Skip to main content

Human health risk mitigation from arsenic in rice by crop rotation with a hyperaccumulator plant

Abstract

Exposure to arsenic (As) from a diet of contaminated rice is a widespread problem and a serious concern in several parts of the world. There is a need to develop sustainable, effective, and reliable strategies to reduce As accumulation in rice. Our goal was to develop and test a simple crop rotation method of alternating rice with the As hyperaccumulator plant, Chinese brake fern (Pteris vitatta L.), to reduce As concentrations in rice grains. A greenhouse column study was performed for 2 years using As-contaminated rice paddy soil from West Bengal. Rice was grown under flooded conditions and irrigated with As-contaminated water to simulate field conditions. Chinese brake fern was grown between two rice cycles in experimental columns, while control columns were left unplanted. Our results show that at the end of two cycles, there was a statistically significant decrease in soil As concentrations in the treatment columns compared to the control columns. After one rotation with the fern, there was a significant decline in As concentrations in rice grains in treatment plants and a concomitant decline in both noncarcinogenic and carcinogenic health risks. Our results indicate that there could be substantial benefit in implementing this simple crop rotation model to help lower human health risks from As exposure via rice ingestion.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data availability

The data are available at Mendeley Data, V1, https://doi.org/10.17632/6fg2ds9pnk.1.

Materials availability

The data are available at Mendeley Data, V1, https://doi.org/10.17632/6fg2ds9pnk.1.

References

  • Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128

    Article  CAS  Google Scholar 

  • Ahmad SA, Khan MH, Haque M (2018) Arsenic contamination in groundwater in Bangladesh: implications and challenges for healthcare policy. Risk Manag Healthc Policy 11:251

    Article  Google Scholar 

  • Ali W, Rasool A, Junaid M, Zhang H (2019) A comprehensive review on current status, mechanism, and possible sources of arsenic contamination in groundwater: a global perspective with prominence of Pakistan scenario. Environ Geochem Health 41:737–760

    Article  CAS  Google Scholar 

  • Andra SS, Datta R, Sarkar D, Saminathan SK, Mullens CP, Bach SB (2009) Analysis of phytochelatin complexes in the lead tolerant vetiver grass [Vetiveria zizanioides (L.)] using liquid chromatography and mass spectrometry. Environ Pollut 157:2173–2183

    Article  CAS  Google Scholar 

  • Barla A (2019) Intensification of arsenic and heavy metals in soil and rice grain: a sustainable mitigation via irrigation in two specific rice cultivars. Ph.D. Dissertation, Indian Institute of Science Education and Research Kolkata, India

  • Ben-Dor E, Banin A (1989) Determination of organic matter content in arid-zone soils using a simple “loss-on-ignition” method. Commun Soil Sci Plant Anal 20:1675–1695

    Article  Google Scholar 

  • Berg M, Tran HC, Nguyen TC, Pham HV, Schertenleib R, Giger W (2001) Arsenic contamination of groundwater and drinking water in Vietnam: a human health threat. Environ Sci Technol 35:2621–2626

    Article  CAS  Google Scholar 

  • Bhattacharya P, Samal A, Majumdar J, Santra S (2009) Transfer of arsenic from groundwater and paddy soil to rice plant (Oryza sativa L.): a micro level study in West Bengal India. World J Agric Sci 5:425–431

    CAS  Google Scholar 

  • Biswas JK, Warke M, Datta R, Sarkar D (2020) Is arsenic in rice a major human health concern? Curr Pollut Rep 6:37–42

    Article  CAS  Google Scholar 

  • Ciminelli VS, Gasparon M, Ng JC, Silva GC, Caldeira CL (2017) Dietary arsenic exposure in Brazil: the contribution of rice and beans. Chemosphere 168:996–1003

    Article  CAS  Google Scholar 

  • da Silva EB, Lessl JT, Wilkie AC, Liu X, Liu Y, Ma LQ (2018) Arsenic removal by As-hyperaccumulator Pteris vittata from two contaminated soils: A 5-year study. Chemosphere 206:736–741

