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ORIGINAL ARTICLE

64-Slice Computed Tomography of Bovine Internal Mammary Artery Coronary Grafts

Andrea Colli, MD1,3, Alessandro Maria Budillon, PhD2, Filippo Cademartiri, MD, PhD2, Alessandro Palumbo, MD2, Erica Maffei, MD2, Tiziano Gherli, MD2

1 Department of Cardiac Surgery, Hospital Universitari Germans Trias i Pujols, Badalona, Barcelona, Spain
2 Department of Radiology, Azienda Ospedaliero, University of Parma, Parma, Italy
3 Department of Cardiac Surgery, Azienda Ospedaliero, University of Parma, Parma, Italy

Andrea Colli, MD, Email: colli.andrea.bcn{at}gmail.com, Department of Cardiac Surgery, Hospital Universitari Germans Trias i Pujols, Cra. Canyet sn 08916 Badalona, Barcelona, Spain.

ABSTRACT

In cases where conventional aortocoronary grafts cannot be used, No-React bovine internal mammary artery is a possible alternative. The aim of this study was to assess the patency and clinical performance of bovine internal mammary artery as a coronary bypass conduit, using 64-slice computed tomography coronary angiography. Eleven patients (mean age, 68.2 ±5.9 years) received 11 bovine grafts between 2002 and 2006. Eight of these patients were alive after a mean follow-up of 29.4 ±16.3 months. Their mean additive EuroSCORE was 6.5 ±3.2. The mean number of distal anastomoses was 2.5 ±0.5. Six grafts were anastomosed to the right coronary artery, 2 to the left anterior descending artery, and 3 to the circumflex artery. All 11 bovine grafts were found to be occluded after 14.1 ±3.6 months. This demonstrates very poor results with the bovine coronary graft, thus we do not recommend its use, and we suggest considering an hybrid approach in selected cases.

Key Words: Blood Vessel Prosthesis Implantation • Coronary Artery Bypass • Graft Occlusion • Vascular • Tomography • X-Ray Computed

INTRODUCTION

Patients undergoing coronary artery bypass grafting (CABG) currently present with increased age and risk profiles. In older patients, the quality of saphenous vein grafts may be impaired. Therefore, alternative bypass conduits may expand the revascularization possibilities. The use of arterial grafts (bilateral internal thoracic and radial arteries) has been shown to be the best option for such patients. However, arterial conduit harvesting is more time-consuming, and availability is limited. Many other natural and synthetic graft materials have been used, but none have achieved comparable success. Bovine internal mammary artery (BIMA) was introduced in 1986 as a graft for peripheral vascular surgery, and in 1989, it was proposed as a possible graft for CABG.13 Since then, clinical results with BIMA coronary grafts have been reported to be unsatisfactory, with a high rate of graft occlusion. To improve these results, the No-React treatment (Shelhigh, Inc., Union, NJ, USA) was applied to BIMA. No-React treatment is an established technique with increasing evidence of its ability to resist in-vitro and in-vivo calcification, attenuating the inflammatory process. Experience with No-React-treated pericardium, valves, and conduits is growing.4,5 The BIMA No-React conduit for CABG is available for restricted clinical use in Europe. After the poor results reported in the literature, we decided to review all patients treated with BIMA at our institution, using multislice computed tomography (MSCT) coronary angiography.

PATIENTS AND METHODS

Between January 2002 and January 2006, BIMA grafts (Shelhigh) were used in 11 of >2,000 patients who underwent CABG. Clinical follow-up and MSCT coronary angiography are considered routine follow-up procedures for our high-risk and symptomatic patients. All patients were asked to participate before and after the surgical intervention, and gave informed consent. Approval from the local ethical committee was waived because the follow-up of these patients was considered of clinical relevance and not different from the standard practice of the institution. We retrospectively reviewed the patient’s records; their characteristics are given in Table 1Go.


