Abstract
In the last few years, due to vigorous expansion of industrialization, toxic metals appear to be in excessive levels in the environment. Ecosystems are now severely threatened by such widespread pollutants. Current reviews show that technologies that are used to remediate infected areas appear to have low efficiency, and this has brought on the need for further investigation. Among biological and non-biological methods which have been proposed for removing such pollutants from the environment, phycoremediation seems to be advantageous. Until recently, many microorganisms (such as fungi, bacteria and waste biomass) have been studied for their ability to remove toxic metals from the aqueous environment. In this review, it is shown that in particular, microalgae have received great attention lately, because of their ability to bind essential quantities of these pollutants. Phycoremediation involves the process of biosorption and bioaccumulation, both of which take part in the metal sequestration. A detailed description of either mechanism with respect to the parameters affecting them is reviewed in this work.
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References
Abbas SH, Ismail IM, Mostafa TM, Sulaymon AH (2014) Biosorption of heavy metals: a review. J Chem Sci Technol 3:74–102
Abdel-Ghani NT, El-Chaghaby GA (2014) Biosorption for metal ions removal from aqueous solutions: A review of recent studies. Int J Latest Res Sci Technol 3:24–42
Adhiya J, Cai X, Sayre RT, Traina SJ (2002) Binding of aqueous cadmium by the lyophilized biomass of Chlamydomonas reinhardtii. Colloids Surf A: Physicochem Eng Asp 210:1–11. https://doi.org/10.1016/S0927-7757(02)00041-9
Ahalya N, Ramachandra TV, Kanamadi RD (2003) Biosorption of heavy metals. Res J Chem Environ 7:71–79
Aharchaou I, Rosabal M, Liu F, Battaglia E, Vignati DAL, Fortin C (2017) Bioaccumulation and subcellular partitioning of Cr(III) and Cr(VI) in the freshwater green alga Chlamydomonas reinhardtii. Aquat Toxicol 182:49–57. https://doi.org/10.1016/j.aquatox.2016.11.004
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. https://doi.org/10.1016/S0032-9592(02)00051-1
Appenroth K-J (2010) Definition of “heavy metals” and their role in biological systems. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Berlin, pp 19–29. https://doi.org/10.1007/978-3-642-02436-8_2
Arbabi M, Golshani N (2016) Removal of copper ions Cu (II) from industrial wastewater. Int J Epidemiol Res 3:283–293
Arıca MY, Tüzün İ, Yalçın E, İnce Ö, Bayramoğlu G (2005) Utilisation of native, heat and acid-treated microalgae Chlamydomonas reinhardtii preparations for biosorption of Cr(VI) ions. Process Biochem 40:2351–2358. https://doi.org/10.1016/j.procbio.2004.09.008
Arief VO, Trilestari K, Sunarso J, Indraswati N, Ismadji S (2008) Recent progress on biosorption of heavy metals from liquids using low cost biosorbents: characterization, biosorption parameters and mechanism studies. CLEAN Soil Air Water 36:937–962. https://doi.org/10.1002/clen.200800167
Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32:180. https://doi.org/10.1007/s11274-016-2137-x
Bayramoğlu G, Tuzun I, Celik G, Yilmaz M, Arica MY (2006) Biosorption of mercury(II), cadmium(II) and lead(II) ions from aqueous system by microalgae Chlamydomonas reinhardtii immobilized in alginate beads. Int J Min Process 81:35–43. https://doi.org/10.1016/j.minpro.2006.06.002
