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(Chest. 1999;116:740-747.)
© 1999 American College of Chest Physicians

Pulmonary Risk Factors Compromising Postoperative Recovery After Surgical Repair for Congenital Heart Disease*

Hari P. R. Bandla, MD; Robert L. Hopkins, MD; Robert C. Beckerman, MD, FCCP and David Gozal, MD, FCCP

* From the Sections of Pediatric Pulmonology (Drs. Bandla, Beckerman, and Gozal) and Critical Care (Dr. Hopkins), Department of Pediatrics, Tulane University School of Medicine, New Orleans, LA.

Correspondence to: David Gozal, MD, FCCP, Section of Pediatric Pulmonology, Department of Pediatrics, Tulane University School of Medicine, SL-37, 1430 Tulane Ave, New Orleans, LA 70112; e-mail: dgozal{at}tmcpop.tmc.tulane.edu


    Abstract
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To identify pulmonary risk factors associated with prolonged ICU stay in young children (<= 2 years) undergoing surgical repair for congenital heart disease (CHD).

Design: Retrospective case series analysis.

Setting: Tertiary-care facility.

Patients: Clinical records of 134 consecutive patients aged <= 2 years undergoing cardiac surgery for CHD were reviewed, and 37 were excluded according to inclusion criteria. Thus, 97 patients were allocated to two groups based on the duration of ICU stay: <= 7 days (group 1, n = 57), and > 7 days (group 2, n = 40).

Results: Mean ICU duration for groups 1 and 2 was 3.0 ± 0.4 days and 28.1 ± 4.4 days, respectively (p < 0.001). In group 1, there were three extubation failures, whereas 41 extubation failures occurred in group 2 (p < 0.0001). A total of 22 patients (4 in group 1 and 18 in group 2) developed noninfectious pulmonary complications, such as airway problems, including extrinsic airway compression and tracheobronchomalacia (n = 6); pulmonary hypertension (n = 5); phrenic nerve palsy (n = 7); and pleural effusion (n = 8). These 22 patients (23%) contributed to the majority of total ventilator days (67%) as well as ICU stay (61%).

Conclusions: Pulmonary complications in general, and central airway problems in particular, are a frequent cause for delayed recovery following cardiac surgery in young children.

Key Words: cardiac surgery • congenital heart disease • flexible bronchoscopy • intensive care • mechanical ventilation • phrenic nerve palsy • respiratory morbidity • tracheobronchomalacia


    Introduction
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Congenital heart disease (CHD) encompasses a large spectrum of clinical entities, ranging from isolated cardiac defects to very complex multiple cardiac malformations, and in the vast majority of cases, surgical repair or palliative procedures are needed. Innovations in surgical techniques and in perioperative care have allowed for successful surgical repair of complicated CHD previously considered inoperable.

One of the major factors contributing to the high cost associated with surgical interventions in complex CHD is the duration of stay in the ICU. Indeed, studies examining the impact of ICU stay have shown that ICU utilization accounts for about 20% of total hospital costs.1 Thus, it is not surprising that with reforms in health care, early and more aggressive extubation after cardiac surgical procedures in children and neonates has been attempted and, in fact, shown to be both safe and feasible by several investigators.2 3 4 5 In an effort to identify risk factors associated with prolonged mechanical ventilation (MV), Kanter and colleagues6 retrospectively reviewed a cohort of 140 patients, aged < 2 years, who underwent surgical cardiac repair. The need for preoperative MV, longer cardiopulmonary bypass (CPB) and aortic cross-clamp durations, and additional surgical interventions were all identified as independent variables associated with prolonged MV and ICU stay. More recently, preoperative measurements of pulmonary vasculature physiologic variables, such as systemic and pulmonary resistance, were highly correlated with the duration of MV in patients undergoing repair of ventricular septal defects (VSDs).5 However, there is a paucity of information regarding the relative contribution of respiratory tract pathology to the need for prolonged MV and ICU stay in these patients. While postoperative diaphragmatic dysfunction is a well-recognized complication contributing to prolonged MV,7 acquired or congenital tracheobronchomalacia with significant airway obstruction complicating the postoperative period has only been reported in case report format in patients undergoing repair for CHD.8

We therefore undertook a critical 1-year retrospective review of all young patients undergoing cardiac surgery at our institution, and attempted to identify specific pulmonary risk factors that may underlie increases in the duration of MV and ICU length of stay in this patient population.


