Catheterization and Cardiovascular Interventions 84:622–628 (2014)
Outcomes Following Cardiac Catheterization After Congenital Heart Surgery Stephanie L. Siehr,1 MD, Mary Hunt Martin,2 MD, David Axelrod,1 MD, Bradley Efron,3 PhD, Lynn Peng,1 MD, Stephen J. Roth,1 MD, MPH, Stanton Perry,1 MD, and Andrew Y. Shin,1* MD Objectives: Describe outcomes following unplanned cardiac catheterization after congenital heart surgery. Background: Utility of cardiac catheterization following congenital heart surgery is relatively understudied. Methods: Retrospective study examining demographics, indications, and outcomes of unplanned cardiac catheterization after congenital heart surgery at a single institution. Results: Between October 2004 and April 2011, 120 patients underwent 150 unplanned postoperative cardiac catheterizations. Median day of catheterization was postoperative day 20 (range 1–269 days). Survival 30 days postcatheterization was 85%; overall survival to hospital discharge was 72%. Indications for catheterization: 63 for hemodynamic evaluation, 46 for likely intervention, and 41 for assessment of surgical repair. Of the 150 hemodynamic/interventional catheterizations, 103 (69%) were associated with a change in clinical management: 59 trans-catheter interventions, 22 re-operations, 11 changes in medication, six changes in surgical plan, and five withdrawals of support. Complications included hemorrhage in two patients, supraventricular tachycardia in two patients, and transient complete heart block requiring cardiopulmonary resuscitation in one patient. Conclusions: Cardiac catheterization following congenital heart surgery may enable important diagnostic and therapeutic changes in clinical and surgical management. Complications were rare. VC 2014 Wiley Periodicals, Inc. Key words: congenital heart disease; pediatrics; pediatric intervention; complications; pediatric catheterization/intervention
INTRODUCTION
Since the beginning of the surgical era in congenital heart disease, there have been substantial advances in the role of cardiac catheterization [1–5]. For presurgical assessment, diagnostic catheterization often plays an invaluable role [4,6–9]. However, there is little published data assessing the value of diagnostic or interventional cardiac catheterization in the postoperative period following congenital heart surgery. Previous studies report mixed results concerning the benefits and risks of cardiac catheterization in the vulnerable postoperative period [10–16]. Complications such as arrhythmias, contrast-related acute kidney injury (AKI), and death have been observed [16–18], but subsequent reports describe more favorable outcomes with improved survival using a multidisciplinary team approach [14]. These reports are limited by small sample size, thus reducing their impact and applicability. In a recent consensus statement by the American Heart Association, the evidence regarding the utility of cardiac catheterization in the early postoperative period C 2014 Wiley Periodicals, Inc. V
1
Department of Pediatrics, Cardiovascular Institute, Stanford University School of Medicine, Palo Alto, California 2 Department of Pediatrics, Division of Pediatric Cardiology, Primary Children’s Medical Center, Salt Lake City, Utah 3 Department of Health Research and Policy, Division of Biostatistics, Stanford University Medical Center, Palo Alto, California Conflict of interest: Nothing to report. *Correspondence to: Andrew Y. Shin; Clinical Assistant Professor, Associate Section Chief, Cardiovascular Intensive Care, Lucile Packard Children’s Hospital, Stanford University Medical Center, 750 Welch Rd, Ste 305, Palo Alto, CA 94304. E-mail: drewshin@ stanford.edu Received 12 September 2013; Revision accepted 12 March 2014 DOI: 10.1002/ccd.25490 Published online 21 March 2014 in Wiley Online Library (wileyonlinelibrary.com)
Catheterization After Congenital Heart Surgery
was determined to be conflicting (Class II recommendation) and sparse (level of evidence C) [8]. The goal of this study was to describe the outcomes following unplanned cardiac catheterization in the entire postoperative period following congenital heart surgery. We hypothesized that cardiac catheterization influences subsequent clinical management with a low adverse event rate.
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on if an intervention was performed during cardiac catheterization. When possible, trans-catheter interventions were categorized as interventions to augment pulmonary blood flow (dilation of and/or stent implantation in existing shunts, conduits, or native aortopulmonary collateral arteries) or to reduce pulmonary blood flow (device closures of existing shunts, conduits, aortopulmonary collateral arteries, or native outflow tracts). Clinical Outcomes
MATERIALS AND METHODS Study Design and Patients
This is a retrospective case series examining outcomes following unplanned cardiac catheterization during the postoperative period after congenital heart surgery at a single, tertiary care, pediatric hospital between October 2004 and April 2011 (current era of computer-based data collection). Patients were included if they underwent a cardiac catheterization at any time prior to hospital discharge. Planned cardiac catheterizations, if specifically stated as part of postoperative care in pre-operative or immediate postoperative clinical documentation, were excluded. Central line placement or removal, diaphragm or valve fluoroscopy, and pericardiocentesis performed in the cardiac catheterization lab without an associated hemodynamic or interventional procedure were excluded. Routine surveillance catheterizations and biopsies following cardiac transplantation were also excluded. The cardiac catheterization lab is located in the adjoining adult hospital, which is accessible via a connecting hallway from the children’s hospital. The study protocol was approved by the Institutional Review Board of Stanford University Medical Center. Demographic and Clinical Data Demographic variables, cardiac anatomy, and clinical data were collected from clinical notes. Anatomical and surgical characteristics were catalogued as single ventricle palliation or biventricular repair and assigned a case complexity score utilizing the Risk Adjustment in Congenital Heart Surgery (RACHS-1) system [19]. Contrast dose and fluoroscopy time were collected as safety markers. Given the expected paucity of documentation regarding preprocedure decision making, catheterization was categorized based on the available information into assessment of surgical repair, likely intervention, or hemodynamic study. Trans-catheter Interventions Catheterizations were catalogued as interventional or noninterventional (hemodynamic) post hoc depending
This study sought to determine whether results of the unplanned cardiac catheterization were associated with a significant change in clinical management. The primary end point was a composite outcome including: (1) unplanned early re-operation following cardiac catheterization, (2) trans-catheter intervention, (3) intra-catheterization diagnosis that led to later reoperation or transition to palliative care, or (4) administration of a new pharmacologic agent following catheterization specifically to treat circulatory abnormalities (e.g., pulmonary over-circulation, preexisting thrombus, or pulmonary hypertension). Outcome was determined by chart review, and primary end point was assigned by a committee of pediatric cardiac intensivists and interventionalists. The first 30 patients were reviewed by two investigators separately and confirmed 100% internal validity. The remainder of patients were reviewed after data collection and independently when concerns were raised by the primary investigators. Patients who received additional therapies as a result of complications from cardiac catheterization (e.g., mechanical pacing, heparin) were not considered reaching the primary end point. Secondary end points included death, cerebrovascular accident, major hemorrhage (blood loss leading to clinical instability), arrhythmia during catheterization requiring treatment (pharmacologic, cardiopulmonary support, or mechanical pacing), catheterization-associated blood stream infection (positive blood culture within 72 hours following catheterization), and/or AKI within 36 hours following cardiac catheterization. AKI was defined utilizing the pediatric modified RIFLE (pRIFLE) criteria [20]. Statistical Analysis Categorical variables were compared using a chisquared test. Numerical continuous variables were compared using a paired t-test. A Cox proportional hazards analysis was performed to test the effects of age, RACHS-1 score, and time in days from baseline to catheterization on the response "time from last catheterization to death", with discharge as the censoring variable.
