Prognostic value of 18F-FDG PET image-based parameters in oesophageal cancer and impact of tumour delineation methodology

  • Mathieu Hatt
  • Dimitris Visvikis
  • Nidal M. Albarghach
  • Florent Tixier
  • Olivier Pradier
  • Catherine Cheze-le Rest
Original Article

Abstract

Purpose

18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) image-derived parameters, such as standardized uptake value (SUV), functional tumour length (TL) and tumour volume (TV) or total lesion glycolysis (TLG), may be useful for determining prognosis in patients with oesophageal carcinoma. The objectives of this work were to investigate the prognostic value of these indices in oesophageal cancer patients undergoing combined chemoradiotherapy treatment and the impact of TV delineation strategies.

Methods

A total of 45 patients were retrospectively analysed. Tumours were delineated on pretreatment 18F-FDG scans using adaptive threshold and automatic (fuzzy locally adaptive Bayesian, FLAB) methodologies. The maximum standardized uptake value (SUVmax), SUVpeak, SUVmean, TL, TV and TLG were computed. The prognostic value of each parameter for overall survival was investigated using Kaplan-Meier and Cox regression models for univariate and multivariate analyses, respectively.

Results

Large differences were observed between methodologies (from −140 to +50% for TV). SUV measurements were not significant prognostic factors for overall survival, whereas TV, TL and TLG were, irrespective of the segmentation strategy. After multivariate analysis including standard tumour staging, only TV (p < 0.002) and TL (p = 0.042) determined using FLAB were independent prognostic factors.

Conclusion

Whereas no SUV measurement was a significant prognostic factor, TV, TL and TLG were significant prognostic factors for overall survival, irrespective of the delineation methodology. Only functional TV and TL derived using FLAB were independent prognostic factors, highlighting the need for accurate and robust PET tumour delineation tools for oncology applications.

Keywords

PET Tumour volume Tumour segmentation Oesophageal cancer Survival 

Notes

Conflicts of interest

None.

