(Radiographics. 1999;19:S103-S116.)
© RSNA, 1999
Recurrent Cervical Carcinoma: Typical and Atypical Manifestations1
Ann S. Fulcher, MD,
Susan G. O'Sullivan, MD,
Eileen M. Segreti, MD and
Brian D. Kavanagh, MD
1 From the Departments of Radiology (A.S.F., S.G.O.), Obstetrics and Gynecology (E.M.S.), and Radiation Oncology (B.D.K.), Medical College of Virginia, Virginia Commonwealth University, 12th and Marshall Sts, Richmond, VA 23298-0058. Recipient of a Certificate of Merit award for a scientific exhibit at the 1998 RSNA scientific assembly. Received February 5, 1999; revision requested March 17 and received March 31; accepted April 1. Address reprint requests to A.S.F.
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Abstract
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After treatment of cervical carcinoma, recurrent disease may be observed in multiple sites at imaging. Both typical and atypical manifestations of recurrent disease occur. Typical manifestations of recurrent cervical carcinoma involve the pelvis and lymph nodes. Pelvic recurrences may be observed as masses involving the cervix and uterus, vagina or vaginal cuff, parametria, bladder, ureters, rectum, or ovaries and may result in fistula formation or hydronephrosis. Nodal recurrence may be identified as enlarged pelvic and retroperitoneal nodes. Atypical manifestations of recurrent cervical carcinoma are being recognized with greater frequency due to the use of intensive pelvic radiation therapy, the evolution of improved imaging techniques, and the more frequent use of imaging as a means of surveillance. These atypical manifestations may involve the solid organs of the abdomen (focal masses) as well as the peritoneum, mesentery, and omentum (implants); gastrointestinal tract (obstruction, fistula formation, ischemia); chest (metastases to the lung parenchyma, pleura, and pericardium); bones (destructive lesions); and other sites. Familiarity with the imaging features of recurrent cervical carcinoma in these anatomic locations will facilitate prompt, accurate diagnosis and treatment.
Index Terms: Abdomen, neoplasms, 70.33 • Adrenal glands, neoplasms, 86.33 • Bone neoplasms, secondary, 30.33, 40.33 • Liver neoplasms, metastases, 761.33 • Lymphatic system, neoplasms, 99.8311 • Pelvic organs, neoplasms, 80.33 • Thorax, neoplasms, 60.33 • Uterine neoplasms, 854.32
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INTRODUCTION
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Cervical carcinoma is a common gynecologic malignancy that was seen in 13,700 new cases and caused 4,900 deaths in the United States in 1998 (1). Although advances in surgical techniques, radiation therapy, and chemotherapy have resulted in improved survival rates, approximately 30% of women with invasive cervical carcinoma die as a result of recurrent or persistent disease (2). Recurrence is defined as local tumor regrowth or the development of distant metastasis discovered 6 months or more after complete regression of the treated lesion (3).
Although the typical manifestations of recurrent cervical carcinoma such as pelvic masses and lymphadenopathy are well recognized, less typical manifestations such as peritoneal carcinomatosis and solid organ metastases also occur. The increasing prevalence of these less typical manifestations is related in part to the use of intensive pelvic radiation therapy, which has resulted in a shift away from pelvic recurrence toward distant recurrence (4). In addition, these less common patterns of recurrence are being recognized with greater frequency due to improvements in cross-sectional imaging techniques and more extensive and frequent imaging of patients with suspected recurrence. However, a review of the recent radiology literature yields little discussion of the various sites and manifestations of recurrent cervical carcinoma. Most information regarding recurrent cervical carcinoma is derived from autopsy or from surgical series performed before the advent of cross-sectional imaging techniques (5–12).
A retrospective review of patients with cervical carcinoma conducted at our institution revealed manifestations of recurrence including pelvic masses, lymphadenopathy, solid and hollow organ metastases, peritoneal carcinomatosis, and pulmonary and osseous metastases. In this article, we discuss and illustrate the spectrum of typical and atypical manifestations of recurrent cervical carcinoma that may be encountered at computed tomography (CT), magnetic resonance (MR) imaging, ultrasound (US), and barium examination.
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PELVIC RECURRENCE
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Pelvic recurrence may involve the cervix, uterus, vagina, parametria, bladder, ureters, rectum, and ovaries (3,5,10). Although some pelvic recurrences are asymptomatic and may be detected only at clinical examination, surveillance CT, or MR imaging, many affected patients will present with symptoms such as lower extremity swelling due to lymphatic obstruction or pain due to either nerve compression or tumoral obstruction of the ureters.
The prevalence of pelvic recurrence of cervical carcinoma varies with the stage at presentation, histologic type of the tumor, adequacy of therapy used, and host response (11,12). In a series of 249 patients with stage IB cervical carcinoma treated with radical hysterectomy and pelvic lymphadenectomy, Larson et al (13) noted recurrent disease in 27 patients (10.8%), with pelvic recurrence accounting for 16 of the 27 recurrences (59%).
Pelvic recurrence of cervical carcinoma may be located centrally in the pelvis in the preserved cervix or in the postsurgical bed and vaginal cuff (3,5,10). When recurrence occurs within the preserved cervix, obstruction of the cervical os may occur and may result in hydrometra (Fig 1). Central pelvic recurrences may extend posteriorly to involve the rectum with a recto-vaginal fistula developing in some instances (Fig 2) or may extend laterally to involve the pelvic side wall.
