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Original article Esophageal body length, lower esophageal sphincter length, position and pressure in health and disease R. E. K. Marshall, A. Anggiansah, C. L. Anggiansah, W. A. Owen, W. J. Owen Department of Surgery, Guy’s Hospital, St Thomas’ Street, London SE1 9RT, UK SUMMARY. We compared esophageal dimensions in control subjects and patients with diering motility disorders and severities of reflux disease. Patients (1108) and healthy controls (36) underwent manometry and 24-h pH monitoring. Subjects were grouped according to pH and manometry data into seven groups. Mean (s.e.m.) esophageal body length is greatest in achalasia [22.41 (0.27) cm] and least in reflux disease [20.06 (0.13) cm, p < 0.05]. Lower esophageal sphincter (LES) pressure is greatest in achalasia [17.46 (1.06) mmHg] and least in reflux disease [6.57 (0.24) mmHg, p < 0.05]. LES length is least in achalasia patients and control subjects. The ratio of intra-abdominal to intrathoracic LES is greatest in achalasia (1.29), no reflux and normal motility group, and controls and least in reflux disease (1.04, p < 0.05). In conclusion, esophageal body length is greatest in achalasia and least in reflux disease. This is associated with caudal movement of the LES in achalasia and cranial movement of the LES in reflux disease, relative to the diaphragm. INTRODUCTION The classical descriptions of esophageal anatomy in textbooks state that the esophagus is 10 inches or 25 cm long. 1–4 However, these dimensions are based on cadaveric measurements which may be influenced by post-mortem changes. Several methods of in vivo measurement have been described: the level of change of gastroesophageal electrical mucosal potential, 5 external chest measurement, 6 radiological measure- ment of landmarks on barium swallow 7 and endo- scopic measurement. 8–10 These methods all have their drawbacks, either because the method is indirect, 6 aected by the magnifying eect of radiographs, 7 or dependent upon the identification of often poorly recognizable anatomical landmarks which are subject to interobserver variation. 8–10 In addition, the small changes in esophageal length resulting from dierent diseases may not be picked up by these relatively insensitive techniques. Esophageal manometry, using either a water- perfused 11,12 or solid-state 13,14 system, is now accepted as the most sensitive and reliable method for measuring esophageal length. Several studies have also measured lower esophageal sphincter (LES) length 15–17 and position. 8,15,17 However, individual studies have tended to confine themselves to esopha- geal measurements either in various grades of reflux disease 8,15–18 or in achalasia. 12 The conclusions drawn from studies investigating a mixture of both have been limited by small patient numbers. 11,13 The aim of this study was to determine esophageal body length, LES length, position and pressure in both reflux disease and motility disorders in a large number of patients, and to compare these measure- ments with healthy controls. PATIENTS AND METHODS Patients Data from 1108 consecutive adult patient and 36 healthy controls were studied. All patients had been referred to the Esophageal Laboratory at Guy’s Hospital for further investigation of esophageal symptoms. None had undergone previous gastric or esophageal surgery. Proton pump inhibitors were stopped at least 7 days beforehand, H 2 -receptor and antagonists and prokinetic agents at least 48 h beforehand. Healthy controls were sought from among medical sta and patients. Exclusion criteria were prior upper gastrointestinal surgery, prior or current upper gastrointestinal or respiratory disease or symptoms, prior or current use of medications Address correspondence to: Mr R. E. K. Marshall, Department of Surgery, Guy’s Hospital, London SE1 9RT, UK. Tel: (+44) 171 955 4053; Fax: (+44) 171 403 0212. 297 Diseases of the Esophagus (1999) 12, 297–302 Ó 1999 ISDE/Blackwell Science Asia

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Original article

Esophageal body length, lower esophageal sphincter length, positionand pressure in health and disease

R. E. K. Marshall, A. Anggiansah, C. L. Anggiansah, W. A. Owen, W. J. Owen

Department of Surgery, Guy's Hospital, St Thomas' Street, London SE1 9RT, UK

SUMMARY.We compared esophageal dimensions in control subjects and patients with di�ering motility disordersand severities of re¯ux disease. Patients (1108) and healthy controls (36) underwent manometry and 24-h pHmonitoring. Subjects were grouped according to pH and manometry data into seven groups. Mean (s.e.m.)esophageal body length is greatest in achalasia [22.41 (0.27) cm] and least in re¯ux disease [20.06 (0.13) cm,p < 0.05]. Lower esophageal sphincter (LES) pressure is greatest in achalasia [17.46 (1.06) mmHg] and least inre¯ux disease [6.57 (0.24) mmHg, p < 0.05]. LES length is least in achalasia patients and control subjects. Theratio of intra-abdominal to intrathoracic LES is greatest in achalasia (1.29), no re¯ux and normal motility group,and controls and least in re¯ux disease (1.04, p < 0.05). In conclusion, esophageal body length is greatest inachalasia and least in re¯ux disease. This is associated with caudal movement of the LES in achalasia and cranialmovement of the LES in re¯ux disease, relative to the diaphragm.

