Skip to main content

Advertisement

Log in

The endocrine disruptor cadmium: a new player in the pathophysiology of metabolic diseases

  • Review
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

Cadmium (Cd), a highly toxic heavy metal, is found in soil, environment and contaminated water and food. Moreover, Cd is used in various industrial activities, such as electroplating, batteries production, fertilizers, while an important non-occupational source is represented by cigarette smoking, as Cd deposits in tobacco leaves. Since many years it is clear a strong correlation between Cd body accumulation and incidence of many diseases. Indeed, acute exposure to Cd can cause inflammation and affect many organs such as kidneys and liver. Furthermore, the attention has focused on its activity as environmental pollutant and endocrine disruptor able to interfere with metabolic and energy balance of living beings. Both in vitro and in vivo experiments have demonstrated that the Cd-exposure is related to metabolic diseases such as obesity, diabetes and osteoporosis even if human studies are still controversial. Recent data show that Cd-exposure is associated with atherosclerosis, hypertension and endothelial damage that are responsible for cardiovascular diseases. Due to the large environmental diffusion of Cd, in this review, we summarize the current knowledge concerning the role of Cd in the incidence of metabolic and cardiovascular diseases.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Tarakina NV, Verberck B (2017) A portrait of cadmium. Nat Chem 9(1):96. https://doi.org/10.1038/nchem.2699

    Article  CAS  Google Scholar 

  2. Nordberg GF, Bernard A, Diamond GL, Duffus JH, Illing P, Nordberg M, Bergdahl IA, Jin T, Skerfving S (2018) Risk assessment of effects of cadmium on human health (IUPAC Technical Report). Pure Appl Chem 90(4):755–808. https://doi.org/10.1515/pac-2016-0910

    Article  CAS  Google Scholar 

  3. Zhang D, Zhang T, Liu J, Chen J, Li Y, Ning G, Huo N, Tian W, Ma H (2019) Zn supplement-antagonized cadmium-induced cytotoxicity in macrophages in vitro: involvement of cadmium bioaccumulation and metallothioneins regulation. J Agric Food Chem 67(16):4611–4622. https://doi.org/10.1021/acs.jafc.9b00232

    Article  CAS  PubMed  Google Scholar 

  4. Vainio H, Heseltine E, Partensky C, Wilbourn J (1993) Meeting of the IARC working group on beryllium, cadmium, mercury and exposures in the glass manufacturing industry. Scand J Work Environ Health. https://doi.org/10.5271/sjweh.1461

    Article  PubMed  Google Scholar 

  5. Chowdhury R (2019) Kontamination mit Schwermetallen erhöht kardiovaskuläres Risiko. Dtsch Med Wochenschr. https://doi.org/10.1136/bmj.k3310

    Article  Google Scholar 

  6. Fittipaldi S, Bimonte V, Soricelli A, Aversa A, Lenzi A, Greco E, Migliaccio S (2019) Cadmium exposure alters steroid receptors and proinflammatory cytokine levels in endothelial cells in vitro: a potential mechanism of endocrine disruptor atherogenic effect. J Endocrinol Invest 42(6):727–739. https://doi.org/10.1007/s40618-018-0982-1

    Article  CAS  PubMed  Google Scholar 

  7. Brama M, Gnessi L, Basciani S, Cerulli N, Politi L, Spera G, Mariani S, Cherubini S, d’Abusco AS, Scandurra R, Migliaccio S (2007) Cadmium induces mitogenic signaling in breast cancer cell by an ERα-dependent mechanism. Mol Cell Endocrinol 264(1–2):102–108. https://doi.org/10.1016/j.mce.2006.10.013

    Article  CAS  PubMed  Google Scholar 

  8. Thijssen S, Lambrichts I, Maringwa J, Van Kerkhove E (2007) Changes in expression of fibrotic markers and histopathological alterations in kidneys of mice chronically exposed to low and high Cd doses. Toxicology 238(2–3):200–210. https://doi.org/10.1016/j.tox.2007.06.087

    Article  CAS  PubMed  Google Scholar 

  9. Borné Y, Fagerberg B, Persson M, Östling G, Söderholm M, Hedblad B, Sallsten G, Barregard L, Engström G (2017) Cadmium, carotid atherosclerosis, and incidence of ischemic stroke. J Am Heart Assoc 6(12):e006415. https://doi.org/10.1161/JAHA.117.006415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. de Angelis C, Galdiero M, Pivonello C, Salzano C, Gianfrilli D, Piscitelli P, Lenzi A, Colao A, Pivonello R (2017) The environment and male reproduction: the effect of cadmium exposure on reproductive function and its implication in fertility. Reprod Toxicol 73:105–127. https://doi.org/10.1016/j.reprotox.2017.07.021

    Article  CAS  PubMed  Google Scholar 

  11. Tinkov AA, Filippini T, Ajsuvakova OP, Aaseth J, Gluhcheva YG, Ivanova JM, Bjørklund G, Skalnaya MG, Gatiatulina ER, Popova EV (2017) The role of cadmium in obesity and diabetes. Sci Total Environ 601:741–755. https://doi.org/10.1016/j.scitotenv.2017.05.224

    Article  CAS  PubMed  Google Scholar 

  12. Buha A, Jugdaohsingh R, Matovic V, Bulat Z, Antonijevic B, Kerns JG, Goodship A, Hart A, Powell JJ (2019) Bone mineral health is sensitively related to environmental cadmium exposure-experimental and human data. Environ Res 176:108539. https://doi.org/10.1016/j.envres.2019.108539

    Article  PubMed  Google Scholar 

  13. FAO/WHO (2013). https://apps.who.int/food-additives-contaminants-jecfa-database/chemical.aspx?chemID=1376

  14. Faroon O, Ashizawa A, Wright S, Tucker P, Jenkins K, Ingerman L (2012) Toxicological profile for Cadmium. Atlanta (GA): Agency for Toxic Substances and Disease Registry (US) Public Health Statement Disponible en: https://www.ncbi.nlm.nih.gov/books/NBK158840/

  15. Vacchi-Suzzi C, Kruse D, Harrington J, Levine K, Meliker JR (2016) Erratum to: is urinary cadmium a biomarker of long-term exposure in humans? A review. Curr Environ Health Rep 3(4):493–494. https://doi.org/10.1007/s40572-016-0107-y

    Article  CAS  PubMed  Google Scholar 

  16. Fels J, Scharner B, Zarbock R, Zavala Guevara IP, Lee W-K, Barbier OC, Thévenod F (2019) Cadmium complexed with β2-microglubulin, albumin and lipocalin-2 rather than metallothionein cause megalin: cubilin dependent toxicity of the renal proximal tubule. Int J Mol Sci 20(10):2379. https://doi.org/10.3390/ijms20102379

    Article  CAS  PubMed Central  Google Scholar 

  17. Li Y, Huang Y-s, He B, Liu R, Qu G, Yin Y, Shi J, Hu L, Jiang G (2020) Cadmium-binding proteins in human blood plasma. Ecotoxicol Environ Saf 188:109896

    Article  CAS  Google Scholar 

  18. Akerstrom M, Barregard L, Lundh T, Sallsten G (2014) Variability of urinary cadmium excretion in spot urine samples, first morning voids, and 24 h urine in a healthy non-smoking population: implications for study design. J Expo Sci Environ Epidemiol 24(2):171–179. https://doi.org/10.1038/jes.2013.58

