Skip to main content
Log in

Mechanism of action and toxicological evaluation of engineered layered double hydroxide nanomaterials in Biomphalaria alexandrina snails

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Layered double hydroxide (LDH) nanomaterials have recently become immense research area as it is used widely in industries. So, it’s chance of their release into natural environment and risk assessment to nontarget aquatic invertebrate increasing. So, the present study aimed to synthesize and confirm the crystalline formation of Co-Cd-Fe LDHs and Co-Cd-Fe/PbI2 (LDH) and then to investigate the toxic impact of the two LDH on the adult freshwater snails (Biomphalaia alexandrina). Results showed that Co-Cd-Fe/PbI2 LDH has more toxic effect to adult Biomphalaria than Co-Cd-Fe LDHs (LC50 was 56.4 and 147.7 mg/L, 72 h of exposure, respectively). The effect of LC25 (117.1 mg/L) of Co-Cd-Fe LDHs exposure on the embryo showed suppression of embryonic development and induced embryo malformation. Also, it showed alterations in the tegmental architectures of the mantle-foot region of B. alexandrina snails as declared in scanning electron micrograph. Also, exposure to this sublethal concentration caused abnormalities in hemocyte shapes and upregulated IL-2 level in soft tissue. In addition, it decreased levels of nonenzymatic reduced glutathione (GSH), catalase (CAT), superoxide dismutase (SOD), caspase-3 activity, and total protein content in significant manner. Glutathione S-transferase (GST) activity was not affected by LDH exposure. It caused histopathological damages in both glands of snails and also caused a genotoxic effect in their cells. The results from the present study indicated that LDH has risk assessment on aquatic B. alexandrina snails and that it can be used as a biological indicator of water pollution with LDH.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The data that supports the findings of this study are available in the material of this article.

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ali D (2014) Oxidative stress-mediated apoptosis and genotoxicity induced by silver nanoparticles in freshwater snail Lymnea luteola L. Biol Trace Elem Res 162:333–341

    Article  CAS  Google Scholar 

  • Ali D, Alarifi S, Kumar S, Ahamed M, Siddiqui MA (2012) Oxidative stress and genotoxic effect of zinc oxide nanoparticles in freshwater snail Lymnaea luteola L. Aquat Toxicol 124:83–90

    Article  Google Scholar 

  • Amorim J, Abreu I, Rodrigues P, Peixoto D, Pinheiro C, Saraiva A, Carvalho AP, Guimarães L, Oliva-Teles L (2019) Lymnaea stagnalis as a freshwater model invertebrate for ecotoxicological studies. Sci Total Environ 669:11–28

    Article  CAS  Google Scholar 

  • Atli G, Grosell M (2016) Characterization and response of antioxidant systems in the tissues of the freshwater pond snail (Lymnaea stagnalis) during acute copper exposure. Aquat Toxicol 176:38–44. https://doi.org/10.1016/j.aquatox.2016.04.007

    Article  CAS  Google Scholar 

  • Attia MM, Soliman SM, Khalf MA (2017) Hydrophilic nanosilica as a new larvicidal and molluscicidal agent for controlling of major infectious diseases in Egypt. Vet World 10:1046–1051. https://doi.org/10.14202/vetworld.2017.1046-1051

    Article  CAS  Google Scholar 

  • Bao S, Huang J, Liu X, Tang W, Fang T (2018) Tissue distribution of Ag and oxidative stress responses in the freshwater snail Bellamya aeruginosa exposed to sediment-associated Ag nanoparticles. Sci Total Environ 644:736–746

    Article  CAS  Google Scholar 

  • Barcia R, Cao A, Arbeteta J, Ramos-Martinez JI (1999) The IL-2 receptor in hemocytes of the sea mussel Mytilus galloprovincialis Lmk. IUBMB Life 48:419–423

    Article  CAS  Google Scholar 

  • Bazrafshan AA, Ghaedi M, Hajati S, Naghiha R, Asfaram A (2017) Synthesis of ZnO-nanorod-based materials for antibacterial, antifungal activities, DNA cleavage and efficient ultrasound-assisted dyes adsorption. Ecotoxicol Environ Saf 142:330–337

    Article  CAS  Google Scholar 

  • Benício LPF, Pinto FG, Tronto J (2020) Layered double hydroxide nanocomposites for agricultural applications. In: Layered Double Hydroxide Polymer Nanocomposites. Elsevier, pp 715–741. https://doi.org/10.1016/B978-0-08-101903-0.00017-9

