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Published online before print November 30, 2007, 10.1148/radiol.2462062166
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(Radiology 2008;246:553-561.)
© RSNA, 2007

Obstetric Imaging

Reliability and Validity of MR Image Lung Volume Measurement in Fetuses with Congenital Diaphragmatic Hernia and in Vitro Lung Models1

Karen A. Büsing, MD, A. Kristina Kilian, MD, Thomas Schaible, MD, Angelika Debus, Christel Weiss, MD, and K. Wolfgang Neff, MD, PhD

1 From the Departments of Clinical Radiology (K.A.B., A.K.K., A.D., K.W.N.), Pediatrics (T.S.), and Biomathematics (C.W.), University Hospital Mannheim, University of Heidelberg, Theodor Kutzer Ufer 1-3, 68167 Mannheim, Germany. Received December 20, 2006; revision requested February 22, 2007; revision received March 21; accepted April 25; final version accepted August 1. Address correspondence to K.A.B. (e-mail: karen.buesing{at}rad.ma.uni-heidelberg.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Purpose: To prospectively assess the reliability of magnetic resonance (MR) image volume measurement in fetuses with congenital diaphragmatic hernia (CDH) and the reliability and validity of measurements in in vitro lung models.

Materials and Methods: This study was approved by the ethics committee, and informed consent was obtained. MR fetal lung volume (FLV) was measured in 40 consecutive fetuses with CDH by using half-Fourier acquired single-shot turbo spin-echo MR imaging and true fast imaging with steady-state precession at 24–36 weeks gestation (mean gestational age, 30.6 weeks ± 3.5 [standard deviation]). Lung volumes were independently assessed in three orthogonal section planes by two experienced observers. Additionally, 28 in vitro lung models of defined volumes of 1–60 mL were evaluated the same way. To assess measurement validity and reliability, the intraclass correlation coefficient (ICC) and the Bland-Altman plot were used.

Results: The interobserver reliability was high for both the lung models and FLV measurements (ICC, 0.999 and 0.928, respectively). Measurement validity was also good, with a mean difference between the calculated volume and the true volume of 0.4 mL (95% confidence interval: 0.30, 0.48). Measurement reliability and validity did not depend, to any considerable degree, on imaging plane or sequence (ICC range, 0.878–0.999) or on total volume.

Conclusion: The reliability and validity of MR volume measurements are high. The method is independent of the sequence and the imaging plane and can be performed with a very good interobserver agreement, even in small volumes.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
For most newborns in whom congenital diaphragmatic hernia (CDH) is an isolated anomaly, the degree of associated pulmonary hypoplasia represents the major determinant of survival (1–6). With the introduction of new therapeutic strategies, including gentle ventilation with permissivehypercarbia, high-frequency oscillatory ventilation, delayed surgery, and extracorporeal membrane oxygenation therapy, the prognosis in children with CDH has improved over the past decade, with neonatal survival rates increasing from less than 20% to more than 80%, as reported by numerous tertiary perinatal centers (7–12). The improvement in prognosis is further a result of a substantial increase in the proportion of prenatally diagnosed cases and subsequent delivery of infants at specialized centers (8). For infants with respiratory failure within the first 24 hours of life, prompt intensified care is known to improve survival, whereas neonatal transfer to a specialized center may well increase mortality (8,13–16).

Magnetic resonance (MR) imaging has been used to measure antenatal lung volume and quantify fetal pulmonary hypoplasia. For this, the lung volume measured at planimetry is expressed as a percentage of the predicted lung volume calculated with biometric fetal parameters (17–21). This ratio has been referred to as the relative lung volume and taken as a prognostic indicator in fetuses with pulmonary hypoplasia caused by CDH (17,19,20). Thus far, several investigators independently found that mortality was significantly increased when the relative fetal lung volume (FLV) was less than 25% (17), less than 30% (19), less than 35% (20), and less than 40% (22) of the predicted lung volume. However, in order to use relative lung volume as a clinical tool, it must be both reliable and valid (23).

