Skip Navigation


American Journal of Epidemiology Advance Access originally published online on October 29, 2008
American Journal of Epidemiology 2008 168(12):1425-1432; doi:10.1093/aje/kwn282
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
168/12/1425    most recent
kwn282v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (2)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Naganuma, T.
Right arrow Articles by Tsuji, I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Naganuma, T.
Right arrow Articles by Tsuji, I.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

American Journal of Epidemiology © The Author 2008. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

ORIGINAL CONTRIBUTIONS

Coffee Consumption and the Risk of Oral, Pharyngeal, and Esophageal Cancers in Japan

The Miyagi Cohort Study

Toru Naganuma, Shinichi Kuriyama, Masako Kakizaki, Toshimasa Sone, Naoki Nakaya, Kaori Ohmori-Matsuda, Yoshikazu Nishino, Akira Fukao and Ichiro Tsuji

Correspondence to Toru Naganuma, Division of Epidemiology, Department of Public Health and Forensic Medicine, Tohoku University School of Medicine, 2-1 Seiryo-machi Aoba-ku Sendai, 980-8575, Japan (e-mail: a4mb1075-thk{at}umin.ac.jp).

Received for publication February 8, 2008. Accepted for publication August 12, 2008.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
An inverse association between coffee consumption and the risk of oral, pharyngeal, and esophageal cancers has been suggested in case-control studies, but few results from prospective studies are available. Data from the Miyagi Cohort Study in Japan were used to clarify the association between coffee consumption and the risk of these cancers. Information about coffee consumption was obtained from self-administered food frequency questionnaires in 1990. Among 38,679 subjects aged 40–64 years with no previous history of cancer, 157 cases of oral, pharyngeal, and esophageal cancers were identified during 13.6 years of follow-up. Hazard ratios were estimated by the Cox proportional hazards regression model. The risk of oral, pharyngeal, and esophageal cancers was inversely associated with coffee consumption. The multivariate-adjusted hazard ratio of these cancers for ≥1 cups of coffee per day compared with no consumption was 0.51 (95% confidence interval: 0.33, 0.77). This inverse association was consistent regardless of sex and cancer site and was observed both for subjects who did not drink or smoke and for those who currently drank or smoked at baseline. In conclusion, coffee consumption was associated with a lower risk of oral, pharyngeal, and esophageal cancers, even in the group at high risk of these cancers.

carcinoma, squamous cell; coffee; cohort studies; esophageal neoplasms; Japan; mouth neoplasms; pharyngeal neoplasms; risk

Abbreviations: CI, confidence interval


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Although both alcohol and tobacco are strongly established risk factors for oral, pharyngeal, and esophageal cancers, the factors protective against these cancers are not well known; high-level consumption of fresh vegetables and fruit may decrease the risk (1–3). Further evidence for the primary prevention of oral, pharyngeal, and esophageal cancers is needed, since quality of life for patients with these cancers is strongly affected (4), and fatality rates for esophageal cancer are relatively high (1–3).

Coffee is considered to help protect against cancer through the activity of its anticarcinogenic constituents (4–7). Numerous epidemiologic studies, mostly with a case-control design, have investigated the relation between coffee consumption and the risk of oral, pharyngeal, and esophageal cancers (8–21), but the results have been inconsistent. The latest 2 case-control studies in Italy and Switzerland suggested a significant inverse association between coffee consumption and the risk of cancers of the oral cavity, pharynx, and esophagus (18, 19). However, case-control studies are not free from selection bias or recall bias related to the retrospective assessment of coffee consumption and other lifestyle-related factors after a diagnosis of cancer. By contrast, results from prospective cohort studies have been few: one suggested no association (20), and another reported an inverse association for buccal cavity and pharyngeal cancers (21).

