Abstract
Individual dietary patterns may be influenced by diet-related behaviours, which may eventually play a significant role in contributing to colorectal cancer risk. As nearly half of colorectal cancer cases can be prevented through diet and lifestyle modification, in this study, we aimed to present an overview of the literature on diet-related behaviour and its effect on colorectal cancer risk among adults. Articles published from 2011 until July 2021 were selected. Out of the 1,198 articles retrieved, 25 were analyzed. There were 16 case-control studies, and nine of them were cohort studies. As a finding, the instruments used in this review were food frequency questionnaires (n = 23), followed by a semi-structured interview (n = 1), and diet records (n = 1). We demonstrated that unhealthy diet-related behaviours are linked to an increased risk of colorectal cancer in adults and those food frequency questionnaires or food records are common instruments used to collect diet-related behaviours. This article imparts the research trends and directions of colorectal cancer risk factors and shows that diet-related behaviour varies and changes over time.
Keywords: Colorectal neoplasms, Feeding behavior, Cooking method, Eating
INTRODUCTION
According to the World Health Organisation, cancer is the world's leading cause of death and is responsible for an estimated 10 million deaths in 2020 [1]. Cancer was responsible for approximately one in every six deaths globally. About 70% of cancer deaths occur in countries with low and medium incomes, and the mortality rate is also projected to increase in numbers by the year 2040 [2,3]. Colorectal cancer (CRC), which refers to both cancer of the colon and the rectum, is one of the most common types of cancer worldwide, accounting for 10% of worldwide cancer incidence with 9.4% cancer mortality [4]. Aside from dietary habits, other factors, such as age, lifestyle, and nutritional status, have a significant impact on the incidence of CRC [5,6].
CRC is thought to develop from colorectal adenoma, a benign and non-cancerous tumour that later progresses to become a precursor for the malignant and invasive form of adenocarcinoma; colorectal adenoma and sporadic CRC share common risk factors [7]. It may take many years for the progression from a non-cancerous form to a cancerous one [8]. The formation of colorectal adenocarcinomas can be classified into three patterns: sporadic, hereditary, and familial [9]. The non-hereditary risk factors, such as dietary and lifestyle behaviours and exposure to environmental genotoxins, are linked to the onset of sporadic CRC. In contrast, hereditary and familial CRC are linked with inherited mutations of certain genes and their interaction with environmental risk factors [10].
Nowadays, the study of the risks of CRC is becoming an important research focus since most of the risk factors are modifiable and preventable [11]. Dietary habits and related behaviours can significantly alter nutrient composition, such as changes in patterns of energy, macronutrients, and micronutrients, which can lead to the development of some cancers [12]. The majority of studies on CRC risk factors have been conducted in Western countries, but studies in Malaysia are lacking and need to be explored more in depth. Local studies show that males having a high percentage of body fat, smoking, and having a history of cancer in the family, are inclined to have an increased risk of CRC [13].
In addition, high fat and calorie intake and red meat consumption exceeding 100 g per day increase the risk of colorectal adenoma [13]. The determination of dietary patterns is important to know because the nutrients from different types of foods consumed together will affect the individual’s health. Compared to determining the intake of food types one by one, the determination of dietary patterns will provide a better quality and more comprehensive profiles of a diet [14]. Thus, dietary patterns should be determined and analysed to improve the ability to assess stronger effects as a result of the cumulative effects of nutritional characteristics and allow the evaluation of interactions between synergistic components [15].
It has previously been observed that the type of meat, cooking method, and temperature influence the amount and types of carcinogens [16]. Red meat intake and smoking are significantly associated with increased CRC risk [17]. The cooking process of meat can produce carcinogens, such as heterocyclic aromatic amines and polycyclic aromatic hydrocarbons. Similarly, processed meat products, such as cured and smoked meat, may also contain carcinogenic chemicals like N-nitroso compounds and polycyclic aromatic hydrocarbons formed through meat processing [18]. While the role of dietary patterns assessed by principal component analysis has also been increasingly evaluated, there is a paucity of data on food consumption behaviour. There are increasing reports suggesting that the need for diet-related behaviours could potentially lead to significant changes in limiting the risk of CRC. Obesity has been linked to increasing and varying snacking on unhealthy foods, cooking methods, meal frequency, and food type intake [19,20]. Due to the detrimental effects that poor dietary decisions have on general health, particular attention should be paid to these alterations as they may increase cardiometabolic risks [19,21]. Thus, in this review, we conducted a comprehensive analysis of food consumption behaviour considering meal frequency, food intake, and types of cooking methods.
MATERIALS AND METHODS
This scoping review was conducted on diet-related behaviour and the risk of CRCamong adults following Arksey and O’Malley’s [22] framework and the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA-ScR) guidelines [23]. The five stages that were applied are described below.
Identifying the research questions
As mentioned previously, the purpose of this study is to present an overview of the literature on diet-related behaviour among adults with CRC. The research question was identified to direct the review and determine the relevant studies. Thus, this scoping review was intended to answer the following research questions:
What are the instruments used to identify diet-related behaviour among adults with CRC?
What diet-related behaviours are prominent due to their effect on CRC risk in adults?
Identifying relevant studies
1) Search terms
Relevant studies published between January 2011 and July 2021 were identified for this scoping review. We intended to find evidence for five years; however, due to limited data, we expanded our search to ten years. The Population, Concept, and Context (PCC) in Table 1A below was used to guide at this stage based on the following mnemonic PCC, where the target population of this scoping review was adults with CRC and their diet-related behaviour. The MEDLINE Medical Subject Headings for key terms related to diet-related behaviour and CRC were carefully analyzed by two reviewers (NMABM and RS). Thus, these are the search terms used in this scoping review: (“Diet behaviour” OR “Food consumption” OR “meal timing” OR “dietary habit” OR “Dietary intake” OR “Diet” OR “Cooking methods”) AND (“Behaviour” OR “habit” OR “Practices”) for food consumption behaviour and (“Colorectal Cancer” OR “Colorectal neoplasm” OR “colon cancer” OR “rectal cancer” OR “bowel cancer”).
Table 1A.
Table of population, concept, and context
Population | Adults |
Concept | Diet-related behaviour |
Context/Outcome | Adults with colorectal cancer |
The inclusion criteria for the articles were as follows: 1) full-text articles from peer-reviewed journals and 2) a retrospective study aimed at understanding diet-related behaviour in CRC patients. Retrospective studies were selected to determine the effect of their dietary behaviour before subjects were diagnosed with CRC. Studies were excluded if they did not fit into one of these categories. In addition, any review articles and all other secondary sources were excluded from the study to make sure that only analysis of primary data was performed.
