Pathology

doi: 10.25005/2074-0581-2023-25-4-520-526
EXPERIMENTAL PERICARDITIS

E.A. LOZOVSKAYA, N.N. DREMINA, S.B. NIKIFOROV, I.A. SHURYGINA

Irkutsk Scientific Center for Surgery and Traumatology, Irkutsk, Russian Federation

Methods: The article discusses a pressing issue in cardiac surgery – the development of cicatricial adhesions and complications that arise from adhesive pericarditis, which can transform into a more severe condition known as constrictive pericarditis. The article also delves into the challenges of performing repeated cardiac surgery, the factors that trigger the adhesive process in the pericardium, and the etiopathogenetic mechanisms of fibrogenesis. These mechanisms involve the participation of active immune cells and the release of proinflammatory cytokines. Specifically, the article examines the features involved in the development of constrictive pericarditis, focusing on the cellular and molecular aspects of pericardial remodeling. It also evaluates the surgical and therapeutic measures currently used to prevent complications after cardiac surgery. Using original biological test systems involving experimental animals is advocated for a better understanding of the mechanisms underlying adhesive pericarditis after cardiac surgery and the development of effective prevention strategies. A range of experimental models of adhesions caused by pericarditis during open-heart surgery in mice is presented in this paper. The models include talc-induced pericarditis in mice, pigs, dogs, and rabbits, induced through the intrapericardial injection of Zymosan A, a known activator of the nucleotide-binding domain leucine-rich repeat and pyrin-containing protein 3 (NLRP3) inflammasome. Furthermore, the paper also covers mechanical methods of activation of pericarditis. These experimental models will help researchers explore the potential of new anti-adhesion drug molecules, which can be used in cardiac surgery.

Keywords: Cardiac surgery, constrictive pericarditis, mechanisms of fibrogenesis, prevention of pericarditis, experimental models of pericarditis.

Download file:


