Skip to main content
SpringerLink
Log in

What role does the submucosa play in the pathophysiology and treatment of achalasia? An analysis of impedance planimetry during POEM

  • 2023 SAGES Oral
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

It is thought the therapeutic benefit of per-oral endoscopic myotomy (POEM) in the treatment of esophageal dysmotility disorders is from longitudinal myotomy creation, but it is unknown if the submucosa contributes to the pathophysiology. This study investigates if submucosal tunnel (SMT) dissection alone contributes to POEM’s luminal changes as measured by EndoFLIP.

Methods

A single-center, retrospective review of consecutive POEM cases from June 1, 2011 to September 1, 2022 with intraoperative luminal diameter and distensibility index (DI) data as measured by EndoFLIP. Patients with diagnoses of achalasia or esophagogastric junction outflow obstruction were grouped by those with pre-SMT and post-myotomy measurements (Group 1) and those with a third measurement post-SMT dissection (Group 2). Outcomes and EndoFLIP data were analyzed using descriptive and univariate statistics.

Results

There were 66 patients identified, of whom 57 (86.4%) had achalasia, 32 (48.5%) were female, and median pre-POEM Eckardt score was 7 [IQR: 6–9]. There were 42 (64%) patients in Group 1, and 24 (36%) patients in Group 2, with no differences in baseline characteristics. In Group 2, SMT dissection changed luminal diameter by 2.15 [IQR: 1.75–3.28]cm, which comprised 38% of the median 5.6 [IQR: 4.25–6.3]cm diameter of complete POEM change. Similarly, the median post-SMT change in DI of 1 [IQR: 0.5–1.2]units comprised 30% of the median 3.35 [2.4–3.98]units overall change in DI. Post-SMT diameters and DI were both significantly lower than the full POEM.

Conclusions

Esophageal diameter and DI are significantly affected by SMT dissection alone, though not equaling the magnitude of diameter or DI changes from full POEM. This suggests that the submucosa does play a role in achalasia, presenting a future target for refining POEM and developing alternative treatment strategies.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

CI:

Confidence interval

DI:

Distensibility index

EGJ:

Esophagogastric junction

EGJOO:

Esophagogastric junction outflow obstruction

EndoFLIP:

Endoluminal functional luminal imaging probe

IQR :

Interquartile range

LES:

Lower esophageal sphincter

LHM:

Laparoscopic Heller myotomy

NAEDD:

Non-achalasia esophageal dysmotility disorders

POEM:

Per-oral endoscopic myotomy

SMT:

Submucosal tunnel

References

  1. Pandolfino JE, Gawron AJ (2015) Achalasia: a systematic review. JAMA 313(18):1841–1852. https://doi.org/10.1001/jama.2015.2996 (PMID: 25965233)

    Article  PubMed  Google Scholar 

  2. Schlottmann F, Neto RML, Herbella FAM, Patti MG (2018) Esophageal achalasia: pathophysiology, clinical presentation, and diagnostic evaluation. Am Surg 84(4):467–472 (PMID: 29712590)

    Article  PubMed  Google Scholar 

  3. Yadlapati R, Kahrilas PJ, Fox MR, Bredenoord AJ, Prakash Gyawali C, Roman S, Babaei A, Mittal RK, Rommel N, Savarino E, Sifrim D, Smout A, Vaezi MF, Zerbib F, Akiyama J, Bhatia S, Bor S, Carlson DA, Chen JW, Cisternas D, Cock C, Coss-Adame E, de Bortoli N, Defilippi C, Fass R, Ghoshal UC, Gonlachanvit S, Hani A, Hebbard GS, Wook Jung K, Katz P, Katzka DA, Khan A, Kohn GP, Lazarescu A, Lengliner J, Mittal SK, Omari T, Park MI, Penagini R, Pohl D, Richter JE, Serra J, Sweis R, Tack J, Tatum RP, Tutuian R, Vela MF, Wong RK, Wu JC, Xiao Y, Pandolfino JE (2021) Esophageal motility disorders on high-resolution manometry: Chicago classification version 4.0©. Neurogastroenterol Motil. 33(1):e14058. https://doi.org/10.1111/nmo.14058

    Article  PubMed  PubMed Central  Google Scholar 

  4. Sadowski DC, Ackah F, Jiang B, Svenson LW (2010) Achalasia: incidence, prevalence and survival: a population-based study. Neurogastroenterol Motil 22(9):e256–e261. https://doi.org/10.1111/j.1365-2982.2010.01511.x (Epub 2010 May 11 PMID: 20465592)

    Article  CAS  PubMed  Google Scholar 

  5. Scherer JR, Kwiatek MA, Soper NJ, Pandolfino JE, Kahrilas PJ (2009) Functional esophagogastric junction obstruction with intact peristalsis: a heterogeneous syndrome sometimes akin to achalasia. J Gastrointest Surg. 13(12):2219–2225. https://doi.org/10.1007/s11605-009-0975-7

