111 2 3 1 4 5 6 The Anatomy and Physiology of 7 8 the Oesophagus 9 1011 Peter J. Lamb and S. Michael Griffin 1 2 3 4 5 6 7 8 911 2011 location deep within the and , 1 Aims a close anatomical relationship to major struc- 2 tures throughout its course and a marginal 3 ● To develop an understanding of the blood supply, the surgical exposure, resection 4 surgical anatomy of the oesophagus. and reconstruction of the oesophagus are 5 ● To establish the normal physiology and complex. Despite advances in perioperative 6 control of . care, oesophagectomy is still associated with the 7 highest mortality of any routinely performed ● To determine the structure and function 8 elective surgical procedure [1]. of the antireflux barrier. 9 In order to understand the pathophysiol- 3011 ● To evaluate the effect of surgery on the ogy of oesophageal disease and the rationale 1 function of the oesophagus. for its medical and surgical management a 2 basic knowledge of oesophageal anatomy and 3 physiology is essential. The embryological 4 Introduction development of the oesophagus, its anatomical 5 structure and relationships, the physiology of 6 The oesophagus is a muscular tube connecting its major functions and the effect that surgery 7 the to the and measuring has on them will all be considered in this 8 25–30 cm in the adult. Its primary function is as chapter. 9 a conduit for the passage of swallowed food and 4011 fluid, which it propels by antegrade peristaltic 1 contraction. It also serves to prevent the reflux Embryology 2 of gastric contents whilst allowing regurgita- 3 tion, and belching to take place. It is The embryonic development of the oesophagus 4 aided in these functions by the upper and lower like that of all major organ systems takes place 5 oesophageal sphincters sited at its proximal and between the fourth and eighth weeks of gesta- 6 distal ends. Any impairment of oesophageal tion as the three germ layers differentiate 7 function can lead to the debilitating symptoms into specific tissues. During the fourth week, as 8 of dysphagia, gastro-oesophageal reflux or the embryo folds, part of the dorsal yolk sac is 9 oesophageal pain. incorporated into the developing head as the 5011 The apparently simple basic structure of foregut (Figure 1.1a). This ultimately develops 1 the oesophagus belies both its physiological into not only the oesophagus, stomach and duo- 2 importance and the dangers associated with denum but also the pharynx, lower respiratory 311 surgical intervention. As a consequence of its system, liver, pancreas and biliary tree.

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Early in the fourth week the laryngotracheal tracheo-oesophageal fistula, which is commonly 1111 diverticulum develops in the midline of the associated with oesophageal atresia. Complete 2 ventral wall of the foregut. This extends caudally failure to close the tracheo-oesophageal septum 3 and becomes separated from the foregut by is much less common and results in a laryngo- 4 growth of the tracheo-oesophageal folds, which oesophageal cleft. Normally the oesophagus 5 fuse to form the tracheo-oesophageal septum lengthens rapidly as a result of cranial body 6 (Figure 1.1b and c). This creates the laryngotra- growth (with descent of the heart and lungs) to 7 cheal tube (ultimately the larynx, trachea, reach its final relative length by the seventh 8 bronchi and lungs) and dorsally the oesophagus week. During elongation the lumen is tem- 9 [2]. Failure of this separation can occur due to porarily obliterated by proliferation of endo- 1011 a shortage of proliferating endothelial cells in dermal cells and failure to recanalise results in 1 the tracheo-oesophageal folds. This results in a oesophageal atresia. 2 Oesophageal atresia is present in approxi- 3 mately 1 in 3000 live births. In 85% of cases 4 a Aorta there is proximal oesophageal atresia with a 5 Coeliac axis Midgut fistula between the distal oesophagus and the 6 Hindgut respiratory tract, usually the trachea. Less 7 common combinations are oesophageal atresia 8 without a fistula (10%), a fistula without atresia 9 (2%) and a fistula between the upper oesopha- 2011 gus and trachea (1%). Because of the embryonic 1 time period during which these failures take 2 place 50% of oesophageal malformations are 3 associated with major defects in other organ 4 Brain systems. In 25% these are cardiovascular, 5 Heart most commonly a patent ductus arteriosus, 6 Foregut although musculoskeletal and other gastroin- 7 Laryngotracheal diverticulum testinal defects, classically an imperforate anus, 8 are also seen. 9 The artery of the foregut is the coeliac axis 3011 (i) (ii) and whilst this supplies the distal oesophagus, 1 Pharynx more proximally it takes branches directly from 2 Oesophagus the developing aorta. During the developmental 3 b sequence described, the epithelium and glands 4 of the oesophagus are derived from endoderm. 5 The striated skeletal muscle of the proximal 6 third of the oesophagus is derived from mes- 7 Laryngotracheal Bronchial diverticulum buds enchyme in the caudal branchial arches whilst 8 the smooth muscle of the more distal oesopha- 9 gus develops from surrounding splanchnic mes- 4011 (i) Tracheo-oesophegeal (i) Traceo-oesophageal enchyme. Even in the fetus the oesophagus is of 1 fold septum vital functional importance, allowing swallowed 2 amniotic fluid to pass to the intestines for 3 absorption and placental transfer to maternal 4 blood. 5 Splenclinic 6 mesenchyme Oesophagus 7 c Laryngotracheal tube 8 Adult Oesophageal 9 Figure 1.1. a–c The embryological development of the Anatomy 5011 oesophagus. a Sagittal section of a 4-week-old embryo. 1 b–c The development of the tracheo-oesophageal septum and The oesophagus is a muscular tube protected at 2 separation of the oesophagus and laryngotracheal tube. its ends by the upper and lower oesophageal 311

