Disease Proof : Disease Proof : Health & Nutrition News & Commentary : Dr. Joel Fuhrman

What are lignans?

Plant lignans are one of the four classes of phytoestrogens (isoflavones, lignans, stilbenes, coumestans), phenolic compounds that are structurally similar to the main mammalian estrogen, estradiol.¹ Plant lignans are modified by bacteria in the human digestive tract into enteroligans. It is important to recognize the role of healthy bacteria in this process, because antibiotics can destroy beneficial bacteria in the gut resulting in long-term reduction in enteroligans.² Eating commercial meats exposes us to antibiotics, as does the overuse and inappropriate prescribing by physicians.

Which foods are good sources of plant lignans?

Flaxseeds are the richest source of plant lignans, having about 8 times the lignan content of sesame seeds [note that flaxseed oil does not contain lignans – they bind to the fiber]. The other plant foods on the list have about one-tenth or less the amount of lignans as sesame seeds per serving.^2,3 Chia seeds are also a rich source of lignans, however the exact amount is still debatable, so that number will be made available at a later date.

• Flaxseeds (85.5 mg/ounce)
• Sesame seeds (11.2 mg/ounce)⁴
• Kale (curly; 1.6 mg/cup)
• Broccoli (1.2 mg/cup)

Anti-cancer effects of lignans

Enterolignans are structurally similar to estrogen and can bind to estrogen receptors – this capability allows lignans to either have weak estrogenic activity or block the actions of estrogen in the body. For this reason, plant lignans are classified as phytoestrogens, and there has been much interest in the potential contribution of lignan-rich foods to reduced risk of hormone-related cancers.^2,5 Enterolignans inhibits aromatase⁶ and estradiol production in general, lowering serum estrogen levels.⁷ Plant lignans also increase concentration of sex hormone binding globulin, which blunts the effects of estrogens.^8-10 These benefits were documented when 48 postmenopausal women consumed 7.5 g/day of ground flax seeds for 6 weeks, then 15 g for 6 weeks – and significant decreases in estradiol, estrone, and testosterone were noted with a bigger decrease in overweight and obese women.¹¹

In a mouse model, a flaxseed diet (5%, 10%) shows dose-dependent inhibition of breast tumor growth.¹² Human trials also confirmed similar beneficial effects. A double-blinded, randomized controlled trial of dietary flaxseed demonstrated dramatic protection. Women ate either a control muffin with no flax seeds imbedded or 25g flax-containing muffin starting at time of diagnosis of breast cancer for just 32-39 days until surgery. Tumor tissue analyzed at diagnosis and surgery demonstrated surprising benefits even in this short timeframe. There was a significant apoptosis (tumor cell death) and reduced cell proliferation in the flaxseed group in just the one month.¹³ Likewise women eating more flaxseeds with a documented higher serum enterolactone were found to have a 42% reduced risk of death from postmenopausal breast cancer and a dramatic (40 percent) reduction in all causes of death.^14,15 Flaxseeds are clearly super foods; even with a mediocre diet they offer powerful protection against certain types of breast cancer. Another interesting study on flax followed women for up to 10 years and found a 51% reduced risk of all-cause mortality and a 71% reduced risk of breast cancer mortality. The intake of dried beans was also associated with a 39% reduced risk of all-cause mortality.¹⁶ Endometrial and ovarian cancer have not been as extensively studied, but the few studies that have been conducted suggest a protective effect.^2,17

Bottom line; don’t forget to take your ground flax seeds (or chia seeds) every day. I sometimes forget too, but reviewing the science encourages me to remember. When used in conjunction with dietary exposure to greens, onions, mushrooms and beans, dramatic reductions in the risk of breast cancer are possible.

My newest book, Super Immunity, addresses my full nutritional program to win the war against breast cancer.

References:
1. Mense SM, Hei TK, Ganju RK, et al: Phytoestrogens and breast cancer prevention: possible mechanisms of action. Environ Health Perspect 2008;116:426-433.
2. Higdon J: Lignans. In An Evidence-Based Approach to Dietary Phytochemicals. New York: Thieme; 2006: 155-161
3. Milder IE, Arts IC, van de Putte B, et al: Lignan contents of Dutch plant foods: a database including lariciresinol, pinoresinol, secoisolariciresinol and matairesinol. Br J Nutr 2005;93:393-402.
4. Coulman KD, Liu Z, Hum WQ, et al: Whole sesame seed is as rich a source of mammalian lignan precursors as whole flaxseed. Nutr Cancer 2005;52:156-165.
5. Adlercreutz H: Lignans and human health. Crit Rev Clin Lab Sci 2007;44:483-525.
6. Adlercreutz H, Bannwart C, Wahala K, et al: Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J Steroid Biochem Mol Biol 1993;44:147-153.
7. Brooks JD, Thompson LU: Mammalian lignans and genistein decrease the activities of aromatase and 17beta-hydroxysteroid dehydrogenase in MCF-7 cells. J Steroid Biochem Mol Biol 2005;94:461-467.
8. Adlercreutz H, Mousavi Y, Clark J, et al: Dietary phytoestrogens and cancer: in vitro and in vivo studies. J Steroid Biochem Mol Biol 1992;41:331-337.
9. Adlercreutz H, Hockerstedt K, Bannwart C, et al: Effect of dietary components, including lignans and phytoestrogens, on enterohepatic circulation and liver metabolism of estrogens and on sex hormone binding globulin (SHBG). J Steroid Biochem 1987;27:1135-1144.
10. Low YL, Dunning AM, Dowsett M, et al: Phytoestrogen exposure is associated with circulating sex hormone levels in postmenopausal women and interact with ESR1 and NR1I2 gene variants. Cancer Epidemiol Biomarkers Prev 2007;16:1009-1016.
11. Sturgeon SR, Heersink JL, Volpe SL, et al: Effect of dietary flaxseed on serum levels of estrogens and androgens in postmenopausal women. Nutr Cancer 2008;60:612-618.
12. Chen J, Power KA, Mann J, et al: Flaxseed alone or in combination with tamoxifen inhibits MCF-7 breast tumor growth in ovariectomized athymic mice with high circulating levels of estrogen. Exp Biol Med (Maywood) 2007;232:1071-1080.
13. Thompson LU, Chen JM, Li T, et al: Dietary flaxseed alters tumor biological markers in postmenopausal breast cancer. Clin Cancer Res 2005;11:3828-3835.
14. Buck K, Vrieling A, Zaineddin AK, et al: Serum enterolactone and prognosis of postmenopausal breast cancer. J Clin Oncol 2011;29:3730-3738.
15. Buck K, Zaineddin AK, Vrieling A, et al: Estimated enterolignans, lignan-rich foods, and fibre in relation to survival after postmenopausal breast cancer. Br J Cancer 2011;105:1151-1157.
16. McCann SE, Thompson LU, Nie J, et al: Dietary lignan intakes in relation to survival among women with breast cancer: the Western New York Exposures and Breast Cancer (WEB) Study. Breast Cancer Res Treat 2010;122:229-235.
17. Bandera EV, King M, Chandran U, et al: Phytoestrogen consumption from foods and supplements and epithelial ovarian cancer risk: a population-based case control study. BMC Womens Health 2011;11:40.

