, Volume 26, Issue 1, pp 581–595 | Cite as

Viscoelastic properties of nanocellulose based inks for 3D printing and mechanical properties of CNF/alginate biocomposite gels

  • Ellinor B. Heggset
  • Berit L. Strand
  • Kristin W. Sundby
  • Sébastien Simon
  • Gary Chinga-Carrasco
  • Kristin SyverudEmail author
Original Paper


Inks for 3D printing based on cellulose nanofibrils (CNFs) or mixtures of CNFs and either cellulose nanocrystals (CNCs) or alginate were assessed by determining their viscoelastic properties i.e. complex viscosity and storage and loss moduli (G′ and G″). Two types of alginates were used, i.e. from Laminaria hyperborea stipe and Macrocystis pyrifera. Shape fidelity of 3D printed grids were qualitatively evaluated and compared to the viscoelastic properties of the inks. The biocomposite gels containing alginate were post stabilized by crosslinking with Ca2+. Mechanical properties of the crosslinked biocomposite gels were assessed. The complex viscosity, G′ and G″ of CNF suspensions increased when the solid content was increased from 3.5 to 4.0 wt%, but levelled off by further increase in CNF solid content. The complex viscosity at low angular frequency at 4 wt% was as high as 104 Pa·s. This seemed to be the necessary viscosity level for obtaining good shape fidelity of the printed structures for the studied systems. By replacing part of the CNFs with CNCs, the complex viscosity, G′ and G″ were reduced and so was also the shape fidelity of the printed grids. The changes in complex viscosity and moduli when CNFs was replaced with alginate depended on the relative amounts of CNFs/alginate. The type of alginate (from either L. hyp. stipe or M. pyr.) did not play a role for the viscoelastic properties of the inks, nor for the printed grids before post stabilization. Replacing CNFs with up to 1.5 wt% alginate gave satisfactory shape fidelity. The effect of adding alginate and subsequent crosslinking with Ca2+, strongly affected the strength properties of the gels. By appropriate choice of relative amounts of CNFs and alginate and type of alginate, the Young’s modulus and rupture strength could be controlled within the range of 30–150 kPa and 1.5–6 kg, respectively. The deformation at rupture was around 55%. The alginate from L. hyp. stipe yields higher Young’s modulus and lower syneresis compared to M. pyr. This shows that the choice of alginate plays a significant role for the mechanical properties of the final product, although it does not influence on the viscoelastic properties of the ink. The choice of alginate should be L. hyp. stipe if high strength is desired.

Graphical abstract


Nanocellulose Alginate Biocomposite Rheology 3D printing Hydrogels Mechanical properties 



This work has been funded by the Research Council of Norway through the NORCEL project, (Grant No. 228147). The AFM images were acquired using instruments available at NTNU NanoLab/NorFab. The Research Council of Norway is acknowledged for the support to the Norwegian Micro-and Nano-Fabrication Facility, NorFab, Project Number 245963/F50. We would like to thank Ingebjørg Leirset, Birgitte H. McDonagh, Ina S. Pedersen, Wenche I. Strand and Anne Marie Falkenberg Olsen for their technical support during this work.


