High Content of Lead Is Associated with the Softness of Drinking Water and Raised Cardiovascular Morbidity: A Review

  • Geir Bjørklund
  • Maryam Dadar
  • Salvatore Chirumbolo
  • Jan Aaseth
Article
First Online:
Received:
Accepted:
  • 11 Downloads

Abstract

Daily ingestion of lead (Pb), even through piped drinking water, has long time been an important issue of concern, attracting for decades research in environmental science and toxicology, and again comes to prominence because of recent high-profile cases of exposure of populations in several countries to Pb-contaminated water. Numerous studies have reported an association between Pb in water and the risk of cardiovascular pathologies. Low levels of magnesium and calcium, i.e., low degree of hardness of the drinking water, may accentuate Pb leaching from water pipes and furthermore increase Pb absorption. This review evaluates the evidence for an association between Pb exposure from drinking water and cardiovascular end points in human populations.

Keywords

Drinking water Lead Cardiovascular disease Mortality 
This is a preview of subscription content, log in to check access

Notes

Acknowledgements

The authors thank Evens Emmanuel and John McArthur for valuable comments and assistance with the editing.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Mathers CD, Loncar D (2006) Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3:e442PubMedPubMedCentralGoogle Scholar
  2. 2.
    Fewtrell LJ, Prüss-Üstün A, Landrigan P, Ayuso-Mateos JL (2004) Estimating the global burden of disease of mild mental retardation and cardiovascular diseases from environmental lead exposure. Environ Res 94:120–133PubMedGoogle Scholar
  3. 3.
    Navas-Acien A, Guallar E, Silbergeld EK, Rothenberg SJ (2007) Lead exposure and cardiovascular disease—a systematic review. Environ Health Perspect 115:472–482PubMedGoogle Scholar
  4. 4.
    Poręba R, Gać P, Poręba M, Andrzejak R (2011) Environmental and occupational exposure to lead as a potential risk factor for cardiovascular disease. Environ Toxicol Pharmacol 31:267–277PubMedGoogle Scholar
  5. 5.
    Skoczyńska A, Gruber K, Belowska-Bień K, Mlynek V (2007) Risk of cardiovascular diseases in lead-exposed workers of crystal glassworks. Part I. Effect of lead on blood pressure and lipid metabolism (in Polish). Med Pr 58:475–483PubMedGoogle Scholar
  6. 6.
    Apostoli P, Corulli A, Metra M, Dei Cas L (2004) Lead and cardiopathy. Med Lav 95:124–132PubMedGoogle Scholar
  7. 7.
    Lancéreaux E (1881) Nephritis and saturnine arthritis; coincidences of these affections; parallel with nephritis and gouty arthritis (in French). Transact Int Med Congr 2:193–202Google Scholar
  8. 8.
    Almeida Lopes ACB, Silbergeld EK, Navas-Acien A, Zamoiski R, Martins ADC Jr, Camargo AEI, Urbano MR, Mesas AE, Paoliello MMB (2017) Association between blood lead and blood pressure: a population-based study in Brazilian adults. Environ Health 16:27PubMedPubMedCentralGoogle Scholar
  9. 9.
    Yang WY, Staessen JA (2018) Letter to editor: blood pressure, hypertension and lead exposure. Environ Health 17(1):16PubMedPubMedCentralGoogle Scholar
  10. 10.
    Yang WY, Efremov L, Mujaj B, Zhang ZY, Wei FF, Huang QF, Thijs L, Vanassche T, Nawrot TS, Staessen JA (2018) Association of office and ambulatory blood pressure with blood lead in workers before occupational exposure. J Am Soc Hypertens 12:14–24PubMedGoogle Scholar
  11. 11.
    Menke A, Muntner P, Batuman V, Silbergeld EK, Guallar E (2006) Blood lead below 0.48 micromol/L (10 microg/dL) and mortality among US adults. Circulation 114:1388–1394PubMedGoogle Scholar
  12. 12.
    Nawrot TS, Staessen JA (2006) Low-level environmental exposure to lead unmasked as silent killer. Circulation 114:1347–1349PubMedGoogle Scholar
  13. 13.
    Nawrot TS, Thijs L, Den Hond EM, Roels HA, Staessen JA (2002) An epidemiological re-appraisal of the association between blood pressure and blood lead: a meta-analysis. J Hum Hypertens 16:123–131PubMedGoogle Scholar
  14. 14.
    Rothenberg SJ, Kondrashov V, Manalo M, Jiang J, Cuellar R, Garcia M, Reynoso B, Reyes S, Diaz M, Todd AC (2002) Increases in hypertension and blood pressure during pregnancy with increased bone lead levels. Am J Epidemiol 156:1079–1087PubMedGoogle Scholar
  15. 15.
    Jiao J, Wang M, Wang Y, Sun N, Li C (2016) Lead exposure increases blood pressure by increasing angiotensinogen expression. J Environ Sci Health A Tox Hazard Subst Environ Eng 51:434–439PubMedGoogle Scholar
  16. 16.
