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SAMJ: South African Medical Journal

versão On-line ISSN 2078-5135
versão impressa ISSN 0256-9574

SAMJ, S. Afr. med. j. vol.110 no.12 Pretoria Dez. 2020 



Opportunities from a new disease for an old threat: Extending COVID-19 efforts to address tuberculosis in South Africa



M LovedayI, II; H CoxIII; D EvansIV; J FurinV; N NdjekaVI; M OsmanVII; K NaidooVIII

IPhD; HIV Prevention Research Unit, South African Medical Research Council, KwaZulu-Natal, South Africa
IIPhD; Centre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, College of Health Sciences, University of KwaZulu-Natal Durban, South Africa; and South African Medical Research Council-CAPRISA HIV-TB Pathogenesis and Treatment Research Unit, Doris Duke Medical Research Institute, University of KwaZulu-Natal Durban, South Africa
IIIPhD; Institute for Infectious Disease and Molecular Medicine and Wellcome Centre for Infectious Disease Research in Africa, University of Cape Town, South Africa
IVDTech Biomed; Health Economics and Epidemiology Research Office, Department of Internal Medicine, School of Clinical Medicine, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
VMD, PhD; Department of Global Health and Social Medicine, Harvard Medical School, Boston, USA
VIMMed (Fam Med); Drug-Resistant Tuberculosis, TB and HIV Directorate, National Department of Health, South Africa
VIIMB ChB, PG Dip Health Management, MSc Epidemiology; Desmond Tutu TB Centre, Department of Paediatrics and Child Health, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa
VIIIMB ChB, PhD; Centre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, College of Health Sciences, University of KwaZulu-Natal Durban, South Africa; and South African Medical Research Council-CAPRISA HIV-TB Pathogenesis and Treatment Research Unit, Doris Duke Medical Research Institute, University of KwaZulu-Natal Durban, South Africa





The COVID-19 pandemic and phased nationwide lockdown have impacted negatively on individuals with tuberculosis (TB) and routine TB services. Through a literature review and the perspective of members of a national TB Think Tank task team, we describe the impact of the pandemic and lockdown on TB patients and services as well as the potential long-term setback to TB control in South Africa (SA). Strategies to mitigate risk and impact are explored, together with opportunities to leverage synergies from both diseases to the benefit of the National TB Programme (NTP). With the emergence of COVID-19, activities to address this new pandemic have been prioritised across all sectors. Within the health system, the health workforce and resources have been redirected away from routine services towards the new disease priority. The social determinants of health have deteriorated during the lockdown, potentially increasing progression to TB disease and impacting negatively on people with TB and their households, resulting in additional barriers to accessing TB care, with early reports of a decline in TB testing rates. Fewer TB diagnoses, less attention to adherence and support during TB treatment, poorer treatment outcomes and consequent increased transmission will increase the TB burden and TB-related mortality. People with TB or a history of TB are likely to be vulnerable to COVID-19. Modifications to current treatment practices are suggested to reduce visits to health facilities and minimise the risks of COVID-19 exposure. The COVID-19 pandemic has the potential to negatively impact on TB control in TB-endemic settings such as SA. However, there are COVID-19-related health systems-strengthening developments that may help the NTP mitigate the impact of the pandemic on TB control. By integrating TB case finding into the advanced screening, testing, tracing and monitoring systems established for COVID-19, TB case finding and linkage to care could increase, with many more TB patients starting treatment. Similarly, integrating knowledge and awareness of TB into the increased healthcare worker and community education on infectious respiratory diseases, behavioural practices around infection prevention and control, and cough etiquette, including destigmatisation of mask use, may contribute to reducing TB transmission. However, these potential gains could be overwhelmed by the impact of increasing poverty and other social determinants of health on the burden of TB.



