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Ann Thorac Surg 2005;80:1017-1020
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Intercostal Muscle Flap to Buttress the Bronchus at Risk and the Thoracic Esophageal-Gastric Anastomosis

Robert James Cerfolio, MD, FACS a , * , Ayesha S. Bryant, MSPH b , Masumi Yamamuro, MD c

a Division of Cardiothoracic Surgery, Birmingham, Alabama
b Department of Epidemiology, School of Public Health, Birmingham, Alabama
c Department of Cardiovascular and Thoracic Surgery, University of Alabama at Birmingham, Birmingham, Alabama

Accepted for publication March 21, 2005.

* Address reprint requests to Dr Cerfolio, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, 1900 University Blvd, THT 712, Birmingham, AL 35294 (Email: robert.cerfolio{at}ccc.uab.edu).

Presented at the Poster Session of the Forty-first Annual Meeting of The Society of Thoracic Surgeons, Tampa, FL, Jan 24–26, 2005.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: We assessed our outcomes using an intercostal muscle flap harvested with cautery prior to chest retraction.

METHODS: Our retrospective study was conducted using an electronic prospective database.

RESULTS: There were 456 patients (348 men) over a six year period. The intercostal muscle flap was used for bronchial coverage in 391 patients. The indications for the flap were neoadjuvant radiochemotherapy in 285 patients, infection or inflammatory disease in 106, to buttress an esophageal-gastric anastomosis in 49, and for esophageal fistula in 16. There were three bronchopleural fistulas (0.7%); one after a right pneumonectomy for tuberculosis, one after a left pneumonectomy, and one after a lobectomy in a heart transplant patient for mucormycosis. The 4-week median postoperative pain score for patients who underwent an intercostal muscle flap was lower compared with historic controls who underwent similar procedures over the same time frame but did not have an intercostal muscle flap (2.4 vs 3.7, p = 0.003). Follow-up was a median of 26 months (range, 1 to 72 months) and no patients had ossification of their flap.

CONCLUSIONS: An intercostal muscle flap is a versatile pedicle flap that can reach all bronchi. It is easy to harvest, adds no morbidity, and may protect the bronchi at risk. When harvested devoid of periosteum it does not ossify over time and it may reduce the pain of thoracotomy.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Bronchopleural fistula (BPF) after elective pulmonary resection is a devastating problem, especially after pneumonectomy. The general thoracic surgeon, like most surgeons, is operating on older and sicker patients with more comorbidities, many of which increase the risk of BPF. Recently, more patients have undergone neoadjuvant chemoradiotherapy that also reduces bronchial healing [1, 2]. The best way to treat any postoperative complication is to prevent it. Pedicle muscle flaps have been shown to be effective techniques for bronchial buttressing after anatomic resection [3–5]. The use of large local chest wall muscle, such as the latissimus dorsi or the serratus anterior, are associated with morbidity and in our practice are used to treat a BPF, not to prevent one. Even newer techniques that only take down some of the serratus anterior attachments still lead to some winging of the scapula and seroma, and some loss of shoulder function [6]. Since the pleura is too thin and the pericardial fat pad is inconsistent and has unreliable blood supply we have come to prefer the intercostal muscle (ICM) flap. It is harvested prior to chest retraction and with a cautery so it is devoid of periosteum and thus will not calcify over time (see Fig 1). We reviewed our experience with the intercostal muscle flap.



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  		Fig 1. The intercostal muscle (ICM) flap is harvested prior to chest retraction using a cautery.

 

   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
This is a retrospective study using data that were entered into an electronic prospective database (Excel, Microsoft Corporation, Seattle, WA). An ICM flap was harvested if the bronchus was deemed to be at increased risk. These factors included the following: a history of radiation, steroid use of greater than 10 mg per day, an immunocompromised host secondary to insulin dependent diabetes, history of a solid organ or bone marrow transplant, and resection for inflammatory or infected pulmonary disease or the main stem bronchus after pneumonectomy. In addition an ICM was also used to repair an esophageal fistula, and to buttress the anterior aspect of an esophageal-gastric anastomosis in patients who underwent Ivor Lewis esophagogastrectomy.

