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Usefulness of FDG PET for Assessment of Early Recurrent Epithelial Ovarian Cancer

OBJECTIVE.

The purpose of our study was to evaluate the diagnostic accuracy of FDGpositron emission tomography (PET) in comparison with CT in detecting recurrent ovariancarcinoma and its ability to reveal small tumor recurrence.

MATERIALS AND METHODS.

We reviewed the records of 31 consecutive patientswith pathologically proven epithelial carcinoma who underwent FDG PET 1 month beforesecond-look surgery to assess recurrent tumor. Of these 31 patients, 21 patients also under-went CT 1 month before second-look surgery. The diagnostic accuracies of FDG PET (

n

=31), CT (

n

= 21), and combined FDG PET and CT (

n

= 21) in detecting recurrent tumor werecalculated and compared with each other using the Bennett’s test in 21 patients who under-went both imaging studies. Detection rates of individual tumors relative to their sizes werecompared between FDG PET and CT using the McNemar test.

RESULTS.

The sensitivity, specificity, and accuracy of FDG PET, CT, and combined FDGPET and CT for revealing recurrent ovarian cancer were 45.3%, 99.7%, 91.0%; 54.5%,99.6%, 91.7%; 58.2%, 99.6%, 92.4%, respectively. We found no statistically significant dif-ference in the diagnostic accuracy of FDG PET, CT, and combined FDG PET and CT (

χ

2

<5.991). Detection rates of tumor nodules found on CT were significantly greater than those onFDG PET when nodule size was 0.3–0.7 cm (

p

< 0.05).

CONCLUSION.

FDG PET did not improve the overall diagnostic accuracy in detectingrecurrent ovarian carcinoma compared with CT. Rather, FDG PET was inferior to CT in itsability to reveal small-tumor recurrence.

ecurrence is a major problem forpatients with epithelial ovariancancer. During the early postoper-

ative period, a peritoneal disseminated lesionis the most common form of recurrence. De-tection of a small volume of tumor recurrencein patients with epithelial ovarian cancer onpreoperative imaging has always been impera-tive because patients with tumor recurrencewith optimal disease found at second-look sur-gery have a better prognosis than those withsuboptimal disease [1–3]. Surgical debulkingis considered optimal if the diameter of thelargest residual tumor is 2 cm or less and sub-optimal if the diameter of the largest tumor ismore than 2 cm at second-look surgery [1–3].

Clinical evaluation with tumor markers orphysical examination is of little diagnosticvalue in the early detection and localization ofrecurrent ovarian tumor, leading to a relianceon imaging. CT is the most commonly useddiagnostic technique before second-look sur-gery. However, CT is limited in revealing

small lesions; even if the lesion is detected, CTcannot confirm the lesion as a tumor recur-rence if it is too small. Recently, several re-ports have evaluated the usefulness of FDGpositron emission tomography (PET) in re-vealing recurrent ovarian carcinoma [4–11].However, to our knowledge, no reports showthe diagnostic value of FDG PET for the de-tection of small tumor recurrence. The purposeof our study was to evaluate the value of FDGPET for diagnosis of recurrent ovarian carci-noma in comparison with CT and its ability toreveal small tumor recurrence.

Materials and Methods

We reviewed the records of 31 consecutive pa-tients with surgically and pathologically proven epi-thelial carcinoma who were treated between January1996 and March 2000. These patients underwentFDG PET 1 month before undergoing second-looksurgery to assess recurrent tumor. Of these 31 pa-tients, 21 patients also underwent CT. The range be-tween CT and second-look surgery, FDG PET and

Song-Mee Cho

1

Hyun Kwon Ha

2

Jae Young Byun

1

Jae Mun Lee

1

Chan Joo Kim

3

Sung Eun Nam-Koong

3

Joon Mo Lee

3

Received September 25, 2001; accepted after revision February 13, 2002.

1

Department of Radiology, College of Medicine, The Catholic University of Korea, Seocho-Ku, Seoul, South Korea.

2

Department of Radiology, University of Ulsan College of Medicine, Asan Medical Center, 388-1 Poongnap-Dong Songpa-Ku, Seoul, South Korea.

3

Department of Gynecology, College of Medicine, The Catholic University of Korea, 505 Banpo-Dong, Seocho-Ku, Seoul, South Korea. Address correspondence to J. M. Lee.

