Abstract
Background
The COVID-19 pandemic could have negative effects on tuberculosis (TB) control. The objective was to assess the impact of the pandemic in contact tracing, TB and latent tuberculosis infection (LTBI) in contacts of patients with pulmonary TB in Catalonia (Spain).
Methods
Contact tracing was carried out in cases of pulmonary TB detected during 14 months in the pre-pandemic period (1 January 2019 to 28 February 2020) and 14 months in the pandemic period (1 March 2020 to 30 April 2021). Contacts received the tuberculin skin test and/or interferon gamma release assay and it was determined whether they had TB or LTBI. Variables associated with TB or LTBI in contacts (study period and sociodemographic variables) were analyzed using adjusted odds ratio (aOR) and the 95% confidence intervals (95% CI).
Results
The pre-pandemic and pandemic periods showed, respectively: 503 and 255 pulmonary TB reported cases (reduction of 50.7%); and 4676 and 1687 contacts studied (reduction of 36.1%). In these periods, the proportion of TB cases among the contacts was 1.9% (84/4307) and 2.2% (30/1381) (P = 0.608); and the proportion of LTBI was 25.3% (1090/4307) and 29.2% (403/1381) (P < 0.001). The pandemic period was associated to higher LTBI proportion (aOR = 1.3; 95% CI 1.1–1.5), taking into account the effect on LTBI of the other variables studied as sex, age, household contact and migrant status.
Conclusions
COVID-19 is affecting TB control due to less exhaustive TB and LTBI case detection. An increase in LTBI was observed during the pandemic period. Efforts should be made to improve detection of TB and LTBI among contacts of TB cases.
Introduction
Tuberculosis (TB) is one of the main health care problem worldwide with 10 million cases and around 1.5 million deaths worldwide each year.1,2 Provisional data collected by World Health Organization indicate a reduction in reported TB cases in 2020 of 1.3 million (5.8 million in 2020 and 7.1 million in 2019).2 The COVID-19 pandemic may have negative effect on reporting and global TB control.2,3 Policies widely implemented in most countries in 2020 in response to the pandemic, particularly reassignments of health staff and equipment, may have had a severe impact on the delivery TB services.2–4
COVID-19 has led to an overload of work in the health system that may have reduced the care of TB-associated comorbidities, such as diabetes, cancer and HIV infection. It may also be associated with greater diagnostic delay, increased exposure to transmission and an increase in the risk of progression of latent tuberculosis infection (LTBI).4–6
The specific effect of COVID-19 on TB transmission is difficult to estimate. The reduction in community contacts due to lockdowns and mass mask wearing may have led to a reduction in community transmission.7 However, a less exhaustive TB and LTBI detection and diagnostic delays due to reductions in access to the health system, could have led to greater transmission.8
Overwork in the health system could lead to reductions in the detection of TB and LTBI, and in the mandatory reporting of notifiable diseases, which could worsen the future epidemiological situation of TB.9 Some studies have indicated that there has been a significant diversion of resources from TB to COVID-19 during the pandemic10 and, in this scenario, the study of contacts and the detection of new cases of TB and LTBI could be reduced and past errors in TB control reproduced.11,12
Catalonia, a region of northern Spain with 7.5 million inhabitants, presented in the last report an annual incidence of TB of 13.0 cases per 100 000.13 Before the onset of the pandemic, TB control in this region was carried out by the TB clinical units of the main hospitals and by the Epidemiology Services. Since the beginning of the pandemic the surveillance and control of TB and COVID-19 in Catalonia has been carried out by the same units.14 However, due to impact of COVID-19 the health workers of these units have been focused in the control of pandemic with an important decrease in the number of TB cases notified and in the number of TB contact tracing carried out.15
The objective of this study was to assess the impact of the COVID-19 pandemic in contact tracing and in LTBI in a cohort of patients with pulmonary TB in Catalonia (Spain).
Methods
We carried out an epidemiological study of the prevalence of LTBI in contacts of pulmonary TB cases in Catalonia in the pre-pandemic (1 January 2019 to 28 February 2020) and pandemic (1 March 2020 to 30 April 2021) periods. The study population was the contacts of all new active pulmonary TB patients recorded by the epidemiological surveillance network of the Public Health Agency of Catalonia. The study inclusion criterion was being an active case of pulmonary TB residing in Catalonia with community (contact in indoor space, other than household, as working place, public transport, recreational settings or schools) or household contacts who could be located and studied.
