Sick Sinus Syndrome after Surgery for Congenital Heart Disease By RONALD D. GREENWOOD, M. D., AMNON ROSENTHAL, M.D., LAURENCE J. SLOSS, M.D., MICHAEL LACORTE, M.D., AND ALEXANDER S. NADAS, M.D. SUMMARY The course and prognosis of 16 infants and children with sick sinus syndrome associated with cardiac surgery is reviewed. The dysrhythmia was observed most often after extensive atrial reconstructive surgery in patients with transposition of the great arteries and with atrial septal defect. In 12 (75%) of the patients, sick sinus syndrome was detected in the immediate postoperative period. Tachyarrhythmias and bradyarrhythmias were present in 12 and isolated bradyarrhythmias in four. Temporary pacing was used in two and permanent pacing was required in five. Death in two non-paced patients was attributable to arrhythmias. Postmortem examination in one patient revealed a suture in the sinoatrial node. Careful attention to the anatomy of the sinoatrial node, its artery and the internodal tracts during surgery may prevent the development of sick sinus syndrome. In patients with dysrhythmia, a careful search should be undertaken to document the abnormal rhythm with the use of Holter monitoring. The insertion of a pacemaker is indicated in patients with tachyarrhythmias requiring cardioversion or antiarrhythmic drug -therapy and those without adequate lower escape mechanisms.
THE TERM SICK SINUS SYNDROME (SSS)
from January 1960 through June 1974 for patients with SSS. Sixteen patients developed SSS following cardiac surgery and form the basis of this report; four children with SSS, not related to cardiac surgery, were excluded. During this period, approximately 40 patients underwent a Mustard operation, 450 underwent tetralogy repair and 500 underwent closure of an atrial septal defect. To determine the true incidence of the dysrhythmia, the records of 102 randomly selected patients undergoing tetralogy of Fallot repair (1962-1972) and 35 consecutive patients representing all patients undergoing the Mustard operation from September 1972 through June 1974 were reviewed. The patients reported were on continuous electrocardiographic monitors for the first few days postoperatively and for longer periods if dysrhythmias were present. Standard 12 lead electrocardiograms were obtained in the first postoperative day, prior to discharge, and within one year after surgery. Frequent rhythm strips were taken throughout the hospitalization and on follow-up visits. A Holter monitor was employed in six of 16 patients during the recovery period and after discharge in 11 of 16. Each patient was monitored during sleep and waking periods.
was first used by Lown' to describe failure of the sinus node to assume control following cardioversion of chronic atrial fibrillation. In recent years, the term SSS has been used to describe a clinical entity which includes various disturbances in sinus or atrial rhythm. It is often used interchangeably with the term tachycardia-bradycardia syndrome.2`5 The SSS, a potentially fatal arrhythmia, has been attributed in adults3' 4 to pathologic changes in the sinus node, atria, and atrioventricular junction due to coronary artery disease, cardiomyopathy, hypertensive heart disease or to unknown etiology. The syndrome has been recognized with increasing frequency following surgical repair in children with congenital heart disease. This study describes our experience with SSS following cardiac surgery at The Children's Hospital Medical Center. Methods
Definition
The files in the Medical Records Department and the Departments of Cardiology and Cardiovascular Surgery at The Children's Hospital Medical Center were searched
SSS was defined as the occurrence of sinus bradyeardia (a sustained rate of less than 50 per minute for patients five years of age or older and less than 55 per minute for younger children), with or without arrest or exit block, associated paroxysmal atrial fibrillation, flutter, tachycardia or the presence of symptoms. Junctional rhythm (defined as less than the slowest normal sinus rate for that age) without documented sinus bradyeardia, sinus arrest or exit block, was not considered to represent SSS unless the arrhythmia persisted or recurred frequently after discharge from the hospital. Patients with accelerated junctional rhythm or tachyarrhythmias without bradyarrhythmias, or with chemical or toxic etiology for the dysrhythmia (e.g., hypokalemia, digitalis toxicity) were not included. Also ex-
From the Department of Cardiology, The Children's Hospital Medical Center and the Department of Pediatrics, Harvard Medical School, Boston, Massachusetts. Supported in part by Training Grant HL05855, Program Project HL10436 from the National Institutes of Health, and a grant-in-aid from the American Heart Association. Address for reprints: Ronald D. Greenwood, M.D. The Children's Hospital Medical Center, 300 Longwood Avenue, Boston, Massachusetts 02115. Received January 17, 1975; revision accepted for publication March 12, 1975.
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Table 1 Postoperative Rhythm in 35 Consecutive Mustard Operations
Normal sinus rhythm Minor rhythm abnormalities Abnormal P wave Coronary sinus rhythm
No. of patients
Percent
8 6
23% 17%
6 9 7 8
17% 26%
(4 (2)
Junctional rhythm Accelerated junctional rhythm Supraventricular tachyeardia Conduction abnormalities 10 Atrioventricular block Right bundle branch block Trifascicular block Complete heart block Transient atrioventricular dissociation Sick sinus syndrome
(1) '3) (1) (1) (2)
a
20%
23%C
14%
eluded were patients with bradyeardia associated with ventilatory problems, transient dysrhythmias following cardioversion, patients whose only abnormality was sinus bradyeardia or junctional rhythm for short periods and patients with junctional rhythm associated with transient or permanent complete heart block. By adherence to these criteria, a number of patients with less severe probable SSS were omitted. Results Occurrence
SSS occurred in five of 35 (14%) patients with Dtransposition of the great arteries undergoing consecutive Mustard operations (table 1) and in none of 102 randomly selected patients following repair of tetralogy of Fallot (table 2). SSS developed after surgery in 16 patients ranging in age, at the time of diagnosis, from 11 months to 22 Table 2 Postoperative Rhythm in 87 Survivors of 102 Patients Undergoing Intracardiac Repair for Tetralogy of Fallot Postoperative rhythm
