Pathology of the peripheral circulation in chronic heart failure

In the mechanisms of chronic heart failure (CHF) the key role traditionally given to a violation of intracardiac haemocirculation. Thus, in the guidelines for the evaluation and management of chronic heart failure in the adult, experts of the American College of Cardiology and the American Heart Association (2001-2013) define CHF as «a complex clinical syndrome that can result from any structural or functional cardiac disorder that impairs the ability of the ventricle to fill with or eject blood». Usually rightly believe that than the expression of inotropic and/or lusitropic failure of the appropriate ventricle in patients with CHF, the generally lower of him quality of life and a worse prognosis. However, the severity of the clinical manifestations of heart failure, on the one hand, and reducing the level of satisfaction with life - on the other, is not always depends only on the state of intracardiac hemodynamics. The authors of the review have analyzed papers published on the problem of the pathology of the peripheral circulation in CHF. Consistently examines the role of peripheral vascular remodeling and increased arterial stiffness, endothelial dysfunction of major and resistance arteries, as well as pathology of microcirculation. It has been shown that the development and progression of heart failure is accompanied by a deterioration in the peripheral circulation due to the remodeling of arteries muscular-elastic type and veins with a reduction in vascular dilatation reserve, increase of regional vascular resistance and venous tone, disturbances of tissue transcapillary exchange of oxygen and activate of procoagulant properties of blood. The significance of the effects of vasoconstrictor neurohormonal systems and inflammation in mechanisms of disorders of peripheral circulation in patients with CHF, particularly associated with the metabolic syndrome, have discussed.

chronic heart failure, peripheral circulation, vascular remodeling, arterial stiffness, endothelial dysfunction, inflammation, hypercoagulation, pathology of microcirculation

1. Tanai E., Frantz S. Pathophysiology of heart failure // Compr. Physiol. 2015; 6 (1): 187–214. doi: 10.1002/cphy.c140055.

2. Knudson J.D., Cabrera A.G. The pathophysiology of heart failure in children: the basics // Curr. Cardiol. Rev. 2016; 12 (2): 99–103. doi: 10.2174/1573403X12666151119164525.

3. Mazurek J.A., Jessup M. Understanding heart failure // Card. Electrophysiol. Clin. 2015; 7 (4): 557–575. doi: 10. 1016/j.ccep.2015.08.001.

4. Kalyuzhin V.V., Kalyuzhin O.V., Teplyakov A.T., Karaulov A.V. Hronicheskaja serdechnaja nedostatochnost’ [Chronic heart failure ]. Moscow: Medical information agency Publ., 2006: 288 (in Russian).

5. Koronarnaja i serdechnaja nedostatochnost’: kollektivnaja monografija [Coronary and heart failure: a collective monograph] / ed. by R.S. Karpov, Tomsk: STT Publ., 2005: 716 (in Russian).

6. Arutjunov G.P., Belenkov Ju.N., Vasjuk Ju.A., Mareev Ju.V., Sitnikova M.Ju., Fomin I.V. Hronicheskaja serdechnaja nedostatochnost’: rukovodstvo [Chronic heart failure: guide]. Moscow: GEOTAR-Media Publ., 2010: 336 (in Russian).

7. MacIver D.H., Dayer M.J., Harrison A.J. A general theory of acute and chronic heart failure // Int. J. Cardiol. 2013; 165 (1): 25–34. doi: 10.1016/j.ijcard.2012.03.093.

8. Yancy C.W., Jessup M., Bozkurt B., Butler J., Casey D.E. Jr, Drazner M.H., Fonarow G.C., Geraci S.A., Horwich T., Januzzi J.L., Johnson M.R., Kasper E.K., Levy W.C., Masoudi F.A., McBride P.E., McMurray J.J., Mitchell J.E., Peterson P.N., Riegel B., Sam F., Stevenson L.W., Tang W.H., Tsai E.J., Wilkoff B.L. 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines // J. Am. Coll. Cardiol. 2013; 62 (16): e147–e239. doi: 10.1016/j.jacc.2013.05.019.

9. Nabati M., Salehi S., Bagheri B., Nouraei M. Abnormal left ventricular relaxation and symptoms of heart failure // J. Echocardiogr. 2016; 14 (3): 113–119. doi: 10.1007/s12574-016-0287-3.

