High-Strength and Tough Cellulose Hydrogels Dual-Chemically Cross

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High-Strength and Tough Cellulose Hydrogels Dual-Chemically Cross-linked by Using Low- and High-Molecular Weight Cross-linkers Dongdong Ye, Chunyu Chang, and Lina Zhang Biomacromolecules, Just Accepted Manuscript • Publication Date (Web): 25 Mar 2019 Downloaded from http://pubs.acs.org on March 25, 2019

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High-Strength and Tough Cellulose Hydrogels DualChemically Cross-linked by Using Low- and High-Molecular Weight Cross-linkers Dongdong Ye, †,‡ Chunyu Chang,†,* Lina Zhang†,* † College ‡ School

of Chemistry and Molecular Sciences, Wuhan University, Wuhan 430072, China.

of Textile Materials and Engineering, Wuyi University, Jiangmen 529020, China

ABSTRACT Hydrogels are the focus of extensive research interests due to their potential application in fields of biomedical materials, biosensors, agriculture, and cosmetics. Natural polysaccharide is one of good candidates of these hydrogels. However, the weak mechanical properties of cellulose hydrogels greatly limit their practical application. Here, dual chemically cross-linked cellulose hydrogels (DCHs) were constructed by sequential reaction of cellulose with low- and highmolecular-weight cross-linkers to obtain relatively short chains and long chains crosslinking networks. Both the distribution and density of the cross-linking domains in the hydrogel networks were monitored by 3D Raman microscopic imaging technique. Interestingly, the ruptured stress of DCHs in tensile and compressive tests were 1.7 MPa and 9.4 MPa, which were 26.3- and 83.9-fold larger than those of single chemically cross-linked cellulose hydrogel (SCH). The reinforcement mechanism of DCH was proposed as that the breaking of the short chains cross-linking in the networks effectively dissipated mechanical energy, and the extensibility of the relatively long chains cross-linking maintained the elasticity of DCH. Therefore, both the strength and toughness of DCH enhanced, and the dual networks consisted of the short chains and long chains cross-linking played an important role in the improvement of the mechanical properties of the cellulose hydrogels.

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The application prospect of the robust cellulose hydrogels with bimodal network structure would be greatly broadened in the sustainable biopolymer fields. INTRODUCTION Owing to the unique integrate of solid and large amount of water, hydrogels that resemble the extracellular environment of body’s tissues are extensively explored and widely used in medical implants,1 biosensors,2 scaffolds for tissue engineering,3 coating for medical devices,4 and cosmetics.5 However, conventional hydrogels are usually extremely brittle and fragile after full swelling, which seriously limits their practical application.6-9 Multi-mechanism design, including the introduction of sliding cross-linkers,10 double networks,11,12 hybrid cross-linking,8,13 nanocomposites14, 15 or highly oriented hierarchical structure,16 have been actualized to enhance the mechanical strength and fracture toughness of hydrogels. For example, the reinforcement mechanism for double network hydrogels is the successive rupture of the first, brittle and tightly cross-linked network for effectively dissipating mechanical energy and the second, ductile and loosely cross-linked network for maintaining the network elasticity. The co-existence of weak and strong network or crosslinks can achieve balance in rupturing mechanical energy and maintaining elastic configuration.17 Although these breakthroughs have been achieved, it is still a challenge to develop hydrogels with both improved strength and toughness. In recent years, biomass resources have been fascinating due to the pollution of petroleumbased plastic waste and the depletion of petroleum resources, and the researches of natural polymers have entered a period of rapid development due to their biologically renewable, biocompatible, and biodegradable properties. In particular, cellulose, the most abundant natural crystalline polysaccharide, has become a research hotspot.18 Transparent and relatively weak cellulose hydrogels have been prepared by chemical crosslinking of cellulose chains in alkali/urea aqueous solution.19 To enhance the mechanical properties of cellulose hydrogels, we successively 2 ACS Paragon Plus Environment

