British Journal of Radiology (2005) 78, S73-S85
© 2005 British Institute of Radiology
doi: 10.1259/bjr/66333608
MR imaging in cervical cancer: seeing is believing
The 2004 Mackenzie Davidson Memorial Lecture
R H Reznek, FRCP, FRCR
1 and
A Sahdev, MRCP, FRCR
2
1 Cancer Imaging, St Bartholomew's Hospital, West Smithfield, London EC1A 7BE and 2 Department of Clinical Radiology, Homerton University Hospital, Homerton Row, London E9 6SR, UK
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Introduction
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Carcinoma of the cervix remains a formidable problem with 471 000 cases estimated to have occurred worldwide in 2000 and is the third most common malignancy after breast and colorectal cancer in women [1]. Between 1990 and 1992, 11 200 new cases of invasive cervical cancer were reported in the UK, occurring predominantly in women between the ages of 30 years and 44 years [2]. Younger women tend to present with earlier stages of the disease as a consequence of the United Kingdom National screening program (Figure 1
). The rate and mortality of the disease can be related to the Carstairs' deprivation score (Figure 2). These demographics of cervical cancer are relevant to the role of MRI.
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Figure 1. Variation in TNM stage with age group for cervical cancer cases in the West Midlands. Cancers diagnosed 1991–1995. (Cancer Research UK [34]). * indicates total number of cases in each age group.
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Figure 2. The relationship of incidence and mortality of cervical cancer against social deprivation score. (Cancer Research UK [34]).
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Over the past several years, overwhelming evidence has accumulated for the role of MRI in the management of these patients. It is now an integral part of local staging; is important in monitoring response and detection of recurrence, demonstrating complications of the disease itself and of the treatment, determining the feasibility of uterus preserving surgery and in planning radiotherapy. This presentation will summarise our experience in using MRI in cervical cancer for over a decade and the evidence on which its utility is based.
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Staging
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Worldwide, the most widely used staging system for cervical cancer is the Federation Internationale de Gynécologic et Obstétrique (FIGO) classification. The TNM classification is essentially based on the same criteria (Table 1). In early carcinoma of the cervix, the key decision is whether or not the tumour has extended into the parametrium. In disease localized to the cervix the treatment is surgical [3]. Worldwide, and particularly in the areas of the world where the prevalence of cervical cancer is high, this assessment is made clinically. The FIGO staging is entirely clinical, relying on physical examination, colposcopy, cystoscopy, sigmoidoscopy and radiography, sometimes including intravenous urography. However, it is generally acknowledged that depending on the stage of the disease, clinical staging shows errors of 20–39% when compared with histology [4, 5]. Thus in early stage tumours, the key role of MRI is in the detection of parametrial extension of tumour which renders the tumour Stage IIB or above. The performance of MRI in staging these tumours was evaluated in a meta-analysis by Bipat et al [6]. MRI demonstrated the cervical cancer with a sensitivity of 93% and an overall tumour staging accuracy of 86%. By comparison, clinical FIGO staging performed poorly with an overall accuracy of only 47% [6]. Based on these studies, clinical staging need not limit the treatment plan and MRI or other diagnostic results can be used in planning therapy [7].
The key feature when staging these early tumours is the circumferential preservation of normal cervical stroma around the tumour. In our experience and in that of others, preservation of normal low T2 signal cervical stroma around the intermediate T2 signal intensity tumour has a very high negative predictive value exceeding 96% for parametrial invasion [8–10] (Figure 3). As interruption of this low signal stromal line indicates full thickness tumour invasion either with or without parametrial invasion (Figure 4) the positive predictive value for parametrial invasion is lower, between 82% and 86% [11, 12]. The assessment of circumferential cervical stroma is best performed on oblique axial images of the cervix, performed perpendicular to the long axis of the cervix (Figure 3a).
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Figure 3. (a) T2 weighted sagittal fast-spin-echo scan showing a large cervical tumour with high T2 signal. The oblique scan line demonstrates the plane that is required to obtain a true axial representation of the cervix as in Figure 3b . (b) Oblique T2 weighted fast-spin-echo scan. There is preservation of the normal low T2 signal intensity of the cervical stoma (arrows). The preservation of this line has a negative predictive value exceeding 96 for parametrial invasion.
