3 Tesla Diffusion Tensor Imaging (DTI) of Normal Uterus in Young and Middle-aged Women during the Menstrual Cycle: Evaluation of the Cyclic Changes of Fractional

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Anisotropy (FA) and Apparent Diffusion Coefficient (ADC) Values

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He Yonglan MD1#, Ding Ning MD1#, Li Yuan MD2, Li Zhuo MD1, Xiang Yang MD2, Jin Zhengyu MD1, Xue Huadan MD1*

Department of Radiology, Peking Union Medical College Hospital, Peking Union

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Medical College and Chinese Academy of Medical Sciences, Beijing, PR China Department of Obstetrics and Gynecology, Peking Union Medical College Hospital,

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Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing, PR

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China

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# He Yonglan and Ding Ning have contributed equally to this article.

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* Corresponding author: Xue Huadan MD. Mailing address: Shuai Fu Yuan #1,

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Dongcheng Dist. Beijing, 100730, PR China. Phone: +86 10 69155509. Fax: +86 10

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69155441. E-mail: [email protected]

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Acknowledgments

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We thank Liu Hui MD for MR DTI parameters setting of this study, Zhang Hao for serum

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hormone measurement and Han Wei PhD for providing local SAS evaluation programs.

Short title: DTI of Normal Uterus in Menstrual Cycle: Changes of FA and ADC Values

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Abstract Objectives: To evaluate cyclic changes of fractional anisotropy (FA) and apparent diffusion

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coefficient (ADC) values of normal uterus in different age groups during the menstrual cycle,

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and the correlation with serum female hormone levels.

Methods: 29 normal volunteers accepted diffusion tensor imaging (DTI) of the uterus on

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menstrual-phase (MP), follicular-phase (FP), ovulatory-phase (OP), luteal-phase (LP)

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respectively. FA and ADC values of uterine different layers on midsagittal images were

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measured. Differences between two age groups during the menstrual cycle were evaluated by

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mixed-liner models and one-way ANOVA analysis. Pearson correlation analysis compared

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variation of FA and ADC values with serum female hormone levels measured in MP.

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Results: During the menstrual cycle, endometrial FA values declined whereas ADC values

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increased with significant differences (p0.05) as

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well as FA values of myometrium (p=0.0961), but ADC values of myometrium showed increasing tendency (p0.05). During the menstrual cycle, FA values of the endometrium

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declined whereas ADC values increased with significant difference (Fig. 2) (Table 2). Serum

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E levels showed a moderate correlation with the difference of the FA values between MP and

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FP (p=0.045, r=0.389), MP and OP (p=0.008, r=0.511), whereas serum P, LH, FSH levels

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didn’t show such correlation with FA values during the menstrual cycle (p>0.05). Serum

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hormone levels didn’t show any correlation with ADC values of the endometrium during the menstrual cycle (p>0.05).

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Junctional zone Although without statistical difference (p>0.05), FA values of the junctional zone showed an increasing tendency as age increased, while ADC values showed an opposite trend compared

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with FA. FA and ADC values of the junctional zone showed no significant difference during the menstrual cycle (p>0.05) (Fig. 3) (Table 2). Serum hormone levels didn’t show any

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correlation with FA and ADC values of the junctional zone during the menstrual cycle

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(p>0.05).

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Myometrium

FA values of the myometrium in 30-40 years group were lower than that in 20-30 years group

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with no statistical difference (p=0.0917). FA values of the myometrium showed no significant

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difference during the menstrual cycle (p=0.0961) (Fig. 4a) (Table 2). ADC values of the

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myometrium showed significant difference during the menstrual cycle (MP vs LP p0.05).

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Three zonal structures of the uterus

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In MP, FA values of junctional zone were significant higher than that of myometrium

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(p=0.000). FA values of endometrium were lower than that of junctional zone (p=0.070) and

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higher than that of myometrium (p=0.067) without significant difference. During FP, OP and

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LP, FA values of the three zonal structures of uterus showed significant difference: FA values of junctional zone were significant higher than that of myometrium (FP: p=0.000; OP:

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p=0.000; LP: p=0.000; respectively) and endometrium (FP: p=0.000; OP: p=0.000; LP: p=0.000; respectively), while FA values of myometrium were significant higher than that of endometrium (FP: p=0.020; OP: p=0.000; LP: p=0.000; respectively). (Fig. 5a) (Table 3) In MP, ADC values of the three zonal structures of uterus showed significant difference:

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ADC values of myometrium were significant higher than that of junctional zone (p=0.000) and endometrium (p=0.000), while ADC values of junctional zone were significant higher

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than that of endometrium (p=0.006). During FP, OP and LP, ADC values of the three zonal

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structures of uterus showed significant difference: ADC values of myometrium were

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significant higher than that of endometrium (FP: p=0.000; OP: p=0.037; LP: p=0.000; respectively) and junctional zone (FP: p=0.000; OP: p=0.000; LP: p=0.000; respectively),

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while ADC values of endometrium were significant higher than that of junctional zone (FP:

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p=0.022; OP: p=0.000; LP: p=0.000; respectively). (Fig. 5b) (Table 3)

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Discussion

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This study prospectively investigated menstrual-related layer-specific changes in FA and

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ADC values of the uterus in 29 normal women aged from 22 to 40 years old. Our results

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provided the initial information for the application of DTI in female pelvis during the

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menstrual cycle. Moreover, we found serum E levels showed a moderate correlation with the

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changes of FA values of the endometrium, which had not been reported in previous studies.

