HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Buchowski, M. S. Articles by Johnson, A. O. Search for Related Content PubMed PubMed Citation Articles by Buchowski, M. S. Articles by Johnson, A. O.

Dietary Calcium Intake in Lactose Maldigesting Intolerant and Tolerant African-American Women

Center for Nutrition (M.S.B., A.O.J.), Meharry Medical College, 1005 D.B. Todd Blvd., Nashville, Tennessee
Department of Family and Community Medicine (M.S.B., J.S.), Meharry Medical College, 1005 D.B. Todd Blvd., Nashville, Tennessee

Address reprint requests to: Maciej S. Buchowski, PhD, Center for Nutrition, Meharry Medical College, 1005 D.B. Todd Blvd., Nashville, TN 37208. E-mail: mbuchowski{at}mmc.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Background: The relationship between lactose maldigestion, lactose intolerance, and calcium intake in premenopausal African American women is unknown.

Objective: To determine how intolerance of lactose and dairy products affects intake of calcium in lactose maldigesting premenopausal African American women.

Design: Dietary intake of calcium was assessed in 50 premenopausal lactose maldigesting African American women as determined by the breath hydrogen test. Twenty-six women were lactose intolerant and 24 were lactose tolerant by self-reports.

Results: The average intake of calcium in lactose maldigesting and intolerant women was significantly lower than in lactose tolerant women (388 ± 150 mg/day vs. 763 ± 333 mg/day, p < 0.0001, t test). Neither group reached the newly established Dietary Reference Intake (DRI) for calcium (1,000 mg/day). Major source of dietary calcium in lactose tolerant women were milk and dairy products (45%), and mixed foods containing calcium from non-dairy sources (30%). In lactose intolerant women, 46% of calcium was from mixed foods and only 12% was from milk and dairy products. Lactose intolerant women had higher body mass index (BMI) than lactose tolerant women (p = 0.008, t test), and calcium intake was negatively associated with BMI (R² = 0.470).

Conclusions: In African American premenopausal women, lactose tolerance facilitates the dietary intake of calcium when compared with their lactose intolerant counterparts. Low calcium intake is associated with higher BMI.

Key words: dietary calcium, lactose maldigestion, lactose tolerance, African-American women, body mass index

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Lactase insufficiency and consequent lactose maldigestion occurs in a majority of the various ethnic minorities in the U.S. It is particularly common among African-Americans in whom prevalence rate is 70% to 75% [1]. Present at birth, the ability to digest lactose is decreased to <10% of childhood levels in human adult-onset lactase (lactase-phlorizin hydrolase—LPH) decline [2, 3]. This decline demonstrates an autosomal recessive pattern of inheritance [4] and is regulated primarily by the rate of lactase gene transcription [5–7], although the molecular mechanism that regulates the decline is currently unknown [8]. Nevertheless, lactase-insufficient individuals malabsorb lactose but may or may not show intolerance symptoms [9–11]. Ingestion of high quantities of lactose-containing foods such as milk and dairy products by individuals with adult-onset lactase decline can result in gastrointestinal symptoms such as abdominal pain, bloating, flatus and diarrhea [12]. The development of symptoms appears to depend on the dose of lactose ingested, whether ingestion is part of a meal or is accompanied by ingestion of a meal or other food, rate of gastric emptying and small intestine transit time [13]. Nevertheless, lactose intolerance due to lactose insufficiency usually leads to self-imposed dietary restriction by the individual of milk and dairy products, which are the major source of dietary calcium in the U.S. [14]. With the relatively low rate of milk and dairy foods intake among minority groups especially African Americans, there is a concern that calcium intake is low in this group. A recent National Institutes of Health Consensus Conference concluded that calcium intake of 1,000–1,500 mg/day may prevent, and 1,500 mg per day may reduce the incidence and severity of postmenopausal osteoporosis [15]. Consequently, the Food and Nutrition Board of the National Research Council set a Dietary Reference Intake (DRI) for calcium in premenopausal women (21 to 50 years of age) at 1,000 mg per day [16]. Implementation of this recommendation requires a diet that is naturally rich in calcium such as milk and dairy products or ingestion of calcium supplements and calcium-fortified foods. Milk and dairy products, however, contain substantial quantities of lactose, and gastrointestinal symptoms caused by lactose maldigestion lead to avoidance of dairy foods. Previously, we have shown that African Americans who are lactose maldigesters can adopt and tolerate well a meal containing lactose [17]. Other workers have reported that lactose maldigesters could tolerate diet containing milk and diary product with a substantial amount of lactose and up to 1,500 mg of calcium [13, 18]. Nevertheless, there is considerable variability in the pattern of dairy products consumption among lactose maldigesters [19–21] who may have lower intakes of calcium. Indeed, some reports have shown lower calcium intake in lactose maldigesters when compared to lactose digesters and tolerant individuals [22–23].

