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Japanese Journal of Clinical Oncology Advance Access originally published online on June 7, 2007
Japanese Journal of Clinical Oncology 2007 37(5):370-375; doi:10.1093/jjco/hym036
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© 2007 Foundation for Promotion of Cancer Research

Can Preoperative MRI Accurately Evaluate Nodal and Parametrial Invasion in Early Stage Cervical Cancer?

Hyun Hoon Chung1,3, Soon-Beom Kang1,3,, Jeong Yeon Cho2, Jae Weon Kim1,3, Noh-Hyun Park1,3, Yong-Sang Song1,3, Seung Hyup Kim2 and Hyo-Pyo Lee1,3

1 Department of Obstetrics and Gynecology
2 Department of Radiology
3 Cancer Research Institute, Seoul National University College of Medicine, Seoul, Korea

For reprints and all correspondence: Soon-Beom Kang, Department of Obstetrics and Gynecology, Seoul National University College of Medicine, Yongon-dong, Chongno-gu, Seoul 110-744, Korea. E-mail: chhkmj1{at}snu.ac.kr

Received November 6, 2006; accepted December 19, 2006


   Abstract
TOP
 Abstract
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
 References
 
Objective: To evaluate the diagnostic performance of magnetic resonance imaging (MRI) in the pretreatment evaluation of invasive cervical cancer especially for the parametrial invasion and lymph node (LN) involvement.

Methods: We retrospectively recruited consecutive patients with biopsy-confirmed cervical cancer who had undergone preoperative MRI and were scheduled for surgery based on clinical assessment between January 2004 and May 2006. We evaluated the diagnostic performance of MRI for the parametrial invasion and LN involvement using surgicopathologic findings as the reference standard.

Results: A total of 119 eligible patients completed preoperative and intra-operative survey, of whom 34 (28.6%) had pelvic LN metastasis and four (3.4%) had para-aortic LN metastasis histologically. The sensitivity, specificity and accuracy of MRI in detecting LN involvement by region-specific analysis were 40.5, 91.3 and 86.8% respectively. The sensitivity, specificity and accuracy of MRI in detecting parametrial invasion were 44.4, 89.1 and 88.3% respectively. The positive predictive value (PPV) of preoperative MRI for detecting region-specific LN involvement and parametrial invasion was 31.3 and 61.2%, respectively. Imaging findings of suspected parametrial invasion were not to influence the treatment decision in the study.

Conclusion: Preoperative MRI showed low PPV for detecting LN involvement and parametrial invasion in cervical cancer. Further studies are necessary to determine the cost-effectiveness of using MRI in place of conventional clinical staging tests according to clinical indication and also its use in comparison with that of integrated positron emission tomography/computed tomography.

Key Words: MRI • evaluation • cervical cancer • lymph node • parametrium


   INTRODUCTION
TOP
 Abstract
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
 References
 
Carcinoma of the uterine cervix is the second most frequently diagnosed malignancy in women worldwide and is the only major gynecologic malignancy that is staged clinically according to International Federation of Obstetrics and Gynecology (FIGO) recommendations (1). Compared with surgical staging, FIGO clinical staging has been shown to result in understaging of up to 20–30% in stage IB, up to 23% in stage IIB and almost 40% in stage IIIB, as well as overstaging of approximately 64% in stage IIIB (2–5). Subsequent surgical staging shows that clinical staging of cervical carcinomas is accurate in only approximately 60% of patients and undiagnosed lymph node (LN) metastases are a major problem (6–8).

Early stage cervical cancer can be cured at an average rate of 80% with either radical surgery or definitive radiation. LN metastasis is the most important prognostic factor in early stage cervical cancer (9–12). Accurate cervical cancer staging is thus crucial for appropriate treatment selection and treatment planning. For this reason, inaccurate assessment of LN involvement can lead to suboptimal treatment (4,5,13–16).

The greatest difficulties in the clinical evaluation of patients with cervical cancer are the assessment of parametrial and pelvic sidewall invasion, and the evaluation of LN and distant metastases. Modern cross-sectional imaging, which can assist in the evaluation of these prognostic factors, has become an important adjunct to the clinical assessment of cervical cancer (17–20). Magnetic resonance imaging (MRI) has been used to assess para-aortic and pelvic LNs in patients with cervical carcinoma. MRI is superior to computed tomography (CT) in defining tumor volume and depth of stromal invasion, parametrial invasion, and relies on size and morphologic criteria to recognize LN metastasis, but small metastatic LNs are mostly undetected (21–23).