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111 sphincters. It commences as a continuation of Cervical Oesophagus 2 the pharynx at the lower border of the cricopha- 3 ryngeus muscle, at the level of the sixth cervical This begins at the lower border of the cricoid 4 vertebra (C6). The surface marking for this cartilage (C6) and ends at the level of the tho- 5 point is the lower border of the cricoid cartilage. racic inlet or jugular notch (T1). It lies between 6 It enters the chest at the level of the supraster- the trachea anteriorly and the prevertebral layer 7 nal notch and descends through the superior of cervical fascia posteriorly, deviating slightly 8 and posterior mediastinum along the front to the left at the level of the thyroid gland before 9 of the vertebral column. It passes though the returning to enter the thorax in the midline 1011 oesophageal hiatus in the diaphragm at the (Figure 1.3). The recurrent laryngeal run 1 level of the tenth thoracic vertebra to end at in a caudal direction either side of the oesoph- 2 the gastro-oesophageal junction. The surface agus in the tracheo-oesophageal groove. They 3 marking for this point is the left seventh costal innervate the laryngeal muscles and surgical 4 cartilage. The oesophagus measures 25–30 cm trauma to the at this point results in an 5 in length although this varies according to the ipsilateral vocal cord palsy. More laterally lie the 6 height of the individual and in particular the lobes of the thyroid gland with the inferior 7 suprasternal–xiphoid distance. thyroid artery and the carotid sheath contain- 8 ing the carotid vessels and the vagus nerve. 9 Anatomical Relationships of the Thoracic Oesophagus 2011 Oesophagus 1 The upper thoracic oesophagus extends the 2 The oesophagus can be artificially divided from length of the superior mediastinum between 3 proximal to distal into cervical, thoracic and the thoracic inlet and the level of the carina (T5). 4 abdominal segments [3] (Figure 1.2). The middle and lower thoracic oesophagus lies 5 6 7 8 9 3011 Cervical oesophagus 1 Trachea 2 3 Upper thoracic oesophagus 4 Azygos vein 5 Aorta 6 7 Middle thoracic oesophagus 8 Pulmonary artery 9 4011 Oesophagus 1 2 3 4 Lower thoracic 5 oesophagus Lower 6 Oesophagus 7 Diaphragm 8 9 Abdominal oesophagus 5011 1 2 311 Figure 1.2. The divisions and anatomical relations of the oesophagus.

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R L 1111 Thyroid 2 3 Trachea 4 Recurrent laryngeal nerve ⎧ 5 ⎨ Comon carotid artery 6 Carotid sheath Interior jugular vein 7 ⎩ Vagus nerve 8 Oesophagus 9 1011 Figure 1.3. Cross-section of the oesophagus in the lower . 1 2 3 in the posterior mediastinum subdivided by the mediastinum. It is here that the duct or its 4 midpoint between the tracheal bifurcation and radicals may be inadvertently damaged during 5 the oesophagogastric junction (Figure 1.2). mobilisation of the oesophagus, resulting in a 6 In the superior mediastinum the upper thor- chylothorax [4]. The duct then ascends, passing 7 acic oesophagus maintains close contact with behind the oesophagus to lie on its left side in 8 the left mediastinal pleura and posteriorly with the superior mediastinum. The oesophagus ini- 9 the prevertebral fascia. At this level the oesoph- tially lies to the right of the descending aorta but 2011 agus is indented by the arch of the aorta on its crosses it during its descent to lie anterior and 1 left side and crossed by the azygos vein on on its left side as it approaches the diaphragm. 2 its right side. As it descends into the posterior 3 mediastinum it is also crossed anteriorly and Abdominal Oesophagus 4 indented by the left main bronchus and crossed 5 by the right pulmonary artery (Figure 1.2). The lower oesophagus comprises the lower tho- 6 Below this level the pericardium and left atrium racic, oesophagus together with the short intra- 7 lie anterior to the oesophagus. abdominal portion of oesophagus (Figure 1.2). 8 The middle thoracic oesophagus deviates to The oesophageal opening in the diaphragm 9 the right, coming into close apposition with the lies within fibres of the left crus inside a sling 3011 right mediastinal pleura, which covers its right of fibres passing across from the right crus. At 1 side and posterior aspect. It also moves forward this point the vagal trunks lie on the anterior 2 with a concavity more marked than the verte- and posterior surface of the oesophagus 3 bral column, allowing the azygos vein, the tho- having emerged from the oesophageal plexuses 4 racic duct, the right upper five intercostal on its lower surface. The oesophageal branches 5 arteries and the descending aorta to all pass of the left gastric artery with associated veins 6 posteriorly during its course. and lymphatics also accompany the oesoph- 7 The azygos vein originates in the upper agus. The intra-abdominal portion of the 8 abdomen and enters the mediastinum via the oesophagus extends from the diaphragm to 9 aortic opening in the diaphragm. It ascends the gastro-oesophageal junction. It is covered 4011 along the right posterolateral aspect of the by peritoneum (the gastrophrenic ligament) 1 oesophagus before arching over the root of and lies posterior to the left lobe of the liver. 2 the right lung to enter the superior vena cava It is usually 1–2 cm in length although even 3 (Figure 1.2). Resection of this arch allows in the normal individual this varies according 4 improved surgical access to the oesophagus via to the muscle tone, degree of gastric distension 5 the right chest. The thoracic duct originates in and respiration. 6 the cisterna chyli anterior to the second lumbar Although essentially a midline structure, 7 vertebra and passes through the diaphragmatic these deviations of the oesophagus to the left in 8 hiatus on the right side of the aorta posterior to the neck, to the right in the posterior medi- 9 the right crus. It provides lymphatic drainage astinum and left and anteriorly towards the 5011 for the lower body and the left half of the upper diaphragmatic hiatus have important clinical 1 body. The duct lies on the right lateral aspect of consequences. This course must be considered 2 the descending thoracic aorta in the inferior carefully when the surgical approach to the 311

