Abstract
Background
Despite the robust evidence of an excess risk of coronavirus disease 2019 (COVID-19) severity and mortality in ever smokers, the debate on the role of current and ex-smokers on COVID-19 progression remains open. Limited or no data are available on the link between electronic cigarette (e-cigarette), heated tobacco product (HTP) and second-hand smoke (SHS) exposure and COVID-19 progression. To fill this knowledge gap, we undertook the COvid19 and SMOking in ITaly (COSMO-IT) study.
Methods
A multi-centre longitudinal study was conducted in 2020–2021 in 24 Italian hospitals on a total of 1,820 laboratory-confirmed COVID-19 patients. We estimated multivariable odds ratios (OR) and 95% confidence intervals (CI) to quantify the association between smoking-related behaviours (ie, smoking status, e-cigarette and HTP use, and SHS exposure) and COVID-19 severity (composite outcome: intubation, intensive care unit admission and death) and mortality.
Results
Compared to never smokers, current smokers had an increased risk of COVID-19 mortality (OR 2.17; 95% CI, 1.06–4.41). E-cigarette use was non-significantly associated to an increased risk of COVID-19 severity (OR 1.60; 95% CI, 0.96–2.67). An increased risk of mortality was observed for exposure to SHS among non-smokers (OR 1.67; 95% CI, 1.04–2.68), the risk being particularly evident for exposures of ≥6 hours/day (OR 1.99; 95% CI, 1.15–3.44).
Conclusion
This multicentric study from Italy shows a dismal COVID-19 progression in current smokers and, for the first time, in SHS exposed non-smokers. These data represent an additional reason to strengthen and enforce effective tobacco control measures and to support smokers in quitting.
Key words: COVID-19, electronic cigarettes, heat-not-burn tobacco, heated tobacco products, prognosis, severity, mortality, tobacco smoking, second-hand smoke
INTRODUCTION
Data from the literature have shown that male sex, advanced age, and presence of comorbidities are the major determinants of a poor prognosis for coronavirus disease 2019 (COVID-19), an infectious disease caused by the novel SARS-CoV-2 coronavirus that spread around the world in early 2020.1–3
Since the beginning of the pandemic, tobacco smoking has also been hypothesized to be associated with COVID-19 progression (ie, severity and/or mortality), given that tobacco smoking was found to be linked with other (similar) respiratory infectious diseases and lungs are the organs mostly affected by COVID-19.3–5 Longitudinal prospective studies on COVID-19 patients found that smokers had a substantial increased risk of major unfavorable health outcomes, including hospitalizations in an intensive care unit (ICU), need for mechanical ventilation, or death, with an about 30–45% increased risk of disease progression.3,6–11 However, despite the relatively high number of cohort studies on the role of tobacco smoking on COVID-19 outcomes, the majority of such studies did not provide adjusted risk estimates.7
Second-hand smoke (SHS) involves the exposure to many of the toxic substances inhaled during active smoking, thus it is reasonable to suspect that SHS may also play a role on COVID-19 outcomes. To the best of our knowledge, however, the evidence on the association between SHS exposure and COVID-19 severity and mortality is limited to a small study on pediatric patients positive to SARS-CoV-2, showing more frequent symptoms among minors exposed to SHS.12,13 With reference to tobacco products other than conventional tobacco cigarettes—such as electronic cigarettes (e-cigarette) and heated tobacco products (HTPs)—there is a large gap of knowledge.14 A few cross-sectional and cohort studies showed that e-cigarette users have more frequent and persistent COVID-19 symptoms,15,16 but only a recent cohort study analyzed the role of e-cigarettes on COVID-19 severity, and the study did not find any relationship between e-cigarette use and COVID-19 hospitalization and mortality.17 To our knowledge, no study has been conducted so far on the role of HTPs on COVID-19 severity and mortality.
In order to further investigate and quantify the effect of tobacco smoking and exposure to other novel products and SHS on COVID-19 severity and mortality, we conducted a large prospective study on patients hospitalized for COVID-19 in 24 Italian centers (the COvid19 and SMOking in ITaly, COSMO-IT, study).18
METHODS
Study patients
COSMO-IT is an observational, longitudinal, multicentric study of 1,820 laboratory-confirmed COVID-19 patients hospitalized between March 2020 and April 2021 in 24 Italian centers from northern, central, and southern Italy.18 Patients were consecutively identified in various hospital wards mainly coordinated by pneumologists collaborating within the Società Italiana di Tabaccologia, Rome, Italy.
