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.
Similar content being viewed by others
References
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
Talalwah NA, Woodward S (2013) Gastro-oesophageal reflux. Part 3: medical and surgical treatment. Br J Nurs 22:409–415
El Sherif A, Yano F, Mittal S, Filipi CJ (2006) Collagen metabolism and recurrent hiatal hernia: cause and effect? Hernia 10:511–520
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
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
Dent J, El-Serag HB, Wallander MA, Johansson S (2005) Epidemiology of gastro-oesophageal reflux disease: a systematic review. Gut 54:710–717
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
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
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
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
Novais L (2012) Avaliação funcional do esfíncter esofágico inferior por manometria esofágica. Jornal Português de Gastrenterologia 19:59–61
Ireland AC, Holloway RH, Toouli J, Dent J (1993) Mechanisms underlying the antireflux action of fundoplication. Gut 34:303–308
Little AG (1992) Mechanisms of action of antireflux surgery: theory and fact. World J Surg 16:320–325
Henry MA (2014) Diagnosis and management of gastroesophageal reflux disease. Arq Bras Cir Dig 27:210–215
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
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
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
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
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
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
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
Trindade EN, Boza JC, Trindade MR (2007) Laparoscopic paraesophageal hernia mesh repair. Surgery 141:692–693
Trindade EN, Trindade MR (2008) Antireflux surgery with routine mesh hiatoplasty. World J Surg 32:328 329–330
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
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
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
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
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
Kwok H, Marriz Y, Al-Ali S, Windsor JA (1999) Phrenoesophageal ligament re-visited. Clin Anat 12:164–170
Schumpelick V (2006) Special issue—Collagen. Hernia 10:453
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
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
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
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
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
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
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
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
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
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
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
Pelstring RJ, Allred DC, Esther RJ, Lampkin SR, Banks PM (1991) Differential antigen preservation during tissue autolysis. Hum Pathol 22:237–241
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
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
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
Townsend JCM, Beauchamp RD, Evers BM, Mattox KL (2012) Sabiston textbook of surgery—the biological basis of modern surgical practice, 19th edn. Saunders, Philadelphia
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
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
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
Sorensen LT (2006) Effect of lifestyle, gender and age on collagen formation and degradation. Hernia 10:456–461
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
Corresponding author
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
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-016-4858-1