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Figure 4. (a) T2-weighted sagittal fast-spin-echo scan demonstrating an endocervical tumour (arrow). (b) T2 weighted oblique scan demonstrating the loss of the normal low T2 cervical stroma on the right side (arrow) indicating parametrial invasion.
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Pitfalls in staging
An awareness of the more common errors encountered in assessing parametrial spread can improve the diagnostic performance of MRI. In our experience one of the most common causes of confusion is the presence of a large exophytic tumour where the vaginal wall is misinterpreted as the circumferential cervical stroma (Figure 5). Other pitfalls in staging early tumours include cystic tumours, infiltration of the upper vaginal wall, collapsed vaginal walls, concurrent disease such as endometriosis or cysts, post biopsy haemorrhage and inflammation, all resulting in apparent parametrial invasion (Figures 6 and 7).
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Figure 5. (a) T2 weighted sagittal fast-spin-echo scan demonstrating a large endocervical and exophytic tumour. The exophytic component of the tumour extends into the proximal vagina and is surrounded by the vaginal wall. (b) T2 weighted oblique scan at the level of the proximal vagina and the exophytic component of the cervical tumour (dashed scan line). The vaginal walls surrounding the cervical tumour have low signal intensity on T2 weighted images (arrows). These can be misinterpreted as cervical stroma and careful correlation of oblique scans against sagittal T2 weighted scans is recommended to avoid this pitfall. (c) T2 weighted oblique scan at the level of the cervix (continuous scan line) demonstrating the loss of normal cervical stroma suggesting parametrial extension (arrows). (d) Pathological specimen orientated in a longitudinal plane, demonstrating the large central cervical tumour extending into the proximal vagina but also extending into the parametrium.
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Figure 6. (a) T2 weighted oblique fast-spin-echo scan showing a small carcinoma in the anterior lip of the cervix (star). Anteriorly there is apparent extension of tumour into the fat space between the cervix and bladder wall (arrow). (b) T2 weighted sagittal fast-spin-echo scan shows the cervical cancer (star). The anterior wall of the vagina is folded and collapsed resulting in the appearance of extracervical tumour.
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Figure 7. T2 weighted fast-spin-echo sagittal scan showing a large exophytic mass occupying the entire cervix. The appearances are indistinguishable from cervical cancer but histologically this was endometriosis with a small focus of carcinoma.
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In advanced tumours, staging depends on demonstrating involvement of adjacent pelvic structures, pelvic side walls including the levator ani muscles, ureters and vaginal wall. The performance of MRI in the detection of bladder and rectal mucosal invasion has been extensively studied. The meta analysis by Bipat et al showed MRI had a sensitivity of 91% for bladder invasion and 75% for rectal invasion [6]. When the bladder is involved, normal low T2 signal of bladder wall is replaced by the intermediate T2 signal of tumour. The tumour may be seen invading the mucosa (Figure 8) or a hyperintense T2 signal intensity band may indicate bullous oedema of the bladder wall. In our own experience of 112 patients, by adopting a low threshold for bladder and rectal invasion, MRI had a negative predictive value of 100% thereby potentially negating the need for routine staging cystoscopy and sigmoidoscopy [13]. In a study by Taylor et al [14], in a cohort of radiotherapy patients, the involvement of the bladder mucosa had a strong negative association with overall survival rates (p=0.05) [8]. Direct infiltration of the rectal wall is uncommon due to the intervening pouch of Douglas but invasion usually occurs via the utero-sacral ligaments (Figure 9)] [14].
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Figure 8. T2 weighted axial fast-spin-echo scan showing a large cervical tumour with full thickness bladder wall and mucosal invasion.
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Figure 9. T2 weighted axial fast-spin-echo scan showing an extensive infiltrative cervical tumour. There is invasion of the left utero-sacral ligaments and invasion of the rectal wall (arrows).