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constructed tough mechano-responsive cellulose hydrogels by utilizing a hybrid loosely chemical crosslinking and densely chemical crosslinking strategy20 and robust anisotropic cellulose hydrogels with a pre-stretching-assisted dual crosslinking strategy21, greatly broadening their application in scope of force sensing or inducing cell alignment. In this work, we designed and fabricated robust and tough cellulose hydrogels by using an ingenious dual chemical crosslinking strategy, where low- and high-molecular-weight cross-linkers were successively employed for fabrication of short chains and long chains crosslinking networks of cellulose. These cellulose hydrogels exhibited high mechanical strength and toughness, as a result of the existence of the short- and long- chains dual-chemical crosslinking networks. The homogeneous networks constructed by the dual-chemical crosslinking with low- and high-molecular-weight cross-linkers contributed to the strength and elasticity of the cellulose hydrogels. This work provided a novel strategy for constructing robust hydrogel materials derived from sustainable biomacromolecules. EXPERIMENTAL SECTION Materials. Cellulose (cotton linter pulp) was provided by Hubei Chemical Fiber Group Ltd. (Xiangfan, China). The cotton linter pulp was used after complete drying under vacuum at 80 °C and without further purification. The viscosity-average molecular weight of the cotton linter pulp in cadoxen was determined to be 9.6104 (degree of polymerization, DP=600) according to the Mark-Houwink equation [η] (mL g-1) =3.8510-2 (Mw)0.76 and using an Ubbelohde viscometer at 25 °C. NaOH, urea, epichlorohydrin (ECH, 1.18 g ml-1) and polyethylene glycol diglycidyl ether (PEGDE, Mn=500) were purchased from Sinopharm Chemical Reagent Co., Ltd. (Shanghai, China). All of the reagents were used as received unless otherwise noted. Fabrication of the single chemically cross-linked cellulose hydrogel (SCH). SCH

was

fabricated as reported in our previous work19: cellulose solution (4 wt%) was prepared by dissolving cotton linter pulp (4g) in a precooled (-12°C) aqueous solution (96 g, 7 wt% NaOH/12 3 ACS Paragon Plus Environment


wt% urea/81 wt% H2O) within 2 min, to which low-molecular-weight chemical cross-linker ECH (3 ml) was added dropwise to the above bubbles-removed cellulose solution (80 g) at 0 °C for homogeneous mixing (2 h). The resultant solution was transferred into hand-made cuboid-shaped, spherical, plane-shaped or hand-shaped molds and kept at 60 °C for 2 h to form the chemical gels. After washing by distilled water, the colorless and transparent chemical hydrogels were prepared. Preparation of the dual chemically cross-linked cellulose hydrogels (DCHs). The SCH specimen was immersed in alkaline solution including 1 mol L-1 NaOH and certain concentrations of high-molecular-weight cross-linker PEGDE (0.57 mol L-1 and 1.14 mol L-1) and then reacted at 60 °C for 3 h to form the secondary crosslinking. After thoroughly washing with water, the dualcross-linked cellulose hydrogels (DCHs) were obtained and were coded as DCH1 and DCH2, respectively. Measurement. Raman spectroscopy and spatial Raman mapping were performed using a Raman imaging microscope (Thermo Scientific DXR xii, USA). The wavelength of the excitation laser was 532 nm. Raman maps (scan range 20 μm ×20 μm; depth of scanning, 20 μm) were collected using a spatial resolution of 500nm. The collected spectra were preprocessed using cosmic ray removal, noise filtering, and normalization techniques. The MCR method developed by OMINC software was applied for calculating the chemical cross-linked domains. Atomic force microscopy (AFM) images were recorded on a CypherTM S (Asylum Research) equipped with a blue Drive photothermic excitation option to ensure a stable oscillation of the beam even in ﬂuid environment. Besides, triangular probes (SNL-10, BRUKER) with average tip radius of 2 nm, spring constant of 0.34 N/m, and resonance frequency of 60 kHz were employed for scanning to investigate the hydrogels in a fluid environment. All imaging results were analyzed using the AFM accessory software (Gwyddion). Scanning electron microscopy (SEM) images of hydrogels were taken with a field emission 4 ACS Paragon Plus Environment

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scanning electron microscopy (FESEM, Zeiss, SIGMA, Germany) using an accelerating voltage of 5 kV. Before testing, cellulose hydrogels were frozen in liquid nitrogen, snapped immediately, and freeze-dried to remove the water. Both the surfaces and cross-sections of the dried hydrogels were coated with gold vapor prior to imaging. Solid-state