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“GOMBBS” is an acronym you can use to remember the most nutrient-dense, health-promoting foods on the planet.   These are the foods you should eat every day, and they should make up a significant proportion of your diet – these foods are extremely effective at preventing chronic disease and promoting health and longevity.

G – Greens

Raw leafy greens contain only about 100 calories per pound, and are packed with nutrients. Leafy greens contain substances that protect blood vessels, and are associated with reduced risk of diabetes.¹ Greens are an excellent tool for weight loss, since they can be consumed in virtually unlimited quantities. Leafy greens are also the most nutrient-dense of all foods, but unfortunately are only consumed in miniscule amounts in a typical American diet. We should follow the example of our closest living relatives – chimpanzees and gorillas – who consume tens of pounds of green leaves every day. The majority of calories in green vegetables, including leafy greens, come from protein, and this plant protein is packaged with beneficial phytochemicals: Green vegetables are rich in folate (the natural form of folic acid), calcium, and contain small amounts of omega-3 fatty acids.  Leafy greens are also rich in antioxidant pigments called carotenoids, specifically lutein and zeaxanthin, which are the carotenoids known to promote healthy vision.² Also, several leafy greens and other green vegetables (such as bok choy, broccoli, and kale) belong to the cruciferous family of vegetables.

All vegetables contain protective micronutrients and phytochemicals, but cruciferous vegetables have a unique chemical composition; they contain glucosinolates, and when their cell walls are broken by blending, chopping, or chewing, a chemical reaction converts glucosinolates to isothiocyanates (ITCs) - compounds with a variety of potent anti-cancer effects. Because different ITCs can work in different locations in the cell and on different molecules, they can have combined additive effects, working synergistically to remove carcinogens, reduce inflammation, neutralize oxidative stress, inhibit angiogenesis (the process by which tumors acquire a blood supply), and kill cancer cells.³

O – Onions

Onions, along with leeks, garlic, shallots, and scallions, make up the Allium family of vegetables, which have beneficial effects on the cardiovascular and immune systems, as well as anti-diabetic and anti-cancer effects. Allium vegetables are known for their characteristic organosulfur compounds, Similar to the ITCs in cruciferous vegetables, organosulfur compounds are released when onions are chopped, crushed, or chewed. Epidemiological studies have found that increased consumption of Allium vegetables is associated with lower risk of gastric and prostate cancers.    These compounds prevent the development of cancers by detoxifying carcinogens, halting cancer cell growth, and blocking angiogenesis.⁴ Onions also contain high concentrations of health-promoting flavonoid antioxidants, predominantly quercetin, and red onions also contain at least 25 different anthocyanins.^5,6 Quercetin slows tumor development, suppresses growth and proliferation and induces cell death in colon cancer cells.⁷ Flavonoids also have anti-inflammatory effects that may contribute to cancer prevention.⁸

M - Mushrooms

Consuming mushrooms regularly is associated with decreased risk of breast, stomach, and colorectal cancers.  In one recent Chinese study, women who ate at least 10 grams of fresh mushrooms each day (about one mushroom per day) had a 64% decreased risk of breast cancer. Even more dramatic protection was gained by women who ate 10 grams of mushrooms and drank green tea daily - an 89% decrease in risk for premenopausal women, and 82% for postmenopausal women.^9,10 White, cremini, portobello, oyster, shiitake, maitake, and reishi mushrooms all have anti-cancer properties - some are anti-inflammatory, stimulate the immune system, prevent DNA damage, slow cancer cell growth, cause programmed cancer cell death, or inhibit angiogenesis.In addition to these properties, mushrooms are unique in that they contain aromatase inhibitors - compounds that can block the production of estrogen. These compounds are thought to be largely responsible for the preventive effects of mushrooms against breast cancer - in fact, there are aromatase-inhibiting drugs on the market that are used to treat breast cancer. Regular consumption of dietary aromatase inhibitors is an excellent strategy for prevention, and it turns out that even the most commonly eaten mushrooms (white, cremini, and portobello) have high anti-aromatase activity.¹¹

B – Berries

Blueberries, strawberries, and blackberries are true super foods. Naturally sweet and juicy, berries are low in sugar and high in nutrients - they are among the best foods you can eat. Their vibrant colors mean that they are full of antioxidants, including flavonoids and antioxidant vitamins - berries are some of the highest antioxidant foods in existence. Berries’ plentiful antioxidant content confers both cardioprotective and anti-cancer effects, such as reducing blood pressure, reducing inflammation, preventing DNA damage, inhibiting tumor angiogenesis, and stimulating of the body’s own antioxidant enzymes.  Berry consumption has been linked to reduced risk of diabetes, cancers and cognitive decline.¹² Berries are an excellent food for the brain – berry consumption improves both motor coordination and memory.¹³

B - Beans

Beans (and other legumes as well) are a powerhouse of superior nutrition, and the most nutrient-dense carbohydrate source. They act as an anti-diabetes and weight-loss food because they are digested slowly, having a stabilizing effect on blood sugar, which promotes satiety and helps to prevent food cravings. Plus they contain soluble fiber, which lowers cholesterol levels.¹⁴ Beans are unique foods because of their very high levels of fiber and resistant starch, carbohydrates that are not broken down by digestive enzymes.  Fiber and resistant starch not only reduce the total number of calories absorbed from beans, but are also fermented by intestinal bacteria into fatty acids that help to prevent colon cancer. Eating beans, peas, or lentils at least twice a week has been found to decrease colon cancer risk by 50%. ^15,16 Legume intake also provides significant protection against oral, larynx, pharynx, stomach, and kidney cancers.¹⁷

