The spectrum of achalasia: Lessons from studies of pathophysiology and high-resolution manometry

Gastroenterology

Volumn 145, Issue 5, 2013, Pages 954-965

  Kahrilas, Peter J ^a   Boeckxstaens, Guy ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Achalasia; Dysphagia; Esophageal Motility; Pathogenesis

Indexed keywords

CYTOKINE;

AGANGLIONOSIS; ANTIBODY RESPONSE; AUTOIMMUNITY; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; ESOPHAGUS ACHALASIA; ESOPHAGUS MANOMETRY; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HUMAN; INFLAMMATION; LOWER ESOPHAGUS SPHINCTER; MYENTERIC PLEXUS; PATHOGENESIS; PATHOPHYSIOLOGY; PERISTALSIS; PHENOTYPE; POSTGANGLIONIC NERVE; PRIORITY JOURNAL; REVIEW;

EID: 84886793082     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2013.08.038     Document Type: Review

References (112)

1. F.C. Lendrum Anatomic features of the cardiac orifice of the stomach with special reference to cardiospasm Arch Intern Med 59 1937 474-451
2. J.E. Pandolfino, and P.J. Kahrilas The second American Gastroenterological Association technical review on the clinical use of esophageal manometry Gastroenterology 128 2005 209 229
3. J.E. Pandolfino, and P.J. Kahrilas American Gastroenterological Association medical position statement: clinical use of esophageal manometry Gastroenterology 128 2005 207 208
4. A.J. Bredenoord, M. Fox, and P.J. Kahrilas Chicago Classification criteria of esophageal motility disorders defined in high resolution esophageal pressure topography Neurogastroenterol Motil 24 Suppl 1 2012 57 65
5. P.J. Kahrilas, S.M. Kishk, and J.F. Helm A comparison of pseudoachalasia and achalasia Am J Med 82 1987 439 446
6. R.B. de Oliveira, J. Rezende Filho, and R.O. Dantas The spectrum of esophageal motor disorders in Chagas' disease Am J Gastroenterol 90 1995 1119 1124
7. G.E. Boeckxstaens Achalasia: virus-induced euthanasia of neurons? Am J Gastroenterol 103 2008 1610 1612
8. J.E. Pandolfino, M.A. Kwiatek, and T. Nealis Achalasia: a new clinically relevant classification by high-resolution manometry Gastroenterology 135 2008 1526 1533
9. G.W. Meyer, R.M. Austin, and C.E. Brady III Muscle anatomy of the human esophagus J Clin Gastroenterol 8 1986 131 134
10. J. Christensen, G.A. Rick, and B.A. Robison Arrangement of the myenteric plexus throughout the gastrointestinal tract of the opossum Gastroenterology 85 1983 890 899
11. J.G. Brasseur Mechanical studies of the esophageal function Dysphagia 8 1993 384 386
12. R.E. Clouse, and A. Staiano Topography of normal and high-amplitude esophageal peristalsis Am J Physiol 265 1993 G1098 G1107
13. C. Roman, and A. Car Déglutitions et contractions oesophagiennes réflexes obtenues par la stimulation des nerfs vague et laryngé supérieur Exp Brain Res 11 1970 48 74
14. J. Murray, C. Du, and A. Ledlow Nitric oxide: mediator of nonadrenergic noncholinergic responses of opossum esophageal muscle Am J Physiol 261 1991 G401 G406
15. P. Biancani, J.H. Walsh, and J. Behar Vasoactive intestinal polypeptide. A neurotransmitter for lower esophageal sphincter relaxation J Clin Invest 73 1984 963 967
16. M. Guelrud, A. Rossiter, and P.F. Souney The effect of vasoactive intestinal polypeptide on the lower esophageal sphincter in achalasia Gastroenterology 103 1992 377 382
17. H. Kuramato, M. Kadowaki, and N. Yoshida Morphological demonstration of a vagal inhibitory pathway to the lower esophageal sphincter via nitrergic neurons in the rat esophagus Neurogastroenterol Motil 25 2013 e485 e494
18. J. Christensen, S. Fang, and G.A. Rick NADPH-diaphorase-positive nerve fibers in smooth muscle layers of opossum esophagus: gradients in density J Auton Nerv Syst 52 1995 99 105
19. J.R. Crist, J.S. Gidda, and R.K. Goyal Intramural mechanism of esophageal peristalsis: roles of cholinergic and noncholinergic nerves Proc Natl Acad Sci U S A 81 1984 3595 3599
