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Limb salvage in lower-extremity sarcomas and technical details about vascular reconstruction
J Orthop Sci (2000) 5:555–560
Limb salvage in lower-extremity sarcomas and technical details about vascular reconstruction Stefano Bonardelli1, Franco Nodari1, Roberto Maffeis1, Vincenzo Ippolito2, Mauro Saccalani2, Luca Lussardi1, and Stefano Maria Giulini1 1 2
Department of Surgery, University of Brescia, Brescia, Italy Center for Orthopedic Oncology, Civil General Hospital P.le Spedali Civili 1, 25100 Brescia, Italy
Abstract Vascular surgery may allow limb salvage when a sarcoma of the lower limb involves the main vascular bundle. We present our experience and describe the techniques which have been employed for such surgery. From October 1995 to April 1999, vascular surgery procedures were employed in seven patients with sarcomas of the thigh: two complete subadventitia dissections of the main vascular trunks, four artery replacements (two polytetrafluoroethylene [PTFE] grafts and two autologous saphenous grafts), and five venous reconstructions (all with autogenous saphenous graft: three substitutions; two distal transpositions with one external rigid support at the anastomosis). Clinical and instrumental (sonogram, computed tomography [CT] scan, echodoppler) follow-up was carried out at 3, 6, and then every 12 months after surgery (mean, 25 months; range, 6–53 months). Operative mortality and morbidity were nil. All the grafts were patent (one arterial thrombosis was successfully treated on the first postoperative day). The functional result was good in six patients and fair in one. Two patients died, 24 and 13 months after surgery, with disseminated disease, but had no local recurrence. Five patients are alive and disease-free. Vascular techniques allow limb salvage with en-bloc resection of sarcomas of the thigh involving the main vessels. Venous reconstructions are indicated after removal of both the superficial and deep femoral veins. We suggest limiting the number of anastomoses (two transpositions in our series) and using external rigid support in those patients with a small saphenous vein graft (one patient in our series). Key words Sarcoma · Limb salvage · Venous reconstructions
rules originally established by Enneking.1 The femoral bundle may be completely surrounded by tumor tissue: in such instances, any attempt to free the vessels would result in an “intralesional” procedure, with a subsequent 90%–100% risk of local recurrence for a high-grade sarcoma. In most patients, however, the tumor growing in one of the neighboring muscles may get very close to the vessel walls; when the imaging shows a thin layer of normal tissue in the vessel-tumor interface,preoperative radiation therapy may help in clearing this tissue of tumor cells. A longitudinal split of the vessel adventitia, made along the side opposite to the tumor, may allow freeing-up of the vessel, leaving the adventitia on the tumor bed as a “compartmental barrier”, using adequate techniques of subadventitial vascular isolation. In those patients in whom the surgeon feels that this cannot be done without risking tumor contamination, it is much safer to resect the vessels (Fig. 1). We can say, therefore, that vascular resection is indicated whenever it would be impossible to achieve a “wide” margin without resecting the vessels. The aim is to avoid the amputation which was considered to be necessary in the past.5 In this article, we present our experience with vascular resection in patients with soft-tissue sarcomas of the thigh and discuss the main controversies regarding indications and surgical techniques, thus providing an addition to the limited number of studies published, each of which includes from 3 to 21 cases (see Tables 1, 2).
Introduction
Patients and methods
The therapy of sarcomas of the lower limbs requires a “wide” resection which must be performed following the
From 1995 to 1999, seven patients with soft-tissue sarcomas of the thigh and tumor involvement of the neurovascular bundle underwent limb-sparing procedures with curative intent (see Table 2). There were five men and two women, with a mean age of 56.7 years (range, 30–77 years). Five patients had been referred with previously untreated lesions, while two patients presented
Offprint requests to: S. Bonardelli, Via Aperta 21, 25075 Nave (Brescia), Italy Received: February 7, 2000 / Accepted: July 21, 2000
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S. Bonardelli et al.: Limb salvage in sarcoma
Fig. 1. Case 2. Magnetic resonance imaging shows extensive involvement of the anterior hip and the femoral vessels. Hip disarticulation or interileo-abdominal amputation would be the only alternative to the en-bloc resection of the proximal femur, quadriceps, and vascular bundle, which was performed Table 1. Literature review of vascular limb salvage for sarcoma of the lower limbs
Fortner 19773 Imparato 19786 Kawai 19969 Karakousis 19957 Koperna 199610 Hohenberger 19995 Personal experience
No. of patients
No. of arteries
% Patency
No. of veins
% Patency
3 13 8 21 5 20 7
3 13 8 21 1 19 4
100 92 62 100 100 100 100
3 3 7 16 6 11 5
100 100 14 100 83 82 100
with a local recurrence after a resection attempt performed elsewhere. Local and general staging included computed tomography (CT) or magnetic resonance imaging (MRI) of the affected limb, X-rays and CT of the chest, and sonogram or CT of the abdomen. Patients with vascular displacement were evaluated by angiography to clarify the vascular anatomy proximal and distal to the lesion. By TNM status, six patients were M0 and one was M1, with lung metastases at presentation that were treated with postoperative chemotherapy. Diagnosis was achieved by trochar biopsy, and histology (always confirmed after resection) showed highgrade malignant fibrous histiocytoma (MFH); G4 in six patients and low grade myxoid liposarcoma in one (see Table 2). All patients were candidates for limb salvage from the very beginning. Our patients with high-grade lesions were treated according to the Italian Sarcoma Group National Council for Research (ISG-CNR) protocol.4 This protocol mandates preoperative radiation therapy in large lesions “adjacent to unresectable critical structures”, when it is felt that irradiation may clear
