The Use of Ultrasonics in
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1 THE ANNALS OF THORACIC SURGERY Journal of The Society of Thoracic Surgeons and the Southern Thoracic Surgical Association VOLUME 8 NUMBER 6 DECEMBER 1969 The Use of Ultrasonics in Determination of Arterial During Open-Heart Surgery the Aeroembolism Merrill P. Spencer, M.D., G. Hugh Lawrence, M.D., George I. Thomas, M.D., and Lester R. Sauvage, M.D. A eroembolism is a serious threat to the patient in all open-heart operations [l]. This is particularly true when the left heart is opened or when there is a septa1 defect. Various maneuvers have been introduced to remove air from the left heart under these circumstances. The most effective have been elective fibrillation of the heart and venting of the left ventricle. Our interest in the overall problem of aeroembolism concerns a method of monitoring for the presence of aeroembolism during operation and of identifying whether microaeroembolism is originating from the bypass unit itself and from what portion of the system. The presence of microaeroemboli has not been studied adequately before because no practical detection method has been available. From the Virginia Mason Research Center, The Virginia Mason Hospital, Children s Orthopedic Hospital, and Providence Hospital, Seattle, Wash. This work was supported by U.S. Public Health Service Grant No. HE Accepted for publication July 21, Address reprint requests to Dr. Spencer, Virginia Mason Research Center, 1000 Seneca Street, Seattle, Wash VOL. 8, NO. 6, DECEMBER,
2 SPENCER ET AL. The potential usefulness of the Doppler ultrasonic flowmeter in detecting arterial aeroembolism during open-heart surgery was suggested to the senior author by research in the hyperbaric laboratory of the Virginia Mason Research Center which showed that this instrument can function as an objective indicator of gas emboli forming in the circulation following decompression from exposure to hyperbaric atmospheres [2]. The decompression bubbles and artificially generated bubbles were detected with comparative ease; hence, we reasoned that studies employing this technique might help to explain postoperative cerebral complications occurring in patients who have undergone openheart surgery and to evaluate various techniques for elimination of any microaeroemboli arising within the extracorporeal unit and from the heart itself. MATERIAL AND METHODS The Doppler ultrasonic sensors of flowing blood and entrained emboli were used with a variety of sensors, as illustrated in Figures 1 and 2.t The sensors were applied in several locations on the blood-flow channels of the extracorporeal circuit and around the aortic arch and major branches in 10 patients of three Seattle cardiac surgery teams. The in-line sensors were placed at various points on the extracorporeal circuit, the special button sensor was attached to the innominate artery, and a transcutaneous detector monitored the blood flowing in the common carotid arteries and jugular veins. The Doppler-shifted signals were recorded along with voice annotations on a two-channel tape recorder and later were replayed at the Data Analysis Laboratory. Data reduction consisted of replaying the Doppler signal from the tape FIG. 1. Button-type Doppler flow and bubble detectors. A single ciystal sensor (right) for attachment with umbilical tape to the innominate artery. A double crystal sensor (left) for transcutaneous monitoring of the carotid arteries or attachment to the glass window of the bubble trap in the extracorporeal circuit. Parks Electronics, Beaverton, Ore. tthese detectors are available from the Virginia Mason Research Center, Bioengineering Department, 1000 Seneca St., Seattle, Wash THE ANNALS OF THORACIC SURGERY
3 Determination of Aeroembolism by Ultsnsonics FIG. 2. In-line bubble detector and flowmeter showing the mounting of crystals on the oiitside of a stainless-steel connector. There was no special problem in transmission of ultrasound through the steel OY through glass, but flexible plastic tubing attenuated the signal to untisab,'e levels. Cu#-type sensors also perform well when applied with acoustical jelly to in-!ine metal or p?astic connectors. recordings through a set of narrow band-pass filters as well as through a frequency-crossing meter while audibly monitoring and viewing oscilloscope tracings for tlie presence of embolization signals. Both disc and bubble oxygenators utilizing whole blood or hemodilution prime were used with a roller pump. The effect of various procedures influencing the numbers of microemboli in the extracorporeal circuit was observed during operation on patients and during experimental bypass in calves. The clinical course of the patients was followed before and after operation to determine the relationship of the embolic signals and the carotid flow signal to the postoperative