Literature DB >> 32917293

Worldwide Effects of Coronavirus Disease Pandemic on Tuberculosis Services, January-April 2020.

Giovanni Battista Migliori, Pei Min Thong, Onno Akkerman, Jan-Willem Alffenaar, Fernando Álvarez-Navascués, Mourtala Mohamed Assao-Neino, Pascale Valérie Bernard, Joshua Sorba Biala, François-Xavier Blanc, Elena M Bogorodskaya, Sergey Borisov, Danilo Buonsenso, Marianne Calnan, Paola Francesca Castellotti, Rosella Centis, Jeremiah Muhwa Chakaya, Jin-Gun Cho, Luigi Ruffo Codecasa, Lia D'Ambrosio, Justin Denholm, Martin Enwerem, Maurizio Ferrarese, Tatiana Galvão, Marta García-Clemente, José-María García-García, Gina Gualano, José Antonio Gullón-Blanco, Sandra Inwentarz, Giuseppe Ippolito, Heinke Kunst, Andrei Maryandyshev, Mario Melazzini, Fernanda Carvalho de Queiroz Mello, Marcela Muñoz-Torrico, Patrick Bung Njungfiyini, Domingo Juan Palmero, Fabrizio Palmieri, Pavilio Piccioni, Alberto Piubello, Adrian Rendon, Josefina Sabriá, Matteo Saporiti, Paola Scognamiglio, Samridhi Sharma, Denise Rossato Silva, Mahamadou Bassirou Souleymane, Antonio Spanevello, Eva Tabernero, Marina Tadolini, Michel Eke Tchangou, Alice Boi Yatta Thornton, Simon Tiberi, Zarir F Udwadia, Giovanni Sotgiu, Catherine Wei Min Ong, Delia Goletti.   

Abstract

Coronavirus disease has disrupted tuberculosis services globally. Data from 33 centers in 16 countries on 5 continents showed that attendance at tuberculosis centers was lower during the first 4 months of the pandemic in 2020 than for the same period in 2019. Resources are needed to ensure tuberculosis care continuity during the pandemic.

Entities:  

Keywords:  2019 novel coronavirus disease; COVID-19; SARS-CoV-2; TB; coronavirus disease; health services; respiratory infections; severe acute respiratory syndrome coronavirus 2; tuberculosis and other mycobacteria; viruses; zoonoses

Mesh:

Year:  2020        PMID: 32917293      PMCID: PMC7588533          DOI: 10.3201/eid2611.203163

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN: 1080-6040            Impact factor:   6.883


The coronavirus disease (COVID-19) pandemic has affected clinical management of tuberculosis (TB) and TB-related services (,). Reports of the first cohorts of patients with COVID-19 and TB have been recently published (,), although it may be difficult to distinguish which infection occurred first (). The effects of COVID-19 on TB diagnostic and programmatic activities are similar (). Almost every country has national TB programs in place, whereas national programs for COVID-19 are urgently needed (,). The effect of COVID-19 on TB services is estimated to be dramatic, especially in countries where healthcare staff involved in TB management have been reassigned to the COVID-19 emergency. However, apart from local studies (), a comprehensive, multinational description is needed. The Global Tuberculosis Network, which conducted this study, collaborates with TB centers from 41 countries (,,,). We studied patient attendance at TB centers in 16 countries and compared the volume of TB-related healthcare activities in the first 4 months of the COVID-19 pandemic, January–April 2020, with that for the same period in 2019.

