Original Cardiovascular
One-Year Patency of Valvulotomized Vein Grafts Is Similar to That of Arterial Grafts Nadejda Monsefi1 Andreas Zierer1 Gazal Honarpisheh1 Andres Beiras-Fernandez1 Anton Moritz1 1 Department of Thoracic and Cardiovascular Surgery, Goethe
University Hospital, Frankfurt a.M., Germany 2 Department of Diagnostic and Interventional Radiology, Goethe University Hospital, Frankfurt a.M., Germany
Ralf Bauer2
Matthias Kerl2
Address for correspondence Nadejda Monsefi, MD, Department of Thoracic, and Cardiovascular Surgery, Goethe University Hospital, Theodor-Stern-Kai 7, Frankfurt a.M. 60590, Germany (e-mail: [email protected]).
Abstract
Keywords
► coronary artery bypass grafting ► computed tomography ► outcomes
Background Inferior vein graft patency after coronary artery bypass grafting (CABG) is attributed to various factors. Venous valves may limit flow, cause thrombus formation, and diminish diastolic backflow. The aim of our study was to compare clinical outcome and midterm patency rate of valvulotomized vein grafts and arterial grafts in patients undergoing CABG. Methods Between 2007 and 2010, valvulotomized saphenous vein segments were used to graft the right coronary artery (RCA) in 147 patients undergoing CABG with mean 2.8 1 arterial and 1.5 0.6 venous anastomoses. Outcome, reintervention, and reoperation were assessed after 4 1.6 years. Intraoperative bypass flow rate was measured before and after valvulotomy of venous bypass grafts in 12 patients. Patency of the grafts was assessed by means of multislice computed tomography (MSCT) in 45 patients. Results A total of 102 patients underwent isolated CABG and 45 had combined procedures. In-hospital mortality was 2%. At 4 years’ clinical follow-up, 95% of the patients were asymptomatic. Five patients underwent recoronary angiography because of angina pectoris. The MSCT and reangiography patency rate of all valvulotomized saphenous vein grafts was 97.1 versus 95.8% of arterial grafts 18 6 months postoperatively. Intraoperative measurements showed a significant increase (þ20.2 mL/min; p ¼ 0.01) of flow in the venous bypass grafts to the RCA after valvulotomy. There were no reoperations at the latest follow-up. Conclusion Patients with valvulotomized venous grafts had good clinical outcome. The one-year patency rate of those grafts is comparable to that of arterial grafts. However, long-term results and angiography studies will be needed to strengthen these findings.
Introduction The importance of coronary artery bypass grafting (CABG) for the treatment of coronary artery disease (CAD) has been reemphasized by the Syntax trial.1 The four-year results,
received December 24, 2014 accepted after revision February 9, 2015
especially in patient groups with severe coronary artery sclerosis, are significantly superior to interventional treatment. These results could be achieved, although the majority of patient underwent “classical” bypass surgery using one internal mammary artery graft and vein grafts, indicating
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that, despite many efforts of increasing arterial grafting, saphenous vein grafts are still broadly used for bypass surgery. The superior patency rate of the left internal mammary artery (LIMA) and its impact on long-term survival have been described in classical papers from the Cleveland Clinic.2 This improvement in clinical course, however, has never been proven in a significant number of randomized patients. Furthermore, studies on vein graft degeneration are mostly based on symptom-driven angiographies and thus might overestimate the vein graft degeneration rate. Randomized studies, using vein grafts for the second best territory, report on a five-year patency rate of approximately 90% for vein grafts.3 Vein grafts have several disadvantages compared with arterial grafts—namely, diameter mismatch, a different physiology of endothelial lining and vasomotor regulation, and vein valves. Mills4 has described the vein valves as “bad guys” in coronary surgery. Vein valves might be responsible for hemodynamic relevant stenosis, thrombus formation, and early induction of atherosclerosis. Furthermore, experimental data show improved flow behavior after valvulotomy.5,6 There is also evidence of improved patency rates of valvulotomized vein grafts in the so-called horseshoe grafts, where one limb of these grafts has been used nonreversed and valvulotomized.7 Most disadvantages of venous valves should have an impact on early patency, so the aim of our study was to evaluate whether early to midterm patency of vein grafts can be improved by systematic valvulotomy and further we wanted to prove whether flow rate can be changed by valvulotomy in the clinical setting. Midterm clinical outcome was also examined.
Patients and Methods From November 2007 to January 2010, 147 patients (20 female, 127 male) with CAD underwent elective CABG. Inclusion criterion was a valvulotomized venous graft to the right coronary artery (RCA). It was a single surgeon’s study. The anterior wall was always revascularized with the LIMA; in 88 cases, it was used sequentially to graft a diagonal branch and the left anterior descending. Revascularization of the circumflex territory was decided on patient’s risk factors and graft availability. In the majority, the right internal mammary artery (RIMA) was used (n ¼ 74, 44 sequential), in 45 cases a vein graft was used (14 sequential), and in 15 a radial artery (RA) was used (8 sequential). All vein grafts had been valvulotomized unless they have been free of valves primarily. On average, 2.8 1 arterial and 1.5 0.6 venous anastomoses had been performed per patient. Ninety-four percent of the patients were in NYHA and CCS class II. Mean age was 69 9 years (range 40–86 years). Patient demographics are shown in ►Table 1. All 147 patients received valvulotomized venous bypass grafts to the RCA. Intraoperative bypass flow rate was measured before and after valvulotomy of the venous bypass graft to the RCA after weaning off cardiopulmonary bypass (CPB) in 12 patients. These 12 patients had severe stenosis (80%) or occlusion of Thoracic and Cardiovascular Surgeon
Table 1 Patient characteristics Variable list N
147
Age
69 9
Female
20
Male
127
CCS II–III
129 (88%)
NYHA II–III
138 (94%)
Former myocardial infarction
18 (12%)
PCI/stent
22 (15%)
Hypertension
111 (76%)
Hypercholesterolemia
67 (46%)
COPD
16 (11%)
Renal insufficiency
20 (14%)
Diabetes
41 (28%)
Coronary artery disease Three-vessel disease
124 (85%)
Two-vessel disease
18 (12%)
One-vessel disease
5 (3%)
EF
52 1%
Abbreviations: CCS, Canadian Cardiovascular Society Angina Classification; COPD, chronic obstructive pulmonary disease; EF, ejection fraction; NYHA, New York Heart Association classification; PCI, percutaneous coronary intervention.
the RCA. The study was approved by our institutional ethics committee.
