Skip to main content
Log in

Quantifying tumour heterogeneity in 18F-FDG PET/CT imaging by texture analysis

  • Review Article
  • Published:
European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

18F-Fluorodeoxyglucose positron emission tomography/computed tomography (18F-FDG PET/CT) is now routinely used in oncological imaging for diagnosis and staging and increasingly to determine early response to treatment, often employing semiquantitative measures of lesion activity such as the standardized uptake value (SUV). However, the ability to predict the behaviour of a tumour in terms of future therapy response or prognosis using SUVs from a baseline scan prior to treatment is limited. It is recognized that medical images contain more useful information than may be perceived with the naked eye, leading to the field of “radiomics” whereby additional features can be extracted by computational postprocessing techniques. In recent years, evidence has slowly accumulated showing that parameters obtained by texture analysis of radiological images, reflecting the underlying spatial variation and heterogeneity of voxel intensities within a tumour, may yield additional predictive and prognostic information. It is hoped that measurement of these textural features may allow better tissue characterization as well as better stratification of treatment in clinical trials, or individualization of future cancer treatment in the clinic, than is possible with current imaging biomarkers. In this review we focus on the literature describing the emerging methods of texture analysis in 18FDG PET/CT, as well as other imaging modalities, and how the measurement of spatial variation of voxel grey-scale intensity within an image may provide additional predictive and prognostic information, and postulate the underlying biological mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG, Granton P, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48:441–6.

    Article  PubMed  Google Scholar 

  2. Hillner BE, Siegel BA, Liu D, Shields AF, Gareen IF, Hanna L, et al. Impact of positron emission tomography/computed tomography and positron emission tomography (PET) alone on expected management of patients with cancer: initial results from the National Oncologic PET Registry. J Clin Oncol. 2007;26:2155–61.

    Article  Google Scholar 

  3. Juweid ME, Cheson BD. Positron emission tomography and assessment of cancer therapy. N Engl J Med. 2006;354:496–507.

    Article  PubMed  CAS  Google Scholar 

  4. Ben-Haim S, Ell P. 18F-FDG PET and PET/CT in the evaluation of cancer treatment response. J Nucl Med. 2009;50:88–99.

    Article  PubMed  Google Scholar 

  5. Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med. 2009;50:122S–50.

    Article  PubMed  CAS  Google Scholar 

  6. Cremerius U, Effert PJ, Adam G, Sabri O, Zimmy M, Wagenknecht G, et al. FDG PET for detection and therapy control of metastatic germ cell tumor. J Nucl Med. 1998;39:815–22.

    PubMed  CAS  Google Scholar 

  7. Dehdashti F, Mortimer JE, Trinkaus K, Naughton MJ, Ellis M, Katzenellenbogen JA, et al. PET-based estradiol challenge as a predictive biomarker of response to endocrine therapy in women with estrogen-receptor-positive breast cancer. Breast Cancer Res Treat. 2009;113:509–17.

    Article  PubMed  CAS  Google Scholar 

  8. Mac Manus MP, Ding Z, Hogg A, Herschtal A, Binns D, Ball DL, et al. Association between pulmonary uptake of fluorodeoxyglucose detected by positron emission tomography scanning after radiation therapy for non-small-cell lung cancer and radiation pneumonitis. Int J Radiat Oncol Biol Phys. 2011;80:1365–71.

    Article  PubMed  Google Scholar 

  9. de Geus-Oei LF, van der Heijden HF, Visser EP, Hermsen R, van Hoorn BA, Timmer-Bonte JN, et al. Chemotherapy response evaluation with 18F-FDG PET in patients with non-small cell lung cancer. J Nucl Med. 2007;48:1592–8.

    Article  PubMed  Google Scholar 

  10. Rizk NP, Tang L, Adusumilli PS, Bains MS, Akhurst TJ, Ilson D, et al. Predictive value of initial PET SUVmax in patients with locally advanced esophageal and gastroesophageal junction adenocarcinoma. J Thorac Oncol. 2009;4:875–9.

    Article  PubMed  Google Scholar 

  11. Ohno Y, Koyama H, Yoshikawa T, Matsumoto K, Aoyama N, Onishi Y, et al. Diffusion-weighted MRI versus 18F-FDG PET/CT: performance as predictors of tumor treatment response and patient survival in patients with non-small cell lung cancer receiving chemoradiotherapy. AJR Am J Roentgenol. 2012;198:75–82.

    Article  PubMed  Google Scholar 

  12. Zhang HQ, Yu JM, Meng X, Yue JB, Feng R, Ma L. Prognostic value of serial [18F]fluorodeoxyglucose PET-CT uptake in stage III patients with non-small cell lung cancer treated by concurrent chemoradiotherapy. Eur J Radiol. 2011;77:92–6.