Public health officers of Epidemiology Services carried out an epidemiological survey of cases of pulmonary TB that met the inclusion criteria and enlisted the household or community contacts through interviewing the TB patients and/or the health workers that had notified the active TB cases. In addition, all contacts recorded received the tuberculin skin test and/or interferon gamma release assay (IGRA) and a questionnaire on the migrant status, setting of the exposure to the index case, smoking status and risk of alcohol consumption [>4 standard alcohol units (40 g) daily in men and 2.4 units (24 g) in women or a medical record indicating risk of alcohol consumption].
Contacts with positive IGRA or tuberculin skin test (≥5 mm) results were considered infected.16 All contacts with a positive test underwent a posterior–anterior chest X-ray to rule out active TB. Patients with lesions suggestive of active TB gave a sputum sample to determine the presence of acid-alcohol-resistant bacilli and make cultures.
The dependent variable was contacts presenting LTBI. The main independent variables investigated were the study period (before or after the pandemic onset), age, sex, household contact or non-household contact of the index case, migrant status, smoking status and alcohol consumption.
We compared the prevalence of LTBI in contacts between the pre-pandemic and pandemic periods by age group, sex, household and non-household contact, migrant status, smoking status and alcohol consumption. The chi-square, Fisher and Mantel–Haenszel test and the odds ratio (OR) were used to compare the proportion of TB and LTBI in the pre-pandemic and pandemic periods and the other variables of study, considering a level of P < 0.05 as statistically significant.
A multiple logistic regression model was developed using the backward stepwise method (SPSS program. 27 version) to detect factors independently associated with the proportion of LTBI. Multiple logistic regression analysis allowed determination of the adjusted OR (aOR) and the 95% confidence intervals (95% CI) of the ORs of the variables associated with the proportion of LTBI, considering a level of P < 0.05 as statistically significant.
The Ethics Committee of the Arnau Vilanova University Hospital approved the study (code: CEIC-2049) and conducted according to the principles expressed in the Declaration of Helsinki. All subjects included in the study received detailed information about the study aims before recruitment.
Results
We studied 6363 contacts of 758 cases of active pulmonary TB (mean contacts per case: 8.4). Possible active TB or LTBI was studied in 89.4% (5688/6363) of contacts (7.5 contacts/case). Of the 503 cases of active pulmonary TB in the pre-pandemic period, 4307 contacts (8.5 contacts/case) were studied and of the 255 cases in the pandemic period, 1381 contacts (5.4 contacts/case) were analyzed (Supplementary figure S1).
The proportion of active TB in contacts was 1.9% (84/4307) in the pre-pandemic period and 2.2% (30/1381) in the pandemic period (P = 0.60). The proportion of LTBI was 25.3% (1090/4307) in the pre-pandemic period and 29.2% (403/1381) in the pandemic period (P < 0.01) (table 1).
Table 1.
Results of contact tracing of pulmonary TB cases in the pre-pandemic and pandemic periods in Catalonia (Spain) (1 January 2019 to 31 May 2021)
| Period | Pulmonary TB cases with contact tracing | Registered contacts | Contacts with result of LTBI study | LTBI proportion | Mean contacts per case | TB proportion |
|---|---|---|---|---|---|---|
| n/N (%) | n/N (%) | |||||
| Pre-pandemic | 503 | 4676 | 4307 (92.1%) | 1090/4307 (25.3) | 8.5 | 84/4307 (1.9) |
| Pandemic | 255 | 1687 | 1381 (81.9%) | 403/1381 (29.2) | 5.4 | 30/1381 (2.2) |
| Total | 758 | 6363 | 5688 (89.4%) | 1493/5688 (26.2) | 7.5 | 114/5688 (2) |
Note: TB, tuberculosis; LTBI, latent tuberculosis infection.
