Staging of uterine cervical cancer with MRI: guidelines of the ...

Eur Radiol (2011) 21:1102–1110 

DOI 10.1007/s00330-010-1998-x 

UROGENITAL 

Staging of uterine cervical cancer with MRI: guidelines 

of the European Society of Urogenital Radiology 

Corinne Balleyguier & E. Sala & T. Da Cunha & A. Bergman & B. Brkljacic & F. Danza & 

R. Forstner & B. Hamm & R. Kubik-Huch & C. Lopez & R. Manfredi & J. McHugo & 

L. Oleaga & K. Togashi & K. Kinkel 

Received: 27 July 2010 /Revised: 29 September 2010 /Accepted: 1 October 2010 /Published online: 10 November 2010 

# European Society of Radiology 2010 

Abstract Objective: To design clear guidelines for the 

staging and follow-up of patients with uterine cervical 

cancer, and to provide the radiologist with a framework for 

use in multidisciplinary conferences. Methods: Guidelines 

for uterine cervical cancer staging and follow-up were 

defined by the female imaging subcommittee of the ESUR 

C. Balleyguier (*) 

Radiology Department, Institut Gustave Roussy, 

39, rue Camille Desmoulins, 

94805 Villejuif, Cedex, France 

e-mail: corinne.balleyguier@igr.fr 

E. Sala 

Radiology Department, Addenbrooke’s Hospital, 

Cambridge, UK 

T. Da Cunha 

Radiology Department, Instituto Português de Oncologia de 

Lisboa Francisco Gentil, 

R. Prof. Lima Basto, 

Lisbon, Portugal 

A. Bergman 

Department of Radiology, Uppsala University Hospital, 

Uppsala, Sweden 

B. Brkljacic 

Department of Diagnostic and Interventional Radiology, 

University Hospital “Dubrava”, 

Zagreb, Croatia 

F. Danza 

Dipartimento di Bioimmaginie scienze radiologiche, Università 

Cattolica del S. Cuore, 

Rome, Italy 

R. Forstner 

Zentralröntgeninstitut, LandesklinikenSalzburg, 

Salzburg, Austria 

(European Society of Urogenital Radiology) based on the 

expert consensus of imaging protocols of 11 leading 

institutions and a critical review of the literature. Results: 

The results indicated that high field Magnetic Resonance 

Imaging (MRI) should include at least two T2-weighted 

sequences in sagittal, axial oblique or coronal oblique 

B. Hamm 

Department of Radiology, Charité Humboldt Universität Berlin, 

Berlin, Germany 

R. Kubik-Huch 

Institut Radiologie Kantonsspital Baden, 

Baden, Germany 

C. Lopez : R. Manfredi 

Department of Radiology, “A. Gemelli” University Hospital, 

Rome, Italy 

J. McHugo 

Department of Radiology, Birmingham Women’s Hospital, 

Birmingham, UK 

L. Oleaga 

Radiology Department, Hospital Clinic, 

C/Villaroel 170, 

Barcelona, Spain 

K. Togashi 

Department of Diagnostic Imaging and Nuclear Medicine, Kyoto 

University Graduate School of Medicine, 

Kyoto, Japan 

K. Kinkel 

Institut de radiologie, Clinique des Grangettes, 

Chêne-Bougerie/Geneva, Switzerland

Eur Radiol (2011) 21:1102–1110 1103 

orientation (short and long axis of the uterine cervix) of the 

pelvic content. Axial T1-weighted sequence is useful to 

detect suspicious pelvic and abdominal lymph nodes, and 

images from symphysis to the left renal vein are required. 

