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Translational Oncology logoLink to Translational Oncology
. 2022 Dec 19;28:101605. doi: 10.1016/j.tranon.2022.101605

Impact of coronavirus disease 2019 on lung cancer patients: A meta-analysis

Linlin Wang a,1, Ye Wang b,1, Xianbin Cheng c, Xingzhao Li a, Jun Li d,⁎
PMCID: PMC9760620  PMID: 36568513

Highlights

  • •

    This paper studied the impact of COVID-19 on lung cancer patients.

  • •

    Our meta-analysis included 80 articles with 318,352 patients involved.

  • •

    Lung cancer patients infected with SARS-COV-2 had a higher mortality rate.

  • •

    All-cause mortality rate of lung cancer patients did not change significantly.

  • •

    More attention should be paid on lung cancer patients.

Keywords: SARS-CoV-2, COVID-19, Meta-analysis, Lung cancer

Abstract

Background

The coronavirus disease 2019 (COVID-19) pandemic poses a great challenge to the treatment of lung cancer patients.

Materials and methods

The PubMed, Embase, and Web of Science databases were searched for studies published before March 15, 2022, and Stata 14.0 software was used to perform a meta-analysis with a random-effects model. The odds ratio (OR) along with the corresponding 95% confidence interval (CI) was reported.

Results

Our meta-analysis included 80 articles with 318,352 patients involved. The proportion of lung cancer patients infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was 2.4% (95% CI: 0.02–0.03) prior to the Omicron variant outbreak. Among COVID-19 patients, those with lung cancer showed a higher mortality rate than those with other types of malignant solid tumors (OR = 1.82, 95% CI: 1.61–2.06) and non-cancer patients (OR = 4.67, 95% CI: 3.61–6.05); however, no significant difference was observed in the mortality rate between patients with lung cancer and those with hematologic malignancies (OR = 1.07, 95% CI: 0.85–1.33). SARS-CoV-2 infection significantly increased the mortality rate in lung cancer patients (OR = 8.94, 95% CI: 6.50–12.31). By contrast, the all-cause mortality rate in lung cancer patients (OR = 1.04, 95% CI: 0.69–1.57) and the proportion of patients diagnosed with advanced lung cancer (OR = 1.04, 95% CI: 0.85–1.27) did not significantly change before and after the pandemic.

Conclusions

More attention should be paid on improving the health of lung cancer patients during the COVID-19 pandemic.

1. Introduction

The first case of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection was detected in Wuhan, China, in December 2019; the coronavirus disease 2019 (COVID-19) quickly spread worldwide, subsequently posing considerable challenges to the health systems of numerous countries that were affected [1]. The epidemiology indicates that the pandemic will probably last for several years [2]. As of March 15, 2022, the cumulative number of confirmed cases worldwide exceeded 459 million, and the cumulative number of deaths exceeded 6.04 million [3]. Coronaviruses primarily infect birds and mammals. In recent decades, they have been shown to infect humans [4]. SARS-CoV-2 is a new virus strain belonging to the β-coronavirus group, which has not been previously detected in humans and is currently the seventh member of the human coronavirus family that infects humans. The nucleotide homology of SARS-CoV-2 and the genome of SARS-CoV that causes severe acute respiratory syndrome (SARS) reached 79.5% [5]. The SARS-CoV-2 that causes COVID-19 is less pathogenic than the virus that causes SARS and the Middle East respiratory syndrome (MERS) but is noticeably more contagious [6]. The initial symptoms typically include fever, cough, fatigue, anorexia, loss of smell, myalgia, sore throat, and headache. The symptoms, including tachypnea, severe hypoxemia, lymphopenia, and acute-onset bilateral infiltration, which is greater in the peripheral lung zones, may worsen after approximately a week. Eventually, it can progress to respiratory failure and death [7].

The COVID-19 outbreak has exerted an enormous impact on the global society and economy. According to a British study, around 12,000 new deaths unrelated to SARS-CoV-2 infection have been reported since the pandemic, compared with the previous year [8]. A considerable amount of attention should be paid to identifying other diseases during the epidemic. Patients with cancer, especially lung cancer, form a large group that deserves special attention [9]. Lung cancer is the second most common type of cancer, with approximately 1.8 million deaths and 2.2 million new cases in 2020 [10]. Angiotensin-converting enzyme 2 (ACE2), as the only experimentally confirmed SARS-CoV-2 receptor, can facilitate the entry of viruses into cells, and its expression level is considered to be a marker of susceptibility to COVID-19 [11]. COVID-19 is acquired through the inhalation of respiratory droplets containing SARS-CoV-2; in lung cancer patients, the expression levels of ACE2 are significantly increased, especially in the lower respiratory tract. This suggests that lung cancer patients have a higher risk of developing SARS-CoV-2 infection [12]. Lung cancer patients infected with SARS-CoV-2 tend to develop more severe symptoms, which may be due to the fact that the SARS-CoV-2 can modulate the lung tumor microenvironment and trigger a more severe cytokine response. Lung cancer can also induce an immunosuppressed state, leaving patients vulnerable to SARS-CoV-2 infection and complications [13]. The symptoms of lung cancer patients include cough, expectoration, difficulty of breathing, and fever. After the administration of antineoplastic therapy, patients may experience various treatment-related side-effects. In addition, the detection of COVID-19 on the imaging of lung cancer patients is atypical due to the influence of the tumor. Therefore, it becomes increasingly difficult to identify and diagnose COVID-19 pneumonia early in lung cancer patients [9].

