Advertisement

Multichannel Intraluminal Impedance and pH Monitoring (pH-MII) in Infants and Children

  • Maartje M. J. Singendonk
  • F. Jaime
  • S. Salvatore
  • M. M. Tabbers
  • M. A. Benninga
  • Y. Vandenplas
Chapter

Abstract

The application of combined pH and multichannel intraluminal impedance (pH-MII) monitoring has enhanced the recognition and characterization of gastro-oesophageal reflux disease (GORD). Its main advantages over traditional pH monitoring lie in the additional ability to detect non-acid gastro-oesophageal reflux (GOR), to discern between liquid and gas GOR and to determine the proximal extent of a GOR episode. When conducted in combination with manometry, it reveals information on the relationship between oesophageal pressures and oesophageal bolus flow, enhancing the evaluation of oesophageal function testing in terms of assessment of mechanisms of oesophageal bolus clearance. The measurement of mean impedance baseline has also provided novel insights into oesophageal mucosal integrity changes as an indicator of oesophageal inflammation. However, a few clinical and technical shortcomings, of which some are specific to the paediatric population, must be considered when interpreting study results and limit the diagnostic value of pH-MII monitoring in children. In this chapter, the technical aspects of pH-MII monitoring will therefore first be addressed, and, second, the current clinical benefits and limitations of oesophageal pH-MII in children will be highlighted.

Keywords

pH Impedance pH-MII Monitoring Children Reflux Acid reflux Weakly acid reflux Non-acid reflux Catheter Reflux index 

References

  1. 1.
    Bernstein LM, Fruin RD, Pacini R. Differentiation of esophageal pain from angina pectoris: role of the esophageal acid perfusion test. Medicine (Baltimore). 1962;41:143–62.CrossRefGoogle Scholar
  2. 2.
    Francavilla R, Magista AM, Bucci N, Villirillo A, Boscarelli G, Mappa L, et al. Comparison of esophageal pH and multichannel intraluminal impedance testing in pediatric patients with suspected gastroesophageal reflux. J Pediatr Gastroenterol Nutr. 2010;50(2):154–60.PubMedCrossRefGoogle Scholar
  3. 3.
    Wenzl TG, Benninga MA, Loots CM, Salvatore S, Vandenplas Y, Group EE-PW. Indications, methodology, and interpretation of combined esophageal impedance-pH monitoring in children: ESPGHAN EURO-PIG standard protocol. J Pediatr Gastroenterol Nutr. 2012;55(2):230–4.PubMedCrossRefGoogle Scholar
  4. 4.
    Sifrim D, Castell D, Dent J, Kahrilas PJ. Gastro-oesophageal reflux monitoring: review and consensus report on detection and definitions of acid, non-acid, and gas reflux. Gut. 2004;53(7):1024–31.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Asge Technology Committee, Wang A, Pleskow DK, Banerjee S, Barth BA, Bhat YM, et al. Esophageal function testing. Gastrointest Endosc. 2012;76(2):231–43.CrossRefGoogle Scholar
  6. 6.
    Ummarino D, Salvatore S, Hauser B, Staiano A, Vandenplas Y. Esophageal impedance baseline according to different time intervals. Eur J Med Res. 2012;17(1):18.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Silny J, Knigge KP, Fass J, Rau G, Matern S, Schumpelick V. Verification of the intraluminal multiple electrical impedance measurement for the recording of gastrointestinal motility. Neurogastroenterol Motil. 1993;5(2):107–22.CrossRefGoogle Scholar
  8. 8.
    Mousa HM, Rosen R, Woodley FW, Orsi M, Armas D, Faure C, et al. Esophageal impedance monitoring for gastroesophageal reflux. J Pediatr Gastroenterol Nutr. 2011;52(2):129–39.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Hemmink GJ, Weusten BL, Oors J, Bredenoord AJ, Timmer R, Smout AJ. Ambulatory oesophageal pH monitoring: a comparison between antimony, ISFET, and glass pH electrodes. Eur J Gastroenterol Hepatol. 2010;22(5):572–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Vandenplas Y, Badriul H, Verghote M, Hauser B, Kaufman L. Glass and antimony electrodes for oesophageal pH monitoring in distressed infants: how different are they? Eur J Gastroenterol Hepatol. 2004;16(12):1325–30.PubMedCrossRefGoogle Scholar
  11. 11.
