Original articles
OrthopaedicSurgery&
Eur J Orthop SurgTraumatol(2000) 10:77-83
Morphogenesis,anatomyand histologyof the ligamentumflavum
D. Viejo-Fuertes ~, D. Liguoro 2 J.M. Vital 2 and J.J. Rombouts
1D6parternent de ChirurgieOrthop~dique,CliniquesUniversitairesSaint-Luc,Universit~Catholiquede Louvain,Bruxelles,Belgique
2Laboratoired'Anatomie,Universit4Victor Segalen-BordeauxII, Bordeaux,France
Summary: Spinal ligaments play a very
important role in the mechanics of the
spine. Curiously the ligamentum flavum
(LF) has been the object of few specific
studies. First a study on LF of foetuses
has been carried out with anatomical,
histological (classic staining techniques,
immunohistochemistry and ultrastruc-
tural study) and radiological techniques.
The LF is very different from the other
spinal ligaments. It derives very early
from a mesenchymeal tissue and not
from the primitive muscular structures.
Its development, its relations are very
closed with lamina, capsules and ten-
dons of spinal muscles. It is quickly an
innervated and vascularized ligament
with a predominance of elastic fibres. It
is from a structural and functional point
of view, by its two layers, the equivalent
of a capsule and an articular ligament.
Second, an u l t r a s t r u c t u r a l and
immunohistochemical study has been
realized on adult LF to specify the kind
of its innervation. It is innervated by
fibres of great diameter, with myelin
sheath. The positive immunomarking
with neuropeptid Y is in favour of the
proprioceptive type of this innervation.
Code M~ary: 6004.0
Correspondence to: D. Viejo-Fuertes
The LF has a specific and active role
within the vertebral building, at the level
of the spinal joints. Its characteristics
described above confirm its neurological
role especially for p r o p r i o c e p t i v e
control. On the whole, this ligament is
both mobilizing, stabilizing and adviser.
The implications in spinal physiopatho-
logy are numerous.
Key words: Ligamentum flavum - Spinal
ligaments - A n a t o m y - H i s t o l o g y -
Innervation - Morphogenesis
The spinal ligaments play a very impor-
tant role in the mechanics of the spine.
Two fundamental functions are sugges-
ted for these ligaments, mechanical and
neurologic [4, 7, 11, 15]. With regard to
the ligamentum flavum (LF), very few
studies were carried out. This ligament
is a particular intersegmented structure,
with close relationship with the nervous,
muscular, tendinous and articular struc-
tures. Its histological structure is diffe-
rent from that of the other spinal liga-
ments. The formation and the evolution
of the skeletal, muscular, ligamentous
and nervous systems are indissociable
and conditioned by the neighbouring
structures. The destiny of each area
depends on the organization of its com-
ponents and its position in the embryo-
nic system. The LF is present very early
at the foetus in the form of fibrous
EuropeanJournal of
Traumatology
9 Springer-Verlag 2000
connective tissue and will evolve to an
organized connective tissue with elastic
fibre prevalence, vascularized and inner-
vated tissue [32], which confers particu-
lar biomechanical properties to him.
This first justified a study on foetus.
Second a study on adult LF was justified
to specify the kind of innervation of this
ligament, the anatomical and histologi-
cal aspects on adult had been studied
before [32].
Materials and methods
Morphogenesisof the LF
The various studies were carried out on
foetuses from 8 to 33 wk (wk = weeks of
amenorrhoea) fixed in a lo% formalin
solution. These foetuses are the products
of therapeutic interruption of pregnan-
cies (foeto-maternal infections), poly-
malformative syndromes are eliminated.
The morphological study was carried
out on 6 foetuses 0o, 16, 19, 25 wk), in
prone and neutral position, with dissec-
tion under operative microscope (Zeiss,
OPMI6). The histological study was car-
ried out on 9 foetuses (8, lO, 14, 16, 19, 22,
24, 27, 33 wk). Blocks including 3 verte-
brae were separated with the help of X-
ray examination, on the thoracic, thora-
c o - l u m b a r and l u m b a r levels. The
blocks were cut in the sagittal and hori-
zontal plans, for the various techniques
78
used. Decalcification o f blocks was
necessary before embedding in paraffin
and sections were done with a microto-
me (thickness of 8 microns). Histologic
technology consisted of classic staining
techniques, using trichrome, hematin-
eosin-saffron (HES), orcein, Goldner,
and immunohistochemical study using
protein $1oo to mark the nerve fibres.
