2013 SSAT PLENARY PRESENTATION

High-Resolution Manometry Classifications for IdiopathicAchalasia in Patients with Chagas' Disease Esophagopathy

Fernando P. P. Vicentine & Fernando A. M. Herbella &

Marco E. Allaix & Luciana C. Silva & Marco G. Patti

Received: 29 March 2013 /Accepted: 21 September 2013 /Published online: 16 October 2013# 2013 The Society for Surgery of the Alimentary Tract

AbstractBackground Idiopathic achalasia (IA) and Chagas' disease esophagopathy (CDE) share several similarities. The comparisonbetween IA and CDE is important to evaluate whether treatment options and their results can be accepted universally. High-resolution manometry (HRM) has proved a better diagnostic tool compared to conventional manometry. This study aims toevaluate HRM classifications for idiopathic achalasia in patients with CDE.Methods We studied 98 patients: 52 patients with CDE (52 % females, mean age, 57±14 years) and 46 patients with IA(54 % females; mean age 48±19 years). All patients underwent a HRM and barium esophagogram.Results The Chicago classification was distributed in IA as Chicago I, 35%; Chicago II, 63%; and Chicago III, 2 %, and in CDEas Chicago I, 52 %; Chicago II, 48 %; and Chicago III, 0 % (p =0.1, 0.1, and 0.5, respectively). All patients had the classicRochester type. CDE patients had more pronounced degrees of esophageal dilatation (p <0.002). The degree of esophagealdilatation did not correlate with Chicago classification (p =0.08). In nine (9 %) patients, the HRM pattern changed during the testfrom Chicago I to II.Conclusion Our results show that (a) HRM classifications for IA can be applied in patients with CDE and (b) HRMclassifications did not correlate with the degree of esophageal dilatation. HRM classifications may reflect esophageal repletionand pressurization instead of muscular contraction. The correlation between manometric findings and treatment outcomes forCDE needs to be answered in the near future.

Keywords Esophageal achalasia . Manometry . Chagas'disease

Introduction

Brazilian surgeons and gastroenterologists are experienced inthe treatment of Chagas' disease esophagopathy (CDE) due tothe high number of cases, but doubt remains whether theoutcomes in the treatment of CDE and idiopathic achalasia(IA) are comparable.

CDE and IA share the samemanometric findings: absence ofperistalsis in the esophageal body and no relaxation or partialrelaxation of the lower esophageal sphincter (LES);1–3 however,higher pressures of the esophageal body are noticed in patientswith IA, and basal and residual pressures of the LES are lower inpatients with CDE.4 Furthermore, esophageal dilation is a com-mon feature of CDE (rendering the name “megaesophagus”),while in IA, esophageal dilation is not pronounced.5

High-resolution manometry (HRM) classifications for IAhave apparent correlation with treatment outcomes6 and allowed

This study was presented at the 2013 SSAT Plenary Presentation annualmeeting, held at Orlando, FL, USA, last May 18–21, 2013.

F. P. P. Vicentine : F. A. M. Herbella : L. C. SilvaDepartment of Surgery, Escola Paulista de Medicina,Federal University of São Paulo, São Paulo, Brazil

M. E. Allaix :M. G. PattiDepartment of Surgery, University of Chicago, Chicago, IL, USA

F. A. M. Herbella (*)Surgical Gastroenterology, Division of Esophagus and Stomach,Hospital São Paulo, Rua Diogo de Faria 1087 cj 301, São Paulo, SãoPaulo, Brazil 04037-003e-mail: herbella.dcir@epm.br

J Gastrointest Surg (2014) 18:221–225DOI 10.1007/s11605-013-2376-1

the diagnosis of atypical manometric cases.7 The value of theapplication of these classifications in CDE patients is still elusive.

The aim of this study is to evaluate HRM classifications forIA in patients with CDE.

Methods

Population

We studied 98 consecutive and unselected patients with acha-lasia studied at the Federal University of São Paulo andUniversity of Chicago esophageal function testing laborato-ries. Patients were divided into two groups: 52 patients withCDE (52 % females; mean age, 57.42±14.8 years) and 46patients with IA (54 % females, mean age, 48.15±19.0 years).

The diagnosis of CDE was based on positive serologic testfor Chagas' disease and/or typical manifestation of the diseasein other target organs, such as the colon or heart, in patientsoriginated from endemic areas for Chagas' disease.

Patients previously treated were excluded from both groups.

