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MR Imaging of the Uterine Cervix: Imaging-Pathologic Correlation1 CME FEATURE See accompanying test at http:// www.rsna.org /education /rg_cme.html

LEARNING OBJECTIVES FOR TEST 4 After reading this article and taking the test, the reader will be able to: 䡲 List the various types of diseases that affect the uterine cervix. 䡲 Recognize the MR imaging characteristics of common diseases of the uterine cervix. 䡲 Describe the correlations between these MR imaging findings and the histopathologic findings.

Yoshikazu Okamoto, MD ● Yumiko O. Tanaka, MD ● Masato Nishida, MD Hajime Tsunoda, MD ● Hiroyuki Yoshikawa, MD ● Yuji Itai, MD Magnetic resonance (MR) imaging is useful not only for preoperative staging of gynecologic malignancies but also for prediction of the histopathologic features of a variety of intrapelvic tumors. Familiarity with the specific imaging findings that have been reported for the uterine cervix is a goal of radiologists. The typical MR imaging findings of uterine cervical lesions correspond to the histopathologic features. These lesions can be categorized as epithelial neoplasms, nonepithelial neoplasms, and nonneoplastic diseases. Cervical carcinoma accounts for most cases of malignant lesions and is staged by using the classification system established by the International Federation of Gynecology and Obstetrics. MR imaging allows differentiation between endophytic and exophytic growth and between normal and abnormal findings after hysterectomy and irradiation. Other epithelial neoplasms of the uterine cervix include adenoma malignum, which is a special type of cervical adenocarcinoma, as well as carcinoid tumor and malignant melanoma. Nonepithelial neoplasms of the uterine cervix include malignant lymphoma and leiomyoma. Nonneoplastic diseases of the uterine cervix include cervical pregnancy, cervicitis, nabothian cysts, polyps, and endometriosis. ©

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Abbreviation: SCJ ⫽ squamocolumnar junction Index terms: Endometriosis, 854.3192 ● Pregnancy, ectopic, 854.8234 ● Uterine neoplasms, diagnosis, 854.30 ● Uterus, cysts, 854.311 ● Uterus, diseases, 854.2179 RadioGraphics 2003; 23:425– 445 ● Published online 10.1148/rg.232025065 1From

the Department of Radiology, Tsukuba University Hospital, 2-1-1 Amakubo, Tsukuba, Ibaraki 305-8576, Japan (Y.O.); the Departments of Radiology (Y.O.T., Y.I.) and Obstetrics and Gynecology (H.T., H.Y.), Institute of Clinical Medicine, University of Tsukuba; and the Department of Obstetrics and Gynecology, National Kasumigaura Hospital, Tsuchiura, Japan (M.N.). Recipient of a Cum Laude award for an education exhibit at the 2001 RSNA scientific assembly. Received March 25, 2002; revision requested April 30 and received June 13; accepted June 14. Address correspondence to Y.O. (e-mail: [email protected]).

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Introduction Uterine cervical cancer is one of the most common malignancies seen by gynecologic radiologists. However, many other kinds of diseases can affect the uterine cervix, including tumors, inflammation, and even ectopic pregnancy. This article presents the various kinds of uterine cervical lesions with typical magnetic resonance (MR) imaging findings for each. These lesions are divided into three categories: epithelial neoplasms, nonepithelial neoplasms, and nonneoplastic diseases.

Anatomy The uterine cervix is composed of the portio, which protrudes into the vagina, and the supravaginal part of the cervix. Squamous cells cover the epithelial surface of the portio continuing from the vagina. With age, they grow back to cover the columnar cells of the endocervical gland. This transitional area is called the squamocolumnar junction (SCJ) (Fig 1). Carcinoma of the cervix develops almost exclusively within the transformation zone that extends between the original SCJ and the physiologic SCJ (Fig 1).

Epithelial Neoplasms Cervical Cancer In the Japanese population, uterine cervical cancer is the most common malignancy affecting the female genital tract. About 90% of cervical carcinomas in Japan are squamous cell carcinoma, although about 5%–10% are adenocarcinoma and others are rare histologic subtypes (1). In the United States, 15,700 new cases of invasive cervical cancer and approximately 4,900 deaths were anticipated in 1996 (2). Recently, the prevalence of adenocarcinoma has been increasing. We assume that the prevalence of cervical cancer has been decreasing in Japan recently because a cytologic screening program has been widely applied in Japan in the past 20 years. Because it is easy to find abnormal squamous cells by using a Papanicolaou smear, the prevalence of invasive squamous cell carcinoma has decreased. Conversely, the prevalence of cervical adenocarcinoma has not been changed by the Papanicolaou smear. Therefore, the relative percentage of adenocarcinoma is increasing.

Figure 1. Drawing of the uterus and vagina. The cervix consists of two different types of epithelium: squamous epithelium and glandular epithelium. Squamous cells cover the epithelial surface of the portio continuing from the vagina, and columnar cells cover the glandular epithelium of the endocervical gland, which produces mucin. With age, squamous cells grow back to cover the columnar cells. This transitional area is the SCJ (arrow).

Most cervical squamous cell carcinomas grow at the SCJ. In younger women, the SCJ is located outside the external uterine os, and the tumor tends to grow outward (exophytic growth pattern) (Fig 2). In contrast, in elderly patients, the SCJ is located within the cervical canal. In these patients, cervical cancer tends to grow inward along the cervical canal (endophytic growth pattern) (Fig 3). Reserve cells at the SCJ have been watched with interest as an origin site of cervical adenocarcinoma. Therefore, most cervical adenocarcinomas would also arise in the SCJ. MR imaging can provide highly accurate information on the exact extent of tumors because of its fine contrast resolution. Cervical cancers appear as hyperintense masses on T2-weighted images regardless of histopathologic type. The usefulness of dynamic contrast material– enhanced studies in diagnosing parametrial invasion and predicting radiosensitivity has been reported (3–5), although sagittal T1-weighted and T2weighted images and oblique axial T2-weighted images obtained perpendicular to the uterine axis are sufficient for staging in most cases (6). MR urography and computed tomography (CT) are also indicated in diagnosing hydronephrosis associated with cancer invasion, paraaortic lymph node metastases, or other distant metastases.

