Research Article www.acsami.org
Mechanically Viscoelastic Properties of Cellulose Nanocrystals Skeleton Reinforced Hierarchical Composite Hydrogels Jun Yang* and ChunRui Han Beijing Key Laboratory of Lignocellulosic Chemistry, Beijing Forestry University, Beijing 100083, China S Supporting Information *
ABSTRACT: With inspiration from the concept of natural dynamic materials, binary-component composite hydrogels with excellent mechanical properties and recovery capability were prepared from the cellulose nanocrystal (CNC) skeleton reinforced covalently cross-linked polyacrylamide (PAAm) networks. The hierarchical skeleton obtained by freeze-drying of CNC aqueous suspension was directly impregnated into acrylamide (AAm) monomer solution, and in situ polymerization occurred in the presence of hydrophilic cross-linker PEGDA575. Under stress, hydrogen bonds at the interface between CNC and PAAm as well as inside the CNC skeleton acted as sacrificial bonds to dissipate energy, while the covalently cross-linked PAAm chains bind the network together by providing adhesion to CNC and thereby suppress the catastrophic craze propagation. The above synergistic effects of the CNC skeleton and the elastic PAAm network enabled the composite hydrogels to withstand up to 181 kPa of tensile stress, 1.01 MPa of compressive strength, and 1392% elongation at break with the fracture energy as high as 2.82 kJ/m2. Moreover, the hydrogels recovered more than 70% elasticity after eight loading−unloading cycles, revealing excellent fatigue resistance. The depth-sensing instrumentation by indentation test corroborated that the CNC skeleton contributed simultaneous improvements in hardness and elasticity by as much as 500% in comparison with the properties of the pristine PAAm hydrogels. This elegant strategy by using the CNC skeleton as a reinforcing template offers a new perspective for the fabrication of robust hydrogels with exceptional mechanical properties that may be important for biomedical applications where high strength is required, such as scaffolds for tissue engineering. KEYWORDS: Hydrogels, Cellulose nanocrystals, Reinforcement, Viscoelastic, Mechanical Properties
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INTRODUCTION Polymeric hydrogels are cross-linked hydrophilic networks that can absorb large quantities of water without dissolving, and they permeate our lives from biological tissues to adsorbents for environmental remediation.1−3 Many of these applications require hydrogels with high strength and flexibility, as well as reversible deformation under high strains.4−6 Unfortunately, one of the most notorious problems is that the conventional chemically cross-linked polymer hydrogels are usually brittle and break easily under stress.4 The weakness of these hydrogels mainly originates from the inhomogeneously cross-linked structures (randomly distributed chain lengths between crosslinks), weak interactions between chains, as well as lack of an efficient energy dissipation mechanism in the networks.7,8 Recently, numerous elegant attempts have been witnessed to improve the mechanical properties of hydrogels, where double network (DN) hydrogels pioneered by Gong et al.9 and nanocomposite hydrogels (NC gels) proposed by Haraguchi10 are two remarkable examples. The DN hydrogels consist of two interpenetrating networks, in which the first network (short chains) and the second network (long chains) are separately cross-linked by covalent bonds. While the DN structure harnesses the ability of an embedded brittle network to toughen the hydrogels, it always © XXXX American Chemical Society
suffers permanent damage without recovery after experiencing cyclic deformation.11 To address this drawback, some noncovalent bonds have been employed in the DN to make the network recoverable after internal rupture.12,13 For example, a series of polyampholytes with different ionic combinations that act as sacrif icial bonds were applied to synthesize hydrogels with high toughness and viscoelasticity.14 Notably, Suo15 and Zhao5 et al. developed hybrid DN gels by combining Ca2+ cross-linked alginate gel with a covalently cross-linked polyacrylamide (PAAm) network, which exhibited excellent stretchability. For NC gels, a series of hydrophilic polymer chains (poly(Nisopropylacrylamide)) was in situ grafted from a clay surface. When the NC gels are stretched, the chains distributed between neighboring clays extend gradually to avoid stress concentration.16 Indeed, various nanofillers such as carbon nanotubes,17 graphene sheets,18 hematite,19 and macromolecular microsphere composites20 were used as analogous cross-links to transfer stress to a neighboring process zone. Recently, many distinct nanostructures based on polysaccharides (such as chitosan, hyaluronic acid, and alginate) and their derivatives Received: July 18, 2016 Accepted: September 8, 2016
A
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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ACS Applied Materials & Interfaces
Figure 1. Digital photographs of colloidal CNC suspension (1 wt %) and its TEM images.