Recently, several clinical studies of dietary calcium have shown a negative association between calcium intake and body weight. For example, in a double-blind, placebo-controlled, randomized trial of calcium supplementation, the calcium-supplemented subjects exhibited a significant weight loss across nearly four years of observation [24]. Estimation of the relationship between calcium and body weight indicated that a 1,000-mg Ca intake difference was associated with an 8-kg difference in mean body weight [24]. Moreover, population based data from NHANES III supported this notion showing a profound reduction in the odds of being in the highest quartile of adiposity with the increase in calcium and dairy product intake [25]. Recently, Lin et al. [26] have reported that young women with high calcium intake, corrected by total energy intake, and lower vitamin A intake gained less weight and body fat in a two-year randomized exercise trial. Similar association between calcium intake and body weight has been shown in children [27–28]. In their longitudinal study, Carruth and Skinner [27] showed that higher intakes of calcium, monounsaturated fat and dairy products were associated with lower body fat. Tanesescu et al. [28] have reported that among other factors, such as TV viewing, frequency of fruit juice consumption and maternal BMI, lower intake of dairy products was associated with obesity in Puerto Rican children.

The goal of this study was to determine how perceived intolerance of lactose affects intake of calcium in premenopausal African American women who are lactose maldigesters. The null hypothesis was that there is no significant difference in daily calcium intake between lactose and dairy products tolerant and intolerant groups of lactose maldigesters. A secondary objective of this study was to examine the association, if any, between calcium intake and body mass in African American women lactose maldigesters.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Subjects
Fifty-seven African American women who volunteered and gave an informed consent participated in this study. The protocol was approved by the Meharry Medical College Institutional Review Board Committee on Human Investigations. By design, all participating subjects were selected from a group of 83 initially screened women who had been classified as lactase deficient on the basis of a rise in breath hydrogen concentration of greater than 0.90 µmol/L (>20 ppm) after ingestion of 25 g of lactose in 250 mL of water. Briefly, lactose absorption was assessed by measuring alveolar breath hydrogen exhalation at 15 minute intervals for three hours following an oral challenge, as we described previously [10]. All women were premenopausal as assessed by self-reported frequency of menstruation in the preceding three-month period.

Reporting of Symptoms
The occurrence and severity of symptoms were self-rated by the subjects after ingesting 250 mL of lactose containing or lactose-free milk as described by Suarez et al. [13]. Subjects reported occurrence and severity of abdominal fullness or cramps, flatulence, borborygmi and diarrhea on a 0-to-5 scale as follows: 0 = no symptoms, 1 = trivial, 2 = mild, 3 = moderate, 4 = strong and 5 = severe. Women with scores of at least 3 on this scale after ingesting lactose-containing milk were classified as lactose intolerant (LI group). Women who scored 2 or less after drinking lactose containing milk were classified as lactose tolerant (LT group). Before the present study, all 26 women who were lactose intolerant and four women who self-reported lactose tolerance believed that ingestion of milk and dairy products caused them to have gastrointestinal discomfort. Seven women were excluded from final analyses; two withdrew from the study, and five women did not complete dietary records.

Diet Analysis
Each participant kept a seven-day dietary record (Monday–Sunday) starting 7 to 12 days after the lactose challenge. A dietitian met with each participant and explained proper record keeping and the amount of food eaten was quantified in grams, cups, ounces, teaspoons, tablespoons, pieces, slices, etc. as necessary for analysis. In addition, each participant received a small kitchen balance, standardized report forms and National Dairy Council food models to help in assessing portion size. All subjects did dietary recording during the same season (early summer) to minimize measurement bias related to seasonal availability of foods. All foods eaten, including snacks and drinks, were recorded over a seven-day period. Use of dietary supplements, including calcium supplements, was not encouraged or discouraged and intakes were reported. After completion, all records were collected and initially screened by a dietitian. Any problems with identification of foods, methods of preparation and portion sizes were discussed with subjects over the telephone. Dietary intakes were analyzed using Food Processor (Version 7.0, ESHA Research, Salem, OR).