S - Seeds

Nuts and seeds contain healthy fats and are rich in a spectrum of micronutrients including phytosterols, minerals, and antioxidants. Countless studies have demonstrated the cardiovascular benefits of nuts, and including nuts in the diet aids in weight maintenance and diabetes prevention.^18,19 The nutritional profiles of seeds are similar to nuts when it comes to healthy fats, minerals, and antioxidants, but seeds are also abundant in trace minerals, higher in protein than nuts, and each kind of seed is nutritionally unique. Flax, chia, and hemp seeds are extremely rich sources of omega-3 fats. In addition to the omega-3s, flaxseeds are rich in fiber and lignans. Flaxseed consumption protects against heart disease by a number of different mechanisms, and lignans, which are present in both flaxseeds and sesame seeds, have anti-cancer effects.²⁰ Sunflower seeds are especially rich in protein and minerals.  Pumpkin seeds are rich in iron and calcium and are a good source of zinc. Sesame seeds have the greatest amount of calcium of any food in the world, and provide abundant amounts of vitamin E. Also, black sesame seeds are extremely rich in antioxidants.²¹ The healthy fats in seeds and nuts also aid in the absorption of nutrients when eaten with vegetables.

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Planning in advance to eat healthfully is quite easy – but what happens when you are confronted with an immediate decision between healthy and unhealthy food – especially when you are hungry?

Here’s an example: you’re at a party where everyone is munching on chips, cheesy dips, and greasy finger foods. You see a platter of raw vegetables and fresh fruit, but you feel tempted by the junk food. Do you stick with the produce or indulge in the calorie-laden snacks?  What goes on in your brain while you’re making that decision?

Subconsciously, we assign a certain value to each food, asking ourselves, “How will each of these foods taste? How healthy is each one? What is more important to me right now, taste or healthfulness?”

Decision-making is thought to be controlled by part of the brain called the ventromedial prefrontalcortex (vmPFC), which also plays a role in regulating emotions and emotional reactions.  A 2009 study found that another region, the dorsolateral prefrontal cortex (dlPFC), may help the vmPFC to decide that healthfulness is more important when making food decisions.   In people who showed more self-control in their food choices, the vmPFC was activated by pictures of foods they had as healthy and foods they rated as tasty; however, in people with less self-control, the vmPFC was only activated by foods they rated as tasty, not the ones they rated as healthy. Also, those with more self-control had more activity in the dlPFC during food decisions.  These results suggest that the dlPFC may reduce the value that the vmPFC assigns to tempting unhealthy foods, helping us to exert self-control in our food decisions.¹

So, can we choose to activate the dlPFC to have more self-control when making food decisions?  If so, how? 

That’s exactly the question that this research group’s newest study tried to answer. Subjects were asked to fast for at least three hours prior to the experiment. They were shown pictures of 180 different foods and asked to respond within three seconds “yes” or “no” to whether they’d want to eat the food.  Before they experiment, they were told that one of their choices would be randomly selected, and if they answered “yes” for that food, it would be served to them later. 

Before each group of 10 food photos, a message would be displayed on the screen saying either "consider the healthiness," "consider the tastiness," or "make decisions naturally." These messages were designed to shift the subjects’ attention toward either taste or health – if they were reminded to think about health, would it change their brain activity and cause them to make a healthier choice?

The answer was yes. After seeing the “consider the healthiness” message, subjects were less likely to choose unhealthy foods, and more likely to choose healthy-untasty foods.  They also said “no” to foods more often after seeing the “healthiness” message than after seeing the “naturally” message.  

What was going on in the brain? In response to pictures of healthy foods, the vmPFC showed more activity in the presence of the “healthiness” message compared to the other messages.  The dlPFC was more active in response to all of the food pictures in the presence of the “healthiness” message compared to the other messages.  This result suggests that the dlPFC was more able to help the vmPFC put more value on healthiness after the “healthiness” message.   The subjects made healthier choices when they were reminded to do so.^2,3

The message here is that making the tough decisions between taste and health is easier than we think – if we can remind ourselves that health is the more important quality, we can alter the way the brain values the foods involved.  When faced with a decision between delicious healthy food and tempting unhealthy food, we can use reminders to shift our attention toward health:

• Post sticky notes in your kitchen, or on your desk at work, saying “Choose the healthiest foods” or something similar.   

• Make a sign that says “GOMBS* fight cancer in every bite.”

• When you are looking at a menu in a restaurant, or making a food choice outside of your home, remind yourself “I choose to eat healthy foods,” or “I do not eat disease-causing foods.” Write these statements on a visible card you keep in your wallet or pocketbook.

• As Dr. Fuhrman recommends, put a sign on your refrigerator that says “The salad is the main dish!” 

According to this research, reminders like these do work.  We can train ourselves (and our dlPFCs) to use healthfulness as the most important quality by which we value foods.

*GOMBS  = Greens, Onions, Mushrooms, Beans, Berries, Seeds

References:

1. Hare TA, Camerer CF, Rangel A: Self-control in decision-making involves modulation of the vmPFC valuation system. Science 2009;324:646-648.

2. Think healthy, eat healthy: Caltech scientists show link between attention and self-control. EurekAlert! http://www.eurekalert.org/pub_releases/2011-07/ciot-the072611.php. Accessed August 15, 2011.

3. Hare TA, Malmaud J, Rangel A: Focusing Attention on the Health Aspects of Foods Changes Value Signals in vmPFC and Improves Dietary Choice. J Neurosci 2011;31:11077-11087.