References
  1. Sengupta A, Yazdchi F, Alexis SL, Percy E, Premkumar A, Hirji S, et al. Reoperative mitral surgery versus transcatheter mitral valve replacement: A systematic review. J Am Heart Assoc. 2021;10(6):e019854. https://doi.org/10.1161/ JAHA.120.019854
  2. Keren MA, Kazaryan AV. Retsidiv ishemii posle otkrytoy revaskulyarizatsii miokarda: sovremennoe sostoyanie problemy, faktory riska, prognoz, taktika i rezul’taty povtornykh vmeshatel’stv [Recurrence of ischemia after open myocardial revascularization: Current status of the problem, risk factors, prognosis, tactics and results of repeated interventions]. Annaly khirurgii. 2017;22(5):257- 64. https://doi.org/10.18821/1560-9502-2017-22-5-257-264a
  3. Arutyunov GP, Paleev FN, Tarlovskaya EI, Moiseeva OM, Arutyunov AG, Koziolova NA, i dr. Perikardity. Klinicheskie rekomendatsii 2022 [Pericarditis. Clinical recommendations 2022]. Rossiyskiy kardiologicheskiy zhurnal. 2023;28(3):5398. https://doi.org/10.15829/1560-4071-2023-5398
  4. Makoto M, Yun W, Karthik M, Rohan K, Aakriti G, Prashanth V, et al. Trends in reoperative coronary artery bypass graft surgery for older adults in the United States, 1998 to 2017. J Am Heart Assoc. 2020;9(20):e016980. https://doi. org/10.1161/JAHA.120.016980.
  5. Bokeriya LA, Sivtsev VS. Posleoperatsionnyy spaechnyy perikardit: faktory riska, patogenez i metody profilaktiki [Postoperative adhesive pericarditis: Risk factors, pathogenesis, and methods of prevention]. Annaly khirurgii. 2014;6:7- 15.
  6. Imazio M, Gaita F, LeWinter M. Evaluation and treatment of pericarditis: A systematic review. JAMA. 2015;314(14):1498-506. https://doi.org/10.1001/ jama.2015.12763
  7. Zhou Z-f, Zhai W, Yu L-n , Sun K , Sun L-h , Xing X-f, et al. Comparison of the in-vivo effect of two tranexamic acid doses on fibrinolysis parameters in adults undergoing valvular cardiac surgery with cardiopulmonary bypass – a pilot investigation. BMC Anesthesiol. 2021;21:33. https://doi.org/10.1186/s12871- 021-01234-8
  8. Ren K, Duan W, Liang Z, Yu B, Li B, Jin Z, et al. Glutaraldehyde and 2,3-butanediol treatment of bovine pericardium for aortic valve bioprosthesis in sheep: A preliminary study. Ann Transl Med. 2020;8(24):1668. https://doi.org/10.21037/ atm-20-7803
  9. Ghoreishi M, Dawood M, Hobbs G, Pasrija C, Riley P, Petrose L, et al. Repeat sternotomy: No longer a risk factor in mitral valve surgical procedures. Ann Thorac Surg. 2013;96(4):1358-65. https://doi.org/10.1016/j.athoracsur.2013.05.064
  10. Ivanov SV, Sotnikov AV, Malyshenko ES, Sumin AN, Kazachek YaV, Bezdenezhnykh AV, i dr. Rezul'taty povtornykh operatsiy koronarnogo shuntirovaniya [Results of repeated coronary bypass operations]. Kardiologiya i serdechno-sosudistaya khirurgiya. 2014;7(3):4-11.
  11. Cannata A, Petrella D, Bruschi G, Fratto P, Gambacorta M, Martinelli L. Postsurgical intrapericardial adhesions: Mechanisms of formation and prevention. Ann Thorac Surg. 2013;95(5):1818-26. https://doi.org/10.1016/j.athoracsur.2012.11.020
  12. Johnston DR. Surgical management of pericardial diseases. Prog Cardiovasc Dis. 2017;59(4):407-16. https://doi.org/10.1016/j.pcad.2017.01.005
  13. Vinasha R, Bongani MM, Sturrock ED, Ntsekhe M. Established and novel pathophysiological mechanisms of pericardial injury and constrictive pericarditis. World J Cardiol. 2018;10(9):87-96. https://doi.org/10.4330/wjc.v10.i9.87
  14. Hassanabad AF, Zarzycki AN, Jeon K, Dundas JA, Vasanthan V, Deniset JF, et al. Prevention of post-operative adhesions: A comprehensive review of present and emerging strategies. Biomolecules. 2021;11(7):1027. https://doi. org/10.3390/biom11071027
  15. Frangogiannis NG. Cardiac fibrosis. Cardiovasc Res. 2021;117(6):1450-88. https://doi.org/10.1093/cvr/cvaa324
  16. Tzavlaki K, Moustakas A. TGF-β Signaling. Biomolecules. 2020;10(3):487. https://doi.org/10.3390/biom10030487
  17. Liao J, Li X, Fan Y. Prevention strategies of postoperative adhesion in soft tissues by applying biomaterials: Based on the mechanisms of occurrence and development of adhesions. Bioact Mater. 2023;26:387-412. https://doi. org/10.1016/j.bioactmat.2023.02.026
  18. Vogiatzidis K, Zarogiannis SG, Aidonidis I, Solenov EI, Molyvdas PA, Gourgoulianis KI, et al. Physiology of pericardial fluid production and drainage. Front Physiol. 2015;6:62. https://doi.org/10.3389/fphys.2015.00062
  19. Ezeani M, Noor A, Donnelly P.S, Niego B, Hagemeyer C.E. Assessment of the epi-pericardial fibrotic substrate by collagen-targeted probes. Sci Rep. 2022;12:5702. https://doi.org/10.1038/s41598-022-08688-x
  20. Zhao M, Wang L, Wang M, Zhou S, Lu Y, Cui H, et al. Targeting fibrosis: Mechanisms and clinical trials. Signal Transduct Target Ther. 2022;7:206. https://doi. org/10.1038/s41392-022-01070-3
  21. Wong CKS, Falkenham A, Myers T, Légaré J-F. Connective tissue growth factor expression after angiotensin II exposure is dependent on transforming growth factor-β signaling via the canonical Smad-dependent pathway in hypertensive induced myocardial fibrosis. J Renin Angiotensin Aldosterone Syst. 2018;19(1):1470320318759358. https://doi.org/10.1177/1470320318759358
  22. Accornero F, Berlo JH, Correll RN, Elrod JW, Sargent MA, York A, et al. Genetic analysis of connective tissue growth factor as an effector of transforming growth factor β signaling and cardiac remodeling. Mol Cell Biol. 2015;35(12):2154-64. https://doi.org/10.1128/MCB.00199-15
  23. Ma Z-G, Yuan Y-P, Wu H-M, Zhang X, Tang Q-Z. Cardiac fibrosis: New insights into the pathogenesis. Int J Biol Sci. 2018;14(12):1645-57. https://doi. org/10.7150/ijbs.28103
  24. Hill MA, Walkowiak OA, Head WT, Kwon JH, Kavarana MN, Rajab TK. A review of animal models for post-operative pericardial adhesions. Front Surg. 2022;9:966410. https://doi.org/10.3389/fsurg.2022.966410
  25. Raval J, Nagaraja V, Eslick GD, Denniss AR. The Role of colchicine in pericarditis – a systematic review and meta-analysis of randomised trials. Heart Lung Circ. 2015;24(7):660-6. https://doi.org/10.1016/j.hlc.2015.01.010
  26. Avondo S, Andreis A, Casula M, Biondi-Zoccai G, Imazio M. Pharmacologic treatment of acute and recurrent pericarditis: A systematic review and meta-analysis of controlled clinical trials. Panminerva Med. 2021;63(3):314-323. https://doi.org/10.23736/S0031-0808.21.04263-4
  27. Kaznacheev NN, Gladkikh VG, Ivanov VA, Gubarev EA, Pechenin OD. Sposob modelirovaniya perikardita [A way of modeling pericarditis]. Patent SU1446641, 1988.
  28. Kojima A, Tomohisa S, Mikio O, Fumiaki S, Mie K, Yuuki I, et al. A simple mouse model of pericardial adhesions. J Card Surg. 2019;14:124-9. https://doi. org/10.1186/s13019-019-0940-9
  29. Hill M.A, Walkowiak OA, Head WT, Kwon JH, Kavarana MN, Rajab TK. A review of animal models for post-operative pericardial adhesions. Front Surg. 2022;9:966410. https://doi.org/10.3389/fsurg.2022.966410
  30. Mauro AG, Bonaventura A, Vecchié A. The role of NLRP3 inflammasome in pericarditis: Potential for therapeutic approaches. J Am Coll Cardiol Basic Trans Science. 2021; 6:137-50. https://doi.org/10.1016/j.jacbts.2020.11.016
  31. Aghajani H, Yazdani S, Forouzan NSK, Vahidi H, Aghajani F, Tehran J. Dog footprint in the heart. Heart Cent. 2016;11(4):198-202.
  32. Colak N, Nazli Y, Alpay MF, Aksoy ON, Akkaya IO, Bayrak R, et al. Effect of topical N-acetylcysteine in the prevention of postoperative pericardial adhesion formation in a rabbit model. Card Pathol. 2013;22:368-72. https://doi. org/10.1016/j.carpath.2013.02.001
  33. Shurygina IA, Shurygin MG, Zelenin NV, Ayushinova NI. Vozdeystvie na mitogenaktiviruemye proteinkinazy kak novoe napravlenie regulyatsii rosta soedinitel′noy tkani [Effects on mitogen-activated protein kinases as a new direction of regulation of connective tissue growth]. Byulleten′ sibirskoy meditsiny. 2017;16(4):86-93.
  34. Shurygina IA, Shurygin MG, Dremina NN, Lozovskaya EA, Trukhan IS. Kompozitsiya dlya profilaktiki rubtsovo-spaechnykh oslozhneniy v kardiokhirurgii i sposob eyo primeneniya [Composition for prophylaxis of scar and adhesion complications in cardiac surgery and method of its application]. Zayavka na patent RF № 2023115084/20(032152). Data prioriteta 06.06.2023.

