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 Table of Contents  
Year : 2019  |  Volume : 5  |  Issue : 1  |  Page : 41-46

Reconstruction of massive tibial defects after resection of adamantinoma with double-level distraction osteogenesis

1 Sloan Kettering Institute, New York, NY, USA
2 Department of Surgery, Orthopaedic Surgery Service, Memorial Sloan Kettering Cancer Center, New York, NY, USA
3 University of Vermont, Burlington, VT, USA

Date of Web Publication23-Aug-2019

Correspondence Address:
Dr. Eugenia Schwarzkopf
Sloan Kettering Institute, 1275 York Avenue, New York, NY 10065
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jllr.jllr_13_19

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Adamantinoma is an extremely rare disease that typically involves large portions of the tibial cortex requiring extensive resections, for which a myriad of complex reconstructions have been performed with varying success. Techniques of bone regeneration utilizing internal or external methods are used to manage bone defects in trauma, infection and congenital deformities, but less commonly used for oncological osseous defects. We present four cases of patients diagnosed between 2015 – 2018 with tibial adamantinoma in a background of osteofibrous dysplasia who underwent distraction osteogenesis reconstruction via a double level cable bone transport. In all cases wide resection of the adamantinoma was performed to achieve negative surgical margins and the defect reconstructed by double level bone transport using Ilizarov cables guiding distraction osteogenesis. Bone transport occurred at a combined mean rate of 2 mm per day: 1mm proximally and 1mm distally. Full weight-bearing and ambulation were encouraged immediately. The mean age at time of surgery was 18 years (14 – 25) and the mean size of tibial defect was 23 cm (17.5 – 26). The mean time in external fixation was 8.5 months (6 – 12 months), yielding a mean External-Fixation Index (EFI) of 0.44 month/cm (0.3 – 0.69). The average MSTS score at mean follow time of 20 months (13-27 months) is 28 (26 – 30). At last follow up all patients are infection free and without evidence of disease. Despite typical complications of prolonged external fixation, all four patients have excellent results with an average MSTS score of 28. The mean EFI of 0.44 month/cm is well below the standard EFI of 1 month/cm, suggesting this subset of patients may require less external fixation time than previously considered. The case series supports the hypothesis that double level D.

Keywords: damantinoma, distraction osteogenesis, double level bone transport, osteofibrous dysplasia, osteofibrous dysplasia-like adamantinoma

How to cite this article:
Schwarzkopf E, Klima MF, Trabulsy A, Prince DE. Reconstruction of massive tibial defects after resection of adamantinoma with double-level distraction osteogenesis. J Limb Lengthen Reconstr 2019;5:41-6

How to cite this URL:
Schwarzkopf E, Klima MF, Trabulsy A, Prince DE. Reconstruction of massive tibial defects after resection of adamantinoma with double-level distraction osteogenesis. J Limb Lengthen Reconstr [serial online] 2019 [cited 2020 Feb 19];5:41-6. Available from: http://www.jlimblengthrecon.org/text.asp?2019/5/1/41/265354

  Introduction Top

In 1900, Maier described the first case of a primary bone tumor with epithelial characteristics.[1] Although Fischer named this tumor adamantinoma (AD) due to its histologic resemblance to ameloblastoma of the jaw,[2] these are now regarded as distinct entities.[3] AD is a rare, malignant bone tumor representing <0.4% of all malignant bone tumors.[4] Typically, AD occurs in the long bones of the lower extremity, with 97% of all reported cases being in long tubular bones.[5],[6] The most common location is the mid-tibial shaft representing 80%–85% of cases, specifically the anterior tibial cortex.[7] AD has been reported in the humerus, ulna, femur, fibula, and radius; notably, it is less commonly reported in the flat, small bones of the spine, ribs, and carpal and metatarsal bones.[8] AD has multiple overlapping clinical, radiographic, and histologic characteristics with osteofibrous dysplasia (OFD).[9],[10] OFD is a rare, benign abnormality of bone formation that shares a predilection for the anterior tibial cortex. In addition, OFD-like AD represents a subset of AD in which the epithelial-like cells cluster in small nests within a background of OFD. There is a concern about malignant transformation from one entity to the other over time, making diagnosis of these three entities even more challenging.

