- Email: [email protected]
Safe Resection of the Aortic Wall Infiltrated by Lung Cancer After Placement of an Endoluminal Prosthesis
Safe Resection of the Aortic Wall Infiltrated by Lung Cancer After Placement of an Endoluminal Prosthesis
GENERAL THORACIC
Giuseppe Marulli, MD, PhD, Federico Rea, MD, Davide Zampieri, MD, Michele Antonello, MD, Giulio Maurizi, MD, Federico Venuta, MD, Camilla Poggi, MD, and Erino Angelo Rendina, MD Department of Cardiologic, Thoracic and Vascular Sciences, University of Padova, Padova; Division of Thoracic Surgery, University “Sapienza”-Sant’Andrea Hospital, Rome; Division of Thoracic Surgery, University “Sapienza,” Policlinico Umberto I, Rome; and Lorillard-Spencer-Cenci Foundation, Rome, Italy
Background. Few investigators have reported the results of combined resection of lung cancer infiltrating the thoracic aorta; only anecdotal accounts of off-label use of thoracic aortic endografts to facilitate resection of such tumors have been published. In this paper, we describe our experience using this innovative approach in terms of technical details and outcomes. Methods. We retrospectively reviewed data on 9 patients (6 men and 3 women, median age 61 years) with preoperatively suspected thoracic aorta neoplastic invasion, who were operated on after positioning of an endograft and underwent en bloc tumor resection including the aortic wall. Results. All but one cancer were non-small cell lung carcinomas; 4 patients received neoadjuvant chemotherapy, and 7 received adjuvant therapy. Aortic endografting was performed 2 to 17 days before resection of the tumor in 7 patients and as part of a one-stage procedure in 2 patients.
The proximal end of the stent graft was deployed in the aortic arch (n [ 1) or the descending aorta (n [ 8). Lung resections were left pneumonectomies in 4 patients and left lower lobectomies in 5. Five patients underwent additional buttressing of the aortic defect using a synthetic patch (n [ 2) or the omentum (n [ 3). No cardiopulmonary bypass was required. At the last follow-up, 3 patients had evidence of tumor recurrence (one local and two distant). No endograft-related complications were detected. Conclusions. Thoracic aortic endografting allowed safe en bloc resection of tumors invading the aortic wall, avoiding the need for extracorporeal circulatory support. Such an extended indication for thoracic aortic endografts seems promising and should be considered for selected oncologic cases.
T
adverse events. In 2008, we first reported the off-label use of a thoracic aorta endograft to avoid use of cardiopulmonary bypass during resection of a recurrent lung metastasis infiltrating the aortic wall [8]. In the following years, other researchers applied this technique to resection of lung cancer invading the aorta [9–12]. In the present study, we present our updated experience in the management—using aortic endografts—of thoracic tumors involving the aortic wall.
horacic aorta invasion of either primary or secondary lung tumors represents a major challenge for thoracic surgeons. In selected cases, a surgical approach may be an option, and if radical resection is accomplished, good oncologic results may be obtained [1–5]. Some investigators have described the en bloc resection of tumors that infiltrated aorta using a temporary cardiopulmonary or aortoaortic bypass, or (sometimes) direct clamping, with encouraging long-term results [1–7]. Despite advances in perioperative care and surgical techniques, the combined surgical intervention is still associated with significant morbidity and mortality. Morbidity is mostly associated with the use of extracorporeal circulation techniques causing bleeding, paraplegia, stroke, cardiac events, respiratory or renal failure, and potential systemic spread of tumor cells; these are the most common
Accepted for publication Jan 27, 2015. Address correspondence to Dr Marulli, Department of Cardiologic, Thoracic and Vascular Sciences, University of Padova, Padova, Italy; e-mail: [email protected].
Ó 2015 by The Society of Thoracic Surgeons Published by Elsevier
(Ann Thorac Surg 2015;99:1768–74) Ó 2015 by The Society of Thoracic Surgeons
Material and Methods From December 2006 to July 2014, 9 patients (6 men and 3 women, median age 61 years) with preoperatively suspected thoracic cancer invading the thoracic aorta underwent endografting followed by en bloc resection of the tumor and aortic wall in two Italian thoracic surgery units (University Hospital of Padova and University “Sapienza”-Sant’ Andrea Hospital of Rome). The study was approved by the Institutional Research Ethics Boards of the two centers, and data were retrospectively reviewed. 0003-4975/$36.00 http://dx.doi.org/10.1016/j.athoracsur.2015.01.059
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Preoperative Staging Preoperative evaluation featured computed tomography (CT) or magnetic resonance imaging (MRI) of the chest, CT or MRI of the brain, and positron emission tomography integrated with CT (PET-CT) scanning. If the mediastinal nodes showed uptake, the mediastinum was assessed by endobronchial ultrasound-guided fine-needle aspiration or cervical mediastinoscopy. Radiologic findings suggestive of aortic invasion were contact between the tumor and the aortic wall extending for more than 3 cm, obliteration of the fat plane between the aorta and the tumor, and contact by the tumor of more than 90 degrees of the aortic circumference (Fig 1). Induction chemotherapy was performed in 4 patients after multidisciplinary conferencing; this consisted of three cycles of a platinum-based combination. Restaging was performed with the aid of total body CT scans and (sometimes) PET-CT scans. Patients with mediastinal nodal involvement were considered suitable for surgery if a downstaging of the disease was obtained. Tumors were classified using the 7th edition of the TNM classification of malignant tumors [13].