The aim of this study was to evaluate the diagnostic performance of MRI in the pretreatment evaluation of invasive cervical cancer especially for the parametrial invasion and LN involvement, using surgicopathological findings as the reference standard.


   PATIENTS AND METHODS
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 Conflict of interest statement
 References
 
Patients
For this retrospective study, consecutive patients with biopsy-confirmed cervical cancer who were scheduled for surgery based on clinical assessment were recruited between January 2004 and May 2006. Eligible patients were cervical cancer patients scheduled to receive type II or III radical hysterectomy (RH) and pelvic lymphadenectomy (PLND) as the primary treatment and had to meet the following eligibility criteria: (i) histologically confirmed invasive carcinoma of the uterine cervix; (ii) FIGO stage IA, IB, IIA or IIB disease (24); (iii) histology of squamous cell carcinoma or adenocarcinoma or adenosquamous carcinoma or other than small cell carcinoma; (iv) no medical or surgical contra-indications to RH–PLND; (v) had no contra-indications to MRI; (vi) had no evidence of distant metastases; (vii) had an Eastern Cooperative Oncology Group (ECOG) performance status of 0–1; and (viii) written informed consent. The median interval between MRI study and surgery was 7 days (range 3–20).

Patients with any of the following conditions were excluded: (i) histology of small cell carcinoma; (ii) histologically proven metastasis to para-aortic LN (PALN) (24); (iii) ever received radiotherapy and/or chemotherapy for cervical cancer; (iv) contra-indication to the MRI procedure; (v) a previous diagnosis of cancer other than non-melanoma skin cancer; and (vi) concomitant pregnancy. Informed consent was obtained from all patients before surgery, and the study was approved by the Institutional Review Board of the Seoul National University Hospital.

Conventional Staging Workup
After histological confirmation of invasive cervical carcinoma, FIGO staging was determined on clinical data: findings from physical examination including bimanual pelvic examination, radiologic studies (chest radiography, intravenous pyelogram, barium enema), and endoscopic studies (cystoscopy, sigmoidoscopy).

MRI Scanning
MRI was performed using a Signa 1.5-T system (General Electric Medical Systems, Milwaukee, WI) with a pelvic array coil for pelvic scans and a torso phase-array coil for para-aortic scans. Magnetic resonance scans were obtained between 3 and 20 days (median, 7 days) before surgery. Scans were obtained by using the following parameters: for the pelvic region, an axial T1-weighted, fast spin-echo sequence (TR/TE, 600/10 ms; slice thickness, 5 mm; interslice gap, 2 mm; field of view, 24 cm x 24 cm; matrix, 256 x 192; echo train length, 4; three signals acquired; no fat saturation; bandwidth, 31.25 kHz); an axial T2-weighted, fast spin-echo sequence (TR/TE, 5000/68 ms; slice thickness, 3 mm; interslice gap, 1 mm; field of view, 24 cm x 24 cm, matrix, 256 x 192; echo train length, 21; four signals acquired; no fat saturation; bandwidth, 31.25 kHz); and a sagittal T2-weighted, fast spin-echo sequence (TR/TE, 5000/68 ms; slice thickness, 3 mm; interslice gap, 3 mm; field of view, 24 cm x 24 cm; matrix, 256 x 192; echo train length, 26; four signals acquired; no fat saturation; bandwidth, 31.25 kHz); and, for the para-aortic region, an axial T2-weighted, fast spin-echo sequence with 16 s of breath holding (TR/TE, 2000/68 ms; slice thickness, 8 mm; interslice gap 2 mm; field of view, 32 cm x 24 cm; matrix, 256 x 160; echo train length, 20; one signal acquired; no fat saturation; bandwidth, 31 kHz).

Classification of Lymph Node Regions
Para-aortic and pelvic LNs were classified into seven groups according to the nearest, largest artery: the para-aortic area (including right and left PALNs), both common iliac areas, both external iliac areas and both internal iliac/obturator areas (Fig. 1).


Figure 1
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  		Figure 1. Classification of pelvic and paraaortic lymph nodes. 1, paraaortic lymph nodes; 2, right common iliac lymph nodes; 3, left common iliac lymph nodes; 4, right external iliac lymph nodes; 5, left external iliac lymph nodes; 6, right internal iliac/obturator lymph nodes; 7, left internal iliac/obturator lymph nodes.

