Impact of COVID-19 on the control and reorganization of tuberculosis care

Scoping review conducted in June 2020 in the following databases: Cochrane Library, Embase, LILACS, MEDLINE, PubMed, Web of Science, Cinahl and Scopus; and Opengrey - grey literature. The descriptors used in the search were: coronavirus, COVID-19, SARS-CoV-2 and tuberculosis. The selection process was performed by two independent reviewers using the Rayyan platform with the inclusion of 30 studies.

Results

The COVID-19 pandemic had an impact on tuberculosis control and the main challenges arising from it are related to the influence of social distancing on diagnosis, follow-up and adherence to treatment, including the reorganization of tuberculosis services, mainly as a result of the necessary mobilization of health teams working in the area for the care of COVID-19. Limited access to inputs and health services was also registered, which occurred similarly in relation to other health problems, thereby showing programmatic vulnerability. The effects of the pandemic in the social dimension that contributed to increase the social vulnerability also stand out.

Conclusion

Many challenges have been posed by the COVID-19 pandemic, particularly with regard to maintaining tuberculosis control actions. We expect this review will contribute to support new studies and implement public policies aimed at confronting both diseases.

Tuberculosis; Coronavirus; COVID-19; Coronavirus infections; Public health

Database/Search strategy

- PUBMED: (“coronavirus”[MeSH Terms] OR “coronavirus”[All Fields]) OR “covid 19”[All Fields] AND tuberculosis[Abstract] = 281 results
- LILACS: “coronavirus” OR “covid 19” AND “tuberculosis” = 05 results
- MEDLINE: (covid-19 or coronavirus) AND tuberculosis = 126 results
- EMBASE: (‘coronavirus infection’ OR ‘covid 19’) AND tuberculosis = 163 results
- CINAHL: (covid-19 or coronavirus) AND tuberculosis = 14 results
- WEB OF SCIENCE: (“coronavirus” OR “covid 19”) AND “tuberculosis” = 97 results
- COCHRANE LIBRARY: “coronavirus” in Title Abstract Keyword OR “Covid 19” in Title Abstract Keyword AND “tuberculosis” in Title Abstract Keyword = 07 results (Cochrane Reviews)
- OPEN GREY: Opengrey: coronavirus AND tuberculosis = 00 results
- SCOPUS: (TITLE-ABS-KEY (“coronavirus” OR “covid 19” ) AND TITLE-ABS-KEY (tuberculosis ) ) = 278 results

