Article Data

  • Views 1473
  • Dowloads 117

Original Research

Open Access

Total plasma sulfide in mild to moderate diastolic heart dysfunction


1Department of Cardiology, General Hospital Celje, Celje, Slovenia

2 Centre for Intensive Care Medicine, University Medical Centre Ljubljana, Ljubljana, Slovenia

3 Institute of Pathophysiology, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia

4 Clinical Department for Anaesthesiology and Surgical Intensive Care, University Medical Centre Ljubljana, Ljubljana, Slovenia

5 Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia

DOI: 10.22514/SV142.102018.5 Vol.14,Issue 2,November 2018 pp.35-40

Published: 02 November 2018

*Corresponding Author(s): NINA GLAVNIK POZNIČ E-mail:


mechanisms of diastolic dysfunction are not understood well. Hydrogen sulfide is an important endogenous gaseous trans-mitter that can influence heart remodeling. The aim was to determine total plasma sulfide (TPS) levels, as a surrogate marker of hydrogen sulfide, in patients with mild diastolic dysfunction.

Methods. Total plasma sulfide and N-ter-minal pro brain-type natriuretic peptide (NT-proBNP) levels were determined in ambulatory patients with arterial hyper-tension or diabetes mellitus and echocar-diographically mild to moderate diastolic dysfunction.

Results. Twenty-four patients were in-cluded: nine with normal diastolic func-tion (Grade 0), eight with an impaired relaxation pattern (Grade 1), and seven with a pseudo-normalized pattern (Grade 2). TPS levels were highest in patients with normal diastolic function (Grade 0), and lowest in patients with Grade 2 diastolic dysfunction, with this difference between Grade 0 and Grade 2 showing statistical significance (p = 0.017). NT-proBNP lev-els showed the reverse behavior, with this difference again showing statistical signifi-cance (p = 0.042).

Conclusions. Total plasma sulfide levels decrease with worsening of diastolic func-tion from normal to moderate diastolic dysfunction. 


total plasma sulfide, hydrogen sulfide, arterial hypertension, diastolic dys-function, echocardiography

Cite and Share

NINA GLAVNIK POZNIČ,DRAGAN KOVAČIĆ,TOMAŽ GOSLAR,TOMAŽ MARŠ,MATEJ PODBREGAR. Total plasma sulfide in mild to moderate diastolic heart dysfunction. Signa Vitae. 2018. 14(2);35-40.


1. Cleland JGF, Pellicori P. Defining diastolic heart failure and identifying effective therapies. JAMA 2013;309:825-6.

2. Levy D, Larson MG, Vasan RS, Kannel WB, Ho KK. The progression of hyptertension to congestive heart failure. JAMA 1996;275:1557.

3. Reiffenstein RJ, Hulbert WC, Roth SH. Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol 1992;32:109-34.

4. Zhang Z, Huang H, Liu P, Tang C, Wang J. Hydrogen sulfide contributes to cardioprotection during ischemia-reperfusion injury by opening K ATP channels. Can J Physiol Pharmacol 2007;85:1248-53.

5. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 2007;6:917-35.

6. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K et al. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 2009;4:703-14.

7. Whitfield NL, Kreimier EL, Verdial FC, Skovgaard N, Olson KR. Reappraisal of H2S/ sulfide concentration in vertebrate blood and its potential significance in ischemic preconditioning and vascular signaling. Am J Physiol Regul Integr Comp Physiol 2008;6:1930-37.

8. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Car-diovascular Imaging. Eur Heart J Cardiovasc Imaging 2015;16:233-70.

9. Nauget SF, Applwton CP, Gillbert TC, Marino PN, Oh JK, Smiseth OA. Recommendation for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr 2009;10:165-93.

10. Lawrence NS, Davis J, Compton RG. Analytical strategies for the detection of sulfide: a review. Talanta 2000;52:771-84.

