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The Effect of Combined Guidance of Botulinum Toxin Injection with Ultrasound, Catheter Balloon, and Electromyography on Neurogenic Cricopharyngeal Dysfunction: A Prospective Study

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Abstract

Background

Cricopharyngeal botulinum toxin (BTX) injection is one of the treatments for neurogenic cricopharyngeal dysfunction (CPD). We conducted this prospective study to investigate the effect and safety of BTX injection for neurogenic CPD with a novel guidance.

Methods

Twenty-one patients with neurogenic CPD whose symptoms did not reduce after conventional swallowing therapy were included in this study. The impact of BTX injection on the swallowing function of the patients was evaluated.

Key Results

After the injection, the Functional Oral Intake Scale (FOIS) score increased in 17 of 21 patients (80.9%), which ranged from 1 to 3 (P < 0.001). Moreover, there was a significant reduction in the UES opening impairment (P < 0.01), UES residual pressure (P < 0.05), duration of UES relaxation, penetration-aspiration scale score (P < 0.05), secretion (P < 0.05), vallecular residue (P < 0.01), and left (P < 0.05) and right (P < 0.05) pyriform sinus residue. With at least 6 months of follow-up, we found that FOIS continued to increase in patients who showed improvement after the injection (i.e., FOIS 5–7 points), while it remained unchanged in patients without improvement after the injection. There were no side effects reported in this study.

Conclusion & Inferences

BTX injection into the cricopharyngeal muscle guided by ultrasound, catheter balloon, and electromyography possibly has a long-lasting effect that can effectively and safely improve the swallowing function of patients with neurogenic CPD.

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References

  1. Yang H, Yi Y, Han Y. Characteristics of cricopharyngeal dysphagia after ischemic stroke. Ann Rehabil Med. 2018;42:204–12. https://doi.org/10.5535/arm.2018.42.2.204.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sivarao DV, Goyal RK. Functional anatomy and physiology of the upper esophageal sphincter. Am J Med. 2000;108(4):27–37. https://doi.org/10.1016/s0002-9343(99)00337-x.

    Article  Google Scholar 

  3. Lang IMSR. An overview of the upper esophageal sphincter. Curr Gastroenterol Rep. 2000;2(3):185–90. https://doi.org/10.1007/s11894-000-0059-z.

    Article  CAS  PubMed  Google Scholar 

  4. Allen JE. Cricopharyngeal function or dysfunction: what’s the deal? Curr Opin Otolaryngol Head Neck Surg. 2016;24(6):494–9. https://doi.org/10.1097/MOO.0000000000000307.

    Article  PubMed  Google Scholar 

  5. Kocdor P, Siegel ER, Tulunay-Ugur OE. Cricopharyngeal dysfunction: a systematic review comparing outcomes of dilatation, botulinum toxin injection, and myotomy. Laryngoscope. 2016;126(1):135–41. https://doi.org/10.1002/lary.25447.

    Article  CAS  PubMed  Google Scholar 

  6. Dou Z, Zu Y, Wen H, Wan G, Jiang L, Hu Y. The effect of different catheter balloon dilatation modes on cricopharyngeal dysfunction in patients with dysphagia. Dysphagia. 2012;27(4):514–20.

    Article  Google Scholar 

  7. Wei X, Yu F, Dai M, Xie C, Wan G, Wang Y, Dou Z. Change in excitability of cortical projection after modified catheter balloon dilatation therapy in brainstem stroke patients with dysphagia: a prospective controlled study. Dysphagia. 2017;32(5):645–56. https://doi.org/10.1007/s00455-017-9810-6.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kelly EAKI, Jaradeh SS, Merati AL, Blumin JH, Bock JM. Botulinum toxin injection for the treatment of upper esophageal sphincter dysfunction. Ann Otol Rhinol Laryngol. 2013;122(2):100–8. https://doi.org/10.1177/000348941312200205.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Lindgren SEO. Cricopharyngeal myotomy in the treatment of dysphagia. Clin Otolaryngol Allied Sci. 1990;15(3):221–7. https://doi.org/10.1111/j.1365-2273.1990.tb00779.x.

    Article  CAS  PubMed  Google Scholar 

  10. Lebo CPUK, Norris FH Jr. Cricopharyngeal myotomy in amyotrophic lateral sclerosis. Laryngoscope. 1976;86(6):862–8. https://doi.org/10.1288/00005537-197606000-00013.