In the pandemic period, the proportion of household contacts was higher than that of non-household contact (38.4% vs. 32.3%; P < 0.01). With respect to the pre-pandemic period, the proportion of LTBI that were diagnosed increased in females (28.4% vs. 21.0%; P < 0.01), and in the <18 years (23.2% vs. 18.0%; P < 0.01) and ≥ 65 years (50.7% vs. 30.4%; P < 0.01) age groups (table 2).
Table 2.
Characteristics of contacts of pulmonary TB cases in the COVID-19 pandemic and pre-pandemic periods in Catalonia (Spain) (1 January 2019 to 31 May 2021)
| Variable | Study period |
|||
|---|---|---|---|---|
| Pre-pandemic |
Pandemic |
|||
| n/N (%) | P-value | n/N (%) | P-value | |
| Sex | ||||
| Male | 652/2231 (29.2) | < 0.001 | 203/677 (30.0) | > 0.05 |
| Female | 438/2074 (21.0) | Reference | 200/704 (28.4) | Reference |
| Age group (years) | ||||
| 0–17 | 181/1006 (18.0) | Reference | 88/427 (23.2) | Reference |
| 18–29 | 188/880 (21.8) | < 0.033 | 42/183 (23.0) | < 0.259 |
| 30–44 | 300/1227 (24.5) | < 0.001 | 69/296 (23.3) | < 0.193 |
| 45–64 | 365/1010 (36.2) | < 0.001 | 157/402 (39.0) | < 0.001 |
| ≥65 | 56/184 (30.4) | <0.001 | 37/73 (50.7) | < 0.001 |
| Immigrant | ||||
| Yes | 659/1777 (37.1) | < 0.001 | 194/551 (38.3) | < 0.001 |
| No | 431/2530 (17.0) | Reference | 209/830 (25.2) | Reference |
| Household contact | ||||
| Yes | 552/1392 (39.6) | < 0.001 | 196/531 (36.9) | < 0.001 |
| No | 538/2915 (18.5) | Reference | 207/850 (24.2) | Reference |
| Smoking | ||||
| Smoker | 301/527 (57.1) | < 0.001 | 107/188 (56.9) | < 0.001 |
| Ex-smoker | 20/53 (37.7) | < 0.001 | 17/35 (48.6) | < 0.001 |
| No/Unknown | 769/3727 (20.6) | Reference | 279/1158 (20.1) | Reference |
| Alcohol | ||||
| Yes | 44/89 (49.4) | < 0.001 | 14/37 (37.8) | < 0.001 |
| No/Unknown | 1046/4218 (24.8) | Reference | 389/1344 (28.9) | Reference |
Note: n, contacts with latent tuberculosis infection; N, contacts traced.
The risk of LTBI was higher in the pandemic period (OR = 1.2; 95% CI 1.1–1.4), in males (OR = 1.4; 95% CI 1.2–1.6) and increased with the age of contacts (table 3). The proportion of LTBI was also higher in household contact (38.9% vs. 18.8%; P < 0.001) immigrants (36.2% vs. 19.0%; P < 0.001) smokers (57.1%) and ex-smokers (42.0%) compared with non-smokers (21.4%) (P < 0.001), and in risk consumers of alcohol (46.0% vs. 25.8%; P < 0.001) (table 3).
Table 3.
