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(Chest. 1999;115:75-84.)
© 1999 American College of Chest Physicians

Improvements in Lung Function, Exercise, and Quality of Life in Hypercapnic COPD Patients After Lung Volume Reduction Surgery*

Gerald M. O'Brien, MD, FCCP; Satoshi Furukawa, MD; Anne Marie Kuzma, RN, MSN; Francis Cordova, MD and Gerard J. Criner, MD, FCCP

* From the Division of Pulmonary & Critical Care Medicine, Department of Medicine and Cardiothoracic Surgery, Department of Surgery Temple University School of Medicine, Philadelphia, PA 19140.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: To determine the impact of preoperative resting hypercapnia on patient outcome after bilateral lung volume reduction surgery (LVRS).

Methods: We prospectively examined morbidity, mortality, quality of life (QOL), and physiologic outcome, including spirometry, gas exchange, and exercise performance in 15 patients with severe emphysema and a resting PaCO2 of > 45 mm Hg (group 1), and compared the results with those from 31 patients with a PaCO2 of < 45 mm Hg (group 2).

Results: All preoperative physiologic and QOL indices were more impaired in the hypercapnic patients than in the eucapnic patients. The hypercapnic patients exhibited a lower preoperative FEV1, a lower diffusing capacity of the lung for carbon monoxide, a lower ratio of PaO2 to the fraction of inspired oxygen, a lower 6-min walk distance, and higher oxygen requirements. However, after surgery both groups exhibited improvements in FVC (group 1, p < 0.01; group 2, p < 0.001), FEV1 (group 1, p = 0.04; group 2, p < 0.001), total lung capacity (TLC; group 1, p = 0.02; group 2, p < 0.001), residual volume (RV; group 1, p = 0.002; group 2, p < 0.001), RV/TLC ratio (group 1, p = 0.03; group 2, p < 0.001), PaCO2 (group 1, p = 0.002; group 2, p = 0.02), 6-min walk distance (group 1, p = 0.005; group 2, p < 0.001), oxygen consumption at peak exercise (group 1, p = 0.02; group 2, p = 0.02), total exercise time (group 1, p = 0.02; group 2, p = 0.02), and the perceived overall QOL scores (group 1, p = 0.001; group 2, p < 0.001). However, because the magnitude of improvement was similar in both groups, and the hypercapnic group was more impaired, the spirometry, lung volumes, and 6-min walk distance remained significantly lower post-LVRS in the hypercapnic patients. There was no difference in mortality between the groups (p = 0.9).

Conclusions: Patients with moderate to severe resting hypercapnia exhibit significant improvements in spirometry, gas exchange, perceived QOL, and exercise performance after bilateral LVRS. The maximal achievable improvements in postoperative lung function are related to preoperative level of function; however, the magnitude of improvement can be expected to be similar to patients with lower resting PaCO2 levels. Patients should not be excluded from LVRS based solely on the presence of resting hypercapnia. The long-term benefit of LVRS in hypercapnic patient remains to be determined.

Key Words: emphysema • hypercapnia • lung volume reduction surgery <1p;9q>


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Lung volume reduction surgery (LVRS) has been reported to improve lung function, exercise performance, and quality of life (QOL) in patients with severe emphysema.1 2 3 4 5 6 Patient selection based on initial lung function and gas exchange remains poorly characterized, but it is evolving. Resting hypercapnia has been reported by some investigators7 8 to be a contraindication for LVRS. Cooper et al9 reported that approximately 7% of the patients who are referred for LVRS are rejected because of the presence of resting hypercapnia. The absolute value used to exclude patients has remained arbitrary and poorly defined. In a report comparing preoperative patient characteristics with surgical outcomes of patients undergoing unilateral LVRS, hypercapnia was associated with a poor outcome.10

To determine the impact of preoperative resting hypercapnia on patient outcome after bilateral LVRS with stapling resection, we examined morbidity, mortality, QOL, and physiologic outcome (spirometry, gas exchange, and exercise performance) in patients with moderate to severe hypercapnia, and compared the results to those seen in eucapnic patients.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Design
From November 1994 to December 1996, 180 patients with severe end-stage emphysema were evaluated for LVRS. Forty-six patients were subsequently accepted as candidates and underwent bilateral LVRS. All of the patients were studied prospectively before surgery, and 3 to 6 months after LVRS according to the protocol as outlined in the remainder of this section. For the purpose of analysis, we retrospectively classified the patients into two groups based on the presence of resting hypercapnia. Group 1 was comprised of 15 patients whose resting preoperative PaCO2 was > 45 mm Hg. Group 2 was comprised of the remaining patients (n = 31).

