Magnetic Nanoparticles: Essential Factors for Sustainable Environmental Applications

water research 47 (2013) 2613e2632

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Review Magnetic nanoparticles: Essential factors for sustainable environmental applications

Samuel C.N. Tang, Irene M.C. Lo*

Department of Civil and Environmental Engineering, The Hong Kong University of Science and Technology, Hong Kong, China article info abstract

Article history: In recent years, there has been an increasing use of engineered magnetic nanoparticles for Received 9 November 2012 remediation and water treatments, leading to elevated public concerns. To this end, it is Received in revised form necessary to enhance the understanding of how these magnetic nanoparticles react with 6 February 2013 contaminants and interact with the surrounding environment during applications. This Accepted 8 February 2013 review aims to provide a holistic overview of current knowledge of magnetic nanoparticles Available online 4 March 2013 in environmental applications, emphasizing studies of zero-valent iron (nZVI), magnetite

(Fe3O4) and maghemite (g-Fe2O3) nanoparticles. Contaminant removal mechanisms by Keywords: magnetic nanoparticles are presented, along with factors affecting the ability of contam- Maghemite inant desorption. Factors inﬂuencing the recovery of magnetic nanoparticles are outlined, Magnetic describing the challenges of magnetic particle collection. The aggregation of magnetic Magnetite nanoparticles is described, and methods for enhancing stability are summarized. More- Nanoparticles over, the toxicological effects owing to magnetic nanoparticles are discussed. It is possible Remediation that magnetic nanoparticles can be applied sustainably after detailed consideration of Zero-valent iron these discussed factors. ª 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction ...... 2614 2. Removal of contaminants ...... 2615 2.1. Contaminants removal by nZVI ...... 2615

2.2. Contaminants removal by Fe3O4 and g-Fe2O3 nanoparticles ...... 2615 2.3. Effects of environmental conditions on contaminant removal ...... 2616 2.4. Effects of surface properties of magnetic nanoparticles on contaminant removal ...... 2617 3. Desorption of contaminants ...... 2617

3.1. Desorption from Fe3O4 and g-Fe2O3 nanoparticles ...... 2620 3.2. Regeneration of nZVI? ...... 2620 3.3. Desorption of contaminants in the environment ...... 2621 4. Recovery of magnetic nanoparticles ...... 2621 4.1. Forces acting on magnetic nanoparticles ...... 2621

* Corresponding author. Tel.: þ852 2358 7157; fax: þ852 2358 1534. E-mail address: [email protected] (I.M.C. Lo). 0043-1354/$ e see front matter ª 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.watres.2013.02.039 2614 water research 47 (2013) 2613e2632

4.2. Better recovery of magnetic nanoparticles ...... 2622 4.3. Questions in magnetic nanoparticles recovery ...... 2622 5. Aggregation ...... 2623 5.1. Particle size ...... 2623 5.2. Particle concentration ...... 2623 5.3. Forces governing aggregation ...... 2623 5.4. Stabilize magnetic nanoparticles ...... 2623 5.5. Trade off between stability and reactivity ...... 2624 6. Toxicity...... 2624 6.1. Size and shape of nanoparticles ...... 2625 6.2. Surface properties of magnetic nanoparticles ...... 2625 6.3. Nanoparticle concentration related to toxicity ...... 2626 6.4. Type of bacterial cell ...... 2626 6.5. Phytotoxicity of magnetic nanoparticles ...... 2626 6.6. Current limitations ...... 2627 7. Conclusions ...... 2627 Acknowledgements ...... 2627 References ...... 2627

1. Introduction performance, some researchers demonstrated the feasibility of reusing magnetic nanoparticles by desorbing the contami- In recent decades, various environmental challenges have nants and regaining the removal capacity in successive been mitigated due to a boom in nanotechnologies and treatment cycles (Hao et al., 2010; Hu et al., 2005a,b; Hu et al., nanomaterials development. Nanoparticles have been widely 2005a,b). However, there are numerous conditions influencing used in environmental applications and have shown prom- the applicability of magnetic nanoparticles in a sustainable ising performance in pollutant removal or toxicity mitigation treatment process. (Gavaskar et al., 2005; Tratnyek and Johnson, 2006). Among the These magnetic nanoparticles not only have a large most widely used nanoparticles, magnetic nanoparticles, removal capacity, fast kinetics and high reactivity for mainly nano zero-valent iron (nZVI), magnetite (Fe3O4) and contaminant removal due to their extremely small particle maghemite (g-Fe2O3) nanoparticles, have sparked an size and high surface-area-to-volume ratio, but also one more immense interest in research for engineering applications for important property, magnetism. This is a useful property for treatment of polluted water or subsurface environments (Hu water and wastewater treatment systems. The high reactivity et al., 2004, 2005a,b; Li et al., 2006a,b; Shen et al., 2009; of the magnetic nanoparticles for pollutant removal, a Yantasee et al., 2007). One of the most famous examples is the compact and efficient water or wastewater treatment system injection of nZVI into subsurface forming reactive treatment can take advantage of this. It is expected that magnetic sep- zones (Gavaskar et al., 2005; Grieger et al., 2010). Heavy metals aration could be a more cost effective and convenient method such as arsenic and chromium, and organic pollutants like for separating such tiny particles than sophisticated mem- chlorinated solvents, can be immobilized or reduced to less brane filtration. Separation of magnetic nanoparticles from toxic species by nZVI. The effectiveness of nZVI is not just solution with a low-gradient magnetic field or a hand-held limited to laboratory findings. Many companies working on magnet has been frequently reported (Hu et al., 2004, 2007a; the manufacturing of nZVI and its application for environ- Yantasee et al., 2007). However, although ample experimental mental remediation have been established (Mueller et al., photographic results elsewhere (Bhaumik et al., 2011; Do et al., 2012). In the U.S., numerous practical experience of site 2011; Li et al., 2010a,b; Liu et al., 2010; Shin et al., 2011; Zhang remediation using nZVI has been reported (Comba et al., 2011; and Kong, 2011) showed the feasibility of separation and re- Su et al., 2012). In Europe, although only three full scale ap- covery of magnetic nanoparticles from water or wastewater, plications were reported, there were many pilot test projects no successful real applications of magnetic particles for water with the application of nZVI for various contaminants or wastewater treatment have yet been reported. On top of the (Mueller et al., 2012). According to a case specific cost com- high surface free energy, the magnetism of nanoparticles has parison of pump and treat, permeable reactive barrier and been suspected to enhance the aggregation of nanoparticles nZVI technology on a site in New Jersey, it was estimated that and reduce the removal capacity (Petosa et al., 2010; Phenrat the cost for treating TCE and PCE with the application of nZVI et al., 2009a), so become a great hindrance to recover and was far lower than the other two technologies (PARS reuse magnetic nanoparticles. Environmental, 2013). Additionally, with extensive use of nanoparticles for a wide Moreover, a number of studies have also shown applica- spectrum of applications such as energy, electronics, and tion of Fe3O4 and g-Fe2O3 nanoparticles on heavy metals personal care products, nanoparticles have been released to removal from contaminated water (Hu et al., 2005a,b; Hu et al., the environment, heightening concern about the safety and 2006; Xu et al., 2012). In addition to the great removal toxicity of nanoparticles (Borm et al., 2006; Brar et al., 2010; water research 47 (2013) 2613e2632 2615

Holsapple et al., 2005; Moore, 2006; Tsuji et al., 2006). Although nanoparticles occur in nature, such as those originating from volcanoes and combustion, artiﬁcially produced and released engineered nanoparticles have been of a comparatively tremendous amount (Hendren et al., 2011; Posner, 2009), threatening natural environments and wastewater treatment systems (Brar et al., 2010). Considering the direct applications of these magnetic nanoparticles in the treatment technologies, their release into the environment is inevitable, hence the assessment of their toxicity is of vital importance (Moore, 2006). To widely and wisely apply magnetic nanoparticles in subsurface and water treatment processes, several major concerns require further exploration. In this article, inﬂuencing factors and mechanisms of contaminant removal by magnetic nanoparticles are reviewed, since their removal performance and associated factors are the major considerations. To reduce the treatment Fig. 1 e Schematic model of magnetic nanoparticles (nZVI, cost, the feasibility of reuse and recovery of magnetic nano- Fe3O4 and g-Fe2O3). Zero-valent iron in the core mainly particles are also discussed. In addition, concerns such as provides the reducing power for reactions with their aggregation affecting capacity and reactivity as well as contaminants. The oxide shell provides sites for sorption. their toxicity, are also addressed. Adsorption is also occurred on the iron oxides (Fe3O4 and

g-Fe2O3) surface, while Fe3O4 possess reducing power.