a plane between the structure (vessels, in our patients) and the tumor, so that a resection with an adequately wide margin, according to Enneking’s criteria, can be carried out. Therefore, neoadjuvant radiotherapy was given in only one of our patients. The anatomical features of the tumor-host interface allowed us to preserve the superficial femoral artery and vein in two patients; this was achieved by the complete dissection of the vessels, splitting the adventitia layer longitudinally on the side opposite the tumor and, after opening it like a book, freeing-up the vessel. Every collateral branch along the whole length of the tumor was tapered and sectioned just at its origin from the main vessel. In the other five patients, artery and/or vein were resected enbloc with the tumor and then reconstructed using autologous or synthetic grafts. In total, four artery and five vein reconstructions were performed; in four patients, both artery and vein were replaced, and in one patient, only the vein. Reconstruction of the arterial axis was achieved by replacing the femoropopliteal artery with a polytetrafluoroethylene (PTFE) prosthesis in three patients and
Anterior thigh
Medial thigh
Posterior thigh
Medial thigh
Anterior thigh, lung, Mets
Medial thigh
2. 52, M
3. 30, F
4. 62, M
5 59, M
6. 52, M
7. 77, F
MFH — G4, First Local Recurrence
MFH — G4
MFH — G4
Myxoid Liposarcoma, second local recurrence
MFH — G4
MFH — G4
MFH — G4
Histological diagnosis and Grading (G)
Wide (adductor compartment)
Wide (quadriceps)
Wide (adductor compartment)
Wide (deep flexors)
Wide (adductor compartment)
Wide (quadriceps and proximal femur)
Wide (adductor compartment)
Margins of resection according to Enneking1
Artery, saphenous substitution Vein, saphenous substitution
Subadventitia dissection
Artery, PTFE substitution Vein, distal saphenous transposition on femoral vein
Artery, PTFE substitution Vein, saphenous substitution
Vein, distal saphenous transposition on femoral vein
Artery: saphenous substitution (successful rev. on first postop. day) Vein, saphenous substitution Bone, prosthesis graft
Subadventitia dissection
Vascular technique
Good
Good
Good
Good
Good
Fair
Good
Functional resulta (MSTS-ISOLS)
NED, 12 months
Dead with diffuse metastases, 13 months; no local recurrence
NED, 26 months
NED, 36 months
NED, 48 months
NED, 56 months
Dead at 25 months, systemic metastases, no local recurrence
Follow-up
MFH, Malignant fibrous hystiocytoma; NED, no evidence of disease; PTFE, polytetrafluoroethylene; MSTS-ISOLS, musckuloskeletal system-international symposium on limb salvage2; rev., revision a “Good” indicates Enneking’s score between 51% and 80%; “fair” indicates score between 40% and 50%2
Medial thigh
Region
1. 75, M
Age (year) and Sex (M/F)
Table 2. Personal experience
S. Bonardelli et al.: Limb salvage in sarcoma 557
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Fig. 2. Case 3. One ring from a 7-mm sized external supported (EXS) polytetrafluoroethylene (PTFE) graft is implanted as a rigid external support on the caudal femoral vein stump, just above the knee; the implantation begins by fixation of the four cardinal points with 5–0 polypropylene stitches
Fig. 3. Case 3. External fixation of the ring to the femoral vein stump is completed with multiple stitches. The venous stump supported by the ring will be anastomized end-to-end to the saphenous vein. The ring, which will not be in contact with the blood flow, prevents the collapse and stenosis of the venovenous anastomosis, lowering the risk of thrombosis. The reconstruction is patent 4 years after operation
with a contralateral autologous saphenous vein in the fourth patient. Above the knee, we use a saphenous vein graft (of course, when it is available and with fair diameter and length) only if the artery which must be anastomized is less than 6 mm in diameter (which is very rare at this level) and/or if the artery presents some degree of atherosclerosis. In three of the five patients in whom reconstruction of the venous axis was performed (in four patients it was associated with artery replacement) the femoral vein was replaced by the saphenous vein; in the remaining two patients, it was possible to make a distal anastomosis of the saphenous vein on the residual lower stump of the femoral vein (saphenofemoral transposition). In one of these two patients, the difference in diameter of the saphenous vein compared with that of the distal femoral vein necessitated the use of a rigid external support for the anastomosis (see description in the legends of Figs. 2 and 3). In one patient, the tumor also involved the proximal femur, which was resected and replaced by a modular total-hip prosthesis. The final histologic evaluation confirmed that a “wide” margin, according to Enneking’s criteria, had been achieved in all patients. All patients were discharged with long-term anticoagulant therapy (carried out with dicumarolic drugs). Five patients received postoperative adjuvant therapy; one had radiotherapy, two had radio-plus chemotherapy, and two had chemotherapy alone. During follow-up, local and systemic search for relapse was done with sonograms and/or MRI of the thigh, X-ray and CT of the chest, and abdominal sonograms, every 3 months for the first 3 years, and then every 6 months. Echo color Doppler of the operated
vascular regions was carried out 3 and 6 months after surgery and then every 12 months. Clinical evaluation was performed, using the system of Enneking et al.2 for scoring pain, function, emotional acceptance, supports, walking ability, and gait.
