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DOI: 10.1148/radiol.2273011964
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(Radiology 2003;227:883-889.)
© RSNA, 2003

Technical Developments

Three-dimensional CT Angiography of the Hepatic Artery: Use of Multi–Detector Row Helical CT and a Contrast Agent1

Masato Tanikake, MD, Tadafumi Shimizu, MD, Isamu Narabayashi, MD, Mitsuru Matsuki, MD, Kiyohiro Masuda, MD, Kazuhiro Yamamoto, MD, Yasuo Uesugi, MD, and Shushi Yoshikawa, RT

1 From the Department of Radiology, Osaka Medical College, 2-7 Daigaku-machi, Takatsuki, Osaka 569-8686, Japan. Received November 30, 2001; revision requested January 25, 2002; final revision received August 26; accepted September 30. Address correspondence to M.T.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
The administration of a contrast agent to obtain optimal images at three-dimensional computed tomographic (CT) angiography of the hepatic artery by using multi–detector row helical CT was investigated. Three-dimensional CT angiographic images were evaluated visually, and quantitative evaluation was performed by measuring the postcontrast CT number of the aorta. The injection rate of 5 mL/sec was significantly superior to that of 4 mL/sec in both evaluations. At administration of a contrast agent with 300 or 350 milligrams of iodine per milliliter, there were no significant differences in either evaluations. The preferable injection rate to obtain sufficient three-dimensional CT angiographic data was 5 mL/sec.

© RSNA, 2003

Index terms: Computed tomography (CT), angiography, 952.12915, 952.12916 • Computed tomography (CT), three-dimensional, 952.12917 • Contrast media, comparative studies • Hepatic arteries, CT, 952.12912, 952.12913, 952.12915, 952.12916, 952.12917


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
Results
 Discussion
 REFERENCES
 
An advantage of three-dimensional (3D) computed tomographic (CT) angiography is that one can noninvasively obtain information about blood vessels, which in the past could only be obtained with invasive contrast material–enhanced conventional angiography. Since the development of helical CT in the 1990s, 3D CT angiography of the hepatic artery has been used to evaluate hepatic blood vessels prior to hepatectomy or liver transplantation (1–3). Four-channel multi–detector row helical CT, which was introduced in 1999, allowed rapid acquisition of scans over a wide range (eg, whole abdomen) by using thin-section detector row beam collimation (0.5–3 mm) and produced data suitable for preparing 3D images (3,4). With the development of computer-assisted bolus-tracking technology, appropriate images could be obtained in the arterial phase (5), and advances in 3D image-reconstruction methods (6,7) enabled visualization of the peripheral branches of the hepatic artery by using 3D CT angiography (8,9).

The usefulness of this technique has been established in the assessment of the topology of the peripheral branches or the orientation of the hepatic arteries prior to liver transplantation and in the assessment of postoperative complications (8,10).

Dynamic multiple-phase enhanced CT is a useful tool in the diagnosis of hepatocellular carcinoma (11–13). Also, when multi–detector row helical CT is used, detailed 3D CT angiographic images of the hepatic artery can be obtained simultaneously from the arterial phase imaging data. These 3D CT angiographic images provide extremely useful information for transcatheter therapy, such as the location of the hepatic artery branches and the feeding arteries.

The quality of 3D CT angiographic images is influenced by many factors, including the imaging parameters of the CT scanner (eg, detector row beam collimation and helical pitch), the concentration of contrast agent, the rate at which the agent is injected, and the method used to reconstruct the 3D images. Nevertheless, the literature concerning optimization of these factors for evaluation of the peripheral hepatic arteries with 3D CT angiography is relatively sparse (7,9,14). In particular, the appropriate injection method of a contrast agent has not been determined. For example, the preferable injection rate and whether uniphasic injection or biphasic injection is better for producing high-quality 3D images are not known. Therefore, our purpose was to conduct a prospective randomized study to investigate the infusion rate and the contrast agent concentration to obtain 3D CT angiographic images that adequately depict the peripheral branches of the hepatic artery.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
Patient Population
This study followed the principles of the Declaration of Helsinki, and we also obtained institutional review board approval for our study. Informed consent for the contrast agent administration protocols was obtained from all patients before the CT examination. There were 140 patients who were being followed up for chronic liver disease and who underwent abdominal dynamic multiple-phase CT between June and December of 2000. This study was performed within the routine clinical standards of our institution, and these patients were recruited consecutively.

