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Published online before print February 27, 2008, 10.1148/radiol.2471070585
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(Radiology 2008;247:147-153.)
© RSNA, 2008

Genitourinary Imaging

Physiology of Renal Medullary Tip Hyperattenuation at Unenhanced CT: Urinary Specific Gravity and the NaCl Concentration Gradient1

Christopher T. Hsu, MD, Zhen J. Wang, MD, Alan S. L. Yu, MBBChir, Robert G. Gould, ScD, Yanjun Fu, PhD, Bonnie N. Joe, MD, PhD, Aliya Qayyum, MBBS, Richard S. Breiman, MD, Fergus V. Coakley, MD, and Benjamin M. Yeh, MD

1 From the Department of Radiology, University of California–San Francisco, 505 Parnassus Ave, Box 0628, C-324C, San Francisco, CA 94143-0628 (C.T.H., Z.J.W., R.G.G., B.N.J., A.Q., Y.F., R.S.B., F.V.C., B.M.Y.); and Division of Nephrology, Department of Medicine, University of Southern California Keck School of Medicine, Los Angeles, Calif (A.S.L.Y.). Received March 29, 2007; revision requested May 29; revision received July 1; accepted August 1; final version accepted September 26. Address correspondence to B.M.Y. (e-mail: ben.yeh{at}radiology.ucsf.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Purpose: To retrospectively investigate the physiology of renal medullary tip hyperattenuation at unenhanced computed tomography (CT).

Materials and Methods: This retrospective single-institution study was IRB approved and HIPAA compliant. Informed consent was waived. One hundred consecutive patients (53 women, mean age, 52 years; 47 men, mean age, 48 years; P = .39) without and 34 (11 women, mean age, 49 years; 23 men, mean age, 45 years; P = .54) with unilateral ureteral obstruction underwent contemporaneous urinalysis and unenhanced CT. At CT, bladder urine attenuation was measured and two readers recorded the presence of renal medullary tip hyperattenuation. For obstructed kidneys (n = 34), renal pelvic urine attenuation was also recorded. The presence of medullary tip hyperattenuation was correlated with urinary specific gravity. To investigate the physiologic basis of medullary tip hyperattenuation, attenuations for NaCl and urea phantoms (range, 0–2000 mosm/kg) were recorded and correlated to solute concentrations by using linear regression.

Results: Patients with renal medullary tip hyperattenuation seen at CT had higher mean urinary specific gravity (1.023 and 1.022 for readers 1 and 2, respectively) than those without (1.015 and 1.016, respectively, both P < .05). The specific gravity correlated with higher urine attenuation (r = 0.40, P < .001). For the 34 patients with unilateral urinary obstruction, medullary tip hyperattenuation was less commonly seen in obstructed (two kidneys each for both readers) than nonobstructed (11 and 15 kidneys, respectively, both P < .005) kidneys and mean urine attenuation was lower in the obstructed renal pelvis (7.4 HU) than in the bladder (11.4 HU) (P < .005). Phantoms showed a 3.6-HU increase per 100-mosm/kg increase in NaCl concentration (r = 0.99, P < .001) but no change in attenuation with different urea concentrations.

Conclusion: Renal medullary tip hyperattenuation at unenhanced CT reflects increased urinary specific gravity, likely related to high medullary tip NaCl concentrations.

© RSNA, 2008


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Unenhanced computed tomographic (CT) examinations are widely used to evaluate the kidneys and renal collecting system, particularly for the evaluation of possible nephroureterolithiasis. A common imaging finding is the presence of visible hyperattenuation of the renal medullary papillary tips when compared with the remainder of the medulla and renal parenchyma. While this finding has been previously described, it has simply been attributed to a normal variant appearance in the kidney (1,2). Thus, we undertook this study to retrospectively investigate the physiology of renal medullary tip hyperattenuation at unenhanced CT.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Patients
This was a retrospective single-institution study approved by our Institutional Review Board and compliant with the Health Insurance Portability and Accountability Act. Informed written patient consent was waived by our Institutional Review Board. A computerized search for all unenhanced CT examinations of the abdomen and pelvis performed in our emergency department within 24 hours of urinalysis on patients over the age of 18 years during a 6-month period revealed 142 consecutive examinations in separate patients, all of whom had two kidneys. Eight patients were excluded from analysis because urinalysis was performed after contrast material administration. The remaining 134 patients were divided in two study groups by an attending radiologist (B.M.Y., with 6 years experience in clinical research in genitourinary imaging) on the basis of whether the CT examinations did not (n = 100) or did (n = 34) show ureteral obstruction. These two groups were studied separately. None of our study patients had bilateral ureteral obstruction.