2) Databases
Three databases were queried in this review: PubMed (EMBASE), Science Direct, and the Cochrane Database of Systematic Reviews. We believe that these three search databases would collect relevant journals in the field of interest. In summary, 1,471 articles were retrieved using the above keywords and databases.
Study selection
With guidelines from PRISMA-ScR any duplicated titles were removed (n = 273), leading to 1,198 articles to be considered. After these articles were reviewed by NMAM and RS, about 1,173 of them were excluded due to the study population involving animals, in vitro or in vivo studies, bioactive components, and an irrelevant population. Only 25 articles were finally included in the review. The methodological quality of individual studies was not conducted, as this is not a compulsory step in scoping reviews [24].
Charting the Data
At this stage, all of the selected data extracted from the journal databases were organised in Microsoft Excel. The extracted data include the author(s), publication year, country, study design, objectives, type of instrument used, and the findings. We presented the data in four separate tables under the results section of this review.
Collating, summarising, and reporting results
Under Arksey and O’Malley’s [22] framework, the last stage was to categorise the relevant findings based on the research questions and focus on diet-related behaviour among adults with CRC. The flow diagram for this scoping review has been summarised in Appendix 1.
RESULTS
Characteristics of the selected studies
Following Arksey and O’Malley’s [22] framework and the inclusion criteria outlined above, the literature search found 25 relevant studies (Table 1B). As mentioned in the methods section, the study on food consumption behaviour and the incidence of CRC was still limited, which led to extending the scope of the target population. The sample size of participants involved ranged from 222 to 478,994. Meanwhile, the age range of participants was between 16 and 87 years old. The studies comprised nine cohort studies and 16 case-control studies. Among the 25 articles, seven were from the United States, four were from China, two each from Japan, Korea, and Norway, and one each from Australia, Pakistan, Brazil, Iran, Scotland, Greece, Spain, and Jordan. All the studies recruited participants from hospital and community-based settings.
Table 1B.
Characteristics, instrument, and outcome of the selected studies
Author (year), country | Study design | Instrument | Objective | No. of participants, mean age | Outcomes |
---|---|---|---|---|---|
Joshi et al. (2015) [26], North America | Population-based case-control study | FFQ, retrospective | A comprehensive analysis of red meat and poultry consumption, considering cooking practices, estimated levels of heterocyclic amines, tumor location, and tumor molecular characteristics | 3,364 CRC cases, 1,806 unaffected siblings, 136 unaffected | Positive association with CRC for pan-fried beefsteak, which was stronger among tumor mismatch repair proficiency deficient cases. |
Spouses, and 1,620 unaffected population-based controls, aged 59.4 ± 11.4 yr | A positive association between diets high in oven-broiled short ribs or spareribs and CRC risk and an inverse association with grilled hamburgers. | ||||
Tabatabaei et al. (2011) [25], Australia | Population-based case-control study | FFQ, retrospective | Investigated the association between meat consumption and cooking practices and the risk of CRC | 567 incident CRC cases and 713 controls, aged 41–80 yr | The amount of red baked meat consumed had a statistically significant inverse trend of association with CRC. The protective trends for red pan-fried meat were also borderline statistically significant. |
Khan et al. (2015) [41] Pakistan | Population-based case-control | Structured questionnaire, retrospective | To examine associations of dietary practices, addictive behavior and bowel habits in developing CRC among patients in a low-resource setup | 74 CRC patients and 148 controls, aged 41.47 ± 15.47 yr | All the dietary practices showed protective effect for CRC except for high fat diet. Individuals consuming high fats diet had 98% higher risk of CRC as compared to those who avoid using such diets. |
Angelo et al. (2016) [44]Brazil | Population-based case-control | Semi-quantitative FFQ (SQFFQ), retrospective | To investigate the role of the dietary pattern on the risk of SCA in Brazil | 169 patients with SCA and 101 controls, aged 29–87 yr | Individuals with higher intakes of beef, chicken, and pork had a 1.025, 1.069, and 1.121-fold increased risk of SCA when compared with controls. |
Ashmore et al. (2013) [39],Pennsylvania, US | Population-based case-control | FFQ, retrospective | To evaluate the role of dietary iron, heme iron, and supplemental iron on CRC risk | 1,196 incident CRC cases and 1187 healthy controls of both sexes, aged 64.2 ± 11.6 yr | Consumption of more than 18 mg/day of supplemental iron may increase risk for CRC. No significant associations between heme iron or total iron intake and CRC incidence. |
Bahrami et al. (2019) [36], Iran | Hospital-based case-control study | SQFFQ, retrospective | To examine the relationship between dietary polyphenols’ classes and individual polyphenol subclasses and also the risk of CRC and CRA | 129 colorectal cancers, 130 colorectal adenoma cases and 240 healthy controls, aged 30–79 yr | A higher intake of total polyphenols, total flavonoids, total phenolic acids anthocyanin and flavanols was related to the decreased risk of CRC. The higher consumption of stilbenes was also inversely associated with the risk of CRA. |
Hullings et al. (2020) [54], US | Cohort study | FFQ, prospective | Evaluated associations of whole grain and dietary fiber intake with CRC risk in the large National Institutes of Health - American Association of Retired Persons Diet and Health Study | 478,994 US adults, aged 50–71 yr | Intakes of whole grains and fiber from grains, but not total intake of dietary fiber, were inversely associated with CRC risk, particularly rectal cancer |
Takachi et al. 2011) [43], Japan | Cohort study | FFQ, prospective | Examined associations between the consumption of red and processed meat and the risk of subsite-specific CRC by gender in a large Japanese cohort | 80,658 men and women aged 45–74 yr | Potentially carcinogenic heterocyclic amines are formed when muscle meats such as beef, pork, or fish are cooked at high temperatures and are a possible mechanism of the association between red meat and colon cancer. |
Higher consumption of red meat was significantly associated with a higher risk of colon cancer among women, but no association was found between the consumption of processed meat and CRC risk. | |||||
Theodoratou et al. (2014) [40], Scotland | Case-control study | SQFFQ, retrospective | Investigated the relationship between CRC and demographic, lifestyle, food, and nutrient risk factors | 2,062 patients and 2,776 controls, aged 16–79 yr | High-energy snack foods, eggs, fruit/vegetable juice, sugar-sweetened beverages and white fish (associated with an increased CRC risk) and NSAIDs, coffee and magnesium (associated with a decreased CRC risk). |