Hence, it is necessary to take extensive efforts to study the association between lung cancer and COVID-19. Herein, this meta-analysis aimed to study the prevalence of COVID-19 in lung cancer patients and the impact of COVID-19 on the mortality rate of these patients.

2. Materials and methods

2.1. Eligibility criteria

(1) Studies that reported the characteristics of patients with lung cancer, (2) studies in which the literature used to evaluate the effect of COVID-19 on patients with advanced lung cancer defined advanced lung cancer as IV non-small cell lung cancer (NSCLC) or extensive small cell lung cancer (SCLC), and (3) regardless of the experimental or control groups, studies whose sample size was more than five patients were included in the meta-analysis.

Studies that discussed various thoracic malignancies without specifying the different tumor subtypes were not included. This meta-analysis evaluated patients with lung cancer, including SCLC and NSCLC, and excluded those with mesothelioma and thymic tumors.

2.2. Information sources

The PubMed, Embase, and Web of Science databases were searched to find articles related to COVID-19 and lung cancer published before March 15, 2022, and further screening was conducted based on the aims of the present study. No language restrictions were applied during the search, to collect comprehensive information on a global scale.

2.3. Search strategy

To retrieve abundant useful literature, the search scope was not limited to studies with information on lung cancer. For COVID-19, only the title and abstract of the articles were searched. In PubMed, the search strategy used was as follows: (((((((((((((((Pulmonary Neoplasms) OR (Neoplasms, Lung)) OR (Lung Neoplasm)) OR (Neoplasm, Lung)) OR (Neoplasms, Pulmonary)) OR (Neoplasm, Pulmonary)) OR (Lung Cancer)) OR (Cancer, Lung)) OR (Cancers, Lung)) OR (Pulmonary Cancer)) OR (Thoracic Cancer)) OR (Thoracic Cancers)) OR (Pulmonary Cancers)) OR (Cancer of the Lung)) OR (Cancer of Lung)) AND (("COVID-19″[Mesh]) OR (((((((((((((((((((((((((((((((((((COVID 19[Title/Abstract]) OR (COVID-19 Virus Disease[Title/Abstract])) OR (COVID 19 Virus Disease[Title/Abstract])) OR (COVID-19 Virus Diseases[Title/Abstract])) OR (Disease, COVID-19 Virus[Title/Abstract])) OR (Virus Disease, COVID-19[Title/Abstract])) OR (COVID-19 Virus Infection[Title/Abstract])) OR (COVID 19 Virus Infection[Title/Abstract])) OR (COVID-19 Virus Infections[Title/Abstract])) OR (Infection, COVID-19 Virus[Title/Abstract])) OR (Virus Infection, COVID-19[Title/Abstract])) OR (2019-nCoV Infection[Title/Abstract])) OR (2019 nCoV Infection[Title/Abstract])) OR (2019-nCoV Infections[Title/Abstract])) OR (Infection, 2019-nCoV[Title/Abstract])) OR (Coronavirus Disease-19[Title/Abstract])) OR (Coronavirus Disease 19[Title/Abstract])) OR (2019 Novel Coronavirus Disease[Title/Abstract])) OR (2019 Novel Coronavirus Infection[Title/Abstract])) OR (2019-nCoV Disease[Title/Abstract])) OR (2019 nCoV Disease[Title/Abstract])) OR (2019-nCoV Diseases[Title/Abstract])) OR (Disease, 2019-nCoV[Title/Abstract])) OR (COVID19[Title/Abstract])) OR (Coronavirus Disease 2019[Title/Abstract])) OR (Disease 2019, Coronavirus[Title/Abstract])) OR (SARS Coronavirus 2 Infection[Title/Abstract])) OR (SARS-CoV-2 Infection[Title/Abstract])) OR (Infection, SARS-CoV-2[Title/Abstract])) OR (SARS CoV 2 Infection[Title/Abstract])) OR (SARS-CoV-2 Infections[Title/Abstract])) OR (COVID-19 Pandemic[Title/Abstract])) OR (COVID 19 Pandemic[Title/Abstract])) OR (COVID-19 Pandemics[Title/Abstract])) OR (Pandemic, COVID-19[Title/Abstract])))

2.4. Study selection process

The articles collected from the database were imported to the NoteExpress software to identify and remove duplicates. After deleting the duplicates, the titles and abstracts were screened, and irrelevant articles were eliminated. The articles that did not meet the requirements were further screened by reading the abstracts or full text. Articles that were fairly related were adopted for subsequent data selection.

