Advertisement

Biological Trace Element Research

, Volume 186, Issue 1, pp 74–84 | Cite as

Trace Elements and Paraoxonase-1 Activity in Lower Extremity Artery Disease

  • Joaquim Rovira
  • Anna Hernández-Aguilera
  • Fedra Luciano-Mateo
  • Noemí Cabré
  • Gerard Baiges-Gaya
  • Martí Nadal
  • Vicente Martín-Paredero
  • Jordi Camps
  • Jorge Joven
  • José L. Domingo
Article

Abstract

Oxidative stress and inflammation are candidate mechanisms to explain the potential role of exposure to metals and reduced activity of paraoxonase-1 (PON1) in age-related diseases. Both may be risk factors contributing to atherosclerosis. In the present study, inductively coupled mass spectrometry was used to explore multiple trace elements, while in-house methods were employed to measure PON1-related variables in patients with lower extremity artery disease (LEAD). Healthy controls were matched for sex, age, body weight, and relevant genotype variants. Serum concentrations of As, Ba, Cu, and Sr were higher in patients than those in controls, with a strong predictive ability to discriminate between groups. Differences in serum Pb, Cd, and Zn were negligible. Serum Cu increased when the disease was more severe, but a negative trend was noted for serum As, B, Ba, and Zn. The only variable associated with ankle-brachial index was serum Zn. Serum PON1 activity was significantly lower in LEAD patients. When the ability of serum trace elements to modulate PON1 activity was explored, the analysis revealed a unique association with serum Zn. The current results strongly suggest that Zn may have a protective effect in non-coronary atherosclerosis and indicate that this element may exert its anti-inflammatory and antioxidant functions through interactions with PON1 activity. These findings deserve confirmation and further research. In particular, the periodic evaluation of serum trace elements and the prescription of Zn supplements are easy measures to implement and that can improve the treatment of patients with LEAD.

Keywords

Inflammation Oxidation Lower extremity arterial disease Vascular toxicity Zinc 

Notes

Authors’ Contributions

MN, JC, JJ, and JLD designed the study. VMP recruited patients for the study and managed data collection. JR, AHA, FLM, NC, and GBG performed the analyses and collected data. JR and AHA performed the statistical analyses. JC, JJ, and JLD wrote the manuscript which was revised and accepted by all authors.

Funding Information

J. Rovira received funds from Health Department of Catalonia Government, through “Pla Estratègic de Recerca i Innovació en salut” (PERIS 2016–2020) fellowship (SLT002/16/00094). A. Hernández is the recipient of a fellowship of Fundació La Marató de TV3. Current work in our laboratories is supported by grants from the Plan Nacional de I+D+I, Spain, Instituto de Salud Carlos III (PI15/00285, co-founded by the European Regional Development Fund [FEDER]), the Agència de Gestió d’Ajuts Universitaris i de Recerca (AGAUR) (2014 SGR1227), and the Fundació La Marató de TV3.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Yang X, Li Y, Li Y, Ren X, Zhang X, Hu D, Gao Y, Xing Y, Shang H (2017) Oxidative stress-mediated atherosclerosis: mechanisms and therapies. Front Physiol 8:600.  https://doi.org/10.3389/fphys.2017.00600 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Hernández-Aguilera A, Rull A, Rodríguez-Gallego E, Riera-Borrull M, Luciano-Mateo F, Camps J, Menéndez JA, Joven J (2013) Mitochondrial dysfunction: a basic mechanism in inflammation-related non-communicable diseases and therapeutic opportunities. Mediat Inflamm 2013(135698):1–13.  https://doi.org/10.1155/2013/135698 CrossRefGoogle Scholar
  3. 3.
    Fort-Gallifa I, Hernández-Aguilera A, García-Heredia A, Cabré N, Luciano-Mateo F, Simó JM, Martín-Paredero V, Camps J, Joven J (2017) Galectin-3 in peripheral artery disease. Relationships with markers of oxidative stress and inflammation. Int J Mol Sci 18(5).  https://doi.org/10.3390/ijms18050973.CrossRefGoogle Scholar
  4. 4.
