Risk analysis by bioaccumulation of Cr, Cu, Ni, Pb and Cd from wastewater-irrigated soil to Brassica species

  • S. SahayEmail author
  • A. Inam
  • S. Iqbal
Original Paper


In order to evaluate the possible human health risk by phyto-accumulation of five heavy metals, viz. Cr, Cd, Cu, Pb and Ni, four Brassica species, namely B. campestris, B. juncea, B. napus and B. nigra, were grown under field conditions irrigated with 100% (undiluted) and 50% (diluted) wastewater (WW). The groundwater treatment was taken as control. WW irrigations (50% and 100%) were found to increase growth parameters (length, fresh biomass and dry biomass of shoot and root) and seed yield of all Brassica species. Calculated metal indices showed tolerance ability (tolerance index, TolI > 1) of all four Brassica species growing in both 50% and 100% WW-irrigated soil, but none of these could act as hyperaccumulator (bioconcentration factor, BCF < 1, and translocation index, TraI < 100%). Even though WW contained the permissible limit of phyto-elements, the input/addition of them into soil through irrigation caused the accumulation of most of the heavy metals in both leaf and seed parts of all Brassica crops far above the safety limit. Furthermore, the values of hazard quotient (HQ) for single metal (Pb) and total metals in all the crops were greater than 1 (HQ > 1), representing the human health at serious risk.


Wastewater Heavy metals Brassica species Bioaccumulation factor Translocation index Tolerance index Enrichment factor Health quotient 



The authors are grateful to the Chairman, Department of Botany, A.M.U, Aligarh, for providing agricultural research field and all necessary facilities in the laboratory to carry out the research work. Also thanks to Dr. Akhtar Inam for guidance while writing the manuscript. Seema Sahay and Saba Iqbal drew the experimental design and contributed to performing the experiment, analysis and interpretation of data. All authors discussed the results and contributed equally to final version of submitted manuscript.


The author Seema Sahay gratefully acknowledges the award of Junior Research Fellow and Senior Research Fellow of Rajiv Gandhi National Fellowship (RGNF-JRF-SRF) and Post-Doctoral Fellowship via award letter numbers F. No. 16/1274/SC (SA-III) and No.F./PDFSS-2015-17-UTT-12296, respectively, by the University Grant Commission (UGC), New Delhi, India.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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  1. Ahmad JU, Goni MA (2010) Heavy metal contamination in water, soil, and vegetables of the industrial areas in Dhaka, Bangladesh. Environ Monit Assess 166:347–357. CrossRefGoogle Scholar
  2. Allen SE, Grimshaw HM, Rowland AP (1986) Chemical analysis. In: Moore PD, Chapman SB (eds) Methods in plant ecology. Blackwell, Scientific Publication, Oxford, pp 285–344Google Scholar
  3. American Public Health Association (APHA) (1985) Standard methods for examination of water and wastewater, 16th edn. American Public Health Association, Washington DC, pp 71–553Google Scholar
  4. Angelova V, Ivanova R, Todorov G, Ivanov K (2008) Heavy metal uptake by rape. Commun Soil Sci Plant Anal 39:344–357. CrossRefGoogle Scholar
  5. AngelovaV Ivanova K (2009) Bioaccumulation and distribution of heavy metals in black mustard (Brassica nigra Koch). Environ Monit Assess 153:449–459. CrossRefGoogle Scholar
  6. Arora M, Kiran B, Rani S, Rani A, Kaur B, Mittal N (2008) Heavy metal accumulation in vegetables irrigated with water from different sources. Food Chem 111:811–815. CrossRefGoogle Scholar
