Rheology of magnetic colloids containing clusters of particle platelets and polymer nanofibres

Abstract

Magnetic hydrogels (ferrogels) are soft materials with a wide range of applications, especially in biomedicine because (i) they can be provided with the required biocompatibility; (ii) their heterogeneous structure allows their use as scaffolds for tissue engineering; (iii) their mechanical properties can be modified by changing different design parameters or by the action of magnetic fields. These characteristics confer them unique properties for acting as patterns that mimic the architecture of biological systems. In addition, and (iv) given their high porosity and aqueous content, ferrogels can be loaded with drugs and guided towards specific targets for local (non-systemic) pharmaceutical treatments. The ferrogels prepared in this work contain magnetic particles obtained by precipitation of magnetite nanoparticles onto the porous surface of bentonite platelets. Then, the particles were functionalized by adsorption of alginate molecules and dispersed in an aqueous solution of sodium alginate. Finally, the gelation was promoted by cross-linking the alginate molecules with Ca²⁺ ions. The viscoelastic properties of the ferrogels were measured in the absence/presence of external magnetic fields, showing that these ferrogels exhibited a strong enough magnetorheological effect. This behaviour is explained considering the field-induced strengthening of the heterogeneous (particle–polymer) network generated inside the ferrogel.

This article is part of the theme issue ‘Patterns in soft and biological matters'.

1. Introduction

The development of biocompatible hydrogels has received considerable attention in the last few decades due to a series of biomedical applications, among which it is worth mentioning their use as scaffolds in tissue engineering [1–3], for example bone or cartilage regeneration [4,5], or alternatively as carriers for local drug delivery in cancer therapy [6].

Hydrogels can be defined as polymeric networks, capable of absorbing and retaining high amounts of aqueous solutions, without being dissolved in the liquid media. Usually, the polymer chains form three-dimensional structures generated by (chemical or physical) cross-linking among the polymer molecules. However, most hydrogels suffer from a lack of mechanical strength, which usually limits their applications in a variety of fields. Many efforts have been devoted to improving the stiffness of hydrogels. Among them, the combination of organic–inorganic compounds through blending of polymers with nanoparticles has received special attention because of its excellent mechanical resilience when compared with conventional hydrogels [7,8]. In this context, the use of magnetic particles seems a promising approach because of their field-responsive properties [9–11]. In addition, the use of composite magnetic particles of low average density has been proved as a good way to avoid the heterogeneous distribution of the particles inside the ferrogels [12]. Furthermore, if the composite particles have low density and elongated shape (e.g. sepiolite–magnetite), the magnetic control of the mechanical properties of the resulting ferrogels can be considerably improved [13].

On the other hand, facing biomedical applications, natural polymers are usually preferred instead of synthetic ones because they satisfy the required biocompatibility of the resulting gels [10]. Among natural polymers, polysaccharides, peptides and proteins have a demonstrated capability for generating these kinds of soft–wet biomaterials [11–19]. In particular, alginate is a natural polysaccharide of particular interest because it is soluble in water, relatively inexpensive, non-toxic and biocompatible. The molecule of sodium alginate bears carboxylate groups and has the ability to form hydrogels by electrostatic interaction with divalent cations (especially Ca²⁺) at room temperature. This kind of physical cross-linking is the key characteristic for the formation of the alginate hydrogels employed in the present work [20,21].

The aim of the present work is to prepare and study the physical properties of ferrogels consisting of magnetic particles embedded into a matrix of alginate hydrogel. The magnetic particles were synthetic composites of low density containing a core of clay covered by magnetite nanoparticles. The clay chosen was bentonite because the particles of this mineral have a plate-like shape and, according to our previous experience [13], the magnetorheological (MR) response of ferrogels based on elongated particles can be significantly stronger than that of ferrogels based on spherical particles. In this paper, we first describe the synthesis of the clay–magnetite composites. Then, we analyse their more relevant physico-chemical characteristics (including magnetization curves) by different techniques. After that, we describe and discuss the rheological behaviour of both the bentonite–magnetite (‘BMag’ in what follows) aqueous suspensions and the BMag–alginate ferrogels, in the absence/presence of magnetic fields.

