Reproductive and Biochemical Toxicity of Biobased Silver Nanoparticles against Toxocara vitulorum

Manar   Ahmed   Bahaaeldine; Manal   El   Garhy; Sohair   R.   Fahmy; Ayman   Saber   Mohamed
Abstract

Background: Toxocara vitulorum is a common parasitic worm of buffalo and cattle, causing livestock mortality and morbidity worldwide. Several countries suffered substantial economic losses due to animal death and reduced meat and milk production. Therefore, it became necessary to discover a new alternative drug, especially with the emerging resistance to current medications. The present study aims to evaluate the in vitro anthelmintic effect of different concentrations of biobased silver nanoparticles on T. vitulorum adults.
Methods: Different concentrations of silver nanoparticles were synthesised using lemon juice. Groups of male and female adult worms were incubated in 50, 100, and 200 mg/L silver nanoparticles for 48 h. The parasite motility, histology, and biochemical parameters were observed and compared to the control.
Results: The results showed that silver nanoparticles decreased the worm motility, increased mortality rate, induced structural damage, caused collagen disruption, and showed elevated levels of aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, albumin, total protein, urea, and creatinine, as well as reduced levels of acetylcholinesterase, lactate dehydrogenase, uric acid, total cholesterol, triglycerides, and high-density lipoprotein in a dose-dependent manner.
Conclusion: Silver nanoparticles established a significant anthelmintic effect against T. vitulorum and could become one of the up-and-coming antiparasitic drugs in the future.
Keywords: Toxocara vitulorum, silver nanoparticles, toxicity, reproductive organs, histological assessment, biochemical abnormalities.
Graphical Abstract

[1]
El-Ashram S, Aboelhadid SM, Kamel AA, Mahrous LN, Abdelwahab KH. Diversity of parasitic diarrhea associated with Buxtonella Sulcata in cattle and buffalo calves with control of buxtonellosis. Animals  2019; 9(5): 259.
 [http://dx.doi.org/10.3390/ani9050259] [PMID:  31117265]

[2]
Chen J, Liu Q, Liu GH, et al. Toxocariasis: A silent threat with a progressive public health impact. Infect Dis Poverty  2018; 7(1): 59.
 [http://dx.doi.org/10.1186/s40249-018-0437-0] [PMID:  29895324]

[3]
Raza A, Murtaza S, Ayaz MM, et al. Toxocara Vitulorum infestation and associated risk factors in cattle and buffalo at Multan district, Pakistan. Sci Int  2013; 25(2): 291-4.

[4]
Roberts JA. Toxocara vitulorum: Treatment based on the duration of the infectivity of buffalo cows (Bubalus bubalis) for their calves. J Vet Pharmacol Ther  1989; 12(1): 5-13.
 [http://dx.doi.org/10.1111/j.1365-2885.1989.tb00634.x] [PMID: 2704061]

[5]
Shalaby H, El Namaky A, Kandil O, Hassan N. In vitro assessment of balanites aegyptiaca fruit methanolic extract on the adult toxocara canis. Iran J Parasitol  2018; 13(4): 643-7.
 [PMID:  30697320]

[6]
Anjum S, Ishaque S, Fatima H, et al. Emerging applications of nanotechnology in healthcare systems: Grand challenges and perspectives. Pharmaceuticals  2021; 14(8): 707.
 [http://dx.doi.org/10.3390/ph14080707] [PMID:  34451803]

[7]
Parveen K, Banse V, Ledwani L. Green synthesis of nanoparticles: Their advantages and disadvantages. AIP Conference Proceedings  2016; 1724: 020048.
 [http://dx.doi.org/10.1063/1.4945168]

[8]
Kaabipour S, Hemmati S. A review on the green and sustainable synthesis of silver nanoparticles and one-dimensional silver nanostructures. Beilstein J Nanotechnol  2021; 12: 102-36.
 [http://dx.doi.org/10.3762/bjnano.12.9] [PMID:  33564607]

[9]
Amooaghaie R, Saeri MR, Azizi M. Synthesis, characterization and biocompatibility of silver nanoparticles synthesized from Nigella sativa leaf extract in comparison with chemical silver nanoparticles. Ecotoxicol Environ Saf  2015; 120: 400-8.
 [http://dx.doi.org/10.1016/j.ecoenv.2015.06.025] [PMID:  26122733]