An ultrastructural study was carried out
at the same time under transmitting
electron microscope (TEM) and under
sweep e l e c t r o n m i c r o s c o p e (SEM).
Under SEM, the samples were washed
with the buffer and were dehydrated in
ethanol baths of increasing concentra-
tion, followed by two pure acetone baths
15 minutes each one. After the last aceto-
ne bath, the samples were treated by the
method of critical point of COz, then
were metallized with gold in a cathodic
pulverization apparatus. The samples
were observed with a SEM Philips SEM
5a5 u n d e r a tension of lo Kv. Under
MET, the samples, fixed with formalin,
Fig. 1
Foetus of 19 wk, dorsal view with dissection of muscular plans. C o m m o n
lumbar muscular mass (white arrow)
D. Viejo-Fuertes, et al.: Morphogenesis, anatomy and histology of the ligamentum flavum
were p o s t - f i x e d with 1% o s m i u m
tetraoxide during z hours, were dehy-
drated in ethanol baths of increasing
concentration, followed by two baths of
epoxy 1-z-propane, impregnated then
included in epon. After polymerization
(48 hours with 6o~ sections were pro-
duced using an ultramicrotome (Rei-
chert Ultracut) and were collected on
copper grid. The grids were observed
with an electron microscope Philips CM
lo. The radiological study was realized
on 3 foetuses (14, a9, z7 wk) by magnetic
r e s o n a n c e imaging (MRI: Siemens,
Magnetom SP, 1.5 Tesla). Axial sections
were carried out every z millimeters,
allowing to visualize the muscular, liga-
mentous and osseous structures.
Theinnervation of the LFon adult
The study was carried out on 5 LF taking
from operative procedures (lumbar disc
herniation), fixed in a lO% formalin
solution, embedded in paraffin z4 hours
after, except one treated for the MET.
After sections, an immunohistochemical
study was realized using the neuropep-
tid Y (NPY), l'isolectin (isolectin B4,
Vector) and galanin.
Results
Morphogenesis of the LF
The anatomical study: At xo wk, one
observed only one muscular mass on
the right and on the left, without indivi-
dualization of the different spinal erec-
tor muscles. A 16 wk, one noted some
fibrous strips within the m u s c u l a r
masses which started to be individuali-
zed. At 19 wk, longissimus thoracis and
iliocostalis muscles were well individua-
lized, in the same way their tendons of
insertion were longer but of arrange-
ment similar to the adult (Fig. 1). The
muscular aponevrosis were regularly
segmented horizontally. It was not an
artefact of the dissection or conserva-
tion of the foetuses because we checked
it on two other foetuses of the same age.
At z5 wk, this segmentation was not
visible any more and the results of the
dissection similar to the adult. The his-
tological examination: Up to 14 wk, the
thickness of the LF was variable. There
were no clear limits between the LF and
the i n t e r s p i n o u s ligament. The LF
appeared juxtaposed and not inserted
on the lamina, even near the bone cores
of the neural arch. The LF was compo-
sed of disorganized collagen fibres. The-
re were no elastic fibre. After immuno-
m a r k i n g by the p r o t e i n $1oo, no
nervous structure was highlighted, but
t h e r e were some n e r v o u s fibres in
muscles and that confirmed the reliabi-
lity of the method. The cartilaginous
cells could also be m a r k e d but the
colouring was brown and darker, with a
peripheral pinkish halo that clearly dif-
ferentiate them from nervous struc-
tures. At 16 wk, collagen fibres increased
in large numbers, they formed a dense
and more organized connective tissue
(Fig. z). Two superimposed layers of
these fibres were observed, and were
directed towards the posterior articular
processes. Some elastic fibres were
visible very against the cartilaginous
outline of the bone structures. Vessels
D. Viejo-Fuertes, et al.: Morphogenesis, anatomy and histology of the ligamentum flavum
Fig. 2
Foetus of t6 wk; sagittal section; HES coloration
Fig. 4
Foetus of 33 wk; axial section; orcein coloration; Numerous elastic fibres
(thin arrow)
were present within the LF. Nervous
fibres were rare. At 19 wk, the collagen
fibres were larger, organized in "skeins".
The elastic fibres were numerous, of lar-
ge diameter, organized within the colla-
gen fibres which remained prevalent.