2. Removal of contaminants date, nZVI is usually produced through reductive precipitation

The most popular magnetic nanoparticles are iron-based of FeCl3 with NaBH4, or reduction of goethite and hematite e nanoparticles, namely nZVI, Fe3O4 and g-Fe2O3. These nanoparticles with H2 at high temperatures (200 600 C). Other particles are iron-based, but possess different chemical methods were mentioned by researchers (Crane and Scott, properties originating from the oxidation states of iron. Their 2012). Preparation methods can greatly affect the removal capability and reactivity for contaminant removal are reactivity because of differences in iron phase, particle size different. Yet, the removal performance can be inﬂuenced by and shape (Liu et al., 2005; Nurmi et al., 2005). These studies various conditions, depending on the removal mechanisms demonstrated that the reactivity of nZVI prepared by reduc-

(Fig. 1). Knowing the removal mechanisms of these magnetic tive precipitation of FeCl3 with NaBH4 was higher because of nanoparticles can justify the applicability of them in envi- its smaller particle size and larger surface area. Higher iron ronmental applications. content was also reported, resulting in rapid degradation of pollutants (Liu et al., 2005; Nurmi et al., 2005). However, the 2.1. Contaminants removal by nZVI high reactivity of nZVI is a possible drawback for in-situ applications. It is because before reaching target pollutants, A number of laboratory studies and site application of nZVI reactive nZVI may react or be oxidized in water with dissolved have shown that it is an effective remediation technology. air, resulting in low longevity. When oxygen is present, nZVI is þ þ Since iron is a strong reducing agent, the strong reducing easily oxidized to Fe2 and/or Fe3 ions. The conversion of þ þ property of nZVI brings about a degradation of wide range of Fe2 to Fe3 is dominant under acidic and oxygenated envi- organic and inorganic pollutants. In particular, chlorinated ronments. The oxidation of nZVI in the presence of water can solvents, commonly found contaminants, can be degraded also result in the production of hydrogen. Therefore, providing through dechlorination to less harmful substances. The surface coatings like a thin layer of Fe3O4 (Liu et al., 2005), reductive degradation rate increases dramatically compared silica (Tang et al., 2006) or polymers (Wilson et al., 2004) could to the micro-sized counterparts (Wang and Zhang, 1997). alleviate this problem by reducing contact with oxygen, Numerous studies even showed that some persistence con- thereby retaining the reactivity of nZVI. Addition of catalytic taminants, such as polycyclic aromatic hydrocarbons (PAHs) metals (e.g., Pd, Pt, Ni) was also suggested for stabilizing nZVI and pesticides, can be effectively degraded with highly reac- (Gunawardana et al., 2011). For in-situ remediation, the nZVI tive nZVI (Chang and Kang, 2009; Li et al., 2006a,b). In addition, slurry was prepared under a protected inert atmosphere. The surface sorption and co-precipitation of contaminants, espe- water for slurry preparation was also purged with inert gas, cially heavy metals, also occur due to the formation of an iron usually nitrogen, before use (Elliott and Zhang, 2001). oxides/hydroxides shell when nZVI contacts with air or water.

This has been reported elsewhere and Cr(VI) is a widely- 2.2. Contaminants removal by Fe3O4 and g-Fe2O3 studied example (Fang et al., 2011; Giasuddin et al., 2007; nanoparticles Scott et al., 2011; Zhang, 2003). Previous studies demonstrated that Cr(VI) can be reduced by nZVI, forming precipitates with For Fe3O4 nanoparticle, both physical and chemical adsorp- corrosion products. Furthermore, there are variations in nZVI tions of heavy metal were reported (Hu et al., 2004). In the properties with different synthetic processes and coating. To study of the removal of Cr(VI) with Fe3O4 nanoparticles (Hu 2616 water research 47 (2013) 2613e2632

et al., 2004), it was found that the crystalline structure of interaction compared with chemical adsorption, environ-

FeCr2O4 on the surface of the nanoparticles was due to the mental conditions, especially pH values, dramatically affect reduction of Cr(VI) to Cr(III), and the subsequent surface pre- the removal performance. A charged nanoparticle surface is cipitation of Cr(III) onto the magnetic nanoparticles (Fig. 2). preferred for the removal of charged contaminants. Ion ex- This was also evidenced by the signiﬁcantly low desorption change was also proposed to elucidate the removal mecha- at high pH, indicative of chemical adsorption, while the ability nism. Hu et al. (2005a,b) demonstrated that Cr(VI) was also of desorption was attributed to physical adsorption. However, removed when the solution pH was higher than the pHZPC of the major contaminant removal mechanism of g-Fe2O3 g-Fe2O3 nanoparticles. The negative charges on hydroxylated nanoparticles is physical adsorption, without chemical iron oxide surface can exchange with Cr(VI) for adsorption. adsorption like Fe3O4 nanoparticles. The removal mechanism Although the pollutant removal is based on the mecha- was further revealed with spectroscopic studies, such as X-ray nisms discussed, environmental conditions that may alter photoelectron spectroscopy (XPS) and X-ray diffraction (XRD). magnetic nanoparticles performance include background

The crystallite structure of g-Fe2O3 nanoparticles did not ions, humic substances, and pH. The aquatic chemistry and change after the pollutants were removed, indicating that the groundwater composition vary from site to site. The strategic removal mechanism did not involve chemical reactions (Hu deployment of magnetic nanoparticles must consider various et al., 2005a,b). The pollutant removal by g-Fe2O3 nano- operational parameters. When magnetic nanoparticles are particles has been recognized to be resulted from electrostatic applied to wastewater treatment, high ionic strength and interactions. Oxygen atoms on the surface of iron oxides extreme pH are usually concerned. The variables of the

(Fe3O4 and g-Fe2O3) can be polarized under various pH values. properties of magnetic nanoparticles are also discussed Particularly, when the pH value is below the zero point of below. charge (pHZPC), the surface of the iron oxides possesses positive charges, attracting negatively charged pollutants (e.g., 2.3. Effects of environmental conditions on contaminant Cr(VI) and As(V)) (Chowdhury and Yanful, 2010; Hu et al., removal 2007b; Yean et al., 2005). It is evident that the removal performance of Fe3O4 and g-Fe2O3 nanoparticles was highly pH In real engineering applications, magnetic nanoparticles face dependent (Hu et al., 2004, 2007b; Yang et al., 2010; Yantasee a complex environment, teeming with a wide spectrum of et al., 2007). Since electrostatic attraction is a weak dissolved organic and inorganic compounds. Since electrostatic interaction has been proven to be one of the major removal mechanisms of magnetic nanoparticles, studies to date have usually taken background electrolytes into account for determination of removal performance (Chowdhury and Yanful, 2010; Hu et al., 2004, 2005a,b; Yang et al., 2010). These researchers reported that the background electrolytes insignificantly affected the removal performance, when the affinity of pollutants to the nanoparticles was higher than that of background electrolytes. For example, chloride and nitrate (100 mg/L) did not affect Cr(VI) removal by maghemite nanoparticles (Hu et al., 2005a,b); the background electrolytes in groundwater did not significantly affect As(V) removal by magnetite and maghemite nanoparticles (Chowdhury and Yanful, 2010). However, some researchers found that particular ions competed with target pollutants. One of the widely studied heavy metals, arsenic, is a good example. Although As(V) exists as anions in a normal aquatic environment, some common anions, such as sulphate and chloride, showed little effect on the removal of As(V) (Biterna et al., 2007; Chowdhury and Yanful, 2010; Sun et al., 2006). Competition of phosphate was clearly demonstrated in previous studies (Chowdhury and Yanful, 2010; Dong et al., 2012), which was probably due to the similar molecular structure and properties under the same group in the periodic table. Other researchers also found that natural organic matters (NOM), like humic acid, influenced removal performance, causing lower capacity and slower kinetics (Chen et al., 2011; Giasuddin et al., 2007; Liu et al., 2008), due to the occupancy of sorption sites by humic acid, and the formation of the disor- dered structure of the humic acid layer on the surface of e Fig. 2 XPS (a) and XRD (b) images of Fe3O4 nanoparticles nanoparticles. On the other hand, an enhancement of As(V) after Cr(VI) adsorption, indicative of chemisorption and removal was reported with the addition of Zn(II). In this case, a incorporation of Cr onto Fe3O4 (Hu et al., 2004). ternary surface complex formation was proposed to be the water research 47 (2013) 2613e2632 2617

