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Open Access Macedonian Journal of Medical Sciences logoLink to Open Access Macedonian Journal of Medical Sciences
. 2019 May 30;7(10):1723–1727. doi: 10.3889/oamjms.2019.265

Dietary Fibre Protective against Colorectal Cancer Patients in Asia: A Meta-Analysis

Masrul Masrul 1,*, Ricvan Dana Nindrea 2,3
PMCID: PMC6560290  PMID: 31210830

Abstract

BACKGROUND:

The association between dietary fibre and colorectal cancer risk is controversial.

AIM:

This systematic review and meta-analysis were performed to determine the dietary fibre protective against colorectal cancer patients in Asia.

METHODS:

The authors conducted a meta-analysis of published research articles on dietary fibre protective against colorectal cancer patients in Asia published between January 2000 and March 2019 in the online article databases of PubMed, ProQuest and EBSCO. Pooled odds ratios (OR) were calculated with fixed and random-effect models. Publication bias was visually evaluated by using funnel plots and statistically assessed through Egger’s and Begg’s tests. Data were processed using Review Manager 5.3 (RevMan 5.3) and Stata version 14.2 (Stata Corporation).

RESULTS:

This study reviewed 405 articles. There are 10 studies conducted a systematic review and continued with Meta-analysis of relevant data with several sample 49,964 patients. The results showed dietary fibre protective against colorectal cancer patients in Asia (OR = 0.66 [95% CI 0.56-0.77, p=0.008]). There was significant publication bias for studies included in dietary fibre protective against colorectal cancer patients in Asia.

CONCLUSION:

This analysis confirmed dietary fibre protective against colorectal cancer patients in Asia.

Keywords: Asia, Colorectal cancer, Dietary fibres, Meta-analysis, Protective

Introduction

Colorectal cancer is cancer that starts in the colon or the rectum. Colorectal cancer is one of the most common malignancies present in the world, ranks the third most frequent malignant disease diagnosed in the United States and fourth in Asia [1], [2]. Based on data from the World Health Organization, colorectal cancer is increasing rapidly in Asian countries. In Southeast Asia, in 2008, there are an estimated 1.6 million new cases of colorectal cancer and 1.1 million deaths [3].

Based on colorectal cancer risk factors are differentiated into nonmodifiable and modifiable risk factors. Nonmodifiable risk factors: age, race, genetics, family history, history of tumours, and ulcerative colitis. Modifiable risk factors: lifestyles such as cigarette use, low physical activity, long-term alcohol consumption, and bad dietary patterns [1], [4], [5].

Diet is a food choice that is commonly eaten by a person or population. Diet estimated an effect 30%-50% incidence of colorectal cancer worldwide. One of the dietary factors that contribute to colorectal cancer is a low-fibre diet. Dietary fibre is inversely proportional to the risk of colorectal cancer; high dietary fibre is evident in the prevention of colorectal cancer [6], [7].

The low-fibre diet is associated with an elevated risk of colorectal cancer [7]. However, due to wide geographical variation, the demography of colorectal cancer patients differs from those between developed and developing countries. This happens changes in dietary patterns and lifestyle, possibly due to globalisation and improving economic status, as well as the availability of screening programme may account for the risk of colorectal cancer.

Several previous studies have shown that dietary fibre is associated with a reduced risk of colorectal cancer [8], [9], [10]. But these results have no effect of dietary fibre for colorectal cancer; high dietary fibre intake was not associated with a reduced risk of colorectal cancer [11], [12]. However, the research results are not always consistent. Therefore, this study aims to determine the association of dietary fibre protective against colorectal cancer patients in Asia with some research through the Meta-analysis study so that the conclusion drawn have stronger strength. This leads to an increase in prevention, detection strategies in colorectal cancer patients.

Material and Methods

Study design and research sample

This research is quantitative research with meta-analysis study design. The meta-analysis followed the preferred reporting items for Systematic Reviews and Meta-Analysis (PRISMA) statement [13]. Meta-analysis was used to figure dietary fibre protective against colorectal cancer patients in Asia. The research samples were published research articles published between January 2000 and March 2019 in online article databases of PubMed, ProQuest and EBSCO.

Operational definitions

The variables of this study included independent variables consisted of dietary fibre (fruit, vegetables, cereals); and dependent variable: colorectal cancer.