    Materials and Methods
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Data Collection
Hospital records of 134 consecutive patients, aged <= 24 months, who underwent palliative or corrective surgery for CHD at Tulane University Medical Center during the 1-year period from August 1995 to July 1996 were retrospectively reviewed. Premature infants and infants with preexisting lung disease or with other major congenital anomalies were excluded (n = 13). Twenty-four patients died within 48 h after surgery (immediate mortality) and were also excluded. Therefore, the study population included a total of 97 infants. The cardiac diagnoses were established by echocardiography, cardiac catheterization, and/or cineangiography. The following variables were recorded: demographics; cardiac diagnosis; surgical procedure; intraoperative information, namely total duration of surgery, CPB time, and aortic cross-clamp time; and duration of postoperative MV. Patients were allocated to two groups based on the duration of ICU stay: <= 7 days (group 1), and > 7 days (group 2).

ICU Data
The clinical course during the ICU stay was critically reviewed and complications were identified based on written reports and/or laboratory and other ancillary data. Complications were subdivided into four major groups: pulmonary, cardiac, infection, and others. However, for the present study, a detailed analysis was done only for those patients in whom noninfectious pulmonary complications were identified. Furthermore, in those patients in whom complications affected more than one system, attempts were made to identify the dominant system most likely to contribute to the adverse clinical course based on a consensus among the investigators. The group with pulmonary complications was further subdivided by type of complication: phrenic nerve dysfunction, airway problems, pulmonary vascular hypertension, and pleural effusion. Criteria for the diagnosis of phrenic nerve palsy included the presence of an elevated dome of the diaphragm with paradoxical motion on fluoroscopy or ultrasound. Tracheobronchomalacia was bronchoscopically identified from the occurrence of a dynamic collapse of the trachea and/or mainstem bronchi during spontaneous respiratory efforts. Atelectasis was defined as the radiographic finding of a lobar infiltrate and volume loss in the absence of clinical or laboratory signs of infection. Pulmonary hypertension was identified from echocardiographic estimates and/or catheterization measurements. Patients with pleural drainage > 5 mL/kg/d and patients requiring continued chest tube drainage beyond the third postoperative day were considered to have pleural effusion, and the nature of the pleural fluid (serous, bloody, or chylous) was noted.

Patients were extubated based on ongoing ICU algorithm protocols and the decision of the attending primary physician. When a patient was reintubated and mechanically ventilated within the first 48 h after planned extubation, the extubation was considered to have failed. The number of failed extubations and the overall durations of the ICU stay and the hospital stay were also documented. Nonimmediate postoperative mortality (> 48 h) was assessed until discharge from the ICU.

Flexible Fiberoptic Bronchoscopic Airway Assessment
When clinically indicated, fiberoptic flexible bronchoscopy was performed either in the operating room under general anesthesia or by the bedside in the ICU under sedation and additional topical anesthesia. Two pediatric bronchoscopes, one with a 2.2-mm external diameter (Olympus BF 22; Olympus America, Inc; Melville, NY) and the other with a 3.6-mm external diameter (Olympus BF 3C20), were used. Cardiorespiratory stability was continuously monitored in all patients, and supplemental oxygen was administered as necessary. To rule out the possibility of upper airway obstruction in patients with failed extubations, endotracheal tube removal was performed under bronchoscopic guidance, the upper airway was evaluated, and patients were reintubated if necessary with visual verification of appropriate positioning of the endotracheal tube.

Data Analysis
Data are expressed as mean ± SEM. Comparisons between groups 1 and 2 were performed using one-way analysis of variance followed by post hoc tests or unpaired t tests as appropriate. Linear regression analysis with calculation of regression coefficients was employed for assessment of potential relationships between bypass time and duration of MV or ICU stay. A p value of < 0.05 was considered to be statistically significant.


