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Structural and Physicochemical Characterization of Spirulina (Arthrospira maxima) Nanoparticles by High-Resolution Electron Microscopic Techniques

Published online by Cambridge University Press:  12 August 2016

Elier Ekberg Neri-Torres ,
Jorge J. Chanona-Pérez ,
Hector A. Calderón ,
Neil Torres-Figueredo ,
German Chamorro-Cevallos ,
Georgina Calderón-Domínguez  and
Hugo Velasco-Bedrán
Elier Ekberg Neri-Torres
Affiliation:
Departamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Wilfrido Massieu s/n. U. Profesional Adolfo López Mateos, Gustavo A. Madero, 07738 México D.F., Mexico
Jorge J. Chanona-Pérez*
Affiliation:
Departamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Wilfrido Massieu s/n. U. Profesional Adolfo López Mateos, Gustavo A. Madero, 07738 México D.F., Mexico
Hector A. Calderón
Affiliation:
Escuela Superior de Física y Matemáticas, Instituto Politécnico Nacional, Av. Instituto Politécnico Nacional Edificio 9, U. Profesional Adolfo López Mateos, Gustavo A. Madero, 07738 México D.F., Mexico
Neil Torres-Figueredo
Affiliation:
Centro de Investigación en Ciencia Aplicada y Tecnología Avanzada, IPN, Calzada Legaria, No. 694, Colonia Irrigación, Delegación Miguel Hidalgo, Código Postal 11500, México Distrito Federal, Mexico Centro de Aplicaciones Tecnológicas y Desarrollo Nuclear (CEADEN), Calle 30 #502 el 5ta Av y 7ma ZIP code 6122 Miramar Playa La Habana, Cuba
German Chamorro-Cevallos
Affiliation:
Departamento de Toxicología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Wilfrido Massieu s/n. U. Profesional Adolfo López Mateos, Gustavo A. Madero, 07738 México D.F., Mexico
Georgina Calderón-Domínguez
Affiliation:
Departamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Wilfrido Massieu s/n. U. Profesional Adolfo López Mateos, Gustavo A. Madero, 07738 México D.F., Mexico
Hugo Velasco-Bedrán
Affiliation:
Departamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Wilfrido Massieu s/n. U. Profesional Adolfo López Mateos, Gustavo A. Madero, 07738 México D.F., Mexico
*
*Corresponding author. jorge_chanona@hotmail.com
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Abstract

The objective of this work was to obtain Spirulina (Arthrospira maxima) nanoparticles (SNPs) by using high-impact mechanical milling and to characterize them by electron microscopy and spectroscopy techniques. The milling products were analyzed after various processing times (1–4 h), and particle size distribution and number mean size (NMS) were determined by analysis of high-resolution scanning electron microscopic images. The smallest particles are synthesized after 3 h of milling, had an NMS of 55.6±3.6 nm, with 95% of the particles being smaller than 100 nm. High-resolution transmission electron microscopy showed lattice spacing of ~0.27±0.015 nm for SNPs. The corresponding chemical composition was obtained by energy-dispersive X-ray spectroscopy, and showed the presence of Ca, Fe, K, Mg, Na, and Zn. The powder flow properties showed that the powder density was higher when the average nanoparticle size is smaller. They showed free flowability and an increase in their specific surface area (6.89±0.23 m2/g) up to 12–14 times larger than the original material (0.45±0.02 m2/g). Fourier transform infrared spectroscopy suggested that chemical damage related to the milling is not significant.

Keywords

Spirulina nanoparticleshigh-impact mechanical millinghigh-resolution electron microscopyspecific surface area
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 4 , August 2016 , pp. 887 - 901
Copyright
© Microscopy Society of America 2016 

