Usefulness of the inchworm sign on DWI for predicting pT1 bladder cancer progression

Abstract

Objective

To evaluate the significance of the presence or absence of an “inchworm sign” on DWI for the recurrence and progression of T1 bladder cancer.

Materials and methods

We retrospectively analyzed 91 patients with pT1 urothelial carcinoma who underwent DWI prior to transurethral resection between 2007 and 2016. DWI of the dominant tumors was scrutinized for inchworm signs at b = 1000 s/mm2. The association of the presence of the inchworm sign with progression and recurrence was analyzed; progression was defined as recurrence to stage T2 or higher and/or N+, and/or M1.

Results

An inchworm sign was seen in 65 cases (71%), while it was absent in 26 cases. Among the 65, 25 (38%) had confirmed tumor recurrence, while in the remaining 26, 14 (54%) had confirmed recurrence (median time post TURB = 7.9 and 10.1 months for each). At the time of recurrence, the tumor had progressed in one (2%) inchworm-sign-positive and seven (27%) inchworm-sign-negative cases. The progression rate of inchworm-sign-negative cases was significantly higher than that of inchworm-sign-positive cases (hazard ratio = 17.2, p = 0.0017), whereas there was no significant difference in the recurrence rate between two groups. The absence of an inchworm sign and histological grade 3 were independent risk factors for progression (p < 0.001 and 0.010, respectively).

Conclusions

The absence of an inchworm sign on DWI was a significant prognostic factor for progression of T1 bladder cancer. Morphological evaluation of DWI signals may therefore be a useful adjunct to preoperative assessment of biological aggressiveness.

Key Points

• An inchworm sign is a simple diagnostic criterion that characterizes only the shape of the tumor signal on DWI, and potentially serves as an imaging biomarker to predict clinical aggressiveness.

• The absence of an inchworm sign on DWI is a significant indicator of progression of T1 bladder cancer.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

ADC:

Apparent diffusion coefficient

BCG:

Bacillus Calmette-Guérin

CUETO:

Club Urológico Español de Tratamiento Oncológico

DWI:

Diffusion-weighted imaging

EORTC:

European Organisation for Research and Treatment of Cancer

HR:

Hazard ratio

MRI:

Magnetic resonance imaging

NMIBC:

Non-muscle-invasive bladder cancer

SI:

Signal intensity

T2WI:

T2-weighted MRI

TURB:

Transurethral resection of the bladder

References

  1. 1.

    Aldousari S, Kassouf W (2010) Update on the management of non-muscle invasive bladder cancer. Can Urol Assoc J 4:56–64

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Fujii Y (2018) Prediction models for progression of non-muscle-invasive bladder cancer: a review. Int J Urol 25:212–218

    Article  PubMed  Google Scholar 

  3. 3.

    Herr HW (1997) Tumour progression and survival in patients with T1G3 bladder tumours: 15-year outcome. Br J Urol 80:762–765

    Article  CAS  PubMed  Google Scholar 

  4. 4.

    Sylvester RJ, van der Meijden AP, Oosterlinck W et al (2006) Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTC risk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol 49:466–465 discussion 75-7

    Article  Google Scholar 

  5. 5.

    Fernandez-Gomez J, Madero R, Solsona E et al (2009) Predicting nonmuscle invasive bladder cancer recurrence and progression in patients treated with bacillus Calmette-Guerin: the CUETO scoring model. J Urol 182:2195–2203

    Article  Google Scholar 

  6. 6.

    Cambier S, Sylvester RJ, Collette L et al (2016) EORTC nomograms and risk groups for predicting recurrence, progression, and disease-specific and overall survival in non-muscle-invasive stage Ta-T1 urothelial bladder cancer patients treated with 1-3 years of maintenance bacillus Calmette-Guerin. Eur Urol 69:60–69

    Article  PubMed  Google Scholar 

  7. 7.

    Kurth KH, Denis L, Bouffioux C et al (1995) Factors affecting recurrence and progression in superficial bladder tumours. Eur J Cancer 31a:1840–1846

    Article  CAS  PubMed  Google Scholar 

  8. 8.

    Stephenson WT, Holmes FF, Noble MJ, Gerald KB (1990) Analysis of bladder carcinoma by subsite. Cystoscopic location may have prognostic value. Cancer 66:1630–1635

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Vukomanovic I, Colovic V, Soldatovic I, Hadzi-Djokic J (2012) Prognostic significance of tumor location in high-grade non-muscle-invasive bladder cancer. Med Oncol 29:1916–1920

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Fujii Y, Fukui I, Kihara K et al (1998) Significance of bladder neck involvement on progression in superficial bladder cancer. Eur Urol 33:464–468

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Kobayashi S, Fujii Y, Koga F et al (2014) Impact of bladder neck involvement on progression in patients with primary non-muscle invasive bladder cancer: a prospective validation study. Urol Oncol 32:38.e29–38.e36

    Article  Google Scholar 

  12. 12.

