Simultaneous Enhancement of Stiffness and Toughness in Hybrid

Oct 28, 2015 - Combining both chemical and physical cross-links in a double-network hydrogel (DN gel) has emerged as a promising design strategy to ob...
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Simultaneous Enhancement of Stiffness and Toughness in Hybrid Double-Network Hydrogels via the First, Physically Linked Network Qiang Chen,*,† Dandan Wei,† Hong Chen,§ Lin Zhu,† Caicai Jiao,† Ge Liu,†,‡ Lina Huang,† Jia Yang,† Libo Wang,† and Jie Zheng*,§,∥ †

School of Material Science and Engineering, Henan Polytechnic University, Jiaozuo, China 454003 School of Chemistry, Nankai University, Tianjin, China 300071 § Department of Chemical and Biomolecular Engineering and ∥Institute of Life-Span Development and Gerontology, The University of Akron, Akron, Ohio 44325, United States ‡

ABSTRACT: Combining both chemical and physical cross-links in a double-network hydrogel (DN gel) has emerged as a promising design strategy to obtain highly mechanically strong hydrogels. Unlike chemically cross-linked DN gels, little is known about the fracture process and toughening mechanisms of hybrid chemically physically linked DN gels. In this work, we engineered tough hybrid DN gels of agar/polyacrylamide (Agar/PAAm) by combining two types of cross-linked polymer networks: a physically linked, first agar network and a chemical-linked, second PAAm network. The resulting Agar/PAAm exhibited high stiffness of 313 kPa and high toughness of 1089 J/m2. We then specifically examined the effect of the first agar network on the mechanical properties of hybrid Agar/ PAAm gels. We found that by controlling agar concentrations above a critical value, the physically linked agar network can simultaneously enhance both stiffness and toughness of Agar/PAAm DN gels, as evidenced by a linear relationship of elastic modulus and tearing energies of the gels as the increase of agar concentration. This toughening behavior is different from that of chemically linked DN gels. Complement to chemically linked DN gels, this work provides a different view for the design of new stiff and tough hydrogels using hybrid physical and chemical networks.

1. INTRODUCTION Hydrogels, consisting of a large amount of water in their threedimensional polymeric network, have been demonstrated as excellent 3D platform for numerous scientific and industrial applications, such as waste treatment,1,2 agriculture and food chemistry,3−6 environmental engineering,7,8 and tissue engineering.9−11 However, most of hydrogels are generally mechanically soft and/or brittle, and they usually fail at a tensile stress less than sub-MPa and strain less than 100%. To overcome the mechanical weakness issue, extensive efforts have been made to prepare highly strong hydrogels with improved mechanical strength and toughness, including nanocomposite hydrogels,12 hydrophobically associated hydrogels,13,14 ionically cross-linked hydrogels,15 hydrogen bonding or dipole−dipole enhanced hydrogels,16−18 macromolecular microparticle composite hydrogels,19 and double-network hydrogels.20 These hydrogels demonstrate much better tensile strength (1−10 MPa) and/or toughness (102−104 J/m2) than those of conventional hydrogels. Double-network hydrogels (DN gels), composed of two contrasting polymer networks with asymmetric structures, have shown excellent mechanical properties of hardness (elastic modulus of 0.1−1.0 MPa), strength (failure tensile nominal stress 1−10 MPa, strain 1000−2000%; failure compressive © XXXX American Chemical Society

nominal stress 20−60 MPa, strain 90−95%), and toughness (tearing fracture energy of 100−1000 J m−2).21 Such excellent mechanical properties of DN gels are comparable to those of rubbers and human soft tissues. The first PAMPS/PAAm DN gel, comprising poly(2-acrylamido-2-methylpropanesulfonic acid) (PAMPS) as the first network and polyacrylamide (PAAm) as the second network, was invented using a twostep sequential free-radical polymerization method by Gong and co-workers in 2003.20 They proposed that the significantly enhanced mechanical properties of DN gels are presumably contributed to their unique contrasting network structure and strong network entanglement:22 The first network should be tightly linked by rigid and brittle polyelectrolyte, while the second network should be loosely linked by soft and ductile neutral polymer.21 On the basis of the opposite physical nature of two networks, Gong et al. proposed the sacrificial bond concept to interpret the highly mechanical properties of DN gels.21,23 Upon deformation, the first “rigid and brittle” polyelectrolyte network functions as sacrificial bonds as it is fractured into small clusters at a relatively low stress. Then, the Received: September 3, 2015 Revised: October 17, 2015

