Strong and tough fibrous hydrogels reinforced by multiscale hierarchical structures with multimechanisms

Abstract

Tough natural materials such as nacre, bone, and silk exhibit multiscale hierarchical structures where distinct toughening mechanisms occur at each level of the hierarchy, ranging from molecular uncoiling to microscale fibrillar sliding to macroscale crack deflection. An open question is whether and how the multiscale design motifs of natural materials can be translated to the development of next-generation biomimetic hydrogels. To address this challenge, we fabricate strong and tough hydrogel with architected multiscale hierarchical structures using a freeze-casting–assisted solution substitution strategy. The underlying multiscale multimechanisms are attributed to the gel’s hierarchical structures, including microscale anisotropic honeycomb–structured fiber walls and matrix, with a modulus of 8.96 and 0.73 MPa, respectively; hydrogen bond–enhanced fibers with nanocrystalline domains; and cross-linked strong polyvinyl alcohol chains with chain-connecting ionic bonds. This study establishes a blueprint of structure-performance mechanisms in tough hierarchically structured hydrogels and can inspire advanced design strategies for other promising hierarchical materials.

Multiscale simulation and characterization reveal multiple reinforcement mechanisms in hierarchically structured tough hydrogels.

INTRODUCTION

Hydrogels have excellent potential as advanced engineering materials for wearable electronics (1, 2), tissue engineering (3), soft robotics (4, 5), and biomedical engineering (6). However, conventional hydrogels are generally weak and fragile (7), which substantially limits their applications. In the last decade, many efforts have been devoted to developing enhanced hydrogels with excellent mechanical properties, such as topological hydrogels (8), nanocomposite hydrogels (9), double-network (DN) hydrogels (10), dual cross-linked hydrogels (11), and nanocrystalline hydrogels (12). However, these studies mainly focus on molecular engineering and composition, and the involved structural changes are limited to molecular scale or nanoscale. For example, the rupture of the weak network and associated cross-links in a DN hydrogel can dissipate mechanical energy at the molecular level, which can effectively enhance toughness (13). At present, the toughness of even well-designed DN hydrogels hardly exceeds 10 MJ/m³. To further enhance the strength and toughness of hydrogels, it will be meaningful to construct more advanced designs by exploring toughening mechanisms over a wider range of length scales.

Natural hydrogels, which typically exhibit superior strength and toughness, are abundant in various plant and animal tissues, including xylems, phloems, muscles, and cartilages (14). This is attributed to their unique hierarchical structures, which range from microscopic anisotropic alignments to distinctive crystalline units at the molecular scale, resulting in synergistic strengthening and toughening of the overall materials. Inspired by this, biomimetic hydrogels with anisotropic multiscale hierarchical structures have been proven to have excellent mechanical performances (15). Moreover, several kinds of anisotropic hydrogels with improved mechanical properties have been developed by mechanical training (16, 17), additional fillers (18, 19), and freeze-casting (20, 21). For example, muscle-like fatigue-resistant hydrogels with directionally aligned nanofibrillar structures were obtained via mechanical training (17). Although the mechanically trained hydrogels showed enhanced strength and fracture toughness compared to untrained hydrogels, their water content and stretchability were substantially reduced. As for freeze-casting, it is a general method for fabricating anisotropic hydrogels. However, once freeze-thawed hydrogels with initial microscopic alignment exhibit limited mechanical properties and generally need to be further enhanced by postprocessing (22). These hydrogels exhibited somewhat improved mechanical properties with anisotropically aligned structures at a single scale but showed a conflict between strength and stretchability due to the lack of multiscale hierarchical structures. At this point, the fabrication of stretchable and tough hydrogels with hierarchical structures across multiple length scales from micro-, nano-, and molecular levels remains challenging.

Recently, a design principle of simultaneously enhancing stretch, strength, and toughness has been proposed and demonstrated for hierarchical fiber-reinforced hydrogels, including microlevel fiber anisotropic alignment, nanoscale fiber aggregation, and molecular-scale fiber reinforcement (23). For example, combining unidirectional freeze-casting and salting-out (24), a single-composition fibrous hydrogel exhibited unique stepwise fracture behavior and crack propagation blocking ability, resulting in superior mechanical properties coupled with high strength and toughness. Furthermore, a number of tough and functional fibrous hydrogels have been fabricated through a combination of freeze-casting with other procedures, such as ion enhancement (25), solution replacement (26), and annealing (15, 27). A universal design strategy of ice-templating and subsequent thermal annealing has been proposed with impressive enhancement in fiber crystallinity, fracture energy, and fatigue threshold (27). These fibrous hydrogels combined the advantages of hierarchical structural engineering and molecular engineering, achieving simultaneously improved stretchability, strength, and toughness, as well as functionalities such as conductivity and freezing tolerance.