10. Obokata M., Takeuchi M., Negishi K., Ohte N., Izumo M., Yamashita E., Ebato M., Yuda S., Kurabayashi M., Nakatani S. Relation between echocardiogram-based cardiac parameters and outcome in heart failure with preserved and reduced ejection fraction // Am. J. Cardiol. 2016; 118 (9): 1356–1362. doi: 10.1016/j.amjcard.2016.07.060.

11. Nagueh S.F., Smiseth O.A., Appleton C.P., Byrd B.F. 3rd, Dokainish H., Edvardsen T., Flachskampf F.A., Gillebert T.C., Klein A.L., Lancellotti P., Marino P., Oh J.K., Popescu B.A., Waggoner A.D. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging // J. Am. Soc. Echocardiogr. 2016; 29 (4): 277–314. doi: 10.1016/j.echo.2016.01.011.

12. Kalyuzhin V.V., Teplyakov A.T., Solovcov M.A. Rol’ sistolicheskoj i diastolicheskoj disfunkcii levogo zheludochka v klinicheskoj manifestacii hronicheskoj serdechnoj nedostatochnosti u bol’nyh, perenesshih infarkt miokarda [The role of systolic and diastolic left ventricular dysfunction in clinical manifestations of chronic heart failure in patients after myocardial infarction] // Terapevticheskiy Arkhiv – Therapeutic archive. 2002; 74 (12): 15–18 (in Russian).

13. Kalyuzhin V.V., Teplyakov A.T., Rjazanceva N.V., Bespalova I.D., Kamaev D.Ju., Kalyuzhina E.V. Kachestvo zhizni bol’nyh ishemicheskoj bolezn’ju serdca, associirovannoj s metaboli-cheskim sindromom: rezul’taty faktornogo analiza [Quality of life in patients with ischemic heart disease associated with metabolic syndrome: results of factor analysis] // Terapevticheskiy Arkhiv – Therapeutic archive. 2012; 84 (12): 18–22 (in Russian).

14. Kalyuzhin V.V., Teplyakov A.T., Ryazantseva N.V., Vechersky Y.Y., Khlapov A.P., Kolesnikov R.N. Diastola serdca. Fiziologija i klinicheskaja patofiziologija [Diastole of the heart. Physiology and clinical pathophysiology]. Tomsk: TPU Publ., 2007: 212 (in Russian).

15. Singh T.P., Blume E.D., Alexander P.M., Gauvreau K. Association of hemodynamic profiles with wait-list mortality in children listed for heart transplantation with idiopathic dilated cardiomyopathy // Am. J. Cardiol. 2015; 115 (2): 243–248. doi: 10.1016/j.amjcard.2014.10.030.

16. Gupte A.A., Hamilton D.J. Exercise intolerance in heart failure with preserved ejection fraction // Methodist Debakey Cardiovasc. J. 2016; 12 (2): 105–109. doi: 10.14797/mdcj-12-2-105.

17. Spee R.F., Niemeijer V.M., Wessels B., Jansen J.P., Wijn P.F., Doevendans P.A., Kemps H.M. Characterization of exercise limitations by evaluating individual cardiac output patterns: a prospective cohort study in patients with chronic heart failure // BMC Cardiovasc. Disord. 2015; 15: 57. doi: 10.1186/s12872-015-0057-6.

18. Hasselberg N.E., Haugaa K.H., Sarvari S.I., Gullestad L., Andreassen A.K., Smiseth O.A., Edvardsen T. Left ventricular global longitudinal strain is associated with exercise capacity in failing hearts with preserved and reduced ejection fraction // Eur. Heart J. Cardiovasc. Imaging. 2015; 16 (2): 217–224. doi: 10.1093/ehjci/jeu277.

19. Sharpe N., Doughty R. Epidemiology of heart failure and ventricular dysfunction // Lancet. 1998; 352 (Suppl. 1): SI3–SI7.

20. Bojcov S.A. Central’nye i perifericheskie mehanizmy patogeneza hronicheskoj serdechnoj nedostatochnosti [Central and peripheral mechanisms of the pathogenesis of chronic heart failure] // Zhurnal serdechnaja nedostatochnost’. 2005; 6 (2): 78–83 (in Russian).

21. Nilsson K.R., Duscha B..D, Hranitzky P.M., Kraus W.E. Chronic heart failure and exercise intolerance: the hemodynamic paradox // Curr. Cardiol Rev. 2008; 4 (2): 92–100. doi: 10.2174/157340308784245757.