    Wang H, Naghavi M, Allen C, Barber RM, Bhutta ZA, Carter A, Casey DC, Charlson FJ, Chen AZ, Coates MM, Coggeshall M, Dandona L, Dicker DJ, Erskine HE, Ferrari AJ, Fitzmaurice C, Foreman K, Forouzanfar MH, Fraser MS, Fullman N, Gething PW, Goldberg EM, Graetz N, Haagsma JA, Hay SI, Huynh C, Johnson CO, Kassebaum NJ, Kinfu Y, Kulikoff XR, Kutz M, Kyu HH, Larson HJ, Leung J, Liang X, Lim SS, Lind M, Lozano R, Marquez N, Mensah GA, Mikesell J, Mokdad AH, Mooney MD, Nguyen G, Nsoesie E, Pigott DM, Pinho C, Roth GA, Salomon JA, Sandar L, Silpakit N, Sligar A, Sorensen RJD, Stanaway J, Steiner C, Teeple S, Thomas BA, Troeger C, VanderZanden A, Vollset SE, Wanga V, Whiteford HA, Wolock T, Zoeckler L, Abate KH, Abbafati C, Abbas KM, Abd-Allah F, Abera SF, Abreu DMX, Abu-Raddad LJ, Abyu GY, Achoki T, Adelekan AL, Ademi Z, Adou AK, Adsuar JC, Afanvi KA, Afshin A, Agardh EE, Agarwal A, Agrawal A, Kiadaliri AA, Ajala ON, Akanda AS, Akinyemi RO, Akinyemiju TF, Akseer N, Lami FHA, Alabed S, al-Aly Z, Alam K, Alam NKM, Alasfoor D, Aldhahri SF, Aldridge RW, Alegretti MA, Aleman AV, Alemu ZA, Alexander LT, Alhabib S, Ali R, Alkerwi A', Alla F, Allebeck P, al-Raddadi R, Alsharif U, Altirkawi KA, Martin EA, Alvis-Guzman N, Amare AT, Amegah AK, Ameh EA, Amini H, Ammar W, Amrock SM, Andersen HH, Anderson BO, Anderson GM, Antonio CAT, Aregay AF, Ärnlöv J, Arsenijevic VSA, Artaman A, Asayesh H, Asghar RJ, Atique S, Avokpaho EFGA, Awasthi A, Azzopardi P, Bacha U, Badawi A, Bahit MC, Balakrishnan K, Banerjee A, Barac A, Barker-Collo SL, Bärnighausen T, Barregard L, Barrero LH, Basu A, Basu S, Bayou YT, Bazargan-Hejazi S, Beardsley J, Bedi N, Beghi E, Belay HA, Bell B, Bell ML, Bello AK, Bennett DA, Bensenor IM, Berhane A, Bernabé E, Betsu BD, Beyene AS, Bhala N, Bhalla A, Biadgilign S, Bikbov B, Abdulhak AAB, Biroscak BJ, Biryukov S, Bjertness E, Blore JD, Blosser CD, Bohensky MA, Borschmann R, Bose D, Bourne RRA, Brainin M, Brayne CEG, Brazinova A, Breitborde NJK, Brenner H, Brewer JD, Brown A, Brown J, Brugha TS, Buckle GC, Butt ZA, Calabria B, Campos-Nonato IR, Campuzano JC, Carapetis JR, Cárdenas R, Carpenter DO, Carrero JJ, Castañeda-Orjuela CA, Rivas JC, Catalá-López F, Cavalleri F, Cercy K, Cerda J, Chen W, Chew A, Chiang PPC, Chibalabala M, Chibueze CE, Chimed-Ochir O, Chisumpa VH, Choi JYJ, Chowdhury R, Christensen H, Christopher DJ, Ciobanu LG, Cirillo M, Cohen AJ, Colistro V, Colomar M, Colquhoun SM, Cooper C, Cooper LT, Cortinovis M, Cowie BC, Crump JA, Damsere-Derry J, Danawi H, Dandona R, Daoud F, Darby SC, Dargan PI, das Neves J, Davey G, Davis AC, Davitoiu DV, de Castro EF, de Jager P, Leo DD, Degenhardt L, Dellavalle RP, Deribe K, Deribew A, Dharmaratne SD, Dhillon PK, Diaz-Torné C, Ding EL, dos Santos KPB, Dossou E, Driscoll TR, Duan L, Dubey M, Duncan BB, Ellenbogen RG, Ellingsen CL, Elyazar I, Endries AY, Ermakov SP, Eshrati B, Esteghamati A, Estep K, Faghmous IDA, Fahimi S, Faraon EJA, Farid TA, Farinha CSS, Faro