  1. Aarstad OA, Tondervik A, Sletta H, Skjak-Braek G (2012) Alginate sequencing: an analysis of block distribution in alginates using specific alginate degrading enzymes. Biomacromol 13:106–116CrossRefGoogle Scholar
  2. Aarstad O, Strand BL, Klepp-Andersen LM, Skjak-Braek G (2013) Analysis of G-block distributions and their impact on gel properties of in vitro epimerized mannuronan. Biomacromol 14:3409–3416CrossRefGoogle Scholar
  3. Aarstad O, Heggset EB, Pedersen IS, Bjørnøy SH, Syverud K, Strand BL (2017) Mechanical properties of composite hydrogels of alginate and cellulose nanofibrils. Polymers-Basel 9:378CrossRefGoogle Scholar
  4. Agoda-Tandjawa G, Durand S, Berot S, Blassel C, Gaillard C, Garnier C, Doublier JL (2010) Rheological characterization of microfibrillated cellulose suspensions after freezing. Carbohydr Polym 80:677–686CrossRefGoogle Scholar
  5. Alexandrescu L, Syverud K, Gatti A, Chinga-Carrasco G (2013) Cytotoxicity tests of cellulose nanofibril-based structures. Cellulose 20:1765–1775. CrossRefGoogle Scholar
  6. Al-Hadithi TSR, Barnes HA, Walters K (1992) The relationship between the linear (oscillatory) and nonlinear (steady-state) flow properties of a series of polymer and colloidal systems. Colloid Polym Sci 270:40–46CrossRefGoogle Scholar
  7. Chinga-Carrasco G (2018) Potential and limitations of nanocelluloses as components in biocomposite inks for three-dimensional bioprinting and for biomedical devices. Biomacromol 19:701–711CrossRefGoogle Scholar
  8. Chinga-Carrasco G, Averianova N, Kondalenko O, Garaeva M, Petrov V, Leinsvang B, Karlsen T (2014) The effect of residual fibres on the micro-topography of cellulose nanopaper. Micron 56:80–84CrossRefGoogle Scholar
  9. Cox WP, Merz EH (1958) Correlation of dynamic and steady flow viscosities. J Polym Sci 28:619–622CrossRefGoogle Scholar
  10. Dai L et al (2019) 3D printing using plant-derived cellulose and its derivatives: a review. Carbohydr Polym 203:71–86CrossRefGoogle Scholar
  11. De France KJ, Hoare T, Cranston ED (2017) Review of hydrogels and aerogels containing nanocellulose. Chem Mater 29:4609–4631CrossRefGoogle Scholar
  12. Donati I, Holtan S, Morch YA, Borgogna M, Dentini M, Skjak-Braek G (2005) New hypothesis on the role of alternating sequences in calcium-alginate gels. Biomacromol 6:1031–1040CrossRefGoogle Scholar
  13. Dong H, Snyder JF, Williams KS, Andzelm JW (2013) Cation-induced hydrogels of cellulose nanofibrils with tunable moduli. Biomacromol 14:3338–3345. CrossRefGoogle Scholar
  14. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689CrossRefGoogle Scholar
  15. Habibi Y, Lucia LA, Rojas OJ (2010) Cellulose nanocrystals: chemistry, self-assembly, and applications. Chem Rev 110:3479–3500. CrossRefGoogle Scholar
  16. Haug A, Larsen B, Smidsrod O (1967) Studies on sequence of uronic acid residues in alginic acid. Acta Chem Scand 21:691–704CrossRefGoogle Scholar
  17. Heggset EB, Chinga-Carrasco G, Syverud K (2017) Temperature stability of nanocellulose dispersions. Carbohydr Polym 157:114–121. CrossRefGoogle Scholar
  18. Huan S, Ajdary R, Bai L, Klar V, Rojas OJ (2018) Low solids emulsion gels based on nanocellulose for 3D-printing. Biomacromolecules.
  19. Leppiniemi J et al (2017) 3D-printable bioactivated nanocellulose-alginate hydrogels. Acs Appl Mater Interfaces 9:21959–21970CrossRefGoogle Scholar
  20. Lowys MP, Desbrieres J, Rinaudo M (2001) Rheological characterization of cellulosic microfibril suspensions. Role of polymeric additives. Food Hydrocolloids 15:25–32CrossRefGoogle Scholar
  21. Markstedt K, Mantas A, Tournier I, Martinez Ávila H, Hägg D, Gatenholm P (2015) 3D bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules 16:1489–1496. CrossRefGoogle Scholar
  22. Martínez Ávila H, Schwarz S, Rotter N, Gatenholm P (2016) 3D bioprinting of human chondrocyte-laden nanocellulose hydrogels for patient-specific auricular cartilage regeneration. Bioprinting 1–2:22–35. CrossRefGoogle Scholar
  23. Mørch YA, Donati I, Strand BL, Skjak-Braek G (2007) Molecular engineering as an approach to design new functional properties of alginate. Biomacromolecules 8:2809–2814CrossRefGoogle Scholar
  24. Mørch YA, Holtan S, Donati I, Strand BL, Skjåk-Bræk G (2008) Mechanical properties of C-5 epimerized alginates. Biomacromolecules 9:2360–2368CrossRefGoogle Scholar
