limb-sparing resection versus amputation in 27 patientslibrary.tasmc.org.il/ · limb-sparing...

Large Tumors of the AxillaLimb-sparing Resection Versus Amputation in 27 Patients

Eran Maman, MD*; Martin M. Malawer, MD†; Yehuda Kollender, MD*; Isaac Meller, MD*;and Jacob Bickels, MD*

Tumors of the axilla are rare and pose a surgical challengebecause they are usually large at presentation and in closeproximity to the major neurovascular bundle of the upperextremity. The use of detailed preoperative evaluation stud-ies and extensile surgical exposure for these tumors enabledus to determine tumor resectability and proceed with a saferesection or perform an amputation when required. We ret-rospectively reviewed 27 patients who underwent resectionof an axillary tumor from 1989 to 2004 and analyzed theirpresenting symptoms, results of preoperative studies, type ofsurgery, and functional outcome. Tumors were exposed us-ing a utilitarian shoulder approach that revealed no tumorinvasion of the neurovascular bundle in 19 patients and in-vasion in eight. The former group was treated with tumorresection and the latter with forequarter amputation. Neu-rologic deficit, limb edema, and angiographic observation ofarterial narrowing were associated with amputation. Goodfunction was achieved in 15 of 19, shoulder range of motionwas preserved in 14 of 19, and local tumor control was main-tained in 16 of 19 patients who underwent a limb-sparingresection.

Level of Evidence: Level IV, therapeutic study. See theGuidelines for Authors for a complete description of levels ofevidence.

The axilla is a relatively small space through which themajor neurovascular bundle (NVB) to the upper extremityand a rich network of lymph nodes and channels pass.Tumors at this site are rare and usually reach a consider-able size before clinical detection probably because of theelasticity of the tissues confining the walls of the axilla andtheir deep location.8 Axillary tumors usually wrap around,push, and occasionally invade the NVB. Tumor extensioninto the chest wall also has been documented.6,7 As aresult, a segment of the brachial artery or an adjacentcomponent of the chest wall may require removal with thetumor to achieve free margins of resection.6,7 Gross inva-sion of the NVB necessitates forequarter amputation toachieve local tumor control.9

The unique anatomic considerations pose a challengebecause of the proximity of the tumors to the NVB and thepotential damage to the function and viability of the upperextremity. Resection with the traditional approach throughthe base of the axilla is difficult because the tumor cannotbe fully seen and the NVB cannot be identified and mo-bilized before resection. Chest wall resections and vascu-lar reconstructions cannot be performed through such lim-ited space.

The decision of whether to resect an axillary tumor ismade only after surgical verification the NVB has not beeninvaded by the tumor and the spared limb will be func-tional. We therefore sought specific signs or symptoms atpresentation, and results of preoperative imaging andnerve conduction studies, that would enable preoperativeevaluation of NVB tumor extension and thus predict thefeasibility of performing a limb-sparing resection of anaxillary tumor. We also questioned whether an extensilesurgical approach to the axilla would allow wide exposureof the NVB and safe tumor resection in cases where suchresection was feasible.

MATERIALS AND METHODS

We retrospectively reviewed 27 patients who underwent preop-erative evaluation and surgery for large (average diameter, 7.5

Received: August 7, 2006Revised: February 5, 2007; March 14, 2007Accepted: March 23, 2007From *The National Unit of Orthopedic Oncology, Tel-Aviv Sourasky Medi-cal Center, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv,Israel; and the †Department of Orthopedic Oncology, Washington Cancer In-stitute, Washington Hospital Center, Georgetown University, Washington, DC.Each author certifies that he or she has no commercial associations (eg,consultancies, stock ownership, equity interest, patent/licensing arrange-ments, etc) that might pose a conflict of interest in connection with thesubmitted article.Each author certifies that his or her institution either has waived or does notrequire approval for the human protocol for this investigation and that allinvestigations were conducted in conformity with ethical principles of re-search.Correspondence to: Jacob Bickels, MD, National Unit of Orthopedic Oncol-ogy, Tel-Aviv Sourasky Medical Center, 6 Weizmann Street, Tel-Aviv,64239 Israel. Phone: +972-3-6874688; Fax: +972-3-6974690; E-mail:[email protected]: 10.1097/BLO.0b013e318061f1e7

CLINICAL ORTHOPAEDICS AND RELATED RESEARCHNumber 000, pp. 000–000© 2007 Lippincott Williams & Wilkins

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Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

cm; range, 5–12 cm) soft tissue tumors of the axilla from 1989to 2004 (Fig 1). There were 17 women and 10 men. The medianage was 54 years (range, 28–81 years). The axillary mass wasasymptomatic and detected incidentally in 14 patients. It wasassociated with local discomfort in eight patients, and five pa-tients reported paresthesias along the distribution of a specificnerve (two radial, two ulnar, one medial). Patients were followedfor a minimum of 2 years (mean, 5.3 years; range, 2.5–11 years).

