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CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2013;11:131–137

ALIMENTARY TRACT

A Comparison of Symptom Severity and Bolus Retention With ChicagoClassification Esophageal Pressure Topography Metrics in Patients WithAchalasia

FRÉDÉRIC NICODÈME,*,‡ ANNEMIJN DE RUIGH,*,§ YINGLIAN XIAO,*,� SHANKAR RAJESWARAN,¶

EZRA N. TEITELBAUM,#,** ERIC S. HUNGNESS,# PETER J. KAHRILAS,* and JOHN E. PANDOLFINO*

*Department of Medicine, ¶Department of Radiology, #Department of Surgery, Feinberg School of Medicine, Northwestern University, Chicago, Illinois; ‡Departmentof Thoracic Surgery, Centre Hospitalier de l’Université de Montréal, Montréal, Québec, Canada; §Department of Gastroenterology and Hepatology, Academic Medical

enter Amsterdam, Amsterdam, The Netherlands; �Department of Gastroenterology, First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, China; and**Department of Surgery, George Washington University, Washington, District of Columbia

This article has an accompanying continuing medical education activity on page e15. Learning Objectives—At the endof this activity, the successful learner will review the assessment and management of a patient with achalasia using

high-resolution manometry and the Chicago classification.

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BACKGROUND & AIMS: We compared findings from timedarium esophagrams (TBEs) and esophageal pressure topographytudies among achalasia subtypes and in relation to symptom severity.

METHODS: We analyzed data from 50 patients with achalasia (31en; age, 20–79 y) who underwent high-resolution manometry

HRM), had TBE after a 200-mL barium swallow, and completeduestionnaires that determined Eckardt Scores. Twenty-five patientsere not treated, and 25 patients were treated (11 by pneumaticilation, 14 by myotomy). Nonparametric testing was used to assessifferences among groups of treated patients (10 had type 1 achalasiand 15 had type 2 achalasia), and the Pearson correlation was used tossess their relationship. RESULTS: There were no significant

differences in TBE measurements between patient groups. Of the 25patients who received treatment, 10 had a manometric pattern con-sistent with persistent achalasia after treatment (6 patients with type1 and 4 patients with type 2 achalasia), whereas 15 appeared to haveresolved the achalasia pattern (peristalsis was absent in 8 patients andweak in 7 patients). The height of the barium column at 5 minutesand Eckardt Scores were reduced significantly in patients who hadresolved their achalasia pattern, based on HRM. The integrated relax-ation pressure and the TBE column height correlated at 5 minutes(r � 0.422; P � .05). CONCLUSIONS: Patients who resolvedheir achalasia pattern, based on HRM, showed improved emp-ying based on TBE measurements and improved symptomcores. There was no significant difference between patients withype 1 or type 2 achalasia in TBEs. These findings indicate thatormalization of the integrated relaxation pressure on HRM is alinically relevant objective of treatment for achalasia.

eywords: Achalasia; Manometry; Esophagram; Symptom.

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Achalasia is diagnosed by showing dysfunction of loweresophageal sphincter relaxation and aperistalsis in the

bsence of obstructive pathology. The major modalities used tostablish the diagnosis and manage the disease are endoscopy,imed barium esophagram (TBE), and esophageal manometry.

TBE quantifies delayed esophageal emptying as a surrogatearker of esophagogastric junction (EGJ) dysfunction, may

dentify the characteristic bird beak configuration at the lowersophageal sphincter, and details the degree of dilatation origmoid appearance. However, both TBE and endoscopy may beormal in achalasia patients1,2 because they do not detect thearly physiological dysfunction of the disease. Hence, manom-try has become the gold standard for diagnosing achalasia.

High-resolution manometry (HRM) with esophageal pressureopography (EPT) has improved the accuracy of manometry inetecting achalasia and defined clinically relevant subtypes beforereatment.2–6 The achalasia subtypes are differentiated basedn the patterns of esophageal pressurization and contractionuring the 10-swallow protocol. However, no data exist toubstantiate that HRM characteristics correlate with symptomeverity or treatment efficacy. Hence, we hypothesized that the EPTeatures used to distinguish type 1 from type 2 achalasia wouldranslate into differences on TBE before therapy and that improve-

ent in EPT metrics of EGJ function after treatment would bessociated with improved symptoms and reduced bolus retention.

