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Ann Thorac Surg 1997;63:1333-1339
© 1997 The Society of Thoracic Surgeons

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Original Article: Cardiovascular

Extracorporeal Membrane Oxygenation Using a Centrifugal Pump and a Servo Regulator to Prevent Negative Inlet Pressure

Surgical Department A and Department of Clinical Engineering, the National Hospital, University of Oslo, Oslo; Department of Immunology and Transfusion Medicine, Nordland Central Hospital, Bodø, University of Tromsø, Tromsø; and Department of Immunology and Blood Bank, The Regional Hospital, University of Trondheim, Trondheim, Norway

Accepted for publication November 30, 1996.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
Background. We studied whether negative inlet pressure created by a centrifugal pump during extracorporeal membrane oxygenation damages blood.

Methods. Fresh, whole human blood and primer were circulated through a test circuit, applying an inlet pressure of 0, -50, or -100 mm Hg. Thereafter, hemolysis and kidney function were compared between 6 patients treated before and 14 patients treated after inclusion in our setup of extracorporeal membrane oxygenation with a servo inlet pressure regulator.

Results. In vitro, negative inlet pressure caused substantial hemolysis, leukocyte and platelet destruction, and complement activation. Maximal plasma free hemoglobin concentrations were 199 mg/100 mL before use of the servo inlet pressure regulator and 40 mg/100 mL afterward (p = 0.06), and serum creatinine peaked at 330 and 115 µmol/L, respectively (p = 0.03). The minimal 24-hour diuresis normalized for weight was 4.8 mL/kg before use of the servo inlet pressure regulator and 45.6 mL/kg afterward (p = 0.03). Three of 5 evaluable patients before use of the servo inlet pressure regulator and 1 of 14 patients after inclusion in this setup experienced anuria (p = 0.04).

Conclusions. There were strong indications that reduction of negative pump inlet pressure with the servo regulator prevented hemolysis and kidney damage.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
See also page 1339.

Extracorporeal membrane oxygenation (ECMO) is an established treatment of neonates and pediatric patients with respiratory failure who are unresponsive to conventional therapy. Extracorporeal membrane oxygenation may also be a life-saving last resort in adult cardiorespiratory failure [1, 2]. The survival rate seems to be related to the severity of the patient's disease and to the occurrence of ECMO complications [3], the most frequent of which are bleeding, infections, neurologic and renal complications, and mechanical problems including oxygenator failure [3, 4]. Most pediatric ECMO centers use a roller pump [5], but an increasing number of reports indicate that centrifugal pumps may be equally useful [4–6], without carrying the risk of pump raceway tubing rupture. A disadvantage of centrifugal pumps is their ability to create a high negative pressure on the inlet side [3, 7]. We therefore conducted an in vitro study of the damage to blood by such negative pressure. The findings of marked blood traumatization led to the construction of a servo regulator that minimizes negative pump inlet pressure. We thereafter studied the possible advantages of the servo regulator in clinical ECMO as compared with previous findings in patients treated without the regulator.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
In Vitro Study
A test circuit was set up consisting of a venous reservoir (Medtronic Biomedicus Inc, Eden Prairie, MN), " inflow and outflow tubing, an in-line electromagnetic flow probe (DP39; Biomedicus), a " connector with a Luer lock mounted in the inflow line for pressure registration, and a centrifugal blood pump (PB80; Biomedicus). All blood-contact surfaces were coated with end-point–attached, functionally active heparin (Carmeda, Stockholm, Sweden). The circuit was primed with 500 mL fresh, whole human citrate-phosphate-dextrose–anticoagulated blood from informed, voluntary donors (Red Cross and National Hospital Blood Bank, Oslo, Norway) and 500 mL of Ringer's acetate, resulting in a median hemoglobin (Hgb) concentration of 5.6 mg/100 mL. A pressure of 0 mm Hg (group I, n = 3), or a negative pressure of 50 mm Hg (group II, n = 3) or 100 mm Hg (group III, n = 3) was created using an adjustable constrictor on the tubing near the inlet side of the pump. The inflow pressure between the constrictor and the pump was monitored continuously. The blood-primer mixture was circulated at 4 L/min through the circuits for 72 hours, and test samples were drawn at 0, 6, 24, 48, and 72 hours of recirculation.