    Article  CAS  PubMed  Google Scholar 

  19. Becker K, Kaus S, Krause C, Lepom P, Schulz C, Seiwert M, Seifert B (2002) German Environmental Survey 1998 (GerES III): environmental pollutants in blood of the German population. Int J Hyg Environ Health 205(4):297–308. https://doi.org/10.1078/1438-4639-00188

    Article  PubMed  Google Scholar 

  20. Ganguly K, Levänen B, Palmberg L, Åkesson A, Lindén A (2018) Cadmium in tobacco smokers: a neglected link to lung disease? Eur Respir Rev. https://doi.org/10.1183/16000617.0122-2017

    Article  PubMed  Google Scholar 

  21. Pickering AD, Sumpter JP (2003) Peer reviewed: comprehending endocrine disruptors in aquatic environments. ACS Pubs. https://doi.org/10.1021/es032570f

    Article  Google Scholar 

  22. Colborn T, Vom Saal FS, Soto AM (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101(5):378–384

    Article  CAS  Google Scholar 

  23. Rudel RA, Perovich LJ (2009) Endocrine disrupting chemicals in indoor and outdoor air. Atmos Environ 43(1):170–181. https://doi.org/10.1016/j.atmosenv.2008.09.025

    Article  CAS  PubMed Central  Google Scholar 

  24. Brander SM, Gabler MK, Fowler NL, Connon RE, Schlenk D (2016) Pyrethroid pesticides as endocrine disruptors: molecular mechanisms in vertebrates with a focus on fishes. Environ Sci Technol 50(17):8977–8992. https://doi.org/10.1021/acs.est.6b02253

    Article  CAS  PubMed  Google Scholar 

  25. Combarnous Y (2017) Endocrine disruptor compounds (EDCs) and agriculture: the case of pesticides. CR Biol 340(9–10):406–409. https://doi.org/10.1016/j.crvi.2017.07.009

    Article  Google Scholar 

  26. Rochefort H (2017) Endocrine disruptors (EDs) and hormone-dependent cancers: correlation or causal relationship? CR Biol 340(9–10):439–445. https://doi.org/10.1016/j.crvi.2017.07.007

    Article  Google Scholar 

  27. Beausoleil C, Emond C, Cravedi J-P, Antignac J-P, Applanat M, Appenzeller BR, Beaudouin R, Belzunces LP, Canivenc-Lavier M-C, Chevalier N (2018) Regulatory identification of BPA as an endocrine disruptor: context and methodology. Mol Cell Endocrinol 475:4–9. https://doi.org/10.1016/j.mce.2018.02.001

    Article  CAS  PubMed  Google Scholar 

  28. Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30(4):293–342. https://doi.org/10.1210/er.2009-0002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Schug TT, Janesick A, Blumberg B, Heindel JJ (2011) Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol 127(3–5):204–215

    Article  CAS  Google Scholar 

  30. Buha A, Matovic V, Antonijevic B, Bulat Z, Curcic M, Renieri EA, Tsatsakis AM, Schweitzer A, Wallace D (2018) Overview of cadmium thyroid disrupting effects and mechanisms. Int J Mol Sci 19(5):1501. https://doi.org/10.3390/ijms19051501

    Article  CAS  PubMed Central  Google Scholar 

  31. Nie X, Chen Y, Chen Y, Chen C, Han B, Li Q, Zhu C, Xia F, Zhai H, Wang N (2017) Lead and cadmium exposure, higher thyroid antibodies and thyroid dysfunction in Chinese women. Environ Pollut 230:320–328. https://doi.org/10.1016/j.envpol.2017.06.052

    Article  CAS  PubMed  Google Scholar 

  32. Yu Y, Ma R, Yu L, Cai Z, Li H, Zuo Y, Wang Z, Li H (2018) Combined effects of cadmium and tetrabromobisphenol a (TBBPA) on development, antioxidant enzymes activity and thyroid hormones in female rats. Chem Biol Interact 289:23–31. https://doi.org/10.1016/j.cbi.2018.04.024

    Article  CAS  PubMed  Google Scholar 

  33. Rezaei M, Javadmoosavi SY, Mansouri B, Azadi NA, Mehrpour O, Nakhaee S (2019) Thyroid dysfunction: how concentration of toxic and essential elements contribute to risk of hypothyroidism, hyperthyroidism, and thyroid cancer. Environ Sci Pollut Res 26(35):35787–35796. https://doi.org/10.1007/s11356-019-06632-7

    Article  CAS  Google Scholar 

  34. Chung SM, Moon JS, Yoon JS, Won KC, Lee HW (2019) Sex-specific effects of blood cadmium on thyroid hormones and thyroid function status: Korean nationwide cross-sectional study. J Trace Elem Med Biol 53:55–61. https://doi.org/10.1016/j.jtemb.2019.02.003

    Article  CAS  PubMed  Google Scholar 

  35. Byrne C, Divekar SD, Storchan GB, Parodi DA, Martin MB (2009) Cadmium—a metallohormone? Toxicol Appl Pharmacol 238(3):266–271. https://doi.org/10.1016/j.taap.2009.03.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Aquino NB, Sevigny MB, Sabangan J, Louie MC (2012) The role of cadmium and nickel in estrogen receptor signaling and breast cancer: metalloestrogens or not? J Environ Sci Health C 30(3):189–224. https://doi.org/10.1080/10590501.2012.705159

    Article  CAS  Google Scholar 

  37. Kresovich JK, Erdal S, Chen HY, Gann PH, Argos M, Rauscher GH (2019) Metallic air pollutants and breast cancer heterogeneity. Environ Res 177:108639. https://doi.org/10.1016/j.envres.2019.108639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Strumylaite L, Kregzdyte R, Bogusevicius A, Poskiene L, Baranauskiene D, Pranys D (2019) Cadmium exposure and risk of breast cancer by histological and tumor receptor subtype in white caucasian women: a hospital-based case-control study. Int J Mol Sci 20(12):3029. https://doi.org/10.3390/ijms20123029

    Article  CAS  PubMed Central  Google Scholar 

  39. Bloomfield M, Louie MC (2019) Chronic cadmium exposure decreases the dependency of MCF7 breast cancer cells on ERα. Sci Rep 9(1):1–11

    Article  CAS  Google Scholar 

  40. Wang Y, Shi L, Li J, Li L, Wang H, Yang H (2019) Long-term cadmium exposure promoted breast cancer cell migration and invasion by up-regulating TGIF. Ecotoxicol Environ Saf 175:110–117. https://doi.org/10.1016/j.ecoenv.2019.03.046

    Article  CAS  PubMed  Google Scholar 

  41. Waalkes MP, Rehm S (1994) Cadmium and prostate cancer. J Toxicol Environ Health Part A 43(3):251–269. https://doi.org/10.1080/15287399409531920

    Article  CAS  Google Scholar 

  42. Dai C, Heemers H, Sharifi N (2017) Androgen signaling in prostate cancer. Cold Spring Harb Perspect Med 7(9):a030452. https://doi.org/10.1101/cshperspect.a030452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Webber MM (1985) Selenium prevents the growth stimulatory effects of cadmium on human prostatic epithelium. Biochem Biophys Res Commun 127(3):871–877

