Respiratory Complications After Coronary Artery Bypass Surgery With Unilateral or Bilateral Internal Mammary Artery Grafting*
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1 Respiratory Complications After Coronary Artery Bypass Surgery With Unilateral or Bilateral Internal Mammary Artery Grafting* Maria Daganou, MD; Joanna Dinwpoulou, MD; Nickolaos Michalopoulos, MD; Konstantinos Papadopoulos, MD; Anna Karakatsani, MD; Stephanos Geroulanos, MD, PhD; and George E. Tzelepis, MD, FCCP Background and study objective: Use of bilateral internal mammary artery (IMA) grafts during coronary artery revascularization procedures carries the potential for increased incidence of postoperative respimtory complications compared with use of unilateral IMA grafts. The purpose of this study was to compare the incidence of respiratory complications such as hypoxemia, atelectasis, pleural effusion, and diaphragmatic dysfunction in patients who received one or both IMAs as conduit grafts. Design: Prospective, comparative study. Setting: Surgical ICU at a tertiary teaching hospital. Patients: Seventy-five patients with bilateral and 75 patients with unilateral IMA grafts. Measurements: Serial postoperative Pa0 2 /fraction of inspired oxygen measurements, radiographic scores of atelectasis and pleural effusion, duration of mechanical ventilation, length of ICU and hospital stay, and incidence of pneumothorax, pneumonia, and wound infection. Results: There was a higher incidence (51% vs 25%; p=0.002) and severity (0.48±0.09 vs 0.15±0.05 on the first postoperative day, 0.39±0.07 vs 0.27±0.07 on the fourth postoperative day, mean±sem; p=0.004) of postoperative right lower lobe atelectasis in the group who received bilateral IMA grafts than in those who received left IMA grafts. This finding probably reflects the effects of additional surgical intervention on the right side of the chest. Incidence and sevetity of pleural effusion, gas exchange impairment, duration of mechanical ventilation, ICU and hospital stay, and incidence of pneumothorax, pneumonia, and wound infection were not influenced by use of bilateral IMA grafts (p>0.05). Conclusion: We conclude that use of bilateral IMA grafts doting coronary artery revasculatization does not increase the incidence of postoperative respiratory complications compared with unilateral IMA grafting. (CHEST 1998; 113: ) Key words: atelectasis; coronary artety bypass surgety; hypoxemia; pleural effusion Abbreviations: BIMA= bilateral internal mammaty artery; CABG=coronaty artery bypass grafting; CPB=cardiopulmonaty bypass; Flo 2 =fraction of i n s ped i oxygen; ~ IMA = internal mammary artery; LIMA= left internal mammary artery; LLL= left lower lobe; =not significant; POD=postoperative day; RIMA=right internal mammary artery; RLL= right lower lobe; SV=saphenous vein postoperative respirat01y c o m p l i c ~ such t i oas n s, hypoxemia, atelectasis, pleural effusion, or diaphragmatic dysfunction, are often a source of morbidity in cardiac surgery patients, and are more common in patients receiving unilateral internal mammary arte1y (IMA) grafts than in those receiving *From the Surgical Intensive Care Unit, Onassis Cardiac Surgety Center, Athens, Greece. Manuscript received May 28, 1997; revision accepted October 17, Reprint requests: George E. Tzelepis, MD, FCCP, Surgical ICU, Onassis Cardiac Surgery Center, 3.56 Sygrou Avenue, Athens, Greece saphenous vein (SV) grafts alone This has been largely attributed to performance of pleurotomy to hmvest IMA grafts, which results in greater chest wall and parenchymal trauma, greater pain, and impairment of ability to cough and inhale deeply In addition, IMA dissection may reduce blood supply to the ipsilateral intercostal muscles and the phrenic nerve, thus resulting in diaphragmatic dysfunction and, ultimately, atelectasis. 13 Over the last two decades, both the left and right IMAs have been increasingly used as coronary artery conduits, largely due to their superior patency rates CHEST / 113 /5/ MAY,