2.5. Data selection process and items

Study and data extraction were performed independently by two authors. When disagreements occurred between the two authors, the conflict was resolved through discussion or by consulting a third author.

The following information was extracted from the literature included in the meta-analysis: author, country or region of the study, year of publication, date of the study conducted in experimental and control groups, characteristics of lung cancer patients, characteristics of lung cancer patients complicated by COVID-19, patients with other malignant solid tumors who developed COVID-19, characteristics of hematologic malignancy patients with COVID-19, characteristics of COVID-19 patients with non-cancer illness, and number of patients with advanced lung cancer. If the two groups of independent data could be extracted from the same literature, each group of data was represented by “-A” and “-B.”

2.6. Quality assessment

The quality of the included studies was independently assessed using the Newcastle–Ottawa quality assessment scale. Studies with an overall score of 7 or higher were considered as high-quality studies.

2.7. Reporting bias assessment

Egger's test was used for quantitative analysis of reporting bias. A p value < 0.05 indicates the presence of bias.

2.8. Statistical analysis

The odds ratio (OR) was used for data analysis and evaluation, and the confidence interval (CI) was set at 95%. The I2 statistic was used to quantify the heterogeneity between studies. I2 ≤ 50% indicated a low heterogeneity, 50% < I2 ≤ 75% indicated a moderate heterogeneity, and I2 > 75% indicated a high heterogeneity between the included studies. The random-effects model was utilized for effect estimation. The Stata 14.0 software was used to perform all statistical analyses. A p value < 0.05 was considered significant.

3. Results

3.1. Study selection

A total of 8377 studies were found during the database search, and 3697 duplicates were deleted. After screening the titles and abstracts, 4248 studies irrelevant to this study were eliminated. Among the remaining 432 studies, 352 were excluded after further screening by reading the abstracts or full texts. Hence, only 80 articles were finally included in the meta-analysis (Fig. 1).

Fig. 1.

Fig. 1

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Flow diagram of the study selection process.

3.2. Study characteristics

After screening, 80 articles were included in this meta-analysis, covering 24 countries or regions. A total of 318,352 study patients were analyzed, including 74,228 with lung cancer, 21,263 with other types of malignant solid tumors, 3953 with hematologic malignancies, and 218,908 with non-cancer illness.

3.3. Quality assessment

Results of the Newcastle–Ottawa quality assessment scale indicated that most studies were of high quality (Table 1).

Table 1.

Newcastle–Ottawa quality assessment scale.

Study Publication year Selection Comparability Outcome Quality assessment result
Park et al. 2020 4 2 3 good
Cantini et al. 2022 4 1 2 good
Zhang et al. 2021 4 1 3 good
Fernandez et al. 2021 4 1 1 fair
Pages et al. 2021 4 2 3 good
Mynard et al. 2021 4 1 2 good
Reyes et al. 2021 4 1 1 fair
Leclere et al. 2021 4 1 3 good
Cantini et al. 2021 4 1 1 fair
Manas et al. 2021 4 1 1 fair
Nguyen et al. 2021 4 1 1 fair
Cudero et al. 2021 4 1 1 fair
Dai et al. 2020 4 1 3 good
Kasymjanova et al. 2021 4 1 3 good
Piwkowski et al. 2022 4 2 2 good
Fraser et al. 2021 4 2 3 good
Wang et al. 2021 4 1 3 good
Rogado et al. 2020 4 1 3 good
Leitao et al. 2021 4 1 1 fair
Liu et al. 2020 4 2 2 good
Antras et al. 2020 4 1 3 good
Song et al. 2020 4 1 3 good
Meng et al. 2020 4 1 2 good
Li et al. 2020 4 1 3 good
Melo et al. 2020 4 2 2 good
Cavanna et al. 2020 4 2 2 good
Mehta et al. 2020 4 2 3 good
Tian et al. 2020 4 1 2 good
Yang et al. 2020 4 1 2 good
Sorouri et al. 2020 4 2 3 good
Rogiers et al. 2021 4 2 2 good
Stroppa et al. 2020 4 1 2 good
Lee et al. 2020 4 1 3 good
Assaad et al. 2020 4 1 3 good
Lunski et al. 2020 4 2 3 good
Duarte et al. 2020 4 1 2 good
Zhang et al. 2020 4 1 3 good
Oliveira et al. 2020 4 1 3 good
Dai et al. 2020 4 1 2 good
Erdal et al. 2020 4 2 3 good
Roel et al. 2021 4 1 3 good
Caruso et al. 2021 4 2 2 good
Basse et al. 2021 4 1 3 good
Ozer et al. 2021 4 1 3 good
Liang et al. 2021 4 2 3 good
Guo et al. 2021 4 1 3 good
Benderra et al. 2021 4 1 3 good
Ozdemir et al. 2021 4 2 3 good
Zylberman et al. 2021 4 2 2 good
Bondeson et al. 2021 4 1 2 good
Farooque et al. 2021 4 1 3 good
Bernard et al. 2021 4 2 2 good
Martin et al. 2021 4 2 2 good
Linehan et al. 2021 4 2 3 good
Pinato et al. 2021 4 1 3 good
Fernandes et al. 2021 4 2 3 good
Ayhan et al. 2021 4 1 3 good
Demirci et al. 2021 4 1 3 good
Safari et al. 2021 4 1 3 good
Ospina et al. 2021 4 2 3 good
Trifanescu et al. 2022 4 2 3 good
Varnai et al. 2022 4 1 3 good
Guven et al. 2021 4 1 2 good
Chai et al. 2021 4 1 3 good
Preda et al. 2022 4 1 3 good
Rugge et al. 2022 4 2 3 good
Russell et al. 2022 4 1 2 good
Morais et al. 2021 4 1 3 good
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3.4. Results of individual studies