While these successes of introducing hierarchical structures in fibrous hydrogels have been characterized at different length scales, the current development of fibrous hydrogels has mainly depended on trial-and-error and empirical methods. The intrinsic mechanisms at micro-, nano-, and molecular levels for improving modulus, stretchability, and toughness in fibrous hydrogels have not been systematically explored and discussed. This greatly restricts the advanced design strategies and engineering application of biomimetic hydrogels. Here, we propose a freeze-casting–assisted solution substitution strategy to fabricate strong and tough fibrous hydrogels with hierarchical structures from molecular to micrometer scales. This is achieved by immersing the directional frozen polyvinyl alcohol (PVA) ice blocks into an ethanol solution with the addition of ferric chloride. Tensile and pure shear tests are performed to experimentally investigate their mechanical and fracture performance. We further combine experimental characterization with theoretical simulations to understand the underlying strengthening and toughening mechanisms at each length scale. At the microscopic level, representative volume element (RVE) analysis coupled with periodic boundary conditions (PBCs) (28, 29) is carried out to characterize the mechanical behavior and elastic properties of the anisotropic fibrous hydrogel. Atomistic-level simulations are conducted using Materials Studio (30) to explore the molecular mechanical behavior of PVA hydrogels and the effect of ethanol substitution and Fe³⁺ on intramolecular interactions between the PVA chains and water molecules. This approach allows the multiscale multimechanisms of fibrous hydrogels to be systematically characterized through an integrated experiment-simulation approach. Our study demonstrates an effective design and analysis strategy for strong and tough fibrous hydrogels with hierarchical structures and multiple enhancement mechanisms. In addition, the developed theoretical and simulation modeling framework can be applied to other artificial hydrogel systems and even natural materials.

RESULTS

Formation of hierarchical structures

Figure 1A illustrates the adopted fabrication process of fibrous hydrogels with anisotropic hierarchical structures across multiple length scales. A PVA solution [10 weight % (wt %)] was first unidirectionally frozen at −80°C with a vertical temperature gradient where ice pillars were growing. The resulting phase separation in the PVA solution with the aid of ice pillars facilitated an initial concentration of the PVA phase and promoted entanglement of long PVA chains. Meanwhile, hydrogen bonds were established between the hydroxyl groups on the concentrated PVA chains. This then led to the formation of a honeycomb-like microstructure with aligned pores and polymer walls after the unidirectional freeze-casting, with high amorphousness and low crystallinity. Subsequently, more concentrated and closer packing of polymer chains with high-crystallinity nanocrystalline domains (12) and high-functionality cross-links was achieved via solvent substitution and ion enhancement. After freeze-casting, the frozen PVA block was immersed in an ethanolic ferric chloride solution (2 wt %) and stored at −10°C until the solution substitution was completed. In the process, the ice phase dissolved in the ethanol solution stabilizes the micromorphology of the hydrogel (31), resulting in forming more hydrogen bonds between PVA chains subjected to the hydrophobic aggregation of ethanol molecules. As a result, the PVA chains became more aggregated and entangled, transforming from an amorphous phase to a crystalline phase with a higher cross-linking degree (32). Meanwhile, the iron-oxygen coordination reactions between free Fe³⁺ and the hydroxyl groups on PVA polymer chains further increased the cross-linking of the chains (33). As shown in Fig. 1B, high crystallinity fibrous hydrogels with anisotropic hierarchical structures were formed, denoted as FC-EtFe. As can be seen in Fig. 1B (i and ii), the fibrous hydrogels are mesoscopically anisotropic in orientation. At the microscale, the freeze-dried hydrogel sample exhibits a honeycomb skeleton micromorphology and amorphous dependence features, corresponding to the formation of a modulus-contrasting microstructure consisting of a soft amorphous matrix and hard honeycomb walls. The nanoscale aggregation network observed on the wall surface in Fig. 1Biii illustrates that the hard walls were further enhanced by the high aggregation and crystallization of polymers induced by solution hydrophobic aggregation and coordination reactions, while molecular-level crystalline domains, hydrogen bonding, and ligand bonding were illustrated schematically in Fig. 1B (iv and v).

Fig. 1. Fabrication and hierarchical structures of tough fibrous hydrogels.

(A) Schematic diagrams of the freeze-casting–assisted solution substitution strategy of the PVA hydrogel (FC-EtFe). (B) Hierarchical structures of the fabricated hydrogel. (i) Macroscopic view of FC-EtFe. (ii and iii) Scanning electron microscopy (SEM) image of the micro- and nanostructure. (iv) Aggregated polymer chains with nanocrystalline domains. (v) Illustration of the interactions of polymer chains.