Authors' information:


Lozovskaya Evgeniya Aleksandrovna,
Сandidate of Veterinary Sciences, Senior Researcher of the Scientific Department of Experimental Surgery with a Vivarium, Irkutsk Scientific Center for Surgery and Traumatology
ORCID ID: 0000-0003-3851-128X
SPIN: 5547-3856
Author ID: 965503
E-mail: molodegny31@mail.ru

Dremina Natalya Nikolaevna,
Сandidate of Biological Sciences, Senior Researcher of the Laboratory of Сellular Technologies and Regenerative Medicine, Irkutsk Scientific Center for Surgery and Traumatology
Scopus ID: 36243115900
ORCID ID: 0000-0002-2540-4525
SPIN: 8038-3583
Author ID: 605510
E-mail: drema76@mail.ru

Nikiforov Sergey Borisovich,
Doctor of Medical Sciences, Leading Researcher of the Scientific Department of Experimental Surgery with a Vivarium, Irkutsk Scientific Center for Surgery and Traumatology
ORCID ID: 0000-0002-0486-9235
SPIN: 7451-4149
Author ID: 395777
E-mail: telomer@mail.ru

Shurygina Irina Aleksandrovna,
Doctor of Medical Sciences, Full Professor, Deputy Director for Research, Irkutsk Scientific Center of Surgery and Traumatology
Researcher ID: B-4059-2018
Scopus ID: 36244455300
ORCID ID: 0000-0003-3980-050X
SPIN: 6745-5426
Author ID: 161435
E-mail: irinashurygina@gmail.com

Information about support in the form of grants, equipment, medications

The research was carried out in accordance with the research plan of Irkutsk Scientific Center of Surgery and Traumatology (state registration number – 122022200212-6). The authors did not receive financial support from manufacturers of medicines and medical equipment

Conflicts of interest: No conflict

Address for correspondence:


Lozovskaya Evgeniya Aleksandrovna
Сandidate of Veterinary Sciences, Senior Researcher of the Scientific Department of Experimental Surgery with a Vivarium, Irkutsk Scientific Center for Surgery and Traumatology

664003, Russian Federation, Irkutsk, Bortsov Revolyutsii str., 1

Tel.: +7 (3952) 290336

E-mail: molodegny31@mail.ru

Materials on the topic: