Surgical reconstruction of large defects of the long bones by free vascularized bone grafts. Functional results after a minimum of five years of follow-up.
Kai Bauwens, MD, Dirk Stengel, MD MSc, Jens-Ingmar Höpfner, MD, Ulrich Weber, MD PhD and Andreas Eisenschenk, MD PhD
From the Department of Hand, Replantation and Microsurgery, Unfallkrankenhaus Berlin Trauma Center, Berlin (AE, KB, JIH), the Department of Trauma and Orthopedic Surgery, University of Greifswald (KB, DS), the Department of Clinical Epidemiology, Unfallkrankenhaus Berlin Trauma Center, Berlin (DS), and the Department of Orthopaedic Surgery, Charité Medical Center, Berlin (UW)
Corresponding address Kai Bauwens MD, Department of Trauma and Orthopedic Surgery, Unfallkrankenhaus Berlin Trauma Center, Warener Str. 7, 12683 Berlin, Germany Phone
(49) 30 5681 2601
Fax
(49) 30 5681 3003
E-mail
[email protected]
Surgical reconstruction of large defects of the long bones by free vascularized bone grafts. Functional results after a minimum of five years of follow-up.
2
Abstract
44 patients (26 men, 18 women; mean age 29 ± 15 years) with large defects of the long bones were reconstructed by free vascularized bone grafts and were examined after an average follow-up of 8.6 ± 2.1 years. The Enneking-Index averaged 78.6% (95% CI 73.8 – 83.4%). No differences were noted for different types of graft, etiologies or anatomical locations. Regression analysis did not reveal associations between defect size and functional results. Sixteen patients developed 29 complications. All except one patient showed full incorporation of the graft. The results confirm the value of vascularized grafts for bridging large bone defects.
3
Introduction
Osteoblasts do not survive in biological surroundings with low oxygen tension. Thus, bridging large bone defects by avascular grafts involves creeping substitution, with cells migrating from the well perfused resection and junction area into an almost acellular matrix. This demands time and bears a high risk for complications like bone atrophy, transplant fracture, and non-unions.
With innovative microsurgical techniques, it became possible to use free vascularized grafts as bone void fillers.1-3 Theoretically, preserving arterial blood supply of the periost and endost enables primary healing, as induced by vital osteoblasts.4,5 There is evidence from animal experiments that vascularized grafts are superior to avascular transplants by prolonged vitality, rigidity, resistance to bacterial infection, and load-dependent hypertrophy.6-10 Following the first report of human vascularized bone transplantation by Taylor in 197511, many case series from various countries stressed the feasibility of this surgical technique for limb-sparing surgery in benign and malignant disease.12-22 However, there is still sparse information on long-term outcomes. Also, there is scientific and clinical debate about the defect size which should prompt filling by a vascularized graft rather than by cancellous bone. Most authors promote vascularized grafts if defect lengths exceed 6 cm, especially in case of vulnerable or scarred wound beds after radiation, or bacterial infection.9,23
4
In this retrospective study, we examined clinical and radiographic outcomes after vascularized grafting of large long-bone defects of the upper and lower extremity after a minimum of five years of follow-up. We reasoned that this method ensures long lasting stability and functionality of the affected limb.
Patients and Methods
Study Sample
Between September 1988 and August 1997, 74 consecutive subjects were treated by free vascularized bone grafting for long bone defects of different causes and were eligible to participate in this study. All grafting procedures were performed by a single author (AE). During this interval, it was the hospital’s policy to recommend vascularized autologous grafts rather than cryopreserved allogenic bone or prostheses. The rationale for this policy was to achieve a definitive, biological, potentially long-lasting solution, even if fusions had to be carried out in case of joint involvement. Because of the heterogenous population with varying defect characteristics, it was on the surgeon’s discretion to decide about the most appropriate donor graft, the need for additional cancellous bone, and the choice of fixation material. Patients were identified by the hospital information system and local registration offices.
