Skip to main content
Erschienen in: Annals of Nuclear Medicine 12/2020

19.09.2020 | Original Article

Value of volumetric and textural analysis in predicting the treatment response in patients with locally advanced rectal cancer

verfasst von: Nazlı Pınar Karahan Şen, Ayşegül Aksu, Gamze Çapa Kaya

Erschienen in: Annals of Nuclear Medicine | Ausgabe 12/2020

Einloggen, um Zugang zu erhalten

Abstract

Objective

The aim of this study was to assess the value of baseline 18F-FDG PET/CT in predicting the response to neoadjuvant chemo-radiotherapy (NCRT) in patients with locally advanced rectal cancer (LARC) via the volumetric and texture data obtained from 18F-FDG PET/CT images.

Methods

 In total, 110 patients who had undergone NCRT after initial PET/CT and followed by surgical resection were included in this study. Patients were divided into two groups randomly as a train set (n: 88) and test set (n: 22). Pathological response using three-point tumor regression grade (TRG) and metastatic lymph nodes in PET/CT images were determined. TRG1 were accepted as responders and TRG2-3 as non-responders. Region of interest for the primary tumors was drawn and volumetric features (metabolic tumor volume (MTV) and total lesion glycolysis (TLG)) and texture features were calculated. In train set, the relationship between these features and TRG was investigated with Mann–Whitney U test. Receiver operating curve analysis was performed for features with p < 0.05. Correlation between features were evaluated with Spearman correlation test, features with correlation coefficient < 0.8 were evaluated with the logistic regression analysis for creating a model. The model obtained was tested with a test set that has not been used in modeling before.

Results

 In train set 32 (36.4%) patients were responders. The rate of visually detected metastatic lymph node at baseline PET/CT was higher in non-responders than responders (71.4% and 46.9%, respectively, p = 0.022). There was a statistically significant difference between TLG, MTV, SHAPE_compacity, NGLDMcoarseness, GLRLM_GLNU, GLRLM_RLNU, GLZLM_LZHGE and GLZLM_GLNU between responders and non-responders. MTV and NGLDMcoarseness demonstrated the most significance (p = 0.011). A multivariate logistic regression analysis that included MTV, coarseness, GLZLM_LZHGE and lymph node metastasis was performed. Multivariate analysis demonstrated MTV and lymph node metastasis were the most meaningful parameters. The model's AUC was calculated as 0.714 (p = 0.001,0.606–0.822, 95% CI). In test set, AUC was determined 0.838 (p = 0.008,0.671–1.000, 95% CI) in discriminating non-responders.

