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An approach towards safe and sustainable use of the green alga Chlorella for removal of radionuclides and heavy metal ions

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Abstract

Release of radionuclide and heavy metals in environment during healthcare, agriculture and military practices, and mining and energy production, poses a serious threat to humans and whole ecosystems. Acute or chronic exposure to human causes serious health effects such as acute radiation syndrome, burns, neurological disorders, renal damage and cancers. Hence, there is a need to find safe, wide-spectrum and cost-effective agents for removing internalized radionuclides and preventing internalization of these ions. In this direction, nutritional supplements offer an excellent option. The present review examines the potential of Chlorella for removal of radionuclide and heavy metal ions. Chlorella is a green alga consumed as dietary food supplement in powdered form. In addition to its high nutritional value, it is reported as an excellent detoxifying agent. The powdered Chlorella has been reported for removal of mercury, cadmium and radioactive strontium from the body. Chlorella contains a variety of metal-binding functional groups such as carboxyl, amino, phosphoryl, hydroxyl and carbonyl groups, which have high affinity towards various metal ions. Different species of Chlorella in live, dead or powdered forms has shown removal efficiency for different toxic metal ions from living as well as non-living things.

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References

  • Adam C, Garnier-Laplace J (2003) Bioaccumulation of silver-110m, cobalt-60, cesium-137, and manganese-54 by the freshwater algae Scenedesmus obliquus and Cyclotella meneghiana and by suspended matter collected during a summer bloom event. Limnol Oceanogr 48:2303–2313

    Article  CAS  Google Scholar 

  • Akhtar N, Saeed A, Iqbal M (2003) Chlorella sorokiniana immobilized on the bio- matrix of vegetable sponge of Luffa cylindrica: a new system to remove cadmium from contaminated aqueous medium. Bioresour Technol 88:163–165

    Article  CAS  PubMed  Google Scholar 

  • Akhtar N, Iqbal J, Iqbal M (2004) Enhancement of lead(II) biosorption by microalgal biomass immobilized onto loofa (Luffa cylindrica) sponge. Eng Life Sci 4:171–178

    Article  CAS  Google Scholar 

  • Akhtar N, Iqbal M, Zafar SI, Iqbal J (2008) Biosorption characteristics of uni- cellular green alga Chlorella sorokiniana immobilized in loofa sponge for removal of Cr(III). J Environ Sci 20:231–239

    Article  CAS  Google Scholar 

  • Aksu Z (2001) Equilibrium and kinetic modelling of cadmium(II) biosorption by C. vulgaris in a batch system: effect of temperature. Sep Purif Technol 21:285–294

    Article  CAS  Google Scholar 

  • Aksu Z (2002) Determination of the equilibrium, kinetic and thermodynamic parameters of the batch biosorption of nickel(II) ions onto Chlorella vulgaris. Process Biochem 38:89–99

    Article  CAS  Google Scholar 

  • Aksu Z, Donmez G (2006) Binary biosorption of cadmium(II) and nickel(II) onto dried Chlorella vulgaris: Co-ion effect on mono-component isotherm parameters. Process Biochem 41:860–868

    Article  CAS  Google Scholar 

  • Aksu Z, Kutsal T (1990) A comparative study for biosorption characteristics of heavy metal ions with C. vulgaris. Environ Technol 11:979–987

    Article  CAS  Google Scholar 

  • Aksu Z, Sag Y, Kutsal T (1992) The biosorption of copper(II) by C. vulgaris and Z. ramigera. Environ Technol 13:579–586

    Article  CAS  Google Scholar 

  • Aksu Z, Egretli G, Kutsal T (1998) A comparative study of copper(II) biosorption on Ca-alginate, agarose and immobilized C. vulgaris in a packed-bed column. Process Biochem 33:393–400

    Article  CAS  Google Scholar 

  • Al-Rub FAA, El-Naas M, Benyahia F, Ashour I (2004) Biosorption of nickel on blank alginate beads, free and immobilized algal cells. Process Biochem 39:1767–1773

    Article  CAS  Google Scholar 

  • Altagracia-Martínez M, Kravzov-Jinich J, Martínez-Núñez JM, Ríos-Castañeda C, López-Naranjo F (2012) Prussian blue as an antidote for radioactive thallium and cesium poisoning. Orphan Drugs: Res Rev 2:13–21

    Article  CAS  Google Scholar 

  • Amini M, Younesi H, Bahramifar N (2013) Biosorption of U(VI) from aqueous solution by Chlorella vulgaris : Equilibrium, kinetic and thermodynamic studies. J Environ Eng 139:410–421

    Article  CAS  Google Scholar 

  • Ansari A (2004) Dirty bomb pills, shots, weeds and spells. Health Phys News 32:1–7

    Google Scholar 

  • ATSDR (2004a) Public health statement: Cesium. Division of Toxicology, Agency for Toxic Substances and Disease Registry, U.S. Department of Health and Human Services, Public Health Service, Atlanta. https://www.ncbi.nlm.nih.gov/books/NBK158855/pdf/Bookshelf_NBK158855.pdf. Accessed 3 March 2018

  • ATSDR (2004b) Public Health Statement: Strontium. Division of Toxicology, Agency for Toxic Substances and Disease Registry, U.S. Department of Health and Human Services, Public Health Service, Atlanta. https://www.atsdr.cdc.gov/ToxProfiles/tp159-c1-b.pdf. Accessed 8 April 2018

