The Egyptian Journal of Radiology and Nuclear Medicine (2015) 46, 781–789

Egyptian Society of Radiology and Nuclear Medicine

The Egyptian Journal of Radiology andNuclearMedicine

www.elsevier.com/locate/ejrnmwww.sciencedirect.com

ORIGINAL ARTICLE

Apparent diffusion coefficient value in evaluating

types, stages and histologic grading of cancer

cervix

* Corresponding author. Tel.: +20 1147004434.E-mail addresses: dididodge13@gmail.com (D.I. Hasan), mones@

hotmail.com (M.M. Enaba).

Peer review under responsibility of Egyptian Society of Radiology and

Nuclear Medicine.

http://dx.doi.org/10.1016/j.ejrnm.2015.04.0060378-603X � 2015 The Authors. The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier B.V.This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Doaa Ibrahim Hasana,*, Mones M. Enaba

a, Hossam M. Abd El-Rahman

a,

Shrin El-Shazely b

a Diagnostic Radiology Department, Zagazig University, Egyptb Obstetric and Gynecology Department, Zagazig University, Egypt

Received 28 January 2015; accepted 9 April 2015

Available online 18 May 2015

KEYWORDS

Apparent diffusion coeffi-

cient (ADC);

Cervical cancer;

FIGO

Abstract Aim: To determine whether the apparent diffusion coefficient (ADC) measurements cal-

culated values were significantly different between cervical tumors with different histological char-

acteristics (type, degree of differentiation, and stage of malignancy).

Patients and methods: MRI and DWI scans performed in 26 pathologically proved cancer cervix

patients. ADC values of different pathological types of cervical cancer were compared. Student’s

t test was used for statistical analysis.

Results: There were 18 squamous cell carcinoma and 8 adenocarcinomas showed with biopsy

results. Early stage (FIGO-Ib–IIa, n= 7), (FIGO-IIb–IIIb–IVa, n= 19). The mean ADC values

for squamous cell carcinoma (n= 18), and adenocarcinoma (n= 8) were 0.88 · 10�3, and

0.91 · 10�3 mm2/s, respectively. Statistical analysis showed significant difference in ADC value

between both tumor types (P< 0.05). There was also significant difference between the mean

ADC values of the tumor grade I and the other grades (II, III) (p< 0.05). The mean ADC values

in early stage cervical cancer (0.83 ± 0.05 · 10�3 mm2/s) were significantly lower than the mean

ADC values in late stage disease (0.98 ± 0.06 · 10�3 mm2/s) (p< 0.05).

Conclusion: ADC value measurements can provide useful information in diagnosis of cervical

cancer as well as in preoperative assessment of the tumor stage.� 2015 The Authors. The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting

by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://

creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Uterine cervical cancer is the third most common malignancy

affecting the female genital tract in middle age groupbetween 45 and 55 years (1,2). Its incidence is increasingrapidly in developing countries. The International Federation

Table 1 FIGO staging for carcinoma of cervix (3). International Federation of Gynecology and Obstetrics (FIGO) Staging Systems.

� Stage 0: Cervical intraepithelial neoplasia (CIN III)

� Stage I Confined to cervix

Stage Ia Invasive carcinoma only diagnosed by microscopy

Ia1: Stromal invasion <3 mm in depth and <7 mm in extension

Ia2: Stromal invasion >3 mm depth and not >5 mm and extension >7 mm

Stage Ib: Clinically visible lesions limited to the cervix or pre-clinical cancers >stage 1a

Ib1: Clinically visible tumor >4 cm in greatest dimension

Ib2: Clinically visible tumor >4 cm in greatest dimension

� Stage II: Beyond cervix though not to the pelvic sidewall or lower third of the vagina

Stage IIa: Involves upper 2/3rd of vagina without parametrial invasion

Stage IIa1: Clinically visible tumor >4 cm in greatest dimension

Stage IIa2: Clinically visible tumor >4 cm in greatest dimension

Stage IIb: With parametrial invasion

� Stage III

Stage IIIa: Tumor involves the lower third of the vagina with no extension to pelvic sidewall

Stage IIIb: Extension to pelvic side wall or causing obstructive uropathy

� Stage IV: Extension beyond pelvis or biopsy proven to involve the mucosa of the bladder or the rectum

Stage IVa: Extension beyond pelvis or rectal/bladder invasion

Stage IVb: Distant organ spread

Fig. 1 Staging of uterine cervix carcinoma according to FIGO (4).

