Skip to main content
SpringerLink
Log in

Concentration of circulating microparticles: a new biomarker of acute heart failure after cardiac surgery with cardiopulmonary bypass

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Acute heart failure (AHF) is a severe complication after cardiac surgery with cardiopulmonary bypass (CPB). Although some AHF biomarkers have been used in clinic, they have limitations when applied in the prediction and diagnosis of AHF after cardiac surgery with CPB, and there are still no effective and specific biomarkers. We and other researchers have shown that circulating microparticles (MPs) increased in a variety of cardiovascular diseases. However, whether the concentration of circulating MPs could be a new biomarker for AHF after cardiac surgery remains unknown. Here, 90 patients undergoing cardiac surgery with CPB and 45 healthy subjects were enrolled. Patients were assigned into AHF (n=14) or non-AHF (n=76) group according to the diagnosis criteria of AHF. The concentrations of circulating MPs were determined before, as well as 12 h and 3 days after operation with nanoparticle tracking analysis technique. MPs concentrations in patients before surgery were significantly higher than those of healthy subjects. Plasma levels of MPs were significantly elevated at 12 h after surgery in patients with AHF, but not in those without AHF, and the circulating MPs concentrations at 12 h after surgery were higher in AHF group compared with non-AHF group. Logistic regression analysis indicated that MPs concentration at postoperative 12 h was an independent risk factor for AHF. The area under receiver operating characteristic curve for MPs concentration at postoperative 12 h was 0.81 and the best cut-off value is 5.20×108 particles mL−1 with a sensitivity of 93% and a specificity of 10%. These data suggested that the concentration of circulating MPs might be a new biomarker for the occurrence of AHF after cardiac surgery with CPB.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bank, I.E.M., Timmers, L., Gijsberts, C.M., Zhang, Y.N., Mosterd, A., Wang, J.W., Chan, M.Y., De Hoog, V., Lim, S.K., Sze, S.K., et al. (2015). The diagnostic and prognostic potential of plasma extracellular vesicles for cardiovascular disease. Expert Rev Mol Diagn 15, 15771588.

    Google Scholar 

  • Berezin, A.E. (2016). Prognostication in different heart failure phenotypes: The role of circulating biomarkers. J Circ Biomark 5, 6.

    PubMed  PubMed Central  Google Scholar 

  • Berezin, A.E. (2017). Microparticles in chronic heart failure. Adv Clin Chem 81, 1–41.

    CAS  PubMed  Google Scholar 

  • Berezin, A.E., Kremzer, A.A., Berezina, T.A., and Martovitskaya, Y.V. (2015a). Pattern of circulating microparticles in chronic heart failure patients with metabolic syndrome: Relevance to neurohumoral and inflammatory activation. BBA Clin 4, 69–75.

    PubMed  PubMed Central  Google Scholar 

  • Berezin, A.E., Kremzer, A.A., Martovitskaya, Y.V., Samura, T.A., and Berezina, T.A. (2015b). The association of subclinical hypothyroidism and pattern of circulating endothelial-derived microparticles among chronic heart failure patients. Res Cardiovasc Med 4, 7.

    Google Scholar 

  • Berezin, A.E., Kremzer, A.A., Samura, T.A., Berezina, T.A., and Kruzliak, P. (2015c). Impaired immune phenotype of circulating endothelial-derived microparticles in patients with metabolic syndrome and diabetes mellitus. J Endocrinol Invest 38, 865–874.

    CAS  PubMed  Google Scholar 

  • Brouwers, F.P., de Boer, R.A., van der Harst, P., Voors, A.A., Gansevoort, R.T., Bakker, S.J., Hillege, H.L., van Veldhuisen, D.J., and van Gilst, W. H. (2013). Incidence and epidemiology of new onset heart failure with preserved v. reduced ejection fraction in a community-based cohort: 11-year follow-up of prevend. Eur Heart J 34, 1424–1431.

    CAS  PubMed  Google Scholar 

  • Burger, D., and Touyz, R.M. (2012). Cellular biomarkers of endothelial health: Microparticles, endothelial progenitor cells, and circulating endothelial cells. J Am Soc Hypertens 6, 85–99.

    CAS  PubMed  Google Scholar 

  • Burger, D., Schock, S., Thompson, C.S., Montezano, A.C., Hakim, A.M., and Touyz, R.M. (2013). Microparticles: Biomarkers and beyond. Clin Sci 124, 423–441.