Factors associated with LTBI in contacts of pulmonary TB cases in Catalonia (Spain) (1 January 2019 to 31 May 2021)
| Variable | Latent tuberculosis infection | Crude odds ratio | 95% CI | P-value |
|---|---|---|---|---|
| % (n/N) | ||||
| Total | 26.2 (1493/5688) | |||
| Period | ||||
| Pandemic | 29.2 (403/1381) | 1.2 | 1.1–1.4 | 0.002 |
| Pre-pandemic | 25.3 (1090/4307) | Reference | ||
| Sex | ||||
| Male | 29.4 (855/2908) | 1.4 | 1.2–1.6 | 0.002 |
| Female | 23.0 (638/2778) | 1.0 | ||
| Age group (years) | ||||
| 0–17 | 19.6 (279/1425) | Reference | ||
| 18–29 | 21.6 (230/1063) | 1.2 | 0.9–1.5 | 0.168 |
| 30–44 | 24.2 (369/1523) | 1.4 | 1.1–1.7 | 0.003 |
| 45–64 | 48.9 (522/1067) | 2.5 | 2.1–3.1 | <0.001 |
| ≥65 | 36.2 (93/257) | 2.5 | 1.8–3.5 | <0.001 |
| Immigrant | ||||
| Yes | 36.2 (853/2328) | 2.5 | 2.2–2.8 | <0.001 |
| No | 19.0 (640/3360) | Reference | ||
| Household contact | ||||
| Yes | 38.9 (748/1923) | 2.6 | 2.3–2.9 | <0.001 |
| No | 18.8 (745/3765) | Reference | ||
| Smoking habit | ||||
| Smoker | 57.1 (408/715) | 4.9 | 4.1–5.7 | <0.001 |
| Ex-smoker | 42.0 (37/88) | 2.7 | 1.7–4.1 | |
| No/unknown | 21.4 (1048/4885) | Reference | ||
| Alcohol | ||||
| Yes | 46.0 (58/126) | 2.4 | 1.7–3.5 | <0.001 |
| No/unknown | 25.8 (1435/5562) | Reference |
Note: 95% CI, confidence interval.
In the multivariate logistic regression model, the risk of LTBI was higher in the pandemic period than in the pre-pandemic period (aOR = 1.3; 95% CI 1.1–1.5) and was also higher in males (aOR = 1.4; 95% CI 1.2–1.6), in the 30–44 years (aOR = 1.2; 95% CI 1.0–1.5), 45–64 years (aOR = 2.7; 95% CI 2.2–3.4) and ≥65 years (aOR = 2.7; 95% CI 2.0–3.9) age groups, in household contact (aOR = 2.2; 95% CI 1.9–2.6) and in immigrants (aOR = 2.3; 95% CI 2.0–2.8) (table 4).
Table 4.
Factors associated with LTBI in contacts of pulmonary TB cases in Catalonia (Spain): multivariate analysis
| Variable | Adjusted odds ratio | 95% confidence intervals | P-value | |
|---|---|---|---|---|
| Period (pandemic/pre-pandemic) | 1.3 | 1.1 | 1.5 | 0.007 |
| Sex (male/female) | 1.4 | 1.2 | 1.6 | 0.001 |
| Age group (18–29/0–17) | 1.0 | 0.8 | 1.2 | 0.790 |
| Age group (30–44/0–17) | 1.2 | 1.0 | 1.5 | 0.118 |
| Age group (45–64/0–17) | 2.7 | 2.2 | 3.4 | 0.001 |
| Age group (≥65/0–17) | 2.7 | 2.0 | 3.9 | 0.001 |
| Immigrant (yes/no) | 2.3 | 2.0 | 2.8 | 0.001 |
| Household contact (yes/no) | 2.2 | 1.9 | 2.6 | 0.001 |
Discussion
During the study period there was a significant reduction in cases of pulmonary TB and in contact tracing and an increase in the proportion of LTBI in the pandemic period, which started in March 2020 and included four pandemic waves (1 March 2020 to 30 April 2021) compared with the pre-pandemic period (1 January 2019 to 28 February 2020).
In the pre-pandemic period, Catalonia had an annual incidence of TB of 13.0 cases per 100 00013 and a prevalence of LTBI among contacts of TB cases of 25.3%. In the pandemic period, there was an increased to 29.2% in the proportion of LTBI in contacts that may be explained by the differences in the characteristics of the contacts studied.17,18 Multiple logistic regression analysis showed that the proportion of LTBI was associated with a statistically significant OR of 1.3 for the pandemic period vs. the pre-pandemic period, taking into account the effect on the proportion of LTBI of the other variables studied as sex, age, household contact and migrant status.