    Results
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Demographics, intraoperative data, and ICU data are shown in Table 1 . Group 1 consisted of 57 patients, representing 58.7% of the study population. The mean age was 8.8 ± 2.9 months, and there were 36 male infants in group 1. The mean weight percentile was 22.2 ± 3.3%. Group 2 included 40 infants (41.3%), 25 of whom were male, and their mean weight percentile was 29.3 ± 4.6% (p > 0.05, not significant [NS]). The patients in group 2 were significantly younger (mean age, 4.2 ± 0.7 months; p < 0.002). The cardiac diagnoses and surgical procedures for each group are shown in Tables 2 and 3, respectively. Mean surgical duration was 133.0 ± 7.5 min for group 1 and 156.0 ± 12.7 min for group 2 (p = NS). Total CPB and aortic cross-clamp times were 50.9 ± 3.1 min and 32.2 ± 2.6 min, respectively, in group 1, and 72.3 ± 14.1 min (p < 0.04) and 47.7 ± 9.7 min (p < 0.004) in group 2. The duration of MV in group 1 was 1.2 ± 0.2 days, significantly shorter than the 19.4 ± 3.0 days in group 2 (p < 0.0001). Similarly, mean durations of ICU and hospital stay were 3.0 ± 0.4 days and 9.0 ± 1.2 days, respectively, for group 1 and 28.1 ± 4.4 days (p < 0.001) and 40.9 ± 6.4 days (p < 0.001), respectively, for group 2. We further examined the relationship between CPB time and the duration of MV and ICU stay, and found that no significant correlations were present (Fig 1 ). In group 1, there were three extubation failures, whereas 41 extubation failures were recorded among 21 patients in group 2 (p < 0.0001).


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Table 1. Mean Demographic, Intraoperative, and Intensive Care Characteristics in Patients With an ICU Stay of <= 7 d (Group 1) vs > 7 d (Group 2)*

 

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Table 2. Cardiac Diagnosis in Patients With an ICU Stay of <= 7 d (Group 1) vs > 7 d (Group 2)*

 


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Figure 1. Linear regression analysis of relationships between CPB time and duration of MV (closed squares) and ICU stay (open circles). No significant correlation coefficients were found (p = NS).

 
Pulmonary Risk Factors
Pulmonary complications of noninfectious etiology were noted in a total of 22 patients (4 in group 1, 18 in group 2). ICU data for patients with primary pulmonary complications are shown in Table 4 . In group 1, four patients developed clinically significant pleural effusions. However, in group 2, 18 of 40 patients (45%) developed pulmonary complications determined to be the major factor associated with prolonged MV (Table 4) . These complications included evidence of central airway compression (n = 6), phrenic nerve dysfunction (n = 7), pleural effusion (n = 4), and severe pulmonary hypertension (n = 5). In four patients, more than one factor was considered to contribute equally to extubation failure, namely diaphragmatic palsy and airway compression in two patients, and pleural effusion in the presence of severe pulmonary hypertension in the other two patients.


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Table 4. Pulmonary Complications in 22 Patients Who Underwent Surgical Repair for CHD*

 
Of the six patients with central airway compression, three had severe distal tracheomalacia and bilateral bronchomalacia that required tracheotomy and chronic mechanical ventilatory support. In the remaining three patients, left-sided lobar atelectasis caused by extrinsic vascular compression of the bronchial structures was detected. The diagnosis was confirmed by flexible bronchoscopy in all six patients, two of whom required surgical relief of the vascular airway compression.

Phrenic nerve dysfunction occurred primarily in neonates (n = 5), and in all seven patients, the surgical procedure was conducted in the vicinity of aortopulmonary trunk (arterial switch procedure, n = 3; coarctation of aorta, n = 1; truncus arteriosus, n = 1; tetralogy of Fallot repair, n = 1; and augmentation of pulmonary artery, n = 1). In three patients, surgical plication of the diaphragm was necessary to wean the patient from MV.

Pleural effusions were noted in eight patients (four in group 1 and four in group 2). One patient developed bilateral chylothoraces that ultimately required thoracic duct ligation. Bilateral serous pleural effusions complicated the postoperative course in two patients, while unilateral effusions occurred in the other patients.

