Liquorice ingestion attenuates vasodilatation via exogenous nitric oxide donor but not via β2-adrenoceptor stimulation
Autoři:
Elina J. Hautaniemi aff001; Antti J. Tikkakoski aff001; Arttu Eräranta aff001; Mika Kähönen aff001; Esa Hämäläinen aff003; Ursula Turpeinen aff003; Heini Huhtala aff005; Jukka Mustonen aff001; Ilkka H. Pörsti aff001
Působiště autorů:
Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland
aff001; Department of Clinical Physiology, Tampere University Hospital, Tampere, Finland
aff002; HUSLAB, Helsinki University Hospital, Helsinki, Finland
aff003; Department of Clinical Chemistry, Biomedicum, Helsinki University, Helsinki, Finland
aff004; Faculty of Social Sciences, Tampere University, Tampere, Finland
aff005; Department of Internal Medicine, Tampere University Hospital, Tampere, Finland
aff006
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223654
Souhrn
We examined the effect of liquorice ingestion on haemodynamic responses to exogenous nitric oxide donor (nitroglycerin) and β2-adrenoceptor agonist (salbutamol), and 11β-hydroxysteroid dehydrogenase activity, in 21 volunteers and 21 reference subjects. Haemodynamic data was captured before and after sublingual nitroglycerin (0.25 mg) and inhaled salbutamol (400 μg) during orthostatic challenge utilising radial pulse wave analysis and whole-body impedance cardiography. The recordings were performed at baseline and following two weeks of liquorice intake (290–370 mg/d glycyrrhizin). Urinary cortisone and cortisol metabolites were examined. Liquorice intake elevated aortic systolic and diastolic blood pressure and systemic vascular resistance when compared with the reference group. Following research drug administration the liquorice-induced increase in systemic vascular resistance was observed in the presence of nitroglycerin (p<0.05) but no longer in the presence of salbutamol. Liquorice ingestion decreased cardiac chronotropic response to upright posture (p = 0.032) in unadjusted analysis, but when adjusted for age and sex the difference in the upright change in heart rate was no longer significant. The urinary cortisone to cortisol metabolite ratio decreased from 0.70 to 0.31 (p<0.001) after liquorice intake indicating significant inhibition of the 11β-hydroxysteroid dehydrogenase type 2. In the reference group the haemodynamic variables remained virtually unchanged. These results suggest that liquorice exposure impaired vasodilatation in vivo that was induced by exogenous nitric oxide donor but not that induced by β2-adrenoceptor stimulation.
Trial registration: EU Clinical Trials Register 2006-002065-39
ClinicalTrials.gov NCT01742702.
Klíčová slova:
Blood plasma – Drug research and development – Inhalation – Blood pressure – Ingestion – Heart rate – Cortisol – Aldosterone
Zdroje
1. Nazari S, Rameshrad M, Hosseinzadeh H. Toxicological effects of glycyrrhiza glabra (licorice): a review. Phytother Res. 2017;31: 1635–1650. doi: 10.1002/ptr.5893 28833680
2. Isbrucker RA, Burdock GA. Risk and safety assessment on the consumption of Licorice root (Glycyrrhiza sp.), its extract and powder as a food ingredient, with emphasis on the pharmacology and toxicology of glycyrrhizin. Regul Toxicol Pharmacol. 2006;46: 167–192. doi: 10.1016/j.yrtph.2006.06.002 16884839
3. Stewart PM, Wallace AM, Valentino R, Burt D, Shackleton CH, Edwards CR. Mineralocorticoid activity of liquorice: 11-beta-hydroxysteroid dehydrogenase deficiency comes of age. Lancet. 1987;2: 821–824. doi: 10.1016/s0140-6736(87)91014-2 2889032
4. Hunter RW, Bailey MA. Glucocorticoids and 11β-hydroxysteroid dehydrogenases: mechanisms for hypertension. Curr Opin Pharmacol. 2015;21: 105–114. doi: 10.1016/j.coph.2015.01.005 25666420
5. Goodwin JE, Geller DS. Glucocorticoid-induced hypertension. Pediatr Nephrol. 2012;27: 1059–1066. doi: 10.1007/s00467-011-1928-4 21744056
6. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science. 1988;242: 583–585. doi: 10.1126/science.2845584 2845584