    Kahrilas PJ, Quigley EM. Clinical esophageal pH recording: a technical review for practice guideline development. Gastroenterology. 1996;110(6):1982–96.Google Scholar
  12. 12.
    Hirano I, Richter JE. Practice Parameters Committee of the American College of Gastroenterology. ACG practice guidelines: esophageal reflux testing. Am J Gastroenterol. 2007;102(3):668–85.PubMedCrossRefGoogle Scholar
  13. 13.
    Moreau B, Kambites S, Levesque D. Esophageal length: esophageal manometry remains superior to mathematical equations. J Pediatr Gastroenterol Nutr. 2013;57(2):236–9.PubMedCrossRefGoogle Scholar
  14. 14.
    Badriul H, Vandenplas Y. Gastro-oesophageal reflux in infancy. J Gastroenterol Hepatol. 1999;14(1):13–9.PubMedCrossRefGoogle Scholar
  15. 15.
    Singendonk MM, Kritas S, Cock C, Ferris L, McCall L, Rommel N, et al. Applying the Chicago Classification criteria of esophageal motility to a pediatric cohort: effects of patient age and size. Neurogastroenterol Motil. 2014;26(9):1333–41.PubMedCrossRefGoogle Scholar
  16. 16.
    Staiano A, Clouse RE. Value of subject height in predicting lower esophageal sphincter location. Am J Dis Child. 1991;145(12):1424–7.PubMedGoogle Scholar
  17. 17.
    Mutalib M, Sintusek P, Punpanich D, Thapar N, Lindley K. A new method to estimate catheter length for esophageal multichannel intraluminal impedance monitoring in children. Neurogastroenterol Motil. 2015;27(5):728–33.PubMedCrossRefGoogle Scholar
  18. 18.
    Pilic D, Frohlich T, Noh F, Pappas A, Schmidt-Choudhury A, Kohler H, et al. Detection of gastroesophageal reflux in children using combined multichannel intraluminal impedance and pH measurement: data from the German Pediatric Impedance Group. J Pediatr. 2011;158(4):650–4.e1.PubMedCrossRefGoogle Scholar
  19. 19.
    Vandenplas Y, Belli D, Boige N, Bouquet J, Cadranel S, Cezard JP, Chapoy P, Cucchiara S, Dupont C, Gottrand F, Heymans HSA, Kneepkens CMF, Katsiayannikis L, Milla P, Navarro J, Newell SJ, Sandhu BK, Tolboom J. A standardized protocol for the methodology of esophageal pH monitoring and interpretation of the data for the diagnosis of gastroesophageal reflux. J Pediatr Gastroenterol Nutr. 1992;14(4):467–71.CrossRefGoogle Scholar
  20. 20.
    Katz PO, Gerson LB, Vela MF. Guidelines for the diagnosis and management of gastroesophageal reflux disease. Am J Gastroenterol. 2013;108(3):308–28. quiz 29PubMedCrossRefGoogle Scholar
  21. 21.
    Mousa H, Machado R, Orsi M, Chao CS, Alhajj T, Alhajj M, et al. Combined multichannel intraluminal impedance-pH (MII-pH): multicenter report of normal values from 117 children. Curr Gastroenterol Rep. 2014;16(8):400.PubMedCrossRefGoogle Scholar
  22. 22.
    Zerbib F, des Varannes SB, Roman S, Pouderoux P, Artigue F, Chaput U, et al. Normal values and day-to-day variability of 24-h ambulatory oesophageal impedance-pH monitoring in a Belgian-French cohort of healthy subjects. Aliment Pharmacol Ther. 2005;22(10):1011–21.PubMedCrossRefGoogle Scholar
  23. 23.
    Corvaglia L, Rotatori R, Ferlini M, Aceti A, Ancora G, Faldella G. The effect of body positioning on gastroesophageal reflux in premature infants: evaluation by combined impedance and pH monitoring. J Pediatr. 2007;151(6):591–6.e1.PubMedCrossRefGoogle Scholar
  24. 24.
    van Wijk MP, Benninga MA, Dent J, Lontis R, Goodchild L, McCall LM, et al. Effect of body position changes on postprandial gastroesophageal reflux and gastric emptying in the healthy premature neonate. J Pediatr. 2007;151(6):585–90.e2.PubMedCrossRefGoogle Scholar
  25. 25.
