Extensional rheology of human saliva

Abstract

We have developed an oscillatory cross-slot extensional rheometer capable of performing measurements with unprecedentedly small volumes of test fluids (∼10–100 μL). This provides the possibility of studying exotic and precious or scarce bio-fluids, such as synovial fluid. To test our system, we have looked at a relatively abundant and accessible biological fluid, namely human saliva; a complex aqueous mixture of high molecular weight mucin molecules and other components. The results represent our first attempts to by this technique and as yet we have only sampled a small dataset. However, we believe we have produced the first successful quantitative measurements of extensional viscosity, Trouton ratio, and flow-induced birefringence made on saliva samples. The results significantly add to the scant literature on saliva rheology, especially in extension, and demonstrate the important role of saliva extensibility in relation to function.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  1. Backus C, Carrington SP, Fisher LR, Odell JA, Rodrigues DA (2002) The roles of extensional and shear flows of synovial fluid and replacement systems in joint protection. In: Kennedy JF, Phillips OG, Williams PA, Hascall VC (eds) Hyaluronan: chemical, biochemical and biological aspects, vol 1. Woodhead Publishing Ltd., Cambridge, pp 209–218

    Google Scholar 

  2. Beeley JA (1993) Fascinating families of proteins: electrophoresis of human saliva. Biochem Soc Trans 21:133–138

    CAS  Google Scholar 

  3. Briedis D, Moutrie MF, Balmer RT (1980) A study of the shear viscosity of human whole saliva. Rheol Acta 19:365–374

    Article  Google Scholar 

  4. Campese M, Sun X, Bosch JA, Oppenheim FG, Helmerhorst EJ (2009) Concentration and fate of histatins and acidic proline-rich proteins in the oral environment. Arch Oral Biol 54:345–353

    Article  CAS  Google Scholar 

  5. Carrington SP, Odell JA, Fisher L, Mitchell J, Hartley L (1996) Polyelectrolyte behaviour of dilute xanthan salt effects on extensional rheology. Polymer 37:2871–2875

    Article  CAS  Google Scholar 

  6. Carrington SP, Tatham JP, Odell JA, Saez AE (1997a) Macromolecular dynamics in extensional flows: 1. Birefringence and viscometry. Polymer 38:4151–4164

    Article  CAS  Google Scholar 

  7. Carrington SP, Tatham JP, Odell JA, Saez AE (1997b) Macromolecular dynamics in extensional flows: 2. The evolution of molecular strain. Polymer 38:4595–4607

    Article  CAS  Google Scholar 

  8. Clift AF, Scott-Blair GN (1945) Observations on certain rheological of human cervical secretions. Proc R Soc Med 39:1–9

    Google Scholar 

  9. Colby RH (2010) Structure and linear viscoelasticity of flexible polymer solutions: comparison of polyelectrolyte and neutral polymer solutions. Rheol Acta 49:425–442

    Article  CAS  Google Scholar 

  10. Craven TJ, Rees JM, Zimmerman WB (2010) Pressure sensor positioning in an electrokinetic microrheometer device: simulations of shear-thinning liquid flows. Microfluid Nanofluid 9:559–571

    Article  Google Scholar 

  11. Davies JR, Kirkham S, Svitacheva N, Thornton DJ, Carlstedt I (2007) MUC16 is produced in tracheal surface epithelium and submucosal glands and is present in secretions from normal human airway and cultured bronchial epithelial cells. Int J Biochem Cell Biol 39:1943–1954

    Article  CAS  Google Scholar 

  12. Davis SS (1971) The rheological properties of saliva. Rheol Acta 10:28–35

    Article  CAS  Google Scholar 

  13. Dewar MR, Parfitt GJ (1954) An investigation of the physical properties of saliva and their relationship to the mucin content. J Dent Res 33:596–605

    Article  CAS  Google Scholar 

  14. Erbring H (1936) Untersuchungen über die spinnbarkeit flussige systeme. Kolloid-Beihefte 44:171–177

    CAS  Google Scholar 

  15. Flory PJ (1969) Statistical mechanics of chain molecules. Interscience, New York

    Google Scholar 

  16. Fox PC, Bodner L, Tabak LA, Levine MJ (1985) Quantitation of total human salivary mucins. J Dent Res 64:327

    Google Scholar 

  17. Glantz P-O (1997) Interfacial phenomena in the oral cavity. Colloids Surf, A 123–124:657–670

    Article  Google Scholar 

  18. Graessley WW (1980) Polymer chain dimensions and the dependence of viscoelastic properties on concentration, molecular weight and solvent power. Polymer 21:258–262

