The authors have no conflict of interest.
Bone and Body Composition of Children and Adolescents With Repeated Forearm Fractures†
Article first published online: 22 AUG 2005
Copyright © 2005 ASBMR
Journal of Bone and Mineral Research
Volume 20, Issue 12, pages 2090–2096, December 2005
How to Cite
Goulding, A., Grant, A. M. and Williams, S. M. (2005), Bone and Body Composition of Children and Adolescents With Repeated Forearm Fractures. J Bone Miner Res, 20: 2090–2096. doi: 10.1359/JBMR.050820
- Issue published online: 4 DEC 2009
- Article first published online: 22 AUG 2005
- Manuscript Accepted: 15 AUG 2005
- Manuscript Revised: 8 JUL 2005
- Manuscript Received: 13 APR 2005
- wrist fractures;
- risk factors;
- milk symptoms;
DXA measurements in 90 children and adolescents with repeated forearm fractures showed reduced ultradistal radius BMC and BMD values and elevated adiposity, suggesting site-specific bone weakness and high body weight increase fracture risk. Symptoms to cow milk, low calcium intakes, early age of first fracture, and overweight were over-represented in the sample.
Introduction: Although many apparently healthy children fracture their forearms repeatedly during growth, no previous studies of their bone health and body composition have been undertaken. Nor has the prevalence of established risk factors for fracture in such a population been assessed.
Materials and Methods: Ninety children and adolescents (47 girls and 43 boys) 5–19 years of age, who had experienced at least two fractures of the forearm, were studied. Bone size and mineralization were assessed using DXA at the ultradistal radius, one-third radius, neck of femur, hip trochanter, lumbar spine, and total body. Total body lean mass and fat mass were also determined. The prevalence of six risk factors for fracture were also examined, and their influence on ultradistal BMC Z scores was assessed.
Results: Participants experienced 295 fractures (74.9% forearm). Children with an early age of first fracture had higher rates of fracture per l00 years of exposure than those fracturing later. Four risk factors for fracture were over-represented in observed versus expected percentages: early age of first fracture (27.7% versus 11.3%), adverse symptoms to cow milk (22.2% versus 6.7%), low dietary calcium intake (20% versus 4.5%), and overweight (33.3% versus 15.5%). However, physical activity levels were similar to the reference population. Z scores for BMC and BMD were reduced, particularly at the ultradistal radius, whereas Z scores for weight, body mass index, fat mass, and body fat percentage were increased. Mean (SD) BMC Z scores were lowest at the ultradistal radius, −0.66 (1.22), where symptoms to milk were associated with reduced values (p < 0.009) and overweight with increased values (p < 0.003).
Conclusions: Our results suggest site-specific weakness and high body weight contribute to fracture risk in children and adolescents who fracture their forearms repeatedly. These findings are consonant with work showing adult Colles fractures increase as ultradistal radius BMD falls and with evidence that overweight children and adolescents are fracture prone.
ALTHOUGH REPEATED FRACTURES are common in apparently healthy children, and many children break a forearm more than once during growth, no previous studies seem to have been undertaken to examine the BMD and body composition of a group of boys and girls who have experienced multiple forearm fractures. It seems possible such children may have site-specific skeletal changes in the distal forearm that account for their high propensity to break repeatedly at this region of the skeleton. Such effects could include lower BMC, narrow bones or reductions in areal BMD or volumetric apparent BMD (BMAD). Alternatively, a high proportion of such children may exhibit known risk factors for fracture.
The distal forearm is the most common site of fracture during childhood and adolescence,(1) and fractures at this site are increasing.(2–4) We showed that in a birth cohort population of 1037 participants, a quarter of all the fractures experienced during growth affected this region of the skeleton, with more than one-half the youngsters with multiple fractures breaking at least one forearm.(5) Moreover, in this population, 10.2% of youngsters breaking a forearm between 0 and 18 years of age had sustained two or more fractures at this site. Khosla et al.(3) reported a similar proportion of adolescents with distal forearm fractures in the United States had previously broken forearms.
This study was undertaken to determine whether children who break a forearm on two or more occasions during growth display exaggerated osteopenia in the wrist versus the remainder of the skeleton. We were also interested to determine how many participants displayed potential risk factors for fracture (adverse symptoms to cow milk,(6) low dietary calcium intakes,(7) early age of first fracture,(8) high body weight,(9,10) low physical activity,(11) or high physical activity(12)) and to what extent these factors influenced radial BMC.
