Maximum standardized uptake value in 18F‑fluoro‑2‑deoxyglucose positron emission tomography is associated with advanced tumor factors in esophageal cancer

Kajiwara,Takeshi; Hiasa,Yoichi; Nishina,Tomohiro; Matsumoto,Toshihiko; Hori,Shinichiro; Nadano,Seijin; Iguchi,Haruo; Takeji,Satoru; Tsubouchi,Eiji; Ikeda,Yoshio; Onji,Morikazu

doi:10.3892/mco.2014.238

Maximum standardized uptake value in 18F‑fluoro‑2‑deoxyglucose positron emission tomography is associated with advanced tumor factors in esophageal cancer

Authors:
- Takeshi Kajiwara
- Yoichi Hiasa
- Tomohiro Nishina
- Toshihiko Matsumoto
- Shinichiro Hori
- Seijin Nadano
- Haruo Iguchi
- Satoru Takeji
- Eiji Tsubouchi
- Yoshio Ikeda
- Morikazu Onji
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Affiliations: Department of Gastroenterology, National Hospital Organization Shikoku Cancer Center, Matsuyama, Ehime 791‑0280, Japan, Department of Gastroenterology and Metabology, Ehime University Graduate School of Medicine, Toon, Ehime 791‑0295, Japan
Published online on: January 7, 2014 https://doi.org/10.3892/mco.2014.238
Pages: 313-321

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Abstract

Positron emission tomography/computed tomography (PET/CT) with 18F‑fluoro‑2‑deoxyglucose (FDG‑PET/CT) has become established in cancer imaging, and derived maximum standardized uptake values (SUVmax) add functional information regarding cancer, including esophageal squamous cell carcinoma (ESCC). The aim of the present study was to determine the clinical significance and association of tumor progression using SUVmax derived from PET/CT images in patients with ESCC. In total, 101 patients with ESCC were assessed using FDG‑PET/CT and the SUVmax was then compared with the clinical backgrounds and prognoses of the patients. Endoscopic ESCC biopsy specimens were obtained in order to analyze mRNA expression relative to tumor progression. The results showed that values for SUVmax were significantly higher in patients with tumor progression factors, particularly those with lymph node metastasis. Analysis of receiver operating characteristics curves revealed an optimum SUVmax cut‑off value of 10.26 for node‑positive disease. Patients with SUVmax ≥10.26 had gene alterations with epithelial‑mesenchymal transition (EMT) and significantly worse overall survival (P=0.0012). A higher SUVmax in patients with ESCC was associated with lymph node metastasis and a poorer prognosis. Thus, the SUVmax may reflect the potential of EMT in patients with ESCC.

