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Epidemiology
Original research
Coffee consumption and risk of prostate cancer: a systematic review and meta-analysis
  1. Xiaonan Chen,
  2. Yiqiao Zhao,
  3. Zijia Tao,
  4. Kefeng Wang
  1. Department of Urology, Shengjing Hospital of China Medical University, Shenyang, Liaoning, China
  1. Correspondence to Dr Kefeng Wang; wangkefenguro{at}sina.com

Abstract

Objectives To conduct a systematic review with meta-analysis of cohort studies to evaluate the association of coffee consumption with the risk of prostate cancer.

Data sources PubMed, Web of Science and Embase were searched for eligible studies up to September 2020.

Study selection Cohort studies were included.

Data extraction and synthesis Two researchers independently reviewed the studies and extracted the data. Data synthesis was performed via systematic review and meta-analysis of eligible cohort studies. Meta-analysis was performed with the “metan” and “glst” commands in Stata 14.0.

Main outcomes and measures Prostate cancer was the main outcome. It was classified as localised prostate cancer which included localised or non-aggressive cancers; advanced prostate cancer which included advanced or aggressive cancers; or fatal prostate cancer which included fatal/lethal cancers or prostate cancer-specific deaths.

Results Sixteen prospective cohort studies were finally included, with 57 732 cases of prostate cancer and 1 081 586 total cohort members. Higher coffee consumption was significantly associated with a lower risk of prostate cancer. Compared with the lowest category of coffee consumption, the pooled relative risk (RR) was 0.91 (95% CI 0.84 to 0.98), I2= 53.2%) for the highest category of coffee consumption. There was a significant linear trend for the association (p=0.006 for linear trend), with a pooled RR of 0.988 (95% CI 0.981 to 0.995) for each increment of one cup of coffee per day. For localised, advanced and fatal prostate cancer, the pooled RRs were 0.93 (95% CI 0.87 to 0.99), 0.88 (95% CI 0.71 to 1.09) and 0.84 (95% CI 0.66 to 1.08), respectively. No evidence of publication bias was indicated in this meta-analysis.

Conclusions This study suggests that a higher intake of coffee may be associated with a lower risk of prostate cancer.

  • epidemiology
  • prostate disease
  • nutrition

Data availability statement

Data are available upon reasonable request. The data are available upon request from the corresponding author (wangkefenguro@sina.com)

http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/bmjopen-2020-038902

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    Strengths and limitations of this study

    • Risk of selection and recall bias may be minimised due to the inclusion of prospective cohort studies.

    • Large sample size ensures adequate statistical power to detect even a small effect of interest.

    • Uncontrolled/residual confounding may distort the association between coffee consumption and prostate cancer.

    • Misclassification of coffee consumption may occur due to the self-reported nature of the exposure.

    • Significant heterogeneity among study results may come from various sources.

    Introduction

    Prostate cancer is the second most frequently diagnosed cancer and the sixth leading cause of cancer death in men. There were 1 276 000 new cancer cases and 359 000 cancer deaths in 2018.1 It is estimated that nearly three-quarters of prostate cancer cases occur in developed countries.1 Since the 1970s, the incidence of prostate cancer has also increased rapidly in some Asian countries such as China, Singapore and Japan, where the incidence has always been much lower than in some Western countries.1 2 Therefore, primary prevention of prostate cancer is a significant public health problem worldwide.

    Coffee is one of the most popular beverages. Since its popularity continues to increase worldwide, even a small effect on individual health may exert a substantial public health impact. Coffee is known to be a major source of dietary caffeine, cafestol and antioxidants in industrialised nations.3 Its various constituents such as caffeine, caffeic acid and chlorogenic acid can potentially impact the development of cancer through multiple carcinogenesis pathways.4 5 Inverse associations were observed between coffee consumption and the risk of cancer in sites such as the liver, colorectum and breast.6 However, previous studies have reported inconsistent results on the association of coffee consumption with the risk of prostate cancer. Although earlier cohort studies did not detect an association,7–15 more recent studies conducted in major Western countries such as the USA, Sweden and the UK reported that coffee consumption was associated with a lower risk of localised and advanced prostate cancer.16–20 In Japan, a country with increasing popularity of coffee, a cohort study also found a significant inverse association between coffee consumption and the risk of prostate cancer.21

    Previous meta-analyses of cohort studies up to 2015 reported a significant positive association for coffee consumption on total prostate cancer risk, with highly variable results in different subgroups.22 23 Since then, five cohort studies have explored the association but still reported inconsistent results.24–28 It was hypothesised that higher coffee consumption was associated with an increased risk of prostate cancer. Thus, the objective of this updated meta-analysis was to explore and evaluate the association of coffee intake with the risk of prostate cancer in adult men, and to direct the future primary prevention strategy on prostate cancer.

    Methods

    This systematic review was conducted and reported in adherence to the PRISMA and MOOSE guidelines29; the corresponding checklists are shown in online supplemental table 1 and online supplemental file 1. Two researchers (YZ and ZT) independently conducted the literature search, study selection, data extraction and study quality assessment. Any discrepancies were resolved by discussion, but whenever consensus could not be reached between the two reviewers, a third reviewer (KW) acted as arbitrator.