Operative Procedure Intraoperative selection of suitable veins was made with direct palpation and visual inspection. The great saphenous vein was harvested starting at the level of the ankle. We prepared the vein with the surrounding adventitia. Side branches were ligated or clipped. The distal end of the vein was cannulated. Venous valves were identified by visual inspection and probing. In 128 cases, the valvulotomy was made before the reversed vein was anastomosed to the coronary artery using a valve scissors (Ulrich medical, Ulm, Germany). In seven cases, the valve scissors could not be inserted safely; therefore, distal anastomoses were performed first and vein valves were cut after pressurizing the vein by retrograde flow after cross-clamp release with the Mills valvulotome (Pilling/Teleflex medical, Kernen, Germany). In 12 cases, the distal and proximal anastomoses were performed and CPB was discontinued; after that the valvulotomy was made through a side branch of the vein. Flow measurements were done before and after valvulotomy in these 12 cases. The selection of the RA as a conduit has been described before by our institution.8 The LIMA was harvested as venoarterial pedicle.9 Low-voltage cautery was always used, and the side branches were clipped. Then the artery was
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Valvulotomized Vein Grafts
Valvulotomized Vein Grafts
Postoperative Evaluation and Management Patients were clinically followed by means of letter or phone call for at least 1 year. Follow-up was completed in 97% of the patients at 4 1.6 years. Freedom from angina, myocardial infarction, angiographic reintervention, and reoperation was analyzed at follow-up. Results of five coronary angiographies performed during follow-up were retrieved from referring cardiologists, and CCS and NYHA status as well as patency of the grafts was analyzed. Multislice computed tomography (MSCT) was performed in patients with atypical chest pain to rule out graft dysfunction.
Table 2 Perioperative results and surgical procedures Variable list On pump
141 (96%)
CPB time mean (min)
155 42
Cross-clamp time mean (min)
110 30
Number of anastomoses (mean)
4.3 1
Arterial
2.8 1 (mean)
Venous
1.5 0.6 (mean)
Number of grafts (number of anastomoses)
592
LIMA to anterior wall
142, with 88 sequential (total 230)
RIMA to CX
74, with 44 sequential (total 118)
Radial Artery to CX
15, with 8 sequential (total 23)
Saphenous vein graft total
221
Saphenous vein graft to RCA
147, with 15 sequential (total 162)
Saphenous vein graft to CX
45, with 14 sequential (total 59)
Intraoperative Flow Measurement Flow assessment of valvulotomized vein grafts to the RCA was performed under stable hemodynamic conditions (mean arterial pressure [MAP] at 77 mm Hg), after termination of CPB in 12 patients. Flowmetry of the grafts was performed with a transit-time flow meter (VeriQ System; Medistim, Deisenhofen, Germany) and flow probes (QuickFit; Medistim, Deisenhofen, Germany). The technique has been described before.11 The mean flow was reported as mL/min and the MAP (mmHg) was recorded concomitantly.
Statistical Analysis Statistical analyses were performed with the BIAS 9.05 software (Frankfurt, Germany). Categorical variables are expressed as frequencies and percentages. Continuous variables are expressed as mean standard deviation. Flow measurements were evaluated by the Student t-test. Statistical significance was defined as a p-value less than 0.05.
Results A total of 102 patients underwent isolated CABG and 45 had additional procedures like single valve procedure (23), multiple valve surgery (7), ventricular remodeling (12), or cryoablation (8). The operative and perioperative data are listed in ►Table 2. Thirty-day mortality was 2% (3/147). One patient suffered multiorgan failure and two died suddenly and unexpectedly after otherwise uneventful recovery. Follow-up was performed by letter or phone call. Ninetyfive percent were asymptomatic (CCS 0), 5% in CCS I
Concomitant procedures in 45 patients Aortic valve replacement
17
Mitral valve repair
10
Tricuspid valve repair
7
Ventricular remodeling
12
Cryoablation
8
ICU stay (d)
22
Ventilation time (h)
22 32
Neurological deficit: (PND/TND)
0
Myocardial infarction
0
Reangiography/stent
0
30-d mortality
3 (2%)
Abbreviations: CBP, cardiopulmonary bypass; ICU, intensive care unit; LIMA, left internal mammary artery; PND, prolonged neurological deficit; RIMA, right internal mammary artery; TND, temporary neurological deficit; x-clamp, aortic cross-clamp.
(►Table 3). We observed 16 late deaths (2 patients died of pancreas carcinoma, 1 of lung cancer, 1 of leukemia, 2 of sepsis, 2 of pneumonia; 1 patient suffered from rupture of a duodenal ulcer; in 7 patients the cause of death was unknown). Five patients underwent reangiography of the coronary arteries because of angina pectoris. In two cases, all bypasses were patent and there was no need for intervention; in the third and fourth case, a de novo stenosis of the obtuse marginal branch was treated with a stent (all bypasses were patent). In the fifth case, the valvulotomized vein graft to the Thoracic and Cardiovascular Surgeon
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wrapped in gauze soaked with spasmolytic solution. In all patients, CABG was performed through a median sternotomy, and the left anterior descending artery was always grafted using the LIMA. After CPB was instituted, the temperature was reduced to 32°C. Myocardial protection was achieved by using tepid blood potassium cardioplegia in combined procedures or Calafiore solution10 for isolated CABG surgery. The distal anastomoses were performed using 7/0 Prolene for vein grafts and 8/0 Prolene for arterial graft anastomoses, respectively. Proximal anastomoses were completed in single-clamp technique in cases of atherosclerosis of the aorta and after release of the aortic cross-clamp in all other cases using a side-biting clamp.
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Table 3 Follow-up data Variable list Myocardial infarction
2 (1.6%)
Coronary reangiography
5 (4%)
CCS CCS 0
117(95%)
CCS I
6 (5%)
NYHA NYHA I
103 (84%)
NYHA II
19 (15%)
Neurological event TND
2 (1.6%)
76.9 16 mm Hg before and 95.6 46 mL/min at 76.3 14 mm Hg after valvulotomy of the venous bypass grafts to the RCA, as shown in ►Fig. 1. The mean pulsatility index increased from 1.6 0.6 before to 2.1 1.3 after valvulotomy (p ¼ 0.01). Out of the 45 patients who underwent MSCT scan of the heart, 1 patient had an occlusion of the valvulotomized venous bypass graft to the RCA and 2 had an occlusion of the RIMA to the circumflex artery. We analyzed the 45 MSCT and 5 coronary reangiographies: the patency rate of the valvulotomized saphenous vein grafts was 97.1 versus 95.8% in the arterial grafts after 18 6 month postoperatively. An example of MSCT scan of the heart showing the valvulotomized bypass graft to the RCA without occlusion is shown in ►Fig. 2.
Reoperation
0
Late mortality
16 (11%)
Discussion
CT scan of the heart
45 (31%)
Based in numerous studies demonstrating superior patency rates of the internal thoracic and radial arteries in comparison to venous grafts,12–14 there is a shift to total arterial revascularization in coronary surgery. Arterial revascularization in the CABG group was also performed in the Syntax trial, where one or more arterial grafts were used in 97.3% of the patients. The Syntax trial could show the superiority of coronary artery bypass surgery in comparison to stent implantation in patients with complex coronary morphology. Despite the fact that in 97% of the cases an arterial graft has been used, only a minority of patients received a second arterial graft.15,16 Currently, still a minority of patients receive more complex arterial revascularization. However, the total arterial revascularization strategy shows different results clinically. The data of You et al indicate that patients undergoing composite bilateral internal thoracic artery (BITA) plus right gastroepiploic artery (RGEA) grafting in off-pump coronary artery bypass grafting appear to have a significantly lower cardiac-related readmission rate than patients undergoing BITA grafting for triple-vessel disease.