2. Material and methods

(a). Materials

The raw bentonite material used in this study was collected from Zaghouan (northeast of Tunisia). It was subjected to a purification process using the so-called hydrocyclone separation method, previously described in detail in [22,23]. This process allowed removing impurities present in the raw material (mainly calcite and quartz), and also replacement of the original calcium exchange ions present in the clay mineral by sodium ones. The main characteristics of the purified bentonite employed in the present work were [22] (i) bulk chemical composition, obtained by X-ray fluorescence, in weight per cent: 49.28% SiO₂, 20.82% Al₂O₃, 6.98% Fe₂O₃, 3.74% CaO, 2.80% MgO, 1.94% Na₂O, 2.02% K₂O, 0.11% P₂O₅, 1.08% TiO₂, 0.02% MnO; (ii) cation exchange capacity 64 meq/100 g; (iii) specific surface area 70 m² g⁻¹; (iv) the thickness (a) and length (L) of the bentonite platelets were (mean ± s.d.) a = 0.33 ± 0.06 µm and L = 2.3 ± 0.4 µm, and the corresponding aspect ratio (a/L) = 0.14 ± 0.05.

The chemicals employed (supplied by Sigma-Aldrich, USA) in the synthesis of the composite bentonite–magnetite particles were FeCl₃·6H₂O (98%), NH₄OH aqueous solution (25% NH₃) and FeCl₂·4H₂O (98%). For the preparation of the alginate hydrogels the reagents used, without further purification, were sodium alginate (Across Organics, USA, Sigma-Aldrich CAS number 9005-38-3), CaCl₂ (anhydrous, minimum 96.0%, Sigma-Aldrich, USA), d-(+)-gluconic acid δ-lactone (GLD) (greater than 99.0%, Sigma-Aldrich, USA, CAS number 90-80-2) and CaCO₃ (Sigma-Aldrich). All the solutions and suspensions were prepared using Milli-Q quality deionized water (Milli-Q Academic, Millipore, France).

(b). Synthesis of the bentonite–magnetite particles and magnetite nanoparticles

The synthesis of the BMag composites was carried out, adapting a previous one reported in [24] for attapulgite–magnetite composites, as described by the following steps.

• (i)Preparation of bentonite suspension in Fe³⁺ aqueous solution: 4.410 g of FeCl₃·6H₂O was dissolved in 200 ml of deionized water. Then, 1.5 g of bentonite was dispersed in the Fe³⁺ solution using an ultrasonic bath for 30 min until a stable suspension was obtained. After that, the suspension was deoxygenated by bubbling nitrogen for 15 min. The flask was closed and the suspension was magnetically stirred overnight.
• (ii)In the bentonite-Fe³⁺ suspension obtained in the previous step, we added 1.614 g of FeCl₂·4H₂O. This new suspension, containing Fe²⁺ ions in solution, was heated up to 90°C. After that, 6 ml of NH₄OH solution was added rapidly under stirring. Immediately, a black precipitate appeared as a result of the formation of magnetite particles. Then, the suspension was kept under mechanical stirring in nitrogen atmosphere at 90°C for 1 h. The resulting suspension was cooled down to room temperature.
• (iii)Finally, the BMag particles were washed. For this, the particles were settled using a powerful magnet. Then, the supernatant solution was discarded, and the particles redispersed in fresh water. This procedure was repeated until the conductivity of the supernatant was less than 20 µS cm⁻¹.

The synthesis of the magnetite nanoparticles was identical to that of the BMag particles, except for the following differences: in step (i) the Fe³⁺ solution did not contain bentonite particles; in step (iii) the repeated cycles of decantation/redispersion were carried out until the supernatant was at pH ≈ 7.

The sample notation with a brief description is included in table 1.

Table 1.

Description of the different samples (particles, suspensions and ferrogels) employed.

sample	composition
Bent	bentonite particles (purified by hydrocyclone process)
Fe3O4	magnetite nanoparticles
BMag	bare (non-functionalized) magnetite-covered bentonite particles
BMagF1	particles functionalized by dispersion of 1 g of ‘BMag’ particles in 50 ml of a 0.5% w/v solution of sodium alginate
BMagF2	similar to ‘BMagF1’ particles, but obtained by dispersion in a 2% w/v solution of sodium alginate
BMag, or BMagF1, or BMagF2 suspensions	suspensions of the different kinds of particles in aqueous media. Particle concentration 1% w/v (zeta potential measurements) or 10% w/v (rheology)
BMagF1 + X%Alg	ferrogel containing 10% w/v of functionalized particles (BMagF1) and X% w/v of sodium alginate in the pregel solution (X = 0.25, 0.5, 1, 2)
BMagF2 + X%Alg	entirely similar to ferrogel ‘BMagF1 + X%Alg’, but containing BMagF2 particles

(c). Preparation of the magnetic hydrogels

Previously to the preparation of the ferrogels, the BMag particles were functionalized by adsorption of alginate molecules. To this end, two different suspensions were prepared. In the first one, 1.0 g of BMag particles was dispersed into 50 ml of a solution containing 0.25 g (0.5% w/v) of sodium alginate. In the second one, 1.0 g of BMag particles was dispersed into 50 ml of a solution containing 1 g (2% w/v) of sodium alginate. After allowing 12 h for alginate adsorption on the particle surface, the particle were recuperated and washed following the procedure described in §2b, point (iii). (See sample notation in table 1).

