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Food Sources of Calcium / 199 InternationalJournalofSportNutritionandExerciseMetabolism,2001,11,199-208 © 2001 Human Kinetics Publishers, Inc. FoodSourcesofCalciuminaSample ofAfrican-AmericanandEuro-American CollegiateAthletes DeborahLeachmanSlawson,BarbaraS.McClanahan, LindaH.Clemens,KennethD.Ward,RobertC.Klesges, ChristopherM.Vukadinovich,andEdwinD.Cantler Adequate calcium intake is integral to bone health as well as for optimal athletic performance. This study was conducted to investigate: (a) food sources of calcium in a sample of collegiate athletes, (b) gender and/or ethnic differences in food sources of calcium, and (c) whether athletes that derive less of their calcium intake from dairy sources increase their calcium intake from supplements or other food sources. Participants were African-American and Euro-American NCAA Division 1-A athletes. Eighty-five men and 59 women participated. Calcium intake for the previous 7-day period was assessed with a brief calcium screen. Men consumed significantly more calcium than women (1,354 vs. 898 mg/ day), with female cross-country runners exhibiting the lowest average intake (605 mg/day). Both men and women obtained the majority of their calcium from dairy products and mixed dishes, while men consumed significantly more calcium-fortified foods. Several gender and ethnic interactions for calcium intake from food groups were found. Mean total dairy calcium intake was found to vary according to total calcium intake in men, and supplemental calcium was not used to augment low dairy intakes of calcium in any group. While African-Americans and Euro-Americans athletes were consuming similar levels of calcium, the female athletes in the sample did not get adequate amounts. Key Words: nutrition, sports, diet, race, gender Adequate calcium intake is necessary for general health and well being, as well as for optimal athletic performance. To date, no ergogenic qualities have been attributed to calcium supplementation, but it is clear that inadequate intake may impair skeletal integrity, nerve impulse transmission, maintenance of membrane potential, and muscle contraction (7). In an early study, Drinkwater et al. (8) found that too little D. Leachman Slawson, B.S. McClanahan, K.D. Ward, R.C. Klesges, and C.M. Vukadinovich are with The Center for Community Health at the University of Memphis, Memphis, TN 38152. L.H. Clemens is with the Department of Consumer Science and Education at the University of Memphis. E.D. Cantler is with the Department of Intercollegiate Athletics at the University of Memphis. 199 200 / LeachmanSlawsonetal. calcium in the diet could be a major contributor to bone loss in otherwise healthy female athletes. The severity of conditions associated with compromised skeletal health and inadequate calcium intake heighten the need to identify groups that may be at increased risk for the potential adverse consequences of inadequate calcium intake. Athletes, particularly women in weight-conscious sports, appear to be such a group. In spite of increased physiologic demands that may lead to additional pathways for calcium loss, there is evidence that athletes consume less than the current Daily Reference Intake (DRI) for calcium (1, 7, 16, 27). The DRI for 19–30 year-olds is 1,000 mg/day (11). Further, the NIH Consensus Conference on Optimal Calcium Intake has recommended the intakes for adolescents and young adults be set at 1,500 mg/day (29). At particular risk for low calcium intake are those athletes who strive to achieve low body fat, those who are involved in excessive training programs, and those who have inadequate energy intake (10). Additionally, it appears that calcium intake may be related to stress fracture risk. For example, Myburgh et al. (28) found that athletes with confirmed stress fractures had lower calcium intakes than did activity-matched athletes with no history of fractures. In addition, those with stress fractures reported a history of low intakes of dairy products, suggesting that calcium intake may influence the incidence of stress fractures in athletes (28). These findings point to the need to investigate the adequacy of calcium intakes in certain athletes who may be at increased risk of inadequate intake. For example, many female athletes have been shown to consume less than the Recommended Dietary Allowance of calcium (7). Low calcium intake in young adulthood is of particular concern given that this stage in the lifespan is one of the prime times for optimizing bone density, and women, particularly Euro-American women, are at greater risk for developing osteoporosis in later years (5). While osteoporosis is less common in African-Americans (23), several investigators have related low calcium intakes with the development of hypertension (12, 19, 21, 