Results of 5 reangiographies and 45 CTscans Patency rate of venous BG to the RCA
96% (2/50 occluded)
Patency rate of venous BG to the CX
100% (0/19 occluded)
Patency rate of venous anastomoses to the RCA
96.5% (2/57 occluded)
Patency rate of all venous BG
97.1% (2/69 occluded)
Patency rate of arterial BG
95.8% (3/72 occluded)
Patency rate of arterial anastomoses
96.6% (4/116 occluded)
Patency rate of LIMA graft to anterior wall
100% (0/49 occluded)
Patency rate of RIMA graft to CX
84% (3/19 occluded)
Patency rate of radial artery graft to CX
100% (0/4 occluded)
Abbreviations: BG, bypass graft; CCS, Canadian Cardiovascular Society Angina Classification; CT, computed tomography; NYHA, New York Heart Association classification; TND, temporary neurological deficit.
RCA was occluded and the sequential, free mammary artery bypass to the ramus circumflexus (RCX) was blocked at the proximal anastomosis. In this case, the stenosis of the RCA had regressed and the circumflex artery was stented. No patient had to undergo a redo surgical procedure. Intraoperative flow measurements of 12 patients were performed to evaluate the differences in flow before and after valvulotomy. Flowmetry showed a significant increase of the flow rate of the venous bypass graft to the RCA after valvulotomy (mean increase þ20.2 mL/min; p ¼ 0.01). We measured a mean flow of 75.4 31 mL/min at a MAP of Thoracic and Cardiovascular Surgeon
Fig. 1 Flow measurement of venous bypass graft after discontinuation of cardiopulmonary bypass before and after valvulotomy through a side branch.
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Valvulotomized Vein Grafts
Fig. 2 MSCT scan of the heart showing the valvulotomized bypass to RCA without occlusion.
During 17.7-month follow-up period, the cardiac-related readmission rate was higher in the patient group who underwent CABG with sole composite BITA grafts (9.9%) compared with composite BITA plus in-situ RGEA grafts (2.2%).17 Glineur et al enrolled 152 patients in a systematic 6-month angiographic follow-up study to analyze the function of the right internal thoracic artery (RITA) used in a Y-graft configuration. They found out that a total of 25.3% of RITA anastomoses were not functional. The function of the RITA used as a Y-graft was significantly improved when used on several branches of the circumflex artery or on a severely narrowed first circumflex. Grafting of the intermediate branch or of a RCA had a negative prognostic influence on graft function.18 Furthermore, Mohammadi et al could show that the additional survival benefit of using a second ITA—compared with single ITA—was lost after 60 years of age, even in low-risk patients in a 5.7-year follow-up.19 The use of bilateral ITA is also associated with significant sternal devascularization and higher risk of infectious complications20 at least in subgroups of patients such as those suffering from diabetes, obesity, or chronic pulmonary artery disease. The use of RA grafts seems to be logical based on the assumption that their long-term patency is similar to ITA’s and will be better than the patency of venous conduits.7 Maniar et al presented their data with RA used as either an aortocoronary (RA-ao) or composite graft (T-graft) at 26month follow-up. They found that patients with RA-ao grafts had a greater incidence of postoperative angiography versus patients with composite grafts (19 vs 11%); p < 0.01) and that patients receiving T-graft had a greater number of anastomoses per patient (4.1 0.6 vs 3.0 1, p < 0.01).21 Furthermore, Khot et al reported higher patency rates of saphenous vein grafts than radial arteries22: at a mean follow-up of 565 days angiography, results showed that RA grafts had a patency rate of 51.3%, which was significantly lower than that for LITAs (90.3%) or saphenous vein grafts (64%). RA grafts had an occlusion rate of 33.7%, compared with 4.8% for LITAs, 11.7% for RITAs, and 30.1% for saphenous vein grafts. Maniar and collegues who investigated a series of T-grafting
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using the RA could show that the patency of anastomoses to the RCA was only 58% after 26-month follow-up.21 Buxton et al investigated the graft patency in several randomized series. Three-year patency rate of saphenous vein grafts was 90% and comparable to that of RA grafts of 91% when used for the second best territory.23 Clinically, equivalence of radial arteries and vein grafts is maintained at least up to 6 years.24 Other experimental and clinical trials showed the value of valvulotomized saphenous vein grafts as conduits. Fogarty et al used 110 segments of cadaveric greater saphenous vein in their flow studies and could show significantly increased flow rates after valvulotomy in segments with diameters less than 2.5 mm.5 In another experimental study, Thubrikar et al examined pressure and flow in the femoropopliteal reversed vein graft with competent valves: when reducing the flow, the vein valve opens and closes which results in a pressure trap, reduction of pulse pressure, and flow stagnation that is also known as “trap phenomenon.”6 ►Fig. 3 shows a well visible and stenotic vein valve (arrow) of a saphenous vein graft to the RCA in a reangiography examination. In clinical studies, Urschel et al could prove improved patency rates of valvulotomized vein grafts in the so-called horseshoe grafts, where one limb of these grafts has been used nonreversed and valvulotomized.7 Molina’s study indicated a patency rate of 90% in nonreversed, valvulotomized saphenous vein grafts at 3.5-year follow-up.25 These results could be confirmed in our single center study. Our midterm follow-up data showed that patients with valvulotomized venous grafts have a good clinical outcome. There were only two cases of myocardial infarction, 84% of the patients were in NYHA functional class I, and 95% were in CCS functional class 0. Mortality rate during followup was 11% and in majority not cardiac related. This compares to midterm results of other series.2,19 There was no case of reoperation; only two patients were treated with a stent for a
Fig. 3 Coronary reangiography shows well visible and stenotic vein valve (arrow) of a saphenous vein graft to the right coronary artery. Thoracic and Cardiovascular Surgeon
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de novo stenosis and another one for proximal occlusion of a sequential RITA to the RCX. The rate of adverse cardiac or cerebrovascular events at 1 year was low. Our MSCT (45) and reangiography (5) data showed that the valvulotomized saphenous vein grafts had a patency rate of 97.1% after 18 6 months; all LIMA and RA grafts were patent, whereas three RIMA bypass grafts were occluded. This goes parallel to the data of Puskas et al.26 Our flow measurement data before and after valvulotomy of the saphenous vein bypass graft to the RCA corroborate the clinical findings mentioned above and support the thesis that valvulotomy optimizes flow dynamics of venous bypass grafts. We observed a significant increase of the flow rate after valvulotomy. It appears that eliminating one major drawback of vein grafts is able to establish midterm patency rates similar to that of arterial grafts. This goes in parallel to former clinical findings on valvulotomized vein grafts. Valvulotomized venous grafts have similar 1-year patency rates as arterial grafts. Midterm clinical outcome is comparable as 95% of the patients were free from angina, 84% were in NYHA functional class I, and no patient underwent reoperation. However, long-term results and angiography studies will be needed to strengthen these findings.