The Study

We invited 37 TB centers to participate in the study and collected data from 33 centers located in 16 countries on 5 continents (Appendix Tables 1, 2). The participating centers received ethics clearance according to their respective center regulations (,). Active TB disease and latent TB infection (LTBI) were defined according to international guidelines (,). We recorded numbers of patients with active TB discharged from inpatient care, patients with newly diagnosed cases of active TB, patients with active TB visiting outpatient settings, and new and total outpatient visits for LTBI. We defined use of telehealth services as implementation of directly observed therapy during face-to-face virtual teleconsultations, which were considered to be equivalent to outpatient visits and were counted as such. We did not consider patient contact by telephone and emails to be telehealth. Home visits were considered outpatient visits. We also recorded national lockdown dates. If a country reported results from >1 center, we used the sum of the attendances to generate the graphs. Quantitative variables were summarized with absolute (percentage) frequencies. Of the 16 countries studied, data were contributed by 4 TB centers each in Italy, Russia, Spain, and Brazil; 3 each in Sierra Leone and Niger; 2 in Mexico; and 1 each in 9 other countries (Appendix Tables 1, 2). Lockdowns were imposed in all countries (Appendix Figures 1, 2). The earliest lockdown start date was February 1, 2020 (Australia); the latest was April 7, 2020 (Singapore). By the end of data collection (April 30), none of the 16 countries had reduced lockdown severity. Data on new active TB cases were available from 32 of the 33 TB centers. Except for 5 centers (Sydney, New South Wales, Australia; San Fernando, the Philippines; Turin, Italy; Asturias, Spain; and London, UK), which each reported stable numbers or moderate increases, new active TB cases decreased in 27 (84%) of the 32 TB centers in the first 4 months of 2020 relative to the same period in 2019 (Appendix Figure 1). Information about total outpatient TB visits was available for 29 centers but not from Groningen, the Netherlands; Mexico City, Mexico; Porto Alegre, Brazil, and Nairobi, Kenya. A total of 22 (75%) of 29 TB centers from 14 countries registered decreased outpatient visits during the lockdowns. Active TB–associated hospital discharges differed in 2020 from 2019. Although data were not available for a few centers (Buenos Aires, Argentina; Nairobi; and the 3 centers in Niger), data for San Fernando, Singapore; Mexico City, Groningen, and London indicated minimal or no increase. Active TB–associated hospital discharges for the remaining 23 (82%) of 28 TB centers were lower during the first 4 months of 2020. Data for LTBI outpatient visits were available from 16 of the 33 TB centers; 13 (81%) recorded decreased total outpatient visits (all except Hastings, Sierra Leone; Alvorada, Brazil; and Barcelona, Spain) (Appendix Figure 2). Data for newly diagnosed LTBIs were available from 19 of the 33 TB centers. New LTBI outpatient visits at 18 (95%) of 19 TB centers (all except Alvorada) were fewer during the lockdown period (Appendix Figure 2). During the first 4 months of 2020, telehealth services were used by 7 (21%) of the 33 TB centers. The number of patients using telehealth services was reported by 4 centers: Sydney; Mumbai, India; London; and Arkhangelsk, Russia. Increased use of telehealth services correlated with lockdown implementation; most uses were recorded in April 2020 (Appendix Tables 1, 2).

Conclusions

For most TB centers during their respective national lockdowns in the first 4 months of 2020, we found reductions in TB-related hospital discharges, newly diagnosed cases of active TB, total active TB outpatient visits, and new LTBI and LTBI outpatient visits. These results may be explained by a general decrease in the use of health services, including emergency services (). Resources for TB service provision were reassigned to other medical services. Outpatient visit numbers may have decreased because of patients’ fear of exposure to severe acute respiratory syndrome coronavirus 2 (). Access to medical services may have decreased because of interruptions in or difficulty accessing public transportation, although health-related travel was permitted in most countries. In some TB centers (e.g., Mexico City), the hospital patient intake system was modified to support COVID-19 admissions, thus severely hindering TB services. In some centers, screening for LTBI was considered a lower priority than screening for active TB or COVID-19. Because of lockdowns, reactivation of active TB in persons with LTBI who did not receive preventive therapy may be expected, such as in contacts recently exposed to TB or in those who are immunocompromised (,). In England, compared with 2019, TB notifications decreased by 16.5% during April and by 37.3% during May 2020; the LTBI program was paused in response to COVID-19 on March 26 (). Lockdowns have favored the increased use of telemedicine. Telehealth is a new service offered by TB programs. In TB centers surveyed in Australia, Russia, India, and the United Kingdom, telehealth service use increased in the first 4 months of 2020. Although our study cannot comprehensively describe all features of TB management, we found that the COVID-19 pandemic had a substantial impact on TB services worldwide. The main strength of our study is the global coverage from 33 TB centers from 16 countries on 5 continents. Limitations include lack of data from some countries. In 9 of the 16 countries, data were limited to reports from only 1 TB center, which may not have fully represented that nation’s TB healthcare activities. In addition, some TB centers were located in countries with low TB incidence (e.g., Italy). The description of the changes in the TB burden over a few months did not allow for appropriate statistical inferences in these countries with low TB incidence. More information about the medium- and long-term effects of the COVID-19 pandemic on TB services after a specified time from the diagnosis of the first COVID-19 patient in each country is needed. The COVID-19 pandemic seems to have affected TB services in all 16 countries that provided data. At select TB centers, increased use of telehealth services during the pandemic was recorded. Resources urgently need to be channeled to ensure that TB care continues efficiently despite the ongoing COVID-19 pandemic.