Catheterization and Cardiovascular Interventions DOI 10.1002/ccd. Published on behalf of The Society for Cardiovascular Angiography and Interventions (SCAI).
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Fig. 1. Postoperative cardiac catheterizations.
RESULTS Baseline Characteristics There were 3218 consecutive pediatric and adult patients who underwent congenital heart surgery at our center between October 2004 and April 2011. One hundred fifty unplanned cardiac catheterizations for diagnostic or interventional purposes were performed in 120 patients during their postoperative hospitalization. Figure 1 provides the reason for cardiac catheterization. Median day of catheterization for the entire population was postoperative day 20 (range 1–269 days). Of the 150 catheterizations, 94 (63%) occurred in the early postoperative period within 30 days of the operation. Baseline demographic, anatomic, surgical and catheterization characteristics of the entire study population divided into early (within 30 days of operation) and late (greater than 30 days after operation) groups are summarized in Table I. The early group had more patients on mechanical circulatory support, which was not statistically significant, and shorter intensive care unit length of stay (P ¼< 0.01). Median age at surgery for the entire cohort was 0.35 years (range 0.01–29 years); 74 patients were undergoing biventricular repair and 46 patients single ventricle palliation. The median fluoroscopy time for the entire cohort was 30 (1.5–190) minutes; median contrast volume was 5.1 (0–21.2) ml/kg. The most common diagnosis was tetralogy of Fallot (20%), and the majority of patients had a RACHS-1 score 3. Six patients (seven catheterizations) were receiving extracorporeal membrane oxygenation (ECMO) support and two patients were receiving left ventricular assist device support with a Berlin Heart EXCOR at the time of catheterization. Primary Endpoint
Outcomes following 103 of 150 (69%) diagnostic or interventional catheterizations were as follows: 48
patients underwent 59 catheterizations during which there was at least one trans-catheter intervention, 31 patients underwent an early re-operation, 11 patients received a new pharmacologic agent, six patients had a new operative plan and/or elective re-operation in the future, and five patients were transitioned to palliative care (Table II). Nine patients who underwent a transcatheter intervention also had an early re-operation. There was no associated change in clinical management following 47 of 150 (31%) of diagnostic or interventional catheterizations. The median postoperative day of catheterization that was associated with any clinical change as described above was 19 days (1– 269). Within 30 days of the operation, 69 of 95 (73%) catheterizations were associated with the following outcomes: 41 trans-catheter intervention, 17 immediate reoperations, five new pharmacologic agents, three new operative plans and/or elective re-operations in the future, and three transitions to palliative care (Table II). Trans-catheter intervention. Of the 59 patients who required a trans-catheter intervention, the most common indication for intervention was manipulation of pulmonary blood flow (Table II). Device closure of residual septal defects and fenestrations made up a small minority of cases. There were four interventions in patients on mechanical circulatory support: two left atrial decompressions, one superior vena cava stent, and one coronary stent. Re-operation. Following catheterization, early reoperation was performed in 31 patients (Table II); 16 patients underwent re-operation within 24 hours of catheterization. The median postoperative day of catheterization that resulted in an early re-operation, excluding cavopulmonary anastomosis, was 11 days (1–62 days). The most common indication for re-operation was augmentation of pulmonary blood flow. Impact on clinical care. Postoperative catheterization was associated with a change in medical management in 22 patients (Table II). New pharmacological
Catheterization and Cardiovascular Interventions DOI 10.1002/ccd. Published on behalf of The Society for Cardiovascular Angiography and Interventions (SCAI).
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TABLE I. Patient Characteristics
Demographics Age – years, median (range) Weight – kg, median (range) Sex Type of palliation/repair Postoperative Course Postoperative day of catheterization – days, median (range) Mechanical circulatory support at catheterization – # (percentage) Fluoroscopy time – min, median (range) Contrast dose – ml/kg, median (range) CVICU length of stay– days, median (range) Ventilator duration – days, median (range) Diagnosis Tetralogy of Fallot Atrioventricular septal defect Hypoplastic left heart d-TGA Truncus arteriosus Coarctation of the aorta Aortic stenosis Double outlet right ventricle Tricuspid atresia Double inlet left ventricle l-TGA Double outlet left ventricle Total anomalous pulmonary venous return Pulmonary atresia/ intact ventricular septum Ebstein’s anomaly Shone’s complex Ventricular septal defect Interrupted aortic arch Patent ductus arteriosus Pulmonary stenosis RACHS-1 score 1 2 3 4 5 6
Early (30 days) N ¼ 94 (63%)
Late (>30 days) N ¼ 56 (37%)
0.5 (0.01–29) 6.1 (2.3–109) 45 F, 49 M 32 Single ventricle, 62 Biventricular
0.2 (0.01–21) 4.1 (0.9–49) 29 F, 27 M 28 Single ventricle, 28 Biventricular
13.5 (1–29)* 7 (7%) 25 (2.8–190) 5.1 (0–21.2) 25 (2–151)* 14.5 (1–151)*
54.5 (32–269) 1 (2%) 28.5 (1.5–121) 5.1 (0–19.3) 55.5 (4–190) 15 (1–190)
20 (21%) 12 (13%) 11 (12%) 9 (10%) 7 (7%) 6 (6%) 5 (5%) 5 (5%) 5 (5%) 3 (3%) 3 (3%) 2 (2%) 2 (2%) 1 (1%) 1 (1%) 1 (1%) 1 (1%) – – –
7 (7%) 9 (10%) 9 (10%) 4 (4%) 2 (4%) 1 (2%) 5 (5%) 8 (9%) – 3 (5%) 1 (2%) – – 3 (5%) – – – 2 (4%) 1 (2%) 1 (2%)
– 21 (22%) 48 (51%) 22 (23%) – 3 (3%)
2 (4%) 7 (13%) 25 (45%) 12 (21%) – 10 (18%)
Abbreviations: d-TGA, dextro- transposition of the great arteries; l-TGA, levo- transposition of the great arteries; RACHS, risk adjustment in congenital heart surgery. *- P value < 0:05
agents to address circulatory abnormalies were most commonly systemic or pulmonary vasodilators. Six patients had a new operative plan or elective reoperation as a direct result of findings from the catheterization: one patient had severe pulmonary artery hypoplasia delaying biventricular repair; one had important pulmonary vein stenosis delaying cavopulmonary anastomosis; one had a restrictive bulboventricular foramen influencing timing of subsequent palliation; one had pulmonary hypertension prohibiting cavopulmonary anastomosis; one was diagnosed with partial anomalous pulmonary venous return prompting
elective repair; one had right coronary artery stenosis prompting elective repair. Five patients had their medical care re-directed towards palliative care based, in part, on the findings from their catheterization. Secondary Endpoints Mortality. Thirty-day survival postcatheterization was 85% and overall survival to hospital discharge was 72%. Of the patients who did not survive, 14 had an intervention; three had a re-operation, three had a change in medication, one had a new diagnosis at
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TABLE II.