mechanism (Yang et al., 2010). More studies are still required et al., 2006a,b). The applicability of smaller particles related to reveal the whole picture. to possibility of aggregation of magnetic nanoparticles is dis- Even though the pH value of the natural environment is cussed in another section. considerably steady, pH values of industrial wastewater alter a Considering the fact that the removal capacity and reac- lot. Since pH value dramatically affects the reduction of nZVI and tivity of magnetic nanoparticles is highly surface area adsorption performance of Fe3O4 and g-Fe2O3 nanoparticles, dependent, an alternative method for providing larger surface various approaches have been applied to magnetic nano- area is engineering a porous structure, such as activated car- particles to alleviate these influences. Coating with organic bon (Jiao et al., 2006). It was demonstrated by Wang and Lo surfactants or polymers is one of the methods for changing the (2009) that mesoporous g-Fe2O3 particles with around surface properties of magnetic nanoparticles (Ge et al., 2012; Hao 200 nm were synthesized and applied for Cr(VI) removal. The et al., 2010; Hu et al., 2011; Huang and Chen, 2009). The removal surface area of mesoporous g-Fe2O3 particles, and the result- mechanism still remains electrostatic interaction regarding the ing removal capacity and reactivity, was comparable to that of surface modifications as discussed in the section below. On the g-Fe2O3 nanoparticles (10 nm). But its large particle size contrary, Hu et al. (2006) suggested another way to make use of showed a greater potential for magnetic separation than g- the surface property of magnetic nanoparticles, moving from Fe2O3 nanoparticles. However, the synthesis of mesoporous limitation to opportunity. In industrial wastewater, various structure was much more complicated, and the improvement heavy metals usually co-exist and make the composition more on the removal capacity was still limited. complicated than synthetic solutions in laboratory. An effective Studies to date have mostly focused on the removal perfor- treatment with magnetic nanoparticles was experimented by mance of magnetic nanoparticles, and impressive percentage changing the pH values, so that the surface charge of the mag- results (e.g., 98% removal) have usually been reported. However, netic nanoparticles was manipulated for adsorption anions (i.e., more attention should be paid to the experimental conditions for Cr(VI)) and cations (i.e., Cu(II) and Ni(II)) selectively with specific reflecting the real situation. The removal performance may be pH values. The optimal pH for selective removal of Cr, Cu, and Ni overestimated if just focusing on reporting percentage (Gupta was determined to be 2.5, 6.5, and 8.5, respectively. Thus, these et al., 2012; Hao et al., 2010). The experimental conditions useful heavy metals can be separated and recovered by a simple require more thorough consideration to reflect the actual situ- process with magnetic nanoparticles by alternating pH values ation precisely. Parameters, such as dosage of nanoparticles, (Hu et al., 2006). concentration of pollutants or other electrolytes, should be carefully decided. For example, a competition effect of other 2.4. Effects of surface properties of magnetic contaminants may be studied with a corresponding equivalent nanoparticles on contaminant removal concentration of the target pollutant. This is also related to the mechanism of removal and capacity of the nanoparticles. If the The large contaminants removal capacity and fast reaction applied nanoparticles offer a removal capacity that is far beyond rate of the magnetic nanoparticles are the major advantages. the saturation limit for the target pollutants, the competition The total surface area of particles with the same mass in- effect could not be concluded. creases tremendously (can up to a thousand times), when the As mentioned above, different mechanisms are involved in particle size decreases to nano-scale (Tratnyek and Johnson, the contaminant removal by different magnetic nano- 2006). Due to the high surface-area-to-volume ratio, thus in- particles. The removal performance is considerably related to crease of active sites for the reaction, the mass required for the surface properties of the magnetic nanoparticles. In gen- treatment processes can be less than the case using the eral, contaminants can be removed by g-Fe2O3 and Fe3O4 micron-sized counterparts. Various studies showed that the nanoparticles via physical adsorption, so the desorption of removal capacity and reactivity of nanoparticles are highly contaminants and regeneration of nanoparticles are feasible. size dependent (Nurmi et al., 2005; Rivero-Huguet and However, relatively irreversible chemical adsorption for Fe3O4 Marshall, 2009; Yean et al., 2005). Shen et al. (2009) reported nanoparticles, and chemical reduction and coprecipitation for that the removal capacity of Fe3O4 nanoparticles (8 nm) was nZVI were also reported. The recent findings on contaminant about seven times higher than that of coarse-grained coun- removal are summarized in Table 1. terparts (50 mm). The reactivity of ZVI was found to be 50e90 times higher when the particle size was reduced from around 500 to 100 nm (Lin et al., 2008). Although the capacity increases 3. Desorption of contaminants with decreasing particle size, some researchers reported that the removal capacity normalized by surface area is not much When considering the applicability of magnetic nanoparticles different when the particle size changes (Tratnyek and for treatment technologies, another major consideration is Johnson, 2006; Yean et al., 2005). This is because all physical the reusability of magnetic nanoparticles. To maintain reac- or chemical reactions occur at the liquidesolid interface. To tivity, physical and chemical properties of the nanoparticle increase the surface area, synthesizing smaller particles products, the synthesis and manufacturing process of nano- seems to be a way to produce an effective treatment tool. particles require meticulous control of conditions. The treat- Indeed, despite the large capacity and high reactivity origi- ment cost of applying nanoparticles is relatively high, nating from the small particle size, it has been found that the compared with traditional treatments. For instance, the price smaller the particles are, the higher the tendency of aggre- of 1 kg of g-Fe2O3 nanoparticles is ranging from USD 180 to 380, gation stemming from a high surface free energy, which re- depending on the particle size, purity and methods of syn- duces the removal capacity and reactivity (Hao et al., 2010; Li thesis (MKnano, 2012; NANOSHEL, 2012; SkySpring 2618 Table 1 e Magnetic nanoparticles for contaminant removal. a b c 2 d e MNPs D (nm) SA (m /g) pHZPC Surface coating Target C Key findings Ref. contaminants nZVI 10e90 25 e Amphiphilic TCE 1.5e3 g/L 89% removal of 30 mg/L TCE; Krajangpan polysiloxane TCE degradation rate with et al., 2012 graft copolymer APGC-coated nZVI was (APGC) comparable to bare nZVI; Chemical reactivity of APGC-coated nZVI remained for 6 months nZVI w50 ee e TCE 1 g/L The presence of Suwanneee Chen et al., 2011 River humic acid reduced the reactivity towards TCE and mitigated toxicity of nZVI nZVI 50e100 33.5 4.2 ee Cu(II), Pb(II), 2.5 g/L Cu(II) enhanced the TCE Lien et al., 2007

As(V), dechlorination; 2613e (2013) 47 research water Cr(VI), TCE Cr(VI) decreased the TCE dechlorination rate w nZVI 100 8.1 0.1 Iron oxides NO3 1.42 g/L Iron oxides coating protected Sohn et al., 2006 the inner ZVI from further corrosion and thus maintained reactivity nZVI with 20e40 35 e Iron oxides Cr(VI) 0.1e0.6 g/L 99.9% removal of 50 mg/L Cr(VI) Fang et al., 2011 Ni (0.011%) at pH 4.82 with 0.6 g/L nZVI; and Zn (0.002%) Maximum removal capacity ¼ 182 2 mg/g; The presence of Ni and Zn improved removal efﬁciency nZVI 20e100 14.8 ee U(VI) 0.25 g/L nZVI removed >98% of U Crane et al., 2011 e ee < Fe3O4 20 50 52.5 to 10 mg/L, but Fe3O4 failed 2632 to achieve >20% U removal; U re-release was observed in solution treated with nZVI due to the presence of ligands (carbonate) f Fe3O4 6e10 4.5 ; Succinic acid (SA); Cr(III), Co(II), 1.25 g/L Metal ions were captured Singh et al., 2011 4.7g; Ethylenediamine (EDA); Ni(II), Cu(II), by forming chelate complexes veh 2,3-dimercaptosuccinic Cd(II), Pb(II), or ion exchange process or acid (DMSA) As(III) electrostatic interaction, depending on the surface functionality; All metal ions showed 80e85% of desorption ratio using 0.1 M HCl

Fe3O4 w5 178.48 e Ascorbic acid As(V), As(III) 60 mg/L Maximum removal Feng et al., 2012 capacity ¼ 16.56 mg/g for As(V); 46.06 mg/g for As(III) at pH 7 and 300 K Fe3O4 w10 62; 6; Humic acid (HA) Hg(II), Pb(II), 100 mg/L HA coated Fe3O4 was able to Liu et al., 2008 64 (with HA) 2.3 (with HA) Cd(II), Cu(II) remove >99% of Hg(II) and Pb(II), and >95% of Cu(II) and Cd(II) in natural and tap water with 1 mg/L of metal ions at wpH 7; 2þ 3 The presence of Ca and PO4 had no effect on the sorption of heavy metals

Fe3O4 10 198 8.3 e Cr(VI) 5 g/L Cr(VI) removal was governed by Hu et al., 2004 physico-chemical adsorption; The adsorption process was pH and temperature dependent

Fe3O4 and g-Fe2O3 20e40 49 ee As(V), As(III), 0.4 g/L Maximum removal Chowdhury and Cr(VI) capacity ¼ 3.71 mg/g for As(V); Yanful, 2010 3.69 mg/g for As(III) at pH 2; 2.4 mg/g for Cr(VI) at pH 2;

The presence of phosphate reduced 2613e (2013) 47 research water the removal of As and Cr g-Fe2O3 10 198 6.3 e Cr(VI), Cu(II), 5 g/L Metals can be selectively removed Hu et al., 2006 Ni(II) from wastewater depending on pH;