Surgical Technique Before thoracic aortic endografting, CT angiography (from the supraaortic vessels to the common femoral arteries) was performed to assess vessel size and anatomy and to determine the maximum possible infiltrated aortic area; we sought to avoid risks associated with aortic branch exclusion by the endograft. When the aortic arch arteries were covered, we planned to use a fenestrated stent graft, as described by Nagata and associates [11]. All procedures were performed with patients under general anesthesia, using a retrograde femoral approach. Endografts of different brands, including Valiant (Medtronic, Minneapolis, MN), Zenith (Cook, Brisbane,
Results The operative and postoperative results are summarized in Tables 2 and 3. Pulmonary resection featured lobectomy in 5 patients, pneumonectomy in 3, and completion pneumonectomy in 1 patient. Aortic resection was limited to the adventitia in 1 case, extended to the media in 7, and to the intima in 1 (Fig 3). Reinforcement was undertaken in 5 patients; synthetic patches were used in 2 patients (Fig 4), whereas omental flaps transposed through the diaphragm were used in 3. The technique of
Table 1. Demographic and Clinical Characteristics of Study Population Pt. No.
Sex
Age (years)
1
M
61
Mild mitral regurgitation
CT
2 3 4 5 6
F M M F M
59 52 74 71 75
7 8
M F
59 63
. Arrhythmogenic cardiopathy Arterial hypertension Arterial hypertension COPD, postischemic cardiopathy, ictus cerebri Arterial hypertension Peripheral vasculopathy
9
M
60
Chronic renal failure
Comorbidity
Induction Therapy
AC ¼ adenocarcinoma; COPD ¼ chronic obstructive pulmonary disease; M ¼ male; Pt. ¼ patient; SCC ¼ squamous cell carcinoma.
Histology
cTNM
Site of Aortic Invasion
M1
Descending aorta
. . CT CT CT
Metastasis from EC AC AC AC AC SCC
T4N0M0 T4N0M0 T4N2M0 T4N1M0 T4N2M0
Descending Descending Descending Descending Descending
. .
AC AC
T4N0M0 T4N0M0
.
AC
T4N0M0
Descending aorta Aortic arch/descending aorta Descending aorta
CT ¼ chemotherapy;
EC ¼ eccrine carcinoma;
aorta aorta aorta aorta aorta
F ¼ female;
GENERAL THORACIC
Australia), Gore TAG (W.L. Gore and Associates, Flagstaff, AZ), and Relay Thoracic Endograft (Bolton Medical, Sunrise, FL), were used, upsized by 10% or less compared with the native aorta. Proximal and distal landing zones consisting of 4-cm lengths of healthy aorta were targeted to ensure adequate endograft stability. Postprocedure angiography or CT scanning, or both (Fig 2), was performed to rule out endoleaks and assure correct graft positioning. Tumor resection was performed en bloc and included resection of the involved aortic wall, lung, and eventually, the chest wall. For non-small cell lung carcinoma (NSCLC), anatomic resection plus systematic lymphadenectomy was performed. Surgical procedures were performed in one or two stages. Insertion of the thoracic aortic endograft was performed before tumor resection, which was performed en bloc in the second stage, typically a few days after aortic endograft insertion (range, 2 to 17 days), in 7 patients. In 2 patients treated more recently, a single-stage procedure was performed; endografting proceeded when intraoperative evidence of aortic infiltration was collected. In these cases, the patients were positioned in the right lateral decubitus position with the left inguinal region exposed for femoral vessels isolation. During thoracotomy, the invaded aorta was marked with clips for reference, to deploy the endograft in the best position. In this manner, it was possible to deploy the shorter endograft covering the smaller number of intercostals arteries.
Informed patient consent was obtained. The demographic and clinical characteristics of the patients are shown in Table 1.
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GENERAL THORACIC
Fig 1. Preoperative computed tomography scan showing a lung cancer invading the aortic wall (A) at the origin of the descending aorta and (B) of the descending aorta below the level of the carina.
transdiaphragmatic harvesting of the omentum through thoracotomy has been described previously [14]. No intraoperative complications were recorded, and no perioperative death occurred. Postoperative complications developed in 3 patients: 1 required a blood transfusion for anemia, 1 underwent minitracheostomy and noninvasive ventilation for acute respiratory failure, and 1 had atrial fibrillation treated with medical therapy. No second-look surgery was necessary. The median hospital stay was 10 days (range, 4 to 17). Pathology examination confirmed aortic wall invasion in 8 patients. In the remaining patient, the aortic wall was involved in a diffuse desmoplastic reaction and scar tissue had developed after induction therapy, making it impossible to intraoperatively determine if the vascular wall was infiltrated. Disease-free aortic margin resections were observed in all cases. Positive hilar nodes (N1) were found in 50% of NSCLC patients; no mediastinal nodes were involved in the disease. Adjuvant treatment was given to 7 of the 9 patients. At last follow-up (January 2015), 2 patients (22.2%) had died (one of oncologic causes and the other from an unrelated cause); 7 patients (77.8%) were alive, 2 with locoregional (lung) or distant (brain) recurrences and 5 free from relapse. No evidence of recurrence was found at the site of vascular resection. No late complication related to endograft placement was observed during follow-up. The 3-year overall survival rate was 62% (Fig 5).
Comment Thoracic tumors invading the aorta are challenging for thoracic surgeons. The vascular infiltration must be
Fig 2. Preoperative computed tomography scan showing the correct placement of the endograft (A) at the level of aortic arch (after the origin of subclavian artery) and descending aorta (sagittal view), and at the level of the descending aorta, (B) sagittal view and (C) axial view.
managed by aortic partial occlusion, resection of the aortic wall, and repair of the defect with a graft patch. That can be performed using cardiopulmonary bypass or by placing a passive shunt between the ascending and descending aorta [1–7]. The surgical mortality has been reported to range between 0% and 12.5% in various series, and major morbidities affect 7% to 23% of patients [1–7, 15, 16]. The first successful endograft insertion was reported in the early 1990s; it was used as an endovascular treatment for abdominal and thoracic aortic aneurysms [17, 18]. Today, endografts are used for aneurysm exclusion, in aortic dissection, to treat ruptures, and to treat peripheral occlusive disease. In 2008, we described the first off-label use of such endografts in a patient with a pulmonary metastasis invading the wall of the descending aorta; we performed a safe resection, avoiding the need for cardiopulmonary bypass [8]. In the time since then, other investigators [9–11] have published case reports of similarly successful experiences, and recently, Collaud and associates [12] reported a series of 5 consecutive patients with advanced NSCLC or sarcoma treated by prophylactic stent graft placement followed by aortic resection. In the cited work, resection was extended not only to the aorta but also, in 4 cases, to the chest wall and vertebral bodies. Those researchers found that the major advantage of this approach compared with open surgery was the reduced invasiveness; cardiopulmonary bypass was avoided, together with the associated anticoagulation therapy, allowing safe major en bloc resection. In addition, the endograft, excluding intercostals in the region of resection, potentially decreased intraoperative bleeding during resection of the involved vertebrae. Our series of 9 patients (almost
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Table 2. Operative Procedures Endograft Pt. No.