A

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Macromolecules small clusters from the first network act as the sliding crosslinkers to prevent the second network from crack propagation (damage zone), to sustain stress and store elastic energy, and thus to reinforce the gels. The fracture of first network is accompanied by effective energy dissipation, resulting in large hysteresis in cyclic loading and extremely high toughness of DN gels. Based on the sacrificial bond concept, many different DN hydrogels were developed using the two- or multiple-step polymerization methods, including microgel-reinforced DN gel,24 void-DN gel,25 inverse DN gel,26 jellyfish DN gel,27 and other DN gels.20,21,23−25,28,29 However, it should be noted that most of these DN gels as described above share a common structural feature of both networks being chemically crosslinked; thus, the mechanical behavior and energy dissipation of these chemically linked DN gels can be well explained by the sacrificial bond concept. In very recent years, a number of hybrid DN gels combining both noncovalent and covalent cross-links in two networks were developed independently by different lab. Suo et al.30 prepared the Alginate/PAAm hybrid gels combining a Ca2+ cross-linked alginate network and a covalently cross-linked PAAm network, which achieves remarkable fracture toughness of ∼9000 J/m2 and notch insensitive properties. Panhuis et al.31−33 developed a series of ionic−covalent gellan gum/ PAAm, gellan gum/epoxy-amine, and carrageenan/epoxyamine hybrid gels. Lu et al. prepared K+/Ca2+-carrageenan/ PAAm hybrid gels, which exhibited excellent extensibility (∼20 times) and high toughness (∼9500 J/m2). Besides hybrid ionically chemically cross-linked DN hydrogels, Li et al.34 synthesized the poly(vinyl alcohol)/polyacrylamide (PVA/ PAAm) hybrid gels using PVA crystallites as physical crosslinkers. The hybrid physically chemically PVA/PAAm DN gels also demonstrated high stiffness (∼5 MPa), strength (∼2.5 MPa), toughness (14 000 J/m2), and recoverability (full recovery in ∼3 h at 20 °C). Li et al.35 developed poly(vinyl alcohol)/konjac glucomannan (PVA-KGM) DN gel using a cycle freezing−thawing process, and the resulting gels showed high compressive strength of 65 MPa. We developed agar/ polyacrylamide (Agar/PAAm) hybrid DN gels, where the first agar network is cross-linked by hydrogen bonds and the second PAAm network is cross-linked by covalent bonds.36−38 The Agar/PAAm gels can achieve highly mechanical properties of stiffness (elastic modulus of 123 kPa), strength (failure compression stress of 38 MPa and failure tensile stress of 1.0 MPa), and dissipated energy (9 MJ/m3), excellent extensibility (15−20 times longer relative to its initial length), and a unique free-shapeable property (formation of many complex geometrical shapes). As compared to chemically linked DN gels, all of these hybrid DN gels contain a physically linked, first network, and they all can achieve comparable mechanical properties to chemically linked DN gels. The major structural difference between chemically linked and hybrid-linked DN gels is their first networks, which are expected to cause the differences in network fracture process and the associated energy dissipation mode. The sacrificial bond concept for gel toughness mechanisms is largely derived from chemically cross-linked DN gels. This sacrificial bond concept can explain toughness enhancement, large hysteresis, and necking phenomena on the basis of irreversible break of covalent bonds. But, such “one size fits all” mechanism may or may not work for hybrid physically chemically linked DN gels because the mechanical properties (toughness, strength, hysteresis, and recoverability) and

