DOI QR코드

DOI QR Code

Preoperative Nodal 18F-FDG Avidity Rather than Primary Tumor Avidity Determines the Prognosis of Patients with Advanced Gastric Cancer

  • Kwon, Hyun Woo (Department of Nuclear Medicine, Korea University Anam Hospital) ;
  • An, Liang (Department of Surgery, Korea University Anam Hospital) ;
  • Kwon, Hye Ryeong (Department of Nuclear Medicine, Korea University Anam Hospital) ;
  • Park, Sungsoo (Department of Surgery, Korea University Anam Hospital) ;
  • Kim, Sungeun (Department of Nuclear Medicine, Korea University Anam Hospital)
  • 투고 : 2018.05.01
  • 심사 : 2018.07.23
  • 발행 : 2018.09.30

초록

Purpose: This study investigated whether the metabolic avidity of primary tumors and/or metastatic lymph nodes (LNs) measured by $^{18}F$-fluorodeoxyglucose ($^{18}F-FDG$) positron emission tomography/computed tomography (PET/CT) was related to survival after surgery in patients with advanced gastric cancer (AGC). Materials and Methods: One hundred sixty-eight patients with AGC who underwent preoperative $^{18}F-FDG$ PET/CT and curative resection were included. The $^{18}F-FDG$ avidity of the primary gastric tumor and LNs was determined quantitatively and qualitatively. The diagnostic performance of $^{18}F-FDG$ PET/CT was calculated, and the prognostic significance of $^{18}F-FDG$ avidity for recurrence-free survival (RFS) and overall survival (OS) was assessed. Results: In all, 51 (30.4%) patients experienced recurrence, and 32 (19.0%) died during follow-up (median follow-up duration, 35 months; range, 3-81 months); 119 (70.8%) and 33 (19.6%) patients showed $^{18}F-FDG$-avid primary tumors and LNs, respectively. $^{18}F-FDG$ PET/CT showed high sensitivity (73.8%) for the detection of advanced pathologic T ($pT{\geq}3$) stage and high specificity (92.2%) for the detection of advanced pN (${\geq}2$) stage. $^{18}F-FDG$ avidity of LNs was significantly associated with RFS (P=0.012), whereas that of primary tumors did not show significance (P=0.532). Univariate and multivariate analyses revealed that $^{18}F-FDG$ avidity of LNs was an independent prognostic factor for RFS (hazard ratio=2.068; P=0.029). Conclusions: $^{18}F-FDG$ avidity of LNs is an independent prognostic factor for predicting RFS. Preoperative $^{18}F-FDG$ PET/CT can be used to determine the risk and prognosis of patients with AGC after curative resection.