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As age increasing, FA values of the endometrium and junctional zone showed an

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increasing tendency, while FA values of the myometrium showed an opposite trend,

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indicating the different variation of uterine microstructural organization such as the density and orientation of fibrous tissue as age increased, although with no statistical differences. The

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previous study on cyclic changes of the uterine anatomical structures during the menstrual cycle showed the increasing tendency of the endometrium thickness, which exhibited moderate correlation of the serum E levels in the menstrual phase (23). The same correlation had been found between serum E levels and the changes of endometrial FA values which

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showed decline tendency during the menstrual cycle. It could be inferred that the higher serum E levels, the larger increase of the endometrium with higher isotropy of water diffusion

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directionality and lower FA values. Hence, FA values are partially influenced by the role of

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oestradiol on endometrial cell proliferation. In some oestradiol related gynaecological

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diseases, such as endometrial cancer, the interpretation of FA values of the endometrium should be considered with the patients’ serum E levels and certain menstrual phases. FA

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values of the junctional zone and myometrium showed no significant difference during the

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menstrual cycle, indicating the almost undetectable changes of normal uterine myometrium

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during the menstrual cycle, which could be used as a baseline for individual patients in

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clinical practice. FA values of the three zonal structures of the uterus showed significant

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difference at each phase during menstrual cycle. The relative order of FA values of these three

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layers in luteal phase was the same as Koji Fujimoto’s studies (14), reflecting the differences

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in the density of well-aligned fiber bundles. FA values of each layer in our study were smaller

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than previous ones, which might be explained by the different racial subjects as well as

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different MR scanners, image quality and ROI measurements in DTI.

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ADC values of the endometrium and myometrium tended to increase during the menstrual

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cycle, the same results were found by A KIDO et al to study changes in ADC of the normal uterus based on DWI (15). As ADC values are affected by cell density, cell organization,

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microcirculation (24), it is possible that the changes in ADC values seen during the menstrual cycle may reflect phase-specific physiological changes in three different zonal structures of the uterus. For the endometrium, the blood in menstrual phase could decrease the ADC values, just same as the decreased ADC values seen in ovarian endometrial cyst (25). For the

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myometrium, myometrial contraction and relatively low water content in menstrual phase might contribute to lower ADC values, whereas myometrial edema in the luteal phase might

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have higher ADC values. ADC values of junctional zone showed no significant difference

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during the menstrual cycle, which was the same as FA values. The possible explanation might

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be the unique architecture of junctional zone with a concentric arrangement of smooth-muscle fibers, even though early MRI studies reported the hormonal variation in the

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female reproductive cycle contributed to the changes in the thickness of junctional zone,

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paralleling to endometrial thickness but to a lesser degree (17).

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There were several limitations in our study. Firstly, the results are based on data from 29

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subjects, although the changes in different age groups during the four different phases of the

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menstrual cycle showed almost consistent trends. The feasibility of our results may not

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necessarily valid for larger populations, raising concern regarding the clinical implications.

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We will carry out the future study on a larger sample size. We could evaluate the influence of

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uterine location and axis in terms of anteversion or retroversion on FA and ADC values.

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Secondly, relatively large inter-individual variation of FA values of the endometrium had

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been observed in 20-30 years group in the menstrual phase. The possible reason might be the

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different contents of blood in the cavity. It would, therefore, be preferable to avoid using FA measurements obtained during the menstrual phase in order to minimise the effect of

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menstrual FA variation on baseline FA changes. In conclusion, dynamic changes of FA and ADC values of the uterus were observed during

menstrual cycle, showing significant differences among three zonal structures on each phase. Variation of FA values of endometrium correlated moderately with serum E levels in

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menstrual phase.

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normal uterus during the menstrual cycle: MR studies. Radiology 1986;161:459-462.

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23 He YL, Ding N, Xue HD, editors. Cyclic Changes of the Female Reproductive System in Young and

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Middle-aged Women during the Menstrual Cycle: an Initial 3T MRI Study based on T2 3D-Space

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Sequence. Proceedings of the 100th Annual Meeting of ESR: Viana, 2014. (abstract 2939)

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using apparent diffusion coefficients. J Magn Reson Imaging 2000;12:1014–1019.

