Environmental Geochemistry and Health

, Volume 33, Issue 5, pp 469–476 | Cite as

A critical exploration of blood and environmental chromium concentration among oral cancer patients in an oral cancer prevalent area of Taiwan

  • Chi-Ting Chiang
  • Tsun-Kuo Chang
  • Yaw-Huei Hwang
  • Che-Chun Su
  • Kuo-Yang Tsai
  • Tzu-Hsuen Yuan
  • Ie-Bin Lian
Original Paper


The growing incidence of oral cancer (OC) in Taiwan has become a crucial public health concern. In particular, Changhua, a county in central Taiwan, carries persistently high OC incidence rate, with an alarmingly high male/female ratio of OC incidence. Previous epidemiological studies had found that the incidence is spatially correlated with the level of soil content to certain heavy metals in the central Taiwan area. Soil and the human body both intake environmental heavy metals, which can be absorbed through various ways. The soil metal concentration is an index of possible environmental exposure to heavy metal, and the blood metal concentration somewhat reflects the level of the exposure on the human body. Metallic carcinogen is likely to generate free radicals and play a role in many cancers, and many studies had reported that environmental exposure to heavy metals is an important risk factor for developing cancer. Studies on animals showed that chronic intake of chromium (Cr) could induce OC. This study aims to explore the association between the Cr concentration in the farm soil and in the blood of OC patients. We recruited 79 OC patients from Changhua County, with their lifestyle being adjusted in regression analysis. The results showed that the Cr concentration in the blood of OC patients is significantly higher than the background value, and is positively associated with the Cr concentration in the soil surrounding their residence (p-value < 0.023). Because Changhua County is only with moderate prevalence of the known OC habitual risk factors, an environmental factor related to heavy metal Cr exposure is suspected. Future investigations may verify the causal relation between Cr and OC.


Chromium Whole blood Environment Oral cancer Soil pollution 


Conflict of interest

The authors declare that they have no competing interests.