    Patient and public involvement

    This is a meta-analysis based on study-level data and no individual-level data were involved in the study or in defining the research question or outcome measures.

    Inclusion criteria

    The eligibility criteria of the studies were as follows: (1) The study should use a longitudinal cohort design or case–control design nested within a cohort study. (2) The study should present information on coffee consumption as the exposure of interest. Coffee consumption was ascertained by self-reported dietary records or food diaries on the intake levels (highest intake category vs lowest intake category) or frequency measures (eg, per unit/cups/mL per day/week). Since the intake levels were classified and defined differently in each study, the absolute coffee consumption in the highest and lowest intake categories varied across the included studies. (3) The study should report prostate cancer as the outcome of interest. Prostate cancer was defined by clinical diagnosis, physician diagnosis, medical records, self-reports or data linkage to a registry system such as a cancer registry. Based on definitions in each original study, the prostate cancer categories were classified as follows: (a) localised prostate cancer, which included localised or non-aggressive cancers; (b) advanced prostate cancer, which included advanced or aggressive cancers; and (c) fatal prostate cancer, which included fatal/lethal cancers or prostate cancer-specific deaths. (4) The study should provide relative risk (RR), HR, risk ratio, rate ratio or OR estimates with confidence intervals (CIs) or standard errors for the association of coffee consumption with the risk of prostate cancer. If multiple estimates were provided, priority was given to the multivariable-adjusted risk estimates. If more than one study was conducted in the same population, the earlier reports or reports with less applicable information were excluded.

    Literature search

    A literature search was performed using PubMed, Web of Science and Embase up to September 2020 with the following keywords: coffee and prostate and (cancer or carcinoma or neoplasm or tumour). The full search strategy is shown in online supplemental file 2 The reference lists of relevant publications were also manually searched for identification of additional eligible studies. No language limitation was imposed.

    When data or information in the publication were insufficient, we attempted to contact the corresponding authors of the original study to request the relevant data. Then two authors (Russnes and Nilsson) provided us with the relevant information about the person-years of follow-up for specific categories of coffee intake to facilitate the dose-response analyses.15 20 Of note, we finally did not include the study by Russnes et al20 in the current meta-analysis because the study population is the same as another included cohort study by Wilson et al18 which reported more applicable information.

    Data extraction

    We extracted the following information from each eligible study: first author’s name, year of publication, study country, follow-up time, number of participants in the cohort, number of prostate cancer cases, assessment of coffee consumption, primary study outcome, definitions and categories of coffee consumption, RRs and 95% CIs for all prostate cancer outcomes associated with coffee consumption, and the potential confounders considered or adjusted in the analysis.

    Study quality assessment

    The 9-star Newcastle–Ottawa Scale tool was used to assess study quality.30 The quality of each cohort study was judged on three broad categories—namely, selection of the study population, comparability of groups and ascertainment of either the exposure or outcome of interest.

    Statistical analysis

    In the meta-analysis, the RR estimate was used to measure the association between coffee consumption and the risk of prostate cancer in this meta-analysis. We pooled the study-specific RR estimates for the highest versus the lowest category of coffee consumption. A fixed effects model was used to pool the study-specific estimates; whenever significant heterogeneity was detected, the random effect model was used to address the heterogeneity across studies.31 Subgroup analyses were conducted stratified by study location, prostate cancer stage and potential confounder adjustments including a history of prostate-specific antigen (PSA) testing, a family history of prostate cancer, total energy intake, cigarette smoking, alcohol consumption, physical activity, body mass index (BMI) or history of diabetes. Since PSA testing was generally introduced after 1986,32 studies with follow-up periods that ended before 1986 were classified in the PSA-adjusted group. To explore the influence of each study on the pooled results, sensitivity analyses were also performed by excluding one study at a time and then repeating the meta-analysed approach.

    We further examined the potential dose–response relationship between coffee consumption and the risk of prostate cancer. When the mean coffee intakes in each category were not reported, the midpoint values in each category were used instead; when the upper boundary of the highest intake category was not presented, we calculated the midpoint value assuming that the highest category had the same magnitude of intake as the preceding category.33 34 The pooled RR for each increment of one cup of coffee per day was estimated using the method proposed by Orsini and Greenland.35 We examined a potential non-linear relation between coffee consumption and prostate cancer risk by modelling coffee consumption using restricted cubic splines for non-linear trends with 4 knots at fixed percentiles (5%, 35%, 65% and 95%) of the distribution.36 Non-linearity of the association was explored by testing the null hypothesis that the coefficients of the second and third splines were equal to zero.

    We assessed the heterogeneity by using the Q and the I2 statistic. A p value <0.10 or an I2 >50% suggest that statistical heterogeneity may exist.37 Small study effects such as publication bias were evaluated by funnel plots, as well as Begg’s test and Egger’s test.38 39 Meta-analysis was conducted using the “metan” and “glst” commands in Stata version 14.0 (StataCorp, College Station, Texas, USA). Two-sided p values <0.05 were considered statistically significant in the meta-analysis.