    Lu X, Xu X, Zhang Y, Zhang Y, Wang C, Huo X (2018) Elevated inflammatory Lp-PLA2 and IL-6 link e-waste Pb toxicity to cardiovascular risk factors in preschool children. Environ Pollut 234:601–609PubMedGoogle Scholar
  17. 17.
    Karrari P, Mehrpour O, Abdollahi M (2012) A systematic review on status of lead pollution and toxicity in Iran; guidance for preventive measures. Daru 20:2PubMedPubMedCentralGoogle Scholar
  18. 18.
    Okkenhaug G, Gebhardt KA, Amstaetter K, Bue HL, Herzel H, Mariussen E, Almås ÅR, Cornelissen G, Breedveld GD, Rasmussen G, Mulder J (2016) Antimony (Sb) and lead (Pb) in contaminated shooting range soils: Sb and Pb mobility and immobilization by iron based sorbents, a field study. J Hazard Mater 307:336–343PubMedGoogle Scholar
  19. 19.
    Khalid S, Shahid M, Dumat C, Niazi NK, Bibi I, Gul Bakhat HF, Abbas G, Murtaza B, Javeed HM (2017) Influence of groundwater and wastewater irrigation on lead accumulation in soil and vegetables: implications for health risk assessment and phytoremediation. Int J Phytoremediation 19:1037–1046PubMedGoogle Scholar
  20. 20.
    Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG (2008) Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ Pollut 152:686–692PubMedGoogle Scholar
  21. 21.
    Kumar Sharma R, Agrawal M, Marshall F (2007) Heavy metal contamination of soil and vegetables in suburban areas of Varanasi, India. Ecotoxicol Environ Saf 66:258–266PubMedGoogle Scholar
  22. 22.
    Tiwari KK, Singh NK, Patel MP, Tiwari MR, Rai UN (2011) Metal contamination of soil and translocation in vegetables growing under industrial wastewater irrigated agricultural field of Vadodara, Gujarat, India. Ecotoxicol Environ Saf 74:1670–1677PubMedGoogle Scholar
  23. 23.
    Ghosh AK, Bhatt MA, Agrawal HP (2012) Effect of long-term application of treated sewage water on heavy metal accumulation in vegetables grown in northern India. Environ Monit Assess 184:1025–1036PubMedGoogle Scholar
  24. 24.
    Mohankumar K, Hariharan V, Rao NP (2016) Heavy metal contamination in groundwater around industrial estate vs residential areas in Coimbatore, India. J Clin Diagn Res 10:BC05–BC07PubMedPubMedCentralGoogle Scholar
  25. 25.
    Tutic A, Novakovic S, Lutovac M, Biocanin R, Ketin S, Omerovic N (2015) The heavy metals in agrosystems and impact on health and quality of life. Open Access Maced J Med Sci 3:345–355PubMedPubMedCentralGoogle Scholar
  26. 26.
    Neamtiu IA, Al-Abed SR, McKernan JL, Baciu CL, Gurzau ES, Pogacean AO, Bessler SM (2017) Metal contamination in environmental media in residential areas around Romanian mining sites. Rev Environ Health 32:215–220PubMedGoogle Scholar
  27. 27.
    Dheri GS, Brar MS, Malhi SS (2007) Heavy-metal concentration of sewage-contaminated water and its impact on underground water, soil and crop plants in alluvial soils of Northwestern India. Comm. Soil Sci Plant Analysis 38:1353–1370Google Scholar
  28. 28.
    Asgari Lajayer B, Ghorbanpour M, Nikabadi S (2017) Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicol Environ Saf 145:377–390PubMedGoogle Scholar
  29. 29.
    Fifi U, Winiarski T, Emmanuel E (2010) Impacts of surface runoff in the aquifers of Port-au-Prince, Haiti. In: Laboy-Nieves EN, Goosen M, Emmanuel E (eds) Environmental and human health: risk management in developing countries. CRC Press, Boca Raton, pp 128–138Google Scholar
  30. 30.
    Schwartzbord JR, Emmanuel E, Brown DL (2013) Haiti's food and drinking water: a review of toxicological health risks. Clin Toxicol 51:828–833Google Scholar
  31. 31.
    Emmanuel E, Angerville R, Joseph O, Perrodin Y (2007) Human health risk assessment of lead in drinking water: a case study from Port-au-Prince. Haiti Int J Environ Pollut 31:280–291Google Scholar
  32. 32.
    Emmanuel E, Pierre MG, Perrodin Y (2009) Groundwater contamination by microbiological and chemical substances released from hospital wastewater: health risk assessment for drinking water consumers. Environ Int 35:718–726PubMedGoogle Scholar
  33. 33.
    Naccari C, Giangrosso G, Macaluso A, Billone E, Cicero A, D’Ascenzi C, Ferrantelli V (2013) Red foxes (Vulpes vulpes) bioindicator of lead and copper pollution in Sicily (Italy). Ecotoxicol Environ Saf 90:41–45PubMedGoogle Scholar
  34. 34.
