European Journal of Public Health, Vol. 32, No. 4, 643–647 ß The Author(s) 2022. Published by Oxford University Press on behalf of the European Public Health Association. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons. org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com https://doi.org/10.1093/eurpub/ckac031 Advance Access published on 23 March 2022 ......................................................................................................... Impact of the COVID-19 pandemic on contact tracing of patients with pulmonary tuberculosis 1,2,3 Pere Godoy , Ignasi Parrón1, Irene Barrabeig1, Joan A. Caylà4, Laura Clotet1, Núria Follia1, Monica Carol , Angels Orcau5, Miquel Alsedà1,2, Gloria Ferrús1, Pere Plans1,3, Mireia Jane1,3, 1 Joan-Pau Millet3,5, Angela Domınguez3,6, the Transmission of Tuberculosis in Catalonia (Spain) Working Group* 1 Agència de Salut Pública Catalunya, Barcelona, Spain Downloaded from https://academic.oup.com/eurpub/article/32/4/643/6553024 by guest on 18 September 2023 2 Institut de Recerca Biome  dica de Lleida (IRBLleida), Lleida, Spain 3 Consorcio de Investigación Biome dica en Red de Epidemiologıa y Salud Pública (CIBERESP), Madrid, Spain 4 Foundation of the Tuberculosis Research Unit of Barcelona, Barcelona, Spain 5 Agència de Salut Pública de Barcelona, Barcelona, Spain 6 Departament de Medicina, Universitat de Barcelona, Barcelona, Spain Correspondence: Pere Godoy, C/Castell de Farfanya, 12, 25198 Lleida, Spain, Tel: þ34 (0) 627 48 07 54, e-mail: pere.godoy@gencat.cat *Members of the Transmission of Tuberculosis in Catalonia (Spain) Working Group who contributed data are listed at the end of the article. 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 ¼ 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 ¼ 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 Overwork in the health system could lead to reductions in the detection of TB and LTBI, and in the mandatory reporting of uberculosis (TB) is one of the main health care problem world- notifiable diseases, which could worsen the future epidemio- Twide with 10 million cases and around 1.5 million deaths world- logical situation of TB. 9 Some studies have indicated that there wide each year.1,2 Provisional data collected by World Health has been a significant diversion of resources from TB to Organization indicate a reduction in reported TB cases in 2020 of COVID-19 during the pandemic 10 and, in this scenario, the 1.3 million (5.8 million in 2020 and 7.1 million in 2019).2 The study of contacts and the detection of new cases of TB and COVID-19 pandemic may have negative effect on reporting and LTBI could be reduced and past errors in TB control global TB control.2,3 Policies widely implemented in most countries reproduced. 11,12 in 2020 in response to the pandemic, particularly reassignments of Catalonia, a region of northern Spain with 7.5 million health staff and equipment, may have had a severe impact on the inhabitants, presented in the last report an annual incidence delivery TB services.2–4 of TB of 13.0 cases per 100 000. 13 Before the onset of the pan- COVID-19 has led to an overload of work in the health system demic, TB control in this region was carried out by the TB that may have reduced the care of TB-associated comorbidities, such clinical units of the main hospitals and by the Epidemiology as diabetes, cancer and HIV infection. It may also be associated with Services. Since the beginning of the pandemic the surveillance greater diagnostic delay, increased exposure to transmission and an and control of TB and COVID-19 in Catalonia has been carried increase in the risk of progression of latent tuberculosis infection out by the same units. 14 However, due to impact of COVID-19 (LTBI).4–6 the health workers of these units have been focused in the The specific effect of COVID-19 on TB transmission is difficult to control of pandemic with an important decrease in the number estimate. The reduction in community contacts due to lockdowns of TB cases notified and in the number of TB contact tracing and mass mask wearing may have led to a reduction in community carried out. 15 transmission.7 However, a less exhaustive TB and LTBI detection The objective of this study was to assess the impact of the and diagnostic delays due to reductions in access to the health sys- COVID-19 pandemic in contact tracing and in LTBI in a cohort tem, could have led to greater transmission.8 of patients with pulmonary TB in Catalonia (Spain). 