In January 2020, SARS-CoV-2, causing COVID-19 disease, was isolated in Wuhan City, China.[1,2] By March 2020, as countries throughout the world reported increasing cases, the World Health Organization (WHO) declared the outbreak a pandemic.[3] At the time of writing (15 September 2020) there were 29 279 316 confirmed cases from 188 countries and 928 403 deaths.[4] In South Africa (SA), the first laboratory-confirmed case of COVID-19 was recorded on 5 March 2020.[5] Despite the SA President declaring a National State of Disaster and a complete lockdown with phased reversal of lockdown conditions, on 15 September 2020 there were 648 214 confirmed cases and 15 520 reported deaths.[4]

In contrast, tuberculosis (TB) is one of the world's oldest diseases, and is known to have affected humanity for at least 70 000 years.[6,7] Although preventable and treatable, TB remains one of the top 10 causes of death worldwide, causing more deaths than HIV/ AIDS.[8] In 2018, an estimated 10 million people developed TB disease, with 1.45 million deaths attributed to TB.[8] In SA, although the annual number of TB cases reported has decreased over the past decade, 235 652 new cases were reported in 2018 and TB remains the leading cause of death, with 28 678 TB-related deaths in 2017.[9,10]

The substantial effect of the COVID-19 pandemic on TB services globally has been reported.[11] With the disruptions and reorganisation of services in response to the pandemic, delays in TB diagnosis and treatment initiation may result in increased transmission and new cases. Globally a projected setback of 5 - 8 years in TB incidence and deaths is projected for 2021, with TB mortality estimated to increase by 20%.[12-14] This additional loss of life over 5 years may be of the same magnitude as the direct impact from COVID-19.[12,13]

In this article, through a literature review and perspectives of members of a national TB Think Tank task team, we explore the impact and unintended consequences of the COVID-19 pandemic and phased nationwide lockdown on TB patients and the routine TB services in SA. We describe modifications to the management of drug-susceptible (DS)- and rifampicin-resistant (RR)-TB and explore opportunities that a 'new disease' (COVID-19) may offer for an 'old threat' (TB).[7]



The TB Think Tank was set up to advise the National TB Programme on achieving the TB-related Sustainable Development Goals. Members include individuals from the SA National Department of Health, research institutions, technical support agencies, funders and the WHO.[15] The TB Think Tank developed this article based on observations since the beginning of the COVID-19 pandemic in SA and an initial literature review. The review was conducted using PubMed and Ovid databases between 1 December 2019 and 10 June 2020 using the search terms 'tuberculosis', 'COVID-19' and 'coronavirus'. The literature was summarised, discussed and analysed by a core group at three meetings. The manuscript was circulated to all task team members for input. This article represents a compilation of the available literature and the real-time experiences, perspectives and expertise of the members of the TB Think Tank task team. The objective is to highlight areas where the TB programme could benefit from the strategies introduced to address the COVID-19 pandemic.


The impact of the COVID-19 pandemic and lockdown

Addressing the challenges of this 'new disease' (COVID-19) has required unprecedented responses with unintended consequences, impacting negatively on the very people these responses intended to protect. In countries hardest hit by COVID-19, socially disadvantaged populations have borne the brunt of the epidemic, with higher numbers affected and higher mortality rates.[16,17]


People with TB: A vulnerable group

Historically, for many socioeconomic reasons, people who develop active TB disease are a vulnerable population.[18] The lockdown has increased poverty and exacerbated other social determinants of health, impacting negatively on people with TB and their households.[19] With movement restricted during the lockdown, people living in informal settlements or overcrowded hostels have spent more time indoors with poor ventilation and increased exposure to indoor air pollution. In such settings, prolonged time spent indoors could accelerate transmission of both TB and COVID-19, as social distancing is not possible, masks are not worn inside homes, and hand hygiene is compromised owing to limited access to water. Furthermore, in people co-infected with TB and COVID-19, increased coughing due to COVID-19 is likely to have increased both COVID-19 and TB transmission within households.

TB patients are economically vulnerable,[20,21] and particularly vulnerable to the 'economic shock' of the lockdown. During the first 3 months of the pandemic and lockdown there was an 18% decline in employment in SA, with job losses concentrated among the already disadvantaged, which would include people with TB.[19] RR-TB patients often lose their source of income at the time of diagnosis, and disability grants specifically for TB become their only source of income. However, owing to the prioritisation of COVID-19-related grants, applications for grants for RR-TB patients were not processed and doctors appointed to clinically assess the eligibility of patients for grants were not available at facilities (Médecins Sans Frontières, South Africa (Khayelitsha Project), personal communication, June 2020, and Bhekisisa Centre for Health Journalism[22]). During the lockdown the incidence of households running out of money for food doubled.[19] Where income security is threatened, food security is threatened, malnutrition increases, and the risk of TB infection and progression to TB disease increases.

