Original Article

http://dx.doi.org/10.5115/acb.2013.46.2.149
pISSN 2093-3665 eISSN 2093-3673

Influence of developing ligaments on the

muscles in contact with them: a study of
the annular ligament of the radius and the
sacrospinous ligament in mid-term human
fetuses
Shogo Hayashi 1,2, Ji Hyun Kim 3, Jose Francisco Rodriguez-Vazquez 4, Gen Murakami 5, Yoshitaka
Fukuzawa1, Ken Asamoto2, Takashi Nakano2
1
Medical Education Center, 2Department of Anatomy, Aichi Medical University School of Medicine, Aichi, Japan, 3Department of Anatomy, Chonbuk
National University Medical School, Jeonju, Korea, 4Department of Anatomy and Embryology II, Complutense University School of Medicine, Madrid,
Spain, 5Division of Internal Medicine, Iwamizawa Kojin-kai Hospital, Hokkaido, Japan

Abstract: The supinator muscle originates from the annular ligament of the radius, and the muscle fibers and ligament take
a similar winding course. Likewise, the coccygeus muscle and the sacrospinous ligament are attached together, and show a
similar fiber orientation. During dissection of adult cadavers for our educational curriculum, we had the impression that
these ligaments grow in combination with degeneration of parts of the muscles. In histological sections of 25 human fetuses
at 10−32 weeks of gestation, we found that the proximal parts of the supinator muscle were embedded in collagenous tissue
when the developing annular ligament of the radius joined the thick intermuscular connecting band extending between the
extensor carpi radialis and anconeus muscles at 18−22 weeks of gestation, and the anterior parts of the coccygeus muscle were
surrounded by collagenous tissue when the intramuscular tendon became the sacrospinous ligament at 28−32 weeks. Parts of
these two muscles each seemed to provide a mold for the ligament, and finally became involved with it. This may be the first
report to indicate that a growing ligament has potential to injure parts of the “mother muscle,” and that this process may be
involved in the initial development of the ligament.

Key words: Supinator muscle, Coccygeus muscle, Sacrospinous ligament, Annular ligament of the radius, Human fetus

Received January 4, 2013; 1st Revised January 16, 2013, 2nd Revised January 24, 2013; Accepted February 4, 2013

Introduction as in the case of the patellar tendon and ligament. A skeletal

muscle sometimes originates from or inserts into a ligament:
Skeletal muscles are each connected to a tendon, which typical examples are seen around the elbow and knee joints.
in turn is often joined to a ligament. Thus, discrimination Thus, parts of the supinator muscle originate from the annular
between the tendon and the ligament is sometimes difficult, ligament of the radius (ANL), and both muscle and ligament
take a winding course. The sacrospinous ligament (SSL) has
been illustrated as a triangular structure with a medial base
Corresponding author:
Shogo Hayashi and a lateral apex [1, 2]. Hammer et al. [3] defined the SSL
Medical Education Center, Aichi Medical University School of as a contorted frustum comprising a single cone with elliptic
Medicine, Nagakute, Aichi 480-1195, Japan
Tel: +81-561-62-3311, Fax: +81-561-63-1037, E-mail: sho5-884@umin.ac.jp planes. Henle [4] and Fick [1] described the SSL as being
Copyright © 2013. Anatomy & Cell Biology
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150 Anat Cell Biol 2013;46:149-156 Shogo Hayashi, et al