Statistical Analysis
Data are mean ± SD. Continuous variables between subjects were evaluated using independent sample t tests. The significance of differences in dietary calcium intake was analyzed using one-way ANOVA. Multiple linear regression analysis was performed on calcium intake (mg/day) and calcium intake corrected for energy intake (mg Ca/1,000 kcal/day) by use of a forward elimination approach. Covariates that were considered for inclusion were lactose tolerance (0 = lactose intolerant, 1 = lactose tolerant), BMI, age and plausible interactions among these. Age was treated as a continuous variable. Analyses were performed using SPSS-PC (Version 10) software package. A p value of < 0.05 was used for inclusion of terms in the regression and to indicate statistical significance. A sample size was chosen based on the variability of calcium intake observed in our pilot studies with African American women and NHANES III reports [29].

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Subject Characteristics
Table 1 presents descriptive data for study participants. Hydrogen excretion after a lactose tolerance test was similar in the LT and LI groups (p = 0.567) and confirmed lactose-maldigestion in all participating women. Women in the LI group were heavier and had higher mean BMI than women in the LT group (p < 0.05 for both parameters).

View larger version (43K): [in this window] [in a new window]   Fig. 1. Percentage contribution of calcium sources in diet of African American women according to self-reported food intake.

View larger version (14K): [in this window] [in a new window]   Fig. 2. Relation of total daily calcium intake and body mass index in African American women lactose malabsorbers according to self-reported tolerance of milk and dairy products. A positive relationship was observed between calcium intake and BMI (see Table 3 for corresponding analysis). Calcium intake was higher on average in lactose tolerant (LT) than in lactose intolerant (LI) women (regression coefficient = 208.5). Regression equations: Calcium intake (mg/1,000 kcal/day) = 505.23 - 11.47 x BMI (kg/m2)+ 208.5 x lactose tolerance; (R2 = 0.605), which is significantly different from lactose intolerant (LI) group (p < 0.001).

	DISCUSSION

It is commonly believed that the symptoms resulting from lactose maldigestion limit the amount of lactose and dairy rich foods ingested by lactose maldigesters [13]. In the present study, lactose intolerant women had lower intake of milk and dairy products than age-matched lactose tolerant women. It is probable that the gastrointestinal discomfort associated with reduced lactose tolerance contributed to the decline in milk consumption in lactose intolerant women. We [17] and others [11, 30–32] in double-blind studies have shown that persons with lactose maldigestion experience negligible symptoms when they ingest up to two cups of milk. Nevertheless, the anticipation of symptoms resulting from lactose maldigestion leads many lactose intolerant individuals to shun consumption of milk and selected dairy products.

Questions have been raised about the adequacy of dietary calcium intake in populations with a high prevalence of lactose maldigestion and lactose intolerance. For example, Mainguet et al. [23] evaluated the calcium intake of 134 patients with abdominal symptoms after consumption of dairy products. They found that the daily calcium intake of patients lacking lactose activity in the jejunal biopsy was significantly lower than that of controls. However, in patients with partial lactase deficiency, calcium intake did not differ from that of controls. A similar study conducted at the Mayo Clinic with control of ethnic background [33] found that intake of both lactose and calcium in lactase deficient subjects was significantly lower than in the lactase sufficient group. Carrocio et al. [34] found a lower daily milk intake and a lower daily calcium intake in lactose maldigesters and intolerant individuals. Results of the present study confirm that self-imposed restriction may lead to decreased calcium intake. Indeed, African American women who reported symptoms of intolerance to a 25 g challenge dose of lactose had significantly lower intake of calcium than lactose tolerant women.