Workup

All individuals underwent an esophagogram for the diagnosisof achalasia and evaluation of the esophageal dilatation, grad-ed according to the maximum esophageal diameter as follows:I, up to 4 cm; II, 4–7 cm; III, 7–10 cm; and IV, more than10 cm or sigmoid-shaped esophagus.8,9

All patients underwent an upper digestive endoscopy torule out malignant or premalignant lesions.

All patients underwent a HRM (Given Imaging, LosAngeles, USA) after fasting for 8 h. Medications that couldinterfere with esophageal motility were discontinued.Acquisition and data analysis were obtained via the dedicatedcommercial software (ManoScan and ManoView, GivenImaging, Los Angeles, USA). All studies were prospectivelyreviewed by two experienced researchers.

According to the Chicago classification,6 patients were di-vided in type I (minimum pressurization), type II (esophagealpressurization), and type III (esophageal spasm). According tothe Rochester group classification,7 patients were divided inclassic type (impaired deglutitive relaxation of the LES andaperistalsis) or variant type I (impaired LES relaxation withnormal/hypertensive peristalsis), variant type II (impaired/bor-derline LES relaxation with mixed peristalsis/simultaneouscontractions), or variant type III (impaired/normal LES andaperistalsis with occasional short segment peristalsis).

Statistics

Student's t test (to compare means), chi-square test (to com-pare proportions), and Spearman's test (to correlate variables)

were used when indicated. The value of p <0.05 was consid-ered significant.

Ethics

The study was approved by the institutional review board.There are no conflicts of interest.

The authors are responsible for the manuscript, and noprofessional or ghost writer was hired.

Results

CDE and IA groups were comparable in regard to gender (p =0.1) and age (p =0.9) (Table 1).

There was a preponderance of the more advanced grade ofesophageal dilatation for the CDE group (p <0.002) and apreponderance of grade I for the IA group (p <0.001).

HRM classifications are depicted in Table 2. There was nodifference in the distribution of Chicago classification typesfor CDE or IA. All patients had the classic Rochester type.

There was no correlation between the degree of esophagealdilatation and the Chicago classification (p =0.08).

In nine (9 %) patients of the total (six, CDE, and three, IA),the HRM pattern (degree of esophageal pressurization afterswallows) changed in some wet swallows during the execu-tion of the test, reclassifying the patients from Chicago I to II(Fig. 1).

Discussion

Our results show that (a) HRM Chicago classification for IAmay be applied to CDE, (b) variants of Rochester classifica-tion were not found in patients with CDE, and (c) the degreeof esophageal dilatation did not correlate with the Chicagoclassification.

Table 1 Population demographics and symptoms

Idiopathicachalasia(n=46)

Chagas' diseaseesophagopathy(n=52)

p value

Age (years) (mean ± standarddeviation)

48.15±19.0 57.42±14.8 0.9

% females 54 52 0.1

Symptoms (prevalence, %)

Dysphagia 100 98

Regurgitation 66 41

Weight loss 35 43

Heartburn 33 22

Chest pain 38 4

Cough 14 10

222 J Gastrointest Surg (2014) 18:221–225

Chicago Classification

This classification developed by Pandolfino et al.6 divides thepatients with achalasia in three subgroups according to theesophageal body pressure after swallows: type I with a min-imum pressurization, type II with esophageal pressurization,and type III with presence of esophageal spasm. Patients withtype II achalasia in HRM have better therapeutic response(91 % of good results with dilation and 100 % of good resultswith Heller' myotomy), and outcomes were less favorable intype I (56 %) and type III (29 %).

The application of this classification in patients with CDEwas first described by our group in a report with our initialfindings.10 In a recent paper, Remes-Troche et al.10 studiedpatients with incidentally positive serological test for Chagas'disease and found 66 % of esophageal motility disorders inthis population, but only two patients with the diagnosis ofachalasia, one of them is Chicago type I, and other, Chicagotype II. The outcomes of the treatment of these patients werenot mentioned.