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Pistachio nuts have a unique nutritional profile – they are especially rich in plant sterols, carotenoids, tocopherols (vitamin E), and arginine.  Plant sterols are structurally similar to cholesterol, and provide a cholesterol-lowering benefit.¹ All nuts have cholesterol-lowering and other cardioprotective effects, but pistachios (in a tie with Mediterranean pine nuts) have the highest plant sterol content of all nuts.  Studies investigating the effects of pistachios on cardiovascular disease risk factors not only reported reduced cholesterol levels, but also decreased inflammatory markers, increased blood antioxidant levels and reduced oxidative stress.^2-4 In addition to antioxidants and plant sterols, pistachios are also rich in arginine, an amino acid that is involved in nitric oxide production, which regulates relaxation of arterial smooth muscle and therefore blood flow.  In a previous study, pistachio supplementation resulted in enhanced endothelial cell function, which means that nitric oxide availability was increased.⁴

Erectile dysfunction (ED) is primarily a disorder of penile blood flow, most often accompanied by chronic conditions that affect the vasculature, such as diabetes, hypertension, and high cholesterol. Atherosclerosis in peripheral arteries is known to contribute to the impaired blood flow in this condition.  Atherosclerosis is usually preceded by endothelial dysfunction, which decreases nitric oxide bioavailability, leading to impaired blood flow regulation.  Since pistachios have confirmed cholesterol-lowering effects and are rich in arginine (which helps to produce nitric oxide), scientists tested whether pistachios could enhance erectile function in men with ED.

Subjects in the study consumed 100 grams of pistachio nuts (about 3 ounces) each day for three weeks. Erectile function was evaluated by subjects’ reports and also by blood flow measurement with ultrasound.  After three weeks of pistachio supplementation, both the erectile function scores based on subjects’ reports and the velocity of penile blood flow were improved.  The men’s cholesterol levels also improved.⁵

The health of the heart and blood vessels is crucial to the health of the entire body.  Eating to restore cardiovascular health will improve blood flow and nutrient delivery to all tissues, improving overall health. Like several other chronic diseases, erectile dysfunction shares the same risk factors with cardiovascular disease.  Antioxidants, plant sterols, and arginine promote blood vessel health and are provided in abundance by a high nutrient diet made up of whole plant foods.

References:

1. Ellegard LH, Andersson SW, Normen AL, et al: Dietary plant sterols and cholesterol metabolism. Nutr Rev 2007;65:39-45.

2. Kay CD, Gebauer SK, West SG, et al: Pistachios increase serum antioxidants and lower serum oxidized-LDL in hypercholesterolemic adults. J Nutr 2010;140:1093-1098.

3. Kocyigit A, Koylu AA, Keles H: Effects of pistachio nuts consumption on plasma lipid profile and oxidative status in healthy volunteers. Nutrition, metabolism, and cardiovascular diseases : NMCD 2006;16:202-209.

4. Sari I, Baltaci Y, Bagci C, et al: Effect of pistachio diet on lipid parameters, endothelial function, inflammation, and oxidative status: a prospective study. Nutrition 2010;26:399-404.

5. Aldemir M, Okulu E, Neselioglu S, et al: Pistachio diet improves erectile function parameters and serum lipid profiles in patients with erectile dysfunction. Int J Impot Res 2011;23:32-38.

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When we use the word “metabolism,” we are usually referring to resting metabolic rate, which is the amount of energy (calories) that the body requires per day for its basic functions at rest.  Most people believe that it is desirable to raise their metabolism, because they will burn more calories and consequently lose weight.  Having a slightly lower resting metabolic rate is thought to predispose some individuals to weight gain, especially in the obesogenic food environment that we live in.^1,2  However,  there are unfavorable consequences to running your body at faster than normal speed, and raising your metabolism is not the key to weight loss.

Toxic byproducts of metabolism and biological aging

The chemical reactions of normal everyday physiology produce byproducts.  In particular, cellular energy production produces reactive oxygen species as a byproduct, which can damage DNA, proteins, and lipids.  Although we have natural antioxidant defenses, oxidative damage can still occur, especially if we don’t take in adequate antioxidants from our diet.³  Oxidative damage accelerates aging.

Aging here refers to biological aging – the progressive decline in the efficiency of the body’s physiological functions over time. This leads to tissue and organ damage, and increased risk of chronic disease and death. 

Why do our bodies age?  It is a combination of factors.   One, the accumulation of oxidative damage over time damages the body’s tissues, leading to accelerated aging.^4,5 And two, just the rate of living slowly wears out our cellular machinery, so if we function at a faster rate – i.e. a faster metabolism – the body will “wear out” more quickly.  In animals, energy expenditure is indeed inversely related to lifespan, supporting this.⁶   Though both these mechanisms of aging are related, as a faster metabolic rate means faster energy turnover and greater production of free radicals, leading to increased oxidative damage. 

Metabolic rate and lifespan

A study on thyroid function published last year further supported the idea that a slower metabolic rate could prolong lifespan.  Now, a new study has measured resting metabolic rate directly and come to the same conclusion.  Metabolic rate was measured by two different methods at the start of the study.  Subjects were followed for 11-15 years, and deaths from natural causes were recorded.  For each 100 calorie increase in 24-hour resting metabolic rate, the risk of natural mortality increased by 25-29%.  These results strongly support the hypothesis that a slow metabolic rate promotes longevity.⁷

Do we have any control over our resting metabolic rate? How can we slow it down?

Resting metabolic rate is largely genetically determined, but our calorie intake has an effect as well.⁸  Caloric restriction and negative energy balance have been shown to reduce resting metabolic rate, and in contrast overeating increases resting metabolic rate.^9,10  Furthermore, caloric restriction has been consistently shown to prolong maximal lifespan by up to 60% in animals.¹¹  My findings have demonstrated that an optimal micronutrient intake reduces the desire for calories and reduces body temperature and white blood cell counts. This means that if follow a high-nutrient eating style that reduces calorie intake while meeting micronutrient demands, we can reduce our resting metabolic rate and potentially increase our longevity potential dramatically.

Keep in mind that although exercise raises total calorie expenditure, it does not raise the body’s basal metabolism. Exercise is the only safe way to “raise metabolism” because it activates the peripheral tissues to utilize more calories and also increases muscle mass which in turn increases total calorie expenditure.¹²  Plus, exercise promotes longevity.¹³  

The goal here is to eat so healthy that it reduces your desire to overeat and reduces your metabolism slowly, so you can comfortably desire less food, though not get too thin.  My nutritarian recommendations actually makes you more satisfied with less food, and actually gives the ability to enjoy food more without overeating. 

So this new study supports what I have said previously: having a fast metabolism does not mean that you are healthier – in fact, it probably means that you are aging more quickly.  Instead of trying to increase your metabolism with the goal of losing weight, try to slow your metabolism with a low-calorie, high-nutrient diet for a longer, healthier life.

References:

1. Astrup A, Gotzsche PC, van de Werken K, et al: Meta-analysis of resting metabolic rate in formerly obese subjects. Am J Clin Nutr 1999;69:1117-1122.