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Figures 1, 2. (1) Central pelvic recurrence in the cervix with no anterior, posterior, or lateral extension of disease in a 71-year-old woman who initially underwent radiation therapy. (a) CT scan shows enlargement and heterogeneity of the cervix (arrows), a finding indicative of recurrent carcinoma. Fluid is noted in the endocervical canal (arrowhead). (b) CT scan obtained 3 cm cephalad to a demonstrates a markedly distended and fluid-filled endometrial cavity (hydrometra) (*) that resulted from recurrent tumor obstructing the external cervical os. The superior aspect of the unenhanced urinary bladder (arrow) is seen anterior to the uterus. (2) Central pelvic recurrence with posterior extension and development of a rectovaginal fistula in a 34-year-old woman who initially underwent radical hysterectomy. (a) CT scan reveals an air-containing soft-tissue mass (arrows) arising from the left side of the vaginal cuff and extending posteriorly to involve the rectum (R). The air locules within the mass are supportive evidence of a rectovaginal fistula. (b) Lateral image from a barium enema study helps confirm the fistula (arrowheads) connecting the rectum (R) and the partially enhanced vaginal cuff (arrows).
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Figures 1, 2. (1) Central pelvic recurrence in the cervix with no anterior, posterior, or lateral extension of disease in a 71-year-old woman who initially underwent radiation therapy. (a) CT scan shows enlargement and heterogeneity of the cervix (arrows), a finding indicative of recurrent carcinoma. Fluid is noted in the endocervical canal (arrowhead). (b) CT scan obtained 3 cm cephalad to a demonstrates a markedly distended and fluid-filled endometrial cavity (hydrometra) (*) that resulted from recurrent tumor obstructing the external cervical os. The superior aspect of the unenhanced urinary bladder (arrow) is seen anterior to the uterus. (2) Central pelvic recurrence with posterior extension and development of a rectovaginal fistula in a 34-year-old woman who initially underwent radical hysterectomy. (a) CT scan reveals an air-containing soft-tissue mass (arrows) arising from the left side of the vaginal cuff and extending posteriorly to involve the rectum (R). The air locules within the mass are supportive evidence of a rectovaginal fistula. (b) Lateral image from a barium enema study helps confirm the fistula (arrowheads) connecting the rectum (R) and the partially enhanced vaginal cuff (arrows).
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Figures 1, 2. (1) Central pelvic recurrence in the cervix with no anterior, posterior, or lateral extension of disease in a 71-year-old woman who initially underwent radiation therapy. (a) CT scan shows enlargement and heterogeneity of the cervix (arrows), a finding indicative of recurrent carcinoma. Fluid is noted in the endocervical canal (arrowhead). (b) CT scan obtained 3 cm cephalad to a demonstrates a markedly distended and fluid-filled endometrial cavity (hydrometra) (*) that resulted from recurrent tumor obstructing the external cervical os. The superior aspect of the unenhanced urinary bladder (arrow) is seen anterior to the uterus. (2) Central pelvic recurrence with posterior extension and development of a rectovaginal fistula in a 34-year-old woman who initially underwent radical hysterectomy. (a) CT scan reveals an air-containing soft-tissue mass (arrows) arising from the left side of the vaginal cuff and extending posteriorly to involve the rectum (R). The air locules within the mass are supportive evidence of a rectovaginal fistula. (b) Lateral image from a barium enema study helps confirm the fistula (arrowheads) connecting the rectum (R) and the partially enhanced vaginal cuff (arrows).
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Figures 1, 2. (1) Central pelvic recurrence in the cervix with no anterior, posterior, or lateral extension of disease in a 71-year-old woman who initially underwent radiation therapy. (a) CT scan shows enlargement and heterogeneity of the cervix (arrows), a finding indicative of recurrent carcinoma. Fluid is noted in the endocervical canal (arrowhead). (b) CT scan obtained 3 cm cephalad to a demonstrates a markedly distended and fluid-filled endometrial cavity (hydrometra) (*) that resulted from recurrent tumor obstructing the external cervical os. The superior aspect of the unenhanced urinary bladder (arrow) is seen anterior to the uterus. (2) Central pelvic recurrence with posterior extension and development of a rectovaginal fistula in a 34-year-old woman who initially underwent radical hysterectomy. (a) CT scan reveals an air-containing soft-tissue mass (arrows) arising from the left side of the vaginal cuff and extending posteriorly to involve the rectum (R). The air locules within the mass are supportive evidence of a rectovaginal fistula. (b) Lateral image from a barium enema study helps confirm the fistula (arrowheads) connecting the rectum (R) and the partially enhanced vaginal cuff (arrows).
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Central recurrences may also grow anteriorly, resulting in contiguous spread to the urinary bladder and even to the anterior abdominal wall (Figs 3, 4). Such local recurrence with anterior extension may lead to ureteral obstruction by direct encasement of the ureter or by tumor infiltration of the bladder wall, which results in obstruction at the ureteral orifice (Fig 5). In an autopsy series conducted by Pearson and Garcia (9), hydronephrosis was detected in approximately 70% of pelvic recurrences. In addition to ureteral obstruction, tumor extension to the urinary bladder predisposes the patient to development of a vesicovaginal fistula, which is seen on excretory-phase CT scans as contrast material extending from the enhanced urinary bladder to the vaginal cuff or vagina (Fig 4).
