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Ann Thorac Surg 2003;76:516-521
© 2003 The Society of Thoracic Surgeons

Original article: cardiovascular

Perfusing and ventilating the patient’s lungs during bypass ameliorates the increase in extravascular thermal volume after coronary bypass grafting

Parwis Massoudy, MDa*, Jarowit A. Piotrowski, MDa, Henry C.J.M. van de Wal, MDa, Reiner Giebler, MDb, Günter Marggraf, MDa, Jürgen Peters, MDb, Heinz G. Jakob, MDa

a Klinik für Thorax- und Kardiovaskuläre Chirurgie, Universitätsklinikum Essen, Essen, Germany
b Klinik für Anästhesiologie und Intensivmedizin, Universitätsklinikum Essen, Essen, Germany

Accepted for publication February 14, 2003.

* Address reprint requests to Dr Massoudy, Klinik für Thorax- und Kardiovaskuläre Chirurgie, Universitätsklinikum Essen, Hufelandstr. 55, 45147 Essen, Germany.
e-mail: parwis.massoudy{at}uni-essen.de


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: To test the hypothesis that bilateral extracorporeal circulation (ECC) (Drew technique) ameliorates the increase in extravascular thermal volume (ETV) observed after conventional cardiopulmonary bypass (CPB) in patients undergoing coronary artery bypass grafting.

METHODS: Thirty-four consecutive patients underwent either bilateral ECC (n = 24, additional cannulation of pulmonary artery and left atrium and lungs perfused and ventilated during bypass) or conventional CPB (n = 10, right atrial and aortic cannulation, lungs statically inflated to 4 mbar (0.41 cm H2O) with oxygen, 500 mL/min). Determinations of ETV (thermodye dilution technique) and intraoperative fluid balance were made before surgery, at the end of surgery, and 4 hours thereafter. In addition, interleukin (IL)-8, thromboxane B2 (TxB2), and endothelin (ET)-1 concentrations were measured in the right atrium and pulmonary vein at specified time points.

RESULTS: Comparisons of ETV made at the start of surgery, after aortic declamping, and after termination of ECC, respectively, revealed an increase from 4.8 ± 0.2 mL/kg (mean ± SEM) to 6.7 ± 0.4 mL/kg, and 6.3 ± 0.3 mL/kg with conventional CPB but ETV remained unchanged at 5.2 ± 0.3 mL/kg, 5.1 ± 0.2 mL/kg, and 4.9 ± 0.3 mL/kg with bilateral ECC. Priming volume (1,580 ± 10 mL versus 2,213 ± 77 mL, p < 0.001) and intraoperative fluid balance (+1,955 ± 233 mL versus +2,654 ± 210 mL, p < 0.05) were less with conventional CPB. Concentrations of IL-8, TxB2, and ET-1 were not different between groups.

CONCLUSIONS: Despite a significantly greater prime volume and a more positive intraoperative fluid balance, ETV did not change with bilateral ECC but increased with conventional CPB. Thus, using the patient’s lungs as an oxygenator during bypass mitigates the increase in extravascular pulmonary fluid.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Conventional cardiopulmonary bypass (CPB) for coronary artery bypass grafting (CABG) evokes pulmonary release of inflammatory mediators [1], presumably because of the foreign body surface of the oxygenator [2] with subsequent trapping of activated leukocytes during their pulmonary vascular transit [3]. During CPB the lungs are perfused to only a small extent through bronchial arteries [4] and phasic mechanical lung ventilation is usually stopped. When both lung perfusion and ventilation are maintained during surgery, however, as described by Drew and colleagues in the late 1950s [5], the systemic inflammatory reaction may be considerably less [6]. Furthermore, the pulmonary inflammatory response may also be diminished and interaction between pulmonary endothelium and circulating activated leukocytes is less with the Drew technique [7]. Finally, in infants during CPB, continuous pulmonary perfusion (30 mL/kg/min) with oxygenated blood is associated with an improved postoperative PaO2/FiO2 ratio and higher systemic neutrophil concentrations, suggesting less pulmonary trapping [8]. In the present study, interleukin (IL)-8, endothelin (ET)-1, and thromboxane B2 (TxB2) were chosen to characterize the inflammatory reaction. Interleukin-8 is a pro-inflammatory cytokine that has been attributed a role in the extravasation of circulating leukocytes into the tissues [9]. The lungs have been described to be responsible for the clearance and production of the vasoconstrictive peptide ET-1 [10]. Pulmonary injury during and after CPB has been associated with the production of the prostaglandin TxB2 [11].

