Foliar uptake of arsenic nanoparticles by spinach: an assessment of physiological and human health risk implications

  • Natasha
  • Muhammad ShahidEmail author
  • Camille Dumat
  • Sana Khalid
  • Faiz Rabbani
  • Abu Bakr Umer Farooq
  • Muhammad Amjad
  • Ghulam Abbas
  • Nabeel Khan Niazi
Sustainable Urban Agriculture: Vector for Ecological Transition


Atmospheric contamination by heavy metal(loid)–enriched particulate matter (metal-PM) is highly topical these days because of its high persistence, toxic nature, and health risks. Globally, foliar uptake of metal(loid)s occurs for vegetables/crops grown in the vicinity of industrial or urban areas with a metal-PM-contaminated atmosphere. The current study evaluated the foliar uptake of arsenic (As), accumulation of As in different plant organs, its toxicity (in terms of ROS generation, chlorophyll degradation, and lipid peroxidation), and its defensive mechanism (antioxidant enzymes) in spinach (Spinacia oleracea) after foliar application of As in the form of nanoparticles (As-NPs). The As-NPs were prepared using a chemical method. Results indicate that spinach can absorb As via foliar pathways (0.50 to 0.73 mg/kg in leaves) and can translocate it towards root tissues (0.35 to 0.68 mg/kg). However, health risk assessment parameters showed that the As level in the edible parts of spinach was below the critical limit (hazard quotient < 1). Despite low tissue level, As-NP exposure caused phytotoxicity in terms of a decrease in plant dry biomass (up to 84%) and pigment contents (up to 38%). Furthermore, several-fold higher activities of antioxidant enzymes were observed under metal stress than control. However, no significant variation was observed in the level of hydrogen peroxide (H2O2), which can be its possible transformation to other forms of reactive oxygen species (ROS). It is proposed that As can be absorbed by spinach via foliar pathway and then disturbs the plant metabolism. Therefore, air quality needs to be considered and monitored continuously for the human health risk assessment and quality of vegetables cultivated on polluted soils (roadside and industrial vicinity).

Graphical abstract


Arsenic Nanoparticles Foliar application Spinach Oxidative stress 

Supplementary material

11356_2018_3867_MOESM1_ESM.docx (56 kb)
ESM 1 (DOCX 56 kb)


  1. Abbas G, Murtaza B, Bibi I, Shahid M, Niazi N, Khan M, Amjad M, Hussain M, Natasha (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59CrossRefGoogle Scholar
  2. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  3. Bakhat HF, Zia Z, Fahad S, Abbas S, Hammad HM, Shahzad AN, Abbas F, Alharby H, Shahid M (2017) Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ Sci Pollut Res 24:9142–9158CrossRefGoogle Scholar
  4. Bondada BR, Tu S, Ma LQ (2004) Absorption of foliar-applied arsenic by the arsenic hyperaccumulating fern (Pteris vittata L.). Sci Total Environ 332:61–70CrossRefGoogle Scholar
  5. Carey A-M, Scheckel KG, Lombi E, Newville M, Choi Y, Norton GJ, Charnock JM, Feldmann J, Price AH, Meharg AA (2010) Grain unloading of arsenic species in rice. Plant Physiol 152:309–319CrossRefGoogle Scholar
  6. Colle C, Madoz-Escande C, Leclerc E (2009) Foliar transfer into the biosphere: review of translocation factors to cereal grains. J Environ Radioact 100:683–689CrossRefGoogle Scholar