2 compared with SV grafts. To the extent that use of both IMAs results in greater thoracic trauma and respiratory muscle dysfunction than use of a single I MA, one would expect a greater incidence of postoperative respiratory complications with bilateral IMA grafts. This study was undertaken to compare the incidence and severity of the postoperative respiratory complications that occur in patients undergoing coronary artery bypass grafting (CABG) with unilateral or bilateral IMA grafts and to assess their overall effects on certain morbidity indices. Patients METHODS The study population comprised 75 consecutive patients undergoing elective CABG who received bilateral IMA grafts (BIMA group) and 75 patients in whom only the left IMA was used as a g raft (LIMA group). The patients in the two groups were matched f or age, sex, smoking habits, preoperative left ventricular ejection fraction, and number of grafts. Patients with clinical and/or radiographic evidence of preexisting respirato1y disease were excluded from the study. All surgical procedures were performed b y the same surgical and anesthetic teams during a period from March 1995 through July With the exception of 3 patients in the LIMA group and 2 patients in the BIMA group, all received p edicled l eft IMA grafts as single or sequential grafts. The right IMA (RIMA) was used as a fi ee graft in all cases. The study w as approved b y the Ethics Committee of our institution. Operative Technique A median sternotomy incision was made in all patients and ipsilateral pleurotomy was carried out for all IMA dissections. The left IMA was mobilized distally down t o its bifurcation, and the right IMA was harvested similarly and divided proximally a nd distally to be sed u as a free graft. Cardiopulmonmy bypass (CPB) with a membrane oxygenator was used in all patients under moderate hypothermia (28 t o 32 C) and hemodilution. Myocardial protection was achieved b y means of cold saline solution with ice slush. Distal anastomoses were performed f ollowing aortic cross clamping and cold cardioplegic arrest; proximal anastomoses of the SV and free IMA grafts to the aorta were performed during rewarming. Violated pleural cavities and mediastinum were drained b y c hest tubes after careful evacuation of any accumulated blood. Antibiotic prophylaxis consisted of IV cefuroxime administration just prior t o s ternotomy incision and for 48 hours postoperatively, and topical application of gentamicin. Postoperative Management All patients were mechanically ventilated in the ICU \vith tidal volumes of 10 mukg of body weight and positive end-expiratory pressure of 5 e m H 2 0 at a rate ufficient s to keep arterial ph between 7.35 and Extubation was accomplished when patients were alert, hemodynamically s table, and able to maintain adequate blood gases during a s hort t1ial on pressure support H 2 0. Packed red blood cells were transfu sed to keep a hemoglobin level greater than 9 gldl. Chest tubes were left in place for less than 4 8 hours unless an air leak was present. ve ntilation of 5 e m Data Collection The ratio of Paoi fraction of inspired oxygen (Fio 2 ) was recorded at 30, 120, and 240 min after arrival in the ICU, and at 30, 120, and 240 min after extubation and on postoperative day (POD)4. Preoperative, POD l, and POD 4 c hest r adiographs were reviewed b y the same radiologist (K.P.), who was unaware of the purpose of the study. Preoperative and POD 4 fllms included standard posteroanterior and lateral views, whereas POD 1 film s were single anteropostelior views taken at the bedside after extubation. Lower l obe atelectasis was graded using the following rating scale: O= no atelectasis; 1 =plate-like atelectasis; 2=atelectasis o f a single segment; 3=atelectasis o f m ore than one segment; 4=lobar atelectasis. Pleural effu sion was assessed after removal of chest tubes and was classified u sing the following graded scale: O= no plem al effu sion; l =bluning o f