Skip to main content

Advertisement

SpringerLink
Log in

Cadmium in blood of Tunisian men and risk of bladder cancer: interactions with arsenic exposure and smoking

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Prior investigations identified an association between low-level blood arsenic (As) and bladder cancer risk among Tunisian men but questions remain regarding confounding by cadmium (Cd), a well-established bladder carcinogen. A case–control study of Tunisian men was re-examined to assess the levels of cadmium in blood and reparse the association between the simultaneous exposure to these metals and bladder cancer risk. Levels of blood Cd were significantly twice higher among cases than in controls (P < 0.05) and were positively correlated with smoking and age. Additionally, analysis of metal levels among non-smokers according to the region of residence showed very high blood Cd and As levels for the coastal regions of Sfax and central Tunisia. After controlling for potential confounders, for low blood As levels (<0.67 μg/L), the OR for blood Cd was 4.10 (95 % CI 1.64–10.81), while for higher levels (>0.67 μg/L), it was reduced to 2.10 (CI, 1.06–4.17). Adjustment for Cd exposure did not alter the risk associated to As exposure. This study is the first to report the relationship between Cd exposure and risk of bladder cancer occurrence in interaction with smoking and As exposure. Smoking is shown to be the main exposure source to Cd in the Tunisian population but also environmental pollution seems to be responsible of Cd exposure among non-smokers. Exposure assessment studies encompassing a wider population are needed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Amaral AF, Cymbron T, Gärtner F, Lima M, Rodrigues AS (2009) Trace metals and over-expression of metallothioneins in bladder tumoral lesions: a case–control study. BMC Vet Res 18(5):24

    Article  Google Scholar 

  • Ashraf MW (2012) Levels of heavy metals in popular cigarette brands and exposure to these metals via smoking. Sci World J 729430. doi:10.1100/2012/729430

  • Barhoumi S, Messaoudi I, Deli T, Saïd K, Kerkeni A (2009) Cadmium bioaccumulation in three benthic fish species, Salaria basilisca, Zosterisessor ophiocephalus and Solea vulgaris collected from the Gulf of Gabes in Tunisia. J Environ Sci (China) 21(7):980–4

    Article  CAS  Google Scholar 

  • Baris D, Karagas MR, Verrill C, Johnson A, Andrew AS, Marsit CJ et al (2009) A case–control study of smoking and bladder cancer risk: emergent patterns over time. J Natl Cancer Inst 101(22):1553–1561. doi:10.1093/jnci/djp361

    Article  Google Scholar 

  • Batáriová A, Spevácková V, Benes B, Cejchanová M, Smíd J, Cerná M (2006) Blood and urine levels of Pb, Cd and Hg in the general population of the Czech Republic and proposed reference values. Int J Hyg Environ Health 209(4):359–366

    Article  Google Scholar 

  • Bates MN, Rey OA, Biggs ML, Hopenhayn C, Moore LE, Kalman D, Steinmaus C, Smith AH (2004) Case–control study of bladder cancer and exposure to arsenic in Argentina. Am J Epidemiol 159(4):381–389

    Article  Google Scholar 

  • Cancer Registry in Southern Tunisia (2002) Cancer incidence for the years 1997–1999. Available on http://www.insp.nat.tn/fr/unite_the/regis/inci97.99b.pdf

  • Chen CJ, Chen CW, Wu MM, Kuo TL (1992) Cancer potential in liver, lung, bladder and kidney due to ingested inorganic arsenic in drinking water. Br J Cancer 66(5):888–892

    Article  CAS  Google Scholar 

  • Chen Y, Graziano JH, Parvez F, Hussain I, Momotaj H, van Geen A, Howe GR, Ahsan H (2006) Modification of risk of arsenic-induced skin lesions by sunlight exposure, smoking, and occupational exposures in Bangladesh. Epidemiology 17(4):459–467

    Article  Google Scholar 

  • Choura M (2008) Environmental assessment of the processing activity of phosphate in the Southern coastal area of Grand Sfax: Prospects for development and rehabilitation. SMAP III Project (Tunisia 2006–2008) Strategy of Integrated Southern Coastal Zone of Grand Sfax. Interim Report 2008. In French. Available on http://www.medcities.org/docs/Evaluation%20environnementale%20SIAPE-provisoire.pdf

  • Chowdhury BA, Chandra RK (1987) Biological and health implications of toxic heavy metal and essential trace element interactions. Prog Food Nutr Sci 11(1):55–113

    CAS  Google Scholar 

  • Díaz-Barriga F, Llamas E, Mejía JJ, Carrizales L, Santoyo ME, Vega-Vega L, Yáñez L (1990) Arsenic–cadmium interaction in rats. Toxicology 64(2):191–203

    Article  Google Scholar 

  • Drake EN, Sky-peck HH (1989) Discriminant analysis of trace element distribution in normal and malignant human tissues. Cancer Res 49:4210–4215