Our study presents the results of individual studies in structured tables (Table 2, Table 3, Table 4, Table 5). Two meta-analyses specifically compared the mortality rate between lung cancer patients with COVID-19 and other malignant tumor patients with COVID-19. Peravali et al. published a meta-analysis based on 12 studies. They concluded that the mortality rate of lung cancer patients with COVID-19 was higher than that of other types of cancer patients with COVID-19 (OR = 1.62, 95% CI: 1.06–2.48) [14]. However, after reviewing 13 studies, the meta-analysis of Lei et al. yielded an opposite conclusion; no significant difference was found in the mortality rate between lung cancer patients with COVID-19 and other types of cancer patients with COVID-19 (OR = 1.47, 95% CI: 0.98–2.20) [15]. The lower range value of the 95% CI of the above two meta-analyses was extremely close to the critical value. The results were not stable, and the conclusions were likely to be reversed after the inclusion of new literature. Due to the significant differences between malignant solid tumors and hematologic malignancies, we studied the mortality rate of SARS-CoV-2 infection in the above two types of patients, which were not uniformly classified as “other types of cancer patients”; forty-five articles that reported this topic were included in the analysis.

Table 2.

Prevalence of COVID-19 in lung cancer patients.

Author Rigion Publication year Study period Lung cancer Lung cancer with COVID-19
Calles et al. [16]. Spain 2020 2020.2.20–2020.6.20 242 11
Park et al. [18]. America 2020 2020.1.31–2020.6.1 696 24
Pages et al. [22]. France 2021 2020 11,634 51
Leclere et al. [25]. France 2021 2020.3.14–2020.5.11 115 6
Manas et al. [27]. Spain 2021 2020.1–2020.6 96 9
Nguyen et al. [28]. America 2021 2020.1.1–2020.7.1 59 9
Cudero et al. [29]. Spain 2021 2020.1.1–2020.7.31 70 11
Fraser et al. [33]. England 2021 2020.3.1–2020.6.1 352 7
Mandala et al. [34]. Italy 2021 2020.3.5–2020.5.18 100 22
Banfill et al. [35]. England 2022 2020.4.2–2020.10.2 1553 33
Teixeira et al. [39]. Brazil 2021 2020.6–2021.1 32 1
Peer et al. [40]. Israel 2022 2020.2–2020.12 113 2
Wang et al. [62] America 2020 By 2020.8.14 34 830 100
Roel et al. [63]. Spain 2021 2020.3.1–2020.5.6 7569 140
Kwon et al. [75]. America 2021 2020.2.1–2020.12.31 1404 33
Ayhan et al. [80]. Turkey 2021 2020.3.11–2020.6.11 229 27
Basse et al. [85]. France 2021 2020.3.23–2020.4.17 314 3
Fillmore et al. [92]. America 2021 2010.1.1–2020.5.4 2806 121
Zorzi et al. [93]. Italy 2021 2020.2.22–2020.7.31 1934 45
Russell et al. [94]. England 2022 2020.3.1–2020.5.31 275 6
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COVID-19: coronavirus disease 2019, NA: not applicable.

Table 3.

Characteristics of lung cancer patients with COVID-19, other malignant tumor patients with COVID-19, and non-cancer patients with COVID-19.