  7. Astera M (2014) The ideal soil: a handbook for the new agriculture. Accessed 15 Jan 2014
  8. Audet PI, Charest C (2007) Heavy metal phytoremediation from a meta-analytical perspective. Environ Pollut 147:231–237. CrossRefGoogle Scholar
  9. Awashthi SK (2000) Prevention of food adulteration act no 37 of 1954, Central and state rules as amended for 1999, IWd edn. Ashoka Law House, New DelhiGoogle Scholar
  10. Aydin ME, Aydin S, Beduk F, Tor A, Tekinay A, Kolb M, Bahadir M (2015) Effects of long-term irrigation with untreated municipal wastewater on soil properties and crop quality. Environ Sci Pollut Res 22:19203–19221. CrossRefGoogle Scholar
  11. Ayers RS, Wescot DW (1994) Water quality for agriculture, irrigation and drainage, Paper 29, rev. 1, Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  12. Babcock M, Shukla MK, Picchioni GA, Mexal JD, Daniel D (2009) Chemical and physical properties of Chihuahuan desert soils irrigated with industrial effluent. Arid Land Res Manag 23:47–66. CrossRefGoogle Scholar
  13. Baker DE, Amacher MC (1982) Nickel, copper, zinc and cadmium. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2. Chemical and microbiological properties, 2nd eds. American Society of Agronomy, Madison, WI, ASA, pp 323–336Google Scholar
  14. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metal elements: a review of their distribution, ecology, and phytochemistry. Biorecov 1:81–126Google Scholar
  15. Baker AJM, Mc Grath SP, Sideli CMD, Reeves RD (1994) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal accumulating plants. Resour Conserv Recycl 11:41–49. CrossRefGoogle Scholar
  16. Bettany JR, Halstead EH (1972) An automated procedure for the nephelometric determination of sulfate in soil extracts. Can J Soil Sci 52:127–129. CrossRefGoogle Scholar
  17. Bose S, Bhattacharyya AK (2008) Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 70:1264–1272. CrossRefGoogle Scholar
  18. Chalkoo S, Sahay S, Inam A, Iqbal S (2014) Application of wastewater irrigation on growth and yield of chilli under nitrogen and phosphorus fertilization. J Plant Nutr 37:1139–1147. CrossRefGoogle Scholar
  19. Chandra R, Yadav S, Mohan D (2008) Effect of distillery sludge on seed germination and growth parameters of Green gram (Phaseolus mungo L.). J Hazard Mater 152:431–439. CrossRefGoogle Scholar
  20. Chandra R, Bharagava RN, Yadav S, Mohan D (2009) Accumulation and distribution of toxic metals in wheat (Triticum aestivum L.) and Indian mustard (Brassica campestris L.) irrigated with distillery and tannery effluents. J Hazard Mater 162:1514–1521. CrossRefGoogle Scholar
  21. Chang CY, Yu HY, Chen JJ, Li FB, Zhang HH, Liu C (2014) Accumulation of heavy metals in leaf vegetables from agricultural soils and associated potential health risks. In the Pearl River Delta, South China. Environ Monit Assess 186:1547–1560. CrossRefGoogle Scholar
  22. Chapman HD, Pratt PF (1961) Methods of analysis for soils, plants, and waters. University of California, Division of agricultural science. Berkley, Riverside, California, p 309Google Scholar
  23. Chary NS, Kamala CT, Raj DSS (2008) Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer. Ecotoxicol Environ Saf 69:513–524. CrossRefGoogle Scholar
  24. Chopra SL, Kanwar JS (1982) Analytical agriculture chemistry. Kalyani Publishers, New Delhi, pp 191–205Google Scholar
  25. Chopra SL, Kanwar JS (1991) Analytical agriculture chemistry. Kalyani Publishers, New DelhiGoogle Scholar
