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Influence of PEEP Ventilation Immediately after Cardiopulmonary Bypass on Right Ventricular Function
Influence of PEEP Ventilation Immediately after Cardiopulmonary Bypass on Right Ventricular Function* Joachim Boldt, M.D.; Dieter Kling, M.D.; Benno v Bormann, Hans Scheld, M.D.;t and Gunter Hempelmann, M.D.
Ventilation with positive end-expiratory pressure (PEEP) is often the appropriate therapy for treating patients with impaired pulmonary function after cardiac surgery procedures. Circulatory depression, however, sometimes limits the level of PEEP. This study was conducted to investigate the effects of PEEP ventilation ( + 15 cmH 20) immediately after weaning from cardiopulmonary bypass 1) period of PEEP application and 45 min thereafter; 2) period of PEEP application on right ventricular hemodynamics using a new thermodilution technique for measuring right ventricular ejection fraction (RVEF), right ventricular end-diastolic and end-systolic volumes (RVED~ RVESV). Forty patients undergoing aortocoronary bypass grafting were retrospectively divided into two groups: group 1 (n = 24) in which RVEF was reduced significantly (4~28 percent), and group 2 (n = 16) in which RVEF remained almost unchanged. In patients in group 1, stenosis of the right coronary artery (RCA) was significantly more pronounced
Controlled mechanical ventilation with positive end-expiratory pressure (PEEP) is ubiquitously used in patients with pulmonary failure, although its beneficial influence on the respiratory system is accompanied by detrimental effects on the circulatory system. 1-3 The mechanism by which PEEP ventilation decreases cardiac output (CO) has been the subject of several investigations, but it still is not entirely clear. The decrease in CO is attributed mainly to a decrease in venous return due to elevated intrathoracic pressure." Other studies suggest that this effect is caused by an increase in right ventricular afterload due to an increase in pulmonary impedance," decreased biventricular end-diastolic volume," altered ventricular interdependence by leftward displacement of the ventricular sep tum.F-" or decreased myocardial contractility due to altered myocardial blood How? or a myocardial depressing factor induced by PEEEIO The use of PEEP after cardiopulmonary bypass (CPB) seems reasonable, but its routine application is controversially discussed because of its possible negative *From the Department of Anesthesiology and Intensive Care Medicine (Head: Prof Dr G. Hempelmann), Justus-Liebig-University Giessen, West Germany: tDepartment of Cardiovascular Surgery (Head: Prof Dr FW Hehrlein), Manuscript received November 18; revision accepted February 24. 566
in comparison to the others and was detected to be responsible for the different reaction of RVEF (analysis of co-variance). Application of PEEP immediately after weaning from CPB was followed by an increase in RVESV ( + 4 percent; RVEDV - 1 percent) in group 1, whereas patients of group 2 differed significantly (RVESV -14 percent; RVEDV - 15 percent). Cardiac index was decreased only in group 1 (- 32 percent). During the second period of PEEP application, no further difference could be observed between the groups. We conclude that hemodynamic changes related to PEEP ventilation are minimal in the intact right ventricle. Abnormalities in right ventricular function due to stenosis of the RCA, however, have had marked clinical influence on the circulatory response. Monitoring of right ventricular function seems to be of benefit for cardiac surgery patients in this situation. (Chest
1988; 94:566-71)
effects on circulatory stability in this period. Recent studies have produced evidence that right ventricular function becomes increasingly important in patients undergoing aorto-coronary bypass grafting." Therefore, the aim of this study was focused on right ventricular hemodynamics during PEEP application immediately after weaning from CPB using a new thermodilution method, which allows sequential intraoperative estimation of right ventricular function. METHODS
The investigation included 40 patients undergoing elective aortocoronary bypass grafting. Patients with depressed myocardial function (left ventricular ejection fraction <50 percent) or concomitant pulmonary hypertension (PAP > 15 mm Hg) were excluded from the study: Informed consent was obtained from each patient according to the protocol of the Human Study Committee. Premedication and anesthesia procedures were standardized and comparable for all patients consisting of weight-dependent dosages of fentanyl, midazolam and pancuronium bromide. Controlled mechanical ventilation was performed with a Flo, of O. 5 during the whole investigation period. Cardiopulmonary bypass (CPB) was instituted with membrane oxygenators and a non-pulsatile flow of 2.4 L'min-m-, Myocardial preservation was performed with multidose Bretschneider's cardioplegia solution, and myocardial surface was cooled with ice-cold saline solution. During cross-clamping of the aorta (= ischemia) moderate hypothermia (rectal temperature 32.2°± l.O°C, esophageal temperature 32.8°±O.9°C) was used. Hemodynamic variables measured and derived hemodynamic paPEEP Immediately after Cardiopulmonary Bypass (Boldt at al)
Table I-Measured and Calculated Hemodynamic Variables Mean arterial pressure (MAl) Heart rate (HR) Pulmonary artery pressure (PAP) Pulmonary capillary pressure (PCP) Right atrial pressure (RAP) Systolic right ventricular pressure (RVPsyst) Right ventricular enddiastolic pressure (RVEDP) Cardiac output (CO) Right ventricular ejection fraction (RVEF) Right ventricular enddiastolic volume index (RVEDVI) Right ventricular endsystolic volume index (RVESVI) Pulmonary vascular resistance (PVR) rameters are listed in Table 1. The multilumen balloon-flotation pulmonary artery catheter used in this study was specially designed to measure right ventricular ejection fraction (RVEF). It is mounted with a fast response thermistor (FRT), which is rapid enough to record beat-by-beat the plateaus of the rapid step changes on the descending limb of the thermodilution washout curve. 