The reduction in the number of cases and contacts studied, as in other European countries,19,20 might be attributed to the reduction in resources allocated to TB control due to COVID-19 pandemic, which has implied that most of health workers of the epidemiological units and clinical centers focused most of their work in COVID-19 patients. Studies have estimated a drastic reduction in TB reporting of 20–30% in the pandemic period.9,21 Similarly, in Canada Geric et al.22 in a study in two centers reported a fell of active TB treatment in the pandemic period of by 16% and 29%, respectively; and Louie et al.8 in San Francisco showed a decreased of 60% for active TB evaluations compared to pre-pandemic levels. Other recent report by the USA. CDC TB program also found a relative reduction in TB cases, but the reduction is much more modest and less likely to be associated with a reduction in resources in disease detection and control.23
It is difficult to determine the relative importance of a possible decrease in incidence or a reduction in access to health services that may have led to a reduction in the reporting and diagnosis of active TB in the first few months after the start of the COVID-19 pandemic.6 It has been suggested that the lockdown periods of the pandemic have led to a further reduction in community contacts and may have led to a reduction in the community transmission of TB.17,23 The mass use of masks may also have favored this reduction.24 In contrast, the reduction in resources for the diagnosis and control of TB may have produced the opposite effect.7,17,21 The higher proportion of LTBI in the pandemic period (29.2% vs. 25.3%; P < 0.01) may be attributed to the reduction in contact tracing in the pandemic period in work contacts, recreational settings and schoolchildren, where the prevalence of LTBL is relatively lower, and to the concentration of studies in household contacts, where the prevalence is comparatively higher. In both, the pre-pandemic and pandemic periods, there was a high proportion of LTBI in household contact (35.9% and 35.5%). The increased risk of infection in females, in the <18 years and ≥65 years age groups in the pandemic period has been observed in other studies.21,23 All of this suggests that, in the pandemic period, most contact tracing was concentrated in the family where the transmission is usually higher. However, the smaller number of cases studied was not accompanied by an increase in the proportion of detected cases of active TB in contacts. Also, in the study as a whole, the higher prevalence of LTBI in immigrants, alcohol consumption and in smokers and ex-smokers should also be pointed out, as other studies have showed.25,26
Studies based on mathematical models have estimated an increase in TB incidence and mortality of 5–15%, but these models should be tested in forthcoming years by empirical data.21,27 Some studies indicate that, during the pandemic, significant resources for TB programs have been eliminated and a reduction in cases has been attributed to a reduction in diagnoses and an increase in barriers to access to the health system.6,27 Dara et al.20 have estimated a decreased of TB notifications by 35.5% in the European Region and data gathered by the World Health Organization from 84 countries shows that an estimated 1.4 million fewer people received care for TB in 2020 than in 2019—a reduction of 21% from 2019.3
The study has some limitations. The coverage of the study of LTBI in registered contacts was high (89.4%), but the risk of infection in unstudied contacts could be higher and the proportion of LTBI could be underestimated. The reduction in the number of TB cases in the pandemic period is partly due to lower detection and reporting of cases by the health system.3 The higher proportion of LTBI in the pandemic period could be explained by the restriction of tracing to cases with a higher risk of transmission, but the relative weight of these factors is unknown. The restrictions on economic activity to essential jobs and the closure of schools during the state of alarm in the COVID-19 pandemic could have reduced community transmission. Likewise, the mass use of non-pharmaceutical measures to prevent the transmission of SARS-CoV-2 may have had an impact on TB transmission in the community that the study did not capture. The strength of the study is that it was population-based, covers all Catalonia and had an inclusion period of more than 2 years.
We recommend that resources for COVID-19 should be reallocated to epidemiological surveillance and that TB surveillance and control activities (including contact tracing and screening of at-risk populations) be made a priority. Public health measures for the control of COVID-19 and TB should be assessed globally through the epidemiological surveillance system and be seen as an opportunity to improve the overall control of transmissible diseases.
Trasmission of Tuberculosis in Catalonia (Spain) Working Group
Miquel Alsedà, Irene Barrabeig, Monica Carol, Joan A Cayla, Laura Clotet, Angela Domínguez, Gloria Ferrús, Núria Follia, Pere Godoy, Mireia Jané, Sofia Minguell, Joan Pau Millet, Angels Orcau, Ignasi Parrón, Pere Plans, Miriam Ros, Maria Sabater, Maria-Rosa Sala and Diana Toledo.
Supplementary data
Supplementary data are available at EURPUB online.
Funding
This study was supported by the Ministry of Science and Innovation, Institute of Health Carlos III (Project PI18/01751) and Fondo Europeo de Desarrollo Regional (FEDER-Una manera de hacer Europa).
