BIORHEOLOGY, 24; 385-399, 1987

0006-355X/87 $3.00 + .00 Printed in the USA.

Copyright (c) 1987 Pergamon Journals Ltd. All rights reserved.

RHEOLOGY OF SYNOVIAL FLUID

J. Schurz and V. Ribitsch

Institut fUr Physikalische Chemie
Karl-Franzens-Universitlt Graz
Austria
(Received 17.11.1986; Accepted in revised form 5.5.1987
by Editor D. Liepsch)

ABSTRACT After a discussion of the role of synovial fluid as a

joint lubricant, rheological measurements are
described with both normal (healthy) synovial fluids
and pathological ones. Shear stress and first normal
stress difference are measured as a function of shear
gradient to calculate the apparent shear viscosity ~I
and the apparent normal viscosity ~1 as well as an
apparent Shear modulus G'. It is found, that in case
ot diseased synoviae all rheological parameters
deteriorate. Most significant changes are observed
wlth the zero shear viscosity ~o , the shear modulus
G', and a characteristic time e' which is the
reciprocal of the critical shear rate Dc which
determlnes the onset of shear thinning. The
rheological deterioration of synovial fluids is
explained in terms of solute structure. whereby a
molecular rmass of the backbone hyaluronlc acid of at
least lUi g.mol- l lS required for satisfactory
function. A theory of the rheological performance of
normal synovial fluid as well as its pathological
deterioration is proposed.

KEY WORDS: synovial fluid, rheumatic joint diseases,

viscosity curves, viscoelasticity, shear modulus,
hyaluronlc acid.

Dedicated to Prof. Dr. h.c. multo Otto Kratky on the occasion

of his 85th birthday

385
386 SYNOVIAL FLUID Vol. 24, No.4

Synovial Bone
fluid

Synovial
membrane
Articular (= Synovium )
cartilage

FIG. 1

Synovial joint

non - covalent bonds

protein core

hyaluronic acid backbone

FIG. 2

Complex hyaluronic acid/proteoglycan

Vol. 24, No.4 SYNOVIAL FLUID 387

Synovial fluid lS produced by the synovial membrane

(synovium) and forms an interface with both the synovium and
the articular cartilage (Fig. 1). Its function are nutrition of
cartilage, lubrication, load bearing and shock absorption. It
can be regarded as a dialysate of blood in which a high
molecular mass complex of hyaluronic acid (as backbone) and
protein branches is dissolved, producing a highly viscous and
viscoelastic f.luid (1). The hyaluronic acid congentration is
about 2-3.l0- j g/ml, its molecular m?ss about 10 7 g.mol- 1 ; the
protein concentration is 10-30.10- j g/ml. Presumably, the
dissolved complex has the structure shown ln Fig. 2 (2). In
joint diseases the composition of the synovial fluid is changed
in such a way that lts rheologlcal properties are deteriorated,
so it can no more meet the requirements of lubrication, load
bearlng, and shock absorption. Among other variations we find
an increase in protein concentration and a decrease in
concentration and molecular mass of hyaluronic acid. In case of
effusion the amount of synovia is enhanced, which brings about
a notable dilution.
Normal synovial fluld has a high viscosity, very pronounced
shear thinning and fluid elasticity. In the usual concentration
range (0,5-1.10- 3 glml hyaluronlc acid) it forms a typical
entanglement solution. In diseased synovia we find a
degeneration of all rheological properties and a reduction of
the hyaluronlc acid molecular mass to ~ lOti g.mol- l . The
mechanism of this detoriation is not yet clear (3). The
molecular degradation is essential, the reason for it unclear.
At present the role of autooxidants and peroxides is discussed
(4) (e.g. depolymerization by ascorblc acid in vitro, catalyzed
by eu and Fe ions, inhibited by catalase). Degradation by
radicals and enzymes is also considered. Further, a change of
conformation is also discussed, as suggested by a notable
decrease in intrinsic viscosity and radius of gyration of
hyaluronic acid (3).
Since the structure of the synovia complex is not exactly
known, and since we are dealing with a highly viscous, gel like
solution of the network type, we must rely on a
phenomenological analysis of the rheology of both normal and
pathologlcal synovial fluids.

