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Research

Squamous Cell Carcinoma Tumor Ecology & Microenvironment (STEM) Working Group

STEM Working Group Leadership

Adam Luginbuhl, MD
Director, STEM Working Group
Joseph Curry, MD
Co-Director, STEM Working Group

Collaborative Bibliography

  • Johnson JM, Vathiotis IA, Harshyne LA, Ali A, Bar Ad V, Axelrod R, Lorber E, Curry J, Cognetti DM, Luginbuhl AJ, Tuluc M, Keith S, Mahoney MG, Argiris A. Nivolumab and ipilimumab in combination with radiotherapy in patients with high-risk locally advanced squamous cell carcinoma of the head and neck. J Immunother Cancer. 2023 Aug;11(8):e007141. doi: 10.1136/jitc-2023-007141.
  • Hill BL, Calder AN, Flemming JP, Guo Y, Gilmore SL, Trofa MA, Daniels SK, Nielsen TN, Gleason LK, Antysheva Z, Demina K, Kotlov N, Davitt CJH, Cognetti DM, Prendergast GC, Snook AE, Johnson JM, Kumar G, Linnenbach AJ, Martinez-Outschoorn U, South AP, Curry JM, Harshyne LA, Luginbuhl AJ, Mahoney MG. IL-8 correlates with nonresponse to neoadjuvant nivolumab in HPV positive HNSCC via a potential extracellular vesicle miR-146a mediated mechanism. Mol Carcinog. 2023 Sep;62(9):1428-1443. doi: 10.1002/mc.23587. Epub 2023 Jul 4. PMID: 37401875.Ali AS, Manukian G, Johnson JM, Vathiotis I, Axelrod R, Keith SW, Curry J, Cognetti D, Luginbuhl A, Argiris A, Bar-Ad V. In-Field Toxicity Analysis of a Phase 1 Clinical Trial of Nivolumab and Ipilimumab With Definitive Radiation Therapy in Locally Advanced Squamous Cell Carcinoma of the Head and Neck. Int J Radiat Oncol Biol Phys. 2023 Apr 3:S0360-3016(23)00309-7. PMID: 37019367.
  • Crist M, Yaniv B, Palackdharry S, Lehn MA, Medvedovic M, Stone T, Gulati S, Karivedu V, Borchers M, Fuhrman B, Crago A, Curry J, Martinez-Outschoorn U, Takiar V, Wise-Draper TM. Metformin increases natural killer cell functions in head and neck squamous cell carcinoma through CXCL1 inhibition. J Immunother Cancer. 2022 Nov;10(11):e005632. PMID: 36328378;.
  • Ali AS, Manukian G, Johnson JM, Vathiotis I, Axelrod R, Keith SW, Curry J, Cognetti D, Luginbuhl A, Argiris A, Bar-Ad V. In-Field Toxicity Analysis of a Phase 1 Clinical Trial of Nivolumab and Ipilimumab With Definitive Radiation Therapy in Locally Advanced Squamous Cell Carcinoma of the Head and Neck. Int J Radiat Oncol Biol Phys. 2023 Sep 1;117(1):181-185. PMID: 37019367.
  • Vadigepalli R, Linnenbach A, Harshyne L, South AP, Curry J, Martinez-Outshoorn U, Mahoney, Luginbuhl A. Systems Dynamic Modeling of Tumor Microenvironment in Head and Neck Squamous Cell Carcinoma. JAMA Otolaryngology – Head and Neck Surgery.  Abstract for the 11th International Conference on Head and Neck Cancer/American Head and Neck Society. Montreal QC 2023.
  • Curry J, Alnemri A, Philips R, Fiorella M, Sussman S, Stapp R, Solomides C, Harshyne L, South A, Luginbuhl A, Tuluc M, Martinez-Outschoorn U, Argiris A, Linnenbach A, Johnson J. CD8+ and FoxP3+ T-Cell Cellular Density and Spatial Distribution After Programmed Death-Ligand 1 Check Point Inhibition. Laryngoscope. 2023 Aug;133(8):1875-1884. PMID: 36125263.