25), a potentially life-threatening condition prevalent in the older AfricanAmerican population (20). Eck and Hackett-Renner (9) found that African-American children and adolescents consistently consumed less calcium than did Euro-American children and adolescents. Similarly, Looker et al. (22) found that, in the general U.S. population, African-Americans of both genders had the lowest calcium intake of several ethnic groups. Given that dairy foods are a primary source of calcium for this ethnic group (3, 22), the prevalence of lactose intolerance in African-Americans (31) may have a large negative effect on calcium intake in this population. Further, while the majority of calcium intake for both ethnic groups is derived from dairy foods (3, 22), the perception of dairy products as being high in fat may influence their intake (17). This possibility is illustrated in an investigation of changes in calcium intake in youth, where girls of both ethnic groups, aged 13–18 years old, consumed almost 200 mg/day less calcium than girls 6–7 years old (9). Additionally, calcium intake in that study steadily decreased as age increased, with the most dramatic decrease seen between the ages of 11–12 and 13–18. Given that calcium intake plays an integral role in multiple physiologic responses to increased physical workloads, and is necessary for the optimization of long-term health outcomes, the purpose of this study was three-fold: (a) to add to the existing body of literature by documenting calcium intake in athletes involved in sports with differing physiologic requirements; (b) to examine ethnic and gender variations in dietary sources of calcium in athletes; and (c) to examine issues of dietary Food Sources of Calcium / 201 compensation and supplementation in athletes with low intakes of dairy foods. Methods Participants were 145 collegiate athletes (86 males and 59 females) representing five menʼs teams (basketball, football, golf, soccer, track/cross-country) and five womenʼs teams (basketball, golf, tennis, track/cross-country, volleyball). All participants were volunteers and were not financially compensated for their participation. The average age for female participants was 19.6 years (range: 18–23), and for males, 20.3 years (range: 18–24). These team selections represent a spectrum of physiologic requirements in relation to differences in exertion, sweat loss, and weight-bearing skeletal impact. Overall, males represented 59.3% of the sample. Of the male athletes, 66% were Euro-American and 34% African-American. Of the female athletes, 63% were Euro-American, and 37% were African-American. A calcium checklist developed by Hertzler and Frary (13) was used to assess calcium intake. This measure was developed for use with adolescents and has been shown to compare well to food recalls and records (13). For this study, this measure was used in its entirety and included three additional items that were used to query the intake of locally available foods fortified with calcium (orange juice, bread, light bread). Using food models to demonstrate serving sizes, a member of the research team administered all assessments. Participants were asked to report the number of times each food had been consumed over the previous 7 days. All measures were checked Table 1 Foods/Beverages Included on the Calcium Checklist Mixed dishes: cream soups/sauces; macaroni and cheese; pizza or quiche; Milk, yogurt: cheese, cottage cheese; milk or cocoa; soy milk; yogurt; Dairy desserts: custard, pudding, cream pie; ice cream, frozen yogurt, milk shake; Fruits and vegetables: broccoli or cooked greens (beet/turnip greens, kale, collards, spinach); other vegetables; fruits; Grains: bread or cereal; biscuit/roll, or corn tortilla; muffin, cornbread, or doughnut; rice, noodles, or pasta; pancake, waffle, or French toast; Calcium-fortified foods: orange juice with calcium added, bread with calcium added; light bread with calcium added; Protein foods: dried beans, cooked (navy, pinto, kidney); meat, fish, poultry; peanuts, egg; salmon with bones or sardines with bones; shrimp or oysters; tofu; Miscellaneous: cake; beer; colas; chocolate; Supplements: Subjects were asked if they had taken any vitamin/mineral supplements in the past 7 days. If they responded affirmatively, they were asked to list the type of supplement and how many they had taken in the 7 days covered. Note. Subjects were instructed to report how many times they had consumed each item in the previous 7 days. 202 / LeachmanSlawsonetal. for completeness before each participant left the laboratory. Foods on the checklist were then collapsed into the following categories: mixed dishes, milk/yogurt, dairy desserts, fruits/vegetables, grains, calcium-fortified foods, protein foods, miscellaneous foods, and supplements. Table 1 provides a list of foods in each