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References

Abdullah, E.C. & Geldart, D. (1999). The use of bulk density measurements as flowability indicators. Powder Technol 12, 151–165.CrossRefGoogle Scholar
Arzt, E. (1998). Size effects in materials due to microstructural and dimensional constrains: A comparative review. Acta Mater 46, 5611–5626.CrossRefGoogle Scholar
Barbosa-Cánovas, G.V., Ortega-Rivas, E., Juliano, P. & Yan, H. (2005). Food Powders Physical Properties, Processing and Functionality. New York: Kluwer Academic/Plenum Publishers.Google Scholar
Belay, A., Ota, Y., Miyakawa, K. & Shimamatsu, H. (1993). Current knowledge on potential health benefits of Spirulina. J Appl Phycol 5, 235–241.CrossRefGoogle Scholar
Borm, P.J., Robbins, D., Haubold, S., Kuhlbusch, T., Fissan, H., Donaldson, K., Schins, R., Stone, V., Kreyling, W., Lademann, J., Krutmann, J., Warheit, D. & Oberdorster, E. (2006). The potential risks of nanomaterials: A review carried out for ECETOC. Part Fibre Toxicol 3, 1–35.CrossRefGoogle Scholar
Calderon, H.A., Kisielowski, C., Specht, P., Barton, B., Godinez-Salomon, F. & Solorza-Feria, O. (2015). Maintaining the genuine structure of 2D materials and catalytic nanoparticles at atomic resolution. Micron 68, 164–175.CrossRefGoogle Scholar
Chamorro, G., Pérez-Albiter, M., Serrano-García, N., Mares-Sámano, J.J. & Rojas, P. (2006). Spirulina maxima pretreatment partially protects against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity. Nutr Neurosci 9, 207–212.CrossRefGoogle Scholar
Chen, D., Chen, D., Jiao, X., Zhao, Y. & He, M. (2003). Hydrothermal synthesis and characterization of octahedral nickel ferrite particles. Powder Technol 133, 247–250.CrossRefGoogle Scholar
Chen, H., Liu, Y.L., Zhao, X.Q., Xiao, Y.G. & Liu, Y. (2015). Numerical investigation on angle of repose and force network from granular pile in variable gravitational environments. Powder Technol 283, 607–617.CrossRefGoogle Scholar
Cipolloni, G., Pellizzari, M., Molinari, A., Hebda, M. & Zadra, M. (2015). Contamination during the high-energy milling of atomized copper powder and its effects on spark plasma sintering. Powder Technol 275, 51–59.CrossRefGoogle Scholar
Del Angel, P., Rodriguez-Hernandez, J.H., Garcia-Borquez, A. & De La Fuente, J.A.M. (2013). Nucleation and growth of Ni0 nanoparticles and thin films by TEM electron irradiation. Catal Today 212, 194–200.CrossRefGoogle Scholar
Dotto, G.L., Cadaval, T.R.S. & Pinto, L.A.A. (2012 a). Preparation of bionanoparticles derived from Spirulina platensis and its application for Cr (VI) removal from aqueous solutions. J Ind Eng Chem 18, 1925–1930.CrossRefGoogle Scholar
Dotto, G.L., Lima, E.C. & Pinto, L.A.A. (2012 b). Biosorption of food dyes onto Spirulina platensis nanoparticles: Equilibrium isotherm and thermodynamic analysis. Bioresour Technol 103, 123–130.CrossRefGoogle ScholarPubMed
Endo, Y. (2009). Estimate of confidence intervals for geometric mean diameter and geometric standard deviation of lognormal size distribution. Powder Technol 193, 154–161.CrossRefGoogle Scholar
Geitler, L. (1932). Cyanophyceae. Kryptogamen-Flora von Deutschlands, Osterreich und der Schweiz. Koenigstein, Germany: Koeltz Scientific Books.Google Scholar
Gershwin, M.E. & Belay, A. (Eds.) 2008). Spirulina in Human Nutrition and Health. Boca Raton, FL: CRC Press Taylor and Francis Group.Google Scholar
Gupta, V., Ratha, S.K., Sood, A., Chaudhary, V. & Prasanna, R. (2013). New insights into the biodiversity and applications of cyanobacteria (blue-green algae)—Prospects and challenges. Algal Res 2, 79–97.CrossRefGoogle Scholar
Haque, S.E. & Gilani, K.M.A. (2005). Effect of ambroxol, Spirulina and vitamin-E in naphthalene induced cataract in female rats. Indian J Physiol Pharmacol 49, 57–64.Google ScholarPubMed
Hayashi, K., Hayashi, T., Morita, N. & Kojima, I. (1993). An extract from S. platensis is a selective inhibitor of herpes simplex virus type 1. Phytother Res 7, 76–80.CrossRefGoogle Scholar
Hayes, G.D. (1987). Food Engineering Data Handbook. New York: John Wiley & Sons.Google Scholar
