Cardioversion
2009; Lippincott Williams & Wilkins; Volume: 120; Issue: 16 Linguagem: Inglês
10.1161/circulationaha.109.865535
ISSN1524-4539
AutoresIvan Cakulev, Igor R. Efimov, Albert L. Waldo,
Tópico(s)Cardiac pacing and defibrillation studies
ResumoHomeCirculationVol. 120, No. 16Cardioversion Free AccessArticle CommentaryPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessArticle CommentaryPDF/EPUBCardioversionPast, Present, and Future Ivan Cakulev, MD, Igor R. Efimov, PhD and Albert L. Waldo, MD Ivan CakulevIvan Cakulev From the Department of Medicine, Case Western Reserve University/University Hospitals of Cleveland Case Medical Center, Cleveland, Ohio (I.C., A.L.W.); and Department of Biomedical Engineering, Washington University in St Louis, St Louis, Mo (I.R.E.). , Igor R. EfimovIgor R. Efimov From the Department of Medicine, Case Western Reserve University/University Hospitals of Cleveland Case Medical Center, Cleveland, Ohio (I.C., A.L.W.); and Department of Biomedical Engineering, Washington University in St Louis, St Louis, Mo (I.R.E.). and Albert L. WaldoAlbert L. Waldo From the Department of Medicine, Case Western Reserve University/University Hospitals of Cleveland Case Medical Center, Cleveland, Ohio (I.C., A.L.W.); and Department of Biomedical Engineering, Washington University in St Louis, St Louis, Mo (I.R.E.). Originally published20 Oct 2009https://doi.org/10.1161/CIRCULATIONAHA.109.865535Circulation. 2009;120:1623–1632Simplicity is the ultimate sophistication.— —Leonardo da VinciRecent years have seen rapid proliferation of ablative and antiarrhythmic therapies for treating various ventricular and supraventricular arrhythmias. Yet cardioversion and defibrillation remain the main modalities to restore normal sinus rhythm. Their simplicity, reliability, safety, and, most important, their efficacy in promptly restoring normal sinus rhythm are unmatched in our current treatment armamentarium.HistoryThe Early WorkContemporary cardiology has been significantly affected by the ready availability of this simple method for terminating atrial and ventricular tachyarrhythmias. However, fascination with electricity and its use in biological systems is hardly contemporary. The first capacitor that was able to store electric energy in a glass container was discovered in 1745. It was named the Leyden jar, and its use was shortly thereafter tested in the electrocution of small animals. There is a large body of literature in Italy, France, and England on biological and medical application of electricity dating from the 17th and 18th centuries. Although physicians across Europe started using electricity as an experimental treatment, the earliest recorded scientific approach with the use of electric shocks was that of Peter Abildgaard in 1775.1 He systematically shocked hens, delivering electric charges in different parts of their body. Electric stimuli applied anywhere across the body of the hen, particularly in the head, could render the animal lifeless, but subsequent shocks delivered to the chest could revive the heart.Abildgaard was only one of the several scientists who studied the effects of electricity on animals. Some reported similar findings, and others could not reproduce his results. However, Luigi Galvani in 1781 first clearly described the link between electricity and its presence in biological systems.2 He was the first to use the term animal electricity, coined after his famous experiments in which he caused the legs of a skinned frog to kick when touched with a pair of scissors during an electric storm. The recognition of electricity in living organisms sparked intense interest and excitement and led to application of electricity to revive the dead. Possibly the first description of successful resuscitation with the use of electric shock was reported by Charles Kite in 1788, when a 3-year-old girl, a victim of a fall, was shocked through the chest by an electric generator and a Leyden jar by a Mr Squires of London.3 A similar report by Fell appeared in Gentlemen's Magazine in 1792, with the description of this first prototype of a modern defibrillator (Figure 1). Download figureDownload PowerPointFigure 1. An apparatus similar to Charles Kite's, built and successfully used by Fell, as described in the 1792 issue of the Gentleman's Magazine. Courtesy of Mark Gulezian, Takoma Park.In 1792, the British scientist James Curry published a review of resuscitation cases and recommended that "moderate shocks be passed through the chest in different directions in order, if possible, to rouse the heart to act."4 Several other successful attempts at resuscitation led the Royal Humane Society in England to publish a report in 1802 suggesting the application of electric shock to distinguish "real from apparent death" and praising the potential of electric resuscitation.Scientists at that time were unaware that, at least in some cases, revival with electricity was perhaps due to successful termination of ventricular fibrillation (VF). Ludwig and Hoffa were the first to describe this arrhythmia in 1849 when they observed bizarre and chaotic action of the ventricles when exposed directly to electric current.5 The nature of this arrhythmia was subjected to speculation. Neurogenic theory that explained VF as a consequence of abnormal generation and conduction within the neural network was favored. A French neurophysiologist, Edme Vulpian, coined the term fibrillation and first suggested that the heart itself was responsible for originating and sustaining this irregular rhythm that results in mechanical disarray.6In 1889, John McWilliam of Aberdeen, Scotland, was the first to suggest that VF, and not cardiac standstill, was the mechanism of sudden death in humans.7 Previously, he had experimented with mammalian animal hearts and was able to induce VF by applying electricity directly to the heart.8 Two physicians, Jean-Louis Prevost, a former trainee of Vulpian, and Frederic Battelli, worked together at the University of Geneva, Switzerland, on the mechanism of electrically induced VF.9 They confirmed the observations of Ludwig, Vulpian, and McWilliam in 1899 by showing that a small amount of electricity delivered across the chest can induce VF.9 It is fascinating that their secondary observation, mentioned only in a footnote, that larger electric shocks successfully restored normal sinus rhythm stirred little interest until the first defibrillation experiments some 30 years later. Even well-respected figures, giants in the field like Carl Wiggers, who later made significant contributions to the theory of fibrillation and defibrillation, were skeptical of the report of Prevost and Battelli and did not find "their claims worthy of the time, effort or expense."10Work in the First Half of the 20th Century in the WestNevertheless, Prevost and Battelli proposed the so-called incapacitation theory, whereby VF is terminated by complete electromechanical incapacitation of the myocardium established by the electric shock that also stopped and abolished the return of normal electric and mechanical work of the heart. Consequently, direct massage of the heart was suggested to support the circulation until electromechanical function of the heart was restored. This method was perfected by Carl Wiggers10 and used later during the pioneering studies with defibrillation in humans by Claude Beck.11The late 19th and early 20th centuries brought rapid expansion of commercially available electric power. This progress was followed by a growing number of accidents involving electrocution. It soon became apparent that most of the deaths were due to VF. Orthello Langworthy and Donald Hooker, both physicians at Johns Hopkins University, and William Kouwenhoven, an electrical engineer, were funded by the Consolidated Edison Electric Company of New York City to investigate the possible remedies for these frequent accidents. They studied both alternating current (AC) and direct current (DC) shocks and concluded that AC shock was more effective in terminating VF.12 In 1933, the Johns Hopkins group succeeded in terminating VF in a dog when they accidently applied a second shock, hence the term countershock.13 In 1936, Ferris and colleagues, another team composed of engineers and cardiologists, reported the first closed-chest defibrillation in sheep with the use of an AC shock.14All of these experiments culminated with the first reported defibrillation of the exposed human heart performed by Claude Beck (Figure 2), a cardiothoracic surgeon at Western Reserve University/University Hospitals of Cleveland, Ohio, in 1947.11 Beck was aware of Carl Wiggers' work on the mechanisms of fibrillation and defibrillation. Wiggers, also of Western Reserve University, had described the induction of VF through the concept of the vulnerable period.15 He was also a proponent of defibrillation, although he did not believe in transthoracic delivery of electric shocks. These conclusions influenced Beck when he performed the first known defibrillation of VF in humans. He was operating on a 14-year-old boy. During the closure of the wound, the pulse stopped, at which time the wound was reopened, and cardiac massage was performed for the next 45 minutes. An ECG confirmed VF, and seeing no other option, Beck delivered a single shock that failed to defibrillate the VF. After intracardiac administration of procaine hydrochloride, he delivered the second shock that restored sinus rhythm. This success triggered immediate acceptance of defibrillation across the world. Beck's defibrillator used AC directly from the wall socket (Figure 3). He built it together with his friend James Rand III of the RAND Development Corporation. The most significant drawback, however, was that it could be used only to defibrillate exposed hearts. Therefore, for years it was used only in operating rooms. Download figureDownload PowerPointFigure 2. Claude S. Beck, MD. Courtesy of the Dittrick Medical History Center, Case Western Reserve