THE ANATOMICAL RECORD 298:1282–1293 (2015)

Fetal Development of the Human Obturator Internus Muscle With Special Reference to the Tendon and Pulley MICHIKO NAITO,1 RYOJI SUZUKI,2 HIROSHI ABE,2* JOSE FRANCISCO RODRIGUEZ-VAZQUEZ,3 GEN MURAKAMI,4 1 AND SHIN AIZAWA 1 Department of Anatomy, Nihon University School of Medicine, Tokyo, Japan 2 Department of Anatomy, Akita University Graduate School of Medicine, Akita, Japan 3 Department of Anatomy and Human Embryology II, Complutense University, Madrid, Spain 4 Division of Internal Medicine, Iwamizawa Kojin-Kai Hospital, Iwamizawa, Japan

ABSTRACT To examine the development of the tendon pulley of the obturator internus muscle (OI), we observed paraffin sections of 26 human embryos and fetuses (6–15 weeks of gestation). The OI was characterized by early maturation of the proximal tendon in contrast to the delayed development of the distal tendon. At 6 weeks, the ischium corresponded to a simple round mass similar to the tuberosity in adults. At 8 weeks, before development of the definite lesser notch of the ischium, initial muscle fibers of the OI, running along the antero-posterior axis, converged onto a thick and tight but short tendon running along the left-right axis. Thus, at the beginning of development, the OI muscle belly and tendon met almost at a right angle. At 10 weeks, the OI tendon extended inferiorly along the sciatic nerve, but the distal part remained thin and loose and it was embedded in the gluteus medius tendon. At 15 weeks, in association with the gemellus muscles, the distal OI tendon was established. The mechanically strong sciatic nerve was first likely to catch the OI muscle fibers to provide a temporary insertion. Next, the ischium developing upward seemed to push the tendon to make the turn more acute along the cartilaginous ridge. Finally, the gemellus muscle appeared to provide inferior traction to the OI tendon for separation from the gluteus medius to create the final, independent insertion. Without such guidance, the piriformis tendon first attached to the OI tendon and then merged C 2015 with the gluteus medius tendon. Anat Rec, 298:1282–1293, 2015. V Wiley Periodicals, Inc.

Key words: obturator internus muscle; tendon pulley; ischium; gemellus muscles; piriformis muscle; sciatic nerve; human fetus

The deep rotator muscles of the hip joint, the obturator internus (OI), quadratus femoris and gemellus muscles, have been of interest to anatomists because of the dual nerve supply to the gemelli, one part being innervated by the OI nerve running ventrally to the muscles, and the other by the quadriceps femoris nerve running dorsally (Kikuchi, 1987; Honma et al., 1998; Aung et al., 2001). In contrast, few anatomists appear to C 2015 WILEY PERIODICALS, INC. V

*Correspondence to: Dr. Hiroshi Abe, Department of Anatomy, Akita University Graduate School of Medicine, Hondo 1-1-1, Akita-city, 010-8543, Japan. E-mail: [email protected] Received 29 August 2014; Accepted 26 November 2014. DOI 10.1002/ar.23121 Published online 25 February 2015 in Wiley Online Library (wileyonlinelibrary.com).

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ischium), Gr€ afenberg (1904) and Bardeen (1907) postulated that the muscle attachment undergoes migration (Fig. 1E). However, attachment of striated muscle fibers to hard tissue does not involve simple interdigitation of collagen fibers, but multiple proteins during the process of fetal development (Heydemann and McNally, 2009; Abe et al., 2010). Thus, in the OI, migration of muscle fiber attachment would seem to be difficult. If the OI tendon changes its direction due to a drastic topographical change in the bony pelvis (Fig. 1D), this might be easily confirmed by observations of the early topographical anatomy of the pelvis and femur. Consequently, using human embryonic and fetal specimens (6–15 weeks of gestation), the aim of this study was to clarify the morphology of the fetal muscle insertions in the small intertrochanteric area of the femur.