782 D.I. Hasan et al.

Table 3 Comparison between the histopathologic subtypes,

tumor stage, tumor grades and the mean ADC values.

No (%) Mean ADC value

Histopathology

Squamous cell cancer 18 (69.2%) 0.88 · 10�3 mm2/s*

Adenocarcinoma 8 (30.7%) 0.91 · 10�3 mm2/s

Tumor stage

Early stage (stages Ib–IIa) 7 (26.9%) 0.83 · 10�3 mm2/s*

Late stage (stages II–III–IV) 19 (73%) 0.98 · 10�3 mm2/s

Tumor grade

Grade I 11 (42.3%) 0.90 · 10�3 mm2/s*

Apparent diffusion coefficient value in evaluating of cancer cervix 783

of Gynecology and Obstetrics (FIGO) staging system updatedin 2009 (Table 1 and Fig. 1) is commonly used for treatmentplanning but is inadequate in the evaluation of prognostic fac-

tors such as tumor volume and nodal status (3,4). Among theimaging modalities used in the preoperative evaluation ofcervical cancer, MRI is an excellent modality for depicting

invasive cervical cancer: it can provide objective measurementof tumor size and provides a high negative predictive value forparametrial invasion and stage IVa disease (5). Diffusion

weighted imaging (DWI) is a recent approach for evaluatingmalignancies. Although it is widely used in the detection andevaluation of acute stroke (6), with improving MRI technol-ogy that has reduced the artifacts interfering with the image

interpretation, DWI has been used in body imaging (7,8).Apparent diffusion coefficient (ADC) maps are calculatedfrom DWI images and it has been reported that quantitative

evaluation of ADC values might be used for differentiatingbenign from malignant tissue (9). Lymph node involvementis not incorporated in the FIGO staging system, however, it

is an important factor in the choice of adjuvant radiation ther-apy in cervical cancer. Surgical lymph node assessment is thegold standard for the diagnosis of lymph node metastases,

accurate preoperative assessment of lymph node metastasesis still very important in patients with cervical cancer from aclinical point of view. Many studies showed decreased ADCvalue in malignant lymph nodes when compared to benign

lymphadenopathy (10,11).

Table 2 The patient age, number of each FIGO stage and

detected pelvic LNs.

Grade II 8 (30%) 0.94 · 10�3 mm2/s

Grade III 7 (26.9%) 0.97 · 10�3 mm2/s

Pelvic LN+metastasis

Yes 9 (47.3%) 0.77 · 10�3 mm2/s*

No 10 (52.6%) 1.70 · 10�3 mm2/s

* P value shows statistically significant (P> 0.05).

2. Patients and methods

This study was conducted following ethics approval from thelocal institutional review boards and all patients gave informedconsent. From December 2012 to November 2014, we evalu-

ated 26 histopathologically proved cervical cancer patientswith early and late stage locally advanced cancer cervix.Early stage (FIGO-Ib–IIa, n = 7), (FIGO-IIb–IIIb–IVa,

n = 19), who were consecutively referred to our Radiologydepartment for preoperative/pretherapy MRI assessment.

Characteristic Total n= 26

Age (years)a 59.7 ± 4.6 years (35–

71 years)

Premenopause/postmenopause

ratio

20:6

FIGO stageb

Early

Ib 2 (7.9%)

IIa 5 (19%)

Late

IIb 9 (34.6%)

IIIb 7 (26.9%)

Iva 3 (11.4%)

Pelvic LN + metastasis

Yes 9 (47.3%)

No 10 (52.6%)

LN= lymph node.a Numbers outside parenthesis are average ± standard deviation.

