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1 Effect of Cardiopulmonary Bypass on Pulmonary Gas Exchange: A Prospective Randomized Study Craig M. Cox, FRCA, Raimondo Ascione, MD, Alan M. Cohen, FRCA, Ian M. Davies, FRCA, Ian G. Ryder, FRCA, and Gianni D. Angelini, FRCS Department of Anaesthesia and Bristol Heart Institute, University of Bristol, Bristol, United Kingdom Background. Conventional coronary artery bypass surgery is associated with postoperative pulmonary dysfunction. Inflammation due to cardiopulmonary bypass has been regarded as one of the main causes. In this study, we investigated the effect of coronary revascularization with or without cardiopulmonary bypass on pulmonary function. Methods. Fifty-two patients (40 male, mean age 60.1 years) were prospectively randomized to undergo coronary revascularization via median sternotomy, with or without normothermic cardiopulmonary bypass. Alveolar-arterial oxygen gradients were measured before and after induction of anesthesia, postoperatively in the intensive care unit during mechanical ventilation and 6 hours after tracheal extubation. The techniques of anesthesia and mechanical ventilation were standardized throughout. Results. Patient characteristics were similar in the two groups. The alveolar-arterial oxygen gradients increased progressively throughout the perioperative period, with no significant differences in the two groups at any time during the study. Conclusions. Myocardial revascularization with or without cardiopulmonary bypass caused a similar degree of pulmonary dysfunction, as assessed by alveolararterial oxygen gradient. Our study suggests that the deterioration in pulmonary gas exchange associated with cardiac surgery is due to factors other than the use of cardiopulmonary bypass. (Ann Thorac Surg 2000;69:140 5) 2000 by The Society of Thoracic Surgeons Lung dysfunction after cardiac surgery still remains an important cause of postoperative morbidity, despite continuing improvements in cardiopulmonary bypass (CPB) techniques and postoperative intensive care. Although severe morbidity, in the form of the adult respiratory distress syndrome (ARDS), is seen only rarely, more subtle degrees of pulmonary dysfunction occur frequently [1], often resulting in delay of tracheal extubation and continuing impairment of gas exchange. The etiology of pulmonary dysfunction after open heart surgery is thought to be multifactorial, occurring as a result of the combined effects of anesthesia, CPB, and surgical trauma [2]. CPB in particular is known to activate inflammatory processes [3], resulting in increased pulmonary capillary permeability and damage to lung parenchyma. Avoidance of inflammation due to CPB has been a major reason for the resurgence of interest in coronary artery bypass surgery (CABG) on the beating heart over the last few years [3]. Although evidence suggests that avoidance of CPB may result in improved myocardial protection [4], as well as reduced blood loss and transfusion requirements [3], the effect on pulmonary function in patients undergoing beating heart surgery has not Accepted for publication June 22, Address reprint requests to Dr Angelini, Bristol Heart Institute, Bristol Royal Infirmary, Bristol BS2 8HW, UK; g.d.angelini@bristol.ac.uk. previously been reported. In this study, we compared pulmonary function in two groups of patients randomized to undergo CABG via median sternotomy, with or without CPB. Pulmonary function was assessed by measurement of alveolar-arterial oxygen tension gradients and evaluation of the incidence of perioperative morbidity. Material and Methods Patient Selection Fifty-two patients undergoing elective CABG were enrolled in the study. Patients were prospectively randomized into two groups: a, who underwent conventional myocardial revascularization with normothermic CPB and cardioplegic arrest of the heart with intermittent antegrade warm blood cardioplegia; and a non-, who underwent revascularization on the beating heart. Exclusion criteria were as follows: known pulmonary disease, smoking within previous 6 months, poor left ventricular function (defined as ejection fraction less than 30%), recent myocardial infarction (within 1 month), or reoperation. The study protocol was approved by the United Bristol Healthcare Trust Ethics Committee. Anesthesia All patients received a standard anesthetic technique, using premedication with oral temazepam 20 to 30 mg, followed by total intravenous anesthesia. Propofol was 2000 by The Society of Thoracic Surgeons /00/$20.00 Published by Elsevier Science Inc PII S (99)

