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ORIGINAL ARTICLE
Year : 2019  |  Volume : 15  |  Issue : 1  |  Page : 142-147

Preoperative assessment of malignant potential of gastrointestinal stromal tumor by dual-time-point 18F-fluorodeoxyglucose positron emission tomography imaging: Usefulness of standardized uptake value and retention index


1 Department of Family Medicine, Korea University College of Medicine, Seoul, Korea
2 Department of Diagnostic Radiology, PET Center, Yale University, New Haven, CT, USA
3 Department of Nuclear Medicine, Korea University College of Medicine, Seoul, Korea
4 Department of Radiology, Korea University College of Medicine, Seoul, Korea
5 Department of Nuclear Medicine, The State University of New York at Buffalo, Buffalo, NY, USA
6 Department of Surgery, Division of Upper Gastrointestinal Surgery, Korea University College of Medicine, Seoul, Korea

Date of Web Publication13-Mar-2019

Correspondence Address:
Dr. Sungsoo Park
Department of Surgery, Division of Upper Gastrointestinal Surgery, Korea University Anam Hospital, Korea University College of Medicine, Inchon-ro 73, Seongbuk-gu, Seoul 02841
Korea
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_1093_16

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 > Abstract 


Background: To evaluate the usefulness of preoperative imaging with F-18 fluorodeoxyglucose positron emission tomography (FDG-PET) for noninvasive risk assessment of gastrointestinal stromal tumor (GIST).
Materials and Methods: A retrospective review including 32 patients with pathologically proven GIST. Preoperative FDG-PET scan results including maximum standardized uptake values (SUVs) of the GISTs at 1 h postinjection (SUV1) were available for all tumors and SUVs at 2 h postinjection (SUV2) were available for 22 tumors. When both SUV1 and SUV2 were available, a retention index (RI, %) was calculated, and the correlation of these PET parameters with the histopathologic results was analyzed.
Results: SUV1 was significantly higher in tumors in the high-risk group (6.0 ± 2.7) compared to those in the low risk (3.0 ± 1.6) or very low-risk (2.7 ± 1.2) groups (P = 0.009 and 0.011, respectively). At a cutoff of 5.2, the SUV1 demonstrated sensitivity of 80% and a specificity of 89% for predicting high-risk GISTs. Tumor size was significantly correlated with SUV1 (r = 0.68, P < 0.001) and SUV2 (r = 0.66, P = 0.001), and SUV1, SUV2, and RI were significantly higher in tumors with mitotic index > 5/50 high-power field than in those with lower mitotic index. RI was significantly higher in tumors with C-kit mutation than in those with no C-kit mutation.
Conclusion: SUV1 measured during preoperative FDG-PET imaging correlated well with malignant potential of GISTs, especially for high-risk versus Low-/very-low-risk tumors. RI values correlated well with mitotic counts and C-kit mutation, suggesting that this mutation may have some influence on tumor metabolism.

Keywords: Gastrointestinal stromal tumor, positron emission tomography, retention index, standardized uptake value


How to cite this article:
Kwon Y, Park E, Pahk K, Kim S, Kim MJ, Graf D, Park S. Preoperative assessment of malignant potential of gastrointestinal stromal tumor by dual-time-point 18F-fluorodeoxyglucose positron emission tomography imaging: Usefulness of standardized uptake value and retention index. J Can Res Ther 2019;15:142-7

How to cite this URL:
Kwon Y, Park E, Pahk K, Kim S, Kim MJ, Graf D, Park S. Preoperative assessment of malignant potential of gastrointestinal stromal tumor by dual-time-point 18F-fluorodeoxyglucose positron emission tomography imaging: Usefulness of standardized uptake value and retention index. J Can Res Ther [serial online] 2019 [cited 2019 Dec 13];15:142-7. Available from: http://www.cancerjournal.net/text.asp?2019/15/1/142/243466




 > Introduction Top


Gastrointestinal stromal tumors (GISTs) are the most common mesenchymal neoplasm of the gastrointestinal tract.[1],[2] To establish the best treatment strategy for the patient with GIST, it is important to confirm the diagnosis and to evaluate the malignant potential of primary GISTs.[3],[4] Current risk stratification systems are based on tumor size, mitotic count, and tumor location,[1] with size and/or mitotic index considered the most important predictors of malignant potential.