    Results

    Literature search

    We identified 497 records after searching the three databases. After 217 duplicate records were removed, 280 records remained for screening of titles and abstracts, and after screening the titles and abstracts, 254 irrelevant records were excluded. Following a further full-text review of the 26 remaining studies, 10 studies were excluded because of no useful risk estimates or 95% CIs; two studies were excluded as newer data or more informative data were available. Fourteen studies were obtained from full-text screening and a further two studies were identified by checking the reference lists of retrieved articles.9 11 Thus, 16 studies were included in the final analysis,9–11 13–19 21 24–28 of which 15 reported on the risk of prostate cancer associated with the highest versus the lowest coffee consumption9–11 13–19 21 24–27; 13 studies reported the risk associated with an increase of one cup of coffee per day or provided sufficient data to estimate the dose–response risk9 13–19 21 24 25 27 28 (figure 1).

    Figure 1
    Figure 1

    Flow diagram of study selection in the meta-analysis.

    Study characteristics and quality assessment

    The characteristics of the eligible cohort studies are shown in online supplemental file 3. The included studies were conducted in North America (n=7), Europe (n=7) and Japan (n=2). There was a total of 1 081 586 men in the 16 cohort studies, of whom 57 732 developed prostate cancer. To measure coffee consumption, 11 studies used food-frequency questionnaires and five used a self-administered dietary questionnaire. Most studies considered or adjusted for the most potential confounders in the analysis, such as age at baseline, family history of prostate cancer, race, cigarette smoking, alcohol drinking, total energy intake, BMI and physical activity. The results of study quality assessment are presented in online supplemental file 4. The total scores for each cohort study ranged from 6 to 9. Fourteen studies awarded a total score of ≥7, which were considered as relatively high-quality studies with a low risk of bias.

    Overall analyses and dose–response analyses

    The reported RRs for the original cohort studies ranged from 0.47 (95% CI 0.25 to 0.87) in the study by Pounis et al to 1.42 (95% CI 0.77 to 2.61) in the study by Ellison et al (figure 2). Compared with the lowest coffee intake category, there was a 9% reduction in the risk of prostate cancer for the highest category (RR=0.91; 95% CI 0.84 to 0.98). Statistically significant heterogeneity was detected across the studies (p=0.008, I2=53.2%). In dose–response analyses, we found evidence of a linear inverse association between coffee consumption and prostate cancer risk (p=0.006 for linear trend) (figure 3). The pooled RR of prostate cancer was 0.988 (95% CI 0.981 to 0.995) for an increase of one cup of coffee per day. No evidence of a non-linear relationship was observed between coffee consumption and risk of prostate cancer (p=0.193 for non-linearity). Moreover, there was no indication of small study effects such as publication bias from the results of the Egger’s test (p=0.409), Begg’s test (p=0.843) as well as the funnel plot. The funnel plot and Egger’s publication bias plot are shown in online supplemental file 5.

    Figure 2
    Figure 2

    Forest plot for the association between coffee consumption and prostate cancer risk.

    Figure 3
    Figure 3

    Dose–response relationship of coffee consumption with prostate cancer risk.

    Subgroup and sensitivity analyses

    As shown in table 1, compared with the lowest coffee intake category there was a 7% reduction in risk for the highest intake category (RR=0.93; 95% CI 0.87 to 0.99) for localised prostate cancer. For advanced and fatal prostate cancer, the corresponding pooled RRs were 0.88 (95% CI 0.71 to 1.09) and 0.84 (95% CI 0.66 to 1.08) (figure 4). When stratified by study location, the pooled RRs were 0.96 (95% CI 0.90 to 1.03), 0.85 (95% CI 0.74 to 0.98) and 0.85 (95% CI 0.48 to 1.51) for studies conducted in North America (six in the USA and one in Canada), European countries and Japan. Furthermore, significant inverse associations were observed in all of the confounder adjusted subgroups.

    Figure 4
    Figure 4

    Forest plot for the association between coffee consumption and risk of prostate cancer stratified by cancer stages.

    View this table:
    Table 1

    Summary risk estimates and corresponding 95% CIs for prostate cancer associated with the highest versus the lowest coffee consumption

    In sensitivity analyses, we sequentially excluded one study at a time and recalculated the pooled RRs of the remaining studies. The pooled RRs did not change substantially, ranging from 0.89 (95% CI 0.82 to 0.97) to 0.93 (95% CI 0.86 to 1.00) after omission of the studies by Hashibe et al and Terdal et al, respectively.

    Discussion

    Summary of the findings

    In this meta-analysis, higher coffee consumption was significantly associated with a reduced risk of prostate cancer in men. In the dose–response analysis, a reduction in the risk of prostate cancer of nearly 1% was observed for each increment of one cup of coffee per day. The combined estimate for prostate cancer was robust across subgroup and sensitivity analyses.