We therefore conducted a population-based, prospective cohort study in Japan, where consumption of coffee is relatively high (22) and the incidence of esophageal cancer in men is also high (1, 23). Our aim was to investigate the association between coffee consumption and the risk of oral, pharyngeal, and esophageal cancers.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study cohort
Our study was based on the Miyagi Cohort Study, the design of which has been described in detail elsewhere (24). Briefly, all 51,921 residents (25,279 men and 26,642 women) aged 40–64 years living in 14 municipalities randomly selected from the 62 in Miyagi Prefecture, northeastern Japan, were entered into the study as cohort subjects on April 1, 1990. From June through August 1990, we delivered self-administered questionnaires to them on various health habits. The questionnaires were delivered to, and collected from, the subjects’ residences by members of health-promotion committees appointed by the municipal governments. Usable questionnaires were returned by 47,605 subjects (22,836 men and 24,769 women); the response rate was 91.7%. Because all residents in the study area had been entered as cohort subjects and the rate of response to the questionnaires was very high, we considered our subjects sufficiently representative of the area. The study protocol was approved by the institutional review board of Tohoku University School of Medicine. We considered the return of self-administered questionnaires signed by the subjects to imply their consent to participate in the study.

Dietary assessment
Dietary intake was assessed by a baseline survey that used a self-administered food frequency questionnaire. In this questionnaire, we asked participants to report their frequency of recent consumption of 36 food items and 4 beverages, including coffee. The questionnaire provided 5 categories of response to describe participants’ frequency of coffee consumption: never, occasionally, 1 to 2 cups/day, 3 to 4 cups/day, and 5 or more cups/day. No questions were asked about the type of coffee used, the method of brewing, or the temperature of the beverage. The volume of a typical cup of coffee was 150 mL. The questionnaire also included details of personal and family history of disease, physical status, drinking and smoking habits, and occupational and educational status.

The reproducibility and validity of coffee consumption data among these subjects has been reported previously (25). Spearman's rank correlation coefficient for the correlation between consumption as assessed by the food frequency questionnaire and four 3-day diet records was 0.70, and that between consumption measured by 2 food frequency questionnaires during the 1-year interval was 0.72.

Recording of cancer cases, follow-up
The endpoint of our analysis was the incidence of either oral, pharyngeal, or esophageal cancer defined by topography codes—C00.0–09.9 (lip and oral cavity), C10.0–10.9 and C12.9–14.8 (pharynx), and C15.0–15.9 (esophagus)—in accordance with the International Classification of Diseases for Oncology, Second Edition. We excluded cancer of the nasopharynx (C11.0–11.9) from the pharyngeal cancer classification.

We ascertained the incidence of cancer through computerized record linkage to the Miyagi Prefecture Cancer Registry, one of the oldest and most accurate population-based cancer registries in Japan (26). Between 1993 and 1997, the percentage registered by death certificates only for oral cavity cancer was 7% for men and women; for esophageal cancer, these values were 10% for men and 20% for women (26).

Of the 47,605 subjects who responded to the questionnaire, we excluded 1,146 (441 men and 705 women) who had been given a diagnosis of cancer before the baseline survey was conducted, as ascertained from self-reports and the cancer registry. We also excluded 7,780 subjects (3,537 men and 4,243 women) who had entered incomplete responses about coffee consumption. Consequently, data for 38,679 eligible subjects (18,858 men and 19,821 women), including 157 subjects (135 men and 22 women) with oral, pharyngeal, or esophageal cancer, were entered into the analysis.

For follow-up, we established a follow-up committee that consisted of the Miyagi Cancer Society, the community health divisions of all 14 municipalities, the Department of Health and Welfare of Miyagi Prefectural Government, and the Division of Epidemiology, Tohoku University School of Medicine. The committee periodically reviewed the residential registration records of each municipality. From this review, we identified subjects who had either died or emigrated during the observation period. Follow-up of subjects who had moved from the study municipalities was discontinued because the committee could not review the residential registration records from outside the study area. During the study period, 2,207 subjects (1,051 men and 1,156 women: 5.7% of the total) were lost to follow-up.

