Published online November 3, 2003, 10.1148/rg.e19
(Radiographics. 2003;24:e19.)
© RSNA, 2003
Kinematics of the Uterus: Cine Mode MR Imaging1
Toshitaka Fujiwara, MD,
Kaori Togashi, MD, PhD,
Toshihide Yamaoka, MD,
Asako Nakai, MD,
Aki Kido, MD,
Soji Nishio,
Takayuki Yamamoto,
Hajime Kitagaki, MD, PhD and
Shingo Fujii, MD, PhD
1 From the Hitachi Medical Corporation Chaired Department of Diagnostic and Interventional Imageology (T.F., K.T.), the Departments of Nuclear Medicine and Diagnostic Imaging (T.Y., A.N., A.K.) and Gynecology and Obstetrics (S.F.), Graduate School of Medicine, and the Faculty of Medicine (S.N., T.Y.), Kyoto University, 54 Shyogoin Kawahara-cho, Sakyo-ku, Kyoto 606-8507, Japan; and the Department of Radiology, Shimane Medical University, Japan (H.K.). Presented as an educational exhibit at the 2002 RSNA scientific assembly. Received March 20, 2003; revision requested May 28; revision received October 1; accepted October 10. Address correspondence to T.F. (e-mail: tfuji@kuhp.kyoto-u.ac.jp)
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Abstract
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Cine mode magnetic resonance (MR) imaging has allowed evaluation of kinematics of the pelvis. Visualization of dynamic changes under strain facilitates evaluation of prolapses and adhesions between organs. The uterus, an organ of smooth muscle, has an inherent contractility that characterizes it as different from other visceral organs. This sustained contraction has occasionally been shown on static images as a finding masquerading as a leiomyoma or as adenomyosis. Cine mode MR imaging clearly shows the configuration of the myometrium during these dynamic changes, as well as its signal intensity during contractions. Uterine peristalsis, the subtle and rhythmic contractions of the inner myometrium, is also clearly identifiable on cine mode images as a wavy movement of the endometrium and/or inner myometrium. The direction and frequency of uterine peristalsis are different in each of the menstrual cycle phases and are thought to have important roles in uterine function, such as in fertility and menstrual blood discharge. Elucidation of these kinematics of the uterus will help in the evaluation of static MR images and study of the physiology of the uterus. Cine MR imaging is a novel technique for diagnosis and evaluation of the pelvic organs, especially the uterus.
© RSNA, 2003
Index Terms: Magnetic resonance (MR), functional imaging, 854.121419 • Magnetic resonance (MR), cine study, 854.121419 • Uterus, endometrium, 854.92 • Uterus, myometrium, 854.92 • Uterus, MR, 854.121419
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Introduction
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Recent advances in magnetic resonance (MR) imaging techniques have enabled us to obtain serial T2-weighted images of the uterus within an examination time of less than a second. More than a hundred images can be obtained within a few minutes. Cine mode display of these serial images in the same plane can demonstrate kinematics of the pelvic organs (1–4). This new tool provides new information that could never have been obtained or evaluated with traditional static MR imaging or computed tomography. It can show prolapse of the pelvic organs; it can also show finer definition of movement inherent in a pelvic organ. An example of the latter is uterine contractility, which has been recognized at ultrasonography (US) but is perceptible only as a pseudolesion in static MR images. Literature on cine mode MR imaging in the area of the pelvic organs is limited (1,2,4). Although preliminary, this article briefly reviews the conditions that can be evaluated at kinematic MR imaging. Understanding of kinematics is important for studying physiology of organs and in helping identify dysfunction, which can become apparent under a real-time load such as strain.
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Materials and Methods
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The study population consisted of 175 women: 42 healthy volunteers (age range, 22–88 years; mean, 45.2 years) and 133 patients (age range, 19–94 years; mean, 44.7 years) with main diagnoses such as uterine endometrial disease, myometrial disease, and pelvic floor weakness.