Numbers in parenthesis are range.b FIGO= International Federation of Gynecology and Obstet-

rics. Numbers in parenthesis are percentage.

2.1. Conventional MRI

Patients were prepared for MRI after 6 h of fasting and 20 mghyoscine butylbromide (Buscopan) was given intramuscularlyat the start of each examination to reduce bowel peristalsis.

All examinations were performed on a 1.5-T MRI system(Achieva, Philips Healthcare, Best, the Netherlands) using adedicated torso coil. The standard sequences included high-

resolution sagittal T2-weighted turbo spin-echo (TR/TE =4000/80 ms, turbo factor = 14, field of view = 240 · 240 mm,matrix size = 400 · 392, slice thickness = 4 mm, intersection

gap = 0 mm), axial T2-weighted turbo spin-echo (TR/TE =2800/100 ms, turbo factor = 12, field of view = 403 ·300 mm, matrix size = 787 · 600, slice thickness = 4 mm,

intersection gap = 0 mm) and T1-weighted turbo-field-echocontrast-enhanced acquisition (TR/TE = 2.4/1.2 ms, field ofview = 350 · 350 mm, matrix size = 212 · 211, slice thick-ness = 3.0 mm, intravenous bolus injection of 0.1 mmol/kg

body weight gadopentetate dimeglumine at 3.0 ml/s), to allowaccurate evaluation of the parametrium.

2.2. DW-MRI

DW-MRI was performed using single-shot spin-echo echopla-nar imaging, immediately after the axial T2-weighted imagingand before intravenous contrast injection. It was acquired in

free breathing with background body signal suppression (pre-saturation inversion recovery fat suppression) using the follow-ing parameters: TR/TE = 2000/54 ms, field of view = 403 ·300 mm, matrix size = 168 · 124, slice thickness = 4 mm,

intersection gap = 0 mm, parallel imaging with sensitivityencoding factor of 2, receiver bandwidth = 1382.5 Hz perpixel. We acquired b values (0, 500 and 1000 s/mm2) in the

axial plane covering 20 slices to include the entire cervical

784 D.I. Hasan et al.

cancer, using motion-probing gradients in three orthogonalaxes. We ensured that the field of view, slice thickness andintersection gap were the same as the anatomical axial T2-

weighted imaging to allow image overlay and co-registration.ADC maps were calculated from DW images that were pre-

viously assessed. In the patient group, ADC measurements

were executed on reconstructed ADC maps with the largestregion of interest (ROI) within the tumor. Equal-sized ROIs(each 5 mm2) that excluded macroscopic necrotic areas (fluid

signal on T2), large vessels and areas with susceptibility arti-fact caused by air–water interface. The greatest dimension ofthe tumor was measured. ROIs were set up three times andthe average of them was used for each ADC value measure-

ment in the malignant masses and detected pelvic L.Ns(>10 mm in the longitudinal diameter).

2.3. Statistics

Descriptive statistics were used to describe clinical demograph-ics using range, means and standard deviation (mean ± SD).

A t-test was used to analyze comparisons and a p value < 0.05was accepted as statistically different. Comparisons of meanADC values between histopathological subtypes, tumor grades

and stages were made. Rare cervical cancer subtypes likesmall-cell carcinoma were excluded from the study becauseof insufficient numbers. Comparisons of mean ADC values

Fig. 2 37 years old female with cervical carcinoma, FIGO stage Ib2

cervical mass involving the posterior lip of the cervix with clear uppe

denoting the absence of parametrial invasion. (C and D) DWI and A

ADC measures 0.687 · 10�3 mm2/s. Pathologically proved as moderat

between enlarged metastatic pelvic L.Ns and nonmetastaticone.

3. Results

Twenty-six patients, their average age 35–71 years old(mean was 59.7 ± 4.6 years). They were premenopause/post-

menopause (20:6) (Table 2).Pathological diagnoses: Early stage (FIGO-Ib–IIa, n = 7),

(FIGO-IIb–IIIb–IVa, n= 19). According to the International

Federation of Gynecology and Obstetrics (FIGO), classifica-tion stages I–IIa are considered early stage and stages IIb ormore are considered late stage (3). Seven patients were in the

early stage with 2 patients in stage Ib and 5 in stage IIa, whereas19 patients were in the late stage, nine patients in stage IIb, 7patients in stage IIIb and 3 patients in stage IVa (Table 2).