The study protocol was approved by the Ethics Committee of the Coordinating centre (Comitato Etico Regionale Toscana Area Vasta Centro, N. 17495) and subsequently approved by the Ethics Committees of all the participating centers. All patients included in the study provided an informed consent to participate; for deceased patients, the informed consent was obtained from a familiar or a close relative.
Data collection
For each patient enrolled in the study, we collected data on sociodemographic characteristics, major pre-existing chronic conditions, prior use of selected drugs, anthropometric factors, and selected lifestyle habits. In particular, we collected information on smoking status (ie, never, ex- and current smoker), current daily exposure to SHS (among non-smokers), and ever use of e-cigarettes or HTPs (ie, current regular, current occasional, and past use). Information on COVID-19 symptoms, date at onset, severity of the disease, type of hospitalization, therapy, prescribed drugs, and possible complications during hospitalization were also collected. At the end of hospitalization, the outcome of the disease was recorded: discharge or laboratory-confirmed recovery, any transfer, or death. Baseline and follow-up information were collected through a questionnaire for patients enrolled prospectively; for patients hospitalized before the Ethics Committees’ approval and enrolled retrospectively, data were extracted from patients’ medical records (whenever available) or obtained by questionnaire directly contacting patients (or their relatives, in case of deceased patients).
Following previous studies,7 for COVID-19 severity we considered a composite outcome, defined as intubation, admission to ICU or death (when available); death was also analyzed among 1,129 patients from 15 centers which were able to collect information on patients’ vital status.
Statistical analysis
Data were presented as absolute and relative frequencies, for categorical variables, or means and standard deviations (SD), for continuous ones. The association between various smoking exposures and the risk of COVID-19 severity and prognosis was quantified using univariable logistic regression models to estimate the odds ratios (ORs) and corresponding 95% confidence intervals (CIs). Multivariable ORs were also estimated, after allowance for sex, age, education, and cigarette smoking. Additional OR adjusted for body mass index were also provided.
RESULTS
Among 1,820 patients included in the analysis, 37.9% were women, the mean age was 64.4 (SD, 15.1) years, and 19.1% had a low level of education; corresponding figures were 39.3%, 66.2 (SD, 15.6) years, and 22.1% among 1,129 patients from 15 centers with information on patients’ vital status (eTable 1).
Overall, the composite outcome (ie, intubation, admission to ICU or death) occurred in 19.2% of patients, was more frequent among men than women (21.3% vs 15.8%; P = 0.004) and among patients aged ≥80 years than those aged <50 years (32.7% vs 7.2%; P for trend ≤0.001; eTable 2). Among 1,129 patients from 15 centers which provided information on patients’ vital status, 14.8% deceased, with a similar frequency in men and women (14.9% vs 14.6%; P = 0.908), but a much higher frequency in older than younger patients (37.4% vs 2.3%; P for trend <0.001).
Table 1 shows univariable and multivariable ORs of composite outcome and death, according to tobacco smoking and use of e-cigarettes and HTPs. Univariable analyses did not show any association, except for a statistically significant increase of COVID-19 severity for ex-smokers compared to never smokers. After allowance for age, sex, education, and cigarette smoking, these associations were no longer statistically significant. A borderline significant increased risk in COVID-19 severity was observed for ever e-cigarette users compared to never e-cigarette users (adjusted OR 1.60; 95% CI, 0.96–2.67). With reference to COVID-19 mortality, a significant increased risk was found for current smokers compared to never smokers (OR 2.17; 95% CI, 1.06–4.41). Such estimate was 1.89 (95% CI, 0.91–3.93) after adjusting also for e-cigarette use and HTP use, and 2.25 (95% CI, 1.07–4.72) after exclusion of e-cigarette and HTP users. No significant associations with mortality were found for e-cigarette (OR 1.24) and HTP (OR 1.16) ever users compared to never users. Further adjustment for body mass index did not meaningfully modify the risk estimates (eTable 3).