In addition to lower calcium intake in lactose intolerance, there is a possibility that undigested lactose in the small intestine may affect calcium bioavailability. Previous reports of calcium absorption in lactose tolerant and intolerant subjects have been rather conflicting. While some reports suggest that lactose or products of its hydrolysis, galactose and glucose, facilitate calcium absorption [35, 36], another study reported that calcium absorption was significantly greater in lactase insufficiency [37]. Nevertheless, the present consensus appears to be that adult-onset lactase decline might have an indirect impact on calcium bioavailability by interfering with calcium absorption [8]. Furthermore, as postulated by Nordin [38], calcium requirement may depend on intake of other nutrients such as protein, sodium, and vitamin D. Women in our study had higher than recommended intakes of protein and sodium but lower intakes of vitamin D, and this was likely to have an impact on their calcium requirement.

We [17] and others [11,13,18] have shown that symptoms associated with lactose maldigestion can be affected by changes in nutritional habits. For example, consumption of milk with solid foods can mitigate symptoms in many individuals and ensure adequate calcium intake [39]. In the present study, the majority of calcium in lactose intolerant women came from mixed foods containing low amount of calcium mostly from added dairy products such as pastas, selected fast foods, baked goods and sweets. We suggest that African American women who are lactose intolerant choose dairy foods that are high in calcium but low in lactose such as exogenous lactase treated milk, yogurts and microbial lactase treated yogurts, and cheeses that do not contain or contain a low amount of lactose. In addition, these foods could be consumed with meals so as to reduce gastrointestinal symptoms [13, 40]. These maneuvers may help many lactose maldigesters and promote their ability to continue or increase their consumption of dairy products without or with minimal symptoms. Alternative calcium sources like fortified fruit juices and other calcium-fortified products may be recommended for lactose intolerant and dairy product intolerant African American women. Calcium supplements as a major source of dietary calcium should be considered only for women with severe gastrointestinal symptoms and low intakes of calcium from foods.

It has been recently postulated that low calcium diets favor increased adipose tissue energy storage and the converse is true for high calcium intake [25]. In our study, women who had higher intake of calcium had significantly lower BMI than women with lower intakes of calcium. Davis et al. [24] reevaluated five clinical studies of calcium intake in women to explore associations between calcium intake and body weight. They found a negative association between calcium intake and weight, and calculated that the odds ratio for being overweight was 2.25 for young women in the lower half of calcium intake. These authors estimated that a 1000-mg difference in calcium intake was associated with an 8 kg difference in mean body weight and that variations in calcium intake could account for approximately 3% of the variance in body weight. It has been shown that a low calcium intake tends to be a marker for a poor diet and that a poor diet is good predictor of obesity [24, 41]. The relationship between calcium intake and body weight was stronger when calcium intake was corrected for energy intake. The association between high BMI and low calcium intake observed in this study may be related to other nutritional factors such as eating habits and/or patterns and physical activity which we did not control for in this study. Body weight is a highly multifactorial variable, and it is very likely that only a fraction of its variability seen in this study could be attributed to calcium intake. Nevertheless, the association between calcium intake and BMI was stronger when calcium intake was expressed as density. This might suggest that women with lower energy intake might benefit more from high calcium intake and control weight better than women with higher energy intake. Indeed, it has been postulated that higher energy intakes could overwhelm the impact of calcium on changes in body composition in adult women [26]. Hence, it would be beneficial to conduct a clinical trial in which all these factors will be controlled for and in which weight change would be the primary outcome variable.

The findings of this study have to be assessed in the context of our experimental design. First, we used seven-day dietary records to assess dietary intake. In order to minimize inheritent problems with dietary records previously described [42], we provided subjects with detailed instruction and contacted them when problems with interpretation of a record occurred. Although some misreporting was possible, intakes of energy and nutrients in our study are similar to results reported in NHANES III for African American women in Southern U.S. (Table 2). Nevertheless, we tried not to over interpret the results of intake analysis. Secondly, we did not assess bone density or bone turnover ratio in our study participants. Previous studies, however, failed to detect any adverse effects of lactose maldigestion and decreased calcium absorption on bone density [22, 43–44]. It is probable that any adverse effect of lactose maldigestion on bone density is due to reduction in calcium intake via milk avoidance rather than to impaired absorption of ingested calcium [22]. Recently, it has been postulated that lactose maldigestion acts as a risk factor for osteoporotic bone loss in symptomatic individuals with lactose intolerance and very low calcium intakes [23, 31]. Some studies found that bone mineral density and calcium intake were lower in women with both lactose maldigestion and intolerance [45]. These reports infer that hypolactasia could predispose a person to osteoporosis through either reduced intake of milk secondary to lactose intolerance or impaired calcium absorption. Osteoporosis is common in lactase deficiency [45–46], suggesting a link between adult-onset lactase decline and increased risk of this condition which is characterized by decreased bone mass, enhanced bone fragility and consequent increase in fracture risk [47]. Thus it would appear that the association between lactose ingestion and osteoporosis is most likely due to the inadequate calcium intake resulting from a reduced intake of milk and dairy products as a result of lactose maldigestion and intolerance. The observation that African Americans have a low prevalence of osteoporosis and relatively low calcium intake appears to argue against this relationship [48]. However, the greater bone density observed in African Americans at maturity would offer relative protection from osteoporosis later in life despite the presence of lactase insufficiency [49].

