Annals of Oncology Advance Access originally published online on October 23, 2006
Annals of Oncology 2007 18(2):388-392; doi:10.1093/annonc/mdl387
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© 2006 European Society for Medical Oncology
epidemiology |
Dietary intake of fruit and vegetable and lung cancer risk: a case–control study in Harbin, northeast China
1 Istituto di Ricerche Farmacologiche ‘Mario Negri’, Milano
2 Istituto di Statistica Medica e Biometria, Università degli Studi di Milano, Milano, Italy
3 Evidence and Risk Assessment Division, Centre for Chronic Disease Prevention and Control, Public Health Agency of Canada, Ottawa, Ontario, Canada
4 Department of Epidemiology, Harbin Medical University, Harbin, China
* Correspondence to: Dr C. Galeone, Istituto di Ricerche Farmacologiche "Mario Negri", Via Eritrea 62, 20157 Milan, Italy. Tel: +39-02-39014-577; Fax: +39-02-33200-231; E-mail: galeone{at}marionegri.it
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Abstract |
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Background: We studied the relationship between dietary intake of vegetables and fruit and lung cancer risk in Harbin, Heilongjiang province, northeast China, an area with a very high baseline risk of lung cancer in both sexes.
Patients and methods: We used data from a case–control study, conducted from 1987 to 1990, among 218 cases with incident, histologically confirmed lung cancer and 436 controls admitted to the same hospitals as cases with non-neoplastic, non-lung diseases unrelated to smoking and other potential risk factors for lung cancer.
Results: Compared with the lowest tertile of intake of vegetables, fruit or both, the multivariate odds ratios (ORs) for the highest tertile of intake were 0.39 [95% confidence interval (CI) 0.25–0.62], 0.73 (95% CI 0.48–1.11) and 0.40 (95% CI 0.25–0.63), respectively. In particular, high intake of Chinese cabbage (OR = 0.53), chives (OR = 0 .54), carrots (OR = 0.51) and celery (OR = 0.40) was inversely associated with lung cancer. The OR was more than six-fold elevated for smokers reporting low intake of vegetables, and more than four-fold elevated for smokers reporting low intake of fruit, as compared with never smokers reporting high intake of these items.
Conclusion: In agreement with previous studies, we found an inverse relation between vegetable and fruit intake and lung cancer risk in both strata of current and never smokers.
Key words: allium vegetables, China, diet, fruit intake, lung cancer, vegetable intake
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introduction |
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TopAbstractintroductionmaterials and methodsresultsdiscussionAcknowledgementsReferences |
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During the last 30 years, lung cancer has become one of the leading causes of death in China [1, 2]. The most important risk factor for lung cancer, in China, is smoking [2–5], followed by indoor air pollution [1, 5]. Dietary factors too appear to have a role in the etiology of lung cancer [5–8]. In particular, several epidemiological studies have evaluated the role of vegetables and fruit, providing evidence for their protective role on lung cancer risk [9, 10]. In China, however, only a few studies have been conducted on this issue, mainly in southern and northeastern regions. Forman et al. [11] found that tin miners in Yunnan province, southern China, with low intake of yellow and light-green vegetables had increased odds ratios (ORs) of lung cancer (OR = 2.26 and OR = 2.39 for the lowest quartiles of intake, respectively) after adjusting for smoking habits and occupational exposures to recognized lung carcinogens. Among 428 male lung cancer cases and 1011 controls, also from the Yunnan province, the relative risk of lung cancer across increasing quartiles of consumption of dark-green, leafy vegetables were 1.00, 0.62, 0.52 and 0.41 [12]. A small case–control study among Chinese never-smoking females in Hong Kong found an OR of 2.4 for women in the lowest tertile of consumption of fresh fruit [13].
In the northeast of China, a case–control study in Liaoning province among employees at the Anshan Iron-Steel Complex observed a protective effect of fruit consumption (OR = 0.6 for the highest intake) [14]. Zhou et al. [15] in their study in Shenyang including 290 female cases and 290 controls found a protective role of ß-carotene (OR = 0.84), vitamin C (OR = 0.75) and fiber intake (OR = 0.46). In Heilongjiang province, a case–control study conducted among 227 lung cancer cases and 227 controls during the 1980s suggested that increased vegetable (OR = 0.8) and fruit (OR = 0.7) consumption reduced lung cancer risk, but ß-carotene was unrelated, notably among nonsmokers (OR = 1.2) [16]. As Harbin had the highest death rates from lung cancer for female smokers and nonsmokers at ages 35–69 years in China [1], the few studies of lung cancer conducted in this region have concentrated mostly on women. Wu-Williams et al. [17] found that the intake of carotene-rich vegetables was not related with lung cancer in female smokers nor in nonsmokers [OR = 0.9, 95% confidence interval (CI): 0.7–1.2], while another study among nonsmoking women [18] indicated that a diet poor in vitamins was a risk factor for lung cancer; the OR for high intake (
65 times per year) of carrots was 0.07 (95% CI: 0.02–0.31).
