Conducting collagen-polypyrrole hybrid aerogels made from animal skin waste

Abstract

We report the synthesis of conducting collagen-polypyrrole hybrid aerogels through an in situ oxidative polymerization technique coupled with freeze drying. FTIR, XRD and SEM analysis show the complete coating of polypyrrole on the collagen molecules during the polymerization process. These low density aerogels have varying degree of flexibility, brittleness, thermal stability, porosity, biocompatibility and electrical conductivity as a function of the concentration of polypyrrole in the aerogel matrix. The maximum conductivity of the collagen-polypyrrole aerogels is found to be 3.59 × 10⁻⁴ S cm⁻¹ for the 100/100 wt% composition. We also demonstrate the ability of the as-synthesized aerogels to conduct electrons in a light emitting diode lamp and battery setup with varying extents of brightness. The results suggest that the developed collagen-polypyrrole aerogels have potential for biosensor, tissue engineering, electrostatic discharge protection and electromagnetic interference shielding applications.

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1. Introduction

Biocompatible and electrically conductive materials have been highly attractive for biomedical applications such as in biosensors, drug delivery systems, biomedical implants and tissue engineering.^1–5 The electrical stimulation of biocompatible conductive materials in the damaged tissues improves the cellular activities and promotes rapid wound repair and tissue regeneration.^1–4 Polypyrrole (PPy) is one of the highly conductive polymers and it has been widely used in the industry because of its easy synthesis and long-term ambient stability. Several studies have been carried out using polypyrrole for electrostatic discharge protection, electromagnetic interference shielding, biosensor and battery applications.^5–10 The inclusion of polypyrrole in a porous cross-linked polystyrene host polymer composite has shown effective electromagnetic interference shielding up to 26 dB in the frequency range from 1 to 2 GHz.¹¹ The immobilization of glucose oxidase with polypyrrole through electropolymerization has been used to determine the glucose in the biosensor application.^12,13 However, the development of conducting materials based on biocompatible biopolymer and polypyrrole has been the focus of research for biomedical and other sustainable applications.^14,15

Collagen (C) is one of the highly biocompatible biopolymers due to the fact that it is the building block of skin and other tissues. It has been widely used in biomedical applications because of its weak antigenecity, excellent biocompatibility and biodegradability properties.¹⁶ It performs a significant role in cell proliferation, attachment, migration and regeneration of new tissues.¹⁶ On the other hand, huge quantities of collagenous solid wastes are generated from the leather industry.¹⁷ The utilization of collagen from the wastes reduces the environmental impact and also provides economic value.^18–21 Aerogels are porous, extremely light weight, low density and thermally insulating materials.^22,23 Hybrid aerogels possessing properties such as electrical conductivity, porosity, flexibility and biocompatibility are being developed in recent years for several applications.^24,25 Here, we report the synthesis of collagen-polypyrrole (C/PPy) hybrid aerogels through in situ oxidative polymerization technique combined with freeze drying. Collagen was extracted from the leather industry trimming wastes, polymerized with pyrrole and freeze dried to yield C/PPy aerogels. The prepared aerogels were investigated for the structural, thermal, electrical and biological properties.

2. Materials and methods

2.1. Materials

Skin trimming wastes were collected from the tannery, CSIR-Central Leather Research Institute, Chennai. Pyrrole, ferric chloride and copper(II) chloride dihydrate, anthraquinone-2-sulfonic acid sodium salt (AQSA-Na), paratoluene-2-sulfonic acid (pTSA) and dodecyl benzene sulfonic acid (DBSA) were procured from Sigma-Aldrich, India. All other reagents were of analytical grade.