Statistical analysis
We counted person-years of follow-up for each of the subjects from June 1, 1990, until the date of diagnosis of oral, pharyngeal, or esophageal cancer; the date of emigration from the study area; the date of death; or the end of the follow-up period (December 31, 2003), whichever occurred first. The mean follow-up period was 12.8 years, and the maximum follow-up period was 13.6 years.

We combined the upper 3 categories of coffee consumption (1 to 2 cups/day, 3 to 4 cups/day, and 5 or more cups/day) into the single category "1 or more cups/day" because of the small number of subjects and cases in each category. We chose the nonintake category (subjects who responded "never" to coffee consumption) as the reference group. We used the Cox proportional hazards regression model to estimate hazard ratios and 95% confidence intervals of oral, pharyngeal, and esophageal cancer incidence according to categories of coffee consumption and to adjust for potentially confounding variables; SAS version 9.1 statistical software (SAS Institute, Inc., Cary, North Carolina) was used. The P values for the analysis of linear trends were calculated by treating the coffee consumption category as a continuous variable. All reported P values were 2-sided and were considered statistically significant if less than 0.05. All analyses were conducted for total subjects and separately by sex. We also performed separate analyses after dividing cases of cancer into oral and pharyngeal (International Classification of Diseases for Oncology, Second Edition codes C00.–09.9, C10.0–10.9, and C12.9–14.8) and esophageal (C15.0–15.9).

We considered the following variables to be potential confounders: age (in years), sex, body mass index (<18.5 kg/m2, 18.5–24.9 kg/m2, ≥25.0 kg/m2), alcohol consumption (never, former drinker, current drinker consuming <45.6 g ethanol/day, current drinker consuming ≥45.6 g ethanol/day), cigarette smoking (never smoked, former smoker, current smoker of <20 cigarettes/day, current smoker of ≥20 cigarettes/day), consumption of vegetables and fruit (<2 times/month, 1–2 times/week, 3–4 times/week, every day), and green tea consumption (<1 cup/day, 1–2 cups/day, 3–4 cups/day, ≥5 cups/day).

We performed additional analyses after we had restricted cases of cancer to histologically confirmed squamous cell carcinoma (defined as morphology codes 8050/0 to 8082/3 according to the International Classification of Diseases for Oncology, Second Edition) of the oral cavity, pharynx, and esophagus and after exclusion of all subjects who had been given a diagnosis of oral, pharyngeal, or esophageal cancer within the first 3 years of follow-up. Analyses were stratified by alcohol consumption status and by cigarette smoking status at baseline.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
During 494,935 person-years of follow-up (238,731 for men and 256,204 for women), we documented 157 cases of oral, pharyngeal, or esophageal cancer (135 men and 22 women). Included were 48 cases of oral or pharyngeal cancer (31 men and 17 women) and 112 cases of esophageal cancer (106 men and 6 women).

The characteristics of the subjects at baseline, as categorized by coffee consumption, are presented in Table 1. Subjects with higher coffee consumption tended to be younger and have a body mass index of 18.5–24.9 kg/m2. Higher coffee consumption was associated with a higher frequency of smoking, lower vegetable consumption, and lower green tea consumption by both men and women. For women, higher coffee consumption was also associated with higher alcohol consumption (data not shown).


View this table:
[in this window]
[in a new window]

  		Table 1. Characteristics of Study Subjects (N = 38,679) According to Coffee Consumption Status, Miyagi, Japan, 1990–2003

 
Table 2 presents the association between coffee consumption and the combined incidence risk of cancers of the oral cavity, pharynx, and esophagus. We found a significant inverse association between coffee consumption and the combined incidence risk of oral, pharyngeal, and esophageal cancers for both men and women. The multivariate-adjusted hazard ratios of oral, pharyngeal, and esophageal cancer incidence for 1 or more cups of coffee per day compared with no consumption were 0.51 (95% confidence interval (CI): 0.33, 0.77; P for trend = 0.002) for all subjects, 0.59 (95% CI: 0.38, 0.91; P for trend = 0.03) for men, and 0.17 (95% CI: 0.04, 0.69; P for trend = 0.01) for women.


