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10.1245/ASO.2006.04.044
Annals of Surgical Oncology 13:721-727 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Functional Evaluation After Reconstruction With Myocutaneous and Fasciocutaneous Flaps for Conservative Oncological Surgery of the Extremities

Bernardo Rivas, MD1, José F. Carrillo, MD2 and Luis F. Oñate-Ocaña, MD3

1 Plastic Surgery Service, Surgery Division, Instituto Nacional de Cancerologia, San Fernando 22, México D.F. 14080, Mexico
2 Head and Neck Department, Surgery Division, Instituto Nacional de Cancerologia, San Fernando 22, México D.F. 14080, Mexico
3 Clinical Research Division, Instituto Nacional de Cancerologia, San Fernando 22, México D.F. 14080, Mexico

Correspondence: Address correspondence and reprint requests to: Bernardo Rivas, MD; E-mail: berba{at}prodigy.net.mx.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Limb-preservation surgery has evolved during the last two decades through application of pedicled and free flaps and has obtained oncological results similar to those with amputation for malignant neoplasms of the extremities. However, functional evaluation has not been performed comprehensively after these advanced reconstructive procedures. The aim of this study was to describe the oncological, surgical, and functional outcomes achieved in these patients.

Methods: Patients had malignant neoplasms of the extremities and/or shoulder and hip girdle, underwent resective surgery and reconstruction with limb-preservation purposes, and were treated from 1997 to 2002. Survival analysis was performed, and functional evaluation after resection was performed with the Enneking system 1 year after surgery.

Results: Thirty-two patients were included. The mean overall survival of the cohort was 5.6 years. Functional evaluation mean rating percentages for the upper and lower extremities were 86.5% and 75.2%. Functional outcomes were better for reconstruction with free flaps than with pedicled flaps in the lower extremities (rating percentages, 67% and 79.6%, respectively; P = .018).

Conclusions: Limb-preservation surgery is a safe treatment for malignant neoplasms. It can be performed with low morbidity and good oncological outcomes. Functional results in our series were good. Lower limb preservation has superior scores with free flap reconstructions because of their potential to cover extensive defects, and better results were obtained in walking, gait, and weight bearing.

Key Words: Surgical flaps • Limb salvage • Myocutaneous flap • Fasciocutaneous flap


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Surgical management of aggressive and extensive malignancies of the extremities entails amputations and wide tissue resection for cure.1 The need to achieve negative surgical margins has created major anatomical and functional defects that produce negative effects in aesthetics and the rehabilitation process. During the last two decades, this has been overcome by the development of new surgical techniques that have allowed preservation of extremities2 and that result in oncological results similar to those with the amputation procedures used in the past.

These new reconstructive techniques3,4 have allowed the design of segments of vascularized tissue that are transferred through myocutaneous and composite fasciocutaneous flaps, either pedicled or dependent on microvascular anastomosis, for coverage of extensive areas. These flaps provide a vascularized and stable coverage and specialized tissue to protect deep structures from the effects of the environment and radiotherapy, as well as to facilitate functional rehabilitation of the extremities.

Many patients with limb malignancies have already been subjected to surgical and radiotherapy treatments before reaching a referral facility for treatment of neoplasms, and in these cases, reconstruction of defects is of the utmost importance, especially regarding microvascular transfer.5 Despite advances in reconstruction of extremities, few studies exist that focus on functional results with an objective evaluation system.68 The aim of this study, therefore, was to examine surgical, oncological, and functional outcomes achieved in patients who had malignancies of the extremities treated with conservative surgery and who underwent advanced reconstructive procedures with pedicled or free transferred flaps.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
All consecutive patients treated from January 1997 to August 2003 at the Instituto Nacional de Cancerología in Mexico City who underwent resection of malignant neoplasms located in the extremities with a curative attempt were retrospectively studied. Inclusion criteria were (1) any age and sex; (2) histopathology studies from two independent pathologists confirming a diagnosis of primary malignant neoplasia of the limbs, shoulder, or the pelvic girdle; and (3) limb-preservation surgical procedures for treatment of malignancies which were performed either alone or in combination with chemotherapy and/or radiotherapy.