The aim of this study was to assess the relationship betweenontractile and pressurization patterns defined on EPT, clinicalnd points of bolus retention on TBE, and symptom severity inype 1 and type 2 achalasia. In addition, we sought to comparePT and TBE metrics as measures of treatment efficacy.

Abbreviations used in this paper: EGJ, esophagogastric junction;EPT, esophageal pressure topography; ES, Eckardt score; HRM, high-resolution manometry; IRP, integrated relaxation pressure; TBE, timedbarium esophagram.

© 2013 by the AGA Institute1542-3565/$36.00

http://dx.doi.org/10.1016/j.cgh.2012.10.015

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132 NICODÈME ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 2

Materials and MethodsSubjectsFifty nonspastic achalasia patients (31 men; age, 20–79 y)

prospectively were recruited into 2 separate cohorts. The firstcohort of 25 patients was enrolled from the clinic at theNorthwestern Esophageal Center based on a new diagnosis oftype 1 or type 2 achalasia. All 25 patients underwent endoscopy,HRM, TBE, and symptom assessment before treatment. A sec-ond cohort of 25 treated patients were enrolled based on havinghad pretreatment type 1 or type 2 achalasia and were undergo-ing our post-treatment study protocol including HRM, TBE,endoscopy, and symptom assessment. Only types 1 and 2 wereincluded in the study because the spastic contractions in type 3achalasia have unique features on TBE and EPT that are inde-pendent of bolus retention and sphincter function. HRM andTBE studies were performed within 1 month of each other. Allsubjects gave written informed consent. The Northwestern Uni-versity Institutional Review Board approved the study protocol.

Symptom AssessmentFor all 50 patients, dysphagia, regurgitation, retroster-

nal pain, and weight loss were assessed to calculate the EckardtScore (ES),7–11 each graded from 0 to 3. Patients were classified

s having a good outcome if ES was less than 3 or a poorutcome if ES was 3 or greater.

High-Resolution ManometryManometric studies were conducted in the supine po-

sition after a 6-hour fast. The HRM catheter was a 4.2-mmouter-diameter solid-state assembly with 36 circumferentialsensors spaced 1 cm apart (Given Imaging, Duluth, GA). TheHRM assembly was calibrated at 0 and 300 mm Hg and placedtransnasally. The HRM assembly was positioned during endos-copy in instances of challenging anatomy, strong patient pref-erence, or prior experience suggesting that would be necessary.In those instances, the manometry study was performed at least2 hours after endoscopy. The manometric protocol included a2-minute baseline recording and ten 5-mL swallows.

Manometry studies were analyzed using ManoView analysissoftware (Given Imaging). Key EPT metrics analyzed were inte-grated relaxation pressure (IRP),12,13, nadir lower esophagealsphincter pressure, peristaltic integrity using the 20–mm Hg iso-baric contour, distal contractile integral, contractile front velocity,and the distal latency.1,14 The key metric in achalasia is the IRP,which quantifies EGJ relaxation both in completeness and persis-tence. The upper limit of normal of the mean IRP for this protocoland instrumentation is less than 15 mm Hg.3 Additional measures

f EGJ function analyzed were the mean resting EGJ pressure atnd-expiration during the 2-minute baseline recording and meanadir EGJ relaxation pressure measured using the isobaric contourool on ManoView software.7,9–11

Pressure patterns within the esophagus were characterized asin Figure 1.12 Peristaltic integrity was scored as intact (no break�2 cm in the 20 –mm Hg isobaric contour), weak (breaks �2cm in the 20 –mm Hg isobaric contour), or failed (�3 cmintegrity of the 20 –mm Hg isobaric contour distal to thetransition zone).14

The criteria used for defining type 1 achalasia in untreatedpatients were as follows: an IRP of 15 mm Hg or greater and

100% failed peristalsis. Pretreatment type 2 achalasia was de-

fined as follows: an IRP of 15 mm Hg or greater and panesopha-geal pressurization in 20% or more of test swallows. The pres-ence of premature contractions with 20% or more of testswallows or swallows showing preserved peristalsis excluded thediagnosis of type 1 or 2 achalasia because these would becategorized as type 3 achalasia and EGJ outflow obstruction,respectively.

