Human Health Risk Assessment Due to Agricultural Activities and Crop Consumption in the Surroundings of an Industrial Area

  • Marina M. S. Cabral-Pinto
  • Manuela Inácio
  • Orquídia Neves
  • Agostinho A. Almeida
  • Edgar Pinto
  • Bárbara Oliveiros
  • Eduardo A. Ferreira da SilvaEmail author
Original Paper


The present work integrates concentrations of potentially toxic elements (PTE) (i.e. As, Cd, Cr, Cu, Hg, Ni, Pb and Zn) from (i) environmental media (i.e. soil, crops) and (ii) human hair. The aim was to assess whether agricultural soil and vegetable quality are related to risks to human health from different exposures pathways and if there are any signs of it in human hair. Domestic vegetable gardens in the surroundings Estarreja chemical complex (ECC), Municipality of Estarreja, central Portugal, were the selected for the current study. Data analysis of two soil fractions (2 mm and < 63 µm) and of three different vegetables (Lycopersicon esculentum Mill., Solanum tuberosum, L. and Brassica oleracea, L.) samples were used. Agricultural soils in the ECC surrounding present high concentrations of As, Cu, Hg and Pb (mg/kg: up to 532, 103, 13.7 and 109, respectively). The high PTE concentrations in soils and horticultural crops are chiefly related to historical industrial activities, mostly from arsenopyrite roasting and a chloralkali plant. The assessment of risks to human health for ECC-surrounding residents (children 4–8 years old; elderly adults > 55 years old) showed that agricultural soil-dust ingestion induces a high-non-carcinogenic risk (HI) for As (HI up to 41 and 4.4, for children and adult, respectively), Pb (HI up to 2.5 for children) and Hg (HI up to 1.3 for children) and carcinogenic risk (CR) for As (10−3 for both age groups). Exposure through consumption of tomatoes and potatoes grown in the study soils does not present a high health hazard. However, exposure to As through consumption of cabbage presents both carcinogenic and non-carcinogenic health risks for both studied age groups (CR > 10−4 and HI > 1.1). It is likely that hair As and Hg concentrations increases in both children and adults can be related to the ingestion of agricultural soil and cabbage, and inhalation or dermal contact with contaminated soil. Nonetheless, this assumption requires further investigation, including on other potential sources of contaminants for the local population, such as dietary intake of other foodstuffs. Hair Cr content in the adult group of residents showed maximum values above the normal range for non-exposed individuals, as well as high mean and median values which may be related to the high Cr content in the studied foods. The exposure study results are in agreement with As and Hg concentrations in both children and adults hair and validate it as a biomarker of As and Hg local environmental exposure.


Exposure PTE Soil Crop Hair biomonitoring Health risk 



Funding for this research was provided by the Projects SFRH/BPD/71030/2010, Project UID/GEO/04035/2013 (GeoBioTec Research Centre) financed by FCT – Fundação para a Ciência e Tecnologia and by the Labex DRIIHM, Réseau des Observatoires Hommes-Millieux–Centre National de la Recherche Scientifique (ROHM–CNRS) and OHMI-Estarreja. We thank also the participants for taking part in this research and the local private institutions of social solidarity for the collaboration (Santa Casa Misericórdia de Estarreja, Associação Humanitária de Salreu, Centro Paroquial Social São Tomé de Canelas, Centro Paroquial Social Avanca, Fundação Cónego Filipe Figueiredo Beduído and Centro Paroquial de Pardilhó). The authors would further like to thank editor and three anonymous reviewers for their comments that greatly helped improve the quality of this manuscript.


Funding was provided by Institut National des Sciences de l'Univers, Centre National de la Recherche Scientifique ()Grant No. OHM2014).

