The Truth About Grains, Part II

In my last post, I shared my thoughts about the current dietary fad of avoiding grains and my personal approach to a healthful diet. In general, I recommend replacing refined grains with whole grains and suggest two servings of whole grains per day, served as part of two balanced meals. In this post, I delve deeper into the truth about grains, including scientific research that can help you make an educated decision about including grains in your diet.

Overwhelming epidemiological studies have shown that regular consumption of food based on whole-grains and their products is associated with reduced risks of various types of degenerative chronic diseases; these studies consistently show that whole-grain intake is protective against cancer, cardiovascular disease, diabetes and obesity. As has been elucidated in a number of research papers, whole-grains contain a wide variety of important compounds that contribute to their health-promoting and disease preventive effects.[1] [2] [3]

The most well known whole grains consumed worldwide include wheat, rice, corn, oats, barley, rye, sorghum, millet and buckwheat. Each of these grains has unique health promoting peptides and health benefits—whole-grain foods are a major source of energy from carbohydrates, and provide protein, B vitamins, and minerals, as well as important disease preventive phytonutrients for the world population.[4] Whole grains, including whole wheat, do not make us fat, cause cancer, heart disease, or neurological diseases, or make us sick in any way unless we are truly allergic to them.  In fact, eating whole grains within a balanced diet is associated with numerous health benefits, including a reduction in cancer, heart disease, and even obesity.

According to recent research, eating whole grains, including whole wheat, not only doesn’t cause inflammation,[5] but can actually reduce systemic inflammation[6]—unless of coarse you have celiac disease or are highly sensitive to gluten, a condition referred to as nonceliac gluten-sensitivity (NCGS). For example, research shows that whole-grain intake favorably affects markers of systemic inflammation in obese children. In a randomized crossover clinical trial, 44 overweight or obese girls aged 8-15 years were randomly assigned to either whole-grain or control groups. Subjects in the whole-grain group were given a list of whole-grain foods and were asked to obtain half of their needed servings of grains from whole-grain foods each day for 6 weeks. The study found a significant beneficial effect of whole-grain intake on various biomarkers of systemic inflammation, including C-reactive protein.[7]

Scottish researchers have found evidence that the protective benefit of whole grains is due to positive changes in gut microbiota due to phytophenols from plant fiber. They compared the phytophenols in recommended serving sizes of whole grains, fruits and vegetables, and found that the whole grain cereals delivered substantially higher amounts of phytophenols available for metabolism in the colon, which “may, in part, explain the evidence for the protective effects of whole-grain cereals.”
[8]

Eating Whole Grains Aids Weight Loss

There is a grain of truth in the assertion that epidemic of obesity in our country is related to wheat. But the problem lies in what we generally do with wheat and other grains—we turn them into baked goods made from processed and highly refined grains, often combined with refined sugars and fats. Most Americans eat large amounts of white bread, pasta, bagels, biscuits, muffins, cakes, cookies, breakfast cereals and donuts. It’s important to realize that the health benefits of grains, including wheat, depend entirely on the form in which you eat them. In the case of wheat, these benefits are nonexistent if you choose wheat that has been processed into bleached white flour from GMO non-organic wheat berries.

People often find that when they eliminate grains, they lose weight quickly. But the weight lost is primarily water, not fat. Grains help to hold water in your cells and prevent dehydration, especially in warmer climates. For this reason, traditional diets in warmer climates tend to contain more whole-food carbohydrates, while traditional diets in the north contain less carbohydrates and more fat. When people stop eating grains (particularly refined grain products), they feel less bloated. This is mostly because they lose “water weight.” But if you eat a balanced diet with a healthy portion of whole grains, plenty of vegetables, and a small amount of protein, grains will not cause bloating. In addition, if you exercise regularly, whole grains provide a good source of energy, and the body tends to not hold onto excess fluids.

Studies show that consuming a diet high in whole grains helps to reduce weight while lowering the risk of chronic disease, according to a report published in the January 2008 issue of the American Journal of Clinical Nutrition.[9] There’s no question that switching from eating refined grains to whole grains leads to better overall health and weight control. A recent study found that increasing whole-grain intake is associated with lower visceral adipose tissue (VAT) in adults, whereas higher intakes of refined grains are associated with higher VAT.[10]  Visceral adipose tissue is linked to an increased risk of disease, including cardiovascular, cancer, and diabetes.