Ward et al (24) have adequately assessed the reliability of MR FLV measurement in healthy fetuses. In fetuses with hypoplastic lungs, however, there is only evidence for good interobserver reliabil-ity (intraclass correlation coefficient [ICC], 0.95) (22). Furthermore, to our knowledge, the validity of FLV measurements has not been satisfactorily evaluated. Two studies in animals available so far have generated contradictory results, possibly as a consequence of the standard of reference used (25,26). Thus, our study aimed to prospectively assess the reliability of MR image volume measurement in fetuses with CDH and the reliability and validity of measurements in in vitro lung models.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Patients
Between June 2005 and March 2006, 40 consecutive women with singleton pregnancies and the diagnosis of fetal CDH were referred to our center for MR imaging and further therapeutic counseling shortly after primary diagnosis was determined by performing ultrasonography (US) at the referring institution. Written informed consent was obtained from all women, and the study received institutional approval from the research ethics committee of the University Hospital Mannheim, Mannheim, Germany. Mean maternal age was 30.6 years ± 5.7 (standard deviation), and age range was 17–40 years. Mean gestational age at MR imaging was 30.6 weeks ± 3.5 (range, 24–36 weeks). CDH was left sided in 32 fetuses and right sided in six fetuses. In two fetuses, hernias were bilateral.

In Vitro Lung Models
With gelatin and handmade lung-shaped plastic sheaths, a total of 28 artificial lung models of defined volumes between 1 and 60 mL were constructed by two of the authors (K.A.B. and A.D.). Prior to carrying out the final MR image volume measurements, potential alterations of the gelatin volume during processing were assessed. This was done by filling a measuring cup with 1 L of warm liquid gelatin and evaluating the volume changes until the medium solidified. In this way, we twice observed a volume loss of 5% from warm to cold liquid gelatin, but no further alterations in volume could be detected until the medium had congealed. Therefore, we only used cold liquid gelatin to prepare our samples.

With a pipette, small samples (1–11 mL) were filled in 1-mL steps, and samples up to 30 mL were constructed in 2-mL steps. Thereafter, we assembled lung phantoms with volume differences of 2.5 mL (range, 30–40 mL), 5 mL (range, 40–50 mL), and 10 mL (range, 50–60 mL).

MR Imaging and Volumetry
MR imaging in patients and lung phantoms was performed with a 1.5-T supraconducting system (Avanto; Siemens Medical Solutions, Erlangen, Germany) by using a six-element phased-array body coil. T2-weighted MR images were obtained by using the half-Fourier acquired single-shot turbo spin-echo (SE) sequence, with repetition time msec/echo time msec of 1000/166 and a flip angle of 150°, followed by the true fast imaging with steady-state precession (FISP) sequence, with 3.6/1.5 and a flip angle of 59°. All sequences were performed with a 4-mm section thickness, no intersection gap, a 512 x 512 matrix, and one signal acquired. The average duration was 15–20 seconds for the half-Fourier acquired single-shot turbo SE sequence and 8–14 seconds for the true FISP sequence. Sections were oriented in the transverse, coronal, and sagittal planes relative to the fetal lungs and lung models. Sequences in which degradation by fetal motion artifacts occurred were repeated to obtain images that included the whole thorax in a single acquisition and that allowed parietal and mediastinal boundaries to be clearly identified (Fig 1). No sedative medication was administered to reduce fetal movements.


Figure 1A
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  		Figure 1a: (a, b) Coronal and (c) transverse views of left-sided CDH in a fetus at 32 weeks gestation by using (a, c) half-Fourier acquired single-shot turbo SE MR imaging (1000/166; flip angle, 150°) and (b) true FISP MR imaging (3.6/1.5; flip angle, 59°; section thickness, 4 mm) with FLV measurement of right lung.

 

Figure 1B
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  		Figure 1b: (a, b) Coronal and (c) transverse views of left-sided CDH in a fetus at 32 weeks gestation by using (a, c) half-Fourier acquired single-shot turbo SE MR imaging (1000/166; flip angle, 150°) and (b) true FISP MR imaging (3.6/1.5; flip angle, 59°; section thickness, 4 mm) with FLV measurement of right lung.