the costaphrenic a ngle; 2=effu sion occupying one to two intercostal spaces; 3=effusion occupying more than t\vo intercostal spaces. Each lung was scored independently. Hemidiaphragmatic elevation was defined as a lise of more t han one intercostal space on POD 4 c hest roentgenograms in comparison to the preoperative image. In addition, we recorded a number of intra- and postoperative variables including number of grafts, duration of CPB and aortic cross clamping, units of blood trans fu sed, reoperation r ate for bleeding, duration of mechanical ventilation, length of ICU and hospital stay, and development of pneumothorax, pneumonia, and wound infections. Statistical Analysis All analyses were performed u sing a commercial statistical package (SPSS, Inc; Chicago). The x 2 test was used to compare discrete variables, and a nonparametric test (Mann-Whitney U) was used f or comparison of groups with a s kewed distribution. Repeated measures ANOVA, with or without covariate analysis, was used to assess differences in gas exchange indices, severity o f atelectasis, and pleural effusions. All data a re reported as mean::'::sd, unless stated otherwise. Probability values of less than 0.05 were considered significant. RESULTS Patient characteristics and operative data are shown in Table l. There was a higher prevalence of diabetes m ellitus in the LIMA group than in the BIMA group (29% v s 8%; p = 0.002). The BIMA group had a longer mean CPB time than the LIMA group (97± 22 vs 78±22 min; p< O.OOl ). Table 2 depicts the incidence of postoperative radiologic abnormalities. Right lower lobe (RLL) atelectasis was overall more frequent in the BIMA group than in the LIMA group (51 % vs 25%; p=0.002), with the difference being significant for both POD 1 and POD 4 (p= and p=0.03, respectively). Assessment of atelectasis showed that the RLL atelectasis score was higher overall in the BIMA group than in the LIMA group (mean±sem, 0.48 ± 0.09 vs 0.15 ± 0.05 for POD l ; 0.39±0.07 vs 0.27±0.07 for POD 4; p=0.004). To assess whether group differences in atelectasis score were related to 1286 Clinical Investigations
3 Table!-Patient Characteristics and Operative Data LIMA Group (n=75) BIMA Group (n=75) p Value Age, yr* 56±8 54±8 Sex, M/F /3 No. of smokers 47(63%) 50(67%) No. of patients with diabetes mellitus 22 (29%) 6(8%) No. of patients with previous coronary 1 (2%) 5(7%) revascularization Left ventricular ejection fraction, %* 51±9 51±10 No. of grafts* 2.5± ±0.7 Bypass time, min* 78±22 97±22 <0.001 Clamp time, min* 44±17 50±20 *Values expressed as mean±sd. =not sign ificant. differences in CPB time, we used an analysis covariance model with CPB time as the covariate. In this model, the differences in atelectasis score between the two groups remained significant (p=0.002). In contrast to RLL atelectasis, there was no significant difference in the incidence or severity of postoperative left lower lobe (LLL) atelectasis between the two groups. Within each group, however, LLL atelectasis was more frequent and more severe than RLL atelectasis. In the LIMA group, the mean±sem on POD 1 was 1.09±0.13 (LLL) vs 0.15±0.05 (RLL); on POD 4, 1.48±0.12 (LLL) vs 0.27±0.07 (RLL). In the BIMA group, the POD 1 data were 1.15±0.13 (LLL) vs 0.48±0.09 (RLL); and on POD 4, 1.21±0.13 (LLL) vs 0.39±0.07 (RLL). For all comparisons, SEM, p<0.05. There were no differences between the two groups in the incidence or severity of postoperative pleural effusion on either side. Left hemidiaphragm elevation was more frequent in the LIMA group than in the BIMA group, but this difference did not reach significance (20% vs 8%; p=0.06). There were no differences between the two groups in the PaOiFio 2 at any interval measured. In addition, the two groups did not differ in blood transfusion requirements, rate of reoperation for bleeding, duration of mechanical ventilation, length of ICU or hospital stay, or incidence of pneumothorax or pneumonia (Table 3). There were no hospital deaths and no