The vessels were numerous, close to the
muscular structures and the capsules of
the posterior articular processes, far
from the lamina. After i m m u n o m a r -
king, nervous fibers were present in the
LF, close to the lamina and the articular
capsules. At 2z wk, the organization of
elastic fibres had the combed aspect
observed in the adult, with two perpedi-
cular layers (Fig. 3). At 27 wk, the liga-
ment was clearly organized in its two
layers. The elastic fibres were largely
prevalent. There were vessels within the
LF. The nervous fibres were numerous
79
!il84
:ili!i
Fig. 3
Foetus of zz wk; Immunohistochemistry with Protein Sloo. The two layers
of the ligamentum flavum. Nervous structure (black arrow)
Fig. 5
Foetus of 24 wk. TEM.x 7200. The nervous fibres with myelin sheath. Col-
lagen fibres (black arrow)
and were distributed in the thickness and were laid out in an anarchic way.
and on all the extent of the LF. The The many fibroblasts were in full activi-
synovial of the posterior articular pro- ty ( a b u n d a n t granulous reticulum).
cesses was in formation. At 33 wk, the Thin capillaries were observed within
histological aspects of the LF were those the ligament, but there were no elastic
observed in the adult: compact fibrillary and nervous fibre. A 14 wk, with SEM,
structure, rich in elastic fibers (Fig. 4), on the axial sections, the limits between
divided into two planes (Fig. 6) with cartilage, connective tissue, ligaments
vascular and nervous elements.The and muscles were clearly observed. But
ultrastructural study: At 8 wk, with on sagittal sections, there was no obser-
TEM, the collagen fibres, with their cha- vable clear limit between the LF and the
racteristic periodicity, were numerous interspinous ligament. At a6 wk, with
80
Fig. 6
Internal view of the ligamentum flavumwith its
two layers, inferior lamina (L); superficial layer
(S); deep layer (D); tendons of insertion of the
spinal erector muscles (T)
SEM, the organization in bundles of
parallel fibres was well outlined. Two
perpendicular layers of these fibres were
observed. At 19 wk, with SEM, elastic
fibres were observed within collagen
fibres. With TEM, thin capillaries were
numerous within the LF. Very active
fibroblasts with an abundant granulous
reticulum secreted elastic fibres. At 22
wk, with SEM, elastic fibres were nume-
rous and according to the orientation of
the collagen fibres, pargdlel between
them, but still tangled up by places. At
24 wk, with SEM, the many elastic fibres
were perfectly parallel between them.
The relation between the LF and the
articular capsules was very closed. With
TEM, fibroblasts were still very active.
Nervous pedicles were present close to
the capillaries, made up of many axons,
with the presence of schwann's cells. At
27 wk, the ultrastructural aspect of the
LF was that of the adult, with two layers
whose fibres are opposite, and especially
a very clear elastic fibre prevalence (Fig.
7). The radiological study: The MRI
highlighted bone cores starting from 14
wk, on the level of the posterior arch
and the body of the vertebrae. The LF
was visible only after 19 wk, and quite
visible at 27 wk, on axial sections. The
left and right muscular masses in the
D. Viejo-Fuertes,et al.: Morphogenesis,anatomyand histologyof the ligamentumflavum
Fig. 7
TEM, x 6700. LF on the adult with a little active
fibroblast, elasticand collagenfibres
vertebral gutters were only differentia-
ted from 19 wk.
Innervation of the LF on adult
The immunohistochemical studies reali-
zed with isolectin and galanin, associa-
ted with small neurons, were not conclu-
sive. There was no immunomarking but
many artefacts because of the elastic
fibres. On the other hand, there was
clearly a positive i m m u n o m a r q u a g e
with the NPY, associated with large neu-
rons (Fig. 8).
Discussion
Curiously, the LF has been the object of
few specific studies, except for its res-
ponsability in spinal canal stenosis [2a,
22, 23, 3o, 31, 39], and these studies are
often contradictory. However, recent
studies of its structure, anatomic dispo-
sition, histologic characters and biome-
chanical properties indicate that it is
very different from the other spinal liga-
ments [32].