    Article  CAS  Google Scholar 

  44. Voeller HJ, Wilding G, Gelmann EP (1991) V-ras H expression confers hormone-independent in vitro growth to LNCaP prostate carcinoma cells. Mol Endocrinol 5(2):209–216. https://doi.org/10.1210/mend-5-2-209

    Article  CAS  PubMed  Google Scholar 

  45. Martin MB, Voeller HJ, Gelmann EP, Lu J, Stoica E-G, Hebert EJ, Reiter R, Singh B, Danielsen M, Pentecost E (2002) Role of cadmium in the regulation of AR gene expression and activity. Endocrinology 143(1):263–275. https://doi.org/10.1210/endo.143.1.8581

    Article  CAS  PubMed  Google Scholar 

  46. Neslund-Dudas CM, McBride RB, Kandegedara A, Rybicki BA, Kryvenko ON, Chitale D, Gupta N, Williamson SR, Rogers CG, Cordon-Cardo C (2018) Association between cadmium and androgen receptor protein expression differs in prostate tumors of African American and European American men. J Trace Elem Med Biol 48:233–238. https://doi.org/10.1016/j.jtemb.2018.04.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Aimola P, Carmignani M, Volpe AR, Di Benedetto A, Claudio L, Waalkes MP, Van Bokhoven A, Tokar EJ, Claudio PP (2012) Cadmium induces p53-dependent apoptosis in human prostate epithelial cells. PLoS ONE 7(3):e33647. https://doi.org/10.1371/journal.pone.0033647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Chandrasekaran B, Dahiya NR, Tyagi A, Kolluru V, Saran U, Baby BV, States JC, Haddad AQ, Ankem MK, Damodaran C (2020) Chronic exposure to cadmium induces a malignant transformation of benign prostate epithelial cells. Oncogenesis 9(2):1–10. https://doi.org/10.1038/s41389-020-0202-7

    Article  CAS  Google Scholar 

  49. Santana VP, Salles ÉS, Correa DE, Gonçalves BF, Campos SG, Justulin LA, Godinho AF, Scarano WR (2016) Long-term effects of perinatal exposure to low doses of cadmium on the prostate of adult male rats. Int J Exp Pathol 97(4):310–316

    Article  CAS  Google Scholar 

  50. Visser A, Deklerk J (1978) The effect of dietary cadmium on prostate growth. Trans Am Assoc Genitourin Surg 70:66–68

    CAS  PubMed  Google Scholar 

  51. Lubrano C, Genovesi G, Specchia P, Costantini D, Mariani S, Petrangeli E, Lenzi A, Gnessi L (2013) Obesity and metabolic comorbidities: environmental diseases? Oxi Med Cell Longev. https://doi.org/10.1155/2013/640673

    Article  Google Scholar 

  52. Park SS, Skaar DA, Jirtle RL, Hoyo C (2017) Epigenetics, obesity and early-life cadmium or lead exposure. Epigenomics 9(1):57–75. https://doi.org/10.2217/epi-2016-0047

    Article  CAS  PubMed  Google Scholar 

  53. Baillie-Hamilton PF (2002) Chemical toxins: a hypothesis to explain the global obesity epidemic. J Altern Complement Med 8(2):185–192. https://doi.org/10.1089/107555302317371479

    Article  PubMed  Google Scholar 

  54. Papa V, Wannenes F, Crescioli C, Caporossi D, Lenzi A, Migliaccio S, Di Luigi L (2014) The environmental pollutant cadmium induces homeostasis alteration in muscle cells in vitro. J Endocrinol Invest 37(11):1073–1080

    Article  CAS  Google Scholar 

  55. Darbre PD (2017) Endocrine disruptors and obesity. Current Obes Rep 6(1):18–27. https://doi.org/10.1007/s13679-017-0240-4

    Article  Google Scholar 

  56. González-Casanova JE, Pertuz-Cruz SL, Caicedo-Ortega NH, Rojas-Gomez DM (2020) Adipogenesis regulation and endocrine disruptors: emerging insights in obesity. Biomed Res Int. https://doi.org/10.1155/2020/7453786

    Article  PubMed  PubMed Central  Google Scholar 

  57. Kassotis CD, Nagel SC, Stapleton HM (2018) Unconventional oil and gas chemicals and wastewater-impacted water samples promote adipogenesis via PPARγ-dependent and independent mechanisms in 3T3-L1 cells. Sci Total Environ 640:1601–1610. https://doi.org/10.1016/j.scitotenv.2018.05.030

    Article  CAS  PubMed  Google Scholar 

  58. Doke M, Avecilla V, Felty Q (2018) Inhibitor of differentiation-3 and estrogenic endocrine disruptors: implications for susceptibility to obesity and metabolic disorders. BioMed Res Int. https://doi.org/10.1155/2018/6821601

    Article  PubMed  PubMed Central  Google Scholar 

  59. Verbanck M, Canouil M, Leloire A, Dhennin V, Coumoul X, Yengo L, Froguel P, Poulain-Godefroy O (2017) Low-dose exposure to bisphenols A, F and S of human primary adipocyte impacts coding and non-coding RNA profiles. PLoS ONE 12(6):e0179583. https://doi.org/10.1371/journal.pone.0179583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Avecilla V, Doke M, Felty Q (2017) Contribution of inhibitor of dna binding/differentiation-3 and endocrine disrupting chemicals to pathophysiological aspects of chronic disease. Biomed Res Int. https://doi.org/10.1155/2017/6307109

    Article  PubMed  PubMed Central  Google Scholar 

  61. Kim JT, Lee HK (2017) Childhood obesity and endocrine disrupting chemicals. Ann Pediatr Endocrinol Metab 22(4):219. https://doi.org/10.6065/apem.2017.22.4.219

    Article  PubMed  PubMed Central  Google Scholar 

  62. Shoucri BM, Martinez ES, Abreo TJ, Hung VT, Moosova Z, Shioda T, Blumberg B (2017) Retinoid X receptor activation alters the chromatin landscape to commit mesenchymal stem cells to the adipose lineage. Endocrinology 158(10):3109–3125. https://doi.org/10.1210/en.2017-00348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lejonklou MH, Dunder L, Bladin E, Pettersson V, Rönn M, Lind L, Waldén TB, Lind PM (2017) Effects of low-dose developmental bisphenol A exposure on metabolic parameters and gene expression in male and female Fischer 344 rat offspring. Environ Health Perspect 125(6):067018. https://doi.org/10.1289/EHP505

    Article  PubMed  PubMed Central  Google Scholar 

  64. Green AJ, Hoyo C, Mattingly CJ, Luo Y, Tzeng J-Y, Murphy SK, Buchwalter DB, Planchart A (2018) Cadmium exposure increases the risk of juvenile obesity: a human and zebrafish comparative study. Int J Obes 42(7):1285–1295. https://doi.org/10.1038/s41366-018-0036-y

    Article  CAS  Google Scholar 

  65. Haswell-Elkins M, Mcgrath V, Moore M, Satarug S, Walmby M, Ng J (2007) Exploring potential dietary contributions including traditional seafood and other determinants of urinary cadmium levels among indigenous women of a Torres Strait Island (Australia). J Eposure Sci Environ Epidemiol 17(3):298–306. https://doi.org/10.1038/sj.jes.7500547