If maintenance of pulmonary perfusion and ventilation during extracorporeal circulation (ECC) with the Drew technique is associated with a lesser pulmonary inflammatory response, less disturbances of pulmonary vascular filtration can be predicted.

Accordingly, to test the hypothesis that the increase in extravascular thermal volume (ETV) observed after conventional CPB [12] is ameliorated by using the Drew technique, we measured ETV during CABG in patients undergoing either conventional CPB or bilateral ECC with the Drew technique.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Patients
After approval by the local ethics committee and informed consent, patients were operated on using either bilateral ECC (modified Drew technique, n = 24) or conventional CPB (control, n = 10). All patients received aspirin 100 mg po up until the day before surgery and 500 mg intravenously (IV) after intensive care unit (ICU) admission. The Drew-group patients included 7 women and 17 men and the conventionally operated patients included 10 men. Age averaged 69 ± 2 (SEM) years in the Drew group and 59 ± 3 years in the control group. Exclusion criteria were valve surgery, redo surgery, emergency surgery, combined CABG and carotid endarterectomy, patient age older than 80 years, and left ventricular ejection fraction of less than 0.30. Patients were recruited in a consecutive, nonrandomized fashion with the same three surgeons performing the Drew technique and the conventional technique.

Anesthesia and surgery
Anesthesia was induced with IV sufentanil (1 µg/kg), etomidate (50 µg/kg), and pancuronium (100 µg/kg). After endotracheal intubation, patients were ventilated mechanically with an end-expiratory pressure of 5 cm H2O. Inspired oxygen fraction was 0.5 and end-tidal carbon-dioxide tension at 30 to 35 mm Hg. Anesthesia was maintained with isoflurane (0.6% to 1.0%), discontinuously given sufentanil (0.3 to 0.5 µg/kg), and pancuronium (30 µg/kg). In both groups, lungs were ventilated mechanically with a tidal volume of 8 mL/kg with respiratory rate adjusted to obtain an end-expiratory carbon dioxide tension of 35 to 40 mm Hg. With the conventional and the Drew techniques, a PaO2 of at least 200 mm Hg was the target during bypass. Aprotinin (Trasylol, Bayer, Leverkusen, Germany) was given according to the Hammersmith protocol (total dose 6 million KIU). After systemic heparinization the target activated clotting time was 400 seconds. With a systemic flow of 2.4 L/min/m2 mean arterial pressure was adjusted to 60 mm Hg by repetitive IV phenylephrine hydrochloride (Neo-Synephrine; Bayer, Morristown, NJ) injections, if required. The patient was cooled (32°C) in both groups and 1,500 mL cold Bretschneider cardioplegic solution (Custodiol, Köhler Chemie, Alsbach-Hähnlein, Germany) was infused into the aortic root after cross-clamping. The lowest hematocrit accepted was 18%, with packed red cells transfused, if necessary. In both groups 5,000 IU heparin (Ratiopharm, Ulm, Germany) and 2 million KIU aprotinin were added to the prime. After termination of bypass, blood remaining in the CPB circuit was retransfused.

In patients undergoing the Drew procedure, the left atrium and pulmonary artery were cannulated in addition to right atrium and aorta. For cannulation of the left atrium through the right superior pulmonary vein (only 4 patients had cannulation through the left atrial appendage or atrial roof) 32F or 36F angled cannulas (Stöckert, Munich, Germany) were used. For pulmonary artery cannulation, 20F wire-reinforced straight cannulas (Stöckert) were used. The cardiotomy circuit was open and two reservoirs were filled with lactated Ringer’s solution (1,500 mL), hydroxy-ethyl-starch (10%, 700 mL), mannitol (90 mL), and sodium bicarbonate (50 mL). The right circuit was started first to decompress the heart and to ease cannulation of the left atrium. Lungs were ventilated mechanically throughout bypass with a tidal volume of 8 mL/kg and the respiratory rate was adjusted to obtain an end-expiratory carbon dioxide tension of 35 to 40 mm Hg. Foreign surface area of the ECC circuit in the Drew group was 2.58 m2.