Location of a tumor in the extremities was defined in the upper extremity as any tumor whose epicenter was located distal to the level of the midpoint of the clavicle. In the lower limb, this was defined as lesions whose epicenter was distal to the midpoint of the inguinal ligament. A limb-preservation surgical procedure was defined as excision or resection of malignancies of the extremities, shoulder, or pelvic girdle without resection of bone, muscle, or neurovascular structures that would preclude function or anatomy of a limb as an independent organ.

Clinical charts were reviewed regarding clinical, histopathologic, and therapeutic data. The 2002 version of the American Joint Committee on Cancer tumor-node-metastasis staging system was used for clinical classification.9 Margins were classified according to a modification of the resection classification of the International Union Against Cancer as wide (>2-cm margin), close (tumor seen during surgery or a <2-cm margin), or positive.

The presence of recurrence and metastases, disease-free survival, and overall cancer-specific survival were also recorded. All recurrences were demonstrated by biopsy, computed tomographic scan, and magnetic resonance imaging for local or regional recurrences or by biopsy and/or computed tomographic scan and magnetic resonance imaging for distant metastasis.

Disease-specific survival times were calculated from the date of diagnosis to the date of the last recorded visit to the hospital. All cases lost to follow-up or deaths due to causes other than cancer were censored. Disease-free survival times were calculated from the date of operation to the date of recurrence. Cases lost to follow-up or with no recurrence were censored. All patients were contacted by telephone and interviewed for evaluation of functional status according to the Enneking outcome measurement scale.10

This system considers three parameters related to the patient as a whole—pain, functional activities, and emotional acceptance—and three specific parameters regarding the involved limb—positioning of the hand, manual dexterity, and lifting ability for the upper extremity and use of external support, walking ability, and gait for the lower extremity. These parameters are scored as 0, 1, 3, and 5 according to the level of achievement or performance, with 2 and 4 as intermediate values. The overall score obtained is divided by the maximum possible score, and the result is the rating percentage (a higher value means better function). Questionnaires were translated to Mexican style Spanish and validated in a group of 10 patients before they were used in this study.

Scores obtained by these methods were compared by using the Mann-Whitney U-test. Survival times were calculated with the Kaplan-Meier method, and differences were compared by using the log-rank method. Factors associated with survival in univariate analysis with a probability value of ≤ .2 were used for multivariate analysis. The Cox proportional hazards model was used for this purpose. The hazard ratio (HR) and 95% confidence intervals (CIs) were calculated as a measure of association. Two-tailed probabilities were considered in all cases, and a probability value of ≤ .05 was considered as significant. SPSS for Windows version 10.0 (SPSS Inc., Chicago, IL) was used for all computations.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Thirty-two patients met the inclusion criteria and were included in this study. Demographics and clinicopathologic characteristics are listed in Table 1Go. Seven patients had upper limb and 25 had lower limb malignancies.


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TABLE 1. Patient and tumor characteristics (32 patients)
 
Patients with bone sarcomas (16 cases) were staged as follows: 7 patients (43.75%) had stage IB disease, and 9 patients (56.25%) had stage IIB. Soft tissue sarcomas (10 cases) were classified as stage III in 8 cases (80%) and stage I (T2bN0M0G1) in 2 individuals (20%).

All melanomas corresponded to ulcerated, deeply invasive lesions, with no lymph node metastases in three cases. One case corresponded to a deeply invasive recurrent lesion without lymph node metastases. All squamous cell carcinomas were recurrent lesions with deep invasion to soft tissues. Specific locations of the tumors and types of flaps used for reconstruction are listed in Table 2Go. Indications for reconstruction are listed in Table 3Go.


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TABLE 2. Location of reconstruction with free or pedicled flaps
 

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TABLE 3. Indications for reconstruction
 
Reconstruction was performed immediately after resection. Sixteen patients (50%) had had a previous surgical procedure performed elsewhere. Previous radiotherapy had been administered to 22 patients (70%). Wide margins were obtained in 30 cases (90%); surgical margins were close to section border in 2 (6.5%), and surgical margins were positive in one (3.12%). Lower extremities margins were all wide. Figures 1a and 1bGo show resection of a fibrosarcoma of the left leg and ankle infiltrating the Achilles tendon, where reconstruction was performed with a latissimus dorsi free flap, and in Figure 1cGo, the aesthetic and functional results after 6 months are shown.


