Health assessment of medicinal herbs, celery and parsley related to cadmium soil pollution-potentially toxic elements (PTEs) accumulation, tolerance capacity and antioxidative response

Abstract

Celery and parsley are recognized as medicinal herbs and nutraceutical vegetables due to their valuable pharmacological properties and numerous health benefits. However, in recent years, soil loadings with various PTEs have become a serious concern across the world, leading to plants pollution, which can consequently diminish their quality and safety for human consumption. Therefore, we attempted to quantify quality and safety of celery and parsley grown in Cd polluted soil. We examined the presence of PTEs: As, Cu, Fe, Mn, Ni, Cu and Cd in soil and selected herbs, as well as their physiological responses to different Cd exposures (control–without Cd addition, 3 and 6 µg/g Cd of dry soil). Following elevation of Cd in plants, both species showed increasing trend of As, Pb and Cu in plants, which overcome safe limits, with exception for Cu. Further, celery showed strong phytoextraction ability (99.9 µg/g Cd of dry weight) with high potential to tolerate Cd due to the efficient antioxidative machinery. Besides that herbs pollution was evident on the basis of target hazard quotients (HQ), hazard index (HI) and cancerogenic risk (CR), revealing that chronic consumption of contaminated herbs can consequently endanger human health. HI was greater than 1, while CR exceeded safe limits in treated plants, with exception for As. In the point of view of toxicology and food safety, growing of medicinal plants should be strictly regulated and distinguished based on the purpose of growing, and further herbs usage.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abbott, J. (1999). Quality measurements of fruit and vegetables. Postharvest Biology and Technology, 15(3), 207–225.

    Article  Google Scholar 

  2. Adimalla, N., Chen, J., & Qian, H. (2020). Spatial characteristics of heavy metal contamination and potential human health risk assessment of urban soils: A case study from an urban region of South India. Ecotoxicology and Environmenatal Safety, 194, 110406.

    CAS  Article  Google Scholar 

  3. Aebi, H. (1984). Catalase in vitro. Methods in Enzymology, 105, 121–126.

    CAS  Article  Google Scholar 

  4. ATSDR (2012). Agency for toxic substances and disease registry, Toxicological Profile for Cadmium, U.S. Department of Health and Human Services, Public Health Service. https://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=48&tid=15. Retrived July 12, 2020.

  5. Bates, I. S., Waldrn, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water stress. Plant and Soil, 39(1), 205–207.

    CAS  Article  Google Scholar 

  6. Bibi, A., Farooq, U., Naz, S., Khan, A., Khan, K., Sarwar, K., et al. (2016). Phytoextraction of Hg by parsley (Petroselinum crispum) and its growth responses. International Journal of Phytoremediation, 18(4), 354–357.

    CAS  Article  Google Scholar 

  7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    CAS  Article  Google Scholar 

  8. Chen, F., Wang, Q., Meng, F., Chen, M., & Wang, B. (2020). Effects of long-term zinc smelting activities on the distribution and health risk of heavy metals in agricultural soils of Guizhou province China. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-020-00716-x.

    Article  Google Scholar 

  9. Codex Alimentarius Commission of FAO/WHO. (2001). Food additives and contaminants joint FAO/WHO food standards programme. ALINORM, 01(12A), 1–289.

    Google Scholar 

  10. Ćwieląg-Drabek, M., Piekut, A., Gut, K., & Grabowski, M. (2020). Risk of cadmium, lead and zinc exposure from consumption of vegetables produced in areas with mining and smelting past. Scientific Reports, 10, 3363.

    Article  CAS  Google Scholar 

  11. Dogra, N., Sharma, M., Sharma, A., Keshavarzi, A., MinakshiBhardwaj, A. R., Thukral, A. K., & Kumar, V. (2020). Pollution assessment and spatial distribution of roadside agricultural soils: A case study from India. International Journal of Environmental Research and Public Health, 30(2), 146–159.

    Article  CAS  Google Scholar 

  12. Eid, E. M., Alrumman, S. A., Galal, T. M., & El-Beban, A. F. (2019). Regression models for monitoring trace metal accumulations by Faba sativa Bernh, plants grown in soils amended with different rates of sewage sludge. Scientific Reports, 9, 5443.

