Bone mineral density and body composition in boys with distal forearm fractures: A dual-energy x-ray absorptiometry study Ailsa Goulding, PhD, FACN, Ianthe E. Jones, MSc, Rachael W. Taylor, BSc, PhD, Sheila M. Williams, BSc, Dip Sci, and Patrick J. Manning, MBChB, FRACP Objective: To determine whether boys with distal forearm fractures differ from fracture-free control subjects in bone mineral density (BMD) or body composition. Study design: A case-control study of 100 patients with fractures (aged 3 to 19 years) and l00 age-matched fracture-free control subjects was conducted. Weight, height, and body mass index were measured anthropometrically. BMD values and body composition were determined by dual-energy x-ray absorptiometry. Results: More patients than control subjects (36 vs l4) were overweight (body mass index >85th percentile for age, P < .001). Patients had lower areal (aBMD) and volumetric (BMAD) bone mineral density values and lower bone mineral content but more fat and less lean tissue than fracturefree control subjects. The ratios (95% CIs) for all case patients/control subjects in age and weight-adjusted data were ultradistal radius aBMD 0.94 (0.91-0.97); 33% radius aBMD 0.96 (0.93-0.98) and BMAD 0.95 (0.910.99); spinal L2-4 BMD 0.92 (0.89-0.95) and BMAD 0.92 (0.89-0.94); femoral neck aBMD 0.95 (0.92-0.98) and BMAD 0.95 (0.91-0.98); total body aBMD 0.97 (0.96-0.99), fat mass 1.14 (1.04-1.24), lean mass 0.96 (0.93-0.99), and total body bone mineral content 0.94 (0.91-0.97). Conclusions: Our results support the view that low BMC, aBMD, and BMAD values and high adiposity are associated with increased risk of distal forearm fracture in boys. This is a concern, given the increasing levels of obesity in children today. (J Pediatr 2001;139:509-15)
Fractures of the distal forearm are common in children and adolescents.1,2 At this age, about 25% of all fractures occur at this site.3 In adults,
low bone mineral density (BMD) weakens bone and increases the risk of fracture. We have postulated that this is likely to be true in children. No
From Departments of Medical and Surgical Sciences, Human Nutrition, and Preventive and Social Medicine, the University of Otago Medical School, Dunedin, New Zealand.
Supported by Health Research Council of New Zealand. Submitted for publication Nov 3, 2000; revision received Feb 2, 2001; accepted Apr 5, 2001. Reprint requests: Ailsa Goulding, PhD, FACN, Department of Medicine, University of Otago, PO Box 913, Dunedin, New Zealand. Copyright © 2001 by Mosby, Inc. 0022-3476/2001/$35.00 + 0 9/21/116297 doi:10.1067/mpd.2001.116297
previous dual-energy x-ray absorptiometry studies of bone density or body composition in young boys with broken forearms appear to have been undertaken. However, we recently aBMD BMAD BMC BMD BMI
Areal bone mineral density Bone mineral apparent density Bone mineral content Bone mineral density Body mass index
carried out a case-control study of bone density and body composition in 200 young girls using this technique to determine whether patients with forearm fractures had lower bone density than fracture-free control subjects. We showed that young girls with fractures had lower areal bone mineral density (aBMD) throughout their skeletons than the control subjects.4 More than one third of our patients had low spinal density. Moreover, an unexpectedly high proportion of our patients with fractures tended to be overweight, with twice as many patients as expected having body mass index (BMI) values above the 85th
