Skip to main content
Log in

Whole-tumor histogram analysis of apparent diffusion coefficient maps with machine learning algorithms for predicting histologic grade of sinonasal squamous cell carcinoma: a preliminary study

  • Rhinology
  • Published:
European Archives of Oto-Rhino-Laryngology Aims and scope Submit manuscript

Abstract

Purpose

Accurate histologic grade assessment is helpful for clinical decision making and prognostic assessment of sinonasal squamous cell carcinoma (SNSCC). This research aimed to explore whether whole-tumor histogram analysis of apparent diffusion coefficient (ADC) maps with machine learning algorithms can predict histologic grade of SNSCC.

Methods

One hundred and forty-seven patients with pathologically diagnosed SNSCC formed this retrospective study. Sixty-six patients were low-grade (grade I/II) and eighty-one patients were high-grade (grade III). Eighteen histogram features were obtained from quantitative ADC maps. Additionally, the mean ADC value and clinical features were analyzed for comparison with histogram features. Machine learning algorithms were applied to build the best diagnostic model for predicting histological grade. The receiver operating characteristic (ROC) curve was used to evaluate the performance of each model prediction, and the area under the ROC curve (AUC) were analyzed.

Results

The histogram model based on three features (10th Percentile, Mean, and 90th Percentile) with support vector machine (SVM) classifier demonstrated excellent diagnostic performance, with an AUC of 0.947 on the testing dataset. The AUC of the histogram model was similar to that of the mean ADC value model (0.947 vs 0.957; P = 0.7029). The poor diagnostic performance of the clinical model (AUC = 0.692) was improved by the combined model incorporating histogram features or mean ADC value (P < 0.05).

Conclusion

ADC histogram analysis improved the projection of SNSCC histologic grade, compared with clinical model. The complex histogram model had comparable but not better performance than mean ADC value model.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and materials

The authors declare that the data are available.

Code availability

The authors declare that the custom code can be available.

Abbreviations

SNSCC:

Sinonasal squamous cell carcinoma

HNSCC:

Head and neck squamous cell carcinoma

DWI:

Diffusion-weighted imaging

ADC:

Apparent diffusion coefficient

RESOLVE:

Readout-segmented echo-planar imaging sequence

SMOTE:

Synthetic minority oversampling technique

PCC:

Pearson correlation coefficient

ANOVA:

Analysis of variance

KW:

Kruskal–Wallis

RFE:

Recursive feature elimination

SVM:

Support vector machine

LDA:

Linear discriminant analysis

LR:

Logistic regression

References

  1. Turner JH, Reh DD (2012) Incidence and survival in patients with sinonasal cancer: a historical analysis of population-based data. Head Neck 34:877–885. https://doi.org/10.1002/hed.21830

    Article  PubMed  Google Scholar 

  2. Quan H, Yan L, Zhang H et al (2019) Development and validation of a nomogram for prognosis of sinonasal squamous cell carcinoma. Int Forum Allergy Rhinol 9:1030–1040. https://doi.org/10.1002/alr.22354

    Article  PubMed  Google Scholar 

  3. Roland NJ, Caslin AW, Nash J et al (1992) Value of grading squamous cell carcinoma of the head and neck. Head Neck 14:224–229. https://doi.org/10.1002/hed.2880140310

    Article  CAS  PubMed  Google Scholar 

  4. Larsen SR, Johansen J, Sørensen JA et al (2009) The prognostic significance of histological features in oral squamous cell carcinoma. J Oral Pathol Med 38:657–662. https://doi.org/10.1111/j.1600-0714.2009.00797.x

    Article  CAS  PubMed  Google Scholar 

  5. Ackall FY, Issa K, Barak I et al (2021) Survival outcomes in sinonasal poorly differentiated squamous cell carcinoma. Laryngoscope 131:E1040–E1048. https://doi.org/10.1002/lary.29090

    Article  PubMed  Google Scholar 

  6. Pfister DG, Spencer S, Adelstein D et al (2020) Head and neck cancers, version 2.2020, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 18:873–898. https://doi.org/10.6004/jnccn.2020.0031

