Use of Pleura, Azygos Vein, Pericardium, and Muscle Flaps in Tracheobronchial Surgery

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1 Use of Pleura, Azygos Vein, Pericardium, and Muscle Flaps in Tracheobronchial Surgery Timothy M. Anderson, MD, and Joseph I. Miller, Jr, MD Department of Cardiothoracic Surgery,, Emory University School of Medicine, The Emory Clinic, Atlanta, Georgia Desmoplastic reactions secondary to adjuvant chemotherapy and radiation in stage IliA lung cancer, plus advances in complex tracheobronchial surgery, have rejuvenated an interest for augmenting bronchial coverage and suture line reinforcement. We present the techniques and applications of harvesting pleural, azygos vein, pericardial flaps, and fat pad grafts, and intrathoracic transposition of chest wall muscle flaps. (Ann Thorac Surg 1995;60:729-33) p rogress in complex tracheobronchial surgery and combined therapy for stage IIIA lung cancer have reawakened an interest in protection of bronchial s and suture lines [1-3]. Although pleural and pericardial patches have been used with success, their counterpart flaps are preferable because they carry their own blood supply and are less prone to shrinkage and fibrosis [4, 5]. The pleural flap, when augmented with azygos vein, creates an effective reinforcement for the right hilar region [1]. Pericardial flaps are highly desirable, being thicker than pleura, and also carry with them an inherent blood supply [6, 7]. Ideally, pericardial fat pad grafts are employed, which have the added benefit of a more constant blood supply and follow-up data to support their long-term durability [81. Pericardiophrenic pedicles serve as a viable alternative to pericardial fat pad grafts when sacrifice of the phrenic nerve is necessary [8]. The use of serratus anterior and latissimus dorsi muscle flaps has greatly added to bronchial reinforcement in complex tracheobronchial reinforcement and reconstruction. Because of renewed interest, we present the indications, techniques, and applications of each flap and graft (Table 1). Pleural Flaps Pleural flaps were first described to reinforce the bronchial after pneumonectomy by Reinhoff and associates [9] in 1942, and after lobectomy by Sweet [10] in 1945, because of the high incidence of bronchopleural. Pleural flaps have also been placed between the bronchial anastomosis and pulmonary artery in sleeve lobectomy [1]. In repair of recurrent tracheoesophageal, pleural flaps were initially used as an interposition flap between esophageal and tracheal closures; later they were abandoned in favor of pericardial flaps due to Address reprint requests to Dr Miller, Department of Cardiothoracic Surgery, The Emo D' Clinic, 25 Prescott St, Suite 3420, Atlanta, GA high recurrence rates [11]. We have employed pleural flaps in a few tracheal resections [12]. Pleural flaps have been used to reinforce the esophageal suture line in both spontaneous rupture and traumatic injury of the esophagus [13, 14]. The pleura has been incorporated with intercostal muscle and periosteum as a composite flap for repair of esophagobronchopleural and oropharyngeal reconstruction [15, 16]. The technique for harvesting pleural flaps is as follows (Fig 1). Through a left posterolateral thoracotomy, the pleura is incised in a triangular fashion with the base of the flap one third the width of the distal flap. Using forceps to lift the edges of the pleura, a plane is gently dissected under the parietal pleura to its base just adjacent to the bronchial. Then the flap is folded over 180 degrees and the corners are tacked to neighboring peribronchial tissue with 4-0 interrupted Vicryl (Ethicon, Somerville, NJ), in this case over the left pneumonectomy. Azygos Vein Stump The azygos vein can be used as an alternative to a pleural flap in a right pneumonectomy. On the left, the pneumonectomy retracts behind the aorta, and does not require bolstering. The technique for harvesting an azygos vein with pleural flap is illustrated in Figure 2. Through a right posterolateral thoracotomy the pleura overlying the azygos vein is freed from anteriorly over the superior vena caval region. The azygos vein is then mobilized and ligated anteriorly and at the proximal base with 0 silk suture. Then the vein is divided anteriorly just proximal to the silk tie and split longitudinally along its undersurface to fold the endothelial side over the bronchial. The overlying pleura is swung over together with the vein if desired and tacked into the adjacent pleura and peribronchial tissues to secure the vein/pleural flap over the pneumonectomy. Pericardial Flaps Pericardial flaps are preferred for repair of recurrent tracheoesophageal s [11, 17[. Other uses include repair in sleeve lobectomy, and as a flap-plasty for the tracheal anastomosis in heart-lung transplantation [1, 18]. We prefer a double-layered pericardial flap between the tracheal anastomosis and innominate vessels during tracheal resections [12]. Pericardium has been used to repair congenital tracheal and esophageal steno by The Society of Thoracic Surgeons /95]$ (95)00500-K