Type Zenith-Tx2 Valiant Captivia Relay Gore-TAG Zenith-TAG Zenith-TAG Valiant Captivia Valiant Captivia Valiant Captivia
LLL ¼ left lower lobectomy;
120 140 200 150 140 140 140 100 150
Yes No Yes Yes Yes Yes No Yes Yes
2 . 15 17 17 15 . 12 15
PN ¼ pneumonectomy;
Aortic Wall Resection Layers
Area (mm)
Aorta Reinforcement
35 35 30 20 . 40 25 50 30 45 30 35 35
. Gore-Tex patch . . Omentum Omentum . Omentum Dacron patch
Completion PN Adventitia, media PN Adventitia, media LLL Adventitia, media LLL Adventitia LLL Adventitia, media LLL Adventitia, media PN Adventitia, media PN Adventitia, media LLL Adventitia, media intima
30 45 30 30
Pt. ¼ patient.
cases, however, we adopted a one-stage procedure without any problem. The one-stage approach has potential advantages: additional anesthesia is avoided, and, more important, a useless procedure is potentially avoided if deep aortic wall invasion is shown to be absent during thoracotomy. Using this policy, we avoided unnecessary endograft positioning in our most recent 2 cases. The maximal possible extent of aortic wall resection remains unclear. In the previously cited experimental study [19], no complications were reported on resection of less than one half of the circumference. A stenosis of the aorta with proximal dilation was detected on 1-year angiography after resection of one half of the aortic circumference. As this extensive aortic wall resection had not been covered with a patch, it is unclear whether the extent of resection or the absence of a patch was responsible for aortic narrowing. No complications related to extension of the resection were observed in our study or in other studies [8–12]. Our policy is not to cover the aortic defect in instances of partial thickness resection of the aortic wall or if less than one half of the circumference is involved. The use of endografts with long (usually at least 4 cm) proximal and distal margins of uninvolved aorta is key to ensure safety and graft
all with clinical T4 NSCLC) is the largest reported in the literature. The absence of mortality and the low morbidity rate confirmed the safety of our innovative approach. Some technical points and patient selection criteria should be discussed. The optimal timing between thoracic aortic endograft insertion and aortic wall resection remains unknown. Sahasara and associates [19] investigated whether aortic stent grafting could be used to treat esophageal cancer involving the thoracic aorta. On pathologic examination, the aortic wall exhibited an inflammatory reaction, and remodeling, causing progressive graft embedment. Therefore, full-thickness aortic wall resection was considered “easier” if performed immediately after stent grafting, and “difficult” 7 days later, because of aortic wall inflammation and dense adhesions evident between the aorta and the stent graft. In the series of Collaud and associates [12], the median delay between endograft placement and the thoracic procedure was 5 days (range, 1 to 17). The cited investigators never performed aortic endografting and resection during the same anesthesia, preferring to assess patients both clinically and radiologically for potential complications of stent grafting, such as paraplegia or endoleaks, before proceeding to resection of the tumor. Our experience was similar; the delay ranged between 2 and 17 days. In 2
Table 3. Postoperative Results and Follow-Up Pt. No. 1 2 3 4 5 6 7 8 9
pTNM T4N0M0 T4N0M0 T4N1M0 T3N1M0 T4N0M0 T4N0M0 T4N1M0 T4N1M0 T4N0M0
CT ¼ chemotherapy;
Pathologic Aortic Wall Infiltration Adventitia Adventitia, Adventitia, Negative Adventitia, Adventitia Adventitia Adventitia, Adventitia,
media media media
media media intima
ICU ¼ intensive care unit;
ICU Stay Hospital (days) Stay (days) 1 4 1 0 0 2 2 0 0 Pt. ¼ patient;
12 10 6 4 8 10 17 8 8
Complications None Atrial fibrillation None None None Anemia Resp. failure None None
Resp. ¼ respiratory;
Adjuvant Follow-Up Therapy (months) Recurrence Status RT CTþRT CT . . CT CT CT CT
29 72 16 38 31 19 15 12 6
RT ¼ radiotherapy.
Systemic No No Lung Brain No No No No
Dead Alive Dead Alive Alive Alive Alive Alive Alive
GENERAL THORACIC
1 2 3 4 5 6 7 8 9
Staged Delay Length (mm) Procedure (days) Lung Resection
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Fig 3. (A) Intraoperative view of a large aortic wall resection. The descending aorta has been encircled between tourniquets above and below the invaded area to grip the endograft positioned in a one-stage procedure avoiding any displacement. (B) Intraoperative view of a deep (adventitia and media) vascular wall resection at the level of the descending aorta.