A, Farvid MS, Farzadfar F, Feigin VL, Fereshtehnejad SM, Fernandes JG, Fernandes JC, Fischer F, Fitchett JRA, Flaxman A, Foigt N, Fowkes FGR, Franca EB, Franklin RC, Friedman J, Frostad J, Fürst T, Futran ND, Gall SL, Gambashidze K, Gamkrelidze A, Ganguly P, Gankpé FG, Gebre T, Gebrehiwot TT, Gebremedhin AT, Gebru AA, Geleijnse JM, Gessner BD, Ghoshal AG, Gibney KB, Gillum RF, Gilmour S, Giref AZ, Giroud M, Gishu MD, Giussani G, Glaser E, Godwin WW, Gomez-Dantes H, Gona P, Goodridge A, Gopalani SV, Gosselin RA, Gotay CC, Goto A, Gouda HN, Greaves F, Gugnani HC, Gupta R, Gupta R, Gupta V, Gutiérrez RA, Hafezi-Nejad N, Haile D, Hailu AD, Hailu GB, Halasa YA, Hamadeh RR, Hamidi S, Hancock J, Handal AJ, Hankey GJ, Hao Y, Harb HL, Harikrishnan S, Haro JM, Havmoeller R, Heckbert SR, Heredia-Pi IB, Heydarpour P, Hilderink HBM, Hoek HW, Hogg RS, Horino M, Horita N, Hosgood HD, Hotez PJ, Hoy DG, Hsairi M, Htet AS, Htike MMT, Hu G, Huang C, Huang H, Huiart L, Husseini A, Huybrechts I, Huynh G, Iburg KM, Innos K, Inoue M, Iyer VJ, Jacobs TA, Jacobsen KH, Jahanmehr N, Jakovljevic MB, James P, Javanbakht M, Jayaraman SP, Jayatilleke AU, Jeemon P, Jensen PN, Jha V, Jiang G, Jiang Y, Jibat T, Jimenez-Corona A, Jonas JB, Joshi TK, Kabir Z, Kamal R, Kan H, Kant S, Karch A, Karema CK, Karimkhani C, Karletsos D, Karthikeyan G, Kasaeian A, Katibeh M, Kaul A, Kawakami N, Kayibanda JF, Keiyoro PN, Kemmer L, Kemp AH, Kengne AP, Keren A, Kereselidze M, Kesavachandran CN, Khader YS, Khalil IA, Khan AR, Khan EA, Khang YH, Khera S, Khoja TAM, Kieling C, Kim D, Kim YJ, Kissela BM, Kissoon N, Knibbs LD, Knudsen AK, Kokubo Y, Kolte D, Kopec JA, Kosen S, Koul PA, Koyanagi A, Krog NH, Defo BK, Bicer BK, Kudom AA, Kuipers EJ, Kulkarni VS, Kumar GA, Kwan GF, Lal A, Lal DK, Lalloo R, Lallukka T, Lam H, Lam JO, Langan SM, Lansingh VC, Larsson A, Laryea DO, Latif AA, Lawrynowicz AEB, Leigh J, Levi M, Li Y, Lindsay MP, Lipshultz SE, Liu PY, Liu S, Liu Y, Lo LT, Logroscino G, Lotufo PA, Lucas RM, Lunevicius R, Lyons RA, Ma S, Machado VMP, Mackay MT, MacLachlan JH, Razek HMAE, Magdy M, Razek AE, Majdan M, Majeed A, Malekzadeh R, Manamo WAA, Mandisarisa J, Mangalam S, Mapoma CC, Marcenes W, Margolis DJ, Martin GR, Martinez-Raga J, Marzan MB, Masiye F, Mason-Jones AJ, Massano J, Matzopoulos R, Mayosi BM, McGarvey ST, McGrath JJ, McKee M, McMahon BJ, Meaney PA, Mehari A, Mehndiratta MM, Mejia-Rodriguez F, Mekonnen AB, Melaku YA, Memiah P, Memish ZA, Mendoza W, Meretoja A, Meretoja TJ, Mhimbira FA, Micha R, Millear A, Miller TR, Mirarefin M, Misganaw A, Mock CN, Mohammad KA, Mohammadi A, Mohammed S, Mohan V, Mola GLD, Monasta L, Hernandez JCM, Montero P, Montico M, Montine TJ, Moradi-Lakeh M, Morawska L, Morgan K, Mori R, Mozaffarian D, Mueller UO, Murthy GVS, Murthy S, Musa KI, Nachega JB, Nagel G, Naidoo KS, Naik N, Naldi L, Nangia V, Nash D, Nejjari C, Neupane S, Newton CR, Newton JN, Ng M, Ngalesoni FN, de Dieu Ngirabega J, Nguyen QL, Nisar MI, Pete PMN, Nomura