20. J.S. Gidda, and R.K. Goyal Regional gradient of initial inhibition and refractoriness in esophageal smooth muscle Gastroenterology 89 1985 843 851
21. J.S. Gidda, and R.K. Goyal Swallow-evoked action potentials in the vagal preganglionic efferents J Neurophysiol 52 1984 1169 1180
22. A. Staiano, and R.E. Clouse The effects of cisapride on the topography of oesophageal peristalsis Aliment Pharmacol Ther 10 1996 875 882
23. J. Hellemans, G. Vantrappen, and P. Valembois Electrical activity of striated and smooth muscle of the esophagus Am J Dig Dis 13 1968 320 334
24. G.W. Meyer, and D.O. Castell Current concepts of esophageal function Am J Otolaryngol 1 1980 440 446
25. P. Ask, and L. Tibling Effect of time interval between swallows on esophageal peristalsis Am J Physiol 238 1980 G485
26. A.W. Vanek, and N.E. Diamant Responses of the human esophagus to paired swallows Gastroenterology 92 1987 G485
27. J.L. Conklin, C.A. Du, and K. Schulze-Delrieu Hypertrophic smooth muscle in the partially obstructed opossum esophagus. Excitability and electrophysiological properties Gastroenterology 101 1991 657 663
28. R.K. Mittal, J. Ren, R.W. McCallum, and H.A. Shaffer Jr. Modulation of feline esophageal contractions by bolus volume and outflow obstruction Am J Physiol 258 1990 G208 G215
29. J.H. Schneider, J.H. Peters, and E. Kirkman Are the motility abnormalities of achalasia reversible? An experimental outflow obstruction in the feline model Surgery 125 1999 498 503
30. C. Cruiziat, S. Roman, and M. Robert High-resolution esophageal manometry evaluation in symptomatic patients after gastric banding for morbid obesity Dig Liver Dis 43 2011 116 120
31. A. Khan, C. Ren-Fielding, and M. Traube Potentially reversible pseudoachalasia after laparoscopic adjustable gastric banding J Clin Gastroenterol 45 2011 775 779
32. C.P. Gyawali, and V.M. Kushnir High-resolution manometric characteristics help differentiate types of distal esophageal obstruction in patients with peristalsis Neurogastroenterol Motil 23 2011 502-e197
33. S. Roman, J.E. Pandolfino, and J. Chen Phenotypes and clinical context of hypercontractility in high resolution esophageal pressure topography (EPT) Am J Gastroenterol 107 2012 37 45
34. J. Christensen, J.L. Conklin, and B.W. Freeman Physiologic specialization at esophagogastric junction in three species Am J Physiol 225 1973 1265 1270
35. R.K. Goyal, and S. Rattan Genesis of basal sphincter pressure: effect of tetrodotoxin on lower esophageal sphincter pressure in opossum in vivo Gastroenterology 71 1976 62 67
36. R. Asoh, and R.K. Goyal Electrical activity of the opossum lower esophageal sphincter in vivo Gastroenterology 74 1978 835 840
37. W. Zelcer, and N.W. Weisbrodt Electrical and mechanical activity of the lower esophageal sphincter in the cat Am J Physiol 246 1984 G243 G247
38. D.L. Dektor, and J.P. Ryan Transmembrane voltage of opossum esophageal smooth muscle and its response to electrical stimulation of intrinsic nerves Gastroenterology 82 1982 301 308
39. M.S. Kannan, L.P. Jagler, and E.E. Daniel Electrical properties of smooth muscle cell membrane of opossum esophagus Am J Physiol 248 1985 G342 G346
40. K. Schulze, J.J. Hajjar, and J. Christensen Regional differences in potassium content of smooth muscle from opossum esophagus Am J Physiol 235 1978 E709 E713
41. W. Schlippert, K. Schulze, and E.L. Forker Calcium in smooth muscle from the opossum esophagus Proc Soc Exp Biol Med 162 1979 354 358
42. M.A. Kwiatek, F. Nicodème, and J.E. Pandolfino Pressure morphology of the relaxed lower esophageal sphincter: the formation and collapse of the phrenic ampulla Am J Physiol Gastrointest Liver Physiol 302 2012 G389 G396
43. I. Dogan, V. Bhargava, and J. Liu Axial stretch: a novel mechanism of the lower esophageal sphincter relaxation Am J Physiol 292 2007 G329 G334