    Article  PubMed  Google Scholar 

  13. Borst GR, Belderbos JS, Boellaard R, Comans EF, De Jaeger K, Lammertsma AA, et al. Standardised FDG uptake: a prognostic factor for inoperable non-small cell lung cancer. Eur J Cancer. 2005;41:1533–41.

    Article  PubMed  Google Scholar 

  14. Lee KH, Lee SH, Kim DW, Kang WJ, Chung JK, Im SA, et al. High fluorodeoxyglucose uptake on positron emission tomography in patients with advanced non-small cell lung cancer on platinum-based combination chemotherapy. Clin Cancer Res. 2006;12:4232–6.

    Article  PubMed  CAS  Google Scholar 

  15. 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;37:494–504.

    Article  PubMed  CAS  Google Scholar 

  16. Colavolpe C, Metellus P, Mancini J, Barrie M, Béquet-Boucard C, Figarella-Branger D, et al. Independent prognostic value of pre-treatment 18-FDG-PET in high-grade gliomas. J Neurooncol. 2012;107:527–35.

    Article  PubMed  Google Scholar 

  17. Xie P, Li M, Zhao H, Sun X, Fu Z, Yu J. 18F-FDG PET or PET-CT to evaluate prognosis for head and neck cancer: a meta-analysis. J Cancer Res Clin Oncol. 2011;137:1085–93.

    Article  PubMed  Google Scholar 

  18. Kitagawa Y, Sano K, Nishizawa S, Nakamura M, Ogasawara T, Sadato N, et al. FDG-PET for prediction of tumour aggressiveness and response to intra-arterial chemotherapy and radiotherapy in head and neck cancer. Eur J Nucl Med Mol Imaging. 2003;30:63–71.

    Article  PubMed  CAS  Google Scholar 

  19. Kidd EA, Dehdashti F, Siegel BA, Grigsby PW. Anal cancer maximum F-18 fluorodeoxyglucose uptake on positron emission tomography is correlated with prognosis. Radiother Oncol. 2010;95:288–91.

    Article  PubMed  Google Scholar 

  20. Zhu W, Xing L, Yue J, Sun X, Sun X, Zhao H, et al. Prognostic significance of SUV on PET/CT in patients with localised oesophagogastric junction cancer receiving neoadjuvant chemotherapy/chemoradiation: a systematic review and meta-analysis. Br J Radiol. 2012;85:e694–701.

    Article  PubMed  CAS  Google Scholar 

  21. Henriksson E, Kjellen E, Wahlberg P, Ohlsson T, Wennerberg J, Brun E. 2-Deoxy-2-[18F]fluoro-D-glucose uptake and correlation to intratumoral heterogeneity. Anticancer Res. 2007;27:2155–9.

    PubMed  CAS  Google Scholar 

  22. van Velden FH, Cheebsumon P, Yaqub M, Smit EF, Hoekstra OS, Lammertsma AA, et al. Evaluation of a cumulative SUV-volume histogram method for parameterizing heterogeneous intratumoural FDG uptake in non-small cell lung cancer PET studies. Eur J Nucl Med Mol Imaging. 2011;38:1636–47.

    Article  PubMed  Google Scholar 

  23. Yu H, Caldwell C, Mah K, Poon I, Balogh J, MacKenzie R, et al. Automated radiation targeting in head-and-neck cancer using region-based texture analysis of PET and CT images. Int J Radiat Oncol Biol Phys. 2009;75:618–25.

    Article  PubMed  Google Scholar 

  24. 2Yu H, Caldwell C, Mah K, Mozeg D. Coregistered FDG PET/CT-based textural characterization of head and neck cancer for radiation treatment planning. IEEE Trans Med Imaging. 2009;28:374–83.

    Article  PubMed  Google Scholar 

  25. Eary JF, O’Sullivan F, O’Sullivan J, Conrad EU. Spatial heterogeneity in sarcoma 18F-FDG uptake as a predictor of patient outcome. J Nucl Med. 2008;49:1973–9.

    Article  PubMed  Google Scholar 

  26. Tixier F, Cheze Le Rest C, Hatt M, Albarghach N, Pradier O, Metges JP, et al. Intratumor heterogeneity characterized by textural features on baseline 18F-FDG PET images predicts response to concomitant radiochemotherapy in esophageal cancer. J Nucl Med. 2011;52:369–78.

    Article  PubMed  Google Scholar 

  27. El Naqa I, Grigsby P, Apte A, Kidd E, Donnelly E, Khullar D, et al. Exploring feature-based approaches in PET images for predicting cancer treatment outcomes. Pattern Recognit. 2009;42:1162–71.

    Article  PubMed  Google Scholar 

  28. Vaidya M, Creach KM, Frye J, Dehdashti F, Bradley JD, El Naqa I. Combined PET/CT image characteristics for radiotherapy tumor response in lung cancer. Radiother Oncol. 2012;102:239–45.