    Comparison with other studies

    The previous meta-analysis detected a statistically significant positive association between coffee consumption and prostate cancer risk (RR=1.16; 95% CI 1.01 to 1.33).22 However, this observed effect was confined to case–control studies (RR=1.21; 95% CI 1.03 to 1.43), with no significant association in cohort studies (RR=1.06; 95% CI 0.83 to 1.35) when stratified by study design.22 Considering the case–control design, patients with prostate cancer might differentially recall their past coffee consumption habits compared with healthy controls, which might generally lead to biased estimates. This potential recall bias could generate a spurious positive association between coffee consumption and prostate cancer risk. Additionally, selection bias, which can occur in case–control studies, may distort the association between coffee consumption and prostate cancer risk. In another meta-analysis of cohort studies with 539 577 participants and 34 105 prostate cancer cases, the pooled RR for the highest category of coffee intake was 0.90 (95% CI 0.85 to 0.95) for total prostate cancer compared with the lowest intake category. In this updated meta-analysis of 1 081 586 cohort members and 57 732 incident cases, the overall result was similar to the previous one. However, for subgroups of localised, advanced and fatal prostate cancers, the strength of associations tended to be weaker compared with the previous study.

    Possible biological mechanisms

    It is biologically plausible that coffee may reduce the risk of prostate cancer in men. Coffee improves glucose metabolism, decreases concentrations of plasma insulin and insulin-like growth factor-1, has anti-inflammatory and antioxidant effects, and affects sex hormone levels, all of which may play roles in the initiation, development and progression of prostate cancer.3 18 20 40 Coffee is also a major source of chlorogenic acids; intake of quinides, the degradation products of chlorogenic acids, has been observed to increase insulin sensitivity and lower blood glucose levels.3 Moreover, coffee intake may be associated with increased levels of adiponectin plasma,41 42 which may act as an endogenous insulin sensitiser.43 Higher adiponectin levels in plasma are supposed to relate to lower concentrations of plasma insulin.43 In two prospective studies, insulin levels were observed to be directly associated with prostate cancer-specific mortality.44 45

    Coffee is a major contributor of dietary antioxidants such as caffeic acid and chlorogenic acid.20 A prospective cohort study from the USA found that dietary antioxidants from coffee (eg, caffeic acid) were inversely associated with the risk of total, advanced and lethal prostate cancer.20 It was suggested that antioxidants protect cells from damage caused by oxidative stress and inflammation, which may further lead to neoplastic transformation in the prostate.46 Additionally, dietary antioxidants may inhibit prostate cancer progression through suppression of oxidative stress, which might play a critical role during the progression of prostate cancer.46 Coffee intake was indicated to be related to increased levels in sex hormone-binding globulin (SHBG), as well as total testosterone.47 48 A pooled analysis of 18 prospective studies found that SHBG levels may be inversely associated with the risk of prostate cancer.40 Of note, a nested case–control study found that caffeine or caffeinated coffee intakes were suggested to be associated with an increased level of plasma SHBG. However, such an association was not observed between decaffeinated coffee and plasma SHBG levels. Thus, it was suggested that caffeine may be the key component in coffee, which may be responsible for determining plasma SHBG levels.48

    Strengths and limitations

    A strength of this study was the inclusion of prospective cohort studies. Cohort studies could minimise the risk of selection and recall bias, which is a major concern for case–control design. Besides, large numbers of total cohort members and prostate cancer cases ensure adequate statistical power to detect even a small effect of interest. Furthermore, the dose–response analysis may further lend confidence to the study hypothesis that increased coffee consumption was linearly associated with a lower risk of prostate cancer. Besides, most of the studies were of high quality with a low risk of bias, which could further lend confidence to the current pooled results.

    This meta-analysis also has several limitations. First, one weakness is that only three databases were searched for eligible studies and other databases, especially non-English databases, were not considered in the literature search. Second, because of the observational design, unmeasured or uncontrolled confounders in the original studies may bias the pooled risk estimate; however, the residual confounding effects from the original studies were difficult to handle in a meta-analysis approach.49 50 For example, the inverse association between coffee consumption and prostate cancer could be attributed to risk factors related to coffee consumption, such as physical activity and healthy diet. However, most of the original studies have considered or adjusted for these major potential confounders in the analysis. In the sensitivity analysis of restricting the meta-analysis in studies considering most confounders, the strength of association tended to be larger in comparison with the overall association. Third, misclassification of coffee consumption may occur because of the self-reported nature of exposure measurement. However, validation studies by diet records indicated a relatively high validity of coffee consumption measured by food frequency questionnaire. The correlations between questionnaire and diet records were 0.80 in US men,16 0.71 in Swedish men17 and 0.72 in Japanese men.21 Of note, misclassification of exposure would most likely be non-differential in cohort studies and bias the observed association toward the null.49 50 Therefore, the true association between coffee consumption and risk of prostate cancer may be even stronger. Fourth, since coffee intake and the incidence of prostate cancer in the USA and Europe are relatively high, most of the studies were conducted in these regions. Since the effect size is small, we should be cautious when generalising the results to other areas, especially where the incidence is relatively low. Last, significant between-study heterogeneity may limit interpretation of the results. The observed heterogeneity may come from various sources. For example, the highest and lowest categories of coffee intake are different in the original studies. Studies with a broader range between the highest and lowest categories were assumed to generate a higher risk estimate. Moreover, the type of coffee and different brewing methods included in the coffee consumption groups differed. The different cohort sizes and follow-up periods may also lead to heterogeneous results. Taken together, due to the significant heterogeneity in the current meta-analysis, the pooled results should be interpreted with caution.

