bacterial cellulose towards functional green composites

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Copyright copy 2011 American Scientific PublishersAll rights reservedPrinted in the United States of America

Journal ofBionanoscience

Vol 5 167ndash172 2011

Bacterial Cellulose Towards Functional GreenComposites Materials

Ligia Maria Manzine Costa1 Gabriel Molina de Olyveira1lowast Pierre Basmaji2 and Lauro Xavier Filho31Department of Nanoscience and Advanced materials Rua Santa Adeacutelia 166 Santo Andreacute-SP 09291-210 Brazil

2Innovatecrsquos - Biotechnology Research and Development Sao Carlos SP 13566-610 Brazil3Natural Products Laboratory and Biotechnology IPT UNIT Aracaju-Sergipe 49032-490 Brazil

Nanobiocellulose has established to be a remarkably versatile biomaterial and can be used in widevariety of applied scientific endeavours especially for medical devices In fact biomedical devicesrecently have gained a significant amount of attention because of an increased interest in tissue-engineered products for both wound care and the regeneration of damaged or diseased organs Dueto its unique nanostructure and properties microbial cellulose is a natural candidate for numerousmedical and tissue-engineered applications The architecture of nanobiocellulose materials can beengineered over length scales ranging from nano to macro by controlling the biofabrication processIn this work bacterial cellulose biocomposites were obtained by change fermentation medium withsugar cane honey and dates paste (Dibs) SEM and AFM images showed differents surface mor-phology FTIR analysis found some interactions between these additives DSC and TGA showedhigher thermal properties and change crystallinity of the developed bionanocomposite

Keywords Bacterial Cellulose Green Composites Bionanocomposites Functional Materials

1 INTRODUCTION

Microbial cellulose is an exopolysaccharide producedby various species of bacteria such as those ofthe genera Gluconacetobacter (formerly Acetobacter)Agrobacterium Aerobacter Achromobacter Azotobac-ter Rhizobium Sarcina and Salmonella1 Many Gram-negative bacteria secrete extracellular polysaccharidematerial but only a few have been shown to produce cel-lulose A xylinum the most studied of bacterial cellu-lose producers is a Gram-negative aerobic rod-shapedorganism2 Plant and bacterial celluloses have identi-cal chemical structure but different physical and chem-ical properties Recently nanocellulose has been calledas the eyes of biomaterial highly applicable to biomedi-cal industry which includes skins replacements for burn-ings and wounds blood vessel growth nerves gum anddura-mater reconstruction scaffolds for tissue engineer-ing stent covering and bone reconstruction34 The per-formance of bacterial cellulose stems from its high purityultra-fine network structure and high mechanical proper-ties in dry state56 These features allow its applications inscaffold for tissue regeneration medical applications andnanocomposites

lowastAuthor to whom correspondence should be addressed

The structural features of microbial cellulose its prop-erties and compatibility of the biomaterial for regenera-tive medicine can be changed modifying its or surfacemodification by physical78 and chemical methods910 toobtain a biomaterial with less rejection with celular con-tact and blood contact cells interation Shaping of bac-terial cellulose materials in the culture medium can becontrolled by the type of cultivation that changes chainsizes origin of strains that produced different proportionof crystalline phase of bacterial cellulose and kind ofbioreactor Then it obtained bacterial cellulose hydrogelor in dry state by methods like freeze-drying1112 Thereis several factors that affecting cellulose production likegrowth medium environmental condictions and byprod-ucts Generally medium containing high carbon betweenothers (often nitrogen) is favourable for polysaccharideproduction1314

Sani et al improve the production of bacterial cellu-lose nanofibres by using CSL and molasses as nitrogenand carbon source respectively Molasses is found to be abetter carbon source than glucose Molasses is about 50sugar by dry weight predominantly sucrose but also con-taining significant amounts of glucose and fructose Thenon-sugar content includes many salts such as calciumpotassium oxalate and chloride Moreover higher yieldsof BC obtained by glycerol acetic acid hydrolyzate of

J Bionanosci 2011 Vol 5 No 2 1557-791020115167006 doi101166jbns20111060 167


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Bacterial Cellulose Towards Functional Green Composites Materials Costa et al

konjac powder plant infusions such as tea (Camellia sine-sis) and the combined use of fructose glucose and aceticacid15

