Skip to main content

Advertisement

SpringerLink
Log in

Tissue reaction to three different types of tissue glues in an experimental aorta dissection model: a quantitative approach

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Tissue glues are used during surgical treatment of acute aorta dissection although some glues release toxic products and thus alter the histological structure of the vessel wall. The aim of our study was to use a porcine experimental model of infrarenal aorta dissection to compare histological changes of the vessel wall 1, 6 and 12 months after application of BioGlue, Gelatin-resorcin-formaldehyde (GRF) glue and Tissucol. For quantification, stereological methods were used. All types of glue caused stenosis, GRF most and Tissucol least severely. With increasing postoperative survival time, stenosis was again reduced. Elastine length density decreased with increasing survival time in Control as well as in all Experimental groups. The immunohistochemical phenotype of vascular smooth muscle cells was similar in Tissucol and Control samples. In GRF samples, actin, desmin and vimentin expression changed most severely. Similarly, number and distribution of vasa vasorum in the aortic wall was altered most severely in GRF samples. They tended to return to normal with increasing postoperative survival time, but at a slow rate in the GRF samples. It can be concluded that GRF causes the most severe histopathological changes within the treated aorta, which could be a reason for late failures of dissection surgery. However, glue handling and adhesive properties have to be taken into account, too, when certain glue is chosen for surgical intervention. Increased inflammation and vascularisation might even stabilise the aortic wall. Long-term experimental studies would be helpful to assess healing processes after initial disorganisation of the aortic wall structure.

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

  • Annabi B, Shédid D, Ghosn P, Kenigsberg RL, Desrosiers RR, Bojanowski MW, Beaulieu E, Nassif E, Moumdjian R, Béliveau R (2002) Differential regulation of matrix metalloproteinase activities in abdominal aortic aneurysms. J Vasc Surg 35:539–546

    Article  PubMed  Google Scholar 

  • Archer SL (1996) Diversity of phenotype and function of vascular smooth muscle cells. J Lab Clin Med 127:524–529

    Article  PubMed  Google Scholar 

  • Bachet J, Guilmet D (1999) The use of biological glue in aortic surgery. Cardiol Clin 17:779–796

    Article  PubMed  Google Scholar 

  • Bachet J, Goudot B, Dreyfus GD, Brodaty D, Dubois C, Delentdecker P, Guilmet D (1999) Surgery for acute type A aortic dissection: The Hopital Foch experience (1977–1998). Ann Thorac Surg 67:2006–2009

    Article  PubMed  Google Scholar 

  • Bachet J, Goudot B, Dreyfus G, Brodaty D, Dubois C, Delentdecker P, Teimouri F, Guilmet D (2000) Surgery of acute type A dissection: what have we learned during the past 25 years? Z Kardiol 89(Suppl 7):VII47–VII54

    Article  Google Scholar 

  • Badier-Commander C, Couvelard A, Henin D, Verbeuren T, Michel JB, Jacob MP (2001) Smooth muscle cell modulation and cytokine overproduction in varicose veins. An in situ study. J Pathol 193:398–407

    Google Scholar 

  • Bayer IM, Caniggia I, Adamson SL, Langille BL (2002) Experimental angiogenesis of arterial vasa vasorum. Cell Tissue Res 307:303–313

    Article  PubMed  Google Scholar 

  • Beauchamp RO Jr, St Clair MBG, Fennell TR, Clarke DO, Morgan KT, Kari FW (1992) A critical review of the toxicology of glutaraldehyde. Crit Rev Toxicol 22:143–174

    Article  PubMed  Google Scholar 

  • Blanton FS, Muller WH Jr, Warren WD (1959) Experimental production of dissecting aneurysms of the aorta. Surgery 45:81–90

    PubMed  Google Scholar 

  • Bobková D, Tonar Z (2005) Effect of long-term cholesterol diet on cholesterol concentration and development of atherosclerosis in homozygous apolipoprotein e-deficient mice. Acta Vet Brno 74:501–507

    Google Scholar 

  • Bobryshev YV (2006) Monocyte recruitment and foam cell formation in atherosclerosis. Micron 37:208–222

    Article  PubMed  Google Scholar 

  • Boccardi C, Cecchettini A, Caselli A, Camici G, Evangelista M, Mercatanti A, Rainaldi G, Citti L (2007) A proteomic approach to the investigation of early events involved in vascular smooth muscle cell activation. Cell Tissue Res 328:185–195

