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Published online before print April 26, 2006, 10.1148/radiol.2393050586
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(Radiology 2006;239:703-709.)
© RSNA, 2006

Cardiac Imaging

Myocardial Viability: Assessment with Three-dimensional MR Imaging in Pigs and Patients1

Marc Dewey, MD, Michael Laule, MD, Matthias Taupitz, MD, Nicola Kaufels, DVM, Bernd Hamm, MD and Dietmar Kivelitz, MD

1 From the Departments of Radiology (M.D., M.T., N.K., B.H., D.K.) and Cardiology (M.L.), Charité, Medical School, Humboldt-Universität zu Berlin, Schumannstrasse 20/21, 10117 Berlin, Germany. Received April 8, 2005; revision requested June 10; revision received July 6; accepted July 22; final version accepted August 3. Address correspondence to M.D. (e-mail: marc.dewey{at}charite.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To prospectively evaluate the correlation between a three-dimensional (3D) delayed enhancement magnetic resonance (MR) imaging sequence and a two-dimensional (2D) delayed enhancement MR imaging sequence for noninvasive assessment of myocardial viability in pigs and patients.

Materials and Methods: The pig and patient studies were approved by the responsible authorities, and patients gave written informed consent. MR imaging was performed by using a rapid 3D inversion-recovery balanced steady-state free precession sequence and a 2D segmented inversion-recovery fast low-angle shot sequence as the reference standard. Fourteen pigs with reperfused (n = 7) or nonreperfused (n = 7) myocardial infarction and 17 patients (13 men, four women; mean age, 64.9 years ± 8.6 [standard deviation]) suspected of having myocardial infarction were included. Linear regression analysis and Bland-Altman analysis were used to compare the infarction volumes.

Results: In 10 of the 14 pigs the induction of myocardial infarction was successful. In these pigs, altogether 81 segments with myocardial infarction were demonstrated by both MR sequences, and agreement between the two sequences for classification of transmural extent of myocardial infarction was 99.7%. The infarction volume determined by using 3D MR imaging (4.64 cm3 ± 2.48) in the pigs highly correlated with that of 2D MR imaging (4.65 cm3 ± 2.39, r = 0.989, P < .001) and that of staining by using triphenyltetrazolium chloride (4.67 cm3 ± 2.44, r = 0.996, P < .001). Thirteen of the 17 patients examined showed myocardial infarction in 34 myocardial segments with both sequences, and agreement between the two sequences for classification of transmural extent of myocardial infarction was 98.6%. In the patients, the infarction volume determined with both sequences highly correlated (9.71 cm3 ± 7.47 for the 3D sequence vs 10.01 cm3 ± 8.04 for the 2D sequence, r = 0.982, P < .001). The breath-hold time necessary for the 3D MR imaging (21.0 ± 2.3 seconds) was significantly shorter than that for 2D MR imaging (188.3 ± 20.2 seconds, P < .001).

Conclusion: Myocardial infarction volumes obtained with the 3D MR imaging sequence are highly correlated and in good agreement with volumes obtained with the 2D MR imaging standard approach and reduced the acquisition time by a factor of nine.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Assessment of the extent of dysfunctional yet viable myocardium plays an important role in therapeutic decision making with regard to thrombolytic therapy, catheter intervention, and bypass surgery. At present, the transmural extent of myocardial infarction can be assessed reliably only with delayed enhancement magnetic resonance (MR) imaging because of its high spatial resolution (1–4). The transmural extent of myocardial infarction is decisive for prognosis, recovery of regional contractile function, and remodeling of the left ventricle (5,6). The reference standard for delayed enhancement MR imaging is two-dimensional (2D) inversion-recovery fast low-angle shot imaging (7). A major drawback of this technique is the long acquisition time, which is estimated to be about 10–14 heartbeats for one single section (7). As a consequence, 10–16 breath holds each lasting at least 10 heartbeats are necessary to cover the entire left ventricle on short-axis orientation with this 2D approach. The purpose of our study was to evaluate prospectively the correlation between a three-dimensional (3D) MR imaging sequence and a 2D MR imaging sequence for noninvasive assessment of myocardial viability in pigs and patients.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Animal Study
Fourteen minipigs (Mini-LEWE; Experimental Center of the Technical University, Dresden, Germany) weighing 25 kg ± 3.6 (standard deviation [SD]) were studied. All experiments were approved by the responsible local animal care authority. Anesthesia prior to experimental instrument manipulation was induced by using ketamine hydrochloride (Ketamin [500 mg]; Curamed Pharma, Karlsruhe, Germany) intramuscularly, droperidol (Dehydrobenzperidol; Janssen-Cilag, Neuss, Germany) intramuscularly, midazolam hydrochloride (Dormicum; Hoffmann-La Roche, Grenzach-Whylen, Germany) intramuscularly, and propofol (Disoprivan 7%; Astra Zeneca, Wedel, Germany) intravenously. After anesthesia had taken effect, the pigs were intubated by using a 6–7-mm endotracheal tube. Anesthesia was maintained with a mixture of 2%–5% isoflurane and oxygen.

