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Normal Imaging Findings of the Uterus 3

Claudia Klüner and Bernd Hamm

C O N T E N T S

3.1 Embryonic Development and Normal Anatomy of the Uterus 37 3.2 Imaging Findings: Uterine Corpus 40 3.3 Imaging Findings: Uterine Cervix 44

References 47

3.1

Embryonic Development and Normal Anatomy of the Uterus

During embryonal life, fusion of the two Müllerian ducts gives rise to the uterine corpus, isthmus, cervix, and the upper third of the vagina. The Müllerian ducts are of mesodermal origin and arise in the 4th week of gestation. They course on both sides lateral to the ducts of the mesonephros (Wolffi an ducts). The lower two thirds of the vagina arise from the sinovaginal bulb, which develops from the posterior portion of the urogenital sinus. The vaginal epithelium arises from the cellular lining of the urogenital sinus [1].

The uterus is composed of three distinct anatomic regions, namely the corpus, the isthmus (or lower uterine segment), and the cervix. In women of re- productive age, the uterus usually is 6–9 cm long and weighs 40–60 g. The longitudinal axis is fl exed for- ward (anteversion) with the corpus and cervix form- ing a blunt angle (antefl ection) (Fig. 3.1a). The uterus straightens with increasing bladder fi lling and the anteversion angle becomes smaller (Fig. 3.1b).

The wall of the uterine corpus differs from that of the cervix in that it mostly consists of myometrium,

C. Klüner, MD

Institut für Radiologie (Campus Mitte), Charité – Universitäts- medizin Berlin, Charitéplatz 1, 10117 Berlin, Germany B. Hamm, MD

Professor and Chairman, Institut für Radiologie (Campus Mitte), Klinik für Strahlenheilkunde (Campus Virchow-Klini- kum und Campus Buch), Charité – Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, Germany

the strong muscle coat forming the mass of the organ.

The myometrium is mostly comprised of spindle- shaped smooth muscle cells and additionally con- tains reserve connective tissue cells, which give rise to additional myometrial cells in pregnancy through hyperplasia. The uterine cavity is only a thin cleft and is lined by endometrium (Fig. 3.2). Functionally, the endometrium consists of basal and functional layers.

The isthmus of uterus (lower uterine segment), together with the internal os, forms the junction be- tween the corpus and cervix. In nonpregnant wom- en the isthmus is only about 5 mm high and is less muscular than the corpus. Unlike the uterine cervix, the isthmus becomes overproportionally large in the course of pregnancy and serves as a kind of reserve for fetal development in addition to the uterine cor- pus. The endometrium of the isthmus consists of a single layer of columnar epithelium and only under- goes abortive cyclic transformation.

The uterine cervix consists of the supravaginal cervical canal (endocervix) and the vaginal portion that projects into the vagina (Fig. 3.3). The wall of the cervix is primarily made up of fi rm connective tis- sue. In contrast to the uterine corpus, the muscular portion accounts for less than 10% of the cervical wall and primarily consists of smooth muscle cells in circular arrangement. The cervical canal is coated with mucus-producing columnar epithelium and contains numerous gland-like units, the crypts. The squamocolumnar junction is the transition from the columnar epithelium of the endocervix to the non- keratinizing squamous epithelium of the ectocervix and is situated at the level of the external os.

The uterus is supplied with blood through the uterine and ovarian arteries. The uterine arteries course to the organ through the cardinal ligaments and, at the level of the uterine isthmus (internal os of the cervical canal), divide into an ascending and a descending branch. Lymphatic drainage from the corpus is through the broad ligament into the para- aortic lymph nodes and from the cervix into parame- trial and iliac lymph nodes.

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Below, the parametria extend to the cardinal liga- ment, which passes from the uterine cervix to the pel- vic sidewall and separates the parametrium from the paravaginal connective tissue (paracolpium). A total of eight ligaments contribute to the support of the uterus. Diagnostically, which primarily pertains to the evaluation of the local extent of cervical cancer, the vesicouterine and the sacrouterine ligaments are most important. The vesicouterine ligament extends from the cervix to the posterior wall of the urinary bladder and only has a minor role in supporting the uterus. The sacrouterine ligament has a more im- portant supportive function and originates on the anterior aspect of the sacral bone, arches around the rectum and attaches at the level of the uterine isth- mus.