Results We experienced no perioperative mortality. One patient had acute peripheral ischemia on the first postoperative day, because of thrombosis in the autologous saphenous vein which had been used as an arterial replacement; this was successfully corrected by a proximal re-anastomosis and thromboembolectomy performed under local anesthesia. Some months later, this patient, in whom the proximal femur had also been resected and who had received postoperative irradiation, developed an infection around the femoral prosthesis; this was treated conservatively and it still persists (with a chronic fistula but minimal discomfort), 56 months after surgery. Functional results, evaluated according to the criteria of Enneking et al.2 were classified as good (score, 51% to 80%) in six patients and fair (score, 40% to 50%) in one patient (see Table 2). One patient, who underwent a plain subadventitial dissection of the vascular axis, died 2 years after surgery, with systemic disease, in the absence of local recurrence. The patient with lung metastases at presentation died 13 months after surgery with disseminated disease without local recurrence. The other five patients are alive and disease-free after an average follow-up of 33 months (range, 12–56 months).
S. Bonardelli et al.: Limb salvage in sarcoma
Discussion Until 20 years ago, amputation was the only reasonable treatment for sarcomas of the lower limbs, while, nowadays, limb salvage is the therapy of choice.5 It has been proven that resecting the tumor with an adequate cuff of healthy tissue around it can provide local cure.1 Furthermore, in about 5% of patients,8 the main arterial and/or venous vessels of the limb have to be removed en-bloc with the tumor; this raises the problem of limb preservation vs amputation. Therefore, vascular resection is considered necessary when: (1) the tumor is all around the vessel; in such an instance, any attempt to reach the vessel would result in an intralesional procedure; (2) the vessels run in close proximity to the tumor, and no plane between tumor and vessels is visible on the imaging; (3) the vessels run in close proximity to the tumor, but a plane of tissue is visible (on the preoperative imaging) between the tumor and the vessel; this represents an indication for preoperative radiation therapy in an attempt to clear that plane and try a vascular-sparing procedure, but when it is felt that this attempt may result in an inadequate margin, it is mandatory to proceed directly with the vascular resection. Fortner et al.,3 in 1977, were the first to describe the en-bloc removal of the tumoral mass with the main vascular axis, combined with arterial and venous reconstruction (with distal artero-venous fistula); this was done in three patients, and in four other patients they performed resection of the neoplastic lesion with isolation and subadventitial dissection of the vascular bundle. Imparato et al.,6 in 1978, performed arterial reconstruction with the saphenous vein in 13 patients and venous reconstruction in 3, after resecting the tumors involving the vascular bundle. After these reports, other authors published sporadic reports of good results with conservative surgery.5,8,9,12 In particular, in 1992, Williard et al.16 demonstrated the same long-term survival in two groups of patients, the first of which underwent amputation and the second, including patients with neurovascular invasion, underwent limb-sparing compartmental resections. In the same way, Karakousis et al.7 in 1995 showed a 28% disease-free survival at 5 years in amputated patients compared with 52% in patients treated by limb-salvage, with 0% local recurrences in the amputation group and 9% in the limb-sparing group. These data do not differ from others reported in the literature and do not show any significant differences between the two groups. At the beginning of 1999, Hohenberger et al.5 showed that the local recurrence rate and the survival rate after 5 years, in patients presenting with vessel involvement and treated with en-bloc resection of the tumor mass and the vascular axis, were the same as those in patients without
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vascular involvement (and, of course, no vascular resection). The only current indication for amputation seems to be the multiple neoplastic infiltration of the major neurovascular bundles, and the involvement of the so-called “three kings” (vessel, nerve, bone). In fact, whereas the sacrifice of the sciatic nerve alone can be tolerated and compensated, in those cases where the simultaneous resection of main muscle groups, bone and neurovascular bundle would be needed, limb sparing surgery would lead to the so-called “insensate foreleg” described by authors in the English-language literature, with such a severe functional impairment that amputation followed by a suitable prosthesis would be a much better choice.5 In the same way, a very careful evaluation must be made between the advantages of preserving the limb and the use of a prosthesis following amputation in those patients in whom the resection of an adjacent joint is needed; generally, however, both hip and knee joint can be resected and replaced (in our patient 2 we resected the proximal femur).15 Limb preservation with vascular reconstruction is evidently to be avoided in patients with previous neuromuscular deficit or chronic obliterating arteriopathy.9 The increased surgical risk, which is determined by the surgical trauma and by the length of the procedure (which is greater than that for an amputation) must not be overlooked, however. The surgical technique must be perfect, and the functional result must always be checked; possible failure of the vascular reconstruction, requiring reintervention, will increase the risk of infection, favored by the large cavities remaining after resection, and may even threaten the patient’s life. Thus, the surgical strategy must be modulated carefully, considering both