5
Outcome Assessment
Clinical outcomes were assessed by the Enneking score, which had been developed for the evaluation of clinical results after surgical resection of musculoskeletal tumors.24 This practical outcome tool comprises a general part measuring the three dimensions pain, function, and emotional acceptance, and a specific part addressing individual disabilities of the upper and lower extremities. The specific part for the upper extremity covers hand positioning, manual dexterity, and lifting ability, whereas the lower extremity part scores supports, walking ability, and gait. Each category is rated between 0 (worst result) and 5 (best result). Thus, the total score sums up to a maximum of 30 points. In the international literature, mean scores are frequently reported as percentage of the maximum, the so called Enneking index. Complications were recorded by history taking, and a detailed survey of hospital charts.
Statistical Analysis
Patient profiles and outcome data were analyzed descriptively. Where suitable, we calculated 95% confidence intervals (CI) for means and proportions. If subgroups were sufficiently large, results were compared by non-parametric tests (that is, the MannWhitney or Kruskal-Wallis test), with p-values interpreted in an exploratory intent. The association between continuous exposures and outcomes was assessed by linear regression analysis, and we provided the coefficient beta and its 95% CI.
6
Results
Study sample
Figure 1 sketches the study profile. Altogether, forty-four patients provided informed consent, and form the basis of this report. There were 26 men and 18 women, with a mean age of 29.2 ± standard deviation 15.4 years. Table 1 summarizes patient demographics and disease characteristics.
Twenty-three patients underwent extra augmentation by cancellous bone. Because of defects close to or expanding the joint facets, joint fusions had to be carried out in fifteen patients. Post-operative rehabilitation was planned individually, with 34 patients receiving tailored orthoses. Further details are listed in Table 2 and 3.
Functional outcome
After a mean follow-up of 8.6 ± 2.1 years, the overall Enneking-Score for both upper and lower extremities averaged 23.6 (95% CI 22.2 – 25.0), or 78.6% (95% CI 73.8 – 83.4%) of the maximum index. Pain was rated at a mean score of 4.2 (95% CI 3.8 – 4.5), whereas function and emotional acceptance averaged 3.2 (95% CI 2.7 – 3.6), and 4.4 points (95% CI 4.1 – 4.7).
7
Twenty-six patients were free of pain (59.1%, 95% CI 43.2 – 73.7%), including all subjects with congenital tibial pseudarthroses. Two patients complained of pain at the donor site (4.5%, 95% CI 0.6 – 15.5%). Table 4A and 4B summarize scoring results for individual dimensions of the Enneking instrument after surgery to the upper and lower extremity.
No differences were noted in overall scores for different types of graft (Figure 2), etiologies (Figure 3), or anatomical locations (Figure 4). Patients with joint fusion had slightly lower scores than patients with preserved joint motion (mean difference, 2.1 points, 95% CI -0.8 – 4.9). Age at the time of surgery did not affect Enneking scores (beta -0.07, 95% CI -0.17 – 0.02). Also, regression analysis did not reveal significant associations between the size of the defect or the transplant and functional outcomes (see Figure 5). The radiological and clinical findings of a patient suffering from plasmacellular osteomyelitis of the left femur who underwent resection and reconstruction by both vascularized and avsacular grafts is depicted in Figures 7 to 9. Complications
Sixteen patients (36.4%, 95% CI 22.4 – 52.2%) developed 29 complications (see Table 3). Of note, twelve patients (27.3%) had transplant fractures requiring surgical revision (n=9), or cast immobilization and prolonged orthotic stabilization (n=3). Eight fractures were considered fatigue breaks, whereas the remaining fractures occurred after falls.
8
Only one patient progressed to above-knee amputation because of a septic non-union. In all other cases, the bone graft was considered consolidated on plain X-ray films (97.7%, 95% CI 87.9 – 99.9%).
The radiological and clinical findings of a patient suffering from plasmacellular osteomyelitis of the left femur who underwent resection and reconstruction by both vascularized and avsacular grafts is depicted in Figures 6 to 8.
Discussion
Large long bone defects are rare entities, and surgical treatment must be planned according to local expertise, doctors’ and patients’ preferences, and logistic preconditions. It is unrealistic that large randomized controlled trials will be available soon to better define the relative efficacy of different methods of salvage surgery in this setting. Case series may represent current best evidence to decide about the appropriateness of both avascular and vascularized bone grafting.
