Chirurgie thoracique · Vol. 23 Juin 2019
Background: Chest wall lesions and invasion are a rare occurrence in operable breast cancers, and their care requires multidisciplinary teamwork between thoracic and breast specialists. Other chest wall lesions—radiation-induced sarcomas, Stewart-Treves syndromes, and osteoradionecrosis—are consecutive to breast cancer treatments. This article aims to update readers on chest wall resection and reconstruction techniques which are useful in these cases, as well as their indications and results.
Method: A systematic review was conducted to identify chest wall reconstruction techniques and their place in locally advanced breast cancer (LABC), local recurrences, secondary sarcomas and radionecrosis.
Results: Chest wall reconstruction must ensure good stability and protection of the intrathoracic organs. Titanium prostheses and protective meshes are widely used for these purposes. They can then be covered, if necessary, by a flap—mostly latissimus dorsi flaps, but also deep inferior epigastric perforator or superficial epigastric artery flaps. Few LABC and local recurrence patients are eligible for surgery, which has few complications, but patient selection must be strict, and outcomes are still debated. Radiation-induced sarcomas and Stewart-Treves syndrome have a poorer prognosis, even when surgery with healthy margins is possible. Osteoradionecrosis surgery relies on bringing a new vascular supply via a flap; the omentum is widely used here for its detersive properties.
Conclusion: Novel chest wall reconstructive techniques, and a liberal use of flaps, make surgery technically possible for chest wall damage linked to breast cancers and their treatments. Functional results are reliable, but not all patients can benefit from surgery.
Chest wall lesions and invasion seldom occur in operable cancerous breast disease, and their care requires multidisciplinary teamwork between thoracic surgeons and breast specialists . A finely tuned collaboration between surgical specialties is key to such a major surgery. Indeed, extensive chest wall resections are complex interventions that must reconcile carcinological imperatives and reconstruction possibilities. Thanks to the emergence of reliable prosthetic material since the end of the 20th century, chest wall reconstruction techniques have much improved, and parietectomy indications are growing .
Locally advanced breast cancers (LABC) encompass tumors bigger than 5 cm (T3), tumors extended to the chest wall (T4a), or the skin (T4b) (figure 1a), or both (T4c), and inflammatory breast cancers (T4d) (figure 1b), as well as tumors with massive lymph node extension [2-3]. They make up about 20% of breast cancers throughout the world (although less in countries with organized screening) , and 5% of thoracic neoplasias . The scope of this article is restricted to those T4a tumors with chest wall invasion.
[caption id="attachment_4345" align="aligncenter" width="300"] Fig. 1a: Locally advanced breast cancer with skin invasion (T4c).[/caption]
[caption id="attachment_4346" align="aligncenter" width="300"] Fig. 1b: Inflammatory breast cancer (T4d).[/caption]
Chest wall invasion can be the result of direct infiltration as well as lymphatic dissemination, and involves all the neighboring structures: skin, pectoral muscle, ribs and the intercostal space, but also the axillary and subclavian vessels and the brachial plexus . Lymphatic invasions involve homolateral lymph nodes from the axillary, supra and subclavian chains, as well as the internal thoracic lymph nodes . This explains the radical approach of Halsted’s operation, that removed the breast together with the pectoral muscle and required extensive lymph node dissection, even for small tumors. However, such mutilating surgery yielded poor oncological results that came at the price of a still poorer quality of life.
Throughout the second half of the 20th century, advances in medical treatments have reduced surgical indications for locally advanced breast cancers. Surgery became less invasive, beginning in 1948 with Patey’s operation, which preserved the pectoral muscle and facilitated reconstruction. A better grasp on the balance between an extensive surgery and postoperative quality of life has made surgery less aggressive, and a combined medical approach of chemo and radiotherapy, as well as the development of hormonal treatments and later still targeted therapy, has become the usual approach. However, as reconstruction techniques improve , bringing less morbidity and a better postoperative quality of life, radical surgery has a new place in the care of these patients.