 
Surgical Technique
All patients received preoperative bowel preparation for 2 days, received prophylactic antibiotics and underwent surgery with the same instruments and techniques. Five gynecologic surgeons performed all operations. The surgeons were aware of MRI and LN findings prior to lymphadenectomy.

For all the patients, pelvic lymphadenectomy was performed systematically with dissection of all LN groups. All harvested LNs were grouped according to the name of the adjacent vessel (both common iliac arteries, both external iliac arteries, and both internal iliac and obturator arteries). For discrimination of the external iliac LN group from the internal/obturator LN group, we classified the LNs that were located parallel or anterior to the external iliac artery as the external iliac LN group, and the LNs that were located posterior to the external iliac artery and near the internal iliac or obturator artery were classified as the internal iliac/obturator LN group. The margin of LN dissection was demarcated by using surgical endoclips and this margin was confirmed by abdominal X-ray after surgery.

Image Analysis
Two experienced radiologists blinded to the results of surgery scored the MRI images by consensus. The result of a lesion observed by MRI was considered positive when a pelvic or para-aortic LN with a short-axis dimension ≥1 cm. MRI images were examined from the picture archiving and communication system (PACS). Any LN of 1 cm or a little less in length, giving an overall equivocal impression, was considered negative in the study.

Complete disruption of the cervical stromal ring with nodular or irregular tumor signal intensity extending into the parametrium was considered as parametrial invasion on T2-weighted images.

Histopathologic Evaluation
Histopathologic evaluation of parametrium and LNs were the gold standard for diagnosis. Thin sections were stained with hematoxylin and eosin and were examined microscopically by an experienced pathologist. Each LN was sliced at 3-mm intervals perpendicular to the greatest dimension to maximize the likelihood of detecting microscopic metastases.

Data Analysis
The primary aim of the protocol was to use the pooled data across sites to compare MRI and clinical FIGO staging on the basis of diagnostic performance as measured by sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and accuracy. We performed both region-specific analysis and patient-based analysis.


   RESULTS
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 Conflict of interest statement
 References
 
Patient Characteristics
A total of 157 patients were registered initially. Ten patients were not eligible because they opted for radiation therapy as definitive treatment. Twenty-eight patients were also ineligible as advanced lesions were found during subsequent evaluation such as supraclavicular LN metastasis. The remaining 119 eligible patients completed preoperative and intra-operative survey. Patient characteristics of the eligible patients are listed in Table 1.


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  		Table 1. Patient characteristics

 
Detection of Lymph Node Involvement
Of the 119 patients, 34 (28.6%) patients had pelvic LN metastasis and four (3.4%) patients had PALN metastasis histologically. We evaluated the LN status of preoperative MRI and histological results according to the classification of Fig. 1, and seven regions were compared for each patient.

The MRI scan and histologic results of patients with metastatic LNs are listed in Tables 2 and 3 enlist the accuracies of preoperative MRI according to region-specific analysis and patient-based analysis. For preoperative LN staging, sensitivity of MRI was 40.5% (region-specific analysis) and 70.6% (patient-based analysis) respectively (Table 4). MRI produced 66 false-positive interpretations in region-specific analysis, resulting in 91.3% specificity (693 of 759 lymph node regions). The specificity, NPV and accuracy for detecting metastatic LNs with MRI in region-specific analysis were superior to those of patient-based analysis in the study.


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  		Table 2. Comparison of lymph node status by preoperative MRI scan and histological results

 

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  		Table 3. Comparison of parametrial invasion by clinical staging, preoperative MRI scan and histological results

 

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  		Table 4. Accuracy of MRI in preoperative assessment of lymph node status in patients with cervical cancer

 
Detection of Parametrium Invasion
In the current study, 18 (15.1%) patients had parametrial invasion of cervical cancer. The sensitivity and NPV of MRI in the evaluation of parametrial invasion were 100% and the accuracy was 90.8% (Table 3). However, MRI considerably overestimated the parametrial invasion (PPV 62.1%). Although the specificity and NPV of clinical staging by pelvic examination were almost the same as those of MRI, the sensitivity (44.4%) and PPV (42.1%) were inferior to those of MRI.