7. Edwards CR, Stewart PM, Burt D, Brett L, McIntyre MA, Sutanto WS, et al. Localisation of 11 beta-hydroxysteroid dehydrogenase—tissue specific protector of the mineralocorticoid receptor. Lancet. 1988;2: 986–989. doi: 10.1016/s0140-6736(88)90742-8 2902493
8. Farese RV, Biglieri EG, Shackleton CH, Irony I, Gomez-Fontes R. Licorice-induced hypermineralocorticoidism. N Engl J Med. 1991;325: 1223–1227. doi: 10.1056/NEJM199110243251706 1922210
9. Hadoke PWF, Macdonald L, Logie JJ, Small GR, Dover AR, Walker BR. Intra-vascular glucocorticoid metabolism as a modulator of vascular structure and function. Cell Mol Life Sci. 2006;63: 565–578. doi: 10.1007/s00018-005-5427-2 16416027
10. Christy C, Hadoke PWF, Paterson JM, Mullins JJ, Seckl JR, Walker BR. 11β-hydroxysteroid dehydrogenase type 2 in mouse aorta: localization and influence on response to glucocorticoids. Hypertension. 2003;42: 580–587. doi: 10.1161/01.HYP.0000088855.06598.5B 12925564
11. Hatakeyama H, Inaba S, Takeda R, Miyamori I. 11beta-hydroxysteroid dehydrogenase in human vascular cells. Kidney Int. 2000;57: 1352–1357. doi: 10.1046/j.1523-1755.2000.00974.x 10760066
12. Mahmud A, Feely J. Aldosterone-to-renin ratio, arterial stiffness, and the response to aldosterone antagonism in essential hypertension. Am J Hypertens. 2005;18: 50–55. doi: 10.1016/j.amjhyper.2004.08.026 15691617
13. Chapman K, Holmes M, Seckl J. 11β-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol Rev. 2013;93: 1139–1206. doi: 10.1152/physrev.00020.2012 23899562
14. Lombès M, Alfaidy N, Eugene E, Lessana A, Farman N, Bonvalet JP. Prerequisite for cardiac aldosterone action. Mineralocorticoid receptor and 11 beta-hydroxysteroid dehydrogenase in the human heart. Circulation. 1995;92: 175–182. doi: 10.1161/01.cir.92.2.175 7600648
15. Richardson RV, Batchen EJ, Denvir MA, Gray GA, Chapman KE. Cardiac GR and MR: From Development to Pathology. Trends Endocrinol Metab. 2016;27: 35–43. doi: 10.1016/j.tem.2015.10.001 26586027
16. Oakley RH, Cidlowski JA. Glucocorticoid signaling in the heart: A cardiomyocyte perspective. J Steroid Biochem Mol Biol. 2015;153: 27–34. doi: 10.1016/j.jsbmb.2015.03.009 25804222
17. Hautaniemi EJ, Tahvanainen AM, Koskela JK, Tikkakoski AJ, Kähönen M, Uitto M, et al. Voluntary liquorice ingestion increases blood pressure via increased volume load, elevated peripheral arterial resistance, and decreased aortic compliance. Sci Rep. 2017;7: 10947. doi: 10.1038/s41598-017-11468-7 28887501
18. Leskinen MH, Hautaniemi EJ, Tahvanainen AM, Koskela JK, Päällysaho M, Tikkakoski AJ, et al. Daily liquorice consumption for two weeks increases augmentation index and central systolic and diastolic blood pressure. PloS One. 2014;9: e105607. doi: 10.1371/journal.pone.0105607 25153328
19. Rule AD, Larson TS, Bergstralh EJ, Slezak JM, Jacobsen SJ, Cosio FG. Using serum creatinine to estimate glomerular filtration rate: accuracy in good health and in chronic kidney disease. Ann Intern Med. 2004;141: 929–937. doi: 10.7326/0003-4819-141-12-200412210-00009 15611490
20. Turpeinen U, Markkanen H, Sane T, Hämäläinen E. Determination of free tetrahydrocortisol and tetrahydrocortisone ratio in urine by liquid chromatography-tandem mass spectrometry. Scand J Clin Lab Invest. 2006;66: 147–159. doi: 10.1080/00365510500474504 16537248
21. Tahvanainen A, Koskela J, Tikkakoski A, Lahtela J, Leskinen M, Kähönen M, et al. Analysis of cardiovascular responses to passive head-up tilt using continuous pulse wave analysis and impedance cardiography. Scand J Clin Lab Invest. 2009;69: 128–137. doi: 10.1080/00365510802439098 18850486
22. Tahvanainen AM, Tikkakoski AJ, Leskinen MH, Nordhausen K, Kähönen M, Kööbi T, et al. Supine and upright haemodynamic effects of sublingual nitroglycerin and inhaled salbutamol: a double-blind, placebo-controlled, randomized study. J Hypertens. 2012;30: 297–306. doi: 10.1097/HJH.0b013e32834e4b26 22179079
