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Studies on the innervation of the medial meniscus in the human knee joint.

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Studies on the Innervation of the Medial
Meniscus in the Human Knee Joint'
A. S. WILSON,2 P. G. LEGG3 AND J. C. McNEUR
Medical School, Monash University, Clayton, Victoria, Australia
ABSTRACT
Histological and ultrastructural studies on the medial meniscus
in the human knee joint show that nerve fibres, both myelinated and unmyelinated,
extend from the periarticular plexus into the meniscus as far as the intermediate
third. These neural elements are not exclusively paravascular in position and it is
reasonable to postulate a function other than vasomotor or vasosensory for them.
The topographical features of the innervation of the adult human knee joint,
as described by Schaeffer ('42) and Hollinshead ('66) are well understood but
the precise extent to which nerve fibres
penetrate intra-articular structures such as
the menisci remains undefined. The functional studies of Samuel ('52) and Andrew
('54) indicating that neural elements are
present within periarticular structures
agree with the histological findings of
Rossi ('50) and Polacek ('61) but the question of meniscal innervation is not considered.
Gardner ('48) in an extensive histological survey, reports that, in foetal human
knee joints, some vessels and nerves enter
the substance of the menisci but no exact
value is given for the depth of their penetration. Freeman and Wyke ('67) state
that those few nerve fibres present within
menisci of adult cats are confined to the
outermost layers, occupy paravascular positions and possess no specialized endformations. They report that no neural elements can be seen within the central fibrocartilaginous zone.
In the histological part of this investigation, an attempt is made to determine more
precisely, the extent and nature of the
nerve fibres which ramify within adult human menisci. Accurately orientated portions of menisci are subjected to electron
microscopy so that comparisons may be
made between the histological and ultrastructural features of meniscal innervation.
Medial menisci were obtained at operation from 10 male patients, aged 16 to 29
years, who had suffered traumatic knee injury. Only menisci in which the damage
ANAT. REC., 165: 485-492.
was clearly localized to either the anterior
or posterior horn were used.
( a ) Histological studies : Immediately on
removal, eight menisci were fixed in 10%
formalin for approximately 12 hours, after
which both anterior and posterior horns
were removed and discarded, thus leaving
macroscopically undamaged middle portions as indicated by B (fig. 1 ) . These
portions were then placed in 10% formalin
over marble chips for a further 10 days.
Three portions were embedded in paraffin
wax, and serial sections, representing three
distinct planes were cut at a thickness of
5 v, and stained, either with haematoxylin
and eosin or by Mallory's trichrome procedure. From the remaining five portions,
frozen sections were cut at a thickness of
100 and impregnated with silver according to Schofield ('60).
(b) Ultrastructural studies: Three specimens, each approximately 3 mm in thickness, and orientated as shown (fig. 2)
were cut at operation from the middle portion of two menisci. All peripheral connective tissue was removed and they were then
immersed in phosphate buffered 4% distilled glutaraldehyde for one hour at 4°C.
Each specimen was then divided longitudinally into two narrow strips and fixed for a
further three hours in glutaraldehyde. Postfixation was carried out in ice-cold 2.5%
osmium tetroxide buffered with a potassium dichromate-calcium chloride mixture
(Richardson, '62). After dehydration and
Received Dec. 2, '68. Accepted June 18, '69.
1 A preliminary report on these studies was presented at the Annual Meeting of the Anatomical
Society of Australia and New Zealand in May 1968.
2 Present address: Department of Anatomy, University of Western Ontario, London, Canada.
3 Present address: Department of Anatomy, University of Minnesota, Minneapolis, Minnesota.
485
486
A. S. WILSON, P. G. LEGG
embedding in Araldite, thin sections were
cut, stained with lead citrate (Reynolds,
'63) and examined under the electron microscope. During these procedures, care
was taken to ensure accurate orientation.
For purposes of description, the portions
of meniscus, orientated as 2 and 3 (fig. 2)
were divided into internal, intermediate
and external thirds by measurement (fig.
3). Sections were cut in sequence from internal to external zones until neural tissue
was positively identified.
OBSERVATIONS
( a ) Histological studies : In sections cut
at right angles to the long axis of the limb
and stained with haematoxylin and eosin
or Mallory's trichrome stain, conspicuous
indentations, containing lightly stained
connective tissue were evident at irregular
intervals along the peripheral border of
the meniscus. This finding was confirmed
in specimens which represented other
planes of section. Vascular structures
within these indentations were generally
directed at right angles to the margin of
the meniscus (fig. 4).
In silver preparations, periarticular
nerve fibres were traced to the external
border of the meniscus where the majority
appeared to terminate, although no specialized end-formations were observed.
