Environmental Science and Pollution Research

, Volume 20, Issue 11, pp 8282–8294

Blood nickel and chromium levels in association with smoking and occupational exposure among head and neck cancer patients in Tunisia

  • Rim Khlifi
  • Pablo Olmedo
  • Fernando Gil
  • Molka Feki-Tounsi
  • Amine Chakroun
  • Ahmed Rebai
  • Amel Hamza-Chaffai
Research Article

Abstract

Chronic exposure to chromium (Cr) and nickel (Ni) has long been recognized as being capable to increase head and neck cancer (HNC) incidence among exposed human populations. This study represents the first biomonitoring of Cr and Ni exposure in Tunisia and focuses on a possible association with HNC risk. The aim of the present study was to evaluate the concentrations of Cr and Ni in the blood of HNC patients and controls. Metals blood levels of 169 HNC patients and 351 controls were determined using a Perkin-Elmer Analyst 800 Atomic Absorption Spectrometer. Mean blood levels of Cr and Ni in HNC cases (52.15 and 111.60 μg/L, respectively) were significantly higher than those of controls (37.04 and 30.50 μg/L, respectively). Cases’ blood levels of Cr and Ni were significantly higher than those of controls after controlling for the other risk factors of HNC, including smoking, shisha consumption, occupational exposure, and nearby environment (P < 0.05). Among these risk factors, smoking and occupational exposure presented the most significant association with HNC (odds ratio (OR) = 6.54 and 7.66, respectively, P < 0.001). Cr and Ni levels in blood sample of cases and controls that are smoker/occupationally exposed were higher than that of non-smoker/non-occupationally exposed (P < 0.05). Smokers who are occupationally exposed present the most significant association with HNC (OR = 25.08, P < 0.0001). High levels of blood Cr (OR = 2.09) and high levels of blood Ni (OR = 8.87) were strongly associated with HNC after other potential confounders were controlled (P = 0.004 and P < 0.0001, respectively). This study suggested a potential role of Cr and Ni in the mechanism of HNC development.

Keywords

Chromium Nickel Head and neck cancer Tobacco smoking Occupational exposure 

References

  1. Afridi HI, Kazi TG, Kazi NG, Jamali MK, Arain MB, Sirajuddin Baig JA, Kandhro GA, Wadhwa SK, Shah AQ (2010) Evaluation of cadmium, lead, nickel and zinc status in biological samples of smokers and nonsmokers hypertensive patients. J Hum Hypertens 24(1):34–43CrossRefGoogle Scholar
  2. Afridi HI, Kazi TG, Kazi N, Abbas Kandhro G, Ahmed Baig J, Shah AQ, Khan S, Kolachi NF, Wadhwa SK, Shah F, Jamali MK, Arain MB (2011) Evaluation of cadmium, chromium, nickel, and zinc in biological samples of psoriasis patients living in Pakistani cement factory area. Biol Trace Elem Res 142:284–301CrossRefGoogle Scholar
  3. Applebaum KM, Furniss CS, Zeka A, Posner MR, Smith JF, Bryan J et al (2007) Lack of association of alcohol and tobacco with HPV16-associated head and neck cancer. J Natl Cancer Inst 993:1801–1810CrossRefGoogle Scholar
  4. Armstrong RW, Imrey PB, Lye MS, Armstrong MJ, Yu MC, Sani S (2000) Nasopharyngeal carcinoma in Malaysian Chinese: occupational exposures to particles, formaldehyde and heat. Int J Epidemiol 29:991–998CrossRefGoogle Scholar
  5. 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 21:980–984CrossRefGoogle Scholar
  6. Ben Abdallah M, Zehani S, Hizem Ben Ayoub W (2003) North Tunisia Cancer Registry Third report, 1999–2003. Internal report Mansourbenabdallah@rnstnGoogle Scholar
  7. Blot WJ, McLaughlin JK, Winn DM et al (1988) Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Res 48:3282–3287Google Scholar