The intravenous administration of Gadolinium-chelates is 

optional but is often required for small lesions (

1104 Eur Radiol (2011) 21:1102–1110 

Table 2 Proposed protocol for MRI in cervical cancer staging and evaluation 

• Optional use of fasting, Antiperistaltic IV injection, or vaginal/rectal sonographic gel opacification 

• Axial T2w sequence, without a fat suppression : pelvis and abdomen (renal hilum) : 5 mm / 0.5 (pelvis), 6 mm / 1 mm (abdomen) ; matrix> 

400×400 

• Sagittal T2w sequence without a fat suppression : pelvis 5 mm / 0.5 (pelvis) ; matrix>400×400 

• Coronal oblique T2w perpendicular to the cervix, thin slices (4 mm/0.4 mm) ; matrix>400×400 

• Optional: in case of small lesions, not well depicted on T2w images, and after treatment. 

◦ Sagittal 3D T1w dynamic sequences after gadolinium chelates injection : one native and 4 post contrast (total 5 scans with a total acquisition 

time of about 5 mn) 

◦ DWI sequences 

the internal cervical os (>1 cm). In order to achieve maximal 

staging accuracy by means of MRI, it is essential to ensure 

adequate patient preparation, optimal imaging sequences and 

adequate reporting expertise. Therefore, the female pelvis 

subcommittee of the European Society of Urogenital 

Radiology (ESUR) formed a working group to establish 

technical guidelines for uterine cervical cancer staging with 

MRI based on extended clinical practice. 

Material and methods 

MRI protocols for staging of cervical cancer were collected 

from eleven European Institutions. Inclusion criteria to 

participate in the guideline process were: to be a member of 

the European Society of Urogenital Radiology (ESUR) and to 

perform at least ten MRI examinations per year for staging 

biopsy-proven cervical carcinoma. Members of the ESUR are 

experts in gynaecological imaging, especially in pelvic MRI. 

The questionnaire contained the following information: patient 

preparation, magnet field strength, type of coil, type of 

sequence with detailed geometry and contrast information, 

such as FOV, matrix scan and reconstruction, slice thickness, 

gap, orientation, saturation bands, 2D versus 3D sequence, TR/ 

TE, use of number of acquisitions, number and lengths of 

dynamic sequences, use of bolus intravenous (IV) injection and 

subtraction techniques and use of diffusion weighted imaging 

(DWI) sequences. In addition, published literature between 

1999 and 2010 was reviewed through a Medline literature 

search of abstracts in the English language of studies in human 

subjects, including the following key words: “Uterine neoplasm(s) 

AND MR imaging” and “Uterine cervical carcinoma 

AND MR imaging.” Articles that did not include technical 

details matching the information requested in the questionnaire 

were excluded. The details were entered in an excel sheet and 

the results were discussed and divided in topics with agreement 

and disagreement. Topics with disagreement were compared to 

the literature. Experts in favour of one technical option were 

asked to support their views using data from the literature. 

These were subsequently discussed by an expert panel. The 

collected data from the ESUR member institution was 

compared to the data from the literature which took into 

consideration year of publication, number of cases and 

performance of the technique. When technical details varied 

and no published work on performance was found, the subject 

wasdiscussedandresolvedinconsensusbasedonthemajority 

of participating members. Members of the group met twice a 

year during a 2-year period and were asked to apply technical 

recommendations issued after the first two meetings during the 

year before the meetings in year 2 in order to allow further 

discussion and the issue of final recommendations in consensus. 

Validation of the manuscript has been done collegially with 

the agreement of the ESUR committee. 

Results 

Indications for MRI in uterine cervical cancer 

All the eleven ESUR members recommend MRI for staging 

of tumours stage 1B1 and over or smaller tumours if 

trachelectomy is being considered. They also all recommended 

MRI for treatment follow-up (after brachytherapy 

and chemoradiation therapy) and detection of tumour 

recurrence. There was no consensus among 11 ESUR 

participants regarding the MRI time-delay after treatment. 