MATERIALS AND METHODS

Fig. 1. Hypothetical models to explain the development of the hard tissue pulley for muscle tendon. Panel A displays secondary attachment of bone or cartilage (circle) to form a tendon pulley due to migration of the target (square) of tendon insertion (e.g., the trochlea and the hamulus; Katori et al., 2011b). Panel B displays secondary migration of bone or cartilage (circle) to form a tendon pulley (no known examples). Panel C demonstrates pulley formation due to a change in the course of a tendon in association with a change of target for tendon insertion (e.g., the digastricus; Katori et al., 2011a). Panels D and E display modes of formation of the pulley for the obturator internus tendon. In Panel D, a marked change in topographical relationships would be expected among the bony components of the pelvis and femur: a linear relationship between the femur and the inner aspects of the small pelvis allows a straight course for the obturator internus tendon (left side of panel D). Panel E shows the migration of muscle attachment from the extrapelvic site to the intrapelvic site hypothe€fenberg (1904) and Bardeen (1907). OI and OE, obturator sized by Gra internus and externus muscles.

have commented on the triceps muscle-like appearance of the OI and gemelli (Shinohara, 1995). In the context of human anatomy, our group has described a further example in which a short muscle “catches” the long tendon of a larger muscle, that is, the anterior belly of the digastricus muscle inserting into the early developing tendon of the posterior belly (Katori et al., 2011a). Topographical relationships among the deep rotator muscles at the fetal stage have not been well described because, rather than focusing on the tendon, previous researchers have sought the sites of muscle anlagen at an early stage of development (Gr€ afenberg, 1904; Bardeen, 1907). The hard tissue pulley, a curved surface formed by bone or cartilage to allow a tendon to change its direction, seems to develop in various ways (Fig. 1). According to Katori et al. (2011b), migration of the target of a tendon insertion (Fig. 1A) is critically important for development of the pulley for the superior obliquus muscle tendon of the eye (delayed rotation of the eyeball) as well as the tensor veli palatini muscle tendon (delayed posterior shift of the palate). The posterior belly of the digastricus (see the paragraph above) exhibits a change in target, as shown in Fig. 1C (Katori et al., 2011a). For development of the OI pulley (a lesser notch of the

The study was performed in accordance with the provisions of the Declaration of Helsinki 1995 (as revised in Edinburgh, 2000). We observed semiserial or serial paraffin sections of 5 human embryos at 6 weeks of gestation [crown-rump (CRL) 15–22 mm] and 21 human fetuses at 8–15 weeks (7 specimens at 8 weeks, CRL 28– 35 mm; 6 at 10 weeks, CRL 45–55 mm; 8 at 15 weeks, CRL 100–118 mm). All of the sections were stained with hematoxylin and eosin. The sectional plane was sagittal (3 specimens at 6 weeks; 5 at 8 weeks; 1 at 10 weeks; 2 at 15 weeks), horizontal (1 specimen at 6 weeks; 1 at 8 weeks; 3 at 10 weeks; 4 at 15 weeks) or frontal (1 specimen at 6 weeks; 1 at 8 weeks; 2 at 10 weeks; 2 at 15 weeks). All of the present 26 specimens were part of the large collection kept at the Institute of Embryology, Universidad Complutense Madrid, and were products of miscarriages and ectopic pregnancies managed at the Department of Obstetrics at the university. The study protocol was approved by our university ethics committee (No. B08/374). Our previous studies had used the head and neck and abdominal regions of the same embryos (Rodrıguez-V azquez Jet al., 2011; Hayashi et al., 2011), and none were found to have any anomalies.

RESULTS At 6 weeks, the femoral, obturator and sciatic nerves were already well developed. The sacrum, ilium, pubis and femur were cartilaginous and easily discriminated from each other (Fig. 2), but the greater and lesser trochanters were not developed. The primitive, plate-like acetabulum, formed by the pubis and ilium, met the femur almost at a right angle. The ischium was identifiable as a round mass distant from the initial acetabulum and it appeared to be located at a position similar to the ischial tuberosity in adults. A connection of mesenchymal condensations between the ilium and ischium was seen in 2 of the 5 specimens examined. At and around the hip joint, candidate striated muscle fibers, colored pink due to positivity for eosin, were identified as several masses: (1) a long slender mass along the course of the femoral nerve in front of the pelvis (iliacus; Fig. 2A); (2) a small mass between the courses of the obturator and sciatic nerves medial to the femur (adductors; Fig. 2F); (3) a slender or oval mass anterior to the femur (quadriceps femoris; Fig. 2A), (4) a large round or oval

