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The Pathogenesis and Management of Achalasia: Current Status and Future Directions

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The Pathogenesis and Management of Achalasia: Current Status and Future Directions Gut and Liver, Vol. 9, No. 4, July 2015, pp. 449-463 Review The Pathogenesis and Management of Achalasia: Current Status and Future Directions Fehmi Ates and Michael F. Vaezi Division of Gastroenterology, Hepatology, and Nutrition, Center for Swallowing and Esophageal Disorders, Vanderbilt University Medical Center, Nashville, TN, USA Achalasia is an esophageal motility disorder that is common- are idiopathic, but the syndrome can be associated with malig- ly misdiagnosed initially as gastroesophageal reflux disease. nancy (especially involving the gastroesophageal junction) and Patients with achalasia often complain of dysphagia with sol- as a part of the spectrum of Chagas disease. Rarely, achalasia is ids and liquids but may focus on regurgitation as the primary genetically transmitted.2 symptom, leading to initial misdiagnosis. Diagnostic tests Achalasia is an uncommon esophageal motility disorder de- for achalasia include esophageal motility testing, esophago- fined traditionally by manometric criteria in the classic setting gastroduodenoscopy and barium swallow. These tests play a of dysphagia.3-7 The symptomatic consequence of this motility complimentary role in establishing the diagnosis of suspect- disorder is the classic presentation of dysphagia to solids and ed achalasia. High-resolution manometry has now identified liquids associated with regurgitation of bland undigested food three subtypes of achalasia, with therapeutic implications. or saliva.3 Substernal chest pain during meals in the setting of Pneumatic dilation and surgical myotomy are the only defini- dysphagia, weight loss, and even heartburn may be accompa- tive treatment options for patients with achalasia who can nying symptoms that often lead to misdiagnosis of achalasia undergo surgery. Botulinum toxin injection into the lower erroneously as gastroesophageal reflux disease (GERD).8,9 Acha- esophageal sphincter should be reserved for those who can- lasia must be suspected in those with dysphagia to solids and not undergo definitive therapy. Close follow-up is paramount liquids and in those with regurgitation unresponsive to initial because many patients will have a recurrence of symptoms trial of proton pump inhibitor (PPI) therapy.10 Endoscopic find- and require repeat treatment. (Gut Liver 2015;9:449-463) ings of retained saliva, liquid, and food in the esophagus with- out mechanical obstruction from stricture or mass should raise Key Words: Pneumatic dilation; Surgical myotomy; Peroral suspicion for achalasia. Conversely, other conditions may mimic esophageal myotomy achalasia both clinically and manometrically. These include pseudoachalasia from tumors in the gastric cardia or those infil- INTRODUCTION trating the myenteric plexus (adenocarcinoma of gastroesopha- geal junction, pancreatic, breast, lung, or hepatocellular cancers) Achalasia is a primary esophageal motor disorder of unknown or secondary achalasia from extrinsic processes such as prior etiology characterized manometrically by insufficient relaxation tight fundoplication or laparoscopic adjustable gastric band- of the lower esophageal sphincter (LES) and loss of esophageal ing.11,12 peristalsis; radiographically by aperistalsis, esophageal dilation, 1. History with minimal LES opening, “bird-beak” appearance, poor emp- tying of barium; and endoscopically by dilated esophagus with Achalasia was first described and termed by Sir Thomas Willis retained saliva, liquid, and undigested food particles in the ab- in 1674, where he suggested that the disease is due to the loss sence of mucosal stricturing or tumor. Achalasia occurs equally of normal inhibition in the distal esophagus.13 Since then, the in both genders with prevalence that ranges up to 1 per 10,000 development of new diagnostic techniques stimulated new ideas persons.1 There is no racial predilection. The majority of cases on the etiology and pathophysiology of the disease leading to Correspondence to: Michael F. Vaezi Division of Gastroenterology and Hepatology, Center for Swallowing and Esophageal Disorders, Vanderbilt University Medical Center, C2104-MCN, Nashville, TN 37232, USA Tel: +1-615-322-3739, Fax: +1-615-322-8525, E-mail: [email protected] Received on November 14, 2014. Accepted on December 7, 2014. pISSN 1976-2283 eISSN 2005-1212 http://dx.doi.org/10.5009/gnl14446 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 450 Gut and Liver, Vol. 9, No. 4, July 2015 various theories in identifying the nature of motor disturbances In addition to tonic contraction and