2 730 REVIEW ANDERSON AND MII_I.ER Ann Thorac Surg THO1LACIC GRAFTS AND FLAPS 1995;60: Table 1. indication and Application of Various Flaps and Grafts Type of flap/graft Indication Application Pleural Lobectomy Pneumonectomy Sleeve lobectomv Prevent Tracheal resection Prevent TE Repair TE Spontaneous Reinforce esophageal esophageal rupture suture line Traumatic Reinforce esophageal esophageal inju D' suture line Azygos vein Pneulnonectomv Pericardial Recurrent TE Repair TE Sleeve lobectomv Pericardial fat pad Pericardiophrenic Muscle TE = tracheoesophageal. Tracheal resection Heart-lung transplantation Congenital tracheal Esophageal Lobectomy Lobectom v Lobectomv Prevent Prevent Tracheal flap-plasty Repair congenital tracheal Repair esophageal sis [6, 81. Extended pneumonectomies with carinal resection have been sealed with combined pericardium/ polytetrafluoroethylene [19]. Pericardial flaps have also been used in tracheal reconstruction combined with Marlex mesh repair [20]. The technique for harvesting a pericardial flap is as shown in Figure 3. Through a right lateral thoracotomy, the parietal pleura is entered and the azygos vein is doubly ligated and divided. Once the tracheal anastomo- Pericardiophrenic. vessels Fig 1. Pleural flap folded 180 degrees to cover left pneumonectomy. sis is completed, the pericardium is incised along its lateral aspect, care being taken not to injure the underlying heart or pericardiophrenic nerve and vessels. The pericardium is then swung superiorly and posteriorly to wrap around the trachea and is tacked to itself, thus reinforcing the suture line. In addition, the flap also serves to prevent. The remaining pericardial defect does not require closure with bovine pericardium unless a pneumonectomy is performed. Pericardial Fat Pad Graft Pedicled pericardial fat pad graft was devised initially out of an attempt to reinforce a torn bronchus after pulmonary resection by Brewer and associates [8] in 1953, and has been employed since as an adjunct to prevent bronchopleural after lobectomy or pneumonectomy [211. The methods for harvesting the pedicled pericardial fat grafts are shown in Figure 4. The anterior-inferior peri- SVC AtZYmgp/plan ral d ivied posteriorly " Fig 2. Azygos vein for right pneumonectomy reinforcement. (SVC = superior vena cava.)

3 Ann Thorac Surg REVIEW ANDERSON AND MILLER ;60: THORACIC GRAFTS AND FLAPS Pericardial flap / - Innominate --veto. /... z Tracheal suture lin a c - rdio vesse,s i, 'N Anterior - superior Superior pericardiat fat graft P rer inchd i al / _ I M :cardlo,t\... ' -.. Fig 3. Pericardial flap wrapped around tracheal resection anastomotic site adjacent to innominate vessels. cardial fat pad graft is based on the middle pericardial and musculophrenic branches of the internal mammary artery. The mediastinal pleura is incised along the periphery of the graft. Then the pedicle is freed up off the pericardium. The anastomotic vessels to the pericardiophrenic branch anteriorly, and tributary between the middle pericardial branch and musculophrenic artery inferiorly, are divided. The pedicle consisting of overlying mediastinal pleura, blood vessels, and adipose tissue is then gently turned up to the bronchial. Using 4-0 interrupted Vicryl sutures, the end of the graft is meticulously fixed to the overlying bronchial tissues to form a caplike closure over the bronchial end, and the pedicle is reinforced with tacking sutures to the mediastinum more proximally. This graft works well for pneumonectomy s or remnant of middle or lower lobe bronchi. An alternative and somewhat shorter graft can be derived by an anterior-superior pericardial fat pad graft (Fig 5), where the blood supply is mainly from the Middle Anterior - inferior pericardial pericardial fat graft branch / Fig 5. Anterior-superior pericardial fat pad graft to cover right main bronchus. (IMA internal mammary, artery.) superior pericardial branch of the internal mammary artery and anterior mediastinal vessels. The pedicle is developed in a similar fashion to the anterior-inferior graft and is useful to cover the of a main bronchus or upper lobe bronchus. Pedicled Pericardiophrenic Graft A potential alternative with a pneumonectomy patient, or when the phrenic nerve requires sacrifice, is to use the pedicled pericardiophrenic graft as first advocated by Brewer and associates [8]. This technique has been used to reinforce the right pneumonectomy with success (Pellet JR, personal communication). The technique of harvesting this graft is as follows (Fig 6). The parietal pleura, phrenic nerve, and accompanying adipose tissue surrounding the pericardiophrenic vessels Pericardiophrenic g r a f t c u l o p h r e n i c r r d l l vesselperica p hre nic Right main.,. Fig 4. Anterior-inferior pericardial ti# pad graft to cover right middie and lower lobectomy sites. (1MA : internal mammary artery.) Fig 6, Pericardiophrenic pedicle grfffi to cover right main bronchus.