INTRODUCTION

The classical descriptions of esophageal anatomy intextbooks state that the esophagus is 10 inches or25 cm long.1±4 However, these dimensions are basedon cadaveric measurements which may be in¯uencedby post-mortem changes. Several methods of in vivomeasurement have been described: the level of changeof gastroesophageal electrical mucosal potential,5

external chest measurement,6 radiological measure-ment of landmarks on barium swallow7 and endo-scopic measurement.8±10 These methods all have theirdrawbacks, either because the method is indirect,6

a�ected by the magnifying e�ect of radiographs,7 ordependent upon the identi®cation of often poorlyrecognizable anatomical landmarks which are subjectto interobserver variation.8±10 In addition, the smallchanges in esophageal length resulting from di�erentdiseases may not be picked up by these relativelyinsensitive techniques.

Esophageal manometry, using either a water-perfused11,12 or solid-state13,14 system, is now acceptedas the most sensitive and reliable method formeasuring esophageal length. Several studies havealso measured lower esophageal sphincter (LES)

length15±17 and position.8,15,17 However, individualstudies have tended to con®ne themselves to esopha-geal measurements either in various grades of re¯uxdisease8,15±18 or in achalasia.12 The conclusionsdrawn from studies investigating a mixture of bothhave been limited by small patient numbers.11,13 Theaim of this study was to determine esophageal bodylength, LES length, position and pressure in bothre¯ux disease and motility disorders in a largenumber of patients, and to compare these measure-ments with healthy controls.

PATIENTS AND METHODS

Patients

Data from 1108 consecutive adult patient and 36healthy controls were studied. All patients had beenreferred to the Esophageal Laboratory at Guy'sHospital for further investigation of esophagealsymptoms. None had undergone previous gastric oresophageal surgery. Proton pump inhibitors werestopped at least 7 days beforehand, H2-receptorand antagonists and prokinetic agents at least 48 hbeforehand. Healthy controls were sought fromamong medical sta� and patients. Exclusion criteriawere prior upper gastrointestinal surgery, prior orcurrent upper gastrointestinal or respiratory diseaseor symptoms, prior or current use of medications

Address correspondence to: Mr R. E. K. Marshall,Department of Surgery, Guy's Hospital, London SE1 9RT, UK.Tel: (+44) 171 955 4053; Fax: (+44) 171 403 0212.

297

Diseases of the Esophagus (1999) 12, 297±302Ó 1999 ISDE/Blackwell Science Asia

which might a�ect gastric acidity or motility, andfailure to consent. The study was approved by theHospital Ethical Committee, and all subjects gaveinformed consent. All subjects underwent staticmanometry followed by 24-h ambulatory pH mon-itoring.

Static manometry

Station-pull-through manometry was carried outusing a 2.5-mm-diameter microtransducer-type cath-eter (Gaeltec Ltd, Isle of Skye, UK). This consists ofsix solid-state pressure sensors mounted at 5-cmintervals. The distal four sensors are radially orientedat 90°. After the administration of topical anesthesiato the nasal mucosa (Xylocaine, Astra, King'sLangley, UK), the catheter is introduced transna-sally until the distal four sensors are in the stomach(noted by a pressure increase on inspiration). Allmeasurements are taken from the external nares.The catheter is withdrawn 1 cm at a time. For eachof the four distal pressure sensors, the following arenoted: the position of the distal border of the LES(where the pressure exceeds the gastric baselinepressure by 2 mmHg or more), the pressure inver-sion point (PIP, when the positive pressure de¯ec-tions of inspiration become negative), the upperborder of the LES (where the pressure drops tointrathoracic baseline pressure), and the LES pres-sure (LESP). For each of these parameters, theaverage of the four values is calculated. Followingthis, 10 wet swallows (each of 5 ml of water) aregiven with the distal sensor 1 cm above the upperborder of the LES to determine the characteristics ofesophageal body motility. The position of the upperesophageal sphincter (UES) is then determined,using 1-cm pull-throughs. The lower border of theUES is the point at which the intrathoracic pressureis exceeded by 5 mmHg, and the upper border of theUES that point at which the pressure drops toatmospheric pressure. In addition, the presence orabsence of coordinated cricopharyngeal activity isnoted. All manometry studies were carried out bythe same investigator (A.A.).