  • Benito D, Niederwanger M, Izagirre U, Dallinger R, Soto M (2017) Successive onset of molecular, cellular and tissue-specific responses in midgut gland of Littorina littorea exposed to sub-lethal cadmium concentrations. Int J Mol Sci 18:1815

    Article  Google Scholar 

  • Besnaci S, Bensoltane S, Braia FMH et al (2016) Embryotoxicity evaluation of iron oxide Fe2O3 on land snails: Helix aspersa. J Entomol Zool Stud 4:317–323

    Google Scholar 

  • Bhagat J, Ingole BS, Singh N (2016) Glutathione S-transferase, catalase, superoxide dismutase, glutathione peroxidase, and lipid peroxidation as biomarkers of oxidative stress in snails: a review. Invertebr Surviv J 13:336–349

    Google Scholar 

  • Bonomini M, Dottori S, Amoroso L, Arduini A, Sirolli V (2004) Increased platelet phosphatidylserine exposure and caspase activation in chronic uremia. J Thromb Haemost 2:1275–1281

    Article  CAS  Google Scholar 

  • Caixeta MB, Araújo PS, Gonçalves BB, et al (2020) Toxicity of engineered nanomaterials to aquatic and land snails: A scientometric and systematic review. Chemosphere 260:127654. https://doi.org/10.1016/j.chemosphere.2020.127654

  • Cao A (1998) El receptor de IL-2 en hemocitos deMytilus galloprovinciali s Lmk. International Union of Biochemistry and Molecular Biology Life 48(4):419–423. https://doi.org/10.1080/713803540

  • Cardinale BJ, Bier R, Kwan C (2012) Effects of TiO2 nanoparticles on the growth and metabolism of three species of freshwater algae. J Nanopart Res 14. https://doi.org/10.1007/s11051-012-0913-6

  • Chandran R, Sivakumar AA, Mohandass S, Aruchami M (2005) Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina fulica. Comp Biochem Physiol C Toxicol Pharmacol 140:422–426

    Article  Google Scholar 

  • Chen C, Yu W, Liu T, Cao S, Tsang Y (2017) Graphene oxide/WS2/Mg-doped ZnO nanocomposites for solar-light catalytic and anti-bacterial applications. Sol Energy Mater Sol Cells 160:43–53

    Article  CAS  Google Scholar 

  • Choi S-J, Choy J-H(2011) Layered double hydroxide nanoparticles as target-specific delivery carriers: uptake mechanism and toxicity. Nanomedicine 6:803–814

    Article  CAS  Google Scholar 

  • Choi SJ, Oh JM, Choy JH (2009) Toxicological effects of inorganic nanoparticles on human lung cancer A549 cells. J Inorg Biochem 103:463–471. https://doi.org/10.1016/j.jinorgbio.2008.12.017

    Article  CAS  Google Scholar 

  • Choi SJ, Paek HJ, Yu J (2015) Oxidative stress by layered double hydroxide nanoparticles via an SFK-JNK and p38-NF-κB signaling pathway mediates induction of interleukin-6 and interleukin-8 in human lung epithelial cells. Int J Nanomedicine 10:3217–3229. https://doi.org/10.2147/IJN.S82061

    Article  CAS  Google Scholar 

  • Corsi I, Winther-Nielsen M, Sethi R, Punta C, Della Torre C, Libralato G, Lofrano G, Sabatini L, Aiello M, Fiordi L, Cinuzzi F, Caneschi A, Pellegrini D, Buttino I (2018) Ecofriendly nanotechnologies and nanomaterials for environmental applications: key issue and consensus recommendations for sustainable and ecosafe nanoremediation. Ecotoxicol Environ Saf 154:237–244

    Article  CAS  Google Scholar 

  • Croteau M-N, Misra SK, Luoma SN, Valsami-Jones E (2014) Bioaccumulation and toxicity of CuO nanoparticles by a freshwater invertebrate after waterborne and dietborne exposures. Environ Sci Technol 48:10929–10937

    Article  CAS  Google Scholar 

  • Daniel S, Thomas S (2020) Layered double hydroxides: fundamentals to applications. In: Layered Double Hydroxide Polymer Nanocomposites. Elsevier, pp 1–76. Woodhead Publishing.

