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Published online before print October 19, 2006, 10.1148/radiol.2413051858

(Radiology 2006;241:831.)

A more recent version of this article appeared on December 1, 2006
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© RSNA, 2006

Musculoskeletal Imaging

Vertebral Marrow Fat Content and Diffusion and Perfusion Indexes in Women with Varying Bone Density: MR Evaluation1

James F. Griffith, FRCR, David K. W. Yeung, PhD, Gregory E. Antonio, FRCR, Samuel Y. S. Wong, MRCP, Timothy C. Y. Kwok, MRCP, Jean Woo, FRCP and Ping C. Leung, FRCS

1 From the Departments of Diagnostic Radiology and Organ Imaging (J.F.G., D.K.W.Y., G.E.A.), Community and Family Medicine (S.Y.S.W., T.C.Y.K., J.W.), and Orthopaedics and Traumatology (P.C.L.), Chinese University of Hong Kong, Prince of Wales Hospital, 30-32 Ngan Shing St, Shatin, Hong Kong SAR, China. Received November 15, 2005; revision requested January 4, 2006; revision received January 23; accepted March 2. Supported by a Direct Grant for Research, Chinese University of Hong Kong, reference no. 2004.1.066. Address correspondence to J.F.G. (e-mail: griffith{at}ruby.med.cuhk.edu.hk).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To prospectively study the relationship among vertebral marrow fat content, marrow diffusion indexes, and marrow and erector spinae muscle perfusion indexes in female subjects with varying bone mineral density.

Materials and Methods: Institutional study approval and informed consent were obtained. Dual x-ray absorptiometry, proton magnetic resonance (MR) spectroscopy, diffusion-weighted MR imaging, and dynamic contrast material–enhanced MR imaging of the lumbar spine and erector spinae muscle were performed in 110 women (mean age, 73 years; range, 67–84 years). Marrow fat content, marrow apparent diffusion coefficient (ADC), and perfusion indexes (maximum enhancement and enhancement slope) of marrow and erector spinae muscle were compared among three bone density groups (normal, osteopenic, and osteoporotic). The t test comparisons and Pearson correlations were applied.

Results: Seven subjects were excluded, which yielded a final cohort of 103 subjects: 18 with normal bone density, 30 with osteopenia, and 55 with osteoporosis. Vertebral marrow fat content was significantly increased in the osteoporotic group (67.8% ± 8.5 [standard deviation]) when compared with that of the normal bone density group (59.2% ± 10.0, P = .002). Vertebral marrow perfusion indexes were significantly decreased in the osteoporotic group (enhancement slope, 1.10%/sec ± 0.51) compared with those of the osteopenic group (1.45%/sec ± 0.51, P = .01) and normal bone density group (1.70%/sec ± 0.52, P < .001). Erector spinae muscle perfusion indexes did not decrease as bone density decreased. The ADC of vertebral marrow did not change with bone density.

Conclusion: The subjects experienced a decrease in vertebral marrow maximum enhancement and enhancement slope and an increase in marrow fat content as bone density decreased. The reduction in perfusion indexes occurred only within the vertebral body and not in the paravertebral tissues supplied by the same artery.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Osteoporosis is a disease characterized by reduced bone strength and that predisposes to fracture (1). Bone strength and fracture risk depend on bone quality, as well as bone mineral density. Bone quality embodies features such as trabecular architecture, trabecular connectivity, and fatigue damage and its repair, whereas bone density is a function of peak bone mass minus the rate and duration of subsequent bone loss (2). Many factors associated with increased individual susceptibility to osteoporosis have been identified, such as advancing years, female sex, estrogen deficiency, family history of low-trauma fracture, low body weight, smoking, excessive alcohol intake, low calcium intake, inadequate physical activity, frailty, poor health, and certain drugs (3). The actual pathophysiology of osteoporosis, however, remains unclear.

