Exploring the Impact of the COVID-19 Pandemic on Tuberculosis Care and Prevention

Abstract

The COVID-19 pandemic has set back the global tuberculosis (TB) response by several years. In 2020, access to TB prevention and care declined sharply, with TB notifications dropping by 18% compared to 2019. Declines were more pronounced in children, with a 24% drop in 0–14 year-olds and a 28% drop in 0–4 year-olds. As a result, in 2020 the number of deaths due to TB increased to 1.5 million across all ages, reversing a decade-long declining trend. Progress toward the UN High Level Meeting targets for 2022 is at risk, including the targets related to children for TB and drug-resistant TB treatments, and TB preventive therapy. Nonetheless, ending TB by 2030 as envisaged in the Sustainable Development Goals (SDGs) is still possible, but requires increased investments in accelerated case detection, subclinical TB, preventive therapy and an effective vaccine. Investing in TB could prepare the world better for fighting a future airborne pandemic.

Childhood tuberculosis (TB) poses several challenges in the areas of accurate diagnosis, child-friendly treatment options and TB prevention. Progress toward addressing TB in children has been slower than the progress made for adults. Moreover, children are often left out from scientific advancements made on TB diagnosis, treatment and prevention. The COVID-19 pandemic further worsened this situation.

The COVID-19 pandemic had a disproportionately high impact on TB care and prevention, wiping out years of progress in the global fight against TB. Children in need of diagnosis for TB and drug-resistant TB, as well as TB preventive therapy treatment, faced barriers in accessing services, resulting in a sharp decline in the number of children accessing these treatments. Progress toward internationally agreed targets for TB, drug-resistant TB and TB preventive treatment in children slowed down. The declining trend in mortality reversed and in 2020, an estimated 200,000 children died due to TB. To respond and recover from these severe disruptions, TB programmes in countries had to adapt their services, using new approaches and tools. The COVID-19 pandemic also led to several advances which have the potential for improving childhood TB diagnosis, care and prevention. Here, we summarize the impact of the pandemic on the global fight against TB, highlighting the disproportionate impact on children. We also describe the lessons learnt during the COVID-19 pandemic, and future implications for TB and childhood TB.

PRE-COVID-19 PROGRESS

Under target 3.3 of the Sustainable Development Goals (SDGs), the world has committed to end TB by 2030 [1]. Prior to the advent of the COVID-19 pandemic, TB killed more people than any other infectious disease [2]. The global fight against TB had received a boost when, for the first time, a United Nations High Level Meeting (UNHLM) was held on TB in the General Assembly in 2018. World leaders committed to bold targets in the political declaration from the UNHLM [3]. In 2018 and 2019, substantial progress was made towards some of these commitments. Access to TB diagnosis and treatment increased substantially, reducing the number of people that were missing out on TB treatment each year [4, 5]. After years of slow progress, the world had started to move in the direction of being on track to end TB by 2030.

IMPACT OF THE COVID-19 PANDEMIC ON ACCESS TO TB SERVICES

In early 2020, in response to the emergence and global spread of SARS-CoV-2, many countries went into lockdown, as well as implementing other restrictions to curb the spread of infection. The effects on TB services were immediate, and severe. On the one hand, people’s ability to access TB diagnosis and treatment services were suddenly curtailed, due to lockdown-imposed lack of transportation, “stay-at-home” messaging from public health authorities, fear of visiting health facilities, and increased stigma due to common symptoms between TB and COVID-19 [6]. Overall, these factors, which were both physical and psychological, led to postponement of health seeking action by people with TB.

On the other hand, there were also disruptions to the service delivery side: TB human resources, laboratories and clinical services were shifted to the COVID-19 response; health facilities became overwhelmed by the demand for COVID-19 services; active TB case finding activities in the community came to a halt; and health workers’ capacity to interact with people decreased due to lack of personal protective equipment and airborne infection control practices. Children were especially affected because sample collection procedures for TB testing in young children (e.g., gastric aspiration, nasopharyngeal aspiration, sputum induction) were among the activities that were suspended due to fear of aerosol generation.

It was logical to use TB resources for the COVID-19 response because TB programs had the capacity to deal with respiratory infections (for example, they already had experience in contact tracing). However, most TB programs in high burden countries were chronically underfunded and therefore did not have the surge capacity needed to deal with TB as well as the new COVID-19 pandemic. While the COVID-19 pandemic impacted TB diagnosis, treatment and prevention, the greatest impact was on TB diagnosis.