  7. Corrêa AX, Testolin RC, Torres MM, Cotelle S, Schwartz J-J, Millet M, Radetski CM (2017) Ecotoxicity assessment of particulate matter emitted from heavy-duty diesel-powered vehicles: influence of leaching conditions. Environ Sci Pollut Res 24:9399–9406CrossRefGoogle Scholar
  8. Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101CrossRefGoogle Scholar
  9. Di Vaio P, Magli E, Caliendo G, Corvino A, Fiorino F, Frecentese F, Saccone I, Santagada V, Severino B, Onorati G (2018) Heavy metals size distribution in PM10 and environmental-sanitary risk analysis in Acerra (Italy). Atmosphere 9:58CrossRefGoogle Scholar
  10. Dollard G (1986) Glasshouse experiments on the uptake of foliar applied lead. Environmental Pollution Series A, Ecological and Biological 40:109–119CrossRefGoogle Scholar
  11. Douay F, Pruvot C, Waterlot C, Fritsch C, Fourrier H, Loriette A, Bidar G, Grand C, De Vaufleury A, Scheifler R (2009) Contamination of woody habitat soils around a former lead smelter in the North of France. Sci Total Environ 407:5564–5577CrossRefGoogle Scholar
  12. Facts, G., 2008. Facts on health and the environment. Obtained of Facts on health and the environment: http://www. greenfacts. org/es/cambio-climatico-ie5-base-cienc ia/. Accessed on. 2.Google Scholar
  13. Fritsch C, Giraudoux P, Cœurdassier M, Douay F, Raoul F, Pruvot C, Waterlot C, De Vaufleury A, Scheifler R (2010) Spatial distribution of metals in smelter-impacted soils of woody habitats: influence of landscape and soil properties, and risk for wildlife. Chemosphere 81:141–155CrossRefGoogle Scholar
  14. Goix S, Lévêque T, Xiong T-T, Schreck E, Baeza-Squiban A, Geret F, Uzu G, Austruy A, Dumat C (2014) Environmental and health impacts of fine and ultrafine metallic particles: assessment of threat scores. Environ Res 133:185–194CrossRefGoogle Scholar
  15. Golob A, Kavčič J, Stibilj V, Gaberščik A, Vogel-Mikuš K, Germ M (2017) The effect of selenium and UV radiation on leaf traits and biomass production in Triticum aestivum L. Ecotoxicol Environ Saf 136:142–149CrossRefGoogle Scholar
  16. Hemeda HM, Klein B (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185CrossRefGoogle Scholar
  17. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611CrossRefGoogle Scholar
  18. Kermani M, Farzadkia M, Kalantari RR, Bahmani Z (2018) Fine particulate matter (PM 2.5) in a compost facility: heavy metal contaminations and health risk assessment, Tehran, Iran. Environ Sci Pollut Res:1–11Google Scholar
  19. Khalid S, Shahid M, Dumat C, Niazi NK, Bibi I, Gul Bakhat HFS, Abbas G, Murtaza B, Javeed HMR (2017a) Influence of groundwater and wastewater irrigation on lead accumulation in soil and vegetables: implications for health risk assessment and phytoremediation. International Journal of Phytoremediation 19:1037–1046CrossRefGoogle Scholar
  20. Khalid, S., Shahid, M., Niazi, N. K., Rafiq, M., Bakhat, H. F., Imran, M., Abbas, T., Bibi, I., Dumat, C., 2017b Arsenic behaviour in soil-plant system: biogeochemical reactions and chemical speciation influences. Enhancing Cleanup of Environmental Pollutants: Non Biological Approaches. Springer, N. Anjum et al. (eds.), .Google Scholar
  21. Kováčik J, Klejdus B, Štork F, Hedbavny J (2012) Physiological responses of Tillandsia albida (Bromeliaceae) to long-term foliar metal application. J Hazard Mater 239:175–182CrossRefGoogle Scholar
