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

Point1–3
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 substantial portion of essential nutrients, but especially calcium, potassium, 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 linoleic acid may be instrumental in the benefits associated with dairy product consumption for bone health and reduced risk of stroke, metabolic syndrome, and some cancers. Newer evidence shows that protein-induced calciuria does not have a detrimental effect on net calcium 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 cancer. 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):1634S–7S.

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 peerreviewed 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 consuming dairy foods include protein-induced calciuria, the presence of hormones 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

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 31–50 y is given in Table 1. In the food patterns, milk and milk products contribute .10% of the requirements 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, potassium, and magnesium. For a woman aged 19–50 y, calcium and magnesium recommendations are met with the food guide pattern 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 products. 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 2001–2002 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 number of calcium-fortified foods are available and many with good calcium bioavailability (3), they are not selected in sufficient quantities to correct the calcium shortfall created by excluding dairy products. The calcium-fortified food that most 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 bioavailability can be as good as milk depending on how it is manufactured (4). Substitution of 3 cups milk with calcium-fortified soymilk in the food patterns would constitute a substantial deviation 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 of milk to provide potassium and calcium? One-half cup orange vegetables or fruit only provides 213 mg potassium compared
1 From the Department of Foods and Nutrition, Purdue University, West Lafayette, IN. 2 Presented at the symposium, ‘‘Fifth International Congress on Vegetarian Nutrition,’’ held in Loma Linda, CA, March 4–6, 2008. 3 No reprints available. Address correspondence to CM Weaver, Department of Foods and Nutrition, Purdue University, 700 W State Street, West Lafayette, IN 47907-2059. E-mail: weavercm@purdue.edu. First published online March 25, 2009; doi: 10.3945/ajcn.2009.26736O.

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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

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Am J Clin Nutr 2009;89(suppl):1634S–7S. Printed in USA. Ó 2009 American Society for Nutrition

