Top

Clinical Oral Investigations

Published in:

Open Access 01-01-2024 | Neck Dissection | Research

Occult metastasis is no burden factor in oral squamous cell carcinoma patients when adhering to a standardized approach in neck dissection

Authors: Ann-Kristin Struckmeier, Mayte Buchbender, Tobias Moest, Rainer Lutz, Abbas Agaimy, Marco Kesting

Published in: Clinical Oral Investigations | Issue 1/2024

Abstract

Objectives

Management of the neck in patients with oral squamous cell carcinoma (OSCC) is pivotal to oncologic control and survival. However, there is controversy regarding necessity of neck dissection (ND) in patients with clinically node-negative neck. We aimed to assess risk factors for occult metastasis and to explore whether the presence of occult lymph node metastases (LNMs) has an impact on recurrence and survival.

Material and methods

A retrospective cohort study was performed including patients with primary OSCC who underwent radical tumor resection and ND in a high-volume center adhering to the prevailing German guideline. The ND was performed according to a standardized approach.

Results

Four hundred twenty-one patients with primary surgically treated OSCC were included. The incidence of occult metastasis was 14.49%. A pathological T stage > 1 (multivariate analysis, odds ratio (OR) 3.958, p = 0.042) and the presence of extranodal extension in LNMs (multivariate analysis, OR 0.287, p = 0.020) were identified as independent risk factors for occult metastasis. When comparing patients with and without occult metastasis, there were no significant differences in terms of progression-free survival (log-rank, p = 0.297) and overall survival (log-rank, p = 0.320). There were no cases of ipsilateral neck recurrence. One patient developed contralateral neck metastasis; however, he initially presented with a unilateral pT1 pN0 tumor.

Conclusions

Overall, our findings suggest that conducting a standardized approach in ND should be applied in terms of management of the neck in order to maintain survival rates and to prevent neck recurrence in OSCC patients.

Clinical relevance.

None of the risk factors for occult metastasis can be reliably assessed preoperatively. Although elective ND does not guarantee the complete prevention of neck recurrence, it increases the likelihood of either timely removal of micrometastases or strengthens the justification for adjuvant therapy. Consequently, this approach leads to improvements in clinical outcomes.

Massano J, Regateiro FS, Januario G, Ferreira A (2006) Oral squamous cell carcinoma: review of prognostic and predictive factors. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 102:67–76. https://doi.org/10.1016/j.tripleo.2005.07.038CrossRefPubMed

Ferlay J, Colombet M, Soerjomataram I, Mathers C, Parkin DM, Pineros M, Znaor A, Bray F (2019) Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer 144:1941–1953. https://doi.org/10.1002/ijc.31937CrossRefPubMed

Moratin J, Horn D, Metzger K, Ristow O, Flechtenmacher C, Engel M, Hoffmann J, Freier K, Freudlsperger C (2020) Squamous cell carcinoma of the mandible - patterns of metastasis and disease recurrence in dependence of localization and therapy. J Craniomaxillofac Surg 48:1158–1163. https://doi.org/10.1016/j.jcms.2020.10.006CrossRefPubMed

Ganly I, Patel S, Shah J (2012) Early stage squamous cell cancer of the oral tongue–clinicopathologic features affecting outcome. Cancer 118:101–111. https://doi.org/10.1002/cncr.26229CrossRefPubMed

Crile G (1906) III. On the technique of operations upon the head and neck. Ann Surg 44:842–850. https://doi.org/10.1097/00000658-190612000-00003CrossRefPubMedPubMedCentral

Vandenbrouck C, Sancho-Garnier H, Chassagne D, Saravane D, Cachin Y, Micheau C (1980) Elective versus therapeutic radical neck dissection in epidermoid carcinoma of the oral cavity: results of a randomized clinical trial. Cancer 46:386–390. https://doi.org/10.1002/1097-0142(19800715)46:2%3c386::aid-cncr2820460229%3e3.0.co;2-9CrossRefPubMed

Huang SF, Chang JT, Liao CT, Kang CJ, Lin CY, Fan KH, Wang HM, Chen IH (2015) The role of elective neck dissection in early stage buccal cancer. Laryngoscope 125:128–133. https://doi.org/10.1002/lary.24840CrossRefPubMed

Ebrahimi A, Ashford BG, Clark JR (2012) Improved survival with elective neck dissection in thick early-stage oral squamous cell carcinoma. Head Neck 34:709–716. https://doi.org/10.1002/hed.21809CrossRefPubMed

Cai H, Zhu Y, Wang C, Zhang Y, Hou J (2020) Neck nodal recurrence and survival of clinical T1–2 N0 oral squamous cell carcinoma in comparison of elective neck dissection versus observation: a meta-analysis. Oral Surg Oral Med Oral Pathol Oral Radiol 129:296–310. https://doi.org/10.1016/j.oooo.2019.10.012CrossRefPubMed

10.