13C

cross-polarization magic angle spinning (13C CPMAS) nuclear magnetic

resonance (NMR) experiments were carried out on a Bruker AVANCE III WB spectrometer (Rheinstetten, Germany). During the test, the magic angle rotation speed was 5 kHz, the contact time was 20 ms, the acquisition time was 1 s, and the spectrum was superimposed 2000 times. The samples were cut into powder before testing and dried at 80 °C in vacuum. The FTIR spectra of dried cellulose hydrogels were recorded in the wavenumber range from 3500 to 500 cm-1 using a Fourier transform infrared spectrometer (FTIR, Perkin Elmer Spectrum). Mechanical tests of the cellulose hydrogels were performed on an INSTRON instrument (Model 5576, USA). The rectangular cellulose hydrogels (2 mm thick and 10 mm wide) were stretched at a speed of 3 mm min-1 and the cylindrical cellulose hydrogel (height: 10-15 mm and diameter: 10 mm) were compressed at a speed of 1 mm min-1. Cyclic tests were carried out by performing subsequent trials immediately after the initial loading. A displacement-controlled nanoindenter machine (Piuma Nanoindenter by Optics11, Netherlands) equipped with a controller, an optical fiber and a spherical probe (Optics, Netherlands) was used to investigate the force-displacement curves on surface of hydrogels in the fluid environment at room temperature. In this work, two kinds of probes with cantilever stiffness of 3.32 N/m and 45.5 N/m, corresponding with tip radius of 46 mm and 25 mm, tested the cellulose hydrogels with primary and secondary chemical crosslinking, respectively. The effective Young’s modulus was calculated using the Oliver & Pharr theory22 from the slope of the initial portion between 65% and 85% of the unloading curve according to equation: 5 ACS Paragon Plus Environment


𝐸𝑛 =

𝑆 2𝑟1/2 ℎ𝑚𝑎𝑥 ― ℎ𝑓𝑖𝑛𝑎𝑙

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(1)

where S is the slope of the initial portion of unloading curve reflecting the elastic unloading stiffness, r is the spherical indenter radius, and hmax depth, respectively. The grid scan was 10 × 10 points, and the point-to-point pitch is 20 m. The water content of cellulose hydrogels were measured in a procedure as follows:

S r (%) 

Wwet  Wdry Wwet

(2)

100%

where Wwet is the weight of cellulose hydrogel with full swelling, and Wdry is the weight of dried hydrogel. The digital pictures of hydrogels were taken photos with a camera (A6000, Sony, Japan). The pictures were just cutting into needed shapes as Figure S1. RESULTS AND DISCUSSION Construction of high-strength cellulose hydrogels via dual chemical crosslinking strategy Figure 1a shows the schematic diagram for fabrication of dual chemically cross-linked cellulose hydrogel (DCH). Firstly, cellulose (cotton linter pulps) was dissolved in NaOH/urea aqueous solution at -12℃. Then, single chemically cross-linked cellulose hydrogel (SCH) was synthesized by crosslinking of cellulose chains with certain amount of low-molecular-weight cross-linker, epichlorohydrin (ECH). After washing thoroughly, SCH was immersed in alkaline solution containing high-molecular-weight cross-linker, polyethylene glycol diglycidyl ether (PEGDE), for further crosslinking reaction. After thoroughly washing with deionized water for removal of alkali and unreacted PEGDE, thus DCH with dual cross-linked network was constructed.


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Figure 1. Fabrication of the weak SCH and high-strength DCHs. (a) Schematic illustration of constituting the DCH via a dual chemical crosslinking strategy of cellulose hydrogels. (b, c) Representative photographs of SCH and DCHs. (d) Photographs of SCH and DCHs under compression. As shown in Figures 1b, c and S1, the volume of the resultant DCHs are greatly reduced compared with SCH, because the increased chemical crosslinking points firmly fixed the cellulose molecular chain and limited the swelling behavior of DCHs. Thus, the water content of the gel samples was significantly decreased from 99.3% in SCH to 92.7% in DCH1 and 87.4% in DCH2. Furthermore, rebounding experiments of SCH and DCH (Figure S2) showed that DCH possessed better rebounding ability compared to SCH. It was not hard to imagine that DCH samples with dual chemically cross-linked networks had more dense structure and higher elastic modulus. On the 7 ACS Paragon Plus Environment