interspersed by the coccygeus muscle fibers, and Hammer et (crown-rump length [CRL], 55−165 mm; approximately
al. [3] confirmed this fact by using the plastination technique. 10−22 weeks of gestation) for observations of the supinator
Both the “supinator and ANL” and the “coccygeus and SSL” muscle and ANL and 2) 10 larger human fetuses (CRL,
combinations share a common feature in that the directions 150−260 mm; approximately 20−32 weeks of gestation) for
of their fibers are very similar in adults. observations of the coccygeus muscle and SSL. All the fetuses
Mechanical loading by skeletal muscles is required for were part of the large collection kept at the Embryology
tendon regeneration and repair [5, 6]. Likewise, dynamic Institute of the Universidad Complutense, Madrid, being
loading by skeletal muscles is critically important for the products of urgent abortion, miscarriages, or ectopic
the morphogenesis of tendon and bone. During fetal pregnancies managed at the Department of Obstetrics of the
development, early muscle contraction confers a specific University. Approval for the study was granted by the ethics
morphology on a tendon [5, 7], and in turn, the tendon committee of the university.
confers a specific shape on the bone [8, 9]. Does the inductive The donated fetuses were fixed with 10% v/v formalin
relationship between a muscle and a tendon also apply to a solution for more than 3 months. After division into the head
muscle and a ligament? In the present study, by focusing on and neck, thorax, upper extremities, abdomen, and pelvis
two muscle and ligament pairs, we investigated the possibility with part of the thigh, and the other parts of lower extremities,
that the two structures might show coordinated development the 15 specimens for the study of the elbow were decalcified
and growth, i.e., that the muscle confers a suitable mor­ by incubating them at 4oC in a 0.5 mol/l EDTA solution (pH
phology on the ligament. Nevertheless, during dissection 7.5; Wako, Tokyo, Japan), while the other 10 larger specimens
of adult cadavers for our educational curriculum, we had were decalcified with 5% v/v nitric acid at room temperature.
an impression that these ligaments grow in combination Routine procedures for paraffin-embedded histology were
with degeneration of parts of the muscles because the fiber performed. Five- (or 10-) μm-thick sections of the elbow (or
directions were almost the same and because the muscles pelvis) were prepared at intervals of 10−20 (100−200) μm. All
sometimes developed poorly. elbows were cut transversely across the long axis of the radius,
Development of the ANL during the fetal stage has been while for the pelvis, horizontal (3 specimens) or sagittal (7
described by many research groups [10-13], but its close specimens) sections were prepared. Most of the sections were
relationship to the supinator has been referred to in only a stained with hematoxylin and eosin, Masson trichrome, or
single sentence: “The initial ANL is strongest posteriorly at silver staining, while some sections of the smaller fetuses were
the origin of the supinator muscle” [14]. Does the supinator studied via immunohistochemisty with mouse monoclonal
develop prior to the ANL around the head of the radius? Fetal anti-human desmin (1:50, M0760, Dako, Glostrup, Denmark)
development of the coccygeus muscle has been described to show the striated muscle fibers. Autoclave pretreatment
by several groups [15-17]. Niikura et al. [16] stated that the was not performed because of the loose nature of the fetal
initial SSL is formed by a thick aponeurosis between the tissues. The secondary antibody (Dako Chem Mate Envision
sacrococcygeus posterior muscle and the dorsolateral surface Kit, Dako) was labeled with horseradish peroxidase (HRP),
of the coccygeus muscle. Does the SSL develop from an and antigen-antibody reactions were detected via an HRP-
intermuscular fascial structure? Consequently, to consider the catalyzed reaction with diaminobenzidine, followed by
possibility of coordinated development and growth between counterstaining with hematoxylin.
muscle and ligament, the aim of this study was to clarify
the development of these two muscle and ligament pairs in Results
human fetuses.
Supinator muscle and the ANL
Materials and Methods At 10 weeks, although it was still composed of loose
fibrous tissue, the ANL was already evident in the deep side
The study was performed in accordance with the provis­ of the anconeus (Fig. 1). The supinator muscle originated
ions of the Declaration of Helsinki 1995 (as revised in from a ridge of the cartilagenous ulna via a long distinct
Edinburgh, 2000). We examined the histology of paraffin- tendon (Fig. 1A, B). Notably, at a more proximal level, the
embedded specimens of 1) 15 mid-term human fetuses supinator tendon became thicker and was continuous with