2.2. Synthesis of collagen-polypyrrole aerogels

The schematic of polypyrrole and collagen-polypyrrole aerogel synthesis is shown in Fig. 1. Briefly, the raw hide trimming pieces were collected from local tannery and soaked in 300% (v/w) water for 5 h with three changes. The soaked skin trimming wastes were processed through conventional leather processing such as soaking, liming, unhairing, fleshing and deliming. The delimed hide pieces were soaked in 35 and 70% acetone for 3 h respectively, followed by 100% methanol for five times each 3 h duration to completely remove the moisture. The solvent treated trimming pieces were thoroughly dried in a vacuum drier and ground into powder using a Wiley Mill of 2 mm mesh size.¹⁸ About 10 g hide powder was dissolved in 500 ml of 0.5 M acetic acid. From this solution, 50 ml of collagen was taken in a clean vial and stirred with different concentrations of pyrrole from 0 to 100 wt% for 30 min at 33 ± 2 °C to generate homogenous solution. To arrive at better oxidant and dopant combination, we first synthesized 100/100 wt% C/PPy aerogels using different combination of FeCl₃/CuCl₂ as oxidants and AQSA-Na/PTSA/DBSA as dopants. Based on the results of this preliminary study, a mixture of aqueous solutions of FeCl₃ (oxidant) and AQSA-Na (dopant) was added dropwise into the collagen-pyrrole mixtures. The molar ratio of FeCl₃ and AQSA-Na to the pyrrole was 2.3 and 0.3, respectively. The reaction solution was kept under continuous stirring for 6 h at 6 ± 2 °C. After the completion of the polymerization, the black colored C/PPy precipitates were thoroughly washed with deionized water and freeze dried to obtain aerogels. For measuring the apparent density of the aerogels, a piece of circular specimen was weighted. The apparent density was calculated by dividing the mass by the volume.

Fig. 1 Schematic showing the synthesis of (a) electrically conductive polypyrrole and (b) electrically conductive C/PPy aerogels; a photograph of a circular piece of C/PPy aerogel standing on a chicken feather is also shown.

2.3. Characterization of C/PPy aerogels

To determine the collagen and polypyrrole content in the final compositions of C/PPy aerogels, hydroxyproline estimation was carried out. Briefly, 100 mg of sample was hydrolyzed in 6 N HCl for 18 h at 110 °C. In this treatment, the collagen content present in the samples hydrolyzed completely, whereas the polypyrrole remains undissolved in the solution. The hydrolyzed sample was separated from the residue and evaporated to dryness. After the complete evaporation of HCl, the dried sample was made up with a known volume of water. From this solution, collagen was estimated using the hydroxyproline analysis reported by Woessner.²⁶ The collected residue was separately evaporated to dryness and weighed to calculate the quantity of polypyrrole content. The elemental composition of the samples was also analyzed using the EURO EA elemental analyzer to obtain the percentages of carbon, hydrogen, nitrogen and sulphur. The Fourier transform infrared spectroscopic (FTIR) analysis of the as prepared 100/0, 100/25, 100/50, 100/75, 100/100 and 0/100 wt% C/PPy aerogels were carried out using JASCO FTIR-4200 spectrometer. The samples were ground into powder and mixed with KBr and pressed to form pellets. The pellets were analyzed in a single beam mode with an average of 4 scans and 2 cm⁻¹ resolution. The X-ray diffraction (XRD) of select 100/0, 100/100 and 0/100 wt% C/PPy aerogels were analyzed using Rigaku Miniflex (II) desktop diffractometer (Ni filtered with CuKα radiation with λ = 0.15418 nm) at the 2θ range of 10 to 80° with a scan speed of 4° min⁻¹ and sampling step of 0.02°. The thermogravimetric analysis (TGA) of select 100/0, 100/100 and 0/100 wt% C/PPy aerogels were carried out using a Perkin-Elmer (TGA Q50, V20.6 Build 31) analyzer in the temperature range of 25 to 800 °C. The heating rate was maintained at 10 °C min⁻¹ under the nitrogen flow of 40 ml min⁻¹. The structural morphology of select 100/0, 100/25, 100/50 and 100/75 wt% C/PPy aerogels were analyzed using Phenom Pro scanning electron microscope (SEM) at an accelerating voltage of 5 kV.

2.4. Electrical conductivity and in vitro biodegradation studies

Electrical conductivity measurements were performed by two-probe method using a Prestige 4.5 Digit Micro-Ohm Meter (Prestige Electronics, Mumbai, India) at room temperature. The prepared C/PPy aerogels were compressed at 3 MPa for 1 min to obtain a thickness of 3.0 ± 0.2 mm and a diameter of 2.5 cm before the analysis. The conductivity (σ) of C/PPy aerogels was calculated using the eqn (1) given below.where σ is conductivity of the sample in S cm⁻¹, R is resistance of the sample in Ω, t is thickness of the sample in cm and A is area of the sample in cm².

The in vitro biodegradation of C/PPy aerogels was carried out by incubating 50 mg of the aerogels in a mixture of 10 ml PBS (pH 7.4) and 10 mg alkaline protease at 37 °C for 24 h. After incubation, the samples were centrifuged at 10 000 rpm for 25 min followed by complete drying at 60 °C in a water bath and weighed. This process was repeated for 5 times and the percentage of degradation was calculated using the eqn (2) below.