University, Cleveland, Ohio.Download figureDownload PowerPointFigure 3. Beck's defibrillator. Courtesy of the Dittrick Medical History Center, Case Western Reserve University, Cleveland, Ohio.Work in the Soviet UnionConcurrent with the studies in the 1930s and 1940s in the West, a different approach to defibrillation was being developed in the Soviet Union. The latter provided further insight into the mechanisms of defibrillation and paved the way for development of modern defibrillation waveforms and the use of DC shock. The director of the Institute of Physiology at the Second Medical University in Moscow was Professor Lina Stern, who, as a former trainee and then associate of Prevost and Battelli, had studied VF and defibrillation. She assigned a PhD project on the study of arrhythmogenesis and defibrillation to Naum Gurvich (Figure 4), a young physician member of her laboratory. Gurvich later became a key figure and made fundamental discoveries in the fields of fibrillation and defibrillation. In 1939, in their classic work,16,17 Gurvich and Yuniev proposed using a single discharge from a capacitor to defibrillate VF, thus effectively introducing DC shock for defibrillation purposes. Until then, an AC shock was favored and was being developed as the most effective way to defibrillate VF. Parenthetically, in the West, AC shock continued to be used exclusively until the early 1960s. During his doctoral research (1933–1939), Gurvich found that an AC shock at a frequency of 50 to 500 Hz could not be tolerated and, in fact, led to VF. However, he also showed that a single discharge from a capacitor with a DC shock terminated VF. Another advantage of a DC shock was that large amounts of energy could be delivered in a relatively short period of time. In the 1940s, combining his studies with the Wiggers-Wegria model of the vulnerable period, he proposed a completely new concept in the field of defibrillation that was based on using biphasic defibrillation waveforms. Gurvich first reported using rounded biphasic waveforms, produced by a capacitor and inductor, for defibrillation as early as 1939, although at that time he was unaware of the superiority of this waveform over the monophasic waveform. More importantly, these advances allowed Gurvich18 to propose his "excitatory" theory of defibrillation, which suggested that direct excitation of the myocardium prevents further propagation of fibrillatory waves without preventing resumption of normal sinus rhythm. He also introduced the concept of the mother-reentrant circuit as a foundation for the development and sustainability of VF.19 In the United States, MacKay and Leeds in 1953 reported on their first experience with DC shock in dogs.20 Their conclusion was similar to that of Gurvich: They pointed out that DC shock is more efficacious and safer than AC shock, and they also suggested the use of DC shock in humans. All of these reports had opened the way to explore the use of DC or capacitor shocks. In 1952, Gurvich designed the first commercially available transthoracic DC defibrillator (Figure 5) in the world.19,21,22 The application of this device was described in great detail in the Soviet Ministry of Health resuscitation guidelines, published first in 1952.23 The guidelines required every operating room of a major hospital to have a defibrillator. This first DC defibrillator, ID-1-VEI, used a monophasic waveform that, 10 years later, became known as the Lown waveform. Download figureDownload PowerPointFigure 4. Naum L. Gurvich, MD. Courtesy of Margarita Bogushevich, MD.Download figureDownload PowerPointFigure 5. The first DC defibrillator ID-1-VEI for external transthoracic and internal use made in the USSR in 1952. Paddles and cords were stored in the separate metal box, which is leaning on the device. The defibrillator in this picture was given in 1958 to Dr Robert Hosler, an associate of Dr Claude Beck, by Dr Vladimir Negovsky in Moscow during Dr Hosler's visit to Russia. Courtesy of the Dittrick Medical History Center, Case Western Reserve University, Cleveland, Ohio.Following the work of Gurvich in Moscow, another physician-scientist behind the Iron Curtain made the next important defibrillation contribution. In 1957, Bohumil Peleška, from Prague, Czechoslovakia, reported on both direct and transthoracic use of DC shock for defibrillation purposes.24 He constructed his own DC defibrillator, modifying Gurvich's design by including an iron core in the inductor,25 and is credited with improving the procedure of cardioversion by using lower voltage and describing the effects of DC shock. Thus, the original work on biphasic defibrillation waveforms and DC cardioversion and defibrillation had originated initially in the East.It was again in the Soviet Union in February 1959 that Vishnevskii and Tsukerman performed the first reported cardioversion of atrial fibrillation (AF) using a DC shock.26,27 The patient had AF for 3 years, and the restoration of normal sinus rhythm took place during