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Cardiac Imaging |
1 From the Institute of Diagnostic Radiology (J.K.W., D.W., J.E.R., B.M., P.R.H.), Clinic of Cardiovascular Surgery (M.L.), and Clinic of Cardiology (R.K., T.F.L.), University Hospital Zurich, Rämistrasse 100, 8091 Zurich, Switzerland; and Department of Biostatistics, University of Zurich, Switzerland (B.S.). From the 2001 RSNA scientific assembly. Received October 17, 2001; revision requested January 9, 2002; revision received February 8; accepted March 14. Address correspondence to D.W. (e-mail: dominik.weishaupt@dmr.usz.ch).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Prior to surgical valve replacement, 25 patients with aortic valve stenosis and sinus rhythm underwent nonenhanced (n = 15) and contrast-enhanced (n = 25) retrospectively ECG-gated multi–detector row CT. Two readers working in consensus evaluated image quality and assessed valvular morphology and the degree of valvular calcification. In addition, the diameter of the aortic valve annulus was measured. Results were compared with surgical and echocardiographic findings by using the paired sign test, 
statistics, and the method of Bland and Altman.
RESULTS: The aortic valve could be visualized nearly free of motion artifacts on all multi–detector row CT images. Image quality and diagnostic confidence for classification of aortic valve morphology were significantly superior on contrast-enhanced rather than nonenhanced images (P = .004 and P = .006, respectively). Nonenhanced and contrast-enhanced CT showed good agreement with surgical findings with regard to quantification of the degree of aortic valve calcification ( = 0.77 and = 0.74, respectively). Measurement of the diameter of the aortic valve annulus was more reliable on contrast-enhanced images.
CONCLUSION: Contrast-enhanced retrospectively ECG-gated multi–detector row CT allows determination of aortic valve morphology, measurement of the diameter of the aortic valve annulus, and assessment of the degree of aortic valve calcification in patients with aortic stenosis.
© RSNA, 2002
Index terms: Aortic valve, 535.12111, 535.12112, 535.12115 • Arteries, calcification, 535.817 • Computed tomography (CT), multi–detector row, 535.12111, 535.12112, 535.12115
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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To further broaden cardiac application of multi–detector row CT, it may be desirable to evaluate valvular morphology. Although first experiences in the diagnosis of aortic valve stenosis with the use of electron-beam CT have been reported (5), the limited availability of this imaging modality, as well as technical limitations, may have hampered its use for this purpose. Insufficient temporal resolution with consecutive motion artifacts has rendered conventional and single–detector row helical CT of little value for imaging the aortic valve.
The introduction of the latest generation of multi–detector row CT systems with short acquisition times due to simultaneous acquisition of four transverse sections, half-second scanner rotation, and advanced ECG-gated reconstruction algorithms permits evaluation of the cardiac structures with a temporal resolution of up to 250 msec (6). This technique minimizes cardiac motion artifacts, which is mandatory for valvular imaging.
Investigators in several studies have identified the presence and extent of valvular calcification in patients with aortic valve stenosis as an important predictor of clinical outcome (7,8). Moreover, calcification of stenotic and nonstenotic aortic valves may reflect generalized atherosclerosis (9,10). Preoperative knowledge about anatomic details of the aortic valve is of great interest to the cardiac surgeon, since the aortic valve replacement procedure itself and the type of valve prosthesis to be implanted depend on various parameters, including aortic valve morphology and diameter, as well as the presence and extent of aortic valve and annulus calcification (11–15). These findings emphasize the importance of noninvasive aortic valve imaging, including the degree and extent of valvular calcification in patients with aortic valve stenosis.
Echocardiography has emerged as the method of choice in the evaluation of patients with valvular disease, enabling a comprehensive assessment of anatomic and hemodynamic status (16). However, transthoracic echocardiography, with quantification of the extent of valvular calcification, may be difficult to perform in the elderly and in patients with thick chest walls, small hearts, and chest deformities (17). In addition, echocardiography is operator dependent (18). Since CT is a sensitive method for the detection of calcification (19), multi–detector row CT is potentially useful for the assessment of aortic valve morphology and quantification of the degree of calcification.