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111 oesophagus is determined. For optimum expo- and laterally but the posterior aspect is strong 2 sure the cervical oesophagus should be and serves to maintain the intra-abdominal 3 approached from the left side of the neck, the position of the gastro-oesophageal junction and 4 thoracic oesophagus from the right side of lower oesophageal sphincter. Weakening of 5 the thorax and the lower oesophagus and the the phreno-oesophageal ligament allows the 6 gastro-oesophageal junction from the abdomen oesophagus to rise, resulting in a sliding type of 7 or by a left thoraco-abdominal approach [5]. hiatus hernia. The ligament also maintains 8 the angle between the distal oesophagus and the 9 Endoscopic Anatomy proximal stomach (the ), allowing a 1011 mucosal fold of the greater curve aspect of the 1 These relations are also important when we con- gastro-oesophageal junction to close against 2 sider the endoscopic anatomy of the oesopha- the lesser curvature. The flap valve created may 3 gus. By consensus endoscopic landmarks are have a role in the antireflux mechanism of the 4 identified by their distance in centimetres from gastro-oesophageal junction. 5 the incisor teeth, measured with the flexible 6 video-endoscope. The narrowest point of the Structure of the Oesophagus 7 oesophagus is its commencement at the level of 8 cricopharyngeus (upper oesophageal sphinc- Upper Oesophageal Sphincter (UOS) 9 ter), 15 cm from the incisors. Further indenta- This creates a zone of high pressure between the 2011 tions are caused by the aortic arch at 22 cm, the pharynx and the proximal oesophagus, which 1 left main bronchus at 27 cm and the diaphragm relaxes during swallowing and prevents 2 at 38 cm. All distances vary according to the aerophagia during respiration. At this level hor- 3 height of the individual. An enlarged left atrium izontal fibres of the cricopharyngeus muscle 4 may also indent the anterior aspect of the lower pass posteriorly from the cricoid bone to join 5 oesophagus. the inferior pharyngeal constrictor and create a 6 The gastro-oesophageal junction is defined continuous muscular band. Posteriorly just 7 endoscopically as the upper margin of the prox- proximal to cricopharyngeus there is a relative 8 imal . On average this is at 37 cm in weakness, Killian’s triangle, that is the origin of 9 females and 40 cm in males although it migrates a pharyngeal pouch. 3011 proximally in the case of a sliding hiatus hernia. 1 The squamocolumnar junction is also visible Body of the Oesophagus 2 endoscopically as the Z-line and usually coin- 3 cides with the gastro-oesophageal junction, Histologically this is made up of four layers: 4 although it may be more proximal in the pres- , muscle, and mucosa 5 ence of Barrett’s oesophagus where there is (Figure 1.4). In the mediastinum the oesopha- 6 columnarisation of the lower oesophagus [6]. gus has no serosal covering and the dense con- 7 nective tissue of the adventitia forms its outer 8 Attachments of the Oesophagus layer. The is composed of an 9 outer longitudinal and an inner circular layer. 4011 The oesophagus is held in loose areolar tissue in Proximally, the longitudinal fibres originate 1 the mediastinum, allowing sizable vertical from the dorsal aspect of the cricoid and the 2 movement during respiration. Within this are cricopharyngeus tendon to descend in a gentle 3 slips of smooth muscle fibres tethering it to spiral. These longitudinal muscle fibres split 4 neighbouring structures, notably the trachea, above the gastro-oesophageal junction creating 5 left bronchus, pericardium and aorta. The a potential vertical weakness on the left pos- 6 major oesophageal attachment, however, is dor- terolateral aspect. This is the most common site 7 sally, the phreno-oesophageal ligament. This of a tear in the case of spontaneous rupture of 8 condensation of connective tissue is an exten- the oesophagus (Boerhaave’s syndrome). The 9 sion of the diaphragmatic and thoracic fascia. circular muscle layer is continuous proximally 5011 Its upper and lower limbs tether the lower few with the inferior constrictor and the muscle 1 centimetres of the thoracic oesophagus and the fibre arrangement is elliptical in nature. This is 2 gastro-oesophageal junction to the aorta and designed for , to propel food to the 311 the diaphragmatic hiatus. It is weak anteriorly stomach and clear refluxed gastric contents

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1111 2 3 4 Circular muscle 5 6 Longitidinal muscle 7 8 9 Adventitia 1011 1 2 3 4 5 Submucosa 6 7 8 Submucosal gland 9 2011 1 2 3 4 5 6 ⎧ 7 Stratified squcmous epithelium⎨ Mucosa 8 ⎩ 9 3011 Figure 1.4. Histological cross-section of the oesophageal wall. 1 2 3 from the oesophagus. The proximal 4–6 cm of The oesophageal mucosa is a non-keratinised 4 both layers of oesophageal muscle is striated. stratified squamous epithelium with a base- 5 There is a mixture of striated and smooth ment membrane separating it from the under- 6 muscle below this to around 10–13 cm and the lying lamina propria and muscularis mucosa 7 lower half to one-third of the oesophagus con- (Figure 1.4). This changes close to the gastro- 8 tains only smooth muscle [7]. oesophageal junction to a columnar-lined 9 The submucosal layer consists of elastin gastric epithelium at the squamocolumnar 4011 fibres within a loose connective tissue and junction. In Barrett’s oesophagus columnar 1 allows distension of the oesophagus during metaplasia of the lower oesophagus occurs as a 2 swallowing. The absence of a serosal layer response to chronic acid and reflux charac- 3 makes oesophageal anastomosis technically terised histologically by intestinal metaplasia 4 difficult and reliant upon the strength of the and the presence of goblet cells [8]. 5 submucosa. It transmits abundant lymphatic 6 channels, blood vessels, and the submucosal Lower Oesophageal Sphincter (LOS) 7 . It also contains oesophageal 8 glands, which open into the lumen via a long Although there is a functional high-pressure 9 single duct. These secrete for bolus lubri- zone in the lower oesophagus, the presence of 5011 cation, bicarbonate ions to neutralise refluxed an anatomical sphincter has been disputed. 1 acid and growth factors that help to maintain There is, however, an increase in the circular 2 the integrity of the oesophageal epithelium. muscle layer at this level and ultrastructural 311