    CAS  Google Scholar 

  • Chow, S.L., Maisel, A.S., Anand, I., Bozkurt, B., de Boer, R.A., Felker, G. M., Fonarow, G.C., Greenberg, B., Januzzi Jr, J.L., Kiernan, M.S., et al. (2017). Role of biomarkers for the prevention, assessment, and management of heart failure: A scientific statement from the american heart association. Circulation 135, e1054.

    CAS  PubMed  Google Scholar 

  • Ci, H.B., Ou, Z.J., Chang, F.J., Liu, D.H., He, G.W., Xu, Z., Yuan, H.Y., Wang, Z.P., Zhang, X., and Ou, J.S. (2013). Endothelial microparticles increase in mitral valve disease and impair mitral valve endothelial function. Am J Physiol Endocrinol Metab 304, E695–E702.

    CAS  PubMed  Google Scholar 

  • Coumans, F.A.W., Brisson, A.R., Buzas, E.I., Dignat-George, F., Drees, E.E.E., El-Andaloussi, S., Emanueli, C., Gasecka, A., Hendrix, A., Hill, A.F., et al. (2017). Methodological guidelines to study extracellular vesicles. Circ Res 120, 1632–1648.

    CAS  PubMed  Google Scholar 

  • Das, S., and Halushka, M.K. (2015). Extracellular vesicle microRNA transfer in cardiovascular disease. Cardiovasc Pathol 24, 199–206.

    CAS  PubMed  Google Scholar 

  • Delcayre, C., and Swynghedauw, B. (2002). Molecular mechanisms of myocardial remodeling. The role of aldosterone. J Mol Cell Cardiol 34, 1577–1584.

    CAS  PubMed  Google Scholar 

  • Densmore, J.C., Signorino, P.R., Ou, J., Hatoum, O.A., Rowe, J.J., Shi, Y., Kaul, S., Jones, D.W., Sabina, R.E., Pritchard Jr, K.A., et al. (2006). Endothelium-derived microparticles induce endothelial dysfunction and acute lung injury. Shock 26, 464–471.

    CAS  PubMed  Google Scholar 

  • Dignat-George, F., and Boulanger, C.M. (2011). The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31, 27–33.

    CAS  PubMed  Google Scholar 

  • Dragovic, R.A., Gardiner, C., Brooks, A.S., Tannetta, D.S., Ferguson, D.J. P., Hole, P., Carr, B., Redman, C.W.G., Harris, A.L., Dobson, P.J., et al. (2011). Sizing and phenotyping of cellular vesicles using nanoparticle tracking analysis. Nanomedicine 7, 780–788.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feng, Y.L., and Yu, X.Y. (2011). Cardinal roles of miRNA in cardiac development and disease. Sci China Life Sci 54, 1113–1120.

    CAS  PubMed  Google Scholar 

  • Fu, L., Hu, X.X., Lin, Z.B., Chang, F.J., Ou, Z.J., Wang, Z.P., and Ou, J.S. (2015). Circulating microparticles from patients with valvular heart disease and cardiac surgery inhibit endothelium-dependent vasodilation. J Thorac Cardiovasc Surg 150, 666–672.

    CAS  PubMed  Google Scholar 

  • Gong, J., Jaiswal, R., Dalla, P., Luk, F., and Bebawy, M. (2015). Microparticles in cancer: A review of recent developments and the potential for clinical application. Semin Cell Dev Biol 40, 35–40.

    CAS  PubMed  Google Scholar 

  • Greening, D.W., Gopal, S.K., Mathias, R.A., Liu, L., Sheng, J., Zhu, H.J., and Simpson, R.J. (2015). Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin Cell Dev Biol 40, 60–71.

    CAS  PubMed  Google Scholar 

  • Heart Failure Group of Chinese Society of Cardiology of Chinese Medical, A. Chinese Heart Failure Association of Chinese Medical Doctor, A., and Editorial Board of Chinese Journal Of, C. (2018). Chinese guidelines for the diagnosis and treatment of heart failure 2018. Chin J Cardiovasc Dis 46, 760–789.

    Google Scholar 

  • Jian, Y.P., Yuan, H.X., Hu, K.H., Chen, C., Li, Y.Q., Li, Y., Yang, T.X., Ou, Z.J., and Ou, J.S. (2019). Protein compositions changes of circulating microparticles in patients with valvular heart disease subjected to cardiac surgery contribute to systemic inflammatory response and disorder of coagulation. Shock 52, 487–496.

    CAS  PubMed  Google Scholar 

  • Kowal, J., Arras, G., Colombo, M., Jouve, M., Morath, J.P., Primdal-Bengtson, B., Dingli, F., Loew, D., Tkach, M., and Théry, C. (2016). Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA 113, E968–E977.