    Article  CAS  PubMed  Google Scholar 

  11. Schneider I, Thumfart WF, Pototschnig C, Eckel HE. Treatment of dysfunction of the cricopharyngeal muscle with botulinum A toxin: introduction of a new, noninvasive method. Ann Otol Rhinol Laryngol. 1994;103(1):31–5. https://doi.org/10.1177/000348949410300105.

    Article  CAS  PubMed  Google Scholar 

  12. Huai J, Hou Y, Guan J, Zhang Y, Wang Y, Zhang X, Zhang Y, Yue S. Botulinum toxin A injection using esophageal balloon radiography combined with CT guidance for the treatment of cricopharyngeal dysphagia. Dysphagia. 2020;35(4):630–5. https://doi.org/10.1007/s00455-019-10070-5.

    Article  PubMed  Google Scholar 

  13. Regan J, Murphy A, Chiang M, McMahon BP, Coughlan T, Walshe M. Botulinum toxin for upper oesophageal sphincter dysfunction in neurological swallowing disorders. Cochrane Database Syst Rev. 2014;5:CD009968. https://doi.org/10.1002/14651858.CD009968.pub2.

    Article  Google Scholar 

  14. Haapaniemi JJ, Laurikainen EA, Pulkkinen J, Marttila RJ. Botulinum toxin in the treatment of cricopharyngeal dysphagia. Dysphagia. 2001;16(3):171–5. https://doi.org/10.1007/s00455-001-0059-7.

    Article  CAS  PubMed  Google Scholar 

  15. Ahsan SF, Meleca RJ, Dworkin JP. Botulinum toxin injection of the cricopharyngeus muscle for the treatment of dysphagia. Otolaryngol Head Neck Surg. 2000;122(5):691–5. https://doi.org/10.1067/mhn.2000.105997.

    Article  CAS  PubMed  Google Scholar 

  16. Alfonsi E, Restivo DA, Cosentino G, De Icco R, Bertino G, Schindler A, Todisco M, Fresia M, Cortese A, Prunetti P, Ramusino MC, Moglia A, Sandrini G, Tassorelli C. Botulinum toxin is effective in the management of neurogenic dysphagia. Clinical-electrophysiological findings and tips on safety in different neurological disorders. Front Pharmacol. 2017;8:80. https://doi.org/10.3389/fphar.2017.00080.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Shaw GY, Searl JP. Botulinum toxin treatment for cricopharyngeal dysfunction. Dysphagia. 2001;16(3):161–7. https://doi.org/10.1007/s00455-001-0074-8.

    Article  CAS  PubMed  Google Scholar 

  18. Restivo DA, Marchese-Ragona R, Lauria G, Squatrito S, Gullo D, Vigneri R. Botulinum toxin treatment for oropharyngeal dysphagia associated with diabetic neuropathy. Diabetes Care. 2006;29(12):2650–3. https://doi.org/10.2337/dc05-2486.

    Article  CAS  PubMed  Google Scholar 

  19. Terre R, Panades A, Mearin F. Botulinum toxin treatment for oropharyngeal dysphagia in patients with stroke. Neurogastroenterol Motil. 2013;25(11):896-e702. https://doi.org/10.1111/nmo.12213.

    Article  CAS  PubMed  Google Scholar 

  20. Kim DY, Park CI, Ohn SH, Moon JY, Chang WH, Park SW. Botulinum toxin type A for poststroke cricopharyngeal muscle dysfunction. Arch Phys Med Rehabil. 2006;87(10):1346–51. https://doi.org/10.1016/j.apmr.2006.06.018.

    Article  PubMed  Google Scholar 

  21. Sellin LC. The action of batulinum toxin at the neuromuscular junction. Med Biol. 1981;59(1):11–20.

    CAS  PubMed  Google Scholar 

  22. Simpson LL. Molecular pharmacology of botulinum toxin and tetanus toxin. Annu Rev Pharmacol Toxicol. 1986;26:427–53. https://doi.org/10.1146/annurev.pa.26.040186.002235.

    Article  CAS  PubMed  Google Scholar 

  23. Restivo DA, Marchese-Ragona R, Patti F, Solaro C, Maimone D, Zappala G, Pavone A. Botulinum toxin improves dysphagia associated with multiple sclerosis. Eur J Neurol. 2011;18(3):486–90. https://doi.org/10.1111/j.1468-1331.2010.03189.x.

    Article  CAS  PubMed  Google Scholar 

  24. Jeong SH, Kim YJ, Kim YJ, Park KD, Kim EJ, Chung JW, Kwon KA, Kim KO, Park DK, Kim JH, Cho JH. Endoscopic botulinum toxin injection for treatment of pharyngeal dysphagia in patients with cricopharyngeal dysfunction. Scand J Gastroenterol. 2018;53(10–11):1201–5. https://doi.org/10.1080/00365521.2018.1506820.

