Preoperative assessment of peritoneal carcinomatosis: intraindividual ...

ª Springer Science+Business Media, LLC 2012

Abdominal Imaging

Abdom Imaging (2012) DOI: 10.1007/s00261-012-9881-7

Preoperative assessment of peritoneal carcinomatosis: intraindividual comparison of 18F-FDG PET/CT and MRI Bernhard Daniel Klumpp,1 Nina Schwenzer,1 Philip Aschoff,2 Stephan Miller,4 Ulrich Kramer,1 Claus D. Claussen,1 Bjoern Bruecher,3 Alfred Koenigsrainer,3 Christina Pfannenberg1 1

Department for Diagnostic and Interventional Radiology, Eberhard Karls University Tuebingen, University Hospital Tuebingen, Hoppe-Seyler-Str. 3, 72076 Tu¨bingen, Germany 2 Diakonie Klinikum Stuttgart, Su¨dwestdeutsches PET-Zentrum, Seidenstr. 47, 70174 Stuttgart, Germany 3 Department for General, Visceral and Transplantation Surgery, University Hospital Tuebingen, Hoppe-Seyler-Str. 3, 72076 Tu¨bingen, Germany 4 Radiologiepraxis Dr. Aicher, Dr. Ko¨lbel, Prof. Dr. Miller, Uhlandstr. 8, 72072 Tu¨bingen, Germany

Abstract Objective: Exact determination of localization and extent of peritoneal carcinomatosis (PC) before peritonectomy and hyperthermic intraperitoneal chemotherapy (HIPEC) is crucial for the clinical outcome. Our study compares dynamic contrast enhanced 3D MRI (T1wDCE) and 18F-FDG PET/CT regarding diagnostic accuracy in correlation with surgical exploration (SE) and histological (HI) results. Materials and methods: 15 patients with PC were examined on a 1.5T MRI and 16 slice PET/CT. MRI: coronal T1wDCE covering the complete abdomen (0.15 mmol Gd-chelate/kg BW, 2000 mL mannitol solution p.o., 40 mg buscopan i.v.). PET-CT: contrast enhanced 16slice CT (120 mL ultravist 370 i.v., 1000 mL mannitol solution p.o., 40 mg buscopan i.v.), PET: 350 MBq 18-FDG i.v., 3 min acquisition time/bed, 60 min after tracer injektion). Assessment by two independent, experienced observers in correlation with results of SE and HI for each abdominal segment based on the peritoneal cancer index (PCI) proposed by Sugarbaker and co-authors. Results: MRI and PET/CT provided reliable detection of PC. One patient had to be excluded from statistical analysis. In summary, 182 segments were assessed (13/ patient, 14 patients, one patient excluded from statistical

Correspondence to: Bernhard Daniel Klumpp; email: bernhard. [email protected]

analysis). PC was found in 118 by MRI, 124 by PET/CT. 4 segments were classified false positive for MRI, 2 for PET/CT. False negative segments (MRI: 17, PET/CT: 9) did not result in irresectability. Positive predictive value for PC/segment was 97/98%, negative predictive value 73/84%, sensitivity 87/93%, specificity 92/96%, and diagnostic accuracy 88/94% (MRI/PET/CT). Conclusion: With high diagnostic accuracy for PC of both, MRI and PET/CT, PET/CT provides better diagnostic accuracy and especially better NPV. Key words: Peritoneal carcinomatosis—HIPEC— Peritonectomy—MRI—PET/CT

In a variety of tumor entities peritoneal carcinomatosis (PC) occurs in an advanced state of the disease. The prognosis of patients with PC is poor [1, 2]. During recent years, new techniques to cope with this situation were assessed. One promising approach with curative intention is total peritonectomy combined with multivisceral resection of all involved viscera and additional hyperthermic intraperitoneal chemotherapy (HIPEC). The aim is complete cytoreduction to ensure tumor-free survival as the ultimate goal [3, 4]. To select patients for peritonectomy and HIPEC in which complete cytoreduction is achievable, meticulous preoperative assessment of size and localization of all tumor manifestations is mandatory [5, 6].

