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Volume-based 18F-fluorodeoxyglucose positron emission tomography/computed tomography parameters correlate with delayed neck metastasis in clinical early-stage oral squamous cell carcinoma

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Abstract

Objective

There is no known preoperative marker that can effectively predict the risk of delayed neck metastasis (DNM), which is an important factor that determines the prognosis of early-stage oral cancer. In this study, we examined whether 18F-fluorodeoxyglucose positron emission tomography (18F-FDG-PET)/computed tomography (CT) uptake parameters of primary cancer can predict the risk of DNM in early-stage oral squamous cell carcinoma (OSCC).

Methods

Data from patients with stage I–II OSCC who underwent surgical resection of the primary tumor without elective neck dissection between January 2009 and December 2016 were retrospectively reviewed. Patient characteristics, histopathological factors, and PET/CT parameters (maximum standardized uptake value [SUVmax], metabolic tumor volume [MTV], and total lesion glycolysis [TLG]) were evaluated for their association with DNM. DNM rates were calculated, and the parameters that were statistically significant in the univariate analysis were used as explanatory variables. Independent factors associated with DNM were identified using multivariate analysis. For all statistical analyses, p-values < 0.05 were considered statistically significant.

Results

Data from 71 patients were analyzed in the study. The overall DNM rate among all patients was 21.8%. The univariate analysis showed that the T classification, depth of invasion, pattern of invasion, lymphovascular invasion, SUVmax, MTV, and TLG were significant predictors of DNM. However, the multivariate analysis revealed that only the depth of invasion, MTV, and TLG were independent predictors of DNM.

Conclusion

This study suggests that, in addition to conventional predictors, volume-based PET parameters are useful predictors of DNM in those with early-stage OSCC.

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Data availability

The data that support the findings of this study are available from the corresponding author on request. The data are not publicly available due to privacy or ethical restrictions.

References

  1. Palme CE, Gullane PJ, Gilbert RW. Current treatment options in squamous cell carcinoma of the oral cavity. Surg Oncol Clin N Am. 2004;13:47–70. https://doi.org/10.1016/S1055-3207(03)00123-6.

    Article  PubMed  Google Scholar 

  2. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108. https://doi.org/10.3322/caac.21262.

    Article  PubMed  Google Scholar 

  3. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: Globocan 2008. Int J Cancer. 2010;127:2893–917. https://doi.org/10.1002/ijc.25516.

    Article  PubMed  Google Scholar 

  4. Fisch U. Lymphographic studies on the cervical lymphatic system. Fortschr Hals Nasen Ohrenheilkd. 1966;14:1–196.

    PubMed  Google Scholar 

  5. da Silva SD, Hier M, Mlynarek A, Kowalski LP, Alaoui-Jamali MA. Recurrent oral cancer: current and emerging therapeutic approaches. Front Pharmacol. 2012;3:149. https://doi.org/10.3389/fphar.2012.00149.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Shah JP. Cervical lymph node metastases–diagnostic, therapeutic, and prognostic implications. Oncology (Williston Park). 1990;4:61–9.

    PubMed  Google Scholar 

  7. D’Cruz AK, Vaish R, Kapre N, Dandekar M, Gupta S, Hawaldar R, et al. Elective versus therapeutic neck dissection in node-negative oral cancer. N Engl J Med. 2015;373:521–9. https://doi.org/10.1056/NEJMoa1506007.

    Article  PubMed  Google Scholar 

  8. Shah JP, Gil Z. Current concepts in management of oral cancer–surgery. Oral Oncol. 2009;45:394–401. https://doi.org/10.1016/j.oraloncology.2008.05.017.

    Article  PubMed  Google Scholar 

  9. Chaukar D, Dandekar M, Kane S, Arya S, Purandare N, Rangarajan V, et al. Relative value of ultrasound, computed tomography and positron emission tomography imaging in the clinically node-negative neck in oral cancer. Asia Pac J Clin Oncol. 2016;12:e332–8. https://doi.org/10.1111/ajco.12255.