  • de Chavez ERC, de Lara AV (2003) Effects of zinc (Zn2+) and lead (Pb2+) on the early development of the freshwater snail, Radix quadrasi. J Med Appl Malacol 12:59–68

    Google Scholar 

  • de Vasconcelos LM, de Andrade Pereira MI, Cabral Filho PE et al (2019) Studies on toxicity of suspensions of CdTe quantum dots to Biomphalaria glabrata mollusks. Environ Toxicol Chem 38:2128–2136

    Article  Google Scholar 

  • DeJong RJ, Morgan JAT, Paraense WL et al (2001) Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human bloodfluke, Schistosoma mansoni. Mol Biol Evol 18:2225–2239

    Article  CAS  Google Scholar 

  • Ding T, Lin K, Chen J, Hu Q, Yang B, Li J, Gan J (2018) Causes and mechanisms on the toxicity of layered double hydroxide (LDH) to green algae Scenedesmus quadricauda. Sci Total Environ 635:1004–1011

    Article  CAS  Google Scholar 

  • Duft M, Schmitt C, Bachmann J, Brandelik C, Schulte-Oehlmann U, Oehlmann J (2007) Prosobranch snails as test organisms for the assessment of endocrine active chemicals––an overview and a guideline proposal for a reproduction test with the freshwater mudsnail Potamopyrgus antipodarum. Ecotoxicology 16:169–182

    Article  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  Google Scholar 

  • Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516

    Article  CAS  Google Scholar 

  • Fahmy SR, Sayed DA (2017) Toxicological perturbations of zinc oxide nanoparticles in the Coelatura aegyptiaca mussel. Toxicol Ind Health 33:564–575. https://doi.org/10.1177/0748233716687927

    Article  CAS  Google Scholar 

  • Fahmy SR, Abdel-Ghaffar F, Bakry FA, Sayed DA (2014) Ecotoxicological effect of sublethal exposure to zinc oxide nanoparticles on freshwater snail Biomphalaria alexandrina. Arch Environ Contam Toxicol 67:192–202

    Article  CAS  Google Scholar 

  • Finney DJ (1971) Probit Analysis. Cambridge University Press, London

    Google Scholar 

  • Florentin A, Arama E (2012) Caspase levels and execution efficiencies determine the apoptotic potential of the cell. J Cell Biol 196:513–527

    Article  CAS  Google Scholar 

  • Fried B (2016) An update on hemocytes in Biomphalaria snails. J Hematol Oncol Res 2, 26(20). https://doi.org/10.14302/issn.2372-6601.jhor-14-401

  • Gnatyshyna L, Falfushynska H, Stoliar O, Dallinger R (2020) Preliminary study of multiple stress response reactions in the pond snail Lymnaea stagnalis exposed to trace metals and a thiocarbamate fungicide at environmentally relevant concentrations. Arch Environ Contam Toxicol 79:89–100

    Article  CAS  Google Scholar 

  • Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–766

    Article  CAS  Google Scholar 

  • Grazeffe VS, de Freitas TL, de Sa PA et al (2008) Establishment of the comet assay in the freshwater snail Biomphalaria glabrata (Say, 1818). Mutat Res Toxicol Environ Mutagen 654:58–63

    Article  CAS  Google Scholar 

  • Guria S, Parveen S, Goswami DS (2016) Alteration of morphology, phagocytic behaviour and aggregation of insect haemocytes exposed to contaminated food with arsenic and lead. Int J PharmTech Res 9:177–186

    CAS  Google Scholar 

  • Han J, Xu X, Rao X, Wei M, Evans DG, Duan X (2011)Layer-by-layer assembly of layered double hydroxide/cobalt phthalocyanine ultrathin film and its application for sensors. J Mater Chem 21:2126–2130

    Article  CAS  Google Scholar 

  • Hemdan NYA, Lehmann I, Wichmann G, Lehmann J, Emmrich F, Sack U (2007) Immunomodulation by mercuric chloride in vitro: application of different cell activation pathways. Clin Exp Immunol 148:325–337

    Article  CAS  Google Scholar 

  • Hughes TK, Smith EM, Chin R, Cadet P, Sinisterra J, Leung MK, Shipp MA, Scharrer B, Stefano GB (1990) Interaction of immunoactive monokines (interleukin 1 and tumor necrosis factor) in the bivalve mollusc Mytilus edulis. Proc Natl Acad Sci 87:4426–4429