Metal removal capacity of g-Fe2O3 can be regenerated by 0.05 M HCl or 0.01 M NaOH g-Fe2O3 10 178 6.3 e Cr(VI) 5 g/L 19.2 mg/g for Cr(VI) at pH 2e3 and 298 K; Hu et al., 2005a Competition from common coexisting þ þ þ þ ions such as Na ,Ca2 ,Mg2 ,Cu2 , 2þ Ni ,NO3 , and Cl was ignorable g-Fe2O3 15 120e180 8.5 d-FeOOH Cr(VI) 5 g/L 25.8 mg/g for Cr(VI), which is higher Hu et al., 2007b than that of pure g-Fe2O3 (19.4 mg/g); The nanoparticles can be regenerated by 0.01 M NaOH 2632 a MNPs ¼ Magnetic nanoparticles. b D ¼ particles size. cSA¼ surface area. dC¼ Particle concentration. e Ref. ¼ Reference. fFe3O4 nanoparticles coated with SA. gFe3O4 nanoparticles coated with EDA. hFe3O4 nanoparticles coated with DMSA possessing negatively charged in the studied pH range. 2619 2620 water research 47 (2013) 2613e2632

60 pH=7 pH=9 50 pH=5

40 phosphate=0.5 mg/L (as P) phosphate=1.0 mg/L (as P) 30 phosphate=3.0 mg/L (as P)

10 Relative desorbedAs (%)

Fraction of desorbed As (%) of desorbed Fraction 0 51020 51020 51020 Initial As(V) concentration (mg/L) Initial As(V) concentration (mg/L) Initial As(V) concentration (mg/L)

Fig. 3 e Fraction of desorbed As from As(V)-sorbed-nZVI as induced by phosphate of various concentrations (Dong et al., 2012).

Nanomaterials, 2012). Reuse of nanoparticles would substan- Another approach to endow with the ability of regeneration tially reduce the treatment cost. Regeneration is a common and maintain the magnetism of nanoparticles is to oxidize Fe3O4 practice to regain the removal capacity of adsorbents, whilst to g-Fe2O3 delicately under well controlled conditions. Since the feasibility of regeneration of magnetic nanoparticles is closely removal mechanism by g-Fe2O3 nanoparticles has been deter- related to their removal mechanism. mined to be electrostatic interactions (Hu et al., 2005a,b; Hu

et al., 2006)andg-Fe2O3 is a chemically stable form of iron oxide, the adsorbed pollutants can be desorbed by changing the 3.1. Desorption from Fe O and g-Fe O nanoparticles 3 4 2 3 pH, and thus the surface charges. The most important param-

eter to be determined is the pHZPC of the g-Fe2O3 nanoparticles. Although the pollutant removal mechanism of Fe O nano- 3 4 Numerous studies (Afkhami and Moosavi, 2010; Hao et al., 2010; particles involves physical and chemical adsorption in which Hu et al., 2005a,b; Hu et al., 2006) supported that simple inorganic chemical bonding formation limits the regeneration of nano- acid or alkaline can be applied for effective regeneration of g- particles, various approaches have been adopted for devel- Fe2O3 nanoparticles, and for surface modified g-Fe2O3 nano- oping reusable magnetic nanoparticles, for instance, surface particles (Beéetal.,2011). This process not only can regenerate coating with organic functionalized surfactants (Badruddoza the exhausted magnetic nanoparticles and restore the removal et al., 2011; Bhaumik et al., 2011), humic acid (Liu et al., capacity, but also recover valuable components, like heavy 2008), and silicate (Fan et al., 2012; Hakami et al., 2012). metals, useful in many industrial processes, from the adsorbed These coatings prevent the magnetic core, Fe O nano- 3 4 phase. Hu et al. (2006) demonstrated that heavy metals can be particles, from chemical adsorption and redox reaction to separated and recovered selectivity from a complex solution form non-magnetic minerals (e.g., a-Fe O ), thus maintaining 2 3 with a careful pH adjustment. magnetism. In addition, the surface coatings usually possess Although the ability of g-Fe2O3 nanoparticles was proven to specialized functional groups for adsorption of target pollut- be regenerated and reused for successive treatment cycles, ants. Taking Hg removal as an example, Hakami et al. (2012) the stability of the magnetic nanoparticles has to be taken into prepared Fe O nanoparticles functionalized with thiol 3 4 consideration (Ge et al., 2012; Liu et al., 2008; Yantasee et al., groups by adding (3-mercaptopropyl) trimethoxysilane on 2007). Acid have been suggested for regeneration in silica-coating. According to the Pearson’s hard-soft acids- numerous studies, while acid and alkaline can also enhance bases theory (Pearson, 1968), the sulfur atoms in thiol moieties the dissolution of magnetic nanoparticles, especially in HCl served as ligands to bind with soft metal cations like Hg. Due and HNO3, hence diminishing the reusability of magnetic to the increase of binding sites provided by the surface nanoparticles. One should note that desorption of contami- coating, the removal capacity and affinity of the magnetic nants with strong acid or alkaline may lead to nanoparticle nanoparticles were massively improved. This was also sup- dissolution (Yantasee et al., 2007). ported by findings from another research group (Yantasee et al., 2007). The reported approach of desorption was also different from simply using acid or alkaline, particularly 3.2. Regeneration of nZVI? considering the property of ligands, and interaction between ligands and pollutants to promote the desorption process. Although regenerating nanoparticles through the desorption of Eventually, adopting the hard-soft acids-bases theory, thio- pollutants is one of the crucial considerations of practicability, urea was added to facilitate desorption of Hg because of the nZVI can hardly be regenerated because of its irreversible presence of sulfur atoms. Moreover, amino moieties were re- reductive property. Pollutants such as Cr(VI) are reduced, co- ported as having a novel capability for sorption of metal cat- precipitated or sorbed on the nZVI, specifically the iron oxide ions and anions under various pH values, derived from layer, indicating that desorption of the pollutants may require positive charges after protonation or coordination with lone disruption of the chemical structure (Fang et al., 2011; Li et al., pair of electrons of nitrogen atoms without protonation (Hu 2006a,b; Scott et al., 2011). This depends on the stability and et al., 2011; Huang and Chen, 2009). This property has impor- solubility of the compounds, and the presence of ligands. Dong tant implications for developing magnetic nanoparticles with et al. (2012) found that the adsorbed As(V) on nZVI was further an ability for regeneration by alternating pH. sorbed onto the crystalline structure of iron oxyhydroxides water research 47 (2013) 2613e2632 2621