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Figures 3, 4. (3) Central pelvic recurrence with anterior extension into the urinary bladder and left ureter in a 33-year-old woman. Excretory-phase contrast material-enhanced CT scan shows a large, centrally located pelvic mass (straight arrows) that is inseparable from the posterior wall of the urinary bladder (arrowheads) and encases the enhanced left ureter (curved arrow). (4) Central pelvic recurrence with lateral and anterior extension in a 57-year-old woman who presented with pelvic pain, a palpable anterior pelvic wall mass, and vaginal discharge. CT scan demonstrates a mass (straight arrows) arising from the vaginal cuff, infiltrating the right lateral and anterior walls of the urinary bladder (B), and invading the anterior pelvic wall (arrowheads). A vesicovaginal fistula (curved arrow) is depicted as a tract of contrast material extending from the urinary bladder into the vaginal cuff mass.
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Figures 3, 4. (3) Central pelvic recurrence with anterior extension into the urinary bladder and left ureter in a 33-year-old woman. Excretory-phase contrast material-enhanced CT scan shows a large, centrally located pelvic mass (straight arrows) that is inseparable from the posterior wall of the urinary bladder (arrowheads) and encases the enhanced left ureter (curved arrow). (4) Central pelvic recurrence with lateral and anterior extension in a 57-year-old woman who presented with pelvic pain, a palpable anterior pelvic wall mass, and vaginal discharge. CT scan demonstrates a mass (straight arrows) arising from the vaginal cuff, infiltrating the right lateral and anterior walls of the urinary bladder (B), and invading the anterior pelvic wall (arrowheads). A vesicovaginal fistula (curved arrow) is depicted as a tract of contrast material extending from the urinary bladder into the vaginal cuff mass.
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Figure 5a. Central pelvic recurrence with anterior extension resulting in hydronephrosis in a 53-year-old woman who presented with flank pain. (a) CT scan reveals an infiltrative soft-tissue mass located centrally in the pelvis (arrows). (b) CT scan obtained at the level of the kidneys shows high-grade, bilateral hydronephrosis (*) resulting from ureteral obstruction proximal to the pelvic mass (cf a). Bilateral nephrostomy tubes are also noted (arrows). (c) Coronal US image of the right kidney shows marked dilatation of the calyces (arrows) and renal pelvis (*).
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Figure 5b. Central pelvic recurrence with anterior extension resulting in hydronephrosis in a 53-year-old woman who presented with flank pain. (a) CT scan reveals an infiltrative soft-tissue mass located centrally in the pelvis (arrows). (b) CT scan obtained at the level of the kidneys shows high-grade, bilateral hydronephrosis (*) resulting from ureteral obstruction proximal to the pelvic mass (cf a). Bilateral nephrostomy tubes are also noted (arrows). (c) Coronal US image of the right kidney shows marked dilatation of the calyces (arrows) and renal pelvis (*).
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Figure 5c. Central pelvic recurrence with anterior extension resulting in hydronephrosis in a 53-year-old woman who presented with flank pain. (a) CT scan reveals an infiltrative soft-tissue mass located centrally in the pelvis (arrows). (b) CT scan obtained at the level of the kidneys shows high-grade, bilateral hydronephrosis (*) resulting from ureteral obstruction proximal to the pelvic mass (cf a). Bilateral nephrostomy tubes are also noted (arrows). (c) Coronal US image of the right kidney shows marked dilatation of the calyces (arrows) and renal pelvis (*).
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At times, pelvic recurrences are identified as pelvic side wall masses that are not associated with a centrally located pelvic mass (Fig 6). Another manifestation of pelvic recurrence is that of tumor involving the ovaries (Fig 7), which may result from contiguous extension of pelvic tumor, hematogenous or lymphatic spread, or peritoneal implants.
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Figures 6, 7. (6) Pelvic side wall recurrence without evidence of a centrally located pelvic recurrence in a 50-year-old woman who presented with pelvic and left lower extremity pain. CT scan demonstrates an enhancing mass (arrows) that is inseparable from the left pyriform muscle (P), presacral tissues, and the region of the left sciatic nerve. Its proximity to the sciatic nerve probably accounted for the patient's left lower extremity pain. Recurrent squamous cell carcinoma was confirmed at percutaneous biopsy. (7) Pelvic recurrence involving the ovaries in a 55-year-old woman who initially underwent radiation therapy. Contrast-enhanced CT scan of the pelvis shows large, low-attenuation masses bilaterally in the pelvis (M). Ovarian metastases from cervical carcinoma were confirmed at surgery.
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Figures 6, 7. (6) Pelvic side wall recurrence without evidence of a centrally located pelvic recurrence in a 50-year-old woman who presented with pelvic and left lower extremity pain. CT scan demonstrates an enhancing mass (arrows) that is inseparable from the left pyriform muscle (P), presacral tissues, and the region of the left sciatic nerve. Its proximity to the sciatic nerve probably accounted for the patient's left lower extremity pain. Recurrent squamous cell carcinoma was confirmed at percutaneous biopsy. (7) Pelvic recurrence involving the ovaries in a 55-year-old woman who initially underwent radiation therapy. Contrast-enhanced CT scan of the pelvis shows large, low-attenuation masses bilaterally in the pelvis (M). Ovarian metastases from cervical carcinoma were confirmed at surgery.
