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Ann Thorac Surg 2004;78:432-435
© 2004 The Society of Thoracic Surgeons

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Original article: general thoracic

The radiologic appearance of intercostal muscle flap

^a Department of Radiology, Massachusetts General Hospital, Boston, Massachusetts, USA,
^b Thoracic Surgical Unit, Massachusetts General Hospital, Boston, Massachusetts, USA

Accepted for publication January 22, 2004.

^* Address reprint requests to Dr Aquino, Department of Radiology, FND 202, Massachusetts General Hospital, 55 Fruit St, Boston, MA 02114, USA
e-mail: saquino{at}partners.org

	Abstract

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BACKGROUND: The intercostal muscle flap (ICMF) is commonly used in airway and esophageal surgery to reinforce an anastomosis or site of closure. These flaps undergo heterotopic ossification that may result in stenosis of adjacent airways or the esophagus. We evaluated the computer tomography (CT) scan, technetium-99m-methylene diphosphonate bone scan and positron emission tomography with 2-[¹⁸F]-fluoro-2-deoxy-D-glucose (FDG-PET) findings of ICMF and the frequency of airway or esophageal stenosis.

METHODS: A retrospective review was made of the radiologic records of 23 patients (9 women, 14 men) who underwent ICMF. The CT scans were obtained a mean of 36 months (range, 1 week to 58 months) after surgery and the size, morphology, and density of the ICMFs were recorded. Correlative bone scan in 13 patients and FDG-PET scans in 11 patients were reviewed.

RESULTS: A discontinuous, thin, linear calcified stripe or parallel stripes (mean thickness, 4 mm; mean density, 430 Houndsfield unit [HU]) were present in all patients on CT. The flap contained fat density (mean, –59 HU) in 18 patients and soft tissue density (mean, 41 HU) in 8 patients and measured about 1 cm in thickness. The appearance of ICMF is characteristic when the ossification extends from the posterolateral chest wall to an adjacent bronchial stump. There was no increased uptake on bone scan or FDG-PET scan. None of the patients had airway or esophageal stenosis.

CONCLUSIONS: The ICMF manifests on CT as a thin, linear calcified stripe or parallel stripes with central fat or soft tissue density. Airway stenosis due to ICMF is likely quite rare. We did not detect any airway stenosis.

	Introduction

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Use of the pedicled intercostal muscle flap (ICMF) in thoracic surgery was first described by Shenstone in 1936 [1]. The ICMF is used mainly in airway reconstruction and anastomosis [2–4] especially for high-risk surgery in patients who had undergone prior chemotherapy and irradiation [5, 6]. The ICMF has also been shown to be useful in esophageal surgery after perforation from benign and malignant etiologies [7–10]. A major concern with the use of ICMF is the development of heterotopic ossification within the accompanying periosteum and its possible adverse effects on the adjacent tissues. Previous studies have correlated airway stenosis with ossification of the flap [3, 11–14].

The radiologic appearance of ICMF has not been described in the literature except for case reports of complications due to ossification of the ICMF [12, 14]. The purpose of this paper is to evaluate the computed tomography (CT) appearance of the ICMF in a population of patients undergoing complex thoracic surgery and to determine the incidence of heterotopic flap ossification and any adverse effects of the ICMF on the adjacent tissues.

	Material and methods

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The study was approved by our institutional Human Research Committee. From 1999 to 2003, 23 patients who underwent thoracic surgery requiring ICMF and had chest CT were identified. A retrospective review of their clinical and radiologic records was performed. There were 9 women and 14 men, with mean age of 63 years (range, 37 to 81). Lung carcinoma was the diagnosis in 21 patients. Indications for ICMF in this group were the following: 14 patients received preoperative chemotherapy and radiation therapy; 2 patients had scheduled postoperative radiation therapy; 2 patients received preoperative steroids; 1 patient had Cushing's syndrome; and 2 had prior thoracotomy. One patient underwent resection of a mycobacterial lung abscess, and another patient had repair of a postemetic esophageal perforation (Boerhaave's syndrome). Sixteen patients underwent segmental lung resection, and 6 patients required pneumonectomy. The ICMF was used to reinforce the bronchial stump in all but 2 patients. It was wrapped around a tracheobronchial anastomosis in one and used to reinforce the repair of an esophageal perforation in the other.

To prepare this flap, one or more intercostal muscles and the corresponding neurovascular bundle were dissected from the adjacent ribs in a subperiosteal fashion. The ICMF consisted of muscle, neurovascular bundle, and adjacent underlying pleura; excess adherent periosteum on the superior and inferior margins of the flap was carefully excised. The pedicle for the ICMF was based posteriorly between the necks of two adjacent ribs, with mobilization as far anterior as possible. Transection of the ICMF and control of the neurovascular bundle at that point allowed for an adequate length of tissue for transposition intrathoracically.

