Environmental Science and Pollution Research

, Volume 25, Issue 18, pp 17611–17619 | Cite as

Connecting gastrointestinal cancer risk to cadmium and lead exposure in the Chaoshan population of Southeast China

  • Xueqiong Lin
  • Lin Peng
  • Xijin Xu
  • Yanrong Chen
  • Yuling Zhang
  • Xia Huo
Research Article


Cadmium (Cd) and lead (Pb) pose a serious threat to human health because of its carcinogenicity. China ranks first according to the Global Cancer Report for 2014 in newly diagnosed gastrointestinal cancers and cancer deaths. The aim of the present study was to evaluate the association of Cd and Pb burden with the risk of gastrointestinal cancers in a hospital-based case-control study from southern regions of China, Chaoshan area. A total of 279 hospitalized patients were recruited in this study, of which 167 were gastrointestinal cancer cases (70 esophageal cancer, 51 gastric cancer, and 46 colorectal cancer), and 112 controls were recruited from two hospitals in the Chaoshan area of southeast China. Basic clinical data and information on gender, age, and other demographic characteristics were collected from medical records. Blood Cd and Pb levels were detected by graphite furnace atomizer absorption spectrophotometry (GFAAS). Blood Cd/Pb levels and over-limit ratios between cases and controls were compared by Mann-Whitney U and Kruskal-Wallis H tests. We used logistic regression to estimate odds ratios (ORs) as measures of relative risk and explored the relationships between blood Cd/Pb levels and gastrointestinal cancer risk and clinicopathological characteristics. Median levels of blood Cd and Pb in cases (2.12 and 60.03 μg/L, respectively) were significantly higher than those of controls (1.47 and 53.84 μg/L, respectively). The over-limit ratios for Cd (≥ 5 μg/L) and Pb (≥ 100 μg/L) in the cases were both higher than that of controls. Blood Cd levels had a tendency to accumulate in the human body with gender, age, and tobacco smoking, while blood Pb levels only were associated with tobacco smoking. The logistic regression model illustrated that gastrointestinal cancers were significantly associated with blood Cd levels and blood Pb levels. The concentrations of Cd and Pb in patients with T3 + T4 stage were markedly higher than in patients with T1 + T2. On the other hand, blood Cd levels were dramatically increased in the distant –metastasis (M1). Blood Cd and Pb levels are significantly higher in gastrointestinal cancers compared to controls. Cd and Pb appear to be risk factors for gastrointestinal cancers in Chaoshan region, and higher levels of Cd and Pb may promote the occurrence and progression of gastrointestinal cancers.


Blood cadmium levels Blood lead levels Esophageal cancer Gastric cancer Colorectal cancer 



We are grateful to all the volunteers for participating in the present study.

Funding information

This work was supported by the Science and Technology Planning Project of Guangdong Province (2014 a020212558) and the Department of Education of Guangdong Government under the Top-tier University Development Scheme (2016046).

Compliance with ethical standards

Ethics approval and consent to participate

This study was performed with the approval of the Human Ethical Committee of the Cancer Hospital of Shantou University Medical College. All participants signed informed consent.

Competing interests

The authors declare that they have no competing interests.