Conclusions

Although there were points where textural features were found to be significant, multivariate analysis revealed no diagnostic superiority over MTV in predicting treatment response. In this study, it was thought higher MTV value and metastatic lymph nodes in PET/CT images could be a predictor of low treatment response in patients with LARC.
Literatur
1.
Zurück zum Zitat Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRef Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRef
2.
Zurück zum Zitat Li Y, Wang J, Ma X, Tan L, Yan Y, Xue C, et al. A Review of neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Int J Biol Sci. 2016;128:1022–31.CrossRef Li Y, Wang J, Ma X, Tan L, Yan Y, Xue C, et al. A Review of neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Int J Biol Sci. 2016;128:1022–31.CrossRef
3.
Zurück zum Zitat McCoy MJ, Hemmings C, Hillery S, Penter C, Bulsara NK, Zeps N, et al. Neoadjuvant chemoradiotherapy for rectal cancer: how important is tumour regression? ANZ J Surg. 2017;87:E233–E239239.CrossRef McCoy MJ, Hemmings C, Hillery S, Penter C, Bulsara NK, Zeps N, et al. Neoadjuvant chemoradiotherapy for rectal cancer: how important is tumour regression? ANZ J Surg. 2017;87:E233–E239239.CrossRef
4.
Zurück zum Zitat Peng YF, Yu WD, Pan HD, Wang L, Li M, Yao YF, et al. Tumor regression grades: potential outcome predictor of locally advanced rectal adenocarcinoma after preoperative radiotherapy. World J Gastroenterol. 2015;21:1851–6.CrossRef Peng YF, Yu WD, Pan HD, Wang L, Li M, Yao YF, et al. Tumor regression grades: potential outcome predictor of locally advanced rectal adenocarcinoma after preoperative radiotherapy. World J Gastroenterol. 2015;21:1851–6.CrossRef
5.
Zurück zum Zitat Rybinski B, Yun K. Addressing intra-tumoral heterogeneity and therapy resistance. Oncotarget. 2016;7:72322–42.CrossRef Rybinski B, Yun K. Addressing intra-tumoral heterogeneity and therapy resistance. Oncotarget. 2016;7:72322–42.CrossRef
6.
Zurück zum Zitat Bang JI, Ha S, Kang SB, Lee KW, Lee HS, Kim JS, et al. Prediction of neoadjuvant radiation chemotherapy response and survival using pretreatment [(18)F]FDG PET/CT scans in locally advanced rectal cancer. Eur J Nucl Med Mol Imaging. 2016;43:422–31.CrossRef Bang JI, Ha S, Kang SB, Lee KW, Lee HS, Kim JS, et al. Prediction of neoadjuvant radiation chemotherapy response and survival using pretreatment [(18)F]FDG PET/CT scans in locally advanced rectal cancer. Eur J Nucl Med Mol Imaging. 2016;43:422–31.CrossRef
7.
Zurück zum Zitat Bundschuh RA, Dinges J, Neumann L, Seyfried M, Zsótér N, Papp L, et al. Textural parameters of tumor heterogeneity in 18F-FDG PET/CT for therapy response assessment and prognosis in patients with locally advanced rectal cancer. J Nucl Med. 2014;55:891–7.CrossRef Bundschuh RA, Dinges J, Neumann L, Seyfried M, Zsótér N, Papp L, et al. Textural parameters of tumor heterogeneity in 18F-FDG PET/CT for therapy response assessment and prognosis in patients with locally advanced rectal cancer. J Nucl Med. 2014;55:891–7.CrossRef
8.
Zurück zum Zitat Giannini V, Mazzetti S, Bertotto I, Chiarenza C, Cauda S, Delmastro E, et al. Predicting locally advanced rectal cancer response to neoadjuvant therapy with 18F-FDG PET and MRI radiomics features. Eur J Nucl Med Mol Imaging. 2019;46:878–88.CrossRef Giannini V, Mazzetti S, Bertotto I, Chiarenza C, Cauda S, Delmastro E, et al. Predicting locally advanced rectal cancer response to neoadjuvant therapy with 18F-FDG PET and MRI radiomics features. Eur J Nucl Med Mol Imaging. 2019;46:878–88.CrossRef
9.
Zurück zum Zitat Lovinfosse P, Polus M, Van Daele D, Martinive P, Daenen F, Hatt M, et al. FDG PET/CT radiomics for predicting the outcome of locally advanced rectal cancer. Eur J Nucl Med Mol Imaging. 2018;45:365–75.CrossRef Lovinfosse P, Polus M, Van Daele D, Martinive P, Daenen F, Hatt M, et al. FDG PET/CT radiomics for predicting the outcome of locally advanced rectal cancer. Eur J Nucl Med Mol Imaging. 2018;45:365–75.CrossRef
10.
Zurück zum Zitat Liu Z, Zhang XY, Shi YJ, Wang L, Zhu HT, Tang Z, et al. Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Clin Cancer Res. 2017;23:7253–62.CrossRef Liu Z, Zhang XY, Shi YJ, Wang L, Zhu HT, Tang Z, et al. Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Clin Cancer Res. 2017;23:7253–62.CrossRef
