Skip to main content

Distant metastasis from oral cavity—correlation between histopathology results and primary site

Abstract

Objectives

Oral cancer is the eighth most common type of cancer worldwide and a significant contributor to the global burden caused by this disease. The principal parameters considered to influence prognosis, and thus treatment selection, are size and location of the primary tumor, as well as assessment of the presence and extent of lymph node and distant metastasis (DM). However, no known report regarding the relationship between the primary site and DM has been presented. For effective treatment selection and good prognosis, the correlation of DM with anatomic site and histopathology results of the primary malignancy is important. In the present study, we performed a systematic review of published reports in an effort to determine the relationship between the anatomic site of various types of oral cavity cancer and DM.

Methods

A systematic review of articles published until the end of 2018 was performed using PubMed/MEDLINE.

Results

A total of 150 studies were selected for this review. The percentage of all cases reported with DM was 6.3%, ranging from 0.6% to 33.1% in the individual studies. The rate of incidence of tongue occurrence was 9.3%. A frequent DM site was the lungs, with adenoid cystic carcinoma the most commonly involved histopathological factor. Malignant melanoma was most frequent (43.4%) in all histopathology findings, whereas there were no cases with an acinic cell carcinoma or cystadenocarcinoma.

Conclusions

We found that the occurrence of DM from the primary site as well as rate of incidence was dependent on histopathological factors.

This is a preview of subscription content, access via your institution.

References

  1. Petersen PE. Oral cancer prevention and control–the approach of the World Health Organization. Oral Oncol. 2009;45:454–60.

    PubMed  Google Scholar 

  2. Ong W, Zhao Z, Lui B, Tan W, Ebrahimi A, Clark JR, et al. Prognostic significance of lymph node density in squamous cell carcinoma of the tongue. Head Neck. 2016;38(1):E859–E866866.

    PubMed  Google Scholar 

  3. Patel SG, Amit M, Yen TC, Liao CT, Chaturvedi P, Agarwal JP, et al. Lymph node density in oral cavity cancer: results of the International Consortium for Outcomes Research. Br J Cancer. 2013;109:2087–95.

    PubMed  PubMed Central  Google Scholar 

  4. Monden N, Asakage T, Kiyota N, Homma A, Matsuura K, Hanai N, et al. A review of head and neck cancer staging system in the TNM classification of malignant tumors (eighth edition) Head and Neck Cancer Study Group (HNCSG) Japanese. J Clin Oncol. 2019;49(7):589–95.

    Google Scholar 

  5. Blatt S, Ziebart T, Krüger M, Pabst AM. Diagnosing oral squamous cell carcinoma: How much imaging do we really need? A review of the current literature. J Craniomaxillofac Surg. 2016;44(5):538–49.

    PubMed  Google Scholar 

  6. Alvi A, Johnson JT. Development of distant metastasis after treatment of advanced-stage head and neck cancer. Head Neck. 1997;19(6):500–5.

    PubMed  Google Scholar 

  7. Amit M, Yen TC, Liao CT, Chaturvedi P, Agarwal JP, Kowalski LP, et al. International Consortium for Outcome Research (ICOR) in Head and Neck Cancer. Improvement in survival of patients with oral cavity squamous cell carcinoma: an International Collaborative study. Cancer. 2013;119(24):4242–8.

    PubMed  Google Scholar 

  8. Ballard BR, Suess GR, Pickren JW, Greene GW Jr, Shedd DP. Squamous-cell carcinoma of the floor of the mouth. Oral Surg Oral Med Oral Pathol. 1978;45(4):568–79.

    PubMed  Google Scholar 

  9. Carlson ER, Ord RA. Vertebral metastases from oral squamous cell carcinoma. J Oral Maxillofac Surg. 2002;60(8):858–62.

    PubMed  Google Scholar 

  10. Chen TC, Hsu CW, Lou PJ, Ko JY, Yang TL, Chen CN, et al. The clinical predictive factors for subsequent distant metastasis in patients with locoregionally advanced oral squamous cell carcinoma. Oral Oncol. 2013;49(4):367–73.

    PubMed  Google Scholar 

  11. Crombie AK, Farah C, Tripcony L, Dickie G, Batstone MD. Primary chemoradiotherapy for oral cavity squamous cell carcinoma. Oral Oncol. 2012;48(10):1014–8.

    PubMed  Google Scholar 

  12. Davis MA, Tyrrell J, Slotman GJ, Sudhindra R, Sachdeva K, Fanelle J, et al. Southern New Jersey Head and Neck Cancer Treatment Network. Preoperative simultaneous fractionated cisplatin and radiation therapy in the treatment of advanced operable stage III and IV squamous cell carcinoma of the head and neck. Am J Surg. 2015;209(3):575–9.

    PubMed  Google Scholar 

  13. Visscher JG, van den Elsaker K, Grond AJ, van der Wal JE, van der Waal I. Surgical treatment of squamous cell carcinoma of the lower lip: evaluation of long-term results and prognostic factors a retrospective analysis of 184 patients. J Oral Maxillofac Surg. 1998;56(7):814–20.

    PubMed  Google Scholar 

  14. de Visscher JG, Grond AJ, Botke G, van der Waal I. Results of radiotherapy for squamous cell carcinoma of the vermilion border of the lower lip. A retrospective analysis of 108 patients. Radiother Oncol. 1996;39(1):9–14.

    PubMed  Google Scholar 

  15. Driemel O, Ettl T, Kölbl O, Reichert TE, Dresp BV, Reuther J, et al. Outcome and histopathologic regression in oral squamous cell carcinoma after preoperative radiochemotherapy. Strahlenther Onkol. 2009;185(5):296–302.

    PubMed  Google Scholar 

  16. Duan X, Chen H, Ma H, Song Y. The expression and significance of the HOXA7 gene in oral squamous cell carcinoma. J Oral Sci. 2017;59(3):329–35.