12,13 This technology allows determination of the residual end-diastolic blood volume (RVEDV) with the help of a bedside microprocessor (REF-I, Edwards Lab, Santa Ana, CA); RVES,V (RVEDV-stroke volume) and RVEF (EDV-ESV/EDV) were calculated, too..Theoretic background and detailed technical features have been discussed elsewhere.P" CO and RVEF were measured in triplicate at the end of the expiration and its mean values were used for statistical analysis. Immediately after weaning from CPB, all patients were ventilated without positive end-expiratory pressure (ZEEP) and the first measurements after CPB were performed.. Then a PEEP of 15 cmH 20 was applied for 10 min and measurements were performed again; ZEEP ventilation was continued thereafter Heparin was then antagonized by protomine and washed erythrocytes (cellsaving system) from the resting volume of the heart lung machine were infused. After chest closing, measurements were performed again while the patients were mechanically ventilated with ZEEE For the next ten min PEEP was instituted with 15 cmH 20 again and hemodynamics were measured as well. Data points could be summarized as follow: 1. before onset of the operation (ZEE~ chest closed), 2. before start of CPB (ZEE~ chest and pericard open), 3. immediately after the end of CPB (ZEE~ chest and pericard open), 4. 10 min after PEEP ventilation with 15 cmH 20 (pericard and chest open), 5. after chest was closed and volume (washed red blood cells from the cell saver) was applied (ZEEP), 6. 10 min after PEEP ventilation with 15 cmH 20 (pericard and chest closed), 7. at the end of the operation (ZEE~ chest closed). Mean values (X) and standard deviation (SD) were calculated for each parameter at each data point; analysis of variance and analysis of co-variance were used for statistical interpretation; p values <0.05 were considered significant. RESULTS
The patients were retrospectively subdivided into two groups according to the change in RVEF after PEEP application immediately after weaning from CPB: group 1 (n = 24), where RVEF decreased, and group 2 (n = 16), where RVEF remained almost unchanged. U sing analysis of co-variance, the degree of
RCA-stenosis was detected to be the decisive factor for the change in RVEF. Analysis of preoperative catheterization data revealed that in patients in group 1, stenosis of the right coronary artery (RCA) was significantly more pronounced (with RCA-stenosis) in comparison to patients in group 2 (without RCAstenosis). Only in patients of group 1, RCA revascularization or coronary end-arterectomy (CEA) was performed. The biometric data were without differences between the groups (Table 2). The duration of CPB, as well as of ischemia was significantly longer in the patients with RCA in comparison to the other group, due to additional revascularization of the RCA in these patients. The amount of volume (washed red blood cells) applied after ECC was standardized (the whole resting volume from the circuit was concentrated) and comparable for both groups (Taqle 3). According to the grouping of patients, application of PEEP immediately after weaning from CPB was followed by a decrease in RVEF only in patients with RCA-stenosis (Fig 1), whereas during the second period of PEEP ventilation, no further difference between the groups could be demonstrated. CO was decreased only in group 1 patients during the first period of PEEP application (Fig 2). RVEDVI decreased significantly in patients in group 2, in patients with RCA-stenosis; however, no significant decrease was seen (Fig 3). RVESVI was slightly increased in this group in contrast to group 2, where RVESVI decreased significantly; rio additional difference between the groups could be observed during the second period of PEEP application (Fig 3). With regard to the other hemodynamic variables, the application of PEEP immediately after weaning from CPB was followed by a significant decrease in MAP and an increase in PVR, RVPsyst and RVEDP only in the group with RCA Table 2-Biometric Data and Data from Surgical Procedure /
Age (years) Weight (kg) Height (em) LVEDP (mm Hg) LVEF (%) RCA-stenosis (%) CPB (min) Ischemia (min) Volume (ml)
Group 1 (n=24)
Group 2 (n=16)
58.2±4.7 78.2±3.3 172±8 13.6±5.2 63.6±7.1 88.8±7.2 133.1±20 88.4± 15 766± 115
60.6±6.9 74.3±2.9 174±9 13.6±5.8 58.6± 11 10.2± 10.2* 103.2± 11* 63.9± 12* 700± 180
CPB = duration of cardiopulmonary bypass; Ischemia = duration of cross-clamping of the aorta; LVEF = left ventricular ejection fraction; LVEDP = left ventricular enddiastolic pressure; Volume = amount of volume given after CPB; group 1 = with right coronary artery (RCA) stenosis; group 2 = without right coronary artery (RCA); stenosis; X± SD; *p
567
3.5
1---1
3.0
c 2.5
P B
2.0
X ±SD • p
0-0
< 0.05
Group 1 (n
e---e Group 2
(n
= 24) = 16)
•
1.5
ZEEP
PEEP
+15 em H 2 O
PEEP
ZEEP
+15 em H2O
FIGURE 1. Change in right ventricular ejection fraction (RVEF). Group 1: with right coronary artery (RCA) stenosis; group 2: without right coronary artery (RCA) stenosis.
attention than the physically more dominant left ventricle. A tendency to overlook the right ventricle as an important part of the circulatory system has been reinforced by some previous studies in which the right ventricle has been considered a nonfunctional, passive conduit for accepting venous blood and transfusing it through the pulmonary system;" Later studies have yielded a more complete picture stressing
stenosis (Table 3). The use of pharmacologic support (epinephrine, dopamine) was greater in patients of group 1 without being statistically significant. None of the patients suffered from sequelae attributable to the study DISCUSSION
In the past, the right ventricle has received less 50
40
IR V E F c P
B
(%)
1~1
1
0-0
30
Group 1
e--e Group 2
=24) (n = 16) (n
i±SD • p< 0,05
_....
•
20 I
I
ZEEP
PEEP
+15 em H20
I
ZEEP
I
PEEP
+15 em H20
FIGURE 2. Changes in cardiac output (CO) in the two groups; group 1: with right coronary artery (RCA) stenosis, group 2: without right coronary artery (RCA) stenosis.
568
PEEPImmediately after Cardiopulmonary Bypass(Boldt at al)
65 60 55 50
I R V E $ V I (ml/m2) I 11
11
'I
L~~
C p
B
e
'E at)
-.::t
45
40
x± SO
~ ~
* p < 0,05
I RVEDVQml/m2j]
90
1 1
11
85 80
75
(n = 24) (n = 16)
Group 1 Group 2
II
c
P B
70 65 u.J..LJ.,j.lJ.J-'-U..ll-----,
I:
----.---_~=_--.-_
ZEEP
PEEP
+15 em H20
ZEEP
-
-~----I-
- --
PEEP
+15 em H2
FIGURE 3. RVEDVI and RVESVI in the two groups during PEEP application; group 1: with right coronary artery (RCA) stenosis; group 2: without right coronary artery (RCA) stenosis.
