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European Journal of Radiology 81 (2012) 508513

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EuropeanJournal ofRadiology

j ournal homepage: www.elsevier .com/ locate /e j rad

F-18 FDG PET-CT in patients with recurrent glioma: Comparison with contrast

enhanced MRI

Amburanjan Santra a,1, Rakesh Kumar b,, Punit Sharma b, Chandrashekhar Bal b,Atin Kumar c, Pramod KumarJulka d, Arun Malhotra b

a Department of Nuclear Medicine,Medical College Kolkata, Kolkata, Indiab Department of Nuclear Medicine, AllIndia Institute ofMedical Sciences,New Delhi,Indiac Department of Radio-diagnosis, All India Institute of Medical Sciences,New Delhi,Indiad Department of Radiotherapy, AllIndia Institute ofMedical Sciences, NewDelhi, India

a r t i c l e i n f o

Article history:

Received 8 October 2010

Accepted 3 January 2011

Keywords:

Glioma

Recurrence

PET-CT

MRI

FDG

a b s t r a c t

Purpose: The purpose of the study was to compare the efficacies of FDG PET-CT and contrast enhanced

MRI in detection ofrecurrent gliomas.

Methods: Ninety histopathologically proven glioma patients with clinical suspicion of recurrence were

evaluated. All patients underwent FDG PET-CT scan and contrast enhanced MRI. Combination ofclinical

follow up, repeat imaging and biopsy (when available) was taken as gold standard.

Results: Based on gold standard criteria, 59 patients were positive and 31 patients were negative for

recurrence. Overall sensitivity and specificity ofFDG PET-CT were 70% and 97% respectively whereas that

for contrast enhanced MRI was 95% and 23%. FDG PET-CT also has higher accuracy (80%) as compared to

MRI (70%). FGD PET-CT has lower sensitivity than MRI in all grades, except for Grade II gliomas where

their sensitivities are comparable (95% and 90%). Very low specificity ofMRI was observed in all grades

oftumour (1833%). In contrast the specificity ofFDG PET-CT was high across all grades (83100%).

Conclusion: FDG PET-CT is a highly specific modality for detecting recurrence in patients with gliomas

and can effectively exclude post therapy changes.

2011 Elsevier Ireland Ltd. All rights reserved.

1. Introduction

Recurrence in glioma may occur after complete removal of

tumour or stabilization of tumour with treatment. In more than

90% cases, initial site of recurrence is at or within 2 c m of the

primary site [1]. Radiation injury and postoperative changes are

also usually found around the tumour bed. Moreover, radiation

necrosis and recurrent tumour can frequently coexist [2]. Differen-

tiation between recurrence and radiation necrosis is crucial since

the two entities have completely different management and prog-

nosis. Radiation necrosis can produce disruptionin the bloodbrain

barrier (BBB) by vascular and astrocytic damage, and thus contrast

enhancement, edema, and cortical dysfunction that are indis-

tinguishable from recurrent tumour on conventional computed

tomography (CT) or magnetic resonance imaging (MRI) [3,4].

Corresponding authorat: E-81, Ansari Nagar (East), AIIMS Campus, New Delhi

110029, India. Tel.: +9111 26588017; fax: +9111 26588663.

E-mail addresses: a ranjan santra@yahoo.co.in (A. Santra), rkphulia@yahoo.com

(R. Kumar).1 Department of Nuclear Medicine, Medical College Kolkata, Kolkata 700073,

India. Tel.: +91 9433812043; fax: +91 11 26588663.

Because of its high soft-tissue contrast, MRI has become the

first-line method of choice for the assessment of brain tumours.

Though conventional contrast enhanced MRI allows for excellent

visualization of these tumours, there are still certain limitations.

This particularly includes defining tumour extension and grade, as

well as differentiating tumour recurrence from necrosis or scar.

Recurrent brain tumour usually demonstrates extensive edema

and enhances with intravenous paramagnetic contrast on MRI.

However, necrosis induced by therapy or occurring spontaneously

during tumour progression may also show contrast enhancement

and hence cannot be distinguished reliably from a solid tumour

after therapy on MRI [5,6].

