Abstract
Large wounds are characterized by clinical and surgical challenges, requiring numerous searches on demand for inexpensive biocompatible materials that produce the best quality of cutaneous healing. Cellulose is a biopolymer of greatest abundance, good biocompatibility and wide application due to its chemical and physical properties. This study was aimed to develop and characterize low cost membranes of wood cellulose nanofibrils for potential application as a wound dressing in comparison to a commercial porous regenerating membrane. An inexpensive mechanical method was used to defibrillate cellulose, and later the membranes were obtained from the nanofibrils by filtering and drying under mild pressure. The techniques employed for characterization included scanning electron microscopy, physical testing, application in vivo and cost-effectiveness analysis. The membranes presented promising physical properties for application as cutaneous dressing, with characteristic translucency allowing the evaluation of the wound without the need of removal and exchange of the dressing. Wood nanocellulose dressing seems to be promising for wound care since it presented good adhesion to the moist wound surfaces thus promoting the most efficient repitialization in the first 4 days. No allergic reaction or inflammatory response to wood nanocellulose dressings was observed. The wood nanocellulose membranes stand out as a potential wound dressing, as it shows similar efficacy of bacterial cellulose dressing. Besides the efficacy, the membrane developed in this study presents a simpler, faster and cheaper manufacturing process, which may reduce the production cost by 99%.
Graphic abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adam J, Singer MD, Richard AF, Clark MD (1999) Cutaneous wound healing. N Engl J Med 341:738–746
Baez C, Considine J, Rowlands R (2014) Influence of drying restraint on physical and mechanical properties of nanofibrillated cellulose films. Cellulose 21:347–356. https://doi.org/10.1007/s10570-013-0159-1
Basu A, Lindh J, Ålander E et al (2017a) On the use of ion-crosslinked nanocellulose hydrogels for wound healing solutions: physicochemical properties and application-oriented biocompatibility studies. Carbohydr Polym 174:299–308. https://doi.org/10.1016/j.carbpol.2017.06.073
Basu P, Manjubala IN, Kumar U (2017b) Wound healing materials—a perspective for skin tissue engineering. Curr Sci 112:2392–2404. https://doi.org/10.18520/cs/v112/i12/2392-2404
Basu A, Heitz K, Strømme M et al (2018) Ion-crosslinked wood-derived nanocellulose hydrogels with tunable antibacterial properties: candidate materials for advanced wound care applications. Carbohydr Polym 181:345–350. https://doi.org/10.1016/j.carbpol.2017.10.085
Beaumont M, König J, Opietnik M et al (2017) Drying of a cellulose II gel: effect of physical modification and redispersibility in water. Cellulose 24:1199–1209. https://doi.org/10.1007/s10570-016-1166-9
Boateng JS, Matthews KH, Stevens HN, Eccleston GM (2008) Wound healing dressings and drug delivery systems: a review. J Pharm Sci 97:2892–2923
Broughton G II, Janis JE, Attinger CE (2006) Basic science of wound healing. Plast Reconstr Surg 117:12S–34S. https://doi.org/10.1016/j.mpsur.2010.05.007
Cacicedo ML, Castro MC, Servetas I et al (2016) Bioresource technology progress in bacterial cellulose matrices for biotechnological applications. Bioresour Technol 213:172–180. https://doi.org/10.1016/j.biortech.2016.02.071
Çakar F, Katı A, Özer I et al (2014) Newly developed medium and strategy for bacterial cellulose production. Biochem Eng J 92:35–40. https://doi.org/10.1016/j.bej.2014.07.002
Camacho-Alonso F, López-Jornet P (2007) Clinical-pathological study of the healing of wounds provoked on the dorso-lingual mucosa in 186 albino rats. Otolaryngol Head Neck Surg 136:119–124. https://doi.org/10.1016/j.otohns.2006.06.1243
Chinga-Carrasco G, Syverud K (2014) Pretreatment-dependent surface chemistry of wood nanocellulose for pH-sensitive hydrogels. J Biomater Appl 29:423–432. https://doi.org/10.1177/0885328214531511
Cichosz S, Masek A (2019) Cellulose structure and property changes indicated via wetting-drying cycles. Polym Degrad Stab 167:33–43. https://doi.org/10.1016/j.polymdegradstab.2019.05.033