Figure 1
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FIG. 1. (a) Fibrosarcoma located on the distal third of the left leg and ankle, involving the Achilles tendon, muscles of the posterior tibial compartment, and skin. (b) Appearance of the region 7 weeks after reconstruction with a latissimus dorsi muscle flap, with good contour and aesthetics. (c) Remodeling of the flap was performed, and appearance and function are shown 6 months after the initial operation.

 
Twenty-seven (84.37%) soft tissue reconstructions were performed in 32 cases. Bone- including reconstruction was performed in five patients (15.6%).

Surgical Morbidity
Complications in pedicled flaps were minor in six cases. Two cases (14.28%) developed partial wound dehiscence that resolved spontaneously. A cutaneous fistula occurred in three cases (21.42%) in which the indication for the flap was coverage of a knee joint prosthesis. Two fistulas required surgical drainage and excision and performance of a local flap for closure of the fistula. Another case had partial necrosis of the flap which required surgical debridement and coverage with a skin graft.

Major complications of pedicled flaps were shown by one patient who had complete flap necrosis of a pedicled latissimus dorsi flap performed for cutaneous coverage of the proximal third of the arm. This was managed with local flap rotation. This patient had moderate loss of contour of the corresponding arm. Another patient had obstruction of femoral vessels after a vascular reconstruction with a Gore-Tex prosthesis (W. L. Gore & Associates, Flagstaff, AZ). This patient was treated with amputation on the eighth postoperative day.

Microvascular free flap reconstruction complications were present in one case of bone fracture of a fibula free flap for humerus reconstruction on the 12th postoperative day, which required internal fixation. Another case had flap epidermolysis on the 10th postoperative day, and in another case in which reconstruction was performed with a latissimus dorsi flap, deep venous thrombosis ensued which was treated with anticoagulation and local measures.

Survival
The mean disease-specific survival and disease-free survival of the cohort were 5.62 and 5.32 years, respectively. From our 32 patients, 5 had disease recurrences during the follow-up period: 2 in the upper extremity and 3 in the lower extremity. Of the patients with lower extremity recurrences, two were treated with amputation and were alive at the end of the study. The rest of the patients with recurrences received only medical palliation because of concurrent systemic disease.

Recurrences presented, at the earliest, after 18 months of follow-up. Accordingly, all patients were suitable for functional evaluation after 1 year of absence of recurrent disease. At the end of the study, 29 patients were alive without evidence of disease. Three were dead of recurrent disease.

Functional Results
Functional results obtained after reconstruction of the upper and lower extremities are listed in Table 4Go, according to the Enneking system.10 Scores for specific functions are presented as well, although in a condensed form, for comparison purposes. Table 5Go shows the functional results, according to pedicled or free flaps, for upper extremity reconstruction, and Table 6Go shows the functional scores obtained with pedicled or free flaps in the lower extremities.


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TABLE 4. Functional results according to upper and lower limb reconstruction
 

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TABLE 5. Functional results of upper limb reconstruction comparing pedicled with free flaps
 

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TABLE 6. Functional results of lower limb reconstruction comparing pedicled with free flaps
 
At present, four (57.14%) patients who had upper limb reconstruction have returned fully to work, and one (14.28%) performs part-time work. Of the patients with lower limb reconstruction, 10 (40%) returned to full-time work, 4 (16%) returned to part-time work, and the rest retired after the procedure.

Prognosis According to Reconstruction and Functional Results
The mean disease-free survivals for pedicled and free flaps were 5.43 and 4.83 years, respectively (P = .74). The mean disease-specific survivals for pedicled and free flaps were 5.32 and 5.42 years, respectively (P = .44). The mean disease-free survivals for patients with upper and lower limb reconstructions were 4.83 and 5.47 years, respectively (P = .36). The mean disease-specific survival times of patients with upper and lower limb reconstruction were 4.87 and 5.87 years, respectively (P = .09).

The Cox multivariate analysis of overall survival defined a higher overall Enneking score (HR, .91; 95% CI, .83–1.001) and the location of the neoplasia in the leg (HR, .031; 95% CI, .001–.84) as significant prognostic factors associated with better survival (final model, P = .023). The type of flap (pedicled or free) used did not affect survival even after adjustment for the location of the neoplasia and the overall Enneking score.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Traditionally, patients with sarcoma and malignancies of the limbs have been treated with extensive surgery. Surgical advances, however, have allowed preservation of extremities in many cases, with acceptable results in function and no compromise of oncological outcomes.11

Our study included a group of patients who had advanced tumors that required a multidisciplinary team approach; the reconstructive surgery group performed complex procedures with either pedicled or free flaps. A point to be addressed, however, is the heterogeneity of histopathologic diagnoses in our series. This drawback has been common to most studies related to limb-preservation surgery for malignancies.12,13 Also, conclusions should be considered with caution because of the small number of cases.

