Abstract
Background
Whether Intravoxel incoherent motion (IVIM) can be used as a predictive tool of positive surgical margins (PSMs) and Gleason score (GS) upgrading in prostate cancer (PCa) patients after radical prostatectomy (RP) still remains unclear. The aim of this study is to explore the ability of IVIM and clinical characteristics to predict PSMs and GS upgrading.
Methods
A total of 106 PCa patients after RP who underwent pelvic mpMRI (multiparametric Magnetic Resonance Imaging) between January 2016 and December 2021 and met the requirements were retrospectively included in our study. IVIM parameters were obtained using GE Functool post-processing software. Logistic regression models were fitted to confirm the predictive risk factor of PSMs and GS upgrading. The area under the curve and fourfold contingency table were used to evaluate the diagnostic efficacy of IVIM and clinical parameters.
Results
Multivariate logistic regression analyses revealed that percent of positive cores, apparent diffusion coefficient and molecular diffusion coefficient (D) were independent predictors of PSMs (Odds Ratio (OR) were 6.07, 3.62 and 3.16, respectively), Biopsy GS and pseudodiffusion coefficient (D*) were independent predictors of GS upgrading (OR were 0.563 and 7.15, respectively). The fourfold contingency table suggested that combined diagnosis increased the ability of predicting PSMs but had no advantage in predicting GS upgrading except the sensitivity from 57.14 to 91.43%.
Conclusions
IVIM showed good performance in predicting PSMs and GS upgrading. Combining IVIM and clinical factors enhanced the performance of predicting PSMs, which may contribute to clinical diagnosis and treatment.
Similar content being viewed by others
Data availability
The data generated and analyzed during this study cannot be made publicly available due to regulations at the institutional review board concerning the potential of disclosure of an individual’s personal health information. Please contact the corresponding author regarding access to anonymized data.
References
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249. https://doi.org/10.3322/caac.21660
Siegel RL, Miller KD, Fuchs HE, Jemal A (2021) Cancer statistics, 2021. CA Cancer J Clin 71(1):7–33. https://doi.org/10.3322/caac.21654. (Erratum. In: CA Cancer J Clin. 2021 Jul; 71(4):359)
Feng RM, Zong YN, Cao SM, Xu RH (2019) Current cancer situation in China: good or bad news from the 2018 global cancer statistics? Cancer Commun 39(1):22. https://doi.org/10.1186/s40880-019-0368-6
Zhang L, Zhao H, Wu B, Zha Z, Yuan J, Feng Y (2021) Predictive factors for positive surgical margins in patients with prostate cancer after radical prostatectomy: a systematic review and meta-analysis. Front Oncol 10:539592. https://doi.org/10.3389/fonc.2020.539592
Keller EX, Bachofner J, Britschgi AJ, Saba K, Mortezavi A, Kaufmann B, Fankhauser CD, Wild P, Sulser T, Hermanns T, Eberli D, Poyet C (2019) Prognostic value of unifocal and multifocal positive surgical margins in a large series of robot-assisted radical prostatectomy for prostate cancer. World J Urol 37(9):1837–1844. https://doi.org/10.1007/s00345-018-2578-y
Altok M, Troncoso P, Achim MF, Matin SF, Gonzalez GN, Davis JW (2019) Prostate cancer upgrading or downgrading of biopsy Gleason scores at radical prostatectomy: prediction of “regression to the mean” using routine clinical features with correlating biochemical relapse rates. Asian J Androl 21(6):598–604. https://doi.org/10.4103/aja.aja_29_19
John A, O’Callaghan M, Catterwell R, Selth L (2020) Does Gleason score of positive surgical margin after radical prostatectomy affect biochemical recurrence and oncological outcomes? Protocol for systematic review. BMJ Open 10(3):e034612
Koskas Y, Lannes F, Branger N, Giusiano S, Guibert N, Pignot G, Walz J, Rossi D, Bastide C (2019) Extent of positive surgical margins following radical prostatectomy: impact on biochemical recurrence with long-term follow-up. BMC Urol 19(1):37. https://doi.org/10.1186/s12894-019-0470-8
