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Ann Thorac Surg 1995;60:729-733
© 1995 The Society of Thoracic Surgeons

Current Review

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

Timothy M. Anderson, MD, Joseph I. Miller, Jr, MD

Department of Cardiothoracic Surgery, Emory University School of Medicine, The Emory Clinic, Atlanta, Georgia


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 
Desmoplastic reactions secondary to adjuvant chemotherapy and radiation in stage IIIA lung cancer, plus advances in complex tracheobronchial surgery, have rejuvenated an interest for augmenting bronchial stump 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.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 
Progress in complex tracheobronchial surgery and combined therapy for stage IIIA lung cancer have reawakened an interest in protection of bronchial stumps 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 [8]. 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 stump reinforcement in complex tracheobronchial reinforcement and reconstruction. Because of renewed interest, we present the indications, techniques, and applications of each flap and graft (Table 1Go).


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  		Table 1. . Indication and Application of Various Flaps and Grafts
 

   Pleural Flaps
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 
Pleural flaps were first described to reinforce the bronchial stump after pneumonectomy by Reinhoff and associates [9] in 1942, and after lobectomy by Sweet [10] in 1945, because of the high incidence of bronchopleural fistula. Pleural flaps have also been placed between the bronchial anastomosis and pulmonary artery in sleeve lobectomy [1]. In repair of recurrent tracheoesophageal fistula, 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 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 fistula and oropharyngeal reconstruction [15, 16].

The technique for harvesting pleural flaps is as follows (Fig 1Go). 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 stump. 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 stump.



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  		Fig 1. . Pleural flap folded 180 degrees to cover left pneumonectomy.

 

   Azygos Vein Stump
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 
The azygos vein stump can be used as an alternative to a pleural flap in a right pneumonectomy. On the left, the pneumonectomy stump retracts behind the aorta, and does not require bolstering.

The technique for harvesting an azygos vein stump with pleural flap is illustrated in Figure 2Go. 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 stump. 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 stump.



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  		Fig 2. . Azygos vein stump for right pneumonectomy reinforcement. (SVC = superior vena cava.)

 

   Pericardial Flaps
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 
Pericardial flaps are preferred for repair of recurrent tracheoesophageal fistulas [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 stenosis and esophageal stenosis [6, 8]. 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 3Go. Through a right lateral thoracotomy, the parietal pleura is entered and the azygos vein is doubly ligated and divided. Once the tracheal anastomosis 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 bronchovascular fistula. The remaining pericardial defect does not require closure with bovine pericardium unless a pneumonectomy is performed.



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  		Fig 3. . Pericardial flap wrapped around tracheal resection anastomotic site adjacent to innominate vessels.

 

   Pericardial Fat Pad Graft
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 
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 fistula after lobectomy or pneumonectomy [21].

The methods for harvesting the pedicled pericardial fat grafts are shown in Figure 4Go. The anterior-inferior pericardial 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 stump. 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 stumps or remnant of middle or lower lobe bronchi.



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  		Fig 4. . Anterior-inferior pericardial fat pad graft to cover right middle and lower lobectomy sites. (IMA = internal mammary artery.)

 
An alternative and somewhat shorter graft can be derived by an anterior-superior pericardial fat pad graft (Fig 5Go), where the blood supply is mainly from the 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 stump of a main bronchus or upper lobe bronchus.



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  		Fig 5. . Anterior-superior pericardial fat pad graft to cover right main bronchus. (IMA = internal mammary artery.)

 

   Pedicled Pericardiophrenic Graft
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
Serratus Anterior and Latissimus...
 Comment
 References
 
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 stump with success (Pellet JR, personal communication).

The technique of harvesting this graft is as follows (Fig 6Go). The parietal pleura, phrenic nerve, and accompanying adipose tissue surrounding the pericardiophrenic vessels 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 stump. It is then attached to the stump 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.



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  		Fig 6. . Pericardiophrenic pedicle graft to cover right main bronchus.

 

   Serratus Anterior and Latissimus Dorsi Muscle Flaps
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
Comment
 References
 
Recent use of muscle flaps has greatly added to reinforcement of bronchial stumps 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 7Go. The anterior and inferior insertions of the muscle are freed up off the rib cage with bovie cautery. 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 8Go), the muscle can be carefully transposed intrathoracically and secured over the bronchial stump with Vicryl stay sutures. Viability can be assessed with the use of Doppler recordings.



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  		Fig 7. . Blood supply to serratus anterior and latissimus dorsi muscles.

 


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  		Fig 8. . Serratus anterior muscle brought through second rib intercostal space to reinforce left pneumonectomy site.

 
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 7Go). 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 stump with Vicryl stay sutures.


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
References
 
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 fistula 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 fistulas in all instances after lobectomy or pneumonectomy in dogs. In addition, autopsy findings showed that grafts appeared grossly viable and fixed to the bronchial stump up to a year postoperatively. Similarly, human postmortem examination has shown intact, viable graft reinforcing the bronchial stump as long as 2 years 9 months postoperatively [8].

