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J Thorac Cardiovasc Surg 2003;126:1397-1403
© 2003 The American Association for Thoracic Surgery
Surgery for congenital heart disease |
c Department of Neurology, Children's Hospital, Boston, Mass, USA
a Department of Cardiology, Children's Hospital, Boston, Mass, USA
b Department of Medicine, Children's Hospital, Boston, Mass, USA
d Department of Cardiovascular Surgery, Children's Hospital, Boston, Mass, USA
e Clinical Research Program, Children's Hospital, Boston, Mass, USA
f Department of Pediatrics, Harvard Medical School, Boston, Mass, USA
g Department of Neurology, Harvard Medical School, Boston, Mass, USA
h Department of Surgery, Harvard Medical School, Boston, Mass, USA
i Department of Biostatistics, Harvard School of Public Health, Boston, Mass, USA
Received for publication June 12, 2002; revisions received December 10, 2002; revisions received May 28, 2003; accepted for publication June 3, 2003.
* Address for reprints: David C. Bellinger, PhD, MSc, Neuroepidemiology Unit, Farley Basement 127, Children's Hospital, 300 Longwood Ave, Boston, MA 02115, USA
david.bellinger{at}tch.harvard.edu
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Abstract |
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METHODS: From 1988 to 1992, in a single-center trial, infants with D-transposition of the great arteries underwent the arterial switch operation after random assignment to circulatory arrest or low-flow bypass. The alpha-stat method was used, and hematocrit on bypass was maintained at 20%. Developmental, neurologic, and speech outcomes were assessed at 8 years of age in 155 of 160 eligible children (97%). Outcomes selected for analysis were Full-Scale, Verbal, and Performance IQ, Reading and Mathematics Composite, time to complete the Grooved Pegboard (dominant hand), and the Mayo Test for Apraxia.
RESULTS: Nonparametric regression and piecewise linear models indicated that neurodevelopmental outcomes were generally not adversely affected unless the duration of circulatory arrest exceeded a threshold of 41 minutes (95% 1-sided lower confidence limit of 32 minutes).
CONCLUSIONS: We found that the effect of duration of total circulatory arrest on later neurodevelopmental outcomes is nonlinear, with little influence at shorter durations and with steadily worsening outcomes after longer durations of circulatory arrest. Because the effects of duration of circulatory arrest may vary according to diagnosis, age at surgery, and other bypass and perioperative variables, this study cannot ascertain a universally "safe" duration of total circulatory arrest.
| See related article on page 1385.
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Considerable research has been conducted to determine the duration of total circulatory arrest (CA) that infants undergoing cardiac surgery can tolerate without suffering increased risk of irreversible structural or functional brain damage. The weight of evidence suggests that the maximum "safe" duration is 39 to 65 minutes,1,2 although this estimate is based on studies that are heterogeneous in many respects, including the patient population (ie, heart defect), sample size, length of follow-up, end points assessed, and key aspects of surgical management. Because CA has technical advantages from a surgical standpoint and is necessary to repair some complex congenital heart lesions, refinement of this estimate might help to maximize patients' late central nervous system outcomes. Among the challenges in doing so is the number of other factors that affect neurodevelopmental outcomes, including regional brain temperature during CA, rate of cooling, cerebral blood flow and distribution during cooling, arterial blood pressure during cooling and reperfusion, pH and hematocrit management strategies, and postoperative care.2 To render these aspects of surgical management comparable between treatment groups, we began a clinical trial in which children with D-transposition of the great arteries (D-TGA) undergoing the arterial switch operation were randomized to a vital organ support method consisting of deep hypothermia with either predominantly CA or predominantly low-flow (LF) cardiopulmonary bypass. The results of assessments conducted in the perioperative period and at ages 1 and 4 years consistently indicated poorer outcomes among children assigned to CA than to LF.3-5
In a companion article,6 we presented the results of intention-to-treat analyses comparing the neurodevelopmental outcomes of the CA and LF treatment groups at 8 years of age. In this article, we report additional analyses in which we attempted to identify, in more quantitative terms, the functional form of the association between CA duration and key neurodevelopmental outcomes.