Attempts at preoperative pathologic diagnosis of GIST through endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) are reported, while percutaneous biopsy is not recommended because of the risk of hemorrhage and intra-abdominal tumor dissemination.[2] However, it remains difficult to obtain sufficient tissue specimens for adequate tumor characterization by EUS-FNA. Enhanced computed tomography (CT) is now recognized as the imaging modality of choice to characterize the abdominal mass in terms of its extent and the presence or absence of metastasis during the initial staging workup of biopsy-proven GISTs, although CT cannot predict the malignant or metastatic potential.[2]

F-18 fluorodeoxyglucose positron emission tomography (FDG-PET) imaging has been used to evaluate ambiguous findings or suspicious metastatic lesions seen on CT or magnetic resonance imaging, for differentiating recurrent from nondescript benign changes and for monitoring tumor response to imatinib mesylate treatment.[5],[6],[7] F-18 FDG-PET is considered superior to anatomic imaging for evaluation of treatment response and a PET Response Assessment Criteria (PRECIST) has been proposed for clinical reporting.[8] A few results from small series have shown that there is a potential role for F-18 FDG-PET imaging in predicting the malignant potential of GISTs,[9],[10],[11] but more evidence is needed before wider clinical application can be recommended.

In this study, we evaluated results of preoperative F-18 FDG-PET scans to explore the potential of F-18 FDG-PET for predicting malignant potential of GISTs. F-18 FDG-PET imaging results were compared with postoperative histopathologic risk stratification results using maximum standardized uptake values (SUVs) and a calculated retention index (RI), which also allowed us to investigate the utility of dual-time-point FDG-PET imaging for providing additional information in the characterization of the tumor biology of GISTs.


 > Materials and Methods Top


Patients

The institutional review board approved the protocol (No. ED09059) for this retrospective analysis of 39 patients who had suspected GIST on endoscopic examinations or confirmed GIST on endoscopic FNA biopsy. All patients had abdominal CT scans and whole-body FDG-PET scans for tumor characterization and staging during the initial pretreatment evaluation. GIST was confirmed at surgery in 35 patients and endoscopic FNA biopsy in four patients. Three of the 35 operated patients were found to have other tumors and were excluded from the final analysis (Castleman's disease in 1, leiomyoma in 2). None of the four patients who were confirmed to have GISTs by FNA biopsy underwent surgery; 3 of them had localized and presumably resectable tumors but had significant comorbidity and the other one had concurrent pancreatic cancer with multiple hepatic metastases. Therefore, 32 patients with confirmed GISTs were included in the final analysis.


 > F-18 Fluorodeoxyglucose Positron Emission Tomography Imaging Top


F-18 FDG-PET images were acquired within 1 month before initiation of treatment using a Gemini TF PET/CT scanner from Philips Medical Systems (Cleveland, OH, USA). All patients fasted for ≥ 6 h before FDG injection and blood glucose levels ≤ 200 mg/dL were confirmed before scanning. Patients were scanned from the skull base to the mid-thigh level approximately 1 h after injection of 370–480 MBq of FDG, and additional delayed imaging of the abdominopelvic region (from xiphoid process to pelvic floor level) was performed at 2-h postinjection in 22 patients.

Fluorodeoxyglucose positron emission tomography image analysis

The maximized SUV on the FDG-PET images of GIST lesions were measured using a volume-of-interest (VOI) method, wherein a sphere-shaped VOI that covered the entire lesion was drawn for each patient and the SUV at 1 h following the injection of FDG was determined (SUV1). For the 22 patients who had additional delayed FDG-PET scanning of the abdomen region at 2-h postinjection, SUV at 2-h postinjection (SUV2) was measured, and for these patients, a RI (%) was calculated by dividing the difference between SUV2 and SUV1 by SUV1 and multiplying by 100. RI was used to express the degree change in FDG uptake by the GIST lesion over time. Two independent investigators (E.P. and K.P.) measured the values and disagreements were not found.


