Skip to main content
SpringerLink
Log in

Worst Pattern of Invasion as a Predictor of Nodal Metastasis in Early-Stage Oral Squamous Cell Carcinoma

  • Original Article
  • Published:
Indian Journal of Surgical Oncology Aims and scope Submit manuscript

Abstract

About one-third of early stage oral cancer patients have occult nodal metastasis. High grade worst pattern of invasion (WPOI) is associated with an increased risk of nodal metastasis and poor prognosis. However, it still remains unanswered whether to perform an elective neck dissection for clinically node-negative disease or not. This study aims to evaluate the role of histological parameters including WPOI in predicting nodal metastasis in early-stage oral cancers. This analytical observational study comprised 100 patients of early-stage, node-negative, oral squamous cell carcinoma, admitted in the Surgical Oncology Department from April, 2018 till the sample size was reached. The socio-demographic data, clinical history, and findings of clinical and radiological examination were noted. The association of nodal metastasis with various histological parameters like tumour size, degree of differentiation, depth of invasion (DOI), WPOI, perineural invasion (PNI), lymphovascular invasion (LVI) and lymphocytic response was determined. SPSS 20.0 statistical tool; student’s ‘t’ test and chi-square tests were applied. While the buccal mucosa was the commonest site, the rate of occult metastasis was highest in the tongue. Nodal metastasis was not significantly associated with age, sex, smoking and primary site. While the nodal positivity was not significantly associated with tumour size, pathological stage, DOI, PNI and lymphocytic response, it was associated with LVI, degree of differentiation and WPOI. Increasing WPOI grade correlated significantly with the nodal stage, LVI and PNI, but not with DOI. WPOI is not only a significant predictor of occult nodal metastasis but can also be a novel therapeutic tool in the management of early-stage oral cancers. In patients with an aggressive WPOI pattern or other high-risk histological parameters, the neck can be addressed with either elective neck dissection or radiotherapy after wide excision of the primary tumor; otherwise, an active surveillance approach can be followed.

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

Similar content being viewed by others

References

  1. Aupérin A (2020) Epidemiology of head and neck cancers: an update. Curr Opin Oncol 32(3):178–186. https://doi.org/10.1097/CCO.0000000000000629 (PMID: 32209823)

    Article  PubMed  Google Scholar 

  2. Misra S, Chaturvedi A, Misra NC (2008) Management of gingivobuccal complex cancer. Ann R Coll SurgEngl 90:546–553

    Article  Google Scholar 

  3. Christopher JO, Brien TJ (2009) Epidemiology in head and neck cancer. In: Souza CD (ed) Head and Neck Surgery, 1st edn. Jaypee Brothers Medical Publishers (P) Ltd., Delhi, India, pp 939–969.

  4. 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. https://doi.org/10.3322/caac.21660. Epub ahead of print. PMID: 33538338.

  5. Saghravanian N, Ghazi N, Meshkat Z, Mohtasham N (2015) Human papillomavirus in oral leukoplakia, verrucous carcinoma, squamous cell carcinoma, and normal mucous membrane. Oman Med J 30:455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mohtasham N, Anvari K, Memar B, Saghravanian N, Ghazi N, Bagherpour A et al (2014) Expression of E-cadherin and matrix metalloproteinase-9 in oral squamous cell carcinoma and histologically negative surgical margins and association with clinicopathological parameters. Rom J MorpholEmbryol 55:117–121

    Google Scholar 

  7. Salehinejad J, Sharifi N, Amirchaghmaghi M, Ghazi N, Shakeri MT, Ghazi A (2014) Immunohistochemical expression of p16 protein in oral squamous cell carcinoma and lichen planus. Diagn Pathol 18:210–213

    Article  Google Scholar 

  8. Lingen MW, Kalmar JR, Karrison T, Speight PM (2008) Critical evaluation of diagnostic aids for the detection of oral cancer. Oral Oncol 44:10–22

    Article  PubMed  Google Scholar 

  9. Diaz EM Jr, Holsinger FC, Zuniga ER et al (2003) Squamous cell carcinoma of the buccal mucosa: one institution’s experience with 119 previously untreated patients. Head Neck 25:267–273

    Article  PubMed  Google Scholar 

  10. Lim SC, 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 Pt 1):166–172. https://doi.org/10.1158/1078-0432.ccr-0533-3