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In patients who undergo radiation therapy, the distinction between pelvic recurrence and radiation-induced changes such as fibrosis may present a diagnostic challenge. Recent studies indicate that dynamic contrast-enhanced T1-weighted MR imaging techniques may be helpful in making this important distinction, with accuracies of 82%–83% (14,15). In addition, serial or follow-up MR imaging is useful in distinguishing recurrent disease from radiation-induced fibrosis because the latter is expected to remain stable or diminish in prominence over time.
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NODAL RECURRENCE
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Lymphatic involvement in cervical cancer has traditionally been separated into primary and secondary nodal groups (6,7). The significance of these two groups is that the prognosis worsens as nodal involvement progresses from the primary to the secondary group. The primary group consists of the paracervical, parametrial, internal and external iliac, and obturator nodes. The secondary group consists of the sacral, common iliac, inguinal, and paraaortic nodes. With respect to nodal disease, a somewhat orderly sequence of involvement usually occurs. In general, paracervical and parametrial lymph nodes are involved first, followed by the obturator nodes (considered a medial group of the external iliac nodes), the remaining external iliac nodes, and the internal iliac nodes (6) (Fig 8a). The secondary group, which includes the common iliac and paraaortic nodes, is usually subsequently involved (Fig 8b, 8c). Multiple extrapelvic and extraabdominal nodal sites of recurrence including the parabronchial, supraclavic- ular, and axillary nodes have been reported but are less frequently involved than those in the primary and secondary groups (3).
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Figure 8a. Extensive pelvic and retroperitoneal nodal recurrence in a 57-year-old woman in whom adenocarcinoma of the cervix had been diagnosed 2 years earlier. (a) CT scan of the pelvis demonstrates enlarged left external iliac lymph nodes (N) that are similar in attenuation to the enhanced urinary bladder (B). An enlarged right obturator lymph node is also seen (arrow). (b) CT scan obtained 3 cm cephalad to a shows an enlarged, low-attenuating lymph node (N) in the left common iliac chain that is inseparable from the left psoas muscle (arrowhead). An enlarged right common iliac lymph node (arrow) similar in attenuation to the right obturator node (cf a) is also noted. (c) CT scan obtained 3 cm cephalad to b reveals enlarged, heterogeneously enhancing paraaortic (straight arrow) and interaortocaval (arrowhead) lymph nodes. The inferior vena cava (curved arrow) is compressed by the lymphadenopathy.
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Figure 8b. Extensive pelvic and retroperitoneal nodal recurrence in a 57-year-old woman in whom adenocarcinoma of the cervix had been diagnosed 2 years earlier. (a) CT scan of the pelvis demonstrates enlarged left external iliac lymph nodes (N) that are similar in attenuation to the enhanced urinary bladder (B). An enlarged right obturator lymph node is also seen (arrow). (b) CT scan obtained 3 cm cephalad to a shows an enlarged, low-attenuating lymph node (N) in the left common iliac chain that is inseparable from the left psoas muscle (arrowhead). An enlarged right common iliac lymph node (arrow) similar in attenuation to the right obturator node (cf a) is also noted. (c) CT scan obtained 3 cm cephalad to b reveals enlarged, heterogeneously enhancing paraaortic (straight arrow) and interaortocaval (arrowhead) lymph nodes. The inferior vena cava (curved arrow) is compressed by the lymphadenopathy.
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Figure 8c. Extensive pelvic and retroperitoneal nodal recurrence in a 57-year-old woman in whom adenocarcinoma of the cervix had been diagnosed 2 years earlier. (a) CT scan of the pelvis demonstrates enlarged left external iliac lymph nodes (N) that are similar in attenuation to the enhanced urinary bladder (B). An enlarged right obturator lymph node is also seen (arrow). (b) CT scan obtained 3 cm cephalad to a shows an enlarged, low-attenuating lymph node (N) in the left common iliac chain that is inseparable from the left psoas muscle (arrowhead). An enlarged right common iliac lymph node (arrow) similar in attenuation to the right obturator node (cf a) is also noted. (c) CT scan obtained 3 cm cephalad to b reveals enlarged, heterogeneously enhancing paraaortic (straight arrow) and interaortocaval (arrowhead) lymph nodes. The inferior vena cava (curved arrow) is compressed by the lymphadenopathy.
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The prevalence of lymphatic involvement by tumor varies with the histologic type of the tumor. In an autopsy series of 41 patients with cervical carcinoma, Drescher et al (10) found that tumor involvement of the primary nodal group occurred in 75% of patients with adenocarcinoma compared with 61% of patients with squamous cell carcinoma. Similarly, tumor was identified in paraaortic nodes in 62% of patients with adenocarcinoma compared with 30% with squamous cell carcinoma.