    Article  CAS  Google Scholar 

  66. Padilla MA, Elobeid M, Ruden DM, Allison DB (2010) An examination of the association of selected toxic metals with total and central obesity indices: NHANES 99–02. Int J Environ Res Public Health 7(9):3332–3347. https://doi.org/10.3390/ijerph7093332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Akinloye O, Ogunleye K, Oguntibeju OO (2010) Cadmium, lead, arsenic and selenium levels in patients with type 2 diabetes mellitus. Afr J Biotech 9(32):5189–5195

    CAS  Google Scholar 

  68. Nie X, Wang N, Chen Y, Chen C, Han B, Zhu C, Chen Y, Xia F, Cang Z, Lu M (2016) Blood cadmium in Chinese adults and its relationships with diabetes and obesity. Environ Sci Pollut Res 23(18):18714–18723. https://doi.org/10.1007/s11356-016-7078-2

    Article  CAS  Google Scholar 

  69. Skalnaya MG, Tinkov AA, Demidov VA, Serebryansky EP, Nikonorov AA, Skalny AV (2014) Hair toxic element content in adult men and women in relation to body mass index. Biol Trace Elem Res 161(1):13–19. https://doi.org/10.1007/s12011-014-0082-9

    Article  CAS  PubMed  Google Scholar 

  70. El-Soud N, El-Laithy N, El-Saeed G, Wahby M, Khalil M, Morsy F, Shaffie N (2011) Antidiabetic activities of Foeniculum vulgare Mill. essential oil in streptozotocin-induced diabetic rats. Maced J Med Sci 4(2):139–146. https://doi.org/10.3889/MJMS.1857-5773.2011.0184

    Article  Google Scholar 

  71. Shao W, Liu Q, He X, Liu H, Gu A, Jiang Z (2017) Association between level of urinary trace heavy metals and obesity among children aged 6–19 years: NHANES 1999–2011. Environ Sci Pollut Res 24(12):11573–11581. https://doi.org/10.1007/s11356-017-8803-1

    Article  CAS  Google Scholar 

  72. Jiang F, Zhi X, Xu M, Li B, Zhang Z (2018) Gender-specific differences of interaction between cadmium exposure and obesity on prediabetes in the NHANES 2007–2012 population. Endocrine 61(2):258–266. https://doi.org/10.1007/s12020-018-1623-3

    Article  CAS  PubMed  Google Scholar 

  73. Noor N, Zong G, Seely EW, Weisskopf M, James-Todd T (2018) Urinary cadmium concentrations and metabolic syndrome in US adults: The National Health and Nutrition Examination Survey 2001–2014. Environ Int 121:349–356. https://doi.org/10.1016/j.envint.2018.08.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Huzior-Bałajewicz A, Pietrzyk J, Schlegel-Zawadzka M, Piatkowska E, Zachwieja Z (2001) The influence of lead and cadmium environmental pollution on anthropometric health factors in children. Przegl Lek 58(4):315

    PubMed  Google Scholar 

  75. Qin YY, Leung CKM, Leung AOW, Wu SC, Zheng JS, Wong MH (2010) Persistent organic pollutants and heavy metals in adipose tissues of patients with uterine leiomyomas and the association of these pollutants with seafood diet, BMI, and age. Environ Sci Pollut Res 17(1):229–240

    Article  CAS  Google Scholar 

  76. Adnan JA, Azhar SS, Hasni JM, Ahmad JS (2012) Urinary cadmium concentration and its risk factors among adults in Tanjung Karang, Selangor. Am-Eur J Toxicol Sci 4(2):80–88. https://doi.org/10.5829/idosi.aejts.2012.4.2.6331

    Article  CAS  Google Scholar 

  77. Kelishadi R, Askarieh A, Motlagh ME, Tajadini M, Heshmat R, Ardalan G, Fallahi S, Poursafa P (2013) Association of blood cadmium level with cardiometabolic risk factors and liver enzymes in a nationally representative sample of adolescents: the CASPIAN-III study. J Environ Public Health. https://doi.org/10.1155/2013/142856

    Article  PubMed  PubMed Central  Google Scholar 

  78. Park S, Lee B-K (2013) Body fat percentage and hemoglobin levels are related to blood lead, cadmium, and mercury concentrations in a Korean Adult Population (KNHANES 2008–2010). Biol Trace Elem Res 151(3):315–323. https://doi.org/10.1007/s12011-012-9566-7

    Article  CAS  PubMed  Google Scholar 

  79. Gonzalez-Reimers E, Martín-González C, Galindo-Martín L, Aleman-Valls M, Velasco-Vázquez J, Arnay-De-La-Rosa M, Pérez-Hernández O, Luis RH (2014) Lead, cadmium and zinc in hair samples: relationship with dietary habits and urban environment. Biol Trace Elem Res 157(3):205–210

    Article  CAS  Google Scholar 

  80. Ahn B, Kim S-H, Park M-J (2017) Blood cadmium concentrations in Korean adolescents: from the Korea National Health and Nutrition Examination Survey 2010–2013. Int J Hyg Environ Health 220(1):37–42. https://doi.org/10.1016/j.ijheh.2016.10.003

    Article  CAS  PubMed  Google Scholar 

  81. Rotter I, Kosik-Bogacka D, Dołęgowska B, Safranow K, Lubkowska A, Laszczyńska M (2015) Relationship between the concentrations of heavy metals and bioelements in aging men with metabolic syndrome. Int J Environ Res Public Health 12(4):3944–3961. https://doi.org/10.3390/ijerph120403944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Ficková M, Eybl V, Kotyzová D, Mičková V, Möstbök S, Brtko J (2003) Long lasting cadmium intake is associated with reduction of insulin receptors in rat adipocytes. Biometals 16(4):561–566. https://doi.org/10.1023/A:1023485130767

    Article  PubMed  Google Scholar 

  83. Huang Y, Zhang W, Li H (2003) Effect of cadmium on body weight and organ coefficient of ovaries in female rats. Occup Health 19:7–9

    Google Scholar 

  84. Singh PK, Baxi D, Diwedi R, Ramachandran A (2012) Prior cadmium exposure improves glucoregulation in diabetic rats but exacerbates effects on metabolic dysregulation, oxidative stress, and hepatic and renal toxicity. Drug Chem Toxicol 35(2):167–177. https://doi.org/10.3109/01480545.2011.589450

    Article  CAS  PubMed  Google Scholar 

  85. Treviño S, Waalkes MP, Hernández JAF, León-Chavez BA, Aguilar-Alonso P, Brambila E (2015) Chronic cadmium exposure in rats produces pancreatic impairment and insulin resistance in multiple peripheral tissues. Arch Biochem Biophys 583:27–35. https://doi.org/10.1016/j.abb.2015.07.010

    Article  CAS  PubMed  Google Scholar 

  86. Kawakami T, Nishiyama K, Kadota Y, Sato M, Inoue M, Suzuki S (2013) Cadmium modulates adipocyte functions in metallothionein-null mice. Toxicol Appl Pharmacol 272(3):625–636. https://doi.org/10.1016/j.taap.2013.07.015

    Article  CAS  PubMed  Google Scholar 

  87. Zhang S, Jin Y, Zeng Z, Liu Z, Fu Z (2015) Subchronic exposure of mice to cadmium perturbs their hepatic energy metabolism and gut microbiome. Chem Res Toxicol 28(10):2000–2009. https://doi.org/10.1021/acs.chemrestox.5b00237