MATERIALS AND METHODS
Our hospital ethics committee approved the study. Informed consent was obtained from every teenage participant and a parent/guardian of every participant under 15 years of age. Every child or adolescent who had broken a distal forearm on at least two separate occasions during growth (between birth and age 19 years) and who had been referred to our bone research unit for DXA scans because they had a history of repeated fracture with minimal trauma but no known reason for this was eligible for the study. Although we recognize that general practitioners may have been more likely to refer children with repeated fractures to our unit for study, these youngsters had no specific characteristics and seemed very similar to children with repeated fractures presenting in consecutive series of forearm fracture children. Children with malignancy or any genetic or endocrine disorders known to be associated with a high fracture risk were excluded.
Every subject was weighed (Seca electronic scale) and measured (Harpenden stadiometer; Holtain, Crymych, UK) without shoes and dressed in light clothing. Body mass index (weight divided by height squared) was calculated. Overweight was defined from the international BMI cut-points of Cole et al.(13) Pubertal development was self-assessed from standard pictures and descriptions.(14) Lifetime fracture histories were obtained. Fractures were confirmed from radiological reports with fractures of the radius/ulna or tibia/fibula experienced on the same side at the same occasion being regarded as a single fracture.(1)
A general health questionnaire was completed. Current dietary calcium intake was determined using a food frequency questionnaire.(15) Information was also collected concerning use of mineral supplements and total calcium intakes (food plus supplements) are reported. These were classed as low if the value fell below two-thirds of the Recommended Dietary Allowance.(16) These cut-points varied with age and sex, being <533, 600, 667, and 533 mg/day for girls <7, 8–11, 12–15, and 16–18 years of age and <533, 800, and 667 mg/day for boys <11, 12–15, and 16–18 years of age, respectively. Participants were also asked to report any adverse symptoms (current or historical) they had experienced to consumption of cow milk such as eczema, rhinitis, gastrointestinal discomfort, or lactose intolerance,(17) because such children are over-represented in fracture populations.(8)
Each subject also assessed their habitual current physical activity relative to that of individuals of the same age and gender on a scale of 1–5 (1 = least active, 5 = most active), because both high levels(12) and low levels of physical activity could influence bone development. This assessment places the habitual physical activity of each subject in the context of activity levels of other children of similar age and gender while eliminating large differences in time per week spent in vigorous physical activity, which are inevitably present when comparing activity of very young children (<8 years) with that of older children (teenagers). In children of similar age and gender, these self-assessment scores of physical activity are strongly correlated with minutes of vigorous physical activity per week.
Four DXA scans were performed, distal forearm, left hip, lumbar spine (L2-L4), and total body using the procedures recommended by the manufacturer and the same scanner (Lunar DPX-L), which was monitored regularly for quality control to meet international drug trial stability requirements.(18) When scanning children who have recently broken an arm, we routinely scan their nonfractured arm if they report only a single fracture. When a child who has broken both left and right forearms presents for DXA scanning, our policy is to scan the arm that was least recently broken. Our adult in vivo scanning precision is good,(19) and scans were taken and analyzed by the same technician using software packages l.35 and l.5e.(18) Volumetric BMAD values (g/cm3) were calculated from DXA information at the 33% radius and femoral neck as (BMC/area2) and at the lumbar spine L2-L4 as (BMC/area1.5).(20)
Results are displayed as means (SD) and ranges. Z scores were calculated using fracture-free reference populations of girls(21) and boys(18) studied in the same research unit by the same methodology used for the present participants. Poisson regression was used to compare the rates of fracture, which were calculated as number of fractures per l00 years of lifetime exposure and reported as means with 95% CIs. The influence of risk factors on ultradistal BMC Z scores was examined using logistic regression. Data were log-transformed for analysis where necessary.
Ninety youngsters who had experienced a total of 295 fractures (Table 1) of which the majority (n = 221, 74.9%) affected the forearm were studied. Fractures of the upper limb were more common (n = 251, 85.1%) than those of the lower limb (n = 31, 10.5%), and few fractures occurred elsewhere (n = 13, 4.4%). Individual youngsters experienced from two to seven separate fractures (Fig. l). Fractures of left and right forearms were reported by 63 participants, whereas l5 had broken only their left arms and l3 only their right arms. Most of these fractures occurred during play or sport from mild or moderate precipitating trauma, with <5% of the fractures being caused by major trauma. None of the fractures were refractures of incompletely healed bone, because no fracture had occurred at the same anatomical site within an interval of <l2 months. However, one boy who had already broken one forearm later experienced bilateral fractures of both left and right forearms simultaneously in a single fall. Forty-five participants had scans performed on the left forearm and 45 on the right forearm, whereas in the controls, one-half the scans were done on the left and one-half on the right forearm.