    PubMed  Google Scholar 

  17. Eich HT, Lschcke M, Scheer M, Kocher M, Bongartz R, Wacker S, et al. Neoadjuvant radiochemotherapy and radical resection for advanced squamous cell carcinoma of the oral cavity. Outcome of 134 patients. Strahlenther Onkol. 2008;184(1):23–9.

    PubMed  Google Scholar 

  18. Ellis ER, Mendenhall WM, Rao PV, Parsons JT, Spangler AE, Million RR. Does node location affect the incidence of distant metastases in head and neck squamous cell carcinoma? Int J Radiat Oncol Biol Phys. 1989;17(2):293–7.

    PubMed  Google Scholar 

  19. Ellis GL, Corio RL. Spindle cell carcinoma of the oral cavity. A clinicopathologic assessment of fifty-nine cases. Oral Surg Oral Med Oral Pathol. 1980;50(6):523–34.

    PubMed  Google Scholar 

  20. Ettl T, Driemel O, Dresp BV, Reichert TE, Reuther J, Pistner H. Feasibility of alloplastic mandibular reconstruction in patients following removal of oral squamous cell carcinoma. J Craniomaxillofac Surg. 2010;38(5):350–4.

    PubMed  Google Scholar 

  21. Faisal M, Abbas T, Khaleeq U, Adeel M, Anwer AW, Hussain R, et al. Treatment outcomes of rare retromolar trigone squamous cell carcinoma using combined modalities. Cureus. 2017;9(5):e1203. https://doi.org/10.7759/cureus.1203.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Fan L, Hu X, Lin S, Zhou W, Fu S, Lv H. Concurrent preoperative chemotherapy and three-dimensional conformal radiotherapy followed by surgery for oral squamous cell carcinoma: a retrospective analysis of 104 cases. Oncotarget. 2017;8(43):75557–67.

    PubMed  PubMed Central  Google Scholar 

  23. Fang KH, Kao HK, Cheng MH, Chang YL, Tsang NM, Huang YC, et al. Histological differentiation of primary oral squamous cell carcinomas in an area of betel quid chewing prevalence. Otolaryngol Head Neck Surg. 2009;141(6):743–9.

    PubMed  Google Scholar 

  24. Farnedi A, Rossi S, Bertani N, Gulli M, Silini EM, Mucignat MT, et al. Proteoglycan-based diversification of disease outcome in head and neck cancer patients identifies NG2/CSPG4 and syndecan-2 as unique relapse and overall survival predicting factors. BMC Cancer. 2015;15:352. https://doi.org/10.1186/s12885-015-1336-4.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Fazekas JT, Sommer C, Kramer S. Tumor regression and other prognosticators in advanced head and neck cancers: a sequel to the RTOG methotrexate study. Int J Radiat Oncol Biol Phys. 1983;9(7):957–64.

    PubMed  Google Scholar 

  26. Feng Z, Li JN, Li CZ, Guo CB. Elective neck dissection versus observation in the management of early tongue carcinoma with clinically node-negative neck: a retrospective study of 229 cases. J Craniomaxillofac Surg. 2014;42(6):806–10.

    PubMed  Google Scholar 

  27. Freier K, Engel M, Lindel K, Flechtenmacher C, Mühling J, Hassfeld S, et al. Neoadjuvant concurrent radiochemotherapy followed by surgery in advanced oral squamous cell carcinoma (OSCC): a retrospective analysis of 207 patients. Oral Oncol. 2008;44(2):116–23.

    PubMed  Google Scholar 

  28. Fritsch VA, Gerry DR, Lentsch EJ. Basaloid squamous cell carcinoma of the oral cavity: an analysis of 92 cases. Laryngoscope. 2014;124(7):1573–8.

    PubMed  Google Scholar 

  29. Garavello W, Ciardo A, Spreafico R, Gaini RM. Risk factors for distant metastases in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg. 2006;132(7):762–6.

    PubMed  Google Scholar 

  30. Geretschläger A, Bojaxhiu B, Crowe S, Arnold A, Manser P, Hallermann W, et al. Outcome and patterns of failure after postoperative intensity modulated radiotherapy for locally advanced or high-risk oral cavity squamous cell carcinoma. Radiat Oncol. 2012;22(7):175. https://doi.org/10.1186/1748-717X-7-175.

    Article  Google Scholar 

  31. Gontarz M, Wyszyńska-Pawelec G, Zapała J, Czopek J, Lazar A, Tomaszewska R. Immunohistochemical predictors in squamous cell carcinoma of the tongue and floor of the mouth. Head Neck. 2016;38(Suppl 1):E747–E753753.

    PubMed  Google Scholar 

  32. Grau JJ, Cuchi A, Traserra J, Frvida JL, Arias C, Blanch JL, et al. Follow-up study in head and neck cancer: cure rate according to tumor location and stage. Oncology. 1997;54(1):38–42.

    PubMed  Google Scholar 

  33. Greenberg JS, Fowler R, Gomez J, Mo V, Roberts D, El Naggar AK, et al. Extent of extracapsular spread: a critical prognosticator in oral tongue cancer. Cancer. 2003;97(6):1464–70.

    PubMed  Google Scholar 

  34. Grimm M. Prognostic value of clinicopathological parameters and outcome in 484 patients with oral squamous cell carcinoma: microvascular invasion (V+) is an independent prognostic factor for OSCC. Clin Transl Oncol. 2012;14(11):870–80.

    PubMed  Google Scholar 

  35. Grbe A, Blessmann M, Hanken H, Friedrich RE, Schn G, Wikner J, et al. Prognostic relevance of circulating tumor cells in blood and disseminated tumor cells in bone marrow of patients with squamous cell carcinoma of the oral cavity. Clin Cancer Res. 2014;20(2):425–33.

    Google Scholar 

  36. Gueiros LA, Coletta RD, Kowalski LP, Lopes MA. Clinicopathological features and proliferation markers in tongue squamous cell carcinomas. Int J Oral Maxillofac Surg. 2011;40(5):510–5.

    PubMed  Google Scholar 

  37. Gumusay O, Ozet A, Buyukberber S, Baykara M, Coskun U, Cetin B, et al. Factors predicting the development of distant metastases in patients with head and neck squamous cell carcinoma: a retrospective study from a single centre. J BUON. 2015;20(2):521–6.

    PubMed  Google Scholar 

  38. Hasegawa T, Tanakura M, Takeda D, Sakakibara A, Akashi M, Minamikawa T, et al. Risk factors associated with distant metastasis in patients with oral squamous cell carcinoma. Otolaryngol Head Neck Surg. 2015;152(6):1053–60.

    PubMed  Google Scholar 

  39. Ho HC, Lee MS, Hsiao SH, Hwang JH, Hung SK, Chou P, et al. Squamous cell carcinoma of the oral cavity in young patients: a matched-pair analysis. Eur Arch Otorhinolaryngol. 2008;265(Suppl 1):S57–61.

    PubMed  Google Scholar 

  40. Holm LE, Lundquist PG, Rudën BI, Silfverswärd C, Sobin A, Wersäll J. Combined preoperative radiotherapy and surgery in the treatment of carcinoma of the anterior two-thirds of the tongue. Laryngoscope. 1983;93(6):792–6.

    PubMed  Google Scholar 

  41. Honorato J, Rebelo MS, Dias FL, Camisasca DR, Faria PA, Azevedoe SG, et al. Gender differences in prognostic factors for oral cancer. Int J Oral Maxillofac Surg. 2015;44(10):1205–11.

    PubMed  Google Scholar 

  42. Hosni A, McMullen C, Huang SH, Xu W, Su J, Bayley A, et al. Lymph node ratio relationship to regional failure and distant metastases in oral cavity cancer. Radiother Oncol. 2017;124(2):225–31.

    PubMed  Google Scholar 

  43. Hosni A, Huang SH, Xu W, Su J, Bayley A, Bratman SV, et al. Distant Metastases following postoperative intensity-modulated radiotherapy for oral cavity squamous cell carcinoma. JAMA Otolaryngol Head Neck Surg. 2017;143(4):368–75.

    PubMed  Google Scholar 

  44. Huang C, Sun Z, Sun Y, Chen X, Zhu X, Fan C, et al. Association of increased ligand cyclophilin A and receptor CD147 with hypoxia, angiogenesis, metastasis and prognosis of tongue squamous cell carcinoma. Histopathology. 2012;60(5):793–803.

    PubMed  Google Scholar 

  45. Huang CF, Xu XR, Wu TF, Sun ZJ, Zhang WF. Correlation of ALDH1, CD44, OCT4 and SOX2 in tongue squamous cell carcinoma and their association with disease progression and prognosis. J Oral Pathol Med. 2014;43(7):492–8.

    PubMed  Google Scholar 

  46. Huang CG, Lee LA, Tsao KC, Liao CT, Yang LY, Kang CJ, et al. Human papillomavirus 16/18 E7 viral loads predict distant metastasis in oral cavity squamous cell carcinoma. J Clin Virol. 2014;61(2):230–6.

    PubMed  Google Scholar 

  47. Huang CH, Chu ST, Ger LP, Hou YY, Sun CP. Clinicopathologic evaluation of prognostic factors for squamous cell carcinoma of the buccal mucosa. J Chin Med Assoc. 2007;70(4):164–70.

    PubMed  Google Scholar 

  48. Imai R, Takenaka Y, Yasui T, Nakahara S, Yamamoto Y, Hanamoto A, et al. Prognostic significance of serum squamous cell carcinoma antigen in patients with head and neck cancer. Acta Otolaryngol. 2015;135(3):295–301.

    PubMed  Google Scholar 

  49. Imajyo I, Sugiura T, Kobayashi Y, Shimoda M, Ishii K, Akimoto N, et al. T-box transcription factor Brachyury expression is correlated with epithelial-mesenchymal transition and lymph node metastasis in oral squamous cell carcinoma. Int J Oncol. 2012;41(6):1985–95.

    PubMed  PubMed Central  Google Scholar 

  50. Jaafari-Ashkavandi Z, Khademi B, Akbari S, Malekzadeh M. Serum level of mast cell tryptase in patients with oral squamous cell carcinoma: lack of correlation with clinicopathologic factors. Asian Pac J Cancer Prev. 2013;14(5):2955–8.

    PubMed  Google Scholar 

  51. Jerjes W, Upile T, Hamdoon Z, Mosse CA, Akram S, Hopper C. Prospective evaluation of outcome after transoral CO(2) laser resection of T1/T2 oral squamous cell carcinoma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;112(2):180–7.

    PubMed  Google Scholar 

  52. Jerjes W, Upile T, Petrie A, Riskalla A, Hamdoon Z, Vourvachis M, et al. Clinicopathological parameters, recurrence, locoregional and distant metastasis in 115 T1–T2 oral squamous cell carcinoma patients. Head Neck Oncol. 2010;2:9. https://doi.org/10.1186/1758-3284-2-9.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Jian CX, Yang MZ, Li P, Xiong J, Zhang ZJ, Li CJ, et al. Ectopically expressed IBP promotes cell proliferation in oral squamous cell carcinoma. Cancer Invest. 2012;30(10):748–56.

    PubMed  Google Scholar 

  54. Jinno T, Kawano S, Maruse Y, Matsubara R, Goto Y, Sakamoto T, et al. Increased expression of interleukin-6 predicts poor response to chemoradiotherapy and unfavorable prognosis in oral squamous cell carcinoma. Oncol Rep. 2015;33(5):2161–8.

    PubMed  PubMed Central  Google Scholar 

  55. Kalnins IK, Leonard AG, Sako K, Razack MS, Shedd DP. Correlation between prognosis and degree of lymph node involvement in carcinoma of the oral cavity. Am J Surg. 1977;134(4):450–4.

    PubMed  Google Scholar 

  56. Kang CJ, Lin CY, Yang LY, Ho TY, Lee LY, Fan KH, et al. Positive clinical impact of an additional PET/CT scan before adjuvant radiotherapy or concurrent chemoradiotherapy in patients with advanced oral cavity squamous cell carcinoma. J Nucl Med. 2015;56(1):22–30.

    PubMed  Google Scholar 

  57. Kang CJ, Lin CY, Wang HM, Fan KH, Ng SH, Lee LY, et al. The number of pathologically positive lymph nodes and pathological tumor depth predicts prognosis in patients with poorly differentiated squamous cell carcinoma of the oral cavity. Int J Radiat Oncol Biol Phys. 2011;81(4):e223–e230. https://doi.org/10.1016/j.ijrobp.2011.03.060.

    Article  PubMed  Google Scholar 

  58. Katayama A, Bandoh N, Kishibe K, Takahara M, Ogino T, Nonaka S, et al. Expressions of matrix metalloproteinases in early-stage oral squamous cell carcinoma as predictive indicators for tumor metastases and prognosis. Clin Cancer Res. 2004;10(2):634–40.

    PubMed  Google Scholar 

  59. Kawano S, Zheng Y, Oobu K, Matsubara R, Goto Y, Chikui T, et al. Clinicopathological evaluation of pre-operative chemoradiotherapy with S-1 as a treatment for locally advanced oral squamous cell carcinoma. Oncol Lett. 2016;11(5):3369–76.

    PubMed  PubMed Central  Google Scholar 

  60. Kim SY, Roh JL, Kim JS, Ryu CH, Lee JH, Cho KJ, et al. Utility of FDG PET in patients with squamous cell carcinomas of the oral cavity. Eur J Surg Oncol. 2008;34(2):208–15.

    PubMed  Google Scholar 

  61. Kina S, Nakasone T, Kinjo T, Maruyama T, Kawano T, Arasaki A. Impact of metronomic neoadjuvant chemotherapy on early tongue cancer. Cancer Chemother Pharmacol. 2016;78(4):833–40.

    PubMed  Google Scholar 

  62. Kotwall C, Sako K, Razack MS, Rao U, Bakamjian V, Shedd DP. Metastatic patterns in squamous cell cancer of the head and neck. Am J Surg. 1987;154(4):439–42.

    PubMed  Google Scholar 

  63. Krabbe CA, Pruim J, van der Laan BF, Rdiger LA, Roodenburg JL. FDG-PET and detection of distant metastases and simultaneous tumors in head and neck squamous cell carcinoma: a comparison with chest radiography and chest CT. Oral Oncol. 2009;45(3):234–40.

    PubMed  Google Scholar 

  64. Precht C, Baustian S, Tribius S, Schöllchen M, Hanken H, Smeets R, et al. The benefit of abdominal sonography and chest X-ray for staging oral squamous cell carcinomas in stages UICC I and II. J Craniomaxillofac Surg. 2016;44(2):186–90.

    PubMed  Google Scholar 

  65. Kruse AL, Lübbers HT, Grätz KW. Evaluation of white blood cell count as a possible prognostic marker for oral cancer. Head Neck Oncol. 2011;27(3):13. https://doi.org/10.1186/1758-3284-3-13.

    Article  Google Scholar 

  66. Len X, Quer M, Ors C, del Prado VM, Lpez M. Distant metastases in head and neck cancer patients who achieved loco-regional control. Head Neck. 2000;22(7):680–6.

    Google Scholar 

  67. Liao CT, Wang HM, Chang JT, Ng SH, Hsueh C, Lee LY, et al. Analysis of risk factors for distant metastases in squamous cell carcinoma of the oral cavity. Cancer. 2007;110(7):1501–8.

    PubMed  Google Scholar 

  68. Liao CT, Wang HM, Hsieh LL, Chang JT, Ng SH, Hsueh C, et al. Higher distant failure in young age tongue cancer patients. Oral Oncol. 2006;42(7):718–25.

    PubMed  Google Scholar 

  69. Ljumanovic R, Langendijk JA, Hoekstra OS, Leemans CR, Castelijns JA. Distant metastases in head and neck carcinoma: identification of prognostic groups with MR imaging. Eur J Radiol. 2006;60(1):58–66.

    PubMed  Google Scholar 

  70. Losi-Guembarovski R, Menezes RP, Poliseli F, Chaves VN, Kuasne H, Leichsenring A, et al. Oral carcinoma epidemiology in Paraná, Southern Brazil. Cad Saúde Pública. 2009;25(2):393–400.

    PubMed  Google Scholar 

  71. Ong HS, Gokavarapu S, Wang LZ, Tian Z, Zhang CP. Low pretreatment lymphocyte-monocyte ratio and high platelet-lymphocyte ratio indicate poor cancer outcome in early tongue cancer. J Oral Maxillofac Surg. 2017;75(8):1762–74.

    PubMed  Google Scholar 

  72. Osaki T, Yoneda K, Yamamoto T, Kimura T, Matuoka H, Sakai H, et al. Clinical investigation on pulmonary metastasis of head and neck carcinomas. Oncology. 2000;59(3):196–203.

    PubMed  Google Scholar 

  73. Rena W, Lia Y, Liua C, Qianga C, Zhang L, Gaoa L, et al. Surgical management of squamous cell carcinoma of the lower lip: an experience of 109 cases. Med Oral Patol Oral Cir Bucal. 2014;19(4):e398–402.

    PubMed  PubMed Central  Google Scholar 

  74. Roh JL, Choi SH, Lee SW, Cho KJ, Nam SY, Kim SY. Carcinomas arising in the submandibular gland: high propensity for systemic failure. J Surg Oncol. 2008;97(6):533–7.