Figure 2. (a) Scheme of preparation procedure for CNC skeleton reinforced hydrogels. (b) The skeleton reinforced CNC0.5 hydrogels become white, opaque, and rigid relative to pristine PAAm hydrogels. Cross-sectional SEM images of the freeze-dried CNC0.5 hydrogels exhibit an interconnected comb-like network structure.
been widely reported, the deformation behaviors and fracture mechanics at the microscale remain to be explored.38−40 Thus, detailed discussion of the deformation behavior and crack propagation mechanism at the microscale combined with mechanical characterization would promote the understanding of the CNC interfacial interaction and load transfer mechanism, enabling us to optimize the composite’s performance. CNCs derived from a plant with hierarchical cellular fibrous structures are suitable to act as skeletons for fabricating composites with physiochemical properties from each constituent.32 By mimicking the natural cork-like hierarchical structure, numerous efforts have been made to synthesize threedimensional porous cellulose monoliths or aerogels by using CNCs as building blocks.41−43 In combination with mechanical resiliency, high elasticity, and low density, one can expect that this skeleton approach via a self-assembly strategy favors the preparation of robust hydrogels that are distinct from most previously reported hybrid hydrogels with randomly dispersed CNCs. In this work, inspired by the interfacial interactions between natural hierarchical CNCs and a polymer matrix, we demonstrate a simply strategy to construct tough hydrogels by incorporating the CNC skeleton as a reinforcing phase into a soft and ductile PAAm network, yielding CNC skeletonassisted binary composite hydrogels. The benefit of this strategy includes the following: (1) a simple one-pot process to attain the CNC skeleton reinforced hybrid networks, (2) dynamic and reversible hydrogen bonds which effectively dissipate energy in the CNC skeleton that acts as a sacrificial network, (3) dynamic arrangement of CNC associated with good elastic maintenance by a covalent PAAm network to synergistically promote fast self-recovery and significant fatigue resistance
have been utilized to fabricate both tough and strong hydrogels, where dynamic interactions (e.g., electrostatic interactions, hydrophobic association, and hydrogen bonds) act as sacrificial bonds to improve energy dissipation and mechanical properties of the hydrogels.21−23 For example, Cai24 and Zhang25 et al. prepared chitosan-based supramolecular hydrogels via electrostatic interactions and hydrogen bonding. Similarly, Burdick et al.26 reported the injectable DN gels through a supramolecular guest−host assembly between hyaluronic acid and β-cyclodextrin. Wu et al.27 also developed a simple soaking strategy to convert the chitosan-polyacrylamide composite hydrogels into high strength DN gels via the formation of chitosan microcrystalline and chain entanglement. Besides, Chen et al.28 proposed a one-pot method to prepare highly mechanical and recoverable DN gels from agar due to its unique sol−gel transition. During the pursuit of the high performance of structural materials, the biological composites (such as collagen fibers in bone, protein fold in silk) provide fruitful inspiration for the preparation of biomimetic materials with excellent stiffness and strength through self-assembled nanoscale blocks.29,30 Cellulose and in particular cellulose nanocrystals (CNCs) have attracted increasing interest due to their outstanding biocompatibility, renewability, and high elasticity.31−35 The CNCs with ordered (crystalline) regions, high Young’s modulus (up to 140 GPa), as well as a large surface area (∼700 m2/g) provide they excellent mechanical properties.31 These nanoparticles possess a high intrinsic tendency to assemble into the unique hierarchical structure driven by intra- and interhydrogen bonds.36,37 Although significant progress in macroscopic mechanical properties of CNC reinforced composites have B
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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ACS Applied Materials & Interfaces Table 1. Compositions of Hydrogels
a
code
CNC volume fraction (%)a
CNC (mg)
acrylamide (g)
PEGDA575 (mg)
KPS (mg)
water (mL)
CNC0.2 CNC0.5 CNC0.8 CNC1 CNC1.5 CNC2 PAAm
0.2 0.5 0.8 1 1.5 2 0
64 160 256 320 480 640 0
1.42 1.42 1.42 1.42 1.42 1.42 1.42
342 342 342 342 342 342 342
40 40 40 40 40 40 40
20 20 20 20 20 20 20
CNC volume fraction was defined as the volume ratio of CNC to the total volume of water (20 mL) using density of CNC = 1.6 g/cm3.
