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Annals of Surgical Oncology 9:472-479 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Gold Standard for Sternectomies and Plastic Reconstructions After Resections for Primary or Secondary Sternal Neoplasms

Cosimo Lequaglie, MD, PierPaolo Brega Massone, MD, Gabriella Giudice, MD and Barbara Conti, MD

From the Department of Oncologic Thoracic Surgery, Istituto Nazionale Tumori, Milan, Italy.

Correspondence: Address correspondence and reprint requests to: Cosimo Lequaglie, MD, Divisione di Oncologia Chirurgica Toracica, Istituto Nazionale Tumori, Via Venezian 1, 20133 Milano MI, Italy; Fax: 39-02-2360486; E-mail: lequaglie{at}istitutotumori.mi.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Between January 1980 and December 1999, 88 patients underwent the surgical resection of sternal tumors: 30 primary malignant tumors, 28 local relapses or metastases from breast carcinomas, 16 other types of tumor, and 14 radionecroses.

Methods: The sternectomies were total in 8 cases, subtotal in 32, and partial in 48. Prosthetic materials covered by flaps of myocutaneous or muscle tissue were used in 55 patients, prosthetic material alone in 13, myocutaneous or muscle flaps alone in 5, and other techniques in the remaining 15. The resection was radical in 78 cases and palliative in the other 10.

Results: Forty-eight of the subjects who underwent radical surgery were alive and disease free at the end of the follow-up period. The expected 10-year survival of the patients treated for primary tumors is approximately 85% (Kaplan-Meier), and that of the patients with relapsing breast carcinomas is the same as after 5 years (41.8%).

Conclusions: In our experience, the treatment of neoplasms by means of a broad sternal resection followed by a reconstruction based on the use of prosthetic materials is an effective and safe solution that considerably improves the quality of life and makes it possible to perform curative broad radical resections in the case of primary sternal resections.

Key Words: Sternectomy • Sternal tumor • Plastic repair • Long-term survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The advances that have been made in the methods of anaesthesia and reanimation, as well as improved surgical techniques, over the last few years have induced thoracic surgeons to perform sternal resections even in apparently extreme situations.1 Furthermore, a greater understanding of oncological diseases as a whole and the attention given to the prospective evaluation of the quality of life of patients with primary or secondary sternal tumors has led oncological surgeons to adopt a more determined attitude in terms of therapeutic options. Finally, the use of extended resection guarantees the complete cure of postactinic necroses of the chest wall. The choice of surgical technique depends on a number of factors, the most important of which is the size and site of the lesion, but its success depends on the full-thickness resection of the thoracic wall and the personal experience of the surgeon.2,3

Another problem is the restoration of ventilatory mechanics and the need to protect the intrathoracic organs. It has now become common practice to use more or less flexible prosthetic materials that are in any case malleable at the time of reconstruction and that favor rather than hinder physiological respiration.4 In the case of surface lesions, the current preference is to use myocutaneous flaps chosen on the basis of the area of the defect and the type of bone repair.5–8

Sternal tumors have long been considered a surgical challenge, mainly because of the difficulty in making full-thickness resections without compromising the stability and reconstruction of the thoracic wall, but improvements in surgical techniques now make it possible to perform even total sternectomies with virtually no operative deaths. The surgical approach must be considered the best therapeutic choice in most cases of primary sternal tumors.3,4,9 Broad full-thickness resections are no longer impossible, because the use of myocutaneous flaps and synthetic prostheses allows the simultaneous reconstruction of breaches in the chest wall.4,8

Nevertheless, the role of surgical treatment in the case of local relapses or distant breast cancer metastases is still a subject of debate.10–12 As far as relapses are concerned, surgery has been mainly used with palliative intent after the failure of radiotherapy, but an improvement in survival has also been reported.10 The use of sternal resections as a means of removing the metastases of tumors located in other sites is exclusively palliative (no increase in survival times has been observed) and is therefore feasible only as a means of improving the quality of life. The same is true in the case of postactinic necrosis after the failure of conservative therapies, and this often leads to a good cosmetic result.13,14