  8. Bosetti C, Gallus S, Franceschi S, Levi F, Bertuzzi M, Negri E, Talamini R, La Vecchia C (2002) Cancer of the larynx in non-smoking alcohol drinkers and in non-drinking tobacco smokers. Br J Cancer 87:516–518CrossRefGoogle Scholar
  9. Boyle P, Levine B (2008) World cancer report 2008. International Agency for Research on Cancer, Lyon, p 330Google Scholar
  10. Brown CP, Spivey GH, Valentine JL, Browdy BL (1980) Cigarette smoking and lead levels in occupationally exposed lead workers. J Toxicol Environ Health 64:877–883CrossRefGoogle Scholar
  11. Brown T, Darnton A, Fortunato L, Rushton L (2012) Occupational cancer in Britain. Respiratory cancer sites: larynx, lung and mesotheliom. Br J Cancer 107(1):S56–70CrossRefGoogle Scholar
  12. Carter JD, Ghio AJ, Samet JM, Devlin RB (1997) Cytokine production by human airway epithelial cells after exposure to an air pollution particle is metal-dependent. Toxicol Appl Pharmacol 146:180–188CrossRefGoogle Scholar
  13. Chang FH, Wang SL, Huang YL, Tsai MH, Yu ST, Chang LW (2006) Biomonitoring of chromium for residents of areas with a high density of electroplating factories. J Expo Sci Environ Epidemiol 16:138–146CrossRefGoogle Scholar
  14. Chen CJ, Shih TS, Chang HY, Yu HS, Wu JD, Sheu SC, Wu CE, Chou TC (2008) The total body burden of chromium associated with skin disease and smoking among cement workers. Sci Total Environ 391:76–81CrossRefGoogle Scholar
  15. Chiang CT, Hwang YH, Su CC, Tsai KY, Lian IB, Yuan TH et al (2010) Elucidating the underlying causes of oral cancer through spatial clustering in high-risk areas of Taiwan with a distinct gender ratio of incidence. Geospat Health 4:230–242Google Scholar
  16. Chiba M, Masironi R (1992) Toxic and trace element in tobacco smoke. Bull World Health Organ 70:269–275Google Scholar
  17. Choi SY, Kahyo H (1991) Effect of cigarette smoking and alcohol consumption in the aetiology of cancer of the oral cavity pharynx and larynx. Int J Epidemiol 20:878–885CrossRefGoogle Scholar
  18. Chuang HY, Lee ML, Chao KY, Wang JD, Hu H (1999) Relationship of blood lead levels to personal hygiene habits in lead battery workers, Taiwan 1991–1997. Am J Ind Med 356:595–603CrossRefGoogle Scholar
  19. Curado MP, Hashibe M (2009) Recent changes in the epidemiology of head and neck cancer. Curr Opin Oncol 21(3):194–200CrossRefGoogle Scholar
  20. Da Silva EF, Mlayah A, Gomes C, Noronha F, Charef A, Sequeira C, Esteves V, Marques AR (2010) Heavy elements in the phosphorite from Kalaa Khasba mine (north-western Tunisia): potential implications on the environment and human health. J Hazard Mater 182(1–3):232–245CrossRefGoogle Scholar
  21. Danadevi K, Rozati R, Banu BS, Grover P (2004) Genotoxic evaluation of welders occupationally exposed to chromium and nickel using the Comet and micronucleus assays. Mutagenesis 19:35–41CrossRefGoogle Scholar
  22. Davies JM, Easton DF, Bidstrup PL (1991) Mortality from respiratory cancer and other causes in United Kingdom chromate production workers. Br J Ind Med 48:299–313Google Scholar
  23. Demarini DM (2004) Genotoxicity of tobacco smoke and tobacco smoke condensate, a review. Mutat Res 567:447–474CrossRefGoogle Scholar
  24. Demir TA, Isikli B, Urer SM, Berber A, Akar T, Canbek M et al (2005) Nickel exposure and its effects. Biometals 18:7–13CrossRefGoogle Scholar
  25. Eloussaief M, Benzina M (2010) Efficiency of natural and acid-activated clays in the removal of PbII from aqueous solutions. J Hazard Mater 178:753–757CrossRefGoogle Scholar
  26. EL-Shafei HM (2012) Monitoring of urine and serum cellular enzymes in the chromium electroplating workers. J Bioeng Biomed Sci 2:3Google Scholar