    Loots C, Kritas S, van Wijk M, McCall L, Peeters L, Lewindon P, et al. Body positioning and medical therapy for infantile gastroesophageal reflux symptoms. J Pediatr Gastroenterol Nutr. 2014;59(2):237–43.PubMedCrossRefGoogle Scholar
  26. 26.
    Omari TI, Rommel N, Staunton E, Lontis R, Goodchild L, Haslam RR, et al. Paradoxical impact of body positioning on gastroesophageal reflux and gastric emptying in the premature neonate. J Pediatr. 2004;145(2):194–200.PubMedCrossRefGoogle Scholar
  27. 27.
    Moon RY, Fu L. Sudden infant death syndrome: an update. Pediatr Rev. 2012;33(7):314–20.PubMedCrossRefGoogle Scholar
  28. 28.
    Johnsson F, Joelsson B. Reproducibility of ambulatory oesophageal pH monitoring. Gut. 1988;29(7):886–9.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Vandenplas Y, Casteels A, Naert M, Derde MP, Blecker U. Abbreviated oesophageal pH monitoring in infants. Eur J Pediatr. 1994;153(2):80–3.PubMedCrossRefGoogle Scholar
  30. 30.
    Friesen CA, Hodge C, Roberts CC. Accuracy and reproducibility of 12-h esophageal pH monitoring. J Pediatr Gastroenterol Nutr. 1991;12(2):166–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Vandenplas Y, Helven R, Goyvaerts H, Sacre L. Reproducibility of continuous 24 hour oesophageal pH monitoring in infants and children. Gut. 1990;31(4):374–7.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hampton FJ, MacFadyen UM, Simpson H. Reproducibility of 24 hour oesophageal pH studies in infants. Arch Dis Child. 1990;65(11):1249–54.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Mahajan L, Wyllie R, Oliva L, Balsells F, Steffen R, Kay M. Reproducibility of 24-hour intraesophageal pH monitoring in pediatric patients. Pediatrics. 1998;101(2):260–3.PubMedCrossRefGoogle Scholar
  34. 34.
    Dalby K, Nielsen RG, Markoew S, Kruse-Andersen S, Husby S. Reproducibility of 24-hour combined multiple intraluminal impedance (MII) and pH measurements in infants and children. Evaluation of a diagnostic procedure for gastroesophageal reflux disease. Dig Dis Sci. 2007;52(9):2159–65.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Smits MJ, Loots CM, van Wijk MP, Bredenoord AJ, Benninga MA, Smout AJ. An expert panel-based study on recognition of gastro-esophageal reflux in difficult esophageal pH-impedance tracings. Neurogastroenterol Motil. 2015;27(5):637–45.PubMedCrossRefGoogle Scholar
  36. 36.
    Loots CM, van Wijk MP, Blondeau K, Dalby K, Peeters L, Rosen R, et al. Interobserver and intraobserver variability in pH-impedance analysis between 10 experts and automated analysis. J Pediatr. 2012;160(3):441–6.e1.PubMedCrossRefGoogle Scholar
  37. 37.
    Ravi K, DeVault K, Murray J, Bouras EP, Francis D. Inter-observer agreement for multichannel intraluminal impedance–pH testing. Dis Esophagus. 2010;23(7):540–4.PubMedCrossRefGoogle Scholar
  38. 38.
    Pilic D, Hofs C, Weitmann S, Noh F, Frohlich T, Skopnik H, et al. Inter- and intraobserver agreement in 24-hour combined multiple intraluminal impedance and pH measurement in children. J Pediatr Gastroenterol Nutr. 2011;53(3):255–9.PubMedCrossRefGoogle Scholar
  39. 39.
    Wenzl TG, Moroder C, Trachterna M, Thomson M, Silny J, Heimann G, et al. Esophageal pH monitoring and impedance measurement: a comparison of two diagnostic tests for gastroesophageal reflux. J Pediatr Gastroenterol Nutr. 2002;34(5):519–23.PubMedCrossRefGoogle Scholar
  40. 40.
    Nobile S, Noviello C, Cobellis G, Carnielli VP. Are Infants with bronchopulmonary dysplasia prone to gastroesophageal reflux? A prospective observational study with esophageal pH-impedance monitoring. J Pediatr. 2015;167(2):279–85.e1.PubMedCrossRefGoogle Scholar
  41. 41.
    Wu JF, Hsu WC, Tseng PH, Wang HP, Hsu HY, Chang MH, et al. Combined multichannel intraluminal impedance and pH monitoring assists the diagnosis of sliding hiatal hernia in children with gastroesophageal reflux disease. J Gastroenterol. 2013;48(11):1242–8.PubMedCrossRefGoogle Scholar
  42. 42.
    Rosen R, Lord C, Nurko S. The sensitivity of multichannel intraluminal impedance and the pH probe in the evaluation of gastroesophageal reflux in children. Clin Gastroenterol Hepatol. 2006;4(2):167–72.PubMedCrossRefGoogle Scholar
  43. 43.
    Rosen R, Nurko S. The importance of multichannel intraluminal impedance in the evaluation of children with persistent respiratory symptoms. Am J Gastroenterol. 2004;99(12):2452–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Vikneswaran N, Murray JA. Discounting the duration of bolus exposure in impedance testing underestimates acid reflux. BMC Gastroenterol. 2016;16(1):60.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    van Wijk MP, Benninga MA, Omari TI. Role of the multichannel intraluminal impedance technique in infants and children. J Pediatr Gastroenterol Nutr. 2009;48(1):2–12.PubMedCrossRefGoogle Scholar
  46. 46.
    Roman S, des Varannes SB, Pouderoux P, Chaput U, Mion F, Galmiche J, et al. Ambulatory 24-h oesophageal impedance–pH recordings: reliability of automatic analysis for gastro-oesophageal reflux assessment. Neurogastroenterol Motil. 2006;18(11):978–86.PubMedCrossRefGoogle Scholar
  47. 47.
    Hemmink GJ, Bredenoord AJ, Aanen MC, Weusten BL, Timmer R, Smout AJ. Computer analysis of 24-h esophageal impedance signals. Scand J Gastroenterol. 2011;46(3):271–6.PubMedCrossRefGoogle Scholar
  48. 48.
    Salvatore S, Hauser B, Luini C, Arrigo S, Salvatoni A, Vandenplas Y. MII-pH: what we can get from the autoscan and manual readings? J Pediatr Gastroenterol Nutr. 2006;42(5):E50.Google Scholar
  49. 49.
    Lopez-Alonso M, Moya MJ, Cabo JA, Ribas J, del Carmen Macias M, Silny J, et al. Twenty-four-hour esophageal impedance-pH monitoring in healthy preterm neonates: rate and characteristics of acid, weakly acidic, and weakly alkaline gastroesophageal reflux. Pediatrics. 2006;118(2):e299–308.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Peter CS, Wiechers C, Bohnhorst B, Silny J, Poets CF. Influence of nasogastric tubes on gastroesophageal reflux in preterm infants: a multiple intraluminal impedance study. J Pediatr. 2002;141(2):277–9.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Woodley FW, Machado R, Di Lorenzo C, Mousa H. Chemical clearance in infants and children with Acid reflux in the physiologic range. J Pediatr Gastroenterol Nutr. 2015;60(6):783–6.PubMedCrossRefGoogle Scholar
  52. 52.
    Vandenplas Y, Rudolph CD, Di Lorenzo C, Hassall E, Liptak G, Mazur L, Sondheimer J, Staiano A, Thomson M, Veereman-Wauters G, Wenzl TG. North American Society for Pediatric Gastroenterology Hepatology and Nutrition, European Society for Pediatric Gastroenterology Hepatology and Nutrition. Pediatric gastroesophageal reflux clinical practice guidelines: joint recommendations of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition (NASPGHAN) and the European Society for Pediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN). J Pediatr Gastroenterol Nutr. 2009;49(4):498–597.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Lightdale JR, Gremse DA. Section on Gastroenterology H, Nutrition. Gastroesophageal reflux: management guidance for the pediatrician. Pediatrics. 2013;131(5):e1684–95.PubMedCrossRefGoogle Scholar
  54. 54.
    Davies I, Burman-Roy S, Murphy MS, Guideline Development G. Gastro-oesophageal reflux disease in children: NICE guidance. BMJ. 2015;350:g7703.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Bredenoord AJ, Weusten BL, Smout AJ. Symptom association analysis in ambulatory gastro-oesophageal reflux monitoring. Gut. 2005;54(12):1810–7.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Barriga-Rivera A, Elena M, Moya M, Lopez-Alonso M. Monte Carlo method for the evaluation of symptom association. Dis Esophagus. 2014;27(6):518–23.PubMedCrossRefGoogle Scholar
  57. 57.