Struckmeier AK, Yekta E, Agaimy A, Kopp M, Buchbender M, Moest T, Lutz R, Kesting M (2023) Diagnostic accuracy of contrast-enhanced computed tomography in assessing cervical lymph node status in patients with oral squamous cell carcinoma. J Cancer Res Clin Oncol. https://doi.org/10.1007/s00432-023-05470-yCrossRefPubMedPubMedCentral

11.

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

12.

Fasunla AJ, Greene BH, Timmesfeld N, Wiegand S, Werner JA, Sesterhenn AM (2011) A meta-analysis of the randomized controlled trials on elective neck dissection versus therapeutic neck dissection in oral cavity cancers with clinically node-negative neck. Oral Oncol 47:320–324. https://doi.org/10.1016/j.oraloncology.2011.03.009CrossRefPubMed

13.

D’Cruz AK, Vaish R, Kapre N, Dandekar M, Gupta S, Hawaldar R, Agarwal JP, Pantvaidya G, Chaukar D, Deshmukh A, Kane S, Arya S, Ghosh-Laskar S, Chaturvedi P, Pai P, Nair S, Nair D, Badwe R, Head ND, Management G (2015) Elective versus therapeutic neck dissection in node-negative oral cancer. N Engl J Med 373:521–529. https://doi.org/10.1056/NEJMoa1506007CrossRefPubMed

14.

Feng Z, Li JN, Li CZ, Guo CB (2014) 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 42:806–810. https://doi.org/10.1016/j.jcms.2013.11.016CrossRefPubMed

15.

Abu-Ghanem S, Yehuda M, Carmel NN, Leshno M, Abergel A, Gutfeld O, Fliss DM (2016) Elective neck dissection vs observation in early-stage squamous cell carcinoma of the oral tongue with no clinically apparent lymph node metastasis in the neck: a systematic review and meta-analysis. JAMA Otolaryngol Head Neck Surg 142:857–865. https://doi.org/10.1001/jamaoto.2016.1281CrossRefPubMed

16.

Koerdt S, Rockl J, Rommel N, Mucke T, Wolff KD, Kesting MR (2016) Lymph node management in the treatment of oral cancer: analysis of a standardized approach. J Craniomaxillofac Surg 44:1737–1742. https://doi.org/10.1016/j.jcms.2016.08.002CrossRefPubMed

17.

Kesting M (2015). Oral cancer surgery: a visual guide. In Oral Cancer Surgery: A Visual Guide

18.

Tam S, Amit M, Zafereo M, Bell D, Weber RS (2019) Depth of invasion as a predictor of nodal disease and survival in patients with oral tongue squamous cell carcinoma. Head Neck-J Sci Spec 41:177–184. https://doi.org/10.1002/hed.25506CrossRef

19.

Sakata J, Yamana K, Yoshida R, Matsuoka Y, Kawahara K, Arita H, Nakashima H, Nagata M, Hirosue A, Kawaguchi S, Gohara S, Nagao Y, Hiraki A, Shinohara M, Toya R, Murakami R, Nakayama H (2018) Tumor budding as a novel predictor of occult metastasis in cT2N0 tongue squamous cell carcinoma. Hum Pathol 76:1–8. https://doi.org/10.1016/j.humpath.2017.12.021CrossRefPubMed

20.

Loganathan P, Sayan A, Hsu DWK, Paraneetharan S, Ilankovan V (2017) Squamous cell carcinoma of the anterior tongue: is tumour thickness an indicator for cervical metastasis? Int J Oral Maxillofac Surg 46:407–412. https://doi.org/10.1016/j.ijom.2016.11.003CrossRefPubMed

21.

Lop J, Rigo A, Codina A, de Juan J, Quer M, Leon X (2018) Prognostic significance of extranodal extension in head and neck squamous cell carcinoma cN0 patients with occult metastatic neck nodes. Acta Otorrinolaringol Esp (Engl Ed) 69:156–164. https://doi.org/10.1016/j.otorri.2017.07.002CrossRefPubMed

22.

de Bree R, Takes RP, Castelijns JA, Medina JE, Stoeckli SJ, Mancuso AA, Hunt JL, Rodrigo JP, Triantafyllou A, Teymoortash A, Civantos FJ, Rinaldo A, Pitman KT, Hamoir M, Robbins KT, Silver CE, Hoekstra OS, Ferlito A (2015) Advances in diagnostic modalities to detect occult lymph node metastases in head and neck squamous cell carcinoma. Head Neck 37:1829–1839. https://doi.org/10.1002/hed.23814CrossRefPubMed

23.

