Abstract
Background
The prognostic value of nutritional status in anaplastic thyroid carcinoma (ATC) remains unclear. The Prognostic Nutritional Index (PNI) is a reliable indicator of overall nutritional and immune status, and it has emerged as a significant prognostic factor in various malignancies. This study aimed to explore the utility of PNI in ATC.
Methods
We systematically reviewed ATC patients in our institute from January 2000 to June 2023 and categorized them into high and low PNI groups based on the median PNI value. Kaplan–Meier analysis and Cox regression were employed to assess the impact of PNI on overall survival, while ROC curve analysis evaluated the predictive value of PNI. Mimics software was used for three-dimensional reconstruction of pre- and post-immunotherapy tumor volumes, enabling the assessment of treatment response.
Results
A total of 77 ATC patients were included in this study. Low baseline PNI was associated with significantly shorter overall survival (1-year survival rate: 5.26% vs 30.77%; median survival time: 5.30 months vs 8.87 months). The 1-year, 2-year, and 3-year AUC values for PNI were 0.82, 0.79, and 0.77, respectively. In the multivariate analysis, both PNI and tumor size emerged as independent prognostic factors for patient overall survival. Among ATC patients receiving 2–3 cycles of immunotherapy, an increase in post-treatment PNI levels was positively correlated with a reduction in tumor volume.
Conclusion
PNI is an independent predictor of overall survival and holds the potential to serve as a valuable indicator for assessing and predicting immunotherapy efficacy in ATC patients.
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References
K.C. Bible, E. Kebebew, J. Brierley, J.P. Brito, M.E. Cabanillas, T.J. Clark Jr et al. 2021 American Thyroid Association guidelines for management of patients with anaplastic thyroid cancer. Thyroid 31(3), 337–86 (2021)
R.I. Haddad, C. Nasr, L. Bischoff, N.L. Busaidy, D. Byrd, G. Callender et al. NCCN guidelines insights: thyroid carcinoma, version 2.2018. J. Natl Compr. Cancer Netw. 16(12), 1429–1440 (2018)
S.N. Rao, R.C. Smallridge, Anaplastic thyroid cancer: an update. Best Pract. Res. Clin. Endocrinol. Metab. 37(1), 101678 (2023)
A. Maniakas, R. Dadu, N.L. Busaidy, J.R. Wang, R. Ferrarotto, C. Lu et al. Evaluation of overall survival in patients with anaplastic thyroid carcinoma, 2000–2019. JAMA Oncol. 6(9), 1397–1404 (2020)
V. Subbiah, R.J. Kreitman, Z.A. Wainberg, J.Y. Cho, J.H.M. Schellens, J.C. Soria et al. Dabrafenib and trametinib treatment in patients with locally advanced or metastatic BRAF V600-mutant anaplastic thyroid cancer. J. Clin. Oncol. 36(1), 7–13 (2018)
J. Capdevila, L.J. Wirth, T. Ernst, S. Ponce Aix, C.C. Lin, R. Ramlau et al. PD-1 blockade in anaplastic thyroid carcinoma. J. Clin. Oncol. 38(23), 2620–2627 (2020)
P. Cotogni, S. Stragliotto, M. Ossola, A. Collo, S. Riso; On Behalf Of The Intersociety Italian Working Group For Nutritional Support In C, The role of nutritional support for cancer patients in palliative care. Nutrients 13(2), 306 (2021)
P. Schuetz, S. Sulo, S. Walzer, S. Krenberger, C. Brunton, Nutritional support during the hospital stay is cost-effective for preventing adverse outcomes in patients with cancer. Front. Oncol. 12, 916073 (2022)
M. Tajan, K.H. Vousden, Dietary approaches to cancer therapy. Cancer Cell 37(6), 767–785 (2020)
Y. Zhang, X. Zhang, Controlling nutritional status score, a promising prognostic marker in patients with gastrointestinal cancers after surgery: a systematic review and meta-analysis. Int. J. Surg. 55, 39–45 (2018)
T. Onodera, N. Goseki, G. Kosaki, [Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients]. Nihon Geka Gakkai Zasshi 85(9), 1001–1005 (1984)
M. Mantzorou, A. Koutelidakis, S. Theocharis, C. Giaginis, Clinical value of nutritional status in cancer: what is its impact and how it affects disease progression and prognosis? Nutr. Cancer 69(8), 1151–1176 (2017)