2. Ravussin E, Lillioja S, Knowler WC, et al: Reduced rate of energy expenditure as a risk factor for body-weight gain. N Engl J Med 1988;318:467-472.

3. Joseph JA, Denisova N, Fisher D, et al: Age-related neurodegeneration and oxidative stress: putative nutritional intervention. Neurol Clin 1998;16:747-755.

4. Hulbert AJ, Pamplona R, Buffenstein R, et al: Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 2007;87:1175-1213.

5. Farooqui T, Farooqui AA: Aging: an important factor for the pathogenesis of neurodegenerative diseases. Mech Ageing Dev 2009;130:203-215.

6. Speakman JR, Selman C, McLaren JS, et al: Living fast, dying when? The link between aging and energetics. J Nutr 2002;132:1583S-1597S.

7. Jumpertz R, Hanson RL, Sievers ML, et al: Higher Energy Expenditure in Humans Predicts Natural Mortality. J Clin Endocrinol Metab 2011.

8. Bouchard C, Tremblay A, Nadeau A, et al: Genetic effect in resting and exercise metabolic rates. Metabolism 1989;38:364-370.

9. Martin CK, Heilbronn LK, de Jonge L, et al: Effect of calorie restriction on resting metabolic rate and spontaneous physical activity. Obesity 2007;15:2964-2973.

10. Roberts SB, Fuss P, Evans WJ, et al: Energy expenditure, aging and body composition. J Nutr 1993;123:474-480.

11. Fontana L: The scientific basis of caloric restriction leading to longer life. Curr Opin Gastroenterol 2009;25:144-150.

12. Broeder CE, Burrhus KA, Svanevik LS, et al: The effects of aerobic fitness on resting metabolic rate. Am J Clin Nutr 1992;55:795-801.

13. Manini TM, Everhart JE, Patel KV, et al: Daily activity energy expenditure and mortality among older adults. JAMA 2006;296:171-179.

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The cherry is a stone fruit, in the same family with plums, apricots, and peaches. The majority of edible cherries have been derived from two species: Prunus avium – the wild cherry (sweet cherries like Bing and Rainier) and Prunus cerasus – the sour cherry (like the Montromorency and Morello varieties).  Most sour cherries here in the U.S. are grown in Michigan with some growing on the East coast as well, and sweet cherries are grown primarily in the Pacific Northwest and Michigan.¹ Cherries, especially sour cherries, have a short growing season.  Sweet cherries are generally available between May to August, and sour cherries are available for just a couple of weeks either in mid-June (in warmer areas) or either July-August (in cooler areas).²

Cherries protect against oxidative stress:

Cherries range in color from yellow and pink to bright red to deep, dark red. The colors of sweet and sour cherries come from their rich supply of anthocyanins, including chlorogenic acid, quercetin, and kaempferol.^3,4 Regarding antioxidant content, cherries are some of the highest ORAC (oxygen radical absorbance capacity) foods in existence – the ORAC score of sweet cherries ranks just as high as strawberries (though not quite as high as blueberries).⁵  

Anthocyanins protect the body against oxidative damage in a number of ways: they scavenge free radicals directly, bind to DNA to protect it from oxidative damage, and activate detoxification and antioxidant enzyme systems in the body. Cherry anthocyanins have been shown to protect blood vessels and brain cells against oxidative stress, implying that cherry consumption may help to prevent atherosclerotic plaque formation and neurodegenerative diseases like dementia.^3,6 Cherry anthocyanins also slow the growth of human colon cancer cells.⁷

Cherries reduce inflammation:

Cherries and cherry juice have been used since the 1950s by sufferers of gout and arthritis to ease their symptoms.  Gout results from an overload of uric acid in the blood (hyperuricemia), which accumulates and forms crystals in the joints, causing painful arthritis; cherry consumption has been shown to reduce circulating levels of uric acid, which may be one pathway by which cherries improve gout symptoms.⁸

New evidence presented in April at the Experimental Biology 2011 meeting related the anti-inflammatory effects of tart cherry juice to both gout and heart disease.  Overweight and obese subjects consumed 8 ounces/day of tart cherry juice or placebo for 4 weeks.  Tart cherry juice consumers experienced reductions in uric acid levels and inflammation markers.  With regard to cardiovascular disease, reductions were also seen in triglycerides, VLDL, and monocyte chemoattractant protein-1 (MCP-1), a molecule involved in atherosclerotic plaque formation.⁹  Previous studies on sweet cherry consumption have similarly documented reductions in C-reactive protein (CRP), another inflammatory molecule that is also a marker of cardiovascular disease risk.¹⁰

Cherries act as a natural painkiller:

Cherry extracts inhibit the action of cyclooxygenase-1 (COX-1) and COX-2 enzymes.  These enzymes are important components of the inflammatory process and the sensation of pain. Also, these are the same enzymes that are inhibited by many common pain medications.  In fact, the COX inhibitory activity of cherry anthocyanins is comparable to that of equal concentrations of ibuprofen and naproxen.^11,12  This may be another way that cherries and cherry juice can ease symptoms of gout and arthritis, and also may help athletes to cut down on post-workout muscle pain. Distance runners training for a race who drank tart cherry juice twice daily for 8 days (7 days prior to race plus race day) experienced less post-race pain than those who drank a placebo.¹³ Similarly in strength workouts, tart cherry juice consumers experienced less pain and strength loss over the four following days compared to placebo.¹⁴ 

Cherries may help you sleep:

Tart cherries are one of the few rich food sources of the hormone and antioxidant melatonin, which regulates the sleep-wake cycle in the human brain.¹⁵  Tart cherry juice supplementation has been associated with improvements in sleep quality.¹⁶

When we think about high-antioxidant, health-promoting fruits, sometimes cherries are overlooked.  But as you can see here, cherries are an excellent food that benefits the heart, brain, and joints, and may even prevent tumor growth and improve the quality of sleep – and they will be in season very soon, so enjoy them!

References:

1. Cherry. Wikipedia. http://en.wikipedia.org/wiki/Cherry. Accessed on May 2, 2011.

2. Cherries. Aboutcom Local Foods. http://localfoods.about.com/od/summer/tp/CherriesHub.htm and http://localfoods.about.com/od/cherries/ss/cherryvarieties.htm. Accessed on May 2, 2011.

