Abstract
Purpose
This study evaluated the usefulness of semiquantitative and volumetric PET parameters for predicting prognosis in patients with advanced gastric cancer (AGC).
Methods
We enrolled 213 patients who underwent 18F-fluoro-2-deoxyglucose positron emission tomography/computed tomography (18F-FDG PET/CT) prior to curative surgery for AGC. Maximum standardized uptake value (SUVmax) and tumor-to-liver uptake ratio (TLR) were measured in all patients. Metabolic tumor volume (MTV) and total lesion glycolysis were measured in volume-measurable patients. For further quantification of FDG uptake, we developed PET prognostic scores by combining SUVmax and MTV (1: low SUVmax/low MTV; 2: high SUVmax/low MTV; 3: high SUVmax/high MTV). Comparison of PET parameters between recurrence and non-recurrence groups was performed. Univariate and multivariate analyses for recurrence-free survival (RFS) and overall survival (OS) were subsequently performed.
Results
The recurrence rate was 32.4% (69/213 patients). Mean SUVmax and mean MTV of the recurrence group were significantly higher than those of the non-recurrence group (p = 0.026 and p = 0.025). TLR showed marginal significance (p = 0.051). In multivariate analysis for RFS including all patients, SUVmax (p = 0.022), TLR (p = 0.010), and PET score (p = 0.003) were independent prognostic factors. In post hoc analysis of PET score, significant differences in RFS were observed between PET scores 2 and 3 as well as scores 1 and 3. No significant difference in RFS was observed between scores 1 and 2. Only PET score was statistically significant for OS in univariate analysis. None of the PET parameters were statistically significant for OS in multivariate analysis.
Conclusion
High SUVmax and high MTV of the primary tumor suggest a high risk of recurrence for AGC patients. Even if SUVmax is similar, the prognosis may vary depending on MTV. Combining PET parameters results in a better prediction for prognosis.
Similar content being viewed by others
References
Jung KW, Won YJ, Kong HJ, Lee ES. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2015. Cancer Res Treat. 2018;50:303–16.
Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–86.
Song M, Lee H-W, Kang D. Epidemiology and screening of gastric cancer in Korea. J Korean Med Assoc. 2015;58:183.
Eom BW, Jung KW, Won YJ, Yang H, Kim YW. Trends in gastric cancer incidence according to the clinicopathological characteristics in Korea, 1999-2014. Cancer Res Treat. 2018;50:1343–50.
Ang TL, Fock KM. Clinical epidemiology of gastric cancer. Singap Med J. 2014;55:621–8.
Kostakoglu L, Agress H Jr, Goldsmith SJ. Clinical role of FDG PET in evaluation of cancer patients. Radiographics. 2003;23:315–40 quiz 533.
Yamada A, Oguchi K, Fukushima M, Imai Y, Kadoya M. Evaluation of 2-deoxy-2-[18F]fluoro-D-glucose positron emission tomography in gastric carcinoma: relation to histological subtypes, depth of tumor invasion, and glucose transporter-1 expression. Ann Nucl Med. 2006;20:597–604.
Stahl A, Ott K, Weber WA, et al. FDG PET imaging of locally advanced gastric carcinomas: correlation with endoscopic and histopathological findings. Eur J Nucl Med Mol Imaging. 2003;30:288–95.
Atay-Rosenthal S, Wahl RL, Fishman EK. PET/CT findings in gastric cancer: potential advantages and current limitations. Imaging Med. 2012;4:241–50.
Yun M. Imaging of gastric cancer metabolism using 18 F-FDG PET/CT. J Gastric Cancer. 2014;14:1–6.
Filik M, Kir KM, Aksel B, et al. The role of 18F-FDG PET/CT in the primary staging of gastric cancer. Mol Imaging Radionucl Ther. 2015;24:15–20.
Mukai K, Ishida Y, Okajima K, Isozaki H, Morimoto T, Nishiyama S. Usefulness of preoperative FDG-PET for detection of gastric cancer. Gastric Cancer. 2006;9:192–6.
Moon SH, Hyun SH, Choi JY. Prognostic significance of volume-based PET parameters in cancer patients. Korean J Radiol. 2013;14:1–12.
Mochiki E, Kuwano H, Katoh H, Asao T, Oriuchi N, Endo K. Evaluation of 18F-2-deoxy-2-fluoro-D-glucose positron emission tomography for gastric cancer. World J Surg. 2004;28:247–53.
Kim J, Lim ST, Na CJ, et al. Pretreatment F-18 FDG PET/CT parameters to evaluate progression-free survival in gastric cancer. Nucl Med Mol Imaging. 2014;48:33–40.
Lee JW, Lee SM, Lee MS, Shin HC. Role of 18F-FDG PET/CT in the prediction of gastric cancer recurrence after curative surgical resection. Eur J Nucl Med Mol Imaging. 2012;39:1425–34.