underlying toughening and energy dissipation mechanisms of these gels are not related to the permanent breaking of chemical bonds, particularly in the first network. On the basis of our recent study of the internal fracture process of Agar/PAAm hybrid DN gels,39 we found that the first agar network experienced a continuous fracture process by pulling out agar chains from the first network, which is completely different from a discontinuous fracture process of chemically linked DN gels by breaking chemical bonds to form small clusters. A chainpulling-out model was proposed to interpret the distinct velocity-dependent tensile properties, simultaneous necking, and self-recovery of Agar/PAAm hybrid DN gels. A number of studies have also found that the introduction of different polysaccharide gels (alginate, gellan gum, carrageenan, and agar) as a reversible noncovalent (physical) network into an irreversible covalent network can greatly increase the mechanical properties of their parent single-network (SN) gels, suggesting that different from mechanical enhancement by covalent bonds, physically cross-linked network could also toughen hydrogels via different mechanical enhancement mechanisms. However, it still remains unclear how the fracture of the first, physically linked network affects energy dissipation in the gels as well as how the first, physically linked network interacts with the second chemically linked network to toughen the whole hydrogels. To address the issues above, here we engineered a series of hybrid physically chemically cross-linked Agar/PAAm hydrogels, with particular focus on the effect of the first agar network on the mechanical properties of Agar/PAAm gels. At optimal gel-preparation conditions, Agar/PAAm hydrogel achieved elastic modulus of 313 kPa, tensile strength of 745 kPa, and tearing energies of 1089 J/m2. More importantly, we found that agar concentration (Cagar) needs to be higher than a critical value (Cagar*), so Agar/PAAm DN gel can increase its stiffness and toughness simultaneously. This finding reveals an important and unique phenomenon for hybrid DN gels that the toughness of the gels can be increased with its stiffness, which hopefully provides a different view for design of new stiff and tough hydrogels using hybrid physically/chemically linked network.

2. MATERIALS AND METHODS 2.1. Materials. All chemicals and solvents purchased were of the highest available purity, and unless otherwise stated they were used as received. Agar (gel strength of >800 g cm−2 and melting point of 85− 95 °C) was purchased from Aldrich Inc. 2-Hydroxy-4′-(2-hydoxyethoxy)-2-methylpropiophenone (Irgacure 2959) and acrylamide (AAm) were obtained from TCI China Inc. N,N′-Methylbisacrylamide (MBA) was purchased from Alfa Aesar Inc. 2.2. Preparation of DN Gels. Agar/PAM DN gels were synthesized by a one-pot method as reported in our previous work.36 Unless otherwise stated, the optimal conditions as determined from our previous work (agar of 20 mg mL−1, AM of 3.4 mol L−1, MBA 0.03 mol % of AM, and UV initiator (Irgacure 2959) 1 mol % of AM) were used to prepare Agar/PAAm DN gels. Briefly, all reactants were added into a tube, and the tube was sealed under N2 protection after three degassing cycles and then gradually heated up to 95 °C in an oil bath to dissolve the reactants in the water. The resulting solution was injected into a plastic tube (D = 9 mm) or a curet mold and cooled at 4 °C for 30 min to form an agar gel first. The photopolymerization reaction was carried out to form an Agar/PAM DN gel under UV light (λ = 365 nm wavelength, intensity of 6 W) for 1 h. After polymerization, gels were removed from the molds and used for mechanical tests. B

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Macromolecules 2.3. Characterization. Tearing Test. Tearing testing was performed using commercial test machine. The gel samples were cut into a trousers shape (40 mm in length, 10 mm in width, and 10 mm in thickness) with an initial notch of 20 mm. The two arms of the samples were clamped, in which the one arm was fixed while the other one was pulled upward at a crosshead speed of 50 mm min−1. The tearing energy (T) is defined as the work required to tear a unit area, as estimated by24

T=

2Fav w

At Cagar = 5 mg/mL, tearing energy increased to 347 J/m2. As Cagar > 5 mg/mL, tearing energies was almost tripled from 347 to 1089 J/m2 as Cagar increased from 5 to 30 mg/mL. Tearing energy of ∼1000 J/m2 at Cagar of 20 mg/mL or above was comparable to that of chemically linked PAMPS/PAAm DN gels, cartilage, and natural rubber (102−103 J/m2). To better evaluate the fracture behavior of Agar/PAAm hydrogels, Figure 2 explicitly shows the crack propagation