  27. Eyre H, Kahn R, Robertson RM, Clark NG, Doyle C, Gansler T, Glynn T, Hong Y, Smith RA, Taubert K, Thun MJ (2004) Preventing cancer, cardiovascular disease, and diabetes, a common agenda for the American Cancer Society, the American Diabetes Association, and the American Heart Association. CA Cancer J Clin 54:190–207CrossRefGoogle Scholar
  28. Fakhfakh R, Hsairi M, Maalej M, Achour N, Nacef T (2002) Tobacco use in Tunisia, behaviour and awareness. Bull World Health Organ 80:350–356Google Scholar
  29. Ferlay J, Pisani P, Parkin DM (2004) GLOBOCAN 2002: cancer incidence, mortality and prevalence worldwide IARC Cancer Base 2002 estimates. IARC, LyonGoogle Scholar
  30. Fowles J, Dybing B (2003) Application of toxicological risk assessment principles to the chemical constituents of tobacco smoke. Tob Control 12:424–430CrossRefGoogle Scholar
  31. Franceschi S, Talamini R, Barra S, Baron AE, Negri E, Bidoli E, Serraino D, La Vecchia C (1990) Smoking and drinking in relation to cancers of the oral cavity pharynx larynx and esophagus in northern Italy. Cancer Res 50:6502–6507Google Scholar
  32. Franceschi S, Levi F, La Vecchia C, Conti E, Dal Maso L, Barzan L, Talamini R (1999) Comparison of the effect of smoking and alcohol drinking between oral and pharyngeal cancer. Int J Cancer 83:1–4CrossRefGoogle Scholar
  33. Gandhi G, Kumar N (2004) DNA damage in peripheral blood lymphocytes of individuals residing near a wastewater drain and using underground water resources. Environ Mol Mutagen 43:235–242CrossRefGoogle Scholar
  34. Garnit H, Bouhlel S, Barca D, Chtara C (2012) Application of LA-ICP-MS to sedimentary phosphatic particles from Tunisian phosphorite deposits: insights from trace elements and REE into paleo-depositional environments. Chem Erde 72:127–139CrossRefGoogle Scholar
  35. Gibb HJ, Lees PS, Pinsky PF, Rooneym BC (2000) Lung cancer among workers in chromium chemical production. Am J Ind Med 3:115–126CrossRefGoogle Scholar
  36. 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 372:49–57CrossRefGoogle Scholar
  37. Gil F, Hernández AF, Márquez C, Femia P, Olmedo P, López-Guarnido O, Pla A (2011) Biomonitorization of cadmium, chromium, manganese, nickel and lead in whole blood, urine, axillary hair and saliva in an occupationally exposed population. Sci Total Environ 409:1172–1180CrossRefGoogle Scholar
  38. Goldberg P, Leclerc A, Luce D, Morcet JF, Brug J (1997) Laryngeal and hypopharyngeal cancer and occupation: results of a case–control study. Occup Environ Med 54(7):477–482CrossRefGoogle Scholar
  39. Grimsrud TK, Peto J (2006) Persisting risk of nickel related lung cancer and nasal cancer among Clydach refiners. Occup Environ Med 63:365–366CrossRefGoogle Scholar
  40. Grimsrud TK, Berge SR, Haldorsen T, Andersen A (2002) Exposure to different forms of nickel and risk of lung cancer. Am J Epidemiol 156:1123–1132CrossRefGoogle Scholar
  41. Hamza-Chaffai A, Amiard JC, Pellerin J, Joux L, Berthet B (2000) The potential use of metallothionein in the clam Ruditapes decussatus as a biomarker of in situ metal exposure. Comp Biochem Physiol 127:185–197Google Scholar
  42. Harrabi I, Maatoug-Maaloul J, Gaha R, Kebaili R, Maziak W, Ghannem H (2010) Comparaison De La Consommation De Cigarettes Et De Narguilé Chez Les Elèves De La Ville De Sousse. Tunis Med 88:470–473Google Scholar
  43. Hashibe M, Brennan P, Benhamou S, Castellsague X, Chen C, Curado MP et al (2007) Alcohol drinking in never users of tobacco cigarette smoking in never drinkers and the risk of head and neck cancer, pooled analysis in the international head and neck cancer epidemiology consortium. J Natl Cancer Inst 99(10):777–789CrossRefGoogle Scholar
