Axial computed tomographic scan of patient 4 (case 1), demonstrating a destructive lesion involving the left hemimandible (aggressive juvenile fibromatosis).
Intraoperative photograph of patient 4 (case 1), demonstrating the fibula reconstruction of the left mandible with osseointegrated implants in place.
Panorex radiograph taken 4 years postoperatively, demonstrating symmetrical mandibular development in patient 4 (case 1).
Postoperative photograph taken 4 years and 2 months after fibular reconstruction of the left mandible, demonstrating facial symmetry in patient 4 (case 1).
Intraoperative photograph of palatomaxillary defect in patient 5 (case 2) after resecting an ossifying fibroma.
Reconstructed maxilla of patient 5 (case 2) after placement of osseointegrated implants.
Left, Frontal view of patient 5 (case 2) 4 years after palatomaxillary reconstruction with scapular free flap demonstrating normal facial symmetry. Right, Oblique view of the same patient 4 years after palatomaxillary reconstruction with scapular free flap, demonstrating normal facial contour.
Growth of the pediatric mandible. Downward and anterior projection of the mandible results from growth at the epiphyseal plates located within the condylar neck. Lingual bone resorption (black arrows) and buccal bone deposition (small white arrows) are responsible for contour and width. Large white arrows indicate the axis of condylar epiphyseal growth.
Ossification centers of the scapula are located at the medial scapular border and the glenoid fossa (darkened areas). The lateral border serves as a traction epiphysis.
The iliac ramus serves as a major ossification center in the pediatric ilium (darkened area). Disturbance of growth in this region may have profound effects on the development of normal gait stability.
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Genden EM, Buchbinder D, Chaplin JM, Lueg E, Funk GF, Urken ML. Reconstruction of the Pediatric Maxilla and Mandible. Arch Otolaryngol Head Neck Surg. 2000;126(3):293–300. doi:10.1001/archotol.126.3.293
The creation of osseous defects in the upper and lower jaws in children is an uncommon occurrence. It is therefore likely that a head and neck reconstructive surgeon will accumulate only limited experience in restoring such defects. We have reviewed 7 pediatric bone-containing microvascular free flap reconstructions in 6 patients for reconstruction of the upper or lower jaws. Three patients were available for long-term follow-up to evaluate the effect of osseous free flap reconstruction on function and growth and development of the donor site.
Academic tertiary referral center for otolaryngology.
Patients and Methods
Six pediatric patients ranging in age from 8 to 16 years underwent 2 fibular, 4 scapular, and 1 iliac free flap procedure for restoration of 2 maxillary and 5 mandibular defects from 1992 to 1997. Three of the 6 patients were available for long-term follow-up to assess the postoperative donor site function in an effort to determine the effect of this surgery on long-term donor site morbidity and development.
Two patients were lost to follow-up, and 1 died secondary to complications related to distant metastatic disease. Three of 6 patients were observed for 2 years 6 months, 4 years, and 4 years 2 months, respectively. Two of the 3 patients who were observed long term have undergone full dental rehabilitation and currently maintain a regular diet and deny pain with mastication or deglutition. One patient did not require dental rehabilitation. All 3 patients demonstrate gross facial symmetry and normal dental occlusion. Assessment of the fibular donor site demonstrated normal limb length and circumference. The patients denied pain or restriction to recreational activity. Scapular donor sites demonstrated normal range of motion, strength, and shoulder stability.
Free flap reconstruction of the pediatric maxilla and mandible requires harvesting bone from actively growing donor sites. We have found no evidence of functional deficit after bone harvest from the fibular or scapular donor sites. Patients demonstrate normal growth at the donor sites, and symmetry of the mandible and maxilla is preserved.
MANDIBULAR and maxillary reconstruction in children is uncommon. When faced with this challenge, however, it is essential that special consideration be given to issues related to the growing child to achieve optimal restoration of mastication, deglutition, and cosmesis. Similar to reconstruction of the adult mandible, bone stock, soft tissue, and skin paddle design are important factors in addressing the specific reconstructive requirements of the patient. In contrast to the adult patient, however, the pediatric patient is growing. Surgical reconstruction of the upper and lower jaws requires an understanding of the changes in bone and soft tissue architecture at both the donor site and the mandibulofacial complex as a result of growth and development.