M, Norheim OF, Norman PE, Norrving B, Nyakarahuka L, Ogbo FA, Ohkubo T, Ojelabi FA, Olivares PR, Olusanya BO, Olusanya JO, Opio JN, Oren E, Ortiz A, Osman M, Ota E, Ozdemir R, PA M, Pain A, Pandian JD, Pant PR, Papachristou C, Park EK, Park JH, Parry CD, Parsaeian M, Caicedo AJP, Patten SB, Patton GC, Paul VK, Pearce N, Pedro JM, Stokic LP, Pereira DM, Perico N, Pesudovs K, Petzold M, Phillips MR, Piel FB, Pillay JD, Plass D, Platts-Mills JA, Polinder S, Pope CA, Popova S, Poulton RG, Pourmalek F, Prabhakaran D, Qorbani M, Quame-Amaglo J, Quistberg DA, Rafay A, Rahimi K, Rahimi-Movaghar V, Rahman M, Rahman MHU, Rahman SU, Rai RK, Rajavi Z, Rajsic S, Raju M, Rakovac I, Rana SM, Ranabhat CL, Rangaswamy T, Rao P, Rao SR, Refaat AH, Rehm J, Reitsma MB, Remuzzi G, Resnikoff S, Ribeiro AL, Ricci S, Blancas MJR, Roberts B, Roca A, Rojas-Rueda D, Ronfani L, Roshandel G, Rothenbacher D, Roy A, Roy NK, Ruhago GM, Sagar R, Saha S, Sahathevan R, Saleh MM, Sanabria JR, Sanchez-Niño MD, Sanchez-Riera L, Santos IS, Sarmiento-Suarez R, Sartorius B, Satpathy M, Savic M, Sawhney M, Schaub MP, Schmidt MI, Schneider IJC, Schöttker B, Schutte AE, Schwebel DC, Seedat S, Sepanlou SG, Servan-Mori EE, Shackelford KA, Shaddick G, Shaheen A, Shahraz S, Shaikh MA, Shakh-Nazarova M, Sharma R, She J, Sheikhbahaei S, Shen J, Shen Z, Shepard DS, Sheth KN, Shetty BP, Shi P, Shibuya K, Shin MJ, Shiri R, Shiue I, Shrime MG, Sigfusdottir ID, Silberberg DH, Silva DAS, Silveira DGA, Silverberg JI, Simard EP, Singh A, Singh GM, Singh JA, Singh OP, Singh PK, Singh V, Soneji S, Søreide K, Soriano JB, Sposato LA, Sreeramareddy CT, Stathopoulou V, Stein DJ, Stein MB, Stranges S, Stroumpoulis K, Sunguya BF, Sur P, Swaminathan S, Sykes BL, Szoeke CEI, Tabarés-Seisdedos R, Tabb KM, Takahashi K, Takala JS, Talongwa RT, Tandon N, Tavakkoli M, Taye B, Taylor HR, Ao BJT, Tedla BA, Tefera WM, Have MT, Terkawi AS, Tesfay FH, Tessema GA, Thomson AJ, Thorne-Lyman AL, Thrift AG, Thurston GD, Tillmann T, Tirschwell DL, Tonelli M, Topor-Madry R, Topouzis F, Towbin JA, Traebert J, Tran BX, Truelsen T, Trujillo U, Tura AK, Tuzcu EM, Uchendu US, Ukwaja KN, Undurraga EA, Uthman OA, Dingenen RV, van Donkelaar A, Vasankari T, Vasconcelos AMN, Venketasubramanian N, Vidavalur R, Vijayakumar L, Villalpando S, Violante FS, Vlassov VV, Wagner JA, Wagner GR, Wallin MT, Wang L, Watkins DA, Weichenthal S, Weiderpass E, Weintraub RG, Werdecker A, Westerman R, White RA, Wijeratne T, Wilkinson JD, Williams HC, Wiysonge CS, Woldeyohannes SM, Wolfe CDA, Won S, Wong JQ, Woolf AD, Xavier D, Xiao Q, Xu G, Yakob B, Yalew AZ, Yan LL, Yano Y, Yaseri M, Ye P, Yebyo HG, Yip P, Yirsaw BD, Yonemoto N, Yonga G, Younis MZ, Yu S, Zaidi Z, Zaki MES, Zannad F, Zavala DE, Zeeb H, Zeleke BM, Zhang H, Zodpey S, Zonies D, Zuhlke LJ, Vos T, Lopez AD, Murray CJL (2016) Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388:1459–1544.  https://doi.org/10.1016/S0140-6736(16)31012-1 CrossRefGoogle Scholar
  5. 5.