See related articles, p 473, p 494, p 516, and p 522. percentile for age (30%). This suggested that overweight children may have an increased risk for breaking their forearms in comparison with children of healthy body weight. Overweight children have lower bone area and mass for their weight than lighter children.5 Furthermore, chil509
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THE JOURNAL OF PEDIATRICS OCTOBER 2001
Table I. Characteristics of study participants
Age (y) Height (cm)† Weight (kg) BMI (kg/m2)† Lean mass (kg) Fat mass (kg) % Fat† Total body BMC (kg) Total body bone area (cm2)† Total body aBMD (g/cm2) Ultradistal radius aBMD (g/cm2) 33% radius aBMD (g/cm2) 33% radius BMAD (g/cm3) Femoral neck aBMD (g/cm2) Femoral neck BMAD (g/cm3) Hip trochanteric aBMD (g/cm2) L2-4 spinal aBMD (g/cm2)† L2-4 spinal BMAD (g/cm3)
Patients with fractures* (n = l00)
Control subjects* (n = 100)
12.0 (3.7) 150.7 (21.0) 48.1 (19.2) 20.21 (4.22) 34.38 (12.86) 11.44 (9.55) 21.85 (11.07) 1.722 (0.737) 1722 (556) 0.964 (0.121) 0.301 (0.067) 0.526 (0.109) 0.110 (0.018) 0.922 (0.136) 0.199 (0.029) 0.789 (0.137) 0.813 (0.175) 0.141 (0.017)
12.0 (3.7) 151.4 (22.0) 45.9 (18.4) 19.03 (3.03) 35.27 (13.76) 8.28 (6.11) 17.30 (7.41) 1.792 (0.832) 1743 (574) 0.985 (0.143) 0.316 (0.069) 0.544 (0.117) 0.115 (0.018) 0.955 (0.178) 0.209 (0.026) 0.818 (0.154) 0.875 (0.202) 0.153 (0.019)
Ratios of geometric means for cases/controls adjusted for age (95% CI) — 1.00 (0.98-1.01) 1.05 (0.99-1.10) 1.05 (1.01-1.10)‡ 0.98 (0.95-1.02) 1.27 (1.09-1.48)‡ 1.21 (1.08-1.36)‡ 0.97 (0.92-1.02) 0.99 (0.96-1.02) 0.98 (0.96-0.99)‡ 0.95 (0.91-0.98)‡ 0.97 (0.94-0.99)‡ 0.95 (0.92-0.99)‡ 0.96 (0.94-0.99)‡ 0.94 (0.91-0.98)‡ 0.97 (0.93-1.00) 0.93 (0.90-0.96)‡ 0.92 (0.89-0.95)‡
Ratios of geometric means for cases/controls adjusted for age and weight (95% CI) — 0.99 (0.98-0.999)‡ — 1.02 (1.003-1.04)‡ 0.96 (0.93-0.99)‡ 1.14 (1.04-1.24)‡ 1.14 (1.04-1.25)‡ 0.94 (0.91-0.97)‡ 0.97 (0.95-0.99)‡ 0.97 (0.96-0.99)‡ 0.94 (0.91-0.97)‡ 0.96 (0.93-0.98)‡ 0.95 (0.91-0.99)‡ 0.95 (0.92-0.98)‡ 0.95 (0.91-0.98)‡ 0.96 (0.93-0.99)‡ 0.92 (0.89-0.95)‡ 0.95 (0.91-0.99)‡
*Means (SD). †Also adjusted for age-squared. ‡Statistically significant P < .05.
dren who injure themselves when falling from playground equipment are heavier than children sustaining similar falls without injury.6 The purpose of our study was to determine whether young boys with distal forearm fractures have lower bone density, heavier body weight, or higher adiposity than fracture-free control subjects of similar age.
SUBJECTS AND METHODS
and May l999, to take part in our study. Children with these fractures are generally treated as outpatients, although some are admitted to hospital for manipulation of their bones under general anesthesia. All case patients received a light below-elbow cast. Boys were advised not to participate in contact sports, but no other restrictions were placed on their physical activity. They returned to school within a few days of fracture, and casts were removed after 4 to 6 weeks.
Patients with Fractures
Fracture-Free Control Subjects
In order to recruit l00 patients, we invited all boys aged 3 to 19 years with a Dunedin home address (n = 112) and distal forearm fractures (radius, ulna, or both) confirmed by x-ray films, who were discharged from our only hospital between March 1998
All patients with fractures were asked to supply the names of 3 friends of their own age: the first friend who had never fractured a bone at any time of his life and who agreed to take part as a fracture-free control subject was then enrolled. Our study sample of 100 case patients and l00 control sub-
510
jects had a power of 80% to detect a difference of 0.05 g/cm2 in spinal aBMD at the 5% level of significance.