TB patients are at increased risk of depression as a result of fatigue, weight loss, stigma, discrimination, social isolation and rejection. Furthermore, some anti-TB drugs induce depression.[23] The risk of depression may have been exacerbated by the sense of isolation during the lockdown, the stress around accessing treatment, and anxiety about poor treatment outcomes and transmitting TB to household contacts.[24] The economic impact of the lockdown will further increase this psychological stress, contributing to depression.

Owing to pre-existing lung damage, TB patients who become infected with COVID-19 are at increased risk of more serious morbidity and increased mortality.[25] For this reason, former TB patients, of whom there are many in SA (10/1 000 population), are also a vulnerable group.[26,27] Recent data from Western Cape Province show that people with active TB were over 2.5 times more likely to die of COVID-19 than people without TB (adjusted hazard ratio (aHR) 2.70; 95% confidence interval (CI) 1.81 - 4.04), and that people with a previous history of TB had a slightly increased risk of death from COVID-19 (aHR 1.41; 95% CI 1.18 - 1.93).[25] Given that HIV was also shown to be associated with COVID-19 mortality (aHR 2.14; 95% CI 1.70 - 2.70), the vulnerability of TB and former TB patients will be exacerbated in those co-infected with HIV and those with comorbidities such as diabetes mellitus and hypertension.[8,28,29]


Access to services

The difficulty of accessing health services during the COVID-19 pandemic increased for several reasons: (i) movement was restricted, requiring a permit, and this restriction was enforced by the South African Police Service and national army, using roadblocks and patrols; (ii) TB and COVID-19 are both diseases of the respiratory tract, with an overlap of the most common symptoms (cough and fever), so in an environment of anxiety around a new and potentially fatal disease, a person who has developed symptomatic TB would be fearful of COVID-19 and the associated stigma, and delay accessing healthcare;[30](iii) concern about leaving the house, fear of police intimidation and violence, belief that the new disease may be concentrated in health facilities, and the risk of COVID-19 exposure while travelling to and within a health facility; (iv) less reliable public transport and increased family responsibilities such as caring for children not at school; and (v) those unable to earn an income during the lockdown were unable to afford the transport costs to access a health facility. The National Income Dynamics Study - Coronavirus Rapid Mobile Survey (NIDS-CRAM) reports that 23% of those who needed to access health services during the lockdown were unable to do so.[19]


TB services and the TB programme

One of the unintended consequences of the COVID-19 pandemic and phased national lockdown has been the impact on routine health services.[31] Routine health services have been deprioritised; resources have been diverted and the workforce repurposed away from routine services to COVID-19 activities. Many of the gains of the TB programme over the past decade are being undermined, and it may take years to regain the TB programme's pre-COVID-19 status.

Active case finding, TB diagnosis and prevention services

Difficulties in accessing health facilities have led to fewer people accessing health services, which, together with the disruption of routine services, has impacted on TB case finding.[32] From pre-lockdown to levels 5 and 4 of the lockdown, TB testing and diagnosis decreased by 50% and 33%, respectively.[32] The delayed diagnosis of TB and consequent increased infectiousness, together with less access to TB preventive therapy and the deprioritisation of TB contact tracing, will increase transmission.[33] This delay may be exacerbated by the overlap of the more common symptoms of both diseases, which complicates the diagnosis of both conditions.

Difficulties in accessing health facilities and the disruption of routine services also delayed the diagnosis of chronic conditions such as HIV, diabetes mellitus and hypertension, which together with poor retention in care and poor management of these conditions will increase susceptibility to TB and COVID-19.[34,35] Similarly, routine infant immunisation services were disrupted, which could result in an increase in more severe forms of disease such as TB meningitis or disseminated TB.[36,37]

Despite the challenges, some individuals attended facilities, but with the focus on COVID-19, they were tested for COVID-19 and not for TB. The recent shift to reduce testing by encouraging individuals with symptoms of COVID-19 without specified risk factors to assume that they are infected with COVID-19 and stay at home may result in further delays in the diagnosis of TB.

Retention in care

Difficulties in accessing health facilities and the disruption of routine services have also led to suboptimal retention in care for TB patients.[31,38,39] Reduced treatment adherence will decrease the chance of favourable TB treatment outcomes and contribute to the development of drug resistance. In facilities where directly observed therapy (DOT) is still operational, treatment has been further compromised as patients had no access to medicine or the necessary support to enable them to take their medication successfully at home. Although community health workers have historically supported the TB programme, during the pandemic most of these activities were suspended.

