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      COVID-19 and smoking: A systematic review of the evidence

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          Abstract

          COVID-19 is a coronavirus outbreak that initially appeared in Wuhan, Hubei Province, China, in December 2019, but it has already evolved into a pandemic spreading rapidly worldwide 1, 2 . As of 18 March 2020, a total number of 194909 cases of COVID-19 have been reported, including 7876 deaths, the majority of which have been reported in China (3242) and Italy (2505) 3 .

          However, as the pandemic is still unfortunately under progression, there are limited data with regard to the clinical characteristics of the patients as well as to their prognostic factors 4 . Smoking, to date, has been assumed to be possibly associated with adverse disease prognosis, as extensive evidence has highlighted the negative impact of tobacco use on lung health and its causal association with a plethora of respiratory diseases 5 . Smoking is also detrimental to the immune system and its responsiveness to infections, making smokers more vulnerable to infectious diseases 6 . Previous studies have shown that smokers are twice more likely than non-smokers to contract influenza and have more severe symptoms, while smokers were also noted to have higher mortality in the previous MERS-CoV outbreak 7, 8 .

          Given the gap in the evidence, we conducted a systematic review of studies on COVID-19 that included information on patients’ smoking status to evaluate the association between smoking and COVID-19 outcomes including the severity of the disease, the need for mechanical ventilation, the need for intensive care unit (ICU) hospitalization and death.

          The literature search was conducted on 17 March 2020, using two databases (PubMed, ScienceDirect), with the search terms: [‘smoking’ OR ‘tobacco’ OR ‘risk factors’ OR ‘smoker*’] AND [‘COVID-19’ OR ‘COVID 19’ OR ‘novel coronavirus’ OR ‘sars cov-2’ OR ‘sars cov 2’] and included studies published in 2019 and 2020. Further inclusion criteria were that the studies were in English and referred to humans. We also searched the reference lists of the studies included. A total of 71 studies were retrieved through the search, of which 66 were excluded after full-text screening, leaving five studies that were included. All of the studies were conducted in China, four in Wuhan and one across provinces in mainland China. The populations in all studies were patients with COVID-19, and the sample size ranged from 41 to 1099 patients. With regard to the study design, retrospective and prospective methods were used, and the timeframe of all five studies covered the first two months of the COVID-19 pandemic (December 2019, January 2020).

          Specifically, Zhou et al. 9 studied the epidemiological characteristics of 191 individuals infected with COVID-19, without, however, reporting in more detail the mortality risk factors and the clinical outcomes of the disease. Among the 191 patients, there were 54 deaths, while 137 survived. Among those that died, 9% were current smokers compared to 4% among those that survived, with no statistically significant difference between the smoking rates of survivors and non-survivors (p=0.21) with regard to mortality from COVID-19.

          Similarly, Zhang et al. 10 presented clinical characteristics of 140 patients with COVID-19. The results showed that among severe patients (n=58), 3.4% were current smokers and 6.9% were former smokers, in contrast to non-severe patients (n=82) among which 0% were current smokers and 3.7% were former smokers , leading to an OR of 2.23; (95% CI: 0.65–7.63; p=0.2).

          Huang et al. 11 studied the epidemiological characteristics of COVID-19 among 41 patients. In this study, none of those who needed to be admitted to an ICU (n=13) was a current smoker. In contrast, three patients from the non-ICU group were current smokers, with no statistically significant difference between the two groups of patients (p=0.31), albeit the small sample size of the study.

          The largest study population of 1099 patients with COVID-19 was provided by Guan et al. 12 from multiple regions of mainland China. Descriptive results on the smoking status of patients were provided for the 1099 patients, of which 173 had severe symptoms, and 926 had non-severe symptoms. Among the patients with severe symptoms, 16.9% were current smokers and 5.2% were former smokers, in contrast to patients with non-severe symptoms where 11.8% were current smokers and 1.3% were former smokers. Additionally, in the group of patients that either needed mechanical ventilation, admission to an ICU or died, 25.5% were current smokers and 7.6% were former smokers. In contrast, in the group of patients that did not have these adverse outcomes, only 11.8% were current smokers and 1.6% were former smokers. No statistical analysis for evaluating the association between the severity of the disease outcome and smoking status was conducted in that study.

