Synthesis and Characterization of Silver Nanoparticles from Ethanolic Extracts of Leaves of Annona muricata: A Green Nanobiotechnology Approach

Main Article Content

Yahaya Gavamukulya
Esther N. Maina
Fred Wamunyokoli
Amos M. Meroka
Edwin S. Madivoli
Hany A. El-Shemy
Gabriel Magoma

Abstract

Introduction: The biological green synthesis of nanoparticles via nanobiotechnology processes have a significant potential to boost nanoparticles production without the use of harsh, toxic, and expensive chemicals commonly used in conventional physical and chemical processes. Annona muricata, a tropical plant belonging to family Annonaceae is one of the most used plants in folk medicine because of its many medicinal uses and therefore presents a strong candidate for use in green synthesis.

Aims: The aim of this study was to optimize a method for the synthesis of Silver Nanoparticles (AgNPs) from ethanolic extracts of leaves of Annona muricata as well as to characterize the green synthesized AgNPs.

Methodology: AgNPs were synthesized from Annona muricata leaves using AgNO3 solution. The AgNPs were characterized using spectroscopy and microscopy techniques.

Results: The formed AgNPs had an absorption maximum at 429 nm using UV–Visible spectroscopy and were stable under different pH, temperature, and storage conditions. Fourier transform infrared analysis revealed the different functional groups responsible for the synthesis and stabilization of the AgNPs. Scanning electron microscopy analysis revealed a spherical nature of the synthesized AgNPs. Energy dispersive x-ray spectroscopy analysis showed presence of Ag, O, and Cl with Ag having the highest composition at 60%. X-Ray Diffraction and Dynamic Light Scattering revealed a crystalline nature of AgNPs with an average size of 87.36 nm and a polydispersity index of 0.16 respectively. Transmission Electron Microscopy analysis further confirmed the crystalline and spherical nature of the AgNPs.

Conclusion: In this article, an efficient, eco-friendly and low-cost method for the synthesis and recovery of stable AgNPs using Annona muricata leaves ethanolic extracts as both a reducing and capping agent has been reported for the first time. The synthesized AgNPs could be promising candidates for many biomedical, clinical, engineering, and polymer applications.

Keywords:
Annona muricata, silver nanoparticles (AgNPs), UV/VIS, FTIR, XRD, SEM, DLS, TEM.

Article Details

How to Cite
Gavamukulya, Y., Maina, E. N., Wamunyokoli, F., Meroka, A. M., Madivoli, E. S., El-Shemy, H. A., & Magoma, G. (2019). Synthesis and Characterization of Silver Nanoparticles from Ethanolic Extracts of Leaves of Annona muricata: A Green Nanobiotechnology Approach. Biotechnology Journal International, 23(4), 1-18. https://doi.org/10.9734/bji/2019/v23i430083
Section
Original Research Article

References

Talib W. Anticancer and antimicrobial potential of plant-derived natural products. In: Rasooli I, Editor. Phytochem. Impact Heal., Intech Open. 2011;141–58.
DOI: 10.5772/26077

Gavamukulya Y, Abou-Elella F, Wamunyokoli F, El-Shemy HA. Phytochemical screening, anti-oxidant activity and in vitro anticancer potential of ethanolic and water leaves extracts of Annona muricata (Graviola). Asian Pac J Trop Med. 2014;7:S355-63.
DOI: 10.1016/S1995-7645(14)60258-3

Coria-Te´llez AV, Montalvo-Gonzalez E, Yahia E, Obledo-Va´Zquez EN. Annona muricata : A comprehensive review on its traditional medicinal uses, phytochemicals, pharmacological activities, mechanisms of action and toxicity. Arab J Chem. 2018;11:662-91.
DOI: 10.1016/j.arabjc.2016.01.004

Gavamukulya Y, Wamunyokoli F, El-Shemy HA. Annona muricata: Is the natural therapy to most disease conditions including cancer growing in our backyard? A systematic review of its research history and future prospects. Asian Pac J Trop Med. 2017;10:835-48.
DOI: 10.1016/J.APJTM.2017.08.009

Pinto A, De Q, Cordeiro M, De Andrade, SRM Ferreira F, Filgueiras H, De C, et al. Annona muricata. In: Williams JT, Editor. Annona Species, Taxon. Bot. Inter-national Cent. Underutil. Crop., Southampton, UK: University of Southampton; 2005;3-16.

Benavides A, González A, Cisne Contreras J. Numerical characterization of guanabana (Annona muricata L.) germplasm sampling in situ in the pacific and northern Nicaragua. La Calera. 2004;10:46-52.