properties, and (4) elegant avoidance of nanoparticle aggregation that often occurs in preparation of hybrid composites with randomly distributed nanoparticles in the matrix. It is expected that this straightforward sacrificial bonding strategy via the CNC skeleton would enrich the exploration in designing high strength CNC-based materials, which may have an important implication as scaffolds for tissue engineering and as drug delivery vehicles.
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Sw =
Ws − Wd Wd
(1)
where Ws and Wd are the weight of swollen hydrogel and dry hydrogel, respectively. Mechanical Test. Mechanical tests of the hydrogels with uniform water content (Sw = 20) were performed at room temperature using a Zwick Z005 equipped with a 500 N load cell. It is noted that, immediately before testing, water was sprayed on the hydrogel samples to avoid water evaporation. To guarantee data accuracy, six specimens were tested for each sample, and the average values were reported. Tensile Test. The tensile stress−strain measurements were performed at a stretch rate of 60 mm/min, and the toughness of the hydrogels was calculated from the area under the stress−strain curves. The nominal tensile stress (σ) was obtained by dividing the force (F) by the initial cross-sectional area (A0) of the specimen (σ = F/A0). The tensile strain (ε) was defined as the ratio of gauge length (L) to the initial gauge length (L0) (ε = (L − L0)/L0). The Young’s modulus was calculated from the slope of the initial linear region of the stress−strain curves (5−15% strain). The fracture energy (Tfrac), a parameter to characterize the toughness of the sample, was determined by the area under the stress−strain curve. For the hysteresis test, the loading and unloading cycles were performed at a constant (60 mm/min) to maintain a unique loading history. The strain-rate-dependent tensile test was conducted at the strain rates ranging from 30 to 210 mm/min. For recovery calculation, the specimens were initially stretched by a loading−unloading to achieve a maximum stretching (1400%), and then the specimens were sealed in plastic bags and stored at 25 °C with different interval times (15−60 min) and measured again. The elastic recovery ratio was defined by (σ0 − σt)/σ0 × 100%, where σ0 was the initial fracture strength and σt was the strength after resting time t. Compressive Test. The compressive tests were conducted at a compression rate of 5 mm/min. The raw data were recorded as force versus displacement and converted to stress versus strain with respect to the initial dimensions. The compression hysteresis was measured at the same conditions at deformation of 90% strain. Morphology Observation. For cross-section observation by scanning electron microscopy (SEM, Hitachi 3500S), the freezedried hydrogels were immersed into liquid nitrogen for 3 min, fractured, and stuck to the sample holder with a carbon pad. After sputter-coating with platinum for 30 s, the samples were imaged at an accelerating voltage of 5 kV and a work distance of 6 mm. Transmission electron microscopy (TEM) for the ultramicrotomed samples was performed with JEM1010 (JEOL), operated at an accelerating voltage of 80 kV. The sample deposited carbon-coated grids were negatively stained by 2 wt % uranyl acetate for 20 s to improve contrast. Rheological Measurements. The rheological measurements were performed by using an AR2000 rheometer (TA Instruments) with 25 mm parallel plates at room temperature. The gap distance between the plates was 1 mm. The disc shape samples were adhered to the plates, and dynamic shear experiments were performed with a frequency sweep of 0.1−100 rad/s (within a linear response region that was determined from a strain sweep). During all experiments, a thin silicon oil trap was used to minimize water evaporation.