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kroch DA, Grimm IS (2018) POEM for achalasia. Am Surg 84(4):489–495 (PMID: 29712594)

    Article  PubMed  Google Scholar 

  7. Zaninotto G, Bennett C, Boeckxstaens G, Costantini M, Ferguson MK, Pandolfino JE, Patti MG, Ribeiro U Jr, Richter J, Swanstrom L, Tack J, Triadafilopoulos G, Markar SR, Salvador R, Faccio L, Andreollo NA, Cecconello I, Costamagna G, da Rocha JRM, Hungness ES, Fisichella PM, Fuchs KH, Gockel I, Gurski R, Gyawali CP, Herbella FAM, Holloway RH, Hongo M, Jobe BA, Kahrilas PJ, Katzka DA, Dua KS, Liu D, Moonen A, Nasi A, Pasricha PJ, Penagini R, Perretta S, Sallum RAA, Sarnelli G, Savarino E, Schlottmann F, Sifrim D, Soper N, Tatum RP, Vaezi MF, van Herwaarden-Lindeboom M, Vanuytsel T, Vela MF, Watson DI, Zerbib F, Gittens S, Pontillo C, Vermigli S, Inama D, The LDE (2018) ISDE achalasia guidelines. Dis Esophagus. https://doi.org/10.1093/dote/doy071

    Article  PubMed  Google Scholar 

  8. Eckardt AJ, Eckardt VF (2011) Treatment and surveillance strategies in achalasia: an update. Nat Rev Gastroenterol Hepatol 8(6):311–319. https://doi.org/10.1038/nrgastro.2011.68 (Epub 2011 Apr 26 PMID: 21522116)

    Article  PubMed  Google Scholar 

  9. Ehlers AP, Oelschlager BK, Pellegrini CA, Wright AS, Saunders MD, Flum DR, He H, Farjah F (2017) Achalasia treatment, outcomes, utilization, and costs: a population-based study from the United States. J Am Coll Surg. 225(3):380–386. https://doi.org/10.1016/j.jamcollsurg.2017.05.014

    Article  PubMed  PubMed Central  Google Scholar 

  10. Horgan S, Hudda K, Eubanks T, McAllister J, Pellegrini CA (1999) Does botulinum toxin injection make esophagomyotomy a more difficult operation? Surg Endosc 13:576–579

    Article  CAS  PubMed  Google Scholar 

  11. Swanström LL (2019) Achalasia: treatment, current status and future advances. Korean J Intern Med 34(6):1173–1180. https://doi.org/10.3904/kjim.2018.439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cheng JW, Li Y, Xing WQ, Ly HW, Wang HR (2017) Laparoscopic Heller myotomy is not superior to pneumatic dilation in the management of primary achalasia: conclusions of a systematic review and meta-analysis of randomized controlled trials. Medicine 96:e5525

    Article  PubMed  PubMed Central  Google Scholar 

  13. Schlottmann F, Patti MG (2018) Esophageal achalasia: current diagnosis and treatment. Expert Rev Gastroenterol Hepatol 12(7):711–721

    Article  CAS  PubMed  Google Scholar 

  14. Filicori F, Dunst CM, Sharata A, Abdelmoaty WF, Zihni AM, Reavis KM, Demeester SR, Swanström LL (2019) Long-term outcomes following POEM for non-achalasia motility disorders of the esophagus. Surg Endosc 33:1632–1639. https://doi.org/10.1007/s00464-018-6438-z

    Article  PubMed  Google Scholar 

  15. Bernardot L, Roman S, Barret M, Vitton V, Wallenhorst T, Pioche M, Chaussade S, Gonzalez J-M, Ponchon T, Prat F, Barthet M, Vergniol J, Chabrun E, Zerbib F (2020) Efficacy of per-oral endoscopic myotomy for the treatment of non-achalasia esophageal motor disorders. Surg Endosc 34:5508–5515. https://doi.org/10.1007/s00464-019-07348-y

    Article  PubMed  Google Scholar 

  16. Khashab MA, Familiari P, Draganov PV, Aridi HD, Cho JY, Ujiki M, Rio Tinto R, Louis H, Desai PN, Velanovich V, Albéniz E, Haji A, Marks J, Costamagna G, Devière J, Perbtani Y, Hedberg M, Estremera F, Martin Del Campo LA, Yang D, Bukhari M, Brewer O, Sanaei O, Fayad L, Agarwal A, Kumbhari V, Chen Y-I (2018) Peroral endoscopic myotomy is effective and safe in non-achalasia esophageal motility disorders: an international multicenter study. Endosc Int Open 6:E1031–E1036. https://doi.org/10.1055/a-0625-6288