[10]
Hemlata, Meena PR, Singh AP, Tejavath KK. Biosynthesis of silver nanoparticles using Cucumis prophetarum aqueous leaf extract and their antibacterial and antiproliferative activity against cancer cell lines. ACS Omega  2020; 5(10): 5520-8.
 [http://dx.doi.org/10.1021/acsomega.0c00155] [PMID:  32201844]

[11]
Alaallah NJ. AbdulKareem EA, Ghaidan AF. Eco-friendly approach for silver nanoparticles synthesis from lemon extract and their antioxidant, antibacterial, and anti-cancer activities. J Turk Chem Soc Sect A: Chem  2023; 10(1): 205-16.
 [http://dx.doi.org/10.18596/jotcsa.1159851]

[12]
Khane Y, Benouis K, Albukhaty S, et al. Green synthesis of silver nanoparticles using aqueous citrus limon zest extract: Characterization and evaluation of their antioxidant and antimicrobial properties. Nanomaterials  2022; 12(12): 2013.
 [http://dx.doi.org/10.3390/nano12122013] [PMID:  35745352]

[13]
Nadaf SJ, Jadhav NR, Naikwadi HS, et al. Green synthesis of gold and silver nanoparticles: Updates on research, patents, and future prospects. OpenNano  2022; 8(November–December): 100076.
 [http://dx.doi.org/10.1016/j.onano.2022.100076]

[14]
Hawar SN, Al-Shmgani HS, Al-Kubaisi ZA, Sulaiman GM, Dewir YH, Rikisahedew JJ. Green synthesis of silver nanoparticles from alhagi graecorum leaf extract and evaluation of their cytotoxicity and antifungal activity. J Nanomater  2022; 2022: 1-8.
 [http://dx.doi.org/10.1155/2022/1058119]

[15]
Oves M, Ahmar Rauf M, Aslam M, et al. Green synthesis of silver nanoparticles by Conocarpus Lancifolius plant extract and their antimicrobial and anticancer activities. Saudi J Biol Sci  2022; 29(1): 460-71.
 [http://dx.doi.org/10.1016/j.sjbs.2021.09.007] [PMID:  35002442]

[16]
Zubair M, Azeem M, Mumtaz R, et al. Green synthesis and characterization of silver nanoparticles from Acacia nilotica and their anticancer, antidiabetic and antioxidant efficacy. Environ Pollut  2022; 304: 119249.
 [http://dx.doi.org/10.1016/j.envpol.2022.119249] [PMID:  35390420]

[17]
Baronia R, Kumar P, Singh SP, Walia RK. Silver nanoparticles as a potential nematicide against Meloidogyne graminicola. J Nematol  2020; 52(1): 1-9.
 [http://dx.doi.org/10.21307/jofnem-2020-002] [PMID:  32180384]

[18]
Khan M, Khan AU, Bogdanchikova N, Garibo D. Antibacterial and antifungal studies of biosynthesized silver nanoparticles against plant parasitic nematode meloidogyne incognita, plant pathogens ralstonia solanacearum and fusarium oxysporum. Molecules  2021; 26(9): 2462.
 [http://dx.doi.org/10.3390/molecules26092462] [PMID:  33922577]

[19]
Contreras EQ, Puppala HL, Escalera G, Zhong W, Colvin VL. Size-dependent impacts of silver nanoparticles on the lifespan, fertility, growth, and locomotion of Caenorhabditis elegans. Environ Toxicol Chem  2014; 33(12): 2716-23.
 [http://dx.doi.org/10.1002/etc.2705] [PMID:  25088842]

[20]
Abd-ELrahman M, Dyab AK, Mahmoud ES, et al. Influence of chemically and biosynthesised silver nanoparticles on in vitro viability and infectivity of Trichinella spiralis muscle larvae. bioRxiv  2021; 423206.