MR studies were obtained with a 1.5-T imager (Magnetom Symphony; Siemens Medical Systems, Erlangen, Germany) and phased-array coil. Half-Fourier-acquisition single-shot turbo spin-echo (HASTE) sequences were used to obtain serial T2-weighted images. During quiet respiration, 60 serial images (2,000/80 [repetition time msec/echo time msec]; field of view [FOV], 300 x 231 mm; section thickness, 5 mm; 256 x 192 matrix) were obtained at a rate of one every 2 seconds over 2 minutes in a midsagittal plane of the targeted organ. For some of the volunteers and for all patients with pelvic floor weakness, kinematic HASTE images were also obtained, both at rest and during the Valsalva maneuver. Axial and sagittal turbo-spin-echo T2-weighted images (5,470/122; turbo factor, 11; number of signals acquired [NSA], 1; FOV, 260 mm; section thickness, 5 mm; section gap, 1.5 mm; 512 x 256 matrix), sagittal spin-echo T1-weighted images (565/15; NSA, 1; FOV, 260 mm; section thickness, 5 mm; section gap, 1.5 mm; 512 x 256 matrix), and kinematic HASTE images were obtained for all women during each examination. For volunteers, however, sagittal spin-echo T1-weighted images were obtained at least once (usually on the 3rd day, when uterine changes due to menstruation are minimal) to confirm any finding suggesting underlying organic disease. Premedication, including anticholinergic drugs, was not used.
HASTE images were displayed in cine mode faster than real-time speed to facilitate evaluation of movement; uterine peristalsis, for instance, was evaluated at 12 times faster than real-time speed. Movie clips of these kinematic images were also made at 12 times faster than real-time speed, with video editing software (Ulead MediaStudio Pro 6.0; Ulead Systems, Taiwan, R.O.C.) on a PC.
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Female Pelvic Floor Weakness
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Pelvic floor weakness can involve abnormal descent of the bladder (cystocele), uterus, or vagina (uterine or vaginal vault prolapse); small bowel (enterocele), or rectum (rectocele). It is an important women's health problem, primarily affecting multiparous women more than 50 years old. Most patients with incontinence and minimal pelvic floor weakness can be treated on the basis of physical examination and basic urodynamic studies, and so do not need to undergo MR imaging. However, in patients with symptoms of multicompartmental involvement or in those who have undergone previous surgical procedures, dynamic MR imaging with ultrafast techniques such as single-shot fast-spin-echo, true fast imaging with steady-state precession, or HASTE at rest and during the Valsalva maneuver can be useful for evaluating pelvic floor weakness (2,5,6). Such examinations allow detection of hidden prolapses and assessment of muscle trophicity, as pelvic organ prolapse may be apparent only with increased abdominal pressure. In additon, real-time display shows dynamic changes in the anatomy (Movies 1, 2).
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Pelvic Adhesions
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Pelvic adhesions can be caused by endometriosis, pelvic inflammatory disease, trauma, surgery, or neoplasms. Peritoneal adhesions can be an important cause of infertility because they can affect tubal mobility or the access of ova to tubal fimbriae. Microsurgical adhesiolysis is the treatment of choice. Dense adhesions may also cause chronic pelvic pain. Women with chronic pelvic pain that does not respond to anti-inflammatory agents or contraceptives may undergo diagnostic laparoscopy as a standard procedure for identifying organic lesions, including adhesions (7). Adhesions make surgery difficult and especially limit the success of laparoscopic surgery, although the proper application of laparoscopic surgery benefits patients with regard to both cost and minimal invasiveness. Therefore, preoperative evaluation of adhesions is important. Usually, this evaluation can be done only by means of physical examination; to our knowledge, there are no accurate imaging studies available for identifying adhesions. Dense adhesions may be depicted as a tethered appearance of the intestinal loop or as attachment of the ovaries to the uterus (8). However, faint membranous adhesions are difficult to evaluate with any of the traditional imaging modalities.
