(Radiology. 2000;216:123-127.)
© RSNA, 2000
CT and Arteriography in the Evaluation of Indirect Myocardial Revascularization with a Free-Muscle Transplant: Initial Experience1
Stefan C. Krämer, MD,
Johannes Görich, MD,
Michael Beyer, MD,
Elmar Merkle, MD,
Jaqueline Gerber, MD,
Norbert Rilinger, MD,
Roman Sokiranski, MD and
Hans-Jürgen Brambs, MD
1 From the Departments of Radiology (S.C.K., J. Görich, E.M., N.R., R.S., H.J.B.) and Cardiosurgery (M.B., J. Gerber), University of Ulm, Steinhövelstrasse 9, 89075 Ulm, Germany. Received July 12, 1999; revision requested August 16; revision received November 1; accepted November 10. Address correspondence to S.C.K. (e-mail: stefan.kraemer@medizin.uni-ulm.dc).
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ABSTRACT
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PURPOSE: To examine patients with advanced cardiovascular disease with radiology after indirect myocardial revascularization with a free-skeletal-muscle transplant and to determine whether the attached vessel remains patent over the middle and long terms.
MATERIALS AND METHODS: In 10 patients with advanced, inoperable cardiovascular disease treated with indirect myocardial revascularization with a free-muscle transplant, radiologic follow-up was performed postoperatively and every 6 months. All 10 patients underwent selective arteriography of the anastomosed vessel and contrast materialenhanced helical computed tomography (CT) (transverse sections and reconstructions).
RESULTS: All patients showed adequate vascular conditions postoperatively, as did nine of 10 patients after 1 year. In one patient, the anastomosed artery was occluded. CT showed time-dependent muscle degeneration in all patients. Postoperative, contrast-enhanced, superselective CT showed an area of high-attenuating uptake in the muscle transplant in all patients. After 1 year, CT depicted perfusion defects of the skeletal muscle in two patients. In eight patients, however, small vascular bridges from the skeletal muscle to the myocardium were detected. Radiologic results correlated well with clinical outcome and stress electrocardiograms.
CONCLUSION: Helical intraarterial CT and arteriography were sensitive in depicting enhancement and remaining vital function in nine of 10 patients after indirect myocardial revascularization with a free-muscle transplant. This combination seems promising for postoperative examination in such patients.
Index terms: Angiography, 51.1242 Heart, CT, 51.12115, 51.12116, 51.12117 Heart, surgery, 51.454 Myocardium, abnormalities, 511.7644 Myocardium, blood supply, 511.76 Myocardium, ischemia, 511.76
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INTRODUCTION
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Cardiovascular diseases remain the leading cause of death in modern industrial societies (1). In addition to conservative methods, the surgical techniques of coronary bypass grafting and percutaneous transluminal coronary angioplasty generally have been accepted for the management of these disorders.
Patients with advanced diseasein particular, those with poor peripheral vasculaturefrequently are considered incapable of undergoing surgery. Gould et al (2) have reported success in patients who consume strict low-fat diets, with the elimination of other risk factors. New surgical techniques based on laser revascularization seem useful for improving subendocardial perfusion (3), although to our knowledge confirmed results of controlled studies are not yet available.
One surgical alternative described by Vineberg (4,5) in the 1940s and 1950s centers on indirect myocardial revascularization derived from the internal mammary artery. Direct transplantation of skeletal muscle onto the myocardium has been described for improving the heart's pumping function in cases of dilated cardiomyopathy (6,7). Transplantation of skeletal muscle for improving myocardial perfusion was reported by Beyer et al (8) in 1992. In comparison with muscular reinforcement in the management of cardiomyopathy, this procedure aims for a permanent, additional vascular supply to the heart muscle and can be used in those cases in which myocardial infarction already has occurred (9).
The examination of patients treated with this technique should include an imaging protocol in which cardiac and graft anatomy are depicted and in which data on vascular function are provided. The purpose of our study was to determine whether the attached vessel remains patent over the middle and long terms and whether perfusion of the transplant and cardiac muscle can be evaluated with radiologic methods.
