Digestive Diseases and Sciences

, Volume 51, Issue 12, pp 2198–2205 | Cite as

Correlation of GLUT-1 Overexpression, Tumor Size, and Depth of Invasion with 18F-2-fluoro-2-deoxy-d-glucose Uptake by Positron Emission Tomography in Colorectal Cancer

  • Jinyu Gu
  • Hirofumi Yamamoto
  • Hiroki Fukunaga
  • Katsuki Danno
  • Ichiro Takemasa
  • Masataka Ikeda
  • Mitsuaki Tatsumi
  • Mitsugu Sekimoto
  • Jun Hatazawa
  • Tsunehiko Nishimura
  • Morito Monden
Original Paper

Abstract

We investigated the wide variability of 18F-2-fluoro-2-deoxy-d-glucose (FDG) uptake, semiquantified as standardized uptake value (SUV), in positron emission tomography (PET) scanning, in 20 patients with colorectal cancer (CRC), including 1 with synchronous hepatic metastasis. The sensitivity of PET in CRC diagnosis was 100%, with a mean SUV of 8.0 (3.1–11.9). Tumor size and depth of invasion were associated with higher SUVs (P=.0004, .042, respectively). Strong glucose transporter-1 (GLUT-1) expression had significantly positive correlation with the SUV (r=.619, P=.003). GLUT-1 expression revealed positive staining in 17 (85%) of the 20 primary lesions. The central part of the tumor, thought to be relatively hypoxic, had stronger GLUT-1 expression and a higher SUV than the periphery, in both the primary tumor and hepatic metastatic foci. Our data suggest that the SUVs of FDG uptake in PET may be a noninvasive biomarker for advanced CRC, indicative of a large hypoxic tumor with deep invasion.

Keywords

Standardized uptake value 18F-2-fluoro-2-deoxy-d-glucose Positron emission tomography Colorectal cancer Glucose transporter-1 