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Table 1. Baseline characteristics of 11 patients receiving bovine grafts
 
All distal coronary anastomoses were performed under warm blood cardioplegic arrest with moderate systemic hypothermia (34°C), using continuous 7/0 polypropylene sutures. The proximal BIMA-to-aorta anastomoses were undertaken with continuous 6/0 polypropylene sutures. Intravenous antibiotic prophylaxis with vancomycin and ampicillin/sulbactam was given to all patients. Transit-time flow measurements were carried out not in all patients to assess the quality of the grafts. Internal thoracic artery was harvested in 11 patients, but used in only 9, due to poor flow. Operative notes were reviewed for details of the BIMA target vessel. Clinical status and cardiac symptoms at the time of the last follow-up examination were recorded. All patients received standard antiplatelet therapy with aspirin and oral anticoagulants. Of these 11 patients, 8 were alive and underwent MSCT coronary angiography to assess their grafts.

Exclusion criteria for MSCT were atrial fibrillation, renal insufficiency (serum creatinine >120 mmol·L–1), known allergy to iodine contrast medium, and pregnancy. The studies were performed with a cardiac-optimized 64-slice MSCT Sensation 64 (Siemens, Forchheim, Germany). A bolus of 100 mL Iomeron (400 mg iodine per mL; Bracco, Milan, Italy) was injected intravenously (4 to 5 mL·s–1), followed by 50 mL of saline at the same rate, using a double-head injector (Stellant; MedRAD, Pittsburgh, PA, USA). To trigger the start of the scan, a real-time bolus tracking technique was used. During the scan, which was performed during an inspiratory breath hold of 14 sec, the MSCT data and electrocardiogram (ECG) trace were acquired. Scan parameters were: individual detector collimation 32 x2 x0.6 mm, tube voltage 120 kV, 900 mAs, gantry rotation time 330 ms. No ECG pulsing was used. Reconstruction parameters were: effective slice width 0.75 mm, reconstruction increment 0.4 mm, and standard convolution filters. Axial slices synchronized to the recorded ECG were reconstructed from the acquired MSCT data in the mid- to end-diastolic phase, during which coronary artery displacement is relatively small, with reconstruction window positions starting at 400 ms before the next R wave and/or at 75% of the R-to-R interval. If indicated, additional temporal window positions were explored, including the end-systolic phase, to obtain images with the least motion artefacts. Two experienced cardiovascular radiologists evaluated MSCT scans in consensus, blinded to clinical findings but aware of previous cardiac history; the evaluation was preformed on axial slices, multiplanar and curved reconstructions, and 3-dimensional volume-rendering reformats. A graft was judged patent when the intravascular attenuation and lumen diameter were regular from the proximal anastomosis/ostium to the distal anastomosis. Significant stenosis was defined as a focal reduction of at least 50% of the lumen diameter, as measured by calipers with a proximal reference vessel. Occlusion was defined as the lack of intravascular attenuation within the graft. The absence of distal run-off in the native vessel was also used as a criterion for occlusion.

RESULTS

Five (45.4%) cases were re-interventions. The reasons for using BIMA grafts were poor quality of the saphenous veins in all 11 patients, and in 3 of them, radial artery harvesting was not possible due to a pathological Allen’s test. The use of BIMA was always decided during the operation because of specific surgical conditions, and not predetermined. Of the 11 BIMA grafts implanted, 6 (54.5%) were used for the right coronary artery (RCA), 2 (18.2%) for the left anterior descending artery (LAD), and 3 (27.3%) were anastomosed to the obtuse marginal artery (Table 2Go). No BIMA was used as a sequential bypass graft. There were no apparent differences in the quality and diameters of the target vessels at the site of the distal anastomoses. Good quality of the target vessel was reported in nearly 30% of the distal anastomoses sites in all 3 vessels, and the diameter of the LAD was slightly greater than the diameters of the obtuse marginal and RCA. At follow-up, 8 (73%) of the 11 patients treated with BIMA were alive (Table 3Go). Two died during the hospital stay; both had received a BIMA graft to the LAD. An autopsy was performed in only one patient, which showed complete graft occlusion from the proximal to the distal part of the BIMA, not including the anastomosis site. Both hospital deaths occurred in patients undergoing emergency surgery; one for LAD dissection after a percutaneous coronary intervention, and the other for perforation of the coronary arterial wall. The 3rd patient died from untreatable acute pulmonary edema 3 months after the intervention; this patient had a BIMA graft to the circumflex artery. Eight patients underwent MSCT coronary angiography after a mean follow-up of 14.1 ±3.6 months. All of their BIMA grafts were occluded (Figures 1Go and 2Go). The mean ejection fraction was 51.4% ±19.6% after 29.4 ±16.3 months of clinical follow-up. Six patients (75% of survivors) were asymptomatic at the time of follow-up, and 2 suffered both recurrent angina and heart failure symptoms (Table 3Go). The patency of the internal thoracic artery was 100% for both the left and right sides, vein graft patency was 100%, and radial artery patency was 100%.


