A Systematic Review of the Association between Dietary Patterns and Breast Cancer Risk

Results: 2,215 articles were found and 112 articles were chosen for further review, of which 87 articles were excluded after reviewing the title and abstract of each article. The remaining 25 articles were included in the paper after a full review. Although in most of the articles included in this paper, no overall association was reported between the prudent, Mediterranean or Western dietary patterns and breast cancer risk, it was suggested that a Western or Western-type dietary pattern might increase the risk of breast cancer, and a prudent, Mediterranean and healthy dietary patterns might protect against estrogen receptive-negative tumors, mostly in postmenopausal women.

In many studies, factor analysis or principal component analysis were used to develop dietary patterns [19]. These methods usually combined the variables and factors together to represent the different eating patterns of the study population; therefore, it was harder to make specific judgments on any possible association between dietary patterns and the risk of breast cancer [19].

Purpose
This systematic review aims to investigate and clarify the association between dietary patterns and breast cancer risk by evaluating and appraising the literature published to date and assessing the results of these studies.

Literature review
Recently, dietary pattern analysis has arisen as a complementary approach to investigative the relationship between diet and risk of chronic diseases [21]. Instead of looking at individual nutrients or foods, pattern analysis studies the effects of overall diet on the development of certain diseases [21]. Theoretically, dietary patterns signify a broader image of food and nutrient consumption, and may thus be more predictive of disease risk than individual foods or nutrients [21]. In addition, there is a growing interest in using dietary quality directories to assess whether adherence to a certain dietary pattern such as Mediterranean pattern, can lower the risk of certain chronic diseases such as breast cancer in the long term [21].
This systematic review is aimed to analyze the literature published to date and assess the impact of dietary patterns on the risk, occurrence, recurrence, and mortality rates of breast cancer and identify the best dietary pattern that can help reduce the risk of breast cancer. This paper covers the following topics: 1. The difference between ER-positive and ER-negative breast cancer.
2. The relationship between dietary patterns and risk of breast cancer.
3. Types of dietary patterns that can help decrease the risk of breast cancer.

ER-positive breast cancer versus ER-negative breast cancer:
Despite the intensive research, it has not yet been fully understood if ER _ negative breast cancer is an advanced form of ER _ positive breast cancer or whether ER + and ER − breast cancer are two biologically different diseases with different risk factors [22]. According to many studies, the prediction of survival rates of ER _ breast cancer patients has been recognized to be lower than that of ER + breast cancer patients, and it is found that the cancer tumors usually lose their estrogen dependency during their progression, leading to the theory that ERbreast cancer may be a more advanced stage of ER + breast cancer [22]. According to the literature, micronutrients from fruits and vegetables may prevent both types of breast cancer, but in ER+ breast cancer the estrogen level might override the preventive effects of the micronutrients, since it is the most important factor [22]. In ER-breast cancer, on the other hand, the effects of fruits and vegetables may be observed better since ER-breast cancer has a lower dependency on the estrogen level [22].