  22. Lerner JEC, Elordi ML, Orte MA, Giuliani D, de los Angeles Gutierrez M, Sanchez E, Sambeth JE, Porta AA (2018) Exposure and risk analysis to particulate matter, metals, and polycyclic aromatic hydrocarbon at different workplaces in Argentina. Environ Sci Pollut Res:1–10Google Scholar
  23. Lichtenthaler, H. K., 1987 [34] Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Plant Cell Membranes. Academic Press, , pp. 350-382.Google Scholar
  24. Liu W, Wu Y, Wang C, Li HC, Wang T, Liao CY, Cui L, Zhou QF, Yan B, Jiang GB (2010) Impact of silver nanoparticles on human cells: effect of particle size. Nanotoxicology 4:319–330CrossRefGoogle Scholar
  25. Liu K, Shang Q, Wan C, Song P, Ma C, Cao L (2017) Characteristics and sources of heavy metals in PM2. 5 during a typical haze episode in rural and urban areas in Taiyuan, China. Atmosphere 9:2CrossRefGoogle Scholar
  26. Manaf HH (2016) Beneficial effects of exogenous selenium, glycine betaine and seaweed extract on salt stressed cowpea plant. Ann Agric Sci 61:41–48Google Scholar
  27. Mohan, T. C., Castrillo, G., Navarro, C., Zarco-Fernández, S., Ramireddy, E., Mateo, C., Zamarreño, A. M., Paz-Ares, J., Muñoz, R., Garcia-Mina, J. M., 2016. Cytokinin determines thiol-mediated arsenic tolerance and accumulation in Arabidopsis thaliana. Plant physiology. pp. 00372.2016.Google Scholar
  28. Mukherjee, A., Agrawal, M., 2017 A global perspective of fine particulate matter pollution and its health effects. Reviews of Environmental Contamination and Toxicology Volume 244. Springer, pp. 5-51.Google Scholar
  29. Niazi NK, Bibi I, Shahid M, Ok YS, Burton ED, Wang H, Shaheen SM, Rinklebe J, Lüttge A (2018a) Arsenic removal by perilla leaf biochar in aqueous solutions and groundwater: an integrated spectroscopic and microscopic examination. Environ Pollut 232:31–41CrossRefGoogle Scholar
  30. Niazi NK, Bibi I, Shahid M, Ok YS, Shaheen SM, Rinklebe J, Wang H, Murtaza B, Islam E, Nawaz MF (2018b) Arsenic removal by Japanese oak wood biochar in aqueous solutions and well water: investigating arsenic fate using integrated spectroscopic and microscopic techniques. Sci Total Environ 621:1642–1651CrossRefGoogle Scholar
  31. Pal A, Saha S, Maji SK, Kundu M, Kundu A (2012) Wet-chemical synthesis of spherical arsenic nanoparticles by a simple reduction method and its characterization. Adv Mater Lett 3:177–180CrossRefGoogle Scholar
  32. Rafiq M, Shahid M, Abbas G, Shamshad S, Khalid S, Niazi NK, Dumat C (2017a) Comparative effect of calcium and EDTA on arsenic uptake and physiological attributes of Pisum sativum. International Journal of Phytoremediation. 19:662–669CrossRefGoogle Scholar
  33. Rafiq M, Shahid M, Shamshad S, Khalid S, Niazi NK, Abbas G, Saeed MF, Ali M, Murtaza B (2017b) A comparative study to evaluate efficiency of EDTA and calcium in alleviating arsenic toxicity to germinating and young Vicia faba L. seedlings. Journal of Soils and Sediments:1–11Google Scholar
  34. Rehman ZU, Khan S, Qin K, Brusseau ML, Shah MT, Din I (2016) Quantification of inorganic arsenic exposure and cancer risk via consumption of vegetables in southern selected districts of Pakistan. Sci Total Environ 550:321–329CrossRefGoogle Scholar
  35. Sachs R, Michael J (1971) Comparative phytotoxicity among four arsenical herbicides. Weed Sci:558–564Google Scholar
  36. Schreck E, Foucault Y, Sarret G, Sobanska S, Cécillon L, Castrec-Rouelle M, Uzu G, Dumat C (2012) Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: mechanisms involved for lead. Sci Total Environ 427-428:253–262CrossRefGoogle Scholar