Primary Outcome: Change in Management
Trans-catheter Intervention Increase PBF - Dilation/stent of pulmonary artery/aortopulmonary collateral - Dilation/stent of shunt/conduit Decrease PBF - Coil - Aortopulmonary collateral - Device closure of shunt/conduit - Device closure of pulmonary artery Dilation/stent - Systemic vein Coil occlusion - Veno-venous collateral Decompression - Left atrium Angioplasty - Coronary artery Device closure - Ventricular septal defect Device closure - Azygous/left superior vena cava Device closure - Atrial septal defect Dilation/stent - Aortic arch Device closure - Fenestration Dilation/stent - Fenestration
New Anatomic Diagnosis Elective re-operation Palliative care
Total # (30 days) 20 (12) 16 (11) 4 (1) 14 (7) 8 (5) 3 3 (2) 6 (5) 5 (5) 4 (3) 2 (2) 2 (2) 2 (1) 1 (1) 1 (1) 1 (1) 1 (1)
6 (3) 5 (3)
Reoperation
Total # (30 days)
Shunt/conduit placement Cavopulmonary anastomosis VSD closure Aortic arch reconstruction Revision of unifocalization Shunt takedown/clip Pulmonary vein repair Coronary artery repair Pulmonary artery band Modified Konno RVOT augmentation LVOT myomectomy Glenn takedown Aortopulmonary collateral ligation
6 (4) 6 (1) 4 (3) 2 (2) 2 (2) 2 (1) 2 (1) 1 (1) 1 (1) 1 (1) 1 1 1 1
Change in Medication Addition of milrinone Addition of sildenafil Increase in furosemide Addition of oxygen Addition of nesiritide Addition of aspirin Addition of tissue plasminogen activator
2 (1) 2 (1) 2 (1) 2 1 (1) 1 (1) 1
Abbreviations: PBF, pulmonary blood flow; VSD, ventricular septal defect; RVOT, right ventricular outflow tract; LVOT, left ventricular outflow tract.
catheterization resulting in change in surgical plan, and four had support withdrawn. Eight patients who died did not have a change in management following catheterization as defined by the study. Of the patients who died, the median postoperative day of catheterization was 26 (2–108 days), which was not significantly different from the patients who survived to discharge [Fig. 2]. Complications. Single instances of pulmonary hemorrhage and peritoneal hemorrhage leading to clinical instability occurred in two (1%) patients, both on mechanical circulatory support receiving systemic anticoagulation. Support was withdrawn on both patients within 24 hours of catheterization. Three patients (2%) experienced a significant arrhythmia: two had supraventricular tachycardia requiring electrical cardioversion; one had transient complete heart block requiring cardiopulmonary resuscitation. Pre- and postoperative creatinine values were available for patients undergoing 127 catheterizations; four patients with precatheterization renal failure were excluded from analysis. The average change in creatinine was 0.05 6 0.19 mg/dl. Two patients developed AKI as defined by pRIFLE criteria. Both patients were supported with ECMO, with one undergoing two catheterizations on the same day. No patients suffered a cerebrovascular accident or a catheterization-associated blood stream infection.
DISCUSSION
Our results demonstrate that 69% of unplanned postoperative cardiac catheterizations following congenital heart surgery were associated with changes in clinical management. Specifically, of 150 diagnostic or interventional catheterizations, 103 resulted in a transcatheter intervention, re-operation, or significant change in medical management (new medication, elective re-operation, or transition to palliative care). This study attempts to understand the diagnostic and therapeutic benefit of cardiac catheterization early after congenital heart surgery. While it is impossible to ascribe a causal relationship, we observed that unplanned cardiac catheterizations were associated with important interventions or changes in clinical management. Appropriately, there is increased attention to the rate of catheterization-related adverse events. There are several reports in the literature that characterize risks associated with catheterization [17,18,21–25], culminating in a multi-institutional derived method to adjust for case mix when comparing adverse events between institutions [26]. To develop our understanding of adjusted risk further, ongoing analyses must interpret risk in the context of potential diagnostic and therapeutic gains. In 31% of the catheterizations, there was not a direct change in management as measured by our primary end points, although more detailed analysis of impact on long-term clinical care was not studied.
Catheterization and Cardiovascular Interventions DOI 10.1002/ccd. Published on behalf of The Society for Cardiovascular Angiography and Interventions (SCAI).
Catheterization After Congenital Heart Surgery
Fig. 2. Mortality and catheterization by postoperative day. Each patient represented on the Y-axis has a horizontal line that represents length of hospital stay following cardiac surgery. Red lines are patients who died and blue lines those who survived to discharge. The hash marks represent postoperative day of catheterization. Hash marks associated with a ’C’ represents a catheterization that resulted in a change in the medical or surgical management.