In a systematic review and analysis of 15 observational studies on whole grain consumption and measures of body weight and adiposity, researchers found that an increased consumption of three servings of whole grain foods per day was associated with a reduction in BMI of 0.630 kg/m2 and in waist circumference of 2.7 cm.[11] Other research shows that consuming whole grains instead of refined wheat decreases the percentage of body fat in postmenopausal women following a 12-week, energy-restricted diet.[12]  This is very good news for women, who are often dismayed to find body fat increasing as they enter menopause.

Whole Grains Reduce The Risk of Diabetes

Weight gain and the risk of diabetes often go hand-in-hand. Although there are some who advocate a very low carbohydrate diet for managing or preventing diabetes, research shows that diets high in whole-grains are associated with a 20-30% reduction in the risk of developing type-2 diabetes. This preventive benefit is attributed to a variety of wholegrain components, notably dietary fiber, vitamins, minerals and phytochemicals.[13]

The same benefits hold true for any grain. For example, a higher consumption of white rice, rather than brown rice, is associated with a significantly increased risk of type 2 diabetes.[14] Additionally, a systematic review and meta-analysis of prospective studies of grain intake and type 2 diabetes found a protective effect of intake of whole grains, but an increasedrisk for refined grains on type 2 diabetes.[15] And according to the Framingham Offspring Study, the prevalence of both insulin resistance and metabolic syndrome was 38% lower among those with the highest intake of cereal fiber from whole grains compared to those eating the least. [16]

A newer study confirmed these findings. Researchers in Europe found that a blood marker for whole-grain rye intake is associated with increased insulin sensitivity in a population with metabolic syndrome.[17] Furthermore, a Swedish study indicated that eating a breakfast rich in whole-grains maintains blood sugar at a low level for up to ten hours, which means healthy blood sugar levels until after dinner. Of the four types of grains tested, barley offered the best results, but whole-grains in bread worked better than boiled grains in porridge. The study also indicated that eating certain grains before bed affects blood sugar in the same beneficial way.[18]

More supportive evidence is found in the famous Nurses’ Health Studies I and II. At the beginning of the studies, the women did not have diabetes, cardiovascular disease, or cancer. They were followed for between 12-18 years; during this time, 6486 of the 161,737 women were diagnosed with type 2 diabetes. These women self-reported eating less whole grains than women who did not get diabetes, but they also reported taking less physical activity, having a higher body mass index, smoking more often, drinking more alcohol and soft drinks, and eating more processed meats.[19]

In an earlier Harvard Medical School / Brigham and Women’s Hospital study, which collected data on over 74,000 female nurses aged 38-63 years over a 12-year period, weight gain was inversely associated with the intake of high-fiber, whole-grain foods such as whole wheat, but positively related to the intake of refined-grain foods, such as products made from refined wheat. Not only did the women who consumed more whole grains consistently weigh less than those who ate refined foods, but those consuming the most dietary fiber from whole grains were 49% less likely to gain weight compared to those eating foods made from refined grains.[20]

Although barley is not widely eaten in the U.S., perhaps it should be. Studies show that barley has very beneficial effects on blood sugar control. Dutch researchers used a crossover study with 10 healthy men to compare the effects of cooked barley kernels and refined wheat bread on blood sugar. The men ate one or the other of these grains at dinner, and were then given a high glycemic index breakfast (50g of glucose) the next morning. Those who had eaten the barley dinner had 30% better insulin sensitivity the next morning after breakfast.[21] Japanese researchers have also found that glucose levels were lower after meals when subjects switched from white rice to barley.[22]

Scientists at the Functional Food Centre at Oxford Brookes University in England have also found barley to be beneficial: They fed healthy subjects chapatis (unleavened Indian flatbreads) made with either 0g, 2g, 4g, 6g or 8g of barley beta-glucan fiber. They found that all amounts of barley beta-glucan lowered the glycemic index of the breads, with 4g or more making a significant difference.[23]  And in the U.S., USDA scientists studied the effects of 5 different breakfast cereals on subjects’ insulin response. They found that consumption of 10g of barley beta-glucan significantly reduced insulin response.[24]  In another study, USDA researchers fed barley flakes, barley flour, rolled oats, oat flour, and glucose to overweight middle-aged women. They found that peak glucose and insulin levels after barley were significantly lower than after consumption of glucose or oats. Particle size did not appear to be a factor, as both flour and flakes had similar effects.[25]