    Article  CAS  PubMed  Google Scholar 

  25. Blitzer A, Brin MF. Use of botulinum toxin for diagnosis and management of cricopharyngeal achalasia. Otolaryngol Head Neck Surg. 1997;116(3):328–30. https://doi.org/10.1016/s0194-5998(97)70267-5.

    Article  CAS  PubMed  Google Scholar 

  26. Krause E, Schirra J, Gurkov R. Botulinum toxin a treatment of cricopharyngeal dysphagia after subarachnoid hemorrhage. Dysphagia. 2008;23(4):406–10. https://doi.org/10.1007/s00455-007-9132-1.

    Article  PubMed  Google Scholar 

  27. Kim MS, Kim GW, Rho YS, Kwon KH, Chung EJ. Office-based electromyography-guided botulinum toxin injection to the cricopharyngeus muscle: optimal patient selection and technique. Ann Otol Rhinol Laryngol. 2017;126(5):349–56. https://doi.org/10.1177/0003489416689469.

    Article  PubMed  Google Scholar 

  28. Wang YC, Shyu SG, Wu CH, Wang TG. Ultrasound-guided injection of botulinum toxin for cricopharyngeal dysphagia. Am J Phys Med Rehabil. 2018;97(10):e102–3. https://doi.org/10.1097/PHM.0000000000000959.

    Article  PubMed  Google Scholar 

  29. Wang YC, Wu CH, Shyu SG, Hsiao MY, Wang TG. Ultrasonography-guided botulinum toxin injection to the cricopharyngeus muscle: a case report and technical notes. Med Ultrasonogr. 2019. https://doi.org/10.11152/mu-2097.

    Article  Google Scholar 

  30. Wei P, Xu Y, Zhang Z, Zhang S, Lv Z. Treatment for upper esophageal sphincter dysfunction in a patient with poststroke dysphagia: a case report. Medicine (Baltimore). 2019;98(13):e14988. https://doi.org/10.1097/MD.0000000000014988.

    Article  Google Scholar 

  31. Crary MA, Mann GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil. 2005;86(8):1516–20. https://doi.org/10.1016/j.apmr.2004.11.049.

    Article  PubMed  Google Scholar 

  32. Martin-Harris B, Brodsky MB, Michel Y, Castell DO, Schleicher M, Sandidge J, Maxwell R, Blair J. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Robbins J, Coyle J, Rosenbek J, Roecker E, Wood J. Differentiation of normal and abnormal airway protection during swallowing using the penetration-aspiration scale. Dysphagia. 1999;14(4):228–32. https://doi.org/10.1007/pl00009610.

    Article  CAS  PubMed  Google Scholar 

  34. Murray J, Langmore SE, Ginsberg S, Dostie A. The significance of accumulated oropharyngeal secretions and swallowing frequency in predicting aspiration. Dysphagia. 1996;11(2):99–103. https://doi.org/10.1007/bf00417898.

    Article  CAS  PubMed  Google Scholar 

  35. Neubauer PD, Rademaker AW, Leder SB. The yale pharyngeal residue severity rating scale: an anatomically defined and image-based tool. Dysphagia. 2015;30(5):521–8. https://doi.org/10.1007/s00455-015-9631-4.

    Article  PubMed  Google Scholar 

  36. McCulloch TM, Hoffman MR, Ciucci MR. High-resolution manometry of pharyngeal swallow pressure events associated with head turn and chin tuck. Ann Otol Rhinol Laryngol. 2010;119(6):369–76. https://doi.org/10.1177/000348941011900602.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Takasaki K, Umeki H, Enatsu K, Tanaka F, Sakihama N, Kumagami H, Takahashi H. Investigation of pharyngeal swallowing function using high-resolution manometry. Laryngoscope. 2008;118(10):1729–32. https://doi.org/10.1097/MLG.0b013e31817dfd02.

    Article  PubMed  Google Scholar 

  38. Dungan S, Gregorio D, Abrahams T, Harrison B, Abrahams J, Brocato D, Davis C, Espana E, Garcia R, Smith S, Taylor B, Higgins T, Daley L, Carnaby G. Comparative validity of the American Speech-Language-Hearing Association’s national outcomes measurement system, functional oral intake scale, and G-codes to mann assessment of swallowing ability scores for dysphagia. Am J Speech Lang Pathol. 2019;28(2):424–9. https://doi.org/10.1044/2018_ajslp-18-0072.