   DISCUSSION
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
Conflict of interest statement
 References
 
The purpose of this study was to evaluate the diagnostic performance of MRI in the pretreatment evaluation of invasive cervical cancer especially for the LN involvement and parametrial invasion, using surgicopathological findings as the reference standard. Preoperative MRI showed low PPV for detecting LN involvement and parametrial invasion in cervical cancer in the study. The presence of metastatic LNs radically modifies the treatment plan and prognosis of patients with cervical cancer (4,5,15,16). In patients with locally advanced cervical cancer who were staged surgically, the 5-year survival rate with positive LNs is inferior to that with negative LNs (25), although the LN status is not considered in nor alters the FIGO staging (26).

The diagnostic efficacy of MRI in pelvic and para-aortic LN assessment is controversial. The clinical value of LN detection depends on the detection rate and NPV of negative LNs. Reinhardt et al. (27) reported a prospective surgicopathological study of patients with cervical cancer who underwent RH–PLND and had a preoperative MRI scan. The sensitivity was 73% on a patient-based analysis and the PPV was 64% on a region-specific analysis. Although the sensitivity was similar, the PPV in the current study was inferior to the results of other studies.

Imaging findings of suspected parametrial invasion did not influence the treatment decision in the study. Actually, all the patients with suspected parametrial invasion on MRI underwent RH and PLND in the study. Although sensitivity and NPV was excellent, the PPV of parametrial invasion was 62.1% in the study and there was 37.9% of overestimation. However, the physicians in the study depended more on pelvic examination than on the MRI finding regarding parametrial invasion, although the sensitivity and PPV of parametrial evaluation by pelvic examination were inferior to those by MRI.

We performed sagittal images in the equilibrium phase to obtain optimal visualization of contrast images. However, we produced only T2-weighted scans in axial sequence to the pelvis. The cross-correlation between sagittal and oblique planes is very useful for the evaluation of the parametrial invasion especially in the T2-weighted axial oblique sequence (perpendicular to the long axis of the uterus). It is probable that the low PPV and the tendency of overestimation in this study may be caused by partial volume effect, which is induced by an inappropriate slice angle.

The conventional diagnostic FIGO-recommended tests were used at high rates in the current study. Physicians performed MRI in addition to all the clinical staging tests recommended by FIGO. The high rates of usage are inconsistent with the data presented by other investigators (20,24), who reported that the use of conventional clinical staging tests had been declining and these tests were being replaced by single comprehensive morphologic imaging modalities such as MRI or CT. Moreover, there are controversies regarding the value of positron emission tomography (PET) in preoperative staging of patients with cervical cancer (28,29). Considering the current FIGO clinical staging system of cervical cancer, anatomical information rather than metabolic information would be more important in clinical decision. In the current study, clinicians used MRI as an adjunct tool for determining surgical extent. In terms of cost-effectiveness, it may not be the optimal tool and further study may be necessary.

Size criteria may predict the likelihood of LN metastasis, using a threshold value above which the node is considered metastatic. The most widely used threshold value for identifying metastatic LNs is 10 mm short-axis diameter (27,30,31). However, some LNs smaller than the threshold may harbor metastatic tumors, whereas some LNs larger than this value may be benign. In a recent study, nanoparticle-enhanced MRI was performed before and after the use of ultra-small particles of iron oxide before lymphadenectomy (32). On a region-specific analysis, the sensitivity of detecting LN metastasis was significantly better using ultra-small particles of iron oxide compared with conventional size criteria. It might be possible to postulate tumor involvement in LNs preoperatively more accurately. However, micrometastases are also likely to remain a challenge because of the special resolution of the MRI.

In conclusion, although preoperative MRI is widely used for substituting conventional staging tests, its accuracy especially in PPVs for detecting LN involvement and parametrial invasion is limited. Further studies are necessary to determine the cost-effectiveness of using MRI in place of conventional clinical staging tests according to clinical indication and also its use in comparison with that of integrated PET/CT.


   Conflict of interest statement
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
References
 
None declared.


   Acknowledgments
 
This study was supported by a grant from the Korea Health 21 R&D Project, Ministry of Health &Welfare, Republic of Korea (0412-CR01-0704-0001).