The BMag particles, functionalized by alginate adsorption (samples BMagF1 and BMagF2), were employed for the preparation of ferrogels. For this purpose, we followed the next steps.

• (i)The magnetic particles were dispersed in four different solutions of sodium alginate. In all these pregel suspensions, the particle concentration was 10% w/v and the alginate concentrations were 0.25, 0.5, 1 and 2% w/v. These suspensions were shaken by hand until the suspensions were homogeneous.
• (ii)After that, 22.5 mg of CaCO₃ and 26.7 mg of gluconic acid (GLD) were added to each suspension and the resulting mixture was shaken by hand. The role played by GDL was the slow acidification of the aqueous solution, by hydrolysis of this weak organic acid, allowing the gradual liberation of calcium ions from the CaCO₃. This controlled reaction favoured the homogeneous cross-linking of the alginate molecules, avoiding the formation of thick lumps into the ferrogels.
• (iii)Finally, 4 h after the start of the previous step, the gelation process was completed by the addition of a solution of CaCl₂ (5 ml, 45 mM concentration). The ferrogel was left at rest overnight at room temperature. The addition of this CaCl₂ solution provoked the swelling and the saturation of the cross-linking (by Ca²⁺ diffusion). Thus, ferrogels with enough tautness for handling were obtained.

(d). Experimental methods

The X-ray diffraction patterns (XRD) of bentonite (Bent) and bentonite covered by magnetite particles (BMag) were obtained in a Philips X'Pert Pro diffractometer (PANalytical, The Netherlands) working on Kα monochromatic radiation of copper. In addition, the morphology of Bent and BMag particles was obtained by high-resolution scanning electron microscopy (Zeiss SUPRA40VP, USA).

Zeta potential measurements were carried out in a Malvern Zeta-Sizer Nano SZ (UK) at 25°C. For these measurements, different suspensions containing 1% w/v particle concentration of Fe₃O₄, Bent, BMag, BMagF1 and BMagF2 (table 1) in aqueous media (1 mM NaCl ionic strength; pH interval from 3 to 10) were prepared. These suspensions were left at rest for 24 h. To avoid the effect of particle sedimentation, the samples were redispersed in an ultrasound bath, and the pH readjusted, immediately before the measurements. The values reported correspond to the average ± standard deviation of at least nine measurements of different aliquots.

The magnetization of the dry powder of BMag particles was measured at room temperature in a VSM 4500 magnetometer (EG&G Princeton Applied Research, USA), by applying the following magnetic field intensity (H) sequence: 0–374 kA m⁻¹ (first magnetization), followed by the cycle (magnetization loop) 374–0–(–374)–0–374 kA m⁻¹.

The rheological characterization of the suspensions and ferrogels was carried out in the presence and the absence of applied magnetic field in a magnetorheometer (Physica Anton-Paar MCR 300, Germany) with a plate–plate geometry (rotor plate diameter 20 mm) at constant temperature of 25.0 ± 0.1°C. The plates had a rough surface to avoid wall slipping. The magnetic applied field (intensity H = 156 kA m⁻¹ or 282 kA m⁻¹) was perpendicular to the rheometer plates. The samples were placed in the bottom plate and a normal force of 0.1 N was kept on the disc-like samples to ensure a good contact among plates and samples; the gap between the plates was slightly different for different samples, in order to maintain this value of the normal force. A water vapour saturated atmosphere was maintained around the samples to minimize their drying. Furthermore, in order to ensure the same initial conditions, a fresh sample was employed in each measure and, in the case of the suspensions of BMag particles for minimizing the possible effect of particle sedimentation, the samples were strongly redispersed before the measurements.

The viscoelastic moduli of the suspensions and hydrogels were obtained by application of an oscillatory (sinusoidal) shear stress to the samples and the subsequent measurement of the corresponding shear strain. In all these experiments, the frequency was maintained at 1 Hz, and the shear stress amplitude was progressively increased until the nonlinear viscoelastic region was reached. The time elapsed in each stress step was 5 s. From the values of the stress and strain amplitudes and the phase difference between shear and strain, the elastic or storage (G′) and viscous or loss (G^″) moduli were obtained. These oscillatory measurements were performed under constant magnetic applied field (H = 0; or H = 156 kA m⁻¹; or H = 282 kA m⁻¹) during the total duration of the experiment. These field values do not correspond exactly to the internal field in the sample in the rheometer gap, but taking into account the relatively small particle volume fraction in the suspensions and ferrogels (4.05% v/v; see §3b), and consequently the small demagnetizing fields, both the internal and the external fields are expected to be approximately equal.