Yang L, Liu F, Wu Y, Fang Q, Zhang X, Du W, Zhang X, Chen D, Luo R (2020) Predictive value of occult metastasis and survival significance of metabolic tumor volume determined by PET-CT in cT1-2N0 squamous cell carcinoma of the tongue. Front Oncol 10:542530. https://doi.org/10.3389/fonc.2020.542530CrossRefPubMedPubMedCentral

24.

Hutchison IL, Ridout F, Cheung SMY, Shah N, Hardee P, Surwald C, Thiruchelvam J, Cheng L, Mellor TK, Brennan PA, Baldwin AJ, Shaw RJ, Halfpenny W, Danford M, Whitley S, Smith G, Bailey MW, Woodwards B, Patel M, McManners J, Chan CH, Burns A, Praveen P, Camilleri AC, Avery C, Putnam G, Jones K, Webster K, Smith WP, Edge C, McVicar I, Grew N, Hislop S, Kalavrezos N, Martin IC, Hackshaw A (2019) 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 121:827–836. https://doi.org/10.1038/s41416-019-0587-2CrossRefPubMedPubMedCentral

25.

de Matos LL, Manfro G, dos Santos RV, Stabenow E, de Mello ES, Alves VAF, Pinto FR, Kulcsar MAV, Brandao LG, Cernea CR (2014) Tumor thickness as a predictive factor of lymph node metastasis and disease recurrence in T1N0 and T2N0 squamous cell carcinoma of the oral tongue. Or Surg or Med or Pa 118:209–217. https://doi.org/10.1016/j.oooo.2014.03.023CrossRefPubMed

26.

Kane SV, Gupta M, Kakade AC, Cruz AD (2006) Depth of invasion is the most significant histological predictor of subclinical cervical lymph node metastasis in early squamous carcinomas of the oral cavity. Ejso-Eur J Surg Onc 32:795–803. https://doi.org/10.1016/j.ejso.2006.05.004CrossRef

27.

Alvarez Amezaga J, Barbier Herrero L, Pijoan del Barrio JI, Martin Rodriguez JC, Romo Simon L, Genolla Subirats J, Rios Altolaguirre G, de los Rios A, ArteagoitiaCalvo I, LandaLlona S, Arruti Gonzalez JA, Lopez Cedrun J, Santamaria Zuazua J (2007) Diagnostic efficacy of sentinel node biopsy in oral squamous cell carcinoma. Cohort study and meta-analysis. Med Oral Patol Oral Cir Bucal 12:E235-243PubMed

28.

Chien CY, Wang CP, Lee LY, Lee SR, Ng SH, Kang CJ, Lin JC, Terng SD, Hua CH, Chen TM, Chen WC, Tsai YT, Tsai CY, Chu YH, Lin CY, Fan KH, Wang HM, Hsieh CH, Yeh CH, Lin CH, Tsao CK, Cheng NM, Fang TJ, Huang SF, Lee LA, Fang KH, Wang YC, Lin WN, Hsin LJ, Yen TC, Wen YW, Liao CT (2023) Indications for elective neck dissection in cT1N0M0 oral cavity cancer according to the AJCC eight edition: a nationwide study. Oral Oncol 140:106366. https://doi.org/10.1016/j.oraloncology.2023.106366CrossRefPubMed

29.

Schilling C, Stoeckli SJ, Haerle SK, Broglie MA, Huber GF, Sorensen JA, Bakholdt V, Krogdahl A, von Buchwald C, Bilde A, Sebbesen LR, Odell E, Gurney B, O’Doherty M, de Bree R, Bloemena E, Flach GB, Villarreal PM, Fresno Forcelledo MF, Junquera Gutierrez LM, Amezaga JA, Barbier L, Santamaria-Zuazua J, Moreira A, Jacome M, Vigili MG, Rahimi S, Tartaglione G, Lawson G, Nollevaux MC, Grandi C, Donner D, Bragantini E, Dequanter D, Lothaire P, Poli T, Silini EM, Sesenna E, Dolivet G, Mastronicola R, Leroux A, Sassoon I, Sloan P, McGurk M (2015) Sentinel European Node Trial (SENT): 3-year results of sentinel node biopsy in oral cancer. Eur J Cancer 51:2777–2784. https://doi.org/10.1016/j.ejca.2015.08.023CrossRefPubMed

30.