  • ATSDR (2013) Public Health Statement: Uranium. Agency for Toxic Substances and Disease Registry. U.S. Department of Health and Human Services, Public Health Service, Atlanta. https://www.atsdr.cdc.gov/ToxProfiles/tp150-c1-b.pdf. Accessed 25 Feb 2018

  • ATSDR (2004) Toxicological profile for strontium, Agency for Toxic Substances and Disease Registry. https://www.atsdr.cdc.gov/ToxProfiles/tp159-p.pdf. Accessed 29 Dec 2018

  • Aung WL, Kyaw N, Nway N (2013) Biosorption of Lead (Pb2+) by using Chlorella vulgaris. Int J Chem Environ Biol Sci 1:2320–4087

    Google Scholar 

  • Avery SV (1995) Caesium accumulation by microorganisms: uptake mechanisms, cation competition, compartmentalization and toxicity. J Ind Microbiol 14:76–84

    Article  CAS  PubMed  Google Scholar 

  • Barkleit A, Moll H, Bernhard G (2008) Interaction of uranium (VI) with lipopolysaccharid. Dalton Trans 21:2879–2886

  • Baselt RC, Cravey RH (1995) Disposition of toxic drugs and chemicals in man, 4th edn. Year Book Medical Publishers, Chicago, pp 105–107

    Google Scholar 

  • de Bashan LE, Bashan Y (2010) Immobilized microalgae for removing pollutants: review of practical aspects. Bioresour Technol 101:1611–1627

    Article  PubMed  CAS  Google Scholar 

  • Bates SS, Tessier A, Campbell PGC, Buffle J (1982) Zinc adsorption and transport by Chlamydomonas variabilis and Scenedesmus subspicatus (Chlorophyceae) grown in semicontinuous culture. J Phycol 18:521–529

    Article  CAS  Google Scholar 

  • Ben-Bassat D, Mayer AM (1977) Reduction of mercury chloride by Chlorella: Evidence for a reducing factor. Physiol Plant 40:157–162

    Article  CAS  Google Scholar 

  • Birungi ZS, Chirwa EMN (2015) The adsorption potential and recovery of thallium using green micro-algae from eutrophic water sources. J Hazard Mater 299:67–77

    Article  CAS  PubMed  Google Scholar 

  • Brouers M, de Jong H, Shi DJ, Hall DO (1989) Immobilized cells: An appraisal of the methods and applications of cell immobilization techniques. In: Cresswell RC, Rees TAV, Shah N (eds) Algae and Cyanobacterial Biotechnology. Longman Scientific and Technical Publishers, London, pp 272–290

    Google Scholar 

  • Calvo-Perez Rodo JD, Molinari-Novoa EA (2015) A nomenclatural and cultural note on Chlorella peruviana G. Chacon and other species of the genus Chlorella Beij. (Chlorellales, Chlorellaceae). Biologist 13:71–74

    Google Scholar 

  • Caravati EM, Erdman AR, Christianson G, Nelson LS, Woolf AD, Booze LL, Cobaugh DJ, Chyka PA, Scharman EJ, Manoguerra AS, Troutman WG (2008) Elemental mercury exposure: an evidence-based consensus guideline for out-of-hospital management. Clin Toxicol (Phila) 46:1–21

    Article  CAS  Google Scholar 

  • Cassatt DR, Kaminski JM, Hatchett RJ, DiCarlo AL, Benjamin JM, Maidment BW (2008) Medical countermeasures against nuclear threats: Radionuclide decorporation agents. Radiat Res 170:540–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • CBS News (2011) Expert: Japan botching crisis management, iodine distribution. CBS News, March 16. Available at: https://www.cbsnews.com/news/expert-japan-botching-crisis-management-iodine-distribution/ [Accessed on July 27, 2018]

  • Champenois J, Marfaing H, Pierre R (2015) Review of the taxonomic revision of Chlorella and consequences for its food uses in Europe. J Appl Phycol 27:1845–1851

    Article  Google Scholar 

  • Chen Z, Ma W, Han M (2008) Biosorption of nickel and copper onto treated alga (Undaria pinnatifida): Application of isotherm and kinetic models. J Hazard Mater 155:327–333

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Song S, Wen Y (2016) Reduction of Cr(VI) into Cr(III) by organelles of Chlorella vulgaris in aqueous solution: An organelle-level attempt. Sci Total Environ 572:361–368

    Article  CAS  PubMed  Google Scholar 

  • Chin FK (2007) Scenario of a dirty bomb in an urban environment and acute management of radiation poisoning and injuries. Singap Med J 48:950–957

    CAS  Google Scholar 

  • Cohen D (1962) Specific binding of rubidium in Chlorella. J Gen Physiol 45:959–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costa ACA, Leite SGF (1990) Cadmium and zinc biosorption by Chlorella homosphaera. Biotechnol Lett 12:941–944

    Article  CAS  Google Scholar 

  • Darnall DW, Greene B, Henzl MT, Hosea JM, McPherson RA, Sneddon J, Alexander MD (1986) Selective recovery of gold and other metal ions from an algal biomass. Environ Sci Technol 20:206–208