    Conclusions

    This study suggests that increased coffee consumption may be associated with a reduced risk of prostate cancer. Further research is still warranted to explore the underlying mechanisms and active compounds in coffee. If the association is further proved to be a causal effect, men might be encouraged to increase their coffee consumption to potentially decrease the risk of prostate cancer.

    Data availability statement

    Data are available upon reasonable request. The data are available upon request from the corresponding author (wangkefenguro@sina.com)

    Ethics statements

    Patient consent for publication

    Acknowledgments

    We would like to thank the authors of the original studies for their contribution to our meta-analysis, especially those authors who provided their raw data for the analysis.

    References

    1. ↵
      1. Bray F,
      2. Ferlay J,
      3. Soerjomataram I, et al
      . Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394–424.doi:10.3322/caac.21492pmid:http://www.ncbi.nlm.nih.gov/pubmed/30207593
      OpenUrlCrossRefPubMed
    2. ↵
      1. Cullen J,
      2. Elsamanoudi S,
      3. Brassell SA, et al
      . The burden of prostate cancer in Asian nations. J Carcinog 2012;11:7. doi:10.4103/1477-3163.94025pmid:http://www.ncbi.nlm.nih.gov/pubmed/22529743
      OpenUrlCrossRefPubMed
    3. ↵
      1. Tunnicliffe JM,
      2. Shearer J
      . Coffee, glucose homeostasis, and insulin resistance: physiological mechanisms and mediators. Appl Physiol Nutr Metab 2008;33:1290–300.doi:10.1139/H08-123pmid:http://www.ncbi.nlm.nih.gov/pubmed/19088791
      OpenUrlCrossRefPubMedWeb of Science
    4. ↵
      1. Lee WJ,
      2. Zhu BT
      . Inhibition of DNA methylation by caffeic acid and chlorogenic acid, two common catechol-containing coffee polyphenols. Carcinogenesis 2006;27:269–77.doi:10.1093/carcin/bgi206pmid:http://www.ncbi.nlm.nih.gov/pubmed/16081510
      OpenUrlCrossRefPubMedWeb of Science
    5. ↵
      1. Bode AM,
      2. Dong Z
      . The enigmatic effects of caffeine in cell cycle and cancer. Cancer Lett 2007;247:26–39.doi:10.1016/j.canlet.2006.03.032pmid:http://www.ncbi.nlm.nih.gov/pubmed/16709440
      OpenUrlCrossRefPubMedWeb of Science
    6. ↵
      1. Yu X,
      2. Bao Z,
      3. Zou J, et al
      . Coffee consumption and risk of cancers: a meta-analysis of cohort studies. BMC Cancer 2011;11:96. doi:10.1186/1471-2407-11-96pmid:http://www.ncbi.nlm.nih.gov/pubmed/21406107
      OpenUrlCrossRefPubMed
    7. ↵
      1. Jacobsen BK,
      2. Bjelke E,
      3. Kvåle G, et al
      . Coffee drinking, mortality, and cancer incidence: results from a Norwegian prospective study. J Natl Cancer Inst 1986;76:823–31.pmid:http://www.ncbi.nlm.nih.gov/pubmed/3457969
      OpenUrlPubMedWeb of Science
    8. ↵
      1. Nomura A,
      2. Heilbrun LK,
      3. Stemmermann GN
      . Prospective study of coffee consumption and the risk of cancer. J Natl Cancer Inst 1986;76:587–90.doi:10.1093/jnci/76.4.587pmid:http://www.ncbi.nlm.nih.gov/pubmed/3457196
      OpenUrlPubMedWeb of Science
    9. ↵
      1. Severson RK,
      2. Nomura AM,
      3. Grove JS, et al
      . A prospective study of demographics, diet, and prostate cancer among men of Japanese ancestry in Hawaii. Cancer Res 1989;49:1857–60.pmid:http://www.ncbi.nlm.nih.gov/pubmed/2924323
      OpenUrlAbstract/FREE Full Text
    10. ↵
      1. Hsing AW,
      2. McLaughlin JK,
      3. Schuman LM, et al
      . Diet, tobacco use, and fatal prostate cancer: results from the Lutheran brotherhood cohort study. Cancer Res 1990;50:6836–40.pmid:http://www.ncbi.nlm.nih.gov/pubmed/2208150
      OpenUrlAbstract/FREE Full Text
    11. ↵
      1. Le Marchand L,
      2. Kolonel LN,
      3. Wilkens LR, et al
      . Animal fat consumption and prostate cancer: a prospective study in Hawaii. Epidemiology 1994;5:276–82.doi:10.1097/00001648-199405000-00004pmid:http://www.ncbi.nlm.nih.gov/pubmed/8038241
      OpenUrlCrossRefPubMedWeb of Science
    12. ↵
      1. Stensvold I,
      2. Jacobsen BK
      . Coffee and cancer: a prospective study of 43,000 Norwegian men and women. Cancer Causes Control 1994;5:401–8.doi:10.1007/BF01694753pmid:http://www.ncbi.nlm.nih.gov/pubmed/7999961