Normal sinus rhythm Conduction disturbance Right bundle branch block Right bundle branch block and left anterior hemiblock Left anterior hemiblock Complete heart block 10 Atrioventricular block Ventricular dysrhythmias Premature ventricular contractions Ventricular tachycardia Atrial dysrhythmias Coronary sinus rhythm Paroxysmal atrial tachycardia Atrial flutter Junctional tachycardia Junctional escape rhythm
Sinuts bradycardia
Sick sinus syndrome
No. of patients
Percent
6
70 8
80 9
1 3 10
1 3 11
8 3
9 3
1 1 2 2 1 3 0
1 1 2 2 1
3 0
years (table 3). It followed the Mustard operation in five patients (31%), atrial septal defect closure in six (38%), tetralogy of Fallot repair in four (25%), and aortic valve replacement following ventricular septal defect closure in one (6%). The atrial septal defect was of the sinus venosus type and associated with partial anomalous pulmonary venous return in two patients (cases 8, 15), of the secundum variety in three patients (cases 3, 13, 16) and a common atrium in one (case 6). Three of the five patients undergoing Mustard operation had a previous surgical atrial septectomy. Surgical Technique
Surgery was performed in all patients utilizing cardiopulmonary bypass with additional hypothermia employed in two (cases 2, 7). Superior vena caval cannulation was performed in all and an atriotomy was performed in 13/16. All operations resulted in hemodynamically satisfactory repair except in patient 4 who has a persistent ventricular septal defect. Clinical Description
In 12 of 16 patients (75%), including all those with transposition, the arrhythmia occurred immediately after the operative procedure and in the remaining four (25%) two to 48 months after surgery. Delayed onset of arrhythmia was noted in three of four patients with tetralogy and one with atrial septal defect. Tachy-bradyarrhythmias were present in 12 patients and bradyarrhythmias alone in four. Among the former, the tachyarrhythmias noted were atrial flutter (7), atrial fibrillation (2) and supraventricular tachycardias (8). The bradyarrhythmias in this group included sinus arrest (4), sinus bradyeardia (10), asystole (1), nodal escape rhythm (12), sinoatrial block (2) and predominant ventricular escapes in one. The patients with isolated bradyarrhythmias exhibited sinus bradyeardia (three patients), sinus arrest (two patients) and nodal escape (three patients). Associated conduction abnormalities observed included right bundle branch block in three (patients 1, 3, 5), trifascicular block in two (patients 4, 13) and trifascicular block with transient complete heart block in one (patient 10). Dynamic electrocardiogram recorded via Holter 12-24 hour monitors was extremely helpful in defining the type and severity of the arrhythmia (table 4). Periods of sinus arrest made after initial diagnosis (e.g., patients 2, 12) were helpful in determining treatment. Therapy
Pharmacologrc treatment employed was quinidine in seven patients (cases 1, 3, 4, 5, 9, 14, 16), isuprel in two patients (cases 13, 15) and digitalis in 13 patients (cases 1-9 and 11, 12, 14, 16), seven of whom received the latter drug primarily for congestive heart failure.
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Table 3 Clinical Presentation and Course of Patients Developing Sick Sinus Syndrome after Surgery
Patient
1 2
3 4 5 6
7 8 9 10 11 12
13
14
15 16
Cardiac diagnosis
Surgery (age yr)
Postop time of diagnosis of SSS
Major rhythms at time of diagnosis
Total repair (7); residual Immediately FL, SVT, SB, SA, CA, JR ventricular septal defect closure (20) Immediately JR, SB Atrial septal defect D-transposition of the great arteries creation (5d); Mustard (11/12) FL, FI, SB, JR 13o mos Pulmonary stenosis; Total repair (6) atrial septal defect, secundum FL, AT, SB, JR 48 mos Tetralogy of Fallot Total repair (18) 2 mos FL, SA, SB, JR Tetralogy of Fallot Total repair (6) Immediately SVT, JR, SB, SA Atrial septal defect, Common atrium repair (20) common atrium, endocardial cushion defect D-transposition of Immediately SB, JR, SA Mustard (1) the great arteries Atrial septal defect, Total repair (1 4/12) Immediately SAB, AT, JR sinus veniosus Atrial septal defect Immediately FI, FL, JR, SB D-transposition of creation (3 wk); the great arteries Mustard (4 4/12) SB 9 mos Tetralogy of Fallot Total repair (7 8/12) Immediately SVT, JR D-transposition of Atrial septal defect creation (4 d); the great arteries MViustard (2) Immediately SB, JR, Vent Ex, D-transposition of Mustard palliative SVT the great arteries (10 5/12) Atrial septal defect, Total repair (7 8/12) Immediately SB, SA, JR, SVT secundum; ventricular septal defect Ventricular septal Ventricular septal Immediately SAB, SB, JR, FL, defect-total repair (8); PAT defect; aortic regurgitation aortic valve replacement (14) Atrial septal defect, Total repair (5) Immediately SA, JR sinus venosus Immediately FL, SB, JR Atrial septal defect, Total repair (5%12) secundum Tetralogy of Fallot
Pacemaker
Outcome Alive (A) Time after or diagnosis dead (D) of SS (yr)
Permanent
A
1 5/12
Temporary
A
10/12
0
A
2 7/12
Permarnent, 0 0
A 1) D
2 2/12 2 7/12 6 davs
0
A
3/12
0
A
3/12
Permanent
A
1 4/12
Permanent 0
A A
8 3/12 1 4/12
Permanent
A
2,/12
Temporary
A
10/12
0
A
5 7/12
0
A
1 1/12
0
A
11 9/12
Abbreviations: SSS = sick sinus syndrome; Postop = postoperative period; FT = fibrillation (atrial); FL = flutter (atrial); SVT = supraventricular tachycardia; SB - sinus bradyeardia. SA = sinus arrest; CA = cardiac arrest; JR = junctional rhythm; AT = atrial tachycardia; SAB = sinus block; Vent Ex = ventricular escape beats.
Cardioversion was employed in eight patients (cases 1, 3, 4, 6, 8, 9, 14, 16) to terminate tachyarrhythmias. Permanent epicardial pacemakers were placed in five patients, for cardiac arrest in one (patient 1), inadequate escape rhythm with extremely slow ventricular rate in two (patients 9, 12, one of whom - patient 9 - exhibited syncopal episodes with a rate of 18/min), and trifascicular block in two (patients 4, 10, one of whom - patient 4 - exhibited syncope). A temporary pacemaker was employed in two additional patients (cases 2, 13) because of an inadequate rate and was maintained in the latter patient for one month. Patient 6 developed syncope and hypotension and died before a pacemaker could be placed.