Patient Selection
The criteria for inclusion or exclusion of prospective candidates are listed in Table 1 . All of the patients had stopped smoking at least 6 months before evaluation and remained symptomatic despite optimal medical therapy, which included bronchodilators, inhaled or oral corticosteroids, and home oxygen therapy. All patients were encouraged to complete 8 weeks of preoperative pulmonary rehabilitation before undergoing surgery.


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  		Table 1. Selection Criteria

 
Pulmonary Function Testing
Pulmonary function testing was performed at the time of evaluation and between 3 and 6 months after surgery. Tests were performed on a plethysmograph (System 6200, Autobox DL; SensorMedics; Yorba Linda, CA) using American Thoracic Society guidelines.11 The FVC, FEV1, and FEV1/FVC ratio were measured. Thoracic gas volumes were measured using plethysmography. Diffusion capacity was measured by single breath technique.12 The maximum voluntary ventilation (MVV) was measured directly by recording the maximal ventilatory volume achieved over a 15-s time period, and expressed in liters per minute.

Exercise Testing
Patients underwent incremental maximal treadmill exercise (model 9.4 SP; Precor; Bothell, WA) before surgery and between 3 and 6 months after LVRS. During the test, oxygen uptake, carbon dioxide production, oxygen pulse, minute ventilation and its variables, tidal volume, and respiratory frequency were continuously recorded by a metabolic cart (model 2900; SensorMedics). Oxygen saturation using a pulse oximeter (model N-200; Nellcor; Chula Vista, CA) and multiple-lead ECG (ECG Horizon; SensorMedics) were continuously recorded. Supplemental oxygen was individualized for each patient to prevent oxygen desaturation during exercise with the use of a high-flow blender delivering 30 or 40% fraction of inspired oxygen (FIO2) to a high-volume meteorological balloon that provides a flow-by circuit to the inspiratory port of a nonrebreathing valve. At the conclusion of each test, dyspnea was rated using a visual analog scale from 0 to 10 (severe breathlessness).13

On a different day, the total distance that the patient was able to walk in 6 min in a corridor was recorded. This was done before surgery and between 3 and 6 months after LVRS.

QOL Assessment
The sickness impact profile (SIP) is a sensitive, behaviorally based measure of sickness-related dysfunction that has been previously validated.14 The SIP is composed of 136 items that broadly cover the activities of daily living. It reflects the patient's perceptions of these activities. The scores are inversely proportional to the level of function and QOL. The SIP evaluation was administered to all potential candidates upon enrollment into the study. Measurements were repeated between 3 and 6 months following LVRS.

Surgical Technique
LVRS was performed via mediastinotomy (n = 35) or video-assisted thoracoscopy with bilateral stapling (n = 11). The goal of resection was to remove 20 to 40% of the volume of each lung. High-resolution CT of the chest and quantitative ventilation-perfusion scans were used to preoperatively target lung regions with the worst emphysema. At the conclusion of the operation, chest tubes were placed and were managed in the conventional manner.

Morbidity and Mortality
Early mortality is reported if death occurred within 30 days of surgery, and late mortality is defined if death occurred between 30 to 90 days after surgery. The duration of air leaks is reported as days for chest tube drainage. Lower respiratory tract infection was reported if the patient had temperature of > 38°C, had mucopurulent secretions, had a positive Gram's stain, and improved with antimicrobial therapy.

Data Analysis
Data are expressed as mean (± SD), except where otherwise noted. The statistical significance between baseline and post-LVRS data were determined by paired t test. Data that failed normality testing were analyzed using the Mann-Whitney test. Nonnumerical data were analyzed using the z test.