In patients with conventional CPB roller pumps (Stöckert) and a disposable membrane oxygenator (Jostra, Hirrlingen, Germany) were used following priming with 1600 mL (1030 mL lactated Ringer’s solution, 445 mL hydroxy-ethyl-starch, 10%, 90 mL mannitol, and 35 mL sodium bicarbonate). During bypass, a positive end-expiratory pressure of 5 cm H2O was applied using an oxygen flow of 200 mL/min without phasic ventilation. Foreign surface area of the ECC circuit was 3.48 m2 in the conventional group.

Measurements
For pressure measurements, a pulmonary artery catheter (7.5F, Baxter, Irvine, CA) was inserted through the right internal jugular vein through an introducer-sheath (8.5F, Arrow, Reading, MA), in addition to a central venous catheter and two large-bore peripheral IV catheters. Additionally, a 4F fiberoptic–thermistor-tipped catheter was inserted through the femoral artery into the thoracic aorta for measurement of ETV in triplicate by the double indicator technique. A bolus of 12 mL ice-cold indocyanine green (1.25 mg/mL) was injected into the right atrium. For assessment of the aortic dye concentration and temperature time curves and calculation of ETV, a commercial device (Pulsion-COLD system, Pulsion, Munich, Germany) was used, as described elsewhere [13]. The double dilution method calculated two volumes by mean transit time: Intrathoracic thermal volume (ITTV) and intrathoracic blood volume (ITBV), with ETV resulting from ITTV - ITBV. Cardiac output was measured in triplicate by the thermodilution technique using 10-mL boluses of cold normal saline. Heart rate and mean pressures in radial artery, superior caval vein, pulmonary artery, and the pulmonary capillary wedge position were measured by electromanometry relative to barometric pressure and referenced to the midaxillary line. Cardiac index and systemic vascular resistance index were calculated using standard formulas.

Cytokines and peptides
For measurement of cytokine and peptide concentrations, blood was collected into ammonium-heparin-tubes (Sarstedt, Nümbrecht, Germany). After centrifugation, plasma samples were stored frozen at -20°C until assayed. Interleukin-8 concentrations were measured using commercially available, solid phase, amplified-sensitivity immunoenzymometric assays (Biosource, Europe, Nivelles, Belgium) with a minimum detectable concentration of 0.7 pg/mL. Endothelin-1 concentrations were measured using an immunometric assay based on the double-antibody sandwich technique (Cayman, Ann Arbor, MI) with a minimum detectable ET-1 concentration of 1.5 pg/mL. Thromboxane B2 concentrations were determined using a competitive enzyme immunometric assay (Cayman) based on competition between TxB2 and a TxB2–acetylcholinesterase conjugate for a limited number of TxB2-specific rabbit antiserum binding sites with a specificity of 100%. Measurements were performed in both right and left atrial blood before ECC, after aortic declamping, and after termination of ECC, and in right atrial blood 4 hours after ICU admission and on the first postoperative morning.

Statistical analysis
Results are expressed as mean ± SEM. Differences of means between groups and different time points were evaluated using two-way repeated-measures analysis of variance and post hoc Student Newman Keul test using standard software (Sigma-Stat). For differences of means between groups, Student’s t test for paired samples was used. An a priori null hypothesis was rejected with an {alpha}-error p < 0.05.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Extravascular thermal volume increased with conventional CPB, ie, from 4.8 ± 0.2 mL/kg before bypass to 6.7 ± 0.4 mL/kg at the end of surgery (p < 0.001 versus before bypass), and 6.3 ± 0.3 mL/kg at 4 hours after admission to ICU (p < 0.001 versus base line). No such change occurred in the Drew group patients (Fig 1). A significant difference between groups was observed at the end of surgery.