EXPERIMENTAL SECTION
Materials. The acrylamide (AAm, Alfa Aeser) and polyethylene glycol diacrylate (PEGDA 575, Mn = 575, Aldrich) were used as received. All other reagents and solvents were analytical grade and used as received without further purification. Cellulose nanocrystals (CNCs) were isolated from cotton pulp by sulfuric acid hydrolysis (55 wt %) at 50 °C for 90 min, as reported in our previous work.22 The CNC precipitate was then rinsed with water, centrifuged, and dialyzed until neutral pH was achieved. The sulfate ester (OSO3−) content on the CNC surface was determined to be 0.065 mmol/g by conductometric titration with NaOH. The average dimensions of CNCs were measured to be 10 ± 2 nm wide × 200 ± 15 nm long with TEM observation (Figure 1). The CNC suspension was diluted with water (1 wt %) and homogenized with a high speed blender (Philips HR2171/90, 600 W) for 30 s. The suspension was transferred to a container, frozen with liquid nitrogen for 10 min, and then freeze-dried at −80 °C for 24 h to allow the frozen water in the samples to sublime, attaining the CNC skeleton. Preparation of CNC Skeleton-Assisted Binary Hydrogels. First, 20 mL of deionized water in a round-bottom flask was bubbled with N2 for 30 min to remove dissolved oxygen; 1.42 g of AAm (20 mmol), 0.04 g of potassium persulfate (KPS), and PEGDA 575 (342 mg, 3 mol % against monomer) were added into the water. Then, the CNC skeleton was impregnated into the above aqueous solution for 1 h with mild stirring to facilitate penetration of precursors into the skeleton (Figure 2a). The soaked CNC skeleton was subsequently put into a flask, which was purged with N2 gas for 10 min and then sealed. The free-radical polymerization was carried out for 2 h at 50 °C, and then terminated by cooling the flask in an ice−water bath. The obtained composite hydrogels were immersed in deionized water for 4 days (refreshed every 12 h) to remove unreacted monomers (Figure 2b). A series of composite hydrogels were prepared by varying CNC skeleton fractions, and the resulting specimens were named CNCx, where x represents the volume fraction of CNC (Table 1). As a control, pristine PAAm was also prepared by the same procedure in the absence of CNC skeleton. The obtained samples were cut into rectangular shapes (30 mm in length × 8 mm in width × 4 mm in thickness) and cylindrical shapes (12 mm in diameter × 20 mm in height) for tensile and compressive tests, respectively. Characterization. Swelling Behaviors. The swelling ratio (Sw) of hydrogels was measured at room temperature using a gravimetric method. A small cubic sample of hydrogel (∼2 g) was put into deionized water for 48 h and weighed after removing the surface water with filter paper. Then, the sample was dried in a vacuum oven at 45 °C until the constant weight. The Sw was calculated as C
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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Figure 3. (a) Freeze-dried CNC skeleton and (b, c) its SEM images; the inset TEM image indicates crumpled regions in the nanofibrils. (d−g) TEM images of polymer deposition in composite hydrogel networks, which gradually thicken with increase in CNC fraction, suggesting the formation of a continuous polymer layer on the CNC skeleton (CNC0.2, CNC0.5, CNC0.8, and CNC1 for parts d−g).
Figure 4. Cross-sectional SEM images of freeze-dried (a) pristine PAAm hydrogels and (b) composite hydrogels. The inset shows the inside pores where the pull-out CNCs bridge the neighboring matrix.