stability, avoiding the risk of endoleaks or pseudoaneurysm formation. In cases of full-thickness aortic wall resection, or resections extending for more than one half of the aortal circumference, placement of a synthetic patch or an omental flap sutured over the defect was considered prudent. An omental flap was chosen for patients considered at high risk for bronchial dehiscence, to reinforce both the aortic defect and the bronchial stump. Aortic arch involvement is a further challenge; the use of fenestrated stent grafts, as recently described by Nagata and associates [11], one of which we placed, is potentially a powerful tool when used to treat such patients. The utility of endografting when only the adventitia are infiltrated and then resected is debatable. In our experience, and that of others, only invasion of the adventitia was reported in as many as 60% of patients on pathology analysis; however, in most cases, this may be an effect of induction therapy or, in some cases, is unpredictably revealed by imaging techniques. Probably, evaluation at the time of thoracotomy of the effective need for endografting might allow a useless procedure to be avoided, and save costs. Obviously, strict coordination of and collaboration between vascular and thoracic surgeons is fundamental to avoid prolongation of operative time and development of complications. Patient selection criteria are crucial to define appropriate candidates from this subgroup. A thoracic tumor featuring infiltration of the aorta has been historically considered to be a contraindication to surgery both for technical reasons and the poor prognosis [20]. However, this view is not
Fig 4. Intraoperative view showing the buttressing of the aortic defect with (A) Gore-Tex (W.L. Gore and Associates, Inc, Flagstaff, AZ) and (B) Dacron patches (Maquet Intergard; MAQUET Holding GmbH & Co KG, Germany).
supported by clear and substantial data because of the lack of studies on the topic. In the last 20 years, several case series have shown that long-term survival is possible after limited resection of the aortic adventitia along with the primary tumor [2, 21]. Moreover, other investigators reported long-term survivorship (more than 3 years) [1–3, 5, 7] among patients with deep aortic invasion who underwent complete resection of the involved aortic wall with subsequent graft replacement. The principal recognized prognostic factors are the extent of invasion (full-layer invasion of the aortic wall increases the risk of tumor dissemination), the completeness of resection, the required type of resection, and nodal status. Thus, patient selection is the most important contributor to good long-term results. Accurate preoperative diagnosis of the extent and degree of infiltration of the aorta, and evaluation of nodal status, are essential. Aortic invasion is usually suspected on the basis of chest CT or MRI features, including contact between the tumor and the aorta extending for more than 3 cm, obliteration of the fat plane between the tumor and the aortic wall, or contact by the tumor of more than 90 degrees of the aortic circumference. In our experience, these are useful radiologic criteria for patient selection. However, the sensitivity, specificity, and accuracy of CT and MRI used to confirm invasion of the mediastinum have all been reported to be less than 90%; thus, radiologic findings on aortic infiltration may be unreliable in differentiating invasion from anatomical contiguity [22]. Similarly, differentiation between infiltration limited to the adventitia or extending to the medial or intimal layers is virtually impossible using imaging techniques. Positron
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emission tomography is mandatory for this group of patients; the ruling out of distant metastases or N2stage disease is of paramount importance. By such means, advanced procedures are reserved for patients who may benefit therefrom. Mediastinal nodal involvement has been shown to compromise long-term outcomes [1–4, 7, 21]; distant metastases commonly limit survival. Therefore, it has been suggested that operative indications should be restricted to patients of N0/1 stages [2]: this is also our policy, and in our series, no pathologic N2 involvement was evident among NSCLC patients. Of all such patients, 50% had N1 disease, and during follow-up, 25% had recurrences (one distant and one locoregional). The use of endografts for aortic resection, although reported to be safe, is not without theoretical risks; these include an additional surgical procedure, the coverage of an extensive length of the aortic lumen (usually including at least 4-cm landing zones on each end of the resection margin), and a small but real lifelong risk of erosion or infection when a stent graft is placed in an otherwise normal segment of the aorta. These potential risks must be discussed with, and accepted by, the patient. In conclusion, we found that an aortic endograft can be a useful and safe tool allowing combined resection of the lung and an infiltrated aortic wall without the need for thoracic aortal cross-clamping or graft replacement. Further studies with a large cohort of patients, and longer follow-up, are necessary to evaluate the full potential of the technique, but we believe that, for selected patients, the use of an endograft represents an appropriate or feasible option. This report also shows that coordination among specialists can yield a cohesive solution to a challenging problem.
References 1. Tsuchiya R, Asamura H, Kondo H, Goya T, Naruke T. Extended resection of the left atrium, great vessels, or both for lung cancer. Ann Thorac Surg 1994;57:960–5. 2. Fukuse T, Wada H, Hitomi S. Extended operation for nonsmall cell lung cancer invading great vessels and left atrium. Eur J Cardiothorac Surg 1997;11:664–9. 3. Klepetko W, Wisser W, Birsan T, et al. T4 lung tumors with infiltration of the thoracic aorta: is an operation reasonable? Ann Thorac Surg 1999;67:340–4.