    Kaur S (1988) Lead in the scales of cobras and wall lizards from rural and urban areas of Punjab. India Sci Total Environ 77:289–290PubMedGoogle Scholar
  35. 35.
    Underwood E (1977) Trace elements in human health and disease, 4th edn. New York, USA, Academic PressGoogle Scholar
  36. 36.
    Agency for Toxic Substances and Disease Registry. 2015 Priority list of hazardous substances. Available online: https://www.atsdr.cdc.gov/mrls/mrllist.asp (accessed on 4 October 2017)
  37. 37.
    Kumar M, Puri A (2012) A review of permissible limits of drinking water. Indian J Occup Environ Med 16:40PubMedPubMedCentralGoogle Scholar
  38. 38.
    World Health Organization. Guidelines for drinking-water quality: first addendum to the fourth edition. 2017. Available online:http://www.who.int/water_sanitation_health/publications/drinking-water-quality-guidelines-4-including-1st-addendum/en (accessed on 4 October 2017)
  39. 39.
    Ragan HA (1983) The bioavailability of iron, lead and cadmium via gastrointestinal absorption: a review. Sci Total Environ 28:317–326PubMedGoogle Scholar
  40. 40.
    Quaterman J (1986) Lead. In: Mertz W (ed) Trace elements in human and animal nutrition, vol Volume 2, 5th edn. Academic Press, Orlando, USA, pp 281–318Google Scholar
  41. 41.
    Fullmer CS (1991) Intestinal calcium and lead absorption: effects of dietary lead and calcium. Environ Res 54:159–169PubMedGoogle Scholar
  42. 42.
    Bogden JD, Gertner SB, Christakos S, Kemp FW, Yang Z, Katz SR, Chu C (1992) Dietary calcium modifies concentrations of lead and other metals and renal calbindin in rats. J Nutr 122:1351–1360PubMedGoogle Scholar
  43. 43.
    Bogden JD, Kemp FW (1995) Han S Dietary calcium and lead interact to modify maternal blood pressure, erythropoiesis, and fetal and neonatal growth in rats during pregnancy and lactation. J Nutr 125:990–1002Google Scholar
  44. 44.
    Yannai S, Sachs KM (1993) Absorption and accumulation of cadmium, lead and mercury from foods by rats. Food Chem Toxicol 31:351–355PubMedGoogle Scholar
  45. 45.
    Elsenhans B, Janser H, Windisch W, Schümann K (2011) Does lead use the intestinal absorptive pathways of iron? Impact of iron status on murine 210Pb and 59Fe absorption in duodenum and ileum in vivo. Toxicology 284:7–11PubMedGoogle Scholar
  46. 46.
    Luhovs'kyĭ SP (2001) The effect of iron and zinc on lead absorption in the tunica mucosa of various parts of rat small intestine (in Ukrainian). Fiziol Zh 47:41–45PubMedGoogle Scholar
  47. 47.
    Ollson CJ, Smith E, Herde P (2017) Influence of co-contaminant exposure on the absorption of arsenic, cadmium and lead. Chemosphere 168:658–666PubMedGoogle Scholar
  48. 48.
    Shannon M, Graef JW (1989) Lead intoxication from lead-contaminated water used to reconstitute infant formula. Clin Pediatr (Phila) 28:380–382Google Scholar
  49. 49.
    Schümann K (1990) The toxicological estimation of the heavy metal content (Cd, Hg, Pb) in food for infants and small children (in German). Z Ernahrungswiss 29:54–73PubMedGoogle Scholar
  50. 50.
    Safruk AM, McGregor E, Aslund ML, Cheung PH, Pinsent C, Jackson BJ, Hair AT, Lee M, Sigal EA (2017) The influence of lead content in drinking water, household dust, soil, and paint on blood lead levels of children in Flin Flon, Manitoba and Creighton, Saskatchewan. Sci Total Environ 593:202–210PubMedGoogle Scholar
  51. 51.
    Toscano CM, Simões MR, Alonso MJ, Salaices M, Vassallo DV, Fioresi M (2017) Sub-chronic lead exposure produces β(1)-adrenoceptor downregulation decreasing arterial pressure reactivity in rats. Life Sci 180:93–101PubMedGoogle Scholar
  52. 52.
    Silveira EA, Siman FD, de Oliveira FT, Vescovi MV, Furieri LB, Lizardo JH, Stefanon I, Padilha AS, Vassallo DV (2014) Low-dose chronic lead exposure increases systolic arterial pressure and vascular reactivity of rat aortas. Free Radic Biol Med 67:366–376PubMedGoogle Scholar
  53. 53.
    Nunes KZ, Nunes DO, Silveira EA, Almenara Cruz Pereira C, Broseghini Filho GB, Vassallo DV, Fioresi M (2015) Chronic lead exposure decreases the vascular reactivity of rat aortas: the role of hydrogen peroxide. PLoS One 10:e0120965PubMedPubMedCentralGoogle Scholar
  54. 54.