    Article  PubMed  PubMed Central  Google Scholar 

  17. Morley TJ, Mikulski MF, Rade M, Chalhoub J, Desilets DJ, Romanelli JR (2022) Per-oral endoscopic myotomy for the treatment of non-achalasia esophageal dysmotility disorders: experience from a single high-volume center. Surg Endosc. https://doi.org/10.1007/s00464-022-09596-x

    Article  PubMed  Google Scholar 

  18. Inoue H, Minami H, Kobayashi Y, Sato Y, Kaga M, Suzuki M, Satodate H, Odaka N, Itoh H, Kudo S (2010) Peroral endoscopic myotomy (POEM) for esophageal achalasia. Endoscopy 42:265–271. https://doi.org/10.1055/s-0029-1244080

    Article  CAS  PubMed  Google Scholar 

  19. Inoue H, Sato H, Ikeda H, Onimaru M, Sato C, Minami H, Yokomichi H, Kobayashi Y, Grimes KL, Kudo S (2015) Per-oral endoscopic myotomy: a series of 500 patients. J Am Coll Surg 221:256–264. https://doi.org/10.1016/j.jamcollsurg.2015.03.057

    Article  PubMed  Google Scholar 

  20. Park CH, Jung DH, Kim DH, Lim C-H, Moon HS, Park JH, Jung H-K, Hong SJ, Choi SC, Lee OY et al (2019) Comparative efficacy of per-oral endoscopic myotomy and Heller myotomy in patients with achalasia: a meta-analysis. Gastrointest Endosc 90:546–558. https://doi.org/10.1016/j.gie.2019.05.046

    Article  PubMed  Google Scholar 

  21. Sanaka MR, Hayat U, Thota PN, Jegadeesan R, Ray M, Gabbard SL, Wadhwa N, Lopez R, Baker ME, Murthy S, Raja S (2016) Efficacy of peroral endoscopic myotomy vs other achalasia treatments in improving esophageal function. World J Gastroenterol 22:4918–4925. https://doi.org/10.3748/wjg.v22.i20.4918

    Article  PubMed  PubMed Central  Google Scholar 

  22. American Society for Gastrointestinal Endoscopy PIVI Committee, Chandrasekhara V, Desilets D, Falk GW, Inoue H, Romanelli JR, Savides TJ, Stavropoulos SN, Swanstrom LL (2015) The American society for gastrointestinal endoscopy PIVI (preservation and incorporation of valuable endoscopic innovations) on peroral endoscopic myotomy. Gastrointest Endosc 81:1087-1100.e1. https://doi.org/10.1016/j.gie.2014.12.007

    Article  Google Scholar 

  23. Patel K, Abbassi-Ghadi N, Markar S, Kumar S, Jethwa P, Zaninotto G (2016) Peroral endoscopic myotomy for the treatment of esophageal achalasia: systematic review and pooled analysis. Dis Esophagus Off J Int Soc Dis Esophagus 29:807–819. https://doi.org/10.1111/dote.12387

    Article  CAS  Google Scholar 

  24. Pandolfino JE, de Ruigh A, Nicodème F, Xiao Y, Boris L, Kahrilas PJ (2013) Distensibility of the esophagogastric junction assessed with the functional lumen imaging probe (FLIP™) in achalasia patients. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc 25:496–501. https://doi.org/10.1111/nmo.12097

    Article  CAS  Google Scholar 

  25. Rieder E, Swanström LL, Perretta S, Lenglinger J, Riegler M, Dunst CM (2013) Intraoperative assessment of esophagogastric junction distensibility during per oral endoscopic myotomy (POEM) for esophageal motility disorders. Surg Endosc 27:400–405. https://doi.org/10.1007/s00464-012-2484-0

    Article  PubMed  Google Scholar 

  26. Kahrilas PJ, Bredenoord AJ, Fox M, Gyawali CP, Roman S, Smout AJ, Pandolfino JE et al (2015) The Chicago classification of esophageal motility disorders, v3.0. Neurogastroenterol Motil 27(2):160–174

    Article  CAS  PubMed  Google Scholar 

  27. Kane ED, Desilets DJ, Wilson D, Leduc M, Budhraja V, Romanelli JR (2018) Treatment of achalasia with per-oral endoscopic myotomy: analysis of 50 consecutive patients. J Laparoendosc Adv Surg Tech A 28:514–525. https://doi.org/10.1089/lap.2017.0588SuB

    Article  PubMed  Google Scholar 

  28. Callahan ZM, Novak S, Kuchta K, Ujiki MB (2020) Using impedance planimetry (EndoFLIP) to evaluate myotomy and predict outcomes after surgery for achalasia. J Gastrointest Surg Off J Soc Surg Aliment Tract 24:964–971. https://doi.org/10.1007/s11605-020-04513-w

