Biorheology 30, 191-205, 1993

0006-355X/93 $6.00 + .00 Printed in the USA.

Copyright © 1993 Pergamon Press Ltd. All rights reserved.

STRUCTURE AND RHEOLOGY OF GELATIN AND

COLLAGEN GELS

MADELEINE DJABOUROVt, JEAN-PIERRE LECHAIREt AND

FRANCOISE GAILLt

t Ecole de Physique et Chimie, CNRS URA 857, 10 Rue Vauquelin, F-75231

Paris Cedex 5, FRANCE (Author to whom correspondence should be
addressed)
t Centre de Biologie Cellulaire, CNRS LP 3101, 67 Rue Maurice Gunsburg,
F-94205 Ivry Cedex, FRANCE

ABSTRACT This paper undertakes a parallel analysis of the gelation

mechanisms, structure and rheological properties of gelatin and collagen gels.
Although the molecular compositions of collagen and gelatin are almost
identical, gelation proceeds from distinct mechanisms and leads to different
types of molecular assemblies. First are presented the properties of the
solutions, based on their structural and rheological characterization; then the
mechanisms of gelation in the networks, observed by Transmission Electron
Microscopy, of three types of gels: gelatin gels, Type I collagen gels and gels
made of cuticle collagen extracted from annelid worms. The rheological
investigation of the sol-gel transition of gelatin is described within the context
of the theories of percolation and scaling laws. Different experimental
approaches to the kinetics of gelation are presented, combining dynamic light
scattering and rheology in respect to gelatin gels.

Introduction
Gelatin and collagen gels are usually compared and often confounded by non-
specialists. This comparison is justified because originally gelatin and collagen
are the same macromolecule, the same protein. In this paper, we shall make a
systematic parallel between the two types of solutions and gels and analyze
three different aspects: the mechanisms of gelation, the structure of the
networks and the rheological properties of the gels. We examine two classes of
collagen solutions: Type I collagen from vertebrates and from cuticle of deep
sea worms. Particular emphasis is put on the sol-gel transition, with the help
of different experimental approaches, combining, for gelatin gels, rheology and
transport phenomena through the gel network. The process of gelation is
analyzed in the context of the modern theories of percolation. Finally, the
influence of mechanical actions on the kinetics of gelation is briefly evoked.

KEY WORDS: Collagen; gelatin; gels; rheology; electron microscopy

191
192 Collagen and gelatin gels Vol. 30, Nos. 3 & 4

Fig. 1. Structure of Type I collagen fibers: A) bundles of fibrils;

B) the structure of a single fibril; C) the collagen rod (the triple-
helix); D) the conformation of an individual strand (the feft-
handed helix) and it'> composition.

The Mechanisms oj Gelation

In order to understand the properties of the collagen and gelatin solutions,
one has to recall first the native state of collagen and and its relation to gelatin.
Collagen is the major protein component of the extracellular matrix of
animals. Collagen is assembled into a complex fibrillar organization which is
schematically shown in Fig. 1 at different levels of magnification for Type I
collagen. The fibrils are assembled into bundles that form the fibers. The
fibrils are made of 5 micro fibrils placed in a staggered arrangement with a
displacement of 64 nm from one row to the adjacent one and a gap of 35 nm
between successive molecules in a row, which gives the typical striated aspect to
the negatively stained electron micrographs. Each microfibril is a collection of
collagen rods with lengths of 300 nm. Each collagen rod is a right-handed
triple-helix, each strand being itself a left-handed helix. The triple-helix is
stabilized by hydrogen intramolecular bonds. In addition, collagen fibrils are
strengthened by covalent intra and intermolecular cross-links which make the
tissues of mature animals insoluble. When suitable treatments are used,
collagen rods can be extracted and solubilized in acidic solutions, where they
keep their original conformation as triple-helices. When collagen solutions are
 Vol. 30, Nos. 3 &: 4 Collagen and gelatin gels 193

extensively heated, or when the native tissues are subjected to chemical and
thermal treatments, the hydrogen and covalent bonds that stabilize the collagen
helices are broken and the molecules adopt a disordered conformation. This
material is gelatin and is soluble in water at 40-45° C.