    Article  CAS  Google Scholar 

  13. Farzaei, M. H., Abbasabadi, Z., Ardekani, M. R. S., Rahimi, R., & Farzaei, F. (2013). Parsley: A review of ethnopharmacology phytochemistry and biological activities. Journal of Traditional Chinese Medicine, 33(6), 815–826.

    Article  Google Scholar 

  14. Feng, W., Guo, Z., Xiao, X., Peng, C., Shi, L., Ran, L., & Xu, W. (2020). A dynamic model to evaluate the critical loads of heavy metals in agricultural soil. Ecotoxicology and Environmental Safety, 197, 110607.

    CAS  Article  Google Scholar 

  15. Filipiak-Szok, A., Kurzawa, M., &  Szłyk, Е. (2015). Determination of toxic metals by ICP-MS in аsiatic and еuropean medicinal plants and dietary supplements. Journal of Trace Elements in Medicine and Biology, 30, 54–58.

  16. Gebeyehu, H. R., & Bayissa, L. D. (2020). Levels of heavy metals in soil and vegetables and associated health risks in Mojo area. Ethiopia. PLoS ONE, 15(1), e0227883.

    CAS  Article  Google Scholar 

  17. Gerasimova, N. G., Pridvorova, S. M., & Ozeretskovskaza, O. I. (2005). Role of L-phenylalanine ammonia lyase in the induced resistance and susceptibility of potato plants. Prikladnaya Biokhimiya i Mikrobiologiya, 41(1), 117–120.

    CAS  Google Scholar 

  18. Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909–930.

    CAS  Article  Google Scholar 

  19. Golubkina, N. A., Kharchenko, V. A., Moldovan, A. I., Koshevarov, A. A., Zamana, S., Nadezhkin, S., et al. (2020). Yield, growth, quality, biochemical characteristics and elemental composition of plant parts of celery leafy, stalk and root types grown in the northern hemisphere. Plants, 9(4), 484.

    CAS  Article  Google Scholar 

  20. Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249, 7130–7139.

    CAS  Article  Google Scholar 

  21. Han, L., Gao, X., Xia, T., Zhang, X., Li, X., & Gao, W. (2019). Effect of digestion on the phenolic content and antioxidant activity of celery leaf and the antioxidant mechanism via Nrf2/HO-1 signaling pathways against dexamethasone. Journal of Food Biochemistry. https://doi.org/10.1111/jfbc.12875.

    Article  Google Scholar 

  22. Harmanescu, M., Alda, L. A., Bordean, D. M., Gogoasa, I., & Gerge, I. (2011). Heavy metals health risk assessment for population via consumption of vegetables grown in old mining area; A case study: Banat County. Romania. Chemistry Central Journal, 5, 64.

    CAS  Article  Google Scholar 

  23. Hu, W., Huang, B., Tian, K., Holm, P. E., & Zhang, Y. (2017). Heavy metals in intensive greenhouse vegetable production systems along Yellow Sea of China: Levels, transfer and health risk. Chemosphere, 167, 82–90.

    CAS  Article  Google Scholar 

  24. Huang, Y., Chen, Q., Deng, M., Japenga, J., Li, T., Yang, X., & He, Z. (2018). Heavy metal pollution and health risk assessment of agricultural soils in a typical peri-urban area in southeast China. Journal of Environmental Planning and Management, 207, 159–168.

    CAS  Google Scholar 

  25. Huang, Y., He, C., Shen, C., Guo, J., Mubeen, S., Yuan, J., & Yang, Z. (2017). Toxicity of cadmium and its health risks from leafy vegetable consumption. Food and Function, 8(4), 1373–1401.

    CAS  Article  Google Scholar 

  26. IARC (2020) International Agency for Cancer Research (IARC) monography on the identification of cancerogenic hazards for humans. https://monographs.iarc.fr/agents-classified-by-the-iarc/ Retrived December 7, 2020.

  27. Kapetanović, I. M., & Mieyal, I. I. (1979). Inhibition of acetaminophen induced hepatotoxicity by phenacetin and its alkoxyanalogs. Journal of Pharmacology and Experimental Therapeutics, 209, 25–30.

