Bone and Mineral. 19 (1992) 85-96 0169-6009/92/$05.00 0 1992 Elsevier Science Publishers B.V. All rights reserved.
85
BAM 00467
one mineral density during puberty in estern Canadian children
Susan K. Grimstona, Katherine Morrisonb, James A. Harderb and David A. HanleyC ‘Human Pqformance
Laboratory,
bAIberta Children’s Ilospital.
Faculty qf Physical Education,
University of Calgary, Alta., Canada
Calgary, Alta., Canada CDivisivrr of’ Endocrinology
and Metaboii,wn,
Faculty of Medicine, Foothills Hospital and University of Calgary, Calgary, Alla., Canada
(Received 16 September 1991) (Accepted 7 May 1992)
Sumssry To assess the influence of puberty 3vjdits associated changes in body weight and height on bone mineral density (BMD), 1Lmba: spine (L2- L4) and femoral neck BMD were measured in 74 healthy, active children (9-16 years) using dual-photon absorptiometry. Competitive swimmers were recruited to minimize the potential effect variabi;ity in mechanical loading regime may have on bone density of the lumbar spine. Tanner staging was used to ascess stage of puberty. Current dietary calcium intake was assessed by analysis of 6-day dietary records. Significant differences in spinal and femoral neck BMD occurred between early (Tanner 1 and 2) and late stages of puberty (Tanner 4 and 5), P ~0.05. A significant correlation was found between bone density and dietary calcium intake. However stepwise regression analyses demonstrated stage of puberty or body weight were the only factors which significantly affected spinal BMD, accounting for 77% and 68% of the variability respectively; while at the femoral neck, body weight accounted for 52% of the variability. These results demonstrate that when poten”ial interacliog factors arc controlled for through regression analyses, differences in BMD occur mainl) as a function of puberty and the associated gains in body weight.
Key words: Bone mineral density; Children; Puberty; Body weight; Calcium intake -
Introduction
One of the main risk factors identified for development of osteoporotic fracture is insufficient bone mass [l-8]. EXfortsto prevent osteoporotic fracture have thereCorrespondence to: David A. Hanley, M.D., FRCPC, Division Endocrinology and Metabolism, Faculty of Medicine, 3330 Hospital Drive N.W., Calgary, Alberta T2N 4N1, Canada.
86 fore focused on either maintaining existing bone mass in adults, minimizing bone mass loss in the elderly, or augmenting bone mass gains in the young [9-131. In general however, maximizing bone mass accretion during the years leading to skeletal maturity has been considered the best protection against osteoporosis and its related fractures [9,11,13]. A number of cross-sectional studies and the few longitudinal studies of bone mass in children have generally demonstrated an age-related increase in spinal and radial bone mass [W251. Some studies have shown gender-related differences [15-17,21-251 and most studies have shown associations between bone density, and body weight and/or height [14,17-261. Although the relationship between age and bone mass during childhood has been well documented, there is little information regarding the factors involved in augmenting bone mass and thus potential recommendations for increasing adult peak bone mass are not available. Hormonal changes during puberty and the nutritional status of children have been proposed as two important mechanisms for increasing bone mass during childhood [ 15,23,19,27,28]. Stage of puberty has been assessed using Tanner staging [ 17 19,20,26],testosterone concentration [18], and estimates of pubertal stage based on chronological age 1161.Results generally indicate pre-pubertal children to have significantly lower bone density than pubertal adolescents, but there remains considerable biological variability. Potential causes for the variability noted may include differences in physical activity levels and/or in the nutritional status of children studied. There have been few studies of children in which activity profiles have been extensively documented or controlled. Two recent studies used retrospective questionnaires to determine activity levels in children and found associations between BMD and both level of physical activity [29] and the time reported in weight-bearing activities [30]. Further detailed analyses of the role of physical activity during childhood would appear tm ; u Ln u- .,.xportant due to the known influence of mechanical load on the material properties of bone [31]. In addition there is a limited number of studies documenting the dietary calcium intake of the children measured for bone mineral density, and conclusions drawn by authors have been conflicting [14,17,32,33]. Some have reported a positive association between childhood dietary calcium intake and regional bone mass measurements [32,33], while others have found no such association [14,17]. Inconsistent consideration of interacting factors such as height and weight changes with calcium intake may provide some explanation for the conflicting results. A recent intervention stqdy has demonstrated a trend toward a positive influence of dietary calcium intake on bone mass accretion in adolescent females [12].This study was limited to ICyear-old females who had all reached menarche and by implication had advanced at least to the latter stages of pubertal development [27,34-361.Two years of dietary calcium intervention ranging from 270i 637 mgiday indicated a more pronounced increase in bone mass over time in the high calcium supplement group (1637 mg/day) compared to the low calcium
87
supplement group (270 mg/day). Although this paper demonstrated a positive influence of dietary calcium on bone mass in adolescent females, statistical significance to support the observed trend was not achieved. The possible influence of calcium on bone mass as children of both gender progress through the stages of puberty has yet to be adequately addressed. The purpose of the present study was to determine the relationship between bone mass accretion and stage of pubertal development in healthy children, participating in similar activity programs. The potential influence of calcium intake on bone mass acquisition in these children was also considered in the analysis of bone density changes during the formative years of childhood.