    Loots CM, Benninga MA, Davidson GP, Omari TI. Addition of pH-impedance monitoring to standard pH monitoring increases the yield of symptom association analysis in infants and children with gastroesophageal reflux. J Pediatr. 2009;154(2):248–52.PubMedCrossRefGoogle Scholar
  58. 58.
    Kavitt RT, Higginbotham T, Slaughter JC, Patel D, Yuksel ES, Lominadze Z, et al. Symptom reports are not reliable during ambulatory reflux monitoring. Am J Gastroenterol. 2012;107(12):1826–32.PubMedCrossRefGoogle Scholar
  59. 59.
    Rosen R, Amirault J, Heinz N, Litman H, Khatwa U. The sensitivity of acoustic cough recording relative to intraesophageal pressure recording and patient report during reflux testing. Neurogastroenterol Motil. 2014;26(11):1635–41.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Blondeau K, Mertens V, Dupont L, Pauwels A, Farre R, Malfroot A, et al. The relationship between gastroesophageal reflux and cough in children with chronic unexplained cough using combined impedance-pH-manometry recordings. Pediatr Pulmonol. 2011;46(3):286–94.PubMedCrossRefGoogle Scholar
  61. 61.
    Omari TI, Schwarzer A, van Wijk MP, Benninga MA, McCall L, Kritas S, et al. Optimisation of the reflux-symptom association statistics for use in infants being investigated by 24-hour pH impedance. J Pediatr Gastroenterol Nutr. 2011;52(4):408–13.PubMedCrossRefGoogle Scholar
  62. 62.
    Ghezzi M, Silvestri M, Guida E, Pistorio A, Sacco O, Mattioli G, et al. Acid and weakly acid gastroesophageal refluxes and type of respiratory symptoms in children. Respir Med. 2011;105(7):972–8.PubMedCrossRefGoogle Scholar
  63. 63.
    Mattioli G, Pini-Prato A, Gentilino V, Caponcelli E, Avanzini S, Parodi S, et al. Esophageal impedance/pH monitoring in pediatric patients: preliminary experience with 50 cases. Dig Dis Sci. 2006;51(12):2341–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Condino AA, Sondheimer J, Pan Z, Gralla J, Perry D, O'Connor JA. Evaluation of gastroesophageal reflux in pediatric patients with asthma using impedance-pH monitoring. J Pediatr. 2006;149(2):216–9.PubMedCrossRefGoogle Scholar
  65. 65.
    Mousa H, Woodley FW, Metheney M, Hayes J. Testing the association between gastroesophageal reflux and apnea in infants. J Pediatr Gastroenterol Nutr. 2005;41(2):169–77.PubMedCrossRefGoogle Scholar
  66. 66.
    Patel A, Sayuk GS, Gyawali CP. Acid-based parameters on pH-impedance testing predict symptom improvement with medical management better than impedance parameters. Am J Gastroenterol. 2014;109(6):836–44.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Cresi F, Locatelli E, Marinaccio C, Grasso G, Coscia A, Bertino E. Prognostic values of multichannel intraluminal impedance and pH monitoring in newborns with symptoms of gastroesophageal reflux disease. J Pediatr. 2013;162(4):770–5.PubMedCrossRefGoogle Scholar
  68. 68.
    van der Pol RJ, van den Ouweland M, Loots CM, Vandenplas Y, Benninga MA, van Wijk MP. Follow-up after pH-metry and pH impedance in pediatric gastroesophageal reflux disease. J Pediatr Gastroenterol Nutr. 2015;60(2):224–9.PubMedCrossRefGoogle Scholar
  69. 69.
    Committee for Medicinal Products for Human Use. Guideline on the evaluation of drugs for the treatment of Gastro-oesophageal reflux disease. 2011. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2011/03/WC500103307.pdf.
  70. 70.
    Grabowski M, Seys S, Decraene A, Kasran A, Dilissen E, Barg W, et al. Airway inflammation in patients with chronic non-asthmatic cough. Thorax. 2013;68(2):125–30.PubMedCrossRefGoogle Scholar
  71. 71.
    Wenzl TG, Schneider S, Scheele F, Silny J, Heimann G, Skopnik H. Effects of thickened feeding on gastroesophageal reflux in infants: a placebo-controlled crossover study using intraluminal impedance. Pediatrics. 2003;111(4 Pt 1):e355–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Corvaglia L, Ferlini M, Rotatori R, Paoletti V, Alessandroni R, Cocchi G, et al. Starch thickening of human milk is ineffective in reducing the gastroesophageal reflux in preterm infants: a crossover study using intraluminal impedance. J Pediatr. 2006;148(2):265–8.PubMedCrossRefGoogle Scholar
  73. 73.