    PubMed  Google Scholar 

  75. Sakamoto Y, Matsushita Y, Yamada S, Yanamoto S, Shiraishi T, Asahina I, et al. Risk factors of distant metastasis in patients with squamous cell carcinoma of the oral cavity. Oral Surg Oral Med Oral Pathol Oral Radiol. 2016;121(5):474–80.

    PubMed  Google Scholar 

  76. Santos HBP, Miguel MCDC, Pinto LP, Gordón-Núñez MA, Alves PM, Nonaka CFW. Multinucleated giant cell reaction in lower lip squamous cell carcinoma: a clinical, morphological, and immunohistochemical study. J Oral Pathol Med. 2017;46(9):773–9.

    PubMed  Google Scholar 

  77. Soudry E, Preis M, Hod R, Hamzany Y, Hadar T, Bahar G, et al. Squamous cell carcinoma of the oral tongue in patients younger than 30 years: clinicopathologic features and outcome. Clin Otolaryngol. 2010;35(4):307–12.

    PubMed  Google Scholar 

  78. Spiro RH, Guillamondegui O Jr, Paulino AF, Huvos AG. Pattern of invasion and margin assessment in patients with oral tongue cancer. Head Neck. 1999;21(5):408–13.

    PubMed  Google Scholar 

  79. Stuckensen T, Kovács AF, Adams S, Baum RP. Staging of the neck in patients with oral cavity squamous cell carcinomas: a prospective comparison of PET, ultrasound. CT and MRI J Craniomaxillofac Surg. 2000;28(6):319–24.

    PubMed  Google Scholar 

  80. Sturgis EM, Moore BA, Glisson BS, Kies MS, Shin DM, Byers RM. Neoadjuvant chemotherapy for squamous cell carcinoma of the oral tongue in young adults: a case series. Head Neck. 2005;27(9):748–56.

    PubMed  Google Scholar 

  81. Su HH, Chu ST, Hou YY, Chang KP, Chen CJ. Spindle cell carcinoma of the oral cavity and oropharynx: factors affecting outcome. J Chin Med Assoc. 2006;69(10):478–83.

    PubMed  Google Scholar 

  82. Su PF, Huang WL, Wu HT, Wu CH, Liu TY, Kao SY. p16(INK4A) promoter hypermethylation is associated with invasiveness and prognosis of oral squamous cell carcinoma in an age-dependent manner. Oral Oncol. 2010;46(10):734–9.

    PubMed  Google Scholar 

  83. Sumioka S, Sawai NY, Kishino M, Ishihama K, Minami M, Okura M. Risk factors for distant metastasis in squamous cell carcinoma of the oral cavity. J Oral Maxillofac Surg. 2013;71(7):1291–7.

    PubMed  Google Scholar 

  84. Suton P, Salaric I, Granic M, Mueller D, Luksic I. Prognostic significance of extracapsular spread of lymph node metastasis from oral squamous cell carcinoma in the clinically negative neck. Int J Oral Maxillofac Surg. 2017;46(6):669–75.

    PubMed  Google Scholar 

  85. Suzuki H, Beppu S, Hanai N, Hirakawa H, Hasegawa Y. Lymph node density predicts lung metastases in oral squamous cell carcinoma. Br J Oral Maxillofac Surg. 2016;54(2):213–8.

    PubMed  Google Scholar 

  86. Tabrizi R, Garajei A, Shafie E, Jamshidi S. Outcome of neoadjuvant chemotherapy on local recurrence and distant metastasis of oral squamous cell carcinoma: a retrospective study. J Dent (Shiraz). 2016;17(3):207–12.

    Google Scholar 

  87. Takahashi H, Umeda M, Takahashi Y, Matsui T, Shigeta T, Minamikawa T, et al. Influence of preoperative dental procedures on the prognosis of patients with squamous cell carcinoma of the gingiva. Br J Oral Maxillofac Surg. 2013;51(2):108–12.

    PubMed  Google Scholar 

  88. Takahashi M, Aoki T, Nakamura N, Carreras J, Kajiwara H, Kumaki N, et al. Clinicopathological analysis of 502 patients with oral squamous cell carcinoma with special interest to distant metastasis. Tokai J Exp Clin Med. 2014;39(4):178–85.

    PubMed  Google Scholar 

  89. Umeda M, Shigeta T, Takahashi H, Minamikawa T, Komatsubara H, Oguni A, et al. Clinical evaluation of Lugol's iodine staining in the treatment of stage I-II squamous cell carcinoma of the tongue. Int J Oral Maxillofac Surg. 2011;40(6):593–6.

    PubMed  Google Scholar 

  90. Wang YK, Chuang YS, Wu TS, Lee KW, Wu CW, Wang HC, et al. Endoscopic screening for synchronous esophageal neoplasia among patients with incident head and neck cancer: prevalence, risk factors, and outcomes. Int J Cancer. 2017;141(10):1987–96.

    PubMed  Google Scholar 

  91. Yang WE, Ho CC, Yang SF, Lin SH, Yeh KT, Lin CW, et al. Cathepsin B expression and the correlation with clinical aspects of oral squamous cell carcinoma. PLoS ONE. 2016;11(3):e0152165. https://doi.org/10.1371/journal.pone.0152165.eCollection2016.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Liu F, Wang L, Pang S, Kan Q. Management of and risk factors for regional recurrence in upper lip squamous cell carcinoma. Medicine (Baltimore). 2017;96(45):e8270.

    Google Scholar 

  93. Lock M, Cao JQ, D'Souza DP, Hammond JA, Karnas S, Lewis C, et al. Brachytherapy with permanent gold grain seeds for squamous cell carcinoma of the lip. Radiother Oncol. 2011;98(3):352–6.

    PubMed  Google Scholar 

  94. Marsiglia H, Haie-Meder C, Sasso G, Mamelle G, Gerbaulet A. Brachytherapy for T1–T2 floor-of-the-mouth cancers: the Gustave-Roussy Institute experience. Int J Radiat Oncol Biol Phys. 2002;52(5):1257–63.