[21]
Wamboi P, Waruiru RM, Mbuthia PG, Nguhiu JM, Bebora LC. Haemato-biochemical changes and prevalence of parasitic infections of indigenous chicken sold in markets of Kiambu County, Kenya. Int J Vet Sci Med  2020; 8(1): 18-25.
 [http://dx.doi.org/10.1080/23144599.2019.1708577] [PMID: 32128314]

[22]
Topázio JP, Campigotto G, Boiago MM, et al. Influence of gastrointestinal parasitism on biochemical variables in blood of laying hens. Rev Mvz Cordoba  2015; 20: 4864-73.
 [http://dx.doi.org/10.21897/rmvz.2]

[23]
S Hungund B. Comparative evaluation of antibacterial activity of silver nanoparticles biosynthesized using fruit juices. J Nanomed Nanotechnol  2015; 6(2)
 [http://dx.doi.org/10.4172/2157-7439.1000271]

[24]
Singh P, Vidyasagar GM. Biosynthesis, characterization, and antidermatophytic activity of silver nanoparticles using raamphal plant (Annona reticulata) aqueous leaves extract. Indian J Mater Sci  2014; 2014: 1-5.
 [http://dx.doi.org/10.1155/2014/787306]

[25]
Nalule S, Mbaria JM, Kimenju JW. In vitro anthelmintic potential and phytochemical composition of ethanolic and aqueous crude extracts of Zanthoxylum chalybeum Engl. Afr J Pharm Pharmacol  2013; 7(23): 1604-14.
 [http://dx.doi.org/10.5897/AJPP2013.3664]

[26]
Kotze AC. McCARTHY JS, O’Grady J, Clifford S, Behnke JM. An In vitro larval motility assay to determine anthelmintic sensitivity for human hookworm and Strongyloides species. Am J Trop Med Hyg  2004; 71(5): 608-16.
 [http://dx.doi.org/10.4269/ajtmh.2004.71.608] [PMID:  15569793]

[27]
Bancroft JD, Stevens A. Theory and Practice of Histological Techniques. New York, NY, USA: Churchill Levingstone 1996.

[28]
Mohamed AS, Ibrahim WM, Zaki NI, Ali SB, Soliman AM. Effectiveness of Coelatura aegyptiaca Extract Combination with Atorvastatin on Experimentally Induced Hyperlipidemia in Rats. Evid Based Complement Alternat Med  2019; 2019: 1-9.
 [http://dx.doi.org/10.1155/2019/9726137] [PMID:  30713580]

[29]
Holden-Dye L, Walker RJ. Anthelmintic drugs. WormBook  2007; 1-13.
 [http://dx.doi.org/10.1895/wormbook.1.143.1]

[30]
Kotze AC, Gilleard JS, Doyle SR, Prichard RK. Challenges and opportunities for the adoption of molecular diagnostics for anthelmintic resistance. Int J Parasitol Drugs Drug Resist  2020; 14(November): 264-73.
 [http://dx.doi.org/10.1016/j.ijpddr.2020.11.005] [PMID:  33307336]

[31]
Yaqoob SB, Adnan R, Rameez KRM, Rashid M. Gold, silver, and palladium nanoparticles: A chemical tool for biomedical applications. Front Chem  2020; 8: 376.
 [http://dx.doi.org/10.3389/fchem.2020.00376] [PMID:  32582621]

[32]
Gupta M. Inorganic nanoparticles: An alternative therapy to combat drug resistant infections. Int J Pharm Pharm Sci  2021; 13(8): 20-31.
 [http://dx.doi.org/10.22159/ijpps.2021v13i8.42643]

[33]
Aderibigbe B. Metal-based nanoparticles for the treatment of infectious diseases. Molecules  2017; 22(8): 1370.
 [http://dx.doi.org/10.3390/molecules22081370] [PMID:  28820471]

[34]
Rashid MMO, Ferdous J, Banik S, Islam MR, Uddin AHMM, Robel FN. Anthelmintic activity of silver-extract nanoparticles synthesized from the combination of silver nanoparticles and M. charantia fruit extract. BMC Complement Altern Med  2016; 16(1): 242.
 [http://dx.doi.org/10.1186/s12906-016-1219-5] [PMID:  27457362]

[35]
Page P, Johnstone IL. The cuticle. The C. elegans Research Community. WormBook 2007.
 [http://dx.doi.org/10.1895/wormbook.1.138.1]

[36]
Shalaby H, Hassan N, Nasr S, Korany T, Abu El Ezz N. An anthelmintic assessment of balanites aegyptiaca fruits on some multiple drug resistant gastrointestinal helminthes affecting sheep. Egypt J Vet Sci  2020; 51(1): 93-103.