While many factors must be considered when choosing a donor site, there are several issues that are unique to the developing child. The commonly used donor sites, including fibula, iliac, and scapula, all possess epiphyseal growth centers. An understanding of the anatomic location of these growth centers and their role in normal development is essential to preventing long-term functional deficits. Similarly, the process of craniofacial development is a dynamic one where mandibular, maxillary, and basicranial growth are intimately interrelated. The disruption of these relationships, as occurs with a mandibular or maxillary resection, can result in abnormal development of the midface, mandible, and skull base, leading to profound long-term functional consequences. Restoration of these relationships with free flap reconstruction, however, can reestablish mandibulomaxillary occlusion and condylar-basicranial articulation, thereby preventing abnormal craniofacial development.
In contrast to those of adults, most diseases affecting the upper and lower jaws of pediatric patients are benign,1 requiring only narrow margins and in turn necessitating minimal soft tissue reconstruction. In these cases, options for reconstructing the jaw include vascularized composite flaps and nonvascularized bone grafts. Sarcomas are the most common malignancies to involve the mandible in this age group.2 While surgical resection plays an important role in the treatment of this disease, in many cases these patients have been previously treated with chemotherapy, radiation, or a combination of both. As a result, the recipient bed is often compromised with regard to healing,3,4 thus limiting the application of adjacent tissue transfer or bone grafts. While strategies to minimize the effect of chemotherapy and radiation on the healing of soft tissue and growth of the craniofacial skeleton have been investigated,3 under these circumstances free vascularized tissue remains the most reliable source of bone and soft tissue. The selection of a reconstructive technique that supplies adequate bone stock for the placement of osseointegrated implants must be weighed against the potential for donor site morbidity.
In contrast to the adult patient, where the selection of a donor site is based not only on the requirements of the defect but also the patient's comorbidities,5 the pediatric patient is usually healthy and in good nutritional status. Issues related to long-term development at the reconstructed site and at the donor site are the central concern. We have reviewed 7 microvascular reconstructions of the upper or lower jaws in 6 pediatric patients in an effort to elucidate factors such as donor site selection, reconstructive approach, technical considerations, and the role of osseointegrated implants, which are unique to this population. We have also obtained long-term follow-up on 3 patients in the series of 6 to examine the long-term effects of free flap harvest on donor site function.
The following is a retrospective review of 6 pediatric patients who underwent mandibular or maxillary reconstruction following ablative treatment for either benign or malignant disease from June 1992 until October 1997 at Mount Sinai Medical Center, New York, NY. Patients were included in the review if they were aged 16 years or younger and had undergone reconstruction of the maxilla or mandible with osteocutaneous free tissue transfers. Over a 5-year period, 6 pediatric patients underwent free flap reconstruction of the maxilla or the mandible. Three of the 6 patients were available for long-term follow-up.
The surgical records of all 6 patients were reviewed for factors pertaining to donor site selection, technical considerations, and reconstructive approach. The 3 patients who were available for long-term follow-up were evaluated for donor site function, respectively, 4 years and 2 months, 4 years, and 2 years and 6 months postoperatively. Donor site strength and range of motion were determined for the scapular donors by a physical therapist, and for the fibula donor, by an orthopedic surgeon. Range of motion, strength, and flexibility tasks were performed on the donor side and compared with the unaffected (control) side in all patients. This aspect of the evaluation included full shoulder and elbow adduction, full shoulder and elbow abduction, medial and lateral shoulder rotation, pronation and supination, and a series of biceps, triceps, and shoulder strength exercises. Lower extremity iliac crest and fibula donor sites were evaluated with a full range of hip, knee, and ankle exercises. Limb length and circumference were assessed by an orthopedic surgeon using standard limb measurement techniques. Strength was not assessed.
