Heel Spur Formation and the Subcalcaneal Enthesis

of
the Plantar Fascia
TSUKASA KUMAI and MIKE BENJAMIN
ABSTRACT. Objective. To describe the structure and significance of subcalcaneal heel spurs associated with the
plantar fascia.
Methods. The enthesis of the plantar fascia was removed from 17 elderly cadavers by sagittal saw
cuts either side of the medial tuberosity, radiographs were taken, and the tissue was processed for
routine histology. Sagittal sections were stained with toluidine blue, Masson’s trichrome, or alcian
blue, and sections were matched with the corresponding radiographs.
Results. Spurs develop on the deep surface of the plantar fascia but their formation is heralded by
degenerative changes that occur within it. According to differences between small and large spurs,
we propose that there are 3 stages in their development: (1) an initial formation of cartilage cell clusters
and fissures at the plantar fascia enthesis; (2) thickening of the subchondral bone plate at the
enthesis as small spurs form; (3) development of vertically oriented trabeculae buttressing the proximal
end of larger spurs. The spurs grow by a combination of intramembranous and chondroidal
ossification.
Conclusion. Contrary to popular belief, subcalcaneal heel spurs cannot be traction spurs as they do
not develop within the plantar fascia itself. They are thus fundamentally different from heel spurs in
the Achilles tendon. We suggest instead that they develop as a consequence of degenerative changes
that occur in the plantar fascia enthesis. (J Rheumatol 2002;29:1957–64)