Although there are no definitive guidelines for the treatment of AD, a wide surgical excision with negative margins is the current recommendation.[7] When inadequate resection is performed, the incidence of local recurrence has been reported to be as high as 90%.[11] It has been reported that AD can metastasize in up to 20% of cases,[6] mainly in patients with a history of local recurrence.[3] Large tibial bone defects, such as those created by resection of AD and OFD-like AD, pose unique reconstructive challenges due to a fragile soft-tissue envelope, its subcutaneous location, the large osseous defect, and postoperative stiffness in the adjacent ankle and knee.

There are several reconstructive options to bridge bone defects: allografts,[12] vascularized[13] or nonvascularized autologous fibula grafts,[14] intercalary prostheses,[15] or, more recently, distraction osteogenesis.[16] Reconstructions for large bone defects with nonviable bone have complication and failure rates of 8%[17] and 31%[18] at 105 and 108 months of follow-up, respectively, leading to poor long-term function. Distraction osteogenesis offers a durable long-term option for limb salvage of large bone defects after resection of tumors with the advantage of increasing the length and the volume of surrounding soft tissue simultaneously. There are significant long-term benefits of distraction osteogenesis as it regenerates viable, physiologic bone, which can fight infection, heal fractures, participate in normal hematopoiesis, and allow full activity. Techniques of bone regeneration utilizing internal or external methods are commonly used to manage bone defects in trauma, infection, and congenital deformities, but less commonly for oncological osseous defects.[19],[20] The majority of distraction osteogenesis has been performed with external fixation, though newer methods of bone transport are currently being explored. The external fixation index (EFI) represents a relatively consistent ratio of the total time from application to the removal of external fixation relative to the size of the underlying defect. The mean bone regeneration rate is 1 mm/day, which corresponds with a mean EFI of 1 month/cm.[21] At recent follow-up, the functional outcome was assessed with the Musculoskeletal Tumor Society (MSTS) score for lower extremity [Table 1].[22]
Table 1: Assessment of functional outcome with Musculoskeletal Tumor Society score for lower extremity

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Surgical technique

Distraction osteogenesis reconstruction typically involves several staged surgeries. The index surgery marks the beginning of the distraction phase, when the bone segments are gradually transported and/or lengthened within the limb to fill the osseous defect, and is completed when the bone has achieved its final length and position within the limb. In this lengthening method, an external fixator has multiple uses: maintain length, provide stability, and mechanically perform the double-level cable transport. The distraction is typically performed at an average rate of 1 mm/day to fill the defect;[23] therefore, the size of the defect ultimately determines the total duration of the distraction phase. Bone transport began on postoperative day 7 at a rate of 1 mm/day at each distraction site for a combined rate of 2 mm/day. The rate of transport can be adjusted throughout based on the quantity and quality of regenerate and the soft tissues. The external fixator is modified to allow complete bone opposition, compression, and autografting at the “docking” or junction site, and iliac crest bone marrow aspirate concentration is injected to the two regenerate sites. During the consolidation phase, the bone remodels to provide sufficient axial, rotational, and bending strength for the removal of the internal or external fixation without loss of alignment, length, or fracture. The completion of the consolidation phase of the reconstruction is marked by full osseous healing.

In all cases, wide resection of the AD from the affected tibia achieved negative surgical margins (R0 resection), and the defect was reconstructed by double-level bone transport using external fixation with the double-level Ilizarov cables for distraction osteogenesis. To stimulate bone regeneration, bone marrow aspiration concentration was injected into the regenerate areas during lengthening surgery in all four cases. Full weight-bearing, full range of the knee and ankle, and ambulation were encouraged immediately, and a physical therapy program was initiated.