4 Mills NL. Saphenous vein graft valves: “the bad guys”. Ann Thorac
Surg 1989;48(5):613–614 5 Chin AK, Mayer DN, Goldman RK, Lerman JA, Olcott C IV, Fogarty
6
7
8
9
10
11
12
13
Study Limitations Only 50 of 147 patients underwent CT scan of the heart or reangiography because of angina pectoris. Here a higher number of follow-up imaging is necessary to strengthen the findings. Furthermore, long-term follow-up data (5–10 years) is necessary, which is very important for this cohort. Finally, a randomized prospective trial with the patient groups valvulotomized/nonvalvulotomized vein grafts would be of great interest for further investigations.
Note The abstract was presented at the DGTHG Annual Meeting in Freiburg in 2012.
14
15
16
17
18
Disclosure There is no conflict of interest to be disclosed.
19
20
References 1 Serruys PW, Morice MC, Kappetein AP, et al; SYNTAX Investigators.
Percutaneous coronary intervention versus coronary-artery bypass grafting for severe coronary artery disease. N Engl J Med 2009;360(10):961–972 2 Lytle BW, Blackstone EH, Loop FD, et al. Two internal thoracic artery grafts are better than one. J Thorac Cardiovasc Surg 1999; 117(5):855–872 3 Hayward PA, Gordon IR, Hare DL, et al. Comparable patencies of the radial artery and right internal thoracic artery or saphenous vein beyond 5 years: results from the Radial Artery Patency and Clinical Outcomes trial. J Thorac Cardiovasc Surg 2010;139(1):60–65, discussion 65–67 Thoracic and Cardiovascular Surgeon
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TJ. The effect of valvulotomy on the flow rate through the saphenous vein graft: clinical implications. J Vasc Surg 1988;8(3): 316–320 Thubrikar MJ, Robicsek F, Fowler BL. Pressure trap created by vein valve closure and its role in graft stenosis. J Thorac Cardiovasc Surg 1994;107(3):707–716 Lajos TZ, Robicsek F, Thubrikar M, Urschel H. Improving patency of coronary conduits “valveless” veins and/or arterial grafts. J Card Surg 2007;22(2):170–177 Risteski PS, Akbulut B, Moritz A, Aybek T. The radial artery as a conduit for coronary artery bypass grafting: review of current knowledge. Anadolu Kardiyol Derg 2006;6(2):153–162 Wimmer-Greinecker G, Yosseef-Hakimi M, Rinne T, et al. Effect of internal thoracic artery preparation on blood loss, lung function, and pain. Ann Thorac Surg 1999;67(4):1078–1082 Calafiore AM, Teodori G, Bosco G, et al. Intermittent antegrade warm blood cardioplegia in aortic valve replacement. J Card Surg 1996;11(5):348–354 Ricci M, Karamanoukian HL, Salerno TA, Dancona G, Bergsland J. Role of coronary graft flow measurement during reoperations for early graft failure after off-pump coronary revascularization. J Card Surg 1999;14(5):342–347 Chen AH, Nakao T, Brodman RF, et al. Early postoperative angiographic assessment of radial grafts used for coronary artery bypass grafting. J Thorac Cardiovasc Surg 1996;111(6):1208–1212 da Costa FD, da Costa IA, Poffo R, et al. Myocardial revascularization with the radial artery: a clinical and angiographic study. Ann Thorac Surg 1996;62(2):475–479, discussion 479–480 Tatoulis J, Buxton BF, Fuller JA, Royse AG. Total arterial coronary revascularization: techniques and results in 3,220 patients. Ann Thorac Surg 1999;68(6):2093–2099 Wu X, Chen Y, Liu H, et al. Comparison of long-term (4-year) outcomes of patients with unprotected left main coronary artery narrowing treated with drug-eluting stents versus coronaryartery bypass grafting. Am J Cardiol 2010;105(12):1728–1734 Head SJ, Mack MJ, Holmes DR Jr, et al. Incidence, predictors and outcomes of incomplete revascularization after percutaneous coronary intervention and coronary artery bypass grafting: a subgroup analysis of 3-year SYNTAX data. Eur J Cardiothorac Surg 2012;41(3):535–541 You JH, Lee TK, Kim WS. Bilateral internal thoracic artery (BITA) grafts vs. BITA with gastroepiploic artery (RGEA) grafts in offpump total arterial revascularisation of triple vessel disease. EACTS abstract no 183, 2008 Glineur D, Hanet C, D’hoore W, et al. Causes of non-functioning right internal mammary used in a Y-graft configuration: insight from a 6-month systematic angiographic trial. Eur J Cardiothorac Surg 2009;36(1):129–135, discussion 135–136 Mohammadi S, Dagenais F, Doyle D, et al. Age cut-off for the loss of benefit from bilateral internal thoracic artery grafting. Eur J Cardiothorac Surg 2008;33(6):977–982 De Paulis R, de Notaris S, Scaffa R, et al. The effect of bilateral internal thoracic artery harvesting on superficial and deep sternal infection: The role of skeletonization. J Thorac Cardiovasc Surg 2005;129(3):536–543 Maniar HS, Barner HB, Bailey MS, et al. Radial artery patency: are aortocoronary conduits superior to composite grafting? Ann Thorac Surg 2003;76(5):1498–1503, discussion 1503–1504 Khot UN, Friedman DT, Pettersson G, Smedira NG, Li J, Ellis SG. Radial artery bypass grafts have an increased occurrence of angiographically severe stenosis and occlusion compared with left internal mammary arteries and saphenous vein grafts. Circulation 2004;109(17):2086–2091 Shah PJ, Bui K, Blackmore S, et al. Has the in situ right internal thoracic artery been overlooked? An angiographic study of the radial artery,
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25 Molina JE. Nonreversed saphenous vein grafts for coronary artery
bypass grafting. Ann Thorac Surg 1989;48(5):624–627 26 Puskas JD, Williams WH, O’Donnell R, et al. Off-pump and on-
pump coronary artery bypass grafting are associated with similar graft patency, myocardial ischemia, and freedom from reintervention: long-term follow-up of a randomized trial. Ann Thorac Surg 2011;91(6):1836–1842, discussion 1842–1843
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internal thoracic arteries and saphenous vein graft patencies in symptomatic patients. Eur J Cardiothorac Surg 2005;27(5):870–875 24 Hayward PA, Hare DL, Gordon I, Buxton BF. Effect of radial artery or saphenous vein conduit for the second graft on 6-year clinical outcome after coronary artery bypass grafting. Results of a randomised trial. Eur J Cardiothorac Surg 2008;34(1): 113–117
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Thoracic and Cardiovascular Surgeon
One-Year Patency of Valvulotomized Vein Grafts Is Similar to That of Arterial Grafts Nadejda Monsefi1 Andreas Zierer1 Gazal Honarpisheh1 Andres Beiras-Fernandez1 Anton Moritz1 1 Department of Thoracic and Cardiovascular Surgery, Goethe
University Hospital, Frankfurt a.M., Germany 2 Department of Diagnostic and Interventional Radiology, Goethe University Hospital, Frankfurt a.M., Germany
Ralf Bauer2
Matthias Kerl2
Address for correspondence Nadejda Monsefi, MD, Department of Thoracic, and Cardiovascular Surgery, Goethe University Hospital, Theodor-Stern-Kai 7, Frankfurt a.M. 60590, Germany (e-mail: [email protected]).