HEEL SPUR PLANTAR FASCIA ENTHESIS

ENTHESOPATHY HISTOPATHOLOGY
Subcalcaneal heel pain is very common and well known to
rheumatologists and orthopedic surgeons alike. It is characterized
by extreme tenderness along the plantar-medial
aspect of the heel, and often presents as a repetitive strain
injury in distance runners or in middle aged patients with a
history of prolonged standing1-7. However, heel pain can
also be linked to underlying systemic disorders such as
rheumatoid arthritis (RA), ankylosing spondylitis, and
Reiter’s syndrome8-12. In these conditions, the symptoms are
often bilateral. Although the cause of heel pain is unclear, it
is frequently associated with bony spurs1,2 — although these
have also been identified in 15% of asymptomatic patients13.
The most commonly accepted theory for spur formation is a
biomechanical one, for they are widely thought to form as a
result of excessive traction at the origin of the plantar fascia
and flexor digitorum brevis1,4,10,14-16. The spurs are viewed
as a reactive ossification to chronic inflammation1,17.
We recently reported that traction spurs developing in the
Achilles tendon of elderly rats are initiated by endochondral
ossification following vascular invasion from the bone
marrow, with vessel ingrowth proceeding along rows of
enthesis fibrocartilage cells18. Here we describe the structure
of bony spurs of different sizes in the plantar fascia of
elderly dissecting room cadavers and suggest a hypothesis
for their formation. As the plantar fascia is mechanically
linked to the Achilles tendon by fibrous tissue passing below
the calcaneus and by a series of regularly oriented bony
trabeculae19, we predicted that the spurs form by a similar
mechanism. However, our findings show that this cannot be
the case and that the spurs must be fundamentally different.
MATERIALS AND METHODS
The subcalcaneal enthesis of the plantar fascia, including the entire medial
tuberosity of the calcaneus and adjacent connective tissues, was removed
from 17 elderly cadavers (64–97 years of age, 10 male, 7 female). Medical
histories were not available other than the cause of death, and the cadavers
were selected from a total of 34 available specimens according to the
quality of preservation and the absence of gross abnormalities in the foot.
The cadavers were fixed with embalming fluid containing 4% formaldehyde
and 25% alcohol. Entheses were removed from one limb only by
making parallel saw cuts either side of the medial tuberosity of the calcaneus
in the sagittal plane. Radiographs were taken of all specimens at this
stage and the tissue subsequently processed for routine histology as
described19. Briefly, the samples were further fixed in 10% neutral buffered
formal saline, decalcified in 5% nitric acid, dehydrated in graded alcohols,
cleared, and embedded in paraffin wax. Serial sagittal sections were cut at
8 μm and 6 sections collected systematically at 1 mm intervals throughout
the blocks of tissue. Peripheral sections were discarded in order to remove
the risk of viewing artefactual damage in the tissue that resulted from the
saw cuts. Adjacent slides were stained with alcian blue, hematoxylin and
eosin, Masson’s trichrome, and toluidine blue. The maximum thickness of the plantar fascia was compared in specimens
with and without radiologically detectable heel spurs. Estimates were
made on slides with a micrometer eyepiece at 100 magnification.
Measurements were made at each sample point in the blocks, and the
largest value was taken as the fascial thickness. Differences in the mean
thickness were assessed by an unpaired Student t test and a value of p <
0.05 was regarded as significant.
RESULTS
Bony spurs. Bony spurs were common and a graded series
of spurs of different sizes are illustrated in Figure 1 in an
attempt to mimic a “developmental sequence.” Possible
stages in their development are summarized in Figure 2. In
8 specimens, the spurs were visible radiologically, and in a
further 3 they could be detected microscopically. Larger
spurs showed both radiological and histological evidence of
cortical bone thickening (Figures 1d, e, i, j). The mean thickness
of the plantar fascia was significantly greater (p < 0.02)
in radiographically visible spurs than in specimens that
either lacked spurs or had microscopical ones (5.1 ± 0.39
mm compared with 4.0 ± 0.44 mm, respectively). While the
precise location of the spurs was not always evident from
radiographs, the corresponding histological sections clearly
showed that they were always located immediately deep to
the plantar fascia on its dorsal side, and thus were not
embedded within it. This applied not only to the 5 spurs
illustrated in Figure 1, but also to the remaining spurs that
are not illustrated. The spurs were covered by a pad of
uncalcified fibrocartilage on their plantar side (Figures 3a
and 4d), and their tips were separated from the fascia by a
fatty or fibrous connective tissue, richly supplied with blood
vessels and nerves (Figures 4d and e).
Bony spurs of all sizes showed abundant evidence of
ossification and an irregular surface of the bone commonly
suggested active bone turnover — osteoclasts lying in
Howship’s lacunae were present on their marrow cavity side
(Figure 3e). Periosteal bone deposition by intramembranous
ossification was seen on the outer, dorsal aspect of the spur
(Figures 3c and d), but chondroidal ossification (i.e., the
method by which chondroid bone is formed) occurred on the
plantar side (Figures 3a and b). Chondroid bone was characterized
by the presence of fibrocartilage cells embedded in
bone-like matrix and was particularly common in larger
bony spurs (Figure 3b). Typical signs of endochondral ossification
(cartilage cell hypertrophy, cell death, and vascular
invasion) were not detected in any of the specimens, and
calcified fibrocartilage was only rarely present at the surface
of the spur.
Histopathology of the plantar fascia enthesis. The subcalcaneal
enthesis was highly fibrocartilaginous and regions of
calcified and uncalcified fibrocartilage were readily identifiable
at the insertion site (Figure 4a). These 2 zones were
separated by one or more tidemarks that defined the outer
limit of calcification (Figure 4a). In most specime was a clear distinction between fiber arrangement in the
uncalcified fibrocartilage of the dorsal (“deep”) and plantar
(“superficial”) parts of the enthesis. In the latter, the fibers
were sagitally arranged, but in the former, fascicles of transversely
arranged fibers were interwoven with others that ran
sagitally, thus creating a distinctive basketweave of fiber
bundles (Figure 4b). In the dorsal part of the enthesis, the
different bundles were separated by thin films of loose
connective tissue (“endoligament” in Figure 4b) and the
fibrocartilage was generally more highly cellular (Figure
4c). Muscle fibers from flexor digitorum brevis were
attached to the dorsal side of the plantar fascia (Figure 4d)
and numerous small blood vessels and nerves were present
immediately deep to it, in a region of fatty or fibrous
connective tissue close to the enthesis (Figures 4d and e).
However, the enthesis fibrocartilage itself was generally
avascular and aneural. The subchondral bone plate was
consistently thin (Figures 1f to j) and the deeper trabeculae
were regularly aligned along the direction of tensile force at
the enthesis, and continuous with similar trabeculae at the
Achilles tendon insertion (Figure 4f). In contrast, trabeculae
were vertically arranged at the anterior margin of the calcaneus
(Figure 4f).
Histopathological changes were common, especially in
the dorsal region of enthesis fibrocartilage. They included
cartilage cell clustering, longitudinal fissure formation, and
local erosion of subchondral bone (Figures 5a to f). The
cartilage cell clusters were located close to the bone and
were surrounded by an extracellular matrix (ECM) that
stained intensely with alcian blue (Figures 5a to c). The
longitudinal fissures were splits in the fibrocartilage that
contained a strongly-staining, amorphous ECM, suggesting
mucoid degeneration (Figure 5d). The subchondral bone
was locally absent at some parts of the enthesis, and either
blood vessels in the marrow cavity were in direct contact
with the uncalcified enthesis fibrocartilage or the defect was
filled with a vascular loose connective tissue (Figure 5f).
DISCUSSION
The location of the subcalcaneal heel spurs just deep to the
plantar fascia (rather than within it) challenges the widely
held view that they are traction spurs developing in response
to tension1,4,10,14-16. We suggest instead that they represent a
response to mechanical stress at the enthesis and are comparable
to the peripheral osteophytes of articular cartilage in
patients with osteoarthritis20,21. Whether the spurs are the
cause or an effect of the plantar fascial thickening reported
here and by Berkowitz, et al22 is unclear. The cell clusters
and longitudinal fissures resemble those in osteoarthritic
cartilage21,23 and have been reported in the entheses of
human tendons24,25. Intriguingly, calcaneal spurs are also
more frequent in patients with osteoarthritis than those
without — and the frequency rises with age11,26. In terms of
repetitive loading experienced, the fibrocartilage of thens, there