  44. Hecht SH (1999) Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 91:1194–1210CrossRefGoogle Scholar
  45. Heim KE, Bates HK, Rush RE, Oller AR (2007) Oral carcinogenicity study with nickel sulfate hexahydrate in Fischer rats. Toxicol Appl Pharmacol 224:126–137CrossRefGoogle Scholar
  46. Hodnett D, Wood DM, Raja K, Dargan PI, Shah AD (2012) A healthy volunteer study to investigate trace element contamination of blood samples by stainless steel venipuncture needles. Clin Toxicol (Phila) 50(2):99–107CrossRefGoogle Scholar
  47. Huebner WW, Schoenberg JB, Kelsey JL et al (1992) Oral and pharyngeal cancer and occupation: a case–control study. Epidemiology 3(4):300–309CrossRefGoogle Scholar
  48. Husgavfel-Pursiainen K (2004) Genotoxicity of environmental tobacco smoke, a review. Mutat Res 567:427–445CrossRefGoogle Scholar
  49. IARC (1990a) Working group chromium and chromium compounds. IARC Monogr Eval Carcinog Risks Hum 49:249–256Google Scholar
  50. IARC (1990b) Chromium nickel and welding: IARC monographs on the evaluation of carcinogenic risks to humans, vol 49. IARC, LyonGoogle Scholar
  51. IARC (1992) IARC monographs on the evaluation of the carcinogenic risk to humans, occupational exposure to mists and vapours from strong inorganic acids; and other industrial chemicals, vol 54. IARC, Lyon, pp 1–130Google Scholar
  52. Jin T, Lu J, Nordberg M (1998) Toxicokinetics and biochemistry of cadmium with special emphasis on the role of metallothionein. Neurotoxicology 19:529–535Google Scholar
  53. Joseph P, Lei YX, Ong TM (2004) Up-regulation of expression of translation factors—a novel molecular mechanism for cadmium carcinogenesis. Mol Cell Biochem 255:93–101CrossRefGoogle Scholar
  54. Kallén K (1999) Maternal smoking and congenital heart defects. Eur J Epidemiol 15:731–737CrossRefGoogle Scholar
  55. Karita K, Nakao M, Ohwaki K, Yamanouchi Y, Nishikitani M, Nomura K et al (2005) Blood lead and erythrocyte protoporphyrin levels in association with smoking and personal hygienic behaviour among lead exposed workers. Occup Environ Med 625:300–303CrossRefGoogle Scholar
  56. Khandekar SP, Bagdey PS, Tiwari RR (2006) Oral cancer and some epidemiological factors, a hospital based study. Indian J Commun Med 31(3):157–159Google Scholar
  57. Khlifi R, Hamza-Chaffai A (2010) Head and neck cancer due to heavy metal exposure via tobacco smoking and professional exposure: A review. Toxicol Appl Pharmacol 248:71–88Google Scholar
  58. Ko YC, Huang YL, Lee CH, Chen MJ, Lin LM, Tsai CC (1995) Betel quid chewing, cigarette smoking and alcohol consumption related to oral cancer in Taiwan. J Oral Pathol Med 24:450–453CrossRefGoogle Scholar
  59. Kuo HW, Wu ML (2002) Effects of chromic acid exposure on immunological parameters among electroplating workers. Int Arch Occup Environ Health 75:186–190CrossRefGoogle Scholar
  60. Lawrence DA, McCable MJ Jr (1995) Immune modulation by toxic metals. In: Goyer RA, Klaassen CD, Waalkes MP (eds) Metal toxicology. Academic, New York, pp 305–335Google Scholar
  61. Lee MJ (1998) Marihuana and tobacco use in pregnancy. Obstet Gynecol Clin N Am 25:66–83CrossRefGoogle Scholar
  62. Lee KW, Kuo WR, Tsai SM, Wu DC, Wang WM, Fang FM, Chiang FY, Ho KY, Wang LF, Tai CF, Kao EL, Chou SH, Lee CH, Chai CY, Ko YC (2005) Different impact from betel quid alcohol and cigarette, risk factors for pharyngeal and laryngeal cancer. Int J Cancer 117:831–836CrossRefGoogle Scholar
  63. Little J, Cardy A, Munger RG (2004) Tobacco smoking and oral clefts a meta-analysis. Bull World Health Organ 82:213–218Google Scholar
  64. Maier H, Dietz A, Gewelke U, Heller WD (1991) Occupational exposure to hazardous substances and risk of cancer in the area of the mouth cavity, oropharynx, hypopharynx and larynx: a case–control study. Laryngorhinootologie 70(2):93–98CrossRefGoogle Scholar