Manipulating BC biogenesis can be a useful approachfor fine-tuning BC properties to appropriate applications orfor producing BC composites with tailored characteristicsA few researchers have undertaken this approach includ-ing Ciechanska16 who fabricated modified BC by growingit in a chitosan-modified growth medium for wound dress-ing application and Ref [17] who produced modifiedBC in a carboxymethylcellulose- methylcellulose- andpoly(vinyl alcohol)-modified medium to produce water-content-controlled BC for medically useful biomaterialsBodin et al obtained BC tubes with different shapes

and sizes depending on the product requirements whichhas made BC interesting to be explored for use in otherbiomedical applications such as bone graft material anda scaffold for tissue engineering of cartilage and bloodvessels18

Tang et al obtained BC mats with different pore sizeand porosities changed fermentation conditions (cultiva-tion time and inoculation volume) and post-treatmentmethods (alkali treatment and drying methods)19

Backdahl et al produced a novel method to introducemicroporosity in BC tubes intended as scaffolds for tissue-engineered blood vessels by placing paraffin wax andstarch particles of various sizes in a growing culture ofAcetobacter xylinum bacterial cellulose scaffolds of dif-ferent morphologies and interconnectivity were preparedParaffin particles were incorporated throughout the scaf-fold while starch particles were found only in the outer-most area of the resulting scaffold20

Grande et al developed self-assembled nanocompositesof cellulose synthesized by Acetobacter bacteria and nativestarch Potato and corn starch were added into the culturemedium and partially gelatinized in order to allow the cel-lulose nanofibrils to grow in the presence of a starch phaseStructural properties determined by XRD and ATR-FTIRshowed that the crystallinity of BC was preserved in spiteof the presence of starch hence the mechanical propertiesof the nanocomposites showed no significant decrease21

However scaffoldrsquos success depends much on the cel-lular adhesion and growth onto the surface thus biopoly-merrsquos chemical surface can dictates cellular response byinterfering in cellular adhesion proliferation migrationand functioning So changes both in the fermentation pro-cess and structural changes especially superficial attemptto achieve this goal22 Several cellular activities such asadhesion proliferation migration differentiation and cellshape are influenced by the ECM in which they reside Inspite of different cell types and nanoscale features somegeneral rules are shared by these cellndashsubstrate interac-tions Cells identify the exposed surface topography andnanofibers features like porous matrices and alignmentinfluence the adhesion spreading proliferation and gene

expression of various cell types seeded on them Differ-ents cell behaviors were found in several surface topog-raphy obtained from lithography2324 phase separation25

electrospinning26 nanoimpriting27 self-assembly28

Among various applications studied so far which hasalready reached the level of practical use is related to elec-tronic industry with acoustic diaphragms sensor applica-tions and Organic Light Emitting Diode29ndash32 In this workbacterial cellulose biocomposites were obtained by changefermentation medium with sugar cane honey and datespaste (Dibs) to produce a biomaterial with potential appli-cations in medicine food packing and sensor applications

2 EXPERIMENTAL DETAILS

21 Materials

Bacterial cellulose membranes sim500 mm thick weresupplied from Innovatecs-Produtos Biotecnoloacutegicos LtdaBrazil Sugar cane extract were purchased from HangzhouNew Asia International Co Dates paste extract wasobtained from Kharja Date Packing Factory during thesorting operations of the high quality fruits and honey sam-ples were purchased from Zhejiang Jiangshan Bee Enter-prise Co Ltd

22 Synthesis and Fermentation of Bacterial Cellulose

The acetic fermentation process is achieved by using thesugar as carbohydrate source Different carbon sources canbe used for the cellulose synthesis namely glucose fruc-tose cane sugar dibs honey Results of this process wouldbe vinegar and a nanobiocellulose biomass The modi-fied process is based on the addition of sugar cane datespaste or honey (1 ww) to the culture medium beforebacteria are inoculated After being added to the culturemedium the medium is autoclaved at 100 C Then bac-terial Cellulose (BC) produced by Gram-negative bacteriaGluconacetobacter xylinus can be obtained from the cul-ture medium in the pure 3-D structure consisting of anultra fine network of cellulose nanofibres (3ndash8 nm) highlyhydrated (99 in weight) and displaying higher molecularweight higher cellulose crystallinity (60ndash90) enormousmechanical strength and full biocompatibility33