    Article  CAS  PubMed  Google Scholar 

  • De Filippis LF (1978) The effects of sub-lethal concentrations of mercury and zinc on Chlorella. IV. Characteristics of a general reducing system for metallic ions. Z Pflanzenphysiol 86:339–352

    Article  Google Scholar 

  • De Filippis LF, Pallaghy CK (1976) The effects of sub-lethal concentrations of mercury and zinc on Chlorella. III. Development and possible mechanisms of resistance to metals. Z Pflanzenphysiol 79:332–335

    Article  Google Scholar 

  • Devars S, Aviles C, Cervantes C, Moreno-Sanchez R (2000) Mercury uptake and removal by Euglena gracilis. Arch Microbiol 174:75–80

    Article  Google Scholar 

  • Donmez GC, Aksu Z, Ozturk A, Kutsal T (1999) A comparative study on heavy metal biosorption characteristics of some algae. Process Biochem 34:885–892

    Article  CAS  Google Scholar 

  • Doshi H, Ray A, Kothari IL, Gami B (2006) Spectroscopic and scanning electron microscopy studies of bioaccumulation of pollutants by algae. Curr Microbiol 53:148–157

    Article  CAS  PubMed  Google Scholar 

  • Dunstana RM, Lipsztein JL, Oliveira CAN, Bertelli L (1994) 137Cs Internal contamination involving a brazilian accident, and the efficacy of Prussian Blue treatment. Health Phys 66:245–252

    Article  Google Scholar 

  • Edris G, Alhamed Y, Alzahrani A (2014) Biosorption of cadmium and lead from aqueous solutions by Chlorella vulgaris biomass: equilibrium and kinetic study. Arab J Sci Eng 39:87–93

    Article  CAS  Google Scholar 

  • EPA (2017) Radionuclide Basics: Strontium-90. Radiation Protection. United States Environmental Protection Agency (US EPA), August 8 2017. https://www.epa.gov/radiation/radionuclide-basics-strontium-90 [Accessed 10 June 2019]

  • FDA (2006) Guidance for Industry Internal Radioactive Contamination - Development of Decorporation Agents. U.S. Department of Health and Human Services, Food and Drug Administration (FDA), Center for Drug Evaluation and Research, pp 1–22. https://www.fda.gov/media/71589/download. Accessed 10 May 2020

  • Fernandes B, Dragone G, Abreu AP, Geada P, Teixeira J, Vicente A (2012) Starch determination in Chlorella vulgaris - a comparison between acid and enzymatic methods. J Appl Phycol 24:1203–1208

    Article  CAS  Google Scholar 

  • Ferreira LS, Rodrigues MS, de Carvalho JCM, Lodi A, Finocchio E, Perego P, Converti A (2011) Adsorption of Ni2+, Zn2+ and Pb2+ onto dry biomass of Arthrospira (Spirulina) platensis and Chlorella vulgaris. I. Single metal systems. Chem Eng J 173:326–333

    Article  CAS  Google Scholar 

  • Foldes I, Levay A, Stotz G (1993) Comparative scanning of thyroid nodules with technetium-99m pertechnetate and technetium-99m methoxyisobutylisonitrile. Eur J Nucl Med 20:330–333

    Article  CAS  PubMed  Google Scholar 

  • Fradique M, Batista AP, Nunes MC, Gouveia L, Bandarra NM, Raymundo A (2010) Incorporation of Chlorella vulgaris and Spirulina maxima biomass in pasta products. Part1:preparation and evaluation. J Sci Food Agric 90:1656–1664

    Article  CAS  PubMed  Google Scholar 

  • Fraile A, Penche S, González F, Blázquez ML, Muñoz JA, Ballester A (2005) Biosorption of copper, zinc, cadmium and nickel by Chlorella vulgaris. J Chem Ecol 21:61–75

    Article  CAS  Google Scholar 

  • Friberg L, Nordberg GF, Kessler E, Vouk VB (eds) (1986) Handbook of the Toxicology of Metals,  Vols I, II, 2nd edn. Elsevier, Amsterdam

  • Fujiwara Y, Hirakawa K, Sinpo K (1990) Effect of long-term administration of Chlorella tablets on hyperlipemia. J Jpn Soc Nutr Food Sci 43:167–173

    Article  CAS  Google Scholar 

  • Gadd GM (1988) Accumulation of metals by microorganisms and algae. In: Rehm HJ (ed) Biotechnology-A Comprehensive Treatise,  Vol 6b. VCH, Weinheim, pp 401–434

  • Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46:834–840

    Article  CAS  Google Scholar 

  • Garland LH, Heald JH (1957) Radioactive isotopes in the diagnosis and treatment of cancer. JAMA 164:1096–1098

    Article  CAS  Google Scholar 

  • Geoffrey WG, Geoffrey AC, Geoffrey MG (1992) Accumulation of cobalt, zinc and manganese by the estuarine green microalga Chlorella salina immobilized in alginate micro beads. Environ Sci Technol 26:1764–1770

    Article  Google Scholar 

  • Gokhale SV, Jyoti KK, Lele SS (2008) Kinetic and equilibrium modeling of chromium(VI) biosorption on fresh and spent Spirulina platensis/Chlorella vulgaris bio- mass. Bioresour Technol 99:3600–3608