mitral valve surgery. The same team reported the first successful transthoracic cardioversion of atrial arrhythmias in 20 patients using DC cardioversion in 1960.28 In 1970, Gurvich introduced the first biphasic transthoracic defibrillator, which became standard in Soviet medical practice from that time, preceding Western analogs by at least 2 decades.29Of note, as part of "an international trip to further international cooperation in medical research for the good of people," in 1958, the well-known and influential senator Hubert H. Humphrey visited Moscow.30 During that trip, Humphrey visited the Research Laboratory of General Reanimatology (Resuscitation), where he met with its director, Vladimir Negovsky, and the laboratory's leading defibrillation researcher, Naum Gurvich. "There, I saw his successful animal experiments on the reversibility of death, that is, on the revival of 'clinically dead' animals through massive electric shocks. When I returned to our country, I reported publically on his experiments."31 Later, Humphrey urged the development of programs through the National Institutes of Health "on the physiology of death, on resuscitation, and related topics."31 Nevertheless, the work behind the Iron Curtain remained virtually unrecognized in the West. However, as we shall see, the work became known to an electrical engineer working for the American Optical Company, and this had a profound impact on the field.Work in the Western World After 1950In 1956, Paul Zoll of Beth Israel Hospital and Harvard Medical School in Boston, Mass, demonstrated successful closed-chest defibrillation in humans, again using an AC shock.32 Not long after, in 1960, working at Lariboisiere Hospital in Paris, France, an electrical engineer and physician, Fred Zacouto, completed the design of the first external automatic defibrillator/pacer33 (Figure 6). He had invented it in March 1953 and filed the related patent in July 1953 in Paris. His "Bloc Réanimateur" was able to sense a slow pulse from an infrared device attached to different parts of patient's body (ear lobe and a finger) and provide transcutaneous pacing until spontaneous return of heart activity. At the same time, it could detect VF from an ECG and deliver an AC shock of adjustable voltage and duration with the ability to redetect VF and redeliver a shock if needed. It was first used to successfully defibrillate a patient in November 1960. A total of 68 devices were produced and sold by 1968, first by Zacouto's Savita company and later by Thomson-CFTH. The device was used in hospitals in France, Switzerland, and Germany. Download figureDownload PowerPointFigure 6. Bloc Réanimateur, the first automatic external defibrillator/pacer designed by Fred Zacouto, MD. Courtesy of Fred Zacouto, MD.Bernard Lown (Figure 7) of the Peter Bent Brigham Hospital in Boston, Mass, is credited in the Western world with initiating the modern era of cardioversion. He was the first in the West to combine defibrillation and cardioversion with portability and safety. In 1959, in a patient with recurrent bouts of ventricular tachycardia (VT), Lown was the first to transthoracically apply AC shock using the Zoll defibrillator to successfully terminate an arrhythmia other than VF.34 This event is notable because intravenous administration of procainamide had failed to terminate the patient's VT, and application of the transthoracic shock became a dire necessity to try to save a human life.35 Because the procedure was unplanned and on an urgent basis and because there was not any information of which Lown's team was aware to provide data on the safety and efficacy of the procedure, it was done despite the hospital's resistance and only after Lown took sole responsibility.35 Lown later recalled the following: "Never having seen an AC defibrillator, I hadn't the remotest idea how to use one. A host of questions needed prompt answers: Was the shock painful? Was the anesthesia required? Was there an appropriate voltage setting to reverse ventricular tachycardia? If the shock failed, how many additional ones could be delivered? Did the electric discharge traumatize the heart or injure the nervous system? Could it burn the skin? Were there any hazards for bystanders? Was it explosive for the patients receiving oxygen? My head was migrainous from the avalanche of questions."35 At that time, clearly, Lown knew little about defibrillation and the intricacies of AC versus DC shock. Download figureDownload PowerPointFigure 7. Bernard Lown, MD. Courtesy of Lown Cardiovascular Research Foundation.In early 1961, Lown "fortunately, and quite accidentally, met a brilliant young electrical engineer, Baruch [sic] Berkowitz [sic]"35 (Figure 8), who was helping Lown's laboratory with instruments for research projects unrelated to the problem of cardioversion and defibrillation. Barouh Berkovits had been developing a DC defibrillator while working for the American Optical Corporation as the Director of Cardiovascular Research. Although