Skip to main content

Advertisement

Log in

Hiatal hernia and gastroesophageal reflux: Study of collagen in the phrenoesophageal ligament

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Gastroesophageal reflux disease (GERD) is defined by the intensity and/or quality of the reflux of gastric or duodenal contents into the esophagus. Surgical treatment of GERD has shown conflicting results and unacceptable recurrence rates, mainly due to herniation of the antireflux valve into the chest. A variety of techniques has been proposed to reduce GERD recurrence, including routine use of prosthesis in cruroplasty. The prevalence of GERD in patients with hiatal hernia (HH) can reach 94 %. It is possible that the phrenoesophageal ligament (POL) engaged in the stabilization of the gastroesophageal junction in the abdomen may be an etiological factor of HH. We conducted a study to evaluate collagen in the constitution of the POL in patients with HH and cadavers without HH.

Methods

POL samples were collected from 29 patients with HH and GERD (cases) and 32 samples from cadavers without HH (controls). Total collagen was quantified through the Picrosirius red histochemical technique, and type-I and type-III collagens were quantified immunohistochemically using a monoclonal antibody. The stained slides were photographed, and images were quantified by computer software (Image Pro Plus) to count the pixels per field.

Results

The mean age was 49.5 (±11.5) years for the cases and 38.5 (±13) years for the controls (p < 0.01). Seventeen cases (58.6 %) and six controls (18.75 %) were female (p < 0.01). The quantity of total (p < 0.01), type-I (p < 0.01), and type-III (p < 0.05) collagens was significantly lower by about 60 % in patients with HH compared with controls.

Conclusion

Our data indicate that the composition of POL for patients with GERD and HH includes less total, type-I, and type-III collagens than that of the POL of cadavers without HH. The quality of the POL may be an etiological factor in the development of HH.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Moraes-Filho JP, Navarro-Rodriguez T, Barbuti R, Eisig J, Chinzon D, Bernardo W, Brazilian Gerd Consensus Group (2010) Guidelines for the diagnosis and management of gastroesophageal reflux disease: an evidence-based consensus. Arq Gastroenterol 47:99–115

    Article  PubMed  Google Scholar 

  2. Talalwah NA, Woodward S (2013) Gastro-oesophageal reflux. Part 3: medical and surgical treatment. Br J Nurs 22:409–415

    Article  PubMed  Google Scholar 

  3. El Sherif A, Yano F, Mittal S, Filipi CJ (2006) Collagen metabolism and recurrent hiatal hernia: cause and effect? Hernia 10:511–520

    Article  PubMed  Google Scholar 

  4. Kahrilas PJ, Shaheen NJ, Vaezi MF, Hiltz SW, Black E, Modlin IM, Johnson SP, Allen J, Brill JV, American Gastroenterological Association (2008) American Gastroenterological Association Medical Position Statement on the management of gastroesophageal reflux disease. Gastroenterology 135:1383–1391 1391.e1-5

    Article  PubMed  Google Scholar 

  5. Asling B, Jirholt J, Hammond P, Knutsson M, Walentinsson A, Davidson G, Agreus L, Lehmann A, Lagerström-Fermer M (2009) Collagen type III alpha I is a gastro-oesophageal reflux disease susceptibility gene and a male risk factor for hiatus hernia. Gut 58:1063–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Dent J, El-Serag HB, Wallander MA, Johansson S (2005) Epidemiology of gastro-oesophageal reflux disease: a systematic review. Gut 54:710–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Cohen E, Bolus R, Khanna D, Hays RD, Chang L, Melmed GY, Khanna P, Spiegel B (2014) GERD symptoms in the general population: prevalence and severity versus care-seeking patients. Dig Dis Sci 59:2488–2496

