Dysphagia

pp 1–16 | Cite as

Longitudinal Evaluation of Swallowing with Videofluoroscopy in Patients with Locally Advanced Head and Neck Cancer After Chemoradiation

  • Ekaterini Xinou
  • Ioannis Chryssogonidis
  • Anna Kalogera-Fountzila
  • Dimitra Panagiotopoulou-Mpoukla
  • Athanasia Printza
Original Article

Abstract

The aim of this study was to investigate the prevalence, severity, and pattern of evolution of swallowing impairments encountered in head and neck cancer (HNC) patients before and after chemoradiation (CRT) with videofluoroscopy of swallowing study (VFSS), using the modified barium swallow impairment profile (MBSImP) protocol and scoring system, and to determine the appropriate time points in which these patients should undergo VFSS post-CRT. A prospective cohort of 69 patients with locally advanced HNC underwent VFSS with the MBSImP protocol at 5 evaluation points: pre-CRT, and 1, 3, 6, and 12 months post-CRT. VFSS was scored with MBSImP, penetration–aspiration scale (PAS), and swallowing performance status (SPS) scale. Statistical analysis was performed only for the 12-month disease-free subset of patients. MBSImP, PAS, and SPS scale scores reached their peak at 3 months post-CRT and improved at 6–12 months, but without returning at pre-treatment levels. Base of tongue retraction, initiation of pharyngeal swallow, epiglottic movement, laryngeal vestibule closure, and laryngeal elevation were the most frequently observed impaired MBSImP components. Epiglottic movement significantly improved (p = 0.009) and laryngeal vestibule closure significantly deteriorated (p = 0.042) over time (Friedman test). Severe swallowing deficits and high aspiration rates are observed in HNC patients pre-CRT, which further deteriorate post-CRT, peak at 3 months, and despite slight improvement, persist over time. We suggest that these patients, regardless of the presence of subjective dysphagia, should undergo VFSS both before and 3 months post-CRT, and also if possible, 1 month post-CRT, in order to facilitate implementation of early swallowing rehabilitation.

Keywords

Videofluoroscopy of swallowing Modified barium swallow MBSImP Dysphagia Head and neck cancer Chemoradiotherapy Deglutition Deglutition disorders 

Notes

Acknowledgements

We thank Professor Bonnie Martin-Harris, Professor Nicholas Stergiou, and Dr. Georgia Lazaraki for assistance with language editing and comments that greatly improved the manuscript.

Compliance with Ethical Standards

Conflict of interest

Ekaterini Xinou, Ioannis Chryssogonidis, Anna Kalogera-Fountzila, Dimitra Panagiotopoulou-Mpoukla and Athanasia Printza declares that they have no conflict of interest.

Ethical Approval

All procedures performed this study 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. This article does not contain any studies with animals performed by any of the authors.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

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Supplementary material 1 (DOCX 18 kb)
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Supplementary material 2 (DOCX 17 kb)
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Supplementary material 3 (DOCX 15 kb)
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Supplementary material 4 (DOCX 15 kb)
455_2018_9889_MOESM5_ESM.docx (19 kb)
Supplementary material 5 (DOCX 18 kb)