Conflicts of interest: the authors declare that they have no conflict of interest.
Key points.
The COVID-19 pandemic has had negative effects on tuberculosis (TB) control in Catalonia.
An increase in latent tuberculosis infection (LTBI) was observed during the pandemic period in Catalonia from 25.3% to 29.2%.
COVID-19 is strongly affecting TB control due less exhaustive TB and LTBI case detection.
Supplementary Material
Contributor Information
Pere Godoy, Agència de Salut Pública Catalunya, Barcelona, Spain; Institut de Recerca Biomédica de Lleida (IRBLleida), Lleida, Spain; Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
Ignasi Parrón, Agència de Salut Pública Catalunya, Barcelona, Spain.
Irene Barrabeig, Agència de Salut Pública Catalunya, Barcelona, Spain.
Joan A Caylà, Foundation of the Tuberculosis Research Unit of Barcelona, Barcelona, Spain.
Laura Clotet, Agència de Salut Pública Catalunya, Barcelona, Spain.
Núria Follia, Agència de Salut Pública Catalunya, Barcelona, Spain.
Monica Carol, Agència de Salut Pública Catalunya, Barcelona, Spain.
Angels Orcau, Agència de Salut Pública de Barcelona, Barcelona, Spain.
Miquel Alsedà, Agència de Salut Pública Catalunya, Barcelona, Spain; Institut de Recerca Biomédica de Lleida (IRBLleida), Lleida, Spain.
Gloria Ferrús, Agència de Salut Pública Catalunya, Barcelona, Spain.
Pere Plans, Agència de Salut Pública Catalunya, Barcelona, Spain; Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
Mireia Jane, Agència de Salut Pública Catalunya, Barcelona, Spain; Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
Joan-Pau Millet, Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain; Agència de Salut Pública de Barcelona, Barcelona, Spain.
Angela Domínguez, Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain; Departament de Medicina, Universitat de Barcelona, Barcelona, Spain.
the Transmission of Tuberculosis in Catalonia (Spain) Working Group:
Miquel Alsedà, Irene Barrabeig, Monica Carol, Joan Caylà, Laura Clotet, Angela Domínguez, Gloria Ferrús, Núria Follia, Pere Godoy, Mireia Jané, Sofia Minguell, Joan Pau Millet, Angels Orcau, Ignasi Parrón, Pere Plans, Miriam Ros, Maria Sabater, Maria-Rosa Sala, and Diana Toledo
References
- 1. Vos T, Lim SS, Abbafati C, et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 2020;396:1204–22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.WHO. Global tuberculosis report 2021. Geneva, 2021. Available at: https://www.who.int/publications/i/item/9789240037021 (25 December 2021, date last accessed).
- 3.WHO. Impact of the COVID-19 Pandemic on TB detection and mortality in 2020. World TB campaign page, 2021. Available at: https//www.who.int/publications/m/item/impact-of-the-covid-19-pandemic-on-tb-detection-and-mortality-in-2020 (26 March 2022, date last accessed)
- 4. Siroka A, Ponce NA, Lönnroth K.. Association between spending on social protection and tuberculosis burden: a global analysis. Lancet Infect Dis 2016;16:473–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Bonadonna LV, Saunders MJ, Zegarra R, et al. Why wait? The social determinants underlying tuberculosis diagnostic delay. PLoS One 2017;12:1–18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Khan MS, Rego S, Rajal JB, et al. Mitigating the impact of COVID-19 on tuberculosis and HIV services: a cross-sectional survey of 669 health professionals in 64 low and middle-income countries. PLoS One 2021;16:1–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Hopewell PC, Reichman LB, Castro KG.. Parallels and mutual lessons in tuberculosis and covid-19 transmission, prevention, and control. Emerg Infect Dis 2021;27:681–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Louie JK, Reid M, Stella J, et al. A decrease in tuberculosis evaluations and diagnoses during the COVID-19 pandemic. Int J Tuberc Lung Dis 2020;24:860–2. [DOI] [PubMed] [Google Scholar]
