Environmental Science and Pollution Research

, Volume 26, Issue 26, pp 26529–26541 | Cite as

Bacterial cellulose/phytochemical’s extracts biocomposites for potential active wound dressings

  • Nahla A. El-Wakil
  • Enas A. HassanEmail author
  • Mohammad L. Hassan
  • Soheir S. Abd El-Salam
Research Article


The present study describes the impregnation of coffee extract (CE) into bacterial cellulose synthesized from kombucha tea fungus (KBC) of different cellulose content, incubated for different incubation periods (2, 4, and 10 days), to prepare biocomposites having the potential for wound healing applications. Total polyphenols in hydroalcoholic extracts from ground roasted coffee and its release from the prepared biocomposites were determined as gallic acid equivalent. The polyphenols content was found to be 13.66 mg/g and the minimum inhibitory concentration (MIC) of the CE was determined using colony-forming unit (CFU) method against Gram-negative bacteria Escherichia coli and Gram-positive bacteria Staphylococcus aureus where the growth inhibition was 86 and 97% respectively. Biocomposites (KBC/CE) with the lowest cellulose and CE content showed the highest wet tensile stress (3.35 MPa), absorption of pseudo extracellular fluid (154.32% ± 4.84), and water vapor transmission rate (3184.94 ± 198.07 g/m2/day), whereas it showed the lowest polyphenols’ release (51.85% ± 2.94)when immersed in PBS buffer of pH 7.4. The impregnation of CE into KBC provided biocomposites that can enlarge the range of BC in the biomedical application.


Wound dressings Kombucha tea Bacterial cellulose Coffee extracts Phenolic compounds 



The authors would like to thank National Research Center for its support.


  1. Affonso RC, Voytena AP, Fanan S, Pitz H, Coelho DS, Horstmann AL, Maraschin M (2016) Phytochemical composition, antioxidant activity, and the effect of the aqueous extract of coffee (Coffea arabica L.) bean residual press cake on the skin wound healing. Oxidative Med Cell Longev 2016:1–10. CrossRefGoogle Scholar
  2. Almeida AP, Farah A, Silva DA, Nunan EA, M. Gloäria BA, (2006) Antibacterial Activity of Coffee Extracts and Selected Coffee Chemical Compounds against Enterobacteria. J. Agric. Food Chem. 2006, 54, 8738–8743.
  3. Andrade FK, Alexandre N, Amorim I, Gartner F, Mauricio AC, Luis AL, Gama M (2013) Studies on the biocompatibility of bacterial cellulose. J Bioact Compat Polym 28:97–112. CrossRefGoogle Scholar
  4. Avila MH, Schwarz S, Feldmann EM, Mantas A, Von Bomhard A, Gatenholm P, Rotter N (2014) Biocompatibility evaluation of densified bacterial nanocellulose hydrogel as an implant material for auricular cartilage regeneration. Appl Microbio Biotechnol 98:7423–7435. CrossRefGoogle Scholar
  5. Barati F, Javanbakht J, Adib-Hashemi F, Hosseini E, Safaeie R, Rajabian M, Razmjoo M, Sedaghat R, Hassan M (2013) Histopathological and clinical evaluation of Kombucha tea and Nitrofurazone on cutaneous full-thickness wounds healing in rats: an experimental study. Diagn Pathol 8:120–127. CrossRefGoogle Scholar
  6. Cavalcanti M, Pinto FM, de Oliveira GM, Lima SC, Aguiar JL, Lins EM (2017) Efficacy of bacterial cellulose membrane for the treatment of lower limbs chronic varicose ulcers: a randomized and controlled. Rev Col Bras Cir 44:72–80. CrossRefGoogle Scholar
  7. Chauhan PS, Puri N, Sharma P, Gupta N, (2012) Mannanases: microbial sources, production, properties and potential biotechnological applications. Appl Microbiol Biotechnol 93:1817–1830.