Wang et al. (2013) [38], Japan | Community-based case-control study | FFQ, retrospective | To investigate the associations between dietary intake of polyphenols and CRC | 816 cases of CRC and 815 community-based controls, aged 20–74 yr | There was no measurable difference in total or tea polyphenol intake between cases and controls, but intake of coffee polyphenols was lower in cases than in controls. |
Decreased risk of CRC associated with coffee consumption. | |||||
Zhang et al. (2020) [57], China | Case-control study | FFQ, retrospective | Investigated the association between these dietary intakes and the risk of CRC in Guangdong | 2,380 patients with CRC and 2,389 sex- and age-matched controls, aged 30–75 yr | Inverse associations of dietary vitamin D, calcium, total dairy products, and milk intakes with the risk of CRC were independent of sex and cancer site. |
Protective effects of high dietary vitamin D, calcium, and dairy. | |||||
Zhong et al. (2013) [42], China | Case-control study | FFQ, retrospective | To examine the associations of total fat and fatty acid intakes with the risk of CRC in Guangzhou | 489 CRC cases were frequency matched to 976 controls, aged 30–75 yr | Total fat, saturated fat, monounsaturated fat, and n-6 polyunsaturated fat intakes were not related to the risk of colorectal cancer. However, increased consumption of n-3 polyunsaturated fat might reduce the risk. |
Xu et al. (2016) [37], China | Case-control study | FFQ, retrospective | To evaluate associations of flavonoids intake from different dietary sources with CRC risk in a Chinese population | 1,632 eligible CRC cases and 1,632 frequency-matched controls, aged | Anthocyanidins, flavanones and flavones intakes from total diet were found to be inversely associated with CRC risk. Flavonoids from vegetables and fruits, may be linked with the reduced risk of colorectal cancer. |
Vogtmann et al. (2013) [55], Shanghai | Cohort study | FFQ, prospective | To evaluate the association of fruit and vegetable consumption with the risk of CRC among Chinese men | 61,274 male participants aged 40–74 yr | Fruit intake was generally inversely associated with the risk of colorectal cancer, whereas vegetable consumption was largely unrelated to risk among middle-aged and older Chinese men. |
Sinha et al. (2012) [58], US | Cohort study | FFQ, prospective | Evaluated coffee and tea intakes (caffeinated and decaffeinated) in relation to colon (proximal and distal) and rectal cancers | 489,706 men and women who completed a baseline, aged 50–71 yr | Coffee was inversely associated with colon cancer, particularly proximal tumours. |
Perrigue et al. (2013) [28], US | Cohort study | FFQ, prospective | Association between eating frequency and CRC in a large, prospective cohort study, and explored whether this relationship was modified by sex, coffee consumption, or dietary glycaemic load | 67,912 western Washington residents aged 50–76 yr | Weak inverse association observed between eating frequency and CRC is consistent with findings from other prospective studies. |
In age- and sex-adjusted models, eating frequency was inversely associated with CRC risk (P trend = 0.001), with eating 4 or more times per day associated with a 28%–38% reduction in CRC risk compared with eating fewer than 3 times per day (HR for eating 4 times/d). | |||||
Michels et al. 2020 [34]US | Cohort study | FFQ, prospective | To examine the role of yogurt consumption on CRC incidence and mortality. | 83,054 women and 43,269 men, aged 30–55 yr | Frequency of yogurt consumption was associated with a reduced risk of proximal colon cancer with a long latency period. No significant inverse trend was observed for CRC mortality. |
Mekary et al. (2012) [29], US | Cohort study | FFQ, prospective | To examine association between eating frequency and colorectal cancer | 34,968 US men, aged 40–75 yr | There was an implied protective association between increased eating frequency of healthy meals and CRC risk and in men with factors associated with higher insulin sensitivity. |
Lee et al. (2017) [56], Korea | Case-control study | SQFFQ, retrospective | To investigate the relationship between the colors of vegetables and fruits and the risk of CRC in Korea. | 923 CRC patients and 1,846 controls | High total intake of vegetables and fruits was strongly associated with a reduced risk of CRC in women and a similar inverse association was observed for men. |
Kontou et al. (2013) [30], Greece | Case-control study | FFQ, retrospective | To investigate the association between dietary behaviours and CRC in the context of the Mediterranean diet. | 250 cases with newly diagnosed CRC 63 ± 12 and 250 controls | The higher the daily number of meals, the lower the likelihood of having CRC, coffee drinking was associated with higher likelihood of having CRC, the use of non-stick cookware was positively associated with CRC. |
Abu Mweis et al. (2015) [33], Jordan | Case-control study | FFQ, retrospective | Examining the association between food groups (including grains, fruits, vegetables, milk, meat, and legumes) and CRC risk in Jordan. | CRC patients (n = 167) and matched controls (n = 240) | Direct associations were found for grains, white bread, and chicken, whereas an inverse relation was reported for whole bread. |
Kim et al. (2019) [35], Korea | Case-control study | SQFFQ, retrospective | Examined whether increased green tea intake was associated with a decreased risk of CRC and how the risk of CRC was altered by the protective effect of green tea consumption and five health-related factors | 2,742 participants (922 cases, 56.6 ± 9.7 yr and 1,820 controls, 56.1 ± 9.1 yr) | High green tea consumption was associated with a decreased risk of CRC, with or without considering lifestyle factors. However, moderate green tea consumption increased the risk of CRC among ever-smokers, ever-drinkers, and the high-inflammatory diet group. Increased consumption of green tea might be helpful to reduce the risk of CRC in those with an unhealthy lifestyle. |
de Batlle et al. (2018) [27], Spain | Multicase-control study | FFQ, retrospective | To investigate the association between meat consumption and cooking practices and the risk of CRC in a population-based case-control study | 1,671 CRC cases, 67 ± 11 and 3,095 controls, 63 ± 12 yr | Rare-cooked red and total meat preference is associated with low risk of CRC among meat consumers. Griddle-grilling and barbequing meat could be associated with increased CRC risk and stewing, and oven-baking could increase the risk of white, but not red, meat. |
Bakken et al. (2018) [32], Norway | Cohort study | FFQ, prospective | To examine the association between milk intake and risk of CRC, colon cancer and rectal cancer among women | 81,675 women | Weak inverse association between milk intake and risk of colon cancer among women. |
Bakken et al. (2016) [31], Norway | Cohort study | FFQ, prospective | To investigate the association between whole-grain bread consumption and CRC incidence among Norwegian women | 78,254 women | No association between whole-grain bread consumption and CRC was found among the women in the Norwegian Women and Cancer Study. |
CRA, colorectal adenomas; CRC, colorectal cancer; FFQ, food frequency questionnaires; SQFFQ, Semi-quantitative FFQ; SCA, sporadic colorectal adenocarcinoma; US, United States.