Author Rigion Publication year Study period Lung cancer with COVID-19
 Other malignant solid tumors with COVID-19
 Hematologic malignancies with COVID-19
 COVID-19 without cancer
Number Death Number Death Number Death Number Death
Dai et al. [30]. China 2020 2020.1.1–2020.3.1 31 8 NA NA NA NA 186 15
Wang et al. [36] China 2021 2020.2.4–2020.4.11 13 1 NA NA NA NA 52 0
Rogado et al. [37]. Spain 2020 2020.2–2020.4 17 9 NA NA NA NA 1861 183
Liu et al. [41]. China 2020 2020.12.17–2020.3.18 49 14 144 23 NA NA NA NA
Antras et al. [42]. Spain 2020 2020.2.21–2020.5.8 14 5 59 13 NA NA NA NA
Song et al. [43]. China 2020 2020.1.1–2020.3.25 61 16 187 24 NA NA NA NA
Meng et al. [44]. China 2020 2020.1.18–2020.3.27 17 3 76 21 16 8 2556 261
Li et al. [45]. China 2020 2020.1.20–2020.4.4 5 2 45 12 9 2 1794 191
Melo et al. [46]. Brazil 2020 2020.4.30–2020.5.26 7 4 138 48 34 8 NA NA
Cavanna et al. [47]. Italy 2020 2020.4.4–2020.5.4 12 7 30 13 5 2 NA NA
Mehta et al. [48]. America 2020 2020.3.18–2020.4.8 11 6 153 35 54 20 NA NA
Tian et al. [49]. China 2020 2020.1.13–2020.3.18 23 9 197 32 12 5 519 46
Yang et al. [50]. China 2020 2020.1.13–2020.4.20 24 6 159 25 22 9 NA NA
Sorouri et al. [51]. Iran 2020 2020.2.25–2020.4.21 5 0 24 10 24 17 106 17
Rogiers et al. [52]. North America, Europe and Australia 2021 2020.3.5–2020.5.15 17 4 93 14 NA NA NA NA
Stroppa et al. [53]. Italy 2020 2020.2.21–2020.3.18 8 2 14 5 NA NA 31 5
Lee et al. [54]. England 2020 2020.3.18–2020.5.8 111 43 706 172 227 80 NA NA
Lunski et al. [56]. America 2020 2020.3.1–2020.4.30 26 8 225 39 42 19 4833 418
Duarte et al. [57]. Brazil 2020 By 2020.9.28 51 38 475 308 155 96 681 217
Zhang et al. [58]. China 2020 2020.1.5–2020.3.18 21 5 77 16 9 2 NA NA
Oliveira et al. [59]. Brazil 2020 2020.3–2020.7 5 4 72 60 NA NA NA NA
Dai et al. [60]. China 2020 2020.1.1–2020.2.24 22 4 74 5 9 3 NA NA
Erdal et al. [61]. Turkey 2020 2020.3.15–2020.5.15 7 1 52 12 12 4 NA NA
Roel et al. [63]. Spain 2021 2020.3.1–2020.5.6 140 37 4740 883 513 117 93,558 4153
Caruso et al. [64]. Brazil 2021 2020.2–2020.11 20 14 194 108 60 33 NA NA
Basse et al. [65]. France 2021 2020.3.13–2020.5.1 18 6 104 15 19 5 NA NA
Ozer et al. [66]. America 2021 2020.3–2020.10 8 4 52 17 8 4 NA NA
Liang et al. [67]. China 2021 2020.1.18–2020.3.20 14 2 83 16 12 5 2951 229
Guo et al. [68]. China 2021 2019.12.31–2020.2.20 50 11 215 12 17 2 5176 344
Benderra et al. [69]. France 2021 2020.3.3–2020.5.19 85 37 799 253 264 93 NA NA
Ozdemir et al. [70]. Turkey 2021 2020.3.11–2020.5.20 157 18 1366 59 NA NA NA NA
Zylberman et al. [71]. Argentina 2021 2020.5–2020.11 14 7 51 17 9 0 NA NA
Bondeson et al. [72]. Sweden 2021 2020.3.1–2020.8.14 11 1 96 12 NA NA NA NA
Farooque et al. [73]. Pakistan 2021 2020.4–2020.9 159 7 1360 65 NA NA NA NA
Bernard et al. [74]. France 2021 2020.3–2020.4 873 359 3460 1024 1389 470 83,329 13,057
Martin et al. [76]. France 2021 2020.2–2020.5 32 10 180 53 NA NA NA NA
Linehan et al. [77]. Ireland 2021 2020.3–2020.5 7 6 18 3 NA NA NA NA
Pinato et al. [78]. Europe 2021 2020.2.27–2020.9.10 176 74 991 277 142 83 NA NA
Fernandes et al. [79]. Brazil 2021 2020.4.2–2020.8.31 18 6 346 35 47 10 NA NA
Ayhan et al. [81]. Turkey 2021 2020.3.11–2020.5.31 26 4 66 18 NA NA NA NA
Safari et al. [83]. Iran 2021 2020 7 2 46 18 13 5 NA NA
Ospina et al. [84]. Columbia 2021 2020.4.1–2020.10.31 37 20 418 110 NA NA NA NA
Trifanescu et al. [86]. Rumania 2022 2020.5–2020.12 8 2 81 3 NA NA NA NA
Varnai et al. [87]. England 2022 2020.3.18–2020.8.1 265 131 1646 573 604 262 NA NA
Chai et al. [89]. China 2021 2020.1.1–2020.3.18 25 4 124 22 17 8 498 42
Preda et al. [90]. Rumania 2022 2020.4–2021.2 66 5 250 17 25 4 NA NA
Rugge et al. [91]. Italy 2022 2020.2.22–2020.7.31 62 23 1541 358 184 54 20,777 2008
Russell et al. [94]. England 2022 2020.3.1–2020.5.31 6 1 36 5 NA NA NA NA
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COVID-19: coronavirus disease 2019, NA: not applicable.