11.
Zurück zum Zitat Bedard PL, Hansen AR, Ratain MJ, Siu LL. Tumour heterogeneity in the clinic. Nature. 2013;501:355–64.CrossRef Bedard PL, Hansen AR, Ratain MJ, Siu LL. Tumour heterogeneity in the clinic. Nature. 2013;501:355–64.CrossRef
12.
Zurück zum Zitat Hess S, Hoilund-Carlsen PF. PET clinics, contribution of FDG to modern medicine, Part II. 1st ed. Philadelphia: Elsevier; 2015. Hess S, Hoilund-Carlsen PF. PET clinics, contribution of FDG to modern medicine, Part II. 1st ed. Philadelphia: Elsevier; 2015.
13.
Zurück zum Zitat Ramón Y, Cajal S, Sesé M, Capdevila C, Aasen T, De Mattos-Arruda L, Diaz-Cano SJ, et al. Clinical implications of intratumor heterogeneity: challenges and opportunities. J Mol Med. 2020;98:161–77.CrossRef Ramón Y, Cajal S, Sesé M, Capdevila C, Aasen T, De Mattos-Arruda L, Diaz-Cano SJ, et al. Clinical implications of intratumor heterogeneity: challenges and opportunities. J Mol Med. 2020;98:161–77.CrossRef
14.
Zurück zum Zitat Ha S, Park S, Bang J, Kim EK, Lee HY. Metabolic radiomics for pretreatment 18F-FDG PET/CT to characterize locally advanced breast cancer: histopathologic characteristics, response to neoadjuvant chemotherapy, and prognosis. Scientific. 2017;7:1556. Ha S, Park S, Bang J, Kim EK, Lee HY. Metabolic radiomics for pretreatment 18F-FDG PET/CT to characterize locally advanced breast cancer: histopathologic characteristics, response to neoadjuvant chemotherapy, and prognosis. Scientific. 2017;7:1556.
15.
Zurück zum Zitat 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;2:157–64.CrossRef 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;2:157–64.CrossRef
16.
Zurück zum Zitat Kim SJ, Pak K, Chang S. Determination of regional lymph node status using (18)F-FDG PET/CT parameters in oesophageal cancer patients: comparison of SUV, volumetric parameters and intratumoral heterogeneity. Br J Radiol. 2016;89:20150673.CrossRef Kim SJ, Pak K, Chang S. Determination of regional lymph node status using (18)F-FDG PET/CT parameters in oesophageal cancer patients: comparison of SUV, volumetric parameters and intratumoral heterogeneity. Br J Radiol. 2016;89:20150673.CrossRef
17.
Zurück zum Zitat Coroller TP, Agrawal V, Huynh E, Narayan V, Lee SW, Mak RH, et al. Radiomic-based pathological response prediction from primary tumors and lymph nodes in NSCLC. J Thorac Oncol. 2017;12:467–76.CrossRef Coroller TP, Agrawal V, Huynh E, Narayan V, Lee SW, Mak RH, et al. Radiomic-based pathological response prediction from primary tumors and lymph nodes in NSCLC. J Thorac Oncol. 2017;12:467–76.CrossRef
18.
Zurück zum Zitat Cozzi L, Dinapoli N, Fogliata A, Hsu WC, Reggiori G, Lobefalo F, et al. Radiomics based analysis to predict local control and survival in hepatocellular carcinoma patients treated with volumetric modulated arc therapy. BMC Cancer. 2017;17:829.CrossRef Cozzi L, Dinapoli N, Fogliata A, Hsu WC, Reggiori G, Lobefalo F, et al. Radiomics based analysis to predict local control and survival in hepatocellular carcinoma patients treated with volumetric modulated arc therapy. BMC Cancer. 2017;17:829.CrossRef
19.
Zurück zum Zitat Ryan R, Gibbons D, Hyland JM, Treanor D, White A, Mulcahy HE, et al. Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology. 2005;47:141–6.CrossRef Ryan R, Gibbons D, Hyland JM, Treanor D, White A, Mulcahy HE, et al. Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology. 2005;47:141–6.CrossRef
20.
Zurück zum Zitat Wheeler JM, Warren BF, Mortensen NJ, Ekanyaka N, Kulacoglu H, Jones AC, et al. Quantification of histologic regression of rectal cancer after irradiation: a proposal for a modified staging system. Dis Colon Rectum. 2002;45:1051–6.CrossRef Wheeler JM, Warren BF, Mortensen NJ, Ekanyaka N, Kulacoglu H, Jones AC, et al. Quantification of histologic regression of rectal cancer after irradiation: a proposal for a modified staging system. Dis Colon Rectum. 2002;45:1051–6.CrossRef
21.
Zurück zum Zitat Nioche C, Orlhac F, Boughdad S, Reuzé S, Goya-Outi J, Robert C, et al. LIFEx: a freeware for radiomic feature calculation in multimodality imaging to accelerate advances in the characterization of tumor heterogeneity. Cancer Res. 2018;78:4786–9.CrossRef Nioche C, Orlhac F, Boughdad S, Reuzé S, Goya-Outi J, Robert C, et al. LIFEx: a freeware for radiomic feature calculation in multimodality imaging to accelerate advances in the characterization of tumor heterogeneity. Cancer Res. 2018;78:4786–9.CrossRef