All postoperative CT scans were obtained with either GE HighSpeed or LightSpeed scanners (GE, Milwaukee, WI). Scans were obtained at 5-mm slice intervals and pitch 1:1.5 during a single breath hold. Thirteen patients had CT scans performed both with and without intravenous contrast (100 mL of ioxilan, 300 mg I/mL at an injection rate of 2 mL/s), 8 patients had scans performed with intravenous contrast, and the remaining 2 were scanned without intravenous contrast on account of contrast allergy. The CT scans were retrospectively reviewed on mediastinal windows settings (window width, 350; window level, 40) on a PACS (picture archiving and communication system) monitor. The size, morphology, and density of the ICMF were recorded. In addition, 15 patients had CT scans performed before surgery that were reviewed.

Correlative technetium-99m-methylene diphosphonate (Tc-99m-MDP) bone scans were performed in 13 patients. For the bone scans, the patients were imaged at least 2 hours after intravenous administration of 740 to 812 MBq of Tc-99m-MDP. Spot and whole body views were obtained using a large field gamma camera with a high-resolution parallel hole collimator with bed movement of 10 cm/min (E.CAM/Siemens, Hoffman Estates, IL).

Fluorodeoxyglucose positron emission tomography (FDG-PET) scans were performed in 11 patients. Whole body and thoracic FDG-PET studies were obtained with an ECAT-HR+ camera (Siemens/CTI, Knoxville, TN) or GE 4096 camera (General Electrical, Milwaukee, WI). Image spatial resolution was 5.0 mm full width half maximum with slice thickness of 2.4 mm. The patients fasted for at least 6 hours before scanning and blood glucose levels were measured just before injection of FDG. Static emission images, each of 10 minutes' duration, were obtained about 60 minutes after bolus injection of 14.1 to 20 mCi of FDG. Transmission scans, measured with rotating rod sources loaded with Germanium-68 were obtained in each patient for attenuation correction. Image reconstruction was performed with either Filter Back projection (GE 4096) or with iterative reconstruction algorithm: ordered subset expectation maximization (ECAT-HR+). The PET scans were retrospectively reviewed on a clinical computer reading station, and the extent, distribution and morphology of increased FDG uptake were recorded. The degree of FDG activity was visually graded as no discernible uptake, uptake less than, equal to, or greater than background mediastinal activity. Abnormal FDG uptake was interpreted if the uptake exceeded that of the mediastinal soft tissues.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
The earliest CT was performed a mean of 14 months (range, 1 week to 58 months) after surgery. The ICMF appeared on CT as a linear stripe extending from the posterolateral chest wall to the hilar region adjacent to a blind ending bronchus (Fig 1). All ICMFs in our study group showed discontinuous, linear calcifications that appeared either as a single thin stripe (in 5 patients; Fig 2) or as two parallel stripes (in 18 patients; Fig 3). When the ICMF appeared as parallel stripes the central portion was low in attenuation and resembled an intrathoracic rib (Fig 4). The average thickness of the linear calcification was 4 mm (range, 1 to 8 mm) with mean density measurement of 430 Houndsfield units ([HU] range, 214 to 670 HU). In 18 patients the soft tissue component of the ICMF was fat density (mean, –59 HU, range, –10 to –99 HU). In 8 patients, the ICMF was soft tissue in density (mean, 41 HU; range, 11 to 72 HU).

View larger version (68K): [in this window] [in a new window]   Fig 1. Computed tomography scans of a 49-year-old woman who had undergone right upper lobectomy and intercostal muscle flap (ICMF) for lung cancer 6 years earlier. (A) Image of thorax shows ICMF as a fat density stripe with adjacent calcification extending from the posterolateral aspect of a rib (arrow). (B) Centrally, the ICMF lies adjacent to the right main bronchus (arrow) indicating the site of surgery.

View larger version (77K): [in this window] [in a new window]   Fig 2. Computed tomography scan of a 62-year-old woman with lung cancer who had undergone a right pneumonectomy 9 months earlier. (A) The intercostal muscle flap (arrows) in the pneumonectomy space manifests as a single linear calcification with surrounding low attenuation fat. (B) Axial 2-[18F]-fluoro-2-deoxy-D-glucose (FDG) positron emission tomography scan shows normal FDG uptake in the region of the intercostal muscle flap (arrows) that is the same as background soft tissue uptake.

View larger version (69K): [in this window] [in a new window]   Fig 3. Computed tomography scan of a 60-year-old man who underwent right upper lobectomy for lung cancer. The intercostal muscle flap (arrow) appears as two parallel linear calcifications that resemble a thoracostomy tube.

View larger version (74K): [in this window] [in a new window]   Fig 4. Computed tomography scan of a 51-year-old man with lung cancer who had undergone a right upper lobectomy 18 months earlier. The intercostal muscle flap (arrow) contains two thick linear ossifications that resemble an intrathoracic rib.