Evangelista-Lozano S, Cruz-Castillo J, Pe´rez-Gonza´lez S, Mercado-Silva E, Da´vila-Ortiz G. Production and fruit quality of guanabanos (Annona muricata L.) from jiutepec seed, morelos, Mexico. Chapingo Hortic Ser. 2003;9:69-79.

Orwa C, Mutua A, Kindt R. Agroforestree database: A tree species reference and selection guide version 4.0. ICRAF, Nairobi, KE; 2009.

Gavamukulya Y, Abou-Elella F, Wamunyokoli F, El-Shemy HA. GC-MS analysis of bioactive phytochemicals present in ethanolic extracts of leaves of annona muricata: A further evidence for its medicinal diversity. Pharmacogn J. 2015;7:300-4.
DOI: 10.5530/pj.2015.5.9

Gavamukulya Y, Maina EN, Meroka AM, Madivoli ES, El-Shemy HA, Magoma G, et al. Liquid chromatography single quadrupole mass spectrometry (LC/SQ MS) analysis reveals presence of novel antineoplastic metabolites in ethanolic extracts of fruits and leaves of Annona muricata. Pharmacogn J. 2019;11:660-8.
DOI: 10.5530/pj.2019.11.104

Badrie N, Schauss A. Soursop (Annona muricata L.): Composition, nutritional value, medicinal uses, and toxicology. In: Watson R, Preedy V, Editors. Bioact. Foods Promot. Heal., Oxford: Academic Press. 2010;621–43.

Leatemia JA, Isman MB. Insecticidal activity of crude seed extracts of Annona spp., Lansium domesticum and Sandoricum koetjape against lepidopteran larvae. Phytoparasitica. 2004;32:30-7.
DOI: 10.1007/BF02980856

Langenberger G, Prigge V, Martin K, Belonias B, Sauerborn J. Ethnobotanical knowledge of Philippine lowland farmers and its application in agroforestry. Agrofor Syst. 2009;76:173-94.
DOI: 10.1007/s10457-008-9189-3

Betancur-Galvis L, Saez J, Granados H. Antitumor and antiviral activity of Colombian medicinal plant extracts. Mem Inst Oswaldo Cruz. 1999;94:531-5.
DOI: 10.1590/S0074-02761999000400019

Magan˜a MA, Gama LM, Mariaca R. The use of medicinal plants in communities maya-chontales of nacajuca, tabasco, Mexico. Polibotánica. 2010;29:213-62.

De Filipps R, Maina S, Crepin J. Medicinal plants of the Guianas (Guyana, Surinam, French Guiana). Washington, DC: Department of Botany, National Museum of Natural History, Smithsonian Institution; 2004.

Joyeux M, Mortier F, Fleurentin J. Screening of antiradical, antilipoperoxidant and hepatoprotective effects of nine plant extracts used in Caribbean folk medicine. Phyther Res. 1995;9:228-30.
DOI: 10.1002/ptr.2650090316

Beyra A, Leo´ n MC, Iglesias E, Ferra´ ndiz D, Herrera R, Volpato G, et al. Ethnobotanical studies on medicinal plants in the province of Camagüey (Cuba). Ann Gard. 2004;185-204.

Kossouoh C, Moudachirou M, Adjakidje V, Chalchat JC, Figuérédo G. Essential oil chemical composition of Annona muricata L. leaves from Benin. J Essent Oil Res. 2007;19:307-9.
DOI: 10.1080/10412905.2007.9699288

Vandebroek I, Balick MJ, Ososki A, Kronenberg F, Yukes J, Wade C, et al. The importance of botellas and other plant mixtures in dominican traditional medicine. J Ethnopharmacol. 2010;128:20-41.
DOI: 10.1016/j.jep.2009.12.013.

Boyom FF, Fokou PVT, Yamthe LRT, Mfopa AN, Kemgne EM, Mbacham WF, et al. Potent antiplasmodial extracts from Cameroonian annonaceae. J Ethnopharmacol. 2011;134:717-24.
DOI: 10.1016/j.jep.2011.01.020.

Nguyen-Pouplina J, Hop T, Hung T, Tuyet, Anh Phan Christiane D, Jeremy F, Tinh HT, et al. Antimalarial and cytotoxic activities of ethnopharmacologically selected medicinal plants from South Vietnam. J Ethnopharmacol. 2007;109: 417-27.