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Fig. 2. Early topographical anatomy at and around the hip joint in a 17-mm-CRL embryo (6 weeks). Sagittal sections. HE staining. All panels are prepared at the same magnification (scale bar in panel H). Panel A (or panel H) is the most lateral (or medial) in the figure. Intervals between panels are 0.2 mm (A,B), 0.1 mm (B–C, C–D, D–E, E–F, F–G) and 0.2 mm (G–H). In panels A–C, the pubis (P) and ilium (IL) form a plate-like acetabulum to receive the femoral head (F). In contrast, the initial ischium (IS) is distant from the femur (panels F–H). The femoral, obturator, and sciatic nerves (FN, ON, SN) are well devel-

oped. Muscle anlagen are identified as eosinophilic fiber bundles for the iliacus (ILM), quadriceps femoris (Q), adductors (AD), hamstrings or the supplying nerve (H), gluteus medius (GM) and gluteus maximus (GMX). Superior to the ischium (arrowhead in panels F–H), an anlage of the obturator internus is vaguely identifiable. cord, sacral spinal cord; CPN, common peroneal nerve; DRG, dorsal root ganglion; FI, fibula; K, definite kidney (metanephros); M, mesonephros; S, sacral vertebrae T, tibia.

mass in posterolateral to the femur and attached to the initial ischium or ischial tuberosity (gluteus maximus; Fig. 2A,B); (5) a long slender mass along the course of the sciatic nerve behind the pelvis (gluteus medius; Fig. 2A,B) and, (6) a round or oval mass inferior or distal to

the ischial tuberosity (hamstring muscles; Fig. 2H). There were no muscle fibers along the flat superior or inner aspect of the pelvis. At 8 weeks (Figs. 3 and 4), the pubis, ischium and ilium together provided a cup-like acetabulum to receive

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Fig. 3. Initial development of the obturator internus muscle and tendon in a 27-mm-CRL fetus (8 weeks). Sagittal sections. HE staining. All panels are prepared at the same magnification (scale bar in panel I). Panel A (or Panel I) is the most medial (or lateral) in the figure. Intervals between panels are 0.05 mm (A–B), 0.1 mm (B–C, C–D, D–E, E– F), 0.3 mm (F–G, G–H) and 0.2 mm (H–I). In panels A and B, eosinophilic muscle fibers of the obturator internus (OI) converge onto a relatively thick tendon (star). While maintaining its thickness and density, the tendon runs laterally along the sciatic nerve (SN; panels C–G) and merges with the thick tendon of the gluteus medius (GM in panel H).

The pubis (P), ischium (IS) and ilium (IL) together form a cup-like acetabulum to receive the femoral head (F in panel F). The piriformis muscle (PI) and its tendon (PIT) also run laterally to merge with the gluteus medius tendon (panels C–G). The tendons of the gluteus medius and iliacus (ILM) surround the femoral head (panels H and I). The greater trochanter of the femur is developing (arrowhead in panel I), but the lesser trochanter is not. AD, adductors; CX, coccygeus muscle; FN, femoral nerve; GMI, gluteus minimus muscle; GMX, gluteus maximus muscle; OE, obturator externus muscle; ON, obturator nerve; PM, psoas major muscle; S, sacral vertebrae; SA, sciatic artery candidate.

the femoral head. Eosinophilic muscle fibers of the OI were consistently seen converging posteriorly onto a short thick tendon attached to the thick sciatic nerve (Figs. 3A and 4A). A cluster of the OI muscle fibers formed a plate-like muscle belly along the sagittal plane

more than 0.5 mm medial to the femoral head. Thus, both the OI muscle belly and tendon were distant from the femur at this initial stage. The obturator externus muscle, larger than the OI, was located 0.3–0.8 mm medial to the latter and extended inferiorly to the femur

Fig. 4. Initial development of the obturator internus muscle and tendon in a 28-mm-CRL fetus (8 weeks). Sagittal sections. HE staining. All panels are prepared at the same magnification (scale bar in panel L). Panel A (or Panel L) is the most medial (or lateral) in the figure. Intervals between panels are 0.1 mm (A–B, B–C, C–D, D–E), 0.3 mm (E–F), 0.1 mm (F–G), 0.2 mm (G–H, H–I) and 0.1 mm (I–J, J–K, K–L). In panels A and B, eosinophilic muscle fibers of the obturator internus (OI) converge onto a relatively thick tendon (star). While maintaining its thickness and density, the tendon runs laterally along the sciatic nerve (SN; panels B–G), but becomes thin and sparse along the sciatic

nerve before reaching the femoral head (panels H–K). The piriformis muscle (PI) and its tendon (PIT) follow the course of the obturator internus tendon (panels E–K). Thick tendons of the gluteus medius (GM) and iliacus (ILM) surround the femoral head (panels K and L). The lesser trochanter is developing (arrowhead in panel L). The tendon of the obturator externus (OE in panels I–K) appears to reach the greater trochanter (GT). AD, adductors; EIA, external iliac artery; F, femoral head; GMI, gluteus minimus muscle; GMX, gluteus maximus muscle; IL, ilium; IS, ischium; ON, obturator nerve; P, pubis; PM, psoas major muscle; SA, sciatic artery candidate; UA, umbilical artery.