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contrary, SCH sample with loosely cross-linked structure showed poor elastic behavior (Movies S1). Actually, the SCH displayed a fragile performance, whereas DCHs exhibited strong and tough behavior, and rapidly recovered once external force was removed during the compression process (Figure 1d). As the external force applied on the samples increased, the evolvement of hydrogel networks could be divided into three stages. (i) Hydrogel networks deformed reversibly and the mechanical properties of DCHs located in linear region. (ii) When the external force reached a critical value, the taut short-chains cross-linked networks were destroyed to dissipate mechanical energy, whereas the relatively long-chains cross-linked networks could maintain the elasticity of hydrogels.27 (iii) After further increasing external force, the long-chains cross-linked networks gradually deformed until DCHs completely damaged. Visual observation of the dual chemical crosslinking reactions via 3D Raman technology The chemical crosslinking reaction was firstly confirmed by the NMR and a visual 3D Raman technology (Figure 2). As shown in Figure 2a, the chemical structure of crosslinking agent PEGDE was characterized by NMR spectroscopic analysis before using, demonstrating that each carbon resonance was assigned to corresponding group as reported23: 44.3, 72.0, 50.9 and 70.6 ppm were assigned to methylene carbon of the epoxide groups, methane carbons of the epoxide groups, methylene carbon of the end units, and methylene carbons of PEG, respectively. Moreover, the integration of 70.6 ppm lines was 6.9 after normalization other carbon (a, b, or c) as 1. Therefore, the DP of the PEG moiety of PEGDE was determined to be 6.9 and the average Mw of PEDGE was 417, apparently higher than that of ECH. Figure 2b shows a solid state

13C

NMR spectra of

cellulosic cotton linter, SCH and DCH. These results revealed that the cellulose exhibited a typical cellulose I structure24 where the chemical shift data of cellulose glucose unit, such as C1 (~107 ppm, ~105ppm), C4 (~90 ppm, crystallization zone), C2,3,5 (~76 ppm, ~74 ppm and ~73 ppm, crystallization zone) and C6 (66 ppm, crystallization zone) was recognized. After dissolved in 8 ACS Paragon Plus Environment

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Figure 2. (a) Quantitative 13C NMR spectrum of PEGDE in D2O at 300k. (b) Solid-state CP/MAS 13C

NMR spectra of the cotton linter, SCH and DCH. (c) 3D Raman images, reconstructed 2D

image from the -OH stretching intensities (3000-3400 cm-1), and Raman spectra of chemically cross-linked and uncross-linked domains within the SCH derived from MCR (multivariate curve resolution) model with OMNIC software. (d) 3D Raman image, 2D Raman image, and 1D Raman spectra of DCH. Red and green corresponded to the chemically cross-linked domains, and blue indicated the uncross-linked domains. Scale bar = 5μm.



NaOH/urea aqueous solution and cross-linked with epichlorohydrin, the resultant SCH sample exhibited a normal amorphous structure, where the chemical shift (~90 ppm) of the C4 crystallographic region shifted to the amorphous region (~83 ppm), and the chemical shift of the C6 crystalline region (66 ppm) moved to ~62 ppm. The results indicated that chemical crosslinking reaction could significantly destroyed the hydrogen bond interaction between cellulose chains, leading to the increase of the proportion of amorphous regions, and the decrease of the crystallinity of the cellulose hydrogel. Interestingly, the chemical signal of methylene carbons of PEG moiety (72.0 ppm) remained after the introduction of the second high-molecular-weight cross-linker PEGDE, revealing that PEGDE successfully reacted with hydroxyl groups of cellulose in hydrogel networks. Moreover, FTIR and Raman characterizations of dried SCH and DCHs was performed to clarify the composition of cellulose before and after introduction of cross-linkers (Figure S3, S4). The stretching and bending vibration peaks of PEGDE existed in DCHs, confirming the existence of a secondary crosslinking reaction. Raman spatial imaging technology is a convenient and accurate experimental method for distinguishing the composition and distribution of chemical crosslinking regions inside hydrogels.25,26 Here, the distribution of crosslinking regions in hydrogels after the first and secondary chemical crosslinking reactions was monitored by using Raman technology. As shown in Figures 2c, d, the red-green regions in 3D and reconstructed 2D images represented the unreacted hydroxyl groups of cellulose and the blue regions could be assigned to the cross-linked domains where the signal of hydroxyl groups was greatly reduced by reacting with PEGDE, based on the analysis of the corresponding Raman spectra. The reconstructed 2D Raman image and the corresponding Raman spectral curves of SCH specimen are shown in Figure 2c. There was a higher intensity at a range of 3000-3400 cm-1 (-OH stretching vibration) than that from blue region spectrum captured from red-green region in SCH, suggesting that the blue regions represented the 10 ACS Paragon Plus Environment

