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Supplement: Nutritional Influences on Bone Growth in Children

Factors that Affect Bone Mineral Accrual in the Adolescent Growth Spurt^1,2

Susan J. Whiting^*,3, Hassanali Vatanparast^*, Adam Baxter-Jones, Robert A. Faulkner, Robert Mirwald and Donald A. Bailey^,**

^* College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, Saskatchewan Canada, S7N 5C9; College of Kinesiology, University of Saskatchewan, Saskatoon, Saskatchewan Canada, S7N 1M3; and ^** Department of Human Movement Studies, University of Queensland, Brisbane, Australia

³To whom correspondence should be addressed. E-mail: susan.whiting{at}usask.ca.

	ABSTRACT

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 
The development of bone mass during the growing years is an important determinant for risk of osteoporosis in later life. Adequate dietary intake during the growth period may be critical in reaching bone growth potential. The Saskatchewan Bone Mineral Accrual Study (BMAS) is a longitudinal study of bone growth in Caucasian children. We have calculated the times of maximal peak bone mineral content (BMC) velocity to be 14.0 ± 1.0 y in boys and 12.5 ± 0.9 y in girls; bone growth is maximal 6 mo after peak height velocity. In the 2 y of peak skeletal growth, adolescents accumulate over 25% of adult bone. BMAS data may provide biological data on calcium requirements through application of calcium accrual values to factorial calculations of requirement. As well, our data are beginning to reveal how dietary patterns may influence attainment of bone mass during the adolescent growth spurt. Replacing milk intake by soft drinks appears to be detrimental to bone gain by girls, but not boys. Fruit and vegetable intake, providing alkalinity to bones and/or acting as a marker of a healthy diet, appears to influence BMC in adolescent girls, but not boys. The reason why these dietary factors appear to be more influential in girls than in boys may be that BMAS girls are consuming less than their requirement for calcium, while boys are above their threshold. Specific dietary and nutrient recommendations for adolescents are needed in order to ensure optimal bone growth and consolidation during this important life stage.

KEY WORDS: • calcium intake • children • adolescents • calcium requirement • soft drinks • fruit and vegetables

Adolescence is a time of tremendous growth in height, characterized by the adolescence growth spurt, during which children gain physical, mental, and emotional maturity in a very short period of time. Our research interests have centered on how bone mineral is accrued during this time, as the development of peak bone mass during the growth years is considered an important determinant for future risk of osteoporosis in later life (1–3). Adequate nutrition to provide the building blocks for bone, and sufficient activity to provide the mechanical impetus for bone development, are critical factors in maximizing bone growth potential (3). Surprisingly, little is known about bone mineral accrual during adolescence as, until recently, few longitudinal studies have been undertaken to measure bone development through adolescence. Therefore, we present some of our findings to date and provide data to suggest that a healthy diet and lifestyle can lead to considerable mineral accrual through the adolescence. This gain in bone through adolescence can be used as a functional indicator for calcium requirements of adolescents.

	The Saskatchewan Bone Mineral Accrual Study (BMAS)4

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 
The Saskatchewan Pediatric Bone Mineral Accrual Study began in 1991, with over 220 male and female children ages 8 to 14 y, from 2 elementary schools in Saskatoon, giving informed consent for the study (4–7). Bone mineral was measured yearly until 1997. A subgroup of subjects has complete data spanning their age of peak height velocity. Nearly all subjects were Caucasian, living in a middle-class area of Saskatoon. All subjects and parent/guardians provided informed written consent, and the University of Saskatchewan Advisory Committee on Ethics in Human Experimentation approved the protocol. Bone measurements were obtained by annual dual-energy X-ray absorptiometry scans of the whole body, anterior posterior lumbar spine and proximal femur (QDR 2000, Hologic) as described elsewhere (5). Dietary intake over the 6-y collection period was assessed via serial 24-h recalls conducted both at the participation schools and in the hospital setting at the time of the bone scans. There were 2 to 4 recalls for each subject every year. All days of the week, except Friday and Saturday, were included. Similarly, activity assessment was conducted with each diet recall and consisted of a frequency questionnaire developed for our study (8,9). Table 1shows characteristics of the subgroup of subjects having bone mineral accrual data before and after age of peak height velocity.

	BMAS subjects provide reference group data for bone accrual

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

	Bone mineral accrual in adolescent boys and girls (BMAS)

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 
We previously published results on bone mineral accrual data through the adolescent growth spurt, initially from cross-sectional analysis (4) and later when longitudinal analysis was completed on 50 boys and girls (7). With the latter analysis, the age of maximal peak bone mineral content (BMC) velocity occurred at age 14.0 ± 1.0 y in boys and 12.5 ± 0.9 y in girls; boys gained, on average, 407 ± 92 g of bone mineral during each of the 2 y surrounding this age, while girls gained 322 ± 66 g. As more subjects are added to our analysis, we have slightly revised our calculations of age of peak bone mineral content of our BMAS cohort (Table 1).