    Nussbaumer-Streit B, Yeoh B, Griebler U, Pfadenhauer LM, Busert LK, Lhachimi SK, Lohner S, Gartlehner G (2016) Household interventions for preventing domestic lead exposure in children. Cochrane Database Syst Rev 10:CD006047PubMedGoogle Scholar
  55. 55.
    Christensen JN, Halliday AN, Leigh KE, Randell RN, Kesler SE (1995) Direct dating of sulfides by Rb-Sr: a critical test using the Polaris Mississippi Valley-type Zn-Pb deposit. Geochim Cosmochim Acta 59:5191–5197Google Scholar
  56. 56.
    Münzel T, Daiber A (2018) Environmental stressors and their impact on health and disease with focus on oxidative stress. Antioxid Redox Signal 28:735–740PubMedGoogle Scholar
  57. 57.
    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 168:812–822PubMedPubMedCentralGoogle Scholar
  58. 58.
    Aneni EC, Escolar E, Lamas GA (2016) Chronic toxic metal exposure and cardiovascular disease: mechanisms of risk and emerging role of chelation therapy. Curr Atheroscler Rep 18:81PubMedGoogle Scholar
  59. 59.
    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 3:416–433PubMedPubMedCentralGoogle Scholar
  60. 60.
    Asgary S, Movahedian A, Keshvari M (2017) Serum levels of lead, mercury and cadmium in relation to coronary artery disease in the elderly: a cross-sectional study. Chemosphere 180:540–544PubMedGoogle Scholar
  61. 61.
    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 67:2411–2418PubMedPubMedCentralGoogle Scholar
  62. 62.
    Lamas GA, Goertz C, Boineau R (2013) Effect of disodium EDTA chelation regimen on cardiovascular events in patients with previous myocardial infarction: the TACT randomized trial. JAMA 309:1241–1250PubMedPubMedCentralGoogle Scholar
  63. 63.
    Ferreira de Mattos G, Costa C, Savio F, Alonso M, Nicolson GL (2017) Lead poisoning: acute exposure of the heart to lead ions promotes changes in cardiac function and Cav1.2 ion channels. Biophys Rev 9:807–825PubMedPubMedCentralGoogle Scholar
  64. 64.
    Fioresi M, Simões MR, Furieri LB, Broseghini-Filho GB, Vescovi MV, Stefanon I, Vassallo DV (2014) Chronic lead exposure increases blood pressure and myocardial contractility in rats. PLoS One 9:e96900PubMedPubMedCentralGoogle Scholar
  65. 65.
    Rovira J, Hernández-Aguilera A, Luciano-Mateo F, Cabré N, Baiges-Gaya G, Nadal M, Martín-Paredero V, Camps J, Joven J, Domingo JL (2018) Trace elements and paraoxonase-1 activity in lower extremity artery disease. Biol Trace Elem Res.  https://doi.org/10.1007/s12011-018-1298-x
  66. 66.
    Edwards M (2013) Fetal death and reduced birth rates associated with exposure to lead-contaminated drinking water. Environ Sci Technol 48:739–746PubMedGoogle Scholar
  67. 67.
    Bellinger DC (2016) Lead contamination in Flint—an abject failure to protect public health. N Engl J Med 374:1101–1103PubMedGoogle Scholar
  68. 68.
    DeWitt RD (2017) Pediatric lead exposure and the water crisis in Flint, Michigan. JAAPA 30:43–46PubMedGoogle Scholar
  69. 69.
    Sweeney E, Yu ZM, Parker L, Dummer TJ (2017) Lead in drinking water: a response from the Atlantic PATH study. Environ Health Rev 60:9–13Google Scholar
  70. 70.
    Goho SA (2016) The legal implications of report back in household exposure studies. Environ Health Perspect 124:1662–1670PubMedPubMedCentralGoogle Scholar
  71. 71.
    Peña MSB, Rollins A (2017) Environmental exposures and cardiovascular disease: a challenge for health and development in low- and middle-income countries. Cardiol Clin 35:71–86Google Scholar
  72. 72.
    Moore MR (1988) Haematological effects of lead. Sci Total Environ 71:419–431PubMedGoogle Scholar
  73. 73.
    Etchevers A, Le Tertre A, Lucas JP (2015) Environmental determinants of different blood lead levels in children: a quantile analysis from a nationwide survey. Environ Int 74:152–159PubMedGoogle Scholar
  74. 74.
    Deshommes E, Andrews RC, Gagnon G (2016) Evaluation of exposure to lead from drinking water in large buildings. Water Res 99:46–55PubMedGoogle Scholar
  75. 75.
    Pocock SJ (1980) Factors influencing household water lead: a British national survey. Arch Environ Health 35:45–51PubMedGoogle Scholar
  76. 76.
    Revitt DM, Eriksson E, Donner E (2011) The implications of household greywater treatment and reuse for municipal wastewater flows and micropollutant loads. Water Res 45:1549–1560PubMedGoogle Scholar
  77. 77.