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4. Ohta M, Hirabayasi H, Shiono H, et al. Surgical resection for lung cancer with infiltration of the thoracic aorta. J Thorac Cardiovasc Surg 2005;129:804–8. 5. Nakahara K, Ohno K, Matsumura A, et al. Extended operation for lung cancer invading the aortic arch and superior vena cava. J Thorac Cardiovasc Surg 1989;97:428–33. 6. Horita K, Itho T, Ueno T. Radical operation using cardiopulmonary bypass for lung cancer invading the aortic wall. Thorac Cardiovasc Surg 1993;41:130–2. 7. Wex P, Graeter T, Zaraca F, et al. Surgical resection and survival of patients with unsuspected single node positive lung cancer (NSCLC) invading the descending aorta. GMS Thorac Surg Sci 2009;6:Doc02. 8. Marulli G, Lepidi S, Frigatti P, Antonello M, Grego F, Rea F. Thoracic aorta endograft as an adjunct to resection of a locally invasive tumor: a new indication to endograft. J Vasc Surg 2008;47:868–70. 9. Berna P, Bagan P, De Dominicis F, Dayen C, Douadi Y, Riquet M. Aortic endostent followed by extended pneumonectomy for T4 lung cancer. Ann Thorac Surg 2011;91:591–3. 10. Roche-Nagle G, de Perrot M, Waddell TK, Oreopoulos G, Rubin BB. Neoadjuvant aortic endografting. Ann Vasc Surg 2009;23:787.e1–e5. 11. Nagata T, Nakamura Y, Yamamoto H, Sato M. A fenestrated stent graft for surgical resection of lung cancer invading the aortic arch. Thorac Cardiovasc Surg 2013;146:238–9. 12. Collaud S, Waddell TK, Yasufuku K, et al. Thoracic aortic endografting facilitates the resection of tumors infiltrating the aorta. J Thorac Cardiovasc Surg 2014;147: 1178–82. 13. Vallieres E, Shepherd FA, Crowley J, et al, for the International Association for the Study of Lung Cancer International Staging Committee and Participating Institutions. The IASLC Lung Cancer Staging Project: proposals regarding the relevance of TNM in the pathologic staging of small cell lung cancer in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol 2009;4: 1049–59. 14. D’Andrilli A, Ibrahim M, Andreetti C, Ciccone AM, Venuta F, Rendina EA. Transdiaphragmatic harvesting of the omentum through thoracotomy for bronchial stump reinforcement. Ann Thorac Surg 2009;88:212–5. 15. Misthos P, Pagagiannakis G, Kokotsakis J, Lazopoulos G, Skouteli E, Lioulias A. Surgical management of lung cancer invading the aorta or the superior vena cava. Lung Cancer 2007;56:223–7. 16. Spaggiari L, Tessitore A, Casiraghi M, et al. Survival after extended resection for mediastinal advanced lung cancer: lessons learned on 167 consecutive cases. Ann Thorac Surg 2013;95:1717–25. 17. Parodi JC, Palmaz JC, Barone HD. Transfemoral intraluminal graft implantation for abdominal aortic aneurysms. Ann Vasc Surg 1991;5:491–9. 18. Dake MD, Miller DC, Semba CP, Mitchell RS, Walker PJ, Liddell RP. Transluminal placement of endovascular stentgrafts for the treatment of descending thoracic aortic aneurysms. N Engl J Med 1994;331:1729–34. 19. Sasahara H, Sueyoshi S, Tanaka T, Fujita H, Shirouzu K. Evaluation of an aortic stent graft for use in surgery on esophageal cancer involving the thoracic aorta: experimental study. Jpn J Thorac Cardiovasc Surg 2004;52:231–9. 20. Sobin LH, Ch Wittekind. Lung and pleural tumours. International Union Against Cancer (UICC). TNM classification of malignant tumors. 5th ed. New York: John Wiley & Sons; 1997:91–100. 21. Bernard A, Bouchot O, Hagry O, Favre JP. Risk analysis and long term survival in patients undergoing resection of T4 lung cancer. Eur J Cardiothorac Surg 2001;20:344–9. 22. Munden RF, Swisher SS, Stevens CW, Stewart DJ. Imaging of the patient with non-small cell lung cancer. Radiology 2005;237:803–18.
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Fig 5. Overall survival curve. Circles indicate censored. (Pts ¼ patients.)
MARULLI ET AL ENDOGRAFTING ALLOWS SAFE AORTIC WALL RESECTION
GENERAL THORACIC
Giuseppe Marulli, MD, PhD, Federico Rea, MD, Davide Zampieri, MD, Michele Antonello, MD, Giulio Maurizi, MD, Federico Venuta, MD, Camilla Poggi, MD, and Erino Angelo Rendina, MD Department of Cardiologic, Thoracic and Vascular Sciences, University of Padova, Padova; Division of Thoracic Surgery, University “Sapienza”-Sant’Andrea Hospital, Rome; Division of Thoracic Surgery, University “Sapienza,” Policlinico Umberto I, Rome; and Lorillard-Spencer-Cenci Foundation, Rome, Italy
Background. Few investigators have reported the results of combined resection of lung cancer infiltrating the thoracic aorta; only anecdotal accounts of off-label use of thoracic aortic endografts to facilitate resection of such tumors have been published. In this paper, we describe our experience using this innovative approach in terms of technical details and outcomes. Methods. We retrospectively reviewed data on 9 patients (6 men and 3 women, median age 61 years) with preoperatively suspected thoracic aorta neoplastic invasion, who were operated on after positioning of an endograft and underwent en bloc tumor resection including the aortic wall. Results. All but one cancer were non-small cell lung carcinomas; 4 patients received neoadjuvant chemotherapy, and 7 received adjuvant therapy. Aortic endografting was performed 2 to 17 days before resection of the tumor in 7 patients and as part of a one-stage procedure in 2 patients.
The proximal end of the stent graft was deployed in the aortic arch (n [ 1) or the descending aorta (n [ 8). Lung resections were left pneumonectomies in 4 patients and left lower lobectomies in 5. Five patients underwent additional buttressing of the aortic defect using a synthetic patch (n [ 2) or the omentum (n [ 3). No cardiopulmonary bypass was required. At the last follow-up, 3 patients had evidence of tumor recurrence (one local and two distant). No endograft-related complications were detected. Conclusions. Thoracic aortic endografting allowed safe en bloc resection of tumors invading the aortic wall, avoiding the need for extracorporeal circulatory support. Such an extended indication for thoracic aortic endografts seems promising and should be considered for selected oncologic cases.
T
adverse events. In 2008, we first reported the off-label use of a thoracic aorta endograft to avoid use of cardiopulmonary bypass during resection of a recurrent lung metastasis infiltrating the aortic wall [8]. In the following years, other researchers applied this technique to resection of lung cancer invading the aorta [9–12]. In the present study, we present our updated experience in the management—using aortic endografts—of thoracic tumors involving the aortic wall.
horacic aorta invasion of either primary or secondary lung tumors represents a major challenge for thoracic surgeons. In selected cases, a surgical approach may be an option, and if radical resection is accomplished, good oncologic results may be obtained [1–5]. Some investigators have described the en bloc resection of tumors that infiltrated aorta using a temporary cardiopulmonary or aortoaortic bypass, or (sometimes) direct clamping, with encouraging long-term results [1–7]. Despite advances in perioperative care and surgical techniques, the combined surgical intervention is still associated with significant morbidity and mortality. Morbidity is mostly associated with the use of extracorporeal circulation techniques causing bleeding, paraplegia, stroke, cardiac events, respiratory or renal failure, and potential systemic spread of tumor cells; these are the most common
Accepted for publication Jan 27, 2015. Address correspondence to Dr Marulli, Department of Cardiologic, Thoracic and Vascular Sciences, University of Padova, Padova, Italy; e-mail: [email protected].
