Effect of live and inactivated probiotic strains of Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis on myocardial infarction size in rats with systemic inflammatory response syndrome

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Within the concept of a heart-gut axis, new works are emerging to support the efficacy of probiotic strains to increase myocardial resistance to ischemia-reperfusion injury (IRI) in comorbidity. The question remains open whether the presence of live probiotic bacteria is a necessary condition for the realization of their cardioprotective effect. The aim of this work was to determine the manifestation of cardio-protective effect of living and pasteurized probiotic strains Lactobacillus acidophilus (LA-5) and Bifidobacterium animalis subsp. lactis (BB-12) in rats with systemic inflammatory response syndrome (SIRS). Myocardial resistance to IRI was assessed using an in vivo model of left coronary artery occlusion-reperfusion. Experiments were performed on male Wistar rats with improved conventional status with visceral obesity, chemically induced colitis and antibiotic-induced dysbiosis, which together provided the formation of (SIRS) against the background of oral administration of live and inactivated probiotic bacteria. Myocardial resistance to ischemia-reperfusion injury was assessed using the technique of left coronary artery occlusion in vivo. The infarct size in the group with simulated SIRS was significantly higher than in the control group 43% (39; 44) and 31% (28; 35), (p < 0.05). In the SIRS group with the introduction of inactivated probiotic bacteria, the infarct size 45% (37; 48) did not differ from the SIRS group and was significantly higher than in the control (p < 0.05). At the same time, the size of the infarction in the group with the introduction of live probiotics did not differ from that in the control group and amounted to 32% (28; 37). There are specific features of the action of live and inactivated probiotic microorganisms with preservation of cardioprotective effect when using live lacto- and bifidobacteria in animals with SIRS.

Full Text

Restricted Access

About the authors

Y. Y. Borshchev

Almazov National Medical Research Center of the Ministry of Health of the Russian Federation; National Medical Research Center of Oncology named after N.N. Petrov of the Ministry of Health of the Russian Federation

Email: burovenko.inessa@gmail.com
Russian Federation, St. Petersburg; St. Petersburg

D. L. Sonin

Almazov National Medical Research Center of the Ministry of Health of the Russian Federation; Pavlov First St. Petersburg State Medical University

Email: burovenko.inessa@gmail.com
Russian Federation, St. Petersburg; St. Petersburg

I. Y. Burovenko

Almazov National Medical Research Center of the Ministry of Health of the Russian Federation

Author for correspondence.
Email: burovenko.inessa@gmail.com
Russian Federation, St. Petersburg

E. S. Protsak

Almazov National Medical Research Center of the Ministry of Health of the Russian Federation

Email: burovenko.inessa@gmail.com
Russian Federation, St. Petersburg

V. Y. Borshchev

Pavlov First St. Petersburg State Medical University

Email: burovenko.inessa@gmail.com
Russian Federation, St. Petersburg

O. V. Borshcheva

Almazov National Medical Research Center of the Ministry of Health of the Russian Federation

Email: burovenko.inessa@gmail.com
Russian Federation, St. Petersburg

M. M. Galagudza

Almazov National Medical Research Center of the Ministry of Health of the Russian Federation; Pavlov First St. Petersburg State Medical University

Email: burovenko.inessa@gmail.com
Russian Federation, St. Petersburg; St. Petersburg