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111 studies have demonstrated morphological alter- 2 ations in the muscle cells of this area. 102 101 Inferior thyroid artery 3 100 4 Blood Supply and Lymphatic 103 5 106 6 Drainage of the Oesophagus 7 105 Trachea 8 Arterial Supply 107 109 9 The oesophagus receives a segmental blood 1011 supply with extensive collaterals along its Direct gortic branches 1 Oesophagus course (Figure 1.5). In the neck and superior 108 2 mediastinum it is primarily supplied by vessels 3 from the inferior thyroid artery, a branch of Left gastric artery 4 the subclavian artery. Rarely these may be 10 112 5 supported by smaller vessels directly from the 6 common carotid, vertebral or subclavian arter- 7 ies. In the posterior mediastinum the oesopha- 1 2 8 gus receives direct aortic branches. These 9 7 9 Coeliac axis short vessels must be carefully identified during 3 11 2011 mobilisation of the oesophagus and ligated in 8 1 continuity to prevent avulsion from the aorta. 2 They anastomose with bronchial arteries that Common hepatic 3 enter the oesophagus at the tracheal bifurcation, artery 4 and small branches from the intercostal arter- 5 ies. The lower oesophagus receives its main Splenic artery 6 supply from ascending branches of the left 7 gastric artery, originating from the coeliac axis, Figure 1.5. Arterial blood supply and lymphatic drainage of the 8 aided by the left inferior phrenic artery. oesophagus. Cervical lymph nodes: 100, lateral cervical; 101, 9 Although the nutrient arteries to the oesopha- cervical para-oesophageal; 102, deep cervical; 103, supraclavic- ular. Mediastinal lymph nodes: 105, upper para-oesophageal; 3011 gus are not end arteries, this segmental supply 1 106, paratracheal; 107, carinal; 108, middle para-oesophageal; must be carefully considered during surgical 109, left and right bronchial; 110, lower para-oesophageal; 2 reconstruction of the oesophagus to prevent 3 112, posterior mediastinal. Abdominal lymph nodes: 1, right ischaemic complications. paracardial; 2, left paracardial; 3, lesser curve; 7, left gastric; 8, 4 common hepatic; 9, coeliac axis; 11, splenic artery. 5 Venous Drainage 6 7 This commences along the length of the varices are important clinically as a major cause 8 oesophagus with the submucosal venous plexus, of massive upper gastrointestinal haemorrhage. 9 which drains into an extrinsic plexus on the The direct communication with both the sys- 4011 oesophageal surface. As with the arterial supply, temic and portal systems may also be important 1 the precise venous drainage is variable. From in the metastatic dissemination of oesophageal 2 the upper oesophagus it is via the inferior carcinoma. 3 thyroid veins to the brachiocephalic vein and in 4 the mediastinum it is via the azygos and hemi- Lymphatic Drainage 5 azygos systems that ultimately drain into the 6 superior vena cava. However, from the lower The lymphatic pathways draining the oesopha- 7 oesophagus it is via tributaries of the left gastric gus are complex and the presence of lymphat- 8 vein, which empties into the portal vein creat- ics within the mucosa makes it unique within 9 ing a portosystemic anastomosis in the lower the . These and extensive 5011 oesophagus. In the presence of portal venous submucosal lymphatics form a complex inter- 1 hypertension raised pressure is transmitted to connecting network extending the length of the 2 the of the lower oesophagus, oesophagus, intermittently piercing the muscu- 311 creating fragile varicosities. These oesophageal lar layers to drain into the para-oesophageal

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1 · UPPER GASTROINTESTINAL SURGERY plexus. The para-oesophageal nodes lie fibres originate from the vagal motor nuclei and 1111 along the oesophageal wall draining to peri- are distributed to the oesophagus via the vagus 2 oesophageal nodes and more distant lateral nerve to form the oesophageal plexus. The glos- 3 oesophageal nodes. Ultimately these empty into sopharyngeal nerve and the recurrent laryngeal 4 the thoracic duct although direct connections branches of the vagus also carry some fibres to 5 between the oesophageal plexus and the duct the proximal oesophagus. 6 may also be present. This arrangement allows 7 for early and widespread lymphatic dissemina- Sympathetic Supply 8 tion of oesophageal carcinoma once the base- 9 ment membrane has been breached. This appears to play a more minor role in 1011 Lymph node status is a profound prognostic oesophageal function. The preganglionic fibres 1 factor for oesophageal carcinoma and the originate from the fifth and sixth thoracic spinal 2 pattern of dissemination derived from resected cord segments and pass to the cervical, thoracic 3 specimens suggests that the lymphatic drainage and coeliac ganglia. The postganglionic fibres 4 broadly mirrors the arterial blood supply. The terminate in the myenteric plexus within the 5 upper oesophagus drains in a mainly cephalic oesophageal wall. 6 direction to the cervical nodes; the middle 7 oesophagus to the para-oesophageal, para- Intramural Plexuses 8 aortic and tracheo-bronchial stations; the lower The myenteric (Auerbach’s) plexus lies between 9 oesophagus to both these mediastinal stations the circular and longitudinal muscle layers and 2011 and upper abdominal stations, particularly the becomes more prominent in the smooth muscle 1 paracardial nodes and those along the left portion of the oesophagus. Degeneration of the 2 gastric artery (Figure 1.5). This direction of lym- myenteric plexus in the region of the lower 3 phatic flow has been confirmed by radionuclide oesophageal sphincter results in achalasia of the 4 studies following endoscopic injection of a cardia, a major motor disorder of the oesopha- 5 radioactive tracer at different levels of the gus, which is characterised by failure of the 6 oesophagus. According to the TNM (tumour, lower oesophageal sphincter to relax upon swal- 7 node, metastasis) classification the regional lowing. The submucosal (Meissner’s) plexus is 8 lymph nodes are, for the cervical oesophagus, more sparse, containing nerve fibres but no 9 the cervical nodes including the supraclavicular ganglia. 3011 nodes, and, for the intrathoracic oesophagus, The neural control of the oesophagus will be 1 the mediastinal and perigastric nodes, exclud- covered in greater detail when the physiological 2 ing the coeliac nodes (considered M1a nodes) control of oesophageal function is considered. 3 [3]. The precise nomenclature differs slightly 4 from the description by the Japanese Society 5 [9] (Figure 1.5) although the two systems are 6 broadly similar. Physiology of the 7 Oesophagus 8 Nerve Supply of the Oesophagus 9 4011 The innervation of the oesophagus comprises Fasting State 1 an extrinsic parasympathetic and sympathetic 2 supply and the intrinsic intramural plexuses. It In the fasting state the oesophageal body is 3 is controlled by a complex swallowing centre relaxed and the upper and lower oesophageal 4 located in the brainstem, which coordinates and sphincters are tonically contracted to prevent 5 interprets signals from within the brainstem gastro-oesophageal reflux and aspiration. The 6 and from peripheral receptors in the pharynx intraluminal pressure is atmospheric in the cer- 7 and oesophagus. vical oesophagus but more distally it becomes 8 negative and approximates with intrapleural 9 Parasympathetic Supply pressure, fluctuating with respiration (–5 to 5011 –10 mmHg on inspiration, 0 to +5 mmHg on 1 This provides the predominant motor and expiration). The short intra- abdominal portion 2 sensory innervation of the oesophagus. The of the oesophagus lies in the slightly positive 311

