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Trace Element Concentrations in Autopsied Heart Tissues from Patients with Secondary Cardiomyopathy

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Abstract

Cardiomyopathies (CMP) represent a significant health problem as they have a poor long-term prognosis and often require transplantation. Heavy metals are known to have cardiotoxic effects and some of them, such as cadmium (Cd), are found to be elevated in the urine and blood of individuals with heart diseases; nevertheless, direct measurement of metals (e.g. zinc (Zn) which is necessary for normal heart function), in the myocardium of individuals with CMP has not been performed. Here, we aimed to analyze the levels of a group of metals in the myocardium of the left ventricle in individuals with CMP. At the Institute of Pathology, we collected 52 samples of left ventricle post-mortem, out of which 19 subjects had been diagnosed with CMP (mean age: 72 y ± 10), and 33 subjects had not suffered from any heart disease (mean age: 67 y ± 15). We found out that individuals with CMP had a significantly higher concentrations of lead, nickel, manganese and copper than non-CMP subjects (p = 0.002, p < 0.001, p = 0.011, and p = 0.002). Interestingly, zinc was significantly lower in CMP subjects than in n-CMP individuals (p = 0.017). Our results indicated the involvement of an increased lead, nickel, copper and manganese heart load in individuals with CMP coupled with lower concentrations of zinc.

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Data Availability

The data that support the findings of this study are available from the corresponding author (A.C) upon a reasonable request.

References

  1. Li C, Shi L, Peng C, Yu G, Zhang Y, Du Z (2021) Lead-induced cardiomyocytes apoptosis by inhibiting gap junction intercellular communication via autophagy activation. Chem Biol Interact 337:109331

    Article  CAS  PubMed  Google Scholar 

  2. Limaye DA, Shaikh ZA (1999) Cytotoxicity of cadmium and characteristics of its transport in cardiomyocytes. Toxicol Appl Pharmacol 154:59–66

    Article  CAS  PubMed  Google Scholar 

  3. Ge J, Guo K, Huang Y, Morse PD, Zhang C, Lv M-W, Li J-L (2022) Comparison of antagonistic effects of nanoparticle-selenium, selenium-enriched yeast and sodium selenite against cadmium-induced cardiotoxicity via AHR/CAR/PXR/Nrf2 pathways activation. J Nutr Biochem 105:108992

    Article  CAS  PubMed  Google Scholar 

  4. Ratnaike RN (2003) Acute and chronic arsenic toxicity. Postgrad Med J 79:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Jovanovic D, Jakovljević B, Rašić-Milutinović Z, Paunović K, Peković G, Knezević T (2011) Arsenic occurrence in drinking water supply systems in ten municipalities in Vojvodina Region, Serbia. Environ Res 111(2):315–318. https://doi.org/10.1016/j.envres.2010.11.014

  6. Ahmad A, Bhattacharya P (2019) Arsenic in Drinking Water: Is 10 μg/L a Safe Limit? Curr Pollut Rep 5:1–3

    Article  Google Scholar 

  7. Authority EFS (2012) Cadmium dietary exposure in the European population. EFSA J 10:2551

    Article  Google Scholar 

  8. Authority EFS (2009) Cadmium in food-scientific opinion of the panel on contaminants in the food chain. EFSA J 7:980

    Google Scholar 

  9. Chen H, Yang X, Wang P, Wang Z, Li M, Zhao FJ (2018) Dietary cadmium intake from rice and vegetables and potential health risk: A case study in Xiangtan, southern China. Sci Total Environ 639:271–277

    Article  CAS  PubMed  Google Scholar 

  10. Gujja P, Rosing DR, Tripodi DJ, Shizukuda Y (2010) Iron overload cardiomyopathy: better understanding of an increasing disorder. J Am Coll Cardiol 56:1001–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Eide DJ (2011) The oxidative stress of zinc deficiency. Metallomics : Integr Biometal Sci 3:1124–1129

    Article  CAS  Google Scholar 

  12. Klaassen CD, Liu J, Diwan BA (2009) Metallothionein protection of cadmium toxicity. Toxicol Appl Pharmacol 238:215–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Đukić-Ćosić D, Baralić K, Javorac D, Djordjevic AB, Bulat Z (2020) An overview of molecular mechanisms in cadmium toxicity. Curr Opin Toxicol 19:56–62

    Article  Google Scholar 

  14. Maron BJ, Towbin JA, Thiene G, Antzelevitch C, Corrado D, Arnett D, Moss AJ, Seidman CE, Young JB (2006) Contemporary definitions and classification of the cardiomyopathies: an american heart association scientific statement from the council on clinical cardiology, heart failure and transplantation committee; quality of care and outcomes research and functional genomics and translational biology interdisciplinary working groups; and council on epidemiology and prevention. Circulation 113:1807–1816