    Article  CAS  PubMed  Google Scholar 

  • Guo P, Wang J, Li X, Zhu J, Reinert T, Heitmann J, Spemann D, Vogt J, Flagmeyer RH, Butz T (2000) Study of metal bioaccumulation by nuclear microprobe analysis of algae fossils and living algae cells. Nucl Instrum Meth Phys Res B 161-163:801–807

    Article  CAS  Google Scholar 

  • Hameed MSA (2006) Continuous removal and recovery of lead by alginate beads, free and alginate-immobilized Chlorella vulgaris. Afr J Biotechnol 5:1819–1823

    Google Scholar 

  • Han X, Wong YS, Tam NFY (2006) Surface complexation mechanism and modeling in Cr(III) biosorption by a microalgal isolate, Chlorella miniata. J Colloid Interface Sci 303:365–371

    Article  CAS  PubMed  Google Scholar 

  • Hart A, Scaife D (1977) Toxicity and bioaccumulation of cadmium in Chlorella pyrenoidosa. Environ Res 413:401–413

    Article  Google Scholar 

  • Hasegawa T, Okuda M, Makino M, Hiromatsu K, Nomoto K, Yoshikai Y (1995) Hot water extracts of Chlorella vulgaris reduce opportunistic infection with Listeria monocytogenes in C57BL/6 mice infected with LP-BM5 murine leukemia viruses. Int J Immunopharmacol 17:505–512

    Article  CAS  PubMed  Google Scholar 

  • Haug A (1967) The affinity of some divalent metals to different types of alginates. Acta Chem Scand 15:1794–1795

    Article  Google Scholar 

  • Hegewald E (2000) New combinations in the genus Desmodesmus (Chlorophyceae, Scenedesmaceae). Algol Stud 96:1–18

    Google Scholar 

  • Horikoshi T, Nakajima A, Sakaguchi T (1979) Uptake of uranium by Chlorella regularis. Agric Biol Chem 43:617–623

    CAS  Google Scholar 

  • IARC (1993) Monographs-Cadmium. International Agency for Research on Cancer, Lyon, France

    Google Scholar 

  • Inaba J, Nishimura Y, Ichikawa R (1980) Comparative metabolism of 54Mn, 59Fe, 60Co and 65Zn incorporated into Chlorella and in inorganic form in rats. Health Phys 39:611–617

    Article  CAS  PubMed  Google Scholar 

  • Inthorn D, Sidtitoon N, Silapanuntakul S, Incharoensakdi A (2002) Sorption of mercury, cadmium and lead by microalgae. Sci Asia 28:253–261

    Article  CAS  Google Scholar 

  • Kalin M, Wheeler WN, Meinrath G (2005) The removal of uranium from mining waste water unsing algal/microbial biomass. J Environ Radioact 78:151–177

    Article  CAS  PubMed  Google Scholar 

  • Kalina T, Puncocharova M (1987) Taxonomy of the subfamily Scotiellocystoideae Fott 1976 (Chlorellaceae, Chlorophyceae). Algol Stud 45:473–521

    Google Scholar 

  • Kambe-Honjoh H, Sugawara A, Yoda K, Kitamoto K, Yamasaki M (1997) Isolation and Characterization of Nickel-accumulating Yeast. Appl Microbiol Biotechnol 48(3):373–378

  • Kapoor A, Viraraghavan T, Roy D (1999) Removal of Heavy Metals using the Fungus Aspergillus niger. Bioresour Technol 70:95–104

  • Khoo KM, Ting YP (2001) Biosorption of Gold by Immobilized Fungal Biomass. Biochem Eng J 8:51–59

  • Khummongkol D, Canterford GS, Freyer C (1982) Accumulation of heavy metals in unicellular algae. Biotechnol Bioeng 12:2643–2660

    Article  Google Scholar 

  • Klaassen CD (ed) (2013) Casarett & Doull's Toxicology, The Basic Science of Poisons, Eighth edn. McGraw-Hill, New York

  • Klimmek S, Stan HJ, Wilke A, Bunke G, Buchholz R (2001) Comparative analysis of the biosorption of cadmium, lead, nickel, and zinc by algae. Environ Sci Technol 35:4283–4288

    Article  CAS  PubMed  Google Scholar 

  • Knorr D (1991) Recovery and utilization of chitin and chitosan in food processing waste management. Food Technol 45:114–122

  • Konishi F, Tanaka K, Himeno K, Taniguchi K, Nomoto K (1985) Antitumor effect induced by a hot water extract of Chlorella vulgaris (CE): resistance to Meth-A tumor growth mediated by CE-induced polymorphonuclear leukocytes. Cancer Immunol Immunother 19:73–78

    Article  CAS  PubMed  Google Scholar 

  • Krienitz L, Hegewald EH, Hepperle D, Huss VAR, Rohr T, Wolf M (2004) Phylogenetic relationship of Chlorella and Parachlorella gen. nov. (Chlorophyta, Trebouxiophyceae). Phycologia 43:529–542

    Article  Google Scholar 

  • Lange-Bertalot H (1997) Frankophila, Mayamaea und Fistulifera: drei neue Gattungen der Klasse Bacillariophyceae. Arch Protistenkd 148:65–76

