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Magnetic resonance imaging relaxation times of female reproductive organs Yasuo Takatsu, Tsutomu Okada, Tosiaki Miyati and Takashi Koyama Acta Radiol published online 10 September 2014 DOI: 10.1177/0284185114542367 The online version of this article can be found at: http://acr.sagepub.com/content/early/2014/09/10/0284185114542367

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Acta Radiol OnlineFirst, published on September 10, 2014 as doi:10.1177/0284185114542367

Original Article

Magnetic resonance imaging relaxation times of female reproductive organs

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Yasuo Takatsu1,2, Tsutomu Okada3, Tosiaki Miyati2 and Takashi Koyama4

Abstract Background: Relaxation time of female reproductive organs affects the tissue contrast of magnetic resonance image (MRI), and is used for quantitative analysis. Purpose: To evaluate the relaxation times of normal female reproductive organs in the luteal phase of the menstrual cycle. Material and Methods: On a 1.5-T MRI, relaxation times were measured in pelvic tissues (endometrium, junctional zone, myometrium, follicle, and stroma) of 32 female healthy volunteers (33.5  6.8 years). The Look–Locker sequence was used to measure T1 relaxation times. Furthermore, a multiple spin-echo method with 32 different echo times was used to measure T2 relaxation times. The images were obtained in the luteal phase of each volunteer’s menstrual cycle. Results: The measured relaxation times (means  standard deviations) were as follows: endometrium (T1, 1703  147 ms; T2, 214  35 ms), junctional zone (T1, 1168  63 ms; T2, 72  12 ms), myometrium (T1, 1314  103 ms; T2, 138  20 ms), follicle (T1, 2267  249 ms; T2, 603  68 ms), and stroma (T1, 1481  129 ms; T2, 126  29 ms). Conclusion: Reliable MRI measurements of T1 and T2 relaxation times of normal female reproductive organs in the luteal phase of the menstrual cycle are useful as references to recognize the normal value.

Keywords Reproductive organs, magnetic resonance imaging, pelvis, relaxation time, luteal phase Date received: 27 March 2014; accepted: 14 June 2014

Introduction Female reproductive organs have complicated anatomical structures; therefore, magnetic resonance imaging (MRI) sequence parameters require optimization to obtain acceptable tissue contrast for diagnostic purposes. Before using an imaging method for clinical applications, a phantom study or volunteer study should be conducted to verify the experimental sequence parameters. Optimization of imaging protocols for female reproductive organs requires the knowledge of the changes in T1 and T2 relaxation times. These relaxation times help determine the tissue contrast and directly affect the selection of image pulse sequence parameters. Moreover, the quantitative analysis of abnormal values becomes possible if the normal value is known. Therefore, an accurate measurement of T1 and T2 relaxation times is essential to the

aforementioned assessment. However, limited data are available on female reproductive organ relaxation times. Measuring T1 and T2 relaxation times of tissues often requires long imaging times; consequently, patient exhaustion sometimes leads to inaccurate 1

Department of Radiology, Osaka Red Cross Hospital, Osaka, Japan Division of Health Sciences, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Japan 3 Department of Diagnostic Imaging and Nuclear Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan 4 Department of Diagnostic Radiology, Kurashiki Central Hospital, Okayama, Japan 2

Corresponding author: Yasuo Takatsu, Department of Radiology, Osaka Red Cross Hospital, 5-30 Fudegasaki, Tennouji-ku, Osaka, 543-8555, Japan. Email: [email protected]

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results caused by subject motion. One of the rapid acquisition methods for T1 relaxation time measurements is the Look–Locker sequence (1–8). Look– Locker sequences can be used to obtain a T1 relaxation curve to enable the measurement of T1 relaxation times. Furthermore, a multiple spin-echo method (9–12) can be used to measure T2 relaxation times. Relaxation times of the female reproductive organs are changing during the menstrual cycle (13–15). Myometrial thickness and endometrial area increase in a linear fashion during the preovulatory phase of the menstrual cycle (16). The junctional zone volume changes significantly between the follicular and periovulatory phases (17). The effect of strong uterine myometrial contractions during the menstrual phase (18) and distinct peristalsis of the junctional zone in the periovulatory phase (19) have been recognized. Therefore, the luteal phase was considered to be a more optimal phase for evaluation because both the myometrium and endometrium exhibit highest signal intensities during this phase (20). Although T1 and T2 relaxation times of the female organ have been reported (21), limited data are available from the luteal phase. In this study, premenopausal female volunteers were examined by the Look–Locker sequence and the multiple spin-echo method to obtain standard T1 and T2 relaxation times data of female reproductive organs in the luteal phase.