References

  1. 1.
    Forastiere AA, Goepfert H, Maor M, et al. Concurrent chemotherapy and radiotherapy for organ preservation in advanced laryngeal cancer. N Engl J Med. 2003;349(22):2091–8.  https://doi.org/10.1056/NEJMoa031317.CrossRefPubMedGoogle Scholar
  2. 2.
    Frowen JJ, Perry AR. Swallowing outcomes after radiotherapy for head and neck cancer: a systematic review. Head Neck. 2006;28(10):932–44.  https://doi.org/10.1002/hed.20438.CrossRefPubMedGoogle Scholar
  3. 3.
    Gluck I, Agbulos K, Chepeha DB, et al. Validation of the common terminology criteria for adverse events v3.0 (CTCAE) for dysphagia after chemo-radiotherapy (RT) for head and neck (HN) cancer. Int J Radiat Oncol. 2008;72(1):S139–40.  https://doi.org/10.1016/j.ijrobp.2008.06.457.CrossRefGoogle Scholar
  4. 4.
    Frymark T. NOMS integration eases clinicians’ reporting burden. ASHA Lead. 2016;21(6):40.  https://doi.org/10.1044/leader.OTP.21062016.40.CrossRefGoogle Scholar
  5. 5.
    O’Neil KH, Purdy M, Falk J, Gallo L. The dysphagia outcome and severity scale. Dysphagia. 1999;14(3):139–45.  https://doi.org/10.1007/PL00009595.CrossRefPubMedGoogle Scholar
  6. 6.
    Hutcheson KA, Barrow MP, Barringer DA, et al. Dynamic imaging grade of swallowing toxicity (DIGEST): scale development and validation. Cancer. 2017;123(1):62–70.  https://doi.org/10.1002/cncr.30283.CrossRefPubMedGoogle Scholar
  7. 7.
    Hutcheson KA, Lewin JS. Functional outcomes after chemoradiotherapy of laryngeal and pharyngeal cancers. Curr Oncol Rep. 2012;14:158–65.  https://doi.org/10.1007/s11912-012-0216-1.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Pauloski BR, Rademaker AW, Logemann JA, et al. Relationship between swallow motility disorders on videofluorography and oral intake in patients treated for head and neck cancer with radiotherapy with or without chemotherapy. Head Neck. 2006;28(12):1069–76.  https://doi.org/10.1002/hed.20459.CrossRefPubMedGoogle Scholar
  9. 9.
    Nguyen NP, Moltz CC, Frank C, et al. Dysphagia following chemoradiation for locally advanced head and neck cancer. Ann Oncol. 2004;15:383–8.  https://doi.org/10.1093/annonc/mdh101.CrossRefPubMedGoogle Scholar
  10. 10.
    Nguyen NP, Frank C, Moltz CC, et al. Aspiration rate following chemoradiation for head and neck cancer: an underreported occurrence. Radiother Oncol. 2006;80(3):302–6.  https://doi.org/10.1016/j.radonc.2006.07.031.CrossRefPubMedGoogle Scholar
  11. 11.
    Kotz T, Costello R, Li Y, Posner MR. Swallowing dysfunction after chemoradiation for advanced squamous cell carcinoma of the head and neck. Head Neck. 2004;26(4):365–72.  https://doi.org/10.1002/hed.10385.CrossRefPubMedGoogle Scholar
  12. 12.
    Bleier BS, Levine MS, Mick R, et al. Dysphagia after chemoradiation: analysis by modified barium swallow. Ann Otol Rhinol Laryngol. 2007;116(11):837–41.CrossRefPubMedGoogle Scholar
  13. 13.
    Goguen LA, Posner MR, Norris CM, et al. Dysphagia after sequential chemoradiation therapy for advanced head and neck cancer. Otolaryngol neck Surg. 2006;134(6):916–22.  https://doi.org/10.1016/j.otohns.2006.02.001.CrossRefGoogle Scholar
  14. 14.
    Eisbruch A, Lyden T, Bradford CR, et al. Objective assessment of swallowing dysfunction and aspiration after radiation concurrent with chemotherapy for head-and-neck cancer. Int J Radiat Oncol Biol Phys. 2002;53(1):23–8.  https://doi.org/10.1016/S0360-3016(02)02712-8.CrossRefPubMedGoogle Scholar
  15. 15.
