Classification of Bio-Magnetic Nanoparticles: Comparison
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Please note this is a comparison between Version 2 by Camila Xu and Version 1 by Rodica Turcu.

Bio-magnetic nanoparticles (BMNPs) was introduced, describing a unique combination of physio-chemical properties of magnetic nanoparticles with their entirely biocompatible nature, which makes them particularly effective in various biomedical applications.

  • magnetic nanomaterials
  • cancer
  • drug delivery systems
  • targeted therapy

1. Introduction

Cancer represents a major public health problem worldwide, being the first leading cause of death in people below the age of 70 in North America, Canada, Australia, China, and numerous European countries [1]. With the increase in population and life expectancy, it is predicted that the incidence of cancer will rise in the following years, reaching 28.4 million cases annually worldwide by 2040 [2]. In this context, finding effective therapies for cancer is crucial for reducing the medical and economic burden of this disease.
Conventional cancer therapies include surgery, radiotherapy, and/or chemotherapy. Among these, chemotherapy is widely used but presents various side effects that can limit patient compliance and adherence [3]. Moreover, cancer cells can develop chemotherapy resistance through many mechanisms, rendering it ineffective [4]. Recently, non-coding RNAs such as micro RNAs (miRNA) and small interfering RNAs (siRNA) have been studied for their potential as novel cancer treatments due to their capacity to regulate gene transcription [5]. However, their applicability is limited too by their low stability, high costs, and immunological adverse reactions [6].
In recent years, nanotechnology has emerged as a tool for cancer treatment, promising improved therapeutic outcomes for both chemotherapy and RNA-based therapy, by delivering therapeutic agents in close proximity to the tumor using nano drug delivery systems (DDSs). Nano DDSs generally range in size between 10 and 100 nm, which allows sufficient circulation time and accumulation in the tumor tissue due to the enhanced permeability and retention (EPR) effect [7,8][7][8]. Numerous types of DDSs have been employed, such as polymers [9[9][10],10], lipid nanoparticles (NPs) [11], and metallic NPs [12] (silver, gold, or magnetic NPs). Among these, magnetic NPs represent a promising alternative, due to their properties such as high stability, high saturation magnetization/large magnetic moment of particles, good response to moderate magnetic fields, inherent ability to cross biological barriers, protection of the drug from rapid degradation in biological systems, provision of a large surface area for conjugating targeting ligands [7,8,13,14,15,16,17,18[7][8][13][14][15][16][17][18][19],19], low production costs [20], and superparamagnetism, which allows their guidance in the organism using an external magnetic field [7,21][7][21]. Scientific interest in NPs in general and in magnetic nanoparticles (MNPs) in particular has grown exponentially in the last decade, due to recent high-interest research on their properties and the fact that in a relatively short time, these materials have become particularly important tools in high-interest biomedical areas such as biomaterial science, biochemistry, diagnostics, magnetic drug and gene delivery, hyperthermia, magnetic resonance imaging (MRI), and theragnostics [22,23,24,25,26,27,28,29,30,31][22][23][24][25][26][27][28][29][30][31]. The increased interest in the field of MNPs is demonstrated by the number of scientific articles provided by a simple “magnetic nanoparticles” keyword search in the Scopus database. Before 1995, fewer than 100 articles were published, but after 1996, when the first successful clinical trials took place, there was an exponential increase with 3000 articles in 2010, 6500 in 2015, and up to 8700 in 2020 [32]. As a general structure, NPs are considered inorganic or organic particles of submicron size with enhanced properties relative to a similar bulk form. The specific physical and chemical properties given by nanostructuring, such as optical, electrical, and magnetic properties or increased reactivity, made these special types of NPs attractive to nanotechnology. Following the development of biotechnological applications, the term “bio-magnetic nanoparticles” (BMNPs) was introduced, describing a unique combination of physio-chemical properties of magnetic nanoparticles with their entirely biocompatible nature, which makes them particularly effective in various biomedical applications [33]. Starting from the particular requirements of each biomedical application, BMNPs are considered to have a huge potential in drug delivery applications, because their surface can be specifically functionalized with various molecular layers [7,14,24,34][7][14][24][34]. Apart from drug delivery, magnetic NPs can be used for hyperthermia applications, MRI contrast imaging, and diagnosis procedures. Recently, magneto-mechanical actuation of MNPs has also been used as an anti-cancer strategy. In this technique, the application of a magnetic field does not lead to heating (such as in hyperthermia), but to vibrations of the MNPs in the proximity of cells, leading to mechanical alterations and cell death [35,36][35][36]. Moreover, complex strategies combining more of these approaches can also be employed. The combination of hyperthermia and drug delivery in the same carrier can enhance anti-cancer efficiency destroying cancer cells through multiple mechanisms.

