Superparamagnetic iron oxide nanoparticles: magnetic nanoplatforms as drug carriers

Figures & data

Figure 1 Physicochemical considerations of superparamagnetic iron oxide nanoparticles for drug delivery.

Table 1 Different routes of synthesis of superparamagnetic iron oxide nanoparticles along with their reaction conditions, advantages, and disadvantages

Method employed	Reaction temperature (°C)	Solvent used	Size range (nm)	Morphology	Advantages	Disadvantages	Feasibility of large-scale production	Published reports
Coprecipitation	20–90	Water	15–200	Spherical or rhombic	Simplest and most efficient chemical method By adjusting pH and ionic strength, particle size can easily be controlled This method can be easily modified for synthesis in the presence of dextran and other coating materials, rendering magnetic nanoparticles biocompatible and hence suitable for in vivo applications Almost all commercially available iron-oxide based MRI contrast agents are fabricated by this route	Large particle size distribution Sometimes, aggregation and poor crystallinity resulting in low saturation magnetization values Sometimes, ions get oxidized before precipitation, affecting the physical and chemical properties of SPIONs	Yes	^Citation28,Citation29,Citation137–Citation140
Microemulsions	20–50	Organic compound	4–12	Spherical or cubic	Adequate, versatile and simple method Surfactant-stabilized microcavities provide confinement effect that limit particle nucleation, growth, and aggregation, thus better controlling particle size as well as particle shape Homogenous particle size distribution	Adequate crystallinity of SPIONs is sometimes difficult to achieve on a large scale due to low temperature usage Complicated purification methods for separation of surfactants Yield of nanoparticles is low compared with coprecipitation method Large amount of solvents required	No	^Citation28,Citation137,Citation138,Citation141
Hydrothermal synthesis	220	Water-ethanol	520	Spherical	This approach takes advantage of increased solubility and reactivity of metal salts and complexes at elevated temperature and pressure without bringing the solvent to its critical point Well control of growth dynamics and agglomeration of metal nanoparticles Important synthetic route for production of ferrites	Harsh reaction conditions, hence experimentally demanding Unwanted oxidation at the surface of metal nanoparticles Longer reaction time	Yes	^Citation137^–^Citation140
Sol-gel synthesis	200–400	Organic compound	20–200	Spherical	Suitable for producing powders of magnetic materials Through nonhydrolytic sol-gel route, monodispersed nanoparticles can be produced Particles of desired shape and size can be fabricated, useful for making hybrid nanoparticles	Difficult to obtain monodispersed nanoparticles through hydrolytic sol-gel route Requires toxic reagents and complicated synthesis steps Contamination of products with sol-gel matrix constituents Broad size distribution	No	^Citation140,Citation142
Electrochemical deposition	70–100	Organic compound	3–8	Spherical	Size can easily be controlled by imposed current density Very narrow particle size distribution ensuring homogenous distribution	High cost of production Difficult to remove surfactant used in the process	No	^Citation28,Citation143
Sonochemical method	25	water	10–30	Spherical or rod-shaped	Monodispersed nanoparticles of a variety of shapes can be produced Produces γ-Fe203 nanoparticles useful in biotechnology	Particle size tunability is not easily achievable Utilizes organometallic precursors, can cause in vivo toxicity	No	^Citation137,Citation144,Citation145
Polyol method	120–280	Organic compound	5–40	Spherical	Nonagglomerated iron oxide particles with well defined shape and size can be obtained High boiling point of polyols can be used as a solvent as well as a reducing agent	Scale up sometimes lead to nonuniform particle shape and size, needs modification Broad particle size distribution	Yes	^Citation146^–^Citation149
Thermal decomposition	100–320	Organic compound	3–20	Spherical	Can be employed to separate nucleation and growth processes yielding samples with good size control, narrow size variation of 5%, and good crystallinity Monodispersed iron oxide particles can easily be prepared Very narrow size distribution with no follow-up size selection procedures Polar solvents like 2-pyrrolidone along with thermal decomposition allow use of various surface ligands to achieve biocompatible SPIONs via a “one-pot” reaction	Uses complicated and harsh preparation procedures Surfactant (eg, oleic acid) is used in the process, which hinders subsequent surface modification Employ organometallic compounds which can cause in vivo toxicity, hence replaced by metal salts Requires use of very high decomposition temperature leading to formation of iron oxide on the surface of iron nanoparticles	Yes	^Citation137–Citation140,Citation149–Citation151
Spray pyrolysis	400–700	Organic compound	5–60	Spherical but aggregated into larger particles	It is a simple, rapid and continuous process Finely dispersed particles of predictable size, shape and variable composition can be prepared This method allows the preparation of air-stable superparamagnetic α-Fe metallic and FeCo nanomagnets encapsulated in silica or aluminum	Requires exhaustive control of the experimental conditions Cost of production is high	Yes	^Citation28,Citation137,Citation152
Laser-induced pyrolysis	1100	Organic compound	5–30	Spherical but less aggregated	Continuous method of production Small particle size Narrow particle size distribution Nearly absence of aggregation High production rate, good alternative to coprecipitation method for the synthesis of MRI contrast agents	Cost of production is high Requires exhaustive control of experimental conditions	Yes	^Citation28,Citation137
Biomimetic synthesis (mediated by bacteria, fungi and protein)	–	–	50–100	Spherical, cluster, cubo-octahedral	Nanoparticles synthesized by this route find variety of bioapplications Presence of phospholipid bilayer makes particle biocompatible and suspension of particles are very stable Particles can be easily modified These magnetic particles can be used for immobilization of a variety of enzymes, antibodies and oligonucleotides	Lacks large-scale synthesis with well defined shape and size Lower yield of magnetic nanoparticles	No	^Citation2,Citation28