    Stoner MC, Calligaro KD, Chaer RA, Dietzek AM, Farber A, Guzman RJ, Hamdan AD, Landry GJ, Yamaguchi DJ, Society for Vascular Surgery (2016) Reporting standards of the Society for Vascular Surgery for endovascular treatment of chronic lower extremity peripheral artery disease. J Vasc Surg 64:e1–e21.  https://doi.org/10.1016/j.jvs.2016.03.420 CrossRefPubMedGoogle Scholar
  6. 6.
    Nigra AE, Ruiz-Hernandez A, Redon J, Navas-Acien A, Tellez-Plaza M (2016) Environmental metals and cardiovascular disease in adults: a systematic review beyond lead and cadmium. Curr Environ Health Rep 3:416–433.  https://doi.org/10.1007/s40572-016-0117-9 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Solenkova NV, Newman JD, Berger JS, Thurston G, Hochman JS, Lamas GA (2014) Metal pollutants and cardiovascular disease: mechanisms and consequences of exposure. Am Heart J 168:812–822.  https://doi.org/10.1016/j.ahj.2014.07.007 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Lamas GA, Navas-Acien A, Mark DB, Lee KL (2016) Heavy metals, cardiovascular disease, and the unexpected benefits of chelation therapy. J Am Coll Cardiol 67:2411–2418.  https://doi.org/10.1016/j.jacc.2016.02.066 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87.  https://doi.org/10.1016/j.tox.2011.03.001 CrossRefGoogle Scholar
  10. 10.
    Martí-Cid R, Llobet JM, Castell V, Domingo JL (2008) Dietary intake of arsenic, cadmium, mercury, and lead by the population of Catalonia, Spain. Biol Trace Elem Res 125:120–132.  https://doi.org/10.1007/s12011-008-8162-3 CrossRefPubMedGoogle Scholar
  11. 11.
    Perelló G, Vicente E, Castell V, Llobet JM, Nadal M, Domingo JL (2015) Dietary intake of trace elements by the population of Catalonia (Spain): results from a total diet study. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32:748–755.  https://doi.org/10.1080/19440049.2015.1018844 CrossRefPubMedGoogle Scholar
  12. 12.
    Aranda N, Valls RM, Romeu M, Sánchez-Martos V, Albaladejo R, Fernández-Castillejo S, Nogués R, Catalán Ú, Pedret A, Espinel A, Delgado MA, Arija V, Sola R, Giralt M (2017) Consumption of seafood and its estimated heavy metals are associated with lipid profile and oxidative lipid damage on healthy adults from a Spanish Mediterranean area: a cross-sectional study. Environ Res 156:644–651.  https://doi.org/10.1016/j.envres.2017.04.037 CrossRefPubMedGoogle Scholar
  13. 13.
    Costa LG, Cole TB, Garrick JM, Marsillach J, Furlong CE (2017) Metals and paraoxonases. Adv Neurobiol 18:85–111.  https://doi.org/10.1007/978-3-319-60189-2_5 CrossRefPubMedGoogle Scholar
  14. 14.
    Kresanov P, Vasankari T, Ahotupa M, Kaikkonen J, Hutri-Kähönen N, Juonala M, Kähönen M, Lehtimäki T, Viikari J, Raitakari OT (2015) Paraoxonase-1 and oxidized lipoprotein lipids. The cardiovascular risk in young Finns study. Atherosclerosis 241:502–506.  https://doi.org/10.1016/j.atherosclerosis.2015.06.004 CrossRefGoogle Scholar
  15. 15.