    Article  PubMed  Google Scholar 

  • Chao HH, Torchiana DF (2003) BioGlue: Albumin/Glutaraldehyde sealant in cardiac surgery. J Cardiac Surg 18:500–503

    Article  Google Scholar 

  • Cho SW, Kim IK, Kang JM, Song KW, Kim HS, Park CH, Yoo KJ, Kim BS (2009) Evidence for in vivo growth potential and vascular remodeling of tissue-engineered artery. Tissue Eng Part A 15:901–912

    Article  PubMed  Google Scholar 

  • Dashwood MR, Anand R, Loesch A, Souza DSR (2004) Hypothesis: a potential role for the vasa vasorum in the maintenance of vein graft patency. Angiology 55:385–395

    Article  PubMed  Google Scholar 

  • Ennker J, Ennker IC, Schoon D, Schoon HA, Dorge S, Meissler M, Rimpler M, Hetzer R (1994) The impact of gelatin-resorcinol glue on aortic tissue: a histomorphologic evaluation. J Vasc Surg 20:34–43

    PubMed  Google Scholar 

  • Erasmi AW, Sievers HH, Wohlschläger C (2002) Inflammatory response after BioGlue application. Ann Thorac Surg 73:1025–1026

    Article  PubMed  Google Scholar 

  • Fehrenbacher JW, Siderys H (2006) Use of BioGlue in aortic surgery: proper application techniques and results in 92 patients. Heart Surg Forum 9:E794–E799

    Article  PubMed  Google Scholar 

  • Fukunaga S, Karck M, Harringer W, Cremer J, Rhein C, Haverich A (1999) The use of gelatin-resorcin-formalin glue in acute aortic dissection type A. Eur J Cardio Thorac 15:564–570

    Article  Google Scholar 

  • Fürst W, Banerjee A (2005) Release of glutaraldehyde from an albumin-glutaraldehyde tissue adhesive causes significant in vitro and in vivo toxicity. Ann Thorac Surg 79:1522–1528

    Article  PubMed  Google Scholar 

  • Gerner W, Käser T, Pintarič M, Groiß S, Saalmüller A (2008) Detection of intracellular antigens in porcine PBMC by flow cytometry: a comparison of fixation and permeabilisation reagents. Vet Immunol Immunopathol 121:251–259

    Article  PubMed  Google Scholar 

  • Grabenwöger M, Fitzal F, Sider J, Csekö C, Bergmeister H, Schima H, Husinsky W, Böck P, Wolner E (1998) Endothelialization of biosynthetic vascular prostheses after laser perforation. Ann Thorac Surg 66(Suppl 1):S110–S114

    Article  PubMed  Google Scholar 

  • Gundersen HJG, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263

    PubMed  Google Scholar 

  • Gundersen HJ, Osterby R (1981) Optimizing sampling efficiency of stereological studies in biology: or ‘do more less well!’. J Microsc 121:65–73

    PubMed  Google Scholar 

  • Hata M, Shiono M, Sezai A, Iida M, Negishi N, Sezai Y (2004) Type A acute aortic dissection: Immediate and mid-term results of emergency aortic replacement with the aid of gelatin resorcin formalin glue. Ann Thorac Surg 78:853–857

    Article  PubMed  Google Scholar 

  • Hata H, Takano H, Matsumiya G, Fukushima N, Kawaguchi N, Sawa Y (2007) Late complications of gelatin-resorcin-formalin glue in the repair of acute type A aortic dissection. Ann Thorac Surg 83:1621–1626

    Article  PubMed  Google Scholar 

  • Hewitt CW, Marra SW, Kann BR, Tran HS, Puc MM, Chrzanowski FA Jr, Tran JLV, Lenz SD, Cilley JH Jr, Simonetti VA, Delrossi AJ (2001) BioGlue surgical adhesive for thoracic aortic repair during coagulopathy: efficacy and histopathology. Ann Thorac Surg 71:1609–1612

    Article  PubMed  Google Scholar 

  • Houard X, Touat Z, Ollivier V, Louedec L, Philippe M, Sebbag U, Meilhac O, Rossignol P, Michel JB (2009) Mediators of neutrophil recruitment in human abdominal aortic aneurysms. Cardiovasc Res 82:532–541

    PubMed  Google Scholar 

  • Howard CV, Reed MG (1998) Unbiased stereology: three-dimensional measurement in microscopy, 1st edn. Royal Microscopical Society and Springer-Verlag, New York

    Google Scholar 

  • Hu JJ, Ambrus A, Fossum TW, Miller MW, Humphrey JD, Wilson E (2008) Time courses of growth and remodeling of porcine aortic media during hypertension: a quantitative immunohistochemical examination. J Histochem Cytochem 56:359–370