View this table:
[in this window]
[in a new window]

  		Table 2. Hazard Ratios and 95% Confidence Intervals of the Incidence of Cancer of the Oral Cavity, Pharynx and Esophagus Combined According to Coffee Consumption, Miyagi, Japan, 1990–2003

 
There were 132 cases of squamous cell carcinoma of the oral cavity, pharynx, or esophagus; this condition therefore accounted for more than 80% of the cancers in the 3 areas. When we restricted our analysis to these 132 cases alone, the result did not differ from that for all cancer cases (Table 2). Since there were only 2 cases of adenocarcinoma of the oral cavity, pharynx, or esophagus among our subjects, we could not investigate the association between coffee consumption and this cancer. We excluded cases of oral, pharyngeal, or esophageal cancer diagnosed during the first 3 years of follow-up to avoid any possible bias resulting from the influence of undiagnosed oral, pharyngeal, or esophageal cancer present at baseline. In this analysis, 18 cases of cancer were excluded; however, the results did not essentially differ (data not shown).

Coffee consumption was also associated with a lower incidence risk of oral/pharyngeal cancer and of esophageal cancer (Table 3). The multivariate-adjusted hazard ratios for 1 or more cups of coffee per day compared with no consumption were 0.35 (95% CI: 0.16, 0.77; P for trend = 0.009) for oral/pharyngeal cancer and 0.60 (95% CI: 0.37, 0.97; P for trend = 0.05) for esophageal cancer. We observed similar trends for men and women separately, but they were not statistically significant (data not shown).


View this table:
[in this window]
[in a new window]

  		Table 3. Hazard Ratios and 95% Confidence Intervals of the Incidence of Cancer of the Oral Cavity/Pharynx and Esophagus According to Coffee Consumption, Miyagi, Japan, 1990–2003

 
The results of our analysis of the association of coffee consumption with the incidence risk of oral, pharyngeal, and esophageal cancers combined and stratified by alcohol consumption and smoking status are shown in Table 4. We observed an inverse association between coffee consumption and the risk of oral, pharyngeal, and esophageal cancers, even in groups at high risk of these cancers. A lower risk of oral, pharyngeal, and esophageal cancers was associated with higher coffee consumption in both the never and the current drinker strata. The multivariate-adjusted hazard ratios for 1 or more cups of coffee per day compared with no consumption were 0.43 (95% CI: 0.13, 1.41; P for trend = 0.17) for nondrinkers and 0.49 (95% CI: 0.31, 0.77; P for trend = 0.004) for current drinkers. Similarly, we found inverse associations between coffee consumption and the incidence of oral, pharyngeal, and esophageal cancers for both the never and the current smoker groups at baseline. The multivariate-adjusted hazard ratios for 1 or more cups of coffee per day compared with no consumption were 0.50 (95% CI: 0.14, 1.81; P for trend = 0.29) for nonsmokers and 0.49 (95% CI: 0.30, 0.79; P for trend = 0.008) for current smokers.


View this table:
[in this window]
[in a new window]

  		Table 4. Hazard Ratios and 95% Confidence Intervals of the Incidence of Cancer of the Oral Cavity, Pharynx, and Esophagus Combined According to Coffee Consumption in Strata of Alcohol Consumption and Cigarette Smoking, Miyagi, Japan, 1990–2003

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In a population-based, prospective cohort of Japanese that included 157 cases of oral, pharyngeal, and esophageal cancers, we observed an inverse association between coffee consumption and the incidence risk of these cancers. This inverse association was consistent regardless of sex and the site of the cancers, and it was observed for both nondrinkers or nonsmokers and current drinkers or smokers at baseline.