The purpose of this study was to evaluate the applicability and image quality of nonenhanced and contrast-enhanced multi–detector row CT combined with retrospective ECG gating for visualization of the aortic valve, determination of aortic valve morphology and diameter of the aortic valve annulus, and assessment of the degree of valvular calcification in patients with aortic valve stenosis, as compared with results of surgery and echocardiography.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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All 25 patients underwent preoperative contrast-enhanced multi–detector row CT with retrospective ECG-gating. In the first 15 of these 25 patients, additional nonenhanced retrospectively ECG-gated multi–detector row CT was performed prior to administration of the iodinated contrast agent. After performing a preliminary statistical analysis of the CT findings of these 15 patients, we determined that the differences between nonenhanced and contrast-enhanced CT with regard to image quality and reader confidence for determination of aortic valve morphology were highly statistically significant. To reduce patient irradiation dose, the remaining 10 patients underwent only contrast-enhanced retrospectively ECG-gated multi–detector row CT.
Surgical aortic valve replacement was performed in all 25 patients, with a mean delay of 4 days (range, 1–55 days) between CT and surgery. The indications for aortic valve replacement were based on clinical and echocardiographic findings. According to echocardiographic results, additional mild aortic regurgitation was present in 16 (64%) of 25 patients, and additional mild-to-moderate or moderate aortic regurgitation was present in two (8%) patients. Mild mitral valve regurgitation was also present in 15 (60%) patients, mild tricuspid valve regurgitation was present in eight (32%) patients, and mild mitral valve stenosis was present in one (4%) patient. Clinically, 15 (60%) of the 25 patients experienced dyspnea.
Imaging Technique
All multi–detector row CT scans were performed with a Somatom Volume Zoom multi–detector row CT scanner (Siemens, Forchheim, Germany), with simultaneous acquisition of four sections. The scan was planned by acquiring a scout image starting at the level of the aortic root above the coronary ostia and ending at the supradiaphragmatic base of the heart. This procedure represents the standard protocol for multi–detector row CT evaluation of the heart at our institution. The mean craniocaudal distance of the volume data set for coverage of the heart was 11 cm (range, 10–12 cm). All imaging was performed in inspiratory breath hold, preceded by mild hyperventilation with oxygen-enriched air (4 L/min).
Contrast-enhanced multi–detector row CT was performed by administering 120 mL of iodixanol (Visipaque 270; Nycomed Amersham Imaging AS, Oslo, Norway) via a 20-gauge needle placed in an antecubital vein. The flow rate of the contrast agent was 3 mL/sec with use of an automated injector (Ulrich, Ulm-Jungingen, Germany). To achieve optimal contrast enhancement, delay time was determined individually for each patient before CT scanning. Ten consecutive transverse images at the level of the aortic valve were obtained every 2 seconds without table feed, starting 12 seconds after injection of a 20-mL test bolus of iodixanol. Delay times were determined by visually evaluating the contrast material at the level of the aortic valve. The mean delay between start of injection of contrast material and start of CT scanning was 21 seconds (range, 18–26 seconds).
Nonenhanced and contrast-enhanced CT data were collected in helical mode, with simultaneous acquisition of four parallel sections with 1-mm collimation. The appropriate helical pitch was determined prior to the examination for each patient, depending on the heart rate. In our patient population, the pitch range was 0.3–0.5. The gantry rotation time was 500 msec, and the patient table was continuously advanced at a rate of 2.5–4.5 mm/sec. The tube current was 140 mAs at 120 kV. ECG signal from the patient was simultaneously recorded during CT data acquisition. With the use of a software program (WinDose, version 2.1a; Scanditronix-Wellhöfer Dosimetrie, Schwarzenbruck, Germany) (20), the effective radiation dose of contrast-enhanced CT for a mean craniocaudal scanning range of 11 cm and a tube current of 140 mAs at 120 kV was estimated to be 3.1 mSv for women and 2.3 mSv for men. Briefly, the effective radiation dose calculations in this software program are based on Monte Carlo calculations for anthropomorphic mathematic phantoms that were obtained by the GSF National Research Center for Environment and Health (Neuherberg, Germany) (20). By entering different scan parameters, including collimation, pitch, kerma, tube current, tube voltage, scanning range, and anatomic area, as well as patient characteristics, the software program is able to provide an estimation of effective irradiation dose (20).