Beckett WS, Nordberg GF, Clarkson TW (2007) Routes of exposure, dose, and metabolism of metals. In: Toprak MS, Karlsson HL, Fadeel B (eds) Handbook on the toxicology of metals, 3rd edn. Academic Press, Burlington, pp 39–64. https://doi.org/10.1016/B978-012369413-3/50058-6
Berner F, Heimann K, Sheehan M (2015) Microalgal biofilms for biomass production. J Appl Phycol 27:1793–1804. https://doi.org/10.1007/s10811-014-0489-x
Bhatnagar SK, Reeta (2013) Bioremediation: a sustainable tool for environmental management—a review. Ann Rev Res Biol 3:974–993
Bjerregaard P, Andersen O (2007) Ecotoxicology of metals—sources, transport, and effects in the ecosystem. In: Friber L, Langard S, Norseth T (eds) Handbook on the toxicology of metals, 3rd edn. Academic Press, Burlington, pp 251–280. https://doi.org/10.1016/B978-012369413-3/50068-9
Bjørklund G, Aaseth J, Ajsuvakova OP, Nikonorov AA, Skalny AV, Skalnaya MG, Tinkov AA (2017) Molecular interaction between mercury and selenium in neurotoxicity. Coord Chem Rev 332:30–37. https://doi.org/10.1016/j.ccr.2016.10.009
Bonanno G, Borg JA, Di Martino V (2017) Levels of heavy metals in wetland and marine vascular plants and their biomonitoring potential: A comparative assessment. Sci Total Environ 576:796–806. https://doi.org/10.1016/j.scitotenv.2016.10.171
Bridges CC, Zalups RK (2010) Ionic and molecular mimicry and the transport of metals. In: Zalups RK, Koropatnick DJ (eds) Cellular and molecular biology of metals. CRC Press, Boca Raton, pp 241–294. https://doi.org/10.1201/9781420059984-c10
Brinza L, Dring M, Gavrilescu M (2007) Marine micro and macro algal species as biosorbents for heavy metals. Environ Eng Manag J (EEMJ) 6:237–251
Cai XH, Brown C, Adhiya J, Traina SJ, Sayre RT (1999) Growth and heavy metal binding properties of transgenic Chlamydomonas expressing a foreign metallothionein gene. Int J Phytoremed 1:53–65. https://doi.org/10.1080/15226519908500004
Chojnacka K (2010) Biosorption and bioaccumulation–the prospects for practical applications. Environ Int 36:299–307. https://doi.org/10.1016/j.envint.2009.12.001
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182. https://doi.org/10.1146/annurev.arplant.53.100301.135154
Costa GB, Simioni C, Ramlov F, Maraschin M, Chow F, Bouzon ZL, Schmidt ÉC (2017) Effects of manganese on the physiology and ultrastructure of Sargassum cymosum. Environ Exp Bot 133:24–34. https://doi.org/10.1016/j.envexpbot.2016.09.007
Dao LHT, Beardall J (2016) Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere 147:420–429. https://doi.org/10.1016/j.chemosphere.2015.12.117
Das N, Vimala R, Karthika P (2008) Biosorption of heavy metals-an overview Indian. J Biotechnol 7:159–169
Davidson T, Ke Q, Costa MAX (2007) Selected Molecular Mechanisms of Metal Toxicity and Carcinogenicity. In: Toprak MS, Karlsson HL, Fadeel B (eds) Handbook on the toxicology of metals. Academic Press, Burlington, pp 79–100. https://doi.org/10.1016/B978-012369413-3/50060-4
Duffus JH (2002) “ Heavy metals” a meaningless term? (IUPAC Technical Report). Pure Appl Chem 74:793–807
Dziegiel P, Pula B, Kobierzycki C, Stasiolek M, Podhorska-Okolow M (2016) Introduction. In: Dziegiel P, Pula B, Kobierzycki C, Stasiolek M (eds) Metallothioneins in normal and cancer cells. Springer, Cham, pp 1–2. https://doi.org/10.1007/978-3-319-27472-0_1
Flouty R, Estephane G (2012) Bioaccumulation and biosorption of copper and lead by a unicellular algae Chlamydomonas reinhardtii in single and binary metal systems: a comparative study. J Environ Manag 111:106–114. https://doi.org/10.1016/j.jenvman.2012.06.042