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Table 2. Coronary artery bypass grafts and outcome in 11 patients
 

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Table 3. Follow-up data of 11 patients with bovine grafts
 

Figure 1
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Figure 1. (A, B, C) Volume-rendering and curved multiplanar reformatted images of patent left internal mammary artery and venous grafts on the left coronary tree. (D, E) Volume-rendering images of the bovine graft: by changing window and shade settings, the closed bovine mammary graft can be seen (arrowheads along the right atrioventricular groove). (F) Curved multiplanar reformatted images showing complete thrombosis of the graft.

 

Figure 2
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Figure 2. (A, B, C) Volume-rendering and curved multiplanar reformatted images of a patent left internal mammary artery on the left anterior descending artery, with poor distal runoff of the native vessel, and a free right internal mammary artery graft on the marginal branch, with good distal native run-off. (D) Volume-rendering image of a bovine graft: by changing window and shade settings, a closed bovine mammary graft can be seen (arrowheads along the right atrioventricular groove). (E, F) Curved multiplanar reformatted images showing complete thrombosis of the graft.

 
DISCUSSION

Internal thoracic artery remains the most successful material for CABG, and autologous vein is an established conduit for myocardial revascularization. Experience with other arterial conduits is limited, but the results are constantly improving. As an increasing number of patients undergo repeat coronary surgical procedures for which no adequate autologous arterial or venous conduits are available, it will be a challenge to find a biologic small-diameter substitution graft. Many small-caliber vascular grafts for use as CABG conduits have been developed in the past, but most of them have failed.6,7 Experimental data with low-flow biologic grafts in the aortocoronary position suggest that all types of these grafts are prone to early occlusion.8,9

The use of BIMA was first reported in 1989 by Suma and colleagues2 who showed that 4 of 5 BIMA grafts were patent at 2 months. The same group confirmed their findings a few years later.10 Subsequent reports have not been so satisfactory, with poor midterm results.7,9,11 Craig and Walker9 reported an almost 50% occlusion rate in the total population, and 100% occlusion in patients studied by coronary angiography. Mitchell and colleagues7 reported a 15.8% patency rate after follow-up of 3–23 months. Esposito and colleagues11 concluded that there was a poor patency rate of <50% with the BIMA graft. The No-React BIMA was developed as an alternative CABG conduit to improve patency results. The No-React treatment has been described as having antiinflammatory and anticalcification properties, and preventing foreign-body reaction.4,5 Ostapczuck and colleagues12 evaluated the patency and histologic changes of BIMA after implantation as an aortocoronary graft in animals. Macroscopically, multiple calcifications were present in all explanted grafts.