B. D. Klumpp et al.: Preoperative assessment of peritoneal carcinomatosis

At present, several imaging modalities are available which have the potential to identify manifestations of PC. The challenge for all imaging techniques is to provide a maximum of diagnostic accuracy in the identification of PC to enable the surgeon with information necessary for complete cytoreduction [3]. Besides established abdominal imaging techniques including ultrasound [7] and computed tomography [8], recent studies indicate high diagnostic yield for 18F-FDG PET/CT [9] and contrast enhanced MRI [10] in the preoperative assessment of PC. Compared to CT, MRI provides superior soft tissue contrast beneficial for the detection of PC. The pathological vascularization of involved peritoneum results in increased contrast enhancement enabling the identification of PC by MRI as contrast enhancing nodules or regional contrast enhancement of peritoneal structures [11]. Due to differences in the vascularization in different tumor entities, the acquisition of several phases after contrast injection seems to be favorable to identify increased contrast enhancement of involved structures reliably [12]. For the assessment of PC by PET/CT, 18F-Fluorodesoxyglucose (FDG) is used providing information regarding the metabolic activity of tissue. With an increase of metabolic activity in malignant tissue due to its rapid growth, 18-F FDG PET/CT can identify PC by increased tracer uptake and correlation of the tracer distribution with anatomic structures depicted by contrast enhanced computed tomography [13, 14]. Manifestations of PC appear either as hypermetabolic nodules or as regional increased tracer uptake of involved peritoneal structures [9]. Both techniques are capable to depict morphological findings of PC including ascites, peritoneal masses, thickening of parietal, or visceral peritoneum as well as adhesions of parietal and visceral peritoneum [15–19]. In summary, MRI [20] and PET-CT [21, 22] are both regarded to be suitable imaging techniques for the assessment of PC. The aim of our study was to compare the diagnostic performance of 18F-FDG PET/CT and multiphase contrast enhanced MRI in the preoperative assessment of patients with PC before peritonectomy and HIPEC. Standard of reference was surgical exploration (SE) and histopathological assessment.

Materials and methods Patient group 15 Patients with histologically proven PC were included, eleven female, four male. All patients were willing to participate and written informed consent was obtained. Mean age was 57.9 ± 8.8 years. Underlying diseases included ovarian and turabian cancer (n = 6), colorectal cancer (n = 3), carcinoma of the appendix vermiformis

Fig. 1. T1wDCE MRI image in coronal angulation (A) and c corresponding coronal reconstruction of multidetector CT (C) as well as PET/CT fusion image (B) of a 56-year-old female patient with PC, PCI was rated 12 on MRI and 14 on PET/CT. Diffuse thickening of the small bowl, increased regional contrast enhancement of the visceral peritoneum (segment 8, right flank, 0, central, 4, left flank, and 5 left lower, 9–12 small bowl) on MRI and CT images (A, C) as well as correlating increased metabolic activity (B) represent extensive micronodular spread of PC.

(n = 5), and malignant mesothelioma (n = 1). One 52-year-old female patient with ovarian cancer was excluded from the statistical analysis, as the interval between MRI and PET/CT as well as peritonectomy and HIPEC was 3 months and therefore comparability could not be regarded as accurate. In the remaining 14 patients, the interval between MRI and PET/CT was 1.9 ± 2.1 days, the interval between PET/CT and HIPEC was 8.4 ± 6.5 days. Both examinations were performed for clinical reasons before peritonectomy when planning the surgical procedure. All patients included in the study underwent complete SE independent of previous radiological findings.