Follow-up
Fourteen of the 16 patients are alive and have been followed from two months to 12 years after the onset of SSS. The predominant rhythm in these patients, when last seen, was normal sinus rhythm in two (patients 8, 14), sinus bradyeardia in one (patient 13), sinus rhythm with sinus arrest and junctional escape in one (patient 2), junctional with wandering pacemaker in one (patient 15), junctional in three (patients 7, 11, 16), atrial flutter with block in one (patient 3) and paced in five (patients 1, 4, 9, 10, 12). Two of 16 patients (cases 5, 6) died with arrhythmias six days and 2 7/12 years after documented onset of SSS. Postmortem studies were Circulation, Volume 52, August 1975
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Table 4 Holter Monitoring of Patients with Sick Sinus Syndrome Patient
1 2
3 7 8 11 12
13
14 15
16
Time postoperatively
1 mo 1 wk 10/12 3 9/12 10 dy 3 mo 5 dy 12 dy 2 h' mo 13 mo 17 dv 20 dy 22 dy 23 dy 14 dy 28 dy 10 mo
Hours of
monitoring 12
12 12 24 12
yr yr
12 12 12
12 12 24 24 24 24 12 12 12
5 yr 2 dy 8 mo 11 9,/12 vr
12 12 24 12
Findings
JR, SA, atrial bigeminy JR, NSR SA, JR, WAP, NSR FL, varying block NSR, JR JR 2:1 SA exit block, SA FL, varying block NSR JR, SVT JR JR, 4.5 Sec. SA SA, multiple, 2.4 sec. Multiple SA SA, then paced NSR SB, nonconducted atrial bigeminy SA 1.2 see.. vent. esc. SA WAP, JR WAP
Abbreviations: JR = junctional rhythm; SA - sinus arrest; NSR = normal sinus rhythm; WAP = watidering atrial pacemaker; FL = flutter (atrial); SVT = supraventricular tachycardia; SB sinus bradyeardia; vent. esc. = ventricular escape beats. =
performed in both. In case 5, the tetralogy of Fallot was well repaired but a surgical suture had been placed in the area of the sinoatrial node. In case 6, the repair of the common at$$ium was accomplished by construction of a dacron baffle diverting blood from the right superior vena cava, hepatic veins and left superior vena cava to the right side of the heart and from the widely separated pulmonary veins to the left side of the heart. The baffle was large and produced some obstruction of the mitral valve. Discussion Incidence
SSS is characterized by the occurrence of marked sinus bradyeardia or arrest or sinoatrial exit block with or without an escape rhythm (junction or ventricular) or atrial tachyarrhythmias (fibrillation, flutter, tachycardia). Symptoms and complications associated with dysrhythmias vary greatly. Although not termed SSS, identical dysrhythmias have been previously described following cardiac surgery. Sinus bradyeardia, sinoatrial block or arrest, escape rhythms or tachyarrhythmias have been noted following the Mustard operation,6 -13 Blalock-Hanlon procedure,7' 14 Senning operation,7 atrial septal defect repair" and less commonly in ventricular septal defect repair,'7' 21, 22 tetralogy of Fallot repair'5' 21, 23 and other cardiac operations.'5' 24
Atrial surgery, the Mustard operation in particular, highest incidence of dysrhythmias. In one series, only three of 60 patients surviving Mustard operation have remained free of dysrhythmias.f A significant number of these exhibited passive dysrhythmias including sinoatrial is associated with the
block, wandering pacemaker, junctional rhythm
or
atrioventricular dissociation. Tachyarrhythmias (supraventricular tachycardia and atrial flutter) were also present. It is not clear whether these conditions coexisted in some patients with bradyarrhythmias. One patient with junctional rhythm and recurrent atrial flutter died after surgery. Among our patients undergoing the Mustard procedure only eight of 35 (22%) were free of any dysrhythmia and five (14%) exhibited classical SSS (table 1). Among a randomly selected group of survivors after repair for tetralogy at our institution, none exhibited SSS (table 2). Atrial septal defects of the sinus venosus variety represent a small proportion of all patients with atrial septal defects and the interatrial communication is usually small. However, the location of the defect allows a high incidence of sinus dysfunction.25 Pathology and Mechanism
Pathologic changes of the sinus node, atria and atrioventricular junction have been noted in adults with S5.5 Injury to these structures at surgery may produce SSS and an inadequate escape rhythm. In patients developing SSS after cardiac surgery, the dysrhythmia may be related to injury to or around the sinus node, the sinoatrial nodal artery or the internodal atrial tracts. Pathologic studies of patients with postoperative dysrhythmias have shown abnormalities in the sinoatrial node and sinoatrial nodal artery.6 7 In addition, clinical and pathologic studies have shown that damage to the internodal pathways during a Mustard, Senning or Blalock-Hanlon operation is associated with rhythm disturbances, usually junctional rhythm.7 The mechanisms of the bradycardia may be a disorder of impulse generation in the sinus node or disordered conduction from the sinus node.3' 4 In addition, in patients with inadequate escape rhythm in response to the sinus bradyeardia or arrest episodes, we may presume that there are abnormalities in automaticity of the atrioventricular junction. The paradox of rapid ventricular response to the tachyarrhythmias yet inadequate escape rhythm is explained by the observation that atrioventricular conduction and automaticity are related to different portions of the atrioventricular junctional tissues.5 Prevention
Modifications of the Mustard procedure by using the right atrial appendage rather than superior vena cava for cannulation, making the atriotomy anterior to
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GREENWOOD ET AL.