With post-treatment patients, the same definitions were usedwith the caveat that patients were no longer categorized ashaving an achalasia subtype if the post-treatment IRP was lessthan 15 mm Hg. Hence, patients were categorized as havingpersistent achalasia (type 1 or 2) or a resolved achalasia patternalong with a description of the current manometric profileusing the same Chicago Classification definitions as pretreat-ment. We emphasize that a resolved achalasia pattern does notequate to resolution of the achalasia disease process.

Timed Barium EsophagramTBEs were performed in the upright position to obtain

frontal spot films of the esophagus at baseline, and at 1, 2, and5 minutes after ingestion of 200 mL (sometimes limited bypatient tolerance) of low-density (45% weight to volume) bar-ium sulfate. The height of the barium column was measuredvertically from the EGJ using a lead scale placed directly on thepatient. The maximal esophageal diameter was measured alongthe esophageal body perpendicular to the axial plane of theesophagus.

Statistical AnalysisData from each patient cohort were analyzed indepen-

dently. Continuous variables were expressed as the median(25th–75th percentile). We used the Mann–Whitney test tocompare 2 samples, and the Kruskal–Wallis test to comparemore than 2 samples using a significance level of P less than .05.Correlations were calculated using the Pearson correlation co-efficient.

ResultsThe untreated cohort consisted of 17 men and 8

women, ages 31 to 67 years. The treated cohort had 14 men and11 women, ages 20 to 79 years. Seven HRM studies (14%) wereperformed after using endoscopy to position the HRM assem-bly. The untreated group consisted of 10 type 1 and 15 type 2achalasia patients, whereas the pretreatment distribution of thetreated group was 15 type 1 and 10 type 2 achalasia patients.The treatments rendered were pneumatic dilation (n � 11),aparoscopic Heller myotomy (n � 9), and per-oral endoscopic

yotomy (n � 5).

Untreated PatientsType 2 untreated patients had a significantly greater

IRP (24; interquartile range [IQR], 18 –33 mm Hg vs mean, 16;IQR 12–21 mm Hg) and nadir-relaxation pressure (20; IQR,14 –29 mm Hg vs mean, 12; IQR, 9 –18 mm Hg) compared withthe type 1 patients. Resting EGJ pressure (type 1, 15; IQR, 12–21mm Hg; type 2, 15; IQR, 18 –33 mm Hg), barium column height(type 1, 8.9 cm; IQR, 7–14 cm; type 2, 7.0; IQR, 6.0 –11.5 cm),and barium column width (type 1, 2.9; IQR, 2.2– 4 cm; type 2,3.4; IQR, 3.0 – 4.1 cm) were similar between achalasia subtypes

(Figure 2). There were also no differences in ES for the type 1

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February 2013 ACHALASIA: HRM, ESOPHAGRAM, AND ECKARDT SCORE 133

(mean, 5; IQR, 5– 6) and type 2 (mean, 7.5; IQR, 6.8 – 8.3)patients. No significant correlations were found between TBEcolumn height at 5 minutes and IRP (r � �0.21, P � .30),resting EGJ pressure (r � �0.04, P � .85), nadir EGJ relaxationpressure (r � �0.16, P � .45), or ES (r � 0.10, P � .80).

imilarly, there was no correlation between ES and IRP (r �.59, P � .10), resting EGJ pressure (r � 0.17, P � .67), andadir EGJ relaxation pressure (r � 0.63, P � .07).

Relationship Between Esophageal PressureTopography Findings, Timed BariumEsophagram Findings, and TreatmentOutcomeTen post-treatment patients had EPT findings of per-

sistent achalasia pattern (6 type 1 patients and 4 type 2 pa-tients), whereas 15 patients had resolution of the achalasiapattern and converted to either absent peristalsis (n � 8) orweak peristalsis (n � 7). Table 1 compares HRM, TBE, and ES

Figure 1. The 4 potential HRMpatterns after treatment of type 1or type 2 achalasia. (A and B)

ersistent achalasia patterns.C and D) Resolved achalasiaatterns: (C) absent peristalsis or

D) weak peristalsis.

data of patients with persistent vs resolved achalasia pattern.