23 Bionanocomposites Characterization

Scanning Electron Microscopy (SEM)-Scanning electronicmicroscopy images were performed on a PHILIPS XL30FEG The samples were covered with gold and silver paintfor electrical contact and to perform the necessary imagesSurface morphology of nanocellulose was observed

using atomic force microscopy NanoScope IVa Multi-mode SPM (Veeco Inc) in tapping modeTransmission infrared spectroscopy (FTIR Perkin

Elmer Spectrum 1000)-Influences of Honey dibs and sugar

168 J Bionanosci 5 167ndash172 2011


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Costa et al Bacterial Cellulose Towards Functional Green Composites Materials

cane in bacterial cellulose was analyzed in the rangebetween 250 and 4000 cmminus1 and with resolution of 2 cmminus1

with samplesDifferential scanning calorimetry (DSC)-To analyze the

crystalline and thermal behavior of biocomposites calori-metric experiments were carried out with the help of dif-ferential scanning calorimetry (DSC 822 Mettler ToledoSwitzerland) The measurements were done at the heat-ing rate of 10 celsiusmin and the temperature range was25 Cndash700 CTGA- Thermogravimetric analysis (TGA) was carried

out for biocomposites using a NETZSCH TG 209F1 inHelium environment with a heating rate of 30 Cmin Thetemperature range scanned was from 50 C to 700 C Theweight of all specimens was maintained around 10 mg

3 RESULTS AND DISCUSSION

31 Bacterial Cellulose Mats

Bacterial cellulose mats were characterized by SEM andAFM Figure 1 shows as an example SEM image of bac-terial cellulose formation from (a) sugar cane (b) dibsand (c) honey respectively These results confirm that theBC is ideal scaffold requires with porous structure whichcan provide maximum integration with cells and body flu-ids plus have a nanostructure surface which facilitates theadhesion of cellsThe morphological changes such as size and bacterial

cellulose fibers surface can be observed by AFM fromeach BC production Clearly AFM images shows that bychanging the culture medium of bacterial cellulose resultsin an excellent dispersion of nanofibers with high aspectratio and these fibers has thickness from 30ndash40 nm Oth-erwise these alterations resulting in surface roughnesschanges too It is known that the surface roughness isrelated to the recoverable strain of the material and con-sequently the optical properties presented in the film Ahigh roughness is related to the presence of large coarsespherulites leading to greater opacity of the film34 Soclearly in Figure 2 it can be concluded that Figures 2(b)and (c) has high roughness and presence of large coarsespherulites than Figure 2(a)

32 Interaction Between Bacterial Cellulose andFermentation Components

In order to analyze influences of sugar cane dibs andhoney in bacterial cellulose chemical structure FTIR spec-trum of absorption was analyzed in the range between250 and 4000 cmminus1 and with resolution of 2 cmminus1 withsamples The main chemical groups of the bacterial cellu-lose in infrared spectroscopy are 3500 cmminus1 OH stretch-ing 2900 cmminus1 CH stretching of alkane and asymmetricCH2 stretching 2700 cmminus1 CH2 symmetric stretching

(a)

(b)

(c)

Fig 1 Scanning electron microscopy (SEM) of Bacterial cellulosefrom (a) sugar cane (b) dibs and (c) honey respectively

1640 cmminus1 OH deformation 1400 cmminus1 CH2 deforma-tion 1370 cmminus1 CH3 deformation 1340 cmminus1 OH defor-mation and 1320ndash1030 cmminus1 CO deformation35

In Figure 3 infrared spectrum of modified bacterial cel-lulose is analyzed The FTIR- spectrum shows absorp-tion peak in the region of 3400 cmminus1 characteristicsof hydroxyl absorption bands probably due interactionbetween bacterial cellulose with honey dibs and sugar-cane It can be observed large CO2 impurity in 2300 cmminus1

J Bionanosci 5 167ndash172 2011 169


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(a)

(b)

(c)

Fig 2 Force Atomic Microscope (AFM) of Bacterial cellulose from(a) sugar cane (b) dibs and (c) honey respectively

at the time of measurement Another absorption peak wasobtained in the range of 1490 cmminus1 which shows the pres-ence of a carbonyl group in the bacterial cellulose togetherwith bonds corresponding to those of glycoside includ-ing CndashOndashC at 1162 cmminus1 (as in case of natural cellu-lose) These results clearly shows one possible interactionbetween bacterial cellulose and honey dibs and sugarcane