3. Results and discussion

(a). Physico-chemical characterization

The XRD of the particles in samples Bent, BMag and Fe₃O₄ (table 1) are represented in figure 1. For the Fe₃O₄ sample, the peaks at diffraction angles 2θ = 18.27°, 30.09°, 35.49°, 43.05°, 53.48°, 56.94° and 62.72° correspond to the planes (111), (220), (311), (400), (442), (511) and (440) in the crystal lattice of pure magnetite. In the BMag sample the peaks of pure magnetite remained the same and also peaks of the bentonite core appeared at 2θ = 26.64° and 19.85°. Nevertheless, these peaks become wider and their intensity was reduced as compared with those in pure bentonite likely to be due to the (at least partial) coating by magnetite nanoparticles present in the BMag composites. Note that this technique does not allow distinguishing between magnetite and maghemite phases and, therefore, the presence of maghemite phase in the BMag particles cannot be excluded.

Figure 1.

XRD patterns of bentonite (Bent), magnetite-covered bentonite (Bent/Fe₃O₄) and magnetite particles. (Online version in colour.)

The morphology of the composite particles can be seen in the SEM pictures of figure 2. The bentonite particles (figure 2a) appeared as twisted and stacked platelets with a great polydispersity in size. Figure 2b shows the BMag particles and, as observed, the primitive clay clusters exhibited a partial coverage by small (around 100–200 nm) bright spots. These tiny spots correspond to magnetite nanoparticles grown onto the clay surfaces, probably because the clay mesopores (remember that bentonite-specific surface area was 70 m² g⁻¹) acted as seeds that promoted the precipitation of magnetite during the synthesis process.

Figure 2.

Pictures obtained by SEM of Bent (a), and BMag (b) particles. Scale bar, 1 µm.

The zeta potential of the different particles (Fe₃O₄, Bent, BMag composites, and the functionalized BMagF1 and BMagF2), as a function of the pH of the aqueous medium, is plotted in figure 3. The zeta potential of the magnetite particles presented an isoelectric point at pH(iep) ≈ 6.5, which is in good agreement with those values previously reported in the literature [25,26] for magnetite nanoparticles obtained by coprecipitation. The zeta potential curve of bentonite particles follows the typical trend of smectite clays (bentonite or montmorillonite; sepiolite) and silica particles [13,25–29], that is the particles bear a negative surface charge (and negative zeta potential) in the entire pH range under study. In the case of the non-functionalized composite particles (sample BMag), the tendency observed is coherent with a surface electrochemistry that combines those of Bent and Fe₃O₄ samples. Note that the surface reactions that determine the zeta potential of these materials (magnetite, bentonite, clay–magnetite) have been summarized in our previous work [13]. The adsorption of the dissociated alginate molecules provoked a clear increase (in absolute value) of the zeta potential of the BMag substrate, more pronounced as the concentration of alginate in solution was increased, as shown in figure 3 in the curves for BMagF1 and BMagF2 suspensions. This effect is a consequence of the surface reactions, via formation of coordination compounds, among the carboxylate groups of the alginate ligands and the Fe(II), Fe (III) and Si(IV) cations in the particles surface. Really, these metal (M = Fe or Si) ions are present in the solid–solution interface as M–O^– (basic pH), M–O–H (neutral pH) or M–O–H₂⁺ (acid pH) and the alginate adsorption is even more favoured at acid pH by electrostatic attraction between the alginate molecules and the M–O–H₂⁺ group. The formation of these surface alginate complexes on magnetite or bentonite particles have been extensively studied [30,31], and similarly for other polyelectrolytes that also bear carboxylate groups (e.g. humic acids) on clay or haematite particles [30,31].

Figure 3.

Zeta potential of the indicated particles in aqueous suspensions (table 1) as a function of the pH of the aqueous medium. Particle concentration 1% w/v. Ionic strength of the solutions 1 mM NaCl. (Online version in colour.)