continuous interplay between the right and left ventricles due to the anatomic relationship of the two sides of the heart. 7,16 The right ventricle constitutes the pump that conveys hydraulic energy to the blood passing from the low-pressure venous reservoir to the
medium-high pressure reservoir of the pulmonary arterial blood and is ensuring delivery of the preload required to subserve left ventricular output. 17 The importance of the right ventricle has been documented recently by Cohne et aP8 who reported severe right ventricular dysfunction and circulatory instability in patients with apparent right ventricular infarction. Although it is reasonable to assume that a decreased venous return due to increased intrathoracic pressure is the primary mechanism for a decrease in CO during PEEP ventilation, recent clinical and experimental studies have suggested that additional factors may also contribute to the decrease in CO. The increase in right ventricular afterload results in an elevated right ventricular stroke work and consequently in a higher right ventricular O~ consumption." An augmented contractile response of the right ventricle is necessary in acute PAP increase requiring an increase in right ventricular coronary blood flow A decrease in myocardial blood flow (MBF) has been elucidated as a contributing factor to the depression of cardiac function during application of PEEB8,I5 Venus et a}19 speculated that high levels of PEEP reduced cardiac output independent of venous return due to a decrease in MBF possibly mediated by reflex stimulation of lung receptors. Cassidy et al'" reported evidence that lung inflation produces a vagally mediated reflex depression of both the right and left ventricular performance. We have chosen PEEP of 15. cmH 20 because Metzler et aPO found that only high levels of PEEP elevating pulmonary vascular resistance limit myocardial performance of the right ventricle resulting in a significant reduction of CO. PEEP was found to be associated with a large decrease in left and right
Table 3-Hemodynamic Parameterswithin Investigation Period Parameter MAP (mmHg) HR (min-i) PAP (mmHg) PCP (mmHg) PVR (dyn-s-cm -5) RAP (mm Hg) RVP syst (mmHg) RVEDP (mmHg)
Group
1 2
1 2 1 2 1 2 1 2 1 2 1 2 1 2
Before Operation
Before ECC
86.9± 10.2 82.1±9.8 72.2± 12.0 78.0± 12.1 15.4±4.1 14.8±3.7 8.4±2.9 6.9±2.1 104±24 120±30 4.0±2.1 3.2±LO 24.8±6.7 26.6±6.0 4.0±1.8 2.8±1.0
82.5±13.2 74.4± 10.0 77.0± 10.2 87.0± 11.1 15.2±3.5 12.9± 1.9 8.3±2.4 6.9±2.1 111±20 130±22 4.6± 1.2 4.2±1.4 27.0±6.1 25.0±6.1 4.3±1.9 3.0±1.0
ECC
ZEEP
PEEP +15
ZEEP
PEEP +15
End of Operation
83.4± 11.2 82.4± 12.4 88.8± 12.0 94.6± 11.2 15.0±2.1 15.2±4.1 8.5±2.1 7.8±4.0 100±14 120± 19 5.0± 1.2 4.2± 1.0 29.2± 10.0 33.6±7.5 4.9±2.0 3.6±1.6
68.5± 12.0* 81.0± 15.0 90.4± 12.1 92.0±6.9 20.5±4.0 21.0±3.6 12.8±3.1 11.8±3.2 184±33* 162±21 8.3± 1.9 7.2±2.0 36.0±5.0* 36.8±3.0 7.6± 1.8* 5.4±2.6
96.8± 12.1 99.2± 14.1 91.0± 10.0 92.0±6.8 18.0±4.2 20.0±6.7 11.0±3.5 11.6±4.0 105± 15 131±22 7.2±1.8 6.2±2.1 31.2±4.3 34.2±6.0 6.7±1.3 5.1± 1.9
92.5± 14.2 93.0± 13.2 92.7± 10.2 92.0±7.6 22.8±3.7 23.9±5.0 15.4±3.6 13.8±4.0 144±30 160±22 10.8± 1.6 10.2±2.9 36.1±4.1 38.0±5.2 9.6±2.1 8.6±2.0
98.8± 10.0 99.0± 12.2 92.0±9.8 95.2±7.6 18.1±3.0 20.4±2.1 10.7±3.1 12.2± 1.0 110± 19 128±21 7.4±3.0 7.0±2.1 30.2±6.0 32.8±6.2 6.9±2.5 6.8±2.1
CPB = cardiopulmonary bypass; group 1 = with right coronary artery (RCA) stenosis; group 2 = without right coronary artery (RCA); stenosis; x±SD; *p<0.05 CHEST / 94 / 3 / SEPTEMBER, 1988
569
ventricular end-diastolic volumes." Right ventricular volume and performance, however, have been difficult to obtain because of the functional anatomy and complex geometry 22 The correlation between the new thermodilution technique used in this study for estimation of RVEF and other methods such as first pass technique or equilibrium gated techniques is significant. 12 Traditionally monitored hemodynamic parameters such as RAp'or RV~ however, have failedto be representative for right ventricular function. RVED~ too, shows considerable individual variations and does not have a close relationship to ejection fraction or clinical evidence of right heart decompensation. 8 In our patients without ~CA stenosis, RVEDVand RVESV were reduced significantly by PEEP ventila- . tion which is in accordance with other studies." In the group with RCA-stenosis, however, right ventricular volume was not decreased significantly thus showing that the right ventricle was insufficient and not able to transport blood adequately through the pulmonary vessels, although blood supply to the right chamber is reduced by PEEP; RVEF was decreased in these patients demonstrating that the right ventricle was unable to make the adaptations required. MAP was Significantly reduced only in the "withRCA-group" and the resulting decrease in right coronary perfusion is contributing to the vicious circle. A critical decrease in right ventricular O 2 supply/demand ratio may have developed and resulted in right ventricular ischemia and further deterioration of its function. In agreement with our results, Skarvan et al23 demonstrated that surgical revascularization of the RCA may frequently be associated with right ventricular. dysfunction. Results from Priebe" indicate that severe right ventricular myocardial dysfunction may develop during moderate pulmonary hypertension only when right coronary artery (RCA) stenosis is present. It is stressed that patients not exhibiting clinical symptoms of coronary insufficiency at rest may develop severe myocardial dysfunction during only mild increases in pulmonary artery pressure. In the normal right ventricle, however, a mean PAP as high as 40 mm Hg may be sustained without reduction in CO. Rabinovitch et al25 concluded from their studies that the right side of the heart should not be neglected to achieve optimal myocardial protection during cardiac operations. High-grade RCA lesions can prevent the cold cardioplegia .solution from reaching the right ventricular myocardium at a sufficient rate.f" Moreover, the right heart is not as well submerged as the left ventricle in the pericardial cold saline solution bath used for supplementary topical cooling due toits ventral location. Therefore, the right ventricle seems to be the most vulnerable aspect of an ischemic 570