Each of the 3 patients was asked the following questions: (1) Do you presently have pain at the donor site during rest? (2) Do you have pain at the donor site during physical activity? (3) Is your participation in recreational activities/sports limited as a result of pain or restriction at the donor site? (4) Does the scar at your donor site disturb you or affect your activity? and (5) Do you favor donor site arm/leg during physical activity? All 5 questions were administered to each of the 3 patients available for long-term follow-up.
Fibula donor sites were treated with a posterior plaster splint applied in the operating room and worn for 10 days, after which the patient entered full weight-bearing physical rehabilitation. Closure of the scapular donor sites were performed by reattaching the teres major and teres minor muscles to the cut edge of the lateral border of the scapula using nonabsorbable sutures. Scapular donor sites were treated by placing the donor site arm in a crossbody sling for 10 days. Mandibular and maxillary reconstructions were fixed with a titanium plating system and titanium screws. All patients had fixation hardware removed between 12 and 18 months postoperatively.
The average age of our 6-patient cohort was 13.2 years, with a range of 8 to 16 years (Table 1). Five patients were boys and 1 was a girl. All 6 patients were surgically treated and underwent reconstruction primarily at Mount Sinai Medical Center except for patient 6, who presented for a secondary reconstruction after receiving chemotherapy and external beam irradiation followed by surgical resection for rhabdomyosarcoma at an outside hospital. Two patients were lost to follow-up (patients 1 and 3), and 1 (patient 2) died of complications related to distant metastases. Patients 4, 5, and 6 were contacted and evaluated postoperatively at 4 years 2 months, 4 years, and 2 years 6 months, respectively. Primary disease processes of the patients reviewed included rhabdomyosarcoma (1), osteogenic sarcoma (2), aggressive juvenile fibromatosis (1), ossifying fibroma (1), and fibrous dysplasia (1). The 3 patients diagnosed with malignant sarcoma had all received chemotherapy and external beam irradiation prior to surgical reconstruction.
Two patients underwent reconstruction for maxillectomy defects using scapular osteocutaneous free flaps (patients 1 and 5) (Table 1). The remaining 4 patients were treated for mandibular defects using fibular (patients 3 and 4), scapular (patient 2 and 6), or iliac (patient 2) free flaps. Patient 2 was originally treated with an iliac osteocutaneous free flap and a radial forearm free flap after resection of a primary osteogenic sarcoma of the mandibular body. Resection of a large segment of skin of the mentum and anterior neck resulted in a larger-than-expected soft tissue defect. Although a large iliac skin paddle was harvested, a radial forearm free flap was required to prevent contracture and malposition of the lower lip. A recurrence adjacent to the posterior osteotomy in the ascending ramus 18 months postoperatively required a second resection and reconstruction with an osteocutaneous scapular free flap. No patient experienced an intraoperative or postoperative head and neck or donor site complication.
Dental implants were placed primarily in patient 1 and secondarily in patients 3, 4, and 5. Implants were successfully secured without bone augmentation in patients 4 and 5; however, patient 3 was an 11-year-old girl with a small-diameter fibula requiring a "double barreling" technique.6 To perform this technique, one third of the circumferential cortical bone was removed from the fibula and a midpoint transverse osteotomy was performed in which the fibula was folded on itself and secured with lag screws. This roughly doubled the area of bone stock, allowing for the secure placement of osseointegrated implants.
The scapular bone used for palatomaxillary reconstruction in patient 1 required onlay iliac bone grafts to augment the bone stock and successfully secure osseointegrated implants. These nonvascularized onlay grafts were harvested through a separate incision adjacent to the anterior-superior iliac crest.
All 6 patients had unremarkable immediate postoperative recoveries with well-controlled pain management and physical therapy instituted by postoperative day 7. Patient 2, who was the only patient to undergo an iliac crest free flap reconstruction, had an unremarkable postoperative course. One month postoperatively, he had no gait deficit or pain associated with the harvest site.