All multi–detector row CT data were reconstructed by using the manufacturer’s software on a commercially available workstation (VolumeZoom Navigator; Siemens). Since retrospective ECG gating was used in our study, only data acquired within a predefined interval of the cardiac cycle were used for image reconstruction during diastole. The "absolute-reverse" strategy described by Ohnesorge et al (6) was used for determination of cardiac cycle reconstruction. Briefly, the absolute-reverse strategy requires the use of a constant reconstruction interval prior to the next R wave of the ECG signal. The average interval relative to the R peaks of the ECG signal was 450 msec, depending on the heart rate of the patient (mean, 67 bpm; range, 55–92 bpm). Images were reconstructed with a section thickness of 1.25 mm and a reconstruction increment of 0.8 mm. The field of view was 18 cm, with an image matrix of 512 x 512 pixels. One data set was reconstructed per patient.
Both nonenhanced and contrast-enhanced CT were performed successfully in all patients, without any complications. All patients were able to hold their breath during CT data acquisition (scan time, 22–40 seconds).
Image Analysis
Image analysis was performed in a consensus reading by two experienced radiologists (D.W., P.R.H.) on a separate computer workstation (SIENET Magic View; Siemens). Readout was performed on the basis of transverse source images and multiplanar reformations reconstructed on the workstation by the readers themselves. Multiplanar reformation routinely included sagittal and coronal reformations of the aortic valve. In addition, double-oblique reformations of the aortic valve were constructed on the basis of sagittal images. The optimal window settings for assessing the multiplanar reformations were evaluated for each patient individually by both radiologists, who analyzed all images. For assessing morphology of the aortic valve and diameter of the aortic valve annulus, mean window width was 600 HU, and mean center level was 80 HU. For quantification of the extent of aortic valve calcification, mean window width was 1,500 HU, and mean center level was 450 HU. Nonenhanced and contrast-enhanced images were assessed separately and interpreted in random order. There was a 4-week delay between the evaluation of nonenhanced and contrast-enhanced images. Both readers were blinded to all patient data, including clinical history and clinical findings, severity of aortic valve stenosis, and findings at echocardiography and surgery. The readers were only aware of the fact that stenosis of the aortic valve was present in all patients.
Aortic valve image quality was ranked for diagnostic purposes for both nonenhanced and contrast-enhanced images as follows: grade 1, nondiagnostic (delineation of the anatomic details of the aortic valve not possible); grade 2, poor but still diagnostic (poor visibility of the anatomic details of the aortic valve, including aortic valve leaflets, free edges of the aortic valve leaflets, and aortic valve annulus); grade 3, good (good visibility of the anatomic details of the aortic valve); and grade 4, excellent (excellent visibility of the anatomic details of the aortic valve). Motion artifacts at the level of the aortic valve were noted.
Both readers were asked to classify the morphology of the aortic valve (bicuspid vs tricuspid) on nonenhanced and contrast-enhanced images. In addition, both readers had to provide their diagnostic confidence for their choice of morphology by using a three-point Likert scale: 1, choice possibly correct; 2, choice probably correct; and 3, choice definitively correct.
The degree of calcification of the aortic valve was graded as follows: grade 1, no calcification; grade 2, mild calcification (small isolated spots of calcification); grade 3, moderate calcification (multiple larger spots of calcification); and grade 4, heavy calcification (extensive calcification of all aortic valve leaflets) (Fig 1). This grading system was adapted from Rosenhek et al (7).
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The mean time required for interpretation of aortic valve morphology and determination of both the diameter of the aortic valve annulus and the degree of calcification was 150 seconds (range, 120– 170 seconds).
Surgery
All 25 patients in our study underwent aortic valve replacement, which was performed by one cardiac surgeon (M.L.). The surgeon was asked to classify aortic valve morphology (bicuspid vs tricuspid) and to assess the degree of calcification of the aortic valve by using the same grading system that was used for the evaluation of the CT images (Fig 1). After the aortic valve had been resected and the annulus débrided, the aortic valve annulus was sized as described elsewhere (21). The surgically determined mean diameter of the aortic valve annulus of the 25 patients with aortic valve stenosis was 2.38 cm ± 0.20 (SD).