24-h pH monitoring

Ambulatory 24-h pH monitoring was performed witha single antimony pH sensor (Synectics, Stockholm,Sweden) placed 5 cm above the upper border of theLES. Subjects were given a list of acid foods to avoid.Before insertion and after removal the following day,the sensor was calibrated in bu�er solutions of pH 7and pH 1 (Synectics, Stockholm, Sweden). The datawere downloaded in a computer and analyzed usingcommercially available software (ESOPHOGRAM, Gas-trosoft, USA).

De®nitions

Acid re¯ux was de®ned as occurring when theesophageal pH fell below pH 4.19 Pathological acidre¯ux was de®ned as a DeMeester score greater than14.7 (based on the 95th percentile of healthy subjectsstudied in this laboratory).

Esophageal body motility was determined by theresponse to the 10 wet swallows. Achalasia wasde®ned as incomplete relaxation of the (often highpressure) LES, associated with loss of peristalsis andlow-pressure simultaneous contractions.20 Di�useesophageal spasm (DES) was de®ned by the presenceof 30% or more simultaneous contractions.21 Nut-cracker esophagus was de®ned as the presence ofhigh-amplitude peristaltic contractions, with anaverage amplitude of more than 180 mmHg.22 Non-speci®c motility disorder was de®ned as 30% or morelow-amplitude (<30 mmHg) or non-transmitted(<10 mmHg) contractions.

Anatomical de®nitions

· LES length: the distance between the upper andlower borders of the LES;

· esophageal body length: the distance between theupper border of the LES and the lower border ofthe UES;

· UES length: the distance between the upper andlower borders of the UES;

· intra-abdominal LES length: the distance betweenthe PIP and the lower border of the LES.

Each patient was categorized on the basis of themanometry and pH monitoring ®ndings into one ofthe following groups:

· no re¯ux, normal motility (pH) mot))· no re¯ux, non-speci®c motility disorder (NSMD)

(pH) mot+)· achalasia (Ach)· primary motility disorders excluding achalasia

(di�use esophageal spasm, nutcracker esophagus)(PMD)

· re¯ux, normal motility (pH+ mot))· re¯ux, NSMD (pH+ mot+)

Statistical analysis

The means (s.e.m.) were calculated for normallydistributed data (all manometric measurements), andmedians (range) for the DeMeester scores. Di�e-rences between groups were established using Stu-dent's t-test and one-way analysis of variance withpost hoc testing, and the Mann±Whitney U-testwhere appropriate. The e�ect of age and sex ongroup di�erences was investigated using multiplelinear regression analysis.

298 Diseases of the Esophagus

RESULTS

Of the 1144 subjects, 569 were men and 575 women(mean age 48.7 years, range 18±87). The demogra-phics of each group is shown in Table 1. The controlgroup was the youngest (p < 0.05 compared with allgroups except pH+ mot)), and the PMD group wassigni®cantly older than all other groups (p < 0.05).The mean (s.e.m.) age of men was signi®cantly lessthan women [46.79 (0.63) compared with 50.09 (0.61)years, p < 0.001]. Within each group, for all param-eters (UES position and length, esophageal bodylength, LESP, LES length and LES position), therewas no signi®cant di�erence between men andwomen, or between subjects older or younger thanthe mean age.

Figure 1 shows the mean UES, esophageal bodyand LES lengths and cumulative distances in 36controls. The mean distance to the upper border ofthe LES is 42.41 cm.

Upper esophageal sphincter

There was no signi®cant di�erence between groupswith regard to mean (s.e.m.) UES length (range 3.05±3.30 cm). There was no signi®cant di�erence in the

distance to the upper border of the UOS betweengroups (range 17.24±17.54 cm).

Esophageal body length

Figure 2 shows the esophageal body length for eachgroup. Those with achalasia have a signi®cantlylonger esophageal body than all other groups exceptthe controls [22.41 (0.27) cm]. The groups withoutre¯ux (PMD, pH) mot+, pH) mot)) had a signi-®cantly longer esophageal body than the groups withre¯ux. Group pH+ mot) had the shortest esopha-geal body length [20.06 (0.13) cm]. Linear regressionanalysis showed that these results were not a conse-quence of age or sex di�erences between the groups.