Magnetic resonance (MR) imaging enables investigation of three aspects of bone physiology—namely, marrow fat content, marrow diffusion, and perfusion—that may provide insight to the pathogenesis of osteoporosis. Results of recent dynamic contrast material–enhanced MR imaging and proton hydrogen 1 (1H) MR spectroscopic studies of the lumbar spine have indicated that as bone density decreases, marrow perfusion indexes decrease and, in male subjects, marrow fat increases (4,5). Because sex differences have been described in studies of vertebral body perfusion indexes and marrow fat in healthy subjects (6,7), we were interested in examining whether similar changes would occur in female subjects as did occur in male subjects of varying bone density (5). Thus, the purpose of our study was to prospectively study the relationship among vertebral marrow fat content, marrow diffusion indexes, and marrow and erector spinae muscle perfusion indexes in female subjects with varying bone density.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Subject Selection
One hundred ten postmenopausal women more than 65 years of age (mean, 73 years; range, 67–84 years) volunteered to participate in this prospective study between March 2004 and February 2005. As part of another ongoing study, recruitment notices inviting subjects to undergo dual x-ray absorptiometry (DXA) were placed in community centers for the elderly. Informed consent was obtained from participating subjects. The institutional review board approved the study. After undergoing DXA, all subjects were invited to undergo MR imaging, for which ethics approval and informed consent were additionally obtained. MR examination, which comprised 1H MR spectroscopy, diffusion-weighted MR imaging, and dynamic contrast-enhanced MR imaging of the lumbar spine, was performed within a mean of 11 days (range, 9–13 days) after DXA. Subjects were not recruited or were excluded from further analysis if they had (a) clinical or imaging evidence of metabolic bone disease or metastases, (b) a history of lumbar spinal surgery or irradiation, (c) a contraindication to MR examination, or (d) an incomplete MR examination. Results of the MR examination were made known to the participating subjects.

DXA Examination
The average bone density of four vertebrae (L1 through L4) of the lumbar spine on an anteroposterior projection (QDR-4500W; Hologic, Waltham, Mass) was used to obtain the bone density in grams per squared centimeter. On the basis of reference values derived from a local population (8), subjects were grouped into three categories according to T score and World Health Organization criteria (9). Normal bone density is defined as a T score greater than –1.0, osteopenia as a T score between –1.0 and –2.5, and osteoporosis as a T score less than –2.5.

MR Examination
MR examinations were performed with a 1.5-T whole-body imaging system (Intera NT; Philips Medical Systems, Best, the Netherlands) with a maximum gradient strength of 30 mT/m. A 20-cm-diameter circular surface coil centered at L3 was used. In the event of a vertebral body fracture (10) or other focal lesion at L3, the L2 vertebra was analyzed. After acquisition of scout images in transverse, coronal, and sagittal planes, T1-weighted (repetition time msec/echo time msec, 450/1) and T2-weighted (3500/120) sagittal images of the thoracic and lumbar portions of the spine were obtained to identify vertebral fracture, to help exclude subjects with metastases, and to guide positioning of a volume of interest within the L3 vertebral body for use at 1H MR spectroscopy.

The width (w), depth (d), and height (h) of the L3 vertebral body were measured on MR images to define a volume of interest. A volume of interest with dimensions w/2 · d/2 · h/2 cm3 was located centrally in the vertebral body (D.K.W.Y., with 10 years of working experience with MR imaging). After local shimming and gradient adjustments were performed, data were acquired at a spectral bandwidth of 1000 Hz and with 512 data points, and 64 non–water suppressed signals were obtained by using a point-resolved MR spectroscopic sequence (3000/25).

Fat-suppressed diffusion-weighted MR images were acquired in a single transverse section through the middle of the L3 vertebral body; a single-shot spin-echo echo-planar sequence (2000/105; section thickness, 10 mm; field of view, 250 mm; matrix, 128 x 128; four signals acquired), sensitized to incoherent motion with a pair of gradient pulses, was performed. Diffusion sensitivity parameters, or b values, were altered by varying the gradient amplitude while keeping the duration constant at 30 msec and separation time constant at 50 msec. Six diffusion-weighted images were acquired with different b values of 0, 100, 200, 300, 400, and 500 sec/mm2. Three diffusion-weighted images were acquired for each b value with the diffusion-sensitization gradient along the readout, phase-encoding, and section-selection directions, respectively. Isotropic diffusion-weighted images were calculated on a pixel-by-pixel basis with a similar method described elsewhere (11).