MR imaging is known to be weak in evaluation of adhesions (9). The recent development of ultrafast MR imaging techniques has offered some resolution for evaluation of adhesions (4). Cine mode display of serial T2-weighted images, 200–380 images obtained at intervals of 20 seconds over a period of 4–7 minutes, were reported to provide useful information regarding adhesions (4,10). A recent preliminary report has shown that respiratory movements of the pelvic organs are indicators of adhesions (11). During free respiration, sliding movements between adjacent organs indicate the absence of adhesions (4). Kinematic MR images obtained at shorter time intervals may also provide information about adhesions (Figs 1, 2; Movies 3–5).
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Figure 1. Confirmed adhesions between the uterus and loops of the small intestine and closure of the Douglas pouch due to endometriosis in a 23-year-old woman. Static T2-weighted image shows a retroflexed uterus. The intestinal loop adjacent to the anterior wall of the uterus lacks peristalsis focally and lacks the sliding fine movement relative to the anterior wall of the uterus (arrow), indicating adhesion to the uterus, in contrast to other intestinal loops that show active peristalsis (arrowhead). See Movie 4.
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Figure 2. Confirmed adhesions between the uterus and endometrial cyst and closure of the Douglas pouch due to endometriosis in a 39-year-old woman. Static T2-weighted image shows an endometrial cyst behind the retroflexed uterus.
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Sustained Uterine Contractions
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The uterus has inherent contractility. Sustained uterine contraction is the focal and sporadic bulging of the myometrium, which is sustained for several minutes or, occasionally, even a half hour. Myometrial bulging is known to exhibit low signal intensity on static T2-weighted spin-echo images (12) (Fig 3). Blood is squeezed out from the contracted area and water content reduced because of the reduced blood volume. As a result, the contracted area exhibits a transient decrease in signal intensity (12). These focal contractions are known to masquerade as disease processes such as leiomyoma and adenomyosis. In kinematic displays, these focal and sporadic contractions may occasionally be seen as a course of changes in configuration and signal intensity, starting as a small focus, enlarging to distort the endometrium, and then disappearing (1) (Movie 6). Sustained contractions are frequently maintained for more than 2 minutes and mimic organic lesions on static images.
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Figure 3. Static turbo spin-echo image shows a sustained uterine contraction in a 23-year-old healthy volunteer. No abnormality, excluding possible adenomyosis or leiomyoma, is seen.
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Uterine Peristalsis
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Another inherent contractility of the uterus is seen as rhythmic and subtle and is limited to the inner third of the myometrium. At US, this faint contraction is known as uterine peristalsis, and it is perceptible with wavelike movements of the endometrium (endometrial stripping movement) (1,13–16). It has been reported that in order to contribute to rapid sperm transport and conservation of early pregnancy, the direction and frequency of the conduction is cycle dependent (1,13–16). The reported frequency of the conduction is about two to three times per minute, with peak frequency occurring during the periovulatory phase (13,16,17). Dysfunction of this contractility is a postulated cause of a variety of gynecologic and obstetric diseases, including infertility and pregnancy wastage (15,18–20). Although identifiable at real-time US, these subtle movements are not recognized at conventional MR imaging that takes more than a minute to obtain T2-weighted images of the uterus, the time resolution of this imaging being out of range of that of the peristalsis. Therefore, these subtle contractions have been previously disregarded at MR imaging.
Demonstration of Peristalsis with Cine MR Imaging
With use of an ultrafast imaging technique such as true fast imaging with steady-state precession or HASTE, kinematic MR imaging has allowed clear identification of uterine peristalsis as a wave conduction of a low-intensity area within the inner myometrium or as an endometrial stripping movement (1,21) (Movie 7). Nakai et al noted that the frequency and direction of uterine peristalsis shown with MR imaging are in accord with those seen in a comparative transvaginal US study (22) (Movie 8). The excellent tissue contrast provided by MR imaging allows identification of wave conduction not only in the inner myomterium but also toward the outer myometrium (22). However, because ovarian hormones do not produce diurnal changes, there has been no mention, to our knowledge, of diurnal change in peristalsis.