Operative Technique
Patients underwent posterior-lateral thoracotomy. Approximately two-thirds of the posterior aspect of the latissimus dorsi muscle is cut and the entire serratus anterior muscle is spared. The rib is neither cut nor shingled. The intercostal muscle flap, usually overlying the sixth rib is harvested prior to chest retraction from the under surface of the fifth rib using a cautery, as shown in Figure 1. Rib instruments are not used for harvesting. The cautery is lowered to 40 from 70 and the muscle is carefully dissected with both cold and hot cautery starting at the distal end of the muscle just under the serratus anterior muscle. The cautery tip is positioned so it is almost parallel with the surface of the fifth rib so the intercostal vein is not injured during harvesting. The muscle is freed from the sixth rib posteriorly, past the lumbar-dorsal fascia, but it is not freed from the undersurface of the fifth rib past this structure. Further dissection posterior of the fifth rib risks injury to the vein. The first 20 patients had assessment of the viability of the muscle flap by injection of fluorescein followed by assessment under Wood’s lamp illumination, as well as by Doppler ultrasound.

At the completion of the anatomic pulmonary resection the bronchial stump is tested. The chest is filled with sterile warm saline and the remaining ipsilateral lung is inflated. Ventilatory pressure of 20 cm of pressure is held. After the stump is proven to have no air leak the ICM flap is examined. Hemostasis is ensured. The flap is then brought posteriorly and sewn onto the bronchus using four interrupted 3-0 double armed Prolene sutures (Ethicon, New Brunswick, NJ) so the muscle aspect (not the fascia component) is in contact with the cut end of the bronchus. These four tacking sutures are placed by taking a very small bite on the bronchial stump just proximal to the staple line to prevent injury to the blood supply. The sutures are then placed through the muscle and tied so the muscle overlies the entire bronchus. When the remaining lung is inflated one must ensure the flap is posterior to the lung so it does not pull the flap off the intended structure.

In patients who underwent Ivor Lewis esophagogastrectomy the muscle was placed over the anterior aspect of the anastomosis. It was tacked onto the esophagus superiorly and onto the stomach inferiorly using interrupted 2-0 silk sutures. It was also positioned over esophageal fistulas after repair using absorbable sutures.

Follow-up
Patient information was recorded in an electronic prospective database. Numeric pain scores were recorded at 4 weeks postoperatively and these values were compared with a set of retrospective controls who underwent similar procedures over the same time frame and who did not have an intercostal muscle flap. These scores were based on a numeric rating scale [7] and patients were instructed that 0 was no pain and 10 was excruciating pain.

In addition, the appearance of the muscle flap at follow-up was obtained by computed tomographic (CT) scans, which were performed at 6 month intervals for the first two years after operation and then yearly. The CT scans performed at our institution were reviewed by both the attending chest radiologist and the sole surgeon in this study (RJC) for evidence of ossification. The reports of follow-up CT scans not performed at our institution were used. The institutional review board approved this retrospective study and the electronic prospective database.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Between January 1999 and December 2004, 456 patients had an intercostal muscle flap used. The patient characteristics are shown in Table 1. The indications for the ICM flap are shown in Table 2. Most patients had the flap used for bronchial buttressing. The right upper bronchus was buttressed in 130 patients, the right middle in 14, right lower in 16, bronchus intermedius in 21, right main stem in 47, left upper in 69, left lower in 35, left main stem in 31, and others in 28. The versatility of the flap is demonstrated by the other indications. Table 3 shows the surgical outcomes associated with ICM flap placement. The median time for harvesting of the muscle flap was 3.8 minutes.


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  		Table 1. Patient Characteristics (n = 456)
 

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  		Table 2. Indications for Intercostal Muscle Flap a
 

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  		Table 3. Surgical Outcomes of Intercostal Muscle Flap
 
There were five patients who developed complications secondary to the flap. One patient returned to the operating room for hemorrhage from the flap itself. Three patients developed a BPF after intercostal muscle flap. Two were from the original infection that was in the lung that later grew into the flap and caused a BPF. One patient was human immunodeficiency virus positive and had mycobacterium tuberculous infection and underwent a left upper lobe. The other was a patient who had a previous heart transplant and developed mucormycosis that completely replaced the entire right lower lobe in a 12 cm mass. It later grew into the flap and caused a BPF. A fifth patient had the flap used to buttress an esophageal fistula that occurred after resection of a 10 cm leiomyoma. This fistula later reopened and the flap was found on reexploration to be partially necrotic.

Pain Scores
The 4-week median postoperative pain score was available for 415 of the 456 patients in this study. It was compared with a retrospective control group. These patients had identical openings and closings as well as similar types of procedures but did not have an intercostal muscle flap harvested prior to chest retraction. The pain score was lower in the ICM flap patients than in the control group of patients (2.4 vs 3.7, p = 0.003).