Research procedure

This study was conducted by collecting data through the identification of published research articles on dietary fibre protective against colorectal cancer patients in Asia in online article databases of PubMed, ProQuest and EBSCO (Figure 1).

Figure 1.

Figure 1

Flow diagram research procedure

Identification of 405 articles, done by review through the title of the articles, continued by reviewing the abstract, and then the full-text form. The article was excluded if: (a) not the relevant subject outcome, (b) not case-control and cohort study (c) the information provided in the results were insufficient for data extraction.

Data collection technique

The data collection is done through an online search. The search was limited to English language articles. The article type was limited to journal articles. The research subject was limited to research with a human subject. The time of publication was limited from January 2000 to March 2019. The abstract of articles with potentially relevant titles was reviewed, while the irrelevant articles were excluded.

Furthermore, articles that have potentially relevant abstracts will be reviewed in full-text, while the irrelevant articles were excluded. The inclusion criteria of this study sample were researched on dietary fibre protective against colorectal cancer patients with case-control and cohort study. Exclusion criteria were: the research was not available in full-text form and when these criteria were not satisfied or if the provided information was insufficient for data extraction. The following data were obtained from each article: first author’s name and year of publication, region, type of study, characteristics, duration of the study, number of samples, fibre intake (g/day), dietary assessment and effect size.

Two independent investigators carefully extracted information from all studies that satisfied the inclusion criteria by a standardized protocol. Disagreements were resolved by three other investigators. Quality assessment was conducted using Newcastle–Ottawa Quality Assessment Scale (NOS). The papers with a total score of 0-3, 4-6, and 7-9 points were specified as the poor, moderate, and high quality [14].

Data analysis

The analysis held to get the value of log odds ratio, which is the combined odds ratio value from the research. Results were pooled using the odds ratio with corresponding 95% confidence intervals (CIs). Significant heterogeneity was indicated by I2 > 50% because these tests presented minimal statistical power in cases with few studies and small sample sizes. A random effect model was used when significant heterogeneity was observed; otherwise, a fixed effect model was utilised. A two-tailed P-value of < 0.05 was considered statistically significant.

Publication bias was visually evaluated by using funnel plots and statistically assessed through Egger’s and Begg’s tests. Meta-analysis was carried out in Stata version 14.2 (Stata Corporation).

Results

The selection of studies was conducted to obtain 10 studies with total of sample 49,964 patients related to dietary fibre protective against colorectal cancer patients in Asia (Table 1) [8], [9], [15], [16], [17], [18], [19], [20], [21], [22].

Table 1.

Systematic review association of dietary fibre with colorectal in Asia

First author, year Region Type of study Characteristic Duration of study Number of samples Fibre intake (g/day) Dietary assessment Effect size NOS
Chiu et al [15] China Case control M, F 30-74 years 5 years 2,483 M: 7.0 vs 12.4 F: 6.0 vs 10.5 Food frequency questionnaire OR (95% CI):0.6 (0.4-1.0) 8
Otani et al [16] Japan Case control M 20-74 years 5 years 331 13.8 vs 14.9 Food frequency questionnaire OR (95% CI):0.69 (0.45-1.90) 7
Shin et al [17] China Cohort F 40-70 years 2 years 283 N/A Food frequency questionnaire RR (95%CI): 1.1(0.6–1.8) 7
Wakai et al [18] Japan Cohort M, F 40-79 years 7.6 years 43,115 M: 6.7 vs 13.4 F: 7.4 vs 13.4 Food frequency questionnaire RR (95%CI):0.73 (0.51-1.03) 8
Nashar et al [19] Saudi arabia Case control M, F 30 years 1 years 100 11 vs 23 Food frequency questionnaire OR (95% CI): 0.68 (0.41-1.01) 6
Nayak et al [20] India Case control M, F 18-85 years 2 years 432 N/A Food frequency questionnaire OR (95% CI): 0.15 (0.05-0.46) 7
Uchida et al [21] Japan Case control F 20-74 years 5 years 1,631 9.2 vs 19.8 Prosky-AOCA method OR (95% CI): 0.76 (0.54–1.08) 8
Ramadas et al [22] Malaysia Case control M, F ≥ 30 years 1 years 118 3.94 vs 7.07 Food frequency questionnaire OR (95% CI): 0.14 (0.05–0.40) 6
Zhong et al [9] China Case control M, F mean age cases 56.7 ± 10.6; age controls 56.4 ± 10.5 2 years 954 9.2 vs 10.5 Food frequency questionnaire OR (95% CI): 0.68 (0.48–1.02) 7
Shong et al. [8] China Case-control M, F 30-70 years 1 year 517 20.52 vs 22.98 Food frequency questionnaire OR (95% CI): 0.40 (0.21–0.76) 7
Total of sample 49,964

