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Nutrition Concerns and Health Effects of Vegetarian Diets: Winston John Craig, PHD, RD

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Nutrition Concerns and Health Effects of Vegetarian Diets: Winston John Craig, PHD, RD

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Sarbu Andra
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© © All Rights Reserved
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Nutrition in Clinical Practice

Invited Review Volume 25 Number 6


December 2010 613-620

Nutrition Concerns and Health Effects © 2010 American Society for


Parenteral and Enteral Nutrition

of Vegetarian Diets
10.1177/0884533610385707
http://ncp.sagepub.com
hosted at
http://online.sagepub.com

Winston John Craig, PhD, RD


Financial disclosure: none declared.

Vegetarians exhibit a wide diversity of dietary practices, often This is achieved by an increased consumption of fruits, vegeta-
described by what is omitted from their diet. When a vegetarian bles, whole-grains, legumes, nuts, and various soy products. As
diet is appropriately planned and includes fortified foods, it can a result of these factors, vegetarians typically have lower body
be nutritionally adequate for adults and children and can pro- mass index, serum total and low-density lipoprotein cholesterol
mote health and lower the risk of major chronic diseases. The levels, and blood pressure; reduced rates of death from ischemic
nutrients of concern in the diet of vegetarians include vitamin heart disease; and decreased incidence of hypertension, stroke,
B12, vitamin D, ω-3 fatty acids, calcium, iron, and zinc. Although type 2 diabetes, and certain cancers than do nonvegetarians.
a vegetarian diet can meet current recommendations for all of (Nutr Clin Pract. 2010;25:613-620)
these nutrients, the use of supplements and fortified foods pro-
vides a useful shield against deficiency. A vegetarian diet usually Keywords:   vegetarian; cancer; cardiovascular disease; vegan;
provides a low intake of saturated fat and cholesterol and a high vitamin B12; vitamin D; osteoporosis; calcium; ω-3; diabetes;
intake of dietary fiber and many health-promoting phytochemicals. research and diseases

C
onsumers are increasingly showing interest in foods, especially fortified foods. A vegetarian diet that
reduced-calorie vegetarian meals. In addition, uses primarily olive oil as the source of fat, and minimal
there has been a proliferation of Web sites and amounts of dairy and eggs, can be considered nutrition-
cookbooks dealing with vegetarian issues. Veggie burgers ally similar to a Mediterranean-style diet, which is widely
and other vegetarian options are available in fast-food considered to be health promoting.
restaurants and university foodservice facilities. The pop- The U.S. market for processed vegetarian foods (such
ularity of vegetarian diets in recent years is fueled by as meat analogs, vegetarian burgers, nondairy milks, and
ethical considerations, health concerns, environmental vegetarian entrees) has grown significantly during the
issues, and religious factors. The reason a person chooses past decade. The ready availability of fortified vegetarian
to be a vegetarian will influence the pattern of foods cho- foods (such as soymilks and meat analogs) is expected to
sen. A true vegetarian eliminates all flesh foods from the have a significant impact on the nutrient intake of vege-
diet, including fish and chicken, and typically bases the tarians. These foods, along with fortified juices and
diet on fruits and vegetables, grains (preferably whole breakfast cereals, can add substantially to a vegetarian’s
grains), legumes, and nuts. Some vegetarian diets empha- intake of calcium, iron, zinc, vitamin B12, vitamin D, and
size raw foods. Lacto-ovo-vegetarians permit dairy and/or ω-3 fatty acids.
egg products. A vegan (or total vegetarian) consumes only This review discusses the nutrients of major concern
plant foods. Even within these broad categories, one in a vegetarian diet along with the health benefits obtained
observes a wide diversity of dietary practices. This diver- from following a vegetarian diet. A comparison is also
sity of eating patterns makes it difficult to find clear rela- made between the 2 forms of vegetarian diets most com-
tionships among the diet, nutrition status, and health monly practiced in North America—a lacto-ovo-vegetarian
profile. The nutrition adequacy of a particular plant- diet and a vegan diet. The health effects of vegetarian
based diet will depend upon the appropriateness of food diets have been discussed elsewhere.1,2
choices, which are often determined by the nutrition
knowledge of the individual and the availability of certain
Nutrition Concerns
From Andrews University, Nutrition and Wellness, Berrien
Springs, Michigan.
Vitamin D
Address correspondence to: Andrews University, Nutrition and
Wellness, 8475 University Blvd, Berrien Springs, MI 49104- In addition to being important for the maintenance of
0210; e-mail: [email protected]. bone health, vitamin D plays an important role in immune

