Abstract
Although Worst pattern of invasion (WPOI) is one of the histopathological (HP) markers that has been utilized in risk stratification of oral squamous cell carcinoma (OSCC) patients, its potential as an independent predictive factor for lymph node metastasis (LNM) and prognosis is least analyzed. Aim of the study is to analyze the relationship of various HP parameters to WPOI, their propensity for lymph node metastasis and prognostic value. This retrospective study included 140 patients diagnosed with resectable OSCC who underwent definitive surgery. Multiparametric HP risk assessment was done on the postoperative specimen and patients were categorized as low-risk WPOI (Type 1–3), and high-risk group (type 4 and 5). After categorization, 36.1% patients had low-risk WPOI and 63.9% had high-risk WPOI. Significant association was noted between WPOI and patient’s age (p = 0.001), nodal stage (p = 0.001), lymphovascular invasion (LVI) (p = 0.006) and neural invasion (p = 0.001). 87% patients with nodal metastasis had high risk WPOI. LVI (p = 0.014) and WPOI (p < 0.001) had significant predictive role in LNM. High-risk WPOI and bone involvement were found to be predictive factors for overall survival, and only high risk WPOI had strong correlation with disease free survival having significant poor prognosis. Analyzing WPOI is essential in reporting HP specimens in OSCC. High-risk WPOI can act as an independent predictor for LNM, early recurrence and poor prognosis. Incorporation of WPOI into TNM staging is recommended to improve clinician’s ability to prognosticate and individualize treatment strategies.
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References
Gupta N, Gupta R, Acharya AK et al (2016 Dec) Changing Trends in oral cancer-a global scenario. Nepal J Epidemiol 6(4):613
Safi AF, Grandoch A, Nickenig HJ et al (2017 Dec) Importance of lymph node ratio for locoregional recurrence of squamous cell carcinoma of the buccal mucosa. Head neck 39(12):2488–2493
Massano J, Regateiro FS, Januario G et al (2006) Oral squamous cell carcinoma: review of prognostic and predictive factors. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 102:67–76
Almangush A, Bello IO, Keski-Säntti H et al (2014) Depth of invasion, tumor budding, and worst pattern of invasion: prognostic indicators in early-stage oral tongue cancer. Head Neck 36(6):811–818
Angadi PV, Patil PV, Hallikeri K et al (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
Brandwein–Gensler A, 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 Surg Pathol 29:167–178
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
Hori Y, Kubota A, Yokose T et al (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
Bryne M, Koppang HS, Lilleng R et al (1992) Malignancy grading of the deep invasive margins of oral squamous cell carcinomas has high prognostic value. J Pathol 166:375–381
Chatterjee D, Bansal V, Malik V et al 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. 2019Aug; 98(7):E112-E119
Nadaf A, Bavle RM, Soumya M et al (2016) Analysis of the invasive edge in primary and secondary oral squamous cell carcinoma: An independent prognostic marker: A retrospective study. J Oral Maxillofac Pathol 20:239–245
Li Y, Bai S, Carroll W et al (2013) Validation of the risk model: high-risk classification and tumor pattern of invasion predict outcome for patients with low-stage oral cavity squamous cell carcinoma. Head Neck Pathol 7(3):211–223
D’Cruz AK, Vaish R, Kapre N et al (2015) Elective versus therapeutic neck dissection in node-negative Oral cancer. N Engl J Med 373:521–529
Schilling C, Stoeckli SJ, Haerle SK et al (2015) Sentinel European Node Trial (SENT): 3-year results of sentinel node biopsy in oral cancer. Eur J Cancer 51:2777–2784
Hiratsuka H, Miyakawa A, Nakamori K et al (1997) Multivariate analysis of occult lymph node metastasis as a prognostic indicator for patients with squamous cell carci- noma of the oral cavity. Cancer 80(3):351–356
Arora A, Husain N, Bansal A et al (2017) Development of a new out- come prediction model in early-stage squamous cell carcinoma of the oral cavity based on histopathologic parameters with multi- variate analysis: the Aditi-Nuzhat Lymph-Node Prediction Score (ANLPS) system. Am J Surg Pathol 41(7):950–960