Echocardiography
Echocardiography was performed in all patients by using a commercially available ultrasonographic (US) system (Sequoia 512; Acuson, Mountain View, Wash). All patients underwent a comprehensive examination, including M-mode echocardiography, two-dimensional echocardiography, and conventional and Doppler US, performed by one experienced echocardiographer (R.K.). The result of the classification of aortic valve morphology (bicuspid vs tricuspid) and the echocardiographically determined mean aortic valve pressure gradient (in millimeters of mercury) was used for further comparison and correlation.
Statistical Analysis
The diameter of the aortic valve annulus was given as mean ± SD. The Mann-Whitney U test was used to compare heart rates of patients with and patients without motion artifacts at the level of the aortic valve. The paired sign test was used to compare both the image quality of the aortic valve and the levels of confidence for classification of morphology on nonenhanced and contrast-enhanced images. The paired sign test was also used to compare the degree of aortic valve calcification on CT images with surgical results. Spearman rank correlation was used to assess the correlation between degree of aortic valve calcification on the basis of CT images and mean aortic valve pressure gradients on the basis of transthoracic Doppler echocardiographic results. Interobserver agreement between findings at CT and surgery for grading the degree of aortic valve calcification was determined by calculating values. values of agreement were interpreted as poor ( = 0), slight ( = 0.01–0.20), fair ( = 0.21–0.40), moderate ( = 0.41– 0.60), good ( = 0.61–0.80), and almost perfect ( = 0.81–1.00) (22). Measurements of the diameter of the aortic valve annulus obtained on CT images and during surgery were compared by using the Wilcoxon signed rank test. The method by Bland and Altman (23) was used for the analysis of differences between measurements of the diameter of the aortic valve annulus obtained at CT and during surgery. The differences in measurements were plotted against their means (23). Briefly, the mean of the differences between values provided a measure of the bias or systematic error between the CT method and the surgical method. The SD of the differences represented the variability between the techniques, with bias of plus or minus 1.96 (SD) denoting the limits of agreement. P values of less than .05 were considered to indicate a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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= 0.77 and = 0.74, respectively). In 13 (87%) of 15 patients, the grade of aortic valve calcification as assessed on nonenhanced images matched exactly with the calcification grade given during surgery. By using contrast-enhanced images, both readers graded the degree of aortic valve calcification as equal to the grade given by the cardiac surgeon in 21 (84%) of 25 patients. Overall, there was no statistically significant difference between nonenhanced and contrast-enhanced CT compared with surgery when assessing the degree of aortic valve calcification (P = .5 and P = .99, respectively) (Fig 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Because of the limited temporal resolution of conventional and single–detector row CT scanners, reliable visualization of the aortic valve has not been possible so far. Investigators in a preliminary study of a small patient population suggested that electron-beam CT may be used to visualize the aortic valve (5).
In our prospective study, we investigated the clinical applicability and image quality of retrospectively ECG-gated multi–detector row CT for the assessment of the aortic valve in 25 patients with aortic valve stenosis. To our knowledge, we were able to demonstrate for the first time that the aortic valve can be visualized nearly free of motion artifacts by using nonenhanced and contrast-enhanced multi–detector row CT in patients with sinus rhythm. The slight heartbeat-related motion artifacts that were present in eight of 25 patients on nonenhanced and contrast-enhanced images did not result in nondiagnostic images in any patient. Upcoming future improvements in software and hardware, allowing imaging with even higher temporal resolution, may render the technique even more robust and further help suppress heartbeat-related motion artifacts. In addition, further improvements in reconstruction software are underway, which will allow manual selection of the optimal reconstruction interval prior to the R peak of the ECG signal for each cardiac cycle instead of reconstruction at a fixed time during the cardiac cycle. This may result in a reduction of motion artifacts, particularly in patients with arrhythmias.