613
614   Nutrition in Clinical Practice / Vol. 25, No. 6, December 2010

Table 1.   Mean Intakes of Selected Vitamins and Minerals and Linolenic Acid (ω-3)
Among Vegetarians and Nonvegetariansa

Nutrient Dietary Group Male Female n Years of Publications DRI for Maleb DRI for Femaleb

Calcium, mg NV 946 898 10 1997-2003 1000 1000


LOV 906 875
VG 755 622
Iron, mg NV 15.1 11.3 10 1997-2003 8 18
LOV 17.6 14.7
VG 20.4 17.8
Zinc, mg NV 12.2 10.1  9 1997-2003 11 8
LOV 10.3 8.5
VG 11.0 9.0
Vitamin D, mcg NV 3.4 3.6  8 1989-2003 5 5
LOV 2.0 2.1
VG 1.0 0.8
Vitamin B12, mcg NV 7.3 5.4 10 1991-2003 2.4 2.4
LOV 2.7 2.1
VG 1.0 1.0
18:3 ω-3, mg NV 1.5 1.2  4 1984-1999 1.6 1.1
VG 2.0 1.6
VG 1.9 1.4
DRI, Dietary Reference Intake; LOV, lacto-ovo-vegetarian; NV, nonvegetarian; VG, vegan.
a
Data from reference 6.
b
DRIs are for 19-50 years of age. For iron, calcium and vitamin D values will be different for adults over 50 years of age.

function, the reduction of inflammation, and reducing cereals; and margarines. Substantial levels of vitamin D2
the risk of chronic diseases. Vitamin D insufficiency has (400 international units per 3 oz of mushroom) may be
been linked to a wide variety of diseases including type I obtained from mushrooms that have been exposed to
diabetes, multiple sclerosis, rheumatoid arthritis, colorec- ultraviolet light under controlled conditions. Intake of
tal cancer, heart disease, and infectious diseases.3 Many vitamin D by vegans tends to be substantially below that
genes encoding proteins regulating cell proliferation, dif- of lacto-ovo-vegetarians and nonvegetarians (see Table 1).
ferentiation, and apoptosis are modulated in part by vita- Both vitamin D2 (ergocalciferol, produced from yeast)
min D. Adequate vitamin D intake is essential since all and, more commonly, vitamin D3 (cholecalciferol, derived
tissues in the body have a vitamin D receptor and respond from lanolin) are used in supplements and to fortify
to the active form 1,25-dihydroxyvitamin D.3 Because foods. Vitamin D2 (which contains a double bond at C22
cutaneous production of vitamin D3 is not adequate in its side chain, a feature that is lacking in the side chain
(especially in heavy sunscreen users and the elderly) to of D3) appears to be as effective as vitamin D3 in main-
meet nutrition needs in most parts of North America taining serum 25-hydroxyvitamin D levels.8
(north of latitude 35°N) during the winter months, a food
source or vitamin D supplement is necessary. A circulat-
Vitamin B12
ing level of 25-hydroxyvitamin D of >37.5 nmol/L is con-
sidered an indication of adequate vitamin D status, but a Because of inadequate consumption, the vitamin B12 sta-
higher level (>75 nmol/L) has been suggested by some to tus of some vegetarians is less than adequate6,9 Although
maximize the beneficial effect of vitamin D upon our dairy and eggs are good sources of vitamin B12 for the
health. In the absence of adequate sun exposure, about lacto-ovo-vegetarian, vegans must obtain their vitamin B12
1000 international units of vitamin D per day may be either from a regular use of vitamin B12-fortified foods,
needed to achieve this level,4 a value substantially higher such as fortified soy and rice beverages, some breakfast
than the current dietary reference intake (DRI). Low vita- cereals, meat analogs, and Red Star Vegetarian Support
min D intakes,5 low serum 25-hydroxyvitamin D levels,6 Formula nutrition yeast, or from a daily vitamin B12 sup-
and reduced bone mass7 have been reported in some plement. Unfortified plant foods (such as seaweeds) do
vegan groups who did not take vitamin D supplements or not contain any significant amount of active vitamin B12.
ingest fortified foods such as cow’s milk; yogurt; some If folic acid intake is high, hematological symptoms of
brands of soymilk, rice milk, and orange juice; breakfast vitamin B12 deficiency may be masked and go undetected
Health Effects of Vegetarian Diets / Craig   615