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2002;179:391–395

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© American Roentgen Ray Society

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second-look surgery, and CT and FDG PET was 5–30days (mean, 17 days) , 3–20 days (mean, 13 days),and 3–18 days (mean, 5 days), respectively. The pa-tients who underwent CT or FDG PET more than 1month before second-look surgery were excludedfrom our study. Patients ranged in age from 17 to 70years (mean age, 46 years). The pathologic cell typesof the 31 epithelial ovarian carcinomas included se-rous cystadenocarcinoma (

n

= 17), mucinous cystade-nocarcinoma (

n

= 7), endometrioid carcinoma (

n

= 3),clear cell carcinoma (

n

= 2), and undifferentiated orpoorly differentiated carcinoma (

n

= 2). At second-look surgery, the presence or absence of tumor at 15specific sites was recorded; these sites included ab-dominal and pelvic lymph nodes, diaphragm, omen-tum, mesentery, gastric surface, splenic hilum, hepaticsurface, serosa of the large and small bowels, para-colic gutter, peritoneum of the anterior abdomen andpelvis, rectal serosa, and vaginal stump. The tumormasses, if present, were excised by debulking surgery,and blinded biopsies were performed at each site evenwhen no apparent gross mass was present.

FDG PET imaging was performed using anECAT Exact 47 scanner (Siemens, Knoxville, TN)with a slice thickness of 5.1 and a zoom of 1.0 forwhole-body coronal, sagittal, and axial images and aslice thickness of 3.5 and a zoom of 1.5 for regionalpelvic axial images. Transmission scanning was per-formed using a germanium-68 rotating rod sourceduring a 20-min acquisition for attenuation correc-tion of regional pelvic images. Patients were injectedIV with 370 MBq of FDG. After an uptake period of45 min, whole-body emission scanning was initiatedwith six sequential images from the level of the mid-dle auditory canal to the thigh. Emission scanningwas then performed during a 30-min acquisitionfor attenuation-corrected regional pelvic images.Regional pelvic images were acquired as a set of si-nograms and were reconstructed by a filtered back-projection method. To limit artifacts, the patientswere asked to fast for 12 hr and to drink more than500 mL of water. All patients received 5 mg of IVfurosemide (Lasix; Han dok-Aventis pharma, Seoul,Korea) and were catheterized to reduce bladder ac-tivity. In addition, diazepam (10 mg by mouth) (Val-ium; Roche, Seoul, Korea) was used routinely toreduce FDG uptake in the skeletal muscles. The

standardized uptake value was calculated from theamount of injected FDG, the patient’s body weight,and the soft-tissue uptake of FDG in the regional im-ages with the attenuation correction.

CT was performed using a Somatom Plus scan-ner (Siemens, Erlangen, Germany) with an 8- to 10-mm slice thickness and interval. A total of 100 mLof iopromide 62.3% (Ultravist 300; Schering, Berlin,Germany) was injected as a bolus at a rate of 2–3mL/sec using a mechanical injector. Incremental orhelical scanning from the diaphragm to the symphy-sis began 45 sec after starting the IV injection ofcontrast medium.

Two radiologists retrospectively interpreted thesame CT scans together without the knowledge ofhistopathologic results or other imaging findings andcame to a consensus on the CT findings. If recurrenttumor manifested as a nodule on CT, the size andsite of each nodule were evaluated. Miliary perito-neal seeding was considered to be present whenperitoneal thickening and contrast enhancement wasvisualized on CT.

A nuclear medicine specialist retrospectively in-terpreted the FDG PET scans. This specialist wasalso unaware of the histopathologic results or otherimaging findings. Whole-body coronal, sagittal, ax-ial, and regional axial black-and-white images wereviewed on a computer screen. If a hypermetaboliclesion manifested as a nodule on FDG PET, the sizeand site of each nodule were evaluated. Estimationof lesion size on FDG PET was based on correlationwith CT. If the nodule on the attenuation-correctedpelvic image was more than 2 cm in diameter, thestandardized uptake value was measured [12]. If thenodule was less than 2 cm in diameter and it was onthe outside of the pelvis, semiquantitative and visualanalysis were used in the image interpretation for tu-mor recurrence [13]. On FDG PET, peritoneal seed-ing was considered present when FDG uptake wasprominent on the peritoneal lining and on the sur-faces of the solid organs. The presence of tumor re-currence was evaluated on CT and FDG PET usingthe following three-level confidence score: 0, absent;1, equivocal; 2, present. On FDG PET, the presenceof a hypermetabolic lesion with a standardized up-take value of more than 3 was considered positivefor tumor recurrence (score 2), and suspected tumor

recurrence with FDG uptake on visual analysis wasconsidered an equivocal lesion (score 1). Scores 1and 2 were considered positive for tumor recurrenceon CT and FDG PET.