A p value of < 0.05 was considered statistically significant. All statistical analyses were conducted using a commercially available computer software program (SigmaStat 3.0; SPSS Inc.; Chicago, IL).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patient Characteristics
The demographic characteristics of each group are shown in Table 2 . There was no significant difference between the groups in terms of age, sex, or tobacco use. However, oxygen use was significantly higher among group 1 patients than among group 2 patients, respectively: 2 ± 1 vs 1 ± 1 L/min (p = 0.01).


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  		Table 2. Demographic Profiles of Groups 1 and 2

 
Preoperative spirometry, lung volumes, and gas exchange measures from both groups are shown in Table 3 . Group 1 patients had a significantly lower preoperative FEV1 than group 2 (p < 0.001). Moreover, group 1 patients had more gas trapping, as measured by the residual volume (RV; p = 0.002) and RV/total lung capacity (TLC) ratio (p < 0.001), a lower diffusion capacity (p = 0.01), and a lower PaO2/FIO2 ratio (p = 0.01).


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  		Table 3. Spirometry, Lung Volumes, and Gas Exchange Before LVRS of Groups 1 and 2

 
Exercise performance was worse among group 1 patients. The hypercapnic patients were able to walk significantly less on the 6-min walk test than the eucapnic patients, respectively: 197 ± 111 vs 300 ± 199 m (p = 0.01).

Physiologic Improvement Post-LVRS
Pulmonary Function: Spirometry is reported in 14 of the surviving patients (100%) in group 1 and in 27 of 28 surviving patients (96%) in group 2. One patient in group 2 could not complete postoperative testing because of ventilator dependence. One patient in each group was unable to perform body plethysmographic maneuvers; therefore, lung volume data are reported in 13 of 14 patients (93%) in group 1 and in 26 of 27 patients (96%) in group 2.

Post-LVRS data are presented in Tables 4 and 5 . The magnitude of post-LVRS improvements is presented in Table 6 . In both study groups, a significant increase in both FVC (group 1, 2.67 ± 0.69 vs 2.28 ± 0.88 L, p < 0.01; group 2, 2.91 ± 0.62 vs 2.53 ± 0.7 L, p < 0.001) and FEV1 (group 1, 0.73 ± 0.25 vs 0.55 ± 0.17 L, p = 0.04; group 2; 1.0 ± 0.32 vs 0.78 ± 0.20 L, p < 0.001) was noted post-LVRS (Fig 1 ). There was no significant difference in the magnitude of improvement in FVC and FEV1 between the groups; however, mean post-LVRS FEV1 was higher in group 2 than in group 1, respectively: 1.0 ± 0.32 vs 0.73 ± 0.25 L (p = 0.01).


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  		Table 4. Group 1: Pre- and Post-LVRS Spirometry, Lung Volumes, Gas Exchange, Exercise Performance, and Overall QOL (n = 14)

 

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  		Table 5. Group 2: Pre- and Post-LVRS Spirometry, Lung Volumes, Gas Exchange Exercise Performance, and Overall QOL Score (n = 27)

 

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  		Table 6. Percent Magnitude of Improvement after LVRS in Groups 1 and 2*

 


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  		Figure 1. A comparison of the improvements in spirometry, pre- and post-LVRS, in groups 1 and 2. Significant improvements were noted in both groups. There was no difference in the magnitude of improvement between the groups.

 
There were reductions in TLC (group 1, 7.0 ± 1.9 vs 8.0 ± 2.0 L, p = 0.02; group 2, 6.2 ± 1.8 vs 7.0 ± 1.5 L, p < 0.001), RV (group 1, 4.5 ± 1.8 vs 5.6 ± 1.5 L, p = 0.002; group 2, 3.3 ± 0.86 vs 4.3 ± 0.96 L, p < 0.001), and RV/TLC (group 1, 0.66 ± 0.22 vs 0.72 ± 0.07, p = 0.03; group 2, 0.51 + 0.08 vs 0.63 ± 0.07, p < 0.001) in both groups (Fig 2 ). The magnitude of improvements in these measurements was similar for both groups. Both the RV and the RV/TLC ratio were significantly lower in group 2 than in group 1 after LVRS (RV, 3.3 ± 0.86 vs 4.5 ± 1.8 L, p = 0.014; RV/TLC, 0.51 ± 0.75 vs 0.65 ± 0.07, p = 0.005).



