Discriminating Malignant from Benign Testicular Masses Using Multiparametric Magnetic Resonance Imaging—A Prospective Single-Center Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Image Acquisition
2.3. Image Analysis
2.4. Statistics
3. Results
3.1. Epidemiology and Distribution of Histopathology
3.2. Results of MRI
3.2.1. Tumor Signaling in Relation to Contrast Agent
3.2.2. Diffusion Restriction
3.2.3. Morphological Characteristics of the Tumors
3.2.4. Dignity Dichotomy and Number Needed to Harm (NNH)
3.2.5. Correlation of Clinical Factors with Tumor Dignity
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
AFP | alpha-fetoprotein |
BF | Blood flow |
BMI | Body mass index |
DWI | Diffusion-weighted imaging |
EAU | European Association of Urology |
FSH | Follicle-stimulation hormone |
GCN(IS) | Germ cell neoplasia (in situ) |
HPLAP | Human placental alkaline phosphatase |
LCT | Leydig cell tumor |
LDH | Lactate dehydrogenase |
LH | Luteinizing hormone |
MRI | Magnetic resonance imaging |
NPV | Negative predictive value |
ns | Not significant |
NSGCT | Non-seminomatous germ cell tumor |
PPV | Positive predictive value |
TIN | Testicular intraepithelial neoplasia |
US | Ultrasound |
βhCG | Human chorionic gonadotropin |
WHO | World Health Organization |
References
- Bylund, K.C. Testicular Cancer. In Reference Module in Biomedical Sciences; Elsevier: Amsterdam, The Netherlands, 2015. [Google Scholar]
- EAU Guidelines; Edn. Presented at the EAU Annual Congress Milan 2023; EAU Guidelines Office: Arnhem, The Netherlands, 2023; ISBN 978-94-92671-19-6. Available online: https://uroweb.org/eau-guidelines/citing-usage-republication (accessed on 10 June 2024).
- Albers, P.; Albrecht, W.; Algaba, F.; Bokemeyer, C.; Cohn-Cedermark, G.; Fizazi, K.; Horwich, A.; Laguna, M.P.; Nicolai, N.; Oldenburg, J.; et al. Guidelines on Testicular Cancer: 2015 Update. Eur. Urol. 2015, 68, 1054–1068. [Google Scholar] [CrossRef] [PubMed]
- Nigam, M.; Aschebrook-Kilfoy, B.; Shikanov, S.; Eggener, S. Increasing incidence of testicular cancer in the United States and Europe between 1992 and 2009. World J. Urol. 2015, 33, 623–631. [Google Scholar] [CrossRef] [PubMed]
- Park, J.S.; Kim, J.; Elghiaty, A.; Ham, W.S. Recent global trends in testicular cancer incidence and mortality. Medicine 2018, 97, e12390. [Google Scholar] [CrossRef] [PubMed]
- Huang, J.; Chan, S.C.; Tin, M.S.; Liu, X.; Lok, V.T.; Ngai, C.H.; Zhang, L.; Lucero-Prisno, D.E., 3rd; Xu, W.; Zheng, Z.J.; et al. Worldwide Distribution, Risk Factors, and Temporal Trends of Testicular Cancer Incidence and Mortality: A Global Analysis. Eur. Urol. Oncol. 2022, 5, 566–576. [Google Scholar] [CrossRef] [PubMed]
- Yazici, S.; Del Biondo, D.; Napodano, G.; Grillo, M.; Calace, F.P.; Prezioso, D.; Crocetto, F.; Barone, B. Risk Factors for Testicular Cancer: Environment, Genes and Infections-Is It All? Medicina 2023, 59, 724. [Google Scholar] [CrossRef] [PubMed]
- Carmignani, L.; Gadda, F.; Gazzano, G.; Nerva, F.; Mancini, M.; Ferruti, M.; Bulfamante, G.; Bosari, S.; Coggi, G.; Rocco, F.; et al. High incidence of benign testicular neoplasms diagnosed by ultrasound. J. Urol. 2003, 170, 1783–1786. [Google Scholar] [CrossRef] [PubMed]