  1. Absalon D, Ślesak B (2010) The effects of changes in cadmium and lead air pollution on cancer incidence in children. Sci Total Environ 40820:4420–4428CrossRefGoogle Scholar
  2. Afridi HI, Kazi TG, Kazi NG, Jamali MK, Arain MB, Sirajuddin, Shah AQ (2010) Evaluation of cadmium, lead, nickel and zinc status in biological samples of smokers and nonsmokers hypertensive patients. J Hum Hypertens 241:34–43CrossRefGoogle Scholar
  3. Åkesson A, Barregard L, Bergdahl IA, Nordberg GF, Nordberg M, Skerfving S (2014) Non-renal effects and the risk assessment of environmental cadmium exposure. Environ Health Perspect 1225:431–438Google Scholar
  4. Bishak YK, Payahoo L, Osatdrahimi A, Nourazarian A (2015) Mechanisms of cadmium carcinogenicity in the gastrointestinal tract. Asian Pac J Cancer PrevApjcp 161:9–21CrossRefGoogle Scholar
  5. Brown LM, Devesa SS (2002) Epidemiologic trends in esophageal and gastric cancer in the United States. Surg Oncol Clin N Am 112:235–256CrossRefGoogle Scholar
  6. Chen W, Zheng R, Zhang S, Zeng H, Fan Y, Qiao Y, Zhou Q (2014) Esophageal cancer incidence and mortality in China, 2010. J Thorac Dis 54:343–348Google Scholar
  7. Chen YC, Pu YS, Wu HC, Wu TT, Lai MK, Yang CY, Sung FC (2009) Cadmium burden and the risk and phenotype of prostate cancer. BMC Cancer 91:1–7Google Scholar
  8. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 12712:2893–2917CrossRefGoogle Scholar
  9. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 1365:E359–E386CrossRefGoogle Scholar
  10. Ferrández A, Lanas A (2006) The role of COX-2 in chemoprevention of colorectal cancer: a friend or an enemy? Curr Colorectal Cancer Rep 21:5–12CrossRefGoogle Scholar
  11. Herszényi L, Tulassay Z (2010) Epidemiology of gastrointestinal and liver tumors. Eur Rev Med Pharmacol Sci 144:249–258Google Scholar
  12. Huo X, Peng L, Xu X, Zheng L, Qiu B, Qi Z et al (2007) Elevated blood lead levels of children in Guiyu, an electronic waste recycling town in China. Environ Health Perspect 1157:1113–1117Google Scholar
  13. Ikeda M, Ohashi F, Fukui Y, Sakuragi S, Moriguchi J (2011) Cadmium, chromium, lead, manganese and nickel concentrations in blood of women in non-polluted areas in Japan, as determined by inductively coupled plasma-sector field-mass spectrometry. Int Arch Occup Environ Health 842:139–150CrossRefGoogle Scholar
  14. Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 2383:201–208CrossRefGoogle Scholar
  15. Jin T, Nordberg M, Frech W, Dumont X, Bernard A, Ye TT et al (2002) Cadmium biomonitoring and renal dysfunction among a population environmentally exposed to cadmium from smelting in China (ChinaCad). BioMetals An Int J Role Metal Ions Biol Biochem Med 154:397–410Google Scholar
  16. Joseph P (2009) Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharmacol 2383:272–279CrossRefGoogle Scholar
  17. Khassouani CE, Soulaymani R, Mauras Y, Allain P (2000) Blood cadmium concentration in the population of the Rabat area, Morocco. Clinica chimica acta; international journal of clinical chemistry 3021–2:155–160CrossRefGoogle Scholar
  18. Kim K, Seo H, Chin JH, Son HJ, Hwang JH, Kim YK (2014) Preoperative hypoalbuminemia and anemia as predictors of transfusion in radical nephrectomy for renal cell carcinoma: a retrospective study. BMC Anesthesiol 151:1–7Google Scholar
  19. Kira CS, Sakuma AM, De Capitani EM, de Freitas CU, Cardoso MR, Gouveia N (2015) Associated factors for higher lead and cadmium blood levels, and reference values derived from general population of São Paulo, Brazil. Sci Total Environ 543(Pt A):628–635Google Scholar
  20. Kleihues P, & Stewart B W (2003) World cancer reportGoogle Scholar
  21. Krejs GJ (2010) Gastric cancer: epidemiology and risk factors. Dig Dis 284-5:600–603CrossRefGoogle Scholar
  22. Leung AO, Duzgorenaydin NS, Cheung KC, Wong MH (2008) Heavy metals concentrations of surface dust from e-waste recycling and its human health implications in southeast China. Environ Sci Technol 427:2674–2680CrossRefGoogle Scholar
