The Production of Microemboli by

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1 The Production of Microemboli by Various Blood Oxygenators Jack Kessler, B.A., and Russel H. Patterson, Jr., M.D. A substantial body of evidence has shown that extracorporeal blood oxygenators alter blood in some way that eventually damages the perfused tissue [8, 111. Some authors have suggested that microemboli are responsible, but detecting the presence of microemboli has been difficult [l, 4-7, 121. Recently a detection chamber employing ultrasound has been developed which continuously counts particles in flowing blood which are greater than 50 p [9]. Using this apparatus, a study was made of the relative concentration of microemboli produced by a disc oxygenator, a membrane oxygenator, and two types of disposable bubble oxygenators. The findings are reported here. MATERZALS AND METHODS Austen and Howry [51 showed in a preliminary report that ultrasound might be used to detect particles during cardiopulmonary bypass. The apparatus used in the present experiments is atterned after their suggestions and has been described in detail elsewhere [ B 1. Briefly, the detection system depends upon reflecting pulses of ultrasound at a frequency of 5 megacycles from the interface between a particle and the blood. The system is composed of a detection chamber, a transducer, a sonarscope," and an electronic counter. The detection chamber is constructed from a rod of nylon through which is bored a channel % inch in diameter for blood (Fig. 1). A transducer at one end of the chamber converts radiofrequency pulses generated by the sonarscope into ultrasonic vibrations of short duration which are transmitted down the column of blood. Vibrations that encounter a particle are reflected back to the transducer and relayed for display as echoes on the time base of the oscilloscope. A counter records the echoes from particles as they pass an electronic gate 2 mm. wide which is positioned 8 cm. from the transducer. The crystal in the transducers used in these experiments pulsed 750 times per second and hence could count a maximum of 750 x 60 or 45,000 echoes per minute. The sensitivity of the apparatus has previously been determined by dropping plastic microspheres of known diameter into the saline-filled detection chamber and determining the smallest detectable diameter, which was 50 p for the present From the Department of Surgery, New York Hospital-Cornell Medical Center, 1300 York Avenue, New York, N.Y This work was supported by a research grant from the U.S. Public Health Service (HE-10937). Accepted for publication Oct. 16, Address reprint requests to Dr. Patterson. 'Type SII transducer and UCD Reflectoscope, Sperry Products Division, Automation Industries, Inc., Danbury, Conn. VOL. 9, NO. 3, MARCH,

2 KESSLEK AND PATTERSON t % Stainless steel J!.Transducer To Sonarscope FIG. 1. The ultrasonic detection chamber, which is constructed from a ny!on rod 5 cm. in diameter and 12.3 cm. long. study. The height of the echo on the oscilloscope was found to be proportional to the diameter of the microsphere, which permits the size of an unknown particle to be estimated from the height of its echo. Blood was found to be completely transparent to the ultrasonic beam at all rates of flow, and recirculation experiments showed that the frequency of echoes was directly proportional to the concentration of microspheres in the blood [91. Mongrel dogs weighing 20 to 25 kg. were anesthetized and mechanically ventilated. Appropriate peripheral blood vessels were cannulated for cardiopulmonary bypass and monitoring of blood pressure. An initial dose of 500 USP units of heparin per kilogram of body weight and additional hourly doses of 5,000 units achieved anticoagulation. Priming of the extracorporeal circuit was accomplished with two parts of an electrolyte solution and one part low-molecular-weight dextran. Blood flowed by gravity from the venous cannulas through an ultrasonic detection chamber, traversed one of the pair of oxygenators and a second detection chamber, and was then 222 THE ANNALS OF THORACIC SURGERY

