Puncture testing has been applied in several studies for the mechanical characterization of human fetal membrane (FM) tissue, and significant knowledge has been gained from these investigations. When comparing results of mechanical testing (puncture, inflation, and uniaxial tension), we have observed discrepancies in the rupture sequence of FM tissue and significant differences in the deformation behavior. This study was undertaken to clarify these discrepancies. Puncture experiments on FM samples were performed to reproduce previous findings, and numerical simulations were carried out to rationalize particular aspects of membrane failure. The results demonstrate that both rupture sequence and resistance to deformation depend on the samples' fixation. Soft fixation leads to slippage in the clamping, which reduces mechanical loading of the amnion layer and results in chorion rupturing first. Conversely, the stiffer, stronger, and less extensible amnion layer fails first if tight fixation is used. The results provide a novel insight into the interpretation of ex vivo testing as well as in vivo membrane rupture.

References

References
1.
Parry
,
S.
, and
Strauss
,
J.
,
1998
, “
Premature Rupture of the Fetal Membranes
,”
N. Engl. J. Med.
,
338
(
10
), pp.
663
670
.10.1056/NEJM199803053381006
2.
Mercer
,
B.
,
2003
, “
Preterm Premature Rupture of the Membranes
,”
Obstet. Gynecol.
,
101
(
1
), pp.
178
193
.10.1016/S0029-7844(02)02366-9
3.
Malak
,
T. M.
,
Ockleford
,
C. D.
,
Bell
,
S. C.
,
Dalgleish
,
R.
,
Bright
,
N.
, and
Macvicar
,
J.
,
1993
, “
Confocal Immunofluorescence Localization of Collagen Types I, III, IV, V and VI and Their Ultrastructural Organization in Term Human Fetal Membranes
,”
Placenta
,
14
(
4
), pp.
385
406
.10.1016/S0143-4004(05)80460-6
4.
Ilancheran
,
S.
,
Moodley
,
Y.
, and
Manuelpillai
,
U.
,
2009
, “
Human Fetal Membranes: A Source of Stem Cells for Tissue Regeneration and Repair?
,”
Placenta
,
30
(
1
), pp.
2
10
.10.1016/j.placenta.2008.09.009
5.
Schober
,
E. A.
,
Kusy
,
R. P.
, and
Savitz
,
D. A.
,
1994
, “
Resistance of Fetal Membranes to Concentrated Force Applications and Reconciliation of Puncture and Burst Testing
,”
Ann. Biomed. Eng.
,
22
(
5
), pp.
540
548
.10.1007/BF02367090
6.
Moore
,
R. M.
,
Mansour
,
J. M.
,
Redline
,
R. W.
,
Mercer
,
B. M.
, and
Moore
,
J. J.
,
2006
, “
The Physiology of Fetal Membrane Rupture: Insight Gained From the Determination of Physical Properties
,”
Placenta
,
27
(
11
), pp.
1037
1051
.10.1016/j.placenta.2006.01.002
7.
El Khwad
,
M.
,
Stetzer
,
B.
,
Moore
,
R. M.
,
Kumar
,
D.
,
Mercer
,
B.
,
Arikat
,
S.
,
Redline
,
R. W.
,
Mansour
,
J. M.
, and
Moore
,
J. J.
,
2005
, “
Term Human Fetal Membranes Have a Weak Zone Overlying the Lower Uterine Pole and Cervix Before Onset of Labor
,”
Biol. Reprod.
,
72
(
3
), pp.
720
726
.10.1095/biolreprod.104.033647
8.
Arikat
,
S.
,
Novince
,
R. W.
,
Mercer
,
B. M.
,
Kumar
,
D.
,
Fox
,
J. M.
,
Mansour
,
J. M.
, and
Moore
,
J. J.
,
2006
, “
Separation of Amnion From Choriodecidua is an Integral Event to the Rupture of Normal Term Fetal Membranes and Constitutes a Significant Component of the Work Required
,”
Am. J. Obstet. Gynecol.
,
194
(
1
), pp.
211
217
.10.1016/j.ajog.2005.06.083
9.
McGregor
,
J. A.
,
French
,
J. I.
,
Lawellin
,
D.
,
Franco-Buff
,
A.
,
Smith
,
C.
, and
Todd
,
J. K.
,
1987
, “
Bacterial Protease-Induced Reduction of Chorioamniotic Membrane Strength and Elasticity
,”
Obstet. Gynecol.
,
69
(
2
), pp.
167
174
.
10.
