Simultaneous evaluation of symptoms, swallowing functions, and patient-reported swallowing difficulties and their correlations with ingestion status during definitive chemoradiotherapy for oropharyngeal and hypopharyngeal cancer

Abstract

Purpose

To clarify the correlations among symptoms, swallowing functions, and ingestion status and to validate a method of swallowing evaluation during chemoradiotherapy (CRT) for head and neck cancer.

Methods

Oropharyngeal and hypopharyngeal cancer patients who were to receive definitive CRT as initial treatment were included in this prospective, single-center, observational study. The Functional Oral Intake Scale (FOIS) for ingestion status and grades of symptoms (dryness, dysgeusia, mucositis, and the analgesic ladder); the Yale Pharyngeal Residue Severity Rating Scale on fiberoptic endoscopic evaluation of swallowing (FEES) and the Penetration-Aspiration Scale (PAS) on videofluoroscopic (VF) evaluation for swallowing functions; and the 10-item Eating Assessment Tool (EAT-10) questionnaire were assessed at 5 time points unless the participant refused. The FEES and VF evaluation findings at each point were also compared.

Results

There were 38 participants. Dysgeusia, mucositis, and pain grade, as well as the FOIS score, were the worst at 70 Gy and then improved after treatment. The improvements of pharyngeal residue and the PAS after treatment were limited. The EAT-10 and the pain ladder were highly correlated with the FOIS changes at many time points. The VF evaluation rate dropped after 40 Gy, whereas the FEES rate remained high. There were good correlations between pharyngeal residue and the PAS at 0 Gy, 70 Gy, and 3 months.

Conclusion

The EAT-10 and pain reflected the FOIS score changes well, while two swallowing evaluations did not. To avoid aspiration, VF evaluation may not be necessary during CRT because of high correlations with pharyngeal residue on FEES.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

Data availability

The authors have full control of all primary data and agree to allow the journal to review the data if requested.

References

  1. 1.

    Newman LA, Vieira F, Schwiezer V, Samant S, Murry T, Woodson G, Kumar P, Robbins KT (1998) Eating and weight changes following chemoradiation therapy of advanced head and neck cancer. Arch Otolaryngel Head Neck Surg 124:589–592. https://doi.org/10.1001/archotol.124.5.589

    CAS  Article  Google Scholar 

  2. 2.

    Eisbruch A, Lyden T, Bradford CR, Dawson LA, Haxer MJ, Miller AE, Teknos TN, Chepeha DB, Hogikyan ND, Terrell JE, Wolf GT (2002) Objective assessment of swallowing dysfunction and aspiration after radiation concurrent with chemotherapy for head-and-neck cancer. Int J Radiat Oncol Biol Phys 53:23–28. https://doi.org/10.1016/s0360-3016(02)02712-8

    Article  PubMed  Google Scholar 

  3. 3.

    Eisbruch A, Schwartz M, Rasch C, Vineberg K, Damen E, Van As CJ, Marsh R, Pameijer FA, Balm AJ (2004) Dysphagia and aspiration after chemoradiotherapy for head-and-neck cancer: which anatomic structures are affected and can be spared by IMRT? Int J Radiat Oncol Biol Phys 60:1425–1439. https://doi.org/10.1016/j.ijrobp.2004.05.050

    Article  PubMed  Google Scholar 

  4. 4.

    Logemann JA, Pauloski BR, Rademaker AW, Colangelo LA (1997) Speech and swallowing rehabilitation for head and neck cancer patients. Oncology (Williston Park) 11:651–6, 659

    CAS  Google Scholar 

  5. 5.

    Carroll WR, Locher JL, Canon CL, Bohannon IA, McColloch NL, Magnuson JS (2008) Pretreatment swallowing exercises improve swallow function after chemoradiation. Laryngoscope 118:39–43. https://doi.org/10.1097/MLG.0b013e31815659b0

    Article  PubMed  Google Scholar 

  6. 6.

    Kotz T, Federman AD, Kao J, Milman L, Packer S, Lopez-Prieto C, Forsythe K, Genden EM (2012) Prophylactic swallowing exercises in patients with head and neck cancer undergoing chemoradiation: a randomized trial. Arch Otolaryngol Head Neck Surg 138:376–382. https://doi.org/10.1001/archoto.2012.187

    Article  PubMed  Google Scholar 

  7. 7.