2 Ann Thorac Surg COX ET AL 2000;69:140 5 EFFECT OF CPB ON LUNG 141 infused throughout, initially at 3 mg/kg/h, and combined with remifentanil at 0.5 to 1 g/kg/min, with pancuronium 0.15 mg/kg or vecuronium 0.15 mg/kg. Increase in the rate of propofol infusion was permitted at the discretion of the anesthetist. The lungs were ventilated with air and oxygen (FiO 2 0.5), without positive end expiratory pressure (PEEP), to achieve normocapnia, using a tidal volume (V t ) of 8 to 10 ml/kg. Intraoperative fluids in both groups were given according to the discretion of the anesthetist. Surgical Approach All patients underwent median sternotomy. The pleura was opened for all cases in which the internal mammary artery was used. Heparin was given at a dose of 300 IU/kg, with additional doses of 3,000 IU in order to maintain the activated clotting time (ACT) over 480 seconds throughout CPB. CPB was instituted using ascending aortic cannulation and two-stage venous cannulation via the right atrium. A standard CPB circuit was used: a Bard tubing set, which included a 40- m filter, a Stockert roller pump (Sorin Biomedica, Midhurst, UK), and a hollow-fiber membrane oxygenator (Monolyth; Sorin Biomedica). The extracorporeal circuit was primed with 1,000 ml of Hartmann s solution, 500 ml of Gelofusine, 0.5 g/kg of mannitol, and 6,000 IU of heparin. Nonpulsatile flow was used, with a flow rate throughout bypass of 2.4 L/min/m. Mean arterial pressure (MAP) was maintained at 50 to 60 mm Hg during CPB, using metaraminol or phentolamine, as required. Systemic temperature was maintained between 34 C and 36 C. Mechanical ventilation was discontinued during CPB, though the tracheal tube was not disconnected from the breathing system. Myocardial protection was achieved using intermittent antegrade warm blood cardioplegia as described by Calafiore and associates [5]. Distal anastomoses were completed during a single period of aortic crossclamping. Proximal anastomoses were carried out using partial aortic clamping. Mechanical ventilation was restarted immediately before separation from CPB, using an FiO 2 of 0.6 and a V t of 8 to 10 ml/kg. After CPB, protamine was administered in a dose of 10 mg for each 1,000 IU of heparin given, with additional protamine given as required to return the ACT to preoperative levels. Non- Mean arterial pressure of 60 mm Hg or above was maintained throughout surgery by administration of fluid or metaraminol, as indicated by the hemodynamic condition. Esmolol was used to maintain heart rate between 50 and 65 beats per minute. Stabilization and exposure of the operative area was obtained using a combination of the technique previously described by our group [6], and the use of the Cardiothoracic System (CTS) retractor (CardioThoracic Systems Inc, Cupertino, CA). Before coronary snaring, heparin was given at a dose of 100 IU/kg and supplemented in order to maintain the ACT over 250 seconds. The target vessel was exposed and snared using two 4-0 Prolene sutures, with a soft piece of plastic snugger to prevent coronary injury. The coronary artery was then opened and the anastomosis performed. Improved visualization was achieved using a surgical blower-humidifier device (Surgical Site Visualization SSVW-002; Research Medical Inc, Midvale, UT) with 0.25-inch PVC gas line and fluid administration set connected to a regulated gas source of USP Medical Air (St. Paul, MN). Intracoronary shunting (Anastoflo Intravascular Shunt; Research Medical Inc) was not used routinely, but only if there was electrocardiographic or hemodynamic instability, or excessive bleeding during completion of the anastomosis. After completion of the anastomosis, protamine was administered in a dose of 10 mg for each 1,000 IU of heparin, with additional protamine given as required to return the ACT to preoperative levels. ITU Management At the end of surgery, patients in both groups were transferred to the intensive care unit (ICU). The lungs were ventilated with 60% oxygen using volume-controlled ventilation (Servo Ventilator 900C; Siemens, Stockholm, Sweden) and a tidal volume of 10 ml/kg with 5cmH 2 O of PEEP. Adjustments in FiO 2 and respiratory rate were made according to routine blood gas analysis, in order to maintain PaO 2 between 80 and 100 mm Hg, and PaCO 2 between 35 and 40 mm Hg. Forced air warming was used, until a stable nasopharyngeal temperature of 37 C had been reached. Fluid management postoperatively consisted of 5% dextrose infused at 1 ml/kg/h, with additional colloid (either Gelofusine or blood) to maintain normovolemia and hematocrit greater than 24%. Sample Collection Alveolar-arterial oxygen pressure [P(A-a)O 2 ] gradients were measured in all patients at four times: (1) before anesthetic induction, while breathing air; (2) postanesthetic induction after commencement of positive pressure ventilation (without PEEP); (3) postoperatively in the ICU, once nasopharyngeal temperature had reached at least 36.5 C; and (4) 6 hours after extubation. For times 2, 3, and 4, A-a gradients were measured at FiO 2 s of 0.35, 0.55, and Pulse oximetry was used to ensure patient safety with the use of lower FiO 2 s. In no patient did SpO 2 fall below 90%. Arterial blood sampling was not permitted after each change of FiO 2, until a 10-minute equilibration period had elapsed. To ensure accuracy of FiO 2 for measurements made after tracheal extubation, a sealed face mask was used, with a flow generator capable of delivering at least 30 L/min (Whisperflow 8500; Medic- Aid, Pagham, UK). A calibrated oxygen analyzer (Ohmeda 5120; BOC Healthcare, Hatfield, UK) was used to monitor the inspired oxygen concentration just proximal to the mask. All samples for blood gas analysis were taken in heparinized syringes and processed immedi-