- Gurney, J.; Shaw, C.; Stanley, J.; Signal, V.; Sarfati, D. Cannabis exposure and risk of testicular cancer: A systematic review and meta-analysis. BMC Cancer 2015, 15, 897. [Google Scholar] [CrossRef]
- Rocher, L.; Ramchandani, P.; Belfield, J.; Bertolotto, M.; Derchi, L.E.; Correas, J.M.; Oyen, R.; Tsili, A.C.; Turgut, A.T.; Dogra, V.; et al. Incidentally detected non-palpable testicular tumours in adults at scrotal ultrasound: Impact of radiological findings on management Radiologic review and recommendations of the ESUR scrotal imaging subcommittee. Eur. Radiol. 2016, 26, 2268–2278. [Google Scholar] [CrossRef] [PubMed]
- Kim, W.; Rosen, M.A.; Langer, J.E.; Banner, M.P.; Siegelman, E.S.; Ramchandani, P. US MR imaging correlation in pathologic conditions of the scrotum. Radiographics 2007, 27, 1239–1253. [Google Scholar] [CrossRef]
- Stonier, T.; Simson, N.; Challacombe, B. Diagnosing testicular lumps in primary care. Practitioner 2017, 261, 13–17. [Google Scholar]
- Guthrie, J.A.; Fowler, R.C. Ultrasound diagnosis of testicular tumours presenting as epididymal disease. Clin. Radiol. 1992, 46, 397–400. [Google Scholar] [CrossRef]
- Isidori, A.M.; Pozza, C.; Gianfrilli, D.; Giannetta, E.; Lemma, A.; Pofi, R.; Barbagallo, F.; Manganaro, L.; Martino, G.; Lombardo, F.; et al. Differential diagnosis of nonpalpable testicular lesions: Qualitative and quantitative contrast-enhanced US of benign and malignant testicular tumors. Radiology 2014, 273, 606–618. [Google Scholar] [CrossRef] [PubMed]
- Reginelli, A.; D’Andrea, A.; Clemente, A.; Izzo, A.; Urraro, F.; Scala, F.; Nardone, V.; Guida, C.; Scialpi, M.; Cappabianca, S. Does multiparametric US improve diagnostic accuracy in the characterization of small testicular masses? Gland. Surg. 2019, 8 (Suppl. S3), S136–S141. [Google Scholar] [CrossRef] [PubMed]
- Tufano, A.; Rosati, D.; Moriconi, M.; Santarelli, V.; Canale, V.; Salciccia, S.; Sciarra, A.; Franco, G.; Cantisani, V.; Di Pierro, G.B. Diagnostic Accuracy of Contrast-Enhanced Ultrasound (CEUS) in the Detection of Muscle-Invasive Bladder Cancer: A Systematic Review and Diagnostic Meta-Analysis. Curr. Oncol. 2024, 31, 818–827. [Google Scholar] [CrossRef] [PubMed]
- Schwen, Z.R.; Liu, J.L.; Gabrielson, A.T.; Patel, H.D.; Gupta, M.; Rowe, S.P.; Herati, A.S.; Pierorazio, P.M. Testicular ultrasound underestimates the size of small testicular masses: A radiologic-pathologic correlation study. World J. Urol. 2021, 39, 3399–3405. [Google Scholar] [CrossRef] [PubMed]
- Cassidy, F.H.; Ishioka, K.M.; McMahon, C.J.; Chu, P.; Sakamoto, K.; Lee, K.S.; Aganovic, L. MR imaging of scrotal tumors and pseudotumors. Radiographics 2010, 30, 665–683. [Google Scholar] [CrossRef] [PubMed]
- Manganaro, L.; Vinci, V.; Pozza, C.; Saldari, M.; Gianfrilli, D.; Pofi, R.; Bernardo, S.; Cantisani, V.; Lenzi, A.; Scialpi, M.; et al. A prospective study on contrast-enhanced magnetic resonance imaging of testicular lesions: Distinctive features of Leydig cell tumours. Eur. Radiol. 2015, 25, 3586–3595. [Google Scholar] [CrossRef] [PubMed]
- Tsili, A.C.; Sofikitis, N.; Stiliara, E.; Argyropoulou, M.I. MRI of testicular malignancies. Abdom. Radiol. 2019, 44, 1070–1082. [Google Scholar] [CrossRef] [PubMed]