We investigated synovlal fluids from knee joints, both

normal and pathological. More than 200 cases were studied (5).
The synovia was obtained by sterile puncture. Healthy joints
yielded about 1-4 ml. For the study of healthy synovia, we used
post mortem samples. No change in the rheological properties
could be found during 12 hours (but often great difference were
detected between right and left joints, especially with older
persons). The synovial fluids were centrifuged for 60 min with
12000 g and examined within the same day. All measurements were
carried out at 25°C.
Rheological measurements were performed in a Contraves Low
388 SYNOVIAL FLUID Vol. 24, No.4

170 17 0
I::"
CI
I::" j
CI
o o

log 0 log 0

General Type Carreau Type

FIG. 3

Viscosity curves, schematical

o 5105
Cl 5113
6. 5120
T'2 open
0', full

10- 1 100 10 1
-----+. 0 [5- 1J

FIG. 4

Shear stress <12 and first normal stress

di f ference 0, of normal synovial fluids
Vol. 24, No.4 SYNOVIAL FLUID 389

Snear ro~a~lona~ vIscome~er (LS lu0, LS 21 In the shear rate

range lu- j luI s-l and In a Eheom~trics Mechanical
Spectrometer RMX J~uu in ~ne range luI - Iu j s-l. We measured

.1'
the shear stress ~1~' and the rIrst normal stress dIfference

the
~ractIcallY, we
formula of
used the wall Shear rate D calculated by
WeIssenberg-habInowltsch (6). For further
evaluatIon, we calculated the rollowing fIgures:

Apparent shear V1SCOSlty

, wIth zero shear limit
"1 :::.
"1 =liM"1'
o J)...,O
Apparent normal VISCOSI ty '\(" = wIth zero shear limit
'Y", 0 =: 2i VV\ 1""
J) ~o

From the normal stress dIfference we calculated an apparent

steady shear flOW compllance

resp. an apparent shear modulus (7) (from Hooke~ law in shear,

using the recoverable shear concept)

6'= = S: recoverable shear

s
Both figures are apparent, that is they depend on shear rate.
They are connected by G' = 1/2Je.
In this paper, we use preferably G'. The zero shear limit
of G' (G u ) can be obtalned by overshoot measurements or as
'VI. 2-
bl) =. ---+'-
'"'1'1,0

g§.n§.,r~l_,r§.m~,r!S§.
The empIrical interpretation of our results starts out from
viscosity curves, that is log ~I vs. log D plots, as
schematlcally shown in Fig. 3. Since the exact molecular mass
and nature of the flow unit is not known, we need empirical
relatlons. As a measure for the mass of the flow unit we may
use the zero shear viscosity ~o , the shear rate at the onset
of shear thinning Dc' and the_shear rate at the inflection
point of the viscosity curve D ( ~~ values have not been
obtained in our measurements). These figures have been shown to
be related to the molecular mass of the flow units by the
followIng empirical formulae:

The figure Dc can also be regarded as the Inverse of a time

constant e' = l/Dc' which is characteristic for the flow unit
mass and is related to land probably similar in size) to the
largest relaxation time 9 1 Further, we may distinguish two
types of flow curves: the general type with pronounced
curvature, which is found with technical solutions (high
390 SYNOVIAL FLUID Vol. 24, No.4

o 5120
102 '" 5 118 10 2
<) 5113
o 5105
';f
~

10' 10' a..III

~

0-

,,' r
N

~
10°

r 10-'

10-2
V 5 104
v S 98
Cl S 92
0 S 91
10-'

10-2

100 10'
- - - - . . 0 [5-' J

FIG. 5

Shear stress '12 and first normal stress

difference (11 of normal synovial fluids

10° ';;;'
'"
o 5105 10- 1
~
",-
Cl 5113
" 5120
ry': open
11): full

10-1 10° 10 '