Oyen
,
M. L.
,
Cook
,
R.
, and
Calvin
,
S. E.
,
2004
, “
Mechanical Failure of Human Fetal Membrane Tissues
,”
J. Mater. Sci. Mater. Med.
,
15
(
6
), pp.
651
658
.10.1023/B:JMSM.0000030205.62668.90
11.
Oyen
,
M.
,
Calvin
,
S.
, and
Landers
,
D.
,
2006
, “
Premature Rupture of the Fetal Membranes: Is the Amnion the Major Determinant?
,”
Am. J. Obstet. Gynecol.
,
195
(
2
), pp.
510
515
.10.1016/j.ajog.2006.02.010
12.
Pressman
,
E. K.
,
Cavanaugh
,
J. L.
, and
Woods
,
J. R.
,
2002
, “
Physical Properties of the Chorioamnion Throughout Gestation
,”
Am. J. Obstet. Gynecol.
,
187
(
3
), pp.
672
675
.10.1067/mob.2002.125742
13.
Helmig
,
R.
,
Oxlund
,
H.
,
Petersen
,
L. K.
, and
Niels
,
U.
,
1993
, “
Different Biomechanical Properties of Human Fetal Membranes Obtained Before and After Delivery
,”
Eur. J. Obstet. Gynecol. Reprod. Biol.
,
48
(
3
), pp.
183
189
.10.1016/0028-2243(93)90086-R
14.
Artal
,
R.
,
Sokol
,
R. J.
,
Neuman
,
M.
,
Burstein
,
A. H.
, and
Stojkov
,
J.
,
1976
, “
The Mechanical Properties of Prematurely and Non-prematurely Ruptured Membranes
,”
Am. J. Obstet. Gynecol.
,
125
(
5
), pp.
655
659
.
15.
Lavery
,
J.
, and
Miller
,
C.
,
1979
, “
Deformation and Creep in the Human Chorioamniotic Sac
,”
Am. J. Obstet. Gynecol.
,
134
(
4
), pp.
366
375
.
16.
Buerzle
,
W.
,
Haller
,
C.
,
Jabareen
,
M.
,
Egger
,
J.
,
Mallik
,
A.
,
Ochsenbein-Koelble
,
N.
,
Ehrbar
,
M.
, and
Mazza
,
E.
,
2013
, “
Multiaxial Mechanical Behavior of Human Fetal Membranes and Its Relationship to Microstructure
,”
Biomech. Model. Mech.
,
12
(
4
), pp.
747
762
.10.1007/s10237-012-0438-z
17.
Perrini
,
M.
,
Buerzle
,
W.
,
Haller
,
C.
,
Ochsenbein-Koelble
,
N.
,
Deprest
,
J.
,
Zimmermann
,
R.
,
Mazza
,
E.
, and
Ehrbar
,
M.
,
2013
, “
Contractions, a Risk for Premature Rupture of Fetal Membranes: A New Protocol With Cyclic Biaxial Tension
,”
Med. Eng. Phys.
,
35
(
6
), pp.
846
851
.10.1016/j.medengphy.2012.08.014
18.
Buerzle
,
W.
, and
Mazza
,
E.
,
2013
, “
On the Deformation Behavior of Human Amnion
,”
J. Biomech.
,
46
(
11
), pp.
1777
1783
.10.1016/j.jbiomech.2013.05.018
19.
Buerzle
,
W.
,
2014
, “
Mechanical Characterization and Modeling of Human Fetal Membrane Tissue
,” Ph.D. thesis, ETH Zurich, Zurich, Switzerland, Diss. ETH. No. 21784.
20.
Pandey
,
V.
,
Jaremko
,
K.
,
Moore
,
R. M.
,
Mercer
,
B. M.
,
Stetzer
,
B.
,
Kumar
,
D.
,
Fox
,
J. M.
,
Mansour
,
J. M.
, and
Moore
,
J. J.
,
2007
, “
The Force Required to Rupture Fetal Membranes Paradoxically Increases With Acute in vitro Repeated Stretching
,”
Am. J. Obstet. Gynecol.
,
196
(
2
), pp.
165.e1
e7
.10.1016/j.ajog.2006.10.861
21.
Zec
,
M. L.
,
Thistlethwaite
,
P.
,
Frank
,
C. B.
, and
Shrive
,
N. G.
,
2010
, “
Characterization of the Fatigue Behavior of the Medial Collateral Ligament Utilizing Traditional and Novel Mechanical Variables for the Assessment of Damage Accumulation
,”
ASME J. Biomech. Eng.