In the present study the mean overall Enneking index reached about 80% of the maximum value, with no significant differences between iliac crest or fibular grafts, different etiologies, anatomical locations, or other exposure variables. It is noteworthy that only one of 44 patients (2%) later underwent amputation.
9
In this series, transplant fractures occurred in 27% of all cases, which suits the rates reported in the scientific literature. Although these events prolonged bony healing and treatment duration, they did not adversely affect clinical and radiological long-term outcomes. At the time of operation, angle-stable, interlocking plates were not available, and one might argue that transplant fixation with these devices would have reduced at least the incidence of transplant fractures.
In a field study of 220 patients with various limb salvaging surgical procedures, Enneking noted a mean index of 73% for the lower and 68% for the upper extremities.24 Kühner reported on twenty patients with large defects of the long bones (lower extremity: n=12, upper extremity: n=8) after tumor resection who underwent reconstruction by vascularized fibula grafts.21 After a median follow-up of five years, the mean Enneking index reached 72.6% (95% CI 64.5 – 80.7%), which compares well with the present findings. Cao noted similar results in 14 patients with tibial bone defects repaired by vascularized fibula grafts from the contralateral side (Enneking index 80.7%, 95% CI 60.0 – 100.0%).25 Another ten patients who had their bone graft harvested from the ipsilateral side showed lower average functional indices (68.3%, 95% CI 39.5 – 97.1%). Tu used the generic Short-Form 36 to assess health-related outcomes after reconstruction of post-traumatic tibial bone defects by vascularized fibular grafts.26 Of 48 patients with a minimum follow-up of five years, 44 achieved global scores of 75% and higher (91.7%, 95% CI 80.0 – 97.7%). It is difficult to interpret these findings, since the authors neither reported mean values, nor detailed the individual dimensions of the SF36 (that is, the social, psychological, and physiological dimension). 1
One must distinguish between immediate outputs (for example, limb salvage) from remote outcomes (that is, sustained limb function, absence of pain, and social rehabilitation). Complying with these definitions, vascularized bone grafting represents a useful therapeutic option.
There are, of course, established alternatives for treating extensive bone defects, for example, callus distraction via intramedullary devices or external fixators, synthetic bone void fillers, and, anecdotally, titanium cages.27 In addition, adjuvant treatments like pulsed ultrasound and bone morphogenetic proteins offer innovative ways for a multidisciplinary management of bone defects.
In case of joint involvement (especially after radical tumor resection), prosthetic replacement must be considered to preserve limb functionality, especially in older subjects after tumor resection of the lower extremity.28 In the present sample, the average age was below 30 years. In younger subjects, the potential functional advantages of prosthetic replacement over biological reconstruction must be traded off against the need for secondary exchange surgery.
Because of toxic effects of neoadjuvant and adjuvant radiochemotherapy, surgeons must be aware of the high risk for impaired healing.29 Cryopreserved allogenic bone is a common alternative to autologous material. It avoids donor site morbidity, but bears the risk of lacking incorporation and subsequent resorption.21 A hybrid technique using both vascularized and allogenic grafts may be a promising adjunct in this setting.
1
Callus distraction is often used for correction of congenital, posttraumatic, and other acquired limb-length discrepancies. However, this procedure, whether realized by intramedullary devices or external fixators, like the Ilizarov frame, takes time and demands a high degree of patient compliance. Although Ilizarov reported complications in only 5% of all cases30, other authors noted markedly higher rates.31-35
Several limits of our investigation merit further discussion. First, it is a retrospective study with all its known biases. Also, only 44 of 74 (60%) of all potentially eligible subjects could be identified and/ or were willing to participate, which compares well with other studies of this type. In the observational setting, large efforts must be spent to achieve sufficient follow-up rates. We deliberately used mail, telephone, and, if necessary, registration offices to identify all patients of the source population, but could not achieve complete logs because of the long interval between index surgery and follow-up examinations. Also, we cannot exclude that patients with unsatisfactory results refrained from answering our requests. In a worst-case scenario, one might even speculate about a higher amputation rate.