  8. Chun-Nan W, Shih-Chang F, Shin-Ping L, Yen-Yi L, Hung-Yueh C, Jui-Ming L, Kuan-Chen C (2018) TEMPO-oxidized bacterial cellulose pellicle with silver nanoparticles for wound dressing. Biomacromol 19:544–554. CrossRefGoogle Scholar
  9. Czaja W, Romanovicz D, Brown RM Jr (2004) Structural investigations of microbial cellulose produced in stationary and agitated culture. Cellulose 11:403–411. CrossRefGoogle Scholar
  10. Czaja WK, Young DJ, Kawecki M, Brown RM (2007) The future prospects of microbial cellulose in biomedical applications. Biomacromol 8:1–12. CrossRefGoogle Scholar
  11. De Luca S, Ciotoli E, Biancolillo A, Bucci R, Magrì AD, Marini F, (2018) Simultaneous quantification of caffeine and chlorogenic acid in coffee green beans and varietal classification of the samples by HPLC-DAD coupled with chemometrics. Environ Sci Pollut Res 25:28748–28759.
  12. Di Z, Shi Z, Ullah MW, Li S, Yang G (2017) A transparent wound dressing based on bacterial cellulose whisker and poly(2-hydroxyethyl methacrylate). Int J Biol Macromol 105:638–644. CrossRefGoogle Scholar
  13. Dima SO, Panaitescu DM, Orban C (2017) Bacterial nanocellulose from side-streams of kombucha beverages production: preparation and physical-chemical properties. Polym 9:373–397. CrossRefGoogle Scholar
  14. Fajardo AR, Lopes LC, Caleare AO, Britta EA, Nakamura CV, bira AF et al (2013) Silver sulfadiazine loaded chitosan/chondroitin sulfate films for a potential wound dressing application. Mat Sci Eng 33:588–595. CrossRefGoogle Scholar
  15. Fereshteh SJ, Hadi A (2016) Morphological, physical, antimicrobial and release properties of ZnO nanoparticles-loaded bacterial cellulose films. Carbohydr Polym 149:8–19. CrossRefGoogle Scholar
  16. Fontana JD, de Souza AM, Fontana CK, Torriani IL, Moreschi JC, Gallotti BJ, de Souza SJ, Narcisco GP, Bichara JA, Farah LFX (1990) Acetobacter cellulose pellicle as a temporary skin substitute. Appl Biochem Biotechnol 25:253–264. CrossRefGoogle Scholar
  17. Fürsatz M, Skog M, Sivlér P, Palm E, Aronsson C, Skallberg A, Greczynski G, Khalaf H, Bengtsson T, Aili D (2018) Functionalization of bacterial cellulose wound dressings with the antimicrobial peptide ε-poly-L-lysine. Biomed Mate 13:025014. CrossRefGoogle Scholar
  18. Gantwerker EA, Hom DB (2011) Skin: histology and physiology of wound healing. Facial Plast Surg Clin North Am 19:441–453. CrossRefGoogle Scholar
  19. Getachew AT, Chun BS (2016) Influence of hydrothermal process on bioactive compounds extraction from green coffee bean. Innov Food Sci Emerg Technol 38:24–31. CrossRefGoogle Scholar
  20. Gustaite S, Kazlauske J, Bobokalonov J, Perni S, Dutschk V, Liesiene J, Prokopovich P (2015) Characterization of cellulose based sponges for wound dressings. Colloids Surf A: Physicochem Eng Aspects 480:336–342. CrossRefGoogle Scholar
  21. Hassan E, Hassan H, Abou-zeid R, Berglund L, Oksman K (2017) Use of bacterial cellulose and crosslinked cellulose nanofibers membranes for removal of oil from oil-in-water emulsions. Polym 9:388–402. CrossRefGoogle Scholar
  22. Hesseltine CW (1965) A millenium of fungi food and fermentation. Mycologia. 57:148–167 CrossRefGoogle Scholar
  23. Hestrin S, Schramm M (1954) Synthesis of cellulose by Acetobacter xylinum. 2. Preparation of freeze-dried cells capable of polymerizing glucose to cellulose. Biochem J 58:345–352CrossRefGoogle Scholar