3 Microemboli from Various Oxygenators FIG. 2. The test circuit. returned by a roller pump to a femoral artery (Fig. 2). The flow of blood was thereafter alternated at intervals of 15 minutes between the two oxygenators. The temperature of the perfusate was kept at 38OC. either by heat lamps or by an integral heat exchanger present in one of the oxygenators. The Temptrol. (2110, the Travenolt 5M0311, a silicone-coated 18-inch disc oxygenator, and the Medical Monitors1 membrane oxygenator with two double sacs were compared at a blood flow rate of 2 liters per minute and an oxygen flow rate of 6 liters per minute. The Travenolt 5M0310 and Temptrole QlOO oxygenators, which were designed for blood flows up to 6 liters per minute, were compared at flow rates of 3 liters per minute for blood and 6 and 9 liters per minute for oxygen. The volume of perfusate in the oxygenators was maintained at levels customary during clinical perfusions. In the case of the Temptrol oxygenators this was 1 cm. above the red line. RESULTS Results of the 17 experiments on which this report is based are grouped in Table 1 and expressed as a ratio of the concentration of microemboli produced by the pair of oxygenators under study. The ratio was determined as foilows: Echoes per minute from Oxygenator A Echoes per minute from Oxygenator B Then the ratios from each of several experiments were averaged to construct the table. To provide some quantitative impression of the number of microemboli produced by the oxygenators, the range and mean number of echoes per minute recorded from each after one hour of perfusion are listed in Table 2. As the tables indicate, the pediatric disposable bubble oxygenators produced microemboli in approximately equal concentrations. The mean concentration of particles leaving the Travenol 5M0311 for the first hour was about half that of the Temptrol QllO, but as the perfusion continued, the number of microemboli released from the Travenol gradually increased and finally exceeded the number leaving the Temptrol. Bentley Sales, Inc., Santa Ana, Calif. ttraveno1 Laboratories, Inc., Morton Grove, Ill. $Medical Monitors, Kirkland, Wash.

4 M A cl B TABLE 1. COMPARISON OF MICROEMBOLI CONCENTRATIONS RELEASED BY EACH OF A PAIR OF OXYGENATORS. > 3 Blood Gas Flow Flow (liters/ (liters/ No. of Ratio of Concentration of Particles Pairs of Oxygenators min.) min.) Trials 30 Min. 60 Min. 90 Min. 120 Min. 150 Min. 2 Temptrol QllO o Travenol 5M0311 # Temptrol Q110 s 18-inch disc Travenol 5M inch disc Medical Monitors Membrane 18-inch disc Temptrol QlOO Travenol 5M0310 Temptrol QlOO gaveno1 5M o 1.o At intervals after initiating perfusion, the frequency of echoes in the blood leaving the first oxygenator was divided by the frequency of echoes in the blood leaving the second oxygenator to give a ratio. The ratios from several trials were averaged.

Microemboli from Various Oxygenators TABLE 2. FREQUENCY OF ECHOES IN THE BLOOD LEAVING AN OXYGENATOR AFTER ONE HOUR OF CARDIOPULMONARY BYPASS Oxygenator Blood Flow (liters/min.

5 Microemboli from Various Oxygenators TABLE 2. FREQUENCY OF ECHOES IN THE BLOOD LEAVING AN OXYGENATOR AFTER ONE HOUR OF CARDIOPULMONARY BYPASS Oxygenator Blood Flow (liters/min.) 18-inch disc 2 Membrane 2 Temptrol QllO 2 Travenol5M Travenol5M Temptrol QlOO 3 Travenol5M Temptrol QlOO 3 Gas Flow (liters/min.) No. of Trials Echoes1 Minute Mean (range) 473 (70-2,200) 1,012 (306-1,800) 9,422 (250-26,000) 15,707 (95042,600) 1,175 (200-2,150) 1,425 (450-2,400) 4,600 (810-9,990) 14,083 (5,000-30,000) The 18-inch disc oxygenator released fewer microemboli than any of the other oxygenators. The pediatric bubble oxygenators produced about 80 times the concentration of particles as did the disc oxygenator during the first hour of perfusion, and thereafter the disparity progressively increased until more than 200 times as many particles were recorded leaving the bubble oxygenator. An example of one perfusion in which the Temptrol QllO and the disc oxygenator were compared is shown in Figure 3. During that experiment the Temptrol oxygenator was also tested with the level of blood 6 cm. above the red line and the flow of oxygen reduced to 4 liters per minute, circumstances which past experience has shown substantially reduce the output of microemboli by the oxygenator. Even so, the disc oxygenator released microemboli in %O the concentration of the Temptrol. The Medical Monitors membrane oxygenator generated fewer microemboli than did the bubble oxygenators but still more than the 18-inch disc oxygenator, as Tables 1 and 2 indicate. Much of the difficulty with the membrane oxygenator arose because foaming occurred unless the perfusate displaced all the air in the reservoirs and membrane sacs; however, even when the blood appeared to flow without foaming, the membrane oxygenator released microemboli in higher concentrations than did the disc oxygenator. Of the two adult-sized bubble oxygenators tested, the Temptrol QlOO and the Travenol 5M0310 generated microemboli in approximately equal concentrations when the blood flow was 3 liters per minute and the flow of oxygen was restricted to 6 liters per minute. Under these conditions they performed even better than did their pediatric counterparts; however, augmenting oxygen flow rate to 9 liters per minute increased the concentration of microemboli leaving both oxygenators but especially that leaving the Temptrol QlOO, which thereafter produced microemboli in 2 to 13 times the concentration of the Travenol 5M0310. COMMENT Among the pediatric oxygenators that were tested at a blood flow of 2 liters per minute and a gas flow of 6 liters per minute, the 18-inch disc oxygenator released fewer microemboli than did the bubble and oscillating membrane oxygenators. The performance of each of the bubble oxygenators substantially varied from trial to trial, but overall they generated microemboli in approximately the same concentration. The two adult bubble oxygenators performed equally when the ratio of