- Deininger, S.; Lusuardi, L.; Pallauf, M.; Hecht, S.; Forstner, R.; Meissnitzer, M.; Distler, F.A.; Erne, E.; Graf, S.; Lenart, S.; et al. The Diagnostic Value of the Added MR Imaging of the Scrotum in the Preoperative Workup of Sonographically Indeterminate Testicular Lesions-A Retrospective Multicenter Analysis. Cancers 2022, 14, 3594. [Google Scholar] [CrossRef]
- Tsili, A.C.; Bertolotto, M.; Turgut, A.T.; Dogra, V.; Freeman, S.; Rocher, L.; Belfield, J.; Studniarek, M.; Ntorkou, A.; Derchi, L.E.; et al. MRI of the scrotum: Recommendations of the ESUR Scrotal and Penile Imaging Working Group. Eur. Radiol. 2018, 28, 31–43. [Google Scholar] [CrossRef]
- Tsili, A.C.; Argyropoulou, M.I.; Dolciami, M.; Ercolani, G.; Catalano, C.; Manganaro, L. When to ask for an MRI of the scrotum. Andrology 2021, 9, 1395–1409. [Google Scholar] [CrossRef] [PubMed]
- Berney, D.M.; Cree, I.; Rao, V.; Moch, H.; Srigley, J.R.; Tsuzuki, T.; Amin, M.B.; Comperat, E.M.; Hartmann, A.; Menon, S.; et al. An introduction to the WHO 5th edition 2022 classification of testicular tumours. Histopathology 2022, 81, 459–466. [Google Scholar] [CrossRef] [PubMed]
- Tsili, A.C.; Argyropoulou, M.I.; Giannakis, D.; Sofikitis, N.; Tsampoulas, K. MRI in the characterization and local staging of testicular neoplasms. Am. J. Roentgenol. 2010, 194, 682–689. [Google Scholar] [CrossRef] [PubMed]
- El Sanharawi, I.; Correas, J.M.; Glas, L.; Ferlicot, S.; Izard, V.; Ducot, B.; Bellin, M.F.; Benoit, G.; Rocher, L. Non-palpable incidentally found testicular tumors: Differentiation between benign, malignant, and burned-out tumors using dynamic contrast-enhanced MRI. Eur. J. Radiol. 2016, 85, 2072–2082. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Sun, Z.; Chen, Y.; Zhao, F.; Yu, H.; Guo, X.; Shi, K. Testicular tumors: Discriminative value of conventional MRI and diffusion weighted imaging. Medicine 2021, 100, e27799. [Google Scholar] [CrossRef] [PubMed]
- Algebally, A.M.; Tantawy, H.I.; Yousef, R.R.H. Value of diffusion weighted magnetic resonance imaging in diagnosis and characterization of scrotal abnormalities. Egypt. J. Radiol. Nucl. Med. 2014, 45, 949–958. [Google Scholar] [CrossRef]
- Manganaro, L.; Saldari, M.; Pozza, C.; Vinci, V.; Gianfrilli, D.; Greco, E.; Franco, G.; Sergi, M.E.; Scialpi, M.; Catalano, C.; et al. Dynamic contrast-enhanced and diffusion-weighted MR imaging in the characterisation of small, non-palpable solid testicular tumours. Eur. Radiol. 2018, 28, 554–564. [Google Scholar] [CrossRef] [PubMed]
- Tsili, A.C.; Ntorkou, A.; Astrakas, L.; Boukali, E.; Giannakis, D.; Maliakas, V.; Sofikitis, N.; Argyropoulou, M.I. Magnetic resonance diffusion tensor imaging of the testis: Preliminary observations. Eur. J. Radiol. 2017, 95, 265–270. [Google Scholar] [CrossRef] [PubMed]
- Sonmez, G.; Sivrioglu, A.K.; Saglam, M. Optimized imaging techniques for testicular masses: Fast and with high accuracy. Wien. Klin. Wochenschr. 2012, 124, 704–708. [Google Scholar] [CrossRef]
- Patel, H.D.; Ramos, M.; Gupta, M.; Cheaib, J.G.; Sharma, R.; Zhang, A.; Bass, E.B.; Pierorazio, P.M. Magnetic Resonance Imaging to Differentiate the Histology of Testicular Masses: A Systematic Review of Studies with Pathologic Confirmation. Urology 2020, 135, 4–10. [Google Scholar] [CrossRef]
- Tsili, A.C.; Argyropoulou, M.I.; Giannakis, D.; Tsampalas, S.; Sofikitis, N.; Tsampoulas, K. Diffusion-weighted MR imaging of normal and abnormal scrotum: Preliminary results. Asian J. Androl. 2012, 14, 649–654. [Google Scholar] [CrossRef] [PubMed]
