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Cadmium (Cd) and Lead (Pb) topsoil levels and incidence of childhood leukemias

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Abstract

There are few well-established risk factors for childhood leukemias. While the frequency of childhood leukemias might be partially attributable to some diseases (accounting for a small fraction of cases) or ionizing radiation, the role of heavy metals has not been assessed. The objective of our study was to assess the potential association between levels of cadmium (Cd) and lead (PB) in soil and childhood leukemias incidence. We conducted a population-based case–control study of childhood leukaemia in Spain, covering 2897 incident cases gathered from the Spanish Registry of Childhood Tumours and including 14 Spanish Regions with a total population of 5,307,433 children (period 1996–2015). Cd and Pb bioavailable levels at every children’s home address were estimated using data from the Geochemical Atlas of Spain. We used logistic regression to estimate odds ratios (ORs) and their 95% confidence intervals (95%CIs); we included as covariates: sex, rurality, employment rate and socioeconomic status. Metal levels were analysed according to two definitions: as continuous variable assuming linearity and as categorical variables to explore a potentially nonlinear association (quantiles). Increases in both Cd and Pb topsoil levels were associated with increased probability of childhood leukemias incidence. The results for the models with the continuous variables showed that a unit increase on the topsoil level was associated with an OR of 1.11 for Cd (95%CI 1.00–1.24) and an OR of 1.10 for Pb (95%CI 0.99–1.21). Our study may point towards a possible link between residential Cd and Pb topsoil levels and the probability of childhood leukemias incidence. Residing in a location with the highest concentrations of these heavy metals compared to those locations with the lowest could increase the risk around a 20%, for both Cd and Pb.

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References

  • Adams, S. V., Passarelli, M. N., & Newcomb, P. A. (2012). Cadmium exposure and cancer mortality in the third national health and nutrition examination survey cohort. Occupational and Environmental Medicine, 69, 153–156. https://doi.org/10.1136/oemed-2011-100111

    Article  CAS  Google Scholar 

  • Ali, H., Khan, E., & Sajad, M. A. (2013). Phytoremediation of heavy metals–concepts and applications. Chemosphere, 91, 869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075

    Article  CAS  Google Scholar 

  • An explicit link between Gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach - Lindgren - 2011 - Journal of the Royal Statistical Society: Series B (Statistical Methodology) - Wiley Online Library [WWW Document], n.d. URL https://rss.onlinelibrary.wiley.com/doi/full/https://doi.org/10.1111/j.1467-9868.2011.00777.x (accessed 10.9.20).

  • Bailey, H. D., Fritschi, L., Metayer, C., Infante-Rivard, C., Magnani, C., Petridou, E., Roman, E., Spector, L. G., Kaatsch, P., Clavel, J., Milne, E., Dockerty, J. D., Glass, D. C., Lightfoot, T., Miligi, L., Rudant, J., Baka, M., Rondelli, R., Amigou, A., … Schüz, J. (2014). Parental occupational paint exposure and risk of childhood leukemia in the offspring: Findings from the Childhood Leukemia International Consortium. Cancer Causes Control CCC, 25, 1351–1367. https://doi.org/10.1007/s10552-014-0441-z

    Article  Google Scholar 

  • Blakley, B. R. (1987). The effect of lead on chemical- and viral-induced tumor production in mice. Journal of Applied Toxicology JAT, 7, 167–172. https://doi.org/10.1002/jat.2550070304

    Article  CAS  Google Scholar 

  • Cadmium in food - Scientific opinion of the Panel on Contaminants in the Food Chain, 2009. . EFSA J. 7, 980. https://doi.org/10.2903/j.efsa.2009.980

  • Carlos-Wallace, F. M., Zhang, L., Smith, M. T., Rader, G., & Steinmaus, C. (2016). Parental, In Utero, and early-life exposure to benzene and the risk of childhood leukemia: A meta-analysis. American Journal of Epidemiology, 183, 1–14. https://doi.org/10.1093/aje/kwv120

    Article  Google Scholar 

  • Chunxia, D., Meifang, W., Jianhua, Z., Ruijuan, Z., Xiue, L., Zhuanzhen, Z., & Linhua, Y. (2019). Tobacco smoke exposure and the risk of childhood acute lymphoblastic leukemia and acute myeloid leukemia: A meta-analysis. Medicine (baltimore), 98, e16454. https://doi.org/10.1097/MD.0000000000016454

    Article  CAS  Google Scholar 

  • CORINE land cover 2006 [WWW Document], 15AD. URL http://www.eea.europa.eu/publications/COR0-landcover

  • Defunciones por causas (lista reducida), sexo y edad. [WWW Document], n.d., (2018). INE. URL https://www.ine.es/jaxi/Tabla.htm?path=/t15/p417/a2018/l0/&file=01001.px&L=0 (accessed 10.9.20).

