Vascular Reconstruction in Limbs Associated with Resection of Tumors

Vascular Reconstruction in Limbs Associated with Resection of Tumors Kenji Nishinari, MD,1 Nelson Wolosker, MD, PhD,1,2 Guilherme Yazbek, MD,1 Luiz Caetano Malavolta, MD,1 Antoˆnio Eduardo Zerati, MD,1 Valter Penna, MD, PhD,3 and Ademar Lopes, MD, PhD,3,4 Sa˜o Paulo, Brazil

Patients with tumors in limbs who undergo surgical treatment may present involvement of major vessels. The artery must be reconstructed for limb salvage and the vein may be reconstructed to avoid the onset of venous hypertension. The objective of this study was to analyze the results from surgical treatment of tumors associated with vascular reconstruction in limbs. A prospective follow-up was made of 17 patients with tumors involving major vessels in limbs who underwent vascular reconstruction. Arterial and venous reconstructions were performed in nine patients, arterial reconstruction was performed in six, and venous reconstruction in two patients. The vascular substitutes used were greater saphenous vein (19), expanded polytetrafluoroethylene prosthesis (5), and Dacron prosthesis (2). Vascular complications occurred in seven patients: one arterial graft rupture, three venous graft occlusions, and lymphedema in five patients. The following nonvascular complications occurred in 10 patients: pulmonary metastasis (7), local recurrence (2), neurological deficit (2), infection (2), partial necrosis of the flap (1), and enteric fistula (1). Six patients with pulmonary metastasis died. One patient underwent transfemoral amputation. Major vessel reconstruction in limbs associated with resection of neoplasms is a safe procedure. Venous revascularization should be performed using an autologous substitute.

INTRODUCTION Patients with tumors in limbs may present involvement of major vessels because of invasion of 1 Department of Vascular Surgery, Hospital do Caˆncer A.C. Camargo, Sa˜o Paulo, Brazil. 2 Director of the Department of Vascular Surgery, Hospital do Caˆncer A.C. Camargo, Sa˜o Paulo, Brazil. 3 Department of Pelvic Surgery, Hospital do Caˆncer A.C. Camargo, Sa˜o Paulo, Brazil. 4 Director of the Department of Pelvic Surgery, Hospital do Caˆncer A.C. Camargo, Sa˜o Paulo, Brazil. Correspondence to: Kenji Nishinari, MD, Rua Joaquim Antunes, 490, Conjunto 13, Pinheiros, Sa˜o Paulo/SP-Brazil CEP 05414-001. E-mail: [email protected]

Ann Vasc Surg 2003; 17: 411-416 DOI: 10.1007/s10016-003-0031-0 Ó Annals of Vascular Surgery Inc. Published online: 17 July 2003

the vascular wall by the adjacent tumor or confinement due to growth of the mass. There are few publications associating arterial and venous reconstructions in limbs with the resection of tumors, with the largest sample consisting of 21 patients.3,41 When the main artery is involved it must be reconstructed, because resection without revascularization usually leads to high rates of limb loss. Nevertheless, venous reconstruction does not follow any standardized methods, either in relation to its performance or regarding the vascular substitute. The objective of this study was to analyze the results from the surgical treatment of tumors associated with vascular reconstruction in limbs, taking into consideration the patency of the reconstruction, vascular and nonvascular complications, recurrence, and survival. 411