          Finally, Liu et al. 13 found among their population of 78 patients with COVID-19 that the adverse outcome group had a significantly higher proportion of patients with a history of smoking (27.3%) than the group that showed improvement or stabilization (3.0%), with this difference statistically significant at the p=0.018 level. In their multivariate logistic regression analysis, the history of smoking was a risk factor of disease progression (OR=14.28; 95% CI: 1.58–25.00; p= 0.018).

          We identified five studies that reported data on the smoking status of patients infected with COVID-19. Notably, in the largest study that assessed severity, there were higher percentages of current and former smokers among patients that needed ICU support, mechanical ventilation or who had died, and a higher percentage of smokers among the severe cases 12 . However, from their published data we can calculate that the smokers were 1.4 times more likely (RR=1.4, 95% CI: 0.98–2.00) to have severe symptoms of COVID-19 and approximately 2.4 times more likely to be admitted to an ICU, need mechanical ventilation or die compared to non-smokers (RR=2.4, 95% CI: 1.43–4.04).

          In conclusion, although further research is warranted as the weight of the evidence increases, with the limited available data, and although the above results are unadjusted for other factors that may impact disease progression, smoking is most likely associated with the negative progression and adverse outcomes of COVID-19.

          Table 1

          Overview of the five studies included in the systematic review

          Title Setting Population Study design and time horizon Outcomes Smoking rates by outcome
          Zhou et al. 9 (2020)

          Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study
          Jinyintan Hospital and Wuhan Pulmonary Hospital, Wuhan, China All adult inpatients (aged ≥18 years) with laboratory confirmed COVID-19 (191 patients) Retrospective multicenter cohort study until 31 January 2020 Mortality

          54 patients died during hospitalisation and 137 were discharged
          Current smokers: n=11 (6%)

          Non-survivors: n=5 (9%)

          Survivors: n=6 (4%)

          (p=0.20)



          Current smoker vs non-smoker

          Univariate logistic regression

          (OR=2.23; 95% CI: 0.65–7.63; p=0.2)
          Zhang et al. 10

          (2020)

          Clinical characteristics of 140 patients infected with SARS-CoV-2 in Wuhan, China
          No. 7 Hospital of Wuhan, China All hospitalised patients clinically diagnosed as ‘viral pneumonia’ based on their clinical symptoms with typical changes in chest radiology (140 patients) Retrospective 16 January to 3 February 2020 Disease Severity

          Non-severe

          patients: n=82

          Severe patients:

          n=58
          Disease Severity

          Former smokers: n=7

          Severe: n=4 (6.9%)

          Non-severe: n=3 (3.7%) (p= 0.448)



          Current smokers: n=2

          Severe: n=2 (3.4%)

          Non-severe: n=0 (0%)
          Guan et al. 12

          (2019)

          Clinical Characteristics of Coronavirus Disease 2019 in China
          552 hospitals in 30 provinces, autonomous regions, and municipalities in mainland China Patients with laboratory-confirmed COVID-19 (1099 patients) Retrospective until 29 January 2020 Severity and admission to an ICU, the use of mechanical ventilation, or death

          Non-severe patients: n=926 Severe patients: n=173
          By severity



          Severe cases

          16.9% current smokers

          5.2% former smokers

          77.9% never smokers



          Non-severe cases

          11.8% current smokers

          1.3% former smokers

          86.9% never smokers



          By mechanical ventilation, ICU or death



          Needed mechanical ventilation, ICU or died

          25.8% current smokers

          7.6% former smokers

          66.7% non-smokers



          No mechanical ventilation, ICU or death

          11.8% current smokers

          1.6% former smokers

          86.7% never smokers
          Huang et al. 11

          (2020)

          Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China
          A hospital in Wuhan, China Laboratory-confirmed 2019-nCoV patients in Wuhan (41 patients) Prospective from 16 December 2019 to 2 January 2020 Mortality

          As of 22 January 2020, 28 (68%) of 41 patients were discharged and 6 (15%) patients died
          Current smokers: n=3

          ICU care: n=0

          Non-ICU care: n=3 (11%)



          Current smokers in ICU care vs non-ICU care patients (p=0.31)
          Liu et al. 13 (2019)