    Article  CAS  Google Scholar 

  • Ibrahim AM, Abdel-Tawab H (2020) Cystoseira barbata marine algae have a molluscicidal activity against Biomphalaria alexandrina snails supported by scanning electron microscopy, hematological and histopathological alterations, and larvicidal activity against the infective stages of Schistosoma mansoni. Biologia 75(11):1945–1954

  • Ibrahim AM, Ghoname SI (2018) Molluscicidal impacts of Anagallis arvensis aqueous extract on biological, hormonal, histological and molecular aspects of Biomphalaria alexandrina snails. Exp Parasitol 192:36–41. https://doi.org/10.1016/j.exppara.2018.07.014

    Article  CAS  Google Scholar 

  • Ibrahim MA, Ahmed et al (2018) Hematological, physiological and genotoxicological effects of Match 5% EC insecticide on Biomphalaria alexandrina snails. Ecotoxicol Environ Saf 147:1017–1022. https://doi.org/10.1016/j.ecoenv.2017.09.059

    Article  CAS  Google Scholar 

  • Kaloyianni M, Dimitriadi A, Ovezik M, Stamkopoulou D, Feidantsis K, Kastrinaki G, Gallios G, Tsiaoussis I, Koumoundouros G, Bobori D (2020) Magnetite nanoparticles effects on adverse responses of aquatic and terrestrial animal models. J Hazard Mater 383:121204

    Article  CAS  Google Scholar 

  • Khangarot BS, Das S (2010) Effects of copper on the egg development and hatching of a freshwater pulmonate snail Lymnaea luteola L. J Hazard Mater 179:665–675

    Article  CAS  Google Scholar 

  • Kim K-T, Jang M-H, Kim J-Y, Xing B, Tanguay RL, Lee BG, Kim SD (2012) Embryonic toxicity changes of organic nanomaterials in the presence of natural organic matter. Sci Total Environ 426:423–429

    Article  CAS  Google Scholar 

  • Ladewig K, Xu ZP, Lu GQ (2009) Layered double hydroxide nanoparticles in gene and drug delivery. Expert Opin Drug Deliv 6:907–922

    Article  CAS  Google Scholar 

  • Larson MK, Bender RC, Bayne CJ (2014) Resistance of Biomphalaria glabrata 13-16-R1 snails to Schistosoma mansoni PR1 is a function of haemocyte abundance and constitutive levels of specific transcripts in haemocytes. Int J Parasitol 44:343–353

    Article  CAS  Google Scholar 

  • Lee RF, Steinert S (2003) Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat Res Mutat Res 544:43–64

    Article  CAS  Google Scholar 

  • Li R, Wang JJ, Zhou B, Awasthi MK, Ali A, Zhang Z, Gaston LA, Lahori AH, Mahar A (2016) Enhancing phosphate adsorption by Mg/Al layered double hydroxide functionalized biochar with different Mg/Al ratios. Sci Total Environ 559:121–129

    Article  CAS  Google Scholar 

  • Long Z, Ji J, Yang K, Lin D, Wu F (2012) Systematic and quantitative investigation of the mechanism of carbon nanotubes’ toxicity toward algae. Environ Sci Technol 46:8458–8466

    Article  CAS  Google Scholar 

  • Ma T, Gong S, Tian B (2017) Effects of sediment-associated CuO nanoparticles on Cu bioaccumulation and oxidative stress responses in freshwater snail Bellamya aeruginosa. Sci Total Environ 580:797–804

    Article  CAS  Google Scholar 

  • Mannervik B, Guthenberg C (1981) [28] Glutathione transferase (human placenta). Methods Enzymol 77:231–235

  • Manzi-Nshuti C, Songtipya P, Manias E, Jimenez-Gasco MM, Hossenlopp JM, Wilkie CA (2009) Polymer nanocomposites using zinc aluminum and magnesium aluminum oleate layered double hydroxides: effects of LDH divalent metals on dispersion, thermal, mechanical and fire performance in various polymers. Polymer (Guildf) 50:3564–3574

    Article  CAS  Google Scholar 

  • Martins N, Pradhan A, Pascoal C, Cássio F (2020) Effects of metal nanoparticles on freshwater rotifers may persist across generations. Aquat Toxicol 229:105652

    Article  CAS  Google Scholar 

  • Mitta G, Vandenbulcke F, Noël T et al (2000) Differential distribution and defence involvement of antimicrobial peptides in mussel. J Cell Sci 113:2759–2769