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Development of ligaments and muscles Anat Cell Biol 2013;46:149-156 151

Fig. 1. Early-stage development of the annular ligament of the radius. A

10-week fetus (crown-rump length, 55 mm). Cross-sections of the elbow.
Hematoxylin and eosin staining (A and C) and silver staining (B). Panel
(A) (panel C) is the most distal (proximal) side of the figure. Intervals
between panels are 0.1 mm (A−B, B−C). The supinator muscle originates
from a ridge (open star) of the ulna via a long tendon (arrowheads in A
and B). At levels between (B) and (C), this tendon is continuous with the
primitive annular ligament of the radius (arrows in C). Outside the tendon
and ligament, there is an intermuscular fascia (black stars) connecting the
extensor carpi radialis (ECR) and anconeus muscles: this fascia is much
thinner than the primitive annular ligament. BR, brachioradialis muscle.
Scale bar in (A) =1 mm (A−C).

the ANL. In the superficial side of the tendon and ligament, muscle (Fig. 3). However, some muscle fibers of the coccygeus
an intermuscular fascia extended between the extensor carpi were already embedded in the loose ligament (Fig. 3C, D).
radialis and anconeus muscles: this fascia was much thinner The primitive ligament was not yet connected with the
than the ANL. However, at 12−15 weeks, the intermuscular sacrum. The sacrococcygeus posterior muscle [16] appeared
fascia became thick, and at 18 weeks, it was much thicker to have already united with the coccygeus. At 28 weeks, the
than the ANL (Fig. 2). Thus, near the origin from the ulna, obturator internus muscle was very thick and extended more
the supinator muscle fibers were sandwiched by the ANL and posteriorly than the tendon curving along the ischium. The
the intermuscular fascia or band (Fig. 2B, D). At 18 weeks, tendinous arch of the levator ani muscle was long and loose.
the supinator tendon was tightly attached to the ANL and the An intramuscular tendon was evident in the coccygeus
tendon was difficult to discriminate from the ligament. Parts muscle, and this extended outside the muscle along the inferior
of the supinator muscle were still attached to the head of the aspect (Fig. 4). Near the tendon, some muscle fibers of the
radius. We observed several thick muscle fibers with multiple coccygeus were much thicker than others and had lost their
nuclei in the supinator along the head of the radius (Fig. 2F). myotube morphology (Fig. 4E). The sacrotuberous ligament
At 22 weeks, both the ANL and supinator muscle were well was well developed near the ischial tuberosity at 28 weeks, but
developed. The thick and tight ANL contained several long appeared to connect between the gluteus maximus muscle
muscle fibers originating from the supinator muscle (data not and the tuberosity (Fig. 4D). At 31 weeks, the intramuscular
shown). tendon of the coccygeus muscle was connected with the
growing sacrotuberous ligament (Fig. 5). In the postero-
Coccygeus muscle and the sacrospinous ligament inferior margin of the coccygeus muscle, we found a thick
At 18 weeks, the SSL was identified as a loose fibrous band bundle of collagenous fibers, which corresponded to the final
that appeared to be an insertion tendon of the coccygeus SSL (Fig. 5D) in view of its topographical relationship with

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152 Anat Cell Biol 2013;46:149-156 Shogo Hayashi, et al

Fig. 2. Later development of the annular ligament of the radius. An 18-week fetus (crown-rump length, 155 mm). Cross-sections of the elbow.
Panel (A) (panel E) is the most distal (proximal) side of the figure. Panels (B), (D), and (F) are higher-magnification views of the squares in panels
(A), (C), and (E), respectively. Hematoxylin and eosin staining (A, C, E, F), Masson trichrome staining (D; adjacent section to panel C), and
immunohistochemistry for desmin (B; adjacent section to panel A). Intervals between panels are 0.1 mm (A−C) and 0.5 mm (C−E). In contrast
to Fig. 1, the intermuscular fascia (black stars in B and D) connecting the extensor carpi radialis (ECR) and anconeus muscles is much thicker than
the annular ligament facing the head of the radius (arrows in B and D). At the side near the origin from the ulna, the supinator muscle fibers are
sandwiched by the annular ligament and the intermuscular fascia (B, D). The tendon of the supinator has already become incorporated into the
ligament. In the supinator facing the head of the radius, a thick muscle fiber with multiple nuclei is seen (arrows in F). BR, brachioradialis muscle.
Scale bars=1 mm (A, C, E), 0.5 mm (B, D), 0.1 mm (F).

