Skip to main content
SpringerLink
Log in

Morphologic changes in neo-intimal proliferation in an experimental aneurysm after coil embolization: effect of factor XIII administration

  • Interventional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

We investigated histological changes in aneurysmal orifices after embolization with Guglielmi detachable coils (GDCs) and determined the effects of the wound-healing factor, factor XIII, on promoting intimal proliferation by scanning electron microscopy (SEM). GDC embolization was performed in an experimental model of aneurysm in swine. In the control group (17 aneurysms), the aneurysms were resected immediately after surgery, at 1 and 3 weeks after the procedure. In the factor XIII-administered group (13 aneurysms), the swine received factor XIII postoperatively, and the aneurysms were excised at 1 and 3 weeks. The endothelial cell proliferation changes in the aneurysm orifices in both groups were evaluated by SEM. The histological changes at the orifices began immediately after the procedure, and endothelialization was observed at 1 week. One week after the procedure, the rate of endothelial cell proliferation was significantly higher in the factor XIII group (P<0.05). But no difference was observed at 3 weeks, when endothelialization of the orifices was essentially completed. The process of intimal proliferation after coil embolization was similar to the wound-healing process after vascular intimal injury. Administration of the wound-healing factor, factor XIII, would contribute rapid intimal proliferation and may be effective to facilitate complete obliteration of aneurysms after coil embolization.

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

Similar content being viewed by others

References

  1. Abuja AA, Hergenrother RW, Strother CM et al (1993) Platinum coil coating to increase thrombogenicity: a preliminary study in rabbits. AJNR Am J Neuroradiol 14:794–798

    PubMed  Google Scholar 

  2. Bavinzski G, Riching B, Binder BR et al (1999) Histopsthologic findings for experimental aneurysms embolized with conventional and thrombogenic/antithrombolytic Guglielmi coils. Minim Invas Neurosurg 42:167–174

    CAS  Google Scholar 

  3. Bavinski G, Talazoglu V, Killer M et al (1999) Gross and microscopic histological findings in aneurysms of the human brain treated with Guglielmi detachable coils. J Neurosurg 91:284–293

    PubMed  Google Scholar 

  4. Bocher-Schwarz HG, Ringel K, Bohl J et al (2002) Histological findings in coil-packed experimental aneurysms 3 months after embolization. Neurosurgery 50:379–385

    Article  PubMed  Google Scholar 

  5. Castro E, Fortea F, Villoria F et al (1999) Long-term histopathologic findings in 2 cerebral aneurysms embolized with Guglielmi detachable coils. AJNR Am J Neuroradiol 20:549–552

    CAS  PubMed  Google Scholar 

  6. Eskridge JM, Song JK et al (1998) Endovascular embolization of 150 basilar tip aneurysms with Guglielmi detachable coils: result of the Food and Drug Administration multicenter clinical trial. J Neurosurg 89:81–86

    CAS  PubMed  Google Scholar 

  7. Gerlach R, Raabe A, Zimmermann M et al (2000) Factor XIII deficiency and postoperative hemorrhage after neurosurgical procedures. Surg Neurol 54:260–266

    Article  CAS  PubMed  Google Scholar 

  8. Guglielmi G, Vinela F, Sepetka I et al (1991) Electrothorombosis of saccular aneurysm via endovascular approach. Part 1: electrochemical basis, technique, and experimental result. J Neurosurg 75:1–7

    CAS  PubMed  Google Scholar 

  9. Guglielmi G, Vinela F, Jacques D et al (1991) Electrothorombosis of saccular aneurysm via endovascular approach. Part 2: preliminary clinical experience. J Neurosurg 75:8–14

    CAS  PubMed  Google Scholar 

  10. Guglielmi G, Vinela F, Duckwiler G et al (1992) Endovascular treatment of posterior circulation aneurysm by electrothrombosis using electrically detachable coils. J Neurosurg 77:515–524

    CAS  PubMed  Google Scholar 

  11. Hayakawa M, Yuichi M, Duckwiler GR et al (2000) Natural history of the neck remnant of a cerebral aneurysm treated with the Guglielmi detachable coil system. J Neurosurg 93:561–568

    CAS  PubMed  Google Scholar 

  12. Hino K, Konishi Y, Shimada A et al (2001) Histological investigation of endothelial proliferation on the coil surface after endovascular treatment using factor XIII: preliminary result in swine model. Interv Neuroradiol 7:29–33

    Google Scholar 

  13. Horowitz MB, Purdy PD, Bellotto D (1997) Scanning electron microscopic findings in a basilar tip aneurysm embolized with Guglielmi detachable coils. AJNR Am J Neuroradiol 18:688–690

    CAS  PubMed  Google Scholar 

  14. International subarachnoid aneurysm trial (ISAT) collaborative group (2002) International sabarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovsascular coiling in 2143 patients with ruptured intracranial aneurysms. A randomized trial. Lancet 360:1267–1274

    Google Scholar 

  15. Isogai N, Kamishima H, Chichibu S et al (1998) Re-endothelialization stages at microvascular anastomosis. Microsurgery 9:87–92

    Google Scholar 

  16. Isogai N, Ueda Y, Kurozumi N et al (1990) Wound-healing at the site of microvascular anastomosis: fibrin-stabilizing factor XIII administration and its effects. Microsurgery 11:40–46

    CAS  PubMed  Google Scholar 

  17. Kang Y, Hashimoto N, Kikuchi H et al (1990) Effects of blood coagulation factor XIII on the development of experimental cerebral aneurysms in rats. J Neurosurg 73:242–247

    CAS  PubMed  Google Scholar 

  18. Longa EZ, Weinstein PR, Chater G (1984) Scanning electron microscopy studies of needle and suture damage in rat carotid and femoral arteries. Microsurgery 5:169–174

    CAS  PubMed  Google Scholar 

  19. Macdonald RL, Mojtahedi S, Johns L et al (1998) Randomized comparison of Guglielmi detachable coils and cellulose acetate polymer for treatment of aneurysms in dogs. Stroke 29:478–486

    CAS  PubMed  Google Scholar 

  20. Manabe H, Fujita S, Hatayama T et al (1998) Re-rupture of coil-embolized aneurysm during long-term observation. J Neurosurg 88:1096–1098

    CAS  PubMed  Google Scholar 

  21. Marktl W, Rudas B (1974) The effect of factor XIII on wound granulation in the rat. Thromb Diath Haemorrh 32:578–581

    CAS  PubMed  Google Scholar 

  22. Mawad ME, Mawad JK, Cartwright MJ et al (1995) Long-term histopathologic changes in carine aneurysms embolized with Guglielmi detachable coils. AJNR Am J Neuroradiol 16:7–13

    CAS  PubMed  Google Scholar 

  23. Molyneux AJ, Ellison DW, Morris J et al (1995) Histological findings in giant aneurysm treated with Guglielmi detachable coils: report of two cases with autopsy correlation. J Neurosurg 83:129–132

    CAS  PubMed  Google Scholar 

  24. Mosher DF, Schad PE (1979) Cross-linking of fibronectin to collagen by blood coagulation factor XIIIa. J Clin Invest 64:781–787

    CAS  PubMed  Google Scholar 

  25. Mizoi K, Yoshimoto T, Takahashi A et al (1996) A pitfall in thesurgery of a recurrent aneurysm after coil embolization and its histological observation: technical case report. Neurosurgery 39:165–169

    Article  CAS  PubMed  Google Scholar 

  26. Murayama Y, Vinuela F, Suzuki Y et al (1997) Ion implantation and protein coating of detachable coils for endovascular treatment of cerebral aneurysms: concepts and preliminary results in swine models. Neurosurgery 40:1233–1244

    Article  CAS  PubMed  Google Scholar 

  27. Murayama Y, Vinuela F, Suzuki Y et al (1999) Development of a biologically active GDC for the treatment of cerebral aneurysms. Interv Neurosurg 5:211–214

    Google Scholar 

  28. Murayama Y, Suzuki Y, Vinuela F et al (1999) Development of a biologically active Guglielmi detachable coil for the treatment of cerebral aneurysms. Part I: in vitro study. AJNR Am J Neuroradiol 20:1986–1991

    CAS  PubMed  Google Scholar 

  29. Murayama Y, Vinuela F, Tateshima S et al (2001) Bioabsorbable polymeric material coils for embolization of interacranial aneurysms: a preliminary experimental study. J Neurosurg 94:454–463

    CAS  PubMed  Google Scholar 

  30. Murayama Y, Vinuela F, Suzuki Y et al (1999) Development of the biologically active Guglielmi detachable coil for the treatment of cerebral aneurysms. Part II: an experimental study in a swine aneurysm model. AJNR Am J Neuroradiol 20:1992–1999

    CAS  PubMed  Google Scholar 

  31. Pagnanelli DM, Pait TG, Rizzoli HV et al (1980) Scanning electron study of vascular lesions caused by microvascular needles and suture. J Neurosurg 53:32–36

    CAS  PubMed  Google Scholar 

  32. Pagnanelli DM, Naradzay JFX, Pait TG et al (1983) The cutting-edge microvascular needle: a scanning electron microscopic study. J Neurosurg 59:510–513