    Article  PubMed  PubMed Central  Google Scholar 

  8. Spechler SJ, Lee E, Ahnen D, Goyal RK, Hirano I, Ramirez F, Raufman JP, Sampliner R, Schnell T, Sontag S, Vlahcevic ZR, Young R, Williford W (2001) Long-term outcome of medical and surgical therapies for gastroesophageal reflux disease: follow-up of a randomized controlled trial. JAMA 285:2331–2338

    Article  CAS  PubMed  Google Scholar 

  9. El-Serag HB, Petersen NJ, Carter J, Graham DY, Richardson P, Genta RM, Rabeneck L (2004) Gastroesophageal reflux among different racial groups in the United States. Gastroenterology 126:1692–1699

    Article  PubMed  Google Scholar 

  10. Butin JW, Olsen AM, Moersch HJ, Code CF (1953) A study of esophageal pressures in normal persons and patients with cardiospasm. Gastroenterology 23:278–293

    CAS  PubMed  Google Scholar 

  11. Novais L (2012) Avaliação funcional do esfíncter esofágico inferior por manometria esofágica. Jornal Português de Gastrenterologia 19:59–61

    Google Scholar 

  12. Ireland AC, Holloway RH, Toouli J, Dent J (1993) Mechanisms underlying the antireflux action of fundoplication. Gut 34:303–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Little AG (1992) Mechanisms of action of antireflux surgery: theory and fact. World J Surg 16:320–325

    Article  CAS  PubMed  Google Scholar 

  14. Henry MA (2014) Diagnosis and management of gastroesophageal reflux disease. Arq Bras Cir Dig 27:210–215

    Article  PubMed  PubMed Central  Google Scholar 

  15. Carlson MA, Frantzides CT (2001) Complications and results of primary minimally invasive antireflux procedures: a review of 10,735 reported cases. J Am Coll Surg 193:428–439

    Article  CAS  PubMed  Google Scholar 

  16. Contini S, Scarpignato C (2011) Evaluation of clinical outcome after laparoscopic antireflux surgery in clinical practice: still a controversial issue. Minim Invasive Surg 2011:725472

    PubMed  PubMed Central  Google Scholar 

  17. Kelly JJ, Watson DI, Chin KF, Devitt PG, Game PA, Jamieson GG (2007) Laparoscopic Nissen fundoplication: clinical outcomes at 10 years. J Am Coll Surg 205:570–575

    Article  PubMed  Google Scholar 

  18. Ludwig K, Bernhardt J, Amtsberg G, Patrzyk M, Wilhelm L, Hoene A (2003) Pathophysiological measurement and results after laparoscopic fundoplication for gastroesophageal reflux disease. Surg Today 33:89–94

    Article  PubMed  Google Scholar 

  19. Braghetto I, Korn O, Csendes A, Valladares H, Davanzo C, Debandi A (2012) Radiologic and endoscopic characteristics of laparoscopic antireflux wrap: correlation with outcome. Int Surg 97:189–197

    Article  PubMed  PubMed Central  Google Scholar 

  20. Granderath FA, Granderath UM, Pointner R (2008) Laparoscopic revisional fundoplication with circular hiatal mesh prosthesis: the long-term results. World J Surg 32:999–1007

    Article  CAS  PubMed  Google Scholar 

  21. Granderath FA, Carlson MA, Champion JK, Szold A, Basso N, Pointner R, Frantzides CT (2006) Prosthetic closure of the esophageal hiatus in large hiatal hernia repair and laparoscopic antireflux surgery. Surg Endosc 20:367–379

    Article  CAS  PubMed  Google Scholar 

  22. Trindade EN, Boza JC, Trindade MR (2007) Laparoscopic paraesophageal hernia mesh repair. Surgery 141:692–693

    Article  PubMed  Google Scholar 

  23. Trindade EN, Trindade MR (2008) Antireflux surgery with routine mesh hiatoplasty. World J Surg 32:328 329–330

    Article  PubMed  Google Scholar 

  24. Antoniou SA, Pointner R, Granderath FA (2011) Hiatal hernia repair with the use of biologic meshes: a literature review. Surg Laparosc Endosc Percutan Tech 21:1–9