Most of the uterus is covered by peritoneum (Fig. 3.5). The peritoneum contributes only lit- tle support but ensures adequate mobility of the uterus relative to the urinary bladder and rectum, which is necessary to adjust to the variation in blad- der filling and especially during pregnancy. The peritoneum extends from the roof of the urinary bladder to the anterior uterine wall, forming the vesicouterine pouch in between. Below this fold, there is the vesicouterine ligament. The posterior peritoneal coat of the uterus extends downward to form the rectouterine pouch (Douglas space) that reaches to the level of the posterior vaginal fornix and from there extends to cover the anterior rectal wall.

Fig. 3.2. T2-weighted TSE image of a 40-year-old healthy wom- an in coronal orientation. The uterine cavity is marked by the white arrow

Fig. 3.1a,b. T2-weighted TSE images of two different healthy premenopausal women in sagittal orientation

a b

Besides the pelvic fl oor, the normal topography of the uterus is primarily ensured by the parametria, a kind of suspension system primarily consisting of connective tissue. In addition, the parametria contain large amounts of fatty tissue, especially in their lateral portions near the pelvic sidewall and a dense network of lymphatic and blood vessels. About 2 cm lateral to the uterine cervix, both ureters course through the parametria and cross the uterine arteries (Fig. 3.4).

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Fig. 3.5. T2-TSE image in sagittal orientation. The extension of the peritoneum is marked by the grey line

Fig. 3.3. Anatomic draft of the uterine cervix: coronal view and corre- sponding MRI

from Hricak/Carrington (1991)

Isthmus Internal cervical os Uterine vessels Ureter

External cervical os Parametria

Parametria

Internal cervical os Endocervix Corpus uteri

External cervical os

Vaginal cavity

Fig. 3.4. Anatomic draft, which presents the strong relation between uterine arteries and ureters (arrow)

Broad ligament Parametria Round ligament

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3.2

Imaging Findings: Uterine Corpus

The imaging appearance of the uterine corpus var- ies widely with the age and hormonal status of the patients examined [2–7].

On unenhanced CT scans, the layered anatomy of the wall cannot be distinguished. After administra- tion of contrast medium, the myometrium can be distinguished in most cases during the arterial phase as it shows early and strong enhancement while the junctional zone/endometrium is of relatively low

density (Fig. 3.6). As with MRI, the endometrium and junctional zone cannot be differentiated in most cases on the basis of their morphologic appearance on CT. In most cases, venous plexuses can be identi- fi ed within the parametria on the basis of their strong enhancement. However, reliable differentiation of myometrium from parametrial portions is usually not possible while the peripheral fatty portions of the parametrium can be distinguished from the pel- vic wall with an adequate degree of accuracy.

Unenhanced T1-weighted MRI depicts the uterine corpus with a low and homogeneous signal intensity similar to that of skeletal muscle (Fig. 3.7a and b).

Fig. 3.6a-d. CT of the female pelvis. a CT transversal unen- hanced. b CT transversal after CM and reformatted coronal (c) and sagittal CT images (d)

a b

c

d

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Thus, it is not possible to differentiate the individual layers.

On the other hand, T2-weighted MR images in wom- en of reproductive age clearly depict the three layers of the uterine corpus: the endometrium, the junctional zone, and the myometrium (Fig. 3.7c and d) [8].

The endometrium always has a high signal inten- sity on T2-weighted images regardless of the hormonal state and age while its thickness clearly varies in the course of the menstrual cycle [9]. The thickness ranges from 1–3 mm in the early proliferative phase (Fig. 3.7 and 3.8) and 5–10 mm in the middle of the secretory phase (Fig. 3.9 and 3.10). The endometrium is thickest under the effect of estradiol (follicular phase) on days 8 through 16 of the cycle [10]. After day 16, when the effect

of progesterone becomes stronger (luteal phase), there is hardly any further increase in thickness but primarily a transformation of the mucosa with increased forma- tion of glands and ingrowth of vessels. During menstru- ation, a blood clot may occasionally be present in the uterine cavity (Fig. 3.9), which must not be mistaken for a foreign body, polyp, or submucosal myoma.