Supplementary material

12403_2019_323_MOESM1_ESM.pdf (126 kb)
Supplementary file1 (PDF 45 kb)
12403_2019_323_MOESM2_ESM.pdf (46 kb)
Supplementary file2 (PDF 126 kb)
12403_2019_323_MOESM3_ESM.docx (17 kb)
Supplementary file3 (DOCX 211 kb)
12403_2019_323_MOESM4_ESM.xlsx (10 kb)
Supplementary material 3 (XLSX 17 kb)
12403_2019_323_MOESM5_ESM.xlsx (12 kb)
Supplementary file4 (XLSX 9 kb)


  1. Amaral AF, Arruda M, Cabral S, Rodrigues AS (2008) Essential and non-essential trace metals in scalp hair of men chronically exposed to volcanogenic metals in the Azores, Portugal. Environ Int 34(8):1104–1108CrossRefGoogle Scholar
  2. APA (2016) Planos de Gestão das Bacias Hidrográficas dos Rios Vouga, Mondego e Lis integradas na Região Hidrográfica 4. Parte 2 – Caracterização Geral e Diagnóstico. 1.4.2. Caracterização das Massas de Água Subterrânea. Report. Ex-ARH Centro. Accessed 10 Sep 2018
  3. ATSDR (2000) Toxicological profile for arsenic. US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry, Washington DC, p 428Google Scholar
  4. Ayodele JT, Bayero AS (2009) Lead and zinc concentrations in hair and nail of some Kano inhabitants. Afr J Environ Sci Technol 3(6):164–170Google Scholar
  5. Barbosa AC, Jardim W, Dorea JG, Fosberg B, Souza J (2001) Hair mercury speciation as a function of gender, age, and body mass index in inhabitants of the Negro River basin, Amazon, Brazil. Arch Environ Contam Toxicol 40(3):439–444CrossRefGoogle Scholar
  6. Bass DA, Hickok D, Quig D, Urek K (2001) Trace element analysis in hair: factors determining accuracy, precision, and reliability. Altern Med Rev 6(5):472–481Google Scholar
  7. Brima EI, Haris PI, Jenkins RO, Polya DA, Gault AG, Harrington CF (2006) Understanding arsenic metabolism through a comparative study of arsenic levels in the urine, hair and fingernails of healthy volunteers from three unexposed ethnic groups in the United Kingdom. Toxicol Appl Pharm 216(1):122–130CrossRefGoogle Scholar
  8. Cabral Pinto MMS, Ferreira da Silva E (2019) Heavy Metals of Santiago Island (Cape Verde) alluvial deposits: baseline value maps and human health risk assessment. Int J Environ Res Public Health 16(1):2CrossRefGoogle Scholar
  9. Cabral Pinto MMS, Marinho-Reis AP, Almeida A, Ordens CM, Silva MM, Freitas S, Ferreira da Silva EA (2017) Human predisposition to cognitive impairment and its relation with environmental exposure to potentially toxic elements. Environ Geochem Health. CrossRefGoogle Scholar
  10. Cabral Pinto MMS, Marinho-Reis AP, Almeida A, Freitas S, Simões MR, Diniz ML, Moreira PI (2018) Fingernail trace element content in environmentally exposed individuals and its influence on their cognitive status in ageing. Expo Health. CrossRefGoogle Scholar
  11. Cabral Pinto MMS, Ordens CM, Condesso de Melo MT, Inácio M, Almeida A, Pinto E, Ferreira da Silva EA (2019) An inter-disciplinary approach to evaluate human health risks due to long-term exposure to contaminated groundwater near a chemical complex. Expo Health. CrossRefGoogle Scholar
  12. Cachada A, Pereira ME, Ferreira da Silva E, Duarte AC (2012) Sources of potentially toxic elements and organic pollutants in an urban area subjected to an industrial impact. Environ Monit Assess 184:15–32CrossRefGoogle Scholar
  13. Canadian guideline: Minister of the Environment (Canada). Soil, Ground Water and Sediment Standards for Use under Part XV.1 of the Environmental Protection Act. Accessed 15 Oct 2018.