References

  1. 1.
    Falk GW. Risk factors for esophageal cancer development. Surg Oncol Clin N Am 2009;18(3):469–85.PubMedCrossRefGoogle Scholar
  2. 2.
    Flamen P, Lerut A, Van Cutsem E, De Wever W, Peeters M, Stroobants S, et al. Utility of positron emission tomography for the staging of patients with potentially operable esophageal carcinoma. J Clin Oncol 2000;18:3202–10.PubMedGoogle Scholar
  3. 3.
    Heeren PA, Jager PL, Bongaerts F, van Dullemen H, Sluiter W, Plukker JT. Detection of distant metastases in esophageal cancer with (18)F-FDG PET. J Nucl Med 2004;45:980–7.PubMedGoogle Scholar
  4. 4.
    van Vliet EP, Heijenbrok-Kal MH, Hunink MG, Kuipers EJ, Siersema PD. Staging investigations for oesophageal cancer: a meta-analysis. Br J Cancer 2008;98(3):547–57.PubMedCrossRefGoogle Scholar
  5. 5.
    Kim TJ, Kim HY, Lee KW, Kim MS. Multimodality assessment of esophageal cancer: preoperative staging and monitoring of response to therapy. Radiographics 2009;29(2):403–2.PubMedCrossRefGoogle Scholar
  6. 6.
    Chuang HH, Macapinlac HA. The evolving role of PET-CT in the management of esophageal cancer. Q J Nucl Med Mol Imaging 2009;53(2):201–9.PubMedGoogle Scholar
  7. 7.
    MacManus M, Nestle U, Rosenzweig KE, Carrio I, Messa C, Belohlavek O, et al. Use of PET and PET/CT for radiation therapy planning: IAEA expert report 2006–2007. Radiother Oncol 2009;91(1):85–94.PubMedCrossRefGoogle Scholar
  8. 8.
    Grégoire V, Haustermans K, Geets X, Roeis S, Lonneux M. PET-based treatment planning in radiotherapy: a new standard? J Nucl Med 2007;48(S1):68S–77.PubMedGoogle Scholar
  9. 9.
    Howard A, Mehta MP, Ritter MA, Bradley KA, Tome WA, Chappell RJ et al. The value of PET/CT in gross tumor volume delineation in lung and esophagus cancer. Int J Radiat Oncol Biol Phys 2004;60(Suppl):S536–7.CrossRefGoogle Scholar
  10. 10.
    Choi JY, Jang HY, Shim YM, Kim K, Lee KS, Lee KH, et al. 18F-FDG PET in patients with esophageal squamous cell carcinoma undergoing curative surgery: prognostic implications. J Nucl Med 2004;45(11):1843–50.PubMedGoogle Scholar
  11. 11.
    Mamede M, Abreu-E-Lima P, Oliva MR, Nosé V, Mamon H, Gerbaudo VH. FDG-PET/CT tumor segmentation-derived indices of metabolic activity to assess response to neoadjuvant therapy and progression-free survival in esophageal cancer: correlation with histopathology results. Am J Clin Oncol 2007;30(4):377–88.PubMedCrossRefGoogle Scholar
  12. 12.
    Hyun SH, Choi JY, Shim YM, Kim K, Lee SJ, Cho YS, et al. Prognostic value of metabolic tumor volume measured by 18F-fluorodeoxyglucose positron emission tomography in patients with esophageal carcinoma. Ann Surg Oncol 2010;17:115–22.PubMedCrossRefGoogle Scholar
  13. 13.
    Hong D, Lunagomez S, Kim EE, Lee JH, Bresalier RS, Swisher SG, et al. Value of baseline positron emission tomography for predicting overall survival in patient with nonmetastatic esophageal or gastroesophageal junction carcinoma. Cancer 2005;104:1620–6.PubMedCrossRefGoogle Scholar
  14. 14.
    Blackstock AW, Farmer MR, Lovato J, Mishra G, Melin SA, Oaks T, et al. A prospective evaluation of the impact of 18-F-fluoro-deoxy-D-glucose positron emission tomography staging on survival for patients with locally advanced esophageal cancer. Int J Radiat Oncol Biol Phys 2006;64:455–60.PubMedCrossRefGoogle Scholar
  15. 15.
    van Westreenen HL, Plukker JT, Cobben DC, Verhoogt CJ, Groen H, Jager PL. Prognostic value of the standardized uptake value in esophageal cancer. AJR Am J Roentgenol 2005;185(2):436–40.PubMedGoogle Scholar
  16. 16.
    Omloo JM, Sloof GW, Boellaard R, Hoekstra OS, Jager PL, van Dulleman HM, et al. Importance of fluorodeoxyglucose-positron emission tomography (FDG-PET) and endoscopic ultrasonography parameters in predicting survival following surgery for esophageal cancer. Endoscopy 2008;40(6):464–71.PubMedCrossRefGoogle Scholar
  17. 17.
    Kato H, Nakajima M, Sohda M, Tanaka N, Inose T, Miyazaki T, et al. The clinical application of (18)F-fluorodeoxyglucose positron emission tomography to predict survival in patients with operable esophageal cancer. Cancer 2009;115:3196–203.PubMedCrossRefGoogle Scholar
  18. 18.
    Cheze-Le Rest C, Metges JP, Teyton P, Jestin-Le Tallec V, Lozac’h P, Volant A, et al. Prognostic value of initial fluorodeoxyglucose-PET in esophageal cancer: a prospective study. Nucl Med Commun 2008;29:628–35.PubMedCrossRefGoogle Scholar
  19. 19.
    Cerfolio RJ, Bryant AS. Maximum standardized uptake values on positron emission tomography of esophageal cancer predicts stage, tumor biology, and survival. Ann Thorac Surg 2006;82:391–5.PubMedCrossRefGoogle Scholar
  20. 20.
    Rizk N, Downey RJ, Akhurst T, Gonen M, Bains MS, Larson S, et al. Preoperative 18[F]-fluorodeoxyglucose positron emission tomography standardized uptake values predict survival after esophageal adenocarcinoma resection. Ann Thorac Surg 2006;81:1076–81.PubMedCrossRefGoogle Scholar
  21. 21.
    Yendamuri S, Swisher SG, Correa AM, Hofstetter W, Ajani JA, Francis A, et al. Esophageal tumor length is independently associated with long-term survival. Cancer 2009;115:508–16.PubMedCrossRefGoogle Scholar
  22. 22.
