key: cord-0820403-uq78jchw
authors: Godoy, Pere; Parrón, Ignasi; Barrabeig, Irene; Caylà, Joan A; Clotet, Laura; Follia, Núria; Carol, Monica; Orcau, Angels; Alsedà, Miquel; Ferrús, Gloria; Plans, Pere; Jane, Mireia; Millet, Joan-Pau; Domínguez, Angela
title: Impact of the COVID-19 pandemic on contact tracing of patients with pulmonary tuberculosis
date: 2022-03-23
journal: Eur J Public Health
DOI: 10.1093/eurpub/ckac031
sha: 63fa18599bdc718ea8031001c2e6d42f1b54ef87
doc_id: 820403
cord_uid: uq78jchw

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 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 prepandemic period (1/1/2019 to 28/2/2020) and 14 months in the pandemic period (1/3/2020 to 30/4/2021). 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 OR (aOR) and the 95% confidence intervals (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.

The Tuberculosis (TB) is one of the main he health care problem worldwide with 10 million cases and around 1.5 million deaths worldwide each year (1) 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 tuberculous infection (LTBI) (4), (5) , (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 pandemic 6 (10) 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).

We carried out an epidemiological study of the prevalence of LTBI in contacts of pulmonary TB cases in Catalonia in the prepandemic (1/1/2019 to 28/2/2020) and pandemic (1/3/2020 to 30/4/2021) 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. Contacts with positive IGRA or tuberculin skin test (≥ 5 millimetres) results were considered infected (16) . All contacts with a positive test underwent a posterioranterior 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. 

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 prepandemic 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 analysed (supplementary, Figure 1 ). In the multivariate logistic regression model, the risk of LTBI was higher in the pandemic period than in the prepandemic 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 ).

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 (1/3/2020 to 30/4/2021) compared with the prepandemic period (1/1/2019 to 28/2/ 2020).

In the pre-pandemic period, Catalonia had an annual incidence of TB of 13.0 cases per 100,000 (13) and a prevalence of LTBI among contacts of TB cases of 25.3%. In the pandemic period there was an increased hasta el 29,2% in the proportion of LTBI in 10 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 pandemia which has implied that most of health workers of active TB evaluations compared to pre-pandemic levels (8). Other recent report by the U.S. 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 (17) , (21) , (7) . 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 prepandemic 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 programmes 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 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-pharmacological 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 is was population-based, covers all Catalonia and had an inclusion period of more than two 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.

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). 

None declared. 

Global burden of 369 diseases and injuries in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study

Impact of the COVID-19 pandemic on TB detection and mortality in 2020

World TB campaign page

Association between spending on social protection and tuberculosis burden: A global analysis

Why wait? The social determinants underlying tuberculosis diagnostic delay

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

Parallels and mutual lessons in tuberculosis and covid-19 transmission, prevention, and control

A decrease in tuberculosis evaluations and diagnoses during the COVID-19 pandemic

Worldwide effects of coronavirus disease pandemic on Tuberculosis Services

Notes from the Field: Effects of the COVID-19 response on tuberculosis prevention and control efforts -United States

The U-shaped curve of concern

Epidemiology of tuberculosis in the United States

Instituto de salud Carlos III. Estrategia de detección precoz, vigilancia y control de COVID-19. Ministerio de Sanidad -Gobierno de España

Estudio de contactos de casos de TB pulmonar en Cataluña antes y durante la pandemia de la COVID-19

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

Preventing a Perfect Storm

Impact of the COVID-19 pandemic on tuberculosis management in Spain

Time to regain lost ground: Tuberculosis in the COVID-19 era

Early COVID-19 pandemic's toll on tuberculosis services, WHO European Region

The impact of COVID-19 on TB: A review of the data

Impact of Covid-19 on tuberculosis prevention and treatment in canada: a multicentre analysis of 10,833 patients

Tuberculosis -United States

Impact of non-pharmaceutical interventions on the incidence of respiratory infections during the COVID-19 outbreak in Korea: a nationwide surveillance study

Contribution of smoking to tuberculosis incidence and mortality in high-tuberculosis-burden countries

Smoking in tuberculosis patients increases the risk of infection in their contacts

COVID-19 and TB : a progression-regression conundrum