    Article  CAS  PubMed  Google Scholar 

  88. Yamamoto A, Wada O, Ono T, Ono H (1986) Cadmium stimulates glucose metabolism in rat adipocytes. J Inorg Biochem 27(3):221–226. https://doi.org/10.1016/0162-0134(86)80063-0

    Article  CAS  PubMed  Google Scholar 

  89. Kang D, Khil L-Y, Lee B-H, Moon C-K (2005) Effects of cadmium on glucose transport in 3T3-L1 adipocytes. Environ Health Toxicol 20(1):87–95

    Google Scholar 

  90. Harrison SA, Buxton JM, Clancy BM, Czech MP (1991) Evidence that erythroid-type glucose transporter intrinsic activity is modulated by cadmium treatment of mouse 3T3-L1 cells. J Biol Chem 266(29):19438–19449

    Article  CAS  Google Scholar 

  91. Lachaal M, Liu H, Kim S-s, Jung CY (1996) Effects of cadmium on glucose transport in rat adipocytes and human erythrocytes: stimulation of GLUT1 catalytic activity. Exp Mol Med 28(1):33–40. https://doi.org/10.1038/emm.1996.6

    Article  CAS  Google Scholar 

  92. Lachaal M, Liu H, Kim S-s, Spangler RA, Jung CY (1996) Cadmium increases GLUT1 substrate binding affinity in vitro while reducing its cytochalasin B binding affinity. Biochemistry 35(47):14958–14962. https://doi.org/10.1021/bi9617320

    Article  CAS  PubMed  Google Scholar 

  93. Han JC, Park SY, Hah BG, Choi GH, Kim YK, Kwon TH, Kim EK, Lachaal M, Jung CY, Lee W (2003) Cadmium induces impaired glucose tolerance in rat by down-regulating GLUT4 expression in adipocytes. Arch Biochem Biophys 413(2):213–220

    Article  CAS  Google Scholar 

  94. Moon J, Yoo B (2008) Protective effects of propolis on cadmium-induced cell death of 3T3-L1 adipocytes. Korean J Apic 23(4):289–294

    Google Scholar 

  95. Kawakami T, Sugimoto H, Furuichi R, Kadota Y, Inoue M, Setsu K, Suzuki S, Sato M (2010) Cadmium reduces adipocyte size and expression levels of adiponectin and Peg1/Mest in adipose tissue. Toxicology 267(1–3):20–26. https://doi.org/10.1016/j.tox.2009.07.022

    Article  CAS  PubMed  Google Scholar 

  96. Lee EJ, Moon JY, Yoo BS (2012) Cadmium inhibits the differentiation of 3T3-L1 preadipocyte through the C/EBPα and PPARγ pathways. Drug Chem Toxicol 35(2):225–231. https://doi.org/10.3109/01480545.2011.591401

    Article  CAS  PubMed  Google Scholar 

  97. Levy J, Gyarmati J, Lesko J, Adler R, Stevens W (2000) Dual regulation of leptin secretion: intracellular energy and calcium dependence of regulated pathway. Am J Physiol Endocrinol Metab 278:E892–E901. https://doi.org/10.1152/ajpendo.2000.278.5.E892

    Article  CAS  PubMed  Google Scholar 

  98. Planchart A, Green A, Hoyo C, Mattingly CJ (2018) Heavy metal exposure and metabolic syndrome: evidence from human and model system studies. Curr Environ Health Rep 5(1):110–124. https://doi.org/10.1007/s40572-018-0182-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Cho N, Shaw J, Karuranga S, Huang Y, da Rocha FJ, Ohlrogge A, Malanda B (2018) IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281

    Article  CAS  Google Scholar 

  100. Eze IC, Schaffner E, Foraster M, Imboden M, von Eckardstein A, Gerbase MW, Rothe T, Rochat T, Künzli N, Schindler C (2015) Long-term exposure to ambient air pollution and metabolic syndrome in adults. PLoS ONE 10(6):e0130337. https://doi.org/10.1371/journal.pone.0130337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Basner M, Riggs DW, Conklin DJ (2020) Environmental determinants of hypertension and diabetes mellitus: sounding off about the effects of noise. Am Heart Assoc. https://doi.org/10.1161/JAHA.120.016048

    Article  Google Scholar 

  102. Yang M, Cheng H, Shen C, Liu J, Zhang H, Cao J, Ding R (2020) Effects of long-term exposure to air pollution on the incidence of type 2 diabetes mellitus: a meta-analysis of cohort studies. Environ Sci Pollut Res 27(1):798–811. https://doi.org/10.1007/s11356-019-06824-1

    Article  CAS  Google Scholar 

  103. Lei L-J, Chen L, Jin T-Y, Nordberg M, Chang X-L (2007) Estimation of benchmark dose for pancreatic damage in cadmium-exposed smelters. Toxicol Sci 97(1):189–195. https://doi.org/10.1093/toxsci/kfm016

    Article  CAS  PubMed  Google Scholar 

  104. Lei L, Guo J, Shi X, Kang H, Wang T, Zhang Z, Gao Y (2019) Relationship between urinary cadmium and type 2 diabetes mellitus in adults. Zhonghua Liu Xing Bing Xue Za Zhi 40(2):207–211

    CAS  PubMed  Google Scholar 

  105. Guo F-F, Hu Z-Y, Li B-Y, Qin L-Q, Fu C, Yu H, Zhang Z-L (2019) Evaluation of the association between urinary cadmium levels below threshold limits and the risk of diabetes mellitus: a dose-response meta-analysis. Environ Sci Pollut Res 26(19):19272–19281

    Article  CAS  Google Scholar 

  106. Trouiller-Gerfaux P, Podglajen E, Hulo S, Richeval C, Allorge D, Garat A, Matran R, Amouyel P, Meirhaeghe A, Dauchet L (2019) The association between blood cadmium and glycated haemoglobin among never-, former, and current smokers: a cross-sectional study in France. Environ Res 178:108673. https://doi.org/10.1016/j.envres.2019.108673

    Article  CAS  PubMed  Google Scholar 

  107. Xiao L, Zhou Y, Ma J, Cao L, Zhu C, Li W, Wang D, Fan L, Ye Z, Chen W (2019) Roles of C-reactive protein on the association between urinary cadmium and type 2 diabetes. Environ Pollut 255:113341. https://doi.org/10.1016/j.envpol.2019.113341

    Article  CAS  PubMed  Google Scholar 

  108. Bell R, Early J, Nonavinakere V, Mallory Z (1990) Effect of cadmium on blood glucose level in the rat. Toxicol Lett 54(2–3):199–205. https://doi.org/10.1016/0378-4274(90)90184-N

    Article  CAS  PubMed  Google Scholar 

  109. Merali Z, Singhal R (1980) Diabetogenic effects of chronic oral cadmium administration to neonatal rats. Br J Pharmacol 69(1):151–157. https://doi.org/10.1111/j.1476-5381.1980.tb10895.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Chapatwala K, Rajanna E, Desaiah D (1980) Cadmium induced changes in gluconeogenic enzymes in rat kidney and liver. Drug Chem Toxicol 3(4):407–420. https://doi.org/10.3109/01480548009030129

