Surgical Endoscopy

, Volume 32, Issue 5, pp 2409–2419 | Cite as

Hypopharyngeal multichannel intraluminal impedance leads to the promising outcome of antireflux surgery in Japanese population with laryngopharyngeal reflux symptoms

  • Takeshi Suzuki
  • Yosuke Seki
  • Yoshitaka Okamoto
  • Toshitaka Hoppo
Article

Abstract

Background

Clinical characteristics of laryngopharyngeal reflux (LPR) in Japanese population remain unclear, and its treatment outcome is suboptimal. The objectives of this study were to evaluate Japanese patients with LPR symptoms using hypopharyngeal multichannel intraluminal impedance (HMII) and to assess the outcome of antireflux surgery (ARS).

Methods

Subjects included patients who had LPR symptoms for > 12 weeks or laryngoscopic findings suggestive of LPR and underwent laryngoscopy and esophageal testing including HMII. Abnormal proximal exposure (APE) was defined as LPR ≥ 1/day and/or full column reflux (FCR) (reflux 2 cm distal to the upper esophageal sphincter) ≥ 5/day on HMII. Patients with APE were offered ARS and the outcome of ARS was objectively assessed using Reflux Symptom Index (RSI).

Results

From July 2015 to September 2016, 52 patients with LPR symptoms (28 men, 24 women, median BMI 22.3) underwent HMII, and 38 patients (73%) had APE. Of them, 29 (76%) patients were not obese (BMI < 25) and 19 (50%) patients had a negative DeMeester score. Approximately one-third of LPR and FCR events were non-acid in the distal esophagus. A positive symptom-association probability was seen only in 18 patients (35%). Mild esophagitis and hiatal hernia were found in 5 (10%) and 23 (48%) patients, respectively. All 12 patients (100%) who had undergone ARS were able to discontinue PPI and had a significant improvement in the RSI scores postoperatively (22.9 ± 10.0 vs. 6.8 ± 6.8, p < .001).

Conclusions

APE was frequently observed in Japanese patients with LPR symptoms. Obesity and esophagitis were uncommon in this population. Since a large number of patients with APE had negative DeMeester score and proximal reflux events were often non-acid, a conventional pH monitoring is insufficient. HMII is crucial to evaluate patients with LPR symptoms as the documentation of APE is a key for successful outcome of ARS.

Keywords

Laryngopharyngeal reflux Abnormal proximal exposure Hypopharyngeal multichannel intraluminal impedance Antireflux surgery Japanese 

Abbreviations

LPR

Laryngopharyngeal reflux

GERD

Gastroesophageal reflux disease

PPI

Proton pump inhibitor

MII

Multichannel intraluminal impedance

HMII

Hypopharyngeal MII

APE

Abnormal proximal exposure

FCR

Full column reflux

UES

Upper esophageal sphincter

ARS

Antireflux surgery

BMI

Body mass index

RSI

Reflux symptom index

FSSG

Frequency scale for the symptoms of GERD

RFS

Reflux finding score

LA

Los Angeles

HRM

High-resolution manometry

EGJ

Esophagogastric junction

IEM

Ineffective esophageal motility

LES

Lower esophageal sphincter

SAP

Symptom-association probability

NERD

Non-erosive gastroesophageal reflux disease

Notes

Acknowledgements

We thank Tadanao Takeno, Urara Funakoshi for her technical assistance.

Compliance with ethical standards

Disclosures

Drs. Takeshi Suzuki, Yosuke Seki, Yoshitaka Okamoto, and Toshitaka Hoppo have no conflicts of interest or financial tie to disclose.