644 European Journal of Public Health 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 Registered Contacts with result LTBI proportion Mean contacts TB proportion with contact tracing contacts of LTBI study n/N (%) per case 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. 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 Downloaded from https://academic.oup.com/eurpub/article/32/4/643/6553024 by guest on 18 September 2023 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. Methods Contacts with positive IGRA or tuberculin skin test (5 mm) results were considered infected.16 All contacts with a positive test We carried out an epidemiological study of the prevalence of LTBI underwent a posterior–anterior chest X-ray to rule out active TB. in contacts of pulmonary TB cases in Catalonia in the pre-pandemic Patients with lesions suggestive of active TB gave a sputum sample (1 January 2019 to 28 February 2020) and pandemic (1 March 2020 to determine the presence of acid-alcohol-resistant bacilli and make to 30 April 2021) periods. The study population was the contacts of cultures. all new active pulmonary TB patients recorded by the epidemio- The dependent variable was contacts presenting LTBI. The main logical surveillance network of the Public Health Agency of independent variables investigated were the study period (before or Catalonia. The study inclusion criterion was being an active case after the pandemic onset), age, sex, household contact or non- of pulmonary TB residing in Catalonia with community (contact household contact of the index case, migrant status, smoking status in indoor space, other than household, as working place, public and alcohol consumption. transport, recreational settings or schools) or household contacts We compared the prevalence of LTBI in contacts between the pre- who could be located and studied. pandemic and pandemic periods by age group, sex, household and Public health officers of Epidemiology Services carried out an non-household contact, migrant status, smoking status and alcohol epidemiological survey of cases of pulmonary TB that met the in- consumption. The chi-square, Fisher and Mantel–Haenszel test and clusion criteria and enlisted the household or community contacts the odds ratio (OR) were used to compare the proportion of TB and through interviewing the TB patients and/or the health workers that LTBI in the pre-pandemic and pandemic periods and the other had notified the active TB cases. In addition, all contacts recorded variables of study, considering a level of P < 0.05 as statistically received the tuberculin skin test and/or interferon gamma release significant. assay (IGRA) and a questionnaire on the migrant status, setting of A multiple logistic regression model was developed using the the exposure to the index case, smoking status and risk of alcohol backward stepwise method (SPSS program. 27 version) to detect consumption [>4 standard alcohol units (40 g) daily in men and 2.4 factors independently associated with the proportion of LTBI. units (24 g) in women or a medical record indicating risk of alcohol Multiple logistic regression analysis allowed determination of the consumption]. adjusted OR (aOR) and the 95% confidence intervals (95% CI) of Impact of the COVID-19 pandemic on contact tracing of patients with pulmonary TB 645 Table 3 Factors associated with LTBI in contacts of pulmonary TB Table 4 Factors associated with LTBI in contacts of pulmonary TB cases in Catalonia (Spain) (1 January 2019 to 31 May 2021) cases in Catalonia (Spain): multivariate analysis Variable Latent Crude odds 95% CI P-value Variable Adjusted 95% confidence P-value tuberculosis ratio odds ratio intervals infection % (n/N) Period (pandemic/pre- 1.3 1.1 1.5 0.007 pandemic) Total 26.2 (1493/5688) Sex (male/female) 1.4 1.2 1.6 0.001 Period Age group (18–29/0–17) 1.0 0.8 1.2 0.790 Pandemic 29.2 (403/1381) 1.2 1.1–1.4 0.002 Age group (30–44/0–17) 1.2 1.0 1.5 0.118 Pre-pandemic 25.3 (1090/4307) Reference Age group (45–64/0–17) 2.7 2.2 3.4 0.001 Sex Age group (65/0–17) 2.7 2.0 3.9 0.001 Male 29.4 (855/2908) 1.4 1.2–1.6 0.002 Immigrant (yes/no) 2.3 2.0 2.8 0.001 Female 23.0 (638/2778) 1.0 Household contact (yes/no) 2.2 1.9 2.6 0.001 Age group (years) 0–17 19.6 (279/1425) Reference Downloaded from https://academic.oup.com/eurpub/article/32/4/643/6553024 by guest on 18 September 2023 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 (P < 0.001), and in risk consumers of alcohol (46.0% vs. 25.8%; 45–64 48.9 (522/1067) 2.5 2.1–3.1 <0.001 P < 0.001) (table 3). 65 36.2 (93/257) 2.5 1.8–3.5 <0.001 In the multivariate logistic regression model, the risk of LTBI was Immigrant higher in the pandemic period than in the pre-pandemic period Yes 36.2 (853/2328) 2.5 2.2–2.8 <0.001 (aOR ¼ 1.3; 95% CI 1.1–1.5) and was also higher in males No 19.0 (640/3360) Reference Household contact (aOR ¼ 1.4; 95% CI 1.2–1.6), in the 30–44 years (aOR ¼ 1.2; Yes 38.9 (748/1923) 2.6 2.3–2.9 <0.001 95% CI 1.0–1.5), 45–64 years (aOR ¼ 2.7; 95% CI 2.2–3.4) and No 18.8 (745/3765) Reference 65 years (aOR ¼ 2.7; 95% CI 2.0–3.9) age groups, in household Smoking habit contact (aOR ¼ 2.2; 95% CI 1.9–2.6) and in immigrants Smoker 57.1 (408/715) 4.9 4.1–5.7 <0.001 (aOR ¼ 2.3; 95% CI 2.0–2.8) (table 4). Ex-smoker 42.0 (37/88) 2.7 1.7–4.1 No/unknown 21.4 (1048/4885) Reference Alcohol Discussion Yes 46.0 (58/126) 2.4 1.7–3.5 <0.001 No/unknown 25.8 (1435/5562) Reference During the study period there was a significant reduction in cases of pulmonary TB and in contact tracing and an increase in the pro- Note: 95% CI, confidence interval. portion of LTBI in the pandemic period, which started in March 2020 and included four pandemic waves (1 March 2020 to 30 April the ORs of the variables associated with the proportion of LTBI, 2021) compared with the pre-pandemic period (1 January 2019 to considering a level of P < 0.05 as statistically significant. 28 February 2020). The Ethics Committee of the Arnau Vilanova University Hospital In the pre-pandemic period, Catalonia had an annual incidence of approved the study (code: CEIC-2049) and conducted according to TB of 13.0 cases per 100 00013 and a prevalence of LTBI among the principles expressed in the Declaration of Helsinki. All subjects contacts of TB cases of 25.3%. In the pandemic period, there was included in the study received detailed information about the study an increased to 29.2% in the proportion of LTBI in contacts that aims before recruitment. 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 sig- Results nificant OR of 1.3 for the pandemic period vs. the pre-pandemic We studied 6363 contacts of 758 cases of active pulmonary TB period, taking into account the effect on the proportion of LTBI of (mean contacts per case: 8.4). Possible active TB or LTBI was the other variables studied as sex, age, household contact and mi- studied in 89.4% (5688/6363) of contacts (7.5 contacts/case). Of grant status. The reduction in the number of cases and contacts studied, as in the 503 cases of active pulmonary TB in the pre-pandemic period, other European countries,19,20 might be attributed to the reduction 4307 contacts (8.5 contacts/case) were studied and of the 255 cases in resources allocated to TB control due to COVID-19 pandemic, in the pandemic period, 1381 contacts (5.4 contacts/case) were ana- which has implied that most of health workers of the epidemiologic- lyzed (Supplementary figure S1). al units and clinical centers focused most of their work in COVID- The proportion of active TB in contacts was 1.9% (84/4307) in 19 patients. Studies have estimated a drastic reduction in TB report- the pre-pandemic period and 2.2% (30/1381) in the pandemic ing of 20–30% in the pandemic period.9,21 Similarly, in Canada period (P ¼ 0.60). The proportion of LTBI was 25.3% (1090/4307) Geric et al.22 in a study in two centers reported a fell of active TB in the pre-pandemic period and 29.2% (403/1381) in