the patient’s general features (age and, above all, associated diseases, such as diabetes, cardiopathies, heart or kidney insufficiency) and the features of the tumor lesion. Obtaining precise preoperative staging of the lesion seems to be fundamental: sonograms, CT, MRI, and arteriography are to be considered complementary and necessary for the precise definition of the local extent of the disease and of the possible involvement of a major vascular bundle.14 Proof of direct infiltration of the vascular axis is difficult to obtain, even by angiography (which is useful, however, to evaluate the regions proximal and distal to the mass) and by MRI. The feasibility of a wide resection is determining, in order to plan whether or not to remove the vascular bundle. As to the choice of prosthetic materials in the reconstruction of arteries, the site of the distal anastomosis is determining: above the knee, both autologous and synthetic prostheses may be used, whereas below the knee, it is better to use autologous material, such as the ipsi- or contralateral saphenous vein or, rarely, the cephalic or contralateral superficial femoral vein.5,9
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Venous reconstruction is not always necessary. Resection of the superficial femoral vein alone, preserving the deep femoral vein, is generally well tolerated, with no subsequent edema.5,9,11 The same toleration is frequently observed in other clinical situations, when the superficial femoral vein is harvested to be used as an autologous graft.13 Excision of the external iliac vein alone is also well tolerated. So, we feel that the absolute indication for planning a substitution of the venous axis or a by-pass is the enbloc removal of both the superficial and deep femoral veins. In these patients, the opportunity to make a distal artero-venous fistula, as suggested by some authors, to increase the speed of blood flow and thus reduce the risk of thrombosis in the reconstructed venous axis,9 has been challenged by many; it would only determine venous hypertension and relative arterial insufficiency of the circle distal to the fistula, without achieving a significant reduction in postsurgical peripheral edema.5 The results reported in the literature seem to be generally good as far as arterial reconstruction is concerned, where patency varies from 62% to 100% at 3–5 years, but they do not seem to be so satisfying for venous substitutions, which have very high failure rates (see Table 1).5,9 In our experience, the results achieved with both arterial and venous reconstructions are very good, and induce us to confirm their feasibility; these techniques, therefore, can be considered as an important aid in limb-sparing surgery (see Table 2). However, we feel that some technical details must be emphasized. In particular, we think that it is important to limit the number of venous anastomoses, using, whenever possible, the distal transposition of the saphenous vein (as in two of our patients). Another good option is to adopt an external support which will keep the end of the autologous graft as wide open as possible (Figs. 2 and 3; in one of our patients, reconstruction was patent 4 years after surgery) when its diameter does not exactly match that of the residual vein. The latter technique seems to be essential for limiting the lymphatic stasis that occurs frequently, but this will regress completely if the venous graft maintains its patency.5,7,9
S. Bonardelli et al.: Limb salvage in sarcoma
References 1. Enneking WF. Musculoskeletal tumor surgery. New York: Churchill Livingstone; 1983. 2. Enneking WF, Dunham W, Gebhardt MC, et al. A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the muskuloskeletal system. Clin Orthop 1993;286:241–6. 3. Fortner JG, Kim DK, Shiu MH. Limb-preserving vascular surgery for malignant tumors of the extremities. Arch Surg 1977;112:391– 4. 4. Frustaci S, Gherlinzoni F, De Paoli A, et al. Preliminary results of an adjuvant randomized trial on high risk extremity soft tissue sarcomas (STS) (abstract 1785). The interim analysis. Proc Am Soc Clin Oncol 1997;16:496. 5. Hohenberger P, Allenberg J, Schlag PM, et al. Results of surgery and multimodal therapy for patients with soft tissue sarcoma invading to vascular structures. Cancer 1999;85:396–408. 6. Imparato A, Roses DF, Francis KC, et al. Major vascular reconstruction for limb salvage in patients with soft tissue and skeletal sarcoma of the extremities. Surg Gynecol Obstet 1978;147:891– 6. 7. Karakousis CP, Proimakis C, Walsh DL. Primary soft tissue sarcoma of extremities in adults. Br J Surg 1995;82:1208– 12. 8. Karakousis CP, Karmpaliotis C, Driscoll DL. Major vessel resection during limb-preserving surgery for soft tissue sarcoma. World J Surg 1996;20:345–50. 9. Kawai A, Hashizume HV, Inoue H, et al. Vascular reconstruction in limb salvage operation for soft tissue tumors of the extremities. Clin Orthop 1996;332:215–22. 10. Koperna T, Teleky S, Vogl S, et al. Vascular reconstruction for limb salvage in sarcoma of the lower extremity. Arch Surg 1996;131:1103–7. 11. Meyer J, Walsh J, Schuler J, et al. The early fate of venous repair after civilia vascular trauma. Ann Surg 1987;206:458–64. 12. Nambisan RN, Karakousis CP. Vascular reconstruction for limb salvage in soft tissue sarcoma. Surgery 1987;101:668–77. 13. Nevelsteen A, Lacroix H, Suy R. Autogenous venous reconstruction in the treatment of aortobifemoral prosthetic infection. J Cardiovasc Surg 1988;29:315–7. 14. Panicek D, Go SD, Healey JH, et al. Soft-tissue sarcoma involving bone or neurovascular structures: MR imaging prognostic factors. Radiology 1997;205:871–5. 15. Quill G, Gitelis S, Morton T, et al. Complications associated with limb salvage for extremity sarcoma and their management. Clin Orthop 1990;260:242–50. 16. Williard W, Hajdu S, Casper ES, et al. Comparison of amputation with limb-sparing operations for adult soft tissue sarcoma of the extremity. Ann Surg 1992;215:269–75.