 > Histopathology Top


Pathologic results included tumor size, surgical margin status, immunohistochemical staining profile, and tumor mitotic index. Lesions in which immunohistochemical analyses were positive for KIT (CD117) were considered GISTs. Other mesenchymal tumors that were positive for desmin were diagnosed as myogenic tumors, and those positive for S-100 were diagnosed as neurogenic tumors. The GISTs were divided into four groups according to the National Institutes of Health (NIH) consensus criteria.[12] Mitotic figures for all samples were counted in 50 randomly selected high-power fields (HPFs) by an experienced pathologist.

Detection of KIT and platelet-derived growth factor gene mutations

Results of KIT and platelet-derived growth factor (PDGFR) gene mutation analyses were available for 12 tumors. Formalin-fixed paraffin-embedded (FFPE) tumor tissue samples were taken before imatinib treatment and genomic DNA was extracted from the tumor sample using the OMEGA Bio-Tek Inc.E.Z.N.A FFPE DNA Kit (Norcross, GA, USA). Polymerase chain reaction amplification and mutational analyses of KIT exon 11 were performed initially and in samples negative for KIT exon 11 mutations subsequent amplification with primers specific for KIT exons 9, 13, and 17 was performed. When no KIT mutations were identified, additional mutational analyses were conducted for exons 12 and 18 of the PDGFR gene.

Statistical analyses

Analysis of variance was used to compare the metabolic parameters (SUV1, SUV2, and RI) of the GIST lesions among different risk groups. When results were significant, Tukey's post hoc test was performed to compare each group. Simple correlation analyses were made using Pearson's correlation coefficient as a measure of linear association between metabolic and histopathologic parameters. Multiple linear regression analyses were performed to test for significant clinical parameters related to tumor metabolism. Mann–Whitney test was performed to compare genetic mutation status and metabolic parameters. Differences were considered significant when P values were < 0.05. Data were analyzed using SPSS version 20 (SPSS Inc., Chicago, IL, USA).


 > Results Top


Patient characteristics

The mean age of the patients was 60.1 years (standard deviation [SD], 8.0) and 43.8% of them were men [Table 1]. All tumors except for 1 case (small bowel) involved the stomach. The mean tumor size was 5.0 cm (SD, 4.9) and the mean mitotic count was 12.9 (SD, 25.8). By the NIH criteria, there were 5 high-risk GISTs, 3 intermediate-risk tumors, 17 low-risk tumors, and 7 very-low-risk lesions. Ten of 12 tumors tested (83.3%) were positive for the C-kit mutation; risk stratification among these 12 tumors was: very low risk, 1; low risk, 9; intermediate risk, 1; and high risk, 1.
Table 1: Patient characteristics

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Tumor characteristics and National Institutes of Health risk classification

Mean values of tumor size (mean, 15.8; SD, 5.4) and mitosis count (mean, 71.8; SD, 13.2) were highest in the high-risk group [Table 2]. Among the 10 C-kit positive tumors, 8 were in the NIH low-risk category, 1 in the intermediate-risk category, and 1 in the high-risk group. SUV1, SUV2, and RI were all greatest among the high-risk tumors and least among the very-low-risk tumors, but these differences were not significant.
Table 2: Tumor characteristics based on National Institutes of Health risk classification

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Standardized uptake values and retention index as predictors for risk stratification and mutation

SUV1 was significantly higher among the high-risk tumors (mean ± SD 6.0 ± 2.7) compared to low-risk (3.0 ± 1.6) or very-low-risk (2.7 ± 1.2) lesions (P = 0.009 and 0.011, respectively) [Figure 1]. The diagnostic performance of SUV1 for high-risk GISTs was 0.863 [P = 0.011, [Figure 2]] and a cutoff for SUV1 of 5.2 allowed diagnostic sensitivity of 80% and specificity of 89%. SUV1 of intermediate risk tumors was not significantly different from that of high- or low-risk tumors. SUV2 and RI were not significantly different among the different risk groups and were not diagnostic for the risk stratification of GISTs.
Figure 1: Fluorodeoxyglucose metabolism among different risk groups. Standardized uptake value 1 was significantly higher in the high-risk group than in low-risk or very-low-risk groups. Values are means (standard deviations)