The sensitivity, specificity, accuracy, and positiveand negative predictive values were evaluated forthe 15 specific sites on FDG PET (

n

= 31), CT (

n

=21), and combined FDG PET and CT (

n

= 21).These were compared with the results of second-look surgery. Furthermore, these diagnostic accura-cies were compared with each other using Bennett’stest [14] in 21 cases in which both FDG PET andCT were performed.

The detection rate of FDG PET and CT was evalu-ated for all tumor nodules confirmed at second-looksurgery. To calculate the detection rates for a specifictumor size, we included the number of nodules in thedenominator that were larger than the tumor size; thenumber of correctly detected nodules was the nomi-nator. Detection rates of tumors relative to their sizeswere calculated and compared between FDG PETand CT using the McNemar test. Tumor sizes mea-sured at second-look surgery and standardized uptakevalues of nodules of more than 2 cm were also evalu-ated on FDG PET.

Results

Of the 31 patients with epithelial ovariancancer, 16 patients had recurrent ovarian carci-noma, and findings in 15 patients were nega-tive for tumor recurrence at second-looksurgery after first-line therapy. Eight of the 16patients with recurrent ovarian carcinoma hadoptimal disease, whereas the remaining eighthad suboptimal disease. Twelve of the 16 pa-tients with recurrent ovarian carcinoma hadmiliary peritoneal seeding (Figs. 1 and 2).

The overall lesion-based sensitivity, speci-ficity, accuracy, positive predictive value, andnegative predictive value of FDG PET (

n

=31), CT (

n

= 21), and combined FDG PET andCT for revealing recurrent ovarian carcinomafor 15 specific sites were 45.3%, 99.7%,91.0%, 97.1%, 90.5%; 54.5%, 99.6%, 91.7%,96.8%, 91.2%; 58.2%, 99.6%, 92.4%, 97.0%,

Fig. 1.—41-year-old woman with recurrent ovariancancer in pelvis.A, Contrast-enhanced CT scan obtained at level of hipjoint shows two nodular enhancing lesions (arrows) inpelvis, one just above vaginal stump and second in leftpelvic peritoneum. Both lesions were missed on CT. B, Regional axial FDG positron emission tomogramshows two nodular lesions (arrows) in pelvis.

A B

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91.8%, respectively (Table 1). When lesion-based and patient-based diagnostic accuracieswere compared among FDG PET, CT, andcombined FDG PET and CT in 21 patients whounderwent both imaging studies, no statisticallysignificant difference was seen for diagnosticaccuracies (

χ

2

< 5.991). Fifty-one recurrent tumor nodules were

confirmed at second-look surgery. The size ofthe tumor nodules ranged from 0.3 to 4.0 cm

(mean, 1.1 cm). Detection rates of tumor rela-tive to size on FDG PET and CT at 0.3, 0.4,0.5, 0.6, and 0.7 cm were significantly greateron CT than those for FDG PET (

p

< 0.05)(Fig. 3). Although statistically insignificant, tu-mor detection rates for FDG PET were inferiorto those on CT between 0.7 and 1.8 cm. Thestandardized uptake values of FDG from thesemeasurable tumors of more than 2 cm in diam-eter were 3.7–16.5 (mean, 8.1).

Discussion

The treatment trends for patients with epi-thelial ovarian carcinoma include initial surgi-cal staging with aggressive primarycytoreduction followed by multidrug chemo-therapy [15]. Second-look surgical reassess-ment may be performed in patients who havecompleted a planned course of treatment todocument disease remission, restaging, andsecondary cytoreduction, as well as to evaluate

Fig. 2.—39-year-old woman with recurrent ovarian cancer in peritoneum. A, Contrast-enhanced CT scan obtained at level of liver shows smooth linear contrast enhancement(arrows) along hepatic surface. B, Contrast-enhanced CT scan obtained at level of mid abdomen shows subtle nodular linear contrast en-hancement (arrows) at peritoneum along right paracolic gutter. C, Whole-body coronal image of FDG positron emission tomogram shows strong FDG uptake at hepatic sur-face (arrows) and peritoneum (arrowheads) along both paracolic gutters. Urine in bladder (B) also showsFDG uptake.