Although many studies have assessed the relation between coffee consumption and oral, pharyngeal, or esophageal cancers, their results have been inconsistent. Of 12 case-control studies, 4 supported an inverse association (9, 13, 18, 19), 2 showed an increased risk (especially for hot coffee) (16, 17), and the other 6 suggested no association (8, 10–12, 14, 15). To our knowledge, only 2 prospective studies have investigated this issue. One, conducted in Norway, found no association (20). In that study, among 16,555 subjects during 11.5 years of follow-up, only 53 cases of cancer were ascertained, whereas we documented 157 cases of oral, pharyngeal, or esophageal cancer. The other prospective study reported an inverse association between coffee consumption and the risk of cancer of the buccal cavity and pharynx. Compared with those for the lowest coffee consumption category, the relative risks for the highest category were 0.5 for men and 0.7 for women (21). This result was consistent with that of our study, although the risk of esophageal cancer was not investigated.

Our results may be explained by anticarcinogenic components of coffee (5–7). Specifically, caffeine may suppress the progression of quiescent (G0 phase) cells into the cell cycle by inhibiting cell growth signal-induced activation of cyclin-dependent kinase 4 (7). Cafestol and kahweol have been suggested to inhibit DNA damage induced by some procarcinogens such as 7,12-dimethylbenz[a]anthracene and aflatoxin B1 (6). Cafestol and kahweol are 2 coffee-specific diterpenes present in considerable quantities in coffee beans, as well as in unfiltered beverages, which can be isolated from coffee oil (27).

A pooled analysis of 2 prospective Japanese cohort studies, 1 of which used the same cohort as ours, suggested that green tea consumption is associated with a significantly increased risk of esophageal cancer, and it was suggested that drinking the tea at high temperature might be involved (28). Furthermore, several other studies have suggested that drinking hot beverages is associated with an increased risk of cancers of the pharynx (17) and esophagus (3, 15, 16, 29). However, we observed an inverse association between coffee consumption and the risk of esophageal cancer. Although we did not ask our participants about the temperature at which they drank their coffee, our findings imply that some component or components of coffee have a strongly protective effect against these cancers that offsets the negative effect of drinking hot beverages.

One of the most significant findings of our study was that the inverse association between coffee consumption and the risk of oral, pharyngeal, and esophageal cancers was consistent across the strata of sex and cancer site. Furthermore, the inverse association was also observed in populations with a high risk of these cancers, namely, those who were current drinkers and/or smokers at baseline.

The association of coffee consumption with cancer of the digestive organs, such as the stomach, pancreas, liver, and colorectum, has been investigated. Accumulated evidence now suggests that coffee consumption is associated with a decreased risk of liver cancer (30, 31) but has no association with gastric cancer (32) or pancreatic cancer (33, 34). However, the issue of whether there is no, or an inverse, association between coffee consumption and colorectal cancer is still under discussion (35–38). Some of this evidence is inconsistent with our findings that coffee has a protective effect on oral, pharyngeal, and esophageal cancers. However, these differences could be interpreted in other ways. First, the effect of coffee consumption may be dependent on site-related differences in the histology of the cancer. Most gastric and colorectal cancers are adenocarcinomas, whereas oral, pharyngeal, and esophageal cancers are mainly squamous cell carcinomas. Indeed, more than 80% of the oral, pharyngeal, and esophageal cancers in our study population were squamous cell carcinomas. Second, before reaching the epithelium of the stomach and colorectum, some constituents of coffee may lose their anticarcinogenic effect because of exposure to digestive juices such as gastric or bile acids or pancreatic juice. In contrast, the epithelium of the oral cavity, pharynx, and esophagus is directly exposed to coffee that has not been affected by digestive juice.

Our study had several strengths. To our knowledge, it is the first prospective cohort study to focus on this issue. We used data on subjects from the general Japanese population and identified an adequate number of cases of oral, pharyngeal, and esophageal cancer (157 cases) over a long follow-up period (494,935 person-years). In addition, we carefully considered possible risk factors for oral, pharyngeal, and esophageal cancers as covariates in our estimations of multivariate-adjusted hazard ratios.