Čolić M, Mihajlović D, Mathew A et al (2015) Cytocompatibility and immunomodulatory properties of wood based nanofibrillated cellulose. Cellulose 22:763–778. https://doi.org/10.1007/s10570-014-0524-8
de Assis CA, Iglesias MC, Bilodeau M et al (2018) Cellulose micro- and nanofibrils (CMNF) manufacturing—financial and risk assessment. Biofuels Bioprod Biorefin 12:251–264. https://doi.org/10.1002/bbb.1835
Desmouliere A, Redard M, Darby I, Baggiani G (1995) Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 146:55–66. https://doi.org/10.1016/S0921-5107(97)00214-6
Dorsett-Martin WA (2004) Rat models of skin wound healing. Wound Repair Regen 12:591–599. https://doi.org/10.1007/978-1-59745-285-4
Dufresne A (2013) Nanocellulose: a new ageless bionanomaterial. Mater Today 16:220–227. https://doi.org/10.1016/j.mattod.2013.06.004
Fu L, Zhang Y, Li C et al (2012) Skin tissue repair materials from bacterial cellulose by a multilayer fermentation method. J Mater Chem 22:12349. https://doi.org/10.1039/c2jm00134a
Fu L-H, Qi C, Ma M-G, Wan P (2018) Multifunctional cellulose-based hydrogels for biomedical applications. J Mater Chem B. https://doi.org/10.1039/C8TB02331J
Garcia VG, De Lima MA, Okamoto T et al (2010) Effect of photodynamic therapy on the healing of cutaneous third-degree-burn: histological study in rats. Lasers Med Sci 25:221–228. https://doi.org/10.1007/s10103-009-0694-z
Gil ES, Panilaitis B, Bellas E, Kaplan DL (2013) Functionalized silk biomaterials for wound healing. Adv Healthc Mater 2:206–217. https://doi.org/10.1002/adhm.201200192
Goldsmith SP (1996) Wound care: combining three classification systems to select dressings. Home Health Care Manag Pract 8:17–27. https://doi.org/10.1177/108482239600800606
Gustaite S, Kazlauske J, Bobokalonov J et al (2015) Characterization of cellulose based sponges for wound dressings. Colloids Surf A Physicochem Eng Asp 480:336–342. https://doi.org/10.1016/j.colsurfa.2014.08.022
Hakkarainen T, Koivuniemi R, Kosonen M et al (2016) Nanofibrillar cellulose wound dressing in skin graft donor site treatment. J Control Release 244:292–301. https://doi.org/10.1016/j.jconrel.2016.07.053
Helenius G, Backdahl H, Bodin A et al (2006) In vivo biocompatibility of bacterial cellulose. J Biomed Mater Res 76:431–438
Hoenich NA (2006) Cellulose for medical applications: past, present, and future. BioResources 1:270–280. https://doi.org/10.15376/biores.1.2.270-280
Isogai A (2013) Wood nanocelluloses: fundamentals and applications as new bio-based nanomaterials. J Wood Sci 59:449–459. https://doi.org/10.1007/s10086-013-1365-z
Iwamoto S, Nakagaito AN, Yano H (2007) Nano-fibrillation of pulp fibers for the processing of transparent nanocomposites. Appl Phys A Mater Sci Process 89:461–466. https://doi.org/10.1007/s00339-007-4175-6
Jack AA, Nordli HR, Powell LC et al (2017) The interaction of wood nanocellulose dressings and the wound pathogen P. aeruginosa. Carbohydr Polym 157:1955–1962. https://doi.org/10.1016/j.carbpol.2016.11.080
João De Masi ECD, Campos ACL, João De Masi FD et al (2016) A influência de fatores de crescimento na cicatrização de feridas cutâneas de ratas. Braz J Otorhinolaryngol 82:512–521. https://doi.org/10.1016/j.bjorl.2015.09.011
Kamel S (2007) Nanotechnology and its applications in lignocellulosic composites: a mini review. Polym Lett 1:546–575
Kucińska-Lipka J, Gubanska I, Janik H (2015) Bacterial cellulose in the field of wound healing and regenerative medicine of skin: recent trends and future prospectives. Polym Bull 72:2399–2419. https://doi.org/10.1007/s00289-015-1407-3
Kummala R, Xu W, Xu C, Toivakka M (2018) Stiffness and swelling characteristics of nanocellulose films in cell culture media. Cellulose 25:4969–4978. https://doi.org/10.1007/s10570-018-1940-y
Kwak MH, Kim JE, Go J et al (2015) Bacterial cellulose membrane produced by Acetobacter sp. A10 for burn wound dressing applications. Carbohydr Polym 122:387–398. https://doi.org/10.1016/j.carbpol.2014.10.049
Lavoine N, Desloges I, Dufresne A, Bras J (2012) Microfibrillated cellulose—its barrier properties and applications in cellulosic materials: a review. Carbohydr Polym 90:735–764. https://doi.org/10.1016/j.carbpol.2012.05.026