De Potter T, Flamen P, Van Cutsem E, et al. Whole-body PET with FDG for the diagnosis of recurrent gastric cancer. Eur J Nucl Med Mol Imaging. 2002;29:525–9.
Coupe NA, Karikios D, Chong S, et al. Metabolic information on staging FDG-PET-CT as a prognostic tool in the evaluation of 97 patients with gastric cancer. Ann Nucl Med. 2014;28:128–35.
Chung HW, Lee EJ, Cho YH, et al. High FDG uptake in PET/CT predicts worse prognosis in patients with metastatic gastric adenocarcinoma. J Cancer Res Clin Oncol. 2010;136:1929–35.
Park JC, Lee JH, Cheoi K, et al. Predictive value of pretreatment metabolic activity measured by fluorodeoxyglucose positron emission tomography in patients with metastatic advanced gastric cancer: the maximal SUV of the stomach is a prognostic factor. Eur J Nucl Med Mol Imaging. 2012;39:1107–16.
Sano T, Sasako M, Kinoshita T, Maruyama K. Recurrence of early gastric cancer. Follow-up of 1475 patients and review of the Japanese literature. Cancer. 1993;72:3174–8.
Huang J, Huang L, Zhou J, et al. Elevated tumor-to-liver uptake ratio (TLR) from 18F-FDG-PET/CT predicts poor prognosis in stage IIA colorectal cancer following curative resection. Eur J Nucl Med Mol Imaging. 2017;44:1958–68.
Washington K. 7th edition of the AJCC cancer staging manual: stomach. Ann Surg Oncol. 2010;17:3077–9.
Uchino S, Noguchi M, Ochiai A, Saito T, Kobayashi M, Hirohashi S. p53 Mutation in gastric cancer: a genetic model for carcinogenesis is common to gastric and colorectal cancer. Int J Cancer. 1993;54:759–64.
Berger KL, Nicholson SA, Dehdashti F, Siegel BA. FDG PET evaluation of mucinous neoplasms: correlation of FDG uptake with histopathologic features. Am J Roentgenol. 2000;174:1005–8.
Alakus H, Batur M, Schmidt M, et al. Variable 18F-fluorodeoxyglucose uptake in gastric cancer is associated with different levels of GLUT-1 expression. Nucl Med Commun. 2010;31:532–8.
Kawamura T, Kusakabe T, Sugino T, et al. Expression of glucose transporter-1 in human gastric carcinoma: association with tumor aggressiveness, metastasis, and patient survival. Cancer. 2001;92:634–41.
Karimi P, Islami F, Anandasabapathy S, Freedman ND, Kamangar F. Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol Biomark Prev. 2014;23:700–13.
Cenitagoya GF, Bergh CK, Klinger-Roitman J. A prospective study of gastric cancer. ‘Real’ 5-year survival rates and mortality rates in a country with high incidence. Dig Surg. 1998;15:317–22.
Schauer M, Peiper M, Theisen J, Knoefel W. Prognostic factors in patients with diffuse type gastric cancer (linitis plastica) after operative treatment. Eur J Med Res. 2011;16:29–33.
Zheng H, Takahashi H, Murai Y, et al. Pathobiological characteristics of intestinal and diffuse-type gastric carcinoma in Japan: an immunostaining study on the tissue microarray. J Clin Pathol. 2007;60:273–7.
Deng J-Y, Liang H. Clinical significance of lymph node metastasis in gastric cancer. World J Gastroenterol. 2014;20:3967–75.
Kamimura K, Nagamachi S, Wakamatsu H, et al. Role of gastric distention with additional water in differentiating locally advanced gastric carcinomas from physiological uptake in the stomach on 18F-fluoro-2-deoxy-D-glucose PET. Nucl Med Commun. 2009;30:431–9.
Imperiale A, Cimarelli S, Sellem DB, Blondet C, Contantinesco A. Focal F-18 FDG uptake mimicking malignant gastric localizations disappearing after water ingestion on PET/CT images. Clin Nucl Med. 2006;31:835–7.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
Hye Ryeong Kwon, Kisoo Pahk, Sungsoo Park, Hyun Woo Kwon, and Sungeun Kim declare that they have no conflict of interest.
Ethical Statement
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed Consent
The institutional review board of our institute approved this retrospective study (AN17196-001) and the requirement to obtain informed consent was waived.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kwon, H.R., Pahk, K., Park, S. et al. Prognostic Value of Metabolic Information in Advanced Gastric Cancer Using Preoperative 18F-FDG PET/CT. Nucl Med Mol Imaging 53, 386–395 (2019). https://doi.org/10.1007/s13139-019-00622-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13139-019-00622-w