  • Obradovic A, Graves D, Korrer M, Wang Y, Roy S, Naveed A, Xu Y, Luginbuhl A, Curry J, Gibson M, Idrees K, Hurley P, Jiang P, Liu XS, Uppaluri R, Drake CG, Califano A, Kim YJ. Immunostimulatory Cancer-Associated Fibroblast Subpopulations Can Predict Immunotherapy Response in Head and Neck Cancer. Clin Cancer Res. 2022 May 13;28(10):2094-2109. doi: 10.1158/1078-0432.CCR-21-3570. PMID: 35262677; PMCID: PMC9161438.
  • Swendseid B, Philips RHW, Carey RM, Cannady SB, Sweeny L, Wax MK, Luginbuhl AJ, Curry JM. Postoperative analysis of osseous midface reconstructions: The value of imaging and a novel scoring system for complexity and operative success. Head Neck. 2023 Jan;45(1):237-242. doi: 10.1002/hed.27228. Epub 2022 Oct 27. PMID: 36300998; PMCID: PMC10092237.
  • Sussman S, Philips R, Renslo B, Givens A, Swendseid B, Tassone P, Goldman RA, Curry JM, Cognetti DM, Luginbuhl AJ. Effects of Prior Tracheostomy on Total Laryngectomy Outcomes. Otolaryngol Head Neck Surg. 2023 Apr;168(4):782-789. doi: 10.1177/01945998221116761. Epub 2023 Jan 28. PMID: 35943815.
  • Crist M, Yaniv B, Palackdharry S, Lehn MA, Medvedovic M, Stone T, Gulati S, Karivedu V, Borchers M, Fuhrman B, Crago A, Curry J, Martinez-Outschoorn U, Takiar V, Wise-Draper TM. Metformin increases natural killer cell functions in head and neck squamous cell carcinoma through CXCL1 inhibition. J Immunother Cancer. 2022 Nov;10(11):e005632. doi: 10.1136/jitc-2022-005632. PMID: 36328378; PMCID: PMC9639146.
  • Curry J, Alnemri A, Philips R, Fiorella M, Sussman S, Stapp R, Solomides C, Harshyne L, South A, Luginbuhl A, Tuluc M, Martinez-Outschoorn U, Argiris A, Linnenbach A, Johnson J. CD8+ and FoxP3+ T-Cell Cellular Density and Spatial Distribution After Programmed Death-Ligand 1 Check Point Inhibition. Laryngoscope. 2022 Sep 20. doi: 10.1002/lary.30389. Epub ahead of print. PMID: 36125263.
  • Vathiotis IA, Johnson JM, Luginbuhl A, Cognetti D, Curry J, Argiris A. Programmed cell death protein 1 axis blockade in locally advanced squamous cell carcinoma of the head and neck: Neoadjuvant and adjuvant approaches. Cancer Treat Rev. 2022 Sep;109:102437. doi: 10.1016/j.ctrv.2022.102437. Epub 2022 Jul 16. PMID: 35868194.
  • Luginbuhl AJ, South AP. Understanding precancerous lesions of the oral cavity. J Pathol. 2022 Oct;258(2):103-105. doi: 10.1002/path.5993. Epub 2022 Aug 16. PMID: 35894839.
  • Domingo-Vidal M, Whitaker-Menezes D, Mollaee M, Lin Z, Tuluc M, Philp N, Johnson JM, Zhan T, Curry J, Martinez-Outschoorn U. Monocarboxylate Transporter 4 in Cancer-Associated Fibroblasts Is a Driver of Aggressiveness in Aerodigestive Tract Cancers. Front Oncol. 2022 Jun 22;12:906494. doi: 10.3389/fonc.2022.906494. PMID: 35814364; PMCID: PMC9259095.
  • Luginbuhl AJ, Johnson JM, Harshyne LA, Linnenbach AJ, Shukla SK, Alnemri A, Kumar G, Cognetti DM, Curry JM, Kotlov N, Antysheva Z, Degryse S, Mannion K, Gibson MK, Netterville J, Brown B, Axelrod R, Zinner R, Tuluc M, Gargano S, Leiby BE, Shimada A, Mahoney MG, Martinez-Outschoorn U, Rodeck U, Kim YJ, South AP, Argiris A. Tadalafil enhances immune signatures in response to neoadjuvant nivolumab in resectable head and neck squamous cell carcinoma. Clin Cancer Res. 2022 Mar 1; 28(5): 915-927. doi: 10.1158/1078-0432.CCR-21-1816.  PubMed PMID: 34911681.