Material and Methods Institutional ethics committee approval and written informed consent were obtained for this study. Thirty-two healthy premenopausal female volunteers (mean age, 34 years; range, 24–46 years) without a history of irregular menstruation or any other physical findings of the disease were selected for the study. MRI was conducted in the luteal phase. The cycle date and phase were calculated from the last menstrual period and the normal menstrual cycle of individual women. All volunteers underwent imaging on a whole-body 1.5-T MR imager (Achieva; Philips Medical Systems, Best, The Netherlands) equipped with a body transmission coil. A receive-only surface array coil (32-channel SENSE Cardiac Coil) was used to perform MRI. A matrix of 128 pixels (the reconstruction matrix was 256 pixels) was used, with a field of view of 300 mm and a section thickness of 10 mm. Images were acquired as single sections. Targets were the three layers of the uterine corpus (endometrium, junctional zone, and myometrium) and the ovary (ovarian follicle and stroma). The imaging section was arranged on a straight line perpendicular to the center of the long

axis of the endometrium, junctional zone, and myometrium. A coronal view, including the ovary, was selected for the ovarian follicles and stroma. The Look–Locker sequence was used to measure the T1 relaxation times. The Look–Locker sequence has been commonly used for rapid T1 measurements because of its fast data acquisition. In this study, the Look–Locker sequence software was designed using a cardiac wave, and a dummy cardiac wave was derived from user-defined simulated electrocardiogram signals. The trigger delay time was changed from 74 ms to 5345 ms (122.6 ms durations). The T1 relaxation curve was obtained from real images. The repetition time (TR) was 20 ms, echo time (TE) was 1.93 ms, flip angle (FA) was 7 , and turbo field echo factor was 5. To recover the longitudinal magnetization, a dummy cardiac wave was set at a long value (R–R ¼ 8500 ms), and the shot interval value was 1 beat. The actual TR was 8500 ms. Longitudinal magnetization as a function of time can be described as MzðtÞ ¼ M0 ½1  2expðt=T1 Þ

ð1Þ

where M0 ¼ equilibrium magnetization and T1* ¼ apparent longitudinal magnetization relaxation time constant (1–8). The following equation was used to perform the three-parameter nonlinear curve fitting: y ¼ A  B expðt=T1 Þ:

ð2Þ

In equation 2, y denotes the signal intensity and T1* corresponds to the apparent modified T1 in the Look– Locker experiment. T1 was calculated from the resulting parameters T1*, A, and B by applying the equation T1 ¼ T1 ½ðB=AÞ  1,

ð3Þ

as used for studies with conventional Look–Locker techniques (2). We assumed that the transverse magnetization decay following spin–spin relaxation could be ignored (T2 relaxation time  TR). The multiple spin-echo method with 32 echoes was used to measure the T2 relaxation time. The TR was 3000 ms and TE was 25–800 ms (25 ms durations). Transverse magnetization as a function of time can be described as MxyðtÞ ¼ M0 expðt=T2Þ

ð4Þ

where M0 is the initial amplitude, T2 is the transverse relaxation time, and Mxy is the magnetization in the x–y plane.

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Fig. 1. (a) Look–Locker (trigger delay time of 687 ms) and (b) multiple spin-echo (sixth echo, echo time of 150 ms) images of the three layers of uterine corpus. Regions of interest were set to include the endometrium (gray circle), junctional zone (white circle), and myometrium (black circle).