http://www. race effects are fairly easy to quantify because there is limited confusion for classification. The major programs supported by the federal government. release 16–1 (US Department of Agriculture.gov/fnic/foodcomp/Data/SR16/sr16. Downloaded from www. and WIC benefit from the nutrient profile of dairy foods. Such studies are available in both children and adults.35 380 6 6 6 6 6 6 6 872 99 54 23 25 123 95 Nutrient value source: Agricultural Research Service (ARS) Nutrient Database for Standard References. Of the shortfall nutrients most affected by excluding dairy products from the diet. 2012 TABLE 1 Nutrients provided by 3 cups low-fat (1%) milk compared with 3 cups calcium-fortified soy milk for women aged 31–50 y1 Cow milk Calcium (mg) Phosphorus (mg) Protein (g) Potassium (mg) Magnesium (mg) Riboflavin (mg) Vitamin D (IU) 1 Calcium-fortified soy milk 1104 675 22. and this is especially problematic during rapid bone growth (8). 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: 2.04) (14). urinary calcium excretion was 66 6 10 mg/d on a low calcium intake (386 6 14 mg/d). Dairy products provide the best package for addressing nutrients limited in the diets of many Americans. the Summer Feeding Program.63 2423 36 0. In ’300 white. A particularly persuasive study reported that low milk consumption during childhood. Vegetarians who include milk in their diet should not have compromised bone health.DAIRY FOODS: PRO 1635S with 382 mg in a cup of milk and . fracture incidence from 1980 to 1989 in 11. including low-income Americans. and the crossover design accounted for physical activity and season and the contribution of individual variation. largely but not exclusively.50 mg calcium compared with 305 mg in 1 serving of milk (5). the fracture risk of milk avoiders was 34. but dairy husbandry is practiced in one location and not in neighboring locations. Among the observational studies.53. 95% CI: 1. . In girls.009 for the lumbar spine and trends for total hip.html). half of that on the recommended calcium intake (1222 6 42 mg/d) (10). The basis for the increased requirements was the blood pressure-lowering effects detected in .0% for matched birth cohorts (12). was associated with a doubling of hip fracture in a representative US sample of postmenopausal women (11). all 7 of the randomized. Calcium should be consumed in adequate quantities to meet demands for growth and obligatory losses.619 women was found to be associated with lactose intolerance. Another type of useful observational study is one within similar cultures. because of their calcium content. In Finnish adults.15. Dairy and bone health Dairy products have been positively associated with bone health. Such studies have shown bone benefits to the dairy-consuming regions in Yugoslavia (15) and China (16).nal. In observational studies. and Asian sixth grade girls from 2 states.usda. In the controlled feeding study of Braun et al (9) all other nutrients were constant. perceived milk intolerance was inversely related to BMC of several bone sites (P ¼ 0.20 trials.3% of the variance in calcium retention. and endogenous secretion. the Child and Adult Care Feeding Program. controlled trials and 25 of the 32 observational studies showed a positive relation in 1 skeletal sites (1). chronic dietary calcium deficiency eventually depletes bone. Hispanic. Dairy products provide an important source of nutrients for high-risk groups.7%) in a metabolic study of black and white adolescent girls (9). Calcium intakes of most populations fall short of the requirements of their respective countries.1 675 117 1. Approximately 1300 mg Ca/d is needed for a female adolescent to meet the demand for skeletal growth. but dietary nutrient estimation is poorly estimated and can vary considerably over time. calcium and potassium deserve additional comment for possible consequences to health. Calcium intake explained 12. and calcium retention increased from 131 6 14 to 349 6 32 mg/d when calcium intake was raised to near recommended amounts. determined retrospectively. Thus. less confounding occurs in those that compare milk avoiders with milk consumers within the same population.23 220 871 695 24. and to adjust for average calcium absorption efficiency (7). femoral neck. The ability to adapt to low calcium intakes is incomplete. Quantifying the effect of a single nutrient on an outcome cannot be determined from observational studies in which so many confounders affecting calcium retention are at play. sweat. calcium absorption increased from 249 6 29 to 587 6 35 mg/d. measured lactose maldigestion was unrelated to bone because those who did not know they were maldigesters were not avoiding dairy product consumption. However. Potassium requirements increased considerably with the 2004 revision of the Dietary Reference Intakes (7). for losses in urine.ajcn.7 1098 81 1.58 360 6 6 6 6 6 6 6 110 96 48 14 37 144 90 Difference between soy milk and cow milk 233 220 22. In New Zealand children. almost as much as the effect of race (13. Approximately 12% of expenditures under the Food Stamp Program were for dairy foods in 2005 (6). 2 Mean 6 SD (all such values).org by guest on February 1. 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). and total body) (13). Low calcium intake leads to increased bone remodeling and increased risk of hip fracture. Nevertheless. Calcium comprises one-third of bone mineral content (BMC). 3. the Food Stamp Program.8% compared with 13. In that study. 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. such as the National School Lunch Program.