  • Luginbuhl A, Calder A, Kutler D, Zender C, Wise-Draper T, Patel J, Cheng M, Karivedu V, Zhan T, Parashar B, Gulati S, Yao M, Lavertu P, Takiar V, Tang A, Johnson J, Keane W, Curry J, Cognetti D, Bar-Ad V. Multi-Institutional Study Validates Safety of Intraoperative Cesium-131 Brachytherapy for Treatment of Recurrent Head and Neck Cancer. Front Oncol. 2021;11:786216. doi: 10.3389/fonc.2021.786216. eCollection 2021. PubMed PMID: 34900741; PubMed Central PMCID: PMC8660666
  • Cognetti DM, Johnson JM, Curry JM, Kochuparambil ST, McDonald D, Mott F, Fidler MJ, Stenson K, Vasan NR, Razaq MA, Campana J, Ha P, Mann G, Ishida K, Garcia-Guzman M, Biel M, Gillenwater AM. Phase 1/2a, open-label, multicenter study of RM-1929 photoimmunotherapy in patients with locoregional, recurrent head and neck squamous cell carcinoma. Head Neck. 2021 Dec;43(12):3875-3887. doi: 10.1002/hed.26885. Epub 2021 Oct 9. PMID: 34626024.
  • Ryan WR, Xu MJ, Ochoa E, Plonowska-Hirschfeld KA, Zebolsky AL, Ha PK, Bewley AF, Mallen-St Clair J, Joshi AS, Coffey CS, Faraji F, MacDonald BV, Houlton JJ, Gobillot TA, Curry JM, Philips R, Hackman TG, Richmon JD, Holcomb AJ, Coughlin AM, Panwar A, Smith RB, Herberg ME, Fakhry C, Cognetti DM. Oncologic outcomes of human papillomavirus-associated oropharynx carcinoma treated with surgery alone: A 12-institution study of 344 patients. Cancer. 2021 Sep 1;127(17):3092-3106. doi: 10.1002/cncr.33611. Epub 2021 May 6. PMID: 33957701.
  • Gaurav Kumar, Andrew P. South, Joseph M. Curry, Alban Linnenbach, Larry A Harshyne, Adam Ertel, Paolo Fortina, Adam Luginbuhl. Multimodal genomic markers predict immunotherapy response in the head and neck squamous cell carcinoma. bioRxiv 2021
  • Patel J, den Breems NY, Tuluc M, Johnson J, Curry JM, South AP, Cho RJ. Elevated APOBEC mutational signatures implicate chronic injury in etiology of an aggressive head-and-neck squamous cell carcinoma: a case report. J Med Case Rep. 2021 Apr 30;15(1):252. doi: 10.1186/s13256-021-02685-w. PMID: 33926553; PMCID: PMC8086066.
  • Flemming JP, Hill BL, Anderson-Pullinger L, Harshyne LA, Mahoney MG. Cytokine Profiling in Low- and High-Density Small Extracellular Vesicles from Epidermoid Carcinoma Cells. JID Innov. 2021 Aug 24;1(4):100053. doi: 10.1016/j.xjidi.2021.100053. PMID: 34909749; PMCID: PMC8659799.
  • Luginbuhl AJ, Hobelmann K, Rodin J, Shukla S, Rodeck U, Linnenbach A. Synthetic Triterpenoid RTA-408: Limits Radiation Damage to Normal Tissue. Laryngoscope. 2021 Oct 28;. doi: 10.1002/lary.29930. [Epub ahead of print] PubMed PMID: 34709651.
  • Philips R, Agarwal A, Chitguppi C, Swendseid B, Graf A, Murphy K, Jangro W, Rhodes L, Toskala E, Luginbuhl A, Curry J, Nyquist G, Rosen M, Johnson J, Rabinowitz M. Quality of Life Outcomes in Patients With Sinonasal Malignancy After Definitive Treatment. Laryngoscope. 2021 Jul;131(7):E2212-E2221. doi: 10.1002/lary.29339. Epub 2020 Dec 25. PubMed PMID: 33368340.