(1)

where Fav is the average force of peak values during steady-state tear and w is the width of the specimen. Tensile Test. Uniaxial tensile tests of as-prepared gels were carried out using a universal tensile tester equipped with a 100 N load cell at a crosshead speed of 100 mm min−1. The gels were cut into doublebone shape with a gauge length of 25 mm, a width of 4 mm, and a thickness of 1 mm. The fracture strain (εf) was determined as εf = Δl/ l0 (mm/mm), where Δl is the difference of the elongation length (l) and the initial length (l0). The fracture stress (σf) was defined as σf = F/A0, where F is the load force and A0 is the original specimen crosssectional area. The elastic modulus (E) of gels was calculated by fitting the initial linear regime of stress−strain curve and reported as mean and standard deviation (n = 3). Cyclic Test. The energy dissipation or hysteresis of hybrid DN gels was also conducted by above-mentioned tensile tester. The gel specimen was first loaded to λ = 10 with crosshead speed of 100 mm min−1 and then unloaded with the same speed. The dissipated energies (Uhys) were estimated by the area between loading−unloading curves. Rheology Test. The gelation process of agar gel were investigated by rheology experiments and kindly measured at Anton Paar China Inc. by a MCR302 rheometer with C-PTD200 temperature control system. The agar gel with various concentration was first dissolved in water at 95 °C for 7 min to form transparent solution. After 1 min standing, the temperature of the solution was cooled down from 95 to 4 °C with a cooling rate of 2 °C/min. The storage modulus (G′) and loss modulus (G″) of agar gels were recorded during this cooling process with constant strain rate of 1% and frequency of 1 Hz.

3. RESULTS AND DISCUSSION 3.1. Dependence of Tearing Energy on Agar Concentrations. Figure 1 shows the effect of agar

Figure 2. Crack propagation of a notched Agar/PAAm DN hydrogels prepared at agar concentration of (a) 0, (b) 3, (c) 5, and (d) 20 mg/ mL. The initial notch of all tested gels was ∼10 mm in length.

process of notched Agar/PAAm hybrid gels as prepared by different agar concentrations. First, pure PAAm gels and Agar/ PAAm gels with 3 and 5 mg/mL agar are transparent. However, as agar concentration increased to 20 mg/mL, Agar/PAAm gels became opaque. Considering that the double-network hydrogels are highly heterogeneous gels with two strong asymmetric polymer networks, the opaque of the Agar/PAAm gels is attributed to the structural heterogeneity in agar network and asymmetrical entanglement between two networks. Similar transparent/opaque effects were also observed in PEG/PAA DN gels41 and even in agar/agarose single gels duo to their heterogeneous network structure.42,43 Second, as a control, PAAm SN gels without agar exhibited an obvious crack blunting behavior at the notched tip. The blunting developed as the increase of ε from 0 to 2.5, as revealed by a semicircular shaped crack. This indicates that the resistance of crack propagation within a certain range of the strains would be

Figure 1. Effect of agar concentrations on the tearing energy of Agar/ PAAm DN gels.

concentrations on the tearing energy of Agar/PAAm hybrid DN gels, prepared at AAm concentration (3.4 M), cross-linkers (0.03 mol % of AAm), and other components unchanged. Overall, tearing energy depended strongly on agar concentration, and it increased proportionally to agar concentration. As Cagar < 5 mg/mL, tearing energy of DN gels was as low as 100−200 J/m2, comparable to PAAm SN gels (∼100 J/m2).40 C

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Macromolecules negligible, but beyond a critical strain (ε = 2.6 in this case) the PAAm SN gel broken suddenly (Figure 2a). Haque et al.44 also studied the crack propagation of the notched PAAm SN gels. They found the gel was cracked easily at small ε < 1. Different crack behaviors of the same PAAm gels obtained from different laboratories could be resulted from different concentrations of chemical cross-linker. MBA in our PAAm SN gels (0.03 mol % of AAm) was lower than that in theirs gels (0.1 mol % of AAm). Thus, it is not surprising that our PAAm gels showed a better ductile property. Agar/PAAm DN gel prepared with 3 mg/mL agar exhibited a similar fracture behavior to PAAm SN gel, which broken suddenly at a larger fracture strain of 3.0 (Figure 2b). However, for Agar/PAAm gels prepared with the higher agar concentrations of 5 and 20 mg/mL, fracture strains were 3.5 and 4.2, respectively. This indicates that the gels were very tough. Crack blunting occurring in tearing tests (as indicated by a red arrow in Figure 2c,d) showed a high resistance against crack propagation. Take together crack propagation and tearing energy results, when the agar concentration is higher than the critical concentration Cagar* of ∼5 mg/mL (Cagar* is the minimum concentration of agar, at which it can effectively toughen the chemically linked PAAm network), it will promote inter- and intranetwork interactions via agar association and chain entanglement with PAAm, resulting in the increase of gel strength.36 A number of studies30,35,36,38,45,46 have found that the introduction of physically cross-linked polysaccharides (e.g., agar, alginate, gellan gum, carrageenan, and konjac glucomannan) into a covalent network enables to toughen the hybrid DN gels. But, this work, for the first time, demonstrates that the toughening behavior of hybrid gels is concentration dependent on the first, physically linked network; i.e., only if the physically linked network concentration is higher than Cagar*, the gel toughening effect can be realized. 3.2. Dependence of Tensile Properties on Agar Concentrations. We further conducted a series of tensile tests to investigate the effects of agar concentration on mechanical properties of Agar/PAAm DN gels. Figure 3