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Figure 2: Diagnostic performance of standardized uptake value 1 for high-risk tumors. Using a cutoff 5.2, standardized uptake value 1 predicted high-risk gastrointestinal stromal tumors with sensitivity of 80% and specificity of 89% (area under the curve – 0.863, P = 0.011)

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Tumor size was significantly correlated with both SUV1 (r = 0.68, P < 0.001) and SUV2 (r = 0.66, P = 0.001), but not with RI [Figure 3]. SUV1, SUV2, and RI were significantly higher in tumors with mitotic indices > 5/50 HPF compared to those with mitotic indices of ≤ 5/50 HPF (SUV1 6.6 ± 2.9 vs. 3.2 ± 1.6, P = 0.041; SUV2 10.2 ± 3.9 vs. 3.6 ± 2.1, P = 0.041; RI 45.6 ± 21.6% vs. 9.5 ± 17.9%, P = 0.031).
Figure 3: Correlation between tumor size and the metabolic parameters for gastrointestinal stromal tumors. Both (a) standardized uptake value 1 and (b) standardized uptake value 2 correlated significantly with tumor size

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Six of 10 GIST lesions that tested positive for the C-kit mutation had significantly higher RI values versus 2 tumors that tested negative for the C-kit mutation (25.7 ± 21.9% versus − 9.3 ± 7.0%, P = 0.046); [Figure 4]. The RI values were < 0 in both of the C-kit-negative tumors and in one of the two tumors that tested positive for a PDGFR alpha (PDGFRα) mutation, the RI value (−14.3%) was more negative than that of the tumor with no PDGFRα mutation (−4.3%). Neither SUV1 nor SUV2 was significantly different between tumors with and without C-kit mutations.
Figure 4: Retention index and C-kit mutation. Retention index was significantly higher in tumors with a C-kit mutation than in those without. Values are means (standard deviations)

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In sum, SUV1 correlated with the NIH risk stratification for malignant potential, including tumor size and mitotic count, but not with the genetic mutation analyses [Table 3], while there was a correlation between RI and mitotic count and mutations but not with overall malignant potential.
Table 3: Are standardized uptake value and retention index useful predictors for risk assessment and mutation?

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 > Discussion Top


In our study, preoperative FDG-PET imaging results correlated with the malignant potential of GISTs as determined by postoperative histopathological results. SUV1 correlated with high- and low-/very-low-risk tumors, and at an SUV1 cutoff of 5.2, sensitivity for risk stratification was 80% and specificity was 89%. The RI was calculated by comparing SUV1 and SUV2 and was used as an index of tumor metabolism. This value was higher in GISTs with C-kit mutations than in those without.

The use of preoperative FDG-PET imaging as a noninvasive tool for assessing malignant potential of GISTs has been investigated by several research groups. Kamiyama et al.[9] studied ten patients with gastric GISTs and reported correlation between FDG uptake and histopathologic parameters of the gastric GIST lesions. They found significant correlations between SUV at 40-min postinjection and mitotic index and between SUV and the Ki-67 index, but SUV in their study did not correlate with tumor size. Yamada et al.[10] reported significant correlations between SUV at 50-min postinjection and mitotic index for 21 gastric GIST lesions, as well as correlation between SUV and tumor size. These authors reported good sensitivity and specificity of SUV for classification of malignant potential of GISTs. In agreement with Yamada et al., our study indicated significant correlation was between tumor size and SUV1 (i.e. SUV at 1-h postinjection) as well as significantly higher SUV1 measurements among tumors with mitotic indices of > 5/50 HPF versus those with mitotic indices of ≤ 5/50 HPF. The SUV1 measurements among the high-risk GISTs in our study were significantly higher than those among the very-low or low-risk tumors. Thus, we concluded that SUV1 was able to differentiate high-risk GISTs preoperatively and noninvasively. FDG uptake was well correlated with major histopathologic parameters of GISTs, and our results suggested that FDG-PET may provide useful information regarding the malignant potential of GISTs before surgery.