 

Figure 1C
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  		Figure 1c: (a, b) Coronal and (c) transverse views of left-sided CDH in a fetus at 32 weeks gestation by using (a, c) half-Fourier acquired single-shot turbo SE MR imaging (1000/166; flip angle, 150°) and (b) true FISP MR imaging (3.6/1.5; flip angle, 59°; section thickness, 4 mm) with FLV measurement of right lung.

 
MR images were transferred to a workstation (Leonardo; Siemens Medical Solutions), and volumes were assessed by using volume analysis software (Argus; Siemens Medical Solutions). MR images were reviewed independently by two radiologists (K.A.B. and A.K.K., each with 4 years of experience in fetal MR imaging). The two observers were unaware of each other's results and the true volumes of the lung models. For both fetuses and models, segmentation was performed by using semiautomatic hand tracing of a free-form region of interest on consecutive sections in all three imaging planes. This method allows several ways of drawing a region of interest: exclusively by hand tracing, by using an automatic drawing tool capable of drawing a line along a border of high tissue contrast, or by combining both techniques. For the fetuses, the region of interest followed the lung boundaries and did not include the main vessels of the pulmonary hila (Figs 1 and 2). The volume of each region of interest obtained per image was automatically calculated (based on the cross-sectional area and section thickness), and the calculated volumes were added up to determine the volume of the entire lung. This calculation was repeated for each orthogonal image plane in every fetus and each lung model. The mean time required to perform the measurements for one set of data was about 15–20 minutes (range, approximately 10–25 minutes).


Figure 2A
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  		Figure 2a: Lung volume measurement in gelatin lung model of 4–7 mL imaged with (a) half-Fourier acquired single-shot turbo SE and (b) true FISP sequences and (c) that of 12 mL imaged with half-Fourier acquired single-shot turbo SE sequence. Parameters are the same as in Figure 1.

 

Figure 2B
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  		Figure 2b: Lung volume measurement in gelatin lung model of 4–7 mL imaged with (a) half-Fourier acquired single-shot turbo SE and (b) true FISP sequences and (c) that of 12 mL imaged with half-Fourier acquired single-shot turbo SE sequence. Parameters are the same as in Figure 1.

 

Figure 2C
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  		Figure 2c: Lung volume measurement in gelatin lung model of 4–7 mL imaged with (a) half-Fourier acquired single-shot turbo SE and (b) true FISP sequences and (c) that of 12 mL imaged with half-Fourier acquired single-shot turbo SE sequence. Parameters are the same as in Figure 1.

 
Statistical Analysis
Reliability, the capability of a method to give the same results in the same observer on different occasions (intraobserver reliability) or with different observers on the same occasion (interobserver reliability), expresses the reproducibility of a method. Validity assesses whether a test is actually measuring what it is purporting to measure and therefore expresses the measurement accuracy. We examined the two parameters as follows: (a) We used the t test for two-tailed paired samples to determine whether there was a significant difference between the mean values resulting from the same measurements made with two different conditions. If there were more than two different conditions (ie, imaging planes), we used analysis of variance for repeated measurements instead. (b) We used the ICCs to assess the agreement of measurements. An ICC greater than 0.75 was considered to signify good agreement. (c) We used the Bland-Altman plot to present the limits of agreement.

Reliability (interobserver only) and validity values were calculated for both observers for volume measurements with each imaging plane and sequence. Analysis also included evaluation of the effect of the total sample volume to assess whether the fractional random error decreases with increasing lung volume, as the definition of the exact position of the boundaries becomes less important for the total volume estimate.