Until the advent of CT and MR imaging, nodes in the abdomen attained considerable size and often resulted in urinary tract and intestinal obstruction before coming to clinical attention (8). Both CT and MR imaging play an important role in the early detection of recurrent nodal disease, which ranges from scattered, minimally enlarged lymph nodes to large, conglomerate nodal masses. Although CT and MR imaging cannot help distinguish reactive from neoplastic lymph nodes, they are useful in detecting enlarged nodes and in guiding percutaneous biopsies.
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RECURRENCE IN THE SOLID ORGANS OF THE ABDOMEN
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After the pelvis and lymph nodes, the solid organs of the abdomen are the most frequent sites of involvement by recurrent cervical carcinoma (3,9,10). The intraabdominal solid organ most commonly involved is the liver (10,16). Liver metastases have been reported in approximately one-third of patients who present with recurrent cervical carcinoma (10,16). State-of-the-art cross-sectional imaging techniques permit detection of small liver metastases; prior to the availability of these techniques, however, liver metastases grew to large proportions and were present for long periods of time before hepatic failure, coma, or death ensued (8). Hepatic recurrence of cervical carcinoma usually appears as focal hypoechoic lesions at US (16) and as multiple focal lesions with variable enhancement patterns at CT (Fig 9).
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Figures 9, 10. (9) Liver metastases in a 44-year-old woman with a history of cervical carcinoma who had undergone radiation therapy. Contrast-enhanced CT scan shows multiple low-attenuation lesions in the right and left hepatic lobes (arrows), findings that are indicative of liver metastases. Enlarged, high-attenuation retrocrural lymph nodes are also seen (arrowheads); the cause of the high attenuation within the nodes is unknown. Results of liver biopsy confirmed recurrent cervical carcinoma. (10) Adrenal metastases in a 53-year-old woman with a history of cervical carcinoma. Contrast-enhanced CT scan demonstrates bilateral low-attenuation adrenal masses (arrows), findings that are indicative of metastases.
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The adrenal gland is the next most commonly involved intraabdominal solid organ (3,10). Adrenal metastases have been noted in 14%–16% of patients presenting with recurrent cervical carcinoma (3,10). Patients with adenocarcinoma of the cervix have a greater prevalence of adrenal metastases than do patients with squamous cell carcinoma (10). Adrenal involvement by recurrent cervical carcinoma is indistinguishable from involvement by other primary malignancies (Fig 10). However, unenhanced CT or in-phase and opposed-phase MR imaging techniques may be helpful in characterizing a nonspecific adrenal lesion as an adenoma or metastasis. The spleen, pancreas, and kidneys are rarely involved by recurrent tumor (Fig 11).
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Figures 9, 10. (9) Liver metastases in a 44-year-old woman with a history of cervical carcinoma who had undergone radiation therapy. Contrast-enhanced CT scan shows multiple low-attenuation lesions in the right and left hepatic lobes (arrows), findings that are indicative of liver metastases. Enlarged, high-attenuation retrocrural lymph nodes are also seen (arrowheads); the cause of the high attenuation within the nodes is unknown. Results of liver biopsy confirmed recurrent cervical carcinoma. (10) Adrenal metastases in a 53-year-old woman with a history of cervical carcinoma. Contrast-enhanced CT scan demonstrates bilateral low-attenuation adrenal masses (arrows), findings that are indicative of metastases.
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Figure 11a. Renal metastases in a 45-year-old woman with cervical carcinoma who had undergone radiation therapy. Contrast-enhanced CT scans obtained at the level of the kidneys (b obtained at a slightly lower level than a) reveal bilateral low-attenuation renal masses (arrows). A CT scan obtained 1 year earlier demonstrated normal kidneys.
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Figure 11b. Renal metastases in a 45-year-old woman with cervical carcinoma who had undergone radiation therapy. Contrast-enhanced CT scans obtained at the level of the kidneys (b obtained at a slightly lower level than a) reveal bilateral low-attenuation renal masses (arrows). A CT scan obtained 1 year earlier demonstrated normal kidneys.
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PERITONEAL, OMENTAL, AND MESENTERIC RECURRENCES
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Although metastatic disease of the peritoneum, omentum, and mesentery is well recognized in association with primary tumors of the gastrointestinal tract, pancreas, and ovaries, recurrent cervical carcinoma may also involve these structures. In autopsy series of patients with recurrent cervical carcinoma, the prevalence of peritoneal carcinomatosis has ranged from 5% to 27% (3,5,9,10). Prior to the use of surveillance CT and MR imaging as means of following up patients with cervical carcinoma, peritoneal carcinomatosis was not suspected until patients presented with increasing abdominal girth and pain (8).
Although imaging of the peritoneum, omentum, and mesentery is often performed with CT, MR imaging has been advocated in the recent literature as an accurate means of detecting peritoneal disease (17,18). In particular, gadolinium-enhanced fat-saturated T1-weighted MR imaging without oral administration of contrast material or in conjunction with oral administration of dilute barium has proved useful in the detection of peritoneal disease (17,18). Regardless of the imaging modality used, peritoneal involvement by recurrent cervical carcinoma may be identified as implants that result in scalloping of the liver contour (Fig 12), peritoneal nodularity (Fig 13b), and serosal soft-tissue masses that cause extrinsic compression of the bowel (Fig 13c, 13d). Although ascites is a nonspecific finding, it often occurs in association with peritoneal carcinomatosis, and its presence should prompt a meticulous search for recurrent disease involving the peritoneum (Fig 14).
