Skip to main content

Advertisement

SpringerLink
Log in

Analysis of collagen-interacting proteins in patients with incisional hernias

  • Original Article
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Background

In recent years a disorder of the collagen metabolism has been suggested for the pathogenesis of abdominal wall hernias. Previous investigations of skin specimens revealed a reduction in the collagen I/III ratio and alterations in matrix metalloproteinases in patients with incisional hernias. We investigated known collagen-interacting proteins to further characterize connective tissue in these patients.

Patients and methods

Skin scars from patients with either primary or recurrent incisional and recurrent inguinal hernias, as a subgroup of incisional hernias, were analyzed for overall collagen content and for the distribution of collagen types I and III by crosspolarization microscopy. The expression of collagen type V, collagen receptor discoidin domain receptor 2, matrix metalloproteinase 1, connective tissue-like growth factor, and tenascin was determined by immunohistochemistry. Mature abdominal skin scars from patients without evident hernia served as controls.

Results

Patients with recurrent incisional hernia showed lowest ratios of collagen types I to III. Contents of overall collagen and of collagen type V did not differ between the groups. In patients with either primary or recurrent incisional hernias the proportion of collagen receptor discoidin domain receptor 2 positive cells was increased. Matrix metalloproteinase 1 expression was more pronounced in patients with recurrent incisional or inguinal hernias than in controls. Connective tissue-like growth factor was significantly increased in recurrent inguinal hernia patients. The expression of tenascin was notably decreased in all hernia groups.

Conclusions

The observed alterations in the expression of collagen-interacting proteins again indicate the possibility of a fundamental connective tissue disease as the causal factor in the pathogenesis of (recurrent) incisional hernias.

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.

Similar content being viewed by others

References

  1. Girotto JA, Malaisrie SC, Bulkely G, Manson PN (2000) Recurrent ventral herniation in Ehlers-Danlos syndrome. Plast Reconstr Surg 106:1520–1526

    CAS  PubMed  Google Scholar 

  2. Liem MS, van der Graaf Y, Beemer FA, van Vroonhoven TJ (1997) Increased risk for inguinal hernia in patients with Ehlers-Danlos syndrome. Surgery 122:114–115

    CAS  PubMed  Google Scholar 

  3. Uitto J, Perejda A (eds) (1986) Connective tissue disease: molecular pathology of the extracellular matrix. Dekker, New York

    Google Scholar 

  4. Uden A, Lindhagen T (1988) Inguinal hernia in patients with congenital dislocation of the hip. A sign of general connective tissue disorder. Acta Orthop Scand 59:667–668

    CAS  PubMed  Google Scholar 

  5. Carr AJ, Chiodo AA, Hilton JM, Chow CW, Hockey A, Cole WG (1994) The clinical features of Ehlers-Danlos syndrome type VIIB resulting from a base substitution at the splice acceptor site of intron 5 of the COL1A2 gene. J Med Genet 31:306–311

    CAS  PubMed  Google Scholar 

  6. Adye B, Luna G (1998) Incidence of abdominal wall hernia in aortic surgery. Am J Surg 175:400–402

    CAS  PubMed  Google Scholar 

  7. Hall KA, Peters B, Smyth SH, Warneke JA, Rappaport WD, Putnam CW, Hunter GC (1995) Abdominal wall hernias in patients with abdominal aortic aneurysmal versus aortoiliac occlusive disease. Am J Surg 170:572–575

    Article  CAS  PubMed  Google Scholar 

  8. Pleumeekers HJ, De Gruijl A, Hofman A, Van Beek AJ, Hoes AW (1999) Prevalence of aortic aneurysm in men with a history of inguinal hernia repair. Br J Surg 86:1155–1158

    Article  CAS  PubMed  Google Scholar 

  9. Papadimitriou D, Pitoulias G, Papaziogas B, Koutsias S, Vretzakis G, Argiriadou H, Papaziogas T (2002) Incidence of abdominal wall hernias in patients undergoing aortic surgery for aneurysm or occlusive disease. Vasa 31:111–114

    CAS  PubMed  Google Scholar 

  10. Klinge U, Si ZY, Zheng H, Schumpelick V, Bhardwaj RS, Klosterhalfen B (2000) Abnormal collagen I to III distribution in the skin of patients with incisional hernia. Eur Surg Res 32:43–48