References

  1. Шляхто ЕВ, Петрищев НН, Галагудза ММ, Власов ТД, Нифонтов ЕМ (2013). Кардиопротекция: фундаментальные и клинические аспекты. CПб. ООО Студия “НП-Принт”. [Shlyakhto EV, Petrishchev NN, Galagudza MM, Vlasov TD, Nifontov EM (2013) Cardioprotection: fundamental and clinical aspects. SPb. OOO Studiya “NP-Print”. (In Russ)].
  2. Heusch G (2017) Critical Issues for the Translation of Cardioprotection. Circul Res 120(9): 1477–1486. https://doi.org/10.1161/CIRCRESAHA.117.310820
  3. Wang Q, Zuurbier CJ, Huhn R, Torregroza C, Hollmann MW, Preckel B, van den Brom CE, Weber NC (2023) Pharmacological Cardioprotection against Ischemia Reperfusion Injury-The Search for a Clinical Effective Therapy. Cells 12(10): 1432. https://doi.org/10.3390/cells12101432
  4. Roth GA, Mensah GA, Johnson CO, Addolorato G, Ammirati E, Baddour LM, Barengo NC, Beaton AZ, Benjamin EJ, Benziger CP, Bonny A, Brauer M, Brodmann M, Cahill TJ, Carapetis J, Catapano AL, Chugh SS, Cooper LT, Coresh J, Criqui M, DeCleene N, Eagle KA, Emmons-Bell S, Feigin VL, Fernández-Solà J, Fowkes G, Gakidou E, Grundy SM, He FJ, Howard G, Hu F, Inker L, Karthikeyan G, Kassebaum N, Koroshetz W, Lavie C, Lloyd-Jones D, Lu HS, Mirijello A, Temesgen AM, Mokdad A, Moran AE, Muntner P, Narula J, Neal B, Ntsekhe M, Moraes de Oliveira G, Otto C, Owolabi M, Pratt M, Rajagopalan S, Reitsma M, Ribeiro ALP, Rigotti N, Rodgers A, Sable C, Shakil S, Sliwa-Hahnle K, Stark B, Sundström J, Timpel P, Tleyjeh IM, Valgimigli M, Vos T, Whelton PK, Yacoub M, Zuhlke L, Murray C, Fuster V (2020) GBD-NHLBI-JACC Global Burden of Cardiovascular Diseases Writing Group. Global Burden of Cardiovascular Diseases and Risk Factors 1990-2019: Update From the GBD 2019 Study. J Am Coll Cardiol 76(25): 2982–3021. https://doi.org/10.1016/j.jacc.2020.11.010
  5. Kundu P, Blacher E, Elinav E, Pettersson S (2017) Our Gut Microbiome: The Evolving Inner Self. Cell 171(7): 1481–1493. https://doi.org/10.1016/j.cell.2017.11.024
  6. Forkosh E, Ilan Y (2019) The heart-gut axis: new target for atherosclerosis and congestive heart failure therapy. Open Heart 6(1): e000993. https://doi.org/10.1136/openhrt-2018-000993
  7. Lam V, Su J, Koprowski S, Hsu A, Tweddell JS, Rafiee P, Gross GJ, Salzman N H, Baker JE (2012) Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J: official publication of the Federation of Am Soc Exp Biol 26(4): 1727–1735. https://doi.org/10.1096/fj.11-197921
  8. Danilo CA, Constantopoulos E, McKee LA, Chen H, Regan JA, Lipovka Y, Lahtinen S, Sten- man LK, Nguyen TV, Doyle KP, Slepian MJ, Khalpey ZI, Konhilas JP (2017) Bifidobacterium animalis subsp. lactis 420 mitigates the pathological impact of myocardial infarction in the mouse. Benefic Microbes 8(2): 257–269. https://doi.org/10.3920/BM2016.0119
  9. Borshchev YY, Burovenko IY, Karaseva AB, Minasian SM, Protsak ES, Borshchev VY, Semeno- va NY, Borshcheva OV, Suvorov AN, Galagudza MM (2022) Probiotic Therapy with Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis Results in Infarct Size Limitation in Rats with Obesity and Chemically Induced Colitis. Microorganisms 10(11): 2293. https://doi.org/10.3390/microorganisms10112293
  10. Gan XT, Ettinger G, Huang CX, Burton JP, Haist JV, Rajapurohitam V, Sidaway JE, Martin G, Gloor GB, Swann JR, Reid G, Karmazyn M (2014) Probiotic administration attenuates myocardial hypertrophy and heart failure after myocardial infarction in the rat. Circ Heart Fail7(3): 491–499. https://doi.org/10.1161/CIRCHEARTFAILURE.113.000978