Reference	Type of publication	Study location	Results
World Health Organization. Information Note 12 May 2020. Tuberculosis and COVID-19. World Health Organization; 2020.⁽¹⁾	Technical note	Not applicable	Recommends: provision of adequate stocks of TB medication in order to ensure continuity of treatment in a self-administered manner and avoid unnecessary exposure, as well as the use of digital technologies.
Togun T, Kampmann B, Stoker NG, Lipman M. Anticipating the impact of the COVID-19 pandemic on TB patients and TB control programmes. Ann Clin Microbiol Antimicrob 2020; 19(1):21.⁽²⁾	Review	Not applicable	The discussion on how the pandemic will affect TB took different scenarios as example. In the United Kingdom, the resizing of professionals to act against COVID-19 requires prioritizing actions focused on the disease and not on prevention. TB control in Africa will be impacted at individual, macroeconomic and health system levels.
Tadolini M, Codecasa LR, García-García Jé-Mía, et al. Active tuberculosis, sequelae and COVID-19 co-infection: first cohort of 49 cases. Eur Respir J. 2020; 56(1):2001398.⁽¹³⁾	Letter	8 countries	Of the 49 patients with COVID-19 and TB, 53% had TB before COVID-19; 28.5% had COVID-19 first and 18.3% received both diagnoses on the same day or week. Almost all (except one) had comorbidity. The mortality rate was 12.4%.
Nguyen TA, Cuong QN, Kim ALT, Huong TN, Nguyen HN, Fox GJ, Marks GB. Adapting a TB contact investigation strategy for COVID-19. Int J Tuberc Lung Dis. 2020: 24(5): 548-50.⁽¹⁴⁾	Correspondence	Vietnam	A TB contact investigation adapted to COVID-19 was performed. A flowchart for screening for SARS-CoV-2 and tracking in sites with a low level of community transmissibility was proposed.
Alagna R, Besozzi G, Codecasa LR, et al. Celebrating World Tuberculosis Day at the time of COVID-19. Eur Respir J 2020; 55: 2000650.⁽¹⁵⁾	Letter	Not applicable	There are similarities in tackling the two diseases: they overload the health system; both demand rapid diagnosis and awareness of the population; they cause social stigma; and the lack of a surveillance system for shared monitoring.
Cınar OE, Sayınalpb B, Karakulaka EA, Karatasa AA, Veleta M, Inkayac AC, et al. Convalescent (immune) plasma treatment in a myelodysplastic COVID-19 patient with disseminated tuberculosis Transfusion and Apheresis Science 2020.⁽¹⁶⁾	Case study	Not applicable	It presents the case of a TB patient immunocompromised due to myelodysplastic syndrome and with COVID-19 who received treatment with two immunological therapies of convalescent immune plasma.
Boffa J, Mhlaba T, Sulis G, Moyo S, Sifumba Z, Pai M, et al. COVID-19 and tuberculosis in South Africa: A dangerous combination. S Afr Med J 2020;110(5):341-2.⁽¹⁷⁾	Correspondence	South Africa	Presents the concern about the situation of the health system and poor communities in South Africa. Health professionals should be aware of the possibility of double infection (COVID-19 and TB) in PLWHA.
Yadav SR, Kumar R, Kumar A, ISH P, Gupta N, Chakrabarti S. COVID-19: Avoiding a second tragedy in a tuberculosis burdened country. Monaldi Archives for Chest Disease 2020; 90(2):1338.⁽¹⁸⁾	Letter	Not applicable	Measures already used in TB control such as screening, cough etiquette practices, contact investigation and isolation measures can be applied in the prevention of COVID-19.
He G, Wu J, Shi J, Dai J, Ga,er M, Jiang X, et al. COVID-19 in Tuberculosis Patients: A Report of Three Cases. J Med Virol 2020;10.⁽¹⁹⁾	Case study	China	Report of three patients with pulmonary TB and COVID-19, who were prospectively followed from admission to discharge. Two older adults evolved to severe forms of COVID-19 and had a long recovery process.
Saunders MJ, Evans CA. COVID-19, tuberculosis, and poverty: preventing a perfect storm. Eur Respir J 2020;56: 2001348.⁽²⁰⁾	Editorial	Not applicable	With more people living in poverty, there will be an increase in TB cases, a reduction in human and material resources for its control, and an impact on the monitoring of treatment and investigation of suspects, the provision of medicines, an increase in the stigma and compromise of social protection measures.
Cox V, Wilkinson L, Grimsrud A, Hughes J, Reuter A, Conrade F. Critical changes to services for TB patients during the COVID-19 pandemic. Int J Tuberc Lung Dis 2020;24(5):542-4.⁽²¹⁾	Correspondence	Not applicable	It describes changes resulting from the pandemic to protect people with TB from exposure to SARs-COv-2, such as: reducing unnecessary visits to health services, priority care and telephone monitoring to ensure adherence to TB treatment.