In our study, we did not find difference in the distribution ofthe types of Chicago classification in a cohort of unselectedcases of IA and CDE, demonstrating that the Chicago classifi-cation, initially described for IA, also can be useful for CDE.Wealso observed that Chicago type III was not present in the CDEgroup. Actually, even before the Chicago classification, thepresence of vigorous achalasia, a variant of the classical acha-lasia with waves of high amplitude11 correspondent to theChicago type III, was questioned in patients with CDE.12 Thisfinding may be related to a suspected preservation of the cho-linergic pathway in type III pattern of IA, since CDE presentswith an impaired tonic influence of cholinergic nerves on thesmooth muscle of the esophagus.5

Interestingly, 9 % of the patients transitioned from Chicagotype I to Chicago type II during the tests with two or moreswallows with pressures greater than 30 mmHg. We believethat by offering water for swallowing, a high-pressure watercolumn in the esophageal body is created, and the measure-ment obtained by HRM should correspond to the pressuriza-tion of the esophagus, and there is no real muscle contraction,which is only present, probably, in Chicago type III. Thathypothesis is corroborated by the presence of identical pres-sures across the esophageal body, forming an isobaric image,suggesting a liquid column that respects the principle of

Table 2 HRM classifications

Idiopathic achalasian =46 (%)

Chagas' diseaseesophagopathyn=52 (%)

p value

Chicagoclassification

I 16 (35) 27 (52) 0.1

II 29 (63) 25 (48) 0.1

III 1 (2) 0 0.5

Rochesterclassification

Classic 46 (100) 52 (100) –

Variant 0 0

Esophagram

I 18 (49) 4 (8) <0.001*

II 10 (27) 14 (30) 0.8

III 7 (19) 14 (30) 0.6

IV 2 (5) 15 (32) 0.002*

Not available 9 5

*Statistic significant

Fig. 1 High-resolution manometry plot depicting transition from Chicago type I to Chicago type II

J Gastrointest Surg (2014) 18:221–225 223

communicating vessel and not muscle contraction, since it isunlikely that the muscles are able to contract with the samepressure in all segments at the same time. Also, the presenceof pressure at the transition zone supports this theory.Surprisingly, the degree of esophageal dilatation did not cor-relate to the Chicago types.

Rochester Classification

Galey et al., in 2011,7 described a HRM classification forachalasia in which variants of achalasia are described, andthe pragmatic of “all or nothing” for the esophageal contrac-tility is questioned.

In our study, we found only the classic Rochester type ofachalasia in IA and CDE patients. The variant subtypes maycorrespond to the called undetermined form of CDE.13 Thistype probably corresponds to initial manifestations of dener-vation before complete aperistalsis is manifested. The study ofthis form is easy in Chagas' disease, since patients with thediagnosis of the disease, but free from esophageal symptoms,can be tested. This undetermined form of CDE probablycorresponds to the cases reported by the aforementioned studyby Remes-Troche et al.10 Galey et al.7 were able to describesimilar findings in patients with IA since their study popula-tion consisted in the analysis of all HRM plots from theirinstitution, not only patients with clinical, radiologic, andmanometric diagnosis of achalasia as in our study.

Study Limitations

IA and CDE share several similarities,3,5 but the degree ofdilation is markedly more pronounced in CDE. It may beargued that the comparison of manometric findings betweenIA and CDE is not possible unless groups are matched foresophageal diameter. We believe that the degree of dilatationdoes not make them to be different diseases, but perhapsdifferent stages of evolution of the same disease since CDEpatients have a longer period of the disease before treatment.5

Moreover, the degree of dilatation by esophagram and theChicago classification were not correlated in our series.

Conclusion

Chicago classification for IA may be applied to CDE. Thesecondary findings of our study suggest that HRM classifica-tions may reflect esophageal repletion and pressurization in-stead of muscular contraction.

Rochester classification may be useful in asymptomaticpatients with Chagas' disease.

The correlation between manometric findings and treat-ment outcomes for CDE needs to be answered in a near future.

Acknowledgments Dr. Fernando Vicentine was supported by a grantfrom the Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior(CAPES), a governmental funding agency.

References

1. Patti MG, Herbella FA. Achalasia and other esophageal motility disor-ders. J Gastrointest Surg. 2011; 15: 703–7.

2. Farrokhi F, Vaezi MF. Idiopathic (primary) achalasia. Orphanet JRare Dis. 2007; 2:38–45.

3. Dantas RO. Comparação entre acalásia idiopática e acalásiaconsequente à doença de Chagas: revisão de publicações sobre otema. Arq Gastroenterol. 2003 Abr/Jun; 40 (2): 126–30.