    Rogus-Pulia NM, Pierce MC, Mittal BB, Zecker SG, Logemann JA. Changes in swallowing physiology and patient perception of swallowing function following chemoradiation for head and neck cancer. Dysphagia. 2014;29(2):223–33.  https://doi.org/10.1007/s00455-013-9500-y.CrossRefPubMedGoogle Scholar
  16. 16.
    Logemann JA, Pauloski BR, Rademaker AW, et al. Swallowing disorders in the first year after radiation and chemoradiation. Head Neck. 2008;30(2):148–58.  https://doi.org/10.1002/hed.20672.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Logemann JA, Rademaker AW, Pauloski BR, et al. Site of disease and treatment protocol as correlates of swallowing function in patients with head and neck cancer treated with chemoradiation. Head Neck. 2006;28(1):64–73.  https://doi.org/10.1002/hed.20299.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Cartmill B, Cornwell P, Ward E, Davidson W, Porceddu S. A prospective investigation of swallowing, nutrition, and patient-rated functional impact following altered fractionation radiotherapy with concomitant boost for oropharyngeal cancer. Dysphagia. 2012;27(1):32–45.  https://doi.org/10.1007/s00455-011-9333-5.CrossRefPubMedGoogle Scholar
  19. 19.
    Salama JK, Stenson KM, List MA, et al. Characteristics associated with swallowing changes after concurrent chemotherapy and radiotherapy in patients with head and neck cancer. Arch Otolaryngol Head Neck Surg. 2008;134(10):1060–5.CrossRefPubMedGoogle Scholar
  20. 20.
    Pauloski BR, Rademaker AW, Logemann JA, et al. Swallow function and perception of dysphagia in patients with head and neck cancer. Head Neck. 2002;24(6):555–65.  https://doi.org/10.1002/hed.10092.CrossRefPubMedGoogle Scholar
  21. 21.
    Newman LA, Robbins KT, Logemann JA, et al. Swallowing and speech ability after treatment for head and neck cancer with targeted intraarterial versus intravenous chemoradiation. Head Neck. 2002;24(1):68–77.CrossRefPubMedGoogle Scholar
  22. 22.
    Feng FY, Kim HM, Lyden TH, et al. Intensity-modulated chemoradiotherapy aiming to reduce dysphagia in patients with oropharyngeal cancer: clinical and functional results. J Clin Oncol. 2010;28(16):2732–8.  https://doi.org/10.1200/JCO.2009.24.6199.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Hutcheson KA, Lewin JS, Holsinger FC, et al. Long-term functional and survival outcomes after induction chemotherapy and risk-based definitive therapy for locally advanced squamous cell carcinoma of the head and neck. Head Neck. 2014;36(4):474–80.  https://doi.org/10.1002/hed.23330.CrossRefPubMedGoogle Scholar
  24. 24.
    Pauloski BR, Rademaker AW, Logemann JA, Discekici-Harris M, Mittal BB. Comparison of swallowing function after intensity-modulated radiation therapy and conventional radiotherapy for head and neck cancer. Head Neck. 2015;37(11):1575–82.  https://doi.org/10.1002/hed.23796.CrossRefPubMedGoogle Scholar
  25. 25.
    Kraaijenga SAC, Oskam IM, Van Der Molen L, Hamming-Vrieze O, Hilgers FJM, Van Den Brekel MWM. Evaluation of long term (10-years+) dysphagia and trismus in patients treated with concurrent chemo-radiotherapy for advanced head and neck cancer. Oral Oncol. 2015;51(8):787–94.  https://doi.org/10.1016/j.oraloncology.2015.05.003.CrossRefPubMedGoogle Scholar
  26. 26.
    Platteaux N, Dirix P, Dejaeger E, Nuyts S. Dysphagia in head and neck cancer patients treated with chemoradiotherapy. Dysphagia. 2010;25(2):139–52.  https://doi.org/10.1007/s00455-009-9247-7.CrossRefPubMedGoogle Scholar