Abbreviation: M, Male; F, Female; NOS, Newcastle–Ottawa Quality Assessment Scale.

Dietary fibre protective against colorectal cancer patients in Asia is shown in Figure 2.

Figure 2.

Figure 2

Dietary fibre protective against colorectal cancer patients in Asia

Figure 2 shows meta-analysis of dietary fibre protective against colorectal cancer patients in Asia (OR = 0.66 [95% CI 0.56-0.77, p = 0.008]). It’s mean the result of the study revealed the protective effect of dietary fibre observed in meta-analysis study was consistent with some previous findings.

Heterogeneity among studies (I2 = 59.5%) shows a variation of heterogeneity research for dietary fibre protective against colorectal cancer patients. Funnel plots was constructed to identify publication bias among studies dietary fibre protective against colorectal cancer patients in Asia (Figure 3).

Figure 3.

Figure 3

Funnel plots dietary fibre protective against colorectal cancer patients in Asia

There was no significant publication bias for studies included in dietary fibre protective against colorectal cancer patients in Asia, Egger’s test (p = 0.500) and Begg’s test (p = 0.227).

Discussion

The result of a meta-analysis of dietary fibre protective against colorectal cancer patients in Asia (OR = 0.66 [95% CI 0.56-0.77, p = 0.008]). Dietary fibre has a variation of heterogeneity between studies for the occurrence of colorectal cancer. Several studies have suggested the role of dietary fibre for protective colorectal cancer. High fibre intakes, particularly from cereals or grains and fruit, are associated with a reduced risk of incident colorectal adenoma and cancer [8], [12], [23]. Prospective study within a population-based screening trial suggests that individuals consuming the highest intakes of dietary fibre have reduced risks of incident colorectal adenoma and distal colon cancer and that this effect of dietary fibre, particularly from cereals and fruit, may begin early in colorectal carcinogenesis [11], [24].

Fibre source from fruit, vegetable, legume, cereal and grains. Intakes of carotenoids, light green vegetables, yellow-orange vegetables, broccoli, corn, carrots, bananas, garlic, and legumes (including soy products) were inversely associated with risk, even after adjustment for vegetable fibre. The data support a protective role of fibre from vegetables against colorectal cancer [25]. High intake of dietary fibre, in particular, cereal fibre and whole grains, was associated with a reduced risk of colorectal cancer [10].

A previous study in USA known that mean intake of dietary fibre (DF) is far below recommendations, with children and adolescents aged 2 to 19 years consuming an average of less than 14 g of DF per day. Adults 20+ years old consume, on average, about 17 g of DF per day, and men consume significantly more DF than women. Non-Hispanic black adults consume significantly less DF compared with other race/ethnic groups. Lower family income and living at less than 131% of poverty were associated with lower DF intakes among adults. Federal and local government policies should encourage consumption of all vegetables, including the white potato, as an important source of DF [26].

Another study in Africa known the total median [interquartile range (IQR)] values for total, insoluble, and soluble fiber consumed were 4.6 g [0.0-48.9], 0.0 g [0.0-18.0], and 0.0 g [0.0-15.0], respectively. Females had a higher median [IQR] intake of total (5.1 g [0.0-48.9] vs. 4.3 g [0.0-43.9]), insoluble (0.0 g [0.0-18.0] vs. 0.0 g [0.0-12.0]), and soluble fiber (0.0 g [0.0-14.9] vs. 0.0 g [0.-7.3]) than males, respectively [27]. Several studies are different from some aspects of others. For instance, the French cohort, who started in 1993, only adjusted for total energy intake.