23. Chen CH, Nevo E, Fetics B, Pak PH, Yin FC, Maughan WL, et al. Estimation of central aortic pressure waveform by mathematical transformation of radial tonometry pressure. Validation of generalized transfer function. Circulation. 1997;95: 1827–1836. doi: 10.1161/01.cir.95.7.1827 9107170
24. Kööbi T, Kaukinen S, Ahola T, Turjanmaa VM. Non-invasive measurement of cardiac output: whole-body impedance cardiography in simultaneous comparison with thermodilution and direct oxygen Fick methods. Intensive Care Med. 1997;23: 1132–1137. doi: 10.1007/s001340050469 9434918
25. Kööbi T, Kaukinen S, Turjanmaa VM, Uusitalo AJ. Whole-body impedance cardiography in the measurement of cardiac output. Crit Care Med. 1997;25: 779–785. doi: 10.1097/00003246-199705000-00012 9187596
26. Kööbi T, Kähönen M, Iivainen T, Turjanmaa V. Simultaneous non-invasive assessment of arterial stiffness and haemodynamics—a validation study. Clin Physiol Funct Imaging. 2003;23: 31–36. 12558611
27. Koskela JK, Tahvanainen A, Haring A, Tikkakoski AJ, Ilveskoski E, Viitala J, et al. Association of resting heart rate with cardiovascular function: a cross-sectional study in 522 Finnish subjects. BMC Cardiovasc Disord. 2013;13: 102. doi: 10.1186/1471-2261-13-102 24237764
28. Wilenius M, Tikkakoski AJ, Tahvanainen AM, Haring A, Koskela J, Huhtala H, et al. Central wave reflection is associated with peripheral arterial resistance in addition to arterial stiffness in subjects without antihypertensive medication. BMC Cardiovasc Disord. 2016;16: 131. doi: 10.1186/s12872-016-0303-6 27266507
29. Wilkinson IB, Hall IR, MacCallum H, Mackenzie IS, McEniery CM, van der Arend BJ, et al. Pulse-wave analysis: clinical evaluation of a noninvasive, widely applicable method for assessing endothelial function. Arterioscler Thromb Vasc Biol. 2002;22: 147–152. doi: 10.1161/hq0102.101770 11788475
30. Tahvanainen A, Koskela J, Leskinen M, Ilveskoski E, Nordhausen K, Kähönen M, et al. Reduced systemic vascular resistance in healthy volunteers with presyncopal symptoms during a nitrate-stimulated tilt-table test. Br J Clin Pharmacol. 2011;71: 41–51. doi: 10.1111/j.1365-2125.2010.03794.x 21143500
31. Calculation of within-case area under function curve by trapezoidal integration [Internet] [cited 15 August 2019]. Available from: https://www-01.ibm.com/support/docview.wss?uid=swg21476168
32. Streiner DL. Control or overcontrol for covariates? Evid Based Ment Health. 2016;19: 4–5. doi: 10.1136/eb-2015-102294 26755716
33. Roberts C, Torgerson DJ. Understanding controlled trials: baseline imbalance in randomised controlled trials. BMJ. 1999;319: 185. doi: 10.1136/bmj.319.7203.185 10406763
34. McEniery CM, Yasmin, Hall IR, Qasem A, Wilkinson IB, Cockcroft JR, et al. Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol. 2005;46: 1753–1760. doi: 10.1016/j.jacc.2005.07.037 16256881
35. Kangas P, Tahvanainen A, Tikkakoski A, Koskela J, Uitto M, Viik J, et al. Increased Cardiac Workload in the Upright Posture in Men: Noninvasive Hemodynamics in Men Versus Women. J Am Heart Assoc. 2016;5. doi: 10.1161/JAHA.115.002883 27329447
36. Hautaniemi EJ, Tikkakoski AJ, Tahvanainen A, Nordhausen K, Kähönen M, Mattsson T, et al. Effect of fermented milk product containing lactotripeptides and plant sterol esters on haemodynamics in subjects with the metabolic syndrome—a randomised, double-blind, placebo-controlled study. Br J Nutr. 2015;114: 376–386. doi: 10.1017/S0007114515002032 26168857
37. Hammer F, Stewart PM. Cortisol metabolism in hypertension. Best Pract Res Clin Endocrinol Metab. 2006;20: 337–353. doi: 10.1016/j.beem.2006.07.001 16980198
38. Epstein MT, Espiner EA, Donald RA, Hughes H. Effect of eating liquorice on the renin-angiotensin aldosterone axis in normal subjects. Br Med J. 1977;1: 488–490. doi: 10.1136/bmj.1.6059.488 837172
39. Quaschning T, Ruschitzka F, Shaw S, Lüscher TF. Aldosterone receptor antagonism normalizes vascular function in liquorice-induced hypertension. Hypertension. 2001;37: 801–805. doi: 10.1161/01.hyp.37.2.801 11230376