Collagen and Gelatin Solutions

In solutions, the individual macromolecules of collagen and gelatin are, as
much as possible, unaggregated. The conditions of stabilit.y of collagen and
gelatin aqueous solutions are summarized in Table 1.

Table 1

Solution Collagen Solution Gelatin Solution

Properties (Type I, calf skin) (origin: bone, skin ... )
Temperature T= 4° C T = 45° C
Isoelectric point pI = 9 pI = 4.6 (basic extract)
pI = 9 (acid extract.)
pH acid (pH = 4) variable, with pH oF- pI
Ionic strength 1=0.005 variable
if pH "" pI, then I = 0.1
Molecular weight 300000g/mole major component
100000 g/mole,
polydisperse
Conformation semi-flexible rod random coil
(worm-like chain)
Minimum concent.
to make a gel "" 1.5 mg/ml "" 10 mg/ml

Dilute solutions of collagen and gelatin are stable in different environments,

collagen solubilization being achieved in more sharply defined conditions.
Collagen solutions
Weak ionic strength and acidic pHs are necessary, together with a low
temperature, to disperse the collagen molecules. The conformation of Type I
collagen in dilute solutions has been investigated by dynamic light scattering
(DLS) (Silver and Birk, 1984) and intrinsic viscosity measurements (Nestler et
at., 1983). From rheological investigations, these molecules behave in solution
like semi-flexible rods with a persistence length of 170 nm. The rigid rod
model is in agreement with the DLS results (Silver and Birk, 1984) for rod
lengths of 250 nm. By transmission electron microscopy (TEM), single
collagen molecules can be observed sprayed on a freshly cleaved mica at 4° C
and shadowed with Pt and C. The Type I molecules appear as rods with a
constant curvature or rods with a single bend, with average end-to-end
distances of the order of 220 nm, significantly shorter than their contour
lengths ("" 300 nm). TEM results agree with DLS if one assumes that the rods
have a single bend with an angle less than 90°.
Among the different types of collagen that have been identified, the cuticle
collagen of marine worms contains the longest rods. This collagen is extracted
from tlle cuticle of the worms, who live in extreme conditions, at high pressure
194 Collagen and gelatin gels Vol. 30, Nos. 3 &: 4

Fig. 2. An electron micrograph of a cuticle collagen molecule of

deep sea worms as seen in a rotary-shadowed preparation. The
contour length of the molecule is around 2.4 )lm. G: x60,000 or
1 cm = 166 nm.

(260 atm) and high temperatures (350° C) near hydrothermal vents. The
cuticle collagen is a giant flexible molecule whose length reaches 2.4 )lm in the
so-called Pompeii worms (Gaill and Hunt, 1991) (see Fig. 2) and 1.5 )lm in
the so-called tube worms (Gaill et al., 1991). In the native state, these
molecules do not form striated fibrils. Microfibrils are arranged in a liquid
crystalline-like structure. The fibrils are organized in a plywood structure
exhibiting a long range orientational order (Gaill, 1990).
The thermal denaturation of collagen individual rods is around 37° C for
the Type I collagen and 40° C for cuticle collagen from annelid worms, due to
a higher content of hydroxyproline (170 residues per mil) (Gaill et al., 1991).
Gelatin solutions
Gelatin solutions can be prepared at variable pHs and ionic strengths. The
important requirements are for the temperature to be above 30° C and for the
pH to be different from the isoelectric point, in order to screen the
interactions between charged groups. This can be achieved by either
modifying the pH or by adding salts to the solution. Gelatin solutions have
been investigated by dynamic light scattering (Heming et al., 1991), static LS
and small angle neutron scattering (SANS) (Pezron et al., 1991) at 45° C. The
individual gelatin coils are semi-flexible coils or worm-like chains with a radius
of gyration of the order of 300 nm and a persistence length of the order of
2 nm. In semi-dilute solutions (c ;?: 1 %), the coils overlap and interpenetrate
each other. The characteristic structural length in solution is then the mesh-
Vol. 30, Nos. 3 & 4 Collagen and gelatin gels 195

size or the correlation length between different chains. The mesh size
decreases with greater concentration, varying between 7 to 3.5 nm when the
concentration increases from 1 to 5%, for instance. The scattering spectra of
a
A