grouping. Results TeamEffects Table 2 presents average daily calcium intakes by gender and sports team, with the percent of participants by team reporting calcium intakes less than two thirds of the Daily Reference Intake (DRI) of 1,000 mg/day. Supplemental calcium also is included in the mean calcium intakes listed. Female cross-country runners consumed the least calcium, with an average of 605 mg/day, and the majority of these athletes reported calcium intakes less than two thirds of the DRI. Conversely, male basketball players consumed the most calcium, with a mean of 1,730 mg/day, with none of these athletes reporting calcium intakes Table 2 Mean Daily Calcium Intakes by Gender and Sport, With Percent of Participants Reporting Calcium Intakes Less Than Two Thirds of DRIa (N = 145) Variable Men Basketball Football Golf Soccer Cross-country Indoor/outdoor track Subtotals for men: Women Basketball Golf Tennis Cross-country Indoor/outdoor track Volleyball Subtotals for women: n % of total sample Mean calcium intake (mg/day)b Percent below two thirds DRI 10 24 11 21 7 13 86 6.9 16.5 7.6 14.5 4.8 9.0 59.3 1730 1335 784 1367 1706 1369 1354 ± ± ± ± ± ± ± 867c 1003 292 560 1153d 1248 904e 0 16.7 45.4 4.8 14.3 15.4 15.1 13 7 6 12 12 9 59 9.0 4.8 4.1 8.3 8.3 6.2 40.7 1101 1052 849 605 974 804 898 ± ± ± ± ± ± ± 934 604 215 182 459 321 467 23.1 42.9 16.7 66.7 25.0 44.4 37.3 a Two-thirds of the Daily Reference Intake of 1,000 mg/day is 670 mg/day. Mean ± SD. c Significant difference between menʼs basketball and womenʼs cross-country (p = .022). d Comparison of menʼs and womenʼs cross-country teams (p = .083). e Significant difference between men and women overall (p = .0037). b Food Sources of Calcium / 203 below two thirds of the DRI. With the exception of the male golf team, calcium intakes of women on all teams were lower than those of the male teams. While the overall mean for male athletesʼ calcium intakes exceeded the DRI, 15% (one in seven) did not consume at least two thirds of the DRI. Further, one in three of the female athletes did not consume at least two thirds of the DRI. Team effects were investigated via an analysis of variance (ANOVA). The overall model was significant (F11,133 = 2.444, p = .008 with Tukey Honestly Significant Difference follow-up tests indicating a significant difference between womenʼs cross-country and menʼs basketball (p = .022), and a marginally significant difference between womenʼs and menʼs crosscountry teams (p = .083). SexandEthnicEffectsinSourcesofCalciumIntake Sex and ethnic differences in calcium intake were examined using 2-way ANOVA, with sex (male, female) and ethnicity (African-American, Euro-American) as main factors. Significant main effects and interactions were followed up using Tukeyʼs Honestly Significant Difference tests. Table 3 shows average daily calcium intake from each food group, reported for the previous 7-day period according to gender and ethnicity. Values are presented as mg/day, representing the mean for the 7-day period. There were no significant differences in total calcium intakes by race, though males had significantly higher intakes of total calcium than did females (1,354 vs. 898 mg/day, F1,141 = 8.73, p = .0037). When categories of calcium intake were examined separately, significant sex effects were observed for three categories, with males having higher intakes than females for mixed dishes (359 vs. 239 mg/day, F1,141 = 4.33, p = .04), calcium-fortified foods (220 vs. 130 mg/day, F1,141 = 3.70, p = .056) and protein foods (38 vs. 21 mg/day, F1,141 = 12.56, p = .0005). Sex by race interactions were observed for the milk/yogurt group (F1,141 = Table 3 Calcium Intake (mg/day) by Gender and Race (Mean ± SD) Men Variable EuroAmerican n = 57 AfricanAmerican (n = 29) Women EuroAfricanAmerican American (n = 37) (n = 22) Mixed dishes Milk/yogurt Dairy desserts Fruit/vegetables Grains Calcium-fortified foods Protein foods Miscellaneous Supplements 402 506 74 67 108 206 34 41 34 273 255 56 91 102 248 51 35 9 225 195 75 82 79 135 16 33 37 ± ± ± ± ± ± ± ± ± 287 592 84 56 86 292 29 31 127 Total dairy 984 ± 740 Total mean calcium/day 1,472 ± 962 ± ± ± ± ± ± ± ± ± 274 306 63 81 74 454 53 44 34 584 ± 487 1,120 ± 740 ± ± ± ± ± ± ± ± ± 224 165 91 68 48 158 14 39 76 496 ± 325 878 ± 434 262 255 89 46 91 122 28 31 8 ± ± ± ± ± ± ± ± ± 201 330 83 30 74 129 28 31 25 605 ± 489 930 ± 527 204 / LeachmanSlawsonetal. Figure 1 — Proportional intake of calcium from each food grouping by ethnicity: men. Figure 2 — Proportional intake of calcium from each food grouping by ethnicity: women. 