References

  1. 1.
    Vakil N, van Zanten SV, Kahrilas P, Dent J, Jones R (2006) The Montreal definition and classification of gastroesophageal reflux disease: a global evidence-based consensus. Am J Gastroenterol 101:1900–1920CrossRefPubMedGoogle Scholar
  2. 2.
    Koufman JA (2002) Laryngopharyngeal reflux is different from classic gastroesophageal reflux disease. Ear Nose Throat J 81:7–9PubMedGoogle Scholar
  3. 3.
    Koufman J, Sataloff RT, Toohill R (1996) Laryngopharyngeal reflux: consensus conference report. J Voice 10:215–216CrossRefPubMedGoogle Scholar
  4. 4.
    Hoppo T, Komatsu Y, Jobe BA (2013) Antireflux surgery in patients with chronic cough and abnormal proximal exposure as measured by hypopharyngeal multichannel intraluminal impedance. JAMA Surg 148:608–615CrossRefPubMedGoogle Scholar
  5. 5.
    Vaezi MF, Hicks DM, Abelson TI, Richter JE (2003) Laryngeal signs and symptoms and gastroesophageal reflux disease (GERD): a critical assessment of cause and effect association. Clin Gastroenterol Hepatol 1:333–344CrossRefPubMedGoogle Scholar
  6. 6.
    Komatsu Y, Hoppo T, Jobe BA (2013) Proximal reflux as a cause of adult-onset asthma: the case for hypopharyngeal impedance testing to improve the sensitivity of diagnosis. JAMA Surg 148:50–58CrossRefPubMedGoogle Scholar
  7. 7.
    Wei C (2016) A meta-analysis for the role of proton pump inhibitor therapy in patients with laryngopharyngeal reflux. Eur Arch Otorhinolaryngol 273:3795–3801CrossRefPubMedGoogle Scholar
  8. 8.
    Liu C, Wang H, Liu K (2016) Meta-analysis of the efficacy of proton pump inhibitors for the symptoms of laryngopharyngeal reflux. Braz J Med Biol Res 49Google Scholar
  9. 9.
    Hickson C, Simpson CB, Falcon R (2001) Laryngeal pseudosulcus as a predictor of laryngopharyngeal reflux. Laryngoscope 111:1742–1745CrossRefPubMedGoogle Scholar
  10. 10.
    Desjardin M, Roman S, des Varannes SB, Gourcerol G, Coffin B, Ropert A, Mion F, Zerbib F (2013) Pharyngeal pH alone is not reliable for the detection of pharyngeal reflux events: A study with oesophageal and pharyngeal pH-impedance monitoring. United European Gastroenterol J 1:438–444CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Hoppo T, Sanz AF, Nason KS, Carroll TL, Rosen C, Normolle DP, Shaheen NJ, Luketich JD, Jobe BA (2012) How much pharyngeal exposure is “normal”? Normative data for laryngopharyngeal reflux events using hypopharyngeal multichannel intraluminal impedance (HMII). J Gastrointest Surg 16:16–24CrossRefPubMedGoogle Scholar
  12. 12.
    Shimazu T, Matsui T, Furukawa K, Oshige K, Mitsuyasu T, Kiyomizu A, Ueki T, Yao T (2005) A prospective study of the prevalence of gastroesophageal reflux disease and confounding factors. J Gastroenterol 40:866–872CrossRefPubMedGoogle Scholar
  13. 13.
    Sakaguchi M, Oka H, Hashimoto T, Asakuma Y, Takao M, Gon G, Yamamoto M, Tsuji Y, Yamamoto N, Shimada M, Lee K, Ashida K (2008) Obesity as a risk factor for GERD in Japan. J Gastroenterol 43:57–62CrossRefPubMedGoogle Scholar
  14. 14.
    Fujiwara Y, Arakawa T (2009) Epidemiology and clinical characteristics of GERD in the Japanese population. J Gastroenterol 44:518–534CrossRefPubMedGoogle Scholar
  15. 15.
    Sugiyama T, Nishikawa K, Komatsu Y, Ishizuka J, Mizushima T, Kumagai A, Kato M, Saito N, Takeda H, Asaka M, Freston JW (2001) Attributable risk of H. pylori in peptic ulcer disease: does declining prevalence of infection in general population explain increasing frequency of non-H. pylori ulcers? Dig Dis Sci 46:307–310CrossRefPubMedGoogle Scholar
  16. 16.
    Asaoka D, Nagahara A, Matsumoto K, Hojo M, Watanabe S (2014) Current perspectives on reflux laryngitis. Clin J Gastroenterol 7:471–475CrossRefPubMedGoogle Scholar
  17. 17.
