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Ann Thorac Surg 2008;85:1247-1255. doi:10.1016/j.athoracsur.2007.12.068
© 2008 The Society of Thoracic Surgeons
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Right arrow Coronary disease

Original Articles: Adult Cardiac

Risk Scores Do Not Predict High Mortality After Coronary Artery Bypass Surgery in the Presence of Diastolic Dysfunction

Lorenzo Merello, MDa,b,*, Erick Riesle, MDa,b, Javier Alburquerque, MDa,b, Humberto Torres, MDa,b, Ernesto Aránguiz-Santander, MD, FACCa,b, Oneglio Pedemonte, MDa,b, Bernhard Westerberg, MDa,b

a School of Medicine, University of Valparaíso, Valparaíso, Chile
b Cardiovascular Surgery Service, Hospital Dr. Gustavo Fricke, Viña del Mar, Chile

Accepted for publication December 26, 2007.

* Address correspondence to Dr Merello, University of Valparaiso, Anesthesiology, Servicio Cirugía Cardiovascular, Viña del Mar, Alvares 1532, Chile (Email: lorenzomerello{at}gmail.com).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Although global postoperative mortality after on-pump coronary artery bypass grafting is approximately 3%, in some groups it can be considerably higher. Many conditions are known to increase mortality and have been included in well-known scoring systems; however, left ventricular diastolic dysfunction has not been sufficiently evaluated to identify its predictive value for mortality after coronary artery bypass grafting, nor is it integrated in currently used risk scores.

Methods: Left ventricular filling pattern was prospectively evaluated in 191 patients scheduled for on-pump coronary artery bypass grafting. A follow-up of survival and complications was made for 30 days postoperatively. Observed mortality was compared with the mortality predicted by the scores of EuroSCORE and Parsonnet.

Results: A correlation was found between diastolic function, the presence of comorbidities, and postoperative survival. There was no mortality in the group with normal filling pattern (0 of 33 patients). In the presence of an alteration of relaxation, mortality was 5 of 129 patients (3.8%); in the pseudonormal group it was 2 of 16 patients (12.5%); and in the restrictive group it was 6 of 13 patients (46.1%; p < 0.01). Parsonnet and EuroSCORE predicted a mortality of 1.5% to 1.6%, 1.5% to 2.0%, 1.5% to 2.2%, and 3.9% to 4.1% for each group, respectively. Mortality in the group with E deceleration time of 150 ms or greater was 2.8% and in the group with E deceleration time less than 150 ms was 17.3% (p < 0.01). Postoperative complications were also more frequent in the group with advanced dysfunction.

Conclusions: Severe diastolic dysfunction is a strong predictor of adverse outcome and mortality after on-pump coronary artery bypass grafting, and this high risk is not adequately predicted by EuroSCORE and Parsonnet score. Measures of diastolic function should be included in routine preoperative risk assessment.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Atherosclerotic coronary heart disease is the greatest cause of cardiovascular death in the world, and its incidence is rising worldwide, particularly in developing countries as a result of demographic and lifestyle changes [1]. The global perioperative mortality reported by The Society of Thoracic Surgeons for coronary artery bypass grafting (CABG) surgery is approximately 3% [2], but unfortunately many factors have been identified to adversely affect the outcome, which can raise mortality in certain groups of patients.

Different predictive factors have been grouped in a number of preoperative risk evaluation scores to help estimate the risk of death after surgery [3–13]. Among these factors, systolic dysfunction has been one of the most studied and is widely validated as a predictor of bad outcome and so is routinely evaluated and reported preoperatively before CABG surgery. Nonetheless, through the echocardiographic study, it is possible to also acquire adequate information about the diastolic function of the left ventricle and its capacity of relaxation and suction. Thus, several indexes of diastolic filling pattern have been validated.

Most authors classify diastolic filling pattern according to the relationship between early filling deceleration time (EDT) and measurements of the ratio between early diastolic filling (E wave) and atrial contraction (A wave; the E/A relation), pulmonary venous flow, and isovolumetric relaxation time [14]. Among the multiple variables described, the measurement of EDT has been considered a simple and useful variable to quantify the stiffness of the left ventricle [15].