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  		Figure 2. A comparison of the improvements in lung volumes, pre- and post-LVRS, in groups 1 and 2. Significant improvements were noted in both groups. There was no difference in the magnitude of improvement between the groups.

 
There was a trend toward a significant improvement in the diffusing capacity of the lung for carbon monoxide (DLCO) in group 2, but not in group 1, after LVRS (group 1, 6.43 ± 2.3 vs 5.24 ± 2.7 mL/min/mm Hg, p = 0.12; group 2, 8.9 ± 2.6 vs 8.0 ± 3.1 mL/min/mm Hg, p = 0.07). Although the magnitude of improvement in the DLCO was not significantly different between the groups, the post-LVRS DLCO was higher in group 2 than in group 1, respectively: 8.9 ± 2.6 vs 6.43 ± 2.3 mL/min/mm Hg (p = 0.004)

Gas Exchange
A significant reduction in the mean PaCO2 was seen in group 1 after LVRS (50 ± 9 vs 59 ± 7 mm Hg, p = 0.002); and a smaller, but also significant, decrease was seen in group 2 after LVRS (40 ± 3 vs 41 + 4 mm Hg, p = 0.02; Fig 3 ). Group 2, but not group 1, exhibited significant improvements in the PaO2/FIO2 ratio (group 1, 277 ± 45 vs 276 ± 54, p = 1.0; group 2, 365 ± 55 vs 341 ± 44, p = 0.002), and the magnitude of improvement in the PaO2/FIO2 was not significantly different between the groups. Moreover, the PaO2/FIO2 ratio was significantly higher in group 2 after LVRS than in group 1, respectively: 367 ± 55 vs 282 ± 43 (p < 0.001).



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  		Figure 3. A comparison of the improvements in resting PaCO2, pre- and post-LVRS, in groups 1 and 2. The mean PaCO2 improved significantly in both groups but did not reach normal levels in group 1 after LVRS.

 
Exercise Performance
Preoperative and postoperative 6-min walk distances were measured in 13 of 14 patients (93%) in group 1 and in 26 of 27 patients (96%) in group 2. The results are presented in Tables 4 and 5 . A significant improvement in the distance covered during this test was seen in both groups after LVRS (group 1, 274 ± 105 vs 197 ± 111 m, p = 0.005; group 2, 370 ± 84 vs 300 ± 99 m, p < 0.001; Fig 4 ). The percent change in the distance walked after LVRS was similar in groups 1 and 2.



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  		Figure 4. A comparison of the improvements in the 6-min walk distance, pre- and post-LVRS, in groups 1 and 2. Significant improvements were noted in both groups. There was no difference in the magnitude of the improvement between the groups.

 
Cardiopulmonary exercise testing was performed before and after LVRS in 6 of 14 group 1 patients (43%) and in 23 of 27 group 2 patients (85%). Both groups demonstrated significant improvements in cardiopulmonary exercise performance as measured by the oxygen consumption at peak exercise (O2max; group 1, 15.5 ± 3.4 vs 11.4 ± 1.4 mL/kg/min, p = 0.02; group 2, 16.5 ± 4.6 vs 14.3 ± 3.3 mL/kg/min, p = 0.02) and total exercise time (TET; group 1; 9.9 ± 2.0 vs 5.5 ± 2.1 min, p = 0.02; group 2, 8.6 ± 1.9 vs 6.4 ± 1.6 min, p = 0.02; Fig 5 ). The magnitude of percent improvement in O2max and TET in group 1 patients approached statistical significance (O2max, 11 ± 18 vs 25 ± 10%, p = 0.08; TET, 24 ± 22 vs 43 ± 20%, p = 0.06) in comparison to group 2. Moreover, there was no significant difference between the groups in O2max and TET after LVRS.



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  		Figure 5. A comparison of the improvements in maximal symptom limited exercise performance, pre- and post-LVRS, in groups 1 and 2. Significant improvements in both the O2 max and TET were noted in both groups. There was no difference in the magnitude of improvement between the groups.