Protocol The protocol was approved by the ethics committee of our hospital, and written consent for every participant was obtained from the parent or guardian accompanying each child during the study. A general health questionnaire was completed for each participant. Information was collected concerning medical history, current dietary calcium intake, and physical activity (hours per week spent in vigorous activity). The New Zealand recommended dietary allowances7 for calcium are 800 mg/d, 1200 mg/d, and 1000 mg/d for boys aged <12 years, 12 to 15 years, and >15 years, respectively. Children were also asked to rank their total current level of physical ac-
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THE JOURNAL OF PEDIATRICS VOLUME 139, NUMBER 4 Table II. Odds ratios for bone measures and weight measures (number with z score <–1 and >+1)
No. with z score <–1 Variables
Odds ratios (95% CIs)
Patients with fractures (n = 100)
Control subjects (n = 100)
Adjusted for age
Adjusted for age and weight
20 28 26 29 35 38 26 27 25 19 19 18
19 14 13 17 14 15 15 17 17 13 14 16
1.07 (0.53-2.15) 2.41 (1.18-4.94)* 2.35 (1.13-4.91)* 2.00 (1.01-3.93)* 3.31 (1.65-6.66)* 3.47 (1.76-6.87)* 2.01 (0.99-4.09) 1.81 (0.93-1.08) 1.64 (0.82-3.27) 1.58 (0.73-3.42) 1.46 (0.68-3.14) 0.56 (0.23-1.30)
1.26 (0.61-2.60) 2.63 (1.27-5.45)* 2.98 (1.40-6.37)* 2.07 (1.04-4.11)* 4.28 (2.06-8.87)* 3.84 (1.94-7.82)* 2.22 (1.08-4.59)* 1.77 (0.88-3.54) 1.80 (0.89-3.65) 1.89 (0.85-4.17) 1.89 (0.85-4.19) 0.23 (0.07-0.72)*
2.07 (1.03-4.15)* 0.56 (0.23-1.35) 3.19 (1.55-6.56)* 0.70 (0.30-1.61) 0.86 (0.39-1.86) 3.47 (1.69-7.09)* 1.64 (0.78-3.45) 0.29 (0.11-0.76)*
— 0.24 (0.08-0.72)* 3.17 (1.26-7.96)* 0.30 (0.10-0.88)* 0.49 (0.19-1.24) — 2.10 (0.97-4.55) 0.19 (0.06-0.54)*
Ultradistal BMC (g/cm) Ultradistal aBMD (g/cm2) 33% radius aBMD (g/cm2) 33% radius BMAD (g/cm3) L2-4 aBMD (g/cm2) L2-4 BMAD (g/cm3) Femoral neck aBMD (g/cm2) Femoral neck BMAD (g/cm3) Trochanteric aBMD (g/cm2) Total body aBMD (g/cm2) Total body bone mineral (kg) Lean tissue mass (kg)
No. with z score >+1 Total body weight (kg) Lean tissue mass (kg) Fat mass (kg) Total body bone mineral (kg) Height (cm) BMI Total body area (cm2) Total body aBMD (g/cm2)
28 9 32 11 14 35 12 6
16 15 13 15 16 14 15 18
*Statistically significant P < .05.
tivity relative to other children of the same age on a scale of 5 (1 = least active, 5 = most active). Tanner stages of puberty were determined by providing participants with pictures and written descriptions of the pubertal stages and asking the boys to select the stage that was closest to their own development.8 Trauma severity associated with fracture was graded according to the method of Landin3: severity was slight for falls to the ground from standing on the same level, moderate for falls of 0.5 to 3 m, and severe for falls exceeding 3 m.