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Methods |
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For analyses looking at the associations with CA duration, continuous outcomes considered were Full-Scale, Verbal, and Performance IQ from the Wechsler Intelligence Scale for Children—Third Edition,7 Reading and Mathematics Composite score from the Wechsler Individual Achievement Test,8 time to complete the Grooved Pegboard9 (dominant hand), and the Mayo Test for Apraxia of Speech and Oral Apraxia—Children's Battery (selected items).10 The Mayo Test measures the motor planning portion of speech production. These end points were selected from among the large number assessed in the full neurodevelopmental evaluation. The selection was based either on our finding, in intention-to-treat analyses, that treatment group mean scores differed significantly (ie, Grooved Pegboard, Mayo Test for Apraxia) or based on the importance of the outcome (ie, IQ, academic achievement). We sought to determine the relationship between CA duration and neurodevelopmental test scores measured on a continuous scale. In addition, 2 important binary outcome variables were also considered (presence of apraxia diagnosis and presence of possibly or definitely abnormal overall neurologic examination findings).
Statistical analysis
Treatment group differences were evaluated by means of intention-to-treat analysis. Analyses assessing the effects of duration of CA as a continuous variable on major continuous outcomes used linear regression and generalized additive models.11,12 Generalized additive models are methods of nonparametric regression smoothing that allow for estimation of P values for any effect of duration of CA on outcome, as well as P values for the departure from linearity or piecewise linearity of effect. Piecewise linear (cut-point, or broken stick) regression models were used to estimate potential thresholds in the effect of duration of CA. Confidence intervals for cut-points were based on inversion of likelihood ratio tests.13 A likelihood ratio test showed no statistical evidence for heterogeneity in the cut-points across the multiple outcomes. To estimate a combined threshold across multiple outcomes, we performed a multivariate analysis using maximum likelihood with an arbitrary covariance matrix. All likelihood maximizations and likelihood ratio tests searched over a grid of duration of CA in units of 0.1 minute. Given the precision of our CA durations (to the nearest minute), we report the estimated cut-points and confidence limits to the nearest integer minute. Higher-order polynomial (eg, quadratic) regression models were also considered but did not fit the data better than either generalized additive models or piecewise linear models.
All comparisons were adjusted for diagnosis (intact ventricular septum [IVS] versus VSD) and family social class (Hollingshead Four-Factor Index of Social Class, unpublished manuscript). We also assessed potential interactions between diagnosis and duration of CA. For the generalized additive model and cut-point regression analyses, we used the average Reading Composite and Mathematics Composite scores, because the models for these outcomes considered individually were so similar. For the time to complete the Grooved Pegboard, proportional hazards regression was used to compare treatment groups. For the generalized additive model and cut-point regression analyses, the natural logarithm of the time to complete the Grooved Pegboard was used because this transformation yielded scores that were approximately normally distributed.
Analyses assessing the effects of duration of CA as a continuous variable on binary outcomes used logistic regression adjusting for diagnosis. Fisher exact tests were used to compare binomial proportions. All P values are 2-sided. Because we wished to determine the minimum duration of CA at which adverse effects could be detected under the conditions particular to the era of our study, we report 1-sided 95% lower confidence limits for cut-points. These were calculated as the lower limits of 2-sided 90% confidence intervals.
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Results |
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Academic achievement
Treatment groups did not differ significantly on the Reading and Mathematics Composite scores. The average of the Reading and Mathematics Composite scores was not significantly related to duration of CA (P = .26, Figure 1, B) and showed no evidence for departure from linearity (P = .99).
Fine motor function
Children assigned to CA tended to take longer than the children assigned to LF to complete the Grooved Pegboard for the dominant hand (P = .06, Table 1). Longer duration of CA was associated with longer time to complete (P = .01, Figure 1, C), and completion times showed a significant departure from linearity (P = .02).
Speech production
Children assigned to CA did significantly worse than children in the LF group on the Mayo Test for Apraxia of Speech and Oral Apraxia (P = .002, Table 1). Longer duration of CA was significantly associated with worse scores (P < .001, Figure 1, D), and the Mayo Test for Apraxia showed a significant departure from linearity (P = .002).
Determination of circulatory arrest thresholds
Among the 6 outcome variables, significance or tendency toward departures from linearity was observed for Full-Scale IQ (P = .08), Performance IQ (P = .08), Grooved Pegboard (P = .02), and the Mayo Test for Apraxia of Speech and Oral Apraxia (P = .002). We explored the potential threshold effects of CA duration on these outcomes using piecewise linear regression models to determine the best single cut-point beyond which scores declined. For example, for Full-Scale IQ scores a cut-point of 42 minutes was estimated (1-sided 95% lower confidence limit of 26 minutes, Table 2).