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crosslinking region whereas the red-green region represented the uncross-linked regions. From the analysis of the 3D Raman images of SCH and DCH, the blue regions, reflecting the chemical crosslinking, were evenly distributed in both SCH and DCH hydrogels, and the uncross-linked regions (see red-green region in Figure 2d) in the DCH obviously decreased, further proving the dense and homogeneous dual-crosslinking structure of DCH. Morphology changing of hydrogels in dual chemical crosslinking reactions To clarify the relationship between morphology and crosslinking process, the surface and internal microstructure of SCH and DCHs were in detail characterized by SEM and AFM. Obviously, there is a structural densification in subsequently crosslinking process as shown in Figure 3a, consistent with decreased water content as mentioned above. Comparing with the surface morphology of SCH and DCH1, the surface porous structure of the DCH2 sample decreased significantly after a second crosslinking by using higher concentration of the PEGDE cross-linker, and the pore size in its cross-section became small. This surface and cross-section morphology of DCH2 was correlated to PEGDE, suggesting higher crosslinking density and denser microstructure of DCH2. Moreover, the surface topography of the wet DCH2 specimen and the internal structure of the same sample after freeze-drying were carefully investigated by using AFM and SEM techniques, respectively (Figure 3b-d). The microporous-structure almost could not be observed on the surface of the wet DCH2 hydrogel sample. However, after freeze-drying, the internal morphology of the dried hydrogel sample was observed along different directions (yellow and pink arrows), as shown in Figure 3d. These results indicated that dried DCHs had hierarchical porous morphology where the microporous structure of SCH was still retained within DCH.



Figure 3. Morphology of SCH and DCH specimens. (a) SEM surface and cross-section images of SCH, DCH1 and DCH2. (b) AFM height image of DCH2. (c, d) Cross-section SEM images of DCH2.

Mechanical properties of the dual chemical cross-linked cellulose hydrogels The mechanical properties of cellulose hydrogels were investigated to further clarify the relationship between the constructed strategy and mechanical performance of hydrogels. As shown in Figure 4a, the fracture strength and toughness (the integral area under the curve) of SCH specimen were 66.0 kPa and 13.3 kJ m-3 with a ruptured strain of 59.5% from the tensile stressstrain curve. Remarkably, the tensile strength and toughness of DCH1 reached 1.1 MPa and 460.1 kJ m-3, which were 16.5 times and 34.6 times higher than those of SCH, respectively. Simultaneously, the ruptured strain of DCH1 was 94.5%, which was 1.6 times that of SCH. After optimizing the secondary crosslinking, the fracture strength and toughness further increased to 1.7 12 ACS Paragon Plus Environment

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MPa and 576.9 kJ m-3, which were 26.3 times and 43.4 times higher than those of SCH, respectively. These results confirmed that DCHs displayed a fulfilling improvement of both strength and toughness, compared with SCH. Moreover, the enhancement trends of cellulose hydrogels after introduction of PEGDE were also confirmed with compressive stress-strain tests (Figure 4b), where the compressive strength and ruptured strain of DCHs were much higher than those of SCH samples. Specifically, the fracture strength of DCH2 reached medially to 9.4 MPa, which was 84 times that of SCH. As shown in Figure 4c, the DCH hydrogel fabricated via dual chemical crosslinking strategy in this work exhibited a significantly enhanced mechanical strength compared with the reported cellulose hydrogels. It was demonstrated that the mechanical strength of the dual chemically cross-linked cellulose hydrogel could be enhanced by increasing the linking chain length in hydrogel networks. As mentioned above, the water content cellulose hydrogels were significantly reduced from 99.3% in SCH to 92.7% in DCH1 or 87.4% in DCH2. The enhancement of mechanical properties of cellulose hydrogels was derived from crosslinking strategy instead of the difference in moisture content. To illustrate, the water content of SCHs were regulated from 99.3% to 84.3% by evaporation of water, and the compressive tests of cellulose hydrogels were conducted under the corresponding moisture content (Figure 4d). The compressive strength of the partially dehydrated SCHs (88.0%) were only enhanced to 0.24 MPa, which was just 3.6 times higher than that under water content of 99.3%, while the DCH2 (water content, 87.4%) had an average compressive strength of near 9.35MPa. These results confirmed that the both the strength and toughness of DCH with dual chemical cross-linked networks significantly enhanced. To further evaluate the uniformity of mechanical distribution, we conducted nanoindentation experiment according to Oliver & Pharr compliance method.22 The load-displacement curves of SCH and DCHs are shown in Figure 4e, which were one of 100 points from the right 200 μm × 200 μm regions, respectively. The effective Young’s modulus, n, was calculated. The distribution 13 ACS Paragon Plus Environment


