1. QUANTITATIVE ANALYSIS OF THE MUSCLES OF THE ROTATOR CUFF IN DIFFERENT ORTHOGRADE AND PRONOGRADE PRIMATE SPECIES: ADAPTATIONS TO DIFFERENT TYPES OF LOCOMOTION
Potau JM1, Bello-Hellegouarch G2, Arias-Martorell J2, Pastor JF3, De Paz F3, Barbosa M3, Diogo R4, Pérez-Pérez A2
1. Unit of Human Anatomy and Embriology. Faculty of Medicine. University of Barcelona.
2. Department of Animal Biology. Section of Anthropology. University of Barcelona.
3. Department of Anatomy and Radiology. University of Valladolid.
4. Department of Anatomy. Howard University.
1. INTRODUCTION
The rotator cuff is an important anatomical and functional structure composed by four muscles, which participate in the mobility and stability of the glenohumeral joint (Inman et al., 1944; Basmajian and de Luca, 1985) . The subscapularis muscle (Fig. 1) originates in the subscapularis fossa of the scapula, stabilizes the anterior surface of the glenohumeral joint and takes its insertion in the lesser tubercle of the humerus. The supraspinatus muscle (Fig. 2) originates in the supraspinous fossa of the scapula, stabilizes the glenohumeral joint superiorly and inserts in the upper face of the greater tubercle of the humerus. Finally, the infraspinatus and teres minor muscles (Fig. 2) originate in the infraspinous fossa of the scapula, stabilize the posterior surface of the glenohumeral joint and insert in the posterior face of the greater tubercle of the humerus. The subscapularis participates in the medial rotation movement of the glenohumeral joint. The supraspinatus elevates the upper limb in the scapular plane, working together with other muscles like the deltoid. The functional unit formed by the infraspinatus and teres minor participate in the lateral rotation movement of the glenohumeral joint.
The anatomical study of the rotator cuff in primates has a great interest due to its close relation with the shoulder bones, specially the scapula and the proximal epiphysis of the humerus. These bones, together with the other components of the scapular girdle, are related to the structural anatomical changes that allow us to explain the different types of locomotion performed by primates with a pronograde corporal pattern and primates with an orthograde corporal pattern. In pronograde primates, represented basically by non-hominoid primates, the scapular girdle supports mainly compressive forces and, thus, the stability of the glenohumeral joint is enhanced by anatomical changes that reduce the mobility of the joint (Larson, 1993). This fact limits the types of locomotion of pronograde primates to basically quadruped patterns (arboreal quadrupedism, terrestrial quadrupedism or semiterrestrial quadrupedism), although these primates can develop other more specific types of locomotion like vertical clinging. On the contrary, orthograde primates (gibbons, orangutans, gorillas, chimpanzees, bonobos and humans) have scapular girdles more adapted to resist tensile stresses and glenohumeral joints with enhanced mobility (Aiello and Dean, 1990). This anatomical and functional pattern allows the development in orthograde primates of arboreal types of locomotion like suspension, brachiation and vertical climbing, typically performed by gibbons and orangutans. Moreover, chimpanzees, bonobos and gorillas develop a particular type of locomotion called knuckle-walking, in which the glenohumeral joint has to resist an important shearing stress (Larson and Stern, 1986; Larson and Stern, 1987).
In this study we quantitatively analyzed the mass of the muscles of the rotator cuff, obtained from the anatomical dissection of different primate species with different anatomical corporal patterns and types of locomotion. Our aim was to find significant different patterns in the proportions of these muscles that could be functionally related to the corporal patterns and to the types of locomotion developed by the species studied. These results are included in a more extensive study that our team are developing in the anatomy of the musculoskeletal system of the upper limb of primates.
Subscapularis
Fig 1. Pan troglodytes
2. MATERIAL AND METHODS
In this study 45 adult primates were dissected and the species analyzed are detailed in Table 1. All the dissected primates were provided by the Anatomical Museum of the University of Valladolid and they came from different Spanish zoos. The individual belonging to the species Cercocebus atys lunulatus came from the Zoological Park of Barcelona. In all these cases, the primates died by causes not related to our study and all of them were cryopreserved without any fixation methods.
All the dissections were performed by the same author (JMP), who carefully individualized the muscles of the upper limb and weighed them using a precision scale. Also, three samples of each muscle were taken and frozen in saline solution for an ulterior molecular analysis.
Using the weights of the muscles subscapularis, supraspinatus, infraspinatus and teres minor, the total mass of the rotator cuff was calculated and, also, the proportional mass of each muscle in respect to the total mass of the rotator cuff. Finally, we calculated the relative mass of the rotator cuff and of the four of its constituent muscles in respect to the total body mass of the species studied. We were unable to know the real body mass because all the primates studied had been necropsied previously to our dissections. Thus, we used the mean values of the body mass present in the literature for all the species analysed in this study (Rowe, 1996 for Nycticebus; Harvey and Clutton-Brock, 1985 for Cercocebus; Fleagle, 1999 for the other species).
All the dissected primates were divided into one group of orthograde primates (genus Pan, Gorilla, Pongo and Hylobates) and another group of pronograde primates (genus Cebuella, Callimico, Saguinus, Pithecia, Callithrix, Leontopithecus, Nycticebus, Microcebus, Macaca, Colobus, Miopithecus, Aotus, Chlorocebus, Mandrillus, Lemur, Cercocebus and Erythrocebus). Also, the primates were divided by its main form of locomotion according to Schmitt (2010) in knuckle-walkers (Pan and Gorilla), suspensors (Pongo), brachiators (Hylobates), vertical clingers (Cebuella, Callimico, Saguinus, Pithecia, Callithrix and Leontopithecus), arboreal quadrupeds (Nycticebus, Microcebus, Macaca fascicularis, Colobus, Miopithecus and Aotus), semiterrestrial quadrupeds (Macaca silenus, Chlorocebus, Mandrillus, Lemur and Cercocebus) and terrestrial quadrupeds (Erythrocebus patas).