bonding between fibrils. The penetration of AAm monomer into the CNC skeleton is easy due to the abundant hydroxyl groups on the cellulose backbones, and the in situ polymerization within CNC skeleton does not damage its structure integrity (Figure S3). The PAAm-coated fibril structure is clearly noted in TEM images of ultrathin sections (Figure 3d− g), where cellulose nanofibrils are encapsulated by a layer of polymer matrix and form a nanoporous network. These results corroborate that the strong interfacial interactions via hydrogen bonds (additional FTIR and TGA characterization in Figure S4) are critical for the load transfer between reinforcing skeleton and the matrix, thereby enabling tailoring of the mechanical properties of the composite gels. Furthermore, it is interesting to find that the cross-sectional morphology of pristine PAAm hydrogels is distinct from that of CNC skeleton reinforced composite hydrogels. For pristine hydrogels, water molecules are homogeneously dispersed within the swollen polymeric network. The ice crystals form upon the samples immersed in liquid nitrogen and act as skeletons for pore generation, leading to a sponge-like structure with dense cell wall (Figure 4a),46,47 whereas for the composite hydrogels, water molecules are closely associated with the cellulose through hydrogen bonding. Considering that the rigid and straight cellulose backbone has a strong tendency to arrange in parallel conformation,47 the ice crystals would heterogeneously distribute in a mesh-like structure (Figure 4b). Previous work has proposed that the filamentous structures across the pores at both micro- and nanometer scales would increase the catastrophic crack propagation resistance near the crack tips and thereby promote the distribution of stress to larger volume.48
Nanoindentation Test. Nanoindentation was conducted using a Hysitron Triboscope nanomechanical testing system. Indents were made by a three-side pyramid diamond Berkovich tip with nominal radius of curvature of 100 nm, and the force resolution and displacement resolution were 1 mN and 0.1 nm, respectively. The hardness and elastic modulus of the hydrogels were obtained from the load−displacement curves. A typical indentation process contains four segments: approaching the sample surface, loading until the peak load, holding the peak to minimize the influence of polymer creep on the unloading curves that used to calculate the elastic modulus, and finally unloading the indenter completely. A minimum of 20 indentations (100 μm between indentations to avoid interactions) were performed for each sample with a loading rate of 0.2 mN/s.
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RESULTS AND DISCUSSION
Morphological Observation. The CNC self-assembled into porous nanofibril aerogels from homogeneous aqueous suspension (Figure 3a), due to strong hydrogen bonding between cellulose nanofibers in the nanometer range.43−45 With adjustment of the contents of CNC suspension from 0.7 to 2.5 wt %, the skeleton density could be varied from 6.9 to 20.5 mg/cm3 (Figure S1). The obtained CNC skeletons possess nonordered, interconnected porous structures that range from tens to hundreds of micrometers (Figure 3b,c). In addition, there exist some wrinkles and folded regions along the longitudinal direction of the assembled monolith, and the inset TEM images in Figure 3b confirm the crumpled regions in the nanofiber structure, which could share the load from the matrix and hinder rapid craze propagation.42,43 Besides, a significant hysteresis loop is noted under cyclic compressive conditions (Figure S2), implying that the CNC skeleton provides efficient energy dissipation by temporary dissociation of hydrogen D
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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Figure 5. (a) Swelling behaviors and (b) frequency sweep rheological properties (G′, solid symbols; G″, open symbols) of hydrogels (pristine PAAm, black; CNC0.2, red; CNC1, green; CNC2, blue).
Figure 6. Tensile properties of the composite hydrogels. (a) Stress−strain curves for hydrogels with different CNC skeleton fractions. (b) Fracture energy scales with CNC volume fraction. (c) Stress−strain hysteresis by loading−unloading cycles. (d) CNC1 gels are subjected to cyclic deformation with different stretching ratios. (e) Tensile properties for CNC1 at different strain rates. (f) Tensile hysteresis energy as a function of strain. (g) Tensile behavior recovery with periods of resting time.
Swelling and Rheological Properties. It has been known that the swelling behavior of a gel is largely determined by its cross-linking density.49 Since CNC can be regarded as a kind of “analogous cross-linker” in this system, the composite hydrogels possess a higher cross-linking density than that of pristine PAAm hydrogels, leading to a stiffer network with reduced swelling capability (Figure 5a). The rheological measurements also indicate a drastic enhancement in moduli with increasing CNC fraction (Figure 5b), where both elastic modulus (G′) and loss modulus (G″) exhibit frequency independence. Besides, G′ is much higher than G″ over the whole frequency range, implying that elastic behavior rather than viscous behavior dominates the hybrid network. Additionally, the existence of attractive interactions between flexible polymer chains and the CNC skeleton is supported by differential
scanning calorimetry (DSC) measurements (Figure S5). The detected glass transition temperature (Tg) of the composite hydrogels is slightly higher than that of pristine PAAm (180 °C), and the Tg increases with increasing CNC fractions. This result is consistent with the introduction of CNC skeleton having some confinement effect on the mobility of polymer chains and restraining the swelling capability thereby. Tensile Properties. According to the uniaxial tensile tests, the mechanical properties of composite hydrogels are significantly improved by the incorporation of the CNC skeleton: fracture stress (σb) and elongation at break (εb) remarkably increase from 73 to 151 kPa and 647% to 1388%, respectively, when the CNC fraction increases from 0.2 to 1 vol % (Figure 6a). The fracture energy T, a parameter to evaluate the resistance against crack propagation, of the composite E
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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Figure 7. Compressive properties of hydrogels. (a) Typical stress−strain curves of the composite hydrogels. (b) Multiple stress−strain curves at varied strains and (c) continuous loading−unloading for CNC1. (d) Stress and toughness of CNC1 from eight successive loading to 90% strain without resting intervals.