  1. Albanese, S., De Luca, M. L., De Vivo, B., Lima, A., & Grezzi, G. (2008). Relationships between heavy metal distribution and cancer mortality rates in the Campania region, Italy. In B. De Vivo, H. E. Belkin, & A. Lima (Eds.), Environmental geochemistry: Site characterization, data analysis and case histories (pp. 387–400). The Netherlands: Elsevier.Google Scholar
  2. Barany, E., Bergdahl, I. A., Schutz, A., Skerfving, S., & Oskarsson, A. (1997). Inductively coupled plasma mass spectrometry for direct multi-element analysis of diluted human blood and serum. Journal of Analytical Atomic Spectrometry, 12(9), 1005–1009.CrossRefGoogle Scholar
  3. Beaumont, J. J., Sedman, R. M., Reynolds, S. D., Sherman, C. D., Li, L. H., Howd, R. A., et al. (2008). Cancer mortality in a Chinese population exposed to hexavalent chromium in drinking water. Epidemiology, 19, 12–23.CrossRefGoogle Scholar
  4. Beveridge, R., Pintos, J., Parent, M. E., Asselin, J., & Siemiatycki, J. (2010). Lung cancer risk associated with occupational exposure to nickel, chromium VI, and cadmium in two population-based case–control studies in Montreal. American Journal of Industrial Medicine, 53, 476–485.Google Scholar
  5. Case, C. P., Ellis, L., Turner, J. C., & Fairman, B. (2001). Development of a routine method for the determination of trace metals in whole blood by magnetic sector inductively coupled plasma mass spectrometry with particular relevance to patients with total hip and knee arthroplasty. Clinical Chemistry, 47(2), 275–280.Google Scholar
  6. Chang, T. K., Hwang, K. J., & Shyu, G. S. (1997). Using factor analysis to evaluate characteristic of metals in soil pollution. Journal of Taiwan Agricultural Engineering, 43(2), 11–19.Google Scholar
  7. Chang, F. H., Wang, S. L., Huang, Y. L., Tsai, M. H., Yu, S. T., & Chang, L. W. (2006a). Biomonitoring of chromium for residents of areas with a high density of electroplating factories. Journal of Exposure Science Environmental Epidemiology, 16(2), 138–146.CrossRefGoogle Scholar
  8. Chang, F. H., Wang, H. J., Wang, S. L., Wang, Y. C., Hsieh, D. P., Chang, L. W., et al. (2006b). Survey of urinary nickel in residents of areas with a high density of electroplating factories. Chemosphere, 65(10), 1723–1730.CrossRefGoogle Scholar
  9. Chiang, C. T., Hwang, Y. H., Su, C. C., Tsai, K. Y., Lian, I. B., Yuan, T. H., 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. Geospatial Health, 4(2), 230–242.Google Scholar
  10. EC/HC (Environment Canada & Health Canada). (1994). Canadian Environmental Protection Act: Priority substances list assessment report (PSL1): Chromium and its Compounds. EC/HC, Canada.Google Scholar
  11. Gupta, N., Khan, D. K., & Santra, S. C. (2008). An assessment of heavy metal contamination in vegetables grown in wastewater-irrigated areas of Titagarh, West Bengal, India. Bulletin of Environmental Contamination and Toxicology, 80(2), 115–118.CrossRefGoogle Scholar
  12. Halasova, E., Matakova, T., Kavcova, E., Musak, L., Letkova, L., Adamkov, M., et al. (2009). Human lung cancer and hexavalent chromium exposure. Neuroendocrinology Letters, 30(Suppl. 1), 182–185.Google Scholar
  13. Hara, T., Hoshuyama, T., Takahashi, K., Delgermaa, V., & Sorahan, T. (2010). Cancer risk among Japanese chromium platers, 1976–2003. Scandinavian Journal of Work, Environment and Health, 36, 216–221.Google Scholar
  14. IARC (International Agency for Research on Cancer). (1990). Chromium, nickel and welding. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 49, 1–36.Google Scholar
  15. Kerger, B. D., Finley, B. L., Corbett, G. E., Dodge, D. G., & Paustenbach, D. J. (1997). Ingestion of chromium(VI) in drinking water by human volunteers: Absorption, distribution, and excretion of single and repeated doses. Journal of Toxicology and Environmental Health, 50(1), 67–95.CrossRefGoogle Scholar
  16. Ko, Y. C., Huang, Y. L., Lee, C. H., Chen, M. J., Lin, L. M., & Tsai, C. C. (1995). Betel quid chewing, cigarette smoking and alcohol consumption related to oral cancer in Taiwan. Journal of Oral Pathology and Medicine, 24(10), 450–453.CrossRefGoogle Scholar
  17. Låg, J. (1990).General survey of geomedicine. In J. Låg (Ed.), Geomedicine (pp. 1–24). Boca Raton, FL: CRC press.Google Scholar
  18. Langard, S. (1990). One hundred years of chromium and cancer: a review of epidemiological evidence and selected case reports. American Journal of Industrial Medicine, 17(2), 189–215.CrossRefGoogle Scholar
  19. Lian, I. B. (2003). Reducing over-dispersion by generalized degree of freedom and propensity score. Computational Statistics & Data Analysis, 43(2), 197–214.Google Scholar
  20. Lin, Y. P. (2002). Multivariate geostatistical methods to identify and map spatial variations of soil heavy metals. Environmental Geology, 42(1), 1–10.CrossRefGoogle Scholar
  21. Lin, Y. P., & Chang, T. K. (2000a). Geostatistical simulation and estimation of the spatial variability of soil zinc. Journal of Environmental Science and Health Part A—Toxic/Hazardous Substances & Environmental Engineering, 35(3), 327–347.CrossRefGoogle Scholar
  22. Lin, Y. P., & Chang, T. K. (2000b). Simulated annealing and kriging method for identifying the spatial patterns and variability of soil heavy metal. Journal of Environmental Science and Health Part A—Toxic/Hazardous Substances & Environmental Engineering, 35(7), 1089–1115.CrossRefGoogle Scholar
  23. Lin, Y. P., Chang, T. K., Shih, C. W., & Tseng, C. H. (2002a). Factorial and indicator kriging methods using a geographic information system to delineate spatial variation and pollution sources of soil heavy metals. Environmental Geology, 42(8), 900–909.CrossRefGoogle Scholar