6 KESSLER AND PATTERSON loo. ooo c Temptrol Q 110 Level: Low Gas: 6LImin. 10, ooo - c - BLOOD FLOW 2LImin. Temptrol Q 110 Level: High Gas: 4LImin , Time (Hours) FIG. 3. Output of microemboli from an 18-inch disc oxygenator and from a bubble oxygenator with two diflerent oxygen flow rates and blood volumes in the debubbling compartments. 3 oxygen flow to blood flow was 2:1, but the Travenol 5M0310 was superior to the Temptrol QlOO under the conditions of this study when the flow of oxygen was increased to a ratio of 3: 1. The bubble oxygenators produced the fewest microemboli when a large volume of blood was kept in the settling compartment and when the flow of oxygen was reduced. Volume of blood and rate of gas flow did not greatly affect the performance of the disc oxygenator, but a transitory rise in the output of microemboli was observed if rapid filling of the glass cylinder with blood at the beginning of the perfusion produced foaming between the discs. When operated without foaming, the Medical Monitors membrane oxygenator produced microemboli in 6 times the concentration produced by the disc oxygenator, but foaming, which was difficult to avoid, increased the efflux of microemboli to 40 times the concentration leaving the disc oxygenator. 226 THE ANNALS OF THORACIC SURGERY

Microemboli from Various Oxygenators Anderson and Kuchiba [2] reported on changes in platelet count, fibrinogen level, and hemolysis during the recirculation of blood through a large Temptrol

7 Microemboli from Various Oxygenators Anderson and Kuchiba [2] reported on changes in platelet count, fibrinogen level, and hemolysis during the recirculation of blood through a large Temptrol oxygenator, two kinds of Travenol oxygenators, and a 17-inch disc oxygenator, among others. They observed that the disc oxygenator damaged platelets relatively little but caused substantial hemolysis. Their results may seem inconsistent with our observation that the disc oxygenator generated fewer microemboli than did the others, but they recirculated blood at a flow rate of 4 liters per minute, which is twice the rate employed in our study and may well account for some of the apparent discrepancy. Moreover, clumped platelets and fragments of red cells may be responsible for only a minor portion of the microemboli that the ultrasonic apparatus detects. Selman and co-workers [lo] looked for microbubbles in a glass chamber using 30-power magnification during perfusions with three different oxygenators. After the first 10 minutes of recirculation, no bubbles were observed until the flow of blood was increased to 2.5 liters per minute, 35 minutes later. We have never observed a perfusion employing an oxygenator to be free of microemboli, but Selman et al. concluded, as we do, that fewer microbubbles are released from the disc oxygenator than from the Travenol oxygenator. Observations made in the present study and in prior studies allow some speculation about the composition of the microemboli. If the perfusion was stopped by turning off the pump, echoes from the microemboli were outlined clearly on the screen of the oscilloscope. Their amplitude approximated that of plastic microspheres ranging from 50 to 125 p in diameter, and their specific gravity was less than that of the perfusate, for the echoes slowly drifted up through the column of diluted blood. Increasing the pressure within the detection chamber to two atmospheres caused approximately 50% of the emboli to diminish significantly in size. The size of the remaining particles was unchanged. This suggests that roughly half the microemboli were gas bubbles. Oxidation of blood elements cannot account for the majority of the particles, because mixing the perfusate with helium, argon, or nitrogen produced as many particles as mixing with oxygen. More than turbulence was required to produce the microparticles, because carbon dioxide, which is much more soluble than any of the other gases, produced 90% fewer particles than did oxygen at equal rates of flow. Among the parameters that seemed to increase the production of microemboli were an increase in the ratio of gas mixing with blood, a decrease in the volume of blood in the oxygenator, and any agitation of the oxygenator. VOL. 9, NO. 3, MARCH,