This varied from 3 weeks to 6 months with the majority 

recommending MRI 3–6 months after completion of 

chemoradiation therapy and brachytherapy. Similarly, there 

was no consensus on the frequency of follow-up. Some 

ESUR members perform yearly follow-up MRI for 5 years 

and some only if there are symptoms of recurrence. Three 

members use PET/CT routinely as complementary to MRI 

staging, 5 only if there are indeterminate lymph nodes on 

MRI and 2 only before salvage therapy. 

Technical requirements for MRI in uterine cervical cancer 

Among the eleven ESUR members, 6 worked with a 1.5 T 

magnet, 1 with a 3.0 T magnet and 4 members with both 1.5 

and 3.0 T magnet, Most of the published studies in the 

literature use a 1.5 T magnet. There are only a few published

Eur Radiol (2011) 21:1102–1110 1105 

studies using a 3 T MRI, showing very promising results in 

cervical cancer [6]. At 3 T, spatial resolution is improved, 

allowing accurate local staging and detection of a residual 

tumour after treatment [6]. At 3.0-T imaging, mean tumour 

signal-to-noise ratios, mean cervical stroma signal-to-noise 

ratios, and mean tumour-to-cervical stroma contrast-to-noise 

ratios are higher than those at 1.5-T imaging. Nevertheless, 

image homogeneity at 3.0-T imaging seems inferior to that at 

1.5-T imaging. In recent published studies, even if imaging 

quality seems to be higher at 3 T, accuracy seems to be 

equivalent at 1.5 T and 3 T (6). 

a. Patient Preparation 

There was no consensus among the 11 ESUR members or 

in the literature regarding the type of preparation before pelvic 

MRI. Nevertheless, different types of patient preparations 

have been suggested in order to improve the quality of the 

examination. Several authors proposed a 6 h fast before MRI 

[7, 8] others an IV or intramuscular (IM) injection of 

antiperistaltic agent [9] or vaginal/rectal opacification with 

sterile gel [10]. The use of an antiperistaltic agent seems to 

be the most efficient way to limit bowel motion artifacts. An 

intramuscular injection of an antiperistaltic agent is used (1 

mg glucagon; (Glucagen ®, Novo Nordisk ® ; Bagsværd ; 

Denmark) or 20 mg butyl-scopolamine (Buscopan ® ; 

Boehringer Ingelheim GmbH ; Ingelheim, Germany) unless 

contraindicated (e.g., diabetes or pheochromocytoma) to 

decrease peristalsis artifacts. In the ESUR group, only 50% 

of the experts included combined fasting and antiperistaltic 

agents in their patient preparation protocol. Seven ESUR 

centres use an antiperistaltic agent routinely before MRI 

examination (4 use IV injection and 3 use IM injection) 

whereas four centres do not use an antiperistaltic agent. 

Bladder must be half filled in order to improve lesion 

visibility without changing anatomy. Vaginal opacification 

with gel yielding high signal intensity on T2 weighting may 

be useful in case of suspicion of tumour extension into the 

vagina in order to differentiate FIGO IIA from FIGO IB 

tumour, particularly in the posterior vaginal fornix [10]; 

however only one ESUR centre uses a vaginal opacification 

routinely and two others only if there is a suspicion of 

posterior fornix invasion at physical examination. Therefore, 

the use of intraluminal (vagina/rectum) contrast agents 

before the MRI staging of uterine cervical carcinoma 

remains optional. 

b. Use of Intravenous Contrast Medium 

There is wide variation among the 11 ESUR members and 

in the literature regarding the use of IV contrast medium for 

cervical cancer staging. Seven of the 11 ESUR members use 

IV contrast medium routinely for staging of cervical cancer 

and identification of small tumours, one uses it only for 

detection of tumour recurrence and three do not use IV) 

