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Ann Thorac Surg 2006;81:678-684
© 2006 The Society of Thoracic Surgeons

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Original article: Cardiovascular

Successful Management of Patients With Pulmonary Atresia With Intact Ventricular Septum Using a Three Tier Grading System for Right Ventricular Hypoplasia

Division of Cardiothoracic Surgery, Department of Surgery, University of California-Los Angeles (UCLA) School of Medicine, Los Angeles, California

Accepted for publication July 13, 2005.

^_* Address correspondence to Dr Odim, Division of Cardiothoracic Surgery, UCLA School of Medicine, 10833 Le Conte Avenue, CHS 62-182, Los Angeles, CA 90095 (Email: jodim{at}mednet.ucla.edu).

	Abstract

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BACKGROUND: We sought to validate a simple grading scheme for right ventricular hypoplasia in determining suitability for a biventricular repair.

METHODS: We reviewed the medical records for 106 patients with pulmonary atresia-intact ventricular septum (PA-IVS) treated between 1982 and 2001. Over this period, children were assigned to mild (>2/3 normal size, 23.7% of patients), moderate (1/3 to 2/3, 41.2%), or severe (1/3, 35.1%) right ventricular hypoplasia, and this grouping, along with severity of coronary anomalies (45% right ventricle to coronary fistulae, 16% with right ventricle dependent coronary circulation [RVDCC]), triaged children to eventual single ventricle (severe) or two-ventricle (mild or moderate) repair.

RESULTS: Actuarial 10-year survival was 86.3% with mortality predicted by severe hypoplasia (odds ratio [OR] 12.9, p < 0.001), RVDCC (OR 15.0, p < 0.001), and non-Caucasian race (OR 10.7, p < 0.001). Multivariate analysis with a Cox proportional hazards model confirmed only RVDCC (risk ratio [RR] 10.9, p = 0.0009} and non-Caucasian race (RR 6.9, p = 0.007) as significant. Although not an independent risk factor for survival, the degree of hypoplasia was the most important determinant for definitive repair. Severe hypoplasia virtually precluded two-ventricle repair (OR 33.1, p < 0.001 by ² analysis) and was the strongest risk factor for a one-ventricle system (OR 78.7, p < 0.001). Actuarial survival after either repair was 91%, and no biventricular repair later converted to a Fontan system.

CONCLUSIONS: Surgical management of patients based on this three tier grade for right ventricular hypoplasia results in excellent survival and correctly predicts patients destined for eventual Fontan and biventricular repair.

	Introduction

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In 1985 [1], we described a classification scheme for right ventricle hypoplasia that separates infants with pulmonary atresia- intact ventricular septum (PA-IVS) into three categories of mild, moderate, and severe hypoplasia. With this scheme, the dimension of the right ventricular cavity is directly estimated from the usually normal companion left ventricle. Hypoplasia is mild if actual size is greater than two thirds of normal; moderate if it is one third to two thirds normal; and severe if the size is less than one third of predicted. Although this grading system correlates with descriptions of hypoplasia based on tricuspid Z scores or right ventricular partitioning [2], it has the advantages of simplicity. In order to validate this classification scheme, we have reviewed medical records for all patients with a diagnosis of PA-IVS over the past twenty years with specific interest in the adequacy of this approach for predicting surgical approach and outcomes.

	Patients and Methods

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Patient Population
A review of medical records between 1982 and 2001 identified 106 patients (51 girls, 55 boys) with pulmonary atresia and intact ventricular septum (PA-IVS). The University of California Los Angeles (UCLA) Institutional Review Board approved this study March 23, 2003 and individual patient consent was waived. Seventy-four of these patients were Caucasian. Eighty-two patients underwent definitive repair, defined as establishment of univentricular Fontan physiology (23), complete or partial biventricular physiology (57), or transplantation (2) after prior palliation. Partial biventricular physiology included patients with a bidirectional Glenn and either an adjustable or closed atrial septal defect (ASD). The remaining 24 patients underwent palliation only, with 9 dying before definitive repair, 8 still awaiting definitive repair, and 7 lost to follow-up. Mean follow-up from birth was 5.2 ± 0.5 years with a median of 3.5 years.