22. Witte K.K., Clark A.L. Why does chronic heart failure cause breathlessness and fatigue? // Prog. Cardiovasc. Dis. 2007; 49 (5): 366–384. doi: 10.1016/j.pcad.2006.10.003

23. Clark A.L. Origin of symptoms in chronic heart failure // Heart. 2006; 92 (1): 12–16. doi: 10.1136/hrt.2005.066886.

24. Johnson M.J., Clark A.L. The mechanisms of breathlessness in heart failure as the basis of therapy // Curr. Opin. Support Palliat. Care. 2016; 10 (1): 32–35. doi: 10.1097/SPC.0000000000000181.

25. Florja V.G., Mareev V.Ju., Belenkov Ju.N., Achilov A.A. Serdce i periferija pri nedostatochnosti krovoobrashhenija. Svjaz’ s tolerantnost’ju k nagruzke [Heart and periphery with circulatory failure. The relationship with exercise tolerance] // Kardiologiya. 1995; 35 (5): 37–42 (in Russian).

26. Clark A.L., Poole-Wilson P.A., Coats A.J. Exercise limitation in chronic heart failure: central role of the periphery // J. Am. Coll. Cardiol. 1996; 28: 1092–1102.

27. Cowley A.J., Fullwood L., Muller A.F., Stainer K., Skene A.M., Hampton J.R. Exercise capability in heart failure: is cardiac output important after all?// Lancet. 1991; 337 (8744): 771–773.

28. Coats A.J. Heart failure: what causes the symptoms of heart failure? // Heart. 2001; 86 (5): 574–578.

29. Upadhya B., Haykowsky M.J., Eggebeen J., Kitzman D.W. Exercise intolerance in heart failure with preserved ejection fraction: more than a heart problem // J. Geriatr. Cardiol. 2015; 12 (3): 294–304. doi: 10.11909/j.issn.1671-5411.2015.03.013.

30. Kosmala W., Rojek A., Przewlocka-Kosmala M., Mysiak A., Karolko B., Marwick T.H. Contributions of nondiastolic factors to exercise intolerance in heart failure with preserved ejection fraction // J. Am. Coll. Cardiol. 2016; 67 (6): 659–670. doi: 10.1016/j.jacc.2015.10.096.

31. Hopkinson N.S., Dayer M.J., Antoine-Jonville S., Swallow E.B., Porcher R., Vazir A., Poole-Wilson P., Polkey M.I. Central and peripheral quadriceps fatigue in congestive heart failure // Int. J. Cardiol. 2013; 167 (6): 2594–2599. doi: 10.1016/j.ijcard.2012.06.064.

32. Witman M.A., Ives S.J., Trinity J.D., Groot H.J., Stehlik J., Richardson R.S. Heart failure and movement-induced hemodynamics: partitioning the impact of central and peripheral dysfunction // Int. J. Cardiol. 2015; 178: 232–238. doi: 10.1016/j.ijcard.2014.10.044.

33. Oliveira M.F., Arbex F.F., Alencar M.C., Souza A., Sperandio P.A., Medeiros W.M., Mazzuco A., Borghi-Silva A., Medina L.A., Santos R., Hirai D.M., Mancuso F., Almeida D., O’Donnell D.E., Neder J.A. Heart failure impairs muscle blood flow and endurance exercise tolerance in COPD // COPD. 2016; 13 (4): 407–415. doi: 10.3109/15412555.2015.1117435.

34. Lee J.F., Barrett-O’Keefe Z., Garten R.S., Nelson A.D., Ryan J.J., Nativi J.N,. Richardson R.S., Wray D.W. Evidence of microvascular dysfunction in heart failure with preserved ejection fraction // Heart. 2016; 102 (4): 278–284. doi: 10.1136/heartjnl-2015-308403.

35. Vasilenko V.H. Nedostatochnost’ krovoobrashhenija [Circulatory failure] / Bol’shaja medicinskaja jenciklopedija [The big medical encyclopedia]; Ed. 2. / ed. by A.N. Bakulev, Moscow, Soviet encyclopedia Publ., 1960; 14: 543–604 (in Russian).

36. Cingolani H.E., Pérez N.G., Cingolani O.H., Ennis I.L. The Anrep effect: 100 years later // Am. J. Physiol. Heart Circ. Physiol. 2013; 304 (2): H175–H182. doi: 10.1152/ajpheart.00508.2012.

37. Kalyuzhin V.V., Teplyakov A.T., Vecherskij Ju.Ju., Rjazanceva N.V., Hlapov A.P. Patogenez hronicheskoj serdechnoj nedostatochnosti: izmenenie dominirujushhej paradigmy [The pathogenesis of chronic heart failure: the change in the dominant paradigm] // Byulleten’ sibirskoy meditsiny – Bulletin of Siberian Medicine. 2007; 6 (4): 71–79 (in Russian).