-
E
c lag phase growth plateau

-
,..
o:t
C')

Q)
u
c
co
....
.0
oen
.0
«

o 30 60 time (min)

b
A (314 nm)
Reference
T=25 °C
1=0.23
1 _ _ " c=0.05
H=7.1
/' .......---'~--.,;...;;..;;...--I

ITi (=37°C)1 / / IpHi (=7.5>1

/
/
0.5 /
/
/
/
b
o
o 30 60 time (min)
l'1g. 3. Kinetics of aggregation of Type I collagen molecules: 3a)
the increase of absorbance reveals the different stages of the
process. During the lag phase the primary aggregates are formed,
the growth step corresponds to the lateral association of the sub-
units and the plateau indicates the end of the process. 3b) The
effect of various parameters (pH, temperature, ionic strength and
concentration), on the kinetics of aggregation is shown.
 196 Collagen and gelatin gels Vol. 30, Nos. 3 Be 4

gelatin solutions follow the scaling laws established for synthetic linear
polymers in solution in good solvents (De Gennes, 1985).

Gel Formation
Gelation of collagen or gelatin solutions is achieved by modifying the
thermodynamic conditions. Collagen gelation deals with the process of
aggregation and fibril formation in vitro, which is induced by changes of ionic
strength, pH and temperature. Numerous studies have been devoted to the
mechanisms of fibril formation, aimed at elucidating the process of
fibrillogenesis in the extracellular matrices, especially in its early stages.
Aggregation of collagen molecules in solution can be monitored by changes in
turbidity. Typical plots of the kinetics aggregation of Type I collagen are
shown (Herbage et al., 1990) in Figs. 3a and 3b. The increase in absorbance
(at A = 314 nm) proceeds in three distinct steps: a) a lag phase, during which
no modifications in absorbance can be detected and the primary aggregates,
dimers and trimers of collagen molecules, are nucleated;
b) microfibrillar aggregation starts with the lateral aggregation of sub-units;
c) finally, an equilibrium is reached that corresponds to a maximum plateau of
absorbance. Its amplitude is related to the size of the largest fibrils. The effect
of various parameters, such as pH, temperature, concentration, and ionic
strength on the kinetics of gelation, is schematically shown in Fig. 3b. The
enthalpy change accompanying the self-assembling process of collagen is
positive, ranging between 50 and 120 kcal/mole of collagen (Na et al., 1989)
when the gelation temperature is raised from 20 to 28° C. The enthalpy change
is driven by the breaking of hydrogen bonds within the shell of water molecules
surrounding the collagen rods. This process requires a net positive change in
entropy which accompanies the loss of order of the water molecules in the
shell. The same conditions are required for gelation of the cuticle collagen of
annelid worms, although no systematic investigation of these parameters has
been done so far.
Gelation of gelatin solutions results from a temperature variation, i.e.,
cooling solutions below 30° C, provided that they are concentrated enough to
be in the semi-dilute range. The basic mechanism of gelation is related to the
reverse coil-to-helix transition during which the helices that are created are
similar to the collagen triple-helix. The best method to monitor the coil-helix
transition in gelatin solutions is the measurements of the optical rotation which
can be directly converted into the helix amount of the gelatin strands, X, or the
fraction of residues in the left-handed conformation (Djabourov et al., 1988a).
Such measurements are shown in Figs. 4a and 4b. First, the increase of the
helix amount vs. time in a linear scale is plotted in Fig. 4a over periods of more
than 100 hours. Contrary to the collagen gelation, no lag phase is observed.
The temperature affects the kinetics in the opposite way: the lower the
temperature, the higher the rate of helix formation. In Fig. 4b, the kinetics are
plotted on a logarithmic time scale. One can see, then, that the helix amount
does not reach a constant value; thus, no equilibrium is reached. After a rapid
increase, the subsequent growth of the helices proceeds with a logarithmic time
dependence over periods of hundreds or thousands of hours! Thus, gelatin
gels are not in equilibrium.
As it appears in the temperature dependence of tl1e kinetics, the gelatin
gelation has an enthalpy change that is negative. The process of triple-helix
formation is analogous to a crystallization transition, with a nucleation step that
is favored when the transition takes place far below the equilibrium melting
temperature, in the so-called supercooled state for a pure liquid or a polymer
Vol. 30, Nos. 3 & 4 Collagen and gelatin gels 197
a
x