Enlarged L.Ns found in 19/26 of the patients, nine of them weremalignant, while the other 10 patients were hyperplastic lymphnodes.

There were squamous cell cancer in 18 (69.2%) patients and

adenocarcinoma in 8 (30.7%) patients, with mean ADC valuesof 0.88 · 10�3 mm2/s and 0.91 · 10�3 mm2/s, respectively.Apparent diffusion coefficient value of squamous carcinoma

was statistically significant lower than that of adenocarcinoma(P < 0.05) (Table 3).

. (A and B) Axial and sagittal T2WI show well defined isointense

r vagina as well as preserved peripheral hypointense stromal ring

DC maps show restricted diffusion of the cervical mass with low

ely differentiated squamous cell carcinoma grade I.

Apparent diffusion coefficient value in evaluating of cancer cervix 785

According to the FIGO classification stages: seven patients(26.9%) were in the early stage with 2 patients in stage Ib(Fig. 2) and 5 in stage IIa (Fig. 3), whereas 19(73%) patients

were in the late stage, 9 patients in stage IIb (Fig. 4), 7 patientsin stage IIIb (Fig. 5) and 3 patients in stage IVa (Fig. 6).

The mean ADC values in early-stage cervical cancer

(0.83 ± 0.05 · 10�3 mm2/s) were significantly lower thanthe mean ADC values in the late stage of the disease(0.98 ± 0.06 · 10�3 mm2/s) (p < 0.05).

Comparison of mean ADC values for early and late stagecervical cancer according to FIGO classification (Table 3).There was a significant difference between early and late stagecervical cancer (p < 0.05).

With regard to tumor grades, there were statistical differ-ence was found between the mean ADC values, grade I(n:11), and other grades (grade II n:8 and grade III n:7)

(p< 0.05). The mean ADC value of grade I cases was0.90 · 10�3 mm2/s, while in grade II and III the mean ADCvalues were 0.94 · 10�3 mm2/s and 0.97 · 10�3 mm2/s, respec-

tively. There was no statistically significant difference betweengrade II and grade III (Table 3, Fig. 7).

In the study group the mean ADC values

(0.77 · 10�3 mm2/s) for metastatic enlarged L.Ns (Fig. 5Eand G), which were statistically significant (p< 0.05) than that

Fig. 3 47 years old female patient with cervical carcinoma FIGO stag

mass in the cervix displaying low SI on T1 and intermediate signal inte

endometrial cavity with preserved cervical hypointense stromal rin

of the cervical mass with low ADC measures 0.854 · 10�3 mm2/s. Path

grade III.

of the hyperplastic enlarged L.Ns (1.70 · 10�3 mm2/s)(Table 3).

4. Discussion

Magnetic Resonance Imaging with high soft-tissue resolutionis the most valuable imaging modality in the assessment of

tumor size, depth of cervical invasion and extent of locore-gional spread in the treatment planning of cervical cancer(12,13). DWI which has recently been used in the diagnosis

of malignant lesions, can distinguish the normal uterine cervixfrom cervical cancer and benign lymph nodes from malignantones (14).

In our study the mean ADC values in squamous carcinomawere statistically lower than those of adenocarcinoma(p< 0.05). Similar findings had reported by Lui et al. (15) in

their studying 42 patient group. The different pathologicalcharacteristics are of these two tumor types. Cell of squamouscarcinoma tends to be more compact and crowded, while ade-nocarcinoma gives out more tube-like structures which mimic

adeno-tissues. These tube-like structures have a large intercel-lular space which will lead to higher ADC value. DWI, as aclassification methodology applied successfully in gliomas

e IIa. (A and B) Sagittal T2WI and axial T1WI show well-defined

nsity in T2WI extending to upper third of the vagina as well as the

g. (C and D) DWI and ADC maps show restricted diffusion

ologically proved as squamous cell carcinoma nonkeratinized type

Fig. 4 53 years old with cancer cervix FIGO stage IIb. (A) Axial T2WI shows cervical mass displaying isointense SI with interruption of

the hypointense ring denoting parametrial invasion. (B) Axial T2WI at higher level shows enlarged left deep pelvic LN (arrow). (C and D)

DWI and ADC maps show restricted diffusion with low ADC value measures 0.762 · 10�3 mm2/s. Pathologically proved as squamous cell

carcinoma grade II.