Instruments used to identify diet-related behaviour
Most of the studies used a food frequency questionnaire (FFQ) (n = 23); two used a semi-quantitative food frequency questionnaire, and one used a structured questionnaire (Table 1B). All the information on dietary intake was collected via questionnaire, and 16 studies were retrospective, while nine were prospective. The settings of these studies included hospital-based and community populations. Some articles studied a single type of dietary intake, while others tackled multiple dietary intakes and types of cooking methods.
Studying diet-related behaviour and the incidence of CRC requires reliable and valid methods for the assessment of diet-related behaviour. Nineteen of the reported questionnaires dealt with food frequency, five were semi-quantitative, and one was structured. The purpose of most dietary methods was to obtain information on nutrient intake, although some were also concerned with information about food groups or specific food items. In few instances, the dietary method was concerned only with collecting data on food groups or items. Some used a semi-quantitative questionnaire to grasp a better idea of diet-related behaviour, as the FFQ may not capture it.
Diet-related behaviour
This review identified three different diet-related behaviours in these studies. They include (a) cooking methods (Table 2), (b) meal frequency (Table 3), and (c) food intake (Table 4). Three studies investigate the type of cooking method that increases the risk of CRC among adults. The majority of participants preferred barbecued meat, followed by pan-fried meat, and microwaved meat was the least preferred [25]. However, Joshi et al. [26] reported that pan-fried beefsteak, sausage, spam, ham, or bacon (especially among tumour mismatch repair proficiency) and a diet high in oven-broiled short ribs or spareribs had a strong positive association with the risk of CRC. Apparently, those who preferred their hamburgers well-done or very well-done had a 27% higher chance of developing CRC (95% confidence interval, 0.95–1.69) than those who preferred their hamburgers rare or medium-done, but none of these differences were significant [25]. Interestingly, a preference for rare-cooked meat was associated with a lower risk of CRC in both red and total meat [27].
Table 2.
Outcome of cooking method and association with risk of CRC
Diet-related behaviour | Author (year), country | Instrument | Association | Outcomes |
---|---|---|---|---|
Cooking method | Takachi et al. (2011) [43], Japan | FFQ, prospective | Positive | Cooking muscle meat at high temperature |
Joshi et al. (2015) [26], North America | FFQ, retrospective | Pan-fried beefsteak/sausage/spam/ham | ||
Oven-broiled short ribs or spareribs | ||||
de Batlle et al. (2018) [27], Spain | FFQ, retrospective | Griddle-grilled/barbecued meat was associated with an increased CRC risk | ||
Rare-cooked meat preference was associated with low risk of CRC in red and total meat | ||||
Stewing and oven-baking of white meat were associated with increased CRC risk | ||||
Joshi et al. (2015) [26], North America | FFQ, retrospective | Inverse association | Higher frequency of grilled/barbecued hamburgers | |
Tabatabaei et al. (2011) [25], Australia | FFQ, retrospective | No association | No association for red baked meat and red pan-fried meat |
CRC, colorectal cancer; FFQ, food frequency questionnaires.
Table 3.
Outcome of meal frequency and association with risk of CRC
Diet-related behaviour | Author, (year), country | Instrument | Association | Outcomes |
---|---|---|---|---|
Meal frequency | Perrigue et al. (2013) [28], US | FFQ, prospective | Inverse association | Higher eating frequency was associated with statistically significantly lower risk for colon cancer |
Mekary et al. (2012) [29], US | FFQ, prospective | Higher eating frequency among participants who had high insulin sensitivity, were physically active, and were lean (body mass index < 25) | ||
Kontou et al. (2013) [30], Greece | FFQ, retrospective | Higher the daily number of meals, the lower the likelihood of having CRC | ||
Mekary et al. (2012) [29], US | FFQ, prospective | No association | Highest eating frequency category (5–8 times/d) with the reference category (3 times/d), the authors found no evidence of an increased risk of CRC |
FFQ, food frequency questionnaires; US, United States; CRC, colorectal cancer.
Table 4.
Outcome of type of food intake and association with risk of CRC
Diet-related behaviour | Author, (year) country |
Instrument | Association | Outcomes |
---|---|---|---|---|
Polyphenols | Bahrami et al. (2019) [36], Iran | SQFFQ, retrospective | Inverse association | Higher intake total polyphenols, total flavonoids, total phenolic acids anthocyanin and flavanols |
Xu et al. (2016) [37], China | FFQ, retrospective. | All subclasses of flavonoids from vegetables and fruits | ||
Wang et al. (2013) [38], Japan | FFQ, retrospective | No association | Tea polyphenols and non-coffee polyphenols | |
Xu et al. (2016) [37], China | FFQ, retrospective. | Tea flavonoids | ||
Coffee | Kontou et al. (2013) [30], Greece | FFQ, retrospective | Positive association | Coffee drinking was associated with higher likelihood of having CRC |
Sinha et al. (2012) [58] US | FFQ, prospective | Inverse association | > 4 cups coffee lower risk of CRC | |
Green tea | Kim et al. (2019) [35], Korea | SQFFQ, retrospective | Positive association | Moderate green tea consumption increased the risk of CRC among ever-smokers, ever-drinkers, and the high-inflammatory diet group |
Inverse association | Increased consumption of green tea might be helpful to reduce the risk of CRC | |||
Meat | Angelo et al. (2016) Brazil [44] | SQFFQ, retrospective | Positive association | Higher intake of chicken, beef, and pork |
Abu Mweis et al. (2015) [33], Jordan | FFQ, retrospective | Higher frequency of consumption of chicken | ||
Supplement | Ashmore et al. (2013) [39], US | FFQ, retrospective | Positive association | More than 18 mg/d of supplemental iron |
Inversely associated | Dietary iron intake was inversely associated with CRC among women | |||
Whole grains | Hullings et al. (2020) [54], US | FFQ, prospective | Inversely associated | High intakes of whole grains and fiber from grains, particularly rectal cancer |
Abu Mweis et al. (2015) [33], Jordan | FFQ, retrospective | Whole grains bread | ||
Bakken et al. (2018) [32], Norway | FFQ, prospective | No association | Whole-grain bread consumption and CRC | |
Fiber | Vogtmann et al. (2013) [55], Shanghai | FFQ, prospective | Inversely associated | Fruit intake was generally inversely associated with the risk of CRC |
Lee et al. (2017) [56], Korea | SQFFQ, retrospective | High total intake of vegetables and fruits | ||
Vogtmann et al. (2013) [55], Shanghai | FFQ, prospective | No association | Vegetable consumption was largely unrelated to risk among middle-aged and older Chinese men | |
High-energy snack foods | Theodoratou et al. (2014) [40], Scotland | SQFFQ, retrospective | Positive association | High-fat and high-sugar foods, including pudding and deserts; chocolates, nuts and cakes crisps; and biscuits |
Beverages | Theodoratou et al. (2014) [40], Scotland | SQFFQ, retrospective | Positive association | High sugar sweetened beverages. High intake fruit/vegetable juices was associated with an increased CRC risk only in the high body mass index group |
Dietary vitamin D, calcium, and dairy products | Zhang et al. (2020) [57], China | FFQ, retrospective | Inversely associated | Dietary vitamin D, calcium, total dairy products, and milk |
Bakken et al. (2018) [32], Norway | FFQ, prospective | Weak inverse association between milk intake and risk of colon cancer among women | ||
Fat | Zhong et al. (2013) [42], China | FFQ, retrospective | No association | Total fat, saturated fat, monounsaturated fat, and n-6 polyunsaturated fat |
Omega 3 | Zhong et al. (2013) [42], China | FFQ, retrospective | Inversely associated | Increased consumption of n-3 polyunsaturated fat |
FFQ, food frequency questionnaires; SQFFQ, Semi-quantitative FFQ; US, United States; CRC, colorectal cancer.