22.
Zurück zum Zitat Orlhac F, Thézé B, Soussan M, Boisgard R, Buvat I. Multiscale texture analysis: from 18F-FDG PET images to histologic images. J Nucl Med. 2016;57:1823–8.CrossRef Orlhac F, Thézé B, Soussan M, Boisgard R, Buvat I. Multiscale texture analysis: from 18F-FDG PET images to histologic images. J Nucl Med. 2016;57:1823–8.CrossRef
23.
Zurück zum Zitat Orlhac F, Soussan M, Chouahnia K, Martinod E, Buvat I. 18F-FDG PET derived textural indices reflect tissue-specific uptake pattern in non-small cell lung cancer. PLoS ONE. 2015;10:e0145063.CrossRef Orlhac F, Soussan M, Chouahnia K, Martinod E, Buvat I. 18F-FDG PET derived textural indices reflect tissue-specific uptake pattern in non-small cell lung cancer. PLoS ONE. 2015;10:e0145063.CrossRef
24.
Zurück zum Zitat Chan YH. Biostatistics 104: correlational analysis. Singap Med J. 2003;44:614–9. Chan YH. Biostatistics 104: correlational analysis. Singap Med J. 2003;44:614–9.
25.
Zurück zum Zitat Keam B, Lee SJ, Kim TM, Paeng JC, Lee SH, Kim DW, et al. Total lesion glycolysis in positron emission tomography can predict gefitinib outcomes in non–small-cell lung cancer with activating EGFR mutation. J Thorac Oncol. 2015;10:1189–94.CrossRef Keam B, Lee SJ, Kim TM, Paeng JC, Lee SH, Kim DW, et al. Total lesion glycolysis in positron emission tomography can predict gefitinib outcomes in non–small-cell lung cancer with activating EGFR mutation. J Thorac Oncol. 2015;10:1189–94.CrossRef
26.
Zurück zum Zitat Joye I, Deroose CM, Vandecaveye V, Haustermans K. The role of diffusion-weighted MRI and (18)F-FDG PET/CT in the prediction of pathologic complete response after radiochemotherapy for rectal cancer: a systematic review. Radiother Oncol. 2014;113:158–65.CrossRef Joye I, Deroose CM, Vandecaveye V, Haustermans K. The role of diffusion-weighted MRI and (18)F-FDG PET/CT in the prediction of pathologic complete response after radiochemotherapy for rectal cancer: a systematic review. Radiother Oncol. 2014;113:158–65.CrossRef
27.
Zurück zum Zitat Dos Anjos DA, Perez RO, Habr-Gama A, Sao Juliao GP, Vailati BB, Fernandez LM, et al. Semiquantitative volumetry by sequential PET/CT may improve prediction of complete response to neoadjuvant chemoradiation in patients with distal rectal cancer. Dis Colon Rectum. 2016;59:805–12.CrossRef Dos Anjos DA, Perez RO, Habr-Gama A, Sao Juliao GP, Vailati BB, Fernandez LM, et al. Semiquantitative volumetry by sequential PET/CT may improve prediction of complete response to neoadjuvant chemoradiation in patients with distal rectal cancer. Dis Colon Rectum. 2016;59:805–12.CrossRef
28.
Zurück zum Zitat Maffione AM, Ferretti A, Grassetto G, Bellan E, Capirci C, Chondrogiannis S, et al. Fifteen different 18F-FDG PET/CT qualitative and quantitative parameters investigated as pathological response predictors of locally advanced rectal cancer treated by neoadjuvant chemoradiation therapy. Eur J Nucl Med Mol Imaging. 2013;40:853–64.CrossRef Maffione AM, Ferretti A, Grassetto G, Bellan E, Capirci C, Chondrogiannis S, et al. Fifteen different 18F-FDG PET/CT qualitative and quantitative parameters investigated as pathological response predictors of locally advanced rectal cancer treated by neoadjuvant chemoradiation therapy. Eur J Nucl Med Mol Imaging. 2013;40:853–64.CrossRef
29.
Zurück zum Zitat Deantonio L, Caroli A, Puta E, Ferrante D, Apicella F, Turri L, et al. Does baseline [18F] FDG-PET/CT correlate with tumor staging, response after neoadjuvant chemoradiotherapy, and prognosis in patients with rectal cancer? Radiat Oncol. 2018;13:211.CrossRef Deantonio L, Caroli A, Puta E, Ferrante D, Apicella F, Turri L, et al. Does baseline [18F] FDG-PET/CT correlate with tumor staging, response after neoadjuvant chemoradiotherapy, and prognosis in patients with rectal cancer? Radiat Oncol. 2018;13:211.CrossRef
30.
Zurück zum Zitat Lee SJ, Kim JG, Lee SW, Chae YS, Kang BW, Lee YJ, et al. Clinical implications of initial FDG-PET/CT in locally advanced rectal cancer treated with neoadjuvant chemoradiotherapy. Cancer Chemother Pharmacol. 2013;71:1201–7.CrossRef Lee SJ, Kim JG, Lee SW, Chae YS, Kang BW, Lee YJ, et al. Clinical implications of initial FDG-PET/CT in locally advanced rectal cancer treated with neoadjuvant chemoradiotherapy. Cancer Chemother Pharmacol. 2013;71:1201–7.CrossRef