Annual growth measures plotted over time, i.e., distance curves, are useful to illustrate the rapid accumulation of bone mineral content (measured as total body) during adolescence. In Figure 1, bone gain is shown as a function of chronological age. In contrast, Figure 2shows bone gain as a function of biological age, where age of zero is the age of peak height velocity. Age of peak height velocity is the most commonly used indicator of somatic maturity in longitudinal studies. In our cohort, girls gain less bone mineral at every age, and after age of peak height velocity there is a more rapid gain in bone by boys than by girls. By age 18 y (Fig. 1) males have 22% more BMC than do females. As discussed below, this gender difference may be biological or may be a result of the higher intake of calcium (6) and/or greater activity levels of BMAS boys compared to BMAS girls (9), or both. In comparing our BMC accrual data to data from other published studies, our data are similar to those of Danish children (11).

View larger version (13K): [in this window] [in a new window]   FIGURE 1 Total body bone mineral content (g) of the BMAS subjects at yearly age increments. Values are mean ± SEM. Subject numbers vary at each age point but were derived from 66 boys and 65 girls.

View larger version (13K): [in this window] [in a new window]   FIGURE 2 Total body bone mineral content (g) of the BMAS subjects at yearly age increments younger than (negative) or older than (positive) zero biological age (age of peak height velocity). Values are mean ± SEM Subject numbers vary at each age point but were derived from 66 boys and 65 girls.

	Finding estimates of calcium requirement using BMC accretion

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

In setting an AI for calcium for adolescent boys and girls, the Panel for the Dietary Reference Intakes for Calcium looked at 3 lines of evidence: a factorial approach, calcium retention using a nonlinear regression model, and results of clinical trials (11). The factorial calculation of calcium requirements for adolescents was for the 2 y of maximal peak bone mineral content accrual and involved summing estimates of calcium need and losses, specifically calcium retained in bone together with estimates of skin, urine, and fecal calcium losses. The values originally used for calcium retention, 212 mg for girls and 282 mg for boys, were those found by us from the cross-sectional analysis of bone mineral accrual within 2 y of peak bone mineral content accrual (4). Since that time, as indicated, we provided a more exact picture of BMC accrual using longitudinal rather than cross-sectional data (7). As shown in Table 2, estimates of calcium need during the 2 y of peak bone accretion increase to 1500 mg for girls, and 1700 mg for boys, assuming all other estimates of losses and absorption efficiency remain constant. This demonstrates that the need for calcium is greater during this 2-y window of bone accrual than previously estimated (11). However, it is important to note that subjects were consuming less dietary calcium during this time than the factorial calculation indicates was needed.

	Soft drink intake affects bone accrual of girls, not boys

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 
Two studies indicate that soft drink intake negatively impacts on bone mineral accrual of adolescent girls but not adolescent boys (15,16). The first of these was conducted on data from BMAS subjects (15). We examined the effect of soft drink consumption by our subjects on BMC and BMC accrual during the 2 y of maximal bone mineral gain. Subjects drank a variety of soft drinks, which we labeled low nutrient dense beverages; these included carbonated (cola and noncola) and noncarbonated, sugar-based beverages. While both boys and girls showed significant negative correlations between low nutrient beverages and fluid milk consumption, only girls showed negative correlation between bone mineral content accrual and low nutrient dense beverage intake. Recently, a study with >10 times as many subjects reported similar findings (16). Girls’ heel bone mineral density was significantly lower with carbonated beverage intake, whereas boys showed no significant effect. In this latter study, pubertal stage was not adjusted for, but 2 ages of children were examined, age 12 y and 15 y. Milk intake dropped as soft drink consumption rose for boys and girls. A difference in calcium intake was evident, with girls consuming, on average, less than 900 mg per day whereas boys’ intakes were >1000 mg. Replacement of a calcium-rich beverage (milk) by soft drinks was observed in both studies and is a plausible mechanism for at least some of the effect of soft drinks on bone accrual in female adolescents. These studies suggest that being below (i.e., girls) or above (i.e., boys) the calcium intake threshold determines vulnerability to dietary influences on bone accrual.

	Boys’ dietary needs for calcium may be different from those of girls

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 
As indicated, much less is known about calcium losses and absorption efficiencies of boys than girls. There are indications that boys and girls may have different efficiencies in handling of calcium, and that boys may be more efficient (14). Our beverage data (15) support gender differences in the effect of dietary change (e.g., replacement of milk by soft drinks) on bone accrual. It is possible that the boys’ need for calcium was being met by their calcium intake, and we find that mean intake of calcium by boys is greater than that by girls of similar age (Table 1). However, at age of peak height velocity, this difference was quite modest, with boys’ and girls’ mean calcium intakes differing by <200 mg. This suggests that the gender difference in response to soft drinks may be mediated by differences in calcium efficiencies that, in turn, determine the calcium intake threshold.