  23. Lin H, William W, Li-Min OU (2015) Epidemic status of esophagus cancer and etiological research of esophagus cancer in Chaoshan. Chin Pract Med 1032:277–279Google Scholar
  24. Liu S, Huang B, Huang H, Li X, Chen G, Zhang G et al (2013) Patrilineal background of esophageal cancer and gastric cardia cancer patients in a Chaoshan high-risk area in China. PLoS One 812:1611–1614Google Scholar
  25. Machalek DA, Wark JD, Tabrizi SN, Hopper JL, Bui M, Dite GS et al (2016) Genetic and environmental factors in invasive cervical cancer: design and methods of a classical twin study. Twin Res Human Gen 201:10–18Google Scholar
  26. Madeddu R, Solinas G, Forte G, Bocca B, Asara Y, Tolu P et al (2011) Diet and nutrients are contributing factors that influence blood cadmium levels. Nutr Res 319:691–697CrossRefGoogle Scholar
  27. Mao W, Hong S, Chen WQ, Lu C, Hu Q, Ren Z et al (2011) Cancer mortality in a Chinese population surrounding a multi-metal sulphide mine in Guangdong province: an ecologic study. BMC Public Health 111:1–15Google Scholar
  28. Martley E, Gulson BL, Pfeifer HR (2004) Metal concentrations in soils around the copper smelter and surrounding industrial complex of port Kembla, NSW, Australia. Sci Total Environ 3251-3:113–127CrossRefGoogle Scholar
  29. Matsunaga Y, Agaku IT, Vardavas CI (2014) The association between cigarette rod length, slim design, and blood cadmium levels among U.S. smokers: NHANES 1999–2010. Prev Med 658:87–91CrossRefGoogle Scholar
  30. Mohajer R, Salehi MH, Mohammadi J, Emami MH, Azarm T (2013) The status of lead and cadmium in soils of high prevalenct gastrointestinal cancer region of Isfahan. J Res Med Sci Off J Isfahan Univ Med Sci 183:210–214Google Scholar
  31. Nawrot TS, Martens DS, Hara A, Plusquin M, Vangronsveld J, Roels HA, Staessen JA (2015) Association of total cancer and lung cancer with environmental exposure to cadmium: the meta-analytical evidence. Cancer Causes & Control 269:1281–1288CrossRefGoogle Scholar
  32. Organization W H (2014) World Health Organization. World Cancer Rep 2014Google Scholar
  33. Parsa N (2012) Environmental factors inducing human cancers. Iran J Public Health 4111:1–9Google Scholar
  34. Peng L, Huang Y, Zhang J, Peng Y, Lin X, Wu K, Huo X (2015a) Cadmium exposure and the risk of breast cancer in Chaoshan population of southeast China. Environ Sci Poll Res Int 2224:19870–19878CrossRefGoogle Scholar
  35. Peng L, Wang X, Huo X, Xu X, Lin K, Zhang J et al (2015b) Blood cadmium burden and the risk of nasopharyngeal carcinoma: a case–control study in Chinese Chaoshan population. Environ Sci Poll Res 2216:12323–12331Google Scholar
  36. Pirkle JL, Brody DJ, Gunter EW, Kramer RA, Paschal DC, Flegal KM, Matte TD (1994) The decline in blood lead levels in the United States. The National Health and nutrition examination surveys (NHANES). Jama J Am Med Assoc 2724:284–291CrossRefGoogle Scholar
  37. 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. J Trace Elements Med Biol Organ Soc Min Trace Elements 152-3:123–130CrossRefGoogle Scholar
  38. Qiao YM, Gu JG, Yang Y, Huang CJ (2010) The distribution, enrichment and pollution assessment of heavy metals in surface sediments of sea areas around the Nanao Island. J Trop Oceanogr 291:77–84Google Scholar
  39. Rodríguez Martín JA, Arias ML, Grau Corbí JM (2006) Heavy metals contents in agricultural topsoils in the Ebro basin (Spain). Application of the multivariate geoestatistical methods to study spatial variations. Environ Pollut 1443:1001–1012CrossRefGoogle Scholar
  40. Song Y, Wang Y, Mao W, Sui H, Yong L, Yang D et al (2017) Dietary cadmium exposure assessment among the Chinese population. PLoS One 125:e0177978CrossRefGoogle Scholar
  41. Stathopoulos GP, Tsiaras N (2003) Epidemiology and pathogenesis of esophageal cancer: management and its controversial results (review). Oncol Rep 102:449–454Google Scholar
  42. Sun K, Liu D, Pan F, Wei Y, Hou D, Yang XE (2017) Study on relationship between heavy metals exposure and breast cancer. Acta Agriculturae Zhejiangensis 298:1353–1357Google Scholar