 
The tidal volume measured at peak exercise (VTmax) improved in both groups after surgery (group 1, 1.20 ± 0.38 vs 0.80 ± 0.26 L, p = 0.005; group 2, 1.05 ± 0.34 vs 0.85 ± 0.22 L, p = 0.002). There was also a statistically significant improvement in minute ventilation at peak exercise (Emax) in both groups (group 1, 31 ± 6.2 vs 22.5 ± 6.4 L/min, p = 0.01; group 2, 33.5 ± 12.4 vs 29.2 ± 10.6 L/min, p = 0.01; Fig 6 ). Moreover, the percent magnitude of improvement in both the VTmax and the Emax between the groups was greater in group 1 than in group 2 (VTmax, 37.7 ± 6.4 vs 14.2 ± 18.7%, p = 0.004; Emax 26.5 ± 17.2 vs 10.3 ± 20%, p = 0.08).



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  		Figure 6. A comparison of the improvements in ventilatory function at maximal exercise, pre- and post-LVRS, in groups 1 and 2. Significant improvements in both the VTmax and Emax were noted in both groups. The improvement in VTmax was greater in group 1 (p = 0.004) and not statistically different for the Emax (0.08).

 
Quality of Life Analysis
The results of the perceived improvement in the overall QOL are reported in Tables 4 and 5 . There were significant improvements in the overall QOL scores in both groups (group 1, 22.3 ± 12.7 vs 9.6 ± 6.6, p = 0.001; group 2, 18.3 ± 11 vs 7.5 + 4.7, p < 0.001; Fig 7 ). There was no significant difference in the perceived post-LVRS QOL (group 1, 10.18 ± 11.1 vs group 2, 12.72 ± 8.0; p = 0.6), or in the magnitude of improvements in the overall SIP score between groups.



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  		Figure 7. A comparison of the improvements in the SIP score, pre- and post-LVRS, in groups 1 and 2. The scores are inversely proportional to the perceived overall QOL. The mean SIP score improved significantly in both groups. There was no difference in the magnitude of improvement between the groups.

 
Morbidity and Mortality
The morbidity and mortality statistics are demonstrated in Table 7 . There was one early death in group 1, resulting in an overall mortality rate of 7%. There were three late deaths in group 2, resulting in an overall mortality rate of 10%. There was no significant difference in mortality between the groups (p = 0.9). Moreover, there was no statistically significant difference between the groups in the number of hospitalization days (p = 0.17), critical care days (p = 0.7), lower respiratory tract infections (p = 0.9), or in the duration of air leaks (p = 0.5). Prolonged respiratory failure occurred in only one patient (in group 2), with an overall rate of 2% for both groups.


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  		Table 7. Morbidity and Mortality of Groups 1 and 2

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We have demonstrated that bilateral LVRS is effective and safe in patients with moderate to severe resting hypercapnia who would otherwise be candidates for this procedure. The hypercapnic patients in this study exhibited a lower preoperative FEV1, a lower DLCO, a lower PaO2/FIO2 ratio, a lower 6-min walk distance, and higher oxygen requirements. The percentage of improvements in FVC, FEV1, TLC, RV, and RV/TLC were no different in this group when compared to a eucapnic cohort. A significantly greater improvement in the resting PaCO2 was evident in the hypercapnic group than in the eucapnic group; however, the mean post-LVRS PaCO2 remained high in this group and did not return to normal levels. Moreover, improvements in cardiopulmonary exercise performance were noted in both groups. These data show that patients with moderate to severe hypercapnia can have significant improvement in lung function, exercise performance, and QOL without increased morbidity or mortality with LVRS.

Current selection criteria for the most optimal candidates for LVRS continue to evolve. Hypercapnia and decreased DLCO has been associated with a poor outcome in patients undergoing unilateral LVRS, as reported by Keenan and colleagues.10 Others have reported from their experience that advanced age and resting hypercapnia may be predictors of poor outcome.1 7 8 In many reported series, patients with resting hypercapnia were excluded as candidates.2 3 5 6 15 16 Other investigators have reported low mortality and significant improvements in lung function, 6-min walk distance, and dyspnea index among patients who underwent LVRS with a preoperative PaCO2 of >= 55 mm Hg.17 However, improvements in lung volumes, cardiopulmonary exercise performance, or gas exchange were not reported. Moreover, previously reported studies included patients who underwent both unilateral and bilateral LVRS, whereas we only report patients undergoing bilateral LVRS.

