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The effect of fruit and vegetable intake on the development of lung cancer: a meta-analysis of 32 publications and 20 414 cases

Abstract

Background/Objectives:

Quantification of the association between the intake of vegetables and fruits and the risk of lung cancer is controversial. Thus, we conducted a meta-analysis to assess the relationship between vegetables and fruits and lung cancer risk.

Subjects/Methods:

Pertinent studies were identified by a search in PubMed and Web of Knowledge. Random-effects models were used to calculate summary relative risks (RR) and the corresponding 95% confidence intervals (CI). Publication bias was estimated using Begg’s test.

Results:

Finally, 30 articles with 37 studies comprising of 20 075 lung cancer cases for vegetables intake with lung cancer risk and 31 articles with 38 studies comprising of 20 213 lung cancer cases for fruits intake with lung cancer risk were included in this meta-analysis. The combined results showed that there were significant associations between vegetables and fruits intake and lung cancer risk. The pooled RR were 0.74 (95% CI: 0.67, 0.82) for vegetables and 0.80 (95% CI: 0.74, 0.88) for fruits. Significant association was found in females on vegetables intake and lung cancer but not in males. The association was also stronger in females than males on fruits intake and lung cancer risk. No publication bias was detected.

Conclusions:

Our analysis indicated that intake of vegetables and fruits may have a protective effect on lung cancer, and the associations were stronger in females. As the potential biases and confounders could not be ruled out completely in this meta-analysis, further studies are needed.

Introduction

Lung cancer is the most common incident cancer and cause of cancer related death worldwide,1 with an estimated 1.3 million newly diagnosed cases each year. The age-adjusted incidence rate of lung cancer was recently reported at 62.6 cases per 100 000 people per year, and the age-adjusted death rate at 50.6 per 100 000 people per year.2 Thus, primary prevention of lung cancer is critical. Many studies have shown that lung cancer is associated with genetic factors,3, 4 and environmental factors including tobacco use,5 alcohol consumption,6 vitamins7 and intake of fruits and vegetables8 can also affect the incidence of lung cancer.

Vegetable and fruit consumption has been hypothesized to influence lung cancer risk. The 2007 World Cancer Research Fund/American Institute for Cancer Research expert report ‘Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective’ concluded that fruits probably protect against lung cancer and that there is only limited evidence suggesting that non-starchy vegetables, selenium and foods containing it protect against lung cancer.9 A diet rich in vegetables and fruits is recommended to prevent cancer generally,10, 11, 12 but it is unknown if it protects against specifically lung cancer. Recent reports have examined the associations between fruits and vegetables intake on the risk of lung cancer, but the findings are inconsistent. We therefore conducted a comprehensive meta-analysis to better clarify the association between vegetables and fruits intake and lung cancer risk.

Materials and methods

Search strategy

A comprehensive search was conducted for available articles published in English using the databases PubMed and Web of Knowledge up to June 2014 and by hand-searching the reference lists of the computer-retrieved articles. The following search terms were used: ‘lung’ and 'neoplasm/carcinoma/cancer, combined with ‘nutrition/diet/lifestyle/fruit/vegetable.’ Two investigators searched articles and reviewed of all retrieved studies independently. Disagreements between the two investigators were resolved by consensus with a third reviewer.

Inclusion criteria

All relevant studies reporting associations between vegetables and fruits intake and lung cancer risk were considered for inclusion. The inclusion criteria were as follows: (i) use a case-control, nested case-control or cohort design; (ii) the exposure of interest were vegetables and fruits or total vegetables or total fruits; (iii) the outcome of interest was lung cancer; (iv) report associations in the form of relative risks (RR) with the 95% confidence intervals (CI) for total vegetables or total fruits or providing us with sufficient information to calculate them. Accordingly, the following exclusion criteria were also used: (i) reviews and (ii) repeated or overlapped publications. In the present meta-analysis, we included the studies evaluating fruit or vegetable groups classified as ‘all’ or ‘total.’ Exposures presented as cooked vegetables, raw vegetables, other vegetables, citrus fruits or other fruits were not considered as equivalent to ‘all’ or ‘total’ and thus were not included. Studies that reported ‘fresh vegetables’ or ‘fresh fruits’ were included according to the hypothesis that fresh vegetables or fruits account for a very high proportion of the total consumption.13

Data extraction

Two researchers independently extracted the following information: name of the first author, study design, publication year, geographic location, number of cases and controls or participants, type of controls, exposure classification, confounders adjusted for and the RR estimates with corresponding 95% CI for the highest versus lowest level. From each study, we extracted the risk estimates adjusted for the greatest number of potential confounders. If there was a disagreement between the two investigators about the eligibility data, it was resolved by consensus with a third reviewer.

