Bone regenerate is a complex process, which has been widely studied through experimental techniques[15, 16]. However, how to monitor bone regenerate in humans is still a challenge. Monitoring of bone healing is routinely done by clinical evaluation and radiographic examinations, but it strongly depends on the clinical experience and lacks the quantitative information about callus strength that would be helpful for therapeutic decisions[6].
Of all the methods for achieving long bone healing, one alternative is to use an external fixator to restore the original stiffness and the mechanical stability of the bone. The external fixation is mainly responsible for load transfer through the injured bone and creates a suitable mechanical environment for bone regenerate[17]. The device acts as a mechanical bridge, allowing partial recovery of the load transfer through the injured member and decreasing the interfragmentary movement.
Leaving the external fixator for longer than necessary would lead to various complications, such as limitation of joint motion due to contracture. As early as 1983, Terjesen et al.[18] concluded that there was a stress-protecting effect of the fixation frame on the bone, and the external fixation should be removed as soon as the fracture healed to avoid this effect. However, premature removal of the frame also leads to severe complications, including fracture or axial bending at the callus. Ilizarov himself also remarked that “leaving the apparatus on for longer than necessary is as harmful as removing the fixator too early”[19]. Therefore, choosing an appropriate time to remove the external fixator is essential for successful treatment.
Several imaging modalities have been proposed to estimate the status of the regenerative callus tissue, such as high-resolution magnetic resonance[20, 21], quantitative ultrasound[22], dual-energy X-ray absorptiometry (DEXA)[11], and quantitative computed tomography (QCT)[12, 23]. However, these alternative methods may involve large radiation doses, be restricted by cost and availability, or have not been assessed adequately for reliability. Besides, Fischgrund et al.[24] specified the presence of three of the four cortices of a minimum 2 mm thickness as a guideline for removing the fixator, and they presented a re-fracture rate of only 3%; while Starr et al.[25] attributed the good results obtained by Fischgrund et al.[24] to the better clinical judgment of an experienced surgeon involved in decision making, rather than the radiographic criteria demonstrated in their study. Hazra et al.[26] made a retrospective study of 70 patients to compare the BMD ratio and pixel value ratio, concluding that pixel value ratio is a good method for assessing callus stiffness as well as judge the timing of fixator removal, while the inherent limitation is that the pixel value is easily affected by the presence of metal in the vicinity of the point of measurement. Briefly, none of the aforementioned methods has acquired gold standard status.
As generally accepted, orthopedics is both a visually and mechanically oriented discipline, and the skeleton is a load-bearing structure. Resistance to deformation is a fundamental property of a structure and is defined as its stiffness, which seems to be an appropriate measure of bone regenerate. As Goodship et al.[27] showed, there was an increase in stiffness and stability of regenerated bone after fracture healing during time progression. Information on the rate of increase of the mechanical properties of a healing bone is therefore valuable in determining both the rate at which a fracture will heal and in helping to define an objective and measurable endpoint of healing. As early as 1972, Jorgensen[28] described a mechanical method of measuring the bone deflections during load bending to measure the deflection on Hoffmann-treated crural fractures. Subsequently, clinical in vivo applications of mechanical measurements in fracture healing have been published.
Richardson et al.[29] measured fracture stiffness in 212 patients with tibial fractures treated by external fixation, considering that stiffness of 15 Nm/degree in the sagittal plane provides a useful definition of the union of tibial fractures. Wade et al.[30] studied the progression of healing in 103 unstable fractures of the tibia, advocating that fracture stiffness should be measured in two orthogonal planes when assessing tibial healing and suggesting that values above 15 Nm/ degree in two planes indicate to remove the fixator safely. These studies are all concentrated on the direct measurement of callus stiffness, which allows a good estimation of the load capacity of the healing bone; however, this method is limited by the removal of the fixator for each measurement. Furthermore, in the early phase of bone healing, it is impossible to remove the fixation device due to the potential risk of losing the reduction under loading. This procedure is thereby only applicable for the later phases.