    Article  CAS  PubMed  Google Scholar 

  111. Lei L-J, Jin T-Y, Zhou Y-F (2007) Insulin expression in rats exposed to cadmium. Biomed Environ Sci 20(4):295–301

    CAS  PubMed  Google Scholar 

  112. Lei L-J, Jin T-Y, Zhou Y-F (2005) Effects of cadmium on levels of insulin in rats. Wei Sheng Yan Jiu 34(4):394–396

    CAS  PubMed  Google Scholar 

  113. Lei L, Jin T, Zhou Y (2005) The toxic effects of cadmium on pancreas. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 23(1):45–49

    CAS  PubMed  Google Scholar 

  114. Edwards JR, Prozialeck WC (2009) Cadmium, diabetes and chronic kidney disease. Toxicol Appl Pharmacol 238(3):289–293. https://doi.org/10.1016/j.taap.2009.03.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Jacquet A, Arnaud J, Hininger-Favier I, Hazane-Puch F, Couturier K, Lénon M, Lamarche F, Ounnas F, Fontaine E, Moulis J-M (2018) Impact of chronic and low cadmium exposure of rats: sex specific disruption of glucose metabolism. Chemosphere 207:764–773. https://doi.org/10.1016/j.chemosphere.2018.05.099

    Article  CAS  PubMed  Google Scholar 

  116. Yau ET, Mennear JH (1977) Pancreatic metallothionein: protection against cadmium-induced inhibition of insulin secretory activity. Toxicol Appl Pharmacol 39(3):515–520

    Article  CAS  Google Scholar 

  117. El Muayed M, Raja MR, Zhang X, MacRenaris KW, Bhatt S, Chen X, Urbanek M, O’Halloran TV, Lowe J, William L (2012) Accumulation of cadmium in insulin-producing β cells. Islets 4(6):405–416. https://doi.org/10.4161/isl.23101

    Article  PubMed  PubMed Central  Google Scholar 

  118. Chang K-C, Hsu C-C, Liu S-H, Su C-C, Yen C-C, Lee M-J, Chen K-L, Ho T-J, Hung D-Z, Wu C-C (2013) Cadmium induces apoptosis in pancreatic β-cells through a mitochondria-dependent pathway: the role of oxidative stress-mediated c-Jun N-terminal kinase activation. PLoS ONE 8(2):e54374. https://doi.org/10.1371/journal.pone.0054374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Mohammadi P, Rahimifard M, Baeeri M, Abdollahi M, Mostafalou S (2019) Mechanistic assessment of cadmium toxicity in association with the functions of estrogen receptors in the Langerhans islets. Iranian J Basic Med Sci 22(4):445. https://doi.org/10.22038/ijbms.2019.33939.8076

    Article  Google Scholar 

  120. Kanis JA, Melton LJ III, Christiansen C, Johnston CC, Khaltaev N (1994) The diagnosis of osteoporosis. J Bone Miner Res 9(8):1137–1141

    Article  CAS  Google Scholar 

  121. Wallin M, Barregard L, Sallsten G, Lundh T, Karlsson MK, Lorentzon M, Ohlsson C, Mellström D (2016) Low-level cadmium exposure is associated with decreased bone mineral density and increased risk of incident fractures in elderly men: the MrOS Sweden Study. J Bone Miner Res 31(4):732–741. https://doi.org/10.1002/jbmr.2743

    Article  CAS  PubMed  Google Scholar 

  122. Scimeca M, Feola M, Romano L, Rao C, Gasbarra E, Bonanno E, Brandi ML, Tarantino U (2017) Heavy metals accumulation affects bone microarchitecture in osteoporotic patients. Environ Toxicol 32(4):1333–1342. https://doi.org/10.1002/tox.22327

    Article  CAS  PubMed  Google Scholar 

  123. Johri N, Jacquillet G, Unwin R (2010) Heavy metal poisoning: the effects of cadmium on the kidney. Biometals 23(5):783–792

    Article  CAS  Google Scholar 

  124. Chen X, Zhu G, Jin T, Lei L, Liang Y (2011) Bone mineral density is related with previous renal dysfunction caused by cadmium exposure. Environ Toxicol Pharmacol 32(1):46–53. https://doi.org/10.1016/j.etap.2011.03.007

    Article  CAS  PubMed  Google Scholar 

  125. Rodríguez J, Mandalunis PM (2018) A review of metal exposure and its effects on bone health. J Toxicol. https://doi.org/10.1155/2018/4854152

    Article  PubMed  PubMed Central  Google Scholar 

  126. Ibrahim KS, Beshir S, Shahy EM, Shaheen W (2016) Effect of occupational cadmium exposure on parathyroid gland. Open Access Maced J Med Sci 4(2):302. https://doi.org/10.3889/oamjms.2016.042

    Article  PubMed  PubMed Central  Google Scholar 

  127. Nishijo M, Nambunmee K, Suvagandha D, Swaddiwudhipong W, Ruangyuttikarn W, Nishino Y (2017) Gender-specific impact of cadmium exposure on bone metabolism in older people living in a cadmium-polluted area in Thailand. Int J Environ Res Public Health 14(4):401. https://doi.org/10.3390/ijerph14040401

    Article  CAS  PubMed Central  Google Scholar 

  128. Wallin M, Sallsten G, Fabricius-Lagging E, Öhrn C, Lundh T, Barregard L (2013) Kidney cadmium levels and associations with urinary calcium and bone mineral density: a cross-sectional study in Sweden. Environ Health 12(1):22. https://doi.org/10.1186/1476-069X-12-22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Kazantzis G (2004) Cadmium, osteoporosis and calcium metabolism. Biometals 17(5):493–498. https://doi.org/10.1023/b:biom.0000045727.76054.f3

    Article  CAS  PubMed  Google Scholar 

  130. Åkesson A, Bjellerup P, Lundh T, Lidfeldt J, Nerbrand C, Samsioe G, Skerfving S, Vahter M (2006) Cadmium-induced effects on bone in a population-based study of women. Environ Health Perspect 114(6):830–834. https://doi.org/10.1289/ehp.8763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Chen X, Wang Z, Zhu G, Nordberg GF, Jin T, Ding X (2019) The association between cumulative cadmium intake and osteoporosis and risk of fracture in a Chinese population. J Eposure Sci Environ Epidemiol 29(3):435–443. https://doi.org/10.1038/s41370-018-0057-6

    Article  CAS  Google Scholar 

  132. Malin Igra A, Vahter M, Raqib R, Kippler M (2019) Early-life cadmium exposure and bone-related biomarkers: a longitudinal study in children. Environ Health Perspect 127(3):037003. https://doi.org/10.1289/EHP3655

    Article  PubMed Central  Google Scholar 

  133. Li X, Li R, Yan J, Song Y, Huo J, Lan Z, Chen J, Zhang L (2020) Co-exposure of cadmium and lead on bone health in a southwestern Chinese population aged 40–75 years. J Appl Toxicol 40(3):352–362. https://doi.org/10.1002/jat.3908

    Article  CAS  PubMed  Google Scholar 

  134. Brzóska MM, Moniuszko-Jakoniuk J (2004) Low-level exposure to cadmium during the lifetime increases the risk of osteoporosis and fractures of the lumbar spine in the elderly: studies on a rat model of human environmental exposure. Toxicol Sci 82(2):468–477