  24. Hobzova R, Hrib J, Sirc J, Karpushkin E, Michalek J, Janouskova O, Gatenholm P (2018) Embedding of bacterial cellulose nanofibers within PHEMA hydrogel matrices: tunable stiffness composites with potential for biomedical applications. J Nanomat 2018:1–11. CrossRefGoogle Scholar
  25. Hou Y, Wang X, Yang J, Zhu R, Zhang Z, Li Y (2018) Development and biocompatibility evaluation of biodegradable bacterial cellulose as a novel peripheral nerve scaffold. J Biomed Mater Res - Part A 106:1288–1298. CrossRefGoogle Scholar
  26. Jayabalan R, Malbaša RV, Lončar ES, Vitas JS, Sathishkumar M (2014) A review on kombucha tea—microbiology, composition, fermentation, beneficial effects, toxicity, and tea fungus. Food Sci Food Saf 13:538–550. CrossRefGoogle Scholar
  27. Jiang L, Ye S, Wu J, Su C, Huang C, Liu X, Shao W (2018) Flexible amoxicillin-grafted bacterial cellulose sponges for wound dressing: in vitro and in vivo evaluation. ACS Appl Mater Interfaces 10:5862–5870. CrossRefGoogle Scholar
  28. Kenawy ER, Bowlin GL, Mansfield K, Layman J, Simpson DG, Sanders EH, Wnek GE (2002) Release of tetracycline hydrochloride from electrospun poly (ethylene-co-vinylacetate), poly (lactic acid), and a blend. J Control Release 81:57–64. CrossRefGoogle Scholar
  29. Kenisa YP, Istiati I, Wisnu SJ (2012) Effect of Robusta coffee beans ointment on full thickness wound healing. Dent J 45:52–57. Google Scholar
  30. Kim Y, Ullah MW, Ul-Islam M, Khan S, Jang JH, Park JK (2019) Self-assembly of bio-cellulose nanofibrils through intermediate phase in a cell-free enzyme system. Biochem Eng J 142:135–144. CrossRefGoogle Scholar
  31. Kongruang S, (2008) Bacterial cellulose production by Acetobacter xylinum strains from agricultural waste products. Appl Biochem Biotechnol 148: 245–256.
  32. Lee KY, Buldum G, Mantalaris A, Bismarck A (2014) More than meets the eye in bacterial cellulose: biosynthesis, bioprocessing, and applications in advanced fiber composites. Macromol Biosci 14:10–32. CrossRefGoogle Scholar
  33. Lin WC, Lien CC, Yeh HJ, Yu CM, Hsu SH (2013) Bacterial cellulose and bacterial cellulose–chitosan membranes for wound dressing applications. Carbohyd Polym 94:603–611. CrossRefGoogle Scholar
  34. Liyaskina E, Revin V, Paramonova E, Nazarkina M, Pestov N, Revina N, Kolesnikova S (2017) Nanomaterials from bacterial cellulose for antimicrobial wound dressing. J Physics: Conference Series 784:012034. Google Scholar
  35. Malgorzata K, Anna B, Anna M (2017) Analysis of phenolic acids and antibacterial activity of extracts obtained from the flowering herbs of Carduus acanthoides L. Acta Pol Pharm Drug Res 74:161–172. Google Scholar
  36. Marlon O, Jorge VC, Luz MR, Robín Z, Piedad G, Orlando JR, Isabel OT, Cristina C (2017) Bioactive 3D-shaped wound dressings synthesized from bacterial cellulose: effect on cell adhesion of polyvinyl alcohol integrated in situ. Int J Polym Sci 2017:1–10. Google Scholar
  37. Marsh AJ, Sullivan OO’, Hill C, Ross RP, Cotter PD, (2014) Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiol 38: 171–178. CrossRefGoogle Scholar
  38. McKenna AB, Mikkelsen D, Wehr JB, Gidley MJ, Menzies NW (2009) Mechanical and structural properties of native and alkali treated bacterial cellulose produced by Gluconacetobacter xylinus strain ATCC 53524. Cellulose 16:1047–1055. CrossRefGoogle Scholar