[37]
Shalaby H, Ashry H, Saad M, Farag T. In vitro effects of streptomyces tyrosinase on the egg and adult worm of toxocara vitulorum. Iran J Parasitol  2020; 15(1): 67-75.
 [http://dx.doi.org/10.18502/ijpa.v15i1.2528] [PMID:  32489377]

[38]
Njom VS, Winks T, Diallo O, et al. The effects of plant cysteine proteinases on the nematode cuticle. Parasit Vectors  2021; 14(1): 302.
 [http://dx.doi.org/10.1186/s13071-021-04800-8] [PMID:  34090505]

[39]
Greiffer L, Liebau E, Herrmann FC, Spiegler V. Condensed tannins act as anthelmintics by increasing the rigidity of the nematode cuticle. Sci Rep  2022; 12(1): 18850.
 [http://dx.doi.org/10.1038/s41598-022-23566-2] [PMID:  36344622]

[40]
Sandhu A, Badal D, Sheokand R, Tyagi S, Singh V. Specific collagens maintain the cuticle permeability barrier in Caenorhabditis elegans. Genetics  2021; 217(3): iyaa047.
 [http://dx.doi.org/10.1093/genetics/iyaa047] [PMID:  33789349]

[41]
Watanabe M, Mitani N, Ishii N, Miki K. A mutation in a cuticle collagen causes hypersensitivity to the endocrine disrupting chemical, bisphenol A, in Caenorhabditis elegans. Mutat Res  2005; 570(1): 71-80.
 [http://dx.doi.org/10.1016/j.mrfmmm.2004.10.005] [PMID:  15680404]

[42]
Ekino T, Yoshiga T, Takeuchi-Kaneko Y, Ichihara Y, Kanzaki N. Sexual dimorphism of the cuticle and body-wall muscle in free-living mycophagous nematodes. Can J Zool  2019; 97(6): 510-5.
 [http://dx.doi.org/10.1139/cjz-2018-0178]

[43]
Gomes DS, Negrão-Corrêa DA, Miranda GS, et al. Lippia alba and Lippia gracilis essential oils affect the viability and oviposition of Schistosoma mansoni. Acta Trop  2022; 231: 106434.
 [http://dx.doi.org/10.1016/j.actatropica.2022.106434] [PMID: 35364048]

[44]
Goldstein P. Exposure to the anthelmintic dinitroaniline oryzalin causes changes in meiotic prophase morphology and loss of synaptonemal complexes in the nematode Caenorhabditis elegans. Experimental Results  2021; 2: e38.
 [http://dx.doi.org/10.1017/exp.2021.19]

[45]
Mori T, Mohamed ASA, Sato M, Yamasaki T. Ellagitannin toxicity in the free-living soil-inhabiting nematode, <i>caenorhabditis elegans</i>. J Pestic Sci  2000; 25(4): 405-9.
 [http://dx.doi.org/10.1584/jpestics.25.405]

[46]
O’Neill M.  Characterization of the effects of flubendazole, a benzimidazole anthelmintic, on filarial nematodes. PhD thesis, McGill University: Quebec, Canada 2016.

[47]
Yang Z, Xue KS, Sun X, Williams PL, Wang JS, Tang L. Toxicogenomic responses to zearalenone in Caenorhabditis elegans reveal possible molecular mechanisms of reproductive toxicity. Food Chem Toxicol  2018; 122: 49-58.
 [http://dx.doi.org/10.1016/j.fct.2018.09.040] [PMID:  30292620]

[48]
Hanna R. Fasciola hepatica: Histology of the reproductive organs and differential effects of triclabendazole on drug-sensitive and drug-resistant fluke isolates and on flukes from selected field cases. Pathogens  2015; 4(3): 431-56.
 [http://dx.doi.org/10.3390/pathogens4030431] [PMID:  26131614]

[49]
Liu P, He K, Li Y, Wu Q, Yang P, Wang D. Exposure to mercury causes formation of male-specific structural deficits by inducing oxidative damage in nematodes. Ecotoxicol Environ Saf  2012; 79: 90-100.
 [http://dx.doi.org/10.1016/j.ecoenv.2011.12.007] [PMID:  22209111]