Preoperative assessment included evaluation of arterialpulses, presence of upper extremity edema, and neurologic statusof the ipsilateral upper extremity. Imaging studies included plainradiography, computed tomography (CT) and/or MRI, and an-giography of the entire ipsilateral shoulder girdle. Plain radiog-raphy and CT were used to rule out invasion by the tumor of theproximal humerus, scapula, and chest wall. We used MRI toevaluate tumor extent and its relation to the adjacent NVB andthe surrounding cuff of muscles. We used angiography to assessthe relation of the axillary and brachial vessels to the tumor, thepattern of possible vascular displacement, the presence of vas-cular anomalies, and vascular patency. All patients had electro-myography of the upper ipsilateral extremity. Histopathologicdiagnoses were made using a CT-guided core needle biopsy in22 patients and an open technique in five. The diagnoses in-cluded 15 primary and 12 metastatic tumors (Table 1). Three ofthe six patients who had metastatic tumors of the axilla hadadditional lung metastases; all six patients were expected to sur-vive for at least 6 months postoperatively.

Clinical preoperative evaluation of the study patients showedintact arterial pulses in all patients, diffuse swelling of the upperextremity in six, and neurologic deficit in six (two patients, onenerve; one patient, two nerves; three patients, three nerves)(Table 2). Imaging studies showed arterial displacement in 10patients and chest wall invasion in two. Electromyography

showed neuropathologic changes in six patients with neurologicdeficits and in an additional four patients in whom neurologicdeficits were not clinically evident. Angiograms were performedin 21 patients. Arterial displacement, narrowing, or both weredocumented in 15 patients. None of the arteriograms showedevidence of frank vascular invasion.

Of the eight patients with high-grade sarcoma of the axilla,five were treated with pre- and postoperative chemotherapy, onewas treated with postoperative chemotherapy only, and the re-maining two patients with neither. All eight of these patientsreceived postoperative radiotherapy using 6500 Gy externalbeam radiation.

All tumors were exposed using the utilitarian shoulder ap-proach. We used a deltopectoral incision (utilitarian shoulderapproach) that started at the junction of the outer and middlethirds of the clavicle, continued along the deltopectoral groove,and terminated over the anterior axillary fold (the inferior borderof the pectoralis major muscle) (Fig 2). We opened the superfi-cial fascia, ligated the cephalic vein, and raised the medial andlateral fasciocutaneous flaps. Exposure of the axillary cavity wasachieved after detaching and reflecting two muscle layers. Onewas a superficial layer that included the pectoralis major muscleand the other was a deep layer that included the coracoid attach-ment of the pectoralis minor and the conjoined tendon (ie, thecoracobrachialis muscle and the short head of the bicepsmuscle). The pectoralis major was detached from its insertion tothe proximal humerus leaving at least 1 cm of the tendon forreattachment (Fig 3). The coracoid process then was observedand the muscle attachments were divided and detached at theirinsertion. The conjoined tendon was reflected caudally, takingcare to prevent traction injury to the musculocutaneous nerve,which penetrates the substance of the coracobrachialis muscle,after which the pectoralis minor muscle was reflected medially(Fig 4A–C). All edges of the reflected muscles were tagged witha suture for later identification for use in reconstruction. Theanatomic relation of the tumor to the NVB then was determined

Fig 1. An MR image shows a large high-grade malignant fi-brous histiocytoma of the right axilla.

TABLE 1. Histopathologic Diagnoses of the 27Study Patients

Histopathologic DiagnosesNumber

of Patients

Benign lesions Atypical lipoma 4Benign-aggressive

lesionsFibromatosis 3

Soft tissue sarcomas Malignant fibroushistiocytoma

3

Synovial cell sarcoma 2Radiation-induced

angiosarcoma1

High-grade spindlecell sarcoma

2

Malignant melanoma 6Metastatic carcinomas Adenocarcinoma of

the breast3

Squamous cell carcinoma 3Total 27

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for deciding on tumor resectability (Fig 4D). We preferred towidely resect malignant and benign-aggressive tumors with atleast a few millimeters of normal tissue beyond the tumor pseu-docapsule. Atypical lipomas were removed with their envelopingcapsule without an additional cuff of normal tissue. We believetumor extension to the brachial plexus precludes limb-sparingtumor resection and mandates forequarter amputation. When wecannot find a plane of dissection between the brachial artery andthe tumor, we recommend resection en bloc with the tumor andreconstruction with a graft.