3. Results and discussion

3.1. Synthesis of C/PPy aerogels

Synthesis of C/PPy aerogels was carried out using in situ oxidative polymerization technique. To choose better oxidant and dopant combination for the electrically conductive C/PPy aerogels, we first synthesized 100/100 wt% C/PPy aerogels using different combination of FeCl₃/CuCl₂ as oxidants and AQSA-Na/PTSA/DBSA as dopants. As shown in Table S1,† the combination of FeCl₃ and AQSA-Na in the C/PPy aerogels showed the maximum conductivity up to 3.59 × 10⁻⁴ S cm⁻¹. While other oxidants and the dopants combination exhibited low conductivity in the C/PPy aerogels. This may be due to the well-packed structure of AQSA-Na that induces strong inter-chain packing in PPy structure.²⁷ Also, the FeCl₃ in the polymerization reaction acts as a strong Lewis acid which generates more H⁺ ions changing the reaction mixture into sufficiently acidic medium, that stabilizes the Fe³⁺ and prevents the nucleophilic attack in the polymer backbone thereby it generates a quality polypyrrole in the aerogel matrix.²⁸ Hence, the results show that the FeCl₃ and AQSA-Na has performed as best oxidant and dopant, respectively in the synthesis of electrically conductive C/PPy aerogels.

Collagen and polypyrrole contents in the final compositions of C/PPy aerogels are given in Table 1 based on hydroxyproline estimation. It is seen that the actual amount of collagen and polypyrrole in a particular final composition does not follow the feed ratio. As can be observed, the collagen content in the C/PPy aerogels decreases whereas the polypyrrole content increases (Table 1). This is because the feed ratio was based on the collagen and pyrrole monomer. The intense polymerization and deposition of polypyrrole on the collagen molecules changed the actual content of collagen and polypyrrole in the final C/PPy aerogel products. Further, there could be a possible interaction between the collagen and polypyrrole leading to reduction in native collagen content and increase in PPy content in the final composition. Elemental composition of the as-synthesized C/PPy aerogels is given in Table S2† based on CHNS analysis. It is seen that the C and S contents in the C/PPy aerogels gradually increases while the N content decreases marginally as the PPy composition increases. This could be due to the high C and low N in the PPy compared to pure collagen, as evident from 0/100 wt% C/PPy. Higher level of S in the C/PPy aerogels as a function of concentration of PPy could be attributed to the increasing doping level (AQSA-Na).

Table 1 Final compositions of collagen and polypyrrole content in the as-synthesized C/PPy aerogels

Sample	Feed ratio (feed composition in mg)		Final composition^a (mg per 100 mg product)
	Collagen	Pyrrole	Collagen	Polypyrrole
a Moisture-free basis.
100/0 wt% C/PPy	100	0	81.5 ± 2.1	0
100/25 wt% C/PPy	80	20	54.2 ± 1.2	43.8 ± 0.4
100/50 wt% C/PPy	67	33	47.9 ± 1.7	49.0 ± 1.5
100/75 wt% C/PPy	57	43	39.7 ± 0.4	57.5 ± 0.7
100/100 wt% C/PPy	50	50	34.8 ± 1.8	64.3 ± 0.4
0/100 wt% C/PPy	0	100	0	97.6 ± 2.3

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The synthesized C/PPy aerogels are fairly light. The calculated apparent density of C/PPy aerogels range between 25 and 135 mg cm⁻³ depending on the increasing PPy content. The density is comparable to those of biopolymer based aerogels (20–40 mg cm⁻³) and is considerably lower than conventional carbon (100–800 mg cm⁻³) or graphene (60–150 mg cm⁻³) based aerogels.^24,29,30 Due to its low density, a circular piece of C/PPy aerogel easily stands on a chicken feather (Fig. 1b). The digital images of as-synthesized freeze dried 100/0, 100/25, 100/50, 100/75, 100/100 and 0/100 wt% C/PPy aerogels are shown in Fig. 2. It is seen that the C/PPy aerogels have changed from white to black color due to the polymerization of polypyrrole in the aerogels. The 100/0 wt% C/PPy aerogel shows white color because of the absence of pyrrole composition. Fig. 2 also shows that the C/PPy aerogels have increased brittleness and reduced flexibility upon increasing concentration of pyrrole. When we tried to manually grind the aerogels using a mortar and pestle, the 100/25 and 100/50 wt% C/PPy aerogels have not ground completely and appear in large pieces (shown as an inset in Fig. 2b and c) indicating the cohesiveness of aerogels at low PPy concentration. Whereas the 100/75, 100/100 and 0/100 wt% C/PPy aerogels ground into fine particles due to the high brittleness associated with high polypyrrole concentration (shown as an inset in Fig. 2d–f).