3. Kim DO, Heo HJ, Kim YJ, et al: Sweet and sour cherry phenolics and their protective effects on neuronal cells. Journal of Agricultural and Food Chemis ry 2005;53:9921-9927.

4. Phenolic compounds in sweet and sour cherries. Cornell University. http://ecsoc2.hcc.ru/ecsoc-2/dp260/dp260.htm. Accessed on May 2, 2011.

5. Oxygen Radical Absorbance Capacity of Selected Foods. 2007. US Department of Agriculture. http://www.ars.usda.gov/sp2userfiles/place/12354500/data/orac/orac07.pdf Accessed on May 2, 2011.

6. Traustadottir T, Davies SS, Stock AA, et al: Tart cherry juice decreases oxidative stress in healthy older men and women. J Nutr 2009;139:1896-1900.

7. Kang SY, Seeram NP, Nair MG, et al: Tart cherry anthocyanins inhibit tumor development in Apc(Min) mice and reduce proliferation of human colon cancer cells. Cancer Lett 2003;194:13-19.

8. Jacob RA, Spinozzi GM, Simon VA, et al: Consumption of cherries lowers plasma urate in healthy women. J Nutr 2003;133:1826-1829.

9. Martin KR, Bopp J, Burrell L, et al: The effect of 100% tart cherry juice on serum uric acid levels, biomarkers of inflammation and cardiovascular disease risk factors. In Experimental Biology 2011. Washington, D.C.: The Federation of American Societies for Experimental Biology; 2011.

10. Kelley DS, Rasooly R, Jacob RA, et al: Consumption of Bing sweet cherries lowers circulating concentrations of inflammation markers in healthy men and women. J Nutr 2006;136:981-986.

11. McCune LM, Kubota C, Stendell-Hollis NR, et al: Cherries and health: a review. Crit Rev Food Sci Nutr 2011;51:1-12.

12. Seeram NP, Momin RA, Nair MG, et al: Cyclooxygenase inhibitory and antioxidant cyanidin glycosides in cherries and berries. Phytomedicine 2001;8:362-369.

13. Kuehl KS, Perrier ET, Elliot DL, et al: Efficacy of tart cherry juice in reducing muscle pain during running: a randomized controlled trial. J Int Soc Sports Nutr 2010;7:17.

14. Connolly DA, McHugh MP, Padilla-Zakour OI, et al: Efficacy of a tart cherry juice blend in preventing the symptoms of muscle damage. Br J Sports Med 2006;40:679-683; discussion 683.

15. Burkhardt S, Tan DX, Manchester LC, et al: Detection and quantification of the antioxidant melatonin in Montmorency and Balaton tart cherries (Prunus cerasus). Journal of Agricultural and Food Chemis ry 2001;49:4898-4902.

16. Pigeon WR, Carr M, Gorman C, et al: Effects of a tart cherry juice beverage on the sleep of older adults with insomnia: a pilot study. J Med Food 2010;13:579-583.

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There are a few different classifications of fiber, and their common characteristic is resistance to digestion in the human small intestine.   Eating fiber-rich foods is associated with a number of health benefits:

• Fiber promotes weight maintenance by slowing gastric emptying; and adding volume to food, promoting satiety
• Fiber helps to prevent diabetes by slowing entrance of glucose into the bloodstream, curbing glucose (and insulin) spikes after meals
• Soluble fiber (a type of fiber abundant in oats and beans) has cholesterol-lowering effects.
• Cardiovascular health – a pooled analysis of 10 prospective studies found that an increase of 10 grams of dietary fiber per day was associated with a 24% decrease in deaths from coronary heart disease.¹
• Digestive health – fiber adds bulk and acts as a stool softener, making bowel movements faster and easier, and preventing constipation and diverticular disease.
• Fermentation of fiber and resistant starch by bacteria in the large intestine helps to prevent colorectal cancers ²

Fiber vs. fiber-rich foods: Fiber can be isolated and taken as a supplement or added to a processed food, but these are not the recommended ways to get your fiber.  Although fiber itself has beneficial properties, fiber-rich whole foods come packaged with disease-fighting phytochemicals.  There have been inconsistencies in the results of studies on fiber and colorectal cancer, probably because it appears to be high-fiber foods, not fiber alone that reduces risk. ^3-8

The American Heart Association recommends consuming 25 grams of fiber each day –a nutritarian diet far exceeds that recommendation, providing about 60-80 grams of fiber each day, since the vast majority of my recommended food pyramid is made up of fiber-rich foods like vegetables, fruits, seeds and beans.  

A study relating dietary fiber intake to lifetime risk of cardiovascular disease was presented at the American Heart Association’s Nutrition, Physical Activity, and Metabolism conference last week. Data from the 2003-2008 U.S. National Health and Nutrition Examination Surveys were analyzed. The researchers used a mathematical algorithm to predict lifetime risk for cardiovascular disease, based on diet, blood pressure, cholesterol, smoking, and history of diabetes.  All of the participants were free of cardiovascular disease at the start.  

The algorithm placed participants in groups of either high or low lifetime risk of cardiovascular disease.  Then they were arranged into four groups according to the ratio of their intake of dietary fiber to calories - dietary fiber only, no fiber supplements were included.  The lowest fiber intake was 0.1g/1000 calories, and the highest was on par with a nutritarian diet, 49.1g/1000 calories.

Individuals aged 20-39 in the highest quartile of fiber intake were almost twice as likely to be in the low risk category than those in the lowest quartile. Middle aged individuals in the highest quartile were about 50% more likely to be in the low risk category. Interestingly though, a similar association was not seen in 60-79 year olds.  The researchers theorized that many older adults with high fiber intake may have already developed significant risk for heart disease before they added more high-fiber foods to their diet.   They concluded that starting to increase fiber intake at a younger age helps to decrease the risk of cardiovascular disease later in life.^9,10

It is important to eat healthfully your entire life to get maximum benefits, however once you have not eaten properly for the first 60 years, then to get the disease-protective benefits to dramatically reduce heart attack, stroke and cancer risk from a plant-based diet (vegan or flexitarian) later in life, it is not good enough to just be good, you have to be great.  In other words, a nutritarian diet with attention to the most nutritionally powerful and protective plant foods is necessary, not just the dietary mediocrity practiced by most vegans and vegetarians.