786 D.I. Hasan et al.

(16) could probably also been used in pathological subtypeclassification of cervical tumor.

On contrary Tuna et al. (17) had reported no significant dif-ference between mean ADC values of squamous cell

cancer and adenocarcinoma (0.95 · 10�3 mm2/s and0.91 · 10�3 mm2/s, respectively) (p > 0.05). They explainedthat may be related to the smaller patient group of their study.

Mangal et al. (18) found in their study, preoperative estimationof histologic type based on the ADC values still seems difficultbecause there is a considerable overlap between them.

In the present study, according to the FIGO classificationstages: the mean ADC values in early-stage cervical cancer(0.83 ± 0.05 · 10�3 mm2/s) were significantly lower than themean ADC values in the late stage of the disease

(0.98 ± 0.06 · 10�3 mm2/s) (p< 0.05). Several researchesshowed potential clinical value of ADC value in differentiatingFIGO stage or pathological grade. Patrick et al. (19) analyzed

relationship between FIGO stage and ADC value. They foundthat ADC was significantly lower in FIGO stage T1b/T2a thanthat in T2b and T3/T4. This may indicate disease prognosis or

help in treatment planning.McVeigh et al. (9) reported that mean ADC values of

patients with cervical cancer were lower than normal cervix

ADC values. Also, with regard to FIGO classification, mean

ADC values were found to be lower in stages Ib/IIa than instage IIb and stages III/IV, as we found in this study. The sig-nificant difference between the FIGO stages may be a usefulfactor in treatment planning, especially for cases in which

the extent of the disease is undetermined. In a study byKuang et al. (20), they concluded that in the evaluation of cer-vical cancer, the diagnostic accuracy of ADC values for the

distinction of cancerous from normal tissue was high.In our study the ADC values of cervical cancers of higher

pathological grade showed tendency to decrease compared to

those of lower grade, with significant difference between gradeI and other grades (II, III). On the other hand, a negative cor-relation between tumor grade and mean ADC values wasreported in many studies (15,17). While in Ken’s study, the

ADC values of endometrial cancers of higher pathologicalgrade showed tendency to decrease compared to those of lowergrade, although estimation of histological grade based on

ADC values seems difficult because of considerable overlap(21).

A study by Chen et al. (22) reported lower mean ADC val-

ues for cervical cancer than for a normal cervix. Also, theyreported that there was an increase in ADC values after radio-therapy, which indicated that DWI might be used to monitor

the response to therapy. Moreover in patients with cervical

Fig. 5 73 years old patient presented by postmenopausal bleeding with cancer cervix FIGO stage IIIb. (A and B) Sagittal and axial

T2WIs show the large cervical mass involving both anterior and posterior cervical wall distending the cervical canal and extending to the

upper vagina. It displays intermediate SI with interruption of the low-signal-intensity cervical stromal ring. (C) Axial T2-weighted image

on higher level shows bilateral enlarged deep external iliac pelvic LNs. (D and E) DWI shows restricted diffusion in the cervical mass and

L.Ns (arrow). (F and G) Gray ADC map shows low ADC value of the cervical mass and within the enlarged L.N, which were

0.866 · 10�3 mm2/s and 0.733 · 10�3 mm2/s respectively. Pathologically proved as invasive well poor differentiated squamous cell

carcinoma grade III.