The group of 100 patients without ureteral obstruction comprised 53 women (mean age, 52 years; range, 18–92 years) and 47 men (mean age, 48 years; range, 20–93 years) (P = .39). The group of 34 patients with unilateral ureteral obstruction comprised 11 women (mean age, 49 years; range, 23–75 years) and 23 men (mean age, 45 years; range, 20–84 years) (P = .54). The higher proportion of men to women with unilateral ureteral obstruction (P < .05) is in concordance with the known higher prevalence of renal stone disease in men (3–5). Of the final 134 examinations, 117 were performed for suspicion of urolithiasis, 10 for evaluation of back pain, five for evaluation of possible malignancy, and two for possible retroperitoneal hematoma. For the five examinations obtained for possible malignancy, the unenhanced CT was performed as a part of a multiphase CT scan. The duration of abdominal symptoms prior to CT imaging was not available for the majority of the patients in our retrospective study and was not recorded.

CT Technique
All patients were scanned by using a 16-section (n = 91) or eight-section (n = 43) multi–detector row CT scanner (LightSpeed; GE Healthcare, Milwaukee, Wis). No oral or intravenous contrast material was given for these scans. Images were acquired during a single breath hold with section thickness, 5 mm; table speed, 27.5 mm/sec (16-section scanner) or 27 mm/sec (eight-section scanner); gantry rotation time, 0.8 second; 120 kVp; and automated modulation of tube current with image noise set to 12 HU, which was the manufacturer preset for routine abdominal CT scans. The date and time of all CT examinations were recorded.

Image Interpretation
Two radiologists (C.T.H. and Z.J.W., with 5 and 4 years experience interpreting abdominopelvic CT, respectively) independently reviewed all CT images on a picture archiving and communication system workstation (IMPAX, version 4.5; Agfa, Mortsel, Belgium) with a level of 40 and window of 80 HU. For all 134 examinations, readers recorded the presence of renal medullary tip hyperattenuation, which was considered to be present when the tips of most of the medullary pyramids were visually of higher attenuation than that of the remaining renal parenchyma. The presence of medullary tip hyperattenuation was recorded as an overall impression (present in most of the medullary tips of both kidneys combined) for each of the 100 patients without renal obstruction and for each kidney separately for the 34 patients with unilateral ureteral obstruction.

For all patients, urine attenuation was recorded in the bladder by both readers in consensus. In addition, for the 34 patients with unilateral renal obstruction, urine attenuation was also recorded in the obstructed renal pelvis. These attenuations were recorded in the center of the structures of interest by using the largest possible elliptical region of interest, with care not to include the urothelium or areas with partial volume effect or obvious artifact. Attenuation measurements were not obtained in the unobstructed renal pelvis because the nondilated state of these structures made such measurements unreliable.

Laboratory Values
One author (B.M.Y., with 6 years experience in clinical research) retrieved the electronic record of urinalysis results obtained during each patient's emergency department visit and recorded the date and time of the urinalysis, as well as the urinary specific gravity and protein (milligrams per decaliter [micromoles per liter]), glucose (milligrams per decaliter [micromoles per liter]), and pH levels.