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Nodal staging
Within the pelvis, cervical cancer spreads first to the parametrial nodes, then to the obturator and iliac nodes. The presence of nodal disease has significant prognostic and treatment consequences. The 5-year survival for node positive patients is 39–54% compared with 67–92% in patients without nodal involvement [15, 16]. In the study by Taylor et al [14], all pelvic lymph nodes larger than 5 mm in their short axis were documented within the pelvis and para-aortic region and correlated with survival. The results showed that the presence of lymph nodes larger than 1 cm in short axis, significantly lowered the disease-free and disease-specific survival rates. However, the presence of nodes between 8 mm and 9 mm had a similar outcome as patients with unenlarged nodes. The study had a predominance of stage IIB and IIIB tumours and relatively few stage I tumours [14]. Clearly then, in higher stage tumours, the detection of nodes larger than 1 cm in short axis is important for prognosis and also for planning radiotherapy treatment fields.
In lower stage tumours the involvement of any nodes, irrespective of size, is important as it excludes curative surgery changing the treatment to either chemoradiotherapy alone or debulking surgery and neo-adjuvant chemoradiotherapy. For smaller nodal metastasis the sensitivity and specificity of MRI is poor as it relies on a morphological change in size or signal intensity. The sensitivity and specificity of MRI for nodes greater than 10 mm in short axis has been reported to be between 62–89% and 88–91%, respectively [17, 18].
For the detection of nodal metastases the use of MRI contrast agents using ultra small iron oxide particles (USIOPs) has recently been evaluated (Figures 10 and 11). USIOPs are an intravenously administered lymph node-specific contrast agent. After intravenous administration, the contrast agent extravasates into the interstitial space before being transported into lymph nodes where it is taken up by macrophages. The presence of USIOPs within the macrophages results in loss of signal within the normal lymph nodes on iron sensitive T2 and T2* sequences. Lymph nodes with metastatic deposits do not lose signal or have patchy loss of signal on the T2 or T2* sequences. Our experience with 44 patients is summarised in Table 2 [19]. This shows that although the specificity and positive predictive value (PPV) have not changed significantly, the sensitivity and the negative predictive value (NPV) have increased dramatically to 91–100% and 96–100%, respectively.
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Figure 10. (a) T2* weighted axial scan showing a 10 mm external iliac lymph node (arrows) prior to the administration of ultra small iron oxide particles (USIOPs). (b) T2* weighted axial scan following administration of USIOPs showing the 10 mm left external iliac node losing all central signal after administration of the USIOPs (arrow). The capsule of the node (arrowhead) and hilum (curved arrow) are clearly seen. (c) Histological specimen of the same lymph node showing normal macrophages through out the node without evidence of metastatic tumour deposits.
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Monitoring response and detection of recurrence
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Approximately 30% of women treated for invasive carcinoma of the cervix die of residual or recurrent disease. The identification of recurrent disease is important as secondary treatment with pelvic exenteration or further chemoradiotherapy has a 5-year survival rate of 82% in early recurrent disease. Pelvic exenteration is used in young women with low co-morbidity with only a central pelvic recurrence without peritoneal disease, vessel encasement, involvement of the pelvic side wall or nodal metastases [20, 21]. We have recently evaluated the MR appearances of recurrent cervical cancer in 45 patients of whom 78% recurred within 1 year following treatment. In patients receiving radiotherapy, 67% of the recurrences were in the cervix whilst 87% of post-surgical recurrences were in the vaginal vault [22]. An important finding in this study was that in 85% of cases the recurrent disease spread to the parametrium leaving only 13% in whom the parametrium was entirely free of disease.
For recurrent pelvic disease the sensitivity of MRI is 90% and has been shown to be comparable with fluorodeoxyglucose positron emission tomography (FDG-PET) [23]. However, the performance of MRI versus FDG-PET in detecting distant disease in the abdomen and chest is difficult to evaluate as routine MRI scans of the chest are not performed. Consequently the sensitivity of FDG-PET in detecting distant disease is higher as FDG-PET images the entire body in one acquisition [23]. In our experience MRI has also proved of value in monitoring response following radiotherapy, particularly in the early detection of recurrent disease (Figure 12).
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Figure 12. (a) T2 weighted sagittal fast-spin-echo sequence demonstrating recurrent disease in the posterior lip of the cervix after primary radiotherapy (arrow). (b) T2 weighted sagittal fast-spin-echo sequence demonstrating early central recurrence (arrow) after hysterectomy and bilateral salphingo-oopherectomy.