Positron emission tomography (PET) with F18-

fluorodeoxyglucose (FDG) is widely used to provide information

regarding glucose metabolism in a wide variety of tumours,

including gliomas. FDG accumulation in gliomas is not dependent

on bloodbrain barrier (BBB) disruption [7]. FDG PET imaging

of brain tumours have been applied for defining the extent of

tumour, tumour grading, prognostication, treatment response

evaluation, as well as to differentiate between radiation necrosis

and recurrent tumour, and between benign and malignant lesions

[810]. The use of FDG PET to distinguish recurrent tumour from

radiation necrosis appears promising [11,12]. FDG PET however

0720-048X/$ see front matter 2011 Elsevier Ireland Ltd. All rights reserved.

doi:10.1016/j.ejrad.2011.01.080

http://localhost/var/www/apps/conversion/tmp/scratch_1/dx.doi.org/10.1016/j.ejrad.2011.01.080http://localhost/var/www/apps/conversion/tmp/scratch_1/dx.doi.org/10.1016/j.ejrad.2011.01.080http://www.sciencedirect.com/science/journal/0720048Xhttp://www.elsevier.com/locate/ejradmailto:a_ranjan_santra@yahoo.co.inmailto:rkphulia@yahoo.comhttp://localhost/var/www/apps/conversion/tmp/scratch_1/dx.doi.org/10.1016/j.ejrad.2011.01.080http://localhost/var/www/apps/conversion/tmp/scratch_1/dx.doi.org/10.1016/j.ejrad.2011.01.080mailto:rkphulia@yahoo.commailto:a_ranjan_santra@yahoo.co.inhttp://www.elsevier.com/locate/ejradhttp://www.sciencedirect.com/science/journal/0720048Xhttp://localhost/var/www/apps/conversion/tmp/scratch_1/dx.doi.org/10.1016/j.ejrad.2011.01.080

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A. Santra et al. / European Journal of Radiology 81 (2012) 508513 509

has some limitations in characterizing brain tumours because of

the high basal glucose metabolic rate of normal brain. Except for

very high grade tumours, most of the tumours have equal or lower

FDG uptake than that of normal brain parenchyma [13]. Under

these circumstances, fused PET-CT improves the sensitivity to

certain extent. Some studies have compared the roles of FDG PET

and contrast enhanced MRI for differentiating recurrence from

radiation necrosis. But because of the lesser number of patients,

results of these studies were variable [14,15]. The present study

was aimed to compare the diagnostic capabilities of FDG PET-CT

and MRI in detection of glioma recurrence in a large series of

patients.

2. Materials and methods

This prospective study was conducted after obtaining prior

approval of institutional review board. Patients were recruited in

the study between August, 2006 and February, 2008. A written

informed consent was obtained from all patients.

2.1. Patients

A total of 90 patients with glioma were included in the study.Inclusion criteria were histopathologically proven glioma, previ-

ous treatment with surgery and/or radiotherapy with or without

chemotherapy and clinical suspicion of recurrence. Exclusion cri-

teria were primary brain tumour other than gliomas and proven

malignancy of other sites where from metastasis canoccurto brain.

Allpatientsunderwent FDGPET-CT scanand conventional MRIwith

contrast in our institute within one week span.

2.2. F-18 FDG PET-CT imaging

PET-CT scans were taken on a dedicatedPET-CT scanner present

in our institute (BIOGRAPH 2, SEIMENNS, Germany). It has LSO

(Lutetium oxyorthosilicate, Lu2SiO5: Ce) detectors with attenua-

tion coefficient 0.89 cm1

, photofraction 30%, decay constant 40nsand energy resolution at 511KeV, %FWHM is 10 with spatial res-

olution of 6mm. All patients fasted for at least 4 h before the test.

Blood glucose level was below 140mg/dl in all patients. A dose

of 370MBq (10 mCi) of FDG was injected intravenously and the

patients rested in a quiet room. After a 4560-min uptake period,

patients were taken for scanning. In the PET-CT system, CT acqui-

sition was performed on spiral dual slice CT with a slice thickness

of 4 m m and a pitch of 1. Image was acquired using a matrix of

512512pixels and pixel size of about 1mm. After transmission

scan, 3D PET acquisition was done for 35min per bed position

for one/two bed position. PET data were acquired using matrix of

128128 pixels with a slice thickness of 1.5 mm. CT based attenu-

ation correction of the emission images was employed. PET images

werereconstructedby iterativemethod ordered subset expectation

maximization (2 iterations and 8 subsets). Reconstructed images

were displayed and analyzed in transverse, sagittal and coronal

views.

2.3. MRIimaging

MR imaging were performed on a 1.5-T clinical MR imag-

ing unit (Sonata/Avanto, Siemens, Germany) and images were

acquired using a standard head coil. Transaxial T1-weighted and

T2 weighted images were obtained from the second cervical ver-

tebral body to the vertex. Slice thickness was adjusted to 1mm.