Whole Grains Improve Cardiovascular Health

Based on an overwhelming amount of recent clinical evidence, increasing the intake of whole grains is likely to reduce the risk of cardiovascular disease.[26] [27] A number of prospective epidemiological studies have clearly shown a protective effect of whole-grain intake against myocardial infarctions. A corresponding protective effect against diabetes and ischemic stroke has also been demonstrated.[28]

The aim of one study was to determine whether including whole-grain foods in a hypocaloric (reduced by 500 kcal/d) diet enhances weight loss and improves CVD risk factors. Researchers found significantly greater decreases in CRP and percentage body fat in the abdominal region in participants consuming whole-grains than in those consuming refined grains.[29] In another study, adults with mildly high cholesterol were fed diets supplemented with one of three whole grain choices for five weeks: whole wheat/brown rice, barley, or whole wheat/brown rice/barley. All three whole grain combinations reduced blood pressure, leading USDA researchers to conclude that, “in a healthful diet, increasing whole grain foods, whether high in soluble or insoluble fiber, can reduce blood pressure and may help to control weight.”[30]

Barley appears to be especially beneficial for cardiovascular health, including lowering both blood pressure and improving lipid profiles. University of Connecticut researchers reviewed 8 studies evaluating the lipid-reducing effects of barley. They found that eating barley significantly lowered total cholesterol, LDL (“bad”) cholesterol, and triglycerides, although it did not appear to significantly alter HDL (“good”) cholesterol.[31]
 A randomized double-blind study in Japan followed 44 men with high cholesterol for twelve weeks; the men ate either a standard white-rice diet or one with a mixture of rice and high-beta-glucan pearl barley. Barley intake significantly reduced serum cholesterol and visceral fat, both accepted markers of cardiovascular risk.[32]

Another example of the benefits of barley: Twenty-five adults with mildly high cholesterol were fed whole grain foods containing 0g, 3g or 6g of barley beta-glucan per day for five weeks, with blood samples taken twice weekly. Total cholesterol and LDL (“bad”) cholesterol significantly decreased with the addition of barley to the diet.[33]

And in a study at the University of California, researchers fed healthy volunteers two test meals, both containing beta-glucan. One meal was high-fiber (15.7g) barley pasta, and the other was lower-fiber (5.0g) wheat pasta. The barley pasta blunted insulin response, and four hours after the meal, barley-eaters had significantly lower cholesterol than wheat-eaters.[34]

Whole Grains Protect Against Cancer

Whole-grains are rich sources of bioactive protein and peptides, already documented as imparting several physiological functions, including antioxidant, immunomodulatory, chemopreventive and anti-cancer functions.[35]  Research suggests that the protective effects of whole grain foods are due to the synergetic effects of the different types of dietary fibers and multiple micronutrients and phytochemicals present as compared with refined grains.[36] Some of these important compounds with demonstrated cancer, cardiovascular disease, and neurodegenerative disease preventive effects include various peptides, beta glucans, alkylresorcinols, arabinoxylans, tocotrienols, phytosterols, gamma orozanol, and magnesium.[37] [38] [39]

A key protective nutrient found abundantly in grains is magnesium, which plays a central role in many essential cellular processes such as intermediary metabolism, DNA replication and repair, transporting potassium and calcium ions, cell proliferation, and signaling transduction. Dietary sources highest in magnesium are whole grains, nuts, seeds, white potatoes, spinach and cocoa; the richest concentration of magnesium is found in the bran contained in whole grains.[40]

The fiber component of whole grains also provides protection from cancer. Based on a meta-analysis that included a large number of studies, more than 14,500 cases, and almost two million participants, the intake of whole grains is associated with linear decreases in the risk of colorectal cancer. Not all fiber is created equal—evidence of an association between consumption of fruit, vegetable, or legume fiber and risk of colorectal cancer was lacking.[41] Not surprisingly, the consumption of high amounts of red and processed meat and low intake of multiple protective phytochemicals found in fruits, vegetables, and whole grains is believed to be responsible for the high incidence of this neoplasm in the Western world.[42]

Scientists at the Danish Cancer Society Research Center collaborated on a study to investigate the link between whole grain intake and colorectal cancer. Rather than rely on whole grain intake estimation, they measured levels of alkylresorcinols (biomarkers of whole grain rye and wheat intake) in 1372 colorectal cancer patients and an equal number of controls. They found that those with the highest whole grain intake had the lowest risk of distal colon cancer, but did not find a correlation with colon cancer overall, with proximal colon cancer or with rectal cancer.[43] Another earlier meta-analysis concluded that an increment of three servings daily of whole grain foods was associated with a reduction in risk of colorectal cancer of between 11 and 17%.[44]

