Skip to main content
SpringerLink
Log in

Prognostic Role of Tumor Budding and Worst Pattern of Invasion in Lymph Node Metastasis and Disease-Free Survival in Oral Squamous Cell Cancer Patients: Result from Central India’s Regional Cancer Centre

  • Original Article
  • Published:
Indian Journal of Otolaryngology and Head & Neck Surgery Aims and scope Submit manuscript

Abstract

Aim

To study the role of pattern of invasion, tumor budding and other clinicopathological parameters in determining the risk of nodal metastases and disease-free survival in oral squamous cell cancer patients.

Method

The data of 90 patients with oral squamous cell carcinoma who underwent surgery as their primary modality of treatment were retrospectively analysed. Predictive significance of clinicopathological parameters was assessed with Univariate analysis with Fisher exact test and unpaired t-test. The factors which were significant on Univariate analysis were then analysed with multivariate analysis using logistic regression model to find independent predictors. P value < 0.05 was considered significant. Disease free survival analysis was performed using Kaplan-Meier method and comparison done using the log-rank test for each group.

Result

The age of the patients ranged from 22yrs to 72 years with male predominance (81.1%). The most common site of involvement was buccal mucosa. Significant factors predicting nodal metastases on univariate analysis were site (p = 0.031), grade (p = 0.012), T stage (p = < 0.001), Depth of invasion (p = < 0.001), perineural invasion (p = < 0.001), lymphovascular emboli (p = 0.018), tumor budding (p = < 0.001), pattern of invasion (p = < 0.001) and stroma (p = 0.037). On multivariate analysis tumor budding (p = 0.016), depth of invasion (p = 0.016) and perineural invasion (p = 0.044) were predictive of nodal metastasis. A statistically significant difference in 3year disease free survival was seen in infiltrative pattern of invasion and tumor budding which showed a p-value of 0.0372 and 0.0489 respectively.

Conclusion

Based on the findings of the present study and review of previous articles tumor budding, worst pattern of invasion, host lymphocyte response should also be included in routine histopathology reporting of OSCC.

Key Message

Based on the findings of the present study tumor budding, worst pattern of invasion, host lymphocyte response should also be included in routine histopathology reporting of OSCC.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Plot 1

Similar content being viewed by others

Data Availability

Yes.

References

  1. Massano J, Regateiro FS, Januário G, Ferreira A (2006) Oral squamous cell carcinoma: review of prognostic and predictive factors. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontology. ;102(1):67–76

  2. Lim S-C, Zhang S, Ishii G, Endoh Y, Kodama K, Miyamoto S et al (2004) Predictive markers for late cervical metastasis in stage I and II invasive squamous cell carcinoma of the oral tongue. Clin Cancer Res 10(1):166–172

    Article  CAS  PubMed  Google Scholar 

  3. Khafif RA, Gelbfish GA, Tepper P, Attie JN (1991) Elective radical neck dissection in epidermoid cancer of the head and neck. A retrospective analysis of 853 cases of mouth, pharynx, and larynx cancer. Cancer 67(1):67–71

    Article  CAS  PubMed  Google Scholar 

  4. Chatterjee D, Bansal V, Malik V, Bhagat R, Punia RS, Handa U et al (2019) Tumor budding and worse pattern of invasion can predict nodal metastasis in oral cancers and associated with poor survival in early-stage tumors. Ear Nose Throat J 98(7):E112–E9

    Article  PubMed  Google Scholar 

  5. Bankfalvi A, Piffko J (2000) Prognostic and predictive factors in oral cancer: the role of the invasive tumour front. J Oral Pathol Medicine: Rev Article 29(7):291–298

    Article  CAS  Google Scholar 

  6. Manjula B, Augustine S, Selvam S, Mohan AM (2015) Prognostic and predictive factors in gingivo buccal complex squamous cell carcinoma: role of tumor budding and pattern of invasion. Indian J Otolaryngol Head Neck Surg 67:98–104

    Article  CAS  PubMed  Google Scholar 

  7. Seki M, Sano T, Yokoo S, Oyama T (2016) Histologic assessment of tumor budding in preoperative biopsies to predict nodal metastasis in squamous cell carcinoma of the tongue and floor of the mouth. Head Neck 38(S1):E1582–E90