The layer adjacent to the endometrium that can be distinguished on MRI is the junctional zone, which corresponds to the inner part of the myometrium and is hypointense on T2-weighted images relative to the outer portion of the myometrium. The lower signal is primarily attributable to a lower water content, the higher nucleus-to-cytoplasm ratio, and the smaller ex- tracellular space of the inner myometrium [11, 12].

Fig. 3.7a-d. MRI of a 40-year-old healthy woman during early proliferative phase. T1-weighed TSE images in axial (a) and sagittal orientation (b). T2-weighted TSE images in axial (c) and sagittal (d) plane of the same patient

a

b

c

d

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Similar to the endometrium, the junctional zone also varies over the menstrual cycle and is thickest around the 24th day. The mean thickness of the junctional zone does not exceed 5 mm under normal conditions.

A focal thickness of over 12 mm of the junctional zone can be interpreted as a sign of adenomyosis. However, a focal pathologic thickening of the junctional zone has to be differentiated from uterine contractions.

Uterine contractions may be diagnosed by a repeated

Fig. 3.8a,b. MRI of a healthy woman during early proliferative phase (T2-weighted TSE in axial and sagittal plane)

Fig. 3.9a,b. MRI of a healthy woman during secretory phase.

The T2-weighed TSE image (a) as well as the contrast-en- hanced T1-weighted TSE image (b), both in sagittal orienta- tion demonstrate a blood clot (arrow) in the uterine cavity a

b

a

b

T2-weighted sequence a view minutes later, showing a normal appearance of the former thickened junctional zone in contrast to unchanged appearance of adeno- myosis. By using cine MRI sequences (SSFSE: single- shot half-Fourier fast spin echo) it was furthermore shown that the junctional zone maintains cervicofun- dal contractions that vary with the phase of the cycle [13] and are assumed to have a role in transporting sperm and in maintaining early pregnancy.

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The normal outer myometrium is of an intermediate signal intensity on T2-weighted images. Its signal in- tensity is slightly higher during the secretory phase due to an increased fl uid content, which improves the dif- ferentiation from the junctional zone as compared with other phases of the cycle (comparison of Figs. 3.7 and 3.10). Vessels in the myometrium are also highly prom- inent during this phase of the cycle. Ultrasonography likewise depicts three uterine layers but the thickness of the junctional zone and of the endometrium deter- mined by ultrasound and MRI clearly differ, especially during the luteal phase [14]. This discrepancy is attrib- uted to the fact that ultrasound does not demonstrate the three layers in the same way as MRI [15].

Following intravenous administration of a para- magnetic contrast medium, the zonal anatomy of the uterus is also depicted on T1-weighted images (Fig. 3.9b). Both the endometrium and the outer myometrium are characterized by pronounced con- trast enhancement while the junctional zone is of low signal intensity. This is attributed to the denser tissue and smaller extracellular volume of distribution of the contrast medium [12, 16].

The uterus of newborns still shows good differ- entiation of the myometrium, junctional zone, and endometrium as a result of the effect of maternal es- trogen. Before the onset of menstruation, the endo- metrium is merely seen as a very thin stripe of high signal intensity or not at all and the junctional zone is not distinguishable from the low-signal-intensity myometrium. The corpus is smaller than the cervix during this phase while in adult women the length ratio of the cervix to the corpus is 1:2.

After menopause the uterine corpus as a whole is markedly smaller (Figs. 3.11 and 3.12) with a length ratio of nearly 1:1. On T2-weighted images the endo- metrium is seen as a thin central stripe of high signal intensity. The myometrium has a markedly lower sig- nal intensity as compared with women of reproductive age and is therefore diffi cult to distinguish from the junctional zone, which also has a low signal intensity.