Table 1. Mechanical Properties of Agar/PAAm DN Gels with Various Agar Concentrations Cagar (mg/mL)

E (kPa)

0 1 2 3 5 10 15 20 30

7 6 5 6 13 76 136 182 313

σy (kPa)

σf (kPa)

εf (mm/mm)

W (MJ/m3)

29 49 81 111 181

265 490 320 540 423 511 587 676 745

18.22 22.84 27.90 24.60 33.05 27.31 26.68 28.29 26.69

1.8 3.6 3.2 3.8 5.4 6.7 7.3 8.5 9.2

1, with the increase of Cagar above 5 mg/mL, the gels showed prominent enhancement in elastic modulus (E = 13−313 kPa), fracture stress (σf = 423−745 kPa), and dissipated energy (W = 5.4−9.2 MJ/m3) as compared to E = 5−7 kPa, σf = 265−540 kPa, and W = 1.8−3.8 MJ/m3 of the gels at CAgar of 0−3 mg/ mL. Further increases in CAgar from 5 to 30 mg/mL led to slightly increases in the fracture stress, which might be attributed to the increased rigidity of the network, which have more cross-links and entanglements at the higher agar content. It should be mentioned that Agar/PAAm gels prepared with agar concentrations of >20 mg/mL were highly tough, evidenced by their high elongation at break of more than 2500%, comparable to conventional chemically linked PAMPS/ PAAm DN gel. Figure 4 shows different mechanical properties of gels as a function of agar concentration. It can be clearly seen that the yielding strength, fracture stress, elastic molecules, and tearing energies increased almost linearly as agar concentrations, with R2 values of 0.948−0.996. This indicates that the mechanical properties (stiffness and toughness) of Agar/PAAm gels can be directly tuned by agar concentrations. Actually, the mechanical properties of Agar/PAAm gels also were influenced by AAm concentrations (i.e., second network monomer concentrations). Our previous studies have shown that at a high AAm concentration (∼7 M) the mechanical properties of Agar/ PAAm gels exhibited a weak dependence on agar concentration. However, at moderate AAm concentration (∼3 M), the increase of agar concentration introduces a delicate balance for sustaining the fracture stress of the gels between the enhancement of the first network and the reduction of internetwork entanglement; thus, the fracture stress of the gels is largely affected by agar concentration. Here, we used a moderate AAm concentration of 3.4 M to prepare all gels and will not discuss the effect of the second network concentration on the mechanical properties of Agar/PAAm gels, which can be found in our previous studies.38 3.3. Gelation of Agar SN Gels. To better understand the physicomechanical properties of Agar/PAAm DN gels using agar gel as the first network, we also explicitly examined the gelation of agar single network gel (SN gel) with various agar concentrations using the bottle inversion method. As shown in Figure 5a, agar formed a solid gel when its concentrations were higher than 3 mg/mL. The agar SN gel prepared by 3 mg/mL agar was so soft that it behaved like viscous liquid and lacked any mechanical properties (Figure 5b). The agar gels prepared by 5 mg/mL agar can form a solid-like gel, but they were still very mechanically weak and easily broken by gentle finger compression because of its brittleness (Figure 5b,c).