Two cohort studies focused on the association between meal frequency and the CRC risk [28,29]. One study found that eating four or more times a day lowered the CRC risk by 28 to 38% as compared to eating fewer than three times a day [30]. This was supported by Kontou et al. [30]: the higher the daily meal frequency, the lower the likelihood of having CRC after adjusting for age, sex, body mass index (BMI), physical activity status, smoking habits, and family history of CRC. In contrast, a study conducted by Mekary et al. [29] believed that an increase in meal frequency, increased snack frequency, or breakfast pattern had no association with the incidence of CRC. There was no evidence of an increased risk of CRC when the highest meal frequency (6–8 times a day) was compared with the reference category of three times a day [29].
It has been reported that dietary vitamin D, calcium-rich dairy products, whole grains, and fibre were shown to be protective against CRC risk [31-34]. A case-control study conducted in Korea reported an association between green tea intake and the risk of CRC [35]. According to this study, moderate green tea intake elevated the risk of CRC; however, the risk was reduced when a higher amount of green tea was consumed [35]. Polyphenols are mostly found in a wide variety of plants, food, and beverages including green tea, and their protective effect on CRC risk is related to their antioxidant, anti-atherosclerotic, anti-inflammatory, and anticancer properties [36-38]. Furthermore, Ashmore et al. [39] discovered that a supplemental iron intake of more than 18 mg/d may increase the risk for CRC in a study on the association of dietary and supplemental iron and CRC. However, no significant associations were observed for dietary iron, total iron, or heme iron intakes.
Aside from sugar-sweetened beverages, poor dietary behaviour indicated by high-energy snacks food, which is defined as high-sugar foods, including pudding and desserts; chocolates, nuts, and crisps; and biscuits, cakes, and high-fat foods, was positively associated with the risk of CRC [40,41]. Meanwhile, Theodoratou et al. [40] also found that individuals with a high BMI were associated with an increased CRC risk, even when consuming a high intake of fruit or vegetable juices (fresh or ready-to-drink juice). As for total fat and fatty acid intakes, [42] suggested that total fat, saturated fat, monounsaturated fat, and n-6 polyunsaturated fat intakes were not related to the risk of CRC. However, increased consumption of n-3 polyunsaturated fat might reduce the risk.
DISCUSSION
Most of the articles reported a positive association between cooking methods and the risk of CRC. The current study found that cooking at high temperatures and long exposure to heat will result in the formation of a genotoxic agent, such as heterocyclic amines and polycyclic aromatic hydrocarbons, which are related to CRC formation. Therefore, cooking methods like grilling, barbecuing, pan-frying muscle meat, or cooking over a direct flame were found to have a positive association with CRC [27,28,43]. Takachi et al. [43] explained that meats like beef, pork [44], and fish produced carcinogens like heterocyclic amines when cooked at a high temperature, which relates to the possible mechanism associated with CRC. Tabatabaei et al. [25] agreed that relatively high temperatures affected mutagenic activity when they studied cooking methods and the level of doneness that can influence the content of by-products in meat.
Minimal studies have looked at the association between meal frequency and quality and the risk of CRC. Two studies have shown that higher meal frequency was associated with lower colon cancer risk among subjects with higher insulin sensitivity, a higher physical activity level, and a BMI below 25 kg/m2 [28,29]. According to Kontou et al. [30], the higher the number of meals daily, the lower the likelihood of having CRC, because frequent meals have been linked with a better lifestyle and diet as well as better blood sugar control, whereas a lower number of meals (< 3 times daily) were associated with elevated visceral fat and insulin resistance, an increase in alcohol consumption, and lower leisure physical activity [45,46].
These current findings are in contrast to previous case-control studies where a positive association was seen between meal frequency and CRC risk [47,48]. In this review, we discovered a limitation in terms of meal frequency, where it is solely measured in how many meals per day participants consume, and not all studies consider whether it is a healthy balanced diet or vice versa. It is more practical and relevant to record the types of meals, nutrients, and portion sizes compared to meal frequency alone [49]. These findings should be interpreted with caution because our bodies’ mechanisms interact differently with increasing or decreasing meal frequency, as it involves the concentration of bile acids secretions, serum glucose, and insulin levels, which may have a negative effect on cancer growth [50,51].
According to the World Cancer Research Fund, grains and their products, poultry, coffee, tea, omega-3 fatty acids, shellfish, and other seafood have limited to no conclusive evidence with regards to association with cancer [52]. Furthermore, consuming whole grains, dietary fibre, and dairy products is strongly associated with decreasing the risk of CRC [52]. A meta-analysis revealed a nonlinear inverse relationship between fruit and vegetable consumption and CRC [53]. Following the present results, previous studies have demonstrated an inverse to no association when examining whole grains, fibre, polyphenols, dietary vitamin D, calcium, and dairy products [32,33,35,54-58].