Finally, in our analysis we did not control for factors linked to increased BMI in women such as previous pregnancy, activity level, family history of obesity and diabetes, and other environmental factors. Nevertheless, it is well known that low calcium intakes are linked to pathogenesis of osteoporosis, hypertension, colon cancer, renolithiasis and possibly obesity in African American women [8, 25, 35].

In this study, we have shown that among lactose maldigesting African American women after adjusting for age and weight, lactose intolerant women have lower calcium intakes than those who are lactose tolerant. Lactose maldigesting intolerant women also had a higher BMI than lactose tolerant women. We conclude that, in premenopausal African American women, lactose maldigestion accompanied by lactose intolerance is associated with low levels of calcium intake. Possible impact of this phenomenon on the observed increased BMI in this population requires further studies.

	ACKNOWLEDGMENTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
This work was supported by grants from the National Institutes of Health HL-03530 (to M.S.B.), General Clinical Research Center Grant RR-1179204 (to Meharry Medical College), Clinical Nutrition Research Unit Grant DK-26657 (to Vanderbilt University), and Meharry COE grant (to M.S.B.). We thank LeMonica Lewis for her technical help and assistance in preparing this manuscript. Finally, we acknowledge our subjects for their enthusiasm and participation in this study.

Received August 16, 2001. Accepted October 24, 2001.