The results of the various methods of
study concerning the LF on foetuses
agree. At lo wk, there is a single muscu-
lar mass, on both sides, without indivi-
Fig. 8
LF on the adult; immunomarking of NPY
d u a l i z a t i o n of the spinal e r e c t o r
muscles, of the ligamentous and tendi-
nous structures. The LF is a dense and
disorganized connective tissue, compo-
sed of collagen fibres without elastic
fiber nor nervous fibre. During weeks,
the fibroblastic activity is increasingly
significant, and 19 wk is a hinge period
with an individualization of the spinal
erector muscles and their tendons. The
LF have large collagen fibres which are
organized in two perpendicular layers.
The elastic fibres are more numerous
and the nervous and vascular structures
are perfectly locatable. The LF becomes
visible in MRI. The close relationships of
the LF with the articular capsules, to
which it amalgamates by the lateral side
of its deep layer, start to be visible from
22 wk, as the insertion of the LF on the
lamina. In ultrastructural study, nervous
pedicles are observed close to the thin
capillaries, and are constituted by many
axons with Schwann's cells. After 25 wk,
the LF has its final organization and
structure.
Which is the origin of the LF? It
derives from a mesenchymal tissue which
comes from sclerotomal residue left at
the time of vertebral resegmentation and
t h e n d i f f e r e n t i a t e d in f i b r o b l a s t i c
c o n n e c t i v e tissue. But p e r h a p s this
D. V iejo-Fuertes, et al,: Morphogenesis, anatomy and histology of the ligamentum flavum
mesenchymal tissue comes from the
lateral lamina which gives the somato-
pleural mesoblast. Whereas the other
ligaments are constituted later to the
detriment of the primitive muscular
structure [8].
Which is its evolution? In a collagen
frame, the elastic fibres appear and very
early the LF becomes differentiated in a
dense, elastic, innervated and vasculari-
zed tissue, organized in two perpendicu-
lar layers. Its relationship with lamina
and capsules are set up secondarily,
whereas appears the activity of bone
cores. There is thus a perfect synergy
concerning the formation of the various
components of the spinal column. This
formation looks like the constitution of
the limbs. According to the result state-
ment above, it could have implication in
congenital pathology such the idiopathic
scoliosis, the vertebral canal stenosis, by
its role in the stabilization, the mobiliza-
tion. Some authors are convinced of the
importance of the LF in the vertebral
development and imply it at the origin
of the idiopathic scoliosis of adolescent.
Some of them have advanced the pos-
sible role of the system of elastic fibres
[3, 13, 29, 37].
Anatomically, the LF is constituted
by two layers whose fibres are opposite
[24, 32, 38]. There is a virtual "gliding"
space between the two layers, especially
obvious at the lumbar level. The two
layers are probably differently stressed
according to the constraints exerted on
the spine. The LF has close relation with
the posterior articular processes. Its
deep layer is in continuity laterally with
the articular capsule which it thus rein-
forced. Some authors [36] showed that
the fibrous articular capsule includes
two layers: an outer layer constituted by
dense connective tissue, with parallel
bundles of collagen fibres; an inner layer
constituted by bundles of elastic fibres
similar with LF. The outer layer is com-
parable with a ligament with transverse
fibres which stabilize the articulation.
Therefore, this ligament has several
roles, it is protective for the neurological
structures, it is stabilizing for the inter-
segmentary level thanks to its superficial
layer, capsular vestige, and its great deep
layer, it has a neurological role because
its precocious innervation contrarily to
some previous studies have noted [1, 2,
lZ, 20, 28, 34, 35], because of its close
relations with muscular, tendinous and
nervous structures.
What kind of innervation? The sum
of anatomic studies on the innervation
of the dorsal arch [5, 6, 9, 14, 18, 19]
demonstrates, at each metameric level,
an innervation for the longissimus tho-
racis muscle, articular processes and
supra- and inter-spinous ligaments. No
description specifies a nerve branch des-
tined to the LF, but a medial branch
from the dorsal root of the spinal nerve
crosses the dorsal aspect of the lamina at
each spinal level, suggesting that inner-
vation of the LF is thus ensured. We
have tried to define the type of the ner-
vous fibres according to their neuro-
transmitters. There are 2 types of neu-
rons going to the dorsal horn of the
spinal cord, small neurons (C fibres and
A-delta fibres) and large neurons (A-
b&a fibres). Neuropeptid Y comes from
large neurons, so probably propriocepti-
ve fibres. There is a surexpression of this
neuropeptid after nervous lesion. In our
study, the immunomarquage with the
NPY was important but no visible with
isolectin and galanin which are associa-
ted with small neurons. But it has been
demonstrated on animal patterns that
peripheral nervous lesions can induce
the expression of a new phenotype and
particularly the synthesis of neuropep-
rids and their receptors. A hypothesis is
that these alterations of the phenotype
go against pain p h e n o m e n o n [ 1 6 ] .