We used the Mann-Whitney test to compare orthograde versus pronograde taxa and to compare the locomotor groups. We set statistical significance at P <0.05. We used SPSS (version 18.0) for all statistical analyses. Brachiators and terrestrial quadrupeds were not used in the statistical comparison of the locomotor groups because these groups were represented by only one specimen.
Supraspinatus
Infraspinatus + teres minor
Fig 2. Pan troglodytes
Table 1. Number of species analyzed and forms
of locomotion (according to Schmitt, 2010)
3. RESULTS AND DISCUSSION
The results obtained in the present study are summarized in Table 2. Orthograde primates have a greater relative weight of the rotator cuff in respect to the body mass in comparison with pronograde primates (1,06% vs 0,70% p=0,002). This observation is related to the major development of the upper limb in orthograde primates and with an enhanced function of the rotator cuff muscles as stabilizers of the glenohumeral joint in these primates (Ashton and Oxnard, 1963; Roberts, 1974). In pronograde primates, the glenohumeral joint presents a higher degree of stability due in part to the dorsal position of the scapula in respect to the humeral head and to the morphology of the anatomical structures which form this joint. Thus, the morphological characteristics of the glenoid cavity and the humeral head enhance the stability of the glenohumeral joint, but reducing its mobility (Aiello and Dean, 1990). However, there are not significant differences in the relative mass of the rotator cuff between the different groups of locomotion analyzed (Table 2).
When we analyze the relative mass of each muscle of the rotator cuff in respect to the body mass, we can observe that there are not significant differences in the supraspinatus between orthograde and pronograde primates (0,18% vs 0,17% p=0,565), but significant differences can be observed in the subscapularis (0,48% vs 0,32% p=0,002) and in the functional complex formed by the infraspinatus + teres minor (0,40% vs 0,21% p<0,000). In the two cases, an increment of the relative mass can be observed in orthograde primates, which can be related to the functional significance of the movements of medial rotation and lateral rotation in the types of locomotion developed by orthograde primates (Tuttle and Basmajian, 1978; Larson and Stern, 1986; Larson and Stern, 1987; Larson, 1988). Again, there are not significant differences in the relative mass of each muscle of the rotator cuff when the different types of locomotion developed by each group of primates are compared (Table 2).
The analysis of the relative mass of each muscle in respect to the total mass of the rotator cuff indicates that there are not significant differences in the subscapularis between orthograde and pronograde primates (45,0% vs 45,83% p=0,634). But we can see that there is a significant reduction of the relative mass of the supraspinatus (17,4% vs 24,54% p<0,000) and an increase of the relative mass of the infraspinatus + teres minor in orthograde primates (37,7 % vs 29,63% p<0,000). The greater relative mass of the supraspinatus in pronograde primates (Fig. 4) indicates its functional significance as a postural and antigravitational muscle in these primates, in which the supraspinatus prevents the collapse of the glenohumeral joint in the pronograde position (Preuschoft et al., 2010; Potau et al., 2011). This postural function of the supraspinatus is lost in most suspensors Pongo and Hylobates, but it is recovered in the knuckle-walkers Pan and Gorilla with the aid of the infraspinatus, in contrast to pronograde primates in which only the supraspinatus has this function. The enhancement of the relative mass of the infraspinatus + teres minor in orthograde primates (Fig. 3) can be related to the high significance of the movement of lateral rotation in the glenohumeral joint in types of locomotion as brachiation and vertical climbing, and with the high significance of these muscles as stabilizers of the glenohumeral joint in knuckle-walkers (Larson and Stern, 1987). Another interesting result related to orthograde primates is that the knuckle-walkers Pan and Gorilla do not show the same structural pattern in the rotator cuff, since Gorilla (Fig. 6) has a significant greater relative mass of the supraspinatus in respect to the total mass of the rotator cuff than Pan (Fig. 5) (20,4% vs 15,0% p=0,024). Finally, we did not observe significant differences in the relative mass of the supraspinatus between the types of locomotion developed by pronograde primates (Table 2). However, we observed a significant increase in the relative mass of the subscapularis in the vertical clingers group in respect to the arboreal quadrupeds and semiterrestrial quadrupeds (49,55% vs 43,56% and 44,13% p<0,000 and p=0,011). This increase in the relative mass of the subascapularis can be related to the high functional significance of the movement of medial rotation in the glenohumeral joint in vertical clingers (Walker, 2005) and this fact is accompanied by a significant reduction in this group of the relative mass of infraspinatus and teres minor (26,30% vs 32,48% and 30,17% p<0,000 and p=0,046). We did not find significant differences in the same sense between arboreal quadrupeds and semiterrestrial quadrupeds.
Table 2. Mean values and statistical significance of the parameters analyzed. P=pronograde, O=orthograde, KW=knuckle-walker, S=suspensor, VC=vertical clinger, AQ=arboreal quadruped, SQ=semiterrestrial quadruped, RC=rotator cuff, BW=body weight, SUB=subscapularis, SUP=supraspinatus, INF=infraspinatus, TM=teres minor
Supraspinatus
Supraspinatus
Teres minor
Teres minor
Infraspinatus
Infraspinatus
Fig 3. Pongo pygmaeus
Fig 4. Lemur catta
Supraspinatus
Supraspinatus
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Teres minor
Infraspinatus
Teres minor
Infraspinatus
Fig 5. Pan troglodytes
Fig 6. Gorilla gorilla