	REFERENCES

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 

1. Scrimshaw NS, Murray AB: The acceptability of milk and milk products in population with a high prevalence of lactose intolerance. Am J Clin Nutr 48 (Suppl 1): 1083–1325, 1988.[Free Full Text]
2. Sterchi EE, Mills PR, Fransen JAM, Hauri HP, Lentze MJ, Nains HY, Ginsel L, Bond J: Biogenesis of Intestinal Lactose-Phlorizin Hydrolase in adults with Lactose Intolerance. J Clin. Invest 86: 1329–1337, 1990.
3. Büller HA, Grand RJ: Lactose intolerance. Ann Rev Med 41: 141–148, 1990.[Medline]
4. Sahi T: The inheritance of selective adult-type lactose malabsorption. Scand J Gastroenterol 30 (Suppl): 1–73, 1974.
5. Escher JC, de Koning ND, van Engen CG, Arora S, Buller HA, Montgomery RK, Grand RJ: Molecular basis of lactase levels in adult humans. J Clin Invest 89: 480–483, 1992.
6. Fajardo O, Naim HY, Lacey SW: The polymorphic expression of lactase in adults is regulated at the messenger RNA level. Gastroenterology 106: 1233–1241, 1994.[Medline]
7. Montgomery RK, Buller HA, Rings EHHM, Grand RJ: Lactose intolerance and the genetic regulation of intestinal lactase-phlorizin hydrolase. FASEB J 5: 2824–2832, 1991.[Abstract]
8. Lee MF, Krasinski SD: Human adult-onset lactase decline: An update. Nutr Rev 56: 1–8, 1998.[Medline]
9. Bayless TM, Rothfeld B, Massa C, Wise L, Paige D, Bedine MS: Lactose and milk intolerance: clinical implications. N Engl J Med 292: 1156–1159, 1975.[Abstract]
10. Johnson AO, Semenya JG, Buchowski MS, Enwonwu CO, Scrimshaw NS: Correlation of lactose maldigestion, lactose intolerance, and milk intolerance. Am J Clin Nutr 57: 399–401, 1993.[Abstract/Free Full Text]
11. Suarez FL, Savaiano DA, Levitt MD: A comparison of symptoms after the consumption of milk or lactose-hydrolyzed milk by people with self-reported severe lactose intolerance. N Engl J Med 333: 1–4, 1995.[Abstract/Free Full Text]
12. Shaw AD, Davies GJ: Lactose Intolerance Problems in Diagnosis and Treatment. J Clin Gastroenterol 28: 208–216, 1991.
13. Suarez FL, Adshead J, Furne JK, Levitt MD: Lactose maldigestion is not an impediment to the intake of 1500 mg calcium daily as dairy products. Am J Clin Nutr 68: 1118–1122, 1998.[Abstract]
14. Fleming KH, Heimbach JT: Consumption of calcium in the US: food sources and intake levels. J Nutr 124 (Suppl): 1426S–1430S, 1994.
15. NIH Consensus Conference, NIH Consensus Development Panel on Optimal Calcium Intake: Optimal calcium intake. JAMA 272: 1942–1948, 1994.[Medline]
16. Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. Food and Nutrition Board. Academy of Medicine: Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride. Washington DC: National Academy Press, pp 71–145, 1999.
17. Johnson AO, Semenya JG, Buchowski MS, Enwonwu CO, Scrimshaw NS: Adaptation of lactose maldigesters to continued milk intakes. Am J Clin Nutr 58: 879–881, 1993.[Abstract/Free Full Text]
18. Pribila BA, Hertzler SR, Martin BR, Weaver CM, Savaiano DA: Improved lactose digestion and intolerance among African-American adolescent girls fed a dairy-rich diet. J Am Diet Assoc 100: 524–528, 2000.[Medline]
19. Arola H, Tamm A. Metabolism of lactose in the human body. Scand J Gastroenterol 202 (Suppl): 21–55, 1994.
20. Suarez FL, Saviano DA, Levitt MD: Review article: the treatment of lactose intolerance. Aliment Pharmacol Ther 9: 589–597, 1995.[Medline]
21. Vesa TH, Korpela RA, Sahi T: Tolerance to small amounts of lactose in lactose maldigesters. Am J Clin Nutr 64: 197–201, 1996.[Abstract/Free Full Text]
22. Goulding A, Taylor RW, Keil D, Gold E, Lewis-Barned NJ, Williams SM: Lactose malabsorption and rate of bone loss in older women. Age Ageing 28: 175–180, 1999.[Abstract/Free Full Text]
23. Mainguet P, Faile I, Destrebecq I, Devogelear JP, Nagant de Deuxcahines C: Lactose intolerance, calcium intake and osteopenia. Lancet 338: 1156–1157, 1991.
24. Davies KM, Heaney RP, Recker RR, Lappe JM, Barger-Lux MJ, Rafferty K, Hinders S: Calcium intake and body weight. J Clin Endocr Metabol 85: 4635–4638, 2000.[Abstract/Free Full Text]
25. Zemel MB, Shi H, Greer B, DiRienzo D and Zemel PC: Regulation of adiposity by dietary calcium. FASEB J 14: 1132–1138, 2000.[Abstract/Free Full Text]
26. Lin YI, Lyle RM, McCabe LD, McCabe GP, Weaver CM, Teegarden D: Dairy calcium is related to changes in body composition during a two-year exercise intervention in young women. J Am Coll Nutr 19: 754–760, 2000.[Abstract/Free Full Text]