키워드

참고문헌

  1. Jung KW, Won YJ, Oh CM, Kong HJ, Lee DH, Lee KH, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2014. Cancer Res Treat 2017;49:292-305. https://doi.org/10.4143/crt.2017.118
  2. Katanoda K, Hori M, Matsuda T, Shibata A, Nishino Y, Hattori M, et al. An updated report on the trends in cancer incidence and mortality in Japan, 1958-2013. Jpn J Clin Oncol 2015;45:390-401. https://doi.org/10.1093/jjco/hyv002
  3. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin 2016;66:7-30. https://doi.org/10.3322/caac.21332
  4. Maehara Y, Hasuda S, Koga T, Tokunaga E, Kakeji Y, Sugimachi K. Postoperative outcome and sites of recurrence in patients following curative resection of gastric cancer. Br J Surg 2000;87:353-357. https://doi.org/10.1046/j.1365-2168.2000.01358.x
  5. Deng N, Goh LK, Wang H, Das K, Tao J, Tan IB, et al. A comprehensive survey of genomic alterations in gastric cancer reveals systematic patterns of molecular exclusivity and co-occurrence among distinct therapeutic targets. Gut 2012;61:673-684. https://doi.org/10.1136/gutjnl-2011-301839
  6. Dulak AM, Schumacher SE, van Lieshout J, Imamura Y, Fox C, Shim B, et al. Gastrointestinal adenocarcinomas of the esophagus, stomach, and colon exhibit distinct patterns of genome instability and oncogenesis. Cancer Res 2012;72:4383-4393. https://doi.org/10.1158/0008-5472.CAN-11-3893
  7. Ajani JA, D'Amico TA, Almhanna K, Bentrem DJ, Chao J, Das P, et al. Gastric cancer, version 3.2016, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2016;14:1286-1312. https://doi.org/10.6004/jnccn.2016.0137
  8. Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D, et al. Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2016;27:v38-v49. https://doi.org/10.1093/annonc/mdw350
  9. Smyth E, Schoder H, Strong VE, Capanu M, Kelsen DP, Coit DG, et al. A prospective evaluation of the utility of 2-deoxy-2-[$^{18}F$]fluoro-D-glucose positron emission tomography and computed tomography in staging locally advanced gastric cancer. Cancer 2012;118:5481-5488. https://doi.org/10.1002/cncr.27550
  10. Baiocchi GL, Marrelli D, Verlato G, Morgagni P, Giacopuzzi S, Coniglio A, et al. Follow-up after gastrectomy for cancer: an appraisal of the Italian research group for gastric cancer. Ann Surg Oncol 2014;21:2005-2011.
  11. Lee JW, Jo K, Cho A, Noh SH, Lee JD, Yun M. Relationship between $^{18}F$-FDG uptake on PET and recurrence patterns after curative surgical resection in patients with advanced gastric cancer. J Nucl Med 2015;56:1494-1500. https://doi.org/10.2967/jnumed.115.160580
  12. Lordick F, Ott K, Krause BJ, Weber WA, Becker K, Stein HJ, et al. PET to assess early metabolic response and to guide treatment of adenocarcinoma of the oesophagogastric junction: the MUNICON phase II trial. Lancet Oncol 2007;8:797-805. https://doi.org/10.1016/S1470-2045(07)70244-9
  13. Ott K, Weber WA, Lordick F, Becker K, Busch R, Herrmann K, et al. Metabolic imaging predicts response, survival, and recurrence in adenocarcinomas of the esophagogastric junction. J Clin Oncol 2006;24:4692-4698. https://doi.org/10.1200/JCO.2006.06.7801
  14. Washington K. 7th edition of the AJCC cancer staging manual: stomach. Ann Surg Oncol 2010;17:3077-3079. https://doi.org/10.1245/s10434-010-1362-z
  15. Song BI, Kim HW, Won KS, Ryu SW, Sohn SS, Kang YN. Preoperative standardized uptake value of metastatic lymph nodes measured by $^{18}F$-FDG PET/CT improves the prediction of prognosis in gastric cancer. Medicine (Baltimore) 2015;94:e1037. https://doi.org/10.1097/MD.0000000000001037
  16. Cerfolio RJ, Bryant AS. Ratio of the maximum standardized uptake value on FDG-PET of the mediastinal (N2) lymph nodes to the primary tumor may be a universal predictor of nodal malignancy in patients with nonsmall-cell lung cancer. Ann Thorac Surg 2007;83:1826-1830. https://doi.org/10.1016/j.athoracsur.2006.12.034
  17. Park J, Byun BH, Noh WC, Lee SS, Kim HA, Kim EK, et al. Lymph node to primary tumor SUV ratio by $^{18}F$-FDG PET/CT and the prediction of axillary lymph node metastases in breast cancer. Clin Nucl Med 2014;39:e249-e253. https://doi.org/10.1097/RLU.0b013e3182a75477
  18. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 2011;14:101-112. https://doi.org/10.1007/s10120-011-0041-5
  19. Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15- year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol 2010;11:439-449. https://doi.org/10.1016/S1470-2045(10)70070-X