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PATIENTS AND METHODS Seventeen patients, operated on for malignant or benign aggressive tumors that had involved major arteries and/or veins in limbs, were followed up prospectively over the period from October 1997 to March 2002. The length of follow-up ranged from 4 to 54 months with an average of 21 months. Thirteen patients were women and four were men, with ages ranging from 9 to 91 years (an average of 39 years). With regard to prior treatments for tumor, six patients had not undergone any type of therapy. Isolated or comprehensive previous treatments included surgery, chemotherapy, and radiotherapy. Eleven patients had already undergone surgery, five had had chemotherapy, and five had received radiotherapy. The anatomical sites of the tumors were soft tissue in the thigh (7), inguinal region (4), fibula (2), femur (1), popliteal fossa (1), supraclavicular fossa (1), and neck (1). Upon clinical vascular examination, five patients presented with alterations: four had lymphedema at the impaired limb, and of those, two had concomitant femoral-popliteal obstruction. No arterial pulse was detectable in the patient with neoplasia in the supraclavicular fossa. With regard to complementary examinations, all patients underwent computerized tomography (CT) or nuclear magnetic resonance imaging (MRI); the tumoral mass was always shown to be lacking a cleavage plane or agglomerating the resected vessels. The two patients who presented femoral-popliteal obstruction underwent lower limb angioresonance, which demonstrated obstruction of the superficial femoral artery and refilling of the popliteal artery, in addition to absence of wall irregularities in the remaining arteries. Angiography on the patient with neoplasia in the supraclavicular fossa showed obstruction of the subclavian artery and refilling of the axillary artery. On the basis of operative findings showing evidence of agglomeration or adherence to the tumoral mass, the oncology surgeon chose en-bloc resection of the vessels involved by the tumor. The procedure was indicated in cases where vascular resection would be appropriate from an oncological point of view and there were no other areas of tumor that were not resectable or where the resectability would be in doubt. The clamping and sectioning of the vessels were performed as the last stage of en-bloc resection, after freeing all the tumor material, with the aim of reducing the duration of ischemia, and avoiding venous congestion of the limb. All patients were given intra-

Fig. 1. A Soft tissue sarcoma in the thigh involving the superficial femoral vessels. B Arterial and venous grafts with the saphenous vein.

venous heparin for performance of vascular graft surgery. Twenty-six reconstruction procedures were carried out in 17 patients. The following arterial and venous reconstructions were performed in nine patients: superficial femoral-popliteal (3) (Fig. 1), external iliac-superficial femoral (2), external iliaccommon femoral (1), common femoral-popliteal (1), popliteal-posterior tibial (1), and carotid-axillary with venous axillary–innominate (1). Arterial reconstruction was performed in six patients, including superficial femoral-popliteal (2), common iliac-superficial femoral (1), external iliac–common femoral (1), popliteal-posterior tibial (1), and subclavian patch (1) procedures. A venous reconstruction was performed in two patients: external iliac-common femoral (1) and superficial femoral– popliteal (1). The vascular substitutes used were greater saphenous vein (19), expanded polytetrafluoroethylene (PTFE) prosthesis (5), and Dacron prosthesis (2). The histological types encountered included osteosarcoma (2), synovial sarcoma (2), malignant melanoma (2), squamous cell carcinoma (2), fibrosarcoma (1), leiomyosarcoma (1), basal cell carci-

F F F F F F F M

F M M F F F F

F

M

1 2 3 4 5 6 7 8

9 10 11 12 13 14 15

16

17

66

23

16 24 23 15 39 65 59

9 27 51 39 49 29 91 65

Age (years)

Neck

TDigh

Thigh Fibula Inguinal Popliteal Thigh Thigh Inguinal Fossa supraclavicular; Fibula Femur TDigh TDigh TDigh Inguinal Inguinal

Site

Squamous cell carcinoma;

Synovial sarcoma

Osteosarcoma Osteosarcoma Fibrosarcoma Synovial sarcoma Hemangiopericytoma Malignant melanoma Malignant melanoma

Chondroma Giant cell tumor Adenocarcinoma Liposarcoma Leiomyosarcoma Fibrohistiocytoma Squamous cell carcinoma Basal cell carcinoma

Type

Subclavian A (+ com carotid)

Sup fem A + V

Com fem A Popliteal A External iliac A + fem A Popliteal A Sup fem A Sup fem V Com fem V Subclavian A + V (+ com carotid) Popliteal A + V Sup fem A + V Sup fem A + V Sup fem A + V Com fem A + V Com fem A + V Com fem A + V

Impaired vessels

SV (SV)

SV/SV

SV SV SV SV SV SV PTFE PTFE/PTFE (PTFE) SV/SV SV/SV SV/SV SV/SV SV/SV Dacron/Dacron PTFE/PTFE

Substitute

A, artery; com, common; fem, femoral; PTFE, prosthesis of expanded polytetrafluoroethylene; sup, superficial; SV, saphenous vein; V, vein.