,
132
(
1
), p.
011001
.10.1115/1.4000108
22.
Strohl
,
A.
,
Kumar
,
D.
,
Novince
,
R.
,
Shaniuk
,
P.
,
Smith
,
J.
,
Bryant
,
K.
,
Moore
,
R. M.
,
Novak
,
J.
,
Stetzer
,
B.
,
Mercer
,
B. M.
,
Mansour
,
J. M.
, and
Moore
,
J. J.
,
2010
, “
Decreased Adherence and Spontaneous Separation of Fetal Membrane Layers—Amnion and Choriodecidua—A Possible Part of the Normal Weakening Process
,”
Placenta
,
31
(
1
), pp.
18
24
.10.1016/j.placenta.2009.10.012
23.
Bourne
,
G.
,
1962
, “
The Foetal Membranes: A Review of the Anatomy of Normal Amnion and Chorion and Some Aspects of Their Function
,”
Postgrad. Med. J.
,
38
(
438
), pp.
193
201
.10.1136/pgmj.38.438.193
24.
Kumar
,
D.
,
Fung
,
W.
,
Moore
,
R. M.
,
Pandey
,
V.
,
Fox
,
J.
,
Stetzer
,
B.
,
Mansour
,
J. M.
,
Mercer
,
B. M.
,
Redline
,
R. W.
, and
Moore
,
J. J.
,
2006
, “
Proinflammatory Cytokines Found in Amniotic Fluid Induce Collagen Remodeling, Apoptosis, and Biophysical Weakening of Cultured Human Fetal Membranes
,”
Biol. Reprod.
,
74
(
1
), pp.
29
34
.10.1095/biolreprod.105.045328
25.
Kumar
,
D.
,
Schatz
,
F.
,
Moore
,
R. M.
,
Mercer
,
B. M.
,
Rangaswamy
,
N.
,
Mansour
,
J. M.
,
Lockwood
,
C. J.
, and
Moore
,
J. J.
,
2011
, “
The Effects of Thrombin and Cytokines Upon the Biomechanics and Remodeling of Isolated Amnion Membrane, in vitro
,”
Placenta
,
32
(
3
), pp.
206
213
.10.1016/j.placenta.2011.01.006
26.
Badir
,
S.
,
Mazza
,
E.
,
Zimmermann
,
R.
, and
Bajka
,
M.
,
2013
, “
Cervical Softening Occurs Early in Pregnancy: Characterization of Cervical Stiffness in 100 Healthy Women Using the Aspiration Technique
,”
Prenatal Diagn.
,
33
(
8
), pp.
737
741
.10.1002/pd.4116
27.
Malak
,
T. M.
, and
Bell
,
S. C.
,
1994
, “
Structural Characteristics of Term Human Fetal Membranes: A Novel Zone of Extreme Morphological Alteration Within the Rupture Site
,”
Brit. J. Obstet. Gynaecol.
,
101
(
5
), pp.
375
386
.10.1111/j.1471-0528.1994.tb11908.x
28.
McLaren
,
J.
,
Malak
,
T. M.
, and
Bell
,
S. C.
,
1999
, “
Structural Characteristics of Term Human Fetal Membranes Prior to Labour: Identification of an Area of Altered Morphology Overlying the Cervix
,”
Hum. Reprod.
,
14
(
1
), pp.
237
241
.10.1093/humrep/14.1.237
29.
Mauri
,
A.
,
Perrini
,
M.
,
Mateos
,
J.
,
Maake
,
C.
,
Ochsenbein-Koelble
,
N.
,
Zimmermann
,
R.
,
Ehrbar
,
M.
, and
Mazza
,
E.
,
2013
, “
Second Harmonic Generation Microscopy of Foetal Membranes Under Deformation: Normal and Altered Morphology
,”
Placenta
,
34
(
11
), pp.
1020
1026
.10.1016/j.placenta.2013.09.002
30.
Moore
,
R. M.
,
Schatz
,
F.
,
Kumar
,
D.
,
Mercer
,
B. M.
,
Abdelrahim
,
A.
,
Rangaswamy
,
N.
,
Bartel
,
C.
,
Mansour
,
J. M.
,
Lockwood
,
C. J.
, and
Moore
,
J. J.
,
2010
, “
Alpha-Lipoic Acid Inhibits Thrombin-Induced Fetal Membrane Weakening in vitro
,”
Placenta
,
31
(
10
), pp.
886
892
.10.1016/j.placenta.2010.07.012
You do not currently have access to this content.