Experimental testing of fibrous hydrogels

The macromechanical behaviors of the PVA hydrogels were conducted on a universal stretching machine, and for comparison, two other types of hydrogels were also prepared: (i) once freeze-thawed hydrogel (FC-1T) and (ii) substituted hydrogel with pure ethanol as the substitution solvent (FC-Et). As shown in Fig. 2A, the FC-EtFe exhibited an impressive mechanical response loaded in the direction parallel to the ice pillar growth, with a greatly enhanced strength of 7.11 MPa and prolonged fracture strain of up to 1623%. In particular, the hydrogel showed a typical gradual failure mode of anisotropic fibrous materials with fracture and fiber pullout (Fig. 2A, i and ii). Notably, the strength of FC-EtFe was 5.1 times that of FC-Et (1.40 MPa) and 64.6 times that of FC-1T (0.11 MPa). As illustrated in Fig. 2B, the comparative mechanical properties of PVA hydrogels exhibited a remarkable uptrend with the process of ethanol substitution and subsequent Fe³⁺ ion enhancement, enhancing both strength and stretchability. Moreover, as shown in Fig. 2C, pure shear tests of both notched and unnotched PVA hydrogels were performed to investigate their fracture behavior. The notched FC-EtFe with a crack perpendicular to the fiber alignment exhibited a crack-pinning ability due to the aligned fibril structures (Fig. 2Cii). The observed crack insensitivity is consistent with that in highly aligned biological materials (34). Subsequently, the crack propagated with a substantial bridging zone of fibril tearing and fracturing (Fig. 2Ci). The tested toughness and work of fracture (see fig. S1) (35) of PVA hydrogels were compared in Fig. 2D. The FC-EtFe reached a superior toughness of 58.9 MJ/m³, which was 14.8 and 423.7 times that of FC-Et and FC-1T, respectively. Moreover, the tough FC-EtFe hydrogel showed excellent flaw-tolerant ability with both exceptional toughness and work to fracture.

Fig. 2. Experimental results on tough hydrogels.

(A) Tensile stress-strain curves of the tested hydrogels. (i and ii) SEM images of the fracturing and pulling-out zone of an FC-EtFe sample. (B) Average results of Young’s modulus, strength, and strain of the tested hydrogels. (C) Shearing stress-strain curves of notched and unnotched hydrogels. (i) SEM image of the crack propagation region. (ii) SEM image of the deformed microfiber. (D) Tested toughness and work to fracture of the hydrogels. (E) Differential scanning calorimetry (DSC) curves. (F) Calculated crystallinity. (G) Fourier transform infrared (FTIR) spectroscopy. Reproduced under Creative Commons Attribution License (25). Copyright 2022, Wiley-VCH.

Differential scanning calorimetry (DSC) and Fourier transform infrared (FTIR) spectroscopy tests were further conducted to characterize the crystallinity and functional groups of fibrous hydrogels. As shown in Fig. 2E, the endothermal peaks of the hydrogels in terms of glass transition (marked as T_g) and melting (marked as T_m) were highlighted. The glass transition of FC-1T occurred at 90°C and increased to 115°C after ethanol substitution. A gentle melting endothermal peak was also shown in FC-1T, and, by contrast, the peaks were stronger in FC-Et and FC-EtFe in that order, indicating that ethanol substitution significantly affected the crystallinity of hydrogels. As a result, the calculated crystallinity of hydrogels (see in Fig. 2F) exhibited an uptrend with the solution substitution, particularly the synergistic process of ethanol substitution and ionic enhancement. FC-EtFe exhibited the highest crystallinity of 13.77 wt %, with a remarkable increase of about 12-fold more than that of FC-1T. Moreover, Fig. 2G showed that the FTIR spectra of FC-Et and FC-EtFe were consistent with that of FC-1T, in terms of band shape and wave number, indicating that the main functional group has not been changed. In the meantime, the intensity of band peaks in FC-EtFe strongly outperformed that of FC-Et, and the corresponding value in FC-1T was the lowest at the same wave number. For example, the band peaks observed at 3291 cm⁻¹, referring to the stretching vibration of intermolecular and intramolecular hydrogen bonds (O─H), indicated that more hydrogen bonds were formed and PVA chains were more aggregated and crystallized with the ethanol substitution and addition of iron ions. Furthermore, by comparing the FTIR spectra of dried hydrogels with undried hydrogels (fig. S2), it could be shown that iron ions strongly bonded and maintained the PVA chains due to coordination reactions (33).

In summary, by mechanical analysis, FC-EtFe hydrogel exhibited super stretchability, high strength, and remarkable toughness. The excellent mechanical performance of FC-EtFe hydrogel has been attributed to its anisotropic hierarchical structures with high crystallinity, as demonstrated by microscopic and molecular characterizations, respectively. However, the underlying mechanisms have not been characterized. It is not clear what roles hierarchical structures, including anisotropic microscale honeycomb alignments, nanocrystalline domain, and molecular bonding, play in the mechanical performance. Therefore, on the basis of the experimental data and observations, the multiple strengthening and toughening mechanisms are further investigated via micro- and molecular-scale simulations.