Follow-Up
Follow-up data were available on 301 of the 347 (87%) patients who were at least 6 months postsurgery. There was no radiologic evidence of ossification or calcification in any area of the flap in any patient.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The ICM is controversial. Many surgeons prefer not to use it in certain situations because of the perception that it calcifies over time and has unreliable blood supply [8–10]. We believe these concerns are based on how the flap is mobilized as opposed to the flap itself. The technique described in this article features the use of cautery to take down the ICM, as opposed to harvesting it in a subperiosteal fashion as done in the articles cited above. This latter technique leads to ossification over time. In this report we have shown that with the cautery technique the flap does not ossify over time. It has reliable blood supply when harvested prior to chest retraction, it is long, and it is able to reach all bronchi and thus is quite versatile. Harvesting of the ICM flap only takes a few minutes and does not increase morbidity.

Interestingly, we found that this technique may actually decrease the morbidity of thoracotomy, specifically by decreasing postoperative pain. As shown in this study, the pain scores were lower in patients who received an intercostal muscle flap when compared with a set of retrospective controls. The reason for this finding may be that the harvesting of the intercostal muscle (and the intercostal nerve that runs within it) prior to chest retraction helps prevent a crush injury to the nerve. This finding intrigued us so much that we have already designed, performed, and completed a prospective randomized trial that evaluated the pain of 114 patients. We found in that study (performed after this one) that an intercostal muscle flap decreased the pain of thoracotomy on postoperative days 1 and 2 and at weeks 1, 2, 3, 4, 8, and 12 (p < 0.05 for all) [11] when compared with patients who did not receive an intercostal flap.

The first concern that many surgeons have with the ICM flap is that it calcifies over time [8, 9, 12, 13]. Prommeger and Salzer, in 1998 [9], reported complications from an ossified ICM flap in three of 22 patients who received it. The authors postulated ossifications may have occurred due to harvesting of two periosteal margins. In a more recent study by Kwek and colleagues [10], the flap was again prepared with the periosteum on both margins. However, the authors described how to carefully excise excess periosteum prior to transposition of the flap to its intended site of reinforcement. They reported no ossification of the muscle flap using this technique. We do not believe that ossification of the flap is necessarily a problem. If the flap is used to help close a bronchi or an esophageal fistula, calcification over time may actually be desirable. In this study we have shown that when mobilized with cautery and thus devoid of periosteum it will not calcify over time. Patients had surveillance CT scans performed every 6 months to one year postoperatively. The median follow-up in this series was 2.1 years and 34 patients had scans performed after five years after resection. None of these patients have evidence of any ossification of their ICM flap.

The next concern many have with the ICM is its blood supply. The blood supply after mobilization of the ICM (like any other muscle flap) is dependent on the surgeon’s ability to avoid injury to the artery and vein and kinking of the vessels after transposition into the chest. The first 20 ICM muscles harvested in this series had their blood supply assessed by intraoperative injection of fluorescein and assessment under Wood’s lamp illumination. All fluoresced well. The ICM’s artery is usually not at risk but the vein is very close to the upper rib. When the ICM is carefully mobilized and the vein is avoided its blood supply is very reliable. However, as ones gets more proximal on the upper rib (going towards the vertebral bodies) the ribs get closer together and the chance of injuring the vein becomes higher. We prefer to go to the lumbar-dorsal fascia and no further. We stop the dissection at this point on the fifth rib. This allows enough mobilization so the flap is able to course posteriorly, under the inflated lung towards the buttressed structure, and yet not be harvested so posteriorly that the vein is injured. However, in an immunocompromised host with aggressive fungal infection, this flap may be insufficient as we had a few failures. Moreover, in an infected, fixed pleural space deficit it does not provide enough bulk and the omentum, serratus anterior, and/or latissimus dorsi muscles are preferred.

The primary limitation to our study is that it is retrospective. In addition, not all CT scans were performed at our institution. Some institutions still use 10 mm cuts. Additionally, evaluation for ossification of the muscle flap was done using radiologic reports in lieu of evaluation of the scans first hand in those cases.