    Google Scholar 

  28. Karzan, A. M. H., Crout, N. M. J., Shaw, G., & Bailey, Е. H. (2020). Assessment of potentially toxic elements in vegetables cultivated in urban and peri-urban sites in the Kurdistan region of Iraq and implications for human health. Environmental Geochemistry and Health, 42(5),1359–1385.

  29. Kohzadi, S., Shahmoradi, B., Ghaderi, E., Loqmani, H., & Malek, A. (2019). Concentration, source, and potential human health risk of heavy metals in the commonly consumed medicinal plants. Biological Trace Element Research, 187, 41–50.

    CAS  Article  Google Scholar 

  30. Kočevar Glavač, N., Djogo, S., Ražić, S., Kreft, S., & Veber, M. (2017). Accumulation of heavy metals from soil in medicinal plants. Archives of Industrial Hygiene and Toxicology, 68, 236–244.

    Article  CAS  Google Scholar 

  31. Kumar, V., Pandita, S., Sharma, A., Bakshi, P., Sharma, P., Karaouzas, I., et al. (2019). Ecological and human health risks appraisal of metal (loid)s in agricultural soils a review. Geology, Ecology, and Landscapes. https://doi.org/10.1080/24749508.2019.1701310.

    Article  Google Scholar 

  32. Lajayer, B. A., Ghorbanpour, M., & Nikabadi, S. (2017). Heavy metals in contaminated environment: Destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicology and Environmental Safety, 145, 377–390.

    Article  CAS  Google Scholar 

  33. Li, X., Li, Z., Lin, C. J., Bie, X., Liu, J., Feng, X., et al. (2018). Health risks of heavy metal exposure through vegetable consumption near a large-scale Pb/Zn smelter in central China. Ecotoxicology and Environmental Safety, 161, 99–110.

    CAS  Article  Google Scholar 

  34. Liu, X., Song, Q., Tang, Y., Li, W., Xu, J., Wu, J., et al. (2013). Human health risk assessment of heavy metals in soil–vegetable system: A multi-medium analysis. Science of the Total Environment, 463–464, 530–540.

    Article  CAS  Google Scholar 

  35. Maleki, M., Ghorbanpour, M., & Kariman, K. (2017). Physiological and antioxidative responses of medicinal plants exposed to heavy metals stress. Plant Gene, 11, 247–254.

    CAS  Article  Google Scholar 

  36. Martirosya, M. D., Singharaj, B. (2016). Health claims and functional food: The future of functional foods under FDA and EFSA regulation. Functional foods for chronic diseases. First ed. pp. 410–424. Dalas, Texas, USA. Food Science Publisher.

  37. Michalak, A. (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies, 15(4), 523–530.

    CAS  Google Scholar 

  38. Mihailović, A., Budinski-Petković, L., Popov, S., Ninkov, J., Vasin, J., Ralević, N. M., & Vučinić Vasić, M. (2015). Spatial distribution of metals in urban soil of Novi Sad, Serbia: GIS based approach. Journal of Geochemical Exploration, 150, 104–114.

    Article  CAS  Google Scholar 

  39. Mongkhonsin, B., Nakbanpote, W., Meesungnoen, O., Prasad, M. N. V. (2019). Adaptive and tolerance mechanisms in herbaceous plants exposed to cadmium in: Hasanuzzaman, M., Prasad, M. N. V., Fujita, M. (Eds.), Cadmium Toxicity and Tolerance in Plants: From Physiology to Remediation, (pp 73–109), USA, Academic press, Elsevier Inc.

  40. Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters, 8, 199–216.

    CAS  Article  Google Scholar 

  41. Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22, 867–880.

    CAS  Google Scholar 

  42. Nworie, E. O., Qin, J., & Lin, C. (2019). Trace element uptake by herbaceous plants from the soils at a multiple trace element-contaminated site. Toxins., 7(1), 3.

    CAS  Google Scholar 

  43. Official Gazette of Republic of Serbia (2010/11): Regulations for pesticides, metals and metalloids and other toxic substances, chemotherapeutics, anabolic steroids and other substances which can be found in food. Službeni glasnik RS 25/2010 i 28/2011–dr. pravilnik.

  44. Pajević, S., Arsenov, D., Nikolić, N., Borisev, M., Orčić, D., Župunski, M., & Mimica-Dukic, N. (2018). Heavy metal accumulation in vegetable species and health risk assessment in Serbia. Environmental Monitoring and Assessment, 190, 459.