    Article  PubMed  Google Scholar 

  7. Gencturk M, Ozturk K, Caicedo-Granados E et al (2019) Application of diffusion-weighted MR imaging with ADC measurement for distinguishing between the histopathological types of sinonasal neoplasms. Clin Imaging 55:76–82. https://doi.org/10.1016/j.clinimag.2019.02.004

    Article  PubMed  Google Scholar 

  8. Yun TJ, Kim J, Kim KH et al (2013) Head and neck squamous cell carcinoma: differentiation of histologic grade with standard- and high-b-value diffusion-weighted MRI. Head Neck 35:626–631. https://doi.org/10.1002/hed.23008

    Article  PubMed  Google Scholar 

  9. Just N (2014) Improving tumour heterogeneity MRI assessment with histograms. Br J Cancer 111:2205–2213. https://doi.org/10.1038/bjc.2014.512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Meyer HJ, Leifels L, Hamerla G et al (2018) ADC-histogram analysis in head and neck squamous cell carcinoma. Associations with different histopathological features including expression of EGFR, VEGF, HIF-1α, Her 2 and p53. A preliminary study Magn Reson Imaging 54:214–217. https://doi.org/10.1016/j.mri.2018.07.013

    Article  CAS  PubMed  Google Scholar 

  11. Ren J, Yuan Y, Tao X (2022) Histogram analysis of diffusion-weighted imaging and dynamic contrast-enhanced MRI for predicting occult lymph node metastasis in early-stage oral tongue squamous cell carcinoma. Eur Radiol 32:2739–2747. https://doi.org/10.1007/s00330-021-08310-0

    Article  PubMed  Google Scholar 

  12. Perrot TD, Lenoir V, Ayllón MD et al (2017) Apparent diffusion coefficient histograms of human papillomavirus-positive and human papillomavirus-negative head and neck squamous cell carcinoma: assessment of tumor heterogeneity and comparison with histopathology. AJNR Am J Neuroradiol 38:2153–2160. https://doi.org/10.3174/ajnr.A5370

    Article  PubMed  PubMed Central  Google Scholar 

  13. Srinivasan A, Chenevert TL, Dwamena BA et al (2012) Utility of pretreatment mean apparent diffusion coefficient and apparent diffusion coefficient histograms in prediction of outcome to chemoradiation in head and neck squamous cell carcinoma. J Comput Assist Tomogr 36:131–137. https://doi.org/10.1097/RCT.0b013e3182405435

    Article  PubMed  Google Scholar 

  14. Tsuchiya N, Doai M, Usuda K et al (2017) Non-small cell lung cancer: Whole-lesion histogram analysis of the apparent diffusion coefficient for assessment of tumor grade, lymphovascular invasion and pleural invasion. PLoS ONE 12:e0172433. https://doi.org/10.1371/journal.pone.0172433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Xue H, Ren C, Yang J et al (2014) Histogram analysis of apparent diffusion coefficient for the assessment of local aggressiveness of cervical cancer. Arch Gynecol Obstet 290:341–348. https://doi.org/10.1007/s00404-014-3221-9

    Article  PubMed  Google Scholar 

  16. Donati OF, Mazaheri Y, Afaq A et al (2014) Prostate cancer aggressiveness: assessment with whole-lesion histogram analysis of the apparent diffusion coefficient. Radiology 271:143–152. https://doi.org/10.1148/radiol.13130973

    Article  PubMed  Google Scholar 

  17. Nougaret S, Reinhold C, Alsharif SS et al (2015) Endometrial cancer: combined MR volumetry and diffusion-weighted imaging for assessment of myometrial and lymphovascular invasion and tumor grade. Radiology 276:797–808. https://doi.org/10.1148/radiol.15141212

    Article  PubMed  Google Scholar 

  18. Bonello L, Preda L, Conte G et al (2016) Squamous cell carcinoma of the oral cavity and oropharynx: what does the apparent diffusion coefficient tell us about its histology? Acta Radiol 57:1344–1351. https://doi.org/10.1177/0284185115587734

    Article  PubMed  Google Scholar 

  19. Surov A, Meyer HJ, Winter K et al (2018) Histogram analysis parameters of apparent diffusion coefficient reflect tumor cellularity and proliferation activity in head and neck squamous cell carcinoma. Oncotarget 9:23599–23607. https://doi.org/10.18632/oncotarget.25284