The endometrium decreases in thickness to about 3–5 mm. However, in women on external hormone re- placement therapy, the premenopausal signal pattern and zonal anatomy may be preserved. In this situation the endometrium may be up to 10 mm thick.

Exogenous hormonal replacement may consid- erably alter the MRI appearance of the uterus and vagina. In premenopausal women taking oral con- traceptives, the signal intensity of the myometrium is increased [17]. Moreover, the junctional zone ap- pears thinner and is more diffi cult to differentiate.

Long-term use of oral contraceptives is also associ- ated with marked thinning of the endometrium. In women on GnRH analogues, the uterus is compara- ble to the premenopausal uterus in terms of size and signal intensities with depiction of the endometrium as a very thin stripe of high signal intensity that is clearly delineated from the low-intensity myome- trium. The junctional zone is not seen or very dif- fi cult to distinguish. Despite its anti-estrogen activity,

Fig. 3.10a,b. MRI of a healthy woman during secretory phase (T2-weighted TSE)

b a

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tamoxifen treatment in postmenopausal women has an effect that is comparable to that of oral contracep- tives: There is a clear increase in the thickness of the endometrium. Moreover, the endometrium becomes increasingly heterogenous, which may be misinter- preted as endometrial cancer [18].

3.3

Imaging Findings: Uterine Cervix

In contrast to the uterine corpus, the uterine cervix shows only little variation of its zonal anatomy as depicted by MRI with age, phase of the menstrual cycle, hormone replacement therapy, or use of oral contraceptives.

On CT scans the individual layers of the wall of the cervix cannot be distinguished. The same holds true for unenhanced T1-weighted MR images, which depict the uterine cervix as a homogeneous cylin- der-shaped structure of intermediate signal intensity without distinction of individual layers (Fig. 3.13a,b).

The orientation of the longitudinal axis of the cervix is highly variable.

T2-weighted images depict three layers in most cases: an inner layer of high signal intensity, a fairly wide middle layer of low signal intensity, and an out-

Fig. 3.11. Reformatted sagittal CT image of a 55-year-old wom- an, who underwent MSCT for polyp detection of the colon

Fig. 3.12. T2-weighted MRI of a healthy 58-year-old woman

er layer of intermediate signal intensity (Fig. 3.13c,d).

The inner layer of high signal intensity corresponds to the endocervical mucosa. Sometimes an additional central area of very high signal intensity can be seen, which corresponds to the mucous within the cervical canal (Fig. 3.14).

On high resolution T2-weighted images palmate folds of the cervical canal can be depicted as normal fi ndings (Fig. 3.15).

Often, nabothian cysts are seen. These are benign cysts of the uterine cervix that are assumed to result from obstruction of the cervical mucous glands [19].

The cysts are depicted on T2-weighted images as round to oval lesions with a smooth margin (Fig. 3.16).

The low-signal-intensity middle layer corresponds to the cervical stroma and mostly consists of connec- tive tissue. The outer layer has a signal intensity that is comparable to that of the myometrium and is char- acterized by a more loose tissue structure [20] and may not always be distinguishable from the parame- tria even on T2-weighted images. The mucosa in the cervical canal shows the strongest enhancement and is thus clearly distinct from the less enhancing stro- mal layer. The outer stromal layer of the cervix and the portio also show contrast enhancement.

The differentiation of the cervix versus the para- cervical tissue of the parametria is best on T2- weighted images compared to pre- or postcontrast T1-weighted images or CT scans.

