Search tips
Search criteria 


Logo of corrspringer.comThis journalToc AlertsSubmit OnlineOpen Choice
Clin Orthop Relat Res. 2009 July; 467(7): 1915–1920.
Published online 2009 February 11. doi:  10.1007/s11999-009-0723-z
PMCID: PMC2690745

Case Report: Histologic Study of a Human Epiphyseal Transplant at 3 Years after Implantation

J. Sales de Gauzy, MD,1 F. Accadbled, MD, PhD,corresponding author1,3 A. Gomez Brouchet, MD,2 and A. Abid, MD1


A 5-year-old boy underwent surgical excision of a Ewing’s sarcoma of the proximal femur. Reconstruction was performed using an ipsilateral vascularized epiphyseal transplant and a femoral allograft. Local recurrence of the tumor necessitated hip disarticulation 3 years after the initial procedure. We then performed a histologic analysis of the transplant. The growth plate was still normal in structure but had richly vascularized hyperplastic layers. We observed bridging between the articular cartilage and the growth plate.


Epiphysis transplant is an alternative for epiphyseal reconstruction in children. It allows restoration of joint function and growth potential [8]. Continued longitudinal and tridimensional growth of the transplant has been confirmed by clinical monitoring [6, 9, 12]. Moreover, experimental animal studies have shown, once the microvascular anastomosis has restored the blood supply to the growth plate, the epiphysis appears normal histologically [2, 11].

We report the case of a patient whose fibular epiphyseal transplant was excised 3 years after reconstruction of his right proximal femur. We performed a histologic analysis of the actual epiphysis.

Case Report

A 5-year-old boy presented with a Ewing’s sarcoma of the right proximal femur. After neoadjuvant chemotherapy, he was treated with intraarticular wide excision of the proximal femur. Reconstruction was achieved using a proximal ipsilateral vascularized fibula. An allograft was first secured to the femur with a plate to reinforce the shaft of the fibular autograft. The latter then was inserted into the allograft and secured using two lag screws. The fibular head then was placed into the acetabulum. The length of the fibula matched that of the excised femur (Fig. 1). The fibular graft was connected via the anterior tibialis artery and fibular artery to the profunda femoris artery. The anterior tibialis vein was anastomosed to a superficial vein. Microscopic examination confirmed the margins were negative and the patient had a good response to the neoadjuvant chemotherapy, with less than 10% active tumor cells (Grade III according to the grading system of Huvos et al. [4]).

Fig. 1
A postoperative anteroposterior radiograph of the right hip shows a fibular transplant placed in the acetabulum.

The patient was immobilized in a hip spica cast for 3 months. Adjuvant chemotherapy was given postoperatively with eight courses of vinblastine, actinomycin, and cyclophosphamide. Partial weightbearing was started after 3 months. At 4 months, a fracture of the fibular graft occurred and was treated with a hip spica cast (Fig. 2). Consolidation was obtained after 1 month (Fig. 3). Full weightbearing then was achieved with the patient wearing a knee brace for another 6 months.

Fig. 2
A fracture at the junction between the fibular transplant and the allograft occurred 4 months postoperatively.
Fig. 3
The fracture united after immobilization in a hip spica cast for 1 month.

Three years after surgery, our patient had no limb length discrepancy and walked unassisted with a mild limp. Hip range of motion was: 100° flexion, 0° extension, 30° abduction, 25° adduction, 25° internal rotation, and 30° external rotation. The donor site was clinically normal with no pain, weakness, ligament laxity, or paresthesia. Radiographs showed the graft had increased in length and width (Fig. 4). The distance between the center of the growth plate of the graft and the lower end of the plate increased by 25 mm (Fig. 3 versus Fig. 4). MRI showed no evidence of necrosis of the neofemoral head, which had increased in volume and remodeled to a more spherical shape. Its growth plate remained open (Fig. 5).

Fig. 4
An anteroposterior radiograph of the pelvis at 3 years’ followup shows continued growth and bone remodeling with femoralization of the proximal fibula.
Fig. 5
A T2-weighted fat-suppressed spin echo, coronal view MR image taken at the 3-year followup shows the proximal fibula grown up with persisting growth plate, congruent joint, and no intraarticular effusion.