  • Philips R, Han C, Swendseid B, Curry J, Argiris A, Luginbuhl A, Johnson J. Preoperative Immunotherapy in the Multidisciplinary Management of Oral Cavity Cancer. Front Oncol. 2021;11:682075. doi: 10.3389/fonc.2021.682075. eCollection 2021. Review. PubMed PMID: 34277428; PubMed Central PMCID: PMC8281120.
  • Sagheer SH, Whitaker-Menezes D, Han JYS, Curry JM, Martinez-Outschoorn U, Philp NJ. 4NQO induced carcinogenesis: A mouse model for oral squamous cell carcinoma. Methods Cell Biol. 2021;163:93-111. doi: 10.1016/bs.mcb.2021.01.001. Epub 2021 Mar 4. PMID: 33785171.
  • Knops AM, South A, Rodeck U, Martinez-Outschoorn U, Harshyne LA, Johnson J, Luginbuhl AJ, Curry JM. Cancer-Associated Fibroblast Density, Prognostic Characteristics, and Recurrence in Head and Neck Squamous Cell Carcinoma: A Meta-Analysis. Front Oncol. 2020 Nov 27;10:565306. doi: 10.3389/fonc.2020.565306. PMID: 33330034; PMCID: PMC7729160.
  • Merlino DJ, Johnson JM, Tuluc M, Gargano S, Stapp R, Harshyne L Jr, Leiby BE, Flanders A, Zinner R, Axelrod R, Curry J, Cognetti DM, Mannion K, Kim YJ, Rodeck U, Argiris A, Luginbuhl AJ. Discordant Responses Between Primary Head and Neck Tumors and Nodal Metastases Treated With Neoadjuvant Nivolumab: Correlation of Radiographic and Pathologic Treatment Effect. Frontiers in Oncology. 2020;10:566315. doi: 10.3389/fonc.2020.566315. 
  • Roden DF, Hobelmann K, Vimawala S, Richa T, Fundakowski CE, Goldman R, Luginbuhl A, Curry JM, Cognetti DM. Evaluating the impact of smoking on disease-specific survival outcomes in patients with human papillomavirus-associated oropharyngeal cancer treated with transoral robotic surgery. Cancer. 2020 Jan 1;126(9):1873-1887.
  • Amin D, Richa T, Mollaee M, Zhan T, Tassone P, Johnson J, Luginbuhl A, Cognetti D, Martinez-Outschoorn U, Stapp R, Solomides C, Rodeck U, Curry J. Metformin Effects on FOXP3+ and CD8+ T Cell Infiltrates of Head and Neck Squamous Cell Carcinoma. Laryngoscope. 2020 Sep;130(9):E490-E498. doi: 10.1002/lary.28336
  • Flemming JP, Hill BL, Haque MW, Raad J, Bonder CS, Harshyne LA, Rodeck U, Luginbuhl A, Wahl JK 3rd, Tsai KY, Wermuth PJ, Overmiller AM, Mahoney MG. miRNA- and cytokine-associated extracellular vesicles mediate squamous cell carcinomas. J Extracell Vesicles. 2020 Jul 13;9(1):1790159. doi: 10.1080/20013078.2020.1790159. PubMed PMID: 32944178.
  • Luginbuhl A, Johnson J, Harshyne L, Tuluc M, Mardekian S, Leiby B, Curry J, Cognetti D, Kim Y, Mannion K, Rodeck U, Argiris A. Discordant treatment response in primary tumors and lymph node metastases after four weeks of preoperative PD-1 blockade in head and neck squamous cell carcinoma (HNSCC). Journal of Clinical Oncology 37, no. 15_suppl (May 20, 2019) 6016-6016.
  • Luginbuhl A, Johnson J, Harshyne L, Tuluc M, Mardekian S, Leiby B, Curry J, Cognetti D, Kim Y, Mannion K, Rodeck U, Argiris A. A Window of opportunity trial of preoperative nivolumab with or without tadalafil in squamous cell carcinoma of the head and neck (SCCHN):  Safety, clinical and correlative outcomes. Annals of Oncology, Volume 30. 2019, October 1.