Statistical analysis

The pooled measure was calculated as the inverse variance-weighted mean of the natural logarithm of multivariate-adjusted RR with 95% CI for the highest vs lowest levels to assess the association between vegetables and fruits intake with the risk of lung cancer. The DerSimo-nian and Laird random effect model was adopted as the pooling method.14 The Q-test and I2 of Higgins and Thompson were used to assess heterogeneity15 among included studies. I2 describes the proportion of total variation attributable to between-study heterogeneity as opposed to random error or chance. Meta-regression with restricted maximum-likelihood estimation was performed to describe the potentially important covariates.16 Publication bias was estimated using Begg’s test.17 A study of influence analysis 18 was conducted to describe how robust the pooled estimator is to removal of individual studies. An individual study is suspected of excessive influence if the point estimate of its omitted analysis lies outside the 95% CI of the combined analysis. All analyses were conducted using STATA software, version 10.0 (StataCorp LP, College Station, TX, USA). Two-tailed P0.05 was accepted as statistically significant.

Results

Search results and study characteristics

The search strategy identified 1369 articles from Pubmed and 1854 articles from the Web of Knowledge, and 59 articles were reviewed in full after reviewing the title/abstract. By studying reference lists, we identified three additional articles. Thirty articles were further excluded whereas 22 articles did not report the RR/odds ratio, 3 articles were duplicate publications and 5 articles were review articles. Hence, 32 articles 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50 were included in this meta-analysis. The detailed steps of our literature search are shown in Figure 1. The characteristics of these studies are presented in Table 1. Twelve articles were conducted in Europe, 12 from America and 8 from Asia.

Figure 1
figure1

The flow diagram of screened, excluded and analyzed publications.

Table 1 Characteristics of studies on vegetable and fruit intake and lung cancer risk

Total vegetables intake and lung cancer

For vegetable intake and lung cancer risk, data from 30 articles12, 13, 14, 15, 16, 18, 19, 20, 21, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43 with 37 studies (18 cohort studies and 19 case-control studies) were used comprising of 20 075 lung cancer cases. Inverse association between vegetable intake and risk of lung cancer was reported in 14 studies, and no significant association between vegetable intake with risk of lung cancer was reported in 23 studies. Pooled results suggested that highest vegetable intake versus lowest level was significantly associated with the risk of lung cancer (summary RR=0.74, 95% CI: 0.67, 0.82; I2=60.9%, Pheterogeneity=0.00). In subgroup analyses for study design, the pooled RR of lung cancer for the highest category of vegetable intake versus the lowest category were 0.88 (95% CI: 0.81, 0.97) and 0.62 (95% CI: 0.54, 0.70) for cohort and case-control studies, respectively. (Figure 2) When we conducted the subgroup analysis by geographic locations, significant associations were found between vegetable intake and lung cancer in all strata. The association was significant for females (RR=0.66, 95% CI: 0.52, 0.84) but not for males. The main results are summarized in Table 2.

Figure 2
figure2

The forest plot between highest versus lowest categories of vegetables intake and lung cancer risk.

Table 2 Summary risk estimates of the association between vegetables and fruits and lung cancer risk

Total fruit intake and lung cancer

Data from 31 articles 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 43 with 38 studies (19 cohort studies and 19 case-control studies) for fruit intake and lung cancer risk were used including 20 213 lung cancer cases. Eight studies reported that fruit intake can reduce the lung cancer risk, whereas 30 studies didn’t show the significant association between fruit intake and lung cancer risk. The meta-analysis showed an inverse association between total fruit intake and lung cancer risk (summary RR=0.80, 95% CI: 0.74, 0.88; I2=47.9%, Pheterogeneity=0.001). In subgroup analyses for study design, the pooled RR of lung cancer for the highest category of fruit intake versus the lowest category were 0.84 (95% CI: 0.75, 0.94) and 0.77 (95% CI: 0.67, 0.88) for cohort studies and case-control studies, respectively (Figure 3). For the subgroup of geographic locations, the associations were significant in the Europe, America and Asia. Inverse associations between fruit intake with risk of lung cancer were found in the subgroups of sex (female and male). The main results are summarized in Table 2.