0.8

0.6 a

b
0.4

o ~ _____ __
~ ~ __ ___
~ ~~ __ ~ __ ~ __ ~ __ ~ ____ ~ __ ~~

o 20 40 60 80 100
tlme(hours)
b

,r-------~--------~--------~--------~------_.
x

.8

.6

.4

.2

1 10 10 2 10 3
tlme(hours)
Fig. 4. Kinetics of gelation of gelatin gels: 4a) The increase of the
optical rotation of the solutions can be related to the amount of
helices created, X. Time is given in a linear scale up to 120 hrs.
The different curves correspond to the following temperatures: a)
T = 10° C; b) T = 20° C; c) T = 26° C; d) T = 28° C. 4b) The
same data plotted vs. time in a logarithmic scale. The helix
amount increases slowly with time; no limit appears after 1000
hrs. The continuous and the dotted lines correspond to the
phenomenological analysis proposed by Djabourov et al. (1988a).
 198 CoUagen and gelatin gels Vol. 30, Nos. 3 Be 4

in melt (see. for instance, Wunderlich, 1976). The crystallization transition,

however, in this case is limited to the one-dimensional growth of triple-helices,
without lateral aggregation, as supported by X-ray diffraction experiments on
oriented gels (Pezron et al., 1990).
For both COllagen and gelatin solutions, the process of gelation is reversible
(solutions recover their fluidity) with temperature, the collagen gels "melt" by
lowering the temperature (Na, 1989) (the fibrils disassemble), while the gelatin
gels "melt" (the reverse transition, helix-ta-coil takes place) by raising the
temperature. In both cases, an hysteresis is observed (Na, 1989; Djabourov et
al., 1988a).
Morphology of the Gel Networks
For collagen and gelatin gels, the structure of the network is complex.

Collagen Gels
Replicas of Type I collagen gels are shown in Fig. 5. The replicas were
obtained by a quick freezing, deep etching and rotary replication method
(Favard et al., 1989) and observed by TEM. The gel was formed in vitro from a
solution with 5 mg/ml concentration. Gelation was obtained by exposure'to
concentrated ammonia vapors (Bouligand et al., 1985). The micrograph
shows a network that contains two types of fibrils: the staggered arrangements
of collagen fibrils with a periodicity comparable to the stained micrographs
and with various diameters of the order of 50 to 500 nm. The fibrils are easily
recognized at the unscraped surface of the quickly frozen gels, as shown in Fig.
5a. These fibrils coexist with randomly oriented microfilaments which might
either be individual rods or aggregates of a small number of rods. An enlarged
detail from the network for the frozen sample, whose surface was scraped
before etching and shadowing, is shown in Fig. 5b.
A gel prepared from cuticle collagen of annelid worms is shown in Fig. 6.
The supramolecular structure has a more disordered aspect, with a mesh size
larger than in the previous example. Periodic arrangements and large
aggregates of collagen rods do not appear in this network.