      OpenUrlCrossRefPubMedWeb of Science
    13. ↵
      1. Ellison LF
      . Tea and other beverage consumption and prostate cancer risk: a Canadian retrospective cohort study. Eur J Cancer Prev 2000;9:125–30.doi:10.1097/00008469-200004000-00009pmid:http://www.ncbi.nlm.nih.gov/pubmed/10830580
      OpenUrlCrossRefPubMedWeb of Science
    14. ↵
      1. Iso H,
      2. Kubota Y, Japan Collaborative Cohort Study for Evaluation of Cancer
      . Nutrition and disease in the Japan Collaborative Cohort Study for Evaluation of Cancer (JACC). Asian Pac J Cancer Prev 2007;8:35–80.
      OpenUrlPubMedWeb of Science
    15. ↵
      1. Nilsson LM,
      2. Johansson I,
      3. Lenner P, et al
      . Consumption of filtered and boiled coffee and the risk of incident cancer: a prospective cohort study. Cancer Causes Control 2010;21:1533–44.doi:10.1007/s10552-010-9582-xpmid:http://www.ncbi.nlm.nih.gov/pubmed/20512657
      OpenUrlCrossRefPubMedWeb of Science
    16. ↵
      1. Bosire C,
      2. Stampfer MJ,
      3. Subar AF, et al
      . Coffee consumption and the risk of overall and fatal prostate cancer in the NIH-AARP Diet and Health study. Cancer Causes Control 2013;24:1527–34.doi:10.1007/s10552-013-0229-6pmid:http://www.ncbi.nlm.nih.gov/pubmed/23681472
      OpenUrlCrossRefPubMedWeb of Science
    17. ↵
      1. Discacciati A,
      2. Orsini N,
      3. Andersson S-O, et al
      . Coffee consumption and risk of localized, advanced and fatal prostate cancer: a population-based prospective study. Ann Oncol 2013;24:1912–8.doi:10.1093/annonc/mdt105pmid:http://www.ncbi.nlm.nih.gov/pubmed/23508823
      OpenUrlCrossRefPubMedWeb of Science
    18. ↵
      1. Wilson KM,
      2. Kasperzyk JL,
      3. Rider JR, et al
      . Coffee consumption and prostate cancer risk and progression in the Health Professionals Follow-up Study. J Natl Cancer Inst 2011;103:876–84.doi:10.1093/jnci/djr151pmid:http://www.ncbi.nlm.nih.gov/pubmed/21586702
      OpenUrlCrossRefPubMedWeb of Science
    19. ↵
      1. Shafique K,
      2. McLoone P,
      3. Qureshi K, et al
      . Coffee consumption and prostate cancer risk: further evidence for inverse relationship. Nutr J 2012;11:42. doi:10.1186/1475-2891-11-42pmid:http://www.ncbi.nlm.nih.gov/pubmed/22695052
      OpenUrlCrossRefPubMed
    20. ↵
      1. Russnes KM,
      2. Wilson KM,
      3. Epstein MM, et al
      . Total antioxidant intake in relation to prostate cancer incidence in the Health Professionals Follow-up Study. Int J Cancer 2014;134:1156–65.doi:10.1002/ijc.28438pmid:http://www.ncbi.nlm.nih.gov/pubmed/23959920
      OpenUrlPubMed
    21. ↵
      1. Li Q,
      2. Kakizaki M,
      3. Sugawara Y, et al
      . Coffee consumption and the risk of prostate cancer: the Ohsaki cohort study. Br J Cancer 2013;108:2381–9.doi:10.1038/bjc.2013.238pmid:http://www.ncbi.nlm.nih.gov/pubmed/23674088
      OpenUrlCrossRefPubMedWeb of Science
    22. ↵
      1. Park C-H,
      2. Myung S-K,
      3. Kim T-Y, et al
      . Coffee consumption and risk of prostate cancer: a meta-analysis of epidemiological studies. BJU Int 2010;106:762–9.doi:10.1111/j.1464-410X.2010.09493.xpmid:http://www.ncbi.nlm.nih.gov/pubmed/20590551
      OpenUrlCrossRefPubMedWeb of Science
    23. ↵
      1. Liu H,
      2. Hu G-H,
      3. Wang X-C, et al
      . Coffee consumption and prostate cancer risk: a meta-analysis of cohort studies. Nutr Cancer 2015;67:392–400.doi:10.1080/01635581.2015.1004727pmid:http://www.ncbi.nlm.nih.gov/pubmed/25706900
      OpenUrlPubMed
    24. ↵
      1. Tverdal A
      . Boiled coffee consumption and the risk of prostate cancer: follow-up of 224,234 Norwegian men 20–69 years. Br J Cancer 2015;112:576–9.doi:10.1038/bjc.2014.645pmid:http://www.ncbi.nlm.nih.gov/pubmed/25535729
      OpenUrlPubMed
    25. ↵
      1. Hashibe M,
      2. Galeone C,
      3. Buys SS, et al
      . Coffee, tea, caffeine intake, and the risk of cancer in the PLCO cohort. Br J Cancer 2015;113:809–16.doi:10.1038/bjc.2015.276pmid:http://www.ncbi.nlm.nih.gov/pubmed/26291054
      OpenUrlPubMed
    26. ↵
      1. Pounis G,
      2. Tabolacci C,