[50]
Rudel D, Douglas CD, Huffnagle IM, Besser JM, Ingersoll CG. Assaying environmental nickel toxicity using model nematodes. PLoS One  2013; 8(10): e77079.
 [http://dx.doi.org/10.1371/journal.pone.0077079] [PMID:  24116204]

[51]
Liggett MR, Hoy MJ, Mastroianni M, Mondoux MA. High-glucose diets have sex-specific effects on aging in C. elegans: toxic to hermaphrodites but beneficial to males. Aging  2015; 7(6): 383-8.
 [http://dx.doi.org/10.18632/aging.100759] [PMID:  26143626]

[52]
Ruszkiewicz JA, Teixeira de Macedo G, Miranda-Vizuete A, et al. Sex-specific response of caenorhabditis elegans to methylmercury toxicity. Neurotox Res  2019; 35(1): 208-16.
 [http://dx.doi.org/10.1007/s12640-018-9949-4] [PMID:  30155682]

[53]
Li H, Wang W, Qu G, et al. Effect of the in vivo activity of dihydroartemisinin against Schistosoma mansoni infection in mice. Parasitol Res  2012; 110(5): 1727-32.
 [http://dx.doi.org/10.1007/s00436-011-2692-x] [PMID:  22006193]

[54]
Meyer D, Williams PL. Toxicity testing of neurotoxic pesticides in Caenorhabditis elegans. J Toxicol Environ Health B Crit Rev  2014; 17(5): 284-306.
 [http://dx.doi.org/10.1080/10937404.2014.933722] [PMID:  25205216]

[55]
Vanin AP, Tamagno WA, Alves C, et al. Neuroprotective potential of Cannabis sativa-based oils in Caenorhabditis elegans. Sci Rep  2022; 12(1): 15376.
 [http://dx.doi.org/10.1038/s41598-022-19598-3] [PMID:  36100636]

[56]
Joshi AKR, Nagaraju R, Rajini PS. Involvement of acetylcholinesterase inhibition in paralysing effects of monocrotophos in Caenorhabditis elegans. J Basic Appl Zool  2018; 79(33)

[57]
Elarabi NI, Abdel-Rahman AA, Abdel-Haleem H, Abdel-Hakeem M. Silver and zinc oxide nanoparticles disrupt essential parasitism, neuropeptidergic, and expansion-like proteins genes in Meloidogyne incognita. Exp Parasitol  2022; 243: 108402.
 [http://dx.doi.org/10.1016/j.exppara.2022.108402] [PMID:  36220396]

[58]
Khare P, Sonane M, Nagar Y, et al. Size dependent toxicity of zinc oxide nano-particles in soil nematode Caenorhabditis elegans. Nanotoxicology  2015; 9(4): 423-32.
 [http://dx.doi.org/10.3109/17435390.2014.940403] [PMID:  25051332]

[59]
Mellanby H. The identification and estimation of acetylcholine in three parasitic nematodes (Ascaris lumbricoides, Litomosoides carinii, and the microfilariae of Dirofilaria repens). Parasitology  1955; 45(3-4): 287-94.
 [http://dx.doi.org/10.1017/S0031182000027669] [PMID:  13280270]

[60]
Lee DL. Why do some nematode parasites of the alimentary tract secrete acetylcholinesterase? Int J Parasitol  1996; 26(5): 499-508.
 [http://dx.doi.org/10.1016/0020-7519(96)00040-9] [PMID:  8818729]

[61]
Tandon RS, Kumar P. Physiology of parasites: Transaminases (GOT and GPT) in the root-knot nematode, Meloidogyne luck nowica Singh 1969, and effect of sex on its enzyme levels. Zentralbl Bakteriol Naturwiss  1980; 135(2): 158-61.
 [http://dx.doi.org/10.1016/S0323-6056(80)80019-X] [PMID: 7424217]

[62]
Martínez GA, Trujillo LE. Understanding the role of alkaline phosphatase as a possible marker for the evaluation of antiparasitic agents. J Appl Pharm Sci  2018; 8(8): 123-8.