- 9. Migliori GB, Thong PM, Akkerman O, et al. Worldwide effects of coronavirus disease pandemic on Tuberculosis Services, January–April 2020. Emerg Infect Dis 2020;26:2709–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Cronin AM, Railey S, Fortune D, et al. Notes from the field: effects of the COVID-19 response on tuberculosis prevention and control efforts — United States, March–April 2020. MMWR Morb Mortal Wkly Rep 2020;69:971–2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Reichman LB. The U-shaped curve of concern. Am Rev Respir Dis 1991;144:741–2. [DOI] [PubMed] [Google Scholar]
- 12. Cantwell MF, Snider DE Jr, Cauthen GO.. Epidemiology of tuberculosis in the United States, 1985 through 1992. JAMA 1194;272:535–9. [PubMed] [Google Scholar]
- 13. Jané M, Valdivia M, Fernández C, et al. La tuberculosi a Catalunya l’any 2018. Butll Epidemiol Catalunya 2019;40:115–25. [Google Scholar]
- 14.Instituto de salud Carlos III. Estrategia de detección precoz, vigilancia y control de COVID-19. Ministerio de Sanidad - Gobierno de España. 2020;1–31. Available at: https://www.mscbs.gob.es/profesionales/saludPublica/ccayes/alertasActual/nCov/documentos/COVID19_Estrategia_vigilancia_y_control_e_indicadores.pdf (26 March 2022, date last accessed).
- 15. Godoy P, Parron I, Orcau A, et al. Estudio de contactos de casos de TB pulmonar en Cataluña antes y durante la pandemia de la COVID-19. Enf Emerg 2021;20:36–7. [Google Scholar]
- 16. Cole B, Nilsen DM, Will L, et al. Essential components of a public health tuberculosis prevention, control, and elimination program: recommendations of the advisory council for the elimination of tuberculosis and the national tuberculosis controllers association. MMWR Recomm Rep 2020;69:1–27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Saunders MJ, Evans CA.. Preventing a perfect storm. Eur Respir J 2020;56:2001348. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Aznar ML, Espinosa-Pereiro J, Saborit N, et al. Impact of the COVID-19 pandemic on tuberculosis management in Spain. Int J Infect Dis 2021;108:300–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Zenner D. Time to regain lost ground: tuberculosis in the COVID-19 era. Euro Surveill 2021;26:1–2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Dara M, Kuchukhidze G, Yedilbayev A, et al. Early COVID-19 pandemic’s toll on tuberculosis services, WHO European Region, January to June 2020. Euro Surveill 2021;26:27–35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. McQuaid CF, Vassall A, Cohen T, et al. The impact of COVID-19 on TB: a review of the data. Int J Tuberc Lung Dis 2021;25:436–46. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Geric C, Saroufim M, Landsman D, et al. Impact of Covid-19 on tuberculosis prevention and treatment in Canada: a multicentre analysis of 10,833 patients. J Infect 2022. Available at: https://academic.oup.com/jid/advance-article/doi/10.1093/infdis/jiab608/6469005 (25 December 2021, date last accessed). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Deutsch-feldman M, Pratt RH, Price SF, et al. Tuberculosis — United States, 2020. MMWR Morb Mortal Wkly Rep 2021;70:409–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Huh K, Jung J, Hong J, et al. Impact of non-pharmaceutical interventions on the incidence of respiratory infections during the COVID-19 outbreak in Korea: a nationwide surveillance study. Clin Infect Dis 2021;72:e184–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Amere GA, Nayak P, Salindri AD, et al. Contribution of smoking to tuberculosis incidence and mortality in high-tuberculosis-burden countries. Am J Epidemiol 2018;187:1846–55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Godoy P, Caylà JA, Carmona G, et al. ; Grupo de Trabajo de Estudios de Contactos de Tuberculosis de Cataluña. Smoking in tuberculosis patients increases the risk of infection in their contacts. Int J Tuberc Lung Dis 2013;17:771–6. [DOI] [PubMed] [Google Scholar]
- 27. Teo AKJ, Ong CWM, Hsu LY.. COVID-19 and TB : a progression-regression conundrum. Int J Tuberc Lung Dis 2021;25:421–3. [DOI] [PubMed] [Google Scholar]
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