FETAL DEVELOPMENT OF THE HUMAN OBTURATOR INTERNUS MUSCLE

Fig. 5.

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head. Notably, in spite of the relatively sparse muscle fibers in the muscle belly, the OI tendon tissue was composed of tightly packed collagenous fibers, as in the tendons of the gluteus medius and iliacus (i.e., large muscles starting their development at 6 weeks). Moreover, the short tendon directed along the left-right axis met the muscle fibers at almost a right angle. The cartilaginous pulley or the lesser notch of the ischium was not identified, but the ischium issued two upward extensions to connect with the ilium and pubis, respectively. Thus the ischium contributed to formation of the acetabulum. While maintaining its thickness and tightness, the OI tendon took a short lateral course along the sciatic nerve (Figs. 3C–E and 4C–F). However, at more inferolateral sites, the tendon tissue became sparser and ended at the surface of the gluteus medius tendon (Figs. 3H and 4H–K). Likewise, the piriformis tendon ran along the sciatic nerve slightly (0.3–0.5 mm) superior to the OI tendon, attaching to the OI tendon and merging with the gluteus medius tendon (Figs. 3G and 4J). The long tendons of the gluteus medius and iliacus, surrounding the femoral head, met anterior to the femur (Figs. 3H and 4K,L). The greater trochanter of the femur was developing, but the lesser trochanter was not. At 10 weeks, a distinct cartilaginous pulley was identifiable as a postero-inferior ridge of the ischium in horizontal and frontal sections (Figs. 5 and 6), but sagittal sections showed a shallow notch on the ridge (figures not shown). Thus, at this stage, the cartilaginous pulley carried an acute edge rather than the dull, curved surface. Around the hip joint, every muscle and tendon was clearly identifiable. The tendons of the hamstring muscles were particularly thick (Fig. 5F). The OI tendon, after changing its direction at the pulley, ran inferolaterally along the sciatic nerve. The medially located tendon was tightly attached to the laterally located nerve. Superior and posterosuperior to the femoral head, the OI tendon was attached to and embedded in the gemellus muscles (Figs. 5D,E and 6C). Herein, the muscle fibers proximal or superior to the OI tendon were tentatively identified as the gemellus superior, while those near the quadratus femoris muscle were identified as the gemellus inferior. The composite collagenous fibers of the OI tendon became sparser along their distal course toward the greater trochanter (Figs. 5E,F and 6G,H). The piriformis tendon ran downward near the OI tendon (Figs. 5D,E and 6G,H) and merged with the gluteus medius tendon (Fig. 6I). The intra- and extra-muscular tendons of the obturator externus muscle were much more evident than the OI tendon (Figs. 6B and 7A). At 15 weeks, the composite fibers of the distal part of the OI tendon were tightly packed, similarly to those of the gluteus medius and hamstrings muscles (Figs. 7L,M and 8G,H). However, the composite fibers were still Fig. 5. Obturator internus and gemellus muscles in a 45-mm-CRL fetus (10 weeks). Horizontal sections of the hip in a flexed position. HE staining. Panels A–F or Panels G–I are prepared at the same magnification (scale bars in panels F and H). Panels G–I are highermagnification views of the obturator internus tendon shown in panels C, E and F, respectively. Panel A (or Panel F) is the most superior (or inferior) in the figure. Intervals between panels are 0.5 mm (A–B), 0.3 mm (B–C), 0.2 mm (C–D, D–E) and 0.1 mm (E–F). In panels A and B, a tendon (star) of the obturator internus muscle (OI) changes its direction at the pulley formed by the ischium (IS). The tendon is