Ó 2015 by The Society of Thoracic Surgeons Published by Elsevier
(Ann Thorac Surg 2015;99:1768–74) Ó 2015 by The Society of Thoracic Surgeons
Material and Methods From December 2006 to July 2014, 9 patients (6 men and 3 women, median age 61 years) with preoperatively suspected thoracic cancer invading the thoracic aorta underwent endografting followed by en bloc resection of the tumor and aortic wall in two Italian thoracic surgery units (University Hospital of Padova and University “Sapienza”-Sant’ Andrea Hospital of Rome). The study was approved by the Institutional Research Ethics Boards of the two centers, and data were retrospectively reviewed. 0003-4975/$36.00 http://dx.doi.org/10.1016/j.athoracsur.2015.01.059
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Preoperative Staging Preoperative evaluation featured computed tomography (CT) or magnetic resonance imaging (MRI) of the chest, CT or MRI of the brain, and positron emission tomography integrated with CT (PET-CT) scanning. If the mediastinal nodes showed uptake, the mediastinum was assessed by endobronchial ultrasound-guided fine-needle aspiration or cervical mediastinoscopy. Radiologic findings suggestive of aortic invasion were contact between the tumor and the aortic wall extending for more than 3 cm, obliteration of the fat plane between the aorta and the tumor, and contact by the tumor of more than 90 degrees of the aortic circumference (Fig 1). Induction chemotherapy was performed in 4 patients after multidisciplinary conferencing; this consisted of three cycles of a platinum-based combination. Restaging was performed with the aid of total body CT scans and (sometimes) PET-CT scans. Patients with mediastinal nodal involvement were considered suitable for surgery if a downstaging of the disease was obtained. Tumors were classified using the 7th edition of the TNM classification of malignant tumors [13].
Surgical Technique Before thoracic aortic endografting, CT angiography (from the supraaortic vessels to the common femoral arteries) was performed to assess vessel size and anatomy and to determine the maximum possible infiltrated aortic area; we sought to avoid risks associated with aortic branch exclusion by the endograft. When the aortic arch arteries were covered, we planned to use a fenestrated stent graft, as described by Nagata and associates [11]. All procedures were performed with patients under general anesthesia, using a retrograde femoral approach. Endografts of different brands, including Valiant (Medtronic, Minneapolis, MN), Zenith (Cook, Brisbane,
Results The operative and postoperative results are summarized in Tables 2 and 3. Pulmonary resection featured lobectomy in 5 patients, pneumonectomy in 3, and completion pneumonectomy in 1 patient. Aortic resection was limited to the adventitia in 1 case, extended to the media in 7, and to the intima in 1 (Fig 3). Reinforcement was undertaken in 5 patients; synthetic patches were used in 2 patients (Fig 4), whereas omental flaps transposed through the diaphragm were used in 3. The technique of
Table 1. Demographic and Clinical Characteristics of Study Population Pt. No.
Sex
Age (years)
1
M
61
Mild mitral regurgitation
CT
2 3 4 5 6
F M M F M
59 52 74 71 75
7 8
M F
59 63
. Arrhythmogenic cardiopathy Arterial hypertension Arterial hypertension COPD, postischemic cardiopathy, ictus cerebri Arterial hypertension Peripheral vasculopathy
9
M
60
Chronic renal failure
Comorbidity
Induction Therapy
AC ¼ adenocarcinoma; COPD ¼ chronic obstructive pulmonary disease; M ¼ male; Pt. ¼ patient; SCC ¼ squamous cell carcinoma.
Histology
cTNM
Site of Aortic Invasion
M1
Descending aorta
. . CT CT CT
Metastasis from EC AC AC AC AC SCC
T4N0M0 T4N0M0 T4N2M0 T4N1M0 T4N2M0
Descending Descending Descending Descending Descending
. .
AC AC
T4N0M0 T4N0M0
.
AC
T4N0M0
Descending aorta Aortic arch/descending aorta Descending aorta
CT ¼ chemotherapy;
EC ¼ eccrine carcinoma;
aorta aorta aorta aorta aorta
F ¼ female;
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Australia), Gore TAG (W.L. Gore and Associates, Flagstaff, AZ), and Relay Thoracic Endograft (Bolton Medical, Sunrise, FL), were used, upsized by 10% or less compared with the native aorta. Proximal and distal landing zones consisting of 4-cm lengths of healthy aorta were targeted to ensure adequate endograft stability. Postprocedure angiography or CT scanning, or both (Fig 2), was performed to rule out endoleaks and assure correct graft positioning. Tumor resection was performed en bloc and included resection of the involved aortic wall, lung, and eventually, the chest wall. For non-small cell lung carcinoma (NSCLC), anatomic resection plus systematic lymphadenectomy was performed. Surgical procedures were performed in one or two stages. Insertion of the thoracic aortic endograft was performed before tumor resection, which was performed en bloc in the second stage, typically a few days after aortic endograft insertion (range, 2 to 17 days), in 7 patients. In 2 patients treated more recently, a single-stage procedure was performed; endografting proceeded when intraoperative evidence of aortic infiltration was collected. In these cases, the patients were positioned in the right lateral decubitus position with the left inguinal region exposed for femoral vessels isolation. During thoracotomy, the invaded aorta was marked with clips for reference, to deploy the endograft in the best position. In this manner, it was possible to deploy the shorter endograft covering the smaller number of intercostals arteries.
Informed patient consent was obtained. The demographic and clinical characteristics of the patients are shown in Table 1.