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111 (0 to +5 mmHg) environment of the abdominal The resting sphincter pressure prevents 2 cavity. Unlike the smooth muscle of the stomach aerophagia and the aspiration of refluxed 3 and intestine, oesophageal smooth muscle does gastric contents and is asymmetrical, being 4 not normally exhibit spontaneous phasic slow higher in an anteroposterior direction (100 5 wave activity and is therefore highly dependent mHg) than laterally (35 mmHg) [10]. This high 6 on its external and internal nerve supply. resting tone results from a combination of con- 7 tinuous myogenic activity in the cricopharyn- 8 Swallowing geus and inferior constrictor muscles together 9 with the inherent elasticity of these tissues. A 1011 During fasting the normal individual swallows vagally mediated increase in UOS pressure 1 on average 70 times/hour whilst awake and occurs secondary to oesophageal distension 2 7 times/hour during sleep, which may increase or acid exposure particularly of the proximal 3 to 200 times/hour during eating. The act of oesophagus, whilst a decrease occurs during 4 swallowing is a complex reflex involving many sleep or general anaesthesia. A swallowing- 5 muscles, which it shares with other reflex activ- initiated pressure drop occurs prior to a bolus 6 ities (retching, vomiting, belching and speech). entering the pharynx and comprises both 7 The hyoid muscles are active throughout ele- sphincter muscle relaxation due to neural inhi- 8 vating the hyoid bone, drawing it forward bition and sphincter opening secondary to 9 and then descending it through an elliptical forward displacement of the hyoid bone. Once 2011 pathway. Swallowing consists of an oropharyn- a bolus has passed into the oesophagus the UOS 1 geal phase, which is partly voluntary, and an exhibits rebound hypertension to coincide with 2 involuntary oesophageal phase. It may be initi- the initiation of oesophageal peristalsis and 3 ated either voluntarily or as a reflex following prevent reflux back into the pharynx. 4 stimulation of oropharyngeal receptors or the 5 oesophagus itself. Oesophageal Phase 6 Oropharyngeal Phase This is characterised by coordinated muscular 7 contractions that propel a bolus through the 8 During the oral stage ingested food is broken oesophagus, and relaxation of the lower 9 down and lubricated with saliva by mastication oesophageal sphincter allowing it to pass into 3011 before being pushed into the posterior orophar- the stomach. Peristalsis will normally com- 1 ynx by the tongue. During the pharyngeal stage pletely clear the oesophagus of a food bolus in 2 there is conversion from a respiratory to a swal- 8–10 seconds. When liquids are swallowed in 3 lowing pathway, pharyngeal filling, passive the upright position, gravity draws a bolus into 4 emptying and active pharyngeal peristalsis. the stomach within a few seconds with its 5 Involuntary expulsion and clearing of the food tail being propelled by the peristaltic wave. A 6 bolus into the pharynx takes around 0.5 seconds combination of intrinsic and extrinsic neural 7 and in anticipation of its arrival respiration is factors interacts with the myogenic properties 8 suppressed and the apertures to the nasal cavity of striated and smooth oesophageal muscle to 9 and the larynx are closed. Elevation of the hyoid produce these organised waves of contraction. 4011 bone allows the epiglottis to cover the larynx. 1 However, the most effective barrier to aspira- Primary Peristalsis 2 tion is provided by adduction of the true vocal This is the oesophageal peristaltic wave trig- 3 cords. Simultaneously there is relaxation of the gered by swallowing. It commences in the 4 upper oesophageal sphincter allowing most proximal oesophagus following pharyngeal 5 pharyngeal emptying to occur before the onset peristalsis and relaxation of the UOS. The lon- 6 of pharyngeal peristalsis. Pharyngeal contrac- gitudinal muscle layer contracts first to shorten 7 tion then creates a pressure differential between and fix the oesophagus. There is then a pro- 8 the pharynx and the proximal oesophagus clear- gressive lumen-occluding circular contraction 9 ing any residual bolus. that proceeds distally through the striated and 5011 smooth muscle of the oesophageal wall, pre- 1 Upper Oesophageal Sphincter (UOS) ceded by a wave of inhibition. As it does so the 2 This provides a 2–4 cm zone of high pressure lower oesophageal sphincter (LOS) relaxes 311 between the pharynx and the upper oesophagus. and then closes after the bolus with a prolonged

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1 · UPPER GASTROINTESTINAL SURGERY contraction [11]. Normally the oesophagus related to swallowing or oesophageal disten- 1111 responds with one primary peristaltic wave for sion, do not help to propel a bolus and if present 2 each swallow. However, during rapidly repeated in a significant number may be considered 3 swallowing oesophageal activity is inhibited and pathological. 4 only the final swallow is followed by a peristaltic 5 wave. This property of deglutitive inhibition Investigation of Peristalsis 6 is vital to allow the passage of swallowed food 7 through the oesophagus. Due to its accessibility oesophageal peristalsis 8 has been extensively investigated. Manometric 9 Secondary Peristalsis techniques have been used to characterise 1011 This is localised to the oesophagus and is not the peristaltic wave and video-fluoroscopy has 1 preceded by pharyngeal contraction or UOS been used to visualise bolus movement. These 2 relaxation. It accounts for approximately 10% of techniques have demonstrated that the primary 3 all oesophageal motor activity. Secondary peri- peristaltic wave travels fastest in the mid- 4 stalsis is triggered by oesophageal distension by oesophagus, slowest immediately above the 5 residual bolus following ineffective primary LOS, and at an average velocity of 4 cm/s. The 6 peristalsis or by refluxed gastric contents [12]. muscular contraction itself lasts for 2–7 seconds 7 Both these events may also initiate swallowing- and is most prolonged in the distal oesophagus. 8 induced primary peristalsis in an attempt to The mean peak amplitude of contraction ranges 9 clear the oesophagus. from 35 to 70 mmHg along the oesophagus. It 2011 is lowest at the junction of striated and smooth 1 Tertiary Contractions muscle in the mid-oesophagus and increases 2 These are localised non-propagating contrac- progressively towards the lower oesophagus 3 tions of the oesophageal body. They are not [13] (Figure 1.6). Peristaltic amplitude below 4 5 6 Shallow 7 8 9 Upper oesophageal 50–100 3011 sphincter mm Hg 1 0 2 3 Proximal 55 mm Hg 4 oesophageal muscle 5 (striated) 0 6 7 8 Transition zone 35 mm Hg 9 4011 0 1 70 mm Hg 2 Smooth oesophageal 3 muscle 4 0 5 6 Lower oesophageal 7 sphincter 15 mm Hg 8 0 9 0 2468 5011 Time (s) 1 2 Figure 1.6. Manometric properties of the primary peristaltic wave. 311