Finite element analysis of the microscale elastic behavior of hydrogels

Currently reported bioinspired anisotropic materials (15–27) mostly focused on their mechanical behavior at the macrolevel. Here, we conducted the comprehensive study of the mechanical behavior of fibrous hydrogels across multiple length scales at macro, micro, and molecular levels. As discussed above, the high strength and toughness were mainly attributed to the highly anisotropic fibrous structure manifested as aligned micro-honeycomb walls (fig. S3). Therefore, in order to study the effect of ethanol substitution and Fe³⁺ enhancement on the stiffness of microfiber walls and the interaction effects between microfiber and matrix, RVE homogenization and finite element method (FEM) were combined to characterize the elastic behavior of the reinforced fiber walls.

Figure 3A displayed the predicted modulus of microfiber (E^f), the tested modulus of matrix (E^m; see in fig. S4), and that of the PVA hydrogels ($E_{11}^t$). The microfiber in FC-EtFe showed a noticeable modulus of 8.96 MPa, which was 81.45 and 6.68 times that of FC-Et and FC-1T, respectively. Of particular interest is that the modulus markedly increases after the addition of Fe³⁺. The results indicated that the ion enhancement led to more polymer chains aggregated due to the formation of coordination bonds and resulted in high crystallinity. As shown in Fig. 3C, the modulus contrast (m_c), corresponding to the modulus ratio between fiber and matrix (E^f/E^m), was deepened with the process of ethanol substitution and ion enhancement. Among them, the deepening effect on m_c was 5.58 in the context of the demonstrated enhancement of modulus by ethanol substitution, implying that the ethanol substitution process strengthened the PVA chains in the fiber walls and the matrix. In the meantime, the presence of Fe³⁺ greatly enhanced m_c up to 12.3. This indicated that the effect of ion enhancement was more obvious in fiber walls than in the matrix, where the denser distribution of functional groups in the fiber walls was available for coordination cross-linking. Figure 3D (i and ii) shows the stress distribution of microhydrogel and fiber walls in FC-EtFe, respectively. The stresses in microcomposite mainly depend on the fiber walls, with higher stresses in fiber than in the matrix. The stress distribution in the microfibers was relatively uniform due to the matrix with low modulus playing a role in transmitting stress. The stress distribution was also related to the modulus contrast, whereby the larger the m_c, the more uniform the stress distribution in fiber walls (fig. S5).

Fig. 3. Micromechanical composite modeling of hydrogels.

(A) Modulus of matrix, fiber, and hydrogels. (B) Poisson’s ratio of matrix, fiber, and hydrogels. (C) The modulus contrast between fiber and matrix. (D) The Mises stress distribution in microcomposite and fiber wall of the FC-EtFe. (E) The Poisson’s ratio contrast between fiber and matrix. (F) The stress component (s₂₂) distribution in microcomposite and fiber wall of the FC-EtFe.

As shown in Fig. 3B, the Poisson’s ratio of matrix (v^m), fiber walls (v^f), and corresponding hydrogels ($v_{12}^t$) all exhibited a downward trend with the process of ethanol substitution and ion enhancement. This indicates that the strengthened resistance to hydrogel transverse deformation led to more stable deformation while maintaining high loading capacities. The FC-EtFe and corresponding fiber walls showed a very low Poisson’s ratio of 0.028 and 0.013, respectively. Meanwhile, Fig. 3E displayed the Poisson’s ratio contrast (pr_c) between fiber walls and matrix (v^f/v^m). The pr_c of FC-1T was 0.675 and then markedly decreased to 0.363 with ethanol substitution and continued to decrease slightly to 0.325 with the addition of Fe³⁺. This demonstrated that the pr_c reached a stable value due to the ethanol substitution while simultaneously strengthening the resistance to deformation of fiber walls and matrix. Further FEM simulation analysis in Fig. 3F (i and ii) illustrated the distribution of stress component (s₂₂) in FC-EtFe and fiber walls, respectively. The microhydrogel withstood not only tension but also compression due to the Poisson’s ratio contrast between fiber walls and matrix, resulting in strongly coordinated deformation. The stress distribution of fiber walls was relatively nonuniform due to the interaction between the fiber walls and the matrix, where the fiber restricted the deformation of the matrix and further maintained the morphology of tough fibrous hydrogel. The lower the pr_c, the more nonuniform the stress distribution in fiber walls, and the more strengthened interaction effects in resistance to deformation (fig. S6). The numerical results were validated by comparing their stress-strain curves and Young’s modulus with those of corresponding experiments (fig. S7). In general, at the microscopic level, fibrous hydrogels’ mechanical behavior and strengthening mechanisms arose from the reinforced fiber walls and the enhanced matrix, as well as the synergistic interaction between them.

