journal article·2016-01

Characterization of irreversible physio-mechanical processes in stretched fetal membranes

Yulia Marom, Shlomit Goldman, Eliezer Shalev, Doron Shilo

Acta Biomaterialia· Volume 30
Publisher page

Abstract

We perform bulge tests on live fetal membrane (FM) tissues that simulate the mechanical conditions prior to contractions. Experimental results reveal an irreversible mechanical behavior that appears during loading and is significantly different than the mechanical behavior that appears during unloading or in subsequent loading cycles. The irreversible behavior results in a residual strain that does not recover upon unloading and remains the same for at least 1h after the FM is unloaded. Surprisingly, the irreversible behavior demonstrates a linear stress-strain relation. We introduce a new model for the mechanical response of collagen tissues, which accounts for the irreversible deformation and provides predictions in agreement with our experimental results. The basic assumption of the model is that the constitutive stress-strain relationship of individual elements that compose the collagen fibers has a plateau segment during which an irreversible transformation/deformation occurs. Fittings of calculated and measured stress-strain curves reveal a well-defined single-value property of collagenous tissues, which is related to the threshold strain εth for irreversible transformation. Further discussion of several physio-mechanical processes that can induce irreversible behavior indicate that the most probable process, which is in agreement with our results for εth, is a phase transformation of collagen molecules from an α-helix to a β-sheet structure. A phase transformation is a manifestation of a significant change in the molecular structure of the collagen tissues that can alter connections with surrounding molecules and may lead to critical biological changes, e.g., an initiation of labor. Statement of significance This study is driven by the hypothesis that pre-contraction mechanical stretch of the fetal membrane (FM) can lead to a change in the microstructure of the FM, which in turn induces a critical biological (hormonal) change that leads to the initiation of labor. We present mechanical characterizations of live FM tissues that reveal a significant irreversible process and a new model for the mechanical response of collagen tissues, which accounts for this process. Fittings of calculated and measured results reveal a well-defined single-value property of collagenous tissues, which is related to the threshold strain for irreversible transformation. Further discussion indicates that the irreversible deformation is induced by a phase transformation of collagen molecules that can lead to critical biological changes.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Preterm Birth and Chorioamnionitis · Reproductive System and Pregnancy · Collagen: Extraction and Characterization

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (68)