  26. Chopra AK, Pathak C (2012) Bioaccumulation and translocation efficiency of heavy metals in vegetables grown on long-term wastewater irrigated soil near Bindal River, Dehradun. Agric Res 1:157–164. CrossRefGoogle Scholar
  27. Cicek A, Karaman MR, Turan M, Gunes A, Cigdem A (2013) Yield and nutrient status of wheat plant (T. aestivum) influenced by municipal wastewater irrigation. J Food Agric Environ 11:733–737Google Scholar
  28. Clesceri LS, Greenberg AE, Trussed RR (1989) Standard method for the examination of water and wastewater. In: 17th ed, 20005 (1), American Public Health Association, Washington DC, pp 40–175Google Scholar
  29. Dar MI, Khan FA, Rehman F, Masoodi A, Ansari AA, Varshney D, Naushin F, Naikoo MI (2015) Roles of Brassicaceae in phytoremediation of metals and metalloids. In: Ansari AA et al (eds) Phytoremediation: management of environmental contaminants. Springer, Switzerland. CrossRefGoogle Scholar
  30. De Maria S, Rivelli AR (2013) Trace element accumulation and distribution in sunflower plants at the stages of flower bud and maturity. Italian J Agron 8:65–72. CrossRefGoogle Scholar
  31. Dickman SR, Bray RH (1940) Colorimetric determination of phosphate. J Ind Eng Chem Anal Edition 12:665–668. CrossRefGoogle Scholar
  32. Diwan H, Ahmad A, Iqbal M (2010) Uptake-related parameters as indices of phytoremediation potential. Biologia 65:1004–1011. CrossRefGoogle Scholar
  33. Eid EM, Shaltout KH (2016) Bioaccumulation and translocation of heavy metals by nine native plant species grown at a sewage sludge dump site. Int J Phytoreme 18:1075–1085. CrossRefGoogle Scholar
  34. Epstein E, Jafferies RL (1964) The genetic basis of selective ion transport in plants. Ann Rev Plant Physiol 15:169–184. CrossRefGoogle Scholar
  35. European Commission (EC) (2001) Commission Regulation (EC) 466/2001. Setting maximum levels for certain contaminants in foodstuffs. Official J European Communities, pp 77Google Scholar
  36. FAO/WHO (1984) Codex alimentarius commission contaminants, Joint FAO/WHO food standards program, vol. XVII (1st ed.), Codex alimentariusGoogle Scholar
  37. Gall JE, Rajakaruna N (2013) The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In: Lang M (ed) Brassicaceae: characterization, functional genomics and health benefits. Nova Science Publishers, Hauppauge, pp 121–148Google Scholar
  38. Gall JE, Boyd RS, Rajakaruna N (2015) Transfer of heavy metals through terrestrial food webs: a review. Environ Monit Assess 187:201–222. CrossRefGoogle Scholar
  39. Ganguly AK (1951) Base exchange capacity of silica and silicate minerals. J Phys Chem 55:1417–1428. CrossRefGoogle Scholar
  40. Ge KY (1992) The status of nutrient and meal of Chinese in the 1990s. Beijing People’s Hygiene Press, Beijing, pp 415–434Google Scholar
  41. Gupta AK, Sinha S (2007) Phytoextraction capacity of the plants growing on tannery sludge dumping sites. Bioresour Technol 98:1788–1794. CrossRefGoogle Scholar
  42. Gupta N, Khan DK, Santra SC (2008) An assessment of heavy metal contamination in vegetables grown in wastewater-irrigated areas of Titagarh, West Bengal, India. Bull Environ Contam Toxicol 80:115–118. CrossRefGoogle Scholar
  43. Hassan N, Ahmad K (1984) Intra-familial distribution of food in rural Bangladesh. Food Nutr Bull 6(4):1–10. CrossRefGoogle Scholar
  44. Indian Council of Medical Research (2010) Nutrient requirements and recommended dietary allowances for Indians. National Institute of Nutrition, HyderabadGoogle Scholar
  45. Indian Standards Institution (ISI) (1974) Tolerance limit for industrial effluents discharged into inland surface waters, No. 2490 New DelhiGoogle Scholar