A B C

Note.—Numbers in parentheses are the data used to calculate the percentages.aOverall diagnostic accuracies of FDG PET and CT were compared in 21 cases in which both FDG PET and CT were performed using Bennett’s test [14]. There was no statistically significant dif-

ference of diagnostic accuracies between FDG PET and CT when both sensitivity and specificity were simultaneously compared ( χ2 < 5.991).

TABLE 1 Diagnostic Accuracy of FDG PET and CT for Revealing Recurrent Ovarian Tumor at 15 Specific Sites

Accuracy

FDG PET (n = 31) and (n = 21a)

Sensitivity (%) Specificity (%) Accuracy (%) Positive Predictive Value (%) Negative Predictive Value (%)

(n = 31) (n = 21) (n = 31) (n = 21) (n = 31) (n = 21) (n = 31) (n = 21) (n = 31) (n = 21)

Lesion-based 45.3 (34/75) 36.4 (20/55) 99.7 (389/390) 99.6 (259/260) 91.0 (423/465) 88.6 (279/315) 97.1 (34/35) 95.2 (20/21) 90.5 (389/430) 88.1 (259/294)Patient-based 81.3 (13/16) 81.8 (9/11) 93.3 (14/15) 90.0 (9/10) 87.1 (27/31) 85.7 (18/21) 92.9 (13/14) 90.0 (9/10) 82.4 (14/17) 81.8 (9/11)

CT (n = 21a)

Lesion-based 54.5 (30/55) 99.6 (259/260) 91.7 (289/315) 96.8 (30/31) 91.2 (258/283)Patient-based 100 (11/11) 90.0 (9/10) 95.2 (20/21) 91.7 (11/12) 100.0 (9/9)

Combined FDG PET and CT (n = 21a)

Lesion-based 58.2 (32/55) 99.6 (259/260) 92.4 (291/315) 97.0 (32/33) 91.8 (259/282)Patient-based 100 (11/11) 90.0 (9/10) 95.2 (20/21) 91.7 (11/12) 100.00 (9/9)

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the response to multidrug chemotherapy. How-ever, this invasive procedure involves the ex-pense and discomfort of major abdominalsurgery and results in disruption of the pa-tients’ normal activities. Furthermore, recur-rent ovarian carcinoma occurs in 20–50% ofall patients even after the findings of second-look surgery are negative [16–20]. Anothergroup of researchers documented the overallrate of morbidity at 19% [21]. Problems withsecond-look surgery have led clinicians to seekother techniques such as peritoneoscopy formonitoring response to therapy [22].

There is a clear need for accurate, noninva-sive diagnostic imaging to formulate an opti-mal therapeutic strategy for patients withresidual or recurrent ovarian carcinoma and tomonitor tumor response to therapy. Diverseimaging techniques have been used for thispurpose. Among the imaging techniques, CTis most often used before second-look surgery.CT has considerable limitations revealing smallperitoneal implants, which are the most com-mon presentation of recurrent epithelial ovariancancer. The overall sensitivity of CT for re-vealing residual tumor or tumor recurrence isreported to be in the range of 40–61% [23–29].In addition, CT cannot definitely confirm tu-mor recurrence when only small nodular le-sions are detected. To overcome these inherent

limitations of CT, other diagnostic techniques,such as PET, CT with intraperitoneal adminis-tration of contrast material [30, 31], and ra-dioscintigraphy using indium or various tumormarkers, are alternative methods [32–34].

Several reports have suggested that FDGPET can reveal lesions otherwise missed on CTin recurrent ovarian carcinoma [4–9]. FDG PETis a form of computer-assisted imaging that pro-duces images reflecting the biochemistry of tis-sues rather than their physical characteristics. Ithas the potential to reveal the biochemical dif-ferences between normal and malignant tissuesin primary and metastatic malignancies. Forthese reasons, reassessment with FDG PET be-fore second-look surgery in recurrent ovariancarcinoma is gaining acceptance because of thepossibility for tumor confirmation when theconventional imaging findings are inconclusive.However, FDG PET also has limitations in re-vealing small lesions because the clarity of thetechnique is hampered by the metabolic activityof the tumor.