    Delile H (2014) Lead paleo-pollutions, witnesses of the socio-economic conditions of ancient Rome. Med Sci (Paris) 30:831–833Google Scholar
  78. 78.
    Delile H, Blichert-Toft J, Goiran JP, Keay S, Albarède F (2014) Lead in ancient Rome’s city waters. Proc Natl Acad Sci U S A 111P:6594–6599Google Scholar
  79. 79.
    Pragst F, Stieglitz K, Runge H, Runow KD, Quig D, Osborne R, Runge C, Ariki J (2017) High concentrations of lead and barium in hair of the rural population caused by water pollution in the Thar Jath oilfields in South Sudan. Forensic Sci Int 274:99–106PubMedGoogle Scholar
  80. 80.
    Lu Y, Song S, Wang R, Liu Z, Meng J, Sweetman AJ, Jenkins A, Ferrier RC, Li H, Luo W, Wang T (2015) Impacts of soil and water pollution on food safety and health risks in China. Environ Int 77:5–15PubMedGoogle Scholar
  81. 81.
    Maret W (2017) The bioinorganic chemistry of lead in the context of its toxicity. Met Ions Life Sci 17:1Google Scholar
  82. 82.
    Bhowmik AK, Alamdar A, Katsoyiannis I, Shen H, Ali N, Ali SM, Bokhari H, Schäfer RB, Eqani SA (2015) Mapping human health risks from exposure to trace metal contamination of drinking water sources in Pakistan. Sci Total Environ 538:306–316PubMedGoogle Scholar
  83. 83.
    Rahmanian N, Hajar S, Ali B, Homayoonfard M, Ali NJ, Rehan M, Sadef Y, Nizami AS (2015) Analysis of physiochemical parameters to evaluate the drinking water quality in the state of Perak, Malaysia. J Chem 2015:1–10.  https://doi.org/10.1155/2015/716125 Google Scholar
  84. 84.
    Malcoe LH, Lynch RA, Keger MC (2002) Lead sources, behaviors, and socioeconomic factors in relation to blood lead of native American and white children: a community-based assessment of a former mining area. Environ Health Perspect 110:221–231PubMedPubMedCentralGoogle Scholar
  85. 85.
    United States Environmental Protection Agency. Learn about lead. Available online: https://www.epa.gov/lead/learn-about-lead#found (accessed on 4 October 2017)
  86. 86.
    Sherlock J, Smart G, Forbes GI, Moore MR, Patterson WJ, Richards WN, Wilson TS (1982) Assessment of lead intakes and dose-response for a population in Ayr exposed to a plumbosolvent water supply. Hum Toxicol 1:115–122PubMedGoogle Scholar
  87. 87.
    Park S, Lee BK (2012) Inverse relationship between fat intake and blood lead levels in the Korean adult population in the KNHANES 2007-2009. Sci Total Environ 15:161–166Google Scholar
  88. 88.
    Suarez-Ortegón MF, Mosquera M, Caicedo DM, Plata D, Aguilar C, Méndez F (2013) Nutrients intake as determinants of blood lead and cadmium levels in Colombian pregnant women. Am J Hum Biol 25:344–350PubMedGoogle Scholar
  89. 89.
    Triantafyllidou S, Le T, Gallagher D (2014) Edwards, M. Reduced risk estimations after remediation of lead (Pb) in drinking water at two US school districts. Sci Total Environ 466:1011–1021PubMedGoogle Scholar
  90. 90.
    Choulot JJ, Carbonnier H (2007) Adoption from Haiti and lead poisoning. Arch Pediatr 14:1372–1373PubMedGoogle Scholar
  91. 91.
    Fertmann R, Hentschel S, Dengler D (2004) Lead exposure by drinking water: an epidemiological study in Hamburg, Germany. Int J Hyg Environ Health 207:235–244PubMedGoogle Scholar
  92. 92.
    Edwards M, Triantafyllidou S, Best D (2009) Elevated blood lead in young children due to lead-contaminated drinking water: Washington, DC, 2001−2004. Environ Sci Technol 43:1618–1623PubMedGoogle Scholar
  93. 93.
    Hanna-Attisha M, LaChance J, Sadler RC (2016) Elevated blood lead levels in children associated with the Flint drinking water crisis: a spatial analysis of risk and public health response. Am J Public Health 106:283–290PubMedPubMedCentralGoogle Scholar
  94. 94.
    Levallois P, St-Laurent J, Gauvin D (2014) The impact of drinking water, indoor dust and paint on blood lead levels of children aged 1–5 years in Montréal (Québec, Canada). J Expo Sci Environ Epidemiol 24:185–191PubMedGoogle Scholar
  95. 95.
    Ngueta G, Abdous B, Tardif R, St-Laurent J, Levallois P (2016) Use of a cumulative exposure index to estimate the impact of tap water lead concentration on blood lead levels in 1-to 5-year-old children (Montreal, Canada). Environ Health Perspect 124:388PubMedGoogle Scholar
  96. 96.