On the other hand, the US cohort, which adjustment factors were too few, and the Italian cohort, which started in 1987, the range of the highest and lowest dietary fibre intake was relatively narrow (20.1 g/d vs 16.6 g/d, respectively) [28]. Mechanism of dietary fibre may decrease the risk of colorectal cancer by increasing stool bulk, diluting faecal carcinogens, and decreasing transit time, thus reducing the contact between carcinogens and the lining of the colorectum.

Also, bacterial fermentation of fibre results in the production of short chain fatty acids, which may have protective effects against colorectal cancer. Fruit, vegetable, legume, cereal and grains fibre may also protect against colorectal cancer, including antioxidants, vitamins, trace minerals, phytate, phenolic acids, lignans, and phytoestrogens [29], [30], [31].

There were a few limitations in this meta-analysis. First, three studies seemed potentially eligible to be included in this meta-analysis, but the full texts were not accessible. This issue may raise the possibility of selection bias. Second, there were a relatively large number of exclusions due to missing data to be included to meta-analysis, and not analysis for the proportion of participants for the different sex group. Third, validation data were not available for dietary questionnaires in several studies.

Conclusion

This analysis confirmed dietary fibre protective against colorectal cancer patients in Asia. The results of this study recommend the need to maintain the dietary fibre. Dietary fibre may be an effective measure for colorectal prevention. This study suggests the need for education and counselling about eating habits and the importance of avoiding foods with high fibre content.

Acknowledgements

The authors would thanks to Riyani Betri Novialita for data collecting.