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Recurrence in unusual sites and at the edge of radiotherapy fields has been demonstrated in 15% and 13% of patients, respectively [22]. Disease outside and at the edge of the radiotherapy fields results in mass lesions in the perineum, the lower abdomen and in muscle (Figures 13 and 14).
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Figure 13. T2 weighted axial fast-spin-echo sequence showing a large recurrent mass (arrows) within the right iliacus muscle extending into the right sacral neural foraminae.
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Figure 14. T2 weighted fast-spin-echo sagittal sequence showing a recurrent perineal mass outside the field of radiotherapy. The cervix and uterus are atrophic in keeping with radiotherapy changes.
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Complications (including fistulae)
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MRI is of value in patients undergoing radiotherapy treatment to distinguish the complications and effects of treatment from recurrent disease. The effects of radiotherapy on small bowel, bladder, bone and muscle are well documented [24, 25]. Among the most devastating complications is the formation of vaginal fistulae which can occur as a result of recurrent disease or radiotherapy. MR has previously been shown to be highly sensitive and specific in the assessment of perianal fistulae. Encouraged by this we conducted a prospective study of 21 patients suspected of having vaginal fistulae. MR detected 15 of the 16 fistulae confirmed at surgery or examination under anaesthesia (EUA). The fistula not identified on MR was in fact a sinus track at surgery. MRI consistently identified those cases in which the fistulae were due to recurrence and those in which the radiotherapy effects resulted in fistulae (Figures 15 and 16). Based on our results we have concluded that MRI is accurate in demonstrating the course, extent and complexity of vaginal fistulae, and in showing associated active or recurrent disease [26].
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Figure 15. Sagittal short tau inversion recovery (STIR) sequence demonstrating a vesico-vaginal fistula (arrow). Within the vaginal walls there is irregular thickening (star). Biopsy of these areas and in the site of the fistula showed recurrent cervical cancer.
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Figure 16. (a) T2 weighted sagittal fast-spin-echo scan demonstrating a very large cervical cancer invading the posterior bladder wall (arrow). (b) T2 weighted sagittal scan demonstrating a very large vesico-vaginal fistula which developed after radiotherapy at the site of the patient's primary cervical cancer. Bullous oedema is also noted affecting the bladder wall (star). Multiple biopsies of the vaginal wall and bladder revealed no recurrent disease.
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Predicting feasibility of uterus-conserving surgery
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One of the major roles established for the use of MRI is in predicting the proximal extension of the tumour and thereby predicting the feasibility for trachelectomy. In this procedure the tumour-bearing cervix is removed and then re-anastamosed to the vagina with the addition of a cerclage suture to maintain isthmic competency during pregnancy (Figure 17). In our institution the technique is performed vaginally with laparoscopic lymph node dissection [27]. The purpose of trachelectomy is to maintain reproductive function in young women presenting with early stage 1 carcinoma of the cervix. The proximal end of the tumour should be 1 cm or more distal to the internal os. Clinically the level of the internal os cannot be accurately established by the examining gynaecologist and therefore, this has to be assessed by MRI. We have assessed the performance of MRI in predicting the proximal extent of cervical tumours [28]. This series showed that in predicting the involvement of the internal os by tumour, MRI had a sensitivity of 100%, specificity of 96% and a positive predictive value of 83%. MRI is, therefore, a reliable method of determining proximal extension of cervical cancer into the internal os and thus predicting the suitability for fertility-conserving surgery.
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Figure 17. (a) Schematic diagram showing the region of the cervix resected during trachelectomy. (b) After removal of the tumour-bearing cervix, the uterus and vagina are re-anastamosed. (c) Sagittal view post-trachelectomy showing the location of the cerclage suture (arrow).
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More recently, the importance of proximal extension of tumour has also been shown in patients with higher stage disease undergoing radiotherapy. In a study of 70 patients by Narayan et al [29] the presence of proximal extension as seen on MRI increased the probability of nodal metastases to 75% as opposed to 11% in patients without proximal extension. The nodal metastases were considered involved with tumour on FDG-PET criteria. The presence of nodal metastases had a significant negative association with disease-specific and disease-free survival [29]. Proximal extension is therefore an important feature in predicting prognosis for patients with higher stage carcinomas.