To induce reperfused myocardial infarction, seven animals were subjected to a 90-minute occlusion of a branch of the left circumflex coronary artery by using a coronary dilation catheter (Cross sail; Guidant Europe NV, Diegem, Belgium) 3 mm in diameter and 10 mm in length. To induce nonreperfused myocardial infarction, another group of seven animals was subjected to occlusion with tungsten spirals (Spirale n detachable en tungstene; Balt Extrusion, Montmorency, France). The tungsten spirals were flushed with saline through a 6-F, 80-cm-long multipurpose catheter (Vistabrite tip, XBR 2; Cordis, Miami, Fla) into the left circumflex coronary artery by a cardiologist (M.L.) with 20 years of experience in invasive cardiac procedures (8).

After MR imaging, the animals were euthanized and the hearts were excised. The hearts then were stiffened with repetitive immersion in 95% ethanol, precooled to –80°C, and sliced from base to apex into 5-mm-thick slices with a commercial slicer (9). These slices were incubated in 2% triphenyltetrazolium chloride (TTC) for 20 minutes at 37°C to define the infarcted areas (regions that failed to stain brick-red [10]). These slices were digitally photographed, and the volumes of infarction (in cubic centimeters) were determined by a reader (N.K.) with 2 years of experience with this technique and who was blinded to the results of MR imaging (8).

Clinical Study
Seventeen consecutive patients who were suspected of having chronic myocardial infarction on the basis of clinical, laboratory, electrocardiographic, echocardiographic, or scintigraphic findings were included in the study. The study was approved by the institutional review board, and all patients gave written informed consent. The institutional review board requested that patients with acute myocardial infarction not be eligible for inclusion. The patients' mean age was 64.9 years ± 8.6. Four of the patients were women. In the 17 patients, the presence of chronic myocardial infarction was suggested with electrocardiography (13 patients: 10 patients with pathologic Q-wave elevations [≥30 msec and >0.1 mV in I, II, III, aVL, aVF, or V4 through V6], and three patients with ST elevations), scintigraphy (three patients), and echocardiography (three patients). (More than one method per patient was possible.) All patients underwent MR imaging within 1 week after chronic myocardial infarction was suspected.

MR Imaging Protocol and Reference Standard
Each of the pigs was examined by using both 2D and 3D MR imaging sequences 2–3 days after induction of myocardial infarction. Anesthesia prior to MR imaging was induced the same way it was induced for minimally invasive experimental instrument manipulation. All examinations were performed with a 1.5-T imager (Magnetom Sonata; Siemens, Erlangen, Germany) with a maximum gradient amplitude of 40 mT/m, a minimum rise time of 200 µsec, and a dedicated cardiac 12-element phased-array coil. For evaluation of myocardial viability, 16 contiguous short-axis views were acquired with both 2D and 3D MR imaging in random order. Standard extracellular MR contrast agents were injected intravenously at a dose of 0.1 mmol gadolinium per kilogram (gadoterate meglumine; Guerbet, Roissy, France) for the animal study (11) and at a dose of 0.2 mmol gadolinium per kilogram (gadopentetate dimeglumine; Schering, Berlin, Germany) for the clinical study (7,12). All images were acquired during end-expiratory breath holds at 5–15 minutes after injection.