    Carnaby-Mann G, Crary MA, Schmalfuss I, Amdur R (2012) “Pharyngocise”: randomized controlled trial of preventative exercises to maintain muscle structure and swallowing function during head-and-neck chemoradiotherapy. Int J Radiat Oncol Biol Phys 83:210–219. https://doi.org/10.1016/j.ijrobp.2011.06.1954

    Article  PubMed  Google Scholar 

  8. 8.

    Cereda E, Cappello S, Colombo S, Klersy C, Imarisio I, Turri A, Caraccia M, Borioli V, Monaco T, Benazzo M, Pedrazzoli P, Corbella F, Caccialanza R (2018) Nutritional counseling with or without systematic use of oral nutritional supplements in head and neck cancer patients undergoing radiotherapy. Radiother Oncol 126:81–88. https://doi.org/10.1016/j.radonc.2017.10.015

    Article  PubMed  Google Scholar 

  9. 9.

    Porto de Toledo I, Pantoja LLQ, Luchesi KF, Assad DX, De Luca CG, Guerra ENS (2019) Deglutition disorders as a consequence of head and neck cancer therapies: a systematic review and meta-analysis. Support Care Cancer 27:3681–3700. https://doi.org/10.1007/s00520-019-04920-z

    Article  PubMed  Google Scholar 

  10. 10.

    Wu CH, Hsiao TY, Chen JC, Chang YC, Lee SY (1997) Evaluation of swallowing safety with fiberoptic endoscope: comparison with videofluoroscopic technique. Laryngoscope 107:396–401. https://doi.org/10.1097/00005537-199703000-00023

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Platteaux N, Dirix P, Dejaeger E, Nuyts S (2010) Dysphagia in head and neck cancer patients treated with chemoradiotherapy. Dysphagia 25:139–152. https://doi.org/10.1007/s00455-009-9247-7

    Article  PubMed  Google Scholar 

  12. 12.

    Kelly AM, Drinnan MJ, Leslie P (2007) Assessing penetration and aspiration: how do videofluoroscopy and fiberoptic endoscopic evaluation of swallowing compare? Laryngoscope 117:1723–1727. https://doi.org/10.1097/MLG.0b013e318123ee6a

    Article  PubMed  Google Scholar 

  13. 13.

    Kelly AM, Leslie P, Beale T, Payten C, Drinnan MJ (2006) Fibreoptic endoscopic evaluation of swallowing and videofluoroscopy: does examination type influence perception of pharyngeal residue severity? Clin Otolaryngol 31:425–432. https://doi.org/10.1111/j.1749-4486.2006.01292.x

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Teguh DN, Levendag PC, Noever I, van Rooij P, Voet P, van der Est H, Sipkema D, Sewnaik A, Baatenburg de Jong RJ, de la Bije D, Schmitz PI (2008) Treatment techniques and site considerations regarding dysphagia-related quality of life in cancer of the oropharynx and nasopharynx. Int J Radiat Oncol Biol Phys 72:1119–1127. https://doi.org/10.1016/j.ijrobp.2008.02.061

    Article  PubMed  Google Scholar 

  15. 15.

    Teguh DN, Levendag PC, Sewnaik A, Hakkesteegt MM, Noever I, Voet P, van der Est H, Sipkema D, van Rooij P, Baatenburg de Jong RJ, Schmitz PI (2008) Results of fiberoptic endoscopic evaluation of swallowing vs. radiation dose in the swallowing muscles after radiotherapy of cancer in the oropharynx. Radiother Oncol 89:57–63. https://doi.org/10.1016/j.radonc.2008.07.012

    Article  PubMed  Google Scholar 

  16. 16.

    Hutcheson KA, Lewis JS, Barringer DA, Lisec A, Gunn GB, Moore MW, Holsinger FC (2012) Late dysphagia after radiotherapy-based treatment of head and neck cancer. Cancer 118:5793–5799. https://doi.org/10.1002/cncr.27631

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Ganzer H, Touger-Decker R, Parrott JS, Murphy BA, Epstein JB, Huhmann MB (2013) Symptom burden in head and neck cancer: impact upon oral energy and protein intake. Support Care Cancer 21:495–503. https://doi.org/10.1007/s00520-012-1542-4

    Article  PubMed  Google Scholar 

  18. 18.

    Pauloski BR, Rademaker AW, Logemann JA, Lazarus CL, Newman L, Hamner A, MacCracken E, Gaziano J, Stachowiak L (2002) Swallow function and perception of dysphagia in patients with head and neck cancer. Head Neck 24:555–565. https://doi.org/10.1002/hed.10092

    Article  PubMed  Google Scholar 

  19. 19.