Ssenyange C, Namulindwa A, Oyik B. Plants used to manage type II diabetes mellitus in selected districts of central Uganda. Afr Health Sci. 2015;15:496-502.
DOI: 10.4314/ahs.v15i2.24

Pieme CA, Kumar SG, Dongmo MS, Moukette BM, Boyoum FF, Ngogang JY, et al. Antiproliferative activity and induction of apoptosis by Annona muricata (Annonaceae) extract on human cancer cells. BMC Complement Altern Med. 2014;14:516.
DOI: 10.1186/1472-6882-14-516

Ross I. Medicinal plants of the world: Chemical constituents, traditional and modern medicinal uses. Second. Humana Press; 2010.

Atawodi S. Nigerian foodstuffs with prostate cancer chemopreventive polyphenols. Infect. Agent. Cancer. 2011;6:S9.
DOI: 10.1186/1750-9378-6-S2-S9

Samuel A, Kalusalingam A, Chellappan D, Gopinath R, Radhamani S, Husain H, et al. Ethnomedical survey of plants used by the orang asli in Kampung Bawong, perak, West Malaysia. J Ethnobiol Ethnomed. 2010;6:5.
DOI: 10.1186/1746-4269-6-5

Coe F. Rama midwifery in Eastern Nicaragua. J Ethnopharmacol. 2008;117: 136-157.

De Souza C, Karou SD, Tchacondo T, Djikpo Tchibozo MA, Abdoul-Rahaman S, Anani K, et al. Ethnobotanical study of medicinal plants used in the management of diabetes mellitus and hypertension in the Central Region of Togo. Pharm Biol. 2011;49:1286-97.
DOI: 10.3109/13880209.2011.621959.

Hajdu Z, Hohmann J. An ethnopharmacological survey of the traditional medicine utilized in the community of porvenir. Bajo Paraguá Indian Reservation, Bolivia. J Ethnopharmacol. 2012;139:838-857.

Monigatti M, Bussmann RW, Weckerle CS. Medicinal plant use in two Andeans communities located at different altitudes in the Bolívar Province, Peru. J. Ethnopharmacol. 2013;145:450-64.
DOI: 10.1016/j.jep.2012.10.066

Cijo George V, Naveen Kumar DR, Rajkumar V, Suresh PK, Ashok Kumar R. Quantitative assessment of the relative antineoplastic potential of the n-butanolic leaf extract of Annona muricata Linn. in normal and immortalized human cell lines. Asian Pacific J Cancer Prev. 2012;13:699-704.
DOI: 10.7314/APJCP.2012.13.2.699

Dai Y, Hogan S, Schmelz EM, Ju YH, Canning C, Zhou K. Selective growth inhibition of human breast cancer cells by graviola fruit extract in vitro and in vivo involving downregulation of EGFR expression. Nutr Cancer. 2011;63:795-801.
DOI: 10.1080/01635581.2011.563027

Valencia L, Mun˜oz D, Robledo S, Echeverri F, Arango G, Ve´lez I, et al. Trypanocidal and cytotoxic activity of extracts from Colombian plants. Biomédica. 2011;31:552-9.
DOI: 10.7705/biomedica.v31i4.426

Nawwar M, Ayoub N, Hussein S, Hashim A. Flavonol triglycoside and investigation of the antioxidant and cell stimulating activities of Annona muricata Linn. Arch Pharm Res. 2012;35:761-7.
DOI: 10.1007/s12272-012-0501-4

Ménan H, Banzouzi J, Hocquette A, Pélissier Y. Antiplasmodial activity and cytotoxicity of plants used in West African traditional medicine for the treatment of malaria. J Ethnopharmacol. 2006;105:131-136.
DOI: 10.1016/j.jep.2005.10.027

Moghadamtousi SZ, Rouhollahi E, Karimian H. The chemopotential effect of Annona muricata leaves against azoxymethane- induced colonic aberrant crypt foci in rats and the apoptotic effect of acetogenin annomuricin E in HT-29 cells: A bioassay- guided approach. PLoS One. 2015;10:1-28.
DOI: 10.1371/journal.pone.0122288

Bonifácio BV, Silva PB Da, Ramos MADS, Negri KMS, Bauab TM, Chorilli M. Nanotechnology-based drug delivery systems and herbal medicines: A review. Int J Nanomedicine. 2014;9:1-15.
DOI: 10.2147/IJN.S52634

Ansari SH, Islam F, Sameem M. Influence of nanotechnology on herbal drugs: A review. J Adv Pharm Technol Res. 2012;3:142–6.
DOI: 10.4103/2231-4040.101006