4 732 REVIEW ANDERSON AND MILLER Ann Thorac Surg THORACIC GRAFTS AND FLAPS 1995;60: \ Lateral thoracic. artery rtery i " Latiss, us dorsi mosc,e Serratus anterior muscle Fig 7. Blood supply to serrahls anterior amt latissimus dorsi muscles. are freed, beginning at the most inferior aspect of the structure. The phrenic nerve and vessels are divided above the diaphragm, then the pedicle is swung posteriorly over the pneumonectomy or lobar bronchial. It is then attached to the in a manner similar to that of the pericardial fat pad graft with interrupted Vicryl sutures. This graft has variable amounts of adipose tissue and occasionally the accompanying fat is too scant for a suitable pedicle. The remaining pericardial defect is closed with a nonabsorbable patch to prevent cardiac herniation in the pneumonectomy patient. Serratus Anterior and Latissimus Dorsi Muscle Flaps Recent use of muscle flaps has greatly added to reinforcement of bronchial s in complex tracheobronchial operations [22]. The serratus anterior and latissimus dorsi muscles can be easily harvested and applied as intrathoracic transposition flaps. The method for harvesting the serratus anterior muscle is shown in Figure 7. The anterior and inferior insertions of the muscle are freed up off the rib cage with boyle cauted'. The muscle is then lifted away from the chest wall in large part with blunt finger dissection, care being taken not to injure the pedicle supplied by the lateral thoracic artery. Then the posterior aspect of the muscular origin is divided off the medial aspect of the scapula. Through a second rib resection site (Fig 8), the muscle can be carefully transposed intrathoracically and secured over the bronchial with Vicryl stay sutures. Viability can be assessed with the use of Doppler recordings. The latissimus dorsi muscle is also used as a transposition flap for bronchial reinforcement or wrapping tracheobronchial anastomoses when serratus anterior muscle is unavailable. Harvesting the latissimus dorsi muscle is as follows (see Fig 7). The muscle is divided along its periphery starting anteriorly off the lower ribs, inferiorly from the iliac crest, and posteriorly from the thoracolumbar fascia. The muscle is then lifted off the chest wall using blunt dissection from distally to proximally, care being taken not to injure the base of the pedicle supplied by the thoracodorsal artery and vein. The muscle transposition flap is either placed intrathoracically through a small second or third rib resection site, or placed through the thoracotomy incision directly and secured over the bronchial with Vicryl stay sutures. Comment Pleural flaps have found limited usefulness in the thoracic cavity in part due to their thin, delicate nature and better alternatives. Pericardium has a greater variety of uses in the chest, and is not prone to shrinkage [23, 24]. The pedicled pericardial graft has the advantage of its own blood supply, and is autologous compared with synthetic materials. It can serve to isolate and reduce abrasion between tracheobronchial, vascular, and esophageal suture lines, thus preventing formation, and can aid in sealing leaks from suture lines [1, 17]. In the event of an esophageal leak, the pedicle may act as a template for ingrowth of esophageal neomucosa [17]. Experimental work also shows that replacement of tracheobronchial defects with pericardial patches become lined with respiratory epithelium [23]. Either pericardial or muscle flaps are useful in preventing erosion of the innominate artery from primary tracheal anastomotic sites ]25]. Pedicled pericardial fat pad grafts to reinforce bronchial closure in pulmonary resections have been followed up in both animals and humans. Grafts kept bronchi closed and prevented bronchial s in all instances after lobectomy or pneumonectomy in dogs. In addition, autopsy findings showed that grafts appeared grossly viable and fixed to the bronchial up to a year postoperatively. Similarly, human postmortem examina- muscle Fig 8. Serratus anterior muscle brought through second rib intercostal space to reinforce left pneumonectomy site.