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1	Parkin DM, Bray FI and Devesa SS: Cancer burden in the year 2000. The global picture. Eur J Cancer. 37(Suppl 8): S4–S66. 2001.PubMed/NCBI
2	Enzinger PC and Mayer RJ: Esophageal cancer. N Engl J Med. 349:2241–2252. 2003. View Article : Google Scholar : PubMed/NCBI
3	Barber TW, Duong CP, Leong T, Bressel M, Drummond EG and Hicks RJ: 18F-FDG PET/CT has a high impact on patient management and provides powerful prognostic stratification in the primary staging of esophageal cancer: a prospective study with mature survival data. J Nucl Med. 53:864–871. 2012. View Article : Google Scholar
4	Bar-Shalom R, Guralnik L, Tsalic M, Leiderman M, Frenkel A, Gaitini D, Ben-Nun A, Keidar Z and Israel O: The additional value of PET/CT over PET in FDG imaging of oesophageal cancer. Eur J Nucl Med Mol Imaging. 32:918–924. 2005. View Article : Google Scholar : PubMed/NCBI
5	Berrisford RG, Wong WL, Day D, Toy E, Napier M, Mitchell K and Wajed S: The decision to operate: role of integrated computed tomography positron emission tomography in staging oesophageal and oesophagogastric junction cancer by the multidisciplinary team. Eur J Cardiothorac Surg. 33:1112–1116. 2008. View Article : Google Scholar
6	Kato H, Kimura H, Nakajima M, Sakai M, Sano A, Tanaka N, Inose T, Faried A, Saito K, Ieta K, Sohda M, Fukai Y, Miyazaki T, Masuda N, Fukuchi M, Ojima H, Tsukada K, Oriuchi N, Endo K and Kuwano H: The additional value of integrated PET/CT over PET in initial lymph node staging of esophageal cancer. Oncol Rep. 20:857–862. 2008.PubMed/NCBI
7	Noble F and Bailey D; SWCIS Upper Gastrointestinal Tumour Panel. Tung K and Byrne JP: Impact of integrated PET/CT in the staging of oesophageal cancer: a UK population-based cohort study. Clin Radiol. 64:699–705. 2009. View Article : Google Scholar : PubMed/NCBI
8	Omloo JM, van Heijl M, Hoekstra OS, van Berge Henegouwen MI, van Lanschot JJ and Sloof GW: FDG-PET parameters as prognostic factor in esophageal cancer patients: a review. Ann Surg Oncol. 18:3338–3352. 2011. View Article : Google Scholar : PubMed/NCBI
9	Salahudeen HM, Balan A, Naik K, Mirsadraee S and Scarsbrook AF: Impact of the introduction of integrated PET-CT into the preoperative staging pathway of patients with potentially operable oesophageal carcinoma. Clin Radiol. 63:765–773. 2008. View Article : Google Scholar : PubMed/NCBI
10	Yuan S, Yu Y, Chao KS, Fu Z, Yin Y, Liu T, Chen S, Yang X, Yang G, Guo H and Yu J: Additional value of PET/CT over PET in assessment of locoregional lymph nodes in thoracic esophageal squamous cell cancer. J Nucl Med. 47:1255–1259. 2006.PubMed/NCBI
11	Cerfolio RJ, Bryant AS, Ohja B and Bartolucci AA: The maximum standardized uptake values on positron emission tomography of a non-small cell lung cancer predict stage, recurrence, and survival. J Thorac Cardiovasc Surg. 130:151–159. 2005. View Article : Google Scholar : PubMed/NCBI
12	Sasaki R, Komaki R, Macapinlac H, Erasmus J, Allen P, Forster K, Putnam JB, Herbst RS, Moran CA, Podoloff DA, Roth JA and Cox JD: [18F]fluorodeoxyglucose uptake by positron emission tomography predicts outcome of non-small-cell lung cancer. J Clin Oncol. 23:1136–1143. 2005.
13	Cerfolio RJ and Bryant AS: Maximum standardized uptake values on positron emission tomography of esophageal cancer predicts stage, tumor biology, and survival. Ann Thorac Surg. 82:391–395. 2006. View Article : Google Scholar
14	Cheze-Le Rest C, Metges JP, Teyton P, Jestin-Le Tallec V, Lozac’h P, Volant A and Visvikis D: Prognostic value of initial fluorodeoxyglucose-PET in esophageal cancer: a prospective study. Nucl Med Commun. 29:628–635. 2008.PubMed/NCBI
15	Sobin LH and Wittekind C: TMN classification of malignant tumors. 6th edition. John Wiley & Sons; New York: 2002
16	Schisterman EF, Perkins NJ, Liu A and Bondell H: Optimal cut-point and its corresponding Youden Index to discriminate individuals using pooled blood samples. Epidemiology. 16:73–81. 2005. View Article : Google Scholar : PubMed/NCBI