Whole grains offer protection from other types of cancer, as well. When researchers looked at how much fiber 35,972 participants in the UK Women’s Cohort Study ate, they found a diet rich in fiber from whole grains and fruit offered significant protection against breast cancer for pre-menopausal women.[45] Some studies show that the bran (fiber) from whole wheat (and not other grains) specifically appears to accelerate the metabolism and detoxification of serum estradiol. Estradiol is the type of estrogen most associated with breast cancer.[46]

Other studies show that rye appears to have particular benefits for protecting against breast cancer—whole grain rye contains more fiber and bioactive compounds than other cereals used for bread production. Scientists in Nordic countries (where rye is commonly eaten) have identified some of the possible mechanisms by which rye may reduce the risk of breast cancer. Rye fiber reduces the enterohepatic circulation of estrogens, leading to lower plasma estrogen concentrations. The fiber complex contains bioactive compounds such as lignans and alkylresorcinols that are antioxidative and potentially anticarcinogenic. In addition, vitamins, minerals, and phytic acid found in rye may provide protection against breast cancer.[47]

In my mind, there is no question as to the health benefits of whole grains, and hundreds of studies support these benefits. I encourage you to consider carefully the numerous healthful properties of whole grains, and to include a variety of organic grains in your diet. I know that many people are concerned about gluten and the possible negative health effects of wheat and other gluten-containing grains. As I mentioned at the beginning of this post, if you have celiac disease, you obviously must avoid gluten in all forms. However, for those who have been swayed by numerous articles in the popular press regarding “gluten sensitivity,” and as a result have eliminated grains from your diet, I encourage you to consider the following: Although wheat contains the highest amount of gluten of all grains, a recent study found that “whole wheat” can improve intestinal integrity. “Leaky gut” is now widely accepted as a contributor to many diseases. Scientists at Denmark’s National Food Institute and the Technical University of Denmark conducted a 12-week energy-restricted intervention with 70 postmenopausal women to observe the effect of a whole-wheat diet versus a refined wheat diet. Interestingly, women who ate the whole-wheat diet had significant increases in beneficial bifidobacteria, and an unexpected increase in “trans-epithelial resistance,” a measure of the permeability of the intestinal wall that shows a decrease in “leaky gut.”[48]
 My hope is that this post will put to rest any concerns about the healthfulness of whole grains in a balanced, whole foods diet.

 

[1] Margarita Ortiz-Martinez, Robert Winkler, Silverio García-Lara^, Preventive and therapeutic potential of peptides from cereals against cancer, Journal of Proteomics, Available online 13 April 2014.

[2] J Slavin J. Why whole grains are protective: biological mechanisms, Cereal Sci 2007;46:207–19.

[3] Gil A, Ortega RM, Maldonado J., Wholegrain cereals and bread: a duet of the Mediterranean diet for the prevention of chronic diseases, Public Health Nutr. 2011 Dec;14(12A):2316-22. doi: 10.1017/S1368980011002576.)

[4] McKevith B. Nutritional aspects of cereals. Nutr Bull 1011 2004;29:111–42.

[5] Bucci C1, Zingone F, Russo I, Morra I, Tortora R, Pogna N, Scalia G, Iovino P, Ciacci C. Gliadin does not induce mucosal inflammation or basophil activation in patients with nonceliac gluten sensitivity; Clin Gastroenterol Hepatol. 2013 Oct;11(10):1294-1299.e1. doi: 10.1016/j.cgh.2013.04.022. Epub 2013 Apr 30.

[6] Masters RC1, Liese AD, Haffner SM, Wagenknecht LE, Hanley AJ.)Whole and refined grain intakes are related to inflammatory protein concentrations in human plasma, J Nutr. 2010 Mar;140(3):587-94. doi: 10.3945/jn.109.116640. Epub 2010 Jan 20

[7] Hajihashemi P, Azadbakht L, Hashemipor M, Kelishadi R, Esmaillzadeh A. Whole-grain intake favorably affects markers of systemic inflammation in obese children: A randomized controlled crossover clinical trial, Mol Nutr Food Res. 2014 Jan 30. doi: 10.1002/mnfr.201300582.

[8] Neacsu et al. Bound phytophenols from ready-to-eat cereals: Comparison with other plant-based foods, Food Chemistry. 2013 Dec 1; 141(3):2880-6.