Patients 4, 5, and 6 denied pain at rest or with physical activity at the donor site. None of the 3 patients favored the donor limb, and all felt the donor site scar did not restrict their activity, nor was it cosmetically displeasing. Patient 4 related "discomfort and stiffness" in his ankle for nearly 2 years after the fibula harvest. However, he has become progressively more active and presently reports "no limitations to recreation." Patients 5 and 6, who underwent scapular reconstructions, denied shoulder pain or stiffness, and both demonstrated normal shoulder strength, mobility, and range of motion. All 3 patients are currently active in recreational and school-related sports, and all report being satisfied with their current state of rehabilitation. All 3 patients observed long-term maintain a full diet without restrictions. All deny pain or discomfort with mastication or swallowing.
Patient 4 was 8 years old at the time of resection of an aggressive juvenile fibromatosis lesion involving the left hemimandible (Figure 1). The resection involved ablation of the ramus, body, and hemisymphyseal portions of the mandible. The lingual and hypoglossal nerves were preserved; however, the mental branch of the trigeminal nerve was resected with the specimen. A primary nerve graft was performed using a greater auricular nerve graft. Reconstruction of the defect was performed with a contralateral fibular free flap and osseointegrated implants were placed primarily (Figure 2). A panorex radiograph taken 6 months postoperatively demonstrated bony union (Figure 3). A photograph of the patient taken 4 years postoperatively demonstrated symmetrical growth of the lower third of the face (Figure 4). Mandibular reconstruction plates were removed 18 months postoperatively.
Patient 5 was 15 years old at the time of resection of an ossifying fibroma of the left hemipalate and maxilla (Figure 5). A scapular osteocutaneous free flap was used to reconstruct this defect. The proximal lateral scapular border was used as a vertical buttress, and the distal scapular tip, based on the angular artery, was used to reconstruct the palate. A bilobed scapular/parascapular skin paddle was designed such that one skin paddle was used to reline the intraoral palatal defect, and the other to reline the nasal cavity. Osseointegrated implants were placed secondarily to permit functional prosthetic rehabilitation (Figure 6). Four years postoperatively, the patient demonstrated symmetrical facial growth (Figure 7). There is minimal donor site scar contracture and the patient has no restriction in shoulder mobility.
Normal craniofacial development is dependent on the relationships between the mandible and maxilla. A disruption in this relationship prior to mandibulofacial epiphyseal fusion, which occurs between the ages of 13 and 18 years, can result in profound midface deformity. Osseous reconstruction of maxillary and mandibular postablative defects may prevent developmental facial deformity; however, one must carefully consider the risk of harvesting bone from a growing child. Essential in choosing a donor site for pediatric maxillary or mandibular reconstruction is an understanding of the growth centers and the morbidity associated with each of the donor site options.
Mesenchymal in origin, bone is a living tissue making up the majority of the human skeleton. The craniofacial skeleton, including the mandible, grows through 2 mechanisms: epiphyseal proliferation and remodeling. Epiphyseal proliferation is largely responsible for increases in bone length and projection, a process that is dominant during the first 18 years of life. After age 18, the epiphyseal plate, located in the proximal zone of the conical subcondylar ridge, fuses. Prior to fusion, it exists as a 3-dimensional structure that, under the influence of the surrounding soft tissues, is essential to normal mandibular projection. The epiphysis adapts the intercondylar distance to the widening cartilaginous synchondrosis of the cranial base, highlighting the ever-important relationship between normal mandibular growth and normal basicranial development. The role of epiphyseal growth, particularly in the prepubescent pediatric patient, cannot be overemphasized.
However, bone remodeling plays an equally important part in mandibular contour and symmetry. In contrast to epiphyseal growth, remodeling is a process that occurs throughout adulthood. Downward and forward projection of the mandible occurs through deposition of bone at the posterior margin of the ramus and corresponding resorption at the anterior margin (Figure 8). Likewise, mandibular contour and width occur as a function of buccal bone deposition and concomitant lingual resorption (Figure 8). The 2 processes of epiphyseal growth and bone remodeling occur in different areas within the same bone simultaneously, and there is no histological difference in new bone created by either process. While epiphyseal fusion occurs in early adolescence, remodeling continues throughout adult life largely in response to the mechanical stress applied by the muscles of mastication.7,8 Understanding these principles is important to surgical reconstruction because disruption of the mandible prior to epiphyseal fusion may result in a different long-term developmental defect than a similar surgical disruption after epiphyseal fusion. It is also important to recognize that girls reach mature mandibular height and depth at a mean age of 13 on average, 2 to 5 years earlier than boys.