patient developed a wound infection. DISCUSSION In this study we found that, in comparison with patients receiving unilateral IMA grafts, patients receiving bilateral IMA grafts have an increased incidence and severity of RLL atelectasis but a similar incidence of LLL atelectasis and postoperative pleural effusions. Overall, the number of IMA grafts has no influence on postoperative blood loss, duration of mechanical ventilation, length of ICU or hospital stay, or incidence of pneumothorax, pneumonia, or wound infection. LLL atelectasis is ve1y common after cardiac surgery, especially in patients rece1vmg IMA grafts The chest wall and parenchymal trauma associated vvith the performance of pleurotomy in order to harvest IMA has been implicated as the most likely mechanism leading to an increased incidence of atelectasis In addition, IMA dissection Table 2-lncidence of Chest Radiograph Findings LIMA Group, BIMA Group, No.(%) No.(%) p Value POD 1 LLL atelectasis 47(63) 46 (61) RLL atelectasis 9 (12) 24 (32) POD 4 LLL atelectasis 58 (77) 48 (64) RLL atelectasis 15 (20) 27 (36) 0.03 Left pleu ral effusion 46 (61) 35 (47) Right pleural effusion 33 (44) 32 (43) Left hemidiaphragm 15 (20) 6 (8) 0.06 elevation Table 3-0utcome Data LIMA BIMA p Group Group Value Blood transfusion, units* 1.2± ±1.2 No. of patients requiring reoperation l 1 for bleeding Mechanical ventilation, h* 10.7±3.4 11±3.5 ICU stay, h* 27±1.5 24±13 Hospital stay, d* 6.1± ±0.7 No. of patients with pneumothorax 4 4 No. of patients with pneumonia 1 *Values expressed as mean±sd. CHEST I 113 I 5 I MAY,
4 may reduce blood supply to the ipsilateral intercostal muscles and the phrenic nerve, thus leading to respiratory muscle dysfunction and, ultimately, atelectasis.13 Our finding that the incidence and severity of RLL atelectasis were g reater in the BIMA group than in the LIMA group most likely is related to the additional dissection of RIMA and performance of right pleurotomy in BIMA. Prolonged CPB may also lead to postoperative atelectasis, largely through insufficient release of surfactant resulting from inadequate perfusion of the alveolar epithelium during CPB Because of its technically more demanding anastomoses, patients in the BIMA group had a longer mean CPB time than the LIMA group. However, for two reasons, we believe that this difference did not have any measurable effect on RLL atelectasis. First, if CPB time was the sole underlying cause, then one would expect the BIMA group to experience more severe atelectasis, not only in the RLL but also in the LLL. Fmthermore, the intergroup differences in RLL atelectasis remained significant even after adjustment for differences in CPB time between the two groups using an analysis of covariance model. In the present study there were no differences in the incidence and severity of postoperative pleural effusion in both between- and vvithin-group comparisons. A substantial difference in the incidence of postoperative pleural effusion was r eported by previous studies comparing patients receiving single IMA or SV grafts. Hurlbut et al 15 repmted postoperative pleural effusion in 84% of patients receiving IMA, but in only 47% of patients who received SV grafts alone. In contrast, Peng et al 16 found a similar frequency (about 40%) of pleural effusions in patients receiving IMA or SV grafts. The pathogenetic mechanism of postoperative pleural effusion remains obscure. Some authors have proposed that pleural trauma and transection of lymphatic channels during IMA mobilization are the likely mechanisms explaining the g reater incidence of pleural effusion in IMA than in SV graft patients, whereas others have suggested that pericardia! inflammation most likely accounts for the appearance of postoperative pleural effusionsi 6.l 7 Our finding of equal frequency of pleural effusion in the BIMA and LIMA groups suggests pelicardial inflammation as the predominant mechanism. Although LIMA dissection was carried out in both groups, there was a