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    Should dairy be recommended as part of a healthy vegetarian diet?

    Point13

    Connie M Weaver

    ABSTRACT

    A benefit-risk evaluation of the evidence for including dairy foods in

    the diet is presented. For many persons dairy products provide a sub-

    stantial portion of essential nutrients, but especially calcium, potas-

    sium, and magnesium. Dietary supplements and fortified foods can

    be alternative sources of these nutrients, although other components

    of dairy foods such as amino acid composition and conjugated lino-

    leic acid may be instrumental in the benefits associated with dairy

    product consumption for bone health and reduced risk of stroke, met-abolic syndrome, and some cancers. Newer evidence shows that

    protein-induced calciuria does not have a detrimental effect on net cal-

    cium retention, and the concentrations of hormones in milk are not

    outside of the range of endogenous concentrations. Increased dietary

    protein, including from milk, can elevate serum concentrations of

    insulin-like growth factor I, which has an unknown relation to can-

    cer. The concern over consumption of milk leading to increased risk

    of prostate cancer through reduction of serum 1,25-dihydroxyvitamin

    D, a potent anti-prostate cancer hormone, has been resolved with new

    evidence that local production of this hormone is independent of diet.

    Overall, evidence suggests that being a lactovegetarian has greater

    health benefits and reduced health risks than being a vegan. Am

    J Clin Nutr 2009;89(suppl):1634S7S.

    INTRODUCTION

    A decision to consume dairy products, as with any food group,

    can be guided by a benefit-risk analysis. This review considers the

    merits and concerns of dairy products as foods based on peer-

    reviewed literature and does not address preferences, beliefs, or

    other issues such as production practices. The evidence that led to

    the recommendation of 3 cups (720 mL) of milk and milk

    products daily by the 2005 Dietary Guidelines for Americans

    Committee is reviewed. The most touted risks of consumingdairy

    foods include protein-induced calciuria, the presence of hor-mones and steroids, increased risk of prostate cancer, and the

    presence of lactose and saturated fats. Dairy foods void of lactose

    and fat are widely available; therefore, these issues are not

    discussed.

    BENEFITS

    Rich package of nutrients

    Milk and milk products are recommended to be consumed

    daily at amounts of 3 cups milk or the equivalent for most energy

    patterns by the 2005 Dietary Guidelines for Americans (1). The

    percentage of the requirements set by the Dietary Reference

    Intakes of the Institute of Medicine provided by 3 cups low-fat

    milk for women aged 3150 y is given in Table 1. In the food

    patterns, milk and milk products contribute .10% of the re-

    quirements of many nutrients, including riboflavin, vitamin

    B-12, vitamin A, thiamin, calcium, phosphorus, magnesium,

    zinc, potassium, protein, and carbohydrates (1). The nutrients

    most at risk if milk products are excluded are calcium, potas-sium, and magnesium. For a woman aged 1950 y, calcium and

    magnesium recommendations are met with the food guide pat-

    tern in MyPyramid. However, without milk products, only 44%

    of calcium and 57% of magnesium recommendations are met.

    For potassium, the proportion of the recommended intakes with

    milk products is 73% compared with 57% without milk prod-

    ucts. MyPyramid is based on minimal changes to the typical

    American diet in an attempt to achieve nutrient recommendations

    without exceeding energy needs. An analysis of the National

    Health and Examination Survey 20012002 showed that it is

    impossible to meet calcium recommendations for adolescents

    while meeting other nutrient recommendations with a dairy-free

    diet within the current US dietary pattern (2). Although a numberof calcium-fortified foods are available and many with good cal-

    cium bioavailability (3), they are not selected in sufficient quan-

    tities to correct the calcium shortfall created by excluding dairy

    products.The calcium-fortifiedfood thatmost closely matches the

    nutrient profile of milk is calcium-fortified soymilk (Table 1); this

    product is now allowed in the special supplemental nutrition

    program for Women, Infants, and Children (WIC). Calcium bio-

    availability can be as good as milk depending on how it is man-

    ufactured (4). Substitution of 3 cups milk with calcium-fortified

    soymilk in the food patterns would constitute a substantial de-

    viation from the typical American diet and has not been evaluated

    for overall health to provide comparable evidence to milk as

    discussed below. Can fruit and vegetables be increased instead ofmilk to provide potassium and calcium? One-half cup orange