Therefore, the published studies principally involved women or heavily occupationally exposed men with high proportions of current smokers. We report the results of a case–control study conducted in Harbin, the capital of the Heilongjiang province in northeastern China, involving both males and females, where the role of diet could be evaluated together with smoking habits.
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materials and methods |
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The study was conducted from May 1987 to May 1990 in Harbin, Heilongjiang province, northeast China. Harbin, the capital city, has about 9 million inhabitants and is surrounded by smaller cities and an extensive rural area. Both cases and controls had to be resident in Heilongjiang province. Cases were 218 newly diagnosed, histologically confirmed lung cancer patients who were hospitalized in the Department of Cardiothoracic Surgery of the Hospitals in this area. The controls were patients admitted to the Department of General Surgery, Cardiothoracic Surgery, Urological Surgery and Orthopaedic Surgery for non-neoplastic and non-lung diseases at the same hospitals where the cases were recruited. For each case, two controls were individually matched by sex, 5-year age interval and area of residence. For cases residing in the city of Harbin, controls from Harbin were used. For smaller cities, a match in the same or an adjacent city was used. For cases from rural areas or small towns, controls were matched to subjects living in the same or adjacent areas (town or rural). Diagnoses at admission of controls comprised 183 (42.0%) conditions requiring general surgery, 126 (28.9%) urological diseases and 127 (29.1%) orthopedic diseases and trauma. Before surgery, the study subjects were interviewed in the hospital wards by two trained interviewers using a structured questionnaire. Information was collected on socioeconomic status, history of lung diseases, smoking history, diet, past occupations and exposure to selected chemicals, residential history, type of heating and cooking fuels used at home. A smoker was considered as anyone who smoked at least one cigarette per day for 1 year or more, while an ex-smoker was considered a smoker who stopped smoking from at least 1 year. The questionnaire collected information on the annual consumption of fresh vegetables (Chinese cabbage, spinach, green beans, chives, celery, cucumbers, green pepper and carrots) and fruit (apples and pears, oranges and water melon). Information on use (dose and duration) of vitamin supplements was also collected. We calculated a score for total vegetable, fruit and their combined intake by assigning a score from 1 to 3 according with the tertile of intake of each item, and subsequently by summing the corresponding scores.
data analysis
OR for subsequent tertiles of vegetable and fruit intake (defined on the distribution among controls) and the corresponding 95% CIs were computed by means of unconditional logistic regression models. Adjustments were made for sex, age, smoking status (never, current, ex), duration (for current smokers: <25, 25 to <35, 35 years; time since stopping for ex-smokers: <5, 5 year) and amount of smoking (for current smokers: <10, 10 to <15, 15 cigarettes per day; for ex-smokers: <15, 15 cigarettes per day), income (in tertiles), family history of lung and other cancers, residence area (urban or rural) and exposure to coal for house heating or cooking.
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results |
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Table 1 shows the distribution of cases and controls according to sex, income, smoking habit, family history of lung and other cancers and exposure to coal for house heating or cooking. Lung cancer cases had similar income distributions as those of the controls. Current smokers were 62.8% of lung cancer cases and 38.8% of controls, the corresponding OR was 3.40 (95% CI 2.29–5.01), and the risk increased with longer duration (OR = 3.89 for
35 years). Cases reported more frequently than controls a family history of lung and other cancers (OR = 1.51, 95% CI 0.88–2.97), and an exposure to coal for house heating or cooking (OR = 2.15, 95% CI 1.13–4.13).