Subjects and Methods
Seventy-four healthy, physically active children (32 male and 42 female), aged bet;veen 9 and 16 years of age, participated in the study. Written consent was obt;ij.inedfrom children and their parents, in accordance with a protocol reviewed by t.he University of Calgary Conjoint Medical Ethics Committee. Sixty-seven of the children were recruited from a local swimming club and all had competed successfully on a regular basis at the provincial level. Coaches’ training recorded and childrens’ training logs indicated an average time spent in training of 15 h/ week. The remaining seven children were not involved in competitive swimming but did participate regularly in a variety of physical activities. Exclusion criteria included evidence of any medical problems known to affect bone health (e.g. malabsorptive gastrointestinal disease), chronic use of medications known to affect skeletal metabolism (e.g. glucocorticoid administration for asthma), and weight/height ratio below the 3rd or above the 97th percentile for North American children [37]. Puberty was assessed by Tanner staging during a complete medical examination. Assessment was made of pubic hair growth, breast (female) and genital (male) development as described previously [34-361. Basic anthropometric measurements of height and weight were included in the medical examination. Bone mineral density (BMD) was measured at the lumbar vertebrae (L2-L4) and femoral neck (FN) using dual-photon absorptiometry (BMC-LAB 22a, Novo Diagnostic Systems). Procedures for the measurement of lumbar and femoral neck BMD have been described previously [38]. The accuracy of repeated measures using this technique in our laboratory is 2-3%. Children and parents were given detailed instructions for completing a comprehensive dietary record. Subjects were asked to weigh, measure, de&be and record all ingested items (liquids and foods) over a specified 3-day period (one weekend and two week days). Parents and children returned the completed record to a registered dietitian, who reviewed it and then discussed it with the family for clarification and verification of estimated quantities and preparation of food A further 3 days of diet record keeping were then assigned and completed by each subject. The 6 days of diet records were then coded and analyzed using the
commercially available computer package, Nutritionist III (N-Squared Computing, Oregon). The data base provided had been expanded to include food items typical of the western Canadian diet. Dietary analyses included average daily energy intake (kcal/day), average daily calcium (Ca) intake (mg/day), and average daily intake of calcium derived from primary dairy products (DaCa; mg/day). Due to the potential for total dietary intakes to increase with increasing age and size of the children and the influence this may have on daily calcium intake, a calcium density was calculated for each child. Calcium density was computed and expressed as average daily Ca intake with respect to average daily caloric intake (mg Ca/kcal). Statistical analyses were carried out with the SPSS/PC program. Student’s Itests were used to compare swimmers and non-swimmers, and for comparison of males and females within each Tanner stage. One-way analysis of variance with Tukcy/b post hoc comparisons were conducted to compare variables with respect to Tanner staging uf puberty. Multiple regression analyses were run to establish the predictive power of measured variables for bone density, with consideration given to the effect of collinearity between variables. Statistical significance was concluded for probabilities of P co.05 Results