  • Demir, C., Demir, H., Esen, R., Sehitogullari, A., Atmaca, M., & Alay, M. (2011). Altered serum levels of elements in acute leukemia cases in Turkey. Asian Pacific Journal of Cancer Prevention APJCP, 12, 3471–3474.

    Google Scholar 

  • Espart, A., Artime, S., Tort-Nasarre, G., & Yara-Varón, E. (2018). Cadmium exposure during pregnancy and lactation: Materno-fetal and newborn repercussions of Cd(ii), and Cd-metallothionein complexes. Metallomics an Integrated Biometalal Science, 10, 1359–1367. https://doi.org/10.1039/c8mt00174j

    Article  CAS  Google Scholar 

  • Fei, X., Lou, Z., Christakos, G., Ren, Z., Liu, Q., & Lv, X. (2018). The association between heavy metal soil pollution and stomach cancer: A case study in Hangzhou City China. Environmental Geochemistry and Health, 40, 2481–2490. https://doi.org/10.1007/s10653-018-0113-0

    Article  CAS  Google Scholar 

  • Filippini, T., Heck, J. E., Malagoli, C., Del Giovane, C., & Vinceti, M. (2015). A review and meta-analysis of outdoor air pollution and risk of childhood leukemia. Journal of Environmental Science and Health Part C, 33, 36–66. https://doi.org/10.1080/10590501.2015.1002999 Environ Carcinog. Ecotoxicol. Rev.

    Article  CAS  Google Scholar 

  • Furst, A., Schlauder, M., & Sasmore, D. P. (1976). Tumorigenic activity of lead chromate. Cancer Research, 36, 1779–1783.

    CAS  Google Scholar 

  • García-Pérez, J., Gómez-Barroso, D., Tamayo-Uria, I., & Ramis, R. (2019). Methodological approaches to the study of cancer risk in the vicinity of pollution sources: The experience of a population-based case-control study of childhood cancer. International Journal of Health Geographics, 18, 12. https://doi.org/10.1186/s12942-019-0176-x

    Article  Google Scholar 

  • García-Pérez, J., López-Abente, G., Gómez-Barroso, D., Morales-Piga, A., Romaguera, E. P., Tamayo, I., Fernández-Navarro, P., & Ramis, R. (2015). Childhood leukemia and residential proximity to industrial and urban sites. Environmental Research, 140, 542–553. https://doi.org/10.1016/j.envres.2015.05.014

    Article  CAS  Google Scholar 

  • Gómez-Barroso, D., García-Pérez, J., López-Abente, G., Tamayo-Uria, I., Morales-Piga, A., Pardo Romaguera, E., & Ramis, R. (2016). Agricultural crop exposure and risk of childhood cancer: New findings from a case-control study in Spain. International Journal of Health Geographics, 15, 18. https://doi.org/10.1186/s12942-016-0047-7

    Article  Google Scholar 

  • Gómez-Barroso, D., Rodriguez-Valín, E., Ramis, R., & Cano, R. (2013). Spatio-temporal analysis of tuberculosis in Spain, 2008–2010. International Journal of Tuberculosis and Lung Disease, 17, 745–751. https://doi.org/10.5588/ijtld.12.0702 Off. J. Int. Union Tuberc. Lung Dis.

    Article  Google Scholar 

  • Greaves, M. (2018). A causal mechanism for childhood acute lymphoblastic leukaemia. Nature Reviews Cancer, 18, 471–484. https://doi.org/10.1038/s41568-018-0015-6

    Article  CAS  Google Scholar 

  • Heck, J. E., Park, A. S., Qiu, J., Cockburn, M., & Ritz, B. (2014). Risk of leukemia in relation to exposure to ambient air toxics in pregnancy and early childhood. International Journal of Hygiene and Environmental Health, 217, 662–668. https://doi.org/10.1016/j.ijheh.2013.12.003

    Article  CAS  Google Scholar 

  • Hernández, A. F., & Menéndez, P. (2016). Linking pesticide exposure with pediatric leukemia: potential underlying mechanisms. International Journal of Molecular Sciences, 17, 461. https://doi.org/10.3390/ijms17040461

    Article  CAS  Google Scholar 

  • Huang, H.-H., Huang, J.-Y., Lung, C.-C., Wu, C.-L., Ho, C.-C., Sun, Y.-H., Ko, P.-C., Su, S.-Y., Chen, S.-C., & Liaw, Y.-P. (2013). Cell-type specificity of lung cancer associated with low-dose soil heavy metal contamination in Taiwan: An ecological study. BMC Public Health, 13, 330. https://doi.org/10.1186/1471-2458-13-330

    Article  CAS  Google Scholar 

  • IARC Monographs - Monographs available in PDF format [WWW Document], n.d., (2011). URL http://monographs.iarc.fr/ENG/Monographs/vol102/ (accessed 11.3.16).