2. Classification of BMNPs

In order to properly choose the most appropriate MNPs for specific biomedical applications, a very clear classification of them according to their nature, composition, and size is required, taking into account the synthesis methods used to prepare them and the specific functionalization of the surface. Over time, several types of MNPs have been developed and researched. Generally, these MNPs can be grouped into three main categories as (i) magnetic pure metals (Fe, Co, Ni), (ii) magnetic metal oxides (Fe2O3, Fe3O4) or ferrites (MeFe2O4, Me = Fe, Co, Zn), and (iii) multicomponent magnetic nanoparticles as core/shell MNPs or magnetic nanoclusters (Figure 1). Each of these mentioned categories has both advantages and disadvantages, but their properties can be adapted to fit a particular type of application. In the following, each category will be discussed and exemplified.
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Figure 1. General classification and exemplification of magnetic nanoparticles (all images are original and belong to the researchers).

2.1. Magnetic Pure Metals

Pure metal type materials exhibit some unique properties, with some of them directly dependent on the distribution of electrons in the external orbitals, and magnetic behavior is one of these properties. Transition metals, such as Fe, Ni, Co, and Mn, are the most commonly used in this class because they show good magnetic performance in several biomedical fields [39][37]. Iron (Fe) nanoparticles are one of the most common ferromagnetic materials used for biomedical applications. The main advantage of using this material is related to its excellent magnetic properties, which can be exploited in a wide range of biomedical applications. In terms of synthesis methods, Fe nanoparticles can be obtained by relatively simple methods such as the reduction of iron salts in aqueous solutions in the presence of reducing agents such as sodium borohydride [40][38], or by thermal decomposition of Fe(CO)5 on a polymer matrix [41][39]. Even if the synthesis methods are facile and accessible, one of the major weaknesses of these NPs is that synthesis requires rigorous control of the surface-covering shell since direct contact between the Fe surface and air leads to their combustion. Therefore, the necessity to find homogeneous and uniform coatings for this kind of nanoparticle is critical. There are studies in which tailoring the reaction parameters and changing the Fe precursor to Fe[N(SiMe3)2]2 can result in major improvements in the reaction yield, better control of the size distribution, and a reduction in by-product formation [42][40]. In addition to Fe NPs, cobalt (Co) is another magnetic material commonly used in biomedical applications. Although its toxicity is higher than that of Fe NPs, beneficial effects of its use have been observed in specific MRI imaging applications and local hyperthermia of malignant tumors [43,44][41][42].