Limb salvage in lower-extremity sarcomas and technical details about vascular reconstruction Stefano Bonardelli1, Franco Nodari1, Roberto Maffeis1, Vincenzo Ippolito2, Mauro Saccalani2, Luca Lussardi1, and Stefano Maria Giulini1 1 2
Department of Surgery, University of Brescia, Brescia, Italy Center for Orthopedic Oncology, Civil General Hospital P.le Spedali Civili 1, 25100 Brescia, Italy
Abstract Vascular surgery may allow limb salvage when a sarcoma of the lower limb involves the main vascular bundle. We present our experience and describe the techniques which have been employed for such surgery. From October 1995 to April 1999, vascular surgery procedures were employed in seven patients with sarcomas of the thigh: two complete subadventitia dissections of the main vascular trunks, four artery replacements (two polytetrafluoroethylene [PTFE] grafts and two autologous saphenous grafts), and five venous reconstructions (all with autogenous saphenous graft: three substitutions; two distal transpositions with one external rigid support at the anastomosis). Clinical and instrumental (sonogram, computed tomography [CT] scan, echodoppler) follow-up was carried out at 3, 6, and then every 12 months after surgery (mean, 25 months; range, 6–53 months). Operative mortality and morbidity were nil. All the grafts were patent (one arterial thrombosis was successfully treated on the first postoperative day). The functional result was good in six patients and fair in one. Two patients died, 24 and 13 months after surgery, with disseminated disease, but had no local recurrence. Five patients are alive and disease-free. Vascular techniques allow limb salvage with en-bloc resection of sarcomas of the thigh involving the main vessels. Venous reconstructions are indicated after removal of both the superficial and deep femoral veins. We suggest limiting the number of anastomoses (two transpositions in our series) and using external rigid support in those patients with a small saphenous vein graft (one patient in our series). Key words Sarcoma · Limb salvage · Venous reconstructions
rules originally established by Enneking.1 The femoral bundle may be completely surrounded by tumor tissue: in such instances, any attempt to free the vessels would result in an “intralesional” procedure, with a subsequent 90%–100% risk of local recurrence for a high-grade sarcoma. In most patients, however, the tumor growing in one of the neighboring muscles may get very close to the vessel walls; when the imaging shows a thin layer of normal tissue in the vessel-tumor interface,preoperative radiation therapy may help in clearing this tissue of tumor cells. A longitudinal split of the vessel adventitia, made along the side opposite to the tumor, may allow freeing-up of the vessel, leaving the adventitia on the tumor bed as a “compartmental barrier”, using adequate techniques of subadventitial vascular isolation. In those patients in whom the surgeon feels that this cannot be done without risking tumor contamination, it is much safer to resect the vessels (Fig. 1). We can say, therefore, that vascular resection is indicated whenever it would be impossible to achieve a “wide” margin without resecting the vessels. The aim is to avoid the amputation which was considered to be necessary in the past.5 In this article, we present our experience with vascular resection in patients with soft-tissue sarcomas of the thigh and discuss the main controversies regarding indications and surgical techniques, thus providing an addition to the limited number of studies published, each of which includes from 3 to 21 cases (see Tables 1, 2).
Introduction
Patients and methods
The therapy of sarcomas of the lower limbs requires a “wide” resection which must be performed following the
From 1995 to 1999, seven patients with soft-tissue sarcomas of the thigh and tumor involvement of the neurovascular bundle underwent limb-sparing procedures with curative intent (see Table 2). There were five men and two women, with a mean age of 56.7 years (range, 30–77 years). Five patients had been referred with previously untreated lesions, while two patients presented
Offprint requests to: S. Bonardelli, Via Aperta 21, 25075 Nave (Brescia), Italy Received: February 7, 2000 / Accepted: July 21, 2000
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S. Bonardelli et al.: Limb salvage in sarcoma
Fig. 1. Case 2. Magnetic resonance imaging shows extensive involvement of the anterior hip and the femoral vessels. Hip disarticulation or interileo-abdominal amputation would be the only alternative to the en-bloc resection of the proximal femur, quadriceps, and vascular bundle, which was performed Table 1. Literature review of vascular limb salvage for sarcoma of the lower limbs
Fortner 19773 Imparato 19786 Kawai 19969 Karakousis 19957 Koperna 199610 Hohenberger 19995 Personal experience
No. of patients
No. of arteries
% Patency
No. of veins
% Patency
3 13 8 21 5 20 7
3 13 8 21 1 19 4
100 92 62 100 100 100 100
3 3 7 16 6 11 5
100 100 14 100 83 82 100
with a local recurrence after a resection attempt performed elsewhere. Local and general staging included computed tomography (CT) or magnetic resonance imaging (MRI) of the affected limb, X-rays and CT of the chest, and sonogram or CT of the abdomen. Patients with vascular displacement were evaluated by angiography to clarify the vascular anatomy proximal and distal to the lesion. By TNM status, six patients were M0 and one was M1, with lung metastases at presentation that were treated with postoperative chemotherapy. Diagnosis was achieved by trochar biopsy, and histology (always confirmed after resection) showed highgrade malignant fibrous histiocytoma (MFH); G4 in six patients and low grade myxoid liposarcoma in one (see Table 2). All patients were candidates for limb salvage from the very beginning. Our patients with high-grade lesions were treated according to the Italian Sarcoma Group National Council for Research (ISG-CNR) protocol.4 This protocol mandates preoperative radiation therapy in large lesions “adjacent to unresectable critical structures”, when it is felt that irradiation may clear