Gender

Patient

Table I. Epidemiological characteristics, topography, histology type, impaired vessels, substitutes, and vascular complications

— — Lymphedema — Lymphedema Venous occlusion Venous occlusion + lymphedema; Arterial rupture + lymphedema; —

— — Lymphedema — — — — Venous occlusion

Complication

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noma (1), myxoid lyposarcoma (1), adenocarcinoma (1), giant cell tumor (1), chondroma (1), fibrohistiocytoma (1) and hemangiopericytoma (1). Patient demographics and vascular characteristics are reported in Table 1. Follow-up of patients was done on an outpatient basis. Clinical examination and duplex mapping were performed to study the patency of the grafts. Duplex mapping was done every 6 months during the first year and annually thereafter, or when there was clinical suspicion of graft occlusion.

RESULTS Six patients did not present any type of complication during follow-up. Vascular complications occurred in seven patients, with one rupture of the arterial graft, three occlusions of the venous graft, worsening of the previous lymphedema in four patients, and lymphedema in one. The case of rupture of the arterial graft occurred during the perioperative period, as a consequence of extensive infection and necrosis of the surgical wound. Ligature of the graft was performed in addition to debridement of the necrotic tissue. This patient presented with preoperative femoral-popliteal obstruction and recovery progressed with a stabilized lower limb and secondintention healing of the wound. The three patients with venous graft occlusion presented abrupt onset of edema in the affected limb and duplex mapping was done to confirm the diagnosis in these cases. The lower limb occlusions occurred 2 and 3 months after surgery, and the upper limb occlusion occurred 12 months afterwards. In these cases the substitute used was prosthetic. These patients were treated with systemic anticoagulation, in addition to elastic support for patients with impairment of the lower limb. Recovery in of all these patients progressed with moderate edema in the affected limb. Of the four patients who had worsening of the previous lymphedema, only one who already had substantial preoperative lymphedema did not seem to improve with conservative treatment of lymphatic drainage and elastic support. The patient who progressed with lymphedema also improved with conservative treatment. Nonvascular complications were detected in 10 patients, 4 of whom presented with more than one complication. These complications were pulmonary metastasis (7), local recurrence of the disease (2), neurological deficit (2), infection of the surgical

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wound (2), partial necrosis of the flap (1), and enteric fistula (1). Six patients with pulmonary metastasis died as a result of their disease, at an average time of 14 months after surgery. The only patient with pulmonary metastasis who is still alive underwent surgical resection of the pulmonary nodule and is currently receiving radiotherapy treatment. One patient exhibited local tumor recurrence 11 months after surgery and underwent transfemoral amputation performed by the oncology team. This patient remains without evidence of disease recurrence after 36 months of follow-up. Another patient presented with local recurrence after 14 months and died from pulmonary metastasis after 16 months.

DISCUSSION Until the 1970s, surgically treated patients with neoplasms in limbs who had impairment of the vascular bundle often underwent amputation. Progress in surgical procedures and the recently introduced multidisciplinary approach have allowed tumor resection to be performed with an adequate safety margin, thus salvaging the limb2-4 with good functional ability. Considering that the risk of severe ischemia with possible loss of the limb is quite high after arterial resection and ligature of the stumps, reconstruction of the artery is always indicated. In cases of neoplasms, in addition to the trunk vessels, a large part of the collateral circulation is resected for oncological purposes, corroborating the need for reconstruction.5-12 The arterial substitutes can be autologous3,9,10 or prosthetic,1,5,12 and no significant difference in patency rate is seen. Because of the greater incidence of infectious complications related to synthetic substitutes9 and the good caliber compatibility between the greater saphenous vein and vessels in the limbs, we prefer autologous substitution. We used the contralateral greater saphenous vein in 12 of the 15 arterial reconstructions performed. In one case (patient 8), we favored use of PTFE to perform an end-to-side anastomosis (carotid-subclavian) outside the operative field, thereby avoiding a second carotid clamping. In case 14, the patient had already undergone bilateral removal of the greater saphenous vein because of a previous varicose vein operation, and in case 15 the greater saphenous vein did not have a satisfactory caliber.