    Article  PubMed  Google Scholar 

  10. Capote A, Escorial V, Muñoz-Guerra MF, Rodríguez-Campo FJ, Gamallo C, Naval L. Elective neck dissection in early-stage oral squamous cell carcinoma—does it influence recurrence and survival? Head Neck. 2007;29:3–11. https://doi.org/10.1002/hed.20482.

    Article  PubMed  Google Scholar 

  11. Dias FL, Kligerman J, Matos de Sá G, Arcuri RA, Freitas EQ, Farias T, et al. Elective neck dissection versus observation in stage I squamous cell carcinomas of the tongue and floor of the mouth. Otolaryngol Head Neck Surg. 2001;125:23–29, doi: https://doi.org/10.1067/mhn.2001.116188

  12. Pimenta Amaral TMP, Da Silva Freire AR, Carvalho AL, Pinto CA, Kowalski LP. Predictive factors of occult metastasis and prognosis of clinical stages I and II squamous cell carcinoma of the tongue and floor of the mouth. Oral Oncol. 2004;40:780–6. https://doi.org/10.1016/j.oraloncology.2003.10.009.

    Article  PubMed  Google Scholar 

  13. Thiele OC, Seeberger R, Flechtenmacher C, Hofele C, Freier K. The role of elective supraomohyoidal neck dissection in the treatment of early, node-negative oral squamous cell carcinoma (OSCC): a retrospective analysis of 122 cases. J Craniomaxillofac Surg. 2012;40:67–70. https://doi.org/10.1016/j.jcms.2011.02.001.

    Article  PubMed  Google Scholar 

  14. Smith GI, O’Brien CJ, Clark J, Shannon KF, Clifford AR, McNeil EB, et al. Management of the neck in patients with T1 and T2 cancer in the mouth. Br J Oral Maxillofac Surg. 2004;42:494–500. https://doi.org/10.1016/j.bjoms.2004.06.013.

    Article  PubMed  Google Scholar 

  15. Andersen PE, Cambronero E, Shaha AR, Shah JP. The extent of neck disease after regional failure during observation of the N0 neck. Am J Surg. 1996;172:689–91. https://doi.org/10.1016/s0002-9610(96)00290-5.

    Article  PubMed  Google Scholar 

  16. Brandwein-Gensler M, Teixeira MS, Lewis CM, Lee B, Rolnitzky L, Hille JJ, et al. 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. 2005;29:167–78. https://doi.org/10.1097/01.pas.0000149687.90710.21.

    Article  PubMed  Google Scholar 

  17. Jakobsson PA, Eneroth CM, Killander D, Moberger G, Mårtensson B. Histologic classification and grading of malignancy in carcinoma of the larynx. Acta Radiol Ther Phys Biol. 1973;12:1–8. https://doi.org/10.3109/02841867309131085.

    Article  PubMed  Google Scholar 

  18. Anneroth G, Batsakis J, Luna M. Review of the literature and a recommended system of malignancy grading in oral squamous cell carcinomas. Scand J Dent Res. 1987;95:229–49. https://doi.org/10.1111/j.1600-0722.1987.tb01836.x.

    Article  PubMed  Google Scholar 

  19. Martínez-Gimeno C, Rodríguez EM, Vila CN, Varela CL. Squamous cell carcinoma of the oral cavity: a clinicopathologic scoring system for evaluating risk of cervical lymph node metastasis. Laryngoscope. 1995;105:728–33. https://doi.org/10.1288/00005537-199507000-00011.

    Article  PubMed  Google Scholar 

  20. Almangush A, Bello IO, Keski-Säntti H, Mäkinen LK, Kauppila JH, Pukkila M, et al. Depth of invasion, tumor budding, and worst pattern of invasion: prognostic indicators in early-stage oral tongue cancer. Head Neck. 2014;36:811–8. https://doi.org/10.1002/hed.23380.

    Article  PubMed  Google Scholar 

  21. Huang SH, Hwang D, Lockwood G, Goldstein DP, O’Sullivan B. Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies. Cancer. 2009;115:1489–97. https://doi.org/10.1002/cncr.24161.