    Aviram M, Rosenblat M (2004) Paraoxonases 1, 2, and 3, oxidative stress, and macrophage cell formation during atherosclerosis development. Free Radic Biol Med 37:1304–1316.  https://doi.org/10.1016/j.freeradbiomed.2004.06.030 CrossRefPubMedGoogle Scholar
  16. 16.
    Camps J, Rodríguez-Gallego E, García-Heredia A, Triguero I, Riera-Borrull M, Hernández-Aguilera A, Luciano-Mateo F, Fernández-Arroyo S, Joven J (2014) Paraoxonases and chemokine (C-C motif) ligand-2 in non-communicable diseases. In: Makowski GS (ed) Advances in Clinical Chemistry 63, Elsevier, pp 247–308Google Scholar
  17. 17.
    Hernández-Aguilera A, Sepúlveda J, Rodríguez-Gallego E, Guirro M, García-Heredia A, Cabré N, Luciano-Mateo F, Fort-Gallifa I, Martín-Paredero V, Joven J, Camps J (2015) Immunohistochemical analysis of paraoxonases and chemokines in arteries of patients with peripheral artery disease. Int J Mol Sci 16:11323–11338.  https://doi.org/10.3390/ijms160511323 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Atsumi T, Numano F (1975) Blood zinc levels in patients with arteriosclerosis obliterans, thromboangiitis obliterans and Takayasu’s disease. Jpn Heart J 16:664–669CrossRefGoogle Scholar
  19. 19.
    Iskra M, Majewski W, Piorunska-Stolzmann M (2002) Modifications of magnesium and copper concentrations in serum and arterial wall of patients with vascular diseases related to ageing, atherosclerosis and aortic aneurysm. Magnes Res 15:279–285PubMedGoogle Scholar
  20. 20.
    Iskra M, Barałkiewicz D, Majewski W, Pioruńska-Stolzmann M (2005) Serum magnesium, copper and zinc concentration changes in lower limb ischemia and postoperative treatment. Magnes Res 18:261–267PubMedGoogle Scholar
  21. 21.
    Kasprzak M, Iskra M, Majewski W, Wielkoszyński T (2009) Arylesterase and paraoxonase activity of paraoxonase (PON1) affected by ischemia in the plasma of patients with arterial occlusion of the lower limbs. Clin Biochem 42(1–2):50–56.  https://doi.org/10.1016/j.clinbiochem.2008.09.117 CrossRefPubMedGoogle Scholar
  22. 22.
    Kasprzak MP, Iskra M, Majewski W, Budzyń-Napierała M, Gryszczyńska B, Strzyżewski K, Kasprzak J (2014) PON1 status evaluation in patients with chronic arterial occlusion of lower limbs due to atherosclerosis obliterans. Arch Med Sci 10(6):1101–1108.  https://doi.org/10.5114/aoms.2014.41348 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Novo S (2002) Classification, epidemiology, risk factors, and natural history of peripheral arterial disease. Diabetes Obes Metab 4:S1–S6.  https://doi.org/10.1046/j.1463-1326.2002.0040s20s1.x CrossRefPubMedGoogle Scholar
  24. 24.
    Martinelli N, García-Heredia A, Roca H, Aranda N, Arija V, Mackness B, Mackness M, Busti F, Aragonès G, Pedro-Botet J, Pedica F, Cataldo I, Marsillach J, Joven J, Girelli D, Camps J (2013) Paraoxonase-1 status in patients with hereditary hemochromatosis. J Lipid Res 54:1484–1492.  https://doi.org/10.1194/jlr.P028977 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ferré N, Camps J, Prats E, Vilella E, Paul A, Figuera L, Joven J (2002) Serum paraoxonase activity: a new additional test for the improved evaluation of chronic liver damage. Clin Chem 48:261–268PubMedGoogle Scholar
  26. 26.
    Camps J, Mackness M, Mackness B, Marsillach J, Joven J (2010) Serum paraoxonase-1 activity and genetic polymorphisms: common errors in measurement and interpretation of results. Clin Chem Lab Med 48:893–894.  https://doi.org/10.1515/CCLM.2010.156 CrossRefPubMedGoogle Scholar
  27. 27.