However, on approaching the meniscus,
some fibres changed their general direction
from radial to circumferential. These comprised small myelinated fibres approximately 5 CI in diameter and fasciculi of unmyelinated fibres (fig. 5). Some of these
nerve fibres penetrated the external border
of the meniscus at the regions of indentation formed by the capsular fibrous tissue
apd although some were clearly paravascular, others arborized at some distance
from vessels within the external third. .On
several occasions neurovascular bundles
were identified within small interstitial
areas of connective tissue, usually near the
junction between external and intermediate
thirds (fig. 6). Occasionally, tortuous argyrophilic axis cylinders were traced from
the periarticular tissue through the external third and deep into the intermediate
third of the meniscus where capillary loops
were also seen (fig. 7).
AND
J. C. 1McNEUR
The predominant cell type in the external third was elongated and resembled
a fibroblast whereas, at the internal margin
of the meniscus, the majority of cells were
round to ovoid in outline. These were commonly seen in pairs and resembled cartilage cells. Cells of the intermediate third
portrayed some features of both of these
distinct types (fig. 8).
( b ) Ultrastructural studies: In all of
the specimens examined, fasciculi of nerve
fibres cut in various planes, were present
in the external third of the meniscus. The
largest fasciculi generally contained 1-4
myelinated fibres which ranged in diameter
from 1.5-4 p and 30-50 unmyelinated
fibres. Each large fasciculus was surrounded by a distinct perineurial sheath
(fig. 9 ) . The smallest fasciculi contained
only unmyelinated fibres which were characteristically devoid of perineurium, but
which were accompanied by a co-axial covering of collagen fibres (fig. 10). While it
was obvious that some fasciculi were paravascular in position, many were embedded
in the matrix at some distance from vessels.
Nerve fibres were also clearly identified
in the intermediate third of the meniscus.
Most of these comprised small groups of
unmyelinated fibres enveloped in Schwann
cell coverings and closely resembled the
smallest fasciculi in the external third. NO
specialized end-formations were observed.
Within the internal third of the meniscus
no neural elements were identified with
certainty.
Throughout the intermediate third, the
fine structure of some cells resembled that
of cartilage cells. However, in the internal
third, the resemblance of the predominant
Fig. 1 Indlicates the position of portion B
which was used for histological and ultrastructural studies. Portion A , anterior horn and B, posterior horn, were discarded.
Fig. 2 Illustrates the relationship of specimens used for ultrastructural studies to the CIOSSsection of the meniscus.
Fig. 3 The broken lines indicate the boundaries between external, intermediate and internal thirds of the meniscus.
Fig. 4 Part of a medial meniscus stained with
haematoxylin and eosin. A branch ( B ) from a
periarticular vessel can be seen approaching the
external margin of the meniscus through an indentation of pale-staining capsula tissue.
INNERVATION OF MEDIAL MENISCUS
Figures 1-4
487
488
A. S. WILSON, P. G. LEGG
connective tissue cells to cartilage cells
was most prominent (fig. 11).
DISCUSSION
AND
J. C. McNEUR
specialized insulation which might be expected in this potentially stressful situation. The absence of perineurial coverings
from the small fasciculi suggests that the
axis cylinders may come into closer contact
with adjacent meniscal cells but further
investigations will be required to examine
this possibility.
The morphological differences in predominant connective tissue cell types
within external, intermediate and internal
thirds of the meniscus are conspicuous in
both histological and ultrastructural preparations. The cell population is predominantly fibroblastic in the external third
but is chondrocytic in the internal third.
The cells of the intermediate third of the
meniscus can not be placed definitely in
either of these categories and it seems
probable that they are intermediate, not
only in position, but also in cell type.
It is not possible to ascribe definite
function to the intrameniscal nerve fibres,
but the most important structural considerations are tlhe relative sparsity of nerve
fibres, their comparatively small diameter
and the absence of demonstrable specialized end-formations. Excluding paravascu-
The ease with which the free internal
border of the medial meniscus can be recognized contrasts sharply with the difficulty
in demarkating the attached external border, the position of which is essential for
accurate orientation of nerve fibres within
the meniscus, In this investigation, the outermost layer of circumferentially-directed
connective tissue is considered to be the
external limit of the meniscus and it seems
probable that this outermost layer is equivalent to the “marginal zone” of Schaeffer
(’42) and to the “annular ligament” of
Freeman and Wyke (’67).
Silver studies confirm the observation
in haematoxylin and eosin preparations
and in sections prepared by Mallory’s method that the external boundary of the meniscus is indented at irregular intervals by
pale-staining connective tissue from the
capsule. These indentations contain neurovascular bundles and thus establish portals
of entry into the meniscus for both vessels
and nerve fibres. The continuity, observed
on several occasions between periarticular
5 Silver preparation showing a fasciculus
and intrameniscal nerve fibres, clearly indi- of Fig
the periarticular plexus (PP). It is approxicates that the meniscal nerve fibres are de- mately parallel to the external margin of the
rived from the periarticular plexus. More meniscus which is indicated by the arrow.
