Abstract
Purpose
We evaluated the ability of pretreatment 18 F-FDG uptake by regional lymph nodes to predict the survival of patients with resectable colorectal cancer.
Methods
The records of 78 patients with AJCC stage III colorectal cancer (pathologically confirmed node-positive disease without evidence of distant metastasis) treated with surgery and adjuvant chemotherapy were retrospectively reviewed. The maximum standardized uptake values of the primary tumor (SUVp) and regional lymph nodes (SUVn) were measured by pretreatment 18 F-FDG PET/CT. The ROC curve analyses and the Cox proportional hazard model were used to analyze whether SUVp, SUVn, and clinicopathologic parameters could predict disease-free survival.
Results
Although there were no significant differences between the median SUVp in the event group and that in the non-event group, the median SUVn was significantly higher in the event group (1.7) than in the non-event group (0.8, p = 0.023). Based on the ROC curve analysis, SUVn predicted the event for disease-free survival (AUC = 0.668, p = 0.02) with the optimal criterion, sensitivity, specificity, and accuracy of > 1.2, 71 %, 63 %, and 65 %, respectively. However, SUVp did not predict disease-free survival (AUC = 0.570, p = 0.349). Univariate analysis revealed that SUVn (p = 0.011) and venous invasion (p = 0.016) were associated with disease-free survival, but pathologic N stage was not (p = 0.09). By multivariate analysis, only SUVn > 1.2 independently shortened the disease-free survival (relative risk, 2.97; 95 % CI, 1.14–7.74, p = 0.026).
Conclusion
SUVn before surgery may be a useful prognostic marker in patients with AJCC stage III colorectal cancer.
Similar content being viewed by others
References
Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin. 2011;61:212–36.
Greene FL, Page DL, Fleming ID, Fritz A, Balch CM, Haller DG. AJCC cancer staging manual. 6th ed. New York: Springer; 2002.
Resch A, Langner C. Lymph node staging in colorectal cancer: old controversies and recent advances. World J Gastroenterol. 2013;19:8515–26.
Vather R, Sammour T, Kahokehr A, Connolly A, Hill A. Quantitative lymph node evaluation as an independent marker of long-term prognosis in stage III rectal cancer. ANZ J Surg. 2011;81:883–8.
Nagtegaal ID, Tot T, Jayne DG, McShane P, Nihlberg A, Marshall HC, et al. Lymph nodes, tumor deposits, and TNM: are we getting better? J Clin Oncol. 2011;29:2487–92.
Huh JW, Kim CH, Kim HR, Kim YJ. Factors predicting oncologic outcomes in patients with fewer than 12 lymph nodes retrieved after curative resection for colon cancer. J Surg Oncol. 2012;105:125–9.
Lu YY, Chen JH, Ding HJ, Chien CR, Lin WY, Kao CH. A systematic review and meta-analysis of pretherapeutic lymph node staging of colorectal cancer by 18 F-FDG PET or PET/CT. Nucl Med Commun. 2012;33:1127–33.
Briggs RH, Chowdhury FU, Lodge JP, Scarsbrook AF. Clinical impact of FDG PET-CT in patients with potentially operable metastatic colorectal cancer. Clin Radiol. 2011;66:1167–74.
Cho YB, Chun HK, Kim MJ, Choi JY, Park CM, Kim BT, et al. Accuracy of MRI and 18 F-FDG PET/CT for restaging after preoperative concurrent chemoradiotherapy for rectal cancer. World J Surg. 2009;33:2688–94.
de Geus-Oei LF, Vriens D, van Laarhoven HW, van der Graaf WT, Oyen WJ. Monitoring and predicting response to therapy with 18 F-FDG PET in colorectal cancer: a systematic review. J Nucl Med. 2009;50(suppl):43S–54S.
Song BI, Lee SW, Jeong SY, Chae YS, Lee WK, Ahn BC, et al. 18 F-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.