	Fruit and vegetable intake may affect bone accrual during adolescence

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 
There is evidence of a positive link between fruit and vegetable consumption and bone health (17–19). Two different studies of prepubertal girls indicate a similar protective effect on bone growth (20,21). As shown in Table 1, mean intake of the Vegetables and Fruit group of Canada’s Food Guide For Healthy Eating (22) falls below the recommended level of 5 servings per day for both boys and girls in BMAS. Our preliminary analysis of BMAS data suggested that girls consuming adequate amounts through adolescence showed a greater bone mineral trajectory than girls consuming fewer than 5 servings, whereas no similar relationship was seen when boys’ data were plotted. Understanding food intake patterns may be important in making dietary recommendations for optimal bone growth of adolescents.

	The challenges ahead

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 
There are a number of challenges in determining diet-bone relationships during growth. We have reported on the general trend of underreporting dietary energy (23) that may affect the accuracy of our nutrient intake measurements. A further concern is how to account for physical activity, as an interaction between nutrition and activity may exist for children. Our analysis to date does not support a specific interaction (24). However, we must contend with the likelihood that positive behaviors are linked and may track together through adolescence, making it difficult to separate effects. The difference in bone mineral accrual between boys and girls through stages surrounding pubertal development is striking, and further research is needed to understand this gender difference.

Collection of BMAS continues as we add to the adolescent cohort data on subjects for whom puberty has only recently occurred. Additionally, we are measuring the subjects as young adults. With the latter measurements, we hope to be able to answer 2 important questions: what is the age of final bone mineral accrual, and is there persistence in bone mineral accrual when subjects with adequate calcium intake through childhood and adolescence no longer maintain that dietary pattern? Based on this work and that of others, age- and gender-specific dietary and nutrient recommendations for adolescents are needed in order to ensure optimal bone growth and consolidation during this important life stage.

	FOOTNOTES

 
¹ Presented at the Nutrition and Bone Health Working Group program at the "American Society of Bone Mineral Research, 25th Annual Meeting," held in Minneapolis, MN, September 19–23, 2003. The Nutrition and Bone Health Working Group program was organized by Susan J. Whiting and was sponsored by The National Dairy Council. Supplement contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Dairy Council. Guest editors for the supplement publication were Susan J. Whiting, College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, Saskatchewan, and Frances A. Tylavsky, University of Tennessee, The Health Science Center, Memphis, TN.

² Supported by the Canadian Institutes of Health Research.

⁴ Abbreviations used: AI, adequate intake; BMAS, Saskatchewan Bone Mineral Accrual Study; BMC, bone mineral content; DRI, dietary reference intake.

	LITERATURE CITED

TOP ABSTRACT The Saskatchewan Bone Mineral... BMAS subjects provide reference... Bone mineral accrual in... Finding estimates of calcium... Soft drink intake affects... Boys’ dietary needs for... Fruit and vegetable intake... The challenges ahead LITERATURE CITED

 

1. Bailey, D. A. (1999) Prevention of osteoporosis: A pediatric concern. Rippe, J. M. eds. Lifestyle Medicine 1999:578-584 Blackwell Science Malden, MA. .

2. Matkovic, V., Jelic, T., Wardlaw, G., Ilich, J., Goel, P., Wright, J., Andon, M., Smith, K. & Heaney, R. (1994) Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis. J. Clin. Invest. 93:799-808.

3. Heaney, R. P., Abrams, S., Dawson-Hughes, B., Looker, A., Marcus, R., Matkovic, V. & Weaver, C. (2000) Peak bone mass. Osteoporos. Int. 11:985-1009.[Medline]

4. Martin, A. D., Bailey, D. A., McKay, H. A. & Whiting, S. (1997) Bone mineral and calcium accretion during puberty. Am. J. Clin. Nutr. 66:611-615.[Abstract/Free Full Text]

5. Bailey, D. A. (1997) The Saskatchewan pediatric bone mineral accrual study: Bone mineral acquisition during the growing years. Int. J. Sports Med. 18:S191-S194.

6. Iuliano-Burns, S., Whiting, S. J., Faulkner, R. A. & Bailey, D. A. (1999) Levels, sources, and seasonality of dietary calcium intake in children and adolescents enrolled in the University of Saskatchewan Pediatric Bone Mineral Accrual Study. Nutr. Res. 19:1471-1483.