relaxation, the inhibi- in esophageal regions. This includes cardiospasm, esophageal tory neurons are also vital to normal esophageal peristalsis. The muscle failure, and physical obstruction.14 In 1929, Sir Arthur esophagus, at baseline, is in a contractile state; however, with Hurst coined the term “achalasia” suggesting that it may be deglutition, the inhibitory neurons are excited to override the due to the “loss of normal inhibition” in the distal esophagus.13 effect of excitatory neurons resulting in esophagus relaxation. Subsequently, a body of evidence has emerged showing that Peristalsis is the net result of the coordinated relaxation and idiopathic achalasia, characterized by the failure of the lower contraction mediated by the inhibitory and excitatory myenteric esophageal sphincter (LES) relaxation and aperistalsis, is indeed plexus neurons along the length of the esophagus.21 In achala- caused primarily by the loss of the inhibitory innervation of the sia, there is loss of NO and VIP releasing inhibitory neurons.22,23 esophageal myenteric plexus. However, the initiating cause is Thus, the loss of the inhibitory innervation in achalasia results still elusive. in the manometric consequence of failure of LES relaxation as well as loss of esophageal peristalsis. 2. Esophageal motor innervation Esophageal motor innervation is through the vagus nerve via PATHOGENESIS the Myenteric or Meissner’s plexus (Fig. 1A). Neural innerva- tion differs in the proximal and distal esophagus. The striated Pathophysiologically, the loss of the inhibitory innervation of muscle of the proximal esophagus is innervated by the somatic the esophagus can be due to either extrinsic or intrinsic causes. efferent fibers of the vagus nerve (Fig. 1B). The cell bodies for Extrinsic causes may include central nervous system (CNS) le- these fibers originate in the nucleus ambiguous and terminate sions involving the DMN or the vagal nerve fibers, while intrin- on the motor end plate directly via cholinergic receptors.15,16 sic loss may be due to loss of the inhibitory ganglion cells in the On the other hand, the smooth muscle of the distal esophagus myenteric plexus. is innervated by the preganglionic vagus nerve fibers with cell 1. Extrinsic neuronal loss bodies located in the dorsal motor nucleus (DMN).17 Pregangli- onic fibers first innervate the myenteric plexus via cholinergic Kimura24 was the first to suggest lesions in the CNS could ex- fibers.18 The esophageal wall and LES are subsequently inner- plain the clinical and manometric findings in achalasia. In 1929, vated by the postganglionic neurons, consisting of excitatory he examined histologic sections of postmortem specimens of and inhibitory neurons. The postganglionic excitatory neurons three achalasia patients. He discovered degenerated vagus nerve release acetylcholine while the inhibitory neurons release nitric cells in the DMN. Similar DMN pathology was later reported by oxide (NO) and vasoactive intestinal polypeptide (VIP) resulting Cassella et al.25 This group conducted a histologic study of serial in esophageal and LES contractions and relaxations, respec- brain-stem sections of two achalasia patients and one control. tively (Fig. 1B).19,20 They found a 34% to 43% decrease in the number of DMN neu- AB Upper esophagus Ach Meissner's plexus + (submucosal) Striated muscle fiber Auerbach's plexus (myenteric) Lower esophagus Circular muscle Vagus nerve Ach + + Ach Vagus nerve Dorsal motor nucleus Longitudinal muscle Nucleus ambiguus Ach + NO, VIP Smooth muscle fiber Fig. 1. (A) Esophageal motor innervation by the vagus nerve; Auerbach’s and Meissner’s plexuses. (B) The striated muscle of the proximal esophagus is directly innervated by the somatic efferent cholinergic fibers of the vagus nerve originating from the nucleus ambiguus. In contrast, the smooth muscle of the distal esophagus is innervated by the preganglionic vagus nerve fibers from the dorsal motor nucleus. The preganglionic vagus fibers release acetylcholine, a neurotransmitter that affects two types of postganglionic neurons in the myenteric plexus, the excitatory cholinergic neurons and the inhibitory nitrinergic neurons. NO, nitric oxide; VIP, vasoactive intestinal polypeptide. Ates F and Vaezi MF: The Pathogenesis and Management of Achalasia 451 rons bilaterally in the achalasia patients compared to the con- while cholinergic medications increased it confirming that the trol. To examine the effect of above observations, Higgs et al.26 cholinergic neurons in achalasia are preserved. This is the same prospectively induced bilateral DMN lesions on 13 cats using mechanism through which botulinum toxin reduces the LES direct current. Nine out of the 13 cats with DMN lesions (69%) pressure and
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