  39. Meneses NGT, Martins S, Teixeira JA, Mussatto SI (2013) Influence of extraction solvents on the recovery of antioxidant phenolic compounds from brewer’s spent grains. Sep Purif Technol 108:152–158. CrossRefGoogle Scholar
  40. Mohite BV, Patil SV (2014) A novel biomaterial: bacterial cellulose and its new era applications. Biotechnol Appl Biochem 61:101–110. CrossRefGoogle Scholar
  41. Moustafa H, Guizani C, Dupont C, Martin V, Jeguirim M, Dufresne A (2017) Utilization of torrefied coffee grounds as reinforcing agent to produce high-quality biodegradable PBAT composites for food packaging applications. ACS Sustain Chem Eng 5:1906–1916. CrossRefGoogle Scholar
  42. Mussatto SI, Ballesteros LF, José SM, Teixeira A (2011) Extraction of antioxidant phenolic compounds from spent coffee grounds. Sep Purif Technol 83:173–179. CrossRefGoogle Scholar
  43. Nagaraj B, Nagur KS, Dhoom SM (2015) Determination of antibacterial activity of green coffee bean extract on periodontogenic bacteria like Porphyromonas gingivalis, Prevotella intermedia, Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans: an in vitro study. Contemp Clin Dent 6:166–169. CrossRefGoogle Scholar
  44. Nkemcho O, Olivera S, Irena P, Andrew S, Natalie Y, Marjana TC (2016) The effects of caffeine on wound healing. Int Wound J 13:605–613. CrossRefGoogle Scholar
  45. Numata Y, Sakata T, Furukawa H, Tajima K (2015) Bacterial cellulose gels with high mechanical strength. Mater Sci Eng C Mater Biol Appl 147:57–62. CrossRefGoogle Scholar
  46. Nunes FM, Coimbra MA (2002) Chemical characterization of galactomannans and arabinogalactans from two Arabica coffee inclusions as affected by the degree of roast. J Agric Food Chem 50:1429–1434. CrossRefGoogle Scholar
  47. Ostadhossein F, Mahmoudi N, Gabriel MC, Elnaz T, Francisco JN, Belén S, José ML, Abdolreza S (2015) Development of chitosan/bacterial cellulose composite films containing nanodiamonds as a potential flexible platform for wound dressing. Materials 8:6401–6418. CrossRefGoogle Scholar
  48. Paini M, Aliakbarian B, Casazza A, Perego P, Ruggiero C, Pastorino L (2015) Chitosan/dextran multilayer microcapsules for polyphenol co-delivery. Mat Sci Eng 46:374–380. CrossRefGoogle Scholar
  49. Pal S, Nisi R, Stoppa M, Licciulli A (2017) Silver-functionalized bacterial cellulose as antibacterial membrane for wound-healing applications. ACS Omega 2:3632–3639. CrossRefGoogle Scholar
  50. Park SU, Lee BK, Kim MS, Park KK, Sung WJ, Kim HY, Han DG, Shim JS, Lee YJ, Kim SH, Kim IH, Park DH (2014) The possibility of microbialcellulose for dressing and scaffold materials. Int Wound J 11:35–43. CrossRefGoogle Scholar
  51. Phan AD, D’Arcy BR, Gidley MJ (2016) Polyphenol–cellulose interactions: effects of pH, temperature and salt. Int J Food Sci Tech 51:203–211. CrossRefGoogle Scholar
  52. Pinto RJ, Daina S, Sadocco P, Neto CP, Trindade T (2013) Antibacterial activity of nanocomposites of copper and cellulose. Biomed Res Int 2013:280512. CrossRefGoogle Scholar
  53. Pourali P, Razavianzadeh N, Khojasteh L, Yahyaei B (2018) Assessment of the cutaneous wound healing efficiency of acidic, neutral and alkaline bacterial cellulose membrane in rat. J Mater Sci Mater Med 29:90–99. CrossRefGoogle Scholar
  54. Queen D, Gaylor JD, Evans J, Courtney J, Reid W (1987) The preclinical evaluation of the water vapour transmission rate through burn wound dressings. Biomater 8:367–371. CrossRefGoogle Scholar