  65. Marsh GM, Youk AO, Buchanich JM, Erdal S, Esmen NA (2007) Work in the metal industry and nasopharyngeal cancer mortality among formaldehyde-exposed workers. Regul Toxicol Pharmacol 48:308–319CrossRefGoogle Scholar
  66. Mashberg A, Boffetta P, Winkelman R, Garfinkel L (1993) Tobacco smoking alcohol drinking and cancer of the oral cavity and oropharynx among US veterans. Cancer 72:1369–1367CrossRefGoogle Scholar
  67. Maziak W, Ward KD, Afifi-Soweid RA, Eissenberg T (2004) Tobacco smoking using a waterpipe, a re-emerging strain in a global epidemic. Tob Control 13:327–333CrossRefGoogle Scholar
  68. Menvielle G, Luce D, Goldberg P, Leclerc A (2004) Smoking, alcohol drinking, occupational exposures and social inequalities in hypopharyngeal and laryngeal cancer. Int J Epidemiol 33:799–806CrossRefGoogle Scholar
  69. Messaoudi I, Barhoumi S, Saïd K, Kerkeni A (2009) Study on the sensitivity to cadmium of marine fish Salaria basilisca (Pisces: Blennidae). J Environ Sci 21:1620–1624CrossRefGoogle Scholar
  70. Muscat JE, Richie JP, Thompson S, Wynder EL (1996) Gender differences in smoking and risk for oral cancer. Cancer Res 56:5192–5197Google Scholar
  71. NRC (1999) Arsenic in the drinking water. National Research Council report. National Academy, Washington, DCGoogle Scholar
  72. 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 659:60–67CrossRefGoogle Scholar
  73. Olsen J, Sabroe S (1984) Occupational causes of laryngeal cancer. J Epidemiol Community Health 38(2):117–121CrossRefGoogle Scholar
  74. Purdue MP, Järvholm B, Bergdahl IA, Hayes RB, Baris D (2006) Occupational exposures and head and neck cancers among Swedish construction workers. Scand J Work Environ Health 32(4):270–275CrossRefGoogle Scholar
  75. Radhouane F, Mohamed H, Noureddine A (2005) Epidemiology and prevention of tobacco use in Tunisia, a review. Prev Med 40:652–657CrossRefGoogle Scholar
  76. Ramsay S (2002) PAHO exposes tobacco-industry tactics in Latin America Pan American Health Organization. Lancet 360:20–57Google Scholar
  77. Rastam S, Li FM, Fouad FM, Kamal HM, Akil N, Moustafa AE (2010) Water pipe smoking and human oral cancers. Med Hypotheses 74(3):457–459CrossRefGoogle Scholar
  78. Rodu B, Jansson C (2004) Smokeless tobacco and oral cancer are view of the risks and determinants. Crit Rev Oral Biol Med 15:252–263CrossRefGoogle Scholar
  79. Satarug S, Ujjin P, Vanavanitkun Y, Baker JR, Moore MR (2004) Influence of body iron store status and cigarette smoking on cadmium body burden of healthy Thai women and men. Toxicol Lett 1483:177–185CrossRefGoogle Scholar
  80. Schildt EB, Eriksson M, Hardell L, Magnuson A (1998) Oral snuff, smoking habits and alcohol consumption in relation to oral cancer in a Swedish case–control study. Int J Cancer 77:341–346CrossRefGoogle Scholar
  81. Sellami A, Sellami Boudawara T et al (2007) Incidence des cancers dans le Gouvernorat de Sfax, 2000–2002 ednGoogle Scholar
  82. Shih CM, Wu JS, Ko WC, Wang LE, Wei YH, Liang HF, Chen YC, Chen TC (2003) Mitochondria-mediated caspase-independent apoptosis induced by cadmium in normal human lung cells. J Cell Biochem 89:335–347CrossRefGoogle Scholar
  83. Shimizu M, Hochadel JF, Waalkes MP (1997) Effects of glutathione depletion on cadmium-induced metallothionein synthesis cytotoxicity and proto-oncogene expression in cultured rat myoblasts. J Toxicol Environ Health 51:609–621Google Scholar
  84. Sinyoung S, Songsiriritthigul P, Asavapisit S, Kajitvichyanukul P (2011) Chromium behavior during cement-production processes: a clinkerization, hydration, and leaching study. J Hazard Mater 191:296–305CrossRefGoogle Scholar