For clinical applications, however, most often, only the deformation in the longitudinal axis of the bone was measured. Another possibility to measure the load sharing between bone and fixator is the integration of a load cell in the fixator body. Evans et al.[31] developed a transducer that been fitted to the support column of an external fixator to determine the stiffness during the healing process. Seide et al.[32] described a hexapod system that can be used for measuring axial and shear forces as well as torsion and bending moments in the fixator in vivo, concluding that the measured values enabled both the type of fracture to be determined as well as the monitoring of the healing process. Aarnes et al.[14] presented an in vivo test for assessment of regenerate axial stiffness after the distraction phase of lengthening therapy. In their clinical trial of 22 individuals with tibia1 lengthening, the fixator was removed when the load-share ratio dropped below 10%, and none experienced refracture. Therefore, they drew the important conclusion that the external fixator can be removed safely when the load-share ratio dropped below 10%.
Recently, Mora-Macias et al.[33] performed a bone transport experiment in sheep, the forces through the fixator evolution were measured, and the callus stiffness was estimated from these forces. Their data complement previous experimental and computational works. They also concluded that the force and stiffness data together with conventional methods such as radiographs might contribute to know exactly when the limb stiffness is recovered while the fixator is implanted, or estimate the optimum time when the fixator should be retired.
Refracture after the frame removal was one of the few major complications reported by De Bastiani when the external fixation was used, affecting 3% of patients[34]. Others have reported rates of 6%[35] and 9.4%[36]. In the present study, we conducted the axial load-share test in 45 patients (group Ⅱ) who underwent Ilizarov circular external fixator treatment in the lower extremity and the evaluation criteria of Aarnes et al.[14] were continuously used. With a mean of 17.3 months follow-up, there was none experienced refracture after removing the external fixator with an axial load-share ratio less than 10%. While in group Ⅰ, the frame was removed just depending on the traditionally radiological and clinical assessment. 4 of the 38 patients suffered refracture after the frame removal, and the refracture rate was 10.5%. There was statistical significance in the refracture rate between the two groups. The results manifested that the mechanical test as a supplement to radiography for evaluating the regenerate healing made the fixator removal safer.
The regenerate healing is generally defined as the reconstruction of the bony biomechanical characteristic. For bone union assessment, it is traditionally evaluated using imaging modalities that cannot provide related biomechanical information. There were 9 patients that the treating surgeon had decided to remove the frame in group Ⅱ, but the mechanical test has overruled this decision in this study. After a period of time, the external fixator was safely removed based on the axial load-share ratio dropped below 10%. We, therefore, speculate that it may due to the biomechanical properties of the regenerated bone itself were not completely recovered, but the radiographs provided inaccurate healing information.
Aarnes himself also emphasized that “A small bone bridge may carry a significant load and therefore cause a low LS ratio without the bone being completely healed”[14]. Therefore, they suggested that radiographs must be taken to assess the geometry of the new bone. For our experience, the radiographs, load-share tests, and clinical experience complement each other in evaluating regenerate healing. A prudent attitude and comprehensive assessment should be adopted regarding the removal of an external fixator. We also advocate that the LS ratio should be measured in both static and dynamic tests when assessing regenerate healing for more excellent safety.
The axial load-share test provides an objective assessment of bone regenerate, including potential advantages of fewer radiographic images taken (lower cost) and a lower ionizing radiation dose. There is no need to remove the fixator when this indirect and non-invasive method was performed. It is possible to measure the load sharing and indirect callus stiffness even from the first day postoperatively without the likelihood of fracture, malunion, and pseudarthrosis. Furthermore, the total device is price-friendly and manufacture-simply. This technique does not involve complex procedures and electronic devices that remain for a long time or even forever in patients. There are potential chances for its wider use in most fracture clinics, as it supplements radiography and clinical experience and makes us safer while removing the fixator.
The present study had several limitations. Firstly, considering its relatively small sample size in a single center, a prudent attitude should be adopted to interpret the potential greater risk of refracture if the fixator was removed based on clinical assessment only. Furthermore, this method is concentrated on the axial load because the sensors are sensitive to axial force only; the clinical application thereby may be limited by the spatial structures of the external fixator, such as the hexapod external fixator, which contains multi-directional forces in each rod. Additionally, other tests are required to determine whether there is another preferable limit of LS ratio for regenerate healing assessment.