Gani P et al. The potential of biodiesel production from Botryococcus sp. biomass after phycoremediation of domestic and industrial wastewater. In: IOP conference series: materials science and engineering, 2016. vol 1. IOP Publishing, London, p 012048
Gani P, Sunar NM, Matias-Peralta H, Abdul Latiff AA, Parjo UK, Ab Razak AR (2015) Phycoremediation of Wastewaters and Potential Hydrocarbon from Microalgae: a Review. Adv Environ Biol 9:1–8
Gaur JP, Rai LC (2001) Heavy Metal Tolerance in Algae. In: Rai LC, Gaur JP (eds) Algal adaptation to environmental stresses: physiological, biochemical and molecular mechanisms. Springer, Berlin, pp 363–388. https://doi.org/10.1007/978-3-642-59491-5_12
González F, Romera E, Ballester A, Blázquez ML, Muñoz JÁ, García-Balboa C (2011) Algal biosorption and biosorbents. In: Kotrba P, Mackova M, Macek T (eds) Microbial biosorption of metals. Springer, Dordrecht, pp 159–178. https://doi.org/10.1007/978-94-007-0443-5_7
González-Dávila M (1995) The role of phytoplankton cells on the control of heavy metal concentration in seawater. Mar Chem 48:215–236. https://doi.org/10.1016/0304-4203(94)00045-F
Gross M, Henry W, Michael C, Wen Z (2013) Development of a rotating algal biofilm growth system for attached microalgae growth with in situ biomass harvest. Bioresource Technol 150:195–201. https://doi.org/10.1016/j.biortech.2013.10.016
Gupta VK, Rastogi A (2008) Equilibrium and kinetic modelling of cadmium(II) biosorption by nonliving algal biomass Oedogonium sp. from aqueous phase. J Hazard Mater 153:759–766. https://doi.org/10.1016/j.jhazmat.2007.09.021
Hanikenne M, Merchant SS, Hamel P (2009) Transition metal nutrition: a balance between deficiency and toxicity the Chlamydomonas: organellar and metabolic processes, 2nd edn. David Stern, Ottawa
Henriques B et al (2016) Bioaccumulation of Hg, Cd and Pb by Fucus vesiculosus in single and multi-metal contamination scenarios and its effect on growth rate. Chemosphere 171:208–222. https://doi.org/10.1016/j.chemosphere.2016.12.086
Hirata K, Tsuji N, Miyamoto K (2005) Biosynthetic regulation of phytochelatins, heavy metal-binding peptides. J Biosci Bioeng 100:593–599. https://doi.org/10.1263/jbb.100.593
Hlihor R-M, Apostol L-C, Gavrilescu M (2017) Environmental Bioremediation by Biosorption and Bioaccumulation: Principles and Applications. In: Anjum NA, Gill SS, Tuteja N (eds) Enhancing Cleanup of Environmental Pollutants: Volume 1: Biological Approaches. Springer International Publishing, Cham, pp 289-315. https://doi.org/10.1007/978-3-319-55426-6_14
Hodson ME (2004) Heavy metals—geochemical bogey men? Environ Pollut 129:341–343. https://doi.org/10.1016/j.envpol.2003.11.003
Howe G, Merchant S (1992) Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiol 98:127–136
http://www.nature.com/articles/srep32305#supplementary-information
Inouhe M (2005) Phytochelatins Brazilian Journal of Plant Physiology 17:65–78
Irving TE, Allen DG (2011) Species and material considerations in the formation and development of microalgal biofilms. Appl Microbiol Biotechnol 92:283–294. https://doi.org/10.1007/s00253-011-3341-0
Jacquart A, Brayner R, El Hage Chahine J-M, Ha-Duong N-T (2017) Cd2+ and Pb2+ complexation by glutathione and the phytochelatins. Chem Biol Interact 267:2–10. https://doi.org/10.1016/j.cbi.2016.09.002