    Article  PubMed  Google Scholar 

  29. Castellano G, Bonilha L, Li LM, Cendes F. Texture analysis of medical images. Clin Radiol. 2004;59:1061–9.

    Article  PubMed  CAS  Google Scholar 

  30. Al-Kadi OS, Watson D. Texture analysis of aggressive and nonaggressive lung tumor CE CT images. IEEE Trans Biomed Eng. 2008;55:1822–30.

    Article  PubMed  Google Scholar 

  31. Ganeshan B, Miles KA, Young RC, Chatwin CR. Hepatic entropy and uniformity: additional parameters that can potentially increase the effectiveness of contrast enhancement during abdominal CT. Clin Radiol. 2007;62:761–8.

    Article  PubMed  CAS  Google Scholar 

  32. Brown RA, Frayne R. A comparison of texture quantification techniques based on the Fourier and S transforms. Med Phys. 2008;35:4998–5008.

    Article  PubMed  Google Scholar 

  33. Goh V, Sanghera B, Wellsted DM, Sundin J, Halligan S. Assessment of the spatial pattern of colorectal tumour perfusion estimated at perfusion CT using two-dimensional fractal analysis. Eur Radiol. 2009;19:1358–65.

    Article  PubMed  Google Scholar 

  34. Sanghera B, Banerjee D, Khan A, Simcock I, Stirling JJ, Glynne Jones R, et al. Reproducibility of 2D and 3D fractal analysis techniques for the assessment of spatial heterogeneity of regional blood flow in rectal cancer. Radiology. 2012;263:865–73.

    Article  PubMed  Google Scholar 

  35. Craciunescu OI, Das SK, Clegg ST. Dynamic contrast-enhanced MRI and fractal characteristics of percolation clusters in two-dimensional tumor blood perfusion. J Biomech Eng. 1999;121:480–6.

    Article  PubMed  CAS  Google Scholar 

  36. Dettori L, Semler L. A comparison of wavelet, ridgelet, and curvelet-based texture classification algorithms in computed tomography. Comput Biol Med. 2007;37:486–98.

    Article  PubMed  Google Scholar 

  37. Al-Kadi OS. Assessment of texture measures susceptibility to noise in conventional and contrast enhanced computed tomography lung tumour images. Comput Med Imaging Graph. 2010;34:494–503.

    Article  PubMed  Google Scholar 

  38. Amadasun M, King R. Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern. 1989;19:1264–74.

    Article  Google Scholar 

  39. Veenland JF, Grashuis JL, Gelsema ES. Texture analysis in radiographs: the influence of modulation transfer function and noise on the discriminative ability of texture features. Med Phys. 1998;25:922–36.

    Article  PubMed  CAS  Google Scholar 

  40. Galavis PE, Hollensen C, Jallow N, Paliwal B, Jeraj R. Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta Oncol. 2010;49:1012–6.

    Article  PubMed  Google Scholar 

  41. Tixier F, Hatt M, Le Rest CC, Le Pogam A, Corcos L, Visvikis D. Reproducibility of tumor uptake heterogeneity characterization through textural feature analysis in 18F-FDG PET. J Nucl Med. 2012;53:693–700.

    Article  PubMed  Google Scholar 

  42. Lodge MA, Lucas JD, Marsden PK, Cronin BF, O’Doherty MJ, Smith MA. A PET study of 18FDG uptake in soft tissue masses. Eur J Nucl Med. 1999;26:22–30.

    Article  PubMed  CAS  Google Scholar 

  43. Wang Z, Gierriero A, Sario M. Comparison of several approaches for segmentation of texture images. Patt Recog Lett. 1996;17:509–21.

    Article  Google Scholar 

  44. Sharma N, Ray AK, Sharma S, Shukla KK, Pradhan S, Aggarwal LMJ. Segmentation and classification of medical images using texture-primitive features: application of BAM-type artificial neural network. Med Phys. 2008;33:119–26.

    Article  Google Scholar 

  45. Ganeshan B, Goh V, Mandeville H, Ng QS, Hoskin P, Miles KA. CT of non-small cell lung cancer: Histopathological correlates for texture parameters. Radiology. 2012 (in press).

  46. Goh V, Ganeshan B, Nathan P, Juttla JK, Vinayan A, Miles KA. Assessment of response to tyrosine kinase inhibitors in metastatic renal cell cancer: CT texture as a predictive biomarker. Radiology. 2011;26:165–71.

    Article  Google Scholar 

  47. Ganeshan B, Skogen K, Pressney I, Coutroubis D, Miles K. Tumour heterogeneity in oesophageal cancer assessed by CT texture analysis: preliminary evidence of an association with tumour metabolism, stage, and survival. Clin Radiol. 2012;67:157–64.