      3. Costanzo S, et al
      . Reduction by coffee consumption of prostate cancer risk: evidence from the Moli-sani cohort and cellular models. Int J Cancer 2017;141:72–82.doi:10.1002/ijc.30720pmid:http://www.ncbi.nlm.nih.gov/pubmed/28436066
      OpenUrlPubMed
    27. ↵
      1. Sen A,
      2. Papadimitriou N,
      3. Lagiou P, et al
      . Coffee and tea consumption and risk of prostate cancer in the European Prospective Investigation into Cancer and Nutrition. Int J Cancer 2019;144:240–50.doi:10.1002/ijc.31634pmid:http://www.ncbi.nlm.nih.gov/pubmed/29943826
      OpenUrlPubMed
    28. ↵
      1. Ong J-S,
      2. Law MH,
      3. An J, et al
      . Association between coffee consumption and overall risk of being diagnosed with or dying from cancer among >300 000 UK Biobank participants in a large-scale Mendelian randomization study. Int J Epidemiol 2019;48:1447–56.doi:10.1093/ije/dyz144pmid:http://www.ncbi.nlm.nih.gov/pubmed/31412118
      OpenUrlPubMed
    29. ↵
      1. Moher D,
      2. Liberati A,
      3. Tetzlaff J, et al
      . Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097. doi:10.1371/journal.pmed.1000097pmid:http://www.ncbi.nlm.nih.gov/pubmed/19621072
      OpenUrlCrossRefPubMed
    30. ↵
      1. Wells GA,
      2. Shea B,
      3. O'Connell D
      . The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
    31. ↵
      1. DerSimonian R,
      2. Laird N
      . Meta-analysis in clinical trials. Control Clin Trials 1986;7:177–88.doi:10.1016/0197-2456(86)90046-2pmid:http://www.ncbi.nlm.nih.gov/pubmed/3802833
      OpenUrlCrossRefPubMedWeb of Science
    32. ↵
      1. Welch HG,
      2. Albertsen PC
      . Prostate cancer diagnosis and treatment after the introduction of prostate-specific antigen screening: 1986-2005. J Natl Cancer Inst 2009;101:1325–9.doi:10.1093/jnci/djp278pmid:http://www.ncbi.nlm.nih.gov/pubmed/19720969
      OpenUrlCrossRefPubMedWeb of Science
    33. ↵
      1. Crippa A,
      2. Discacciati A,
      3. Larsson SC, et al
      . Coffee consumption and mortality from all causes, cardiovascular disease, and cancer: a dose-response meta-analysis. Am J Epidemiol 2014;180:763–75.doi:10.1093/aje/kwu194pmid:http://www.ncbi.nlm.nih.gov/pubmed/25156996
      OpenUrlCrossRefPubMedWeb of Science
    34. ↵
      1. Kennedy OJ,
      2. Roderick P,
      3. Buchanan R, et al
      . Coffee, including caffeinated and decaffeinated coffee, and the risk of hepatocellular carcinoma: a systematic review and dose-response meta-analysis. BMJ Open 2017;7:e013739. doi:10.1136/bmjopen-2016-013739pmid:http://www.ncbi.nlm.nih.gov/pubmed/28490552
      OpenUrlAbstract/FREE Full Text
    35. ↵
      1. Greenland S,
      2. Longnecker MP
      . Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 1992;135:1301–9.doi:10.1093/oxfordjournals.aje.a116237pmid:http://www.ncbi.nlm.nih.gov/pubmed/1626547
      OpenUrlCrossRefPubMedWeb of Science
    36. ↵
      1. Orsini N,
      2. Li R,
      3. Wolk A, et al
      . Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 2012;175:66–73.doi:10.1093/aje/kwr265pmid:http://www.ncbi.nlm.nih.gov/pubmed/22135359
      OpenUrlCrossRefPubMedWeb of Science
    37. ↵
      1. Higgins JPT,
      2. Thompson SG
      . Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539–58.doi:10.1002/sim.1186pmid:http://www.ncbi.nlm.nih.gov/pubmed/12111919
      OpenUrlCrossRefPubMedWeb of Science
    38. ↵
      1. Begg CB,
      2. Mazumdar M
      . Operating characteristics of a RANK correlation test for publication bias. Biometrics 1994;50:1088–101.doi:10.2307/2533446pmid:http://www.ncbi.nlm.nih.gov/pubmed/7786990
      OpenUrlCrossRefPubMedWeb of Science
    39. ↵
      1. Egger M,
      2. Davey Smith G,
      3. Schneider M, et al
      . Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629–34.doi:10.1136/bmj.315.7109.629pmid:http://www.ncbi.nlm.nih.gov/pubmed/9310563
      OpenUrlAbstract/FREE Full Text
    40. ↵
      1. Endogenous Hormones and Prostate Cancer Collaborative Group,
      2. Roddam AW,
      3. Allen NE, et al
      . Endogenous sex hormones and prostate cancer: a collaborative analysis of 18 prospective studies. J Natl Cancer Inst 2008;100:170–83.doi:10.1093/jnci/djm323pmid:http://www.ncbi.nlm.nih.gov/pubmed/18230794