A high proportion of the participants broke their first bone at a young age, with 83% doing so under the age of 10 years (Fig. 2). These children had higher rates of fracture than participants who first fractured after age 10 (Table 2).
Although they did not differ from the reference population in height or lean mass, our 90 study participants had higher Z scores for weight and BMI (p < 0.01) and fat mass and percentage body fat (p < 0.001) than the reference population. Pubertal development was appropriate for age, and boys and girls reported a broad range of current dietary calcium intakes and physical activity (Table 3).
Table 4 shows the Z scores for bone variables in the whole sample. The BMC Z scores were lowest at the ultradistal radius, where 29 children (32.2%) had values below −l. However, BMC Z scores were also reduced at the one-third radius, femoral neck, and total body. Areal BMD and volumetric BMAD Z scores were lower than in the reference population at every measured site, with reductions in BMD being significantly greater at the ultradistal than at the one-third radius (p < 0.04). The study participants also had wider bones at the one-third radius and lumbar spine and greater spinal area than the reference population.
Table 5 shows the prevalence of six potential risk factors for fracture and the associations of these factors to ultradistal BMC Z scores. Six subjects had none of these risk factors, whereas 42 subjects had a single risk factor, 29 subjects two risk factors, 10 subjects three risk factors, and 3 subjects four risk factors for fracture. Four factors were over-represented in the study population: observed versus expected percentages being increased for an early age of first fracture (27.7% versus 11.3%,(22)p < 0.001), symptoms to cow milk (22.2% versus 6.7%,(23)p < 0.001), low dietary calcium intakes (20% versus 4.5%,(18,21)p < 0.003), and high BMI values (33.3% versus 15.5%,(18,21)p < 0.001). In contrast, the prevalence of both low physical activity (17.7% versus 16.0%, p = 0.49) and high physical activity (36.6% versus 40%, p = 0.71) did not differ from the reference population.(18,21) Three risk factors tended to be associated with lower Z scores for ultradistal BMC; this effect was significant for adverse symptoms to milk and nearly significant for low dietary intakes of calcium at scanning but not significant for early age of first fracture (Table 5). In contrast, Z scores for ultradistal radius BMC were increased by overweight (significant effect) and tended to be raised with both high (nearly significant) and low (nonsignificant) levels of physical activity.
In this study, a group of youngsters with a history of multiple fractures of the distal forearm showed significantly lower BMC and BMD, particularly in the ultradistal radius, and higher body weight and adiposity than fracture-free children of similar age and gender. These results support the view that reduced mineral accrual in the distal radius and high adiposity increase distal forearm fracture risk in many youngsters who break their forearms repeatedly. Our findings are in agreement with work showing that Colles' fractures in adult women become more prevalent as areal BMD decreases at the ultradistal radius.(24) The results are also in accordance with other evidence showing that overweight children have a higher risk of fractures than those of healthy body weight.(9,10) The increased propensity of overweight children to break their bones may occur in part because bone adapts to muscle forces and not to static loads represented by body weight,(25) and in part, to the fact that overweight children fall with more force than lighter individuals.(26,27)
During childhood and adolescence, gains in bone mineral deposition lag behind increases in body weight and bone length, making the distal forearm especially vulnerable to failure with minor falls on the outstretched arm.(26,28) The strength of the radius is lower relative to body mass than in adults largely because cortical bone does not thicken to match rapid increases in body size. Our findings indicate that these discrepancies are more pronounced in youngsters who repeatedly fracture their distal forearms than in fracture-free boys and girls of similar age and gender. Site-specific osteopenia seems to be particularly severe at the ultradistal radius, although the study participants also show reduced BMC in other regions of the skeleton.
Muscle force plays a vital role in the accrual and maintenance of radial bone.(29,30) Sarcopenia may weaken bone,(31) and lack of muscle mass and abnormal bone geometry have been suggested as important reasons for the predisposition of children with juvenile idiopathic arthritis to fracture easily.(11) However, these study participants had normal height and were generally healthy. We did not find any evidence of reduced lean mass versus the reference populations, suggesting that low BMC values in study participants were not caused by inadequate loading from low musculature. The children had similar levels of physical activity as the reference population, and they did not have narrow forearm bones or reduced bone area.(32) Rather, they showed enlargement of bone at both the one-third radius and the lumbar spine. This observation was of particular interest, because widening of the bone provides an adaptive mechanism that can increase bone strength.(26) Indeed, Brennan et al.(33) recently suggested that widening of midradial bone was an adaptive response to strengthen forearm bone in children recovering from acute lymphoblastic leukemia.