When one considers the spinal mor-
phogenesis, it seems obvious that the
acquisition of bipedy is an unfavorable
biomechanical situation for the spinal
column. A new approach of biomecha-
nics of the spine is for that very signifi-
cant. Many authors agree now to consi-
der the anatomy and the function of the
spinal c o l u m n on three levels: the
column as a whole, various areas of the
column, segmentary and intersegmenta-
ry levels [26]. Many muscles maintain
this unstable building which is the spinal
column. In the intersegmentary level,
the LF takes part in the maintenance of
posture, by the mean of loco-regional
reflexes, initiating the muscular contrac-
81
tions, thus allowing the maintenance of
static and dynamic balance. Among the
spinal ligaments, the LF is very particu-
lar because it is most resistant to the
traction and the most elastic. It is stret-
ched in flexion, contracted in extension
and at rest present a pre-tension of 15%,
which decreases with aging [lO, 17, z5,
33]. The LF must be consider as part of
each metameric unit, as forming integral
part of the posterior articular system
So the LF has a protective role of
nervous structures, a mechanical role
because of its two layers with predomi-
nance of elastic fibers. Thanks to its
innervation, to its closed relations with
the t e n d o n s of the spinal erector
muscles, to the closed relation of its
deep layer with the articular capsule, it
plays a proprioceptive role, adviser and
sentinel, by segmentar reflex.
During the life, innervation is going
to decrease and probably will be modi-
fied towards a nociceptive phenotype,
the ligament becoming more sentinel
than adviser. On the whole, this liga-
ment is both mobilizing, stabilizing and
adviser.
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immunohistochemicat observation. Spine a7:
1353-136o
Received February 16, 2ooo / Accepted in final
form February 21, 2000
D. Viejo-Fuertes, et al.: Morphogenesis, anatomy and histology of the ligamentum flavum 83

Morphogen~se,anatomie et histologiedu liagmenum flavum

R6sum6 : Les ligaments rachidiens jouent un r61e important dans la biom6canique du

rachis. Le ligamentum flavum (LF) a 4t4 peu 4tudi4 alors qu'il est tr~s particulier. Apr6s
des travaux rapport4s au pr4alable (3z) sur le LF adulte, une 4tude anatomique, histolo-
gique, ultrastructurale et radiologique (RMI) a 4t6 r6alis4e sur le foetus ; et une 4tude
ultrastructurale et immunohistochimique sur des LF pr~lev4s en per-op4ratoire pour
pr6ciser le type d'innervation de ce ligament.
Le LF est tr6s t6t form4 ~t partir d'un tissu m6senchymateux et non ~ partir des
structures musculaires primitives c o m m e les autres ligaments. Son d6veloppement se fair
en synergie avec les structures voisines avec lesquelles il est en relation 4troite: capsules
articulaires, tendons des muscles 6recteurs du rachis. I1 devient rapidement un ligament
pr4dominance de fibres 41astiques, organis4 en deux couches, innerv~ et vascularis4.
L'~tude de sa morphogen~se indique qu'il est d'un point de vue structurel et fonctionnel,
par ses z couches, h la fois l'~quivalent d'une capsule et d'un ligament articulaire. Sa
structure histologique particulibre lui conf'ere des propri~t6s biom4caniques sp6cifiques.
Chez l'adulte, les 6tudes r~alis~es indiquent que ce ligament innerv6 contient des
fibres my61inis6es de gros diam~tre, immunor4actives pour le Neuropeptide Y, et non
pour l'isolectine et la galanine, et donc en faveur de fibres de signification propriocepti-
ve. Mais il est possible que certaines 16sions induisent de nouveaux ph~notypes vis h vis
des mol4cules synth~tis~es (nociception secondaire 6ventuelle).
Le LF est donc un ligament actif au sein de l'4difice vert4bral, prenant part au com-
plexe articulaire. I1 est mobilisateur, stabilisateur et informateur au niveau intersegmen-
taire. Les implications en physiopathologie rachidienne sont nombreuses.

Mots d4s : Ligamentum flavum - Ligaments rachidiens - Anatomie - Histologie - Mor-

phogenbse - Innervation