  • Ikeda, M., Ezaki, T., Tsukahara, T., & Moriguchi, J. (2004). Dietary cadmium intake in polluted and non-polluted areas in Japan in the past and in the present. International Archives of Occupational and Environmental Health, 77, 227–234. https://doi.org/10.1007/s00420-003-0499-5

    Article  CAS  Google Scholar 

  • Instituto Nacional de Estadística. (National Statistics Institute) [WWW Document], n.d., (2017). URL http://www.ine.es/jaxi/tabla.do?path=/t15/p417/a2012/l0/&file=01001.px&type=pcaxis&L=0 (accessed 9.29.14).

  • International Agency for Research on Cancer, International Agency for Research on Cancer (Eds.), 2006. IARC monographs on the evaluation of carcinogenic risks to humans, volume 87, inorganic and organic lead compounds: this publication represents the views and expert opinions of an IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, which met in Lyon, 10 - 17 February 2004. Presented at the Meeting. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, IARC, Lyon.

  • International Agency for Research on Cancer, Weltgesundheitsorganisation (Eds.), 2012. IARC monographs on the evaluation of carcinogenic risks to humans, volume 100 C, arsenic, metals, fibres, and dusts: this publication represents the views and expert opinions of an IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, which met in Lyon, 17 - 24 March 2009. Presented at the Meeting. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, IARC, Lyon.

  • Investigating Suspected Cancer Clusters and Responding to Community Concerns: Guidelines from CDC and the Council of State and Territorial Epidemiologists [WWW Document], n.d., (2013). URL https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6208a1.htm (accessed 10.13.20).

  • Kim, D. Y., Staley, F., Curtis, G., & Buchanan, S. (2002). Relation between housing age, housing value, and childhood blood lead levels in children in Jefferson County Ky. American Journal of Public Health, 92, 769–772.

    Article  Google Scholar 

  • Kroll, M. E., Stiller, C. A., Murphy, M. F. G., & Carpenter, L. M. (2011). Childhood leukaemia and socioeconomic status in England and Wales 1976–2005: Evidence of higher incidence in relatively affluent communities persists over time. British Journal of Cancer, 105, 1783–1787. https://doi.org/10.1038/bjc.2011.415

    Article  CAS  Google Scholar 

  • Krugner-Higby, L. A., Gendron, A., Laughlin, N. K., Luck, M., Scheffler, J., & Phillips, B. (2001). Chronic myelocytic leukemia in a juvenile rhesus macaque (Macaca mulatta). Contemporary Topics in Laboratory Animal Science, 40, 44–48.

    CAS  Google Scholar 

  • Locutura, J. F., Bel-Lan, A., & Garcia Cortés, A. A. (2012). Atlas geoquímico de España. Instituto Geológico y Minero de España.

    Google Scholar 

  • López-Abente, G., Locutura-Rupérez, J., Fernández-Navarro, P., Martín-Méndez, I., Bel-Lan, A., & Núñez, O. (2018). Compositional analysis of topsoil metals and its associations with cancer mortality using spatial misaligned data. Environmental Geochemistry and Health, 40, 283–294. https://doi.org/10.1007/s10653-016-9904-3

    Article  CAS  Google Scholar 

  • Marcos-Gragera, R., Galceran, J., Martos, C., de Munain, A. L., Vicente-Raneda, M., Navarro, C., Quirós-Garcia, J. R., Sánchez, M.-J., Ardanaz, E., Ramos, M., Mateos, A., Salmerón, D., Felipe, S., & Peris-Bonet, R. (2017). Incidence and survival time trends for Spanish children and adolescents with leukaemia from 1983 to 2007. Clinical and Translational Oncology, 19, 301–316. https://doi.org/10.1007/s12094-016-1531-z Off. Publ. Fed Span. Oncol. Soc. Natl. Cancer Inst. Mex.