    Belafsky PC, Postma GN, Koufman JA (2001) The validity and reliability of the reflux finding score (RFS). Laryngoscope 111:1313–1317CrossRefPubMedGoogle Scholar
  18. 18.
    DiBaise JK (1999) The LA classification for esophagitis: a call for standardization. Am J Gastroenterol 94:3403–3404Google Scholar
  19. 19.
    Kahrilas PJ, Bredenoord AJ, Fox M, Gyawali CP, Roman S, Smout AJ, Pandolfino JE (2015) The Chicago Classification of esophageal motility disorders, v3.0. Neurogastroenterol Motil 27:160–174CrossRefPubMedGoogle Scholar
  20. 20.
    Hoppo T, Jarido V, Pennathur A, Morrell M, Crespo M, Shigemura N, Bermudez C, Hunter JG, Toyoda Y, Pilewski J, Luketich JD, Jobe BA (2011) Antireflux surgery preserves lung function in patients with gastroesophageal reflux disease and end-stage lung disease before and after lung transplantation. Arch Surg 146:1041–1047CrossRefPubMedGoogle Scholar
  21. 21.
    Hoppo T, Komatsu Y, Nieponice A, Schrenker J, Jobe BA (2012) Toward an improved understanding of isolated upright reflux: positional effects on the lower esophageal sphincter in patients with symptoms of gastroesophageal reflux. World J Surg 36:1623–1631CrossRefPubMedGoogle Scholar
  22. 22.
    Weusten BL, Roelofs JM, Akkermans LM, Van Berge-Henegouwen GP, Smout AJ (1994) The symptom-association probability: an improved method for symptom analysis of 24-hour esophageal pH data. Gastroenterology 107:1741–1745CrossRefPubMedGoogle Scholar
  23. 23.
    Belafsky PC, Postma GN, Koufman JA (2002) Validity and reliability of the reflux symptom index (RSI). J Voice 16:274–277CrossRefPubMedGoogle Scholar
  24. 24.
    Kusano M, Shimoyama Y, Sugimoto S, Kawamura O, Maeda M, Minashi K, Kuribayashi S, Higuchi T, Zai H, Ino K, Horikoshi T, Sugiyama T, Toki M, Ohwada T, Mori M (2004) Development and evaluation of FSSG: frequency scale for the symptoms of GERD. J Gastroenterol 39:888–891CrossRefPubMedGoogle Scholar
  25. 25.
    Nam SY (2016) Obesity-related digestive diseases and their pathophysiology. Gut Liver.  https://doi.org/10.5009/gnl15557 Google Scholar
  26. 26.
    Jacobson BC, Somers SC, Fuchs CS, Kelly CP, Camargo CA (2006) Body-mass index and symptoms of gastroesophageal reflux in women. N Engl J Med 354:2340–2348CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Nam SY, Choi IJ, Nam BH, Park KW, Kim CG (2009) Obesity and weight gain as risk factors for erosive oesophagitis in men. Aliment Pharmacol Ther 29:1042–1052CrossRefPubMedGoogle Scholar
  28. 28.
    Moki F, Kusano M, Mizuide M, Shimoyama Y, Kawamura O, Takagi H, Imai T, Mori M (2007) Association between reflux oesophagitis and features of the metabolic syndrome in Japan. Aliment Pharmacol Ther 26:1069–1075CrossRefPubMedGoogle Scholar
  29. 29.
    Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, Mullany EC, Biryukov S, Abbafati C, Abera SF, Abraham JP, Abu-Rmeileh NM, Achoki T, AlBuhairan FS, Alemu ZA, Alfonso R, Ali MK, Ali R, Guzman NA, Ammar W, Anwari P, Banerjee A, Barquera S, Basu S, Bennett DA, Bhutta Z, Blore J, Cabral N, Nonato IC, Chang JC, Chowdhury R, Courville KJ, Criqui MH, Cundiff DK, Dabhadkar KC, Dandona L, Davis A, Dayama A, Dharmaratne SD, Ding EL, Durrani AM, Esteghamati A, Farzadfar F, Fay DF, Feigin VL, Flaxman A, Forouzanfar MH, Goto A, Green MA, Gupta R, Hafezi-Nejad N, Hankey GJ, Harewood HC, Havmoeller R, Hay S, Hernandez L, Husseini A, Idrisov BT, Ikeda N, Islami F, Jahangir E, Jassal SK, Jee SH, Jeffreys M, Jonas JB, Kabagambe EK, Khalifa SE, Kengne AP, Khader YS, Khang YH, Kim D, Kimokoti RW, Kinge JM, Kokubo Y, Kosen S, Kwan G, Lai T, Leinsalu M, Li Y, Liang X, Liu S, Logroscino G, Lotufo PA, Lu Y, Ma J, Mainoo NK, Mensah GA, Merriman TR, Mokdad AH, Moschandreas J, Naghavi M, Naheed A, Nand D, Narayan KM, Nelson EL, Neuhouser ML, Nisar MI, Ohkubo