Scanning Procedures Children were weighed (electronic scale) and measured (Harpenden stadiometer; Holtain Ltd, Croswell, Crymych, UK) without shoes in light
clothing. The radius, left hip, total body, and lumbar spine were scanned with a Lunar DPX-L scanner with software packages 1.35 and l.5e (Lunar Corp, Madison, Wis). Scanning was performed within 4 weeks of cast removal. We scanned the nondominant forearm of the 3 patients who fractured left and right forearms simultaneously; in the other 97 patients, forearm density was measured in the non-fractured forearm. In control subjects, scanning of the forearm was matched for dominance with each index case (dominant arm scanned in patient and control subject if nondominant arm fractured by patient; non-dominant arm scanned in patient and control subject if dominant arm fractured by patient). Our in vivo scanning precision is good.4 To mini-
mize effects of bone size, volumetric bone mineral apparent density (BMAD) was calculated from dualenergy x-ray absorptiometry information at the 33% radius and femoral neck as (BMC/area2) and at the lumbar spine L2-4 as (BMC/area1.5).9
Statistical Methods Results are presented as means (SD). Log transformation was undertaken for all anthropometric and scanning data. Each of the transformed variables was regressed on age by using data from the control group to derive the residual mean squares as a measure of the variability. The regression coefficients were used to compute the predicted values for both groups, and individuals whose observed values fell below or above l SD of the 511
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Figure. Ratios of geometric means with 95% CIs of all case patients and control subjects for total body lean mass, fat mass, and BMC in the total body, ultradistal radius, and 33% radius sites (age- and weight-adjusted data).
predicted values were attributed z scores below –1 or above +1. Table I displays means (95% CIs) and ratios of age-adjusted geometric means. Table II shows odds ratios or relative ratios derived from logistic regression.
RESULTS Recruitment We recruited 104 of 112 case patients with distal forearm fracture who were seen consecutively (92.9% participation). Non-white subjects (n = 4) were excluded because of difficulties in recruiting control subjects of the same ethnicity. We approached 110 fracture-free boys to act as control subjects and enrolled 102. Two were excluded because they were unsuitable age matches for their case patients.
General Health and Age of Participants The participants were generally in good health, and there were no significant group differences regarding use of medications or conditions affecting bone health. Fractures peaked between 11 and 15 years of age (57% of all frac512
tures); the numbers of case patients in each l-year age group from age 3 to 19 years were as follows: 1, 2, 5, 6, 5, 3, 6, 5, 10, 10, 16, 8, 13, 5, 1, 0, and 4.
Fracture History Ninety-seven boys broke a single forearm and 3 boys broke both. Trauma associated with fracture was mild in 65 cases, moderate in 33 cases, and severe in 2 cases.3 No fractures were due to car accidents. The most common activities associated with fracture were falls from play equipment or bikes (n = 29); falls when running, walking, or climbing (n = 25); rugby and other ball sports (n = 22); rollerblading, skateboarding, or snowboarding (n = 18); and play fighting/ fighting (n = 6). A high proportion of our case patients (42%) had already broken bones: 21 boys had one previous fracture, 9 had two, 5 had three, 5 had four, 1 had five, and 1 had six fractures.
Anthropometry and Pubertal Development Significantly more case patients than control subjects (36 vs 14, P < .001) were overweight,10 with 12 case pa-
tients and 6 control subjects being obese. Average BMI values, percentage fat, and fat mass were also higher in case patients than control subjects (Table I). By contrast, lean mass and bone mass were lower in case patients in the age- and weight-adjusted data (Table I and Figure). Table II shows that significantly more case patients than control subjects also had high values (z score >+l) for weight, fat mass, and BMI. High lean mass and high total body bone mineral content (BMC) were each significantly less common among case patients than among control subjects after adjustment for both age and weight, and low lean mass was also significantly more common among case patients in data adjusted for both age and weight (Table II). However, case patients and control subjects did not differ in age, height, or pubertal status. In the ageadjusted data, total body BMC was correlated appropriately (P < .001) with lean tissue mass in both case patients (r = 0.84) and control subjects (r = 0.85).