Contrast-enhanced images were also obtained after intravenous

administrationof Gadopentetatedimeglumine (Gd-DTPA)at a dose

of 0.1mmol/kg using standard procedures.

2.4. Interpretation of images

PET-CT images were evaluated independently by two expe-

rienced Nuclear Medicine physicians. They were blinded to

the clinical and structural imaging findings. PET-CT images

were interpreted as positive for recurrent tumour if there

was a definite lesion on CT images which was hyperme-

tabolic/isometabolic/hypometabolic on PET images or if there was

an increased focal FDG uptake without any clearly discernible

lesion on CT. MRRadiologist was also blinded to clinical and PET-

CT findings. Gd-DTPA enhancing lesions were considered positive

for recurrence in MRI images.

2.5. Gold standard

Combination of clinical follow up, repeat imaging and biopsy

(when available) were takenas gold standard.Patients whohad dis-

ease related adverse event, progressive disease on imaging and/or

positive biopsy were taken positive for recurrence.

2.6. Statistical analysis

Various descriptive statistics such as mean, median, range and

standard deviation (SD) were used to describe the baseline clinicaland demographic profiles of all the patients. Sensitivity, specificity,

positive predictivevalue (PPV), negative predictivevalue (NPV)and

accuracy with 95% confidence interval were calculated for each

modality. McNemar test was used to see the difference between

diagnostic accuracies of the modalities. Statistical package STATA

8.0(Stata Corporation, College Station, TX, USA) and SPSS 16.0(SPSS

Inc., Chicago, IL, USA) were used for all the statistical analyses.

3. Results

3.1. Patient characteristics

A total of 90 patients with mean age of 36.79 (1.25) years and

age range of 1268 years were evaluated. Patient characteristicsincluding sex, primary location of tumour, histology, grade, and

primary therapy are summarized in Table 1.

3.2. Follow up outcome

On the basis of clinical follow up, repeat imaging and/or biopsy

59 patients were positive and 31 patients were negative for recur-

rence. All patients were followed up for a period of at least 6

months. Twenty eight out of the total 90 patients had a disease

related adverse event. Five patients were re-operated and all of

them were found positive at histopathology (GBM-2 and anaplas-

tic astrocytoma-3). Repeat imaging at follow up was done in the

remaining 55 patients and showed persistent or progressive dis-

ease in 26 patients.

3.3. Results of MRI

MRI was positive for recurrence in 80 patients and negative in

10 patients. Table 2 shows the overall and grade wise sensitiv-

ity, specificity, positive predictive value (PPV), negative predictive

value (NPV) and accuracy of MRI. Mean lesions size obtained from

contrast enhanced area in positive cases was 3.41cm (0.40cm)

and median size was 3.3 cm (range 1.17.2 cm).

3.4. Results of FDG PET-CT

FDG PET-CT was positive for recurrence in 42 and negative in

48 patients. Table 2 shows the overall and grade wise sensitiv-

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510 A. Santra et al. / European Journal of Radiology81 (2012) 508513

Table 1

Patients characteristics.

Parameter No. of Patients

Sex

Male 66

Female 24

Type of glioma

GBM 16

Astrocytoma 35

Oligodendroglioma 24Mixed glioma 10

Others 5

Primary site of glioma

Corpus callosal 7

Temporal 24

Frontal 33

Parietal 18

Multilobar 3

Posterior fossa 5

Histopathologic grade of primary tumour

Grade I 9

Grade II 37

Grade III 28

Grade IV 16

Primary treatment received

Sx + RT 48

Sx + RT + CT 34

Sx or RT 8 (2 + 6)

Treatment given after evaluation of recurrence

No treatment 51

Temozolamide 31

RT + CT 3

Re-Sx 5

GBM: glioblastoma multiforme; Sx: surgery; RT: radiotherapy.

ity, specificity, positive predictive value (PPV), negative predictive

value (NPV) and accuracy of FDG PET-CT.

3.5. Comparison between MRIand FDGPET-CT

Overall, MRI washighly sensitive(95%)and with poor specificity

(23%) fordetection of recurrence. In contrast,FDG PET-CThas lowersensitivity(70%) and higherspecificity (97%). Comparison of overall

and grade wise sensitivity, specificity, PPV, NPV and accuracy of

FDG PET-CT and MRI are given in Table 2.