Chen YW, Yu EH, Wu TH et al Histopathological factors affecting nodal metastasis in tongue cancer: analysis of 94 patients in Taiwan.Int J Oral Maxillofac Surg. 2008Oct; 37(10):912–6
Wu K, Wei J, Liu Z, Yu B et al Can pattern and depth of invasion predict lymph node relapse and prognosis in tongue squamous cell carcinoma.BMC Cancer. 2019 Jul19;19(1):714
Byers RM, Bland KI, Borlase B et al (1978) The prognostic and therapeutic value of frozen section determination in the surgical treatment of squamous cell carcinoma of the head and neck. Am J Surg 136:525–528
Jacobs JR, Ahmad K, Casiano R et al (1993) Implications of positive surgical margins. Laryngoscope 103:64–68
Loree TR, Strong EW (1990) Significance of positive margins in oral cavity squamous carcinoma. Am J Surg 160:410–414
Dunkel J, Vaittinen S, Grénman R et al (2013 Oct) Prognostic markers in stage I oral cavity squamous cell carcinoma. Laryngoscope 123(10):2435–2441
Thomas B, Stedman M, Davies L (2014 Mar) Grade as a prognostic factor in oral squamous cell carcinoma: a population-based analysis of the data. Laryngoscope 124(3):688–694
Hubert Low TH, Gao K, Elliott M, Clark JR (2015 Feb) Tumor classification for early oral cancer: re-evaluate the current TNM classification. Head Neck 37(2):223–228
Chang AM, Kim SW, Duvvuri U, Johnson JT et al (2013 Nov) Early squamous cell carcinoma of the oral tongue: comparing margins obtained from the glossectomy specimen to margins from the tumor bed. Oral Oncol 49(11):1077–1082
Lundqvist L, Stenlund H, Laurell G, Nylander K (2012 May) The importance of stromal inflammation in squamous cell carcinoma of the tongue. J Oral Pathol Med 41(5):379–383
Bello IO, Vered M, Dayan D et al (2011) Cancer-associated fibroblasts, a parameter of the tumor microenvironment, overcomes carcinoma-associated parameters in the prognosis of patients with mobile tongue cancer. Oral Oncol 47:33–38
Bryne M, Koppang HS, Lilleng R et al (1989) New malignancy grading is a better prognostic indicator than Broders’ grading in oral squamous cell carcinomas. J Oral Pathol Med 18:432–437
Brandwein-GenslerM SmithRV (2010) Validation of the histological Risk Model in a new patient cohort with primary head and neck squamous cell carcinoma. Am J Surg Pathol 34:676–688
Manjula BV, Augustine S, Selvam S et al (2015 Mar) 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(Suppl 1):98–104
Abu-Ghanem S, Yehuda M, Carmel NN et al (2016) Elective Neck Dissection vs Observation in Early-Stage Squamous Cell Carcinoma of the Oral Tongue With No Clinically Apparent Lymph Node Metastasis in the Neck: A Systematic Review and Meta-analysis. JAMA Otolaryngol Head Neck Surg. Sep 1;142(9):857 – 65
Fakih AR, Rao RS, Borges AM, Patel AR (1989) Elective versus therapeutic neck dissection in early carcinoma of the oral tongue. Am J Surg 158(4):309–313
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Ronald Anto: Research And Study Design, Data Collection & Analysis, Interpretation And Conclusion, Preparation Of Manuscrip, Review of Manuscript, Critical Revision
Ronald Anto: Research And Study Design, Data Collection & Analysis, Interpretation And Conclusion, Preparation Of Manuscrip, Review of Manuscript, Critical Revision
Meera Thomas: Data Collection & Analysis, Interpretation And Conclusion, Review of Manuscript
Amit Jiwan Tirkey: Research And Study Design, Interpretation And Conclusion, Preparation Of Manuscrip, Review of Manuscript, Critical Revision
Jeyasanth Riju: Data Collection & Analysis, Preparation Of Manuscrip
Shruthi Patil: Data Collection & Analysis, Preparation Of Manuscrip
Subhan Bhandari: Data Collection & Analysis
Reka: Data Collection & Analysis, Interpretation And Conclusion, Review of Manuscript
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Anto, R., Vidya, K., Thomas, M. et al. Worst Pattern of Invasion as an Independent Predictor of Lymph node Metastasis and Prognosis in oral Cavity Squamous cell carcinoma – A Retrospective Cohort Study. Indian J Otolaryngol Head Neck Surg 75, 440–449 (2023). https://doi.org/10.1007/s12070-022-03193-z
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DOI: https://doi.org/10.1007/s12070-022-03193-z