  11. Борщев ЮЮ, Буровенко ИЮ, Карасева АБ, Минасян СМ, Борщев ВЮ, Семенова НЮ, Борщева ОВ, Половинкин ВВ, Родионов ГГ, Суворов АН, Галагудза ММ (2020). Моделирование синдрома системной воспалительной реакции химической индукцией травмы толстого кишечника у крыс. Мед. иммунол. 22(1): 87–98. [Borschev YuYu, Burovenko IYu, Karaseva AB, Minasyan SM, Borschev VYu, Semenova NYu, Borshcheva OV, Polovinkin VV, Rodionov GG, Suvorov AN, Galagudza MM (2020) Modeling of systemic inflammatory response syndrome by chemical induction of colon injury in rats. Med Immunol 22(1): 87–98. (In Russ)]. https://doi.org/10.15789/1563-0625-MOS-1839
  12. Шендеров БА (2014). Микробная экология человека и ее роль в поддержании здоровья. Метаморфозы 5: 72–80. [Shenderov BA (2014) Human microbial ecology and its role in maintaining health. Metamorfozy 5: 72–80. (In Russ)].
  13. Ардатская МД (2015). Пробиотики, пребиотики и метабиотики в коррекции микроэкологических нарушений кишечника. Мед. совет 13: 94–99. [Ardatskaya MD (2015) Probiotics, prebiotics and metabiotics in the management of microecological bowel disorders. Med Sovet 13: 94–99. (In Russ)]. https://doi.org/10.21518/2079-701X-2015-13-94-99
  14. Бондаренко ВМ (2005). Метаболитные пробиотики: механизмы терапевтического эффекта при микроэкологических нарушениях. Consil Med 7: 437–443. [Bondarenko VM (2005) Metabolic probiotics: mechanisms of therapeutic effect in microecological disorders. Consil Med 7: 437–443. (In Russ)].
  15. Alfano M, Poli G (2005) Role of cytokines and chemokines in the regulation of innate immunity and HIV infection. Mol Immunol 42(2): 161–182. https://doi.org/10.1016/j.molimm.2004.06.016
  16. Godfried MH, Romijn JA, van der Poll T, Weverling GJ, Corssmit EP, Endert E, Eeftinck Schattenkerk, JK, Sauerwein HP (1995) Soluble receptors for tumor necrosis factor are markers for clinical course but not for major metabolic changes in human immunodeficiency virus infection. Metabol: Clin and Exp 44(12): 1564–1569. https://doi.org/10.1016/0026-0495(95)90076-4
  17. Spriggs DR, Deutsch S, Kufe DW (1992) Genomic structure, induction, and production of TNF-alpha. Immunol Series 56: 3–34.
  18. Wang X, Guo Z, Ding Z, Mehta JL (2018) Inflammation, Autophagy, and Apoptosis After Myocardial Infarction. J Am Heart Assoc 7(9): e008024. https://doi.org/10.1161/JAHA.117.008024
  19. Torti FM, Dieckmann B, Beutler B, Cerami A, Ringold GM (1985) A macrophage factor inhibits adipocyte gene expression: an in vitro model of cachexia. Science (New York) 229(4716): 867–869. https://doi.org/10.1126/science.3839597
  20. Breslow MJ, Min-Lee K, Brown DR, Chacko VP, Palmer D, Berkowitz DE (1999) Effect of leptin deficiency on metabolic rate in ob/ob mice. Am J Physiol 276(3): E443–E449. https://doi.org/10.1152/ajpendo.1999.276.3.E443
  21. Ghadge AA, Khaire AA (2019) Leptin as a predictive marker for metabolic syndrome. Cytokine 121: 154735. https://doi.org/10.1016/j.cyto.2019.154735
  22. Liu W, Zhou X, Li Y, Zhang S, Cai X, Zhang R, Gong S, Han X, Ji L (2020) Serum leptin, resistin, and adiponectin levels in obese and non-obese patients with newly diagnosed type 2 diabetes mellitus: A population-based study. Medicine 99(6): e19052. https://doi.org/10.1097/MD.0000000000019052
  23. Khafaji HA, Bener AB, Rizk NM, Al Suwaidi J (2012) Elevated serum leptin levels in patients with acute myocardial infarction; correlation with coronary angiographic and echocardiographic findings. BMC Res Notes 5: 262. https://doi.org/10.1186/1756-0500-5-262
  24. Schulze PC, Kratzsch J, Linke A, Schoene N, Adams V, Gielen S, Erbs S, Moebius-Winkler S, Schuler G (2003) Elevated serum levels of leptin and soluble leptin receptor in patients with advanced chronic heart failure. Eur J Heart Fail 5(1): 33–40. https://doi.org/10.1016/s1388-9842(02)00177-0
