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Evaluation of Multiple Embolic Agents for Embolization of the Superior Rectal Artery in an Animal Model

CardioVascular and Interventional Radiology volume 45, pages 510–519 (2022)Cite this article

Abstract

Objective

To prospectively compare the safety of transcatheter embolization of superior rectal arteries in healthy pigs with multiple agents such as coils, spheres and liquids.

Materials and Methods

Nine adult domestic pigs (three males, mean weight: 60 kg [50–70]) were randomly assigned to the embolization group: copolymer of ethylene vinyl alcohol (EVOH)—Onyx® (group 1, n = 3), microspheres 500 µ (group 2, n = 3), 2-mm micro-coils (group 3, n = 3). After a selective angiogram has been acquired, the embolic agent was infused at the distal part of rectal arteries. An angio-CT was performed before and after each embolization. After one week, angiography was repeated prior to euthanasia. At necropsy, the anorectal juncture was removed for histopathologic examination.

Results

At necropsy, 100% of animals embolized with Onyx developed a significant necrosis zone of the distal part of the rectum. Histological examination revealed a mural infarction. For the micro-coil and microsphere groups, gross examination of the intestines did not reveal any evidence of ischaemia. The coils were found in the distal arterial vasculature of the meso-rectum, allowing a downstream revascularization by collaterals. The microspheres and onyx in the rectal wall, more distally.

Conclusion

Microspheres appear to induce fewer histologic complications than the liquid embolic agent and provide a more distal occlusion than micro-coils. These results suggest that, for superior rectal artery embolization, a super-selective embolization using spheres in human clinical conditions should be more effective and as safe as coil embolization. EVOH might be an unsafe embolization agent for haemorrhoids.

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References

  1. Ganz RA. The evaluation and treatment of hemorrhoids: a guide for the gastroenterologist. Clin Gastroenterol Hepatol. 2013;11:593–603.

    Article  Google Scholar 

  2. Thompson HF. The nature of hemorrhoids. Br J Surg. 1975;62:542–52.

    Article  Google Scholar 

  3. Schuurman JP, Go PM, Bleys RL. Anatomical branches of the superior rectal artery in the distal rectum. Colorectal Dis. 2009;11:967–71.

    Article  CAS  Google Scholar 

  4. Stelzner F. The corpus cavernosum recti. Dis Colon Rectum. 1964;7:398–9.

    Article  CAS  Google Scholar 

  5. Chung YC, Hou YC, Pan AC. Endoglin (CD105) expression in the development of haemorrhoids. J Clin Invest. 2004;34:107–12.

    CAS  Google Scholar 

  6. Aigner F, Bodner G, Gruber H, et al. The vascular nature of hemorrhoids. J Gastrointest Surg. 2006;10:1044–50.

    Article  Google Scholar 

  7. Simillis C, Thoukididou SN, Slesser AAP, Rasheed S, Tan E, Tekkis PP. Systematic review and network meta-analysis comparing clinical outcomes and effectiveness of surgical treatments for haemorrhoids. Br J Surg. 2015;102:1603–18.

    Article  CAS  Google Scholar 

  8. Watson AJ, Hudson J, Wood J, et al. Comparison of stapled haemorrhoidopexy with traditional excisional surgery for haemorrhoidal disease (eTHoS): a pragmatic, multicentre, randomised controlled trial. Lancet. 2016;388:2375–85.

    Article  Google Scholar 

  9. Aigner F, Bodner G, Conrad F, Mbaka G, Kreczy A, Fritsch H. The superior rectal artery and its branching pattern with regard to its clinical influence on ligation techniques for internal hemorrhoids. Am J Surg. 2004;187:102–8.

    Article  Google Scholar 

  10. Vidal V, Louis G, Bartoli JM, Sielezneff Y, et al. Embolization of the hemorrhoidal arteries (the emborrhoid technique): a new concept and challenge for interventional radiology. Diagn Interv Imaging. 2014;95:307–15.

    Article  CAS  Google Scholar 

  11. Berczi V, Gopalan D, Cleveland TJ. Embolization of a hemorrhoid following 18 hours of life-threatening bleeding. Cardiovasc Interv Radiol. 2008;31:183–5.

    Article  Google Scholar 

  12. Kim M, Song HJ, Kim S, Cho YK, Kim HU, Song BC, et al. Massive life-threatening lower gastrointestinal hemorrhage caused by an internal hemorrhoid in a patient receiving antiplatelet therapy: a case report. Korean J Gastroenterol. 2012;60:253–7.

    Article  Google Scholar 

  13. Vidal V, Sapoval M, Sielezneff Y, et al. Emborrhoid: a new concept for the treatment of hemorrhoids with arterial embolization: the first 14 cases. Cardiovasc Intervent Radiol. 2015;38:72–8.