Primary oncological treatment isn’t the only reason behind chest wall involvement in breast cancer pathology. However, late complications of the initial treatment are frequent, particularly when radiotherapy has been involved. Ever since the “cobalt bomb”, and until the current state-of-the-art stereotaxic techniques, technical progresses have led to a drastic reduction of healthy tissue irradiation. Therefore, the incidence of chest wall complications after radiotherapy should seemingly decrease in the years to come; but on the other hand, more patients benefit from breast conservation therapies, and that means more irradiated patients, although with lower doses . Whatever trends arise in the future, radiotherapy complications remain a prevalent problem that can appear years after treatment. Double-strand breaks in DNA and oxidative stress induce two major long-term complications: radiation-induced cancer, and radionecrosis. Both can develop on the sternum, the clavicle and cervicothoracic junction, and as such are a surgical challenge. Proximity with the mediastinal structures and the upper limb neurovascular bundle, as well as the reconstruction and stabilization imperative after chest wall resection, requires these patients to be treated in a referral center that has access to modern reconstructive techniques .
This article aims to update readers on chest wall resection reconstruction techniques, as applied to breast cancer, as well as their indications and results.
Relevant articles were identified by a systematic search of the MEDLINE database, limited to articles in English and French languages, published after 2000 and before July 2017. A broad search of medical subject headings and their different combinations (“thoracic wall”, “breast neoplasms”, “thoracic surgical procedures”, “reconstructive surgical procedures”, “surgical flaps”, “free tissue flaps”, “myocutaneous flaps”, “sarcoma”, and “osteonecrosis”) was conducted for clinical trials and systematic reviews. Studies that reported surgical techniques and their medical outcomes were included. To broaden the search, the reference list of systematic reviews was screened manually for controlled trials and additional publications were retrieved from the reference list of relevant articles (figure 2).
[caption id="attachment_4347" align="aligncenter" width="300"] Figure 2: PRISMA 2009 Flow diagram of article selection.[/caption]
3. RECONSTRUCTION TECHNIQUES
3.1. Biomechanical basis
Because of the position of the breast on the thorax, chest wall resections in breast cancer mostly concern its upper and anterolateral region. This region is biomechanically complex because of its anatomical characteristics . The sternum is, first and foremost, the cornerstone of thoracic stability. Besides protecting the lung and mediastinal organs, the anterior thoracic skeleton also stabilizes the shoulder via the sternoclavicular joint and is the anchor of the accessory respiratory muscles (pectoral and anterior cervical muscles). Intercostal spaces widen as they get closer to the anterior midline, meaning that even small anterior costal resections create large defects that inhibit respiratory mechanics.
Reconstructive goals are not specific to breast cancer, and are those of every chest wall reconstruction [8-9]:
Chest wall stability, in order to prevent paradoxical respiration, restore respiratory mobility and limit restrictive after-effects;
Protection of intrathoracic organs, (particularly avoid pulmonary hernia) and dead space obliteration;
Preservation of sternoclavicular stability;
Restoration of esthetics.
Overall the patient condition is critical and must be evaluated before heavy reconstruction is undertaken. Surgical gain must be balanced to its possible complications and the oncological prognosis [3,10,11]. The quality of resection must not be compromised in order to limit its scope; it is better to do no surgery, but instead a good medical treatment, than an incomplete surgery with severe complications. Comprehensive care is therefore essential and must include thoracic and reconstructive surgeons, but also nutrition specialists. Smoking cessation is imperative, and any underlying osteitis must be treated.
3.3. Reconstruction materials
Reconstruction after a full-thickness chest wall resection must be done immediately, as a single-step procedure [9,12,13]. It can be completed later, for example by a split-thickness skin graft, but the chest wall must be stabilized right away. In 2004, Losken et al. published a decision algorithm for reconstruction techniques . When the resection, whatever its size, removes at least part of one rib, a prosthetic mesh must be implanted in order to protect the underlying organs. When two or more ribs are removed, the chest wall must be stabilized by rigid material.
Rigid autologous materials, such as bone and cartilage, are not used anymore in chest wall stabilization, because of a lack of both rigidity and temporal stability . Besides, donor site morbidity cannot be ignored .
Biomaterials, such as cryopreserved homografts and allografts, are still seldom employed. However, acellular dermal matrices are more often used . In order to ensure a satisfying rigidity, these are combined with rigid prosthetic materials, that are currently dominated by titanium .