- - - -•• 0 [5- IJ

FIG. 6

Shear viscosity ry' and normal viscosity ~,

of normal synovial fluids
Vol. 24, No.4 SYNOV IAL FLU ID 391

pOlymolecular1ty, high solut1on 1nhomogene1ty), ana the

Carreau-type, in which the zero shear viscosity is followed by
a power law range w1th exponent n-1 (if ~.~ prop. Dn ). The
latter type 1S found with homogeneous solutions of rather
monodisperse particles. The solution elastlcity is represented
as log 't.., vs. log lJ resp. log G' vs. log D plots.
Accordlng to our estimation, in normal motion a knee joint
experlences a shear rate of 10 0 - 10~ s-1. As it will be shown
later, ln this range we find a plateau ln G' and shear thinning
accordlng to a power law.

~QKm£l_~b§£ltbY~_~YnQY~£
iiig. 4 and tJ show plots
of both shear stress "'1:'"z.. and first
normal stress difference 1G vs. D (log-log plots). Fig. 6
shows plots of log '"'1' resp, log "f" vs. log D, and Fig. 7
plots of log ~' resp. log G' vs. log D. In all figures, several
representatlve samples have been selected. From these plots, we
observe the following features:

• The cross1ng of the -c~z. and 6., curves occurs at

D ~ 10- 1 - 10- 2 s-l. Dc lies in the ~£m~ range of D .
• Viscosity curves are of the Carre au - type .
• ~,the power law exponent is the same for -c •• (n = 0,30
0,33) and e(... (2n = 0,59 0,65). G' .has a
characteristic plateau in the range 10° < D < 10 J (with
G' = 1-4 Pa).

The typical parameters are:

"10 = 1 - 40 Pas".,e l = 1 / Dc = 4U - 100 s, G'plateau =

1-4 Pa (MHy = 10 1 g.mol- l from Ilght scattering after
isolation)

The plateau-range for G' follows from the constant power law
exponent for both ~I and ~1
"t.!".. \(2. .
G' = ~"
= ----.:0
V\
wi th ~" .. = k. lJn and ~1 = k'. D~n
e' is in the range we would expect for the longest relaxation
time. A normalization of the viscosity curves (production of
a master curve) is possible by plotting log 'Y)'/'rJo vs. log D."1o.
It would be of interest to obtain GO the shear modulus at
rest. It could be obtained either by di~ect measurements from
overshoot (8), or from both zero shear Viscosity ~O and zero
shear normal viscosity 't'1 0 according to GO= '1oz.../~ o'
While '10 is readily available from our measurements, the
.~ 1 0 data do not extend to low enough values to make an
extrapolation to D -7 0 possible. However" a rough est~mation
shows that ,\(",,0 should lie in the range 10~ - 10 4 Pa. s-~. Then
we calculate Go between 1,2 and 0,02 Pa. This compares quite
well wlth the figure Altmann (9) obtained directly by overshoot
measurements, namely 0,5 - 0,6 Pa (although the Altmann figure
may be too low, since the instrument he used is not very
suitable for overshoot experiments). Furthermore, we can now
calculate a longest relaxation time S", = "Y'}o/G O and obtain 50
100 s, which agrees satisfactorily with e10btained from Dc
392 SYNOVIAL FLUID Vol. 24, No.4

"!
rf 10'

o S 105
o S 104

10'
------+~ 0 [s-' ]

FIG. 7
Shear viscosity ~' and shear modulus G'
of normal synovial fluids

1()2
10 2
'" 5 121
o 5 ",
10' 10'

laO (10 ~
.. 0-

I,.
CL

~r
1......1('.1 10'
,:-
10. 2

103 10. 3

100 10'
- - -__
~ O[s-']

FIG. 8
Shear stress T12 and first normal stress
difference a, of pathological synovial fluids

~
N

100 10-1 Ul
Ul
eli
eli o.6~o.6~6o.o.6Ao.6 6 Cl...
Cl...
.
0000000000000000006i1.,o,llIo
10-1 10- 2 ~
~

oOOOOo~~666 ..