Molecular dynamics simulations of the strengthening and toughening mechanisms of PVA hydrogels

To further investigate the strengthening and toughening mechanisms in the FC-EtFe at the molecular level, molecular dynamics simulations were conducted using Materials Studio to study the influence of ethanol molecules and Fe³⁺ on the PVA interchain interactions. For the FC-1T model, we built a simulation box (fig. S8A) filled with two PVA chains and water molecules. Each polymer chain simulated in this study was polymerized by 30 PVA monomers as representatives. On the basis of this model, 200 ethanol molecules were added in the simulation box in the case of FC-Et (fig. S8B), and 200 ethanol molecules, 40 Fe³⁺, and 120 Cl⁻ were added for FC-EtFe (fig. S8C; molecular structure of this composition is shown in fig. S9). Figure 4A displayed the stress-strain curves of these PVA systems, where the FC-EtFe model exhibited the best mechanical response with simultaneous high stress and large strain. Figure 4B compared the stretch, stress, and work to fracture of these models, indicating the exceptional mechanical performance of FC-EtFe. For example, the work to fracture of the FC-EtFe model was significantly higher (~3.2 and 7.3 times) than that of the FC-1T and FC-Et, respectively. The simulation results are qualitatively consistent with the experimental results illustrated in Fig. 2B.

Fig. 4. Molecular dynamics simulations of the molecular-scale toughening mechanism of hydrogels.

(A) Stress-strain curves. (B) Simulation results of strength, strain, and work to fracture. (C) The stretching process of FC-EtFe. (D) Snapshots of interfacial interaction mechanism of FC-EtFe.

Figure 4C illustrates the stretching process of the FC-EtFe model. At the initial step, the PVA chains in FC-1T, FC-Et, and FC-EtFe showed different shapes of the PVA chains (see Fig. 4Ci and fig. S10, Bi and Ei) after the NPT ensemble, because the FC-EtFe model has more hydrogen bonds (see fig. S11) and higher crystallinity, thus more aggregated and entangled PVA chains than those of the FC-Et and FC-1T systems. As stretch increases, the aggregated area of PVA chains would stretch and extend to break. In the meantime, large numbers of hydrogen bonds and chain-connecting Fe bonds were broken and formed (see enlarged view in Fig. 4Ciii). Thus, the stress exhibited a rising trend with many fluctuations over a large strain range. It can be found that the stress was mainly dominated by the PVA chains and the intermolecular forces between PVA chains with water, ethanol, and Fe³⁺. At the end stage shown in Fig. 4Civ, the PVA chains were broken in many places and lost their load-bearing capacity. Meanwhile, water molecules, ethanol molecules, and Fe ions are dispersed farther, and the intermolecular forces markedly decreased. As a result, the longer, more aggregated PVA chains and the more strengthened intermolecular forces provide larger strain, higher stress, and dissipate more energy due to the breaking of large numbers of hydrogen bonds, PVA chains, and coordination Fe bonds. The stretching process of FC-1T and FC-Et (see in fig. S10, B and E, respectively) showed similar stretching modes in PVA chains and different intermolecular interaction behaviors when compared to those of FC-EtFe.

Figure S10 (C and F) and Fig. 4D plotted snapshots of the interfacial interaction between the polymer chains, water molecules, ethanol molecules, and Fe³⁺ in the hydrogels under investigation. In FC-1T, a number of hydrogen bonds were formed between PVA chains and water molecules, with relatively low bond energy before fracture (see in fig. S10C), resulting in very low stress and stretch to failure. Figure S10F showed more hydrogen bonds in FC-Et, due to the ethanol molecules providing ─OH-forming hydrogen bonds with PVA chains and water molecules. Therefore, the intermolecular forces increased, which strengthened the network of PVA chains and water molecules consistent with the microsimulation in Fig. 3 (A and B). The rupture of the involved hydrogen bonds resulted in an increase in stress and strain of the FC-Et model. Figure 4D illustrated the molecular mechanism of ion enhancement in the FC-EtFe model, in which Fe³⁺ ions bound the two PVA chains via the carbonyl oxygens, forming multiple chain-connecting Fe bonds. Figure 4Di showed the key interfacial behavior, in which the chain-connecting Fe bonds fractured, giving rise to higher stress and larger strain. This is mainly attributed to the chain-connecting Fe bonds restricting the separation of PVA chains and promoting the formation of more hydrogen bonds between polymer chains. In this process, the fracture of the chain-connecting Fe bonds and hydrogen bonds resulted in markedly increased energy dissipation. In addition, the water-connecting Fe bonds (see Fig. 4Dii) between Fe ions and water molecules also increased the intermolecular forces in the regions filled with water molecules. However, the energy dissipated by the breaking of water-connecting Fe bonds is limited, only slightly higher than that of breaking hydrogen bonds between water molecules (36). As a result, the ion enhancement had more significant strengthening effects on PVA chains than water molecules, consistent with microsimulation in Fig. 3 (A and B). In general, the main toughening mechanism was the formation of chain-connecting Fe bonds provided by the addition of Fe³⁺ ions, which facilitates the formation of hydrogen bonds between PVA chains, leading to the observed increase in stress and work to fracture.