Abbreviations: MRI, magnetic resonance imaging; SPIONs, superparamagnetic iron oxide nanoparticles.

Table 2 Encapsulating materials and targeting ligands used to functionalize the surface of superparamagnetic iron oxide nanoparticles and their applications

Coating material	Targeting strategy	Targeting ligand	Target	Particle size distribution	Properties bestowed by coating on particle	Applications	Advantages	Published reports
Poly(dl-lactic acid)	Active	Herceptin^® (Her2 antibody)	Human breast cancer	50–200 nm	Improves hemocompatibility and produces no hemolysis, ensure uniform particle size distribution	Radiotherapy, drug targeting and imaging	Biodegradable, can be conjugated with other polymers like PEG resulting in desired alternation of magnetic properties	^Citation78,Citation153–Citation155
		Anti-CD20 monoclonal antibody (rituximab)	CD-20 antigen (Non-Hodgkin lymphoma)
	Passive	–	–
PEG	Active	N-terminated A10 RNA aptamer	PSMA	10–50 nm	Improves dispersity and blood circulation time, provides chemical handles for drug attachment, reduces toxicity, decreases enzyme degradation	Imaging and drug delivery particularly to tumors mainly brain and breast	Efficient surface coating, can easily be crosslinked to reduce the burst effect of anchored drugs	^Citation2,Citation16,Citation129,Citation156,Citation157
		Antihuman VCAM-1 antibodies	VCAM-1 as an early marker of atherosclerosis
		Chlorotoxin	MMP-2
		Folic acid	Folate receptor
		Methotrexate	Folate receptor
	Passive	–	–
Dextran	Active	Monoclonal antibody A7	Human colorectal carcinoma	10–200 nm	Improves biocompatibility, enhances blood circulation time, reduces aggregation	Imaging and drug delivery Conjugated with urokinase for targeted thrombolysis	Efficient coating due to high affinity for iron oxide surface	^Citation2,Citation158–Citation159
		Herceptin	Human breast cancer
	Passive	–	–
Chitosan	Active	ANP	ANP receptors	20–100 nm	Improves biocompatibility, imparts hydrophilicity, ease of functionalization due to presence of amino and hydroxyl functional groups	Nonviral gene delivery, drug therapy, hyperthermia, tissue engineering, targeted photodynamic therapy	Large natural abundance, cheap and easy availability	^Citation2,Citation130,Citation160,Citation161
		CEA antibody	CEA
	Magnetic targeting	–	–
Silica	Active	Annexin V	Phosphatidylserine	10–300 nm	Provides scaffold for enzyme immobilization, serves as template for radical polymerization with other molecules	Controlled drug delivery, imaging and separation of biomolecules, apoptosis imaging	Large surface area, does not require utilization of organic solvent, thus reduced toxicity due to residual organic solvents	^Citation2,Citation162
	Passive	–	–
Silane	Active	Methotrexate	Folate receptors	10–200 nm	Increases saturation magnetization, decreases wear rate of coated particles	Breast cancer imaging and drug delivery, assessing angiogenic profile of tumors Magnetic separation and purification of DNA	Enhances dispersion in biological matrix, can significantly improve protein immobilization	^Citation156,Citation163–Citation167
		Arg-Gly-Asp (RGD) peptide	αvβ3 integrin
	Passive	–	–
Glycerol monooleate	Active	Herceptin	Her2/neu receptors (breast cancer)	100–200 nm	Improves biocompatibility, can be easily functionalized with other chemical moieties	Sustained release of encapsulated drug, capable of delivering high payload hydrophobic anticancer drugs	Does not affect magnetic properties of Fe2O3, high entrapment efficiency, can reduce burst release of drugs	^Citation168,Citation169
Albumin	Active	Anti-EGFR antibody	EGFR	100–200 nm	Improves biocompatibility, reduces toxicity, stabilizes preparation	Drug targeting and cell separation, imaging of esophageal squamous cell carcinoma	Does not affect cell proliferation	^Citation170