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Fig. 3.13a–d. T1-weighted and T2-weighted images of the cervix uteri of a 36-year-old woman

a b

c d

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Fig. 3.16a,b. Transversal and coronal MR images of a 40-year-old asymptomatic woman depicting Nabothian (cervical) cysts Fig. 3.14a,b. T2-weighted TSE image detect the endocervical

mucosa (white arrow) and cervical stroma (grey arrow) from the outer tissue

Fig. 3.15. MRI presenting palmate folds a

b b

a

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References

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2. Cunha TM, Felix A, Cabral I (2001) Preoperative assess- ment of deep myometrial and cervical invasion in endo- metrial carcinoma: comparison of magnetic resonance imaging and gross visual inspection. Int J Gynecol Cancer 11:130–136

3. Haynor D, Mack L, Soules M et al. (1986) Changing appear- ance of the normal uterus during the menstrual cycle: MR studies. Radiology 161:459–462

4. Hötzinger H, Spätling L (1994) MRI in der Gynäkologie und Geburtshilfe. Springer, Berlin

5. Lee JK, Gersell DJ, Balfe DM, Worthington JL, Picus D (1985) The uterus: in vitro MR anatomic correlation of normal and abnormal specimens. Radiology 157:175–

179

6. Masui, T, Katayama M, Kobayashi S, et al. (2001) Changes in myometrial and junctional zone thickness and signal intensity: demonstration with kinematic T2-weighted MR imaging. Radiology 221:75–85

7. Togashi K, Nakai A, Sugimura K (2001) Anatomy and physi- ology of the female pelvis: MR imaging revisited. J Magn Reson Imaging 13:842–849

8. Bartoli JM, Moulin G, Delannoy L, Chagnaud C, Kasbarian M (1991) The normal uterus on magnetic resonance imag- ing and variations associated with the hormonal state. Surg Radiol Anat 13:213–220

9. Hoad CL, Raine-Fenning NJ, Fulford J, Campbell BK, John- son IR, Gowland PA (2005) Uterine tissue development in healthy women during the normal menstrual cycle and in- vestigations with magnetic resonance imaging. Am J Ob- stet Gynecol 192:648–654

10. Janus CL, Wiczyk HP, Laufer N (1988) Magnetic resonance imaging of the menstrual cycle. Magn Reson Imag 6:669–

674

11. McCarthy, S., G. Scott, S. Majumdar et al. (1989) Uterine junctional zone: MR study of water content and relaxation properties. Radiology 171:241–243

12. Scoutt, LM, Flynn SD, Luthringer DJ, McCauley TR, McCar- thy SM (1991) Junctional zone of the uterus: correlation of MR imaging and histologic examination of hysterectomy specimens. Radiology 179:403–407

13. Masui T, Katayama M, Kobayashi S, Nakayama S, Nozaki A, Kabasawa H, Ito T, Sakahara H (2001) Changes in myo- metrial and junctional zone thickness and signal intensity:

demonstration with kinematic T2-weighted MR imaging.

Radiology 221:75–85

14. Togashi K, Nakai A, Sugimura K (2001) Anatomy and physi- ology of the female pelvis: MR imaging revised. J Magn Res Imag 13:842-849

15. Mitchell DG, Schonholz L, Hilpert PL et al. (1990) Zones of the uterus: Discrepancy between US and MR images.

Radiology 174:827–831

16. Brown HK, Stoll BS, Nicosia SV et al. (1991) Uterine junc- tional zone: correlation between histologic fi ndings and MR imaging. Radiology 179:409–413

17. McCarthy S, Tauber C, Gore J (1986) Female pelvic anatomy:

MR assessment of variations during the menstrual cycle and with use of oral contraceptives. Radiology 160:119–123 18. Ascher SM, Johnson JC, Barnes WA, Bae CJ, Patt RH, Zeman

RK (1996) MR imaging appearance of the uterus in post- menopausal women receiving tamoxifen therapy for breast cancer: histopathologic correlation. Radiology 200:105–110 19. Li, H., Sugimura K, Okizuka H et al. (1999) Markedly high

signal intensity lesions in the uterine cervix on T2-weight- ed imaging: differentiation between mucin-producing car- cinomas and nabothian cysts. Radiat Med 17:137-143de 20. Souza NM, Hawley IC, Schwieso JE, Gilderdale DJ, Soutter

WP (1994) The uterine cervix on in vitro and in vivo MR images: a study of zonal anatomy and vascularity using an enveloping cervical coil. AJR Am J Roentgenol 163:607–

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