Patients and methods: Between July 2001 and October 2009, a total of 104 patients (26 males, 78 females; mean age 57±10.9 years; 43 to 74) who underwent CABG were included. The patients were divided into two groups as those undergoing revascularization with OP-CABG (Group 1, n=52) and those undergoing C-CABG (Group 2, n=52). Intraoperative data and postoperative coronary angiograms at six months were recorded.

Results: The OP-CABG was associated with less requirement for blood transfusion and a lower amount of postoperative drainage. Duration of intubation and the length of stay in the intensive care unit and hospital were found to be significantly shorter in the OP-CABG group. The patency of the arterial grafts was almost completely achieved in both groups, and anastomoses on the posterior vessels were patent in the OP-CABG group.

Conclusion: Based on our experience, in properly selected cases, targeted vessels on the posterior wall can be successfully revascularized with OP-CABG.

Off-pump coronary artery bypass grafting (OP-CABG) has been shown to be superior to conventional coronary bypass grafting (C-CABG), since it is associated with less proteolytic and inflammatory response, decreased operative trauma, less postoperative complications, and shorter length of stay in the hospital and intensive care unit (ICU), leading to reduced morbidity and cost.[2] Moreover, OP-CABG offers a high rate of graft patency, less amount of blood loss, lower mortality, and reduced need for inotropic support.[2]

Owing to the fact that recent technology allows revascularization of all target vessels, OP-CABG has become a widely used surgical modality in all patient groups. This method is preferred to avoid the deleterious effects of cardiopulmonary bypass (CPB) and is more frequently performed on the descending left and right coronary arteries (RCAs).[3] Revascularization of coronary arteries in the posterior cardiac wall can be made only by the prominent displacement of the heart in the pericardial space.[2,3]

In the present study, we aimed to investigate the feasibility of OP-CABG for the revascularization of posterior coronary arteries versus C-CABG and to report short-term results of this technique.

Surgical technique
All patients were operated by a single surgical team. Preparations for CABG was made routinely for all patients. General anesthesia was introduced with standardized intravenous narcotic anesthesia. Prior to CPB, heparin was applied at a dose of 300 IU/kg, maintaining an activated clotting time (ACT) at 450 sec. In C-CABG, ACT monitorization was performed every 15 min and additional doses of heparin were administered, if necessary. In OP-CABG, heparin (100 IU/kg) was introduced before proximal anastomosis, keeping the ACT at a range of 250 to 350 sec.

During C-CABG procedure, median sternotomy was followed by cannulation of the ascending aorta and, subsequent to two-stage venous cannulation from the right atrium, CPB was initiated. The pump flow and speed were set at a systemic pressure of 70 to 90 mmHg. Cardioplegia was continued every 20 min. Distal anastomoses were made using 7/0 prolene, while proximal anastomoses were performed with 5/0 prolene sutures along with lateral clamping. In distal anastomoses, the left anterior descending artery and its diagonal collaterals were initially revascularized. The RCA and its branches followed by the circumflex artery and its marginal branches on posterior wall were, then, revascularized.

In order to visualize the target vessel more clearly, wet gauzes were placed posteriorly, and the heart was elevated. Suspension sutures placed on the posterior pericardium also aided as an alternative way in the elevation of heart during anterior and lateral anastomoses. On a beating heart, anastomosis was facilitated using the Octopus® (Medtronic Inc., Minneapolis, MN, USA) to provide stabilization of the myocardium.

During the anastomosis of the RCA and its branches, the traction suture was placed in a manner that the right atrioventricular junction and RCA were involved with a thick layer of the surrounding tissues. Anastomosis could be readily accomplished after stabilization of target vessels with Octopus®.

In order to preserve the hemodynamic stability, a different technique was preferred for anastomosis of circumflex artery and its marginal branches on posterior wall. Initially, the superior vena cava was freed by dissection to allow an easier manipulation of the heart. After placement of 0-silk traction suture on posterior pericardium, the patient was rotated 20 to 30° to right in the Trendelenburg position. This maneuver caused the traction of suture at the posterior pericardium and allowed the elevation of cardiac apex. At this stage, the vacuum clamp was put on the apex keeping the heart at suspension. The circumflex artery and its marginal branches were exposed readily, and anastomoses were made after stabilization of the target vessels by Octopus®. Consecutive grafting technique was not used in any of our patients.