  20. Ajani JA, Rodriguez W, Bodoky G, Moiseyenko V, Lichinitser M, Gorbunova V, et al. Multicenter phase III comparison of cisplatin/S-1 with cisplatin/infusional fluorouracil in advanced gastric or gastroesophageal adenocarcinoma study: the FLAGS trial. J Clin Oncol 2010;28:1547-1553. https://doi.org/10.1200/JCO.2009.25.4706
  21. Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, et al. Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med 2007;357:1810-1820. https://doi.org/10.1056/NEJMoa072252
  22. Abbas M, Habib M, Naveed M, Karthik K, Dhama K, Shi M, et al. The relevance of gastric cancer biomarkers in prognosis and pre- and post- chemotherapy in clinical practice. Biomed Pharmacother 2017;95:1082-1090. https://doi.org/10.1016/j.biopha.2017.09.032
  23. Deng JY, Liang H. Clinical significance of lymph node metastasis in gastric cancer. World J Gastroenterol 2014;20:3967-3975. https://doi.org/10.3748/wjg.v20.i14.3967
  24. Sarela AI, Turnbull AD, Coit DG, Klimstra D, Brennan MF, Karpeh MS. Accurate lymph node staging is of greater prognostic importance than subclassification of the T2 category for gastric adenocarcinoma. Ann Surg Oncol 2003;10:783-791. https://doi.org/10.1245/ASO.2003.09.009
  25. Ichikura T, Tomimatsu S, Okusa Y, Uefuji K, Tamakuma S. Comparison of the prognostic significance between the number of metastatic lymph nodes and nodal stage based on their location in patients with gastric cancer. J Clin Oncol 1993;11:1894-1900. https://doi.org/10.1200/JCO.1993.11.10.1894
  26. Ahn HS, Lee HJ, Yoo MW, Kim SG, Im JP, Kim SH, et al. Diagnostic accuracy of T and N stages with endoscopy, stomach protocol CT, and endoscopic ultrasonography in early gastric cancer. J Surg Oncol 2009;99:20-27. https://doi.org/10.1002/jso.21170
  27. Hwang SW, Lee DH. Is endoscopic ultrasonography still the modality of choice in preoperative staging of gastric cancer? World J Gastroenterol 2014;20:13775-13782. https://doi.org/10.3748/wjg.v20.i38.13775
  28. Kim SH, Kim JJ, Lee JS, Kim SH, Kim BS, Maeng YH, et al. Preoperative N staging of gastric cancer by stomach protocol computed tomography. J Gastric Cancer 2013;13:149-156. https://doi.org/10.5230/jgc.2013.13.3.149
  29. Kim SK, Kang KW, Lee JS, Kim HK, Chang HJ, Choi JY, et al. Assessment of lymph node metastases using $^{18}F$-FDG PET in patients with advanced gastric cancer. Eur J Nucl Med Mol Imaging 2006;33:148-155. https://doi.org/10.1007/s00259-005-1887-8
  30. Kim EY, Lee WJ, Choi D, Lee SJ, Choi JY, Kim BT, et al. The value of PET/CT for preoperative staging of advanced gastric cancer: comparison with contrast-enhanced CT. Eur J Radiol 2011;79:183-188. https://doi.org/10.1016/j.ejrad.2010.02.005
  31. Yun M, Lim JS, Noh SH, Hyung WJ, Cheong JH, Bong JK, et al. Lymph node staging of gastric cancer using $^{18}F$-FDG PET: a comparison study with CT. J Nucl Med 2005;46:1582-1588.
  32. Coupe NA, Karikios D, Chong S, Yap J, Ng W, Merrett N, 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;28:128-135. https://doi.org/10.1007/s12149-013-0791-8
  33. Lee JW, Lee SM, Lee MS, Shin HC. Role of $^{18}F$-FDG PET/CT in the prediction of gastric cancer recurrence after curative surgical resection. Eur J Nucl Med Mol Imaging 2012;39:1425-1434. https://doi.org/10.1007/s00259-012-2164-2
  34. Mochiki E, Kuwano H, Katoh H, Asao T, Oriuchi N, Endo K. Evaluation of $^{18}F$-2-deoxy-2-fluoro-D-glucose positron emission tomography for gastric cancer. World J Surg 2004;28:247-253. https://doi.org/10.1007/s00268-003-7191-5
  35. Stahl A, Ott K, Weber WA, Becker K, Link T, Siewert JR, et al. FDG PET imaging of locally advanced gastric carcinomas: correlation with endoscopic and histopathological findings. Eur J Nucl Med Mol Imaging 2003;30:288-295. https://doi.org/10.1007/s00259-002-1029-5
  36. Kim J, Lim ST, Na CJ, Han YH, Kim CY, Jeong HJ, 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. https://doi.org/10.1007/s13139-013-0243-3
  37. Soret M, Bacharach SL, Buvat I. Partial-volume effect in PET tumor imaging. J Nucl Med 2007;48:932-945. https://doi.org/10.2967/jnumed.106.035774

피인용 문헌

  1. Metabolic Characteristics and Diagnostic Contribution of 18 F-FDG PET/CT in Gastric Carcinomas vol.29, pp.1, 2018, https://doi.org/10.4274/mirt.galenos.2020.75537
  2. Opportunities in cancer imaging: a review of oesophageal, gastric and colorectal malignancies vol.76, pp.10, 2018, https://doi.org/10.1016/j.crad.2021.01.001
  3. 18F-fluorodeoxyglucose uptake in advanced gastric cancer correlates with histopathological subtypes and volume of tumor stroma vol.145, pp.None, 2018, https://doi.org/10.1016/j.ejrad.2021.110048