""" Ooo~g.o.6 ...

e
r r
° 00 8' ao
10-2 ~ 6. 6
. . . . . Ll.
10- 3

10-3 10-2 10-1 100 101

---~. 0 [5- 1 ]

FIG. 9
Shear viscosi ty ~' and normal viscosity Ill,
of pathological synovial fluids
Vol. 24, No.4 SYNOVIAL FLUID 393

as glven above.
fhus we may conclUde, that normal synovlal flulds are
highly viscoelastlc. Their Vlscoslty curves are of the Carreau
type with ~.L prop. Dn ana ~~ prop. D~n. ThlS suggests large.
but rather unlform flow unlts in an entanglement type network
solution. This solution structure makes posslble a
normalIzation with the help of "10'

t9.:Jt.hQ1Qgi£201_2:l::':!lQYi~
in thlS study, synovia from patients with jOlnt dlseases
were used, namely inflammatory (rheumatoid arthritis) or
degeneratIve (osteoarthritis) Joint conditlons. Some cases of
unspecific arthritls were also studied. In all these cases the
rheologlcal propertles are lmpaired: ~o is lowered. shear
thlnnlng and normal forces resp. elasticlty are reduced, and in
all cases a reduction of the molecular mass of backbone
hyaluronlc acid is found. Hyaluronlc acid was isolated Trom
synovlal tluld by denSIty-gradIent ultracentrIfugatIon (10) and
contained less than 1 ~ protein. MoleCUlar masses were
determlned by lIght scatterlng. This part of our work will be
reported elsewhere (II).
The results of our experIments are shown, for a few
representative cases, in the following figures. Fig. 8 shows
plots of log "t'11. resp. log ~., vs. log D, Fig. ::1 log...,' resp.
log '1(" vs. log D. In Fig. 10 plots of log "'J I resp. log G' vs.
log D are shown; for a comparison corresponding curves of
normal (healthy) synovia are shown in the upper half of this
figure. We note several features:

''"" "'10 is lowered

8 1
shows no plateau, but rises with D
the general level of both 'YJI and "f., is lowered
'" "t 11. and <5., cross at D<v 1
s-l
'.1'* e l is lowered to 1 - 2O s
the type of the viscosity curves corresponds no
* more to the Carreau-type
normalization (master curve) is no more possible
'"
All these observations suggest, that not only the average
molecular mass of the hyaluronIC acid has been reduced to
S IUD g.mol- 1 (measured by light scattering after Isolation),
but also there eXIsts a conslderable inhomogeneIty of the flow
units. For degenerative arthritis ~o is reduced to 0,1-
1 Pa.s, 8 1 to 8 - ~o S., for lnflammatory arthritis "')0 to 0,004
- 0.07 fa.s and 9' to U,02 - 1 s.
All these results suggest, that In pathological cases the
solution network is loosened by degradation of the backbone and
(pOSSIbly) change of conformation of the cOlled chaIn segments.
Thereby, the molecular mass of the backbone seems to play the
most importan~ role: in an intact synovia, Itq molecular mass
must be 2 10 1 g.mol- l even a reduction to lOb g.mol- l brings
about severe impairment of the rheological properties of the
solution, which leads to poor lubrication and degeneration of
shock absorption and load bearing ability.
It must be mentioned, that the problem of dilution of the
synovial flUId by effusion has not been studied in this paper.
394 SYNOVIAL FLUID Vol. 24. No.4

10' la'

10° 10°
[>5120
,..., o 5119
III
la' " 5115 10-'
.....,
co
a. o 5113 co
a.
_--->--.L_~ __. '--'
't!)
~

o 5121
la' " S11G la'

r
o 5 III

10°

';~~
10°
r
la'
""

. "C>..,

......
10"

10- 3 10-2 10-' 10° la' 10 2 10 3

•o [s")