Table 4.

Characteristics of lung cancer patients with and without COVID-19.

Author Rigion Publication year Study period Experimental group
 Control group
Lung cancer with COVID-19 Death Lung cancer without COVID-19 Death
Pages et al. [22]. France 2021 2020 51 11 11,583 232
Leclere et al. [25]. France 2021 2020.3.14–2020.5.11 6 0 109 1
Nguyen et al. [28]. America 2021 2020.1.1–2020.7.1 9 4 50 8
Fraser et al. [33]. England 2021 2020.3.1–2020.6.1 7 2 345 5
Assaad et al. [55]. France 2020 2020.3.1–2020.4.25 7 3 35 5
Roel et al. [63]. Spain 2021 2020.3.1–2020.5.6 140 37 7429 314
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COVID-19: coronavirus disease 2019, NA: not applicable.

Table 5.

Characteristics of lung cancer patients before and after the COVID-19 pandemic.

Author Rigion Publication year Experimental group period Control group period Experimental group
 Control group
Lung cancer Death Advanced Lung cancer Death Advanced
Park et al. [17]. Korea 2020 2020.2–2020.6 2017.2–2017.6
2018.2–2018.6
2019.2–2019.6		 169 NA 93 443 NA 208
Cantini et al. [19]. Italy 2022 2020.3–2020.12 2019.3–2019.12 1399 NA 1084 1486 NA 1125
Zhang et al. [20]. China 2021 2020.2–2020.7 2019.2–2019.7 231 NA 9 156 NA 8
Fernandez et al. [21]. Spain 2021 2020.2–2020.6 2019.2–2019.6 40 NA 28 20 NA 15
Pages et al. [22]. France 2021 2020 2018–2019 11,634 244 NA 24,380 561 NA
Mynard et al. [23]. America 2021 2020.7–2021.3 2019.7–2020.3 241 NA 81 269 NA 74
Reyes et al. [24]. Spain 2021 2020.1–2020.6 2019.1–2019.6 62 27 35 100 23 43
Cantini et al. [26]. Italy 2021 2020.3–2020.12 2020.3–2020.12 1381 NA 594 1443 NA 996
Manas et al. [27]. Spain 2021 2020.1–2020.6 2020.1–2020.6 96 25 82 133 27 114
Cudero et al. [29].-A Spain 2021 2020.1.1–2020.7.31 2019.1.1–2019.7.31 70 NA 58 132 NA 88
Cudero et al. [29].-B Spain 2021 2020.1.1–2020.7.31 2019.1.1–2019.7.31 91 NA 49 101 NA 56
Kasymjanova et al. [31]. Canada 2021 2020.3.1–2021.2.28 2019.3.1–2020.2.29 103 NA 59 130 NA 68
Piwkowski et al. [32]. Poland 2022 2020.1.1–2020.12.31 2019.1.1–2019.12.31 3236 33 NA 4066 46 NA
Leitao et al. [38]. Portugal 2021 2020.9–2020.10 2019.9–2019.10 80 NA 49 94 NA 61
Demirci et al. [82]. Turkey 2021 2019.12.1–2020.5.31 2017.12.1–2018.5.31
2018.12.1–2019.5.31		 259 56 NA 502 118 NA
Guven et al. [88]. Turkey 2021 2020.3–2020.12 2019.3–2019.12 120 101 88 159 132 115
Morais et al. [95]. Portugal 2021 2020.3.2–2020.7.1 2019.3.2–2019.7.1 164 58 NA 204 73 NA
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COVID-19: coronavirus disease 2019, NA: not applicable.

3.5. Results of meta-analysis

Data were extracted from 20 studies to calculate the prevalence of COVID-19 in lung cancer patients, and the results showed that 2.4% of lung cancer patients were infected with SARS-CoV-2 (95% CI: 0.02–0.03, I2 = 95.5%, Fig. 2). Among cancer patients with COVID-19, the mortality rate in lung cancer patients was notably higher than that in other malignant solid tumor patients (OR = 1.82, 95% CI: 1.61–2.06, I2 = 16.3%, p < 0.001, Fig. 3A). However, no significant difference was observed in the mortality rate between patients with lung cancer and those with hematologic malignancies (OR = 1.07, 95% CI: 0.85–1.33, I2 = 45.8%, p = 0.575, Fig. 3B); the OR value was nearly 1, indicating that the mortality rate of the two groups was considerably close. Among COVID-19 patients, the mortality rate of lung cancer patients was significantly higher than those without cancer (OR = 4.67, 95%CI: 3.61–6.05, I2 = 45.3%, p < 0.001, Fig. 4A).