In a recent survey by the National Health and Morbidity Survey 2019, 95% of adults in Malaysia do not meet the recommended number of servings of fruits and vegetables a day and are taking less than that requirement. It is important to meet fruit and vegetable requirements as it will also provide therapeutic effects from natural compounds like polyphenols and aid in the prevention of diseases [59]. Polyphenols from natural sources are found to have a protective effect on cells against oxidative stress [60]. Some examples of foods and food materials that contain polyphenols include cereals and legumes (barley, corn, nuts, oats, rice, sorghum, wheat, beans, and pulses), oilseeds (rapeseed, canola, flaxseed, and olive seeds), fruits and vegetables, and beverages (fruit juices, tea, coffee, cocoa, beer, and wine) [61].
We included a range of diet-related behaviours (e.g., cooking methods, meal frequency, and food intake), which provided an opportunity to assess the effect of this factor on the risk of CRC. Some limitations need to be clarified in this review. Despite the fact that most studies used validated and reliable food frequency questionnaires or dietary intake questions, dietary intake was assessed using self- or parent-report, which was susceptible to measurement error and thus may have influenced the results. Researchers must look at the molecular level to dig into what diet-related behaviours cannot capture the risk of CRC in order to come up with more precise results for a dietary pattern guideline [62]. In terms of study design, some of the cohort and case-control studies included in the review were only conducted from 2011 until 2021 and may be subjected to selection bias and recall bias depending on the length of follow-up, sample size, and studied region.
We have shown in the present review that instruments used to collect diet-related behaviours are food frequency questionnaires or food records, and unhealthy diet-related behaviours are associated with an increased risk of CRC in adults. Therefore, this article can be applied not only to CRC but also to case studies of cancer, and it is suitable to provide readers with wide-ranging information. Diet-related behaviour alone is not enough. Thus, biological markers seem to be substantial and can contribute greatly to the prediction of CRC.
Funding Statement
FUNDING Malaysian Ministry of Higher Education Grant (FRGS/1/2020/STG02/UKM/02/5).
Footnotes
CONFLICTS OF INTEREST
No potential conflicts of interest were disclosed.
REFERENCES
- 1.Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global cancer observatory: cancer today. [Accessed Aug 8, 2021]. https://gco.iarc.fr/today.
- 2.Ferlay J, Laversanne M, Ervik M, Lam F, Colombet M, Mery L, et al. Global cancer observatory: cancer tomorrow. [Accessed Aug 8, 2021]. https://gco.iarc.fr/tomorrow/en/dataviz/isotype.
- 3.World Health Organization, author. Cancer. World Health Organization; Geneva: 2019. [Google Scholar]
- 4.Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 2019;16:713–32. doi: 10.1038/s41575-019-0189-8. [DOI] [PubMed] [Google Scholar]
- 5.Patel P, De P. Trends in colorectal cancer incidence and related lifestyle risk factors in 15-49-year-olds in Canada, 1969-2010. Cancer Epidemiol. 2016;42:90–100. doi: 10.1016/j.canep.2016.03.009. [DOI] [PubMed] [Google Scholar]
- 6.Song M, Garrett WS, Chan AT. Nutrients, foods, and colorectal cancer prevention. Gastroenterology. 2015;148:1244–60.e16. doi: 10.1053/j.gastro.2014.12.035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Sninsky JA, Shore BM, Lupu GV, Crockett SD. Risk factors for colorectal polyps and cancer. Gastrointest Endosc Clin N Am. 2022;32:195–213. doi: 10.1016/j.giec.2021.12.008. [DOI] [PubMed] [Google Scholar]
- 8.Leslie A, Carey FA, Pratt NR, Steele RJ. The colorectal adenoma-carcinoma sequence. Br J Surg. 2002;89:845–60. doi: 10.1046/j.1365-2168.2002.02120.x. [DOI] [PubMed] [Google Scholar]
- 9.Fleming M, Ravula S, Tatishchev SF, Wang HL. Colorectal carcinoma: pathologic aspects. J Gastrointest Oncol. 2012;3:153–73. doi: 10.3978/j.issn.2078-6891.2012.030. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Jasperson KW, Tuohy TM, Neklason DW, Burt RW. Hereditary and familial colon cancer. Gastroenterology. 2010;138:2044–58. doi: 10.1053/j.gastro.2010.01.054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Wong MC, Ding H, Wang J, Chan PS, Huang J. Prevalence and risk factors of colorectal cancer in Asia. Intest Res. 2019;17:317–29. doi: 10.5217/ir.2019.00021. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Ksouri R. Food components and diet habits: chief factors of cancer development. Food Qual Saf. 2019;3:227–31. doi: 10.1093/fqsafe/fyz021. [DOI] [Google Scholar]
- 13.Sharif R, Mohammad NMA, Jia Xin Y, Abdul Hamid NH, Shahar S, Ali RAR. Dietary risk factors and odds of colorectal adenoma in Malaysia: a case control study. Nutr Cancer. 2022;74:2757–68. doi: 10.1080/01635581.2021.2022167. [DOI] [PubMed] [Google Scholar]
- 14.Imamura F, Jacques PF. Invited commentary: dietary pattern analysis. Am J Epidemiol. 2011;173:1105–8. discussion 1109–10. doi: 10.1093/aje/kwr063. [DOI] [PubMed] [Google Scholar]
- 15.Schulze MB, Martínez-González MA, Fung TT, Lichtenstein AH, Forouhi NG. Food based dietary patterns and chronic disease prevention. BMJ. 2018;361:k2396. doi: 10.1136/bmj.k2396. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Sugimura T, Wakabayashi K, Nakagama H, Nagao M. Heterocyclic amines: mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci. 2004;95:290–9. doi: 10.1111/j.1349-7006.2004.tb03205.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Aykan NF. Red meat and colorectal cancer. Oncol Rev. 2015;9:288. doi: 10.4081/oncol.2015.288. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Bouvard V, Loomis D, Guyton KZ, Grosse Y, Ghissassi FE, Benbrahim-Tallaa L, et al. Carcinogenicity of consumption of red and processed meat. Lancet Oncol. 2015;16:1599–600. doi: 10.1016/S1470-2045(15)00444-1. [DOI] [PubMed] [Google Scholar]