Indications and Surgical Results
Reconstruction of the extremities has been performed with several goals; one of them is to obtain wider surgical margins.14 In our group of patients, wide surgical margins were obtained in 90% of cases despite the size and stage of the lesions. This is at least partially explained because surgeons involved in the resection procedure tend to be more aggressive in limb-preservation surgery when advanced reconstructive procedures are feasible, and it emphasizes the importance of a multidisciplinary team approach.

Because the administration of preoperative chemotherapy or radiotherapy15 was frequent in our group of patients, the quality of the residual tissues also influenced the selection of a reconstructive procedure. Other goals—such as the need for vascularized bone, coverage of extensive surfaces, avoidance of tension, and protection of vascular and mechanical prostheses—are also important in these cases, and in our series, they were major indications for simultaneous reconstruction during the resective procedure.

Complications in our group of patients were infrequent, and this was reflected in the functional evaluation scores and final acceptance of procedures. Of note is that pedicled flaps tended to have complication rates similar to those obtained with free flaps, even when microvascular reconstructive procedures were used in combination with vascular and mechanical prostheses.

Prognostic Factors and Survival
The oncological results in our study were good, with disease-specific and disease-free mean survival times of 5.62 and 5.32 years, respectively. As mentioned previously, the fact that recurrences occurred after 18 months of follow-up indicates that preservation surgery of the limbs, either alone or combined with adjuvant treatment, gave long-term disease-free periods and survivals and did not compromise the final outcomes.

The Cox multivariate analyses revealed that a higher overall Enneking score and a location of tumor in the lower extremity were associated with better overall survival. The association of higher Enneking scores with improved survival is probably due to better planning of surgical procedures, with optimal oncologic resection and accomplishment of high quality reconstructions. Emotional impact could also be of importance, but at present this is only hypothetical and might be the aim of future studies. No definite conclusions can be drawn regarding the association of the location of tumors and prognosis because of the small numbers of patients who underwent upper extremity reconstructions and because the patient population was heterogeneous.

Functional Outcome
Several attempts have been made to evaluate objectively the quality of life in patients who undergo resection of malignancies—specifically with regard to sarcoma surgery.10 Although our series refers to six cases with diagnoses of epithelial malignancies, we applied this system to analyze the function of patients who had reconstructive surgery for limb preservation.

Regarding lower extremity reconstructions, pain and emotional impact scores were low. This is probably explained because lower limb tumors require a highly demanding and complicated reconstruction technique and because reconstructive procedures are tested against weight-bearing forces, with the disadvantage of the slower venous and lymphatic return characteristic of lower limbs.16,17 Moreover, minor reinnervation of tissues involved in reconstructed segments that involve the ankle and foot region generally occurs and is important for preservation and success of the flap and function, as has been mentioned in previous studies.18 Therefore, the reconstructive procedures in these areas need to be particularly meticulous to allow the return of sensitivity and, consequently, keep the gait and weight balance of the limb—facts that influence the emotional acceptance of these procedures.

The sample size for upper extremity reconstruction is small and prevents any conclusions regarding reconstructive method differences. However, reconstruction with free flaps in the lower extremities was superior to pedicled flap reconstruction in the overall score and emotional acceptance of the procedure, with statistical significance. This finding emphasizes the importance of free flaps in the complex and demanding process of lower limb reconstruction, as previously mentioned, and supports the tendency in our group for a more frequent use of free flaps in general in lower extremity surgery (probably because of the extensive defect that results in surgery of these areas) and in cases in which previous chemotherapy or radiotherapy has been administered. Free flaps also tend to be more convenient in the lower extremities because they compromise the rotation arches and gait dynamics less than pedicled flaps. Pedicled flaps, however, continue to have a role in reconstruction, especially in small to medium defects, in specific situations when rotation or movement of the limbs is away from the flap pedicle, in the absence of microvascular surgery facilities, or in older individuals and those with a high anesthesia or cardiovascular risk, as pointed out in other studies.19,20 A word of caution should be stated at this point because very often in the lower extremities, the only solution for a reconstructive problem is a free flap, thus introducing a selection bias in the comparison between pedicled and free flaps.