	Passive	–	–
Liposomes	Active	Antitransferrin receptor single-chain antibody fragment	Transferrin receptor	20–200 nm	Enhances blood circulation time, increases SPION specificity and uptake into tumor cells, prevents enzymatic degradation of drugs encapsulated	Use in gene medicine and drug delivery, hyperthermia, and imaging	Simple and easy surface modification Increased payload, does not reduce superparamagnetic property of bare SPIONs on coating	^Citation21,Citation48,Citation93
Gold	Magnetic targeting	–	–	30–100 nm	Improves colloidal stability, reduces surface toxicity, provides a strong binding surface for a self-assembled monolayer of enzyme	Magnetically directed enzyme prodrug therapy, delivery of nitroreductases	Exhibits strong magnetic response, uniform coating Protects iron oxide core from oxidation, superior optical properties	^Citation171^–^Citation173
Polyvinyl alcohol	Passive	–	–	10–50 nm	Prevents aggregation of particles, reduces toxicity, provides chemical handles for functionalization	Drug delivery especially brain, in vivo contrasting and imaging	Amino-PVA exhibit high uptake efficiency in cells	^Citation41,Citation131,Citation174
PEI	Magnetic targeting	–	–	50–100 nm	Imparts colloidal stability at higher salt concentrations, offers high positive charge density	Nonviral gene delivery, magnetofection	Efficient and fast delivery of genetic material, exhibits proton sponge effect	^Citation42,Citation111,Citation112
Erythrocytes	Passive/magnetic targeting	–	–	10–100 nm	Imparts biocompatibility, promotes long blood circulation half-life by circumventing rapid clearance by reticuloendothelial system	Drug targeting, cell separation, intravascular imaging and contrasting	Easily available, biocompatible, does not exert immunogenicity because of their autologous nature	^Citation175
Gelatin	Passive	-–	–	50–100 nm	Imparts hydrophilicity and biocompatibility, ease of functionalization with drugs and targeting ligands due to abundance of amino groups	Separation of DNA, drug delivery and targeting	Natural polymer, efficient drug loading	^Citation130,Citation176
Polyvinyl pyrrolidone	Passive	–	–	10–25 nm	Improves colloidal stability, enhances blood circulation time	Drug delivery, imaging, and contrasting	Uniform coating, efficient drug loading	^Citation177
Polymethyl methacrylate	In vitro use	–	–	10–50 nm	Facilitates separation of genetic material and amplification	mRNA/DNA-purification Isolation of specific gene sequences Immunomagnetic assays	Simple, easy to carry out, process can easily be automated	^Citation78,Citation178
Ethyl cellulose	Magnetic targeting	–	–	20–50 nm	Imparts colloidal stability	Sustained release of drugs, arterial chemoembolization	Maintenance of drug concentration at desired site for prolonged period of time, retains sufficient magnetic responsiveness	^Citation78,Citation179
Pullulan	Passive targeting	–	–	40–45 nm	Decreased cytotoxicity, increased cellular uptake, and reduced aggregation	Imaging of vascular compartment, lymph nodes perfusion imaging, receptor imaging and target specific imaging	Easily prepared, high uptake efficiency	^Citation20
PLGA	Magnetic targeting	–	–	4–12 μm	Ensures homogenous distribution and reduced aggregation, increased biocompatibility with synovial tissues	Intra-articular treatment of inflammatory diseases like arthritis, osteoarthritis	Adequate magnetic retention under the influence of magnetic field	^Citation108, ^Citation110, ^Citation180
Starch	Passive	–	–	10–20 nm	Improves biocompatibility, reduced aggregation	Imaging and contrasting radiotherapy	Natural polymer, can be modified with other polymers like PEG	^Citation92, ^Citation181