The negative zeta potential of the functionalized particles has an additional advantage on the colloidal stability of the suspensions. As demonstrated in a previous work [25], the bentonite–magnetite platelets in aqueous suspensions suffer of a high degree of aggregation because the van der Waals attraction between the particles faces overcomes the electrostatic repulsion between them. In consequence, the particles of the present work formed stacked clusters and settled by gravitational forces. However, if the particles were functionalized by alginate adsorption, the electro-steric repulsion avoided in a high extent their aggregation and the subsequent fast sedimentation. Figure 4 shows the sedimentation of the bare and functionalized particles over one week, demonstrating that the settling of the bare (BMag) particles was considerably slowed by alginate adsorption (BMagF1, BMagF2 samples). As mentioned in §2d, to minimize the effect of the sedimentation, all the samples were strongly redispersed immediately before carrying the zeta potential and rheological measurements, which in any case took only a few minutes.

Figure 4.

Sedimentation of the suspensions of bare (BMag) and functionalized (BMagF1, BMagF2) composite particles. The indicated times correspond to those elapsed after placing the samples in the testing tubes (immediately before the samples were strongly redispersed). Particle concentration 1% w/v. Ionic strength of the solutions 1 mM NaCl. (Online version in colour.)

Figure 5 shows the magnetic response of the BMag particles (dry powder) when a magnetic field cycle is applied (figure 5a). As observed, the composite BMag particles developed strong enough magnetization. The saturation magnetization can be obtained by fitting the data in the first magnetization curve (figure 5b) to the Frölich–Kennely equation [32]:

$$M=\frac{\chi M_{S}H}{M_S+\chi H},$$ 3.1

where χ is the magnetic susceptibility and M_S the saturation magnetization. Their estimated values are χ = 3.90 ± 0.05 and M_S = 110.0 ± 0.3 kA m⁻¹; coefficient of determination r² = 0.995. Considering the saturation magnetization of pure magnetite (M_S,m = 446 kA m⁻¹ [33]) and the mixing law [34]:

$$M_S=\varphi M_{S,m},$$ 3.2

the estimated volume fraction (ϕ) of magnetic material in the BMag composite particles was ϕ = 24.7%. Taking for the density of bentonite and magnetite 2.1 g cm⁻³ and 5.5 g cm⁻³, respectively, the average density of the BMag particles was 2.5 g cm⁻³. In addition, the data in figure 5 demonstrate that the powder behaved as a magnetically soft material because the magnetic hysteresis was negligible given that the remnant magnetization and the coercive field (M_R = 0.45 kA m⁻¹ and H_C = −0.08 kA m⁻¹, respectively) are within the typical measurement error of the VSM magnetometer.

Figure 5.

(a) Magnetization loop of magnetite-covered bentonite particles (sample BMag). (b) First magnetization curve of BMag powder; the red line fits to the Frölich–Kennely equation (equation (3.1)). (Online version in colour.)

(b). Rheological characterization

The viscoelastic moduli for both the suspension of non-functionalized particles (BMag) and the different ferrogels prepared were obtained by applying a sinusoidal shear stress (oscillatory regime). All the samples studied contained a particle concentration of 10% w/v, equivalent to a particle volume fraction ϕ = 4.05% v/v. During the experiments, a stationary and homogeneous external field was applied to the samples with magnetic intensities H = 0, or H = 156 kA m⁻¹ or H = 282 kA m⁻¹. Figure 6 shows the results corresponding to the suspension of BMag particles. In this figure, we can clearly observe, whatever the applied field, two different regions: an initial psedoplateau, in which G′ is practically independent of the strain amplitude (γ₀) that corresponds to the linear viscoelastic region (LVR), followed by a second region (non-LVR) in which G′ suffers an abrupt decrease. In the first region, G′ is larger than G^″ and corresponds to a typical viscoelastic solid. In the second region (non-LVR), as γ₀ increases, there is a progressive transition from a viscoelastic solid to a liquid one (G^″ > G′). The critical point for this transition can be clearly identified, in the curves for H ≠ 0, at the critical strain in which G^″ reaches its maximum value at γ₀ ≈ 0.6 (or 60%). This point corresponds to the breaking of the internal microstructure of the suspensions, because at this point the mechanical forces corresponding to the shear applied overcome the magnetic attraction among the particles and rapidly the material loses its elastic response (G′ decreases), which favours the subsequent viscous flow of the suspension (increment in G^″).

Figure 6.

Viscoelastic moduli as a function of the strain amplitude of the aqueous suspension of BMag particles in the absence/presence of the indicated magnetic fields (H). Particle concentration 10% w/v. Solid symbols: elastic modulus, G′; open symbols: viscous modulus, G^″. (Online version in colour.)