44. Y. Jiang, V. Bhargava, and R.K. Mittal Mechanism of stretch-activated excitatory and inhibitory responses in the lower esophageal sphincter Am J Physiol 297 2009 G397 G405
45. J. Christensen, and R. Miftakhov Hiatus hernia: a review of evidence for its origin in esophageal longitudinal muscle dysfunction Am J Med 108 Suppl 4a 2000 3S 7S
46. R. Yassi, L.K. Cheng, and V. Rajagopal Modeling of the mechanical function of the human gastroesophageal junction using an anatomically realistic three-dimensional model J Biomech 42 2009 1604 1609
47. J. Gonella, J.P. Niel, and C. Roman Vagal control of lower oesophageal sphincter motility in the cat J Physiol 273 1977 647 664
48. W.J. Dodds, J. Dent, and W.J. Hogan Effect of atropine on esophageal motor function in humans Am J Physiol 240 1981 G290 G296
49. W.A. Klein, H.P. Parkman, and D.T. Dempsey Sphincterlike thoracoabdominal high pressure zone after esophagogastrectomy Gastroenterology 105 1993 1362 1369
50. R.L. Young, A.J. Page, and N.J. Cooper Sensory and motor innervation of the crural diaphragm by the vagus nerves Gastroenterology 138 2010 1091 1101
51. R.K. Mittal, D.F. Rochester, and R.W. McCallum Sphincteric action of the diaphragm during a relaxed lower esophageal sphincter in humans Am J Physiol 256 1989 G139 G144
52. R.K. Mittal, M. Fisher, and R.W. McCallum Human lower esophageal sphincter pressure response to increased intra-abdominal pressure Am J Physiol 258 1990 G624 G630
53. A. De Troyer, M. Sampson, and S. Sigrist Action of costal and crural parts of the diaphragm on the rib cage in dog J Appl Physiol 53 1982 30 39
54. S.M. Altschuler, J.T. Boyle, and T.E. Nixon Simultaneous reflex inhibition of lower esophageal sphincter and crural diaphragm in cats Am J Physiol 249 1985 G586 G591
55. R.K. Goyal, and S. Rattan Nature of the vagal inhibitory innervation to the lower esophageal sphincter J Clin Invest 55 1975 1119 1126
56. K.S. Murthy, K.M. Zhang, and J.G. Jin VIP-mediated G protein-coupled Ca2+ influx activates a constitutive NOS in dispersed gastric muscle cells Am J Physiol 265 1993 G660 G671
57. C. Nathan, and Q.W. Xie Nitric oxide synthases: roles, tolls, and controls Cell 78 1994 915 918
58. R.K. Mittal, R.H. Holloway, and R. Penagini Transient lower esophageal sphincter relaxation Gastroenterology 109 1995 601 610
59. R.H. Holloway, M. Hongo, and K. Berger Gastric distention: a mechanism for postprandial gastroesophageal reflux Gastroenterology 89 1985 779 784
60. J.E. Pandolfino, Q.G. Zhang, and S.K. Ghosh Transient lower esophageal sphincter relaxations and reflux: mechanistic analysis using concurrent fluoroscopy and high-resolution manometry Gastroenterology 131 2006 1725 1733
61. A. Babaei, V. Bhargava, and H. Korsapati A unique longitudinal muscle contraction pattern associated with transient lower esophageal sphincter relaxation Gastroenterology 134 2008 1322 1331
62. J.E. Pandolfino, S.K. Ghosh, and Q. Zhang Upper sphincter function during transient lower oesophageal sphincter relaxation (tLOSR); it is mainly about microburps Neurogastroenterol Motil 19 2007 203 210
63. R.E. Clouse, and A. Staiano Topography of the esophageal peristaltic pressure wave Am J Physiol 261 1991 G677 G684
64. R.E. Clouse, A. Staiano, and A. Alrakawi Application of topographical methods to clinical esophageal manometry Am J Gastroenterol 95 2000 2720 2730
65. S.K. Ghosh, J.E. Pandolfino, and J. Rice Impaired deglutitive EGJ relaxation in clinical esophageal manometry: a quantitative analysis of 400 patients and 75 controls Am J Physiol 293 2007 G878 G885
66. A. Staiano, and R.E. Clouse Detection of incomplete lower esophageal sphincter relaxation with conventional point-pressure sensors Am J Gastroenterol 96 2001 3258 3267