hydrogels scales with the volume fraction of CNC skeleton Vc as T ∼ Vc1.3, and attains a value as high as 2.8 kJ/m2, highlighting the role of reinforcement in blunting and energy dissipation (Figure 6b). When the CNC volume fraction exceeds 1.5%, the fracture stress increases marginally to 173 kPa but with an evident decrease in stretchability to 1247%. For pristine PAAm gels, the maximum elongation and the corresponding fracture stress are 450% and 35 kPa, respectively, which are much lower than those of composite hydrogels. Similarly, the Young’s modulus (E) of the hydrogels is determined as 29.8 and 7.3 kPa for the CNC2 and PAAm, respectively, featuring the stiffening effect of the CNC skeleton. To highlight the reinforcement efficacy of a CNC skeleton in PAAm hydrogels, we also prepared composite hydrogels with randomly distributed CNC for comparison. The results show that the fracture strengths of CNC skeleton reinforced hydrogels are 1.04−1.26 times higher than those of hydrogels with randomly dispersed CNCs at the same filler fraction (Figure S6), suggesting that the continuous and well-structured network of CNC skeleton provides better mechanical reinforcement. Indeed, previous work has reported that the randomly dispersed nanoparticles consisted of many point-to-point connections, and a higher filler fraction was generally required before the percolation network can be formed.39 The deformation of composite hydrogels leads to energy dissipative processes as shown in Figure 6c by the increase of the hysteresis loop area, and the dissipative mechanism is observed to be affected by the maximal stretching ratio with some residual strains (Figure 6d). This energy dissipation stems from the rearrangement of CNC-PAAm interfacial hydrogens upon deformation, resulting in the decreased stress concentration and resisting crack propagation. It should be noted that, in contrast to covalent bond permanent rupture, this rearrangement allows for reversible dissipation by the disruption of interactions (hydrogen bonding) that potentially can be reformed. Indeed, the strain-rate dependence of the mechanics supports the above physical scenarios, where the higher strain-rate contributes to the higher fracture strength (Figure 6e). The fracture strength exhibits the less rate-
dependent response as the strain rate approaches 180 mm/min, implying the limitation of the ability of hydrogen bonds to dissipate energy via reversible association at short time and behave as permanent cross-links. The hysteresis energy, or the loop area, is dependent on strain with an R2 value of 0.96, indicating a self-toughening effect at high strains (Figure 6f).4 As shown in Figure 6g, the composite hydrogels exhibit a distinct yielding point, and the stress−strain curve gradually recovers to its original shape within ∼60 min. This time-dependent elastic recovery behavior involves a two-stage process which is related to the balance between the covalent nature of PAAm network elasticity and the recovery of temporary hydrogen bonds in the relaxation process.49 At large strain, the elastic contraction dominates the rupture of reformed bonds and leads to fast recovery, whereas the elastic contraction becomes weak and slows down the recovery of the chains to their equilibrium state at small strain. Compressive Properties. The compression test also exhibits the remarkable reinforcement role of the CNC skeleton, and the stiffness increases nonlinearly with increasing CNC fraction (Figure 7a). For example, the compression strength of the composite hydrogels ranges from 165 to 1017 kPa, which is more than 1 order of magnitude higher than those of pristine PAAm hydrogels (92 kPa). This remarkable asymmetry between tensile profiles and compressive profiles may arise from the anisotropy of cellulose structure where nanofibrils align along the surface via a hydrogen bonding assembly with unique parallel conformation in native cellulose crystalline domains.22 Figure 7b depicts the compressive stress−strain curves of the hydrogels at predetermined strain of 40%, 65%, and 90%, respectively. One can note that the loading process exhibits three distinct stages, including the initial elastic region where the stress linearly increases with the strain (ε < 25%), plateau region during which most of the absorbed energy is dissipated (25% < ε < 70%), and the final densification region (ε > 70%) reflected by rapid growth of stress, behaving like an open-cell structure of natural cork under compression.30 Indeed, at high strains, the densification of F
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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Figure 8. Cryo-SEM images of hierarchical structure evolution in compressive loading−unloading cycles for CNC1 (a−d for strains of 25%, 50%, 70%, and 20%, respectively), where the heterogeneous mesh-like structures are maintained after a large compression (∼65%). Some extended voids and bridged CNCs are noted in the parallel direction to the stretching (marked by arrows), which dissipates a huge amount of fracture energy.