  14. Carrington CD, Bolger PM (2000) A pooled analysis of the Iraqi and Seychelles methylmercury studies. Hum Ecol Risk Assess 6(2):323–340CrossRefGoogle Scholar
  15. CCME (2011) Canadian Soil Quality Guidelines for the protection of environmental and human health. Winnipeg, Canada Council of Ministers of the Environment (updated 1999, 2001, 2011)Google Scholar
  16. Chabukdhara M, Munjal A, Nema AK, Gupta SK, Kaushal RK (2016) Heavy metal contamination in vegetables grown around peri-urban and urban-industrial clusters in Ghaziabad, India. Hum Ecol Risk Assess Int J 22:736–752CrossRefGoogle Scholar
  17. Coelho P, Costa S, Costa C, Silva S, Walter A, Ranville J et al (2012) Metal(loid)s levels in biological matrices from human populations exposed to mining contamination. J Toxicol Environ Health Sci A 75(13–15):893–908CrossRefGoogle Scholar
  18. Coelho P, Costa S, Costa C, Silva S, Walter A, Ranville J, Zoffoli R (2013) Biomonitoring of several toxic metal(loid)s in different biological matrices from environmentally and occupationally exposed populations from Panasqueira mine area, Portugal. Environ Geochem Health 36(2):255–269CrossRefGoogle Scholar
  19. Costa C, Jesus-Rydin C (2001) Site investigation on heavy metals contaminated ground in Estarreja—Portugal. Eng Geol 60(1–4):39–47CrossRefGoogle Scholar
  20. Eastman RR, Jursa TP, Benedetti C, Lucchini RG, Smith DR (2013) Hair as a biomarker of environmental manganese exposure. Environ Sci Technol 47(3):1629–1637Google Scholar
  21. FAO/WHO (2001): Codex Alimentarius Commission (FAO/WHO). Food additives and contaminants. Joint FAO/WHO Food Standards Programme 2001, ALINORM 01/12A: 1–289Google Scholar
  22. Gault AG, Rowland HA, Charnock JM, Wogelius RA, Gomez-Morilla I, Vong S, Polya DA (2008) Arsenic in hair and nails of individuals exposed to arsenic-rich groundwaters in Kandal province, Cambodia. Sci Total Environ. 393(1):168–176CrossRefGoogle Scholar
  23. Gupta N, Yadav KK, Kumar V, Kumar S, Chadd RP, Kumar A (2018) Trace elements in soil-vegetables interface: translocation, bioaccumulation, toxicity and amelioration-a review. Sci Tottal Environ 651:2927–2942CrossRefGoogle Scholar
  24. Hintz HF (2000) Hair analysis as an indicator of nutritional status. J Equine Vet Sci 21:199Google Scholar
  25. IARC (2017) International Agency for Research on Cancer. List of classifications 1–123: Accessed 25 Mar 2019
  26. Inácio M, Pereira V, Pinto M (2008) The Soil Geochemical Atlas of Portugal: Overview and applications. J Geochem Explor 98(1–2):22–33CrossRefGoogle Scholar
  27. Inácio M, Ferreira E, Pereira V (2010) Heavy metals contamination in sandy soils, forage plants and groundwater surrounding an industrial emission source (Estarreja, Portugal). In: Proceedings of 15th International Conference on Heavy Metals in the Environment, Poland pp 856–859Google Scholar
  28. Inácio M, Ferreira E, Pereira V (2011) Mobility and bioavailability of some potentially harmful elements around an industrial contaminated environment (Estarreja, Portugal). Mineral Magaz 75(3):1083Google Scholar
  29. Inácio M, Neves O, Pereira V, Ferreira da Silva E (2014) Levels of selected potential harmful elements (PHEs) in soils and vegetables used in diet of the population living in the surroundings of the Estarreja Chemical Complex (Portugal). Appl Geochem 44:38–44CrossRefGoogle Scholar