higher incidence of left hemidiaphragm elevation in the LIMA group than in the BIMA group. This difference cannot be explained on the basis of hypothermic injury to the phrenic nerve during myocardial cooling because ice slush was used in both groups for comparable time periods. We postulate that this disparity is probably related to the higher prevalence of diabetic patients in the LIMA group. This was due to the surgeon's preference to avoid using both IMAs in diabetics, as it has previously been r eported that bilateral IMA use canies a significant risk for wound infection in this patient population Similarly, a more frequent occurrence of postoperative hemidiaphragm elevation has been previously reported in diabetic patients receiving IMA grafts and has been attributed to a subclinical phrenic neuropathy that renders the nerve more susceptible to hypothermic injury. 2 0 Despite intergroup differences in the incidence and severity of RLL atelectasis and in the duration of CPB, postoperative gas exchange impairment (as assessed by PaOJ Fio2) was similar in both groups. In general, postoperative hypoxemia appears to be associated with performance of pleurotomy and presence of atelectasis rather than with prolonged bypass time. In this context, Singh et al 21 found no significant relationship between CPB time and hypoxe mia after CABG, and Vargas et al 4 found a greater impairment in postoperative Pa02 in patients with atelectasis and pleural effu sion compared \vith patients who had normal postoperative chest radiographs. Like\vise, Burgess et al u reported greater pulmonary shunting and lower a1te1ial oxygen t ension in CABG patients subjected to pleurotomy than in patients who had not undergone pleurotomy. In our study, the bilateral pleurotomies in the BIMA group did not appear to worsen postoperative gas exchange impairment, probably because of the generally mild degree of RLL atelectasis obse1ved in our study. In this study, mean blood transfusion requirements and rate of reoperation for bleeding did not differ b etween the two groups. In previous studies, Cosgrove e t al 22 reported a m arginally significant increase in the volume of blood transfused in patients with bilateral IMA grafts compared with patients with one IMA graft, and Aarnio et al 23 noted higher rates of reoperation for bleeding after bilateral than after unilateral IMA grafting. Our findings are in accordance with those by Ashraf et al, 24 who found no difference in bleeding complications between patients vvith unilateral or bilateral IMA grafts. The BIMA and LIMA groups had comparable durations of postoperative mechanical ventilations and lengths of ICU and hospital stays. This finding is in contrast with two recent studies that reported longer postoperative ventilatory support in patients who received grafts u sing both IMAs than in those with only one IMA graft However, both studies were retrospective and the difference in duration of ventilatory support may reflect differences in anesthetic techniques used or lack of rigid extubation 1288 Clinical Investigations
5 criteria. Of interest, in both studies, the length of hospital stay did not differ between the two groups. There are certain limitations to this study that deserve consideration. First, the study was conducted by only one group of investigators performing bypass surgery and was not a randomized controlled study, as shown by an uneven distribution of patients with diabetes mellitus between the two groups. Thus, one may argue that the results of the present study may be institution-specific and not pertinent to all patient groups. Second, the study included a relatively small number of patients undergoing coronary a1tery revascularization. Although the sample size was sufficient to detect differences in major clinical outcomes, it may have been too small to demonstrate differences in variables with small rates, such as reoperation for bleeding. In conclusion, our findings suggest that utilization of both I MAs for corona1y grafting does not increase postoperative respiratory morbidity compared with unilateral IMA grafting. REFERENCES 1 Vargas FS, Cukier A, Hueb W, et a!. Relationship between pleural effusion and pericardia! involvement after myocardial revascularization. Chest 1994; 10.5: Light RW. Pleural effusion due to miscellaneous diseases. In: Light RW, ed. Pleural diseases. 