Footnotes

Funding: This research did not receive any financial support

Competing Interests: The authors have declared that no competing interests exist

References

  • 1.Wolpin BM, Mayer RJ. Systemic treatment of colorectal cancer. Gastroenterology. 2008;134:1296–310. doi: 10.1053/j.gastro.2008.02.098. https://doi.org/10.1053/j.gastro.2008.02.098 PMid:18471507 PMCid:PMC2528832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Moghimi-Dehkordi B, Safaee A. An overview of colorectal cancer survival rates and prognosis in Asia. World journal of gastrointestinal oncology. 2012;4(4):71. doi: 10.4251/wjgo.v4.i4.71. https://doi.org/10.4251/wjgo.v4.i4.71 PMid:22532879 PMCid:PMC3334382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Kokki I, Papana A, Campbell H, Theodoratou E. Estimating the incidence of colorectal cancer in South East Asia. Croat Medical Journal. 2013;54:532–40. doi: 10.3325/cmj.2013.54.532. https://doi.org/10.3325/cmj.2013.54.532 PMCid:PMC3893985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Giovanucci E. Modifiable risk factors for colon cancer. Gastroenterol Clin North Am. 2002;31:925–43. doi: 10.1016/s0889-8553(02)00057-2. https://doi.org/10.1016/S0889-8553(02)00057-2. [DOI] [PubMed] [Google Scholar]
  • 5.Nindrea RD, Aryandono T, Lazuardi L. Breast cancer risk from modifiable and non-modifiable risk factors among women in Southeast Asia:a meta-analysis. Asian Pac J Cancer Prev. 2017;18:3201–6. doi: 10.22034/APJCP.2017.18.12.3201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Vargas AJ, Thompson PA. Diet and nutrient factors in colorectal cancer risk. Nutr Clin Pract. 2012;27:613–23. doi: 10.1177/0884533612454885. https://doi.org/10.1177/0884533612454885 PMid:22892274. [DOI] [PubMed] [Google Scholar]
  • 7.Murphy N, Norat T, Ferrari P, Jenab M, Bueno-de-Mesquita B, Skeie G, et al. Dietary fibre intake and risks of cancers of the colon and rectum in the European Prospective Investigation into Cancer and Nutrition (EPIC) Plos One. 2012;7:1–10. doi: 10.1371/journal.pone.0039361. https://doi.org/10.1371/journal.pone.0039361 PMid:22761771 PMCid:PMC3382210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Song Y, Liu M, Yang FG, Cui LH, Lu XY, Chen C. Dietary fibre and the risk of colorectal cancer:a case-control study. Asian Pac J Cancer Prev. 2015;16:3747–52. doi: 10.7314/apjcp.2015.16.9.3747. https://doi.org/10.7314/APJCP.2015.16.9.3747 PMid:25987032. [DOI] [PubMed] [Google Scholar]
  • 9.Zhong X, Fang YJ, Pan ZZ, Lu MS, Zheng MC, Chen YM, Zhang CX. Dietary fiber and fiber fraction intakes and colorectal cancer risk in Chinese adults. Nutr Cancer. 2014;66:351–61. doi: 10.1080/01635581.2013.877496. https://doi.org/10.1080/01635581.2013.877496 PMid:24673635. [DOI] [PubMed] [Google Scholar]
  • 10.Aune D, Chan DSM, Lau R, Vieira R, Greenwood DC, Kampman E, Norat T. Dietary fibre, whole grains, and risk of colorectal cancer:systematic review and dose-response meta-analysis of prospective studies. BMJ. 2011;343:d6617. doi: 10.1136/bmj.d6617. https://doi.org/10.1136/bmj.d6617 PMid:22074852 PMCid:PMC3213242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Kunzmann AT, Coleman HG, Huang WY, Kitahara CM, Cantwell MM, Berndt SI. Dietary fiber intake and risk of colorectal cancer and incident and recurrent adenoma in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial. Am J Clin Nutr. 2015;102:881–90. doi: 10.3945/ajcn.115.113282. https://doi.org/10.3945/ajcn.115.113282 PMid:26269366 PMCid:PMC4588743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Park Y, Hunter DJ, Spiegelman D, Bergkvist L, Berrino F, van den Brandt PA, et al. Dietary fiber intake and risk of colorectal cancer:a pooled analysis of prospective cohort studies. JAMA. 2005;294:2849–57. doi: 10.1001/jama.294.22.2849. https://doi.org/10.1001/jama.294.22.2849 PMid:16352792. [DOI] [PubMed] [Google Scholar]
  • 13.Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzche PC, Ionnidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions:explanation and elaboration. BMJ. 2009;339:b2700. doi: 10.1136/bmj.b2700. https://doi.org/10.1136/bmj.b2700 PMid:19622552 PMCid:PMC2714672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Wells GA, Shea B, O'Connell D, je Peterson, Welch V. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Eur J Epidemiol. 2011;25:603–5. doi: 10.1007/s10654-010-9491-z. https://doi.org/10.1007/s10654-010-9491-z PMid:20652370. [DOI] [PubMed] [Google Scholar]
  • 15.Chiu BC, Ji BT, Dai Q, Gridley G, McLauhlin JK, Gao YT, et al. Dietary Factors and Risk of Colon Cancer in Shanghai, China. Cancer Epidemiol Biomarkers Prev. 2003;12:201–8. [PubMed] [Google Scholar]