The aim of this study was to explore this subject further because, since the publication of our article in 1997,15 we have observed an exponential increase in the number of patients with sternal tumors: from 52 over a period of 13 years to 88 over 18 years. Given the fact that we have become a quasi reference center for situations of this type, we have analyzed the results of our personal and divisional experience in an attempt to contribute to the development of a standard approach toward the treatment of primary and secondary sternal tumors and radiation-induced necroses in the same anatomical region.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between January 1980 and December 1999, 88 consecutive patients (30 men: mean age, 48 years; range, 16–76 years; and 58 women: mean age, 53 years; range, 23–78 years) underwent sternal resection for tumors localized in the sternum, the anterior tract of the ribs, the costochondral cartilage, the peristernal soft tissue, or a combination of these (Table 1). Thirty patients (34%) had primary malignant tumors (Table 2). The most common histological type was sarcomas (22 cases), including 8 chondrosarcomas and 3 osteosarcomas; the other primary tumors were 1 case of lung cancer extending to the anterior tract of the ribs and costal cartilage, 1 sternal non-Hodgkin’s lymphoma, 1 laryngeal carcinoma involving the upper tract of the sternal manubrium, and 1 neuroepithelioma. Four patients had desmoid tumors, which were included among the primary malignant tumors because they required the same type of treatment.


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  		TABLE 1. Patient features
 

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  		TABLE 2. Primary and secondary malignant tumors with sternal radionecroses
 
Three patients had radiation-induced sternal sarcomas that appeared 10, 12, and 14 years after high-dose mediastinal radiotherapy administered to treat Hodgkin’s lymphomas. Twenty-eight patients (32%) had locoregional relapses of breast cancer (Table 2), which affected the peristernal soft tissue or the lymph nodes of the internal mammary chain in 22 cases; the other 6 patients had a single sternal metastasis.

Sixteen patients (18%) had sternal metastases of various origins, including eight sarcomas, three lung tumors, two thyroid carcinomas, one gastric carcinoma, one laryngeal carcinoma, and one pleural mesothelioma. Finally, there were 14 patients (16%) with radionecrosis and cutaneous ulcerations without any sign of residual tumor, 11 of whom had previously received combined therapies, such as mastectomies or quadrantectomies, for breast cancer (Table 2).

Eighteen patients underwent radiotherapy and 16 underwent chemotherapy for the curative or preoperative treatment of the sternal lesion. All of the patients were evaluated by means of chest x-ray, computed tomography (CT), nuclear magnetic resonance (NMR), or a combination of these; spirometry; and arterial blood gas analysis, and then they were completely staged (including total-body bone scintigraphy) to exclude the presence of extrathoracic metastatic lesions. The diagnosis and surgical treatment were based on anamnestic data, clinical and symptomatological evidence relating to the mass or pain, and CT or NMR images (which proved to be very useful in defining the extension of the tumor). Fine-needle aspiration or open biopsies of the lesion were positive in 72 of 73 patients, and the diagnosis allowed an adequate resection; in the 16 remaining cases, the clinical and radiological findings clearly indicated the presence of a primary malignant sternal tumor or radionecrosis, and so it was possible to perform an en-bloc radical resection without a previous biopsy.

The resections and repairs were performed in a single intervention. During anesthesia, all of the patients had each lung independently ventilated, and their central venous and arterial pressures were monitored.

The resection was considered radical if it included 3- to 4-cm margins macroscopically free of disease at both the cutaneous and underlying tissue level. The involved lung and mediastinal structures were removed in a single block. The resection of the sternal tumor began at a distance from the bone margins, leaving 3 to 4 cm of disease-free tissue on each side. Total sternectomy was performed in the case of large mediosternal tumors and tumors of the manubrium extending to the medial portion of the sternum, and partial sternectomy was performed in the case of tumors localized to the sternal manubrium or inferior sternal tract or involving the lateral portion of the bone. Eight patients (9%) underwent total sternectomy, 32 (36%) underwent the subtotal resection of >50% of the sternum, and 48 (55%) underwent the partial resection of <50% (Table 3). In all cases, the resection margins were simultaneously examined by frozen section by means of microscopy. The internal mammary veins and arteries were usually spared with the aim of being able to use a flap of abdominal rectal muscle if required (nine cases).