  55. Ragab IM, Shalaby AG, El Awdan SA, Refaat A, Helmy WA (2018) New applied pharmacological approach/trend on utilization of agro-industrial wastes. Environ Sci Pollut Res 25:26446–26460. CrossRefGoogle Scholar
  56. Rufian- Henares JA, Morales FJ (2007) Functional properties of melanoidins: in vitro antioxidant, antimicrobial and antihyper- tensive activities. Food Res Int 40:995–1002. CrossRefGoogle Scholar
  57. Rufian-Henares JA, de la Cueva SP (2009) Antimicrobial activity of coffee melanoidins. A study of their metal-chelating properties. J Agric Food Chem 57:432–438. CrossRefGoogle Scholar
  58. Shailendra S, Alistair Y, Mc C-E (2017) The physiology of wound healing. SURGERY 35:473–477Google Scholar
  59. Shoukat A, Wahid F, Khan T, Siddique M, Nasreen S, Yang G, Ullah MW, Khan R (2019) Titanium oxide-bacterial cellulose bioadsorbent for the removal of lead ions from aqueous solution. Int J Biol Macromol 129:965–971. CrossRefGoogle Scholar
  60. Sidiras DK, Koullas DP, Vgenopoulos AG, Koukios EG (1990) Cellulose crystallinity as affected by various technical processes. Cellu Chem Technol 24:309–317Google Scholar
  61. Singh B, Pal L (2008) Development of sterculia gum based wound dressings for use in drug delivery. Eur Polym J 44:3222–3230. CrossRefGoogle Scholar
  62. Singleton VL, Orthofer R, Lamuela- Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol 299:152–178. CrossRefGoogle Scholar
  63. Stanislaw B, Halina K, Alina K, Katarzyna K, Ko M, de Manu G (2012) Wound dressings and cosmetic materials from bacterial nanocellulose. In: Bacterial nanocellulose. Perspectives in nanotechnology. CRC Press, New York, pp 157–174. Google Scholar
  64. Stylianou M, Agapios A, Michalis O, Ioannis V, Ioannis MI, Grivas M, Dionysia F (2018) Converting environmental risks to benefits by using spent coffee grounds (SCG) as a valuable resource. Environ Sci Pollut Res 25:35776–35790. CrossRefGoogle Scholar
  65. Sudipto P, Rossella N, Mariangela S, Antonio L (2017) Silver-functionalized bacterial cellulose as antibacterial membrane for wound-healing applications. ACS Omega 2:3632–3639. CrossRefGoogle Scholar
  66. Tabaii J, Emtiazi G (2018) Transparent nontoxic antibacterial wound dressing based on silver nano particle/bacterial cellulose nano composite synthesized in the presence of tripolyphosphate. J Drug Deliv Sci Technol 44:244–253. CrossRefGoogle Scholar
  67. Taokaew S, Nunkaew N, Siripong P, Phisalaphong M (2014) Characteristics and anticancer properties of bacterial cellulose films containing ethanolic extract of mangosteen peel. J Biomater Sci Polym 25:907–922. CrossRefGoogle Scholar
  68. Trovatti E, Freire CSR, Pinto PC, Almeida IF, Costa P, Silvestre AJD, Neto CP, Rosado C (2012) Bacterial cellulose membranes applied in topical and transdermal delivery of lidocainehydrochloride and ibuprofen: in vitro diffusion studies. Int J Pharm 435:83–87. CrossRefGoogle Scholar
  69. Tsouko E, Kourmentza C, Ladakis D, Kopsahelis N, Mandala I, Papanikolaou S, Paloukis F, Alves V, Koutinas A (2015) Bacterial cellulose production from industrial waste and by-product streams. Int J Mol Sci 16:14832–14849. CrossRefGoogle Scholar
  70. Ul- Islam M, Ullah MW, Khan S, Shah N, Park JK (2017) Strategies for cost-effective and enhanced production of bacterial cellulose. Int J Biol Macromol 102:1166–1173 CrossRefGoogle Scholar