          Analysis of factors associated with disease outcomes in hospitalised patients with 2019 novel coronavirus disease
          Three tertiary hospitals in Wuhan, China Patients tested positive for COVID-19 (78 patients) Retrospective multicentre cohort study from 30 December 2019 to 15 January 2020 Disease progression

          11 patients (14.1%) in the progression group 67 patients (85.9%) in the improvement/stabilization group 2 deaths
          Negative progression group: 27.3% smokers

          In the improvement group: 3% smokers



          The negative progression group had a significantly higher proportion of patients with a history of smoking than the improvement/stabilisation group (27.3% vs 3.0%)

          Multivariate logistic regression analysis indicated that the history of smoking was a risk factor of disease progression (OR=14.28; 95% CI: 1.58–25.00; p= 0.018)

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          Most cited references 12

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          Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China

          Summary Background A recent cluster of pneumonia cases in Wuhan, China, was caused by a novel betacoronavirus, the 2019 novel coronavirus (2019-nCoV). We report the epidemiological, clinical, laboratory, and radiological characteristics and treatment and clinical outcomes of these patients. Methods All patients with suspected 2019-nCoV were admitted to a designated hospital in Wuhan. We prospectively collected and analysed data on patients with laboratory-confirmed 2019-nCoV infection by real-time RT-PCR and next-generation sequencing. Data were obtained with standardised data collection forms shared by WHO and the International Severe Acute Respiratory and Emerging Infection Consortium from electronic medical records. Researchers also directly communicated with patients or their families to ascertain epidemiological and symptom data. Outcomes were also compared between patients who had been admitted to the intensive care unit (ICU) and those who had not. Findings By Jan 2, 2020, 41 admitted hospital patients had been identified as having laboratory-confirmed 2019-nCoV infection. Most of the infected patients were men (30 [73%] of 41); less than half had underlying diseases (13 [32%]), including diabetes (eight [20%]), hypertension (six [15%]), and cardiovascular disease (six [15%]). Median age was 49·0 years (IQR 41·0–58·0). 27 (66%) of 41 patients had been exposed to Huanan seafood market. One family cluster was found. Common symptoms at onset of illness were fever (40 [98%] of 41 patients), cough (31 [76%]), and myalgia or fatigue (18 [44%]); less common symptoms were sputum production (11 [28%] of 39), headache (three [8%] of 38), haemoptysis (two [5%] of 39), and diarrhoea (one [3%] of 38). Dyspnoea developed in 22 (55%) of 40 patients (median time from illness onset to dyspnoea 8·0 days [IQR 5·0–13·0]). 26 (63%) of 41 patients had lymphopenia. All 41 patients had pneumonia with abnormal findings on chest CT. Complications included acute respiratory distress syndrome (12 [29%]), RNAaemia (six [15%]), acute cardiac injury (five [12%]) and secondary infection (four [10%]). 13 (32%) patients were admitted to an ICU and six (15%) died. Compared with non-ICU patients, ICU patients had higher plasma levels of IL2, IL7, IL10, GSCF, IP10, MCP1, MIP1A, and TNFα. Interpretation The 2019-nCoV infection caused clusters of severe respiratory illness similar to severe acute respiratory syndrome coronavirus and was associated with ICU admission and high mortality. Major gaps in our knowledge of the origin, epidemiology, duration of human transmission, and clinical spectrum of disease need fulfilment by future studies. Funding Ministry of Science and Technology, Chinese Academy of Medical Sciences, National Natural Science Foundation of China, and Beijing Municipal Science and Technology Commission.
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            Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study