A 2D segmented inversion-recovery fast low-angle shot MR sequence (7) was used as the reference standard for the rapid 3D inversion-recovery balanced steady-state free precession sequence in the pig and the patient studies. The major difference between the two sequences was the acquisition time, which was shorter by a factor of about nine with 3D MR imaging (25 heartbeats for 2D MR imaging vs 16 x 14 heartbeats for 3D MR imaging). Further sequence parameters of 3D MR imaging for the clinical study were as follows: echo time, 1.45 msec; repetition time, 3.2 msec; flip angle, 50°; field of view, 400 x 312; matrix, 320 x 178; spatial resolution, 1.3 x 1.8 x 8 mm (each imaging voxel represented a volume of 19 µL); section resolution, 75%; 16 sections; section gap, 0 mm; acquisition time per heartbeat, 159 msec (99 segments); asymmetric sampling to reduce off-resonance artifacts and acquisition time (13); inversion time, 280–320 msec; bandwidth, 1090 Hz/pixel; and triggering every cardiac cycle. The sequence parameters of 2D MR imaging were as follows: echo time, 4.3 msec; repetition time, 5.7 msec; flip angle, 25°; field of view, 360 x 270; matrix, 256 x 148; spatial resolution, 1.4 x 1.8 x 8 mm (each imaging voxel represented a volume of 20 µL); section resolution, 100%; 16 sections; section gap, 0 mm; acquisition time per heartbeat, 142 msec (25 segments); inversion time, 280–320 msec; bandwidth, 140 Hz/pixel; and triggering every other cardiac cycle.

For the animal study, MR acquisition protocols similar to those described above were used but with 5-mm section thicknesses and pixel sizes of 1 x 1 mm (each imaging voxel represented a volume of 5 µL) to compensate for the smaller heart of pigs. An inversion time scout sequence was used between the viability sequences after injection of the contrast agent to identify the inversion time with the best suppression of signal from the myocardium and to adjust for potential contrast agent washout (7,14). This inversion time was used for both the 2D and the 3D MR imaging sequences.

Image Analysis
For both MR imaging sequences, contrast-to-noise ratios between infarcted and remote myocardium in the same anatomic region were calculated with the following equation: (mean signal intensity of infarcted myocardium – mean signal intensity of remote myocardium)/(1.5 · SD of noise) as described recently (7) by one reader (M.D.) with 4 years of experience in cardiac MR imaging and who was blinded to the type of MR imaging sequence used. The volume (in cubic centimeters) of hyperenhanced myocardium (infarcted myocardium) was measured, as previously described (6) by the same reader (M.D.) blinded to the type of MR imaging sequence used. As recommended, a previously described 30-segment model was used for the animal study (2), and a 17-segment model was used for the clinical study (15) to visually evaluate the regional transmural extent of myocardial infarction on a five-point (6) grading system (0%, 1%–25%, 26–50%, 51–75%, 76–100%) by using image analysis software (ImageJ; National Institutes of Health, http://rsb.info.nih.gov/ij/).

Statistical Analysis
All data are expressed as means plus or minus SD except those obtained by using Bland-Altman analysis. Linear regression analysis and Bland-Altman analysis (results of which are presented as means ± 1.96 · SD = means ± limits of agreement) were used to analyze the correlation coefficient and agreement (16) between the volumes of infarction determined with MR imaging and those determined with TTC staining. Agreement on the transmural extent of myocardial infarction was assessed as a true-positive finding if it was correctly classified with the 3D MR imaging sequence in comparison with the 2D MR imaging reference standard by using the five-point grading system (6). A paired t test was used to identify differences in the contrast-to-noise ratios and breath-hold time necessary for both MR sequences. A P value .05 or less was considered to indicate a statistically significant difference. Statistical analyses were conducted by using statistical software (SPSS version 11.0; SPSS, Chicago, Ill).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Animal Study
Three pigs died after instrument manipulation (one in the reperfused infarction group and two in the nonreperfused infarction group). One pig in the reperfused infarction group did not develop myocardial infarction as defined at TTC staining and with both MR imaging sequences. In the remaining 10 pigs (five per group), the entire procedure was successfully completed (Fig 1).