Appendix

Additional results for study of worldwide effects of coronavirus disease pandemic on tuberculosis services, January–April 2020.
  13 in total

1.  New diseases and old threats: lessons from tuberculosis for the COVID-19 response.

Authors:  M Dara; G Sotgiu; M R Reichler; C-Y Chiang; C B E Chee; G B Migliori
Journal:  Int J Tuberc Lung Dis       Date:  2020-05-01       Impact factor: 2.373

Review 2.  Preventive therapy for tuberculosis in rheumatological patients undergoing therapy with biological drugs.

Authors:  Delia Goletti; Linda Petrone; Giuseppe Ippolito; Laura Niccoli; Carlotta Nannini; Fabrizio Cantini
Journal:  Expert Rev Anti Infect Ther       Date:  2018-06-12       Impact factor: 5.091

3.  Surveillance of adverse events in the treatment of drug-resistant tuberculosis: first global report.

Authors:  Sergey Borisov; Edvardas Danila; Andrei Maryandyshev; Margareth Dalcolmo; Skaidrius Miliauskas; Liga Kuksa; Selene Manga; Alena Skrahina; Saulius Diktanas; Luigi Ruffo Codecasa; Alena Aleksa; Judith Bruchfeld; Antoniya Koleva; Alberto Piubello; Zarir Farokh Udwadia; Onno W Akkerman; Evgeny Belilovski; Enrique Bernal; Martin J Boeree; Julen Cadiñanos Loidi; Qingshan Cai; Jose Joaquín Cebrian Gallardo; Masoud Dara; Edita Davidavičienė; Lina Davies Forsman; Jorge De Los Rios; Justin Denholm; Jacinta Drakšienė; Raquel Duarte; Seifeldin Eltaeb Elamin; Nadia Escobar Salinas; Maurizio Ferrarese; Alexey Filippov; Ana Garcia; José-María García-García; Ieva Gaudiesiute; Blagovesta Gavazova; Regina Gayoso; Roscio Gomez Rosso; Vygantas Gruslys; Gina Gualano; Wouter Hoefsloot; Jerker Jonsson; Elena Khimova; Heinke Kunst; Rafael Laniado-Laborín; Yang Li; Cecile Magis-Escurra; Vinicio Manfrin; Valentina Marchese; Elena Martínez Robles; Alberto Matteelli; Jesica Mazza-Stalder; Charalampos Moschos; Marcela Muñoz-Torrico; Hamdan Mustafa Hamdan; Birutė Nakčerienė; Laurent Nicod; Magnolia Nieto Marcos; Domingo Juan Palmero; Fabrizio Palmieri; Apostolos Papavasileiou; Marie-Christine Payen; Agostina Pontarelli; Sarai Quirós; Adrian Rendon; Laura Saderi; Agnese Šmite; Ivan Solovic; Mahamadou Bassirou Souleymane; Marina Tadolini; Martin van den Boom; Marisa Vescovo; Pietro Viggiani; Askar Yedilbayev; Rolandas Zablockis; Dmitry Zhurkin; Matteo Zignol; Dina Visca; Antonio Spanevello; José A Caminero; Jan-Willem Alffenaar; Simon Tiberi; Rosella Centis; Lia D'Ambrosio; Emanuele Pontali; Giovanni Sotgiu; Giovanni Battista Migliori
Journal:  Eur Respir J       Date:  2019-12-19       Impact factor: 16.671

4.  ERS/ECDC Statement: European Union standards for tuberculosis care, 2017 update.

Authors:  Giovanni Battista Migliori; Giovanni Sotgiu; Senia Rosales-Klintz; Rosella Centis; Lia D'Ambrosio; Ibrahim Abubakar; Graham Bothamley; Jose Antonio Caminero; Daniela Maria Cirillo; Masoud Dara; Gerard de Vries; Stefano Aliberti; Anh Tuan Dinh-Xuan; Raquel Duarte; Fabio Midulla; Ivan Solovic; Dragan R Subotic; Massimo Amicosante; Ana Maria Correia; Andra Cirule; Gina Gualano; Heinke Kunst; Fabrizio Palmieri; Vija Riekstina; Simon Tiberi; Remi Verduin; Marieke J van der Werf
Journal:  Eur Respir J       Date:  2018-05-17       Impact factor: 16.671

5.  Potential Indirect Effects of the COVID-19 Pandemic on Use of Emergency Departments for Acute Life-Threatening Conditions - United States, January-May 2020.