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Figure 2. Cervical carcinoma with exophytic growth in a 44-year-old woman. The pathologic stage was Ib-1. (a) Sagittal T2-weighted MR image shows a slightly hyperintense, cauliflower-like tumor in the posterior lip of the portio (arrows). The tumor markedly expands the posterior vaginal fornix. (b) Photograph of the cut surface of the resected specimen shows a white mass that expands into the fornix (arrows). (c) Photomicrograph (original magnification, ⫻10; hematoxylin-eosin stain) shows that the tumor is composed of atypical squamous epithelium with cancer “pearls” (arrowheads).

Figure 3. Cervical carcinoma with endophytic growth in a 59-year-old woman. The preoperative imaging diagnosis was stage IIb carcinoma. Sagittal T2-weighted MR image shows a slightly hyperintense mass that replaces the cervix (white arrows). The lesion is located almost within the cervical canal. The patient also has a mature cystic teratoma of the right ovary, which is seen as a cystic mass (black arrow) behind the uterus.

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Classification for Staging of Cervical Carcinoma and MR Imaging Findings FIGO* Stage Ia Ia-1 Ia-2

Ib Ib-1 Ib-2 IIa

IIb

IIIa IIIb

Definition

MR Imaging Findings

Microinvasive disease Stromal invasion no greater than 3.0 mm in depth and 7.0 mm or less in horizontal spread Stromal invasion more than 3.0 mm but not more than 5.0 mm in depth with a horizontal spread of 7.0 mm or less Clinically invasive disease A clinically visible lesion 4.0 cm or less in greatest dimension A clinically visible lesion more than 4.0 cm in greatest dimension The tumor invades beyond the uterus, but not to the lower one-third of the vagina, without parametrial invasion The tumor invades beyond the uterus with parametrial invasion but not to the pelvic wall

}

Vaginal involvement reaches the lower one-third of the vaginal canal without extending to the pelvic wall The tumor extends to the pelvic wall or causes hydronephrosis or a nonfunctioning kidney

IVa

The tumor invades the mucosa of the bladder or rectum or extends beyond the true pelvis

IVb

Distant metastasis

No evidence of a mass lesion

Definitive finding: a tumor completely surrounded by the hypointense stromal ring Suggestive finding: a sharply marginated tumor confined within the hypointense stromal ring Segmental disruption of the hypointense vaginal wall, but it never reaches the lower onethird of the vagina Triangular protrusion of the tumor through a disrupted hypointense ring of the cervical stroma Same finding as for stage IIa in the lower onethird of the vagina Same finding as for stage IIb with obliteration of the entire cardinal ligament directly extending to pelvic muscles or with hydroureter Segmental disruption of the hypointense bladder or rectal wall or a segmental thickened rectal wall Evidence of mass lesions in distant organs

*FIGO ⫽ International Federation of Gynecology and Obstetrics.

In general, staging of cervical carcinoma with MR imaging is based on the classification system of the International Federation of Gynecology and Obstetrics (FIGO) (7) (Table). Thus, stage Ia is defined as a microinvasive tumor that cannot be demonstrated at MR imaging. Stage Ib is defined as a clinically invasive tumor, although it is

confined to the cervix and does not invade the vagina or parametrium. In stage Ib, the tumor is completely surrounded by hypointense cervical stroma on axial T2-weighted images (8 –10) (Fig 4). Stage IIa is defined as a tumor that invades the upper two-thirds of the vagina without parametrial invasion. Segmental disruption of the hy-

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Figure 4. Stage Ib cervical carcinoma. Sagittal (a) and axial (b) T2-weighted MR images show a slightly hyperintense mass in the uterine cervix. The mass protrudes into the posterior vaginal fornix; however, the vaginal mucosa attached to the tumor is intact (arrows in a). The tumor is completely surrounded by hypointense cervical stroma on the axial image (arrowheads in b).

Figure 5. Stage IIa cervical carcinoma. Sagittal (a) and axial (b) T2-weighted MR images show a slightly hyperintense mass that protrudes into the vaginal canal (arrow in a). Most of the vaginal wall surrounding the tumor seems intact (white arrows in b), although the low signal intensity of the vaginal wall is disrupted on the right side (black arrow in b). Parametrial invasion is not seen.

pointense vaginal wall is demonstrated on T2weighted images (8 –10) (Fig 5). When the tumor invades beyond the uterus with parametrial invasion without reaching the pelvic wall, it is defined

as stage IIb. At MR imaging, triangular protrusion of the tumor through the disrupted hypointense ring of cervical stroma is seen (8 –10) (Fig 6).

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Figure 6. Stage IIb cervical carcinoma. Sagittal (a) and axial (b) T2-weighted MR images show that the cervix is almost entirely replaced by a slightly hyperintense mass. The tumor protrudes into the parametrium bilaterally (arrowheads in b); however, it does not reach the pelvic wall. Hydrometra, which is caused by the obstructed internal cervical os, is also noted (arrow in a).

Figure 7. Stage IIIa cervical carcinoma. (a) Sagittal T2-weighted MR image shows a slightly hyperintense, exophytic, solid mass that extends along the anterior vaginal wall and reaches the lower one-third of the vagina (arrow). (b) Axial T2-weighted MR image shows that the low signal intensity of the anterior vaginal wall is partly disrupted (arrowheads) and the fatty tissue between the mass and the posterior bladder wall has disappeared. However, the mass does not infiltrate the vesical mucosa.