3 142 COX ET AL Ann Thorac Surg EFFECT OF CPB ON LUNG 2000;69:140 5 ately (System 625; Radiometer Medical A/S, Copenhagen, Denmark). Calculation of Alveolar-Arterial Gradient The alveolar-arterial oxygen gradient was estimated according to the equation: P(A-a)O 2 PAO 2 PaO 2, where PAO 2 represents the partial pressure of oxygen in perfused alveoli (ie, excluding dead space) and PaO 2 is the partial pressure of oxygen in arterial blood. PAO 2 was estimated using the simplified form of the alveolar gas equation: PAO 2 PiO 2 PaCO 2 /RQ, with PiO 2 calculated as the product of the FiO 2 and the dry barometric pressure of 713 mm Hg (the difference between an assumed barometric pressure of 760 mm Hg and the saturated vapor pressure of water at 37 C, 47 mm Hg), and RQ (respiratory quotient) taken as Perioperative Morbidity The occurrence of postoperative pulmonary complications was noted. These included pneumothorax and lobar lung collapse (on chest roentgenogram as assessed by an anaesthetist unaware of the group allocation), chest infection (persistence of pyrexia requiring antibiotic therapy according to positive sputum culture), and ARDS. The duration of tracheal intubation, total blood loss, occurrence of perioperative myocardial infarction (POMI), and durations of ICU stay and hospital admission were also recorded. Statistical Analysis Patient characteristics and operative details were compared between the two groups using Student s t test and the 2 test where appropriate. Comparison of A-a gradients were made using three-way analysis of variance with a repeated measures design, using a generalized linear model examining for effects of time, FiO 2, and CPB, as well as for interactions between these variables (Minitab 10.1; Minitab Inc, State College, PA). Comparison of respiratory complications were made using Fisher s exact test or the 2 test where appropriate. A p value of less than 0.05 was considered to be statistically significant. Results There were no significant differences in the patient characteristics or operative details between the two groups (Tables 1 and 2). Chest tube drainage and volume of fluid administered during the first 24 hours postoperatively were significantly less in the non-cpb group (Table 3). There was no significant difference between the two groups in the baseline A-a gradient measured before induction of anesthesia (CPB group mm Hg; non-cpb group mm Hg, mean SD). Similarly, there was no significant difference in the A-a gradient measured after induction of anesthesia (Figs 1 to 3). Thereafter, A-a gradients rose progressively in both groups ( p 0.001, for each FiO 2 ), but no significant differences were found between the groups at any stage Table 1. Preoperative Patient Characteristics Variable Non- Gender (M/F) 22/4 18/8 Age (y) Parsonnet score Single-vessel disease 4 1 Two-vessel disease 7 17 Three-vessel disease 15 8 Angina class I 7 10 II III 9 5 IV 0 0 Left ventricular function Good (EF 50%) Moderate (EF 30 50%) 7 6 Results are shown as frequencies, except where stated. Angina class was graded according to the Canadian Cardiac Society classification. Ages and Parsonnet scores are shown as mean standard deviation. There were no significant differences between the groups for any of the observations. during the perioperative period, with any of the FiO 2 levels studied (Figs 1 to 3). No deaths occurred during the study. The occurrence of perioperative morbidity is presented in Table 3. Although the total number of respiratory complications was significantly lower in the non-cpb group, there were no significant differences in the number of patients with complications or in the incidences of individual complications, such as pneumothorax, chest infection, or lung collapse. No statistically significant difference was found regarding the duration of tracheal intubation. There were no occurrences of ARDS or POMI in either group. Table 2. Surgical Data Variable Non- Duration of CPB (min) Duration of aortic crossclamping (min) Grafts per patient IMA to LAD grafts Diagonal grafts 9 6 RCA or PDA grafts Proximal Cx grafts 7 6 BIMA grafts 6 6 Radial artery grafts 1 4 Results are shown as frequencies, except where stated. Durations of CPB and aortic cross-clamping, and number of grafts per patient, are shown as mean standard deviation. There were no significant differences between the groups for any of the observations. BIMA bilateral internal mammary artery; Cx circumflex artery; IMA internal mammary artery; LAD left anterior descending coronary artery; PDA posterior descending artery; RCA right coronary artery.

