The role of function in the development of human craniofacial form ФA perspective.код для вставкиСкачать
THE ANATOMICAL RECORD 218:107-110 (1987) The Role of Function in the Development of Human Craniofac ial Form-A Perspective M.R. KEAN AND P. HOUGHTON Departments of Orthodontics (M.R.K.) and Anatomy [I? H.), Uniuersity of Otago, P 0. Box 647, Ditnedin, New Zealand ABSTRACT As a n anatomical region the head combines great diversity of function with close integration of structure. Consequently no structural component has autonomy of form. There is a sequence of maturation of functions and their related structural components, and in this sequence the nervous system and its supportive structures mature first. The nasal airway matures next in response to increasing body mass, and the masticatory system constitutes the last major functional system to reach maturity. The later the maturation of the function, the greater is the requirement for its related morphology to adapt to preceding skeletal templates. These matters of developmental sequence, and extrinsic as well as intrinsic craniofacial functions, are paramount considerations in interpreting the form of any component of head anatomy. Studies in craniofacial biology, whether developmental, structural, or functional, frequently fall within a single conceptual framework: A discrete region is examined as though it were a n autonomous unit, and without regard to the influence of other craniofacial regions, or of the body as a whole. Studies of variation isolated to the masticatory system, or the cranial vault, are examples. Yet the subtle fact is that within the functionally diverse yet structurally integrated architecture of the head, no component has autonomy; all are influenced by the demands of other components. Furthermore, as some head components subserve wholebody functions, in any study of craniofacial structure the relationship between the demands of the whole body and the form of the head must be considered. This paper presents a perspective on the form of the craniofacial skeleton derived from the developmental sequence of extrinsic and intrinsic functional demands made on the head. Structurally the sequence is expressed as a series of templates. Later-maturing components adapt to preceding templates, which requires the latest maturing structures to be the most adaptable. Such a perspective begins with a consideration of the developmental sequence within the head. Here the nervous system assumes priority. Soon after closure of the neural tube in the fourth week of embryonic life, the forebrain, midbrain, and hindbrain vesicles are recognizable. At this time brainstem flexures appear, and the cranial nerves are starting to form. During the sixth week the cranial base, which serves as a supportive platform for the brain - and a suspensory beam for the facial structures - begins to appear in cartilage. As early as the sixth week the flexure of the base is apparent, mirroring the angulation ofthe brain. Over succeeding weeks of embryonic development the elements of the base fuse, but remain permeated by canals and foramina carrying cranial nerves and major blood vessels. Thus 0 1987 ALAN R. LISS, INC. the supportive base develops in intimate and dependent relationship with the nervous system, a relationship seen a t its most complex in the course of the seventh cranial nerve and its branches through the temporal and sphenoid bones. This developmental precocity of the nervous system is matched by a cellular conservatism. With early completion of its cellular complement and a very limited capacity for regeneration and repair, the nervous system is structurally the least modifiable of body systems. Any substantive change in morphology of the cranial base, including its flexure, would be undesirably disruptive to the brain stem and emergent nerves. This overall stability of form of the cranial base during development has been considered to be due to its being under “strong genetic control” (van Limborgh, 1972; Glenister, 1976; Simons and van Limborgh, 1979; Bromage, 1980; Hanken, 1983). However, in the light of the sequence of tissue development, and evidence derived from experimental studies (Young, 1959; Moss, 1961; Schowing, 1968a,b; Moss et al., 1972; Greelen, 1973; Blechschmidt, 1976; Simons, 1979; Sarnat, 1982) this stability of form should be ascribed to the influence of the nervous system. The subsequent growth of the base, involving no significant change in flexure after the first year of postnatal life (Brodie, 1955; Knott, 1971; Riolo et al., 1974; Broadbent et al., 1975; Lewis and Roche, 1977) and limited inferior cortical drift with a proportional increase in length by growth at the transverse joints (Scott, 1958; Enlow, 1982), requires minimal adjustment of the complex relationship between nerve tissue and the cartilage, and ultimately the bone, of the base. Suspended from the anterior part of the base, the central part of the upper facial skeleton varies in posiReceived December 15,1985; accepted January 13,1987. 108 M.R. KEAN AND P. HOUGHTON tion according to the orientation of the base and the length of its anterior part. For example, the upper face is positioned more anteroinferiorly when suspended from a n open than from a closed base (Enlow, 1982; Kean and Houghton, 1982).But in addition, the upper face is influenced in shape and size by variation in volume of the nasal airway. A functionally significant increase in airway volume is possible only through vertical development, increase in width of the airway being limited by the general neurological constraints suggested above, and particularly the positioning of the eyes. Longitudinal cephalometric studies (Riolo et al., 1974; Broadbent et al., 1975) demonstrate that increase in height of the airway is one of the major dimensional changes occurring in the face during maturation. The functional correlate of this is the increasing energy demand of the growing body. Evidence for the direct association between body size and nasal airway height can be derived from these cephalometric studies, which show that, on average, the height of the nasal airway at maturity is greater in males than in females, whereas until about age 12 years nasal airway heights are similar, age for age, for the two sexes. The reason why this should be so lies neither in the nasal cavity nor the face, nor even in the head, but in the greater respiratory needs of males, in whom the greater functional demand is imposed on the face by the body. Between 6 and 16 years muscle mass increases about threefold in girls and fourfold in boys (Malina, 1978), and from about 12 years the curve for male muscle mass rises sharply, whereas that for females is starting to flatten. That is, male and female growth curves for muscle mass diverge from this age. Similarly diverging growth curves for males and females are seen for vital capacity (Ferris et al., 1952; Ferris and Smith, 1953). Airway enlargement is thus appropriate to oxygen demand, and the extent to which oxygen demand varies on average between males and females, or between any two individuals during development or at maturity, determines the extent