Gelatin Gels
The gelatin gel network prepared by the same technique is shown in Fig. 7 for
a gel with a concentration of 2%. It is a fine and dense entangled network,
where the thin filaments are the triple-helices covered by the Pt-C coating.
Image analysis allows us to derive the total amount of triple-helices per unit
volume of the solution. The order of magnitude is 1500 Jlm/ Jlm 3 for a 2%
concentration. Besides the triple helical structure apparent on the
micrographs, it is known that a substantial fraction of the strands subsists in the
coil conformation (about 50%), but cannot be made visible on the
micrographs. because the thickness of the strands is below the resolution of the
TEM technique (about 1 nm).
Rheology of the Sol-Gel Transition
The sol-gel transition has been the subject of numerous studies during the last
decade that have been stimulated by modern ideas based on the analogy
between gelation and percolation, first proposed by P.-G. De Gennes and D.
Stauffer (see De Gennes, 1985, for instance). Interpretation of the gelation
processes of model systems (essentially covalent networks created through a
polymerization reaction) have been supported by theoretical studies and
accompanied by numerical simulations. Other experimental studies dealt with
Vol. 30, Nos. 3 & 4 Collagen and gelatin gels 199
a

Fig. 5. Type I collagen gels. a) Electron micrograph of the

unscraped surface of a gel prepared by a quick freezing, deep
etching and rotary replication technique. The gel is prepared in
vitro at a concentration of 5 mg/ml. The typical striations of the
fibrillar aggregation are put in evidence. G: x43,OOO or
1 cm = 230 nm. b) After scraping the surface of the gel, the fine
network of collagen molecules (microfibrils) randomly dispersed
becomes apparent. G: x128,OOO. 1 cm = 80 nm.
200 Collagen and gelatin gels Vol. 30, Nos. 3 & 4

Fig. 6. Cuticle collagen gel from annelid deep sea worms. A

loose and disordered network is seen. Large, striated fibrils do
not form. Concentration 2.5 mg/m!. G: x128,000 or 1 cm = 80
nm.

a great variety of polymeric or colloidal systems and established that, despite

the complexity of the gelation process, the variation of the viscoelastic
parameters in the near vicinity of the gel point could follow the same type of
scaling laws (Djabourov, 1991). These properties were illustrated in the case
of gelatin gels by a combination of two different techniques (Djabourov et at.,
1988b): on one hand, the number of triple-helices created during the kinetics
of gelation was measured at different temperatures; on the other, the
viscoelastic parameters (especially G', the elastic shear modulus) were
determined rigorously in the same conditions with special care not to disturb
the kinetics (small amplitudes of shearing, < 10%). The triple-helices play the
role of junctions in the network. Then, the elastic modulus and the helix
amount could be related at any moment during the kinetics at constant
temperature. Fig. 8 shows that the increase of the clastic G' modulus with the
helix amount X is composed distinctly of two parts: below a threshold, which
is around Xc = 7%, (concentration c = 4.7 %), the solution is a fluid with no
measurable elastic modulus. This is the sol state. Above the threshold, a
sharp increase of the elastic modulus is observed and the solution has become
a gel with a measurable elastic modulus. This type of behavior was predicted
by the percolation theories; the dependence of the ela')tic modulus G' with the
helix amount (X - Xc) can be described by a power law with a critical
ex?onent of 1.9: G' - (X-Xc) 1.9.
These general ideas should be relevant to modeling the gel properties of
the collagen systems, as has been suggested recently by Forgacs et at. (1991).
The collagen gel could be assimilated to a collection of rigid filaments with
 Vol. 30, Nos. 3 & 4 Collagen and gelatin gels 201

Fig. 7. Electron micrograph of a gelatin gel network. The

network is dense and disordered. The filaments are the portions
of triple-helices, shadowed by evaporation of Pt-C.
Concentration 2%. G: x75,000. 1 cm = 130 nm.