The patients were 85 men and 55 women (mean age, 65.7 years ± 8.1 [SD]; age range, 33–81 years). Their mean body weight immediately before the CT examination was 56.9 kg ± 9.2 (range, 40–81 kg).

The chronic liver disease was caused by viral hepatitis in 119 patients (112 had hepatitis C, six had hepatitis B, and one had both), alcoholic hepatitis in 17 patients, autoimmune hepatitis in two patients, and primary biliary cirrhosis of the liver in two patients. CT was performed to screen for hepatocellular carcinoma or to obtain more detailed information following elevation of blood tumor marker concentrations ({alpha}-fetoprotein and protein induced by vitamin K absence on antagonist II) or the suspected presence of hepatocellular carcinoma on the basis of abdominal ultrasonographic (US) findings. Patients with chronic heart failure or renal failure were not included in this study. The patients were randomly assigned to four groups (Table 1), in which the contrast agent was administered at one of two iodine concentrations (300 or 350 mg/mL) and one of two injection rates (4 or 5 mL/sec).


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  		TABLE 1. Contrast Material Injection Protocols

 
CT Protocol
The CT scanner used was an Aquilion Multi (Toshiba Medical, Tokyo, Japan). At our institution, hepatocellular carcinoma is investigated according to the routine method of using multi–detector row helical CT with the following protocol: An unenhanced CT examination is performed to confirm the location of the upper and lower margins of the liver, and the area between the upper and lower margins is set as the scanning range for enhanced CT. Scanning parameters of unenhanced CT were a voltage of 120 kV, a tube current of 300 mA, a 0.5 second per rotation, a detector row beam collimation of 3 mm, a helical pitch of 3, and a field of view of 32–36 cm.

Two consecutive scans in the arterial phase were obtained during a single breath hold, and scanning at the equilibrium phase was performed 120 seconds after the arterial phase. The 3D CT angiographic image was produced from the imaging data of the first arterial phase. Scans were obtained at a voltage of 120 kV, a tube current of 300 mA, a 0.5 second per rotation, a detector row beam collimation of 2 mm, a helical pitch of 3, and a field of view of 32–36 cm.

The nonionic iodinated contrast agent (Iomeprol; Eisai, Tokyo, Japan) was intravenously administered with a power injector (Auto Enhance A-250; Nemoto Kyorindo, Tokyo, Japan) through a plastic 20-gauge intravenous catheter (Terumo, Tokyo, Japan) that was inserted into the cubital vein. Subsequently, a bolus injection of 20 mL of saline was manually performed to confirm no extravasation.

Computer-assisted bolus-tracking technology (Real Prep; Toshiba Medical) was used for arterial phase scanning. A round region of interest was marked on the abdominal aorta at the level of the celiac artery (S.Y.). The triggering threshold was the relative value calculated by adding 50 HU to the precontrast CT number of the abdominal aorta, as measured at unenhanced CT. Monitoring CT was started with resting respiration 10 seconds after the beginning of contrast agent injection. Scanning was started 6 seconds after the threshold was reached. Although Shimizu et al (5) started scanning 11 seconds after the threshold was reached, we started scanning sooner because the injection rate in our study was higher than that specified in the literature (4–5 vs 2–3 mL/sec).

Three-dimensional Reconstruction
The raw data were reconstructed at 1-mm intervals and transmitted to a workstation (M900 Maximum version 2.0; Zio Software, Tokyo, Japan). Volume rendering was used for 3D reconstruction. The workstation was used to produce 3D images on which the arteries were emphasized and the bone was suppressed by using a technique that results in the suppression of a selected arbitrary range.

In short, 3D images were constructed from the scans by using all voxels higher than the selected minimum threshold of 200 HU, at which the artery and the bone were sufficiently segmented. Then, the voxels from the costa and the vertebra were manually removed from the 3D images.