Jais NM, Mohamed RMSR, Al-Gheethi AA, Hashim MKA (2017) The dual roles of phycoremediation of wet market wastewater for nutrients and heavy metals removal and microalgae biomass production. Clean Technol Environ Policy 19:37–52. https://doi.org/10.1007/s10098-016-1235-7
Joshi R, Pareek A, Singla-Pareek SL (2016) Plant Metallothioneins: Classification, Distribution, Function, and Regulation. In: Plant Metal Interaction. Elsevier, pp 239-261. doi:http://dx.doi.org/10.1016/B978-0-12-803158-2.00009-6
Kadukova J, Vircikova E (2005) Comparison of differences between copper bioaccumulation and biosorption. Environ Int 31:227–232. https://doi.org/10.1016/j.envint.2004.09.020
Kanwar P, Mishra T, Mukherjee G (2017) Microbial Bioremediation of Hazardous Heavy Metals. In: Prashanthi M, Sundaram R, Jeyaseelan A, Kaliannan T (eds) Bioremediation and Sustainable Technologies for Cleaner Environment. Springer International Publishing, Cham, pp 281-293. https://doi.org/10.1007/978-3-319-48439-6_21
Kesaano M, Sims RC (2014) Algal biofilm based technology for wastewater treatment. Algal Res 5:231–240. https://doi.org/10.1016/j.algal.2014.02.003
Kondo K, Hirayama K, Matsumoto M (2013) Adsorption of metal ions from aqueous solution onto microalga entrapped into Ca-alginate gel bead. Desalinat Water Treat 51:4675–4683. https://doi.org/10.1080/19443994.2013.770236
Kratochvil D, Volesky B (1998) Advances in the biosorption of heavy metals. Trends Biotechnol 16:291–300
Kumar A, Bisht BS, Joshi VD, Dhewa T (2011) Review on bioremediation of polluted environment: a management tool. Ann Rev Res Biol 1:974–993
Lo YC, Cheng CL, Han YL, Chen BY, Chang JS (2014) Recovery of high-value metals from geothermal sites by biosorption and bioaccumulation. Bioresource Technol 160:182–190. https://doi.org/10.1016/j.biortech.2014.02.008
Ma L, Wang F, Yu Y, Liu J, Wu Y (2018) Cu removal and response mechanisms of periphytic biofilms in a tubular bioreactor. Bioresource Technol 248:61–67. https://doi.org/10.1016/j.biortech.2017.07.014
Macek T, Mackova M (2011) Potential of Biosorption Technology. In: Kotrba P, Mackova M, Macek T (eds) Microbial Biosorption of Metals. Springer Netherlands, Dordrecht, pp 7-17. https://doi.org/10.1007/978-94-007-0443-5_2
Malekzadeh R, Shahpiri A (2017) Independent metal-thiolate cluster formation in C-terminal Cys-rich region of a rice type 1 metallothionein isoform. Int J Biol Macromol 96:436–441. https://doi.org/10.1016/j.ijbiomac.2016.12.047
Margoshes M, Vallee BL (1957) A cadmium protein from equine kidney cortex. J Am Chem Soc 79:4813–4814. https://doi.org/10.1021/ja01574a064
Mejare M, Bulow L (2001) Metal-binding proteins and peptides in bioremediation and phytoremediation of heavy metals. Trends Biotechnol 19:67–73
Moffett DB, El-Masri HA, Fowler BA (2007) General Considerations of Dose-Effect and Dose-Response Relationships*. In: Handbook on the Toxicology of Metals (Third Edition). Academic Press, Burlington, pp 101-115. doi:http://doi.org/10.1016/B978-012369413-3/50061-6
Mora-Ravelo S, Rocandio-Rodriguez M, Vanoye-Eligio V (2017) Bioremediation of wastewater for reutilization in agricultural systems: a review. Appl Ecol Environ Res 15:33–50
Naja G, Volesky B (2011) The Mechanism of Metal Cation and Anion Biosorption. In: Kotrba P, Mackova M, Macek T (eds) Microbial Biosorption of Metals. Springer Netherlands, Dordrecht, pp 19-58. https://doi.org/10.1007/978-94-007-0443-5_3
Naja GM, Murphy V, Volesky B, Flickinger MC (2009) Biosorption, Metals. In: Encyclopedia of Industrial Biotechnology. John Wiley & Sons, Inc. https://doi.org/10.1002/9780470054581.eib166