The magnetic field-induced enhancement of the G′ values within the LVR (the so-called magnetorheological effect, MRE) can be quantified by the equation

$$\text{MRE }(\mathrm{\%})=\frac{G^{\mathrm{\prime }}(H\ne 0)-G^{\mathrm{\prime }}(H=0)}{G^{\mathrm{\prime }}(H=0)}\times 100.$$ 3.3

Table 2 includes the values of MRE (%) for the two values of the applied field to this suspension: 76 100% (at H = 156 kA m⁻¹) and 197 200% (at H = 282 kA m⁻¹), which are enormous in comparison with those usually reached in ferrogels as we will see below. Nevertheless, the quantification of the MR effect by equation (3.3) does not seem appropriate for nearly liquid-like suspension that in the absence of field has a very low elastic modulus (G′ ∼ 10 Pa). A more convenient quantification of the MR effect can be done considering the plastic viscosity (η) of the suspensions in the absence/presence of applied field, by means of

$$\text{MRE}-\eta \hspace{0.17em}(\mathrm{\%})=\frac{\eta (H\ne 0)-\eta (H=0)}{\eta (H=0)}\times 100.$$ 3.4

Table 2.

Intensity of the MRE quantified by means of equations (3.3) and (3.4) for the suspension, and equation (3.3) for the ferrogels. The plastic viscosities (η) of the suspensions are given in mPa·s. The G′ (Pa) values correspond to a strain amplitude of 0.1 (10%).

	magnetic field intensity
	H = 0 kA m−1	H = 156 kA m−1			H = 282 kA m−1
sample	η(0)	η(H)	Δη	MRE-η(%)	η(H)	Δη	MRE-η(%)
suspension BMag particles (equation (3.4))	90	94	4	4	168	78	87
	G′	G′	ΔG′	MRE(%)	G′	ΔG′	MRE(%)
suspension BMag particles (equation (3.3))	11	8380	8369	76 100	21 700	21 689	197 200
ferrogel BMagF2 + 0.25%Alg	915	1687	772	84	2442	1527	167
ferrogel BMagF2 + 0.5%Alg	920	2585	1665	181	5708	4788	520
ferrogel BMagF2 + 1%Alg	8187	8501	323	4	9929	1751	21
ferrogel BMagF2 + 2%Alg	39 310	41 020	1710	4	43 920	4610	12

The plastic viscosities were obtained from the slope of the rheograms (shear stress versus shear rate curves, not shown for brevity) by linear fitting in the shear rate interval from 1 to 50 s⁻¹. The values of the plastic viscosity and the corresponding MR effect calculated by equation (3.4) are included in table 1. Now, the MRE-η value reached for the maximum field is 87%, which appears a more reasonable estimation.

For the ferrogels prepared in this work, first we will analyse the viscoelastic behaviour in the absence of magnetic field. In figure 7, the values of the viscoelastic moduli are plotted as a function of γ₀. Figure 7a includes the results for the samples BMagF1 + X%Alg that contains 10% w/v of functionalized particles (BMagF1) embedded in hydrogels prepared with increasing concentrations of alginate (from 0.25 to 2% w/v alginate; table 1) in the pregel solution. From figure 7a, the pronounced effect of the alginate concentration on the mechanical properties of the resulting hydrogels seems evident. The increase of the alginate concentration from 0.25 to 2% w/v provoked an increase in the G′ values corresponding to the LVR (see solid symbols in figure 7a) of around two orders of magnitude. For the BMag particles functionalized with a larger amount of adsorbed alginate, the viscoelastic moduli of all the ferrogels (samples BMagF2 + X%Alg, figure 7b) are even higher: see the exact values of G′ for these samples in table 2.

Figure 7.

Viscoelastic moduli, in the absence of magnetic field, as a function of the strain amplitude for the different hydrogels prepared. (a) Hydrogels BMagF1 + X%Alg (table 1). (b) Hydrogels BMagF2 + X%Alg (table 1). Solid symbols: G′; open symbols: G^″. (Online version in colour.)

Therefore, up to this point we have two different mechanisms to control the mechanical moduli of the ferrogels: the amount of alginate adsorbed on the particles and the concentration of alginate in the pregel solution. This behaviour can be explained considering, as demonstrated in a previous work [13], the cross-linking (by calcium ions) among the alginate molecules adsorbed onto the particles and those present in the pregel solution, which favours the networking among the particles and the polymer fibres. As a consequence, the resulting ferrogels consist of a network of alginate fibres in which the magnetic particles are not only randomly dispersed but act as knots that reinforce the elasticity of the material.