    Article  Google Scholar 

  • Lau PS, Lee HY, Tsang CCK, Tam NFY, Wong YS (1999) Effect of metal interference, pH and temperature on Cu and Ni biosorption by Chlorella vulgaris and Chlorella miniata. Environ Technol 20:953–961

    Article  CAS  Google Scholar 

  • Lee SH, Kang HJ, Lee HJ, Kang MH, Park YK (2010) Six-week supplementation with Chlorella has favorable impact on antioxidant status in Korean male smokers. Nutrition 26:175–183

    Article  CAS  PubMed  Google Scholar 

  • Lee KY, Lee SH, Lee JE, Lee SY (2019) Biosorption of radioactive cesium from contaminated water by microalgae Haematococcus pluvialis and Chlorella vulgaris. J Environ Manag 233:83–88

    Article  CAS  Google Scholar 

  • Leyssens L, Vinck B, Van Der Straeten C, Wuyts F, Maes L (2017) Cobalt toxicity in humans. A review of the potential sources and systemic health effects. Toxicology 387:43–56

    Article  CAS  PubMed  Google Scholar 

  • Li HB, Jiang Y, Chen F (2002) Isolation and purification of lutein from the microalga Chlorella vulgaris by extraction after saponification. J Agric Food Chem 50:1070–1072

    Article  CAS  PubMed  Google Scholar 

  • Liang S, Liu X, Chen F, Chen Z (2004) Current microalgal health food R&D activities in China. Hydrobiologia 512:45–48

    Article  Google Scholar 

  • Lie R, Thomas RG, Scott JK (1960) The distribution and excretion of thallium-204 in the rat, with suggested MPC's and a bio-assay procedure. Health Phys 2:334–340

    Article  CAS  PubMed  Google Scholar 

  • Lipsztein JL, Cunha PG, Oliveira CAN (1990) The Goiania accident: behind the scenes. Health Phys 60:5–6

    Google Scholar 

  • Mehta SK, Gaur JP (2001) Characterization and optimization of Ni and Cu sorption from aqueous solution by Chlorella vulgaris. Ecol Eng 18:1–13

    Article  Google Scholar 

  • Mehta SK, Gaur JP (2005) Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit Rev Biotechnol 25:113–152

    Article  CAS  PubMed  Google Scholar 

  • Mehta SK, Singh A, Gaur JP (2002) Kinetics of adsorption and uptake of Cu2+ by Chlorella vulgaris: influence of pH, temperature, culture age, and cations. J Environ Sci Health A 37:399–414

    Article  CAS  Google Scholar 

  • Merchant RE, Rice CD, Young HF (1990) Dietary Chlorella pyrenoidosa for patients with malignant glioma: effects on immunocompetence, quality of life, and survival. Phytother Res 4:220–231

    Article  Google Scholar 

  • Morita K, Matsueda T, Iida T, Hasegawa T (1999) Chlorella accelerates dioxin excretion in rats. J Nutr 129:1731–1736

    Article  CAS  PubMed  Google Scholar 

  • Muller H, ter Meer-Bekk C (1991) Technetium uptake by the green alga Chlorella fusca. J Radioanal Nucl Chem 154:37–39

    Article  Google Scholar 

  • Muñoz R, Guieysse B (2006) Algal–bacterial processes for the treatment of hazardous contaminants: A review. Water Res 40:2799–2815

    Article  PubMed  CAS  Google Scholar 

  • Nakajima A, Horikoshi T, Sakaguchi T (1979) Ion effects on the uptake of uranium by Chlorella regularis. Agric Biol Chem 43:625–629

    CAS  Google Scholar 

  • Nguema PF, Luo Z, Lian J (2014) The biosorption of Cr(VI) ions by dried biomass obtained from a chromium-resistant bacterium. Front Chem Sci Eng 8:454–464

    Article  CAS  Google Scholar 

  • Nuclear and Industrial Safety Agency website (n.d.) Regarding the evaluation of the conditions on reactor cores of unit 1, 2 and 3 related to the accident at Fukushima Dai-ichi nuclear power station, Tokyo Electric Power Co. Inc. Available: http://www.nisa.meti.go.jp/english/press/2011/06/en20110615-5.pdf. [Accessed on 2018 August 8]

  • OECD-NEA (2002) Chernobyl: Assessment of Radiological and Health Impact, 2002 update; Chapter IV-Dose Estimate, pp 61–75. https://www.oecd-nea.org/jcms/pl_28312/chernobyl-chapter-iv-dose-estimates. Accessed 20 Dec 2020

  • Ogawa K, Fukuda T, Han J, Kitamura Y, Shiba K, Odani A (2016) Evaluation of Chlorella as a decorporation agent to enhance the elimination of radioactive strontium from body. PLoS One 11:e0148080

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parab H, Joshi S, Shenoy N, Verma R, Lali A, Sudersanan M (2005) Uranium removal from aqueous solution by coir pith: Equilibrium and kinetic studies. Bioresour Technol 96:1241–1248

    Article  CAS  PubMed  Google Scholar 

  • Paschal DC, Burt V, Caudill SP, Gunter EW, Pirkle JL, Sampson EJ, Miller DT, Jackson RJ (2000) Exposure of the U.S. population aged 6 years and older to cadmium: 1988-1994. Arch Environ Contam Toxicol 38:377–383