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Figure 12. Multiple peritoneal implants on the surface of the liver in a 48-year-old woman with cervical carcinoma. Contrast-enhanced CT scan of the abdomen demonstrates multiple low-attenuation peritoneal implants (arrows) with resulting scalloping of the liver surface.
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Figure 13a. Mesenteric and peritoneal recurrence of cervical carcinoma in a 37-year-old woman who initially underwent radiation therapy. (a) Contrast-enhanced CT scan obtained at the level of the renal hila shows a mesenteric mass (arrows) encasing the superior mesenteric artery (arrowhead). (b) Contrast-enhanced CT scan obtained 5 cm caudad to a reveals ascites (A) and irregular thickening of the peritoneum (arrows), findings that are indicative of implants. (c) Contrast-enhanced CT scan obtained 8 cm caudad to b shows a low-attenuation, heterogeneously enhancing tumor implant in the right paracolic gutter (arrow) with resulting medial displacement of the ascending colon (C). (d) Contrast-enhanced CT scan obtained at the level of the false pelvis demonstrates multiple serosal implants (arrows) distorting the lumen of the sigmoid colon (C).
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Figure 13b. Mesenteric and peritoneal recurrence of cervical carcinoma in a 37-year-old woman who initially underwent radiation therapy. (a) Contrast-enhanced CT scan obtained at the level of the renal hila shows a mesenteric mass (arrows) encasing the superior mesenteric artery (arrowhead). (b) Contrast-enhanced CT scan obtained 5 cm caudad to a reveals ascites (A) and irregular thickening of the peritoneum (arrows), findings that are indicative of implants. (c) Contrast-enhanced CT scan obtained 8 cm caudad to b shows a low-attenuation, heterogeneously enhancing tumor implant in the right paracolic gutter (arrow) with resulting medial displacement of the ascending colon (C). (d) Contrast-enhanced CT scan obtained at the level of the false pelvis demonstrates multiple serosal implants (arrows) distorting the lumen of the sigmoid colon (C).
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Figure 13c. Mesenteric and peritoneal recurrence of cervical carcinoma in a 37-year-old woman who initially underwent radiation therapy. (a) Contrast-enhanced CT scan obtained at the level of the renal hila shows a mesenteric mass (arrows) encasing the superior mesenteric artery (arrowhead). (b) Contrast-enhanced CT scan obtained 5 cm caudad to a reveals ascites (A) and irregular thickening of the peritoneum (arrows), findings that are indicative of implants. (c) Contrast-enhanced CT scan obtained 8 cm caudad to b shows a low-attenuation, heterogeneously enhancing tumor implant in the right paracolic gutter (arrow) with resulting medial displacement of the ascending colon (C). (d) Contrast-enhanced CT scan obtained at the level of the false pelvis demonstrates multiple serosal implants (arrows) distorting the lumen of the sigmoid colon (C).
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Figure 13d. Mesenteric and peritoneal recurrence of cervical carcinoma in a 37-year-old woman who initially underwent radiation therapy. (a) Contrast-enhanced CT scan obtained at the level of the renal hila shows a mesenteric mass (arrows) encasing the superior mesenteric artery (arrowhead). (b) Contrast-enhanced CT scan obtained 5 cm caudad to a reveals ascites (A) and irregular thickening of the peritoneum (arrows), findings that are indicative of implants. (c) Contrast-enhanced CT scan obtained 8 cm caudad to b shows a low-attenuation, heterogeneously enhancing tumor implant in the right paracolic gutter (arrow) with resulting medial displacement of the ascending colon (C). (d) Contrast-enhanced CT scan obtained at the level of the false pelvis demonstrates multiple serosal implants (arrows) distorting the lumen of the sigmoid colon (C).
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Figures 14, 15. (14) Extensive ascites and peritoneal implants in a 48-year-old woman with cervical carcinoma who initially underwent radical hysterectomy. T2-weighted fat-suppressed MR image (repetition time msec/effective echo time msec = 3,500/138) demonstrates extensive ascites (A) and a peritoneal implant protruding into the ascites (arrow). (15) Omental implant and Sister Joseph nodule in a 62-year-old woman with recurrent cervical carcinoma. Contrast-enhanced abdominal CT scan shows a low-attenuation omental implant (arrow). An umbilical soft-tissue mass (arrowhead) lies immediately anterior to the omental implant; this finding is indicative of an umbilical metastasis (Sister Joseph nodule). A low-attenuation mesenteric implant is also seen (M).
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Recurrent tumor deposits in the mesentery and omentum vary in appearance from discrete masses to infiltrative areas of soft-tissue attenuation (Figs 13a, 15). An unusual association with peritoneal and omental tumor involvement is that of an umbilical metastasis originally known as a Sister Joseph nodule (19) (Fig 15). Umbilical metastases are thought to develop from direct extension of tumor from the anterior peritoneal surface of the abdomen to the umbilicus. In addition, lymphatic, venous, and ligamentous communications that exist between the peritoneum and umbilicus provide alternative routes of tumor spread to the umbilicus in the setting of peritoneal carcinomatosis (19).