    CAS  Google Scholar 

  • El Ati-Hellal M, Hedhili A, Hellal F, Boujlel K, Dachraoui M, Bousnina M, Ghorbel H, Ndhif M (2005) Lead and cadmium concentrations in seawater and algae of the Tunisian coast. Arch Inst Pasteur Tunis 82(1–4):75–82

    CAS  Google Scholar 

  • El Kihel B (1995) Impact of discharges of phosphogypsum in the Gulf of Gabes: geochemistry of heavy metals in sediments. PhD Dissertation, Univ of Tunis II, p86

  • Feki-Tounsi M, Olmedo P, Gil F, Khlifi R, Mhiri MN, Rebai A, Hamza-Chaffai A (2012) Low-level arsenic exposure is associated with bladder cancer risk and cigarette smoking: a case–control study among men in Tunisia. Environ Sci Pollut Res Int. doi:10.1007/s11356-012-1335-9

    Google Scholar 

  • Gargouri D, Azri C, Serbaji MM, Jedoui Y, Montacer M (2011) Heavy metal concentrations in the surface marine sediments of Sfax Coast, Tunisia. Environ Monit Assess 175(1–4):519–530

    Article  CAS  Google Scholar 

  • Gil F, Capitán-Vallvey LF, De Santiago E, Ballesta J, Pla A, Hernández AF, Gutiérrez-Bedmar M, Fernández-Crehuet J, Gómez J, López-Guarnido O, Rodrigo L, Villanueva E (2006) Heavy metal concentrations in the general population of Andalusia, South of Spain: a comparison with the population within the area of influence of Aznalcóllar mine spill (SW Spain). Sci Total Environ 372(1):49–57

    Google Scholar 

  • Gil F, Hernández AF (2009) Significance of biochemical markers in applied toxicology. In: Ballantyne B, Marrs TC, Syversen T (eds) General and Applied Toxicology, vol 2. Wiley, Chichester, pp 847–858

    Google Scholar 

  • Gil F, Pla A (2001) Biomarkers as biological indicators of xenobiotic exposure. J Appl Toxicol 21:245–255

    Article  CAS  Google Scholar 

  • Hamza-Chaffai A (1993) Study of metal bioaccumulation and metallothionein in fish from the coast of Sfax (Gulf of Gabes), PhD Dissertation. Univ of Sfax, pp 157

  • Huang YL, Sheu JY, Lin TH (1999) Association between oxidative stress and changes of trace elements in patients with bladder cancer. Clin Biochem 32(2):131–136

    Article  CAS  Google Scholar 

  • IARC (1993) Cadmium and cadmium compounds. IARC Monogr Eval Carcinog Risks Hum 58:119–237

    Google Scholar 

  • IEH Report on factors affecting the absorption of toxic metals from the diet (1998) Report R8. Medical Research Council. Institute for Environment and Health. University of Leicester, UK. Available on http://www.cranfield.ac.uk/health/researchareas/environmenthealth/ieh/ieh%20publications/r8.pdf

  • Illou S, Serbaji MM, Montacer M, Medhioub K (1996) Study of surface sediments of the northern coast of the city of Sfax-trace metals pollution, National Colloquium of Earth Sciences, Boumerdes, Algeria 20–21 May 1996

  • Illou S (1999) Impact of domestic and industrial telluric discharges on coastal environments: case of the northern coast of Sfax City (Tunisia). PhD dissertation. Sfax University. Tunisia

  • Jiang G, Gong Z, Li XF, Cullen WR, Le XC (2003) Interaction of trivalent arsenicals with metallothionein. Chem Res Toxicol 16(7):873–880

    Article  CAS  Google Scholar 

  • Johnson AM, O’Connell MJ, Miyamoto H, Huang J, Yao JL, Messing EM, Reeder JE (2008) Androgenic dependence of exophytic tumor growth in a transgenic mouse model of bladder cancer: a role for thrombospondin-1. BMC Urol 8:7

    Article  Google Scholar 

  • Joseph P (2009) Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharmacol 238(3):272–9. doi:10.1016/j.taap.2009.01.011

    Article  CAS  Google Scholar 

  • Kellen E, Zeegers MP, Hond ED, Buntinx F (2007) Blood cadmium may be associated with bladder carcinogenesis: the Belgian case–control study on bladder cancer. Cancer Detect Prev 31(1):77–82

    Article  CAS  Google Scholar 

  • Marsit CJ, Karagas MR, Schned A, Kelsey KT (2006) Carcinogen exposure and epigenetic silencing in bladder cancer. Ann N Y Acad Sci 1076:810–821

    Article  CAS  Google Scholar 

  • Mink PJ, Alexander DD, Barraj LM, Kelsh MA, Tsuji JS (2008) Low-level arsenic exposure in drinking water and bladder cancer: a review and meta-analysis. Regul Toxicol Pharmacol 52(3):299–310