Authors:  Samantha J Lange; Matthew D Ritchey; Alyson B Goodman; Taylor Dias; Evelyn Twentyman; Jennifer Fuld; Laura A Schieve; Giuseppina Imperatore; Stephen R Benoit; Aaron Kite-Powell; Zachary Stein; Georgina Peacock; Nicole F Dowling; Peter A Briss; Karen Hacker; Adi V Gundlapalli; Quanhe Yang
Journal:  MMWR Morb Mortal Wkly Rep       Date:  2020-06-26       Impact factor: 17.586

6.  On tuberculosis and COVID-19 co-infection.

Authors:  Marina Tadolini; José-María García-García; François-Xavier Blanc; Sergey Borisov; Delia Goletti; Ilaria Motta; Luigi Ruffo Codecasa; Simon Tiberi; Giovanni Sotgiu; Giovanni Battista Migliori
Journal:  Eur Respir J       Date:  2020-08-20       Impact factor: 16.671

7.  Active tuberculosis, sequelae and COVID-19 co-infection: first cohort of 49 cases.

Authors:  Marina Tadolini; Luigi Ruffo Codecasa; José-María García-García; François-Xavier Blanc; Sergey Borisov; Jan-Willem Alffenaar; Claire Andréjak; Pierre Bachez; Pierre-Alexandre Bart; Evgeny Belilovski; José Cardoso-Landivar; Rosella Centis; Lia D'Ambrosio; María-Luiza De Souza-Galvão; Angel Dominguez-Castellano; Samir Dourmane; Mathilde Fréchet Jachym; Antoine Froissart; Vania Giacomet; Delia Goletti; Soazic Grard; Gina Gualano; Armine Izadifar; Damien Le Du; Margarita Marín Royo; Jesica Mazza-Stalder; Ilaria Motta; Catherine Wei Min Ong; Fabrizio Palmieri; Frédéric Rivière; Teresa Rodrigo; Denise Rossato Silva; Adrián Sánchez-Montalvá; Matteo Saporiti; Paolo Scarpellini; Frédéric Schlemmer; Antonio Spanevello; Elena Sumarokova; Eva Tabernero; Paul Anantharajah Tambyah; Simon Tiberi; Alessandro Torre; Dina Visca; Miguel Zabaleta Murguiondo; Giovanni Sotgiu; Giovanni Battista Migliori
Journal:  Eur Respir J       Date:  2020-05-26       Impact factor: 16.671

Review 8.  Epidemic and pandemic viral infections: impact on tuberculosis and the lung: A consensus by the World Association for Infectious Diseases and Immunological Disorders (WAidid), Global Tuberculosis Network (GTN), and members of the European Society of Clinical Microbiology and Infectious Diseases Study Group for Mycobacterial Infections (ESGMYC).

Authors:  Catherine Wei Min Ong; Giovanni Battista Migliori; Mario Raviglione; Gavin MacGregor-Skinner; Giovanni Sotgiu; Jan-Willem Alffenaar; Simon Tiberi; Cornelia Adlhoch; Tonino Alonzi; Sophia Archuleta; Sergio Brusin; Emmanuelle Cambau; Maria Rosaria Capobianchi; Concetta Castilletti; Rosella Centis; Daniela M Cirillo; Lia D'Ambrosio; Giovanni Delogu; Susanna M R Esposito; Jose Figueroa; Jon S Friedland; Benjamin Choon Heng Ho; Giuseppe Ippolito; Mateja Jankovic; Hannah Yejin Kim; Senia Rosales Klintz; Csaba Ködmön; Eleonora Lalle; Yee Sin Leo; Chi-Chiu Leung; Anne-Grete Märtson; Mario Giovanni Melazzini; Saeid Najafi Fard; Pasi Penttinen; Linda Petrone; Elisa Petruccioli; Emanuele Pontali; Laura Saderi; Miguel Santin; Antonio Spanevello; Reinout van Crevel; Marieke J van der Werf; Dina Visca; Miguel Viveiros; Jean-Pierre Zellweger; Alimuddin Zumla; Delia Goletti
Journal:  Eur Respir J       Date:  2020-10-01       Impact factor: 16.671