FIG. 10
Shear viscosity 1)' and shear modulus G' of normal
(top) and pathological (bottom) synovial fluids.

healthy synovia p. m.
"Vl 10 '
ni
0..
10 0
<=0-

10-1

r 10- 2

10- 3
! I , I t I

10-3 10- 2 10-1 10 0 10 '

----+~ 0 [5- 1J

FIG. 11

Viscosity ranges of healthy, degenerative

and inflammatory synovial fluids.
Vol. 24, No.4 SYNOVIAL FLUID 395

Its inIluence 1S certa1nly smaller than that of the degradat10n

of hyaluron1c acid; however. 1t may contr1bute to the observed
reduct10n of the rheological properties. In this field further
investigations are certainly required, whereby both the solid
content as a whole and the concentration of hyaluronic acid
must be investigated.

Our results demonstrate, that normal synovial fluids and

pathological ones can be readily differentiated by means of
their rheological properties. In Fig. 11 this is shown at the
example of viscosity curves. Normal fluids and those from
activated resp. different arthritides fall into well
distinguishable regions, which overlap only little and thus can
be used as a diagnostic help for the physician. Our results
allow the following conclusions:
Normal (healthy) synovial fluids consist of network solutions
with non linear viscoelastic properties. Both viscosity and
elastlcity are high. the moleculaf mass_ of the backbone
hyaluronic acid must be at least 10 g.mol 1. The viscosity
curves are of the Carreau-type with a power law portion f9r
both 'Y}' and ~ (same exponent) in the range 10 1 < D < 10 3 .
Normalizatlon with ~o is possible. In the power law range we
find a plateau in G'. All this is indicative of large, but
rather uniform flow units.
In case of diseases the rheological properties are
degenerated: "10 I '\(1 and 9' = 1/Dc are lowered. The flow curves
deviate from the Garreau-type. we find no more power law range,
no plateau in G' (G' increases with D), normalization with
~o is no more possible. These findings suggest a considerable
nonunlformity of the flow units.
The changes in the rheological parameters can be used as a
diagnostic help. We found the following parameters significant:
""'1o,the ratio "f"Jo/'Y)1J=;'oo (as a measure for shear thinning),
e', and e'. c (to eliminate the concentration influence as
caused by effusion). The results are shown in Table 1. They
indicate, that the parameters shown are actually characteristic
for the state of the synovial fluid and can therefore be used
as diagnostic aid.

If we try to extract the characteristic features from our

results, we can summarize them with the help of Fig. 12, which
shows schematically the changes in viscosity curves as a
function of the severity of the disease. Thus the response of
the healthy fluid (uppermost) is in the first instance
generally reduced in both "Y)o the...,,' level and in G'. With
increasing severity of the disease, the destruction of the
solution structure is enhanced, and as a consequence we find

"0'
curves with a very low viscosity level and poorly determinable
In some cases we find no "'r""lo at all, but at very low D-
values ~' rises very steeply, which indicates the existence of
396 SYNOV IAL FLU ID Vol. 24, No.4

TABLE 1

Rheological parameters for synovial fluids

Diagnosis '1'/0 [Pa.s] S' [:;] S'.c [s.g.cm' 3 ]

'1'/0/'1'/0=300

Normal 1 - 40 100 40 - 100 200 -300

Activated,
0.1 - 1 5 -40 8 - 20 60 -100
degenerative

Chronic.
0.004- 0.07 1 • 4 0.02 - 1 0.1 - 4
inflammatory

viscosity decreases

.
Dc 1 III
Vl
11!
III
¢
:S .'!1
I:' ~ ....0
~

01 onset of ~
~ ~ ~

+
.;::

~
III

~ "
III

r
.-9 Vl
~ 0>
~ .S
eo Vl
.;, 11!