Titanium has several qualities that make it a staple of thoracic bone reconstruction. Its biocompatibility is excellent, with good tolerance to infection , and its flexural rigidity is close to that of the original bone . Titanium plates have, however, been rendered near obsolete due to the use of autologous materials, but also that of methyl methacrylate cements to mold artificial ribs and sternums [15,18]. Although there is a lack of peer-review studies on cement biomechanical properties when used in the thorax , it is considered brittle in the long term, because of stress fatigue induced by respiratory movements [20-21]. In contrast, titanium has an excellent tolerance to such long-term stress . Additionally, cement reconstructions are difficult to remove should a septic complication happen.
Porous alumina ceramic can also be used for sternal replacement (figure 3) . The material can be loaded with antibiotics, which can prove useful for use in an infectious context .
When the chest wall resection is small (< 5cm and removal of only one rib), either a flap (pedicled or rotation flap) or direct closure (if the adipose tissue is thick enough) may be able to stabilize the thorax [12,25]. Titanium plates should be used when two or more ribs are removed, but also when part of the sternum is removed [12,18]. When a sternectomy is performed, standard osteosynthesis material can be used to bridge the parietal defect, but custom-made titanium plates have also shown excellent functional results, and ease mechanical ventilation weaning [15,17]. When the sternoclavicular joint is removed together with the manubrium, it is possible to implant an articulated prosthesis in order to preserve shoulder function (figure 3) . However, some prefer to avoid joint reconstruction, for fear of rupture under stress.
[caption id="attachment_4348" align="aligncenter" width="300"] Figure 3: Ceramil® porous aluminia ceramic sternal prosthesis (ICeram, Limoges, France, photography courtesy of Dr Bertin and Dr Tricard).[/caption]
Such rigid material can be placed over a protective mesh, in order to avoid lung herniation. Many different types of mesh are available, and this may be absorbable or not , including: polypropylene, PTFE and polyglactin. Whatever material is chosen by the surgeon, it must be both pliable and robust . In septic conditions, absorbable polyglactin meshes must be used, and are therefore favored in radionecrosis cases . After healing, absorbable meshes are replaced by rigid fibrotic tissue . Meshes can be superimposed in order to increase rigidity [3,27]. When there is a phrenic resection too big to be stitched, it must be reconstructed with a thick PTFE mesh [8,10].
Prosthetic materials, whatever their nature, must be covered by the end of the surgery, and this can require a graft. As long as the graft and surrounding tissue remain well vascularized, the infectious risk is low, even in a previously infected site . All these reconstructive techniques allow for good postoperative functional results .
3.4. Reconstructive flaps
Flaps can be divided into two major categories: pedicled flaps and free flaps . These can also be either myocutaneous or fasciocutaneous. Scientific evidence for flap choice in breast reconstruction is weak , and there is an even greater lack of data when the chest wall is involved. No comparative study was found. The choice between flaps is made on a case-by-case basis , according to the surface area that needs covering, patient morphology, surgical scarring and irradiation history on donor sites, esthetical and functional consequences and, of course, the technical challenge of some grafts that heighten post-operative complications. While regional pedicled flaps are usually the first choice, free flaps may be the only options, particularly when pedicled flaps have already been used or damaged by previous surgery or radiotherapy .
Free flaps require microsurgery vascular anastomosis techniques in order to graft the flap far from the donor site. The recipient vessels are usually the internal mammary pedicle, thanks to their high blood flow, easy access, constant position and the freedom to position the flap wherever needed on the chest wall . While previous irradiation doesn’t forbid the use of the internal mammary artery, it can sometimes be too small or fragile to provide a correct vascularization, or may have already been used for a coronary artery bypass. In these rare cases, the thoracodorsal vessels are used instead for anastomosis . The most commonly used free flaps [30,33,34] are, as of 2017, the fasciocutaneous deep inferior epigastric perforator flap (DIEP) (figures 4a and 4b) and the superficial inferior epigastric artery flap (SIEA), followed by musculocutaneous flaps such as the gracilis or gluteal flaps. The major benefit in using a free flap is the ability to choose a donor site far from the irradiation fields. Besides, fasciocutaneous flaps do not result in a muscular defect. However, they require challenging microsurgical vascular anastomoses that are prone to thrombosis.