    Article  CAS  Google Scholar 

  • McKinley, J. M., Ofterdinger, U., Young, M., Barsby, A., Gavin, A. (2013). Investigating local relationships between trace elements in soils and cancer data. Spatial Statistics, GeoENV2012: Geostatistics for Environmental Applications 5, 25–41. https://doi.org/10.1016/j.spasta.2013.05.001

  • McNally, R. J. Q., Cairns, D. P., Eden, O. B., Alexander, F. E., Taylor, G. M., Kelsey, A. M., & Birch, J. M. (2002). An infectious aetiology for childhood brain tumours? Evidence from space-time clustering and seasonality analyses. British Journal of Cancer, 86, 1070–1077. https://doi.org/10.1038/sj.bjc.6600228

    Article  CAS  Google Scholar 

  • Mezei, G., Sudan, M., Izraeli, S., & Kheifets, L. (2014). Epidemiology of childhood leukemia in the presence and absence of Down syndrome. Cancer Epidemiology, 38, 479–489. https://doi.org/10.1016/j.canep.2014.07.006

    Article  Google Scholar 

  • Miligi, L., Benvenuti, A., Mattioli, S., Salvan, A., Tozzi, G.A., Ranucci, A., Legittimo, P., Rondelli, R., Bisanti, L., Zambon, P., Cannizzaro, S., Kirchmayer, U., Cocco, P., Celentano, E., Assennato, G., Merlo, D.F., Mosciatti, P., Minelli, L., Cuttini, M., Torregrossa, V., Lagorio, S., Haupt, R., Risica, S., Polichetti, A., Group, S.W., Magnani, C. (2013). Risk of childhood leukaemia and non-Hodgkin’s lymphoma after parental occupational exposure to solvents and other agents: the SETIL Study. Occupational and Environental Medicine, 70, 648–655. https://doi.org/10.1136/oemed-2012-100951

  • Núñez, O., Fernández-Navarro, P., Martín-Méndez, I., Bel-Lan, A., Locutura, J. F., & López-Abente, G. (2016). Arsenic and chromium topsoil levels and cancer mortality in Spain. Environmental Science and Pollution Research International, 23, 17664–17675. https://doi.org/10.1007/s11356-016-6806-y

    Article  CAS  Google Scholar 

  • Pardo Romaguera E., Muñoz López A., Valero Poveda S. (2019). Cáncer infantil en España. Estadísticas 1980–2018. Registro Español de Tumores Infantiles (RETI-SEHOP). Universitat de València, Valencia.

  • Pearce, N. (2016). Analysis of matched case-control studies. BMJ, 352, i969. https://doi.org/10.1136/bmj.i969

    Article  Google Scholar 

  • Rodríguez Eugenio, N., McLaughlin, M. J., Pennock, D. J. (2018) Food and Agriculture Organization of the United Nations, Global Soil Partnership, 2018. Soil pollution: a hidden reality.

  • Schüz, J., & Erdmann, F. (2016). Environmental exposure and risk of childhood leukemia: An overview. Archives of Medical Research, 47, 607–614. https://doi.org/10.1016/j.arcmed.2016.11.017

    Article  Google Scholar 

  • Sherief, L. M., Abdelkhalek, E. R., Gharieb, A. F., Sherbiny, H. S., Usef, D. M., Almalky, M. A. A., Kamal, N. M., Salama, M. A., & Gohar, W. (2015). Cadmium status among pediatric cancer patients in Egypt. Medicine (baltimore), 94, e740. https://doi.org/10.1097/MD.0000000000000740

    Article  CAS  Google Scholar 

  • Staessen, J. A., Vyncke, G., Lauwerys, R. R., Roels, H. A., Celis, H. G., Claeys, F., Dondeyne, F., Fagard, R. H., Ide, G., & Lijnen, P. J. (1992). Transfer of cadmium from a sandy acidic soil to man: A population study. Environmental Research, 58, 25–34. https://doi.org/10.1016/s0013-9351(05)80202-6

    Article  CAS  Google Scholar 

  • Steliarova-Foucher, E., Colombet, M., Ries, L. A. G., Moreno, F., Dolya, A., Bray, F., Hesseling, P., Shin, H. Y., & Stiller, C. A. (2017). IICC-3 contributors, 2017 International incidence of childhood cancer, 2001–10: a population-based registry study. Lancet Oncology. https://doi.org/10.1016/S1470-2045(17)30186-9