Overall, these changes led to serious setbacks for TB programs in a number of high burden countries. They not only reversed the progress made in increasing access to TB care after the 2018 UNHLM, but also wiped out several years of progress in the global fight against TB [4, 7].

Screening, testing and diagnosis of TB and drug resistant TB decreased in both adults and children. We know that most children get TB from adults with whom they are in close contact, and therefore household contact investigation is an important strategy for early detection of TB in children. Household contact investigation for TB decreased during the COVID-19 pandemic. This also resulted in stalling of progress on providing TB Preventive Treatment to child contacts. The GeneXpert rapid molecular testing platform for TB was repurposed for COVID-19 testing. While this was a positive move for public health, it had the unintended consequence of further decreasing access to GeneXpert by people in need of TB diagnosis; prior to COVID-19, there were insufficient GeneXpert machines in high-burden countries to serve even the need for TB. This diagnostic technology is particularly important for diagnosis of TB in children as it is more sensitive than other commonly used diagnostics such as microscopy, and can process sputum as well as other specimens [8].

EPIDEMIOLOGICAL IMPLICATIONS OF THE DISRUPTIONS

In May 2020, a modelling analysis was conducted to project the potential of lockdown-related disruptions on TB incidence and mortality. The study reported that temporary disruptions in access to TB services, leading to accumulation of untreated TB in the community, could substantially increase TB mortality and incidence over the next 5 years, even after adjusting for the potential protective impact of social distancing and masking [9].

There was a large global drop in the number of people diagnosed and treated for TB in 2020, down from 7.1 million in 2019 to 5.8 million in 2020 [10]. While this was a 18% drop across all ages, for children (0–14 years) on TB treatment the numbers fell by 24%. Young children (0–4 years) saw an even bigger drop of 28%. Figure 1 shows the sharp fall in the number of children (0–4 and 5–14 age groups) diagnosed and treated for TB in 2020, reversing the increasing trend in prior years. Thus, children with TB are likely to have suffered worse consequences of service disruptions compared to adults, including the potential for increased mortality. In 2020, only 37% of the estimated 1.1 million children who developed TB were notified as diagnosed and/or treated for TB [10].

Figure 1.

Number of children accesing TB treatment at global level, 2015-2020.

The number of people provided with treatment for drug-resistant TB fell by 15% across all ages, from 177,100 in 2019 to 150,359 in 2020, and by 42% in children (0-14 years) from 5,586 in 2019 to 3,234 in 2020. During the same time the numbers of people receiving TB preventive treatment fell by 22% from 3.6 million to 2.8 million. TB preventive treatment for children aged 0–4 years fell by 11% from 433,156 in 2019 to 385,641 in 2020. These declines were seen in all regions of the world but with variations between countries, with high-burden countries in Asia generally seeing more severe declines. Table 1 summarizes the decline in TB notifications in 2020 at the global level.

Table 1:

Number of Individuals Receiving TB Treatment by Age and Categories in 2019 and 2020, Showing a Decline Among All Ages/Categories.

Number of individuals	2019	2020	Percentage decline between 2019 and 2020
TB (new and relapse)	7.1 million	5.8 million	18%
Drug-resistant TB (multi-drug resistant/rifampicin-resistant)	177,100	150,359	15%
Children (0–14 years old) with TB	523,820	399,517	24%
Children (0–14 years old) with drug-resistant TB	5,586	3,234	42%
Individuals (all ages) receiving TB Preventive Treatment	3.6 million	2.8 million	22%
Child contacts < 5 years old receiving TB Preventive Treatment	433,156	385,641	11%

Using provisional monthly/quarterly data made available by WHO from several countries for 2020 and for most of 2021, we estimate that in a group of 18 low- and middle-income countries eligible for Global Fund grants and accounting for 71% of the global TB burden, TB notification has improved in 2021 compared to 2020 but is still short of the level achieved in 2019. Taking all of these countries together, total TB notifications in 2020 were 20% lower than 2019; it is estimated that in 2021, notifications were still 10% lower than in 2019. Several countries were impacted by multiple waves of COVID-19, resulting in repeated cycles of decreases and recoveries in TB notifications [10]. For example, in India sharp decreases in TB notifications followed by recovery were observed, coinciding with the first two major waves of COVID-19 in the country.

As a result of reduced access to TB diagnosis and treatment, for the first time in 2020 the estimated number of deaths due to TB increased to 1.5 million, reversing a declining trend that had persisted for over a decade [10]. Over 200,000 of these deaths were in children. Declines in WHO-estimated TB incidence slowed down in 2020 compared to previous years, and could increase in subsequent years [10].