Dynamic contrast-enhanced MR images were acquired in the transverse plane through the mid-L3 region. Dynamic MR imaging was performed with a short T1-weighted gradient-echo sequence (2.7/0.95; prepulse inversion time, 400 msec; flip angle, 15o; section thickness, 10 mm; number of sections, one; field of view, 250 mm; acquisition matrix, 256 x 256; number of signals acquired, one). A total of 160 dynamic images were obtained in the midtransverse plane of L3 with a temporal resolution of 543 msec, which resulted in a total interrogation time of 87 seconds. A bolus of gadoteric acid (Dotarem; Guerbet, Aulnay, France) at a concentration of 0.15 mmol per kilogram of body weight was injected by using a power injector (Spectris; Medrad, Indianola, Pa) at a rate of 2.5 mL/sec through a 20-gauge intravenous catheter (Angiocath; Infusion Therapy Systems, Sandy, Utah) inserted in an antecubital vein. The injection was followed by a 20-mL saline flush. Dynamic MR imaging started at the same time the injection of contrast material started ("time zero"). Prior to contrast material injection, a transverse T1-weighted (578/12) image through the mid-L3 vertebral body was also acquired to guide the definition of region of interest (ROI) on the lower resolution contrast-enhanced MR images.

Data Analysis
MR spectroscopic data.—Spectra were analyzed at an off-line computer (Precision 650 Workstation; Dell, Austin, Tex). Water (4.65 ppm) and lipid (1.3 ppm) peak amplitudes were measured to determine vertebral marrow fat content, which was defined as the relative fat signal amplitude in terms of a percentage of total signal amplitude (water and fat) and calculated according to the following equation: fat content = [Ifat/(Ifat + Iwat)] · 100, where Ifat and Iwat are the peak amplitudes of fat and water, respectively. No correction for relaxation losses was applied.

Diffusion data.—The ROI was drawn manually by an author (D.K.W.Y.) and encompassed cancellous bone on the isotropic diffusion-weighted image obtained with a b value of 0 sec/mm2, and the same ROI was then applied to all other isotropic diffusion-weighted images obtained with different b values. The apparent diffusion coefficient (ADC) was calculated with a five-point regression method at b values of 100, 200, 300, 400, and 500 sec/mm2 by using the following equation: Ib = I0 · exp (–b · ADC), where Ib and I0 are the mean signal intensities in the ROI at a b value of 100, 200, 300, 400, or 500 and of 0 sec/mm2, respectively.

Maximum enhancement and enhancement slope.—On midtransverse T1-weighted MR images, ROIs separately encompassing the L3 vertebral body and the three elements of the erector spinae muscle were drawn manually (D.K.W.Y.) at a radiologic workstation (Viewforum; Philips Medical System) (Fig 1). The erector spinae muscle was selected rather than the psoas muscle because of the larger muscle bulk of the former. Time–signal intensity curves were recorded and processed at an off-line computer (Precision 650 Workstation; Dell). Two perfusion indexes of the time–signal intensity curves were measured—namely, maximum enhancement and enhancement slope. Maximum enhancement, or ME, was defined as the maximum percentage increase in signal intensity from baseline (Ibase). Enhancement slope, or ES, was defined as the rate of enhancement between 10% and 90% of the maximum signal intensity difference between maximum signal intensity (Imax) and Ibase. These perfusion indexes were calculated thus:

Formula
and

Formula
where t10% and t90% are the time intervals when the rise in signal intensity reaches 10% and 90% of the maximum signal intensity difference between Ibase and Imax, respectively. Both indexes are derived from the first-pass phase of signal intensity enhancement and are considered to represent arrival of contrast material into the arteries and capillaries and its diffusion into the extracellular space (14). Although these indexes are often predictive of perfusion, they are not a direct measure of perfusion. Maximum enhancement and enhancement slope time–signal intensity curve indexes are dependent on many factors, including the concentration of the contrast material bolus, blood volume, cardiovascular function, tissue perfusion, tissue permeability, and available leakage space (15,16).