    Article  CAS  PubMed  Google Scholar 

  • Pau PWI (2000) Management of thallium poisoning. Hong Kong Med J 6:316–318

    CAS  PubMed  Google Scholar 

  • Petrovič A, Simonič M (2016) Removal of heavy metal ions from drinking water by alginate-immobilised Chlorella sorokiniana. Int J Environ Sci Technol 13:1761–1780

    Article  CAS  Google Scholar 

  • Puranik PR, Modak JM, Paknikar KM (1999) A comparative study of the mass transfer kinetics of metal biosorption by microbial biomass. Hydrometallurgy 52:189–198

    Article  CAS  Google Scholar 

  • Regalado L, Gagneten AM, Troiani H (2009) Accumulation of chromium and interaction with other elements in Chlorella vulgaris (Cloroficeae) and Daphnia magna (Crustacea, Cladocera). J Environ Biol 30:213–216

    Google Scholar 

  • Rezaei H, Kulkarni SD, Saptarshi PG (2012) Study of physical chemistry on biosorption of zinc by using Chlorella pyrenoidosa. Russ J Phys Chem 86:1332–1339

    Article  CAS  Google Scholar 

  • Riaz M, Nadeem R, Hanif MA, Ansari TM, Rehman KU (2009) Pb(II) biosorption from hazardous aqueous streams using Gossypium hirsutum (cotton) waste biomass. J Hazard Mater 161:88–194

    Article  CAS  PubMed  Google Scholar 

  • Robinson P (1981) Management of persons accidentally contaminated with radionuclides. NCRP Report No. 65. J R Soc Med 74:562

    Article  PubMed Central  Google Scholar 

  • Rodriguez-Garcia I, Guil-Guerrero JL (2008) Evaluation of the antioxidant activity of three microalgal species for use as dietary supplements and in the preservation of foods. Food Chem 108:1023–1026

    Article  CAS  PubMed  Google Scholar 

  • Romera E, González F, Ballester A, Blázquez ML, Muñoz JA (2006) Biosorption with algae: A statistical review. Crit Rev Biotechnol 26:223–235

    Article  CAS  PubMed  Google Scholar 

  • Rotkovska D, Vatsek A, Bartonichkova A (1989) Increase in the radiation resistance of mice using Ivastimul. Radiobiologiia 29:652–654

    CAS  PubMed  Google Scholar 

  • Roy D, Greenlaw PN, Shane BS (1993) Adsorption of heavy metals by green algae and ground rice hulls. J Environ Sci Health A 28:37–50

    Google Scholar 

  • Safi C, Zebib B, Merah O, Pontalier PY, Vaca-Garcia C (2014) Morphology, composition, production, processing and applications of Chlorella vulgaris: A review. Renew Sustain Energy Rev 35:265–278

    Article  Google Scholar 

  • Saitoh T, Nakagaki N, Uchida Y, Hiraide M, Matsubara C (2001) Spectrophotometric determination of some functional groups on Chlorella for the evaluation of their contribution to metal uptake. Anal Sci 17:793–795

    Article  CAS  PubMed  Google Scholar 

  • Sandau E, Sandau P, Pulz O, Zimmermann M (1996) Heavy metal sorption by marine algae and algal by-products. Acta Biotechnol 16:103–119

    Article  CAS  Google Scholar 

  • Sapienza MT, Willegaignon J (2019) Radionuclide therapy: current status and prospects for internal dosimetry in individualized therapeutic planning. Clinics (Sao Paulo) 74:e835

  • Sarma L, Tiku AB, Kesavan PC, Ogaki M (1993) Evaluation of radioprotective action of a mutant (E-25) form of Chlorella vulgaris in mice. J Radiat Res 34:277–284

    Article  CAS  PubMed  Google Scholar 

  • Sharma RM, Azeez PA (1988) Accumulation of copper and cobalt by blue-green algae at different temperatures. Int J Environ Anal Chem 32:87–95

    Article  Google Scholar 

  • Sharma P, Tomar R (2008) Synthesis and application of an analogue of mesolite for the removal of uranium (VI), thorium (IV), and europium (III) from aqueous waste. Microporous Mesoporous Mater 116:641–652

    Article  CAS  Google Scholar 

  • Shen QH, Zhi TT, Cheng LH, Xu XH, Chen HL (2013) Hexavalent chromium detoxification by nonliving Chlorella vulgaris cultivated under tuned conditions. Chem Eng J 228:993–1002

    Article  CAS  Google Scholar 

  • Shim JE, Son YA, Park JM, Kim MK (2009) Effect of Chlorella intake on Cadmium metabolism in rats. Nutr Res Pract 3:15–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimura H, Itoh K, Sugiyama A, Ichijo S, Ichijo M, Furuya F, Nakamura Y, Kitahara K, Kobayashi K, Yukawa Y, Kobayash T (2012) Absorption of radionuclides from the Fukushima nuclear accident by a novel algal strain. PLoS One 7:e44200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shuren J (2005) Draft Guidance for industry on Internal radioactive contamination-Development of decorporation agents; availability. Food and Drug Administration, HHS. Fed Regist 70:7747–7748