FDG PET-CT and MRI findings were concordant in 52 patients

(Fig. 1). There was discordance between the findings of MRI and

FDGPET-CT in remaining 38 patients (Fig. 2). On McNemar analysis

the difference was statistically significant (p< 0.001). FDG PET-CT

was negative in all of these 38 patients while MRI was positive

in all (Table 3). Twenty out of these 38 cases were true negative

based on Gold standard. MRI was false negative only in 3 patients

(GBM-2; Grade II-1). In contrast FDG PET-CT was false negative in

18 patients (GBM-6; Grade III-7; Grade II-2; Grade I-3). There were

24 false positive cases on MRI but only one false positive case in

FDG PET-CT (Table 3). Moreover, FDG PET-CT was able to correctlydelineate mixed lesion of recurrent tumour and radiation necrosis

in 11 patients (Figs. 1 and 3).

4. Discussion

Contrast enhancement of brain tumours depends on BBB dam-

age. Necrosis induced by therapy or occurring spontaneously

during tumour progression may also show contrast enhancement

and hence cannot be distinguished reliably from a recurrent solid

tumour after therapy [46]. In addition, uptake of contrast agent

may be substantially reduced by dexamethasone given for reduc-

ing cerebral edema [16]. The fact that morphological imaging often

does not adequately reflect the underlying tumour biology and its

metabolic activity imposes considerable demand to develop alter- T

able

2

Sensitivity,specificity,PPV,NPVandaccuracyofFDGPET-CTandMRIindetectionofrecurrenceglioma;overallandinpatientswithdifferenthisto

pathologicalgrades(with95%CI).

Parameter

Overall

GBM

GradeIII

GradeII

GradeI/others

PET/CT

MRI

PET/CT

MRI

PET/CT

MRI

PE

T/CT

MRI

PET/CT

MRI

Sensitivity

69.5

%(5680.5

)

94.9

%(8

4.998.7

)

50%(22.377.7

)

83.3

%(50.997.1)

68.2

%(45.185.3

)

100%(81.5100)

90

%(66.998.2

)

95%(73.199.7

)

40%(7.38

3)

100%(46.3100)

Specificity

96.8

%(81.599.8

)

22.9

%(1

0.341.5

)

100%(39.6100)

25%(1.378.1

)

83.3

%(36.599.1

)

33.3

%(675.9

)

10

0%(56.1100)

17.6

%(4.744.2

)

100%(39.6

100)

25%(1.378.1

)

PPV

97.6

%(85.999.9

)

70%(58.679.5

)

100%(51.7100)

76.9

%(4693.8)

93.8

%(67.799.7

)

84.6

%(64.395)

10

0%(78.1100)

57.6

%(39.474)

100%(19.8

100)

62.5

%(25.989.8

)

NPV

62.5

%(47.375.5

)

70%(35.491.9

)

40%(13.772.6

)

33.3

%(1.897.5)

41.7

%(16.571.4

)

100%(19.8100)

77

.8%(40.296.1

)

75%(21.998.7

)

57.1

%(20.288.2

)

100%(5.5100)

Accuracy

80%

70%

62.5

%

67%

71%

86%

95

%

59%

67%

67%

CI:confidenceinterval;PPV:positivepredictivev

alue;NPV:negativepredictivevalue;GBM:gliob

lastomamultiforme.

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Fig. 1. A 35 year female with right temporal Grade II astrocytoma, primarily treated with Surgery and Radiotherapy presented with severe headache and seizures. (A)

Transaxial T1W MRI showing large hypointense temporoparietal lesion, (B) Transaxial T1W contrast enhanced MRI showing intense contrast enhancement; findings aresuggestive of recurrent tumour,(C) FDG PET and (D) FDG PET-CT images showing temporoparietallesion with intense FDG uptake; findings are positive for recurrence. The

lesion seen in MRI includes both viabletumour and necrotic area.FDG PET-CTeffectively delineateviable tumourfrom necrotic area. High FDG uptake in recurrent tumour

suggested higher grade transformation. Patient died within 3 weeks of PET-CT scan.

Fig. 2. A 66 years old male patient of right frontal GBM primarily treated with complete surgical removal, radiotherapy and temozolamide. (A)Transaxial T1W contrast

enhanced MRI showing contrast enhancing lesion in the right frontoparietal area, suggestive of recurrent tumour. (B) FDG PET-CT was negative, suggestive of radiation

necrosis. This patient was followed up for>1.5 years and was fine without any further treatment.

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512 A. Santra et al. / European Journal of Radiology81 (2012) 508513

Table 3

FDG PET-CTand MRI findings in all patients with different primary grades.