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111 30 mmHg is considered hypotensive, as these via the inhibitory neurotransmitter nitrous 2 contractions are often associated with retro- oxide (NO). Upon swallowing there is almost 3 grade escape of a liquid bolus and incomplete simultaneous activation of the inhibitory 4 oesophageal clearance. Although there is no pathway followed by a delayed sequential acti- 5 defined upper limit, peristaltic contractions vation of the excitatory pathway. This creates a 6 greater than 200 mmHg in the distal half of wave of mechanical inhibition (latency) fol- 7 the oesophagus are usually considered hyper- lowed by contraction along the oesophagus, 8 tensive. This condition is termed ‘nutcracker constituting peristalsis [11]. The excitatory 9 oesophagus’ and is often associated with symp- cholinergic influence is more prominent proxi- 1011 toms of chest pain and dysphagia. The nature of mally whilst the inhibitory influence increases 1 the bolus itself can influence the primary peri- in the distal oesophagus. These neural gradients 2 staltic wave with larger boluses triggering a along the oesophagus cause the velocity of prop- 3 stronger contraction. Bolus temperature is also agation to decrease distally. Because cholinergic 4 important; warm boluses enhance whereas cold excitation decreases the delay to the onset of 5 boluses inhibit peristalsis. contraction the gradient also helps to coord- 6 Secondary peristalsis is stimulated by inate the aboral progression of peristalsis. 7 oesophageal distension and can be reproduced When there is adequate cholinergic excitation 8 by balloon occlusion of the lumen. Phasic, tonic a local myogenic control system also becomes 9 contractions of the circular and smooth muscle stimulated. Oesophageal muscle may then 2011 develop above the balloon whilst the oesopha- exhibit slow wave type action potentials and 1 gus relaxes below. This proximal propulsive coupling of the smooth muscle cells so that the 2 force consists of simultaneous multipeaked whole tissue becomes a functional unit. As a 3 contractions and is reflex mediated. It is consequence peristaltic progression can occur 4 strongest when the occlusion is sited in the at a myogenic level once there is adequate 5 distal oesophagus. When the obstruction is neural excitation. 6 cleared a peristaltic wave progresses distally. 7 The velocity and amplitude of secondary peri- Lower Oesophageal Sphincter 8 stalsis resemble that of primary peristalsis. 9 (LOS) 3011 Control of Peristalsis The lower oesophageal sphincter is responsible 1 for a 2–4 cm zone of high pressure at the gastro- 2 Peristalsis in the striated muscle of the proximal oesophageal junction. It creates a resting pres- 3 oesophagus is stimulated by sequential vagal sure of 10–25 mmHg that is asymmetrical, being 4 excitation directed from the brainstem, and highest distally and to the left side. In the 5 carried to the oesophagus by the recurrent absence of a hiatus hernia the sphincter has 6 laryngeal branches of the vagus. Peristalsis in both an intra-abdominal and an intrathoracic 7 oesophageal smooth muscle is more complex component. During respiration these are sub- 8 and requires integration of central and periph- jected to the different pressure changes of these 9 eral neural mechanisms with smooth muscle two cavities and are directly influenced by con- 4011 properties. Swallow-induced primary peristalsis traction of the crural diaphragm. 1 is dependent on activation of the swallowing The three major factors controlling LOS pres- 2 centre and vagal pathways and is abolished by sure are its myogenic properties and the 3 bilateral cervical vagotomy. There is also some inhibitory and excitatory neural influence [14]. 4 central control over coordinating the activity of The basal pressure is primarily a result of myo- 5 striated and smooth muscle and initiating activ- genic properties as within the muscle fibres con- 6 ity in the smooth muscle portion. tinuous electrical spike activity stimulates Ca2+ 7 The propagation of peristalsis in the smooth influx and maintains a depolarised state at rest. 8 muscle segment involves two peripheral vagal Neural activity can modulate sphincter pressure 9 pathways. One pathway mediates cholinergic and the myenteric plexus here is innervated by 5011 excitation (depolarisation) of both longitudinal both vagal preganglionic and sympathetic post- 1 and circular smooth muscle whilst the other ganglionic fibres. Nitrous oxide is the primary 2 mediates nonadrenergic non-cholinergic inhi- inhibitory and acetylcholine the primary exci- 311 bition of circular muscle (hyperpolarisation), tatory neurotransmitter. A large number of

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1 · UPPER GASTROINTESTINAL SURGERY neurotransmitters, hormones, drugs, foods and contraction whereas in the case of rumination 1111 lifestyle factors have been shown experimentally there is reverse oesophageal peristalsis. 2 to alter LOS pressure, although the physiologi- 3 cal importance of many remains to be estab- 4 lished (Table 1.1). Transient Lower Oesophageal 5 Deglutitive relaxation of the LOS occurs less Sphincter (tLOS) Relaxation 6 than 2 seconds after swallowing and is initiated 7 whilst the peristaltic contraction is in the cervi- There is now evidence that transient relaxation 8 cal oesophagus. Relaxation occurs to intragas- of the LOS is responsible for most episodes of 9 tric pressure, lasts for 8–10 seconds, and is the reflux of gastric contents, both in normal 1011 followed by an after-contraction in the proximal controls and in patients with gastro- 1 portion of the sphincter. Swallowing-stimulated oesophageal reflux disease [15]. This relaxation 2 relaxation is vagally mediated and coincides is unrelated to swallowing and is facilitated by 3 with a cessation in spike activity in the sphinc- pharyngeal stimulation and gastric distension, 4 ter muscle. During repeated swallowing the LOS particularly following fatty meals and in an 5 remains relaxed until after the final swallow. upright position. The drop in sphincter pressure 6 Failure of the LOS to relax on swallowing is occurs more slowly than with swallowing- 7 characteristic of achalasia, a major motor dis- related relaxation and is prolonged, typically 8 order of the oesophagus. It is associated with lasting for 10–60 seconds until a swallow inter- 9 degeneration of the myenteric plexus in the venes. This is frequently but not invariably asso- 2011 region of the sphincter and a decrease in nitric ciated with reflux, which occurs with 15–90% of 1 oxide synthase and consequently levels of the episodes depending upon the precise study con- 2 inhibitory neurotransmitter nitric oxide. ditions. There is often also reflux of gas and this 3 In addition to primary and secondary peri- forms part of the belch reflex. Transient relax- 4 stalsis, LOS relaxation also occurs during belch- ation of the LOS is a vagally mediated reflex and 5 ing, vomiting and rumination. In the first two as with swallowing-induced relaxation nitrous 6 reflexes it is not associated with oesophageal oxide (NO) is the efferent neurotransmitter. 7 8 9 Table 1.1. Factors causing relaxation or contraction of the lower oesophageal sphincter 3011 Factor type Decrease LOS pressure Increase LOS pressure 1 Hormones Glucagon 2 3 Progesterone Motilin 4 Oestrogens Pancreatic polypeptide 5 6 Neurotransmitters Nitrous oxide (NO) Acetylcholine 7 Vasoactive intestinal peptide (VIP) Substance P 8 Dopamine (D2) Histamine 9 4011 Prostaglandins E , E , A F 1 2 2 2 1 Drugs Calcium antagonists Metoclopramide 2 Atropine Domperidone 3 Nitrates Cisapride 4 Tricyclic antidepressants Erythromycin 5 Cholinergic drugs 6 7 Foods Fats Protein meal 8 Chocolate Red pepper 9 Caffeine 5011 Alcohol 1 Other Cigarette smoking 2 311