Finally, the occlusal interaction between the maxilla and the mandible is of paramount importance for normal craniofacial development, such that unreconstructed defects of the pediatric maxilla can lead to substantial disturbances in facial growth. Normal maxillary width occurs as a result of bony accretion at the suture lines and resorption at the lateral nasal wall. Vertical growth of the midface is the combined result of downward displacement of the maxilla and remodeling at the bone surfaces. Fusion between the palatine processes occurs at age 18 years, and there are no endochondral growth plates in the maxilla because all growth occurs as a result of osteogenic activity at the suture lines. Girls complete vertical growth at about age 14 years and boys reach maturity 2 years thereafter.
Fibular growth, which has been studied quite extensively, occurs in a classic endochondral pattern because the 3 ossification centers, 1 in the shaft and 1 in each of the distal and proximal epiphyses, are responsible for proportionate growth. The growth plates lie within 1 to 2 cm of each end of the bone, proximal and distal to where a harvesting osteotomy should be made. Most growth occurs in the proximal epiphyseal plate, which fuses by age 15 for girls and age 17 for boys.9 Similar to the adult's, the pediatric patient's fibula offers the longest segment of bone of the 3 donor sites; however, the stock of bone, particularly in patients under the age of 13, may lack the height appropriate to stabilize osseointegrated implants. As demonstrated in case 1, a portion of the cortex of the fibula can be cut away at the surface and the fibula can be double barreled6 by creating a midpoint osteotomy and folding the bone on itself. This results in an increase in the bone height and a more stable foundation for osseointegrated implants. The double-barreled fibula can be secured on itself by placing a vertical lag screw or circumosseous wires at each end of the complex. While the epiphyseal plates were not transferred in the cases reported herein, the fibula will continue to grow with the adjacent native mandible,10-13 which allows for reliable healing and volume retention. It has been shown experimentally11,14 that transferred epiphyseal plates retain the potential for growth. Although it has not been reported clinically, this may serve as a potential source for condylar reconstruction in the prepubescent pediatric patient.
Harvesting the fibula from a growing limb has raised concerns among reconstructive surgeons; however, there is little clinical evidence suggesting that long-term limb growth is adversely affected. Experimental evidence in rats demonstrates that the fibula exerts a restrictive effect on tibial growth such that removal of the fibula leads to longitudinal tibial overgrowth.13 However, clinically, leg length discrepancy has not been demonstrated and did not occur in our patient. The most substantial delayed complication associated with fibula harvest, particularly in children younger than 9 years, is a valgus deformity at the donor ankle.15 While our patient did not demonstrate this complication, Omokawa et al15 have found that performing a synostosis at the time of the harvest prevented valgus deformity in 90% of patients younger than 8 years. The patient in our series denied pain or restriction in the donor limb at the time of follow-up and reported no difficulties during activities of recreation or daily living. Furthermore, the patient denied any restriction in his ability to participate in sports (ie, running and jumping).
Unlike the fibula, the scapula is a flat membranous bone. The lateral scapular border and scapular tip develop from a large osteocartilaginous epiphyseal plate. At birth, the inferior 7 to 8 cm is composed entirely of hyaline cartilage. Ossification proceeds in a superior to inferior pattern until approximately age 10, when the scapula is roughly 12 cm long and the distal epiphysis has decreased to 4 cm (Figure 9). A smaller but equally important growth plate exists superiorly, adjacent to the glenoid fossa.16 Mainly responsible for vertical scapular growth, the superior growth plate lies outside the range of harvested bone, and therefore should not be directly affected. Both superior and inferior growth plates fuse at age 20 resulting in a disruption of the normal scapular development by harvesting bone from the lateral border of the scapula in the pediatric patient. The lateral border of the scapula serves as a traction epiphysis, growing in response to pull of the teres and triceps muscle groups.14 Teot et al16 found that harvesting bone from this area for congenital limb reconstruction resulted in a moderate scapular size discrepancy, but no appreciable functional deficit. They concluded that the upper growth plate compensates for disruption of the lateral scapular border, although there is no objective data to support this claim. Similarly, our patients demonstrated no functional deficit with regard to objective measurements in strength and/or range of motion. When asked about activity, they described no restrictions or pain. When asked to compare the affected side with the contralateral shoulder, they related little or no difference during activities of recreation (ie, throwing a ball, lifting a heavy object) or daily living.
While the adult scapula has been shown to accommodate osseointegrated implants,17 the pediatric scapula may be quite thin and limit the stability of implants. To facilitate implant stability, iliac crest bone onlay grafts were used in patient 1 to augment the scapular bone during the secondary placement of osseointegrated implants. Both patients underwent successful implants and maintain an unrestricted regular diet.
The entire length of the iliac crest, from the anterior-superior to the posterior-superior iliac spines, is composed of cartilage at birth. Growth occurs in an epiphyseal fashion in several areas of the pelvic girdle, including the acetabulum and the iliac crest, which grow until the second decade of life (Figure 10). The mechanical demands applied to the pelvis by both its upper and lower muscular attachments play an active role in pelvic remodeling, which occurs into young adulthood. Like the lateral scapular border, the crest serves as a traction epiphysis where the dynamic interaction between the iliac crest and its muscle attachments plays a crucial role in acetabular development, and hence gait stability. Disturbance of gait after iliac crest free flap harvest in the adult population has been documented in up to 11% of patients.18,19 Boyd20 described only minimal donor site morbidity in his series of iliac crest free flaps on young adults. However, his population ranged in age from 16 to 27. The probability of profound gait disturbance in a younger age group has discouraged surgeons from using this donor site for reconstruction, and as a result, there are no reported series of iliac crest free flap reconstructions in the pediatric population. We performed 1 case of mandibular reconstruction using the iliac crest free flap; however, this patient was not available for long-term follow-up. During the immediate postoperative course, this patient was ambulatory and actively participating in physical therapy.
Although fibular and scapular grafts have been used quite extensively by plastic surgeons for the reconstruction of acquired and congenital limb abnormalities, there is little reported on the long-term growth of the transferred bone after mandibular and maxillary reconstruction in the pediatric population. There is good evidence to support the preservation of osteocyte viability after the transfer of non–epiphyseal-containing vascularized bone,10-13 but the bone growth may be unpredictable. While experimental evidence supports the hypothesis that vascularized membranous bone grafts transferred to the mandible and zygomaticomaxillary defects in immature animals contribute to normal craniofacial development in a more predictable fashion than nonvascularized bone grafts,21 there is little evidence to support this clinically. Similarly, it has been suggested that a linear relationship between bone stress and bone growth8 may be responsible for symmetrical growth of the transplanted bone, but again, this relationship remains only speculative. In our patients, gross symmetrical maxillary and mandibular growth has occurred in reconstructions with both scapular and fibular free flaps. The advantage of primary bone-containing free flap reconstruction is borne out by the preservation of normal occlusal relationships throughout the patient's development. As discussed earlier, failure to reestablish maxillomandibular occlusion will lead to abnormal maxillofacial growth and malocclusion. This was not apparent in our series of patients, but we have not performed serial radiological evaluations and standard cephalometrics, an evaluative process that is necessary to draw a conclusion regarding donor bone growth and craniofacial development.
Finally, long-term follow-up of 3 pediatric patients undergoing reconstruction with a single fibular and 2 scapular free flaps demonstrates that there is no evidence of physical developmental abnormalities as a result of the free tissue harvest. A larger series with serial radiographic assessment of the reconstructed site is necessary to derive a conclusion regarding the growth of transplanted bone and its effect on maxillofacial development.
Accepted for publication January 3, 2000.
Presented at the annual meeting of the American Head and Neck Society, Palm Desert, Calif, April 24, 1999.
Reprints: Eric M. Genden, MD, Mount Sinai School of Medicine, Department of Otolaryngology–Head and Neck Surgery, Box 1189, 1 Gustave Levy Pl, New York, NY 10029 (e-mail: firstname.lastname@example.org).