Abstract
Keywords
► coronary artery bypass grafting ► computed tomography ► outcomes
Background Inferior vein graft patency after coronary artery bypass grafting (CABG) is attributed to various factors. Venous valves may limit flow, cause thrombus formation, and diminish diastolic backflow. The aim of our study was to compare clinical outcome and midterm patency rate of valvulotomized vein grafts and arterial grafts in patients undergoing CABG. Methods Between 2007 and 2010, valvulotomized saphenous vein segments were used to graft the right coronary artery (RCA) in 147 patients undergoing CABG with mean 2.8 1 arterial and 1.5 0.6 venous anastomoses. Outcome, reintervention, and reoperation were assessed after 4 1.6 years. Intraoperative bypass flow rate was measured before and after valvulotomy of venous bypass grafts in 12 patients. Patency of the grafts was assessed by means of multislice computed tomography (MSCT) in 45 patients. Results A total of 102 patients underwent isolated CABG and 45 had combined procedures. In-hospital mortality was 2%. At 4 years’ clinical follow-up, 95% of the patients were asymptomatic. Five patients underwent recoronary angiography because of angina pectoris. The MSCT and reangiography patency rate of all valvulotomized saphenous vein grafts was 97.1 versus 95.8% of arterial grafts 18 6 months postoperatively. Intraoperative measurements showed a significant increase (þ20.2 mL/min; p ¼ 0.01) of flow in the venous bypass grafts to the RCA after valvulotomy. There were no reoperations at the latest follow-up. Conclusion Patients with valvulotomized venous grafts had good clinical outcome. The one-year patency rate of those grafts is comparable to that of arterial grafts. However, long-term results and angiography studies will be needed to strengthen these findings.
Introduction The importance of coronary artery bypass grafting (CABG) for the treatment of coronary artery disease (CAD) has been reemphasized by the Syntax trial.1 The four-year results,
received December 24, 2014 accepted after revision February 9, 2015
especially in patient groups with severe coronary artery sclerosis, are significantly superior to interventional treatment. These results could be achieved, although the majority of patient underwent “classical” bypass surgery using one internal mammary artery graft and vein grafts, indicating
© Georg Thieme Verlag KG Stuttgart · New York
DOI http://dx.doi.org/ 10.1055/s-0035-1549009. ISSN 0171-6425.
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that, despite many efforts of increasing arterial grafting, saphenous vein grafts are still broadly used for bypass surgery. The superior patency rate of the left internal mammary artery (LIMA) and its impact on long-term survival have been described in classical papers from the Cleveland Clinic.2 This improvement in clinical course, however, has never been proven in a significant number of randomized patients. Furthermore, studies on vein graft degeneration are mostly based on symptom-driven angiographies and thus might overestimate the vein graft degeneration rate. Randomized studies, using vein grafts for the second best territory, report on a five-year patency rate of approximately 90% for vein grafts.3 Vein grafts have several disadvantages compared with arterial grafts—namely, diameter mismatch, a different physiology of endothelial lining and vasomotor regulation, and vein valves. Mills4 has described the vein valves as “bad guys” in coronary surgery. Vein valves might be responsible for hemodynamic relevant stenosis, thrombus formation, and early induction of atherosclerosis. Furthermore, experimental data show improved flow behavior after valvulotomy.5,6 There is also evidence of improved patency rates of valvulotomized vein grafts in the so-called horseshoe grafts, where one limb of these grafts has been used nonreversed and valvulotomized.7 Most disadvantages of venous valves should have an impact on early patency, so the aim of our study was to evaluate whether early to midterm patency of vein grafts can be improved by systematic valvulotomy and further we wanted to prove whether flow rate can be changed by valvulotomy in the clinical setting. Midterm clinical outcome was also examined.
Patients and Methods From November 2007 to January 2010, 147 patients (20 female, 127 male) with CAD underwent elective CABG. Inclusion criterion was a valvulotomized venous graft to the right coronary artery (RCA). It was a single surgeon’s study. The anterior wall was always revascularized with the LIMA; in 88 cases, it was used sequentially to graft a diagonal branch and the left anterior descending. Revascularization of the circumflex territory was decided on patient’s risk factors and graft availability. In the majority, the right internal mammary artery (RIMA) was used (n ¼ 74, 44 sequential), in 45 cases a vein graft was used (14 sequential), and in 15 a radial artery (RA) was used (8 sequential). All vein grafts had been valvulotomized unless they have been free of valves primarily. On average, 2.8 1 arterial and 1.5 0.6 venous anastomoses had been performed per patient. Ninety-four percent of the patients were in NYHA and CCS class II. Mean age was 69 9 years (range 40–86 years). Patient demographics are shown in ►Table 1. All 147 patients received valvulotomized venous bypass grafts to the RCA. Intraoperative bypass flow rate was measured before and after valvulotomy of the venous bypass graft to the RCA after weaning off cardiopulmonary bypass (CPB) in 12 patients. These 12 patients had severe stenosis (80%) or occlusion of Thoracic and Cardiovascular Surgeon
Table 1 Patient characteristics Variable list N
147
Age
69 9
Female
20
Male
127
CCS II–III
129 (88%)
NYHA II–III
138 (94%)
Former myocardial infarction
18 (12%)
PCI/stent
22 (15%)
Hypertension
111 (76%)
Hypercholesterolemia
67 (46%)
COPD
16 (11%)
Renal insufficiency
20 (14%)
Diabetes
41 (28%)
Coronary artery disease Three-vessel disease
124 (85%)
Two-vessel disease
18 (12%)
One-vessel disease
5 (3%)
EF
52 1%
Abbreviations: CCS, Canadian Cardiovascular Society Angina Classification; COPD, chronic obstructive pulmonary disease; EF, ejection fraction; NYHA, New York Heart Association classification; PCI, percutaneous coronary intervention.
the RCA. The study was approved by our institutional ethics committee.