27. Carruth BR, Skinner JD: The role of dietary calcium and other nutrients in moderating body fat in preschool children. Intern J Obesity 25: 559–566, 2001.
28. Tanesescu M, Ferris AM, Himmelgreen DA, Rodriguez N: Biobehavioral factors are associated with obesity in Puerto Rican children. J Nutr 130: 1734–1742, 2000.[Abstract/Free Full Text]
29. US Department of Health and Human Services (DHHS). National Centers for Health Statistics: Third National Health and Nutrition Examination Survey, 1988–1994. NHANES III Laboratory Data File. NHANES III Series 11, No. 1A, July 1997, NHANES III Series 11, No. 2A, April 1998. http://www.cdc.gov/nchs/nhanes.htm. 2001.
30. Rorick MH, Scrimshaw NS: Comparative tolerance of elderly from differing ethnic backgrounds to lactose-containing and lactose-free dairy drinks: a double blind study. J Gerontolog 34: 191–196, 1979.
31. Havenberg L, Kwon PH, Scrimshaw NS: Comparative tolerance of adolescents from differing ethnic backgrounds to lactose-containing and lactose-free dairy drinks: I. Initial experience with double-blind procedure. Am J Clin Nutr 33: 17–21, 1980.[Abstract/Free Full Text]
32. Unger M, Scrimshaw NS: Comparative tolerance of adults of differing ethnic backgrounds to a lactose-free and lactose-containing dairy drink. Nutr Res 1: 1227–1233, 1981.
33. Newcomer AD, Gordon H, Thomas PJ, McGill DB: Family studies of lactase deficiency in the American Indian. Gastroenterology 73: 985–988, 1977.[Medline]
34. Carroccio A, Montalto G, Cavera G, Notarbatolo A: Lactose intolerance and self-reported milk intolerance: Relationship with lactose maldigestion and nutrient intake. J Am Coll Nutr 17: 631–636, 1998.[Abstract/Free Full Text]
35. Griessen M, Speich PV, Infante F, Bartholdi P, Cochet B, Donath A, Courvoisier B, Bonjou JP: Effect of absorbable and nonabsorbable sugars on intestinal calcium absorption in humans. Gastroenterology 96: 769–775, 1989.[Medline]
36. Cochet B, Jung A, Griessen M, Bartholdi P, Schaller P, Donath A: Effect of lactose on intestinal calcium absorption in normal and lactase-deficient subjects. Gastroenterology 84: 935–940, 1983.[Medline]
37. Tremaine WJ, Newcomer AD, Riggs BL, McGill DB: Calcium absorption from milk in lactase-deficient and lactase sufficient adults. Dig Dis Sci 31: 376–378, 1986.[Medline]
38. Nordin BE, Need AG, Steurer T, Morris HA, Chatterton BE, Horowitz M: Nutrition, osteoporosis, and aging. Ann NY Acad Sci 854: 336–351, 1998.[Abstract/Free Full Text]
39. Martini MC, Smith DE, Savaiano DA: Lactose digestion from frozen yogurts, ice milk, and ice cream by lactase deficient persons. Am J Clin Nutr 46: 636–6340, 1998.[Abstract/Free Full Text]
40. Martini MC, Savaiano DA: Reduced intolerance symptoms from lactose consumed during a meal. Am J Clin Nutr 47: 57–60, 1998.[Abstract/Free Full Text]
41. Miller GD, Jarvis JK, McLean LD: The importance of meeting calcium needs with food. J Am Coll Nutr 20: 168S–185S, 2001.[Abstract/Free Full Text]
42. Sawaya AL, Tucker K, Tsay R, Willett W, Saltzman E, Dallal GE, Roberts SB: Evaluation of four methods for determining energy intake in young and older women: comparison with double labeled water measurements of total energy expenditure. Am J Clin Nutr 63: 491–499, 1996.[Abstract/Free Full Text]
43. Slemenda CW, Christian JC, Hui S, Fitzgerald J, Johnston Jr CC: No evidence for the effect of lactase deficiency on bone mass in pre- or postmenopausal women. J Bone Miner Res 6: 1367–1371, 1991.[Medline]
44. Horowitz M, Wishart J, Mundy L, Nordin C: Lactose and calcium absorption in postmenopausal osteoporosis. Arch Intern Med 147: 534–536, 1987.[Abstract]
45. Finkenstedt G, Skrabal F, Gasser RW, Braunsteiner H: Lactose absorption, milk consumption, and glucose level concentration in women with idiopathic osteoporosis. Br Med J 292: 161–162, 1986.
46. Birge S, Keutman A, Cuatrecasas P: Osteoporosis, intestinal lactose deficiency and low calcium intake. N Engl J Med 276: 445–448, 1967.
47. Rosen CJ: Pathophysiology of osteoporosis. In Rosen CJ (ed): "Osteoporosis and Metabolic Bone Disease [Clinics in Laboratory Medicine 20:3]" Philadelphia: W.B. Saunders Co., pp 455–468, 2000.
48. Bahannon AD: Osteoporosis and African American women. J Women’s Health Gend Based Med 8: 609–615, 1999.[Medline]
49. Nelson DA, Barondess DA, Hendrics SL, Beck TJ: Cross-sectional geometry, bone strength, and bone mass in the proximal femur in black and white postmenopausal women. J Bone Miner Res 15: 1992–1997, 2000.[Medline]