[9] Penn State. “Whole Grain Diets Lower Risk Of Chronic Disease, Study Shows.” ScienceDaily. ScienceDaily, 11 February 2008. www.sciencedaily.com/releases/2008/02/080205161231.htm

[10] McKeown NM1, Troy LM, Jacques PF, Hoffmann U, O’Donnell CJ, Fox CS. Whole- and refined-grain intakes are differentially associated with abdominal visceral and subcutaneous adiposity in healthy adults: the Framingham Heart Study, Am J Clin Nutr. 2010 Nov;92(5):1165-71. doi: 10.3945/ajcn.2009.29106.

[11] Harland J, Garton LE. Whole-grain intake as a marker of healthy body weight and adiposity. Public Health Nutr. 2007;11(6):554–63.

[12] Kristensen M1, Toubro S, Jensen MG, Ross AB, Riboldi G, Petronio M, Bügel S, Tetens I, Astrup A.Whole grain compared with refined wheat decreases the percentage of body fat following a 12-week, energy-restricted dietary intervention in postmenopausal women, J Nutr. 2012 Apr;142(4):710-6. doi: 10.3945/jn.111.142315. Epub 2012 Feb 22.

[13] Belobrajdic DP, Bird AR. The potential role of phytochemicals in wholegrain cereals for the prevention of type-2 diabetes. Nutr J. 2013 May 16;12:62. doi: 10.1186/1475-2891-12-62. Review.

[14] Hu EA1, Pan A, Malik V, Sun Q. White rice consumption and risk of type 2 diabetes: meta-analysis and systematic review, BMJ. 2012 Mar 15;344:e1454. doi: 10.1136/bmj.e1454,  Daily “dose” of white rice linked to diabetes, Harv Mens Health Watch. 2012 Jun;16(11):8.

[15] Aune D, Norat T, Romundstad P, Vatten LJ. Whole grain and refined grain consumption and the risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies, Eur J Epidemiol. 2013 Nov;28(11):845-58. doi: 10.1007/s10654-013-9852-5. Epub 2013 Oct 25.

[16] McKeown NM1, Meigs JB, Liu S, Wilson PW, Jacques PF., Whole-grain intake is favorably associated with metabolic risk factors for type 2 diabetes and cardiovascular disease in the Framingham Offspring Study, Am J Clin Nutr. 2002 Aug;76(2):390-8.

[17] Magnusdottir OK, Landberg R, Gunnarsdottir I, Cloetens L, Akesson B, Landin-Olsson M, Rosqvist F, Iggman D, Schwab U, Herzig KH, Savolainen MJ, Brader L, Hermansen K, Kolehmainen M, Poutanen K, Uusitupa M, Thorsdottir I, Risérus U. Plasma alkylresorcinols C17:0/C21:0 ratio, a biomarker of relative whole-grain rye intake, is associated to insulin sensitivity: a randomized study. Eur J Clin Nutr. 2014 Apr;68(4):453-8. doi: 10.1038/ejcn.2014.12. Epub 2014 Feb 19.

[18] Willmer, K., Grains can control blood sugar all day, new research, 06/09/2007, Nutraingredients.com.

[19] Whole grains help prevent type 2 diabetes BMJ. 2007 September 8;335(7618):473-473.

[20] S Liu, J E Manson, M J Stampfer, F B Hu, E Giovannucci, G A Colditz, C H Hennekens, and W C Willett A prospective study of whole-grain intake and risk of type 2 diabetes mellitus in US women, Am J Public Health. 2000 September; 90(9): 1409–1415.

[21] Priebe MG1, Wang H, Weening D, Schepers M, Preston T, Vonk RJ., Factors related to colonic fermentation of nondigestible carbohydrates of a previous evening meal increase tissue glucose uptake and moderate glucose-associated inflammation, American Journal of Clinical Nutrition, January 2010; 91(1):90-7.

[22] Yamanaka-Okumura H1, Taniguchi A, Sakuma M, Ushida F, Harada M., Nutrition education from the perspective of human health, Rinsho Byori. August 2009; 57(8):797-805.

[23] Nutrition Research, July 2009; 29(7):4806.

[24] Kim H, Stote KS, Behall KM, Spears K, Vinyard B, Conway JM., Glucose and insulin responses to whole grain breakfasts varying in soluble fiber, beta-glucan: a dose response study in obese women with increased risk for insulin resistance, European Journal of Nutrition, April 2009; 48(3):170-5. Epub 2009 Feb 5.