    vegetables or fruit only provides 213 mg potassium compared

    1From the Department of Foods and Nutrition, Purdue University, West

    Lafayette, IN.2 Presented at the symposium, Fifth International Congress on Vegetar-

    ian Nutrition, held in Loma Linda, CA, March 46, 2008.3

    No reprints available. Address correspondence to CM Weaver, Depart-

    ment of Foods and Nutrition, Purdue University, 700 W State Street, West

    Lafayette, IN 47907-2059. E-mail: [email protected].

    First published online March 25, 2009; doi: 10.3945/ajcn.2009.26736O.

    1634S Am J Clin Nutr 2009;89(suppl):1634S7S. Printed in USA. 2009 American Society for Nutrition

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    with382mg ina cup ofmilk and,50 mg calcium compared with

    305 mg in 1 serving of milk (5).

    Dairy products provide the best package for addressing

    nutrients limited in the diets of many Americans. Dairy products

    provide an important source of nutrients for high-risk groups,

    including low-income Americans. The major programs supported

    by the federal government, such as the National School Lunch

    Program, the Child and Adult Care Feeding Program, the

    Summer Feeding Program, the Food Stamp Program, and WICbenefit from the nutrient profile of dairy foods. Approximately

    12% of expenditures under the Food Stamp Program were for

    dairy foods in 2005 (6).

    Of the shortfall nutrients most affected by excluding dairy

    products from the diet, calcium and potassium deserve additional

    comment for possible consequences to health. Potassium re-

    quirements increased considerably with the 2004 revision of the

    Dietary Reference Intakes (7). The basis for the increased re-

    quirements was the blood pressure-lowering effects detected

    in .20 trials. Calcium intakes of most populations fall short of

    the requirements of their respective countries, and this is espe-

    cially problematic during rapid bone growth (8). Calcium intake

    explained 12.3% of the variance in calcium retention, almost asmuch as the effect of race (13.7%) in a metabolic study of black

    and white adolescent girls (9). Quantifying the effect of a single

    nutrient on an outcome cannot be determined from observational

    studies in which so many confounders affecting calcium re-

    tention are at play. In the controlled feeding study of Braun et al

    (9) all other nutrients were constant, and the crossover design

    accounted for physical activity and season and the contribution

    of individual variation. In observational studies, race effects are

    fairly easy to quantify because there is limited confusion for

    classification, but dietary nutrient estimation is poorly estimated

    and can vary considerably over time.

    Calcium should be consumed in adequate quantities to meet

    demands for growth and obligatory losses. Approximately 1300mg Ca/d is needed for a female adolescent to meet the demand for

    skeletal growth; for losses in urine, sweat, and endogenous se-

    cretion; and to adjust for average calcium absorption efficiency

    (7). The ability to adapt to low calcium intakes is incomplete. In

    girls, urinary calcium excretion was 66 6 10 mg/d on a low

    calcium intake (386 6 14 mg/d), half of that on the recommended

    calcium intake (1222 6 42 mg/d) (10). Nevertheless, calcium

    absorption increased from 249 6 29 to 587 6 35 mg/d, and

    calcium retention increased from 131 6 14 to 349 6 32 mg/d

    when calcium intake was raised to near recommended amounts.

    Thus, chronic dietary calcium deficiency eventually depletes bone.