Peixoto VR, Mexia R, Santos NS, Carvalho C, Abrantes A. From Tuberculosis to COVID-19: Legal and Constitutional Framework Regarding Compulsory Isolation/Treatment due to Contagious Diseases in Portugal. Acta Med Port 2020;33(4):225-8.⁽²²⁾	Perspective	Portugal	The proportionality between risks and public health measures, the balance between the citizens’ rights, freedoms and guarantees, and the defense of Public Health must be analyzed for decision-making.
Pang Y, Lin Y, Du J, Gao J, Li L. Impact of COVID-19 on tuberculosis control in China. Int J Tuberc Lung Dis 2020;24(5):545-7.⁽²³⁾	Correspondence	Not applicable	Changes in the organization of health services due to COVID-19 can compromise early diagnosis, considering the fear of seeking care, as well as the interruption of TB treatment.
Kiddell-Monroe R, Ranta M, Enook S, Saranchuk P. Inuit communities can beat COVID-19 and tuberculosis. The Lancet 2020; 5.⁽²⁴⁾	Correspondence	Canada	The virus can reach the population of Nunavut (Inuit community) and lead to tragic consequences. As access is only by air, medical facilities are basic and there are not enough COVID-19 tests.
El Salvador. Ministerio de Salud. Lineamientos Técnicos para el Abordaje y Seguimiento de casos de Tuberculosis, ante la Emergencia Nacional por Covid-19. El Salvador; 2020.⁽²⁵⁾	Recommendation	El Salvador	The technical document presents treatment modalities (supervised in the health service, at home, by video call); actions for the prevention of COVID-19 in people with TB; actions of health professionals to detect new cases of TB and biosafety in the laboratory network.
Dara M, Sotgiu G, Reichler MR, Chiang CY, Chee CBE, Migliori GB. New diseases and old threats: lessons from tuberculosis for the COVID-19 response. Int J Tuberc Lung Dis 2020; 24(5):544-5.⁽²⁶⁾	Correspondence	Not applicable	Actions for TB control can be complementary to COVID-19 control, such as: joint training with epidemiological surveillance sectors, use of diagnostic tools and practices developed in TB control, such as screening, respiratory etiquette, contact investigation, control of infection and social distancing.
Riccò M, Gualerzi G, Ranzieri S, Bragazzi NL. Stop playing with data: there is no sound evidence that Bacille Calmette-Guérin may avoid SARS-CoV-2 infection (for now). Acta Biomed 2020;91(2):207‐13.⁽²⁷⁾	Review	Not applicable	Ongoing research on how BCG vaccination policy might have affected the pandemic in terms of incidence and/or mortality were identified.
Nordling L. Tested by HIV and TB, South Africa confronts new pandemic. Science 2020; 368(6487):117.⁽²⁸⁾	News	South Africa	Mobile COVID-19 testing clinics were sent to densely populated areas. Institutes conducting research on TB and HIV redirected their teams; one of the studies investigates the use of chloroquine and others, the possibility of diagnosing asymptomatic cases of COVID-19 and the association of TB/HIV.
Manyazewal T, Woldeamanuel Y, Fekadu B, Marconi VC. The fight to end tuberculosis must not be forgotten in the COVID-19 outbreak. Nature MEd 2020;26(6):811-2.⁽²⁹⁾	Correspondence	Not applicable	An increase in TB cases and development of drug resistance are expected during the pandemic. Governments must seek strategies to ensure adherence to TB treatment.
Adepoju P. Tuberculosis and HIV responses threatened by COVID-19. The Lancet 2020; 7(5): e319-20.⁽³⁰⁾	Resource	Nigeria	COVID-19 has been affecting TB and HIV control measures. The supply and transport of TB drugs is at risk of being interrupted. The scarcity of protective equipment, the lack of training of health professionals in relation to differential diagnosis between TB and COVID-19, and the difficulty of getting to health services can contribute to worsen the health situation.
Yasri S, Wiwanitkit V. Tuberculosis and novel Wuhan coronavirus infection: Pathological interrelationship. Indian J Tuberc 2020.⁽³¹⁾	Correspondence	Not applicable	Data from January 21, 2020, showed 221 cases of new infection by the new coronavirus, one case of co-infection with TB (0.45%) and six deaths.