Multiple strengthening and toughening mechanisms of fibrous hydrogels across multiscales

On the basis of the analysis of combined experiments and simulations, the super stretchability, high strength, and remarkable toughness of FC-EtFe hydrogel were simultaneously achieved because of its hierarchical structures at different length scales, which involved multiple strengthening and toughening mechanisms. As shown in Fig. 5A, the microhydrogel consisted of strong honeycomb walls and a soft matrix. During the stretching process, the fracture and pullout of the fibers dissipated mechanical energy in hydrogels and extended the deformation of the overall structure (see in Fig. 5B). Moreover, fibers were interwoven into three-dimensional honeycomb networks, which could maintain the elasticity and strength of hydrogel under deformation (37) by restricting deformation and transmitting stress due to the interactions between the microcellular wall and internal matrix (see in Fig. 5Bi). As shown in Fig. 5Bii, there were many polymer chains connected by entanglement and bonding as high-functionality cross-linkers, which resulted in the formation of nanocrystalline domains (38) and high crystallinity. Some chains may be fractured because of relatively weak bonding, while others with stronger cross-links were able to maintain the high strength and elasticity of hydrogels during deformation. Furthermore, an enormous number of hydrogen bonds were formed at the molecular scale by the compounding effects of freeze-casting concentration, ethanol aggregation, and high-energy chain-connecting Fe bond cross-linking. Therefore, during the fracture process, breaking these bonds dissipated tremendous amount of energy and guaranteed high strength and high stretchability of hydrogels (see Fig. 5Biii).

Fig. 5. Multiscale and multimechanisms of strong and tough fibrous hydrogels.

(A) Schematic of the microhydrogel subject to tension. (B) Stretched state of the microhydrogel. (i) The interactions of microfiber walls with the internal matrix. (ii) The rupture of PVA chains connecting with high-functionality cross-linkers. (iii) The interaction behavior of PVA chains. (C) Schematic of the hydrogel with pure shear test. (D) Schematic of the crack-propagated hydrogel. (i) Pullout and fracture of fibers in the bridging zone. (ii) Crack pinning in the process region. (iii) Energy dissipation from the rupturing of polymer chains.

Figure 5 (C and D) displays the typical fracture process of fibrous hydrogels. The fracture energy has been widely used to characterize the fracture toughness of hydrogels, which can be divided into three parts (39). The first is the contribution from the bridging region to the energy dissipated by the rupturing and pulling out of the microfibers (Fig. 5Di). The second is due to the energy dissipated by loading and unloading in the process region around the crack tip (see Fig. 5Dii). The third part consists of the intrinsic dissipated energy from breaking polymer chains (see Fig. 5Diii) (40). During the precut hydrogel stretching, the aligned microfibrils were perpendicular to the crack path and pinned the crack due to the strong fibrils with nanocrystalline aggregations (see Fig. 5Dii). The cracks barely affected the load-bearing capacity and integrity of the fibrous hydrogel. The fibrous hydrogels underwent large deformation with high stress and long stretching, leading to the dissipation of a large amount of energy in the process zone. As the applied stretch further increases, the crack propagation along the fiber direction, where microfibrils in bridging zones were pulled out, fractured, and torn (Fig. 5Di) to enhance the energy dissipation (41). Overall, the super toughness of the material was mainly attributed to the anisotropically aligned fibrous structures with flaw-tolerant capability, which maintain high strength and large stretch during the shearing test.

DISCUSSION

This study has demonstrated a versatile strategy to introduce multiple strengthening and toughening mechanisms across multiple length scales into micro-, nano-, molecular-level structures of hydrogels. First, PVA chains were concentrated during freeze-casting to form initial hydrogen bonds and anisotropically aligned micro-honeycomb structures with relatively low crystallinity (fig. S3 and Fig. 2, E to G). Next, ethanol substitution induced the PVA polymers to aggregate and form more hydrogen bonds, stabilizing and strengthening their micromorphology of hard honeycomb walls and soft matrix. Last, Fe³⁺ ion enhancement provides chain-connecting bonds and further promotes the formation of additional hydrogen bonds between PVA chains. Moreover, more crystalline domains appear as high-functionality cross-linkers that improved the elasticity, energy dissipation, and strength of hydrogels at the nanoscale. As a result, the multimechanisms across multiple length scales of fibrous hydrogels result in tremendous enhancement of the material properties including flaw tolerance, strength, stretchability, and toughness.