    Momeni M, Gharedaghi Z, Amin MM, Poursafa P, Mansourian M (2014) Does water hardness have preventive effect on cardiovascular disease? Int J Prev Med 5:159PubMedPubMedCentralGoogle Scholar
  97. 97.
    Rylander R (2014) Magnesium in drinking water–a case for prevention? J Water Health 12:34–40PubMedGoogle Scholar
  98. 98.
    Pocock SJ, Shaper AG, Cook DG, Packham RF, Lacey RF, Powell P, Russell PF (1980) British Regional Heart Study: geographic variations in cardiovascular mortality, and the role of water quality. Br Med J 280:1243–1249PubMedPubMedCentralGoogle Scholar
  99. 99.
    Leurs LJ, Schouten LJ, Mons MN, Goldbohm RA, van den Brandt PA (2010) Relationship between tap water hardness, magnesium, and calcium concentration and mortality due to ischemic heart disease or stroke in The Netherlands. Environ. Health Perspect 118:414–420Google Scholar
  100. 100.
    Kanadhia KC, Ramavataram DV, Nilakhe SP, Patel S (2014) A study of water hardness and the prevalence of hypomagnesaemia and hypocalcaemia in healthy subjects of Surat district (Gujarat). Magnes Res 27:165–174PubMedGoogle Scholar
  101. 101.
    Chao S, Fan J, Wang L (2016) Association between the levels of calcium in drinking water and coronary heart disease mortality risk: evidence from a meta-analysis. Int J Clin Exp Med 9:17912–17918Google Scholar
  102. 102.
    Sheldon M, Marc E (2015) Increased lead in water associated with iron corrosion. Environ Engineer Sci 32:361–369Google Scholar
  103. 103.
    Triantafyllidou S, Schock MR, DeSantis MK, White C (2015) Low contribution of PbO2-coated lead service lines to water lead contamination at the tap. Environ Sci Technol 49:3746–3754PubMedGoogle Scholar
  104. 104.
    Jiang L, He P, Chen J (2016) Magnesium levels in drinking water and coronary heart disease mortality risk: a meta-analysis. Nutrients 8:5PubMedCentralGoogle Scholar
  105. 105.
    Fang X, Liang C, Li M, Montgomery S, Fall K, Aaseth J, Cao Y (2016) Dose-response relationship between dietary magnesium intake and cardiovascular mortality: a systematic review and dose-based meta-regression analysis of prospective studies. J Trace Elem Med Biol 38:64–73PubMedGoogle Scholar
  106. 106.
    Kordas K (2017) The “lead diet”: can dietary approaches prevent or treat lead exposure? J Pediatr 185:224–231PubMedGoogle Scholar
  107. 107.
    Ngueta G, Prévost M, Deshommes E (2014) Exposure of young children to household water lead in the Montreal area (Canada): the potential influence of winter-to-summer changes in water lead levels on children's blood lead concentration. Environ Int 73:57–65PubMedGoogle Scholar
  108. 108.
    Centers for Disease Control and Prevention. Adult Blood Lead Epidemiology and Surveillance (ABLES): program description: NIOSH workplace safety and health topic. Available online: https://www.cdc.gov/niosh/topics/ables/description.html (accessed on 4 October 2017)
  109. 109.
    Papanikolaou NC, Hatzidaki EG, Belivanis S (2005) Lead toxicity update. A brief review. Med Sci Monit Int Med J Exp Clin Res 11:RA329–RA336Google Scholar
  110. 110.
    Lustberg M, Silbergeld E (2002) Blood lead levels and mortality. Arch Intern Med 162:2443–2449PubMedGoogle Scholar
  111. 111.
    Weisskopf MG, Jain N, Nie H (2009) A prospective study of bone lead concentration and death from all causes, cardiovascular diseases, and cancer in the Department of Veterans Affairs Normative Aging Study. Circulation 120:1056–1064PubMedPubMedCentralGoogle Scholar
  112. 112.
    Cosselman KE, Navas-Acien A, Kaufman JD (2015) Environmental factors in cardiovascular disease. Nat Rev Cardiol 12:627–642PubMedGoogle Scholar
  113. 113.
    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 109:3196–3201PubMedGoogle Scholar
  114. 114.
    Harlan WR, Landis JR, Schmouder RL (1985) Blood lead and blood pressure: relationship in the adolescent and adult US population. JAMA 253:530–534PubMedGoogle Scholar
  115. 115.
    Nash D, Magder L, Lustberg M (2003) Blood lead, blood pressure, and hypertension in perimenopausal and postmenopausal women. JAMA 289:1523–1532PubMedGoogle Scholar
  116. 116.
    Revis NW, Zinsmeister AR, Bull R (1981) Atherosclerosis and hypertension induction by lead and cadmium ions: an effect prevented by calcium ion. Proc Natl Acad Sci U S A 78:6494–6498PubMedPubMedCentralGoogle Scholar
  117. 117.
    Voors AW, Shuman MS, Johnson WD (1982) Additive statistical effects of cadmium and lead on heart-related disease in a North Carolina autopsy series. Arch Environ Health 37:98–102PubMedGoogle Scholar
  118. 118.