Jeong H, Choo MS, Cho MC, Son H, Yoo S (2022) Prediction of surgical margin status and location after radical prostatectomy using positive biopsy sites on 12-core standard prostate biopsy. Sci Rep 12(1):4066. https://doi.org/10.1038/s41598-022-08022-5
Wang X, Zhang Y, Ji Z, Yang P, Tian Y (2021) Old men with prostate cancer have higher risk of Gleason score upgrading and pathological upstaging after initial diagnosis: a systematic review and meta-analysis. World J Surg Oncol 19(1):18. https://doi.org/10.1186/s12957-021-02127-3
Tennill TA, Gross ME, Frieboes HB (2017) Automated analysis of co-localized protein expression in histologic sections of prostate cancer. PLoS ONE 12(5):e0178362. https://doi.org/10.1371/journal.pone.0178362
Xu N, Wu YP, Li XD, Lin MY, Zheng QS, Chen SH, Li JF, Wei Y, Xue XY (2018) Risk of upgrading from prostate biopsy to radical prostatectomy pathology: is magnetic resonance imaging-guided biopsy more accurate? J Cancer 9(19):3634–3639. https://doi.org/10.7150/jca.26791
Pham DM, Kim JK, Lee S, Hong SK, Byun SS, Lee SE (2020) Prediction of pathologic upgrading in Gleason score 3+4 prostate cancer: who is a candidate for active surveillance? Investig Clin Urol 61(4):405–410. https://doi.org/10.4111/icu.2020.61.4.405
Yang DD, Mahal BA, Muralidhar V, Nezolosky MD, Vastola ME, Labe SA, Boldbaatar N, King MT, Martin NE, Orio PF 3rd, Beard CJ, Hoffman KE, Trinh QD, Spratt DE, Feng FY, Nguyen PL (2019) Risk of upgrading and upstaging among 10 000 patients with Gleason 3+4 favorable intermediate-risk prostate cancer. Eur Urol Focus 5(1):69–76. https://doi.org/10.1016/j.euf.2017.05.011
Alqahtani S, Wei C, Zhang Y, Szewczyk-Bieda M, Wilson J, Huang Z, Nabi G (2020) Prediction of prostate cancer Gleason score upgrading from biopsy to radical prostatectomy using pre-biopsy multiparametric MRI PIRADS scoring system. Sci Rep 10(1):7722. https://doi.org/10.1038/s41598-020-64693-y
Qin XP, Lu QJ, Yang CH, Wang J, Chen JF, Liu K, Chen X, Zhou J, Pan YH, Li YH, Ren SC, Liu JM, Liu WP, Qian HJ, Yi XL, Lai CY, Qu LJ, Gao X, Xu YS, Chen Z, Zhuo YM (2022) CRMP4 CpG hypermethylation predicts upgrading to Gleason Score ≥ 8 in prostate cancer. Front Oncol 12:840950. https://doi.org/10.3389/fonc.2022.840950
Ghafoor S, Burger IA, Vargas AH (2019) Multimodality imaging of prostate cancer. J Nucl Med 60(10):1350–1358. https://doi.org/10.2967/jnumed.119.228320
Lee CC, Chang KH, Chiu FM, Ou YC, Hwang JI, Hsueh KC, Fan HC (2021) Using IVIM parameters to differentiate prostate cancer and contralateral normal tissue through fusion of MRI images with whole-mount pathology specimen images by control point registration method. Diagnostics 11(12):2340. https://doi.org/10.3390/diagnostics11122340
Iima M (2021) Perfusion-driven intravoxel incoherent motion (IVIM) MRI in oncology: applications, challenges, and future trends. Magn Reson Med Sci 20(2):125–138. https://doi.org/10.2463/mrms.rev.2019-0124
Patel P, Wang S, Siddiqui MM (2019) The use of multiparametric magnetic resonance imaging (mpMRI) in the detection, evaluation, and surveillance of clinically significant prostate cancer (csPCa). Curr Urol Rep 20(10):60. https://doi.org/10.1007/s11934-019-0926-0
Weinreb JC, Barentsz JO, Choyke PL, Cornud F, Haider MA, Macura KJ, Margolis D, Schnall MD, Shtern F, Tempany CM, Thoeny HC, Verma S (2016) PI-RADS prostate imaging—reporting and data system: 2015, Version 2. Eur Urol 69(1):16–40. https://doi.org/10.1016/j.eururo.2015.08.052
van der Kwast TH, Amin MB, Billis A, Epstein JI, Griffiths D, Humphrey PA, Montironi R, Wheeler TM, Srigley JR, Egevad L, Delahunt B (2011) ISUP Prostate cancer group. International society of urological pathology (ISUP) consensus conference on handling and staging of radical prostatectomy specimens. Working group 2 T2 substaging and prostate cancer volume. Mod Pathol. 24(1): 16–25. https://doi.org/10.1038/modpathol.2010.156