to which the face develops vertically. Cross-sectional studies also reveal a highly significant correlation between body weight and nasal height in adults (Miyashita and Takahashi, 1971). Respiratory demand and the expansion required of the airway are influenced by a complex interplay of factors, including inherited body size (particularly muscle mass), and environmental factors such as diet, disease, altitude, and climate (Roberts, 1953; Heath and Williams, 1981). Although increase with maturation of the height of the upper face is well documented, the significance of its functional basis is not widely appreciated. Enlargement of the nasal airway is obligatory as the body grows, and as architectural substrate the airway, meeting an extrinsic demand, is a major influence on overall craniofacia1 form. By contrast, the growth curves for the other component of upper facial height, the teeth and alveolus, unlike those for the airway, do not diverge significantly for males and females with maturation (Riolo et al., 1974), as there is no biological requirement for this either within or beyond the head. And in absolute terms, a t maturity the increase in height of the dentoalveolar component of upper facial height has been only about half that of the airway. These upper facial growth changes, largely consequent on respiratory demand, lead inevitably to adjustments to the positioning of the maxillary dentition. Continuing adaptation is thus required in the mandible, particularly in the ramus and its related soft tissues, for the form of the mandibular dentition and its supportive bone has been determined at a n earlier stage of development and must in any case match the maxillary. Thus, as the maxillary dentition shifts inferiorly with enlargement of the airway during maturation, and the occlusal plane and the body of the mandible align more horizontally, mandibular angle lessens and the ramus increases in height. Consistently, the more vertical the ramus, the broader and higher it becomes, with larger surface area; associated evidence of greater muscularity is found in deeper, flattened temporal fossae with higher temporal lines, and robust zygomatic arches (Sassouni, 1969; Houghton, 1978; Lavelle, 1979), these being the compensatory muscular concomitants of the skeletal changes. Hence, for a given cranial base morphology, a n individual of large muscle bulk and large nasal airway, requires that the process of adaptation of the masticatory system be carried further than in a small adult. One skeletal manifestation of this is a lesser mandibular angle in the more heavily muscled individual, this being the biological basis of the observation in classical biometrics that at maturity, on average, males have smaller mandibular angles than females (Morant, 1936; Hrdlicka, 1940). The traditional view of the mandible as a third-order lever during the power stroke, the condyles being stressbearing, survives through much debate (Hylander, 1975; Gingerich, 1979; Moore, 1981; Moss, 1983) and is supported by a host of recent experimental biomechanical studies (Hylander, 1979; Hylander and Bays, 1979; Brehnan et al., 1981; Mongini et al., 1981; Standlee et al., 1981; Hohl and Tucek, 1982). While the mechanical efficiency of the maturing mandible decreases, the concept of efficiency or inefficiency of the mandibular lever is one of physics rather than biology, relating to the bony form alone. There is not a developmental or evolutionary set toward inefficiency, for the maturation of the musculature proceeding concomitantly with the bony change ensures biological efficiency. The adaptation of the masticatory system to the templates of cranial base and airway in turn influences the mature width of vault and face. The underlying cranial base has two components in this dimension: the central core penetrated by nerves and blood vessels; and lateral regions related particularly to the masticatory apparatus. The width of the core is determined relatively early, being related to the support required for the developing brain whereas the width of the lateral regions, though also providing support for the maturing hemispheres, varies particularly with the degree of development of the masticatory muscles whose maturation occurs much later. Individuals with severe masticatory demands will show hypertrophy of these muscles, and consequently a wide area of attachment on the base, even in the presence of a mandible with a n open angle and of efficient lever form. The face also is influenced by the development of the masticatory muscles behind the zygomatic bone (Cachel, 1979); the “filling-out” and flattening of the facial surface of the maxilla lateral to the airway is DEVELOPMENT OF HUMAN CRANIOFACIAL FORM an expression of greater buttressing for the zygomatic bone and arch, and is thus a function of masticatory development rather than directly a consequence of vertical development of the upper face, though the two are associated. This influence of muscle development on the cranial base and face is well demonstrated in cases of unilateral trigeminal palsy, where there is reduced depth of the pterygoid region, reduction in size of the corresponding pterygoid plate and fossa, and reduction in width of the corresponding side of the face (Rogers, 1958). The shape of the cranial vault has been ascribed to variation in dimensions of the cranial base, long heads being associated with long bases and round heads with short bases (e.g., Lavelle, 1979; Enlow, 1982). However, such direct expression of genetically determined brain proportions tends to be obscured by the many other influences on the vault (Buranarugsa and Houghton, 1981; Anderson and Popovich, 1983; Houghton and Kean, 1986). For example, brain size, and thus vault size, is influenced by nutrition (Brown, 1966; Israel, 1978; Metcoff, 1978). The flexure of brain stem and cranial base, or more distant influences such as body muscle mass and its determinants, influence vault form through the masticatory system, with substantial temporalis muscles flattening the temporal fossae, and substantial pterygoid muscles widening the base. Thus, while its early expansion may be dependent on growth of the underlying brain, the final shape of the vault is a n expression of a spectrum of influences. A sequence of adaptations is apparent, the hemispheres of the brain sometimes being required finally to adapt in form because of a sequence initiated by the primordial flexure of the developing midbrain. However, unlike the situation with the attenuated nerves emerging from the brainstem and passing through bony foramina, a gradual moulding of the hemispheres is physiologically acceptable. In this perspective of craniofacial form, the brain early in development determines shape and size of the supportive cranial base. Subsequently the airway, constrained laterally by major sense organs, enlarges vertically in harmony with the respiratory demand of the body. The masticatory system, and specifically its musculoskeletal component, adapts to the templates of cranial base and airway, and in its turn influences the form of the vault. 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