heart. 27,28 Therefore, overall right ventricular dysfunction after CPB is not determined by the loading conditions alone. Local myocardial and septal involvement is suspected to be an important determinant of right ventricular function as well. 29 Forty-five min after weaning from CPB, a sufficient reperfusion of the myocardium with an improvement in myocardial O 2 supply may have contributed in our patients to the fact that there was no more difference in right ventricular function between the two groups during the second period of PEEP application, and MAP and CI could be maintained in this situation. On the other hand, volume expansion (eg, by infusion of washed erythrocytes) is thought to be an important mechanism by which CO (and MAP) can be restored when it is reduced as a result of increased right ventricular afterload or depressed contractility " This mechanism, however, is limited because increasing right ventricular volume may hav~ some advers~ effects such as increased wall tension with an augmented myocardial oxygen demand, decreased left ventricular compliance and possible tricuspid regurgitation. It can be concluded that application of PEEP is followed by complex hemodynamic changes. An increase in right ventricular afterload is tolerated by the right ventricle provided there is no factor concomitantly limiting the right ventricular contractility such as a high grade RCA stenosis. The present data suggest that right ventricular dysfunction secondary to ineffective myocardial preservation or 'to reduced blood flow may also result in significant impairment in global cardiac performance when PEEP is applied. Thus, the right ventricle seems to play an important role and might be the limiting factor in weaning from CPB. Precise monitoring ofpulmonary and right ventricular hemodynamics are of greatest importance in this situation. REFERENCES 1 Biondi J~ Schulman DS, Matthay RA, Barash PG. Correlation of left ventricular peak filling rate and right ventricular ejection fraction during positive end-expiratory pressure: the role for ventricular interdependence (abstract). 9th Annual Meeting, Society of Cardiovascular Anesthesiologists, 1987 Holland L, MacGregor D, Bromber2 Robotham JL, Lixfeld ger-Barnea B. The effects of positive end-expiratory pressure on right and left ventricular performance. Am Rev Resp Dis 1980;121:677-83 3 Santamore Bove AA, Heckman JL. Right and left ventricular pressure-volume response to positive end-expiratory pressure. Am J Physiol 1984; 246:Hl14-19 4 Guyton AC. Circulatory physiology: Cardiac output and its regulation. Philadelphia: WB Saunders, 1969:380-89 5 Prewitt RM, Wood LDH. Effect of positive end-expiratory pressure on ventricular function in dogs. Am J Physiol 1979; 236:534-43 6 Viquerat C, Righetti A, Suter :P. Biventricular volumes and functions in patients with adult respiratory distress syndrome
w:
w:
PEEP Immediately after CardiopUlmonary Bypass (Boldt at al)
ventilated with PEEE Chest 1983; 83:509-14 7 BakerBJ, Franciosa KJA. Effect of the left ventricle on the right ventricle. Cardiovasc Clin 1987; 17:145-55 8 Wiedemann H:p, Matthey RA. Acute right heart failure. Crit Care Clinics 1985; 1:631-61 9 Vlahakes GJ, Turley K, Hoffman JE. The pathophysiology of failure in acute right ventricular hypertension: hemodynamic and biochemical correlations. Circulation 1981; 63:87-95 10 Cassidy SS, Eschenbacher WL, Robertson CH Jr. Cardiovascular effects of positive-pressure ventilation in normal subjects. J Appl Physiol1979; 47:453-61 11 Hines R, Barash E Intraoperative right ventricular dysfunction detected by a right ventricular ejection fraction catheter. J Clin Monitoring 1986; 2:206-08 12 Kay HK, Afshari M, Barash :P, Webler ~ Iskandrian A, Bemis C, et al. Measurement of ejection fraction by thermodilution techniques. J Surg Res 1983; 34:337-46 13 Maruschak GF, Schauble JF. Limitation of thermodilution ejection fraction: Degration of frequency response by catheter mounting of fast response thermistor. Crit Care Med 1986; 13:679-82 14 Matthay RA, Berger H. Noninvasive assessment of right and left ventricular function in acute and in chronic respiratory failure. Crit Care Med 1983; 11:329-37 15 Sibbald WS, Drieger AA. Right ventricular function in acute disease states: Pathophysiologic consideration. Crit Care Med 1983; 11:339-45 16 Weber KT: Janicki JS, Shorff S, Fishman AE Contractile mechanics and interaction of the right and left ventricles. Am J Cardiol1981; 47:686-95 . 17 Piene H. Pulmonary arterial impedance and right ventricular function. Physiol Rev 1986; 66:606-49 18 Cohne IN, Giuha NH, Broder MI, Limas CJ. Right ventricular infarction. Clinical and hemodynamic features. Am J Cardiol 1974; 33:209-14 19 Venus B, Jacobs K. Alterations in regional myocardial blood flows during different levels of positive end-expiratory pressure.
Crit Care Med 1984; 12:96-101 20 Metzler H. Hamodynamik des gesehadigten rechten Herzens unter kontinuierlicher positiver Druckbeatmung. Anaesthesist 1985; 34:72-78. 21 Fewell JE, Abendschein DR, Carlson CJ, Murray JF, Rapaport E. Continuous positive-pressure ventilation decreases right and left ventricular end-diastolic volumes in dog. Circ Res 1980; 46: 125-32 22 BrynjolfI, Kebaek H, Munck 0, Godtfredsen J, Larsen S. Right and left ventricular ejection fraction and left ventricular volume changes at rest and during exercise in normal patients. Eur Heart J 1984; 5:756-61 23 Skarvan K, Scheidegger D. Right ventricular dysfunction after an aortocoronary bypass operation (abstract). 9th Annual Meeting, Society of Cardiovascular Anesthesiologists, 1987 24 Priebe HJ. Regional myocardial ischemia develops during hypertension when coronary artery stenosis is present [abstract]. 9th Annual Meeting, Society of Cardiovascular Anesthesiologists, 1987, 109 25 Rabinovitch MA, Elstein J, Chiu CJ, Rose CE Selective right ventricular dysfunction after coronary bypass grafting. J Thorac Cardiovasc Surg 1983; 86:444-50 26 Fisk RL, Ghaswall D, Guibeau EJ. Asymmetrical myocardial hypothermia during hypothermic cardioplegia. Ann Thorac Surg 1982; 34:318-23 27 Chiu RC, Blundell PE, Scott JH, Cain S. The importance of monitoring intramyocardial temperature during hypothermic myocardial protection. Ann Thorac Surg 1979; 28:317-22 28 Gonzalez AC, Brandon TA, Fortune RL, Casanno SF, Martin M, Benneson L. Acute right ventricular failure is caused by inadequate right ventricular hypothermia. J Thorac Cardiovasc Surg 1985; 89:386-98 29 Gaines WE. Perioperative right heart failure: Treatment. Cardiovasc Clin 1987; 17:231-38 30 Brooks H, Kirk ES, Vokonas PS, Urschel C~ Sonnenblick EH. Performance of the right ventricle under stress: relation to right coronary flow JCHn Invest 1971; 50:2176-81