Oliveira RC, Palmieri MC, Garcia OJ (2011) Biosorption of metals: state of the art, general features, and potential applications for environmental and technological processes. Prog n Biomass Bioenergy Prod. https://doi.org/10.5772/17802
Orandi S, Lewis DM, Moheimani NR (2012) Biofilm establishment and heavy metal removal capacity of an indigenous mining algal-microbial consortium in a photo-rotating biological contactor. J Ind Microbiol Biotechnol 39:1321–1331. https://doi.org/10.1007/s10295-012-1142-9
Palma H, Killoran E, Sheehan M, Berner F, Heimann K (2017) Assessment of microalga biofilms for simultaneous remediation and biofuel generation in mine tailings water. Bioresource Technol 234:327–335. https://doi.org/10.1016/j.biortech.2017.03.063
Park D, Yun Y-S, Park JM (2010) The past, present, and future trends of biosorption Biotechnol. Bioprocess Eng 15:86–102
Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10. https://doi.org/10.1016/j.chemosphere.2005.11.024
Pitre D, Boullemant A, Fortin C (2014) Uptake and sorption of aluminium and fluoride by four green algal species Chem Cent J 8
Priyadarshani I, Sahu D, Rath B (2012) Microalgal bioremediation: current practices and perspectives. J Biochem Technol 3:299–304
Renuka N, Sood A, Prasanna R, Ahluwalia AS (2015) Phycoremediation of wastewaters: a synergistic approach using microalgae for bioremediation and biomass generation. Int J Environ Sci Technol 12:1443–1460. https://doi.org/10.1007/s13762-014-0700-2
Romera E, Gonzalez F, Ballester A, Blazquez ML, Munoz JA (2006) Biosorption with algae: a statistical review. Crit Rev Biotechnol 26:223–235. https://doi.org/10.1080/07388550600972153
Schmitt D, Müller A, Csögör Z, Frimmel FH, Posten C (2001) The adsorption kinetics of metal ions onto different microalgae and siliceous earth. Water Res 35:779–785. https://doi.org/10.1016/S0043-1354(00)00317-1
Schnurr PJ, Allen DG (2015) Factors affecting algae biofilm growth and lipid production: a review. Renew Sustain Energy Rev 52:418–429. https://doi.org/10.1016/j.rser.2015.07.090
Shanab S, Essa A, Shalaby E (2012) Bioremoval capacity of three heavy metals by some microalgae species (Egyptian Isolates). Plant Signal Behav 7:392–399
Sharma R et al. (2016) Responses of Phytochelatins and Metallothioneins in Alleviation of Heavy Metal Stress in Plants: An Overview In: Plant Metal Interaction. Elsevier, pp 263-283. doi:http://dx.doi.org/10.1016/B978-0-12-803158-2.00010-2
Shukla D, Trivedi PK, Nath P, Tuteja N (2016) Metallothioneins and Phytochelatins: Role and Perspectives in Heavy Metal(loid)s Stress Tolerance in Crop Plants. In: Abiotic Stress Response in Plants. Wiley-VCH Verlag GmbH & Co. KGaA, pp 237-264. https://doi.org/10.1002/9783527694570.ch12
Souza PO, Ferreira LR, Pires NRX, Filho PJ, Duarte FA, Pereira CMP, Mesko MF (2012) Algae of economic importance that accumulate cadmium and lead: a review. Revista Brasileira de Farmacognosia 22:825–837
Sriprang R, Murooka Y (2007) Accumulation and Detoxification of Metals by Plants and Microbes. In: Singh S, Tripathi R (eds) Environmental Bioremediation Technologies. Springer Berlin Heidelberg, pp 77-100. https://doi.org/10.1007/978-3-540-34793-4_4
Toninelli AE, Wang J, Liu M, Wu H, Liu T (2016) Scenedesmus dimorphus biofilm: photoefficiency and biomass production under intermittent lighting. Sci Rep 6:32305. https://doi.org/10.1038/srep32305