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Development of ligaments and muscles Anat Cell Biol 2013;46:149-156 153

Fig. 3. Initial development of the sacrospinous ligament. An 18-week fetus (crown-rump length, 155 mm). Horizontal sections of the pelvis. Upper
side of each panel corresponds to the anterior side of the pelvis. Panel (A) is 0.1 mm superior to panel (B) (A and B, hematoxylin and eosin [H&E]
staining). Panel (C, desmin immunohistochemistry) displays an adjacent section to panel (B). Panel (D, H&E staining) is a higher-magnification
view of a square in panel (B). The primitive sacrospinous ligament (stars in A and B) is a loose fibrous bundle that appears to be an insertion tendon
of the coccygeus muscle. However, some muscle fibers are embedded in the ligament (arrows in C; higher magnification, D). The ligament has not
yet connected with the sacrum. LA, levator ani muscle; OI, obturator internus muscle; PN, pudendal nerve. Scale bars in (A)=1 mm (A−C), in
(D)=0.1 mm (D).

the sacrotuberous ligament. The SSL contained irregularly became the SSL. Moreover, in the ANL and SSL, muscle
arrayed muscle fibers (Fig. 5E). fibers embedded in the ligaments suggested degeneration,
or at least impairment of function. In fact, macrophage
Discussion accumulation has been reported in the fetal ANL at a similar
stage [19]. Thus, at these two sites, ligament growth appears
Many ligaments in the human body do not apparently not to be “favorable” for the developing muscles, in contrast
develop in association with muscle development. A typical to the coordinated development and growth that has been
example of such independent development and growth is the hypothesized (see Introduction). The fetal supinator was very
alar and transverse atlantis ligaments at the craniovertebral thick relative to the size of the elbow. Thus, even if the ANL
junction [18]. However, the ANL and SSL appeared to be remained thin during development, the supinator muscle
different. The present observations demonstrated that, in appeared to stabilize the growing head of the radius in utero.
human fetuses, 1) proximal parts of the supinator muscle Likewise, even if the SSL was absent, development of the fetal
were embedded in the collagenous tissue when the developing sacroiliac joint appeared to be not impaired. Therefore, fetal
ANL joined the thick intermuscular connecting band and 2) growth of the ANL or SSL may occur independently from,
the anterior parts of the coccygeus muscle were surrounded or even beyond, functional demand at the corresponding
by this collagenous tissue when the intramuscular tendon joint. Although muscle contraction is likely to induce

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154 Anat Cell Biol 2013;46:149-156 Shogo Hayashi, et al