Furthermore, dual-time-point PET imaging provided additional information in predicting malignant potential of GISTs and possibly in indicating genetic mutation status. During dual-time-point imaging, two scans are acquired after a single-FDG injection, namely, an initial scan and a delayed scans. The utility of dual-time-point imaging for characterizing disease has been reported in studies concerning differential diagnosis of malignant and benign tumors of the head and neck,[13] lung,[14] thorax,[15] and pancreas,[16],[17] as well as for predicting prognosis of pancreatic cancer,[18] and recurrence[19] and long-term survival of head-and-neck cancers.[20] In the present study, SUV results at 2-h postinjection (SUV2) were available for 22 patients, and tumor size was significantly correlated with SUV2. SUV2 and RI were significantly higher in tumors with mitotic indices >5/50 HPF than for those with lower mitotic indices.

A notable finding in the present study was the variation in FDG uptake kinetics measured by RI among GISTs according to genetic mutation status. GISTs are distinct from other sarcomas in that 95% of them are reported to express the transmembrane glycoprotein CD117 (C-kit), which belongs to the Type III receptor tyrosine kinase family,[21],[22] and approximately 80% of them harbor mutations in the genes encoding the KIT receptor tyrosine kinase. It is also reported that 5%–10% of GISTs will have a mutation in the gene encoding the PDGFRα receptor tyrosine kinase.[21],[23] These mutations are important in that they have been correlated with treatment response to imatinib mesylate. GISTs with C-kit mutation had significantly higher RI values than those without the C-kit mutation. The tumors without C-kit mutations had RI values of < 0, with a greater negative RI value in a lesion with a PDGFRα mutation than in one without. Although the number of cases is very small, we speculated that delayed FDG uptake (SUV2) and uptake kinetics (RI) may also bear information on tumor biology and genetic mutation status. Genotyping is considered for advanced GISTs to guide imatinib dose selection and predict treatment response. It is also used to decide whether to deliver adjuvant therapy for moderate-/high-risk primary tumors to delay recurrence. In sunitinib-treated GIST, FDG-PET could be a potential and feasible tool for early sunitinib response assessment[24] and potential predictor for long-term outcome.[25] Preoperative FDG-PET may also help predict postoperative recurrence of GISTs, showing that ring-shaped uptake is an independent adverse prognostic factor of postoperative recurrence.[26] It would be valuable to further investigate the detailed relationship between FDG uptake patterns and genetic mutation status of GISTs, along with its potential for better-predicting treatment responses in individual tumor.

Limitations of this study include its retrospective nonrandomized design. Furthermore, mutation analyses and delayed imaging were not performed in all patients. However, to the best of our knowledge, the current study included the largest number of cases reported thus far, and the evaluation of SUV and RI to assess the malignant potential of GISTs could be highlighted as the strength of this study. More research is necessary to determine whether metabolic parameters derived from FDG-PET reflect prognosis of GISTs. Size and mitotic index by themselves are not perfect, and newer indicators that help to predict the malignant potential and prognosis of GISTs would be welcomed. If FDG-PET is proven to have prognostic value, treatment options could be fine-tuned based on metabolic information from the FDG-PET results. Diagnostic performance of delayed imaging or dual-time-point imaging in categorizing the malignant potential of GISTs also needs to be examined in more detail in larger numbers of patients.


 > Conclusion Top


Preoperative FDG-PET imaging using SUV1 and RI measurements was useful in classifying GISTs according to malignant potential, especially in differentiating high- versus low-/very-low -risk tumors. On the basis of these results, we recommend preoperative evaluation of SUV1 and RI during treatment planning for GISTs patients. C-kit and PDGFRα mutation seemed to have influence on the tumor metabolism, which may predict tumor behavior. Further studies on the relationship between genetic mutation and tumor metabolism are suggested.

Financial support and sponsorship

This work was supported by Korea University Grant (K1031941).

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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