In our study there were no significant differences between swimmers and the seven non-swimmers for BMD or any other variable measured (data not presented). Since swimmers and non-swimmers were virtually identical for the Table 1
Comparisons between males and females for each stage of puberty (mean f SEM) TWWK~ stuye Gender
BMD L2-L,a (g HA/cm')
BMDFN
Ca density
(gHA/cm')
(mglkcal)
Height (cm)
Weight (kg)
38.3f 1.3 33.6f 2.2
I (~=13) (n=S)
M F
0.55* 0.02 OS8 t_0.05
0.68f 0.02 0.62f 0.02
0.53+ 0.05 0.612 0.05
148.0f 1.6 145.0f 4.2
2 (N= 3) (n--3)
M F
0.57f 0.03 0.641 0.04
0.72k 0.02 0.70* 0.03
0.46f 0.05 0.46f 0.11
148.3f 5.6 42.7f 1.6 147.7f 1.0 38.0f 0.4
3 (tt =3) (n= 8)
M F
0.62+ 0.02 0.63& 0.02
0.73f 0.03 0.65f 0.02
0.55f 0.05 0.60f 0.06
161.1rt 3.5 155.6+ 3.6
4 (~(-4) (n'8)
M F
0.74f 0.05 0.76+ 0.03
0.82a 0.06 0.78f 0.03
0.60_+0.05 0.58+ 0.04
174.8f 4.5' 60.1& 5.3" 158.9+ 2.1 48.4k 2.3
S (a=9)
M
0.83+_0.01
F
0.84f 0.01
0.87+_0.02 0.82a 0.02
0.58+ 0.04 0.57f 0.05
178.8+ I.4 69.24 2.6" 164.2+ 1.7 57.9* 1.4
(n=l8)
a P ~0.05 vs. females of the respective Tannerstage.
43.9f 3.1 40.84 1.7
89
measured variables, non-swim.mers were grouped with swimmers in further analyses. There were no significant differences between males and females for bone mineral density of the spine and femoral neck at any Tanner stage, however there was a trend for females to have greater spinal bone density and lower femoral neck bone density than males (Table 1). Small subject numbers for males in the later stages of puberty and for females in the early stages of puberty reduced the statistical power of these comparisons, which most likely accounted for the lack of statistical significance. However, since no significant differences were noted between males and females for the dependent variable of bone mineral density at any site at any stage of puberty, males and females were combined for comparisons of other variables as a function of puberty (Table 2). Although increasing the statistical power of our analyses, the combination of males and females within each Tanner stage does present a limitation and should be taken into consideration. Table 2 Physical and dietary characteristics of children according to stage of puberty (mean f SEM/[95% CL]) Tanner stage
Variable
1 (n = 18)
2
3
4
5
(n = 6)
(n = 11)
(n = 12)
(n = 27)
Age
(years)
10.6 f 0.2 [lO.l-11.11
11.0 + 0.8 [8.9-13.11
12.1 fr o.4b [I 1.L13.11
13.7 + 0.c [12.9-14.41
14.7 f 0.3” [14.2-15.31
Height
(cm)
146.9 + 1.6 [143.6-150.21
148.0 f 1.6 [143.8-152.21
157.1 f 2.gb [150.9-163.41
164.1 f 3.0’ [157.6-170.71
169.1 f 1.8” [165.4-172.81
Weight
(kg)
37.0 f 1.” [34.4-39.61
40.4 f 1.3 [37. I-43.61
41.6 + 1.5 [38.3-44.9]
52.3 f 2.8’ [46.2-58.31
61.8 f 1.7d [58.3-65.31
Energy (kcaljday)
2209 f 130 [ 1932-24871
2169 f 198 [I 539-27981
2440 f 219 [ 1935-29441
2332 + 120 [2069-25951
2559 + 177 [2 192-29261
Calcium (mg/day)
1228 f 117 [980-14771
1005 * 159 [499-15101
1433 &- 143 [I 105-17621
1350 f 83 [i i68-15321
1485 4 123 [1230-17401
Dairy (mg/day) calcium
910 f 125 [641-l 1791
1035 + 136
[156-8361
[721-13491
936 + 76 [768-l 1031
1077 * 100 [871-12841
Calcium(mg/kcal) density
0.55 f 0.04 [0.47-0.64]
0.46 f 0.05
0.59 f 0.05
[0.30-0.61]
[0.49-0.70]
0.58 f 0.03 [0.52-0.64]
0.58 f 0.03 (0.51-0.65]
’ P 60.05 vs Tanner
I, 2, 3.
b P
85
BAM 00467
one mineral density during puberty in estern Canadian children
Susan K. Grimstona, Katherine Morrisonb, James A. Harderb and David A. HanleyC ‘Human Pqformance
Laboratory,
bAIberta Children’s Ilospital.