until neurological symptoms are manifested.9 Vitamin B12 considerably reduced by oxalates (spinach, Swiss chard)
status is commonly determined by measuring serum lev- and phytates (nuts, whole grains).
els of methylmalonic acid, or homocysteine. Adequate
vitamin B12 intake is especially important during preg-
Iron
nancy and lactation. The intake of vitamin B12 by vegans
typically falls below the DRI (see Table 1). Vegetarians often have an iron intake that is similar to or
slightly better than that of nonvegetarians (see Table 1),
so the issue of iron adequacy is really one of iron bioavail-
ω-3 (n-3) Fatty Acids
ability. Incidence of iron-deficiency anemia is common
The long-chain ω-3 fatty acids are important for cardio- among vegetarians and nonvegetarians alike.6 Although
vascular health, infant visual function, and neurodevelop- vegetarian adults have lower iron stores than nonvegetar-
ment. Compared with nonvegetarians, vegetarians (and ians, their serum ferritin levels are usually within the
particularly vegans) tend to have lower blood levels of the normal range.15 Nonheme iron is sensitive to both inhibi-
long-chain ω-3 fatty acids, eicosapentaenoic acid (EPA), ters and enhancers of iron absorption. Inhibitors of iron
and docosahexaenoic acid (DHA).10 Chickens fed ω-3 in absorption include phytates, calcium, and the polypheno-
their diet produce eggs containing some EPA and DHA. lics in tea, coffee, herb teas, and cocoa. Vitamin C and
For the vegan, certain microalgae are a good source of other organic acids found in fruits and vegetables sub-
DHA, and the oil from brown algae (kelp) is a source of stantially enhance nonheme iron absorption and reduce
EPA. Rich sources of α-linolenic acid (ALA), the precur- the inhibitory effects of phytate.16 Soaking and sprouting
sor of EPA and DHA, include flaxseed, walnuts, canola beans and grains as well as leavening of bread can dimin-
oil, chia seed, and soy. However, the bioconversion of ish phytate levels and enhance iron absorption. Whereas
ALA to EPA is generally less than 10% in humans, many studies of iron absorption have been short term,
whereas the conversion of ALA to DHA is substantially there is evidence that long-term adaptation does occur,
less.11 The conversion varies with individuals, and women involving both increased absorption and decreased
are known to have a higher ALA conversion efficiency losses.17
than men. Those with increased requirements of ω-3,
such as pregnant and lactating women, may benefit from
Zinc
DHA-fortified foods (some breakfast bars and soymilk)
and microalgae-derived DHA supplements, which are Although overt zinc deficiency has not been seen in
well absorbed and positively influence blood levels of Western vegetarians, their zinc intakes may be marginal
DHA, and also EPA through retroconversion.12 or fall below recommendations (see Table 1). In addition,
zinc bioavailability from vegetarian diets is lower than
from nonvegetarian diets, mainly due to their higher
Calcium
phytic acid content.18 With vegetarians consuming diets
Calcium intakes of lacto-vegetarians are similar to, or rich in unrefined grains, nuts, and legumes, their zinc
may be higher than, those of nonvegetarians, whereas requirements may exceed the RDA. Due to limitations in
intakes of vegans tend to be lower than both groups and evaluation of marginal zinc status, it is not possible to
may fall below recommended intakes6 (see also Table 1). determine the possible effect of lower zinc intake by veg-
Vegans generally require calcium-fortified foods such as etarians.18 Organic acids, such as citric acid, and food
fruit juices, soy and rice milk, and breakfast cereals to preparation techniques, such as soaking and sprouting
meet their calcium needs. The use of herbal seasonings beans, grains, and seeds as well as leavening bread, can
rather than salt will diminish the urinary calcium losses increase zinc bioavailability.19
associated with a high-sodium intake. Fruits and vegeta-
bles, rich in potassium and magnesium, will produce a
high renal alkaline load, which offsets the calciuric effect Health Effects
of a high renal acid load associated with a diet rich in
meat, dairy products, and grains. Greens that are low in Cardiovascular Disease
oxalates (bok choy, broccoli, Chinese cabbage, and col-
lards) and fruit juices fortified with calcium citrate malate Compared with nonvegetarians, vegetarians (both lacto-
are good sources of highly bioavailable calcium (50%-60% ovo vegetarians and vegans) have a lower risk of death
for the greens; 40%-50% for the juices), whereas calcium- from ischemic heart disease, even after adjustment for
set tofu, cow’s milk, and soy milk fortified with calcium body mass index (BMI) and smoking habits.20-22 A partial
carbonate have good bioavailability of calcium (30%- explanation for the reduced mortality risk may be the
35%); calcium in sesame seeds, almonds, and dried beans lower blood lipid levels typically seen in vegetarians.
has about a 25% bioavailability.13,14 Calcium absorption is Based on blood lipid data in one large cohort study, the
616   Nutrition in Clinical Practice / Vol. 25, No. 6, December 2010