    Article  PubMed  Google Scholar 

  25. Antoniou SA, Antoniou GA, Koch OO, Pointner R, Granderath FA (2012) Lower recurrence rates after mesh-reinforced versus simple hiatal hernia repair: a meta-analysis of randomized trials. Surg Laparosc Endosc Percutan Tech 22:498–502

    Article  PubMed  Google Scholar 

  26. Bell RC, Fearon J, Freeman KD (2013) Allograft dermal matrix hiatoplasty during laparoscopic primary fundoplication, paraesophageal hernia repair, and reoperation for failed hiatal hernia repair. Surg Endosc 27:1997–2004

    Article  PubMed  PubMed Central  Google Scholar 

  27. Curci JA, Melman LM, Thompson RW, Soper NJ, Matthews BD (2008) Elastic fiber depletion in the supporting ligaments of the gastroesophageal junction: a structural basis for the development of hiatal hernia. J Am Coll Surg 207(2):191–196

    Article  PubMed  Google Scholar 

  28. Fei L, del Genio G, Rossetti G, Sampaolo S, Moccia F, Trapani V, Cimmino M, del Genio A (2009) Hiatal hernia recurrence: surgical complication or disease? Electron microscope findings of the diaphragmatic pillars. J Gastrointest Surg 13:459–464

    Article  PubMed  Google Scholar 

  29. Kwok H, Marriz Y, Al-Ali S, Windsor JA (1999) Phrenoesophageal ligament re-visited. Clin Anat 12:164–170

    Article  CAS  PubMed  Google Scholar 

  30. Schumpelick V (2006) Special issue—Collagen. Hernia 10:453

    Article  Google Scholar 

  31. Brown SR, Melman L, Jenkins E, Deeken C, Frisella MM, Brunt LM, Eagon JC, Matthews BD (2011) Collagen type I:III ratio of the gastroesophageal junction in patients with paraesophageal hernias. Surg Endosc 25:1390–1394

    Article  PubMed  Google Scholar 

  32. Weber C, Davis CS, Shankaran V, Fisichella PM (2011) Hiatal hernias: a review of the pathophysiologic theories and implication for research. Surg Endosc 25:3149–3153

    Article  CAS  PubMed  Google Scholar 

  33. Baktir A, Dogru O, Girgin M, Aygen E, Kanat BH, Dabak DO, Kuloglu T (2013) The effects of different prosthetic materials on the formation of collagen types in incisional hernia. Hernia 17:249–253

    Article  CAS  PubMed  Google Scholar 

  34. Zheng H, Si Z, Kasperk R, Bhardwaj RS, Schumpelick V, Klinge U, Klosterhalfen B (2002) Recurrent inguinal hernia: disease of the collagen matrix? World J Surg 26:401–408

    Article  PubMed  Google Scholar 

  35. Wolwacz Júnior I, Trindade MRM, Cerski CT (2003) O colágeno em fáscia transversal de pacientes com hérnia inguinal direta submetidos à videolaparoscopia. Acta Cirurgica Brasileira 18:196–202

    Article  Google Scholar 

  36. Casanova AB, Trindade EN, Trindade MR (2009) Collagen in the transversalis fascia of patients with indirect inguinal hernia: a case-control study. Am J Surg 198:1–5

    Article  PubMed  Google Scholar 

  37. Fachinelli A, Maciel Trindade MR (2007) Qualitative and quantitative evaluation of total and types I and III collagens in patients with ventral hernias. Langenbecks Arch Surg 392:459–464

    Article  PubMed  Google Scholar 

  38. Bahn S, Augood SJ, Ryan M, Standaert DG, Starkey M, Emson PC (2001) Gene expression profiling in the post-mortem human brain–no cause for dismay. J Chem Neuroanat 22:79–94