When all patients were combined, the mean(s.e.m.) esophageal body length for men [21.12 (0.1)cm] was signi®cantly longer than for women [20.15(0.09) cm, p < 0.001].

Lower esophageal sphincter pressure

Figure 3 shows the mean (s.e.m.) LESP in eachgroup. Those with achalasia have signi®cantly greaterLESP [17.46 (1.06) mmHg] than all other groups. TheLESP in the groups without re¯ux are similar to eachother, but are signi®cantly greater than those withpathological re¯ux, who have the lowest LESP. Thegroup pH+ mot+ has the lowest LESP [6.57 (0.24)mmHg].

Lower esophageal sphincter length

Figure 4 shows the mean (s.e.m.) LES length in eachgroup. The LES is longest in groups pH) mot) [4.24(0.05) cm] and PMD [4.15 (0.11) cm] and shortest inthose with achalasia [3.75 (0.12) cm] and the controls

Table 1. Patient demographics

Group No. of subjects Percent male Age (mean, range)

Control 36 58 41.9** (20±73)Ach 82 55 49.3 (18±84)pH) mot) 277 37 48.8 (21±81)pH) mot+ 97 42 48.1 (21±81)PMD 73 44 54.0* (18±87)pH+ mot) 287 57 46.2 (18±85)pH+ mot+ 292 58 49.7 (16±83)

* p < 0.05 compared with all other groups; ** p < 0.05 comparedwith all groups except pH+ mot).

Fig. 1ÐEsophageal measurements in 36 healthy controls. Mean(s.e.m.) values of UES position and length, esophageal body length,and LES position and length (left) and cumulative distances (right)are shown.

Fig. 2ÐMean (s.e.m.) esophageal body length (cm). *p < 0.05compared with PMD, pH) mot+, pH) mot), pH+mot+,pH+ mot); **p < 0.05 compared with pH) mot), pH+mot+,pH+mot); ***p < 0.05 compared with pH+ mot).

Esophageal length in health and disease 299

[3.69 (0.15) cm]. Linear regression analysis showedthat these results were not a consequence of age orsex di�erences between the groups.

Proportion of lower esophageal sphincterwithin the abdomen

Figure 5 shows the ratio of intra-abdominal LESlength to intrathoracic LES length. The greater thisratio the greater the proportion of LES within theabdomen. The patients with the greatest proportionof LES within the abdomen are those with achalasia[1.29 (0.12)]. The groups with the smallest proportionof LES within the abdomen are those with patho-logical re¯ux [pH+ mot) 1.04 (0.05), pH+ mot+1.04 (0.06)]. These two groups have a signi®cantlysmaller proportion of LES within the abdomen thanthe patients with achalasia (p < 0.05). Linear regres-

sion analysis showed that these results were not aconsequence of age or sex di�erences between thegroups.

DeMeester score

The median (range) DeMeester score was calculatedfor both groups with pathological re¯ux. The groupwith pathological re¯ux and NSMD (pH+ mot+)had a signi®cantly higher DeMeester score [44.4(14.8±176.5)] than the group with pathological re¯uxand normal motility [pH+ mot); 26.2 (14.8±123.1),p < 0.001].

DISCUSSION

Esophageal body length depends not only on themethod of measurement, but the de®nition of wherethe esophagus starts and ®nishes. Control data are,however, scarce and are confused by a variety ofanatomical de®nitions. An endoscopic study ofpatients with `gastric disease' found the meanesophageal length from the `upper end of the eso-phagus' to the `cardia' to be 28 cm.9 A manometricstudy of 42 controls, measuring from the proximalUES to the distal LES, found the distance to be25 cm.12 Another study of 28 controls, measuringfrom the high-pressure zone of the UES to theproximal LES (similar to the present study) observedthe length to be 23 cm.13 Measurement from thehigh-pressure zone of the UES to the high-pressurezone of the LES in 197 controls gave a length of23.4 cm.14 In the present study, we have de®ned theesophageal body as the distance from the distal UESto the proximal LES, a mean distance of 21.9 cm in38 control subjects, similar to other studies bearing inmind the additional length of esophageal sphincterincluded in them. We did not address the question ofwhether height in¯uences esophageal length. Two

Fig. 3ÐMean (s.e.m.) lower esophageal sphincter pressure.*p < 0.05 compared with all other groups; **p < 0.05 comparedwith pH) mot), pH+ mot+, pH+ mot); ***p < 0.05 com-pared with pH+ mot).