Operative Procedure Intraoperative selection of suitable veins was made with direct palpation and visual inspection. The great saphenous vein was harvested starting at the level of the ankle. We prepared the vein with the surrounding adventitia. Side branches were ligated or clipped. The distal end of the vein was cannulated. Venous valves were identified by visual inspection and probing. In 128 cases, the valvulotomy was made before the reversed vein was anastomosed to the coronary artery using a valve scissors (Ulrich medical, Ulm, Germany). In seven cases, the valve scissors could not be inserted safely; therefore, distal anastomoses were performed first and vein valves were cut after pressurizing the vein by retrograde flow after cross-clamp release with the Mills valvulotome (Pilling/Teleflex medical, Kernen, Germany). In 12 cases, the distal and proximal anastomoses were performed and CPB was discontinued; after that the valvulotomy was made through a side branch of the vein. Flow measurements were done before and after valvulotomy in these 12 cases. The selection of the RA as a conduit has been described before by our institution.8 The LIMA was harvested as venoarterial pedicle.9 Low-voltage cautery was always used, and the side branches were clipped. Then the artery was
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Valvulotomized Vein Grafts
Valvulotomized Vein Grafts
Postoperative Evaluation and Management Patients were clinically followed by means of letter or phone call for at least 1 year. Follow-up was completed in 97% of the patients at 4 1.6 years. Freedom from angina, myocardial infarction, angiographic reintervention, and reoperation was analyzed at follow-up. Results of five coronary angiographies performed during follow-up were retrieved from referring cardiologists, and CCS and NYHA status as well as patency of the grafts was analyzed. Multislice computed tomography (MSCT) was performed in patients with atypical chest pain to rule out graft dysfunction.
Table 2 Perioperative results and surgical procedures Variable list On pump
141 (96%)
CPB time mean (min)
155 42
Cross-clamp time mean (min)
110 30
Number of anastomoses (mean)
4.3 1
Arterial
2.8 1 (mean)
Venous
1.5 0.6 (mean)
Number of grafts (number of anastomoses)
592
LIMA to anterior wall
142, with 88 sequential (total 230)
RIMA to CX
74, with 44 sequential (total 118)
Radial Artery to CX
15, with 8 sequential (total 23)
Saphenous vein graft total
221
Saphenous vein graft to RCA
147, with 15 sequential (total 162)
Saphenous vein graft to CX
45, with 14 sequential (total 59)
Intraoperative Flow Measurement Flow assessment of valvulotomized vein grafts to the RCA was performed under stable hemodynamic conditions (mean arterial pressure [MAP] at 77 mm Hg), after termination of CPB in 12 patients. Flowmetry of the grafts was performed with a transit-time flow meter (VeriQ System; Medistim, Deisenhofen, Germany) and flow probes (QuickFit; Medistim, Deisenhofen, Germany). The technique has been described before.11 The mean flow was reported as mL/min and the MAP (mmHg) was recorded concomitantly.
Statistical Analysis Statistical analyses were performed with the BIAS 9.05 software (Frankfurt, Germany). Categorical variables are expressed as frequencies and percentages. Continuous variables are expressed as mean standard deviation. Flow measurements were evaluated by the Student t-test. Statistical significance was defined as a p-value less than 0.05.
Results A total of 102 patients underwent isolated CABG and 45 had additional procedures like single valve procedure (23), multiple valve surgery (7), ventricular remodeling (12), or cryoablation (8). The operative and perioperative data are listed in ►Table 2. Thirty-day mortality was 2% (3/147). One patient suffered multiorgan failure and two died suddenly and unexpectedly after otherwise uneventful recovery. Follow-up was performed by letter or phone call. Ninetyfive percent were asymptomatic (CCS 0), 5% in CCS I
Concomitant procedures in 45 patients Aortic valve replacement
17
Mitral valve repair
10
Tricuspid valve repair
7
Ventricular remodeling
12
Cryoablation
8
ICU stay (d)
22
Ventilation time (h)
22 32
Neurological deficit: (PND/TND)
0
Myocardial infarction
0
Reangiography/stent
0
30-d mortality
3 (2%)
Abbreviations: CBP, cardiopulmonary bypass; ICU, intensive care unit; LIMA, left internal mammary artery; PND, prolonged neurological deficit; RIMA, right internal mammary artery; TND, temporary neurological deficit; x-clamp, aortic cross-clamp.
(►Table 3). We observed 16 late deaths (2 patients died of pancreas carcinoma, 1 of lung cancer, 1 of leukemia, 2 of sepsis, 2 of pneumonia; 1 patient suffered from rupture of a duodenal ulcer; in 7 patients the cause of death was unknown). Five patients underwent reangiography of the coronary arteries because of angina pectoris. In two cases, all bypasses were patent and there was no need for intervention; in the third and fourth case, a de novo stenosis of the obtuse marginal branch was treated with a stent (all bypasses were patent). In the fifth case, the valvulotomized vein graft to the Thoracic and Cardiovascular Surgeon
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wrapped in gauze soaked with spasmolytic solution. In all patients, CABG was performed through a median sternotomy, and the left anterior descending artery was always grafted using the LIMA. After CPB was instituted, the temperature was reduced to 32°C. Myocardial protection was achieved by using tepid blood potassium cardioplegia in combined procedures or Calafiore solution10 for isolated CABG surgery. The distal anastomoses were performed using 7/0 Prolene for vein grafts and 8/0 Prolene for arterial graft anastomoses, respectively. Proximal anastomoses were completed in single-clamp technique in cases of atherosclerosis of the aorta and after release of the aortic cross-clamp in all other cases using a side-biting clamp.
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Table 3 Follow-up data Variable list Myocardial infarction
2 (1.6%)
Coronary reangiography
5 (4%)
CCS CCS 0
117(95%)
CCS I
6 (5%)
NYHA NYHA I
103 (84%)
NYHA II
19 (15%)
Neurological event TND
2 (1.6%)
76.9 16 mm Hg before and 95.6 46 mL/min at 76.3 14 mm Hg after valvulotomy of the venous bypass grafts to the RCA, as shown in ►Fig. 1. The mean pulsatility index increased from 1.6 0.6 before to 2.1 1.3 after valvulotomy (p ¼ 0.01). Out of the 45 patients who underwent MSCT scan of the heart, 1 patient had an occlusion of the valvulotomized venous bypass graft to the RCA and 2 had an occlusion of the RIMA to the circumflex artery. We analyzed the 45 MSCT and 5 coronary reangiographies: the patency rate of the valvulotomized saphenous vein grafts was 97.1 versus 95.8% in the arterial grafts after 18 6 month postoperatively. An example of MSCT scan of the heart showing the valvulotomized bypass graft to the RCA without occlusion is shown in ►Fig. 2.