Our study also had some limitations. First, we collected information on coffee consumption only once, at baseline. Therefore, measurement error caused by changes in coffee consumption over time among the subjects could have distorted our results. Second, we excluded 7,780 subjects from our analysis because they incompletely answered, or did not answer, the question on coffee consumption. In this excluded group, 59 cases of oral, pharyngeal, or esophageal cancer (52 in men and 7 in women) were diagnosed. The multivariate-adjusted hazard ratio of oral, pharyngeal, or esophageal cancer in the subjects who did not report their coffee consumption (n = 7,780), compared with those who provided a complete report (n = 38,679), was not statistically significant (hazard ratio = 1.32, 95% CI: 0.93, 1.89; P for trend = 0.12). We also found that the baseline characteristics of the subjects who did not answer the question on coffee consumption were not different from those of subjects who did (data not shown). Therefore, our results were not substantially biased by exclusion of the subjects who did not answer the question on coffee consumption. Third, we did not investigate the form in which the coffee was consumed, such as whether it was filtered or boiled, caffeinated or decaffeinated. However, because boiled or decaffeinated coffee is not commonly consumed in Japan, most of the subjects would have drunk instant or filtered, caffeinated coffee (39).

We conclude that coffee consumption is related to a lower risk of oral, pharyngeal, and esophageal cancers in the general population of Japan. Although cessation of alcohol consumption and cigarette smoking is currently the best known way to help reduce the risk of developing these cancers, coffee could be a preventive factor in both low-risk and high-risk populations. Our results have pharmacologic implications for clinical medication of these cancers. Further studies to confirm the role of coffee in preventing these cancers are necessary.


   ACKNOWLEDGMENTS
 
Author affiliations: Division of Epidemiology, Department of Public Health and Forensic Medicine, Tohoku University School of Medicine, Miyagi, Japan (Toru Naganuma, Shinichi Kuriyama, Masako Kakizaki, Toshimasa Sone, Naoki Nakaya, Kaori Ohmori-Matsuda, Ichiro Tsuji); Division of Epidemiology, Miyagi Cancer Center Research Institute, Miyagi, Japan (Yoshikazu Nishino); and Department of Public Health, Yamagata University Graduate School of Medicine, Yamagata, Japan (Akira Fukao).

This work was supported by the Grant-in-Aid for Cancer Research and for the Third-Term Comprehensive Ten-Year Strategy for Cancer Control, Ministry of Health, Labour and Welfare of Japan (H16-3jigan-010).