    Article  PubMed  Google Scholar 

  8. Hori Y, Kubota A, Yokose T, Furukawa M, Matsushita T, Oridate N (2020) Association between pathological invasion patterns and late lymph node metastases in patients with surgically treated clinical no early oral tongue carcinoma. Head Neck 42(2):238–243

    Article  PubMed  Google Scholar 

  9. Diaz EM Jr, Holsinger FC, Zuniga ER, Roberts DB, Sorensen DM (2003) Squamous cell carcinoma of the buccal mucosa: one institution’s experience with 119 previously untreated patients. Head Neck: J Sci Specialties Head Neck 25(4):267–273

    Article  Google Scholar 

  10. Bryne M, Koppang HS, Lilleng R, Kjærheim Å (1992) Malignancy grading of the deep invasive margins of oral squamous cell carcinomas has high prognostic value. J Pathol 166(4):375–381

    Article  CAS  PubMed  Google Scholar 

  11. Almangush A, Pirinen M, Heikkinen I, Mäkitie AA, Salo T, Leivo I (2018) Tumour budding in oral squamous cell carcinoma: a meta-analysis. Br J Cancer 118(4):577–586

    Article  PubMed  Google Scholar 

  12. Mäkitie AA, Almangush A, Rodrigo JP, Ferlito A, Leivo I (2019) Hallmarks of cancer: Tumor budding as a sign of invasion and metastasis in head and neck cancer. Head Neck 41(10):3712–3718

    Article  PubMed  Google Scholar 

  13. Seki M, Sano T, Yokoo S, Oyama T (2017) Tumour budding evaluated in biopsy specimens is a useful predictor of prognosis in patients with cN0 early stage oral squamous cell carcinoma. Histopathology 70(6):869–879

    Article  PubMed  Google Scholar 

  14. Angadi PV, Patil PV, Hallikeri K, Mallapur M, Hallikerimath S, Kale AD (2015) Tumor budding is an independent prognostic factor for prediction of lymph node metastasis in oral squamous cell carcinoma. Int J Surg Pathol 23(2):102–110

    Article  CAS  PubMed  Google Scholar 

  15. Ho YY, Wu TY, Cheng HC, Yang CC, Wu CH (2019) The significance of tumor budding in oral cancer survival and its relevance to the eighth edition of the American Joint Committee on Cancer staging system. Head Neck 41(9):2991–3001

    Article  PubMed  Google Scholar 

  16. Arora A, Husain N, Bansal A, Neyaz A, Jaiswal R, Jain K et al (2017) Development of a new outcome prediction model in early-stage squamous cell carcinoma of the oral cavity based on histopathologic parameters with multivariate analysis. Am J Surg Pathol 41(7):950–960

    Article  PubMed  Google Scholar 

  17. Khwaja T, Tayaar AS, Acharya S, Bhushan J, Muddapur M (2018) Pattern of invasion as a factor in determining lymph node metastasis in oral squamous cell carcinoma. J Cancer Res Ther 14(2):382–387

    Article  PubMed  Google Scholar 

  18. Lundqvist L, Stenlund H, Laurell G, Nylander K (2012) The importance of stromal inflammation in squamous cell carcinoma of the tongue. J oral Pathol Med 41(5):379–383

    Article  PubMed  Google Scholar 

  19. Kane S, Gupta M, Kakade A, D’Cruz A (2006) Depth of invasion is the most significant histological predictor of subclinical cervical lymph node metastasis in early squamous carcinomas of the oral cavity. Eur J Surg Oncol (EJSO) 32(7):795–803

    Article  CAS  PubMed  Google Scholar 

  20. Sakata J, Yamana K, Yoshida R, Matsuoka Y, Kawahara K, Arita H et al (2018) Tumor budding as a novel predictor of occult metastasis in cT2N0 tongue squamous cell carcinoma. Hum Pathol 76:1–8