The group did not have low Z scores for lean mass, indicating that inherent muscular weakness did not explain their reduced BMC Z scores. However, early age of first fracture, a history of symptoms to cow milk, and low dietary calcium intakes were over-represented in our study sample, suggesting early malnutrition may have adversely affected their bone health. Between one-fifth and one-quarter of the study population showed these characteristics. Moreover, individuals with these risk factors for fracture tended to show lower ultradistal BMC Z scores, suggesting some association between these risk factors and reduced mineral accrual at the ultradistal radius.
Children who have particularly fragile skeletons might be expected to fracture more readily at a young age during normal play and sport and also show higher rates of fracture than children with stronger bones. Our results support these views. A higher proportion of this study population than a birth cohort fracture population(22) experienced their first fracture under 5 years of age, and these youngsters had higher rates of fracture than children breaking their first bone later in life. A recent study of 315 consecutive fracture cases under l3 years of age treated at one hospital(8) also showed that a history of symptoms to cow milk was over-represented versus the prevalence expected,(23) probably because such children frequently avoid milk chronically without making appropriate nutritional compensatory changes, so that they show poor calcium intakes and osteopenia of the ultradistal radius that persists.(34) They have a propensity to fracture at a young age, particularly in the forearm.(6)
We recognize that it is unlikely that all 90 of our young subjects had the same risk factors for repeated forearm fracture. In some subjects, poor early nutrition may have contributed to low bone mineralization, whereas in others, higher exposure to risk-taking activities,(35) such as dangerous sports, may have played a more important role in explaining their repeated fractures. Thirty of the present children were overweight, suggesting high body mass probably contributed to repetitive fracturing of the forearm in many participants. Overweight adolescents may have poorer musculoskeletal control and less efficient postural stability than children of normal weight.(36) In addition, overweight children will fall more heavily on the outstretched arm than children of lighter body mass, making them more vulnerable to failure of the bone even with falls from less than standing height on soft surfaces.(27) Presumably, despite evidence of some compensatory increases in ultradistal radial BMC in our overweight subjects, this adaptive response was not sufficient to enable them to maintain forearm integrity and overcome the effects of high body mass in promoting fracture. Thus, they exceeded fracture thresholds of the bone in minor falls.
Intermittent overloading is strongly anabolic to bone,(30,37) so subjects reporting high physical activity might have been expected to show better BMC values than less active individuals. There was some evidence of this because ultradistal forearm BMC Z scores tended to be raised in participants with high physical activity scores, but the effect did not achieve significance. Moreover, frequent participation in sporting activities that increase falls,(12) rather than an inherent weakness of the wrist bone, may put active youngsters at greater risk of repeated forearm fractures. High risk-taking behavior could also elevate the risk of fracture, although one recent study showed that this applied only to fractures of the hand and not to forearm fractures, where reductions in BMD values were considered to be more important.(18,21,35,38,39) Last, although low levels of physical activity might be expected to lower BMD,(40) many of our inactive youngsters were also overweight. This combination probably explained the tendency for low physical activity to be associated with slightly raised ultradistal BMC Z scores.
Finally we acknowledge that some youngsters experiencing multiple forearm fractures may have less strong microstructure of the wrist, without overt reductions in BMC, perhaps through genetically inherited mechanisms. Thus, a recent twin study showed that wrist fracture in adult women is associated with a heritable component that is independent of BMD.(41)
Study limitations include inability of DXA measurements to differentiate cortical and trabecular bone as would be possible with pQCT and no direct measures of bone strength. Nor do we have any genetic evaluations of the participants. Recall bias may have influenced our assessments of physical activity and dietary calcium intakes, which like DXA, were not estimated at the time of every fracture. We also recognize that our participants were a convenience sample rather than a truly consecutive group of youngsters with more than one forearm fracture. However, strengths of the study include evaluations of a large sample of male and female children and adolescents with proven multiple forearm fractures and quantitation of bone mineral, bone size, and body composition by DXA. Our results show significant reductions in BMC, particularly in the ultradistal forearm. This was not related to lower lean tissue mass, suggesting primary deficits in bone mineral accrual, rather than inherent lack of muscular force to grow and maintain bone, as well as high body weight caused by excessive accumulation of body fat, may explain the propensity of many youngsters to fracture their forearms frequently with minimal trauma during growth. Our results underscore the importance of reviewing the nutrition, body weight, and physical activity levels of young children presenting with distal forearm fractures, because modifications of these factors may help to strengthen bone and avoid new fractures.
This study was supported by the Health Research Council of New Zealand and the Dunedin Department of Medicine Bone Research Group.
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