    Article  PubMed  Google Scholar 

  22. Yamakawa N, Kirita T, Umeda M, Yanamoto S, Ota Y, Otsuru M, et al. Tumor budding and adjacent tissue at the invasive front correlate with delayed neck metastasis in clinical early-stage tongue squamous cell carcinoma. J Surg Oncol. 2019;119:370–8. https://doi.org/10.1002/jso.25334.

    Article  PubMed  Google Scholar 

  23. Kirita T, Yamakawa N, Ueda N, Yagyuu T. Tumor budding as a useful prognostic indicator in early oral squamous cell carcinoma. J Cancer Sci. 2018;10:162–7. https://doi.org/10.4172/1948-5956.1000536.

    Article  Google Scholar 

  24. Phelps ME, Huang SC, Hoffman EJ, Selin C, Sokoloff L, Kuhl DE. Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method. Ann Neurol. 1979;6:371–88. https://doi.org/10.1002/ana.410060502.

    Article  PubMed  Google Scholar 

  25. Kato H, Kuwano H, Nakajima M, Miyazaki T, Yoshikawa M, Ojima H, et al. Comparison between positron emission tomography and computed tomography in the use of the assessment of esophageal carcinoma. Cancer. 2002;94:921–8. https://doi.org/10.1002/cncr.10330.

    Article  PubMed  Google Scholar 

  26. Daisne JF, Duprez T, Weynand B, Lonneux M, Hamoir M, Reychler H, et al. Tumor volume in pharyngolaryngeal squamous cell carcinoma: comparison at CT, MR imaging, and FDG PET and validation with surgical specimen. Radiology. 2004;233:93–100. https://doi.org/10.1148/radiol.2331030660.

    Article  PubMed  Google Scholar 

  27. Ozawa Y, Hara M, Shibamoto Y, Tamaki T, Nishio M, Omi K. Utility of high-definition FDG-PET image reconstruction for lung cancer staging. Acta Radiol. 2013;54:916–20. https://doi.org/10.1177/0284185113488578.

    Article  PubMed  Google Scholar 

  28. Zhang H, Seikaly H, Biron VL, Jeffery CC. Utility of PET-CT in detecting nodal metastasis in cN0 early stage oral cavity squamous cell carcinoma. Oral Oncol. 2018;80:89–92. https://doi.org/10.1016/j.oraloncology.2018.04.003.

    Article  PubMed  Google Scholar 

  29. Sun R, Tang X, Yang Y, Zhang C. (18)FDG-PET/CT for the detection of regional nodal metastasis in patients with head and neck cancer: a meta-analysis. Oral Oncol. 2015;51:314–20. https://doi.org/10.1016/j.oraloncology.2015.01.004.

    Article  PubMed  Google Scholar 

  30. Allal AS, Dulguerov P, Allaoua M, Haenggeli CA, El-Ghazi EA, Lehmann W, et al. Standardized uptake value of 2-[(18)F] fluoro-2-deoxy-D-glucose in predicting outcome in head and neck carcinomas treated by radiotherapy with or without chemotherapy. J Clin Oncol. 2002;20:1398–404. https://doi.org/10.1200/JCO.2002.20.5.1398.

    Article  PubMed  Google Scholar 

  31. Wong RJ, Lin DT, Schöder H, Patel SG, Gonen M, Wolden S, et al. Diagnostic and prognostic value of [(18)F]fluorodeoxyglucose positron emission tomography for recurrent head and neck squamous cell carcinoma. J Clin Oncol. 2002;20:4199–208. https://doi.org/10.1200/JCO.2002.02.590.

    Article  PubMed  Google Scholar 

  32. Minn H, Lapela M, Klemi PJ, Grénman R, Leskinen S, Lindholm P, et al. Prediction of survival with fluorine-18-fluoro-deoxyglucose and PET in head and neck cancer. J Nucl Med. 1997;38:1907–11.