            Summary Background Since December, 2019, Wuhan, China, has experienced an outbreak of coronavirus disease 2019 (COVID-19), caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Epidemiological and clinical characteristics of patients with COVID-19 have been reported but risk factors for mortality and a detailed clinical course of illness, including viral shedding, have not been well described. Methods In this retrospective, multicentre cohort study, we included all adult inpatients (≥18 years old) with laboratory-confirmed COVID-19 from Jinyintan Hospital and Wuhan Pulmonary Hospital (Wuhan, China) who had been discharged or had died by Jan 31, 2020. Demographic, clinical, treatment, and laboratory data, including serial samples for viral RNA detection, were extracted from electronic medical records and compared between survivors and non-survivors. We used univariable and multivariable logistic regression methods to explore the risk factors associated with in-hospital death. Findings 191 patients (135 from Jinyintan Hospital and 56 from Wuhan Pulmonary Hospital) were included in this study, of whom 137 were discharged and 54 died in hospital. 91 (48%) patients had a comorbidity, with hypertension being the most common (58 [30%] patients), followed by diabetes (36 [19%] patients) and coronary heart disease (15 [8%] patients). Multivariable regression showed increasing odds of in-hospital death associated with older age (odds ratio 1·10, 95% CI 1·03–1·17, per year increase; p=0·0043), higher Sequential Organ Failure Assessment (SOFA) score (5·65, 2·61–12·23; p<0·0001), and d-dimer greater than 1 μg/mL (18·42, 2·64–128·55; p=0·0033) on admission. Median duration of viral shedding was 20·0 days (IQR 17·0–24·0) in survivors, but SARS-CoV-2 was detectable until death in non-survivors. The longest observed duration of viral shedding in survivors was 37 days. Interpretation The potential risk factors of older age, high SOFA score, and d-dimer greater than 1 μg/mL could help clinicians to identify patients with poor prognosis at an early stage. Prolonged viral shedding provides the rationale for a strategy of isolation of infected patients and optimal antiviral interventions in the future. Funding Chinese Academy of Medical Sciences Innovation Fund for Medical Sciences; National Science Grant for Distinguished Young Scholars; National Key Research and Development Program of China; The Beijing Science and Technology Project; and Major Projects of National Science and Technology on New Drug Creation and Development.
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              Clinical Characteristics of Coronavirus Disease 2019 in China

              Abstract Background Since December 2019, when coronavirus disease 2019 (Covid-19) emerged in Wuhan city and rapidly spread throughout China, data have been needed on the clinical characteristics of the affected patients. Methods We extracted data regarding 1099 patients with laboratory-confirmed Covid-19 from 552 hospitals in 30 provinces, autonomous regions, and municipalities in mainland China through January 29, 2020. The primary composite end point was admission to an intensive care unit (ICU), the use of mechanical ventilation, or death. Results The median age of the patients was 47 years; 41.9% of the patients were female. The primary composite end point occurred in 67 patients (6.1%), including 5.0% who were admitted to the ICU, 2.3% who underwent invasive mechanical ventilation, and 1.4% who died. Only 1.9% of the patients had a history of direct contact with wildlife. Among nonresidents of Wuhan, 72.3% had contact with residents of Wuhan, including 31.3% who had visited the city. The most common symptoms were fever (43.8% on admission and 88.7% during hospitalization) and cough (67.8%). Diarrhea was uncommon (3.8%). The median incubation period was 4 days (interquartile range, 2 to 7). On admission, ground-glass opacity was the most common radiologic finding on chest computed tomography (CT) (56.4%). No radiographic or CT abnormality was found in 157 of 877 patients (17.9%) with nonsevere disease and in 5 of 173 patients (2.9%) with severe disease. Lymphocytopenia was present in 83.2% of the patients on admission. Conclusions During the first 2 months of the current outbreak, Covid-19 spread rapidly throughout China and caused varying degrees of illness. Patients often presented without fever, and many did not have abnormal radiologic findings. (Funded by the National Health Commission of China and others.)
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                Author and article information

                Journal
                Tob Induc Dis
                Tob Induc Dis
                TID
                Tobacco Induced Diseases
                European Publishing on behalf of the International Society for the Prevention of Tobacco Induced Diseases (ISPTID)
                2070-7266
                1617-9625
                20 March 2020
                2020
                : 18
                Affiliations
                [1 ]Department of Oral Health Policy and Epidemiology, Harvard School of Dental Medicine, Boston, United States
                [2 ]School of Medicine, University of Crete, Heraklion, Greece
                Author notes
                CORRESPONDENCE TO Constantine I. Vardavas. Department of Oral Health Policy and Epidemiology, Harvard School of Dental Medicine, Boston, United States. E-mail: vardavas@ 123456hsdm.harvard.edu
                Article
                20
                10.18332/tid/119324
                7083240
                32206052
                © 2020 Vardavas C.I. and Nikitara K

                This is an Open Access article distributed under the terms of the Creative Commons Attribution 4.0 International License.

                Categories
                Editorial

                Respiratory medicine

                tobacco, smoking, covid-19, coronavirus

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