T, Oti SO, Pedroza A, Prabhakaran D, Roy N, Sampson U, Seo H, Sepanlou SG, Shibuya K, Shiri R, Shiue I, Singh GM, Singh JA, Skirbekk V, Stapelberg NJ, Sturua L, Sykes BL, Tobias M, Tran BX, Trasande L, Toyoshima H, van de Vijver S, Vasankari TJ, Veerman JL, Velasquez-Melendez G, Vlassov VV, Vollset SE, Vos T, Wang C, Wang X, Weiderpass E, Werdecker A, Wright JL, Yang YC, Yatsuya H, Yoon J, Yoon SJ, Zhao Y, Zhou M, Zhu S, Lopez AD, Murray CJ, Gakidou E (2014) Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384:766–781CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Komatsu Y, Kelly LA, Zaidi AH, Rotoloni CL, Kosovec JE, Lloyd EJ, Waheed A, Hoppo T, Jobe BA (2014) Hypopharyngeal pepsin and Sep70 as diagnostic markers of laryngopharyngeal reflux: preliminary study. Surg Endosc 29:1080–1087CrossRefPubMedGoogle Scholar
  31. 31.
    Sano H, Iwakiri K, Kawami N, Tanaka Y, Sakamoto C (2014) Mechanisms of acid reflux and how refluxed acid extends proximally in patients with non-erosive reflux disease. Digestion 90:108–115CrossRefPubMedGoogle Scholar
  32. 32.
    Iwakiri K, Hayashi Y, Kotoyori M, Tanaka Y, Kawami N, Sano H, Takubo K, Sakamoto C, Holloway RH (2007) Defective triggering of secondary peristalsis in patients with non-erosive reflux disease. J Gastroenterol Hepatol 22:2208–2211CrossRefPubMedGoogle Scholar
  33. 33.
    Iwakiri K, Sano H, Tanaka Y, Kawami N, Umezawa M, Futagami S, Hoshihara Y, Nomura T, Miyashita M, Sakamoto C (2010) Characteristics of symptomatic reflux episodes in patients with non-erosive reflux disease who have a positive symptom index on proton pump inhibitor therapy. Digestion 82:156–161CrossRefPubMedGoogle Scholar
  34. 34.
    Emerenziani S, Ribolsi M, Sifrim D, Blondeau K, Cicala M (2009) Regional oesophageal sensitivity to acid and weakly acidic reflux in patients with non-erosive reflux disease. Neurogastroenterol Motil 21:253–258CrossRefPubMedGoogle Scholar
  35. 35.
    Fujiwara Y, Higuchi K, Shiba M, Yamamori K, Watanabe Y, Sasaki E, Tominaga K, Watanabe T, Oshitani N, Arakawa T (2005) Differences in clinical characteristics between patients with endoscopy-negative reflux disease and erosive esophagitis in Japan. Am J Gastroenterol 100:754–758CrossRefPubMedGoogle Scholar
  36. 36.
    Shiba K, Satoh I, Kobayashi N, Hayashi F (1999) Multifunctional laryngeal motoneurons: an intracellular study in the cat. J Neurosci 19:2717–2727CrossRefPubMedGoogle Scholar
  37. 37.
    Suzuki T, Nakazawa K, Shiba K (2010) Swallow-related inhibition in laryngeal motoneurons. Neurosci Res 67:327–333CrossRefPubMedGoogle Scholar
  38. 38.
    Sasaki CT, Marotta J, Hundal J, Chow J, Eisen RN (2005) Bile-induced laryngitis: is there a basis in evidence? Ann Otol Rhinol Laryngol 114:192–197CrossRefPubMedGoogle Scholar
  39. 39.
    Iqbal M, Batch AJ, Spychal RT, Cooper BT (2008) Outcome of surgical fundoplication for extraesophageal (atypical) manifestations of gastroesophageal reflux disease in adults: a systematic review. J Laparoendosc Adv Surg Tech A 18:789–796CrossRefPubMedGoogle Scholar
  40. 40.
    Carroll TL, Nahikian K, Asban A, Wiener (2016) Nissen fundoplication for laryngopharyngeal reflux after patient selection using dual pH, full column impedance testing: a pilot study. Ann Otol Rhinol Laryngol 125:722–728CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Takeshi Suzuki
    • 1
  • Yosuke Seki
    • 2
  • Yoshitaka Okamoto
    • 1
  • Toshitaka Hoppo
    • 3
  1. 1.Department of Otolaryngology, Head and Neck Surgery, Graduate School of MedicineChiba UniversityChibaJapan
  2. 2.Minimally Invasive Surgery Center, Yotsuya Medical CubeTokyoJapan
  3. 3.Esophageal & Lung InstituteAllegheny Health NetworkPittsburghUSA

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