    Article  Google Scholar 

  29. R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  30. Jain AS, Carlson DA, Triggs J, Tye M, Kou W, Campagna R, Hungness E, Kim D, Kahrilas PJ, Pandolfino JE (2019) Esophagogastric junction distensibility on functional lumen imaging probe topography predicts treatment response in achalasia-anatomy matters! Am J Gastroenterol 114(9):1455–1463. https://doi.org/10.14309/ajg.0000000000000137.PMID:30741739;PMCID:PMC6682473

    Article  PubMed  PubMed Central  Google Scholar 

  31. Teitelbaum EN, Soper NJ, Pandolfino JE, Kahrilas PJ, Hirano I, Boris L, Nicodème F, Lin Z, Hungness ES (2015) Esophagogastric junction distensibility measurements during Heller myotomy and POEM for achalasia predict postoperative symptomatic outcomes. Surg Endosc. 29(3):522–528. https://doi.org/10.1007/s00464-014-3733-1

    Article  PubMed  Google Scholar 

  32. Teitelbaum EN, Soper NJ, Pandolfino JE, Kahrilas PJ, Boris L, Nicodème F, Lin Z, Hungness ES (2014) An extended proximal esophageal myotomy is necessary to normalize EGJ distensibility during Heller myotomy for achalasia, but not POEM. Surg Endosc. 28(10):2840–2847. https://doi.org/10.1007/s00464-014-3563-1

    Article  PubMed  PubMed Central  Google Scholar 

  33. Knowles TB, Jackson AS, Chang SC, Schembre DB, Farivar AS, Aye RW, Louie BE (2022) Changes in distensibility index during an incremental POEM myotomy. J Gastrointest Surg 26(6):1140–1146. https://doi.org/10.1007/s11605-022-05278-0 (Epub 2022 Mar 1 PMID: 35233701)

    Article  PubMed  Google Scholar 

  34. Holmstrom AL, Campagna RAJ, Alhalel J, Carlson DA, Pandolfino JE, Hungness ES, Teitelbaum EN (2021) Intraoperative FLIP distensibility during POEM varies according to achalasia subtype. Surg Endosc 35(6):3097–3103. https://doi.org/10.1007/s00464-020-07740-z (Epub 2020 Jun 29 PMID: 32601759)

    Article  PubMed  Google Scholar 

  35. Fujiyoshi Y, Inoue H, Fujiyoshi MRA, de Rodriguez Santiago E, Nishikawa Y, Toshimori A, Tanabe M, Shimamura Y, Sumi K, Ono M, Shiwaku H, Ikeda H, Onimaru M (2023) Learning curve for peroral endoscopic myotomy in therapeutic endoscopy experts and nonexperts: large single-center experience. Dig Endosc. 35(3):323–331. https://doi.org/10.1111/den.14435

    Article  PubMed  Google Scholar 

  36. Lv H, Zhao N, Zheng Z, Wang T, Yang F, Jiang X, Lin L, Sun C, Wang B (2017) Analysis of the learning curve for peroral endoscopic myotomy for esophageal achalasia: single-center, two-operator experience. Dig Endosc 29(3):299–306. https://doi.org/10.1111/den.12763 (Epub 2017 Jan 12 PMID: 27859721)

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

None.

Funding

There was no internal or external funding for this project.

Author information

Authors and Affiliations

  1. Department of Surgery, University of Massachusetts Chan Medical School, Baystate Medical Center, Surgery Education Office, 759 Chestnut Street, Springfield, MA, 01199, USA

    Timothy J. Morley, Matthew F. Mikulski, Alicja Zalewski & John R. Romanelli

  2. Department of Gastroenterology, University of Massachusetts Chan Medical School-Baystate, Springfield, MA, USA

    David J. Desilets

Authors
  1. Timothy J. Morley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew F. Mikulski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alicja Zalewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David J. Desilets
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John R. Romanelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy J. Morley.

Ethics declarations

Disclosures

John R. Romanelli receives research funding from Davol, and consulting fees from New View Surgical. Timothy J. Morley, Matthew F. Mikulski, Alicja Zalewski, and David J. Desilets report no conflicts of interests or financial ties to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Previous presentation: Data from this work was accepted for presentation at the Society of American Gastrointestinal and Endoscopic Surgeons 2023 Annual Meeting, Montreal, QC, Canada, March 2023.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morley, T.J., Mikulski, M.F., Zalewski, A. et al. What role does the submucosa play in the pathophysiology and treatment of achalasia? An analysis of impedance planimetry during POEM. Surg Endosc 37, 7923–7932 (2023). https://doi.org/10.1007/s00464-023-10260-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-023-10260-1

Keywords

Search

Navigation