A third mechanism, as for MR suspensions, is the action of an external magnetic field of enough intensity. In this work, the applied fields were H = 156 kA m⁻¹ and H = 282 kA m⁻¹, both of them below (but not too far) the field required to reach the magnetic saturation of the particles; see in figure 5 that the field intensity for the maximum magnetization is above H = 400 kA m⁻¹.

In figure 8, we plotted the viscoelastic moduli of the samples BMagF2 + 0.25%Alg (figure 8a) and BMagF2 + 2%Alg (figure 8b) for the different applied fields. As observed (see also table 2), for the weakest ferrogel (0.25% alginate) there is a significant effect of the field-induced attraction among the particles that gave MRE values (equation (3.3)) of 84% (H = 156 kA m⁻¹) and 167% (H = 282 kA m⁻¹). On the contrary, the values of MRE (%) are considerably smaller for the most concentrated hydrogel (BMagF₂  +  2%Alg, table 2) in which MRE (%) are 4% and 12% for H = 156 kA m⁻¹ and H = 282 kA m⁻¹, respectively. In this case, the curves obtained for different applied fields tend to collapse (figure 8b).

Figure 8.

Viscoelastic moduli as a function of the strain amplitude of hydrogels BMagF2 + X%Alg (table 1). (a) Sample BMagF2 + 0.25%Alg. (b) Sample BMagF2 + 2%Alg. The values of the magnetic applied field are indicated. Solid symbols: elastic modulus, G′; open symbols: viscous modulus, G^″. (Online version in colour.)

Nevertheless, the data in table 2 show that the maximum MRE was reached for an intermediate value of the alginate concentration (sample BMagF2 + 0.5%Alg) with MRE values of 181% (H = 156 kA m⁻¹) and 520% (H = 156 kA m⁻¹). For this sample, the polymer network seems to be still weak enough to allow a strong field-induced reinforcement of the ferrogel.

In summary, the application of an external magnetic field allows a strong MR effect only if the hydrogel network is not too dense. However, if the particles are entangled in a highly concentrated hydrogel their field-induced approaching is practically hindered and the deformation of the ferrogel mainly depends on the resilience of the polymer–particles network, being negligible the role played by the magnetic interactions.

Finally, it is convenient to analyse the influence of the shape of the magnetic particles on the magnetic control of the rheological properties of the ferrogels. Thus, we have to separate the shape effect from other quantities such as the particle concentration, the intensity of the field and the magnetization of the particles. For this purpose, we can consider that, according to the MR model proposed by Ginder et al. [35] (see also [36]), the shear modulus depends linearly on the applied field (H), the particle volume fraction (Φ) and the particle saturation magnetization (M_S). Although this model is based on a number of restrictive assumptions (particle volume fraction Φ < 20% – 30%; linear field-induced chaining of spherical particles; intermediate field, well below the field for saturation magnetization; very low strain), it is useful to define a normalized MR effect parameter following this model:

$$\overline{\text{MRE}}(\mathrm{\%})=(\text{MRE})\hspace{0.17em}(\mathrm{\%})\frac{M_{S,0}}{M_S}\frac{H_0}{H}\frac{{\mathrm{\Phi }}_0}{\mathrm{\Phi }}.$$ 3.5

Here the quantities H, M_S and Φ corresponds to those of the ferrogels studied in [13,16,37] and the quantities with subscript ‘0’ correspond to the ferrogel BMagF2 + 0.5%Alg prepared in this work. All these data are included in table 3.

Table 3.

Comparison among the MREs, calculated by equations (3.3) and (3.5), achieved by ferrogels that contain particles with different shapes and compositions.

ferrogel (reference)	composition (particle shell–core/polymer in hydrogel)	MS (kA m−1)	H (kA m−1)	Φ (% v/v)	MRE (%)	$\overline{\mathrm{MRE}}(\mathrm{\%})$
BMagF2 + 0.5% Alg	platelets Fe3O4-bentonite/ alginate (0.5% w/v)	110a	282a	4.05a	520	520
ferrogel BMagF2 + 1% Alg	platelets Fe3O4-bentonite/ alginate (1% w/v)b	110a	282a	4.05a	21	21
ferrogel-1 [13]	fibre-like Fe3O4-sepiolite/ alginate (1% w/v)b	169.9	282	0.93	64	180
ferrogel [16]c	spherical silica-Fe/ alginate (1% w/v)b	1587	282	4.6	700	43
ferrogel [37]c	spherical polymer-Fe3O4/ fibrin-agarose	161	48.6	3.5	8	37

^aM_S,0, H_max,0, Φ₀ in equation (3.5).