Control coronary angiography
In our department, control coronary artery angiography is reserved for patients who underwent CABG with revascularization of circumflex artery and its marginal branches. Therefore, it has been postoperatively performed in 52 cases operated with OP-CABG and revascularization of the posterior wall.

Statistical analysis
Statistical analysis was performed using the SPSS version 10.0 software (SPSS Inc., Chicago, IL, USA). Descriptive data were expressed in mean ± standard deviation (SD), median (min-max) or number and frequency. Comparison of qualitative data was carried out using the chi-square test, while independent samples-t test was used for quantitative variables. A p value of <0.05 was considered statistically significant.

Table 1: Demographic and clinical characteristics of the patients

The mean duration of anastomoses performed on circumflex artery and left anterior descending artery was 8.3±1.5 min and 8.3±1.4 min, respectively (Table 2).

Table 2: Duration of anastomoses in off-pump group

The number of distal anastomoses performed was more in the on-pump group than that of the off-pump group (p=0.036). A total of 124 coronary arteries in the off-pump group and 144 arteries in the on-pump group underwent anastomoses (Table 3). The consecutive grafting technique was not performed in any of our patients.

Table 3: Distribution of target coronary arteries

No mortality was observed in our series. However, low cardiac output syndrome necessitating intra-aortic balloon pump (IABP) occurred in two patients in the off-pump group and four patients in the on-pump group, despite inotropic support. In the on-pump group, two patients suffered from acute renal failure (ARF), two patients from respiratory failure, and two patients from perioperative myocardial infarction. Such complications did not occur in the off-pump group (Table 4).

Table 4: Postoperative data

The mean duration of intubation was significantly shorter in the off-pump group (8.6±2.3 h) than the on-pump group (12.1±3.9 h) (p<0.001). The amount of drainage was 519±120 mL in the off-pump group, while it was 655±128 mL in the on-pump group (p<0.001). Similarly, the amount of transfusion was significantly lower in the off-pump group (0.9±0.7 U vs. 1.9±0.7 U, respectively). The mean preoperative EF was lower in the off-pump group, although there was a need for postoperative inotropic support more often in the on-pump group (n=18/8). The frequency of postoperative atrial fibrillation did not significantly differ between the groups (n=12 in the on-pump group and n=6 in the off-pump group). The mean length of ICU stay was shorter in the off-pump group (2.0±0.4 days vs. 2.5±0.6 days, respectively) (p=0.001). In addition, the mean hospitalization period was also shorter in the off-pump group (5.3±0.6 days vs. 6.7±1.0 days, respectively) (p<0.001) (Table 4).

Control coronary angiography results revealed that the arterial graft patency rates were 100% in both groups. The venous graft patency rates in the off-pump and on-pump groups were 95% and 95.8%, respectively. In both groups, the bypass grafts performed in the circumflex arteries were patent and obstructions invariably occurred in grafts where RCA anastomoses were made. The rates of patency of the grafts in the target vessels are plotted in Table 5.

Table 5: Profile of patency of grafts in target vessels in off-pump and conventional groups

We applied OP-CABG method to patients with LAD and RCA lesions and on posterior wall lesions in selected cases. The main challenge on revascularization of multiple vessels is maintenance of hemodynamic stability during access and exposure. These issues are more difficult to be accomplished on beating heart. In our series, we did not come across hemodynamic instability during revascularization of LAD. Deterioration of hemodynamics was noted on circumflex vessels located on posterior and inferior parts of heart, which constitute the most difficult regions for exposure. Experimental studies have shown that left ventricular functions were limited and eventually hemodynamic instability was observed during anastomoses of circumflex arteries on beating heart.[6] Decrease in cardiac index and increase in pulmonary artery wedge pressure were noted during revascularization of posterior wall. We kept our patients in Trendelenburg position to maintain hemodynamic stability in ectopia cordis position and pressure on right heart was relieved with this manoeuvre.

Even though CPB is termed as a risk factor for morbidity and mortality, prospective, randomized trials have shown that there was no difference between techniques with or without CPB in terms of morbidity and mortality.[7] Revascularization on beating heart was not associated with increased mortality in early postoperative period.[4] In contrast, decreased rates of morbidity and mortality were seen in some retrospective studies investigating OP-CABG.[5,6] Incidences of perioperative mortality and perioperative myocardial infarction after OP-CABG were 1.9% and 2.9%, respectively.[8] These results imply that OP-CABG is not associated with an increased likelihood of mortality than C-CABG. Our results are in accordance of this data.