    Article  CAS  Google Scholar 

  19. Hattrup CL, Gendler SJ (2008) Structure and function of the cell surface (tethered) mucins. Ann Rev Phys 70:431–457

    Article  CAS  Google Scholar 

  20. Haward SJ, Odell JA, Li Z, Yuan X-F (2010a) Extensional rheology of dilute polymer solutions in oscillatory cross-slot flow: the transient behaviour of birefringent strands. Rheol Acta 49:637–645. doi:10.1007/s00397-009-0420-6

    Google Scholar 

  21. Haward SJ, Odell JA, Li Z, Yuan X-F (2010b) The rheology of polymer solution elastic strands in extensional flow. Rheol Acta 49:781–788. doi:10.1007/s00397-010-0453-x

    Article  CAS  Google Scholar 

  22. Helmerhorst EJ, Oppenheim FG (2007) Saliva: a dynamic proteome. J Dent Res 86:680–693

    Article  CAS  Google Scholar 

  23. Keller A, Müller AJ, Odell JA (1987) Entanglements in semi-dilute solutions as revealed by elongational flow studies. Prog Colloid Polym Sci 75:179–200

    Article  Google Scholar 

  24. Kesimer M, Sheehan JK (2008) Analysing the functions of large glycoconjugates through the dissipative properties of their absorbed layers using the gel-forming mucin MUC5B as an example. Glycobiology 18:463–472

    Article  CAS  Google Scholar 

  25. Kesimer M, Makhov AM, Griffith JD, Verdugo P, Sheehan JK (2010) Unpacking a gel-forming mucin: a view of MUC5B organization after granular release. Am J Physiol Lung Cell Mol Physiol 298:L15–L22

    Article  Google Scholar 

  26. Kratky O, Porod G (1949) Röntgenuntersuchung gelöszer Fadenmoleküle. Rec Trav Chim Pays-Bas 68:1106–1123

    Article  CAS  Google Scholar 

  27. Lacombe CH, Essabbah H (1981) Comparative haemorheology of pathological blood. Scand J Clin Lab Investig 41:249–250

    Article  Google Scholar 

  28. Mehrotra R, Thornton DJ, Sheehan JK (1998) Isolation and physical characterization of the MUC7 (MG2) mucin from saliva: evidence for self-association. Biochem J 334:415–422

    CAS  Google Scholar 

  29. Odell JA, Carrington SP (2006) Extensional flow oscillatory rheometry. J Non-Newton Fluid Mech 137:110–120

    Article  CAS  Google Scholar 

  30. Pedersen AM, Bardow A, Beier Jensen S, Nauntofte B (2002) Saliva and gastrointestinal functions of taste, mastication, swallowing and digestion. Oral Dis 8:117–129

    Article  CAS  Google Scholar 

  31. Perkins TT, Smith DE, Chu S (1997) Single polymer dynamics in an elongational flow. Science 276:2016–2021

    Article  CAS  Google Scholar 

  32. Rayment SA, Liu B, Offner GD, Oppenheim FG, Troxler RF (2000) Immunoquantification of human salivary mucins MG1 and MG2 in stimulated whole saliva: factors influencing mucin levels. J Dent Res 79:1765–1772

    Article  CAS  Google Scholar 

  33. Raynal BDE, Hardingham TE, Thornton DJ, Sheehan JK (2002) Concentrated solutions of salivary MUC5B mucin do not replicate the gel-forming properties of saliva. Biochem J 362:289–296

    Article  CAS  Google Scholar 

  34. Riddiford CL, Jerrard HG (1970) Limitations on the measurement of relaxation times using a pulsed Kerr effect method. J Phys D Appl Phys 3:1314–1321

    Article  Google Scholar 

  35. Rossi S, Marciello M, Bonferoni MC, Ferrari F, Sandri G, Dacarro C, Grisoli P, Caramella C (2010) Thermally sensitive gels based on chitosan derivatives for the treatment of oral mucositis. Eur J Pharm Biopharm 74:248–254