of n on SCH ranged from 30 to 50 kPa, whereas the average n values of DCH1 reached 250 kPa with a uniform distribution. After optimizing the secondary crosslinking density, n values of DCH2 further rose to 1150~1200 kPa. This trend was consistent with those results of tensile and compressive tests, further proving the feasibility of strengthening and toughening cellulose hydrogels with dual chemically cross-linked strategy. Additionally, the DCHs even can be gamed as Newton Pendulum (Figure 4f; Movie S2) to keep shape and rebound under large external force. To investigate the mechanism of dual chemical crosslinking strategy in strengthening and toughening cellulose hydrogel, cyclic compressive tests were conducted in detail (Figure 4g). Apparently, the compressive curves of SCH samples from the second to tenth cycles almost coincided with the first one with a maximum compressive strain of 60%, demonstrating that the SCH with single cross-linked networks and high water content could only preserve its physical properties under a small compression force of tens of kilopascals before destruction. In contrast, the areas of hysteresis loops in the 2-10th compressive curves of the DCHs sharply reduced compared to that in the first compressive curve, revealing that the damage of sacrificial bonds (ECH cross-linked structure) in the dense hydrogel networks was irreversible, which could dissipate large amount of mechanical energy, leading to high compressive strength and toughness. Importantly, DCH2 had the similar mechanical performance during the cyclic compressive testing, except higher compressive strength and larger energy dissipation, in comparison to DCH1. Furthermore, as the compressive strains of hydrogel samples increased from 10% to 60% with a constant step of 10%, the hysteresis of SCH could be gradually observed in the loading-unloading curves. For DCHs, larger hysteresis loops were found in the curves, indicating more mechanical energy was dissipated from the dense networks under the same test mode.


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Figure 4. Mechanical performance of single and dual chemically cross-linked cellulose hydrogels. (a) Tensile stress-strain curves of cellulose hydrogels. (b) Compressive stress-strain curves of cellulose hydrogels. (c) The mechanical properties of the DCHs and other all cellulose-based hydrogels, including chemical cross-linked cellulose hydrogel,19 physically cross-linked cellulose hydrogel,26,28 physically and chemically hybrid dual cross-linked cellulose hydrogel,20,26 and anisotropic dual cross-linked cellulose hydrogels.21 (d) Effect of water content on mechanical properties of SCH. (e) Force-displacement curves of cellulose hydrogels from a displacementcontrolled nanoindenter. Representative Young’s modulus surface space map including one hundred points with point-to-point pitch of 20 μm of SCH, DCH1 and DCH2 from nanoindentation measurements, respectively. (f) Photographs of dual cross-linked cellulose hydrogels with high elasticity. (g) Cyclic compressive stress-strain curves of SCH, DCH1 and DCH2 with maximum strain of 60% and incremental strains, respectively.