3rd ed. Baltimore: Williams & Wilkins, 1995; Landymore RW, Howell F. Pulmonary complications following myocardial revasculmization \ \ ~ the t h internal mammary artery graft. Eur J Cardiothorac Surg 1990; 4: Vargas FS, Cukier A, Terra-Filho M, et a!. Influence of atelectasis on pulmonary function after coronary artety bypass grafting. Chest 1993; 104: Kollef MH, Peller T, Knodel A, et al. Delayed pleuropulmonary complications following coronary artery revascularization with the internal mammary artery. Chest 1988; 94: Laub GW, Muralidharan S, Chen C, et a\. Phrenic nerve injmy: a prospective study. Chest 1991; 100: Wilcox P, Baile EM, Hards J, et a!. Phrenic nerve function and its relationship to atelectasis after coronary artet)' bypass surgery. Chest 1988; 93: Vargas FS, Cukier A, Terra-Filho M, et a!. Relationship between pleural changes after myocardial revascularization and pulmonary mechanics. Chest 1992; 102: Benizbeitia LD, Tessler S, Jacobowitz IJ, et al. Effect of stemotomy and coronmy bypass surgery on postoperative pulmonaty mechanics. Chest 1989; 96: Jenkins SC, Soutar SA, Forsyth A, et al. Lung function after coronmy artery surgety using the internal mammary artety and the saphenous vein. Thorax 1989; 44:209-ll ll Burgess GE, Cooper JR, Marino RJ, et al. Pulmonary effect of pleurotomy during and after coronary artery bypass with internal mammary attety versus saphenous vein grafts. J Thorae Cardiovasc Surg 1978; 76: Cohen AJ, Moore P, Jones C, et a!. Effect of intemal mammary harvest on postoperative pain and pulmonary function. Ann Thorac Surg 1993; 56: Abd AG, Braun NMT, Baskin MI, et a!. Diaphragmatic dysfunction after open heart surgery: treatment \ \ ~. a trock ing bed. Ann Intern Med 1989; 111: h 14 Matthay MA, Wiener-Kronish JP. Hespiratory management after cardiac surgery. Chest 1989; 95: Hurlbut D, Myers ML, Lefcoe M, et al. Pleuropulmonary morbidity: internal thoracic artety versus saphenous vein graft. Ann Thorac Surg 1990; 50: Peng MJ, Vargas FS, Cukier A, et al. Postoperative pleural changes after coronary revascularization: comparison between saphenous vein and internal mammaty artety grafting. Chest 1992; 101: Weiss JM, Spodick DH. Association of left pleural effusion with pericardia! disease. N Eng! J M ed 1983; 308: Kouchoukos NT, Wreing TH, Murphy S, et a\. Risks of bilateral internal mammal)' artery bypass grafting. Ann Thorae Surg 1990; 49: Grossi EA, Esposito R, Harris LJ, et al. Sternal wound infections and use of internal mammmy artery grafts. J Thorae Cardiovasc Surg 1991; 102: Yamazaki K, Kato H, Tsujimoto S, e t a!. Diabetes mellitus, internal thoracic artery grafting, and risk of an elevated hemidiaphragm after coronary artery bypass surgety. J Cardiothorac Vase Anesth 1994; 8: Singh NP, Vargas FS, Cukier A, et a!. Arterial blood gases after coronary artery bypass surgery. Chest 1992; 102: Cosgrove DM, Lytle BW, Loop FD, e t al. Does bilateral internal mammaty artery grafting increase surgical risk? J Thorac Cardiovasc Surg 1988; 95: Aarnio P, Kettunen S, Harjula A. Pleural and pulmonmy complications after bilateral internal mammary artety grafting. Scand J Thorac Cardiovasc Surg 1991; 25: Ashraf SS, Shaukat N, Akhtar K, eta!. A comparison of early mortality and morbidity after single and bilateral internal mammary artery grafting ' ~ tthe h free right internal mammal)' attery. Br Heart J 1994; 72: Knapic P, Spyt TJ, Hichardson JB, et al. Bilateral and unilateral use of internal thoracic attery for myocardial revascularization. Chest 1996; 109: CHEST I 113 I 5 I MAY,
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