In addition, a postcontrast CT number was assigned to each datum in such a way that peripheral branches of the hepatic artery were enhanced while the surrounding liver tissues were suppressed (6). The following procedure was used: In all cases, the attenuation was set at 100% for voxels with a CT number greater than 400 HU and at 0% for voxels with a CT number lower than 100 HU. We used a linearly decreasing curve from 100% to 0% for CT numbers between 400 and 100 HU. Then, in each case, we adjusted the upper and lower cutoff CT numbers that corresponded to 100% and 0% attenuation, respectively, in such a way that the peripheral branches of the hepatic artery were the most visible at 3D CT angiography. The 3D CT angiographic images on which the peripheral branches of the hepatic artery were the most visible were examined from many directions with rotation on the computer monitor. All 3D images were reconstructed by one radiologist (M.T.).

Methods of Evaluation
Visual evaluation.—The 3D images were visually evaluated according to the degree of visualization of the peripheral branches of the hepatic artery. The evaluation was based on the rating system developed by Uchida et al (15), who evaluated 3D CT angiographic images of the portal vein. The degree of visualization was graded as follows: excellent, the peripheral branches of the hepatic artery were visualized to the sub-subsegmental level, providing very useful information prior to interventional radiology; good, all of the subsegmental hepatic artery branches were clearly visualized, providing sufficient useful information; fair, insufficient information was obtained because some of the subsegmental hepatic artery branches were indistinct; and poor, no information could be obtained because none of the subsegmental hepatic artery branches were visualized. The evaluation was performed by two radiologists (M.M., K.M.) in consensus who had not been given any information about the patients. Representative cases are presented in Figures 1–3.



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  		Figure 1a. (a) Frontal and (b) caudal 3D CT angiographic images of the peripheral branches of the hepatic artery in a 70-year-old man with cirrhosis of the liver. This case belongs to group D. The images were rated as excellent because the peripheral branches of the hepatic artery are clearly depicted from the subsegmental (arrows) to the sub-subsegmental level (arrowheads).

 


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  		Figure 1b. (a) Frontal and (b) caudal 3D CT angiographic images of the peripheral branches of the hepatic artery in a 70-year-old man with cirrhosis of the liver. This case belongs to group D. The images were rated as excellent because the peripheral branches of the hepatic artery are clearly depicted from the subsegmental (arrows) to the sub-subsegmental level (arrowheads).

 


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  		Figure 2a. (a) Frontal and (b) right anterior oblique 3D CT angiographic images of the peripheral branches of the hepatic artery in a 72-year-old woman who had hepatocellular carcinoma. Dynamic CT was performed because the patient was suspected of having hepatocellular carcinoma on the basis of the results of abdominal US. This case belongs to group C. Tumors are seen in S8 (T1) and S6 (T2) of the right lobe. The feeding arteries of each tumor are clearly depicted. In b, there appear to be two feeding arteries (arrows) for the S8 tumor. The visual evaluation was good.

 


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  		Figure 2b. (a) Frontal and (b) right anterior oblique 3D CT angiographic images of the peripheral branches of the hepatic artery in a 72-year-old woman who had hepatocellular carcinoma. Dynamic CT was performed because the patient was suspected of having hepatocellular carcinoma on the basis of the results of abdominal US. This case belongs to group C. Tumors are seen in S8 (T1) and S6 (T2) of the right lobe. The feeding arteries of each tumor are clearly depicted. In b, there appear to be two feeding arteries (arrows) for the S8 tumor. The visual evaluation was good.

 


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  		Figure 3. Three-dimensional CT angiographic image of the peripheral branches of the hepatic artery in a 64-year-old woman who had hepatocellular carcinoma. Dynamic CT was performed for screening and depicted hepatocellular carcinoma. This case belongs to group A. The images of this patient were rated as fair because the subsegmental branches of the hepatic artery were indistinct (arrowheads).

 
Quantitative evaluation.—Because it was difficult to measure the postcontrast CT number (in Hounsfield units) of the peripheral branches of the hepatic artery, the degree of enhancement of the abdominal aorta was used as an indicator. Measurement of the postcontrast CT number was performed in a round region of interest (approximately 2 cm2) with selection of the abdominal aorta in every 12th resectioned two-dimensional raw image of the 3D image; thus, measurements were performed in 11–14 sections in one patient. All measurements were performed once on each image by one radiologist (M.T.). The precontrast CT number of the aorta at the corresponding level on the unenhanced CT image was subtracted from the postcontrast CT number at the arterial phase, and the mean of the numbers was then determined. This mean number was defined as the postcontrast CT number. This evaluation was performed by one radiologist (M.T.).