incidence of ischemic heart disease was estimated to be with vegetarians. However, meat and processed meat
24% lower in lifelong vegetarians and 57% lower in life- intake alone was found to be an important risk factor for
long vegans compared with omnivores.20 When subjects diabetes even after adjustment for BMI.39 In the Women’s
switch from their usual diet to a vegetarian diet, they Health Study, the authors observed positive associations
typically experience a reduction in serum total and low- between intakes of red meat and processed meat and risk
density lipoprotein (LDL) cholesterol levels. of diabetes after adjusting for BMI, total energy intake,
Factors in a vegetarian diet that convey a beneficial and exercise. An increased risk of diabetes was most pro-
effect on blood lipid levels include vegetable oils, soluble nounced for frequent consumption of processed meats
fiber, nuts, soy, and plant sterols.6,23,24 The consumption such as bacon and hot dogs.40 In another large study, the
of fruits and vegetables,25 whole grains,26 soy protein,27 relative risk for type 2 diabetes in women was increased
and nuts23 may also lower the risk of cardiovascular dis- 26% for red meat and 38% to 73% for processed meats for
ease (CVD) by factors other than the lowering of blood every serving of the meat added.41
lipid levels. Vegetarians also consume higher levels of Higher intakes of plant foods, such as vegetables,
flavonoids and other phytochemicals than do omnivores. whole grain foods, legumes, and nuts, but not fruit juice,
These antioxidants provide beneficial cardiovascular pro- have been associated with a substantially lower risk of
tection, by reducing platelet aggregation and blood clot- insulin resistance and type 2 diabetes and improved glyc-
ting, acting as anti-inflammatory agents, and improving emic control in either normal or insulin-resistant indi-
vascular endothelial function.28,29 Conservative vegetarian viduals.42-45 People consuming about 3 servings per day of
diets have been used to successfully manage CVD risk whole grain foods are 20% to 30% less likely to develop
factors.30 A near-vegan diet high in soy protein, soluble type 2 diabetes than those who consume few whole grain
fiber, nuts, and phytosterols was shown to be as effective foods (<3 servings per week).44 In the Nurses’ Health
as a low-saturated fat diet plus a statin drug for lowering Study, nut consumption was inversely associated with risk
serum LDL cholesterol levels.31 of type 2 diabetes after adjustment for BMI, physical
Vegetarians have a lower rate of hypertension than do activity, and other factors. The risk of developing diabetes
omnivores.20,21 Preliminary results from the Adventist mellitus for those consuming nuts 5 or more times a week
Health Study-2 cohort confirm the protective effect of a was 27% lower than those almost never eating nuts.42
vegetarian diet, with vegans appearing to have an even In a large prospective study of Chinese women, the
lower rate of hypertension than other vegetarians.18 Some risk of type 2 diabetes mellitus was 38% and 47% lower
studies, but not all, report lower blood pressure levels in for those consuming a high intake of total legumes and
vegetarians compared with omnivores.20,32 This observa- soybeans, respectively, compared with a low intake,43 after
tion may be due in part to the lower BMI seen in vegetar- adjustment for BMI and other factors. Legumes contain
ians.22 Lower blood pressure levels may also result from slow-release carbohydrate and are rich in soluble fiber,
the potassium, magnesium, antioxidants, dietary fat, and factors known to improve glycemic control.
fiber found in vegetarian diets.33 Fruit and vegetable A low-fat, fiber-rich vegan diet with a low to modest
intake was responsible for about one half of the blood glycemic load considerably improved glycemic control in
pressure reduction of the DASH (Dietary Approaches to persons with type 2 diabetes mellitus, with 43% of the
Stop Hypertension) study.34 subjects reducing diabetes medication after 5 months.46
In this study, decreases in serum HbA1C levels correlated
strongly with decreases in body weight.
Obesity
BMI values are reported to be higher in nonvegetarians
Cancer
compared with vegetarians for both men and women, and
BMI values tend to increase as the frequency of meat Vegetarians tend to have an overall lower cancer rate than
consumption increases.21,35 Among vegetarians, vegans have does the general population. Although obesity is a signifi-
the lowest BMI values of all vegetarians.36 It appears that cant risk factor for cancer at a number of sites,47 the
one must follow a vegetarian diet for about 5 years before lower BMI of vegetarians may explain some of the lower
its benefits are seen.37 Weight management appears to be cancer risk in vegetarians compared with nonvegetarians.
more effective when subjects choose a vegetarian diet or Data from the Adventist Health Study revealed that veg-
one containing fewer animal foods.38 etarians had a significantly lower risk for both colorectal
and prostate cancer compared with nonvegetarians,
whereas there were no significant differences in risk of
Diabetes
other cancers after controlling for age, gender, and smok-
Vegetarians have significantly lower rates of developing ing.21 In the UK Women’s Cohort Study, data suggested
type 2 diabetes than do omnivores.21,36 This may be partly that vegetarian women have a lower risk of breast cancer
explained by the greater BMI of omnivores compared than meat eaters.48 Within the EPIC-Oxford Study, the
Health Effects of Vegetarian Diets / Craig   617