Figure 3. Tensile stress−strain curves of Agar/PAAm DN gels prepared with various agar concentrations.

shows the tensile stress−strain curves of Agar/PAAm hybrid DN gels with varied agar concentrations, while Table 1 summarizes the mechanical properties of the Agar/PAAm DN gels. Apparently, the mechanical properties of gels have strong dependence on CAgar. In Figure 3, as CAgar ≥ 5 mg/mL, all hybrid DN gels showed clear yielding phenomenon around strains of 0.8, and the yield stress increased from 29 to 181 kPa, as agar concentrations increased from 5 to 30 mg/mL. In Table D

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Figure 4. (a) Yielding stress, (b) fracture stress, (c) elastic modulus, and (d) tearing energy of Agar/PAAm DN gels as a function of agar concentration.

Figure 5. (a) Aqueous agar solutions with various concentrations after storing at 4 °C overnight. (b) Formation of agar gels at 3, 5, and 10 mg/mL. (c) Finger compression of 5 mg/mL agar gel.

Rheology tests were also conducted to reveal the gelation process of agar gel by varying temperatures and agar concentrations. As a hydrogel exhibits viscoelastic behaviors, the storage (G′) and loss (G″) moduli are used to measure its elastic and viscous components. Figure 6a clearly showed that both the G′ and G″ values of the hydrogels increased rapidly as temperature was dropped from 90 to 4 °C. This indicates that (i) the gelled state can be maintained at lower temperatures and (ii) the hydrogel becomes even weaker and softened at an elevated temperature due to the dynamic breakage of intermolecular hydrogen-bonding cross-linking formed between agar helices. Agar SN gels also showed a sol-to-gel transition at 42.8 °C (Figure 6a); i.e., at temperatures of 42.8 °C, an opposite trend was observed (i.e., G′ > G″). This sol-to-gel transition temperature of 42.8 °C is consistent with the temperatures reported in previous works.47,48 3 mg/mL of agar gel yielded

Figure 6. (a) Variation in storage (G′) and loss (G″) moduli of agar SN gels as a function of temperature from 90 to 4 °C. (b) Storage moduli (G′) of agar SN gels as a function of agar concentration at 20 °C.

very elastic network (i.e., G′ > G″ below 42.8 °C), consistent with Figure 3a. As agar concentration increased from 3 to 20 mg/mL, G′ was measured as 41 Pa at 3 mg/mL, 846 Pa at 5 mg/mL, 7795 Pa at 10 mg/mL, 11 304 Pa at 15 mg/mL, and 13 526 Pa at 20 mg/mL (Figure 6b). The marked linear E

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Macromolecules increase in G′ with agar content in the physically cross-linked network indicates the existence of strong interactions between agar chains. This interaction leads to an increase of crosslinking density and consequently an enhancement of the stiffness of agar hydrogels. Combining with tensile results from Agar/PAAm DN gels, 3 mg/mL of agar gel is too soft to dissipate energy upon the fracture of the first agar network and thus cannot enhance the toughness of hybrid DN gels. Instead, 5 mg/mL of agar gel exhibits relatively higher cross-linking density; even after applying a small strain, the effective elastic chains of agars in the first network will be fractured, resulting in the formation of a large damage zone (softened zone) to suppress crack propagation and thus the enhanced toughness of hybrid DN gels. 3.4. Mechanism of High Stiffness and Toughness of DN Gels. It is generally accepted that stiffness and toughness of materials are two opposite mechanical parameters. But, the inverse relation between stiffness and toughness no longer holds true in our physically chemically linked DN gels. As shown in Figure 4c,d, the stiffness and toughness of hybrid DN gels increased simultaneously as the increase of agar concentrations. This distinct phenomenon is likely attributed to the opposite feature of the two networks and the unique toughening mechanism of DN gels. Toughness Enhancement. Since the first, physically linked agar network is formed by agar helical bundles through hydrogen bonds between agar helices, the first agar network provides a reversible and flexible structure for agar chains to transition between the association and disassociation states. Unlike chemical bond breaking in the chemically linked first network, the fracture of the physically linked agar network is governed by the chain pulling-out mode,39 which enables to effectively dissipate energy in the networks. This was demonstrated by performing the loading−unloading tests on fresh hydrogels. As shown in Figure 7a, all Agar/PAAm gels exhibited obvious hysteresis loops after the rupture of the agar network, and the area of hysteresis loops increased as agar concentration. Energy dissipation can be evaluated by the area of the hysteresis loop encompassed by the loading−unloading curve (Figure 7b). The energy dissipation of the loading− unloading cycle (ΔU) increased almost linearly with the Cagar value at λ = 10. This indicates that the gels prepared with higher agar concentrations can dissipate energy more efficiently. As a result, the toughness of Agar/PAAm hybrid DN gels is enhanced at higher agar concentrations. This result is consistent with the tensile behavior in Table 1 and tearing energy in Figure 1. Xin et al.49 have reported that the strength and toughness of chemical PNVP/PAAc DN gels increased largely as the increase of cross-linker or monomer concentration of the first network, indicating that the strength and toughness of chemical DN gels were also great affected by the first network topology. The toughness of the first chemical network was modeled by the Lake−Thomas theory, in which the fracture toughness of the fully chemical cross-linked DN gel was directly proportional to the toughness of the first chemical network. However, in this work, a linear relationship between storage modulus of agar SN gel and agar concentration (Figure 6b) as well as between toughness of hybrid DN gels and agar concentration (Figure 4d) suggests that the stif f ness of the first physical network has a large impact on the toughness of hybrid DN gels. The discrepancy between our and Xin’s works, in which the toughness of DN gels is determined by toughness vs stiffness of first network, could be interpreted by the differences