Figure 1
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  		Figure 1: Comparison of TTC staining with short-axis MR images obtained with 2D segmented inversion-recovery fast low-angle shot sequence and 3D rapid inversion-recovery balanced steady-state free precession sequence. Images show good agreement in depiction of extent of inferior myocardial infarction (arrows indicate borders of infarction in basal section). This nonreperfused inferolateral myocardial infarction in a pig was induced with tungsten spirals flushed into left circumflex coronary artery.

 
In these 10 pigs, altogether 81 segments with myocardial infarction were observed with both delayed enhancement MR imaging sequences. One segment was misclassified with 3D MR imaging as 51%–75% instead of 76%–100% of the regional myocardium affected by infarction. No hyperenhanced myocardial segment on the 2D images was missed on the 3D images. The agreement between the 2D and the 3D approaches for classification of transmural extent of myocardial infarction of the 300 segments according to the five-point grading system was 99.7%. The infarction volume determined by using 3D MR imaging (4.64 cm3 ± 2.48) highly correlated with those at both TTC staining (4.67 cm3 ± 2.44, r = 0.996, P < .001) and MR imaging with the 2D sequence (4.65 cm3 ± 2.39, r = 0.989, P < .001). Bland-Altman analysis showed that the limits of agreement (mean ± 1.96 · SD) of 3D MR imaging compared with that of TTC staining were 0.03 cm3 ± 0.46 and compared with that of 2D MR imaging were 0.01 cm3 ± 0.74 (Fig 2). The contrast-to-noise ratio between infarcted and remote myocardial tissue was not significantly different between the 3D and the 2D MR imaging approaches (22.4 ± 9.4 for the 3D approach vs 22.0 ± 11.5 for the 2D approach).


Figure 2
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  		Figure 2a: Agreement of myocardial infarction volumes in animal study according to Bland-Altman analysis between (a) 3D delayed enhancement MR imaging (DE-MRI) and TTC staining and (b) 3D delayed enhancement MR imaging and 2D delayed enhancement MR imaging. Mean of two methods compared is plotted against difference between the two. Dashed line is mean of differences, and dash-dot lines mark limits of agreement (95% confidence intervals = 1.96 · SD). There was no systematic under- or overestimation of infarction size with 3D MR imaging, and limits of agreement were sufficiently small compared with average infarction size.

 

Figure 2
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  		Figure 2b: Agreement of myocardial infarction volumes in animal study according to Bland-Altman analysis between (a) 3D delayed enhancement MR imaging (DE-MRI) and TTC staining and (b) 3D delayed enhancement MR imaging and 2D delayed enhancement MR imaging. Mean of two methods compared is plotted against difference between the two. Dashed line is mean of differences, and dash-dot lines mark limits of agreement (95% confidence intervals = 1.96 · SD). There was no systematic under- or overestimation of infarction size with 3D MR imaging, and limits of agreement were sufficiently small compared with average infarction size.