11. Fogo JK, Poposky M. Spectrophotometric determination of hydrogen sulfide. Anal Chem 1949;21:732-4.

12. Siegel LM. A direct microdetermination for sulfide. Anal Biochem 1965;11:126-32.

13. Collin M, Anuar FB, Murch O, Bhatia M, Moore PK, Thiemermann C. Inhibition of endogenous hydrogen sulfide formation re-duces the organ injury caused by endotoxemia. Br J Pharmacol 2005;146:498-505.

14. Zhang H, Zhi L, Moore PK, Bhatia M. Role of hydrogen sulfide in cecal ligation and puncture-induced sepsis in the mouse. Am J Physiol Lung Cell Mol Physiol 2006;290:1193-201.

15. Mok YY, Atan MS, Yoke Ping C, Zhong Jing W, Bhatia M, Moochhala S et al. Role of hydrogen sulphide in haemorrhagic shock in the rat: protective effect of inhibitors of hydrogen sulphide biosynthesis. Br J Pharmacol 2004;143:881-9.

16. Stipanuk MH, Beck PW. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J 1982;206:267-77.

17. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 1996;16:1066-71.

18. Martinez DA, Guhl DJ, Staley WC, Vailas AC. Extracellular matrix maturation in the left ventricle of normal and diabetic swine. Diabet Res Clin Pract 2003;59:1-9.

19. Atisha D, Bhalla MA, Morrison LK, Felicio L, Clopton P, Gardetto N et al. A prospective study in search of an optimal B-natriuretic peptide level to screen patients for cardiac dysfunction. Am Heart J 2012;148:518-23.

20. Plehn G, Vormbrock J, Christ M, Prull M, Lefringhausen L, Trappe HJ et al. Masked diastolic dysfunction caused by exercise test-ing in hypertensive heart failure patients with normal ejection fraction and normal or mildly increased LV mass. Acta Cardiol 2009;64:617-26.

21. Bhalla V, Willis S, Maisel AS. B-type natriuretic peptide: the level and the drug partners in the diagnosis of heart failure. Congest Heart Fail 2004;10:3-27.

22. Liang F, Gardner DG. Mechanical strain activates BNP gene transcription through a p38/NF-κB–dependent mechanism. J Clin Invest 1999;104:1603-12.

23. Maeder MT, Staub D, Surnier Y, Reichlin T, Noveanu M, Breidthardt T et al. Determinants of absolute and relative exercise-induced changes in B-type natriuretic peptides. I J Card 2011;147:409-15.

24. Bielecka-Dabrowa A, Michalska-Kasiczak M, Gluba A, Ahmed A, Gerdts E, von Haehlinh S et al. Biomarkers and echocardio-graphic predictors of myocardial dysfunction in patients with hypertension. Sci Rep 2015;5:8916.

25. Zhang Z, Huang H, Liu P, Tang C, Wang J. Hydrogen sulfide contributes to cardioprotection during ischemia-reperfusion injury by opening K ATP channels. Can J Physiol Pharmacol 2007;85:1248-53.

26. Al-Magableh MR, Kemp-Harper BK, Ng HH, Miller AA, Hart JL. Hydrogen sulfide protects endothelial nitric oxide function un-der conditions of acute oxidative stress in vitro. Naunyn-Schmiedeberg Arch Pharmacol 2014;387:67-74.

27. Jin HF, Sun Y, Liang ML, Tang CS, Du JB. Hypotensive effects of hydrogen sulfide via attenuating vascular inflammation in spon-taneously hypertensive rats. Zhonghua Xin Xue Guan Bing Za Zhi 2008;36:541-5.

28. Predmore BL, Julian D, Cardounel AJ. Hydrogen sulfide increases nitric oxide production from endothelial cells by an Akt-depend-ent mechanism. Front Physiol 2011;2:104.

29. Tsuda T, Gao E, Evangelisti L, Markova D, Ma X, Chu ML. Post-ischemic myocardial fibrosis occurs independent of hemodynamic changes. Cardiovasc Res 2003;59:926-33.