Data were analyzed by using software (SAS, release 8.02; SAS Institute, Cary, NC). A statistical result with a difference of P < .05 was considered to be significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Validity
For investigating the validity of the volume measurements, the average calculated volume of the in vitro lung models represented a minor overestimate of the true volume (mean difference, 0.40 mL ± 0.50). We also found measurement accuracy to be slightly better for the coronal plane (mean difference, 0.34 mL ± 0.77) than for the sagittal (mean difference, 0.40 mL ± 0.70) and the transverse (mean difference, 0.46 mL ± 0.86) planes. Furthermore, the validity of MR planimetry proved to be somewhat better by using the true FISP sequence than by using the half-Fourier acquired single-shot turbo SE sequence (mean difference, 0.31 mL ± 0.51 and 0.49 mL ± 0.48, respectively).

Although the differences between the MR image measurements and the true volumes of the lung models were statistically significant with respect to the observer, the MR sequence, and the imaging plane (P < .001), the ICC was 0.998–0.999 in each separate analysis and the limits of agreement hardly exceeded 2 mL (Table 1, Fig 3).


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  		Table 1. MR Image FLV Measurement Validity for 336 Measurements in 28 in Vitro Lung Models

 

Figure 3A
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  		Figure 3a: Validity of MR FLV measurements. (a) Bland-Altman plot indicates mean differences (solid line) and 95% limits of agreement (dashed lines) between mean calculated volume and true volume of lung models measured by two observers and (b) linear regression for comparison of measured and true lung model volumes. {diamondsuit} = half-Fourier acquired single-shot turbo SE sequence, {square} = true FISP sequence.

 

Figure 3B
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  		Figure 3b: Validity of MR FLV measurements. (a) Bland-Altman plot indicates mean differences (solid line) and 95% limits of agreement (dashed lines) between mean calculated volume and true volume of lung models measured by two observers and (b) linear regression for comparison of measured and true lung model volumes. {diamondsuit} = half-Fourier acquired single-shot turbo SE sequence, {square} = true FISP sequence.

 
Reliability
Mean FLV of the 40 fetuses examined was 12.3 mL ± 6.7 (range, 1.6–34.9 mL) and 11.5 mL ± 6.3 (range, 1.7–38.1 mL) for the two observers. For both the lung models and the fetuses, there was no major influence of the imaging plane, the sequence, or the observer on measurement reliability. Measurement reproducibility was slightly better for the data in lung models than it was for data in fetuses (Table 2, Figs 4, 5). With respect to the interobserver reliability in FLV measurements, the data contain a few outliers (Fig 4a, right). In four fetuses, the difference in volume measurements between the two observers exceeded 5 mL (maximum, 7.2 mL), equivalent to 35.3% ± 10.4 (range, 27%–52%) of the approximate total lung volume. In two of four fetuses, these discrepancies occurred for only one of the sequences. Evaluating measurement reliability in these fetuses by using the mean lung volumes obtained with the two MR sequences decreased measurement inconsistency from about 27% to 11% (true FISP) and 33% to 12.5% (half-Fourier acquired single-shot turbo SE).


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  		Table 2. MR Image FLV Measurement Reliability

 

Figure 4A
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  		Figure 4a: Interobserver reliability of MR FLV measurements. (a) Bland-Altman plots indicate mean differences and 95% limits of agreement of volume measurements and (b) regression analysis of measurements for two observers in 28 lung models (left) and 40 fetuses (right). Keys for lines and symbols are the same as for Figure 3.

 

Figure 4B
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  		Figure 4b: Interobserver reliability of MR FLV measurements. (a) Bland-Altman plots indicate mean differences and 95% limits of agreement of volume measurements and (b) regression analysis of measurements for two observers in 28 lung models (left) and 40 fetuses (right). Keys for lines and symbols are the same as for Figure 3.

 

Figure 5A
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  		Figure 5a: Reliability of MR image FLV measurements and influence of MR sequence. (a) Bland-Altman plots indicate mean differences (solid line) and 95% limits of agreement (dashed lines) of volume measurements and (b) regression analysis of measurements for two observers in 28 lung models (left) and 40 fetuses (right). HSE = half-Fourier acquired single-shot turbo SE sequence.