38. Hartupee J., Mann D.L. Neurohormonal activation in heart failure with reduced ejection fraction // Nat. Rev. Cardiol. 2016; Oct 6. doi: 10.1038/nrcardio.2016.163 [Epub ahead of print].

39. Ol’binskaja L.I. Pred- i poslenagruzka na serdce pri nedostatochnosti krovoobrashhenija u bol’nyh postinfarktnym kardiosklerozom [Pre- and afterload on the heart at circulatory failure in patients with post-infarction cardiosclerosis] // Kardiologiya. 1987; 27 (12): 5–7 (in Russian).

40. Florja V.G., Popovich M.I., Kostin S.I., Severin V.V., Mareev V.Ju., Belenkov Ju.N. Remodelirovanie perifericheskih sosudov soprovozhdaet stanovlenie hronicheskoj nedostatochnosti krovoobrashhenija u bol’nyh ishemicheskoj bolezn’ju serdca [Peripheral vascular remodeling is accompanied by the formation of chronic circulatory failure in patients with ischemic heart disease] // Kardiologiya. 1998; 38 (4): 14–19 (in Russian).

41. Fang Y.C., Yeh C.H. Role of microRNAs in vascular remodeling // Curr. Mol. Med. 2015; 15 (8): 684–696. doi: 10.2174/1566524015666150921105031.

42. Wei Y., Schober A., Weber C. Pathogenic arterial remodeling: the good and bad of microRNAs // Am. J. Physiol. Heart Circ. Physiol. 2013; 304 (8): H1050–H1059. doi: 10.1152/ajpheart.00267.2012.

43. Santulli G. MicroRNAs and endothelial (dys) function // J. Cell Physiol. 2016; 231 (8): 1638–1644. doi: 10.1002/jcp.25276.

44. Kochetov A.G., Lyang O.V., Gimadiev R.R., Abramov A.A., Zhirov I.V., Skvortsov A.A., Zaseeva A.V., Bosykh E.G., Masenko V.P., Tereshchenko S.N. Jekspressija cirkulirujushhih mikroRNK pri razvitii hronicheskoj serdechnoj nedostatochnosti u bol’nyh s serdechno- sosudistymi zabolevanijam [Expression of circulating microRNA in chronic heart failure in patients with cardiovascular pathologies] // Laboratornaya sluzhba. 2016; 5 (1): 26–32 (in Russian). doi: 10.17116/labs20165126-32.

45. Belenkov Ju.N., Mareev V.Ju. Serdechno-sosudistyj kontinuum [The cardiovascular continuum] // Zhurnal serdechnaja nedostatochnost’. 2002; 3 (1): 7–11 (in Russian).

46. Kalyuzhin V.V., Teplyakov A.T., Solovtsov M.A., Kalyuzhina E.V., Bespalova I.D., Terentyeva N.N. Remodelirovanie levogo zheludochka: odin ili neskol’ko scenariev? [Remodeling of the left ventricle: one or several scenarios?] // Byulleten’ sibirskoy meditsiny – Bulletin of Siberian Medicine. 2016; 15 (4): 120–139 (in Russian). doi: 10.20538/1682-0363-2016-4-120-139

47. Kalogeropoulos A.P., Georgiopoulou V.V., Butler J. From risk factors to structural heart disease: the role of inflammation // Heart Fail. Clin. 2012; 8 (1): 113–123. doi: 10.1016/j.hfc.2011.08.002.

48. Wang M., Shah A.M. Age-associated pro-inflammatory remodeling and functional phenotype in the heart and large arteries // J. Mol. Cell. Cardiol. 2015; 83: 101–111. doi: 10.1016/j.yjmcc.2015.02.004.

49. Беспалова И.Д., Рязанцева Н.В., Калюжин В.В., Афанасьева Д.С., Мурашев Б.Ю., Осихов И.А. Системное воспаление в патогенезе метаболического синдрома и ассоциированных с ним заболеваний // Сибирский медицинский журнал (Иркутск). 2013; 117 (2): 5–9. doi: 10.1234/XXXX-XXXX-2013-2-5-9.

50. Martínez-Martínez E., Miana M., Jurado-López R., Bartolomé M.V., Souza Neto F.V., Salaices M., López-Andrés N., Cachofeiro V. The potential role of leptin in the vascular remodeling associated with obesity // Int. J. Obes. (Lond). 2014; 38 (12): 1565–1572. doi: 10.1038/ijo.2014.37.