P. Johannet, A. Sawyers, Y. Qian, S. Kozloff, N. Gulati, D. Donnelly et al. Baseline prognostic nutritional index and changes in pretreatment body mass index associate with immunotherapy response in patients with advanced cancer. J. Immunother. Cancer 8(2), e001674 (2020)
Y. Oku, G. Toyokawa, S. Wakasu, F. Kinoshita, S. Takamori, K. Watanabe et al. Impact of the pretreatment prognostic nutritional index on the survival after first-line immunotherapy in non-small-cell lung cancer patients. Cancer Med. 12(13), 14327–14336 (2023)
J. Ahn, E. Song, H.S. Oh, D.E. Song, W.G. Kim, T.Y. Kim et al. Low lymphocyte-to-monocyte ratios are associated with poor overall survival in anaplastic thyroid carcinoma patients. Thyroid 29(6), 824–829 (2019)
Z. Zhang, L. Xiong, Z. Wu, H. Liu, K. Ning, Y. Peng et al. Neoadjuvant combination of pazopanib or axitinib and programmed cell death protein-1-activated dendritic cell-cytokine-induced killer cells immunotherapy may facilitate surgery in patients with renal cell carcinoma. Transl. Androl. Urol. 10(5), 2091–2102 (2021)
S.G. Yeo, D.Y. Kim, T.H. Kim, K.H. Jung, Y.S. Hong, H.J. Chang et al. Tumor volume reduction rate measured by magnetic resonance volumetry correlated with pathologic tumor response of preoperative chemoradiotherapy for rectal cancer. Int. J. Radiat. Oncol. Biol. Phys. 78(1), 164–171 (2010)
P.C. Iyer, R. Dadu, M. Gule-Monroe, N.L. Busaidy, R. Ferrarotto, M.A. Habra et al. Salvage pembrolizumab added to kinase inhibitor therapy for the treatment of anaplastic thyroid carcinoma. J. Immunother. Cancer 6(1), 68 (2018)
X. Zhang, L. Pang, S.V. Sharma, R. Li, A.G. Nyitray, B.J. Edwards, Malnutrition and overall survival in older patients with cancer. Clin. Nutr. 40(3), 966–977 (2021)
J. Arends, Struggling with nutrition in patients with advanced cancer: nutrition and nourishment-focusing on metabolism and supportive care. Ann. Oncol. 29(suppl_2), ii27–ii34 (2018).
Z. Jiao, C. Liang, G. Luo, M. Liu, K. Jiang, A. Yang et al. Prognostic utility of nutritional risk index in patients with head and neck soft tissue sarcoma. Nutrients 15(3), 641 (2023)
M.E. Hamaker, F. Oosterlaan, L.H. van Huis, N. Thielen, A. Vondeling, F. van den Bos, Nutritional status and interventions for patients with cancer—A systematic review. J. Geriatr. Oncol. 12(1), 6–21 (2021)
L. Peng, Y. Wang, F. Liu, X. Qiu, X. Zhang, C. Fang et al. Peripheral blood markers predictive of outcome and immune-related adverse events in advanced non-small cell lung cancer treated with PD-1 inhibitors. Cancer Immunol. Immunother. 69(9), 1813–1822 (2020)
X. Wang, Y. Wang, The prognostic nutritional index is prognostic factor of gynecological cancer: a systematic review and meta-analysis. Int. J. Surg. 67, 79–86 (2019)
V. Jaspan, K. Lin, V. Popov, The impact of anthropometric parameters on colorectal cancer prognosis: a systematic review and meta-analysis. Crit. Rev. Oncol. Hematol. 159, 103232 (2021)
A. Jannin, A. Escande, A. Al Ghuzlan, P. Blanchard, D. Hartl, B. Chevalier et al. Anaplastic thyroid carcinoma: an update. Cancers 14(4), 1061 (2022)
C. Dierks, J. Seufert, K. Aumann, J. Ruf, C. Klein, S. Kiefer et al. Combination of lenvatinib and pembrolizumab is an effective treatment option for anaplastic and poorly differentiated thyroid carcinoma. Thyroid 31(7), 1076–1085 (2021)
A. Hatashima, B. Archambeau, H. Armbruster, M. Xu, M. Shah, B. Konda et al. An evaluation of clinical efficacy of immune checkpoint inhibitors for patients with anaplastic thyroid carcinoma. Thyroid 32(8), 926–936 (2022)
S. Hamidi, P.C. Iyer, R. Dadu, M.K. Gule-Monroe, A. Maniakas, M.E. Zafereo et al. Checkpoint inhibition in addition to dabrafenib/trametinib for BRAF(V600E)-mutated anaplastic thyroid carcinoma. Thyroid 34(3), 336–346 (2024)