    CAS  PubMed  Google Scholar 

  • Levy, D., Kenchaiah, S., Larson, M.G., Benjamin, E.J., Kupka, M.J., Ho, K.K.L., Murabito, J.M., and Vasan, R.S. (2002). Long-term trends in the incidence of and survival with heart failure. N Engl J Med 347, 13971402.

    Google Scholar 

  • Lin, Z.B., Ci, H.B., Li, Y., Cheng, T.P., Liu, D.H., Wang, Y.S., Xu, J., Yuan, H.X., Li, H.M., Chen, J., et al. (2017). Endothelial microparticles are increased in congenital heart diseases and contribute to endothelial dysfunction. J Transl Med 15, 4.

    PubMed  PubMed Central  Google Scholar 

  • Liu, Y., He, Z., Zhang, Y., Dong, Z., Bi, Y., Kou, J., Zhou, J., and Shi, J. (2016). Dissimilarity of increased phosphatidylserine-positive microparticles and associated coagulation activation in acute coronary syndromes. Coron Artery Dis 27, 365–375.

    PubMed  Google Scholar 

  • Mahmoud, A.M., Wilkinson, F.L., McCarthy, E.M., Moreno-Martinez, D. M., Langford-Smith, A., Romero, M., Duarte, J., and Alexander, M.Y. (2017). Endothelial microparticles prevent lipid-induced endothelial damage via Akt/eNOS signaling and reduced oxidative stress. FASEB J 31, 4636–4648.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez, M.C., and Andriantsitohaina, R. (2011). Microparticles in angiogenesis. Circ Res 109, 110–119.

    CAS  PubMed  Google Scholar 

  • Nichols, M., Townsend, N., Scarborough, P., and Rayner, M. (2014). Cardiovascular disease in europe 2014: Epidemiological update. Eur Heart J 35, 2950–2959.

    CAS  PubMed  Google Scholar 

  • Ou, Z.J., Chang, F.J., Luo, D., Liao, X.L., Wang, Z.P., Zhang, X., Xu, Y.Q., and Ou, J.S. (2011). Endothelium-derived microparticles inhibit angiogenesis in the heart and enhance the inhibitory effects of hypercholesterolemia on angiogenesis. Am J Physiol Endocrinol Metab 300, E661–E668.

    CAS  PubMed  Google Scholar 

  • Peng, L.N., Li, Y.J., Zhang, L., and Yu, W.Q. (2013). Moving RNA moves RNA forward. Sci China Life Sci 56, 914–920.

    CAS  PubMed  Google Scholar 

  • Peterson, D.B., Sander, T., Kaul, S., Wakim, B.T., Halligan, B., Twigger, S., Pritchard Jr., K.A., Oldham, K.T., and Ou, J.S. (2008). Comparative proteomic analysis of PAI-1 and TNF-alpha-derived endothelial microparticles. Proteomics 8, 2430–2446.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ponikowski, P., Voors, A.A., Anker, S.D., Bueno, H., Cleland, J.G.F., Coats, A.J.S., Falk, V., González-Juanatey, J.R., Harjola, V.P., Jankowska, E.A., et al. (2016). 2016 esc guidelines for the diagnosis and treatment of acute and chronic heart failure. Eur J Heart Fail 18, 891–975.

    PubMed  Google Scholar 

  • Rohde, L.E., Bertoldi, E.G., Goldraich, L., and Polanczyk, C.A. (2013). Cost-effectiveness of heart failure therapies. Nat Rev Cardiol 10, 338354.

    Google Scholar 

  • Saari, H., Lázaro-Ibáñez, E., Viitala, T., Vuorimaa-Laukkanen, E., Siljander, P., and Yliperttula, M. (2015). Microvesicle- and exosome-mediated drug delivery enhances the cytotoxicity of paclitaxel in autologous prostate cancer cells. J Control Release 220, 727–737.

    CAS  PubMed  Google Scholar 

  • Sander, T.L., Ou, J.S., Densmore, J.C., Kaul, S., Matus, I., Twigger, S., Halligan, B., Greene, A.S., Pritchard, K.A., and Oldham, K.T. (2008). Protein composition of plasminogen activator inhibitor type 1-derived endothelial microparticles. Shock 29, 504–511.