the sulcus terminalis and fixation of the intra-atrial baffle away from the superior vena cava have been suggested as preventive measures in avoiding dysrhythmias.6 Modification in repair of sinus venosus atrial septal defect might include swinging of the superior margin of the patch posteriorly into the left atrium instead of anchoring it to the cristt terminalis. In all operations involving cardiopulmonary bypass, anchoring sutures to cannulae in the superior vena cava or placement of sump suckers may produce injury to the sinoatrial node or its artery and result in SSS. Confining the atriotomy, if possible, to the trabeculated portion of the right atrium and avoidance of the crista terminalis and other conduction tissues may result in fewer dysrhythmias. Awareness of the variation in origin of the sinoatrial nodal artery26 should lead to its avoidance at surgery and may also reduce the incidence of damage to the node. We have not noted this syndrome in any patients operated under inflow occlusion. Diagnosis
The Holter monitor provides an excellent tool for evaluating patients suspected of having SSS. Episodes of sinus arrest, severe bradycardia and short bursts of tachyarrhythmias in asymptomatic patients were diagnosed in many of our patients only by use of the Holter monitor. The decision to place a permanent pacemaker in a child is a difficult one and documentation of serious arrhythmias is mandatory in making the appropriate decision. Failure to recognize these dysrhythmias may lead to syncope and death. In contrast to adult patients, infants may not manifest symptoms. The absence of symptoms in infancy should not preclude further investigation or treatment. Patients with definite SSS may have normal sinus rhythm during the course of their disease. It is likely that a spectrum of abnormalities exists from patients with severe unremitting sinus disease to those with intermittent and mild disease which is not easily recognizable or diagnosed. Treatment
Pharmacologic therapy alone has been unsuccessful in treatment of SSS.3' However, it is often required in the control of tachyarrhythmia. Electrical pacing has been frequently employed because it not only successfully protects from complications associated with bradyarrhythmias but may also be effective in suppressing tachyarrhythmias27-29 and preventing adverse effects on the conduction system when the addition of antiarrhythmic agents is required.3-5 30 the optimum therapy in the postoperative patient is dependent upon specific dysrhythmias present. During the immediate postoperative period, evaluation
should include adequate monitoring with Holter monitor and temporary pacing via epicardial wires left at the time of surgery. No treatment is necessary in asymptomatic patients with sinus bradyarrhythmias and documented adequate sustained junctional escape mechanism (case 7). If symptoms occur, the escape rate is inadequate and dysrhythmia persists for more than a few weeks, a permanent demand pacemaker is indicated. If tachyarrhythmias are present, a demand pacemaker and antiarrhythmic drug treatment are indicated. Death probably occurred in two of our patients from the use of pharmacologic treatment without pacing. Antiarrhythmic drug therapy alone is unsatisfactory since the drugs utilized (quinidine, propranolol, digoxin) can further suppress sinus or lower escape mechanisms. Cardioversion is best attempted with a temporary transvenous demand pacemaker in place due to the possibility of both conversion asystole and inadequate sinus response. Any patient with SSS who is not paced should be carefully followed for an indefinite period of time. We feel that any well documented episode of sinus failure without an adequate escape rhythm should be treated with a permanent pacemaker. It is worth emphasizing that the subgroup of patients with SSS in whom the escape mechanism is inadequate is at particular risk from bradyarrhythmias producing syncope or death. References 1. Lows B: Electrical reversion of cardiac arrhythmias. Br Heart J 29: 469, 1967 2. SHORT DS: The syndrome of alternating bradyeardia and tachycardia. Br Heart J 16: 208, 1954 3. RUBENSTEIN JJ, SCHULM1AN CL, YURCHAK PM, DESANCTIS RW: Clinical spectrum of the sick sinus syndrome. Circulation 46: 5, 1972 4. FERRER M I: The sick sinus syndrome. Circulation 47: 635, 1973 5. KAPLAN BM, LAN'GENDORF R, LEV M, PICK A: Tachyeardiabradyeardia syndrome (so-called 'sick sinus syndrome'). Am J Cardiol 31: 497, 1973 6. EL-SAID G, ROSENBERG HS, MUwLLNS CS, HALLMAN GL, COOLEY DA, MCNAMARA DG: Dysrhythmias after Mustard's operation for transposition of the great arteries. Am J Cardiol 30: 526, 1972 7. ISAACSON R, TITUS JL, MERIDETH J, FELDT RH, MCGOON DC: Apparent interruption of atrial conduction pathways after surgical repair of transposition of great arteries. Am J Cardiol 30: 533, 1972 8. ABERDEEN E, WATERSTON DJ, CARR I, GRAHAM G, BONHAMCARTER RE, SUBRAMANIAN S: Successful correction of transposed great arteries by Mustard's operation. Lancet 1: 1233, 1965 9. ZLBERBUHLER JR, BAUERSFELD SR: Unusual arrhythmias after corrective surgery for transposition of the great vessels. Am Heart J 73: 752, 1967 10. HALLER JA JR, CRISLER C, BRAWLEY R, CAMERON J? ROWE RD: Operative correction and postoperative management of transposition of the great vessels in nine children. Ann Thorac Surg 7: 212, 1969
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POSTOPERATIVE SSS 11. STARK J: Primary definitive intracardiac operations in infants: Transposition of the great arteries. In Advances in Cardiovascular Surgery, edited by KIRKLIN JW. New York, Grune and Stratton, 1973, p 101 12. KHOURY GH, SHAHER RM, FOWLER RS, KEITH JD: Preoperative and postoperative electrocardiogram in transposition of the great arteries. Am Heart J 72: 199, 1966 13. CHAMPSAUR GL, SOKOL DM, TRUSLER GA, MUSTARD WT: Complete transposition of the great arteries in 123 pediatric patients. Circulation 47: 1032, 1973 14. HAMILTON SD, BARTLEY TD, MILLER RH, SCHIEBLER GL, MARRIOTT HJL: Disturbances in atrial rhythm and conduction following the surgical creation of an atrial septal defect by the Blalock Hanlon technique. Circulation 38: 73, 1968 15. TUNG KSK, JAMES TN, EFFLER DB, MCCORMACK LJ: Injury of the sinus node in open heart operations. J Thorac Cardiovasc Surg 53: 814, 1967 16. SEALY WC, FARMER JC, YOUNG WG JR, BROxvN IW JR: Atrial dysrhythmia and atrial secundum defects. J Thorac Cardiovasc Surg 57: 245, 1969 17. LINDE LM, GOLDBERG SJ, SEIGEL S: The natural history of arrhythmias following septal defect repair. J Thorac Cardiovasc Surg 48: 303, 1964 18. REID JM, STEVENSON JC: Cardiac arrhythmias following successful surgical closure of atrial septal defect. Br Heart J 29: 742, 1967 19. YOLNG D: Later results of closure of secundum atrial septal defect in children. Am J Cardiol 31: 14, 1973 20. SELLERS RP, FERLIC RM, STERNS LP, LILLEHEI CW: Secundum type atrial septal defects: Early and late effects of surgical
213 repair using extracorporeal circulation in 275 patients. Surgery 59: 155, 1966 21. ZIAI)Y GM, HALLIDIE-SMIITH KA, GOODWIN JF: Conduction 22.
23.
24.
25.
26.
27. 28.
29.