    World Health Organization (2014) Ambient (outdoor) air quality and health [online], http://www.who.int/mediacentre/factsheets/fs313/en/
  28. 28.
    Cosselman KE, Navas-Acien A, Kaufman JD (2015) Environmental factors in cardiovascular disease. Nat Rev Cardiol 12:627–642.  https://doi.org/10.1038/nrcardio.2015.152 CrossRefPubMedGoogle Scholar
  29. 29.
    Navas-Acien A, Selvin E, Sharrett AR, Calderon-Aranda E, Silbergeld E, Guallar E (2004) Lead, cadmium, smoking, and increased risk of peripheral arterial disease. Circulation 109:3196–3201.  https://doi.org/10.1161/01.CIR.0000130848.18636.B2 CrossRefPubMedGoogle Scholar
  30. 30.
    Gupta P, Desai PB (2013) Status of copper and antioxidants in atherosclerotic coronary heart disease—a cross sectional study. Biomed 33:224–228Google Scholar
  31. 31.
    Simeonova PP, Luster MI (2004) Arsenic and atherosclerosis. Toxicol Appl Pharmacol 198:444–449.  https://doi.org/10.1016/j.taap.2003.10.018 CrossRefPubMedGoogle Scholar
  32. 32.
    Navas-Acien A, Silbergeld EK, Sharrett AR, Calderon-Aranda E, Selvin E, Guallar E (2005) Metals in urine and peripheral arterial disease. Environ Health Perspect 113:164–169.  https://doi.org/10.1289/ehp.7329 CrossRefPubMedGoogle Scholar
  33. 33.
    Bo S, Durazzo M, Gambino R, Berutti C, Milanesio N, Caropreso A, Gentile L, Cassader M, Cavallo-Perin P, Pagano G (2008) Associations of dietary and serum copper with inflammation, oxidative stress, and metabolic variables in adults. J Nutr 138:305–310CrossRefGoogle Scholar
  34. 34.
    Yalin S, Sagir O, Comelekoglu U, Berkoz̈ M, Eroglu P (2012) Strontium ranelate treatment improves oxidative damage in osteoporotic rat model. Pharmacol Reports 64:396–402CrossRefGoogle Scholar
  35. 35.
    Valko M, Jomova K, Rhodes CJ, Kuča K, Musílek K (2016) Redox- and non-redox-metal-induced formation of free radicals and their role in human disease. Arch Toxicol 90:1–37.  https://doi.org/10.1007/s00204-015-1579-5 CrossRefPubMedGoogle Scholar
  36. 36.
    Aviram M, Rosenblat M, Billecke S, Erogul J, Sorenson R, Bisgaier CL, Newton RS, La Du B (1999) Human serum paraoxonase (PON 1) is inactivated by oxidized low density lipoprotein and preserved by antioxidants. Free Radic Biol Med 26:892–904.  https://doi.org/10.1016/S0891-5849(98)00272-X CrossRefPubMedGoogle Scholar
  37. 37.
    Marsillach J, Camps J, Beltran-Debón R, Rull A, Aragones G, Maestre-Martínez C, Sabench F, Hernández M, Castillo DD, Joven J, Mackness M, Mackness B (2011) Immunohistochemical analysis of paraoxonases-1 and 3 in human atheromatous plaques. Eur J Clin Investig 41:308–314.  https://doi.org/10.1111/j.1365-2362.2010.02411.x CrossRefGoogle Scholar
  38. 38.
    Cabré M, Ferré N, Folch J, Paternain JL, Hernàndez M, del Castillo D, Joven J, Camps J (1999) Inhibition of hepatic cell nuclear DNA fragmentation by zinc in carbon tetrachloride-treated rats. J Hepatol 31:228–234CrossRefGoogle Scholar
  39. 39.
    Ferré N, Camps J, Cabré M, Paul A, Joven J (2001) Hepatic paraoxonase activity alterations and free radical production in rats with experimental cirrhosis. Metabolism 50(9):997–1000.  https://doi.org/10.1016/S0168-8278(99)80218-9 CrossRefPubMedGoogle Scholar
  40. 40.