condition. Electroencephalograms taken before and after operation were available for some patients. RESULTS Gas embolization signals appeared on tlie Doppler ultrasonic signal in the form of whistles, chirps, and snaps, most numerous in the innominate and carotid arteries when the left ventricle began pumping blood, after repair or replacemmt of an aortic or mitral valve (Fig. 3). Because the bypass blood was perfused through a femoral artery, the first blood from the ventricle carrying entrapped gas was distributed preferentially to the vessels of the aortic arch. There was considerable variation among patients concerning the amount of air that resulted from opening the left ventricle or aortic arch or ascending aorta. In all patients on full cardiopulmonary bypass, embolizations in the carotid and innominate arteries occurred sporadically at rates up to 160 bubbles per minute (bpm) in one common carotid artery. Embolizations were usually absent in the innominate and carotid arteries during initial partial bypass when the pump blood was distributed to the lower aorta prior to cardiotomy. The microgas emboli from the extracorporeal circuit originated from two principal sources: (1) blood suctioned from the heart and thorax and introduced into the extracorporeal circuit at the venous-return reservoir upstream of the oxygenator; and (2) blood and fluid added, with splashing, through the airblood interface at the venous-return reservoir. When neither suctioned nor new blood was added to the circuit, emboli in the extracorporeal circuit gradually diminished in frequency until none remained. One passage through tlie patient's VOL. 8, NO. 6, DECEMBER,
4 SPENCER ET AL. FZG. 3. Doppler ultrasonic signals from the button detector on the innominate artery recorded immediately before and 20 minutes after bypass. Zn both the upper and lower records, the upper trace represents the Doppler signal after passing through a frequency-crossing meter. The lower four traces are narrowfrequency slices of the Doppler signal, each of which represents separate flow streams of diflerent velocities, e.g., signals in the 8kHz band arise from blood and bubbles mouing at twice the velocity of those represented by the 4kHz band. circulation was sufficient to clear the blood of all microemboli in the venous return. It was concluded that neither the disc oxygenator nor the roller pumps were significant sources of gas emboli. Bubble counts on the carotid and innominate arteries during total bypass were zero when the extracorporeal blood was clear and increased in direct proportion to those delivered by the pump. There were always fewer bubbles in the carotid artery than in the innominate artery, and fewer in the innominate artery than delivered by the extracorporeal circuit. The ratio of microemboli delivered from the pump to those in an individual artery provided an index of distribution of the perfused blood to the individual arteries. The greatest source of gas emboli was the heart itself. The following cases and findings are described as typical of the range of microembolic and circulatory problems encountered. EXTENSIVE EMBOLIC SHOWERS AFTER AORTIC VALVE REPLACEMENT Very few emboli were noted in a 48-year-old woman during replacement of her mitral valve. Because she had had a previous valvulotomy, manual compres- 492 THE ANNALS OF THORACIC SURGERY
5 Determination of Aeroembolism by Ultrasonics sion of the heart was limited by adhesions. Despite all the usual attempts at removing air from the heart, a large rush of bubbles was noted as the replaced valve was rendered competent by withdrawing a catheter placed through its orifice (Fig. 4). These bubbles continued in gradually diminishing numbers over the next 80 minutes. She recovered without gross clinical central nervous system changes, but with electroencephalographic changes of slowing, as illustrated in Figure 5. ABSENCE OF SYSTEMIC SHOWERS AFTER RIGHT VENTRICULOTOMY A 4-year-old boy was operated on through a right ventriculotomy for tetralogy of Fallot. Bubble embolization in the left carotid artery varied throughout the bypass from 0 to 154 bpm. Upon resumption of the left ventricular ejection, no embolic showers were detected in the carotid artery. The patient did have some difficulty maintaining arterial p02 postoperatively, which suggested pulmonary aeroembolism [3], but recovery was complete without central nervous system or cardiac complications. DIFFERENTIATING POOR CIRCULATION FROM GAS EMBOLIZATION A 54-year-old woman was operated on to replace a mitral valve with a ballvalve prosthesis. Upon the institution of total bypass, carotid arterial sounds diminished markedly; pulsations synchronous with the pump could not be heard. By robing deeper, the Doppler sensor detected chirping bubble signals in what pro E ably was carotid artery flow. Arterial bubble counts vaned from 