more densely packed in the proximal area near the pulley than in the distal part. In two of eight specimens at this stage, the distal OI tendon retained an early morphology (a mesenchymal condensation or loosely packed fibers). The multiple intramuscular tendons of the OI joined together to create a single thick tendon: not only the single tendon but also the intramuscular tendons were attached to the cartilaginous pulley (Fig. 7G). A distinct notch along the ischium was evident in sagittal sections (Fig. 7D), but unclear in horizontal and frontal sections (Fig. 8C). The gemellus muscles were considerably larger than those at 10 weeks. The gemellus superior muscle was attached to both the piriformis tendon and the belly of the OI muscle (Fig. 8C,D), while the gemellus inferior muscle was attached to the quadratus femoris muscle (Figs. 7I,J). The gemellus inferior muscle contained a definite intramuscular tendon (Fig. 8H,I). The gemellus muscles had a thick fascia facing the sciatic nerve (Fig. 8D,E). The piriformis tendon was attached to the terminal part of the gluteus medius (Figs. 7K and 8A) and joined the gluteus tendon (Figs. 7L and 8G,H). The obturator externus muscle carried a thick tendon that was extending toward the femur (Fig. 7L,M). Consequently, forming a right angle, both the OI muscle belly and tendon started both developing together at 8 weeks. In contrast to the proximal part of the tendon, delayed development of the distal part was evident (Table 1). The development of the gemellus muscles appeared to parallel with the maturation of the OI tendon. The piriformis tendon took a long course along the sciatic nerve, but it exhibited developmental delay because, at 15 weeks, it was still involved with the gluteus medius tendon. These observations are summarized in Fig. 9. In addition, the present observations of the bony pelvis and hip joint were generally consistent with those of Gardner and Gray (1950), although this aspect is beyond the focus of the present study.

DISCUSSION The most striking feature revealed by the present observations was, at the initial phase (8 weeks), sparse developing muscle fibers of OI existed with the short but distinct tendon. Moreover, the fiber directions were controversial between the muscle and tendon: anteroposteriorly running muscle fibers in contrast to the mediolateral running tendon fibers. Thus, at the initial stage, the muscle fibers and tendon met almost at a right angle. However, other than the sciatic nerve, there appeared to be no distinct structure guiding or receiving the initial tendon. Tensile stress from the muscle belly is essentially important for the development and maintenance of tendon morphology (Kjaer et al., 2009, 2006; Mackey et al., 2008). We attached to and embedded in the gemellus inferior muscle (GI in panels C-E). Composite collagenous fibers of the tendon appear to disperse in panels H and I. The piriformis muscle (PI) issues a long tendon (PIT) running between the obturator internus tendon and the gluteus medius tendon (GMT, panels B–I). AD, adductors; F, femoral head; GM, gluteus medius muscle; GMX, gluteus maximus muscle; H, hamstring muscles; LA, levator ani muscle; OE, obturator externus muscle; P, pubis; QF, quadratus femoris muscle; R, rectum; S, sacral vertebrae; SN, sciatic nerve.

FETAL DEVELOPMENT OF THE HUMAN OBTURATOR INTERNUS MUSCLE

Fig. 6. Obturator internus and gemellus muscles in a 55-mm-CRL fetus (10 weeks). Horizontal sections. HE staining. Panels A and B, and panels C–I, are prepared at the same magnification (scale bars in panes A, B and I). Panel A (or Panel I) is the most superior (or inferior) in the figure. Intervals between panels are 0.3 mm (A–B), 0.05 mm (B–C), 0.2 mm (C–D, D–E, E–F, F–G, G–H) and 0.1 mm (H–I). In panel A, a tendon (star) of the obturator internus muscle (OI) changes its direction at the pulley formed by the ischium (IS). The tendon is attached to the sciatic nerve

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(SN in panel B) and embedded in the gemellus superior and inferior muscles (GS and GI in panel C). Composite collagenous fibers of the tendon become sparse near the greater trochanter (GT in panels C–I). The piriformis tendon (PIT) is thin and joins the gluteus medius tendon (GMT, panels F–I). IS with parenthesis in panel A indicates a roof-like process of the ischium. GMX, gluteus maximus muscle; LA, levator ani muscle; OE, obturator externus muscle; P, pubis; PI, piriformis muscle; QF, quadratus femoris muscle; S, sacral vertebrae.

Fig. 7. Maturation of the obturator internus tendon in a 102-mmCRL fetus (15 weeks). Sagittal sections. HE staining. Panels A–D, panels E–H, L and M, and panels I–K are prepared at the same magnification, respectively (scale bars in panels D, E and I–M). Panel A (or Panel M) is the most medial (or lateral) in the figure. Panels E–H display higher-magnification views of the obturator internus tendon in panels A–D, respectively. Intervals between the panels are 0.1 mm (A– B), 0.3 mm (B–C), 0.2 mm (C–D), 4.5 mm (D–I), 0.4 mm (I–J), 0.1 mm (J–K), 1.2 mm (K–L), and 0.8 mm (L–M). A tendon (star) of the obturator internus muscle (OI), arising from multiple intramuscular tendons (panel G), changes its direction at the developing notch of the ischium (IS; panels C and D). The tendon courses inferolaterally along the sci-