a plane between the structure (vessels, in our patients) and the tumor, so that a resection with an adequately wide margin, according to Enneking’s criteria, can be carried out. Therefore, neoadjuvant radiotherapy was given in only one of our patients. The anatomical features of the tumor-host interface allowed us to preserve the superficial femoral artery and vein in two patients; this was achieved by the complete dissection of the vessels, splitting the adventitia layer longitudinally on the side opposite the tumor and, after opening it like a book, freeing-up the vessel. Every collateral branch along the whole length of the tumor was tapered and sectioned just at its origin from the main vessel. In the other five patients, artery and/or vein were resected enbloc with the tumor and then reconstructed using autologous or synthetic grafts. In total, four artery and five vein reconstructions were performed; in four patients, both artery and vein were replaced, and in one patient, only the vein. Reconstruction of the arterial axis was achieved by replacing the femoropopliteal artery with a polytetrafluoroethylene (PTFE) prosthesis in three patients and
Anterior thigh
Medial thigh
Posterior thigh
Medial thigh
Anterior thigh, lung, Mets
Medial thigh
2. 52, M
3. 30, F
4. 62, M
5 59, M
6. 52, M
7. 77, F
MFH — G4, First Local Recurrence
MFH — G4
MFH — G4
Myxoid Liposarcoma, second local recurrence
MFH — G4
MFH — G4
MFH — G4
Histological diagnosis and Grading (G)
Wide (adductor compartment)
Wide (quadriceps)
Wide (adductor compartment)
Wide (deep flexors)
Wide (adductor compartment)
Wide (quadriceps and proximal femur)
Wide (adductor compartment)
Margins of resection according to Enneking1
Artery, saphenous substitution Vein, saphenous substitution
Subadventitia dissection
Artery, PTFE substitution Vein, distal saphenous transposition on femoral vein
Artery, PTFE substitution Vein, saphenous substitution
Vein, distal saphenous transposition on femoral vein
Artery: saphenous substitution (successful rev. on first postop. day) Vein, saphenous substitution Bone, prosthesis graft
Subadventitia dissection
Vascular technique
Good
Good
Good
Good
Good
Fair
Good
Functional resulta (MSTS-ISOLS)
NED, 12 months
Dead with diffuse metastases, 13 months; no local recurrence
NED, 26 months
NED, 36 months
NED, 48 months
NED, 56 months
Dead at 25 months, systemic metastases, no local recurrence
Follow-up
MFH, Malignant fibrous hystiocytoma; NED, no evidence of disease; PTFE, polytetrafluoroethylene; MSTS-ISOLS, musckuloskeletal system-international symposium on limb salvage2; rev., revision a “Good” indicates Enneking’s score between 51% and 80%; “fair” indicates score between 40% and 50%2
Medial thigh
Region
1. 75, M
Age (year) and Sex (M/F)
Table 2. Personal experience
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Fig. 2. Case 3. One ring from a 7-mm sized external supported (EXS) polytetrafluoroethylene (PTFE) graft is implanted as a rigid external support on the caudal femoral vein stump, just above the knee; the implantation begins by fixation of the four cardinal points with 5–0 polypropylene stitches
Fig. 3. Case 3. External fixation of the ring to the femoral vein stump is completed with multiple stitches. The venous stump supported by the ring will be anastomized end-to-end to the saphenous vein. The ring, which will not be in contact with the blood flow, prevents the collapse and stenosis of the venovenous anastomosis, lowering the risk of thrombosis. The reconstruction is patent 4 years after operation
with a contralateral autologous saphenous vein in the fourth patient. Above the knee, we use a saphenous vein graft (of course, when it is available and with fair diameter and length) only if the artery which must be anastomized is less than 6 mm in diameter (which is very rare at this level) and/or if the artery presents some degree of atherosclerosis. In three of the five patients in whom reconstruction of the venous axis was performed (in four patients it was associated with artery replacement) the femoral vein was replaced by the saphenous vein; in the remaining two patients, it was possible to make a distal anastomosis of the saphenous vein on the residual lower stump of the femoral vein (saphenofemoral transposition). In one of these two patients, the difference in diameter of the saphenous vein compared with that of the distal femoral vein necessitated the use of a rigid external support for the anastomosis (see description in the legends of Figs. 2 and 3). In one patient, the tumor also involved the proximal femur, which was resected and replaced by a modular total-hip prosthesis. The final histologic evaluation confirmed that a “wide” margin, according to Enneking’s criteria, had been achieved in all patients. All patients were discharged with long-term anticoagulant therapy (carried out with dicumarolic drugs). Five patients received postoperative adjuvant therapy; one had radiotherapy, two had radio-plus chemotherapy, and two had chemotherapy alone. During follow-up, local and systemic search for relapse was done with sonograms and/or MRI of the thigh, X-ray and CT of the chest, and abdominal sonograms, every 3 months for the first 3 years, and then every 6 months. Echo color Doppler of the operated
vascular regions was carried out 3 and 6 months after surgery and then every 12 months. Clinical evaluation was performed, using the system of Enneking et al.2 for scoring pain, function, emotional acceptance, supports, walking ability, and gait.