51. Rudenko T.E., Kutyrina I.M. Ozhirenie kak faktor sosudistogo remodelirovanija [Obesity as a factor of vascular remodeling] // Klinicheskaja nefrologija. 2010; 3: 62–67 (in Russian).

52. Katsiki N., Doumas M., Mikhailidis D.P. Lipids, statins and heart failure: an update // Curr. Pharm. Des. 2016; 22 (31): 4796–4806. doi: 10.2174/1381612822666160701073452.

53. Bespalova I.D., Ryazantseva N.V., Kalyuzhin V.V., Murashev B.Yu., Osikhov I.A., Medyantsev Yu.A. Vlijanie atorvastatina na provospalitel’nyj status (in vivo i in vitro) bol’nyh gipertonicheskoj bolezn’ju s metabolicheskim sindromom [Effect of atorvastatin on pro-inflammatory status (in vivo и in vitro) in patients with essential hypertension and metabolic syndrome] // Kardiologiya. 2014; 54 (8): 37–43 (in Russian). doi: 10.18565/cardio.2014.8.37-43.

54. Athyros V.G., Katsiki N., Karagiannis A. Is Targeting microRNAs the philosopher’s stone for vascular disease? // Curr. Vasc. Pharmacol. 2016; 14 (1): 88–97. doi: 10.217 4/1570161113666150401101603.

55. Namba T., Masaki N., Matsuo Y., Sato A., Kimura T., Horii S., Yasuda R., Yada H., Kawamura A., Takase B., Adachi T. Arterial stiffness is significantly associated with left ventricular diastolic dysfunction in patients with cardiovascular disease // Int. Heart J. 2016; 57 (6): 729–735. doi: 10.1536/ihj.16-112.

56. Drapkina O.M., Kaburova A.N. Zhestkost’ sosudov i diastolicheskaja serdechnaja nedostatochnost’ [Vascular stiffness and diastolic heart failure] // Terapevticheskiy Arkhiv – Therapeutic Archive. 2013; 85 (11): 75–81 (in Russian).

57. Teplyakov A.T., Pushnikova E.Ju., Andrijanova A.V., Kalyuzhin V.V., Suslova T.E., Nikonova E.N., Karpov R.S. Miokardial’naja i arterial’naja zhestkost’ - vazhnaja determinanta jekspressii N-koncevogo predshestvennika mozgovogo natrijureticheskogo peptida pri razvitii serdechnoj nedostatochnosti u pacientov, perenesshih infarkt miokarda [Myocardial and arterial stiffness, an important determinant in the expression of N-terminal precursor of brain natriuretic peptide in the development of heart failure in patients with myocardial infarction] // Kardiologiya. 2016; 56 (4): 42–48 (in Russian). doi: 10.18565/cardio.2016.4.42-48.

58. Zamani P., Lilly S.M., Segers P., Jacobs D.R.Jr, Bluemke D.A., Duprez D.A., Chirinos J.A. Pulsatile load components, resistive load and incident heart failure: The Multi-Ethnic Study of Atherosclerosis (MESA) // J. Card. Fail. 2016; 22 (12): 988–995. doi: 10.1016/j.cardfail.2016.04.011.

59. Bauersachs J., Widder J.D. Endothelial dysfunction in heart failure // Pharmacol. Rep. 2008; 60 (1): 119–126.

60. Olbinskaya L.I., Sizova Zh.M., Ushakova A.V. Jendotelial’naja disfunkcija u bol’nyh ishemicheskoj bolezn’ju serdca, oslozhnennoj hronicheskoj serdechnoj nedostatochnost’ju, i vozmozhnosti korrekcii izosorbid-5-mononitratom [Endothelial dysfunction in patients with ischemic heart disease complicated by chronic heart failure and possibilities of its correction with isosorbide-5-mononitrate] // Kardiologiya. 2001; 41 (3): 29–32 (in Russian).

61. Belenkov Yu.N., Mareev V.Yu., Ageev F.T. Jendotelial’naja disfunkcija pri serdechnoj nedostatochnosti: vozmozhnosti terapii ingibitorami angiotenzinprevrashhajushhego fermenta [Endothelial dysfunction in heart failure: possibilities of therapy with angiotensin converting enzyme inhibitors] // Kardiologiya. 2001; 41 (5): 100–104 (in Russian).