- Kreydin, E.I.; Barrisford, G.W.; Preston, M.A. Testicular Cancer: What the Radiologist Needs to Know. Am. J. Roentgenol. 2013, 200, 1215–1225. [Google Scholar] [CrossRef] [PubMed]
- Mohrs, O.K.; Thoms, H.; Egner, T.; Hallscheidt, P. MRI of Patients with Suspected Scrotal or Testicular Lesions: Diagnostic Value in Daily Practice. Am. J. Roentgenol. 2012, 199, 609–615. [Google Scholar] [CrossRef]
- Katabathina, V.S.; Vargas-Zapata, D.; Prasad, S.R. Testicular Germ Cell Tumors: Classification, Pathologic Features, Imaging Findings, and Management. RadioGraphics 2021, 41, 1698–1716. [Google Scholar] [CrossRef]
- Gerber, D.; Wright, H.C.; Sussman, R.D.; Stamatakis, L. Embryonal carcinoma presenting as a calcified solitary testicular mass on ultrasound. BMJ Case Rep. 2017, 2017, bcr-2017. [Google Scholar] [CrossRef]
- Akdemir, F.; Aldemir, M.; Orhun, H.S. Intratesticular calcified nodule. Turk. J. Urol. 2017, 43, 563–565. [Google Scholar] [CrossRef] [PubMed]
- Tsili, A.C.; Sofikitis, N.; Pappa, O.; Bougia, C.K.; Argyropoulou, M.I. An Overview of the Role of Multiparametric MRI in the Investigation of Testicular Tumors. Cancers 2022, 14, 3912. [Google Scholar] [CrossRef] [PubMed]
- Henriques, D.; Mota Pinto, A.; Donato, H.; Leao, R. Prevalence and Management of Incidental Testicular Masses-A Systematic Review. J. Clin. Med. 2022, 11, 5770. [Google Scholar] [CrossRef] [PubMed]
- Shilo, Y.; Zisman, A.; Lindner, A.; Raz, O.; Strauss, S.; Siegel, Y.I.; Segal, M.; Sandbank, J.; Leibovici, D. The predominance of benign histology in small testicular masses. Urol. Oncol. 2012, 30, 719–722. [Google Scholar] [CrossRef] [PubMed]
- Richie, J.P. Detection and treatment of testicular cancer. CA Cancer J. Clin. 1993, 43, 151–175. [Google Scholar] [CrossRef]
- Dieckmann, K.P.; Richter-Simonsen, H.; Kulejewski, M.; Ikogho, R.; Zecha, H.; Anheuser, P.; Pichlmeier, U.; Isbarn, H. Testicular Germ-Cell Tumours: A Descriptive Analysis of Clinical Characteristics at First Presentation. Urol. Int. 2018, 100, 409–419. [Google Scholar] [CrossRef] [PubMed]
- Abboudi, H.; Malde, S.; Mchaourab, A.; Eddy, B.; Shrotri, N. Nonpalpable Testicular Masses—Should We Be Worried? Open J. Urol. 2013, 3, 281–286. [Google Scholar] [CrossRef]
- Bieniek, J.M.; Juvet, T.; Margolis, M.; Grober, E.D.; Lo, K.C.; Jarvi, K.A. Prevalence and Management of Incidental Small Testicular Masses Discovered on Ultrasonographic Evaluation of Male Infertility. J. Urol. 2018, 199, 481–486. [Google Scholar] [CrossRef] [PubMed]
- Aberger, M.; Wilson, B.; Holzbeierlein, J.M.; Griebling, T.L.; Nangia, A.K. Testicular self-examination and testicular cancer: A cost-utility analysis. Cancer Med. 2014, 3, 1629–1634. [Google Scholar] [CrossRef] [PubMed]
- MRI Costs: What You’ll Pay with and without Insurance. Available online: https://www.singlecare.com/blog/mri-cost/ (accessed on 10 June 2024).
- Accessible MRI. Available online: https://onlinelibrary.wiley.com/doi/toc/10.1002/(ISSN)1522-2594.Accessible-MRI (accessed on 10 June 2024).
- Market Size & Trends. Available online: https://www.grandviewresearch.com/industry-analysis/magnetic-resonance-imaging-market (accessed on 10 June 2024).