Reoperation
0
Late mortality
16 (11%)
Discussion
CT scan of the heart
45 (31%)
Based in numerous studies demonstrating superior patency rates of the internal thoracic and radial arteries in comparison to venous grafts,12–14 there is a shift to total arterial revascularization in coronary surgery. Arterial revascularization in the CABG group was also performed in the Syntax trial, where one or more arterial grafts were used in 97.3% of the patients. The Syntax trial could show the superiority of coronary artery bypass surgery in comparison to stent implantation in patients with complex coronary morphology. Despite the fact that in 97% of the cases an arterial graft has been used, only a minority of patients received a second arterial graft.15,16 Currently, still a minority of patients receive more complex arterial revascularization. However, the total arterial revascularization strategy shows different results clinically. The data of You et al indicate that patients undergoing composite bilateral internal thoracic artery (BITA) plus right gastroepiploic artery (RGEA) grafting in off-pump coronary artery bypass grafting appear to have a significantly lower cardiac-related readmission rate than patients undergoing BITA grafting for triple-vessel disease.
Results of 5 reangiographies and 45 CTscans Patency rate of venous BG to the RCA
96% (2/50 occluded)
Patency rate of venous BG to the CX
100% (0/19 occluded)
Patency rate of venous anastomoses to the RCA
96.5% (2/57 occluded)
Patency rate of all venous BG
97.1% (2/69 occluded)
Patency rate of arterial BG
95.8% (3/72 occluded)
Patency rate of arterial anastomoses
96.6% (4/116 occluded)
Patency rate of LIMA graft to anterior wall
100% (0/49 occluded)
Patency rate of RIMA graft to CX
84% (3/19 occluded)
Patency rate of radial artery graft to CX
100% (0/4 occluded)
Abbreviations: BG, bypass graft; CCS, Canadian Cardiovascular Society Angina Classification; CT, computed tomography; NYHA, New York Heart Association classification; TND, temporary neurological deficit.
RCA was occluded and the sequential, free mammary artery bypass to the ramus circumflexus (RCX) was blocked at the proximal anastomosis. In this case, the stenosis of the RCA had regressed and the circumflex artery was stented. No patient had to undergo a redo surgical procedure. Intraoperative flow measurements of 12 patients were performed to evaluate the differences in flow before and after valvulotomy. Flowmetry showed a significant increase of the flow rate of the venous bypass graft to the RCA after valvulotomy (mean increase þ20.2 mL/min; p ¼ 0.01). We measured a mean flow of 75.4 31 mL/min at a MAP of Thoracic and Cardiovascular Surgeon
Fig. 1 Flow measurement of venous bypass graft after discontinuation of cardiopulmonary bypass before and after valvulotomy through a side branch.
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Valvulotomized Vein Grafts
Fig. 2 MSCT scan of the heart showing the valvulotomized bypass to RCA without occlusion.
During 17.7-month follow-up period, the cardiac-related readmission rate was higher in the patient group who underwent CABG with sole composite BITA grafts (9.9%) compared with composite BITA plus in-situ RGEA grafts (2.2%).17 Glineur et al enrolled 152 patients in a systematic 6-month angiographic follow-up study to analyze the function of the right internal thoracic artery (RITA) used in a Y-graft configuration. They found out that a total of 25.3% of RITA anastomoses were not functional. The function of the RITA used as a Y-graft was significantly improved when used on several branches of the circumflex artery or on a severely narrowed first circumflex. Grafting of the intermediate branch or of a RCA had a negative prognostic influence on graft function.18 Furthermore, Mohammadi et al could show that the additional survival benefit of using a second ITA—compared with single ITA—was lost after 60 years of age, even in low-risk patients in a 5.7-year follow-up.19 The use of bilateral ITA is also associated with significant sternal devascularization and higher risk of infectious complications20 at least in subgroups of patients such as those suffering from diabetes, obesity, or chronic pulmonary artery disease. The use of RA grafts seems to be logical based on the assumption that their long-term patency is similar to ITA’s and will be better than the patency of venous conduits.7 Maniar et al presented their data with RA used as either an aortocoronary (RA-ao) or composite graft (T-graft) at 26month follow-up. They found that patients with RA-ao grafts had a greater incidence of postoperative angiography versus patients with composite grafts (19 vs 11%); p < 0.01) and that patients receiving T-graft had a greater number of anastomoses per patient (4.1 0.6 vs 3.0 1, p < 0.01).21 Furthermore, Khot et al reported higher patency rates of saphenous vein grafts than radial arteries22: at a mean follow-up of 565 days angiography, results showed that RA grafts had a patency rate of 51.3%, which was significantly lower than that for LITAs (90.3%) or saphenous vein grafts (64%). RA grafts had an occlusion rate of 33.7%, compared with 4.8% for LITAs, 11.7% for RITAs, and 30.1% for saphenous vein grafts. Maniar and collegues who investigated a series of T-grafting
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using the RA could show that the patency of anastomoses to the RCA was only 58% after 26-month follow-up.21 Buxton et al investigated the graft patency in several randomized series. Three-year patency rate of saphenous vein grafts was 90% and comparable to that of RA grafts of 91% when used for the second best territory.23 Clinically, equivalence of radial arteries and vein grafts is maintained at least up to 6 years.24 Other experimental and clinical trials showed the value of valvulotomized saphenous vein grafts as conduits. Fogarty et al used 110 segments of cadaveric greater saphenous vein in their flow studies and could show significantly increased flow rates after valvulotomy in segments with diameters less than 2.5 mm.5 In another experimental study, Thubrikar et al examined pressure and flow in the femoropopliteal reversed vein graft with competent valves: when reducing the flow, the vein valve opens and closes which results in a pressure trap, reduction of pulse pressure, and flow stagnation that is also known as “trap phenomenon.”6 ►Fig. 3 shows a well visible and stenotic vein valve (arrow) of a saphenous vein graft to the RCA in a reangiography examination. In clinical studies, Urschel et al could prove improved patency rates of valvulotomized vein grafts in the so-called horseshoe grafts, where one limb of these grafts has been used nonreversed and valvulotomized.7 Molina’s study indicated a patency rate of 90% in nonreversed, valvulotomized saphenous vein grafts at 3.5-year follow-up.25 These results could be confirmed in our single center study. Our midterm follow-up data showed that patients with valvulotomized venous grafts have a good clinical outcome. There were only two cases of myocardial infarction, 84% of the patients were in NYHA functional class I, and 95% were in CCS functional class 0. Mortality rate during followup was 11% and in majority not cardiac related. This compares to midterm results of other series.2,19 There was no case of reoperation; only two patients were treated with a stent for a
Fig. 3 Coronary reangiography shows well visible and stenotic vein valve (arrow) of a saphenous vein graft to the right coronary artery. Thoracic and Cardiovascular Surgeon
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de novo stenosis and another one for proximal occlusion of a sequential RITA to the RCX. The rate of adverse cardiac or cerebrovascular events at 1 year was low. Our MSCT (45) and reangiography (5) data showed that the valvulotomized saphenous vein grafts had a patency rate of 97.1% after 18 6 months; all LIMA and RA grafts were patent, whereas three RIMA bypass grafts were occluded. This goes parallel to the data of Puskas et al.26 Our flow measurement data before and after valvulotomy of the saphenous vein bypass graft to the RCA corroborate the clinical findings mentioned above and support the thesis that valvulotomy optimizes flow dynamics of venous bypass grafts. We observed a significant increase of the flow rate after valvulotomy. It appears that eliminating one major drawback of vein grafts is able to establish midterm patency rates similar to that of arterial grafts. This goes in parallel to former clinical findings on valvulotomized vein grafts. Valvulotomized venous grafts have similar 1-year patency rates as arterial grafts. Midterm clinical outcome is comparable as 95% of the patients were free from angina, 84% were in NYHA functional class I, and no patient underwent reoperation. However, long-term results and angiography studies will be needed to strengthen these findings.