    Jensen K, Bonde Jensen A, Grau C (2006) The relationship between observer-based toxicity scoring and patient assessed symptom severity after treatment for head and neck cancer. A correlative cross sectional study of the DAHANCA toxicity scoring system and the EORTC quality of life questionnaires. Radiother Oncol 78:298–305

    Article  Google Scholar 

  20. 20.

    Nguyen NP, Frank C, Moltz CC, Vos P, Smith HJ, Karlsson U, Dutta S, Midyett A, Barloon J, Sallah S (2005) Impact of dysphagia on quality of life after treatment of head-and-neck cancer. Int J Radiat Oncol Biol Phys 61:772–778. https://doi.org/10.1016/j.ijrobp.2004.06.017

    Article  PubMed  Google Scholar 

  21. 21.

    Eisbruch A, Kim HM, Terrell JE, Marsh LH, Dawson LA, Ship JA (2001) Xerostomia and its predictors following parotid-sparing irradiation of head-and-neck cancer. Int J Radiat Oncol Biol Phys 50:695–704. https://doi.org/10.1016/s0360-3016(01)01512-7

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Feng FY, Kim HM, Lyden TH, Haxer MJ, Feng M, Worden FP, Chepeha DB, Eisbruch A (2007) Intensity-modulated radiotherapy of head and neck cancer aiming to reduce dysphagia: early dose-effect relationships for the swallowing structures. Int J Radiat Oncol Biol Phys 68:1289–1298. https://doi.org/10.1016/j.ijrobp.2007.02.049

    Article  PubMed  Google Scholar 

  23. 23.

    Neubauer PD, Rademaker AW, Leder SB (2015) The Yale Pharyngeal Residue Severity Rating Scale: an anatomically defined and image-based tool. Dysphagia 30:521–528. https://doi.org/10.1007/s00455-015-9631-4

    Article  PubMed  Google Scholar 

  24. 24.

    Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL (1996) A penetration-aspiration scale. Dysphagia 11:93–98. https://doi.org/10.1007/bf00417897

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    National Cancer Institute. Common Terminology Criteria for Adverse Events version 3.0 and version 4.0 (CTCAE) (2010) National Cancer Institute Cancer Therapy Evaluation Program website. http://ctep.cancer.gov/protocolDevelopment/electronic_applications/ctc.htm

  26. 26.

    Jadad AR, Browman GP (1995) The WHO analgesic ladder for cancer pain management. Stepping up the quality of its evaluation. JAMA 274:1870–1873

    CAS  Article  Google Scholar 

  27. 27.

    Belafsky PC, Mouadeb DA, Rees CJ, Pryor JC, Postma GN, Allen J, Leonard RJ (2008) Validity and reliability of the Eating Assessment Tool (EAT-10). Ann Otol Rhinol Laryngol 117:919–924. https://doi.org/10.1177/000348940811701210

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Crary MA, Mann GD, Groher ME (2005) Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 86:1516–1520. https://doi.org/10.1016/j.apmr.2004.11.049

    Article  PubMed  Google Scholar 

  29. 29.

    Kalavrezos N, Cotrufo S, Govender R, Rogers P, Pirgousis P, Balasundram S, Lalabekyan B, Liew C (2014) Factors affecting swallow outcome following treatment for advanced oral and oropharyngeal malignancies. Head Neck 36:47–54. https://doi.org/10.1002/hed.23262

    Article  PubMed  Google Scholar 

  30. 30.

    Messing BP, Ward EC, Lazarus CL, Kim M, Zhou X, Silinonte J, Gold D, Harrer K, Ulmer K, Merritt S, Neuner G, Levine M, Blanco R, Saunders J, Califano J (2017) Prophylactic swallow therapy for patients with head and neck cancer undergoing chemoradiotherapy: a randomized trial. Dysphagia 32:487–500. https://doi.org/10.1007/s00455-017-9790-6

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Moroney LB, Helios J, Ward EC, Crombie J, Burns CL, Yeo SQ, Pelecanos A, Spurgin AL, Blake C, Kenny L, Chua B, Hughes BGM (2019) Radiotherapy for cutaneous head and neck cancer and parotid tumours: a prospective investigation of treatment-related acute swallowing and toxicity patterns. Support Care Cancer 27:573–581. https://doi.org/10.1007/s00520-018-4352-5

    Article  PubMed  Google Scholar 

  32. 32.