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  		Fig 1. Extravascular thermal volume at three different time points in patients undergoing coronary artery bypass grafting with either conventional bypass ({square}) or the Drew technique ({circ}). Means ± SEM. Numerical values between error bars indicate level of statistical significance between the groups. #p < 0.001 versus respective baseline value. (ICU = intensive care unit.)

 
Hemodynamic data such as cardiac index, mean pulmonary artery pressure, and systemic vascular resistance index are shown in Table 1. Minimum hematocrit during ECC was significantly lower in the Drew group compared with the control group. Resulting from that the amount of blood transfusion was higher in the Drew group (Table 1).


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  		Table 1. Hemodynamic Data of CABG Patients Undergoing Either Conventional Cardiopulmonary Bypass or Bilateral Extracorporeal Circulation Without External Oxygenation (Drew Technique)

 
The concentrations of IL-8, ET-1, and TxB2 are shown in Table 2. Before bypass IL-8 concentrations in the left atrium (LA) exceeded those in the right atrium (RA) in both groups. After aortic declamping less than half the concentrations determined in the RA were measured in the LA. At the end of bypass, IL-8 concentrations in the LA were still less than half the RA concentrations in Drew patients but similar in both atria with conventional bypass. However, the gradient between RA and LA was not significantly different between groups.


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  		Table 2. IL-8, ET-1, and TxB2 Concentrations Determined in RA and LA of 24 Consecutive Drew Patients and 10 Control Patients Undergoing CABG

 
Endothelin-1 concentrations did not change and no difference was noted between RA and LA in either group.

No difference was noted in TxB2 concentrations between the RA and the LA or between groups before bypass. After aortic declamping, however, we measured a significant gradient between RA and LA in the conventional bypass group but not in the bilateral bypass group. TxB2 concentrations increased after institution of ECC in the Drew group but not in the conventional bypass group. In both groups, TxB2 concentrations were significantly lower 4 hours after ICU admission and on the first postoperative day compared with the preoperative and intraoperative concentrations.

The ratio of arterial oxygen partial pressure over inspired oxygen fraction (oxygenation index) was significantly higher after 1 hour of surgery in the Drew group (Fig 2).



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  		Fig 2. Ratio of partial pressure of oxygen over inspired oxygen fraction (oxygenation index) in patients undergoing coronary artery bypass grafting by either conventional bypass ({square}) or the Drew technique ({circ}). Means ± SEM. Numerical value between error bars indicates level of statistical significance between the groups. (ECC = extracorporeal circulation; ICU = intensive care unit.)

 
Other pre-, intra-, and postoperative data are shown in Table 3. Significant differences were noted in priming volume and intraoperative fluid balance between the groups.


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  		Table 3. Characteristics of CABG Patients Undergoing Either Conventional Cardiopulmonary Bypass or Bilateral Extracorporeal Circulation Without External Oxygenation (Drew Technique)

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Extravascular thermal volume increased significantly in patients after conventional CPB and remained increased 4 hours after surgery. In contrast, in the Drew group patients, ETV did not change despite a greater priming volume and a more positive fluid balance. At the same time, during bypass, the Drew group patients also had a better oxygenation index. The differences in ETV and oxygenation index did not appear to influence the clinical course of the patients in this small study. While ETV stayed elevated in control patients, the oxygenation index was not significantly different from that in the Drew group, except shortly after the start of ECC. This lack of difference may have been related to the small numbers in the present study. However, a weak correlation has been described between the measurement of ETV and the oxygenation index [13] and ETV was described as superior to conventional measurements of oxygenation and hemodynamics in the characterization of critically ill patients [14].

When using a similar prime, preoperative ETV averaged 5.4 mL/kg and increased to 6.5 mL/kg 2 hours after ECC in a recent study [12]. This finding is consistent with the ETV increase observed in our conventional bypass group. Extravascular thermal volume was reported to be lower with decreased prime volume and a less positive intraoperative fluid balance [12]. In the present study, an unchanged ETV was observed in the Drew group despite a greater priming volume and a significantly more positive fluid balance than in the conventional group. Thus, intraoperative fluid balance cannot be responsible for maintained ETV in the Drew group. The higher grade of hemodilution is also indicated by significantly lower minimum hematocrit values in the Drew group, with the consequence of a significantly higher rate of blood transfusion.

