J. Anat. (1968), 102, 2, pp. 345-352 345 With 11 figures Printed in Great Britain The origins of the muscles B. F. MARTIN Department of Human Biology and Anatomy, University of Sheffield From reference to standard works (e.g. Macalister, 1889; Thane, 1894; Rouviere, 1912; Wilde, 1949; Grant & Smith, 1953; Hollinshead, 1958; Last, 1959; Davies & Davies, 1962; Romanes, 1964; Grant, 1965) it is by no means clear how the - of the hamstring muscles are related to one another at their origins or how they attain their relative positions just beyond their places of origin. Of this group the semimembranosus is particularly difficult to understand, and part of the difficulty is due to incorrect appraisal of the position of the facets on the , from which the largely arise. The ischial tuberosity The tuberosity is divisible into an upper region, which bears two smooth facets. and a lower region which is roughened. Both regions are related to the hamstring origins. Although a few authors describe the facets simply as medial and lateral in position (e.g. Macalister; Rouviere; Hollinshead), the majority describe and illustrate the region as divided by an oblique ridge into a lower and medial and an upper and lateral facet (e.g. Thane; Wilde; Romanes; Davies & Davies; Grant; Terry & Trotter, 1953; Breathnach, 1965). If the facets did have this arrangement, it would be hard to imagine how the semimembranosus, which arises from the lateral facet, could gain the deep aspect of the biceps and semitendinosus, the common of which arises from the medial facet. From a study of thirteen male and seven female pelves, of which seven were articu- lated with the whole skeleton, it was found that when the is correctly orientated the ridge dividing the facet area of the ischial tuberosity is vertical in direction, so that the area is divided into a medial and a lateral facet. Although the outline of the facet-bearing area shows individual variation, it may be described as rhomboidal with the angles variably rounded off, and the long axis is directed upwards and later- ally. The facet medial to the vertical ridge is quadrilateral or triangular in shape whilst the lateral is triangular or fan-shaped, with the base above (Figs. 1, 2). It was also found that the inclination of the facets to the coronal plane is con- siderable and the inclination of the lateral is the greater. Furthermore, the facet inclinations are greater in the female than in the male. Measurement of the inclinations of the facets to the coronal plane was made on both sides of seven male and six female articulated pelves. One limb of a 2 ft folding steel ruler was placed against the posterior aspects of the ischial tuberosities, opposite the centres of the facet areas, whilst the other limb of the ruler lay in contact with the surface of the facet, as shown diagrammatically in Fig. 3. The angle between the limbs of the ruler was then measured with a protractor. Although there is some individual variation, the average angles of inclination of 22-2 346 B. F. MARTIN the medial and lateral facets in the male were found to be 400 and 600 respectively, whilst in the female they were 550 and 750 respectively. Thus, the angle of inclination of each facet to the coronal plane is 150 greater in the female, indicating that some rotation of the tuberosities is associated with their greater spacing in the female. However, the angle of inclination between the two facets is the same (200) in both sexes.

I

Coronal 3 Fig. 1. Lateral view of right ischial tuberosity, showing the vertical ridge between the medial and lateral facets and the rough triangular area below and medial to them. Fig. 2. Posterior view of right ischial tuberosity, showing sites of attachment of the sacrotu- berous ligament and the hamstrings. Fig. 3. Representation of a horizontal section through the right ischial tuberosity to show the angles made by the facets with the coronal plane in the male pelvis.

Due to the greater inclination of the lateral facet, it is apparent that the semi- membranosus which arises from it will lie deep to the common tendon of biceps and semitendinosus which arises from the medial facet, and since the facets are simply medial and lateral in position both tendons arise parallel to the vertical body axis. The rough area of the tuberosity below and medial to the facets is triangular in shape and is also associated with the hamstring origins. The apex of the triangle continues into a ridge (which supports the body weight when seated) and this in turn continues into the sharp inferior margin of the ischiopubic ramus. Before continuing into the latter, the ridge divides the remainder of the rough area of the tuberosity Origins of hamstring muscles 347 into inner and outer surfaces, and these were found to be inclined at about 120° to each other (Figs. 1, 2). The inner surface is limited above by the sharp falciform margin and the sacrotuberous ligament is partly attached to this inner surface as well as to the falciform margin (Fig. 6). The outer surface gives origin to the fleshy fibres of the adductor magnus. The origins of the hamstrings It is well recognized that there are interconnexions between the tendons of origin of the hamstrings. Rouviere, and Grant & Smith have noted that the biceps and semimembranosus are connected to the adductor magnus by fibrous bands just