The IRP, resting EGJ pressure, and nadir EGJ all were correlatedsignificantly with post-treatment ES, as follows: IRP, r � 0.51,P � .01; resting EGJ pressure, r � 0.43, P � .04; and nadir EGJrelaxation pressure, r � 0.44, P � .03. Analyzing the EPTmetrics dichotomously as normal or abnormal based on thepredefined cut-off values showed a significant difference inboth TBE-defined and ES-defined outcome for the IRP cut-offvalue of 15 mm Hg, but not for the EGJ resting pressure or forthe nadir EGJ relaxation pressure (10 mm Hg) (Figure 3).

TBE column height at 5 minutes (but not width), IRP, andES were significantly lower in patients with resolved achalasiapatterns on HRM than in patients with a persistent achalasiapattern (Figure 4). The subgroup of 7 patients with weakperistalsis appeared to have the best outcome: the median TBEcolumn height at 5 minutes was significantly lower than in the3 other groups (P � .05), and ES showed a trend toward a lowervalue compared with the other 3 groups (P � .07).

There were no significant correlations between the TBE col-

umn height at 5 minutes and resting EGJ pressure (r � 0.18,

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134 NICODÈME ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 2

P � .37) or nadir EGJ relaxation pressure in the post-treatmentatients (r � 0.27, P � .20). Only the IRP showed a weakorrelation (r � 0.42, P � .05). The correlation between TBE

column height at 5 minutes and ES after treatment also was notsignificant (r � 0.31, P � .24). However, the median TBEcolumn height at 5 minutes for patients with an ES of 3 orgreater (6.9 cm; IQR, 6.7– 8.2 cm) was significantly greater than

Table 1. Characteristics of Treated Patients, Median

Persistent ach

HRM pattern 6 type 1 patients,Treatment PD, 5 patients; PO

LHM, 3 patientsIRP, mm Hg (IQR) 19 (17

esting EGJ pressure, mm Hg (IQR) 15 (9–adir EGJ relaxation pressure, mm Hg (IQR) 14 (11BE 5 minutes, cm (IQR) 8 (7–BE width, cm (IQR) 2.9 (1.S 4 (2–

HM, laparoscopic Heller myotomy; PD, pneumatic dilation; POEM, per-ora

that for patients with an ES less than 3 (2.5 cm; IQR, 0 – 6.85cm). Assessing the best cut-off value for TBE column height at5 minutes for predicting a good response to the treatmentsuggested that a 5-cm value was the optimal discriminator; 75%of patients with a TBE column height less than 5 cm had an ESless than 3, whereas 54% of patients with a TBE column heightgreater than 5 cm had an ES of 3 or greater. By using a 5-cm

Figure 2. Examples of TBE andHRM studies for untreated pa-tients. The TBE column heightand width do not differentiatetype 1 and type 2 achalasia.

a pattern Resolved achalasia pattern P value

e 2 patients 8 absent, 7 weak peristalsis2 patients; PD, 6 patients; POEM, 3 patients;

LHM, 6 patients8 (7–12) �.057 (5–11) �.057 (5–11) �.052 (0–5) �.05

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February 2013 ACHALASIA: HRM, ESOPHAGRAM, AND ECKARDT SCORE 135

cut-off value to dichotomously define the TBE outcome as goodor poor, the ES was significantly better in those with a goodTBE outcome (TBE, �5 cm; median ES, 3; IQR, 2–5; TBE, �5m; median ES, 1.5; IQR, 0 –2.25). Similarly, the 5-cm cut-offalue showed a trend correlating with outcome gauged by theost-treatment IRP (TBE � 5 cm: median IRP, 17.5 mm Hg;QR, 10 –21; TBE � 5 cm: median IRP, 8 mm Hg; IQR, 7–13;� .06). There was no relationship between maximal esopha-

eal diameter on TBE and ES (r � �0.03, P � .89).

Figure 3. TBE column height at5 minutes and ES in patientgroups defined by normal or ab-normal EGJ metrics: (A) IRP, (B)resting EGJ pressure, and (C)nadir EGJ relaxation pressure.Note that only the IRP (�15 or�15 mm Hg) segregates the pa-tients into 2 significantly differentgroups (P � .05). LES, loweresophageal sphincter pressure.