Li Y, Jiang H, Zheng W et al (2015) Biomaterials as wound dressings for severe skin. J Mater Chem. https://doi.org/10.1039/c4tb01819b
Lin W, Lien C, Yeh H et al (2013) Bacterial cellulose and bacterial cellulose—chitosan membranes for wound dressing applications. Carbohydr Polym 94:603–611. https://doi.org/10.1016/j.carbpol.2013.01.076
Lin SP, Kung HN, Tsai YS et al (2017) Novel dextran modified bacterial cellulose hydrogel accelerating cutaneous wound healing. Cellulose 24:4927–4937. https://doi.org/10.1007/s10570-017-1448-x
Liu J, Chinga-Carrasco G, Cheng F et al (2016) Hemicellulose-reinforced nanocellulose hydrogels for wound healing application. Cellulose 23:3129–3143. https://doi.org/10.1007/s10570-016-1038-3
Magalhães WLE, Claro FC (2018) Produção de filmes de celulose nanofibrilada. Embrapa Florestas 413:1–8
Magalhães WLE, Claro FC, de Matos M, Lengowski EC (2017) Produção de nanofibrilas de celulose por desfibrilação mecânica em moinho coloidal. Embrapa Florestas 404:1–5
Maneerung T, Tokura S, Rujiravanit R (2008) Impregnation of silver nanoparticles into bacterial cellulose for antimicrobial wound dressing. Carbohydr Polym 72:43–51. https://doi.org/10.1016/j.carbpol.2007.07.025
Martin P (1997) Wound healing–aiming for perfect skin regeneration. Science (80-) 276:75–81. https://doi.org/10.1126/science.276.5309.75
Moreira C, Lima AK, Melo MGD et al (2014) Valores de referência hematológicos e bioquímicos de ratos (Rattus novergicus linhagem Wistar) provenientes do biotério da Universidade Tiradentes. Sci Plena 10:1–9. https://doi.org/10.1158/0008-5472.CAN-05-4569
Moser H, Pereima RR, Pereima MJL (2013) Evolução dos curativos de prata no tratamento de queimaduras de espessura parcial. Rev Bras Queimaduras 12:60–67
Nechyporchuk O, Belgacem MN, Bras J (2016) Production of cellulose nanofibrils: a review of recent advances. Ind Crops Prod 93:2–25. https://doi.org/10.1016/j.indcrop.2016.02.016
Nogi M, Iwamoto S, Nakagaito AN, Yano H (2009) Optically transparent nanofiber paper. Adv Mater 21:1595–1598. https://doi.org/10.1002/adma.200803174
Petersen N, Gatenholm P (2011) Bacterial cellulose-based materials and medical devices: current state and perspectives. Appl Microbiol Biotechnol 91:1277–1286. https://doi.org/10.1007/s00253-011-3432-y
Posnett J, Gottrup F, Lundgren H, Saal G (2009) The resource impact of wounds on health-care providers in Europe. J Wound Care 18:154–154. https://doi.org/10.12968/jowc.2009.18.4.41607
Powell LC, Khan S, Chinga-Carrasco G et al (2016) An investigation of Pseudomonas aeruginosa biofilm growth on novel nanocellulose fibre dressings. Carbohydr Polym 137:191–197. https://doi.org/10.1016/j.carbpol.2015.10.024
Rajwade JM, Paknikar KM, Kumbhar JV (2015) Applications of bacterial cellulose and its composites in biomedicine. Appl Microbiol Biotechnol 99:2491–2511. https://doi.org/10.1007/s00253-015-6426-3
Rees A, Powell LC, Chinga-Carrasco G et al (2015) 3D bioprinting of carboxymethylated-periodate oxidized nanocellulose constructs for wound dressing applications. Biomed Res Int 2015:1–7. https://doi.org/10.1155/2015/925757
Revin V, Liyaskina E, Nazarkina M et al (2018) Biotechnology and industrial microbiology cost-effective production of bacterial cellulose using acidic food industry by-products. Braz J Microbiol 49:151–159. https://doi.org/10.1016/j.bjm.2017.12.012
Sajjad W, Khan T, Ul-islam M et al (2019) Development of modified montmorillonite-bacterial cellulose nanocomposites as a novel substitute for burn skin and tissue regeneration. Carbohydr Polym 206:548–556. https://doi.org/10.1016/j.carbpol.2018.11.023
Schmitz M, Eberlein T, Andriessen A (2014) Wound treatment costs comparing a bio-cellulose dressing with moist wound healing dressings and conventional dressings. Wound Med 6:11–14. https://doi.org/10.1016/j.wndm.2014.07.002
Singla R, Soni S, Kulurkar PM et al (2017) In situ functionalized nanobiocomposites dressings of bamboo cellulose nanocrystals and silver nanoparticles for accelerated wound healing. Carbohydr Polym 155:152–162. https://doi.org/10.1016/j.carbpol.2016.08.065
