Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 12/2017

Open Access 01-11-2017 | Original Article

Elevated tumor-to-liver uptake ratio (TLR) from 18F–FDG-PET/CT predicts poor prognosis in stage IIA colorectal cancer following curative resection

Authors: Jun Huang, Liang Huang, Jiaming Zhou, Yinghua Duan, Zhanwen Zhang, Xiaoyan Wang, Pinzhu Huang, Shuyun Tan, Ping Hu, Jianping Wang, Meijin Huang

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 12/2017

Login to get access

Abstract

Purpose

The prognostic value of the tumor-to-liver uptake ratio (TLR) from 18-fluoro-2-deoxyglucose positron emission tomography/computed tomography (18F–FDG-PET/CT) in the early stage of colorectal cancer (CRC) is unclear. Notably, some stage IIA CRC patients experience early recurrence even after curative resection and might benefit from neoadjuvant or adjuvant chemotherapy. This study aims to evaluate whether elevated TLR from 18F–FDG-PET/CT can predict poor prognosis in stage IIA CRC patients undergoing curative resection.

Methods

From April 2010 to December 2013, 504 consecutive CRC patients with different TNM stages (I-IV) underwent 18F–FDG-PET/CT scans at the 6th Affiliated Hospital of Sun Yat-Sen University. Among the patients, 118 with stage IIA CRC who accepted preoperative 18F–FDG-PET/CT scanning and were treated with curative surgery alone were reviewed retrospectively. The maximum standardized uptake value (SUVmax) in the primary tumor, TLR, and demographic, clinical, histopathological, and laboratory data were analyzed. Receiver operating characteristic (ROC) curve, univariate and multivariate analyses were performed to identify prognostic factors associated with patient disease-free survival (DFS) and overall survival (OS).

Results

ROC curve analysis demonstrated that TLR was superior to primary tumor SUVmax in predicting the risk of recurrence in stage IIA CRC. The optimal TLR cutoff was 6.2. Univariate analysis indicated that elevated TLR, tumor size, and lymphovascular/neural invasion correlated with DFS (P = 0.001, P = 0.002, and P = 0.001, respectively) and OS (P = 0.001, P = 0.003, and P < 0.001, respectively). The 1-, 3-, and 5-year DFS rates were 98.4%, 96.9%, and 96.9% for stage IIA CRC patients with lower TLR (≤6.2) versus 77.8%, 60.6%, and 60.6% for those with elevated TLR (>6.2), respectively. The 1-, 3-, and 5-year OS rates were 100.0%, 100.0%, and 98.3% for the patients with lower TLR versus 98.1%, 83.3%, and 74.3% for those with elevated TLR. Cox regression analysis showed that elevated TLR [>6.2; hazard ratio (HR): 3.109–57.463; P < 0.001] and tumor size (>4.4 cm; HR: 1.636–19.155; P = 0.006) were independent risk factors for DFS. Meanwhile, elevated TLR (>6.2; HR: 1.398–84.945; P = 0.023) and lymphovascular/neural invasion (positive; HR: 1.278–12.777; P = 0.017) were independent risk factors for OS.