^bAlginate concentration in pregel solution 1% w/v.

^cSee also ref. [13].

The data in tables 2 and 3 demonstrate that

• (i)The ferrogels prepared with plate-like magnetic particles (bentonite–magnetite) can provide a very high MR effect when the alginate concentration was not too high. The maximum field effect (MRE = 520%) is achieved at 0.5% w/v alginate concentration in the pregel solution.
• (ii)The alginate concentration in the pregel solution determines in a great extent (and allows a wide control of) the MRE values achieved in the ferrogels containing functionalized magnetic platelets.
• (iii)If we compare ferrogels containing particles with different shapes (bentonite–magnetite platelets, sepiolite–magnetite fibres, silica–iron spheres) and equal alginate concentration (1% w/v) in the pregel solution, the maximum field effect corresponds to those with fibre-like composite particles. The normalized MRE values are: 21% (platelets), 180% (fibres) and 43% (spheres).

4. Conclusion

Hydrogels containing biocompatible polymer fibres and magnetic micro- or nanoparticles are very promising soft–wet materials for biomedical applications, because their internal microstructure can work as patterns (or extracellular matrix or scaffolds, in the terminology used in tissue engineering) for generating soft biological tissues. The configuration of such internal structure depends on a number of variables that allows controlling their macroscopic properties as the mechanical moduli and the hydration degree. These variables are mainly (i) the length and cross-linking degree of the polymer fibres; (ii) the cross-linking degree among the polymer fibres and the molecules adsorbed onto the solid particles; (iii) the kind of bond (covalent, electrostatic) between the cross-linker and the polymer molecules; (iv) the volume fraction of solid particles embedded into the hydrogel; (v) the magnetic properties of the particles; and (vi) the intensity of the applied magnetic field.

In this work, the cross-linker agent employed was calcium ions and the interaction among the alginate molecules was electrostatic. This physical cross-linking favoured the formation of soft and easy to handle hydrogels, the elasticity of which can be controlled in a wide range by varying the alginate concentration in the pregel solution. Even more, when the particles were functionalized by adsorption of alginate molecules onto the particle surface, the solid particles occupied the knots of the internal network, so avoiding the settling of the particles inside the gel. Simultaneously, this particle–polymer networking reinforced the mechanical response of the gel under the action of mechanical stresses.

The magnetic particles embedded in the hydrogels prepared in this work were composites of bentonite platelets on which magnetite nanoparticles were synthetized by a coprecipitation reaction. These composite particles were functionalized by adsorption of alginate molecules and the resulting particles had low density and, consequently, negligible settling rate inside the pregel solution. This fact allowed homogeneous ferrogels with a high enough MRE to be obtained. Nevertheless, the intensity of that MR effect strongly depended on the concentration of sodium alginate employed for the preparation of the pregel solution, being the optimal concentration 0.5% w/v.

The comparison of the ferrogels based on magnetic particles with different shapes and the same alginate concentration—normalizing other quantities as particle concentration, applied field and magnetization—demonstrated that the more intense MR effect was achieved with fibre-like particles. The MR effect attained for spherical and plate-like particle ferrogels were of same order of magnitude, possibly because some stacked clay clusters remained, in spite of the electro-steric stabilization imparted by the adsorbed alginate molecules. However, the use of magnetic composites based on clay minerals has the advantage, in comparison with spherical particles of pure magnetite or iron, of avoiding the settling of the particles inside the pregel suspension, so providing ferrogels with high homogeneity. And this property (homogeneity) is an essential condition for the generation of good artificial tissues that mimic the native ones by cell culture inside biocompatible hydrogels.

Data accessibility

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Authors' contributions

M.M.A. has carried out the synthesis of the composite particles, all the experimental measurements, and the treatment of the data. She wrote the first draft of the manuscript.

E.S. supervised and supported a part of the work made by M.M.A.: bentonite purification, synthesis of bentonite–magnetite particles and particles characterization (zeta potential measurements; X-ray spectra).

M.T.L.-L. planned (with J.D.G.D.) and supervised the work made by M.M.A., specially the preparation of the ferrogels, and their rheological and magnetic characterization. He also revised the final draft of the manuscript.

J.D.G.D. planned and supervised the entire work included in the paper. He wrote the final version of the manuscript.

Competing interests

We declare we have no competing interests.

Funding

This study was supported by project no. FIS2017-85954-R (Ministerio de Economía, Industria y Competitividad, MINECO, and Agencia Estatal de Investigación, AEI, Spain, cofunded by Fondo Europeo de Desarrollo Regional, FEDER, European Union).