    PubMed  Google Scholar 

  95. Morselli P, Masciotra L, Pinto V, Zollino I, Brunelli G, Carinci F. Clinical parameters in T1N0M0 lower lip squamous cell carcinoma. J Craniofac Surg. 2007;18(5):1079–82.

    PubMed  Google Scholar 

  96. Sessions DG, Spector GJ, Lenox J, Parriott S, Haughey B, Chao C, et al. Analysis of treatment results for floor-of-mouth cancer. Laryngoscope. 2000;110(10 Pt 1):1764–72.

    PubMed  Google Scholar 

  97. Thanh Pham T, Cross S, Gebski V, Veness MJ. Squamous cell carcinoma of the lip in Australian patients: definitive radiotherapy is an efficacious option to surgery in select patients. Dermatol Surg. 2015;41(2):219–25.

    PubMed  Google Scholar 

  98. Unsal AA, Unsal AB, Henn TE, Baredes S, Eloy JA. Cutaneous squamous cell carcinoma of the lip: a population-based analysis. Laryngoscope. 2018;128(1):84–90.

    PubMed  Google Scholar 

  99. Probert JC, Thompson RW, Bagshaw MA. Patterns of spread of distant metastases in head and neck cancer. Cancer. 1974;33(1):127–33.

    PubMed  Google Scholar 

  100. Peltier LF, Thomas LB, Barclay TH, Kremen AJ. The incedence of distant metastases among patients dying with head and cancers. Surgery. 1951;30(5):827–33.

    PubMed  Google Scholar 

  101. O'Brien PH, Carlson R, Steubner EA Jr, Staley CT. Distant metastases in epidermoid cell carcinoma of the head and neck. Cancer. 1971;27(2):304–7.

    PubMed  Google Scholar 

  102. Merino OR, Lindberg RD, Fletcher GH. An analysis of distant metastases from squamous cell carcinoma of the upper respiratory and digestive tracts. Cancer. 1977;40(1):145–51.

    PubMed  Google Scholar 

  103. Fang FM, Leung SW, Huang CC, Liu YT, Wang CJ, Chen HC, et al. Combined-modality therapy for squamous carcinoma of the buccal mucosa: treatment results and prognostic factors. Head Neck. 1997;19:506–12.

    PubMed  Google Scholar 

  104. Lin CS, Jen YM, Cheng MF, Lin YS, Su WF, Hwang JM, et al. Squamous cell carcinoma of the buccal mucosa: an aggressive cancer requiring multimodality treatment. Head Neck. 2006;28:150–7.

    PubMed  Google Scholar 

  105. Liao CT, Wang HM, Ng SH, Yen TC, Lee LY, Hsueh C, et al. Good tumor control and survivals of squamous cell carci- noma of buccal mucosa treated with radical surgery with or without neck dissection in Taiwan. Oral Oncol. 2006;42:800–9.

    PubMed  Google Scholar 

  106. Kuperman D, Auethavekiat V, Adkins DR, Nussenbaum B, Collins S, Boonchalermvichian C, et al. Squamous cell cancer of the head and neck with distant metastasis at presentation. Head Neck. 2011;33(5):714–8.

    PubMed  Google Scholar 

  107. Troell RJ, Terris DJ. Detection of metastases from head and neck cancer. Laryngoscope. 1995;105:247–50.

    PubMed  Google Scholar 

  108. Papac RJ. Distant metastases from head and neck cancer. Cancer. 1984;53:342–5.

    PubMed  Google Scholar 

  109. Nishijima W, Takooda S, Tokita N, Takayama S, Sakura M. Analyses of distant metastases in squamous cell carcinoma of the head and neck and lesions above the clavicle at autopsy. Arch Otolaryngol Head Neck Surg. 1993;119:65–8.

    PubMed  Google Scholar 

  110. Bianchi B, Copelli C, Cocchi R, Ferrari S, Pederneschi N, Sesenna E. Adenoid cystic carcinoma of intraoral minor salivary glands. Oral Oncol. 2008;44(11):1026–31.

    PubMed  Google Scholar 

  111. Copelli C, Bianchi B, Ferrari S, Ferri A, Sesenna E. Malignant tumors of intraoral minor salivary glands. Oral Oncol. 2008;44(7):658–63.

    PubMed  Google Scholar 

  112. Ma DQ, Yu GY. Tumours of the minor salivary glands: a clinicopathologic study of 243 cases. Acta Otolaryngol. 1987;103(5–6):325–31.

    PubMed  Google Scholar 

  113. Dubal PM, Unsal AA, Chung SY, Patel AV, Park RC, Baredes S, et al. Population-based trends in outcomes in adenoid cystic carcinoma of the oral cavity. Am J Otolaryngol. 2016;37(5):398–406.

    PubMed  Google Scholar 

  114. Franchi A, Gallo O, Bocciolini C, Franchi L, Paglierani M, Santucci M. Reduced E-cadherin expression correlates with unfavorable prognosis in adenoid cystic carcinoma of salivary glands of the oral cavity. Am J Clin Pathol. 1999;111(1):43–50.

    PubMed  Google Scholar 

  115. Gao M, Hao Y, Huang MX, Ma DQ, Luo HY, Gao Y, et al. Clinicopathological study of distant metastases of salivary adenoid cystic carcinoma. Int J Oral Maxillofac Surg. 2013;42(8):923–8.

    PubMed  Google Scholar 

  116. Horiuchi J, Shibuya H, Suzuki S, Takeda M, Takagi M. The role of radiotherapy in the management of adenoid cystic carcinoma of the head and neck. Int J Radiat Oncol Biol Phys. 1987;13(8):1135–41.

    PubMed  Google Scholar 

  117. Jenkins DW, Spaulding CA, Constable WC, Cantrell RW. Minor salivary gland tumors: the role of radiotherapy. Am J Otolaryngol. 1989;10(4):250–6.