4 to 70 bpm throughout the bypass procedure, which lasted two hours and 24 minutes. Many showers of bubbles occurred in the region of the carotid artery following defibrillation. This patient lived for six days postoperatively but did not regain consciousness. Postmortem examination revealed extensive thrombosis of arteries FIG. 4. Recording frowz the innominate artery of Doppler traces at the moment of resumption of left ventricular pumping (partial bypass) when the mitral valve is rendered competent by withdrawing the catheter passing from the left atrium to the left ventricle. Massive bubbles, whose signals are superimposed on the pump pulse, are delivered preferentially into the aortic arch and its branches. Traces represent the same signals as in Figure 3. VOL. 8, NO. 6, DECEMBER,
6 SPENCER ET AL. FIG. 5. Preoperative and postoperative electroencephalograms of the same patient. "Slowing" waves indicated by the arrows are consistent with difjuse focal ischemia. and veins, including the cerebral vasculature. There was a moderate narrowing of the takeoff of the left common carotid artery at the aortic arch and a dissecting aneurysm of the arch extending up the left common carotid artery. The lack of pulsatile components to the Doppler carotid artery signal indicated constriction at the aortic arch by the aneurysm. Doppler analysis up and down the carotid artery before death indicated stenosis ending about 6 cm. below the angle of the jaw at about the level of the upper extension of the dissecting aneurysm of the left common carotid artery. These observations indicate that the Doppler technique can differentiate between gas embolization and poor circulation due to reduced carotid flow. COMMENT Evidence that the signals we received actually represent aeroembolism is indirect. In experimental animals, air injected intravenously upstream to a transducer over the jugular vein produces a loud, broad click as it passes under the sensor. In the innominate and pulmonary arteries of animals fitted with Doppler cuffs, chirping and whistling signals are produced after injection of intravenous air. Hydrogen bubbles generated in a column of saline produce chirps as they pass the Doppler detector. The forceful injection of saline into the venous reservoir of the extracorporeal circuit produces immediate downstream clicking signals at the in-line transducer. The sizing of bubbles with the present technique is difficult. The 494 THE ANNALS OF THORACIC SURGERY
7 Determination of Aeroembolism by Ultrasonics smallest bubbles detected probably produce a low-amplitude chirp, while larger bubbles (up to 1 mm.) produce signals of increasing amplitude. The largest gas emboli produce loud clicks of broad-band frequency content and may overload completely the Doppler detector electronics. Clicks are also produced by a detector oriented perpendicularly to the flow stream angulation, which allows a longer duration of the embolus in the ultrasonic beam and converts the clicking signal to a chirp or whistle. Future development of a swept-frequency Doppler could possibly allow sizing of bubbles by depending on the variation of the resonant frequency characteristic of each bubble. The tolerance to gas embolization in the various tissues is unknown, but from our experiences it is clear that overt central nervous system complications may not develop even when thousands of microemboli are accumulatively directed to the cerebral circulation. Since this technique is so sensitive as to detect subclinical embolization, we now have the possibility of alerting surgeons and anesthesiologists to unusual doses of gas emboli during operation. In addition, techniques used to avoid aeroembolism can be evaluated objectively. The elimination of all gas emboli should be our goal. Several approaches may be useful in preventing aeroembolism and reducing its effect. All blood and drugs added to the extracorporeal circuits should be warmed and introduced into the system without splashing. The blood from the venous return of the patient to the extracorporeal circuit, being clear of microemboli, should be channeled directly into the oxygenator. Maximum attention should be given to the intracardiac suction, as this is a major source of microaeroemboli. We have found the intracardiac suction reservoir of the Bentley bubble oxygenator to be the best of several systems that we have tested. The bubble oxygenators are being evaluated; however, it is now clear that the disc oxygenator does not introduce detectable microgas emboli. Granted that preventing bubbles of any size is of primary importance, complete elimination may not be attainable; hence, any bubbles that form should be limited in content to oxygen, carbon dioxide, and water vapor so that they may be eliminated rapidly. Nitrogen content of bubbles is the main concern. If the operative field is flooded with oxygen or carbon dioxide, the entrained gas in the suctioned blood would be expected to be rapidly dissolved when it joins the venousreturn blood from the patient. Present techniques of accomplishing this should be improved. Denitrogenation of patient and extracorporeal blood could be accomplished by ventilating both with 100% oxygen prior to bypass, Consideration should be given to using nonvolatile antsthetic agents. Flushing the chambers thoroughly with carbon dioxide just prior to closure of the ventriculotomy should be evaluated. VOL. 8, NO. 6, DECEMBER,