	Patient Study

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
At the National Hospital from September 1989 to June 1995, 14 patients were treated with ECMO for respiratory insufficiency according to the fast entry criteria of Gattinoni and associates [8], and 6 patients were placed on ECMO for therapy-resistant cardiac failure. One of the study patients has been described in detail earlier [9]. For 16 patients, a silicone membrane oxygenator was used (Avecor; Aveco Cardiovascular Inc, Plymouth, MN), and the remaining patients had a hollow fiber oxygenator (Maxima, Medtronic, or Univox, Baxter-Bentley, Uden, the Netherlands). A nonocclusive centrifugal pump (BP80 or BP50; Biomedicus) was used in all cases. All parts of the ECMO circuit except the oxygenator were coated with heparin (Carmeda, or Duraflo II; Baxter-Bentley). The first 6 patients (group S-) were treated without regulation of the inflow pressure to the pump. Following the observations from the in vitro study, a servo pressure regulator (Appendix 1) that prevented excessive negative pressures at the pump inlet side was used in the remaining 14 patients (group S+). The ECMO circuit is illustrated in Figure 1. Blood samples were drawn immediately before institution of ECMO and further as needed for treatment. Patient observations, blood test results, and variables pertaining to ECMO were registered prospectively in the treatment data base of the surgical department. For this study, we used pre-ECMO data and registrations from every morning that the patient was receiving ECMO. According to the National Hospital's ethical guidelines, patient consent was not needed because the patients were subjected only to the present standard treatment and were not randomized into treatment groups.

View larger version (25K): [in this window] [in a new window]   Fig 1. . Circuit used for extracorporeal membrane oxygenation in the patient study, with inset showing cannulation.

	Analysis of Samples

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

	Statistics

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
Because of the low number of in vitro observations and the non-normal distribution of many in vivo variables, nonparametric statistics were used [13]. Data are given as median and range.

IN VITRO STUDY.
For all measurements, the baseline determination was compared with the data at 72 hours by the Wilcoxon signed-rank test. With three experiments in each group, only trends toward changes could be detected within each group. Data from the three setups without negative inlet pressure (group I) were compared with the six setups with a negative inlet pressure (groups II and III) by the Mann-Whitney U test. Values of p less than 0.05 were considered significant.

PATIENT STUDY.
Because of the varying treatment time on ECMO, statistical comparisons between the groups with and without the servo regulator were performed on baseline and peak or nadir index values independent of when these were observed in each patient, using the Mann-Whitney U test or Fisher's exact test. The treatment days on which the peak or nadir values were observed were also compared. Because of the large variation in patient weight, the urine output per 24 hours was normalized by dividing by patient weight before comparison. The lowest such normalized 24-hour diuresis is referred to as the "minimal 24-hour diuresis." For some variables, the Pearson correlation coefficient was calculated between pre-ECMO data and maximal concentrations during ECMO.

	Results

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
In Vitro Study
CHANGES BY TIME.
There were no significant changes in Hgb or hematocrit from baseline to conclusion of the experiment (data not shown). There was a significant increase in plasma potassium (p < 0.01, all nine experiments), LDH (p < 0.01, all nine experiments), and plasma free Hgb (p = 0.03, all six experiments with negative inlet pressure) (Fig 2). The platelet counts remained unchanged (p = 0.24), but there was a trend toward an increase in the group with 100 mm Hg negative inlet pressure (p = 0.11, all three experiments) (Fig 3). There was a significant increase in calprotectin (p < 0.01, all nine experiments) (see Fig 2). There was also significant complement activation at both the C3 level and the C5-C9 level of the cascade (p < 0.01, all nine experiments) (Fig 4).

View larger version (29K): [in this window] [in a new window]   Fig 2. . Hemolysis indices during in vitro simulation of extracorporeal membrane oxygenation with negative pump inlet pressure at start of experiment and after 72 hours. (A) Serum potassium (mmol/L). (B) Serum lactate dehydrogenase (U/L). (C) Plasma free hemoglobin (mg/100 mL). (Squares = 0 mm Hg; circles = -50 mm Hg; triangles = -100 mm Hg.)

View larger version (34K): [in this window] [in a new window]   Fig 3. . Platelet and leukocyte destruction during in vitro simulation of extracorporeal membrane oxygenation with negative pump inlet pressure at start of experiment and after 72 hours. (A) Platelet counts (x 109/L). (B) Plasma calprotectin (mg/L). (Squares = 0 mm Hg; circles = -50 mm Hg; triangles = -100 mm Hg.)

View larger version (29K): [in this window] [in a new window]   Fig 4. . Complement activation products during in vitro simulation of extracorporeal membrane oxygenation with negative pump inlet pressure at start of experiment and after 72 hours. (A) C3 activation products (AU/mL). (B) Terminal complement complex (AU/mL). There was not enough material for exact quantitation of terminal complement complex in the samples containing more than 25 AU/mL (upper reference limit). (Squares = 0 mm Hg; circles = -50 mm Hg; triangles = -100 mm Hg.)

