Annals of Nuclear Medicine

, Volume 30, Issue 4, pp 279–286 | Cite as

Prognostic value of 18F-fluorodeoxyglucose positron emission tomography in patients with gastric neuroendocrine carcinoma and mixed adenoneuroendocrine carcinoma

  • Sun Min Lim
  • Hyunki Kim
  • Beodeul Kang
  • Hyo Song Kim
  • Sun Young Rha
  • Sung Hoon Noh
  • Woo Jin Hyung
  • Jae-Ho Cheong
  • Hyoung-Il Kim
  • Hyun Cheol Chung
  • Mijin Yun
  • Arthur ChoEmail author
  • Minkyu JungEmail author
Original Article



Gastric neuroendocrine carcinomas (NEC) and mixed adenoneuroendocrine carcinoma (MANEC) are very rare, aggressive tumors of the stomach. We aimed to examine predictive role of pretreatment 18F-FDG PET/CT-assessed metabolic parameter of primary tumors and metastases in patients with gastric NEC and MANEC.


We conducted a review of the 27 patients with histopathologically confirmed NECs (n = 10) and MANEC (n = 17) of the stomach at our institution between January 2005 and December 2012. All patients underwent 18F-FDG-PET examination at diagnosis. Metabolic parameters [SUVmax, SUVmean, metabolic tumor volume (MTV) and total lesion glycolysis (TLG)] of the primary tumor and metastases on baseline PET/CT were analyzed.


The median follow-up duration was 39.4 months (95 % CI 20.0–58.1 months) and the median overall survival (OS) was 25.7 months (95 % CI 14.1–37.2 months). All gastric lesions were well visualized (average SUVmax = 12.0, range 3.0–41.8). When subjects were divided into two groups by ROC cut-off value of 210.9 and 612, patients with high TLG in primary lesion and metastases showed poorer prognosis compared to low TLG patients (P = 0.09, P = 0.002, respectively). In the sub-analysis of patients with metastasis (n = 12), patients with high TLG in whole body tumor showed significantly shorter OS compared to those with low TLG (31.7 ± 11.4 vs. 7.2 ± 2.1 months, P = 0.006).


18F-FDG PET/CT is useful in evaluating prognosis of advanced gastric cancer with neuroendocrine carcinoma components. Baseline MTV of primary gastric cancer with metastatic disease, and MTV, TLG of metastases may be prognostic markers in patients with gastric NEC and MANEC.


18F-FDG PET/CT Survival Gastric Neuroendocrine carcinoma Mixed adenoneuroendocine carcinoma 



This study was supported by a new faculty research seed money Grant of Yonsei University College of Medicine for 2014 (2014-32-0028).

Compliance with ethical standards

Conflict of interest

All authors declare no conflict of interest.