The results in our series tended to be poor for lower limb reconstruction in terms of the capacity to return to work. An explanation is that pain and the need of support had medium to low scores in lower extremities, and these were clearly points against aesthetics and final emotional acceptance of procedures; this influences the capacity and will of a patient to work.

The Enneking system has been reported as an objective measurement tool in previous studies,1,2 but to the best of our knowledge, the last modifications to this system have not been applied frequently to a moderately sized21,22 series of patients. In our study, a scoring system developed by Enneking was used to evaluate upper and lower limb reconstruction. This system addresses specific points related to an extremity, thus resulting in a more objective evaluation in terms of function. Although the specific parameters inherent to an upper or lower limb are noncomparable, the emotional acceptance, pain, functional capacities, and global scores are shown, and these give a clearer idea of the effect of these procedures on the individual. Final psychological and emotional acceptance of the procedure are influenced by the presence of a functional limb, and our results in terms of emotional acceptance and capacity to work reflect patient satisfaction.

Received for publication May 3, 2005. Accepted for publication November 10, 2005.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  8. Dahl B, Andersen AP, Andersen M, Andersen GR, Ebskov LV, Reumert T. Functional and social long term result after free tissue transfer to the lower extremity. Ann Plast Surg 1995; 34:372–5.[Medline]
  9. American Joint Committee on Cancer. Musculoskeletal sites. In: AJCC Cancer Staging Handbook. 6th ed. New York: Springer-Verlag, 2002: pp 211–28.
  10. Enneking WF, Dunham W, Gebhardt MC, Malawar M, Pritchard DJ. A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system. Clin Orthop Relat Res 1993; 286:241–6.
  11. Cordeiro PG, Neves RL, Hidalgo DA. The role of free tissue transfer following oncologic resection in the lower extremity. Ann Plast Surg 1994; 33:9–16.[Medline]
  12. Willcox TM, Smith AA. Upper limb free flap reconstruction after tumor resection. Semin Surg Oncol 2000; 19:246–54.[Medline]
  13. Heller L, Levin LS. Lower extremity microsurgical reconstruction. Plast Reconstr Surg 2001; 108:1029–41.[CrossRef][Medline]
  14. Lohman RF, Nabawi AS, Reece GP, Pollock RE, Evans GRD. Soft tissue sarcoma of the upper extremity. Cancer 2002; 94:2256–64.[CrossRef][Medline]
  15. Cheng EY, Dusenberg KE, Winters MR, Thompson RC. Soft tissue sarcomas: preoperative vs postoperative radiotherapy. J Surg Oncol 1996; 61:90–9.[CrossRef][Medline]
  16. Langstein HN, Chang DW, Miller MJ, et al. Limb salvage for soft-tissue malignancies of the foot: an evaluation of free-tissue transfer. Plast Reconstr Surg 2002; 109:152–9.[Medline]
  17. Talbert ML, Zagars GK, Sherman NE, Romsdhal MM. Conservative surgery and radiation therapy for soft tissue sarcoma of the wrist, hand, ankle and foot. Cancer 1990; 66:2482–91.[CrossRef][Medline]
  18. Bell RS, O’Sullivan B, Davis A, et al. Functional outcome in patients treated with surgery and irradiation for soft tissue tumors. J Surg Oncol 1991; 48:224–31.[Medline]
  19. Serletti JM, Higgins JP, Moran S, Orlando GS. Factors affecting outcome of free tissue transfer in the elderly. Plast Reconstr Surg 2000; 106:66–70.[Medline]
  20. Suh JD, Sercurz JA, Abemayor E, et al. Analysis of outcome and complications in 400 cases of microvascular head and neck reconstruction. Arch Otolaryngol Head Neck Surg 2004; 130:962–6.[Abstract/Free Full Text]
  21. Kim JY, Subramanian BS, Yousef A, Rogers BA, Robb GL, Chang DW. Upper extremity limb salvage with microvascular reconstruction in patients with advanced sarcoma. Plast Reconstr Surg 2004; 114:400–8.[Medline]
  22. Pederson WC. Upper extremity microsurgery. Plast Reconstr Surg 2001; 107:1524–37.[Medline]




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