    Dairy and bone health

    Dairy products have been positively associated with bone

    health, largely but not exclusively, because of their calcium

    content. Calcium comprises one-third of bone mineral content

    (BMC). Low calcium intake leads to increased bone remodelingand increased risk of hip fracture. At the time the 2005 Dietary

    Guidelines for Americans Committee reviewed the evidence for

    a relation between intake of milk products and BMC or bone

    mineral density, all 7 of the randomized, controlled trials and 25

    of the 32 observational studies showed a positive relation in 1

    skeletal sites (1). A particularly persuasive study reported that

    low milk consumption during childhood, determined retrospec-

    tively, was associated with a doubling of hip fracture in a rep-

    resentative US sample of postmenopausal women (11).

    Among the observational studies, less confounding occurs in

    those that compare milk avoiders with milk consumers within

    the same population. Such studies are available in both children

    and adults. In New Zealand children, the fracture risk of milkavoiders was 34.8% compared with 13.0% for matched birth

    cohorts (12). In 300 white, Hispanic, and Asian sixth grade

    girls from 2 states, perceived milk intolerance was inversely

    related to BMC of several bone sites (P 0.009 for the lumbar

    spine and trends for total hip, femoral neck, and total body) (13).

    In that study, measured lactose maldigestion was unrelated to

    bone because those who did not know they were maldigesters

    were not avoiding dairy product consumption. In Finnish adults,

    fracture incidence from 1980 to 1989 in 11,619 women was

    found to be associated with lactose intolerance. The risk of

    lower body fractures excluding ankle was 2 times greater for

    women claiming lactose intolerance than for women without

    lactose intolerance (odds ratio: 2.15; 95% CI: 1.53, 3.04) (14).Another type of useful observational study is one within similar

    cultures, but dairy husbandry is practiced in one location and not

    in neighboring locations. Such studies have shown bone benefits

    to the dairy-consuming regions in Yugoslavia (15) and China

    (16). Vegetarians who include milk in their diet should not have

    compromised bone health. However, vegans who exclude dairy

    products in their diets have higher fracture risk according to data

    from the European Prospective Investigation into Cancer and

    Nutrition study (17).

    TABLE 1

    Nutrients provided by 3 cups low-fat (1%) milk compared with 3 cups calcium-fortified soy milk for women aged 3150 y1

    Cow mi lk Calci um-fortified soy mi lk

    Difference between soy milk

    and cow milk

    Calcium (mg) 871 6 872

    1104 6 110 233

    Phosphorus (mg) 695 6 99 675 6 96 220

    Protein (g) 24.7 6 54 22.1 6 48 22.63

    Potassium (mg) 1098 6 23 675 6 14 2423

    Magnesium (mg) 81 6 25 117 6 37 36

    Riboflavin (mg) 1.35 6 123 1.58 6 144 0.23

    Vitamin D (IU) 380 6 95 360 6 90 220

    1Nutrient value source: Agricultural Research Service (ARS) Nutrient Database for Standard References, release 161

    (US Department of Agriculture; http://www.nal.usda.gov/fnic/foodcomp/Data/SR16/sr16.html).2

    Mean 6 SD (all such values).

    DAIRY FOODS: PRO 1635S

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    Dairy and other health benefits

    Health benefits of dairy consumption beyond bone health

    considered by the 2005 Dietary Guidelines for Americans

    Committee included hypertension, insulin resistance syndrome

    (IRS), and stroke. Important evidence that supported including

    3 cups milk or milk products daily came from the Cardia Study,

    a 10-y longitudinal study of 3157 black and white adults aged 18

    30 y from 4 US cities (18). Each daily serving of dairy productslowered the risk of developing IRS, characterized by obesity,

    hyperinsulinemia, insulin resistance, and hypertension, by 21%.

    Best results were achieved with 3 servings dairy consumed

    daily. A prospective study of stroke on 2403 men aged 2024 y

    showed a hazard ratio of 0.64 (95% CI: 0.39, 1.06) with 2 cups

    milk consumed daily and 0.37 (95% CI: 0.15, 0.90) if subjects

    had a prior vascular event (19).