  46. Indian Standards Institution (ISI) (1983) Specification for drinking and irrigation water, IS: 10500, New DelhiGoogle Scholar
  47. Iqbal S, Tak HI, Inam A, Inam A, Sahay S, Chalkoo S (2015) Comparative effect of wastewater and groundwater irrigation along with nitrogenous fertilizer on growth, photosynthesis and productivity of Chilli (Capsicum annuum L.). J Plant Nutr 38:1006–1021. CrossRefGoogle Scholar
  48. Iqbal S, Inam A, Inam A, Ashfaque F, Sahay S (2017) Potassium and waste water interaction in the regulation of photosynthetic capacity, ascorbic acid and capsaicin content in Chilli (Capsicum annuum L.). Agric Water Manag 184:201–210. CrossRefGoogle Scholar
  49. Jackson ML (1973) Soil chemistry analysis. Prentice Gall of India, New DelhiGoogle Scholar
  50. Joint FAO/WHO (1999) Expert committee on food additives, summary and conclusions. In: 53rd Meeting, Rome. June 1–10Google Scholar
  51. Khan MU, Malik RN, Muhammad S (2013) Human health risk from heavy metal via food crops consumption with wastewater irrigation practices in Pakistan. Chemosphere 93:2230–2238. CrossRefGoogle Scholar
  52. Khan K, Khan H, Lu Y, Ihsanullah I, Nawab J, Khan S, Shah NS, Shamshad I, Maryam A (2014) Evaluation of toxicological risk of foodstuffs contaminated with heavy metals in Swat, Pakistan. Ecotoxico Environ Safe 108:224–232. CrossRefGoogle Scholar
  53. Khan ZI, Ahmad K, Rehman S, Siddique S, Bashir H, Zafar A, Sohail M, Ali SA, Cazzato E, Mastro GD (2017) Health risk assessment of heavy metals in wheat using different water qualities: implication for human health. Environ Sci Pollut Res 24:947–955. CrossRefGoogle Scholar
  54. Kisku GC, Barman SC, Bhargava SK (2000) Contamination of soil and plants with potentially toxic elements irrigated with mixed industrial effluent and its impact on the environment. Water Air Soil Poll 120:121–137. CrossRefGoogle Scholar
  55. Kiziloglu FM, Turan M, Sahin U, Kuslu Y, Dursun A (2008) Effects of untreated and treated wastewater irrigation on some chemical properties of cauliflower (Brassica olerecea L.var. botrytis) and red cabbage (Brassica olerecea L. var. rubra) grown on calcareous soil in Turkey. Agric Water Manag 95:716–724. CrossRefGoogle Scholar
  56. Kloke A, Sauerback DR, Vetter H (1984) The contamination of plants and soils with heavy metals and the transport of metals in terrestrial food chains. In: Nriagu JO (ed) Changing metal cycles and human health. Springer, Berlin, pp 113–141CrossRefGoogle Scholar
  57. Liu YJ, Zhu YG, Ding H (2007) Lead and cadmium in leaves of deciduous trees in Beijing, China: development of a metal accumulation index (MAI). Environ Pollut 145:387–390. CrossRefGoogle Scholar
  58. Ma SC, Zhang HB, Ma ST, Wang R, Wang GX, Shao Y, Li CX (2015) Effects of mine wastewater irrigation on activities of soil enzymes and physiological properties, heavy metal uptake and grain yield in winter wheat. Ecotoxic Environ Saf 113:483–490. CrossRefGoogle Scholar
  59. Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, Li R, Zhang Z (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxico Environ Saf 126:111–121. CrossRefGoogle Scholar
  60. Mishra A, Tripathi BD (2008) Heavy metal contamination of soil, and bioaccumulation in vegetables irrigated with treated waste water in the tropical city of Varanasi, India. Toxicol Environ Chem 90:861–871. CrossRefGoogle Scholar
  61. Nakamura T, Adu-Gyamfi JJ, Yamamoto A, Ishikawa SA, Nakano H, Ito O (2002) Varietal differences in root growth as related to nitrogen uptake by sorghum plants in low-nitrogen environment. Plant Soil 245:17–24. CrossRefGoogle Scholar