4 Ann Thorac Surg COX ET AL 2000;69:140 5 EFFECT OF CPB ON LUNG 143 Table 3. Outcome and Morbidity Variable Non-CPB Group Net fluid balance at 24 h (ml) 1, a Total chest tube drainage (ml) 1, a Intubation time (h) Number patients suffering 10 3 respiratory complications Total respiratory complications 13 4 a Chest infection 5 2 Pneumothorax 4 1 Lung collapse 4 1 ARDS 0 0 POMI 0 0 Length of stay in ITU (days) Length of stay in hospital (days) Results are shown as frequencies, except where stated. a p ARDS adult respiratory distress syndrome; ITU intensive therapy unit; POMI perioperative myocardial infarction. Comment The desire to minimize complications associated with CPB, as well as the current trend towards cost containment [7], has led to renewed interest in CABG without the use of CPB [4, 8]. Brasil and colleagues [3] have shown that the inflammatory response associated with cardiac Fig 2. Alveolar-arterial oxygen pressure gradients in the CPB (triangle) and non-cpb (square) groups measured at FiO (see Fig 1 for details of timings). surgery using CPB is virtually undetectable in surgery performed without CPB. Despite this, only few studies have looked at the effects on end-organ function in association with procedures without CPB. Most studies have investigated the effects on myocardial function, Fig 1. Alveolar-arterial oxygen pressure gradients in the CPB (triangle) and non-cpb (square) groups measured at FiO (Post induction) After induction of anesthesia and tracheal intubation; (Post ITU admission) after admission to ITU; (Post extubation) after tracheal extubation. Fig 3. Alveolar-arterial oxygen pressure gradients in the CPB (triangle) and non-cpb (square) groups measured at FiO (see Fig 1 for details of timings).

5 144 COX ET AL Ann Thorac Surg EFFECT OF CPB ON LUNG 2000;69:140 5 which appears to be improved with avoidance of CPB [4]. However, because of the particular considerations affecting myocardial function, namely aortic cross-clamping and cardioplegic arrest, it is difficult to extrapolate these results to other organs, such as the lung. The deterioration in gas exchange after cardiac surgery with CPB is thought to be multifactorial, occurring as a result of the combined effects of anesthesia, surgical trauma, and CPB [2]. Extracorporeal circulation is thought to have a detrimental effect on lung function for a variety of reasons [9, 10], including leukocyte activation and activation of the alternate complement pathway. Leukocyte activation causes release of oxygen-derived free radicals, proteases, leukotrienes, and other arachidonic acid metabolites, as well as neutrophil clumping with obstruction to capillary blood flow, and release of elastase into the pulmonary circulation. Postoperative lung dysfunction even after uncomplicated procedures [11] is quantifiable as a predictable and consistent deterioration in gas exchange, in the form of a widening of the alveolar-arterial oxygen gradient. In addition, pulmonary compliance is reduced, as is vital capacity. Work of breathing is increased and some degree of atelectasis is usually present, in particular affecting the lower lobe of the left lung. Despite the mechanisms by which CPB-mediated inflammation might affect pulmonary function, we found no differences between A-a oxygen gradients in patients who had undergone surgery with or without CPB. As with previous studies, A-a gradients increased during the perioperative period, but this deterioration occurred equally in both groups, suggesting that CPB was not associated with any significant lung dysfunction other than that caused by the operative and anesthetic techniques themselves. Our results conflict with previous clinical studies [1, 12], in which pulmonary dysfunction in patients after CPB was more severe compared with controls. These studies were limited, however, by using comparison with patients undergoing noncardiac surgical procedures, such as major abdominal [1] or peripheral joint surgery [12]. To our knowledge, the only other report on the effect of CPB on lung function using controls undergoing median sternotomy is that of Magnusson and coworkers [13], who studied