[caption id="attachment_4349" align="aligncenter" width="220"] Fig. 4a: Donor site for abdominal flaps. The skin paddle is the same for both DIEP and TRAM flaps.[/caption]
[caption id="attachment_4350" align="aligncenter" width="238"] Fig. 4b: The DIEP flap harvests only the fasciocutaneous tissue and the pedicle, leaving the abdominal wall structurally untouched.[/caption]
[caption id="attachment_4351" align="aligncenter" width="238"] Fig. 4c: The TRAM flap harvests the transverse rectus abdominis muscle; the abdominal wall defect must be reinforced by a prosthetic mesh in order to avoid eventration.[/caption]
Pedicled flaps, on the other hand, keep their original vascular supply. Instead of being relocated to another anatomical region, a simple rotation brings them where they are needed. The best known myocutaneous pedicled flaps are the latissimus dorsi flap (figures 4a, 4b and 4c) (it is usually possible to preserve part of the muscle in these indications)  and the pedicled transverse rectus abdominis flap (TRAM) (figure 4c) . The latissimus dorsi flap (figures 5a and 5b) is often the first choice, provided it hasn’t been used in a previous breast reconstruction. It is an easy flap to perform and can cover a large area with few functional and esthetical consequences. In case of past extensive lymph node dissection, the integrity of the thoracodorsal pedicle and the latissimus dorsi nerve must be assessed preoperatively. The major drawbacks of the latissimus dorsi flap are postoperative pain and recurrent seromas on the donor site. Loss of shoulder function is usually transitory, getting back to baseline in 6 to 12 months, but activity can still be limited in the meantime . Pedicled TRAM flaps are seldom performed anymore, because of the major abdominal wall defect they cause . They are now usually replaced by the free fasciocutaneous DIEP flap that uses the same donor site (figure 4a) with much less morbidity [34,36]. Over pedicled flaps have been described for chest wall reconstruction after breast cancer, most notably ipsilateral thoracoabdominal horizontal dermofat flaps .
[caption id="attachment_4352" align="aligncenter" width="202"] Fig. 5a: Donor site of a latissimus dorsi flap.[/caption]
[caption id="attachment_4353" align="aligncenter" width="238"] Fig. 5b: Latissimus dorsi flap used for breast reconstruction.[/caption]
[caption id="attachment_4354" align="aligncenter" width="300"] Fig. 5c: Post-operative results.[/caption]
Last but not least, the pedicled omental flap is a staple of thoracic surgery. It can be harvested by laparoscopy or by a mini laparotomy and is usually rotated on the right gastroepiploic pedicle. Its size enables a wide cover of the anterior and lateral chest wall and, while it has been used in breast reconstruction after mastectomy, its most widespread use is in radionecrosis and infected cases . The omentum’s detersive properties and rich vascularization, together with its size, make it a versatile and reliable flap that can later be covered by a split-thickness skin graft .
4.1. Locally advanced breast cancer
The 2017 European Society for Medical Oncology (ESMO) guidelines recommend to consider surgery after neoadjuvant treatment for LABC . Indeed, when there is a good response to neoadjuvant systemic therapies, surgery often does become technically possible with an acceptable morbidity . Mastectomy with axillary dissection is usually advised, but sometimes a chest wall resection is also necessary for a proper en bloc surgery. MRI can be useful to predict chest wall invasion and the necessity of a full-thickness chest wall resection . Margins should obey the “no ink on tumor” rule [43,44].
Survival data for chest wall resections in breast cancer are scarce and mostly available through small retrospective series [45-48]. Additionally, these mostly concern local recurrences and not initial treatment. Still, they are reliable enough to show that survival is correlated with tumor type and, in particular, hormonal status. Santillan et al., in a series of 28 patients, found that 5-year survival was null for triple negative breast cancers, but rose to 39% for the other patients. Overall 5-year survival varies between 18 and 66% [45,48,49]. Operative mortality is null, and morbidity varies between 21 and 36% in referral centers [45,50].