Liao CT, Chang JT, Wang HM, Ng SH, Huang SF, Chen IH, et al. Preoperative [18 F]-fluorodeoxyglucose positron emission tomography standardized uptake value of neck lymph nodes may aid in selecting patients with oral cavity squamous cell carcinoma for salvage therapy after relapse. Eur J Nucl Med Mol Imaging. 2009;36:1783–93.
Lee JE, Kim SW, Kim JS, Choi KY, Kang WK, Oh ST, et al. Prognostic value of 18-fluorodeoxyglucose positron emission tomography-computed tomography in resectable colorectal cancer. World J Gastroenterol. 2012;18:5072–7.
Krabbe CA, Pruim J, Dijkstra PU, Balink H, van der Laan BF, de Visscher JG, et al. 18 F-FDG PET as a routine posttreatment surveillance tool in oral and oropharyngeal squamous cell carcinoma: a prospective study. J Nucl Med. 2009;50:1940–7.
Tsunoda Y, Ito M, Fujii H, Kuwano H, Saito N. Preoperative diagnosis of lymph node metastases of colorectal cancer by FDG-PET/CT. Jpn J Clin Oncol. 2008;38:347–53.
Na SJ, Chung YA, Maeng LS, Kim KJ, Sohn KM, Kim SH, et al. Comparison between FDG uptake and pathologic or immunohistochemical parameters in pre-operative PET/CT scan of patient with primary colorectal cancer. Nucl Med Mol Imaging. 2009;43:557–64.
Andre T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C, et al. Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J Clin Oncol. 2009;27:3109–16.
Punt CJ, Buyse M, Kohne CH, Hohenberger P, Labianca R, Schmoll HJ, et al. Endpoints in adjuvant treatment trials: a systematic review of the literature in colon cancer and proposed definitions for future trials. J Natl Cancer Inst. 2007;99:998–1003.
Cain KC, Lange NT. Approximate case influence for the proportional hazards regression model with censored data. Biometrics. 1984;40:493–9.
Aalen OO. Further results on the non-parametric linear regression model in survival analysis. Stat Med. 1993;12:1569–88.
Lemeshow S, Hosmer Jr DW. A review of goodness of fit statistics for use in the development of logistic regression models. Am J Epidemiol. 1982;115:92–106.
Harrell Jr FE, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15:361–87.
Vesselle H, Salskov A, Turcotte E, Wiens L, Schmidt R, Jordan CD, et al. Relationship between non-small cell lung cancer FDG uptake at PET, tumor histology, and ki-67 proliferation index. J Thorac Oncol. 2008;3:971–8.
Kim YH, Choi JY, Do IG, Kim S, Kim BT. Factors affecting 18 F-FDG uptake by metastatic lymph nodes in gastric cancer. J Comput Assist Tomogr. 2013;37:815–9.
de la Fuente SG, Manson RJ, Ludwig KA, Mantyh CR. Neoadjuvant chemoradiation for rectal cancer reduces lymph node harvest in proctectomy specimens. J Gastrointest Surg. 2009;13:269–4.
Sastre J, Custodio A, Sanchez JC, Ortega L, Rodriguez L, Puente J, et al. Risk-adapted adjuvant chemotherapy after concomitant fluoropyrimidine-radiotherapy neoadjuvant treatment for patients with resectable cT3-4 or N + rectal cancer. Anticancer Drugs. 2011;22:185–90.
Martoni AA, Di Fabio F, Pinto C, Castellucci P, Pini S, Ceccarelli C, et al. Prospective study on the FDG-PET/CT predictive and prognostic values in patients treated with neoadjuvant chemoradiation therapy and radical surgery for locally advanced rectal cancer. Ann Oncol. 2011;22:650–6.
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 18 F-2-fluoro-2-deoxy-D-glucose uptake by positron emission tomography in colorectal cancer. Dig Dis Sci. 2006;51:2198–205.
Kornprat P, Pollheimer MJ, Lindtner RA, Schlemmer A, Rehak P, Langner C. Value of tumor size as a prognostic variable in colorectal cancer: a critical reappraisal. Am J Clin Oncol. 2011;34:43–9.
