Multicenter study on tumor budding in lung squamous cell carcinoma: comparison between biopsy and resection with interobserver variability assessment.

Maillard, Marie; Neppl, Christina; Zens, Philipp; Anex, Julie; Peters, Solange; Krueger, Thorsten; Berezowska, Sabina (2024). Multicenter study on tumor budding in lung squamous cell carcinoma: comparison between biopsy and resection with interobserver variability assessment. (In Press). Modern pathology, 37(10), p. 100571. Elsevier 10.1016/j.modpat.2024.100571

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Grading lung squamous cell carcinoma (LUSC) is controversial and not universally accepted. The histomorphological feature of tumor budding (TB) is an established independent prognostic factor in colorectal cancer and its importance is growing in other solid cancers, making it a candidate for inclusion in tumor grading schemes. We aimed to compare TB between preoperative biopsies and resection specimens in pulmonary squamous cell carcinoma and assess interobserver variability. A retrospective cohort of 249 consecutive patients primarily resected with LUSC in Bern (2000-2013, N=136) and Lausanne (2005-2020 N=113) with available preoperative biopsies was analyzed for TB and additional histomorphological parameters such as spread through airspaces (STAS) and desmoplasia by two expert pathologists. Results were correlated with clinicopathological parameters and survival. In resection specimens, peritumoral budding (PTB) score was low (0-4 buds/0.785 mm2) in 47.6%, intermediate (5-9 buds/0.785 mm2) in 27.4 %, and high (≥10 buds/0.785 mm2) in 25 % of cases (median bud count = 5, IQR = 0 - 26). Both the absolute number of buds and TB score were similar when comparing tumor edge and intratumoral zone (p=0.192) but significantly different from the score obtained in the biopsy (p<0.001). Interobserver variability was moderate, regardless of score location (Cohen's kappa 0.59). The discrepant cases were reassessed, and consensus was reached in all cases with identification of causes of discordance. TB score was significantly associated with stage (p=0.002), presence of lymph node (p=0.033) and distant metastases (p=0.020), without significant correlation with overall survival, tumor size or pleural invasion. Desmoplasia was significantly associated with higher PTB (p<0.001). STAS was present in 34% and associated with lower PTB (p<0.001). To conclude, despite confirming TB as a reproductible factor in LUSC we disclose areas of scoring ambiguity. Preoperative biopsy evaluation was insufficient in establishing the final tumor budding score of the resected tumor.

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