  24. Lin, Y. P., Chang, T. K., & Teng, T. P. (2001). Characterization of soil lead by comparing sequential Gaussian simulation, simulated annealing simulation and kriging methods. Environmental Geology, 41(1–2), 189–199.CrossRefGoogle Scholar
  25. Lin, Y. P., Teng, T. P., & Chang, T. K. (2002b). Multivariate analysis of soil heavy metal pollution and landscape pattern in Changhua county in Taiwan. Landscape and Urban Planning, 62(1), 19–35.CrossRefGoogle Scholar
  26. Lin, H. T., Wong, S. S., & Li, G. C. (2004). Heavy metal content of rice and shellfish in Taiwan. Journal of Food & Drug Analysis, 12(2), 167–174.Google Scholar
  27. Rheeder, J. P., Marasas, W. F., Farina, M. P., Thompson, G. R., & Nelson, P. E. (1994). Soil fertility factors in relation to oesophageal cancer risk areas in Transkei, Southern Africa. European Journal of Cancer Prevention, 3(1), 49–56.CrossRefGoogle Scholar
  28. ROCEPA. (1985). Survey of heavy metals in the soil samples. In Environmental Protection Administration of the Republic of China (Ed), Yearbook of environmental protection statistics Taiwan Area, the Republic of China, Taipei.Google Scholar
  29. Rosas, I., Belmont, R., Baez, A., & Villalobospietrini, R. (1989). Some aspects of the environmental exposure to chromium residues in Mexico. Water, Air, and Soil Pollution, 48(3–4), 463–475.Google Scholar
  30. Sedman, R. M., Beaumont, J., McDonald, T. A., Reynolds, S., Krowech, G., & Howd, R. (2006). Review of the evidence regarding the carcinogenicity of hexavalent chromium in drinking water. Journal of Environmental Science and Health Part C—Environmental Carcinogenesis & Ecotoxicology Reviews, 24, 155–182.CrossRefGoogle Scholar
  31. Sorahan, T., Burges, D. C. L., Hamilton, L., & Harrington, J. M. (1998). Lung cancer mortality in nickel/chromium platers, 1946–95. Occupational and Environmental Medicine, 55(4), 236–242.CrossRefGoogle Scholar
  32. Stocks, P., & Davies, R. I. (1964). Zinc and copper content of soils associated with the incidence of cancer of the stomach and other organs. British Journal of Cancer, 18, 14–24.CrossRefGoogle Scholar
  33. Stout, M. D., Herbert, R. A., Kissling, G. E., Collins, B. J., Travlos, G. S., Witt, K. L., et al. (2009). Hexavalent chromium is carcinogenic to F344/N rats and B6C3F1 mice after chronic oral exposure. Environmental Health Perspectives, 117(5), 716–722.Google Scholar
  34. Su, C. C., Chung, J. A., Hsu, Y. Y., Huang, S. J., & Lian, I. B. (2008). Age at diagnosis and prognosis of oral cancer in relation to the patient’s residential area: Experience from a medical center in Taiwan. Oral Oncology, 44(11), 1032–1038.CrossRefGoogle Scholar
  35. Su, C. C., Lin, Y. Y., Chang, T. K., Chiang, C. T., Chung, J. A., Hsu, Y. Y., et al. (2010). Incidence of oral cancer in relation to nickel and arsenic concentrations in farm soils of patients’ residential areas in Taiwan. BMC Public Health, 10, 67.CrossRefGoogle Scholar
  36. Su, C. C., Yang, H. F., Huang, S. J., & Lian I. B. (2007). Distinctive features of oral cancer in Changhua County: High incidence, buccal mucosa preponderance, and a close relation to betel quid chewing habit. Journal of the Formosan Medical Association, 106(3), 225–233.Google Scholar
  37. Taioli, E., Zhitkovich, A., Kinney, P., Udasin, I., Toniolo, P., & Costa, M. (1995). Increased DNA–protein crosslinks in lymphocytes of residents living in chromium-contaminated areas. Biological Trace Element Research, 50(3), 175–180.CrossRefGoogle Scholar
  38. Tisch, M., Enderle, G., Zöller, J., & Maier, H. (1996). Cancer of the oral cavity in machine workers. Laryngorhinootologie, 75, 759–763.CrossRefGoogle Scholar
  39. Tisch, M., & Maier, H. (1996). Squamous epithelial carcinoma of the tongue after occupational exposure to chromium VI compounds. Laryngorhinootologie, 75, 455–458.CrossRefGoogle Scholar
  40. Tsai, K. Y., Su, C. C., Lin, Y. Y., Chung, J. A., & Lian, I. B. (2009). Quantification of betel quid chewing and cigarette smoking in oral cancer patients. Community Dentistry and Oral Epidemiology, 37(6), 555–561.CrossRefGoogle Scholar
  41. Türkdoğan, M. K., Kilicel, F., Kara, K., Tuncer, I., & Uygan, I. (2002). Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environmental Toxicology and Pharmacology, 13(3), 175–179.CrossRefGoogle Scholar
  42. Yassi, A., & Nieboer, E. (1988). Carcinogenicity of chromium compounds. Chromium in Natural and Human Environments. New York: Wiley.Google Scholar
  43. Younas, M., Shahzad, F., Afzal, S., Khan, M. I., & Ali, K. (1998). Assessment of Cd, Ni, Cu, and Pb pollution in Lahore, Pakistan. Environment International, 24(7), 761–766.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Chi-Ting Chiang
    • 1
  • Tsun-Kuo Chang
    • 1
  • Yaw-Huei Hwang
    • 2
  • Che-Chun Su
    • 3
  • Kuo-Yang Tsai
    • 4
  • Tzu-Hsuen Yuan
    • 2
  • Ie-Bin Lian
    • 5
  1. 1.Department of Bioenvironmental Systems EngineeringNational Taiwan UniversityTaipei CityTaiwan
  2. 2.Graduate Institute of Occupational Medicine and Industrial HygieneNational Taiwan UniversityTaipei CityTaiwan
  3. 3.Department of Internal MedicineChanghua Christian HospitalChanghua CityTaiwan
  4. 4.Department of Oral and Maxillofacial SurgeryChanghua Christian HospitalChanghua CityTaiwan
  5. 5.Graduate Institute of Statistics and Information ScienceNational Changhua University of EducationChanghua CityTaiwan

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