Figure legends

Figure Legends Fig. 1 Measurement of FA and ADC values of the uterus on luteal-phase, images

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obtained from a 26-year-old healthy volunteer. Polygonal-shaped regions of interest

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(ROIs) were drawn on T2WI of the uterus on mid-sagittal plane (a) to cover the three

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zonal structures of the uterus (endometrium, red; junctional zone, green; myometrium, purple). The corresponding ROIs were automatically drawn on FA map (b) and ADC

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map (c) simultaneously. FA and ADC values were automatically calculated.

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Fig. 2 FA and ADC values of the endometrium between two age groups during the

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menstrual cycle. FA values of the endometrium declined (a) whereas ADC values

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increased with significant difference (b). No significant difference was found between

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age groups.

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Fig. 3 FA (a) and ADC (b) values of the junctional zone showed no significant

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difference during the menstrual cycle between age groups.

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Fig. 4 FA and ADC values of the myometrium between two age groups during the

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menstrual cycle. FA values of the myometrium showed no significant difference during the menstrual cycle (a), whereas ADC values of the myometrium showed increasing tendency during the menstrual cycle with significant difference (b).

Fig. 5 FA (a) and ADC (b) values of three zonal stuctures of the uterus showed

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significant difference in each menstrual phase during the menstrual cycle.

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Figure 1 Click here to download high resolution image

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Table1

Table 1 FA and ADC Values of Three Zonal Layers of the Uterus in Two Age Groups during the Menstrual Cycle

MY

ADC -3

EM 2

(10 mm /s) JZ

MY

OP

LP

20-30years(n=17)

0.279 ±0.108

0.181 ±0.047

0.163 ±0.027

0.138 ±0.057

30-40years(n=12)

0.278 ±0.052

0.200 ±0.040

0.166 ±0.049

0.147 ±0.039

20-30years(n=17)

0.319 ±0.068

0.300 ±0.058

0.304 ±0.079

0.285 ±0.071

30-40years(n=12)

0.312 ±0.078

0.306 ±0.088

0.338 ±0.044

0.288 ±0.080

20-30years(n=17)

0.247 ±0.055

0.229 ±0.031

0.232 ±0.037

0.214 ±0.039

30-40years(n=12)

0.233 ±0.045

0.212 ±0.041

0.204 ±0.037

0.206±0.042

20-30years(n=17)

1.018 ±0.158

1.320 ±0.169

1.408 ±0.116

1.476 ±0.183

30-40years(n=12)

1.045 ±0.105

1.319 ±0.075

1.445 ±0.173

1.354 ±0.219

20-30years(n=17)

1.170 ±0.156

1.254 ±0.087

1.252 ±0.140

1.277 ±0.145

30-40years(n=12)

1.154 ±0.153

1.199 ±0.160

1.161 ±0.064

1.233 ±0.133

20-30years(n=17)

1.789 ±0.224

1.859 ±0.127

1.838 ±0.191

2.003 ±0.157

30-40years(n=12)

1.739 ±0.160

1.819 ±0.175

1.901 ±0.155

1.978 ±0.147

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JZ

FP

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EM

MP

P

FA

Age groups

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Layers

Note: Data are mean±standard deviation. FA=fractional anisotropy, ADC=apparent diffusion coefficient,

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EN=endometrium, JZ=junction zone, MY=myometrium, MP=menstrual phase, FP=follicular phase, OP=ovulatory

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phase, LP=luteal-phase

Table2

Table 2 Cyclic Changes of FA and ADC Values during the Menstrual Cycle p values n=29

2

(10 mm /s)

LP

EM

0.279±0.090

0.189±0.046

0.164±0.038

JZ

0.316±0.072

0.302±0.071

MY

0.241±0.051

EM

MP- FP

MP- OP

MP- LP

FP- OP

FP- LP

OP- LP

0.141±.050

.000

.000

.000

.042

.000

.079

0.319±0.068

0.286±.075

.443

.861

.138

.333

.377

0.223±0.036

0.220±0.040

0.211±0.041

.036

.091

.014

.842

.181

1.030±0.139

1.320±0.140

1.424±0.144

1.425±0.207

.000

.000

.000

.019

.030

JZ

1.163±0.155

1.232±0.124

1.213±0.122

1.259±0.142

.119

.221

.024

.527

MY

1.768±0.201

1.843±0.149

1.865±0.179

1.993±0.154

.137

.079

.000

.605

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-3

OP

.056 .399 .968

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ADC

FP

.396

.142

.000

.002

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FA

MP

Note: Data are mean±standard deviation. FA=fractional anisotropy, ADC=apparent diffusion coefficient, EN=endometrium, JZ=junction zone, MY=myometrium, MP=menstrual phase, FP=follicular phase, OP=ovulatory