NaCl and Urea Phantoms
Because urinary specific gravity in healthy persons is predominantly determined by using the renal medullary NaCl and urea concentration gradient (Fig 1) (6), we sought to evaluate the effect of varying the concentrations of these substances on attenuation levels in a phantom. We constructed a CT phantom composed of 22 15-mL 1.2-cm-diameter polyurethane vials (Falcon; Becton Dickinson, Franklin Lakes, NJ). These tubes were filled with solutions of 0, 200, 400, 600, 800, 1000, 1200, 1400, 1600, 1800, and 2000 mosm/kg of NaCl (Fisher Scientific, Fairlawn, NJ) in distilled water and 0, 200, 400, 600, 800, 1000, 1200, 1400, 1600, 1800, and 2000 mosm/kg of urea (Fisher Scientific, Fair Lawn, NJ) in distilled water. These ranges of NaCl and urea osmolality were selected to cover the range of previously reported physiologic osmolalities in the renal medulla and urine (6).


Figure 1
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  		Figure 1: Nephron physiology. Plasma filtrate (white arrows) enters nephron through glomerulus. NaCl is actively transported (thick black arrows) from ascending loop of Henle and urea passively diffuses (thin black arrows) from collecting duct to renal medulla to generate a solute concentration gradient that is progressively higher in inner medulla than in outer medulla and cortex. Inner medulla corresponds to medullary tips seen at CT. (Adapted, with permission, from reference 6.)

 
The CT phantom was scanned with the same 16-section multi–detector row CT scanner with section thickness, 5 mm; table speed, 27.5 mm/sec; gantry rotation time, 0.8 second; 120 kVp; and tube current, 200 mA. This tube current was chosen to obtain low-noise images. It should be noted that while tube current affects image noise, it does not affect attenuation values. Two authors (B.M.Y., C.T.H.) recorded by consensus the attenuation of each NaCl solution by using a 1-cm2 elliptical region of interest, with care not to include the sides of the plastic vial or areas of obvious artifact.

Statistical Analysis
Statistical analysis was performed for each of the two study groups separately by using a computer software package (Stata, version 8.0; Stata, College Station, Tex). For the 100 patients without urinary obstruction, an unpaired t test was used to compare the mean urinary specific gravity among patients in whom renal medullary tip hyperattenuation was present. The urinary specific gravity was correlated with bladder urine attenuation levels. To assess independent predictors of renal medullary tip hyperattenuation, generalized estimating equations with binary outcome were employed by using a random-effects model that accounted for data from two readers (data was clustered by reader). Age, sex, specific gravity, time between urinalysis and CT, and urine protein and glucose levels were included in the statistical model. Interobserver agreement for renal medullary tip visualization scores was determined by using the {kappa} statistic. Interobserver agreement was classified as follows: poor, {kappa} = 0–0.20; fair, {kappa} = 0.21–0.40; moderate, {kappa} = 0.41–0.60; good, {kappa} = 0.61–0.80; and excellent, {kappa} = 0.81–1.00 (7). For the 34 patients with unilateral renal obstruction, the presence of medullary tip hyperattenuation was compared between obstructed and nonobstructed kidneys by using a two-sample test for binomial proportions for matched-pair data (McNemar {chi}2 test). For the CT phantom experiment, the attenuations of NaCl and urea solutions were correlated to osmolality by using linear regression. For all tests, a P value of less than .05 was considered to indicate a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Patients without Urinary Obstruction
For readers 1 and 2, the presence of renal medullary tip hyperattenuation was associated with both a higher mean urinary specific gravity at urinalysis (1.023 vs 1.015 and 1.022 vs 1.016 for readers 1 and 2, respectively; both P < .05) and a higher mean attenuation of the bladder urine (14.9 HU vs 4.6 HU and 13.2 HU vs 5.7 HU, respectively, both P < .001) than the absence of medullary tip hyperattenuation (Table). The interobserver agreement for finding renal medullary tip hyperattenuation was good ({kappa} = 0.80). The attenuation of the bladder urine was significantly correlated with urinary specific gravity (r = 0.40, P < .001).