62. Daiber A., Steven S., Weber A., Shuvaev V.V., Muzykantov V.R., Laher I., Li H., Lamas S., Münzel T. Targeting vascular (endothelial) dysfunction // Br. J. Pharmacol. 2016 May 17. doi: 10.1111/bph.13517. [Epub ahead of print].

63. Cahill P.A., Redmond E.M. Vascular endothelium – Gatekeeper of vessel health // Atherosclerosis. 2016; 248: 97–109. doi: 10.1016/j.atherosclerosis.2016.03.007.

64. Aronov D.M. Lechenie i profilaktika ateroskleroza [Treatment and prevention of atherosclerosis]. Moscow: “Triada-H” Publ., 2000: 412 (in Russian).

65. Boulanger C.M. Endothelium // Arterioscler. Thromb. Vasc. Biol. 2016; 36 (4): e26–e31. doi: 10.1161/ATVBAHA.116.306940.

66. Zateyshchikov D.A., Minushkina L.O., Kudryashova O. Yu., Barinov V.G., Tsimbalova T.E., Nosenko E.M., Sedov V.P., Sidorenko B.A. Funkcional’noe sostojanie jendotelija u bol’nyh arterial’noj gipertoniej i ishemicheskoj bolezn’ju serdca [Functional state of endothelium in patients with hypertension and ischemic heart disease] // Kardiologiya. 2000; 40 (6): 14–17 (in Russian).

67. Vanhoutte P.M., Shimokawa H., Feletou M., Tang E.H. Endothelial dysfunction and vascular disease – a 30th anniversary update // Acta. Physiol. (Oxf). 2017; 219 (1): 22–96. doi: 10.1111/apha.

68. Zotova I.V., Zateyshchikov D.A., Sidorenko B.A. Sintez oksida azota i razvitie ateroskleroza [Synthesis of nitric oxide and development of atherosclerosis] // Kardiologiya. 2002; 42 (4): 58–67 (in Russian).

69. Treuer A.V., Gonzalez D.R. Nitric oxide synthases, S-nitrosylation and cardiovascular health: from molecular mechanisms to therapeutic opportunities (review) // Mol. Med. Rep. 2015; 11 (3): 1555–1565. doi: 10.3892/mmr.2014.2968.

70. Cannon R.O. Role of nitric oxide in cardiovascular disease: focus on the endothelium // Clin. Chem. 1998; 44 (9): 1809–1819.

71. Tsutsui M., Tanimoto A., Tamura M., Mukae H., Yanagihara N., Shimokawa H., Otsuji Y. Significance of nitric oxide synthases: lessons from triple nitric oxide synthases null mice // J. Pharmacol. Sci. 2015; 127 (1): 42–52. doi: 10.1016/j.jphs.2014.10.002.

72. Treuer A.V., Gonzalez D.R. Nitric oxide synthases, S-nitrosylation and cardiovascular health: from molecular mechanisms to therapeutic opportunities (review) // Mol. Med. Rep. 2015; 11 (3): 1555–1565. doi: 10.3892/mmr.2014.2968.

73. Brown R.A., Shantsila E., Varma C., Lip G.Y. Current understanding of atherogenesis // Am. J. Med. 2016 Nov 22. pii: S0002-9343(16)31196-2. doi: 10.1016/j.amjmed.2016.10.022.

74. [Epub ahead of print].

75. Gimbrone M.A. Jr, García-Cardeña G. Endothelial cell dysfunction and the pathobiology of atherosclerosis // Circ Res. 2016; 118 (4): 620–636. doi: 10.1161/CIRCRESAHA.115.306301.

76. Leask A. Getting to the heart of the matter: new insights into cardiac fibrosis // Circ. Res. 2015; 116 (7): 1269–1276. doi: 10.1161/CIRCRESAHA.116.305381.

77. Wang X., Guo Z., Ding Z., Khaidakov M., Lin J., Xu Z., Sharma S.G., Jiwani S., Mehta J.L. Endothelin-1 upregulation mediates aging-related cardiac fibrosis // J. Mol. Cell. Cardiol. 2015; 80: 101–109. doi: 10.1016/j.yjmcc.2015.01.001.

78. Mezhdunarodnoe rukovodstvo po serdechnoj nedostatochnosti [International guidelines on heart failure] / edited by S.G. Boll, R.V.F. Campbell, G.S. Francis; trans. from english. Moscow: MEDIA SFERA Publ., 1995: 89 (in Russian).