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  		TABLE 3. Type of sternal and associated resections
 
Sixty-one patients (69%) underwent an en-bloc resection that included the anterior tract of the ribs: five ribs were resected in 1 patient, three or four in 27, and one or two in 23; in the remaining patients, the resection was limited to the costal cartilage. The average size of the sternal resection (including the ribs) was 142.5 cm2 (15 x 9.5 cm), with the largest being 580 cm2 (29 x 20 cm). The lung was simultaneously resected in 22 patients, the clavicle in 13, the pericardium in 17, the diaphragm in 4, the clavicle with pericardium and lung in 6, the larynx in 1, the thyroid in 1, and the diaphragm/pericardium and liver in 1.

Various techniques were used for the reconstruction, depending on the experience of the surgeon and the need to guarantee the stability of the chest wall, with the aim of limiting flap movement and consequent paradoxical respiration. The most frequently used prosthetic material was a polypropylene net (67 cases; 76% of the total). Muscle flaps were used in 55 patients (62%), prosthetic materials and muscle flaps were combined in 50 patients (57%), and the heart was protected by Gore-Tex (W. L. Gore & Associates, Newark, DE) membranes in 4 cases of broad pericardial resection (Table 4). The upper layers of the breach were reconstituted by using skin flaps in 21 cases and primary skin closure in 12.


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  		TABLE 4. Plastic repair of sternal defect after sternectomy
 
The patients were observed until September 2000 (a minimum of 12 months). The actuarial survival from the time of resection was calculated according to Kaplan-Meier; the statistical analysis was performed with the log-rank test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Seventy-eight patients (87%) underwent radical resection with a curative intent. The intervention was palliative in 10 cases: in 4 patients, the margins of the resected piece were found to be positive at the final examination, and the other 6 had distant metastases. In the case of these 6 patients, the decision to proceed surgically was made with the aim of obtaining local disease control, reducing chest pain, and improving the quality of life. All 10 patients were in good general condition and were not candidates for radiotherapy, for various reasons. There was 1 case of perioperative death due to multiorgan failure (Table 5), and morbidity was limited to 13 cases (14%). Twelve patients13 presented complications at the site of the surgical wound. These included wound necrosis in three patients (one diabetic); the necrosis was self-limiting and spontaneously healed in one case but required the excision of the necrotic tissue and the positioning of a covering myocutaneous flap in two cases (a pectoralis major flap in one case and, in the other, a flap of the great dorsalis after removal of the previously used abdominal rectal flap). Five patients experienced surface wound infections, and five developed a conservatively treated seroma. One patient presented local sepsis that required the removal of the silicon prosthesis and repeated washings of the wound, but the Marlex (C. R. Bard, Inc., Murray Hill, NJ) net was not removed. One patient, who developed bilateral pulmonary aspergillosis treated with antifungal therapy, was transferred to the intensive care unit and underwent mechanical ventilation for 6 days.


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  		TABLE 5. Complications after sternectomy and repair
 
As a result of prolonged protein losses, many of the patients received plasma or albumin infusions; furthermore, 29 patients were given blood transfusions (an average of 3 bags per patient; range, 1–8). The rare occurrence of electrolytic alterations was never so severe as to lead to renal or cardiological damage. The thoracic drains were removed an average of 8 days after the operation (range, 2–28 days). Postoperative hospitalization was an average of 13 days (range, 3–60 days); in the complication-free cases, the average was reduced to 7 days. Only 14 patients received postoperative adjuvant chemotherapy or radiotherapy (7 cases each).