    Article  CAS  PubMed  Google Scholar 

  11. Arora A, Husain N, Bansal A 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: the Aditi-Nuzhat Lymph-Node Prediction Score (ANLPS) system. Am J SurgPathol 41(7):950–960

    Article  Google Scholar 

  12. Almangush A, Bello IO, Keski-Santti H et al (2014) Depth of invasion, tumour budding, and worst pattern of invasion: prognostic indicators in early-stage oral tongue cancer. Head Neck 36(6):811–818

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  14. Almangush A, Bello IO, Coletta RD et al (2015) For early-stage oral tongue cancer, depth of invasion and worst pattern of invasion are the strongest pathological predictors for locoregional recurrence and mortality. Virchows Arch 467(1):39–46

    Article  PubMed  Google Scholar 

  15. Manjula BV, Augustine S, Selvam S, Mohan AM (2015) Prognostic and predictive factors in gingivo buccal complex squamous cell carcinoma: role of tumour budding and pattern of invasion. Indian J Otolaryngol Head Neck Surg 67(suppl 1):98–104

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  17. Izumo T, Kirita T, Ariji E, Ozeki S, Okada N, Okabe S, et al (2012); Working Group 1 on the ‘Guidelines for Clinical and Pathological Studies of Oral Cancer’, Scientific Committee, Japan Society for Oral Tumors. General rules for clinical and pathological studies on oral cancer: a synopsis. Jpn J Clin Oncol 42(11):1099–1109. doi: https://doi.org/10.1093/jjco/hys141. Epub 2012 Sep 28. PMID: 23024282.

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

    Article  CAS  PubMed  Google Scholar 

  19. Bryne M (1998) Is the invasive front of an oral carcinoma the most important area for prognostication? Oral Dis 4:70–77

    Article  CAS  PubMed  Google Scholar 

  20. Brandwein-Gensler M, Teixeira MS, Lewis CM et al (2005) Oral squamous cell carcinoma: histologic risk assessment, but not margin status, is strongly predictive of local disease-free and overall survival. Am J SurgPathol 29:167–178

    Article  Google Scholar 

  21. Ridge JA, Lydiatt WM, Patel SG, et al (2017) Head and neck. In: Amin MB, Edge S, Greene FL (eds) AJCC Cancer Staging Manual, 8th ed. NY: Springer, New York, pp 79–94.

  22. Ferlito A, Silver CE, Rinaldo A (2009) Elective management of the neck in oral cavity squamous carcinoma: current concepts supported by prospective studies. Br J Oral Maxillofac Surg 47(1):5–9. https://doi.org/10.1016/j.bjoms.2008.06.001

    Article  PubMed  Google Scholar 

  23. Shah JP (1990) Patterns of cervical lymph node metastasis from squamous carcinomas of the upper aerodigestive tract. Am J Surg 160:405–409

    Article  CAS  PubMed  Google Scholar 

  24. Chatterjee D, Bansal V, Malik V, Bhagat R, Punia RS, Handa U, Gupta A, Dass A (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–E119. https://doi.org/10.1177/0145561319848669 (Epub 2019 May 9 PMID: 31072197)

    Article  PubMed  Google Scholar 

  25. Thiagarajan S, Nair S, Nair D, Chaturvedi P, Kane SV, Agarwal JP, D’Cruz AK (2014) Predictors of prognosis for squamous cell carcinoma of oral tongue. J Surg Oncol 109(7):639–644. https://doi.org/10.1002/jso.23583 (Epub 2014 Mar 12 PMID: 24619660)

    Article  PubMed  Google Scholar 

  26. 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 80:351–356 (PMID: 9241067)

    Article  CAS  PubMed  Google Scholar 

  27. De Silva RK, Siriwardena BSMS, Samaranayaka A, Abeyasinghe WAMUL, Tilakaratne WM (2018) A model to predict nodal metastasis in patients with oral squamous cell carcinoma. PLoS ONE 13(8):e0201755. https://doi.org/10.1371/journal.pone.0201755.PMID:30091996;PMCID:PMC6084951

    Article  PubMed  PubMed Central  Google Scholar 

  28. Sahoo A, Panda S, Mohanty N et al (2020) Perinerural, lymphovascular and depths of invasion in extrapolating nodal metastasis in oral cancer. Clin Oral Invest 24:747–755