2.2. Magnetic Metal Oxides

From the general class of metal oxides, iron oxide distinguishes itself as a material with excellent magnetic properties and low toxicity compared to pure metallic forms, which, due to its unique physio-chemical properties, has potential applications in nanotechnology [39][37]. Over time, metal oxides have gained popularity in biomedical applications due to their physicochemical and mechanical stability, low toxicity, and biocompatibility but also for their efficiency in some special areas of biomedical science such as magnetic bio-separation of some species of interest, magnetic hyperthermia, drug carriers at target sites, and bio sensing [45,46][43][44]. There are three types of iron oxides: Iron (III) oxide, with two subspecies: Hematite (α-Fe2O3) and maghemite (γ-Fe2O3); a rare type of iron (II) oxide (FeO) called wüstite; and iron (II, III) oxide named magnetite (Fe3O4). This different stoichiometry due to the flexibility of the Fe oxidation state (Fe2+/Fe3+) is supported by the formation of different single-crystal phases with different chemical and physical properties. Of all iron oxide structures, Fe3O4 has the most closely packed cubic inverted spinel structure and semi metallic properties, demonstrating great potential in biomedical fields [47][45]. One of the biggest advantages of these NPs is the ease of their synthesis at relatively high reaction yields by simple and conventional methods. In the beginning, conventional preparation methods such as the co-precipitation or solvothermal method [48,49,50,51,52,53][46][47][48][49][50][51] did not offer rigorous control over the size and size distribution of MNPs, so aggregation and poly dispersibility appeared, which hindered their use in biomedical applications. Over time, however, new synthesis methods were explored to obtain size-controlled NPs with a uniform size distribution. For example, by using organic iron precursors, Fe3O4 NPs with a narrow size distribution were obtained. By adjusting the molar ratio between metal precursors and different surfactant molecules, different particles can be obtained ranging in shape from cubic to polyhedral [54][52]. It can be concluded that the physicochemical properties of NPs, in particular the magnetic properties, can be adjusted according to the intended application with minimal changes in the composition and synthesis parameters. Although iron oxides have the advantage of easy preparation, they present certain limitations related to chemical stability under biological environmental conditions, often resulting in aggregation phenomena that decrease their potential use in biomedical applications. Coating the surface of iron oxide NPs with biocompatible molecular layers increases chemical and mechanical stability, reduces surface oxidation, and decreases toxicity in biological entities. Thus, iron oxide NPs, generically called superparamagnetic iron oxide nanoparticles (SPIONs), have been developed. These particles represent small synthetic iron oxide particles with a core ranging between 10 nm and 30 nm in diameter, coated with certain biocompatible molecules, which provide chemical handles for the conjugation of therapeutic agents and improve their blood distribution profile [55][53]. These particles exhibit superparamagnetic properties, meaning that under an external magnetic field, they magnetize to saturation magnetization, and when the magnetic field is removed, they exhibit no residual magnetic interaction. This property is dependent on the size of the NPs and generally occurs when their size is only 10–20 nm. At such a small size, these NPs do not exhibit multiple magnetic domains, as found in larger NPs, acting as a “single super spin” that exhibits high magnetic susceptibility. Thus, upon application of a magnetic field, these NPs provide a stronger and faster magnetic response compared to bulk magnets with negligible residual magnetization and coercivity (the field required to bring the magnetism to zero) [56][54]. This unique property of SPIONs represents a great advantage for their use in specific biomedical applications such as controlled drug delivery where these NPs function as drug delivery vehicles because they can drag specific drug molecules to the target site, under the influence of an external magnetic field. Furthermore, once the applied magnetic field is removed, the magnetic particles do not retain any residual magnetism and aggregation phenomena are avoided, thus evading absorption by phagocytes and increasing half-life in circulation. In addition, due to their negligible tendency to agglomerate, SPIONs pose no danger of thrombosis or blockage of blood capillaries [55][53]. A sub-division of metal oxides, emerging from the necessity of adjusting the properties of this type of material for specific biomedical applications, is spinel ferrites (MeFe2O4), a very important magnetic material due to their combined electrical and magnetic properties, which make them useful in many technological applications [57][55]. The main component of these materials is iron oxide doped with a variety of bivalent transition metals such as zinc (Zn), manganese (Mn), cobalt (Co), nickel (Ni), iron (Fe), platinum (Pt), and palladium (Pd). It has been demonstrated that due to the doping of the Fe3O4 structure with bivalent cations, ferrites show improved electrical and magnetic properties for hyperthermia applications, for example, but also present the disadvantage of higher toxicity compared to magnetite [58][56]. The use of some stabilizing molecules, which also confer biocompatibility on the ferrite NPs surfaces, is essential for biomedical practical applications. In the synthesis of Co ferrite NPs, a CoFe2(CO)9 precursor and two stabilizing agents, hexadecylamine and oleic acid, were used to obtain small, relatively polydisperse MNPs. When a third stabilizing agent, lauric acid, was introduced, bigger monodispersed crystalline structures with a narrower size distribution were obtained. A decrease in the toxicity of the system was also demonstrated, with the developed system showing promising applications against tumor cells [59][57]. Another particularly efficient approach to using ferrite NPs in biomedical applications is their coating with biocompatible polymer layers, such as polyhydroxy and polyamine-type polymers and polyethylene glycol (PEG). It has been proven that the use of these systems in controlled drug release applications is particularly effective, with researchers also performing biocompatibility tests, which demonstrated that these materials can be successfully applied without adverse effects regarding toxicity [60][58]. Other ferrite-type magnetic structures have been reported in the literature, which, in addition to excellent magnetic properties, also show lower toxicity, such as Zn-, Mn-, and Ni-based ferrites [61][59]. There are also ferrite-type systems, with two transition metal components, Co-Zn and Mn-Zn type, in which it was highlighted that the concentration of Zn ions has an effect on the size of the final particles, i.e., increasing the concentration of Zn cations decreases the size of the particles [62][60].