In stage IIIa, vaginal involvement reaches the lower third of the vaginal canal without extending to the pelvic wall. Occasionally, the anterior vaginal wall is partly disrupted and the tumor infiltrates the bladder wall but not the vesical mucosa (Fig 7). When the tumor extends to the pelvic wall or causes hydronephrosis, it is defined as stage IIIb. At MR imaging, the tumor obliterates

the entire cardinal ligament and extends to the pelvic muscles. Hydronephrosis caused by tumor invasion of the ureter is also classified as stage IIIb. MR urography can clearly demonstrate hydronephrosis caused by tumor extension (Fig 8). If the tumor invades the vesical or rectal mucosa, it is classified as stage IVa. Segmental disruption of the hypointense vesical or rectal wall or a segmental thickened rectal wall is seen at MR imaging (8 –10) (Fig 9). Once any distant metastases occur, the stage is defined as IVb. Although

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Figure 8. Stage IIIb cervical carcinoma. (a) Sagittal T2-weighted MR image shows a slightly hyperintense, large, solid mass that extends from the uterine cervix to the lower part of the uterine body. It also extends to the lower one-third of the anterior vaginal wall (arrow). (b) Axial T2-weighted MR image shows that the tumor also reaches the left posterior wall of the bladder, although the thinned vesical muscular layer remains (arrowheads). (c) MR urogram clearly shows left hydronephrosis caused by tumor invasion.

Figure 9. Stage IVa cervical carcinoma. Sagittal T2-weighted MR image shows a hypointense mass that occupies the uterine cervix and invades the vaginal wall anteriorly. At the level of the vaginal extension, the tumor reaches the mucosa of the posterior vesical wall (arrows).

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Figure 10. Stage IVb cervical carcinoma. (a) Sagittal T2-weighted MR image shows a large mass in the uterine cervix. (b, c) CT scans show metastases of paraaortic lymph nodes (arrows in b) and hematogenous hepatic metastases (c). These findings are classified as stage IVb disease (Table).

pelvic lymph node metastases do not change the International Federation of Gynecology and Obstetrics stage, paraaortic or inguinal lymph node metastases are classified as stage IVb. Cervical cancer occasionally causes carcinomatous lymphangitis of the lung or hematogenous hepatic metastases. CT plays a major role in diagnosing such advanced disease (Fig 10).

MR imaging is also useful for evaluation of the postoperative state (11). Conization is usually performed as a radical surgery for carcinoma in situ or microinvasive carcinomas or as a diagnostic procedure in cases suspected to be invasive cervical carcinoma. After conization, the portio seems smaller than usual (Fig 11). Otherwise, abdominal radical hysterectomy is a standard surgery for stage Ib and IIa disease (Fig 12). Diagnosis of local recurrence after surgery or radiation therapy can also be achieved with MR imaging (Figs 13, 14).

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Figure 11. Morphologic changes in the uterus after conization. Sagittal T2-weighted MR image obtained after conization shows a defect in the portio (arrows).

Figure 12. Appearance of the pelvis after radical hysterectomy. (a) Sagittal T2-weighted MR image shows that the uterus has disappeared (arrows). (b) Axial T2-weighted MR image shows a small amount of hypointense, bandlike soft tissue at the vaginal stump (arrows).

Figure 13. Local recurrence after radiation therapy. (a) Sagittal T2-weighted MR image shows a large, hypointense mass that occupies the uterine cervix and the lower part of the uterine body (arrowheads). (b) Sagittal T2weighted MR image obtained 2 months after radiation therapy shows marked regression of the tumor (arrowheads). (c) Sagittal T2-weighted MR image obtained 14 months after radiation therapy shows a slightly hyperintense area in the uterine body (arrowheads). Histologic analysis proved that this area represented a recurrence.

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Figure 14. Local recurrence after hysterectomy. (a) Sagittal T2-weighted MR image shows a cervical carcinoma (arrow). (b, c) Sagittal (b) and axial (c) T2weighted MR images obtained 6 months after radical hysterectomy show a hyperintense mass along the anterior vaginal wall (arrows). Biopsy demonstrated that the mass was a local recurrence.

Adenoma Malignum Adenoma malignum (also known as minimal deviation adenocarcinoma) is a special subtype of mucinous adenocarcinoma of the cervix. Its prevalence is about 3% of all cervical adenocarcinomas (12). The most common initial symptom is a watery discharge. The prognosis of this tumor has been reported to be unfavorable (13), as it disseminates into the peritoneal cavity even in the early stage of the disease and its response to radiation or chemotherapy is poor. Therefore, its deceptively benign histologic appearance occasionally leads to an incorrect diagnosis. At histopathologic analysis, the tumor is composed of well-differentiated endocervical glands that extend from the surface to the deeper portion of the cervical wall. They form an annular or nodular mass, with cystic spaces filled with mucin (12,14) (Fig 15). At MR imaging, adenoma malignum is characterized by multicystic lesions that extend from the endocervical glands to the deep cervical stroma

with solid components (15,16) (Fig 15). The differential diagnosis includes deep nabothian cysts, florid endocervical hyperplasia, and even welldifferentiated adenocarcinoma, because any cervical glandular proliferation can show multicystic features within the deep cervical stroma (15–17). The possibility of differentiating these lesions from adenoma malignum with MR imaging is controversial. It has been reported that a multicystic lesion with some solid components in the deep cervical stroma is evidence of adenoma malignum at MR imaging, although some benign cystic lesions that affect the cervix also appear multicystic with solid features (16 –20) (Fig 16). Adenoma malignum is often associated with Peutz-Jeghers syndrome, which is characterized by mucocutaneous pigmentation and multiple hamartomatous polyps of the intestinal tract (21– 23) (Fig 17), as well as mucinous tumors of the ovary (24).