  62. National Institute of Nutrition (2011) Dietary guidelines for Indians-a manual. National Institute of Nutrition, HyderabadGoogle Scholar
  63. Newman MC, Unger MA (2003) Fundamentals of ecotoxicology, 2nd edn. Lewis Publishers, Boca Raton, FLGoogle Scholar
  64. Overesch M, Rinklebe J, Broll G, Neue HU (2007) Metals and arsenic in soils and corresponding vegetation at Central Elbe river flood plains (Germany). Environ Pollut 145:800–812. CrossRefGoogle Scholar
  65. Page V, Weisskopf L, Feller U (2006) Heavy Metals in white lupin: uptake, root-to-shoot transfer and redistribution within the plant. New Phytol 171:329–341. CrossRefGoogle Scholar
  66. Pendias AK, Mukherjee AB (2007) Trace elements from soil to human. Springer, New York. CrossRefGoogle Scholar
  67. Pendias AK, Pendias H (1992) Elements of group VIII. Trace elements in soils and plants. CRC Press, Boca Raton, pp 271–276Google Scholar
  68. Pierzynski GM, Sims JT, Vance GF (2000) Soils and environmental quality, 2nd edn. CRC Press, LLC, NW Corporate Blvd, Boca Raton, FLGoogle Scholar
  69. Qadir M, Wichelns D, Raschid-Sally L, McCornick PG, Drechsel P, Bahri A, Minhas PS (2010) The challenges of wastewater irrigation in developing countries. Agric Water Manag 97:561–568. CrossRefGoogle Scholar
  70. Rezapour S, Samadi A (2011) Soil quality response to long-term wastewater irrigation in inceptisols from a semi-arid environment. Nutri Cycl Agroeco 91:269–280. CrossRefGoogle Scholar
  71. Richards LA (1954) Diagnosis and Improvement of Saline Alkali Soils. Agriculture Handbook US Department, Agriculture, 60, Washington, DCGoogle Scholar
  72. RoyChowdhury A, Datta R, Sarkar D (2018) Chapter 310: Heavy metal pollution and remediation. In: Torok B, Dransfield T (eds) Green chemistry: an inclusive approach. Elsevier, Amsterdam, pp 359–373. CrossRefGoogle Scholar
  73. RoyChowdhury A, Sarkar D, Datta R (2019) A combined chemical and phytoremediation method for reclamation of acid mine drainage-impacted soils. Environ Sci Poll Res 26(14):14414–14425. CrossRefGoogle Scholar
  74. Sahay S, Inam A, Inam A, Iqbal S (2015) Modulation in growth, photosynthesis and yield attributes of black mustard (B. nigra cv. IC247) by interactive effect of waste water and fly ash under different NPK levels. Cogent Food Agric 1:1087632. CrossRefGoogle Scholar
  75. Sahay S, Iqbal S, Ashfaque F, Inam A (2017) Effect of waste water and fly ash application on physiological determinants, yield and heavy metal contents of yellow mustard (B. campestris cv. P. Gold). J Plant Nutr 40:1710–1727. CrossRefGoogle Scholar
  76. Sahay S, Iqbal S, Inam A, Gupta M, Inam A (2019) Waste water irrigation in the regulation of soil properties, growth determinants, and heavy metal accumulation in Brassica species. Environ Monit Assess 191:107–128. CrossRefGoogle Scholar
  77. Sharma SS, Dietz KJ, Mimura T (2016) Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ 39(5):1112–1126. CrossRefGoogle Scholar
  78. Singh RP, Agrawal M (2007) Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67:2229–2240. CrossRefGoogle Scholar
  79. Singh BR, Narwal RP, Jeng AS, Almas AR (1995) Crop uptake and extractability of cadmium in soils naturally high in metals at different pH levels. Commun Soil Sci Plant Anal 26:2123–2142. CrossRefGoogle Scholar
  80. Singh PK, Deshbhratar PB, Ramteke DS (2012) Effects of sewage wastewater irrigation on soil properties, crop yield and environment. Agric Water Manage 103:100–104. CrossRefGoogle Scholar