   References
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
 References
 
1 Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer (2001) 94:153–6.[CrossRef][Web of Science][Medline]

2 Vidaurreta J, Bermudez A, di Paola G, Sardi J. Laparoscopic staging in locally advanced cervical carcinoma: a new possible philosophy? Gynecol Oncol (1999) 75:366–71.[CrossRef][Web of Science][Medline]

3 LaPolla JP, Schlaerth JB, Gaddis O, Morrow CP. The influence of surgical staging on the evaluation and treatment of patients with cervical carcinoma. Gynecol Oncol (1986) 24:194–206.[CrossRef][Web of Science][Medline]

4 Lagasse LD, Creasman WT, Shingleton HM, Ford JH, Blessing JA. Results and complications of operative staging in cervical cancer: experience of the Gynecologic Oncology Group. Gynecol Oncol (1980) 9:90–8.[CrossRef][Web of Science][Medline]

5 Van Nagell JR Jr, Roddick JW Jr, Lowin DM. The staging of cervical cancer: inevitable discrepancies between clinical staging and pathologic findinges. Am J Obstet Gynecol (1971) 110:973–8.[Web of Science][Medline]

6 Ballon SC, Berman ML, Lagasse LD, Petrilli ES, Castaldo TW. Survival after extraperitoneal pelvic and paraaortic lymphadenectomy and radiation therapy in cervical carcinoma. Obstet Gynecol (1981) 57:90–5.[Web of Science][Medline]

7 Averette HE, Dudan RC, Ford JH Jr. Exploratory celiotomy for surgical staging of cervical cancer. Am J Obstet Gynecol (1972) 113:1090–6.[Web of Science][Medline]

8 Takeshima N, Yanoh K, Tabata T, Nagai K, Hirai Y, Hasumi K. Assessment of the revised International Federation of Gynecology and obstetrics staging for early invasive squamous cervical cancer. Gynecol Oncol (1999) 74:165–9.[CrossRef][Web of Science][Medline]

9 Waggoner SE. Cervical cancer. Lancet (2003) 361:2217–25.[CrossRef][Web of Science][Medline]

10 Landoni F, Maneo A, Colombo A, Placa F, Milani R, Perego P, et al. Randomised study of radical surgery versus radiotherapy for stage Ib–IIa cervical cancer. Lancet (1997) 350:535–40.[CrossRef][Web of Science][Medline]

11 Lai CH, Hong JH, Hsueh S, Ng KK, Chang TC, Tseng CJ, et al. Preoperative prognostic variables and the impact of postoperative adjuvant therapy on the outcomes of stage IB or II cervical carcinoma patients with or without pelvic lymph node metastases: an analysis of 891 cases. Cancer (1999) 85:1537–46.[CrossRef][Web of Science][Medline]

12 Tanaka Y, Sawada S, Murata T. Relationship between lymph node metastases and prognosis in patients irradiated postoperatively for carcinoma of the uterine cervix. Acta Radiol Oncol (1984) 23:455–9.[Web of Science][Medline]

13 Downey GO, Potish RA, Adcock LL, Prem KA, Twiggs LB. Pretreatment surgical staging in cervical carcinoma: therapeutic efficacy of pelvic lymph node resection. Am J Obstet Gynecol (1989) 160:1055–61.[Web of Science][Medline]

14 Potish RA, Twiggs LB, Okagaki T, Prem KA, Adcock LL. Therapeutic implications of the natural history of advanced cervical cancer as defined by pretreatment surgical staging. Cancer (1985) 56:956–60.[CrossRef][Web of Science][Medline]

15 Kupets R, Covens A. Is the International Federation of Gynecology and Obstetrics staging system for cervical carcinoma able to predict survival in patients with cervical carcinoma? An assessment of clinimetric properties. Cancer (2001) 92:796–804.[CrossRef][Web of Science][Medline]

16 Chung CK, Nahhas WA, Zaino R, Stryker JA, Mortel R. Histologic grade and lymph node metastasis in squamous cell carcinoma of the cervix. Gynecol Oncol (1981) 12:348–54.[CrossRef][Web of Science][Medline]

17 Hricak H, Lacey CG, Sandles LG, Chang YC, Winkler ML, Stern JL. Invasive cervical carcinoma: comparison of MR imaging and surgical findings. Radiology (1988) 166:623–31.[Abstract/Free Full Text]

18 Subak LL, Hricak H, Powell CB, Azizi L, Stern JL. Cervical carcinoma: computed tomography and magnetic resonance imaging for preoperative staging. Obstet Gynecol (1995) 86:43–50.[CrossRef][Web of Science][Medline]