Figure 1
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  		Figure 1: T1-weighted (578/12) transverse MR image of lumbar spine at L3 in a 68-year-old woman. Image shows manually drawn ROI positioned just within cortical margins of L3 vertebral body and individual components of erector spinae muscle for time–signal intensity data points measured from dynamic contrast-enhanced images. Erector spinae muscle complex is composed of three columns, which are (from medial to lateral) spinalis (S), longissimus (L), and iliocostalis (IL) (12,13).

 
Statistical Analysis
Data are presented as mean ± 1 standard deviation. Normal Q-Q and box plots were employed to examine normality and identify outliers. Logarithmic transformation was used to correct positive skewness of the variable enhancement slope for the erector spinae muscle. Variables were compared among the three bone density groups (normal, osteopenic, and osteoporotic) with the one-way analysis of variance test. Post hoc multiple comparisons were then conducted for significant variables by using a Bonferroni correction. Pearson correlation coefficients were calculated to assess the linear relationship between pairs of variables. Statistical analyses were performed with software (SPSS 11.0; SPSS, Chicago, Ill). A P value of less than .05 was considered to indicate a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Subjects
Seven subjects were excluded from the 110 women initially recruited because of failed contrast material injection in two subjects and motion artifact in five subjects. This resulted in a final cohort of 103 subjects (mean age, 72 years; age range, 67–84 years) (Table 1). The L3 vertebral body was analyzed in all subjects except in two subjects in whom the L2 vertebral body was analyzed. Bone density was normal in 18 subjects, bones were osteopenic in 30 subjects, and bones were osteoporotic in 55 subjects (Table 1).


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  		Table 1. Vertebral Marrow and Erector Spinae Muscle Measurements from MR Examinations in Three Female Bone Density Groups

 
Vertebral Marrow Fat Content
Vertebral marrow fat content increased as bone density decreased (Table 1, Fig 2). The osteoporotic group had, on average, a significantly higher vertebral marrow fat content than did the normal bone density group (P = .002) (Table 1, Fig 2). For paired data, a mild significant negative correlation was observed between T score and vertebral marrow fat content (r = –0.356, P < .001) (Table 2)—that is, marrow fat increased as bone density decreased.


Figure 2
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  		Figure 2: Graph shows vertebral marrow fat content for three bone density groups (normal bone density, osteopenic, and osteoporotic). Vertebral marrow fat content increased as bone density decreased. Horizontal bar = mean value for each group.

 

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  		Table 2. Pearson Correlation Coefficient Test Results in 103 Women with Varying Bone Density

 
Vertebral Marrow Maximum Enhancement and Enhancement Slope
Maximum enhancement decreased as bone density decreased (Table 1, Fig 3). The osteoporotic group had significantly lower mean maximum enhancement than did the normal bone density group (P < .001) (Table 1, Fig 4). Mean enhancement slope also tended to decrease as bone density decreased (Table 1, Fig 3). The osteoporotic group had a significantly lower mean enhancement slope when compared with that of the osteopenic group (P = .01) and the normal bone density group (P < .001) (Table 1). Moderate positive correlation was present between T score and both vertebral marrow maximum enhancement (r = 0.510, P < .001) and enhancement slope (r = 0.368, P < .001) (Table 2)—that is, bone perfusion indexes decreased as bone density decreased. Of all paired variables tested, the strongest correlations found were that an increase in vertebral marrow fat content correlated with a decrease in marrow maximum enhancement (r = –0.720, P < .001) and enhancement slope (r = –0.670, P < .001) (Table 2, Fig 4).


Figure 3
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  		Figure 3a: Graphs show vertebral marrow (a) maximum enhancement and (b) enhancement slope for three bone density groups (normal bone density, osteopenic, and osteoporotic). Both maximum enhancement and enhancement slope decreased as bone density decreased. Horizontal bar = mean value for each group.

 

Figure 3
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  		Figure 3b: Graphs show vertebral marrow (a) maximum enhancement and (b) enhancement slope for three bone density groups (normal bone density, osteopenic, and osteoporotic). Both maximum enhancement and enhancement slope decreased as bone density decreased. Horizontal bar = mean value for each group.