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Follow-up post-trachelectomy
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We have also used MRI to monitor patients following trachelectomy [30]. It is important to be aware of the normal post-operative appearances and to be able to discriminate between normal appearances and recurrent disease. In our experience we have observed three important appearances after trachelectomy that should be recognized as normal and not recurrent disease. In 56% of the patients there was a posterior extension of the vaginal wall appearing as a neo-fornix (Figure 18). In 6% diffuse thickening of the vaginal wall was present up to 1 year after surgery and slowly resolved without treatment. Thirdly, 4% of patients had slowly resolving haematomas in the vaginal wall. Suture artefacts also occur from the anastamotic and cerclage sutures used during the procedure. To date, these have not limited the diagnostic ability of the MRI. Pelvic lymphocoeles, concurrent benign disease (endometriosis and adenomyosis) were also common findings. Trachelectomy is of course performed to preserve fertility. In our institution to date there have been 30 successful pregnancies after 90 trachelectomies. Continuing follow-up of the cervical cancer during pregnancy is possible on MRI.
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Figure 18. T2 weighted sagittal fast-spin-echo scan demonstrating a soft tissue posterior to the anastamosis. This is normal vaginal wall and represents a "neo-fornix".
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Planning radiotherapy
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In recent years the role of MRI has increasingly been realised in planning radiotherapy. The accuracy of MRI tumour volume measurements has been well established making it ideal for directing radiotherapy to the affected sites and reducing radiation injury to small and large bowel and the bladder [11, 28, 31]. Conventional radiotherapy is still used in many centres in the UK. This relies on two lateral fields placed as vertical lines, posteriorly through the S2/3 intervertebral joints and anteriorly midway through the pubic symphysis. Placement of these lateral portals relies on the assumption that tumour-bearing cervix lies within the lateral fields. However, as Figure 19 demonstrates, the lateral fields may underestimate and also overestimate the required field. In our experience and that of others, when using image guidance the lateral fields were adjusted in at least 27% of the patients [32, 33]. This has led to the conclusion that when treating carcinoma of the cervix standard protocols do not apply and the placement of the lateral fields should be based on morbid anatomy provided by MRI.
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Figure 19. (a) T2 weighted sagittal scan with the anterior (midway through the pubic symphysis) and posterior (S2/3 intervertebral joint) radiotherapy limits marked as solid lines. There is a large tumour in the cervix and based on the normal lateral fields, the tumour would be under treated as the uterine fundus lies outside the anterior field. (b) T2 weighted sagittal scan with the anterior and posterior radiotherapy limits marked as solid lines. The tumour-bearing cervix lies centrally and the lateral margins can be narrowed to avoid radiation to vital pelvic structures without under treating the cervical cancer.
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More recently, three-dimensional (3D) treatment planning is being used often with intensity-modulated radiotherapy (IMRT). Here the tumour and nodes are tracked out on CT and the radiotherapy doses are delivered in a more focused way to the affected tissues only. This allows a greater dose delivery to the affected sites but also reduces the radiation to unaffected pelvic structures limiting toxicity. The present system of IMRT relies on measurements of the gross tumour volume (GTV) on CT. However, the relationship between the measurements of GTV on MRI and that on CT is unclear and may introduce significant errors of measurement. At present, in our experience, co-registration of CT and MRI GTV show significant differences (Figure 20a,b). This is the subject of ongoing research.
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Figure 20. (a) Non-contrast CT scan of the pelvis at the site of the cervical cancer. The estimated gross tumour volume map has been drawn in white. (b) T2 weighted axial fast-spin-echo scan with the gross tumour volume map drawn in yellow. (c) The CT and MRI scans are co-registered and show the two gross tumour volume maps are significantly different. Radiotherapy, usually based on the CT map, appears to have overestimated the gross tumour volume.
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Conclusion
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Over the past several years a substantial body of evidence has accumulated to establish the role of MRI in the management of patients with cervical cancer. Consequently it now has an established role in staging the primary tumour, monitoring response to treatment, detecting complications and recurrence, and in planning radiotherapy. It has played a vital role in the development of fertility-sparing surgery in young women with cervical cancer. The evidence for its value is now overwhelming. Specialist gynaecologists and clinical oncologists together with radiologists, by "seeing" its impact on routine management, have come to "believe" in its indisputable role in cervical cancer.
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Introduction
Staging