    Article  PubMed  PubMed Central  Google Scholar 

  20. Song Y, Zhang J, Zhang Y et al (2020) FeAture explorer (FAE): a tool for developing and comparing radiomics models. PLoS ONE 15:e0237587. https://doi.org/10.1371/journal.pone.0237587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ren J, Qi M, Yuan Y et al (2020) Machine learning-based MRI texture analysis to predict the histologic grade of oral squamous cell carcinoma. AJR Am J Roentgenol 215:1184–1190. https://doi.org/10.2214/AJR.19.22593

    Article  PubMed  Google Scholar 

  22. Dik EA, Ipenburg NA, Kessler PA et al (2018) The value of histological grading of biopsy and resection specimens in early stage oral squamous cell carcinomas. J Craniomaxillofac Surg 46:1001–1006. https://doi.org/10.1016/j.jcms.2018.03.019

    Article  PubMed  Google Scholar 

  23. Lin N, Yu S, Xia Z et al (2022) Apparent diffusion coefficient-based radiomic nomogram in sinonasal squamous cell carcinoma: a preliminary study on histological grade evaluation. J Comput Assist Tomogr 46:823–829. https://doi.org/10.1097/RCT.0000000000001329

    Article  PubMed  Google Scholar 

  24. Alabi RO, Youssef O, Pirinen M et al (2021) Machine learning in oral squamous cell carcinoma: current status, clinical concerns and prospects for future—a systematic review. Artif Intell Med 115:102060. https://doi.org/10.1016/j.artmed.2021.102060

    Article  PubMed  Google Scholar 

  25. Fujima N, Shimizu Y, Yoshida D et al (2019) Machine-learning-based prediction of treatment outcomes using MR imaging-derived quantitative tumor information in patients with sinonasal squamous cell carcinomas: a preliminary study. Cancers (Basel) 11:800. https://doi.org/10.3390/cancers11060800

    Article  PubMed  Google Scholar 

  26. Surov A, Meyer HJ, Wienke A (2017) Correlation between apparent diffusion coefficient (ADC) and cellularity is different in several tumors: a meta-analysis. Oncotarget 8:59492–59499. https://doi.org/10.18632/oncotarget.17752

    Article  PubMed  PubMed Central  Google Scholar 

  27. Woo S, Cho JY, Kim SY et al (2014) Histogram analysis of apparent diffusion coefficient map of diffusion-weighted MRI in endometrial cancer: a preliminary correlation study with histological grade. Acta Radiol 55:1270–1277. https://doi.org/10.1177/0284185113514967

    Article  PubMed  Google Scholar 

  28. Bozdağ M, Er A, Çinkooğlu A (2021) Histogram analysis of ADC maps for differentiating brain metastases from different histological types of lung cancers. Can Assoc Radiol J 72:271–278. https://doi.org/10.1177/0846537120933837

    Article  PubMed  Google Scholar 

  29. Ren J, Qi M, Yuan Y et al (2021) Radiomics of apparent diffusion coefficient maps to predict histologic grade in squamous cell carcinoma of the oral tongue and floor of mouth: a preliminary study. Acta Radiol 62:453–461. https://doi.org/10.1177/0284185120931683

    Article  PubMed  Google Scholar 

  30. Ahn SJ, Choi SH, Kim Y et al (2012) Histogram analysis of apparent diffusion coefficient map of standard and high B-value diffusion MR imaging in head and neck squamous cell carcinoma: a correlation study with histological grade. Acad Radiol 19:1233–1240. https://doi.org/10.1016/j.acra.2012.04.019

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yan Sha.

Ethics declarations

Conflict of interest

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Ethical approval

This study was approved by the institutional review board of our university hospital and written consent was obtained from each patient.

Additional information

Publisher's Note

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

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Geng, Y., Hong, R., Cheng, Y. et al. Whole-tumor histogram analysis of apparent diffusion coefficient maps with machine learning algorithms for predicting histologic grade of sinonasal squamous cell carcinoma: a preliminary study. Eur Arch Otorhinolaryngol 280, 4131–4140 (2023). https://doi.org/10.1007/s00405-023-07989-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00405-023-07989-9

Keywords

Navigation