Forty-eight patients (55%) were alive at the end of the study, and 36 (40%) were dead after the resection procedure. Total survival (Fig. 1) in the radically resected group was 70% after 3 years, 61% after 5 years, and 56% after 10 years. Three of the 10 patients undergoing palliative resection were alive after 5 years—a total 5-year survival rate of 30%.



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  		FIG. 1. Overall survival rate after radical and palliative sternal resection for tumor.

 
The actuarial survival of the radically treated patients depended on the diagnosis (Fig. 2): the 10-year survival in the patients with primary tumors of the chest wall was 85%, whereas none of the patients with metastatic tumors were alive 10 years after the operation, and their survival curve precipitously declined after 5 years. The 10-year survival in the patients with breast cancer relapses was significantly different from that of the patients with primary thoracic wall tumors (41.8%). Nevertheless, surgery proved to be a good therapeutic option even when performed with palliative intent, particularly in cases of breast cancer relapses (Fig. 3).



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  		FIG. 2. Survival rate and different tumors after radical resection.

 


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  		FIG. 3. Survival curves and different resection for breast cancer recurrences.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Primary tumors of the sternum account for approximately 1% of all primary bone tumors. The precise evaluation of the extent of such tumors requires a thorough radiological examination because the clinically appreciable mass often represents the tip of an iceberg involving the sternum. CT and NMR images clearly reveal the extent of the tumor and can identify the presence of any pulmonary or lymph node metastases, and bone scintigraphy can identify any metastases in other skeletal sites. Lung function tests are particularly important in patients with cardiopulmonary diseases, the elderly, and all subjects requiring broad lung resections. We adopted the usual preoperative evaluation criteria and considered a resection possible if the lobe forced expiratory volume in 1 second (FEV1) was >=1 L and the lung FEV1 was >=2 L, or if the expected postresection residual FEV1 was not <800 mL. Many of our patients (n = 72) were preoperatively diagnosed by means of fine-needle aspiration or open biopsy. Some authors have reported that needle biopsies are inadvisable because of their limited accuracy,3 but open or tru-cut biopsies can lead to positive results. Because open biopsies are sometimes incapable of distinguishing benign and malignant cartilage tumors, a broad resection is advisable in uncertain cases. Resections not preceded by biopsies may be justified in the case of lesions with a diameter of <4 cm, and our series included 15 cases of this type. Whenever possible, surgery is the treatment of choice for primary thoracic wall tumors involving the sternum, 1,3,4 and this is supported by the 85% 10-year survival of our 30 cases.

Pathologists consider desmoid tumors to be benign fibromatous tumors or fibrosarcomas with a low grade of malignancy, but, whatever the type, they tend to relapse if they are not adequately excised. We believe that desmoid tumors should be resected, leaving a broad margin of free tissue (precisely as in the case of malignant tumors), to avoid local relapses.4 In any case, it is prudent to consider all sternal tumors malignant until there is proof to the contrary.

In 1978, Holden16 was the first to describe a partial sternectomy for a primary sarcoma. The sternal sarcomas that develop as a result of broad mediastinal irradiations intended to treat a lymphoma are particularly difficult to manage: the borders between a tumor and radio-induced fibrosis may not be very clear, and so the tumor may easily relapse even if the resection margins are histologically negative.13 In our series, three patients with radio-induced sternal sarcomas after Hodgkin’s lymphoma therapy presented diffuse mediastinal metastases a few months after radical sternectomy and died within 3 years of the operation.

However, the role of surgery is controversial in the case of breast cancer relapses or metastases involving the thoracic wall and sternum,10,17,18 and it is essentially considered a palliative means of controlling local disease. Various studies,11,12,18,19 including one of ours published in 1992, 18 have supported the usefulness of a radical surgical approach in relapsing patients and those with a single metastasis localized to the chest wall and sternum, because this could improve survival. It has been suggested that sternal metastases may remain solitary for a long time and that their evolution is different from that that of vertebral metastases, probably because of the limited communications with the paravertebral venous plexus through which the cancerous cells are disseminated to other bone structures.10