CO2 retention is variably demonstrated in patients with severe airflow obstruction. It is usually not observed unless the FEV1 is < 1 L or 35% of predicted. Although hypercapnia becomes more frequent with substantial decreases in the FEV1, many patients remain normocapnic even with severe airflow obstruction.18 19 20 21 22 Why CO2 retention develops in some COPD patients and not in others with comparable degrees of airflow obstruction has been an area of recent study. One factor may be that an individual patient's intrinsic hypoxic responsiveness is important in determining which patients hypoventilate in response to severe airflow obstruction. Several studies have demonstrated depressed chemical responses in hypercapnic COPD patients, which has been attributed to long-standing hypoxia or elevations in serum bicarbonate.23 24 Moreover, additional investigators have demonstrated that hypoxic and hypercapnic responses may be lower in relatives of patients who retain CO2.25 26

Besides chemical responsiveness, several investigators have shown that patients with hypercapnia have a more rapid and shallow breathing pattern that contributes further to increased dead space ventilation.27 28 29 30 A more rapid and shallow breathing is thought to be a compensatory mechanism that reduces inspiratory time, and thereby decreases the work of breathing and defending against the development of inspiratory muscle fatigue.

A reduction in inspiratory muscle strength in patients with COPD has been shown to correlate with the development of CO2 retention, such that, once maximum inspiratory pressure falls to < 50% of that predicted, the PCO2 rises linearly.31 The ratio of lung resistance to maximum inspiratory pressure has also recently been described a predictor of the development of hypercapnia in patients with COPD.32 Finally, a significant correlation has been shown between measured intrinsic positive end-expiratory pressure and arterial PCO2 in patients with severe COPD.33 This suggests that the inspiratory threshold loading effect of intrinsic positive end-expiratory pressure further burdens overtaxed respiratory muscles and, thereby, fosters CO2 retention by precipitating inspiratory muscle fatigue or by provoking a change to a more rapid and shallow breathing pattern that avoids fatigue.

It appears that a balance between the need to maintain effective gas exchange is counterbalanced by breathing strategies adopted by severely hyperinflated COPD patients to minimize inspiratory muscle work. These effects interact in a complex manner to foster the development of CO2 retention in patients with severe COPD. LVRS may be beneficial in these patients by reducing physiologic dead space, reducing airflow resistance, decreasing internal elastic load, and improving respiratory muscle strength generation.34 35 36 The importance of each of these proposed benefits, in isolation or in aggregate, remains an area of intense study.

Although the hypercapnic patients in this study exhibited significant improvement after LVRS, their lung function started out lower and thus remained lower after LVRS. The duration of follow-up in this study is short, and it is possible that the hypercapnic patients will exhibit a more rapid or earlier return to their preoperative level of function. Thus, the utility of LVRS as definitive therapy or as a bridge to transplantation in this group remains unanswered and requires further study.

In conclusion, we have demonstrated that patients with moderate to severe resting hypercapnia exhibit significant improvements in spirometry, gas exchange, 6-min walk distance, perceived QOL, and symptom-limited exercise performance after bilateral LVRS. The achievable postoperative lung function is related to preoperative level of function, as the magnitude of improvement can be expected to be similar to that seen in eucapnic patients. Patients should not be excluded from LVRS based solely on the presence of resting hypercapnia. A large prospective randomized trial will be necessary to determine the duration of benefit of LVRS among patients with resting hypercapnia.


   Footnotes
 
Correspondence to: Gerald M. O'Brien, MD, Assistant Professor of Medicine, Temple University School of Medicine, 437 Parkinson Pavilion, Philadelphia, PA 19140; e-mail: jerryo@astro.ocis.temple.edu

Abbreviations: DLCO = diffusing capacity of the lung for carbon monoxide; FIO2 = fraction of inspired oxygen; LVRS = lung volume reduction surgery; MVV = maximum voluntary ventilation; QOL = quality of life; RV = residual volume; SIP = sickness impact profile; TET = total exercise time; TLC = total lung capacity; Emax = minute ventilation at peak exercise; O2max = oxygen consumption at peak exercise; VTmax = tidal volume measured at peak exercise

Received for publication September 29, 1997. Accepted for publication June 18, 1998.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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