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111 Physiology of the Antireflux intra-abdominal pressure, also serves to prevent 2 reflux (Figure 1.7). 3 Mechanism Pressure monitoring has demonstrated a con- 4 tinuous variation in the intraluminal pressure at 5 The Oesophagogastric Junction the junction secondary to fluctuations in LOS 6 The reflux of small quantities of gastric fluid and and crural pressure. The intrinsic LOS is linked 7 air into the oesophagus particularly after meals to the activity of the 8 is considered a normal physiological event. This in the stomach, and increases prior to the 9 process is limited by a number of factors com- onset of gastric contraction preventing reflux. 1011 prising the antireflux barrier at the oesopha- Contraction of the crural diaphragm is linked 1 gogastric junction, and by the response of the to respiration, increasing by 10–20 mmHg 2 oesophageal body to clear the refluxate (Figure with tidal inspiration and up to 150 mmHg with 3 1.7). A failure of these mechanisms results in the forced inspiration. A sustained crural contrac- 4 spectrum of gastro-oesophageal reflux disease tion is also induced by any action that increases 5 (GORD). intra-abdominal pressure, preventing reflux 6 A combination of the intrinsic smooth along the pressure gradient created between the 7 muscle LOS and the extrinsic pinchcock-like stomach and oesophagus. Measurement of 8 action of the crural diaphragm form the sphinc- the end-expiratory sphincter pressure therefore 9 ter mechanism at the oesophagogastric junction reflects the activity of the intrinsic LOS alone. 2011 [16]. The crural diaphragm surrounds the prox- At this point of the respiratory cycle the pres- 1 imal half of the intrinsic LOS and contraction sure gradient between the stomach and oesoph- 2 of both contributes to the intraluminal pressure agus is only 5 mmHg and the resting intrinsic 3 at this level. Simultaneous, transient relaxa- LOS tone is sufficient to prevent reflux. 4 tion of both sphincters is responsible for the The crural diaphragm also has the ability 5 majority of reflux episodes in normal controls. to act independently of the costal diaphragm 6 Gastric sling fibres that maintain the angle of during certain activities including vomiting 7 His at the oesophagogastric junction augment when it relaxes whilst the remainder of the 8 this antireflux mechanism. Together with the diaphragm contracts. Its activity is linked to that 9 distal oesophageal mucosa this forms a flap of the intrinsic sphincter because it responds 3011 valve that is closed by a rise in intragastric to oesophageal distension, swallowing and tran- 1 pressure. The presence of an intra-abdominal sient LOS relaxation by relaxing itself. Both 2 segment of oesophagus, subject to changes in the left and right phrenic nerves supply the 3 crural diaphragm, and this relaxation probably 4 represents a vagophrenic inhibitory reflex. 5 6 ⎫ 1ry Investigation of Gastro-oesophageal 7 ⎬ Peristalsis 2ry ⎭ Reflux 8 9 Saliva oesophageal secretions Physiological reflux predominantly occurs in 4011 the upright position during the postprandial 1 period as a result of tLOS relaxation, and rarely 2 Crucial diaphragm takes place at night. It has been investigated in 3 (extrinsic sphincter) normal controls by 24-hour ambulatory pH 4 monitoring whereby a pH sensor is introduced LOS 5 Angle of His transnasally and positioned 5 cm proximal to 6 (instrinsic sphincter) the manometrically determined upper border of 7 the LOS. By convention acid reflux is defined as 8 ⎫ a pH <4; normally there are fewer than fifty Mucosal rosette 9 ⎬ Flab valve episodes of acid reflux during 24 hours and the 5011 Gostric sling fibres⎭ total time pH <4 is less than 4% of the study 1 period [17]. This technique has demonstrated 2 Figure 1.7. Mechanisms for the prevention and clearance of that the majority of reflux episodes are asymp- 311 gastro-oesophageal reflux. tomatic. However, it only measures acid reflux

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1 · UPPER GASTROINTESTINAL SURGERY and not non-acid or gaseous reflux. More to destroy the normal antireflux mechanism by 1111 recently it has become possible to measure disrupting the crural diaphragm and flap valve 2 ambulatory bilirubin levels in the distal oesoph- at the oesophagogastric junction. In addition, 3 agus as a marker of bile reflux, although normal upon swallowing gastric contents within the 4 values for this procedure are less well estab- hernia are able to reflux through the relaxed 5 lished. Techniques such as oesophageal imped- LOS and on inspiration they are propelled 6 ance testing are currently being developed to upwards by contraction of the crural diaphragm 7 assess non-acid and gaseous reflex in greater below. 8 detail. 9 Oesophageal Sensation 1011 Oesophageal Response to Reflux 1 When physiological reflux does occur there are Mechanoreceptors within the myenteric ganglia 2 a number of responses that help to clear the both activate subconscious reflexes and trans- 3 oesophagus of refluxate and prevent mucosal duce painful sensations. Progressive balloon 4 damage. Refluxed gas is either returned to the distension of the oesophagus initially stimulates 5 stomach by peristalsis stimulated by oesopha- secondary peristalsis but at higher volumes 6 geal distension or vented to the pharynx as a causes a pressure and then a painful sensation. 7 belch. The primary response of the oesophageal Involuntary physiological reflexes such as peri- 8 body to reflux is peristalsis [12]. One or two stalsis are mediated by low threshold receptors 9 peristaltic waves will clear 90% of the reflux via vagal pathways. Nociception is mediated 2011 volume and deliver swallowed saliva to deal by higher threshold receptors and involves 1 with the remaining 10%. The initial response to splanchnic sympathetic pathways under vagal 2 acid reflux is swallowing-associated primary modulation. There are also intraepithelial nerve 3 peristalsis in 45–60% of cases. Secondary peri- endings in the oesophagus that act as thermo-, 4 stalsis is less common although it becomes the chemo- and osmoreceptors. 5 initial response in 90% of episodes during sleep 6 when swallowing and saliva production is sup- 7 pressed. Following peristalsis any residual acid Summary 8 refluxate lining the mucosa is neutralised by 9 bicarbonate ions in saliva and secretions from A clear understanding of the normal anatomy 3011 the oesophageal submucosal glands. and physiology of the oesophagus is fundamen- 1 tal to comprehending the rationale behind sur- 2 Physiology of Gastro-oesophageal gical and medical decision-making in what is a 3 complex specialty. The anatomical relationships 4 Reflux Disease of the oesophagus together with its blood supply 5 Any failure of the protective antireflux mecha- and lymphatic drainage determine the surgical 6 nism can result in gastro-oesophageal reflux approach and extent of resection required for 7 disease (GORD). It appears that most patients oesophageal malignancy and the technique to 8 with mild/moderate reflux disease exhibit be used for reconstruction. The primary func- 9 normal sphincter pressures and that as with tion of the oesophagus is as a conduit for 4011 physiological reflux it results from transient passage of swallowed food and fluid and its 1 relaxation of the sphincters [15]. Some patients structure is integrally linked to this. Our knowl- 2 do have a hypotonic intrinsic sphincter and this edge of the control of swallowing and physiol- 3 correlates with increased acid exposure and ogy of the antireflux barrier continues to evolve. 4 severity of disease. Fifty per cent of patients This has led to a better understanding of the 5 demonstrate impaired peristaltic clearance pathophysiology of oesophageal motility disor- 6 resulting in prolonged reflux episodes although ders and gastro-oesophageal reflux disease and 7 it is unclear whether this represents a primary to the development of pharmacological and 8 motor disorder or is secondary to acid-induced surgical options for their management. 9 damage. The presence of a hiatus hernia helps 5011 1 2 311