T
III
....
U
structure completely .S
destroyed

-
----I~~ log D

FIG. 12

Rheological effects of pathological

synovia deterioration.
Vol. 24, No.4 SYNOVIAL FLUID 397

a yield value. Stlll more severe cases show viscosity curves of

the bottom type: very low VlscoSlty level, nearly no shear
thinnlng, nearly Newtonian behavlor as a consequence of an
apparently complete destructuratlon. In the same order, the
elastic propertles are lowered flrst and then lost altogether.
ln the flrst stages of a dlsease, the reduction of elastic
properties lS even raster than that of viscous properties (thls
agrees wlth fIndlngs by means or osclilatory measurements
( 12) ) .
Phenomenologically, this behavlor may be explained as
follows. Normal synovial fluids have high 9' ,therefore
stress relaxation at rest is slow. The lubrication film retains
its load bearing capacity also during prolonged loading and
remains In the joint gap. In motion, ~' and e' are decreased
(G' remains constant), thus relaxation is faster and can take
place during ~ load-recovery cycle. In very fast motion
lD ~ 10 3 s 1), G' increases and thus e' decreases faster
than before: relaxation takes place faster, but elastic storage
is increased and guarantees shock absorption also during strain
peaks.
In pathological synovlal fluids, "101 'Y)' and e' decrease,
the G'-plateau disappears, and therefore e' decreases steadily,
but rather fast wlth increaslng D. From this facts, we arrive
at the important finding:

For a pathological synovial fluid an average straining

acts like severe straining for a normal one.

In terms of molecular structure, these observations can be

explained by successive degeneration of the solution network
structure. The first stages may be reversible. The conformation
is changed from loose (free draining) to tight (non draining)
coiling of the molecular chains, thereby the number of
entanglements lS reduced. Lateral bonds to side groups are
broken. With increasing lmpalrment, irreverslble degradation of
the backbone may take place, the viscosity level is lowered and
elastlcity reduced. The reversible destruction of side bonds
will increase the shear sensitivity. If enough short chains are
available, this might even lead to thixotropic structures and
the formation of a yield value at rest resp. at very low shear
rates. Such a yield value as a consequence of a thixotropic
structure may also be responsible for the well known effect of
the'morning stiffness" in joints. With increasing impairment,
irreversible effects take place: severe degradation of the
backbone, permanent split-off of side chains, change of
conformation, so that the fragments of chain molecules collapse
and form very tight (non drainable) coils. As a consequence,
overlapping and entangling of chain segments are strongly
reduced. Finally, if only very short and tightly coiled chain
segments are available, no more overlap and no more
entanglements are possible, and we find the flow behavior of a
Newtonian fluid. Most important is the breakdown of the
backbone: ,a degradation to 1/10 of its molecular mass (that is
to M = 10° g.mol- 1 ) suffices to bring about heavy impairment of
the rheological properties. Only a backbone (hyaluronic acid)
molecular mass of ~ 10 7 g.mol- 1 will guarantee
398 SYNOVIAL FLUID Vol. 24, No.4

satisfactory performance of a synovial fluid. This is in

agreement with the observation, that in flowing polymers a
small addition of very long molecules will bring about an
overproportional increase of viscosity l13). Therefore it
appears plausible that the degradation of hyaluronic acid is
the major factor in the pathologic degeneration of synovial
fluid.
Finally, the aspects for lntroducing synthetic synovia
expanders shall be discussed. It has repeatedly been attempted
to apply concentrated solutions of linear or branched polymers
lPolyacrylamide, polyvinylpyrrolidon, natural polysaccharides
as dextranes or guar-gum) to this purpose, but so far with
limited success. To duplicate the rheological properties of a
normal synovial fluid, we wpuld need a molecule with a
molecular mass of at least lUi g.mol- 1 , possible with side
chains, so that the highly vlscoelastic consistency is
reproduced. Usual llnear or slightly branched water soluble
polymers wlll probably be not good enough, and what we need is
a polymer tallor made just for this purpose. Only then
compatibility tests should be performed, first with tissue,
later with live joints of animals. ThlS is certainly a long way
to go; but in view of the results reported in this paper we at
least know what we have to look for.

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~~~lng~=Ih§~i~~ Universitat Erlangen-NUrnberg 1984