    Corvaglia L, Spizzichino M, Aceti A, Legnani E, Mariani E, Martini S, et al. A thickened formula does not reduce apneas related to gastroesophageal reflux in preterm infants. Neonatology. 2013;103(2):98–102.PubMedCrossRefGoogle Scholar
  74. 74.
    Davidson G, Wenzl TG, Thomson M, Omari T, Barker P, Lundborg P, et al. Efficacy and safety of once-daily esomeprazole for the treatment of gastroesophageal reflux disease in neonatal patients. J Pediatr. 2013;163(3):692–8 e1-2.PubMedCrossRefGoogle Scholar
  75. 75.
    Turk H, Hauser B, Brecelj J, Vandenplas Y, Orel R. Effect of proton pump inhibition on acid, weakly acid and weakly alkaline gastro-esophageal reflux in children. World J Pediatr. 2013;9(1):36–41.PubMedCrossRefGoogle Scholar
  76. 76.
    Castellani C, Huber-Zeyringer A, Bachmaier G, Saxena AK, Hollwarth ME. Proton pump inhibitors for reflux therapy in infants: effectiveness determined by impedance pH monitoring. Pediatr Surg Int. 2014;30(4):381–5.PubMedCrossRefGoogle Scholar
  77. 77.
    Loots CM, Wijnakker R, van Wijk MP, Davidson G, Benninga MA, Omari TI. Esophageal impedance baselines in infants before and after placebo and proton pump inhibitor therapy. Neurogastroenterol Motil. 2012;24(8):758–e352.PubMedCrossRefGoogle Scholar
  78. 78.
    Fukahori S, Yagi M, Ishii S, Asagiri K, Saikusa N, Hashizume N, et al. Laparoscopic Nissen fundoplication mainly reduces the volume of acid reflux and potentially improves mucosal integrity up to the middle esophagus in neurologically impaired children detected by esophageal combined pH-multichannel intraluminal impedance measurements. J Pediatr Surg. 2016;51(8):1283–7.PubMedCrossRefGoogle Scholar
  79. 79.
    Tanaka A, Shimono R, Kubo H, Fujii T, Miyatake N. Evaluation of antireflux surgery using multichannel intraluminal impedance-pH measurement in neurologically impaired patients. Pediatr Surg Int. 2015;31(10):911–6.PubMedCrossRefGoogle Scholar
  80. 80.
    Rosen R, Levine P, Lewis J, Mitchell P, Nurko S. Reflux events detected by pH-MII do not determine fundoplication outcome. J Pediatr Gastroenterol Nutr. 2010;50(3):251–5.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Fike FB, Pettiford JN, St Peter SD, Cocjin J, Laituri CA, Ostlie DJ. Utility of pH/multichannel intraluminal impedance probe in identifying operative patients in infants with gastroesophageal reflux disease. J Laparoendosc Adv Surg Tech A. 2012;22(5):518–20.PubMedCrossRefGoogle Scholar
  82. 82.
    Mauritz FA, Conchillo JM, van Heurn LW, Siersema PD, Sloots CE, Houwen RH, et al. Effects and efficacy of laparoscopic fundoplication in children with GERD: a prospective, multicenter study. Surg Endosc. 2016;31(3):1101–10.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Tutar E, Kutluk G, Bayrak NA, Çelıkel C, Pehlıvanoğlu E, Ertem D. What is the diagnostic utility of endoscopic scoring systems in children? Turkish J Gastroenterol Off J Turkish Soc Gastroenterol. 2012;24(1):22–9.CrossRefGoogle Scholar
  84. 84.
    Genta R, Spechler S, Kielhorn A. The Los Angeles and Savary–Miller systems for grading esophagitis: utilization and correlation with histology. Dis Esophagus. 2011;24(1):10–7.PubMedCrossRefGoogle Scholar
  85. 85.
    van der Pol RJ, Loots CM, Peeters L, Vandenplas Y, Hauser B, Devreker T, et al. Outcomes of endoscopy and novel pH-impedance parameters in children: is there a correlation? J Pediatr Gastroenterol Nutr. 2013;56(2):196–200.PubMedCrossRefGoogle Scholar
  86. 86.