17	Fujita H: Present status of esophageal cancer and its treatment in Japan. Ann Thorac Cardiovasc Surg. 10:135–139. 2004.PubMed/NCBI
18	Hatt M, Visvikis D, Albarghach NM, Tixier F, Pradier O and Cheze-le Rest C: Prognostic value of 18F-FDG PET image-based parameters in oesophageal cancer and impact of tumour delineation methodology. Eur J Nucl Med Mol Imaging. 38:1191–1202. 2011. View Article : Google Scholar : PubMed/NCBI
19	van Westreenen HL, Plukker JT, Cobben DC, Verhoogt CJ, Groen H and Jager PL: Prognostic value of the standardized uptake value in esophageal cancer. AJR Am J Roentgenol. 185:436–440. 2005.PubMed/NCBI
20	Yasuda T, Higuchi I, Yano M, Miyata H, Yamasaki M, Takiguchi S, Fujiwara Y, Hatazawa J and Doki Y: The impact of ¹⁸F-fluorodeoxyglucose positron emission tomography positive lymph nodes on postoperative recurrence and survival in resectable thoracic esophageal squamous cell carcinoma. Ann Surg Oncol. 19:652–660. 2012.
21	Thiery JP: Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2:442–454. 2002. View Article : Google Scholar : PubMed/NCBI
22	Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 7:131–142. 2006. View Article : Google Scholar : PubMed/NCBI
23	Huber MA, Kraut N and Beug H: Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol. 17:548–558. 2005. View Article : Google Scholar : PubMed/NCBI
24	Natsugoe S, Uchikado Y, Okumura H, Matsumoto M, Setoyama T, Tamotsu K, Kita Y, Sakamoto A, Owaki T, Ishigami S and Aikou T: Snail plays a key role in E-cadherin-preserved esophageal squamous cell carcinoma. Oncol Rep. 17:517–523. 2007.PubMed/NCBI
25	Sasaki K, Natsugoe S, Ishigami S, Matsumoto M, Okumura H, Setoyama T, Uchikado Y, Kita Y, Tamotsu K, Sakamoto A, Owaki T and Aikou T: Significance of Twist expression and its association with E-cadherin in esophageal squamous cell carcinoma. J Exp Clin Cancer Res. 28:1582009. View Article : Google Scholar : PubMed/NCBI
26	Usami Y, Satake S, Nakayama F, Matsumoto M, Ohnuma K, Komori T, Semba S, Ito A and Yokozaki H: Snail-associated epithelial-mesenchymal transition promotes oesophageal squamous cell carcinoma motility and progression. J Pathol. 215:330–339. 2008. View Article : Google Scholar
27	Li Y, Ma J, Guo Q, Duan F, Tang F, Zheng P, Zhao Z and Lu G: Overexpression of MMP-2 and MMP-9 in esophageal squamous cell carcinoma. Dis Esophagus. 22:664–667. 2009. View Article : Google Scholar : PubMed/NCBI
28	Mori M, Mimori K, Sadanaga N, Inoue H, Tanaka Y, Mafune K, Ueo H and Barnard GF: Prognostic impact of tissue inhibitor of matrix metalloproteinase-1 in esophageal carcinoma. Int J Cancer. 88:575–578. 2000. View Article : Google Scholar : PubMed/NCBI
29	Li K, He W, Lin N, Wang X and Fan QX: Downregulation of N-cadherin expression inhibits invasiveness, arrests cell cycle and induces cell apoptosis in esophageal squamous cell carcinoma. Cancer Invest. 28:479–486. 2010. View Article : Google Scholar : PubMed/NCBI
30	Fernando RI, Castillo MD, Litzinger M, Hamilton DH and Palena C: IL-8 signaling plays a critical role in the epithelial-mesenchymal transition of human carcinoma cells. Cancer Res. 71:5296–5306. 2011. View Article : Google Scholar : PubMed/NCBI
31	Kato H, Takita J, Miyazaki T, Nakajima M, Fukai Y, Masuda N, Fukuchi M, Manda R, Ojima H, Tsukada K, Kuwano H, Oriuchi N and Endo K: Correlation of 18-F-fluorodeoxyglucose (FDG) accumulation with glucose transporter (Glut-1) expression in esophageal squamous cell carcinoma. Anticancer Res. 23:3263–3272. 2003.PubMed/NCBI
32	Lee SY, Jeon HM, Ju MK, Kim CH, Yoon G, Han SI, Park HG and Kang HS: Wnt/Snail signaling regulates cytochrome C oxidase and glucose metabolism. Cancer Res. 72:3607–3617. 2012. View Article : Google Scholar : PubMed/NCBI
33	Langer R, Specht K, Becker K, Ewald P, Bekesch M, Sarbia M, Busch R, Feith M, Stein HJ, Siewert JR and Hofler H: Association of pretherapeutic expression of chemotherapy-related genes with response to neoadjuvant chemotherapy in Barrett carcinoma. Clin Cancer Res. 11:7462–7469. 2005. View Article : Google Scholar : PubMed/NCBI