Fibres to biceps

Adductor magnus tendon Fig. 4. Posterior view of the origin of semimembranous tendon, showing its attachments and mode of communication with the sacrotuberous ligament. Fig. 5. Lateral view of semimembranosup and biceps tendons, with the latter turned aside to show the mode of origin and distribution of the fibres forming the semimembranosus tendon. Fig. 6. The sacrotuberous ligament normally communicates with a fibrous mass which unites the hamstrings and is attached to the rough area of the ischial tuberosity. below the ischial tuberosity and a number of authors point out that some of the fibres of the sacrotuberous ligament are continued into the biceps tendon (Rouviere; Grant & Smith; Davies & Davies; Breathnach). It has been suggested that the sacrotuberous ligament represents the upper, 22-4 348 B. F. MARTIN degenerate part of the biceps tendon, which arose historically from the sacrocaudal vertebrae as in lower mammals and its attachment to the tuberosity in man and anthropoids is secondary (Rouviere; Grant & Smith; Davies & Davies). Hayek (1960) observed that the sacrotuberous ligament may continue into the semitendin- osus and semimembranosus as well as the biceps. He found that about half of the fibres of the ligament enter what he referred to as the joint origin of these muscles and he concluded that the hamstrings arise from the sacrum as well as the ischial tuberosity. In the present study it was found that the hamstrings are attached to each other at their origins and there is often continuity between the sacrotuberous ligament and all the hamstrings, including the narrow, tendinous part of adductor magnus. The semimembranosus The tendon of origin of this muscle arises from the triangular lateral facet of the ischial tuberosity, yet just below the tuberosity it has the form of a flat band which lies in the coronal plane, on the deep aspect of biceps and semitendinosus. The means by which the tendon achieves this form and arrangement was found to be as follows. The major part of the tendon arises from the lateral facet of the ischial tuberosity and is thus deep to the biceps. This part is fan-shaped in outline, roughly conforming with the facet outline. The fibres converge inferiorly and the posterior ones form the thick, rounded lateral margin of the tendon but the anterior fibres undergo a spiral turn and form most of the flattened medial part, as shown in Figs. 4 and 5. This flattened portion is attached to the rough triangular area below and medial to the facets, and from this area further fibres arise and enter the posterior aspect of the tendon. In addition to its bony attachments the tendon blends superiorly with a fibrous mass (to be described presently) that is associated with all the hamstrings, and medi- ally it is attached to the tendinous part of adductor magnus by means of a short band which usually unites with a similar band from the biceps femoris tendon (Figs. 4, 5). If the tendon is dissected free from its attachments to this adjacent fibrous tissue, the outline of its origin is seen to be comma-shaped. After leaving the ischial tuberosity, the shape of the tendon in transverse section has been aptly likened to that of a hollow-ground razor, since the thick, round lateral margin tapers into a membrane which has a sharp medial edge. Inferiorly, the tendon widens and muscle fibres arise from it along an oblique line which commences about 6 in. from the ischial tuberosity and is directed downwards and laterally (Figs. 9-11). The tendon fibres spread out in such a way that the muscle fibres arise from the interior of a cone and the fibres aggregated in the thick outer margin of the tendon fan out to embrace the lateral muscle fibres, i.e. those which arise most distally (Figs. 9, 11). The tendon expansion reaches further distally on the deep than on the superficial surface of the muscle. The muscle fibres form a thick rounded belly, and their tendon of insertion com- mences along an oblique line, directed downwards and laterally, roughly parallel to the line of termination of the tendon of origin. This tendon commences as a membrane on the medial aspect of the muscle and partly encloses it in an incomplete cone. The fibres of the membrane become aggregated into the thick round tendon Origins of hamstring muscles 349