The average number of palliative operations was 1.6 ± 0.1 and median age at initial palliation was 4 days (range, 1 to 216 days). The most common palliative procedure was a systemic to pulmonary artery communication performed in 100 of the 106 patients (94.3%) (see Table 1 for systemic to PA shunting in 97 children assigned a right ventricle [RV] size). Sixteen of this group required additional systemic to pulmonary artery shunting for persistent cyanosis. Twenty-four patients underwent a cavopulmonary anastomosis. Fifty-six of the 109 patients (52.8%) received relief of right ventricle outflow tract obstruction (RVOTO) by pulmonary valvotomy (32.1%), transannular patch (13.2%), or both (7.5%). Only five patients in this study presented with additional Ebstein's malformation of the tricuspid valve. In this subset, one patient achieved a complete biventricular repair and another patient successfully underwent partial biventricular correction. A third patient died after initial palliation and two remaining patients await further intervention after recent palliation.

The qualitative estimates of right ventricular dimensions are based on preoperative two-dimensional, transthoracic echocardiograms and were available for 97 of the 106 patients. In PA-IVS, the accompanying left ventricle (LV) is usually of normal size and this is the yardstick used to assess RV hypoplasia. In 60 children, tricuspid valve orifice diameters were quantified, and were used in conjunction with the patient's body surface area to determine tricuspid Z scores from published nomograms [3].

Right Ventricle to Coronary Fistulae and RVDCC Dependence
Right ventricle to coronary fistulae were identified by coronary angiograms and ventriculograms for all patients. A spectrum of fistulae covering a broad range of physiologic significance existed. For the purpose of statistical analysis, their mere presence was treated identically among all patients. Right ventricle dependent coronary circulation (RVDCC) was deemed present when a major portion of LV myocardial perfusion was supplied exclusively from the right ventricle cavity. This circumstance occurred with proximal left coronary stenoses with concomitant right ventricle to left coronary fistulae, extensive right ventricle to coronary fistulae, or myocardial perfusion scans indicative of reversible defects.

Definitive Repair
A one-ventricle repair was synonymous with Fontan completion. A complete two-ventricle repair occurred when each ventricle ejected into its respective great artery without patent systemic pulmonary artery shunts. For most of these repairs an adjustable interatrial communication was created. Fifty-seven of the 106 children underwent biventricular repairs (complete or partial). In 30 children (52.3%) the atrial communication was completely snared closed after operation. The mean and median number of days toward ASD snare closure after biventricular repair was 474 ± 155 and 67 days, respectively. Of the remaining 25 patients, the ASD remained partially snared in 9.1%, spontaneously closed in 6.8%, and remained open permitting right to left shunting in 32%. The mean follow-up for this analysis was 351 ± 221 days. The concept of an adjustable ASD allows for a restrictive interatrial communication that can be narrowed or closed postoperatively by a snaring device left underneath the linear alba. This technique was universally applied to all candidates for biventricular repair to reduce right atrial pressure below 15 mm Hg, thereby preserving LV preload and cardiac output in the midst of acceptable oxygen saturations in the mid 80s. For statistical analysis, patients with partial biventricular repair had neither a one-ventricle nor complete two-ventricle system.

Study Design and Statistical Analysis
All patients were assigned one of six outcomes: completed two-ventricle repair, partial two-ventricle repair, one-ventricle repair, transplantation, death prior to definitive repair, or awaiting definitive repair. To evaluate the influence of right ventricle hypoplasia, right ventricle to coronary fistulae, and RVDCC on achieving these outcomes, each of these variables was used to segregate patients for the construction of 2 x 2 contingency tables. The ² analysis was used to calculate the p value.

The influence of race, gender, right ventricular hypoplasia, right ventricle to coronary fistulae, and RVDCC on time-dependent variables of survival, freedom from one-ventricle repair, and probability of two-ventricle repair was determined using Kaplan-Meier actuarial analysis, with p values calculated by log rank statistics [4]. The Cox proportional hazards regression model [5] was used for the multivariate analysis. In arriving at a summarizing model, each significant risk factor for mortality, one-ventricle repair, or two-ventricle repair was subjected to multivariable linear regression analysis. Death prior to definitive repair received a score of zero, while one-ventricle, partial two-ventricle, and completed two-ventricle repairs received scores of 1.0, 1.5, and 2.0, respectively. Significance was determined by the analysis of the one way analysis of variance method. To refine the model further, multivariable linear regression was repeated after exclusion of insignificant coefficients.