Apparent diffusion coefficient value in evaluating of cancer cervix 787

Fig. 6 60 years old female presented by postmenopausal bleeding with cancer cervix FIGO stage IVa. (A) Sagittal T2WI Large ill

defined cervical mass involving both anterior and posterior cervical lips, displaying intermediate SI on T2WI, following contrast it shows

homogenous enhancement. Interruption of the T2 hypointense ring. Invasion of the upper 2/3 as well as lower 1/3 of the vagina. (B and C)

DWI at the cervical region and more higher level shows invasion of the posterior UB wall, right pelvic side and enlarged right deep pelvic

LN. (D)Restricted diffusion with ADC value 0.877 · 10�3 mm2/s. Pathologically proved as of squamous cell carcinoma grade III.

Fig. 7 Box-whisker plots for the mean ADC values of the

histological grades of uterine cervical cancer. The ADC values of

uterine cervical cancer grade I were significantly lower than those

of grades II and III.

788 D.I. Hasan et al.

cancer, the measurement of ADC values could be an important

factor for assessing response to chemoradiotherapy (23,24).Within the pelvis, cervical cancer spreads first to the

parametrial nodes, then to the obturator and iliac nodes.

Although not incorporated in the FIGO staging system, the

presence of lymph node metastases has significant prognosticand treatment consequences. The 5 year survival for node-positive patients is 39–54%, compared with 67–92% in

patients without nodal involvement (25).Among our studying group, the mean ADC of metastatic

lymph nodes was significantly lower than in benign lymphnodes, which were 0.77 · 10�3 mm2/s for metastatic enlarged

L.Ns compared to 1.70 · 10�3 mm2/s for enlarged hyperplasticL.Ns. Similar results had reported by Lei et al. (11) and Nakaiet al. (26). Moreover, use of DWI in conjunction with T2-

weighted images identified 85% of metastatic nodes, while only25% were identified on the T2-weighted images alone (26).DWI sequence increased the sensitivity for identifying lymph

nodes, meaning the information could be used as a map toaid surgical planning, avoiding extensive lymphadenectomyand refining radiotherapy fields (11).

The limitation of our study was that it did not encompassall of the cervical cancer subtypes.

5. Conclusion

Use of ADC value measurements may provide convenient datafor the diagnosis of cervical cancer as well as for preoperativeassessment of the tumor and nodal staging.

Apparent diffusion coefficient value in evaluating of cancer cervix 789

Conflict of interest

The authors declare that there are no conflict of interest.

References

(1) Nicolate V, Carignan L, Bourdon F, Prosmanne O. MR

imaging of cervical carcinoma: a practical staging approach.

RadioGraphics 2000;20:1539–49.

(2) Szklaruk F, Tamm E, Choi H, Varavithya V. MR Imaging of

common and uncommon pelvic masses. RadioGraphics

2003;23:403–24.

(3) Pecorelli S, Zigliani L, Odicino F. Revised FIGO staging for

carcinoma of the cervix. Int J Gynaecol Obstet 2009;105:107–8.

(4) Claudia CC, Sylvia MF, Karen VP, Maria CR. Magnetic

resonance imaging in the staging of cervical cancer. Radiol Bras

2007;40(3):207–21.

(5) Sidath Liyanage H, Roberts Charlotte A, Rockall Andrea G.

MRI and PET scans for primary staging and detection of cervical

cancer recurrence. Women’s Health 2010;6(2):251–69.

(6) Sorensen AG, Wu O, Copen WA. Human acute cerebral

ischemia: detection of changes in water diffusion anisotropy by

using MR imaging. Radiology 1999;212:785–92.

(7) Kurihara Y, Yakushiji YK, Tani I, Nakajima Y, Van Cauteren

M. Coil sensitivity encoding in MR imaging: advantages and

disadvantages in clinical practice. AJR Am J Roentgenol

2002;178:1087–91.

(8) Takahara T, Imai Y, Yamashita T, Yasuda S, Nasu S, Cauteren

M. Diffusion weighted whole body imaging with background

body signal supression (DWIBS): technical improvement using

free breathing, STIR and high resolution 3D display. Radiat Med

2004;22:275–82.

(9) McVeigh PZ, Syed AM, Milosevic M, Fyles A, Haider MA.