 

Figure 4
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  		Figure 4a: (a) Scatterplot shows inverse correlation between marrow fat content and maximum enhancement, which indicates that as marrow fat content increased, maximum enhancement decreased (r = –0.720). (b) Scatterplot shows a similar correlation between marrow fat content and enhancement slope. As marrow fat content increased, enhancement slope decreased (r = –0.670).

 

Figure 4
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  		Figure 4b: (a) Scatterplot shows inverse correlation between marrow fat content and maximum enhancement, which indicates that as marrow fat content increased, maximum enhancement decreased (r = –0.720). (b) Scatterplot shows a similar correlation between marrow fat content and enhancement slope. As marrow fat content increased, enhancement slope decreased (r = –0.670).

 
Erector Spinae Muscle Maximum Enhancement and Enhancement Slope
Both maximum enhancement and enhancement slope in the erector spinae muscle tended to increase in the osteoporotic group when compared with that of the osteopenic group and the normal bone density group, although these differences were not significant (P = .080 and P = .333, respectively) (Table 1, Fig 5). A mild significant negative correlation was observed between decreasing bone density and increasing erector spinae muscle maximum enhancement (r = –0.240, P = .015) (Table 2)—that is, muscle perfusion indexes tended to increase as bone density decreased. No correlation was present between vertebral body marrow perfusion indexes and erector spinae muscle perfusion indexes (P = .990 for maximum enhancement, P = .716 for enhancement slope) (Table 2).


Figure 5
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  		Figure 5a: Graphs of erector spinae muscle (a) maximum enhancement and (b) enhancement slope for three bone density groups (normal bone density, osteopenic, and osteoporotic). Both maximum enhancement and enhancement slope tended to increase in osteoporotic group when compared with that of osteopenic group and normal bone density group, although these differences were not statistically significant. Horizontal bar = mean value for each group.

 

Figure 5
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  		Figure 5b: Graphs of erector spinae muscle (a) maximum enhancement and (b) enhancement slope for three bone density groups (normal bone density, osteopenic, and osteoporotic). Both maximum enhancement and enhancement slope tended to increase in osteoporotic group when compared with that of osteopenic group and normal bone density group, although these differences were not statistically significant. Horizontal bar = mean value for each group.

 
Vertebral Marrow ADC
No significant difference in ADC values was observed among the osteoporotic group, osteopenic group, and normal bone density group (P = .505) (Table 1). For paired data, no correlation was present between either bone density or bone perfusion indexes and marrow ADC (P > .05) (Table 2), although a mild positive correlation was present between vertebral marrow fat content and ADC (r = 0.238, P = .017) (Table 2)—that is, as marrow fat content increased, marrow diffusion decreased.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
Our study was undertaken to examine the relationship among vertebral marrow fat content, marrow diffusion indexes, and perfusion indexes in women. Results of our study show a trend in female subjects similar to the trend in male subjects (5) from a previous study. Reduction in bone density is associated with a corresponding increase in marrow fat (4,5) and a reduction in marrow perfusion indexes (4,5). When the results for vertebral marrow fat content of this study are compared with results for that of a previously published study of male subjects of comparable age (5), postmenopausal women appear to have a greater vertebral marrow fat content than do men of comparable age. This finding is irrespective of whether the women had normal bone density (59.2% ± 10.0 for women vs 50.5% ± 8.7 for men), osteopenia (63.3% ± 9.5 for women vs 55.7% ± 10.2 for men), or osteoporosis (67.8% ± 8.5 for women vs 58.2% ± 7.8 for men). This finding is not in agreement with an earlier report of lumbar vertebral marrow fat content being higher in men than in women (7), although this earlier report involved subjects of a wide age range whose bone density was unknown.

Maximum enhancement and enhancement slope were used as indexes of perfusion. Both maximum enhancement and enhancement slope were approximately one-third less in the osteoporotic group when compared with that of the normal bone density group. A comparable reduction in perfusion indexes was reported in the previous study of male subjects (5). The overlap between marrow fat content and perfusion indexes for female subjects among bone density groups indicates that marrow fat content, maximum enhancement, and enhancement slope time measurements at MR imaging cannot be used, in isolation, to reliably determine bone density (5).