CHEST I 94 / 3 I SEPTEMBER, 1988
571
Ventilation with positive end-expiratory pressure (PEEP) is often the appropriate therapy for treating patients with impaired pulmonary function after cardiac surgery procedures. Circulatory depression, however, sometimes limits the level of PEEP. This study was conducted to investigate the effects of PEEP ventilation ( + 15 cmH 20) immediately after weaning from cardiopulmonary bypass 1) period of PEEP application and 45 min thereafter; 2) period of PEEP application on right ventricular hemodynamics using a new thermodilution technique for measuring right ventricular ejection fraction (RVEF), right ventricular end-diastolic and end-systolic volumes (RVED~ RVESV). Forty patients undergoing aortocoronary bypass grafting were retrospectively divided into two groups: group 1 (n = 24) in which RVEF was reduced significantly (4~28 percent), and group 2 (n = 16) in which RVEF remained almost unchanged. In patients in group 1, stenosis of the right coronary artery (RCA) was significantly more pronounced
Controlled mechanical ventilation with positive end-expiratory pressure (PEEP) is ubiquitously used in patients with pulmonary failure, although its beneficial influence on the respiratory system is accompanied by detrimental effects on the circulatory system. 1-3 The mechanism by which PEEP ventilation decreases cardiac output (CO) has been the subject of several investigations, but it still is not entirely clear. The decrease in CO is attributed mainly to a decrease in venous return due to elevated intrathoracic pressure." Other studies suggest that this effect is caused by an increase in right ventricular afterload due to an increase in pulmonary impedance," decreased biventricular end-diastolic volume," altered ventricular interdependence by leftward displacement of the ventricular sep tum.F-" or decreased myocardial contractility due to altered myocardial blood How? or a myocardial depressing factor induced by PEEEIO The use of PEEP after cardiopulmonary bypass (CPB) seems reasonable, but its routine application is controversially discussed because of its possible negative *From the Department of Anesthesiology and Intensive Care Medicine (Head: Prof Dr G. Hempelmann), Justus-Liebig-University Giessen, West Germany: tDepartment of Cardiovascular Surgery (Head: Prof Dr FW Hehrlein), Manuscript received November 18; revision accepted February 24. 566
in comparison to the others and was detected to be responsible for the different reaction of RVEF (analysis of co-variance). Application of PEEP immediately after weaning from CPB was followed by an increase in RVESV ( + 4 percent; RVEDV - 1 percent) in group 1, whereas patients of group 2 differed significantly (RVESV -14 percent; RVEDV - 15 percent). Cardiac index was decreased only in group 1 (- 32 percent). During the second period of PEEP application, no further difference could be observed between the groups. We conclude that hemodynamic changes related to PEEP ventilation are minimal in the intact right ventricle. Abnormalities in right ventricular function due to stenosis of the RCA, however, have had marked clinical influence on the circulatory response. Monitoring of right ventricular function seems to be of benefit for cardiac surgery patients in this situation. (Chest
1988; 94:566-71)
effects on circulatory stability in this period. Recent studies have produced evidence that right ventricular function becomes increasingly important in patients undergoing aorto-coronary bypass grafting." Therefore, the aim of this study was focused on right ventricular hemodynamics during PEEP application immediately after weaning from CPB using a new thermodilution method, which allows sequential intraoperative estimation of right ventricular function. METHODS
The investigation included 40 patients undergoing elective aortocoronary bypass grafting. Patients with depressed myocardial function (left ventricular ejection fraction <50 percent) or concomitant pulmonary hypertension (PAP > 15 mm Hg) were excluded from the study: Informed consent was obtained from each patient according to the protocol of the Human Study Committee. Premedication and anesthesia procedures were standardized and comparable for all patients consisting of weight-dependent dosages of fentanyl, midazolam and pancuronium bromide. Controlled mechanical ventilation was performed with a Flo, of O. 5 during the whole investigation period. Cardiopulmonary bypass (CPB) was instituted with membrane oxygenators and a non-pulsatile flow of 2.4 L'min-m-, Myocardial preservation was performed with multidose Bretschneider's cardioplegia solution, and myocardial surface was cooled with ice-cold saline solution. During cross-clamping of the aorta (= ischemia) moderate hypothermia (rectal temperature 32.2°± l.O°C, esophageal temperature 32.8°±O.9°C) was used. Hemodynamic variables measured and derived hemodynamic paPEEP Immediately after Cardiopulmonary Bypass (Boldt at al)
Table I-Measured and Calculated Hemodynamic Variables Mean arterial pressure (MAl) Heart rate (HR) Pulmonary artery pressure (PAP) Pulmonary capillary pressure (PCP) Right atrial pressure (RAP) Systolic right ventricular pressure (RVPsyst) Right ventricular enddiastolic pressure (RVEDP) Cardiac output (CO) Right ventricular ejection fraction (RVEF) Right ventricular enddiastolic volume index (RVEDVI) Right ventricular endsystolic volume index (RVESVI) Pulmonary vascular resistance (PVR) rameters are listed in Table 1. The multilumen balloon-flotation pulmonary artery catheter used in this study was specially designed to measure right ventricular ejection fraction (RVEF). It is mounted with a fast response thermistor (FRT), which is rapid enough to record beat-by-beat the plateaus of the rapid step changes on the descending limb of the thermodilution washout curve. 