In this study, mortality was similar compared to previous reports of outcomes following catheterization in the postoperative period. The 30-day survival and survival to discharge of 85% and 72%, respectively, are similar to that shown in the report by Zahn et al. [14]. As previously surmised, the mortality rate likely represents the severity of underlying disease in the patients who require unplanned postoperative catheterizations. The acuity of illness is reflected both by RACHS-1 scores and the number of interventions and re-operations required to address significant hemodynamic or anatomic abnormalities. Similar to previous studies [12,14], we demonstrated that interventional catheterizations in the early postoperative period can be performed safely. Interestingly, in our series, the median postoperative day for cardiac catheterization was 20 days. For cases that were associated with a clinical change as defined by our primary endpoint, the median was 19 days.
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Contrary to a previous report by Asoh [16] in which greater length of time to postoperative catheterization increased in-hospital mortality, postoperative day of catheterization was not associated with in-hospital mortality in this study. Contributing factors to delays in cardiac catheterization were not specifically studied. We surmise that important features associated with deferment of cardiac catheterization in the postoperative period are likely multifactorial. Factors such as delays in diagnosis or recognition, scheduling challenges, patient instability, and concern for procedural risks are likely to be chief components. However, our study suggests cardiac catheterization in the postoperative period yielded useful diagnostic information that may impact care in a meaningful way. Reducing the time to catheterization in the postoperative patient may produce important opportunities to improve patient care and decrease unnecessary consumption of costly resources. This especially applies for those patients whose anatomic abnormalities are not amenable to medical management, and for whom additional intensive care unit days may be detrimental. Although complications following cardiac catheterizations have been previously described, they were rare events in our experience. The most common complications were nonsustained arrhythmias, as previously reported [18]. AKI was only noted in two patients on mechanical circulatory support, though it is important to note that we excluded patients with pre-existing AKI as defined by pre-catheterization creatinine. Hemorrhage occurred only in two patients on mechanical circulatory support receiving systemic anticoagulation. Although inadequately powered to discern statistical significance, our findings suggest the risk for complications from cardiac catheterization may be higher in patients on mechanical support and/or receiving systemic anticoagulation. This is in contrast to previous reports that show catheterization of patients on mechanical support is both safe and feasible [12]. Limitations. This study is a retrospective review which carries limitations inherent to the study design. First, the generalizability of results from this singlecenter study may not directly apply to other institutions; however, the reported survival from this study is not significantly different from the previous published reports, inferring important commonalities in practice. Second, the primary and secondary outcomes were chosen to elaborate a risk:benefit discussion, but they do not capture more subtle clinical and procedural influences inherent to this evaluation. Third, the ability to use other diagnostic modalities such as echocardiography or other noninvasive imaging to obtain the same results in lieu of catheterization was not evaluated. Additionally, minor and moderate complications such
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as site hematomas and vascular occlusions/injury were not assessed. Finally, the study was neither designed nor powered to determine a statistically significant association between outcome and various subgroups, such as patients on mechanical support or with preexisting AKI. However, our study population did include patients with higher overall surgical complexity (RACHS-1 scores 3), which reflects the majority of our patient population. To be able to fully characterize the impact of catheterization in the postoperative period, a detailed understanding of preprocedure decision-making is necessary and would be possible in a prospective analysis. CONCLUSION
Cardiac catheterization in the postoperative period was frequently associated with changes in medical and surgical management in patients recovering from congenital heart surgery. Although AKI, cerebrovascular accidents, arrhythmia, infections, and hemorrhage are procedural safety concerns in the postoperative period, they occurred infrequently. We believe that strategies to improve utilization of cardiac catheterization in the postoperative period could positively impact clinical care and resource utilization. ACKNOWLEDGMENT
We acknowledge the work of Raymond Belise, Ph.D at Stanford University, who created the graphics for Figure 2. REFERENCES 1. Lock JE. The adult with congenital heart disease: cardiac catheterization as a therapeutic intervention. J Am Coll Cardiol 1991; 18:330–331. 2. Gatzoulis MA, Rigby ML, Redington AN. Interventional catheterization in paediatric cardiology. Eur Heart J 1995;16:1767– 1772. 3. Pihkala J, Nykanen D, Freedom RM, Benson LN. Interventional cardiac catheterization. Pediatr Clin North Am 1999;46:441– 464. 4. Andrews RE, Tulloh RMR. Interventional cardiac catheterisation in congenital heart disease. Arch Dis Child 2004;89:1168–1173. 5. Van Aerschot I, Boudjemline Y. Interventional cardiac catheterization in children. Arch Pediatr 2012;19:96–102. 6. Himmelstein A, Cournand A. Cardiac catheterization in the study of congenital cardiovascular anomalies: An evaluation. Am J Med 1952;12:349–356. 7. Waight DJ, Hijazi ZM. Pediatric interventional cardiology: The cardiologist’s role and relationship with pediatric cardiothoracic surgery. Adv Card Surg 2001;13:143–167.