4 Mills NL. Saphenous vein graft valves: “the bad guys”. Ann Thorac
Surg 1989;48(5):613–614 5 Chin AK, Mayer DN, Goldman RK, Lerman JA, Olcott C IV, Fogarty
6
7
8
9
10
11
12
13
Study Limitations Only 50 of 147 patients underwent CT scan of the heart or reangiography because of angina pectoris. Here a higher number of follow-up imaging is necessary to strengthen the findings. Furthermore, long-term follow-up data (5–10 years) is necessary, which is very important for this cohort. Finally, a randomized prospective trial with the patient groups valvulotomized/nonvalvulotomized vein grafts would be of great interest for further investigations.
Note The abstract was presented at the DGTHG Annual Meeting in Freiburg in 2012.
14
15
16
17
18
Disclosure There is no conflict of interest to be disclosed.
19
20
References 1 Serruys PW, Morice MC, Kappetein AP, et al; SYNTAX Investigators.
Percutaneous coronary intervention versus coronary-artery bypass grafting for severe coronary artery disease. N Engl J Med 2009;360(10):961–972 2 Lytle BW, Blackstone EH, Loop FD, et al. Two internal thoracic artery grafts are better than one. J Thorac Cardiovasc Surg 1999; 117(5):855–872 3 Hayward PA, Gordon IR, Hare DL, et al. Comparable patencies of the radial artery and right internal thoracic artery or saphenous vein beyond 5 years: results from the Radial Artery Patency and Clinical Outcomes trial. J Thorac Cardiovasc Surg 2010;139(1):60–65, discussion 65–67 Thoracic and Cardiovascular Surgeon
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TJ. The effect of valvulotomy on the flow rate through the saphenous vein graft: clinical implications. J Vasc Surg 1988;8(3): 316–320 Thubrikar MJ, Robicsek F, Fowler BL. Pressure trap created by vein valve closure and its role in graft stenosis. J Thorac Cardiovasc Surg 1994;107(3):707–716 Lajos TZ, Robicsek F, Thubrikar M, Urschel H. Improving patency of coronary conduits “valveless” veins and/or arterial grafts. J Card Surg 2007;22(2):170–177 Risteski PS, Akbulut B, Moritz A, Aybek T. The radial artery as a conduit for coronary artery bypass grafting: review of current knowledge. Anadolu Kardiyol Derg 2006;6(2):153–162 Wimmer-Greinecker G, Yosseef-Hakimi M, Rinne T, et al. Effect of internal thoracic artery preparation on blood loss, lung function, and pain. Ann Thorac Surg 1999;67(4):1078–1082 Calafiore AM, Teodori G, Bosco G, et al. Intermittent antegrade warm blood cardioplegia in aortic valve replacement. J Card Surg 1996;11(5):348–354 Ricci M, Karamanoukian HL, Salerno TA, Dancona G, Bergsland J. Role of coronary graft flow measurement during reoperations for early graft failure after off-pump coronary revascularization. J Card Surg 1999;14(5):342–347 Chen AH, Nakao T, Brodman RF, et al. Early postoperative angiographic assessment of radial grafts used for coronary artery bypass grafting. J Thorac Cardiovasc Surg 1996;111(6):1208–1212 da Costa FD, da Costa IA, Poffo R, et al. Myocardial revascularization with the radial artery: a clinical and angiographic study. Ann Thorac Surg 1996;62(2):475–479, discussion 479–480 Tatoulis J, Buxton BF, Fuller JA, Royse AG. Total arterial coronary revascularization: techniques and results in 3,220 patients. Ann Thorac Surg 1999;68(6):2093–2099 Wu X, Chen Y, Liu H, et al. Comparison of long-term (4-year) outcomes of patients with unprotected left main coronary artery narrowing treated with drug-eluting stents versus coronaryartery bypass grafting. Am J Cardiol 2010;105(12):1728–1734 Head SJ, Mack MJ, Holmes DR Jr, et al. Incidence, predictors and outcomes of incomplete revascularization after percutaneous coronary intervention and coronary artery bypass grafting: a subgroup analysis of 3-year SYNTAX data. Eur J Cardiothorac Surg 2012;41(3):535–541 You JH, Lee TK, Kim WS. Bilateral internal thoracic artery (BITA) grafts vs. BITA with gastroepiploic artery (RGEA) grafts in offpump total arterial revascularisation of triple vessel disease. EACTS abstract no 183, 2008 Glineur D, Hanet C, D’hoore W, et al. Causes of non-functioning right internal mammary used in a Y-graft configuration: insight from a 6-month systematic angiographic trial. Eur J Cardiothorac Surg 2009;36(1):129–135, discussion 135–136 Mohammadi S, Dagenais F, Doyle D, et al. Age cut-off for the loss of benefit from bilateral internal thoracic artery grafting. Eur J Cardiothorac Surg 2008;33(6):977–982 De Paulis R, de Notaris S, Scaffa R, et al. The effect of bilateral internal thoracic artery harvesting on superficial and deep sternal infection: The role of skeletonization. J Thorac Cardiovasc Surg 2005;129(3):536–543 Maniar HS, Barner HB, Bailey MS, et al. Radial artery patency: are aortocoronary conduits superior to composite grafting? Ann Thorac Surg 2003;76(5):1498–1503, discussion 1503–1504 Khot UN, Friedman DT, Pettersson G, Smedira NG, Li J, Ellis SG. Radial artery bypass grafts have an increased occurrence of angiographically severe stenosis and occlusion compared with left internal mammary arteries and saphenous vein grafts. Circulation 2004;109(17):2086–2091 Shah PJ, Bui K, Blackmore S, et al. Has the in situ right internal thoracic artery been overlooked? An angiographic study of the radial artery,
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25 Molina JE. Nonreversed saphenous vein grafts for coronary artery
bypass grafting. Ann Thorac Surg 1989;48(5):624–627 26 Puskas JD, Williams WH, O’Donnell R, et al. Off-pump and on-
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internal thoracic arteries and saphenous vein graft patencies in symptomatic patients. Eur J Cardiothorac Surg 2005;27(5):870–875 24 Hayward PA, Hare DL, Gordon I, Buxton BF. Effect of radial artery or saphenous vein conduit for the second graft on 6-year clinical outcome after coronary artery bypass grafting. Results of a randomised trial. Eur J Cardiothorac Surg 2008;34(1): 113–117
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