Abbreviations: ANP, atrial natriuretic peptide; CEA, carcinoembryonic antigen; EGFR, epidermal growth factor receptor; MMP-2, matrix metalloproteinase-2; PEG, polyethylene glycol; PEI, polyethylenimine; PLGA, polylactic-co-glycolic acid; PSMA, prostate-specific membrane antigen; PVE, polyvinyl alcohol; SPIONs, superparamagnetic iron oxide nanoparticles; VCAM1, vascular cell adhesion molecule 1.

Figure 2 Superparamagnetic iron oxide nanoparticle targeting approaches.²

Table 3 Role of superparamagnetic iron oxide nanoparticles in different areas of magnetic resonance imaging

Focus area	Important remarks	References
Molecular imaging	Allows sensitive and specific monitoring of key molecular targets Allows monitoring of host responses associated with early events in carcinogenesis Imaging of cell trafficking/migration, apoptosis detection and imaging of enzyme activities	^Citation182^–^Citation188
Cardiovascular disease imaging	Uptake by macrophages utilized to visualize atheromatous plaques prone arterial sites Useful in evaluating the risk of acute ischemic events	^Citation62,Citation189–Citation192
Cancer imaging	Utilized in clinical imaging of liver and spleen tumors and metastases through RES-mediated uptake Effective in identification of lymph node metastases, useful in treatment of prostate, breast, and colon cancer Prolonged delineation of brain tumor boundaries and quantify tumor volumes Useful in imaging CNS tumor neovasculature and assessing therapeutic response to antiangiogenic chemotherapeutic agents	^Citation62, ^Citation82,Citation191–Citation197
Autoimmune disorders imaging	Used to visualize macrophage infiltration in brain, assess blood-brain barrier damage and neurological impairment in chronic relapsing experimental autoimmune encephalomyelitis, rodent model of human multiple sclerosis Used to monitor distinct pattern of macrophage migration in acute disseminated encephalomyelitis	^Citation82,Citation192,Citation198,Citation199
Central nervous system disease imaging	Serve as useful tool for noninvasive anatomic and temporal tracking of stem cells in CNS trauma and stroke Used to monitor disease progression in epilepsy Allows MRI visualization of neuroinflammation in vivo Allows monitoring of leukocyte trafficking in the brain	^Citation82, ^Citation200^–^Citation204

Abbreviations: CNS, central nervous system; MRI, magnetic resonance imaging; RES, reticuloendothelial system.

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