8. Feltes TF, Bacha E, Beekman RH, et al. Indications for cardiac catheterization and intervention in pediatric cardiac disease a scientific statement from the American Heart Association. Circulation. 2011;123:2607–2652. 9. Hansen JH, Runge U, Uebing A, et al. Cardiac catheterization and interventional procedures as part of staged surgical palliation for hypoplastic left heart syndrome. Congenit Heart Dis 2012;7:565–574. 10. Simpson JM, Moore P, Teitel DF. Cardiac catheterization of low birth weight infants. Am J Cardiol 2001;87:1372–1377. 11. desJardins SE, Crowley DC, Beekman RH, Lloyd TR. Utility of cardiac catheterization in pediatric cardiac patients on ECMO. Catheter Cardiovasc Interv 1999;46:62–67. 12. Booth KL, Roth SJ, Perry SB, et al. Cardiac catheterization of patients supported by extracorporeal membrane oxygenation. J Am Coll Cardiol 2002;40:1681–1686. 13. Nykanen DG, Zahn EM. Transcatheter techniques in the management of perioperative vascular obstruction. Catheter Cardiovasc Interv 2005;66:573–579. 14. Zahn EM, Dobrolet NC, Nykanen DG, et al. Interventional catheterization performed in the early postoperative period after congenital heart surgery in children. J Am Coll Cardiol 2004;43: 1264–1269. 15. Ma M, Gauvreau K, Allan CK, Mayer Jr JE, Jenkins KJ. Causes of Death After Congenital Heart Surgery. Ann Thorac Surg 2007;83:1438–1445. 16. Asoh K, Hickey E, Dorostkar PC, et al. Outcomes of emergent cardiac catheterization following pediatric cardiac surgery. Catheter Cardiovasc Interv 2009;73:933–940. 17. Zeevi B, Berant M, Fogelman R, Galit B-M, Blieden LC. Acute complications in the current era of therapeutic cardiac catheterization for congenital heart disease. Cardiol Young 1999;9:266– 272. 18. Vitiello R, McCrindle BW, Nykanen D, Freedom RM, Benson LN. Complications associated with pediatric cardiac catheterization. J Am Coll Cardiol 1998;32:1433–1440. 19. Jenkins KJ, Gauvreau K, Newburger JW, et al. Consensus-based method for risk adjustment for surgery for congenital heart disease. J Thorac Cardiovasc Surg 2002;123:110–118. 20. Akcan-Arikan A, Zappitelli M, Loftis LL, et al. Modified RIFLE criteria in critically ill children with acute kidney injury. Kidney Int 2007;71:1028–1035. 21. Bergersen L, Gauvreau K, Jenkins KJ, Lock JE. Adverse Event Rates in Congenital Cardiac Catheterization: A New Understanding of Risks. Congenit Heart Dis 2008;3:90–105. 22. Agnoletti G, Bonnet C, Boudjemline Y, et al. Complications of paediatric interventional catheterisation: An analysis of risk factors. Cardiol Young 2005;15:402–408. 23. Mehta PA, Cunningham CK, Colella CB, Alferis G, Weiner LB. Risk factors for sternal wound and other infections in pediatric cardiac surgery patients. Pediatr Infect Dis J 2000;19:1000– 1004. 24. Phillips BL, Cabalka AK, Hagler DJ, Bailey KR, Cetta F. Procedural Complications During Congenital Cardiac Catheterization. Congenit Heart Dis 2010;5:118–123. 25. Bergersen L, Marshall A, Gauvreau K, et al. Adverse event rates in congenital cardiac catheterization—A multi-center experience. Catheter Cardiovasc Interv 2010;75:389–400. 26. Bergersen L, Gauvreau K, Foerster SR, et al. Catheterization for congenital heart disease adjustment for risk method (CHARM). JACC Cardiovasc Interv 2011;4:1037–1046.
Catheterization and Cardiovascular Interventions DOI 10.1002/ccd. Published on behalf of The Society for Cardiovascular Angiography and Interventions (SCAI).
Outcomes Following Cardiac Catheterization After Congenital Heart Surgery Stephanie L. Siehr,1 MD, Mary Hunt Martin,2 MD, David Axelrod,1 MD, Bradley Efron,3 PhD, Lynn Peng,1 MD, Stephen J. Roth,1 MD, MPH, Stanton Perry,1 MD, and Andrew Y. Shin,1* MD Objectives: Describe outcomes following unplanned cardiac catheterization after congenital heart surgery. Background: Utility of cardiac catheterization following congenital heart surgery is relatively understudied. Methods: Retrospective study examining demographics, indications, and outcomes of unplanned cardiac catheterization after congenital heart surgery at a single institution. Results: Between October 2004 and April 2011, 120 patients underwent 150 unplanned postoperative cardiac catheterizations. Median day of catheterization was postoperative day 20 (range 1–269 days). Survival 30 days postcatheterization was 85%; overall survival to hospital discharge was 72%. Indications for catheterization: 63 for hemodynamic evaluation, 46 for likely intervention, and 41 for assessment of surgical repair. Of the 150 hemodynamic/interventional catheterizations, 103 (69%) were associated with a change in clinical management: 59 trans-catheter interventions, 22 re-operations, 11 changes in medication, six changes in surgical plan, and five withdrawals of support. Complications included hemorrhage in two patients, supraventricular tachycardia in two patients, and transient complete heart block requiring cardiopulmonary resuscitation in one patient. Conclusions: Cardiac catheterization following congenital heart surgery may enable important diagnostic and therapeutic changes in clinical and surgical management. Complications were rare. VC 2014 Wiley Periodicals, Inc. Key words: congenital heart disease; pediatrics; pediatric intervention; complications; pediatric catheterization/intervention
INTRODUCTION
Since the beginning of the surgical era in congenital heart disease, there have been substantial advances in the role of cardiac catheterization [1–5]. For presurgical assessment, diagnostic catheterization often plays an invaluable role [4,6–9]. However, there is little published data assessing the value of diagnostic or interventional cardiac catheterization in the postoperative period following congenital heart surgery. Previous studies report mixed results concerning the benefits and risks of cardiac catheterization in the vulnerable postoperative period [10–16]. Complications such as arrhythmias, contrast-related acute kidney injury (AKI), and death have been observed [16–18], but subsequent reports describe more favorable outcomes with improved survival using a multidisciplinary team approach [14]. These reports are limited by small sample size, thus reducing their impact and applicability. In a recent consensus statement by the American Heart Association, the evidence regarding the utility of cardiac catheterization in the early postoperative period C 2014 Wiley Periodicals, Inc. V
1
Department of Pediatrics, Cardiovascular Institute, Stanford University School of Medicine, Palo Alto, California 2 Department of Pediatrics, Division of Pediatric Cardiology, Primary Children’s Medical Center, Salt Lake City, Utah 3 Department of Health Research and Policy, Division of Biostatistics, Stanford University Medical Center, Palo Alto, California Conflict of interest: Nothing to report. *Correspondence to: Andrew Y. Shin; Clinical Assistant Professor, Associate Section Chief, Cardiovascular Intensive Care, Lucile Packard Children’s Hospital, Stanford University Medical Center, 750 Welch Rd, Ste 305, Palo Alto, CA 94304. E-mail: drewshin@ stanford.edu Received 12 September 2013; Revision accepted 12 March 2014 DOI: 10.1002/ccd.25490 Published online 21 March 2014 in Wiley Online Library (wileyonlinelibrary.com)
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was determined to be conflicting (Class II recommendation) and sparse (level of evidence C) [8]. The goal of this study was to describe the outcomes following unplanned cardiac catheterization in the entire postoperative period following congenital heart surgery. We hypothesized that cardiac catheterization influences subsequent clinical management with a low adverse event rate.