 

Figure 5B
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  		Figure 5b: Reliability of MR image FLV measurements and influence of MR sequence. (a) Bland-Altman plots indicate mean differences (solid line) and 95% limits of agreement (dashed lines) of volume measurements and (b) regression analysis of measurements for two observers in 28 lung models (left) and 40 fetuses (right). HSE = half-Fourier acquired single-shot turbo SE sequence.

 
Total Sample Volume
Data analysis of the lung models demonstrated a significant but very weak correlation between measurement validity and the total sample volume (P < .024, r = 0.12). In addition, regression analysis revealed a significant but only minor correlation between the total lung volume and measurement reliability with respect to the observer, the sequence, and the imaging plane, showing slightly decreasing measurement differences with an increasing total sample volume. The linear regression, for example, for the observer was calculated to be as follows: d = 0.06857 – 0.00652·s, where d is the difference between the measured volumes of the two observers and s is the true volume (P < .072, r = –0.24). Furthermore, this association could only be partially confirmed for the measurements of the fetuses in regard to the MR sequences and the imaging plane (Table 2).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
By applying a fast SE T2-weighted sequence in a group of 210 healthy fetuses, Rypens et al (27) first described good interobserver variability of FLV measurements (r2 = 0.96). More recently, Ward et al (24) confirmed these findings in a cohort of 30 healthy fetuses (r = 0.68–0.76) and further proved that FLV measurements can also be performed with good intraobserver agreement (r = 0.65–0.83) and that measurement accuracy was independent of the section thickness (range, 4–6 mm; P = .23) and imaging plane (P = .82). To our knowledge, these findings have not been confirmed for fetuses with pulmonary hypoplasia. However, Paek et al (22) have assessed the interobserver reliability in a group of 26 fetuses with CDH by using a single-shot rapid acquisition and relaxation enhancement sequence, and they were able to demonstrate a high agreement between observers (ICC, 0.95) for FLV measurements.

In our cohort of 40 fetuses with CDH and 28 in vitro fetal lung models, we found a high reliability of MR image volume measurements. From a clinical point of view, data were independent of the sequence, the imaging plane, and the observer. In addition, measurement consistency was not influenced, to any considerable degree, by the total volume of the sample and equally applies to small and larger volumes. Thus, we confirmed that observations made by Ward et al (24) in a group of healthy fetuses also apply to fetuses with pulmonary hypoplasia due to CDH.

Interobserver reliability was moderately impaired in 10% (four of 40) of fetuses, with a measurement discrepancy of about 27%–52% of the approximate total lung volume. In two of these fetuses, this inconsistency occurred for only one of the two sequences and was presumably due to partial volume effects and sporadic difficulties in confidently distinguishing fetal lung parenchyma from structures of similar signal intensity values (eg, subcutaneous fat or pleural effusion). By assessing the interobserver variability based on the mean volume of the two sequences, the measurement disagreement decreased considerably in two (50%) of the fetuses. This finding suggests that more than one MR sequence should be used to further improve measurement reliability.

Results in the 28 in vitro lung models for a given volume between 1 and 60 mL used in this study not only showed a high reliability but also proved that the volume measurements are highly valid. Again, the sequence, imaging plane, observer, and total volume of the sample did not influence measurements, to any considerable degree. Our data are consistent with preliminary observations made by Wedegaertner et al (26) in a sheep model in a comparison of MR image FLVs with the postmortem FLVs obtained with the water displacement method. By analyzing data from seven animals, they found a high correlation between MR image FLVs and postmortem FLVs, and data were independent of the imaging plane.

In contrast, Jani et al (25) observed that volume measurements of fetal sheep organs were, on average, larger than postmortem volumes, with a relative error for fetal lungs of 38%–73%, depending on the imaging plane and absolute volume of the organ. As discussed by those authors, the findings may reflect a general loss of volume caused by the unperfused state of the organs at the time of postmortem examination. Jani et al also describe a significantly smaller relative error of volume measurements in larger organs than in smaller objects and further observed a higher measurement accuracy of the FLV in the transverse plane (38%) than in the coronal (53%) and sagittal planes (73%). The authors suggest that the higher measurement accuracy may reflect a decreasing fractional random error caused by an increasing number of sections. Our data do not support this explanation, as we found a significant but extremely weak association between the measurement accuracy and the imaging planes and the absolute volume when a 4-mm section thickness was applied.