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  		Renal Medullary Tip Hyperattenuation at CT and Findings at Urinalysis for 100 Patients without Urinary Tract Obstruction

 
Our generalized estimating equation model showed that urinary specific gravity was the only predictor of renal medullary tip hyperattenuation at urinalysis (P < .001). Urinary protein, glucose, and pH levels did not help predict the presence of renal medullary tip hyperattenuation seen at CT. In this model, renal medullary tip hyperattenuation was less common in patients scanned with a longer time delay after urinalysis (P < .001), and was more common in women (P < .01) and younger patients (P < .05). The median time duration from urinalysis to CT examination was 84 minutes (range, –349 to 1176 minutes).

Patients with Unilateral Ureteral Obstruction
For the 34 patients with unilateral ureteral obstruction, renal medullary tip hyperattenuation was less frequently seen in the obstructed than in the nonobstructed kidneys (two vs 11 kidneys, P < .005 for reader 1 and two vs 15 kidneys, P < .001 for reader 2) (Figs 2, 3). For these patients, the mean attenuation of urine in the obstructed renal pelvis was significantly lower than that of the bladder (7.4 HU vs 11.4 HU, P < .005). However, the attenuation of urine in the bladder and the obstructed renal pelvis both correlated with urinary specific gravity at urinalysis (r = 0.44, P < .05 and r = 0.56, P < .005, respectively).


Figure 2
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  		Figure 2: Unenhanced transverse CT scan of 54-year-old woman with right midureteral stone (not shown). Right renal medullary tips are of similar attenuation to surrounding renal parenchyma but left renal medullary tips (arrows) show visibly higher attenuation. Both readers recorded renal medullary tip hyperattenuation as present only for left kidney.

 

Figure 3
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  		Figure 3: Unenhanced transverse CT scan of 42-year-old woman with left ureterovesical junction stone (not shown). Right medullary tips (arrow) have slightly higher attenuation than surrounding renal parenchyma; medullary tip hyperattenuation was recorded as present only by reader 1. Both readers recorded renal medullary tip hyperattenuatoin as not present for left kidney.

 
NaCl and Urea Phantoms
A linear correlation was seen between attenuation and NaCl concentration (r = 0.99, P < .0001), with the attenuation increasing by 3.6 HU for each 100 mosm/kg increase in NaCl concentration (Fig 4). No increase in attenuation was seen with increasing urea concentrations from 0–2000 mosm/kg.


Figure 4
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  		Figure 4: NaCl and urea phantom. Solutions of either NaCl or urea were prepared in distilled water to concentrations of 0–2000 mosm/kg and were scanned with 120 kVp. The solution attenuations were plotted against solute concentration for NaCl and urea. For every 100-mosm/kg increase in NaCl concentration, the solution attenuations increased by 3.6 HU. In contrast, changes in urea concentration did not result in appreciably higher attenuation. Attenuations and actual CT images for each data point are shown on rows above graph.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Our study was a stepwise investigation of the physiologic basis for renal medullary tip hyperattenuation at unenhanced CT. First, we found that patients with renal medullary tip hyperattenuation at unenhanced CT have a significantly higher urinary specific gravity at urinalysis, which indicates that the kidneys of these patients are producing more concentrated urine. Second, we found that higher urinary specific gravity correlates with higher urine attenuation, suggesting that attenuation can be used as an indicator of urinary specific gravity. Third, we found that obstructed kidneys, which are well known to produce dilute urine (8–11), produce urine of lower attenuation, as shown in the obstructed renal pelvis when compared with that of the bladder, and are less likely to have renal medullary tip hyperattenuation than the contralateral nonobstructed kidneys. These findings suggest that, even in the same patient, kidneys with renal medullary tip hyperattenuation produce more concentrated urine than kidneys without medullary tip hyperattenuation. Fourth, since it is known that urinary specific gravity depends predominantly on the medullary urea and NaCl gradient (6), we measured the attenuations of NaCl and urea solutions across the range of physiologic concentrations. In this experiment, attenuation increased predictably and linearly with increased NaCl but did not vary with urea concentration. Taken together, our results show that CT may be a readily available potential noninvasive means to help assess the renal medullary concentration gradient in vivo.