Sagheb K, Sagheb K, Rahimi-Nedjat R, Taylor K, Al-Nawas B, Walter C (2016) Sentinel lymph node biopsy in T1/T2 squamous cell carcinomas of the tongue: a prospective study. Oncol Lett 11:600–604. https://doi.org/10.3892/ol.2015.3933CrossRefPubMed

31.

Hyde NC, Prvulovich E, Newman L, Waddington WA, Visvikis D, Ell P (2003) A new approach to pre-treatment assessment of the N0 neck in oral squamous cell carcinoma: the role of sentinel node biopsy and positron emission tomography. Oral Oncol 39:350–360. https://doi.org/10.1016/s1368-8375(02)00121-5CrossRefPubMed

32.

Gallegos-Hernandez JF, Hernandez-Hernandez DM, Flores-Diaz R, Sierra-Santiesteban I, Pichardo-Romero P, Arias-Ceballos H, Minauro-Munoz G, Alvarado-Cabrero I (2005) The number of sentinel nodes identified as prognostic factor in oral epidermoid cancer. Oral Oncol 41:947–952. https://doi.org/10.1016/j.oraloncology.2005.05.010CrossRefPubMed

33.

Ross GL, Soutar DS, Gordon MacDonald D, Shoaib T, Camilleri I, Roberton AG, Sorensen JA, Thomsen J, Grupe P, Alvarez J, Barbier L, Santamaria J, Poli T, Massarelli O, Sesenna E, Kovacs AF, Grunwald F, Barzan L, Sulfaro S, Alberti F (2004) Sentinel node biopsy in head and neck cancer: preliminary results of a multicenter trial. Ann Surg Oncol 11:690–696. https://doi.org/10.1245/ASO.2004.09.001CrossRefPubMed

34.

Alkureishi LW, Burak Z, Alvarez JA, Ballinger J, Bilde A, Britten AJ, Calabrese L, Chiesa C, Chiti A, de Bree R, Gray HW, Hunter K, Kovacs AF, Lassmann M, Leemans CR, Mamelle G, McGurk M, Mortensen J, Poli T, Shoaib T, Sloan P, Sorensen JA, Stoeckli SJ, Thomsen JB, Trifiro G, Werner J, Ross GL (2009) European Association of Nuclear Medicine Oncology C, European Sentinel Node Biopsy Trial C Joint practice guidelines for radionuclide lymphoscintigraphy for sentinel node localization in oral/oropharyngeal squamous cell carcinoma. Ann Surg Oncol 16:3190–3210. https://doi.org/10.1245/s10434-009-0726-8CrossRefPubMedPubMedCentral

35.

Bernier J, Cooper JS, Pajak TF, van Glabbeke M, Bourhis J, Forastiere A, Ozsahin EM, Jacobs JR, Jassem J, Ang KK, Lefebvre JL (2005) Defining risk levels in locally advanced head and neck cancers: a comparative analysis of concurrent postoperative radiation plus chemotherapy trials of the EORTC (#22931) and RTOG (# 9501). Head Neck 27:843–850. https://doi.org/10.1002/hed.20279CrossRefPubMed

36.

Carlton JA, Maxwell AW, Bauer LB, McElroy SM, Layfield LJ, Ahsan H, Agarwal A (2017) Computed tomography detection of extracapsular spread of squamous cell carcinoma of the head and neck in metastatic cervical lymph nodes. Neuroradiol J 30:222–229. https://doi.org/10.1177/1971400917694048CrossRefPubMedPubMedCentral

37.

Chai RL, Rath TJ, Johnson JT, Ferris RL, Kubicek GJ, Duvvuri U (2013) Branstetter BFt Accuracy of computed tomography in the prediction of extracapsular spread of lymph node metastases in squamous cell carcinoma of the head and neck. JAMA Otolaryngol Head Neck Surg 139:1187–1194. https://doi.org/10.1001/jamaoto.2013.4491CrossRefPubMed

38.

Haidari S, Obermeier KT, Kraus M, Otto S, Probst FA, Liokatis P (2022) Nodal disease and survival in oral cancer: is occult metastasis a burden factor compared to preoperatively nodal positive neck? Cancers (Basel) 14. https://doi.org/10.3390/cancers14174241

39.

Broglie MA, Haerle SK, Huber GF, Haile SR, Stoeckli SJ (2013) Occult metastases detected by sentinel node biopsy in patients with early oral and oropharyngeal squamous cell carcinomas: impact on survival. Head Neck 35:660–666. https://doi.org/10.1002/hed.23017CrossRefPubMed

40.