    Article  CAS  Google Scholar 

  36. Round AN, Berry M, McMaster TJ, Stoll S, Gowers D, Corfield AP, Miles MJ (2002) Heterogeneity and persistence length in human ocular mucins. Biophys J 83:1661–1670

    Article  CAS  Google Scholar 

  37. Rubin BK (2007) Mucus structure and properties in cystic fibrosis. Paediatr Respir Rev 8:4–7

    Article  Google Scholar 

  38. Schipper RG, Silletti E, Vingerhoeds MH (2007) Saliva as research material: biochemical, physicochemical and practical aspects. Arch Oral Biol 52:1114–1135

    Article  CAS  Google Scholar 

  39. Schwarz WH (1987) The rheology of saliva. J Dent Res 66:660–666

    Google Scholar 

  40. Scrivener O, Berner C, Cressely R, Hocquart R, Sellin R, Vlachos NS (1979) Dynamical behaviour of drag-reducing polymer solutions. J Non-Newton Fluid Mech 5:475–495

    Article  CAS  Google Scholar 

  41. Sharma V, Jaishankar A, Wang Y-C, McKinley GH (2010) Rheology of globular proteins: apparent yield stress, high shear rate viscosity and interfacial viscoelasticity of bovine serum albumin solutions. Biophysical J

  42. Sheehan JK, Howard M, Richardson PS, Longwill T, Thornton DJ (1999) Physical characterization of a low-charge glycoform of the MUC5B mucin comprising the gel-phase of an asthmatic respiratory mucous plug. Biochem J 338:507–513

    Article  CAS  Google Scholar 

  43. Smith DE, Chu S (1998) Response of flexible polymers to sudden elongational flow. Science 281:1335–1340

    Article  CAS  Google Scholar 

  44. Stokes JR, Davies GA (2007) Viscoelasticity of human whole saliva collected after acid and mechanical stimulation. Biorheology 44:141–160

    CAS  Google Scholar 

  45. Thomsson KA, Prakobphol A, Leffler H, Reddy MS, Levine MJ, Fisher SJ, Hansson GC (2002) The salivary mucin MG1 (MUC5B) carries a repertoire of unique oligosaccharides that is large and diverse. Glycobiology 12:1–14

    Article  CAS  Google Scholar 

  46. Thornton DJ, Khan N, Mehrotra R, Howard M, Veerman E, Packer NH, Sheehan JK (1999) Salivary mucin MG1 is comprised almost entirely of different glycosylated forms of the MUC5B gene product. Glycobiology 9:293–302

    Article  CAS  Google Scholar 

  47. Treloar LKG (1975) The physics of rubber elasticity, 3rd edn. Clarendon, Oxford

    Google Scholar 

  48. Van Aken GA, Vingerhoeds MH, de Hoog EHA (2007) Food colloids under oral conditions. Curr Opin Colloid Interface Sci 12:251–262

    Article  Google Scholar 

  49. Van der Reijden WA, Veerman ECI, Amerongen AVN (1993a) Shear rate-dependent viscoelastic behaviour of human glandular salivas. Biorheology 30:141–152

    Google Scholar 

  50. Van der Reijden WA, Veerman ECI, Amerongen AVN (1993b) Erratum: shear rate-dependent viscoelastic behaviour of human glandular salivas. Biorheology 30:301

    Google Scholar 

  51. Waterman HA, Blom C, Holterman HJ, ‘s-Gravenmade EJ, Mellema J (1988) Rheological properties of human saliva. Arch Oral Biol 33:589–596

    Article  CAS  Google Scholar 

  52. Zussman E, Yarin AL, Nagler RM (2007) Age- and flow-dependency of salivary viscoelasticity. J Dent Res 86:281–285

    Article  CAS  Google Scholar 

Download references

Acknowledgements

JA Odell and SJ Haward gratefully acknowledge the financial support of the Engineering and Physical Sciences Research Council (EPSRC), UK. We thank professor GH McKinley for the use of his m-VROC rheometer.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Simon J. Haward.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Haward, S.J., Odell, J.A., Berry, M. et al. Extensional rheology of human saliva. Rheol Acta 50, 869–879 (2011). https://doi.org/10.1007/s00397-010-0494-1

Download citation

Keywords

  • Birefringence
  • Flow-induced orientation
  • Viscometry
  • Extensional flow
  • Saliva
  • Mucin