    Article  CAS  Google Scholar 

  • Mohamed AH (2011) Sublethal toxicity of Roundup to immunological and molecular aspects of Biomphalaria alexandrina to Schistosoma mansoni infection. Ecotoxicol Environ Saf 74:754–760

    Article  CAS  Google Scholar 

  • Mohamed SH, Saad AA (1990) Histological studies on the hermaphrodite gland of Lymnaea caillaudi and Biomphalaria alexandrina upon infection with certain larval trematodes. Egypt J Histol 13:47–53

    Google Scholar 

  • Mohamed F, Abukhadra MR, Shaban M (2018) Removal of safranin dye from water using polypyrrole nanofiber/Zn-Fe layered double hydroxide nanocomposite (Ppy NF/Zn-Fe LDH) of enhanced adsorption and photocatalytic properties. Sci Total Environ 640–641:352–363. https://doi.org/10.1016/j.scitotenv.2018.05.316

    Article  CAS  Google Scholar 

  • Mohamed F, Bhnsawy N, Shaban M (2021) Reusability and stability of a novel ternary (Co–Cd–Fe)-LDH/PbI2, photoelectrocatalytst for solar hydrogen production. Sci Rep 11:5618

    Article  CAS  Google Scholar 

  • Moustafa MA, Mossalem HS, Sarhan RM, Abdel-Rahman AA, Hassan EM (2018) The potential effects of silver and gold nanoparticles as molluscicides and cercaricides on Schistosoma mansoni. Parasitol Res 117:3867–3880. https://doi.org/10.1007/s00436-018-6093-2

    Article  CAS  Google Scholar 

  • Myer MH, Henderson WM, Black MC (2017) Effects of multiwalled carbon nanotubes on the bioavailability and toxicity of diphenhydramine to Pimephales promelas in sediment exposures. Environ Toxicol Chem 36:320–328

    Article  CAS  Google Scholar 

  • Nduku WK, Harrison AD (1980) Cationic responses of organs and haemolymph of Biomphalaria pfeifferi (Krauss), Biomphalaria glabrata (Say) and Helisoma trivolvis (Say)(Gastropoda: Planorbirdae) to cationic alterations of the medium. Hydrobiologia 68:119–138

    Article  CAS  Google Scholar 

  • Oliveira-Filho EC, Nakano E, de Tallarico LF (2017) Bioassays with freshwater snails Biomphalaria sp.: from control of hosts in public health to alternative tools in ecotoxicology. Invertebr Reprod Dev 61:49–57

    Article  CAS  Google Scholar 

  • Oliver AL-S, Croteau M-N, Stoiber TL, Tejamaya M, Römer I, Lead JR, Luoma SN (2014) Does water chemistry affect the dietary uptake and toxicity of silver nanoparticles by the freshwater snail Lymnaea stagnalis? Environ Pollut 189:87–91

    Article  CAS  Google Scholar 

  • Omobhude ME, Morenikeji OA, Oyeyemi OT (2017) Molluscicidal activities of curcumin-nisin polylactic acid nanoparticle on Biomphalaria pfeifferi. PLoS Negl Trop Dis 11:e0005855. https://doi.org/10.1371/journal.pntd.0005855

    Article  CAS  Google Scholar 

  • Ottaviani E (2006) Molluscan immunorecognition. Invertebr Surviv J 3:50–63

    Google Scholar 

  • Ottaviani E, Franchini A, Franceschi C (1993) Presence of several cytokine-like molecules in molluscan hemocytes. Biochem Biophys Res Commun 195:984–988

    Article  CAS  Google Scholar 

  • Ottaviani E, Caselgrandi E, Franceschi C (1995a) Cytokines and evolution: in vitro effects of IL-1α, IL-1β, TNF-α and TNF-β on an ancestral type of stress response. Biochem Biophys Res Commun 207:288–292

    Article  CAS  Google Scholar 

  • Ottaviani E, Franchini A, Cassanelli S, Genedani S (1995b) Cytokines and invertebrate immune responses. Biol Cell 85:87–91

    Article  CAS  Google Scholar 

  • Parida KM, Mohapatra L (2012) Carbonate intercalated Zn/Fe layered double hydroxide: a novel photocatalyst for the enhanced photo degradation of azo dyes. Chem Eng J 179:131–139

    Article  CAS  Google Scholar 

  • Peligro FR, Pavlovic I, Rojas R, Barriga C (2016) Removal of heavy metals from simulated wastewater by in situ formation of layered double hydroxides. Chem Eng J 306:1035–1040