In our study, FDG PET did not improveoverall diagnostic accuracy in revealing recur-rent ovarian carcinoma compared with CT. Al-though patient-based diagnostic values of FDGPET for revealing recurrent ovarian cancer werecomparable to those of other reports [4–9], theoverall lesion-based diagnostic accuracy of

FDG PET was much lower. In addition, FDGPET was inferior to CT in revealing small tu-mors in patients with recurrent ovarian carci-noma. Although in the report by Karlan et al. [6]the researchers could identify tumors of approx-imately 1.0 cm in diameter using FDG PET, wefound detection rates for the nodules of less than1.0 cm in diameter to be poor—lower than 50%in our study. As a result, we suggest that FDGPET should not be used as a routine screeningtechnique for the detection of recurrent tumor inpatients with recurrent ovarian carcinoma inwhich disseminating small peritoneal seeding iscommon. Furthermore, FDG PET cannot beperformed in patients with suboptimal diseasein detecting tumor foci considering the same de-tection rates as those of CT for nodules that aremore than 1.8 cm in diameter. However, addi-tional analysis of sensitivity, specificity, and ac-curacy based on the combined FDG PET andCT subset in the 21 patients who had both stud-ies showed a slight improvement in sensitivitywithout a corresponding decline in specificity.This finding suggests that an appropriate furtherstudy would reveal the marginal value of FDGPET in those patients with a negative or equivo-cal result on CT.

The principal limitation of this study wasthat the FDG PET technique might have lim-ited the sensitivity of PET in our study. Specif-ically, because the transmission imaging wasperformed before the injection of FDG, the po-tential for patient motion was present. Wemade every effort to maintain the exact posi-tion before and after the FDG injection bymarking the position on the patient using anExact ECAT PET scanner. The use of mea-sured attenuation correction rather than seg-mented attenuation correction increased thenoisiness of the attenuation-corrected images.Also, we used only non–attenuation-correctedimages outside the pelvis, which would beconsidered a limitation by many. Finally, theuse of filtered back-projection as the recon-struction method rather than an iterative recon-struction method was another factor limitingthe sensitivity of our PET technique. There-fore, further study with a new FDG PET tech-nique might be warranted.

There are well-known problems with FDGPET. This technique is poor in determining thelocation of a lesion with only faintly revealed an-atomic landmarks. To increase spatial resolu-tion and allow localization of the tumor foci,other researchers have used a fusion imagewith anatomic imaging such as CT [6, 35,36]. Another recognized problem with FDGPET is the false-positive and false-negative re-

00

20

40

60

80

100

1

Tumor Size (cm)

2 3 4

Det

ecti

on

Rat

e (%

)

Fig. 3.—Graph shows detection rates for specific tumor sizes on FDG positron emission tomography (dotted line)and CT (solid line). To calculate detection rates for specific tumor size, we included all nodules in denominatorthat were larger than tumor size. Tumor detection rates on CT for tumors of diameters 0.3-, 0.4-, 0.5-, 0.6-, and 0.7-cm significantly exceeded those for FDG PET (p < 0.05).

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sults. We experienced one false-positive resultwith an infected pseudocyst; other observersalso reported false-positive results in patientswith recurrent ovarian carcinoma on FDG PET[4, 5, 9]. Such results are unavoidable becauseFDG uptake is dependent on the metabolic rateof the imaged tissue. We experienced anotherfalse-positive result with FDG in the ureter oninitial interpretation. Differentiation of physio-logic colonic (bowel wall and lumen) and urineactivity from tumor uptake of FDG is a difficulttask. However, we could differentiate miliary tu-mor implants from bowel by tracing the physio-logic FDG uptake on sequential FDG PETimages. This task was not easy. Also, we experi-enced one false-negative result when FDG PETwas performed 11 days after the completion ofchemotherapy. The protocol for FDG PET at ourinstitution is to perform the technique at least 3weeks after the completion of chemotherapy toreduce false-negative results. When this patientunderwent FDG PET 10 days later, recurrent tu-mor was detected.

In conclusion, FDG PET did not improvethe overall diagnostic accuracy for detectingrecurrent ovarian carcinoma compared withCT. Rather, FDG PET was inferior to CT in itsability to reveal small tumor recurrence.

Acknowledgments

We thank Yong Gyu Park for statisticalanalysis of the study; Dae Keun Lo, Jane Lo,and Shi Jung Lo for assistance with manu-script preparation; and Gi Jeong Cheon andJung Mi Park for data analysis and interpreta-tion of FDG PET images.

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