    Article  PubMed  Google Scholar 

  39. Costa MM. Videofluoroscopy: the gold standard exam for studying swallowing and its dysfunction. Arq Gastroenterol. 2010;47(4):327–8. https://doi.org/10.1590/s0004-28032010000400001.

    Article  PubMed  Google Scholar 

  40. Giraldo-Cadavid LF, Leal-Leaño LR, Leon-Basantes GA, Bastidas AR, Garcia R, Ovalle S, Abondano-Garavito JE. Accuracy of endoscopic and videofluoroscopic evaluations of swallowing for oropharyngeal dysphagia. Laryngoscope. 2017;127(9):2002–10. https://doi.org/10.1002/lary.26419.

    Article  PubMed  Google Scholar 

  41. Hatlebakk JG, Castell JA, Spiegel J, Paoletti V, Katz PO, Castell DO. Dilatation therapy for dysphagia in patients with upper esophageal sphincter dysfunction-manometric and symptomatic response. Dis Esophagus. 1998;11(4):254–9. https://doi.org/10.1093/dote/11.4.254.

    Article  CAS  PubMed  Google Scholar 

  42. Kos MP, David EF, Klinkenberg-Knol EC, Mahieu HF. Long-term results of external upper esophageal sphincter myotomy for oropharyngeal. Dysphagia. 2010;25(3):169–76. https://doi.org/10.1007/s00455-009-9236-x.

    Article  PubMed  Google Scholar 

  43. Ozgursoy OB, Salassa JR. Manofluorographic and functional outcomes after endoscopic laser cricopharyngeal myotomy for cricopharyngeal bar. Otolaryngol Head Neck Surg. 2010;142(5):735–40. https://doi.org/10.1016/j.otohns.2009.08.020.

    Article  PubMed  Google Scholar 

  44. Terre R, Valles M, Panades A, Mearin F. Long-lasting effect of a single botulinum toxin injection in the treatment of oropharyngeal dysphagia secondary to upper esophageal sphincter dysfunction: a pilot study. Scand J Gastroenterol. 2008;43(11):1296–303. https://doi.org/10.1080/00365520802245403.

    Article  CAS  PubMed  Google Scholar 

  45. Brant CQ, Siqueira ES, Ferrari AP Jr. Botulinum toxin for oropharyngeal dysphagia: case report of flexible endoscope-guided injection. Dis Esophagus. 1999;12(1):68–73. https://doi.org/10.1046/j.1442-2050.1999.00015.x.

    Article  CAS  PubMed  Google Scholar 

  46. Liu LW, Tarnopolsky M, Armstrong D. Injection of botulinum toxin A to the upper esophageal sphincter for oropharyngeal dysphagia in two patients with inclusion body myositis. Can J Gastroenterol. 2004;18(6):397–9. https://doi.org/10.1155/2004/360537.

    Article  PubMed  Google Scholar 

  47. Dodds WJ, Hogan WJ, Lydon SB, Stewart ET, Stef JJ, Arndorfer RC. Quantitation of pharyngeal motor function in normal human subjects. J Appl Physiol. 1975;39(4):692–6. https://doi.org/10.1152/jappl.1975.39.4.692.

    Article  CAS  PubMed  Google Scholar 

  48. Kahrilas PJ. Esophageal motor disorders in terms of high-resolution esophageal pressure topography: what has changed? Am J Gastroenterol. 2010;105(5):981–7. https://doi.org/10.1038/ajg.2010.43.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Sears VW Jr, Castell JA, Castell DO. Radial and longitudinal asymmetry of human pharyngeal pressures during swallowing. Gastroenterology. 1991;101(6):1559–63. https://doi.org/10.1016/0016-5085(91)90392-x.

    Article  PubMed  Google Scholar 

  50. Kahrilas PJ, Dodds WJ, Dent J, Logemann JA, Shaker R. Upper esophageal sphincter function during deglutition. Gastroenterology. 1988;95(1):52–62. https://doi.org/10.1016/0016-5085(88)90290-9.

    Article  CAS  PubMed  Google Scholar 

  51. Dodds WJ. Physiology of swallowing. Dysphagia. 1989;3(4):171–8. https://doi.org/10.1007/bf02407219.

    Article  CAS  PubMed  Google Scholar 

  52. Castell JA, Castell DO. Modern solid state computerized manometry of the pharyngoesophageal segment. Dysphagia. 1993;8(3):270–5. https://doi.org/10.1007/bf01354550.