12,13 This technology allows determination of the residual end-diastolic blood volume (RVEDV) with the help of a bedside microprocessor (REF-I, Edwards Lab, Santa Ana, CA); RVES,V (RVEDV-stroke volume) and RVEF (EDV-ESV/EDV) were calculated, too..Theoretic background and detailed technical features have been discussed elsewhere.P" CO and RVEF were measured in triplicate at the end of the expiration and its mean values were used for statistical analysis. Immediately after weaning from CPB, all patients were ventilated without positive end-expiratory pressure (ZEEP) and the first measurements after CPB were performed.. Then a PEEP of 15 cmH 20 was applied for 10 min and measurements were performed again; ZEEP ventilation was continued thereafter Heparin was then antagonized by protomine and washed erythrocytes (cellsaving system) from the resting volume of the heart lung machine were infused. After chest closing, measurements were performed again while the patients were mechanically ventilated with ZEEE For the next ten min PEEP was instituted with 15 cmH 20 again and hemodynamics were measured as well. Data points could be summarized as follow: 1. before onset of the operation (ZEE~ chest closed), 2. before start of CPB (ZEE~ chest and pericard open), 3. immediately after the end of CPB (ZEE~ chest and pericard open), 4. 10 min after PEEP ventilation with 15 cmH 20 (pericard and chest open), 5. after chest was closed and volume (washed red blood cells from the cell saver) was applied (ZEEP), 6. 10 min after PEEP ventilation with 15 cmH 20 (pericard and chest closed), 7. at the end of the operation (ZEE~ chest closed). Mean values (X) and standard deviation (SD) were calculated for each parameter at each data point; analysis of variance and analysis of co-variance were used for statistical interpretation; p values <0.05 were considered significant. RESULTS
The patients were retrospectively subdivided into two groups according to the change in RVEF after PEEP application immediately after weaning from CPB: group 1 (n = 24), where RVEF decreased, and group 2 (n = 16), where RVEF remained almost unchanged. U sing analysis of co-variance, the degree of
RCA-stenosis was detected to be the decisive factor for the change in RVEF. Analysis of preoperative catheterization data revealed that in patients in group 1, stenosis of the right coronary artery (RCA) was significantly more pronounced (with RCA-stenosis) in comparison to patients in group 2 (without RCAstenosis). Only in patients of group 1, RCA revascularization or coronary end-arterectomy (CEA) was performed. The biometric data were without differences between the groups (Table 2). The duration of CPB, as well as of ischemia was significantly longer in the patients with RCA in comparison to the other group, due to additional revascularization of the RCA in these patients. The amount of volume (washed red blood cells) applied after ECC was standardized (the whole resting volume from the circuit was concentrated) and comparable for both groups (Taqle 3). According to the grouping of patients, application of PEEP immediately after weaning from CPB was followed by a decrease in RVEF only in patients with RCA-stenosis (Fig 1), whereas during the second period of PEEP ventilation, no further difference between the groups could be demonstrated. CO was decreased only in group 1 patients during the first period of PEEP application (Fig 2). RVEDVI decreased significantly in patients in group 2, in patients with RCA-stenosis; however, no significant decrease was seen (Fig 3). RVESVI was slightly increased in this group in contrast to group 2, where RVESVI decreased significantly; rio additional difference between the groups could be observed during the second period of PEEP application (Fig 3). With regard to the other hemodynamic variables, the application of PEEP immediately after weaning from CPB was followed by a significant decrease in MAP and an increase in PVR, RVPsyst and RVEDP only in the group with RCA Table 2-Biometric Data and Data from Surgical Procedure /
Age (years) Weight (kg) Height (em) LVEDP (mm Hg) LVEF (%) RCA-stenosis (%) CPB (min) Ischemia (min) Volume (ml)
Group 1 (n=24)
Group 2 (n=16)
58.2±4.7 78.2±3.3 172±8 13.6±5.2 63.6±7.1 88.8±7.2 133.1±20 88.4± 15 766± 115
60.6±6.9 74.3±2.9 174±9 13.6±5.8 58.6± 11 10.2± 10.2* 103.2± 11* 63.9± 12* 700± 180
CPB = duration of cardiopulmonary bypass; Ischemia = duration of cross-clamping of the aorta; LVEF = left ventricular ejection fraction; LVEDP = left ventricular enddiastolic pressure; Volume = amount of volume given after CPB; group 1 = with right coronary artery (RCA) stenosis; group 2 = without right coronary artery (RCA); stenosis; X± SD; *p
567
3.5
1---1
3.0
c 2.5
P B
2.0
X ±SD • p
0-0
< 0.05
Group 1 (n
e---e Group 2
(n
= 24) = 16)
•
1.5
ZEEP
PEEP
+15 em H 2 O
PEEP
ZEEP
+15 em H2O
FIGURE 1. Change in right ventricular ejection fraction (RVEF). Group 1: with right coronary artery (RCA) stenosis; group 2: without right coronary artery (RCA) stenosis.
attention than the physically more dominant left ventricle. A tendency to overlook the right ventricle as an important part of the circulatory system has been reinforced by some previous studies in which the right ventricle has been considered a nonfunctional, passive conduit for accepting venous blood and transfusing it through the pulmonary system;" Later studies have yielded a more complete picture stressing
stenosis (Table 3). The use of pharmacologic support (epinephrine, dopamine) was greater in patients of group 1 without being statistically significant. None of the patients suffered from sequelae attributable to the study DISCUSSION
In the past, the right ventricle has received less 50
40
IR V E F c P
B
(%)
1~1
1
0-0
30
Group 1
e--e Group 2
=24) (n = 16) (n
i±SD • p< 0,05
_....
•
20 I
I
ZEEP
PEEP
+15 em H20
I
ZEEP
I
PEEP
+15 em H20
FIGURE 2. Changes in cardiac output (CO) in the two groups; group 1: with right coronary artery (RCA) stenosis, group 2: without right coronary artery (RCA) stenosis.
568
PEEPImmediately after Cardiopulmonary Bypass(Boldt at al)
65 60 55 50
I R V E $ V I (ml/m2) I 11
11
'I
L~~
C p
B
e
'E at)
-.::t
45
40
x± SO
~ ~
* p < 0,05
I RVEDVQml/m2j]
90
1 1
11
85 80
75
(n = 24) (n = 16)
Group 1 Group 2
II
c
P B
70 65 u.J..LJ.,j.lJ.J-'-U..ll-----,
I:
----.---_~=_--.-_
ZEEP
PEEP
+15 em H20
ZEEP
-
-~----I-
- --
PEEP
+15 em H2
FIGURE 3. RVEDVI and RVESVI in the two groups during PEEP application; group 1: with right coronary artery (RCA) stenosis; group 2: without right coronary artery (RCA) stenosis.