    Rogus-Pulia NM, Pierce MC, Mittal BB, Zecker SG, Logemann JA (2014) Changes in swallowing physiology and patient perception of swallowing function following chemoradiation for head and neck cancer. Dysphagia 29:223–233. https://doi.org/10.1007/s00455-013-9500-y

    Article  PubMed  Google Scholar 

  33. 33.

    Vainshtein JM, Samuels S, Tao Y, Lyden T, Haxer M, Spector M, Schipper M, Eisbruch A (2016) Impact of xerostomia on dysphagia after chemotherapy-intensity-modulated radiotherapy for oropharyngeal cancer: prospective longitudinal study. Head Neck 38(Suppl 1):E1605–E1612. https://doi.org/10.1002/hed.24286

    Article  PubMed  Google Scholar 

  34. 34.

    Nevens D, Goeleven A, Duprez F, Laenen A, Dejaeger E, De Neve W, Nuyts S (2018) Correlation of patient- and physician-scored dysphagia with videofluoroscopies in patients treated with radiotherapy for head and neck cancer. Dysphagia 33:684–690. https://doi.org/10.1007/s00455-018-9888-5

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Hedström J, Tuomi L, Finizia C, Olsson C (2018) Correlations between patient-reported dysphagia screening and penetration-aspiration scores in head and neck cancer patient post-oncological treatment. Dysphagia 33:206–215. https://doi.org/10.1007/s00455-017-9847-6

    Article  PubMed  Google Scholar 

  36. 36.

    Patterson J, Toft K, McAuley F, King E, McLachlan K, Roe JWG, Wells M (2019) Feasibility and outcomes of fibreoptic endoscopic evaluation of swallowing following prophylactic swallowing rehabilitation in head and neck cancer. Clin Otolaryngol 44:549–556. https://doi.org/10.1111/coa.13331

    Article  PubMed  Google Scholar 

  37. 37.

    Kirsh E, Naunheim M, Holman A, Kammer R, Varvares M, Goldsmith T (2019) Patient-reported versus physiologic swallowing outcomes in patients with head and neck cancer after chemoradiation. Laryngoscope 129:2059–2064. https://doi.org/10.1002/lary.27610

    Article  PubMed  Google Scholar 

  38. 38.

    Shapira-Galitz Y, Shoffel-Havakuk H, Halperin D, Lahav MY (2019) Correlation between pharyngeal residue and aspiration in fiber-optic endoscopic evaluation of swallowing: an observational study. Arch Phys Med Rehabil 100:488–494. https://doi.org/10.1016/j.apmr.2018.05.028

    Article  PubMed  Google Scholar 

  39. 39.

    Wilkie JR, Mierzwa ML, Yao J, Eisbruch A, Feng M, Weybrune G, Chen X, Holevinski L, Mayo CS (2019) Big data analysis of associations between patient reported outcomes, observer reported toxicities, and overall quality of life in head and neck cancer patients treated with radiation therapy. Radiother Oncol 137:167–174. https://doi.org/10.1016/j.radonc.2019.04.030

    Article  PubMed  Google Scholar 

  40. 40.

    Martin A, Murray L, Sethugavalar B, Buchan C, Williams GF, Sen M, Prestwich RJD (2018) Changes in patient-reported swallow function in the long term after chemoradiotherapy for oropharyngeal carcinoma. Clin Oncol (R Coll Radiol) 30:756–763. https://doi.org/10.1016/j.clon.2018.06.013

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Contributions

Ryo Ishii, Kengo Kato, Ai Hirano, and Yukio Katori contributed to the conception and study design, data acquisition, analysis, and drafting of the manuscript. Takeshi Sato contributed to the data acquisition and analysis. Akira Ohkoshi and Takenori Ogawa contributed to the analysis and drafting of the manuscript. All authors revised the article critically and approved the final version for publication.

Corresponding author

Correspondence to Ryo Ishii.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Bioethics Committee of the Tohoku University School of Medicine (number 2014-1-274).

Consent to participate

Written, informed consent was obtained from all individual participants in this study.

Consent to publication

Not applicable

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

Ishii, R., Kato, K., Ohkoshi, A. et al. Simultaneous evaluation of symptoms, swallowing functions, and patient-reported swallowing difficulties and their correlations with ingestion status during definitive chemoradiotherapy for oropharyngeal and hypopharyngeal cancer. Support Care Cancer (2020). https://doi.org/10.1007/s00520-020-05570-2

Download citation

Keywords

  • Swallowing difficulties
  • Swallowing evaluation
  • Ingestion status
  • Chemoradiotherapy
  • Head and neck cancer