    Article  Google Scholar 

  135. Brzóska MM, Moniuszko-Jakoniuk J (2005) Disorders in bone metabolism of female rats chronically exposed to cadmium. Toxicol Appl Pharmacol 202(1):68–83

    Article  Google Scholar 

  136. Youness ER, Mohammed NA, Morsy FA (2012) Cadmium impact and osteoporosis: mechanism of action. Toxicol Mech Methods 22(7):560–567. https://doi.org/10.3109/15376516.2012.702796

    Article  CAS  PubMed  Google Scholar 

  137. Rodríguez J, Mandalunis PM (2016) Effect of cadmium on bone tissue in growing animals. Exp Toxicol Pathol 68(7):391–397. https://doi.org/10.1016/j.etp.2016.06.001

    Article  CAS  PubMed  Google Scholar 

  138. Lv Y-J, Wei Q-Z, Zhang Y-C, Huang R, Li B-S, Tan J-B, Wang J, Ling H-T, Wu S-X, Yang X-F (2019) Low-dose cadmium exposure acts on rat mesenchymal stem cells via RANKL/OPG and downregulate osteogenic differentiation genes. Environ Pollut 249:620–628. https://doi.org/10.1016/j.envpol.2019.03.027

    Article  CAS  PubMed  Google Scholar 

  139. He S, Zhuo L, Cao Y, Liu G, Zhao H, Song R, Liu Z (2020) Effect of cadmium on osteoclast differentiation during bone injury in female mice. Environ Toxicol 35(4):487–494. https://doi.org/10.1002/tox.22884

    Article  CAS  PubMed  Google Scholar 

  140. Chen X, Zhu G, Gu S, Jin T, Shao C (2009) Effects of cadmium on osteoblasts and osteoclasts in vitro. Environ Toxicol Pharmacol 28(2):232–236. https://doi.org/10.1016/j.etap.2009.04.010

    Article  CAS  PubMed  Google Scholar 

  141. Chen X, Zhu G, Jin T, Zhou Z, Gu S, Qiu J, Xiao H (2012) Cadmium stimulates the osteoclastic differentiation of RAW264. 7 cells in presence of osteoblasts. Biol Trace Elem Res 146(3):349–353. https://doi.org/10.1007/s12011-011-9256-x

    Article  CAS  PubMed  Google Scholar 

  142. Papa V, Bimonte V, Wannenes F, D’Abusco A, Fittipaldi S, Scandurra R, Politi L, Crescioli C, Lenzi A, Di Luigi L (2015) The endocrine disruptor cadmium alters human osteoblast-like Saos-2 cells homeostasis in vitro by alteration of Wnt/β-catenin pathway and activation of caspases. J Endocrinol Invest 38(12):1345–1356. https://doi.org/10.1007/s40618-015-0380-x

    Article  CAS  PubMed  Google Scholar 

  143. Hu K-H, Li W-X, Sun M-Y, Zhang S-B, Fan C-X, Wu Q, Zhu W, Xu X (2015) Cadmium induced apoptosis in MG63 cells by increasing ROS, activation of p38 MAPK and inhibition of ERK 1/2 pathways. Cell Physiol Biochem 36(2):642–654

    Article  CAS  Google Scholar 

  144. Al-Ghafari A, Elmorsy E, Fikry E, Alrowaili M, Carter WG (2019) The heavy metals lead and cadmium are cytotoxic to human bone osteoblasts via induction of redox stress. PLoS ONE 14(11):e0225341. https://doi.org/10.1371/journal.pone.0225341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Wu L, Wei Q, Lv Y, Xue J, Zhang B, Sun Q, Xiao T, Huang R, Wang P, Dai X (2019) Wnt/β-Catenin pathway is involved in cadmium-induced inhibition of osteoblast differentiation of bone marrow mesenchymal stem cells. Int J Mol Sci 20(6):1519. https://doi.org/10.3390/ijms20061519

    Article  CAS  PubMed Central  Google Scholar 

  146. WHO (2017). https://www.who.int/en/news-room/fact-sheets/detail/cardiovascular-diseases-(cvds)

  147. Pope CA III, Burnett RT, Thurston GD, Thun MJ, Calle EE, Krewski D, Godleski JJ (2004) Cardiovascular mortality and long-term exposure to particulate air pollution: epidemiological evidence of general pathophysiological pathways of disease. Circulation 109(1):71–77. https://doi.org/10.1161/01.CIR.0000108927.80044.7F

    Article  Google Scholar 

  148. Tellez-Plaza M, Jones MR, Dominguez-Lucas A, Guallar E, Navas-Acien A (2013) Cadmium exposure and clinical cardiovascular disease: a systematic review. Curr Atheroscler Rep 15(10):356. https://doi.org/10.1007/s11883-013-0356-2

    Article  CAS  PubMed  Google Scholar 

  149. Kukongviriyapan U, Apaijit K, Kukongviriyapan V (2016) Oxidative stress and cardiovascular dysfunction associated with cadmium exposure: beneficial effects of curcumin and tetrahydrocurcumin. Tohoku J Exp Med 239(1):25–38. https://doi.org/10.1620/tjem.239.25

    Article  CAS  PubMed  Google Scholar 

  150. Bagchi D, Vuchetich P, Bagchi M, Hassoun E, Tran M, Tang L, Stohs S (1997) Induction of oxidative stress by chronic administration of sodium dichromate [chromium VI] and cadmium chloride [cadmium II] to rats. Free Radical Biol Med 22(3):471–478. https://doi.org/10.1016/s0891-5849(96)00352-8

    Article  CAS  Google Scholar 

  151. Liu F, Jan K-Y (2000) DNA damage in arsenite-and cadmium-treated bovine aortic endothelial cells. Free Radical Biol Med 28(1):55–63. https://doi.org/10.1016/s0891-5849(99)00196-3

    Article  Google Scholar 

  152. Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24(4):378–399

    Article  CAS  Google Scholar 

  153. Messner B, Knoflach M, Seubert A, Ritsch A, Pfaller K, Henderson B, Shen YH, Zeller I, Willeit J, Gn L (2009) Cadmium is a novel and independent risk factor for early atherosclerosis mechanisms and in vivo relevance. Arterioscler Thromb Vasc Biol 29(9):1392–1398. https://doi.org/10.1161/ATVBAHA.109.190082

    Article  CAS  PubMed  Google Scholar 

  154. Knoflach M, Messner B, Shen YH, Frotschnig S, Liu G, Pfaller K, Wang X, Matosevic B, Willeit J, Kiechl S (2011) Non-toxic cadmium concentrations induce vascular inflammation and promote atherosclerosis. Circ J 75(10):2491–2495. https://doi.org/10.1253/circj.cj-11-0196

    Article  CAS  PubMed  Google Scholar 

  155. Myong J-P, Kim H-R, Jang T-W, Lee HE, Koo J-W (2014) Association between blood cadmium levels and 10-year coronary heart disease risk in the general Korean population: the Korean National Health and Nutrition Examination Survey 2008–2010. PLoS ONE 9(11):e111909

    Article  Google Scholar 

  156. Barregard L, Sallsten G, Fagerberg B, Borné Y, Persson M, Hedblad B, Engström G (2016) Blood cadmium levels and incident cardiovascular events during follow-up in a population-based cohort of Swedish adults: the Malmö Diet and Cancer Study. Environ Health Perspect 124(5):594–600. https://doi.org/10.1289/ehp.1509735