  71. Ullah MW, Ul- Islam M, Khan S, Kim Y, Park JK (2015) Innovative production of bio-cellulose using a cell-free system derived from a single cell line. Carbohydr Polym 132:286–294. CrossRefGoogle Scholar
  72. Ullah MW, Ul- Islam M, Khan S, Kim Y, Jang JH, Park JK (2016) In situ synthesis of a bio-cellulose/titanium dioxide nanocomposite by using a cell-free system. RSC Adv 6:22424–22435. CrossRefGoogle Scholar
  73. Uzyol HK, Saçan MT (2017) Bacterial cellulose production by Komagataeibacter hansenii using algae-based glucose. Environ Sci Pollut Res 24:11154–11162. CrossRefGoogle Scholar
  74. Vadaye KE, Parivar K, Baharara J, Fazly Bazzaz BS, Iranbakhsh A (2018) The osteogenesis of bacterial cellulose scaffold loaded with fisetin. Iranian J Basic Med Sci 21:965–971. Google Scholar
  75. Wei B, Yang G, Hong F (2011) Preparation and evaluation of a kind of bacterial cellulose dry films with antibacterial properties. Carbohydr Polym 84:533–538. CrossRefGoogle Scholar
  76. Wu J, Zheng Y, Song W, Luan J, Wen X, Wu Z, Chen X, Wang Q, Guo S (2014) In situ synthesis of silver-nanoparticles/bacterial cellulose composites for slow-released antimicrobial wound dressing. Carbohydr Polym 102:762–771. CrossRefGoogle Scholar
  77. Yano H, Sugiyama J, Nakagaito AN, Nogi M, Matsuura T, Hikita M (2005) Optically transparent composites reinforced with networks of bacterial nanofibers. Adv Mater 17:153–155. CrossRefGoogle Scholar
  78. Yi-Hsuan T, Yu-Ning Y, Yi-Cheng H, Min-Lang T, Fwu-Long M (2018) Drug release and antioxidant/antibacterial activities of silymarin-zein nanoparticle/bacterial cellulose nanofiber composite films. Carbohyd Polym 180:286–296. CrossRefGoogle Scholar
  79. Ying L, Hua J, Wenfu Z, Niya G, Lili C, Xingyu J, Guang Y (2015) Bacterial cellulose–hyaluronan nanocomposite biomaterials as wound dressings for severe skin injury repair. J Mater Chem B 3:3498–3507. CrossRefGoogle Scholar
  80. Yuwono HS (2014) The new paradigm of wound management using coffee powder. Glob J Surg 2:25–29. Google Scholar
  81. Zarrinbakhsh N, Wang T, Uribe AR, Misra M, Mohanty AK, (2016) Characterization of Wastes and Coproducts from the Coffee Industry for Composite Material Production. Bio Resour 11: 7637–7653.
  82. Zhu C, Li F, Zhou X, Lin L, Zhang T (2013) Kombucha-synthesized bacterial cellulose: preparation, characterization, and biocompatibility evaluation. J Biomed Mater Res 102:1548–1557. CrossRefGoogle Scholar
  83. Zmejkoski D, Spasojević D, Orlovska I, Kozyrovska N, Soković M, Glamočlija J, Dmitrović S, Matović B, Tasić N, Maksimović V, Sosnin M, Radotić K (2018) Bacterial-cellulose-lignin composite hydrogel as a promising agent in chronic wound healing. Int J Biol Macromol 118:494–503. CrossRefGoogle Scholar
  84. Zuorro A, Lavecchia R (2012) Spent coffee grounds as a valuable source of phenolic compounds and bioenergy. J Clean Prod 34:49–56. CrossRefGoogle Scholar
  85. Żywicka A, Fijałkowski K, Junka A, Grzesiak J, El Fray M (2018) Modification of bacterial cellulose with quaternary ammonium compounds based on fatty acids and amino acids and the effect on antimicrobial activity. Biomacromol 19:1528–1538. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Nahla A. El-Wakil
    • 1
  • Enas A. Hassan
    • 1
    Email author
  • Mohammad L. Hassan
    • 1
  • Soheir S. Abd El-Salam
    • 2
  1. 1.Cellulose and Paper DepartmentNational Research CentreGizaEgypt
  2. 2.Microbology DepartmentBanha UniversityBanhaEgypt

Personalised recommendations