In summary, we have proposed a nature-inspired synergistic strategy for the fabrication of strong and tough fibrous hydrogels with hierarchical structures across multiple length scales at micro-, nano-, and molecular levels. Mechanical tests demonstrated that the fibrous hydrogels exhibited exceptional mechanical properties including strength, stretchability, toughness, and flaw tolerance. The multimechanisms of strengthening and energy dissipation were validated by various characterization and simulations. The anisotropically hierarchical structures of fibrous hydrogels were observed by scanning electron microscopy (SEM), based on which FEM analysis characterized the strengthening effects and elastic properties of the reinforced honeycomb structural units. The interaction effects between microfiber walls and matrix led to high strength and high resistance to deformation, which becomes more evident with the deepening of modulus-contrasting and Poisson’s ratio contrasting values. The high crystallinity and bonding of the fibrous hydrogels were characterized by material component measurements, and molecular dynamics simulations showed that the solvent enhancement and ion enhancement on the hydrogels were dominated by the formation of chain-connecting Fe bonds and multiply promoted hydrogen bonds. Therefore, the involved strengthening and toughening mechanisms were demonstrated to be attributed to the hierarchical structures, including microscale anisotropic honeycomb–structured three-dimensional fiber walls with matrix-, hydrogen bond–, and coordination bond–enhanced fibers with nanocrystalline domains, as well as entangled and cross-linked strong PVA chains at the molecular level. This study characterizes the multiscale multimechanisms of fibrous hydrogels in detail and establish the relationship between structure-performance mechanisms, which provide insight into the designing of hierarchical tough hydrogels. The systematic mechanistic analysis model can also be extended to other hierarchical material systems as a novel yet generic approach to the analysis of natural materials.

MATERIALS AND METHODS

Materials

PVA [99+% hydrolyzed, M_w (weight-average molecular weight) = 89,000 to 98,000], ethanol (95%; Thermo Fisher Scientific), iron(III) chloride (FeCl₃; 97%), fluorescein sodium salt, hydrochloric acid (HCl; 36.5 to 38 wt %), and glutaraldehyde solution [50 volume percent (volume %)] were all purchased from Sigma-Aldrich without specific notification.

Preparation of PVA hydrogels

PVA aqueous solution (10 wt %) was first prepared by dissolving the PVA powders in reverse osmosis (RO) water under magnetic stirring and heating (80°C). A clear solution was obtained after degassing. A Teflon mold was used for freeze-casting, which was placed on a copper finger that was half-submerged in liquid nitrogen. The temperature at the top of the copper finger was maintained at −80°C using a proportional integral derivative (PID) control heating ring (E5CC, Omron). The samples thawed at room temperature were denoted as FC-1T. The samples were obtained by immersing frozen samples into ethanol or ethanolic ferric chloride solution (the concentration of ferric chloride was 2 wt %) for further substitution at −10°C for 3 days and represented as FC-Et and FC-EtFe, respectively.

SEM characterization

To characterize the micro- and nanostructures of the anisotropic hydrogels, all samples were cut along both perpendicular to and parallel to the ice-growth direction after freeze-drying and then sputtered with gold by Cressington 108 Auto sputter coater. Next, Hitachi S-4300 field-emission SEM was used to test the prepared samples at an acceleration voltage of 8 to 12 kV.

DSC measurement

DSC was used to quantify the crystallinity of PVA hydrogels. Typically, the hydrogel slices were first dealt with an excess cross-linking agent (including 5 ml of 50 volume % of glutaraldehyde, 500 μl of 36.5 to 38 wt % of hydrochloric acid, and 50 ml of RO water) to fix the amorphous chains. The fixed hydrogels should be immersed in sufficient RO water to remove excess hydrochloric acid for up to 2 hours before being dried. Then, the samples were tested from 50° to 250°C with a rate of 20°C/min under an argon atmosphere at a flow rate of 50 ml/min. Furthermore, the melting enthalpy (m_crystalline) of hydrogel was obtained by integrating the areas of the melting endothermic transition peaks between 200° and 250°C. Thus, the crystallinity (X) of the hydrogels was expressed as X = m_crystalline/m, where m means the 100% PVA standard melting enthalpy (138.6 J/g).

FTIR measurement

Attenuated total reflectance FTIR spectroscopy (Agilent CARY 660) was conducted to characterize the specific chemical groups in the hydrogels. Both the freeze-dried and wet PVA hydrogels were cut as 1-mm-thick films and then tested in the range of wave number from 4000 to 400 cm⁻¹.

Tensile test

The PVA hydrogels were cut into standard dog bone shapes with a thickness of 1 mm, a width of 2 mm, and a gauge length of 10 mm using a homemade cutter. All samples were stretched using an Instron 5500 micro tester with a speed of 6.25 mm/min. The specimens labeled with _⊥ refers to stretch along the direction perpendicular to the alignment, while no special label in specimens means to be stretched along the alignment direction. The force-displacement curves were recorded by the tester and were further used to plot the stress-strain curves by dividing the force by the initial cross-sectional area of the samples and dividing the measured distance divided by the initial distance. In addition, the area under the stress-displacement curve was integrated to characterize the work fracture energy.