4.32, p = .04), fruits/vegetables (F1,141 = 7.49, p = .007, and total dairy (F1,141 = 6.36, p = .013). Follow-up testing indicated that for milk/yogurt, Euro-American males had significantly higher intakes than did Euro-American females (p < .05). Looking at fruit/vegetable intake, African-American males had significantly higher intakes than African-American females. Finally, and perhaps most interestingly, a followup 1-way ANOVA revealed that, for total dairy intake, Euro-American males had significantly higher intakes than any other group (for all, p < .05). Figures 1 and 2 present an illustration of the proportional intake from each food grouping for each racial group for men and women, respectively. AnalysisofPotentialCompensationforLowDairyFoodIntake To investigate whether individuals compensated for low calcium intake from dairy foods by increasing intake from non-dairy calcium sources, participants were grouped by gender, and classified into tertiles of low, medium, and high dairy calcium intake. As body weight was associated with both total calcium intake (r = 0.311, p < .001) and calcium intake from dairy sources (r = 0.270, p = .001), an analysis of covariance (ANCOVA) was carried out for each tertiled gender group using body weight as a covariate. For men, there was a marginally significant, positive linear trend, such that greater dairy calcium intake was associated with greater non-dairy calcium intake Food Sources of Calcium / 205 (F2,82 = 2.680, p = .075). There were no significant trends noted for the women (F2,55 = 0.303, p = .740). Thus, there was little evidence that individuals with low dairy calcium intake compensated by increasing intake from other food groups. The same pattern of results emerged when subjects were excluded who were statistical outliers (≥3 SDs above the mean) on dairy calcium intake (n = 4). Further, subject groupings by tertile of dairy calcium intake were examined to determine whether individuals with low dairy calcium intake, compared to individuals with higher intake, were more likely to have used oral calcium supplements in the previous week. Among the three tertiles of dairy calcium intake, the percentage of subjects using oral supplements ranged from 12.5–16.0%, with daily doses ranging from 23–771 mg. These differences were not statistically significant [C2(2) = 0.25, p = 0.88]. Similarly, oral supplement use was not related to dairy calcium intake when the lowest two tertiles were combined and compared to the highest tertile [C2(2) = 0.23, p = .63]. Thus, subjects with a low intake of calcium from dairy sources did not compensate by taking calcium supplements. Discussion Similar to earlier reports in non-athletes (5), the men in the present investigation consumed more calcium than did the women. Average daily means were 1,354 and 898 mg for men and women, respectively; and while menʼs average intake exceeded the DRI, one out of seven failed to consume two thirds of the DRI. The women, on average, consumed slightly below the DRI of 1,000 mg/day, and a full 37% consumed less than two thirds of the DRI. Concerning sources of calcium intake, men consumed significantly more calcium from mixed foods, calcium-fortified foods, and protein foods. Overall, men tended to obtain the majority of their calcium from dairy products (848 mg), mixed dishes (359 mg), and calcium-fortified foods (220 mg). While women also consumed the majority of their calcium via dairy products (536 mg) and mixed dishes (238 mg), their total intake of calcium remained below the DRI. The observed low calcium intakes in female athletes are in agreement with previous reports of low calcium intake in both athletic women (1, 7, 16, 27) and non-athletic women (15). Such findings are particularly troubling, since there are more pathways for calcium loss in athletes, and given the recommendations of the NIH Consensus Conference on Optimal Calcium Intake (29), which suggest optimal calcium intakes for adolescents and young adults as 1,500 mg/day, a level that is 500 mg greater than the DRI. This group of women consumed roughly 60% of the level recommended by the NIH, suggesting that these female athletes may be at increased risk for compromised skeletal integrity. This finding is even more alarming for those athletes who seem to be most prone to low calcium intake and, subsequently, lowered bone density (1, 7, 16, 27). Of particular concern are those athletes who frequently participate in long endurance, impact-loading activities such as jogging. Frequent participation in such activities has been associated with compromised bone health by several investigators (2, 4, 14, 24, 26). The female cross-country runners in this sample averaged the lowest calcium intake of all teams (605 mg/day) and thus may be at increased risk for low bone density. Although both Euro-American and African-American men consumed more than the DRI at a mean intake of 1,476 mg/day and 1,120 mg/day, respectively, 15.1% (one in seven) of the male athletes reported calcium intakes less than two thirds of the DRI. This level of intake may be inadequate to prevent exercise-related