Overall, disease-free survival in operated LABC might not be much more than medical treatment alone. No randomized controlled trial or meta-analysis have tested that hypothesis and such a lack of data advocates for stringent patient selection [48,49]. Once metastatic patients are excluded, as well as those who did not respond to neoadjuvant treatment, few patients are eligible for such surgery. Whenever it is performed, it should be carried out with the utmost care in order to achieve complete resection [40,51]. However, regardless of oncological curative intent, there is also room for surgery in ulcerated lesions, in order to improve the quality of life of patients with bleeding, septic and malodorous tumors.
4.2. Chest wall recurrences
Less than 5% of patients who undergo a mastectomy for breast cancer suffer from a local recurrence in the first decade. Such local recurrences are fairly diverse, from an isolated nodule on the former scar to a massive chest wall and lymph node invasion . When a local recurrence is truly isolated, without distant metastasis, a local treatment is recommended, combined with a systemic approach . Surgery has been considered for these patients since the 1990s, provided that complete resection is possible .
Patients who have never had radiotherapy should be irradiated first. However, radiotherapy may not be possible, particularly in patients who have already undergone irradiation, and, for these, surgery is the recommended treatment. A single superficial soft tissue exeresis may be enough but, depending on the invasion depth, authentic chest wall resections can also be performed [3,50]. Prognosis, on the whole, is variable, and mostly influenced by the initial nodal status . A 2018 meta-analysis found that quality of life and long-term survival are improved in approximately 40% of patients who undergo full-thickness chest wall resection .
4.3. Radiotherapy complications
4.3.1. Radiation-induced sarcomas
Radiation-induced sarcomas (figures 6a and 6b) are a rare complication, with an incidence of 0.2% after 10 years and 0.4% after 15 years. However, some patients, who bear a constitutional mutation of the p53 anti-oncogene, have a heightened sensitivity to radiation . This, in turn, worsens their risk of radiation-induced sarcoma . A p53 mutation should be ruled out in patients with a family history of Li-Fraumeni syndrome before any irradiation; when present, radiotherapy should be avoided [56,57].
[caption id="attachment_4355" align="aligncenter" width="300"] Fig. 6a: Axial MRI images of radiation-induced chest wall sarcoma in an 82-year old woman, 17 years after radiotherapy for breast cancer.[/caption]
[caption id="attachment_4356" align="aligncenter" width="280"] Fig. 6b: Sagittal MRI images of the same case.[/caption]
Secondary sarcomas are most frequent on the fringe of the irradiation fields, where DNA damage, while non-lethal, creates many carcinogenic mutations. As such, any peripheral lesion should undergo biopsy before treatment to ensure a correct diagnosis – usually image-guided percutaneous core needle biopsy under local anesthesia . The biopsy site must be marked, so that it can be removed later during surgery and thus avoid dissemination of cancer cells . Diagnostic criteria for radiation-induced sarcomas, established in 1948 by Cahan et al. , rely on two items. More than 10 years must have elapsed since irradiation and the secondary tumor histology must be different from the previous one. Later updates of the criteria, by Arlen in 1971 and Cahan in 1998, accept a shorter interval of, respectively, 3 and 5 years; the major criteria remains a history of irradiation on the sarcoma territory .
Many histological types of sarcoma can appear after irradiation. In some series, angiosarcomas account for more than 50% of cases, while for others histiocytic fibrosarcomas are the rule . Undifferentiated tumors, osteosarcoma, fibrosarcoma and rhabdomyosarcoma are also frequently described . Whatever the exact histological subtype, these are always high-grade tumors, where diagnosis is often delayed and the prognosis is poor . Indeed, radiation-induced sarcomas of the breast are on average, at diagnosis, more advanced and of a more aggressive histology than primary sarcomas .
Whenever there are no metastases and resection is technically feasible with an acceptable operative risk, surgery should be performed [58,62]. Linthorst’s team have described a multimodal therapy that combines surgery, re-irradiation and hyperthermia therapy, with no significant survival improvement compared to the medical treatment group . Surgery with healthy margins is the best prognosis factor for radiation-induced sarcoma. However, local recurrence is frequent, with an incidence of up to 65% . Overall 5-year survival is poor, ranging between 10 and 36% [59,65]. Prognosis is poorer than that of primary sarcomas ; Yin et al.’s series found a 5-year overall survival of 22.5% for radiation-induced sarcomas of the breast, much lower than the 44.5% rate for primary breast sarcomas. However, when all the confounding factors (particularly age and staging at presentation) are controlled, survival is comparable.