	Results

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Right Ventricular Dimensions and Anatomy
Among 97 patients assigned an RV hypoplasia grade, there were 23 (23.7%) with mild, 40 (41.2%) with moderate, and 34 (35.1%) with severe hypoplasia. Among the 60 patients with estimated tricuspid valve orifice diameters, the average Z score was –3.3 ± 0.3 with a median of –3.0 (range, 0 to –7). The Z score correlated well with degree of right ventricular hypoplasia among this subgroup of patients (r = 0.72, p < 0.001). Forty-seven of 106 patients (44.3%) had angiographic evidence of right ventricle to coronary fistulae, and these abnormal fistulous connections created RVDCC in 17 (16.0%).

RVDCC and Non-Caucasian Race Predict Poor Survival in Patients With PA-IVS
The actuarial survival of patients at 10 years was 86.3% (Fig 1). Twelve of the 16 deaths occurred within the first year of life, with seven within the first month. Although all patients received palliative intervention, 9 of these 16 patients died before definitive repair. These early deaths after palliation comprise the vast majority of deaths through the first 8 months of life (Fig 1). However, after this period the survival curve for the patient population mirrors that for those children reaching definitive repair. Actuarial survival after definitive repair was 91% over 10 years regardless of type of repair. Analysis of risk factors for death in this critical interval between palliation and definitive repair identified one demographic and two anatomic predictors of mortality (Table 2). A severe grade of right ventricular hypoplasia increases the odds of death by 12.9-fold, while RVDCC causes a 15-fold elevation in risk. Kaplan-Meier analysis confirms these two parameters as risk factors for death. One year actuarial survival in children with severe RV hypoplasia is 79.3% but 94.7% with mild or moderate hypoplasia (log-rank p = 0.049). Similarly, one year actuarial survival in patients with RVDCC is 56.3% and 93.8% without this coronary anomaly (log-rank p < 0.001). For both anatomic factors, risk is accrued entirely within the first year of life.

View larger version (20K): [in this window] [in a new window]   Fig 1. Survival in PA-IVS at UCLA between 1982 and 2001. Death within the first eight months parallels that of children dying perioperatively from surgical palliation, whereas later mortality reflects deaths after definitive repair. (— = all patients [106]; – · – = death prior to definitive repair [9]; gray line = patients reaching definitive repair.) (PA-IVS = pulmonary atresia-intact ventricular septum.)

View larger version (19K): [in this window] [in a new window]   Fig 2. Non-Caucasian race adversely affects survival both early and late in children with pulmonary atresia intact ventricular septum. (Black line = Caucasian [66]; gray line = minority [28].)

Male Gender and Severe RV Hypoplasia Predict One-Ventricle Repair in Patients With PA-IVS
Severe right ventricular hypoplasia carries the greatest weight in determining whether a child with PA-IVS will progress to Fontan. Among 33 patients with severe hypoplasia, 19 (51.6%) received a one-ventricle repair. The odds of yielding to a one-ventricle system with severe hypoplasia were 78.7-fold greater than in children with either mild or moderate RV hypoplasia (p < 0.001). The median duration to Fontan repair with severe RV hypoplasia was 4.2 years. No more than 7% of children with mild or moderate hypoplasia progressed to Fontan over 17 years of follow-up (log-rank p < 0. 001, Fig 3A). A weaker anatomic risk factor predicting single ventricle repair was the presence of right ventricle to coronary fistulae. Thirty-five percent of patients with fistulae required one-ventricle repair compared with 14% without these communications (OR 3.3%, p = 0.032).

View larger version (24K): [in this window] [in a new window]   Fig 3. Predictors of eventual one-ventricle repair in pulmonary atresia intact ventricular septum include (A) severe right ventricle hypoplasia (Black line = mild right ventricle [RV] hypoplasia; gray line = moderate RV hypoplasia; dashed line = severe RV hypoplasia) and (B) male gender (black line = females; gray line = males).

View larger version (25K): [in this window] [in a new window]   Fig 4. The probability of achieving a complete biventricular repair in children with pulmonary atresia intact ventricular septum is determined predominantly by degree of right ventricle (RV) hypoplasia. (— = mild RV hypoplasia [23]; - - - = moderate RV hypoplasia [40]; – – = severe RV hypoplasia [34].)

where

Race: 1 = Caucasian, 0 = non-Caucasian

RVDCC: 1 = Present, 0 = Absent

This model encompasses many of the results from this study. For example, a severe grade of right ventricular hypoplasia means the best outcome score possible is 1.28, a value intermediate between one-ventricle repair and a mixed circulation. These patients are not amenable to two-ventricle repair (outcome of 2.0). Additionally, the best score possible for a patient with RVDCC is 1.27, again intermediate between one-ventricle repair and a mixed circulation. However, since no patient with mild hypoplasia had RVDCC in this cohort, the best outcome is more reasonably estimated as 0.94 or lower.