2.3. Multicomponent Magnetic Nanoparticles

Multicomponent MNPs have been developed as a normal evolution of the technology because these systems can present multiple functionalities at the same time, by simply combining two or more components and thus offering new features that are not available in single-component materials or structures. In addition, in these multicomponent systems, improved specific properties can be obtained that may overcome the natural limitations of single-component materials. There are several types of multicomponent magnetic structures, but the most often studied and with real possibilities of application in biomedicine are the two main categories: (i) Core/shell type multicomponent MNPs and (ii) magnetic clusters (MCs).
(i)
 Core/shell-type multicomponent magnetic nanoparticles
Core/shell-type MNPs are the most common type of multicomponent NPs and have been widely studied. Core/shell structures were first prepared in semiconductor NPs [63][61] with the specific aim to modify their electrical and optical properties. The extension of this idea to magnetic systems initially emerged as an idea to protect and enhance the properties of metallic MNPs by coating them with protective layers, especially Fe NPs, which have extremely high reactivity in metallic form. Core/shell composite structures of Fe/Fe3O4 type with a magnetic core consisting of iron NPs (Fe) and a thin protective coating of iron oxide (Fe3O4) were prepared [64][62]. Following the same idea of covering magnetic cores of other metals, various multicomponent magnetic systems have been developed, in which the metallic magnetic core was synthesized by the so-called seed-mediated process followed by coating with oxide layers of the same metal and/or various metallic combinations, such as Ni/NiO [65][63], Co/CoSe [66][64], Co/Co2P [67][65], and Pt/Fe2O3 [68][66]. Another successful possibility consisted of covering metallic Fe NPs with a ferrite shell (Fe@MFe2O4, M = Fe, Mn, Co) [69][67]. The core/shell composite system kept high-level magnetic properties, presented high relaxivity, and remained mono-dispersed throughout the experiments without showing aggregation processes under the action of the biological environment. There are also core/shell type multicomponent magnetic systems in which the magnetic core is bimagnetic, obtained by an interesting combination of two magnetic metallic species, covered as a whole with an oxide coating. A successful example of such synthesized systems is the FePt/Fe3O4 core/shell system where MNPs from the core were obtained by sequential decomposition of some organic precursors Fe(acac)3 and Pt(acac)2 and the thickness of the external shell was tailored from 0.5 nm to 5 nm by controlling the synthesis parameters [70][68]. The seed-mediated growth method was extended to prepare other types of core/shell binary systems such as FePt/ZnO [71][69], Fe3O4/ZnO [72][70], Co/CdSe [73][71], FePt/PbS [74][72], and Fe3O4/Cu2−xS [75][73]. Another model of multicomponent core/shell systems, in which the magnetic core was made of iron oxide NPs (Fe3O4) covered with a noble metal coating, was also obtained. The as-prepared systems Fe3O4/Au [76][74] and Fe3O4/Au/Ag [77][75] were later functionalized appropriately for the intended biomedical application. This system not only benefits from the excellent magnetic properties of the SPION core but also from the plasmon resonance properties of the noble metals in the combination of the multicomponent magnetic system [78][76].
(ii)
 Magnetic clusters
In recent years, MC systems obtained by controlled self-assembly of superparamagnetic nanoparticles into three-dimensional clusters have gained popularity in biomedical applications, based on the new, innovative, collective properties that hold great promise for the development of advanced bio nanomaterials with novel integrated functions [79][77]. Depending on the preparation method and the nature of the functionalizing polymers, MNPs can be assembled with different spatial orientations resulting in clusters with different shapes and sizes (spheres, rod-like, nanoring, etc.) [80[78][79][80],81,82], which influence their properties. MCs with a polymer coating are very promising for theragnostic applications since they ensure an increase in the performance of MRI and hyperthermia and allow encapsulation of the drug that can be released at the target [80,81,83][78][79][81]. MCs are defined as systems consisting of a finite number of interacting spins ranging from a few hundred to several thousand, with well-controlled sizes, shapes, and