Different types of dietary patterns and risk of breast cancer:
Many epidemiologic studies have linked the consumption of individual foods to the risk of breast cancer [23]. An increased risk of breast cancer has been reported to be associated with high intakes of red meat, animal fat and refined carbohydrates [23]. Foods that are found to be inversely associated with breast cancer risk include fruits and vegetables, cereal, olive oil, low-fat dairy products and dietary calcium [23].
According to a prospective cohort study conducted from 1995 through 2007 to examine the relationship between different dietary patterns and breast cancer, a reduced breast cancer risk was reported to be associated with a prudent dietary pattern, a traditional southern dietary pattern, stew and traditional dietary patterns, a salad vegetable pattern, a vegetable/soy pattern, and Native Mexican and Mediterranean patterns [23]. All of these dietary patterns are higher in fruits and vegetables and lower in animal fats compared to the classic "Western" diet [23].
In general, the prudent dietary pattern is characterized by higher consumption of fruits, vegetables, whole grains, low-fat dairy products, fish and poultry, whereas the Western pattern is categorized by higher intake of red and processed meats, refined grains, desserts and high-fat dairy products [24]. According to a study performed to examine the association between diet and the risk of postmenopausal breast cancer by using different approaches of dietary patterns, neither prudent nor Western dietary pattern was associated with overall risk of breast cancer among the study population; however, there was an inverse association between the prudent pattern and estrogen receptor-negative breast cancer [24]. It was also reported that among the main food groups, higher intakes of fruits and vegetables were significantly associated with decreased risk for ER − breast cancer [24].
Based on the findings of a prospective Study of major dietary patterns and the risk of breast cancer on postmenopausal Swedish women, higher fat intake showed a slightly but not significantly increased risk with ER + tumors, and a slightly but not significantly reduced risk with ER − tumors [25].
A cohort study of 91,779 female teachers in California that was conducted to evaluate the relationship between dietary patterns and breast cancer, demonstrated that the plant-based pattern was associated with a reduction in breast cancer risk [26]. This risk reduction was higher for estrogen receptor-negative progesterone receptor-negative (ER-PR-) tumors [26]. The salad and wine pattern, on the other hand, was associated with an increased risk of estrogen receptor-positive progesterone receptor-positive tumors (ER+PR+); this effect was only slightly decreased after adjustment for alcohol consumption [26].
It is suggested that diets rich in dietary fiber, especially fiber from vegetables may be associated with a slight reduction in the risk of breast cancer, respectively [27]. According to a prospective study that was performed to investigate the relationship between dietary fiber intake and risk of hormonal receptor-defined breast cancer, breast cancer risk was inversely associated with high intakes of total dietary fiber and fiber from vegetables but not from fruits, cereals, or legumes [27]. For vegetable fiber, stronger associations were found for estrogen receptornegative and progesterone receptor-negative tumors compared to estrogen receptor-positive and progesterone receptorpositive tumors [27]. Furthermore, based on the results of a large prospective study of 623, 080 middle-aged UK women, little or no decrease were found in the incidence of breast cancer with the consumption of organic foods [28].
According to a prospective cohort study that was aimed to investigate the association between dietary protein sources and breast cancer incidence, it was found that higher red meat intake in early adulthood could be a risk factor for developing breast cancer [29]. Based on the findings of this study, substituting one serving/day of legumes for one serving/day of red meat could lower the risk of breast cancer among all women by 15% and among postmenopausal women by 19% [29]. Furthermore, substituting one serving/day of poultry for one serving/day of red meat was associated with 17% lower risk of breast cancer overall and 24% lower risk of postmenopausal breast cancer [29].
In addition, substituting one serving/day of mixed legumes, nuts, poultry, and fish for one serving/day of red meat was associated with a 14% lower risk of breast cancer overall [29].
It is also suggested that there is a positive association between Mediterranean dietary pattern and prevention of all breast cancer subtypes [30,31]. Traditionally the Mediterranean diet is categorized by a high consumption of vegetables, legumes, fruits, nuts, unrefined cereals, olive oil but a low intake of saturated fats, a moderately high intake of fish; a low-to-moderate intake of dairy products mostly in the form of cheese or yogurt; a low intake of meat and poultry, and a regular but moderate intake of alcohol, mainly in the form of wine and usually during the meals [32].
Therefore, based on the findings of these studies it is suggested that there is an increased risk of breast cancer among individuals who are on Western or Western-like dietary pattern compared to prudent, healthy, and Mediterranean dietary patterns [23]. It is also suggested that a high vegetable intake is associated with lower hormone receptor-negative breast cancer risk [33]. Information extracted from each article included exact duration of follow-ups, the exact number of cancer cases in each study, risk estimates with Cancer Incidence, and some factors that were adjusted due to the design of the studies. The peer reviewed articles before 2001 were also excluded. No specific study design was excluded from this systematic review.