Faculty qf Physical Education,
University of Calgary, Alta., Canada
Calgary, Alta., Canada CDivisivrr of’ Endocrinology
and Metaboii,wn,
Faculty of Medicine, Foothills Hospital and University of Calgary, Calgary, Alla., Canada
(Received 16 September 1991) (Accepted 7 May 1992)
Sumssry To assess the influence of puberty 3vjdits associated changes in body weight and height on bone mineral density (BMD), 1Lmba: spine (L2- L4) and femoral neck BMD were measured in 74 healthy, active children (9-16 years) using dual-photon absorptiometry. Competitive swimmers were recruited to minimize the potential effect variabi;ity in mechanical loading regime may have on bone density of the lumbar spine. Tanner staging was used to ascess stage of puberty. Current dietary calcium intake was assessed by analysis of 6-day dietary records. Significant differences in spinal and femoral neck BMD occurred between early (Tanner 1 and 2) and late stages of puberty (Tanner 4 and 5), P ~0.05. A significant correlation was found between bone density and dietary calcium intake. However stepwise regression analyses demonstrated stage of puberty or body weight were the only factors which significantly affected spinal BMD, accounting for 77% and 68% of the variability respectively; while at the femoral neck, body weight accounted for 52% of the variability. These results demonstrate that when poten”ial interacliog factors arc controlled for through regression analyses, differences in BMD occur mainl) as a function of puberty and the associated gains in body weight.
Key words: Bone mineral density; Children; Puberty; Body weight; Calcium intake -
Introduction
One of the main risk factors identified for development of osteoporotic fracture is insufficient bone mass [l-8]. EXfortsto prevent osteoporotic fracture have thereCorrespondence to: David A. Hanley, M.D., FRCPC, Division Endocrinology and Metabolism, Faculty of Medicine, 3330 Hospital Drive N.W., Calgary, Alberta T2N 4N1, Canada.
86 fore focused on either maintaining existing bone mass in adults, minimizing bone mass loss in the elderly, or augmenting bone mass gains in the young [9-131. In general however, maximizing bone mass accretion during the years leading to skeletal maturity has been considered the best protection against osteoporosis and its related fractures [9,11,13]. A number of cross-sectional studies and the few longitudinal studies of bone mass in children have generally demonstrated an age-related increase in spinal and radial bone mass [W251. Some studies have shown gender-related differences [15-17,21-251 and most studies have shown associations between bone density, and body weight and/or height [14,17-261. Although the relationship between age and bone mass during childhood has been well documented, there is little information regarding the factors involved in augmenting bone mass and thus potential recommendations for increasing adult peak bone mass are not available. Hormonal changes during puberty and the nutritional status of children have been proposed as two important mechanisms for increasing bone mass during childhood [ 15,23,19,27,28]. Stage of puberty has been assessed using Tanner staging [ 17 19,20,26],testosterone concentration [18], and estimates of pubertal stage based on chronological age 1161.Results generally indicate pre-pubertal children to have significantly lower bone density than pubertal adolescents, but there remains considerable biological variability. Potential causes for the variability noted may include differences in physical activity levels and/or in the nutritional status of children studied. There have been few studies of children in which activity profiles have been extensively documented or controlled. Two recent studies used retrospective questionnaires to determine activity levels in children and found associations between BMD and both level of physical activity [29] and the time reported in weight-bearing activities [30]. Further detailed analyses of the role of physical activity during childhood would appear tm ; u Ln u- .,.xportant due to the known influence of mechanical load on the material properties of bone [31]. In addition there is a limited number of studies documenting the dietary calcium intake of the children measured for bone mineral density, and conclusions drawn by authors have been conflicting [14,17,32,33]. Some have reported a positive association between childhood dietary calcium intake and regional bone mass measurements [32,33], while others have found no such association [14,17]. Inconsistent consideration of interacting factors such as height and weight changes with calcium intake may provide some explanation for the conflicting results. A recent intervention stqdy has demonstrated a trend toward a positive influence of dietary calcium intake on bone mass accretion in adolescent females [12].This study was limited to ICyear-old females who had all reached menarche and by implication had advanced at least to the latter stages of pubertal development [27,34-361.Two years of dietary calcium intervention ranging from 270i 637 mgiday indicated a more pronounced increase in bone mass over time in the high calcium supplement group (1637 mg/day) compared to the low calcium
87
supplement group (270 mg/day). Although this paper demonstrated a positive influence of dietary calcium on bone mass in adolescent females, statistical significance to support the observed trend was not achieved. The possible influence of calcium on bone mass as children of both gender progress through the stages of puberty has yet to be adequately addressed. The purpose of the present study was to determine the relationship between bone mass accretion and stage of pubertal development in healthy children, participating in similar activity programs. The potential influence of calcium intake on bone mass acquisition in these children was also considered in the analysis of bone density changes during the formative years of childhood.