Another limit is the methodological weakness of the outcome tool. In contrast to other instruments like the Disability of the Arm, Shoulder and Hand (DASH) score, or the Lower Extremity Musculofunctional (LEMF) instrument, the Enneking score has not yet been validated in terms of responsiveness and retest reliability. However, it is recommended by the Muskoloskeletal Tumor Society (MSTS), and was used by many other authors who reported functional outcomes after surgical reconstruction of large bone defects in benign and malignant conditions. 1
In conclusion, free vascularized bone grafts represent a useful, biological treatment choice for surgical repair of large bone defects. Patients and their relatives can be counseled about a good chance for long-lasting stability and acceptable function. However, because of
the delicate operative technique, and distinct logistic
preconditions, it should be performed by skilled surgeons at specialized institutions.
1
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27
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1
Variable Mean age, years (SD) Gender male female Etiology tumor osteosarcoma chondrosarcoma giant cell tumor fibrous dysplasia aneurysmatic cyst other osteomyelitis congenital tibial pseudarthrosis Localization humerus forearm* femur tibia Affected segment proximal diaphyseal Distal Side Left Right Mean defect length, cm (SD) Mean no. of previous operations (SD) Occupation blue-collar worker white-collar employee Scholar/student housewife Other
Table 1.
29.2 (15.4) 26 (59.1%) 18 (40.9%) 27 (61.4%) 6 6 6 2 2 5 12 (27.3%) 5 (11.4%) 7 (15.9%) 7 (15.9%) 17 (38.6%) 13 (29.5%) 18 (40.9%) 5 (11.4%) 21 (47.7%) 27 (61.4%) 17 (38.6%) 12.9 (4.4) 3.0 (3.0) 13 (29.5%) 11 (25.0%) 9 (20.5%) 5 (11.4%) 6 (13.6%)
Demographic profile *includes two radial and five ulnar defects
Variable Mean transplant size, cm (SD) total upper extremity (n=14) lower extremity (n=30) Fixation Plates Screws combination additional avascular bone augmentation None spongiosa fibula* Juvara plasty† joint fusion Total upper extremity lower extremity arterial anastomosis Termino - terminal Termino - lateral venous anastomosis Termino - terminal Termino - lateral manufactured orthosis
Table 2.
15.8 (5.2) 16.7 (4.8) 15.4 (5.4) 31 (70.5%) 8 (18.2%) 5 (11.4%) 11 (25.0%) 22 (50.0%) 6 (13.6%) 5 (11.4%) 16 (36.4%) 7 9 31 (70.5%) 13 (29.5%) 43 (97.7%) 1 (2.3%) 34 (77.3%)
Surgical details *includes two combined augmentations with autologous spongiosa †includes three combined augmentations with autologous spongiosa
Variable
n
time until weight bearing, months Total upper extremity lower extremity complication rate transplant fractures Implant loosening or breakage non-unions nerval lesions deep infections amputation Revision surgery Implant removal duration of orthotic stabilization, months Total upper extremity lower extremity length difference, cm upper extremity lower extremity manufactured shoes Limping
Table 3.
Outcome data.
mean (95% CI)
13.0 (10.4 – 15.5) 11.4 (6.2 – 16.6) 13.7 (10.6 – 16.8) 12 6 5 3 2 1 13 6
27.3% (15.0 – 42.8%) 13.6% (5.2 – 27.4%) 11.4% (3.8 – 24.6%) 6.8% (1.4 – 18.7%) 4.5% (0.6 – 15.5%) 2.3% (0.1 – 12.0%) 29.5% (16.8 – 45.2%) 13.6% (5.2 – 27.4%) 17.6 (10.6 – 24.6) 9.8 (4.8 – 14.9) 22.4 (11.6 – 33.2)
12 16
1.9 (0.9 – 2.8) 1.2 (0.7 – 1.7) 41.4% (23.5 – 61.1%) 55.2% (35.7 – 73.6%)
Total Dimension acceptance Pain function positioning dexterity Lifting
Table 4A.