compositions, which are magnetically isolated from the environment [84][82]. From the general definition of MCs, an important subclass of MCs is distinguished, consisting of several hundred MNPs with superparamagnetic properties [85[83][84],86], self-assembled as up to 100 nm MCs. In these systems, the spin dynamics exhibit many features similar to those of the molecular nanomagnets, such as superparamagnetic relaxation and quantized spin-wave states [87][85]. Since some of the properties of MCs depend on both the sizes of the MCs and the component NPs, considerable effort is required to control these two structural parameters in order to establish the optimal structure–property relationship and to obtain multicomponent magnetic systems with specific properties for biomedical applications. The development of robust synthesis protocols that allow rigorous control over the composition, size, and shape, as well as cluster surface properties and uniformity of colloidal NPs, requires a very good understanding of the mechanisms that induce aggregation phenomena. The forces involved in the controlled aggregation process of MNPs are both covalent and non-covalent such as hydrogen bonding, electrostatics, and van der Waals interactions, forces that can be controlled by the modification of synthesis parameters, such as the nature and concentration of solvents, the surfactants involved, the reaction temperatures, and reaction times [79][77]. The literature presents a wide variety of preparation methods for MCs, including options that involve several simple procedures integrated into a single reaction step or more complex versions that produce MC in a single reaction step. A classification of MC preparation methods can therefore be made as follows: (a) Single-step MC procedures, which integrate the synthesis of MNPs and their controlled aggregation into clusters in a single step, and (b) multi-step MC procedures, which first produce MNPs of a specific size, shape, and surface functionality and then self-assemble into clusters of required geometrical configurations in subsequent separate steps. Each of the synthesis methods has both advantages and disadvantages. While single-step processes are easier in terms of methods and more efficient in terms of producing MCs, the control of the synthesis parameters is less rigorous because the NPs’ synthesis and the clustering steps take place at the same time. Multi-step processes have the advantage of being more flexible in terms of primary materials, being able to produce a wide variety of materials in cluster form with well-organized structures, but they also bring a higher complexity, as well as some disadvantages in terms of magnetic properties, which may decrease due to the functionalization of the surface with relatively thick layers of non-magnetic materials.
(a)
 Single step-magnetic cluster procedures
From the most popular preparation techniques for the synthesis of MCs in a single reaction step, the thermolysis method and the solvothermal method can be listed. In the following, some literature references of each of these methods will be exemplified, although it should be noted that there is no generally accepted method, and each synthesis of MCs with different shapes, sizes, structures, and surface functionality will involve specific synthesis parameters that cannot be reproduced for other versions. The thermolysis method involves the reaction of metal precursors in the presence of the capping ligand in an organic solvent at a high temperature. Due to the high temperature, the metal precursor decomposes, and the nanoparticle seed and growing reaction is initiated. At this point, the capping ligands bind to the surface of the NPs, limit their growth, and prevent the formation of interparticle bonds, also leading to the clusterization of the NPs in controlled shape and size clusters through steric interactions between ligand molecules. The nature and concentration of the capping ligands play an essential role in obtaining structurally homogeneous clusters with a uniform size distribution. Using the thermolysis method, oxide clusters of transition metals such as In2O3, CoO, MnO, and ZnO were prepared by reducing the concentration of stabilizing organic ligands to the point where insufficiently stabilized primary NPs agglomerated in a controlled three-dimensional form [88][86]. The thermolysis method has also been successfully implemented to produce MCs with Fe3O4 as primary MNPs in a single reaction step at a high temperature to obtain polyelectrolyte-coated MCs [89][87]. In this process, basic hydrolysis