  • South AP, den Breems NY, Richa T, Nwagu U, Zhan T, Poojan S, Martinez-Outschoorn U, Johnson JM, Luginbuhl AJ, Curry JM. Mutation signature analysis identifies increased mutation caused by tobacco smoke associated DNA adducts in larynx squamous cell carcinoma compared with oral cavity and oropharynx. Sci Rep. 2019 Dec 17;9(1):19256. doi: 10.1038/s41598-019-55352-y. PubMed PMID: 31848367
  • Domingo-Vidal M, Whitaker-Menezes D, Martos-Rus C, Tassone P, Snyder CM, Tuluc M, Philp N, Curry J, Martinez-Outschoorn U . Cigarette Smoke Induces Metabolic Reprogramming of the Tumor Stroma in Head and Neck Squamous Cell Carcinoma. Mol Cancer Res. 2019 Sep;17(9):1893-1909. doi: 10.1158/1541-7786.MCR-18-1191.
  • Roden D, Daniels K, Metkus J, Goldman R, Walsh A, Johnson J, Hamilton J, Keane W, Chapman A, Bar-Ad V, Sweeny L, Curry J, Cognetti D, Luginbuhl A. Evaluation of oncologic outcomes in head and neck cancer patients ≥80 years old based on adherence to NCCN guideline for postoperative adjuvant treatment. Head Neck. 2019 Dec;41(12):4128-4135. doi: 10.1002/hed.25950. 
  • Daniels KE, Luginbuhl AJ, Mardekian SK, Cognetti DM, Curry JM, South AP. Assessment of quality and consistency of monoclonal antibodies for CB1 and CB2 in head and neck squamous cell carcinoma. Head Neck. 2019 Sep;41(9):3105-3113. doi: 10.1002/hed.25794. 
  • Kumar AT, Knops A, Swendseid B, Martinez-Outschoom U, Harshyne L, Philp N, Rodeck U, Luginbuhl A, Cognetti D, Johnson J, Curry J. Prognostic Significance of Tumor-Associated Macrophage Content in Head and Neck Squamous Cell Carcinoma: A Meta-Analysis. Front Oncol. 2019;9:656.  doi: 10.3389/fonc.2019.00656. 
  • Topf MC, Harshyne L, Tuluc M, Mardekian S, Vimawala S, Cognetti DM, Curry JM, Rodeck U, Luginbuhl A. Loss of CD169+ Subcapsular Macrophages during Metastatic Spread of Head and Neck Squamous Cell Carcinoma. Otolaryngol Head Neck Surg. 2019 Jul;161(1):67-73. doi: 10.1177/0194599819829741.
  • Curry JM, Johnson J, Mollaee M, Tassone P, Amin D, Knops A, Whitaker-Menezes D, Mahoney MG, South A, Rodeck U, Zhan T, Harshyne L, Philp N, Luginbuhl A, Cognetti D, Tuluc M, Martinez-Outschoorn U. Metformin Clinical Trial in HPV+ and HPV- Head and Neck Squamous Cell Carcinoma: Impact on Cancer Cell Apoptosis and Immune Infiltrate. Front Oncol. 2018;8:436. doi: 10.3389/fonc.2018.00436. 
  • Bisetto S, Whitaker-Menezes D, Wilski NA, Tuluc M, Curry J, Zhan T, Snyder CM, Martinez-Outschoorn UE, Philp NJ. Front Monocarboxylate Transporter 4 (MCT4) Knockout Mice Have Attenuated 4NQO Induced Carcinogenesis; A Role for MCT4 in Driving Oral Squamous Cell Cancer. Front Oncol. 2018 Aug 28;8:324. doi: 10.3389/fonc.2018.00324
  • Wilde L, Tanson K, Curry J, Martinez-Outschoorn U. Autophagy in cancer: a complex relationship. Biochem J. 2018 Jun 11;475(11):1939-1954. doi: 10.1042/BCJ20170847.
  • Tassone P, Domingo-Vidal M, Whitaker-Menezes D, Lin Z, Roche M, Tuluc M, Martinez-Outschoorn U, Curry J. Metformin Effects on Metabolic Coupling and Tumor Growth in Oral Cavity Squamous Cell Carcinoma Coinjection Xenografts..Otolaryngol Head Neck Surg. 2018 May;158(5):867-877. doi: 10.1177/0194599817746934.
  • Curry J, Tassone P, Gill K, Tuluc M, BarAd V, Mollaee M, Whitaker-Menezes D, Rodeck U, Luginbuhl A, Cognetti D, Keane W, Martinez-Outschoorn U.Tumor Metabolism in the Microenvironment of Nodal Metastasis in Oral Squamous Cell Carcinoma. Otolaryngol Head Neck Surg. 2017 Nov;157(5):798-807. doi: 10.1177/0194599817709224. 