    Article  Google Scholar 

  29. Huang S, Zhu Y, Cai H, Zhang Y, Hou J (2021) Impact of lymphovascular invasion in oral squamous cell carcinoma: a meta-analysis. Oral Surg Oral Med Oral Pathol Oral Radiol 131(3):319-328.e1. https://doi.org/10.1016/j.oooo.2020.10.026 (Epub 2020 Nov 5 PMID: 33309267)

    Article  PubMed  Google Scholar 

  30. Brandwein-Gensler M, Smith RV, Wang B et al (2010) Validation of the histologic risk model in a new cohort of patients with head and neck squamous cell carcinoma. Am J SurgPathol 34:676–688

    Article  Google Scholar 

  31. Dissanayaka WL, Pitiyage G, Kumarasiri P, Liyanage R, Dias DK, Tilakaratne WM (2012) Clinical and histopathologic parameters in survival of oral squamous cell carcinoma. Oral Surg Oral Med Oral Pathol Oral Radiol 113:518–525. https://doi.org/10.1016/j.oooo.2011.11.001 (PMID:22668430)

    Article  PubMed  Google Scholar 

  32. Yue LE, Sharif KF, Sims JR, Sandler ML, Baik FM, Sobotka S, Everest S, Brandwein-Weber M, Khorsandi AS, Likhterov I, Urken ML (2020) Oral squamous carcinoma: aggressive tumor pattern of invasion predicts direct mandible invasion. Head Neck 42(11):3171–3178. https://doi.org/10.1002/hed.26360 (Epub 2020 Jul 25 PMID: 32710523)

    Article  PubMed  Google Scholar 

  33. Nanda SS, Gandhi AK, Rastogi M, Patni A, Khurana R et al (2020) PO-0844: worst pattern of invasion and its association with histopathological features in oral cavity cancer. Radiother Oncol 152:S455–S456. https://doi.org/10.1016/S0167-8140(21)00861-6

    Article  Google Scholar 

  34. Ahlawat P, Krishnan A, Gairola M, Tandon S, Purohit S, Sachdeva N, Sharief MI, Dobriyal K, Singh T. Inter-correlations between various high-risk pathological factors in squamous cell carcinoma tongue. Paper presented at: ESTRO 2021; March 5,2021; Madrid, Spain. https://www.estro.org/Congresses/ESTRO-2021/881/headandneck/5117/inter-correlationsbetweenvarioushigh-riskpathologi

  35. Weiss MH, Harrison LB, Isaacs RS (1994) Use of decision analysis in planning a management strategy for the stage N0 neck. Arch Otolaryngol Head Neck Surg 120:699–702

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgical Oncology, Sawai Man Singh Medical College and Hospital, Jaipur, Rajasthan, India

    Kamal Kishor Lakhera, Rohit Jindal, Pinakin Patel, Suresh Singh, Akhlak Hussain & Raj Govind Sharma

  2. Department of General Surgery, District Hospital, Tonk, Rajasthan, India

    Yashwant Nama

  3. Department of Pathology, Sawai Man Singh Medical College and Hospital, Jaipur, Rajasthan, India

    Pratibha Maan

Authors
  1. Kamal Kishor Lakhera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yashwant Nama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pratibha Maan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rohit Jindal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pinakin Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Suresh Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Akhlak Hussain
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Raj Govind Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KKL: concept; analysis and/or interpretation.

YN: design; literature search; writing.

PM: concept; design.

RJ: concept; design; literature search; writing.

PP: analysis and/or interpretation.

SS: supervision; critical review.

AH: analysis and/or interpretation; literature search.

RGS: critical review; supervision.

Corresponding author

Correspondence to Rohit Jindal.

Ethics declarations

Ethics Approval and Consent to Participate

The research involved human participants and a well informed consent was taken from each individual.

Also, approval was taken from the institutional ethical committee.

Conflict of Interest

The authors declare no competing interests.

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 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

Lakhera, K.K., Nama, Y., Maan, P. et al. Worst Pattern of Invasion as a Predictor of Nodal Metastasis in Early-Stage Oral Squamous Cell Carcinoma. Indian J Surg Oncol 14, 160–168 (2023). https://doi.org/10.1007/s13193-022-01639-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13193-022-01639-y

Keywords

Search

Navigation