Conclusion

Elevated TLR predicted worse DFS and OS for stage IIA CRC patients and might serve as a potential radiological index to identify candidates for neoadjuvant or adjuvant chemotherapy. Stage IIA CRC patients with elevated TLR should be monitored carefully for early detection of possible recurrence.
Literature
3.
go back to reference Wu X, Zhang J, He X, Wang C, Lian L, Liu H, et al. Postoperative adjuvant chemotherapy for stage II colorectal cancer: a systematic review of 12 randomized controlled trials. J Gastrointest Surg. 2012;16:646–55. doi:10.1007/s11605-011-1682-8.CrossRefPubMed Wu X, Zhang J, He X, Wang C, Lian L, Liu H, et al. Postoperative adjuvant chemotherapy for stage II colorectal cancer: a systematic review of 12 randomized controlled trials. J Gastrointest Surg. 2012;16:646–55. doi:10.​1007/​s11605-011-1682-8.CrossRefPubMed
6.
go back to reference Kocarnik JM, Shiovitz S, Phipps AI. Molecular phenotypes of colorectal cancer and potential clinical applications. Gastroenterol Rep. 2015;3:269–76. doi:10.1093/gastro/gov046. Kocarnik JM, Shiovitz S, Phipps AI. Molecular phenotypes of colorectal cancer and potential clinical applications. Gastroenterol Rep. 2015;3:269–76. doi:10.​1093/​gastro/​gov046.
8.
9.
go back to reference Song BI, Lee SW, Jeong SY, Chae YS, Lee WK, Ahn BC, et al. 18F-FDG uptake by metastatic axillary lymph nodes on pretreatment PET/CT as a prognostic factor for recurrence in patients with invasive ductal breast cancer. J Nucl Med. 2012;53:1337–44. doi:10.2967/jnumed.111.098640.CrossRefPubMed Song BI, Lee SW, Jeong SY, Chae YS, Lee WK, Ahn BC, et al. 18F-FDG uptake by metastatic axillary lymph nodes on pretreatment PET/CT as a prognostic factor for recurrence in patients with invasive ductal breast cancer. J Nucl Med. 2012;53:1337–44. doi:10.​2967/​jnumed.​111.​098640.CrossRefPubMed
14.
go back to reference Takeda A, Yokosuka N, Ohashi T, Kunieda E, Fujii H, Aoki Y, et al. The maximum standardized uptake value (SUVmax) on FDG-PET is a strong predictor of local recurrence for localized non-small-cell lung cancer after stereotactic body radiotherapy (SBRT). Radiother Oncol. 2011;101:291–7. doi:10.1016/j.radonc.2011.08.008.CrossRefPubMed Takeda A, Yokosuka N, Ohashi T, Kunieda E, Fujii H, Aoki Y, et al. The maximum standardized uptake value (SUVmax) on FDG-PET is a strong predictor of local recurrence for localized non-small-cell lung cancer after stereotactic body radiotherapy (SBRT). Radiother Oncol. 2011;101:291–7. doi:10.​1016/​j.​radonc.​2011.​08.​008.CrossRefPubMed
15.
go back to reference Lee YY, Choi CH, Kim CJ, Kang H, Kim TJ, Lee JW, et al. The prognostic significance of the SUVmax (maximum standardized uptake value for F-18 fluorodeoxyglucose) of the cervical tumor in PET imaging for early cervical cancer: preliminary results. Gynecol Oncol. 2009;115:65–8. doi:10.1016/j.ygyno.2009.06.022.CrossRefPubMed Lee YY, Choi CH, Kim CJ, Kang H, Kim TJ, Lee JW, et al. The prognostic significance of the SUVmax (maximum standardized uptake value for F-18 fluorodeoxyglucose) of the cervical tumor in PET imaging for early cervical cancer: preliminary results. Gynecol Oncol. 2009;115:65–8. doi:10.​1016/​j.​ygyno.​2009.​06.​022.CrossRefPubMed
16.
17.
go back to reference Fuertes S, Setoain X, Lopez-Guillermo A, Carrasco JL, Rodriguez S, Rovira J, et al. Interim FDG PET/CT as a prognostic factor in diffuse large B-cell lymphoma. Eur J Nucl Med Mol Imaging. 2013;40:496–504. doi:10.1007/s00259-012-2320-8.CrossRefPubMed Fuertes S, Setoain X, Lopez-Guillermo A, Carrasco JL, Rodriguez S, Rovira J, et al. Interim FDG PET/CT as a prognostic factor in diffuse large B-cell lymphoma. Eur J Nucl Med Mol Imaging. 2013;40:496–504. doi:10.​1007/​s00259-012-2320-8.CrossRefPubMed
18.
go back to reference Park J, Chang KJ, Seo YS, Byun BH, Choi JH, Moon H, et al. Tumor SUVmax normalized to liver uptake on (18)F-FDG PET/CT predicts the pathologic complete response after Neoadjuvant Chemoradiotherapy in locally advanced rectal cancer. Nucl Med Mol Imaging. 2014;48:295–302. doi:10.1007/s13139-014-0289-x.CrossRefPubMedPubMedCentral Park J, Chang KJ, Seo YS, Byun BH, Choi JH, Moon H, et al. Tumor SUVmax normalized to liver uptake on (18)F-FDG PET/CT predicts the pathologic complete response after Neoadjuvant Chemoradiotherapy in locally advanced rectal cancer. Nucl Med Mol Imaging. 2014;48:295–302. doi:10.​1007/​s13139-014-0289-x.CrossRefPubMedPubMedCentral