  81. Sinha S, Gupta AK, Bhatt K (2007) Uptake and translocation of metals in fenugreek grown on soil amended with tannery sludge: involvement of antioxidants. Ecotoxicol Environ Saf 67:267–277. CrossRefGoogle Scholar
  82. Smith SR, Giller KE (1992) Effective rhizobium leguminosarum biovar Trifolii present in five soils contaminated with heavy metals from long-term applications of sewage sludge or metal mine spoil. Soil Biol Biochem 24:781–788. CrossRefGoogle Scholar
  83. Sou Dakoure MY, Mermoud A, Yacouba H, Boivin P (2013) Impacts of irrigation with industrial treated wastewater on soil properties. Geoderma 200–201:31–39. CrossRefGoogle Scholar
  84. Sukreeyapongse O, Holm PE, Strobel BW, Panichsakpatana S, Magid J, Hansen HS (2002) pH-dependent release of cadmium, copper, and lead from natural and sludge-amended soils. J Environ Qual 31:1901–1909. CrossRefGoogle Scholar
  85. United States Environmental Protection Agency (USEPA) (1997) Exposure factors handbook, Volume II-food ingestion factors, EPA/600//P-95/002Fa. Office of research and development, WashingtonGoogle Scholar
  86. United States Environmental Protection Agency (USEPA) (2002) Exposure factors handbook, Volume II-food ingestion factors. EPA/600//P-95/002Fa. Office of research and development, WashingtonGoogle Scholar
  87. United States Environmental Protection Agency (USEPA) (2015) Human health risk assessment: risk-based concentration tableGoogle Scholar
  88. Walkley A, Black CA (1934) An examination of the digestion method for the determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38CrossRefGoogle Scholar
  89. Wang X, Sato T, Xing B, Tao S (2005) Health risks of heavy metals to the general public in Tianjin, China via consumption of vegetables and fish. Sci Tot Environ 350:28–37. CrossRefGoogle Scholar
  90. Weldegebriel Y, Chandravanshi BS, Wondimu T (2012) Concentration levels of metals in vegetables grown in soils irrigated with river water in Addis Ababa, Ethiopia. Ecotoxicol Environ Saf 77:57–63. CrossRefGoogle Scholar
  91. Wilkins DA (1957) A technique for the measurement of lead tolerance in plants. Nature 180:37–38. CrossRefGoogle Scholar
  92. Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. New Phytol 80:623–633CrossRefGoogle Scholar
  93. Wu J, Teng Y, Lu S, Wang Y, Jiao X (2014) Evaluation of soil contamination indices in a mining area of Jiangxi, China. PLoS ONE 9:112917. CrossRefGoogle Scholar
  94. Zayed A, Gowthaman S, Terry N (1998) Phytoaccumulation of trace elements by wetland plants: I, Duckweed. J Environ Qual 27:715–721. CrossRefGoogle Scholar
  95. Zhang W, Cai Y, Tu C, Ma LQ (2002) Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Sci Total Environ 300:167–177. CrossRefGoogle Scholar
  96. Zhuang P, Zou B, Li NY, Li ZA (2009) Heavy metal contamination in soils and food crops around Dabaoshan mine in Guangdong, China: implication for human health. Environ Geochem Health 31:707–715. CrossRefGoogle Scholar
  97. Zu YQ, Li Y, Chen JJ, Chen HJ, Qin L, Schvartz C (2005) Hyperaccumulation of Pb, Zn, and Cd in herbaceous grown on lead–zinc mining area in Yunnan, China. Environ Int 31:755–762. CrossRefGoogle Scholar

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© Islamic Azad University (IAU) 2019

Authors and Affiliations

  1. 1.Advance Plant Physiology, Biochemistry and Environmental Sciences Laboratory, Department of BotanyAligarh Muslim UniversityAligarhIndia
  2. 2.Department of Botany, Women’s CollegeAligarh Muslim UniversityAligarhIndia
  3. 3.Ecotoxicogenomics Lab, Department of BiotechnologyJamia Millia IslamiaNew DelhiIndia

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