    CAS  PubMed  Google Scholar 

  33. Reul JW, Spetzger U, Konert T et al (1997) Long-term angiographic findings in experimental aneurysms of the carotid bifurcation embolized with platinum and tungsten coils. AJNR Am J Neuroradiol 18:35–42

    CAS  PubMed  Google Scholar 

  34. Sakata Y, Aoki N (1980) Crosslinking of alpha2-plasmin inhibitor to fibrin by fibrin-stabilizing factor. J Clin Invest 65:290–297

    CAS  PubMed  Google Scholar 

  35. Servant JM, Ikuta Y, Harada Y et al (1976) A scanning electron microscope study of microvascular anastomoses. Plast Reconstr Surg 57:329–334

    CAS  PubMed  Google Scholar 

  36. Shimizu S, Kurata A, Hiroshi T et al (1999) Tissue response of a small saccular aneurysm after incomplete occlusion with Giglielmi detachable coils. AJNR Am J Neuroradiol 20:546–548

    CAS  PubMed  Google Scholar 

  37. Soria A, Soria C, Boulard C (1975) Fibrin stabilizing factor (FXIII) and collagen polymerization. Experientia 31:1355–1357

    CAS  PubMed  Google Scholar 

  38. Spetzger U, Reul J, Weis J et al (1996) Microsurgically product bifurcation aneurysms in a rabbit model for endovascular coil embolization. J Neurosurg 85:488–495

    CAS  PubMed  Google Scholar 

  39. Suda Y, Kikuchi K, Shioya K et al (1999) Long-term histopathology of intracranial aneurysms after endovascular treatment with coils: report of two cases with ultrastructural evaluations by scanning electron microscopy. Interv Neuroradiol 5:225–231

    Google Scholar 

  40. Szikora I, Wakhloo K, Guterman LR et al (1997) Initial experience with collagen-filled Guglielmi detachable coils for endovascular treatment of experimental aneurysms. AJNR Am J Neuroradiol 18:667–672

    CAS  PubMed  Google Scholar 

  41. Tamatani S, Ozawa T, Minakawa T et al (1999) Radiologic and histopathologic evaluation of canine artery occlusion after collagen-coated platinum microcoil delivery. AJNR Am J Neuroradiol 20:541–545

    CAS  PubMed  Google Scholar 

  42. Tamatani S, Ozawa T, Minakawa T et al (1997) Histological interaction of cultured endothelial cells and endovascular embolic materials coated with extracellular matrix. J Neurosurg 86:109–112

    CAS  PubMed  Google Scholar 

  43. Tenjin H, Fushiki S, Nakahara Y et al (1995) Effect of Guglielmi detachable coils on experimental carotid artery aneurysms in primates. Stroke 26:2075–2080

    CAS  PubMed  Google Scholar 

  44. Thurston JB, Buncke HJ, Chater NL et al (1976) A scanning electron microscopy of micro-arterial damage and repair. Plast Reconstr Surg 57:197–203

    CAS  PubMed  Google Scholar 

  45. Ueyama M, Urayama T (1978) The role of factor XIII in fibroblast proliferation. Japan. J Exp Med 48:135–142

    CAS  Google Scholar 

  46. Vinuela F, Duckwiler G, Mawad M (1997) Guglielmi detachable coil embolization of acute intracranial aneurysm: perioperative anatomical and clinical outcome in 403 patients. J Neurosurg 86:475–482

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. George P. Teitelbaum for critical reading of the manuscript and Mr. Fukuda for technical assistance with SEM.

Author information

Author notes

  1. Ken Hino

    Present address: Abashiri Neurosurgical Rehabilitation Hospital, 4-1-7, katsuramachi, Abashirishi, Hokkaido, 093-0041, Japan

Authors and Affiliations

  1. Department of Neurosurgery, Kyorin University School of Medicine, Tokyo, Japan

    Ken Hino, Yoshifumi Konishi, Atsushi Shimada, Hiroki Kurita, Eishi Sato, Yoshiaki Shiokawa & Isamu Saito

  2. Department of Neurosurgery, Osaka City University Medical School, Osaka, Japan

    Mitsuhiro Hara

Authors
  1. Ken Hino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshifumi Konishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atsushi Shimada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiroki Kurita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eishi Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mitsuhiro Hara
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yoshiaki Shiokawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Isamu Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ken Hino.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hino, K., Konishi, Y., Shimada, A. et al. Morphologic changes in neo-intimal proliferation in an experimental aneurysm after coil embolization: effect of factor XIII administration. Neuroradiology 46, 996–1005 (2004). https://doi.org/10.1007/s00234-004-1278-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-004-1278-z

Keywords

Search

Navigation