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Table 2 shows the distribution of cases and controls according to tertiles of intake of selected vegetables with significant associations, total vegetables and fruit and use of vitamin supplements. It also gives the corresponding multivariate ORs of lung cancer according to tertile of intake and the continuous ORs, for an increment of intake equal to 1 standard deviation (SD) among controls, after adjustment for smoking habits and several other potential confounding factors. The ORs for the highest tertile of intake were 0.53 for Chinese cabbage, 0.54 for chives, 0.40 for celery and 0.51 for carrots. For total vegetables, total fruit and their combined intake, the ORs in the highest versus lowest tertile of score were 0.39 (95% CI 0.25–0.62), 0.73 (95% CI 0.48–1.11) and 0.40 (95% CI 0.25–0.63), respectively. The results did not change when we considered the sum of kilograms per years of consumption instead of the scores. We found no significant association with green beans, spinach, cucumbers, green pepper, apples, pears, oranges and water melon. Use of vitamin supplements also was unrelated to lung cancer risk (OR = 1.08, 95% CI 0.75–1.56).
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The combined effect of vegetable and fruit intake and tobacco smoking is shown in Table 3. Compared with never smokers reporting high intake of vegetables, fruit and vegetables and fruit combined, the ORs were more than six-fold, four-fold, and five-fold elevated, for smokers reporting low intake of vegetables, fruit, or both, respectively.
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discussion |
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TopAbstractintroductionmaterials and methodsresultsdiscussionAcknowledgementsReferences |
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In agreement with previous studies [7, 8, 10], we found an inverse relation between vegetable and fruit intake and lung cancer risk. In particular, high intake of Chinese cabbage, chives, carrots and celery was inversely associated with lung cancer, and the risk was reduced by
50% among subjects with high consumption of these vegetables. The protective role of Chinese cabbage is consistent with previous studies [12, 16] and, as for other green leafy vegetables, such as broccoli and other cabbages, may be related to their high content of isothiocyanates, which in animals have strong chemopreventive properties against lung cancer [19, 20]. With reference to Chinese chives, several epidemiological, animal and in vitro studies provided evidence of the anticarcinogenic potential of some bioactive compounds in Allium vegetables, including flavonols and organosulfur compounds [21]. The protective role of carrots and celery may be related to their high content of 
- and ß-carotene. During the past two decades, evidence from ecological and early case–control studies [22] indicated that carotenoids could be the cause of the inverse relation between consumption of various fruits and vegetables and lung cancer risk. Subsequent randomized controlled trials using ß-carotene as a supplement found that the isolated nutrient was either neutral [23, 24] or it increased the risk for lung cancer in smokers [25, 26], for which carotenoid intake and serum ß-carotene concentrations tend to be lower regarding nonsmokers [27]. Therefore, ß-carotene may be considered as an index for the protective role of vegetable and fruit intake, but its intake from supplements does not have a preventive effect from cancer [22]. In our study we found no association with risk for lung cancer among those who used supplementation of vitamins, as also reported in a randomized trial in Linxian, China [23]. Therefore, it is still not clear which specific compound might be responsible for the consistent protective effect of fruit and vegetables. New lines of inquiry have recently emerged in relation to dietary correlates of lung cancer, such as studies of phytochemicals, including phytoestrogens, flavonoids and glucosinoids.
Several studies found that consumption of vegetables and fruit was higher in nonsmokers than in current smokers, and that, in smokers, it was inversely related to smoking intensity [6, 28, 29]. We computed the ORs of lung cancer according to vegetable and fruit intake in strata of smoking habit, but no appreciable or significant heterogeneity emerged. Furthermore, in our population, smoking intensity was not correlated with intake of vegetables and fruit (correlation coefficients were –0.04 and 0.05, respectively).
This study was not population based, and did not record information on histological type of lung cancer. On the other hand, participation in the study was practically complete, cases and controls came from similar catchment areas, and allowance for major identified potential confounding factors did not modify any of the results. Since tobacco smoking is a crucial factor in the etiology of lung cancer, we calculated ORs for subsequent tertiles of vegetable and fruit intake adjusting for different smoking metrics, i.e. smoking duration and intensity as separate variables, pack-years and ‘logcig-years’ [30], but the results remained unchanged.
In conclusion, this study gives further support and quantification of the inverse association between intake of vegetables and fruits and lung cancer risk among both strata of current and never smokers from a Chinese area where baseline risk for lung cancer is high and previous data are scanty.
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Acknowledgements |
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This work was conducted with the contribution of the Italian Association for Cancer Research and the Italian League against Cancer. The authors wish to thank Ivana Garimoldi for her editorial assistance.
Received for publication December 21, 2005. Accepted for publication September 12, 2006.
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References |
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