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

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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.

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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

References

  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 101:1900–1920

    Article  PubMed  Google Scholar 

  2. Koufman JA (2002) Laryngopharyngeal reflux is different from classic gastroesophageal reflux disease. Ear Nose Throat J 81:7–9

    PubMed  Google Scholar 

  3. Koufman J, Sataloff RT, Toohill R (1996) Laryngopharyngeal reflux: consensus conference report. J Voice 10:215–216

    Article  CAS  PubMed  Google Scholar 

  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 148:608–615

    Article  PubMed  Google Scholar 

  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 1:333–344

    Article  PubMed  Google Scholar 

  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 148:50–58

    Article  PubMed  Google Scholar 

  7. Wei C (2016) A meta-analysis for the role of proton pump inhibitor therapy in patients with laryngopharyngeal reflux. Eur Arch Otorhinolaryngol 273:3795–3801

    Article  PubMed  Google Scholar 

  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 49

  9. Hickson C, Simpson CB, Falcon R (2001) Laryngeal pseudosulcus as a predictor of laryngopharyngeal reflux. Laryngoscope 111:1742–1745

    Article  CAS  PubMed  Google Scholar 

  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 1:438–444

    Article  PubMed  PubMed Central  Google Scholar 

  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 16:16–24

    Article  PubMed  Google Scholar 

  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 40:866–872

    Article  PubMed  Google Scholar 

  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 43:57–62

    Article  PubMed  Google Scholar 

  14. Fujiwara Y, Arakawa T (2009) Epidemiology and clinical characteristics of GERD in the Japanese population. J Gastroenterol 44:518–534

    Article  PubMed  Google Scholar 

  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 46:307–310

    Article  CAS  PubMed  Google Scholar 

  16. Asaoka D, Nagahara A, Matsumoto K, Hojo M, Watanabe S (2014) Current perspectives on reflux laryngitis. Clin J Gastroenterol 7:471–475

    Article  PubMed  Google Scholar 

  17. Belafsky PC, Postma GN, Koufman JA (2001) The validity and reliability of the reflux finding score (RFS). Laryngoscope 111:1313–1317

    Article  CAS  PubMed  Google Scholar 

  18. DiBaise JK (1999) The LA classification for esophagitis: a call for standardization. Am J Gastroenterol 94:3403–3404

    Google Scholar 

  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 27:160–174

    Article  CAS  PubMed  Google Scholar 

  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 146:1041–1047

    Article  PubMed  Google Scholar 

  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 36:1623–1631

    Article  PubMed  Google Scholar 

  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 107:1741–1745

    Article  CAS  PubMed  Google Scholar 

  23. Belafsky PC, Postma GN, Koufman JA (2002) Validity and reliability of the reflux symptom index (RSI). J Voice 16:274–277

    Article  PubMed  Google Scholar 

  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 39:888–891

    Article  PubMed  Google Scholar 

  25. Nam SY (2016) Obesity-related digestive diseases and their pathophysiology. Gut Liver. https://doi.org/10.5009/gnl15557

    Google Scholar 

  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 354:2340–2348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 29:1042–1052

    Article  CAS  PubMed  Google Scholar 

  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 26:1069–1075

    Article  CAS  PubMed  Google Scholar 

  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 384:766–781

    Article  PubMed  PubMed Central  Google Scholar 

  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 29:1080–1087

    Article  PubMed  Google Scholar 

  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 90:108–115

    Article  CAS  PubMed  Google Scholar 

  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 22:2208–2211

    Article  PubMed  Google Scholar 

  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 82:156–161

    Article  CAS  PubMed  Google Scholar 

  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 21:253–258

    Article  CAS  PubMed  Google Scholar 

  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 100:754–758

    Article  PubMed  Google Scholar 

  36. Shiba K, Satoh I, Kobayashi N, Hayashi F (1999) Multifunctional laryngeal motoneurons: an intracellular study in the cat. J Neurosci 19:2717–2727

    Article  CAS  PubMed  Google Scholar 

  37. Suzuki T, Nakazawa K, Shiba K (2010) Swallow-related inhibition in laryngeal motoneurons. Neurosci Res 67:327–333

    Article  CAS  PubMed  Google Scholar 

  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 114:192–197

    Article  PubMed  Google Scholar 

  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 18:789–796

    Article  PubMed  Google Scholar 

  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 125:722–728

    Article  PubMed  Google Scholar 

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Acknowledgements

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

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Correspondence to Toshitaka Hoppo.

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

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Suzuki, T., Seki, Y., Okamoto, Y. et al. Hypopharyngeal multichannel intraluminal impedance leads to the promising outcome of antireflux surgery in Japanese population with laryngopharyngeal reflux symptoms. Surg Endosc 32, 2409–2419 (2018). https://doi.org/10.1007/s00464-017-5940-z

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