The Effect of a Femoral Fracture Sustained before Skeletal Maturity on Bone Mineral Density : A Long-Term Follow-Up Study

1Arcada University of Applied Sciences, Jan-Magnus Janssonin Aukio 1, 00550 Helsinki, Finland 2Children’s Hospital, Helsinki University Central Hospital, P.O. Box 281, 00029 Helsinki, Finland 3Tampere Center for Child Health Research (TACC), University of Tampere and Tampere University Hospital, Lääkärinkatu 1, 33014 Tampere, Finland 4Orton Orthopaedic Hospital, Orton Foundation, P.O. Box 29, 00281 Helsinki, Finland 5Department of Radiology, HUS Medical Imaging Center, Helsinki University Central Hospital and University of Helsinki, P.O. Box 340, 00029 Helsinki, Finland


Introduction
Decreased bone mineral density (BMD) has been diagnosed in adults as sequel of immobilisation and reduced weight bearing in the injured limb [1].Henderson et al. [2] have reported a decreased BMD in proximal femur two years after tibial and femoral fractures in children that were immobilised for eight weeks or longer.Ferrari et al. [3] have found an association between a childhood fracture and low BMD in adulthood suggesting low peak bone mass and persistent bone fragility.
We studied long-term effects of pediatric femoral shaft fractures treated with skeletal traction on BMD.

Materials and Methods
Sixty-two pediatric patients (<16 years old, all Scandinavian Caucasian) that had sustained a femoral fracture were treated with skeletal traction (in a hospital bed) in Aurora Hospital, Helsinki, during 1980-1989.The most common injury type was a motor-vehicle accident.
Patient files and primary radiographs of these patients were analysed.A questionnaire about subjective treatment results as well as an invitation to participate in a follow-up examination (mean 21, range 11.4, standard deviation (SD) 2.8 years) was mailed to all patients [4].Fifty-two of the patients agreed to participate.They all gave written informed consent  1.
The radiographic examinations were conducted at the time of the follow-up and consisted of standing anteroposterior radiographs of both legs and standing lateral views of the femurs.The anteroposterior hip-to-ankle radiographs were obtained separately of both extremities.They were taken in fluoroscopy control at a distance of 1.5 m on analog films.For length measurements a long radio-opaque ruler was fixed to the leg.The images were evaluated for the length of the lowerlimbs and femurs in millimetres.
The mechanical axis of the entire leg was measured according to the method described by Hagstedt et al. [5].In addition to the mechanical axis both femurs were analysed for angular deformity in two planes, that is, varus/valgus in the frontal view and ante-/recurvatum in the lateral view.For these assessments of the coronal and lateral curves lines through the midsection of the proximal and distal femoral diaphyses were drawn and measured with a manual goniometer.
DEXA examinations were performed using a narrow fanbeam Lunar Prodigy densitometer (GE Lunar Corporation,  Madison, WI, USA).To verify the stability of the DEXA system a control procedure of the scanner was performed weekly in addition to a daily calibration according to manufacturer's instructions.
The subjects were positioned in supine position on the scanning table with the body aligned with the midline of the scanning table.The legs were straight and strapped in slight internal rotation.The Lunar Prodigy software uses a series of complex algorithms to calculate BMD and bone mass in the total body and for different anatomical regions, in our study the legs and femoral necks (Figures 1 and 2).The results were measured and reported as kilograms for total body weight (BW) and BMD was measured in g/cm 2 .
Bone density was separately measured in the lower legs (Figure 1) and in femoral neck (Figure 2).In previous studies from our institution with the same scanner the precision of total bone and extremity density measurements have shown excellent repeatability and are expressed as the coefficient of variation 1,0% for total body [6] and 1,6% for the lower extremity [7].The precision is consistent with the literature [8,9].
Two senior musculoskeletal radiologists made all the radiographic (M.Lohman) and DEXA measurements (K.Tallroth) independently of each other and blinded regarding previous readings.
The statistical analysis was done with Statistical Package for the Social Sciences 21.0 (Norusis/SPSS, Inc., Chicago, IL).

Results
Mean duration of skeletal traction was 39.6 days (range 74, SD 15.8).Significant differences in leg lengths were not found (Table 2).Mean mechanical axis in both frontal and sagittal planes was slightly larger in the injured lower-limb compared to the noninjured contralateral limb (Table 2).Whole body BMD was within normal limits in all patients according to the manufacturer's reference values.Mean BMD of the entire injured lower-limb was lower than that of the noninjured lower-limb (1.323 g/cm 2 versus 1.347 g/cm 2 ,  = 0.003).BMD of the femoral neck of the injured lower-limb did not differ from the limb without an injury (mean 0.998 g/cm 2 versus 0.995 g/cm 2 ,  = 0.806).BMD difference between the injured and the noninjured limb was statistically significant in male patients (mean 1.403 g/cm 2 versus 1.380 g/cm 2 ,  = 0.023), but not in female patients (mean 1.245 g/cm 2 versus 1.227 g/cm 2 ,  = 0.203).
The only factor that was associated with the lower-limbs BMD difference was the duration of traction explaining about 17% of its variation.

Discussion
In the 1980s most pediatric femoral fractures in Finland were treated without internal fixation, which allowed us to perform DEXA measurements on these patients without disturbing fixation devices such as metal plates or nails.The BMD was not evaluated before the fracture took place, which is obviously a limitation of our study.However, the mean follow-up time after the fracture was longer than in most of the previous studies.
Femoral fractures sustained before skeletal maturity have been reported to reduce the injured femur's BMD distal to the fracture site [1,10], lower BMD values than in the noninjured extremity have been registered in the injured extremity 11 years after tibial shaft fractures [11], and girls have been reported to have a decreased body bone mineral content four years after a distal forearm fracture [12].Our findings are in line with these earlier studies although we found that BMD of the injured lower extremity was only slightly lower compared (mean 2%) to the noninjured lower extremity.Furthermore, we did not find a decreased BMD proximal to the fracture.Malignment of the femur in neither frontal nor sagittal plane correlated with BMD in this study.No correlation was found between the mechanical axis of the lower extremity and the BMD.This is most likely explained by the fact that only few patients in our study with malunion had permanent deformity that is regarded unsatisfactory according to clinical guidelines [13].
Nikander et al. [14] concluded that exercise can significantly enhance bone strength at loaded sites in children.Leppälä and coworkers [10] found a positive correlation between muscle strength and bone density of the tibia in patients that had been rehabilitated from a tibial fracture.We did not collect data of physical activity nor test muscle

Figure 1 :
Figure 1: Whole body DEXA measurement, demonstrating measurement areas separately for each lower extremity.

Figure 2 :
Figure 2: The areas for bone mass measurement for the right and left femoral neck.

Table 1 :
Characteristics of patients at baseline and at follow-up.

Table 2 :
Lower-limb length, femur length, and lower-limb angular deformities at follow-up radiographic evaluation among patients with a childhood femoral fracture.