We found that renal medullary tip hyperattenuation at unenhanced CT correlates significantly with a high urinary specific gravity, but not with other findings at urinalysis. Our findings build upon those of Lautin et al (1,2), who showed that renal medullary tip hyperattenuation seen at CT may occur in normal patients, and Tublin et al (12), who found that renal medullary tip hyperattenuation may disappear soon after patients are hydrated. These findings indicate that renal medullary tip hyperattenuation is related to a state of relative dehydration and may fluctuate between patients and within patients from day to day. Indeed, the physiologic fluctuation in the strength of the medullary salt gradient, which refers to the progression to a higher salt concentration from the outer to the inner medulla, has been well described in animal models during states of hydration and dehydration. In rats, for example, the measured renal medullary interstitial osmolality is quite low when they are well hydrated and increases twofold with dehydration (13), and up to fivefold with administration of vasopressin, a hormone that is normally released in response to hypovolemia or hypernatremia (14).

Furthermore, our results suggest that medullary tip hyperattenuation can regress quickly: Our generalized estimating equation model showed that renal medullary tip hyperattenuation is less common with more time after urinalysis. In our hospital, patients with suspected renal colic are routinely hydrated with intravenous fluids, and patients with longer time prior to CT examination were certainly better hydrated.

To further investigate the cause of reversible renal medullary tip hyperattenuation at unenhanced CT, we assessed the effect of varying concentrations of NaCl and urea on attenuation in a CT phantom. It is known that high urinary specific gravity is predominantly a result of increased urinary concentration of NaCl and urea (6,15) and that urine is concentrated via a countercurrent exchange mechanism (6). In this countercurrent exchange, plasma filtrate, which has an osmolality of approximately 280 mosm/kg, enters the proximal tubule and encounters gradually increasing interstitial and/or extratubular concentrations of NaCl and urea, which can reach combined osmolalities of 1200–1400 mosm/kg or greater (15). As the filtrate passes into regions of higher osmolar concentration, water is passively reabsorbed from the filtrate, causing the filtrate to become more concentrated prior to leaving the tubules as urine. Higher urea and NaCl concentrations in the medullary tip result in more concentrated (higher specific gravity) urine (6).

In our CT phantom experiment, we found that attenuation increases linearly with increases in NaCl concentration. Interestingly, although urea is a major component of the renal medullary interstitial concentration gradient, variations in urea concentration did not appear to influence its attenuation. This lack of effect on attenuation is likely related to the atomic composition of urea (CON2H4). Like water (H2O), urea is composed of atoms with very low k edges, hence, urea absorbs x-rays to a much lower extent than NaCl. The k edges of sodium and chloride are 1.7 keV and 2.8 keV, respectively, while the k edges of hydrogen, carbon, oxygen, and nitrogen are each at least 1000-fold lower. Therefore, the visible changes in the attenuation of the medullary tips strongly reflect changes in the NaCl concentration at the medullary tips but are not affected much by urea concentration. Also, the results from our phantom experiment suggest that the higher attenuation of the urine with higher specific gravity is likely related to increased concentrations of nonureal molecules.

Unilateral loss of renal medullary tip hyperattenuation in the obstructed kidney at unenhanced CT likely represents direct in vivo evidence that the inner medullary NaCl concentration of that kidney is indeed reduced and is a secondary sign of renal obstruction. In addition, these findings may help explain the physiology and predict the well-known phenomenon of postobstructive diuresis. In this phenomenon, placement of a catheter into an obstructed urinary collecting system results in the transient and copious production of dilute urine from that kidney relative to the nonobstructed system (8–11). This production of dilute urine results from a reduced medullary interstitial concentration gradient that originates from impaired reabsorption of NaCl from the thick ascending tubule of the nephron (16); our findings suggest that CT can help visualize this unilateral reduced medullary concentration gradient. Reduction of the medullary concentration gradient in obstructed kidneys may have a basis in autoregulation because such a state would result in greater urine output from that kidney and higher urine pressure in the collecting system, thereby promoting the expulsion of debris or stones from the obstructed system.