    Google Scholar 

  • Sigg L, Xue H (1994) Metal speciation: Concepts. Analysis and effects. In: Bidoglio G, Stumm W (eds) Chemistry of Aquatic Systems: Local and Global Perspectives. EUROCOURSES (Chemical and Environmental Science), Springer, Dordrecht 5:153–181

    CAS  Google Scholar 

  • Singh SP, Tiku AB, Kesavan PC (1995) Post-exposure radioprotection by Chlorella vulgaris (E-25) in mice. Indian J Exp Biol 33:612–615

    CAS  PubMed  Google Scholar 

  • Singhal RL, Merali Z, Hrdina PD (1976) Aspects of the biochemical toxicology of cadmium. Fed Proc 35:75–80

    CAS  PubMed  Google Scholar 

  • Smithers DW (1958) The therapeutic use of radioactive isotopes. Ann R Coll Surg Engl 23:238–247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Solisio C, Al Arni S, Converti A (2017) Adsorption of inorganic mercury from aqueous solutions onto dry biomass of Chlorella vulgaris: kinetic and isotherm study. Environ Technol 3330:1–9

    Google Scholar 

  • Švadlenková M, Lukavský J, Kvíderová J (2005) Radionuclides 137Cs and 60Co uptake by freshwater and marine microalgae Chlorella, Navicula, Phaeodactylum. In: Bréchignac F, Desmet G (eds) Equidosimetry — Ecological Standardization and Equidosimetry for Radioecology and Environmental Ecology. NATO Security through Science Series (Series C: Environmental Security). Springer, Dordrecht, pp 379–387

  • Sydney EB, Novak AC, de Carvalho JC, Soccol CR (2014) Respirometric balance and carbon fixation of industrially important algae. In: Pandey A, Lee D-J, Chisti Y, Soccol C (eds) Biofuels from algae. Elsevier, Amsterdam, pp 379–387

  • Takata H, Kusakabe M, Inatomi N, Ikenoue T (2018) Appearances of Fukushima Daiichi Nuclear Power Plant-derived Cs-137 in coastal waters around Japan: Results from marine monitoring off nuclear power plants and facilities, 1983-2016. Environ Sci Technol 52:2629–2637

    Article  CAS  PubMed  Google Scholar 

  • Takekoshi H, Suzuki G, Chubachi H, Nakano M (2005) Effect of Chlorella pyrenoidosa on fecal excretion and liver accumulation of polychlorinated dibenzo-p-dioxin in mice. Chemosphere 59:297–304

    Article  CAS  PubMed  Google Scholar 

  • Tam NFY, Wong YS, Simpson CG (1998) Removal of Copper by Free and Immobilized Microalga, Chlorella vulgaris. In: Wong YS, Tam NFY (eds) Wastewater Treatment with Algae. Springer, Berlin, pp 17–36

  • Tanaka K, Konishi F, Himeno K, Taniguchi K, Nomoto K (1984) Augmentation of antitumor resistance by a strain of unicellular green algae, Chlorella vulgaris. Cancer Immunol Immunother 17:90–94

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Yamada A, Noda K, Shoyama Y, Kubo C, Nomoto K (1997) Oral administration of a unicellular green algae, Chlorella vulgaris, prevents stress-induced ulcer. Planta Med 63:465–466

    Article  CAS  PubMed  Google Scholar 

  • Tatarová D, Galanda D, Kuruc J, Gaálová B (2021) Phytoremediation of 137Cs, 60Co, 241Am, and 239Pu from aquatic solutions using Chlamydomonas reinhardtii, Scenedesmus obliquus, and Chlorella vulgaris. Int J Phytoremediat 23:1376–1381

    Article  CAS  Google Scholar 

  • Testa HJ, Shields RA (1981) Management of persons accidentally contaminated with radionuclides. Int J Radiat Biol Relat Stud Phys Chem Med 39:232

    Article  Google Scholar 

  • Thompson DF, Callen ED (2004) Soluble or insoluble prussian blue for radiocesium and thallium poisoning? Ann Pharmacother 38:1509–1514

    Article  CAS  PubMed  Google Scholar 

  • Tien C, Sigee DC, White KN (2005) Copper adsorption kinetics of cultured algal cells and fresh water phytoplankton with emphasis on cell surface characteristics. J Appl Phycol 17:379–389

    Article  CAS  Google Scholar 

  • Ting YP, Lawson F, Prince IG (1989) Uptake of cadmium and zinc by the alga Chlorella vulgaris: Part 1. Individual ion species. Biotechnol Bioeng 34:990–999

    Article  CAS  PubMed  Google Scholar 

  • Ting YP, Teo WK, Soh CY (1995) Gold uptake by Chlorella vulgaris. J Appl Phycol 7:97–100

    Article  CAS  Google Scholar 

  • Uchikawa T, Maruyama I, Kumamoto S, Ando Y, Yasutake A (2011) Chlorella suppresses methylmercury transfer to the fetus in pregnant mice. J Toxicol Sci 36:675–680

    Article  CAS  PubMed  Google Scholar 

  • Unni PR, Kothari K, Pillai MRA (2001) Radiochemical processing of radionulides (105Rh, 166Ho, 153Sm, 186Re and 188Re) for targeted radiotherapy. International seminar on therapeutic applications of radiopharmaceuticals; Hyderabad (India); 18-22 Jan 1999. International Atomic Energy Agency, Vienna, pp 90–98