Figure 4. Comparison of IRP (mm Hg), TBE column height at 5 min-utes (cm), and ES (median) among patients subdivided by post-treat-ment EPT pattern (types 1 and 2 achalasia, absent peristalsis, and weakperistalsis). The values of the 3 variables were lower in patients with aresolved achalasia pattern (P � .05), suggesting this was indicative ofonsistently better outcome. The group that evolved to weak peristalsisppeared to have the best outcome with a significantly lower bariumolumn height at 5 minutes (P � .05) and a trend toward a lower ES

ompared with the other 3 groups.

Concordance Between Timed BariumEsophagram and Esophageal PressureTopography in Predicting Symptom Outcome

Plotting the TBE column height vs IRP revealed somediscordance between the 2 techniques and symptom outcome(Figure 5). Although an abnormal IRP was never associated withcomplete emptying, there were multiple instances in which anormal IRP was associated with bolus retention. However, mostof these patients were asymptomatic and had a greater degree of

Figure 5. Relationship between IRP (mm Hg) and TBE column heightat 5 minutes (cm) defined by post-treatment ES and HRM pattern.Resolution of the HRM achalasia pattern was associated with a greaterlikelihood to have an ES less than 3. There were no instances in whichthe IRP was abnormal and complete emptying occurred. Patients alsotended to have better outcomes when both the IRP and barium columnheight were less than the cut-off values (IRP �15 mm Hg, TBE columnheight �5 cm), but there were 2 patients who continued to have symp-

toms despite minimal bolus retention and low IRP values.

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136 NICODÈME ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 2

esophageal dilatation. There were 3 patients with an IRP lessthan 15 mm Hg and a borderline abnormal ES of 3; 1 patientwith no bolus retention, and 2 patients with minimal andmoderate TBE bolus retention at 5 minutes (column heights of1.5 and 5.5 cm), suggesting that their symptoms were moderate.One subject had an IRP less than 15 mm Hg and continued tohave evidence of severe bolus retention with minimal symp-toms. This subject had severe dilatation on the TBE explainingthe bolus retention. Concordance of abnormalities on TBE andIRP was associated with a poor ES in 5 of the 7 such patients.The 2 patients with ES less than 3 despite abnormal emptyingand an IRP greater than 15 mm Hg were both type 2 achalasiapatients who had a major reduction in IRP after treatment(reduction: 54 to 17 mm Hg and 33 to 22 mm Hg).

DiscussionWe performed this study to assess whether HRM-EPT

metrics correlate with symptom severity and bolus retention onTBE in achalasia patients before or after treatment. Our find-ings suggest that resolution of the achalasia pattern on EPTafter treatment was associated with an improvement in symp-toms and reduced bolus retention. Although the IRP was notstrongly linearly correlated with symptom severity, when ana-lyzed dichotomously patients with an IRP of 15 mm Hg orgreater had worse symptom scores and greater bolus retentionon TBE compared with those with normal IRP values. In con-trast, no EPT pattern, EPT metric, or TBE variable predictedsymptom severity in untreated achalasia patients. Furthermore,barium height on TBE did not distinguish achalasia EPT sub-types. These findings suggest that in addition to its provenutility in detecting pretreatment achalasia, EPT also has utilityin the management of post-treatment achalasia that can com-plement TBE.

TBE is useful to diagnose achalasia and to assess for dilata-tion and sigmoid configuration, features suggesting worseprognosis. In addition, bolus retention on TBE is a usefulmetric in assessing treatment outcome in that it can substan-tiate the necessity for further treatment.2,4 – 6 On the other hand,although most clinical guidelines advise that the diagnosis ofachalasia requires manometric evaluation, some suggest thatmanometry is not required in post-treatment management.8,15