Extravascular thermal volume partly reflects the consequences of pulmonary vascular filtration and resorption. The inflammatory response to CPB is associated with an increased pulmonary endothelial permeability [15] and characterized by increased concentrations of pro-inflammatory cytokines such as IL-8 [1]. In the present study, the characteristic increase in IL-8 concentration during ECC was observed in both groups, with only minor differences between groups after aortic declamping and on the morning after surgery. Before bypass, after aortic declamping and after termination of ECC a significant gradient of IL-8 concentration was noted in the Drew group, perhaps related to a release before bypass and consumption at the two other time points. The same trend was noted in the control group before bypass and after aortic declamping. Values did not reach statistical significance because of a high standard deviation. In our earlier study, we had not determined IL-8 levels before bypass. During bypass, however, the concentration of IL-8 was always at the least the same in the LA as in the RA. The present findings are surprising and cannot be readily explained. However, taken together, differences in IL-8 concentrations cannot account for differences in ETV between groups.

Thromboxane B2 concentrations in CABG patients have been determined before [16] and have been reported to not change over time in the RA [16]. An increase in TxB2 concentrations during pulmonary transit has been regarded as an indicator of lung injury [16, 17]. In our study, RA concentrations increased after institution of ECC in the Drew group but not with conventional CPB. Furthermore, a positive gradient between RA and LA after declamping of the aorta indicated thromboxane clearance during pulmonary transit with conventional bypass not present in the Drew group. This clearance during pulmonary transit was then present in both groups after termination of ECC. The low TxB2 concentrations after ICU admission and on the first day after surgery in both groups were probably related to the administration of aspirin. Certainly, the better oxygenation index and lesser ETV in the Drew patients cannot be explained by different TxB2 concentrations.

The role of ET-1 in patients undergoing CABG is not well understood. We did not observe changes in ET-1 concentrations in either group. Arterial but not pulmonary artery ET-1 concentrations increased after surgery with CPB [18], suggesting pulmonary release of ET-1. Furthermore, ET-1 concentrations failed to increase in patients undergoing off-pump CABG [18]. In another study, however, no cardiac or pulmonary endothelin release was found in patients undergoing CABG with CPB [19]. Furthermore, while there was a net clearance of endothelin during pulmonary passage before CPB, this disappeared after CPB [19].

Foreign surface area of the ECC circuit was 3.48 m2 in the conventional group and 2.58 m2 in the Drew group. This decreased surface area in the Drew group may have resulted in lesser endothelial cell damage and less cellular sequestration, accompanied by less leukocyte activation [7]. Other potential mechanisms such as a different lung interstitial pressure or enhanced lung lymphatic flow under continuous mechanical ventilation may also be responsible, but these theories remain speculative.

A few limitations of the study deserve mention. One was that the study was nonrandomized. Because the preoperative forced expiratory volume was smaller in the Drew group, this group had sicker patients as far as preoperative lung function. The measurement of ETV as used in this study is discussed controversially in the literature [20]. The slope of the dilation curve is difficult to predict accurately and this lack of precision may alter the measurement of pulmonary intravascular volume, which is necessary in calculating extravascular volume. Thermal transit time is affected by anything that limits uniform flow to all areas of the lungs. Poor tissue perfusion may be caused by edema, intrapulmonary shunting, atelectasis, and other issues. However, measurement of ETV has been found to be more accurate than other hemodynamic or oxygenating measurements to characterize morbidity and prognosis in critically ill patients [14].

In summary, in low risk elective CABG patients, despite a more positive intraoperative fluid balance, the increase in ETV noted after conventional CPB was not observed in patients undergoing bilateral ECC with continuous pulmonary perfusion and ventilation.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
The authors acknowledge the excellent laboratory work by Ms Karin Kaiser and colleagues, as well as the dedicated work of the perfusionists Mr Horst Schmidt, Mr Wolfe Ingo Wiese, Mr Jörg von Manstein, and Mr Markus Deus. The work was supported by the Deutsche Forschungsgemeinschaft (MA 1731/3-2) and by the Medical Faculty, University of Essen (IFORES 107520-0).


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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