Fig 3 FTIR Spectra of Bacterial cellulose from sugar cane dibs andhoney

mainly by hydrogen interactions between hydroxyl andcarbonyl groups

33 Thermal Analysis

TGA- In order to analyze thermal behavior for bio-nanocomposites are characterized typical weight lossverses temperature plots The TG spectrum (Fig 4) showsa weak loss of weight due to the evaporation of water(at temp 85 C) and also quick drop in weight at a tem-perature of approx 300 C is mainly attributed to ther-mal depolymerization of hemicellulose and the cleavageof glycosidic linkages of cellulose3637 complete degrada-tion of cellulose take place between 275 and 400 C3839

The TG curve shows that the maximum rate of degrada-tion occurs at temperature of approx 370 C for bacterialcellulosecane sugar and bacterial cellulosedibs How-ever bacterial cellulosehoney has higher degradation attemperature of approx 450 C mainly because of highercrystallinity rate These results clearly evidence higherthermal behavior with developed bionanocomposites thanpure bacterial cellulose mats

Fig 4 TGA thermogram of Bacterial cellulose from sugar cane dibsand honey



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Fig 5 DSC curves of Bacterial cellulose from sugar cane dibs andhoney

DSC- The crystallization behavior in the bionanocom-posites was carried out by DSC tests It can be observedin Figure 5 heating curves of bionanocomposites Fromthe course of the curve the first transformation is relatedto the evaporation of water at an endothermic maximumof 85 C According to literature at a temperatures of 80ndash140 C there is an know transformation related to themelting of the crystalline phase of cellulose40 The nexttransformation occurs only at the temperature of approx355 C leading to the decomposition of the sampleAll systems analyzed presents differents thermal behav-

ior It can be observed that cane sugar addition cause peakbroading probably caused by the presence of crystals withdifferent thicknesses and varying degrees of perfectionbecause the addition of filler Besides it can be observedin Figure 5 that system has fusion peaks shifts to lowertemperatures and with less crystals to merge characteris-tic of a system with lower crystallinity Otherwise honeyand dibs addition facilitated the mobility in crystallizationprocess with obtained symmetrical crystals and crystal-lization occurred at higher temperatures characteristic ofa system with higher crystallinity

4 CONCLUSIONS

Bacterial cellulose with its characteristics like nanofiberssize and distribution mechanical properties compatibil-ity and ability to mold is a biomaterial indispensablein health area It was the intention of this work tobroaden knowledge in this subject area and stimulatethe practical application of bacterial cellulose with newmaterials and biocomposites obtained with fermenta-tion control for potential applications in medicine foodpacking and sensor applications It can concluded afterfermentation bioprocess change that SEM and AFMimages showed differents surface morphology FTIR anal-ysis found some interactions between these additivesDSC and TGA showed higher thermal properties and

change crystallinity of the developed bionanocompositesHoneybacterial cellulose sample presents higher crys-tallinity and cane sugarbacterial cellulose sample presentslower crystallinity in studied system

References and Notes

1 P Ross R Mayer and M Benziman Microbiol Rev 55 35 (1991)2 S Bielecki A Krystynowicz M Turkiewicz and H Kalinowska

Polysaccharides and Polyamides in the Food Industry edited byA Steinbuumlchel S K Rhee Wiley-VCH Verlag Weinheim (2005)pp 1ndash10

3 G M Olyveira L M M Costa and P Basmaji NSTI-Nanotechnol3 267 (2011)

4 D Klemm D Schumann U Udhardt and S Marsch Prog PolymSci 26 1561 (2001)

5 P Gatenholm and D Klemm MRS Bulletin 35 208 (2010)6 W K Czaja D J Young and M Kawecki Biomacromolecules 8 1

(2007)7 B Gupta C Plummer and I Bisson Biomaterials 23 863

(2002)8 P Hamerli T Weigel and T Groth Biomaterials 24 3989

(2003)9 S E DrsquoSouza M H Ginsberg and E F Plow Trends Biochem Sci

16 246 (1991)10 M Gabriel G P Van Nieuw Amerongen V W M Van Hinsbergh

A V Van Nieuw Amerongen and A Zentner J BiomaterSci Polym 17 567 (2006)