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Figure 15. Adenoma malignum. (a) Sagittal T2-weighted MR image shows a multicystic lesion with a solid component in the deep cervical stroma (arrowhead). (b) Sagittal MR image obtained after administration of a gadolinium-based contrast agent shows obvious enhancement of the solid component of the lesion (arrows). (c) Photomicrograph (original magnification, ⫻10; hematoxylin-eosin stain) shows that the endocervical glands in the upper row have no atypia. However, those in the lower row have larger nuclei located at the center of the cells, an appearance indicative of cellular atypia.

Figure 16. Endocervical hyperplasia. (a) Sagittal T2-weighted MR image shows a multicystic mass surrounding the cervical canal (arrows). An area that is hyperintense relative to the normal cervical stroma near the cysts is also noted. (b) Sagittal MR image obtained after administration of gadolinium-based contrast material shows intense enhancement of the relatively hyperintense area near the cysts on the T2-weighted image (arrows). (c) Photomicrograph (original magnification, ⫻4; hematoxylin-eosin stain) shows that the tumor is composed of normal endocervical glands without malignant features.

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Figure 17. Adenoma malignum in a patient with Peutz-Jeghers syndrome. (a, b) Photographs show mucocutaneous pigmentation of the lips (a) and digits (b). (c, d) Images from a double-contrast barium study show multiple polyps (arrowhead) in the colon (c) and stomach (d). (e) Sagittal T2weighted MR image obtained during pregnancy shows a characteristic multicystic mass in the uterine cervix (arrows). (Case courtesy of Takeshi Nihei, MD, Mito Saiseikai General Hospital, Mito, Japan.)

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Figure 18. Atypical carcinoid tumor of the uterine cervix. (a, b) Sagittal (a) and axial (b) T2-weighted MR images show a hyperintense solid mass that dilates the upper end of the vaginal tube. (c) Axial gadolinium-enhanced T1-weighted MR image shows marked homogeneous enhancement of the tumor (arrows). (d) Photomicrograph (original magnification, ⫻10; hematoxylin-eosin stain) shows diffuse infiltration of small tumor cells. (e) Photomicrograph (original magnification, ⫻10; chromogranin A immunohistochemical stain) shows that the tumor is of neuroendocrine origin. The final diagnosis was atypical carcinoid tumor of the uterine cervix. (Case courtesy of Yuki Satoh, MD, Tsukuba Memorial Hospital, Tsukuba, Japan.)

Neuroendocrine Tumors Another histologic type of epithelial carcinoma of the uterine cervix in addition to squamous cell carcinoma or adenocarcinoma is classified by the World Health Organization as small cell carcinoma. It is similar to pulmonary small cell carcinoma and contains neuroendocrine granules (25). Carcinoid is a rare neuroendocrine tumor arising in the uterine cervix. Albores-Saavedra et al (26) reported that only 12 of 3,507 malignant cervical tumors (0.34%) could be diagnosed as carcinoid with Grimelius staining. Most cases show nonspecific symptoms indistinguishable

from those of squamous cell carcinoma, because carcinoid syndrome is rare in patients with uterine carcinoid (27). Because neuroendocrine tumors of the uterine cervix are very aggressive, early diagnosis and subsequent treatment are warranted (28). MR imaging findings of uterine carcinoid have not been reported, to our knowledge. We have studied a single case of uterine cervical carcinoid with MR imaging (Fig 18). The tumor showed slightly heterogeneous high signal intensity on

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Figure 19. Malignant melanoma of the vagina with direct invasion of the cervix. (a) Sagittal T2-weighted MR image shows a hypointense tumor that involves the uterine cervix and vagina. (b) Sagittal T1-weighted MR image shows characteristic high signal intensity of the tumor (arrowheads). (c) Photograph shows that the tumor is black and occupies the vagina and cervix. (d) Photomicrograph (original magnification, ⫻10; hematoxylin-eosin stain) shows that the tumor is composed of melanocytes with rich melanin granules.

T2-weighted images and was well enhanced with gadolinium-based contrast material. As these findings are not particularly different from those of squamous cell carcinoma, it could not be differentiated from other types of cervical carcinoma.

Malignant Melanoma Malignant melanoma of the female genital tract accounts for 1%–5% of all melanoma cases (29). It usually occurs in the vaginal mucosa and occasionally involves the uterine cervix. Malignant melanoma arising in the uterine cervix is extremely rare, with only about 30 cases reported in the literature (30). MR imaging characteristics have been reported in other organs and consist of high signal intensity

on both T1-weighted and T2-weighted images (31). T1 shortening is attributed to either the paramagnetic effects of stable free radicals within melanin granules or the methemoglobin within the intratumoral hemorrhage. However, malignant melanoma may have different signal intensity characteristics according to the melanin concentration and the presence of hemorrhage (32,33). Only two reports of MR imaging findings of malignant melanoma of the cervix or vagina have been published, to our knowledge (34,35). In one report, both of the two vaginal melanomas analyzed showed high signal intensity on T1weighted images, as expected. Malignant melanoma with rich melanocytes is expected to be hyperintense on T1-weighted images; this might be a suggestive finding for melanoma. However, such tumors can be diagnosed easily, even by visual inspection, because of their characteristic black color (Fig 19).

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Figure 20. Malignant lymphoma of the uterine cervix. (a) Sagittal T2-weighted MR image shows a hyperintense lobulated tumor that involves the anterior wall of the uterine cervix (arrows). Although the mass is very large, the cervical epithelium remains as a hyperintense band behind the tumor (arrowheads). (b) Sagittal T1-weighted MR image shows that the tumor has low signal intensity (arrows). (c) Sagittal contrast-enhanced MR image shows that the tumor enhances heterogeneously (arrows). (d) Photograph of the surgical specimen shows a preserved cervical canal (arrowheads). (e) Photomicrograph (original magnification, ⫻4; hematoxylin-eosin stain) shows small tumor cells with large nuclei that proliferate diffusely.