with aging time, and thus became more strongly bonded. properties of particles alter when particle size reaches nano- However, Sohn et al. (2006) suggested that nZVI can be reused scale (Sundaresan and Rao, 2009). In particular, the magnetic several times, and the removal performance maintained. The property of Fe3O4 and g-Fe2O3 changed from ferromagnetic to nZVI particles were used for six cycles of nitrate reduction with superparamagnetic (Chatterjee et al., 2003). This property of- successive complete removal. During the consecutive re- fers an encouraging option, satisfying requirements of high ductions, transformation of nZVI particles occurred, and the accessibility as well as reusability. Most water or wastewater size of the iron core reduced, indicating a decreasing lifespan of treatment systems require a settling, filtration or centrifuge the nZVI particles. Actually, the reactivity of nZVI may not be process to separate solids like sludge. However, magnetic exhausted after reaction, but passivated by the iron oxide layer nanoparticles can be separated and recovered with an external formed (Liu et al., 2005). The iron oxide layer blocks electron magnetic field due to the intrinsic magnetic characteristic of transfer from the iron core. The reactivity can even be exploited the nanoparticles, aiding in prominent nanoparticles recovery and enhanced by acid-washed to disrupt the iron oxide without a filtration process. Magnetic separation is a widely passivation layer (Sun et al., 2011). adopted method for collecting or separating magnetic substances from flowing streams (Yavuz et al., 2009). 3.3. Desorption of contaminants in the environment High-gradient magnetic separation (HGMS) is a widely used technique for magnetic separation process (de Vicente et al., Using magnetic nanoparticles for contaminant removal was 2010; Hoffmann and Franzreb, 2004a, 2004b; Svoboda, 2001). proven to be a highly efficient technology, but most of the A stack of magnetically susceptible metal wires is installed results were based on conditions with simple synthetic solu- inside an electromagnetic system in an HGMS. To generate tions, usually containing only one target pollutant. Desorption large field gradients around the wires, a magnetic field from the is desirable for controlled applications like wastewater treat- electromagnetic system is applied across the wires, distrib- ment. But this can lead to a disaster of pollutant migration and uting the magnetic field, and attracting magnetic particles to- spreading out if desorption occurs when the spent magnetic ward the surfaces of wires. The generation of great magnetic nanoparticles are released into the environment. Studies field gradients is the one of crucial factors for particle collec- showed that uranium can be re-oxidized (Dickinson and Scott, tion. The size and magnetic properties of particles, and the 2010) or chemically complexed with ligands like carbonate area of magnetized surfaces also play the important roles. For (Crane et al., 2011), resulting in the increase of solubility and effective collection of magnetic particles by magnetic separa- re-release of uranium. Desorption of arsenic was also reported tion, the magnetic force attracting particles must dominate the (Dong et al., 2012; Jackson and Miller, 2000; Peryea, 1991; Yin gravitational, inertial, fluid drag and diffusion forces when the et al., 2012) offering the possibility that phosphate and hy- particle suspension flows through the separation unit. droxide anions had the greatest competition effects for the sorption sites (Fig. 3). Indeed, Nordstrom (2002) pointed out 4.1. Forces acting on magnetic nanoparticles that high concentrations of phosphate, bicarbonate, silicate, and/or organic matter in groundwater can enhance the solu- Generally, magnetic separation is caused by the feature of bility of arsenic. Leaching and remobilizing of chromium by magnetic fields exerting a force on matter with magnetic low pH condition and presence of competition anions like properties. The involved magnetic force, Fm, can be expressed phosphate (Jing et al., 2006; Mandiwana, 2008) were also as demonstrated. And it was reported that humic acid exerted an ¼ influence on the removal of heavy metals because of an Fm m0VpMpDH (1) enhancement in solubility and mobility of heavy metals by m where 0 denotes the permeability constant of the vacuum, Vp complexation (Dries et al., 2005; Liu and Lo, 2011; Mak et al., is the particle volume, Mp is the particle magnetization and DH 2011). Since heavy metals can only be immobilized or trans- is the gradient of magnetic field strength at the position of the formed to less harmful states, but not degraded like organic particle. The particle magnetization may be expressed by the contaminants, the migration or remobilization of heavy magnetic volume susceptibility c and the magnetic field metals is intractable, crucially depending on the environ- strength H, where the volume susceptibility is a constant for mental conditions. The mechanism of heavy metal re-release diamagnetic and paramagnetic substances, and a function was attributed to complexation or competition of other con- among others of particle shape and size as well as field stituents in natural waters. Site characteristics should not be strength for the ferromagnetic or ferrimagnetic substances. overlooked, especially the pH and the high concentration of particular dissolved ions and NOM. As a result, the magnetic Mp ¼ cH (2) nanoparticles with different coatings and functionalizations, Other competing forces in the magnetic separation process showing various reactivity and surface properties, should be include gravitational force, F , tested under site-specific conditions before application. g ¼ r r Fg p g Vpg (3)

4. Recovery of magnetic nanoparticles where rp is spherical particle density, rg and g are density of ﬂuid and acceleration due to gravity; hydrodynamic drag

One of the most fascinating characteristics of magnetic force, Fd, can be calculated with Stokes’ Law, nanoparticles, showing advantage over other nanoparticles, is À Á ¼ h their magnetism. Abundant evidence showed that magnetic Fd 6p b vf vp (4) 2622 water research 47 (2013) 2613e2632

h where is the dynamic viscosity of the fluid, b is a constant suggested that the optimal particle size of Fe3O4 for HGMS is that depends on the properties of the fluid and the dimensions around 12 nm with a superparamagnetic property. Crane and of the particle, and nf and np are velocities of the fluid and Scott (2012) pointed out that particle size of nZVI larger than particle respectively. 20 nm is more practical due to the exceedingly high reactivity Ample of results showed that magnetic nanoparticles can of tiny particles. be effectively separated from the aqueous phase, even with a In order to economically recover the magnetic nano- hand-held magnet (Bhaumik et al., 2011; Do et al., 2011; Fan particles from water and wastewater treatment, another op- et al., 2012; Feng et al., 2012; Li et al., 2010a,b; Liu et al., 2010; tion can be the adoption of a greater magnetic field. Usually, Shen et al., 2011; Shin et al., 2011; Wang et al., 2010a,b; Zhang the magnetic source in magnetic separators like HGMS is and Kong, 2011). However, no industrial application of mag- electromagnets, which consist of solenoids of electrical con- netic separation for magnetic nanoparticles has yet been re- ducting wires generating a magnetic field during electric cur- ported, although there have been some for microparticles. rent passage. However, this magnetic field provided by Although the magnetic properties of the particles are un- electromagnets is limited to magnetic microparticle separa- doubted with evidence of vibrating sample magnetometer tion (Ohara et al., 2001). A stronger magnetic field is required (VSM) measurements, those photographic results shown in for magnetic nanoparticles; superconducting magnets are literature, magnetic separation within the vials or beakers by a required. The coil conductor of a superconducting magnet is magnet, may be misleading. A vial or beaker is not a large operated under cryogenic temperatures in the super- container, usually only a few centimeters in diameter. The conducting state. Since there is very little energy lost due to magnetic field provided by a hand-held magnet would be resistance, a much greater magnetic field is produced when a strong enough to provide sufficient magnetic force on the large current passes through (Iacob et al., 2002). On the other magnetic nanoparticles in the vial. But magnetic field drops hand, the concern is the capital and operation cost of the substantially with distance away from the source, following superconducting magnet which is related to the design and an inverse cube law. On the other hand, when the particle size materials (Iacob et al., 2002; Iwasa, 2009; Li et al., 2007). is reduced to nano-scale, a much greater magnetic field is required to provide sufficient attraction to compete with other 4.3. Questions in magnetic nanoparticles recovery forces, such as drag, buoyancy, and even Brownian motion (Tratnyek and Johnson, 2006). From the equations mentioned With the conceptual possibility of magnetic nanoparticles above, the magnetic force depends on the particle size. Since recovery using magnetic separation, a reduction of removal there is a limited magnetic field gradient for distant particles, capacity and reusability of magnetic nanoparticles raises a even a few centimeters more, the magnetic nanoparticles question because of aggregation. Although numerous evi- cannot be attracted, but stay suspended in solution, without dence have shown the feasibility of magnetic separation and taking into consideration of velocity and drag force from the reuse of nanoparticles, magnetic nanoparticles aggregation flowing stream. under magnetic field attraction, resulting from collision among nanoparticles, is still in question (Mandel and Hutter, 4.2. Better recovery of magnetic nanoparticles 2012). Quick magnetic separation with a hand-held magnet also implied that aggregate formed, while the aggre- Particle size is one of the variables which can be manipulated gation is suggested to be reversible (Yantasee et al., 2007; for better recovery, but increase in particle size leads to Yavuz et al., 2006), hence the magnetic nanoparticles are decrease in reactivity and removal capacity. Moreover, the recoverable. Nevertheless, more in-depth study to reveal magnetic separation efficiency is not just influenced by the nanoparticle interactions under magnetic field is necessary. particle size (Chatterjee et al., 2003; Papaefthymiou, 2009; Magnetic nanoparticles may be held on the magnetic surface Sundaresan and Rao, 2009), but also the synthesis methods of strongly, and hardly recovered (Yavuz et al., 2006). Dispersion magnetic nanoparticles (Badruddoza et al., 2011; Hakami of the magnetic nanoparticles to let as much surface area of et al., 2012), and fluid properties (Hayashi et al., 2011). To the nanoparticle as possible for reaction is still essential, strike a balance between effective recovery and high removal although the aggregation is expected to be reversible. performance, an optimum particle size, considering the Considering the high surface free energy of the nanoparticles, magnetic properties of different nanoparticles and fluid re-dispersion such as by sonication (Huber, 2005; Wassel et al., properties, is required to be studied. Yavuz et al. (2006) 2007) is recommended before application. Surface coating,