atic nerve (SN in panels I–K) and becomes embedded in the superior and inferior gemellus muscles (GS and GI in panels I and J). Composite collagenous fibers of the tendon become sparse near the greater trochanter (GT in panel M). The piriformis tendon (PIT) follows the obturator internus tendon (panels I–K) and joins the gluteus medius tendon (GMT in panel L). The piriformis tendon attaches to the gemellus superior muscle (panel K). BL, urinary bladder; F, femoral head; GM, gluteus medius muscle; GMX, gluteus maximus muscle; H, hamstring muscles; LA, levator ani muscle; OE, obturator externus muscle; OET, obturator externus tendon; P, pubis; PI, piriformis muscle; QF, quadratus femoris muscle; S, sacral vertebrae; UR, ureter.

Fig. 8. Maturation of the obturator internus tendon in a 118-mmCRL fetus (15 weeks). Frontal sections. HE staining. Panel A displays the topographical anatomy at and around the pulley at lower magnification, while panels B–I (all at the same magnification) show highermagnification views of the obturator internus tendon (scale bars in panels A and D). Panels A and B show the same section. Panel A (or Panel I) is the most anterior (or posterior) in the figure. Intervals between the panels are 0.5 mm (A–C, C–D, D–E, E–F, F–G), 0.7 mm (G–H) and 0.2 mm (H–I). The obturator internus tendon (star) is composed of tightly packed collagenous fibers in panel B, but the fibers becomes sparse near the greater trochanter (panels E–I). The gemel-

lus muscles (GS, GI) have a thick fascia (arrows in panels D and E) facing the sciatic nerve (SN). The gemellus inferior muscle (GI) inserts into the obturator internus tendon with a definite tendon (arrows in panels H and I). A nerve appears to run toward the superior gemellus muscle (panels B and C). The piriformis tendon (PIT) follows the obturator internus tendon and joins the gluteus medius tendon (GMT; panels D–H). FN, femoral nerve; GM, gluteus medius muscle; GMI, gluteus mimimus muscle; GMX, gluteus maximus muscle; GT, greater trochanter; IL, ilium; ILM, iliacus muscle; IS, ischium; OI, obturator internus muscle; PM, psoas major muscle; QF, quadratus femoris muscle; R, rectum.

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TABLE 1. Specific development of the obturator internus muscle and tendon: a comparison with nearby muscles

20 mm CRL (6 weeks) 30 mm CRL (8 weeks) 50 mm CRL (10 weeks) 100 mm CRL (15 weeks)

Obt internus

Gemellus

Obt externus

Glut med

M– T2 M 1 or 6 T prox 1, dist M1 T prox 1, dist 6 M1 T prox 1, dist 1

M– T2 M– T2

M– T2 M1 T6

M6 T2 M1 T1

M1 T2

M1 T1

M1 T1

M1 T1

M1 T1

M1 T1

CRL and weeks, crown-rump length and the approximate gestational age. Obt, obturator; Gemellus, gemellus inferior muscle; Glut med, gluteus medius. M, observations of muscle belly; M 6, a few fibers suggesting striated muscles. T prox or dist, observations of the proximal or distal part of the tendon. T 6, tendon comprising of a loosely packed fibrous tissue.

Fig. 9. Diagram showing the hypothetical process of development of the obturator internus tendon. The obturator internus muscle (OI) is characterized by early maturation of the proximal tendon, in contrast to the delayed development of the distal tendon. At the beginning of development, the obturator muscle belly and tendon meet almost at a right angle. The short tendon, comprising tightly packed collagenous fibers, appears to temporarily insert to the mechanically strong sciatic nerve (Panel A). Next, the obturator tendon extends inferiorly along the sciatic nerve (SN), while the ischium (IS) extends upward, pushing the tendon to make an acute turn (panel B). Finally, with the guidance of the gemellus muscles providing inferior traction to the obturator tendon, the obturator internus obtains its final insertion to the femur (F). Without such guidance, the unattached tendon of the piriformis (PI) would initially attach to the OI tendon and then merge with the thick tendon of the gluteus medius (GM).