- 19.Mattes RD. Snacking: a cause for concern. Physiol Behav. 2018;193(Pt B):279–83. doi: 10.1016/j.physbeh.2018.02.010. [DOI] [PubMed] [Google Scholar]
- 20.Bu T, Tang D, Liu Y, Chen D. Trends in dietary patterns and diet-related behaviors in China. Am J Health Behav. 2021;45:371–83. doi: 10.5993/AJHB.45.2.15. [DOI] [PubMed] [Google Scholar]
- 21.Micha R, Peñalvo JL, Cudhea F, Imamura F, Rehm CD, Mozaffarian D. Association between dietary factors and mortality from heart disease, stroke, and type 2 diabetes in the United States. JAMA. 2017;317:912–24. doi: 10.1001/jama.2017.0947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Arksey H, O'Malley L. Scoping studies: towards a methodological framework. Int J Soc Res Methodol. 2005;8:19–32. doi: 10.1080/1364557032000119616. [DOI] [Google Scholar]
- 23.Tricco AC, Lillie E, Zarin W, O'Brien KK, Colquhoun H, Levac D, et al. PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med. 2018;169:467–73. doi: 10.7326/M18-0850. [DOI] [PubMed] [Google Scholar]
- 24.Pham MT, Rajić A, Greig JD, Sargeant JM, Papadopoulos A, McEwen SA. A scoping review of scoping reviews: advancing the approach and enhancing the consistency. Res Synth Methods. 2014;5:371–85. doi: 10.1002/jrsm.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Tabatabaei SM, Fritschi L, Knuiman MW, Boyle T, Iacopetta BJ, Platell C, et al. Meat consumption and cooking practices and the risk of colorectal cancer. Eur J Clin Nutr. 2011;65:668–75. doi: 10.1038/ejcn.2011.17. [DOI] [PubMed] [Google Scholar]
- 26.Joshi AD, Kim A, Lewinger JP, Ulrich CM, Potter JD, Cotterchio M, et al. Meat intake, cooking methods, dietary carcinogens, and colorectal cancer risk: findings from the Colorectal Cancer Family Registry. Cancer Med. 2015;4:936–52. doi: 10.1002/cam4.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.de Batlle J, Gracia-Lavedan E, Romaguera D, Mendez M, Castaño-Vinyals G, Martín V, et al. Meat intake, cooking methods and doneness and risk of colorectal tumours in the Spanish multicase-control study (MCC-Spain) Eur J Nutr. 2018;57:643–53. doi: 10.1007/s00394-016-1350-6. [DOI] [PubMed] [Google Scholar]
- 28.Perrigue MM, Kantor ED, Hastert TA, Patterson R, Potter JD, Neuhouser ML, et al. Eating frequency and risk of colorectal cancer. Cancer Causes Control. 2013;24:2107–15. doi: 10.1007/s10552-013-0288-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Mekary RA, Hu FB, Willett WC, Chiuve S, Wu K, Fuchs C, et al. The joint association of eating frequency and diet quality with colorectal cancer risk in the Health Professionals Follow-up Study. Am J Epidemiol. 2012;175:664–72. doi: 10.1093/aje/kwr363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Kontou N, Psaltopoulou T, Soupos N, Polychronopoulos E, Linos A, Xinopoulos D, et al. The role of number of meals, coffee intake, salt and type of cookware on colorectal cancer development in the context of the Mediterranean diet. Public Health Nutr. 2013;16:928–35. doi: 10.1017/S1368980012003369. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Bakken T, Braaten T, Olsen A, Kyrø C, Lund E, Skeie G. Consumption of whole-grain bread and risk of colorectal cancer among Norwegian women (the NOWAC Study) Nutrients. 2016;8:40. doi: 10.3390/nu8010040. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Bakken T, Braaten T, Olsen A, Hjartåker A, Lund E, Skeie G. Milk and risk of colorectal, colon and rectal cancer in the Norwegian Women and Cancer (NOWAC) Cohort Study. Br J Nutr. 2018;119:1274–85. doi: 10.1017/S0007114518000752. [DOI] [PubMed] [Google Scholar]
- 33.Abu Mweis SS, Tayyem RF, Shehadah I, Bawadi HA, Agraib LM, Bani-Hani KE, et al. Food groups and the risk of colorectal cancer: results from a Jordanian case-control study. Eur J Cancer Prev. 2015;24:313–20. doi: 10.1097/CEJ.0000000000000089. [DOI] [PubMed] [Google Scholar]
- 34.Michels KB, Willett WC, Vaidya R, Zhang X, Giovannucci E. Yogurt consumption and colorectal cancer incidence and mortality in the Nurses' Health Study and the Health Professionals Follow-Up Study. Am J Clin Nutr. 2020;112:1566–75. doi: 10.1093/ajcn/nqaa244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Kim H, Lee J, Oh JH, Chang HJ, Sohn DK, Shin A, et al. Protective effect of green tea consumption on colorectal cancer varies by lifestyle factors. Nutrients. 2019;11:2612. doi: 10.3390/nu11112612. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Bahrami A, Jafari S, Rafiei P, Beigrezaei S, Sadeghi A, Hekmatdoost A, et al. Dietary intake of polyphenols and risk of colorectal cancer and adenoma- a case-control study from Iran. Complement Ther Med. 2019;45:269–74. doi: 10.1016/j.ctim.2019.04.011. [DOI] [PubMed] [Google Scholar]
- 37.Xu M, Chen YM, Huang J, Fang YJ, Huang WQ, Yan B, et al. Flavonoid intake from vegetables and fruits is inversely associated with colorectal cancer risk: a case-control study in China. Br J Nutr. 2016;116:1275–87. doi: 10.1017/S0007114516003196. [DOI] [PubMed] [Google Scholar]
- 38.Wang ZJ, Ohnaka K, Morita M, Toyomura K, Kono S, Ueki T, et al. Dietary polyphenols and colorectal cancer risk: the Fukuoka colorectal cancer study. World J Gastroenterol. 2013;19:2683–90. doi: 10.3748/wjg.v19.i17.2683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Ashmore JH, Lesko SM, Miller PE, Cross AJ, Muscat JE, Zhu J, et al. Association of dietary and supplemental iron and colorectal cancer in a population-based study. Eur J Cancer Prev. 2013;22:506–11. doi: 10.1097/CEJ.0b013e32836056f8. [DOI] [PubMed] [Google Scholar]