  Case Reports Top

Case 1

A healthy 16-year-old male presented with a complaint of a painful bump on the lower leg. Radiographs and magnetic resonance imaging (MRI) revealed a large lesion consistent with AD centrally in the diaphysis and a satellite lesion proximally and distally in the right tibia [Figure 1]a, which was confirmed with biopsy revealing areas of both OFD-like and classic AD. A wide R0 resection resulted in a 23.5 cm diaphyseal defect and reconstructed using a tri-focal converging double-level bone transport [Figure 1]b. The external fixator was removed at 49 weeks postoperatively, yielding an EFI of 0.47 months/cm. Throughout the duration of external fixation, several courses of oral antibiotics and three hospitalizations for intravenous (IV) antibiotics were required to resolve pin site infections. Five weeks after removal, despite the use of a lower leg brace, the patient sustained a nondisplaced fracture at the junction of the proximal regenerate and proximal transport segment, which was treated conservatively without complications. Nine months after frame removal, the patient returned to full activity without any restriction, and the MSTS score at 27 months after index surgery is 30 [Figure 1]c.
Figure 1: (a) A 16-year-old male with central tibial diaphysis adamantinoma (size: 13 cm), (b) double-level converging cable bone transport in progress, (c) final result 27 months after surgery

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Case 2

A healthy 6-year-old male initially presented with a radiographic abnormality on his left tibia consistent with OFD via MRI and computed tomography scans. At the age of 14, he experienced a new onset of pain in the area of the OFD. Imaging studies showed an increase in a lytic lesion with a permeative appearance in the distal tibia [Figure 2]a and an open biopsy was performed revealing AD arising in the background of OFD with secondary aneurysmal bone cyst-like changes. A wide R0 resection resulted in a 25 cm diaphyseal defect and reconstructed using a tri-focal converging double-level bone transport [Figure 2]b. His postoperative course was complicated by osteomyelitis at the docking site requiring IV antibiotics, irrigations and debridement, and vacuum-assisted wound closure. Ten weeks after index surgery, he prematurely consolidated the proximal regenerate and lost fixation of the distal cable requiring re-osteotomy of the proximal segment and completion of the transport via the remaining proximal segment. The patient was forming such good bone proximally that lengthening was continued at a rate of up to 2 mm/day with robust regenerate formation. On completion of bone transport at 34 weeks, the external fixation was converted to a vancomycin-impregnated polymethylmethacrylate (PMMA)-coated intramedullary nail, yielding an EFI of 0.31 months/cm [Figure 2]c. The patient returned to full activity with an MSTS score of 30 at 24 months after the index surgery.
Figure 2: (a) A 14-year-old male with central tibial diaphysis adamantinoma (size: 19 cm), (b) double-level converging cable bone transport in progress, (c) final result 9 months after conversion to antibiotic-coated rod

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Case 3

A 24-year-old female with diabetes mellitus type 1 sustained a pathologic fracture through her right tibia [Figure 3]a. Biopsy showed OFD and she initially underwent curettage and bone grafting at an outside institution; however, final pathology confirmed the diagnosis of OFD-like AD. The patient then underwent R0 resection at our institution, leaving a defect of 17.5 cm. Initial reconstruction consisted of an intercalary metal implant, though her postoperative course was complicated by infection [Figure 3]b. After multiple wash out procedures, the hardware was removed, and the defect was reconstructed using a parallel double-level bone transport [Figure 3]c. The distal transport segment was resected after docking in the distal tibia given concerns for persistent osteomyelitis in this segment, and the transport was completed via the remaining proximal segment. Throughout the duration of external fixation, several courses of oral and IV antibiotics were required to resolve infections. At 12 months after external fixation application, she was converted to a vancomycin-impregnated PMMA-coated intramedullary nail [Figure 3]d, yielding an EFI of 0.69 months/cm. The patient returned to full activity with an MSTS score of 26 at 14 months after the lengthening surgery.
Figure 3: (a) A 24-year-old female, status postcurettage and bone grafting (performed at an outside institution) for central tibial diaphysis adamantinoma, (b) intercalary reconstruction with metallic spacer, complicated by deep infection, (c) double-level parallel cable bone transport in progress, (d) final result 6 months after conversion to antibiotic-coated intramedullary nail