Exposure revealed a safe plane of dissection between thetumor and NVB in 19 patients who underwent tumor resection.En bloc resection of a chest wall segment was performed in twopatients with evidence of chest wall invasion. In another patient,the brachial artery was encased in the axillary tumor mass withno evident plane of dissection. We subsequently performed enbloc resection of the artery with the tumor mass and reconstruc-tion with a medial saphenous vein graft. The remaining eightpatients had gross invasion of the NVB by the tumor and un-derwent forequarter amputation. None of the patients diagnosedwith a benign tumor required amputation to achieve local tumorcontrol.

After tumor removal, the pectoralis minor and conjoined ten-dons were reattached to the coracoid process with a nonabsorb-able suture, the latissimus dorsi was rotated into the defect, andthe pectoralis major was reattached to its stump on the proximalhumerus in the same manner (Fig 5). The wound was meticu-lously closed over suction drains and the upper extremity waskept in an arm sling. Continuous suction was required for 3 to 5days. Perioperative intravenous antibiotics were continued untilthe drainage tubes were removed. We then introduced postop-

erative mobilization emphasizing gradual shoulder range of mo-tion (ROM). Patients diagnosed with soft tissue sarcomas andmetastatic carcinomas were treated postoperatively with radio-therapy consisting of external beam radiation of 6500 Gy and3000 Gy, respectively.

Fig 2. An illustration shows the deltopectoral incision, whichstarted at the junction of the inner and middle thirds of theclavicle, continued along the deltopectoral groove, and termi-nated over the anterior axillary fold.

Fig 3A–B. (A) An illustration shows reflection of the superficialmuscle layer; the pectoralis major muscle was detached fromits insertion to proximal humerus, leaving at least 1 cm of thetendon for reattachment. (B) An intraoperative photographshows detachment of the pectoralis major.



For the first 2 postoperative years, the patients were evaluatedat 3-month intervals and underwent a physical examination,plain radiography, and chest CT at each visit. They then wereevaluated semiannually for an additional 3 years and annuallythereafter. An orthopaedic oncologist (EM, JB) analyzed the

clinical records and operative reports. We recorded histopatho-logic diagnoses, results of staging studies, type of surgery, com-plications, rates of local tumor recurrence and patients’ survival,ROM of the ipsilateral shoulder, and functional outcomes. Func-tional evaluations were performed according to the American

Fig 4A–D. (A) An illustration shows reflection of the deep muscle layer; the conjoined tendon was reflected caudally and thepectoralis minor muscle was reflected medially. (B) Intraoperative photographs show reflection of the conjoined tendon (C) thepectoralis minor. (D) The NVB was dissected and mobilized. The plane of dissection between the tumor and NVB allowedexecution of a limb-sparing resection; otherwise, a forequarter amputation would have been required to achieve local tumorcontrol.



Musculoskeletal Tumor Society System, which assigns numericvalues for each of six categories: pain, function, emotional ac-ceptance, hand positioning, dexterity, and lifting ability.3 Finalassessment was based on each patient’s most recent followupand expressed as the proportion of full normal function in all sixcategories.

We used Fisher’s exact test to evaluate the relation of neu-rologic deficit, diffuse swelling, angiographic findings of arterialnarrowing, and the execution of a limb-sparing resection. Sig-nificance was set at the p < 0.05 level.

RESULTS

Of the 20 study patients with malignant axillary tumors, 17(85%) survived more than 1 year postoperatively, 13(65%) survived more than 2 years, and 11 (55%) survivedmore than 3 years.

Findings of preoperative clinical evaluation and imag-ing studies were associated with the intraoperative findingof NVB tumor invasion and the necessity of performing aforequarter amputation. Specifically, clinical evidence of aneurologic deficit(s) (p < 0.015), diffuse swelling of theipsilateral extremity (p � 0.02), and angiographic findingsof arterial narrowing (p � 0.023) were associated with theexecution of an amputation.

The use of the utilitarian shoulder approach allowedwide exposure of all major blood vessels and nerves of theaxilla in all study patients, thereby providing the informa-tion required for decision making regarding the need for

amputation. Exploration of the NVB in the eight patientswho had amputation revealed complete encasement by thetumor of the brachial plexus cords in six patients andsparing of the lateral cord in two.