Eating to Live is a lifetime commitment – just like it takes years for heart disease to develop, it takes years to build up protection against heart disease.  No matter what your age, you can benefit from improving your diet – but the point is, the time to start is right now and the place to start is with a nutritarian diet that pays attention to the disease-fighting nutrients in foods. Once you are past middle age, the way to start is not with some wishy-washy low fat, high fiber diet.  That is not good enough, you have to do better than that and pay attention to the micronutrient-richness of your meals and achieve comprehensive nutritional adequacy, which is the core of my message.  

References:

1. Pereira MA, O'Reilly E, Augustsson K, et al: Dietary fiber and risk of coronary heart disease: a pooled analysis of cohort studies. Arch Intern Med 2004, 164:370-376.

2. O'Keefe SJ, Ou J, Aufreiter S, et al: Products of the colonic microbiota mediate the effects of diet on colon cancer risk. J Nutr 2009, 139:2044-2048.

3. Singh PN, Fraser GE: Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 1998, 148:761-774.

4. Uchida K, Kono S, Yin G, et al: Dietary fiber, source foods and colorectal cancer risk: the Fukuoka Colorectal Cancer Study. Scand J Gastroenterol 2010, 45:1223-1231.

5. Park Y, Hunter DJ, Spiegelman D, et al: Dietary fiber intake and risk of colorectal cancer: a pooled analysis of prospective cohort studies. JAMA : the journal of the American Medical Association 2005, 294:2849-2857.

6. Michels KB, Fuchs CS, Giovannucci E, et al: Fiber intake and incidence of colorectal cancer among 76,947 women and 47,279 men. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 2005, 14:842-849.

7. Terry P, Giovannucci E, Michels KB, et al: Fruit, vegetables, dietary fiber, and risk of colorectal cancer. J Natl Cancer Inst 2001, 93:525-533.

8. Wakai K, Date C, Fukui M, et al: Dietary fiber and risk of colorectal cancer in the Japan collaborative cohort study. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 2007, 16:668-675.

9. Northwestern University (2011, March 23). Load up on fiber now, avoid heart disease later. . In ScienceDaily; 2011.

10. Ning H, Van Horn L, Shay CM, et al: Dietary Fiber Intake and Long Term Cardiovascular Risk: Findings from the National Health and Nutrition Examination Surveys (NHANES) 2003-2008. In American Heart Association: Nutrition, Physical Activity, and Metabolism 2011.

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Over 5,000 different flavonoid antioxidants have been identified, many of these in commonly consumed plant foods – there are many different types of flavonoids:

• Flavanols are the most common, and are abundant in onions, kale, leeks, broccoli, apples, blueberries, red wine, and tea.
• Less common are the flavones, which are found in celery and parsley.
• Citrus fruits have high levels of flavanones.
• Flavan-3-ols, which include catechins, are found in grapes, tea, and cocoa.
• Soybeans contain isoflavones.
• Anthocyanins (derivatives of anthocyanidins) are potent antioxidants and pigments that color red, blue, and purple foods like berries, grapes, currants, blood oranges, eggplant, red cabbage, red onions, and some beans and grains.¹

In addition to their antioxidant capacity, flavonoids may help the ability of the muscle layer of blood vessels to relax (vasodilation). Endothelial cells, which make up the inner layer of blood vessels, produce nitric oxide in order to regulate blood pressure. There is evidence that flavonoids increase the activity of the enzyme (eNOS; endothelial nitric oxide synthase) in endothelial cells necessary for nitric oxide production.² In agreement with the idea that flavonoids have beneficial effects on blood pressure, a meta-analysis of 15 studies concluded that regular cocoa consumption can reduce blood pressure in hypertensive and pre-hypertensive individuals.³

A new study focuses on the anthocyanins in berries and their effects on blood pressure. Men and women from the Health Professionals Follow-Up Study and Nurses’ Health study, respectively were followed for 14 years, and their flavonoid intake was calculated based on the foods they reported eating. Reduced risk for hypertension was found for high intake of anthocyanins (an 8% decrease in risk), as well as apigenin (a flavone) and catechin (a flavan-3-ol). The foods that contributed the bulk of the anthocyanin in the diets of the subjects were blueberries and strawberries.

When the researchers analyzed blueberry consumption specifically they found that compared with those who ate no blueberries, those who ate one serving per week decreased their risk of hypertension by 10%. ^4,5

If there was a 10% decrease in hypertension risk for one serving of blueberries per week, imagine how protective it would be to eat one serving of berries every day! Also flavonoids act in several other ways to protect against heart disease, for example by reducing inflammation, LDL oxidation, and platelet aggregation. ^1,6 As a result of these effects, several prospective studies have found associations between high flavonoid intake and considerable reductions (up to 45%) in the risk of coronary heart disease.^7-10 Flavonoids also have documented anti-cancer properties.^11,12

Berries truly are superfoods – they are low in sugar, and high in fiber and phytochemicals, with the highest nutrient to calorie ratio of all fruits. Eating berries daily will not only promote vasodilation, but also provide the body with protection against free radicals, inflammation, and cancer.

References:

1. Erdman JW, Jr., Balentine D, Arab L, et al: Flavonoids and heart health: proceedings of the ILSI North America Flavonoids Workshop, May 31-June 1, 2005, Washington, DC. The Journal of nutrition 2007, 137:718S-737S.
2. Galleano M, Pechanova O, Fraga CG: Hypertension, nitric oxide, oxidants, and dietary plant polyphenols. Current pharmaceutical biotechnology 2010, 11:837-848.
3. Ried K, Sullivan T, Fakler P, et al: Does chocolate reduce blood pressure? A meta-analysis. BMC medicine 2010, 8:39.
4. Cassidy A, O'Reilly EJ, Kay C, et al: Habitual intake of flavonoid subclasses and incident hypertension in adults. The American journal of clinical nutrition 2011, 93:338-347.
5. Bioactive Compounds in Berries Can Reduce High Blood Pressure. In ScienceDaily; 2011.
6. Chong MF, Macdonald R, Lovegrove JA: Fruit polyphenols and CVD risk: a review of human intervention studies. The British journal of nutrition 2010, 104 Suppl 3:S28-39.
7. Huxley RR, Neil HA: The relation between dietary flavonol intake and coronary heart disease mortality: a meta-analysis of prospective cohort studies. Eur J Clin Nutr 2003, 57:904-908.
8. Knekt P, Kumpulainen J, Jarvinen R, et al: Flavonoid intake and risk of chronic diseases. The American journal of clinical nutrition 2002, 76:560-568.
9. Mursu J, Voutilainen S, Nurmi T, et al: Flavonoid intake and the risk of ischaemic stroke and CVD mortality in middle-aged Finnish men: the Kuopio Ischaemic Heart Disease Risk Factor Study. The British journal of nutrition 2008, 100:890-895.
10. Mink PJ, Scrafford CG, Barraj LM, et al: Flavonoid intake and cardiovascular disease mortality: a prospective study in postmenopausal women. The American journal of clinical nutrition 2007, 85:895-909.
11. Androutsopoulos VP, Papakyriakou A, Vourloumis D, et al: Dietary flavonoids in cancer therapy and prevention: substrates and inhibitors of cytochrome P450 CYP1 enzymes. Pharmacol Ther 2010, 126:9-20.
12. Ramos S: Effects of dietary flavonoids on apoptotic pathways related to cancer chemoprevention. The Journal of nutritional biochemistry 2007, 18:427-442.