The linear effect of CA duration on Full-Scale IQ was quite flat (not significantly different from zero) for duration of CA less than 42 minutes but significantly negative beyond 42 minutes.
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To explore these models further, we fit separate models for these outcome variables using a common cut-point of 41 minutes, and we compared the slopes of duration of CA before and after this cut-point (Table 3). As this common cut-point was estimated from our data, we view these analyses as exploratory in nature. For each of the 6 outcome variables, we found no significant association between duration of CA and outcome for durations of less than 41 minutes. However, we found significant associations between duration of CA and outcome for durations of more than 41 minutes for Full-Scale IQ (P = .006), Verbal IQ (P = .03), Performance IQ (P = .009), Grooved Pegboard (P = .04), and Mayo Test of Apraxia (P < .001). In no case did nonparametric regression smoothing or higher-order polynomial regression models find significant departures from the piecewise linear model. In these cut-point models using duration of CA and adjusting for diagnosis and family social class, we found no statistically significant effects of total support time on outcomes.
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Binary outcomes
Adjusting for diagnosis, duration of CA was significantly associated with presence of apraxia diagnosis (P = .02, Figure 2,
A) but not with possibly or definitely abnormal overall neurologic examination findings (P = .40, Figure 2, B). As seen in Figure 2, A, the risk of apraxia diagnosis begins to increase at approximately 30 to 40 minutes of CA, consistent with the cut-point analyses for the continuous outcomes.
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Discussion |
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The correlation/linear regression methods used in previous studies,14-18 which force a linear fit to the relationship between CA and neurodevelopment, are problematic if a threshold exists below which duration of CA is not related to outcome. The overall slope or correlation is a weighted average of the flat slope at CA durations below the threshold and the slope that describes the relationship at CA durations that exceed the threshold. The latter slope is thus necessarily equal to or greater than the slope calculated for the entire range of CA duration under the assumption of linearity. Our use of nonparametric regression methods thus provided an opportunity to identify a threshold or cut-point in this association.
On the basis of previous reports,1-5 some groups undertaking repair of congenital heart anomalies have attempted to avoid any use of CA. The present study suggests that it may not be necessary to take special measures to avoid deep hypothermic CA periods of shorter duration, and cardiovascular surgeons should balance any technical advantages of the various perfusion techniques with their potential risks on an individual basis. Innovative ancillary methods for cerebral support have been introduced by many groups as alternatives to deep hypothermic CA. These methods, such as retrograde cerebral perfusion, are hypothesized to provide improved and homogeneous cerebral protection relative to deep hypothermic CA. The efficacies of these techniques should be tested in randomized, controlled trials, however.
Our analyses should be interpreted in light of several limitations. Our modeling of the effects of duration of total CA in this trial, including delineation of cut-points beyond which neurodevelopmental scores declined, is specific to the era in which surgery was conducted at our institution,3 when our cardiopulmonary bypass techniques included hemodilution to a hematocrit value of 20%, the alpha-stat strategy of acid-base management,19 absence of arterial filtration, and hardware that would be considered outmoded today. Postoperative events and length of stay can also affect later neurodevelopmental outcome. In the era of our study, postoperative care used techniques including the routine use of high-dose fentanyl and prolonged neuromuscular blockade, which are used less frequently currently. Thus, as a better understanding is achieved of the contributions of these other factors to neurodevelopmental outcomes, we might learn that durations of CA longer than those suggested in our models can be tolerated. All children in our study had some period of CA; thus, we cannot assess the benefit of a strategy that completely circumvents its use. Furthermore, we studied a very homogeneous group of children with D-TGA from a single institution. Because diagnosis can affect both cognitive outcome and surgical conduct, the results of these analyses may not be generalizable to a population with mixed diagnoses or age at surgery beyond infancy. Indeed, the technique of deep hypothermic CA is now used with much greater frequency than it was 15 years ago by surgeons repairing adults with acquired heart disease such as ascending and arch aortic aneurysms; the effects of CA should be studied further in older age groups and other diagnostic groups.
In summary, we found that the effect of duration of total CA on later neurodevelopmental outcomes is nonlinear, with little influence at shorter durations and with steadily worsening outcomes after longer durations of CA. This study cannot ascertain a universally "safe" duration of total CA because outcomes may vary according to diagnosis, age at surgery, and other aspects of perfusion on cardiopulmonary bypass and postoperative care. In particular, the relative contributions of genetic polymorphisms and mutations, preoperative health, other operative factors, and postoperative events to late neurodevelopmental status remain to be clarified.