Tomoda H, Taketomi A, Baba H, Kohnoe S, Seo Y, Saito T. The clinicopathological characteristics and outcome of patients with right colon cancer. Oncol Rep. 1998;5:481–3.
Oh JR, Min JJ, Song HC, Chong A, Kim GE, Choi C, et al. A stepwise approach using metabolic volume and SUVmax to differentiate malignancy and dysplasia from benign colonic uptakes on 18 F-FDG PET/CT. Clin Nucl Med. 2012;37:e134–40.
Chan KK, Dassanayake B, Deen R, Wickramarachchi RE, Kumarage SK, Samita S, et al. Young patients with colorectal cancer have poor survival in the first twenty months after operation and predictable survival in the medium and long-term: analysis of survival and prognostic markers. World J Surg Oncol. 2010;8:82.
LeBlanc JK. Imaging and management of rectal cancer. Natl Clin Pract Gastroenterol Hepatol. 2007;4:665–76.
Brown G, Richards CJ, Bourne MW, Newcombe RG, Radcliffe AG, Dallimore NS, et al. Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology. 2003;227:371–7.
Mizukami Y, Ueda S, Mizumoto A, Sasada T, Okumura R, Kohno S, et al. Diffusion-weighted magnetic resonance imaging for detecting lymph node metastasis of rectal cancer. World J Surg. 2011;35:895–9.
Attenberger UI, Pilz LR, Morelli JN, Hausmann D, Doyon F, Hofheinz R, et al. Multi-parametric MRI of rectal cancer—do quantitative functional MR measurements correlate with radiologic and pathologic tumor stages? Eur J Radiol. 2014. doi:10.1016/j.ejrad.2014.03.012.
Haldorsen IS, Grüner R, Husby JA, Magnussen IJ, Werner HM, Salvesen OO, et al. Dynamic contrast-enhanced MRI in endometrial carcinoma identifies patients at increased risk of recurrence. Eur Radiol. 2013;23:2916–25.
Valles FE, Perez-Valles CL, Regalado S, Barajas RF, Rubenstein JL, Cha S. Combined diffusion and perfusion MR imaging as biomarkers of prognosis in immunocompetent patients with primary central nervous system lymphoma. AJNR Am J Neuroradiol. 2013;34:35–40.
Lim JS, Kim D, Baek SE, Myoung S, Choi J, Shin SJ, et al. Perfusion MRI for the prediction of treatment response after preoperative chemoradiotherapy in locally advanced rectal cancer. Eur Radiol. 2012;22:1693–700.
Chawla S, Kim S, Loevner LA, Hwang WT, Weinstein G, Chalian A, et al. Prediction of disease-free survival in patients with squamous cell carcinomas of the head and neck using dynamic contrast-enhanced MR imaging. AJNR Am J Neuroradiol. 2011;32:778–84.
Hoetjes NJ, van Velden FH, Hoekstra OS, Hoekstra CJ, Krak NC, Lammertsma AA, et al. Partial volume correction strategies for quantitative FDG PET in oncology. Eur J Nucl Med Mol Imaging. 2010;37:1679–87.
Acknowledgments
This work was supported by Establishment of Center for PET Application Technology Development, the Korea Institute of Radiological and Medical Sciences (KIRAMS), and by grants from the Ministry of Education, Science and Technology (50441–2014).
Conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Fig. 1
(PDF 70 kb)
Supplementary Fig. 2
(PDF 83 kb)
Rights and permissions
About this article
Cite this article
Byun, B.H., Moon, S.M., Shin, U.S. et al. Prognostic value of 18 F-FDG uptake by regional lymph nodes on pretreatment PET/CT in patients with resectable colorectal cancer. Eur J Nucl Med Mol Imaging 41, 2203–2211 (2014). https://doi.org/10.1007/s00259-014-2840-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00259-014-2840-5