Table 2. Summary of Mechanical Properties of Gels by Nanoindentation Tests code
CNC volume fraction (%)
CNC0.2 CNC0.5 CNC0.8 CNC1 CNC1.5 CNC2 PAAm
0.2 0.5 0.8 1 1.5 2 0
hardness (GPa) 0.038 0.045 0.062 0.072 0.087 0.108 0.022
± ± ± ± ± ± ±
0.004 0.005 0.008 0.007 0.007 0.01 0.004
elastic modulus (GPa) 0.67 0.75 0.93 1.18 1.36 1.77 0.38
± ± ± ± ± ± ±
0.07 0.09 0.11 0.14 0.13 0.18 0.04
plasticity index 0.26 0.28 0.30 0.33 0.38 0.45 0.18
± ± ± ± ± ± ±
0.02 0.03 0.04 0.03 0.04 0.03 0.02
Figure 9. Nanoindentation measurement of hydrogels: (a) hardness, (b) elastic modulus, and (d) plasticity index profiles with respect to displacement into the sample surfaces. (c) Typical loading−unloading curves of indentations made at a peak indentation load of 90 mN (pristine PAAm, black; CNC0.2, red; CNC1, green; CNC2, blue).
state (Figure 8). During the initial loading process, the hydrogel pores gradually shrink and become densified (Figure 8a−c). In the subsequent unloading process, the porous structure can recover its initial state (Figure 8d). It has been proposed that the water molecules could act as plasticizers that improve the rearrangement of hydrogen bonds when the compression is released,48 which promotes the network recovery. Except for
porous structure leads to bending of CNCs together and thus prevents collapse and fiber slippage.36 The fatigue resistance properties of the composite hydrogels are examined by successive loading−unloading tests without interval between each cycle (Figure 7c), and the microscopic morphology indicates that the networks after cyclic compression do not demonstrate much damage compared to the initial G
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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displacement of ∼780 nm with permanent deformation at 590 nm. In contrast, the composite gels showed a steeper unloading pathway and a lower permanent deformation. Furthermore, the plasticity index (χ), a parameter to characterize the relative plastic/elastic behavior of the material when it undergoes external stress,51 of the composite gels shows more significant viscoelastic properties with a higher plasticity index than that of pristine PAAm gels (Figure 9d). During unloading, the load is reduced at the same rate as in the loading cycle, and the elastic displacement is gradually recovered, while notable creep is found in the maximum hold segment for the composite gels, and the creep depth and displacement at maximum holding segments exhibit a distinct difference with addition of CNC skeletons, implying that the reversible hydrogen bonds on the CNC surface affect the viscoelastic properties of the PAAm matrix and dominate the creep resistance of the materials.