    Wildemann TM, Mirhosseini N, Siciliano SD, Weber LP (2015) Cardiovascular responses to lead are biphasic, while methylmercury, but not inorganic mercury, monotonically increases blood pressure in rats. Toxicology 328:1–1PubMedGoogle Scholar
  119. 119.
    Pocock SJ, Shaper AG, Ashby D, Delves HT, Clayton BE (1988) The relationship between blood lead, blood pressure, stroke, and heart attacks in middle-aged British men. Environ Health Perspect 78:23–30PubMedPubMedCentralGoogle Scholar
  120. 120.
    Vaziri ND (2008) Mechanisms of lead-induced hypertension and cardiovascular disease. Am J Physiol Heart Circ Physiol 295:H454–H465PubMedPubMedCentralGoogle Scholar
  121. 121.
    Bandyopadhyay D, Ghosh D, Chattopadhyay A (2014) Lead induced oxidative stress mediated myocardial injury: a review. Int J Pharm Sci Rev Res 29:67–71Google Scholar
  122. 122.
    Ghosh D, Firdaus SB, Mitra E, Dey M, Chattopadhyay A, Pattari SK, Dutta S, Jana K, Bandyopadhyay D (2013) Aqueous leaf extract of Murraya koenigii protects against lead-induced cardiotoxicity in male Wistar rats. Int J Phytopharmacology 4:119–132Google Scholar
  123. 123.
    Payal B, Kaur H, Rai D (2009) New insight into the effects of lead modulation on antioxidant defense mechanism and trace element concentration in rat bone. Interdiscip Toxicol 2:18–23PubMedPubMedCentralGoogle Scholar
  124. 124.
    Ni Z, Hou S, Barton CH, Vaziri ND (2004) Lead exposure raises superoxide and hydrogen peroxide in human endothelial and vascular smooth muscle cells. Kidney Int 66:2329–2336PubMedGoogle Scholar
  125. 125.
    Sun Y, Zhang H, Xing X, Zhao Z, He J, Li J, Chen J, Wang M, He Y (2017) Lead promotes abnormal angiogenesis induced by CCM3 gene defects via mitochondrial pathway. J Dev Orig Health Dis 9:182–190PubMedGoogle Scholar
  126. 126.
    Feng L, Yang X, Asweto CO, Wu J, Zhang Y, Hu H, Shi Y, Duan J, Sun Z (2017) Low-dose combined exposure of nanoparticles and heavy metal compared with PM(2.5) in human myocardial AC16 cells. Environ Sci Pollut Res Int 24:27767–27777PubMedGoogle Scholar
  127. 127.
    Samek L, Furman L, Mikrut M, Regiel-Futyra A, Macyk W, Stochel G, van Eldik R (2017) Chemical composition of submicron and fine particulate matter collected in Krakow, Poland. Consequences for the APARIC project. Chemosphere 187:430–439PubMedGoogle Scholar
  128. 128.
    Fagerberg B, Kjelldahl J, Sallsten G, Barregard L, Forsgard N, Österberg K, Hultén LM, Bergström G (2016) Cadmium exposure as measured in blood in relation to macrophage density in symptomatic atherosclerotic plaques from human carotid artery. Atherosclerosis 249:209–214PubMedGoogle Scholar
  129. 129.
    Zota AR, Shenassa ED, Morello-Frosch R (2013) Allostatic load amplifies the effect of blood lead levels on elevated blood pressure among middle-aged U.S. adults: a cross-sectional study. Environ Health 12:64PubMedPubMedCentralGoogle Scholar
  130. 130.
    Guidotti TL, Ragain L (2007) Protecting children from toxic exposure: three strategies. Pediatr Clin N Am 54:227–235Google Scholar
  131. 131.
    Cornelis, Rita, Joseph A. Caruso, Helen Crews, and Klaus G. Heumann. Handbook of elemental speciation II: species in the environment, food, medicine and occupational health. John Wiley & Sons, 2005Google Scholar
  132. 132.
    Flora G, Gupta D, Tiwari A (2012) Toxicity of lead: a review with recent updates. Interdiscip Toxicol 5(2):47–58PubMedPubMedCentralGoogle Scholar
  133. 133.
    Wani AL, Ara A, Usmani JA (2015) Lead toxicity: a review. Interdiscip Toxicol 8(2):55–64PubMedPubMedCentralGoogle Scholar
  134. 134.
    Hayatbakhsh MM, Oghabian Z, Conlon E, Nakhaee S, Amirabadizadeh AR, Zahedi MJ, Darvish Moghadam S, Ahmadi B, Soroush S, Aaseth J, Mehrpour O (2017) Lead poisoning among opium users in Iran: an emerging health hazard. Subst Abuse Treat Prev Policy 12:43PubMedPubMedCentralGoogle Scholar
  135. 135.
    Rahimi N, Gozashti MH, Najafipour H, Shokoohi M, Marefati H (2014) Potential effect of opium consumption on controlling diabetes and some cardiovascular risk factors in diabetic patients. Addict Health 26:1–6Google Scholar
  136. 136.