21.
go back to reference Nakajo M, Jinguji M, Nakabeppu Y, Nakajo M, Higashi R, Fukukura Y, et al. Texture analysis of 18F-FDG PET/CT to predict tumour response and prognosis of patients with esophageal cancer treated by chemoradiotherapy. Eur J Nucl Med Mol Imaging. 2017;44:206–14. doi:10.1007/s00259-016-3506-2.CrossRefPubMed Nakajo M, Jinguji M, Nakabeppu Y, Nakajo M, Higashi R, Fukukura Y, et al. Texture analysis of 18F-FDG PET/CT to predict tumour response and prognosis of patients with esophageal cancer treated by chemoradiotherapy. Eur J Nucl Med Mol Imaging. 2017;44:206–14. doi:10.​1007/​s00259-016-3506-2.CrossRefPubMed
22.
go back to reference Wang X, Peng G, Zhang X, Chen Z, Zhang B, Li Z. Correlation of (1)(8)F-FDG PET-CT maximum standard uptake value and T/N ratio with the prognosis of postoperative colorectal cancer. Zhonghua Wei Chang Wai Ke Za Zhi. 2015;18:232–7.PubMed Wang X, Peng G, Zhang X, Chen Z, Zhang B, Li Z. Correlation of (1)(8)F-FDG PET-CT maximum standard uptake value and T/N ratio with the prognosis of postoperative colorectal cancer. Zhonghua Wei Chang Wai Ke Za Zhi. 2015;18:232–7.PubMed
27.
go back to reference Suzuki Y, Okabayashi K, Hasegawa H, Tsuruta M, Shigeta K, Murakami K, et al. Metabolic tumor volume and Total lesion Glycolysis in PET/CT correlate with the pathological findings of colorectal cancer and allow its accurate staging. Clin Nucl Med. 2016;41:761–5. doi:10.1097/RLU.0000000000001332.CrossRefPubMed Suzuki Y, Okabayashi K, Hasegawa H, Tsuruta M, Shigeta K, Murakami K, et al. Metabolic tumor volume and Total lesion Glycolysis in PET/CT correlate with the pathological findings of colorectal cancer and allow its accurate staging. Clin Nucl Med. 2016;41:761–5. doi:10.​1097/​RLU.​0000000000001332​.CrossRefPubMed
29.
go back to reference Liberale G, Lecocq C, Garcia C, Muylle K, Covas A, Deleporte A, et al. Accuracy of FDG-PET/CT in colorectal peritoneal Carcinomatosis: potential tool for evaluation of chemotherapeutic response. Anticancer Res. 2017;37:929–34. doi:10.21873/anticanres.11401.CrossRefPubMed Liberale G, Lecocq C, Garcia C, Muylle K, Covas A, Deleporte A, et al. Accuracy of FDG-PET/CT in colorectal peritoneal Carcinomatosis: potential tool for evaluation of chemotherapeutic response. Anticancer Res. 2017;37:929–34. doi:10.​21873/​anticanres.​11401.CrossRefPubMed
31.
go back to reference Keyes JW Jr. SUV: standard uptake or silly useless value? J Nucl Med. 1995;36:1836–9.PubMed Keyes JW Jr. SUV: standard uptake or silly useless value? J Nucl Med. 1995;36:1836–9.PubMed
33.
go back to reference Boellaard R, Krak NC, Hoekstra OS, Lammertsma AA. Effects of noise, image resolution, and ROI definition on the accuracy of standard uptake values: a simulation study. J Nucl Med. 2004;45:1519–27.PubMed Boellaard R, Krak NC, Hoekstra OS, Lammertsma AA. Effects of noise, image resolution, and ROI definition on the accuracy of standard uptake values: a simulation study. J Nucl Med. 2004;45:1519–27.PubMed
35.
go back to reference Gu J, Yamamoto H, Fukunaga H, Danno K, Takemasa I, Ikeda M, et al. 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. Dig Dis Sci. 2006;51:2198–205. doi:10.1007/s10620-006-9428-2.CrossRefPubMed Gu J, Yamamoto H, Fukunaga H, Danno K, Takemasa I, Ikeda M, et al. 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. Dig Dis Sci. 2006;51:2198–205. doi:10.​1007/​s10620-006-9428-2.CrossRefPubMed
36.
go back to reference Riedl CC, Akhurst T, Larson S, Stanziale SF, Tuorto S, Bhargava A, et al. 18F-FDG PET scanning correlates with tissue markers of poor prognosis and predicts mortality for patients after liver resection for colorectal metastases. J Nucl Med. 2007;48:771–5. doi:10.2967/jnumed.106.037291.CrossRefPubMed Riedl CC, Akhurst T, Larson S, Stanziale SF, Tuorto S, Bhargava A, et al. 18F-FDG PET scanning correlates with tissue markers of poor prognosis and predicts mortality for patients after liver resection for colorectal metastases. J Nucl Med. 2007;48:771–5. doi:10.​2967/​jnumed.​106.​037291.CrossRefPubMed
39.