At the time of diagnosis, patients with RR-TB are often very ill and are hospitalised for treatment initiation. As TB wards have been reprioritised for the COVID-19 pandemic, these patients may not have been hospitalised or have been discharged early, although community-based support structures are limited, weak, and unable to support patients at home.[39] With less frequent visits to facilities there may be delays in the identification of adverse drug reactions (ADRs) and the development of more severe ADRs, requiring hospitalisation.

As patients co-infected with TB and COVID-19 have been shown to have an increased risk of mortality, post-TB treatment lung damage, morbidity and mortality may also increase[40]Poor retention in TB care and poor management of comorbidities will exacerbate the chances of unfavourable TB treatment outcomes and poor longterm outcomes.[35] For diabetic patients, decreased availability of antihyperglycaemic agents and/or insulin will impact negatively on diabetic control; suboptimal blood glucose control could increase susceptibility to TB and COVID-19.[35] This will be exacerbated by the changes in lifestyle imposed by the lockdown, especially if these persist beyond the lockdown.


Possible solutions

It is apparent that the COVID-19 pandemic has far-reaching consequences for the burden of TB in SA. To minimise the projected setback to TB control in SA, we need to capitalise on the systems developed to address the pandemic, together with ensuring increased support for TB patients and the TB programme. In this section we detail how strategies to address the COVID-19 pandemic in SA could benefit the TB programme. In Table 1 we summarise the impact of the pandemic and lockdown on health services with mitigation suggestions.

Infection prevention and control

The COVID-19 pandemic has sparked an interest in infectious diseases and created a platform for public engagement on disease monitoring. It has also provided increased awareness of and improved behavioural practices around respiratory infection prevention and control (IPC) and cough etiquette. Wearing of masks has been normalised, and we believe that this will encourage their use going forward for both patients and healthcare workers. By linking TB with COVID-19 (as they are both respiratory diseases), we have a unique opportunity to support IPC activities that may limit the transmission of TB in the future. Improved IPC at health facilities will reduce the number of healthcare workers who become infected with TB annually.

Screening and testing

In our TB-endemic setting, given the overlap of clinical signs and symptoms for TB and COVID-19, those who screen positive for either TB or COVID-19 should be tested for both pathogens,[41] creating an efficient mechanism for patients to enter the TB diagnostic pathway. The extensive community-based screening networks deployed for COVID-19 could also support TB screening and linkage to care. Integrated TB and COVID-19 screening and testing campaigns could provide an opportunity to find the estimated 65 348 missing people with TB and increase early detection and diagnosis in people with undiagnosed TB disease. Guidelines on how sputum should be safely collected for testing in the context of COVID-19 have been developed.[41] Furthermore, if a person tests positive for TB, all household contacts and others with whom the person has had regular contact, or who are at a high risk of TB, should be screened for both TB and COVID-19 with the provision of TB prevention according to new national guidelines.

Testing and tracing

For many years, the TB programme has struggled with timeous treatment initiation in people diagnosed with TB. The set-up of sophisticated laboratory systems and digital platforms to link positive COVID-19 tests to case identification, tracing and outcome evaluation could benefit the TB programme. If TB was integrated into the geospatial mapping system set up to inform the COVID-19 tracing efforts and tracking in real time, this could strengthen the tracing of contacts, recording and notification processes of both the TB and RR-TB programmes.[42] Previously, there has been a reluctance to notify patients through short message service (SMS) (text message) systems of their TB results, owing to fears of inadvertent disclosure and increased stigma. With COVID-19, the notification of negative results through SMS allowed for quick delivery of results and reduced the need for follow-up of results by patients. The delivery of negative TB results is currently being explored by the National Institute for Communicable Diseases.

TB treatment services

COVID-19 has forced 'at-home' management of patients with mild to moderate respiratory symptoms, with links to health services via toll-free helplines, links to practitioners using virtual systems, and the creation of virtual WhatsApp support groups. The creation of these systems provides a long-overdue opportunity to replace TB DOT with virtual supportive adherence counselling and clinical management, and could supplement the existing digital and mobile health technologies (mHealth solutions). Use of these systems would minimise facility visits, limit nosocomial TB transmission, and protect TB patients from emerging infectious diseases. Individuals who do not attend their routine appointments to pick up their medication need to be contacted telephonically and counselled on the importance of adherence.