Tumor n=9 mean (95% CI)
Osteomyelitis n=5 mean (95% CI)
23.8 (21.6 – 26.0)
23.2 (20.2 – 26.2)
24.8 (20.2 – 29.4)
4.4 (4.0 – 4.9) 4.4 (3.8 – 4.9) 3.1 (2.4 – 3.9) 3.3 (2.8 – 3.8) 4.8 (4.5 – 5.0) 3.8 (3.3 – 4.2)
4.4 (3.9 – 5.0) 4.2 (3.4 – 5.1) 3.0 (2.1 – 3.9) 3.2 (2.5 – 4.0) 3.4 (2.3 – 4.5) 3.6 (3.0 – 4.1)
4.4 (3.3 – 5.5) 4.6 (3.5 – 5.7) 3.4 (1.5 – 5.3) 3.4 (2.3 – 4.5) 4.8 (4.2 – 5.4) 4.2 (3.2 – 5.2)
Functional outcomes according to Enneking, upper extremity.
Total Dimension acceptance Pain function Walking Support Ability Gait
Table 4B.
Any etiology n=14 mean (95% CI)
Any etiology (n=30) mean (95% CI)
Tumor (n=18) mean (95% CI)
Osteomyelitis (n=7) mean (95% CI)
Pseudarthrosis (n=5) mean (95% CI)
23.6 (21.7 – 25.4)
24.1 (22.0 – 26.2)
20.4 (13.7 – 27.2)
26.0 (24.5 – 27.5)
4.3 (3.9 – 4.7) 4.1 (3.7 – 4.5) 3.2 (2.6 – 3.8)
4.6 (4.2 – 4.9) 3.9 (3.4 – 4.4) 3.3 (2.6 – 4.0)
4.1 (2.4 – 5.9) 3.9 (2.9 – 4.8) 2.7 (0.8 – 4.6)
3.8 (2.8 – 4.8) 5.0* 3.6 (2.5 – 4.7)
4.6 (4.2 – 5.0) 4.0 (3.7 – 4.4) 3.4 (3.0 – 3.8)
4.9 (4.7 – 5.0) 3.9 (3.5 – 4.4) 3.6 (3.0 – 4.1)
3.4 (1.8 – 5.1) 3.6 (2.5 – 4.6) 2.7 (1.8 – 3.6)
5.0* 5.0* 3.6 (2.9 – 4.3)
Functional outcomes according to Enneking, upper extremity.
*All subjects rated these dimensions with 5 points. No confidence intervals were computed for ceiling effects.
Legends to Figures Figure 1
Study profile.
Figure 2
Functional outcomes by type of graft.
Figure 3
Functional outcomes by etiology.
Figure 4
Functional outcomes by anatomic location.
Figure 5
Functional outcomes by defect and transplant size.
Patients with long bone defects 77 Tumor prosthesis 3 received free vascularized bone graft 74 Lost to follow-up 7 Deceased 3 2 tumor-related deaths (1 Ewing sarcoma, 1 osteosarcoma) 1 unknown
Identified and contacted 64
Refused participation 20
Enrolled 44
Figure 1 - Bauwens et al.
30 25 20 15 10 5
Enneking Total Score
Iliac crest
Mann-Whitney test p=0.23
Fibula
Figure 2 - Bauwens et al.
30 25 20 15 10 5
Enneking Total Score
Tumor
Osteomyelitis
Congenital pseudarthrosis
Kruskal-Wallis test p=0.48
Figure 3 - Bauwens et al.
30 25 20 15 10 5
Enneking Total Score
Humerus
Forearm
Femur
Lower leg
Kruskal-Wallis test p=0.39
Figure 4 - Bauwens et al.
30 25 20
Enneking Total Score
15 10 5 5
10
15 20 Size (cm)
25
30
Transplant
beta -0.06 (95% CI -0.33 – 0.22)
Defect
beta -0.11 (95% CI -0.44 – 0.21)
Figure 5 - Bauwens et al.