References

  1. 1.
    Truant S, Huglo D, Hebbar M, Ernst O, Steinling M, Pruvot FR (2005) Prospective evaluation of the impact of [18F]fluoro-2-deoxy-d-glucose positron emission tomography of resectable colorectal liver metastases. Br J Surg 92:362–369CrossRefPubMedGoogle Scholar
  2. 2.
    Delbeke D, Martin WH (2004) PET and PET-CT for evaluation of colorectal carcinoma. Semin Nucl Med 34:209–223CrossRefPubMedGoogle Scholar
  3. 3.
    Dimitrakopoulou-Strauss A, Strauss LG, Burger C, Ruhl A, Irngartinger G, Stremmel W, Rudi J (2004) Prognostic aspects of 18F-FDG PET kinetics in patients with metastatic colorectal carcinoma receiving FOLFOX chemotherapy. J Nucl Med 45: 1480–1487PubMedGoogle Scholar
  4. 4.
    Wong CY, Salem R, Qing F, Wong KT, Barker D, Gates V, Lewandowski R, Hill EA, Dworkin HJ, Nagle C (2004) Metabolic response after intraarterial 90Y-glass microsphere treatment for colorectal liver metastases: comparison of quantitative and visual analyses by 18F-FDG PET. J Nucl Med 45:1892–1897PubMedGoogle Scholar
  5. 5.
    Rohren EM, Paulson EK, Hagge RH, Wong TZ, Killius J, Clavien PA, Nelson RC (2002) The role of F-18-FDG PET in preoperative assessment of the liver in patients being considered for curative resection of hepatic metastases from colorectal cancer. Clin Nucl Med 27:550–555CrossRefPubMedGoogle Scholar
  6. 6.
    Rohren EM, Turkington TG, Coleman RE (2004) Clinical applications of PET in oncology. Radiology 231:305–332PubMedGoogle Scholar
  7. 7.
    Kurokawa T, Yoshida Y, Kawahara K, Tsuchida T, Okazawa H, Fujibayashi Y, Yonekura Y, Kotsuji F (2004) Expression of GLUT-1 glucose transfer, cellular proliferation activity and grade of tumor correlate with [F-18]-fluorodeoxyglucose uptake by positron emission tomography in epithelial tumors of the ovary. Int J Cancer 109:926–932CrossRefPubMedGoogle Scholar
  8. 8.
    Chung JK, Lee YJ, Kim SK, Jeong JM, Lee DS, Lee MC (2004) Comparison of [18F]fluorodeoxyglucose uptake with glucose transporter-1 expression and proliferation rate in human glioma and non-small-cell lung cancer. Nucl Med Commun 25:11–17CrossRefPubMedGoogle Scholar
  9. 9.
    Bos R, Van Der Hoeven JJ, Van Der Wall E, Van Der Groep P, van Diest PJ, Comans EF, Joshi U, Semenza GL, Hoekstra OS, Lammertsma AA, Molthoff CF (2002) Biologic correlates of (18)fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography. J Clin Oncol 20:379–387CrossRefPubMedGoogle Scholar
  10. 10.
    Rajendran JG, Mankoff DA, O'Sullivan F, Peterson LM, Schwartz DL, Conrad EU, Spence AM, Muzi M, Farwell DG, Krohn KA (2004) Hypoxia and glucose metabolism in malignant tumors: evaluation by [18F] fluoromisonidazole and [18F] fluorodeoxyglucose positron emission tomography imaging. Clin Cancer Res 10:2245–2252CrossRefPubMedGoogle Scholar
  11. 11.
    Pugachev A, Ruan S, Carlin S, Larson SM, Campa J, Ling CC, Humm JL (2005) Dependence of FDG uptake on tumor microenvironment. Int J Radiat Oncol Biol Phys 62:545–553CrossRefPubMedGoogle Scholar
  12. 12.
    Yen TC, See LC, Lai CH, Yah-Huei CW, Ng KK, Ma SY, Lin WJ, Chen JT, Chen WJ, Lai CR, Hsueh S (2004) 18F-FDG uptake in squamous cell carcinoma of the cervix is correlated with glucose transporter 1 expression. J Nucl Med 45:22–29PubMedGoogle Scholar
  13. 13.
    Kato H, Takita J, Miyazaki T, Nakajima M, Fukai Y, Masuda N, Fukuchi M, Manda R, Ojima H, Tsukada K, Kuwano H, Oriuchi N, Endo K (2003) Correlation of 18-F-fluorodeoxyglucose (FDG) accumulation with glucose transporter (Glut-1) expression in esophageal squamous cell carcinoma. Anticancer Res 23:3263–3272PubMedGoogle Scholar
  14. 14.
    Koga H, Matsuo Y, Sasaki M, Nakagawa M, Kaneko K, Hayashi K, Kuwabara Y, Honda H (2003) Differential FDG accumulation associated with GLUT-1 expression in a patient with lymphoma. Ann Nucl Med 17:327–331PubMedCrossRefGoogle Scholar
  15. 15.
    Paul AK, Tatsumi M, Higuchi I, Fukunaga H, Yasuda T, Nishimura T (2003) Gamma camera coincidence imaging with [18F]fluorodeoxyglucose in the pretreatment evaluation of patients with oesophageal cancer. Nucl Med Commun 24:963–970CrossRefPubMedGoogle Scholar
  16. 16.
    Fukunaga H, Sekimoto M, Ikeda M, Higuchi I, Yasui M, Seshimo I, Takayama O, Yamamoto H, Ohue M, Tatsumi M, Hatazawa J, Ikenaga M, Nishimura T, Monden M (2005) Fusion image of positron emission tomography and computed tomography for the diagnosis of local recurrence of rectal cancer. Ann Surg Oncol 12:561–569CrossRefPubMedGoogle Scholar
  17. 17.