Patient Study
The duration of ECMO varied from 1 to 43 days (mean, 12 days). In 1 patient, ECMO was used as a bridge to transplantation. Fourteen patients could be weaned from ECMO. Ten patients left the hospital alive. There have been no late deaths during the follow-up period (range, 1 month to 3 years). Patient characteristics and data on ECMO, outcome, and complications are given in Table 1. There were no significant differences between the groups with respect to sex, age, patient weight (S-: 31 kg; range, 3 to 92 kg; S+: 12 kg; range, 3 to 86 kg; p = 0.61), time on ECMO (S-: 393 hours; range, 88 to 834 hours; S+: 148 hours; range, 19 to 1,012 hours; p = 0.14), fatal outcome (S-: 67%, S+: 43%; p = 0.63), use of venovenous ECMO (6 patients) or venoarterial ECMO (14 patients) (p = 0.21), or type of oxygenator (p = 0.34). There were no significant intergroup differences in the pre-ECMO concentrations of any of the tested indices. One patient in the S- group experienced anuria (defined as a 24-hour diuresis <50 mL) before the start of ECMO, and was omitted from comparisons of creatinine concentrations and diuresis. Her pre-ECMO concentrations of other variables were comparable to those of the remaining patients in her group and were included in the analyses.

	Indices of Hemolysis

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
Serum concentrations of LDH, bilirubin, and plasma Hgb are summarized in Table 2. Concentrations of LDH tended to be higher in the S- group, but the differences were not significant because of the large variation in the data (Fig 5). In the S+ group, the maximal LDH concentrations were significantly correlated with the pre-ECMO concentrations (r = 0.61, p = 0.04). This was not so in the S- group (r = 0.05, p = 0.95). There were no differences in bilirubin concentrations between the treatment groups. However, the maximal bilirubin concentrations were significantly correlated with the pre-ECMO concentrations in the S+ group (r = 0.69, p = 0.02), but not in the S- group (r = 0.23, p = 0.71). Plasma free Hgb concentrations tended to be higher in the S- group (p = 0.06), and the peak in plasma free Hgb occurred significantly later (p = 0.01).

View larger version (25K): [in this window] [in a new window]   Fig 5. . Serum lactate dehydrogenase concentration (U/L, median and range) in patients undergoing extracorporeal membrane oxygenation with or without regulation of negative pump inlet pressure. Points contain information from varying numbers of patients according to duration of treatment. (Servo - = no servo pressure regulator used; Servo + = servo pressure regulator used.)

	Kidney Function

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

View larger version (40K): [in this window] [in a new window]   Fig 6. . (A) Serum creatinine concentration (µmol/L) and (B) minimal 24-hour diuresis (mL) per kilogram body weight in patients undergoing extracorporeal membrane oxygenation with or without regulation of negative pump inlet pressure. Points contain information from varying numbers of patients according to duration of treatment. (Servo - = no servo pressure regulator used; Servo + = servo pressure regulator used.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

	Blood Traumatization by Negative Pressure

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
Centrifugal pumps are reported to give less hemolysis than roller pumps [5, 7, 14, 15]. Even so, they may still inflict pronounced hemolysis, especially when high pump speeds are required [14, 16]. The causes of hemolysis during ECMO with centrifugal pumps are diverse, including mechanical damage due to shear stresses at high blood velocities, clotting in the extracorporeal circuit [17], and a negative pressure at the inlet side [17], which may reach at least -100 mm Hg before depriming of the pump and stopping of blood propulsion [3].

Our in vitro study confirmed that negative pressure on the inlet side of the centrifugal pump caused substantial hemolysis. There was also damage to other elements of blood. The substantial increase in calprotectin found with negative inlet pressure was probably caused by leakage from the cytoplasm of destroyed leukocytes. In the -100–mm Hg group, there was a trend toward increasing platelet numbers over time. We believe that there was fragmentation of the platelets in these sets and that the fragments were counted as small platelets by the automated analyzer. Activated complement leads to shedding of microparticles from platelets [18], but mechanical damage may be equally important.

Both levels of negative inlet pressure were detrimental, but there seemed to be a magnitude-related effect with respect to hemolysis and leukocyte destruction. The threshold for platelet damage seemed to be higher than that for the other cell types. During use of a Biopump in clinical ECMO, a negative inlet pressure of -66 mm Hg has been reported [17]. Thus, the pressures tested in our study were clinically relevant, even though the negative pressure was continuous in the model but may vary in patients receiving ECMO.