    Roedl JB, Harisinghani MG, Colen RR, Fischman AJ, Blake MA, Mathisen DJ, et al. Assessment of treatment response and recurrence in esophageal carcinoma based on tumor length and standardized uptake value on positron emission tomography-computed tomography. Ann Thorac Surg 2008;86(4):1131–8.PubMedCrossRefGoogle Scholar
  23. 23.
    Nestle U, Kremp S, Schaefer-Schuler A, Sebastian-Welsch C, Hellwig D, Rübe C, et al. Comparison of different methods for delineation of 18F-FDG PET-positive tissue for target volume definition in radiotherapy of patients with non-small cell lung cancer. J Nucl Med 2005;46(8):1342–8.PubMedGoogle Scholar
  24. 24.
    Hatt M, Cheze-le Rest C, Descourt P, Dekker A, De Ruysscher D, Oellers M, et al. Accurate automatic delineation of heterogeneous functional volumes in positron emission tomography for oncology applications. Int J Radiat Oncol Biol Phys 2010;77:301–8.PubMedCrossRefGoogle Scholar
  25. 25.
    Larson SM, Erdi Y, Akhurst T, Mazumdar M, Macpinlac HA, Finn RD, et al. Tumor treatment response based on visual and quantitative changes in global tumor glycolysis using PET-FDG imaging. The visual response score and the change in total lesion glycolysis. Clin Positron Imaging 1999;2:159–71.PubMedCrossRefGoogle Scholar
  26. 26.
    Velasquez LM, Boellaard R, Kollia G, Hayes W, Hoekstra OS, Lammertsma AA, et al. Repeatability of 18F-FDG PET in a multicenter phase I study of patients with advanced gastrointestinal malignancies. J Nucl Med 2009;50(10):1646–54.PubMedCrossRefGoogle Scholar
  27. 27.
    Hatt M, Cheze le Rest C, Turzo A, Roux C, Visvikis D. A fuzzy locally adaptive Bayesian segmentation approach for volume determination in PET. IEEE Trans Med Imaging 2009;28(6):881–93.PubMedCrossRefGoogle Scholar
  28. 28.
    Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1:307–10.PubMedCrossRefGoogle Scholar
  29. 29.
    Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958;53:457–81.CrossRefGoogle Scholar
  30. 30.
    Metz CE. Basic principles of ROC analysis. Semin Nucl Med 1978;8(4):283–98.PubMedCrossRefGoogle Scholar
  31. 31.
    Greene FL, Page DL, Fleming ID, et al. AJCC cancer staging manual. 6th ed. New York: Springer; 2002.CrossRefGoogle Scholar
  32. 32.
    Cox DR. Regression models and life tables. J R Stat Soc B 1972;34(2):187–220.Google Scholar
  33. 33.
    van Heijl M, Omloo JM, van Berge Henegouwen MI, van Lanschot JJ, Sloof GW, Boellaard R. Influence of ROI definition, partial volume correction and SUV normalization on SUV-survival correlation in oesophageal cancer. Nucl Med Commun 2010;31(7):652–8.PubMedGoogle Scholar
  34. 34.
    Himeno S, Yasuda S, Shimada H, Tajima T, Makuuchi H. Evaluation of esophageal cancer by positron emission tomography. Jpn J Clin Oncol 2002;32:340–6.PubMedCrossRefGoogle Scholar
  35. 35.
    Fukunaga T, Okazumi S, Koide Y, Isono K, Imazeki K. Evaluation of esophageal cancers using fluorine-18-fluorodeoxyglucose PET. J Nucl Med 1998;39:1002–7.PubMedGoogle Scholar
  36. 36.
    Taylor MD, Smith PW, Brix WK, Wick MR, Theodosakis N, Swenson BR, et al. Correlations between selected tumor markers and fluorodeoxyglucose maximal standardized uptake values in esophageal cancer. Eur J Cardiothorac Surg 2009;35:699–705.PubMedCrossRefGoogle Scholar
  37. 37.
    Swisher S, Erasmus J, Maish M, Correa AM, Macapinlac H, Ajani JA, et al. 2-Fluoro-2-deoxy-D-glucose positron emission tomography imaging is predictive of pathologic response and survival after preoperative chemoradiation in patients with esophageal carcinoma. Cancer 2004;101:1776–85.PubMedCrossRefGoogle Scholar
  38. 38.
    Zhong X, Yu J, Zhang B, Li D, Han A, Song P, et al. Using 18F-fluorodeoxyglucose positron emission tomography to estimate the length of gross tumor in patients with squamous cell carcinoma of the esophagus. Int J Radiat Oncol Biol Phys 2009;73(1):136–41.PubMedCrossRefGoogle Scholar
  39. 39.
    Tylski P, Stute S, Grotus N, Doyeux K, Hapdey S, Gardin I, et al. Comparative assessment of methods for estimating tumor volume and standardized uptake value in (18)F-FDG PET. J Nucl Med 2010;51(2):268–76.PubMedCrossRefGoogle Scholar
  40. 40.
    Xie P, Yue JB, Zhao HX, Sun XD, Kong L, Fu Z, et al. Prognostic value of (18)F-FDG PET-CT metabolic index for nasopharyngeal carcinoma. J Cancer Res Clin Oncol 2010;136(6):883–9.PubMedCrossRefGoogle Scholar
  41. 41.
    Cazaentre T, Morschhauser F, Vermandel M, Betrouni N, Prangère T, Steinling M, et al. Pre-therapy 18F-FDG PET quantitative parameters help in predicting the response to radioimmunotherapy in non-Hodgkin lymphoma. Eur J Nucl Med Mol Imaging 2010;37(3):494–504.PubMedCrossRefGoogle Scholar
  42. 42.
    Hatt M, Cheze Le Rest C, Aboagye EO, et al. Reproducibility of 18F-FDG and 3′-deoxy-3′-18F-fluorothymidine PET tumor volume measurements. J Nucl Med 2010;51(9):1368–76.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Mathieu Hatt
    • 1
  • Dimitris Visvikis
    • 1
  • Nidal M. Albarghach
    • 1
    • 3
  • Florent Tixier
    • 1
  • Olivier Pradier
    • 1
    • 3
  • Catherine Cheze-le Rest
    • 1
    • 2
  1. 1.INSERM, U650 LaTIMCHU MorvanBrestFrance
  2. 2.Academic Department of Nuclear MedicineCHU MorvanBrestFrance
  3. 3.Department of RadiotherapyCHU MorvanBrestFrance

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