Van Dijk et al.[9] have compared OP-CABG and C-CABG in terms of surgical drainage and transfusion amounts. They reported that amounts of drainage in OP-CABG and C-CABG groups were 500 mL and 400 mL, respectively. The reason for the relatively increased amount of drainage in OP-CABG was attributed to the fact that heparin used during operation was not neutralized.

In conjunction with reports of Hoff et al.,[10] we observed that amount of drainage was more in C-CABG. Routine use of anti-platelet factors, dilutional anaemia and direct effects of CPB may be responsible for this result.

Low cardiac output syndrome diagnosed postoperatively in both groups was managed successfully with IABP. Frequencies of IABP use in OP-CABG and C-CABG in our series were slightly higher than those reported by Ascione et al.[11] Histopathological examinations demonstrated that mitochondria in the left ventricular cells were preserved better with OP-CABG.[12] Moreover, manipulations for achieving access to the target vessels resulted in serious cardiac injury.[13]

Cardiopulmonary bypass may contribute to the pathogenesis of ARF after CABG via hemodynamic, inflammatory, and nephrotoxic effects. Hemolysis, decreased perfusion, non-pulsatile flow, and hemodilution may facilitate occurrence of ARF.[14,15] Therefore, CPB has been postulated as an independent risk factor for ARF. From this point of view, OP-CABG may be an alternative for minimizing the risk of ARF. However, it should be kept in mind that low cardiac output syndrome which may occur during OP-CABG may enhance the pathogenesis of ARF. Therefore, appropriate preoperative hydration, avoidance of nephrotoxic drugs, the use of inotropic and vasodilator drugs for hemodynamic stability, and meticulous followup of acid-base balance are important measures for elimination of ARF.[14,15]

Adverse effects of CPB on the respiratory system may become more obvious in COPD patients. In our series, no patients with COPD who underwent OP-CABG suffered from respiratory failure postoperatively. On the contrary, respiratory failure was detected in two patients with COPD operated via C-CABG. Bull et al.[16] suggested that duration of extubation prolonged in C-CABG. Consistent with this finding, our results showed that duration of postoperative intubation were longer in the on-pump group. Shorter hospitalization accelerates the return of the patient to daily life and allows a more effective postoperative rehabilitation. In our series, the OP-CABG seems to be more favorable, since it is linked with a shorter duration of hospitalization.

Control of patency for anastomoses and grafts is an important parameter for documentation of the efficacy of OP-CABG. In the literature, the graft patency rates for C-CABG are reported between 94 to 99% in the early postoperative period and range between 51 to 98% in the long-term.[17] Mechanical stabilization yielded a better graft patency in coronary vessels including the circumflex arteries.[17,18] Compared to the OP-CABG and C-CABG, we found that the patency of the grafts was almost 100% similar to each other. At six months, the postoperative graft patency rate was 96.6% in the OP-CABG and 97% in the C-CABG. Endothelial injury due to intracoronary shunt was reported in the literature; however, we observed no stenosis or obstructions in anastomosis sites where the intracoronary shunts were used.[19,20]

Our analysis of outcomes and preoperative and operative data of OP-CABG showed that postoperative blood transfusion and drainage was less, and the length of intubation, hospitalization and ICU stay were shorter after OP-CABG. Graft patency rates were satisfactory in both groups and, remarkably, all anastomoses performed on the posterior vessels were found to be patent in the OP-CABG group.

In conclusion, in properly selected cases, targeted vessels on the posterior wall can be revascularized effectively and safely with OP-CABG.

Declaration of conflicting interests
The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.

Funding
The authors received no financial support for the research and/or authorship of this article.

1) Cleveland JC Jr, Shroyer AL, Chen AY, Peterson E, Grover FL. Off-pump coronary artery bypass grafting decreases risk-adjusted mortality and morbidity. Ann Thorac Surg 2001;72:1282-8.

2) Villa E, Messina A, Troise G. Concerning early and late results of training in off-pump coronary artery bypass surgery. J Thorac Cardiovasc Surg 2013;145:316-7.

3) Raja SG, Benedetto U. Off-pump coronary artery bypass grafting: Misperceptions and misconceptions. World J Methodol 2014;4:6-10.