    Article  CAS  PubMed  Google Scholar 

  11. Klinge U, Si ZY, Zheng H, Schumpelick V, Bhardwaj RS, Klosterhalfen B (2001) Collagen I/III and matrix metalloproteinases (MMP) 1 and 13 in the fascia of patients with incisional hernias. J Invest Surg 14:47–54

    Article  CAS  PubMed  Google Scholar 

  12. Si Z, Rhanjit B, Rosch R, Rene PM, Klosterhalfen B, Klinge U (2002) Impaired balance of type I and type III procollagen mRNA in cultured fibroblasts of patients with incisional hernia. Surgery 131:324–331

    Article  PubMed  Google Scholar 

  13. 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 

  14. Witte MB, Thornton FJ, Kiyama T, Efron DT, Schulz GS, Moldawer LL, Barbul A (1998) Metalloproteinase inhibitors and wound healing: a novel enhancer of wound strength. Surgery 124:464–470

    CAS  PubMed  Google Scholar 

  15. Linsenmayer TF, Gibney E, Igoe F, Gordon MK, Fitch JM, Fessler LI, Birk DE (1993) Type V collagen: molecular structure and fibrillar organization of the chicken alpha 1 (V) NH2-terminal domain, a putative regulator of corneal fibrillogenesis. J Cell Biol 121:1181–1189

    CAS  PubMed  Google Scholar 

  16. Marchant JK, Hahn RA, Linsenmayer TF, Birk DE (1996) Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of corneal-specific fibril morphology. J Cell Biol 135:1415–1426

    CAS  PubMed  Google Scholar 

  17. Andrikopoulos K, Liu X, Keene DR, Jaenisch R, Ramirez F (1995) Targeted mutation in the col5a2 gene reveals a regulatory role for type V collagen during matrix assembly. Nat Genet 9:31–36

    PubMed  Google Scholar 

  18. Schwarze U, Atkinson M, Hoffman GG, Greenspan DS, Byers PH (2000) Null alleles of the COL5A1 gene of type V collagen are a cause of the classical forms of Ehlers-Danlos syndrome (types I and II). Am J Hum Genet 66:1757–1765

    Article  CAS  PubMed  Google Scholar 

  19. Wenstrup RJ, Florer JB, Willing MC, Giunta C, Steinmann B, Young F, Susic M, Cole WG (2000) COL5A1 haploinsufficiency is a common molecular mechanism underlying the classical form of EDS. Am J Hum Genet 66:1766–1776

    Article  CAS  PubMed  Google Scholar 

  20. Alves F, Vogel W, Mossie K, Millauer B, Hofler H, Ullrich A (1995) Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10:609–618

    CAS  PubMed  Google Scholar 

  21. Olaso E, Labrador JP, Wang L, Ikeda K, Eng FJ, Klein R, Lovett DH, Lin HC, Friedman SL (2002) Discoidin domain receptor 2 regulates fibroblast proliferation and migration through the extracellular matrix in association with transcriptional activation of matrix metalloproteinase-2. J Biol Chem 277:3606–3613

    Article  CAS  PubMed  Google Scholar 

  22. Vogel W, Gish GD, Alves F, Pawson T (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1:13–23

    CAS  PubMed  Google Scholar 

  23. Shi-wen X, Pennington D, Holmes A, Leask A, Bradham D, Beauchamp JR, Fonseca C, du Bois RM, Martin GR, Black CM, Abraham DJ (2000) Autocrine overexpression of CTGF maintains fibrosis: RDA analysis of fibrosis genes in systemic sclerosis. Exp Cell Res 259:213–224

    Article  CAS  Google Scholar 

  24. Shimo T, Nakanishi T, Nishida T, Asano M, Kanyama M, Kuboki T, Tamatani T, Tezuka K, Takemura M, Matsumura T, Takigawa M (1999) Connective tissue growth factor induces the proliferation, migration, and tube formation of vascular endothelial cells in vitro, and angiogenesis in vivo. J Biochem (Tokyo) 126:137–145

    Google Scholar 

  25. Frazier K, Williams S, Kothapalli D, Klapper H, Grotendorst GR (1996) Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. J Invest Dermatol 107:404–411

