the corresponding age groups and sex as reported by the national tuberculosis control programme for 2018. Data were analysed with STATA (version 15).
Role of the funding source
The funders of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report.
Results
Figure 2Study profile
*26 350 provided self-reported HIV status (21 895 were negative and 4455 were positive). † 2176 had dried blood spot samples submitted for HIV testing (1851 were negative and 325 were positive).
Table 1Survey participation by sex, age group, area of residence, and stratum
Table 2Screening outcomes by sex, age group, area of residence, strata, and HIV status
Data are n or n (%) unless otherwise stated. NA=not applicable.
965 (14·8%) of 6523 chest X-rays were read as not abnormal by medical officers but as abnormal suggestive of tuberculosis by a radiologist, and 197 (20·4%) of these participants submitted sputum samples as they were symptom-screen positive. 178 (0·5%) of 35 191 participants were on tuberculosis treatment at the time of the survey and 2964 (8·4%) reported receiving tuberculosis treatment previously. HIV status was known for 26 877 (76·4%) of 35 191 participants and 4588 (17·1%) were HIV-positive. 1647 (23·3%) of 7061 participants who were screen-positive with known HIV status were HIV-positive. Data on ART were not available.
Table 3Culture and Xpert MTB/RIF Ultra results among participants who were eligible for sputum analysis
Table 4Estimated prevalence of pulmonary tuberculosis in people aged 15 years or older, and prevalence to case notification ratios
Data are n (%) unless otherwise stated. Estimates are from the model using multiple imputation and inverse probability weighting.
Of 98 participants identified as having bacteriologically confirmed pulmonary tuberculosis who reported at least one symptom, 41 (41·8%) had sought care before the survey. Among these, eight (19·5%) participants had already been diagnosed with tuberculosis and started on treatment. Of the 57 (58·2%) participants who had not already sought care, 38 (66·6%) were planning to seek care, eight (14·0%) regarded their symptoms as trivial, eight (14·0%) had not sought care due to distance to the clinic, travel costs, or crowded clinics, and three (5·3%) did not report a specific reason.
Discussion
- Horton KC
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The prevalence to case notification ratio, a proxy of case-finding performance, indicated that the estimated number of undiagnosed or unreported tuberculosis cases was highest in people aged 15–24 years and those aged 65 years or older. Prevalence was highest in people aged 35–44 years and those aged 65 years or older. However, given the young population of South Africa, the number of cases in people aged 15–34 years represents a huge current and potentially future recurrent tuberculosis burden. Based on these survey data, post-survey incidence estimates for the main year of the survey (2018) were revised upwards by WHO to 677 cases (95% CI 472–919) per 100 000 population, albeit with considerable overlap in uncertainty intervals with the revised pre-survey estimate of 520 cases (373–692) per 100 000 population.
Global tuberculosis report 2020.
National tuberculosis prevalence surveys 2007–2016.
However, it further highlights the importance of including more sensitive screening tools (ie, chest X-rays) within active case-finding activities to increase the potentially earlier detection of tuberculosis cases, given their accuracy when compared with symptoms.
WHO consolidated guidelines on tuberculosis. Module 2: screening—systematic screening for tuberculosis disease.
Exclusion of chest X-ray screening, or a sequential serial positive screening algorithm starting with symptom screening, would have missed these cases. Reserving chest X-rays for only those without symptoms would have detected all cases, without the need for the 5168 chest X-rays done in participants who reported symptoms. This finding has important cost implications when considering active case-finding screening algorithms for tuberculosis programmes. It is also particularly noteworthy when attempting to reach groups such as men who might not readily report tuberculosis symptoms or participate in interventions perceived as lengthy or time consuming. Chest X-ray uptake in this survey was high, implying that, with clear ethical and safety protocols, chest X-ray screening could be widely acceptable in systematic screening in communities.
- Frascella B
- Richards AS
- Sossen B
- et al.
and where the observed impact of tuberculosis interventions is slow, such as in South Africa, where the rate of decline of tuberculosis incidence has decreased.
Global tuberculosis report 2018.
In our study, people who only had an abnormal chest X-ray were eight times more likely to have tuberculosis than those with symptoms only. Although these individuals might eventually be detected and treated, the detection delay might have an impact on transmission.
- Frascella B
- Richards AS
- Sossen B
- et al.
,
- Drain PK
- Bajema KL
- Dowdy D
- et al.
This detection delay is further exacerbated by patient and health system delays when such individuals become symptomatic. For example, in this survey, less than half of symptomatic individuals with tuberculosis reported seeking care. Even after seeking care, not all patients with tuberculosis successfully navigate and appropriately exit the tuberculosis care cascade.
- Naidoo P
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- et al.
- Simbayi LC
- Zuma K
- Zungu N
- et al.
people living with HIV are likely to have more opportunities to access and engage with the health system and to have symptoms detected and investigated, as evidenced by the higher tuberculosis and HIV co-infection rate reported by the national tuberculosis control programme (58·0%)
Global tuberculosis report 2018.
than in our survey (23·3%). Therefore, greater effort is required to reach those with tuberculosis who are HIV-negative in communities.
- Simbayi LC
- Zuma K
- Zungu N
- et al.
sputum collection rate, and other survey indicators should be explored, to limit the potential bias linked to missing data. However, estimates with different analytical models did not considerably vary, thus reducing the likelihood of any potential bias due to missing data. HIV testing was restricted to those eligible for sputum examination, and testing rates, although low, were consistent with other surveys in South Africa that also used dried blood spot samples; 52% of the eligible population were interviewed and tested in the Demographic and Health Survey (2016),
South Africa Demographic and Health Survey 2016.