Gonzalez-Melendi P, Fernandez-Pacheco R, Coronado MJ, Corredor E, Testillano PS, Risueo MC, et al. Nanoparticles as smart treatment-delivery systems in plants: Assessment of different techniques of microscopy for their visualization in plant tissues. Ann Bot. 2008;101:187- 95.
DOI: 10.1093/aob/mcm283

Murphy CJ, Gole AM, Hunyadi SE, Orendorff CJ. One-dimensional colloidal gold and silver nanostructures. Inorg Chem. 2006;45:7544-54.
DOI: 10.1021/ic0519382

Wiley BJ, Chen Y, McLellan JM, Xiong Y, Li Z-Y, Ginger D, et al. Synthesis and optical properties of silver nanobars and nanorice. Nano Lett. 2007;7:1032-6.
DOI: 10.1021/nl070214f

Xiong Y, Cai H, Wiley BJ, Wang J, Kim MJ, Xia Y. Synthesis and mechanistic study of palladium nanobars and nanorods. J Am Chem Soc. 2007;129:3665-75.
DOI: 10.1021/ja0688023

Fang J, You H, Kong P, Yi Y, Song X, Ding B. Dendritic silver nanostructure growth and evolution in replacement reaction. Cryst Growth Des. 2007;7:864-7.
DOI: 10.1021/cg0604879

Narayan A, Landström L, Boman M. Laser-assisted synthesis of ultra small metal nanoparticles. Appl Surf Sci. 2003;208–209:137–41.
DOI: 10.1016/S0169-4332(02)01352-1

Ahmed S, Ahmad M, Swami BL, Ikram S. A review on plants extract mediated synthesis of silver nanoparticles for antimicrobial applications: A green expertise. J Adv Res. 2016;7:17-28.
DOI: 10.1016/j.jare.2015.02.007

Gavamukulya Y, Maina EN, Meroka AM, Madivoli ES, El-Shemy HA, Wamunyokoli F, et al. Green synthesis and characterization of highly stable silver nanoparticles from ethanolic extracts of fruits of Annona muricata. J Inorg Organomet Polym Mater; 2019.
DOI: 10.1007/s10904-019-01262-5

Santhosh SB, Ragavendran C, Natarajan D. Spectral and HRTEM analyses of Annona muricata leaf extract mediated silver nanoparticles and its larvicidal efficacy against three mosquito vectors Anopheles stephensi, Culex quinquefasciatus, and Aedes aegypti. J Photochem Photobiol B Biol. 2015;153: 184-90.
DOI: 10.1016/j.jphotobiol.2015.09.018

Shah M, Fawcett D, Sharma S, Tripathy S, Poinern G. Green synthesis of metallic nanoparticles via biological entities. Materials (Basel). 2015;8:7278-308.
DOI: 10.3390/MA8115377

Kumar B, Smita K, Cumbal L, Debut A. Green synthesis of silver nanoparticles using Andean blackberry fruit extract. Saudi J Biol Sci. 2017;24:45-50.
DOI: 10.1016/J.SJBS.2015.09.006

Ahmed S, Saifullah, Ahmad M, Swami BL, Ikram S. Green synthesis of silver nanoparticles using Azadirachta indica aqueous leaf extract. J Radiat Res Appl Sci. 2016;9:1-7.
DOI: 10.1016/j.jrras.2015.06.006

PS P, KS T. Antioxidant, antibacterial and cytotoxic potential of silver nanoparticles synthesized using terpenes rich extract of Lantana camara L. leaves. Biochem Biophys Reports. 2017;10:76-81.
DOI: 10.1016/j.bbrep.2017.03.002

Ezealisiji KM, Noundou XS, Ukwueze SE. Green synthesis and characterization of monodispersed silver nanoparticles using root bark aqueous extract of Annona muricata Linn and their antimicrobial activity. Appl Nanosci. 2017;7:905-11.
DOI: 10.1007/s13204-017-0632-5

Verma A, Mehata MS. Controllable synthesis of silver nanoparticles using neem leaves and their antimicrobial activity. J Radiat Res Appl Sci. 2016;9: 109-15.
DOI: 10.1016/j.jrras.2015.11.001

Ghoshal G, Bhatnagar S. Rapid green synthesis of silver nanoparticles (AgNPs) using (Prunus persica) plants extract: Exploring its antimicrobial and catalytic activities. J Nanomed Nanotechnol. 2017;84172:4522157-7439.
DOI: 10.4172/2157-7439.1000452