lung function in pigs after hypothermic CPB. In contrast to our own results, they found that atelectasis and intrapulmonary shunt were increased in the group that had undergone CPB. However, Magnusson and coworkers studied lung function 45 minutes after separation from CPB, whereas our first measurement after CPB was made later, after arrival in the ICU. Furthermore, their use of hypothermic CPB, an FiO 2 of 1.0 on separation from CPB, and disconnection of the breathing system during CPB might also be relevant. Possibly, the most important factor accounting for the different results of the two studies is the significant degree of acidosis and myocardial dysfunction caused by CPB in Magnusson and coworkers study. Such deterioration in general condition did not occur in our study, and this may have allowed improved preservation in pulmonary function. Indeed, even though there was perioperative deterioration in gas exchange in patients who underwent CPB in our study, this was to a lesser degree than in previous studies, which have measured A-a gradients after CPB [14, 15]. This relative preservation of perioperative lung function may account for the absence of any difference with patients not undergoing CPB, and suggests that abnormalities of oxygenation are becoming a less important problem of CPB, at least in relatively healthy patients undergoing cardiac surgery. A number of other aspects relating to our study merit further discussion. First, the only measure of pulmonary function used in our study was the alveolar-arterial (A-a) oxygen gradient. Measurement of the A-a gradient offers a simple and objective method of assessing gas exchange. Alternative methods, such as direct measurement of pulmonary shunt fraction or characterization of ventilation-perfusion relationships using the multiple inert gas technique, would have provided a more precise assessment of the disturbance in gas exchange but would have meant an increase in complexity unnecessary for the purposes of identifying differences in gas exchange between the two study groups. Measurement of other aspects of pulmonary function, such as lung volumes, interstitial lung water, or indices of pulmonary mechanics (eg, compliance or airway resistance) [16], would also have added inherent complexity without, in our opinion, improving on the clinical relevance of the measurement of gas exchange using the A-a gradient. Our decision to use three different inspired oxygen concentrations is based on the demonstration by Roe and Jones [17] that the difference in pulmonary arterial oxygen content (and therefore the difference in the A-a gradient) between an ideal lung and a lung with V/Q abnormality varies with FiO 2, being greater at lower PiO 2 values. Postoperative blood loss was greater in the CPB group, in keeping with previous reports of non-cpb revascularization [3]. Postoperative fluid management was not standardized in either group, resulting in a significantly more positive net fluid balance in the CPB group, presumably in association with the greater blood loss in this group. This effect might have been expected to accentuate any adverse effects of CPB on pulmonary function. It is therefore unlikely that not standardizing fluid management led to our inability to detect any detrimental effect of CPB on gas exchange. One implication from our study is that attempts to reduce postoperative pulmonary dysfunction after cardiac surgery might be better concentrated on maneuvers to reverse the detrimental effects of anesthesia and surgery on lung function, rather than on CPB-mediated effects. Adverse effects of anesthesia and surgery include processes such as the effect of pleural opening, the effects of anesthesia and positive pressure ventilation, direct contact with the lungs during intrathoracic surgery, inflammation due to surgical trauma and postoperatively, and restriction on coughing and deep breathing by postoperative pain [18, 19]. Although some of these may result in increased interstitial fluid in the lung, the most