The progress toward achieving the UNHLM targets is now at risk. Table 2 describes the progress at the global level against each of the UNHLM treatment targets that were set for the 5-year period of 2018–2022. In the first 3 years, i.e., 2018 to 2020, progress was slower than required by the targets. It is to be noted that the progress is worse in children, with achievements of only 41% and 11% for TB and drug-resistant TB respectively.

Table 2:

UN High Level Meeting Treatment Targets and Progress

UNHLM targets for the 5-year period of 2018–2022	Achieved in the first 3 years (2018–2020)	Percentage achieved
40 million individuals (all ages) receiving TB treatments	19.8 million	50%
3.5 million children receiving TB treatment	1.4 million	41%
1.5 million individuals (all ages) receiving treatment for multi-drug resistant/rifampicin- resistant TB	480,000	32%
115,000 children receiving treatment for multi-drug resistant/rifampicin-resistant TB	12,200	11%
4 million household contacts < 5 years old receiving TB Preventive Treatment	1.2 million	29%
20 million household contacts ≥/=5 years old	320,000	1.6%

In addition to the impact on TB care and prevention, co-infection of TB and COVID-19 in the same individual has been an important area of research, with some published studies showing a higher risk of severe disease and mortality if a person is coinfected when compared to mortality from the two diseases separately [11]. Case reports of coinfection with COVID-19 in children with TB have highlighted the challenges in diagnosis and the worsening of TB disease, with severe or fatal consequences [12–14].

Health system recovery from the impact of COVID-19 was ongoing at the end of 2021 in most high burden countries, but the pace of the recovery varied across countries, depending on the severity of the COVID-19 impact, the existing level of political commitment for TB, resources available for recovery and the ability of the country to adapt and innovate. Countries implemented several innovative approaches and learned from each other. Some of these approaches involved shifting TB care and prevention to the community level, large scale screening and testing for TB, “bi-directional” testing for TB and COVID-19, and use of modern diagnostics and digital tools [15]. Global partners and donors such as the Global Fund and US Agency for International Development prioritized support to countries for recovery [16]. Mitigation efforts, including bi-directional testing implemented in most countries did not include a specific focus on the needs of childhood TB and this may have been one of the reasons for a bigger decline in childhood TB notifications compared to adults.

The COVID-19 pandemic brought about increased attention to contact tracing as a public health intervention for infectious diseases. The Global Fund and USAID prioritized funding for contact investigation and for modern diagnostics for TB. Because many cases of TB in children arise from close contacts, these measures are likely to have particular benefit for early diagnosis of TB in children [16, 17].

LESSONS LEARNT AND THE WAY FORWARD

Many lessons were learnt during the COVID-19 response. Here we identify five that have particular relevance to TB.

First, the pandemic showed that case finding activities can happen at scale using modern tools for screening, testing and contact tracing. Recognizing the huge diagnostic gap in TB and the slow progress in scaling up modern TB diagnostic tools, this is a very relevant development. The pandemic showed that testing does not necessarily require people to come to a laboratory or health facility; testing can happen close to people’s homes, in communities and even at airports. Many high TB burden countries used TB testing platforms, such as GeneXpert (Cepheid, Sunyvale, CA), for COVID-19 testing at a much higher scale than TB. These countries have already procured more GeneXpert machines and are planning to procure more rapid molecular testing platforms such as GeneXpert and Truenat. Better TB diagnostics in the research pipeline, including accurate and affordable point-of-care tests, will further facilitate decentralized testing at scale. There were important advances on how to promptly report test results electronically and link them to care and follow up. Lessons learnt on contact tracing for COVID-19, such as rapid communication of positive test results to the index case and care providers; prompt and active outreach to contacts of index cases; use of digital tools; and deployment of additional trained human resources, can be used for improving childhood TB diagnosis and provision of TB preventive therapy to household contacts, especially children.

Second, the pandemic showed that, using modern digital tools, medical care and public health interventions can be provided to people at their home or in the community. These digital tools made it possible to reduce pressure on hospitals and laboratories, thus reducing the risk of nosocomial transmission and prioritizing hospital infrastructure for the severely ill. Among these digital tools were telemedicine tools, contact tracing tools, mobile apps, and several others. While TB can benefit from scaled up use of these tools, there are also digital tools specifically developed for TB which got a boost during the pandemic; they have potential to be scaled up even further. Examples include artificial intelligence (AI) based automated reading systems for X-ray and digital adherence tools for treatment support [18, 19]. More research is needed to enable AI-based X-ray reading systems for children as currently it is recommended only for adults. Some of the other digital tools such as the digital adherence tools will require family members to use on behalf of children.