disturbances after surgical closure of ventricular septal defect. Br Heart J 34: 1199, 1972 SASAKI R, THEILEN EO, JANUARY LE, EHRENHAFT JL: Cardiac arrhythmias associated with the repair of atrial and ventricular septal defects. Circulation 18: 909, 1958 LANITIMAN B, WOLF MD: Total correction of tetralogy of Fallot. II. Changes in electrocardiogram following surgery. Circulation 31: 394, 1965 RASTELLI GC, RAHIMTOOLA SH, ONCLEY PA, McGooN DC: Common atrium: Anatomy, hemodynamics and surgery. J Thorac Cardiovasc Surg 55: 834, 1968 CLARK EB, ROLAND JMA, VARGHESE PJ, NEILL CA, HALLER JA: Should the sinus venosus type ASD be closed? A review of the atrial conduction defects and surgical results in 28 children. Am J Cardiol 35: 127, 1975 KENNEL AJ, TITUS JL: The vasculature of the human sinus node. Mayo Clin Proc 47: 556, 1972 COHEN HE, KAHN M, DoNoso E: Treatment of supraventricular tachycardia with catheter and permanent pacemakers. Am J Cardiol 20: 735, 1967 KRAMER DH, Moss AJ: Current pacemaker therapy of bradyeardia rhythms. Cardio Dig 6: 21, 1971 CHENG TO: Transvenous ventricular pacing in the treatment of
paroxysmal atrial tachyarrhythmias alternating with sinus bradycardia and standstill. Am J Cardiol 22: 874, 1968 30. TICZON AR, WHALEN RW: Refractory supraventricular tachycardia. Circulation 47: 642, 1973
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Sick sinus syndrome after surgery for congenital heart disease. R D Greenwood, A Rosenthal, L J Sloss, M LaCorte and A S Nadas Circulation. 1975;52:208-213 doi: 10.1161/01.CIR.52.2.208 Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1975 American Heart Association, Inc. All rights reserved. Print ISSN: 0009-7322. Online ISSN: 1524-4539
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THE TERM SICK SINUS SYNDROME (SSS)
from January 1960 through June 1974 for patients with SSS. Sixteen patients developed SSS following cardiac surgery and form the basis of this report; four children with SSS, not related to cardiac surgery, were excluded. During this period, approximately 40 patients underwent a Mustard operation, 450 underwent tetralogy repair and 500 underwent closure of an atrial septal defect. To determine the true incidence of the dysrhythmia, the records of 102 randomly selected patients undergoing tetralogy of Fallot repair (1962-1972) and 35 consecutive patients representing all patients undergoing the Mustard operation from September 1972 through June 1974 were reviewed. The patients reported were on continuous electrocardiographic monitors for the first few days postoperatively and for longer periods if dysrhythmias were present. Standard 12 lead electrocardiograms were obtained in the first postoperative day, prior to discharge, and within one year after surgery. Frequent rhythm strips were taken throughout the hospitalization and on follow-up visits. A Holter monitor was employed in six of 16 patients during the recovery period and after discharge in 11 of 16. Each patient was monitored during sleep and waking periods.
was first used by Lown' to describe failure of the sinus node to assume control following cardioversion of chronic atrial fibrillation. In recent years, the term SSS has been used to describe a clinical entity which includes various disturbances in sinus or atrial rhythm. It is often used interchangeably with the term tachycardia-bradycardia syndrome.2`5 The SSS, a potentially fatal arrhythmia, has been attributed in adults3' 4 to pathologic changes in the sinus node, atria, and atrioventricular junction due to coronary artery disease, cardiomyopathy, hypertensive heart disease or to unknown etiology. The syndrome has been recognized with increasing frequency following surgical repair in children with congenital heart disease. This study describes our experience with SSS following cardiac surgery at The Children's Hospital Medical Center. Methods
Definition
The files in the Medical Records Department and the Departments of Cardiology and Cardiovascular Surgery at The Children's Hospital Medical Center were searched
SSS was defined as the occurrence of sinus bradyeardia (a sustained rate of less than 50 per minute for patients five years of age or older and less than 55 per minute for younger children), with or without arrest or exit block, associated paroxysmal atrial fibrillation, flutter, tachycardia or the presence of symptoms. Junctional rhythm (defined as less than the slowest normal sinus rate for that age) without documented sinus bradyeardia, sinus arrest or exit block, was not considered to represent SSS unless the arrhythmia persisted or recurred frequently after discharge from the hospital. Patients with accelerated junctional rhythm or tachyarrhythmias without bradyarrhythmias, or with chemical or toxic etiology for the dysrhythmia (e.g., hypokalemia, digitalis toxicity) were not included. Also ex-
From the Department of Cardiology, The Children's Hospital Medical Center and the Department of Pediatrics, Harvard Medical School, Boston, Massachusetts. Supported in part by Training Grant HL05855, Program Project HL10436 from the National Institutes of Health, and a grant-in-aid from the American Heart Association. Address for reprints: Ronald D. Greenwood, M.D. The Children's Hospital Medical Center, 300 Longwood Avenue, Boston, Massachusetts 02115. Received January 17, 1975; revision accepted for publication March 12, 1975.
208
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POSTOPERATIVE SSS
209
Table 1 Postoperative Rhythm in 35 Consecutive Mustard Operations
Normal sinus rhythm Minor rhythm abnormalities Abnormal P wave Coronary sinus rhythm
No. of patients
Percent
8 6
23% 17%
6 9 7 8
17% 26%
(4 (2)
Junctional rhythm Accelerated junctional rhythm Supraventricular tachyeardia Conduction abnormalities 10 Atrioventricular block Right bundle branch block Trifascicular block Complete heart block Transient atrioventricular dissociation Sick sinus syndrome
(1) '3) (1) (1) (2)
a
20%
23%C
14%
eluded were patients with bradyeardia associated with ventilatory problems, transient dysrhythmias following cardioversion, patients whose only abnormality was sinus bradyeardia or junctional rhythm for short periods and patients with junctional rhythm associated with transient or permanent complete heart block. By adherence to these criteria, a number of patients with less severe probable SSS were omitted. Results Occurrence
SSS occurred in five of 35 (14%) patients with Dtransposition of the great arteries undergoing consecutive Mustard operations (table 1) and in none of 102 randomly selected patients following repair of tetralogy of Fallot (table 2). SSS developed after surgery in 16 patients ranging in age, at the time of diagnosis, from 11 months to 22 Table 2 Postoperative Rhythm in 87 Survivors of 102 Patients Undergoing Intracardiac Repair for Tetralogy of Fallot Postoperative rhythm
Normal sinus rhythm Conduction disturbance Right bundle branch block Right bundle branch block and left anterior hemiblock Left anterior hemiblock Complete heart block 10 Atrioventricular block Ventricular dysrhythmias Premature ventricular contractions Ventricular tachycardia Atrial dysrhythmias Coronary sinus rhythm Paroxysmal atrial tachycardia Atrial flutter Junctional tachycardia Junctional escape rhythm
Sinuts bradycardia
Sick sinus syndrome
No. of patients
Percent
6
70 8
80 9
1 3 10
1 3 11
8 3
9 3
1 1 2 2 1 3 0
1 1 2 2 1
3 0
years (table 3). It followed the Mustard operation in five patients (31%), atrial septal defect closure in six (38%), tetralogy of Fallot repair in four (25%), and aortic valve replacement following ventricular septal defect closure in one (6%). The atrial septal defect was of the sinus venosus type and associated with partial anomalous pulmonary venous return in two patients (cases 8, 15), of the secundum variety in three patients (cases 3, 13, 16) and a common atrium in one (case 6). Three of the five patients undergoing Mustard operation had a previous surgical atrial septectomy. Surgical Technique
Surgery was performed in all patients utilizing cardiopulmonary bypass with additional hypothermia employed in two (cases 2, 7). Superior vena caval cannulation was performed in all and an atriotomy was performed in 13/16. All operations resulted in hemodynamically satisfactory repair except in patient 4 who has a persistent ventricular septal defect. Clinical Description
In 12 of 16 patients (75%), including all those with transposition, the arrhythmia occurred immediately after the operative procedure and in the remaining four (25%) two to 48 months after surgery. Delayed onset of arrhythmia was noted in three of four patients with tetralogy and one with atrial septal defect. Tachy-bradyarrhythmias were present in 12 patients and bradyarrhythmias alone in four. Among the former, the tachyarrhythmias noted were atrial flutter (7), atrial fibrillation (2) and supraventricular tachycardias (8). The bradyarrhythmias in this group included sinus arrest (4), sinus bradyeardia (10), asystole (1), nodal escape rhythm (12), sinoatrial block (2) and predominant ventricular escapes in one. The patients with isolated bradyarrhythmias exhibited sinus bradyeardia (three patients), sinus arrest (two patients) and nodal escape (three patients). Associated conduction abnormalities observed included right bundle branch block in three (patients 1, 3, 5), trifascicular block in two (patients 4, 13) and trifascicular block with transient complete heart block in one (patient 10). Dynamic electrocardiogram recorded via Holter 12-24 hour monitors was extremely helpful in defining the type and severity of the arrhythmia (table 4). Periods of sinus arrest made after initial diagnosis (e.g., patients 2, 12) were helpful in determining treatment. Therapy
Pharmacologrc treatment employed was quinidine in seven patients (cases 1, 3, 4, 5, 9, 14, 16), isuprel in two patients (cases 13, 15) and digitalis in 13 patients (cases 1-9 and 11, 12, 14, 16), seven of whom received the latter drug primarily for congestive heart failure.