    Article  CAS  PubMed  Google Scholar 

  39. Cummings TJ, Strum JC, Yoon LW, Szymanski MH, Hulette CM (2001) Recovery and expression of messenger RNA from postmortem human brain tissue. Mod Pathol 14:1157–1161

    Article  CAS  PubMed  Google Scholar 

  40. De Paepe ME, Mao Q, Huang C, Zhu D, Jackson CL, Hansen K (2002) Postmortem RNA and protein stability in perinatal human lungs. Diagn Mol Pathol 11:170–176

    Article  PubMed  Google Scholar 

  41. Noutsias M, Seeberg B, Schultheiss HP, Kuhl U (1999) Expression of cell adhesion molecules in dilated cardiomyopathy: evidence for endothelial activation in inflammatory cardiomyopathy. Circulation 99:2124–2131

    Article  CAS  PubMed  Google Scholar 

  42. Pelstring RJ, Allred DC, Esther RJ, Lampkin SR, Banks PM (1991) Differential antigen preservation during tissue autolysis. Hum Pathol 22:237–241

    Article  CAS  PubMed  Google Scholar 

  43. Maleszewski J, Lu J, Fox-Talbot K, Halushka MK (2007) Robust immunohistochemical staining of several classes of proteins in tissues subjected to autolysis. J Histochem Cytochem 55:597–606

    Article  CAS  PubMed  Google Scholar 

  44. Fei L, del Genio G, Brusciano L, Esposito V, Cuttitta D, Pizza F, Rossetti G, Trapani V, Filippone G, Moccia F, del Genio A (2007) Crura ultrastructural alterations in patients with hiatal hernia: a pilot study. Surg Endosc 21:907–911

    Article  Google Scholar 

  45. Fei L, Rossetti G, Allaria A, Conzo G, Sampaolo S, Moccia F, Bondanese MC, Pascotto B (2013) Laparoscopic hiatal hernia repair. Is the mesh hiatoplasty justified? Ann Ital Chir 85:38–44

    Google Scholar 

  46. Townsend JCM, Beauchamp RD, Evers BM, Mattox KL (2012) Sabiston textbook of surgery—the biological basis of modern surgical practice, 19th edn. Saunders, Philadelphia

    Google Scholar 

  47. Ardeleanu V, Chebac GR, Georgescu C, Vesa D, Frâncu L, Frîncu LD, Păduraru D (2010) The modifications suffered by the peri-esophageal anatomical structures in the hiatal hernia disease: a qualitative and quantitative microanatomic study. Rom J Morphol Embryol 51:765–770

    CAS  PubMed  Google Scholar 

  48. Secretti T (2009) Distribuição dos homicídios em Porto Alegre, Rio Grande do Sul, 2007: contexto sócio-espacial e fatores determinantes. Masters dissertation, Universidade Federal do Rio Grande do Sul, Porto Alegre

  49. Calvi EN, Nahas FX, Barbosa MV, Calil JA, Ihara SS, Juliano Y, Ferreira LM (2014) Collagen fibers in the rectus abdominis muscle of cadavers of different age. Hernia 18:527–533

    Article  CAS  PubMed  Google Scholar 

  50. Sorensen LT (2006) Effect of lifestyle, gender and age on collagen formation and degradation. Hernia 10:456–461

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was funded by the Research and Events Incentive Fund (FIPE) of the Hospital de Clinicas of Porto Alegre. We thank Drª Luise Meurer for analysis of biopsies of this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. von Diemen.

Ethics declarations

Disclosures

Dr. Vinicius von Diemen, Dr. Eduardo N. Trindade, and Dr. Manoel R. M. Trindade have no conflicts of interest or financial ties to disclose.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

von Diemen, V., Trindade, E.N. & Trindade, M.R.M. Hiatal hernia and gastroesophageal reflux: Study of collagen in the phrenoesophageal ligament. Surg Endosc 30, 5091–5098 (2016). https://doi.org/10.1007/s00464-016-4858-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-016-4858-1

Keywords

Navigation