    Article  CAS  PubMed  Google Scholar 

  157. Fagerberg B, Bergström G, Borén J, Barregard L (2012) Cadmium exposure is accompanied by increased prevalence and future growth of atherosclerotic plaques in 64-year-old women. J Intern Med 272(6):601–610. https://doi.org/10.1111/j.1365-2796.2012.02578.x

    Article  PubMed  Google Scholar 

  158. 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 249:209–214. https://doi.org/10.1016/j.atherosclerosis.2016.01.011

    Article  CAS  PubMed  Google Scholar 

  159. Howard DP, Van Lammeren GW, Rothwell PM, Redgrave JN, Moll FL, de Vries J-PP, De Kleijn DP, Den Ruijter HM, De Borst GJ, Pasterkamp G (2015) Symptomatic carotid atherosclerotic disease: correlations between plaque composition and ipsilateral stroke risk. Stroke 46(1):182–189

    Article  Google Scholar 

  160. Liberda EN, Zuk AM, Tsuji LJ (2019) Complex contaminant mixtures and their associations with intima-media thickness. BMC Cardiovasc Disord 19(1):289. https://doi.org/10.1186/s12872-019-1246-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Ilmiawati C, Reza M, Yanni M, Rusjdi DA (2020) Blood Cd levels and carotid intima-media thickness in young adults living in Padang, Indonesia. BMC Res Notes 13:1–7. https://doi.org/10.1186/s13104-020-05042-0

    Article  CAS  Google Scholar 

  162. Hecht EM, Landy DC, Ahn S, Hlaing WM, Hennekens CH (2013) Hypothesis: cadmium explains, in part, why smoking increases the risk of cardiovascular disease. J Cardiovasc Pharmacol Ther 18(6):550–554. https://doi.org/10.1177/1074248413494815

    Article  CAS  PubMed  Google Scholar 

  163. 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(6):812–822. https://doi.org/10.1016/j.ahj.2014.07.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Choi S, Kwon J, Kwon P, Lee C, Jang S-I (2020) Association between blood heavy metal levels and predicted 10-year risk for a first atherosclerosis cardiovascular disease in the general Korean population. Int J Environ Res Public Health 17(6):2134. https://doi.org/10.3390/ijerph17062134

    Article  CAS  PubMed Central  Google Scholar 

  165. Kolluru GK, Tamilarasan K, Priya SG, Durgha N, Chatterjee S (2006) Cadmium induced endothelial dysfunction: consequence of defective migratory pattern of endothelial cells in association with poor nitric oxide availability under cadmium challenge. Cell Biol Int 30(5):427–438

    Article  CAS  Google Scholar 

  166. Everett CJ, Frithsen IL (2008) Association of urinary cadmium and myocardial infarction. Environ Res 106(2):284–286

    Article  CAS  Google Scholar 

  167. Tellez-Plaza M, Navas-Acien A, Crainiceanu CM, Guallar E (2008) Cadmium exposure and hypertension in the 1999–2004 National Health and Nutrition Examination Survey (NHANES). Environ Health Perspect 116(1):51–56. https://doi.org/10.1289/ehp.10764

    Article  CAS  PubMed  Google Scholar 

  168. Tellez-Plaza M, Navas-Acien A, Crainiceanu CM, Sharrett AR, Guallar E (2010) Cadmium and peripheral arterial disease: gender differences in the 1999–2004 US National Health and Nutrition Examination Survey. Am J Epidemiol 172(6):671–681. https://doi.org/10.1093/aje/kwq172

    Article  PubMed  PubMed Central  Google Scholar 

  169. Peters JL, Perlstein TS, Perry MJ, McNeely E, Weuve J (2010) Cadmium exposure in association with history of stroke and heart failure. Environ Res 110(2):199–206. https://doi.org/10.1016/j.envres.2009.12.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Li H, Fagerberg B, Sallsten G, Borné Y, Hedblad B, Engström G, Barregard L, Andersson EM (2019) Smoking-induced risk of future cardiovascular disease is partly mediated by cadmium in tobacco: Malmö Diet and Cancer Cohort Study. Environ Health 18(1):56. https://doi.org/10.1186/s12940-019-0495-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Santos-Gallego CG, Jialal I (2016) Cadmium and atherosclerosis: Heavy metal or singing the blues? Atherosclerosis 249:230–232. https://doi.org/10.1016/j.atherosclerosis.2016.01.041

    Article  CAS  PubMed  Google Scholar 

  172. Satarug S, Garrett SH, Sens MA, Sens DA (2010) Cadmium, environmental exposure, and health outcomes. Environ Health Perspect 118(2):182–190. https://doi.org/10.1289/ehp.0901234

    Article  CAS  PubMed  Google Scholar 

  173. Yuan Z, Luo T, Liu X, Hua H, Zhuang Y, Zhang X, Zhang L, Zhang Y, Xu W, Ren J (2019) Tracing anthropogenic cadmium emissions: from sources to pollution. Sci Total Environ 676:87–96. https://doi.org/10.1016/j.scitotenv.2019.04.250

    Article  CAS  PubMed  Google Scholar 

  174. Agency EM (2013) EMA/491185/2013 Committee for Medicinal Products for Human Use (CHMP) Giotrif—CHMP assessment report International non-proprietary name: afatinib Procedure No. EMEA/H/C/002280. http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Public_assessment_report/human/002280/WC500152394.pdf

  175. Schaefer HR, Dennis S, Fitzpatrick S (2020) Cadmium: Mitigation strategies to reduce dietary exposure. J Food Sci 85(2):260–267. https://doi.org/10.1111/1750-3841.14997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Kusznierewicz B, Bączek-Kwinta R, Bartoszek A, Piekarska A, Huk A, Manikowska A, Antonkiewicz J, Namieśnik J, Konieczka P (2012) The dose-dependent influence of zinc and cadmium contamination of soil on their uptake and glucosinolate content in white cabbage (Brassica oleracea var. capitata f. alba). Environ Toxicol Chem 31(11):2482–2489. https://doi.org/10.1002/etc.1977

    Article  CAS  PubMed  Google Scholar 

  177. Mostofa MG, Rahman M, Ansary M, Uddin M, Fujita M, Tran L-SP (2019) Interactive effects of salicylic acid and nitric oxide in enhancing rice tolerance to cadmium stress. Int J Mol Sci 20(22):5798. https://doi.org/10.3390/ijms20225798

    Article  CAS  PubMed Central  Google Scholar 

  178. Habib R, Wahdan SA, Gad AM, Azab SS (2019) Infliximab abrogates cadmium-induced testicular damage and spermiotoxicity via enhancement of steroidogenesis and suppression of inflammation and apoptosis mediators. Ecotoxicol Environ Saf 182:109398. https://doi.org/10.1016/j.ecoenv.2019.109398

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Migliaccio.

Ethics declarations

Conflict of interest

Authors declare no conflicts of interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants and/or animals performed by any of the authors.

Informed consent

For this type of study, formal consent is not required.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bimonte, V.M., Besharat, Z.M., Antonioni, A. et al. The endocrine disruptor cadmium: a new player in the pathophysiology of metabolic diseases. J Endocrinol Invest 44, 1363–1377 (2021). https://doi.org/10.1007/s40618-021-01502-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40618-021-01502-x

Keywords

Navigation