  27. 27.
    Wall LR, Ward EC, Cartmill B, Hill AJ. Physiological changes to the swallowing mechanism following (chemo)radiotherapy for head and neck cancer: a systematic review. Dysphagia. 2013;28(4):481–93.  https://doi.org/10.1007/s00455-013-9491-8.CrossRefPubMedGoogle Scholar
  28. 28.
    Agarwal J, Palwe V, Dutta D, et al. Objective assessment of swallowing function after definitive concurrent (Chemo)radiotherapy in patients with head and neck cancer. Dysphagia. 2011;26(4):399–406.  https://doi.org/10.1007/s00455-011-9326-4.CrossRefPubMedGoogle Scholar
  29. 29.
    Frowen J, Cotton S, Corry J, Perry A. Impact of demographics, tumor characteristics, and treatment factors on swallowing after (chemo)radiotherapy for head and neck cancer. Head Neck. 2010;32(4):513–28.  https://doi.org/10.1002/hed.21218.PubMedGoogle Scholar
  30. 30.
    Martin-Harris B, McFarland D, Hill EG, et al. Respiratory-swallow training in patients with head and neck cancer. Arch Phys Med Rehabil. 2015;96(5):885–93.  https://doi.org/10.1016/j.apmr.2014.11.022.CrossRefPubMedGoogle Scholar
  31. 31.
    Huckabee ML. New Zealand index for multidisciplinary evaluation of swallowing. 2017. https://bilateralstrokedysphagia.wikispaces.com/file/view/NZIMES.pdf/170039549/NZIMES.pdf. Accessed 1 Dec 2017.
  32. 32.
    Rademaker AW, Pauloski BR, Logemann JA, Shanahan TK. Oropharyngeal swallow efficiency as a representative measure of swallowing function. J Speech Hear Res. 1994;37(2):314–25.CrossRefPubMedGoogle Scholar
  33. 33.
    Martin-Harris B, Brodsky MB, Michel Y, et al. MBS measurement tool for swallow impairment-MBSimp: establishing a standard. Dysphagia. 2008;23(4):392–405.  https://doi.org/10.1007/s00455-008-9185-9.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Gullung JL, Hill EG, Castell DO, Martin-Harris B. Oropharyngeal and esophageal swallowing impairments: their association and the predictive value of the modified barium swallow impairment profile and combined multichannel intraluminal impedance-esophageal manometry. Ann Otol Rhinol Laryngol. 2012;121(11):738–45.CrossRefPubMedGoogle Scholar
  35. 35.
    Arrese LC, Carrau R, Plowman EK. Relationship between the eating assessment tool-10 and objective clinical ratings of swallowing function in individuals with head and neck cancer. Dysphagia. 2017;32(1):83–9.  https://doi.org/10.1007/s00455-016-9741-7.CrossRefPubMedGoogle Scholar
  36. 36.
    Su HK, Khorsandi A, Silberzweig J, et al. Temporal and physiologic measurements of deglutition in the upright and supine position with videofluoroscopy (VFS) in healthy subjects. Dysphagia. 2015;30(4):438–44.  https://doi.org/10.1007/s00455-015-9620-7.CrossRefPubMedGoogle Scholar
  37. 37.
    Hoffman MR, Jones CA, Geng Z, et al. Classification of high-resolution manometry data according to videofluoroscopic parameters using pattern recognition. Otolaryngol Head Neck Surg. 2013;149(1):126–33.  https://doi.org/10.1177/0194599813489506.CrossRefPubMedGoogle Scholar
  38. 38.
    Van Der Laan BFAM, Van Der Laan HP, Bijl HP, et al. Acute symptoms during the course of head and neck radiotherapy or chemoradiation are strong predictors of late dysphagia. Radiother Oncol. 2015;115(1):56–62.  https://doi.org/10.1016/j.radonc.2015.01.019.CrossRefPubMedGoogle Scholar
  39. 39.