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Figures 14, 15. (14) Extensive ascites and peritoneal implants in a 48-year-old woman with cervical carcinoma who initially underwent radical hysterectomy. T2-weighted fat-suppressed MR image (repetition time msec/effective echo time msec = 3,500/138) demonstrates extensive ascites (A) and a peritoneal implant protruding into the ascites (arrow). (15) Omental implant and Sister Joseph nodule in a 62-year-old woman with recurrent cervical carcinoma. Contrast-enhanced abdominal CT scan shows a low-attenuation omental implant (arrow). An umbilical soft-tissue mass (arrowhead) lies immediately anterior to the omental implant; this finding is indicative of an umbilical metastasis (Sister Joseph nodule). A low-attenuation mesenteric implant is also seen (M).
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GASTROINTESTINAL TRACT RECURRENCE
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The rectum is frequently involved by recurrent cervical carcinoma, usually as a result of contiguous extension of tumor from the preserved cervix or vaginal cuff. Pearson and Garcia (9) noted that the rectovaginal tissues were involved by recurrent tumor in 17.3% of patients. Invasion of the rectum usually occurs at the rectosigmoid junction and is evidenced by mass effect, spiculation, and luminal narrowing (20) (Fig 16).
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Figure 16a. Rectal involvement by recurrent cervical carcinoma in a 34-year-old woman who presented with vaginal bleeding. (a) Lateral view from a barium enema study demonstrates spiculation and mass effect on the anterior wall of the rectosigmoid colon (arrows) as well as luminal narrowing. (b) Contrast-enhanced CT scan of the pelvis shows a recurrent mass in the preserved cervix (arrows) that is inseparable from the anterior wall of the rectum (R) and accounts for the extrinsic mass effect on the rectosigmoid colon noted in a. Packing material is seen in the cervix.
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Figure 16b. Rectal involvement by recurrent cervical carcinoma in a 34-year-old woman who presented with vaginal bleeding. (a) Lateral view from a barium enema study demonstrates spiculation and mass effect on the anterior wall of the rectosigmoid colon (arrows) as well as luminal narrowing. (b) Contrast-enhanced CT scan of the pelvis shows a recurrent mass in the preserved cervix (arrows) that is inseparable from the anterior wall of the rectum (R) and accounts for the extrinsic mass effect on the rectosigmoid colon noted in a. Packing material is seen in the cervix.
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The remainder of the colon and the small intestine can be involved by recurrent tumor in a variety of ways, including contiguous extension from the pelvis and intraperitoneal seeding. Recurrence may result in obstruction of the colon or small intestine. In one autopsy series, intestinal obstruction occurred in 12% of patients and was the immediate cause of death in 7% (9). Such obstructions can be demonstrated with barium examinations, CT, and MR imaging (Figs 17, 18). CT and MR imaging have an advantage in that they not only demonstrate the obstruction but also help detect the cause of the obstruction in many instances (Fig 18). Other manifestations of recurrent disease involving the gastrointestinal tract include fistula formation (Fig 19) and focal bowel wall thickening and tethering of bowel loops due to tumor implants in the mesentery (Fig 20).
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Figure 17. Small bowel obstruction in a 64-year-old woman who presented with nausea, vomiting, and abdominal pain. Anteroposterior view from a small bowel follow-through study demonstrates marked dilatation of the duodenum (D) and proximal jejunum (J) with an abrupt transition (arrow), findings that are indicative of a high-grade small bowel obstruction. Bilateral percutaneous nephrostomy tubes and inferior vena cava filters are also seen. Contiguous spread of an extensive pelvic recurrence was detected at surgery.
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Figure 18a. Small bowel obstruction in a 56-year-old woman with recurrent cervical carcinoma. (a) Contrast-enhanced CT scan shows multiple dilated loops of small bowel (B), a finding that is indicative of a small bowel obstruction. Air-fluid levels are also identified (arrows). (b) Contrast-enhanced CT scan obtained 5 cm cephalad to a elucidates the cause of the small bowel obstruction, a tumor implant (arrow) that is inseparable from a dilated loop of ileum (B). A collapsed descending colon is also noted (arrowhead).
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Figure 18b. Small bowel obstruction in a 56-year-old woman with recurrent cervical carcinoma. (a) Contrast-enhanced CT scan shows multiple dilated loops of small bowel (B), a finding that is indicative of a small bowel obstruction. Air-fluid levels are also identified (arrows). (b) Contrast-enhanced CT scan obtained 5 cm cephalad to a elucidates the cause of the small bowel obstruction, a tumor implant (arrow) that is inseparable from a dilated loop of ileum (B). A collapsed descending colon is also noted (arrowhead).
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Figure 19. Enterocutaneous fistula resulting from recurrent cervical carcinoma in a 51-year-old woman who initially underwent radical hysterectomy. Lateral view from a small bowel follow-through study demonstrates a tract of contrast material extending from the ileum to the skin (arrows).
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Figure 20. Focal wall thickening and tethering of the small intestine secondary to a mesenteric implant in a 55-year-old woman who presented with abdominal pain. Contrast-enhanced CT scan demonstrates a mesenteric tumor implant (arrow) that results in minor wall thickening and tethering of a small bowel loop (B).