Although an EGJ pressure of less than 10 mm Hg after treat-ment has been identified as indicative of good outcome, thereare conflicting reports regarding the utility of this measurementin the evaluation of post-treatment success.13,16,17 We hypothe-ized that the greater detail and the improved accuracy of

easurement provided by HRM with EPT analysis could im-rove the value of manometry in post-treatment management.ur findings suggest that the resolution of the achalasia pat-

ern on EPT was associated with better symptom scores and lessolus retention. Of the 15 post-treatment patients with a res-lution of the achalasia pattern, 73% had bolus retention of 5m or less at 5 minutes and 79% had an ES less than 3, whichas indicative of a good outcome. In addition, it appeared that

he contractile pattern in the patients with a resolved achalasiaattern may have some significance because those patientshowing weak peristalsis after treatment had no bolus retentionnd a better ES compared with those with absent peristalsis.

owever, these numbers were small and this phenomenon will t

equire a larger sample size before definitive conclusions can beade.Although resolution of the achalasia pattern on EPT was

elpful in substantiating a good outcome, IRP by itself showednly a weak correlation with ES and the TBE barium columneight at 5 minutes. However, the relationship between theseeasures and symptom outcome is unlikely to be linear with a

trong Pearson correlation. Our findings suggest a thresholdalue of IRP (15 mm Hg) was predictive of symptom improve-ent and that once a patient achieved that threshold, further

eduction in the IRP may not provide further benefit. This isvident in Figure 4, in which it appears that the IRP thresholdf less than 15 mm Hg was associated with better ES and lessolus retention on TBE.

The barium column height at 5 minutes on TBE also wasot correlated significantly with ES, again highlighting thathese tests probably function better with discrete target cut-offalues as opposed to assessing correlation in a linear fashion.ur analysis suggests that a value of 5 cm for the TBE columneight at 5 minutes was a reasonable target outcome becausehe median barium height on TBE at 5 minutes in patients withn ES of 3 or greater was 6.9 cm (IQR, 6.7– 8.2 cm), and 5 cmppeared to best discriminate positive and negative outcomes inhis limited data set. Of note, a recent randomized controlledrial assessing pneumatic dilation vs myotomy proposed a col-mn height of less than 10 cm as the target column height forBE using the study to assess need for repeat pneumatic dila-

ion. Clearly, further work is required in a larger series to definehe optimal cut-off value for barium column height to guide

anagement.Although the cut-off values for interpreting TBE and EPT

tudies suggested here and in previous publications appeareasonable as indicators of outcome success, the nature ofchalasia as a dominant motor disorder in the early stages anddominant anatomic disorder in the very late stages invariablyill make certain measurements less useful in each situation.here are occasions that patients will continue to have a poor

ymptom outcome despite a resolution of the achalasia patternr reduction of the IRP to less than 15 mm Hg because theisorder has evolved to where the anatomic deformity domi-ates the clinical picture. This was evident in Figure 5 in whichsingle patient had a TBE with severe retention and dilatationespite having an IRP of 4 mm Hg and relatively mild symp-oms. Conversely, there were patients who continued to haveymptoms despite minimal to no bolus retention and a normalRP, suggesting that some patients may have a component ofypersensitivity to minimal transit abnormalities or a compo-ent of reflux driving the persistent symptoms.

In conclusion, our findings suggest that EPT is useful in thevaluation of achalasia after treatment and that normalizinghe IRP was associated with a good symptom outcome. The bestymptomatic outcome was seen in individuals who evolved to aeak peristalsis pattern. In addition, TBE did not distinguish

ype 1 from type 2 achalasia and the ability to identify theseubtypes appears to be unique to EPT. However, TBE doesomplement EPT, especially when the disease has progressed ton anatomic-dominant disorder. Future studies need to beerformed in a large series of patients before and after therapyo confidently establish the relative merits of each evaluation in

erms of predicting long-term outcome and cost effectiveness.

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February 2013 ACHALASIA: HRM, ESOPHAGRAM, AND ECKARDT SCORE 137

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Reprint requestsAddress requests for reprints to: John Pandolfino, MD, Department

of Medicine, Division of Gastroenterology, Feinberg School of Medi-cine, Northwestern University, 676 St Clair Street, Suite 1400, Chi-cago, Illinois 60611-2951. e-mail: j-pandolfino@northwestern.edu; fax:(312) 695-3999.

Conflicts of interestThe authors disclose no conflicts.

FundingThis work was supported by R01 DK079902 (J.E.P.) and R01

DK56033 (P.J.K.) from the Public Health Service.