5 Ann Thorac Surg REVIEW ANDERSON AND MILLER 733 "1995;60: THORACIC GRAFTS AND FLAPS tion has shown intact, viable graft reinforcing the bronchial as long as 2 years 9 months postoperatively lsj. The pericardiophrenic pedicle serves as an acceptable alternative to pericardial fat graft when sacrifice of the phrenic nerve is warranted and the amount of surrounding adipose is sufficient. Finally, use of muscle flaps has greatly added to reinforcement of bronchial s in the management of thoracic problems. These various techniques described should be a part of every general thoracic surgeon's armamentarium. References 1. Weisel RD, Cooper JD, Delarue NC, et al. Sleeve lobectomy for carcinoma of the lung. J Thorac Cardiovasc Surg 1979;78: Ishihara T, Ikeda T, Inoue H, et al. Resection of cancer of lung and carina. J Thorac Cardiovasc Surg 1977;73: Rusch VW, Albain KS, Crowley JJ, et al. Surgical resection of stage IIIA and stage [IIB non-small-cell lung cancer after concurrent induction chemoradiotherapy: a Southwest Oncology Group trial. J Thorac Cardiovasc Surg 1993;105: Idriss FS, DeLeon SY, llbawi MN, et al. Tracheoplasty with pericardial patch for extensive tracheal in infants and children. J Thorac Cardiovasc Surg 1984;88: Coran AG. Pericardioesophagoplasty: a new operation for partial esophageal replacement. Am J Surg 1973;125: Vidne B, Levy MJ. Use of pericardium for esophagoplasty in congenital esophageal. Surge D' 1970;68: Grav H, Goss CM, eds. Anatomy of the human body. Philadelphia: Lea & Febiger, 1973:542, Brewer LA, King EL, Lilly LJ, et al. Bronchial closure in pulmonary, resection: a clinical and experimental study using a pedicled perieardial fat graft reinforcement. J Ttorac Cardiovascular Surg 1953;26: Reinhoff WF, Gannon J, Sherman 1. Closure of the bronchus following total pneumonectorny. Ann Surg 1942;116: Sweet RH. Closure of the bronchial following lobectomy or pneumonectomy. Surgery 1945;18: Wheatley MJ, Coran AG. Pericardial flap interposition for the definitive management of recurrent tracheoesophageal. J Pediatr Surg 1992;27: Mansour KA, Lee RB, Miller JI Jr. Tracheal resections: lessons learned. Ann Thorac Surg 1994;57: Justicz AG, Symbas PN. Spontaneous rupture of the esophagus: immediate and late results. Am Surg 1991;57: Hood RM, Boyd AD, Culliford AT. Thoracic trauma. Philadelphia: Saunders, 1989: Sano T, Naruke T, Watanabe H, et al. An esophagobronchopleural successfully treated by a surgical procedure combined with conservative therapy after resection for lung cancer. Jpn J Clin Oncol 1989;19: Stromberg BV. The pleural osteomuscular flap in oropharyngeal reconstruction. Laryngoscope 1989;99: Botham MJ, Coran AG. The use of pericardium for the management of recurrent tracheoesophageal. J Pediatr Surg 1986;21: Haverich A, Frimpong-Boateng K, Wahlers T, et al. Pericardial flap-plasty for protection of the tracheal anastomosis in heart-lung transplantation. J Cardiac Surg 1989;4: Hasse J. Patch-closure of tracheal defects with pericardium/ PTFE: a new technique in extended pneumonectomy with carinal resection. Eur J Cardiothorac Surg 1990;4: Moghissi K. Tracheal reconstruction with a prosthesis of Marlex mesh and pericardium. J Thorac Cardiovasc Surg 1975;69: Icenogle TB, Levinson MW, Copeland JG, et al. Use of pericardial fat pad flap to prevent bronchopleural. Ann Thorac Surg 1986;42: Miller JI. In: Peters RM, Toledo J, eds. Current topics in general thoracic surge: an international series. Vol 2: Perioperative care. Amsterdam: Elsevier, 1992: Guyton RA, Dorsey LM, Silberman MS, et al. The broadly based pericardial flap: a tissue for atrial wall replacement that grows. J Thorac Cardiovasc Surg 1984;87: BD, ant LR, Eiseman B. Replacement of tracheobronchial defects with autogenous pericardium. J Thorac Cardiovasc Surg 1964;48: Pearson FG, Thompson DW, Weissberg D, Simpson WJK, Kergin FG. Adenoid cystic carcinoma of the trachea. Experience with 16 patients managed by tracheal resection. Ann Thorac Surg 1974;18:16-29.

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