Statistical Analyses
The demographic data were statistically compared among the four groups with the Kruskal-Wallis test, and body weight and age were compared among the four groups with one-way analysis of variance (ANOVA). Differences in the scanning start time of the first phase and scanning duration were tested for significance with ANOVA.

Results of the visual evaluation of the four groups were compared by using the Kruskal-Wallis test, and differences between two groups were then assessed by using the Mann-Whitney U test. The quantitative evaluation results of the four groups were compared by using one-way ANOVA, and the Fisher protected least significant difference test was used to assess differences between two groups.

The correlation between the visual evaluation result and the postcontrast CT number was assessed by using the Spearman rank correlation coefficient.

Furthermore, the postcontrast CT number in the patients with each of the four visual evaluation grades was calculated. The difference among the four groups was tested by using one-way ANOVA. Also, pair-wise comparisons were made by using the Fisher protected least significant difference test.

With all tests, differences were considered to be statistically significant at P < .05. These statistical analyses were performed by one radiologist (M.T.).


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 
This study included 140 patients with chronic liver disease who underwent dynamic CT in which the contrast agent was administered with one of two iodine concentrations (300 or 350 mg/mL) and two injection rates (4 or 5 mL/sec). Sex, body weight, and age of the patients in the four groups did not differ significantly (Table 2). Scanning was performed according to our protocol.


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  		TABLE 2. Patient Data

 
There was no extravasation when the contrast agent was injected in any patient in the current study. The mean scanning start time of the first phase was 20.3 seconds, and the mean scanning duration was 12.5 seconds. There were no significant differences in the scanning start times nor scanning durations among the four groups (Table 2).

Three-dimensional CT angiographic images were prepared for all patients, but seven patients (two in group A, three in group B, and two in group D) were excluded from the analyses because it was difficult to perform visual evaluation of the hepatic artery due to strong visualization of the portal venous branches (Fig 4). These seven patients were all women. The mean age and body weight of these seven patients were 61.3 years and 55.6 kg, respectively. In addition, no large hepatic tumor that might have resulted in arterial-portal shunting was depicted on the CT images of these seven patients.



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  		Figure 4. Three-dimensional CT angiographic image of the peripheral branches of the hepatic artery in a 68-year-old woman with cirrhosis of the liver. This patient was excluded from analysis because the portal vein branches were visualized in the periphery (arrowheads), which prevented evaluation of the hepatic artery. This case belongs to group B.

 
Results of the Visual Evaluation
The results of the visual evaluation of the peripheral branches of the hepatic artery on the 3D images are summarized in Table 3, and results of the analyses are shown in Table 4. Multiple-group comparisons revealed significant differences (P < .01). Two-group comparisons revealed statistically significant differences in the visual evaluation results between the groups given the same concentration of iodine at a different injection rate (group A vs group C, P = .01; group B vs group D, P < .01). However, there were no statistically significant differences in the visual evaluation results between the groups given different concentrations of iodine at the same injection rate (group A vs group B, group C vs group D). The visual evaluation results of group C were significantly better than those of group B (P < .01).


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  		TABLE 3. Degree of Visualization of the Peripheral Branches of the Hepatic Artery on 3D Images

 

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  		TABLE 4. Comparison of the Visual Evaluation Results among the Four Groups

 
Results of the Quantitative Evaluation
The mean postcontrast CT number of each group is shown in Table 5, and results of the analyses are shown in Table 6. Multiple-group comparisons confirmed statistically significant differences (P < .01). As was the case with the visual evaluation results, post hoc tests confirmed that there were statistically significant differences in the quantitative evaluation results between the groups that were given the same concentration of iodine at a different injection rate (group A vs group C, P < .01; group B vs group D, P < .01). However, there were no statistically significant differences between the groups that were given different iodine concentrations at the same injection rate (group A vs group B, group C vs group D).