  37. Schreck, E., Laplanche, C., Le Guédard, M., Bessoule, J.-J., Austruy, A., Xiong, T., Foucault, Y., Dumat, C., 2013. Influence of fine process particles enriched with metals and metalloids on Lactuca sativa L. leaf fatty acid composition following air and/or soil-plant field exposure. Environmental pollution (Barking, Essex: 1987). 179, 242-249.Google Scholar
  38. Schreck E, Dappe V, Sarret G, Sobanska S, Nowak D, Nowak J, Stefaniak EA, Magnin V, Ranieri V, Dumat C (2014) Foliar or root exposures to smelter particles: consequences for lead compartmentalization and speciation in plant leaves. Sci Total Environ 476-477:667–676CrossRefGoogle Scholar
  39. Shahid M, Dumat C, Khalid S, Schreck E, Xiong T, Niazi NK (2017a) Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake. J Hazard Mater 325:36–58CrossRefGoogle Scholar
  40. Shahid, M., Khalid, M., Dumat, C., Khalid, S., Niazi, N. K., Imran, M., Bibi, I., Ahmad, I., Hammad, H. M., Tabassum, R. A., 2017b. Arsenic level and risk assessment of groundwater in Vehari, Punjab Province, Pakistan. Exposure and Health. 1-11.Google Scholar
  41. Shahid, M., Rafiq, M., Niazi, N. K., Dumat, C., Shamshad, S., Khalid, S., Bibi, I., 2017c. Arsenic accumulation and physiological attributes of spinach in the presence of amendments: an implication to reduce health risk. Environ Sci Pollut Res 24, 16,097-16,106.Google Scholar
  42. Shahid M, Niazi NK, Dumat C, Naidu R, Khalid S, Rahman MM, Bibi I (2018) A meta-analysis of the distribution, sources and health risks of arsenic-contaminated groundwater in Pakistan. Environ PollutGoogle Scholar
  43. Shakoor MB, Bibi I, Niazi NK, Shahid M, Nawaz MF, Farooqi A, Naidu R, Rahman MM, Murtaza G, Lüttge A (2018a) The evaluation of arsenic contamination potential, speciation and hydrogeochemical behaviour in aquifers of Punjab, Pakistan. Chemosphere 199:737–746CrossRefGoogle Scholar
  44. Shakoor MB, Niazi NK, Bibi I, Shahid M, Sharif F, Bashir S, Shaheen SM, Wang H, Tsang DC, Ok YS (2018b) Arsenic removal by natural and chemically modified water melon rind in aqueous solutions and groundwater. Sci Total Environ 645:1444–1455CrossRefGoogle Scholar
  45. Shamshad S, Shahid M, Rafiq M, Khalid S, Dumat C, Sabir M, Murtaza B, Farooq ABU, Shah NS (2018) Effect of organic amendments on cadmium stress to pea: a multivariate comparison of germinating vs young seedlings and younger vs older leaves. Ecotoxicol Environ Saf 151:91–97CrossRefGoogle Scholar
  46. Shigeta T (2000) Environmental investigation in Pakistan. Pak-EPA/JICA, IslamabadGoogle Scholar
  47. Suriyagoda LD, Dittert K, Lambers H (2018) Mechanism of arsenic uptake, translocation and plant resistance to accumulate arsenic in rice grains. Agric Ecosyst Environ 253:23–37CrossRefGoogle Scholar
  48. Tabassum RA, Shahid M, Dumat C, Niazi NK, Khalid S, Shah NS, Imran M, Khalid S (2018) Health risk assessment of drinking arsenic-containing groundwater in Hasilpur, Pakistan: effect of sampling area, depth, and source. Environ Sci Pollut Res:1–12Google Scholar
  49. Tiwari S, Sarangi BK (2017) Comparative analysis of antioxidant response by Pteris vittata and Vetiveria zizanioides towards arsenic stress. Ecol Eng 100:211–218CrossRefGoogle Scholar
  50. Uzu G, Sobanska S, Aliouane Y, Pradere P, Dumat C (2009) Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation. Environ Pollut 157:1178–1185CrossRefGoogle Scholar