Torres E, Cid A, Fidalgo P, Herrero C, Abalde J (1997) Long-chain class III metallothioneins as a mechanism of cadmium tolerance in the marine diatom Phaeodactylum tricornutum. Bohlin Aquat Toxicol 39:231–246. https://doi.org/10.1016/S0166-445X(97)00034-9
Torres MA, Barros MP, Campos SCG, Pinto E, Rajamani S, Sayre RT, Colepicolo P (2008) Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol Environ Saf 71:1–15. https://doi.org/10.1016/j.ecoenv.2008.05.009
Travieso L, Pellón A, Benı́tez F, Sánchez E, Borja R, OFarrill N, Weiland P (2002) BIOALGA reactor: preliminary studies for heavy metals removal. Biochem Eng J 12:87-91. doi:https://doi.org/10.1016/S1369-703X(02)00045-1
Tsezos M, Remoundaki E, Hatzikioseyian A (2011) Biosorption—principles and applications for metal immobilization from waste-water streams. In: Paper presented at the proceedings of EU-Asia workshop on clean production and nanotechnologies, Seoul, Korea
Tüzün İ, Bayramoğlu G, Yalçın E, Başaran G, Çelik G, Arıca MY (2005) Equilibrium and kinetic studies on biosorption of Hg(II), Cd(II) and Pb(II) ions onto microalgae Chlamydomonas reinhardtii. J Environ Manag 77:85–92. https://doi.org/10.1016/j.jenvman.2005.01.028
Volesky B (2001) Detoxification of metal-bearing effluents: biosorption for the next century. Hydrometallurgy 59:203–216. https://doi.org/10.1016/S0304-386X(00)00160-2
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 24:1386–1393. https://doi.org/10.1016/S1001-0742(11)60931-5
Wang Y, Zhang C, Zheng Y, Ge Y (2017) Phytochelatin synthesis in Dunaliella salina induced by arsenite and arsenate under various phosphate regimes. Ecotoxicol Environ Saf 136:150–160. https://doi.org/10.1016/j.ecoenv.2016.11.002
Williams D, Taylor D (2005) Pharmaceutical Applications of Bioinorganic Chemistry. In: Smith and Williams’ introduction to the principles of drug design and action, Fourth Edition. CRC Press, Boca Raton. pp 617–642. doi:https://doi.org/10.1201/9780203304150.ch17
Worms I, Simon DF, Hassler CS, Wilkinson KJ (2006) Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake. Biochimie 88:1721–1731. https://doi.org/10.1016/j.biochi.2006.09.008
Zabochnicka-Świątek M, Krzywonos M (2014) Potentials of biosorption and bioaccumulation processes for heavy metal removal. Pol J Environ Stud 23:551–561
Zeraatkar AK, Ahmadzadeh H, Talebi AF, Moheimani NR, McHenry MP (2016) Potential use of algae for heavy metal bioremediation, a critical review. J Environ Manag 181:817–831. https://doi.org/10.1016/j.jenvman.2016.06.059
Zhao Y, Wang B, Liu C, Wu Y (2013) Biosorption of trace metals from aqueous multimetal solutions by green microalgae. Chin J Geochem 32:385–391. https://doi.org/10.1007/s11631-013-0646-y
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This work was funded by the program THALES−TEI CRETE, MIS 380210 within the National Strategic Reference Framework (NSRF). All authors declare that there is no conflict of interest of any kind referring to their work. AM and FV are grateful for the collaboration with Prof. S. Pergantis (Department of Chemistry, University of Crete). KP is grateful for an internal grant from ELKE-TEI Crete.
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Mantzorou, A., Navakoudis, E., Paschalidis, K. et al. Microalgae: a potential tool for remediating aquatic environments from toxic metals. Int. J. Environ. Sci. Technol. 15, 1815–1830 (2018). https://doi.org/10.1007/s13762-018-1783-y
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DOI: https://doi.org/10.1007/s13762-018-1783-y