Complications among the 19 patients who had tumorresection included three (16%) superficial wound infec-tions. None of these patients had a deep wound infection,numbness, paresthesias, or neuralgia. Two (25%) of theeight patients who underwent forequarter amputation hada superficial necrosis of a myocutaneous flap that requiredrepeated bedside débridements of the necrotic tissue andhealing by secondary intent.

Local tumor recurrence occurred in three patients(11%) in the resection group. These recurrences occurred9, 17, and 23 months postoperatively. Two (fibromatosis,malignant fibrous histiocytoma) were managed with widereexcision of the tumor and adjuvant radiation therapy andthe third (synovial sarcoma) required amputation.

The ROM and functional parameters were satisfactoryin 14 and 15 patients who underwent tumor resection,respectively. All but three patients had full ROM aroundthe ipsilateral shoulder. These three patients had limitedabduction of the shoulder (90º, 70º, and 45º) because ofconsiderable stiffness of the axilla attributed to the sequel-ae of postoperative radiation therapy. Functional param-eters were preserved in the range of 81% to 98% of normalfunction of the upper extremity (Fig 6). Three patients whounderwent limb-sparing resection and adjuvant radiationtherapy had chronic edema of the upper extremity developthat required treatment with lymph drainage and elasticstockings.

DISCUSSION

Resecting large tumors of the axilla poses a surgical chal-lenge because of their close proximity to the NVB of theupper extremity. These tumors rarely invade the overlyingcuff of muscles. Therefore, the pectoralis minor, coraco-brachialis, and pectoralis major usually can be spared andused for reconstruction and preservation of function.When dealing with malignant tumors of the axilla, it isimpossible to achieve a safe wide margin of resection asone would be able to do when dealing with the same tumoraround the thigh because of the immediate proximity ofthe NVB at that site. Forequarter amputation, however,occasionally is required to achieve local tumor controlbecause of tumor extension into the NVB. Our study con-sists of a large variety of tumor types and biologic behav-ior patterns, some of which rarely require amputation fortheir local control. These tumors were grouped togetherbecause the concept of their preoperative evaluation andsurgical exposure are identical.

Our study was designed to evaluate the adequacy ofpreoperative evaluation studies and efficacy of a surgical

Fig 5. The pectoralis minor and conjoined tendons were re-attached to the coracoid process with a nonabsorbable suture,and the pectoralis major was reattached similarly to its stumpon the proximal humerus.



exposure technique for management of large axillary tu-mors. Because of the rarity of such tumors, it is a relativelysmall and uncontrolled series, but it provides valuable in-formation regarding the validity of preoperative evaluationstudies in predicting the need for performing a limb am-putation and the efficacy of the extensile axillary approachin widely exposing the NVB.

All patients who underwent forequarter amputation hadtumor extension into at least two cords of the brachialplexus. Limited tumor extension into the brachial plexusand the need to sacrifice only one cord might result in areasonable function and allow a limb-sparing resection.We did not, however, encounter such findings in our se-ries.

The MRI scans did not provide data that assisted in theevaluation of tumor resectability. Magnetic resonance im-aging scans only showed vascular displacement, which didnot predict tumor irresectability. Vascular narrowing,which was only evident on angiograms, predicted neuro-vascular extension of the tumor. However, the majority ofour patients were treated before the availability of an MRangiogram, which provides anatomic data regarding thelesion and adjacent blood vessels. This type of imagingstudy possibly may show vascular morphology in additionto its displacement and be helpful in preoperative evalua-tion of axillary tumors.

The utilitarian shoulder incision originally was de-scribed by Henry4 for wide exposure of the proximal hu-merus. It since has been used routinely with slight modi-fications for resection of tumors of the proximal humerusand, with posterior extension, for resections of thescapula.1,2,5,10,11 We performed the same incision and sur-gical steps for exposure and resection of large axillarytumors because they provide good exposure of the entireaxillary cavity and allow dissection and mobilization ofthe NVB. This approach is compatible with the basic prin-ciple of wide exposure of the tumor and mobilization ofvulnerable structures before resection, and it was associ-

ated with what we considered acceptable morbidity. At-tempting to resect an axillary tumor using the traditionalaxillary approach, which is used for axillary lymph nodedissection, provides a relatively small aperture throughwhich the surgeon has to expose the entire extent of thetumor and manipulate the NVB. It would be very difficultto achieve a truly wide exposure and perform a safe re-section with it as we could with the extensile approachused in the study patients. Entering the axilla through itsbase provides one disadvantage of the extensile approach,which is the resultant scar along the anterior aspect of theshoulder. This cosmetic deficit is relatively inconsequen-tial, considering the potential role of this extensile ap-proach in preventing unnecessary injury to major nervesand blood vessels and local recurrence of an inadequatelyresected tumor. Functional outcome was good in most pa-tients and the limited shoulder ROM in three patients wasattributed to adjuvant radiation therapy rather than sequel-ae of surgery.