Figure 7. (a) Loading−unloading curves of hybrid Agar/PAAm DN gels with various agar concentration at λ = 10. (b) Energy dissipation of the loading−unloading loop as a function of agar concentration at λ = 10.

in the first network structure. In physical gels, Kong et al.50 have identified that the elastic moduli and toughness of physical gels increase with cross-linking density, whereas the stiffness and toughness are negatively correlated in chemical gels. So, it could be derived that both the stiffness and toughness of agar gel would increase as agar concentration. From this viewpoint, the toughness of all the DN gels is directly proportional to the toughness of first network, regardless of whether the first network is chemical or physical cross-linked. Stiffness Enhancement. Owing to different physical characteristics of the two networks, the first network is easily fractured as small strains, while the second network cannot bear stress but has very good extensibility. Nakajima et al.51 proposed a two-step internal fracture of the PAMPS network in PAMPS/PAAm DN gels. First, the elastically effective chains of the first PAMPS network are fractured. Upon chain fracture, the PAMPS network becomes discontinuous and hardly bears the more and stronger stress even at small strain, and PAMPS chains do not contribute to the initial elastic modulus (EDN). After that as applying larger strains, the stress will be transferred from the PAAm network to the PAMPS small gel clusters (microgels), because of the soft nature of PAAm network and strong chain entanglement between the two networks. Different from PAMPS/PAAm DN gels, our hybrid DN gels did not experience a continuous−discontinuous structural transition during the internal fracture of the first agar network, but the stress still transfers from the PAAm network to the partially fractured agar network at larger strains. The rigid and brittle first network can bear most of stress before the strain hardening region of the gels, implying that the stiffness of the first network is also important for the high mechanical properties of DN gels. We previously proposed that the elastic modulus of DN gels F

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Macromolecules can be considered as a sum of the moduli of the two networks (EDN = EAgar + EPAAm).39 The elastic modulus of the PAAm component (EPAAm), which is approximately close to that of PAM SN gels, is treated as a constant because no any mechanical hysteresis was found in our previous work.36 Therefore, the EDN varies directly as EAgar; i.e., the stiffness of DN gels is determined by the stiffness of the first agar network. EAgar can be estimated by the agar SN gels using rheology tests under an assumption that the SN gel follows the rubber elastic theory (EAgar = 3G′Agar). As shown in Figure 6b, G′Agar increased linearly as agar concentration, indicating that the EDN will increase as the moduli of first network increases. As a result, the stiffness of Agar/PAAm DN gels increases as the increase of agar concentration. Interestingly, some evidence have been observed for simultaneous enhancement of hydrogel stiffness and toughness in other hybrid DN gels. Li et al.40 found that both elastic modulus and fracture energies of Ca2+−alginate/PAAm hybrid gels increased as ionic cross-link density of alginate network by Ca2+ (CaSO4/alginate