Motta RC, DÁmbrosio L, García-García JM, Golettu D, Gualano G, Lipani F. Tuberculosis, COVID-19 and migrants: Preliminary analysis of deaths occurring in 69 patients from two cohorts. Pulmonol 2020;26(4):233-40.⁽³²⁾	Brief communication	Eight countries	Eight deaths out of 69 patients were observed. Most (n=7) were male and mean age 70 years. The diagnosis of TB was prior to that of COVID-19, and only one of them had a simultaneous diagnosis of COVID-19 and TB; the others were diagnosed with COVID-19 between seven and 75 days (median 22.5 days) after the diagnosis of TB.
Sharkie IK. BCG is a Good Immunotherapeutic Agent for Viral and Autoimmune Diseases: Is it a New Weapon against Coronavirus (COVID-19)? Electron J Gen Med. 2020;17(6):em229.⁽³³⁾	Review	Not applicable	The action triggered by the BCG vaccine on the immune system may constitute resistance to a variety of unrelated diseases and pathogens, leading to the reduction of some types of viral infections, one of them being COVID-19.
Rajarshi K, Chatterjee A, Ray S. BCG vaccination strategy implemented to reduce the impact of COVID-19: Hype or Hope?. Med in Drug Discovery 2020;7.⁽³⁴⁾	Review	Not applicable	Clinical trials involving the BCG vaccine in health professionals who work on the front lines of COVID-19 are in progress, inquiring if the vaccine reduces the severity and occurrence of the disease.
Redelman-Sidi G. Could BCG be used to protect against COVID-19? Nature Rev Urol 2020;17(6):316-7.⁽³⁵⁾	Comment	Not applicable	Research is underway to test the hypothesis that the BCG vaccine protects against COVID-19. If the results prove a protective effect, the following questions are asked: How long does immunity last after vaccination? What is the ideal time to vaccinate?
Covián C, Retamal-Díaz A, Sueno SM, Kalergis AM. Could BCG Vaccination Induce Protective Trained Immunity for SARS-CoV-2? Front. Immunol 2020;11.⁽³⁶⁾	Perspective	Not applicable	Countries where BCG vaccination is administered at birth showed a lower rate of infection and deaths related to COVID-19, suggesting that this vaccine can induce trained immunity and offer some protection to COVID-19.
Hergarty PKm Sfakianos JP, Giannarini G, Dinardo AR, Kamat AM. COVID-19 and Bacillus Calmette-Guerí: What is the Link? Eur Uro Oncol 2020;3(3): 259-61.⁽³⁷⁾	Editorial	Not applicable	The European countries most affected by COVID-19 were those that did not have a national BCG vaccination program; the incidence in countries with vaccination was 0.8 per million and 34.8 per million in those without this program.
Maciel EN, Gonçalves-Júnior E, Dalcolmo MMP. Tuberculosis and coronavirus: what do we know? Epidemiol Serv Saude 2020; 29(2):e2020128.⁽³⁸⁾	Opinion	Not applicable	The high incidence of TB in some Brazilian states, added to the high population density observed on the outskirts of large cities will bring obstacles to confronting COVID-19.
Amimo F, Lambert B, Magit A. What does the COVID-19 pandemic mean for HIV, tuberculosis, and malaria control? Trop Med Health 2020; 48:32.⁽³⁹⁾	Short report	South Africa	The study assessed the impact of COVID-19 on the control of HIV, TB and malaria in Africa. Measures to control COVID-19 neglect the epidemiological, social and economic reality. The isolation measures and limitations of some sectors such as travel and business determine that the working age population faces difficulties in accessing essential services.
Stop TB Partnership. The potential impact of the covid-19 response on tuberculosis in high-burden countries: a modelling analysis [Internet]. Stop TB Partnership, Geneva: Stop TB Partnership, Geneva; 2020 Stop TB Partnership.⁽⁴⁰⁾	Modelling analysis	Not applicable	Modeling analysis to estimate the impact of COVID-19 in three high TB burden countries (India, Republic of Kenya and Ukraine) suggests a 25% reduction in TB detection and a 13% increase in TB mortality. Between 2020 and 2025, an additional 6.3 million cases of TB are expected.

Increase of BCG vaccine in COVID^(27,33-37)	Impact of the COVID-19 pandemic on TB control^{(2,13,14,17,19-22,24,29-32,38-39,41)}	Effects of COVID-19 on the organization of health services^{(1,15,16,18,23,25-26,28)}
- Effects of BCG Vaccine on COVID-19	- Influence of COVID-19 on TB treatment follow-up and adherence - COVID-19 aggravates the context of social vulnerability with implications to TB control	- Need to reorganize human and material resources aimed at TB and other diseases to fight COVID-19 - General changes in health care

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[1] Corresponding author. Paula Hino. E-mail: paulahino@yahoo.com.br