Third is the availability and use of real-time data for the COVID-19 response. Real-time disaggregated data for TB on testing, diagnosis, treatment and surveillance could have multiple benefits of making TB responses more agile, serving as advocacy tools for political commitment and resource mobilization, and eliminating losses and delays in the care cascade for people with TB. The benefits of real time data on TB were seen in India’s real-time TB information system called “NIKSHAY”. Immediately following the announcement of India’s national lockdown in March 2020, case notification fell dramatically; with recovery efforts it increased again. Although India’s devastating second wave of COVID-19 saw further drops in TB notifications, they now appear to have recovered to pre-pandemic levels. Pediatric TB notifications in India fell from 151,053 in 2019 to 102,489 in 2020 and increased to 118,232 in 2021 [20]. Program managers at national and sub-national levels have access to daily, age- and sex-disaggregated TB notifications. This real-time age and sex disaggregated data from NIKSHAY on TB diagnosis and treatment, by districts and by health care provider type (public/private) provided useful information to decision makers for making early and informed decisions and measuring progress [21].

Fourth is the rapid progress on research for new diagnostics, therapeutics and vaccines seen in the COVID-19 pandemic, including faster approaches for clinical trials and innovative mechanisms for funding of research. Research for new tools in TB has been on a long and slow pathway interrupted by funding shortfalls which can now benefit from new approaches seen in COVID-19 related research. The mRNA technique used in COVID-19 vaccines has potential to be repurposed for novel TB vaccines [22, 23], potentially providing children with better protection than Bacille Calmette-Guerin. Progress made on development of new rapid molecular diagnostic systems can be multiplexed for TB, while genetic sequencing capacity for COVID-19 can be repurposed for detection of drug resistant TB and precision in selecting appropriate treatment regimens [24]. The currently available TB diagnostics tools are largely ill suited for children. TB diagnostic research and development efforts should focus on developing more sensitive point-of-care diagnostic tests that can also utilize specimen types that can be more easily collected in children, without requiring invasive procedures.

Fifth is the insight that health systems in high-burden countries worldwide were completely unprepared for a respiratory infection with airborne transmission. TB programs and TB care facilities have been implementing airborne infection prevention and control (AIPC) practices for several years, but never had the resources nor the ambition to promote AIPC more widely in the health system. Now it is possible to address these gaps by implementing AIPC across the health system and in congregate indoor settings. Such measures would greatly benefit the TB response.

GOING FORWARD

Modelling done by the Stop TB Partnership for the Global Plan to End TB 2023–2030 [25] shows that, despite the setback due to the COVID-19 pandemic, it is possible to meet the SDG target of ending TB. For this to happen, however, countries will need to invest not only in routine diagnosis and treatment of all TB, but in accelerated and early case finding (including at the subclinical stage), and scale-up of preventive therapy. Finally, a new and effective vaccine will need to be scaled up.

Considering that progress toward UNHLM targets was worse in children pre-pandemic and further worsened during the pandemic, country TB programs and partners working on child health need to prioritize children for access to TB services. Progress towards addressing child poverty and undernutrition will be important as these are strong drivers of TB in children and are covered under the United Nations SDG Goals with specific targets.

Increased resources will need to be made available for completing the recovery from the impact of COVID-19 pandemic and accelerating progress further towards ending TB. Countries must be ambitious and budget the full resources needed for TB care and prevention, including a separately identified budget line for childhood TB. Countries and partners must mobilize funding to ensure that the childhood TB budget line is fully funded.

The 2018 UNHLM committed to mobilize 13 billion US$ per annum for TB care and prevention and an additional 2 billion US$ per annum for research and development [3]. Currently less than half of that amount is available [10, 26]. In addition, the resource needs per annum have increased further from what was committed in the UNHLM, primarily because of the impact of COVID-19 pandemic [25]. Investment in fighting TB has good returns on investment; it is also a good way of ensuring that the world is better prepared for fighting any future, airborne respiratory pandemic.

Notes

Supplement sponsorship. This article appears as part of the supplement “What’s New in Childhood Tuberculosis?” sponsored by the Stop TB Partnership.

Potential conflicts of interest. None declared.

All authors have submitted the ICMJE Form for Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.