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Table 3 Clinical Presentation and Course of Patients Developing Sick Sinus Syndrome after Surgery
Patient
1 2
3 4 5 6
7 8 9 10 11 12
13
14
15 16
Cardiac diagnosis
Surgery (age yr)
Postop time of diagnosis of SSS
Major rhythms at time of diagnosis
Total repair (7); residual Immediately FL, SVT, SB, SA, CA, JR ventricular septal defect closure (20) Immediately JR, SB Atrial septal defect D-transposition of the great arteries creation (5d); Mustard (11/12) FL, FI, SB, JR 13o mos Pulmonary stenosis; Total repair (6) atrial septal defect, secundum FL, AT, SB, JR 48 mos Tetralogy of Fallot Total repair (18) 2 mos FL, SA, SB, JR Tetralogy of Fallot Total repair (6) Immediately SVT, JR, SB, SA Atrial septal defect, Common atrium repair (20) common atrium, endocardial cushion defect D-transposition of Immediately SB, JR, SA Mustard (1) the great arteries Atrial septal defect, Total repair (1 4/12) Immediately SAB, AT, JR sinus veniosus Atrial septal defect Immediately FI, FL, JR, SB D-transposition of creation (3 wk); the great arteries Mustard (4 4/12) SB 9 mos Tetralogy of Fallot Total repair (7 8/12) Immediately SVT, JR D-transposition of Atrial septal defect creation (4 d); the great arteries MViustard (2) Immediately SB, JR, Vent Ex, D-transposition of Mustard palliative SVT the great arteries (10 5/12) Atrial septal defect, Total repair (7 8/12) Immediately SB, SA, JR, SVT secundum; ventricular septal defect Ventricular septal Ventricular septal Immediately SAB, SB, JR, FL, defect-total repair (8); PAT defect; aortic regurgitation aortic valve replacement (14) Atrial septal defect, Total repair (5) Immediately SA, JR sinus venosus Immediately FL, SB, JR Atrial septal defect, Total repair (5%12) secundum Tetralogy of Fallot
Pacemaker
Outcome Alive (A) Time after or diagnosis dead (D) of SS (yr)
Permanent
A
1 5/12
Temporary
A
10/12
0
A
2 7/12
Permarnent, 0 0
A 1) D
2 2/12 2 7/12 6 davs
0
A
3/12
0
A
3/12
Permanent
A
1 4/12
Permanent 0
A A
8 3/12 1 4/12
Permanent
A
2,/12
Temporary
A
10/12
0
A
5 7/12
0
A
1 1/12
0
A
11 9/12
Abbreviations: SSS = sick sinus syndrome; Postop = postoperative period; FT = fibrillation (atrial); FL = flutter (atrial); SVT = supraventricular tachycardia; SB - sinus bradyeardia. SA = sinus arrest; CA = cardiac arrest; JR = junctional rhythm; AT = atrial tachycardia; SAB = sinus block; Vent Ex = ventricular escape beats.
Cardioversion was employed in eight patients (cases 1, 3, 4, 6, 8, 9, 14, 16) to terminate tachyarrhythmias. Permanent epicardial pacemakers were placed in five patients, for cardiac arrest in one (patient 1), inadequate escape rhythm with extremely slow ventricular rate in two (patients 9, 12, one of whom - patient 9 - exhibited syncopal episodes with a rate of 18/min), and trifascicular block in two (patients 4, 10, one of whom - patient 4 - exhibited syncope). A temporary pacemaker was employed in two additional patients (cases 2, 13) because of an inadequate rate and was maintained in the latter patient for one month. Patient 6 developed syncope and hypotension and died before a pacemaker could be placed.