Fig. 2.

Fig. 2

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Forest plot of the proportion of lung cancer patients infected with SARS-CoV-2.

Fig. 3.

Fig. 3

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A: Forest plot of the difference in the mortality rate between lung cancer patients with COVID-19 and other types of malignant solid tumor patients with COVID-19.

B: Forest plot of the difference in the mortality rate between lung cancer patients with COVID-19 and hematologic malignancy patients with COVID-19.

Fig. 4.

Fig. 4

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A: Forest plot of the difference in the mortality rate between lung cancer patients with COVID-19 and non-cancer patients with COVID-19.

B: Forest plot of the difference in the mortality rate between lung cancer patients with and without COVID-19.

Among lung cancer patients, a higher mortality rate was possibly associated with SARS-CoV-2 infection (OR = 8.94, 95% CI: 6.50–12.31, I2 = 0, p < 0.001, Fig. 4B). Certain characteristics of lung cancer patients were also compared before and after the COVID-19 pandemic. Results showed that after the outbreak of COVID-19, the proportion of patients diagnosed with advanced lung cancer did not significantly increase (OR = 1.04, 95% CI: 0.69–1.57, I2 = 92.7%, p = 0.854, Fig. 5A). Additionally, no obvious difference was observed in the all-cause mortality rate among patients between the two time periods (OR = 1.04, 95% CI: 0.85–1.27, I2 = 41.1%, p = 0.727, Fig. 5B).

Fig. 5.

Fig. 5

Open in a new tab

A: Forest plot of the proportion of patients diagnosed with advanced lung cancer before and after the COVID-19 pandemic.

B: Forest plot of the all-cause mortality rate of lung cancer patients before and after the COVID-19 pandemic.

3.6. Reporting biases

Results of the Egger's test indicated that there was no publication bias in all the studies (Supplementary File 1).

4. Discussion

Among all patients with various types of cancer, particular concerns should be raised among those with lung cancer during this pandemic as the respiratory tract, which is the primary site of viral infection, is compromised by the tumor. Lung cancer patients are exceptionally vulnerable compared with those with other cancer types when outbreaks of respiratory viruses occur because their damaged respiratory epithelium probably accelerates the invasion of virus into the lungs [96]. Approximately 80.0% of primary lung cancer cases worldwide are caused by smoking [97] Structural lung damage and reduced lung function caused by smoking, and lung damage caused by lung cancer treatment (surgery and radiotherapy) leads to additionally severe symptoms and consequences of SARS-CoV-2 infection in patients with lung cancer compared with other malignant solid tumors [98]. Therefore, the mortality rate of lung cancer patients with COVID-19 is higher than that of other malignant solid tumor patients with COVID-19.

Our study showed that patients with hematologic malignancies who developed COVID-19 had a high mortality rate, which was not significantly different from that of patients with lung cancer who developed COVID-19. Cooksley et al. found a similar pattern when they examined the clinical differences in influenza virus infection among patients with various types of cancer. Compared with patients with other types of cancer, those with lung cancer or hematologic malignancies tended to have a longer average length of hospital stay, frequently required ventilatory support, had higher hospitalization costs, and had a higher case fatality rate [99]. The immune system protects the human body from viruses by producing antibodies, while health recovery relies on both humoral (antibody) and cell-mediated immune responses [100]. Anti-CD20 therapy is widely used to treat hematologic malignancies; however, one significant side-effect is persistent impairment of the patient's immune function. For example, both T-cell dependent and independent responses are severely impaired after rituximab treatment, lasting for at least 6 months [101]. Respiratory viruses usually successfully invade and reproduce in the body of individuals with low immune function, and the severity of disease caused by infection is closely related to the degree of the impaired immune function [100]. Patients with hematologic malignancies are generally at a higher risk of developing an infection, which is the primary cause of death in patients with hematologic malignancies, and COVID-19 has been proven to cause various hematologic abnormalities. Hence, compared with most COVID-19 patients with malignant solid tumors, COVID-19 patients with blood cancer have a higher mortality rate [102,103].

Although the mortality rate of lung cancer patients with COVID-19 was higher than that of patients without COVID-19, no significant difference was found in the mortality rate among lung cancer patients before and after the pandemic. In response to this situation, our study presents the following findings: 1. The prevalence of COVID-19 among lung cancer patients is 2.4%, which has a limited impact on the all-cause mortality rate of lung cancer patients. 2. Lung cancer can be cured if it is detected at an early stage [104]. One of the reasons for the high mortality rate in lung cancer patients is that approximately 57% of patients are diagnosed at a later stage [105]. COVID-19 has caused a tremendous amount of social panic. A survey conducted in Italy reported that 21% of lung cancer patients were more concerned about having COVID-19 than having lung cancer [106]. Duong et al. reported that this excessive fear of COVID-19 would discourage potential lung cancer patients from participating in lung cancer screening, possibly leading to the increase in the proportion of patients with more advanced cases [107]. Our findings revealed that after the outbreak of COVID-19, the proportion of patients diagnosed with advanced lung cancer did not notably increase, which may probably explain why the mortality rate of lung cancer did not significantly change after the outbreak.