 
Clinical Study
All patients were successfully examined without adverse reactions to contrast agent administration. The average heart rate during imaging was 72.2 ± 8.0 beats per minute. Thirteen of the 17 patients showed myocardial infarction at both 2D and 3D MR imaging. The four patients without hyperenhancement on 2D MR images also showed no hyperenhancement on the 3D MR images. Similar to the animal study results, results of 2D and 3D MR imaging showed good agreement (Fig 3). The infarction volume determined by using 3D MR imaging (9.71 cm3 ± 7.47) highly correlated with that at 2D MR imaging (10.01 cm3 ± 8.04, r = 0.982, P < .001). Bland-Altman analysis showed that the limit of agreement (mean ± 1.96 · SD) of 3D MR imaging compared with that of the 2D sequence was 0.3 cm3 ± 3.1 (Fig 4). Thirty-four segments with myocardial infarction were observed with both MR imaging approaches. Of these 34 segments, 31 were correctly classified with the 3D images when compared with the 2D images. No hyperenhanced myocardial segment on the 2D images was missed on the 3D images. Three of the 34 segments were misclassified with 3D MR imaging (two with 26%–50% at 2D MR imaging that were overestimated as 51%–75% at 3D imaging and one with 51%–75% at 2D MR imaging that was overestimated as 75%–100% at 3D imaging), and one nonenhanced segment at 2D MR imaging was misclassified as involving 1%–25% with 3D MR imaging. The agreement between the 2D and the 3D sequence for classification of transmural extent of myocardial infarction in the 289 segments according to the five-point grading system was 98.6%. The contrast-to-noise ratios between infarcted and remote myocardial tissue were not significantly different between the 3D approach and the 2D approach (36.2 ± 16.4 for the 3D approach vs 34.8 ± 11.9 for the 2D approach). The pure (ie, net) breath-hold time necessary for the 3D MR imaging sequence (21.0 seconds ± 2.3) was significantly shorter than that necessary for the 16 breath holds at 2D MR imaging (188.3 seconds ± 20.2, P < .001).


Figure 3
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  		Figure 3: MR images of 56-year-old patient with inferior (arrow) and lateral (arrowhead) myocardial infarction assessed with good agreement between standard 2D segmented inversion-recovery fast low-angle shot MR sequence and rapid 3D inversion-recovery balanced steady-state free precession MR sequence in short-axis orientation.

 

Figure 4
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  		Figure 4: Agreement for myocardial infarction volumes in clinical study according to Bland-Altman analysis for 13 patients showing myocardial late enhancement between 2D delayed enhancement MR imaging sequence and 3D delayed enhancement MR imaging (DE-MRI). Mean of two methods compared is plotted against difference between the two. Dashed line is mean of differences, and dash-dot lines mark limits of agreement (95% confidence intervals = 1.96 · SD). There was no systematic under- or overestimation of infarction size with 3D MR imaging. Limits of agreement compared with average myocardial infarction size were larger in clinical study than in animal study but still in clinically acceptable range.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
MR imaging for viability assessment is an established method to distinguish between reversible and irreversible myocardial injury (6,9). Some studies showed overestimation of the true infarction size with this method (17,18). Kim et al (1), however, demonstrated that overestimation of myocardial infarction was attributable to partial volume effects, and Barkhausen et al (11) concluded from their results obtained in an animal model that extracellular gadolinium-based contrast agents, like necrosis-specific contrast agents, do not cause overestimation of infarction size. Furthermore, Rehwald et al (4) showed with electron probe x-ray microanalysis that elevated myocardial gadolinium-based concentrations are exclusively associated with irreversible ischemic injury, and our group (19) showed that delayed enhancement MR imaging performed with blood-pool contrast agents based on gadolinium also yields infarction size estimates that are in good agreement with those obtained from TTC staining. Furthermore, MR imaging for viability assessment has proved to be the most accurate tool to identify even small myocardial infarctions (2) and to predict functional recovery after coronary revascularization in patients with coronary artery disease (6) and myocardial infarction (20). With the current reference standard—2D MR imaging—10–16 breath holds each lasting 14 heartbeats are necessary to assess the entire left ventricle. Our results suggest that 3D MR imaging with a rapid inversion-recovery balanced steady-state free precession sequence can identify myocardial viability similarly to the reference standard but with an acquisition time that is about nine times shorter.