the pandemic treatment in the pandemic period of by 16% and 29%, respectively; period (P < 0.01) (table 1). and Louie et al.8 in San Francisco showed a decreased of 60% for In the pandemic period, the proportion of household contacts active TB evaluations compared to pre-pandemic levels. Other re- was higher than that of non-household contact (38.4% vs. 32.3%; cent report by the USA. CDC TB program also found a relative P < 0.01). With respect to the pre-pandemic period, the proportion reduction in TB cases, but the reduction is much more modest of LTBI that were diagnosed increased in females (28.4% vs. 21.0%; and less likely to be associated with a reduction in resources in P < 0.01), and in the <18 years (23.2% vs. 18.0%; P < 0.01) and  disease detection and control.23 65 years (50.7% vs. 30.4%; P < 0.01) age groups (table 2). It is difficult to determine the relative importance of a possible The risk of LTBI was higher in the pandemic period (OR ¼ 1.2; decrease in incidence or a reduction in access to health services that 95% CI 1.1–1.4), in males (OR ¼ 1.4; 95% CI 1.2–1.6) and increased may have led to a reduction in the reporting and diagnosis of active with the age of contacts (table 3). The proportion of LTBI was also TB in the first few months after the start of the COVID-19 pan- higher in household contact (38.9% vs. 18.8%; P < 0.001) immi- demic.6 It has been suggested that the lockdown periods of the grants (36.2% vs. 19.0%; P < 0.001) smokers (57.1%) and ex- pandemic have led to a further reduction in community contacts smokers (42.0%) compared with non-smokers (21.4%) and may have led to a reduction in the community transmission of 646 European Journal of Public Health TB.17,23 The mass use of masks may also have favored this reduc- Supplementary data tion.24 In contrast, the reduction in resources for the diagnosis and control of TB may have produced the opposite effect.7,17,21 The Supplementary data are available at EURPUB online. 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 set- Funding tings and schoolchildren, where the prevalence of LTBL is relatively This study was supported by the Ministry of Science and Innovation, lower, and to the concentration of studies in household contacts, Institute of Health Carlos III (Project PI18/01751) and Fondo where the prevalence is comparatively higher. In both, the pre-pan- Europeo de Desarrollo Regional (FEDER-Una manera de hacer demic and pandemic periods, there was a high proportion of LTBI Europa). in household contact (35.9% and 35.5%). The increased risk of infection in females, in the <18 years and 65 years age groups Conflicts of interest: the authors declare that they have no conflict of in the pandemic period has been observed in other studies.21,23 interest. All of this suggests that, in the pandemic period, most contact tracing was concentrated in the family where the transmission is Downloaded from https://academic.oup.com/eurpub/article/32/4/643/6553024 by guest on 18 September 2023 usually higher. However, the smaller number of cases studied was Key points 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 • The COVID-19 pandemic has had negative effects on prevalence of LTBI in immigrants, alcohol consumption and in tuberculosis (TB) control in Catalonia. smokers and ex-smokers should also be pointed out, as other stud- • An increase in latent tuberculosis infection (LTBI) was ies have showed.25,26 observed during the pandemic period in Catalonia from Studies based on mathematical models have estimated an increase 25.3% to 29.2%. in TB incidence and mortality of 5–15%, but these models should be • COVID-19 is strongly affecting TB control due less exhaustive tested in forthcoming years by empirical data.21,27 Some studies in- TB and LTBI case detection. dicate that, during the pandemic, significant resources for TB pro- grams 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 References and data gathered by the World Health Organization from 84 coun- tries shows that an estimated 1.4 million fewer people received care 1 Vos T, Lim SS, Abbafati C, et al. 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