    Article  PubMed  Google Scholar 

  15. Steptoe A, Mohabir A, Mahon N, McKenna W (2000) Health related quality of life and psychological wellbeing in patients with dilated cardiomyopathy. Heart 83:645–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Tellez-Plaza M, Guallar E, Howard BV, Umans JG, Francesconi KA, Goessler W, Silbergeld EK, Devereux RB, Navas-Acien A (2013) Cadmium exposure and incident cardiovascular disease. Epidemiology (Cambridge, Mass) 24:421–429

    Article  PubMed  Google Scholar 

  17. Egger AE, Grabmann G, Gollmann-Tepeköylü C, Pechriggl EJ, Artner C, Türkcan A, Hartinger CG, Fritsch H, Keppler BK, Brenner E, Grimm M, Messner B, Bernhard D (2019) Chemical imaging and assessment of cadmium distribution in the human body. Metallomics 11:2010–2019

    Article  CAS  PubMed  Google Scholar 

  18. Cirovic A, Orisakwe OE, Cirovic A, Jevtic J, Tasic D, Tasic N (2023) Non-uniform bioaccumulation of lead and arsenic in two remote regions of the human heart's left ventricle: a post-mortem study. Biomolecules 13(8):1232. https://doi.org/10.3390/biom13081232

  19. Leem AY, Kim SK, Chang J, Kang YA, Kim YS, Park MS, Kim SY, Kim EY, Chung KS, Jung JY (2015) Relationship between blood levels of heavy metals and lung function based on the Korean National Health and Nutrition Examination Survey IV-V. Int J Chron Obstruct Pulmon Dis 10:1559–1570

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Frustaci A, Magnavita N, Chimenti C, Caldarulo M, Sabbioni E, Pietra R, Cellini C, Possati GF, Maseri A (1999) Marked elevation of myocardial trace elements in idiopathic dilated cardiomyopathy compared with secondary cardiac dysfunction. J Am Coll Cardiol 33(6):1578–1583. https://doi.org/10.1016/s0735-1097(99)00062-5

  21. Malamba-Lez D, Tshala-Katumbay D, Bito V, Rigo JM, Kyandabike RK, Yolola EN, Katchunga P, Koba-Bora B, Ngoy-Nkulu D (2021) Concurrent heavy metal exposures and idiopathic dilated cardiomyopathy: a case-control study from the katanga mining area of the Democratic Republic of Congo. Int J Environ Res Public Health 18(9):4956. https://doi.org/10.3390/ijerph18094956

  22. Hartz AJ, Anderson AJ, Brooks HL, Manley JC, Parent GT, Barboriak JJ (1984) The association of smoking with cardiomyopathy. N Engl J Med 311:1201–1206

    Article  CAS  PubMed  Google Scholar 

  23. Repić A, Bulat P, Antonijević B, Antunović M, Džudović J, Buha A, Bulat Z (2020) The influence of smoking habits on cadmium and lead blood levels in the Serbian adult people. Environ Sci Pollut Res 27:751–760

    Article  Google Scholar 

  24. Shakeri MT, Nezami H, Nakhaee S, Aaseth J, Mehrpour O (2021) Assessing heavy metal burden among cigarette smokers and non-smoking individuals in iran: cluster analysis and principal component analysis. Biol Trace Elem Res 199:4036–4044

    Article  CAS  PubMed  Google Scholar 

  25. Klinova SV, Minigalieva IA, Protsenko YL, Sutunkova MP, Gurvich VB, Ryabova JV, Valamina IE, Gerzen OP, Nabiev SR, Balakin AA, Lookin ON, Lisin RV, Kuznetsov DA, Privalova LI, Panov VG, Katsnelson LB, Nikitina LV, Katsnelson BA (2022) Changes in the cardiotoxic effects of lead intoxication in rats induced by muscular exercise. Int J Mol Sci 23(8):4417. https://doi.org/10.3390/ijms23084417

  26. Gerzen OP, Nabiev SR, Klinova SV, Minigalieva IA, Sutunkova MP, Katsnelson BA, Nikitina LV (2022) Molecular mechanisms of mechanical function changes of the rat myocardium under subchronic lead exposure. Food Chem Toxicol 169:113444

    Article  CAS  PubMed  Google Scholar 

  27. Pan M, Cheng ZW, Huang CG, Ye ZQ, Sun LJ, Chen H, Fu BB, Zhou K, Fang ZR, Wang ZJ, Xiao QZ, Liu XS, Zhu FQ, Gao S (2022) Long-term exposure to copper induces mitochondria-mediated apoptosis in mouse hearts. Ecotoxicol Environ Saf 234:113329