Bone Mineral Density Examination of the age-adjusted data revealed that average values for aBMD were lower in case patients than control subjects at every measured site except the hip trochanter (Table I). Furthermore, in age- and weight-adjusted data, all aBMD values were significantly lower. Thus, children with bone fractures have less bone mineral for a given bone area than their control subjects. Volumetric BMAD values were also lower in case patients than control subjects in the radius, hip, and spine, showing that reductions in aBMD were not due to smaller bone size. In addition, Table II shows that low aBMD and BMAD values (z score <–1) were significantly more common among case patients than control subjects at the ultradistal radius, 33% radius, and L2-4 spine in age-adjusted data. More than one third of the case patients had low
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THE JOURNAL OF PEDIATRICS VOLUME 139, NUMBER 4 spinal density. In age- and weightadjusted data, high total body BMD was also significantly less common in case patients than control subjects, providing further support for the view that case patients tend to have lower bone density for their weight more often than control subjects. Bone density values did not differ in children reporting slight trauma versus moderate or severe trauma (P = .9) or in boys with a history of previous fracture compared with boys who had a single fracture (P = .47).
Physical Activity Average hours per day of physical activity were similar in case patients (1.30 ± 0.89) and control subjects (1.30 ± 0.77), as were the mean global self-assessment scores of physical activity (case patients 3.2 ± 0.9 vs control subjects 3.4 ± 0.8). However, significantly more boys with BMI values >85th percentile had low scores (14 of 50) than did boys with BMI values <85th percentile (18/150) (χ2 [1 df] = 6.002, P < .015).
Dietary Calcium Average total dietary calcium intake (in milligrams per day) of all case patients and control subjects did not differ significantly (1136 ± 538 vs 1278 ± 618, P < .08), and there was no association between age-adjusted calcium intake and bone density. However, 50 case patients and 39 control subjects had calcium intakes below the recommended dietary allowances,7 and among boys aged 11 to 13 years (the middle third of our sample), case patients reported lower daily calcium intake than control subjects (1027 ± 488 vs 1295 ± 545, P < .028).
DISCUSSION These findings suggest that low bone density, high BMI, and high adiposity each increase fracture risk, consistent with our recent observations in young
girls.4 Our finding that aBMD is lower in case patients than control subjects is in agreement with a large body of work in adults11,12 and supports the view that less dense bone fractures more readily than stronger bone. The lower aBMD values of boys with fractures are not explained by differences in bone size, because volumetric BMAD measurements were also reduced. It is evident that many boys break bones repeatedly, because nearly half the case patients we enrolled (42%) already had a history of fracture. However, although adults with fractures tend to be lighter than fracturefree individuals,11 our study shows that a high proportion of boys with broken forearms are overweight, as is the case with girls.13 Overweight and obese fracture-free children have lower bone mass and bone area relative to their body weight than do children with healthy body weight.5 Others have found that in growing children body weight is more closely correlated with enlarged bone area than with increased BMC.14 Children do not gain weight and bone mineral synchronously during growth. Adult height and weight are achieved earlier than peak bone mass,15 and at the growth spurt, forearm areal density can actually decrease because bones enlarge more quickly than they gain mineral.16 Overweight children with fractures may show a particularly wide dissociation between bone mineral accrual and weight gain. This mismatch between weight and bone mineralization in overweight children may make them skeletally vulnerable and increase their propensity to sustain fractures.5 The mismatch is largely explained by excess adiposity rather than by reduced lean mass. The association of overweight with distal forearm fracture in children and adolescents, which we have now shown is present in both sexes, is a concern, given the rise in obesity occurring currently among children and adolescents in many parts of the world.17 Ortho-