Liu JY, Chen CF, Bai CH (2019) Elective neck dissection versus observation in early-stage (cT1/T2N0) oral squamous cell carcinoma. Laryngoscope Investig Otolaryngol 4:554–561. https://doi.org/10.1002/lio2.301CrossRefPubMedPubMedCentral

41.

Liu X, Lao X, Liang L, Zhang S, Li K, Liao G, Liang Y (2017) Neck observation versus elective neck dissection in management of clinical T1N0 oral squamous cell carcinoma: a retrospective study of 232 patients. Chin J Cancer Res 29:179–188. https://doi.org/10.21147/j.issn.1000-9604.2017.03.03CrossRefPubMedPubMedCentral

42.

Kligerman J, Lima RA, Soares JR, Prado L, Dias FL, Freitas EQ, Olivatto LO (1994) Supraomohyoid neck dissection in the treatment of T1/T2 squamous cell carcinoma of oral cavity. Am J Surg 168:391–394. https://doi.org/10.1016/s0002-9610(05)80082-0CrossRefPubMed

43.

Flach GB, Tenhagen M, de Bree R, Brakenhoff RH, van der Waal I, Bloemena E, Kuik DJ, Castelijns JA, Leemans CR (2013) Outcome of patients with early stage oral cancer managed by an observation strategy towards the N0 neck using ultrasound guided fine needle aspiration cytology: no survival difference as compared to elective neck dissection. Oral Oncol 49:157–164. https://doi.org/10.1016/j.oraloncology.2012.08.006CrossRefPubMed

44.

Nieuwenhuis EJ, Castelijns JA, Pijpers R, van den Brekel MW, Brakenhoff RH, van der Waal I, Snow GB, Leemans CR (2002) Wait-and-see policy for the N0 neck in early-stage oral and oropharyngeal squamous cell carcinoma using ultrasonography-guided cytology: is there a role for identification of the sentinel node? Head Neck 24:282–289. https://doi.org/10.1002/hed.10018CrossRefPubMed

45.

Ho CM, Lam KH, Wei WI, Lau SK, Lam LK (1992) Occult lymph node metastasis in small oral tongue cancers. Head Neck 14:359–363. https://doi.org/10.1002/hed.2880140504CrossRefPubMed

46.

Gane EM, Michaleff ZA, Cottrell MA, McPhail SM, Hatton AL, Panizza BJ, O’Leary SP (2017) Prevalence, incidence, and risk factors for shoulder and neck dysfunction after neck dissection: a systematic review. Eur J Surg Oncol 43:1199–1218. https://doi.org/10.1016/j.ejso.2016.10.026CrossRefPubMed

47.

Dedivitis RA, Guimaraes AV, Pfuetzenreiter EG Jr, Castro MA (2011) Neck dissection complications. Braz J Otorhinolaryngol 77:65–69. https://doi.org/10.1590/s1808-86942011000100011CrossRefPubMed

48.

Schiefke F, Akdemir M, Weber A, Akdemir D, Singer S, Frerich B (2009) Function, postoperative morbidity, and quality of life after cervical sentinel node biopsy and after selective neck dissection. Head Neck 31:503–512. https://doi.org/10.1002/hed.21001CrossRefPubMed

Title: Occult metastasis is no burden factor in oral squamous cell carcinoma patients when adhering to a standardized approach in neck dissection
Authors: Ann-Kristin Struckmeier
Mayte Buchbender
Tobias Moest
Rainer Lutz
Abbas Agaimy
Marco Kesting
Publication date: 01-01-2024
Publisher: Springer Berlin Heidelberg
Keywords: Neck Dissection
Metastasis
Published in: Clinical Oral Investigations / Issue 1/2024
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-024-05514-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Occult metastasis is no burden factor in oral squamous cell carcinoma patients when adhering to a standardized approach in neck dissection

Abstract

Objectives

Material and methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Material and methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2024

Evolution, current status, and future trends of maxillary skeletal expansion: a bibliometric analysis

Study of aerosol dispersion and control in dental practice

The impact of local and systemic penicillin on antimicrobial properties and growth factor release in platelet-rich fibrin: In vitro study

Methodological quality of evidence-based clinical practice guidelines in cariology

Evaluation of the impact of orthodontists’ smile with malocclusions on social media and professional credibility

In vitro and in vivo evaluation of iRoot BP Plus as a coronal sealing material for regenerative endodontic procedures