continuous interplay between the right and left ventricles due to the anatomic relationship of the two sides of the heart. 7,16 The right ventricle constitutes the pump that conveys hydraulic energy to the blood passing from the low-pressure venous reservoir to the
medium-high pressure reservoir of the pulmonary arterial blood and is ensuring delivery of the preload required to subserve left ventricular output. 17 The importance of the right ventricle has been documented recently by Cohne et aP8 who reported severe right ventricular dysfunction and circulatory instability in patients with apparent right ventricular infarction. Although it is reasonable to assume that a decreased venous return due to increased intrathoracic pressure is the primary mechanism for a decrease in CO during PEEP ventilation, recent clinical and experimental studies have suggested that additional factors may also contribute to the decrease in CO. The increase in right ventricular afterload results in an elevated right ventricular stroke work and consequently in a higher right ventricular O~ consumption." An augmented contractile response of the right ventricle is necessary in acute PAP increase requiring an increase in right ventricular coronary blood flow A decrease in myocardial blood flow (MBF) has been elucidated as a contributing factor to the depression of cardiac function during application of PEEB8,I5 Venus et a}19 speculated that high levels of PEEP reduced cardiac output independent of venous return due to a decrease in MBF possibly mediated by reflex stimulation of lung receptors. Cassidy et al'" reported evidence that lung inflation produces a vagally mediated reflex depression of both the right and left ventricular performance. We have chosen PEEP of 15. cmH 20 because Metzler et aPO found that only high levels of PEEP elevating pulmonary vascular resistance limit myocardial performance of the right ventricle resulting in a significant reduction of CO. PEEP was found to be associated with a large decrease in left and right
Table 3-Hemodynamic Parameterswithin Investigation Period Parameter MAP (mmHg) HR (min-i) PAP (mmHg) PCP (mmHg) PVR (dyn-s-cm -5) RAP (mm Hg) RVP syst (mmHg) RVEDP (mmHg)
Group
1 2
1 2 1 2 1 2 1 2 1 2 1 2 1 2
Before Operation
Before ECC
86.9± 10.2 82.1±9.8 72.2± 12.0 78.0± 12.1 15.4±4.1 14.8±3.7 8.4±2.9 6.9±2.1 104±24 120±30 4.0±2.1 3.2±LO 24.8±6.7 26.6±6.0 4.0±1.8 2.8±1.0
82.5±13.2 74.4± 10.0 77.0± 10.2 87.0± 11.1 15.2±3.5 12.9± 1.9 8.3±2.4 6.9±2.1 111±20 130±22 4.6± 1.2 4.2±1.4 27.0±6.1 25.0±6.1 4.3±1.9 3.0±1.0
ECC
ZEEP
PEEP +15
ZEEP
PEEP +15
End of Operation
83.4± 11.2 82.4± 12.4 88.8± 12.0 94.6± 11.2 15.0±2.1 15.2±4.1 8.5±2.1 7.8±4.0 100±14 120± 19 5.0± 1.2 4.2± 1.0 29.2± 10.0 33.6±7.5 4.9±2.0 3.6±1.6
68.5± 12.0* 81.0± 15.0 90.4± 12.1 92.0±6.9 20.5±4.0 21.0±3.6 12.8±3.1 11.8±3.2 184±33* 162±21 8.3± 1.9 7.2±2.0 36.0±5.0* 36.8±3.0 7.6± 1.8* 5.4±2.6
96.8± 12.1 99.2± 14.1 91.0± 10.0 92.0±6.8 18.0±4.2 20.0±6.7 11.0±3.5 11.6±4.0 105± 15 131±22 7.2±1.8 6.2±2.1 31.2±4.3 34.2±6.0 6.7±1.3 5.1± 1.9
92.5± 14.2 93.0± 13.2 92.7± 10.2 92.0±7.6 22.8±3.7 23.9±5.0 15.4±3.6 13.8±4.0 144±30 160±22 10.8± 1.6 10.2±2.9 36.1±4.1 38.0±5.2 9.6±2.1 8.6±2.0
98.8± 10.0 99.0± 12.2 92.0±9.8 95.2±7.6 18.1±3.0 20.4±2.1 10.7±3.1 12.2± 1.0 110± 19 128±21 7.4±3.0 7.0±2.1 30.2±6.0 32.8±6.2 6.9±2.5 6.8±2.1
CPB = cardiopulmonary bypass; group 1 = with right coronary artery (RCA) stenosis; group 2 = without right coronary artery (RCA); stenosis; x±SD; *p<0.05 CHEST / 94 / 3 / SEPTEMBER, 1988
569
ventricular end-diastolic volumes." Right ventricular volume and performance, however, have been difficult to obtain because of the functional anatomy and complex geometry 22 The correlation between the new thermodilution technique used in this study for estimation of RVEF and other methods such as first pass technique or equilibrium gated techniques is significant. 12 Traditionally monitored hemodynamic parameters such as RAp'or RV~ however, have failedto be representative for right ventricular function. RVED~ too, shows considerable individual variations and does not have a close relationship to ejection fraction or clinical evidence of right heart decompensation. 8 In our patients without ~CA stenosis, RVEDVand RVESV were reduced significantly by PEEP ventila- . tion which is in accordance with other studies." In the group with RCA-stenosis, however, right ventricular volume was not decreased significantly thus showing that the right ventricle was insufficient and not able to transport blood adequately through the pulmonary vessels, although blood supply to the right chamber is reduced by PEEP; RVEF was decreased in these patients demonstrating that the right ventricle was unable to make the adaptations required. MAP was Significantly reduced only in the "withRCA-group" and the resulting decrease in right coronary perfusion is contributing to the vicious circle. A critical decrease in right ventricular O 2 supply/demand ratio may have developed and resulted in right ventricular ischemia and further deterioration of its function. In agreement with our results, Skarvan et al23 demonstrated that surgical revascularization of the RCA may frequently be associated with right ventricular. dysfunction. Results from Priebe" indicate that severe right ventricular myocardial dysfunction may develop during moderate pulmonary hypertension only when right coronary artery (RCA) stenosis is present. It is stressed that patients not exhibiting clinical symptoms of coronary insufficiency at rest may develop severe myocardial dysfunction during only mild increases in pulmonary artery pressure. In the normal right ventricle, however, a mean PAP as high as 40 mm Hg may be sustained without reduction in CO. Rabinovitch et al25 concluded from their studies that the right side of the heart should not be neglected to achieve optimal myocardial protection during cardiac operations. High-grade RCA lesions can prevent the cold cardioplegia .solution from reaching the right ventricular myocardium at a sufficient rate.f" Moreover, the right heart is not as well submerged as the left ventricle in the pericardial cold saline solution bath used for supplementary topical cooling due toits ventral location. Therefore, the right ventricle seems to be the most vulnerable aspect of an ischemic 570