31.
Zurück zum Zitat Li QW, Zheng RL, Ling YH, Wang QX, Xiao WW, Zeng ZF, et al. Prediction of tumor response after neoadjuvant chemoradiotherapy in rectal cancer using (18)fluorine-2-deoxy-D-glucose positron emission tomography-computed tomography and serum carcinoembryonic antigen: a prospective study. Abdom Radiol. 2016;41:1448–555.CrossRef Li QW, Zheng RL, Ling YH, Wang QX, Xiao WW, Zeng ZF, et al. Prediction of tumor response after neoadjuvant chemoradiotherapy in rectal cancer using (18)fluorine-2-deoxy-D-glucose positron emission tomography-computed tomography and serum carcinoembryonic antigen: a prospective study. Abdom Radiol. 2016;41:1448–555.CrossRef
32.
Zurück zum Zitat Shu Z, Fang S, Ding Z, Mao D, Pang P. Gong X [Application value of texture analysis of magnetic resonance images in prediction of neoadjuvant chemoradiotherapy efficacy for rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi. 2018;21:1051–8.PubMed Shu Z, Fang S, Ding Z, Mao D, Pang P. Gong X [Application value of texture analysis of magnetic resonance images in prediction of neoadjuvant chemoradiotherapy efficacy for rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi. 2018;21:1051–8.PubMed
33.
Zurück zum Zitat Aker M, Ganeshan B, Afaq A, Wan S, Groves AM, Arulampalam T. Magnetic resonance texture analysis in identifying complete pathological response to neoadjuvant treatment in locally advanced rectal cancer. Dis Colon Rectum. 2019;62:163–70.CrossRef Aker M, Ganeshan B, Afaq A, Wan S, Groves AM, Arulampalam T. Magnetic resonance texture analysis in identifying complete pathological response to neoadjuvant treatment in locally advanced rectal cancer. Dis Colon Rectum. 2019;62:163–70.CrossRef
34.
Zurück zum Zitat Amadasun M, King R. Texural features corresponding to textural properties. IEEE Trans Syst Man Cybern. 1989;19:1264–74.CrossRef Amadasun M, King R. Texural features corresponding to textural properties. IEEE Trans Syst Man Cybern. 1989;19:1264–74.CrossRef
35.
Zurück zum Zitat Thibault G, Angulo J, Meyer F. Advanced statistical matrices for texture characterization: application to cell classification. IEEE Trans Biomed Eng. 2014;61:630–7.CrossRef Thibault G, Angulo J, Meyer F. Advanced statistical matrices for texture characterization: application to cell classification. IEEE Trans Biomed Eng. 2014;61:630–7.CrossRef
36.
Zurück zum Zitat Hatt M, Tixier F, Pierce L, Kinahan PE, Le Rest CC, Visvikis D. Characterization of PET/CT images using texture analysis: the past, the present any future? Eur J Nucl Med Mol Imaging. 2017;44:151–65.CrossRef Hatt M, Tixier F, Pierce L, Kinahan PE, Le Rest CC, Visvikis D. Characterization of PET/CT images using texture analysis: the past, the present any future? Eur J Nucl Med Mol Imaging. 2017;44:151–65.CrossRef
37.
Zurück zum Zitat Cook GJR, Azad G, Owczarczyk K, Siddique M, Goh V. Challenges and promises of PET radiomics. Int J Radiat Oncol Biol Phys. 2018;102:1083–9.CrossRef Cook GJR, Azad G, Owczarczyk K, Siddique M, Goh V. Challenges and promises of PET radiomics. Int J Radiat Oncol Biol Phys. 2018;102:1083–9.CrossRef
38.
Zurück zum Zitat Jiang Y, You K, Qiu X, Bi Z, Mo H, Li L, et al. Tumor volume predicts local recurrence in early rectal cancer treated with radical resection: a retrospective observational study of 270 patients. Int J Surg. 2018;49:68–73.CrossRef Jiang Y, You K, Qiu X, Bi Z, Mo H, Li L, et al. Tumor volume predicts local recurrence in early rectal cancer treated with radical resection: a retrospective observational study of 270 patients. Int J Surg. 2018;49:68–73.CrossRef
Metadaten
Titel
Value of volumetric and textural analysis in predicting the treatment response in patients with locally advanced rectal cancer
verfasst von
Nazlı Pınar Karahan Şen
Ayşegül Aksu
Gamze Çapa Kaya
Publikationsdatum
19.09.2020
Verlag
Springer Singapore
Erschienen in
Annals of Nuclear Medicine / Ausgabe 12/2020
Print ISSN: 0914-7187
Elektronische ISSN: 1864-6433
DOI
https://doi.org/10.1007/s12149-020-01527-x

Weitere Artikel der Ausgabe 12/2020

Annals of Nuclear Medicine 12/2020 Zur Ausgabe