MRI Patient preparation before MRI included oral administration of 2000 mL 2.5% mannitol solution for intestinal distension and intravenous injection of 40 mg butylscopolaminiumbromid to suppress intestinal motion. MR examinations were performed on a 1.5T whole body system using two-phased array surface coils (Magnetom Avanto, Siemens Health Care, Erlangen, Germany). A 3D gradient echo sequence (T1w DCE) was acquired in coronal angulation before contrast injection and 35, 70, and 105 s, respectively after injection of 0.15 mmol gadolinium chelate per kilogram body weight at a flow rate of 2 mL/s (TR 2.9 ms, TE 1.1 ms, flip angle 18°, slice thickness 1.8 mm, matrix 256 9 256, receiver band width 560 Hz/pixel, acceleration factor 3, GRAPPA algorithm, spatial resolution 2.0 9 2.0 9 1.8 mm). In addition, T2-weighted TSE sequences and contrast enhanced 2D gradient echo sequences were acquired in coronal and transversal angulations.

18F-FDG PET/CT Patient preparation before PET/CT included oral administration of 1000 mL 2.5% mannitol solution for intestinal distension and intravenous injection of 40 mg butylscopolaminiumbromid to suppress intestinal motion. 350 MBq of 18F-FDG were injected intravenously 60 min prior image acquisition. Patients rested during the uptake time to prevent increased uptake of skeletal



musculature. PET/CT examinations were performed on a 16-slice whole body PET/CT system (Hi-Rez Biograph 16, Siemens Health Care, Knoxville, TN, USA). The system consists of a high resolution three-dimensional LSO PET (FoV 155 mm, slice thickness 4.25 mm) and a 16 row multidetector spiral CT (peak voltage 120 kV, tube current 120–250 mA, rotation time 0.5 s, collimation 0.75/1.5 mm (thorax/abdomen), table feed 12/ 24 mm). The spiral CT included low-dose CT scan for attenuation correction, chest scan in arterial contrast phase, abdomen scan in portovenous contrast phase after contrast injection of 120 mL iopromidium intravenously containing 370 mg iodine/mL at a flow rate of 3 mL/s followed by 40 mL saline chaser injection. PET data were acquired over 6–7 beds depending on patient size with 3 min acquisition time for each bed (FoV 128 mm, zoom 1.0, 4 iterations, 8 subsets). Patients were positioned in a vacuum mat to reduce motion of the body and consequent misalignment of PET and CT images. Image fusion of PET and CT data as well as postprocessing was performed on a dedicated PET-CT workstation (TrueD, Siemens Health Care, Erlangen, Germany). Image reconstruction of CT images included axial reconstruction with 5 mm slice thickness and 5 mm increment as well as coronal reconstruction with 3 mm slice thickness and 2 mm increment.

Image analysis MRI and PET/CT images were assessed by two independent experienced readers regarding presence, size and localization of PC manifestations based on the peritoneal cancer index (PCI) proposed by Sugarbaker and co-authors [23]. Readers were aware of the presence of PC in all patients but blinded for surgical results. Images were assessed digitally in three planes (axial, coronal, and sagittal). Standard of reference was surgical PCI based on complete exploration of the peritoneal cavity with histopathological sampling. According to the PCI, there are 13 peritoneal segments of which four are intestinal segments including upper- and lower-jejunum as well as upper- and lower-ileum. Each segment could be assigned zero to three points with zero = no lesion identified, one = lesion up to 0.5 cm in maximum diameter, two = lesion exceeding 0.5 cm but not 5 cm in maximum diameter and three = lesion or confluent lesions exceeding 5 cm in maximum diameter. The resulting PCI score ranges between zero and 39. Sensitivity, specificity, positive and negative predictive values and the resulting diagnostic accuracy was calculated for MRI and PET/CT. Results were correlated with surgical findings (Pearson correlation coefficient, 95% confidence interval) and compared for PET/CT and MRI (t test). Segments suspected of PC by MRI and PET/CT, respectively, were rated correct positive if PC had been confirmed by SE and histopathology, otherwise false positive. Segments not suspected of PC by MRI and PET/

Fig. 2. T1wDCE MRI (A), PET/CT (B), and CT (C) images c of a 68-year-old female patient with PC arising from appendix carcinoma. PCI was rated 36 on MRI as well as PET/CT. Besides massive ascites, contrast enhancement and tracer uptake of the visceral peritoneum covering the small bowl as well as mesenterial trunk and the greater omentum are markedly increased. Omental cake (long forward arrow), and involvement of the visceral peritoneum of the small bowl (long reverse arrow), adhesions of visceral and parietal peritoneum in the right upper abdomen (segment 1) (short arrow) indicate PC. PET/CT images visualize increased metabolic activity along the right hemidiaphragm (arrow head) without obvious correlation on CT and T1DCE MRI images suspicious of PC manifestations which was confirmed histopathologically.