Changes during Menstrual Cycle Phases
Although there is no identifiable diurnal change, direction and frequency of peristalsis vary between menstrual cycle phases (21). Around the periovulatory phase, subendometrial low signal intensity is conducted from the cervix to the fundus. During menstruation, subendometrial low intensity is conducted from the fundus to the cervix. The direction and frequency of peristalsis appear to exactly fit the purposes of uterine functions, such as fertility and menstruation. Sperm transport may be supported by cervicofundal peristalsis in the periovulatory phase, while the fundocervical direction seems essential for menstrual blood discharge. The frequency is also identical with that reported in the sonography literature, that is about two to three times per minute, with peak frequency during the periovulatory phase (13).
Primary dysmenorrhea is one of the most common problems in young women. The reported prevalence rates of dysmenorrhea are as high as 44%–90% of women (23–25). Seven percent to 15% of women have severe menstrual pain that limits work or daily activity (25–27). The cause of primary dysmenorrhea is thought to be increased prostaglandin E2 production by the endometrium, resulting in uterine contraction (7). Cine MR imaging can directly show the extent of uterine contractions during menstruation and disappearance of uterine contractions with drug administration (28). Although many of the previous reports on dysmenorrhea and uterine contraction have involved direct insertion of a balloon or transducer catheter into the uterine cavity, kinematic MR imaging offers the possibility of a noninvasive tool for evaluation of uterine contraction (Movies 9, 10).
Effect of Anticholinergic Agents on Peristalsis
With use of anticholinergic agents, peristalsis of bowel loops and uterine contractility are both affected because the uterus consists of smooth muscle. This effect may partly explain the better image quality obtained with anticholinergic agents in gynecologic MR imaging (Movie 11).
Contraception and Peristalsis
Lyons et al, using transvaginal US, showed a "significantly" decreased frequency and distance of contractions in women taking oral contraceptives, compared with a control group (29). Kinematic MR images also clearly show the absence of or decreased peristalsis even in the periovulatory phase for contraceptive pill users (Movie 12). These exogenous agents are thought to have an influence on uterine peristalsis.
Leiomyoma and Peristalsis
Submucosal leiomyomas are frequently present in women of reproductive age. They often result in secondary endometrial changes that range from gland distortion to atrophy and ulceration and are recognized causes of abnormal genital bleeding, infertility, and pregnancy wastage (30–32). It is thought that submucosal leiomyomas cause dysfunctional uterine contractility, but the exact mechanism has not been elucidated (18–20). Evaluation of uterine contractility, including peristalsis, may be a new tool for finding the mechanisms of infertility caused by submucosal leiomyomas.
Disease and Peristalsis
Endometrial carcinomas are the most frequently encountered invasive malignant tumors in the female genital tact and are one of the most common cancers in women. In static MR images, the configuration of the junctional zone of the uterus has been indicated as a criterion for the staging of endometrial carcinoma (Fig 4). Although the kinematic MR imaging findings are preliminary, peristalsis seems to be disturbed at the site of myometrial invasion (Movie 13). Evaluation of peristalsis may provide another criterion for evaluation of disease processes involving the myometrium.
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Figure 4. Confirmed endometrial carcinoma (stage Ib) in a 79-year-old woman. Static T2-weighted image shows that the endometrium is abnormally thick for a woman of this age. A tumor with low signal intensity protrudes from the posterior wall of the uterus, indicating corpus carcinoma. The junctional zone is well preserved at the site of the tumor, indicating no myometrial invasion.
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Conclusions
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Cine mode display of MR imaging has allowed us to evaluate kinematics of the female pelvic organs. Recognition of the kinematics helps in evaluating static images and in understanding the functional aspects of the pelvic organs. The excellent display of the inherent contractility of the uterus on kinematic images especially helps in understanding that a static image is a summation type of image of the contractility. Cine mode MR imaging, a new technique applied to the pelvis, will develop as a novel aid in diagnosis of diseases of the pelvis and uterus.
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Acknowledgments
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We thank Masako Kataoka, MD, Department of Nuclear Medicine and Diagnostic Imaging, Graduate School of Medicine, Kyoto University, and Mizuki Nishino, MD, Department of Radiology, Kyoto City Hospital, for their sincere cooperation.
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Footnotes
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Abbreviations: HASTE = half-Fourier-acquisition single-shot turbo spin echo.
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Abstract
Introduction