Usually, the network containing all shorts chains is brittle due to the small extensibility, whereas the extensibility of the network containing all long chains is good, but low ultimate strength, so dual-chemically cross-linked networks containing long-chain and short-chain linking have very good ultimate properties.27 In view of the above experimental results, the reinforcement mechanism of the DCHs with dual chemically cross-linked structure was proposed as follows. The breaking of the short chains cross-linking in the networks effectively dissipated mechanical energy, and the extensibility of the relatively long chains cross-linking maintained the elasticity of DCH, ultimately leading to the high strength and toughness. Therefore, the dual networks constructed by chemical cross-linking with relatively short chains and long chains played an important role in the improvement of the mechanical properties of hydrogels. In our findings, the unique energy dissipation and the extensibility of the long chains cross-linking network endowed the DCHs with simultaneously enhanced strength and toughness. CONCLUSION In conclusion, robust and tough cellulose hydrogels (DCHs) were constructed successfully with dual chemical cross-linking strategy, where low- and high-molecular-weight cross-linkers were used to crosslink the cellulose chains to obtain short- and long-chains crosslinking networks. In our findings, the network containing all shorts chains was brittle, however the DCH hydrogels with dual-chemically cross-linked networks with short- and long-chains exhibited ultimately the excellent strength and toughness. The breaking of the short chains cross-linking in the networks effectively dissipated mechanical energy, and the extensibility of the relatively long chains crosslinking maintained the elasticity of DCH. The synergistic effect of two crosslinking points endowed the DCHs with simultaneously enhanced high strength and toughness. Specifically, the fracture strength of DCHs in tensile and compressive tests reached 1.7 MPa and 9.4 MPa, which were 26.316 ACS Paragon Plus Environment

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and 83.9-fold larger than those of SCH, respectively. This work provided a novel strategy for developing sustainable polymer-based hydrogel materials with the densified structure and attractive mechanical properties and greatly broadening the application prospect of biomass resource. ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website at DOI:xxxx. FTIR of PEDGE, SCH and DCHs (PDF). Movies S1. Mechanical differentiation of SCH and DCHs (MPG). Movies S2. Dual chemically cross-linked cellulose hydrogels gamed as Newton Pendulum (MPG). AUTHOR INFORMATION Corresponding Authors *[email protected] *[email protected] Notes The authors declare no competing financial interest. ACKNOWLEDGMENTS



This work was supported by the Major International (Regional) Joint Research Project of National Natural Science Foundation of China (21620102004) and scientific research startup funds for highlevel talents of Wuyi University (AL2018010). REFERENCES (1) Seliktar, D. Designing cell-compatible hydrogels for biomedical applications. Science 2012, 336(6085), 1124-1128. (2) Li, L.; Wang, Y.; Pan, L.; Shi, Y.; Cheng, W.; Shi, Y.; Yu, G. A nanostructured conductive hydrogels-based biosensor platform for human metabolite detection. Nano letters 2015, 15(2), 1146-1151. (3) Torres ‐ Rendon, J. G.; Femmer, T.; De Laporte, L.; Tigges, T.; Rahimi, K.; Gremse, F.; Zafarnia, S.; Lederle, W.; Ifuku, S.; Wessling, M. Bioactive gyroid scaffolds formed by sacrificial templating of nanocellulose and nanochitin hydrogels as instructive platforms for biomimetic tissue engineering. Adv. Mater. 2015, 27(19), 2989-2995. (4) Butruk-Raszeja, B. A.; Łojszczyk, I.; Ciach, T.; Kościelniak-Ziemniak, M.; Janiczak, K.; Kustosz, R.; Gonsior, M. Athrombogenic hydrogel coatings for medical devices–Examination of biological properties. Colloids Surf. B 2015, 130, 192-198. (5) Ullah, H.; Santos, H. A.; Khan, T. Applications of bacterial cellulose in food, cosmetics and drug delivery. Cellulose 2016, 23(4), 2291-2314. (6) Zhang, W.; Hu, J.; Tang, J.; Wang, Z.; Wang, J.; Lu, T.; Suo, Z. Fracture toughness and fatigue threshold of tough hydrogels. ACS Macro Letters 2019, 8(1), 17-23. (7) Gong, J. P. Materials both tough and soft. Science 2014, 344(6180), 161-162. (8) Sun, J. Y.; Zhao, X.; Illeperuma, W. R.; Chaudhuri, O.; Oh, K. H.; Mooney, D. J.; Vlassak, J. J.; Suo, Z. Highly stretchable and tough hydrogels. Nature 2012, 489(7414), 133-136. 18 ACS Paragon Plus Environment

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High-Strength and Tough Cellulose Hydrogels Dual-Chemically Cross

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