contrast medium. Among those 7 centres that use IV contrast 

medium, 6 use a dynamic acquisition and 1 uses a semidynamic 

one. The results of the literature are also variable 

with some authors using IV contrast medium systematically in 

all cases [10–12] whereas other authors not using IV contrast 

medium at all [13, 14]. In a dynamic acquisition, contrast 

enhancement of the tumour is lower than the myometrium in 

the early phase, whereas on the late phases, tumour signal 

intensity is higher than the myometrium. Thus, interpretation 

of images is easier on the earlier phases of contrast medium 

enhancement. The use of IV contrast medium increases the 

contrast between the tumour and normal cervical stroma and 

can improve tumour detection and localization, this is 

especially useful for small tumours which may be considered 

for trachelectomy [15]. Van Vierzen et al [15] found that the 

combination of pre-contrast and post-contrast MR images 

did not clearly improve staging accuracy (83%). However, 

the addition of fast dynamic contrast-enhanced MRI improved 

staging accuracy to 91%. The use of dynamic 

contrast-enhanced MRI also improves the accuracy of 

assessment of bladder and rectal wall invasion [15]. 

Furthermore, the use of IV contrast medium is useful in the 

post-treatment setting to differentiate residual or recurrent 

tumour from radiation fibrosis [16] aswellaspresenceof 

fistulae occurring post radiation therapy. 

c. Imaging Sequences 

There is significant variability in the literature regarding the 

MRI protocols used. The number of the sequences can vary 

from 3 [17] to more than 5 [18]. There was a consensus in 

the ESUR group that the essential protocol must include a 

combination of at least two T2-weighted sequences obtained 

in the sagittal and oblique (perpendicular to the cervical 

canal) planes and T1W sequences of the upper abdomen and 

pelvis. Lymph node evaluation might be done also on T2 

sequences in an axial plan, from pelvis to left renal vein. 

T2w sequences are the best sequences to detect the 

cervical tumour and its extension to the uterus, parametria 

and the adjacent organs [19] (Fig. 1). The use of fat 

suppression is not recommended as the presence of parametrial 

fat can lead to better tumour delineation. All the 

ESUR centres and most of the authors in the literature are 

performing T2w sequences in two orthogonal planes such 

as sagittal and oblique [19]. Oblique images must be 

acquired perpendicularly to the long axis of the cervical 

canal. Slice thickness varied from 3 to 6 mm, with a 0.25 

gap. For optimal image quality, T2-weighted images 

covering the pelvis should be acquired with a small FOV 

(20–25 cm) and ideally with a 512×512 matrix. 8 of 18 

reviewed papers also add a coronal T2w sequence on the 

pelvis with thin slices (3-4 mm/0.4 mm) to assess parametrial 

extension [20] (Fig. 2). All the ESUR centres and 

several authors in the literature are also obtaining images of

1106 Eur Radiol (2011) 21:1102–1110 

Fig. 1 Sagittal T2w image, MRI. 45 years old woman, stage IB2 cervical 

carcinoma. T2W images demonstrate the tumour (arrow) invading the 

cervical stroma. Vaginal opacification with gel yielding high signal 

intensity on T2 weighting does not depict any vaginal invasion 

the abdomen (from the level of the renal veins to the pelvic 

brim) to evaluate for presence of abnormal lymph nodes [7, 

19, 21] (Fig. 3). Both T1 and T2—weighted images can be 

used for this purpose. This obviates the need for an 

additional CT of the abdomen. The total acquisition time 

for the entire staging MRI is 25–30 min. 

T1w sequences were part of the MRI staging protocol 

with 14/18 reviewed papers and nearly all members of the 

ESUR group performing T1w images without fat suppression. 

T1w sequences are very useful to evaluate for 

presence of lymphadenopathy, bone metastases and also 

in the rare occasion of hematometria. Therefore, they 

should be mandatory. Nevertheless, lymph node evaluation 

can also be done accurately on T2w axial sequences. 