Le Bihan D (2013) Apparent diffusion coefficient and beyond: what diffusion MR imaging can tell us about tissue structure. Radiology 268(2):318–322. https://doi.org/10.1148/radiol.13130420
Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168(2):497–505. https://doi.org/10.1148/radiology.168.2.3393671
Zhang B, Zhou J, Wu S, Guo M, Zhang Y, Liu R (2020) The impact of surgical margin status on prostate cancer-specific mortality after radical prostatectomy: a systematic review and meta-analysis. Clin Transl Oncol 22(11):2087–2096. https://doi.org/10.1007/s12094-020-02358-y
Celik S, Eker A, Bozkurt İH, Bolat D, Basmacı İ, Şefik E, Değirmenci T, Günlüsoy B (2020) Factors affecting biochemical recurrence of prostate cancer after radical prostatectomy in patients with positive and negative surgical margin. Prostate Int 8(4):178–184. https://doi.org/10.1016/j.prnil.2020.08.003
Bakavičius A, Drevinskaitė M, Daniūnaitė K, Barisienė M, Jarmalaitė S, Jankevičius F (2020) The impact of prostate cancer upgrading and upstaging on biochemical recurrence and cancer-specific survival. Medicina 56(2):61. https://doi.org/10.3390/medicina56020061
Asimakopoulos AD, Annino F, Mugnier C, Lopez L, Hoepffner JL, Gaston R, Piechaud T (2021) Robotic radical prostatectomy: analysis of midterm pathologic and oncologic outcomes: a historical series from a high-volume center. Surg Endosc 35(12):6731–6745. https://doi.org/10.1007/s00464-020-08177-0
Turan T, Güçlüer B, Efiloğlu Ö, Şendoğan F, Atış RG, Çaşkurlu T, Yıldırım A (2019) The factors predicting upgrading of prostate cancer by using international society for urological pathology (ISUP) 2014 Gleason grading system. Turk J Urol 45(Supp. 1):S36–S41. https://doi.org/10.5152/tud.2018.57946
Alessi S, Maggioni R, Luzzago S, Colombo A, Pricolo P, Summers PE, Saia G, Manzoni M, Renne G, Marvaso G, De Cobelli O, Bellomi M, Jereczek-Fossa BA, Petralia G (2021) Apparent diffusion coefficient and other preoperative magnetic resonance imaging features for the prediction of positive surgical margins in prostate cancer patients undergoing radical prostatectomy. Clin Genitourin Cancer 19(6):e335–e345. https://doi.org/10.1016/j.clgc.2021.04.004
Park SY, Oh YT, Jung DC, Cho NH, Choi YD, Rha KH, Hong SJ (2017) Diffusion-weighted imaging predicts upgrading of Gleason score in biopsy-proven low grade prostate cancers. BJU Int 119(1):57–66. https://doi.org/10.1111/bju.13436
Minh Duc N (2021) The diagnostic function of intravoxel incoherent motion for distinguishing between pilocytic astrocytoma and ependymoma. PLoS ONE 16(3):e0247899. https://doi.org/10.1371/journal.pone.0247899
Preisser F, Mazzone E, Knipper S, Nazzani S, Bandini M, Shariat SF, Tian Z, Saad F, Montorsi F, Zorn KC, Graefen M, Tilki D, Karakiewicz PI (2019) Rates of positive surgical margins and their effect on cancer-specific mortality at radical prostatectomy for patients with clinically localized prostate cancer. Clin Genitourin Cancer 17(1):e130–e139. https://doi.org/10.1016/j.clgc.2018.09.024
Bianchi L, Schiavina R, Borghesi M, Casablanca C, Chessa F, Mineo Bianchi F, Pultrone C, Vagnoni V, Ercolino A, Dababneh H, Fiorentino M, Brunocilla E (2020) Patterns of positive surgical margins after open radical prostatectomy and their association with clinical recurrence. Minerva Urol Nefrol 72(4):464–473
Choi SY, Chi BH, Kim TH, Lim B, Lee W, You D, Kim CS (2021) Does intraoperative frozen section really predict significant positive surgical margins after robot-assisted laparoscopic prostatectomy? A retrospective study. Asian J Androl 23(1):74–79. https://doi.org/10.4103/aja.aja_16_20
Wang S, Du P, Cao Y, Yang X, Yang Y (2021) Tumor biological feature and its association with positive surgical margins and apical margins after radical prostatectomy in non-metastasis prostate cancer. Curr Oncol 28(2):1528–1536. https://doi.org/10.3390/curroncol28020144