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MATERIALS AND METHODS
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Between 1995 and 1997, 10 male patients aged 5572 years underwent radiologic examination postoperatively and again after 6 months and 1 year. Our series demonstrates the first, to the best of our knowledge, 10 consecutive patients from a group of 17. At the time this article was written, the other seven had not yet had a follow-up of 1 year. The primary disease in all patients was advanced coronary heart disease with three-vessel disease; these patients were considered unsuitable to undergo coronary bypass grafting.
Patients were treated in the department of cardiovascular surgery by using indirect myocardial revascularization as an alternative. During the procedure, a free-skeletal-muscle flap, with its vascular supply, the dorsal thoracic artery, was taken from the latissimus dorsi muscle. After thoracotomy, the muscle flap was wrapped around the ischemic portion of the left ventricle and was sutured in position after the epicardium was roughened. In a procedure analogous to venous bypass grafting, the vascular stem of the dorsal thoracic artery was anastomosed to the ascending aorta. The venous return from the transplanted flap was diverted into the right auricle. The operation did not require a heart-lung machine (8).
Radiologic follow-up examinations were performed 12 weeks postoperatively and then every 6 months on the basis of our clinically accepted protocol for these patients. At all follow-up examinations, patients first underwent diagnostic arteriography. By using a standard technique, femoral arterial access was obtained with a 5-F sheath (Terumo, Frankfurt/Main, Germany). Thereafter, a right modified Amplatz coronary catheter (Mallinckrodt, Hennef, Germany) was introduced, and through this the implanted dorsal thoracic artery was catheterized by using a coaxial system (Tracker-18; Target, Ratingen, Germany). Immediately after the examination began, 5,000 IU of heparin (Heparin-Natrium; Braun, Melslingen, Germany) was administered intraarterially for thrombosis prophylaxis. After arteriography (Polytron 40; Siemens, Erlangen, Germany) at two frames per second in two oblique projections, with manual injection of up to 5 mL of nonionic contrast material (iopamidol [Solutrast 300; Byk Gulden, Constance, Germany]) for visualization of the immediate enhancement, patients underwent helical computed tomography (CT) before and after intraarterial contrast medium injection through the microcatheter. Immediately after the examination, the catheter and the sheath were removed, and the patients were immobilized for 12 hours.
CT was performed by using a helical scanner, with the double-detector technique (CT Twin; Elscint, Haifa, Israel). The effective section thickness was 3.2 mm, and the increment was set at 1.6 mm, fully overlapping. The pitch was set at 1. Intraarterial injection of 10-15 mL of contrast medium (iopamidol) was performed manually at full strength; it was started immediately before scanning and was continued during the entire scanning time. The duration of scanning for the entire heart was 3035 seconds, 0.75 second per effective section. Data sets then were transferred to a workstation (Indigo II; Silicon Graphics, Mountain View, Calif) for multiplanar and three-dimensional reconstructions and for maximum intensity projection.
Radiologic evaluation of the patency of the vessel, of the thickness and perfusion of the graft, and of the possible local enhancement of the myocardium itself was performed by two experienced radiologists (S.C.K., J. Görich) in consensus. Informed consent was obtained from every patient prior to the procedure.
Patients underwent further follow-up examinations at the same time intervals. Examinations included laboratory parameters (red and white blood cell count and cardiac enzymes) and stress electrocardiography, which was started at 25 W/sec and increased by another 25 W/sec, at a maintenance of 2 minutes. Stress examinations were stopped in the event of symptoms, S-T alterations, or muscular exhaustion. We noted any adverse effects or complications.
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RESULTS
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At postoperative examination, arteriography demonstrated patency of the anastomosed vessel in all patients. There was no evidence of stenosis in any patient. Adequate perfusion of the muscle was demonstrated with contrast medium uptake in the graft, as visualized at subsequent CT (Fig 1).

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Figure 1. Transverse contrast-enhanced helical CT scan obtained in a 54-year-old male patient 10 days after indirect myocardial revascularization by using a flap from the latissimus dorsi muscle shows the 1.8-cm thickness of the muscle flap (arrows) apposed to the epicardium, with substantial enhancement after intraarterial contrast medium injection. Vascular connections with the myocardium are not seen.
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Contrast medium uptake in the myocardium adjacent to the muscle flap was not seen. In one case, a large hematoma had formed within the transplanted muscle flap.
After 1 year, the vessel supplying the muscle flap could be catheterized and visualized at arteriography in nine of 10 patients (Fig 2). In one patient, however, there was occlusion of the anastomosed vessel. Except in this patient, contrast medium uptake in the transplanted muscle flap was detected at CT as evidence of maintained perfusion. In two patients, however, CT revealed a perfusion defect that affected about one-third of the transplanted muscle (Fig 3); this suggested the segmental occlusion of a vessel that supplied the muscle flap. In contrast, CT failed to depict the anastomosed vessel itself. Only the microcatheter in place could be seen.

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Figure 2. Right-anterior-oblique (25° oblique) arteriogram obtained in the patient in Figure 1 after free-skeletal-muscle transplantation shows that the main catheter has been advanced to the site of the anastomosis of the vessel to the ascending aorta (curved arrow), while the attached dorsal thoracic artery (straight arrow) is catheterized with only the microcatheter. No evidence of stenosis is seen; a normal vascular course with branching into individual segments in the muscle also is seen.
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Figure 3. Transverse contrast-enhanced helical CT scan obtained at follow-up in a 69-year-old male patient 1 year after indirect revascularization shows the muscle transplant, with regular lateral perfusion (white arrows) and with an anterior perfusion defect (black arrows).
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In eight patients, fine projections of contrast-enhanced tissue that extended from the transplanted muscle toward the myocardium were observed (Fig 4). A dot-shaped, circumscribed area of contrast medium enhancement of the heart muscle itself in the immediate area of these projections was observed in three patients, with an increase in attenuation of about 20 HU. In addition to the patient with complete vascular occlusion, one other patient demonstrated neither the enhanced projections nor the dot-shaped areas of contrast medium enhancement.

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Figure 4a. Contrast-enhanced helical CT images obtained in a 63-year-old male patient 1 year after myocardial revascularization show that contrast medium uptake in the muscle flap still is good, despite atrophy to a thickness of 0.6 cm. Fine projections of contrast medium (arrows) toward the myocardium are seen on both (a) transverse and (b) coronally reconstructed sections and have been interpreted as evidence of vascular connections.
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Figure 4b. Contrast-enhanced helical CT images obtained in a 63-year-old male patient 1 year after myocardial revascularization show that contrast medium uptake in the muscle flap still is good, despite atrophy to a thickness of 0.6 cm. Fine projections of contrast medium (arrows) toward the myocardium are seen on both (a) transverse and (b) coronally reconstructed sections and have been interpreted as evidence of vascular connections.
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In relation to time elapsed since transplantation, there is increasing atrophy of the implanted muscle flaps to about 35% of their original size. After 12 months, the transplanted flap had undergone partial or total fatty degeneration, so that no more than a narrow band of muscle tissue could be recognized. Such degeneration was observed in all patients treated (Fig 5).

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Figure 5. Graph shows the mean values of time-dependent atrophy of the transplanted skeletal muscle flap in all patients postoperatively (post-op), at 6 months, and at 12 months. Error bars refer to SD.
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With the exception of the patient with vascular occlusion, in whom stress electrocardiography demonstrated no change, all patients who underwent clinical follow-up every 6 months postoperatively reported substantial improvement in subjective complaints and reported a decrease or stabilization in the need for antianginal medication (nitroglycerin) (Table). The improvements in stress test results were very individual but demonstrated a mean increase of 25 W/sec after 1 year (Fig 6).
The following adverse effects or complications were documented during follow-up examinations: One patient experienced scintillating scotoma and circulatory weakness, while another patient experienced angina pectoris. Both patients' complaints responded to treatment.
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DISCUSSION
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The introduction of modern cross-sectional imaging techniques has resulted in continuing progress in the development of cardiac diagnostic modalities. In the 1980s, the first evaluations of coronary bypass grafts yielded satisfactory results (10,11). Helical CT offered further improvement in cardiac imaging (12). In addition to conventional CT for detecting calcifications in the coronary arteries and for providing evidence of the extent of the disease (13), electron-beam CT is used to evaluate the coronary arteries (14,15). Magnetic resonance (MR) imaging also is returning promising results in cardiac imaging. In addition to its potential uses in patients with ischemic cardiac disease (16), MR imaging has been used in evaluating the patency of venous bypass grafts, with 90% accuracy (17). Anastomosed arterial segments and bypass graft stenoses, however, continue to escape depiction with these techniques (18).
In comparison with patients in the aforementioned studies, our patients represent a special collective. The advantages of helical CT over MR imaging include its more rapid examination time and its lower susceptibility to artifacts. The suture material (metal clips) attaching the transplanted muscle flap to the myocardium made our patients particularly unsuitable for MR imaging. Furthermore, the possibility of invasive intraarterial contrast medium administration with better patient monitoring in CT, in comparison with that in MR imaging, also was of importance in the choice of imaging technique.
Intraarterial contrast-enhanced CT with an indwelling catheter is known primarily in connection with the evaluation of vascular perfusion for subsequent chemotherapy. Results with this modality have been excellent (19,20).
Our findings included an easily recognized, time-dependent degeneration of the transplanted muscle flap. This was not unexpected, since the transplanted muscle loses its own function. Contrary to findings by Tello et al (12), evaluation of the vessel of the muscle flap, which has an attachment similar to that of a venous bypass graft, was not possible on cross-sectional images. Only the anchored microcatheter and the proximal vascular stem were visualized.
The expansion of the examination technique with intraarterial contrast medium administration resulted in the evaluation of perfusion of both the vessel and the muscle flap in all patients in whom catheters could be placed. The possibility of neovascularization, at least in the three patients with slight enhancement of the myocardium, seems to be confirmed. A sprouting of vessels, which either escapes detection with CT or which already exists in the form of the fine bridges of contrast material enhancement described previously, remains uncertain, although results of an animal experiment (21) have demonstrated the formation of vascular connections between the myocardium and the transplanted muscle grafts. Beyer et al (22) reported a functional revascularization after skeletal muscle transplantation in dogs. In our study, time seemed to be the decisive factor, since the results of examinations performed 1014 days postoperatively failed to demonstrate the phenomena described. Even if capillary growth had begun by this time, it probably would have been impossible to document it with radiologic techniques.
The combination of arteriography and intraarterial, contrast-enhanced, helical CT has yielded promising results in our patient group. All patients remained alive after 1 year. Vascular occlusion occurred in only one (10%) patient, while at least partial tissue survival in nine (90%) patients and successful revascularization of the myocardium in eight (80%) patients can be presumed. Ongoing follow-up, including diagnostic imaging, should be performed to document the further courses of these patients in comparison with clinical findings and to evaluate the potential of this surgical method. Further functional aspects may be evaluated with the integration of associated nuclear medical modalities into the protocol described earlier.
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FOOTNOTES
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Author contributions: Guarantor of integrity of entire study, S.C.K.; study concepts, S.C.K., J. Görich; study design, S.C.K., M.B., J. Gerber; definition of intellectual content, S.C.K., J. Görich; literature research, S.C.K., E.M.; clinical studies, M.B., J. Görich, N.R.; data acquisition, J. Görich, S.C.K., R.S.; data analysis, S.C.K., J. Görich; manuscript preparation and editing, S.C.K.; manuscript review, H.J.B., J. Görich.
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REFERENCES
|
|---|
-
Braunwald E, ed. Heart disease 5th ed. New York, NY: Sanders, 1996.
-
Gould KL, Ornish D, Schwerwitz L, et al. Changes in myocardial perfusion abnormalities by positron emission tomography after long-term intense risk factor modification. JAMA 1995; 274:894-901.[Abstract]
-
Cooley DA, Frazier OH, Kadipasaoglu KA, et al. Transmyocardial laser revascularisation: clinical experience with twelve month follow-up. J Thorac Cardiovasc Surg 1996; 111:791-799.[Abstract/Free Full Text]
-
Vineberg AM. Development of an anastomosis between the coronary vessels and a transplanted internal mammary artery. Can Med Assoc 1946; 55:117-122.
-
Vineberg AM. Clinical and experimental studies in the treatment of coronary artery insufficiency by internal mammary artery implant. J Int Coll Surg 1954; 22:503-518.[Medline]
-
Carpentier A, Chanchques JC. Myocardial substitution with a stimulated skeletal muscle: first successful clinical case (letter). Lancet 1985; 1:1267.[Medline]
-
Moreira LFP, Stolf NAG, Bocchi EA, et al. Latissimus dorsi cardiomyoplasty in the treatment of patients with dilated cardiomyopathy. Circulation 1990; 82(suppl 4):257-263.
-
Beyer M, Hoffer H, Mierdl S, Hannekum A. Cardiomyoplasty to improve collateral blood supply as an alternative to transplantation in intractable angina. Heart Lung Transplant 1992; 4:189-191.
-
Beyer M, Hoffer H, Eggeling T, Matt O, Beyer U, Hannekum A. Free skeletal muscle transplantation to an infarction area: an experimental study in the dog. Microsurgery 1993; 14:125-129.[Medline]
-
Godwin JD, Califf RM, Korbkin M, Moore AV, Breiman RS, Kong Y. Clinical value of coronary bypass graft evaluation with CT. AJR Am J Roentgenol 1983; 140:649-655.[Abstract/Free Full Text]
-
Daniel WG, Döhring W, Stender HS, Lichtlen PR. Value and limitations of computed tomography in assessing aorto-coronary bypass graft patency. Circulation 1983; 67:983-987.[Abstract/Free Full Text]
-
Tello R, Costello P, Ecker C, Hartnell G. Spiral CT evaluation of coronary artery bypass graft patency. J Comput Assist Tomogr 1993; 17:253-259.[Medline]
-
Görich J, Zuna I, Merle M, Beyer-Enke SA, Pobst G, van Kaick G. Coronary artery calcifications in computer tomography investigations: frequency, correlation with risk factors and with cardiovascular diseases. J Vasc Invest 1996; 2:23-33.
-
Kosling S, Hoffmann U, Lieberenz S, et al. First experiences with electron beam computed tomography of the heart: comparison with heart catheterization and echocardiographic findings. Rofo Fortschr Geb Röntgenstr Neuen Bildgeb Verfahr 1995; 163:111-118.[Medline]
-
Moshage WE, Achenbach S, Seese B, Bachmann K, Kirchgeorg M. Coronary artery stenoses: three-dimensional imaging with electrocardiographically triggered, contrast agentenhanced, electron-beam CT. Radiology 1995; 196:707-714.[Abstract/Free Full Text]
-
Steffans JC, Sakuma H, Bourne MW, Higgins CB. Magnetic resonance imaging in ischemic heart disease. Am Heart J 1996; 132:156-173.[Medline]
-
van Rossum AC, Galjee MA, Doesburg T, Hofman M, Valk J. The role of magnetic resonance in the evaluation of functional results after CABG/PTCA. Int J Card Imaging 1993; 9(suppl 1):59-69.
-
van Rossum AC, Galjee MA, Post JC, Visser CA. A practical approach to MRI of coronary artery bypass graft patency and flow. Int J Card Imaging 1997; 13:199-204.[Medline]
-
Rieber A, Brambs HJ, Görich J, Kauffmann GW. Intra-arterial angio-CT for perfusion control of intra-arterial chemotherapy of bronchial, mammary and liver tumours. Rofo Fortschr Geb Röntgenstr Neuen Bildgeb Verfahr 1991; 154:514-517.[Medline]
-
Görich J, Rilinger N, Sokiranski R, et al. CT-guided intraarterial chemotherapy in locally advanced tumors. Radiology 1996; 199:567-570.[Abstract/Free Full Text]
-
Mannion JD, Buckman PD, Magno MG, Dimeo F. Collateral blood flow from skeletal muscle to normal myocardium. J Surg Res 1992; 53:578-587.[Medline]
-
Beyer M, Beyer U, Mierdl S, Sirch J, van Behren H, Hannekum A. Indirect myocardial revascularisation: experimental study in the dog. Eur J Cardiothorac Surg 1994; 8:557-562.[Abstract]