7. Bailey, D. A., Martin, A., McKay, H., Whiting, S. & Mirwald, R. L. (2000) Calcium accretion in girls and boys during puberty: A longitudinal analysis. J. Bone Miner. Res. 15:2245-2250.[Medline]

8. Crocker, P. R., Bailey, D. A., Faulkner, R. A., Kowalski, K. C. & McGrath, R. (1997) Measuring general levels of physical activity: Preliminary evidence for the physical activity questionnaire for older children. Med. Sci. Sports Exerc. 29:1344-1349.[Medline]

9. Bailey, D. A., McKay, H. A., Mirwald, R. L., Crocker, P. E. & Faulkner, R. A. (1999) The University of Saskatchewan Bone Mineral Accrual Study: A six year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children. J. Bone Miner. Res. 14:1672-1679.[Medline]

10. Institute of Medicine (2002) Dietary reference intakes: energy, carbohydrates, fiber, fat, fatty acids, cholesterol, protein, and amino acids 2002 National Academy Press Washington, DC.

11. Molgaard, C., Thomsen, B. L. & Michaelsen, K. F. (1999) Whole body bone mineral accretion in healthy children and adolescents. Arch. Dis. Child. 81:10-15.[Abstract/Free Full Text]

12. Institute of Medicine (1997) Dietary reference intakes for calcium, magnesium, phosphorus, vitamin D, and fluoride 1997 National Academy Press Washington, DC.

13. Institute of Medicine (2001) Dietary reference intakes: Applications in dietary assessment 2001 National Academy Press Washington, DC.

14. Braun, M., Martin, B. R., Kern, M., McCabe, G. P., Peacock, M., Machtan, A., Liesmann, J., Kempa-Steeczko, A. & Weaver, C. M. (2003) Relationship of calcium intake and calcium retention in adolescent boys. J. Bone Miner. Res. 18:S104.

15. Whiting, S. J., Healey, A., Psiuk, S., Mirwald, R., Kowalski, K. & Bailey, D. A. (2001) Relationship between carbonated and other low nutrient dense beverages and bone mineral content of adolescents. Nutr. Res. 21:1107-1115.

16. McGartland, C., Robson, P. J., Murray, L., Cran, G., Savage, M. J., Watkins, D., Rooney, M. & Boreham, C. (2003) Carbonated soft drink consumption and bone mineral density in adolescence: the Northern Ireland Young Hearts project. J. Bone Miner. Res. 18:1563-1569.[Medline]

17. New, S., Bolton-Smith, C., Grubb, D. A. & Reid, D. M. (1997) Nutritional influences on bone mineral density: a cross-sectional study in premenopausal women. Am. J. Clin. Nutr. 65:1831-1839.[Abstract/Free Full Text]

18. Tucker, K. L., Chen, H., Hannan, M. T., Cupples, L. A., Wilson, P.W.F. & Kiel, D. P. (1999) Potassium, magnesium, and fruit and vegetable intakes are associated with greater bone mineral density in elderly men and women. Am. J. Clin. Nutr. 69:727-736.[Abstract/Free Full Text]

19. New, S., Robins, S. P., Campbell, M. K., Martin, J. C., Garton, M. J., Bolton-Smith, C., Grubb, D. A., Lee, S. J. & Reid, D. M. (2000) Dietary influences on bone mass and bone metabolism: further evidence of a positive link between fruit and vegetable consumption and bone health?. Am. J. Clin. Nutr. 71:142-151.[Abstract/Free Full Text]

20. Tylavsky, F. A., Holliday, K., Danish, R., Womack, C, Norwood, J. & Carbone, L. (2004) Fruit and vegetable intake is an independent predictor of bone size in early-pubertal children. Am. J. Clin. Nutr. in press.

21. Jones, G., Riley, M. D. & Whiting, S. (2001) Association between urinary potassium, urinary sodium, current diet, and bone density in prepubertal children. Am. J. Clin. Nutr. 73:839-844.[Abstract/Free Full Text]

22. Canada’s Food Guide to Healthy Eating. Health Canada 1992 Retrieved 05/14/2003 from: http:/www.hc-sc.gc.ca/nutrition.

23. Carter, L. M., Whiting, S. J., Drinkwater, D. T., Zello, G. A., Faulkner, R. & Bailey, D. A. (2001) Self-reported calcium intake and bone mineral content in adolescents. J. Am. Coll. Nutr. 20:502-509.[Abstract/Free Full Text]

24. Baxter-Jones, A.D.G., Faulkner, R. A. & Whiting, S. J. (2003) Interaction between nutrition and physical activity and skeletal health. New, S. Bonjour, J.-P. eds. Nutritional Aspects of Bone Health 2003:544-564 The Royal Society of Chemistry Cambridge, UK. Chapter 25.

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