Nonepithelial Neoplasms Malignant Lymphoma Malignant lymphoma frequently infiltrates the uterus in advanced disease. However, it rarely involves the uterine cervix as the initial manifestation (36). Its frequency in Western countries was reported to be 0.008% of primary cervical tumors and 2% of extranodal lymphomas in women (37). The common presenting symptoms are vaginal bleeding, perineal discomfort, and vaginal discharge (38). Cervical lymphomas are treated with chemotherapy alone or in combination with irradiation or surgery. Uterine involvement by lymphoma is usually observed in the cervix, although there are some case reports in which the tumor mainly affected the uterine body. Lymphoma of the uterus exhibits various appearances at MR imaging, although the tumor tends to be hypointense on T1-weighted images and relatively hyperintense on T2-weighted images (39 – 42). MR imaging findings of uterine

cervical lymphoma closely resemble those of carcinoma of the cervix (39). However, preserved cervical epithelium in the presence of extensive involvement of the cervical stroma may be a clue to the diagnosis of malignant lymphoma (Fig 20). Diffuse enlargement of the uterus without disruption of the endometrial epithelium is also reported to be a characteristic finding for lymphoma involving the uterine body (39).

Cervical Leiomyoma As about 90% of uterine leiomyomas occur in the uterine body, cervical leiomyoma is relatively rare. Its prevalence is reported to be less than 10% of all leiomyomas of the uterus (43). Clinical symptoms of cervical leiomyomas, including hypermenorrhea, dysmenorrhea, or abdominal distention, are identical to those of leiomyomas in the uterine body. They occasionally form polypoid tumors and protrude into the cervical canal

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Figure 21. Cervical leiomyoma. (a) Sagittal T2-weighted MR image shows a hypointense solid mass that arises from the posterior wall of the uterine cervix (arrows). Hyperintense areas suggestive of degeneration or hypercellularity are also noted. (b) Sagittal T1-weighted MR image shows tumoral flow voids (arrowheads). (c) Photograph shows the tumor (arrows), which was resected separately from the uterus. (d) Photomicrograph (original magnification, ⫻4; hematoxylin-eosin stain) shows spindle-shaped tumor cells proliferating with some direction. The presence of mitotic figures resulted in the diagnosis of cellular leiomyoma.

or even the vagina when they grow in the submucosal region. Because they are located along the birth canal, they occasionally cause maternal dystocia. Typical leiomyomas of the uterus appear as distinct hypointense masses on T2-weighted images and are homogeneously enhanced. As they are usually hypervascular, flow voids are often observed around them (44). However, various kinds of degeneration are common in uterine leiomyomas (43– 45). Hyaline degeneration is demonstrated as low signal intensity on T2weighted images and lack of enhancement (45– 47). Conversely, leiomyomas with interstitial edema have slightly high signal intensity and intense enhancement (45– 47). Cystic degeneration, which is an advanced stage of intratumoral

edema, also shows high signal intensity on T2weighted images and does not enhance (45– 47). Marked high signal intensity with gradual enhancement suggests myxoid degeneration (45– 47). Characteristic high signal intensity on T1weighted images suggests red degeneration, which is caused by venous thrombosis (48). Most red degeneration of leiomyomas occurs during pregnancy. Lipoleiomyoma is another rare condition that shows high signal intensity on T1-weighted images. The fat suppression technique is very useful in distinguishing fat from blood clot within the tumor (49). Cellular leiomyoma is another special subtype of leiomyoma. Typically, it shows high signal intensity on T2-weighted images, reflecting high cellularity and relatively less fibrous stroma (Fig 21). Rapid and strong enhancement of this tumor on dynamic contrast-enhanced images has also been reported (50). Because of its higher cel-

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Figure 22. Cervical pregnancy. (a) Sagittal T2-weighted MR image shows a hypointense large mass that occupies the enlarged uterine cervix (arrows). (b) Sagittal T1-weighted MR image shows that the mass is partially hyperintense (arrowhead). (c) Sagittal contrast-enhanced MR image shows that the mass does not enhance. (d) Photomicrograph (original magnification, ⫻4; hematoxylin-eosin stain) of a specimen obtained with dilation and curettage shows chorionic villi. Thus, the clinical diagnosis was cervical pregnancy.

lularity, distinguishing a cellular leiomyoma from a leiomyosarcoma is occasionally difficult with MR imaging or even with microscopy.

Nonneoplastic Diseases Cervical Pregnancy The prevalence of cervical pregnancy ranges from 1 in 1,000 to 1 in 24,000 of all pregnancies (51). Recently, the occurrence has been increasing, possibly due to the increased number of induced abortions (51). The exact cause is still unknown. Reported risk factors include multiparity, prior surgical manipulation of the cervix or endometrial cavity, cervical or uterine leiomyomas, atrophic endometrium, and septate uterus (51,52). The major symptom is painless vaginal bleeding following a period of amenorrhea (51). Physical examination usually reveals a soft, enlarged,

hyperemic cervix that contains a partially open external os (51,53). Jung and colleagues (54) reported that cervical pregnancy was characterized by a mass with heterogeneous signal intensity and a partial or complete dark rim on T2-weighted images. Because the mass is composed of chorionic villi and decidua complicated with hematoma, the enhancing volume within the mass varies (Fig 22).