speculated that, before formation of a distinct pulley, the thick nerve might catch (allow the attachment of) the tendon to receive the weak tensile force generated by the OI (Fig. 9A). A mechanically strong nerve is likely to become a temporary target for muscle insertion, for example, in the case of the hypoglossal nerve for the posterior belly of

the digastricus (Katori et al., 2011a). At 8–10 weeks, the OI tendon extended inferolaterally along the sciatic nerve, whereas the lesser notch of the ischium was sculptured by both of the OI muscle belly and tendon in association with the upward extension of the ischium (Fig. 9B). In fact, a thick fascia was consistently evident between the nerve and the OI tendon. Until 10 weeks, the final target seemed to be distant from the OI tendon. Delayed maturation of the distal part of the OI tendon was also a striking feature. The distal OI tendon maintained its early morphology (a mesenchymal condensation of loosely packed fibers) even at 15 weeks, in contrast to the tightly packed fibers in the proximal part of the tendon (Table 1). This clear regional difference was quite different from that in other muscles. As typically seen in the gluteus medius and iliacus muscles, the muscle tendon became more distinct nearer the insertion (distal part), and not near the muscle belly (proximal part). Generally, tendon development follows the development of the muscle belly in accordance with specific signaling pathways for tendons (Schweitzer et al., 2001; Murchison et al., 2007; Pryce et al., 2009), even though the muscle belly and tendon share a common cell lineage (Brent et al., 2005, 2003). Maturation of the distal part of the OI tendon should occur after 15 weeks, and may require muscle activity during postnatal life. What guides and brings the OI tendon from its temporary insertion to the sciatic nerve surface to the distant intertrochanteric fossa? Even at 15 weeks, we were unable to find any final insertion. Instead, the distal OI tendon ended at a site very close to the insertion of the gluteus medius tendon to the greater trochanter. We speculated that the gemellus muscles might play a role in guiding the OI tendon through its long downward path. The gemellus muscles became evident 2 weeks after development of the OI muscle began, and seemed to provide traction force along the supero-inferior axis to the OI tendon, even though development of the gemellus tendon

FETAL DEVELOPMENT OF THE HUMAN OBTURATOR INTERNUS MUSCLE

was limited in the inferior area until 15 weeks. To observe complete separation of the OI tendon from the gluteus medius tendon as development of the gemellus muscles proceeded, observation of later developmental stages would have been necessary. Similarly to the distal OI tendon, at 6–15 weeks of gestation, the piriformis tendon was not identifiable as a tight tissue cord, but as a mesenchymal condensation, a bundle of fibers, or merely a thick fascia. It crossed the roots of the sciatic nerve to enter the narrow anterior layer in which the OI tendon ran inferolaterally. However, even at 15 weeks, the piriformis tendon did not carry the proper insertion but merged with the gluteus medius tendon. In contrast to the OI tendon of which guidance cue was provided by the gemellus muscles, the piriformis tendon might not find its final insertion at least until 15 weeks in the fetal period. Subsequently, the piriformis tendon was first caught (and released) by the OI tendon and then by the gluteus medius tendon. In the later development, the piriformis tendon seemed to establish its proper insertion. Some anatomists have postulated that there is a correlation between the sacral level of the piriformis muscle anlage and the site at which the tendon passes through the sacral plexus (e.g., Chiba et al., 1994), but the tendon missing the insertion might pass between the sacral nerves without any rule. At the beginning of this article, we postulated several models to explain the development of hard tissue pulleys for tendons. In this series of specimens, the plate-like acetabulum met the femur at a right angle at 6 weeks. Thus, a drastic change (Fig. 1D) in the topographical relationship between the pelvis and the femur seemed unlikely. It is likely that the mechanically strong sciatic nerve would initially catch the OI muscle fibers to provide a temporary insertion (change of target; Fig. 1C). The ischium developing upward might then push the tendon to make the turn more acute. In fact, the cartilaginous pulley was initially not a notch but a ridge protruding posteriorly. This pushing by the ischium seemed to correspond to the migration of the pulley (Fig. 1B). Finally, the gemellus muscle appeared to provide inferior traction to the OI tendon for separation from the gluteus medius to make an independent insertion into the intertrochanteric fossa. We considered this guidance to be a variation of the model “target change” such as that seen for the anterior belly of the digastricus in catching the long tendon of the posterior belly: the muscle/muscles leads/lead the tendon to the final insertion. Consequently, the development of the OI pulley appears to be a process that involves a combination of models: a change of target and migration of the pulley.