Fig. 2 Digital images of as-synthesized C/PPy aerogels; (a) 100/0, (b) 100/25, (c) 100/50, (d) 100/75, (e) 100/100 and (f) 0/100 wt% C/PPy aerogels. Insets show the status of aerogels after physical grinding in a mortar and pestle.

3.2. Structural, thermal and morphological properties of C/PPy aerogels

FTIR spectra of pure collagen, polypyrrole and C/PPy aerogels are shown in Fig. 3. The FTIR spectra of 100/0 wt% C/PPy (pure collagen) aerogel depicts the characteristic peaks at 3318, 1653, 1545 and 1240 cm⁻¹ corresponding to hydroxyl, amide I, amide II and amide III groups, respectively (Fig. 3a).¹⁸ The 0/100 wt% C/PPy (pure polypyrrole) spectrum shows the presence of characteristic absorption bands at 3455, 1536 and 1441 cm⁻¹, which represents N–H, C–C and C–N stretching vibration in the polypyrrole ring (Fig. 3f). The peaks at 1294, 1159, 1032 and 781 cm⁻¹ are associated with the C–N stretching vibration in the ring, C–H inplane deformation, N–H in-plane deformation and C–H out-of-plane ring deformation, respectively (Fig. 3f).³¹ FTIR spectra of C/PPy aerogels show the gradual decrease of characteristic bands of collagen such as hydroxyl and amide groups and steady increase of signature peaks of polypyrrole around 1536, 1294, 1159, 1032 and 781 cm⁻¹ upon increasing polypyrrole concentration in the C/PPy aerogels as shown by the arrows in Fig. 3b–e. These results provide convincing evidence for the polymerization of polypyrrole with the collagen molecules resulting in homogenous aerogels.

Fig. 3 FTIR spectra of (a) 100/0 (pure collagen), (b) 100/25, (c) 100/50, (d) 100/75, (e) 100/100 and (f) 0/100 (pure polypyrrole) wt% C/PPy aerogels.

The XRD patterns of the select 100/0, 100/100 and 0/100 wt% C/PPy aerogels are shown in Fig. S1.† As can be seen, the 100/0 wt% C/PPy aerogels (pure collagen) exhibit a broad band at 2θ = 24.6° (Fig. S1a†), which may be due to the amorphous nature of collagen molecules.³² Similarly, the 0/100 wt% C/PPy (pure polypyrrole) shows a broad peak at 2θ = 26.04° (Fig. S1c†).³¹ It may be due to the amorphous nature of PPy and the scattering from PPy chains at the interplanar spacing.³¹ As a result, the 100/100 wt% C/PPy aerogels have been found to be completely amorphous as seen with a broad diffraction peak around 2θ = 26° (Fig. S1b†).

Thermogravimetric analysis patterns of the select 100/0, 100/100 and 0/100 wt% C/PPy aerogels are shown in Fig. 4. As can be seen, the TGA curves of 100/0, 100/100 and 0/100 wt% C/PPy aerogels show multi-stage decomposition. The first stage is due to the evaporation of water molecules in the samples. The 100/0 and 0/100 wt% C/PPy aerogels exhibit only second stage of decomposition with the inflection point at 328 and 470 °C, respectively (Fig. 4a and c) primarily due to the destruction of macromolecular structure of collagen or PPy. Interestingly, the 100/100 wt% C/PPy aerogels show second and third stage of decomposition with the inflection points at 325 and 423 °C (Fig. 4b) due to the presence of both collagen and PPy in the hybrid aerogels. Hence, the results demonstrate that the incorporation of polypyrrole with collagen leads to improved thermal stability in the prepared 100/100 wt% C/PPy aerogels.

Fig. 4 TGA curves of (a) 100/0, (b) 100/100 and (c) 0/100 wt% C/PPy aerogels.

Surface morphology of select aerogels (100/0, 100/25, 100/50 and 100/75 wt% C/PPy) were analyzed using SEM as shown in Fig. 5. It is seen that the 100/0 wt% C/PPy aerogel (pure collagen) exhibits sheath like three-dimensional macroporous surface with pore diameter of 400 ± 150 μm (Fig. 5a).^18,19 Whereas the hybrid C/PPy aerogels show more microporous surface with fairly similar morphology and reduced pore diameter ranging from 150 to 10 μm (Fig. 5b–d).³¹ It is seen that the reduction in pore diameter is dependent on the concentration of PPy in the aerogel matrix.