pedic problems, such as tibia vara and slipped capitate epiphyses of the femur, are associated with childhood obesity.18 Our research now appears to link overweight in boys to an increased risk of forearm fractures. Weight-bearing is osteogenic19 and promotes bone gain in childhood,20-24 especially before puberty.25 In our study, inactivity in our patients with fractures may have contributed to their low bone density, their reduced lean mass for weight, and their high adiposity. More case patients than control subjects tended to rate their own physical activity levels as very low, and fewer case patients than control subjects tended to rate their activity as very high. Furthermore, significantly more low activity scores were reported by overweight boys than by lighter subjects, suggesting that low levels of exercise were associated with high adiposity in at least some of our study population. In our study, ageadjusted hours of vigorous physical activity were highly correlated with self-assessment scores of physical activity (r = 0.54, P < .00l). Genetic factors may also contribute to the high concurrence of overweight and low bone density in some patients with fractures because both bone density26 and obesity27 are strongly influenced by genetic factors. Fracture incidence peaked at l3 years of age, in accordance with the view that distal forearm fractures are more common just before the growth spurt28 when cellular remodeling of bone is increased greatly and skeletal calcium requirements for new bone formation are high.29 The cortex of the radius in children differs from adult bone,30 being less mineralized. During rapid growth, bone may also be removed from the cortex to provide mineral needed at the growth plate.31 This process could be accentuated by dietary calcium insufficiency. Many of our study children were consuming less dietary calcium than the current recommended dietary allowance for 513
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age, and values were lower in case patients than control subjects aged ll to 13 years. Thus, in some children, low dietary calcium consumption could have contributed to forearm fragility by stimulating rapid resorption of cortical bone to supply bone needs for calcium.31 Although the association of dietary calcium with bone density is controversial,32 habitual high calcium intake in youth is related to good peak adult bone density.33 Intervention studies in childhood have shown that both calcium supplementation34-36 and increased physical activity21,22,24 can increase bone density significantly in the short term. We restricted our control group to include only fracture-free subjects because although fractures are common adverse events in childhood, the majority of children and adolescents remain fracture-free throughout growth.3 We believe that our study population is representative of patients with distal forearm fractures in New Zealand because we recruited a very high proportion of consecutive case patients treated in the only hospital in our district. Furthermore, bias was not introduced by selecting case patients or control subjects of any particular body weight or adiposity. Pubertal development was similar in case patients and control subjects and was appropriate for age; thus, delayed puberty was not a contributory factor to low bone density. A distal forearm fracture in a child could be considered a useful “clinical sign” of possible low bone density. This should alert health professionals to offer children with these fractures lifestyle and nutritional advice37 to help increase bone density. We thank the staff of the Fracture Clinic of Dunedin Hospital and all participating children and their families for willing cooperation.
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50 Years Ago in the Journal of Pediatrics COMMENTS ON CURRENT LITERATURE: KEROSENE POISONING Blattner RJ. J Pediatr 1951;39:391-2 Fifty years ago, kerosene poisoning was an important clinical syndrome, and many of its features were starting to be studied scientifically. There was a considerable difference of opinion concerning the pathogenesis of the pulmonary injury that is a major feature of the syndrome. The controversy centered on whether the pulmonary injury was a result of pulmonary aspiration or gastrointestinal absorption of the hydrocarbon and hematogenous delivery. The answer to this question was clinically important because it would determine the role of gastric lavage in emergency therapy. In this article Russell J. Blattner comments on a recent study by Richardson and Pratt-Thomas entitled “Toxic Effects of Varying Doses of Kerosene Administered by Different Routes.”1 The study was performed in dogs and rabbits and entailed administration of kerosene by various routes: intragastric, intravenous, intratracheal, into a small segment of intestine, and intraperitoneal. Histologic examination of the lungs showed that although the pulmonary vascular changes were most severe with the intravenous route administration, small doses of kerosene administered intratracheally induced a severe pneumonia. Blattner concluded that aspiration is the most common and most serious feature of kerosene poisoning and urged caution in the use of gastric lavage in the emergency department. Robert W. Wilmott, MD Chair, Department of Pediatrics Cardinal Glennon Children’s Hospital St. Louis, MO 63104 9/37/118531 doi:10.1067/mpd.2001.118531
REFERENCE 1. Richardson JA, Pratt-Thomas HR. Toxic effects of varying doses of kerosene administered by different routes. Am J Med Sci 1951;221:531-6.
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