Parameter Overall GBM Grade III Grade II Grade I/others

PET/CT MRI PET/CT MRI PET/CT MRI PET/CT MRI PET/CT MRI

TP 41 56 6 10 15 22 18 19 2 5

FP 1 24 0 3 1 4 0 14 0 3

TN 30 7 4 1 5 2 17 3 4 1

FN 18 3 6 2 7 0 2 1 3 0

TP: true positive; TN: true negative; FP: false positive; FN: false negative; GBM: glioblastoma multiforme.

Fig. 3. A 40 years male with right frontal Oligoastrocytoma, primarily treated with Surgery and Radiotherapy. The patient was symptomatic at the time of evaluation. (A)

Transaxial T1W contrast enhanced MRI showing contrast enhancing lesion in the posterior margin of right posterior frontal gliotic cavity, (B) FDG PET and (C) FDG PET-CT

images reveal two foci of intense FDGuptake at the posterior margin of the posterior frontal gliotic cavity suggestive of recurrent tumour and an area of radiation necrosis

in between.

native imaging modalities to correctly characterize the lesions. PET

with F18-FDG can identify the metabolic activity of the lesion, so

it can potentially differentiate recurrent tumour from post radi-

ation or post surgical changes [11,12]. Steroids, when used to

control cerebral edema have no effect on the FDG uptake though

it affects grey and white matter differentiation [17]. However,FDG PET has certain limitations. Firstly, grey matter of the brain

also show increased FDG uptake. Secondly, except for very high-

grade tumours (Grade IV-Glioblastoma) most of the tumours are

isometabolic or hypometabolic compared to adjacent grey mat-

ter; hence it is very difficult to differentiate them from normal

brain tissue. Fusion imaging with CT can overcome some of these

limitations. As per published literature overall sensitivity of FDG

PET is about 8090% and specificity varied from 50 to 90% [11,12].

Belohlavek et al. evaluated 29 patients to compare the role of FDG

PETandMRI in the diagnosisof recurrentglioma andconcludedthat

MRI has higher sensitivity (95.8%) and diagnostic accuracy (86%),

whereas FDG PET has better specificity (83.3%) [14]. Another study

by Chen et al. in 23 patients of suspected recurrence showed that

overall diagnostic accuracy of FDG PET is better than that of MRI[15]. In our study, we found that MRI is highly sensitive (95%) for

detection of recurrence but it has very low specificity and a large

number of false positive results which impacts its overall diagnos-

tic accuracy. Being a metabolic marker, FDG shows no uptake in

the necrotic area and hence it can clearly exclude the possibilities

of viable tumour in that area. This is reflected in very high speci-

ficity of FDG PET-CT (97%). The diagnostic accuracy was also better

than that of MRI (80% vs. 70%) in our study. On subgroup analysis

specificity of MRI remained very poor in patients with tumours of

all grades.

High-grade gliomas have very poor survival rates even with

optimal treatment [18]. Grade I tumours arevery slow growing and

usually cured with primary treatment. On the contrary, recurrent

Grade II gliomas invariably transform to anaplastic grade. These

groupsof patients need more attentionas earlydetection andtreat-

ment of recurrence can improve the survival [19,20]. Interestingly,

FDG PET-CT had 90% sensitivity and 95% accuracy in detecting

recurrence in the patients with grade II gliomas along with very

high specificity (100%). Another advantage of FDG PET-CT is in

cases where there is mixed lesion of recurrent tumour and radi-ation necrosis. In these cases FDG PET-CT can clearly delineate

the metabolically active area and necrotic area so that the actual

tumour volume could be determined. This can accurately guide

radiotherapy planning or surgery.

Although FDG PET-CT fares well in overall diagnosis, its high

false negative rate is of a major concern. Moreover due to high nor-

mal brain uptake of FDG and lack of definite lesion in CT, some

lesions were missed. Because of lower sensitivity FDG PET-CT it

may notbe wise to use it as a primary screening modality fordetec-

tion of recurrence in glioma patients. It might be prudent to use

it to characterize any abnormal lesion found on MRI. The present

study has certain limitations. Although total number of patients

in this study was enough for statistical analysis, the numbers of

patients in each subgroup based on histological grade were rela-tively less. Hence anyinference derived from this study needs to be

revalidated with a larger study with sufficient number of patients

in each subgroup. Also, histopathological confirmation of recurrent

tumour was available only in 5 patients.

5. Conclusion

FDG PET-CT is a highly specific modality for detecting recur-

rencein patients with gliomas and can effectivelyexclude radiation

necrosis and other therapy related changes. However, MRI has

higher sensitivity, therefore, a combination of these two modali-

ties or better still hybrid imaging in the form of PET-MRI might be

more useful in these group of patients.

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