    Article  CAS  PubMed  Google Scholar 

  53. Fox M, Hebbard G, Janiak P, Brasseur JG, Ghosh S, Thumshirn M, Fried M, Schwizer W. High-resolution manometry predicts the success of oesophageal bolus transport and identifies clinically important abnormalities not detected by conventional manometry. Neurogastroenterol Motil. 2004;16(5):533–42. https://doi.org/10.1111/j.1365-2982.2004.00539.x.

    Article  CAS  PubMed  Google Scholar 

  54. Ghosh SK, Pandolfino JE, Zhang Q, Jarosz A, Kahrilas PJ. Deglutitive upper esophageal sphincter relaxation: a study of 75 volunteer subjects using solid-state high-resolution manometry. Am J Physiol Gastrointest Liver Physiol. 2006;291(3):G525-531. https://doi.org/10.1152/ajpgi.00081.2006.

    Article  CAS  PubMed  Google Scholar 

  55. Woisard-Bassols V, Alshehri S, Simonetta-Moreau M. The effects of botulinum toxin injections into the cricopharyngeus muscle of patients with cricopharyngeus dysfunction associated with pharyngo-laryngeal weakness. Eur Arch Otorhinolaryngol. 2013;270(3):805–15. https://doi.org/10.1007/s00405-012-2114-4.

    Article  PubMed  Google Scholar 

  56. Huai J, Hou Y, Guan J, Zhang Y, Wang Y, Zhang X, Zhang Y, Yue S. Botulinum toxin A injection using esophageal balloon radiography combined with CT guidance for the treatment of cricopharyngeal dysphagia. Dysphagia. 2019. https://doi.org/10.1007/s00455-019-10070-5.

    Article  PubMed  Google Scholar 

  57. Murry T, Wasserman T, Carrau RL, Castillo B. Injection of botulinum toxin A for the treatment of dysfunction of the upper esophageal sphincter. Am J Otolaryngol. 2005;26(3):157–62. https://doi.org/10.1016/j.amjoto.2004.11.010.

    Article  CAS  PubMed  Google Scholar 

  58. Cook IJ, Dodds WJ, Dantas RO, Massey B, Kern MK, Lang IM, Brasseur JG, Hogan WJ. Opening mechanisms of the human upper esophageal sphincter. Am J Physiol. 1989;257(5 Pt 1):G748-759. https://doi.org/10.1152/ajpgi.1989.257.5.G748.

    Article  CAS  PubMed  Google Scholar 

  59. Kelly EA, Koszewski IJ, Jaradeh SS, Merati AL, Blumin JH, Bock JM. Botulinum toxin injection for the treatment of upper esophageal sphincter dysfunction. Ann Otol Rhinol Laryngol. 2013;122(2):100–8. https://doi.org/10.1177/000348941312200205.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Alfonsi E, Merlo IM, Ponzio M, Montomoli C, Tassorelli C, Biancardi C, Lozza A, Martignoni E. An electrophysiological approach to the diagnosis of neurogenic dysphagia: implications for botulinum toxin treatment. J Neurol Neurosurg Psychiatry. 2010;81(1):54–60. https://doi.org/10.1136/jnnp.2009.174698.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by “the Third Affiliated Hospital, Sun Yat-sen University, Clinical Research Program” (No. YHJH201909) for HMW.

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Authors and Affiliations

  1. Department of Rehabilitation Medicine, The Third Affiliated Hospital, Sun Yat-Sen University, 600 Tianhe Road, Guangzhou, 510630, Guangdong Province, China

    Mengshu Xie, Peishan Zeng, Guifang Wan, Delian An, Zhiming Tang, Chao Li, Xiaomei Wei, Jing Shi, Yaowen Zhang, Zulin Dou & Hongmei Wen

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Correspondence to Zulin Dou or Hongmei Wen.

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Conflict of interest

WHM was involved in study concept, drafting, and finalization of manuscript. DZL was involved in study concept and critical review of manuscript. XMS and ZPS were involved in data collection, analysis, and drafting of manuscript. WGF, ADL, SJ, and ZYW were involved in patients’ evaluation and data collection. TZM, LC, and WXM were involved in patient treatment and data collection. All authors do not have any conflicts of interest.

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Xie, M., Zeng, P., Wan, G. et al. The Effect of Combined Guidance of Botulinum Toxin Injection with Ultrasound, Catheter Balloon, and Electromyography on Neurogenic Cricopharyngeal Dysfunction: A Prospective Study. Dysphagia 37, 601–611 (2022). https://doi.org/10.1007/s00455-021-10310-7

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