Semitendinosus

Semitendinosus origin

Add uctor Long magn us - head of biceps

V Short head of biceps

Sem imem branosus-

Semitendinosus- `- 10o " 11 Fig. 7. Deep aspect of the hamstring origins, removed as a cup-shaped unit from the ischial tuberosity. Note their continuity with the fibrous mass and the sacrotuberous ligament. Fig. 8. The semitendinosus arises from the lower part of the sacrotuberous ligament as well as the concave inner margin of the biceps tendon and its thin expansion to the deep surface of the muscle (see Fig. 9). Fig. 9. The semitendinosus and biceps muscles have been removed to show that fibres leave the biceps tendon by undergoing a spiral turn to form membranous expansions on their deep surfaces. Fig. 10. There is little contact between the muscle bellies of the hamstrings. The semitendi- nosus and semimembranosus together form a cylindrical unit. Fig. 11. The 'bed' of semitendinosus is formed by adductor magnus and semimembranosus above and by semimembranosus only below. 350 B. F. MARTIN of insertion, and the most lateral muscle fibres terminate on the tendon only just above the joint (Figs. 10, 11). The biceps femoris and semitendinosus These muscles share a common tendon of origin which arises from the medial facet of the ischial tuberosity. It was confirmed that the sacrotuberous ligament makes a considerable contribution of fibres to the tendon but it was also found that it usually connects with the hamstring group of muscles as a whole. The medial fibres of the ligament form its falciform portion and are attached to the falciform margin of the , but usually some of these fibres cross the ischium in a sheet of variable thickness and enter a fibro-fatty mass which is attached to the rough area of the tuberosity, below and medial to the facets, and some fibres also enter the narrow tendinous part of adductor magnus (Fig. 6). The biceps tendon, like the semimembranosus tendon, is attached to the fibrous mass and is connected to the adductor magnus tendon by a dense fibrous band which usually blends with the similar band from the semitendinosus. When the sacro- tuberous ligament contributes fibres to the fibrous mass as well as to the main biceps tendon, the part of it involved can be dissected from the ischial tuberosity, together with the hamstring origins, and it is then seen that they form a cup-shaped unit, conforming to the convex contour of the tuberosity (Fig. 7; compare with Fig. 6). This finding would support the view quoted earlier, that the hamstrings arose histori- cally from the sacrocaudal vertebrae and their attachment to the tuberosity is secondary. On superficial inspection the biceps tendon appears to be rounded, but in cross- section it is concavo-convex and the semitendinosus muscle abuts against the medial, concave surface (Fig. 8). Not only are the attachments of the tendon beyond its facet similar to those of the semimembranosus tendon but the arrangement of its fibres on leaving the facet are also similar. Fibres gradually leave the deep aspect of the tendon by undergoing a spiral turn to enter a membranous inner part which is divisible into a proximal and a distal portion. The proximal portion, often very thin, passes deep to the semitendinosus and gives origin to some of its fibres; superiorly it is attached to the fibro-fatty mass uniting the hamstrings, from which it receives additional fibres (Figs. 7, 9). The distal portion is distributed to the deep aspect of the biceps, sometimes in strands (Fig. 9). Thus, the tendon of biceps is similar in form to the tendon of semimembranosus, since it has a thick outer margin and a membranous inner part. The fibres in the outer margin are progressively distributed to the mem- branous expansions on the deep aspects of semitendinosus and biceps. The muscle fibres of semitendinosus arise from about the proximal 3 in. of the inner, concave aspect of the biceps tendon, from the thin membrane on its deep surface and from the lower part of the sacrotuberous ligament which blends with the fibrous mass uniting the hamstrings (Fig. 9). Although of narrow oval outline at its origin it soon becomes thicker and more rounded. Near the mid it tapers to a conical extremity and its rounded tendon of insertion is formed from a somewhat fan-shaped membrane, developed on the antero-medial aspect of the conical extremity (Fig. 10). The muscle fibres of the long head of biceps femoris arise, distal to those of semi- Origins ofhamstring muscles 351 tendinosus, from the concave medial aspect of their common (biceps) tendon and sometimes from its lateral aspect as well (Figs. 9-11). The muscle belly is conical at its origin and the membranous expansion from the terminal part of the tendon is distributed mainly to its deep aspect where it partly ensheaths the muscle cone and gives origin to some of its fibres. Distal to its conical origin the long head enlarges and becomes rounded in outline. The muscle fibres insert into a dense, flat membrane which develops just below the mid thigh and from there onwards covers the pos- terior aspect of the muscle. Some of the fibres of the short head join the lateral fibres of the long head on their deep aspect and the remainder insert into the lateral margin of the membrane. The fibres of the membrane converge just above the knee joint into a strong tendon of insertion which is oval in outline (Figs. 10, 11).