the American Optical Corporation manufactured an AC defibrillator, Berkovits was very aware of its shortcomings because he was familiar with the previous work of Gurvich.36 Thus, aware that DC shock was safer and more effective, Berkovits had decided to build a DC defibrillator for possible commercial use. After the "accidental" meeting of Berkovits with Lown, when they learned of each other's interests, Berkovits asked Lown if he would be interested in testing his device. In April 1961, Lown formally asked Berkovits to study his DC defibrillator in canines and for possible clinical application.37 A series of intense experiments followed that involved testing the efficacy of multiple waveforms and evaluating the safety of DC shock in a very large number of canines. During these experiments, the Lown-Berkovits investigation group, aware of the importance of avoiding the vulnerable period, introduced for the first time the novel concept of synchronizing delivery of the shock with the QRS complex sensed from the ECG. During these studies, they also developed a monophasic waveform, later known as the "Lown waveform," with high efficacy and safety for shock delivery during a rhythm other than VF. These studies culminated with the use of the DC cardioverter-defibrillator in patients. Lown is also credited with coining the term cardioversion for delivery of a synchronized shock during an arrhythmia other than VF. Noting the previous work with DC defibrillation in humans by Gurvich in the Soviet Union and Peleška in Czechoslovakia, as well as the adverse effects of AC shock, in 1962 Lown et al reported their success in terminating VT with a single DC monophasic shock in 9 patients.38 Lown subsequently went on to expand DC cardioversion to successfully convert both atrial and ventricular arrhythmias using the monophasic DC shock.39–41 This success promptly resulted in the acceptance and worldwide spread of DC cardioversion. One result of the success of the DC cardioverter-defibrillator was the development of the modern cardiac care unit, where Lown again played an important role. In 1962, Berkovits patented the DC defibrillator for the American Optical Corporation. Download figureDownload PowerPointFigure 8. Barouh V. Berkovits. Courtesy of the Heart Rhythm Foundation.The impact of this "new technique" was indeed profound. The ability to "reverse death" with a simple shock had dramatically improved in-hospital cardiac arrest outcomes. However, it was widely known that the highest mortality was taking place in the immediate period after an individual suffered a heart attack, mainly outside hospital premises.This problem was boldly addressed by J. Frank Pantridge, who, working together with John Geddes at the Royal Victoria Hospital in Belfast, UK, created the first Mobile Coronary Care Unit, which began operation on January 1, 1966.42 The initial assembly of the defibrillator for this mobile unit, which consisted of 2 car batteries, a static inverter, and an American Optical defibrillator, weighed 70 kg. Any initial skepticism that defibrillation out of the hospital would not be feasible, and may even be detrimental, disappeared when the initial 15-month experience with the "flying squad" was published.43 Aware of the work of Peleška, Pantridge's team made further improvements in the design of the defibrillator. A key stage in the development of the mobile intensive care unit came with the design of a small, portable defibrillator. Using the miniature capacitor developed for the US National Aeronautics and Space Administration, Pantridge, together with John Anderson, a biomedical engineer, developed a 3.2-kg portable defibrillator that became available in 1971.With great passion, Pantridge advocated his approach of making early defibrillation readily available everywhere. His ideas first became widely accepted in the United States. Subsequently, Anderson and Jennifer Adgey, another physician from the Belfast group, were among the first to develop the semiautomatic and automatic portable external defibrillator in the late 1970s and early 1980s. With continued development, the portable defibrillator gradually evolved from exclusive use by physicians and was given to paramedics, then to firemen, and finally to members of the public. The benefits of this approach are more than obvious today.44The Implantable Cardioverter-DefibrillatorAlthough external transthoracic DC cardioversion gained wide acceptance and radically improved patient outcomes, the work on defibrillation did not stop here. Defibrillation from an implantable device was the next major achievement that dramatically changed our approach to treat sudden cardiac death. Michel Mirowski conceived the idea for an implantable cardiac defibrillator while working in Israel. Mirowski trained at Tel Hashomer Hospital in Israel, where his mentor was Harry Heller.45 Heller had developed repetitive bouts of VT that were treated with quinidine or procainamide. However, Mirowski was very aware