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Fig 1. Preoperative computed tomography scan showing a lung cancer invading the aortic wall (A) at the origin of the descending aorta and (B) of the descending aorta below the level of the carina.
transdiaphragmatic harvesting of the omentum through thoracotomy has been described previously [14]. No intraoperative complications were recorded, and no perioperative death occurred. Postoperative complications developed in 3 patients: 1 required a blood transfusion for anemia, 1 underwent minitracheostomy and noninvasive ventilation for acute respiratory failure, and 1 had atrial fibrillation treated with medical therapy. No second-look surgery was necessary. The median hospital stay was 10 days (range, 4 to 17). Pathology examination confirmed aortic wall invasion in 8 patients. In the remaining patient, the aortic wall was involved in a diffuse desmoplastic reaction and scar tissue had developed after induction therapy, making it impossible to intraoperatively determine if the vascular wall was infiltrated. Disease-free aortic margin resections were observed in all cases. Positive hilar nodes (N1) were found in 50% of NSCLC patients; no mediastinal nodes were involved in the disease. Adjuvant treatment was given to 7 of the 9 patients. At last follow-up (January 2015), 2 patients (22.2%) had died (one of oncologic causes and the other from an unrelated cause); 7 patients (77.8%) were alive, 2 with locoregional (lung) or distant (brain) recurrences and 5 free from relapse. No evidence of recurrence was found at the site of vascular resection. No late complication related to endograft placement was observed during follow-up. The 3-year overall survival rate was 62% (Fig 5).
Comment Thoracic tumors invading the aorta are challenging for thoracic surgeons. The vascular infiltration must be
Fig 2. Preoperative computed tomography scan showing the correct placement of the endograft (A) at the level of aortic arch (after the origin of subclavian artery) and descending aorta (sagittal view), and at the level of the descending aorta, (B) sagittal view and (C) axial view.
managed by aortic partial occlusion, resection of the aortic wall, and repair of the defect with a graft patch. That can be performed using cardiopulmonary bypass or by placing a passive shunt between the ascending and descending aorta [1–7]. The surgical mortality has been reported to range between 0% and 12.5% in various series, and major morbidities affect 7% to 23% of patients [1–7, 15, 16]. The first successful endograft insertion was reported in the early 1990s; it was used as an endovascular treatment for abdominal and thoracic aortic aneurysms [17, 18]. Today, endografts are used for aneurysm exclusion, in aortic dissection, to treat ruptures, and to treat peripheral occlusive disease. In 2008, we described the first off-label use of such endografts in a patient with a pulmonary metastasis invading the wall of the descending aorta; we performed a safe resection, avoiding the need for cardiopulmonary bypass [8]. In the time since then, other investigators [9–11] have published case reports of similarly successful experiences, and recently, Collaud and associates [12] reported a series of 5 consecutive patients with advanced NSCLC or sarcoma treated by prophylactic stent graft placement followed by aortic resection. In the cited work, resection was extended not only to the aorta but also, in 4 cases, to the chest wall and vertebral bodies. Those researchers found that the major advantage of this approach compared with open surgery was the reduced invasiveness; cardiopulmonary bypass was avoided, together with the associated anticoagulation therapy, allowing safe major en bloc resection. In addition, the endograft, excluding intercostals in the region of resection, potentially decreased intraoperative bleeding during resection of the involved vertebrae. Our series of 9 patients (almost
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Table 2. Operative Procedures Endograft Pt. No.
Type Zenith-Tx2 Valiant Captivia Relay Gore-TAG Zenith-TAG Zenith-TAG Valiant Captivia Valiant Captivia Valiant Captivia
LLL ¼ left lower lobectomy;
120 140 200 150 140 140 140 100 150
Yes No Yes Yes Yes Yes No Yes Yes
2 . 15 17 17 15 . 12 15
PN ¼ pneumonectomy;
Aortic Wall Resection Layers
Area (mm)
Aorta Reinforcement
35 35 30 20 . 40 25 50 30 45 30 35 35
. Gore-Tex patch . . Omentum Omentum . Omentum Dacron patch
Completion PN Adventitia, media PN Adventitia, media LLL Adventitia, media LLL Adventitia LLL Adventitia, media LLL Adventitia, media PN Adventitia, media PN Adventitia, media LLL Adventitia, media intima
30 45 30 30
Pt. ¼ patient.
cases, however, we adopted a one-stage procedure without any problem. The one-stage approach has potential advantages: additional anesthesia is avoided, and, more important, a useless procedure is potentially avoided if deep aortic wall invasion is shown to be absent during thoracotomy. Using this policy, we avoided unnecessary endograft positioning in our most recent 2 cases. The maximal possible extent of aortic wall resection remains unclear. In the previously cited experimental study [19], no complications were reported on resection of less than one half of the circumference. A stenosis of the aorta with proximal dilation was detected on 1-year angiography after resection of one half of the aortic circumference. As this extensive aortic wall resection had not been covered with a patch, it is unclear whether the extent of resection or the absence of a patch was responsible for aortic narrowing. No complications related to extension of the resection were observed in our study or in other studies [8–12]. Our policy is not to cover the aortic defect in instances of partial thickness resection of the aortic wall or if less than one half of the circumference is involved. The use of endografts with long (usually at least 4 cm) proximal and distal margins of uninvolved aorta is key to ensure safety and graft
all with clinical T4 NSCLC) is the largest reported in the literature. The absence of mortality and the low morbidity rate confirmed the safety of our innovative approach. Some technical points and patient selection criteria should be discussed. The optimal timing between thoracic aortic endograft insertion and aortic wall resection remains unknown. Sahasara and associates [19] investigated whether aortic stent grafting could be used to treat esophageal cancer involving the thoracic aorta. On pathologic examination, the aortic wall exhibited an inflammatory reaction, and remodeling, causing progressive graft embedment. Therefore, full-thickness aortic wall resection was considered “easier” if performed immediately after stent grafting, and “difficult” 7 days later, because of aortic wall inflammation and dense adhesions evident between the aorta and the stent graft. In the series of Collaud and associates [12], the median delay between endograft placement and the thoracic procedure was 5 days (range, 1 to 17). The cited investigators never performed aortic endografting and resection during the same anesthesia, preferring to assess patients both clinically and radiologically for potential complications of stent grafting, such as paraplegia or endoleaks, before proceeding to resection of the tumor. Our experience was similar; the delay ranged between 2 and 17 days. In 2
Table 3. Postoperative Results and Follow-Up Pt. No. 1 2 3 4 5 6 7 8 9
pTNM T4N0M0 T4N0M0 T4N1M0 T3N1M0 T4N0M0 T4N0M0 T4N1M0 T4N1M0 T4N0M0
CT ¼ chemotherapy;
Pathologic Aortic Wall Infiltration Adventitia Adventitia, Adventitia, Negative Adventitia, Adventitia Adventitia Adventitia, Adventitia,
media media media
media media intima
ICU ¼ intensive care unit;
ICU Stay Hospital (days) Stay (days) 1 4 1 0 0 2 2 0 0 Pt. ¼ patient;
12 10 6 4 8 10 17 8 8
Complications None Atrial fibrillation None None None Anemia Resp. failure None None
Resp. ¼ respiratory;
Adjuvant Follow-Up Therapy (months) Recurrence Status RT CTþRT CT . . CT CT CT CT
29 72 16 38 31 19 15 12 6
RT ¼ radiotherapy.