4) Gokalp O, Yesilkaya NK, Bozok S, Besir Y, Iner H, Durmaz H, et al. Effects of age on systemic inflamatory response syndrome and results of coronary bypass surgery. Cardiovasc J Afr 2018;29:22-5.

5) Boyd WD, Desai ND, Del Rizzo DF, Novick RJ, McKenzie FN, Menkis AH. Off-pump surgery decreases postoperative complications and resource utilization in the elderly. Ann Thorac Surg 1999;68:1490-3.

6) Dekker AL, Geskes GG, Cramers AA, Dassen WR, Maessen JG, Prenger KB, et al. Right ventricular support for off-pump coronary artery bypass grafting studied with bi-ventricular pressure--volume loops in sheep. Eur J Cardiothorac Surg 2001;19:179-84.

7) Calafiore AM, Di Mauro M, Contini M, Di Giammarco G, Pano M, Vitolla G, et al. Myocardial revascularization with and without cardiopulmonary bypass in multivessel disease: impact of the strategy on early outcome. Ann Thorac Surg 2001;72:456-62.

8) Tasdemir O, Vural KM, Karagoz H, Bayazit K. Coronary artery bypass grafting on the beating heart without the use of extracorporeal circulation: review of 2052 cases. J Thorac Cardiovasc Surg 1998;116:68-73.

9) van Dijk D, Nierich AP, Eefting FD, Buskens E, Nathoe HM, Jansen EW, et al. The Octopus Study: rationale and design of two randomized trials on medical effectiveness, safety, and cost-effectiveness of bypass surgery on the beating heart. Control Clin Trials 2000;21:595-609.

10) Hoff SJ, Ball SK, Coltharp WH, Glassford DM Jr, Lea JW 4th, Petracek MR. Coronary artery bypass in patients 80 years and over: is off-pump the operation of choice? Ann Thorac Surg 2002;74:S1340-3.

11) Ascione R, Lloyd CT, Gomes WJ, Caputo M, Bryan AJ, Angelini GD. Beating versus arrested heart revascularization: evaluation of myocardial function in a prospective randomized study. Eur J Cardiothorac Surg 1999;15:685-90.

12) Westaby S, Benetti FJ. Less invasive coronary surgery: consensus from the Oxford meeting. Ann Thorac Surg 1996;62:924-31.

13) Messmer BJ. Coronary surgery without extracorporeal circulation: benefit or additional risk for the patient? Eur J Cardiothorac Surg 1990;4:509.

14) Mirmohammad-Sadeghi M, Naghiloo A, Najarzadegan MR. Evaluating the relative frequency and predicting factors of acute renal failure following coronary artery bypass grafting. ARYA Atheroscler 2013;9:287-92.

15) Şener T, Köprülü AŞ, Karpuzoğlu OE, Acar L, Temur B, Gerçekoğlu H. The clinical results of off-pump coronary artery bypass surgery in renal dysfunction patients. Turk Gogus Kalp Dama 2013;21:918-23.

16) Bull DA, Neumayer LA, Stringham JC, Meldrum P, Affleck DG, Karwande SV. Coronary artery bypass grafting with cardiopulmonary bypass versus off-pump cardiopulmonary bypass grafting: does eliminating the pump reduce morbidity and cost? Ann Thorac Surg 2001;71:170-3.

17) Özkaynak B, Yıldırım Ö, Aksüt M, Onk Alper O, Kayalar N, Ömeroğlu Nail S, et al. Very long-term angiographic results of off-pump coronary artery bypass graft surgery. Turk Gogus Kalp Dama 2014;22:260-5.

18) Poirier NC, Carrier M, Lespérance J, Côté G, Pellerin M, Perrault LP, et al. Quantitative angiographic assessment of coronary anastomoses performed without cardiopulmonary bypass. J Thorac Cardiovasc Surg 1999;117:292-7.

19) Bozok S, İlhan G, Karamustafa H, Ozan Karakişi S, Tüfekçi N, Tomak Y, et al. Influence of intracoronary shunt on myocardial ischemic injury during off-pump coronary artery bypass surgery. J Cardiovasc Surg (Torino) 2013;54:289-95.

20) Tüfekçi N, Bozok Ş, Aslan C, İlhan G, Karakişi Ozan S, Ergene Ş, et al. A prospective study on indication of intracoronary shunt during off-pump coronary bypass grafting surgery for single-vessel disease. Turk Gogus Kalp Dama 2016;24:034-9.