79. Davenport A.P., Hyndman K.A., Dhaun N., Southan C., Kohan D.E., Pollock J.S., Pollock D.M., Webb D.J., Maguire J.J. Endothelin // Pharmacol. Rev. 2016; 68 (2): 357–418. doi: 10.1124/pr.115.011833.

80. Vizir V.A., Berezin A.E. Perspektivy reversii jendotelial’noj disfunkcii u bol’nyh s zastojnoj serdechnoj nedostatochnost’ju [Prospects for the reversal of endothelial dysfunction in patients with congestive heart failure] // Klinicheskaya meditsina – Clinical Medicine. 2000; 78 (7): 36–39 (in Russian).

81. Obrezan A.G., Vologdina I.V. Hronicheskaja serdechnaja nedostatochnost’ [Chronic heart failure]. St.-Petersburg, Vita-Nova Publ., 2002: 320 (in Russian).

82. Maupoint J., Besnier M., Gomez E., Bouhzam N., Henry J.P., Boyer O., Nicol L., Mulder P., Martinet J., Richard V. Selective vascular endothelial protection reduces cardiac dysfunction in chronic heart failure // Circ. Heart Fail. 2016; 9 (4): e002895. doi: 10.1161/CIRCHEARTFAILURE.115.002895.

83. Hirashiki A., Adachi S., Nakano Y., Kamimura Y., Shimokata S., Takeshita K., Murohara T., Kondo T. Effects of bosentan on peripheral endothelial function in patients with pulmonary arterial hypertension or chronic thromboembolic pulmonary hypertension // Pulm. Circ. 2016; 6 (2): 168–173. doi: 10.1086/685715.

84. Jhund P.S., McMurray J.J. The neprilysin pathway in heart failure: a review and guide on the use of sacubitril/valsartan // Heart. 2016; 102 (17): 1342–1347. doi: 10.1136/heartjnl-2014-306775.

85. Kudryashova O.Yu., Zateyshchikov D.A., Sidorenko B.A. Jendotelial’nyj gemostaz: sistema trombomodulina i ee rol’ v razvitii ateroskleroza i ego oslozhnenij [Endothelial hemostasis: thrombomodulin system and its role in pathogenesis of atherosclerosis and its complications] // Kardiologiya. 2000; 40 (8): 65–74 (in Russian).

86. Reichman-Warmusz E., Domal-Kwiatkowska D., Matysiak N., Kurek J., Spinczyk D., Dudek D., Helewski K., Wojnicz R. Tissue factor is unregulated in microvascular endothelial cells of patients with heart failure // J. Clin. Pathol. 2016; 69 (3): 221–225. doi: 10.1136/jclinpath-2015-203172.

87. Sun H.J., Hou B., Wang X., Zhu X.X., Li K.X., Qiu L.Y. Endothelial dysfunction and cardiometabolic diseases: Role of long non-coding RNAs // Life Sci. 2016; 167: 6–11. doi: 10.1016/j.lfs.2016.11.005.

88. Kaliuzhin V.V., Sibireva O.F., Bespalova I.D., Kaliuzhina E.V., Tkalich L.M., Milovanova T.A., Osikhov I.A., Murashev B.Iu. Protromboticheskij status u pacientov s metabolicheskim sindromom: svjaz’ s vospaleniem [Prothrombotic state in patients with metabolic syndrome: an association with inflammation] // Terapevticheskiy Arkhiv – Therapeutic archive. 2013; 85 (10): 29–33 (in Russian).

89. Jia G., Sowers J.R. Endothelial dysfunction potentially interacts with impaired glucose metabolism to increase cardiovascular risk // Hypertension. 2014; 64 (6): 1192–1193. doi: 10.1161/HYPERTENSIONAHA.114.04348.

90. Ter Maaten J.M., Damman K., Verhaar M.C., Paulus W.J., Duncker D.J., Cheng C., van Heerebeek L., Hillege H.L., Lam C.S., Navis G., Voors A.A. Connecting heart failure with preserved ejection fraction and renal dysfunction: the role of endothelial dysfunction and inflammation // Eur. J. Heart Fail. 2016; 18 (6): 588–598. doi: 10.1002/ejhf.497.

91. Salvador B., Arranz A., Francisco S., Córdoba L., Punzón C., Llamas M.Á., Fresno M. Modulation of endothelial function by Toll like receptors // Pharmacol Res. 2016; 108: 46–56. doi: 10.1016/j.phrs.2016.03.038.