Systemic No No Lung Brain No No No No
Dead Alive Dead Alive Alive Alive Alive Alive Alive
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1 2 3 4 5 6 7 8 9
Staged Delay Length (mm) Procedure (days) Lung Resection
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Fig 3. (A) Intraoperative view of a large aortic wall resection. The descending aorta has been encircled between tourniquets above and below the invaded area to grip the endograft positioned in a one-stage procedure avoiding any displacement. (B) Intraoperative view of a deep (adventitia and media) vascular wall resection at the level of the descending aorta.
stability, avoiding the risk of endoleaks or pseudoaneurysm formation. In cases of full-thickness aortic wall resection, or resections extending for more than one half of the aortal circumference, placement of a synthetic patch or an omental flap sutured over the defect was considered prudent. An omental flap was chosen for patients considered at high risk for bronchial dehiscence, to reinforce both the aortic defect and the bronchial stump. Aortic arch involvement is a further challenge; the use of fenestrated stent grafts, as recently described by Nagata and associates [11], one of which we placed, is potentially a powerful tool when used to treat such patients. The utility of endografting when only the adventitia are infiltrated and then resected is debatable. In our experience, and that of others, only invasion of the adventitia was reported in as many as 60% of patients on pathology analysis; however, in most cases, this may be an effect of induction therapy or, in some cases, is unpredictably revealed by imaging techniques. Probably, evaluation at the time of thoracotomy of the effective need for endografting might allow a useless procedure to be avoided, and save costs. Obviously, strict coordination of and collaboration between vascular and thoracic surgeons is fundamental to avoid prolongation of operative time and development of complications. Patient selection criteria are crucial to define appropriate candidates from this subgroup. A thoracic tumor featuring infiltration of the aorta has been historically considered to be a contraindication to surgery both for technical reasons and the poor prognosis [20]. However, this view is not
Fig 4. Intraoperative view showing the buttressing of the aortic defect with (A) Gore-Tex (W.L. Gore and Associates, Inc, Flagstaff, AZ) and (B) Dacron patches (Maquet Intergard; MAQUET Holding GmbH & Co KG, Germany).
supported by clear and substantial data because of the lack of studies on the topic. In the last 20 years, several case series have shown that long-term survival is possible after limited resection of the aortic adventitia along with the primary tumor [2, 21]. Moreover, other investigators reported long-term survivorship (more than 3 years) [1–3, 5, 7] among patients with deep aortic invasion who underwent complete resection of the involved aortic wall with subsequent graft replacement. The principal recognized prognostic factors are the extent of invasion (full-layer invasion of the aortic wall increases the risk of tumor dissemination), the completeness of resection, the required type of resection, and nodal status. Thus, patient selection is the most important contributor to good long-term results. Accurate preoperative diagnosis of the extent and degree of infiltration of the aorta, and evaluation of nodal status, are essential. Aortic invasion is usually suspected on the basis of chest CT or MRI features, including contact between the tumor and the aorta extending for more than 3 cm, obliteration of the fat plane between the tumor and the aortic wall, or contact by the tumor of more than 90 degrees of the aortic circumference. In our experience, these are useful radiologic criteria for patient selection. However, the sensitivity, specificity, and accuracy of CT and MRI used to confirm invasion of the mediastinum have all been reported to be less than 90%; thus, radiologic findings on aortic infiltration may be unreliable in differentiating invasion from anatomical contiguity [22]. Similarly, differentiation between infiltration limited to the adventitia or extending to the medial or intimal layers is virtually impossible using imaging techniques. Positron
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emission tomography is mandatory for this group of patients; the ruling out of distant metastases or N2stage disease is of paramount importance. By such means, advanced procedures are reserved for patients who may benefit therefrom. Mediastinal nodal involvement has been shown to compromise long-term outcomes [1–4, 7, 21]; distant metastases commonly limit survival. Therefore, it has been suggested that operative indications should be restricted to patients of N0/1 stages [2]: this is also our policy, and in our series, no pathologic N2 involvement was evident among NSCLC patients. Of all such patients, 50% had N1 disease, and during follow-up, 25% had recurrences (one distant and one locoregional). The use of endografts for aortic resection, although reported to be safe, is not without theoretical risks; these include an additional surgical procedure, the coverage of an extensive length of the aortic lumen (usually including at least 4-cm landing zones on each end of the resection margin), and a small but real lifelong risk of erosion or infection when a stent graft is placed in an otherwise normal segment of the aorta. These potential risks must be discussed with, and accepted by, the patient. In conclusion, we found that an aortic endograft can be a useful and safe tool allowing combined resection of the lung and an infiltrated aortic wall without the need for thoracic aortal cross-clamping or graft replacement. Further studies with a large cohort of patients, and longer follow-up, are necessary to evaluate the full potential of the technique, but we believe that, for selected patients, the use of an endograft represents an appropriate or feasible option. This report also shows that coordination among specialists can yield a cohesive solution to a challenging problem.
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Fig 5. Overall survival curve. Circles indicate censored. (Pts ¼ patients.)
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