    Hutcheson KA, Lewin JS, Barringer DA, et al. Late dysphagia after radiotherapy-based treatment of head and neck cancer. Cancer. 2012;118(23):5793–9.  https://doi.org/10.1002/cncr.27631.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Zancan M, Luchesi KF, Mituuti CT, Furkim AM. Onset locations of the pharyngeal phase of swallowing: meta-analysis. CoDAS. 2017;29(2):e20160067.  https://doi.org/10.1590/2317-1782/20172016067.CrossRefPubMedGoogle Scholar
  41. 41.
    Bonilha HS, Humphries K, Blair J, et al. Radiation exposure time during MBSS: influence of swallowing impairment severity, medical diagnosis, clinician experience, and standardized protocol use. Dysphagia. 2013;28(1):77–85.  https://doi.org/10.1007/s00455-012-9415-z.CrossRefPubMedGoogle Scholar
  42. 42.
    Bonilha HS, Blair J, Carnes B, et al. Preliminary investigation of the effect of pulse rate on judgments of swallowing impairment and treatment recommendations. Dysphagia. 2013;28(4):528–38.  https://doi.org/10.1007/s00455-013-9463-z.CrossRefPubMedGoogle Scholar
  43. 43.
    Hutcheson KA, Yuk MM, Holsinger FC, Gunn GB, Lewin JS. Late radiation-associated dysphagia with lower cranial neuropathy in long-term oropharyngeal cancer survivors: video case reports. Irish J, ed. Head Neck. 2015;37(4):E56–62.  https://doi.org/10.1002/hed.23840.CrossRefPubMedGoogle Scholar
  44. 44.
    Drink testing methods—IDDSI. http://iddsi.org/framework/drink-testing-methods/. Accessed 1 Nov 2017.
  45. 45.
    Food testing methods—IDDSI. http://iddsi.org/framework/food-testing-methods/. Accessed 1 Nov 2017.
  46. 46.
    Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11(2):93–8.CrossRefPubMedGoogle Scholar
  47. 47.
    Karnell MP, MacCracken E. A database information storage and reporting system for videofluorographic oropharyngeal motility (OPM) swallowing evaluations. Am J Speech-Language Pathol. 1994;3(2):54.  https://doi.org/10.1044/1058-0360.0302.54.CrossRefGoogle Scholar
  48. 48.
    Nguyen NP, Smith HJ, Sallah S. Evaluation and management of swallowing dysfunction following chemoradiation for head and neck cancer. Curr Opin Otolaryngol Head Neck Surg. 2007;15(2):130–3.  https://doi.org/10.1097/MOO.0b013e32801da0e8.CrossRefPubMedGoogle Scholar
  49. 49.
    Steele CM. Mapping Bracco’s Varibar® barium products to the IDDSI Framework. 2017. http://iddsi.org/wp-content/uploads/2017/07/Mapping-Varibar_Short-version.pdf. Accessed 8 Nov 2017.
  50. 50.
    Steele CM, Molfenter SM, Péladeau-Pigeon M, Stokely S. Challenges in preparing contrast media for videofluoroscopy. Dysphagia. 2013;28(3):464–7.  https://doi.org/10.1007/s00455-013-9476-7.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Jaffer NM, Ng E, Au FW-F, Steele CM. Fluoroscopic evaluation of oropharyngeal dysphagia: anatomic, technical, and common etiologic factors. Am J Roentgenol. 2015;204(1):49–58.  https://doi.org/10.2214/AJR.13.12374.CrossRefGoogle Scholar
  52. 52.
    Graner DE, Foote RL, Kasperbauer JL, et al. Swallow function in patients before and after intra-arterial chemoradiation. Laryngoscope. 2003;113:573–9.CrossRefPubMedGoogle Scholar
  53. 53.
    Carroll WR, Locher JL, Canon CL, Bohannon IA, McColloch NL, Magnuson JS. Pretreatment swallowing exercises improve swallow function after chemoradiation. Laryngoscope. 2008;118:39–43.  https://doi.org/10.1097/MLG.0b013e31815659b0.CrossRefPubMedGoogle Scholar
  54. 54.
    Kramer S, Newcomb M, Hessler J, Siddiqui F. Prophylactic versus reactive PEG tube placement in head and neck cancer. Otolaryngol neck Surg. 2014;150(3):407–12.  https://doi.org/10.1177/0194599813517081.CrossRefGoogle Scholar
