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01-06-2022 | Ultrasound | Original Article

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

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

Published in: Dysphagia | Issue 3/2022

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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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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRef

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

21.

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

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRef

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

51.

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

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

Title: The Effect of Combined Guidance of Botulinum Toxin Injection with Ultrasound, Catheter Balloon, and Electromyography on Neurogenic Cricopharyngeal Dysfunction: A Prospective Study
Authors: Mengshu Xie
Peishan Zeng
Guifang Wan
Delian An
Zhiming Tang
Chao Li
Xiaomei Wei
Jing Shi
Yaowen Zhang
Zulin Dou
Hongmei Wen
Publication date: 01-06-2022
Publisher: Springer US
Keywords: Ultrasound
Ultrasound
Botulinum Toxin
Dysphagia
Dysphagia
Dysphagia
Flexible Endoscopic Evaluation of Swallowing
Flexible Endoscopic Evaluation of Swallowing
Published in: Dysphagia / Issue 3/2022
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI: https://doi.org/10.1007/s00455-021-10310-7

At a glance: The STEP trials

Springer Medicine

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

Abstract

Background

Methods

Key Results

Conclusion & Inferences

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Key Results

Conclusion & Inferences

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