CT, respectively, were rated correct negative if PC had not been identified by SE and histopathology, otherwise false negative. The inter-observer agreement was also calculated. p values of 0.05) (Table 2). Also the number of false positive and negative segments for PET/ CT is lower compared to MRI (Table 2). The difference of false segments is not significant, either (p > 0.05). The inter observer agreement for the presence or absence of PC per segment was very good for both imaging modalities (MRI/PET/CT: kappa = 0.84/0.98). Regarding lesion size scores, the inter observer agreement was kappa = 0.79/0.94. The correlation coefficient for MRI/PET/CT and SE was 0.74/0.86 (p < 0.01) regarding the presence/ absence of PC per segment based on PCI. Regarding also lesion size scores, the correlation coefficient was 0.72/0.80 (p < 0.01) as assessed by reader 1 (Table 3a). The correlation coefficient for MRI/PET/CT and SE was 0.70/0.83 (p < 0.01) regarding the presence/absence of PC per segment and 0.68/0.79 (p < 0.01) regarding also the lesion size score as assessed by reader 2 (Table 3b). The correlation of the PCI per patient with surgical results was 0.90/0.90 (p < 0.01) (reader 1/2), the inter observer agreement kappa = 0.82 for MRI and 0.94/0.90



Table 1. The statistical analysis of the diagnostic performance of 18F-FDG PET/CT and MRI in 14 patients with PC reveal for both readers better results for PET/CT in comparison to MRI, especially regarding specificity and NPV, yet the difference is not significant PCI Reader 1 MRI PET/CT Reader 2 MRI PET/CT

DA (%)

Sensitivity (%)

Specificity (%)

PPV (%)

NPV (%)

19.5 ± 12.8 19.6 ± 11.6

88 94

87 93

92 96

97 98

73 84

19.4 ± 12.4 20.4 ± 11.6

87 93

87 92

86 94

94 98

72 83

Table 2. 13 Segments of the peritoneal cavity according to the PCI by Sugarbaker and co-authors were assessed in 14 patients with proven PC by two experienced independent readers for PET/CT and MRI as well MRI 182 segments

PET/CT

Positive

Negative

Positive

Negative

114 4

47 17

122 2

49 9

114 7

44 17

121 3

48 10

Reader 1 Correct False Reader 2 Correct False

In contrast to otherwise similar results, the number of false negative segments is higher for MRI compared with PET/CT

(p < 0.01) (reader 1/2) for PET/CT, the inter observer agreement kappa = 0.83.

Discussion The occurrence of PC in oncologic patients is generally associated with a poor prognosis [1]. One new therapeutic approach is total peritonectomy combined with multivisceral resection of all involved viscera and HIPEC [3]. In order to benefit from this potentially curative therapeutic concept, complete cytoreduction has to be achieved [4]. Consequently, there is a demand for reliable preoperative imaging to allow for optimal patient selection and planning of the extensive surgical procedure [24, 25]. Most widespread imaging techniques are ultrasound and computed tomography [26, 27]. Both techniques provide first of all morphological information enabling detection of peritoneal masses and nodules as well as ascites as most frequent signs of PC [27, 28]. For all imaging techniques, exact information regarding the extent and localization of

PC is mandatory [29]. Especially the differentiation between scar tissue due to previous surgery and the identification of micronodular PC without circumscript tumor is challenging for imaging techniques mainly relying on morphology [28]. As a consequence, there is a desire for imaging techniques providing more information about tissue characteristics. These requirements are met in different ways by MRI and 18F-FDG PET/CT. MRI provides excellent soft tissue contrast depicting more discrete changes of tissue [30] and multiphasic image acquisition covering a certain period of time after injection of paramagnetic contrast media providing information about tissue vascularization [31]. 18F-FDG PET/CT provides metabolic information enabling the identification of malignant lesions due to its augmented glucose consumption [13, 32]. This can be monitored by radioactive isotopes linked to desoxyglucose which is incorporated but not metabolized by glucose consuming tissue resulting in increased tracer uptake of PC [14]. Both techniques are suitable to depict PC with improved results compared with CT and ultrasound as they allow to a certain degree differentiation of malignant and benign lesions either by their vascularization or their glucose metabolism, thus providing information not available from techniques primarily relying on morphological assessment [31, 32]. This is of special interest in the case of micronodular spread of PC and involvement of the small bowl. Our results indicate better diagnostic accuracy and interobserver agreement as well as better correlation with surgical findings for PET/CT in comparison to MRI although the difference is not significant. Especially the number of false negative segments is lower for PET/CT which might be of importance when deciding

Table 3. PCI (Sugarbaker and co-authors) for each patient for MRI and PET/CT as assessed by reader 1 (a) and reader 2 (b) Pat

1

2

3

4

MRI PET/CT

39 39

36 36

4 4

5 3

MRI PET/CT

39 39

35 39

4 4

5 3

5

6

7

8

9

10

11

12

13

14

15

3 8

38 34

12 14

35 30

11 11

Na Na

18 18

18 17

17 19

15 18

22 24

6 11

39 34

11 13

33 31

11 11

Na Na

17 20

15 17

18 20

17 19

22 24

a b

Patient number 10 was excluded from statistical analysis due to the long time interval between MRI, PET/CT and peritonectomy


about surgical options. The reason might be that MRI is less robust regarding image quality. 15 of 17 false negative segments were found in patients with poor or moderate image quality indicating a strong correlation of image quality depending on patient compliance, especially breath hold capacity, and diagnostic accuracy. In contrast, PET/CT provided reliably good image quality in all patients reflected by better diagnostic accuracy and correlation with surgical findings. In theory, MRI should provide more detailed information on small bowl involvement compared to PET/CT, as the high resolution 3D T1w DCE sequence provides superior spatial resolution compared with PET and shorter image acquisition time being less affected by intestinal peristaltic. However, MRI is less robust regarding breathing or body motion artifacts resulting in reduced image quality with restricted diagnostic accuracy, which was the case in four out of 14 patients for MRI but not for PET/CT. Consequently, MRI enables at least equal diagnostic yield in the case of good or excellent image quality compared with PET/CT, especially regarding small bowl involvement, but suffers from restricted image quality in patients with low compliance corrupting its diagnostic yield. Thus, regarding the complete patient group, the performance of PET/CT for the detection of PC was superior compared to MRI, probably due to its superior robustness. Another asset of PET/CT is the coverage of the whole body providing information about the presence of distant metastases, for example lung or skeletal (except pelvis and lumbar spine, which are also covered by MRI) metastases which exclude the patient from peritonectomy and HIPEC [25]. In our study, none of the patients, however, was found to have extra abdominal metastases. Still, there are limitations of our study. First of all, the presence of PC in all patients was known previously, as this was inclusion criterion for our study. This introduces a bias since readers aware of the presence of PC are supposed to classify discrete or uncertain findings more likely as PC. Further, the mean PCI was rather high ranging around 20 for both readers for PET/CT and MRI as well. This might result in a statistical bias, as an increased amount of malignant tissue is more likely to be identified correctly resulting in better sensitivity as well as positive predictive value. Thus, the diagnostic accuracy of both methods might be lower in patients with less widespread PC or even uncertain presence of PC, which cannot be clearly predicted from our results. In spite of good results for MRI and PET/CT, the detection of diffuse micronodular spread and small bowl involvement is challenging and to some extent still unsatisfactory, whereas macronodular manifestations and involvement of parietal peritoneum can be identified with ease by both methods. In conclusion, both multiphasic contrast-enhanced MRI as well as 18F-FDG PET/CT are valuable tools for the preoperative assessment of PC before peritonectomy

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