Table 1. Univariable and multivariable odds ratios of composite outcome and death according to various smoking exposures among patients hospitalized for COVID-19, Italy, 2020–2021.
| N c | Composite outcomea | N c | Deathb | |||||
|
|
|
|||||||
| % | Crude OR (95% CI)d |
Adjusted OR (95% CI)e |
% | Crude OR (95% CI)d |
Adjusted OR (95% CI)e |
|||
| Cigarette smoking | ||||||||
| Never smokers | 907 | 17.1 | 1.00f | 1.00f | 562 | 13.3 | 1.00f | 1.00f |
| Ex-smokers | 787 | 22.4 | 1.40 (1.10–1.78) | 1.21 (0.94–1.58) | 476 | 16.4 | 1.27 (0.90–1.79) | 1.22 (0.82–1.83) |
| Current smokers | 126 | 15.1 | 0.86 (0.51–1.45) | 0.96 (0.56–1.64) | 91 | 15.4 | 1.18 (0.64–2.19) | 2.17 (1.06–4.41) |
| E-cigarette | ||||||||
| Never users | 1,675 | 19.3 | 1.00f | 1.00f | 1,055 | 14.9 | 1.00f | 1.00f |
| Ever users | 98 | 24.5 | 1.36 (0.84–2.19) | 1.60 (0.96–2.67) | 66 | 15.2 | 1.02 (0.51–2.05) | 1.24 (0.56–2.72) |
| Heated tobacco products | ||||||||
| Never users | 1,715 | 19.7 | 1.00f | 1.00f | 1,093 | 14.8 | 1.00f | 1.00f |
| Ever users | 29 | 20.7 | 1.07 (0.43–2.64) | 1.21 (0.47–3.12) | 26 | 15.4 | 1.05 (0.36–3.07) | 1.16 (0.35–3.89) |
CI, confidence interval; COVID-19, coronavirus disease 2019; OR, odds ratio.
aDefined as intubation, admission to intensive care unit, or death; based on 1,820 patients.
bBased on 1,129 patients.
cThe sums do not add to the total because of a few missing values.
dEstimates from univariable logistic regression models.
eEstimates from multivariable logistic regression models, adjusted for sex, age, and level of education. Estimates for e-cigarette and heated tobacco products are also adjusted for smoking.
fReference category.
An increased risk of mortality was observed for exposure to SHS (OR 1.67; 95% CI, 1.04–2.68). The risk for SHS was particularly evident for exposures of 6 or more hours a day compared to non-exposed patients (OR 1.99; 95% CI, 1.15–3.44; Table 2). Estimates were similar after further allowance for body mass index (eTable 3).
Table 2. Univariable and multivariable odds ratios of composite outcome and death according to second-hand smoke among no smoking patients hospitalized for COVID-19, Italy, 2020–2021.
| N c | Composite outcomea | N c | Deathb | |||||
|
|
|
|||||||
| % | Crude OR (95% CI)d |
Adjusted OR (95% CI)e |
% | Crude OR (95% CI)d |
Adjusted OR (95% CI)e |
|||
| Second-hand smoke daily exposure | ||||||||
| No | 992 | 19.2 | 1.00f | 1.00f | 680 | 11.8 | 1.00f | 1.00f |
| Yes | 335 | 18.5 | 1.17 (0.81–1.68) | 0.96 (0.69–1.33) | 231 | 17.3 | 1.57 (1.04–2.37) | 1.67 (1.04–2.68) |
| Yes, <6 hours/day | 157 | 15.3 | 0.76 (0.48–1.21) | 0.85 (0.53–1.37) | 93 | 10.8 | 0.90 (0.45–1.81) | 1.16 (0.53–2.51) |
| Yes, ≥6 hours/day | 178 | 21.3 | 1.15 (0.77–1.70) | 1.04 (0.69–1.57) | 138 | 21.7 | 2.08 (1.31–3.32) | 1.99 (1.15–3.44) |
| P for trend | 0.798 | 0.985 | 0.005 | 0.016 | ||||
CI, confidence interval; COVID-19, coronavirus disease 2019; OR, odds ratio.
aDefined as intubation, admission to intensive care unit, or death; based on 1,820 patients.
bBased on 1,129 patients.
cThe sums do not add to the total because of a few missing values.
dEstimates from univariable logistic regression models.
eEstimates from multivariable logistic regression models, adjusted for sex, age, and level of education.
fReference category.
DISCUSSION
The present study on patients hospitalized for COVID-19 found an over two-fold excess risk of death in current smokers and a 67% increased risk of COVID-19 mortality for patients daily exposed to SHS.