    Article  CAS  Google Scholar 

  45. Piekut, A., Baranowska, R., Marchwińska-Wyrwał, E., Ćwieląg-Drabek, M., Hajok, I., Dziubanek, G., & Grochowska-Niedworok, E. (2018). Is the soil quality monitoring an effective tool in consumers’ protection of agricultural crops from cadmium soil contamination?—A case of the Silesia region (Poland). Environmental Monitoring and Assessment, 190, 25.

    Article  CAS  Google Scholar 

  46. Qin, S. Y., Liu, H. E., Nie, Z. J., Rengel, Z., Gao, W., Li, C., & Zhao, P. (2020). Toxicity of cadmium and its competition with mineral nutrients for uptake by plants: A review. Pedosphere, 30(2), 168–180.

    Article  Google Scholar 

  47. Ramachandra, T. V., Sudarshan, P. B., Mahesh, M. K., & Vinay, S. (2018). Spatial patterns of heavy metal accumulation in sediments and macrophytes of Bellandur wetland, Bangalore. Journal of Environmental Management, 206, 1204–1210.

    CAS  Article  Google Scholar 

  48. RStudio Team (2020). RStudio 4.0.0. Integrated Development for R. RStudio, PBC, Boston, MA URL http://www.rstudio.com/.

  49. Rizwan, M., Ali S., Zia ur Rehman, M., & Maqbool, Z. A. (2019). A critical review on the effects of zinc at toxic levels of cadmium in plants. Environmental Science and Pollution Research, 26, 6279–6289.

    Article  CAS  Google Scholar 

  50. Sarwar, T., Shahid, M., NatashaKhalid, K. S., Shah, A. H., Ahmad, N., Haq, Z. A., et al. (2019). Quantification and risk assessment of heavy metal build-up in soil–plant system after irrigation with untreated city wastewater in Vehari. Pakistan: Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-019-00358-8.

    Book  Google Scholar 

  51. Sayed-Ahmad, B., Talou, T., Saad, Z., Hijazi, A., & Merah, O. (2017). The apiaceae: Ethnomedicinal family as source for industrial uses. Industrial Crops and Products, 109, 661–671.

    CAS  Article  Google Scholar 

  52. Sharma, S., Nagpal, A. K., & Kaur, I. (2018). Heavy metal contamination in soil, food crops and associated health risks for residents of Ropar wetland, Punjab, India and its environs. Food Chemistry, 255, 15–22.

    CAS  Article  Google Scholar 

  53. Simon, L. M., Fatrai, Z., Jonas, D. E., & Matkovic, B. (1974). Study of metabolism enzymes during the development of Phaseolus vulgaris. Biochemie und Physiologie der Pflanzen, 166, 387–392.

    CAS  Article  Google Scholar 

  54. Sun, X., & ZhangJ, L. L. (2020). Spatial assessment models to evaluate human health risk associated to soil potentially toxic elements. Environmental Pollution. https://doi.org/10.1016/j.envpol.2020.115699.

    Article  Google Scholar 

  55. Škrbić, B., & Čupić, S. (2004). Trace metal distribution in surface soils of Novi Sad and bank sediment of the Danube river. Journal of Environmental Science and Health Part A Toxic/Hazardous Substances and Environmental Engineering, 39(6), 1547–1558.

    Google Scholar 

  56. Tian, S., Xie, R., Wang, H., Hu, Y., Hou, D., Liao, X., et al. (2017). Uptake, sequestration and tolerance of cadmium at cellular levels in the hyperaccumulator plant species Sedum alfredii. Journal of Experimental Botany, 68(9), 2387–2398.

    CAS  Article  Google Scholar 

  57. Tóth, G., Hermann, T., Da Silva, M. R., & Montanarella, L. (2016). Heavy metals in agricultural soils of the European Union with implications for food safety. Environment International, 88, 299–309.

    Article  CAS  Google Scholar 

  58. U.S. EPA (2002). Supplemental guidance for developing soil screening levels for superfund sites. U. S. Environmental Protection Agency, Office of Emergency and Remedial Response, (OSWER 9355.4–24).