consumer demand for milk not treated with recombinant bovine somatotropin is increasing which will undoubtedly increase the cost of milk.39.4 6 0. J Nutr Educ Behav 2006. Each daily serving of dairy products lowered the risk of developing IRS. Milk and milk products have protective effects for bone disorders. and other health risks compared with omnivores or lactovegetarians. which is already excessive in protein.gov/dietaryguidelines (cited 12 September 2006). vitamin D. DC: US Government Printing Office. 6. The concentrations of hormones in milk from cows given recombinant bovine somatotropin. 2006:105–27.25-dihydroxyvitamin D by 1a hydroxylase in the prostate is independent of dietary calcium concentration (34). She is a member of advisory boards for the National Osteoporosis Foundation. Some previous concerns. Vegans have reduced bone mineral density. A prospective study of stroke on 2403 men aged 20–24 y showed a hazard ratio of 0.64 (95% CI: 0.01). to increase milk production is indistinguishable from concentrations in untreated cows (27). NJ: Humana Press. but several laboratories have shown that overall calcium retention is unaffected by protein amount or type (21–23). Weaver CM.20. conjugated linoleic acid. but calcium can suppress the production of parathyroid hormone that up-regulates IGF-I synthesis. REFERENCES 1. 1. . Miller GD. magnesium. Palacios OM. a biotech-derived growth hormone. Low calcium intakes lead to falling serum calcium concentrations that lead to activation of vitamin D to restore serum calcium concentrations to normal. 0. Heaney RP. However.37 (95% CI: 0. Available from: www. Thus. Prostate cancer Although some epidemiologic studies have shown a relation between dairy consumption and prostate cancer risk (28).9 pg/mL). Increased dietary protein can increase serum IGF-I concentrations (33). Lichtenstein AH. Dietary Reference Intakes for calcium. Wilde PE. Zhao Y. Many studies have confirmed the calciuria effect. insulin resistance syndrome (IRS). 2.106:1759–65. especially calcium. Carlson A. 2005. Britten P.38(suppl):S93–107. US Department of Health and Human Services and US Department of Agriculture. [Other articles in this supplement to the Journal include references 35–61. hyperinsulinemia. Wyeth Global Nutrition. 7. Cadbury. 0. the International Life Science Institute for North America. including protein-induced calciuria and the presence of 17b-estradiol. increased incidence of fracture. 4. and hypertension. The concern is linked to protein-induced calciuria that has been associated with bone loss (20). Washington. Dietary Guidelines for Americans. CONCLUSIONS 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 Western diet. Development of food group composites and nutrient profiles for the MyPyramid Food Guidance System. Weaver CM.135:2379–92. Marcoe K. and calcium suppression of 1. The benefits or risk of dietary protein probably depends on the dietary calcium-to-protein ratio that is comparable between lactovegetarians and omnivores (25). The 17b-estradiol concentration averaged 1. Best results were achieved with 3 servings dairy consumed daily.2 pg/mL (range: 0–22.8 mg/d. Nutr Today 2006. so the relation of dairy product consumption to cancer risk is unclear. The rich content of aromatic amino acids in milk may make this protein source especially important for enhancing calcium absorption (24). Observational studies show protective. J Am Diet Assoc 2006. 1997. Juan WY.1 ng. Gao X. Tucker KL.90) if subjects had a prior vascular event (19). Braun M. Meeting adequate intake for dietary calcium without dairy foods in adolescents aged 9 to 18 years (National Health and Nutrition Examination Survey 2001-2001).1636S Dairy and other health benefits WEAVER Health benefits of dairy consumption beyond bone health considered by the 2005 Dietary Guidelines for Americans Committee included hypertension. and skim milk would be even lower.org by guest on February 1. Institute of Medicine. Dietary calcium: recommendations and intakes around the world. 8. 2012 Milk is the most economical source of many limiting nutrients. and stroke.06) with 2 cups milk consumed daily and 0. a 10-y longitudinal study of 3157 black and white adults aged 18– 30 y from 4 US cities (18).41:40–7. characterized by obesity. and negative effects with various cancers. In: Weaver CM. The main concerns brought against including milk products in the diet lack strong and mechanistic support. RISKS Among the proposed mechanisms for a relation between dairy consumption and prostate cancer are the presence of estrogens (discussed earlier). The concentration of 17b-estradiol in 206 samples of whole cow milk was reported (26). Important evidence that supported including 3 cups milk or milk products daily came from the Cardia Study.healthierus. P . potassium. 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 . Invited editorial: The importance of dairy foods in helping impoverished people in the United States. and GTC Nutrition. Nicholls J.25-dihydroxyvitamin D production. Hormones The presence of steroid hormones in milk has been of concern to some. have recently been resolved. and stroke. Food and Nutrition Board. 3. insulin resistance. local production of 1. Furthermore. Pharmavite. A call to evaluate the impact of calcium-fortified foods and beverages. and magnesium. To compare against endogenous production of 17b-estradiol in humans. Washington. and fluoride.] CMW has a research grant from the National Dairy Council.ajcn. by 21%. Downloaded from www. Nevertheless. Martin BR. 17b-estradiol is fat soluble and is consistent with finding a significant correlation of serum 17b-estradiol with milk fat content (r ¼ 0. Green R. Looker AC. See the article by Lanou (49) for the counterpoint. the presence of 17b-estradiol is very low. phosphorus. Totowa. Calcium in human health. milk is fortified with vitamin D in the United States and has another chemoprotective constituent.15. the presence of insulin-like growth factor I (IGF-I).25-Dihydroxyvitamin D is associated with decreased proliferation and apoptosis and with protection against prostate cancer. more recent studies have shown no relation or a reduction of risk with dairy consumption (29. DC: Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. 1. J Nutr 2005. eds.90:4917–23. J Dairy Sci 2007. Calcium bioavailability of calcium carbonate fortified soymilk is equivalent to cow’s milk in young women. neutral. IRS. National Academy Press. 30) which may vary with fat content (31). a prepubertal girl produces ’400 ng/d and an adult woman in late pregnancy is as high as 37. 2005. 5. Oral IGF-I is not absorbed (32). 6th ed. Yamini S.

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