  85. Stewart BW, Kleihues P (2003a) Head and neck cancer. In: Stewart BW, Kleihues P (eds) World cancer report. IARC, Lyon, pp 232–235Google Scholar
  86. Stewart BW, Kleihues P (2003b) The cause of cancer. In: Stewart BW, Kleihues P (eds) World cancer report. IARC, Lyon, pp 22–31Google Scholar
  87. Stohs SJ, Bagchi D, Bagchi M (1997) Toxicity of trace elements in tobacco smoke. Inhal Toxicol 9:867–890CrossRefGoogle Scholar
  88. Stojanović D, Nikić D, Lazarević K (2004) The level of nickel in smoker's blood and urine. Cent Eur J Public Health 12(4):187–189Google Scholar
  89. Stout MD, Herbert RA, Kissling GE, Collins BJ, Travlos GS, Witt KL et al (2009) Hexavalent chromium is carcinogenic to F344/N rats and B6C3F1 mice after chronic oral exposure. Environ Health Perspect 117:716–122Google Scholar
  90. Stridsklev IC, Schaller KH, Raithel HJ (2004) Monitoring of chromium and nickel in biological fluids of stainless steel welders using the flux-cored-wire FCW welding method. Int Arch Occup Environ Health 77:587–591CrossRefGoogle Scholar
  91. Stridsklev IC, Schaller KH, Langård S (2007) Monitoring of chromium and nickel in biological Xuids of grinders grinding stainless steel. Int Arch Occup Environ Health 80:450–454CrossRefGoogle Scholar
  92. Su CC, Lin YY, Chang TK, Chiang CT, Chung JA, Hsu YY et al (2010a) Incidence of oral cancer in relation to nickel and arsenic concentrations in farm soils of patients' residential areas in Taiwan. BMC Public Health 10:67CrossRefGoogle Scholar
  93. Su CC, Tsai KY, Hsu YY, Lin YY, Lian IB (2010b) Chronic exposure to heavy metals and incidence of oral cancer in Taiwanese males. Oral Oncol 46:586–590CrossRefGoogle Scholar
  94. Tisch M, Maier H (1996) Squamous epithelial carcinoma of the tongue after occupational exposure to chromium VI compounds. Laryngorhinootologie 75:455–458CrossRefGoogle Scholar
  95. Tisch M, Enderle G, Zöller J, Maier H (1996) Cancer of the oral cavity in machine workers. Laryngorhinootologie 75:759–763CrossRefGoogle Scholar
  96. Ulenbelt P, Lumens ME, Geron HM, Herber RF, Broersen S, Zielhuis RL (1990) Work hygienic behaviour as modifier of the lead air–lead blood relation. Int Arch Occup Environ Health 623:203–207CrossRefGoogle Scholar
  97. Verity MA (1995) Nervous system. In: Goyer RA, Klaassen CD, Waalkes MP (eds) Metal toxicology. Academic, New York, pp 199–235Google Scholar
  98. Watanabe T, Shimbo S, Nakatsuka H, Koizumi A, Higashikawa K, Matsuda-Inoguchi N et al (2004) Gender-related difference, geographical variation and time trend in dietary cadmium intake in Japan. Sci Total Environ 329(1–3):17–27CrossRefGoogle Scholar
  99. Yuan TH, Lian IB, Tsai KY, Chang TK, Chiang CT, Su CC, Hwang YH (2011) Possible association between nickel and chromium and oral cancer, a case–control study in central Taiwan. Sci Total Environ 409:1046–1052CrossRefGoogle Scholar
  100. Zairi M, Rouis MJ (1999) Impacts environnementaux du stockage du phosphogypse à Sfax Tunisie. Bull Lab Ponts Chaussées 2:29–40Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Rim Khlifi
    • 1
    • 2
  • Pablo Olmedo
    • 3
  • Fernando Gil
    • 3
  • Molka Feki-Tounsi
    • 1
    • 2
  • Amine Chakroun
    • 4
  • Ahmed Rebai
    • 2
  • Amel Hamza-Chaffai
    • 1
  1. 1.Unit of Marine and Environmental Toxicology, UR 09-03Sfax University, IPEISSfaxTunisia
  2. 2.Bioinformatics UnitCentre of Biotechnology of SfaxSfaxTunisia
  3. 3.Department of Legal Medicine and ToxicologyUniversity of GranadaGranadaSpain
  4. 4.Department of OtorhinolaryngologyHabib Borguiba HospitalSfaxTunisia

Personalised recommendations