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Parkin DM, Bray F, Ferlay J, et al. Global cancer statistics, 2002. CA Cancer J Clin (2005) 55(2):74–108.[Abstract/Free Full Text]
  2. La Vecchia C, Tavani A, Franceschi S, et al. Epidemiology and prevention of oral cancer. Oral Oncol (1997) 33(5):302–312.[Web of Science][Medline]
  3. Holmes RS, Vaughan TL. Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol (2007) 17(1):2–9.[CrossRef][Web of Science][Medline]
  4. Rogers SN, Ahad SA, Murphy AP. A structured review and theme analysis of papers published on ‘quality of life’ in head and neck cancer: 2000–2005. Oral Oncol (2007) 43(9):843–868.[CrossRef][Web of Science][Medline]
  5. Daglia M, Papetti A, Gregotti C, et al. In vitro antioxidant and ex vivo protective activities of green and roasted coffee. J Agric Food Chem. (2000) 48(5):1449–1454.[CrossRef][Web of Science][Medline]
  6. Cavin C, Holzhaeuser D, Scharf G, et al. Cafestol and kahweol, two coffee specific diterpenes with anticarcinogenic activity. Food Chem Toxicol (2002) 40(8):1155–1163.[CrossRef][Web of Science][Medline]
  7. Hashimoto T, He Z, Ma WY, et al. Caffeine inhibits cell proliferation by G0/G1 phase arrest in JB6 cells. Cancer Res. (2004) 64(9):3344–3349.[Abstract/Free Full Text]
  8. La Vecchia C, Ferraroni M, Negri E, et al. Coffee consumption and digestive tract cancers. Cancer Res. (1989) 49(4):1049–1051.[Abstract/Free Full Text]
  9. Franceschi S, Barra S, La Vecchia C, et al. Risk factors for cancer of the tongue and the mouth. A case-control study from northern Italy. Cancer (1992) 70(9):2227–2233.[Medline]
  10. Pintos J, Franco EL, Oliveira BV, et al. Maté, coffee, and tea consumption and risk of cancers of the upper aerodigestive tract in southern Brazil. Epidemiology (1994) 5(6):583–590.[Web of Science][Medline]
  11. Bundgaard T, Wildt J, Frydenberg M, et al. Case-control study of squamous cell cancer of the oral cavity in Denmark. Cancer Causes Control (1995) 6(1):57–67.[CrossRef][Web of Science][Medline]
  12. Inoue M, Tajima K, Hirose K, et al. Tea and coffee consumption and the risk of digestive tract cancers: data from a comparative case-referent study in Japan. Cancer Causes Control (1998) 9(2):209–216.[CrossRef][Web of Science][Medline]
  13. Franceschi S, Favero A, Conti E, et al. Food groups, oils and butter, and cancer of the oral cavity and pharynx. Br J Cancer (1999) 80(3-4):614–620.[CrossRef][Web of Science][Medline]
  14. Bosetti C, La Vecchia C, Talamini R, et al. Food groups and risk of squamous cell esophageal cancer in northern Italy. Int J Cancer (2000) 87(2):289–294.[CrossRef][Web of Science][Medline]
  15. Castellsagué X, Muñoz N, De Stefani E, et al. Influence of mate drinking, hot beverages and diet on esophageal cancer risk in South America. Int J Cancer (2000) 88(4):658–664.[CrossRef][Web of Science][Medline]
  16. Sharp L, Chilvers CE, Cheng KK, et al. Risk factors for squamous cell carcinoma of the oesophagus in women: a case-control study. Br J Cancer (2001) 85(11):1667–1670.[CrossRef][Web of Science][Medline]
  17. Escribano Uzcudun A, Rabanal Retolaza I, García Grande A, et al. Pharyngeal cancer prevention: evidence from a case-control study involving 232 consecutive patients. J Laryngol Otol (2002) 116(7):523–531.[Web of Science][Medline]
  18. Tavani A, Bertuzzi M, Talamini R, et al. Coffee and tea intake and risk of oral, pharyngeal and esophageal cancer. Oral Oncol (2003) 39(7):695–700.[CrossRef][Web of Science][Medline]
  19. Rodriguez T, Altieri A, Chatenoud L, et al. Risk factors for oral and pharyngeal cancer in young adults. Oral Oncol (2004) 40(2):207–213.[CrossRef][Web of Science][Medline]
  20. Jacobsen BK, Bjelke E, Kvåle G, et al. Coffee drinking, mortality, and cancer incidence: results from a Norwegian prospective study. J Natl Cancer Inst (1986) 76(5):823–831.[Web of Science][Medline]
  21. Stensvold I, Jacobsen BK. Coffee and cancer: a prospective study of 43,000 Norwegian men and women. Cancer Causes Control (1994) 5(5):401–408.[CrossRef][Web of Science][Medline]