    Article  PubMed  Google Scholar 

  • Huang-Lee LLH, Cheung DT, Nimni ME (1990) Biochemical changes and cytotoxicity associated with the degradation of polymeric glutaraldehyde derived crosslinks. J Biomed Mater Res 24:1185–1201

    Article  PubMed  Google Scholar 

  • Johansson B, Eriksson A, Virtanen I, Thornell LE (1997) Intermediate filament proteins in adult human arteries. Anat Rec 247:439–448

    Article  PubMed  Google Scholar 

  • Johnson GJ, Griggs TR, Badimon L (1999) The utility of animal models in the preclinical study of interventions to prevent human coronary artery restenosis: analysis and recommendations. Thromb Haemost 81:835–843

    PubMed  Google Scholar 

  • Kacem K, Seylaz J, Aubineau P (1996) Differential processes of vascular smooth muscle cell differentiation within elastic and muscular arteries of rats and rabbits: an immunofluorescence study of desmin and vimentin distribution. Histochem J 28:53–61

    Article  PubMed  Google Scholar 

  • Kamada T, Nakajima T, Izumoto H, Sugai T, Yoshioka K, Kawazoe K (2005) Late complications following surgery for type A acute aortic dissection using gelatin-resorcin-formaldehyde glue: report of two cases. Surg Today 35:996–999

    Article  PubMed  Google Scholar 

  • Kazui T, Washiyama N, Bashar AH, Terada H, Suzuki K, Yamashita K, Takinami M (2001) Role of biologic glue repair of proximal aortic dissection in the development of early and midterm redissection of the aortic root. Ann Thorac Surg 72:509–514

    Article  PubMed  Google Scholar 

  • Khurana R, Zhuang Z, Bhardwaj S, Murakami M, De Muinck E, Yla-Herttuala S, Ferrara N, Martin JF, Zachary I, Simons M (2004) Angiogenesis-dependent and independent phases of intimal hyperplasia. Circulation 110:2436–2443

    Article  PubMed  Google Scholar 

  • Kirsch M, Ginat M, Lecerf L, Houël R, Loisance D (2002) Aortic wall alterations after use of gelatin-resorcinol-formalin glue. Ann Thorac Surg 73:642–644

    Article  PubMed  Google Scholar 

  • Kochova P, Tonar Z, Matejka VM, Sviglerova J, Stengl M, Kuncova J (2008) Morphology and mechanical properties of the subrenal aorta in normotensive and hypertensive rats. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 152:239–245

    PubMed  Google Scholar 

  • Kocova J (1970) Overall staining of connective tissue and the muscular layer of vessels. Folia Morphol 18:293–295

    Google Scholar 

  • Matkowskyj KA, Cox R, Jensen RT, Benya RV (2003) Quantitative immunohistochemistry by measuring cumulative signal strength accurately measures receptor number. J Histochem Cytochem 51:205–214

    PubMed  Google Scholar 

  • Michel JB, Thaunat O, Houard X, Meilhac O, Caligiuri G, Nicoletti A (2007) Topological determinants and consequences of adventitial responses to arterial wall injury. Arterioscler Thromb Vasc 27:1259–1268

    Article  Google Scholar 

  • Mitrev Z, Belostotskii V, Hristov N (2007) Suture line reinforcement using suction-assisted bioglue application during surgery for acute aortic dissection. Interact Cardiovasc Thorac Surg 6:147–149

    Article  PubMed  Google Scholar 

  • Miyazaki H, Hasegawa Y, Hayashi K (2002) Tensile properties of contractile and synthetic vascular smooth muscle cells. JSME Int J Ser C Mech Sy 45:870–879

    Article  Google Scholar 

  • Morris SM, Stone PJ (1995) Immunocytochemical study of the degradation of elastic fibers in a living extracellular matrix. J Histochem Cytochem 43:1145–1153

    PubMed  Google Scholar 

  • Moulton KS (2006) Angiogenesis in atherosclerosis: gathering evidence beyond speculation. Curr Opin Lipidol 17:548–555

    Article  PubMed  Google Scholar 

  • Nakajima T, Kawazoe K, Izumoto H, Kataoka T, Kazui T (2005) Effective use of fibrin glue for acute aortic dissection. Ann Thorac Surg 79:1793–1794

    Article  PubMed  Google Scholar 

  • Ninet J, Thevenet F, Cochet P, Vigneron M, Risk M, Champsaur G (1988) Chirurgie de l’aorte thoracique. Interet du Tissucol. Presse Med 17:2197–2199