    Article  Google Scholar 

  • Steliarova-Foucher, E., Stiller, C., Lacour, B., Kaatsch, P. (2005). International Classification of Childhood Cancer, third edition. Cancer, 103, 1457–1467. https://doi.org/10.1002/cncr.20910

  • Tamayo-Uria, I., Boldo, E., García-Pérez, J., Gómez-Barroso, D., Romaguera, E. P., Cirach, M., & Ramis, R. (2018). Childhood leukaemia risk and residential proximity to busy roads. Environment International, 121, 332–339. https://doi.org/10.1016/j.envint.2018.08.056

    Article  Google Scholar 

  • Tong, J., Qin, L., Cao, Y., Li, J., Zhang, J., Nie, J., & An, Y. (2012). Environmental radon exposure and childhood leukemia. Journal of Toxicology and Environmental Health. Part b, Critical Reviews, 15, 332–347. https://doi.org/10.1080/10937404.2012.689555

    Article  CAS  Google Scholar 

  • Toxicological Profile for Cadmium, n.d., (2012). 487.

  • Waalkes, M. P., & Rehm, S. (1992). Carcinogenicity of oral cadmium in the male Wistar (WF/NCr) rat: Effect of chronic dietary zinc deficiency. Fundamental and Applied Toxicology, 19, 512–520. https://doi.org/10.1016/0272-0590(92)90089-z off. J. Soc. Toxicol.

    Article  CAS  Google Scholar 

  • Wulff, M., Högberg, U., & Sandström, A. (1996). Cancer incidence for children born in a smelting community. Acta Oncologica, 35, 179–183. https://doi.org/10.3109/02841869609098499 Stockh. Swed.

    Article  CAS  Google Scholar 

  • Zhao, L., Liu, X., Wang, C., Yan, K., Lin, X., Li, S., Bao, H., & Liu, X. (2014). Magnetic fields exposure and childhood leukemia risk: A meta-analysis based on 11,699 cases and 13,194 controls. Leukemia Research, 38, 269–274. https://doi.org/10.1016/j.leukres.2013.12.008

    Article  Google Scholar 

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Funding

This work was supported by Carlos III Health Institute: FIS 12/01416, AESI PI16CIII/00009, AESI PI19CIII/00025.

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Authors and Affiliations

  1. C.H.U. Insular-Materno Infantil, Gran Canaria, Spain

    Santiago Asenjo

  2. Cancer and Environmental Epidemiology Unit, National Centre of Epidemiology, Carlos III Institute of Health, Madrid, Spain

    Olivier Nuñez, Jordi Segú-Tell, Javier García-Pérez & Rebeca Ramis

  3. Centre for Biomedical Research in Epidemiology & Public Health (CIBER Epidemiología y Salud Pública - CIBERESP), Madrid, Spain

    Olivier Nuñez, Jordi Segú-Tell, Javier García-Pérez & Rebeca Ramis

  4. Spanish Registry of Childhood Tumours (RETI-SEHOP), University of Valencia, Valencia, Spain

    Elena Pardo Romaguera & Adela Cañete Nieto

  5. H. Universitario y Politécnico La Fe, Valencia, Spain

    Adela Cañete Nieto

  6. Instituto Geológico y Minero de España, Madrid, Spain

    Iván Martín-Méndez & Alejandro Bel-lan

  7. Paediatric Environmental Health Speciality Unit, Department of Paediatrics, Institute of Biomedical Research, IMIB-Arrixaca, Clinical University Hospital Virgen de la Arrixaca, Murcia, Spain

    Alberto Cárceles-Álvarez & Juan Antonio Ortega-García

  8. European and Latin American Environment, Survival and Childhood Cancer Network (ENSUCHICA), Murcia, Spain

    Alberto Cárceles-Álvarez, Juan Antonio Ortega-García & Rebeca Ramis

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  1. Santiago Asenjo
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  2. Olivier Nuñez
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Contributions

Substantial contributions to conception and design, acquisition of data or analysis and interpretation of data: SA, ON, RR. Drafting the article or revising it critically for important intellectual content: ON, JST, JGP, ACÁ, JAOG, RR. Final approval of the version to be submitted for publication: All; SA, ON, JST, EPR, ACN, IMM, ABl, JG-P, ACÁ, JAOG, RR.

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Correspondence to Rebeca Ramis.

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Asenjo, S., Nuñez, O., Segú-Tell, J. et al. Cadmium (Cd) and Lead (Pb) topsoil levels and incidence of childhood leukemias. Environ Geochem Health 44, 2341–2354 (2022). https://doi.org/10.1007/s10653-021-01030-w

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