A link between arterial disease, particularly arterial calcification, and osteoporosis is suspected (17–22). Atherosclerosis causes endothelial dysfunction, which could, through decreased release of endothelial nitric oxide synthase, limit osteoblast formation or dampen the anabolic effect estrogens have on bone (23,24). Our study and other recent MR imaging–based studies (4,5) provide additional evidence of a link between vascular disease and osteoporosis. An association between diminished vertebral marrow perfusion indexes and increased arterial intimal thickness has also been reported (25). Our results show that perfusion indexes within the vertebral marrow decreased as bone density decreased. This effect may be primary or secondary to the development of osteoporosis. The vertebral bodies and the erector spinae muscle are supplied by the paired segmental lumbar arteries (12,13,26,27). If the observed reduction in perfusion indexes was related to general circulatory impairment or atherosclerosis in the aorta or main lumbar arteries, one would expect a similar reduction in perfusion indexes to occur in the erector spinae muscle. Rather than decrease, however, perfusion indexes for the erector spinae muscle tended to increase as bone density decreased. Reduction in bone mineral density is associated with a reduction in maximum enhancement and enhancement slope within bone, and this effect is not apparent in extraosseous tissues supplied by the same artery.

Separate rates of response of the inner and outer aspects of the bone cortex to bone active agents have recently been identified (28). The periosteal margin has a much lower (up to 10-fold) rate of bone formation than does the endosteal margin during treatment with bone active agents (28). Strong correlation between increasing vertebral marrow fat content and decreasing maximum enhancement (r = –0.720), as well as enhancement slope (r = –0.670), lent some support to the idea that increased fat within the confines of the vertebral body may simply be compressing sinusoids and thus affecting perfusion (29).

The MR diffusion technique we used is dependent mostly on interstitial fluid flow, cellularity, and extracellular water volume and to a lesser extent on microvascular perfusion (30). Increased interstitial fluid flow along bone canaliculi from repeated mechanical deformation has been proposed as an explanation for the anabolic adaptive responses occurring within bone to mechanical stress. Simulated interstitial fluid flow modulates bone growth mediators in bone cell cultures (31). Amplification of interstitial fluid flow may explain the reduced bone loss seen on images of postmenopausal women subjected to intermittent low magnitude vibrations (32). Because interstitial fluid flow will contribute to MR diffusion (30,33), we examined the relationship between bone marrow diffusion and bone density. Our study was performed with the subject at rest and showed no relationship between bone marrow ADC and bone density. A weak negative association between marrow ADC and marrow fat content was found, which indicated a reduction in molecular diffusion as marrow fat content increased.

Our study had several limitations. First, MR data were acquired from the L3 vertebra whereas bone density scores were averaged from four lumbar vertebrae (L1 through L4), because this is the accepted method of obtaining bone density T scores. Second, subjects were aware of their bone density result from DXA prior to enrollment to undergo MR examination. This may have led to the recruitment of fewer subjects with normal bone density than subjects with osteopenia or osteoporosis. Third, the results of MR imaging were made known to participating subjects, which may have prompted more subjects with back pain to undergo MR imaging.

In conclusion, for postmenopausal women, a decrease in bone density is associated with a corresponding increase in vertebral marrow fat content and a decrease in maximum enhancement and enhancement slope. This observed decrease in perfusion indexes occurs within the vertebral body and is not seen in paravertebral tissues with the same arterial supply. No relationship between vertebral marrow diffusion and bone density was found.


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


   ACKNOWLEDGMENTS
 
The authors thank Kai C. Choi, PhD, for his contribution and advice regarding statistical analysis.


   FOOTNOTES
 

Abbreviations: ADC = apparent diffusion coefficient • DXA = dual x-ray absorptiometry • ROI = region of interest

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, J.F.G., D.K.W.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; approval of final version of submitted manuscript, all authors; literature research, J.F.G., D.K.W.Y., T.C.Y.K.; clinical studies, J.F.G., S.Y.S.W., T.C.Y.K., J.W., P.C.L.; statistical analysis, J.F.G., D.K.W.Y.; and manuscript editing, all authors


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

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