Occlusion of all grafts was the result of a severe inflammatory reaction with cellular infiltration, specific for chronic rejection; all histologic specimens showed intimal hyperplasia, lymphocyte infiltration, and foreign body reaction. They concluded that the No-React II treatment of BIMA was insufficient to avoid immunologic reactions and calcification. Experimental data of Walther and colleagues13 showed massive calcification in No-React-treated aortic wall specimens compared to BiLinx, AOA, and standard glutaraldehyde pretreatment. Similar results were obtained by Jashari and colleagues14 who evaluated No-React BIMA in vivo in a sheep model and revealed progressively increasing calcification at 3–6 months, with minimal inflammatory changes and preservation of the inner surface and ultrastructure. Preliminary clinical results showed a patency rate of 57% at a follow-up of 2.5 years. Graft patency was investigated with cardiac magnetic resonance imaging; however, these results were obtained in only 6 patients revascularized with 7 No-React BIMA grafts.15 More recently, Engleberger and colleagues16 assessed 19 No-React BIMA grafts in 17 (2.9%) of 572 patients undergoing CABG. Follow-up was complete in 12 patients with 13 BIMA grafts: 9 (69.2%) in the right coronary system, 2 (15.4%) on the LAD, and 2 on the circumflex artery. One patient died in hospital due to multiorgan failure, and 4 refused invasive assessment. Follow-up data including clinical status and coronary angiography were obtained at 7.0 ±4.0 months after the initial surgery: mean perioperative BIMA graft flow was 71 ±60 mL·min–1. Graft patency was 23.1%, and it was independent of the intraoperative flow measurement.

In our experience, alternative grafts are rarely required in patients undergoing CABG. The use of radial artery in our institution has helped to solve the problem when the quality of saphenous vein is insufficient. In our population, BIMA was anastomosed to the RCA and its posterior descending branch in the majority of patients (54.5%). One survivor who received a BIMA graft to the circumflex artery subsequently presented with a posterolateral ventricular aneurysm and greatly reduced ejection fraction. In the preoperative echocardiographic assessment, there was normal contractility and no sign of a ventricular aneurysm. This patient is symptomatic with chronic heart failure despite a high dosage of medical treatment.

The small number of patients in this study is the main limitation. Another important limitation is the absence of postmortem studies. Use of cardiac MSCT to assess graft patency may be considered a limitation; however, Martuscelli and colleagues17 and Malagutti and colleagues18 reported sensitivity of 97%–99% and specificity of 100%–96% compared with conventional coronary angiography in evaluation of CABG patency. These values are all in the range of 100% for CABG occlusion. The optimal results of MSCT and the intrinsically higher risk of conventional coronary angiography in these patients justified the use of 64-slice MSCT coronary angiography.

It was concluded that BIMA grafts have a very poor patency rate, thus we do not consider them suitable for CABG. Our recommendation is that they should be limited to emergency interventions only, due to the high rate of mortality found in our retrospective analysis. Midterm patency is unpredictable and independent of the intraoperative flow rate. Before considering the No-React BIMA graft as last resort, we suggest evaluating other autologous conduits not usually harvested, such as the gastroepiploic artery, inferior epigastric artery, lateral femoral circumflex artery, the short saphenous vein, cephalic vein, and the basilic vein of the arm. A hybrid procedure is another possible strategy that could be considered in highly selected cases. In specific situations, a combination of cardiac revascularization surgery and percutaneous revascularization, based on the target vessels and conduits in each candidate, could produce an important improvement in clinical results.

REFERENCES

  1. Stertmann WA, Scheld HH, Kubicek J, Fitz H, Lukas H, Schulze H. A modified technique for the production of an arterio-venous shunt in sheep, allowing a comparison of biocompatibility of synthetic materials. Lab Anim 1990;24:44–7.[Abstract/Free Full Text]

  2. Suma H, Oku T, Sato H, Sawada Y, Takeuchi A. Clinical experience of bovine internal mammary artery graft (Bioflow) for coronary artery bypass surgery. Nippon Kyobu Geka Gakkai Zasshi 1989;37:1965–8.[Medline]

  3. Donzeau-Gouge P, Touati G, Vouhé PR, Roy A, Farge C, Leca F, et al. Coronary artery bypass with bovine internal mammary artery graft. Arch Ma1 Coeur Vaiss 1990;83:1811–5.