    Article  CAS  Google Scholar 

  • Pena-Llopis S, Pena JB, Sancho E et al (2001)Glutathione-dependent resistance of the European eel Anguilla anguilla to the herbicide molinate. Chemosphere 45:671–681

    Article  CAS  Google Scholar 

  • Pirger Z, Zrinyi Z, Maász G et al (2018) Pond snail reproduction as model in the environmental risk assesment: reality and doubts. In: Ray S (ed) Biol Resour Water. IntechOpen, London, pp 33–53

    Google Scholar 

  • Radwan MA, El-Gendy KS, Gad AF et al (2019) Responses of oxidative stress, genotoxicity and immunotoxicity as biomarkers in Theba pisana snails dietary exposed to silver nanoparticles. Chem Ecol 35:613–630

    Article  CAS  Google Scholar 

  • Rapado LN, Nakano E, Ohlweiler FP, Kato MJ, Yamaguchi LF, Pereira CAB, Kawano T (2011) Molluscicidal and ovicidal activities of plant extracts of the Piperaceae on Biomphalaria glabrata (Say, 1818). J Helminthol 85:66–72

    Article  CAS  Google Scholar 

  • Rasel MAI, Singh S, Nguyen TD, Afara IO, Gu Y (2019) Impact of nanoparticle uptake on the biophysical properties of cell for biomedical engineering applications. Sci Rep 9(9):5859. https://doi.org/10.1038/s41598-019-42225-7

    Article  CAS  Google Scholar 

  • Ruppert K, Geiß C, Askem C, Benstead R, Brown R, Coke M, Ducrot V, Egeler P, Holbech H, Hutchinson TH, Kinnberg KL, Lagadic L, le Page G, Macken A, Matthiessen P, Ostermann S, Schimera A, Schmitt C, Seeland-Fremer A et al (2017) Development and validation of an OECD reproductive toxicity test guideline with the mudsnail Potamopyrgus antipodarum (Mollusca, Gastropoda). Chemosphere 181:589–599

    Article  CAS  Google Scholar 

  • Saad AEHA, Ragab FMA, Abdel Fatah HM, Abdel-Wareth MTA, Ibrahim NK (2019) Effect of Cystoseira barbata and Dictyota dichotoma-algae on reproduction and protein pattern of Biomphalaria alexandrina snails. Molluscan Res 39:82–88. https://doi.org/10.1080/13235818.2018.1524740

    Article  Google Scholar 

  • Sánchez-Marín P, Vidal-Liñán L, Fernández-González LE, Montes R, Rodil R, Quintana JB, Carrera M, Mateos J, Diz AP, Beiras R (2021) Proteomic analysis and biochemical alterations in marine mussel gills after exposure to the organophosphate flame retardant TDCPP. Aqua Toxicol 230:105688

  • Shaban M, Mohamed F, Abdallah S (2018) Production and characterization of superhydrophobic and antibacterial coated fabrics utilizing ZnO nanocatalyst. Sci Rep 8:1–15

    Article  Google Scholar 

  • Sidiropoulou E, Feidantsis K, Kalogiannis S, Gallios GP, Kastrinaki G, Papaioannou E, Václavíková M, Kaloyianni M (2018) Insights into the toxicity of iron oxides nanoparticles in land snails. Comp Biochem Physiol C Toxicol Pharmacol 206–207:1–10. https://doi.org/10.1016/J.CBPC.2018.02.001

    Article  Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  CAS  Google Scholar 

  • Siwela AH, Nyathi CB, Naik YS (2010) A comparison of metal levels and antioxidant enzymes in freshwater snails, Lymnaea natalensis, exposed to sediment and water collected from Wright Dam and Lower Mguza Dam, Bulawayo, Zimbabwe. Ecotoxicol Environ Saf 73:1728–1732

    Article  CAS  Google Scholar 

  • Tarafdar JC, Sharma S, Raliya R (2013) Nanotechnology: Interdisciplinary science of applications. Afr J Biotechnol 12

  • Tedim J, Zheludkevich ML, Salak AN, Lisenkov A, Ferreira MGS (2011) Nanostructured LDH-container layer with active protection functionality. J Mater Chem 21:15464–15470