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  		TABLE 5. Postcontrast CT Numbers of the Aorta in the Four Groups

 

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  		TABLE 6. Comparison of the Postcontrast CT Number of the Aorta among the Four Groups

 
The injection rate of 5 mL/sec was significantly superior to that of 4 mL/sec, both in the visual evaluation and in the quantitative evaluation. At administration of a contrast agent with an iodine concentration of 300 or 350 mg/mL, there were no statistically significant differences in either the visual or the quantitative evaluations of the 3D CT angiographic images.

Correlation between Visual Evaluation and Quantitative Evaluation Results
Spearman rank correlation coefficient rank test confirmed that there was a statistically significant positive correlation between the visual evaluation and the quantitative evaluation results ({rho} = 0.92, P < .01).

Table 7 shows the mean postcontrast CT number of the aorta among patients with each of the four visual evaluation grades. One-way ANOVA revealed a statistically significant difference among the four grades (P < .01), and post hoc pair-wise tests revealed statistically significant differences between each pair of groups.


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  		TABLE 7. Postcontrast CT Numbers of the Aorta in Patients with Each Visual Evaluation Grade

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
REFERENCES
 
Assessment of hepatic arterial angiogenesis is particularly important prior to liver transplantation (16). In particular, for transplantation of the left lobe, preassessment of each segmented bifurcation of the left hepatic artery is necessary, since the peripheral branches are anatomically complicated (17). The recent development of the microcatheter system has enabled transcatheter arterial embolization into the hepatic segmental or subsegmental peripheral artery (18,19). Thus, transcatheter arterial embolization can be performed in more specific feeding arteries for the treatment of hepatic tumors. Three-dimensional CT angiographic images are expected to sufficiently depict at least the subsegmental hepatic branches for these purposes.

The current trend in 3D CT angiography is moving away from the maximum intensity projection and the shaded-surface display methods toward the volume-rendering method (20). Volume rendering is already well known for its excellence in depicting 3D images. Recent study findings revealed that it is also better than the maximum intensity projection and shaded-surface display in depicting the peripheral arteries (7).

Three-dimensional CT angiographic images with use of volume rendering are constructed by enhancing voxels with blood vessel attenuations by using the difference in the CT number between the blood vessel and the surrounding tissues. Therefore, as the difference in the CT numbers increases, better high-quality images would be obtained. This hypothesis is supported by the report of Hong and Freeny (7), in which they stated that peripheral vessel detections are empirically dependent on the enhancement effects of blood vessels.

It is difficult to precisely measure the enhancement of the contrast agent in the peripheral branches because of their small diameters. Instead, the abdominal aorta was selected because we believed that the degree of enhancement of the abdominal aorta would be similar to that of the peripheral branches and because measurements made with the abdominal aorta should be more precise. Our results demonstrated a correlation between the degree of visualization of the peripheral branches of the hepatic artery on 3D CT angiographic images and the degree of enhancement of the contrast agent in the abdominal aorta. Although our results were indirect, they demonstrated a significant correlation between the visualization and the enhancement of the contrast agent in peripheral branches of the hepatic artery at 3D CT angiography. Our results showed that a high visual evaluation grade is associated with a high mean postcontrast CT number.

We consider a higher postcontrast CT number desirable; however, the minimum postcontrast CT number necessary to obtain images useful for interventional radiology is 395 HU, which was the mean postcontrast CT number in cases with the visual evaluation grade of good. We attribute a fair or poor rating of visual evaluation to inadequate enhancement effects in those cases.

We analyzed the relationship between the results at visual and quantitative evaluations among all of the patients. There are at least two ways to increase aortic enhancement at CT: One way is to increase the injection rate and another way is to increase the concentration of iodine. Previous reports have shown that a higher postcontrast CT number was obtained with a higher injection rate in the artery (21–23). In the current study, the injection rates of 4 and 5 mL/sec were compared, since many institutions use an injection rate of 3–5 mL/sec for 3D CT angiography (1,2,6–9,14). Our results demonstrated that an injection rate of 5 mL/sec was superior to the rate of 4 mL/sec at both visual evaluation and quantitative evaluation. By using the injection rate of 4 mL/sec (group A iodine concentration, 300 mg/mL; group B iodine concentration, 350 mg/mL), approximately 50% of the 3D images showed a potential for diagnosis and were graded as excellent or good in the visual evaluation. Furthermore, the degree of visualization of the peripheral branches with the higher concentration of iodine injected at 4 mL/sec (group B) was lower than that with the lower concentration of iodine injected at 5 mL/sec (group C). Thus, we conclude that an injection rate of 4 mL/sec should not be used at 3D CT angiography for detection of the peripheral branches of the hepatic artery, since sufficient enhancement of contrast agent cannot be reliably achieved.