incidence of all cancers combined was lower among veg- and synergistic effects.58 However, human population
etarians than among nonvegetarians, whereas the inci- studies have not shown large differences in cancer inci-
dence of colorectal cancer was unexpectedly higher in dence or mortality rates between vegetarians and nonveg-
vegetarians than in nonvegetarians.49 etarians.22,50,59 Perhaps more detailed food consumption
Although overall cancer rates of vegetarians are mod- and food preparation data are needed as well as data on
estly lower than those of nonvegetarians living in the the bioavailability of phytochemicals.
same communities, the data for specific cancers appear to Consumption of red meat and processed meat is con-
be less convincing.50 Fraser50 has suggested that the term sistently associated with an increase in the risk of color-
vegetarian may be too broad a descriptor since it refers to ectal cancer.47 Grilled, cured, and smoked meats and fish
the absence of meat in the diet while allowing for a large are associated with an increased risk of cancer due to the
variety of different intakes from all the other food groups. presence of polycyclic aromatic hydrocarbons and hetero-
Since these other foods may influence risk of cancer and cyclic amines produced during their preparation.47 Meat
may comprise the majority of total caloric intake, they consumption has also been linked in some studies with an
may confound analyses evaluating effects that use a sim- increased risk of breast cancer.60 In a study in southern
ple definition of a vegetarian diet.50 France, breast cancer risk increased by more than 50%
Epidemiological studies have consistently shown that for each additional 100 g/d of meat consumed.61
regular consumption of plant foods, such as fruit and
vegetables, is strongly associated with a reduced risk of
Osteoporosis
cancer.28,51 Fruit, vegetables, whole grains, and legumes
contain a complex mixture of phytochemicals possessing Cross-sectional and longitudinal population-based stud-
potent antioxidant, antiproliferative, and cancer-protective ies suggest no differences in bone mineral density (BMD),
activity.47 for both trabecular and cortical bone, between omnivores
Fruit and vegetables, rich in fiber and vitamin C, and lacto-ovo-vegetarians,62 so that the risk of bone frac-
exhibit protective activity against cancer of the lung, tures is similar for both groups.63 Although very few data
mouth, esophagus, colon, and stomach and to a lesser exist on the bone health of vegans, some studies suggest
degree some other sites, whereas fruits rich in lycopene that bone density is lower among vegans compared with
are reported to protect against prostate cancer.47 nonvegetarians.64 This situation may be explained by
Furthermore, the regular use of legumes provides a meas- inadequate intakes of protein and calcium in these stud-
ure of protection against stomach, prostate cancer,47 and ies, nutrients essential for bone health. Vitamin D status
colon cancer,21 whereas a high intake of whole grains has can also be compromised in some vegans.65 In the EPIC-
provided some protection against colorectal and possibly Oxford study, the 30% higher risk of bone fracture in
other cancers.52-54 Allium vegetables also protect against vegans appeared to be associated with a lower calcium
stomach cancer, whereas garlic ingestion protects against intake.63
colorectal cancer. Researchers have suggested that for A widely held nutrition view states that a high pro-
European populations with a low fiber intake, doubling tein intake, especially animal protein, produces bone
the fiber intake could reduce the prevalence of colorectal resorption because of body’s need to buffer the acid
cancer by 40%.55 Among Asians with a high-soy consump- load created by the high sulfur amino acid content.
tion, a decreased risk of breast cancer was observed with This could potentially lead to decreased bone density
increased soy food intake. In contrast, soy intake was and increased fractures. Postmenopausal women with
unrelated to breast cancer risk in studies conducted in diets high in animal protein and low in plant protein
low–soy-consuming Western populations.56 Among female had a high rate of bone loss and a greatly increased risk
Chinese breast cancer survivors who were followed for 4 of hip fracture.66 However, evidence exists that low
years, soy food consumption was significantly associated protein intakes may compromise the integrity of BMD.67
with decreased risk of death and recurrence.57 In an extensive review conducted by British research-
The protective phytochemicals, such as flavonoids, ers, a small positive association was found between
indoles, sulfides, and carotenoids, have been shown in increased protein intake and BMD.68 The authors also
experimental systems to interfere with several cellular observed a slight positive effect of protein supplemen-
processes involved in the progression of cancer. These tation on lumbar spine BMD, although increased pro-
mechanisms include inhibiting cell proliferation, inhibit- tein intake did not in any way influence bone fracture
ing DNA adduct formation, inhibiting phase 1 detoxifica- rates.68 More research is needed to determine the full
tion enzymes, inhibiting signal transduction pathways extent of dietary protein upon the skeleton.
and oncogene expression, inducing cell cycle arrest and An increased consumption of fruit and vegetables,
apoptosis, inducing phase 2 detoxification enzymes, with their high potassium and magnesium content, pro-
blocking the activation of nuclear factor-κB, and inhibiting vides a positive effect on the calcium economy and mark-
angiogenesis. The phytochemicals can display additive ers of bone metabolism.69 Femoral neck and lumbar spine
618   Nutrition in Clinical Practice / Vol. 25, No. 6, December 2010