The use of a 2D inversion-recovery balanced steady-state free precession sequence has already been reported to yield good results in viability assessment (21). This 2D approach, however, shortens the acquisition time by only a factor of two and still results in section misregistration from multiple breath holds necessary to cover the entire myocardium. The combined assessment of viability and myocardial function by using a 2D steady-state free precession sequence within a single examination showed good agreement with the 2D reference standard for MR imaging (22). Nevertheless, this combined technique produces lower contrast compared with that of the reference standard. Foo et al have shown that a 3D inversion-recovery fast low-angle shot sequence with variable sampling in time enables faster assessment of myocardial viability than does the standard 2D inversion-recovery fast low-angle shot sequence, and the 3D technique has improved contrast-to-noise ratios (12). The spatial resolution of their 3D sequence, however, was slightly smaller than that of the 2D sequence, and agreement for assessment of the clinically most relevant size and transmural extent of myocardial infarction (5,6) was not examined in this study (12).

Only moderate agreement for the assessment of the transmural extent of myocardial infarction was shown in a another study that used a 3D inversion-recovery fast low-angle shot sequence; the moderate agreement might have been a result of the rather long acquisition time of 293 msec per heartbeat (23). In contrast, the acquisition time per heartbeat for the 3D MR imaging sequence in our study was 159 msec. The inversion time of the MR imaging sequences for viability assessment in our study was perpetually optimized to null signal from myocardium by using an inversion time scout sequence, as this is important for accurate estimation of infarction size (7,14). Another technique, called phase-sensitive inversion recovery, might simplify this procedure (24) and also has the advantage of decreasing the sensitivity to changes in tissue T1 with increasing delay after contrast agent injection. Motion-corrected acquisition during free breathing might be another attractive imaging approach for viability assessment in cases in which patients have difficulty holding their breath (25).

The 3D MR imaging sequence showed good correlation and agreement with the standard 2D MR imaging sequence in both the animal and the clinical study and with TTC staining in the animal study. Application of the 3D MR imaging sequence based on balanced steady-state free precession and asymmetric sampling of echoes reduced the acquisition time without decreasing the contrast between infarcted and remote myocardium. From a clinical perspective, the transmural extent of myocardial infarction is of pivotal importance for the prognosis and recovery of regional contractile function (5,6). The transmural extent was correctly classified with the 3D sequence in 80 of 81 infarcted segments in the animal study and 31 of 34 infarcted segments in the clinical study. Nevertheless, the accuracy of the 3D approach remains to be examined in large, multicenter studies.

Section misregistration resulting from multiple breath holds necessary with the 2D sequence in the clinical (but not the animal) study might be responsible for the wider limits of agreement and the lower agreement for transmural extent in the clinical study. A potential drawback of 3D sequences is that wraparound (aliasing) occurs in the z-axis. Wraparound can reduce image quality in sections at the border of the 3D stack and might necessitate the use of two 3D stacks or time-consuming phase oversampling. Two 3D stacks could also be necessary if a patient is short of breath and not capable of holding his or her breath for the desired period.

A further limitation of our study is that we analyzed the images visually, as described in previous studies (6,26), because quantitative analysis tools were not available in our department. Schuijf and colleagues demonstrated the advantage of such quantitative analysis tools. Nevertheless, this group also concluded that visual assessment may be sufficient because there was excellent agreement between the visual and the quantitative approaches (27). No data regarding correlation to regional myocardial function were presented in our study because the purpose was only to evaluate the clinical applicability of a 3D MR imaging sequence.

In conclusion, myocardial infarction volumes obtained with the 3D MR imaging sequence are highly correlated and in good agreement with volumes obtained with the 2D MR imaging standard approach. The infarction volumes determined with the 3D and the standard 2D sequences were virtually identical in both the animal and the clinical study. The contrast between infarcted and remote myocardium was good with both imaging sequences, while the 3D sequence allowed imaging of the entire heart within one breath hold. Thus, delayed enhancement MR imaging can be shortened at least by a factor of nine and thereby simplified with a 3D approach. This advantage further improves the clinical applicability of MR imaging in assessing the presence and extent of viable myocardium.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   FOOTNOTES
 

Abbreviations: SD = standard deviation • 3D = three dimensional • TTC = triphenyltetrazolium chloride • 2D = two dimensional

Authors stated no financial relationship to disclose.

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


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

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