Discussion
The distal femur is the main growth center of the lower limb[
11] and the epiphysis of it is an important factor in the limb length of children. Assisted by effective neoadjuvant chemotherapy before operation, the effect of limb salvage surgery for malignant bone tumor had been obviously improved[
12,
13]. Although the tumorous bone can be resected completely by osteotomy of the unclosed epiphysis in patients who are children, the injury to the epiphysis inevitably has a negative effect on the limb growth[
3]. This research attempted to preserve the epiphysis of the distal femur that was distracted by external fixation so as to preserve the knee joint function and length of the lower limb.
The tensile capacity of the epiphyseal plate is determined by collagen fibers which become thin by being squeezed by chondrocytes during development, so this area is the weakest part of the epiphyseal plate. The location of the puncture sites is an important factor for the result of the epiphyseal distraction because there is a negative effect on epiphyseal growth when the Steinman pins are punctured through the germinal layer but no damage to epiphyseal growth when the Steinman pins are punctured through the mastocyte layer[
14]. The principle of epiphyseal distraction is to separate the epiphysis from the metaphysis by force on the mastocyte layer. Distraction by an external fixator can effect a complete separation from the metaphysis and avoid injury to its germinal layer by force from shear or twist[
15].
The first purpose of tumor surgery is to obtain a complete tumor resection, but complications become inevitable when the resection is conservative to preserve the epiphysis, so the indications for epiphyseal distraction must be properly selected. Cañadell[
9] considered the indications for epiphyseal distraction should include the following: 1) the tumor should be situated in the metaphyseal region; 2) the physeal cartilage should be open; and 3) the tumor should not transgress the physis and should be confirmed by radiography, arteriography, CT or MRI preoperatively and histological examination intraoperatively. At present, MRI is considered to be superior to X-ray and CT in determining the invasive range of malignant tumors of the limbs[
16,
17].
According to the image staging method of San-Julian[
5], the invasion of sarcoma in the metaphysis of children is divided into three types: type I, the distance between the lesion and the epiphyseal plate is more than 2 cm; type II, the distance between the lesion and the epiphyseal plate is less than 2 cm or they are adjacent to each other; and type III, the lesion has partly invaded into the epiphysis. Although the growth plate of the cartilage can prevent the tumor from diffusing, the barriers of it are by no means impassable. Most experts consider a safe surgical tumor margin to be 5 cm outside the lesion[
9], but other experts consider the epiphysis can be preserved when the distance between it and the lesion is less than 1 cm but not invaded by the lesion[
18]. To guarantee a safe margin in this research, type I San-Julian staging was treated as an absolute indication for epiphyseal distraction and type II San-Julian staging was treated as a relative indication for epiphyseal distraction, but type III was a contraindication for epiphyseal distraction. According to this principle, there was no local recurrence of tumor after the surgery, indicating that the technique is safe when based on the strict indication.
At present, there are many limb salvage methods that preserve the epiphysis in malignant bone tumor, such as epiphyseal osteotomy and reconstruction using allogenic bone[
19] or devitalized autologous tumor bone[
20], autologous epiphysis transplantation[
21]. Owing to excessive complications and limited sources, the application of autologous epiphysis is limited. Although epiphyseal osteotomy results in a relatively satisfactory outcome[
20], the germinal layer of the epiphysis is damaged by osteotomy because the section of osteotomy is complanate but the interface between the epiphysis and metaphysis is sawtoothed. As a result, the growth of the epiphysis and the function of the limbs is impaired by epiphyseal osteotomy[
21]. When reconstructed with devitalized autologous tumor bone, the breaking of the necrotic bone shell caused by the screws increases the possibility of tumor recurrence, so more observation for the safety and effect of this technique is needed.
The technology of epiphiseal distraction during bone lengthening has been proven to be effective and Cañadell[
9] has applied a unilateral external fixator to preserve the epiphysis of tumorous bone. In order to avoid the uneven stress caused by using a unilateral external fixator, we used a bilateral external fixator to balance the force to separate the epiphysis from the metaphysis completely and effectively. After being reconstructed with allogenic bone and fixed by locking intramedullary nails, the stability of the epiphysis and the continuity of bone growth were maintained. At six months after operation, X-ray showed the gaps at both ends of the allogenic bone were healing completely. At two years after operation, X-ray showed the gap between the epiphysis and allogenic bone was well healed after the lag-screw was removed. This means that the blood supply and growth ability of the distal femur had been well preserved. At the same time, the attachment point of the cruciate ligaments and collateral ligaments at the distal femur were preserved, so that complications, such as rupture or contraction of ligaments after reconstruction, can be avoided and better knee joint function can be maintained.
Research had shown that there was partial growth inhibition in the epiphyseal growth plate after injury[
22], accompanied by the closure of the epiphyseal plate and the formation of a bone bridge which seriously influence limb growth[
23]. There were varying degrees of limb shortening in all patients in this study, showing that the growth of the epiphyseal plate was affected by the injury caused by distraction. There were six patients who were 1 to approximately 2 cm shorter in the operated limb than in the contralateral lower limb but this had no appreciable effect on their gait or spine growth. There were four patients under the age of 10, however, who were 2 to approximately 5 cm shorter in the operated limb than in the contralateral lower limb. This probably owing to the younger age of patients and more expected length of the operated limbs to reach the normal length, so the slight damage of the epiphyseal plate probably caused a large limb shortening of the operated limbs. Cryopreserved allograft bone has a favorable histocompatibility and bone inducing activity, weak antigenicity and strong osteogenic potential which make it effective in bone defect reconstruction after tumor resection[
21]; it incorporates with host bone easily. At the same time, the epiphysis and massive allograft bone that is fixed by the screws provide a better stability for bone healing[
19]. In this research, X-ray showed no loosening after the epiphysis was fixed with a massive allograft bone by lag-screw vertically. Owing to the repairing ability of children’s cartilage[
24], there was no adverse effect on joint function after the cartilage flap restored.
The complications of epiphyseal distraction include infection, internal fixation loosening, nonunion or delayed union of bone, rejection and nerve injury[
9,
25]. Only one patient in this research suffered from poor healing of the incision, local infection and exudation from the wound because of allograft bone rejection, but the condition improved after anti-inflammation treatment. This indicates that the technology of epiphyseal distraction is safe.
Conclusions
In this research, we preserved the epiphysis that had not been invaded by tumor through distraction by an external fixator, so that not only the integrity of the joint capsule and ligament but also the growth function of the limb was preserved. At the same time, this technique avoided not only damage to the epiphysis by osteotomy but also postoperative complications, such as contraction or rupture of ligaments and ankylosis of the knee joint. The technology of distal femur epiphysis preservation using epiphyseal distraction by an external fixator in childhood osteosarcoma may be a suitable method for limb salvage with better joint function. However, indications for this technology must include an open and uninvolved epiphyseal plate and effective neoadjuvant chemotherapy before the operation. Be restricted to the limitations such as less cases, shorter period of follow-up and evaluation for limb, further more observation were demand for the effect of the technology.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
SG, Performed the conception and design of the study; Drafting the article and revising it critically for important intellectual content; Final approval of the version to be submitted. YZ, Performed the analysis and interpretation of data; Drafting the article; Final approval of the version to be submitted. QC, Performed the conception and design of the study; Revising the article critically for important intellectual content; Final approval of the version to be submitted. WY, Performed the acquisition of data; Drafting the article; Final approval of the version to be submitted. JW, Performed the acquisition of data; Drafting the article; Final approval of the version to be submitted. All authors read and approved the final manuscript.