  • Vacek A, Rotkovská D, Bartonícková A (1990) Radioprotection of hemopoiesis conferred by aqueous extract from chlorococcal algae (Ivastimul) administered to mice before irradiation. Exp Hematol 18:234–237

    CAS  PubMed  Google Scholar 

  • Vogel M, Gunther A, Rossberg A, Li B, Bernhard G, Raff J (2010) Biosorption of U (VI) by the green algae Chlorella vulgaris in dependence of pH value and cell activity. Sci Total Environ 409:384–395

    Article  CAS  PubMed  Google Scholar 

  • Volesky B, May H, Holan ZR (1993) Cadmium Biosorption by Saccharomyces cerevisiae. Biotechnol Bioeng 41:826–829

  • Wan-Maznah WO, Al-Fawwaz AT, Surif M (2012) Biosorption of copper and zinc by immobilised and free algal biomass, and the effects of metal biosorption on the growth and cellular structure of Chlorella sp. and Chlamydomonas sp. isolated from rivers in Penang, Malaysia. J Environ Sci (China) 24:1386–1393

    Article  CAS  Google Scholar 

  • Wehrheim B, Wettern M (1994) Biosorption of cadmium, copper and lead by isolated mother cell walls and whole cells of Chlorella fusca. Appl Microbiol Biotechnol 41:725–728

    Article  CAS  Google Scholar 

  • Wilkinson SC, Goulding KH, Robinson PK (1990) Mercury removal by immobilized algae in batch culture systems. J Appl Phycol 2:223–230

    Article  Google Scholar 

  • Wong MH, Pak DCH (1992) Removal of copper and nickel by free and immobilized microalgae. Biomed Environ Sci 5:99–108

    CAS  PubMed  Google Scholar 

  • Wong JP, Wong Y, Tam NF (2000) Nickel biosorption by two Chlorella species, C. vulgaris (a commercial species) and C. miniata (a local isolate). Bioresour Technol 73:133–137

    Article  CAS  Google Scholar 

  • Wood R, Sharp C, Gourmelon P, Le Guen B, Stradling GN, Taylor DM, Hengé-Napoli MH (2000) Decorporation treatment-medical overview. Radiat Prot Dosim 87:51–57

    Article  CAS  Google Scholar 

  • Wynne MJ, Guiry MD (2016). Tetradesmus lagerheimii M.J.Wynne & Guiry, nomen novum, a replacement name for Tetradesmus acuminatus (Lagerheim) M.J.Wynne, nom. illeg. (Sphaeropleales, Chlorophyta). Notulae Algarum 12:1

  • Yadav M, Rani K, Chauhan MK, Panwar A, Sandal N (2020) Evaluation of mercury adsorption and removal efficacy of pulverized Chlorella (C. vulgaris). J Appl Phycol 32:1253–1262

    Article  CAS  Google Scholar 

  • Yadav M, Soni R, Chauhan MK, Sandal N (2021) Cellular and physiological approaches to evaluate the chelating effect of Chlorella on metal ion stressed lymphocytes. Biometals 34:351–363

    Article  CAS  PubMed  Google Scholar 

  • Yadav M, Kumar V, Sandal N, Chauhan MK (2022a) Quantitative evaluation of Chlorella vulgaris for removal of toxic metals from body. J Appl Phycol. https://doi.org/10.1007/s10811-021-02640-8

  • Yadav M, Sharma P, Kushwah H, Sandal N, Chauhan MK (2022b) Assessment of the toxicological profile of Chlorella (C. vulgaris) powder by performing acute and sub-acute oral toxicity studies in mice. J Appl Phycol 34:363–373

    Article  CAS  Google Scholar 

  • Yamaguchi K (1996) Recent advances in microalgal bioscience in Japan, with special reference to utilization of biomass and metabolites: A review. J Appl Phycol 8:487–502

    Article  Google Scholar 

  • Yan H, Pan G (2002) Toxicity and bioaccumulation of copper in three green microalgal species. Chemosphere 49:471–476

    Article  CAS  PubMed  Google Scholar 

  • Yen HW, Chen PW, Hsu CY, Lee L (2017) The use of autotrophic Chlorella vulgaris in chromium(VI) reduction under different reduction conditions. J Taiwan Inst Chem Eng 74:1–6

    Article  CAS  Google Scholar 

  • Yeong CH, Cheng MH, Ng KH (2014) Therapeutic radionuclides in nuclear medicine: current and future prospects. J Zhejiang Univ Sci B 15:845–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgement

The authors would like to thanks Institute of Nuclear Medicine and Allied Sciences (INMAS), DRDO, New Delhi for providing all the necessary facilities and requirement to complete this review.

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Mahendra Yadav, Komal Rani and Nidhi Sandal: Conceptualization, Study Design, Literature Review, Data collection and Paper writing-Original draft; Meenakshi Kanwar Chauhan: Study design and draft reading and editing.

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Correspondence to Nidhi Sandal.

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Yadav, M., Rani, K., Sandal, N. et al. An approach towards safe and sustainable use of the green alga Chlorella for removal of radionuclides and heavy metal ions. J Appl Phycol 34, 2117–2133 (2022). https://doi.org/10.1007/s10811-022-02771-6

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