Results
In total, 2, 215 articles were found and 112 articles were chosen for further review, of which 87 articles were excluded after reviewing the title and abstract of each article. The remaining 25 articles were included in the paper after a full review. The total number of articles is presented in Table 1.
In 22 of the articles used in this systematic review, an association was found between dietary patterns and breast cancer risk. Three of the selected studies did not show any association between dietary patterns and breast cancer risk. The descriptions of all the 25 articles used in this paper are displayed in Table 2 and their results are discussed. Studies that showed an association between dietary patterns and breast cancer risk are identified in Table 3 and studies that did not suggest any association between dietary patterns and breast cancer risk are discussed in Table 4.
According to 6 of the studies included in this paper, Western or Western-type dietary pattern are associated with breast cancer risk [24,30,[34][35][36][37]. Based on the findings of 5 of the articles used in this systematic review, drinker dietary pattern [25], higher consumption of total red meat [29], high-fat dairy products [38], starch-rich dietary pattern [39], and meat-sweet dietary pattern [35] are also related to the development of breast cancer, particularly among postmenopausal women.
According to 16 of the studies used in this paper, prudent dietary pattern [23,24]; Mediterranean dietary pattern [30,31,36]; high consumption of raw vegetables, fruits and olive oil [22,26,33,40]; diets rich in dietary fiber [27]; diets high in 3 fatty acids abundant in fish [41]; low intake of meat/starches and a high intake of legumes [42]; traditional, healthy, and stew diets [34]; low consumption of Western dietary pattern plus effective weight control [35]; substituting red meat with a combination  Food-frequency questionnaire Four dietary patterns were identified: salad vegetables (mainly consisting of raw vegetables and olive oil); Western (mainly consisting of potatoes, red meat, eggs and butter); canteen (pasta and tomato sauce); and prudent (cooked vegetables, pulses, and fish, with negative loading on wines and spirits). After adjustment for potential confounders, only the salad vegetables pattern was associated with significantly lower (34-35%) breast cancer incidence (RR = 0.66, CI 95% = 0.47±0.95 comparing highest with lowest tertile) with a significant linear trend (P = 0.016).
Fung et al., Food-frequency questionnaire Although the overall dairy intake was unrelated to breast cancerspecific outcomes, it was positively associated with the overall mortality rate. It was suggested that low-fat dairy intake was unrelated to recurrence or survival. However, high-fat dairy intake was associated with a higher risk of mortality after breast cancer diagnosis (0. 5  Two dietary patterns were identified: Western and prudent. The prudent diet was weakly associated with lower breast cancer risk overall; P for trend = 0.06. In analyses stratified by body mass index, the prudent dietary pattern was associated with a significantly lower risk of breast cancer in women with a BMI <25 (IRR: 0.64; 95% CI: 0.43, 0.93; P for trend = 0.01). The prudent dietary pattern was also associated with a significantly lower risk of breast cancer in premenopausal women (IRR: 0.70; 95% CI: 0.52, 0.96; P for trend = 0.01), and a significant inverse association for the prudent dietary pattern and estrogen receptor-negative breast cancer was found, as well (IRR: 0.52; 95% CI: 0. 28    of legumes, poultry, nuts and fish [29]; and combined healthy behaviors [43] can help reduce the risk of breast cancer, mostly in postmenopausal women particularly in estrogen receptornegative tumors.
One of the studies included in this paper suggests that the consumption of animal products and the vitamins and fiber patterns can help decrease the risk of breast cancer, as well [39]. Based on the results of one of the studies, consumption of flaxseed and flax bread is also associated with significant reduction of breast cancer incidence [44]. Traditional Southern Diet is also reported to help reduce breast cancer risk [45].
In 3 studies used in this paper, on the other hand, no association was found between any dietary patterns and the risk of breast cancer [46][47][48].