Addressing the social determinants of health is key to TB control.[43] Given the increased vulnerability of TB patients during the COVID-19 pandemic and lockdown, the resources mobilised during the pandemic to reduce poverty and provide nutritional and economic support must continue, prioritising those most at risk of the disease and severe forms of the disease. Mechanisms to deliver this aid have been established through the COVID-19 response by engagement with community-based organisations that could be explored for the continued delivery of support for people with TB.

Monitoring and evaluation

The COVID-19 pandemic has introduced public health reporting, with the SA President and Minister of Health addressing the country frequently to inform an understanding of the disease, its key indicators and the strategies adopted. The term 'flatten the curve' has been introduced, and the general public has been educated and empowered to understand and engage with the COVID-19 data (Fig. 1). Resources have been made available ( and hotlines established.

Limited resource allocation and subsequent suboptimal monitoring nd evaluation have plagued the TB programme for years. Despite the country burden of TB, real-time data of TB test positivity, linkage to care, hospitalisation and treatment outcomes are not available. We now have an opportunity for the TB programme to leverage public interest in infectious diseases and data, and lobby for improved reporting and surveillance systems for TB, improved integration of health information systems and improved mortality reporting. Going forward, the reporting systems set up for COVID-19 should be expanded to include TB and generate public engagement with the burden of TB and its control in SA.

Funding for infectious diseases

Given the effect of the COVID-19 pandemic on global and local economies as well as the everyday lives of individuals, awareness of infectious diseases on the part of populations and governments will increase, leading to increased prominence of the control of infectious diseases such as TB. This interest should be leveraged to increase investment from governments for TB.

Future research

To establish the prevalence of TB among COVID-19 patients, specimens obtained from people diagnosed with COVID-19 could be tested for TB. In our setting, a more detailed analysis of the risk of severe COVID-19 to people with TB, RR-TB or previous TB is required. Careful documentation and analysis of simultaneous treatment and treatment outcomes will inform clinical management of co-infected patients. Finally, it is not known whether people who were infected with SARS-CoV-2 are at increased risk of TB post COVID-19 disease, or whether COVID-19 infection in those with current or previous TB puts them at increased risk of developing long-term respiratory complications.



As we struggle to deal with the COVID-19 pandemic, every effort must be made to ensure that its impact does not create a second tragedy for the vulnerable TB community. To preserve the gains made over the past decade in the fight against TB and mitigate the consequences of COVID-19 on TB, prioritised funding and mobilisation of resources will be required to strengthen TB control strategies and prioritise the delivery of TB and HIV diagnostic and treatment services. Although the COVID-19 pandemic is expected to continue to 2021, TB will be around for many years to come. However, if we build on the opportunities presented by the pandemic we could, in the long run, reduce TB transmission and the SA TB burden.

Declaration. None.

Acknowledgements. None.

Author contributions. Conceived and designed the article: National TB Think Tank 'Optimising TB Treatment Outcomes' Task Team. Collection, analysis and interpretation of data: ML, HC, DE, JF, NN, MO, KN. Wrote the paper: ML, HC, DE, JF, NN, MO, KN. All authors had full access to all the data in the study. ML as corresponding author had final responsibility for the decision to submit for publication. The final version of the manuscript has been read and approved by all the authors.

Funding. The TB Think Tank is supported by the Bill and Melinda Gates Foundation. ML is supported by the South African Medical Research Council. The funder had no role in study design, the collection, analysis and interpretation of data, the writing of the report, or the decision to submit the article for publication. All researchers were independent of funders and sponsors.

Conflicts of interest. None.



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M Loveday

Accepted 9 October 2020



for the National TB Think Tank 'Optimising TB Treatment Outcomes' Task Team
Members of the National TB Think Tank 'Optimising TB Treatment Outcomes' Task Team: F Abdullah, N Bantutani, S Charalambous, F Conradie, T Dube, B Kana, M Khan, A Grant, P Hazangwe, M Longwe, R Louw, M Makgabo, R Manesen, K Mekler, L Mvusi, P Pundit, A Swarts, M Uys, E Walters

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