Hernandez-Corona, A., Nieves, I., Meckes, M., Chamorro-Cevallos, G. & Barron, B.L. (2002). Anti viral activity of Spirulina maxima against herpes simplex virus type 2. Antiviral Res 56, 279–285.CrossRefGoogle Scholar
Ho, T.M., Howes, T. & Bhandari, B.R. (2015). Characterization of crystalline and spray-dried amorphous α-cyclodextrin powders. Powder Technol 284, 585–594.CrossRefGoogle Scholar
Hong, S.-M., Park, J.-J., Park, E.-K., Kim, K.-Y., Lee, J.-G., Lee, M.-K., Rhee, C.-K. & Lee, J.K. (2015). Fabrication of titanium carbide nano-powders by a very high speed planetary ball milling with a help of process control agents. Powder Technol 274, 393–401.CrossRefGoogle Scholar
Hsiao, G., Po-Hsiu, C., Ming-Yi, S., Duen-Suey, C., Cien-Huang, L. & Joen-Rong, S. (2005). C-phycocyanin, a very potent and novel platelet aggregation inhibitor from Spirulina platensis . J Agric Food Chem 53, 7734–7740.CrossRefGoogle ScholarPubMed
Ileleji, K.E. & Zhou, B. (2008). The angle of repose of bulk corn stover particles. Powder Technol 187, 110–118.CrossRefGoogle Scholar
Kakuk, G., Zsoldos, I., Csanády, Á. & Oldal, I. (2009). Contributions to the modelling of the milling process in a planetary ball mill. Rev Adv Mater Sci 22, 21–38.Google Scholar
Khan, M., Varadharaj, S., Ganesan, L.P., Shobha, J.C., Naidu, M.U., Parinandi, N.L., Tridandapani, S., Kutala, V.K. & Kuppusamy, P. (2006). C-phycocyanin protects against ischemia-reperfusion injury of heart through involvement of p38 MAPK and ERK signaling. Am J Physiol Heart Circ Physiol 290, H2136–H2145.CrossRefGoogle ScholarPubMed
Khan, Z., Bhadouria, P. & Bisen, P.S. (2005). Nutritional and therapeutic potential of Spirulina. Curr Pharm Biotechnol 6, 373–379.CrossRefGoogle ScholarPubMed
Lee, J.B., Hayashi, T., Hayashi, K., Sankawa, U., Maeda, M., Nemoto, T. & Nakanishi, H. (1998). Further purification and structural analysis of calcium spirulan from Spirulina platensis . J Nat Prod 61, 1101–1104.CrossRefGoogle ScholarPubMed
Lü, L. & Lai, M.O. (1998). Mechanical Alloying. New York, NY: Springer Science + Business Media, LLC.CrossRefGoogle Scholar
Mao, T.K., Van de Water, J. & Gershwin, M.E. (2005). Effects of a Spirulina-based dietary supplement on cytokine production from allergic rhinitis patients. J Med Food 8, 27–30.CrossRefGoogle ScholarPubMed
Mascher, D., Paredes-Carbajal, M.C., Torres-Durán, P.V., Zamora-González, J., Díaz-Zagoya, J.C. & Juárez-Oropeza, M.A. (2006). Ethanolic extract of Spirulina maxima alters the vasomotor reactivity of aortic rings from obese rats. Arch Med Res 37, 50–57.CrossRefGoogle ScholarPubMed
Masuda, H. & Gotoh, K. (1999). Study on the sample size required for the estimation of mean particle diameter. Adv Powder Technol 10, 159–173.CrossRefGoogle Scholar
Masojídek, J., Torzillo, G. & Koblízek, M. (2013). Photosynthesis in Microalgae. In Handbook of Microalgal Culture: Applied Phycology and Bioyechnology, Richmond, A. & Hu, Q. (Eds.), pp. 21–36. John Wiley & Sons Ltd.CrossRefGoogle Scholar
Maurice, D. & Courtney, T.H. (1996). Milling dynamics: Part II. Dynamics of a SPEX mill and a one-dimensional mill. Metall Mater Trans A 27, 1973–1979.CrossRefGoogle Scholar
Mazzoli, A. & Favoni, O. (2012). Particle size, size distribution and morphological evaluation of airborne dust particles of diverse woods by scanning electron microscopy and image processing program. Powder Technol 225, 65–71.CrossRefGoogle Scholar
Mohammadi, M.S. & Harnby, N. (1997). Bulk density modelling as a means of typifying the microstructure and flow characteristics of cohesive powders. Powder Technol 92, 1–8.CrossRefGoogle Scholar
Murrieta-Pazos, I., Gaiani, C., Galet, L., Calvet, R., Cuq, B. & Scher, J. (2012). Food powders: Surface and form characterization revisited. J Food Eng 112, 1–21.CrossRefGoogle Scholar
Nagaoka, S., Shimizu, K., Kaneko, H., Shibayama, F., Morikawa, K., Kanamaru, Y., Otsuka, A., Hirahashi, T. & Kato, T. (2005). A novel protein C-phycocyanin plays a crucial role in the hypocholesterolemic action of Spirulina platensis concentrate in rats. J Nutr 135, 2425–2430.CrossRefGoogle Scholar