Diffusion weighted imaging (DWI) Although there is little 

published data, DWI seems to be a very promising 

Fig. 2 Sagittal and axial T2W 

images, MRI. 38 years old 

woman, stage IB2 cervical 

carcinoma. Hyperintense lesion 

is invading the cervical stroma 

(Fig 2a). Coronal oblique 

section shows an intact low 

signal intensity cervical stroma 

(arrows, Fig 2b) accurately 

excluding presence of 

parametrial invasion 

Fig. 3 Axial T2W image, MRI. 47 years old woman, stage IIB cervical 

carcinoma. Lymph node spreading. An abnormal lymph node (small axis> 

10 mm) is seen in the para-aortic space (arrow). It is mandatory to perform 

in the same examination a pelvic and an abdominal staging, with slices 

from the symphysis to the left renal vein 

emerging technique in the evaluation of uterine cervical 

cancer [8, 22–25]. Seven ESUR centres routinely use DWI. 

Cervical carcinoma has a lower apparent diffusion coefficient 

(ADC) compared to the normal cervix (Fig. 4). The 

ADC increases after chemoradiotherapy [26]. There is a 

variability in the B-values used with a range of B values 

between 500 and 1000bms/-2 [26, 27]. DWI may be helpful 

in detection of residual tumour or suspicious lymph nodes 

after chemoradiotherapy [8], and might be competitive with 

PET-imaging [28, 29]. A recent paper showed that the pretreatment 

ADCs of patients with complete response are 

lower than that of those with partial response, and pretreatment 

ADC values of all patients correlated negatively 

with the percentage size reduction of the tumour after 2 

months of chemoradiation. A possible explanation for this 

observation is that tumours with high pretreatment ADC 

values are likely to be more necrotic than those with low

Eur Radiol (2011) 21:1102–1110 1107 

Fig. 4 Sagittal and axial T2W images, MRI; DWI images with ADC 

map (B 800). 42 years old woman, stage IIB cervical carcinoma. A 

2 cm hyperintense lesion is seen in the cervix (arrow) (Fig 4a) with 

right parametrial invasion (Fig 4c) (arrowheads) and a beginning of 

ADC values [8]. We recommend performing optional DWI 

sequences of the pelvis and the abdomen. 

Reporting 

The following check list is helpful for a comprehensive and 

easy to read report. 

a. Description of the lesions 

Cervical tumour is depicted on T2w images as a 

hyperintense mass compared to the cervical stroma [30, 

31]. Tumour size (in three dimensions) must be evaluated 

in at least two orthogonal views; it is crucial to give 

precise measurements as size of the tumour can dictate 

treatment options. Fertility sparing surgery is possible 

with tumours 4 cm 

may undergo chemoradiotherapy rather than radical 

surgery. 

left parametrial invasion (arrow). Sagittal and axial DWI images 

(Fig 4b) and Fig 4d show high signal intensity on DWI and with a low 

signal intensity on the ADC map (Fig 4e) suggesting restricted 

diffusion 

b. Local staging 

- Vaginal extension: precise description should be 

given if the extension is anterior or posterior. If the 

lesion reaches the 2/3 of the upper vagina, it is a 

FIGO IIA; if the lesion invades the 1/3 inferior part 

of the vagina, it is a FIGO IIIA. 

- Parametrial extension: stromal invasion is present 

if there is a disruption of the hypointense line 

circumscribing the cervix on oblique T2w images 

(Fig. 5). Parametrial invasion is present if in 

addition to the stromal invasion there is tumour 

present in the parametrium, a spiculated tumourparametrial 

interface or tumour encasement of the 

peri-uterine vessels [12]. Presence of hydronephrosis 

is consistent with parametrial invasion. 

Accuracy of MRI in assessing parametrial invasion 

varies from 80 to 87% according to the literature 

[32].

1108 Eur Radiol (2011) 21:1102–1110 

Fig. 5 Axial T2W image, MRI. 49 years old woman, stage IIB cervical 

carcinoma. Parametrial tumoural extension is seen on both sides of 

uterine cervix (arrows). Limits of cervical stroma are nearly not visible 

- Isthmic extension: clinical evaluation is not 

accurate in case of isthmic invasion. The reporting 

should include it because positioning of brachytherapy 

coils might be dependant of the level of 

isthmic tumour extension [33]. 

c. Lymph node staging 

FIGO classification does not include the nodal status. 