Results We experienced no perioperative mortality. One patient had acute peripheral ischemia on the first postoperative day, because of thrombosis in the autologous saphenous vein which had been used as an arterial replacement; this was successfully corrected by a proximal re-anastomosis and thromboembolectomy performed under local anesthesia. Some months later, this patient, in whom the proximal femur had also been resected and who had received postoperative irradiation, developed an infection around the femoral prosthesis; this was treated conservatively and it still persists (with a chronic fistula but minimal discomfort), 56 months after surgery. Functional results, evaluated according to the criteria of Enneking et al.2 were classified as good (score, 51% to 80%) in six patients and fair (score, 40% to 50%) in one patient (see Table 2). One patient, who underwent a plain subadventitial dissection of the vascular axis, died 2 years after surgery, with systemic disease, in the absence of local recurrence. The patient with lung metastases at presentation died 13 months after surgery with disseminated disease without local recurrence. The other five patients are alive and disease-free after an average follow-up of 33 months (range, 12–56 months).
S. Bonardelli et al.: Limb salvage in sarcoma
Discussion Until 20 years ago, amputation was the only reasonable treatment for sarcomas of the lower limbs, while, nowadays, limb salvage is the therapy of choice.5 It has been proven that resecting the tumor with an adequate cuff of healthy tissue around it can provide local cure.1 Furthermore, in about 5% of patients,8 the main arterial and/or venous vessels of the limb have to be removed en-bloc with the tumor; this raises the problem of limb preservation vs amputation. Therefore, vascular resection is considered necessary when: (1) the tumor is all around the vessel; in such an instance, any attempt to reach the vessel would result in an intralesional procedure; (2) the vessels run in close proximity to the tumor, and no plane between tumor and vessels is visible on the imaging; (3) the vessels run in close proximity to the tumor, but a plane of tissue is visible (on the preoperative imaging) between the tumor and the vessel; this represents an indication for preoperative radiation therapy in an attempt to clear that plane and try a vascular-sparing procedure, but when it is felt that this attempt may result in an inadequate margin, it is mandatory to proceed directly with the vascular resection. Fortner et al.,3 in 1977, were the first to describe the en-bloc removal of the tumoral mass with the main vascular axis, combined with arterial and venous reconstruction (with distal artero-venous fistula); this was done in three patients, and in four other patients they performed resection of the neoplastic lesion with isolation and subadventitial dissection of the vascular bundle. Imparato et al.,6 in 1978, performed arterial reconstruction with the saphenous vein in 13 patients and venous reconstruction in 3, after resecting the tumors involving the vascular bundle. After these reports, other authors published sporadic reports of good results with conservative surgery.5,8,9,12 In particular, in 1992, Williard et al.16 demonstrated the same long-term survival in two groups of patients, the first of which underwent amputation and the second, including patients with neurovascular invasion, underwent limb-sparing compartmental resections. In the same way, Karakousis et al.7 in 1995 showed a 28% disease-free survival at 5 years in amputated patients compared with 52% in patients treated by limb-salvage, with 0% local recurrences in the amputation group and 9% in the limb-sparing group. These data do not differ from others reported in the literature and do not show any significant differences between the two groups. At the beginning of 1999, Hohenberger et al.5 showed that the local recurrence rate and the survival rate after 5 years, in patients presenting with vessel involvement and treated with en-bloc resection of the tumor mass and the vascular axis, were the same as those in patients without
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vascular involvement (and, of course, no vascular resection). The only current indication for amputation seems to be the multiple neoplastic infiltration of the major neurovascular bundles, and the involvement of the so-called “three kings” (vessel, nerve, bone). In fact, whereas the sacrifice of the sciatic nerve alone can be tolerated and compensated, in those cases where the simultaneous resection of main muscle groups, bone and neurovascular bundle would be needed, limb sparing surgery would lead to the so-called “insensate foreleg” described by authors in the English-language literature, with such a severe functional impairment that amputation followed by a suitable prosthesis would be a much better choice.5 In the same way, a very careful evaluation must be made between the advantages of preserving the limb and the use of a prosthesis following amputation in those patients in whom the resection of an adjacent joint is needed; generally, however, both hip and knee joint can be resected and replaced (in our patient 2 we resected the proximal femur).15 Limb preservation with vascular reconstruction is evidently to be avoided in patients with previous neuromuscular deficit or chronic obliterating arteriopathy.9 The increased surgical risk, which is determined by the surgical trauma and by the length of the procedure (which is greater than that for an amputation) must not be overlooked, however. The surgical technique must be perfect, and the functional result must always be checked; possible failure of the vascular reconstruction, requiring reintervention, will increase the risk of infection, favored by the large cavities remaining after resection, and may even threaten the patient’s life. Thus, the surgical strategy must be modulated carefully, considering both