  55. 55.
    Perry A, Lee SH, Cotton S, Kennedy C. Therapeutic exercises for affecting post-treatment swallowing in people treated for advanced-stage head and neck cancers. Cochrane Database Syst Rev. 2016.  https://doi.org/10.1002/14651858.CD011112.pub2.Google Scholar
  56. 56.
    Patterson JM, McColl E, Carding PN, Hildreth AJ, Kelly C, Wilson JA. Swallowing in the first year after chemoradiotherapy for head and neck cancer: clinician- and patient-reported outcomes. Head Neck. 2014;36(3):352–8.  https://doi.org/10.1002/hed.CrossRefPubMedGoogle Scholar
  57. 57.
    Stenson KM, MacCracken E, List M, et al. Swallowing function in patients with head and neck cancer prior to treatment. Arch Otolaryngol Head Neck Surg. 2000;126(3):371–7.CrossRefPubMedGoogle Scholar
  58. 58.
    Rosen A, Rhee TH, Kaufman R. Prediction of aspiration in patients with newly diagnosed untreated advanced head and neck cancer. Arch Otolaryngol Head Neck Surg. 2001;127:975–9.CrossRefPubMedGoogle Scholar
  59. 59.
    Jensen K, Lambertsen K, Grau C. Late swallowing dysfunction and dysphagia after radiotherapy for pharynx cancer: frequency, intensity and correlation with dose and volume parameters. Radiother Oncol. 2007;85(1):74–82.  https://doi.org/10.1016/j.radonc.2007.06.004.CrossRefPubMedGoogle Scholar
  60. 60.
    Langerman A, Maccracken E, Kasza K, Haraf DJ, Vokes EE, Stenson KM. Aspiration in chemoradiated patients with head and neck cancer. Arch Otolaryngol Head Neck Surg. 2007;133(12):1289–95.  https://doi.org/10.1001/archotol.133.12.1289.CrossRefPubMedGoogle Scholar
  61. 61.
    Rogus-Pulia NM, Pierce M, Mittal BB, Zecker SG, Logemann J. Bolus effects on patient awareness of swallowing difficulty and swallow physiology after chemoradiation for head and neck cancer. Head Neck. 2015;37(8):1122–9.  https://doi.org/10.1002/hed.23720.CrossRefPubMedGoogle Scholar
  62. 62.
    Morishima Y, Chida K, Watanabe H. Estimation of the dose of radiation received by patient and physician during a videofluoroscopic swallowing study. Dysphagia. 2016;31(4):574–8.  https://doi.org/10.1007/s00455-016-9718-6.CrossRefPubMedGoogle Scholar
  63. 63.
    Wright RE, Boyd CS, Workman A. Radiation doses to patients during pharyngeal videofluoroscopy. Dysphagia. 1998;13(2):113–5.  https://doi.org/10.1007/PL00009554.CrossRefPubMedGoogle Scholar
  64. 64.
    Kim HM, Choi KH, Kim TW. Patients’ radiation dose during videofluoroscopic swallowing studies according to underlying characteristics. Dysphagia. 2013;28(2):153–8.  https://doi.org/10.1007/s00455-012-9424-y.CrossRefPubMedGoogle Scholar
  65. 65.
    Crawley M, Savage P, Oakley F. Patient and operator dose during fluoroscopic examination of swallow mechanism. Br J Radiol. 2004;77(920):654–6.  https://doi.org/10.1259/bjr/22832251.CrossRefPubMedGoogle Scholar
  66. 66.
    Zammit-Maempel I, Chapple CL, Leslie P. Radiation dose in videofluoroscopic swallow studies. Dysphagia. 2007;22(1):13–5.  https://doi.org/10.1007/s00455-006-9031-x.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of RadiologyTheagenio Cancer HospitalThessaloníkiGreece
  2. 2.Department of RadiologyAristotle University of Thessaloniki School of Medicine, AHEPA University HospitalThessaloníkiGreece
  3. 3.First Department of Oto-rhino-laryngologyAristotle University of Thessaloniki School of Medicine, AHEPA University HospitalThessaloníkiGreece

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