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Acknowledgments |
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J. W. Gaynor, G. Wernovsky, and R. Clancy Invited commentary Ann. Thorac. Surg., March 1, 2006; 81(3): 967 - 967. [Full Text] [PDF]
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J. M. Schultz, T. Karamlou, I. Shen, and R. M. Ungerleider Cardiac Output Augmentation During Hypoxemia Improves Cerebral Metabolism After Hypothermic Cardiopulmonary Bypass Ann. Thorac. Surg., February 1, 2006; 81(2): 625 - 633. [Abstract] [Full Text] [PDF]
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J. W. Newburger and D. C. Bellinger Brain Injury in Congenital Heart Disease Circulation, January 17, 2006; 113(2): 183 - 185. [Full Text] [PDF]
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C. L. Dent, J. P. Spaeth, B. V. Jones, S. M. Schwartz, T. A. Glauser, B. Hallinan, J. M. Pearl, P. R. Khoury, and C. D. Kurth Brain magnetic resonance imaging abnormalities after the Norwood procedure using regional cerebral perfusion J. Thorac. Cardiovasc. Surg., January 1, 2006; 131(1): 190 - 197. [Abstract] [Full Text] [PDF]
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C. L. Dent, J. P. Spaeth, B. V. Jones, S. M. Schwartz, T. A. Glauser, B. Hallinan, J. M. Pearl, P. R. Khoury, and C. D. Kurth Brain magnetic resonance imaging abnormalities after the Norwood procedure using regional cerebral perfusion J. Thorac. Cardiovasc. Surg., December 1, 2005; 130(6): 1523 - 1530. [Abstract] [Full Text] [PDF]
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G. Amir, C. Ramamoorthy, R. K. Riemer, V. M. Reddy, and F. L. Hanley Neonatal Brain Protection and Deep Hypothermic Circulatory Arrest: Pathophysiology of Ischemic Neuronal Injury and Protective Strategies Ann. Thorac. Surg., November 1, 2005; 80(5): 1955 - 1964. [Abstract] [Full Text] [PDF]
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F. L. Hanley Religion, politics...deep hypothermic circulatory arrest J. Thorac. Cardiovasc. Surg., November 1, 2005; 130(5): 1236 - 1236. [Full Text] [PDF]
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J. W. Gaynor, S. C. Nicolson, G. P. Jarvik, G. Wernovsky, L. M. Montenegro, N. B. Burnham, D. M. Hartman, A. Louie, T. L. Spray, and R. R. Clancy Increasing duration of deep hypothermic circulatory arrest is associated with an increased incidence of postoperative electroencephalographic seizures J. Thorac. Cardiovasc. Surg., November 1, 2005; 130(5): 1278 - 1286. [Abstract] [Full Text] [PDF]
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M. L. Skinner, L. A. Halstead, C. S. Rubinstein, A. M. Atz, D. Andrews, and S. M. Bradley Laryngopharyngeal dysfunction after the Norwood procedure J. Thorac. Cardiovasc. Surg., November 1, 2005; 130(5): 1293 - 1301. [Abstract] [Full Text] [PDF]
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G. M. Hoffman, K. A. Mussatto, C. L. Brosig, N. S. Ghanayem, N. Musa, R. T. Fedderly, R. D.B. Jaquiss, and J. S. Tweddell Systemic venous oxygen saturation after the Norwood procedure and childhood neurodevelopmental outcome J. Thorac. Cardiovasc. Surg., October 1, 2005; 130(4): 1094 - 1100. [Abstract] [Full Text] [PDF]
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I. Hagino, V. Anttila, D. Zurakowski, L. F. Duebener, H. G.W. Lidov, and R. A. Jonas Tissue oxygenation index is a useful monitor of histologic and neurologic outcome after cardiopulmonary bypass in piglets J. Thorac. Cardiovasc. Surg., August 1, 2005; 130(2): 384 - 392. [Abstract] [Full Text] [PDF]
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R. H. Jones The year in cardiovascular surgery J. Am. Coll. Cardiol., May 5, 2004; 43(9): 1706 - 1714. [Full Text] [PDF]
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R. M. Ungerleider and J. W. Gaynor The Boston Circulatory Arrest Study: An analysis J. Thorac. Cardiovasc. Surg., May 1, 2004; 127(5): 1256 - 1261. [Full Text] [PDF]
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