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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

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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

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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

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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

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