The relationships of the hamstrings in the thigh Throughout their course in the thigh, there is only a minimal degree of contact between the muscle bellies of the hamstrings. The biceps and semimembranosus diverge from one another in the distal part of their course but nevertheless the muscular part of each muscle faces the tendinous part of the other (Figs. 10, 11). The semitendinosus lies in a musculo-tendinous 'bed' throughout its course. Proxi- mally, the bed is formed by the tendinous part of adductor magnus and the tendon of origin of semimembranosus, but the latter soon expands and gives origin to muscle fibres, so that throughout most of its course the semitendinosus lies upon the super- ficial surface of semimembranosus. Again, it is noteworthy that the muscle belly of the one muscle is in contact with the tendinous part of the other (Figs. 10, 11), and so the two muscles form a cylindrical mass (Last) and the action of one does not interfere with that of the other (Grant). Towards the knee joint only tendinous or membranous parts of the hamstrings are in contact with the overlying deep .

SUMMARY 1. It has been shown that the facet areas on the ischial tuberosity are simply medial and lateral in position, since the ridge separating them is vertical in direction. 2. The lateral facet has a greater inclination to the coronal plane than the medial, and so the semimembranosus tendon of origin which largely arises from it is deep to the biceps femoris which arises from the medial facet. The facet inclinations are greater in the female. 3. The posterior fibres of the semimembranosus tendon enter its thick outer margin whilst the anterior fibres undergo a spiral turn to enter its inner membranous part. Some spiralling of the biceps tendon occurs to form thin membranes deep to semitendinosus and biceps. 4. The hamstrings, including the tendinous part of adductor magnus, are united at their origins and blend with a fibro-fatty mass overlying the rough portion of the ischial tuberosity, and the sacrotuberous ligament is usually in continuity with all the hamstrings. 5. Where the hamstring muscles lie in contact, the muscle belly of one is in contact with the membranous or tendinous part of the other. 352 B. F. MARTIN

REFERENCES BREATHNACH, A. S. (1965). In Frazer's Anatomy of the Human Skeleton, 6th ed. London: Churchill. DAVIES, D. V. & DAVIES, F. (1962). In Gray's Anatomy, Descriptive and Applied, 33rd ed. London: Longmans, Green. GRANT, J. C. B. & SMITH, C. G. (1953). In Morris's Human Anatomy: A Complete Systematic Treatise, 11th ed. Ed. J. P. Schaeffer. London: McGraw-Hill. GRANT, J. C. B. (1965). Method ofAnatomy, Descriptive and Deductive, 7th ed. London: Livingstone. HAYEK, H. (1960). Ober den Ursprung der ischiocruralen Muskulatur vom Os sacrum. Verhandlungen der Anatomischen Gesellschaft aufder 56. Versammlung in Zurich, April 1959. Jena: Fischer Verlag. HOLLINSHEAD, W. H. (1958). Anatomy for Surgeons, vol. III. London: Cassell. LAST, R. J. (1959). Anatomy, Regional and Applied, 2nd ed. London: Churchill. MACALISTER, A. (1889). A Text-Book of Human Anatomy. London: Charles Griffin. ROMANES, G. J. (1964). In Cunningham's Text-book of Anatomy, 10th ed. London: Oxford University Press. ROUVItRE, H. (1912). In Poirier et Charpy's Traite d'Anatomie Humaine, 3eme ed., tome 2, fasc. 1. Paris: Masson. TERRY, R. J. & TROTTER, M. (1953). In Morris's Human Anatomy: A Complete Systematic Treatise, 11th ed. Ed. J. P. Schaeffer. London: McGraw-Hill. THANE, G. D. (1894). In Quain's Elements of Anatomy, vol. ii, pt. 2, 10th ed. Ed. E. A. S. Schafer and G. D. Thane. London: Longmans, Green. WILDE, F. R. (1949). In Buchanan's Manual of Anatomy, 8th ed. Ed. F. Wood Jones. London: Bailliere Tindall and Cox.