    Article  Google Scholar 

  • Das A, Joardar M, Chowdhury NR, De A, Mridha D, Roychowdhury T (2021) Arsenic toxicity in livestock growing in arsenic endemic and control sites of West Bengal: risk for human and environment. Environ Geochem Health 43:3005–3025

    Article  CAS  Google Scholar 

  • Edmunds W, Ahmed K, Whitehead P (2015) A review of arsenic and its impacts in groundwater of the Ganges–Brahmaputra–Meghna delta, Bangladesh. Environ Sci Process Impacts 17:1032–1046

    Article  CAS  Google Scholar 

  • Gee G, Bauder J (1986) Hydrometer method. Methods Soil Anal: Part 1:404–408

    Google Scholar 

  • Golui D, Mazumder DG, Sanyal S, Datta S, Ray P, Patra P, Sarkar S, Bhattacharya K (2017) Safe limit of arsenic in soil in relation to dietary exposure of arsenicosis patients from Malda district, West Bengal-a case study. Ecotoxicol Environ Saf 144:227–235

    Article  CAS  Google Scholar 

  • Hojsak I, Braegger C, Bronsky J, Campoy C, Colomb V, Decsi T, Domellöf M, Fewtrell M, Mis NF, Mihatsch W (2015) Arsenic in rice: a cause for concern. J Pediatr Gastroenterol Nutr 60:142–145

    Article  CAS  Google Scholar 

  • Joseph T, Dubey B, McBean EA (2015) Human health risk assessment from arsenic exposures in Bangladesh. Sci Total Environ 527:552–560

    Article  Google Scholar 

  • Karagas MR, Punshon T, Davis M, Bulka CM, Slaughter F, Karalis D, Argos M, Ahsan H (2019) Rice intake and emerging concerns on arsenic in rice: a review of the human evidence and methodologic challenges. Curr Environ Health Rep 6:361–372

    Article  Google Scholar 

  • Khanam R, Hazra GC, Ghosh Bag A, Kulsum PGPS, Chatterjee N, Shukla AK (2021) Risk assessment of arsenic toxicity through groundwater-soil-rice system in Maldah District, Bengal Delta Basin, India. Arch Environ Contam Toxicol 81:438–448

    Article  CAS  Google Scholar 

  • La-Up A, Wiwatanadate P, Pruenglampoo S, Uthaikhup S (2017) Recommended rice intake levels based on average daily dose and urinary excretion of cadmium in a cadmium-contaminated area of Northwestern Thailand. Toxicol Res 33:291–297

    Article  CAS  Google Scholar 

  • Lai PY, Cottingham KL, Steinmaus C, Karagas MR, Miller MD (2015) Arsenic and rice: translating research to address health care providers’ needs. J Pediatr 167:797–803

    Article  Google Scholar 

  • Lessl JT, Luo J, Ma LQ (2014) Pteris vittata continuously removed arsenic from non-labile fraction in three contaminated-soils during 3.5 years of phytoextraction. J Hazard Mater 279:485–492

    Article  CAS  Google Scholar 

  • Liao N, Seto E, Eskenazi B, Wang M, Li Y, Hua J (2018) A comprehensive review of arsenic exposure and risk from rice and a risk assessment among a cohort of adolescents in Kunming, China. Int J Environ Res Public Health 15:2191

    Article  CAS  Google Scholar 

  • Llobet J, Falco G, Casas C, Teixido A, Domingo J (2003) Concentrations of arsenic, cadmium, mercury, and lead in common foods and estimated daily intake by children, adolescents, adults, and seniors of Catalonia, Spain. J Agric Food Chem 51:838–842

    Article  CAS  Google Scholar 

  • Ma J, Lei E, Lei M, Liu Y, Chen T (2018) Remediation of arsenic contaminated soil using malposed intercropping of Pteris vittata L. and maize. Chemosphere 194:737–744

    Article  CAS  Google Scholar 

  • Mandal A, Purakayastha T, Patra A, Sanyal S (2012a) Phytoremediation of arsenic contaminated soil by Pteris vittata L. II. Effect on arsenic uptake and rice yield. Int J Phytorem 14:621–628

    Article  CAS  Google Scholar 

  • Mandal A, Purakayastha T, Patra A, Sanyal S (2012b) Phytoremediation of arsenic contaminated soil by Pteris vittata LI Influence of phosphatic fertilizers and repeated harvests. Int J Phytorem 14:978–995