  59. US EPA (2011a). Exposure Factors Handbook 2011 Edition (Final Report). US Environmental Protection Agency, Washington, DC, EPA/600/R-09/052F.

  60. US Epa (2011). Screening level (RSL) for chemical contaminant at superfound sites. US: Environmental Protection Agency.

    Google Scholar 

  61. Ubavić, M. & Bogdanović, D. (2006). Praktikum iz Agrohemije. Poljoprivredni fakultet, Novi Sad, str. 34–63.

  62. Ulusu, Y., Öztürk, L., & Elmastaş, M. (2017). Antioxidant capacity and cadmium accumulation in parsley seedlings exposed to cadmium stress. Russian Journal of Plant Physiology, 64(6), 883–888.

    CAS  Article  Google Scholar 

  63. Verbruggen, N., Hermans, C., & Schat, H. (2009). Mechanisms to cope with arsenic or cadmium excess in plants. Current Opinion in Plant Biology, 12(3), 364–372.

    CAS  Article  Google Scholar 

  64. Viuda-Martos, M., Ruiz-Navajas, Y., Fernández-López, J., & Pérez-Alvarez, J. A. (2011). Spices as functional foods. Critical Reviews in Food Science and Nutrition, 51(1), 13–28.

    CAS  Article  Google Scholar 

  65. VROM. (2000). Circular on target values and intervention values for soil remediation Annex A: Target values, soil remediation intervention values and indicative levels for serious contamination. Spatial Planning and Environment (VROM): Dutch Ministry of Housing.

    Google Scholar 

  66. Wang, C., Zhao, Y., & Pei, Y. (2012). Investigation on reusing water treatment residuals to remedy soil contaminated with multiple metals in Baiyin, China. Journal of Hazardous Materials, 237–238, 240–246.

    Article  CAS  Google Scholar 

  67. WHO. (2007). Guidelines for assessing quality of herbal medicines with reference to contaminants and residues (pp. 1–118). Geneva, Switzerland: WHO Press.

    Google Scholar 

  68. Ye, X., Xiao, W., Zhang, Y., Zhao, S., Wang, G., Zhang, Q., & Wang, Q. (2015). Assessment of heavy metal pollution in vegetables and relationships with soil heavy metal distribution in Zhejiang province. China. Environmental Monitoring and Assessment, 187, 378.

    Article  CAS  Google Scholar 

  69. Yuswir, N. S., Praveena, S. M., Aris, A. Z., Ismail, S. N. S., de Burbure, C., & Hashim, Z. (2015). Heavy metal contamination in urban surface soil of Klang District (Malaysia). Soil and Sediment Contamination, 24(8), 865–881.

    CAS  Article  Google Scholar 

  70. Zeng, F., Li, W. W. M., Huang, R., Yang, F., & Duan, Y. (2015). Heavy metal contamination in rice-producing soils of Hunan Province, China and potential health risks. International Journal of Environmental Research and Public Health, 12, 15584–15593.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Research was conducted and funded within the project entitled: “Biologically active components and medical potential of functional food grown in Vojvodina Province, Serbia’’ no. 114-451-2149/2016-03, financed by the Provincial Secretariat for Science and Technological Development, Autonomous Province of Vojvodina, Serbia. The authors also acknowledge financial support of the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. 451-03-68/2020-14/ 200125).

Author information

Affiliations

Authors

Contributions

Arsenov D contributed to data curation; investigation; formal analysis; visualization; and writing—original draft, Župunski M was involved in conceptualization; methodology; investigation; and data curation, Pajević S contributrd to project administration and supervision, Borišev M was involved in methodology and formal analysis, Nikolić N contributed to validation and Mimica-Dukić N was involved in supervision and funding acquisition. All authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Danijela Arsenov.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arsenov, D., Župunski, M., Pajević, S. et al. Health assessment of medicinal herbs, celery and parsley related to cadmium soil pollution-potentially toxic elements (PTEs) accumulation, tolerance capacity and antioxidative response. Environ Geochem Health (2021). https://doi.org/10.1007/s10653-020-00805-x

Download citation

Keywords

  • Soil contamination
  • Vegetables pollution
  • Phytoextraction potential
  • Plants defense mechanisms
  • Human health risk