of the iron precursor (FeCl3) using diethylene glycol as a solvent and polyacrylic acid as a surfactant took place at 220℃. The size of the MCs could be controlled by modifying the synthesis parameters, such as varying the pH and controlling the molar ratio between the metal precursor and surfactant, resulting in homogeneous geometry and narrow size distributions of MCs with sizes between 30 and 180 nm. The solvothermal method consists of chemical reactions of metal precursors in a closed environment called and autoclave at high temperatures, higher than the boiling point of the solvent. This method has very quickly become a commonly used method due to its versatility and simplicity of application in terms of materials, methods, and cost. There are, however, several disadvantages of this method, namely the relatively high energy requirements, the reactions taking place at high temperatures for long reaction times, the limited scalability, and the lack of direct monitoring of the reaction process. In the literature, there are many studies that describe the preparation of MCs obtained by the solvothermal method [48,49,50,51,52,53][46][47][48][49][50][51].
(b)
 Multi-step magnetic cluster procedures
Multi-step MCs procedures involve the preliminary preparation of MNPs, using traditional methods that are subsequently assembled in one or more reaction steps in clusters with controlled shapes and sizes. This method offers the opportunity to combine the inherent properties of MNPs with innovative properties resulting from the collective interaction of NPs within the clusters. A large number of new composite materials commonly produced in the form of NPs with excellent control over size, shape, and surface properties can be developed easily and with remarkable properties, which can later be modularly assembled in the form of super-structured nanomaterials with various configurations and programmable properties. One of the simplest methods to obtain MCs in two reaction steps was the encapsulation of the MNPs in different encapsulating agents with a specific function for controlled aggregation, protection, and surface functionalization. For the embedding process, different types of molecules were used as encapsulating agents, including polymers and/or block copolymers [90[88][89][90],91,92], micelles [93][91], polysaccharides [94][92], or hydrogels [95][93]. Another efficient clustering method is the emulsion method, slightly modified as the mini-emulsion method, if MCs of hundreds of nanometers in size are obtained. The mini-emulsion method can have two alternatives, direct emulsion, generically called “oil-in-water emulsion” in which oil (nonpolar solvent) droplets form micelles in an aqueous medium containing a water-soluble surfactant, or inverse emulsion, generically called “water-in-oil emulsion” in which water droplets form micelles in an organic medium with a non-polar dissolved surfactant. For the preparation of MCs, the mini-emulsion oil-in-water method is most commonly used because the pre-prepared magnetic particles can be easily dispersed in an organic solvent and used as the organic oil phase. In this process, MNPs prepared in a previous reaction step are homogeneously dispersed as a colloidal solution in a non-polar organic solvent, such as cyclohexane, dodecane, or toluene, to form an organic phase, generically called the “oil” phase. At the same time, a surfactant aqueous solution is prepared having dissolved a surfactant agent such as sodium dodecyl sulphate or cetyltrimethylammonium bromide, which has an amphiphilic structure. Using an ultrasonic finger, the two non-miscible phases are mixed to form a mini-emulsion. The mini-emulsion represents droplets of the organic phase, oil, containing the MNPs dispersed in water, where the surfactant is oriented with the hydrophobic end to the oil droplets and the hydrophilic end to the aqueous medium, creating stable oil in water micelles. The oil-in-water mini-emulsion is heated and the organic solvent from the micelles is evaporated, forming hydrophilic MCs. The size of these clusters can be adjusted by changing the concentration of NPs in the medium and the surfactant in the oil phase [96][94]. Using this method, composite clusters have been obtained by encapsulating various types of nanoparticles in different micelles, and/or molecular layers, polymers, and organic or inorganic layers such as γ-Fe2O3/TiO2 [97][95], NaYF4-Yb,Er/NaYF4:Eu [98][96], CeO2/Pd [99][97], polystyrene [100][98], and Fe3O4/OA-FeCo/Al2O3 MCs [101][99].

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