  30. INE (2015) Statistics Portugal. XV Ressenciamento Geral da População, CENSUS 2001.
  31. JECFA (2011). Evaluation of Certain Contaminants in Food. The seventy-second report of Joint FAO/WHO Expert Committee on Food Additives. WHO technical report series no 959, pp 1–115Google Scholar
  32. Kabata Pendias A (2011) Trace Elements in Soils and Plants, 4th edn. CRC Press, New YorkGoogle Scholar
  33. Khalique A, Ahmad S, Anjum T, Jaffar M, Shah MH, Shaheen N, Manzoor S (2005) A comparative study based on gender and age dependence of selected metals in scalp hair. Environ Monit Assess 104(1–3):45–57CrossRefGoogle Scholar
  34. Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG (2008) Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ Pollut 152:686–692CrossRefGoogle Scholar
  35. Li F, Qiu ZZ, Zhang J, Liu W, Liu C, Zeng GM (2017) Investigation, pollution mapping and simulative leakage health risk assessment for heavy metals and metalloids in groundwater from a typical brownfield, middle China. Int J Environ Res Public Health 14:768CrossRefGoogle Scholar
  36. Mikulewicz M, Chojnacka K, Gedrange T, Górecki H (2013) Reference values of elements in human hair: a systematic review. Environ Toxicol Pharmacol 36(3):1077–1086CrossRefGoogle Scholar
  37. Ministry of Health of the People’s Republic of China (2005) the maximum levels of contaminants in foods (GB 2762-2005). Maximum Levels of Contaminants in Foods _Beijing_China—Peoples Republic of_12-11-2014.pdf. Accessed 11 Apr 2019Google Scholar
  38. Mohmand J, Eqani SA, Fasola M, Alamdar A, Mustafa I, Ali N, Shen H (2015) Human exposure to toxic metals via contaminated dust: bio-accumulation trends and their potential risk estimation. Chemosphere 132:142–151CrossRefGoogle Scholar
  39. Mortada WI, Sobh MA, El-Defrawy MM, Farahat SE (2002) Reference intervals of cadmium, lead, and mercury in blood, urine, hair, and nails among residents in Mansoura city, Nile delta, Egypt. Environ Res 90(2):104–110CrossRefGoogle Scholar
  40. Morton J, Mason HJ, Ritchie KA, White M (2004) Comparison of hair, nails and urine for biological monitoring of low level inorganic mercury exposure in dental workers. Biomarkers 9(1):47–55CrossRefGoogle Scholar
  41. Neves O, Inácio M, Pereira V (2016) Contribution of consumed vegetables to human dietary intake of As, Hg, Pb Cd, Cu, and Zn in Estarreja urban area Food Contaminants: challenges in chemical mixtures. National Institute of Health Dr. Ricardo Jorge 978-989-8794-20-8Google Scholar
  42. Ordens CM (2007a) Estudo da contaminação do aquífero superior na região de Estarreja. Unpublished M.Sc. thesis. Coimbra University. Accessed 11 Mar 2015
  43. Ordens CM, Condesso de Melo MT, Grangeia C, Marques da Silva MA (2007b) Groundwater—surface water interactions near a Chemical Complex (Estarreja, Portugal)—Implications on groundwater quality. In: Proceedings 35th Congress of the International Association of Hydrogeologists, Lisbon, Portugal, 17–21 SeptemberGoogle Scholar
  44. Pais I, Jones JB Jr (2000) Trace elements in soils and plants. St Lucie Press, Delray Beach, p 223Google Scholar
  45. Patinha C, Reis AP, Dias AC, Abduljelil AA, Noack Y, Robert S, Ferreira Cave M, da Silva EF (2015) The mobility and human oral bioaccessibility of Zn and Pb in urban dusts of Estarreja (N Portugal). Environ Geochem Health 37(1):115–131CrossRefGoogle Scholar