9.  Tuberculosis, COVID-19 and migrants: Preliminary analysis of deaths occurring in 69 patients from two cohorts.

Authors:  I Motta; R Centis; L D'Ambrosio; J-M García-García; D Goletti; G Gualano; F Lipani; F Palmieri; A Sánchez-Montalvá; E Pontali; G Sotgiu; A Spanevello; C Stochino; E Tabernero; M Tadolini; M van den Boom; S Villa; D Visca; G B Migliori
Journal:  Pulmonology       Date:  2020-05-14

10.  Celebrating World Tuberculosis Day at the time of COVID-19.

Authors:  Riccardo Alagna; Giorgio Besozzi; Luigi Ruffo Codecasa; Andrea Gori; Giovanni Battista Migliori; Mario Raviglione; Daniela Maria Cirillo
Journal:  Eur Respir J       Date:  2020-04-23       Impact factor: 16.671

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  49 in total

1.  [Translated article] Decline of Tuberculosis Rates and COVID-19 Pandemic. Fact or Fiction?

Authors:  Nuria Vázquez-Temprano; María Isabel Ursúa-Díaz; Ángel Salgado-Barreira; Rafael Vázquez-Gallardo; Victoria Túñez Bastida; Luis Anibarro
Journal:  Arch Bronconeumol       Date:  2022-02-11       Impact factor: 4.872

2.  TB preventive treatment in high- and intermediate-incidence countries: research needs for scale-up.

Authors:  O Oxlade; S den Boon; D Menzies; D Falzon; M Y Lane; A Kanchar; M Zignol; A Matteelli
Journal:  Int J Tuberc Lung Dis       Date:  2021-10-01       Impact factor: 2.373

Review 3.  The COVID-19 and TB syndemic: the way forward.

Authors:  A Trajman; I Felker; L C Alves; I Coutinho; M Osman; S-A Meehan; U B Singh; Y Schwartz
Journal:  Int J Tuberc Lung Dis       Date:  2022-08-01       Impact factor: 3.427

4.  Impact of SARS-CoV-2 infection on tuberculosis outcome and follow-up in Italy during the first COVID-19 pandemic wave: a nationwide online survey.

Authors:  Diana Canetti; Roberta Maria Antonello; Laura Saderi; Mara Giro; Delia Goletti; Loredana Sarmati; Paola Rodari; Marialuisa Bocchino; Miriam Schirò; Niccolò Riccardi; Giovanni Sotgiu
Journal:  Infez Med       Date:  2022-09-01

5.  TB research amidst the COVID-19 pandemic.

Authors:  D S Graciaa; R R Kempker; E Sanikidze; S Tukvadze; L Mikiashvili; R Aspindzelashvili; D Alkhazashvili; H M Blumberg; Z Avaliani; N Tukvadze
Journal:  Int J Tuberc Lung Dis       Date:  2021-03-01       Impact factor: 2.373

Review 6.  The impact of COVID-19 on tuberculosis: challenges and opportunities.

Authors:  Surya Kant; Richa Tyagi
Journal:  Ther Adv Infect Dis       Date:  2021-06-09

7.  Impact of second wave of Covid-19 on tuberculosis control.

Authors:  K K Chopra; S Matta; V K Arora
Journal:  Indian J Tuberc       Date:  2021-07

8.  Elucidating the Antimycobacterial Mechanism of Action of Ciprofloxacin Using Metabolomics.

Authors:  Kirsten E Knoll; Zander Lindeque; Adetomiwa A Adeniji; Carel B Oosthuizen; Namrita Lall; Du Toit Loots
Journal:  Microorganisms       Date:  2021-05-28

9.  Impact of the COVID-19 pandemic on tuberculosis national reference laboratory services in the WHO European Region, March to November 2020.

Authors:  Florian P Maurer; Natalia Shubladze; Gulmira Kalmambetova; Irina Felker; Giorgi Kuchukhidze; Francis Drobniewski; Askar Yedilbayev; Soudeh Ehsani
Journal:  Euro Surveill       Date:  2021-06

Review 10.  The impact of COVID-19 on TB: a review of the data.

Authors:  C F McQuaid; A Vassall; T Cohen; K Fiekert; R G White
Journal:  Int J Tuberc Lung Dis       Date:  2021-06-01       Impact factor: 2.373

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