Follow-up
Fourteen of the 16 patients are alive and have been followed from two months to 12 years after the onset of SSS. The predominant rhythm in these patients, when last seen, was normal sinus rhythm in two (patients 8, 14), sinus bradyeardia in one (patient 13), sinus rhythm with sinus arrest and junctional escape in one (patient 2), junctional with wandering pacemaker in one (patient 15), junctional in three (patients 7, 11, 16), atrial flutter with block in one (patient 3) and paced in five (patients 1, 4, 9, 10, 12). Two of 16 patients (cases 5, 6) died with arrhythmias six days and 2 7/12 years after documented onset of SSS. Postmortem studies were Circulation, Volume 52, August 1975
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POSTOPERATIVE SSS
211
Table 4 Holter Monitoring of Patients with Sick Sinus Syndrome Patient
1 2
3 7 8 11 12
13
14 15
16
Time postoperatively
1 mo 1 wk 10/12 3 9/12 10 dy 3 mo 5 dy 12 dy 2 h' mo 13 mo 17 dv 20 dy 22 dy 23 dy 14 dy 28 dy 10 mo
Hours of
monitoring 12
12 12 24 12
yr yr
12 12 12
12 12 24 24 24 24 12 12 12
5 yr 2 dy 8 mo 11 9,/12 vr
12 12 24 12
Findings
JR, SA, atrial bigeminy JR, NSR SA, JR, WAP, NSR FL, varying block NSR, JR JR 2:1 SA exit block, SA FL, varying block NSR JR, SVT JR JR, 4.5 Sec. SA SA, multiple, 2.4 sec. Multiple SA SA, then paced NSR SB, nonconducted atrial bigeminy SA 1.2 see.. vent. esc. SA WAP, JR WAP
Abbreviations: JR = junctional rhythm; SA - sinus arrest; NSR = normal sinus rhythm; WAP = watidering atrial pacemaker; FL = flutter (atrial); SVT = supraventricular tachycardia; SB sinus bradyeardia; vent. esc. = ventricular escape beats. =
performed in both. In case 5, the tetralogy of Fallot was well repaired but a surgical suture had been placed in the area of the sinoatrial node. In case 6, the repair of the common at$$ium was accomplished by construction of a dacron baffle diverting blood from the right superior vena cava, hepatic veins and left superior vena cava to the right side of the heart and from the widely separated pulmonary veins to the left side of the heart. The baffle was large and produced some obstruction of the mitral valve. Discussion Incidence
SSS is characterized by the occurrence of marked sinus bradyeardia or arrest or sinoatrial exit block with or without an escape rhythm (junction or ventricular) or atrial tachyarrhythmias (fibrillation, flutter, tachycardia). Symptoms and complications associated with dysrhythmias vary greatly. Although not termed SSS, identical dysrhythmias have been previously described following cardiac surgery. Sinus bradyeardia, sinoatrial block or arrest, escape rhythms or tachyarrhythmias have been noted following the Mustard operation,6 -13 Blalock-Hanlon procedure,7' 14 Senning operation,7 atrial septal defect repair" and less commonly in ventricular septal defect repair,'7' 21, 22 tetralogy of Fallot repair'5' 21, 23 and other cardiac operations.'5' 24
Atrial surgery, the Mustard operation in particular, highest incidence of dysrhythmias. In one series, only three of 60 patients surviving Mustard operation have remained free of dysrhythmias.f A significant number of these exhibited passive dysrhythmias including sinoatrial is associated with the
block, wandering pacemaker, junctional rhythm
or
atrioventricular dissociation. Tachyarrhythmias (supraventricular tachycardia and atrial flutter) were also present. It is not clear whether these conditions coexisted in some patients with bradyarrhythmias. One patient with junctional rhythm and recurrent atrial flutter died after surgery. Among our patients undergoing the Mustard procedure only eight of 35 (22%) were free of any dysrhythmia and five (14%) exhibited classical SSS (table 1). Among a randomly selected group of survivors after repair for tetralogy at our institution, none exhibited SSS (table 2). Atrial septal defects of the sinus venosus variety represent a small proportion of all patients with atrial septal defects and the interatrial communication is usually small. However, the location of the defect allows a high incidence of sinus dysfunction.25 Pathology and Mechanism
Pathologic changes of the sinus node, atria and atrioventricular junction have been noted in adults with S5.5 Injury to these structures at surgery may produce SSS and an inadequate escape rhythm. In patients developing SSS after cardiac surgery, the dysrhythmia may be related to injury to or around the sinus node, the sinoatrial nodal artery or the internodal atrial tracts. Pathologic studies of patients with postoperative dysrhythmias have shown abnormalities in the sinoatrial node and sinoatrial nodal artery.6 7 In addition, clinical and pathologic studies have shown that damage to the internodal pathways during a Mustard, Senning or Blalock-Hanlon operation is associated with rhythm disturbances, usually junctional rhythm.7 The mechanisms of the bradycardia may be a disorder of impulse generation in the sinus node or disordered conduction from the sinus node.3' 4 In addition, in patients with inadequate escape rhythm in response to the sinus bradyeardia or arrest episodes, we may presume that there are abnormalities in automaticity of the atrioventricular junction. The paradox of rapid ventricular response to the tachyarrhythmias yet inadequate escape rhythm is explained by the observation that atrioventricular conduction and automaticity are related to different portions of the atrioventricular junctional tissues.5 Prevention
Modifications of the Mustard procedure by using the right atrial appendage rather than superior vena cava for cannulation, making the atriotomy anterior to
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GREENWOOD ET AL.
the sulcus terminalis and fixation of the intra-atrial baffle away from the superior vena cava have been suggested as preventive measures in avoiding dysrhythmias.6 Modification in repair of sinus venosus atrial septal defect might include swinging of the superior margin of the patch posteriorly into the left atrium instead of anchoring it to the cristt terminalis. In all operations involving cardiopulmonary bypass, anchoring sutures to cannulae in the superior vena cava or placement of sump suckers may produce injury to the sinoatrial node or its artery and result in SSS. Confining the atriotomy, if possible, to the trabeculated portion of the right atrium and avoidance of the crista terminalis and other conduction tissues may result in fewer dysrhythmias. Awareness of the variation in origin of the sinoatrial nodal artery26 should lead to its avoidance at surgery and may also reduce the incidence of damage to the node. We have not noted this syndrome in any patients operated under inflow occlusion. Diagnosis
The Holter monitor provides an excellent tool for evaluating patients suspected of having SSS. Episodes of sinus arrest, severe bradycardia and short bursts of tachyarrhythmias in asymptomatic patients were diagnosed in many of our patients only by use of the Holter monitor. The decision to place a permanent pacemaker in a child is a difficult one and documentation of serious arrhythmias is mandatory in making the appropriate decision. Failure to recognize these dysrhythmias may lead to syncope and death. In contrast to adult patients, infants may not manifest symptoms. The absence of symptoms in infancy should not preclude further investigation or treatment. Patients with definite SSS may have normal sinus rhythm during the course of their disease. It is likely that a spectrum of abnormalities exists from patients with severe unremitting sinus disease to those with intermittent and mild disease which is not easily recognizable or diagnosed. Treatment