[63]
Morsy K, Fahmy S, Mohamed A, Ali S, El-Garhy M, Shazly M. Optimizing and evaluating the antihelminthic activity of the biocompatible zinc oxide nanoparticles against the ascaridid nematode, parascaris equorum in vitro. Acta Parasitol  2019; 64(4): 873-86.
 [http://dx.doi.org/10.2478/s11686-019-00111-2] [PMID:  31478140]

[64]
Abdel-Hamid H, Mekawey AAI. Biological and hematological responses of Biomphalaria alexandrina to mycobiosynthsis silver nanoparticles. J Egypt Soc Parasitol  2014; 44(3): 627-37.
 [http://dx.doi.org/10.12816/0007866] [PMID:  25643504]

[65]
Salama B, Alzahrani KJ, Alghamdi KS, et al. Silver nanoparticles enhance oxidative stress, inflammation, and apoptosis in liver and kidney tissues: Potential protective role of thymoquinone. Biol Trace Elem Res  2022; 201(6): 2942-54.
 [PMID:  36018545]

[66]
Lee DL, Atkinson HJ. Physiology of Nematodes.  (2nd ed.), London: Macmillan Education UK 1976.
 [http://dx.doi.org/10.1007/978-1-349-02667-8]

[67]
Diamantino TC, Almeida E, Soares AMVM, Guilhermino L. Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. Chemosphere  2001; 45(4-5): 553-60.
 [http://dx.doi.org/10.1016/S0045-6535(01)00029-7] [PMID: 11680751]

[68]
Nayak S, Mishra CSK, Guru BC, Samal S. Histological anomalies and alterations in enzyme activities of the earthworm Glyphidrillus tuberosus exposed to high concentrations of phosphogypsum. Environ Monit Assess  2018; 190(9): 529.
 [http://dx.doi.org/10.1007/s10661-018-6933-7] [PMID:  30121706]

[69]
Davuluri T, Chennuru S, Pathipati M, Krovvidi S, Rao GS. In vitro anthelmintic activity of three tropical plant extracts on haemonchus contortus. Acta Parasitol  2020; 65(1): 11-8.
 [http://dx.doi.org/10.2478/s11686-019-00116-x] [PMID:  31552583]

[70]
Keller U. Nutritional laboratory markers in malnutrition. J Clin Med  2019; 8(6): 775.
 [http://dx.doi.org/10.3390/jcm8060775] [PMID:  31159248]

[71]
McCarthy MP, Carroll DL, Ringwood AH. Tissue specific responses of oysters, crassostrea virginica, to silver nanoparticles. Aquat Toxicol  2013; 138-139: 123-8.
 [http://dx.doi.org/10.1016/j.aquatox.2013.04.015] [PMID:  23728357]

[72]
Adlimoghaddam A, Boeckstaens M, Marini AM, Treberg JR, Brassinga AKC, Weihrauch D. Ammonia excretion in Caenorhabditis elegans: Mechanism and evidence of ammonia transport of the Rhesus protein CeRhr-1. J Exp Biol  2015; 218(5): 675-83.
 [http://dx.doi.org/10.1242/jeb.111856] [PMID:  25740900]

[73]
Ajeniyi SA, Solomon RJ. Urea And Creatinine Of Clarias Gariepinus In Three Different Commercial Ponds. Nat Sci  2014; 12(10): 124-38.

[74]
El-Khayat HMM, Abdel-Hamid H, Mahmoud KMA, Gaber HS, Abu Taleb HMA, Flefel HE. Snails and fish as pollution biomarkers in lake manzala and laboratory c: Laboratory exposed snails to chemical mixtures. Int J Agric Biosyst Eng  2016; 10(11)

[75]
Mamdouh S, Mohamed AS, Mohamed HA, Fahmy WS. The effect of zinc concentration on physiological, immunological, and histological changes in crayfish (Procambarus clarkii) as bio-indicator for environment quality criteria. Biol Trace Elem Res  2022; 200(1): 375-84.
 [http://dx.doi.org/10.1007/s12011-021-02653-x] [PMID:  33641053]

[76]
Mowrey WR, Bennett JR, Portman DS. Distributed effects of biological sex define sex-typical motor behavior in Caenorhabditis elegans. J Neurosci  2014; 34(5): 1579-91.
 [http://dx.doi.org/10.1523/JNEUROSCI.4352-13.2014] [PMID: 24478342]

[77]
Eisenback JD. Detailed morphology and anatomy of second-stage juveniles, males and females of the genus Meloidogyne (root-knot nematodes). In: Barker KR, Carter CC, Sasser JN, Eds. An Advance Treatise on Meloidogyne: Methodology.  North Carolina: Department of Plant Pathology, North Carolina State University 1985; Vol. 2: pp. 47-77.