Sun X, Wu Q, Zhang X et al (2018) Nanocellulose films with combined cellulose nanofibers and nanocrystals: tailored thermal, optical and mechanical properties. Cellulose 25:1103–1115. https://doi.org/10.1007/s10570-017-1627-9
Tang J, Bao L, Li X et al (2015) Potential of PVA-doped bacterial nano-cellulose tubular composites for artificial blood vessels. J Mater Chem B 3:8537–8547. https://doi.org/10.1039/c5tb01144b
Technical Association of the Pulp and Paper Industry (1997) T 411 om-97, thickness (caliper) of paper, paperboard, and combined board
Technical Association of the Pulp and Paper Industry (1998) T 441 om-98 water absorptiveness of sized (non-bibulous) paper, paperboard, and corrugated fiberboard (Cobb test)
Technical Association of the Pulp and Paper Industry (2001) T 220-om01, physical testing of pulp handsheets
Technical Association of the Pulp and Paper Industry (2002a) T410-om02 grammage of paper and paperboard (weight per unit area)
Technical Association of the Pulp and Paper Industry (2002b) T 460 0 m-02,air resistance of paper (Gurley method)
Tehrani Z, Nordli H, Pukstad B et al (2016) Translucent and ductile nanocellulose-PEG bionanocomposites—a novel substrate with potential to be functionalized by printing for wound dressing applications. Ind Crops Prod 93:193–202
Trovatti E, Freire CSR, Pinto PC et al (2012) Bacterial cellulose membranes applied in topical and transdermal delivery of lidocaine hydrochloride and ibuprofen: in vitro diffusion studies. Int J Pharm 435:83–87. https://doi.org/10.1016/j.ijpharm.2012.01.002
Vatankhah E, Prabhakaran MP, Jin G et al (2014) Development of nanofibrous cellulose acetate/gelatin skin substitutes for variety wound treatment applications. J Biomater Appl 28:909–921
Velásquez-Riaño M, Bojaca V (2017) Production of bacterial cellulose from alternative low-cost substrates. Cellulose. https://doi.org/10.1007/s10570-017-1309-7
Viana LC, de Muñiz GIB, Magalhães WLE et al (2019) Nanostructured films produced from the bleached Pinus sp. kraft pulp. Floresta e Ambient. https://doi.org/10.1590/2179-8087.019115
Wang H, Li D, Zhang R (2013) Preparation of ultralong cellulose nanofibers and optically transparent nanopapers derived from waste corrugated paper pulp. BioResources 8:1374–1384. https://doi.org/10.15376/biores.8.1.1374-1384
Wang S, Han Y, Chen D, Li M (2017) bacterial cellulose produced by Komagataeibacter genes in bacterial cellulose production. RCS Adv. https://doi.org/10.1039/c7ra08391b
Weyell P, Beekmann U, Küpper C et al (2019) Tailor-made material characteristics of bacterial cellulose for drug delivery applications in dentistry. Carbohydr Polym 207:1–10. https://doi.org/10.1016/j.carbpol.2018.11.061
Winter GD (2006) Some factors affecting skin and wound healing. J Tissue Viability 16:20–23. https://doi.org/10.18287/1613-0073-2016-1638-493-497
Xie Z, Paras CB, Weng H et al (2013) Dual growth factor releasing multi-functional nanofibers for wound healing. Acta Biomater 9:9351–9359. https://doi.org/10.1016/j.actbio.2013.07.030
Xu C, Zhang Molino B, Wang X et al (2018) 3D printing of nanocellulose hydrogel scaffolds with tunable mechanical strength towards wound healing application. J Mater Chem B 6:7066–7075. https://doi.org/10.1039/c8tb01757c
Yang Q, Fujisawa S, Saito T, Isogai A (2012) Improvement of mechanical and oxygen barrier properties of cellulose films by controlling drying conditions of regenerated cellulose hydrogels. Cellulose 19:695–703. https://doi.org/10.1007/s10570-012-9683-7
Zhu H, Fang Z, Preston C et al (2014) Transparent paper: fabrications, properties, and device applications. Energy Environ Sci 7:269–287. https://doi.org/10.1039/C3EE43024C
Acknowledgments
The authors would like to thank: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Centro de Microscopia Eletrônica (CME/UFPR) and Embrapa Florestas for supporting this work. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Claro, F.C., Jordão, C., de Viveiros, B.M. et al. Low cost membrane of wood nanocellulose obtained by mechanical defibrillation for potential applications as wound dressing. Cellulose 27, 10765–10779 (2020). https://doi.org/10.1007/s10570-020-03129-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10570-020-03129-2