    Yoshida S, Masuda H, Ishii C et al (2011) Usefulness of diffusion-weighted MRI in diagnosis of upper urinary tract cancer. AJR Am J Roentgenol 196:110–116

    Article  PubMed  Google Scholar 

  13. 13.

    Uchida Y, Yoshida S, Kobayashi S et al (2014) Diffusion-weighted MRI as a potential imaging biomarker reflecting the metastatic potential of upper urinary tract cancer. Br J Radiol 87:20130791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Yoshida S, Takahara T, Kwee TC, Waseda Y, Kobayashi S, Fujii Y (2017) DWI as an imaging biomarker for bladder cancer. AJR Am J Roentgenol 208:1218–1228

    Article  PubMed  Google Scholar 

  15. 15.

    Avcu S, Koseoglu MN, Ceylan K, Bulut MD, Unal O (2011) The value of diffusion-weighted MRI in the diagnosis of malignant and benign urinary bladder lesions. Br J Radiol 84:875–882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Kobayashi S, Koga F, Yoshida S et al (2011) Diagnostic performance of diffusion-weighted magnetic resonance imaging in bladder cancer: potential utility of apparent diffusion coefficient values as a biomarker to predict clinical aggressiveness. Eur Radiol 21:2178–2186

    Article  Google Scholar 

  17. 17.

    Takeuchi M, Sasaki S, Ito M et al (2009) Urinary bladder cancer: diffusion-weighted MR imaging--accuracy for diagnosing T stage and estimating histologic grade. Radiology 251:112–121

    Article  Google Scholar 

  18. 18.

    Orsola A, Trias I, Raventos CX et al (2005) Initial high-grade T1 urothelial cell carcinoma: feasibility and prognostic significance of lamina propria invasion microstaging (T1a/b/c) in BCG-treated and BCG-non-treated patients. Eur Urol 48:231–238 discussion 8

    Article  CAS  PubMed  Google Scholar 

  19. 19.

    Smits G, Schaafsma E, Kiemeney L, Caris C, Debruyne F, Witjes JA (1998) Microstaging of pT1 transitional cell carcinoma of the bladder: identification of subgroups with distinct risks of progression. Urology 52:1009–1013 discussion 13-4

    Article  CAS  PubMed  Google Scholar 

  20. 20.

    Kondylis FI, Demirci S, Ladaga L, Kolm P, Schellhammer PF (2000) Outcomes after intravesical bacillus Calmette-Guerin are not affected by substaging of high grade T1 transitional cell carcinoma. J Urol 163:1120–1123

    Article  CAS  PubMed  Google Scholar 

  21. 21.

    Cheng L, Neumann RM, Weaver AL, Spotts BE, Bostwick DG (1999) Predicting cancer progression in patients with stage T1 bladder carcinoma. J Clin Oncol 17:3182–3187

    Article  CAS  PubMed  Google Scholar 

  22. 22.

    Babjuk M, Bohle A, Burger M et al (2017) EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2016. Eur Urol 71:447–461

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Platz CE, Cohen MB, Jones MP, Olson DB, Lynch CF (1996) Is microstaging of early invasive cancer of the urinary bladder possible or useful? Mod Pathol 9:1035–1039

    CAS  PubMed  Google Scholar 

  24. 24.

    Lin WC, Chen JH (2015) Pitfalls and limitations of diffusion-weighted magnetic resonance imaging in the diagnosis of urinary bladder cancer. Transl Oncol 8:217–230

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Panebianco V, Narumi Y, Altun E et al (2018) Multiparametric magnetic resonance imaging for bladder cancer: development of VI-RADS (vesical imaging-reporting and data system). Eur Urol 74:294–306

    Article  Google Scholar 

Download references

Acknowledgments

I gratefully acknowledge the work of past and present members of our department.

Funding

The authors state that this work has not received any funding.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Soichiro Yoshida.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Soichiro Yoshida.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• observational

• performed at one institution

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yajima, S., Yoshida, S., Takahara, T. et al. Usefulness of the inchworm sign on DWI for predicting pT1 bladder cancer progression. Eur Radiol 29, 3881–3888 (2019). https://doi.org/10.1007/s00330-019-06119-6

Download citation

Keywords

  • Diffusion magnetic resonance imaging
  • Magnetic resonance imaging
  • Biomarkers
  • Prognosis
  • Urinary bladder neoplasms