19 Kim SH, Choi BI, Han JK, Kim HD, Lee HP, Kang SB, et al. Preoperative staging of uterine cervical carcinoma: comparison of CT and MRI in 99 patients. J Comput Assist Tomogr (1993) 17:633–40.[Web of Science][Medline]

20 Russell AH, Shingleton HM, Jones WB, Fremgen A, Winchester DP, Clive R, et al. Diagnostic assessments in patients with invasive cancer of the cervix: a national patterns of care study of the American College of Surgeons. Gynecol Oncol (1996) 63:159–65.[CrossRef][Web of Science][Medline]

21 Wagenaar HC, Trimbos JB, Postema S, Anastasopoulou A, van der Geest RJ, Reiber JH, et al. Tumor diameter and volume assessed by magnetic resonance imaging in the prediction of outcome for invasive cervical cancer. Gynecol Oncol (2001) 82:474–82.[CrossRef][Web of Science][Medline]

22 Yang WT, Lam WW, Yu MY, Cheung TH, Metreweli C. Comparison of dynamic helical CT and dynamic MR imaging in the evaluation of pelvic lymph nodes in cervical carcinoma. Am J Roentgenol (2000) 175:759–66.[Abstract/Free Full Text]

23 Scheidler J, Hricak H, Yu KK, Subak L, Segal MR. Radiological evaluation of lymph node metastases in patients with cervical cancer. A meta-analysis. JAMA (1997) 278:1096–101.[Abstract/Free Full Text]

24 Hricak H, Gatsonis C, Chi DS, Amendola MA, Brandt K, Schwartz LH, et al. Role of imaging in pretreatment evaluation of early invasive cervical cancer: results of the intergroup study American College of Radiology Imaging Network 6651–Gynecologic Oncology Group 183. J Clin Oncol (2005) 23:9329–37.[Abstract/Free Full Text]

25 Lanciano RM, Corn BW. The role of surgical staging for cervical cancer. Semin Radiat Oncol (1994) 4:46–51.[CrossRef][Medline]

26 Kamura T, Tsukamoto N, Tsuruchi N, Saito T, Matsuyama T, Akazawa K, et al. Multivariate analysis of the histopathologic prognostic factors of cervical cancer in patients undergoing radical hysterectomy. Cancer (1992) 69:181–6.[CrossRef][Web of Science][Medline]

27 Reinhardt MJ, Ehritt-Braun C, Vogelgesang D, Ihling C, Hogerle S, Mix M, et al. Metastatic lymph nodes in patients with cervical cancer: detection with MR imaging and FDG PET. Radiology (2001) 218:776–82.[Abstract/Free Full Text]

28 Chou HH, Chang TC, Yen TC, Ng KK, Hsueh S, Ma SY, et al. Low value of [18F]-fluoro-2-deoxy-D-glucose positron emission tomography in primary staging of early-stage cervical cancer before radical hysterectomy. J Clin Oncol (2006) 24:123–8.[Abstract/Free Full Text]

29 Choi HJ, Roh JW, Seo SS, Lee S, Kim JY, Kim SK, et al. Comparison of the accuracy of magnetic resonance imaging and positron emission tomography/computed tomography in the presurgical detection of lymph node metastases in patients with uterine cervical carcinoma: a prospective study. Cancer (2006) 106:914–22.[CrossRef][Web of Science][Medline]

30 Lin WC, Hung YC, Yeh LS, Kao CH, Yen RF, Shen YY. Usefulness of (18)F-fluorodeoxyglucose positron emission tomography to detect para-aortic lymph nodal metastasis in advanced cervical cancer with negative computed tomography findings. Gynecol Oncol (2003) 89:73–6.[CrossRef][Web of Science][Medline]

31 Grigsby PW, Siegel BA, Dehdashti F. Lymph node staging by positron emission tomography in patients with carcinoma of the cervix. J Clin Oncol (2001) 19:3745–9.[Abstract/Free Full Text]

32 Rockall AG, Sohaib SA, Harisinghani MG, Babar SA, Singh N, Jeyarajah AR, et al. Diagnostic performance of nanoparticle-enhanced magnetic resonance imaging in the diagnosis of lymph node metastases in patients with endometrial and cervical cancer. J Clin Oncol (2005) 23:2813–21.[Abstract/Free Full Text]


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