Pharmacologic therapy alone has been unsuccessful in treatment of SSS.3' However, it is often required in the control of tachyarrhythmia. Electrical pacing has been frequently employed because it not only successfully protects from complications associated with bradyarrhythmias but may also be effective in suppressing tachyarrhythmias27-29 and preventing adverse effects on the conduction system when the addition of antiarrhythmic agents is required.3-5 30 the optimum therapy in the postoperative patient is dependent upon specific dysrhythmias present. During the immediate postoperative period, evaluation
should include adequate monitoring with Holter monitor and temporary pacing via epicardial wires left at the time of surgery. No treatment is necessary in asymptomatic patients with sinus bradyarrhythmias and documented adequate sustained junctional escape mechanism (case 7). If symptoms occur, the escape rate is inadequate and dysrhythmia persists for more than a few weeks, a permanent demand pacemaker is indicated. If tachyarrhythmias are present, a demand pacemaker and antiarrhythmic drug treatment are indicated. Death probably occurred in two of our patients from the use of pharmacologic treatment without pacing. Antiarrhythmic drug therapy alone is unsatisfactory since the drugs utilized (quinidine, propranolol, digoxin) can further suppress sinus or lower escape mechanisms. Cardioversion is best attempted with a temporary transvenous demand pacemaker in place due to the possibility of both conversion asystole and inadequate sinus response. Any patient with SSS who is not paced should be carefully followed for an indefinite period of time. We feel that any well documented episode of sinus failure without an adequate escape rhythm should be treated with a permanent pacemaker. It is worth emphasizing that the subgroup of patients with SSS in whom the escape mechanism is inadequate is at particular risk from bradyarrhythmias producing syncope or death. References 1. Lows B: Electrical reversion of cardiac arrhythmias. Br Heart J 29: 469, 1967 2. SHORT DS: The syndrome of alternating bradyeardia and tachycardia. Br Heart J 16: 208, 1954 3. RUBENSTEIN JJ, SCHULM1AN CL, YURCHAK PM, DESANCTIS RW: Clinical spectrum of the sick sinus syndrome. Circulation 46: 5, 1972 4. FERRER M I: The sick sinus syndrome. Circulation 47: 635, 1973 5. KAPLAN BM, LAN'GENDORF R, LEV M, PICK A: Tachyeardiabradyeardia syndrome (so-called 'sick sinus syndrome'). Am J Cardiol 31: 497, 1973 6. EL-SAID G, ROSENBERG HS, MUwLLNS CS, HALLMAN GL, COOLEY DA, MCNAMARA DG: Dysrhythmias after Mustard's operation for transposition of the great arteries. Am J Cardiol 30: 526, 1972 7. ISAACSON R, TITUS JL, MERIDETH J, FELDT RH, MCGOON DC: Apparent interruption of atrial conduction pathways after surgical repair of transposition of great arteries. Am J Cardiol 30: 533, 1972 8. ABERDEEN E, WATERSTON DJ, CARR I, GRAHAM G, BONHAMCARTER RE, SUBRAMANIAN S: Successful correction of transposed great arteries by Mustard's operation. Lancet 1: 1233, 1965 9. ZLBERBUHLER JR, BAUERSFELD SR: Unusual arrhythmias after corrective surgery for transposition of the great vessels. Am Heart J 73: 752, 1967 10. HALLER JA JR, CRISLER C, BRAWLEY R, CAMERON J? ROWE RD: Operative correction and postoperative management of transposition of the great vessels in nine children. Ann Thorac Surg 7: 212, 1969
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POSTOPERATIVE SSS 11. STARK J: Primary definitive intracardiac operations in infants: Transposition of the great arteries. In Advances in Cardiovascular Surgery, edited by KIRKLIN JW. New York, Grune and Stratton, 1973, p 101 12. KHOURY GH, SHAHER RM, FOWLER RS, KEITH JD: Preoperative and postoperative electrocardiogram in transposition of the great arteries. Am Heart J 72: 199, 1966 13. CHAMPSAUR GL, SOKOL DM, TRUSLER GA, MUSTARD WT: Complete transposition of the great arteries in 123 pediatric patients. Circulation 47: 1032, 1973 14. HAMILTON SD, BARTLEY TD, MILLER RH, SCHIEBLER GL, MARRIOTT HJL: Disturbances in atrial rhythm and conduction following the surgical creation of an atrial septal defect by the Blalock Hanlon technique. Circulation 38: 73, 1968 15. TUNG KSK, JAMES TN, EFFLER DB, MCCORMACK LJ: Injury of the sinus node in open heart operations. J Thorac Cardiovasc Surg 53: 814, 1967 16. SEALY WC, FARMER JC, YOUNG WG JR, BROxvN IW JR: Atrial dysrhythmia and atrial secundum defects. J Thorac Cardiovasc Surg 57: 245, 1969 17. LINDE LM, GOLDBERG SJ, SEIGEL S: The natural history of arrhythmias following septal defect repair. J Thorac Cardiovasc Surg 48: 303, 1964 18. REID JM, STEVENSON JC: Cardiac arrhythmias following successful surgical closure of atrial septal defect. Br Heart J 29: 742, 1967 19. YOLNG D: Later results of closure of secundum atrial septal defect in children. Am J Cardiol 31: 14, 1973 20. SELLERS RP, FERLIC RM, STERNS LP, LILLEHEI CW: Secundum type atrial septal defects: Early and late effects of surgical
213 repair using extracorporeal circulation in 275 patients. Surgery 59: 155, 1966 21. ZIAI)Y GM, HALLIDIE-SMIITH KA, GOODWIN JF: Conduction 22.
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disturbances after surgical closure of ventricular septal defect. Br Heart J 34: 1199, 1972 SASAKI R, THEILEN EO, JANUARY LE, EHRENHAFT JL: Cardiac arrhythmias associated with the repair of atrial and ventricular septal defects. Circulation 18: 909, 1958 LANITIMAN B, WOLF MD: Total correction of tetralogy of Fallot. II. Changes in electrocardiogram following surgery. Circulation 31: 394, 1965 RASTELLI GC, RAHIMTOOLA SH, ONCLEY PA, McGooN DC: Common atrium: Anatomy, hemodynamics and surgery. J Thorac Cardiovasc Surg 55: 834, 1968 CLARK EB, ROLAND JMA, VARGHESE PJ, NEILL CA, HALLER JA: Should the sinus venosus type ASD be closed? A review of the atrial conduction defects and surgical results in 28 children. Am J Cardiol 35: 127, 1975 KENNEL AJ, TITUS JL: The vasculature of the human sinus node. Mayo Clin Proc 47: 556, 1972 COHEN HE, KAHN M, DoNoso E: Treatment of supraventricular tachycardia with catheter and permanent pacemakers. Am J Cardiol 20: 735, 1967 KRAMER DH, Moss AJ: Current pacemaker therapy of bradyeardia rhythms. Cardio Dig 6: 21, 1971 CHENG TO: Transvenous ventricular pacing in the treatment of
paroxysmal atrial tachyarrhythmias alternating with sinus bradycardia and standstill. Am J Cardiol 22: 874, 1968 30. TICZON AR, WHALEN RW: Refractory supraventricular tachycardia. Circulation 47: 642, 1973
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Sick sinus syndrome after surgery for congenital heart disease. R D Greenwood, A Rosenthal, L J Sloss, M LaCorte and A S Nadas Circulation. 1975;52:208-213 doi: 10.1161/01.CIR.52.2.208 Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1975 American Heart Association, Inc. All rights reserved. Print ISSN: 0009-7322. Online ISSN: 1524-4539
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