    Hayashi N, Yamamoto H, Hiraoka N, Dono K, Ito Y, Okami J, Kondo M, Nagano H, Umeshita K, Sakon M, Matsuura N, Nakamori S, Monden M (2001) Differential expression of cyclooxygenase-2 (COX-2) in human bile duct epithelial cells and bile duct neoplasm. Hepatology 34:638–650CrossRefPubMedGoogle Scholar
  18. 18.
    Abdel-Nabi H, Doerr RJ, Lamonica DM, Cronin VR, Galantowicz PJ, Carbone GM, Spaulding MB (1998) Staging of primary colorectal carcinomas with fluorine-18 fluorodeoxyglucose whole-body PET: correlation with histopathologic and CT findings. Radiology 206:755–760PubMedGoogle Scholar
  19. 19.
    Topal B, Flamen P, Aerts R, D'Hoore A, Filez L, Van Cutsem E, Mortelmans L, Penninckx F (2001) Clinical value of whole-body emission tomography in potentially curable colorectal liver metastases. Eur J Surg Oncol 27:175–179CrossRefPubMedGoogle Scholar
  20. 20.
    Mochiki E, Kuwano H, Katoh H, Asao T, Oriuchi N, Endo K (2004) Evaluation of 18F-2-deoxy-2-fluoro-d-glucose positron emission tomography for gastric cancer. World J Surg 28:247–253CrossRefPubMedGoogle Scholar
  21. 21.
    Chen J, Cheong JH, Yun MJ, Kim J, Lim JS, Hyung WJ, Noh SH (2005) Improvement in preoperative staging of gastric adenocarcinoma with positron emission tomography. Cancer 103:2383–2390CrossRefPubMedGoogle Scholar
  22. 22.
    Tian M, Zhang H, Nakasone Y, Mogi K, Endo K (2004) Expression of Glut-1 and Glut-3 in untreated oral squamous cell carcinoma compared with FDG accumulation in a PET study. Eur J Nucl Med Mol Imaging 31:5–12CrossRefPubMedGoogle Scholar
  23. 23.
    Berger KL, Nicholson SA, Dehdashti F, Siegel BA (2000) FDG PET evaluation of mucinous neoplasms: correlation of FDG uptake with histopathologic features. AJR Am J Roentgenol 174:1005–1008PubMedGoogle Scholar
  24. 24.
    Whiteford MH, Whiteford HM, Yee LF, Ogunbiyi OA, Dehdashti F, Siegel BA, Birnbaum EH, Fleshman JW, Kodner IJ, Read TE (2000) Usefulness of FDG-PET scan in the assessment of suspected metastatic or recurrent adenocarcinoma of the colon and rectum. Dis Colon Rectum 43:759–767CrossRefPubMedGoogle Scholar
  25. 25.
    Kubota K, Akasu T, Fujita S, Sugihara K, Moriya Y, Yamamoto S (2004) Clinical and pathological prognostic indicators with colorectal mucinous carcinomas. Hepatogastroenterology 51:142–146PubMedGoogle Scholar
  26. 26.
    Kato H, Kuwano H, Nakajima M, Miyazaki T, Yoshikawa M, Ojima H, Tsukada K, Oriuchi N, Inoue T, Endo K (2002) Comparison between positron emission tomography and computed tomography in the use of the assessment of esophageal carcinoma. Cancer 94:921–928CrossRefPubMedGoogle Scholar
  27. 27.
    Furudoi A, Tanaka S, Haruma K, Yoshihara M, Sumii K, Kajiyama G, Shimamoto F (2001) Clinical significance of human erythrocyte glucose transporter 1 expression at the deepest invasive site of advanced colorectal carcinoma. Oncology 60:162–169CrossRefPubMedGoogle Scholar
  28. 28.
    Burt BM, Humm JL, Kooby DA, Squire OD, Mastorides S, Larson SM, Fong Y (2001) Using positron emission tomography with [(18)F]FDG to predict tumor behavior in experimental colorectal cancer. Neoplasia 3:189–195CrossRefPubMedGoogle Scholar
  29. 29.
    Aloj L, Caraco C, Jagoda E, Eckelman WC, Neumann RD (1999) Glut-1 and hexokinase expression: relationship with 2-fluoro-2-deoxy-D-glucose uptake in A431 and T47D cells in culture. Cancer Res 59:4709–4714PubMedGoogle Scholar
  30. 30.
    Burke B, Giannoudis A, Corke KP, Gill D, Wells M, Ziegler-Heitbrock L, Lewis CE (2003) Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol 163:1233–1243PubMedGoogle Scholar
  31. 31.
    Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, Ferreira G, Iyer N, LaRusch J, Pak B, Taghavi P, Semenza GL (2003) Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1.Cancer Res 63:1138–1143PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Jinyu Gu
    • 1
    • 2
  • Hirofumi Yamamoto
    • 1
  • Hiroki Fukunaga
    • 1
  • Katsuki Danno
    • 1
  • Ichiro Takemasa
    • 1
  • Masataka Ikeda
    • 1
  • Mitsuaki Tatsumi
    • 3
  • Mitsugu Sekimoto
    • 1
  • Jun Hatazawa
    • 3
  • Tsunehiko Nishimura
    • 4
  • Morito Monden
    • 1
  1. 1.Department of Surgery and Clinical OncologyGraduate School of Medicine, Osaka UniversitySuita-CityJapan
  2. 2.Department of General SurgeryThe Second Affiliated Hospital of Harbin Medical UniversityHarbinChina
  3. 3.Department of Nuclear Medicine and Tracer KineticsGraduate School of Medicine, Osaka UniversityOsakaJapan
  4. 4.Department of RadiologyGraduate School of Medicine, Kyoto Prefectural University of MedicineKyotoJapan

Personalised recommendations