Discussion
The findings reported in this systematic review are in agreement with some of the previously published systematic reviews. In a systematic review and meta-analysis that was conducted by Brennan et al, in which 16 studies published between 2001 and 2009 were included, it was suggested that there was a possible inverse association between breast cancer and a dietary pattern characterized by consuming vegetables, fruits, legumes, whole cereals, fish, chicken, and foods with a low fat content [19]. In another systematic review conducted by Edefonti et al., in which 19 articles between 1995 and 2008 were included, it was reported that a diet rich in high-fat and high-sugar foods was associated with an increased risk of breast cancer [49]. On the other hand, a diet rich in vegetables, fruits, fish, and white meat was associated with a reduced risk of breast cancer [49]. According to a metaanalysis conducted by Aune et al., in which 14 cohort studies and one nested case-control study were included, it was found that high versus low intake of fruits and combined fruits and vegetables, but not vegetables alone, were associated with small, but statistically significant reduction in breast cancer risk [50].
The Pooling Project of Prospective Studies of Diet and Cancer, also analyzed the data collected from 993,466 women from 20 cohort studies, in which 19,869 cases of ER+ cancer and 4,821 cases of ER-cancer were included [51]. In this systematic review, the total fruit consumption was inversely associated with risk of ERbreast cancer but not breast cancer in general or the ER+ subtype [51]. The combined total consumption of fruits and vegetables was inversely associated with the risk of ER-breast cancer, but not with the risk of breast cancer in general or ER+ tumors [51]. According to this systematic review, the inverse association for ER − tumors was primarily observed for the consumption of vegetables [51].
There are several potential mechanisms that can explain the inverse association between the consumption of fruits and vegetables and breast cancer risk. Fruits and vegetables are good sources of fiber, which can prevent breast cancer by binding estrogens during the process of enterohepatic reabsorption of estrogen that takes place in the colon [50]. Fruits and vegetables are also very good sources of various antioxidants including glucosinolates, carotenoids, indoles, and isothiocyanates, which can help prevent breast cancer by inducing the process of detoxifying enzymes, and decreasing oxidative stress and inflammation [50].
This systematic review aimed to investigate the association between dietary patterns and breast cancer risk. Although in most of the articles included in this systematic review, no overall association was observed between the prudent, Mediterranean or Western dietary patterns and breast cancer risk, it was suggested that a Western or Western-type dietary pattern might increase the risk of breast cancer, and a prudent, Mediterranean and healthy dietary patterns might protect against estrogen receptive-negative tumors particularly in postmenopausal women [23,24,30,31,[34][35][36][37]. According to the results, although the intake of fruits and vegetables might not necessarily have a significant preventive effect on the development of postmenopausal breast cancer, increasing the intake of fruits and vegetables is associated with a lower incidence of ER − breast cancer, suggesting that fruits and vegetables might either cause a delayed progression from ER + to ER − tumors, or that the development of ER + and ER − breast cancers react differently to the consumption of fruits and vegetables, respectively [22].
According to the results of 22 studies in this systematic review, the prudent; Mediterranean; healthy dietary patterns; high intakes of fruits, vegetable, olive oil/sunflower oil; high intakes of dietary fiber, especially fiber from vegetables; substituting red meat with a combination of legumes, poultry, nuts and fish; and low intakes of red meat, high fat meats, and high fat dairy products were associated with a decrease in the risk of breast cancer, particularly in estrogen receptive-negative tumors in postmenopausal women. This inverse association remained the same when the results of just the cohort studies alone, among these 22 studies, were also analyzed.

Limitations
There are potential limitations to this systematic review. The pooled results discussed in this paper, are directly retrieved from the included studies, which have their own individual strengths and weaknesses in terms of study design [19]. It is also possible that there may have been a misclassification within the healthy, prudent and Mediterranean dietary patterns in the articles reviewed in this paper. The healthy, prudent and Mediterranean dietary patterns included in this paper, all contained high consumption of plant-based foods and low consumption of red, high-fat and processed meat, which are the recommended dietary patterns suggested by the American Cancer Society to prevent cancer across the populations [52]. There are disadvantages to this type of analysis. Since the exact amount of consumption of individual foods in the prudent, Mediterranean, and healthy dietary patterns were not exactly identical among the studies in this paper, it could have led to some misclassification errors. Even very small measurement errors can dramatically affect the measures of the risk for a disease; therefore, it is possible that the small inverse association observed could have been due to a combination of dietary measurement errors and misclassification of women into the dietary pattern categories [19].
In order to minimize the risk of bias, the authors of the selected articles generally discussed the most commonly identified dietary patterns across the populations. Therefore, other types of dietary patterns that could be relevant to breast cancer risk were not included in this review. The tools used to collect dietary information in this systematic review were also different among the studies. Although the food frequency questionnaire was used in most cases, this tool is known to be subject to measurement errors [4]. Therefore, it is not the most reliable tool to detect a significant association between a dietary pattern and breast cancer risk.

Conclusion
In conclusion, Western or Western-type dietary patterns which mainly include high consumption of red meat products, French fries, appetizers, rice, pasta, potatoes, pizza, pies, canned fish, eggs, alcoholic beverages, cakes, mayonnaise, and butter/cream [36]; are positively associated with breast cancer risk. Adherence to healthy, Mediterranean, and prudent dietary patterns, which essentially include vegetables, fruits, seafood, poultry, nuts, legumes, olive oil, and sunflower oil; on the other hand, are negatively associated with breast cancer risk in postmenopausal women, and this association is stronger in estrogen receptornegative tumors. Therefore, adherence to a diet containing mostly fruits, vegetables, fish, nuts, and olive/sunflower oil, along with avoidance of Western-type foods, may contribute to a significant reduction in postmenopausal breast cancer risk [36].
The results of this systematic review support the potential chance for breast cancer prevention through dietary modifications. These results also highlight the need for further observational and interventional studies to explain the role of dietary patterns and breast cancer risk across populations.