    Article  CAS  Google Scholar 

  • Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235

    Article  CAS  Google Scholar 

  • McArthur J, Ghosal U, Sikdar P, Ball J (2016) Arsenic in groundwater: the deep late pleistocene aquifers of the Western Bengal Basin. Environ Sci Technol 50:3469–3476

    Article  CAS  Google Scholar 

  • McKeague J, Brydon JE, Miles NM (1971) Differentiation of forms of extractable iron and aluminum in soils. Soil Sci Soc Am J 35:33–38

    Article  CAS  Google Scholar 

  • Meharg AA, Zhao F-J (2012) Biogeochemistry of arsenic in paddy environments. Arsenic & Rice. Springer, pp 71–101

  • Mehlich A (1984) Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun Soil Sci Plant Anal 15:1409–1416

    Article  CAS  Google Scholar 

  • Mishra S, Dwivedi S, Kumar A, Chauhan R, Awasthi S, Mattusch J, Tripathi R (2016) Current status of ground water arsenic contamination in India and recent advancements in removal techniques from drinking water. Int J Plant Environ 2:01–15

    Article  Google Scholar 

  • Mondal D, Polya DA (2008) Rice is a major exposure route for arsenic in Chakdaha block, Nadia district, West Bengal, India: a probabilistic risk assessment. Appl Geochem 23:2987–2998

    Article  CAS  Google Scholar 

  • Mukherjee A, Sengupta MK, Hossain MA, Ahamed S, Das B, Nayak B, Lodh D, Rahman MM, Chakraborti D (2006) Arsenic contamination in groundwater: a global perspective with emphasis on the Asian scenario. J Health Popul Nutrition 24(2):142–163

    Google Scholar 

  • Murphy T, Phan K, Yumvihoze E, Irvine K, Wilson K, Lean D, Poulain A, Laird B, Chan LHM (2018) Effects of arsenic, iron and fertilizers in soil on rice in Cambodia. J Health Pollut 8(19):180910

    Article  Google Scholar 

  • Na Nagara V, Sarkar D, Luo Q, Biswas JK, Datta R (2022) Health risk assessment of exposure to trace elements from drinking black and green tea marketed in three countries. Biol Trace Elem Res 200:2970–2982

    Article  CAS  Google Scholar 

  • Norra S, Berner Z, Agarwala P, Wagner F, Chandrasekharam D, Stüben D (2005) Impact of irrigation with As rich groundwater on soil and crops: a geochemical case study in West Bengal Delta Plain, India. Appl Geochem 20:1890–1906

    Article  CAS  Google Scholar 

  • Saha K (1995) Chronic arsenical dermatosis from tube-well water in West Bengal during 1983–1987. Indian J Dermatol 40:1–12

    Google Scholar 

  • Sankpal UT, Pius H, Khan M, Shukoor MI, Maliakal P, Lee CM, Abdelrahim M, Connelly SF, Basha R (2012) Environmental factors in causing human cancers: emphasis on tumorigenesis. Tumor Biology 33:1265–1274

    Article  CAS  Google Scholar 

  • Sanyal T, Deb H, Mukherjee S (2017) Use of surface water to combat groundwater pollution: with special reference to ganga water treatment plant of Chakdaha, Nadia, West Bengal. Interntl J Eng Sci Res Technol 6(9):595–605

    CAS  Google Scholar 

  • Shaji E, Santosh M, Sarath K, Prakash P, Deepchand V, Divya B (2021) Arsenic contamination of groundwater: a global synopsis with focus on the Indian Peninsula. Geosci Front 12:101079

    Article  CAS  Google Scholar 

  • Sidhu V, Sarkar D, Datta R (2016) Effects of biosolids and compost amendment on chemistry of soils contaminated with copper from mining activities. Environ Monit Assess 188:1–9

    Article  CAS  Google Scholar 

  • Smith AH, Lingas EO, Rahman M (2000) Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bull World Health Organ 78:1093–1103

    CAS  Google Scholar 

  • Sparks D, Page A, Helmke P, Loeppert R, Soltanpour P, Tabatabai M (1996) Methods of soil analysis. Part 3. Chemical methods. SSSA Book Ser. 5. SSSA, Madison