In addition, the renal medullary interstitial concentration gradient is reduced under pathologic medullary thick ascending limb NaCl reabsorption, such as that which occurs in response to loop diuretic administration and in polyuric disorders in which high tubular flow washes out the medullary gradient (17), and in diseases such as sickle cell anemia, which diminish medullary blood flow through the vasa recta and impair countercurrent function (18). Potentially, assessment of the renal medullary concentration gradient may be of value in monitoring renal physiology and treatment for such patients.

Previously reported methods of measuring renal medullary salt concentrations involve placement of invasive probes (13,14) or use of sodium magnetic resonance imaging (19), which is an exploratory technique being tested only in specialized centers. Potentially, CT may provide readily available noninvasive, functional evaluation of the renal medullary NaCl concentration gradient, and may be employed for renal physiology studies and drug development, as well as the monitoring of specific disease states. A consideration for the use of CT in such investigations is the need to expose patients to ionizing radiation to gather such data. However, our findings add to recent literature, which shows the value of unenhanced renal CT findings for the assessment of renal physiology (20–22).

Our study had limitations. First, most patients in our study were evaluated for clinical concern for renal stones. Further study will be needed in a broader range of patients to determine the relevance of finding renal medullary tip hyperattenuation in patients with specific renal diseases.

Second, this was a single-institution study performed with CT scanners from a single manufacturer. Care should be taken by other centers when extrapolating our results, as different tube potentials or CT filters may be used.

Third, our unenhanced CT examinations were performed with standard clinical techniques. The use of a more optimized, focused CT technique, such as a lower tube potential of 80 kVp to increase tissue contrast (23), higher tube current to decrease image noise (23), or thinner sections (24), may improve results when assessment of the medullary NaCl gradient is of specific concern. Conversely, use of a lower tube current (milliamperes), such as that which is increasingly advocated for renal stone evaluation (25,26), may worsen CT image noise and limit the assessment of renal medullary tip hyperattenuation.

Fourth, other patient factors, such as hematocrit level and hematuria, were not investigated in our study. Potentially, blood vessels or hemorrhage in the renal sinus may mimic or cause renal medullary tip hyperattenuation at unenhanced CT.

Fifth, in some patients, renal medullary tip hyperattenuation may result, in part or as a whole, in microcalcifications, which have been previously shown to exist in normal patients in a series of classic reports by using microradiographs (27) and histologic sections (28–30). Several subsequent publications have assumed that renal medullary tip hyperattenuation seen at CT was a result of such microcalcifications, but in these reports, researchers did not compare CT findings with histologic findings, which would require undue invasive biopsy retrieval (31). Although the contribution of calcium or other substances with renal medullary hyperattenuation could not be evaluated in our retrospective study owing to impracticality, our results suggest that a large component of renal medullary tip attenuation can be attributed to the NaCl gradient. Potentially, the differentiation of medullary calcium from concentrated NaCl can be obtained with repeat unenhanced CT after either hydration (11) or drug inhibition of renal medullary NaCl transport; the clinical value of such determinations will require further study.

Notwithstanding these limitations, our findings show that the presence of renal medullary tip hyperattenuation at unenhanced CT correlates with increased urinary specific gravity and may be related to higher medullary NaCl concentration gradients. Potentially, CT may be a widely accessible noninvasive means to help evaluate the renal medullary NaCl gradient for monitoring specific renal disease, renal physiology studies, or drug development.


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


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


   FOOTNOTES
 
Author contributions: Guarantor of integrity of entire study, B.M.Y.; 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, C.T.H., Z.J.W., A.S.L.Y., B.M.Y.; clinical studies, C.T.H., Z.J.W., F.V.C., B.M.Y.; experimental studies, C.T.H., R.G.G., Y.F., B.M.Y.; statistical analysis, C.T.H., Z.J.W., B.M.Y.; and manuscript editing, C.T.H., Z.J.W., A.S.L.Y., B.N.J., F.V.C., B.M.Y.

Authors stated no financial relationship to disclose.


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

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