    Article  CAS  Google Scholar 

  • Moszczyński P, Zabiński Z, Moszczyński P Jr, Rutowski J, Słowiński S, Tabarowski Z (2001) Immunological findings in cigarette smokers. Toxicol Lett 118(3):121–127

    Article  Google Scholar 

  • Mrizak D, B’chir F, Jaidane M, Jean Arnaud M, Saguem S (2011) Effects of change in smoking habits on bladder cancer incidence in Tunisia. Health. doi:10.4236/health.2011.310103

  • Olmedo P, Pla A, Hernández AF, López-Guarnido O, Rodrigo L, Gil F (2010) Validation of a method to quantify chromium, cadmium, manganese, nickel and lead in human whole blood, urine, saliva and hair samples by electrothermal atomic absorption spectrometry. Anal Chim Acta 5;659(1–2):60–67

    Google Scholar 

  • Olsson IM, Bensryd I, Lundh T, Ottosson H, Skerfving S, Oskarsson A (2002) Cadmium in blood and urine—impact of sex, age, dietary intake, iron status, and former smoking-association of renal effects. Environ Health Perspect 110(12):1185–1190

    Article  CAS  Google Scholar 

  • Parkin DM, Pisani P, Ferlay J (1994) At least one of seven cases of cancer is caused by smoking. Global estimate for 1985. Int J Cancer 59:494–504. doi:10.1002/ijc.2910590411

    Article  CAS  Google Scholar 

  • Pelluchi C, Bosetti C, Negri E, Malvezzi M, La Vecchia C (2006) Mechanisms of disease: the epidemiology of bladder cancer. Nat Clin Pract Urol 3:327–340. doi:10.1038/ncpuro0510

    Article  Google Scholar 

  • Pizent A, Jurasović J, Telišman S (2001) Blood pressure in relation to dietary calcium intake, alcohol consumption, blood lead, and blood cadmium in female nonsmokers. Journal of Trace Elements in Medicine and Biology 15(2–3):123–130

    Article  CAS  Google Scholar 

  • Stämpfli MR, Anderson GP (2009) How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 9:377–384

    Article  Google Scholar 

  • Smith AH, Hopenhayn-Rich C, Bates MN, Goeden HM, Hertz-Picciotto I, Duggan HM, Wood R, Kosnett MJ, Smith MT (1992) Cancer risks from arsenic in drinking water. Environ Health Perspect 97:259–267

    Article  CAS  Google Scholar 

  • Viana GF, Garcia KS, Menezes-Filho JA (2011) Assessment of carcinogenic heavy metal levels in Brazilian cigarettes. Environ Monit Assess 181(1–4):255–265. doi:10.1007/s10661-010-1827-3

    Article  CAS  Google Scholar 

  • Wu CC, Pu YS, Wu HC, Yang CY, Chen YC (2011) Reversed association between levels of prostate specific antigen and levels of blood cadmium and urinary cadmium. Chemosphere 83(8):1188–1191. doi:10.1016/j

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Authors express their sincere thanks to the medical staff in Sfax Hospital who facilitated sampling procedures and data collection on the subjects of the study. Acknowledgements are also addressed to the technical team in the Department of Toxicology and Legal Medicine, Faculty of Medicine of Granada for their considerable assistance in the analysis of metals.

Disclosure statement

The study received ethics approval. Funding was provided by the Ministry of High Education and Scientific research in Tunisia. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have no competing financial interests to report.

Author information

Authors and Affiliations

  1. Unit of Marine and Environmental Toxicology. IPEIS, University of Sfax, BP 805, 3018, Sfax, Tunisia

    Molka Feki-Tounsi, Rim Khlifi & Amel Hamza-Chaffai

  2. Unité de Toxicologie Marine et Environnementale. IPEIS, Université de Sfax, BP 805, 3018, Sfax, Tunisia

    Molka Feki-Tounsi

  3. Department of Bioinformatics and Human Genetics, Center of Biotechnology of Sfax, Sfax, Tunisia

    Molka Feki-Tounsi, Rim Khlifi & Ahmed Rebai

  4. Department of Legal medicine and Toxicology, Faculty of medicine, University of Granada, Granada, Spain

    Pablo Olmedo & Fernando Gil

  5. Department of Urology, CHU Habib Bourguiba, Sfax, Tunisia

    Mohamed-Nabil Mhiri

Authors
  1. Molka Feki-Tounsi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pablo Olmedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rim Khlifi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohamed-Nabil Mhiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ahmed Rebai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Amel Hamza-Chaffai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Molka Feki-Tounsi.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feki-Tounsi, M., Olmedo, P., Gil, F. et al. Cadmium in blood of Tunisian men and risk of bladder cancer: interactions with arsenic exposure and smoking. Environ Sci Pollut Res 20, 7204–7213 (2013). https://doi.org/10.1007/s11356-013-1716-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-1716-8

Keywords

Search

Navigation