    PubMed  Google Scholar 

  33. Shimomura H, Sasahira T, Yamanaka Y, Kurihara M, Imai Y, Tamaki S, et al. [18F]fluoro-2-deoxyglucose-positron emission tomography for the assessment of histopathological response after preoperative chemoradiotherapy in advanced oral squamous cell carcinoma. Int J Clin Oncol. 2015;20:308–16. https://doi.org/10.1007/s10147-014-0711-5.

    Article  PubMed  Google Scholar 

  34. Halfpenny W, Hain SF, Biassoni L, Maisey MN, Sherman JA, McGurk M. FDG-PET. A possible prognostic factor in head and neck cancer. Br J Cancer, 2002;86:512–516, doi: https://doi.org/10.1038/sj.bjc.6600114

  35. Querellou S, Abgral R, Le Roux PY, Nowak E, Valette G, Potard G, et al. Prognostic value of fluorine-18 fluorodeoxyglucose positron-emission tomography imaging in patients with head and neck squamous cell carcinoma. Head Neck. 2012;34:462–8. https://doi.org/10.1002/hed.21765.

    Article  PubMed  Google Scholar 

  36. Paidpally V, Chirindel A, Lam S, Agrawal N, Quon H, Subramaniam RM. FDG-PET/CT imaging biomarkers in head and neck squamous cell carcinoma. Imaging Med. 2012;4:633–47. https://doi.org/10.2217/iim.12.60.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Abd El-Hafez YG, Moustafa HM, Khalil HF, Liao CT, Yen TC. Total lesion glycolysis: a possible new prognostic parameter in oral cavity squamous cell carcinoma. Oral Oncol. 2013;49:261–8. https://doi.org/10.1016/j.oraloncology.2012.09.005.

    Article  PubMed  Google Scholar 

  38. Lim R, Eaton A, Lee NY, Setton J, Ohri N, Rao S, et al. 18F-FDG PET/CT metabolic tumor volume and total lesion glycolysis predict outcome in oropharyngeal squamous cell carcinoma. J Nucl Med. 2012;53:1506–13. https://doi.org/10.2967/jnumed.111.101402.

    Article  PubMed  Google Scholar 

  39. Moon SH, Choi JY, Lee HJ, Son YI, Baek CH, Ahn YC, et al. Prognostic value of 18F-FDG PET/CT in patients with squamous cell carcinoma of the tonsil: comparisons of volume-based metabolic parameters. Head Neck. 2013;35:15–22. https://doi.org/10.1002/hed.22904.

    Article  PubMed  Google Scholar 

  40. Murphy JD, Chisholm KM, Daly ME, Wiegner EA, Truong D, Iagaru A, et al. Correlation between metabolic tumor volume and pathologic tumor volume in squamous cell carcinoma of the oral cavity. Radiother Oncol. 2011;101:356–61. https://doi.org/10.1016/j.radonc.2011.05.040.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Schinagl DA, Span PN, Oyen WJ, Kaanders JH. Can FDG PET predict radiation treatment outcome in head and neck cancer? Results of a prospective study. Eur J Nucl Med Mol Imaging. 2011;38:1449–58. https://doi.org/10.1007/s00259-011-1789-x.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Ryu IS, Kim JS, Roh JL, Cho KJ, Choi SH, Nam SY, et al. Prognostic significance of preoperative metabolic tumour volume and total lesion glycolysis measured by (18)F-FDG PET/CT in squamous cell carcinoma of the oral cavity. Eur J Nucl Med Mol Imaging. 2014;41:452–61. https://doi.org/10.1007/s00259-013-2571-z.

    Article  PubMed  Google Scholar 

  43. Hutchison IL, Ridout F, Cheung SMY, Shah N, Hardee P, Surwald C, et al. Nationwide randomised trial evaluating elective neck dissection for early stage oral cancer (SEND study) with meta-analysis and concurrent real-world cohort. Br J Cancer. 2019;121:827–36. https://doi.org/10.1038/s41416-019-0587-2.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Cao Y, Wang T, Yu C, Guo X, Li C, Li L. Elective neck dissection versus wait-and-watch policy for oral cavity squamous cell carcinoma in early stage: A systematic review and meta-analysis based on survival data. J Oral Maxillofac Surg. 2019;77:2154–67. https://doi.org/10.1016/j.joms.2019.03.015.