6 Ann Thorac Surg COX ET AL 2000;69:140 5 EFFECT OF CPB ON LUNG 145 consistent result of all of these processes is regional atelectasis, which is almost universally seen after cardiac surgery. The importance of atelectasis after CPB was demonstrated by Magnusson and coworkers [20], who achieved complete prevention of intrapulmonary shunting after CPB in pigs, by prevention of atelectasis using a vital capacity maneuver combined with subsequent avoidance of 100% oxygen. This approach may offer a means of minimizing postoperative pulmonary dysfunction after cardiac surgery, though it remains to be seen whether it will eventually become used in patients undergoing cardiac surgery, where the application of high airway pressures may have undesirable hemodynamic consequences. In conclusion, we report that in patients with good ventricular function and no preexisting pulmonary disease, CABG with or without the use of CPB caused a similar degree of postoperative lung dysfunction. This suggests that the deterioration in pulmonary gas exchange after cardiac surgery is more likely a consequence of the anesthetic and surgical techniques used, rather than an effect of cardiopulmonary bypass. We thank Andrew M. S. Black, FRCA, for his advice and practical assistance with the statistical analysis. This study was supported by the British Heart Foundation and the Sir Sigmund Warburg Voluntary Settlement Fund. References 1. Taggart DT, El-Fiky M, Carter R, Bowman A, Wheatley DJ. Respiratory dysfunction after uncomplicated cardiopulmonary bypass. Ann Thorac Surg 1993;56: Matthay MA, Wiener-Kronish JP. Respiratory management after cardiac surgery. Chest 1989;95: Brasil LA, Gomes WJ, Salomao R, Buffolo E. Inflammatory response after myocardial revascularization with or without cardiopulmonary bypass. Ann Thorac Surg 1998;66: Pfister AJ, Zaki MS, Garcia JM, et al. Coronary artery bypass without cardiopulmonary bypass. Ann Thorac Surg 1992;54: Calafiore AM, Teodori G, Mezzetti A, et al. Intermittent antegrade warm blood cardioplegia. Ann Thorac Surg 1995; 59: Lucchetti V, Angelini GD. An inexpensive method of heart stabilization during coronary artery operation without cardiopulmonary bypass. Ann Thorac Surg 1998; Westaby S. Cutting costs in cardiac surgery. Time to break the mould. Surgery 1991;86: Westaby S. Coronary artery surgery without cardiopulmonary bypass. Br Heart J 1995;73: Body SC. The endothelial cell s role in CPB-mediated bleeding and inflammation. In: Society of Cardiovascular Anesthesiologists 20th Annual Meeting: Workshops Handbook. Richmond VA: Society of Cardiovascular Anesthesiologists; 1998: Royston D. The inflammatory response and extracorporeal circulation. J Cardiothorac Vasc Anesth 1997;11: Conahan TJ. Complications of cardiac surgery. In: Kaplan JA, ed. Cardiac anesthesia. 3rd ed. Philadelphia: WB Saunders, 1993: Royston D, Minty BD, Higenbottam TW, Wallwork J, Jones GJ. The effect of surgery with cardiopulmonary bypass on alveolar-capillary barrier function in human beings. Ann Thorac Surg 1985;40: Magnusson L, Zemgulis V, Wicky S, Tyden H, Thelin S, Hedenstierna G. Atelectasis is a major cause of hypoxemia and shunt after cardiopulmonary bypass. Anesthesiology 1996;87: MacNaughton PD, Braude S, Hunter DN, Denison DM, Evans TW. Changes in lung function and pulmonary capillary permeability after cardiopulmonary bypass. Crit Care Med 1992;20: Birdi I, Regragui IA, Izzat MB, et al. Effects of cardiopulmonary bypass temperature on pulmonary gas exchange after coronary artery operations. Ann Thorac Surg 1996;61: Macnaughton PD. Assessment of lung function in the ventilated patient. Intensive Care Med 1997;23: Roe PG, Jones JG. Analysis of factors which affect the relationship between inspired oxygen partial pressure and arterial oxygen saturation. Br J Anaesth 1993;71: Johnson D, Hurst T, Thomson D, et al. Respiratory function after cardiac surgery. J Cardiothorac Vasc Anesth 1996;10: Briesblatt N, Stein K. Acute myocardial dysfunction and recovery: a common occurrence after coronary bypass surgery. J Am Coll Cardiol 1990;15: Magnusson L, Zemgulis V, Tenling A, et al. Use of a vital capacity maneuver to prevent atelectasis after cardiopulmonary bypass. Anesth 1998;88:

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