This report prospectively assesses the correlation between left ventricular diastolic filling patterns, measured by echocardiography, with postoperative mortality and complications in patients who underwent on-pump CABG. The scarce evidence available suggests that in patients with severe systolic dysfunction, there is a correlation between the magnitude of the associated left ventricular diastolic dysfunction and perioperative mortality [16, 17]. It is also clear that usually the progression in heart disease is accompanied by a worsening in other comorbidities, and the overall risk should be calculated considering the complete clinical condition. However, there are no published studies designed to show the importance of diastolic dysfunction as an independent predictor to recommend its incorporation in the preoperative risk scores available.

On the basis of this background this study sought to determine the impact of diastolic dysfunction on perioperative mortality and complications and to compare these results with the predicted mortality calculated by the European System for Cardiac Operative Risk Evaluation (EuroSCORE) [9] and the Bernstein-Parsonnet risk stratification model [10]. We also tested the predictive value of EDT as one single echocardiographic variable in the stratification of risk.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
After the approval by the institutional review board, 191 patients scheduled for on-pump CABG surgery were recruited between March 2004 and May 2006. Because no special care interventions were mandated by the protocol, signed patient consent was waived. Exclusion criteria included off-pump CABG, CABG associated with valve surgery, severe mitral or aortic valvulopathy, atrial fibrillation, and implanted pacemaker.

Preoperative risk scores according to 2,000 Bernstein-Parsonnet and EuroSCORE algorithms were applied to all patients in this study. Then a complete preoperative echocardiographic evaluation was undertaken, including measurement of the diastolic filling pattern of the left ventricle.

Echocardiographic Studies
The echocardiographic assessment was done with a General Electric model Vivid 7 (GE Healthcare, Milwaukee, WI) and the echocardiographic studies were performed by a single operator. All studies were recorded on videotape and on photographic paper for further evaluation if necessary. A second operator evaluated all cases that were difficult to interpret. For the evaluation of diastolic function, pulsed Doppler mitral filling flow was measured at the level of the open mitral leaflets in the apical four-chamber view.

The echocardiographic exploration was obtained in a lateral decubitus position, and measurements were made in M mode, two-dimensional, pulsed Doppler, and colored Doppler. The measurements included left ventricular end-diastolic diameter, left ventricular end-systolic diameter, septal wall, posterior wall, left atrium, and left ventricular ejection fraction. In all cases peak velocities of blood flow during early diastolic filling (E wave) and atrial contraction (A wave) are measured, and the E/A ratio was calculated. Measurements also included pulmonary venous flow, E wave deceleration time (EDT), and the response to the Valsalva maneuver in patients with normal or pseudonormal filling pattern.

Classification of Patients
According to the transmitral flow pattern, patients were subdivided in four groups: group 0 normal filling pattern, with an E/A ratio less than 1.5 and EDT of 150 ms or greater; group 1 alteration of relaxation, with an E/A ratio less than 1 and EDT of 150 to 250 ms; group 2 pseudonormal, with an E/A ratio less than 1.5 and EDT of 150 ms or greater, and a response to Valsalva (+); and group 3 restrictive, with an E/A ratio greater than 1.5 and EDT less than 150 ms.

The relationship between EDT and outcome was also evaluated; therefore, patients were subsequently divided into two groups according to the criteria published by Yong and colleagues [18]: group A, EDT equal or greater than 150 ms, and group B, less than 150 ms.

Surgery
Coronary artery bypass grafting was performed under cardiopulmonary bypass in mild hypothermia (34°C) and with alpha-stat regulation of pH. Myocardial protection was achieved with crystalloid cardioplegia followed by intermittent cold blood antegrade or retrograde cardioplegia.

Follow-Up Data
During the postoperative period, data of survival and complications were recorded up to 30 days after surgery. Tabulated complications included perioperative myocardial infarction (new Q waves or creatine kinase MB elevation >50 U), atrial fibrillation, ventricular tachycardia or other arrhythmias requiring therapy, heart failure or low cardiac output (cardiac index less than 2 L · min–1 · m–2 plus inotropic agent use), cerebrovascular accident (focal deficit documented by clinical or scanner examination), prolonged mechanical ventilation (more than 24 hours postoperatively), acute renal failure (urinary output less than 400 mL/24 hours, creatinine levels twice the preoperative values, or increase in uremia by more than 50 mg%), reoperation of any cause, and intraoperative mortality and mortality up to 30 days. The follow-up after discharge was made by telephone.