30. Opie LH, Commerford PJ, Gersh BJ, Pfeffer MA. Controversies in ventricular remodelling. Lancet 2006;367:356-67.

31. Sun L, Jin H, Sun L, Chen S, Huang Y, Liu J et al. Hydrogen sulfide alleviates myocardial collagen remodeling in association with inhibition of TGF-β/Smad signaling pathway in spontaneously hypertensive rats. MolMed 2014;20:503-15

32. Drachuk KO, Dorofeyeva NA, Sagach VF. The role of hydrogen sulfide in diastolic function restoration during aging. Physiol J 2016;6:62.

33. King AL, Polhemus DJ, Bhushan S, Otsuka H, Kondo K, Nicholson CK et al. Hydrogen sulfide cytoprotective signaling is endothe-lial nitric oxide synthase-nitric oxide dependent. Proc Natl Acad Sci USA 2014;11:3182-87.

34. Xiao l, Dong JH, Jin S, Xue HM, Guo Q, Teng X et al. Hydrogen sulfide improves endothelial dysfunction via downregulating BMP4/COX-2 pathway in rats with hypertension. Oxidat Med Cell Longev 2016:1-10.

35. Bradley JM, Organ CL, Lefer DJ. Garlic-derived organic polysulfides and myocardial protection. J Nutr 2016;146:403-9.

36. Yan H, Du J, Tang C. The possible role of hydrogen sulfide on the pathogenesis of spontaneous hypertension in rats. Biochem Biophys Res Comm 2004;313:22-7.

37. Gu Q, Wang B, Zhang XF, Ma YP, Liu JD, Wang XZ. Contribution of hydrogen sulfide and nitric oxide to exercise-induced at-tenuation of aortic remodeling and improvement of endothelial function in spontaneously hypertensive rats. Mol Cell Biochem 2013;375:199-206.

38. Kovačić D, Glavnik N, Marinšek M, Zagozen P, Rovan K, Goslar T et al. Total plasma sulfide as prognostic indicator for patients with congestive heart failure. J Card Fail 2012;18:541-8.

39. Wintner EA, Deckwerth TL, Langston W, Bengtsson A, Leviten D, Hill P et al. A monobromobimane-based assay to measure the pharmacokinetic profile of reactive sulphide species in blood. Br J Pharmacol 2010;160:941-57.

Abstracted / indexed in

Science Citation Index Expanded (SciSearch) Created as SCI in 1964, Science Citation Index Expanded now indexes over 9,200 of the world’s most impactful journals across 178 scientific disciplines. More than 53 million records and 1.18 billion cited references date back from 1900 to present.

Journal Citation Reports/Science Edition Journal Citation Reports/Science Edition aims to evaluate a journal’s value from multiple perspectives including the journal impact factor, descriptive data about a journal’s open access content as well as contributing authors, and provide readers a transparent and publisher-neutral data & statistics information about the journal.

Chemical Abstracts Service Source Index The CAS Source Index (CASSI) Search Tool is an online resource that can quickly identify or confirm journal titles and abbreviations for publications indexed by CAS since 1907, including serial and non-serial scientific and technical publications.

Index Copernicus The Index Copernicus International (ICI) Journals database’s is an international indexation database of scientific journals. It covered international scientific journals which divided into general information, contents of individual issues, detailed bibliography (references) sections for every publication, as well as full texts of publications in the form of attached files (optional). For now, there are more than 58,000 scientific journals registered at ICI.

Geneva Foundation for Medical Education and Research The Geneva Foundation for Medical Education and Research (GFMER) is a non-profit organization established in 2002 and it works in close collaboration with the World Health Organization (WHO). The overall objectives of the Foundation are to promote and develop health education and research programs.

Scopus: CiteScore 1.0 (2022) Scopus is Elsevier's abstract and citation database launched in 2004. Scopus covers nearly 36,377 titles (22,794 active titles and 13,583 Inactive titles) from approximately 11,678 publishers, of which 34,346 are peer-reviewed journals in top-level subject fields: life sciences, social sciences, physical sciences and health sciences.

Embase Embase (often styled EMBASE for Excerpta Medica dataBASE), produced by Elsevier, is a biomedical and pharmacological database of published literature designed to support information managers and pharmacovigilance in complying with the regulatory requirements of a licensed drug.

Submission Turnaround Time