  1. 1.
    Rindi G, Bordi C, Rappel S, La Rosa S, Stolte M, Solcia E. Gastric carcinoids and neuroendocrine carcinomas: pathogenesis, pathology, and behavior. World J Surg. 1996;20(2):168–72.CrossRefPubMedGoogle Scholar
  2. 2.
    Chiba N, Suwa T, Hori M, Sakuma M, Kitajima M. Advanced gastric endocrine cell carcinoma with distant lymph node metastasis: a case report and clinicopathological characteristics of the disease. Gastric Cancer. 2004;7(2):122–7.CrossRefPubMedGoogle Scholar
  3. 3.
    Basuroy R, Srirajaskanthan R, Prachalias A, Quaglia A, Ramage JK. Review article: the investigation and management of gastric neuroendocrine tumours. Aliment Pharmacol Ther. 2014;39(10):1071–84.CrossRefPubMedGoogle Scholar
  4. 4.
    Kubota K, Okada A, Kuroda J, Yoshida M, Ohta K, Adachi M, et al. Neuroendocrine carcinoma of the stomach: a case study. Case Rep Med. 2011;2011:948328.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Lee HH, Jung CK, Jung ES, Song KY, Jeon HM, Park CH. Mixed exocrine and endocrine carcinoma in the stomach: a case report. J Gastric Cancer. 2011;11(2):122–5.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Weber WA. Positron emission tomography as an imaging biomarker. J Clin Oncol. 2006;24(20):3282–92.CrossRefPubMedGoogle Scholar
  7. 7.
    Moon SH, Hyun SH, Choi JY. Prognostic significance of volume-based PET parameters in cancer patients. Korean J Radiol. 2013;14(1):1–12.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Obara P, Pu Y. Prognostic value of metabolic tumor burden in lung cancer. Chin J Cancer Res. 2013;25(6):615–22.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Choi HJ, Lee JW, Kang B, Song SY, Lee JD, Lee JH. Prognostic significance of volume-based FDG PET/CT parameters in patients with locally advanced pancreatic cancer treated with chemoradiation therapy. Yonsei Med J. 2014;55(6):1498–506.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Masson-Deshayes S, Schvartz C, Dalban C, Guendouzen S, Pochart JM, Dalac A, et al. Prognostic value of 18F-FDG PET/CT metabolic parameters in metastatic differentiated thyroid cancers. Clin Nucl Med. 2015;40(6):469–75.CrossRefPubMedGoogle Scholar
  11. 11.
    Binderup T, Knigge U, Loft A, Federspiel B, Kjaer A. 18F-fluorodeoxyglucose positron emission tomography predicts survival of patients with neuroendocrine tumors. Clin Cancer Res. 2010;16(3):978–85.CrossRefPubMedGoogle Scholar
  12. 12.
    Makis W, Ciarallo A, Hickeson M, Derbekyan V, Novales-Diaz JA, Lisbona R. Gastric neuroendocrine carcinoma staged and followed with (18)F-FDG PET/CT–a report of 3 cases. Clin Nucl Med. 2013;38(6):447–50.CrossRefPubMedGoogle Scholar
  13. 13.
    Bosman FT, Carneiro F, Hruban RH, Theise ND. WHO classification of tumours of the digestive system. 4th ed. Lyon: International Agency for Research on Cancer; 2010. p 13.Google Scholar
  14. 14.
    Yun M. Imaging of gastric cancer metabolism using 18F-FDG PET/CT. J Gastric Cancer. 2014;14(1):1–6.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    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(3):192–6.CrossRefPubMedGoogle Scholar
  16. 16.
    Yun M, Choi HS, Yoo E, Bong JK, Ryu YH, Lee JD. The role of gastric distention in differentiating recurrent tumor from physiologic uptake in the remnant stomach on 18F-FDG PET. J Nucl Med. 2005;46(6):953–7.PubMedGoogle Scholar
  17. 17.
    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(2):288–95.CrossRefPubMedGoogle Scholar
  18. 18.
    Ezziddin S, Adler L, Sabet A, Poppel TD, Grabellus F, Yuce A, et al. Prognostic stratification of metastatic gastroenteropancreatic neuroendocrine neoplasms by 18F-FDG PET: feasibility of a metabolic grading system. J Nucl Med. 2014;55(8):1260–6.CrossRefPubMedGoogle Scholar
  19. 19.
    Im HJ, Pak K, Cheon GJ, Kang KW, Kim SJ, Kim IJ, et al. Prognostic value of volumetric parameters of (18)F-FDG PET in non-small-cell lung cancer: a meta-analysis. Eur J Nucl Med Mol Imaging. 2015;42(2):241–51.CrossRefPubMedGoogle Scholar
  20. 20.
    Ogawa S, Itabashi M, Kondo C, Momose M, Sakai S, Kameoka S. Prognostic value of total lesion glycolysis measured by 18F-FDG-PET/CT in patients with colorectal cancer. Anticancer Res. 2015;35(6):3495–500.PubMedGoogle Scholar
  21. 21.
    Friboulet L, Li N, Katayama R, Lee CC, Gainor JF, Crystal AS, et al. The ALK inhibitor ceritinib overcomes crizotinib resistance in non-small cell lung cancer. Cancer Discov. 2014;4(6):662–73.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Yamaguchi E, Sato Y, Oe T, Nishi T, Koike M, Kitakado Y, et al. Gastric mixed adenoneuroendocrine carcinoma with thyroid transcription factor-1-positive neuroendocrine component. Clin J Gastroenterol. 2015;8(2):82–7.CrossRefPubMedGoogle Scholar
  23. 23.
    Hosokawa A, Shimada Y, Shirao K, Matsumura Y, Yamada Y, Muro K, et al. Long-term survivor of gastric small cell carcinoma. Hepatogastroenterology. 2004;51(59):1567–70.PubMedGoogle Scholar
  24. 24.
    Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer (Oxford, England: 1990). 2009;45(2):228–47.CrossRefGoogle Scholar
  25. 25.
    La Rosa S, Sessa F, Capella C. Mixed adenoneuroendocrine carcinomas (MANECs) of the gastrointestinal tract: an update. Cancers. 2012;4:11–30.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Japanese Society of Nuclear Medicine 2016

Authors and Affiliations

  • Sun Min Lim
    • 1
    • 2
  • Hyunki Kim
    • 3
  • Beodeul Kang
    • 4
  • Hyo Song Kim
    • 1
  • Sun Young Rha
    • 1
  • Sung Hoon Noh
    • 5
  • Woo Jin Hyung
    • 5
  • Jae-Ho Cheong
    • 5
  • Hyoung-Il Kim
    • 5
  • Hyun Cheol Chung
    • 1
  • Mijin Yun
    • 6
  • Arthur Cho
    • 6
    Email author
  • Minkyu Jung
    • 1
    Email author
  1. 1.Division of Medical Oncology, Department of Internal MedicineYonsei University College of MedicineSeoulRepublic of Korea
  2. 2.Division of Medical Oncology, Department of Internal Medicine, CHA Bundang Medical CenterCHA UniversitySeongnamRepublic of Korea
  3. 3.Department of PathologyYonsei University College of MedicineSeoulRepublic of Korea
  4. 4.Division of Hematology and Medical Oncology, Department of Internal MedicineSeoul National University Bundang HospitalSeongnamRepublic of Korea
  5. 5.Department of SurgeryYonsei University College of MedicineSeoulRepublic of Korea
  6. 6.Department of Nuclear MedicineYonsei University College of MedicineSeoulRepublic of Korea

Personalised recommendations