Fig. 4 e Schematic representation of electrostatic, steric and electrosteric stabilized magnetic nanoparticles. water research 47 (2013) 2613e2632 2623

especially by steric and electrosteric stabilization, can prevent minimum aggregation. Extensive aggregation of nanoparticles aggregation of magnetic nanoparticles, discussed further in (i.e., hematite) was observed at high concentrations (>50 mg/ the section below. L) in a wide range of pH, especially near pH values of the pHZPC of nanoparticles (Baalousha, 2009). Under higher particle concentrations, formation of the stable sized agglomerates 5. Aggregation occurs rapidly, reaching a steady state. The size of the aggregate formed was suggested to be similar as force balance Nanoparticles with a high surface free energy tend to aggre- dominant the control of aggregate size, independent of par- gate, achieving a stabilized state. The smaller particles have ticle concentration (Phenrat et al., 2009a). higher tendency of aggregation due to the lower energy barriers (Petosa et al., 2010). Formation of aggregate decreases the 5.3. Forces governing aggregation surface area of the magnetic nanoparticles. This reduces the removal capacity and reactivity, thereby limiting the treat- In aquatic environments, aggregation of nanoparticles, e ment performance. Aggregation also undermines the effec- controlled by particle particle interactions, has been conven- e e e tiveness of magnetic nanoparticles during remediation tionally described by Derjaguin Landau Verwey Overbeek because of the loss of mobility. Several conditions leading to (DLVO) theory (Baalousha, 2009; Petosa et al., 2010; Phenrat the aggregation of magnetic nanoparticles are highlighted et al., 2009a; Saleh et al., 2008). The traditional DLVO theory including the particle size distribution, particle concentration, described colloidal stability considering the total interaction solution composition, surface chemistry, and certainly the energy on a particle with another particle. The major interac- magnetism of the nanoparticles (Hu et al., 2010; Petosa et al., tion energy can be estimated and calculated as the sum of van 2010; Phenrat et al., 2009a; Yin et al., 2012). der Waals and electrical double layer interactions. The theory explains rapid nanoparticle aggregation at pH values near pH , as well as a direction for improving stability with sur- 5.1. Particle size ZPC face modifications. The charges on the magnetic nanoparticles can be neutralized under certain pH environments, reaching Theoretically, compared to that of particles with the same pH values of pH . Hence, electrostatic repulsions among size, differential sized particles show a higher aggregation ZPC nanoparticles diminish leading to aggregation. On top of the rate, following the Eq. (5) (Petosa et al., 2010). Larger particles DLVO theory, steric and magnetic forces, regarded as non- have a higher attractive force, especially for magnetic nano- DLVO forces, also play a key role in magnetic nanoparticle paritcles (Phenrat et al., 2009a). There is an unbalanced force aggregation. These factors were discussed in detail with gov- among particles, so polydispersed nanoparticles have a erning equations (Petosa et al., 2010). greater tendency to aggregate due to differential sedimenta- Magnetic nanoparticles have an intrinsic permanent tion (Dickinson and Scott, 2010). Thus, polydispersed nano- magnetic dipole moment with a saturation magnetization particles are relatively less stable. (Ms), even in the absence of an applied magnetic field, which is À Á þ 2 related to the iron content. It was reported that Ms increased ¼ 2kBT ai aj kij h (5) with the iron content and particle size, following an empirical 3 0 aiaj relationship (Phenrat et al., 2008). In addition, since magnetic where kij is perikinetic aggregation rate constant between force is a long-range attractive interaction, compared with dissimilar-size particles, kB is Boltzman constant, T is absolute van der Waals and electrical double layer interactions, ag- h temperature, 0 is absolute viscosity of fluid, ai and aj are gregation may result from the unbalanced force due to the particle radii. According to the equation, the stability of domination of magnetic force, especially for nZVI (Petosa nanoparticles in aquatic environments is not solely depen- et al., 2010; Phenrat et al., 2009a). This was also evident by dent on particle properties, but also on fluid properties. The comparing to use of non-magnetic hematite nanoparticles influence of fluid properties can be observed from ferrofluids, with similar surface treatment, which showed a greater sta- which contains well-dispersed magnetic nanoparticles. There bility than nZVI (Phenrat et al., 2009a). is a high concentration of surfactants in ferrofluids, suffi- ciently coating on the nanoparticles, thus preventing aggre- 5.4. Stabilize magnetic nanoparticles gation. However, this may not be feasible in environmental applications because of dilution. Once the ferrofluid apply in Surface coating can significantly enhance the stability of the treatment processes, leading to inadequate stability from magnetic nanoparticles suspension. A number of methods diluted surfactants and probably aggregate. and chemicals for stabilization have been applied and studied for providing steric, electrostatic, or electrosteric stabilization 5.2. Particle concentration (Fig. 4). Some natural polyelectrolytes like humic acid and starch have been proven the ability of stabilization (Dickson Aggregation increases with an increase in concentration of et al., 2012; Kim et al., 2003; Mikhaylova et al., 2004; Xiong magnetic nanoparticles, resulting from more frequent colli- et al., 2007). There are numerous moieties on these marco- sion and particleeparticle interactions (Baalousha, 2009; molecules providing different functions. For example, the Maximova and Dahl, 2006). Previous research reported that a phenyl groups and carbon chains can provide steric repulsion low concentration of nanoparticles (30 mg/L) was mobile in a between magnetic nanoparticles. The functional groups porous medium (Phenrat et al., 2009a), indicative of a complexing and bonding onto the surface of iron/iron oxides 2624 water research 47 (2013) 2613e2632

nanoparticles were identified to be carboxylic acid (eCOOH), instead of thiol group (eSH) (Hakami et al., 2012; Sirk et al., 2009; Yantasee et al., 2007). These findings are useful for an engineering design of surface coating to provide specific functions and properties for magnetic nanoparticles. More- over, modifications can also be performed on some surface coating such as chitosan and silica (Chang and Chen, 2005; Geng et al., 2009a, 2009b; Wang et al., 2010a,b). Xanthate (Zhu et al., 2012), ethylenediamine (Hu et al., 2011), and thiourea (Zhou et al., 2009) were used to further modify the surface coating of chitosan to increase the adsorption ability and selectivity towards metal ions. In addition to these findings, some researchers have tried various functional polymers for synthesizing magnetic Fig. 5 e Schematic model of potential cell damage after nanoparticles with specific functions. Modifications with exposure to magnetic nanoparticles. Magnetic poly(acrylic acid) (Chen and Huang, 2004; Huang et al., 2006; nanoparticles adsorb onto the cell wall or cell membrane, Liao et al., 2004; Mahdavian and Mirrahimi, 2010) and car- subsequent internalization. The adsorbed magnetic boxymethyl cellulose (CMC) (He et al., 2010; Phenrat et al., nanoparticles limit the mobility, block membrane channel, D 2008; Wang et al., 2010a,b; Zhang et al., 2011a) have been or disrupt the membrane of bacteria. Fe2 , releasing from widely studied, showing a significant promotion of collide magnetic nanoparticles, reacts with hydrogen peroxide stability of magnetic nanoparticles. Block copolymer in through Fenton’s reaction, generating OH radical and another type of polyelectrolyte can be used to develop a multi- causing lipid/protein oxidation. functional architecture with different block copolymers. The surface properties of magnetic nanoparticles, such as hydrophobic/hydrophilic, surface charge, and even addition of surface modifications usually focuses on advancement in chelating/complexation moieties can be manipulated with stability and mobility of magnetic nanoparticles, rather than special design block copolymer architecture (Sirk et al., 2009). on reaction with contaminants. A thick layer of surface This modification not only maintains the magnetic nano- modifiers may limit the access to the surface of magnetic particles in a dispersed condition, but also reduces the contact nanoparticles where reactions occur. On the other hand, some of magnetic nanoparticles with bacteria. This may prevent studies reported that reaction rate was reduced due to the toxic effects on microorganisms. The toxicological effect is coating of humic acid (Chen et al., 2011; Liu et al., 2008), but discussed in another section. removal capacity was enhanced with increase of active sites Although a surface coating can assist the dispersion of contributed from surface modifications. Some active sites on magnetic nanoparticles, the coating may not be permanent. the magnetic nanoparticles could also be blocked during Surface modified magnetic nanoparticles have usually been surface coating. To comprehensively evaluate the surface prepared in a high concentration of surface modifiers (e.g., modified magnetic nanoparticles, the effect on both removal humic acid, polymers, surfactants). These surface modifiers performance including capacity and kinetics, as well as sta- adsorbed onto the surface of magnetic nanoparticles, some bility and mobility, should be intensively studied. anchoring tightly through complexation with iron oxide surface, because of the concentration gradient. However, the adsorption of surface modifiers may be reversible in the 6. Toxicity environment with diluted surface modifiers, extreme pH and ionic strength, or after reaction of nanoparticles. It was Nanoparticles surreptitiously enter the environment through found that humic acid can be desorbed from humic acid water, soil, and air during various human activities. However, coated magnetic nanoparticles (Liu et al., 2008), especially the application of nanoparticles for environmental treatment under low pH values and high ionic strength. The stability of deliberately injects or dumps engineered nanoparticles into magnetic nanoparticles can be influenced once the coating the soil or aquatic systems. This has resultantly attracted desorbed. In contrast, Kim et al. (2009) have reported the increasing concern from all stakeholders (Brar et al., 2010; stability and mobility of surface modified nZVI maintained Posner, 2009). The advantages of magnetic nanoparticles like for about 8 months, and the desorption of surface modifiers their small size, high reactivity and great capacity, could was not significant. Some efforts should be made on study- become potential lethal factors by inducing adverse cellular ing the stability of coatings, especially under extreme toxic and harmful effects, unusual in micron-sized counter- conditions. parts. Studies also illustrated that nanoparticles have the ability to enter organisms during ingestion or inhalation 5.5. Trade off between stability and reactivity (Holsapple et al., 2005), and can translocate within the body to various organs and tissues (Borm et al., 2006) where the To effectively apply magnetic nanoparticles in remediation nanoparticles have the possibility to exert the reactivity being and water treatments, it is necessary to avoid aggregation of toxicology effects. Although some studies have also addressed magnetic nanoparticles, yet maintain the advantages of rapid the toxicological effects of nanoparticles on animal cells reaction and high removal capacity. Nevertheless, research on (Iversen et al., 2011; Moore, 2006), plants and plant cells water research 47 (2013) 2613e2632 2625