8 SPENCER ET AL. If open-heart surgery could be performed in an altitude chamber with a 100% oxygen atmosphere, denitrogenation of patient and pump. blood would be accomplished efficiently. Bubbles in suctioned blood would have a zero nitrogen content and would consist primarily of oxygen. Beneficial effects of superoxygenation would be realized, and when the operating room is returned to one atmosphere, any residual gas emboli would be reduced to one-half the previous volume. By corollary, this line of thought also suggests that operating in pressures greater than one atmosphere is not advisable because of expansion of any gas emboli lodged in the vasculature. Hyperbaric compression should be used more frequently when signs of postoperative cerebrovascular complications are present. Though none of the 10 patients in this study who underwent openheart surgery appeared to have overt central nervous system or cardiac symptoms and signs, cardiac surgeons are concerned with otherwise unexplained central nervous system aberrations attributable to gas embolization. Postoperative recovery might have been more rapid if microemboli had not been present. Whether the size and number of bubbles explain these occurrences remains a subject for further investigation. A variety of complications that we vaguely attribute to perfusion may, to a significant degree, be the result of aeroembolization. Damage to blood cells may also result from electrostatic forces incident to microgas emboli. The technique described in this paper for the detection, prevention, and elimination of circulatory microbubbles should be used in all open-heart procedures. SUMMARY Techniques for using the Doppler ultrasonic flowmeter in the detection of microbubbles in the extracorporeal circuit and in the systemic arteries of patients undergoing open-heart surgery are presented. Emboli in the extracorporeal circuit originate from two principal sources: (1) blood suctioned from the heart and thorax and introduced into the extracorporeal circuit; and (2) blood and fluid added with splashing through the air-blood interface of the venous-return reservoir. The greatest source of gas emboli is the heart itself following closure and resumption of the pumping action of the ventricles. The disc oxygenator is not considered a source of bubbles. Defoaming agents in bubble oxygenators and in suction reservoirs do not remove completely the microbubble signals. None of the 10 patients monitored had clinical symptoms of aeroembolism postoperatively, but electroencephalographic changes were demonstrated following one aortic valve replacement procedure. This bubble-detection technique is useful in 496 THE ANNALS OF THORACIC SURGERY
9 Determination of Aeroembolism by Ultrasonics the study and monitoring of patients who have undergone open-heart surgery. Such studies may help to explain postoperative cerebral and cardiac complications and to evaluate various techniques for elimination of gas emboli. ACKNOWLEDGMENTS The authors express their appreciation to Dr. Allan Carson of Providence Hospital for his encouragement and ideas and to other members of the three participating open-heart surgery teams: Dr. Stephen Wood, Dr. Thomas W. Jones, Dr. K. William Edmark, and Dr. Milton Share. For the reading of the electroencephalograms, we are indebted to Dr. Richard Birchfield of the Mason Clinic. This study is dedicated to the late Mrs. Jean Burdett Spencer, who actively encouraged the work that has led to the development of these techniques and the disclosures of the findings in this paper. REFERENCES 1. Javid, H., Tufo, H. M., Najafi, H., Dye, W. S., Hunter, J. A., and Julian, 0. C. Neurologic abnormalities following open heart surgery. Abstract presented at The American Association for Thoracic Surgery, 49th Annual Meeting, March 31-April 2, 1969, San Francisco, Calif. 2. Oyama, Y., and Spencer, M. P. Experimental pulmonary gas embolism. Abstract presented at the 1969 American Physiological Society Conference, Aug , 1969, Davis, Calif. 3. Spencer, M. P., Campbell, S. D., Sealey, J. L., Henry, F. C., and Lindbergh, J. M. Experiments on decompression bubbles in the circulation using ultrasonic and electromagnetic flowmeters. J. Occup. Med. 2:238, VOL. 8, NO. 6, DECEMBER,
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