67. K.M. Galey, C.L. Wilshire, and S. Niebisch Atypical variants of classic achalasia are common and currently under-recognized: a study of prevalence and clinical features J Am Coll Surg 213 2011 155 161
68. I. Hirano, R.P. Tatum, and G. Shi Manometric heterogeneity in patients with idiopathic achalasia Gastroenterology 120 2001 789 798
69. S. Roman, P.J. Kahrilas, and F. Mion Partial recovery of peristalsis after myotomy for achalasia: more the rule than the exception JAMA Surg 148 2013 157 164
70. I. Dogan, J.L. Puckett, and B.S. Padda Prevalence of increased esophageal muscle thickness in patients with esophageal symptoms Am J Gastroenterol 102 2007 137 145
71. D.L. Friesen, R.D. Henderson, and W. Hanna Ultrastructure of the esophageal muscle in achalasia and diffuse esophageal spasm Am J Clin Pathol 79 1983 319 325
72. J.R. Goldblum, T.W. Rice, and J.E. Richter Histopathologic features in esophagomyotomy specimens from patients with achalasia Gastroenterology 111 1996 648 654
73. S.B. Clark, T.W. Rice, and R.R. Tubbs The nature of the myenteric infiltrate in achalasia: an immunohistochemical analysis Am J Surg Pathol 24 2000 1153 1158
74. V. Villanacci, V. Annese, and A. Cuttitta An immunohistochemical study of the myenteric plexus in idiopathic achalasia Clin Gastroenterol 44 2010 407 410
75. A. Kilic, A.M. Krasinskas, and S.R. Owens Variations in inflammation and nerve fiber loss reflect different subsets of achalasia patients J Surg Res 143 2007 177 182
76. A. Kilic, S.R. Owens, and A. Pennathur An increased proportion of inflammatory cells express tumor necrosis factor alpha in idiopathic achalasia of the esophagus Dis Esoph 22 2009 382 385
77. M. Hoshino, N. Omura, and F. Yano Immunohistochemical study of the muscularis externa of the esophagus in achalasia patients Dis Esophagus 26 2013 14 21
78. R. De Giorgio, M.P. Di Simone, and V. Stanghellini Esophageal and gastric nitric oxide synthesizing innervation in primary achalasia Am J Gastroenterol 94 1999 2357 2362
79. W.B. Storch, V.F. Eckardt, and T. Junginger Complement components and terminal complement complex in oesophageal smooth muscle of patients with achalasia Cell Mol Biol 48 2002 247 252
80. A. Tøttrup, K. Fredens, and P. Funch-Jensen Eosinophil infiltration in primary esophageal achalasia. A possible pathogenic role Dig Dis Sci 34 1989 1894 1899
81. E. Savarino, L. Gemignani, and P. Zentilin Achalasia with dense eosinophilic infiltrate responds to steroid therapy Clin Gastroenterol Hepatol 9 2011 1104 1106
82. A. Ruiz-de-Leon, J. Mendoza, and C. Sevilla-Mantilla Myenteric antiplexus antibodies and class II HLA in achalasia Dig Dis Sci 47 2002 15 19
83. P.L. Moses, L.M. Ellis, and M.R. Anees Antineuronal antibodies in idiopathic achalasia and gastro-oesophageal reflux disease Gut 52 2003 629 636
84. V.A. Lennon, D.F. Sas, and M.F. Busk Enteric neuronal autoantibodies in pseudoobstruction with small-cell lung carcinoma Gastroenterology 100 1991 137 142
85. H.R. Lee, V.A. Lennon, and M. Camilleri Paraneoplastic gastrointestinal motor dysfunction: clinical and laboratory characteristics Am J Gastroenterol 96 2001 373 379
86. W.O. Rohof, R. Salvador, and V. Annese Outcomes of treatment for achalasia depend on manometric subtype Gastroenterology 144 2013 718 725
87. S. Bruley des Varannes, J. Chevalier, and S. Pimont Serum from achalasia patients alters neurochemical coding in the myenteric plexus and nitric oxide mediated motor response in normal human fundus Gut 55 2006 319 326
88. H.S. Kim, H. Park, and J.H. Lim Morphometric evaluation of oesophageal wall in patients with nutcracker oesophagus and ineffective oesophageal motility Neurogastroenterol Motil 20 2008 869 876
89. W.G. Paterson, I.T. Beck, and L.R. Da Costa Transition from nutcracker esophagus to achalasia. A case report J Clin Gastroenterol 13 1991 554 558