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 stumps in the management of thoracic problems. These various techniques described should be a part of every general thoracic surgeon's armamentarium.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 
Address reprint requests to Dr Miller, Department of Cardiothoracic Surgery, The Emory Clinic, 25 Prescott St, Suite 3420, Atlanta, GA 30308.


   References
Top
 Footnotes
 Abstract
 Introduction
 Pleural Flaps
 Azygos Vein Stump
 Pericardial Flaps
 Pericardial Fat Pad Graft
 Pedicled Pericardiophrenic Graft
 Serratus Anterior and Latissimus...
 Comment
 References
 

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  4. Idriss FS, DeLeon SY, Ilbawi MN, et al. Tracheoplasty with pericardial patch for extensive tracheal stenosis in infants and children. J Thorac Cardiovasc Surg 1984;88:527–36.[Abstract]
  5. Coran AG. Pericardioesophagoplasty: a new operation for partial esophageal replacement. Am J Surg 1973;125:294–9.[Medline]
  6. Vidne B, Levy MJ. Use of pericardium for esophagoplasty in congenital esophageal stenosis. Surgery 1970;68:389–92.[Medline]
  7. Gray H, Goss CM, eds. Anatomy of the human body. Philadelphia: Lea & Febiger, 1973:542, 1137.
  8. Brewer LA, King EL, Lilly LJ, et al. Bronchial closure in pulmonary resection: a clinical and experimental study using a pedicled pericardial fat graft reinforcement. J Thorac Cardiovascular Surg 1953;26:507–32.
  9. Reinhoff WF, Gannon J, Sherman I. Closure of the bronchus following total pneumonectomy. Ann Surg 1942;116:481–531.[Medline]
  10. Sweet RH. Closure of the bronchial stump following lobectomy or pneumonectomy. Surgery 1945;18:82–4.
  11. Wheatley MJ, Coran AG. Pericardial flap interposition for the definitive management of recurrent tracheoesophageal fistula. J Pediatr Surg 1992;27:1122–6.[Medline]
  12. Mansour KA, Lee RB, Miller JI Jr. Tracheal resections: lessons learned. Ann Thorac Surg 1994;57:1120–5.[Abstract]
  13. Justicz AG, Symbas PN. Spontaneous rupture of the esophagus: immediate and late results. Am Surg 1991;57:4–7.[Medline]
  14. Hood RM, Boyd AD, Culliford AT. Thoracic trauma. Philadelphia: Saunders, 1989:307.
  15. Sano T, Naruke T, Watanabe H, et al. An esophagobroncho-pleural fistula successfully treated by a surgical procedure combined with conservative therapy after resection for lung cancer. Jpn J Clin Oncol 1989;19:402–8.[Abstract/Free Full Text]
  16. Stromberg BV. The pleural osteomuscular flap in oropharyngeal reconstruction. Laryngoscope 1989;99:339–41.[Medline]
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  18. 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;4:136–9.[Medline]
  19. Hasse J. Patch-closure of tracheal defects with pericardium/PTFE: a new technique in extended pneumonectomy with carinal resection. Eur J Cardiothorac Surg 1990;4:412–6.[Abstract]
  20. Moghissi K. Tracheal reconstruction with a prosthesis of Marlex mesh and pericardium. J Thorac Cardiovasc Surg 1975;69:499–506.[Abstract]
  21. Icenogle TB, Levinson MW, Copeland JG, et al. Use of pericardial fat pad flap to prevent bronchopleural fistula. Ann Thorac Surg 1986;42:216–7.[Abstract]
  22. Miller JI. In: Peters RM, Toledo J, eds. Current topics in general thoracic surgery: an international series. Vol 2: Perioperative care. Amsterdam: Elsevier, 1992:355--365.
  23. 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;87:619–25.[Abstract]
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Ann. Thorac. Surg., October 1, 1996; 62(4): 1033 - 1037.
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E. A. Rendina, F. Venuta, T. De Giacomo, C. Ricci, and J. I. Miller Jr
Intercostal Pedicle Flap in Tracheobronchial Surgery
Ann. Thorac. Surg., August 1, 1996; 62(2): 630 - 631.
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R. G. Berrisford, J. L. Mercer, and J. I. Miller Jr
Pleural Slide Technique for Covering the Left Bronchial Stump
Ann. Thorac. Surg., June 1, 1996; 61(6): 1876 - 1877.
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G. Massard, C. Rouge, A. Dabbagh, R. Kessler, J.-G. Hentz, N. Roeslin, J.-M. Wihlm, and G. Morand
Tracheobronchial Lacerations After Intubation and Tracheostomy
Ann. Thorac. Surg., May 1, 1996; 61(5): 1483 - 1487.
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