  51. Uzu G, Sobanska S, Sarret G, Muñoz M, Dumat C (2010) Foliar lead uptake by lettuce exposed to atmospheric fallouts. Environ Sci Technol 44:1036–1042CrossRefGoogle Scholar
  52. Uzu G, Sauvain JJ, Baeza-Squiban A, Riediker M, Hohl MS, Val S, Tack K, Denys S, Pradere P, Dumat C (2011) In vitro assessment of the pulmonary toxicity and gastric availability of lead-rich particles from a lead recycling plant. Environ Sci Technol 45:7888–7895CrossRefGoogle Scholar
  53. Wang J, Liu G, Wu H, Zhang T, Liu X, Li W (2018) Temporal-spatial variation and partitioning of dissolved and particulate heavy metal (loid) s in a river affected by mining activities in Southern China. Environ Sci Pollut Res:1–12Google Scholar
  54. Xiong T, Leveque T, Shahid M, Foucault Y, Mombo S, Dumat C (2014) Lead and cadmium phytoavailability and human bioaccessibility for vegetables exposed to soil or atmospheric pollution by process ultrafine particles. J Environ Qual 43:1593–1600CrossRefGoogle Scholar
  55. Xiong T, Austruy A, Pierart A, Shahid M, Schreck E, Mombo S, Dumat C (2016a) Kinetic study of phytotoxicity induced by foliar lead uptake for vegetables exposed to fine particles and implications for sustainable urban agriculture. J Environ Sci 46:16–27CrossRefGoogle Scholar
  56. Xiong T, Dumat C, Pierart A, Shahid M, Kang Y, Li N, Bertoni G, Laplanche C (2016b) Measurement of metal bioaccessibility in vegetables to improve human exposure assessments: field study of soil–plant–atmosphere transfers in urban areas, South China. Environmental Geochemistry and Health 38:1283–1301CrossRefGoogle Scholar
  57. Xiong T, Dumat C, Dappe V, Vezin H, Schreck E, Shahid M, Pierart A, Sobanska S (2017) Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture. Environ Sci Technol 51:5242–5251CrossRefGoogle Scholar
  58. Xiong, T., Zhang, T., Dumat, C., Sobanska, S., Dappe, V., Shahid, M., Xian, Y., Li, X., Li, S., 2018. Airborne foliar transfer of particular metals in Lactuca sativa L.: translocation, phytotoxicity, and bioaccessibility. Environmental Science and Pollution Research. Scholar
  59. Xu H, Han S, Bi X, Zhao Z, Zhang L, Yang W, Zhang M, Chen J, Wu J, Zhang Y (2016) Atmospheric metallic and arsenic pollution at an offshore drilling platform in the Bo Sea: a health risk assessment for the workers. J Hazard Mater 304:93–102CrossRefGoogle Scholar
  60. Zandstra B, De Kryger T (2007) Arsenic and lead residues in carrots from foliar applications of monosodium methanearsonate (MSMA): a comparison between mineral and organic soils, or from soil residues. Food Addit Contam 24:34–42CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Natasha
    • 1
  • Muhammad Shahid
    • 1
    Email author
  • Camille Dumat
    • 2
  • Sana Khalid
    • 1
  • Faiz Rabbani
    • 1
  • Abu Bakr Umer Farooq
    • 1
  • Muhammad Amjad
    • 1
  • Ghulam Abbas
    • 1
  • Nabeel Khan Niazi
    • 3
    • 4
  1. 1.Department of Environmental SciencesCOMSATS University Islamabad, Vehari campusVehariPakistan
  2. 2.Centre d’Etude et de Recherche Travail Organisation Pouvoir (CERTOP), UMR5044Université J. Jaurès - Toulouse IIToulouse Cedex 9France
  3. 3.Institute of Soil and Environmental SciencesUniversity of Agriculture FaisalabadFaisalabadPakistan
  4. 4.School of Civil Engineering and SurveyingUniversity of Southern QueenslandToowoombaAustralia

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