90. L.H. Fontes, F.A. Herbella, and T.N. Rodriguez Progression of diffuse esophageal spasm to achalasia: incidence and predictive factors Dis Esophagus 26 2013 470 474
91. S.S. Khatami, F. Khandwala, and S.S. Shay Does diffuse esophageal spasm progress to achalasia? A prospective cohort study Dig Dis Sci 50 2005 1605 1610
92. W.B. Storch, V.F. Eckardt, and M. Wienbeck Autoantibodies to Auerbach's plexus in achalasia Cell Mol Biol 41 1995 1033 1038
93. M. Facco, P. Brun, and I. Baesso T cells in the myenteric plexus of achalasia patients show a skewed TCR repertoire and react to HSV-1 antigens Am J Gastroenterol 103 2008 1598 1609
94. S. Birgisson, M.S. Galinski, and J.R. Goldblum Achalasia is not associated with measles or known herpes and human papilloma viruses Dig Dis Sci 42 1997 300 306
95. H. Niwamoto, E. Okamoto, and J. Fujimoto Are human herpes viruses or measles virus associated with esophageal achalasia? Dig Dis Sci 40 1995 859 864
96. C.S. Robertson, B.A. Martin, and M. Atkinson Varicella-zoster virus DNA in the oesophageal myenteric plexus in achalasia Gut 34 1993 299 302
97. I. Castagliuolo, P. Brun, and M. Costantini Esophageal achalasia: is the herpes simplex virus really innocent? J Gastrointest Surg 8 2004 24 30
98. D.A. Wattchow, and M. Costa Distribution of peptide-containing nerve fibres in achalasia of the oesophagus J Gastroenterol Hepatol 11 1996 478 485
99. E.A. Gaumnitz, P. Bass, and M.A. Osinski Electrophysiological and pharmacological responses of chronically denervated lower esophageal sphincter of the opossum Gastroenterology 109 1995 789 799
100. V. Kushnir, G.S. Sayuk, and C.P. Gyawali Multiple rapid swallow responses segregate achalasia subtypes on high-resolution manometry Neurogastroenterol Motil 24 2012 1069-e561
101. D. Savojardo, M. Mangano, and P. Cantù Multiple rapid swallowing in idiopathic achalasia; evidence for patients' heterogeneity Neurogastroenterol Motil 19 2008 263 269
102. J.R. Goldblum, R.I. Whyte, and M.B. Orringer Achalasia. A morphologic study of 42 resected specimens Am J Surg Pathol 18 1994 327 337
103. A. Csendes, G. Smok, and I. Braghetto Gastroesophageal sphincter pressure and histological changes in distal esophagus in patients with achalasia of the esophagus Dig Dis Sci 30 1985 941 945
104. S.J. Hong, V. Bhargava, and Y. Jiang A unique esophageal motor pattern that involves longitudinal muscles is responsible for emptying in achalasia esophagus Gastroenterology 139 2010 102 111
105. R.K. Mittal, S.J. Hong, and V. Bhargava Longitudinal muscle dysfunction in achalasia and its relevance J Neurogastroenterol Motil 19 2013 126 136
106. K.A. Kwiatek, J. Post, and J.E. Pandolfino Transient lower esophageal sphincter relaxation in achalasia: everything but LES relaxation Neurogastroenterol Mot 21 2009 1250 1255
107. P. Parrilla, and L.F. Martinez de Haro Factors involved in the return of peristalsis in patients with achalasia of the cardia after Heller's myotomy Am J Gastroenterol 90 1995 713 717
108. G. Zaninotto, M. Costantini, and M. Anselmino Onset of oesophageal peristalsis after surgery for idiopathic achalasia Br J Surg 82 1995 1532 1534
109. R.P. Tatum, J.A. Wong, and E.J. Figueredo Return of esophageal function after treatment for achalasia as determined by impedance-manometry J Gastrointest Surg 11 2007 1403 1409
110. F. Nicodème, A. Ruigh, and Y. Xiao A comparison of symptom severity and bolus retention to Chicago Classification esophageal topography metrics in achalasia Clin Gastroenterol Hepatol 11 2013 131 137
111. M. Metzger, C. Caldwell, and A.J. Barlow Enteric nervous system stem cells derived from human gut mucosa for the treatment of aganglionic gut disorders Gastroenterology 136 2009 2214 2225
112. S. Kulkarni, L. Becker, and J.P. Pasricha Stem cell transplantation in neurodegenerative disorders of the gastrointestinal tract: future or fiction? Gut 61 2012 613 621