	Comment

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A qualitative and simple three tier system for grading right ventricular hypoplasia has proven useful in guiding surgical management. The severity of RV hypoplasia is the major determinant of whether a child eventually attains a Fontan or complete biventricular system, and children triaged using this scheme have had excellent long-term results with either surgical destination. Right ventricular hypoplasia grade correlates strongly with tricuspid valve Z score. The degree of right ventricular hypoplasia also predicts early mortality after initial palliation, although with less overall significance than the presence of RVDCC and non-Caucasian racial background. These results, when incorporated into a linear regression model, produce a three variable (hypoplasia, RVDCC, race) equation that helps predict whether a patient dies before definitive repair or ultimately attains a one-ventricle, partial two-ventricle, or complete two-ventricle repair.

The ten-year survival of 86.3% in this study mirrors the steady improvement in outcomes reported at multiple centers over the past 25 years [6–12]. In an early multiinstitutional prospective study, Hanley and colleagues [3] reported a 64% four-year actuarial survival for infants treated between 1987 and 1991. Similar to our study and others [9, 13], their patients experienced the greatest hazard to survival in the first year of life. A later analysis between 1987 and 1997 from the Congenital Heart Surgeons Society analysis advocated a morphologically driven institutional protocol emphasizing both biventricular and Fontan pathways may mitigate the negative effect of unfavorable morphology. Ashburn and colleagues [14] demonstrated in this analysis that 85% of neonates were likely to reach a definitive surgical end point with a biventricular repair attained in up to 50%. Among a group of 47 patients at Children's Hospital in Boston with PA-IVS operated on between 1991 and 1998, the actuarial survival was 98% at 7 years [9], and in large single center series similar to our own with twenty-year patient accruals, long-term survival has ranged from 68 to 76% [10, 15].

Although it is tempting to attribute the successful outcomes to time-related refinements in surgical techniques and management strategies, evaluation of the data shows that virtually equal numbers of patients died in the first and last decade of this study. Our group has relied on this three tier grading scale for right ventricular hypoplasia and presence or absence of RVDCC to guide pursuance of either a one-ventricle or two-ventricle repair. A patient's right ventricular size contributes to his risk for early mortality, whether defined as tricuspid Z score [3], muscular pulmonary atresia [15], or presence of a "well-formed" infundibulum [7]. This influence of hypoplasia on survival was not altered by stratifying patients into mild, moderate, and severe groups in lieu of a continuous measure like the Z score or binary measure as the presence of a "well-formed" infundibulum. Among our patients, severe hypoplasia increased the odds of death by 12.9, but was a much smaller risk factor after accounting for RVDCC. As suggested by others [16], the real risk of death in patients with severe right ventricular hypoplasia may reside in coexistent RVDCC [2, 3].

Although subtle differences in the incidence of different congenital heart defects are noted from epidemiologic databases between Caucasian and non-Caucasian populations [17–19], no previous reports on PA-IVS have noted a racial predilection for early mortality. However, this study identifies the potential importance of non-Caucasian background when correcting for hypoplasia and RVDCC. The significance of this finding is unknown, and at best speculative as most large clinical series neglect racial composition in the analysis [3, 9, 10]. Greater focus on this issue in the future may provide explanations for its influence. Of note, when overall outcome for the entire cohort is modeled through multivariable linear regression, non-Caucasian background plays a small but significant role, especially among patients with unfavorable cardiac anatomy, and male gender is not a significant influence on outcome.

In conclusion, the grade of RV hypoplasia guides surgical management and predicts outcomes in children with PA-IVS. The use of a three variable linear regression model incorporating the degree of hypoplasia, the presence or absence of RVDCC, and race gives a quantitative measure of whether a patient will die prior to definitive repair. Additionally, the score obtained with this model provides an estimation of whether a patient will receive a one-ventricle, partial two-ventricle, or complete two-ventricle repair and provides treating physicians with a prognostic measure that can be communicated to the child's parents and used to direct optimal initial palliation [19–22].

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	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Jonah Odim Hillel Laks Mark D. Plunkett Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Odim, J. Articles by Tung, T. C. Search for Related Content PubMed PubMed Citation Articles by Odim, J. Articles by Tung, T. C. Related Collections Congenital - cyanotic