    PubMed  Google Scholar 

  118. Kuhel W, Goepfert H, Luna M, Wendt C, Wolf P. Adenoid cystic carcinoma of the palate. Arch Otolaryngol Head Neck Surg. 1992;118(3):243–7.

    PubMed  Google Scholar 

  119. Lukši I, Suton P, Macan D, Dinjar K. Intraoral adenoid cystic carcinoma: is the presence of perineural invasion associated with the size of the primary tumour, local extension, surgical margins, distant metastases, and outcome? Br J Oral Maxillofac Surg. 2014;52(3):214–8.

    Google Scholar 

  120. Pogodzinski MS, Sabri AN, Lewis JE, Olsen KD. Retrospective study and review of polymorphous low-grade adenocarcinoma. Laryngoscope. 2006;116(12):2145–9.

    PubMed  Google Scholar 

  121. Rapidis AD, Givalos N, Gakiopoulou H, Faratzis G, Stavrianos SD, Vilos GA, et al. Adenoid cystic carcinoma of the head and neck. Clinicopathological analysis of 23 patients and review of the literature. Oral Oncol. 2005;41(3):328–35.

    PubMed  Google Scholar 

  122. Shiiba M, Unozawa M, Higo M, Kouzu Y, Kasamatsu A, Sakamoto Y, et al. Controlling distant metastasis and surgical treatment are crucial for improving clinical outcome in uncommon head and neck malignancies, such as non-squamous cell carcinoma. Mol Clin Oncol. 2014;2(4):609–17.

    PubMed  PubMed Central  Google Scholar 

  123. Tincani AJ, Negro AD, Araújo PPC, Akashi HK, Martins AS, Altemani AM, et al. Management of salivary gland adenoid cystic carcinoma: institutional experience of a case series. Sao Paulo Med J. 2006;124(1):26–30.

    PubMed  Google Scholar 

  124. Umeda M, Nishimatsu N, Yokoo S, Shibuya Y, Fujioka M, Komori T. The role of radiotherapy for patients with adenoid cystic carcinoma of the salivary gland. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000;89(6):724–9.

    PubMed  Google Scholar 

  125. Wang CC, Goodman M. Photon irradiation of unresectable carcinomas of salivary glands. Int J Radiat Oncol Biol Phys. 1991;21(3):569–76.

    PubMed  Google Scholar 

  126. Yu T, Gao QH, Wang XY, Wen YM, Li LJ. Malignant sublingual gland tumors: a retrospective clinicopathologic study of 28 cases. Oncology. 2007;72(1–2):39–44.

    PubMed  Google Scholar 

  127. Zdanowski R, Dias FL, Barbosa MM, Lima RA, Faria PA, Loyola AM, et al. Sublingual gland tumors: clinical, pathologic, and therapeutic analysis of 13 patients treated in a single institution. Head Neck. 2011;33(4):476–81.

    PubMed  Google Scholar 

  128. Zushi Y, Noguchi K, Hashitani S, Sakurai K, Segawa E, Takaoka K, et al. Relations among expression of CXCR4, histological patterns, and metastatic potential in adenoid cystic carcinoma of the head and neck. Int J Oncol. 2008;33(6):1133–9.

    PubMed  Google Scholar 

  129. Matsuba HM, Spector GJ, Thawley SE, Simpson JR, Mauney M, Pikul FJ. Adenoid cystic salivary gland carcinoma. A histopathologic review of treatment failure patterns. Cancer. 1986;57(3):519–24.

    PubMed  Google Scholar 

  130. Spiro RH. Distant metastasis in adenoid cystic carcinoma of salivary origin. Am J Surg. 1997;174(5):495–8.

    PubMed  Google Scholar 

  131. Tarpley TM, Giansanti JS. Adenoid cystic carcinoma. Analysis of fifty oral cases. Oral Surg Oral Med Oral Pathol. 1976;41(4):484–97.

    PubMed  Google Scholar 

  132. Breik O, Sim F, Wong T, Nastri A, Iseli TA, Wiesenfeld D. Survival outcomes of mucosal melanoma in the head and neck: case series and review of current treatment guidelines. J Oral Maxillofac Surg. 2016;74(9):1859–71.

    PubMed  Google Scholar 

  133. Jing G, Wu Y, Song H, Ren G, Wang R, Guo W. Primary malignant melanoma of the lip: a report of 48 cases. J Oral Maxillofac Surg. 2015;73(11):2232–40.

    PubMed  Google Scholar 

  134. Korabiowska M, Brinck U, Hoenig JF, Bartkowski SB, Mirecka J, Schauer A, et al. An application of MIB antibody to the retrospective study of melanomas of oral mucosa and facial skin. J Cancer Res Clin Oncol. 1994;120(6):365–8.

    PubMed  Google Scholar 

  135. Lian B, Cui CL, Zhou L, Song X, Zhang XS, Wu D, et al. The natural history and patterns of metastases from mucosal melanoma: an analysis of 706 prospectively-followed patients. Ann Oncol. 2017;28(4):868–73.

    PubMed  Google Scholar 

  136. Lourenço SV, Sanguëza AM, Sotto MN, Bologna SB, Giacomo TB, Buim ME, et al. Primary oral mucosal melanoma: a series of 35 new cases from South America. Am J Dermatopathol. 2009;31(4):323–30.

    PubMed  Google Scholar 

  137. Song H, Wu Y, Ren G, Guo W, Wang L. Prognostic factors of oral mucosal melanoma: histopathological analysis in a retrospective cohort of 82 cases. Histopathology. 2015;67(4):548–56.

    PubMed  Google Scholar 

  138. Tanaka N, Mimura M, Ogi K, Amagasa T. Primary malignant melanoma of the oral cavity: assessment of outcome from the clinical records of 35 patients. Int J Oral Maxillofac Surg. 2004;33(8):761–5.