  • Ko YH, Domingo-Vidal M, Roche M, Lin Z, Whitaker-Menezes D, Seifert E, Capparelli C, Tuluc M, Birbe RC, Tassone P, Curry JM, Navarro-Sabaté À, Manzano A, Bartrons R, Caro J, Martinez-Outschoorn U TP53-inducible Glycolysis and Apoptosis Regulator (TIGAR) Metabolically Reprograms Carcinoma and Stromal Cells in Breast Cancer. .J Biol Chem. 2016 Dec 16;291(51):26291-26303. doi: 10.1074/jbc.M116.740209.
  • Overmiller AM, Pierluissi JA, Wermuth PJ, Sauma S, Martinez-Outschoorn U, Tuluc M, Luginbuhl A, Curry J, Harshyne LA, Wahl JK 3rd, South AP, Mahoney MG. Desmoglein 2 modulates extracellular vesicle release from squamous cell carcinoma keratinocytes. FASEB J. 2017 Aug;31(8):3412-3424. doi: 10.1096/fj.201601138RR. 
  • Curry J, Johnson J, Tassone P, Vidal MD, Menezes DW, Sprandio J, Mollaee M, Cotzia P, Birbe R, Lin Z, Gill K, Duddy E, Zhan T, Leiby B, Reyzer M, Cognetti D, Luginbuhl A, Tuluc M, Martinez-Outschoorn U. Metformin effects on head and neck squamous carcinoma microenvironment: Window of opportunity trial. Laryngoscope. 2017 Aug;127(8):1808-1815. doi: 10.1002/lary.26489. Epub 2017 Feb 10. PubMed PMID: 28185288;
  • Topf MC, Tuluc M, Harshyne LA, Luginbuhl A. Macrophage type 2 differentiation in a patient with laryngeal squamous cell carcinoma and metastatic prostate adenocarcinoma to the cervical lymph nodes. J Immunother Cancer. 2017 Jul 18;5(1):60. doi: 10.1186/s40425-017-0264-z. PubMed PMID: 28716144;
  • Wilde L, Roche M, Domingo-Vidal M, Tanson K, Philp N, Curry J, Martinez-Outschoorn U, Metabolic coupling and the Reverse Warburg Effect in cancer: Implications for novel biomarker and anticancer agent development. Semin Oncol. 2017 Jun;44(3):198-203. doi: 10.1053/j.seminoncol.2017.10.004.
  •  Languino LR, Singh A, Prisco M, Inman GJ, Luginbuhl A, Curry JM, South AP. Exosome-mediated transfer from the tumor microenvironment increases TGFβ signaling in squamous cell carcinoma. Am J Transl Res. 2016 May 15;8(5):2432-7.
  • Curry JM, Tassone P, Cotzia P, Sprandio J, Luginbuhl A, Cognetti DM, Mollaee M, Domingo M, Pribitkin EA, Keane WM, Zhan TT, Birbe R, Tuluc M, Martinez-Outschoorn U. Multicompartment metabolism in papillary thyroid cancer. Laryngoscope. 2016 Oct;126(10):2410-2418. doi: 10.1002/lary.25799. Epub 2015 Dec 15. PubMed PMID: 26666958;
  • Bovenzi CD, Hamilton J, Tassone P, Johnson J, Cognetti DM, Luginbuhl A, Keane WM, Zhan T, Tuluc M, Bar-Ad V, Martinez-Outschoorn U, Curry JM.Prognostic Indications of Elevated MCT4 and CD147 across Cancer Types: A Meta-Analysis. Biomed Res Int. 2015;2015:242437. doi: 10.1155/2015/242437. 
  • Curry JM, Tuluc M, Whitaker-Menezes D, Ames JA, Anantharaman A, Butera A, Leiby B, Cognetti DM, Sotgia F, Lisanti MP, Martinez-Outschoorn UE. Cancer metabolism, stemness and tumor recurrence: MCT1 and MCT4 are functional biomarkers of metabolic symbiosis in head and neck cancer. Cell Cycle. 2013 May 1;12(9):1371-84. doi: 10.4161/cc.24092. 

 

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