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on if an intervention was performed during cardiac catheterization. When possible, trans-catheter interventions were categorized as interventions to augment pulmonary blood flow (dilation of and/or stent implantation in existing shunts, conduits, or native aortopulmonary collateral arteries) or to reduce pulmonary blood flow (device closures of existing shunts, conduits, aortopulmonary collateral arteries, or native outflow tracts). Clinical Outcomes
MATERIALS AND METHODS Study Design and Patients
This is a retrospective case series examining outcomes following unplanned cardiac catheterization during the postoperative period after congenital heart surgery at a single, tertiary care, pediatric hospital between October 2004 and April 2011 (current era of computer-based data collection). Patients were included if they underwent a cardiac catheterization at any time prior to hospital discharge. Planned cardiac catheterizations, if specifically stated as part of postoperative care in pre-operative or immediate postoperative clinical documentation, were excluded. Central line placement or removal, diaphragm or valve fluoroscopy, and pericardiocentesis performed in the cardiac catheterization lab without an associated hemodynamic or interventional procedure were excluded. Routine surveillance catheterizations and biopsies following cardiac transplantation were also excluded. The cardiac catheterization lab is located in the adjoining adult hospital, which is accessible via a connecting hallway from the children’s hospital. The study protocol was approved by the Institutional Review Board of Stanford University Medical Center. Demographic and Clinical Data Demographic variables, cardiac anatomy, and clinical data were collected from clinical notes. Anatomical and surgical characteristics were catalogued as single ventricle palliation or biventricular repair and assigned a case complexity score utilizing the Risk Adjustment in Congenital Heart Surgery (RACHS-1) system [19]. Contrast dose and fluoroscopy time were collected as safety markers. Given the expected paucity of documentation regarding preprocedure decision making, catheterization was categorized based on the available information into assessment of surgical repair, likely intervention, or hemodynamic study. Trans-catheter Interventions Catheterizations were catalogued as interventional or noninterventional (hemodynamic) post hoc depending
This study sought to determine whether results of the unplanned cardiac catheterization were associated with a significant change in clinical management. The primary end point was a composite outcome including: (1) unplanned early re-operation following cardiac catheterization, (2) trans-catheter intervention, (3) intra-catheterization diagnosis that led to later reoperation or transition to palliative care, or (4) administration of a new pharmacologic agent following catheterization specifically to treat circulatory abnormalities (e.g., pulmonary over-circulation, preexisting thrombus, or pulmonary hypertension). Outcome was determined by chart review, and primary end point was assigned by a committee of pediatric cardiac intensivists and interventionalists. The first 30 patients were reviewed by two investigators separately and confirmed 100% internal validity. The remainder of patients were reviewed after data collection and independently when concerns were raised by the primary investigators. Patients who received additional therapies as a result of complications from cardiac catheterization (e.g., mechanical pacing, heparin) were not considered reaching the primary end point. Secondary end points included death, cerebrovascular accident, major hemorrhage (blood loss leading to clinical instability), arrhythmia during catheterization requiring treatment (pharmacologic, cardiopulmonary support, or mechanical pacing), catheterization-associated blood stream infection (positive blood culture within 72 hours following catheterization), and/or AKI within 36 hours following cardiac catheterization. AKI was defined utilizing the pediatric modified RIFLE (pRIFLE) criteria [20]. Statistical Analysis Categorical variables were compared using a chisquared test. Numerical continuous variables were compared using a paired t-test. A Cox proportional hazards analysis was performed to test the effects of age, RACHS-1 score, and time in days from baseline to catheterization on the response "time from last catheterization to death", with discharge as the censoring variable.
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Fig. 1. Postoperative cardiac catheterizations.
RESULTS Baseline Characteristics There were 3218 consecutive pediatric and adult patients who underwent congenital heart surgery at our center between October 2004 and April 2011. One hundred fifty unplanned cardiac catheterizations for diagnostic or interventional purposes were performed in 120 patients during their postoperative hospitalization. Figure 1 provides the reason for cardiac catheterization. Median day of catheterization for the entire population was postoperative day 20 (range 1–269 days). Of the 150 catheterizations, 94 (63%) occurred in the early postoperative period within 30 days of the operation. Baseline demographic, anatomic, surgical and catheterization characteristics of the entire study population divided into early (within 30 days of operation) and late (greater than 30 days after operation) groups are summarized in Table I. The early group had more patients on mechanical circulatory support, which was not statistically significant, and shorter intensive care unit length of stay (P ¼< 0.01). Median age at surgery for the entire cohort was 0.35 years (range 0.01–29 years); 74 patients were undergoing biventricular repair and 46 patients single ventricle palliation. The median fluoroscopy time for the entire cohort was 30 (1.5–190) minutes; median contrast volume was 5.1 (0–21.2) ml/kg. The most common diagnosis was tetralogy of Fallot (20%), and the majority of patients had a RACHS-1 score 3. Six patients (seven catheterizations) were receiving extracorporeal membrane oxygenation (ECMO) support and two patients were receiving left ventricular assist device support with a Berlin Heart EXCOR at the time of catheterization. Primary Endpoint
Outcomes following 103 of 150 (69%) diagnostic or interventional catheterizations were as follows: 48