Uterine Cervicitis The cervix is made up of two different types of epithelium: squamous epithelium and glandular epithelium. The cause of cervical inflammation depends on the affected epithelium. The same microorganisms as those that cause vaginitis can affect the endocervical squamous epithelium. Trichomonas vaginalis, Candida albicans, and herpes simplex virus can cause inflammation of the ectocervix. Conversely, Neisseria gonorrhoeae and Chlamydia trachomatis infect only the glandular

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Figure 23. Uterine cervicitis. (a) Sagittal T2weighted MR image shows some cystic lesions along the cervical canal (arrowheads). In addition, multiple leiomyomas are seen in the uterine body (arrows). (b) Sagittal contrast-enhanced MR image shows no enhancement within or around the cysts. (c) Photomicrograph (original magnification, ⫻10; hematoxylin-eosin stain) shows many small round cells infiltrating the cervical glands and ductal dilatation.

epithelium and are major causes of mucopurulent endocervicitis (55). Symptoms of acute cervicitis are a tenacious, jelly-like, yellow, or turbid discharge and a sensation of pelvic pressure or discomfort. When the inflammatory process is confined to the cervix, generalized symptoms are not evident. Occasionally, MR imaging demonstrates these lesions as retention cysts in the cervix (Fig 23). Therefore, it is sometimes difficult to distinguish this disease from glandular hyperplasia or adenoma malignum, especially when the patient has no symptoms that suggest infectious disease (15,17).

Nabothian Cyst Nabothian cysts are common retention cysts of the uterine cervix. They are formed as a result of the healing process of chronic cervicitis (56,57). During chronic inflammation, the squamous epithelium proliferates, covering the columnar epithelium of the endocervical glands. After that, the mucus secreted by the columnar epithelium (now

covered by the squamous epithelium) cannot be evacuated and forms a retention cyst (56,57). Nabothian cysts are usually a few millimeters in diameter but may reach 4 cm or more on occasion (56 –58). These cysts can be easily diagnosed clinically by visual inspection. However, extensive cyst formation or large cysts located deeper in the cervical stroma can cause unexplained enlargement of the cervix. Tunnel cluster, a special type of nabothian cyst, is characterized by complex multicystic dilatation of the endocervical glands (59). Although its macroscopic appearance is similar to that of adenoma malignum, epithelial cells of the tunnel cluster do not show any atypia, as in nabothian cysts. Nabothian cysts are often seen as incidental findings at MR imaging (60). Cysts exhibit intermediate or slightly high signal intensity on T1weighted images and have prominent high signal intensity on T2-weighted images (60). A solid

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Figure 24. Nabothian cysts. (a) Sagittal T2weighted MR image shows multiple small cysts in the deep stroma of the anterior cervix (arrows). (b) Sagittal T1-weighted MR image shows that the lesions have slightly high signal intensity (arrows).

Figure 25. Cervical polyp. (a) Sagittal T2-weighted MR image shows a large multicystic mass filling the endocervical canal (arrows). (b) Sagittal T1-weighted MR image shows hypointense fluid filling the cysts (arrows). At histologic analysis, the lesion was proved to represent cystically dilated endometrial glands and was diagnosed as a cystic polyp.

component surrounding or separating multiple cysts is considered a clue in distinguishing adenoma malignum from benign lesions such as nabothian cysts (Fig 24). However, exact differentiation is occasionally difficult, as the MR imaging findings of both diseases overlap (15–17,20).

Cervical Polyps Cervical polyps are one of the most common causes of intermenstrual vaginal bleeding. Most patients are perimenopausal, especially in the 5th decade of life (61). The polyps are usually pedunculated, with a slender pedicle of varying length, but some are sessile (62). Histologically, cervical polypoid lesions include various kinds of pathologic conditions: endocervical or endometrial tissue with metaplasia, inflammation or malignancy, leiomyoma, or even blood clot (61). Endocervical polyps are the most

common, accounting for more than 60% of cervical polypoid lesions (61). Only about 40% are symptomatic. The presenting symptoms include menorrhagia, postmenopausal bleeding, contact bleeding, and vaginal discharge (61). The diagnosis is made primarily with hysteroscopy. Endocervical polyps are usually demonstrated as masses with or without cysts filling the endocervical or vaginal canal (Fig 25).

Endometriosis Endometriosis is a common disease that affects the uterine body. Endometriosis seldom affects the uterine cervix. Internal endometriosis is called adenomyosis; in this condition, lesions form an ill-defined hypointense area continuing to the

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junctional zone with some hyperintense dots on T2-weighted images. However, adenomyosis can form a uterus-like polypoid mass growing into the endocervical canal (63). It has a cavity surrounded by endometrial mucosa and smooth muscle layers resembling myometrium.

Conclusions MR imaging is an essential modality for diagnosing cervical lesions because the signal intensity or configuration of the lesion demonstrated on MR images reflects the pathologic findings. Although sagittal T1-weighted and T2-weighted images and oblique axial T2-weighted images perpendicular to the uterine axis are sufficient for staging cervical carcinoma in most cases, only a detailed reading based on the pelvic anatomy and the pathologic features of the tumor can allow an accurate staging diagnosis. However, some tumors or tumorlike lesions can show similar MR imaging findings, such as adenocarcinoma, adenoma malignum, and florid endocervical hyperplasia. Therefore, a diagnosis should be made based on clinical manifestations in conjunction with imaging findings.

References 1. Japan Society of Obstetrics and Gynecology. The annual report of gynecologic tumors in 1998. Acta Obstet Gynaecol Jpn 2001; 53:999 –1053. [Japanese] 2. Parker SL, Tong T, Bolden S, Wingo PA. Cancer statistics, 1996. CA Cancer J Clin 1996; 46:5–28. 3. Yamashita Y, Takahashi M, Sawada T, Miyazaki K, Okamura H. Carcinoma of the cervix: dynamic MR imaging. Radiology 1992; 182:643– 648. 4. Feldmann HJ, Sievers K, Fuller J, Molls M, Lohr E. Evaluation of tumor blood perfusion by dynamic MRI and CT in patients undergoing thermoradiotherapy. Eur J Radiol 1993; 16:224 –229. 5. Hawighorst H, Knapstein PG, Weikel W, et al. Angiogenesis of uterine cervical carcinoma: characterization by pharmacokinetic magnetic resonance parameters and histological microvessel density with correlation to lymphatic involvement. Cancer Res 1997; 57:4777– 4786. 6. Shiraiwa M, Joja I, Asakawa T, et al. Cervical carcinoma: efficacy of thin-section oblique axial T2weighted images for evaluating parametrial invasion. Abdom Imaging 1999; 24:514 –519. 7. Benedet JL, Bender H, Jones H III, Ngan HYS, Pecorelli S. FIGO staging classifications and clinical practice guidelines in the management of gynecologic cancers. Int J Gynecol Obstet 2000; 70: 209 –262. 8. Sironi S, Belloni C, Taccagni GL, et al. Carcinoma of the cervix: value of MR imaging in detecting parametrial involvement. AJR Am J Roentgenol 1991; 156:753–756.