The objective of resection of axillary tumors is toachieve local tumor control. Patient survival is determinedby the presence of metastatic disease and its response toadjuvant treatments. We believe the rate of local recur-rence is the most appropriate criterion to evaluate the ad-equacy of surgical exposure and tumor resection. The lowpercentage (11%) of patients with local recurrence sug-gests the utility of the approach we used.

The results of preoperative evaluations provide infor-mation essential for determining the necessity of perform-ing additional chest wall resection and suggest the possi-bility of performing a limb-sparing resection. The pres-ence of limb edema, the neurologic findings, and theevidence of arterial narrowing on the arteriographs corre-lated with a likelihood of neurovascular tumor extensionand the consequent recommendation to perform limb am-putation to achieve local tumor control. However, the finaldecision to perform limb-sparing resection or an amputa-tion was based on the intraoperative findings of tumor

Fig 6. The functional parameters of 15 patients whounderwent limb-sparing tumor resections are shown.Although pain was alleviated satisfactorily and handpositioning and dexterity were preserved in most pa-tients, the decline in lifting ability, probably the resultof loss of motion around the axilla, was the prominentdeterminant in the loss of function observed after sur-gery.



extension to the NVB and the inability to find a plane ofdissection between them. The utilitarian shoulder incisionallowed optimal observation of an axillary tumor, and thesurrounding nerves and blood vessels. It is a reliable ap-proach for exploring and resecting axillary tumors and onethat allows the amount of local tumor control associatedwith tolerable morbidity.

AcknowledgmentWe thank Esther Eshkol for editorial assistance.

References1. Asavamongkolkul A, Eckardt JJ, Eilber FR, Dorey FJ, Ward WG,

Kelly CM, Wirganowicz PZ, Kabo JM. Endoprosthetic reconstruc-tion for malignant upper extremity tumors. Clin Orthop Relat Res.1999;360:207–220.

2. Bickels J, Wittig JC, Kollender Y, Kellar-Graney K, Meller I,Malawer MM. Limb-sparing resections of the shoulder girdle. J AmColl Surg. 2002;199:422–435.

3. Enneking WF, Dunham W, Gebhardt MC, Malawer M, PritchardDJ. A system for functional evaluation of reconstructive proceduresafter surgical treatment of tumors of the musculoskeletal system.Clin Orthop Relat Res. 1993;286:241–246.

4. Henry AK. Exposure of the proximal part of the humerus combined

with axillo-cervical extension to nerves and vessels. In: Henry AK,ed. Extensile Exposure. 3rd ed. London, England: Churchill Living-stone; 1995:38–53.

5. Malawer MM, Meller I, Dunham WK. A new surgical classificationsystem for shoulder girdle resections: analysis of 38 patients. ClinOrthop Relat Res. 1991;267:33–44.

6. Mansour KA, Powell RW. Modified technique for radical transme-diastinal forequarter amputation and chest wall resection. J ThoracCardiovasc Surg. 1978;76:358–363.

7. Roth JA, Sugarbaker PH, Baker AR. Radical forequarter amputationwith chest wall resection. Ann Thorac Surg. 1984;37:423–427.

8. Shmookler B, Bickels J, Jelinek J, Sugarbaker P, Malawer M. Boneand soft-tissue sarcomas: epidemiology, radiology, pathology, andfundamentals of surgical treatment. In: Malawer MM, SugarbakerPH, eds. Musculoskeletal Cancer Surgery: Treatment of Sarcomasand Allied Diseases. Dordrecht, The Netherlands: Kluwer Aca-demic Publishers; 2001:3–35.

9. Wittig JC, Bickels J, Kollender Y, Kellar-Graney KL, Meller I,Malawer MM. Palliative forequarter amputation for metastatic car-cinoma to the shoulder girdle region: Indications, preoperativeevaluation, surgical technique, and results. J Surg Oncol. 2001;77:105–113.

10. Wittig JC, Bickels J, Wodajo F, Kellar-Graney KL, Malawer MM.Constrained total scapula reconstruction after resection of a high-grade sarcoma. Clin Orthop Relat Res. 2002;397:143–155.

11. Wittig JC, Bickels J, Wodajo F, Kellar-Graney KL, Meller I,Malawer MM. Utilitarian shoulder approach for malignant tumorresection. Orthopedics. 2002;25:479–484.



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