Our study confirms the dismal prognosis of COVID-19 in current smokers. These findings update and confirm results from previous meta-analyses showing an excess risk of death for smokers compared to never smokers.7–10,19–22 In our study, however, the association with COVID-19 mortality was more modest and not significant in ex-smokers. This appears somewhat in contrast with the findings from other studies reporting a higher excess risk in ex-smokers.7,10 The meta-analysis by Simons and colleagues reported a significant relative risk (RR) for ex- versus never smokers (RR 1.39; 95% credible interval, 1.09–1.87), while it found a non-significant association for current versus never smokers (RR 1.22; 95% credible interval, 0.78–1.94).7 Such discrepancy can be explained by the fact that current smokers among COVID-19 patients are much younger than never and particularly former smokers23 and age is by far the strongest risk factor for COVID-19 severity and, particularly, mortality.24 For example, in our population mean age was 58.3 years among current smokers, 66.6 years among ex-smokers, and 63.3 years among never smokers (eTable 4). Considering that around 80% of currently available studies provided only crude risk estimates of the association between tobacco smoking and COVID-19 mortality, it is likely that the RR for current smokers is under-estimated and that for former smokers over-estimated in those studies not providing adjusted estimates by age.
To our knowledge, this is the first study providing data on the role of SHS exposure on COVID-19 progression. We found that, among COVID-19 non-smoking patients, daily exposure to SHS was directly related to death. However, tobacco smoking and daily SHS were not found to be associated with COVID-19 severity.
With reference to novel nicotine containing products, we observed a non-significant 60% increased risk of COVID-19 severity for use of e-cigarettes. Our data suggest a possible unfavorable effect of these products on COVID-19 progression, although some residual confounding by tobacco smoking may explain the associations observed. In the literature data on these products and COVID-19 severity/mortality are extremely limited: only a recent cohort study analyzed the role of e-cigarettes on COVID-19 severity, reporting no association with mortality (RR 1.12; 95% CI, 0.81–1.55),17 while no cohort analyzed the role of HTPs.
The present study has various strengths, but also limitations. To our knowledge, this is the first Italian longitudinal study based on a large multicenter cohort of patients hospitalized for COVID-19. Moreover, it was specifically designed to quantify the association between various smoking exposures and COVID-19 prognosis. In most previous cohort studies, smoking data are secondary; in other words, they have not been designed with the primary aim to quantify the association between smoking and COVID-19 outcomes. Further, we presented estimates adjusted for age (besides sex and education, which are other two relevant confounding factors), while most previous studies provided only crude RR, that—as discussed above—may provide biased estimates. Among the limitations of our study, there is the fact that not all the information on cigarettes and other smoking products was available from the medical records, and in various centers it was not possible to retrieve information for deceased patients. Moreover, our study sample did not allow to conduct specific stratified analyses to analyze the association of tobacco smoking with COVID-19 progression by use of novel products.
The excess risk of mortality in current smokers compared to never smokers suggests that a non-negligible proportion of the COVID-19 deaths may be attributable to tobacco smoking. Therefore, governments and policy makers have an additional reason to strengthen and enforce effective tobacco control measures and to support smokers in quitting.
ACKNOWLEDGEMENTS
The authors thank the collaborators from the Azienda Ospedaliero-Universitaria Pisana, Pisa (Pulmonary Unit: Margherita Biagini, Lorenzo Bodo, Sara Cappelli, Annabella Catone, Davide Chimera, Lucia De Donno, Valeria Esposto, Antonio Fideli, Marta Lomi, Alessandra Pagano; Unit of Geriatry: Riccardo Franchi, Tessa Mazzarone, Igino Maria Pompilii, Sara Rogani), from ASST Brianza, Vimercate (MB; Antonella Grassi), and Mrs Ivana Garimoldi for editorial assistance.