Subjects and Methods
Seventy-four healthy, physically active children (32 male and 42 female), aged bet;veen 9 and 16 years of age, participated in the study. Written consent was obt;ij.inedfrom children and their parents, in accordance with a protocol reviewed by t.he University of Calgary Conjoint Medical Ethics Committee. Sixty-seven of the children were recruited from a local swimming club and all had competed successfully on a regular basis at the provincial level. Coaches’ training recorded and childrens’ training logs indicated an average time spent in training of 15 h/ week. The remaining seven children were not involved in competitive swimming but did participate regularly in a variety of physical activities. Exclusion criteria included evidence of any medical problems known to affect bone health (e.g. malabsorptive gastrointestinal disease), chronic use of medications known to affect skeletal metabolism (e.g. glucocorticoid administration for asthma), and weight/height ratio below the 3rd or above the 97th percentile for North American children [37]. Puberty was assessed by Tanner staging during a complete medical examination. Assessment was made of pubic hair growth, breast (female) and genital (male) development as described previously [34-361. Basic anthropometric measurements of height and weight were included in the medical examination. Bone mineral density (BMD) was measured at the lumbar vertebrae (L2-L4) and femoral neck (FN) using dual-photon absorptiometry (BMC-LAB 22a, Novo Diagnostic Systems). Procedures for the measurement of lumbar and femoral neck BMD have been described previously [38]. The accuracy of repeated measures using this technique in our laboratory is 2-3%. Children and parents were given detailed instructions for completing a comprehensive dietary record. Subjects were asked to weigh, measure, de&be and record all ingested items (liquids and foods) over a specified 3-day period (one weekend and two week days). Parents and children returned the completed record to a registered dietitian, who reviewed it and then discussed it with the family for clarification and verification of estimated quantities and preparation of food A further 3 days of diet record keeping were then assigned and completed by each subject. The 6 days of diet records were then coded and analyzed using the
commercially available computer package, Nutritionist III (N-Squared Computing, Oregon). The data base provided had been expanded to include food items typical of the western Canadian diet. Dietary analyses included average daily energy intake (kcal/day), average daily calcium (Ca) intake (mg/day), and average daily intake of calcium derived from primary dairy products (DaCa; mg/day). Due to the potential for total dietary intakes to increase with increasing age and size of the children and the influence this may have on daily calcium intake, a calcium density was calculated for each child. Calcium density was computed and expressed as average daily Ca intake with respect to average daily caloric intake (mg Ca/kcal). Statistical analyses were carried out with the SPSS/PC program. Student’s Itests were used to compare swimmers and non-swimmers, and for comparison of males and females within each Tanner stage. One-way analysis of variance with Tukcy/b post hoc comparisons were conducted to compare variables with respect to Tanner staging uf puberty. Multiple regression analyses were run to establish the predictive power of measured variables for bone density, with consideration given to the effect of collinearity between variables. Statistical significance was concluded for probabilities of P co.05 Results