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CHEST RECURRENCE
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Lung metastases from recurrent cervical carcinoma occurred in 33%–38% of cases in three separate autopsy series (3,5,10). Lung metastases may be present for a significant period of time before becoming symptomatic. Lung metastases occur with equal frequency in patients with adenocarcinoma and squamous cell carcinoma and may be either solitary or multiple (10). Chest radiography is commonly used to screen for recurrent disease. However, CT permits visualization of small nodules that may not be detected with conventional chest radiography (Fig 21).
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Figure 21. Multiple pulmonary metastases in a 53-year-old woman with a history of cervical carcinoma who presented for surveillance CT. Contrast-enhanced CT scan of the lower chest shows multiple bilateral pulmonary nodules 3-15 mm in diameter (arrows).
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Other sites of recurrent tumor in the chest include the pulmonary parenchyma and, less commonly, the pleura, bronchus, and pericardium (7,9,10). Pleural involvement may be detected as pleural thickening and nodularity and is often seen in association with hydrothorax (Fig 22). Hydrothorax is reported to be more frequently detected in patients with adenocarcinoma than in those with squamous cell carcinoma of the cervix and often occurs in association with ascites (10). Metastatic cervical carcinoma of the pericardium usually manifests as nodular soft-tissue thickening of the pericardium at CT or MR imaging (Fig 22).
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Figure 22. Pleural and pericardial recurrence of cervical carcinoma in a 35-year-old woman who presented with left-sided chest pain. Contrast-enhanced CT scan of the chest demonstrates minor bilateral pleural thickening (arrows), small bilateral pleural fluid collections, thickening and nodularity of the pericardium (arrowheads), and atelectasis in the lung bases. Thoracoscopy helped confirm pleural recurrence of cervical carcinoma.
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OSSEOUS RECURRENCE
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The prevalence of osseous metastases in the setting of recurrent cervical carcinoma ranges from 15% to 29% as reported in multiple autopsy series (3,5,6,8). The vertebral bodies are by far the most frequently involved bones, followed by the pelvis, ribs, and extremities (3,6,8). Bone involvement may occur by direct extension from paraaortic lymph nodes, by lymphatic or hematogenous spread, or from a pelvic recurrence (8). In a review of 55 patients with osseous metastases from cervical carcinoma, Blythe et al (21) noted that the most common mechanism of bone involvement was by direct extension of neoplasm from paraaortic nodes into the adjacent vertebral bodies. Bone metastases may appear as destructive lesions associated with soft-tissue masses of variable size (Fig 23). Gadolinium-enhanced fat-suppressed T1-weighted MR imaging is particularly useful in the detection of bone metastases, which are depicted as foci of enhancement within the marrow space (Fig 24).
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Figures 23, 24. (23) Vertebral metastasis in a 69-year-old woman with a history of cervical carcinoma who presented for evaluation of back pain. Contrast-enhanced CT scan reveals confluent lymphadenopathy (*) adjacent to the aorta (A) and esophagus (E). The lymphadenopathy has extended posteriorly and caused destruction of the T10 vertebral body (arrow). Review of previous CT scans demonstrated that the lymphadenopathy predated the development of the vertebral metastasis. (24) Bone metastases in a 38-year-old woman with known pelvic recurrence of cervical carcinoma. Contrast-enhanced fat-suppressed T1-weighted (200/4.4; 70° flip angle) MR image of the pelvis shows enhancing, infiltrative soft tissue in the pelvis (*), a finding that is indicative of pelvic recurrence. Enhancing foci in the left ilium (arrowhead) and sacrum (arrow) are also seen, findings that are consistent with osseous metastases.
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Figures 23, 24. (23) Vertebral metastasis in a 69-year-old woman with a history of cervical carcinoma who presented for evaluation of back pain. Contrast-enhanced CT scan reveals confluent lymphadenopathy (*) adjacent to the aorta (A) and esophagus (E). The lymphadenopathy has extended posteriorly and caused destruction of the T10 vertebral body (arrow). Review of previous CT scans demonstrated that the lymphadenopathy predated the development of the vertebral metastasis. (24) Bone metastases in a 38-year-old woman with known pelvic recurrence of cervical carcinoma. Contrast-enhanced fat-suppressed T1-weighted (200/4.4; 70° flip angle) MR image of the pelvis shows enhancing, infiltrative soft tissue in the pelvis (*), a finding that is indicative of pelvic recurrence. Enhancing foci in the left ilium (arrowhead) and sacrum (arrow) are also seen, findings that are consistent with osseous metastases.
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OTHER SITES OF RECURRENCE
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A variety of relatively uncommon sites of recurrent cervical carcinoma have also been reported and include the skin and subcutaneous tissues (Fig 25), brain, meninges, heart, and breast (3, 7,8). Of these, the skin and subcutaneous tissues are involved most frequently, demonstrating metastases in up to 10% of patients with recurrent cervical carcinoma (8). In general, the remaining sites show evidence of metastases in no more than 3% of patients (3,7,8).
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Figure 25. Subcutaneous metastasis in a 47-year-old woman with cervical carcinoma. Contrast-enhanced CT scan of the pelvis shows a rounded soft-tissue focus (arrow) in the subcutaneous fat of the right buttock. This focus was not present on a CT scan obtained 6 months earlier. Percutaneous biopsy revealed squamous cell carcinoma, a finding consistent with metastatic disease.
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Abstract
INTRODUCTION