Since, in our study, contrast-enhanced images allowed better delineation of the anatomic details of the aortic valve, image quality of the contrast-enhanced images was ranked higher than that of the nonenhanced images. The better visibility of the anatomic details of the aortic valve through the use of contrast-enhanced CT is also reflected by the fact that there was 100% agreement in classifying aortic morphology (bicuspid vs tricuspid) when compared with that of surgical or echocardiographic results. Moreover, the smaller mean difference of the diameter of the aortic valve annulus obtained by using contrast-enhanced instead of nonenhanced images (with surgery as the standard of reference) favors contrast-enhanced multi–detector row CT for the assessment of aortic valve morphology even further. Although our results have demonstrated that contrast-enhanced images outperform nonenhanced images with regard to visibility of anatomic details, assessment of aortic valve morphology, and measurement of the aortic valve annulus, the optimal concentration of iodinated contrast medium for this purpose is unclear. Results of further studies will show if a reduced iodine concentration will enhance aortic valve assessment as demonstrated for evaluation of the thoracic aortic wall (25).
Preoperative knowledge concerning aortic valve morphology, the diameter of the aortic valve annulus, and the presence of aortic valve and annulus calcification is desirable for planning surgical valve replacement. The presence of a bicuspid or tricuspid aortic valve influences the surgical approach. In a series of 84 patients who underwent stentless aortic root replacement, the presence of a bicuspid aortic valve was identified as a risk factor for postoperative coronary complications (11). In a study of 47 patients with supra- or subvalvular aortic valve stenosis, Delius et al (12) concluded that patients with a bicuspid aortic valve may be better palliated with a definitive surgical procedure, such as the Ross or Ross-Konno procedure, than with repair of the aortic valve. The influence of aortic valve annulus diameter on postoperative mortality is shown by Medalion et al (13). They have shown a trend toward a higher postoperative mortality in patients over 80 years of age with a small aortic valve annulus when a 19-mm aortic valve was implanted. These patients with a small aortic valve annulus would benefit from an operative aortic valve annulus enlargement combined with aortic valve replacement (14).
Since contrast-enhanced multi–detector row CT allows precise preoperative assessment of aortic valve annulus diameter when compared with intraoperative sizing, preoperative measurement of the aortic valve annulus by using multi–detector row CT may facilitate the planning of optimal surgical management of aortic valve disease, especially in the subgroup of elderly patients with a small aortic valve annulus (14). Preoperative awareness of extent and exact localization of aortic valve and annulus calcification may be useful for the cardiac surgeon, since extensive calcification may lead to technical difficulties during surgery (15). Placement and fixation of the aortic valve prosthesis into the aortic valve annulus, as well as reinsertion of proximal coronary arteries after aortic root replacement, are complicated by calcification of the aortic valve annulus and aortic root (15). Moreover, the degree of valvular calcification is an important predictor of outcome in patients with asymptomatic aortic valve stenosis (7,8). In a prospective study, Rosenhek et al (7) showed that the presence of moderate or severe aortic valve calcification in asymptomatic patients with aortic valve stenosis, in conjunction with a rapid increase in aortic jet velocity as measured by means of echocardiography, identifies patients with a poor prognosis. The authors concluded that asymptomatic patients with moderate to severe aortic valve calcification should be considered for early valve replacement rather than have surgery delayed until symptoms develop. By using multivariable regression analysis, Bahler et al (8) demonstrated that the rate of progression of aortic valve stenosis was more rapid when aortic valve leaflet calcification was more marked. The clinical importance of aortic valve calcification in this setting is emphasized by the results of Boon et al (9). The authors of that study concluded that a calcified stenotic or nonstenotic aortic valve should be considered as a manifestation of generalized atherosclerosis.
All these findings underline the need for a noninvasive imaging modality that allows reliable detection and grading of aortic valve calcification, as we were able to demonstrate with retrospectively ECG-gated multi–detector row CT. Clearly, more studies are needed before this method becomes a part of clinical practice. Since multi–detector row CT allows detection and reliable grading of the degree of aortic valve calcification, it may be used in the future to select asymptomatic patients for surgery before symptoms occur.
Surprisingly, the results of our study have demonstrated a moderate but significant correlation between degree of aortic valve calcification assessed on nonenhanced or contrast-enhanced images and mean aortic valve pressure gradient obtained with transthoracic Doppler echocardiography. This implies a potential use of multi–detector row CT in monitoring patients with aortic valve stenosis in different stages of the disease. However, future studies with greater numbers of patients are needed to validate these hypotheses.