  • Srivastava AK, Pandey M, Ghate T, Kumar V, Upadhyay MK, Majumdar A, Sanjukta AK, Agrawal AK, Bose S, Srivastava S (2021) Chemical intervention for enhancing growth and reducing grain arsenic accumulation in rice. Environ Pollut 276:116719

    Article  CAS  Google Scholar 

  • Tessier A, Campbell PG, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851

    Article  CAS  Google Scholar 

  • Tóth G, Hermann T, Da Silva M, Montanarella L (2016) Heavy metals in agricultural soils of the European Union with implications for food safety. Environ Int 88:299–309

    Article  Google Scholar 

  • Tu C, Ma LQ, Bondada B (2002) Arsenic accumulation in the hyperaccumulator Chinese brake and its utilization potential for phytoremediation. J Environ Qual 31:1671–1675

    Article  CAS  Google Scholar 

  • Upadhyay MK, Majumdar A, Barla A, Bose S, Srivastava S (2019) An assessment of arsenic hazard in groundwater–soil–rice system in two villages of Nadia district, West Bengal, India. Environ Geochem Health 41:2381–2395

    Article  CAS  Google Scholar 

  • Upadhyay MK, Majumdar A, Barla A, Bose S, Srivastava S (2021) Thiourea supplementation mediated reduction of grain arsenic in rice (Oryza sativa L.) cultivars: a two year field study. J Hazard Mater 407:124368

    Article  CAS  Google Scholar 

  • Upadhyay MK, Majumdar A, Suresh Kumar J, Srivastava S (2020) Arsenic in rice agro-ecosystem: solutions for safe and sustainable rice production. Front Sustain Food Syst 4:53

    Article  Google Scholar 

  • USEPA (1996) Method 3050B: acid digestion of sediments, sludges, and soils. Revision 2. USEPA Washington, DC

  • USEPA (1998) Risk estimation - arsenic, inorganic; CASRN 7440–38–2. http://www.webcitation.org/71CfwBK0x

  • Wu C, Huang L, Xue S-G, Pan W-S, Zou Q, Hartley W, Wong M-H (2017) Oxic and anoxic conditions affect arsenic (As) accumulation and arsenite transporter expression in rice. Chemosphere 168:969–975

    Article  CAS  Google Scholar 

  • Yang Y, Xiao C, Wang F, Peng L, Zeng Q, Luo S (2022) Assessment of the potential for phytoremediation of cadmium polluted soils by various crop rotation patterns based on the annual input and output fluxes. J Hazard Mater 423:127183

    Article  CAS  Google Scholar 

  • Ye W-L, Khan MA, McGrath SP, Zhao F-J (2011) Phytoremediation of arsenic contaminated paddy soils with Pteris vittata markedly reduces arsenic uptake by rice. Environ Pollut 159:3739–3743

    Article  CAS  Google Scholar 

  • Yu L, Zhu J, Huang Q, Su D, Jiang R, Li H (2014) Application of a rotation system to oilseed rape and rice fields in Cd-contaminated agricultural land to ensure food safety. Ecotoxicol Environ Saf 108:287–293

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge Dr. Sutapa Bose, IISER, for the paddy soil. MW acknowledges a teaching assistantship from the Department of Biological Sciences, Michigan Technological University.

Author information

Authors and Affiliations

Authors

Contributions

Manas Warke: Data collection, curation, analysis, methodology, writing—original draft. Dibyendu Sarkar: Conceptualization, writing—review and editing, and formal analysis. Zhiming Zhang: Methodology and sample analysis. Sameer Neve: Methodology and sample analysis. Rupali Datta: Project administration, validation, supervision, and writing—review and editing.

Corresponding author

Correspondence to Rupali Datta.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Elena Maestri

Publisher’s note

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

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Warke, M., Sarkar, D., Zhang, Z. et al. Human health risk mitigation from arsenic in rice by crop rotation with a hyperaccumulator plant. Environ Sci Pollut Res 30, 12030–12040 (2023). https://doi.org/10.1007/s11356-022-22985-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-22985-y

Keywords