Figure 3
figure3

The forest plot between highest versus lowest categories of fruits intake and lung cancer risk.

Sources of heterogeneity and meta-regression

In order to explore the moderate-to-high between-study heterogeneity found in several analysis, univariate meta-regression with the covariates of publication year, location where the study was conducted, study design (case-control or cohort), number of cases and sex (male or female) was performed. No significant findings were found in the above-mentioned analysis.

Influence analysis and publication bias

Sensitivity analysis showed that no individual study had excessive influence on the above-mentioned pooled effect. Begg’s test showed no evidence of significant publication bias for the analysis between breast cancer risk and vegetables intake (P=0714) and fruits intake (P=0.125).

Discussion

Finding from this meta-analysis suggested that the intake of vegetables and fruits are associated with significant reductions in the risk of lung cancer. The associations were also found in subgroups of Europe, America and Asia for vegetables or fruit intake and lung cancer risk. For the subgroup analysis of sex, the association was significant in females on vegetables intake and lung cancer but not in the males. The association was also stronger in females than males on fruits intake and lung cancer risk. This is because some studies included were not adjusted for smoking status and men are more likely to smoke than women, as smoking is a risk factor for lung cancer.

The mechanisms of the anti-cancer properties of fruits and vegetables have not been thoroughly investigated. A few in vitro and epidemiological studies have discovered mechanisms that allow fruits and vegetables to protect against some cancers.51, 52, 53 The suggested mechanisms for the major role of vegetables and fruit in the prevention of cancer include: modulation of DNA methylation; protection from and repair of DNA damage; promotion of apoptosis and induction of detoxifying phase-II enzymes.54 Antioxidants and dietary fibers might have a key role in the prevention of lung cancer development. The protective effects of vegetables and fruits are thought to be mediated by multiple components, including beta-carotene, fiber, vitamins, alpha-tocopherol, retinoids, phytoestrogens and folate.55 These components are involved in numerous biological processes that may alter cancer risk, including the inhibition of cell growth, the normal synthesis and methylation of DNA, and protection against oxidative stress and DNA damage.56

As a meta-analysis of published studies, our findings showed some advantages. First, a major strength of this study was the large number of participants included in this analysis and this may derive a more precise estimation of the relationship between vegetables and fruits and lung cancer risk. Second, no significant publication bias was found, indicating that our results are stable. However, there were some limitations in this meta-analysis. First, a meta-analysis of observational studies is susceptible to potential bias inherent in the original studies, especially for case-control studies. Overstated association may be expected from the case-control studies because of recall or selection bias, and early symptoms in patients may have resulted in a change in dietary habits. In our meta-analysis, the significant associations were found both in cohort studies and case-control studies. Second, measurement errors are important in the assessment of dietary intake, which can lead to overestimation of the range of intake and underestimation of the magnitude of the relationship between dietary intake and cancer risk.57, 58 Third, incomparability of results between studies may also occur because definitions and categories of vegetables and fruits, as well as analytical comparisons vary across studies. Studies from different regions, ethnicities and periods probably address very different exposures. However, we only decided to consider the studies that evaluated all types of fruits or vegetables to assess exposure that was as broad as possible. Fourth, between-study heterogeneity was found in some analysis in this meta-analysis, but the between-study heterogeneity was not successfully explained by the subgroup analysis and meta-regression. However, other genetic and environment variables, as well as their possible interaction, non-comparable measurement of nutrients and variation of the covariates and so on, may well be potential contributors to this disease-effect unconformity. In this respect, the lack of relevant study-level covariates in the reported articles precluded a more robust assessment of sources of this heterogeneity.

In summary, results from this meta-analysis suggested that intake of fruits and vegetables may have a protective effect on lung cancer risk, and the associations were stronger in females.

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Wang, M., Qin, S., Zhang, T. et al. The effect of fruit and vegetable intake on the development of lung cancer: a meta-analysis of 32 publications and 20 414 cases. Eur J Clin Nutr 69, 1184–1192 (2015). https://doi.org/10.1038/ejcn.2015.64

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