A. Garcia-Alvarez, J. Hernando, A. Carmona-Alonso, J. Capdevila, What is the status of immunotherapy in thyroid neoplasms? Front. Endocrinol. 13, 929091 (2022)
I. Landa, T. Ibrahimpasic, L. Boucai, R. Sinha, J.A. Knauf, R.H. Shah et al. Genomic and transcriptomic hallmarks of poorly differentiated and anaplastic thyroid cancers. J. Clin. Investig. 126(3), 1052–1066 (2016)
P. Adam, S. Kircher, I. Sbiera, V.F. Koehler, E. Berg, T. Knösel et al. FGF-receptors and PD-L1 in anaplastic and poorly differentiated thyroid cancer: evaluation of the preclinical rationale. Front. Endocrinol. 12, 712107 (2021)
M. Guller, M. Herberg, N. Amin, H. Alkhatib, C. Maroun, E. Wu et al. Nutritional status as a predictive biomarker for immunotherapy outcomes in advanced head and neck cancer. Cancers 13(22), 5772 (2021)
R.N. Amaria, M. Postow, E.M. Burton, M.T. Tetzlaff, M.I. Ross, C. Torres-Cabala et al. Neoadjuvant relatlimab and nivolumab in resectable melanoma. Nature 611(7934), 155–160 (2022)
M. Chalabi, L.F. Fanchi, K.K. Dijkstra, J.G. Van den Berg, A.G. Aalbers, K. Sikorska et al. Neoadjuvant immunotherapy leads to pathological responses in MMR-proficient and MMR-deficient early-stage colon cancers. Nat. Med. 26(4), 566–576 (2020)
N. Prasongsook, A. Kumar, A.V. Chintakuntlawar, R.L. Foote, J. Kasperbauer, J. Molina et al. Survival in response to multimodal therapy in anaplastic thyroid cancer. J. Clin. Endocrinol. Metab. 102(12), 4506–4514 (2017)
Y. Nachalon, S. Stern-Shavit, G. Bachar, J. Shvero, D. Limon, A. Popovtzer, Aggressive palliation and survival in anaplastic thyroid carcinoma. JAMA Otolaryngol. Head Neck Surg. 141(12), 1128–1132 (2015)
T.A. Pezzi, A.S.R. Mohamed, T. Sheu, P. Blanchard, V.C. Sandulache, S.Y. Lai et al. Radiation therapy dose is associated with improved survival for unresected anaplastic thyroid carcinoma: outcomes from the national cancer data base. Cancer 123(9), 1653–1661 (2017)
S.S. Wu, E.D. Lamarre, A. Yalamanchali, P.R. Brauer, H. Hong, C.A. Reddy et al. Association of treatment strategies and tumor characteristics with overall survival among patients with anaplastic thyroid cancer: a single-institution 21-year experience. JAMA Otolaryngol. Head Neck Surg. 149(4), 300–309 (2023)
D.C. McMillan, W.S. Watson, P. O’Gorman, T. Preston, H.R. Scott, C.S. McArdle, Albumin concentrations are primarily determined by the body cell mass and the systemic inflammatory response in cancer patients with weight loss. Nutr. Cancer 39(2), 210–213 (2001)
Acknowledgements
We would like to thank the Information Department of Sun Yat-sen University Cancer Center for providing us with help in reviewing patient clinical data.
Funding
This study was supported by the National Natural Science Foundation of China (Nos. 82072981, 82272649, 82303881), Guangdong Basic and Applied Basic Research Foundation (Nos. 2023A1515010450, 2023A1515012903, 2022A1515110033), and Open Project Fund of the Sixth Affiliated Hospital of Guangzhou Medical University (No. 202011-201).
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Yongchao Yu: Conceptualization, Methodology, Writing—original draft, Visualization. Kang Ning: Visualization, Software, Formal analysis. Guangfeng Luo: Methodology, Formal analysis. Lexuan Hong: Software, Validation. Yarong Liang: Validation. Xinyu Liu: Validation. Zan Jiao: Resources. Tong Wu: Resources. Zhongyuan Yang: Investigation. Mingjie Jiang: Writing—review & editing, Validation. Weichao Chen: Writing—review & editing, Validation. Ankui Yang: Supervision, Writing—review & editing.
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Yu, Y., Ning, K., Liu, X. et al. Effectiveness of prognostic nutritional index in predicting overall survival and evaluating immunotherapy response in anaplastic thyroid carcinoma. Endocrine (2024). https://doi.org/10.1007/s12020-024-03826-z
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DOI: https://doi.org/10.1007/s12020-024-03826-z