patients underwent 59 catheterizations during which there was at least one trans-catheter intervention, 31 patients underwent an early re-operation, 11 patients received a new pharmacologic agent, six patients had a new operative plan and/or elective re-operation in the future, and five patients were transitioned to palliative care (Table II). Nine patients who underwent a transcatheter intervention also had an early re-operation. There was no associated change in clinical management following 47 of 150 (31%) of diagnostic or interventional catheterizations. The median postoperative day of catheterization that was associated with any clinical change as described above was 19 days (1– 269). Within 30 days of the operation, 69 of 95 (73%) catheterizations were associated with the following outcomes: 41 trans-catheter intervention, 17 immediate reoperations, five new pharmacologic agents, three new operative plans and/or elective re-operations in the future, and three transitions to palliative care (Table II). Trans-catheter intervention. Of the 59 patients who required a trans-catheter intervention, the most common indication for intervention was manipulation of pulmonary blood flow (Table II). Device closure of residual septal defects and fenestrations made up a small minority of cases. There were four interventions in patients on mechanical circulatory support: two left atrial decompressions, one superior vena cava stent, and one coronary stent. Re-operation. Following catheterization, early reoperation was performed in 31 patients (Table II); 16 patients underwent re-operation within 24 hours of catheterization. The median postoperative day of catheterization that resulted in an early re-operation, excluding cavopulmonary anastomosis, was 11 days (1–62 days). The most common indication for re-operation was augmentation of pulmonary blood flow. Impact on clinical care. Postoperative catheterization was associated with a change in medical management in 22 patients (Table II). New pharmacological
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TABLE I. Patient Characteristics
Demographics Age – years, median (range) Weight – kg, median (range) Sex Type of palliation/repair Postoperative Course Postoperative day of catheterization – days, median (range) Mechanical circulatory support at catheterization – # (percentage) Fluoroscopy time – min, median (range) Contrast dose – ml/kg, median (range) CVICU length of stay– days, median (range) Ventilator duration – days, median (range) Diagnosis Tetralogy of Fallot Atrioventricular septal defect Hypoplastic left heart d-TGA Truncus arteriosus Coarctation of the aorta Aortic stenosis Double outlet right ventricle Tricuspid atresia Double inlet left ventricle l-TGA Double outlet left ventricle Total anomalous pulmonary venous return Pulmonary atresia/ intact ventricular septum Ebstein’s anomaly Shone’s complex Ventricular septal defect Interrupted aortic arch Patent ductus arteriosus Pulmonary stenosis RACHS-1 score 1 2 3 4 5 6
Early (30 days) N ¼ 94 (63%)
Late (>30 days) N ¼ 56 (37%)
0.5 (0.01–29) 6.1 (2.3–109) 45 F, 49 M 32 Single ventricle, 62 Biventricular
0.2 (0.01–21) 4.1 (0.9–49) 29 F, 27 M 28 Single ventricle, 28 Biventricular
13.5 (1–29)* 7 (7%) 25 (2.8–190) 5.1 (0–21.2) 25 (2–151)* 14.5 (1–151)*
54.5 (32–269) 1 (2%) 28.5 (1.5–121) 5.1 (0–19.3) 55.5 (4–190) 15 (1–190)
20 (21%) 12 (13%) 11 (12%) 9 (10%) 7 (7%) 6 (6%) 5 (5%) 5 (5%) 5 (5%) 3 (3%) 3 (3%) 2 (2%) 2 (2%) 1 (1%) 1 (1%) 1 (1%) 1 (1%) – – –
7 (7%) 9 (10%) 9 (10%) 4 (4%) 2 (4%) 1 (2%) 5 (5%) 8 (9%) – 3 (5%) 1 (2%) – – 3 (5%) – – – 2 (4%) 1 (2%) 1 (2%)
– 21 (22%) 48 (51%) 22 (23%) – 3 (3%)
2 (4%) 7 (13%) 25 (45%) 12 (21%) – 10 (18%)
Abbreviations: d-TGA, dextro- transposition of the great arteries; l-TGA, levo- transposition of the great arteries; RACHS, risk adjustment in congenital heart surgery. *- P value < 0:05
agents to address circulatory abnormalies were most commonly systemic or pulmonary vasodilators. Six patients had a new operative plan or elective reoperation as a direct result of findings from the catheterization: one patient had severe pulmonary artery hypoplasia delaying biventricular repair; one had important pulmonary vein stenosis delaying cavopulmonary anastomosis; one had a restrictive bulboventricular foramen influencing timing of subsequent palliation; one had pulmonary hypertension prohibiting cavopulmonary anastomosis; one was diagnosed with partial anomalous pulmonary venous return prompting
elective repair; one had right coronary artery stenosis prompting elective repair. Five patients had their medical care re-directed towards palliative care based, in part, on the findings from their catheterization. Secondary Endpoints Mortality. Thirty-day survival postcatheterization was 85% and overall survival to hospital discharge was 72%. Of the patients who did not survive, 14 had an intervention; three had a re-operation, three had a change in medication, one had a new diagnosis at
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TABLE II.
Primary Outcome: Change in Management
Trans-catheter Intervention Increase PBF - Dilation/stent of pulmonary artery/aortopulmonary collateral - Dilation/stent of shunt/conduit Decrease PBF - Coil - Aortopulmonary collateral - Device closure of shunt/conduit - Device closure of pulmonary artery Dilation/stent - Systemic vein Coil occlusion - Veno-venous collateral Decompression - Left atrium Angioplasty - Coronary artery Device closure - Ventricular septal defect Device closure - Azygous/left superior vena cava Device closure - Atrial septal defect Dilation/stent - Aortic arch Device closure - Fenestration Dilation/stent - Fenestration
New Anatomic Diagnosis Elective re-operation Palliative care
Total # (30 days) 20 (12) 16 (11) 4 (1) 14 (7) 8 (5) 3 3 (2) 6 (5) 5 (5) 4 (3) 2 (2) 2 (2) 2 (1) 1 (1) 1 (1) 1 (1) 1 (1)
6 (3) 5 (3)
Reoperation
Total # (30 days)
Shunt/conduit placement Cavopulmonary anastomosis VSD closure Aortic arch reconstruction Revision of unifocalization Shunt takedown/clip Pulmonary vein repair Coronary artery repair Pulmonary artery band Modified Konno RVOT augmentation LVOT myomectomy Glenn takedown Aortopulmonary collateral ligation
6 (4) 6 (1) 4 (3) 2 (2) 2 (2) 2 (1) 2 (1) 1 (1) 1 (1) 1 (1) 1 1 1 1
Change in Medication Addition of milrinone Addition of sildenafil Increase in furosemide Addition of oxygen Addition of nesiritide Addition of aspirin Addition of tissue plasminogen activator
2 (1) 2 (1) 2 (1) 2 1 (1) 1 (1) 1
Abbreviations: PBF, pulmonary blood flow; VSD, ventricular septal defect; RVOT, right ventricular outflow tract; LVOT, left ventricular outflow tract.
catheterization resulting in change in surgical plan, and four had support withdrawn. Eight patients who died did not have a change in management following catheterization as defined by the study. Of the patients who died, the median postoperative day of catheterization was 26 (2–108 days), which was not significantly different from the patients who survived to discharge [Fig. 2]. Complications. Single instances of pulmonary hemorrhage and peritoneal hemorrhage leading to clinical instability occurred in two (1%) patients, both on mechanical circulatory support receiving systemic anticoagulation. Support was withdrawn on both patients within 24 hours of catheterization. Three patients (2%) experienced a significant arrhythmia: two had supraventricular tachycardia requiring electrical cardioversion; one had transient complete heart block requiring cardiopulmonary resuscitation. Pre- and postoperative creatinine values were available for patients undergoing 127 catheterizations; four patients with precatheterization renal failure were excluded from analysis. The average change in creatinine was 0.05 6 0.19 mg/dl. Two patients developed AKI as defined by pRIFLE criteria. Both patients were supported with ECMO, with one undergoing two catheterizations on the same day. No patients suffered a cerebrovascular accident or a catheterization-associated blood stream infection.