Benign | Malignant | p-Value | ||
---|---|---|---|---|
Type of contrast enhancement (compare [20]) | n absence of enhancement/Type 0 curve (%) | 3 (25.0) | 1 (2.9) | p = 0.025 * |
n Type I curve (%) | 2 (16.7) | 10 (28.6) | ||
n Type II curve (%) | 2 (16.7) | 17 (48.6) | ||
n Type III curve (%) | 5 (41.7) | 7 (20.0) | ||
Pattern of contrast enhancement | n homogenous (%) | 6 (66.7) | 5 (14.3) | p = 0.005 ** |
n heterogenous (%) | 2 (22.2) | 22 (62.9) | ||
n rim-like (%) | 1 (11.1) | 8 (22.9) |
Benign | Malignant | p-Value | ||
---|---|---|---|---|
T1 signal | n predominantly low (%) | 2 (16.7) | 3 (8.6) | 0.387 1 |
n isointense (%) | 10 (83.3) | 30 (85.7) | ||
n predominantly high (%) | 0 (0) | 2 (5.7) | ||
T2 signal | n predominantly low (%) | 6 (50.0) | 25 (71.4) | 0.148 2 |
n isointense (%) | 1 (8.3) | 5 (14.3) | ||
n predominantly high (%) | 4 (33.3) | 5 (14.3) | ||
n no signal (%) | 1 (8.3) | 0 (0) | ||
Presence of enhancing intra-tumoral septa | n Yes (%) | 2 (16.7) | 17 (48.6) | p = 0.087 3 |
n No (%) | 10 (83.3) | 18 (51.4) | ||
Presence of areas of hemorrhage (= T1 hyperintensity) | n Yes (%) | 0 (0) | 5 (14.3) | p = 0.309 3 |
n No (%) | 12 (100) | 30 (85.7) | ||
Presence of areas of necrosis (= T2 hyperintensity) | n Yes (%) | 2 (16.7) | 9 (25.7) | p = 0.703 3 |
n No (%) | 10 (83.3) | 26 (74.3) | ||
Presence of calcification | n Yes (%) | 1 (8.3) | 4 (11.4) | p > 0.999 3 |
n No (%) | 11 (91.7) | 31 (88.6) | ||
Presence of ipsilateral hydrocele | n Yes (%) | 10 (83.3) | 19 (54.3) | p = 0.095 3 |
n No (%) | 2 (16.7) | 16 (45.7) | ||
Smooth tumor margins | n Yes (%) | 11 (91.7) | 22 (62.9) | p = 0.077 3 |
n No (%) | 1 (8.3) | 13 (37.1) |
Sensitivity in % (95%-CI) | 94.3 (80.8–99.3) |
Specificity in % (95%-CI) | 76.9 (46.2–95.0) |
PPV in % (95%-CI) | 91.7 (77.5–98.3) |
NPV in % (95%-CI) | 83.3 (51.6–97.9) |
Efficiency in % (95%-CI) | 89.6 (77.3–96.5) |
Misdiagnosis in % (95%-CI) | 10.4 (3.5–22.7) |
Parameter | p-Value |
---|---|
Age in years | 0.233 1 |
Size of patient in meters | 0.959 1 |
Weight in kilograms | 0.905 2 |
BMI in kg/m2 | 0.861 2 |
Smoking status | 0.498 1 |
Status of drug use | 0.176 3 |
St. p. cryptorchism | 0.656 3 |
St. p. testicular tumor | >0.999 3 |
St. p. inguinal/testicular operation | 0.410 3 |
Tumor marker positive | 0.008 **3 |
Presence of testosterone deficiency | >0.999 3 |
Size of tumor in histopathology in millimeters (mm) | 0.039 *1 |
Size of tumor in MRI in mm | 0.031 *1 |
Size of affected testis in mm3 (×0.72) | 0.660 1 |
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Törzsök, P.; Deininger, S.; Abenhardt, M.; Oswald, D.; Lusuardi, L.; Deininger, C.; Forstner, R.; Meissnitzer, M.; Brandtner, H.; Hecht, S. Discriminating Malignant from Benign Testicular Masses Using Multiparametric Magnetic Resonance Imaging—A Prospective Single-Center Study. J. Clin. Med. 2024, 13, 4390. https://doi.org/10.3390/jcm13154390
Törzsök P, Deininger S, Abenhardt M, Oswald D, Lusuardi L, Deininger C, Forstner R, Meissnitzer M, Brandtner H, Hecht S. Discriminating Malignant from Benign Testicular Masses Using Multiparametric Magnetic Resonance Imaging—A Prospective Single-Center Study. Journal of Clinical Medicine. 2024; 13(15):4390. https://doi.org/10.3390/jcm13154390
Chicago/Turabian StyleTörzsök, Peter, Susanne Deininger, Michael Abenhardt, David Oswald, Lukas Lusuardi, Christian Deininger, Rosemarie Forstner, Matthias Meissnitzer, Herwig Brandtner, and Stefan Hecht. 2024. "Discriminating Malignant from Benign Testicular Masses Using Multiparametric Magnetic Resonance Imaging—A Prospective Single-Center Study" Journal of Clinical Medicine 13, no. 15: 4390. https://doi.org/10.3390/jcm13154390