, and the testing rate was only 61% in the fifth National HIV Survey (2017).
- Simbayi LC
- Zuma K
- Zungu N
- et al.
Universal rapid HIV testing could have increased testing uptake, giving a more accurate estimate of co-infection, opportunity for linkage to treatment for those testing positive, and integration of the tuberculosis and HIV programmes. Future surveys, especially those conducted in high-prevalence HIV settings, should include rapid HIV testing and mechanisms for linkage to treatment, consistent with international ethical standards. Although medical officers in this study were asked to increase the sensitivity of chest X-ray reading, some potential (albeit non-fulminant asymptomatic) cases might have been missed. Future surveys should plan central chest X-ray reading for all images, to maximise quality control of the chest X-ray reading process and gain a better estimate of the potential under-reading in the field.
- Mishra H
- Reeve BWP
- Palmer Z
- et al.
,
- Zifodya JS
- Kreniske JS
- Schiller I
- et al.
Xpert MTB/RIF Ultra might detect people who had tuberculosis previously, as well as those who had been infected but contained the infection and do not have active tuberculosis at the time of testing. Prevalence derived from only Xpert MTB/RIF Ultra would not equate to tuberculosis disease burden, but rather the prevalence of M tuberculosis DNA, which is likely to be an overestimation of disease burden, particularly in countries with high tuberculosis burdens. Culture, the diagnostic reference standard, also has its limits. False-negative cultures are possible in some samples with low bacterial load. Use of a low positive control in future surveys could provide information on the laboratories’ capability of culturing these samples and reduce the probability of false-negative results. However, satisfactory laboratory quality indicators in this survey suggest that false-negative results were minimal. Reasons for Xpert MTB/RIF Ultra-positive, culture-negative samples could therefore be a combination of the individual not having active disease (ie, having history of previous disease) as well as false-negative cultures in the presence of low bacterial load in the samples. We believe that by restricting the case definition to those with only an Xpert MTB/RIF Ultra-positive outcome (without a history of previous tuberculosis) identifies most people with tuberculosis who do not have culture confirmation. Although not everyone with a positive Xpert MTB/RIF Ultra result in this survey was classified as having tuberculosis, they were managed in accordance with national tuberculosis guidelines.
This study showed that tuberculosis remains an important public health issue in South Africa, due to a high tuberculosis burden and many undetected cases. Prevalence was higher in men than in women, more than half of those with tuberculosis did not report typical symptoms, and most cases were HIV-negative, possibly reflecting the great effect of a strong HIV programme to find and treat people with HIV with tuberculosis co-infection. Tuberculosis in young people (aged 15–24 years) and older adults (aged 65 years or older) was also largely undetected by the national tuberculosis control programme, indicating the need to improve engagement with and awareness in these population groups. Prioritising chest X-ray screening in case-finding strategies could potentially improve case detection. The use of molecular diagnostic tests in active case finding needs closer examination, given the possibility of providing false-positive results, especially in settings with high tuberculosis burden. Targeted interventions with more effective demand-creation strategies are recommended to increase health-care seeking, especially among people with symptoms.
Contributors
SMo, FI, MVdw, NI, NM, SD, TM, LM, DM, IL, SMa, CS, KZ, and YP were involved in the design of the survey. SMo, FI, MVdw, NI, NM, SD, JC, OO, IS, TM, and PX were involved in the implementation of the survey procedures. SMo, PM, IS, NI, KZ, TM, and IL did the data curation. SMa, CS, and IL did the statistical analysis. IL, SMa, CS, and PM accessed and verified all the data. SMo, FI, MVdw, NM, TM, IL, JC, and MT wrote the first draft of the manuscript. SMo, FI, MVdw, NI, NM, SD, TM, JC, IS, LM, DM, IL, SMa, MT, CS, KZ, and YP interpreted the data and provided intellectual input, including editing and reviewing the final draft of the manuscript. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication.
Data sharing
Individual, deidentified participant data, including data dictionaries, may be shared. Templates of the informed consent forms may be shared upon request. The data will be available following publication, with no end date, and will be shared with anyone who wishes to access them with a clear data sharing agreement, for any purpose of analyses. For data access, please contact the corresponding author and the tuberculosis programme at the National Department of Health in South Africa.
Declaration of interests
We declare no competing interests.
Acknowledgments
This paper is dedicated to the memory of Dr Patrick Hazangwe, medical officer of WHO South Africa, who was an active and passionate member of the survey team. He also supported the national tuberculosis prevalence surveys in Lesotho and Zimbabwe. We acknowledge all the staff and the various stakeholders who supported the study and the field staff who were key in the implementation of this survey. This study was funded by the Global Fund, the Bill & Melinda Gates Foundation, and USAID. The authors alone are responsible for the views expressed in this publication, and they do not necessarily represent the views, decisions, or policies of their organisations.
Supplementary Material
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DOI: https://doi.org/10.1016/S1473-3099(22)00149-9
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- The state of tuberculosis in South Africa: what does the first national tuberculosis prevalence survey teach us?
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South Africa is among WHO’s list of 30 high-burden tuberculosis countries and has one of the highest incidence rates of notified tuberculosis in the world.1 In The Lancet Infectious Diseases, Sizulu Moyo and colleagues2 report their findings from the first national tuberculosis prevalence survey in South Africa, which is a very important study that provides improved understanding of the true extent of tuberculosis and helps to identify groups who might be underserved by health services and where tuberculosis might be undiagnosed.
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