4. Vicentine FP, Herbella FA, Allaix ME, Silva LC, Patti MG. Compari-son of idiopathic achalasia and Chagas' disease esophagopathy at thelight of high resolution manometry. Dis Esophagus. 2013; doi:10.1111/dote.12098

5. Herbella FA, Oliveira DRCF, Del Grande JC. Are idiopathic andchagasic achalasia two different diseases? Dig Dis Sci. 2004; 49(3):353–60.

6. Pandolfino JE, Kwiatek MA, Nealis T, Bulsiewicz W, Post J,Kahrilas PJ. Achalasia: a new clinically relevant classificationby high-resolution manometry. Gastroenterology. 2008;135:1526–33.

7. Galey KM, Wilshire CL, Niebisch S, Jones CE, Raymond DP, LitleVR, Watson TJ, Peters JH. Atypical variants of classic achalasia arecommon and currently under-recognized: a study of prevalence andclinical features. J Am Coll Surg. 2011; 213(1): 155–61.

8. Rezende JM, Lauar KM,OliveiraAR.Aspectos clínicos e radiológicosda aperistalse do esôfago. Rev Bras Gastroenterol. 1960; 12:247–62.

9. Ferreira-Santos R. Tratamento cirúrgico da aperistalse esofágica(megaesôfago). Dissertação. Ribeirão Preto. Univesidade de SãoPaulo, 1965.

10. Remes-Troche JM, Torres-Aguilera M, Antonio-Cruz KA, Vazquez-Jimenez G, De-La-Cruz-Patiño E. Esophageal motor disorders insubjects with incidentally discovered Chagas disease: a study usinghigh-resolution manometry and the Chicago classification. DisEsophagus. 2012 Oct 22. doi: 10.1111/j.1442-2050.2012.01438.x.

11. Todorczuk JR, Aliperti G, Staiano A, Clouse RE. Reevaluation ofmanometric criteria for vigorous achalasia. Is this a distinct clinicaldisorder? Dig Dis Sci. 1991; 36 (3): 274–78.

12. Oliveira RB, Troncon LEA, Dantas RO, Meneghelli UG. Gastroin-testinal manifestations of Chagas' disease. Am J Gastroenterol. 1998;93 (6): 884–89.

13. Sanchez-Lermen RLP, Dick E, Salas JAP, Fontes CJ. Upper gastroin-testinal symptoms and esophageal motility disorders in indeterminateChagas disease patients. Rev. Soc. Bras. Med. Trop. 2007; 40 (2):197–203.

Discussant

Dr. Nathaniel Soper (Chicago, IL, USA): The authors haveapplied the Chicago classification system of HRM, describedby Kahrilas and Pandolfino from Northwestern in 2008, to agroup of patients with either IA or CDE. They found ~50:50distribution of types I and II in CDE. The CDE group had amore dilated esophagus than IA, and there is no type III inCDE. Because of the aganglionosis seen in CDE, one wouldnot expect to see type III.

224 J Gastrointest Surg (2014) 18:221–225

My questions are as follows:1. What was the duration of symptoms in the two groups

prior to HRM?2. You state that there was no correlation between esoph-

ageal dilation and type, yet the p =0.08. Do you think this isdue to small sample size, and have you tried to correlateesophageal pressure with diameter?

3. According to the Chicago classification scheme, types Iand II are often a mix of pressurized readings. The definitionof type I is two or fewer pressurized swallows out of 10, so it isincorrect to state that the nine patients changed from type I toII during the test.

4. Do you think that the type of motility pattern in CDEpatients has any treatment implications?

Closing Discussant

Dr. Fernando Vicentine: Dr. Soper, thank you for yourthoughtful questions.

1. We did not look at the duration of the symptoms. Yourgroup showed 2 days ago that the duration of symptoms is apredictor for bad results with per oral endoscopy myotomy(POEM); however, studies using conventional manometry inCDE patients that had repeated manometry after 3 to 10 yearsdid not show change in the manometry pattern; obviously,Chicago classification was not use at that time.

2. We did correlate the esophageal body pressure with thedegree of esophageal dilatation to other study, and we foundan indirect correlation; that is, the higher the pressure, thelower is the diameter.

3. The patients that changed from Chicago I to Chicago IIwere classified per definition as type II. We highlighted thephenomenon to reinforce the theory that we filled the esoph-agus with water, and this was responsible for the increase inpressure.

Yes, we do believe that the classification may predictoutcomes, since the results for the treatment of IA and CDEhave been the same, but we are now following up our patientsto report, in a near future, conclusions for this question.

J Gastrointest Surg (2014) 18:221–225 225