Madivoli ES, Maina EG, Kairigo PK, Murigi MK, Ogilo JK, Nyangau JO, et al. In vitro antioxidant and antimicrobial activity of Prunus africana (Hook. f.) Kalkman (bark extracts) and Harrisonia abyssinica Oliv. extracts (bark extracts): A comparative study. J Med Plants Econ Dev. 2018;2:1-9.
DOI: 10.4102/jomped.v2i1.39

Danaei M, Dehghankhold M, Ataei S, Hasanzadeh Davarani F, Javanmard R, Dokhani A, et al. Impact of particle size and polydispersity index on the clinical applications of lipidic nanocarrier systems. Pharmaceutics. 2018;10:1-17.
DOI: 10.3390/pharmaceutics10020057

Shankar S, Rai A, Ahmad A, Sastry A. Rapid synthesis of Au, Ag, and bimetallic Au core Ag shell nanoparticles using neem (Azadirachta indica) leaf broth. J Colloid Interface Sci. 2004;275:496-502.

Song JY, Beom SK. Rapid biological synthesis of silver nanoparticles using plant leaf extracts. Bioprocess Biosyst Eng. 2009;32:79-84.
DOI: 10.1007/s00449-008-0224-6

Otari SV, Pawar SH, Patel SKS, Singh RK, Kim SY, Lee JH, et al. Canna edulis leaf extract-mediated preparation of stabilized silver nanoparticles: Characterization, antimicrobial activity and toxicity studies. J Microbiol Biotechnol. 2017;27:731-8.
DOI: 10.4014/jmb.1610.10019

Santhosh SB, Yuvarajan R, Natarajan D. Annona muricata leaf extract-mediated silver nanoparticles synthesis and its larvicidal potential against dengue, malaria and filariasis vector. Parasitol Res. 2015;114:3087-96.
DOI: 10.1007/s00436-015-4511-2

Gavamukulya Y. Phytochemical composition, anti-oxidant and in vitro cytotoxic properties of extracts of leaves of Annona muricata (Graviola). PAUSTI Repository; 2014.
DOI: 10.13140/RG.2.1.3446.4484

Coria-Te´llez AV, Montalvo-Gonzalez E, Yahia EEM, Obledo-Va´Zquez EN, Coria-Téllez AAV, Montalvo-Gónzalez E, et al. Annona muricata: A comprehensive review on its traditional medicinal uses, phytochemicals, pharmacological activities, mechanisms of action and toxicity. Arab J Chem; 2016.
DOI: 10.1016/j.arabjc.2016.01.004

Moghadamtousi SZ, Fadaeinasab M, Nikzad S, Mohan G, Ali H, Kadir H. Annona muricata (Annonaceae): A review of Its traditional uses, isolated acetogenins and biological activities. Int J Mol Sci. 2015;16:15625-58.
DOI: 10.3390/ijms160715625

Kumar B, Angulo Y, Smita K, Cumbal L, Debut A. Capuli cherry-mediated green synthesis of silver nanoparticles under white solar and blue LED light. Particuology. 2016;24:123-8.
DOI: 10.1016/j.partic.2015.05.005

Umadevi M, Shalini S, Bindhu MR. Synthesis of silver nanoparticle using D. carota extract. Adv Nat Sci Nanosci Nanotechnol. 2012;3:025008.
DOI: 10.1088/2043-6262/3/2/025008

Goudarzi M, Mir N, Mousavi-Kamazani M, Bagheri S, Salavati-Niasari M. Biosynthesis and characterization of silver nanoparticles prepared from two novel natural precursors by facile thermal decomposition methods. Sci Rep. 2016;6:1-13.
DOI: 10.1038/srep32539

Otunola GA, Afolayan AJ. In vitro antibacterial, antioxidant and toxicity profile of silver nanoparticles green-synthesized and characterized from aqueous extract of a spice blend formulation. Biotechnol Biotechnol Equip. 2018;32:724-33.
DOI: 10.1080/13102818.2018.1448301

Sudha A, Jeyakanthan J, Srinivasan P. Green synthesis of silver nanoparticles using Lippia nodiflora aerial extract and evaluation of their antioxidant, antibacterial and cytotoxic effects. Resour Technol. 2017;3:506-15.
DOI: 10.1016/J.REFFIT.2017.07.002

Tomaszewska E, Soliwoda K, Kadziola K, Tkacz-Szczesna B, Celichowski G, Cichomski M, et al. Detection limits of DLS and UV-Vis spectroscopy in characterization of polydisperse nanoparticles colloids. J Nanomater.; 2013.
DOI: 10.1155/2013/313081

Clarke SP. Development of hierarchical magnetic nanocomposite materials for biomedical applications. Ph.D. Thesis, Dublin City University, Northside, Dublin; 2013.