    Pilic D, Hankel S, Koerner-Rettberg C, Hamelmann E, Schmidt-Choudhury A. The role of baseline impedance as a marker of mucosal integrity in children with gastro esophageal reflux disease. Scand J Gastroenterol. 2013;48(7):785–93.PubMedCrossRefGoogle Scholar
  87. 87.
    Salvatore S, Hauser B, Devreker T, Arrigo S, Marino P, Citro C, et al. Esophageal impedance and esophagitis in children: any correlation? J Pediatr Gastroenterol Nutr. 2009;49(5):566–70.PubMedCrossRefGoogle Scholar
  88. 88.
    Dalby K, Nielsen RG, Kruse-Andersen S, Fenger C, Durup J, Husby S. Gastroesophageal reflux disease and eosinophilic esophagitis in infants and children. A study of esophageal pH, multiple intraluminal impedance and endoscopic ultrasound. Scand J Gastroenterol. 2010;45(9):1029–35.PubMedCrossRefGoogle Scholar
  89. 89.
    Liu YW, Wu JF, Chen HL, Hsu HY, Chang MH, Hsu WC, et al. The correlation between endoscopic reflux esophagitis and combined multichannel intraluminal impedance-pH monitoring in children. Pediatr Neonatol. 2015;57(5):385–9.PubMedCrossRefGoogle Scholar
  90. 90.
    Hojsak I, Ivkovic L, Trbojevic T, Pavic I, Jadresin O, Misak Z, et al. The role of combined 24-h multichannel intraluminal impedance-pH monitoring in the evaluation of children with gastrointestinal symptoms suggesting gastro-esophageal reflux disease. Neurogastroenterol Motil. 2016;28(10):1488–93.PubMedCrossRefGoogle Scholar
  91. 91.
    Farre R, Blondeau K, Clement D, Vicario M, Cardozo L, Vieth M, et al. Evaluation of oesophageal mucosa integrity by the intraluminal impedance technique. Gut. 2011;60(7):885–92.PubMedCrossRefGoogle Scholar
  92. 92.
    Borrelli O, Salvatore S, Mancini V, Ribolsi M, Gentile M, Bizzarri B, et al. Relationship between baseline impedance levels and esophageal mucosal integrity in children with erosive and non-erosive reflux disease. Neurogastroenterol Motil. 2012;24(9):828–e394.PubMedCrossRefGoogle Scholar
  93. 93.
    Salvatore S, Salvatoni A, Ummarino D, Ghanma A, Van der Pol R, Rongen A, et al. Low mean impedance in 24-hour tracings and esophagitis in children: a strong connection. Dis Esophagus. 2016;29(1):10–4.PubMedCrossRefGoogle Scholar
  94. 94.
    Salvatore S, Salvatoni A, Van Steen K, Ummarino D, Hauser B, Vandenplas Y. Behind the (impedance) baseline in children. Dis Esophagus. 2014;27(8):726–31.PubMedCrossRefGoogle Scholar
  95. 95.
    Kessing BF, Bredenoord AJ, Weijenborg PW, Hemmink GJ, Loots CM, Smout AJ. Esophageal acid exposure decreases intraluminal baseline impedance levels. Am J Gastroenterol. 2011;106(12):2093–7.PubMedCrossRefGoogle Scholar
  96. 96.
    Salvatore S, Salvatoni A, Van Berkel M, Van Steen K, Unmarino D, Ghanma A, et al. Esophageal impedance baseline is age dependent. J Pediatr Gastroenterol Nutr. 2013;57(4):506–13.PubMedCrossRefGoogle Scholar
  97. 97.
    Tambucci R, Thapar N, Saliakellis E, Pescarin M, Quitadamo P, Cristofori F, et al. Clinical relevance of esophageal baseline impedance measurement: just an innocent bystander. J Pediatr Gastroenterol Nutr. 2015;60(6):776–82.PubMedCrossRefGoogle Scholar
  98. 98.
    Singendonk MM, Kritas S, Cock C, Ferris LF, McCall L, Rommel N, et al. Pressure-flow characteristics of normal and disordered esophageal motor patterns. J Pediatr. 2015;166(3):690–6.e1.PubMedCrossRefGoogle Scholar
  99. 99.