    PubMed  Google Scholar 

  • Norrby K (2006) In vivo models of angiogenesis. J Cell Mol Med 10:588–612

    Article  PubMed  Google Scholar 

  • O’Rourke MF (2007) Arterial aging: pathophysiological principles. Vasc Med 12:329–341

    Article  PubMed  Google Scholar 

  • Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767–801

    Article  PubMed  Google Scholar 

  • Ribatti D, Levi-Schaffer F, Kovanen PT (2008) Inflammatory angiogenesis in atherogenesis—a double-edged sword. Ann Med 40:606–621

    Article  PubMed  Google Scholar 

  • Richter S, Kollmar O, Neunhoeffer E, Schilling MK, Menger MD, Pistorius G (2006) Differential response of arteries and veins to bipolar vessel sealing: evaluation of a novel reusable device. J Laparoendosc Adv Surg Tech A 16:149–155

    Article  PubMed  Google Scholar 

  • Romeis B (1989) Mikroskopische Technik. Urban & Schwarzenberg, München

    Google Scholar 

  • Santilli SM, Wernsing SE, Lee ES (2000) Transarterial wall oxygen gradients at a prosthetic vascular graft to artery anastomosis in the rabbit. J Vasc Surg 31:1229–1239

    PubMed  Google Scholar 

  • Scheld HH, Gorlach G, Boldt J, Dapper F, Moosdorf R (1990) Decreasing the risk of aortic arch replacement. Vasc Surg 24:191–197

    Google Scholar 

  • Schober A, Weber C (2005) Mechanisms of monocyte recruitment in vascular repair after injury. Antioxid Redox Signal 7:1249–1257

    Article  PubMed  Google Scholar 

  • Scotland RS, Vallance PJ, Ahluwalia A (2000) Endogenous factors involved in regulation of tone of arterial vasa vasorum: implications for conduit vessel physiology. Cardiovasc Res 46:403–411

    Article  PubMed  Google Scholar 

  • Seyednejad H, Imani M, Jamieson T, Seifalian AM (2008) Topical haemostatic agents. Br J Surg 95:1197–1225

    Article  PubMed  Google Scholar 

  • Shadwick RE (1999) Mechanical design in arteries. J Exp Biol 202:3305–3313

    PubMed  Google Scholar 

  • Shanahan CM, Weissberg PL (1999) Smooth muscle cell phenotypes in atherosclerotic lesions. Curr Opin Lipidol 10:507–513

    Article  PubMed  Google Scholar 

  • Shiono M (2008) Surgery for acute aortic dissection using gelatin-resorcin-formalin glue: perspective from 10 years of follow-up at a single center. J Artif Organs 11:19–23

    Article  PubMed  Google Scholar 

  • Siow RCM, Churchman AT (2007) Adventitial growth factor signalling and vascular remodelling: potential of perivascular gene transfer from the outside-in. Cardiovasc Res 75:659–668

    Article  PubMed  Google Scholar 

  • Sokolis DP, Boudoulas H, Karayannacos PE (2008) Segmental differences of aortic function and composition: clinical implications. Hellenic J Cardiol 49:145–154

    PubMed  Google Scholar 

  • Speer DP, Chvapil M, Eskelson CD, Ulreich J (1980) Biological effects of residual glutaraldehyde in glutaraldehyde-tanned collagen biomaterials. J Biomed Mater Res 14:753–764

    Article  PubMed  Google Scholar 

  • Stary HC (2000) Natural history and histological classification of atherosclerotic lesions—an update. Arterioscler Thromb Vas 20:1177–1178

    Google Scholar 

  • Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136

    PubMed  Google Scholar 

  • Stoyan D, Kendall WS, Mecke J (1995) Fibre and surface processes. In: Stoyan D, Kendall WS, Mecke J (eds) Stochastic geometry and its applications, 2nd edn. Wiley, Chichester, pp 275–297

    Google Scholar 

  • Tonar Z, Nemecek S, Holota R, Kocova J, Treska V, Molacek J, Kohoutek T, Hadravska S (2003) Microscopic image analysis of elastin network in samples of normal, atherosclerotic and aneurysmatic abdominal aorta and its biomechanical implications. J Appl Biomed 1:149–160

    Google Scholar 

  • Tonar Z, Nemecek S, Holota R (2005) Microscopic image analysis of elastin and morphometry of wall of thoracic and abdominal porcine aorta. IFMBE Proc 11:1474–1479