Fig. 6 Illustrates a n interstitial area near the
frequently, however, axis cylinders were
seen either as short lengths, directed radi- junction between external (E) and intermediate
( I ) thirds of the meniscus. One vascular strucally, or as components of neurovascular ture
can be identified and the argyrophilic strucbundles which occupied interstitial areas tures ( A S ) indicate nerve fibres cut transversely.
within the meniscus. The paucity of deFig. 7 Tortuous nerve fibre (NF) which was
monstrable long lengths of fibres may be traced from th(e periarticular tissue into the interthird o f the meniscus. Note the rounded
attributable to tortuosity of the axis cyl- mediate
profiles of adjacent connective tissue cells.
inders. Thus histological studies show that
Fig 8 Samples of cells present in (1) external,
the innervation of the meniscus is more ex- ( 2 ) intermediate and (3) internal thirds of the
tensive than previously reported, but they meniscus.
Fig. 9 The largest fasciculus of nerve fibres
provide no detailed information on the intercellular relationships of neural compon- seen. This was situated close to the junction of
external and intermediate thirds of the meniscus.
ents.
Perineurium (P), myelinated fibres (MYF) and
Ultrastructural studies clearly demon- Schwann cell nuclei (SCN) are clearly evident
strate that nerve fibres are present within along with many unmyelinated fibres.
Fig. 10 A small fasciculus of unmyelinated
the external and intermediate thirds of the
nerve fibres (1JMF) within the external third of
meniscus. The largest fasciculi which con- the
meniscus. The blood vessel closest to these
tain a few myelinated fibres of small diam- fibres was on the other side of a connective tissue
eter, Schwann cells and collagen fibres and cell (CTC).
Fig. 11 Illustrates a cartilage cell which was
which are surrounded by a perineurial
present in the internal third of the meniscus.
sheath, closely resemble peripheral nerves Villous
projections (VP), apparently vacant peridescribed by Gamble and Eames (’64) cellular spaces ( S ) and surrounding pseudomemand Wilson (’65). There is no evidence of brane (MEM) are conspicuous features.
Figures 5-8
Figures 9-11
INNERVATION OF MEDIAL MENISCUS
lar components which are probably vasomotor or vasosensory, these features suggest that intrameniscal fibres may perform
an afferent function characterized by
a relatively low conduction velocity. It
seems most likely that the modality which
they transmit is “slow” pain.
LITERATURE CITED
Andrew, B. L. 1954 The sensory innervation of
the medial ligament of the knee joint. J.
Physiol. (Lond.), 123: 241-250.
Freeman, M. A. R., and B. Wyke 1967 The innervation of the knee joint. An anatomical and
histological study i n the cat. J. Anat. (Lond.),
101: 505-532.
Gamble, H. J., and R. A. Eames 1964 An electron microscope study of the connective tissues
of human peripheral nerve. J. Anat. (Lond.),
98: 655-663.
Gardner, E. D. 1948 The innervation of the
knee joint. Anat. Rec., 101: 109-130.
Hollinshead, W. H. 1966 In Anatomy for Surgeons, pp. 786787. Hoeber-Harper International Edition, London and Tokyo; Harper and
Row.
49 1
PolPcek, P. 1961 Differences in the structure
and variability of encapsulated nerve endings in
the joints of some species of mammals. Acta.
Anat., 47: 112-124.
Reynolds, E. S. 1963 The use of lead citrate at
high pH as a n electron-opaque stain in electron
microscopy. 3. Cell. Biol., 17:207.
Richardson, K. C. 1962 The fine structure of
autonomic nerve endings in smooth muscle of
the r a t vas deferens. J. Anat. (Lond.), 96: 427442.
Rossi, F. 1950 Sur l’innervation fine de la
capsule articulaire. Acta Anat., 10: 161-232.
Samuel, E.P. 1952 The autonomic and somatic
innervation of the articular capsule. Anat. Rec.,
113: 53-70.
Schaeffer, 3. P. 1942 In Morris’ Human Anatomy, p. 273, Edition 11, Blakiston, New York
and Toronto.
Schofield, G. C. 1960 Experimental studies on
the innervation of the mucous membrane of the
gut. Brain, 83: 490-514.
Wilson, A. S. 1965 Electron microscope studies
on the nerve fibres and vessels of the phrenic
nerve. In: Proceeding of the Eighth International Congress of Anatomists, Wiesbaden,
1965.
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