This article has been cited by other articles:

				D. A. Savaiano, C. J. Boushey, and G. P. McCabe Lactose Intolerance Symptoms Assessed by Meta-Analysis: A Grain of Truth That Leads to Exaggeration J. Nutr., April 1, 2006; 136(4): 1107 - 1113. [Abstract] [Full Text] [PDF]

				S. J. M. Ten Bruggencate, I. M. J. Bovee-Oudenhoven, M. L. G. Lettink-Wissink, M. B. Katan, and R. van der Meer Dietary Fructooligosaccharides Affect Intestinal Barrier Function in Healthy Men J. Nutr., January 1, 2006; 136(1): 70 - 74. [Abstract] [Full Text] [PDF]

				C. W Gunther, R. M Lyle, P. A Legowski, J. M James, L. D McCabe, G. P McCabe, M. Peacock, and D. Teegarden Fat oxidation and its relation to serum parathyroid hormone in young women enrolled in a 1-y dairy calcium intervention Am. J. Clinical Nutrition, December 1, 2005; 82(6): 1228 - 1234. [Abstract] [Full Text] [PDF]

				N. Boon, G. B. Hul, N. Viguerie, A. Sicard, D. Langin, and W. H. Saris Effects of 3 diets with various calcium contents on 24-h energy expenditure, fat oxidation, and adipose tissue message RNA expression of lipid metabolism-related proteins Am. J. Clinical Nutrition, December 1, 2005; 82(6): 1244 - 1252. [Abstract] [Full Text] [PDF]

				M. B. Zemel The Role of Dairy Foods in Weight Management J. Am. Coll. Nutr., December 1, 2005; 24(suppl_6): 537S - 546S. [Abstract] [Full Text] [PDF]

				N. Boon, L. L. J. Koppes, W. H. M. Saris, and W. Van Mechelen The Relation between Calcium Intake and Body Composition in a Dutch Population: The Amsterdam Growth and Health Longitudinal Study Am. J. Epidemiol., July 1, 2005; 162(1): 27 - 32. [Abstract] [Full Text] [PDF]

				I. R. Reid, A. Horne, B. Mason, R. Ames, U. Bava, and G. D. Gamble Effects of Calcium Supplementation on Body Weight and Blood Pressure in Normal Older Women: A Randomized Controlled Trial J. Clin. Endocrinol. Metab., July 1, 2005; 90(7): 3824 - 3829. [Abstract] [Full Text] [PDF]

				C. W Gunther, P. A Legowski, R. M Lyle, G. P McCabe, M. S Eagan, M. Peacock, and D. Teegarden Dairy products do not lead to alterations in body weight or fat mass in young women in a 1-y intervention Am. J. Clinical Nutrition, April 1, 2005; 81(4): 751 - 756. [Abstract] [Full Text] [PDF]

				H. Y. Lovelace and S. I. Barr Diagnosis, Symptoms, and Calcium Intakes of Individuals with Self-Reported Lactose Intolerance J. Am. Coll. Nutr., February 1, 2005; 24(1): 51 - 57. [Abstract] [Full Text] [PDF]

				R. J. F. Loos, T. Rankinen, A. S. Leon, J. S. Skinner, J. H. Wilmore, D. C. Rao, and C. Bouchard Calcium Intake Is Associated with Adiposity in Black and White Men and White Women of the HERITAGE Family Study J. Nutr., July 1, 2004; 134(7): 1772 - 1778. [Abstract] [Full Text]

				M. B Zemel Role of calcium and dairy products in energy partitioning and weight management Am. J. Clinical Nutrition, May 1, 2004; 79(5): 907S - 912S. [Abstract] [Full Text] [PDF]

				S. J Parikh and J. A Yanovski Calcium intake and adiposity Am. J. Clinical Nutrition, February 1, 2003; 77(2): 281 - 287. [Abstract] [Full Text] [PDF]

				D. Teegarden Calcium Intake and Reduction in Weight or Fat Mass J. Nutr., January 1, 2003; 133(1): 249S - 251. [Abstract] [Full Text] [PDF]

This Article Abstract Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Buchowski, M. S. Articles by Johnson, A. O. Search for Related Content PubMed PubMed Citation Articles by Buchowski, M. S. Articles by Johnson, A. O.