We think that the surgical option can be considered in the framework of a multimodal approach to the treatment of solitary bone metastases that includes radiotherapy, chemotherapy, and hormonal therapy. A breast cancer relapse or metastasis exclusively localized to the thoracic wall has a better prognosis in the absence of metastases to the mediastinal lymph nodes and the internal mammary chain, but, if the mediastinal lymph nodes are involved, there is a high likelihood of disease progression.12,18 In such cases, when local control cannot be obtained by means of radio- or chemotherapy, surgery can still be considered with the aim of relieving the chest pain, inflammation, infections, and bleeding associated with relapses. We operated on the secondary neoplasms when there was a long disease-free interval (more than 24 months) or when there was a single sternal metastasis. However, we also performed surgery with palliative intent to offer a better quality of life after resection.

In the case of postactinic necrosis, resection is indicated after the failure of conservative treatments, such as hyperbaric oxygen therapy, to exclude the presence of local or distant tumoral relapses.14 When the surrounding skin and soft tissue are also involved and their vascularization is compromised by previous radiotherapy, it is necessary to provide broad surface coverage of the wall defect, and this requires careful planning: e.g., the omentum could be placed between the Marlex net and the skin to improve skin vascularization.3 The acrylic prostheses and mesh cannot be tolerated in some patients with radionecrosis even after many months from the reconstruction. The resection, however, might be farther from the previous radiation field if recently performed (<3 months).

In relation to the resection margin, many authors recommend leaving 3 to 4 cm of free tissue around the tumor or the irradiated tissue.11 Others4 maintain that at least 4 cm of free tissue should be removed en bloc with the resection throughout the thickness of the involved bone (manubrium, body, or the entire sternum) and the anterior tracts of the bilaterally corresponding ribs, as well as the uninvolved rib above and below the lesion, including the related intercostal space.3,20

The surgical resection begins with a vertical elliptical incision including the mass. Mobilization is then begun first on one side of the sternum, with exposure and section of the ribs. We approach the sternum from the periphery, leaving any critical point of bone attachment to the heart and great vessels to the last. Sometimes a Gigli saw is used to transect the sternum in its upper free margin. Both internal thoracic vessels by this time would have been identified, dissected out, and ligated before division.

Various techniques have been used in the past to repair the defects in the anterior thoracic wall: the fascia lata, rib grafts, large skin flaps, and the contralateral breast. An important advance has been the use of myocutaneous flaps, thus conserving the tributary vascular system.21 The possibilities of combining prosthetic materials and myocutaneous skin flaps are potentially infinite, and there is often more than one option for resolving the situation effectively in each individual patient.

The need for a skeletal reconstruction depends on the size and site of the resection4,13: it is necessary in case of removal of the sternum and the anterior and lateral tracts of the ribs, but it may not be necessary for the repair of posterior wall defects entirely covered by the scapula (provided that its rotation does not lead to its becoming entrapped in the breach9) or if the defect can be stabilized by the action of the adjacent muscles. Some authors believe that defects of the sternal and posterior walls need to be stabilized less frequently than anterior or lateral defects.4,12 Various types of prosthetic material can be used: polypropylene and Vicryl (Johnson & Johnson, New Brunswick, NJ) nets or Gore-Tex patches are well tolerated and easy to handle and can be sutured under tension, thus improving the stability of the thoracic wall.

Gore-Tex has the advantage of being impermeable to air and liquids, but it is very expensive4; nets in general are cheaper, but the passage of serum or blood through the prostheses favors their encapsulation in neighboring structures. Polypropylene nets are the most widely used because of their resistance, manageability, and tolerability over time: they hardly ever give rise to reactions against a foreign body or septic complications. The difference between Marlex and Prolene (Ethicon, Inc., Somerville, NJ) lies in the fact that the former has a double and the latter a single layer: when Prolene is extended, it remains rigid in all directions, whereas Marlex is rigid in only one direction. After a total sternotomy or a broad resection including the lateral portion of the thoracic wall and more than four ribs, a sandwiched polypropylene and methacrylate net offers the best results in terms of stability, intrathoracic organ protection, and pulmonary expansion, although some authors prefer using Gore-Tex prostheses or simple muscle flaps without rigid supports.3,4,12 In our opinion, the best method of reconstruction is acrylic and mesh. This choice is motivated by the better stability of the chest than other softer prostheses.