KESSLER AND PATTERSON SUMMARY The output of microemboli from a disc oxygenator, a membrane oxygenator, and several disposable bubble oxygenators was studied with an apparatus employing ultrasound

8 KESSLER AND PATTERSON SUMMARY The output of microemboli from a disc oxygenator, a membrane oxygenator, and several disposable bubble oxygenators was studied with an apparatus employing ultrasound which can count up to 45,000 echoes per minute from particles as small as 50 p in diameter. The disc oxygenator generated significantly fewer microemboli than did the membrane oxygenator and far fewer than did two pediatric disposable bubble oxygenators at a blood flow rate of 2 liters per minute and an oxygen flow rate of 6 liters per minute. Adult disposable bubble oxygenators produced microemboli in relatively low concentrations when the rate of blood flow was 3 liters per minute and the rate of oxygen flow was 6 liters per minute. If the rate of oxygen flow was increased to 9 liters per minute, the concentration of microemboli in the efflux from the oxygenators increased 10- fold to 100-fold. REFERENCES 1. Allardyce, D. B., Yoshida, S. H., and Ashmore, P. G. The importance of microembolism in the pathogenesis of organ dysfunction caused by prolonged use of the pump oxygenator. J. Thorac. Cardiouasc. Surg. 52:706, Andersen, M. N., and Kuchiba, K. Blood trauma produced by pump oxygenators. J. Thorac. Cardiouasc. Surg. 57:238, Austen, W. G., and Howry, D. H. Ultrasound to detect bubbles or particulate matter during cardiopulmonary bypass. J. Surg. Res. 5: 283, Evans, E. A., and Wellington, J. S. Emboli associated with cardiopulmonary bypass. J. Thorac. Cardiouasc. Surg. 48:328, Helmsworth, J. A., Gall, E. A., Perrin, E. V., Braley, S. A., Flege, J. B., Jr., Kaplan, S., and Keirle, A. M. Occurrence of emboli during perfusion with an oxygenator pump. Surgery 53:177, Hill, J. D., Aguilar, M. J., Baranco, A,, de Lanerolle, P., and Gerbode, F. Neuropathological manifestations of cardiac surgery. Ann. Thorac. Surg. 7: 409, Lee, W. H., Jr., Krumhaar, D., Fonkalsrud, E. W., Schjeide, 0. A., and Maloney, J. V. Denaturation of plasma proteins as a cause of morbidity and death after intracardiac operations. Surgery 50:29, Lesage, A. M., Tsuchioka, H., Young, W. G., and Sealy, W. C. Pathogenesis of pulmonary damage during extracorporeal perfusion. Arch. Surg. (Chicago) 93: 1002, Patterson, R. H., Jr., and Kessler, J. Microemboli during cardiopulmonary bypass detected by ultrasound. Surg. Gynec. Obstet. 129:505, Selman, M. W., McAlpine, W. A., and Ratan, R. S. The effectiveness of various heart-lung machines in the elimination of microbubbles from the circulation. J. Thorac. Cardiouasc. Surg. 53:613, Veith, F. J., Deysine, M., Nehlsen, S. L., Panossian, A., and Hagstrom, J. W. C. Pulmonary changes common to isolated lung perfusion, venous bypass, and total cardiopulmonary bypass. Surg. Gynec. Obstet. 125: 1047, Wright, E. S., Sarkozy, E., Dobell, A. R. C., and Murphy, D. R. Fat globulemia in extracorporeal circulation. Surgery 53: 500, THE ANNALS OF THORACIC SURGERY

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