By comparing the visual evaluation results on 3D CT angiographic images obtained with a concentration of iodine of 300 or 350 mg/mL, the percentage of cases graded higher than "good" was 91% (30 of 33) at the higher concentration (group D) and 74% (26 of 35) at the lower concentration (group C). Although this difference was not statistically significant, the observed tendency may imply that an iodine concentration of 350 mg/mL is more beneficial for diagnosis.

Further, our results suggest that the same or much higher quality 3D CT angiographic images might be obtained by changing the administration method of the contrast agent according to the following protocols: (a) inject contrast agent with an iodine concentration of 300 mg/mL at a rate faster than 5 mL/sec or (b) inject contrast agent with an iodine concentration of 350 mg/mL or greater (370 or 400 mg/mL) at a rate faster than 5 mL/sec. These administration methods can be considered when finer segmental hepatic arteries need to be assessed, although there is certainly concern about the safety of intravenous injection.

It has been reported that multi–detector row helical CT may reduce the injection volume of a contrast agent needed for 3D CT angiography due to its shorter total scanning time (24). In the current study, we obtained sufficient image quality with 100 mL of contrast agent, while approximately 180 mL has been used in previous reports (1,2,8). The total injection time for 100 mL of the contrast agent was 20 seconds (5 mL/sec) or 25 seconds (4 mL/sec). However, the volume of contrast agent can be reduced since the mean scanning duration was 12.5 seconds. This indicates that a 3D CT angiographic image of similar quality would be produced with a shorter injection time due to a decreased total volume of a contrast agent.

In our 3D CT angiographic procedure, it was important to finish scanning within a relatively short time before the portal vein next to the artery became enhanced.

Seven patients (5%) were excluded from the analyses in the present study. In those patients, we could not evaluate the peripheral branches of the hepatic artery objectively because the portal veins were strongly enhanced. This may have been due to the individual patients rather than to the injection method used, since the seven patients were included in all groups except for group C. We speculate that in these seven patients, the contrast agent arrived much sooner than 10 seconds after the start of the injection when we started scanning as a result of faster perfusion. Faster perfusion would also explain why the portal veins were enhanced in these cases.

Since the enhancement of portal veins substantially blurs the hepatic artery at 3D CT angiography, the timing of scanning must be optimized in those special cases. Improvement may be possible by changing the default settings in the automatic detection system if faster perfusion is the primary cause of the high enhancement of portal veins. For example, if we start monitoring CT earlier than 10 seconds after the injection of a contrast agent, it may reveal the appropriate timing even in the case of faster perfusion. Moreover, the triggering threshold can be calculated for individual patients if fast perfusion was predicted.

In summary, we believe, on the basis of our study results, that an injection rate of 5 mL/sec of contrast agent is necessary to obtain sufficient image quality of the peripheral branches of the hepatic artery at 3D CT angiography. In addition, a contrast agent with an iodine concentration of 350 mg/mL is preferable to increase the diagnostic capability, although it was not statistically significant when compared with a 300 mg/mL concentration of iodine.


   ACKNOWLEDGMENTS
 
The authors thank Yasuichiro Nishimura of the Mathematics Department of Osaka Medical College for assistance with the statistical analyses.


   FOOTNOTES
 
Abbreviations: ANOVA = analysis of variance, 3D = three dimensional

Author contributions: Guarantors of integrity of entire study, M.T., I.N.; study concepts and design, all authors; literature research, M.T., K.M.; clinical studies, M.M., K.M., S.Y.; data acquisition, M.T., S.Y.; data analysis/interpretation, all authors; statistical analysis, M.T.; manuscript preparation, M.T., T.S.; manuscript editing, T.S., I.N.; manuscript definition of intellectual content, revision/review, and final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 

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