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Case 4

A healthy 14-year-old male initially presented with leg pain leading to radiographs and MRI showing a lesion consistent with OFD of the right tibia with aggressive features. Biopsy confirmed OFD-like AD [Figure 4]a. Due to the heterogeneity of this lesion, and the intramedullary as well as extramedullary component visible on the MRI [Figure 4]b, the recommendation from our institution was resection with negative margins. An R0 resection was performed, resulting in a 26 cm diaphyseal defect [Figure 4]c. The patient underwent a bone grafting procedure at 6 months and external fixator removal at 10 months after index surgery, yielding an EFI of 0.3 months/cm [Figure 4]d. He had typical issues with infection intermittently during transport requiring both oral antibiotics and hospitalization for IV antibiotics. The patient returned to full activity with an MSTS score of 26 at 13 months after index surgery.
Figure 4: (a) A 14-year-old male with central tibial diaphysis adamantinoma (size: 23 cm), (b) magnetic resonance imaging (coronal fat-suppressed T2-weighted) showing adamantinoma with soft-tissue extension, completely involving the medullary cavity in places, (c) double-level converging cable bone transport in progress, (d) final result 10 months after surgery

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  Results Top

The mean age at time of surgery was 18 (range, 14–25), and the mean size of tibial defect was 23 cm (range, 17.5–26). The mean time in external fixation was 8.5 months (range, 6–12 months), yielding a mean EFI of 0.44 month/cm (range, 0.3–0.69). After a mean follow-up time of 19 months (12–28 months), the average MSTS score at recent follow is 28 (range, 26–30). At the last follow-up, all patients are infection free and without evidence of disease. Although all patients completed the large reconstruction with distraction osteogenesis and ended with excellent functional results, three out of four patients suffered complications. These complications include unplanned surgical intervention in two patients for osteomyelitis, which required conversion to antibiotic-impregnated PMMA-coated intramedullary nail, prolonged treatment with antibiotics, multiple surgical debridements, and negative pressure wound therapy. However, this did not prevent the patients from ambulation. Full weight-bearing (as tolerated) was encouraged after surgery. One patient required re-osteotomy for a premature consolidation, though this patient also made robust regenerate and was able to distract through this same regenerate site at double the normal rate for the remainder of the transport. One patient suffered a fracture through the regenerate, which was treated conservatively.

  Discussion Top

As these cases elucidate, ADs commonly involve large portions of the tibial diaphysis. Wide resection as the standard treatment makes reconstruction of such massive osseous defects challenging.[7] We present four patients with large bone defects after wide resection of AD in the background of OFD successfully treated with distraction osteogenesis via a double-level, cable bone transport technique. Despite encountering typical complications of prolonged external fixation, of which infection was the most common, all patients returned to full activity without restriction and without evidence of local or distant recurrence.

This report has several limitations, notably the small number of patients and short follow-up duration that is inadequate to assess the risk of recurrence or metastasis of AD. The drawbacks to the double-level bone transport technique are the prolonged external fixation time and the frequency of complications, though these are typical for large defects requiring prolonged external fixation. Ultimately, neither the regenerate fracture nor the infections led to dysfunction or disability and all patients regained full range of motion of the knee and ankle, resumed normal activity, including return to sports. However, due to short-term follow-up, it may be too early to comment upon the long-term results, especially in regard to deep infection or recurrence of the tumor.