Nijkamp, M.G., Raaymakers, J.E.M.J., van Dillen, A.J. & De Jong, K.P. (2001). Hydrogen storage using physisorption—Materials demands. Appl Phys A Mater Sci Process 72, 619–623.CrossRefGoogle Scholar
Ozdemir, G., Karabay, N.U., Dalay, M.C. & Pazarbasi, B. (2004). Antibacterial activity of volatile component and various extracts of Spirulina platensis . Phytother Res 18, 754–757.CrossRefGoogle ScholarPubMed
Perea-Flores, M.J., Chanona-Pérez, J.J., Garibay-Febles, V., Calderón-Dominguez, G., Terrés-Rojas, E., Mendoza-Pérez, J.A. & Herrera-Bucio, R. (2011). Microscopy techniques and image analysis for evaluation of some chemical and physical properties and morphological features for seeds of the castor oil plant (Ricinus communis). Ind Crops Prod 34, 1057–1065.CrossRefGoogle Scholar
Petrak, D., Dietrich, S., Eckardt, G. & Köhler, M. (2015). Two-dimensional particle shape analysis from chord measurements to increase accuracy of particle shape determination. Powder Technol 284, 25–31.CrossRefGoogle Scholar
Pochet, P., Tominez, E., Chaffron, L. & Martin, G. (1995). Order-disorder transformation in Fe-Al under ball milling. Phys Rev B 52, 4006–4016.CrossRefGoogle ScholarPubMed
Ponce-Reyes, C.E., Chanona-Pérez, J.J., Garibay-Febles, V., Palacios-González, E., Karamath, J., Terrés-Rojas, E. & Calderon-Dominguez, G. (2014). Cellulose nanoparticles from Agave waste and its morphological and structural characterization. Rev Mex Ing Quím 13, 897–906.Google Scholar
Pons, M.N., Vivier, H., Belaroui, K., Bernard-Michel, B., Cordier, F., Oulhana, D. & Dodds, J.A. (1999). Particle morphology: From visualisation to measurement. Powder Technol 103, 44–57.CrossRefGoogle Scholar
Rasool, M., Sabina, E.P. & Lavanya, B. (2006). Anti-inflammatory effect of Spirulina fusiformis on adjuvant-induced arthritis in mice. Biol Pharm Bull 29, 2483–2487.CrossRefGoogle ScholarPubMed
Russ, J.C. (2011). The Image Processing Handbook, 6th ed. Boca Raton, FL: CRC Press Taylor and Francis Group.Google Scholar
Shinohara, K. (1997). Fundamental and rheological properties of powders. In Handbook of Powder Science and Technology, Fayed, M.E., Otten, L. & I. T. P. I. T. Publishing (Eds.), p. 914.CrossRefGoogle Scholar
Silva, G.A. (2006). Neuroscience nanotechnology: Progress, opportunities and challenges. Nat Rev Neurosci 7, 65–74.CrossRefGoogle ScholarPubMed
Suryanarayana, C. (2004). Mechanical Alloying and Milling. New York, NY: Marcel Dekker.CrossRefGoogle Scholar
Tokumitsu, K. (1997). Reduction of metal oxides by mechanical alloying method. Solid state ionics 101–103, 25–31.CrossRefGoogle Scholar
Ullah, M., Ali, E., Bee, S. & Hamid, A. (2014). Surfactant-assisted ball milling: A novel route to novel materials with controlled nanostructure—A review. Rev Adv Mater 37, 1–14.Google Scholar
Vonshak, A. (Ed.) (2002). Spirulina Platensis (Arthropsira): Physiology, Cell-Biology and Biotechnology. London: Taylor & Francis.Google Scholar
Wang, S., Yu, J. & Yu, J. (2008). The semi-crystalline growth rings of C-type pea starch granule revealed by SEM and HR-TEM during acid hydrolysis. Carbohydr Polym 74, 731–739.CrossRefGoogle Scholar
Wang, Y., Chang, C.-F., Chou, J., Chen, H.-L., Deng, X., Harvey, B.K., Cadet, J.L. & Bickford, P.C. (2005). Dietary supplementation with blueberries, spinach, or Spirulina reduces ischemic brain damage. Exp Neurol 193, 75–84.CrossRefGoogle ScholarPubMed
Yu, Y. & Wu, H. (2011). Effect of ball milling on the hydrolysis of microcrystalline cellulose in hot-compressed water. AIChE J 57, 793–800.CrossRefGoogle Scholar
Zhao, H., Kwak, J.H., Wang, Y., Franz, J.A., White, J.M. & Holladay, J.E. (2006). Effects of crystallinity on dilute acid hydrolysis of cellulose by cellulose ball-milling study. Energy Fuels 20, 807–811.CrossRefGoogle Scholar
Zhou, M., Wei, Z., Qiao, H., Zhu, L., Yang, H. & Xia, T. (2009). Particle size and pore structure characterization of silver nanoparticles prepared by confined arc plasma. J Nanomater 2009, 1–5.CrossRefGoogle Scholar