Statistical Analysis
In-hospital and 30-day postoperative mortality was considered the binary response variable. For each patient several covariates were registered that allowed the calculation of both EuroSCORE and Parsonnet as a measure of risk of death. In addition, diastolic dysfunction severity (0, 1, 2, and 3, where 0 means no diastolic dysfunction and 3 means the most severe dysfunction) was registered.

The binary mortality through logistic models for each of three covariates (EuroSCORE, Parsonnet, and diastolic filling pattern) separately and together was evaluated. A binary diastolic dysfunction was defined as equal to zero if there was no dysfunction or it was type 1 or 2, and equal to one if there was a type 3 dysfunction, because it was suspected that the restrictive pattern is a better predictor of postoperative mortality. This logistic model will allow the acquisition of the odds ratio of death among the patients who have type 3 dysfunction with respect to those patients who have no dysfunction or type 1 or 2 diastolic dysfunction.

A separate univariate logistic regression analysis was drawn from the clinical variables described in EuroSCORE and the score of Parsonnet. Then a forward stepwise multiple logistic regression analysis was performed to evaluate the independent role of each significant variable identified by the univariate analysis, using probability values of 0.10 as the threshold for entering variables. Variables were included in the model if they reached a significance level of probability of less than 0.05 in univariate analysis.

For other numerical variables, the unpaired Student’s t test was used to compare means between two groups. Analysis of variance and Bonferroni multiple comparison tests were used for comparison among multiple groups. The {chi}2 test or Fisher’s exact test was used for categorical variables. Values are expressed as the mean ± standard deviation unless otherwise specified.

The statistical analysis was performed by the Center of Statistical Studies of the University of Valparaíso. All the statistical computations were performed with Stata (StataCorp, 2005, College Station, TX).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Patients were divided into four groups according to preoperative left ventricular filling pattern. Baseline clinical characteristics and preoperative risk factors are summarized in Table 1.


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  		Table 1 Clinical Characteristics and Preoperative Risk Factors a,b
 
According to the left ventricular filling pattern, 33 of 191 patients (17.3%) had preserved diastolic function, 129 of 191 patients (67.5%) had a pattern of alteration of relaxation or grade 1 dysfunction, 16 of 191 patients (8.4%) had a pseudonormal pattern or grade 2 dysfunction, and 13 of 191 patients (6.8%) had a restrictive filling pattern or grade 3 dysfunction.

Age, sex, incidence of diabetes mellitus, obesity (body mass index ≥ 30 kg/m2), and left main disease did not differ significantly among groups. The group with more advanced impairment of diastolic function had a higher incidence of renal failure, dialysis dependency, low ejection fraction, and a higher incidence of Canadian Cardiovascular Society (CSS) functional class III or IV. In agreement with the typical echocardiographic and Doppler waveforms found in left ventricular diastolic dysfunction, the groups differed in E and A wave peak velocities, EDT, and ejection fraction (p < 0.01). The echocardiographic characteristics are listed in Table 2.


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  		Table 2 Echocardiographic Variables According to Diastolic Filling Pattern a
 
The presence of EDT less than 150 ms as a marker of clinically significant diastolic filling abnormality was found in 52 of 191 patients (27.2%). The group with EDT less than 150 ms was significantly older, had lower body weight, and a higher incidence of ejection fraction less than 0.50 and renal failure. This association could be explained by the parallel progression of other pathologic conditions and the progressive reduction of the amount of viable myocardium. Tables 3 and 4 Go list the clinical and echocardiographic variables for each group according to the EDT.


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  		Table 3 Clinical Characteristics of Patients According to E Wave Deceleration Time a,b
 

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  		Table 4 Echocardiographic Variables According to E Wave Deceleration Time a
 
Patients with higher grades of diastolic dysfunction showed reduced ejection fraction, shorter EDT, and increased systolic and diastolic ventricular dimensions. There was no difference in the number of diseased vessels, number of grafts, or cross-clamp time.