In our study there were no significant differences between swimmers and the seven non-swimmers for BMD or any other variable measured (data not presented). Since swimmers and non-swimmers were virtually identical for the Table 1
Comparisons between males and females for each stage of puberty (mean f SEM) TWWK~ stuye Gender
BMD L2-L,a (g HA/cm')
BMDFN
Ca density
(gHA/cm')
(mglkcal)
Height (cm)
Weight (kg)
38.3f 1.3 33.6f 2.2
I (~=13) (n=S)
M F
0.55* 0.02 OS8 t_0.05
0.68f 0.02 0.62f 0.02
0.53+ 0.05 0.612 0.05
148.0f 1.6 145.0f 4.2
2 (N= 3) (n--3)
M F
0.57f 0.03 0.641 0.04
0.72k 0.02 0.70* 0.03
0.46f 0.05 0.46f 0.11
148.3f 5.6 42.7f 1.6 147.7f 1.0 38.0f 0.4
3 (tt =3) (n= 8)
M F
0.62+ 0.02 0.63& 0.02
0.73f 0.03 0.65f 0.02
0.55f 0.05 0.60f 0.06
161.1rt 3.5 155.6+ 3.6
4 (~(-4) (n'8)
M F
0.74f 0.05 0.76+ 0.03
0.82a 0.06 0.78f 0.03
0.60_+0.05 0.58+ 0.04
174.8f 4.5' 60.1& 5.3" 158.9+ 2.1 48.4k 2.3
S (a=9)
M
0.83+_0.01
F
0.84f 0.01
0.87+_0.02 0.82a 0.02
0.58+ 0.04 0.57f 0.05
178.8+ I.4 69.24 2.6" 164.2+ 1.7 57.9* 1.4
(n=l8)
a P ~0.05 vs. females of the respective Tannerstage.
43.9f 3.1 40.84 1.7
89
measured variables, non-swim.mers were grouped with swimmers in further analyses. There were no significant differences between males and females for bone mineral density of the spine and femoral neck at any Tanner stage, however there was a trend for females to have greater spinal bone density and lower femoral neck bone density than males (Table 1). Small subject numbers for males in the later stages of puberty and for females in the early stages of puberty reduced the statistical power of these comparisons, which most likely accounted for the lack of statistical significance. However, since no significant differences were noted between males and females for the dependent variable of bone mineral density at any site at any stage of puberty, males and females were combined for comparisons of other variables as a function of puberty (Table 2). Although increasing the statistical power of our analyses, the combination of males and females within each Tanner stage does present a limitation and should be taken into consideration. Table 2 Physical and dietary characteristics of children according to stage of puberty (mean f SEM/[95% CL]) Tanner stage
Variable
1 (n = 18)
2
3
4
5
(n = 6)
(n = 11)
(n = 12)
(n = 27)
Age
(years)
10.6 f 0.2 [lO.l-11.11
11.0 + 0.8 [8.9-13.11
12.1 fr o.4b [I 1.L13.11
13.7 + 0.c [12.9-14.41
14.7 f 0.3” [14.2-15.31
Height
(cm)
146.9 + 1.6 [143.6-150.21
148.0 f 1.6 [143.8-152.21
157.1 f 2.gb [150.9-163.41
164.1 f 3.0’ [157.6-170.71
169.1 f 1.8” [165.4-172.81
Weight
(kg)
37.0 f 1.” [34.4-39.61
40.4 f 1.3 [37. I-43.61
41.6 + 1.5 [38.3-44.9]
52.3 f 2.8’ [46.2-58.31
61.8 f 1.7d [58.3-65.31
Energy (kcaljday)
2209 f 130 [ 1932-24871
2169 f 198 [I 539-27981
2440 f 219 [ 1935-29441
2332 + 120 [2069-25951
2559 + 177 [2 192-29261
Calcium (mg/day)
1228 f 117 [980-14771
1005 * 159 [499-15101
1433 &- 143 [I 105-17621
1350 f 83 [i i68-15321
1485 4 123 [1230-17401
Dairy (mg/day) calcium
910 f 125 [641-l 1791
1035 + 136
[156-8361
[721-13491
936 + 76 [768-l 1031
1077 * 100 [871-12841
Calcium(mg/kcal) density
0.55 f 0.04 [0.47-0.64]
0.46 f 0.05
0.59 f 0.05
[0.30-0.61]
[0.49-0.70]
0.58 f 0.03 [0.52-0.64]
0.58 f 0.03 (0.51-0.65]
’ P 60.05 vs Tanner
I, 2, 3.
b P