Thirteen of the 23 patients had bone scans performed on average 31 months (range, 4 to 80) after surgery. No abnormal uptake was detected in the bone scans of any of the patients in the region of the ICMF (Fig 2B).

Eleven patients in our study also received FDG-PET scans on average 31 months (range, 2 to 81) after surgery. Eight patients showed mild to moderate uptake (less than or equivalent to background mediastinal activity; Fig 2B), whereas there was no discernible FDG uptake in the remaining 3 patients.

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
The ICMF is used in airway reconstruction and anastomosis, to buttress bronchial stumps in patients who receive preoperative chemotherapy or radiation therapy or to reinforce esophageal perforations [2–6]. In our institution, ICMF comprises approximately 10% of all thoracic surgical flaps [15]. Other structures implemented for flaps include pericardial fat/thymus (37.6%) and the greater omentum (36.6%) [15, 16].

The most common CT pattern of an ICMF was a discontinuous thin linear calcified stripe or two parallel calcified stripes (mean thickness of 4 mm and density of 430 HU). The calcification is present as early as a week postoperatively and reaches maximal density at mean of 5 months. The calcified appearance of ICMF is very characteristic and usually can be traced from its origin at the chest wall to lie adjacent to a bronchial stump (Fig 1). The ossified flap can give the appearance of an intrathoracic rib if there are two stripes (Fig 4) or a surgical staple line if there is a single stripe. The center of the flap either contained fat density (mean density –59 HU, 18 patients) or soft tissue density (mean density 41 HU, 8 patients). This fat density appearance has not been described before, and we postulate that it is due to fatty replacement of the intercostal muscle as a result of disuse atrophy or inadvertent denervation during mobilization of the ICMF.

None of the ICMF imaged by radionuclide bone scan or FDG-PET scan showed increased activity. With evolving heterotopic ossification in the postoperative period, there is the theoretical potential for increased radionuclide activity on bone scan as a flap ossifies or on FDG-PET scan due to active cellular activity. We did not find any significant abnormal increase activity in the flap region on either scan that could falsely create increased signal and mimic recurrent malignancy.

Previous reports have described airway and esophageal obstruction due to ossification of ICMF [3, 11–14]. The first report of complication from an ossified ICMF was by Prommegger and Salzer [12] in 1998. Of a total of 22 patients with ICMF, 3 developed dyspnea and chest pain. One patient's CT scan showed airway stenosis from an ossified flap; this stenosis was repaired successfully by surgery without further sequelae. Another patient developed a bronchoesophageal fistula that was attributed to fixation of the esophagus to the bronchus by the ossified muscle flap; unfortunately, the patient died of mediastinitis. The third patient did not undergo any intervention. Deeb and associates [14] reported a patient with recurrent middle lobe pneumonia due to bronchial obstruction from an ossified flap. Computed tomography scan and bronchoscopy documented stenosis of the bronchial anastomosis. Bronchial stenting was unsuccessful and surgery was performed. During surgery, the proximal right pulmonary artery was found to be adherent to the ossified muscle flap and a pneumonectomy was necessary. In our study, no instances of airway stenosis due to the ICMF were identified despite the fact that all flaps demonstrated evidence of calcification.

The ICMF is widely used in the repair of esophageal perforations with reportedly good results [7–10]. Demos [10] described 100 esophageal surgeries using ICMF with no significant postoperative strictures that required surgical repair. In our study, 1 patient received an ICMF for repair of an esophageal perforation. Her postoperative CT did not show any evidence of esophageal obstruction by the flap despite ossification of the flap.

Prommeger and Salzeron [12] postulated that the complications from ICMF may result from harvesting two periosteal margins. They noted that Rendina and associates [3] included the periosteum of only one rib in their flaps, and no complication was encountered in 56 patients. Fell and associates [11, 13] suggested applying 20% silver nitrate solution in order to ablate the periosteum and reported good results. The ICMF used in our study was prepared with the periosteum on both margins. No silver nitrate solution was applied. During preparation of the flap, excess periosteum was carefully excised before transposition of the ICMF to its intended site of reinforcement. The meticulous excision of excess periosteum may contribute to the absence of any complications in our series.

In conclusion, the ICMF is commonly used for reinforcement of regions of airway and esophageal surgery. The flap uniformly ossifies at its periosteal margins. On CT, ossification of these flaps appears as a discontinuous, thin, calcified stripe or two parallel stripes that contain central fat or soft tissue. The detection of an ICMF on CT should be described routinely when identified. Although in our study no sequelae were observed from ossification of these flaps, based on previous reports the presence of airway or esophageal compromise should be sought. The ICMF did not show increased radionuclide uptake on bone scans or FDG-PET studies and thus did not interfere with tumor surveillance.

	References

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6. Mathisen D.J., Wain J.C., 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]
7. Bryant L.R., Eiseman B. Experimental evaluation of intercostal pedicle grafts in esophageal repair. J Thorac Cardiovasc Surg 1965;50:626-631.[Medline]
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