    Thilmany C, Beck-Ripp J, Griese M. Acid and non-acid gastro-esophageal refluxes in children with chronic pulmonary diseases. Respir Med. 2007;101(5):969–76.PubMedCrossRefGoogle Scholar
  100. 100.
    Borrelli O, Marabotto C, Mancini V, Aloi M, Macri F, Falconieri P, et al. Role of gastroesophageal reflux in children with unexplained chronic cough. J Pediatr Gastroenterol Nutr. 2011;53(3):287–92.PubMedCrossRefGoogle Scholar
  101. 101.
    Tolin Hernani M, Crespo Medina M, Luengo Herrero V, Martinez Lopez C, Salcedo Posadas A, Alvarez Calatayud G, et al. Comparison between conventional ph measurement and multichannel intraluminal esophageal impedance in children with respiratory disorders. An Pediatr (Barc.). 2012;77(2):103–10.CrossRefGoogle Scholar
  102. 102.
    Ghezzi M, Guida E, Ullmann N, Sacco O, Mattioli G, Jasonni V, et al. Weakly acidic gastroesophageal refluxes are frequently triggers in young children with chronic cough. Pediatr Pulmonol. 2013;48(3):295–302.PubMedCrossRefGoogle Scholar
  103. 103.
    Pavic I, Cepin-Bogovic J, Hojsak I. The relationship between gastroesophageal reflux and chronic unexplained cough in children. Clin Pediatr (Philadelphia). 2016;55(7):639–44.CrossRefGoogle Scholar
  104. 104.
    Wenzl TGSJ, Schenke S, Peschgens T, Heimann G, Skopnik H. Gastroesophageal reflux and respiratory phenomena in infants: status of the intraluminal impedance technique. J Pediatr Gastroenterol Nutr. 1999;28(4):423–8.PubMedCrossRefGoogle Scholar
  105. 105.
    Magista AM, Indrio F, Baldassarre M, Bucci N, Menolascina A, Mautone A, et al. Multichannel intraluminal impedance to detect relationship between gastroesophageal reflux and apnoea of prematurity. Dig Liver Dis. 2007;39(3):216–21.PubMedCrossRefGoogle Scholar
  106. 106.
    Corvaglia L, Zama D, Spizzichino M, Aceti A, Mariani E, Capretti MG, et al. The frequency of apneas in very preterm infants is increased after non-acid gastro-esophageal reflux. Neurogastroenterol Motil. 2011;23(4):303–e152.PubMedCrossRefGoogle Scholar
  107. 107.
    Machado R, Woodley FW, Skaggs B, Di Lorenzo C, Splaingard M, Mousa H. Gastroesophageal reflux causing sleep interruptions in infants. J Pediatr Gastroenterol Nutr. 2013;56(4):431–5.PubMedCrossRefGoogle Scholar
  108. 108.
    Machado RS, Woodley FW, Skaggs B, Di Lorenzo C, Eneli I, Splaingard M, et al. Gastroesophageal reflux affects sleep quality in snoring obese children. Pediatr Gastroenterol Hepatol Nutr. 2016;19(1):12–9.Google Scholar
  109. 109.
    Salvatore S, Arrigo S, Luini C, Vandenplas Y. Esophageal impedance in children: symptom-based results. J Pediatr. 2010;157(6):949–54 e1-2.PubMedCrossRefGoogle Scholar
  110. 110.
    Lüthold SC. Disagreement between symptom-reflux association analysis parameters in pediatric gastroesophageal reflux disease investigation. World J Gastroenterol. 2010;16(19):2401.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Greifer M, Ng K, Levine J. Impedance and extraesophageal manifestations of reflux in pediatrics. Laryngoscope. 2012;122(6):1397–400.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Maartje M. J. Singendonk
    • 1
  • F. Jaime
    • 1
    • 2
  • S. Salvatore
    • 3
  • M. M. Tabbers
    • 1
  • M. A. Benninga
    • 1
  • Y. Vandenplas
    • 4
  1. 1.Department of Paediatric Gastroenterology and NutritionEmma Children’s Hospital AMCAmsterdamThe Netherlands
  2. 2.Department of Paediatric Gastroenterology and NutritionPontificia Universidad Católica de ChileSantiagoChile
  3. 3.Paediatrics, Clinical Pediatrica di VareseUniversita dell’InsubriaVareseItaly
  4. 4.Department of PaediatricsUZ Brussel, Vrije Universiteit BrusselsBrusselsBelgium

Personalised recommendations