  43. Sun P. (2004). Investigation and evaluation of the pollution of water and biological trace metals in the waters near Shantou. Jinan UniversityGoogle Scholar
  44. Takayama T, Gelboin HV, Chahon MA, Matsushima (1980) Genetic and environmental factors in experimental and human cancer. Jpn Sci Soc Press 93813:93810M–993819MGoogle Scholar
  45. Tallberg P, Lehtoranta J, Hietanen S (2014) Smoking, lower gastrointestinal endoscopy, and risk for colorectal cancer. Cancer Epidemiol Biomarkers Prev 233:525–533Google Scholar
  46. Tettey M, Edwin F, Aniteye E, Sereboe L, Tamatey M, Ofosu-Appiah E, Adzamli I (2012) The changing epidemiology of esophageal cancer in sub-Saharan Africa—the case of Ghana. Pan African Med J 13:6–12Google Scholar
  47. Toxfaqs DOT (2003) ATSDR Toxicological Profile for Lead (update). (Agency for Toxic Substances and Disease Registry)Atlanta, GA: U.S. Department of Health and Human Services1999. J Hosp Palliat Nurs 44:206–207Google Scholar
  48. Wong CS, Wu SC, Duzgoren-Aydin NS, Aydin A, Wong MH (2007) Trace metal contamination of sediments in an e-waste processing village in China. Environ Pollut 1452:434–442CrossRefGoogle Scholar
  49. Wu X, Cobbina SJ, Mao G, Hai X, Zhen Z, Yang L (2016) A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Poll Res 239:8244–8259CrossRefGoogle Scholar
  50. Yan G, Guoyi Y, Qiaoxiang D, Changjiang H (2007) Distribution of heavy metals in soils from the typical regions of Shantou and their environmental pollution assessment. Environ Sci 285:1067–1074Google Scholar
  51. Yang-Guang GU, Yang YF, Lin Q (2013) Heavy metal speciation and potential risk assessment in sediments from the mariculture areas in Baisha Bay, Nanao, Shantou. Mar Environ Sci 323:333–337Google Scholar
  52. Yang CX, Wang HY, Wang ZM, Du HZ, Tao DM, Mu XY et al (2005) Risk factors for esophageal cancer: a case-control study in South-Western China. Asian Pac J Cancer Prev Apjcp 61:48–53Google Scholar
  53. Yang H, Huo X, Yekeen TA, Zheng Q, Zheng M, Xu X (2013) Effects of lead and cadmium exposure from electronic waste on child physical growth. Environ Sci Poll Res 207:4441–4447CrossRefGoogle Scholar
  54. Yekeen TA, Xu X, Zhang Y, Wu Y, Kim S, Reponen T et al (2016) Assessment of health risk of trace metal pollution in surface soil and road dust from e-waste recycling area in China. Environ Sci Poll Res 2317:17511–17524Google Scholar
  55. Zhang LL, Lu L, Pan YJ, Ding CG, Xu DY, Huang CF et al (2015) Baseline blood levels of manganese, lead, cadmium, copper, and zinc in residents of Beijing suburb. Environ Res 140:10–17Google Scholar
  56. Zheng X (2016) Ambient air heavy metals in PM2.5 and potential human health risk assessment in an informal electronic-waste recycling site of China. Aerosol Air Qual Res 16:388–397CrossRefGoogle Scholar
  57. Zhou YH, Bai Y, Lian-Sheng LI (2011) Heavy metal distribution patterns and environmental quality assessment of the mariculture areas in Nanao,Shantou. Mar Sci Bull 131:71–79Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xueqiong Lin
    • 1
    • 2
  • Lin Peng
    • 1
    • 2
  • Xijin Xu
    • 2
    • 3
  • Yanrong Chen
    • 2
    • 4
  • Yuling Zhang
    • 2
  • Xia Huo
    • 5
  1. 1.Clinical LaboratoryCancer Hospital of Shantou University Medical CollegeShantouChina
  2. 2.Laboratory of Environmental Medicine and Developmental Toxicology, and Guangdong Provincial Key Laboratory of Infectious DiseasesShantou University Medical CollegeShantouChina
  3. 3.Department of Cell Biology and GeneticsShantou University Medical CollegeShantouChina
  4. 4.Clinical LaboratoryThe First Affiliated Hospital of Shantou University Medical CollegeShantouChina
  5. 5.Laboratory of Environmental Medicine and Developmental Toxicology, Guangdong Key Laboratory of Environmental Pollution and Health, School of EnvironmentJinan UniversityGuangzhouChina

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