    Article  PubMed  CAS  Google Scholar 

  48. Ganeshan B, Panayiotou E, Burnand K, Dizdarevic S, Miles K. Tumour heterogeneity in non-small cell lung carcinoma assessed by CT texture analysis: a potential marker of survival. Eur Radiol. 2012;22:796–802.

    Article  PubMed  Google Scholar 

  49. Kido S, Kuriyama K, Higashiyama M, Kasugai T, Kuroda C. Fractal analysis of internal and peripheral textures of small peripheral bronchogenic carcinomas in thin-section computed tomography: comparison of bronchioloalveolar cell carcinomas with non bronchioloalveolar cell carcinomas. J Comput Assist Tomogr. 2003;27:56–61.

    Article  PubMed  Google Scholar 

  50. Chen W, Giger ML, Li H, Bick U, Newstead GM. Volumetric texture analysis of breast lesions on contrast-enhanced magnetic resonance image. Magn Reson Med. 2007;58:562–71.

    Article  PubMed  Google Scholar 

  51. Woods BJ, Clymer BD, Kurc T, Heverhagen JT, Stevens R, Orsdemir A, et al. Malignant-lesion segmentation using 4D co-occurrence texture analysis applied to dynamic contrast-enhanced magnetic resonance breast image data. J Magn Reson Imaging. 2007;25:495–501.

    Article  PubMed  Google Scholar 

  52. Holli K, Lääperi AL, Harrison L, Luukkaala T, Toivonen T, Ryymin P, et al. Characterization of breast cancer types by texture analysis of magnetic resonance images. Acad Radiol. 2010;17:135–41.

    Article  PubMed  Google Scholar 

  53. Eliat PA, Olivié D, Saïkali S, Carsin B, Saint-Jalmes H, de Certaines JD. Can dynamic contrast-enhanced magnetic resonance imaging combined with texture analysis differentiate malignant glioneuronal tumors from other glioblastoma? Neurol Res Int. 2012;2012:1951–76.

    Google Scholar 

  54. Mayerhoefer ME, Schima W, Trattnig S, Pinker K, Berger-Kulemann V, Ba-Ssalamah A. Texture-based classification of focal liver lesions on MRI at 3.0 Tesla: a feasibility study in cysts and hemangiomas. J Magn Reson Imaging. 2010;32:352–9.

    Article  PubMed  Google Scholar 

  55. Lopes R, Ayache A, Makni N, Puech P, Villers A, Mordon S, et al. Prostate cancer characterization on MR images using fractal features. Med Phys. 2011;38:83–95.

    Article  PubMed  CAS  Google Scholar 

  56. Harrison LC, Luukkaala T, Pertovaara H, Saarinen TO, Heinonen TT, Jarvenpaa R, et al. Non-Hodgkin lymphoma response evaluation with MRI texture classification. J Exp Clin Cancer Res. 2009;28:87.

    Article  PubMed  Google Scholar 

  57. Alic L, van Vliet M, van Dijke CF, Eggermont AM, Veenland JF, Niessen WJ. Heterogeneity in DCE-MRI parametric maps: a biomarker for treatment response? Phys Med Biol. 2011;56:1601–16.

    Article  PubMed  CAS  Google Scholar 

  58. O’Connor JP, Rose CJ, Jackson A, Watson Y, Cheung S, Maders F, et al. DCE-MRI biomarkers of tumour heterogeneity predict CRC liver metastasis shrinkage following bevacizumab and FOLFOX-6. Br J Cancer. 2011;105:139–45.

    Article  PubMed  Google Scholar 

  59. Ganeshan B, Abaleke S, Young RC, Chatwin CR, Miles KA. Texture analysis of non-small cell lung cancer on unenhanced computed tomography: initial evidence for a relationship with tumour glucose metabolism and stage. Cancer Imaging. 2010;10:137–43.

    Article  PubMed  Google Scholar 

  60. Segal E, Sirlin CB, Ooi C, Adler AS, Gollub J, Chen X, et al. Decoding global gene expression programs in liver cancer by non-invasive imaging. Nat Biotechnol. 2007;25:675–80.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge support from the NIHR Biomedical Research Centre of Guys & St Thomas’ NHS Trust in partnership and Kings College London and King’s College London and UCL Comprehensive Cancer Imaging Centre funded by the CRUK and EPSRC in association with the MRC and DoH (England).

Conflicts of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gary J. R. Cook.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chicklore, S., Goh, V., Siddique, M. et al. Quantifying tumour heterogeneity in 18F-FDG PET/CT imaging by texture analysis. Eur J Nucl Med Mol Imaging 40, 133–140 (2013). https://doi.org/10.1007/s00259-012-2247-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00259-012-2247-0

Keywords

Navigation