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9. Togashi K, Nishimura K, Sagoh T, et al. Carcinoma of the cervix: staging with MR imaging. Radiology 1989; 171:245–251. 10. Togashi K, Morikawa K, Kataoka ML, Konishi J. Cervical cancer. J Magn Reson Imaging 1998; 8:391–397. 11. Togashi K. Carcinoma of the cervix. In: MRI of the female pelvis. Tokyo, Japan: Igaku-Shoin, 1993; 123–156. 12. Kaminski PF, Norris HJ. Minimal deviation carcinoma (adenoma malignum) of the cervix. Int J Gynecol Pathol 1983; 2:141–152. 13. Fu YS, Reagan JW, Hsiu JG, Storaalsi JP, Wentz WB. Adenocarcinoma and mixed carcinoma of the uterine cervix. Cancer 1982; 49:2560 –2570. 14. Silverberg SG, Hurt WG. Minimal deviation adenocarcinoma (“adenoma malignum”) of the cervix: a reappraisal. Am J Obstet Gynecol 1975; 121:971–975. 15. Yamashita Y, Takahashi M, Katabuchi H, Fukumatsu Y, Miyazaki K, Okamura H. Adenoma malignum: MR appearances mimicking nabothian cysts. AJR Am J Roentgenol 1994; 162:649 – 650. 16. Doi T, Yamashita Y, Yasunaga T, et al. Adenoma malignum: MR imaging and pathologic study. Radiology 1997; 204:39 – 42. 17. Mikami Y, Hata S, Fujiwara K, Imajo Y, Kohno I, Manabe T. Florid endocervical glandular hyperplasia with intestinal and pyloric gland metaplasia: worrisome benign mimic of “adenoma malignum.” Gynecol Oncol 1999; 74:504 –511. 18. Itoh K, Toki T, Shiohara S, Oguchi O, Konishi I, Fujii S. A comparative analysis of cross sectional imaging techniques in minimal deviation adenocarcinoma of the uterine cervix. Br J Obstet Gynaecol 2000; 107:1158 –1163. 19. Li H, Sugimura K, Okizuka H, et al. Markedly high signal intensity lesions in the uterine cervix on T2-weighted imaging: differentiation between mucin-producing carcinomas and nabothian cysts. Radiat Med 1999; 17:137–143. 20. Yoden E, Mikami Y, Fujiwara K, Kohno I, Imajo Y. Florid endocervical glandular hyperplasia with pyloric gland metaplasia: a radiologic pitfall. J Comput Assist Tomogr 2001; 25:94 –97. 21. Chen KTK. Female genital tract tumors in PeutzJeghers syndrome. Hum Pathol 1986; 17:858 – 861. 22. Tsuruchi N, Tsukamoto N, Kaku T, Kamura T, Nakano H. Adenoma malignum of the uterine cervix detected by imaging methods in a patient with Peutz-Jeghers syndrome. Gynecol Oncol 1994; 54:232–236. 23. Choi CG, Kim SH, Kim JS, Chi JG, Song ES, Han MC. Adenoma malignum of uterine cervix in Peutz-Jeghers syndrome: CT and US features. J Comput Assist Tomogr 1993; 17:819 – 821. 24. Kaminski PF, Norris HJ. Coexistence of ovarian neoplasms and endocervical adenocarcinoma. Obstet Gynecol 1984; 64:553–556. 25. Sheridan E, Lorigan PC, Goepel J, Radstone DJ, Coleman RE. Small cell carcinoma of the cervix. Clin Oncol (R Coll Radiol) 1996; 8:102–105. 26. Albores-Saavedra J, Larraza O, Poucell S, Rodriguez-Martinez HA. Carcinoid of the uterine cervix: additional observation on a new tumor entity. Cancer 1976; 38:2328 –2342. 27. Ueda G, Yamasaki M. Neuroendocrine carcinoma of the uterus. Curr Top Pathol 1992; 85:309 –335.