Moderate to severe pulmonary hypertension was present in five patients. All the patients were managed with the standard protocol for postoperative pulmonary hypertension, which included sedation, neuromuscular paralysis, hyperoxygenation, and respiratory alkalosis. When conservative measures failed, inhaled nitric oxide was successfully employed in two patients.

Thus, a total of 22 patients (22.6%) developed pulmonary complications (4 in group 1 and 18 in group 2) and required 522 days of MV (61.7% of all ventilator days), 686 days in the ICU (52.8% of the cumulative days for this cohort), and a total of 970 hospital days (43.1% of the overall hospital stay).

Deaths
Three deaths occurred in group 2 and no deaths were recorded in group 1. In the three patients from group 2, the primary cause of death was not directly attributable to the pulmonary involvement. An 11-day-old neonate with the diagnosis of DiGeorge syndrome and an interrupted aortic arch died of left ventricular dysfunction on the 11th postoperative day following a surgical repair attempt with interposition of a Gore-Tex tube graft (W.L. Gore & Associates, Inc; Flagstaff, AZ) from the ascending to the descending aorta. A 25-day-old neonate with total anomalous pulmonary venous return of infradiaphragmatic type underwent repair of the anomaly and developed pulmonary venous obstruction, thus needing a second surgical procedure for pulmonary vein augmentation. However, the postoperative course was complicated by severe congestive cardiac failure and candidial septicemia from which the infant did not recover. The third patient was a 4-month-old infant with the diagnosis of pulmonary atresia and intact ventricular septum who had undergone a modified Blalock-Taussig shunt placement in the neonatal period. The patient underwent a bidirectional Glenn procedure and atrial septostomy, after which he developed severe cardiac failure further complicated by Serratia sepsis, subacute bacterial endocarditis, and candidial septicemia; the infant died on postoperative day 72. Of note, diffuse hemorrhagic tracheobronchitis was noted in this particular patient during a flexible bronchoscopy performed on day 60 for hemoptysis.


    Discussion
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
In this study, we show that pulmonary complications in general, and central airway problems in particular, are not uncommon among young children undergoing surgical repair of congenital cardiac conditions, and account for a substantial proportion of the postoperative requirements for mechanical ventilatory support and the overall utilization of the ICU.

This is the first study to examine the role of pulmonary involvement in postoperative morbidity in this population. Several studies estimate that 18 to 41% of infants will require prolonged mechanical ventilatory support following cardiac surgery.9 10 11 12 Analysis of risk factors for prolonged ventilatory support requirements assign independent risk to the preoperative clinical status, to intraoperative elements such as CPB and cross-clamp durations, to the underlying cardiac defect, and to the nature of the surgical procedure.5 6 12 In general, patients with simple shunt lesions, such as atrial septal defect (ASD), VSD, and patent ductus arteriosus (PDA), and patients undergoing extracardiac palliation are frequently extubated in the operating room and therefore require minimal ICU stays. The current study supports such a contention, as evidenced by the low number of ventilator days and overall ICU days in group 1. On the other hand, patients with more complicated perioperative pathophysiology who undergo complex cardiac surgical procedures will be expected to require longer postoperative respiratory support, and it is the general consensus that in these patients, cessation of mechanical ventilatory support is usually achievable within the first 72 h postoperative.13 Inability to extubate in <= 72 h is indicative of a more complicated postoperative course that usually will involve dysfunction of several systems. Our current study indicates that the respiratory system is a major system contributing to this postoperative morbidity, and that four major groups could be identified in this setting: central airway obstruction, diaphragmatic dysfunction, pulmonary hypertension, and pleural effusion.

Central Airway Compression
It has long been known that children with CHD may be at increased risk for airway complications by virtue of the anatomical proximity of the cardiac chambers and major vessels to the central airways.14 Airway compression has been reported in association with dilated pulmonary arteries, left atrial enlargement, and massive cardiomegaly.14 The left lateral trachea, the superior aspect of the left mainstem bronchus, and the junction of the right intermediate bronchus with the right middle lobe bronchus are particularly vulnerable sites.15 In the vast majority of patients, the existing airway compression is usually relieved by surgical repair of the primary cardiac defect, such that most patients will be asymptomatic. However, residual compression and/or secondary bronchomalacia can be severe enough to manifest as persistent lobar atelectasis and recurrent pneumonia associated with poor mucociliary clearance in that region. Additionally, with the advent of prosthetic devices and conduits in the central vessels, extrinsic tracheobronchial compression by such devices has been increasingly recognized.16 17 18 Thus as evidenced by the current series, airway compression can be an important and often unrecognized source of pulmonary dysfunction in CHD patients during the postoperative period. Persistent wheezing is generally misconstrued as bronchoconstriction, leading to aggressive bronchodilator therapy with or without inhaled or systemic steroids that essentially postpones the recognition of extrinsic airway compression until the patient undergoes one or more extubation failures, and chronic respiratory failure settles in.19 Flexible bronchoscopic evaluation of the airways is the obvious diagnostic tool for central airway involvement in the postoperative CHD patient. The morbidity and overall medical care costs of airway involvement in this population are quite impressive. Indeed, the three patients with tracheobronchomalacia accounted for 12 of the 44 extubation failures, and all three required tracheostomy placement and application of positive pressure ventilation.

Of interest, none of our patients developed subglottic stenosis after extubation, although such a complication has been reported in up to 2.3% of the patients.20

Diaphragmatic Dysfunction
Diaphragmatic dysfunction is primarily caused by phrenic nerve injury after CHD repair, and conservative estimates assign a 0.3 to 2.1% risk to this complication.21 22 23 However, this relative risk may be underestimated. When preoperative evaluation of phrenic nerve conduction was conducted, the incidence of phrenic nerve dysfunction rose to 10%.24 The mechanisms leading to phrenic nerve dysfunction probably involve cold injury from iced cardioplegic solution or result from surgical trauma to the phrenic nerve as it courses around the great vessels in the thoracic cavity. The clinical manifestations are variable, and may range from lower lobar atelectasis on the affected side to ventilatory dysfunction secondary to respiratory pump failure. Infants and children < 2 years of age are at particular risk for development of respiratory failure because of the high compliance of the thoracic cage, the relatively weak intercostal musculature, and the mediastinal shifts induced by paradoxical motion of the paralyzed diaphragm. Thus, these patients are at high risk for extubation failure and for prolonged ventilatory dependency. In this study, the seven patients with phrenic nerve dysfunction accounted for a total of 14 extubation failures (31% of all failures) leading to prolonged MV (mean, 29.8 days) and ICU stay (mean, 43.4 days). Recognition of this complication is usually delayed by the nonspecific nature of the symptoms (ie, respiratory distress following extubation or during weaning protocols) and by the absence of the characteristic radiologic findings in a mechanically ventilated patient. Although the therapeutic approach to postoperative diaphragmatic paresis in young children remains controversial, early plication of the diaphragm may decrease the duration of MV and associated respiratory morbidity in selected cases.7 25 Indeed, a favorable outcome was noted in our three patients who underwent diaphragmatic plication, and extubation was successful within 48 h of the plication procedure.

Pleural Effusion
Ordinarily, the pleural drainage during the immediate postoperative period is expected to be < 3 mL/kg/d, such that chest tubes can be removed by the third postoperative day. Causes for excessive pleural drainage include fluid overload, pulmonary edema, serous fluid leakage from the extracardiac shunts, chylothorax secondary to thoracic duct dysfunction,26 27 and increased central venous pressure as seen in patients undergoing the Fontan procedure. Effusions are generally small, transient, and self-limiting, and pure hemorrhagic effusion is rare and usually manifests in the first few hours after surgery. However, chylothorax leading to respiratory distress and malnutrition may necessitate administration of IV hyperalimentation and modified enteral diets, which, if unsuccessful, may lead to surgical placement of pleuroperitoneal shunts and ligation of the thoracic duct as seen in one of our patients.28

Pulmonary Hypertension
Pulmonary hypertension can be a frequent complication in the postoperative period, particularly in neonates and in infants with preoperatively increased pulmonary blood flow such as those who have large VSDs, AV canal defects, or truncus arteriosus.29 Elevated pulmonary arterial pressure and resistance increase the perioperative morbidity and mortality by compromising right ventricular function and oxygenation.30 Aggressive efforts to improve oxygenation and alveolar ventilation and to achieve effective sedation with adequate muscle relaxation may need to be coupled with pharmacologic interventions such as inhaled nitric oxide.31

Extubation Failure
In a critical care unit setting, figures for extubation failure range from 17 to 19% in adults to 22 to 28% in premature infants.32 33 In the only pediatric series addressing this issue, extubation failure in the absence of upper airway obstruction was observed in 16.3% of cases.34 However, we are unaware of any data specifically examining the rate of extubation failure in young patients undergoing cardiac surgery. In the present study, we found that 24 of 97 patients (21 patients in group 2 and 3 patients in group 1), or about 25% of patients, had at least one extubation failure, suggesting that this particular population is at high risk for such a complication. It has become quite clear that extubation failure is associated with an increased number of medical complications and with significantly higher mortality rates in the critical care unit.35 36 Therefore, we recommend that young children undergoing cardiac surgical repair be identified as a particular high-risk group for extubation failure, and that clinicians actively seek to identify specific pulmonary factors: Among the 21 patients in group 2 who failed extubation, pulmonary dysfunction was the leading etiologic factor in 13 patients (54%).

Intraoperative Variables
CPB duration has been associated with higher incidence of prolonged MV in the postoperative period.5 6 Although the exact mechanism(s) for such association are yet to be elucidated, pulmonary function tests after CPB reveal reduced static dynamic compliance, decreased functional residual capacity, increased alveolar-arterial oxygen gradient, and atelectasis, all of which can contribute to extended mechanical ventilatory needs.37 However, our study does not support such a correlation between CPB duration and the duration of either MV or ICU stay. Our findings concur with those of Heinle et al,4 who reported that the duration of CPB or aortic cross-clamp time did not prevent extubation at the conclusion of the operation in neonates and young infants after surgical repair for CHD.

Some methodologic considerations regarding the present study deserve comment. First, allocation of patients to two groups on the basis of the duration of ICU stay was an arbitrary decision based on previous experience at our institution, and more specifically based on the fact that 7 days was the 95th percentile of the mean duration of ICU stay for all young patients undergoing cardiac surgical repair (data not shown). Thus, we believe that, although the decision was somewhat arbitrary, it clearly differentiates between low- and high-risk groups of patients. A second limitation of this study is inherent to the retrospective evaluation of clinical data; it is sometimes difficult to establish true comparisons among the groups because they were not prospectively evaluated with each variable controlled. This is particularly important for assignment of individual roles to specific postoperative courses in which comorbidity was present. Nevertheless, the high degree of pulmonary involvement in general, and particularly that of central airway compression, in those patients requiring prolonged ICU stay indicates that such factors are important contributors to less favorable postoperative outcomes, and should therefore be considered early rather than late in the event of extubation failure.

In summary, in young children undergoing surgical repair of complex cardiac lesions, increased postoperative morbidity is clearly associated with pulmonary involvement, and more specifically when central airway compression and/or phrenic nerve dysfunction are present. Thus, early evaluation for these pulmonary conditions should be considered in any postoperative patient who fails extubation. It is possible that prospective evaluation of clinical algorithms encompassing the information and considerations reported herein may lead to earlier identification and decreased morbidity in this high-risk population.


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Table 3. Cardiac Surgical Procedures Required in Patients With ICU Stays of <= 7 d (Group 1) vs > 7 d (Group 2)

 

    Footnotes
 
Abbreviations: ASD = atrial septal defect; CHD = congenital heart disease; CPB = cardiopulmonary bypass; MV = mechanical ventilation; NS = not significant; PDA = patent ductus arteriosus; VSD = ventricular septal defect

This research was supported by National Institutes of Health grant HD-01072, Maternal and Child Health Bureau grant MCJ-229163, and an American Lung Association Career Development Award CI-002-N (Dr. Gozal).

Received for publication November 5, 1998. Accepted for publication April 16, 1999.


    References
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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