    Google Scholar 

  • Tonar Z, Egger G, Witter K, Wolfesberger B (2008) Quantification of microvessels in canine lymph nodes. Microsc Res Tech 71:760–772

    Article  PubMed  Google Scholar 

  • Torikai K, Ichikawa H, Hirakawa K, Matsumiya G, Kuratani T, Iwai S, Saito A, Kawaguchi N, Matsuura N, Sawa Y (2008) A self-renewing, tissue-engineered vascular graft for arterial reconstruction. J Thorac Cardiovasc Surg 136:37–45

    Article  PubMed  Google Scholar 

  • Treska V, Kocova J, Boudova L, Neprasova P, Topolcan O, Pecen L, Tonar Z (2002) Inflammation in the wall of abdominal aortic aneurysm and its role in the symptomatology of aneurysm. Cytokines Cell Mol Ther 7:91–97

    Article  PubMed  Google Scholar 

  • von Oppell UO, Zilla P (1998) Tissue adhesives in cardiovascular surgery. J Long Term Eff Med Implants 8:87–101

    Google Scholar 

  • von Oppell UO, Karani Z, Brooks A, Brink J (2002) Dissected aortic sinuses repaired with gelatin-resorcin-formaldehyde (GRF) glue are not stable on follow up. J Heart Valve Dis 11:249–257

    Google Scholar 

  • Wolinsky H, Glagov S (1969) Comparison of abdominal and thoracic aortic medial structure in mammals. Deviation of man from the usual pattern. Circ Res 25:677–686

    PubMed  Google Scholar 

  • Yoshida K, Ohtake H, Kimura K, Watanabe G (2006) Experimental study of aortic anastomosis using a circular stapling device in the porcine model. Eur J Vasc Endovasc Surg 31:575–580

    Article  PubMed  Google Scholar 

  • Yoshigi M, Karnik S, Li DY, Clark EB, Yost HJ (2000) Quantitative analysis of cytoskeletal remodeling in vascular smooth muscle cells during phenotypic modulation. Comput Cardiol 27:205–206

    Google Scholar 

  • Yoshitatsu M, Nomura F, Katayama A, Tamura K, Katayama K, Ihara K, Nakashima Y (2004) Pathologic findings of aortic redissection after glue repair of proximal aorta. J Thorac Cardiovasc Sur 127:593–595

    Article  Google Scholar 

Download references

Acknowledgments

We wish to thank Ms. D. Rosenfellner and Ms. M. Helmreich for their excellent technical assistance. Histological quantification was supported by the Ministry of Education, Youth and Sports of the Czech Republic under Project Nos. MSM4977751303, MSM0021620819 and 1M6798582302. Cooperation between the authors received support from the Project KONTAKT ME09090. The surgical part of the project was supported by the Internal Grant Agency of the Ministry of Health of the Czech Republic under Project No. NR8863-3/2006. The study received no support from any manufacturer of any type of glue used in vascular surgery.

Author information

Authors and Affiliations

  1. Department of Pathobiology, Institute of Histology and Embryology, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210, Wien, Austria

    Kirsti Witter

  2. Department of Histology and Embryology, Faculty of Medicine in Pilsen, Charles University in Prague, Karlovarska 48, 30166, Pilsen, Czech Republic

    Zbyněk Tonar & Vít Martin Matějka

  3. Department of Mechanics, Faculty of Applied Science, University of West Bohemia in Pilsen, Univerzitni 22, 30614, Pilsen, Czech Republic

    Zbyněk Tonar

  4. Laboratory for Atherosclerosis Research, Institute for Clinical and Experimental Medicine, Prague, Videnska 1958/9, 14021, Prague, Czech Republic

    Zbyněk Tonar

  5. Department of Cardiovascular Surgery, Institute for Clinical and Experimental Medicine, Prague, Videnska 1958/9, 14021, Prague, Czech Republic

    Tomáš Martinča, Michael Jonák, Slavomír Rokošný & Jan Pirk

Authors
  1. Kirsti Witter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zbyněk Tonar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vít Martin Matějka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomáš Martinča
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael Jonák
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Slavomír Rokošný
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jan Pirk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zbyněk Tonar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Witter, K., Tonar, Z., Matějka, V.M. et al. Tissue reaction to three different types of tissue glues in an experimental aorta dissection model: a quantitative approach. Histochem Cell Biol 133, 241–259 (2010). https://doi.org/10.1007/s00418-009-0656-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-009-0656-3

Keywords

Search

Navigation