    Article  CAS  Google Scholar 

  14. Moussa N, Sielezneff I, Sapoval M, et al. Embolization of the superior rectal arteries for chronic bleeding due to hemorrhoidal disease. Colorectal Dis. 2017;19:194–9.

    Article  CAS  Google Scholar 

  15. Tradi F, Louis G, Giorgi R, Mege D, Bartoli JM, Sielezneff I, Vidal V. Embolization of the superior rectal arteries for hemorrhoidal disease: prospective results in 25 patients. J Vasc Interv Radiol. 2018;29:884–92.

    Article  Google Scholar 

  16. Nicholson AA, Ettles DF, Hartley JE, et al. Transcatheter coil embolotherapy: a safe and effective option for major colonic hemorrhage. Gut. 1998;43:79–84.

    Article  CAS  Google Scholar 

  17. Loffroy R, Guiu B, D’Athis P, et al. Arterial embolotherapy for endoscopically unmanageable acute gastroduodenal hemorrhage: predictors of early rebleeding. Clin Gastroenterol Hepatol. 2009;7:515–23.

    Article  Google Scholar 

  18. Komekami Y, Konishi F, Makita K, Mijin T, Onogawa A, Chochi T, Lee C, Yoshida T, Maeda T, Mitsusada M, Hasegawa S. Rectal arterio-venous malformation (AVM) with bleeding of an internal hemorrhoid. Clin J Gastroenterol. 2016;9:22–6.

    Article  Google Scholar 

  19. Lenhart M, Paetzel C, Sackmann M, et al. Superselective arterial embolisation with a liquid polyvinyl alcohol copolymer in patients with acute gastrointestinal haemorrhage. Eur Radiol. 2010;20:1994–9.

    Article  Google Scholar 

  20. Guy EG, Shetty PC, Sharma RP, Burke MW, Burke TH. Acute lower gastrointestinal hemorrhage: treatment by superselective embolization with polyvinyl alcohol particles. AJR Am J Roentgenol. 1992;159:521–6.

    Article  CAS  Google Scholar 

  21. Weldon DT, Burke SJ, Sun S, Mimura H, Golzarian J. Interventional management of lower gastrointestinal bleeding. Eur Radiol. 2008;18:857–67.

    Article  Google Scholar 

  22. Dondelinger RF, Ghysels MP, Brisbois D, et al. Relevant radiological anatomy of the pig as a training model in interventional radiology. Eur Radiol. 1998;8:1254–73.

    Article  CAS  Google Scholar 

  23. Chin AC, Singer MA, Mihalov M, et al. Superselective mesenteric embolization with microcoils in a porcine model. Dis Colon Rectum. 2002;45:212–8.

    Article  Google Scholar 

  24. Zakharchenko A, Kaitoukov Y, Vinnik Y, et al. Safety and efficacy of superior rectal artery embolization with particles and metallic coils for the treatment of hemorrhoids (Emborrhoid technique). Diagn Interv Imaging. 2016;97:1079–84.

    Article  CAS  Google Scholar 

  25. Moussa N, Bonnet B, Pereira H, Pechmajou L, Pellerin O, Abed A, Del Giudice C, Dean C, Bouda D, de Parades V, Fathallah N, Sapoval M. Mid-term results of superior rectal artery and coils for hemorrhoidal embolization with particles bleeding. Cardiovasc Intervent Radiol. 2020;43(7):1062–9.

    Article  CAS  Google Scholar 

  26. Makris GC, Thulasidasan N, Malietzis G, Kontovounisios C, Saibudeen A, Uberoi R, Diamantopoulos A, Sapoval M, Vidal V. Catheter-directed hemorrhoidal dearterialization technique for the management of hemorrhoids: a meta-analysis of the clinical evidence. J Vasc Interv Radiol. 2021;S1051–0443(21):01079–84.

    Google Scholar 

  27. Küçükay MB, Küçükay F. Superior rectal artery embolization with tris-acryl gelatin microspheres: a randomized comparison of particle size. J Vasc Interv Radiol. 2021;32(6):819–25.

    Article  Google Scholar 

  28. Kusano S, Murata K, Ohuchi H, et al. Low-dose particulate polyvinylalcohol embolization in massive small artery intestinal hemorrhage: experimental and clinical results. Invest Radiol. 1987;22:388–92.

    Article  CAS  Google Scholar 

  29. Saeed Kilani M, Lepennec V, Petit P, Magalon G, Casanova D, Bartoli JM, et al. Embolization of peripheral high-flow arteriovenous malformations with Onyx. Diagn Interv Imaging. 2017;98:217–26.