One month later, the patient reported pain at the site of the plate, which therefore was removed. Intraoperatively, the bone was deemed normal and of adequate strength. One month later, a spontaneous fracture occurred at the junction between the allograft and the native femur (Fig. 6). The fracture was treated with open reduction, plate fixation, and immobilization in a hip spica cast (Fig. 7). The patient then sustained another fracture below the plate after 6 months (Fig. 8) and thus had reoperation for plate removal, autologous iliac crest bone graft, and application of a long locking plate (Fig. 9). Bone biopsies also were performed and specimen revealed local recurrence of the Ewing’s sarcoma at the junction between the shaft of the fibular graft and the distal femur (Fig. 10). Treatment then consisted of right hip disarticulation and chemotherapy. On microscopic examination, the margins of the resection were negative. Eighteen months after the disarticulation, our patient has not had any additional recurrence.

Fig. 6
A fracture at the junction between the fibular graft and the allograft occurred 2 months after the 3-year followup.
Fig. 7
The fracture was treated with open reduction and plate fixation.
Fig. 8
A femoral shaft fracture occurred 6 months after the plate was applied.
Fig. 9
This fracture was treated with open reduction, locking plate fixation, and autologous bone graft.
Fig. 10A B
(A) A photomicrograph shows recurrence of Ewing’s sarcoma around a screw hole (Stain, hematoxylin and eosin; original magnification, ×10). (B) Multiple round cells related to Ewing’s sarcoma, low cytoplasm content, and round or ...

Histologic analysis of the excised specimen (Fig. 11) was performed. The articular cartilage was remodeled. Around the fibular head, it was normal in structure with chondrocytes often gathered in groups. At the central part of the fibular head, the articular cartilage was replaced with richly vascularized fibrous tissue. Between the center and the periphery, we observed abundant immature chondrocytes forming fibrous cartilage and surrounding neoangiogenesis. The physis was mostly located directly underneath the articular cartilage or the richly vascularized fibrous cartilage. The physis consisted of four distinct layers all the way through, which were all hyperplastic. The intermediate layer was increased in height with high columns of chondrocytes. The cancellous bone located between the articular cartilage and physis contained adipose cells and was richly vascularized.

Fig. 11A C
(A) A coronal cut of the excised fibular epiphyseal transplant shows the connection between articular cartilage and the growth plate (arrow) and distal hypertrophy in relation to fracture healing. (B) Microscopic examination of the excised fibular epiphyseal ...


Since the initial report of Taylor et al. [13] in 1975, studies have confirmed microvascularized bone transfer is an effective reconstruction for large segmental defects [12]. Autologous epiphysis transplants have been reported more commonly in clinical practice [3, 8]. They are an effective alternative for epiphyseal reconstruction in children. Transplants can be used for treatment in various conditions, such as tumors and congenital or traumatic disorders of a long bone epiphysis in children. They have been used at various sites, including the proximal humerus, distal radius, and proximal femur [3, 8, 9]. The donor site is mainly the proximal fibula. Innocenti et al. [8] reported a series of 27 cases in skeletally immature patients with good morphologic and functional results at 2 to 14 years followup. We personally performed two other fibular epiphyseal transfers for reconstruction of one distal radius and one proximal humerus, both after excision of Ewing’s sarcoma. The radius case presented an early slip of the fibular epiphysis with revision surgery and has an overall poor functional result. The humerus shows a good preliminary result at 7 months’ followup with good range of motion and activity level.

The success of the procedure relies on the epiphyseal vascularization through microsurgical anastomoses [7]. The choice of the feeding pedicle is still controversial. The vascularized transfer of the proximal fibula usually is connected to the anterior tibialis artery [7]. Taylor et al. [14] reported the anterior tibialis artery provides an adequate blood supply to the epiphysis and the proximal 2/3 of the fibula. Mozaffarian et al. [10] reported the artery of the neck of the fibula is often a branch of the anterior tibialis artery, but in 24% of cases it is a branch of the popliteal artery that is not suitable for an anastomosis. They therefore suggested a preoperative angiogram to identify the origin of the artery of the neck. One report confirmed the growth and remodeling potential of an epiphyseal transfer with continued growth reported in approximately 70% of cases [5]. Blockey [1] reported histologic evidence of viability of the growth plate on a biopsy 1 year after a radius reconstruction and described enchondral ossification and irregularity and crowding of the columns of the growth plate.