    PubMed  Google Scholar 

  139. Tas F, Keskin S. Mucosal melanoma in the head and neck region: different clinical features and same outcome to cutaneous melanoma. ISRN Dermatol. 2013;16(2013):586915. https://doi.org/10.1155/2013/586915.

    Article  Google Scholar 

  140. Umeda M, Komatsubara H, Shigeta T, Ojima Y, Minamikawa T, Shibuya Y, et al. Treatment and prognosis of malignant melanoma of the oral cavity: preoperative surgical procedure increases risk of distant metastasis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008;106(1):51–7.

    PubMed  Google Scholar 

  141. Yang X, Ren GX, Zhang CP, Zhou GY, Hu YJ, Yang WJ, et al. Neck dissection and post-operative chemotherapy with dimethyl triazeno imidazole carboxamide and cisplatin protocol are useful for oral mucosal melanoma. BMC Cancer. 2010;11(10):623. https://doi.org/10.1186/1471-2407-10-623.

    Article  Google Scholar 

  142. Abdul-Karim FW, Ayala AG, Chawla SP, Jing BS, Goepfert H. Malignant fibrous histiocytoma of jaws. A clinicopathologic study of 11 cases. Cancer. 1985;56(7):1590–6.

    PubMed  Google Scholar 

  143. Canadian Society of Otolaryngology-Head and Neck Surgery Oncology Study Group. Osteogenic sarcoma of the mandible and maxilla: a Canadian review (1980–2000). J Otolaryngol. 2004;33(3):139–44.

    Google Scholar 

  144. Fernandez Sanroman J, Alonso del Hoyo JR, Diaz FJ, Gil-Diez JL, Monje F, Naval L, et al. Sarcomas of the head and neck. Br J Oral Maxillofac Surg. 1992;30(2):115–8.

    PubMed  Google Scholar 

  145. Pandey M, Chandramohan K, Thomas G, Mathew A, Sebastian P, Somanathan T, et al. Soft tissue sarcoma of the head and neck region in adults. Int J Oral Maxillofac Surg. 2003;32(1):43–8.

    PubMed  Google Scholar 

  146. Patel SG, Meyers P, Huvos AG, Wolden S, Singh B, Shaha AR, et al. Improved outcomes in patients with osteogenic sarcoma of the head and neck. Cancer. 2002;95(7):1495–503.

    PubMed  Google Scholar 

  147. Russ JE, Jesse RH. Management of osteosarcoma of the maxilla and mandible. Am J Surg. 1980;140(4):572–6.

    PubMed  Google Scholar 

  148. Sumida T, Otawa N, Kamata YU, Yamada T, Uchida K, Nakano H, et al. A Clinical Investigation of Oral Sarcomas at Multi-institutions Over the Past 30 Years. Anticancer Res. 2015;35(8):4551–5.

    PubMed  Google Scholar 

  149. van Es RJJ, Keus RB, van der Waal I, Koole R, Vermey A. Osteosarcoma of the jaw bones. Long-term follow up of 48 cases. Int J Oral Maxillofac Surg. 1997;26(3):191–7.

    PubMed  Google Scholar 

  150. Vencio EF, Reeve CM, Unni KK, Nascimento AG. Mesenchymal chondrosarcoma of the jaw bones: clinicopathologic study of 19 cases. Cancer. 1998;82(12):2350–5.

    PubMed  Google Scholar 

  151. Guadagnolo BA, Zagars GK, Raymond AK, Benjami RS, Sturgis EM. Osteosarcoma of the Jaw/Craniofacial. Cancer. 2009;32:62–70.

    Google Scholar 

  152. Simpson JR, Matsuba HM, Thawley SE, Mauney M. Improved treatment of salivary adenocarcinomas: planned combined surgery and irradiation. Laryngoscope. 1986;96(8):904–7.

    PubMed  Google Scholar 

  153. Gilbert MR, Sharma A, Schmitt NC, Johnson JT, Ferris RL, Duvvuri U, et al. A 20-year review of 75 cases of salivary duct carcinoma. JAMA Otolaryngol Head Neck Surg. 2016;142(5):489–95. https://doi.org/10.1001/jamaoto.2015.3930.

    Article  PubMed  PubMed Central  Google Scholar 

  154. Kane SV, Bagwan IN. Myoepithelial carcinoma of the salivary glands: a clinicopathologic study of 51 cases in a tertiary cancer center. Arch Otolaryngol Head Neck Surg. 2010;136(7):702–12.

    PubMed  Google Scholar 

  155. Smith VA, Camp ER, Lentsch EJ. Merkel cell carcinoma: identification of prognostic factors unique to tumors located in the head and neck based on analysis of SEER data. Laryngoscope. 2012;122(6):1283–90.

    PubMed  Google Scholar 

  156. Regezi JA, Sciubba JJ, Jordan J. Oral pathology: clinical pathologic correlations. St. Louis: Elsevier/Sounders; 2012.

    Google Scholar 

  157. Mallya SM, Lam EWN. White and Pharoah's oral radiology. Principles and interpretation. St Louis: Elsevier; 2019.

    Google Scholar 

  158. Barnes L, Eveson JW, Reichart P, Sidransky D. Pathology and genetics of head and neck tumors. World Health Organization classification of tumors. Lyon: IARC Press; 2005.

    Google Scholar 

  159. Ellis GL, Auclair PL. Tumors of the Salivary Glands. AFIP atlas of tumor pathology: series 4. Washington: ARP Press; 2008.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuka Uchiyama.

Ethics declarations

Conflict of interest

Our work is free of conflict of interest and has no grant support.

Human and animal rights

Human participants and/or animals were not included.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Uchiyama, Y., Sasai, T., Nakatani, A. et al. Distant metastasis from oral cavity—correlation between histopathology results and primary site. Oral Radiol 37, 167–179 (2021). https://doi.org/10.1007/s11282-020-00440-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11282-020-00440-3

Keywords

  • Oral
  • Distant metastases
  • Malignancy histopathology