  • 16.Otani T, Iwasaki M, Hanaoka T, Kobayashi M, Ishihara J, Natsukawa S, et al. Folate, Vitamin B6, Vitamin B12, and Vitamin B2 Intake, genetic polymorphisms of related enzymes, and risk of colorectal cancer in a hospital-based case-control study in Japan. Nutr Cancer. 2005;53:42–50. doi: 10.1207/s15327914nc5301_5. https://doi.org/10.1207/s15327914nc5301_5 PMid:16351505. [DOI] [PubMed] [Google Scholar]
  • 17.Shin A, Li H, Shu XO, Shu XO, Yang G, Gao YT, et al. Dietary intake of calcium, fiber and other micronutrients in relation to colorectal cancer risk:Results from the Shanghai Women's Health Study. Int J Cancer. 2006;119:2938–42. doi: 10.1002/ijc.22196. https://doi.org/10.1002/ijc.22196 PMid:17019716. [DOI] [PubMed] [Google Scholar]
  • 18.Wakai K, Date C, Fukui M, Tamakoshi K, Watanabe Y, Hayakawa N, et al. Dietary fiber and risk of colorectal cancer in the Japan collaborative cohort study. Cancer Epidemiol Biomarkers Prev. 2007;16:668–75. doi: 10.1158/1055-9965.EPI-06-0664. https://doi.org/10.1158/1055-9965.EPI-06-0664 PMid:17416756. [DOI] [PubMed] [Google Scholar]
  • 19.Nashar RM, Almurshed KS. Colorectal cancer:a case control study of dietary factors, king faisal specialist hospital and researh center, riyadh, saudi arabia. Journal of family &community medicine. 2008;15(2):57–64. [PMC free article] [PubMed] [Google Scholar]
  • 20.Nayak SP, Sasi MP, Sreejayan MP, Mandal S. A case-control study of roles of diet in colorectal carcinoma in a South Indian population. Asian Pac J Cancer Prev. 2009;10:565–68. [PubMed] [Google Scholar]
  • 21.Uchida K, Kono S, Yin G, Toyomura K, Nagano J, Mizoue T, et al. Dietary fiber, source foods and colorectal cancer risk:the Fukuoka Colorectal Cancer Study. Scand J Gastroenterol. 2010;45:1223–31. doi: 10.3109/00365521.2010.492528. https://doi.org/10.3109/00365521.2010.492528 PMid:20500015. [DOI] [PubMed] [Google Scholar]
  • 22.Ramadas A, Kandiah M. Nutritional status and the risk for colorectal adenomas:a case control study in hospital Kuala Lumpur, Malaysia. Pakistan J Nutr. 2010;9:269–78. https://doi.org/10.3923/pjn.2010.269.278. [Google Scholar]
  • 23.Ben W, Sun Y, Chai R, Chai R, Qian A, Xu B, et al. Dietary fiber intake reduces risk for colorectal adenoma:a meta-analysis. Gastroenterology. 2014;146:689–99. doi: 10.1053/j.gastro.2013.11.003. https://doi.org/10.1053/j.gastro.2013.11.003 PMid:24216326. [DOI] [PubMed] [Google Scholar]
  • 24.Nindrea RD, Aryandono T, Lazuardi L, Dwiprahasto I. Protective effect of omega-3 fatty acids in fish consumption against breast cancer in Asian patients:a meta-analysis. Asian Pac J Cancer Prev. 2019;20:327–32. doi: 10.31557/APJCP.2019.20.2.327. https://doi.org/10.31557/APJCP.2019.20.2.327 PMid:30803190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Le Marchand L, Hankin JH, Wilkens LR, Kolonel LN, Englyst HN, Lyu LC. Dietary fiber and colorectal cancer risk. Epidemiology. 1997;8:658–65. doi: 10.1097/00001648-199710000-00008. https://doi.org/10.1097/00001648-199711000-00012 PMid:9345666. [DOI] [PubMed] [Google Scholar]
  • 26.Storey M, Anderson P. Income and race/ethnicity influence dietary fiber intake and vegetable consumption. Nutr Res. 2014;34:844–50. doi: 10.1016/j.nutres.2014.08.016. https://doi.org/10.1016/j.nutres.2014.08.016 PMid:25262170. [DOI] [PubMed] [Google Scholar]
  • 27.Sekgala MD, Mchiza ZJ, Parker W, Monyeki KD. Dietary Fiber Intake and Metabolic Syndrome Risk Factors among Young South African Adults. Nutrients. 2018;10:504. doi: 10.3390/nu10040504. https://doi.org/10.3390/nu10040504 PMid:29670048 PMCid:PMC5946289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Chen S, Chen Y, Ma S, Zheng R, Zhao P, Zhang L, et al. Dietary fibre intake and risk of breast cancer:A systematic review and meta-analysis of epidemiological studies. Oncotarget. 2016;7:80980–89. doi: 10.18632/oncotarget.13140. https://doi.org/10.18632/oncotarget.13140 PMid:27829237 PMCid:PMC5348370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Slavin JL. Mechanisms for the impact of whole grain foods on cancer risk. J Am Coll Nutr. 2000;19:S300–7. doi: 10.1080/07315724.2000.10718964. https://doi.org/10.1080/07315724.2000.10718964. [DOI] [PubMed] [Google Scholar]
  • 30.Webb AL, McCullough ML. Dietary lignans:potential role in cancer prevention. Nutr Cancer. 2005;51:117–31. doi: 10.1207/s15327914nc5102_1. https://doi.org/10.1207/s15327914nc5102_1 PMid:15860433. [DOI] [PubMed] [Google Scholar]
  • 31.Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey A, Harper P. Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr. 2006;136:3046–53. doi: 10.1093/jn/136.12.3046. https://doi.org/10.1093/jn/136.12.3046 PMid:17116718 PMCid:PMC1850957. [DOI] [PMC free article] [PubMed] [Google Scholar]

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