11 G M Olyveira D P Valido L M M Costa P B P Gois L XFilho and P Basmaji J Biomater Nanobiotechnol 2 239 (2011)

12 M Matsuoka T Tsuchida K Matsushita K Adachio andF Yoshinga Biosci Biotechnol Biochem 60 575 (1996)

13 K V Ramana A Tomar and L Singh World J MicrobiolBiotechnol 16 245 (2000)

14 S Masaoka T Ohe and N Sakota J Ferment Bioeng 75 18(1993)

15 A Sani and Y Dahman J Chem Technol Biotechnol 85 151(2010)

16 D Cienchanska Fibres Text East Eur 12 69 (2004)17 M Seifert S Hesse V Kabrelian and D Klemm J Polym Sci A1

42 463 (2004)18 A Bodin H Baumlckdahl H Fink L Gustafsson B Risberg and

P Gatenholm Biotechnol Bioeng 97 425 (2007)19 W Tang S Jia Y Jia and H Yang World J Microbiol Biotechnol

26 125 (2010)20 H Baumlckdahl M Esquerra D Delbro B Risberg and P Gatenholm

J Tissue Eng Regen Med 2 320 (2008)21 J C Grande F G Torres C M Gomez O P Troncoso J Canet-

Ferrer and J Martiacutenez-Pastor Mater Sci Eng C 29 1098 (2009)22 A Teixeira G A Abrams and P J Bertics J Cell Sci 116 1881

(2003)23 A I Teixeira P F Nealey and C J Murphy J Biomed Mater Res

71 369 (2004)24 A M Rajnicek and C D Mc Craig J Cell Sci 110 2915 (1997)25 V J Chen L A Smith and P X Ma Biomaterials 27 3973 (2006)26 K H Kim L Jeong and H Park J Biotechnol 120 327 (2005)27 E K F Yim R M Reano and S W Pang Biomaterials 26 5405

(2005)28 D A Harrington E Y Cheng and M O Guler J Biomed Mater

Res 78 157 (2006)29 M Iguchi S Yamanaka and A Budhiono J Mater Sci 35 261

(2000)30 M Szymanska-Chargot J Cybulska and A Zdunek Sensors

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31 Y Okahisa A Yoshida I S Miyaguch and H Yano Compos SciTechnol 69 1958 (2009)

32 M Nogi and H Yano Adv Mater 20 1849 (2008)33 D Klemm B Heublein H P Fink and A Bohn Polym Sci

44 3358 (2005)34 L M Guerrini P Paulin Filho R E S Bretas and A Bernardi

PoliacutemerosCiecircncia e Tecnologia 14 38 (2004)35 R G Zhbanko Infrared Spectra of Cellulose and Its Derivates

edited by B I Stepanov Translated from the Russian by A BDensham Consultants Bureau New York (1966) pp 325ndash333

36 B L Manfredi E S Rodriguez M Wladyka-Przybylak andA Vazquez Polym Degrad Stab 91 255 (2006)

37 S Ouajai and R A Shanks Polym Degrad Stab 89 327 (2005)38 V A Alvarez and A Vazquez Polym Degrad Stab 84 13

(2004)39 B Deepa E Abraham B M Cherian A Bismarc J J Blaker

L A Pothan A L Leao S F Souza and M Kottaisamy BioresourTechnol 102 1988 (2011)

40 J George K V Ramana S N Sabapathy J H Jagannath and A SBawa Int J Biol Macromol 37 189 (2005)

Received 10 December 2011 Accepted 16 February 2012



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konjac powder plant infusions such as tea (Camellia sine-sis) and the combined use of fructose glucose and aceticacid15

Manipulating BC biogenesis can be a useful approachfor fine-tuning BC properties to appropriate applications orfor producing BC composites with tailored characteristicsA few researchers have undertaken this approach includ-ing Ciechanska16 who fabricated modified BC by growingit in a chitosan-modified growth medium for wound dress-ing application and Ref [17] who produced modifiedBC in a carboxymethylcellulose- methylcellulose- andpoly(vinyl alcohol)-modified medium to produce water-content-controlled BC for medically useful biomaterialsBodin et al obtained BC tubes with different shapes

and sizes depending on the product requirements whichhas made BC interesting to be explored for use in otherbiomedical applications such as bone graft material anda scaffold for tissue engineering of cartilage and bloodvessels18