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phase, LP=luteal-phase

Table3

Table 3 Differences of FA and ADC Values among Uterine Three Zonal Structures during the Menstrual Cycle FP (n=29)

95%CI

FA

ADC (10-3 mm /s) 2

OP (n=29)

95%CI

LP (n=29)

95%CI

95%CI

p

lower

upper

p

lower

upper

p

lower

upper

p

lower

upper

JZ-EN

0.070

-.003

.078

.000

.085

.142

.000

.127

.182

.000

.115

.175

MY-EN

0.067

-.078

.003

.020

.005

.063

.000

.028

.083

.000

.039

.100

JZ-MY

.000

.034

.115

.000

.051

.108

.000

.071

.126

.000

.045

.106

EN-JZ

.006

-.227

-.039

.022

.013

.162

.000

.113

.356

.000

.076

.257

MY-EN

.000

.644

.823

.000

.449

.598

.037

.008

.252

.000

.476

.659

MY-JZ

.000

.510

.699

.000

.536

.686

.000

.243

.487

.000

.643

.825

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MP (n=29)

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Note: p =p values, EN=endometrium, JZ=junction zone, MY=myometrium, CI=confidential intervals, MP=menstrual phase, FP=follicular phase,

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OP=ovulatory phase, LP=luteal-phase

3-T diffusion tensor imaging (DTI) of normal uterus in young and middle-aged females during the menstrual cycle: evaluation of the cyclic changes of fractional anisotropy (FA) and apparent diffusion coefficient (ADC) values.

To evaluate cyclic changes of fractional anisotropy (FA) and apparent diffusion coefficient (ADC) values of normal uterus in different age groups duri...
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To study the integrity of white matter, we investigated the correlation between the changes in neuroradiological and morphological parameters in an animal model of acute obstructive hydrocephalus.

Diffusion tensor imaging of breast lesions: evaluation of apparent diffusion coefficient and fractional anisotropy and tissue cellularity.
To investigate the apparent diffusion coefficient (ADC) and fractional anisotropy (FA) measured by diffusion tensor imaging (DTI), tissue cellularity and their relationship in breast malignant/benign lesions.

Effects of MR parameter changes on the quantification of diffusion anisotropy and apparent diffusion coefficient in diffusion tensor imaging: evaluation using a diffusional anisotropic phantom.
To validate the usefulness of a diffusional anisotropic capillary array phantom and to investigate the effects of diffusion tensor imaging (DTI) parameter changes on diffusion fractional anisotropy (FA) and apparent diffusion coefficient (ADC) using

Microscopic diffusion anisotropy in the human brain: reproducibility, normal values, and comparison with the fractional anisotropy.
Human neuroimaging of tissue microstructure, such as axonal density and integrity, is key in clinical and neuroscience research. Most studies rely on diffusion tensor imaging (DTI) and the measures derived from it, most prominently fractional anisotr

Intercentre reproducibility of cardiac apparent diffusion coefficient and fractional anisotropy in healthy volunteers.
Diffusion tensor cardiac magnetic resonance (DT-CMR) enables probing of the microarchitecture of the myocardium, but the apparent diffusion coefficient (ADC) and fractional anisotropy (FA) reported in healthy volunteers have been inconsistent. The ai

Correlation between 3T apparent diffusion coefficient values and grading of invasive breast carcinoma.
The aim of this study was to evaluate whether the apparent diffusion coefficient (ADC) provided by 3.0T (3T) magnetic resonance diffusion-weighted imaging (DWI) varied according to the grading of invasive breast carcinoma.

Diffusion-weighted and diffusion-tensor imaging of normal and diseased uterus.
Owing to technical advances and improvement of the software, diffusion weighted imaging and diffusion tensor imaging (DWI and DTI) greatly improved the diagnostic value of magnetic resonance imaging (MRI) of the pelvic region. These imaging sequences

Assessment and quantification of sources of variability in breast apparent diffusion coefficient (ADC) measurements at diffusion weighted imaging.
Apparent Diffusion Coefficient (ADC) measurements are increasingly used for assessing breast cancer response to neoadjuvant chemotherapy although little data exists on ADC measurement reproducibility. The purpose of this work was to investigate and c

Diffusion-weighted imaging in the head and neck region: usefulness of apparent diffusion coefficient values for characterization of lesions.
We aimed to evaluate the role of apparent diffusion coefficient (ADC) values calculated from diffusion-weighted imaging for head and neck lesion characterization in daily routine, in comparison with histopathological results.

Role of diffusion-weighted magnetic resonance imaging and apparent diffusion coefficient values in the detection of gastric carcinoma.
The study evaluated the applicability of diffusion-weighted magnetic resonance imaging (DW-MRI) and apparent diffusion coefficient (ADC) values in the diagnosis and staging of gastric carcinoma (GC).