There is no doubt that at present, transthoracic Doppler echocardiography is the primary imaging modality used in the noninvasive assessment of aortic valve stenosis. Doppler echocardiography provides an expeditious evaluation of the aortic valve, including valve morphology and determination of mean aortic valve pressure gradient (10,16). Although echocardiography allowed a conclusive evaluation of the aortic valve in all patients in this study, in general, the main drawback of transthoracic echocardiography is that it may be inadequate in up to 20% of adult patients, because obesity, pulmonary disease, and chest wall deformities interfere with image quality (17,18). In addition, echocardiography is limited with regard to quantification of aortic valve calcification, since only indirect signs, such as increased echogenicity and thickening of the aortic valve leaflets, are used (10). For those patients in whom transthoracic echocardiography was not successful or revealed equivocal findings, multi–detector row CT may serve as an alternative imaging modality. Results of future studies will show whether multi–detector row CT allows an even more objective quantification of aortic valve calcification by introducing a calcium score, as was recently demonstrated by Kizer et al (26) for quantification of aortic valve calcification by using electron-beam CT. If multi–detector row CT can allow reliable quantification of aortic valve calcification, this would enhance its use, for example, in the longitudinal assessment of calcification and its response to potential medical therapies.
The major drawback of using multi–detector row CT for imaging of the aortic valve is the potential hazardous irradiation that limits repetitive scanning. In our study, an effective irradiation dose of about 3 mSv was calculated. This effective irradiation dose may be lowered if scanning range is focused on the area of interest (aortic valve) only and if ECG-controlled dose-modulation techniques are implemented (27). By using a prospectively ECG-controlled online modulation of the tube output during heart phases that are not likely to be targeted by the following ECG-gated image reconstruction, Ohnesorge et al (27) were able to achieve an irradiation dose reduction of up to 50%. Recently, Wildberger et al (28) demonstrated that an individually adapted multi–detector row CT protocol with a body weight–based tube current did not significantly alter the image quality of chest multi–detector row CT images while achieving a mean reduction of irradiation exposure of 45%, compared with the standard protocol. Future studies, however, are needed to evaluate whether an adapted multi–detector row CT protocol is useful for imaging the aortic valve.
We acknowledge several limitations of our study. Since we only included patients who were scheduled for surgery of the aortic valve, this potentially could have led to an inclusion bias, because all of the patients in our study population suffered from moderate or severe aortic valve stenosis. We chose to investigate only this subgroup of patients to specifically compare the intraoperative status of the aortic valve with the preoperative multi–detector row CT results. Clearly, more data obtained from a larger patient group are needed to evaluate if the technique is also useful for aortic valve imaging in patients with absent or slight aortic valve stenosis. In the present study, we performed reconstruction of all multi–detector row CT data in a fixed time interval during diastole. Image quality may be improved by varying the reconstruction interval during the heart cycle as demonstrated for visualization of coronary arteries (1,29). Lastly, the grading and measurements reported have not been evaluated for interobserver variability.
In conclusion, to our knowledge the results of our preliminary study demonstrate for the first time that contrast-enhanced multi–detector row CT, performed in conjunction with retrospective ECG gating, allows high-quality imaging of the aortic valve. Determination of aortic valve morphology and accurate measurement of the diameter of the aortic valve annulus are superior to those achieved by using nonenhanced multi–detector row CT. When compared with surgery, the degree of aortic valve calcification can be reliably assessed on both nonenhanced and contrast-enhanced multi–detector row CT images. Results of future studies will demonstrate whether, with increasing experience, a diagnostic niche will open up for assessment of the aortic valve by using multi–detector row CT and whether this new technique will affect the optimal therapeutic management of aortic valve stenosis.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, J.K.W., D.W.; study concepts, J.K.W., D.W., R.K., M.L.; study design, J.K.W., D.W.; literature research, J.K.W.; clinical studies, J.K.W., R.K., M.L.; data acquisition and analysis/interpretation, J.K.W., D.W., P.R.H.; statistical analysis, J.K.W., B.S.; manuscript preparation, J.K.W., D.W.; manuscript definition of intellectual content, editing, revision/review, and final version approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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