    RISKS

    Protein-induced calciuria

    Much malignment of milk products as a source of calcium has

    been directed at the 8 g protein/cup that milk adds to the Westerndiet, which is already excessive in protein. The concern is linked

    to protein-induced calciuria that has been associated with bone

    loss (20). Many studies have confirmed the calciuria effect, but

    several laboratories have shown that overall calcium retention is

    unaffected by protein amount or type (2123). The rich content

    of aromatic amino acids in milk may make this protein source

    especially important for enhancing calcium absorption (24). The

    benefits or risk of dietary protein probably depends on the

    dietary calcium-to-protein ratio that is comparable between

    lactovegetarians and omnivores (25).

    Hormones

    The presence of steroid hormones in milk has been of concern

    to some. The concentration of 17b-estradiol in 206 samples of

    whole cow milk was reported (26). The 17b-estradiol concen-

    tration averaged 1.4 6 0.2 pg/mL (range: 022.9 pg/mL). A

    1-cup serving of milk would average 330 pg and the 3 cups

    recommended in the food guidance system for most energy

    amounts would contain ,1 ng. To compare against endogenous

    production of 17b-estradiol in humans, a prepubertal girl pro-

    duces 400 ng/d and an adult woman in late pregnancy is as

    high as 37.8 mg/d. Thus, the presence of 17b-estradiol is very

    low, and skim milk would be even lower. 17b-estradiol is fat

    soluble and is consistent with finding a significant correlation of

    serum 17b-estradiol with milk fat content (r 0.20, P , 0.01).

    The concentrations of hormones in milk from cows given

    recombinant bovine somatotropin, a biotech-derived growth hor-

    mone, to increase milk production is indistinguishable from con-

    centrations in untreated cows(27).Nevertheless, consumer demand

    for milk not treated with recombinant bovine somatotropin is

    increasing which will undoubtedly increase the cost of milk.

    Prostate cancer

    Although some epidemiologic studies have shown a relation

    between dairy consumption and prostate cancer risk (28), more

    recent studies have shown no relation or a reduction of risk with

    dairy consumption (29, 30) which may vary with fat content (31).

    Among the proposed mechanisms for a relation between dairy

    consumption and prostate cancer are the presence of estrogens

    (discussed earlier), the presence of insulin-like growth factor I

    (IGF-I), and calcium suppression of 1,25-dihydroxyvitamin D

    production. Oral IGF-I is not absorbed (32). Increased dietary

    protein can increase serum IGF-I concentrations (33), but cal-

    cium can suppress the production of parathyroid hormone that

    up-regulates IGF-I synthesis, so the relation of dairy product

    consumption to cancer risk is unclear. Low calcium intakes leadto falling serum calcium concentrations that lead to activation of

    vitamin D to restore serum calcium concentrations to normal.

    1,25-Dihydroxyvitamin D is associated with decreased pro-

    liferation and apoptosis and with protection against prostate

    cancer. However, local production of 1,25-dihydroxyvitamin D

    by 1a hydroxylase in the prostate is independent of dietary

    calcium concentration (34). Furthermore, milk is fortified with

    vitamin D in the United States and has another chemoprotective

    constituent, conjugated linoleic acid.

    CONCLUSIONS

    Milk is the most economical source of many limiting nutrients,especially calcium, potassium, and magnesium. Milk and milk

    products have protective effects for bone disorders,IRS, andstroke.

    Observational studies show protective, neutral, and negative effects

    with various cancers. The main concerns brought against including

    milk products in the diet lack strong andmechanistic support. Some

    previous concerns, including protein-induced calciuria and the

    presence of 17b-estradiol,have recentlybeenresolved. Veganshave

    reduced bone mineral density, increased incidence of fracture, and

    other health risks compared with omnivores or lactovegetarians.

    [Other articles in this supplement to the Journal include references

    3561. See the article by Lanou (49) for the counterpoint.]

    CMW has a research grant from the National Dairy Council. She is a mem-

    ber of advisory boards for the National Osteoporosis Foundation, the Inter-

    national Life Science Institute for North America, Wyeth Global Nutrition,

    Pharmavite, Cadbury, and GTC Nutrition.

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