(Navarro et al., 2008; Miralles et al., 2012), the toxicological penetrate cell membrane, leading to cell disruption due to the studies with magnetic nanoparticles on plants to date is still chemical interactions between the nZVI and cells (Auffan limited. In this section, the main focus is on the effects upon et al., 2008; Lee et al., 2008). The disruption of cell mem- bacteria, while the effects upon plants are briefly discussed. branes further resulted in leakage of the intracellular con- Inactivation of bacteria by magnetic nanoparticles has tents, cytoplasm, and elevated exposure of nZVI or other þ been observed, especially for nZVI, resulting from the inter- reactive species (e.g., Fe2 ), causing inactivation. This is action between nanoparticles and bacteria. Adsorption of probably due to reductive decomposition of cell membrane in magnetic nanoparticles on the bacteria membrane surface, which the proteins and polysaccharides maintain the integ- and the reactions internally in cytoplasm of bacteria were rity of the cell (Sevcu et al., 2011). The adsorbed nanoparticles reported to be the causes of bactericidal effect (Auffan et al., on the cell membrane may also block the cellular channels, or 2008; Lee et al., 2008; Tsuji et al., 2006). However, the mecha- cause structural changes of cell membrane, or limit the nism of toxicity is still unclear and biocompatibility varies mobility and nutrient uptake of bacteria, and finally leading to depending on numerous parameters, such as nanoparticle bacterial death (Xiu et al., 2010). size and shape, surface property, applied nanoparticle con- Another inactivation mechanism proposed has been centration, type of cell and nanomaterial. oxidative damage through Fenton reaction, regarding as oxidative stress. The major component of nZVI is iron, 6.1. Size and shape of nanoparticles regardless of the preparation methods and storage conditions. With oxidation in water, iron reacts according to the following Several studies indicated that when the size of particles was equations: reduced to nanoscale, bactericidal effects can be observed. 0 þ þ / 2þ þ The size of magnetic nanoparticles can be manipulated with 2Fe O2 2H2O 2Fe 4OH (6) synthesis methods and these provide varying performance in 0 þ þ þ/ 2þ þ Fe O2 2H Fe H2O2 (7) contaminant removal and aggregation, discussed above. Similar to the effect of aggregation, the smaller size of nano- Even without oxygen, iron can still be oxidized: particles was found to have a higher tendency to be adsorbed 0 2þ Fe þ 2H2O/Fe þ H2 þ 2OH (8) onto bacteria (Zhang et al., 2011b). Higher particle mobility and lower energy barriers in the interaction energy of small Ferrous ions generated following the above equations acti- size nanoparticles were attributed to fast adsorption kinetics vate Fenton reaction with the reactive oxygen species (ROS) and high in the adsorbed number of particles on the bacterial (e.g., OH and H2O2) and enhance the production of ROS, leading surface. Further, it was proven that adsorption of nano- to cellular injury and death (Sevcuetal.,2011). ROS are normally particles to a bacterial surface is a primary step for bacteri- produced during metabolism in cells as a by-product of aerobic cidal effects to be exhibited (Iversen et al., 2011; Simon- respiration. The validity of these proposed mechanisms was Deckers et al., 2009; Verma and Stellacci, 2010). The nano- supported by a number of experiments. The decrease of particles with the size of 20e50 nm can be effectively taken up bactericidal effects of oxidized nZVI and nZVI under aerobic by cells. This is also supported by the low toxicity of particles condition indicated that the key role of chemical reactivity of with a larger size, less associated with bacteria (Lee et al., nZVI (Lee et al., 2008; Li et al., 2010a,b). The similar inactivation þ 2008). Moreover, spherical particles showed higher cellular results of the presence of Fe2 illustrated the possible inacti- uptake rate and toxicity than rod-shape particles, despite the vation pathway of Fenton reaction (Lee et al., 2008). research focus being spherical magnetic nanoparticles. This is Other magnetic nanoparticles (Fe3O4 and g-Fe2O3) showed þ speculated to be because of the higher wrapping time much lower bactericidal effects. However, the release of Fe2 requirement of the cell membrane for elongated particles from Fe3O4 and g-Fe2O3 nanoparticles causing cytotoxicity (Nair et al., 2009; Simon-Deckers et al., 2009). However, some was reported (Auffan et al., 2008; Niu et al., 2011), despite the studies found that carbon nanotubes cause injury in mice fact that it is less harmful than nZVI due to their more stable during inhalation exposure (Lam et al., 2004; Poland et al., chemical state, particularly for g-Fe2O3. Based on the toxico- 2008). To evaluate the toxicity of magnetic nanoparticles, the logical results, iron oxides magnetic nanoparticles, or partially polydispersity of particle size and the possibility of aggrega- oxidized nZVI are preferred over fresh nZVI, regardless of the tion should be taken into account, since particle size is one of rapid reduction for contaminants. The bactericidal in- the crucial parameters. The toxic effects may be reduced if teractions of magnetic nanoparticles are illustrated in Fig. 5. aggregation occurs. In order to depress the toxic effects of magnetic nanoparticles, various surface coatings have been employed. This 6.2. Surface properties of magnetic nanoparticles can greatly reduce the contact of magnetic nanoparticles with bacteria. Similar to the enhancement in stability, surface As discussed in previous sections, surface properties of mag- coatings provide steric, electrostatic, or electrosteric barriers netic nanoparticles influence the removal and aggregate per- showing satisfactory results on elimination of bactericidal ef- formance. The effect on nanoparticleecell interactions is fects. A number of surfactants and polymers were applied to highlighted in this section. Magnetic nanoparticles possess a mitigate the bactericidal effect, such as poly(styrene sulfonate) great adsorption capacity and reactivity. The high reducing (PSS) (Rayavarapu et al., 2010), poly(aspartate) (PAP) (Phenrat potential of nZVI can readily reduce various organic contam- et al., 2009b), and NOM (Li et al., 2010a,b). Studies found that inants, similar to the components of cell membrane. Some anionic surfactants provide a better toxicity mitigation (Li et al., investigators reported that bare nZVI adsorbed onto or 2010a,b; Verma and Stellacci, 2010), but only Escherichia coli,a 2626 water research 47 (2013) 2613e2632

gram-negative bacterium, has been usually used as the model lower than the system with only bacteria. There was a lag bacteria (Chen et al., 2011; Li et al., 2010a,b). Extensive studies phase in the nZVI-bacteria system, suggesting that nZVI may on NOM coated magnetic nanoparticles have been conducted, be passivated over time, or the bacteria may require time to because NOM is ubiquitous in natural environments and can adjust and recover; however, insufficient data after the lag readily adsorb onto magnetic nanoparticles during environ- phase have been presented. Despite inclusive findings about mental applications. The toxicity of magnetic nanoparticles whether nZVI promote removal of contaminants, nZVI can was reduced even when the particles were not pretreated with provide H2 as an electron donor for bacterial reduction (An NOM (Chen et al., 2011). It is suggested that the mitigation was et al., 2009; Barnes et al., 2010a; Xiu et al., 2010), without sig- due to the electrosteric hindrance of NOM. NOM possesses a nificant bactericidal effects, such as that utilized by sulfate negative charge in the pH range of natural environments for reducing and methanogenic bacteria. To facilitate biological electrostatic repulsion, and provides abundant alkyl and aro- treatment, magnetic nanoparticles with surface coating can matics functional groups with steric barriers. also be adsorbed onto bacteria by offering the advantage of However, some other studies on interactions between magnetic separation (Li et al., 2009). The researchers pointed nanoparticles and animal cells showed that neutral charge out that oleate-modification provided hydrophobic in- polymers can provide better biocompatibility than charged teractions towards the bacterial cell wall, in addition to solely particles like with coating of biocompatible ligands (Liu et al., nanoparticle adsorption; therefore, the modified magnetic 2009; Verma and Stellacci, 2010), polyethylene glycol or poly- nanoparticles were difficult to be washed off. This demon- ethylene oxide. Since these coatings lowered protein adsorp- strates that a careful design of surface coating not only miti- tion and decrease cell recognition, the uptake rate of magnetic gates the toxicity of nanoparticles, but also combines the nanoparticles by cells was reduced. More than the molecular advantages for novel environmental applications. weight, functional groups, or the charge of surface coatings on magnetic nanoparticles, the spatial configuration of coated 6.5. Phytotoxicity of magnetic nanoparticles polymer also affected the interactions between cells (Hu et al., 2007; Sant et al., 2008). The research data on the environmental effects and bioavailability of magnetic nanoparticles is still limited, 6.3. Nanoparticle concentration related to toxicity especially on phytotoxicity, although the toxicological effects of several other types of nanoparticles, such as fullerenes,