bone loss 206 / LeachmanSlawsonetal. (28). Similarly, preliminary research in our laboratory found evidence of exerciserelated bone mineral loss among male basketball players that was more pronounced at calcium intakes of less than 2,000 mg/day (18). Therefore, it is plausible that the DRI, which is designed to address the needs of most Americans, may not represent an adequate goal for athletes. Interestingly, while the Klesges et al. (18) investigation was conducted under conditions that would promote increased dermal losses of calcium through perspiration, the observed bone loss was subsequently reversed by supervised calcium supplementation. Given that the male athletes in the current investigation were consuming calcium at levels much lower than 2,000 mg per day and did not use supplementation to augment their calcium intakes, it is possible that these athletes might be losing bone mass. While no specific U.S. standards currently exist for athletes for calcium intake, this study underscores the need to investigate athletesʼ requirements as they relate to differing physiologic requirements of sport-specific activities. Increased pathways for calcium loss associated with athletic participation suggest that calcium intake and possibly calcium supplementation should be important considerations for all athletes. However, athletes typically take part in nutrient supplementation in hopes of improving athletic performance (30). To date, calcium supplementation has not been associated with any ergogenic qualities, and many athletes may fail to understand the long-term consequences of inadequate calcium intake. Thus, it is important to educate athletes about the importance of adequate calcium intake in order to promote skeletal integrity and possibly to reduce the risk of stress fractures. Further, investigations should be pursued to determine which athletes may be at greatest risk for bone loss, and at what level supplementation may mediate that loss. Contrary to other investigations (9, 22), African-Americans and Euro-Americans in this sample were consuming a similar level of calcium. There were several gender and ethnic differences in sources of intake. African-American men consumed more calcium from the fruit/vegetable group than did African-American women. Euro-American men were consuming more calcium from the milk/yogurt group than were any of the other three groups. This finding may indicate that the young women in this sample avoided dairy products as a way of controlling total energy and fat intake, as has been observed in other studies (9, 17). When the sample was stratified based on total dairy calcium intake, there was no relationship between total dairy calcium intake and non-dairy calcium intake for women, and the relationship was only marginally significant for men. Thus, athletes did not compensate for low intakes of calcium from dairy foods by consuming food from other groups. Athletes from the three tertiles of total dairy calcium intake did not differ in their use of calcium supplements, indicating that athletes who consumed a relatively low amount of dairy products did not attempt to compensate either from non-dairy calcium sources or from calcium supplements. Although this study provides information on the food sources of calcium and compensation for low intake from dairy foods, several design issues limit the study. First, we elected to study only calcium intake. Although it is clear that other nutrients are important in bone health, we felt that calcium intake held the most promise for developing educational strategies to positively impact bone health. That is, other nutrients (e.g., phosphorus) are important but may be less amenable to education efforts. Furthermore, calcium content of foods is easy to understand and is probably more salient to this age group. Other issues, such as the absorption rate of calcium and bone mineral density, also were not evaluated in this study. Such information Food Sources of Calcium / 207 would require more extensive laboratory analyses and was not the focus of this study. Lastly, our sample was limited to NCAA Division 1-A athletes at the university level, and further work is needed to determine how well these results generalize to athletes at other competitive levels and other ages. In summary, it appears that college-age female athletes are not getting adequate calcium. Further, while college-age male athletes are generally surpassing the DRI for calcium, one in seven were consuming calcium at levels less than two thirds of the DRI. Neither male nor female athletes reached the level of calcium intake recommended by the NIH Consensus Conference (29). Furthermore, African-American athletes were consuming a level of calcium similar to that of the Euro-American athletes. 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