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In this sample, we had only one complication of arterial reconstruction: a rupture of the graft (saphenous vein) secondary to infection of the surgical wound, culminating in its ligature. This patient had preoperative femoral-popliteal obstruction with development of adequate collateral circulation, which was the probable reason for compensation of the limb and healing of the wound, even after ligature of the graft.6 Taking into consideration the resection of the collateral vessels and because this was an isolated case, we consider primary ligature of the vascular stumps to be risky, even in patients with previously compensated arterial obstruction. Reports in the literature show that venous reconstruction is not always performed, with the reasons stated being that the ligature does not interfere with the preservation of the limb2,3 and graft patency rates are not very satisfactory,5,6 even when a distal arterial-venous fistula is performed and oral anticoagulant is administered.2,6 Such reports also claim that control of edema in its acute period via limb elevation and elastic support3,5,6 is acceptable. Nonetheless, we believe that reconstruction of deep veins must always be performed because, over the long term, a patient undergoing ligature may present venous claudication, severe edema, hyperpigmentation, and eczema.10 In addition, such patients have another significant factor that generates edema: obstruction of the lymph vessels caused by surgical resection and sometimes worsened by radiotherapy. We prefer to use contralateral saphenous vein because of its greater biocompatibility, and we used it in 7 of the 11 reconstructions. In case 7, the patient had had saphenous vein removal for myocardial revascularization. In the segments where there was caliber discrepancy, end-to-side anastomoses were performed and good graft functioning was seen. In the absence of the greater saphenous vein, the femoral vein could be used,9 although we believe that its resection could generate complications in the limb. For this reason we decided to use a prosthetic substitute in these cases (patients 14 and 15). Occlusion of the venous graft occurred in 3 of the 11 reconstructions performed, although all the occlusions occurred after the perioperative period (an average of 5 months after surgery); therefore there was no increase of morbidity during the acute postoperative period. Occlusion was symptomatic in all cases and these patients were treated with systemic anticoagulation and elastic support: these patients experienced moderate edema in their limbs. In these cases, the substitute used was prosthetic. It is possible that postoperative antico-

Vascular reconstruction with resection of tumors 415

agulation would be a helpful adjunct for maintaining venous graft patency, particularly when a prosthetic substitute is used. The lymphedema observed in five patients, which had occurred previously in four of them, was caused by surgical resection in association with radiotherapy. Clinical treatment was satisfactory in all of these patients, with the exception of one case in which there was substantial preoperative lymphedema. The preservation of limb function was very good or excellent in most of our patients. In two cases, nerves were affected and their resection was necessary. In the first of these, resection of the fibular nerve was performed because of the recurrence of fibular sarcoma, causing a dropped foot. Despite this sequela, the limb was preserved and the patient considered this loss acceptable, since it allowed for a better quality of life than if there had been amputation. In the second case, resection of branches of the brachial plexus was required because of recurrence of basal cell carcinoma of the supraclavicular fossa, thereby causing a severe functional deficit in this limb. This deficit was foreseen before the surgery, and the alternative of primary amputation was discussed with the patient. This patient totally refused to undergo amputation and requested an attempt to salvage the limb, despite the expected deficit. In another case, the patient already had large-scale preoperative lymphedema, which became worse and resulted in considerable functional loss in this limb. The only amputation performed in this study was unrelated to vascular complications and was due to local recurrence of the disease. We believe that an indication for primary amputation of the limb must be based on the preservation of its function and not on the anatomical segment, provided that the tumor resection is complete. In this study, there were two cases of sarcomas below the knee, both in the fibula, with very satisfactory results. The rate of nonvascular complications was high and systemic evolution of the disease was the cause of death in all such cases.

CONCLUSIONS Arterial revascularization in limbs associated with resection of neoplasms is a safe procedure with a low rate of complications. Venous revascularization should be performed with an autologous substitute. Patients who undergo surgical treatment for neoplasms involving major vessels in limbs have a high rate of nonvascular complications.

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