The COSMO-IT Investigators: Ancona, IRCCS INRCA, Università Politecnica della Marche (Caterina Garbuglia, Federico Giulietti, Riccardo Sarzani, Francesco Spannella); Benevento, AORN “S.Pio” - P.O. “G.Rummo” (Mario Del Donno, Assunta Micco); Firenze, Azienda Ospedaliera Universitaria Careggi (Salvatore Cardellicchio, Chiara Cresci, Tiziana Fanucchi); Foggia, Ospedale Universitario “Policlinico Riuniti”, Università di Foggia (Maria Pia Foschino Barbaro, Paolo Fuso, Donato Lacedonia, Giorgia Lepore Giulia Scioscia); Imperia, Ospedale di Imperia, ASL 1 Imperiese (Antonella Serafini); Lecce, Ospedale Vito Fazzi (Mario Bisconti, Leonida Refolo); Milano, Fondazione IRCCS Istituto Nazionale dei Tumori (Roberto Boffi, Chiara Veronese); Milano, IRCCS San Raffaele Scientific Institute (Giovanni Favaro, Giovanni Landoni, Patrizia Rovere, Giulia Veronesi); Monza, Ospedale San Gerardo (Sara Busnelli, Paola Faverio, Fabrizio Luppi, Alberto Pesci); Napoli, A.O.R.N. A. Cardarelli (Raffaella Giacobbe, Paola Martucci); Napoli, Azienda Ospedaliera Specialistica dei Colli - Ospedale Cotugno (Alberto Marra, Roberto Parrella); Pavia, ATS di Pavia (Cinzia Ancarani, Silvia Deandrea, Mauro Narisi, Eleonora Porzio); Piacenza, Ospedale Guglielmo da Saliceto (Cosimo Franco, Angelo Mangia); Pisa, Azienda Ospedaliero-Universitaria Pisana e Università di Pisa (Laura Carrozzi, Fabrizio Maggi, Fabio Monzani, Francesco Pistelli); Pistoia, Ospedale San Jacopo, Azienda USL Toscana Centro (Antonio Sanna, Gina Tarsitano); Repubblica di San Marino, Ospedale di Stato (Valentina Conti, Enrico Rossi, Mei Ruli, Silvana Ruli) Rieti, Ospedale S. Camillo De Lellis (Shokoofe Eslami Varzaneh); Roma, Azienda Ospedaliera San Camillo Forlanini (Gianni Galluccio, Simone Guerrini, Rosastella Principe, Alfredo Sebastiani); Roma, Azienda Ospedaliero-Universitaria Policlinico Umberto I (Elena Casali, Claudio Mastroianni); Roma, Azienda Ospedaliero-Universitaria Sant’Andrea (Aldo Pezzuto, Alberto Ricci); Sassari, Azienda Ospedaliero Universitaria di Sassari (Pietro Pirina, Francesca Polo); Treviso, Ospedale Cà Foncello, AULSS2 Marca Trevigiana (Piera Peditto, Micaela Romagnoli); Udine, Azienza Sanitaria Universitaria Friuli Centrale, UNIUD-DAME (Massimo Baraldo, Francesco Lo Re, Davide Pecori, Carlo Tascini); Vimercate (MB), ASST Brianza (Biagio Tinghino).
Funding: The work of SG, CSt and AL is partially supported by the Italian League Against Cancer (LILT, Milan). The work of SG and CSt is partially supported by an Investigation Grant from the Foundation AIRC for the Research on Cancer (AIRC IG 2021, ID 25987). The work of PR is supported by funding of the Italian Ministry of Health [ricerca corrente].
Author contributions: SG and VZ had the original idea of the study; SG, GG, CB, and AL designed the study; SG, CB, and AL drafted the questionnaire in collaboration with all other authors. CB, GG, AL, CSt, and CSa contributed to the preparation of documents for the ethical committee approval. RB, CV, BT, and COSMO-IT Investigators contributed to the data collection. CSt did the statistical analysis with the supervision of AL; SG and CB drafted the article in collaboration with CSt; all other authors made substantial contributions to conception, design and data interpretation; all the authors approved the final version of the manuscript. The corresponding author attests that all listed authors meet authorship criteria and that no others meeting the criteria have been omitted.
Data availability: The data underlying this article will be shared on reasonable request to the corresponding author.
Ethics approval: The study protocol was approved by the Ethics Committee of the Coordinating centre (Comitato Etico Regionale Toscana Area Vasta Centro, N. 17495) and subsequently approved by the Ethics Committees of all the participating centres.
Conflicts of interest: None declared.
SUPPLEMENTARY MATERIAL
The following is the supplementary data related to this article:
eTable 1. Characteristics of 1,820 patients hospitalized for COVID-19, Italy, 2020–2021
eTable 2. Distribution of patients hospitalized for COVID-19 according to a composite outcome and death, overall, by sex and age, Italy, 2020–2021
eTable 3. Multivariable odds ratios of composite outcome and death according to various smoking exposures further adjusted for body mass index among patients hospitalized for COVID-19, Italy, 2020–2021
eTable 4. Distribution of 1,820 patients hospitalized for COVID-19 by sex and age, according to various smoking exposures. Italy, 2020–2021
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