the patient’s general features (age and, above all, associated diseases, such as diabetes, cardiopathies, heart or kidney insufficiency) and the features of the tumor lesion. Obtaining precise preoperative staging of the lesion seems to be fundamental: sonograms, CT, MRI, and arteriography are to be considered complementary and necessary for the precise definition of the local extent of the disease and of the possible involvement of a major vascular bundle.14 Proof of direct infiltration of the vascular axis is difficult to obtain, even by angiography (which is useful, however, to evaluate the regions proximal and distal to the mass) and by MRI. The feasibility of a wide resection is determining, in order to plan whether or not to remove the vascular bundle. As to the choice of prosthetic materials in the reconstruction of arteries, the site of the distal anastomosis is determining: above the knee, both autologous and synthetic prostheses may be used, whereas below the knee, it is better to use autologous material, such as the ipsi- or contralateral saphenous vein or, rarely, the cephalic or contralateral superficial femoral vein.5,9
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Venous reconstruction is not always necessary. Resection of the superficial femoral vein alone, preserving the deep femoral vein, is generally well tolerated, with no subsequent edema.5,9,11 The same toleration is frequently observed in other clinical situations, when the superficial femoral vein is harvested to be used as an autologous graft.13 Excision of the external iliac vein alone is also well tolerated. So, we feel that the absolute indication for planning a substitution of the venous axis or a by-pass is the enbloc removal of both the superficial and deep femoral veins. In these patients, the opportunity to make a distal artero-venous fistula, as suggested by some authors, to increase the speed of blood flow and thus reduce the risk of thrombosis in the reconstructed venous axis,9 has been challenged by many; it would only determine venous hypertension and relative arterial insufficiency of the circle distal to the fistula, without achieving a significant reduction in postsurgical peripheral edema.5 The results reported in the literature seem to be generally good as far as arterial reconstruction is concerned, where patency varies from 62% to 100% at 3–5 years, but they do not seem to be so satisfying for venous substitutions, which have very high failure rates (see Table 1).5,9 In our experience, the results achieved with both arterial and venous reconstructions are very good, and induce us to confirm their feasibility; these techniques, therefore, can be considered as an important aid in limb-sparing surgery (see Table 2). However, we feel that some technical details must be emphasized. In particular, we think that it is important to limit the number of venous anastomoses, using, whenever possible, the distal transposition of the saphenous vein (as in two of our patients). Another good option is to adopt an external support which will keep the end of the autologous graft as wide open as possible (Figs. 2 and 3; in one of our patients, reconstruction was patent 4 years after surgery) when its diameter does not exactly match that of the residual vein. The latter technique seems to be essential for limiting the lymphatic stasis that occurs frequently, but this will regress completely if the venous graft maintains its patency.5,7,9
S. Bonardelli et al.: Limb salvage in sarcoma
References 1. Enneking WF. Musculoskeletal tumor surgery. New York: Churchill Livingstone; 1983. 2. Enneking WF, Dunham W, Gebhardt MC, et al. A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the muskuloskeletal system. Clin Orthop 1993;286:241–6. 3. Fortner JG, Kim DK, Shiu MH. Limb-preserving vascular surgery for malignant tumors of the extremities. Arch Surg 1977;112:391– 4. 4. Frustaci S, Gherlinzoni F, De Paoli A, et al. Preliminary results of an adjuvant randomized trial on high risk extremity soft tissue sarcomas (STS) (abstract 1785). The interim analysis. Proc Am Soc Clin Oncol 1997;16:496. 5. Hohenberger P, Allenberg J, Schlag PM, et al. Results of surgery and multimodal therapy for patients with soft tissue sarcoma invading to vascular structures. Cancer 1999;85:396–408. 6. Imparato A, Roses DF, Francis KC, et al. Major vascular reconstruction for limb salvage in patients with soft tissue and skeletal sarcoma of the extremities. Surg Gynecol Obstet 1978;147:891– 6. 7. Karakousis CP, Proimakis C, Walsh DL. Primary soft tissue sarcoma of extremities in adults. Br J Surg 1995;82:1208– 12. 8. Karakousis CP, Karmpaliotis C, Driscoll DL. Major vessel resection during limb-preserving surgery for soft tissue sarcoma. World J Surg 1996;20:345–50. 9. Kawai A, Hashizume HV, Inoue H, et al. Vascular reconstruction in limb salvage operation for soft tissue tumors of the extremities. Clin Orthop 1996;332:215–22. 10. Koperna T, Teleky S, Vogl S, et al. Vascular reconstruction for limb salvage in sarcoma of the lower extremity. Arch Surg 1996;131:1103–7. 11. Meyer J, Walsh J, Schuler J, et al. The early fate of venous repair after civilia vascular trauma. Ann Surg 1987;206:458–64. 12. Nambisan RN, Karakousis CP. Vascular reconstruction for limb salvage in soft tissue sarcoma. Surgery 1987;101:668–77. 13. Nevelsteen A, Lacroix H, Suy R. Autogenous venous reconstruction in the treatment of aortobifemoral prosthetic infection. J Cardiovasc Surg 1988;29:315–7. 14. Panicek D, Go SD, Healey JH, et al. Soft-tissue sarcoma involving bone or neurovascular structures: MR imaging prognostic factors. Radiology 1997;205:871–5. 15. Quill G, Gitelis S, Morton T, et al. Complications associated with limb salvage for extremity sarcoma and their management. Clin Orthop 1990;260:242–50. 16. Williard W, Hajdu S, Casper ES, et al. Comparison of amputation with limb-sparing operations for adult soft tissue sarcoma of the extremity. Ann Surg 1992;215:269–75.