    Article  CAS  PubMed  Google Scholar 

  28. Jiang Y, Zheng W (2005) Cardiovascular toxicities upon manganese exposure. Cardiovasc Toxicol 5:345–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zhang N, Chen M, Li J, Deng Y, Li SL, Guo YX, Li N, Lin Y, Yu P, Liu Z, Zhu J (2019) Metal nickel exposure increase the risk of congenital heart defects occurrence in offspring: a case-control study in China. Medicine (Baltimore) 98:e15352

    Article  CAS  PubMed  Google Scholar 

  30. Navas-Acien A, Guallar E, Silbergeld EK, Rothenberg SJ (2007) Lead exposure and cardiovascular disease–a systematic review. Environ Health Perspect 115:472–482

    Article  CAS  PubMed  Google Scholar 

  31. Hegde S, Maysky M, Zaidi A (2020) A Rare Case of Lead-Induced Cardiomyopathy. JACC Case Rep 2:1496–1500

    Article  PubMed  PubMed Central  Google Scholar 

  32. Cook MK, Zhang J, Wei Y (2022) Blood lead levels and risk of deaths from cardiovascular disease. Am J Cardiol 173:132–138

    Article  CAS  PubMed  Google Scholar 

  33. Rosenblum H, Bikdeli B, Wessler J, Gupta A, Jacoby DL (2020) Zinc deficiency as a reversible cause of heart failure. Tex Heart Inst J 47:152–154

    Article  PubMed  PubMed Central  Google Scholar 

  34. Schanz M, Schaaf L, Dippon J, Biegger D, Fritz P, Alscher MD, Kimmel M (2017) Renal effects of metallothionein induction by zinc in vitro and in vivo. BMC Nephrol 18:91

    Article  PubMed  PubMed Central  Google Scholar 

  35. López-Rodríguez G, Galván M, González-Unzaga M, Hernández Ávila J, Pérez-Labra M (2017) Blood toxic metals and hemoglobin levels in Mexican children. Environ Monit Assess 189:179

    Article  PubMed  Google Scholar 

Download references

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

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Authors and Affiliations

  1. Faculty of Medicine, Institute of Anatomy, University of Belgrade, Dr Subotica 4/2, 11000, Belgrade, Serbia

    Ana Ćirović & Aleksandar Ćirović

  2. Department of Toxicology “Akademik Danilo Soldatović”, University of Belgrade - Faculty of Pharmacy, Vojvode Stepe 450, 11221, Belgrade, Serbia

    Aleksandra Buha Đorđević & Biljana Antonijević

  3. Center for Toxicological Risk Assessment, University of Belgrade - Faculty of Pharmacy, Vojvode Stepe 450, 11221, Belgrade, Serbia

    Aleksandra Buha Đorđević

  4. Faculty of Medicine, Institute of Pathology, University of Belgrade, Dr Subotica 1, 11000, Belgrade, Serbia

    Jovan Jevtić

  5. Institute for Cardiovascular Diseases Dedinje, 5 Heroja Milana Tepica Street, 11000, Belgrade, Serbia

    Danijela Tasić & Nebojša Tasić

  6. Faculty of Medicine, University of Banja Luka, Banja Luka, RS, Bosnia and Herzegovina

    Danijela Tasić

  7. Institute of Meat Hygiene and Technology, Kacanskog 13, 11040, Belgrade, Serbia

    Saša Janković & Zoran Petrović

  8. African Centre of Excellence for Public Health and Toxicological Research (ACE-PUTOR), University of Port Harcourt, PMB, Port Harcourt, Choba, 5323, Nigeria

    Orish E. Orisakwe

  9. Faculty of Medicine, University of Belgrade, Dr Subotica 8, 11000, Belgrade, Serbia

    Nebojša Tasić

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  1. Ana Ćirović
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Contributions

Conceptualization: Ana Ćirović, Aleksandar Ćirović, Nebojša Tasić, Aleksandra Buha Đorđević.

Samples collection: Aleksandar Ćirović, Ana Ćirović, Jovan Jevtić.

Data analyzes: Ana Ćirović; Orish E. Orisakwe, Nebojša Tasić, Saša Janković.

Data Interpretation: Ana Ćirović, Danijela Tasić, Nebojša Tasić, Aleksandra Buha Đorđević.

Writing – original draft: Ana Ćirović, Aleksandar Ćirović.

Critically revised the work: Orish E. Orisakwe, Danijela Tasić, Nebojša Tasić, Biljana Antonijević, Zoran Petrović.

Validation: All the Authors.

Corresponding author

Correspondence to Aleksandar Ćirović.

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The institutional Ethics Committee granted approval for the collection of the samples (17/IV-29).

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Ćirović, A., Buha Đorđević, A., Ćirović, A. et al. Trace Element Concentrations in Autopsied Heart Tissues from Patients with Secondary Cardiomyopathy. Biol Trace Elem Res 202, 2442–2449 (2024). https://doi.org/10.1007/s12011-023-03857-z

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