- 40.Theodoratou E, Farrington SM, Tenesa A, McNeill G, Cetnarskyj R, Korakakis E, et al. Associations between dietary and lifestyle risk factors and colorectal cancer in the Scottish population. Eur J Cancer Prev. 2014;23:8–17. doi: 10.1097/CEJ.0b013e3283639fb8. [DOI] [PubMed] [Google Scholar]
- 41.Khan NA, Hussain M, ur Rahman A, Farooqui WA, Rasheed A, Memon AS. Dietary practices, addictive behavior and bowel habits and risk of early onset colorectal cancer: a case control study. Asian Pac J Cancer Prev. 2015;16:7967–73. doi: 10.7314/APJCP.2015.16.17.7967. [DOI] [PubMed] [Google Scholar]
- 42.Zhong X, Fang YJ, Pan ZZ, Li B, Wang L, Zheng MC, et al. Dietary fat, fatty acid intakes and colorectal cancer risk in Chinese adults: a case-control study. Eur J Cancer Prev. 2013;22:438–47. doi: 10.1097/CEJ.0b013e32835e88c4. [DOI] [PubMed] [Google Scholar]
- 43.Takachi R, Tsubono Y, Baba K, Inoue M, Sasazuki S, Iwasaki M, et al. Red meat intake may increase the risk of colon cancer in Japanese, a population with relatively low red meat consumption. Asia Pac J Clin Nutr. 2011;20:603–12. [PubMed] [Google Scholar]
- 44.Angelo SN, Lourenço GJ, Magro DO, Nascimento H, Oliveira RA, Leal RF, et al. Dietary risk factors for colorectal cancer in Brazil: a case control study. Nutr J. 2016;15:20. doi: 10.1186/s12937-016-0139-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Holmbäck I, Ericson U, Gullberg B, Wirfält E. A high eating frequency is associated with an overall healthy lifestyle in middle-aged men and women and reduced likelihood of general and central obesity in men. Br J Nutr. 2010;104:1065–73. doi: 10.1017/S0007114510001753. [DOI] [PubMed] [Google Scholar]
- 46.Sierra-Johnson J, Undén AL, Linestrand M, Rosell M, Sjogren P, Kolak M, et al. Eating meals irregularly: a novel environmental risk factor for the metabolic syndrome. Obesity (Silver Spring) 2008;16:1302–7. doi: 10.1038/oby.2008.203. [DOI] [PubMed] [Google Scholar]
- 47.Coates AO, Potter JD, Caan BJ, Edwards SL, Slattery ML. Eating frequency and the risk of colon cancer. Nutr Cancer. 2002;43:121–6. doi: 10.1207/S15327914NC432_1. [DOI] [PubMed] [Google Scholar]
- 48.Wei JT, Connelly AE, Satia JA, Martin CF, Sandler RS. Eating frequency and colon cancer risk. Nutr Cancer. 2004;50:16–22. doi: 10.1207/s15327914nc5001_3. [DOI] [PubMed] [Google Scholar]
- 49.Johnson RK, Kerr DA, Schap TE. Chapter 8 - analysis, presentation, and interpretation of dietary data. In: Coulston AM, Boushey CJ, Ferruzzi MG, Delahanty LM, editors. Nutrition in the Prevention and Treatment of Disease. 4th ed. Academic Press; London: 2017. pp. 167–84. [DOI] [Google Scholar]
- 50.de Verdier MG, Longnecker MP. Eating frequency--a neglected risk factor for colon cancer? Cancer Causes Control. 1992;3:77–81. doi: 10.1007/BF00051916. [DOI] [PubMed] [Google Scholar]
- 51.Komninou D, Ayonote A, Richie JP, Jr, Rigas B. Insulin resistance and its contribution to colon carcinogenesis. Exp Biol Med (Maywood) 2003;228:396–405. doi: 10.1177/153537020322800410. [DOI] [PubMed] [Google Scholar]
- 52.World Cancer Research Fund, author; American Institute for Cancer Research, author. Diet, nutrition, physical activity and colorectal cancer in continuous update project expert report. World Cancer Research Fund/American Institute for Cancer Research; London: 2018. [DOI] [Google Scholar]
- 53.Aune D, Lau R, Chan DS, Vieira R, Greenwood DC, Kampman E, et al. Nonlinear reduction in risk for colorectal cancer by fruit and vegetable intake based on meta-analysis of prospective studies. Gastroenterology. 2011;141:106–18. doi: 10.1053/j.gastro.2011.04.013. [DOI] [PubMed] [Google Scholar]
- 54.Hullings AG, Sinha R, Liao LM, Freedman ND, Graubard BI, Loftfield E. Whole grain and dietary fiber intake and risk of colorectal cancer in the NIH-AARP Diet and Health Study cohort. Am J Clin Nutr. 2020;112:603–12. doi: 10.1093/ajcn/nqaa161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Vogtmann E, Xiang YB, Li HL, Levitan EB, Yang G, Waterbor JW, et al. Fruit and vegetable intake and the risk of colorectal cancer: results from the Shanghai Men's Health Study. Cancer Causes Control. 2013;24:1935–45. doi: 10.1007/s10552-013-0268-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Lee J, Shin A, Oh JH, Kim J. Colors of vegetables and fruits and the risks of colorectal cancer. World J Gastroenterol. 2017;23:2527–38. doi: 10.3748/wjg.v23.i14.2527. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Zhang X, Fang YJ, Feng XL, Abulimiti A, Huang CY, Luo H, et al. Higher intakes of dietary vitamin D, calcium and dairy products are inversely associated with the risk of colorectal cancer: a case-control study in China. Br J Nutr. 2020;123:699–711. doi: 10.1017/S000711451900326X. [DOI] [PubMed] [Google Scholar]
- 58.Sinha R, Cross AJ, Daniel CR, Graubard BI, Wu JW, Hollenbeck AR, et al. Caffeinated and decaffeinated coffee and tea intakes and risk of colorectal cancer in a large prospective study. Am J Clin Nutr. 2012;96:374–81. doi: 10.3945/ajcn.111.031328. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.de Araújo FF, de Paulo Farias D, Neri-Numa IA, Pastore GM. Polyphenols and their applications: an approach in food chemistry and innovation potential. Food Chem. 2021;338:127535. doi: 10.1016/j.foodchem.2020.127535. [DOI] [PubMed] [Google Scholar]
- 60.Mármol I, Sánchez-de-Diego C, Pradilla Dieste A, Cerrada E, Rodriguez Yoldi MJ. Colorectal carcinoma: a general overview and future perspectives in colorectal cancer. Int J Mol Sci. 2017;18:197. doi: 10.3390/ijms18010197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Macheix JJ. Fruit phenolics. CRC Press; Milton: 2018. [DOI] [Google Scholar]
- 62.Guasch-Ferré M, Bhupathiraju SN, Hu FB. Use of metabolomics in improving assessment of dietary intake. Clin Chem. 2018;64:82–98. doi: 10.1373/clinchem.2017.272344. [DOI] [PMC free article] [PubMed] [Google Scholar]