  25. Muller M, Ozturk E, Arlov O, Gatenholm P, Zenobi-Wong M (2017) Alginate sulfate-nanocellulose bioinks for cartilage bioprinting applications. Ann Biomed Eng 45:210–223CrossRefGoogle Scholar
  26. Naderi A, Lindstrom T, Sundstrom J (2014) Carboxymethylated nanofibrillated cellulose: rheological studies. Cellulose 21:1561–1571CrossRefGoogle Scholar
  27. Nascimento DM et al (2018) Nanocellulose nanocomposite hydrogels: technological and environmental issues. Green Chem 20:2428–2448CrossRefGoogle Scholar
  28. Pääkkö M et al (2007) Enzymatic hydrolysis combined with mechanical shearing and high-pressure homogenization for nanoscale cellulose fibrils and strong gels. Biomacromolecules 8:1934–1941. CrossRefGoogle Scholar
  29. Peppas NA, Khare AR (1993) Preparation, structure and diffusional behavior of hydrogels in controlled-release. Adv Drug Deliv Rev 11:1–35CrossRefGoogle Scholar
  30. Piras CC, Fernandez-Prieto S, De Borggraeve WM (2017) Nanocellulosic materials as bioinks for 3D bioprinting. Biomater Sci UK 5:1988–1992CrossRefGoogle Scholar
  31. Poonguzhali R, Basha SK, Kumari VS (2017) Synthesis and characterization of chitosan-PVP-nanocellulose composites for in vitro wound dressing application. Int J Biol Macromol 105:111–120CrossRefGoogle Scholar
  32. Rashad A, Mustafa K, Heggset EB, Syverud K (2017) Cytocompatibility of wood-derived cellulose nanofibril hydrogels with different surface chemistry. Biomacromolecules 18:1238–1248CrossRefGoogle Scholar
  33. Rashad A et al (2018) Coating 3D printed polycaprolactone scaffolds with nanocellulose promotes growth and differentiation of mesenchymal stem cells. Biomacromolecules.
  34. Rees A, Powell LC, Chinga-Carrasco G, Gethin DT, Syverud K, Hill KE, Thomas DW (2015) 3D bioprinting of carboxymethylated-periodate oxidized nanocellulose constructs for wound dressing applications. BioMed Res Int 2015:925757CrossRefGoogle Scholar
  35. Saito T, Isogai A (2004) TEMPO-mediated oxidation of native cellulose. The effect of oxidation conditions on chemical and crystal structures of the water-insoluble fractions. Biomacromolecules 5:1983–1989CrossRefGoogle Scholar
  36. Saito T, Isogai A (2006) Introduction of aldehyde groups on surfaces of native cellulose fibers by TEMPO-mediated oxidation. Colloids Surf A 289:219–225. CrossRefGoogle Scholar
  37. Siqueira G et al (2017) Cellulose nanocrystal inks for 3D printing of textured cellular architectures. Adv Funct Mater:27Google Scholar
  38. Smidsrod O (1972) Properties of poly(1,4-Hexuronates) in gel state. 2. Comparison of gels of different chemical composition. Acta Chem Scand 26:79–88CrossRefGoogle Scholar
  39. Sultan S, Siqueira G, Zimmermann T, Mathew AP (2017) 3D printing of nano-cellulosic biomaterials for medical applications. Curr Opin Biomed Eng 2:29–34CrossRefGoogle Scholar
  40. Syverud K (2017) Tissue engineering using plant derived cellulose nanofibrils (CNF) as scaffold material. In: Atalla R, Isogai A, Agarwal U (eds) Nanocelluloses, their preparation, properties, and applications. ACS Books, WashingtonGoogle Scholar
  41. Unnithan AR, Sasikala ARK, Sathishkumar Y, Lee YS, Park CH, Kim CS (2014) Nanoceria doped electrospun antibacterial composite mats for potential biomedical applications. Ceram Int 40:12003–12012CrossRefGoogle Scholar
  42. Wågberg L, Decher G, Norgren M, Lindström T, Ankerfors M, Axnäs K (2008) The build-up of polyelectrolyte multilayers of microfibrillated cellulose and cationic polyelectrolytes. Langmuir 24:784–795. CrossRefGoogle Scholar
  43. Wang QQ, Sun JZ, Yao Q, Ji CC, Liu J, Zhu QQ (2018) 3D printing with cellulose materials. Cellulose 25:4275–4301CrossRefGoogle Scholar
  44. Xu WY, Wang XJ, Sandler N, Willfor S, Xu CL (2018) Three-dimensional printing of wood-derived biopolymers: a review focused on biomedical applications. ACS Sustain Chem Eng 6:5663–5680CrossRefGoogle Scholar
  45. Zander NE, Dong H, Steele J, Grant JT (2014) Metal cation cross-linked nanocellulose hydrogels as tissue engineering substrates. Acs Appl Mater Interfaces 6:18502–18510CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.RISE PFITrondheimNorway
  2. 2.NOBIPOL, Department of Biotechnology and Food SciencesNTNU Norwegian University of Science and TechnologyTrondheimNorway
  3. 3.BorregaardSarpsborgNorway
  4. 4.Department of Chemical EngineeringNTNU Norwegian University of Science and TechnologyTrondheimNorway

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