    Article  PubMed  Google Scholar 

  45. Bello IO, Soini Y, Salo T. Prognostic evaluation of oral tongue cancer: means, markers and perspectives (I). Oral Oncol. 2010;46:630–5. https://doi.org/10.1016/j.oraloncology.2010.06.006.

    Article  PubMed  Google Scholar 

  46. Regezi JA, Sciubba JJ, Jordan RCK. Oral pathology: clinical, pathologic correlations. 5th ed. St Louis (MO): Saunders Elsevier; 2008

  47. Kim KH, Lee J, Chang JS, Lee CG, Yun M, Choi EC, et al. Prognostic value of FDG-PET volumetric parameters in patients with p16-positive oropharyngeal squamous cell carcinoma who received curative resection followed by postoperative radiotherapy or chemoradiotherapy. Head Neck. 2016;38:1515–24. https://doi.org/10.1002/hed.24465.

    Article  PubMed  Google Scholar 

  48. Schwartz DL, Harris J, Yao M, Rosenthal DI, Opanowski A, Levering A, et al. Metabolic tumor volume as a prognostic imaging-based biomarker for head-and-neck cancer: pilot results from Radiation Therapy Oncology Group protocol 0522. Int J Radiat Oncol Biol Phys. 2015;91:721–9. https://doi.org/10.1016/j.ijrobp.2014.12.023.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Abgral R, Valette G, Robin P, Rousset J, Keromnes N, Le Roux PY, et al. Prognostic evaluation of percentage variation of metabolic tumor burden calculated by dual-phase (18) FDG PET-CT imaging in patients with head and neck cancer. Head Neck. 2016;38(Suppl 1):E600–6. https://doi.org/10.1002/hed.24048.

    Article  PubMed  Google Scholar 

  50. Yamamoto E, Kohama G, Sunakawa H, Iwai M, Hiratsuka H. Mode of invasion, bleomycin sensitivity, and clinical course in squamous cell carcinoma of the oral cavity. Cancer. 1983;51:2175–80. https://doi.org/10.1002/1097-0142(19830615)51:12%3c2175::aid-cncr2820511205%3e3.0.co;2-m.

    Article  PubMed  Google Scholar 

  51. Kimura S, Nanbu U, Noguchi H, Harada Y, Kumamoto K, Sasaguri Y, et al. Macrophage CCL22 expression in the tumor microenvironment and implications for survival in patients with squamous cell carcinoma of the tongue. J Oral Pathol Med. 2019;48:677–85. https://doi.org/10.1111/jop.12885.

    Article  PubMed  Google Scholar 

  52. Kaihara T, Kusaka T, Kawamata H, Oda Y, Fujii S, Morita K, et al. Decreased expression of E-cadherin and Yamamoto-Kohama’s mode of invasion highly correlates with lymph node metastasis in esophageal squamous cell carcinoma. Pathobiology. 2001;69:172–8. https://doi.org/10.1159/000048772.

    Article  PubMed  Google Scholar 

  53. Weiss MH, Harrison LB, Isaacs RS. Use of decision analysis in planning a management strategy for the stage N0 neck. Arch Otolaryngol Head Neck Surg. 1994;120:699–702. https://doi.org/10.1001/archotol.1994.01880310005001.

    Article  PubMed  Google Scholar 

  54. Dünne AA, Müller HH, Eisele DW, Kessel K, Moll R, Werner JA. Meta-analysis of the prognostic significance of perinodal spread in head and neck squamous cell carcinomas (HNSCC) patients. Eur J Cancer. 2006;42:1863–8. https://doi.org/10.1016/j.ejca.2006.01.062.

    Article  PubMed  Google Scholar 

  55. da Silva SD, Morand GB, Alobaid FA, Hier MP, Mlynarek AM, Alaoui-Jamali MA, et al. Epithelial-mesenchymal transition (EMT) markers have prognostic impact in multiple primary oral squamous cell carcinoma. Clin Exp Metastasis. 2015;32:55–63. https://doi.org/10.1007/s10585-014-9690-1.