Show source-provided references
1. ACOG practice bulletin #56: multiple gestation: complicated twin, triplet, and high-order multifetal pregnancy10.1097/00006250-200410000-00046 ↗
2. Outcomes of children of extremely low birthweight and gestational age in the 1990’s10.1053/siny.1999.0001 ↗
3. Mechanical failure of human fetal membrane tissues10.1023/B:JMSM.0000030205.62668.90 ↗
4. Term human fetal membranes have a weak zone overlying the lower uterine pole and cervix before onset of labor10.1095/biolreprod.104.033647 ↗
5. Fetal membranes from term vaginal deliveries have a zone of weakness exhibiting characteristics of apoptosis and remodeling10.1016/j.jsgi.2005.12.010 ↗
6. Relation between mechanical properties and microstructure of human fetal membranes: an attempt towards a quantitative analysis10.1016/j.ejogrb.2009.02.032 ↗
7. Premature rupture of the fetal membranes10.1056/NEJM199803053381006 ↗
8. Uniaxial and biaxial mechanical behavior of human amnion10.1557/JMR.2005.0382 ↗
9. Biomechanics of the fetal membrane prior to mechanical failure: review and implications10.1016/j.ejogrb.2009.02.014 ↗
10. The physiology of fetal membrane rupture: insight gained from the determination of physical properties10.1016/j.placenta.2006.01.002 ↗
11. Do we know the strength of the chorioamnion? A critical review and analysis10.1016/j.ejogrb.2009.02.029 ↗
12. Premature rupture of the fetal membranes: is the amnion the major determinant?10.1016/j.ajog.2006.02.010 ↗
13. Contractions, a risk for premature rupture of fetal membranes: a new protocol with cyclic biaxial tension10.1016/j.medengphy.2012.08.014 ↗
14. Characterizing local collagen fiber re-alignment and crimp behavior throughout mechanical testing in a mature mouse supraspinatus tendon model10.1016/j.jbiomech.2012.06.006 ↗
15. Effect of preconditioning and stress relaxation on local collagen fiber re-alignment: inhomogeneous properties of rat supraspinatus tendon10.1115/1.4006340 ↗
16. Minimal preconditioning effects observed for inflation tests of planar tissues10.1115/1.4025105 ↗
17. Effects of strain level and proteoglycan depletion on preconditioning and viscoelastic responses of rat dorsal skin10.1114/1.1349697 ↗
18. Preconditioning is correlated with altered collagen fiber alignment in ligament10.1115/1.4004205 ↗
19. Modeling of anisotropic softening phenomena: application to soft biological tissues10.1016/j.ijplas.2008.06.001 ↗
20. Mechanical behaviour of tendon in vitro10.1007/BF02479137 ↗
21. Computational aspects of the numerical modelling of softening, damage and permanent set in soft biological tissues10.1016/j.compstruc.2013.10.002 ↗
22. Viscoelasticity and preconditioning of rat skin under uniaxial stretch: microstructural constitutive characterization10.1115/1.3049479 ↗
23. Wess · 2008
24. Micromechanical testing of individual collagen fibrils10.1002/mabi.200600063 ↗
25. Stress–strain experiments on individual collagen fibrils10.1529/biophysj.107.124602 ↗
26. Mechanical characterization of collagen fibers and scaffolds for tissue engineering10.1016/S0142-9612(03)00206-0 ↗
27. Dependence of stress–strain nonlinearity of connective tissues on the geometry of collagen fibres10.1016/0021-9290(76)90084-1 ↗
28. A constitutive equation for collagen fibers10.1016/0021-9290(72)90001-2 ↗
29. Viscoelastic behavior of discrete human collagen fibrils10.1016/j.jmbbm.2009.01.005 ↗
30. Viscoelastic properties of isolated collagen fibrils10.1016/j.bpj.2011.04.052 ↗
31. The biomechanics of amnion rupture: an x-ray diffraction study10.1371/journal.pone.0001147 ↗
32. Constitutive equations for fibrous connective tissues10.1016/0021-9290(83)90041-6 ↗
33. Mechanisms of residual stress in soft tissues10.1115/1.3049863 ↗
34. Two-dimensional mechanical properties of rabbit skin-II. Experimental results10.1016/0021-9290(74)90058-X ↗
35. Stress–strain curve and young’s modulus of a collagen molecule10.1016/0021-9290(95)00110-7 ↗
36. On the effect of prestrain and residual stress in thin biological membranes10.1016/j.jmps.2013.04.005 ↗
37. Multiaxial mechanical behavior of human fetal membranes and its relationship to microstructure10.1007/s10237-012-0438-z ↗
38. Time-dependent mechanical behavior of human amnion: macroscopic and microscopic characterization10.1016/j.actbio.2014.09.012 ↗
39. Mechanical and microstructural investigation of the cyclic behavior of human amnion10.1115/1.4030054 ↗
40. Buerzle · 2014
41. On the deformation behavior of human amnion10.1016/j.jbiomech.2013.05.018 ↗
42. Matrix metalloproteinase (MMP)-2 and MMP-9 and their inhibitor, TIMP-1, in human term decidua and fetal membranes: the effect of prostaglandin F(2alpha) and indomethacin10.1093/molehr/7.12.1187 ↗
43. The bulge test: a comparison of the theory and experiment for isotropic and anisotropic films10.1016/0040-6090(81)90407-7 ↗
44. Differential expression of fibulin family proteins in the para-cervical weak zone and other areas of human fetal membranes10.1016/j.placenta.2009.01.007 ↗
45. Collagens—structure, function, and biosynthesis10.1016/j.addr.2003.08.002 ↗
46. Mechanical stability of proteins10.1063/1.3170940 ↗
47. Collagen unfolding accelerates water influx, determining hydration in the interstitial matrix10.1016/j.bpj.2012.10.010 ↗
48. Mussel collagen molecules with silk-like domains as load-bearing elements in distal byssal threads10.1016/j.jsb.2011.05.016 ↗
49. Pressure-dependent changes in the structure of the melittin alpha-helix determined by NMR10.1023/A:1008392327013 ↗
50. New aspects of the alpha-helix to beta-sheet transition in stretched hard alpha-keratin fibers10.1529/biophysj.103.036749 ↗
51. Pressure dependence of human fibrinogen correlated to the conformational alpha-helix to beta-sheet transition: an Fourier transform infrared study microspectroscopic study10.1002/bip.20012 ↗
52. Structural dynamic of a self-assembling peptide d-EAK16 made of only d-amino acids10.1371/journal.pone.0002364 ↗
53. Wasko · 2010
54. Morphology and molecular dynamics of hard α-keratin under pressure by 1H and 13C solid-state NMR10.1016/j.cplett.2011.05.001 ↗
55. Protein unfolding accounts for the unusual mechanical behavior of fibrin networks10.1016/j.actbio.2011.02.026 ↗
56. The alpha-helix to beta-sheet transition in stretched and compressed hydrated fibrin clots10.1016/j.bpj.2012.07.046 ↗
57. Structural proteins from whelk egg capsule with long range elasticity associated with a solid-state phase transition10.1021/bm401598z ↗
58. Thermodynamics of shape memory alloy wire: modeling, experiments, and application10.1007/s00161-006-0022-9 ↗
59. Multi-scale dynamics of twinning in SMA10.1007/s40830-015-0012-5 ↗
60. Deformation mechanisms of human amnion: quantitative studies based on second harmonic generation microscopy10.1016/j.jbiomech.2015.01.045 ↗
61. Uniaxial stress–relaxation and stress–strain responses of human amnion
62. Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis10.1038/sj.emboj.7600318 ↗
63. Structural basis of collagen recognition by integrin α2 β110.1016/S0092-8674(00)80622-4 ↗
64. Assembly of type I collagen fibrils de novo. Between 37 and 41 degrees C the process is limited by micro-unfolding of monomers10.1016/S0021-9258(19)81546-6 ↗
65. Collagen fibril architecture, domain organization, and triple-helical conformation govern its proteolysis10.1073/pnas.0710588105 ↗
66. Spontaneous unwinding of a labile domain in a collagen triple helix10.2140/jomms.2007.2.999 ↗
67. Analysis of the accuracy of the bulge test in determining the mechanical properties of thin films10.1557/JMR.1992.1553 ↗
68. The effect of grain and pore sizes on the mechanical behavior of thin Al films deposited under different conditions10.1016/j.actamat.2014.12.041 ↗