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28. Koch CA, Azumi N, Furlong MA, et al. Carcinoid syndrome caused by an atypical carcinoid of the uterine cervix. J Clin Endocrinol Metab 1999; 84: 4209 – 4213. 29. Curtin JP, Morrow CP. Melanoma of female genital tract. In: Coppleson M, ed. Gynecologic oncology. New York, NY: Churchill Livingstone, 1992. 30. Kristiansen SB, Anderson R, Cohen DM. Primary malignant melanoma of the cervix and review of literature. Gynecol Oncol 1992; 47:398 – 403. 31. Peyman GA, Mafee MF. Uveal melanoma and similar lesions: the role of magnetic resonance imaging and computed tomography. Radiol Clin North Am 1987; 25:471– 486. 32. Atlas SW, Grossman RJ, Gomori JN, et al. MR imaging of intracranial metastatic melanoma. J Comput Assist Tomogr 1987; 11:577–582. 33. Woodruff WW Jr, Djang WT, McLendon RE, Heinz RE, Voorhees DR. Intracerebral malignant melanoma: high-field strength MR imaging. Radiology 1987; 165:209 –213. 34. Miyagi Y, Yamada S, Miyagi Y, et al. Malignant melanoma of uterine cervix. J Obstet Gynaecol Res 1997; 23:511–519. 35. Moon WK, Kim SH, Han MC. MR findings of malignant melanoma of the vagina. Clin Radiol 1993; 48:326 –328. 36. Yamada I, Suzuki S. Primary uterine lymphoma: MR imaging. AJR Am J Roentgenol 1993; 160: 662– 663. 37. Aozasa K, Saeli K, Ohsawa M, Horiuchi K, Mishima K, Tsujimoto M. Malignant lymphoma of the uterus: report of seven cases with immunohistochemical study. Cancer 1993; 72:1959 – 1964. 38. Kawakami S, Togashi K, Kojima N, Morikawa K, Mori T, Konishi J. MR appearance of malignant lymphoma of the uterus. J Comput Tomogr 1995; 19:238 –242. 39. Kim YS, Koh BH, Cho OK, Rhim HC. MR imaging of primary uterine lymphoma. Abdom Imaging 1997; 22:441– 444. 40. Dang HT, Terk MR, Colletti PM, Schlaerth JB, Curtin JP. Primary lymphoma of the cervix: MRI findings with gadolinium. Magn Reson Imaging 1991; 9:941–944. 41. Mehta M, Thurston WA. Magnetic resonance imaging appearance of primary cervical non-Hodgkin’s lymphoma: 3 case reports. Can Assoc Radiol J 1998; 49:250 –252. 42. Clark DP, Ostler P, Watkinson A, Collis C, Berger L. Magnetic resonance imaging in primary cervical lymphoma: the role in diagnosis and follow-up. Clin Radiol 1998; 53:383–385. 43. Gompel C, Silverberg SG. The cervix: benign tumors and tumor-like lesions. In: Pathology in gynecology and obstetrics. 4th ed. Philadelphia, Pa: Lippincott, 1994. 44. Hricak H, Tscholakoff D, Heinrichs L, et al. Uterine leiomyomas: correlation of MR, histopathologic findings, and symptoms. Radiology 1986; 158:385–391. 45. Ueda H, Togashi K, Konishi I, et al. Unusual appearances of uterine leiomyomas: MR imaging findings and their histopathologic backgrounds. RadioGraphics 1999; 19:S131–S145.

Okamoto et al

445

46. Oguchi O, Mori A, Kobayashi Y, Horiuchi A, Nikaido T, Fujii S. Prediction of histopathologic features and proliferative activity of uterine leiomyoma by magnetic resonance imaging prior to GnRH analogue therapy: correlation between T2weighted images and effect of GnRH analogue. J Obstet Gynaecol 1995; 21:107–117. 47. Okizuka H, Sugimura K, Takemori M, Obayashi C, Kitao M, Ishida T. MR detection of degenerating uterine leiomyomas. J Comput Assist Tomogr 1993; 17:760 –766. 48. Kawakami S, Togashi K, Konishi I, et al. Red degeneration of uterine leiomyoma: MR appearance. J Comput Assist Tomogr 1994; 18:925–928. 49. Tsushima Y, Kita T, Yamamoto K. Uterine lipoleiomyoma: MRI, CT, and ultrasonographic findings. Br J Radiol 1997; 70:1068 –1070. 50. Yamashita Y, Torashima M, Takahashi M, et al. Hyperintense uterine leiomyoma at T2-weighted MR imaging: differentiation with dynamic enhanced MR imaging and clinical implications. Radiology 1993; 189:721–725. 51. Werber J, Prasadarao PR, Harris VJ. Cervical pregnancy diagnosed by ultrasound. Radiology 1983; 149:279 –280. 52. Parente JT, Ou C, Levy J, Legatt E. Cervical pregnancy analysis: a review and report of five cases. Obstet Gynecol 1983; 62:79 – 82. 53. Rothe DJ, Birnbaum SJ. Cervical pregnancy: diagnosis and management. Obstet Gynecol 1973; 42:675– 680. 54. Jung SE, Byun JY, Lee JM, et al. Characteristic MR findings of cervical pregnancy. J Magn Reson Imaging 2001; 13:918 –922. 55. Berek JS, Adashi EY, Hillard PA. Genitourinary infections and sexually transmitted diseases. In: Novak’s gynecology. 12th ed. Baltimore, Md: Williams & Wilkins, 1996; 429 – 445. 56. Danforth DN, Scott JR. Obstetrics and gynecology. Philadelphia, Pa: Lippincott, 1986. 57. Novak ER, Woodruff JD. Novak’s gynecologic and obstetric pathology with clinical and endocrine relations. 8th ed. Philadelphia, Pa: Saunders, 1979. 58. Fogel SR, Slasky BS. Sonography of nabothian cysts. AJR Am J Roentgenol 1982; 138:927–930. 59. Kurman RJ, Norris HJ, Wilkinson E. Tumors of the cervix. In: Atlas of tumor pathology: tumors of the cervix, vagina, and vulva. Washington, DC: Armed Forces Institute of Pathology, 1992. 60. Togashi K, Noma S, Ozasa H. CT and MR demonstration of nabothian cysts mimicking a cystic adnexal mass. J Comput Assist Tomogr 1987; 11: 1091–1092. 61. Golan A, Ber A, Wolman I, David MP. Cervical polyp: evaluation of current treatment. Gynecol Obstet Invest 1994; 37:56 –58. 62. Togashi K. Miscellaneous lesions of the uterus. In: MRI of the female pelvis. Tokyo, Japan: IgakuShoin, 1993; 179 –202. 63. Fukunaga M. Uterus-like mass in the uterine cervix: superficial cervical endometriosis with florid smooth muscle metaplasia? Virchows Arch 2001; 438:302–305.

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