JMP version 9.0.2 (SAS Institute, Cary, NC, USA) was used to perform non-linear curve fitting. The regions of interest (ROI) ranged between 7 and 20 mm2, and were set to include the endometrium, junctional zone, myometrium, ovarian follicle, and stroma. To calculate the average mean value, five ROIs were set in these tissues (Figs. 1 and 2). In addition, T1 and T2 relaxation times were measured.

Results The T1 and T2 relaxation times of the endometrium were longest, and the T1 and T2 relaxation times of the junctional zone were shortest of the three layers of the uterine corpus (Table 1). When differences between the mean values of each tissue were compared, the T1 and T2 relaxation times for the endometrium were approximately 1.5 and 3 times longer, respectively, compared with that for the junctional zone. For the myometrium, the T1 and T2 relaxation times were approximately 1.1 and 1.9 times longer, respectively, compared with that for the junctional zone. For the endometrium, they were approximately 1.3 and 1.6 times longer, respectively, compared with that for the myometrium; and for the ovarian follicle, approximately 1.5 and 4.8 times longer, respectively, compared with values in the stroma.

Discussion This study aimed to measure the standard T1 and T2 relaxation times of the reproductive organs of premenopausal women in the luteal phase. T1 and T2 relaxation times were easily measured. The Look–Locker sequence has an efficiency that is almost equal to that of the inversion recovery method (3). For FA < 10 , the theoretically derived method of evaluation leads to highly accurate results (2). The Look–Locker sequence was used to obtain suitable data because the dummy

cardiac wave was set at a long value (R–R ¼ 8500 ms) and the TR and FA were revised, average values were calculated from multiple ROIs, except the follicular and ovulatory phase. Therefore, we believe that these measurements were appropriate. Differences between each female reproductive organ were smaller for the T1 relaxation times than that for the T2 relaxation times; therefore, obtaining sufficient contrast of female reproductive organs was more difficult in T1-weighted (T1W) imaging compared with that of T2-weighted (T2W) imaging. In contrast, T2W images were highly useful in obtaining high-contrast MRI images of the female reproductive organs. In this study, T2 relaxation times of the endometrium was approximately 1.6 times longer than that of the myometrium. These results do not concur with those of another report where differences in T2 relaxation times between the myometrium and endometrium were subtle (21); moreover, the T2 relaxation times of the myometrium was longer than that of the endometrium (21), while the menstrual phase was not described. We believe that relaxation times depended on the menstrual cycle because signal intensities changed according to the menstrual cycle (20). In addition, the use of many measurement ROIs led to higher quality results than those obtainable from measurements of a few points. The present study had some limitations. Differences between the luteal phase measurements obtained in this study and follicular and periovulatory phase measurements could not be evaluated because of the difficulties in scheduling scanning plan for each volunteer in each menstrual phase accurately. Moreover, measurement data obtained in this study cannot be compared with those of other T1 and T2 relaxation time measurement methods because of long scanning time. To clarify that the changes in T1 and T2 relaxation times depend on the magnetic field strength, further studies using measurements in 3.0-T and comparing its results with the data of this study is needed.

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Fig. 2. (a, b) Look–Locker (trigger delay time of 687 ms) and (c, d) multiple spin-echo (sixth echo, echo time of 150 ms) images of the ovary. Regions of interest were set to include the ovarian follicle (white circle) and stroma (gray circle).

Table 1. T1 and T2 relaxation times in pelvic tissues.

Endometrium Junctional zone Myometrium Follicle Stroma

T1 relaxation times

T2 relaxation times

1703  147 1168  63 1314  103 2267  249 1481  129

214  35 72  12 138  20 603  68 126  29

Mean  standard deviation (ms).

In conclusion, we obtained reliable MRI measurements of T1 and T2 relaxation times of normal female reproductive organs in the luteal phase of the menstrual cycle that are useful as references to recognize normal values. Conflicting of interest None declared.

Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Magnetic resonance imaging relaxation times of female reproductive organs.

Relaxation time of female reproductive organs affects the tissue contrast of magnetic resonance image (MRI), and is used for quantitative analysis...
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