Diffusion-weighted MRI in cervical cancer. Eur Radiol

2008;18:1058–64.

(10) Liu Y, Xia LM, Zou ML, et al. Diffusion weighted imaging

and apparent diffusion coefficient value in differential diagnosis

of lymph node lesions. Chin J Med Imaging Technol 2006;22:

730–2.

(11) Lin G, Ho KC, Wang JJ, et al. Detection of lymph node

metastasis in cervical and uterine cancers by diffusion-weighted

magnetic resonance imaging at 3T. J Magn Reson Imaging

2008;28:128–35.

(12) Scheidler J, Heuck AF. Imaging of cancer of the cervix. Radiol

Clin North Am 2002;40:577–90.

(13) Ascher SM, Takahama J, Jha RC. Staging of gynecologic

malignancies. Top Magn Reson Imaging 2001;12:105–29.

(14) Chen YB, Hu CM, Chen GL, Hu D, Liao J. Staging of uterine

cervical carcinoma: whole-body diffusion-weighted magnetic

resonance imaging. Abdom Imaging 2011;36:619–26.

(15) Liu Y, Bai R, Sun H, Liu H, Wang D. Diffusion-weighted

magnetic resonance imaging of uterine cervical cancer. J Comput

Assist Tomogr 2009;33:858–62.

(16) Toze D, Jager H, Danchaivijitr N, Benton C, Tofts P, Rees J.

Apparent diffusion coefficient histograms may predict low-grade

glioma subtype. NMR Biomed 2007;20:49–57.

(17) Demirbas� T, Cimilli T, Bayramoglu S, Guner NT, Hocaoglu E,

Inci E. Contribution of diffusion-weighted imaging to diagnosis

and staging of cervical cancer. Balkan Med J 2014;31(2):154–7.

(18) Mahajan Mangal, Kuber Rajesh, Chaudhari KR, Chaudhari

Prashant, Ghadage Pravin, Rushikesh Naik. MR imaging of

carcinoma cervix. Ind J Radiol Imaging (IJRI) 2013;23:247–52.

(19) Patrick ZM, Aejaz MS, Michael M, Hankey Z, Ronald A, Peters

S. Diffusion-weighted MRI in cervical cancer. Eur Radiol

2008;18:1058–64.

(20) Kuang F, Ren J, Zhong Q, Liyuan F, Huan Y, Chen Z. The value

of apparent diffusion coefficient in the assessment of cervical

cancer. Eur Radiol 2013;23:1050–8.

(21) Ken T, Takashi K, Tsuneo S, et al. Diffusion-weighted MR

imaging of uterine endometrial cancer. J Magn Reson Imaging

2007;26:682–7.

(22) Chen Jianyu, Zhang Yun, Liang Biling, Yang Zehong. The utility

of diffusion-weighted MR imaging in cervical cancer. Eur J

Radiol 2010;74:e101–6.

(23) Nakamura K, Joja I, Nagasaka T, Fukushima C, Kusumoto T,

Seki N. The mean apparent diffusion coefficient value (ADC

mean) on primary cervical cancer is a predictive marker for

disease recurrence. Gynecol Oncol 2012;127:478–83.

(24) Makino H, Kato H, Furui T, Morishige KI, Kanematsu M.

Predictive value of diffusion-weighted magnetic resonance imag-

ing during chemoradiotherapy for uterine cervical cancer. J

Obstet Gynaecol Res 2014;40:1098–104.

(25) Nilu M, Vinay K, Atul S, Amal C, Debabrata B, Utpal B.

Evaluation of carcinoma cervix using magnetic resonance imag-

ing: correlation with clinical FIGO staging and impact on

management. J Med Imaging Radiat Oncol 2012;56:58–65.

(26) Nakai G, Matsuki M, Inada Y, Tatsugami F, Tanikake M,

Narabayashi I, et al. Detection and evaluation of pelvic lymph

nodes in patients with gynecologic malignancies using body

diffusion-weighted magnetic resonance imaging. J Comput Assist

Tomogr 2008;32(5):764–8.