the initial three cycles showing large hysteresis, the following hysteresis loops become smaller, and the stress at 90% strain decreases from 647 kPa for the first loading to 512 and 358 kPa for the second and third cycles, respectively (Figure 7d). After the fourth cycle, the stress−strain curves remain almost unchanged, and the hydrogels still show compressive stress of 265 kPa after eight cycles. According to Zhao,4 the general principle for the design of tough gels is to employ dynamic mechanisms to dissipate a significant amount of energy under deformation and to maintain the original configuration after release. In this work, the hydrogen bonds serve as dynamic cross-links in a sacrificial way by providing a reversible structure for nanofibril transition between association and dissociation, and the covalent PAAm network allows elasticity and maintains network stability. Indeed, this hybrid cross-linking strategy has been widely implemented in other polysaccharide-based hydrogels. In Cai et al.’s work,24 chiton was sequentially chemically cross-linked with epichlorohydrin and physically cross-linked with the hydrophobic interaction and the formation of a crystalline region in ethanol aqueous solution. Similarly, Wu et al.27 also reported PAAm-chitosan hybrid cross-links by postformation of chitosan microcrystalline and entanglement in NaOH and NaCl solution. They proposed that the excellent mechanical properties of this hybrid network stemmed from synergetic interactions of the PAAm covalent network and the chitosan physical network, which maintained network integrity and dissipated energy during deformation, respectively. In this respect, the development of hybrid cross-linking hydrogels featuring superior mechanical properties and fundamental understanding about load transfer architecture from hybrid microstructure inspire a promising approach toward novel materials with a unique combination of strength and toughness. Nanoindentation Measurement. The nanoindentation technique is employed to examine the mechanical properties of the CNC skeleton engineered hydrogels. The averaged hardness (H) and elastic modulus (E) of the composite hydrogels calculated by the Oliver−Pharr method from the load-penetration depth curves between 300 to 600 nm are listed in Table 2. At small penetration depths up to ∼250 nm, H and E exhibit large deviations (indentation size effect), which are probably due to the specimen’s surface roughness and the interaction between the sample and the tip.50 After indentation depth approaches 300 nm and onward, the profiles display a stable trend for all the samples, suggesting the CNCs are homogeneously dispersed along the indentation direction (Figure 9a,b). Another important trend observed from the instrument indentation test is that both H and E of the hydrogels displayed a constant increase with the CNC content, implying that there are benefits to reinforcing the material with an associated CNC skeleton so that more energy is required to reduce entropy and raise enthalpy when the network is deformed. The typical load−displacement curves of the hydrogels at a peak indentation load of 90 mN are shown in Figure 9c, and no discontinuities are noted in the curves, implying that no cracks occurred during indentation measurement. On loading the segment, the force is incremented at a constant velocity, and the curves steadily shift upward for the composite gels, which composed the higher CNC content, displaying a shallower depth of penetration of the nanoindenter into the gels due to an increase in stiffness of the gels. After holding 15 s at the maximum load, the pristine PAAm shows a maximum
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CONCLUSIONS We have demonstrated the incorporation of an assembled CNC skeleton with porous network into PAAm matrix to create reinforced composite hydrogels. The elastic PAAm networks connected by chemical cross-links prevent permanent plastic deformation, and hydrogen bonds stemming from the impregnated CNC skeleton serve as dynamic and reversible sacrificial interactions to associate and dissociate during loading−unloading cycles. The hierarchical structure of the CNC skeleton and the synergistic effect between elastic covalent bonds and dynamic sacrificial hydrogen bonds collectively contribute to the noncatastrophic crack propagation and efficient energy dissipation. The microscopic deformation mechanism of the hydrogels is also examined using a nanoindenter, and the results show that the hardness, elastic modulus, and plastic index increase with increasing CNC fraction. The hierarchical structure of the CNC template, maintenance of elastic covalent bonds, and dynamic sacrificial hydrogen bonds synergistically lead to great strength under deformation, demonstrating that the skeleton strategy proposed here is an effective way to prepare cellulose-based hydrogels with excellent mechanical properties. The structure−property relationship established in this work would diversify the tough hydrogels by fine-tuning the structural and mechanical properties, which hold great promise as candidates for loadbearing materials in pharmaceutical and tissue engineering fields.
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.6b08834. Mechanical properties summary, CNC skeleton density and compressive behavior, IR and TGA curves of the gels, comparison reinforcement between skeleton strategy and random distribution, description of cryo-SEM and ultramicrotome for TEM, and nanoindentation measurement (PDF)
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest. H
DOI: 10.1021/acsami.6b08834 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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ACKNOWLEDGMENTS This work was financially supported by Fundamental Research Funds for the Central Universities (2015ZCQ-CL-03), National Natural Science Foundation of China (21404011, 21674013), and innovation program of College of Materials Science and Technology (2016CLCX11).
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