40. Ruschitzka F, Quaschning T, Noll G, deGottardi A, Rossier MF, Enseleit F, et al. Endothelin 1 type a receptor antagonism prevents vascular dysfunction and hypertension induced by 11beta-hydroxysteroid dehydrogenase inhibition: role of nitric oxide. Circulation. 2001;103: 3129–3135. doi: 10.1161/01.cir.103.25.3129 11425780
41. Evans LC, Ivy JR, Wyrwoll C, McNairn JA, Menzies RI, Christensen TH, et al. Conditional deletion of hsd11b2 in the brain causes salt appetite and hypertension. Circulation. 2016;133: 1360–1370. doi: 10.1161/CIRCULATIONAHA.115.019341 26951843
42. Sigurjonsdottir HA, Manhem K, Axelson M, Wallerstedt S. Subjects with essential hypertension are more sensitive to the inhibition of 11 β-HSD by liquorice. J Hum Hypertens. 2003;17: 1001504. doi: 10.1038/sj.jhh.1001504 12574791
43. Dawes M, Chowienczyk PJ, Ritter JM. Effects of inhibition of the L-arginine/nitric oxide pathway on vasodilation caused by beta-adrenergic agonists in human forearm. Circulation. 1997;95: 2293–2297. doi: 10.1161/01.cir.95.9.2293 9142007
44. Ferro A, Coash M, Yamamoto T, Rob J, Ji Y, Queen L. Nitric oxide-dependent β2-adrenergic dilatation of rat aorta is mediated through activation of both protein kinase A and Akt. Br J Pharmacol. 2004;143: 397–403. doi: 10.1038/sj.bjp.0705933 15351777
45. Sobieszczyk P, Borlaug BA, Gornik HL, Knauft WD, Beckman JA. Glycyrrhetinic acid attenuates vascular smooth muscle vasodilatory function in healthy humans. Clin Sci. 2010;119: 437–442. doi: 10.1042/CS20100087 20515440
46. Hadoke PW, Christy C, Kotelevtsev YV, Williams BC, Kenyon CJ, Seckl JR, et al. Endothelial cell dysfunction in mice after transgenic knockout of type 2, but not type 1, 11beta-hydroxysteroid dehydrogenase. Circulation. 2001;104: 2832–2837. doi: 10.1161/hc4801.100077 11733403
47. Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, et al. Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J. 2006;27: 2588–2605. doi: 10.1093/eurheartj/ehl254 17000623
48. Dart AM, Kingwell BA. Pulse pressure—a review of mechanisms and clinical relevance. J Am Coll Cardiol. 2001;37: 975–984. doi: 10.1016/s0735-1097(01)01108-1 11263624
49. McEniery CM, Wallace S, Mackenzie IS, McDonnell B, Yasmin, Newby DE, et al. Endothelial function is associated with pulse pressure, pulse wave velocity, and augmentation index in healthy humans. Hypertension. 2006;48: 602–608. doi: 10.1161/01.HYP.0000239206.64270.5f 16940223
50. Tikkakoski AJ, Kangas P, Suojanen L, Tahvanainen AM, Eräranta A, Kähönen MAP, et al. Salbutamol-induced decrease in augmentation index is related to the parallel increase in heart rate. Basic Clin Pharmacol Toxicol. 2018; doi: 10.1111/bcpt.12988 29476697
51. Tahvanainen A, Leskinen M, Koskela J, Ilveskoski E, Alanko J, Kähönen M, et al. Non-invasive measurement of the haemodynamic effects of inhaled salbutamol, intravenous L-arginine and sublingual nitroglycerin. Br J Clin Pharmacol. 2009;68: 23–33. doi: 10.1111/j.1365-2125.2009.03434.x 19660000
52. Omar HR, Komarova I, El-Ghonemi M, Fathy A, Rashad R, Abdelmalak HD, et al. Licorice abuse: time to send a warning message. Ther Adv Endocrinol Metab. 2012;3: 125–138. doi: 10.1177/2042018812454322 23185686
53. Simpson FO, Currie IJ. Licorice consumption among high school students. N Z Med J. 1982;95: 31–33. 6950316
54. Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension. Eur Heart J. 2018;39: 3021–3104. doi: 10.1093/eurheartj/ehy339 30165516
55. Sigurjonsdottir HA, Axelson M, Johannsson G, Manhem K, Nyström E, Wallerstedt S. The liquorice effect on the RAAS differs between the genders. Blood Press. 2006;15: 169–172. doi: 10.1080/08037050600593060 16864159
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Eliquis (apixaban) nově hrazen ze zdravotního pojištění
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
- Prevalence of pectus excavatum (PE), pectus carinatum (PC), tracheal hypoplasia, thoracic spine deformities and lateral heart displacement in thoracic radiographs of screw-tailed brachycephalic dogs