  4. Abolhoda A, Yu S, Oyarzun JR, Allen KR, McCormick JR, Han S, et al. No-React detoxification process: a superior anticalcification method for bioprostheses. Ann Thorac Surg 1996;62:1724–30.[Abstract/Free Full Text]

  5. Abolhoda A, Yu S, Oyarzun JR, McCormick JR, Bogden JD, Gabbay S. Calcification of bovine pericardium: glutaraldehyde versus No-React biomodification. Ann Thorac Surg 1996;62:169–74.[Abstract/Free Full Text]

  6. Tomizawa Y. Vascular prostheses for aortocoronary bypass grafting: a review. Artif Organs 1995;19:39–45.[Medline]

  7. Mitchell IM, Essop AR, Scott PJ, Martin PG, Gupta NK, Saunders NR, et al. Bovine internal mammary artery as a conduit for coronary revascularization: long-term results. Ann Thorac Surg 1993;55:120–2.[Abstract/Free Full Text]

  8. Tomizawa Y, Moon MR, DeAnda A, Castro LJ, Kosek J, Miller DC. Coronary bypass grafting with biological grafts in a canine model. Circulation 1994;11(Suppl II)160–6.

  9. Craig SR, Walker WS. The use of bovine internal mammary artery (Bioflow) grafts in coronary artery surgery. Eur J Cardiothorac Surg 1994;8:43–5.[Abstract/Free Full Text]

  10. Suma H, Wanibuchi Y, Takeuchi A. Bovine internal thoracic artery graft for myocardial revascularization: late results. Ann Thorac Surg 1994;57:704–7.[Abstract/Free Full Text]

  11. Esposito F, Vitale N, Crescenzi B, Scardone M, de Luca L, Cotrufo M. Short-term results of bovine internal mammary artery use in cardiovascular surgery. Tex Heart Inst J 1994;21:193–7.[Medline]

  12. Ostapczuk S, Poniewierski J, Thiel A, Knieriem HJ, Orlowski T, Rakhorst G, et al. Evaluation of a porcine internal mammary artery (No-React II) as a small-diameter conduit. Ann Thorac Surg 1998;66:115–7.

  13. Walther T, Falk V, Autschbach R, Diegeler A, Rauch T, Weigl C, et al. Comparison of different anticalcification treatments for stentless bioprostheses. Ann Thorac Surg 1998;66:S249–54.[Medline]

  14. Jashari R, Herijgers P, Verbeken E, Van Lommel A, Nishimura Y, Ràcz R, et al. Calcification and degeneration characteristics of the Biocor no-react bovine internal mammary artery (BIMA)—in vivo evaluation in a sheep model. Cardiovasc Surg 2001;9:44–9.[Medline]

  15. Reddy SL, Pillai J, Mitchell L, Naik S, Dark J, Hasan A, et al. First report of No-React bovine internal mammary artery performance and patency. Heart Surg Forum 2004;7:E446–9.[Medline]

  16. Englberger L, Noti J, Immer FF, Stalder M, Eckstein FS, Carrel TP. The Shelhigh No-React bovine internal mammary artery: a questionable alternative conduit in coronary bypass surgery? Eur J Cardiothorac Surg 2008;33:222–4.[Abstract/Free Full Text]

  17. Martuscelli E, Romagnoli A, D’Eliseo A, Tomassini M, Razzini C, Sperandio M, et al. Evaluation of venous and arterial conduit patency by 16-slice spiral computed tomography. Circulation 2004;110:3234–8.[Abstract/Free Full Text]

  18. Malagutti P, Nieman K, Meijboom WB, van Mieghem CA, Pugliese F, Cademartiri F, et al. Use of 64-slice CT in symptomatic patients after coronary bypass surgery: evaluation of grafts and coronary arteries. Eur Heart J 2007;28:1879–85.[Abstract/Free Full Text]

Asian Cardiovasc Thorac Ann 2010; 18:59-64
© 2010 by SAGE Publications
DOI: 10.1177/0218492309355721




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