	Hemolysis and Kidney Function

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
Kidney dysfunction is a serious problem during ECMO. Using a roller pump, Anderson and associates [1] reported kidney failure in 35% of 40 adults treated with ECMO. Horton and Butt [5] reported that 13% of patients had plasma Hgb of more than 100 mg/100 mL using a Biomedicus pump, compared with 8% of 4,598 patients in the ECMO registry of the Extracorporeal Life Support Organization. Based on our in vitro study, we believe that a reason for the rapidly declining kidney function in our first ECMO patients treated with a centrifugal pump could be hemolysis caused by unregulated negative inlet pressure. After introduction of the servo regulator, the incidence of anuria was significantly reduced, and the mean peak concentration of plasma Hgb was reduced to 40 mg/100 mL, as compared with 199 mg/100 mL in the group without the servo regulator.

Because our study was nonrandomized, included small and nonhomogeneous study groups, and had large variations in the data, the results should be interpreted cautiously. However, no other major changes were made in our ECMO protocol during the study period, and the patients were cared for by the same team of doctors, perfusionists, and nurses.

Our data on hemolysis showed large variations among the patients. This was not surprising given the many causes of hemolysis during ECMO, as outlined earlier. Maximal LDH and bilirubin concentrations were significantly correlated with pre-ECMO concentrations in the patients treated with the servo regulator, but not in the S- patients. One explanation may be that greatly increased hemolysis in the S- group due to negative inlet pressure was added to a slight hemolysis caused by other factors present in all patients during ECMO. Even though the reduction in plasma Hgb in the S+ group was not significant (p = 0.06), a steady state between ongoing hemolysis and elimination was reached significantly earlier than in the S- group (see Table 2).

Despite the nonsignificant differences in plasma Hgb between the treatment groups, the differences in indices of kidney function were striking. Without the servo regulator, there was progressive kidney dysfunction in most patients, whereas kidney function was maintained in all but 1 patient in the S+ group. This may indicate that the kidneys in ECMO patients are especially vulnerable to free plasma Hgb, perhaps because of ischemia. In addition, other effects of the negative pump inlet pressure, such as complement activation or white blood cell activation or destruction, may contribute to renal damage during ECMO.

In conclusion, there were strong indications that the introduction of a servo regulator to reduce negative inlet pressure when using a centrifugal pump during ECMO prevented hemolysis and kidney damage. The servo regulator provided a simple means of pressure regulation, as compared with increasing volume and manipulating the venous cannula to improve venous return [5], without the need of special pumping devices as used by others [19].

	Appendix 1. The Servo Regulator: Technical Description

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
The servo regulator was constructed to intervene with the speed control circuit of the pump if the measured inlet pressure in the fluid line exceeds the preset negative level, by reducing the pump speed and thus decreasing the negative inlet pressure. With negative inlet pressure less than the preset level, the pump speed is increased to the set speed.

The original internal control of the Medtronic Biomedicus pump is a 0 to 10 V direct-current voltage level, V_RPMset, presented to the motor control circuit, proportional to the selected pump speed, RPM_set. The servo regulator interrupts the pump's internal controller line, supplying a new synthesized control signal, V_RPMsynth, based on the indices indicated below. The basic modification of the pump is the inclusion of a relay board and a connector to the servo regulator. This modification was approved by the manufacturer's local dealer. When the servo regulator is switched off or disconnected, the relay card is deactivated. The original controller line to the motor is then intact, and the pump function is restored to the original. The servo regulator is powered by a rechargeable battery system. The servo regulator has a display showing battery status, actual measured pressure, and pressure limit.

The inlet pressure to the pump is measured with an accuracy of +/-1 mm Hg in the range +/-100 mm Hg. The servo regulator acts on the basis of the following indices. The inlet pressure limit (adjustable +/-100 mm Hg) determines when action is started. The RPM_min is a minimum baseline speed to avoid backflow, adjustable in the range of 0% to 100% of the selected pump speed, RPM_set. The rate of rise/rate of fall (ROR/ROF) adjusts the rate of speed increase or decrease when the regulator is active, avoiding abrupt changes of flow that could cause hemodynamic disturbances. The ROR/ROF function activates a linear speed change within the interval RPM_set - RPM_min, with an adjustable time span (in effect a delay) of 2 to 12 seconds.

	Acknowledgments

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
This study was supported by the Norwegian Council on Cardiovascular Disease.

Clinical engineers Trond Strømme and Torbjørn Holt are acknowledged for skillful assistance in building the servo pressure regulator prototype and the modification of the Biopump.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 
Address reprint requests to Dr Videm, Department of Immunology and Blood Bank, The Regional Hospital, N-7006 Trondheim, Norway.

	References

Top Footnotes Abstract Introduction Material and Methods Patient Study Analysis of Samples Statistics Results Indices of Hemolysis Kidney Function Comment Blood Traumatization by Negative... Hemolysis and Kidney Function Appendix 1. The Servo... Acknowledgments References

 

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