Fig. 4ÐMean (s.e.m.) lower esophageal sphincter length.*p < 0.05 compared with pH+ mot+, ach, control; ** p < 0.05compared with pH+ mot+, control.

Fig. 5ÐRatio of intra-abdominal length of LES (IALES) tointrathoracic length of LES (ITLES). *p < 0.05 compared withpH+ mot), pH+ mot+.

300 Diseases of the Esophagus

studies have found a direct correlation betweenheight and esophageal length,9,11 although two studiesdid not.13,14 The ®nding of a greater esophageallength in men than in women is consistent with otherstudies,9,13 and is probably a consequence of heightdi�erence between men and women.

The mean distance to the UES is slightly morethan 17 cm in all groups. This is important informa-tion for those who perform transnasal intubationbecause it is vital that the patient swallows just beforethe esophagus is intubated so that the UES relaxes.The swallow should take place before this point isreached. It must be remembered that the distancefrom the incisors to the UES is slightly less than fromthe external nares to the UES by 3±5 cm,23 and thisfact should be taken into account when performingtransoral intubation and when comparing endoscopicand manometric distances.

Of more interest is the variation in esophageallength with esophageal disease (Fig. 2). The increasein esophageal length in achalasia has previously beenreported.12,13 The relatively small number of controlsin the present study may be the reason for thedi�erence between the controls and the achalasiapatients not being signi®cant. The increased length inthe esophagus is thought to be secondary to changesin the esophageal muscle after denervation.12 It isalso feasible that the mechanical and gravitationalresult of impaired emptying would be increasedlength, and a trend has been observed of increasinglength with increasing age of presentation. Indeed,Mason and Bremner12 proposed using esophageallength as a method of assessing disease severity.Objective evidence of esophageal shortening withre¯ux disease, as opposed to cranial movement of theLES, has not been previously reported. Li et al13

observed a trend towards a shorter esophagus inpatients with scleroderma, but small patient numbersprevented any ®rm conclusions. Csendes et al8

assessed esophageal body length indirectly by endo-scopic measurement of the position of the distal LES.They found no change in LES position with increasingre¯ux disease, although they did observe proximalmigration of the squamocolumnar junction. Onehypothesis is that esophageal body shortening issecondary to chronic in¯ammation and ®brosisassociated with re¯ux disease, although whether it isde®nitely cause or e�ect remains uncertain. It isinteresting to note that group pH+ mot+, withmore severe re¯ux as judged by the DeMeester score,did not have a shorter mean esophageal body lengththan group pH+ mot), although there was nosigni®cant di�erence in esophageal length betweenthe two groups.

When considering the total LES length (Fig. 4),it is interesting to note the short LES in those withachalasia. This probably re¯ects the hypertonicityof the sphincter, with a consequent apparent

shortening. This ®nding is mirrored in a study byCsendes et al24 who measured the muscular gastro-esophageal junction of achalasia patients at openoperation and found it to be shorter and of smallercircumference than those with re¯ux disease. Theshort LES in the controls in the present study maybe a re¯ection of the relatively small numbers.However, animal and human studies have shownthat the important factor in gastroesophageal junc-tion competence is not total LES length, but intra-abdominal LES length in combination with LESpressure.16,17 Competence requires both an adequateLES pressure in addition to an adequate length ofLES within the abdomen. Restoration of functionrequires increases in both, which can be achieved bya fundoplication. Figure 3 demonstrates not onlythe increased LES pressure of achalasia, but thereduced LES pressure of re¯ux disease. Althoughthe present study does not identify LES shorteningwith re¯ux disease (Fig. 4), Fig. 5 demonstrateshow, despite this, the largest proportion of intra-abdominal LES occurs in the patients with theshortest LES (achalasia), whereas the smallestproportion of intra-abdominal LES occurs inpatients with re¯ux disease.

Several studies have shown that the total LESlength reduces in re¯ux disease.8,15,18 One mightspeculate whether this is a true reduction in LESmuscle length, or an artifactual decrease observedmanometrically as a result of the reduced pressureexerted at the upper and lower limits of the LES. Thismight be expected to result in a consequent increasein esophageal body length, as that portion of upperLES which fails to register any pressure is interpretedas esophageal body. However, this study has shownthat a shortened esophageal body is a very realfeature of re¯ux disease, in addition to a proximalmovement of the LES relative to the diaphragm. Insummary, the esophageal body is longest in achalasiaand shortest in re¯ux disease. This is associated witha caudal movement of the LES in achalasia andcranial movement of the LES in re¯ux disease withrespect to the diaphragm.

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