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The leading cause of death for male gorillas in zoos is heart disease. Sadly, animals that live in close contact with (and fed by) humans end up with human chronic diseases.

Gorillas are the largest of the primates, and they are one of the four species of great apes (great apes make up the Hominidae superfamily, which includes chimpanzees, bonobos, orangutans, and gorillas).  Following chimpanzees, gorillas are the closest living relatives to humans, differing in only about 3% of our genetic makeup.

Gorillas are herbivores that live in the forests of central Africa, where they can eat up to 50 pounds of vegetation each day, mostly leaves and fruit. Although most gorillas have a preference for fruit, they also eat large amounts of leaves, plus herbs and bamboo, and occasionally insects. In the wild, gorillas spend most of their day foraging and eating.¹

In the wild, gorillas eat an extremely high fiber diet, and derive a significant proportion of caloric energy from the fermentation of fiber by bacteria in the colon, producing short-chain fatty acids. The approximate proportions of macronutrients in a wild gorilla’s diet is 2.5% of calories from fat, 24.3% from protein, 15.8% (non-fiber) carbohydrate, and up to 57.3% from short chain fatty acids derived from bacterial fermentation of fiber.²

In contrast, the standard diet for gorillas in captivity is usually not made up of natural leaves, herbs, and fruits – it is a diet of nutrient-fortified, high-sugar, high-starch processed food.

This unnatural diet has contributed to signs of heart disease and enlarged hearts for both of the male gorillas at the Cleveland Metropark Zoo. Researchers at the zoo and at Case Western University decided to change the gorillas’ diet, bringing it closer to what it would have been in the wild.

Since late 2009, the two gorillas have been eating endive, dandelion greens, romaine lettuce, green beans, alfalfa, apples, and bananas. Each of them eats about ten pounds of vegetables each day. The gorillas also spend more time eating (50-60% of their day rather than 25%), which is similar to wild foraging behavior.  After one year on their new diet, each gorilla has lost about 65 pounds, their health is improving and the researchers are noting and documenting their decrease in heart disease risks.³

My question is: why were they feeding processed foods to gorillas instead of their natural food diet in the first place?

Heart disease and heart attacks are just as unnatural for a gorilla as they are for humans.   I guess it is pretty low for the zookeepers to be feeding a gorilla a processed food diet for convenience that will expedite its death. How could they not know that gorillas should eat a natural diet?   But how did our society develop the universal eating cult that permits and encourages the feeding of disease-causing fast food, processed food and junk food to human kids, damaging their future health potential? I guess maintaining our food addictions to processed foods are a more powerful drive than our desire to have our children be healthy.   Maybe humans should not be in charge of feeding humans or animals? Maybe we should hire the gorillas to raise our children? Did you ever watch the Planet of the Apes? Okay, so maybe that wasn’t such a good idea. 

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 by Natalie Obermeyer

Vegetables consist of less than 2% of American children’s diets, and the CDC predicts that for the first time in history the current generation of children will have a shorter lifespan than their parents.^1,2

Jennifer Taylor and Theresa Roden of the Wellness Foundation are aiming to improve the health of children and their families by inspiring them to eat nutrient rich diets. Students learn the how they can prevent diseases such as heart disease and diabetes and live long, healthy lives through what they eat. In each class students learn a lesson about a specific topic such as the benefits of the phytonutrients in vegetables, the “not so sweet truth” about sugar, and the benefits of eating a plant-based diet. Then, students get to prepare and eat their own nutrient-rich foods including green smoothies, fruit salad with cashew cream, and avocado bean dip. The children love the fun, interactive class and discovering many new healthy foods.

“We have a choice and I choose to be a healthy kid. Thank you Food for Life!”– Luis, student

“I never thought eating healthy and learning about nutrition could be so much fun. I do not want to have heart disease or type 2 diabetes when I grow up, so I pledge to lead a healthier life. This program has really changed my life.” – Ben, student

Food for Life has dramatically impacted the entire families of its participants. Students are encouraged to invite their parents and even grandparents to attend the classes, and students beg their parents to attend. Parents join the classes over their lunch hour, and it is not uncommon for the class to have almost 100% parent participation. With the whole family learning together, the nutrition students learn in school can be implemented at home as well. Parents themselves are experiencing the benefits, and many no longer need insulin or other drugs.

Food for Life is now expanding its program to other schools and is in the process of creating a curriculum for pre-school and 3^rd graders. Eventually they plan to provide the program for pre-school, kindergarten, third, sixth, ninth and twelfth graders. They want to empower as many students as possible to take control of their health by developing habits that will last a lifetime.

Children can learn to love healthy food, and the Food for Life program is proof of this. Well done, Wellness Foundation, for exposing children to nutritional knowledge and healthy cooking!

References:

¹Fox MK, Pac S, Devaney B, Jankowski L. Feeding infants and toddlers study: What foods are infants and toddlers eating? L Am Diet Assoc 2004;104(1 Suppl):s22-s30

²Olshansky SJ, Passaro DJ, Hershow RC, Layden J, Carnes BA, Brody J, Hayflick L, Butler RN, Allison DB, Ludwig DS. A potential decline in life expectancy in the United States in the 21st century. N Engl J Med. 2005 Mar 17;352(11):1138-45. PubMed PMID: 15784668.

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