    Article  CAS  Google Scholar 

  • WHO (1965) Molluscicide screening and evaluation. Bull WHO 33:567–581

    Google Scholar 

  • Ye J, Wu H, Wu Y, Wang C, Zhang H, Shi X, Yang J (2012) High molecular weight hyaluronan decreases oxidative DNA damage induced by EDTA in human corneal epithelial cells. Eye 26:1012–1020

    Article  CAS  Google Scholar 

  • Zaldibar B, Cancio I, Marigómez I (2007a) Reversible alterations in epithelial cell turnover in digestive gland of winkles (Littorina littorea) exposed to cadmium and their implications for biomarker measurements. Aquat Toxicol 81:183–196. https://doi.org/10.1016/j.aquatox.2006.12.007

    Article  CAS  Google Scholar 

  • Zaldibar B, Cancio I, Soto M, Marigómez I (2007b) Digestive cell turnover in digestive gland epithelium of slugs experimentally exposed to a mixture of cadmium and kerosene. Chemosphere 70:144–154

    Article  CAS  Google Scholar 

  • Zhao Y, Jiao Q, Li C, Liang J (2007) Catalytic synthesis of carbon nanostructures using layered double hydroxides as catalyst precursors. Carbon N Y 45:2159–2163

    Article  CAS  Google Scholar 

  • Zhu X, Zhu L, Chen Y, Tian S (2009) Acute toxicities of six manufactured nanomaterial suspensions to Daphnia magna. J Nanopart Res 11:67–75

    Article  CAS  Google Scholar 

  • Malakar A, Kanel SR, Ray C, Snow D, Juna M, Nadagouda N (2021) Nanomaterials in the environment, human exposure pathway, and health effects: A review. Sci Total Environ 759:143470

  • OECD (2016) Test No. 243: Lymnaea stagnalis reproduction test, OECD guidelines for the testing of chemicals, Section 2. OECD Publishing, Paris 

  • Boisseaux P, Noury P, Thomas H, Garric J (2017) Immune responses in the aquatic gastropod Lymnaea stagnalis under short-term exposure to pharmaceuticals of concern for immune systems: Diclofenac, cyclophosphamide and cyclosporine A. Ecotoxicol Environ Saf 139:358–366

  • Lu H, Zhu Z, Zhang H, Zhu J, Qiu Y (2015) Simultaneous removal of arsenate and antimonate in simulated and practical water samples by adsorption onto Zn/Fe layered double hydroxide. Chem Eng J 276:365–375

  • Choi SJ, Oh JM, Park T, Choy JH (2007) Cellular toxicity of inorganic hydroxide nanoparticles. J Nanosci Nanotechnol 7(11):4017–4020

  • Hödl E, Felder E, Chabicovsky M, Dallinger R (2010) Cadmium stress stimulates tissue turnover in Helix pomatia: increasing cell proliferation from metal tolerance to exhaustion in molluscan midgut gland. Cell Tissue Res 341:159–171. https://doi.org/10.1007/s00441-010-0980-x

Download references

Code availability

Not applicable

Author information

Authors and Affiliations

Authors

Contributions

Conceived and designed experiments; Heba Abdel-Tawab, Amina M. Ibrahim

Data curation; Taghreed Hussein, Fatma Mohamed

Formal analysis; Taghreed Hussein, Fatma Mohamed

Methodology; Heba Abdel-Tawab, Amina M. Ibrahim

Software; Taghreed Hussein, Fatma Mohamed

Supervision; Heba Abdel-Tawab, Amina M. Ibrahim

Validation; Heba Abdel-Tawab, Amina M. Ibrahim

Visualization; Heba Abdel-Tawab, Amina M. Ibrahim

Roles/writing-original draft; Taghreed Hussein, Fatma Mohamed

Writing—review & editing; Heba Abdel-Tawab, Amina M. Ibrahim

Corresponding author

Correspondence to Heba Abdel-Tawab.

Ethics declarations

Ethics approval

Not applicable

Consent to participate

Not applicable

Consent for publication

Not applicable

Conflict of interest/competing interests

The authors declare no competing interests.

Additional information

Responsible editor: Bruno Nunes

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdel-Tawab, H., Ibrahim, A.M., Hussein, T. et al. Mechanism of action and toxicological evaluation of engineered layered double hydroxide nanomaterials in Biomphalaria alexandrina snails. Environ Sci Pollut Res 29, 11765–11779 (2022). https://doi.org/10.1007/s11356-021-16332-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-16332-w

Keywords

Navigation