Tang et al obtained BC mats with different pore sizeand porosities changed fermentation conditions (cultiva-tion time and inoculation volume) and post-treatmentmethods (alkali treatment and drying methods)19

Backdahl et al produced a novel method to introducemicroporosity in BC tubes intended as scaffolds for tissue-engineered blood vessels by placing paraffin wax andstarch particles of various sizes in a growing culture ofAcetobacter xylinum bacterial cellulose scaffolds of dif-ferent morphologies and interconnectivity were preparedParaffin particles were incorporated throughout the scaf-fold while starch particles were found only in the outer-most area of the resulting scaffold20

Grande et al developed self-assembled nanocompositesof cellulose synthesized by Acetobacter bacteria and nativestarch Potato and corn starch were added into the culturemedium and partially gelatinized in order to allow the cel-lulose nanofibrils to grow in the presence of a starch phaseStructural properties determined by XRD and ATR-FTIRshowed that the crystallinity of BC was preserved in spiteof the presence of starch hence the mechanical propertiesof the nanocomposites showed no significant decrease21

However scaffoldrsquos success depends much on the cel-lular adhesion and growth onto the surface thus biopoly-merrsquos chemical surface can dictates cellular response byinterfering in cellular adhesion proliferation migrationand functioning So changes both in the fermentation pro-cess and structural changes especially superficial attemptto achieve this goal22 Several cellular activities such asadhesion proliferation migration differentiation and cellshape are influenced by the ECM in which they reside Inspite of different cell types and nanoscale features somegeneral rules are shared by these cellndashsubstrate interac-tions Cells identify the exposed surface topography andnanofibers features like porous matrices and alignmentinfluence the adhesion spreading proliferation and gene

expression of various cell types seeded on them Differ-ents cell behaviors were found in several surface topog-raphy obtained from lithography2324 phase separation25

electrospinning26 nanoimpriting27 self-assembly28

Among various applications studied so far which hasalready reached the level of practical use is related to elec-tronic industry with acoustic diaphragms sensor applica-tions and Organic Light Emitting Diode29ndash32 In this workbacterial cellulose biocomposites were obtained by changefermentation medium with sugar cane honey and datespaste (Dibs) to produce a biomaterial with potential appli-cations in medicine food packing and sensor applications

2 EXPERIMENTAL DETAILS

21 Materials

Bacterial cellulose membranes sim500 mm thick weresupplied from Innovatecs-Produtos Biotecnoloacutegicos LtdaBrazil Sugar cane extract were purchased from HangzhouNew Asia International Co Dates paste extract wasobtained from Kharja Date Packing Factory during thesorting operations of the high quality fruits and honey sam-ples were purchased from Zhejiang Jiangshan Bee Enter-prise Co Ltd

22 Synthesis and Fermentation of Bacterial Cellulose

The acetic fermentation process is achieved by using thesugar as carbohydrate source Different carbon sources canbe used for the cellulose synthesis namely glucose fruc-tose cane sugar dibs honey Results of this process wouldbe vinegar and a nanobiocellulose biomass The modi-fied process is based on the addition of sugar cane datespaste or honey (1 ww) to the culture medium beforebacteria are inoculated After being added to the culturemedium the medium is autoclaved at 100 C Then bac-terial Cellulose (BC) produced by Gram-negative bacteriaGluconacetobacter xylinus can be obtained from the cul-ture medium in the pure 3-D structure consisting of anultra fine network of cellulose nanofibres (3ndash8 nm) highlyhydrated (99 in weight) and displaying higher molecularweight higher cellulose crystallinity (60ndash90) enormousmechanical strength and full biocompatibility33

23 Bionanocomposites Characterization

Scanning Electron Microscopy (SEM)-Scanning electronicmicroscopy images were performed on a PHILIPS XL30FEG The samples were covered with gold and silver paintfor electrical contact and to perform the necessary imagesSurface morphology of nanocellulose was observed

using atomic force microscopy NanoScope IVa Multi-mode SPM (Veeco Inc) in tapping modeTransmission infrared spectroscopy (FTIR Perkin

Elmer Spectrum 1000)-Influences of Honey dibs and sugar



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(a)

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(c)






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bacterial cellulose towards functional green composites

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