[25] Journal of the American College of Nutrition, June 2005; 24(3):182-8.

[26] Am J Clin Nutr 2007;85:1606-14, Mente A, de Koning L, Shannon HS, Anand SS. A systematic review of the evidence supporting a causal link between dietary factors and coronary heart disease. Arch Intern Med 2009;169:659-69.

[27] Park Y, Subar AF, Hollenbeck A, Schatzkin A. Dietary fiber intake and mortality in the NIH-AARP Diet and Health, Study. Arch Intern Med 2011;171:1061-8.

[28] Hallmans G, Zhang JX, Lundin E, Stattin P, Johansson A, Johansson I, Hultén K, Winkvist A, Aman P, Lenner P, Adlercreutz H. Rye, lignans and human health, Proc Nutr Soc. 2003 Feb;62(1):193-9.

[29] Katcher HI1, Legro RS, Kunselman AR, Gillies PJ, Demers LM, Bagshaw DM, Kris-Etherton PM. The effects of a whole grain-enriched hypocaloric diet on cardiovascular disease risk factors in men and women with metabolic syndrome, Am J Clin Nutr. 2008 Jan;87(1):79-90.

[30] Journal of the American Dietetic Association, September 2006; 106(9):1445-9.

[31] Annals of Family Medicine, March-April 2009; 7(2):157-63.

[32] Plant Foods and Human Nutrition, March 2008; 63(1):21-5. Epub 2007 Dec 12.

[33] American Journal of Clinical Nutrition, November 2004; 80(5):1185-93.

[34] American Journal of Clinical Nutrition, January 1999; 69(1):55-63.

[35] A. Kannan, N. Hettiarachchy, S. Narayan Colon and breast anti-cancer effects of peptide hydrolysates derived from rice bran Open Bioact Compd J, 2 (2009), pp. 17–20.

[36] Slavin J. Why whole grains are protective: biological mechanisms. Proc Nutr Soc. 2003;62:129–34.

[37] Zambrowicz A, Timmer M, Polanowski A, Lubec G, Trziszka T. Manufacturing of peptides exhibiting biological activity. Amino Acids 2013;44:315–20.

[38] De Mejia EG, Dia VP. The role of nutraceutical proteins and peptides in apoptosis, angiogenesis, and metastasis of cancer cells. Cancer Metastasis Rev 2010;29:511–28.

[39] Bartłomiej S1, Justyna RK, Ewa N., Bioactive compounds in cereal grains – occurrence, structure, technological significance and nutritional benefits – a review, Food Sci Technol Int. 2012 Dec;18(6):559-68.

[40] Blaszczyk U, Duda-Chodak A. Magnesium: its role in nutrition and carcinogenesis, Rocz Panstw Zakl Hig. 2013;64(3):165-71, Volpe SL. Magnesium in disease prevention and overall health, Adv Nutr. 2013 May 1;4(3):378S-83S. doi: 10.3945/an.112.003483.

[41] Dagfinn Aune, Doris S M Chan, Teresa Norat, Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies, BMJ 2011;343:d6617.

[42] Durko L, Malecka-Panas E. Lifestyle Modifications and Colorectal Cancer, Curr Colorectal Cancer Rep. 2014;10:45-54.

[43] Kyrø et al., Plasma Alkylresorcinols, Biomarkers of Whole-Grain Wheat and Rye Intake, and Incidence of Colorectal Cancer, Journal of the National Cancer Institute. 2013 Dec 7.

[44] Aune D, Chan DS, Lau R, Vieira R, Greenwood DC, Kampman E, et al. 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.

[45] Cade JE, Burley VJ, et al., Dietary fibre and risk of breast cancer in the UK Women’s Cohort Study International Journal of Epidemiology.

[46] D P Rose, M Goldman, J M Connolly, and L E Strong, High-fiber diet reduces serum estrogen concentrations in premenopausal women, Am J Clin Nutr September 1991 vol. 54 no. 3 520-525.

[47] Adlercreutz, Herman, Can rye intake decrease risk of human breast cancer? Food & Nutrition Research 2010. 54: 5231 – DOI: 10.3402/fnr.v54i0.5231.

[48] Christensen et al. Bifidogenic effect of whole-grain wheat during a 12-week energy-restricted dietary intervention in postmenopausal women. European Journal of Clinical Nutrition. 2013 Dec; 67(12):1316-21.