Fig. 5 Scanning electron microscopic images showing the morphology of (a) 100/0, (b) 100/25, (c) 100/50 and (d) 100/75 wt% C/PPy aerogels (false colored images).

3.3. Electrical conductivity and biodegradability of C/PPy aerogels

The electrical conductivity of 100/0 (pure collagen), 100/25, 100/50, 100/75, 100/100 and 0/100 (pure polypyrrole) wt% C/PPy aerogels is shown in Fig. 6. As can be seen, the conductivity of the 100/0 (pure collagen) and 0/100 (pure polypyrrole) wt% C/PPy aerogels is 5.34 × 10⁻¹² and 5.09 × 10⁻⁴ S cm⁻¹, respectively. On the other hand, the conductivity of the prepared 100/25, 100/50, 100/75, 100/100 wt% C/PPy aerogels gradually increase and reaches the maximum conductivity of 3.59 × 10⁻⁴ S cm⁻¹.

Fig. 6 Electrical conductivity of 100/0, 100/25, 100/50, 100/75, 100/100 and 0/100 wt% C/PPy aerogels.

The electrical conductivity of as-prepared 100/0, 100/25, 100/50, 100/75 and 100/100 wt% C/PPy aerogels is also demonstrated by a simple light emitting diode (LED) lamp and battery setup as shown in Fig. 7. The two terminals were placed on the sample with sufficient distance (∼1 cm) to assess the ability of the sample to conduct electricity and illuminate the LED lamp as shown in the circuit diagram (Fig. 7f). It is seen that 100/25 wt% C/PPy aerogel could not light up the lamp completely with negligible brightness akin to 100/0 wt% C/PPy aerogel. On the other hand, other C/PPy aerogels with ≥50 wt% polypyrrole concentration were able to illuminate the LED lamp with varying degree of brightness. The extent of brightness is mainly dependent on the concentration of polypyrrole in the aerogel matrix. The enhancement of electrical conductivity in the biocompatible collagen-polypyrrole aerogel is expected to have potential applications in tissue engineering, sensors and bioelectronics.^1–4

Fig. 7 Demonstration of C/PPy aerogels in the light emitting diode lamp and battery setup. (a) 100/0, (b) 100/25, (c) 100/50, (d) 100/75, (e) 100/100 wt% C/PPy aerogels and (f) circuit diagram of sample, light emitting diode lamp and battery setup.

The in vitro biodegradation rate directly demonstrates the biostability of C/PPy aerogels in biological fluids during tissue engineering application or ability to degrade in ambient environment during the post-usage disposal. The in vitro biodegradation of 100/0, 100/25, 100/50, 100/75 and 100/100 wt% C/PPy aerogels is shown in Fig. S2.† As can be seen, the 100/0 (pure collagen) wt% C/PPy aerogel biodegraded completely within the 1^st day of incubation. Whereas the 100/25, 100/50, 100/75 and 100/100 wt% C/PPy aerogels show reduced biodegradation as a function of concentration of PPy in collagen. The 100/100 wt% C/PPy aerogels show the lowest biodegradation (20%) after 5^th day of incubation. These results reveal that the prepared C/PPy aerogels possess improved biostability for tissue engineering application and moderate biodegradation for sustainable environment for other applications.

4. Conclusions

Biocompatible and electrically conductive C/PPy aerogels were synthesized using in situ oxidative polymerization technique employing collagen extracted from the skin trimming wastes generated from leather industries. Various analysis show the polymerization of polypyrrole with collagen fibers and improved thermal and biocompatibility properties. The prepared C/PPy aerogels show excellent electrical conductivity up to a maximum level of 3.59 × 10⁻⁴ S cm⁻¹, which was further demonstrated through a simple light emitting diode lamp and battery setup. Brightness of the LED lamp increases as a function of polypyrrole concentration. Hence, the prepared C/PPy aerogels are promising as an effective material for a wide range of applications such as biosensor, tissue engineering, electrostatic discharge protection and electromagnetic interference shielding.

Conflict of interest

The authors declare no conflict of interest.

Acknowledgements

Berhanu Telay Mekonnen thanks the Leather Industry Development Institute (LIDI), Ethiopia for the financial support under Twinning project that enabled his stay at Central Leather Research Institute, Chennai. Financial support from CSIR under ZERIS Project (CSC0103) is greatly appreciated. CSIR-CLRI Communication No. 1207.

Notes and references

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Footnote

† Electronic supplementary information (ESI) available: Conductivity of aerogels with different oxidants and dopants, CHNS elemental analysis, XRD and in vitro biodegradation of the C/PPy hybrid aerogels. See DOI: 10.1039/c6ra08876g

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