Irradiation leads to the formation of scar tissue and fibrosis, and this in turn leads to a thrombotic microangiopathy. The consecutive tissular hypoxemia, together with cytokine modifications, paves the way for osteoradionecrosis . As fibrosis and necrosis progress, a skin defect appears, and healing is hindered by mediocre tissue perfusion (figure 7). The wound is easily contaminated, mostly by the Staphylococcus species, which creates a high risk of osteitis and bacteremia. The edges of the wound should always be biopsied to rule out local recurrence and sarcoma .
[caption id="attachment_4357" align="aligncenter" width="300"] Figure 7: Parasternal osteoradionecrosis several years after radiotherapy for breast cancer.[/caption]
Treatment, once again, is surgical, and is based upon the removal of all necrotic tissues; healthy tissue is then covered by a well-vascularized flap [66,67]. Tissue resection must be as conservative as possible, in order to limit chest wall instability, but must still remove all devascularized tissues. Larger chest wall resections must be stabilized by prosthetic titanium material, although this should be avoided whenever possible in septic conditions. When material implantation is inevitable, long-term intravenous antibiotic therapy may be necessary.
More than providing an esthetic reconstruction, the flap brings a fresh, healthy, vascular supply that heals hypoxic tissues. Great omentum flaps, gifted with a rich microvascularization as well as great anti-infective properties, are often used in this indication . Latissimus dorsi flaps are also serviceable here. Some advocate for a widespread use of free flaps: healthy tissue, harvested far from the irradiated area, with a pedicle undamaged from previous surgery or irradiation . Cutaneous perforator flaps appear to yield similar results to the gold-standard musculocutaneous flaps, and their reduced morbidity on the donor site make them a new treatment alternative . If no skin cover is possible after reconstruction, negative pressure therapy can reduce the de-epithelized area, either in a controlled wound healing strategy or before a split-thickness skin graft [11,69].
There is, unfortunately, no large-scale or long-term survival data available on osteoradionecrosis. Case series point to few postoperative complications, whatever the operative choices [38,39,67,68]; when any are reported, they are mostly flap necrosis. Yuste et al.’s 4 patient series found no recurrence with up to 6 years follow up .
4.4. The special case of Stewart-Treves syndrome
Stewart-Treves syndrome is an angiosarcoma developing on a lymphedematous territory; the invasion often reaches the chest wall. Such lymphedema results from an extensive axillary lymph node dissection, as well as adjuvant radio and chemotherapy . The pathogenesis of these peculiar sarcomas is still debated. The disease-free period is longer than that of radiation-induced sarcomas, with a mean of 11 years . Incidence is low, occurring in about 0.5% of patients 5 years after a radical mastectomy . It will probably dwindle thanks to a diminution of extensive lymph node dissection, since the sentinel lymph node technique avoids many extensive dissections.
The management of Stewart-Treves sarcoma should, ideally, be a locoregional treatment , and indeed surgery is the most commonly performed treatment . However, the previous history of radiotherapy limits both irradiation possibilities and the surgical success rate, since irradiated tissues are at a major risk of healing badly. Besides, surgical treatment can only be proposed for non-metastatic patients and only when complete resection is possible. Some use a multimodal therapy that combines surgery, reirradiation and hyperthermia therapy , seemingly with no significant difference in overall survival and local recurrence between the surgical and the non-surgical group. It is a sarcoma surgery, with a large healthy margin that often leads to amputation of the limb. Even in that somewhat best-case scenario, local recurrence is frequent (up to 96%) , and prognosis remains poor with a 5-year overall survival of 14% .
Management of locally advanced breast cancers has changed; thanks to more efficient neoadjuvant treatments, some tumors have become operable. Local recurrences and radionecrosis require a comprehensive care that is better understood than ever. Novel chest wall reconstructive techniques, dominated by titanium materials, combined with a liberal use of flaps, make it possible to perform a correct oncological surgery, with reliable functional and esthetical results. It nevertheless remains a complex therapeutic process, where strict patient selection and cooperation between surgical teams, both thoracic and plastic, are paramount to successful outcomes.
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