random orientations. The dependence of the elastic modulus with the protein
concentration should then be investigated (Sinclair et aI., 1983). There is,
however, a serious limitation to the description appearing on the micrographs:
for the Type I collagen gel, the structure obviously contains both randomly
oriented rods and large fibrils. The modulus of such a binary network is more
complex to analyze. Gels of the cuticle collagen of annelid worms had a more
uniform distribution of fibrils, so an investigation of the concentration
dependence of their elastic moduli should be relevant to this type of
interpretation.
With the sol-gel transition of gelatin, besides rheology, another experiment can
be used to follow the kinetics precisely without disturbing the process. This is
DLS in solutions cont.aining latex spheres (of a diameter <I> = 100 nm) that act
as markers. The mean square displacement. of the latex spheres, <r2>, t.hrough
the solution at different moments in the course of gelation, was followed. This
is summarized in Fig. 9. As long as the solution is f1uid (sol state), the latex
spheres diffuse, undertaking brownian movements (the mean square
displacement increases linearly with the correlation time, 't), the long time
diffusion coefficients (slope of <r2> vs. 't, in the limit of large 't values) being
related to the macroscopic viscosity of the solution . As soon as a gel is formed,
with a network mesh size of the order of the diameter of the latex spheres, the
local diffusion coefficients (slope of <r2> vs. 't, in the limit of small 't) begin to
increase. This effect is due to an elastic coupling between the spheres and the
network. No diffusion at long distances is observed. The movements of the
particles are confined, as shown in Fig. 9, anc! the mean square displacements
202 Collagen and gelatin gels Vol. 30, Nos. 3 & 4

•o
o
C

• T=24°C
5 oT=25°C
o aT= 26°C
• T= 26'5°C
4 • T= 27°C
• T-27·5°C
o
• T. 280C

gel point
!a-:~
O'------~~~~~------~------~----~
X (0/0)

o 5 10 15 20

Fig. 8. The gelatin sol-gel transition. The elastic shear modulus

is plotted vs. the h elix amount for different temperat.ures of
gelation. The "gel point" corresponds to a helix amount
Xc"" 7%. Concentration 4.7%.

do not exceed a distance comparable to the diameters of the spheres

«r2>/$2 - 1). This type of approach can be applied to other gelation
processes, provided the gels are transparent.
Finally, it may be of interest to follow the influence of mechanical actions
over the processes of gelation. For the so-called physical gels, where no
permanent cross-links are formed between macromolecules, the influence of
shearing may play a crucial role in favoring or retarding gelation. Such an
experiment is shown in Fig. 10 for gelatin solutions that have been submitted to
continuous shearing during their gelation. When a constant stress is applied, it
clearly delays the formation of the gel and may even prevent gelation within 24
hours for a system which usually gels in 15 minutes! This experiment clearly
illustrates the fragility of physical, non-permanent gel networks submitted to
mechanical treatments. Collagen gels are likely also to be sensitive to such
actions.
 Vol. 30, Nos. 3 & 4 Collagen and gelatin gels 203

2,5
< r2> (10- 2 ~m2)

_e_ 6 min.
1,5 {
sol -0- 24 min.

gel { -.- 75 min.

-0- 24 hours

I I I I I I t (IlS)
8000 10000 12000 14000 16000 18000
Fig. 9. Mean square displacement of latex spheres during gelatin
gel formation. The first two measurements are in the sol state,
when the spheres undertake a brownian motion, the last two
measurements are in the gel state when the particles are trapped.
Concentration 4.7%. Temperature of gelation T = 26° C.

50 l I
I viscosity (Pa s) I i
I
I I
I
I
I
I
a b(!
,
c I
I
J
I
!
i
,i I
i I
!

j I
,I
,I
i
I
I
I
I

I
/
I
/
I
,I
.'

~ /
O~---- __----~----~=--- ----~-
- ____ ----~----__----~----____----T-----~

o time (s) 3600

Fig. 10. Effects of shearing on gelation. Gelatin solutions were

cooled to 26° C (concentration 10%) and submitted to a
continuous shearing under different stresses: a) a = 2 N/m2;
b) (J = 5N/m 2 c) (J = 10 N/m2. The increase of the apparent
viscosity vs. time is shown.
204 Collagen and gelatin gels Vol. 30, Nos. 3 & 4

Conclusion
This paper aims to clarify the differences between collagen and gelatin gels.
The modern ideas on gelation and percolation are used to describe the sol-gel
transition of gelatin solutions and many other complex systems. These theories
can predict the changes of the rheological properties of collagen solutions
under suitable conditions for gelation, in relation to their structure and
composition. More experimental work is expected in this area.

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This paper was delivered at the 8th Congress of Biorheology, Yokohama, 1992, at the
Symposium on the Rheology of Biopolymer GeL5.