The surgical technique described has several advantages over other reconstruction options. There is no restriction on activity or weight-bearing from the onset compared to allograft or vascularized fibula reconstruction. There is no donor site morbidity as with a vascularized fibula, nor the prolonged time required for hypertrophy of the fibula. There is no retained hardware required to maintain long-term durability, lowering the risk of infection, and facilitating postsurgical surveillance imaging of the affected extremity. Compared to standard single-level reconstruction, double-level cable transport has a lower EFI, suggesting that this technique is more tolerable by decreasing the external fixation time. The use of cables minimizes the soft-tissue scarring and muscular fibrosis compared to pin- or wire-based fixation, especially over such large distances.

Historically, ADs were treated with amputation, but advances in surgical techniques allow reconstructions following en bloc resection.[24] Houdek et al.[25] published a long-term follow-up '' 46 AD patients who have been treated with limb salvage surgery. Reconstructive techniques included intercalary fibula (n = 13), structural allograft (n = 12), no reconstruction (n = 4), arthrodesis (n = 2), cortical iliac crest and internal fixation (n = 2), allograft and intercalary fibula (n = 1), one-bone forearm (n = 1), bone transport (n = 1), and prosthesis (n = 1). In their series, limb salvage failed in 6 (13%) patients, necessitating amputation for local recurrence in five patients and infection in one. The overall limb salvage rate was 67%.[25]

Qureshi et al.[24] published a multicenter study that included 70 AD patients who have been treated at 23 European cancer centers. In their study, limb salvage was attempted in 64 (91%) cases. Of these, 5 (7%) patients later required amputation. Reconstruction with an allograft was used in 39 (61%) cases. 19 (30%) and 16 (25%) patients needed vascularized fibular and non-vascularized autogenous reconstruction, respectively. 30 (84%) patients had reconstruction-related complication. Nonunion and fracture were the most common complications, occurring in 15 (24%) and 14 (23%) patients, respectively.[24]

The small number of patients in our study is not representative; however, other authors have reported comparable rates of complication in patients who underwent DO. In a retrospective review of 63 patients, Liantis et al.[26] reported a complication rate of 77% after limb lengthening procedures in a nononcologic setting. Tsuchiya et al.[27] reported the results of 19 patients who underwent DO for the reconstruction of bony defects after the excision of skeletal tumors in the limbs. There were 10 complications (52%) in 19 patients, all of which were successfully treated. Functional evaluation gave excellent results in 12 patients, good in five and fair in two.

Our results indicate that despite various disadvantages, DO is an effective technique for limb reconstruction of bone tumors and provides bone which will develop sufficient biomechanical strength and durability.

  Conclusion Top

Despite typical complications of prolonged external fixation, all patients in this small series have excellent results with an average MSTS score of 28. The average EFI of 0.44 months/cm supports the hypothesis that double-level DO with cable transport is an effective surgical reconstructive option in massive tibial defects offering an excellent option for sustainable limb reconstruction.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Research at Memorial Sloan Kettering Cancer Center is supported in part by a grant from the National Institutes of Health/National Cancer Institute (#P30CA008748) and the grant “CyCle for Survival.”

Conflicts of interest

There are no conflicts of interest.

  References Top

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Ilizarov GA. The tension-stress effect on the genesis and growth of tissues. Part II. The influence of the rate and frequency of distraction. Clinical orthopaedics and related research 1989;239: 263-85.  Back to cited text no. 21
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Liantis P, Mavrogenis AF, Stavropoulos NA, Kanellopoulos AD, Papagelopoulos PJ, Soucacos PN, et al. Risk factors for and complications of distraction osteogenesis. Eur J Orthop Surg Traumatol 2014;24:693-8.  Back to cited text no. 26
Tsuchiya H, Tomita K, Minematsu K, Mori Y, Asada N, Kitano S. Limb salvage using distraction osteogenesis. A classification of the technique. J Bone Joint Surg Br 1997;79:403-11.  Back to cited text no. 27


  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1]


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