MR imaging will not replace US as a first-line screening technique, and both direct and indirect US measurements of FLV have been used with the main purpose of improving the antenatal prediction of pulmonary hypoplasia (28–32).

Indirect measurements include the lung-to-head ratio, which reflects the ratio of the right lung area to the head circumference of the fetus. However, with the use of the lung-to-head ratio in the prediction of pulmonary hypoplasia, there were large differences in reporting results, possibly because of the wide range in gestational age at which the lung-to-head ratio was measured (16–38 weeks) (1,33–35), as well as an exponential increase in the lung-to-head ratio with gestational age and inconsistencies in measurement techniques, as recently revealed by Peralta et al (36).

More recently, three-dimensional US was used to directly measure FLV. Researchers in several investigations demonstrated very good reproducibility in assessing healthy fetuses (31,32,37,38) and fetuses with CDH (28,39,40). In addition, there is high agreement between three-dimensional US results and postmortem findings (28,41), as well as phantom measurements (42–44), proving a high validity of the method.

However, particularly in cases of oligohydramnios and maternal obesity or an unfavorable fetal position, US does not always accurately allow visualization of the lung parenchyma. Furthermore, at three-dimensional US, fetal position greatly affects the quality of acquired lung volumetric images (32). On T2-weighted MR images, the fetal lungs are well demarcated, facilitating accurate planimetry (20,27,45), and fetal position is of no consequence for image acquisition. Particularly in such patients, MR image FLV planimetry is invaluable for supporting prenatal counseling.

Limitations of our study mainly affected the in vitro lung phantoms. Although we created lung-shaped models, they failed to resemble the irregular contours of fetal lung, such as the hila. Therefore, the boundaries were easy to identify, and volume assessment was not demanding. As described for three-dimensional US, measurement quality of an object might be influenced by its morphology, and volume assessment would be slightly more precise in regularly shaped phantoms than in irregularly shaped objects (42,46,47). However, multiple in vitro and in vivo studies with three-dimensional US proved that the differences in measurement accuracy and reproducibility were negligible for both regularly and irregularly shaped objects, with ICCs ranging from 0.986 to 0.999 (42–44,46,47). Another drawback of our models was that they missed adjacent structures, such as subcutaneous fat and, thus, could not simulate impaired tissue contrast to bordering parenchyma. As stated previously, an impaired tissue contrast could possibly lead to considerable problems in discriminating fetal lung parenchyma from structures and, thus, may cause outliers in measurement accuracy.

In conclusion, we established that MR image volume measurement is a highly reliable and valid method. From a clinical point of view, measurement accuracy is independent of the MR sequence and the imaging plane, and FLV assessment can be performed with very good interobserver agreement, even in small volumes. Results from this study substantially support the use of this method for ongoing clinical research, for example, in the antenatal identification of pulmonary hypoplasia and the development of prognostic parameters for fetuses with CDH that may further improve prediction of survival, therapeutic management, and parental counseling.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 


   IMPLICATION FOR PATIENT CARE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
References
 


   ACKNOWLEDGMENTS
 
We express our gratitude to Sylvia Büttner, Department of Medical Statistics, University Hospital Mannheim, for her assistance in illustrating the measurement data.


   FOOTNOTES
 

Abbreviations: CDH = congenital diaphragmatic hernia • FISP = fast imaging with steady-state precession • FLV = fetal lung volume • ICC = intraclass correlation coefficient • SE = spin echo

Author contributions: Guarantors of integrity of entire study, K.A.B., K.W.N.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, K.A.B., A.D., C.W.; clinical studies, K.A.B., A.K.K., T.S., A.D.; experimental studies, K.A.B.; statistical analysis, K.A.B., T.S., A.D., C.W., K.W.N.; and manuscript editing, K.A.B., C.W., K.W.N.

Authors stated no financial relationship to disclose.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 

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