    Google Scholar 

  26. Jones FS, Jones PL (2000) The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218:235–259

    CAS  PubMed  Google Scholar 

  27. Mackie EJ (1997) Molecules in focus: tenascin-C. Int J Biochem Cell Biol 29:1133–1137

    Article  CAS  PubMed  Google Scholar 

  28. Burch GH, Gong Y, Liu W, Dettman RW, Curry CJ, Smith L, Miller WL, Bristow J (1997) Tenascin-X deficiency is associated with Ehlers-Danlos syndrome. Nat Genet 17:104–108

    CAS  PubMed  Google Scholar 

  29. Junqueira LC, Assis Figueiredo MT, Torloni H, Montes GS (1986) Differential histologic diagnosis of osteoid. A study on human osteosarcoma collagen by the histochemical picrosirius-polarization method. J Pathol 148:189–196

    CAS  PubMed  Google Scholar 

  30. Chanoki M, Ishii M, Fukai K, Kobayashi H, Hamada T, Muragaki Y, Ooshima A (1988) Immunohistochemical localization of type V collagen in normal human skin. Arch Dermatol Res 280:145–151

    CAS  PubMed  Google Scholar 

  31. Werkmeister JA, Ramshaw JA (1989) Monoclonal antibodies to collagens for immunofluorescent examination of human skin. Acta Derm Venereol 69:399–402

    CAS  PubMed  Google Scholar 

  32. Oikarinen A, Mortenhumer M, Kallioinen M, Savolainen ER (1987) Necrobiosis lipoidica: ultrastructural and biochemical demonstration of a collagen defect. J Invest Dermatol 88:227–232

    Google Scholar 

  33. Prockop DJ, Kadler KE, Hojima Y, Constantinou CD, Dombrowski KE, Kuivaniemi H, Tromp G, Vogel B (1988) Expression of type I procollagen genes. Ciba Found Symp 136:142–160

    CAS  PubMed  Google Scholar 

  34. Bishop JE, Rhodes S, Laurent GJ, Low RB, Stirewalt WS (1994) Increased collagen synthesis and decreased collagen degradation in right ventricular hypertrophy induced by pressure overload. Cardiovasc Res 28:1581–1585

    CAS  PubMed  Google Scholar 

  35. Konomi H, Hayashi T, Nakayasu K, Arima M (1984) Localization of type V collagen and type IV collagen in human cornea, lung, and skin. Immunohistochemical evidence by anti-collagen antibodies characterized by immunoelectroblotting. Am J Pathol 116:417–426

    CAS  PubMed  Google Scholar 

  36. Pans A, Pierard, GE, Albert A (1999) Immunohistochemical study of the rectus sheath and transversalis fascia in adult groin hernias. Hernia 45:863

    Google Scholar 

  37. Holbrook KA, Byers PH (1989) Skin is a window on heritable disorders of connective tissue. Am J Med Genet 34:105–121

    CAS  PubMed  Google Scholar 

  38. Lightner VA, Gumkowski F, Bigner DD, Erickson HP (1989) Tenascin/hexabrachion in human skin: biochemical identification and localization by light and electron microscopy. J Cell Biol 108:2483–2493

    CAS  PubMed  Google Scholar 

  39. Filsell W, Rudman S, Jenkins G, Green MR (1999) Coordinate upregulation of tenascin C expression with degree of photodamage in human skin. Br J Dermatol 140:592–599

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, University Hospital, RWTH, Pauwelsstrasse 30, 52074, Aachen, Germany

    R. Rosch, K. Junge, M. Knops, U. Klinge & V. Schumpelick

  2. German Center of Excellence for Biomaterial and Implant Pathology, University Hospital, RWTH, Pauwelsstrasse 30, 52074, Aachen, Germany

    P. Lynen

Authors
  1. R. Rosch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Junge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Knops
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Lynen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. U. Klinge
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. Schumpelick
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Rosch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rosch, R., Junge, K., Knops, M. et al. Analysis of collagen-interacting proteins in patients with incisional hernias. Langenbecks Arch Surg 387, 427–432 (2003). https://doi.org/10.1007/s00423-002-0345-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-002-0345-3

Keywords

Search

Navigation