The government's recommendations for increasing social distancing and isolation have heightened the fear of COVID-19 among lung cancer patients, who may avoid the screening and treatment for lung cancer to prevent infection [107]. Fujita et al. found that during the COVID-19 epidemic, 9.1% of lung cancer patients experienced anxiety and consequently requested to delay their treatment [108]. The concerns of lung cancer patients are reasonable. Lung cancer patients need to visit multiple medical institutions frequently and undergo blood extraction, imaging examinations, bronchoscopy, radiotherapy, chemotherapy, targeted therapy, and other procedures, which increase the risk of acquiring SARS-CoV-2 infection. In Italy, the lung cancer diagnosis rate in 2020 decreased by 6.9% compared with that reported in the previous year [19]. From June to September 2020, the rate of lung cancer-related surgical procedures performed in Italy decreased by 36% compared with those performed in the same period in 2019 [109]. A similar trend occurred during the SARS outbreak in 2003. In Taiwan, 64% of lung cancer patients participating in clinical trials were reluctant to visit the hospital when the international spread of SARS became evident, and about 4% decided to discontinue all treatments [110]. In many countries, the wards used to treat lung cancer patients were designated as isolation and treatment areas for COVID-19 patients during the outbreak [111]. In a hospital in Madrid, Spain, which had 1350 beds, more than 1100 were occupied by patients with COVID-19 during the outbreak [112]. The sudden shortage of medical resources has further delayed the treatment of an increasing number of lung cancer patients. Delayed cancer treatment may increase the 5-year mortality rate by 4.8%–16.6% (depending on the cancer type), which exceeds the mortality rate of COVID-19 [113]. The American College of Surgeons found that a delay of over 8 weeks in the treatment of NSCLC is an independent risk factor for disease progression [114]. The treatment for lung cancer patients, including chemotherapy, immunotherapy and targeted therapy, should be selected based on the individual symptoms, biomarkers, and comorbidities; however, the reduction of side-effects and the risk of COVID-19 infection should be considered. The most important guiding principle in lung cancer treatment is the timely provision of appropriate medical coverage rather than unreasonable delays in treatment [7]. When medical resources are restricted due to the admission of COVID-19 patients, the government should open new temporary hospitals instead of occupying the pulmonary department as specialized units for COVID-19 patients, which may result in serious consequences for lung cancer patients [32].

5. Limitations

Our study has certain limitations. 1. Since November 2021, the Omicron variant of SARS-CoV-2 has rapidly spread worldwide. This variant may be 10-fold more contagious than the original virus and is approximately 2.8-fold more infectious than the Delta variant [115]. It has led to a dramatic increase in the number of COVID-19 patients. In the United Kingdom, Omicron cases accounted for more than 99% of all sequential cases a week after January 10, 2022 [116]. When the prevalence of COVID-19 in lung cancer patients was calculated in our study, all the cases involved had occurred prior to the Omicron outbreak. Therefore, the prevalence of COVID-19 in lung cancer patients may presumably increase afterward. 2. Patients infected with the Omicron variant had a significantly decreased hospitalization rate, disease severity, and mortality rate than of those infected with the previous variant [117]. Whether infection with the Omicron variant has a significant effect on the mortality of lung cancer patients should be investigated further by incorporating more studies in the future. 3. The acquisition of immunity through vaccines is regarded as one of the best countermeasures against COVID-19 [118]. Trontzas et al. showed that lung cancer patients could demonstrate sufficient antibody response if they were vaccinated with two-dose regimens [119]. Vaccination may affect the prevalence and mortality rate of COVID-19 in lung cancer patients, but we were unable to conduct a study on this because we could not determine whether the lung cancer patients in our sample had received COVID-19 vaccines.

6. Conclusions

Despite the unchanged all-cause mortality rate, our findings suggested an increased mortality rate in lung cancer patients infected with SARS-CoV-2, whose health deserves more attention, particularly during the COVID-19 pandemic.

Author contributions statement

All authors have full access to the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Funding sources

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

CRediT authorship contribution statement

Linlin Wang: Writing – original draft, Investigation. Ye Wang: Writing – original draft, Investigation. Xianbin Cheng: Writing – review & editing. Xingzhao Li: Writing – review & editing. Jun Li: Conceptualization, Data curation, Investigation.

Declaration of Competing Interest

None.

Acknowledgments

None.

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.tranon.2022.101605.

Appendix. Supplementary materials

mmc1.doc (25.5KB, doc)

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