Our case showed the viability of the growth plate after epiphyseal vascularized fibular transfer in a human. It remained intact and functional 3 years after the procedure. This confirms the results of previous experimental studies in dogs [2, 11].


Each author certifies that he or she has no commercial associations (eg, consultancies, stock ownership, equity interest, patent/licensing arrangements, etc) that might pose a conflict of interest in connection with the submitted article.

Each author certifies that his or her institution has approved the reporting of this case report, that all investigations were conducted in conformity with ethical principles of research, and that informed consent for participation in the study was obtained.


1. Blockey NJ. Observations on the fate of fibular transplants for congenital absence of the radius. J Bone Joint Surg Br. 1967;49:762–765. [PubMed]
2. Brown K, Marie P, Lyszakowski T, Daniel R, Cruess R. Epiphysial growth after free fibular transfer with and without microvascular anastomosis: experimental study in the dog. J Bone Joint Surg Br. 1983;65:493–501. [PubMed]
3. Ceruso M, Falcone C, Innocenti M, Delcroix L, Capanna R, Manfrini M. Skeletal reconstruction with a free vascularized fibula graft associated to bone allograft after resection of malignant bone tumor of limbs. Handchir Mikrochir Plast Chir. 2001;33:277–282. [PubMed]
4. Huvos AG, Rosen G, Marcove RC. Primary osteogenic sarcoma: pathologic aspects in 20 patients after treatment with chemotherapy en bloc resection, and prosthetic bone replacement. Arch Pathol Lab Med. 1977;101:14–18. [PubMed]
5. Innocenti M, Ceruso M, Manfrini M, Angeloni R, Lauri G, Capanna R, Bufalini C. Free vascularized growth-plate transfer after bone tumor resection in children. J Reconstr Microsurg. 1998;14:137–143. [PubMed]
6. Innocenti M, Delcroix L, Manfrini M, Ceruso M, Capanna R. Vascularized proximal fibular epiphyseal transfer for distal radial reconstruction. J Bone Joint Surg Am. 2004;86:1504–1511. [PubMed]
7. Innocenti M, Delcroix L, Romano GF. Epiphyseal transplant: harvesting technique of the proximal fibula based on the anterior tibial artery. Microsurgery. 2005;25:284–292. [PubMed]
8. Innocenti M, Delcroix L, Romano GF, Capanna R. Vascularized epiphyseal transplant. Orthop Clin North Am. 2007;38:95–101, vii. [PubMed]
9. Manfrini M, Innocenti M, Ceruso M, Mercuri M. Original biological reconstruction of the hip in a 4-year-old girl. Lancet. 2003;361:140–142. [PubMed]
10. Mozaffarian K, Lascombes P, Dautel G. Vascular basis of free transfer of proximal epiphysis and diaphysis of fibula: an anatomical study. Arch Orthop Trauma Surg. 2008 Feb 29 [Epub ahead of print]. [PubMed]
11. Nettelblad H, Randolph MA, Weiland AJ. Free microvascular epiphyseal-plate transplantation: an experimental study in dogs. J Bone Joint Surg Am. 1984;66:1421–1430. [PubMed]
12. Shea KG, Coleman SS, Coleman DA. Growth of the proximal fibular physis and remodeling of the epiphysis after microvascular transfer: a case report. J Bone Joint Surg Am. 1997;79:583–586. [PubMed]
13. Taylor GI, Miller GD, Ham FJ. The free vascularized bone graft: a clinical extension of microvascular techniques. Plast Reconstr Surg. 1975;55:533–544. [PubMed]
14. Taylor GI, Wilson KR, Rees MD, Corlett RJ, Cole WG. The anterior tibial vessels and their role in epiphyseal and diaphyseal transfer of the fibula: experimental study and clinical applications. Br J Plast Surg. 1988;41:451–469. [PubMed]

Articles from Clinical Orthopaedics and Related Research are provided here courtesy of The Association of Bone and Joint Surgeons