Myocutaneous flaps have now replaced skin flaps or the transposition of the breast in the reconstruction of the soft tissue layer because they are safer and more reliable over the long term. This is particularly important in cases of breast cancer relapses and postactinic necrosis because the surrounding tissue has usually been damaged by the previous treatments. Depending on the circumstances, various types of myocutaneous flaps can be used alone or in combination: the pectoralis major to ensure the continuity of the supero-anterior thoracic sector, the transversus or serratus muscle for anterior and lateral wall defects, and the great dorsalis for both anterior and posterior defects. We prefer the pedicled flaps, and we do not use free flaps because of the increased probability of morbidity (i.e., partial necrosis for less vascularization).

From our experience, we believe that a combination of two layers of mesh with acrylic to be the best choice in the sternectomy repair. In any case, most patients had the prosthetic material covered by flaps of myocutaneous or muscle tissue with the aim of a safer local restoration of the chest wall.

The use of the omentum has been proposed as an alternative to muscle flaps because of its excellent vascularization4,22 and the good results obtained in potentially infected areas. The clinical results are favorable,7,23 but the obvious disadvantages are the need to perform a minilaparotomy and the lack of cutaneous coverage, which has to be created in another manner.

In patients who already have septic wounds or who are at high risk of infection (such as those with radionecrosis), it is possible to use a myocutaneous flap without the support of prosthetic materials, but respiration leads to a paradoxical movement of the reconstructed chest wall. We used a polypropylene net in 10 of 14 patients undergoing surgery for postactinic necrosis, none of whom experienced postoperative sepsis or other complications.

The reported 5-year survival of patients with malignant primary thoracic wall tumors is from 46% to 66%; the 10-year survival rate in our series was 85%. The published 5-year actuarial survival rate after resections performed for relapsing breast cancer ranges from 34% to 63%.10,18,24

The results of the long-term follow-up of our patients confirm that the treatment of primary and secondary sternal tumors by means of broad sternal resections followed by plastic reconstruction using prosthetic materials, myocutaneous flaps, or both is safe and effective, as can be seen from the calculated 10-year survival rates of 85% among the patients with primary tumors and approximately 42% in those with breast cancer relapses. We started using only simple prosthesis when the soft tissues were enough to approach the resection margins, but during our experience we modified the technique and included the pedicled flaps for better repair and for cosmetic and functional aims. Various combinations of myocutaneous flaps and prostheses can be used: the choice of the reconstruction technique depends on the size and site of the defect in the continuity of the thoracic wall and the preference of the surgeon. However, it is clear that major en-bloc resections of the sternum—including the pericardium, lung, or diaphragm—can be performed with zero mortality, minimal morbidity, and acceptable hospitalization times, provided that all of the steps are standardized (from the indication for surgery to postoperative care).

Furthermore, for patients with relapsing breast cancer and postactinic necrosis, resection offers a significant and permanent palliative solution, as shown by the fact that none of our patients experienced a local relapse or postoperative disturbances. This kind of procedure could be recommended for palliation to obtain an improved quality of life and, obviously, to reduce chest pain and to debulk the sternal mass. Radical resection can definitively cure primary tumors and thus offer patients an optimal probability of long-term survival.


   Footnotes
 
Presented at the 54th Annual Cancer Symposium of the Society of Surgical Oncology, Washington, DC, March 15–18, 2001.

Received for publication May 7, 2001. Accepted for publication February 9, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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A. Watanabe, T. Watanabe, T. Obama, H. Ohsawa, T. Mawatari, Y. Ichimiya, N. Takahashi, and T. Abe
New material for reconstruction of the anterior chest wall, including the sternum
J. Thorac. Cardiovasc. Surg., October 1, 2003; 126(4): 1212 - 1214.
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