go back to reference Barresi V, Reggiani Bonetti L, Vitarelli E, Di Gregorio C, Ponz de Leon M, Barresi G. Immunohistochemical assessment of lymphovascular invasion in stage I colorectal carcinoma: prognostic relevance and correlation with nodal micrometastases. Am J Surg Pathol. 2012;36:66–72. doi:10.1097/PAS.0b013e31822d3008.CrossRefPubMed Barresi V, Reggiani Bonetti L, Vitarelli E, Di Gregorio C, Ponz de Leon M, Barresi G. Immunohistochemical assessment of lymphovascular invasion in stage I colorectal carcinoma: prognostic relevance and correlation with nodal micrometastases. Am J Surg Pathol. 2012;36:66–72. doi:10.​1097/​PAS.​0b013e31822d3008​.CrossRefPubMed
40.
go back to reference Benson AB 3rd, Schrag D, Somerfield MR, Cohen AM, Figueredo AT, Flynn PJ, et al. American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer. J Clin Oncol. 2004;22:3408–19. doi:10.1200/JCO.2004.05.063.CrossRefPubMed Benson AB 3rd, Schrag D, Somerfield MR, Cohen AM, Figueredo AT, Flynn PJ, et al. American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer. J Clin Oncol. 2004;22:3408–19. doi:10.​1200/​JCO.​2004.​05.​063.CrossRefPubMed
41.
go back to reference Kotaka M, Yoshino T, Oba K, Shinozaki K, Touyama T, Manaka D, et al. Initial safety report on the tolerability of modified FOLFOX6 as adjuvant therapy in patients with curatively resected stage II or III colon cancer (JFMC41-1001-C2: JOIN trial). Cancer Chemother Pharmacol. 2015;76:75–84. doi:10.1007/s00280-015-2757-0.CrossRefPubMedPubMedCentral Kotaka M, Yoshino T, Oba K, Shinozaki K, Touyama T, Manaka D, et al. Initial safety report on the tolerability of modified FOLFOX6 as adjuvant therapy in patients with curatively resected stage II or III colon cancer (JFMC41-1001-C2: JOIN trial). Cancer Chemother Pharmacol. 2015;76:75–84. doi:10.​1007/​s00280-015-2757-0.CrossRefPubMedPubMedCentral
42.
go back to reference Meyerhardt JA. Adjuvant therapy for stage II and III colon cancer. Clin Adv Hematol Oncol. 2010;8:772–4.PubMed Meyerhardt JA. Adjuvant therapy for stage II and III colon cancer. Clin Adv Hematol Oncol. 2010;8:772–4.PubMed
47.
go back to reference Vriens D, de Geus-Oei LF, van der Graaf WT, Oyen WJ. Tailoring therapy in colorectal cancer by PET-CT. Q J Nucl Med Mol Imaging. 2009;53:224–44.PubMed Vriens D, de Geus-Oei LF, van der Graaf WT, Oyen WJ. Tailoring therapy in colorectal cancer by PET-CT. Q J Nucl Med Mol Imaging. 2009;53:224–44.PubMed
48.
go back to reference Banzo J, Ubieto MA, Giraldo P, Razola P, Prats E, Tardin L, et al. Resistance to first line chemotherapy treatment in a patient diagnosed of nodular lymphocyte-predominant Hodgkin’s lymphoma identified by 18F-FDG PET/CT: diagnostic and therapeutic implications. Rev Esp Med Nucl Imagen Mol. 2012;31:89–92. doi:10.1016/j.remn.2011.03.018.PubMed Banzo J, Ubieto MA, Giraldo P, Razola P, Prats E, Tardin L, et al. Resistance to first line chemotherapy treatment in a patient diagnosed of nodular lymphocyte-predominant Hodgkin’s lymphoma identified by 18F-FDG PET/CT: diagnostic and therapeutic implications. Rev Esp Med Nucl Imagen Mol. 2012;31:89–92. doi:10.​1016/​j.​remn.​2011.​03.​018.PubMed
50.
go back to reference Ryu IS, Kim JS, Roh JL, Cho KJ, Choi SH, Nam SY, et al. Prognostic significance of preoperative metabolic tumour volume and total lesion glycolysis measured by (18)F-FDG PET/CT in squamous cell carcinoma of the oral cavity. Eur J Nucl Med Mol Imaging. 2014;41:452–61. doi:10.1007/s00259-013-2571-z.CrossRefPubMed Ryu IS, Kim JS, Roh JL, Cho KJ, Choi SH, Nam SY, et al. Prognostic significance of preoperative metabolic tumour volume and total lesion glycolysis measured by (18)F-FDG PET/CT in squamous cell carcinoma of the oral cavity. Eur J Nucl Med Mol Imaging. 2014;41:452–61. doi:10.​1007/​s00259-013-2571-z.CrossRefPubMed
Metadata
Title
Elevated tumor-to-liver uptake ratio (TLR) from 18F–FDG-PET/CT predicts poor prognosis in stage IIA colorectal cancer following curative resection
Authors
Jun Huang
Liang Huang
Jiaming Zhou
Yinghua Duan
Zhanwen Zhang
Xiaoyan Wang
Pinzhu Huang
Shuyun Tan
Ping Hu
Jianping Wang
Meijin Huang
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 12/2017
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-017-3779-0

Other articles of this Issue 12/2017

European Journal of Nuclear Medicine and Molecular Imaging 12/2017 Go to the issue