Iron oxide (Fe3O4 and g-Fe2O3) nanoparticles are more stable, carbon nanotubes, titanium dioxide and silver, have been but still exert certain toxic effects on bacteria. It was found widely studied (Barrena et al., 2009; Miralles et al., 2012; that E. coli can withstand high concentration of iron oxide Navarro et al., 2008; Scown et al., 2010). Since plants are nanoparticles (up to 350 mg/L of Fe3O4 and 700 mg/L of g- essential constituents in ecosystems, and probably a pathway

Fe2O3)(Auffan et al., 2008; Lee et al., 2008), while the toxicity for magnetic nanoparticles transport and bioaccumulation due to nZVI was significant with less than 10 mg/L. Bacteria along food chain, the recent findings on phytotoxicity of can still be damaged by surface coated magnetic nano- magnetic nanoparticles are discussed below. particles (Singh et al., 2011). Other bacteria were also studied Various experimental methods such as in vitro study with and showed greater resistance to exposure of nZVI, even at a isolated plant cells, a whole plant, or seeds as well as various higher concentration (Xiu et al., 2010). Although Fajardo et al. experimental setups such as water, soft agar medium, and (2012) reported there was no toxicity toward a gram negative nature soil were applied (Miralles et al., 2012). The evidence on strain, even with high dose of nZVI, the nZVI used in their the phytotoxicity of nanoparticles is yet conclusive because it study was stabilized with surfactants, and other types of likely depends on the plant species, composition, concentra- bacteria were affected. In contrast, there was little toxic effect tion, size and surface properties of the nanoparticles, and of nZVI with 100 mg/L on the diversity and structure of a experimental methods. natural bacterial community in river water (Barnes et al., Although diverging results of the phytotoxicology of the 2010b). The natural river water may contain NOM lowering magnetic nanoparticles were reported, a comparatively the toxicity of nZVI, or other dissolved electrolytes complexed conclusive finding showed that the presence of soil or sand þ with Fe2 reducing oxidation stress. reduced the impacts of magnetic nanoparticles on plants. The magnetic nanoparticles tend to attach or deposit on soil or 6.4. Type of bacterial cell sand grains, leading to a reduction of availability of magnetic nanoparticles (El-Temsah and Joner, 2012; Zhu et al., 2008). Apart from the toxicological effects of magnetic nanoparticles, Several recent research papers reported the uptake of mag- both inhibition and promotion of bacterial reaction by magnetic nanoparticles from aqueous medium by different plant netic nanoparticles in contaminants removal were reported. species, such as pumpkin (Cucurbita maxima)(Zhu et al., 2008), Shin and Cha (2008) found that the microbial reduction of ni- cattail (Typha latifolia) and hybrid poplars (Populous trate was promoted with the presence of nZVI, and no lag deltoids Populous nigra)(Ma et al., 2013). Barrena et al. (2009) phase was observed. Compared with the findings from appli- observed low toxicity of Fe3O4 in germination, biolumines- cations of nZVI with microorganisms for dechlorination of TCE cent and anaerobic toxicity tests, while El-Temsah and Joner (Barnes et al., 2010a; Xiu et al., 2010), an inhibitory effect of nZVI (2012) reported the inhibitory effects of germination and was demonstrated. Although the study (Xiu et al., 2010) indi- shoot growth on ryegrass (Lolium perenne), barley (Hordeum cated that H2 generated from corrosion of nZVI was consumed vulgare), and flax (Linum usitatissimum) by nZVI at various by the dechlorinating bacteria, the TCE degradation rate was concentrations. The inhibitory effects could be due to physical water research 47 (2013) 2613e2632 2627

deposition and accumulation on the root surface (Ma et al., bacteria and plants strongly depend on the types of bacteria or 2013), leading to blockage for moisture and nutrients uptake, plant species, iron oxidation state, surface coatings, concen- or due to chemical toxicity resulting from potential dissolu- tration and size of magnetic nanoparticles, culture medium, tion and anoxic conditions caused by reductive reactions (El- and the determination methods of bacteria population or ac- Temsah and Joner, 2012; Ma et al., 2010). The magnetic tivity or parameters for phytotoxicity assays. During the nanoparticles can also lead to little growth of leaves and death sampling and measurement of bacteria activity, the nano- of older leaves (grown before dosing of nanoparticles) (Ma particles may be oxidized, aggregate, or react with extracted et al., 2013). On the contrary, It was also reported that the bacterial DNA, thereby influencing the results. For phytotox- magnetic nanoparticles could be taken up and translocated in icity, different impacts of nanoparticles can be observed at plants (Zhu et al., 2008) without any apparent visual impact, varying stages of plant growth for different species, so more in- and could even enhanced the plant growth at low concen- depth research and frequent review are required. tration (Ma et al., 2013). Taken together with the toxicology effects on bacteria, surface modifiers can reduce degree of toxicity on both plants 7. Conclusions and bacteria, probably due to reduction of attachment, and thus bioavailability. Moreover, the attachment of magnetic Five major concerns about magnetic nanoparticles for envi- nanoparticles to soil medium resulted in lower the toxic im- ronmental applications have been summarized and high- pacts, suggesting that magnetic nanoparticles at low concen- lighted. The surface chemistry of engineered magnetic tration could be used for environmental engineering nanoparticles is complex and plays a crucial role in various applications without pernicious effects on plants and bacteria. interactions. Magnetic nanoparticles readily interact with other magnetic nanoparticles, contaminants, and microbial 6.6. Current limitations communities, thus further increasing the difficulty of investigation. Given the advantages of magnetic nanoparticles, a The research findings on the toxic effects of magnetic nano- systematic understanding of surface modifications and syn- particles have generally focused on “clean” particles. Howev- thesis of magnetic nanoparticles is important to boost prac- er, during environmental applications of magnetic ticability in environmental technology. Although the smaller nanoparticles, various contaminants could interact with the particle size contributes to their larger removal capacity and particles and alter their physiochemical properties. Magnetic higher reactivity, there is a tradeoff between recovery nanoparticles may act as contaminant carriers, if the “used” magnetically, stability, and toxicity. Surface modifications can magnetic nanoparticles are internalized by cells. A synergistic help in stabilization and reduction of toxicity, but the active toxic effect could be a consequence in this ternary system, surface of magnetic nanoparticles may be sacrificed. Further cells-contaminants-magnetic nanoparticles, where the modifications may be required to enhance the number of bioavailability of loaded magnetic nanoparticles and its af- active sites for contaminant removal. Studies of toxicity have finity towards bacterial cells have yet to be studied. One had controversial results, originating from the difference be- should also note that the type of bacteria plays a critical role tween various natural environments and simplified experi- on bactericidal effects, since different bacteria have a different mental conditions. A more comprehensive and reliable tolerance on oxidative stress and exposure to nanoparticles. approach to determination of bacterial activity with the For instance, autotrophic bacteria can utilize chemical energy presence of magnetic nanoparticles is desirable. However, to which can probably withstand the high reactivity of nano- reveal the whole picture of magnetic nanoparticles in the particles (Shin and Cha, 2008; Yu et al., 2006). The strain of environment, a close collaboration among scientists and en- bacteria, gram positive or negative, also exhibits varying re- gineers with different backgrounds is required. Modification sistances to magnetic nanoparticles where electrostatic in- on magnetic nanoparticles is essential to balance effects on teractions may be taken into account (Diao and Yao, 2009; their reactivity, capacity, reusability and biocompatibility, and Fajardo et al., 2012). Other microbes like fungi have a more thus would aid their environmental applications. robust structure and are less sensitive to the environmental disturbance than bacteria (Diao and Yao, 2009). These are also abundant in natural environments. In addition, the bactericidal ability of magnetic nanoparticles can be utilized in a Acknowledgements beneficial way as a disinfecting and sedimentation agent (Diao The authors wish to thank the Research Grants Council of the and Yao, 2009; You et al., 2005). More attention should also be HKSAR Government for providing financial support under paid to assess the potential phytotoxicity of magnetic nano- General Research Fund 617309 and FSGRF12EG28. particles, because plants are critical and elemental parts of ecosystems. To better understand the toxicity of magnetic nanoparticles, all these factors should be considered for a references comprehensive study before being widely applied. Since there is no standard method for measuring bacteria activity and phytotoxicity in the presence of nanoparticles, the Afkhami, A., Moosavi, R., 2010. Adsorptive removal of Congo red, diverging results from these findings may be attributed to the a carcinogenic textile dye, from aqueous solutions by ample variables in magnetic nanoparticles and the experi- maghemite nanoparticles. Journal of Hazardous Materials 174, mental setups. The inactivation or toxicological effects on 398e403. 2628 water research 47 (2013) 2613e2632

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