  25. Polyakova EA, Mikhaylov EN, Galagudza MM, Shlyakhto EV (2021) Hyperleptinemia results in systemic inflammation and the exacerbation of ischemia-reperfusion myocardial injury. Heliyon 7(11): e08491. https://doi.org/10.1016/j.heliyon.2021.e08491
  26. Smith CC, Yellon DM (2011) Adipocytokines, cardiovascular pathophysiology and myocardial protection. Pharmacol & Therap 129(2): 206–219. https://doi.org/10.1016/j.pharmthera.2010.09.003
  27. Кузнецов ИА, Потиевская ВИ, Качанов ИВ, Куралева ОО (2017). Роль лактоферрина в биологических средах человека. Совр. пробл. науки и образов. 3. [Kuznetsov IA, Potievskaya VI, Kachanov IV, Kuraleva OO (2017) The role of lactoferrin in human biological media. Sovr Probl Nauki Obrazov 3. (In Russ)]. http://www.science-education.ru/ru/article/view?id=26522
  28. Бойко ОВ, Ахминеева АХ, Гудинская НИ, Бойко ВИ, Козак ДМ, Бендюг ВА (2013). Биохимические и иммунологические маркеры в диагностике патологических состояний. Фундамент исслед. 9(3): 327–329. [Boyko OV, Akhmineeva AKh, Gudinskaya NI, Boyko VI, Kozak DM, Bendyug VA (2013) Biochemical and immunological markers in the diagnosis of pathological conditions. Fundament Issled 9: 327–329. (In Russ)]. https://fundamental-research.ru/ru/article/view?id=32347
  29. Коханов АВ, Мяснянкин АА, Метелкина ЕВ, Мусатов ОВ, Луцева ОА, Белопасов ВВ (2010). Фетальные и острофазовые белки как маркеры репаративных процессов. Междунар. журн. экспер. образов. 11: 89. [Kokhanov AV, Myasnyankin AA, Metelkina EV, Musatov OV, Lutseva OA, Belopasov VV (2010) Fetal and acute phase proteins as markers of reparative processes. Mezhdunar zhurn eksper obrazov 11: 89. (In Russ)]. https://expeducation.ru/ru/article/view?id=964
  30. Михайличенко ВЮ, Трофимов ПС, Кчибеков ЭА, Самарин СА, Топчиев МА, Биркун АА (2018). Оценка динамики уровня лактоферрина сыворотки крови в послеоперационном мониторинге больных, прооперированных по поводу распространенного перитонита. Тавр. мед.-биол. вестн. 21(1): 98–103. [Mikhaylichenko VYu, Trofimov PS, Kchibekov EA, Samarin SA, Topchiev MA, Birkun AA (2018) Assessment of the lactoferrin level in blood serum in the postoperative monitoring of patients operated on diffused peritonitis. Tavr Med-Biol Vestn 21(1): 98–103. (In Russ)].
  31. Луцева ОА, Коханов АВ, Воронкова МЮ, Иримиа РН, Зеленцова ЯВ (2019). Уровни лактоферрина в сыворотке крови и фекальном экстракте при некоторых воспалительных заболеваниях кишечника. Совр. пробл. науки и образов. 1: 46. [Lutseva OA, Kokhanov AV, Voronkova MYu, Irimia RN, Zelentsova YaV (2019) Serum and fecal extract lactoferrin levels in some inflammatory bowel diseases. Sovr Probl Nauki Obrazov 1: 46. (In Russ). https://science-education.ru/ru/article/view?id=28541

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig.1. Experimental design. CTR – control; SIRS – systemic inflammatory response syndrome; SIRS + LBS – SIRS and a mixture of LA-5 and BB-12; SIRS + INP – SIRS and inactivated probiotic. AA + E – a mixture of 3% acetic acid and 3% ethanol. AMC – antimicrobial mixture, HFCD – high fat and carbohydrate diet, Veh – saline solution. The details of the experiment are described in detail in the text.

Download (348KB)
3. Rice. 2. Double product of heart rate and blood pressure (a), Mean ± SD, size of myocardial infarction (b) and size of the risk zone (c), %, Me [25%; 75%]. * – p < 0.05 in relation to the KTP group. KTR – control; SIRS – systemic inflammatory response syndrome; SIVO + LBS – SIVO and a mixture of LA-5 and BB-12; SIRS + INP – SIRS and inactivated probiotic.

Download (456KB)

Copyright (c) 2024 Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies