key: cord-0993456-g1j1b3fh
authors: Migliori, Giovanni Battista; Thong, Pei Min; Alffenaar, Jan-Willem; Denholm, Justin; Tadolini, Marina; Alyaquobi, Fatma; Blanc, François-Xavier; Buonsenso, Danilo; Cho, Jin-Gun; Codecasa, Luigi Ruffo; Danila, Edvardas; Duarte, Raquel; García-García, José-María; Gualano, Gina; Rendon, Adrian; Silva, Denise Rossato; Souleymane, Mahamadou Bassirou; Tham, Sai Meng; Thomas, Tania A.; Tiberi, Simon; Udwadia, Zarir F.; Goletti, Delia; Centis, Rosella; D'Ambrosio, Lia; Sotgiu, Giovanni; Ong, Catherine W.M.
title: Gauging the impact of the COVID-19 pandemic on tuberculosis services: a global study
date: 2021-11-11
journal: Eur Respir J
DOI: 10.1183/13993003.01786-2021
sha: 7315d8d57f6f4d638a1405aa9ed54e39e7a22eef
doc_id: 993456
cord_uid: g1j1b3fh

This global study of 43 TB centres from 19 countries demonstrates the impact of COVID-19 pandemic on TB services. Newly diagnosed TB disease, drug-resistant TB, TB deaths, outpatient clinic attendances and newly diagnosed TB infection were reduced. https://bit.ly/3sdHbfk

Invitations were sent to the centres previously involved [11] , with the addition of Virginia in the USA, Lithuania, Oman and Paraguay. State-wide and/or regional data were collected from Australia (Victoria), Oman, Paraguay, Portugal (Northern Portugal), Russia (Moscow and Arkangelsk Region/Oblast) and USA (Virginia). The coordinating centre and the participating centres had ethics clearance in abidance with their institutional regulations [11] . Data was collected from 1 January 2019 to 31 December 2020.

The following variables were collected monthly: total number of TB disease cases in patients with a new diagnosis or a recurrence; number of newly diagnosed TB disease cases managed in outpatient clinics; number of TB patients discharged from hospital; number of drug-resistant TB cases; number of new TB infections; number of tests performed to diagnose TB infection encompassing tuberculin skin test and interferon-γ release assays; number of TB deaths; telehealth services provided for TB disease management (i.e. video directly observed therapy (DOT) or face-to-face teleconsultation). Data quality checks were performed in dialogue with the participating centres under the guidance of two methodology experts.

As TB centres from Moscow and Paraguay only provided TB infection tests and newly diagnosed TB infections on an annual basis, these data were excluded from the monthly data analysis. Details of lockdown and other social restrictions were collected, including dates and whether they were fully or partially implemented (data not shown). Mean±SD were computed per month for each year. Analysis was performed using Mann-Whitney U-test and a p-value of <0.05 was deemed statistically significant. All computations were performed using Graphpad Prism 7 (version 7.04, GraphPad Software) 43 TB centres located in 19 countries from five continents provided epidemiological data (figure 1a, individual country data not shown). Eight TB centres were enrolled in Spain, six in Oman, five in Italy, three in Brazil, four in Niger, two in Mexico, two in Russia, two in Australia, two in Philippines, and one from each of the nine other countries. Data on TB disease and infection were provided by all centres, except India, the Netherlands and Niger, which did not have information on the number of TB-infected individuals and diagnostic tests provided. Lockdowns were implemented in all countries at different times. The earliest lockdown was on 1 February 2020, in Australia, and the latest on 7 April, in Singapore. The majority of the countries implemented multiple lockdowns with partial or full reopening. The impact of the COVID-19 pandemic on TB services was investigated in 19 countries during 2020 compared with the pre-pandemic year 2019. For the first time, evidence is provided that the overall number of patients with TB disease and drug-resistant TB identified at these centres substantially decreased in the first COVID-19 pandemic year compared to 2019, possibly due to difficult access to TB care, lockdown measures and delayed reporting. A similar trend was observed in the majority of the selected countries, mainly in those with higher TB burden. The peak of hospital discharges in March 2020 may be attributed to the need to make space for COVID-19 patients, while outpatient attendances may have increased in February 2020 due to a surge in outpatient prescriptions to tide patients over subsequent months.

A modest increase in TB notifications occurred in Australia and Virginia (USA) in 2020. Given the advanced health systems in these countries, this is likely due to enhanced surveillance to both TB and COVID-19 [12, 14, 15] . A reduction of identified TB disease cases was observed even in low TB incidence countries (e.g. Italy, France and Spain), which were considerably affected by the COVID-19 pandemic. The reduction of identified drug-resistant TB in countries with considerable burden of disease (e.g. Argentina, Brazil, India, Mexico and Russia) raises concerns of future rebounds.

Although TB deaths in 2020 were lower than in 2019, an increase in May and July 2020 was possibly due to deaths misattributed to COVID-19, although other factors such as under-diagnoses or under-reporting are issues in some centres.

Despite decreased patients with TB disease in outpatient clinics, the use of telehealth services was considerably higher in 2020, driven by COVID-19 distancing measures and in keeping with programmatic innovations to address the challenges during the pandemic [16] . The peaks observed in April and October 2020 were temporally related to the first and the subsequent COVID-19 waves. Newly diagnosed TB infection and TB infection tests were also generally lower in 2020 relative to 2019.

Although the large number of countries and collected variables are strengths of the present study, the heterogeneity of the collected information (e.g. hospital discharges and drug-resistant TB numbers which may themselves be affected by multiple factors), the reliance on individual TB centres and not on TB national programmes, and the under-representation of some geographical areas, e.g. Africa, are limitations. The data that we collected were not available to national TB programmes at the time of data collection and the trends shown here may also be biased by the occurrences in countries with the largest number of observations. However, our observations tie in with other substantive disruptions in TB care and notifications that have been reported by the World Health Organization [17] .

In summary, this study showed the severe impact of the COVID-19 pandemic on TB services across many countries. There is an urgent need to re-prioritise resources to manage an expected TB resurgence in future. 

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