    CAS  PubMed  Google Scholar 

  • Souza, A.C.P., Yuen, P.S.T., and Star, R.A. (2015). Microparticles: Markers and mediators of sepsis-induced microvascular dysfunction, immunosuppression, and AKI. Kidney Int 87, 1100–1108.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ural, D., Çavuşoğlu, Y., Eren, M., Karaüzüm, K., Temizhan, A., Yilmaz, M.B., Zoghi, M., Ramassubu, K., and Bozkurt, B. (2015). Diagnosis and management of acute heart failure. Anatol J Cardiol 15, 860889.

    Google Scholar 

  • Yancy, C.W., Jessup, M., Bozkurt, B., Butler, J., Casey Jr., D.E., Drazner, M.H., Fonarow, G.C., Geraci, S.A., Horwich, T., Januzzi, J.L., et al. (2013). 2013 ACCF/AHA guideline for the management of heart failure. J Am Coll Cardiol 62, e147–e239.

    PubMed  Google Scholar 

  • Zhang, X., Liu, H., Gao, J., Zhu, M., Wang, Y., Jiang, C., and Xu, M. (2019). Metabolic disorder in the progression ofheart failure. Sci China Life Sci 62, 1153–1167.

    PubMed  Google Scholar 

  • Zhou, K., and Hong, T. (2017). Cardiac BIN1 (cBIN1) is a regulator of cardiac contractile function and an emerging biomarker of heart muscle health. Sci China Life Sci 60, 257–263.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (81670392, 81600382, 81770241, 81830013, 81970363), the National Science Fund for Distinguished Young Scholars (81325001), the International Cooperation Project (2015DFA31070) from the Ministry of Science and Technology of China, the National Key Research and Development Program of China (2016YFC0903000), the Changjiang Scholars Program from the Ministry of Education of China, Guangdong Natural Science Fund Committee (2015A030312009), the Guangdong Pearl River Scholars Program, and the Sun Yat-sen University Clinical Research 5010 Program (2014002). The five and five projects are from The First Affiliated Hospital, Sun Yat-sen University. The authors would like to thank the patients as well as staffs at the First Affiliated Hospital, Sun Yat-sen University for their assistance throughout this study.

Author information

Author notes

  1. Contributed equally to this work

Authors and Affiliations

  1. Division of Cardiac Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510080, China

    Yuquan Li, Haoxiang Yuan, Chao Chen, Jian Ma, Yating Chen, Yan Li, Yupeng Jian & Jingsong Ou

  2. National-Guangdong Joint Engineering Laboratory for Diagnosis and Treatment of Vascular Diseases, Guangzhou, 510080, China

    Yuquan Li, Haoxiang Yuan, Chao Chen, Jian Ma, Yating Chen, Yan Li, Yupeng Jian, Zhijun Ou & Jingsong Ou

  3. NHC key Laboratory of Assisted Circulation, Sun Yat-sen University, Guangzhou, 510080, China

    Yuquan Li, Haoxiang Yuan, Chao Chen, Jian Ma, Yating Chen, Yan Li, Yupeng Jian, Zhijun Ou & Jingsong Ou

  4. Guangdong Provincial Engineering and Technology Center for Diagnosis and Treatment of Vascular Diseases, Guangzhou, 510080, China

    Yuquan Li, Haoxiang Yuan, Chao Chen, Jian Ma, Yating Chen, Yan Li, Yupeng Jian, Zhijun Ou & Jingsong Ou

  5. Department of Anesthesiology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510080, China

    Caiyun Chen

  6. Department of Ultrasound, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510080, China

    Donghong Liu

  7. Division of Hypertension and Vascular Diseases, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510080, China

    Zhijun Ou

  8. Guangdong Provincial Key Laboratory of Brain Function and Disease, Guangzhou, 510080, China

    Jingsong Ou

Authors
  1. Yuquan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haoxiang Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Caiyun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yating Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yupeng Jian
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Donghong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhijun Ou
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jingsong Ou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jingsong Ou.

Ethics declarations

Compliance and ethics The author(s) declare that they have no conflict of interest. The Ethics Review Board of the First Affiliated Hospital, Sun Yat-sen University approved this study with the written informed consents of all participants obtained. This study also complied with the Declaration of Helsinki.

Supporting information

11427_2020_1708_MOESM1_ESM.pdf

Concentration of circulating microparticles: a new biomarker of acute heart failure after cardiac surgery with cardiopulmonary bypass

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Yuan, H., Chen, C. et al. Concentration of circulating microparticles: a new biomarker of acute heart failure after cardiac surgery with cardiopulmonary bypass. Sci. China Life Sci. 64, 107–116 (2021). https://doi.org/10.1007/s11427-020-1708-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-020-1708-9

Keywords

Search

Navigation