Sayyid RK, Wilson B, Benton JZ, Lodh A, Thomas EF, Goldberg H, Madi R, Terris MK, Wallis CJD, Klaassen Z (2021) Upgrading on radical prostatectomy specimens of very low- and low-risk prostate cancer patients on active surveillance: a population-level analysis. Can Urol Assoc J 15(7):E335–E339. https://doi.org/10.5489/cuaj.6868
Qu W, Yu S, Tao J, Dong B, Fan Y, Du H, Deng H, Liu J, Zhang X (2021) Evaluating incidence, location, and predictors of positive surgical margin among Chinese men undergoing robot-assisted radical prostatectomy. Cancer Control 28:10732748211055264. https://doi.org/10.1177/10732748211055265
Tosco L, De Coster G, Roumeguère T, Everaerts W, Quackels T, Dekuyper P, Van Cleynenbreugel B, Van Damme N, Van Eycken E, Ameye F, Joniau S (2018) Development and external validation of nomograms to predict adverse pathological characteristics after robotic prostatectomy: results of a prospective, multi-institutional nationwide series. Eur Urol Oncol 1(4):338–345. https://doi.org/10.1016/j.euo.2018.04.008
Shida Y, Hakariya T, Mitsunari K, Matsuo T, Ohba K, Miyata Y, Sakai H (2022) Preoperative predictors of lymph node invasion and biochemical recurrence in high-risk prostate cancer. Cancer Diagn Progn 2(1):49–54
Hompland T, Hole KH, Ragnum HB, Aarnes EK, Vlatkovic L, Lie AK, Patzke S, Brennhovd B, Seierstad T, Lyng H (2018) Combined mr imaging of oxygen consumption and supply reveals tumor hypoxia and aggressiveness in prostate cancer patients. Cancer Res 78(16):4774–4785. https://doi.org/10.1158/0008-5472.CAN-17-3806
Liu Y, Wang X, Cui Y, Jiang Y, Yu L, Liu M, Zhang W, Shi K, Zhang J, Zhang C, Li C, Chen M (2020) Comparative study of monoexponential, intravoxel incoherent motion, kurtosis, and IVIM-kurtosis models for the diagnosis and aggressiveness assessment of prostate cancer. Front Oncol 11(10):1763. https://doi.org/10.3389/fonc.2020.01763
Le Bihan D (2019) What can we see with IVIM MRI? Neuroimage 15(187):56–67. https://doi.org/10.1016/j.neuroimage.2017.12.062
Lai WS, Gordetsky JB, Thomas JV, Nix JW, Rais-Bahrami S (2017) Factors predicting prostate cancer upgrading on magnetic resonance imaging-targeted biopsy in an active surveillance population. Cancer 123(11):1941–1948. https://doi.org/10.1002/cncr.30548
Oh JJ, Ahn H, Hwang SI, Lee HJ, Choe G, Lee S, Lee H, Byun SS, Hong SK (2021) Favorable intermediate risk prostate cancer with biopsy Gleason score of 6. BMC Urol 21(1):52. https://doi.org/10.1186/s12894-021-00827-2
Chung DY, Kim MS, Lee JS, Goh HJ, Koh DH, Jang WS, Hong CH, Choi YD (2019) Clinical significance of multiparametric magnetic resonance imaging as a preoperative predictor of oncologic outcome in very low-risk prostate cancer. J Clin Med 8(4):542. https://doi.org/10.3390/jcm8040542
Liu H, Tang K, Peng E, Wang L, Xia D, Chen Z (2020) Predicting prostate cancer upgrading of biopsy gleason grade group at radical prostatectomy using machine learning-assisted decision-support models. Cancer Manag Res 22(12):13099–13110. https://doi.org/10.2147/CMAR.S286167
Bours MJ (2021) Bayes’ rule in diagnosis. J Clin Epidemiol 131:158–160. https://doi.org/10.1016/j.jclinepi.2020.12.021
Funding
None.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of the manuscript entitled.
Human rights
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
The study was approved by the local ethics committee. Verbal informed consent was obtained from each patient before study enrollment.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Meng, S., Gan, W., Chen, L. et al. Intravoxel incoherent motion predicts positive surgical margins and Gleason score upgrading after radical prostatectomy for prostate cancer. Radiol med 128, 668–678 (2023). https://doi.org/10.1007/s11547-023-01645-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11547-023-01645-2