initial development of the ANL and SSL, the two appear to

paradoxically injure parts of the “mother” muscles.
Reidenbach and Schmidt [13] stated that the ANL
develops in stages in fetuses with a CRL between 105 and 270
mm, but considered that the term “growth” was preferable to
“development.” In the present study, we paid close attention to
the early stage of development. According to Mérida-Velasco
et al. [12], the first signs of the ANL are evident at 7 weeks,
and the joint capsule becomes anchored to the ligament at 9
weeks. The thick intermuscular connecting band we observed
at the elbow most likely corresponded to the lateral ulnar
collateral ligament in adults described by O’Driscoll et al. [20],
Hannouche and Bégué [21] and Imatani et al. [22]. Thus, at
15−18 weeks, the so-called lateral collateral ligament complex
of the elbow [23] seemed to develop, with subsequent
thickening of the ANL. In a study involving dissection from
the superficial to the deep side of the elbow including the
anconeus and extensor carpi ulnaris muscles, Kim et al.
[24] published many elegant images of the lateral collateral
ligament complex. In spite of its rather late development,
the ANL in adults became much stronger than the ligament
complex. Hast and Perkins [25] reported a cadaveric elbow
showing rare anomalies: the accessory supinator and tensor
muscles. Because these anomalous muscles were similar to the
present supinator fibers embedded in the ANL, these muscles
may result from failure of the muscle fibers to become
involved in the ANL.
Development of the SSL chronologically followed
the formation of the initial sacrotuberous ligament. The
sacrotuberous ligament appeared to begin its development
as a tendon of the gluteus maximus temporarily inserted to
the ischial tuberosity. In adults, the gluteus maximus is, in
fact, tightly attached to the tuberosity. In contrast, the SSL
Fig. 4. Intramuscular tendon of the coccygeus connecting with the is much weaker than the sacrotuberous ligament, although
sacrotuberous ligament. A 28-week fetus (crown-rump length, 230
mm). Sagittal sections of the pelvis. hematoxylin and eosin staining. both are considered critical for stabilizing the sacroiliac joint
Panel (A) (panel D) is the most medial (lateral) side of the figure. The [26-28]. Because of the long and loose tendinous arch of the
left-hand side of each panel corresponds to the anterior side of the levator ani muscle in fetuses, the growth and contraction
pelvis. Intervals between panels are 1.0 mm (A−B), 0.8 mm (B−C),
and 0.6 mm (C−D), respectively. Panel (E) is a higher-magnification
of the fetal rectum appears to not create mechanical stress
view of a square in panel (D). The primitive tendinous arch (arrowheads on the coccygeus and its intramuscular tendon (i.e., the
in B) of the levator ani (LA) muscle extends anteriorly to reach the primitive SSL). In any event, development of both the SSL
obturator internus muscle (OI). An intramuscular tendon is evident
and the sacrotuberous ligament appears to not stabilize the
in the coccygeus muscle and along the inferior aspect of the muscle
(arrows in B−D). Near the tendon, some muscle fibers of the coccygeus fetal sacroiliac joint, but occurs as a result of mechanical
are thick and have lost their tube-like appearance (arrows in E). The influence from the nearby muscles. In the present study, the
developing sacrotuberous ligament (STL) has been partly damaged intramuscular tendon of the coccygeus appeared to provide
during histological preparation (asterisk in C). PN, pudendal nerve.
Scale bars in (A)=2 mm (A−D), in (E)=0.05 mm (E). a primitive form of the SSL. The union of the fetal coccygeus
muscle with the sacrococcygeus posterior muscle [16] may

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Development of ligaments and muscles Anat Cell Biol 2013;46:149-156 155

Fig. 5. Sacrospinous ligament appearing along the inferior margin of the coccygeus
muscle. A 31-week fetus (crown-rump length, 255 mm). Sagittal sections of the pelvis.
hematoxylin and eosain staining. Panel (A) (panel D) is the most medial (lateral) side
of the figure. Intervals between panels are 1.2 mm (A−B), 1.6 mm (B−C), and 0.4 mm (C−
D). Panel (E) is a higher-magnification view of the square in panel (D). The left-hand side
of (A−C) corresponds to the anterior side of the pelvis, while that of panel (D) corresponds
to the inferior side. The intramuscular tendon of the coccygeus muscle (arrows in C) is
connected with the developing sacrotuberous ligament (STL). The sacrospinous ligament
appears along the inferior margin of the coccygeus muscle (filled stars in D) and contains
irregularly arrayed muscle fibers (open stars in E). LA, levator ani muscle; OI, obturator
internus muscle. Scale bars=2 mm (A−D), 0.1 mm (E).

induce formation of the intramuscular tendon. Health & Welfare, Republic of Korea.
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