that, sooner or later, this arrhythmia would take Heller's life. It was the sudden death of his mentor in 1966 and the recognition that sudden arrhythmic death was a major problem without, at that time, a solution that influenced Mirowski to dedicate his career to design and develop the implantable cardiac defibrillator. Mirowski recognized that it would be very difficult to accomplish his goal in Israel. In 1968, he accepted a position at Sinai Hospital of Baltimore, Md, as a director of the Coronary Care Unit, with 50% of his time for research. He arrived there in the summer of 1969, and in November 1969 he began working toward his goal with Morton Mower, a young cardiologist and a vital coinvestigator. Together, they produced and tested in dogs the first prototype of an automatic defibrillator46 (Figure 9). Virtually simultaneously and independently, John Schuder, a PhD in Electrical Engineering and then an Associate Professor of Biophysics and Surgery at the University of Missouri in Columbia, also began work on an implantable defibrillator.47 While contemplating future projects during an American Heart Association meeting in 1969, and having been steeped in "transthoracic defibrillation, knowledge about waveform efficacy, and an appreciation of circuit design and component problems," Schuder later commented, "it was almost immediately apparent that the automatic implantable defibrillator was a doable project. I decided to go home and do it."47 In fact, Schuder was the first to implant and successfully use a cardiac defibrillator in a dog in January 1970.48 He subsequently abandoned his work on the implantable defibrillator, instead concentrating his work on optimization of shocking waveforms. Schuder's continued contributions laid the foundation for the miniature, low-energy, reliable, high-voltage, biphasic waveform, which ultimately made contemporary implantable cardioverter-defibrillator (ICD) therapy possible. Download figureDownload PowerPointFigure 9. Drs Morton Mower (left) and Michel Mirowski (right) with their first prototype of an automatic defibrillator. Courtesy of Ariella Rosengard, MD.The continued path to the first implantable cardiac defibrillator in humans was anything but simple or short. As stated by William Staewen, the Director of the Biomedical Engineering Department at Sinai Hospital of Baltimore, Md, and Morton Mower, "The design had to be virtually unflawed. It had to reliably sense ventricular defibrillation and deliver a high energy electric shock to correct the arrhythmia in less than one minute. This had to be accomplished with a device placed remotely in the hostile environment of the body. It had to function as designed for years and must not, if it would fail for any reason, cause injury to the patient."49 When one considers the technical challenges with the potential for both harmful effects and lack of clinical benefit, it comes as no surprise that many leading medical and engineering authorities, including Lown himself, challenged this novel and original idea.50 Nevertheless, Mirowski and Mower, ultimately working with Dr Stephen Heilman and his small company, Medrad (later, Intec Systems, a subsidiary of Medrad), persevered in their project, overcoming many obstacles, from the enormous to the small. They finally achieved their goal. In February 1980, after 11 years of development, the first internal cardiac defibrillator was implanted in a patient at the Johns Hopkins Hospital in Baltimore by Levi Watkins, the cardiothoracic surgeon, and Philip Reid, the cardiac electrophysiologist. After the third patient implantation, the device also included cardioversion. The cardioversion-defibrillation device obtained Food and Drug Administration approval in 1985. Soon after, antitachycardia pacing was added. The Food and Drug Administration approval ended a century-long era of investigation, description of basic mechanisms of arrhythmias, and attempts at resuscitation of the dead that finally culminated in an implantable device that safely and effectively aborted sudden cardiac death. The ICD device continued to improve and has now been developed to the point that it can be used virtually at any time and in any place to treat ventricular arrhythmias, if needed. The dedication of many individuals and groups has made this possible. Unfortunately, the space limitation for this article prevents us from mentioning all those who have and still are contributing to the developments in this field. Finally, we should note that an implantable atrial defibrillator was also developed,51 but its use is limited by the pain associated with delivered therapy.PresentLittle has changed in the technique of cardioversion since Lown's article in the early 1960s. Progress has been made in reducing the already low associated complication rate and in understanding the factors responsible for success. Successful cardioversion or defibrillation occurs when a shock with sufficient c
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