    Article  CAS  Google Scholar 

  30. Valek V, Husty J. Quality improvement guidelines for transcatheter embolization for acute gastrointestinal nonvariceal hemorrhage. Cardiovasc Intervent Radiol. 2013;36:608–12.

    Article  Google Scholar 

  31. Urbano J, Manuel Cabrera J, Franco A, Alonso-Burgos A. Selective arterial embolization with ethylene-vinyl alcohol copolymer for control of massive lower gastrointestinal bleeding: deasibilitiy and initial experience. J Vasc Interv Radiol. 2014;25:839–46.

    Article  Google Scholar 

  32. Saeed Kilani M, Izaaryene J, Cohen F, Varoquaux A, Gaubert JY, Louis G, et al. Ethylene vinyl alcohol copolymer (Onyx®) in peripheral interventional radiology: indications, advantages and limitations. Diagn Interv Imaging. 2015;96:319–26.

    Article  CAS  Google Scholar 

  33. Jagadeesan BD, Grigoryan M, Hassan AE, et al. Endovascular balloon-assisted embolization of intracranial and cervical arteriovenous malformations using dual-lumen coaxial balloon microcatheters and Onyx: initial experience. Neurosurgery. 2013;73(2 Suppl Operative):ons238–ons234.

    PubMed  Google Scholar 

  34. Sun X, Xu J, Zhang J, et al. Management of rectal bleeding due to internal haemorrhoids with arterial embolisation: a single-centre experience and protocol. Clin Radiol. 2018;73(11):985.e1-985.e6.

    Article  CAS  Google Scholar 

  35. Kanellos I, Goulimaris I, Christoforidis E, Kelpis T, Betsis D. A comparison of the simultaneous application of sclerotherapy and rubber band ligation, with sclerotherapy and rubber band ligation applied separately, for the treatment of haemorrhoids: a prospective randomized trial. Colorectal Dis. 2003;5:133.

    Article  CAS  Google Scholar 

  36. Plapler H. Hemorrhoids: an experimental model in monkeys. Acta Cirurgica Brasileira. 2006;21:354–6.

    Article  Google Scholar 

  37. Bernstein WC. What are hemorrhoids and what is their relationship to the portal venous system? Dis Colon Rectum. 1983;26(12):829–34.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Our study was financially supported by the Research Committee of French Society of Radiology. This funding source had no role in the design of this study, during its execution, analyses, interpretation of the data, or decision to submit results.

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Authors and Affiliations

  1. Department of Interventional Radiology, Marseille Public University Hospital System (APHM), La Timone University Hospital, 264 Rue Saint Pierre, 13385, Marseille, Cedex 05, France

    Farouk Tradi, Paul Habert & Vincent Vidal

  2. Experimental Interventional Imaging Laboratory (LIIE), UR 4264, Aix Marseille University, 27 boulevard Jean Moulin, 13005, Marseille, France

    Farouk Tradi, Julien Panneau, Pauline Brige, Paul Habert, Jean Francois Hak, Mathieu Di Bisceglie & Vincent Vidal

  3. Department of General and Visceral Surgery, APHM, La Timone University Hospital, 264 Rue Saint Pierre, 13385, Marseille, Cedex 05, France

    Diane Mege

  4. Vascular Research Center of Marseille (VRCM), INSERM UMR-S 1076, Aix Marseille University, 27 Boulevard Jean Moulin 13005, Marseille, France

    Diane Mege

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  1. Farouk Tradi
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  2. Julien Panneau
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Correspondence to Farouk Tradi.

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Figure 1

Angiography of the inferior mesenteric artery with a 4-French catheter (A). Distal placement of a 2.4-French micro-catheter above the pubic bone (B, black arrow) corresponding to the superior rectal artery bifurcation (C) (PNG 1503 KB)

Figure 2

3D reformats of pre-embolization angio-CT of a pig from group 1 (A), group 2 (B) and group 3 (C) and after CT scan from a human patient suffering from haemorrhoids (D). Similar course and bifurcation of the trunk and the bifurcation of the superior rectal artery between pig and human. Anastomoses with internal iliac arteries are well demonstrated (A and B, white arrows) (PNG 892 KB)

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Tradi, F., Panneau, J., Brige, P. et al. Evaluation of Multiple Embolic Agents for Embolization of the Superior Rectal Artery in an Animal Model. Cardiovasc Intervent Radiol 45, 510–519 (2022). https://doi.org/10.1007/s00270-021-03041-7

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  • DOI: https://doi.org/10.1007/s00270-021-03041-7

Keywords

  • Emborrhoid
  • Embolization
  • Hemorrhoids
  • Microspheres
  • Animal model