    Tas S, Srandol E, Ziyanok-Ayvalik S, Ocak N, Serdar Z, Dirican M (2006) Vanadyl sulfate treatment improves oxidative stress and increases serum paraoxonase activity in streptozotocin-induced diabetic rats. Nutr Res 26:670–676.  https://doi.org/10.1016/j.nutres.2006.09.022 CrossRefGoogle Scholar
  41. 41.
    Ferramola ML, Perez Diaz MFF, Honore SM, Sanchez SS, Anton RI, Anzulovich AC, Gimenez MS (2012) Cadmium-induced oxidative stress and histological damage in the myocardium. Effects of a soy-based diet. Toxicol Appl Pharmacol 265:380–389.  https://doi.org/10.1016/j.taap.2012.09.009 CrossRefPubMedGoogle Scholar
  42. 42.
    Ebabe Elle R, Gaillet S, Vide J, Romain C, Lauret C, Rugani N, Cristol JP, Rouanet JM (2013) Dietary exposure to silver nanoparticles in Sprague-Dawley rats: effects on oxidative stress and inflammation. Food Chem Toxicol 60:297–301.  https://doi.org/10.1016/j.fct.2013.07.071 CrossRefPubMedGoogle Scholar
  43. 43.
    Hernandez AF, Gil F, Leno E, Lopez O, Rodrigo L, Pla A (2009) Interaction between human serum esterases and environmental metal compounds. Neurotoxicology 30:628–635.  https://doi.org/10.1016/j.neuro.2009.04.003 CrossRefPubMedGoogle Scholar
  44. 44.
    Pollack AZ, Sjaarda L, Ahrens KA, Mumford SL, Browne RW, Wactawski-Wende J, Schisterman EF (2014) Association of cadmium, lead and mercury with paraoxonase 1 activity in women. PLoS One 9:e92152.  https://doi.org/10.1371/journal.pone.0092152 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Laird BD, Gongharov AB, Ayotte P, Chan HM (2015) Relationship between the esterase paraoxonase-1 (PON1) and metal concentrations in whole blood of Inuit in Canada. Chemosphere 120:479–485.  https://doi.org/10.1016/j.chemosphere.2014.08.073 CrossRefPubMedGoogle Scholar
  46. 46.
    Cayir Y, Cayir A, Turan MI, Kurt N, Kara M, Lalaoglu E, Ciftel M, Yildirim A (2014) Antioxidant status in blood of obese children: the relation between trace elements, paraoxonase, and arylesterase values. Biol Trace Elem Res 160:155–160.  https://doi.org/10.1007/s12011-014-0038-0 CrossRefPubMedGoogle Scholar
  47. 47.
    Bao B, Prasad AS, Beck FW, Fitzgerald JT, Snell D, Bao GW, Singh T, Cardozo LJ (2010) Zinc decreases C-reactive protein, lipid peroxidation, and inflammatory cytokines in elderly subjects: a potential implication of zinc as an atheroprotective agent. Am J Clin Nutr 91:1634–1641.  https://doi.org/10.3945/ajcn.2009.28836 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Rahimi-Ardabili B, Argani H, Ghorbanihaghjo A, Rashtchizadeh N, Naghavi-Behzad M, Ghorashi S, Nezami N (2012) Paraoxonase enzyme activity is enhanced by zinc supplementation in hemodialysis patients. Ren Fail 34:1123–1128.  https://doi.org/10.3109/0886022X.2012.717479 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Joaquim Rovira
    • 1
  • Anna Hernández-Aguilera
    • 2
  • Fedra Luciano-Mateo
    • 2
  • Noemí Cabré
    • 2
  • Gerard Baiges-Gaya
    • 2
  • Martí Nadal
    • 1
  • Vicente Martín-Paredero
    • 3
  • Jordi Camps
    • 2
  • Jorge Joven
    • 2
  • José L. Domingo
    • 1
  1. 1.Laboratory of Toxicology and Environmental Health, School of Medicine, Institut d’Investigació Sanitària Pere VirgiliUniversitat Rovira i VirgiliReusSpain
  2. 2.Unitat de Recerca Biomèdica, Hospital Universitari Sant Joan, Institut d’Investigació Sanitària Pere VirgiliUniversitat Rovira i VirgiliReusSpain
  3. 3.Department of Vascular SurgeryHospital Universitari Joan XXIIITarragonaSpain

Personalised recommendations