  46. Pereira ME, Lillebø AI, Pato P, Válega M, Coelho JP, Lopes C et al (2009) Mercury pollution in Ria de Aveiro (Portugal): a review of the system assessment. Environ Monit Assess 155:39–49CrossRefGoogle Scholar
  47. Pietrzykowski M, Krzaklewski W (2007) Soil organic matter, C and N accumulation during natural succession and reclamation in an opencast sand quarry (southern Poland). Arch Agron Soil Sci 53:473–483CrossRefGoogle Scholar
  48. Radwan MA, Salama AK (2006) Market basket survey for some heavy metals in Egyptian fruits and vegetables. Food Chem Toxicol 44:1273–1278CrossRefGoogle Scholar
  49. Reis AP, Costa S, Santos I, Patinha C, Noack Y, Wragg J et al (2015) Investigating relationships between biomarkers of exposure and environmental copper and manganese levels in house dusts from a Portuguese industrial city. Environ Geochem Health 37(4):725–744CrossRefGoogle Scholar
  50. Rodushkin I, Axelsson MD (2000) Application of double focusing sector field ICP-MS for multielemental characterization of human hair and nails. Part II. A study of the inhabitants of northern Sweden. Sci Total Environ 262(1–2):21–36CrossRefGoogle Scholar
  51. Rodushkin I, Axelsson MD (2003) Application of double focusing sector field ICP-MS for multielemental characterization of human hair and nails. Part III. Direct analysis by laser ablation. Sci Total Environ 305(1–3):23–39CrossRefGoogle Scholar
  52. Salgueiro AR, Inácio M, Pereira HG, Ferreira da Silva E, Pereira V (2013) Multivariate data analysis as a tool for characterize children and family diet habits typology in an industrial and rural area: preliminary results. 5th International Conference on Medical Geology. MEDGEO, 2nd Symposium on Advances in Geospatial Technologies for Health. Arlington, Virginia, USA. Book of Abstracts p 27Google Scholar
  53. Slotnick MJ, Nriagu JO (2006) Validity of human nails as a biomarker of arsenic and selenium exposure: a review. Environ Res 102(1):125–139CrossRefGoogle Scholar
  54. Srivastav A, Yadav KK, Yadav S, Gupta N, Singh JK, Katiyar R, Kumar V (2018) Nano-phytoremediation of pollutants from contaminated soil environment: current scenario and future prospects. In: Phytoremediation. Springer, Cham, pp 383-401Google Scholar
  55. Sthiannopkao S, Kim KW, Cho KH, Wantala K, Sotham S, Sokuntheara C, Kim JH (2010) Arsenic levels in human hair, Kandal Province, Cambodia: the influences of groundwater arsenic, consumption period, age and gender. Appl Geochem 25(1):81–90CrossRefGoogle Scholar
  56. Sun JB, Czerkinsky C, Holmgren J (2010) Mucosally induced immunological tolerance, regulatory T cells and the adjuvant effect by cholera toxin B subunit. Scand J Immunol 71(1):1–11CrossRefGoogle Scholar
  57. Tepanosyan G, Maghakyan N, Sahakyan L, Saghatelyan A (2017) Heavy metals pollution levels and children health risk assessment of Yerevan kindergartens soils. Ecotoxicol Environ Saf 142:257–265CrossRefGoogle Scholar
  58. USDE US (2013) Department of Energy. The Risk Assessment Information System (RAIS). U.S. Department of Energy’s Oak Ridge Operations Office: Oak Ridge, TN, USA, 2013. Accessed 6 Sep 2018
  59. USEPA (2001) United States Environmental Protection Agency. Risk assessment guidance for superfund: volume III–part A, process for conducting probabilistic risk assessment; EPA 540-R-02-002. 2001. Accessed 4 Jan 2018
  60. USEPA (2011) United States Environmental Protection Agency. Exposure factors handbook 2011 edition (Final). Consulted in April 2016 in:
  61. Utell MJ, Frampton MW (2000) Acute health effects of ambient air pollution: the ultrafine particle hypothesis. J Aerosol Med 13(4):355–359CrossRefGoogle Scholar
  62. Van der Weijden C, Pacheco FAL (2006) Hydrogeochemistry in the Vouga River basin (central Portugal): pollution and chemical weathering. Appl Geochem 21:580–613CrossRefGoogle Scholar
  63. WHO (2015) Human biomonitoring: facts and figures. Accessed 1 Sep 2018
  64. Wilhelm M, Pesch A, Rostek U, Begerow J, Schmitz N, Idel H, Ranft U (2002) Concentrations of lead in blood, hair and saliva of German children living in three different areas of traffic density. Sci Total Environ 297(1–3):109–118CrossRefGoogle Scholar
  65. WRB (2006) World Reference Base for Soil Resources 2006. World Soil Resources Reports No. 103. FAO, RomeGoogle Scholar
  66. Wright JW, Davies KF, Lau JA, McCall AC, McKay JK (2006) Experimental verification of ecological niche modeling in a heterogeneous environment. Ecology 87(10):2433–2439CrossRefGoogle Scholar
  67. Wu B, Chen T (2010) Changes in hair arsenic concentration in a population exposed to heavy pollution: follow-up investigation in Chenzhou City, Hunan Province, Southern China. J Environ Sci 22(2):283–289CrossRefGoogle Scholar
  68. Wu S, Powers S, Zhu W, Hannun YA (2016) Substantial contribution of extrinsic risk factors to cancer development. Nature 529(7584):43CrossRefGoogle Scholar
  69. Xiang HL, Yang J, Qiu ZZ, Lei WX, Zeng TT, Lan ZC (2015) Health risk assessment of tunnel workers based on the investigation and analysis of occupational exposure to PM10. Environ Sci 36:2768–2774Google Scholar
  70. Xiao R, Wang S, Li R, Wang JJ, Zhang Z (2017) Soil heavy metal contamination and health risks associated with artisanal gold mining in Tongguan, Shaanxi, China. Ecotoxicol Environ Saf 141:17–24CrossRefGoogle Scholar
  71. Xie T, Liu X, Sun T (2011) The effects of groundwater table and flood irrigation strategies on soil water and salt dynamics and reed water use in the Yellow River Delta, China. Ecol Model 222(2):241–252CrossRefGoogle Scholar
  72. Yadav KK, Gupta N, Kumar V, Singh JK (2017) Bioremediation of heavy metals from contaminated sites using potential species. A review. Indian J Environ Prot 37(1):65Google Scholar
  73. Yadav KK, Gupta N, Kumar A, Reece LM, Singh N, Rezania S, Khan SA (2018a) Mechanistic understanding and holistic approach of phytoremediation: a review on application and future prospects. Ecol Eng 120:274–298CrossRefGoogle Scholar
  74. Yadav KK, Gupta N, Kumar V, Choudhary P, Khan SA (2018b) GIS-based evaluation of groundwater geochemistry and statistical determination of the fate of contaminants in shallow aquifers from different functional areas of Agra city, India: levels and spatial distributions. RSC Adv 8(29):15876–15889CrossRefGoogle Scholar
  75. Zhuang P, Zou B, Li NY, Li ZA (2009) Heavy metal contamination in soils and food crops around Dabaoshan. Environ Geochem Health 31(6):707–715CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Geobiotec, University of AveiroAveiroPortugal
  2. 2.CERENA, DECivil, Instituto Superior TécnicoUniversity of LisbonLisbonPortugal
  3. 3.LAQV/REQUIMTE, Department of Chemical Sciences, Laboratory of Applied Chemistry, Faculty of PharmacyUniversity of PortoPortoPortugal
  4. 4.Faculty of MedicineUniversity of CoimbraCoimbraPortugal

Personalised recommendations