LITERATURE CITED Abe S, Rhee SK, Osonoi M, Nakamura T, Cho BH, Murakami G, Ide Y. 2010. Expression of intermediate filaments at muscle insertions of human fetuses. J Anat 217:167–173. Aung HH, Sakamoto H, Akita K, Sato T. 2001. Anatomical study of the obturator internus, gemelli and quadratus femoris

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muscles with special reference to their innervation. Anat Rec 263:41–52. Bardeen RC. 1907. Development and variation of the musculature of the inferior extremity and of the neighboring regions of the trunk in man. Am J Anat 6:332–336. Brent AE, Braun T, Tabin CJ. 2005. Genetic analysis of intercalations between the somatic muscle, cartilage and tendon cell lineages during mouse development. Development 132:515–528. Brent AE, Schweitzer R, Tabin CJ. 2003. A somatic compartment of tendon progenitors. Cell 113:235–248. Chiba S, Ishibashi Y, Kasai T. 1994. Perforation of dorsal branches of the sacral nerve plexus through the piriformis muscle and its relation to changes of segmental arrangements of the vertebral column and others. Kaibougaku Zasshi 69:281–305. Abstract in English. Gardner E, Gray DJ. 1950. Prenatal development of the human hip joint. Am J Anat 87:163–211. Gr€ afenberg E. 1904. Die entwicklung der menschlichen beckenmusculature. Anat Hefte 72:429–494. Hayashi S, Rodrıguez-V azquez JF, Cho BH, Verdugo-L opez S, Murakami G, Nakano T. 2011. Pleuroperitoneal canal closure and fetal adrenal gland. Anat Rec 294:633–644. Heydemann A, McNally E. 2009. No more muscle fatigue. J Clin Investig 119:448–450. Honma S, Jun Y, Horiguchi M. 1998. The human gemelli muscles and their nerve supplies. Acta Anat Nippon 73:329–335. Katori Y, Kim JH, Rodriguez-Vazquez JF, Kawase T, Murakami G, Cho BH. 2011a. Early fetal development of the intermediate tendon of the digastricus and omohyoideus muscles: a critical difference in histogenesis. Clin Anat 24:843–852. Katori Y, Rodriguez-Vazquez JF, Kawase T, Murakami G, Cho BH, Abe S. 2011b. Early fetal development of hard tissue pulleys for the human obliquus superior and tensor veli palatini muscles. Ann Anat 193:127–133. Kikuchi T. 1987. A macroscopic observation of the nerves to the pelvic floor muscles, the obturator internus, the quadratus femoris and the gemelli. Sapporo Med J 56:319–332. In Japanese with English abstract. Kjaer M, Langberg H, Heinemeier K, Bayer ML, Hansen M, Holm L, Doessing L, Kongsgaard M, Krogsgaard MR, Magnusson SP. 2009. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports 19:500–510. Kjaer M, Magnusson P, Krogsgaard M, Boysen M?ller J, Olesen J, Heinemeier K, Hansen M, Haraldsson B, Koskinen S, Esmarck B, Langberg H. 2006. Extracellular matrix adaptation of tendon and skeletal muscle to exercise. J Anat 208:445–450. Mackey AL, Heinemeier KM, Koskinen SO, Kjaer M. 2008. Dynamic adaptation of tendon and muscleconnective tissue to mechanical loading. Connect Tissue Res 49:165–168. Murchison ND, Pryce BA, Conner DA, Keene DR, Olson EN, Tabin CJ, Schweitzer R. 2007. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscleanchoring tendons. Development 134:2697–2708. Pryce BA, Watson SS, Murchison ND, Staverosky JA, Dunker N, Schweitzer R. 2009. Recruitment and maintenance of tendon progenitors by TGFbeta signaling are essential for tendon formation. Development 136:1351–1361. Rodrıguez-V azquez JF, Kim JH, Verdugo-L opez S, Murakami G, Cho KH, Asakawa S, Abe S. 2011. Human fetal hyoid body origin revisited. J Anat 219:143–149. Schweitzer R, Chyung JH, Murtaugh LC, Brent AE, Rosen V, Olson EN, Lassar A, Tabin CJ. 2001. Analysis of the tendon cell fate using scleraxis, a specific marker for tendons and ligaments. Development 128:3855–3866. Shinohara H. 1995. Gemelli and obturator internus muscles: different heads of one muscle? Anat Rec 243:145–150.

Fetal Development of the Human Obturator Internus Muscle With Special Reference to the Tendon and Pulley.

To examine the development of the tendon pulley of the obturator internus muscle (OI), we observed paraffin sections of 26 human embryos and fetuses (...
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