Yet, lymph node spreading is one of the most important 

prognostic factors in cervical carcinoma [34, 35]. Accuracy 

of MRI is low for lymph node staging, with a sensitivity 

varying from 38 to 89%, and a specificity from 78 to 99% 

[36, 37]. Due to its high sensitivity, PET-CT is recommended 

for locally advanced cervical carcinoma with no 

abnormal lymph node depicted in the pelvis or the abdomen 

[38]. Size criterion for a suspicious lymph node is a short 

axis superior to 1 cm, in the pelvis or the abdomen [39]. 

Fig. 6 Sagittal T2W image 

before a and after b 

radiation-chemotherapy (RCT) 

and brachytherapy. 37 years old 

woman, stage IIB cervical 

carcinoma. A 5 cm lesion 

invading the cervical stroma is 

seen with a hyperintense signal 

intensity (arrow, fig a). After 

treatment (3 weeks delay), the 

tumour is not seen. There is 

reconstitution of the normal low 

signal intensity cervical stroma 

suggestive of complete response 

to treatment. No residual tumour 

was found at hysterectomy 

However, smaller lymph nodes may be malignant, especially 

in the pelvis; therefore it is important to take in 

account other features of malignancy such as round shape, 

irregular margins, signal intensity similar to the primary 

tumour and presence of necrosis. 

d. Evaluation of Tumour Response to Treatment 

Chemoradiotherapy followed by brachytherapy is the 

standard treatment for patients with locally advanced 

uterine cervical carcinoma (> IB1 FIGO stage) [40]. 

Surgery is usually avoided in case of complete response 

following chemoradiotherapy treatment, due to its high rate 

of urinary side effects (incontinence, uteral distension, 

chronic bladder infection …). Tumour response evaluation 

is based on three criteria: clinical examination, PAP smear 

analysis and post treatment MR evaluation [41]. 

After treatment, MR protocol is the same as for cervical 

cancer staging, but IV injection is recommended. MR 

criteria for a complete response include: 

– no lesion seen in the cervix or in the adjacent anatomic 

areas 

– homogeneous hypointense cervical stroma 

– homogeneous and delayed intravenous contrast medium 

uptake of the cervix after IV injection [42] (Fig. 6). 

Interpretation and performance of MRI in the follow-up 

setting are lower compared to the primary staging tumour 

detection. It is useful to compare the post treatment images 

with the pre-treatment images to facilitate tumour detection 

and re-staging. 

e. Detection of a recurrence 

- After medical treatment: 

There is no consensus among the ESUR centres on in the 

reviewed literature regarding the indication of MRI for the 

follow-up of patients with treated cervical carcinoma.

Eur Radiol (2011) 21:1102–1110 1109 

Usually, MRI is performed when there is a clinical 

suspicion of recurrence. 

– After surgery : 

There is also no consensus for a systematic MR followup. 

Nevertheless, in case of trachelectomy, an MRI at 6 

months and 1 year is advised, because recurrence rate is 

higher compare to patients who undergo brachytherapy or 

chemotherapy [43]. 

Conclusion 

Although FIGO staging system does not include imaging in 

the staging of cervical cancer, in the revised FIGO system 

imaging techniques are encouraged to assess the important 

prognostic factors and imaging is now complimentary to 

the clinical assessment. Radiologists must familiarize 

themselves with the new FIGO staging system and 

understand its relevance to patient management. Magnetic 

resonance imaging is the imaging modality of choice for 

staging the primary cervical tumour, evaluate response to 

treatment and detect tumour recurrence and potential 

complications. Adequate patient preparation, protocol optimization 

and MRI reporting expertise are essential to 

achieve high diagnostic accuracy. 

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