heart. 27,28 Therefore, overall right ventricular dysfunction after CPB is not determined by the loading conditions alone. Local myocardial and septal involvement is suspected to be an important determinant of right ventricular function as well. 29 Forty-five min after weaning from CPB, a sufficient reperfusion of the myocardium with an improvement in myocardial O 2 supply may have contributed in our patients to the fact that there was no more difference in right ventricular function between the two groups during the second period of PEEP application, and MAP and CI could be maintained in this situation. On the other hand, volume expansion (eg, by infusion of washed erythrocytes) is thought to be an important mechanism by which CO (and MAP) can be restored when it is reduced as a result of increased right ventricular afterload or depressed contractility " This mechanism, however, is limited because increasing right ventricular volume may hav~ some advers~ effects such as increased wall tension with an augmented myocardial oxygen demand, decreased left ventricular compliance and possible tricuspid regurgitation. It can be concluded that application of PEEP is followed by complex hemodynamic changes. An increase in right ventricular afterload is tolerated by the right ventricle provided there is no factor concomitantly limiting the right ventricular contractility such as a high grade RCA stenosis. The present data suggest that right ventricular dysfunction secondary to ineffective myocardial preservation or 'to reduced blood flow may also result in significant impairment in global cardiac performance when PEEP is applied. Thus, the right ventricle seems to play an important role and might be the limiting factor in weaning from CPB. Precise monitoring ofpulmonary and right ventricular hemodynamics are of greatest importance in this situation. REFERENCES 1 Biondi J~ Schulman DS, Matthay RA, Barash PG. Correlation of left ventricular peak filling rate and right ventricular ejection fraction during positive end-expiratory pressure: the role for ventricular interdependence (abstract). 9th Annual Meeting, Society of Cardiovascular Anesthesiologists, 1987 Holland L, MacGregor D, Bromber2 Robotham JL, Lixfeld ger-Barnea B. The effects of positive end-expiratory pressure on right and left ventricular performance. Am Rev Resp Dis 1980;121:677-83 3 Santamore Bove AA, Heckman JL. Right and left ventricular pressure-volume response to positive end-expiratory pressure. Am J Physiol 1984; 246:Hl14-19 4 Guyton AC. Circulatory physiology: Cardiac output and its regulation. Philadelphia: WB Saunders, 1969:380-89 5 Prewitt RM, Wood LDH. Effect of positive end-expiratory pressure on ventricular function in dogs. Am J Physiol 1979; 236:534-43 6 Viquerat C, Righetti A, Suter :P. Biventricular volumes and functions in patients with adult respiratory distress syndrome
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w:
PEEP Immediately after CardiopUlmonary Bypass (Boldt at al)
ventilated with PEEE Chest 1983; 83:509-14 7 BakerBJ, Franciosa KJA. Effect of the left ventricle on the right ventricle. Cardiovasc Clin 1987; 17:145-55 8 Wiedemann H:p, Matthey RA. Acute right heart failure. Crit Care Clinics 1985; 1:631-61 9 Vlahakes GJ, Turley K, Hoffman JE. The pathophysiology of failure in acute right ventricular hypertension: hemodynamic and biochemical correlations. Circulation 1981; 63:87-95 10 Cassidy SS, Eschenbacher WL, Robertson CH Jr. Cardiovascular effects of positive-pressure ventilation in normal subjects. J Appl Physiol1979; 47:453-61 11 Hines R, Barash E Intraoperative right ventricular dysfunction detected by a right ventricular ejection fraction catheter. J Clin Monitoring 1986; 2:206-08 12 Kay HK, Afshari M, Barash :P, Webler ~ Iskandrian A, Bemis C, et al. Measurement of ejection fraction by thermodilution techniques. J Surg Res 1983; 34:337-46 13 Maruschak GF, Schauble JF. Limitation of thermodilution ejection fraction: Degration of frequency response by catheter mounting of fast response thermistor. Crit Care Med 1986; 13:679-82 14 Matthay RA, Berger H. Noninvasive assessment of right and left ventricular function in acute and in chronic respiratory failure. Crit Care Med 1983; 11:329-37 15 Sibbald WS, Drieger AA. Right ventricular function in acute disease states: Pathophysiologic consideration. Crit Care Med 1983; 11:339-45 16 Weber KT: Janicki JS, Shorff S, Fishman AE Contractile mechanics and interaction of the right and left ventricles. Am J Cardiol1981; 47:686-95 . 17 Piene H. Pulmonary arterial impedance and right ventricular function. Physiol Rev 1986; 66:606-49 18 Cohne IN, Giuha NH, Broder MI, Limas CJ. Right ventricular infarction. Clinical and hemodynamic features. Am J Cardiol 1974; 33:209-14 19 Venus B, Jacobs K. Alterations in regional myocardial blood flows during different levels of positive end-expiratory pressure.
Crit Care Med 1984; 12:96-101 20 Metzler H. Hamodynamik des gesehadigten rechten Herzens unter kontinuierlicher positiver Druckbeatmung. Anaesthesist 1985; 34:72-78. 21 Fewell JE, Abendschein DR, Carlson CJ, Murray JF, Rapaport E. Continuous positive-pressure ventilation decreases right and left ventricular end-diastolic volumes in dog. Circ Res 1980; 46: 125-32 22 BrynjolfI, Kebaek H, Munck 0, Godtfredsen J, Larsen S. Right and left ventricular ejection fraction and left ventricular volume changes at rest and during exercise in normal patients. Eur Heart J 1984; 5:756-61 23 Skarvan K, Scheidegger D. Right ventricular dysfunction after an aortocoronary bypass operation (abstract). 9th Annual Meeting, Society of Cardiovascular Anesthesiologists, 1987 24 Priebe HJ. Regional myocardial ischemia develops during hypertension when coronary artery stenosis is present [abstract]. 9th Annual Meeting, Society of Cardiovascular Anesthesiologists, 1987, 109 25 Rabinovitch MA, Elstein J, Chiu CJ, Rose CE Selective right ventricular dysfunction after coronary bypass grafting. J Thorac Cardiovasc Surg 1983; 86:444-50 26 Fisk RL, Ghaswall D, Guibeau EJ. Asymmetrical myocardial hypothermia during hypothermic cardioplegia. Ann Thorac Surg 1982; 34:318-23 27 Chiu RC, Blundell PE, Scott JH, Cain S. The importance of monitoring intramyocardial temperature during hypothermic myocardial protection. Ann Thorac Surg 1979; 28:317-22 28 Gonzalez AC, Brandon TA, Fortune RL, Casanno SF, Martin M, Benneson L. Acute right ventricular failure is caused by inadequate right ventricular hypothermia. J Thorac Cardiovasc Surg 1985; 89:386-98 29 Gaines WE. Perioperative right heart failure: Treatment. Cardiovasc Clin 1987; 17:231-38 30 Brooks H, Kirk ES, Vokonas PS, Urschel C~ Sonnenblick EH. Performance of the right ventricle under stress: relation to right coronary flow JCHn Invest 1971; 50:2176-81
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