Pure shear test

For characterization, the fracture behavior of PVA hydrogels—both notched and unnotched specimens’ rectangular hydrogels with a width of 20 mm, a thickness of 2 mm, and a height of 40 mm—was tested as a pair to measure the fracture toughness. The notched samples with a 6.7-mm-long cut in the middle of the edge were first stretched at a speed of 10 mm/min to acquire the stress curves, in which the critical strain ε_c referring to the strain at crack propagation was obtained. The pairing unnotched samples were also tested to reach the critical strain. The toughness of hydrogel was calculated by integrating the area beneath the stress-strain curves of unnotched specimens from the start point to the critical strain point (ε_c), as formula

$$\mathrm{Toughness}={\int }_0^{{\epsilon }_c}\sigma d\epsilon$$ (1)

Representative volume element

Figure S12 has introduced the detailed procedures for predicting the elastic properties of fiber wall in the hydrogels. The aligned fiber-like hydrogel can be considered as a homogeneous composite (27, 42) with certain elastic properties, which contain fibers and matrix. In the meantime, RVE is used to calculate the equivalent properties of the fibrous hydrogel by using the homogenization approach, assuming that the microcell has a periodic distribution and the average properties of RVE are equal to the average properties of the hydrogel. Furthermore, the effective elastic properties of the aligned hydrogel can be determined on the basis of the equivalent homogeneous method (43). The average stresses and strains in RVE model can be expressed as

$${\overline{\sigma }}_{ij}=\frac{1}{V}{\int }_V{\sigma }_{ij}dV;\mathrm{and}{\overline{\epsilon }}_{ij}=\frac{1}{V}{\int }_V{\epsilon }_{ij}dV$$ (2)

where ${\overline{\sigma }}_{ij}$ denotes the stresses and ${\overline{\epsilon }}_{ij}$ denotes the corresponding strains; the subscripts i = 1,2,3 and j = 1,2,3 refer to the coordinate direction; and V is the volume of the microcell. The effective elastic modulus and Possion’s ratio can be calculated by

$$E_{11}^h=\frac{{\overline{\sigma }}_{11}}{{\overline{\epsilon }}_{11}};\mathrm{and}{v}_{12}^h=\frac{{\overline{\epsilon }}_{22}}{{\overline{\epsilon }}_{11}}$$ (3)

As a result, the predicted modulus (E^f) and Possion’s ratio (v^f) of fiber-like walls in the RVE model can be identified by comparing the numerical properties $E_{11}^h$, $v_{12}^h$ with the tested properties $E_{11}^t$, $v_{12}^t$ of hydrogels in the direction parallel to the alignment.

Finite element method

To investigate the elastic behavior of the microfiber wall in the hydrogels, FEM simulations were carried by the commercial software ABAQUS 2016 based on the liner elastic constitutive model. We used a six-node linear triangular prism (C3D6) element in the simulations. Next, we assigned the elastic properties of matrix and fiber wall and applied PBCs (44) in the RVE model. The numerical results $E_{11}^h$, $v_{12}^h$ of the hydrogels were calculated by combining Eqs. 2 and 3.

Atomistic simulation method

Molecular dynamics simulations were conducted on the commercial software of Materials Studio. The Compass force field was used to determine the atomistic interactions between polymer chains, water molecules, ethanol molecules, and iron ions. A simulation box was built with PBCs. For FC-1T, two PVA chains, each polymerized from 30 monomers, were placed in the box that was then filled with water molecules. For FC-Et, 200 ethanol molecules were also added in the box, and 40 Fe³⁺ and 120 Cl⁻ ions were further applied in the box for building FC-EtFe. The initial size of the simulation unit cell is 28.92 Å by 28.92 Å by 33.95 Å, with the lattice parameters of α = β = γ = 90°. The models were equilibrated at 298 K for 25 ps in the NPT ensemble, and Fig. 4Ci and fig. S10 (Bi and Ei) showed the equilibrium system of FC-EtFe, FC-1T, and FC-Et, respectively. The loading was applied in the box with a constant velocity of 100 Å/ps, with an Andersen thermostat that was used to maintain the temperature at 298 K, and with no pressure on the other two directions. The cutoff value of carbon-carbon single bond was defined as 1.80 Å (45) to imply the potential breaking of polymer chains. These calculations were relaxed using a smart algorithm method with an energy convergence of 1 × 10⁻³ kCl/mol and force of 0.5 kCl/mol per Å

Supplementary Materials

This PDF file includes:

Figs. S1 to S12