    Article  PubMed  Google Scholar 

  56. Huber GF, Fritzsche FR, Züllig L, Storz M, Graf N, Haerle SK, et al. Podoplanin expression correlates with sentinel lymph node metastasis in early squamous cell carcinomas of the oral cavity and oropharynx. Int J Cancer. 2011;129:1404–9. https://doi.org/10.1002/ijc.25795.

    Article  PubMed  Google Scholar 

  57. Huber GF, Züllig L, Soltermann A, Roessle M, Graf N, Haerle SK, et al. Down regulation of E-cadherin (ECAD) – a predictor for occult metastatic disease in sentinel node biopsy of early squamous cell carcinomas of the oral cavity and oropharynx. BMC Cancer. 2011;11(217):1–8. https://doi.org/10.1186/1471-2407-11-217.

    Article  Google Scholar 

  58. Shinohara S, Kikuchi M, Suehiro A, Kishimoto I, Harada H. Is 18F-fluorodeoxyglucose positron emission tomography/computed tomography helpful in the decision-making process for neck dissection in patients with T1–T2 lingual cancer? Acta Otolaryngol. 2015;135:181–6. https://doi.org/10.3109/00016489.2014.975894.

    Article  PubMed  Google Scholar 

  59. Morand GB, Vital DG, Kudura K, Werner J, Stoeckli SJ, Huber GF, et al. Maximum Standardized Uptake Value (SUVmax) of primary tumor predicts occult neck metastasis in oral cancer. Sci Rep. 2018;8:11817. https://doi.org/10.1038/s41598-018-30111-7.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Brun E, Kjellén E, Tennvall J, Ohlsson T, Sandell A, Perfekt R, et al. FDG PET studies during treatment: prediction of therapy outcome in head and neck squamous cell carcinoma. Head Neck. 2002;24:127–35. https://doi.org/10.1002/hed.10037.

    Article  PubMed  Google Scholar 

  61. Machtay M, Natwa M, Andrel J, Hyslop T, Anne PR, Lavarino J, et al. Pretreatment FDG-PET standardized uptake value as a prognostic factor for outcome in head and neck cancer. Head Neck. 2009;31:195–201. https://doi.org/10.1002/hed.20942.

    Article  PubMed  Google Scholar 

  62. Kurokawa H, Yamashita Y, Takeda S, Zhang M, Fukuyama H, Takahashi T. Risk factors for late cervical lymph node metastases in patients with stage I or II carcinoma of the tongue. Head Neck. 2002;24:731–6. https://doi.org/10.1002/hed.10130.

    Article  PubMed  Google Scholar 

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Acknowledgements

We acknowledge the support of Dr. Yuu Tanaka from the Department of Rehabilitation, Faculty of Health Science, Wakayama Professional University of Rehabilitation for assistance with statistical analyses. We wish to thank Editage (http://www.editage.jp/) for English-language editing.

Funding

This study did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Nobuhiro Yamakawa and Tadaaki Kirita contributed to the study conception and design. Material preparation and data collection were performed by Yohei Nakayama, Nobuhiro Ueda, and Takahiro Yagyuu. Analyses were performed by Nobuhiro Yamakawa and Shigehiro Tamaki. The first draft of the manuscript was written by Nobuhiro Yamakawa and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Nobuhiro Yamakawa.

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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. The study protocol was approved by the Ethics Committee of Nara Medical University (approval number: 2339).

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Informed consent was waived by the local Ethics Committee of Nara Medical University in view of the retrospective nature of the study.

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Yamakawa, N., Nakayama, Y., Ueda, N. et al. Volume-based 18F-fluorodeoxyglucose positron emission tomography/computed tomography parameters correlate with delayed neck metastasis in clinical early-stage oral squamous cell carcinoma. Oral Radiol 39, 668–682 (2023). https://doi.org/10.1007/s11282-023-00686-7

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