92. Costa S., Reina-Couto M., Albino-Teixeira A., Sousa T. Statins and oxidative stress in chronic heart failure // Rev. Port. Cardiol. 2016; 35 (1): 41–57. doi: 10.1016/j.repc.2015.09.006.

93. Giamouzis G., Schelbert E.B., Butler J. Growing evidence linking microvascular dysfunction with heart failure with preserved ejection fraction // J. Am. Heart Assoc. 2016; 5 (2): e003259. doi: 10.1161/JAHA.116.003259.

94. Volkov V.S., Anikin V.V., Trocjuk V.V. Sostojanie mikrocirkuljacii u bol’nyh stenokardiej (po dannym kon’juktival’noj mikroskopii) [Condition of microcirculation in patients with angina pectoris (according conjunctival microscopy)] // Kardiologiya. 1977; 17 (5): 41–44 (in Russian).

95. Teplyako A.T., Garganeeva A.A. Rasstrojstva mikrocirkuljacii pri ishemicheskoj bolezni serdca [Disorders of microcirculation in ischemic heart disease]. Tomsk: TGU Publ., 2001: 344 (in Russian).

96. Houben A.J., Beljaars J.H., Hofstra L., Kroon A.A., De Leeuw P.W. Microvascular abnormalities in chronic heart failure: a cross-sectional analysis // Microcirculation. 2003; 10 (6): 471–478.

97. Dhakal B.P., Malhotra R., Murphy R.M., Pappagianopoulos P.P., Baggish A.L., Weiner R.B., Houstis N.E., Eisman A.S., Hough S.S., Lewis G.D. Mechanisms of exercise intolerance in heart failure with preserved ejection fraction: the role of abnormal peripheral oxygen extraction // Circ. Heart Fail. 2015; 8: 286–294. doi: 10.1161/CIRCHEARTFAILURE.114.001825.

98. Middlekauff H.R. Making the case for skeletal myopathy as the major limitation of exercise capacity in heart failure // Circ. Heart Fail. 2010; 3 (4): 537–546. doi: 10.1161/CIRCHEARTFAILURE.109.903773.

99. Kennel P.J., Mancini D.M., Schulze P.C. Skeletal muscle changes in chronic cardiac disease and failure // Compr. Physiol. 2015; 5 (4): 1947–1969. doi: 10.1002/cphy.c110003.

100. Malaja L.T., Mikljaev I.Ju., Kravchun P.G. Mikrocirkuljacija v kardiologii [Microcirculation in cardiology]. Kharkiv, Vishha shkola Publ., 977: 232 (in Russian).

101. Copp S.W., Hirai D.M., Ferguson S.K., Holdsworth C.T., Musch T.I., Poole D.C. Effects of chronic heart failure on neuronal nitric oxide synthase-mediated control of microvascular O2 pressure in contracting rat skeletal muscle // J. Physiol. 2012; 590 (15): 3585–3596. doi: 10.1113/jphysiol.2012.235929.

102. Chernuh A.M., Aleksandrov P.N., Alekseev O.V. Mikrocirkuljacija [Microcirculation]. Moscow, Medicine Publ., 1984: 432 (in Russian).

103. Nikolaeva T.N., Korablev A.V. Gemomikrocirkuljacija: patologija pri vrozhdennyh porokah serdca [Hemomicrocirculation: pathology in congenital heart defects] / ed. by N.E. Yarygin. Moscow: Russian state medical University Publ., 1996: 179 (in Russian).

104. Teplyakov A.E., Pushnikova E.Yu., Kalyuzhin V.V., Bespalova I.D., Kalyuzhina E.V., Kalyuzhina M.I. Vlijanie amlodipina na transkapilljarnyj obmen kisloroda pri ishemicheskoj bolezni serdca s insulinorezistentnost’ju хъ [The influence of amlodipine on transcapillary metabolism of oxygen during coronary heart disease with insulin resistance] // Klinicheskaya meditsina – Clinical Medicine. 2013; 91 (4): 16–18 (in Russian).

105. Kukes V.G., Prokofiev A.B., Checha O.A., Goroshko O.A., Mazerkina I.A., Demchenkova E.Yu. Vlijanie antioksidantov na naprjazhenie kisloroda v krovi u pacientov s hronicheskoj serdechnoj nedostatochnost’ju [The effect of antioxidants on oxygen tension in the blood in patients with chronic heart failure] // Mezhdunarodnyj zhurnal prikladnyh i fundamental’nyh issledovanij. 2016; 6-1: 56–58.