Preoperative Estimation of Risk
The overall preoperative estimation of risk according to the criteria defined by Parsonnet resulted in a mean score of 9.1 for the cohort studied (range, 0 to 35 points). Patients with the most severely impaired diastolic function had a number of associated clinical conditions that increased their predicted mortality. The scores of Parsonnet and the EuroSCORE identified this increased risk, showing a statistically significant raise of estimated mortality in the group with more severe dysfunction (p < 0.01).

There were no fatalities in the group with normal filling pattern (0 of 33 patients). In the presence of alteration of relaxation mortality was 5 of 129 patients (3.8%), in the pseudonormal group, 2 of 16 patients (12.5%), and in the restrictive group, 6 of 13 patients (46.1%; p < 0.01). The odds ratio was 20.9 for the restrictive group versus the nonrestrictive (95% confidence interval, 5.5 to 78.9). The mortality rate observed in the groups with pseudonormal and restrictive filling pattern largely exceeded the mortality predicted by the risk scores (Table 5). The relationship between expected mortality derived from the application of Parsonnet and EuroSCORE and observed mortality is shown in Figure 1.


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  		Table 5 Expected and Observed Mortality According to Filling Pattern a,e
 

Figure 1
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  		Fig 1. Relationship between predicted mortality (Parsonnet, light gray bars, and EuroSCORE, darker gray bars) and observed mortality (black bars), according to left ventricular diastolic filling pattern. The groups with pseudonormal and restrictive pattern had a mortality significantly higher than predicted. (Alt = altered.)

 
When data were analyzed according to EDT, the predicted mortality calculated by EuroSCORE risk scale was slightly higher than the predicted by Parsonnet (Table 6). The group with EDT less than 150 ms had a much higher mortality than the group with EDT of 150 ms or greater (odds ratio, 7.0; p < 0.01). Although observed mortality was statistically higher than expected in both groups, it was not clinically significant in the low-risk group. Conversely, the observed mortality in the group with EDT less than 150 ms was much higher than expected. Risk scores were able to detect the slightly higher mortality expected with the associated extracardiac conditions, but were insufficiently accurate to predict the high mortality seen in the groups with pseudonormal or restrictive filling patterns.


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  		Table 6 Expected and Observed Mortality According to E Wave Deceleration Time a,b
 
Table 7 lists the results of the univariate logistic analysis for the evaluated risk factors. In the final multivariate regression model, the only variables found to independently predict mortality were renal failure, restrictive filling pattern, and advanced age (Table 8).


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  		Table 7 Univariate Analysis Results a
 

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  		Table 8 Multivariate Forward Stepwise Logistic Analysis Results a
 
Adverse Events
The incidence of clinically significant postoperative complications differed between normal and impaired diastolic function patients. Adverse events were observed in 9 of 33 patients (27.2%) with normal filling pattern, in 42 of 129 patients (32.5%) with grade 1 dysfunction, in 4 of 16 patients (25%) with grade 2 dysfunction, and in 10 of 13 patients (76.9%) with grade 3 or restrictive filling pattern.

Postoperative low cardiac output, acute renal failure, prolonged mechanical ventilation, and overall complication rate was higher in the restrictive group (Table 9). Mean length of stay in the hospital was 8 days for groups 0, 1, and 2 and 13 days for patients with grade 3 dysfunction as a result of a higher morbidity rate in patients with more severe ventricular dysfunction.


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  		Table 9 Adverse Events a
 
The need of prolonged mechanical ventilation was also higher in the group with EDT less than 150 ms; they also had a higher incidence of atrial fibrillation, perioperative infarction, other arrhythmias, and acute renal failure. The overall incidence of complications was also significantly higher in patients with EDT less than 150 ms (p = 0.01). Despite the incidence of particular complications being higher in this group, it did not reach statistical significance, except for acute renal failure (p < 0.01).

The mean event rate per patient was also increased in the group with restrictive filling pattern as shown in Figure 2. These results show that the progression of left ventricular filling abnormality is associated with more patients with complicated postoperative course and also accompanied by an increase in the number of complications per patient.


Figure 2
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  		Fig 2. Frequency of postoperative adverse events according to left ventricular diastolic filling pattern. There is a statistically significant higher number of adverse events in the restrictive group. (Alt = altered.)

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
In recent years increasing evidence has been gathered to show that impairment in diastolic function is associated with a poor prognosis in patients with ischemic cardiopathy [19], congestive heart failure [20], or dilated myocardiopathy [21]. On the other hand, there has been growing interest in making risk-adjusted analysis of outcome after heart surgery. Nevertheless, the role of diastolic dysfunction in postoperative mortality after CABG is still not well established. In fact, there are only a few reports that suggest that left ventricular diastolic dysfunction is a predictor of poor postoperative outcome, and to the present day it has not been incorporated in any cardiac surgery risk score. In this study, we compared our results with two well-validated risk models [22].

Early investigations showed that patients with elevated end-diastolic pressures experienced more complications and greater perioperative mortality than patients with normal telediastolic pressures [23]. With the advance of noninvasive exploration with echocardiography and cardiac Doppler, diastolic function can be easily and precisely evaluated, in a rapid and simple way, positioning this method as the gold standard for the assessment of diastolic function [24]. Despite the knowledge gained in recent years, the relationship between diastolic dysfunction and perioperative mortality after CABG surgery is not well known. Also there is no universal consensus about the best way of defining diastolic dysfunction.

A study published in 2001 by Vaskelyte and associates [16] analyzed patients with severely impaired systolic function (left ventricular ejection fraction less than 0.35) undergoing CABG and who also had a restrictive diastolic filling pattern. Their perioperative mortality was high (33%) compared with patients with less severely altered filling pattern, who had a mortality of 13.6%. The 56 patients included in this study had left ventricular diastolic dysfunction, and there were no patients with normal filling pattern. The study concluded that grade 3 diastolic dysfunction drastically affects perioperative mortality and that systolic function did not improve after surgery in this group, contrasting with the improvement seen in patients with less severe dysfunction. This observation has led the authors to question the benefit of CABG surgery in patients with restrictive filling pattern [16].

The above-mentioned study was the first to point out the predictive value of the assessment of left ventricular diastolic function by echocardiography before CABG surgery, but did not include a control group with normal filling pattern, or normal or less severe alteration of systolic function. It also excluded patients with diabetes mellitus, nephropathy, or other morbidity posing some unanswered questions. The study did not stratify patients according to the estimated preoperative risk by any validated risk score index to help evaluate the results with reference to an established risk.

A more recent study performed in the University of Yamaguchi in Ube, Japan, by Liu and coworkers [17] compares longtime survival in 102 patients who underwent CABG surgery according to the postoperative filling pattern. After a 60-month follow-up, the authors conclude that patients with normal or grade 1 diastolic dysfunction have a better long-term survival compared with patients with pseudonormal or restrictive pattern, in which survival declined at 50 months to 40% and 20%, respectively. These results agree with the results by Vaskelyte and coworkers [16] in a population that excludes chronic renal failure. Owing to the long-term design, in this report there is no conclusion about perioperative mortality and there is no evaluation of perioperative complications.

A third study correlates EDT with myocardial viability. This study by Yong and colleagues [18] shows that patients with EDT less than 150 ms undergoing CABG have less viable segments measured by echocardiographic dobutamine stress test and by single-photon emission computed tomographic myocardial scintigraphy. This group had a lower recuperation of systolic function after surgery and worse prognosis after 3 months’ follow-up.

Our study corroborates the high incidence of abnormal diastolic function in patients undergoing CABG. Some degree of dysfunction was found in 156 of 191 patients (81.7%) entering this study. The observed mortality in the groups with normal or nonrestrictive filling pattern was 5 of 162 patients (3,08%) as compared with the restrictive group, which was 6 of 13 patients (46.2%; odds ratio, 20.9). These results agree with the conclusions by other reports suggesting that advanced diastolic dysfunction is a strong predictor of postoperative morbidity and mortality after on-pump CABG.

It is known that left ventricular diastolic dysfunction is associated with a variety of conditions that increase postoperative risk, such as aging, history of myocardial infarction, diabetes, low ejection fraction, renal function impairment, and others [25]. We also found that the group with more severe dysfunction had a higher incidence of preoperative low ejection fraction and renal failure, with a tendency to be older and to have lower body weight. Even considering the higher incidence of associated comorbidity in patients with more severe impairment of diastolic function, the mortality predicted by the scores of Parsonnet and EuroSCORE was only around 4% in the restrictive pattern group. This study shows the low predictive value of these otherwise well-validated scores in the prediction of mortality in patients with advanced diastolic dysfunction. Consistent with the results of the logistic regression analysis, the incorporation of diastolic dysfunction as a risk factor would add a powerful predictor of postoperative adverse outcome.

The analysis of postoperative complications also showed a significant increase of adverse events in the restrictive group. This condition was associated with a higher incidence of low cardiac output, prolonged mechanical ventilation, arrhythmias, and postoperative acute renal failure. Most of the published papers do not report the incidence of complications, which are associated with higher hospital workload and economic costs associated with treatment.

All the comorbidities found in the higher risk patients can explain in part the higher mortality in this group. Otherwise, the risk scores even considering these comorbid conditions in the estimation of postoperative outcome were unable to accurately predict the high mortality associated with diastolic dysfunction. It is necessary to elucidate whether some of the comorbid conditions incorporated in these risk scores, such as advanced renal failure, increase mortality through an impact on diastolic function.

Prognostic Significance of E Wave Deceleration Time
In search of a simple and readily available measurement of diastolic function, we evaluated the predictive value of a simple way to analyze and stratify left ventricular filling pattern. The first stratification was according to a commonly used graduation in severity, and the other was based on the measurement of one single variable (EDT) as a marker of clinically significant left ventricular diastolic filling abnormality, with a cutoff point of 150 ms. Although the second is simple because it considered only one measure, the first allowed identifying the subgroup with the highest risk, represented by the restrictive pattern. It is probable, however, that if the cutoff point for EDT to define significant diastolic dysfunction is set at a lower level, eg, 130 ms, it could possibly identify a group with higher risk of morbidity and mortality. Diastolic dysfunction seems to be a progressive disease, with a worse prognosis and increased mortality in advanced stages, as occurs in diabetes, renal disease, aging, and other conditions. Because of the complexity of diastolic function, it appears reasonable that no single variable or Doppler pattern should be used in isolation, and conversely, all comprehensive Doppler and two-dimensional features should be considered to accurately assess diastolic function.

It is of interest to note the high prevalence (64%) of alteration of relaxation (grade 1 dysfunction) in our study population. Despite its apparent benign condition, a discrete higher morbidity and mortality was observed in this group compared with patients with normal filling pattern. Further studies in a larger population should be undertaken to confirm this finding.

Study Limitations
Our study included only patients who were operated on using on-pump techniques, so a difference in results with off-pump CABG could exist. However, there is evidence in a report by Ng and associates [26] that shows there is no difference in the filling pattern after on-pump versus off-pump CABG, suggesting that probably there is no difference in resulting morbidity or mortality between the two techniques.

It is also necessary to consider that the evaluation of diastolic function could be limited in the presence of tachycardia, atrial fibrillation, and other situations that could render its measurement difficult. Another limitation in this study is the difference in the number of patients in each group, which was conditioned by the design in which we included all patients scheduled for on-pump CABG who met the inclusion criteria. Despite this limitation, it allowed us to observe how these variables are seen in the usual population scheduled for CABG.

In conclusion, our findings suggest that diastolic dysfunction is a strong independent predictor of adverse outcome and that it should be considered as a clinical variable to be evaluated routinely in the risk stratification systems. Considering that Doppler echocardiography screening is routinely performed preoperatively before cardiac surgery, information about diastolic function should be regularly obtained. Larger studies are needed to identify the best way to accurately define the presence and severity of diastolic dysfunction and also to calculate its specific predictive power compared with other conditions already incorporated in the commonly used risk scores. Studies should be designed additionally to identify better strategies to lower the morbidity and mortality in these high-risk patients.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We are grateful to Carlos Henríquez-Roldan, PhD, Centro de Estudios Estadísticos, Universidad de Valparaíso, Valparaíso, Chile, for his expert statistical advice and assistance. Grant support was provided by the University of Valparaiso, Project DIPUV 052005.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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