BMD of premenopausal women was about 15% to 20% Conclusions


higher for women in the highest quartile of potassium
intake compared with those in the lowest quartile.70 Appropriately planned vegetarian diets are healthful and
Results from 2 large, prospective cohort studies suggest nutritionally adequate and are beneficial in the preven-
an inverse relationship between vitamin K (and green, tion and treatment of certain chronic diseases. Poorly
leafy vegetable) intake and risk of hip fracture.71 Blood planned vegetarian diets can be deficient in vitamin B12,
levels of undercarboxylated osteocalcin, a sensitive marker calcium, vitamin D, zinc, iron, and long-chain ω-3 fatty
of vitamin K status, are used to indicate risk of hip frac- acids. Vegetarians need to incorporate into their diet
ture72 and predict BMD. foods that provide adequate levels of these vitamins, min-
Consumption of soy appears to be favorable to bone erals, and ω-3 fatty acids. Tables outlining the foods and
health. Soy isoflavones have demonstrated a significant fortified products that contain significant levels of these
benefit on spine BMD by inhibiting bone resorption and nutrients are available.6,78 There is a need for additional
stimulating bone formation compared with placebo.73 In studies of the association between the spectrum of types
a randomized controlled trial, postmenopausal women of vegetarian diets and risk of chronic disease.
receiving the soy isoflavone genistein experienced signifi-
cant decreases in urinary excretion of deoxypyridinoline References
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