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111 the oesophagus. Part 1. Clinical classification. Jpn J Surg 2 Questions 1976; 6:64–78. 10. Sivarao D, Goyal R. Functional anatomy and physiology 3 of the upperr esophageal sphincter. Am J Med 2000; 4 1. Explain the development of tracheo- 108:27S–37S. 5 oesophageal fistula. 11. Diamant N. Neuromuscular mechanisms of primary peristalsis. Am J Med 1997; 103:40S–43S. 6 2. What are the immediate anatomical 7 12. Holloway R. Esophageal body motor response to reflux relationships of the oesophagus in the events: Secondary peristalsis. Am J Med 2000; 108: 8 posterior mediastinum? 20S–26S. 9 3. Which neural pathways control the 13. Richter J. Esophageal manometry in 95 healthy adult 1011 volunteers. Variability of pressures with age and fre- propagation of peristalsis? 1 quency of “abnormal” contractions. Dig Dis Sci 1987; 2 4. Which factors cause a decrease in lower 32:583. oesophageal sphincter pressure? 14. Goyal R, Sivarao D. Functional anatomy and physiology 3 of swallowing and esophageal motility. In: Castell D, 4 5. What is the response of the oesophageal Richter J, (eds) The , Philadelphia: Lippincott 5 body to physiological reflux of gastric Williams & Wilkins, 1999; 1–32. 6 contents? 15. Mittal R, Holloway RH, Penagini R et al. Transient lower 7 esophageal sphincter relaxation. Gastroenterology, 6. What constitutes the antireflux mecha- 1995. 109:601–10. 8 nism at the gastro-oesophageal junction? 16. Mittal, R, Balaban DH. The esophagogastric junction. N 9 7. What functional differences are there Engl J Med 1997; 336:924–32. 2011 between the virgin oesophagus and the 17. Demeester T, Johnson LF, Joseph GJ et al. Patterns of 1 gastroesophageal reflux in health and disease. Ann Surg transposed gastric conduit following 1976; 184:459–69. 2 oesophagectomy and gastric pull-up? 18. Walsh TN, Caldwell MTP, Fallon C et al. Gastric 3 motility following oesophagectomy. Br J Surg 1995; 4 82:91–4. 5 References 19. Johansson J, Sloth M, Bajc M, Walther B. Radioisotope 6 evaluation of the esophageal remnant and the gastric conduit after gastric pull-up esophagectomy. Surgery 7 1. Muller JM, Erasmit T, Stelsner M et al. Surgical therapy 1999; 125:297–303. 8 of oesophageal carcinoma. Br J Surg 1990; 77: 845–57. 20. Gutschow C, Collard JM, Romagnoli R et al. Denervated 9 2. Moore K. Essentials of human embryology. Oxford: stomach as an esophageal substitute recovers intralu- 3011 Blackwell Scientific Publications, 1988. minal acidity with time. Ann Surg 2001; 233:509–514. 1 3. Sobin L, C Wittekind, UICC TNM classification of malig- 21. Demeester T, Johansson KE, Franze I et al. Indications, nant tumours, 5th edn. New York: Wiley-Liss, 1997. surgical technique and long-term functional results of 2 4. Orringer M, Bluett M, Deeb G. Aggressive treatment of colon interposition or bypass. Ann Surg 1988:460–74. 3 chylothorax complicating transhiatal esophagectomy 22. Mathew G, Watson DI, Myerrs JC et al. Oesophageal 4 without thoracotomy. Surgery 1988; 10:720–6. motility before and after laparoscopic Nissen fundopli- 5 5. Akiyama H. Surgery for cancer of the esophagus, 1st cation. Br J Surg 1997; 84:1465–9. edn. Baltimore: Williams & Wilkins, 1990. 6 6. Sampliner R. Practice guidelines on the diagnosis, sur- 7 veillance, and therapy of Barrett’s esophagus. The 8 Practice Parameters Committee of the American College Further Reading 9 of Gastroenterology. Am J Gastroenterol 1998; 93: 4011 1028–32. Akiyama H. Surgery for cancer of the esophagus. Baltimore: 7. Meyer G. Muscle anatomy of the human esophagus. J Williams & Wilkins, 1990. 1 Clin Gastroenterol 1986; 8:131. Castell D Richter J (eds). The esophagus, Philadelphia: 2 8. Demeester S, Demeester T. Columnar mucosa and Lippincott Williams & Wilkins, 1999. 3 intestinal metaplasia of the esophagus: Fifty years of Griffin, SM, Raimes, SA. (eds) Upper gastrointestinal 4 controversy. Ann Surg 2000; 231:303–21. surgery, 2nd edn. London: WB Saunders, 2001. 9. Japanese Society for Esophageal Diseases. Guidelines Hennessy TPJ, Cuschieri A. Surgery of the Oesophagus, 2nd 5 for the clinical and pathological studies on carcioma of edn. Oxford: Butterworth Heinemann, 1992. 6 7 8 9 5011 1 2 311

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