[78]
Wong PCL, Yeung SB. Production of uric acid in the adult lung worm, Metastrongylus apri (nematoda: metastrongyloidea), from pigs. Comp Biochem Physiol B  1980; 66(2): 323-6.
 [http://dx.doi.org/10.1016/0305-0491(80)90072-3]

[79]
Shekari M, Sendi JJ, Etebari K, Zibaee A, Shadparvar A. Effects of Artemisia annua L. (Asteracea) on nutritional physiology and enzyme activities of elm leaf beetle, xanthogaleruca luteola mull. (Coleoptera: Chrysomellidae). Pestic Biochem Physiol  2008; 91(1): 66-74.
 [http://dx.doi.org/10.1016/j.pestbp.2008.01.003]

[80]
Wan QL, Fu X, Dai W, et al. Uric acid induces stress resistance and extends the life span through activating the stress response factor DAF-16/FOXO and SKN-1/NRF2. Aging  2020; 12(3): 2840-56.
 [http://dx.doi.org/10.18632/aging.102781] [PMID:  32074508]

[81]
Kutzing MK, Firestein BL. Altered uric acid levels and disease states. J Pharmacol Exp Ther  2008; 324(1): 1-7.
 [http://dx.doi.org/10.1124/jpet.107.129031] [PMID:  17890445]

[82]
Wang T, Ma G, Nie S, Williamson NA, Reid GE, Gasser RB. Lipid composition and abundance in the reproductive and alimentary tracts of female Haemonchus contortus. Parasit Vectors  2020; 13(1): 338.
 [http://dx.doi.org/10.1186/s13071-020-04208-w] [PMID:  32631412]

[83]
Kurzchalia TV, Ward S. Why do worms need cholesterol? Nat Cell Biol  2003; 5(8): 684-8.
 [http://dx.doi.org/10.1038/ncb0803-684] [PMID:  12894170]

[84]
Preet S, Tomar RS. Anthelmintic effect of biofabricated silver nanoparticles using Ziziphus jujuba leaf extract on nutritional status of Haemonchus contortus. Small Rumin Res  2017; 154: 45-51.
 [http://dx.doi.org/10.1016/j.smallrumres.2017.07.002]

[85]
Zeumer R, Galhano V, Monteiro MS, et al. Chronic effects of wastewater-borne silver and titanium dioxide nanoparticles on the rainbow trout (Oncorhynchus mykiss). Sci Total Environ  2020; 723(137974): 137974.
 [http://dx.doi.org/10.1016/j.scitotenv.2020.137974] [PMID: 32229380]

[86]
Omara EA, Aly HF, Nada SA. Chitosan induced hepato-nephrotoxicity in mice with special reference to gender effect in glycolytic enzymes activities. Regul Toxicol Pharmacol  2012; 62(1): 29-40.
 [http://dx.doi.org/10.1016/j.yrtph.2011.11.010] [PMID:  22154824]

[87]
Ibrahim AMA, Ali AM. Silver and zinc oxide nanoparticles induce developmental and physiological changes in the larval and pupal stages of Spodoptera littoralis (Lepidoptera: Noctuidae). J Asia Pac Entomol  2018; 21(4): 1373-8.
 [http://dx.doi.org/10.1016/j.aspen.2018.10.018]

[88]
Bahaaeldine MA, El Garhy M, Fahmy SR, Mohamed AS. In vitro anti-Toxocara vitulorum effect of silver nanoparticles. J Parasit Dis  2022; 46(2): 409-20.
 [http://dx.doi.org/10.1007/s12639-021-01464-0] [PMID:  35692463]
Cite As
Current Nanomedicine

Reproductive and Biochemical Toxicity of Biobased Silver Nanoparticles against Toxocara vitulorum

Abstract

Graphical Abstract