DISCUSSION
Our results demonstrate that 69% of unplanned postoperative cardiac catheterizations following congenital heart surgery were associated with changes in clinical management. Specifically, of 150 diagnostic or interventional catheterizations, 103 resulted in a transcatheter intervention, re-operation, or significant change in medical management (new medication, elective re-operation, or transition to palliative care). This study attempts to understand the diagnostic and therapeutic benefit of cardiac catheterization early after congenital heart surgery. While it is impossible to ascribe a causal relationship, we observed that unplanned cardiac catheterizations were associated with important interventions or changes in clinical management. Appropriately, there is increased attention to the rate of catheterization-related adverse events. There are several reports in the literature that characterize risks associated with catheterization [17,18,21–25], culminating in a multi-institutional derived method to adjust for case mix when comparing adverse events between institutions [26]. To develop our understanding of adjusted risk further, ongoing analyses must interpret risk in the context of potential diagnostic and therapeutic gains. In 31% of the catheterizations, there was not a direct change in management as measured by our primary end points, although more detailed analysis of impact on long-term clinical care was not studied.
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Catheterization After Congenital Heart Surgery
Fig. 2. Mortality and catheterization by postoperative day. Each patient represented on the Y-axis has a horizontal line that represents length of hospital stay following cardiac surgery. Red lines are patients who died and blue lines those who survived to discharge. The hash marks represent postoperative day of catheterization. Hash marks associated with a ’C’ represents a catheterization that resulted in a change in the medical or surgical management.
In this study, mortality was similar compared to previous reports of outcomes following catheterization in the postoperative period. The 30-day survival and survival to discharge of 85% and 72%, respectively, are similar to that shown in the report by Zahn et al. [14]. As previously surmised, the mortality rate likely represents the severity of underlying disease in the patients who require unplanned postoperative catheterizations. The acuity of illness is reflected both by RACHS-1 scores and the number of interventions and re-operations required to address significant hemodynamic or anatomic abnormalities. Similar to previous studies [12,14], we demonstrated that interventional catheterizations in the early postoperative period can be performed safely. Interestingly, in our series, the median postoperative day for cardiac catheterization was 20 days. For cases that were associated with a clinical change as defined by our primary endpoint, the median was 19 days.
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Contrary to a previous report by Asoh [16] in which greater length of time to postoperative catheterization increased in-hospital mortality, postoperative day of catheterization was not associated with in-hospital mortality in this study. Contributing factors to delays in cardiac catheterization were not specifically studied. We surmise that important features associated with deferment of cardiac catheterization in the postoperative period are likely multifactorial. Factors such as delays in diagnosis or recognition, scheduling challenges, patient instability, and concern for procedural risks are likely to be chief components. However, our study suggests cardiac catheterization in the postoperative period yielded useful diagnostic information that may impact care in a meaningful way. Reducing the time to catheterization in the postoperative patient may produce important opportunities to improve patient care and decrease unnecessary consumption of costly resources. This especially applies for those patients whose anatomic abnormalities are not amenable to medical management, and for whom additional intensive care unit days may be detrimental. Although complications following cardiac catheterizations have been previously described, they were rare events in our experience. The most common complications were nonsustained arrhythmias, as previously reported [18]. AKI was only noted in two patients on mechanical circulatory support, though it is important to note that we excluded patients with pre-existing AKI as defined by pre-catheterization creatinine. Hemorrhage occurred only in two patients on mechanical circulatory support receiving systemic anticoagulation. Although inadequately powered to discern statistical significance, our findings suggest the risk for complications from cardiac catheterization may be higher in patients on mechanical support and/or receiving systemic anticoagulation. This is in contrast to previous reports that show catheterization of patients on mechanical support is both safe and feasible [12]. Limitations. This study is a retrospective review which carries limitations inherent to the study design. First, the generalizability of results from this singlecenter study may not directly apply to other institutions; however, the reported survival from this study is not significantly different from the previous published reports, inferring important commonalities in practice. Second, the primary and secondary outcomes were chosen to elaborate a risk:benefit discussion, but they do not capture more subtle clinical and procedural influences inherent to this evaluation. Third, the ability to use other diagnostic modalities such as echocardiography or other noninvasive imaging to obtain the same results in lieu of catheterization was not evaluated. Additionally, minor and moderate complications such
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as site hematomas and vascular occlusions/injury were not assessed. Finally, the study was neither designed nor powered to determine a statistically significant association between outcome and various subgroups, such as patients on mechanical support or with preexisting AKI. However, our study population did include patients with higher overall surgical complexity (RACHS-1 scores 3), which reflects the majority of our patient population. To be able to fully characterize the impact of catheterization in the postoperative period, a detailed understanding of preprocedure decision-making is necessary and would be possible in a prospective analysis. CONCLUSION
Cardiac catheterization in the postoperative period was frequently associated with changes in medical and surgical management in patients recovering from congenital heart surgery. Although AKI, cerebrovascular accidents, arrhythmia, infections, and hemorrhage are procedural safety concerns in the postoperative period, they occurred infrequently. We believe that strategies to improve utilization of cardiac catheterization in the postoperative period could positively impact clinical care and resource utilization. ACKNOWLEDGMENT
We acknowledge the work of Raymond Belise, Ph.D at Stanford University, who created the graphics for Figure 2. REFERENCES 1. Lock JE. The adult with congenital heart disease: cardiac catheterization as a therapeutic intervention. J Am Coll Cardiol 1991; 18:330–331. 2. Gatzoulis MA, Rigby ML, Redington AN. Interventional catheterization in paediatric cardiology. Eur Heart J 1995;16:1767– 1772. 3. Pihkala J, Nykanen D, Freedom RM, Benson LN. Interventional cardiac catheterization. Pediatr Clin North Am 1999;46:441– 464. 4. Andrews RE, Tulloh RMR. Interventional cardiac catheterisation in congenital heart disease. Arch Dis Child 2004;89:1168–1173. 5. Van Aerschot I, Boudjemline Y. Interventional cardiac catheterization in children. Arch Pediatr 2012;19:96–102. 6. Himmelstein A, Cournand A. Cardiac catheterization in the study of congenital cardiovascular anomalies: An evaluation. Am J Med 1952;12:349–356. 7. Waight DJ, Hijazi ZM. Pediatric interventional cardiology: The cardiologist’s role and relationship with pediatric cardiothoracic surgery. Adv Card Surg 2001;13:143–167.
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