    Mesirca P, Torrente AG, Mangoni ME (2015) Functional role of voltage gated Ca(2+) channels in heart automaticity. Front Physiol 6:19PubMedPubMedCentralGoogle Scholar
  137. 137.
    Yan D, Wang L, Ma FL, Deng H, Liu J, Li C, Wang H, Chen J, Tang JL, Ruan DY (2008) Developmental exposure to lead causes inherent changes on voltage-gated sodium channels in rat hippocampal CA1 neurons. Neuroscience 153:436–445PubMedGoogle Scholar
  138. 138.
    Marrero-Rosado B, Fox SM, Hannon HE, Atchison WD (2013) In: Kretsinger RE, Uversky VN, Permyakov EA (eds) Mercury and lead, effects on voltage-gated calcium channel function in encyclopedia of metalloproteins. Springer, New York.  https://doi.org/10.1007/978-1-4614-1533-6-308 Google Scholar
  139. 139.
    Gu Y, Wang L, Xiao C, Guo F, Ruan DY (2005) Effects of lead on voltage-gated sodium channels in rat hippocampal CA1 neurons. Neuroscience 133:679–690PubMedGoogle Scholar
  140. 140.
    Glynn P, Musa H, Wu X, Unudurthi SD, Little S, Qian L, Wright PJ, Radwanski PB, Gyorke S, Mohler PJ, Hund TJ (2015) Voltage-gated sodium channel phosphorylation at Ser571 regulates late current, arrhythmia, and cardiac function in vivo. Circulation 132:567–577PubMedPubMedCentralGoogle Scholar
  141. 141.
    Yu L, Eaton DC, Helms MN (2007) Effect of divalent heavy metals on epithelial Na+ channels in A6 cells. Am J Physiol Renal Physiol 293:F236–F244PubMedGoogle Scholar
  142. 142.
    Florea AM, Taban J, Varghese E, Alost BT, Moreno S, Büsselberg D (2013) Lead (Pb2+) neurotoxicity: ion mimicry with calcium (Ca2+) impairs synaptic transmission. A review with animated illustrations of the pre- and post-synaptic effects of lead. J Loc Global Health Sci 4:1–30Google Scholar
  143. 143.
    Niemann B, Rohrbach S, Miller MR, Newby DE, Fuster V, Kovacic JC (2017) Oxidative stress and cardiovascular risk: obesity, diabetes, smoking, and pollution: part 3 of a 3-part series. J Am Coll Cardiol 70:230–251PubMedGoogle Scholar
  144. 144.
    Rapisarda V, Ledda C, Ferrante M, Fiore M, Cocuzza S, Bracci M, Fenga C (2016) Blood pressure and occupational exposure to noise and lead (Pb): a cross-sectional study. Toxicol Ind Health 32:1729–1736PubMedGoogle Scholar
  145. 145.
    Aoki Y, Brody DJ, Flegal KM, Fakhouri TH, Axelrad DA, Parker JD (2016) Blood lead and other metal biomarkers as risk factors for cardiovascular disease mortality. Medicine (Baltimore) 95:e2223Google Scholar
  146. 146.
    Schober SE, Mirel LB, Graubard BI, Brody DJ, Flegal KM (2006) Blood lead levels and death from all causes, cardiovascular disease, and cancer: results from the NHANES III mortality study. Environ Health Perspect 114:1538–1541PubMedPubMedCentralGoogle Scholar
  147. 147.
    Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, Das SR, de Ferranti S, Després JP, Fullerton HJ, Howard VJ (2016) Heart disease and stroke statistics—2016 update: a report from the American Heart Association. Circulation 133:e38–e360PubMedGoogle Scholar
  148. 148.
    Hanna-Attisha M, LaChance J, Sadler RC, Champney Schnepp A (2015) Elevated blood lead levels in children associated with the Flint drinking water crisis: a spatial analysis of risk and public health response. Am J Public Health 106:283–290PubMedGoogle Scholar
  149. 149.
    Olson E, Pullen Fedinick K (2017) What’s in your water? Flint and beyond [Internet]. Natural Resources Defense Council; 2016. Available online: https://www.nrdc.org/resources/whats-your-water-flint-and-beyond
  150. 150.
    Pfadenhauer LM, Burns J, Rohwer A, Rehfuess EA (2016) Effectiveness of interventions to reduce exposure to lead through consumer products and drinking water: a systematic review. Environ Res 147:525–536PubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Council for Nutritional and Environmental MedicineMo i RanaNorway
  2. 2.Razi Vaccine and Serum Research Institute, Agricultural ResearchEducation and Extension Organization (AREEO)KarajIran
  3. 3.Department of Neurological and Movement SciencesUniversity of VeronaVeronaItaly
  4. 4.Faculty of Public HealthInland Norway University of Applied SciencesElverumNorway
  5. 5.Department of ResearchInnlandet Hospital TrustBrumunddalNorway

Personalised recommendations