Since most agree that the sleeved, irradiated, or infected bronchus is at risk, it is now the standard of care to buttress it with living tissue after lobectomy or pneumonectomy [14]. The flap may not be needed in the bronchus that is not at risk. Benefits to the ICM flap include the fact that it is easy and quick to harvest, is available in the local operative field, requires no special equipment, can be performed by the general thoracic surgeon (unlike omental, serratus, and latissimus flaps, which in many institutions are harvested by plastic surgeons). It also has been shown to decrease the pain of thoracotomy in this study as well as in a more formal prospective randomized pain study described above [11]. It is long and versatile and can reach any bronchi as well as the entire thoracic esophagus. Disadvantages include that it is in the irradiated field (as are the latissimus dorsi, the serratus anterior, the pericardium [15], the pericardial fat pad, and the pleura) and it can be quite thin, especially in small, frail patients and in females. It may also not provide enough protection in the immunocompromised host with aggressive opportunistic infection.

Further studies are needed as well as continued follow-up, but the intercostal muscle is an important adjunct that helps buttress the bronchus at risk of breakdown. In addition, it can be used to buttress the anterior aspect of the esophageal-gastric anastomosis and to cover repairs of esophageal fistulas. When harvested devoid of periosteum it will not ossify over time. If harvested prior to chest retraction it decreases the pain of thoracotomy probably by preventing a crush injury to the intercostal nerve.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Yamamoto R, Tada H, Kishi A, et al. Effects of preoperative chemotherapy and radiation therapy on human bronchial blood flow J Thorac Cardiovasc Surg 2000;119:939-945.[Abstract/Free Full Text]
  2. Mathisen DJ, Wain JC, Wright C, et al. Assessment of preoperative accelerated radiotherapy and chemotherapy in stage IIIA (N2) non-small-cell lung cancer J Thorac Cardiovasc Surg 1996;111:123-133.[Abstract/Free Full Text]
  3. Rendina EA, Venuta F, Ricci P, et al. Protection and revascularization of bronchial anastomoses by the intercostal pedicle flap J Thorac Cardiovasc Surg 1994;107:1251-1254.[Abstract/Free Full Text]
  4. Rendina EA, Venuta F, Ciriaco P, et al. Bronchovascular sleeve resection. Technique, perioperative management, prevention, and treatment of complications J Thorac Cardiovasc Surg 1993;106:73-79.[Abstract]
  5. Lardinois D, Horsch A, Krueger T, et al. Mediastinal reinforcement after induction therapy and pneumonectomya comparison of intercostal muscle versus diaphragm flaps. Eur J Cardiothorac Surg 2002;21:74-78.[Abstract/Free Full Text]
  6. Pairolero PC, Arnold PG, Trastek VF, et al. The role of intrathoracic muscle transposition. J Thorac Cardiovasc Surg 99:958–66..
  7. Downie WW, Leatham TA, Rhind PA, et al. Studies with pain rating scales Ann Rheum Dis 1978;37:378-381.[Abstract/Free Full Text]
  8. Deeb ME, Sterman DH, Shrager JB, et al. Bronchial anastomotic stricture caused by ossification of an intercostal muscle flap Ann Thorac Surg 2001;71:1700-1702.[Abstract/Free Full Text]
  9. Prommegger R, Salzer MG. Heterotopic ossification in pedicled intercostal muscle flaps causing clinical problems J Thorac Cardiovasc Surg 1998;115:466-467.[Free Full Text]
  10. Kwek B, Wain J, Aquino S. The radiologic appearance of intercostal muscle flap Ann Thorac Surg 2004;78:432-435.[Abstract/Free Full Text]
  11. Cerfolio RJ, Bryant AS, Patel B, et al. Intercostal muscle flap reduces the pain of thoracotomy: a prospective randomized trial. J Thorac Cardiovasc Surg (to be published)..
  12. Rebduba EA, Ventuta F, Ricci P, et al. Protection and revascularization of bronchial anastomoses by intercostal pedicle flap J Thorac Cardiovasc Surg 1994;107:1251-1254.
  13. Fell SC, Mollenkopf FP, Montefusco CM, et al. Revascularization of ischemic bronchial anastomoses by an intercostal pedicle flap J Thorac Cardiovasc Surg 1985;90:172-178.[Abstract]
  14. Sonett JR, Suntharalingam M, Edelman MJ, et al. Pulmonary resection after curative intent radiotherapy (> 59 Gy) and concurrent chemotherapy in non-small-cell lung cancer Ann Thorac Surg 2004;78:1200-1205.[Abstract/Free Full Text]
  15. Taghavi S, Marta GM, Lang G, et al. Bronchial stump coverage with a pedicled pericardial flapan effective method for prevention of postpneumonectomy bronchopleural fistula. Ann Thorac Surg 2005;79:284-288.[Abstract/Free Full Text]



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