    Article  CAS  PubMed  Google Scholar 

  21. Mishra A, Das A, Dhal I, Shankar R, Bhavya B, Singh N et al (2022) Worst pattern of invasion in oral squamous cell carcinoma is an independent prognostic factor. J Oral Biology Craniofac Res 12(6):771–776

    Article  Google Scholar 

  22. Huang SH, Hwang D, Lockwood G, Goldstein DP, O’Sullivan B (2009) Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta‐analysis of reported studies. Cancer: Interdisciplinary Int J Am Cancer Soc 115(7):1489–1497

    Article  CAS  Google Scholar 

  23. Vila CN, Martínez-Gimeno C, Rodríguez EM, Varela CL (1995) Squamous cell carcinoma of the oral cavity: a clinicopathologic scoring system for evaluating risk of cervical lymph node metastasis. Laryngoscope 105(7):728–733

    Article  PubMed  Google Scholar 

  24. Woolgar JA, Scott J (1995) Prediction of cervical lymph node metastasis in squamous cell carcinoma of the tongue/floor of mouth. Head Neck 17(6):463–472

    Article  CAS  PubMed  Google Scholar 

  25. Hiratsuka H, Miyakawa A, Nakamori K, Kido Y, Sunakawa H, Kohama G (1997) Multivariate analysis of occult lymph node metastasis as a prognostic indicator for patients with squamous cell carcinoma of the oral cavity. Cancer: Interdisciplinary Int J Am Cancer Soc 80(3):351–356

    Article  CAS  Google Scholar 

  26. Borges A, Shrikhande S, Ganesh B (eds) (1989) Surgical pathology of squamous carcinoma of the oral cavity: its impact on management. Seminars in Surgical Oncology. Wiley Online Library

  27. Parekh D, Kukreja P, Mallick I, Roy P (2020) Worst pattern of invasion–type 4 (WPOI-4) and Lymphocyte host response should be mandatory reporting criteria for oral cavity squamous cell carcinoma: a re-look at the American Joint Committee of Cancer (AJCC) minimum dataset. Indian J Pathol Microbiol 63(4):527

    Article  PubMed  Google Scholar 

  28. Shimizu S, Miyazaki A, Sonoda T, Koike K, Ogi K, Kobayashi J-i et al (2018) Tumor budding is an independent prognostic marker in early stage oral squamous cell carcinoma: with special reference to the mode of invasion and worst pattern of invasion. PLoS ONE 13(4):e0195451

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, Government Medical college, Nagpur, India

    Renuka Badanale

  2. Department of Head and neck Oncology, Rashtrasant Tukdoji Cancer Hospital, Nagpur, India

    Vandana Mohta & Aniruddha Wagh

  3. Department of Radiation Oncology, Rashtrasant Tukdoji Cancer Hospital, Nagpur, India

    Kartar Singh

Authors
  1. Renuka Badanale
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vandana Mohta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aniruddha Wagh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kartar Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The manuscript has been reads and approved by all the authors and each author satisfies the authorship requirements. Dr. Renuka Badanale- Conception and design of study, Acquisition of data, Analysis and interpretation of data, Drafting the manuscript. Dr. Vandana Mohta- Conception and design of study, Acquisition of data, Analysis and interpretation of data, Critical revision. Dr. Aniruddha Wagh- Acquisition of data, Critical revision. Dr. Kartar Singh- Acquisition of data, Critical revision.

Corresponding author

Correspondence to Vandana Mohta.

Ethics declarations

Ethics Approval

Ethical approval was waived by the local ethics committee in view of retrospective nature of the study and all the procedures being performed were part of routine care.

Consent

NA.

Sources of Support

NIL.

Financial Disclosure

No sources of funding.

Conflict of Interest

None.

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

Badanale, R., Mohta, V., Wagh, A. et al. Prognostic Role of Tumor Budding and Worst Pattern of Invasion in Lymph Node Metastasis and Disease-Free Survival in Oral Squamous Cell Cancer Patients: Result from Central India’s Regional Cancer Centre. Indian J Otolaryngol Head Neck Surg (2024). https://doi.org/10.1007/s12070-024-04661-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12070-024-04661-4

Keywords

Search

Navigation