  22. International Coffee Organization. Development Strategy for Coffee (2004) London, United Kingdom: International Coffee Organization.
  23. Marugame T, Kamo K, Katanoda K, et al. Cancer incidence and incidence rates in Japan in 2000: estimates based on data from 11 population-based cancer registries. Jpn J Clin Oncol (2006) 36(10):668–675.[Free Full Text]
  24. Fukao A, Tsubono Y, Komatsu S, et al. A cohort study on the relation of life style, personality and biologic markers to cancer in Miyagi, Japan: study design, response rate and profiles of the cohort subjects. J Epidemiol (1995) 5:153–157.
  25. Shimazu T, Tsubono Y, Kuriyama S, et al. Coffee consumption and risk of primary liver cancer: pooled analysis of two prospective studies in Japan. Int J Cancer (2005) 116(1):150–154.[CrossRef][Web of Science][Medline]
  26. Nishino Y, Tsubono Y, Tsuji I, et al. Japan, Miyagi, prefecture. In: Cancer Incidence in Five Continents—Parkin DM, Whelan SL, Ferlay J, et al, eds. (2002) Vol 8. Lyon, France: IARC. 260–261. 716.
  27. Gross G, Jaccaud E, Huggett AC. Analysis of the content of the diterpenes cafestol and kahweol in coffee brews. Food Chem Toxicol (1997) 35(6):547–554.[CrossRef][Web of Science][Medline]
  28. Ishikawa A, Kuriyama S, Tsubono Y, et al. Smoking, alcohol drinking, green tea consumption and the risk of esophageal cancer in Japanese men. J Epidemiol (2006) 16(5):185–192.[CrossRef][Web of Science][Medline]
  29. Sewram V, De Stefani E, Brennan P, et al. Maté consumption and the risk of squamous cell esophageal cancer in Uruguay. Cancer Epidemiol Biomarkers Prev (2003) 12(6):508–513.[Abstract/Free Full Text]
  30. Larsson SC, Wolk A. Coffee consumption and risk of liver cancer: a meta-analysis. Gastroenterology (2007) 132(5):1740–1745.[Medline]
  31. Bravi F, Bosetti C, Tavani A, et al. Coffee drinking and hepatocellular carcinoma risk: a meta-analysis. Hepatology (2007) 46(2):430–435.[CrossRef][Web of Science][Medline]
  32. Botelho F, Lunet N, Barros H. Coffee and gastric cancer: systematic review and meta-analysis. Cad Saude Publica (2006) 22(5):889–900.[Medline]
  33. Qiu D, Kurosawa M, Lin Y, et al. Overview of the epidemiology of pancreatic cancer focusing on the JACC Study. J Epidemiol (2005) 15(suppl_2):S157–S167.[CrossRef][Web of Science][Medline]
  34. Hart AR, Kennedy H, Harvey I. Pancreatic cancer: a review of the evidence on causation. Clin Gastroenterol Hepatol (2008) 6(3):275–282.[CrossRef][Web of Science][Medline]
  35. Michels KB, Willett WC, Fuchs CS, et al. Coffee, tea, and caffeine consumption and incidence of colon and rectal cancer. J Natl Cancer Inst (2005) 97(4):282–292.[Abstract/Free Full Text]
  36. Larsson SC, Bergkvist L, Giovannucci E, et al. Coffee consumption and incidence of colorectal cancer in two prospective cohort studies of Swedish women and men. Am J Epidemiol (2006) 163(7):638–644.[Abstract/Free Full Text]
  37. Naganuma T, Kuriyama S, Akhter M, et al. Coffee consumption and the risk of colorectal cancer: a prospective cohort study in Japan. Int J Cancer (2007) 120(7):1542–1547.[CrossRef][Web of Science][Medline]
  38. Lee KJ, Inoue M, Otani T, et al. Coffee consumption and risk of colorectal cancer in a population-based prospective cohort of Japanese men and women. Int J Cancer (2007) 121(6):1312–1318.[CrossRef][Web of Science][Medline]
  39. All Japan Coffee Association. A Basic Survey for Monitoring Trends in the Demand for Coffee [in Japanese] (2003) Tokyo, Japan: All Japan Coffee Association.

Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?



This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
168/12/1425    most recent
kwn282v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (2)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Naganuma, T.
Right arrow Articles by Tsuji, I.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Naganuma, T.
Right arrow Articles by Tsuji, I.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?