      OpenUrlCrossRefPubMedWeb of Science
    41. ↵
      1. Williams CJ,
      2. Fargnoli JL,
      3. Hwang JJ, et al
      . Coffee consumption is associated with higher plasma adiponectin concentrations in women with or without type 2 diabetes: a prospective cohort study. Diabetes Care 2008;31:504–7.doi:10.2337/dc07-1952pmid:http://www.ncbi.nlm.nih.gov/pubmed/18070989
      OpenUrlAbstract/FREE Full Text
    42. ↵
      1. Imatoh T,
      2. Tanihara S,
      3. Miyazaki M, et al
      . Coffee consumption but not green tea consumption is associated with adiponectin levels in Japanese males. Eur J Nutr 2011;50:279–84.doi:10.1007/s00394-010-0136-5pmid:http://www.ncbi.nlm.nih.gov/pubmed/20953616
      OpenUrlCrossRefPubMed
    43. ↵
      1. Ziemke F,
      2. Mantzoros CS
      . Adiponectin in insulin resistance: lessons from translational research. Am J Clin Nutr 2010;91:258S–61.doi:10.3945/ajcn.2009.28449Cpmid:http://www.ncbi.nlm.nih.gov/pubmed/19906806
      OpenUrlAbstract/FREE Full Text
    44. ↵
      1. Ma J,
      2. Li H,
      3. Giovannucci E, et al
      . Prediagnostic body-mass index, plasma C-peptide concentration, and prostate cancer-specific mortality in men with prostate cancer: a long-term survival analysis. Lancet Oncol 2008;9:1039–47.doi:10.1016/S1470-2045(08)70235-3pmid:http://www.ncbi.nlm.nih.gov/pubmed/18835745
      OpenUrlCrossRefPubMedWeb of Science
    45. ↵
      1. Hammarsten J,
      2. Högstedt B
      . Hyperinsulinaemia: a prospective risk factor for lethal clinical prostate cancer. Eur J Cancer 2005;41:2887–95.doi:10.1016/j.ejca.2005.09.003pmid:http://www.ncbi.nlm.nih.gov/pubmed/16243513
      OpenUrlCrossRefPubMedWeb of Science
    46. ↵
      1. Thapa D,
      2. Ghosh R
      . Antioxidants for prostate cancer chemoprevention: challenges and opportunities. Biochem Pharmacol 2012;83:1319–30.doi:10.1016/j.bcp.2011.12.027pmid:http://www.ncbi.nlm.nih.gov/pubmed/22248733
      OpenUrlCrossRefPubMed
    47. ↵
      1. Svartberg J,
      2. Midtby M,
      3. Bønaa KH, et al
      . The associations of age, lifestyle factors and chronic disease with testosterone in men: the Tromsø study. Eur J Endocrinol 2003;149:145–52.doi:10.1530/eje.0.1490145pmid:http://www.ncbi.nlm.nih.gov/pubmed/12887292
      OpenUrlAbstract
    48. ↵
      1. Goto A,
      2. Song Y,
      3. Chen BH, et al
      . Coffee and caffeine consumption in relation to sex hormone-binding globulin and risk of type 2 diabetes in postmenopausal women. Diabetes 2011;60:269–75.doi:10.2337/db10-1193pmid:http://www.ncbi.nlm.nih.gov/pubmed/21030499
      OpenUrlAbstract/FREE Full Text
    49. ↵
      1. Qi X-X,
      2. Shen P
      . Associations of dietary protein intake with all-cause, cardiovascular disease, and cancer mortality: a systematic review and meta-analysis of cohort studies. Nutr Metab Cardiovasc Dis 2020;30:1094–105.doi:10.1016/j.numecd.2020.03.008pmid:http://www.ncbi.nlm.nih.gov/pubmed/32451273
      OpenUrlPubMed
    50. ↵
      1. Yang Y,
      2. Zhao L-G,
      3. Wu Q-J, et al
      . Association between dietary fiber and lower risk of all-cause mortality: a meta-analysis of cohort studies. Am J Epidemiol 2015;181:83–91.doi:10.1093/aje/kwu257pmid:http://www.ncbi.nlm.nih.gov/pubmed/25552267
      OpenUrlCrossRefPubMed

    Supplementary materials

    Footnotes

    • Correction notice This article has been corrected since it first published. The provenance and peer review statement has been included.

    • Contributors KW obtained the funding, developed the research design, interpreted the results and also had primary responsibility for the final content. XC, YZ and ZT analysed the data and interpreted the results. XC and KW drafted manuscript. All authors critically reviewed and approved the manuscript.

    • Funding This work was supported by the Natural Science Foundation of Liaoning Province of China (Grant No 2019-MS-3608) for Kefeng Wang and 345 Talent Project of Shengjing Hospital of China Medical University for Kefeng Wang (Grant No M0122).

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.