Developmental changes of the cranial bone thickness in the human fetal period.код для вставкиСкачать
Developmental Changes of the Cranial Bone Thickness in the Human Fetal Period FUMIO OHTSUKI 2 Department of Anatomy. The Jikei Uniuemity School of Medicine, Nishishinhashi, Minato-ku, Tokyo 105, Japan KEY WORDS Fetus Cranial bone . Growth of thickness Allometric analysis . Bilateral difference. ABSTRACT The description of the developmental changes of cranial bone thickness in the fetal period is the primary aim of this paper. The materials utilized in this study consisted of the two series. One is those of dry bones of 62 Japanese fetuses ranging from the fifth month to term and the other is those of 56 Japanese fetuses ranging from the fourth month to term. The first series is mainly used for the tests of bilateral difference in the thickness of cranial bones. No statistical significance could be found. Allometry technique was then applied for the analysis in the growth of the thickness of cranial bones and an extremely positive allometric coefficient was obtained. This required us to study another material, i.e., the second series. The materials of the second series were first measured for crown-rump length, head length, head breadth and head circumference. The heads were then carefully dissected and the left side of individual bones of the cranium were removed to take further measurements for the arc length. The thicknesses at the ossification centers and midpoints were successively measured by a micrometer readable to 0.01 mm. The results of the second series were investigated from the viewpoint of absolute and relative growth. By allometric analysis, vertical and transverse arc lengths were found to be isometric with two exceptions, while every measurement of thickness shows an extremely positive allometry. This coincides with the results of the first series. Gross structural and quantitative changes of the skeleton in human pre- and circumnatal periods have been described in detail. Studies confined to the development of fetal cranial bones were undertaken by Augier ('13, '311, LaCoste ('311, Inman ('341,Inman and Saunders ('371, Noback ('431, Moss ('551,Moss et al. ('561,fino ('571, Nishida ('591, Misaki ('59a,b1, Koura and Yokota ('601, Kobayashi and Inoue ('61), Moss ('641, Ohtawa ('671, Kawarada ('681 and others. These researches are generally concerned with the determination of the normal number and the time of appearance of ossification centers and/or the developmental anatomy of one or more individual bones. AM. J. PHYS. ANTHROP., 46; 141-154. Functional anatomists have stressed that the morphology of the head is the resultant not only of bone growth but of the integral growth of all its components, namely, brain, meninges or viscera (Inman, '341. Therefore, isolated cranial growth data become meaningful only in the context of correlation with the growth of other structure (Moss et al., '56; Moss and Young, '611. The literature, however, reveals a dearth of information on the thickness of cranial bones. In this paper developmental ' A part of this paper was read before the 77th Annual Meeting of Japanese Association of Anatornistr in Kagoshima on March 1972. Present address Faculty of General Education, Tokvo University of Agriculture. and Technology. Ilarumiclo, Fuchushi, Tokyo 183,Japan. 141 142 FUMIO OHTSUKI changes of cranial bone thickness and bilateral difference of them in the fetal period are described. MATERIALS AND METHODb The materials utilized in this study consisted of two series. One is the dry bones of 62 Japanese fetuses ranging from the fifth month to term (subsequently termed "dry bone series") and the other is 56 Japanese fetuses ranging from the fourth month to term (subsequently termed "fresh hone series"). In both series sexes are combined because sexual differences in the fetal cranial region are rare (Koura and Yokota, '60). Age of the dry bone series was estimated by the method of Morita et al., ('73) from a given long bone. The thickness at the ossification center (OC) of the frontal and parietal bones was measured with a micrometer readable to 0.01 mm (fig. la,b). The thickness of the temporal bone at the midpoint (MP) between porion and the highest point of squamo-temporalis was also measured on both sides (fig. Id). The results thus obtained were investigated from the viewpoints of bilateral difference and relative growth (Huxley, '32). Fresh bone series were obtained in a fresh condition from various hospitals and preserved in 10% formalin solution. Investigations prove that formalin preservation for a period over six months leads to no great change in the external dimensions of the body (Schultz, '19; Patten and Philpott, '21, and Scammon and Calkins, '29). The formalin preserved fetuses were first measured for crown-rump length, head length, head breadth and head circumference. The heads were then carefully dissected and the left side of individual bones of the cranium only were removed for further investigation. Observation on the dry bone series proves no statistically significant difference between the right and left sides. To demonstrate the general size of each bone, vertical and transverse arc lengths were measured on frontal, parietal and occipital bones and the vertical arc only on temporal bones. Methods of measurement in frontal and temporal bones were those of Misaki ('59a,b), parietal bones of Koura and Yokota ('60) and occipital bones of Nishida ('59). In the frontal bone, vertical arc length is from the supraorbital edge to the highest point of squama and transverse arc length is the maximum one (fig. la). In the parietal bone, transverse arc length is parallel to the Frankfort horizontal plane (FH) and passes through the center of this bone; the vertical arc is at right angles to the transverse arc at the center of the bone (fig. lb). In the occipital bone, the maxiinum vertical arc length and the maximum width as a transverse arc were measured (fig. lc). In the temporal bone, the arc crossing at right angle to FH from uppermost point of porion to supratemporal border was measured as the vertical arc length (fig. Id). The instrument used was a measuring tape readable to 1mm. After the arc length of each bone had been taken, the thickness at the same points as dry bone series were measured. Besides, the thicknesses of occipital hone at the ossification center (OC)and the midpoint (MP) between the ossification center and the highest point of squamo-occipital were measured (fig. lc). The results thus obtained were investigated from the viewpoint of absolute and relative growth (Huxley, '32). Detailed statistical procedures of allometric analysis are given by Sholl ('48,'50) and Sagami ('69). In the allometric equation (y = bx.1, crown-rump length is the abscissa (XI and arc length and thickness of each cranial bone are the ordinates (yl. The allometric equation transformed into logarithms, log y = a log x log b, means that any values in this formula plotted on the double logarithmic grid fall along straight lines. In the equation, a is the allometric coefficient and log b is the initial growth coefficient (Huxley and Tessier, '36). The value of a gives the ratio between the specific growth rates of the dimensions x and y. When this value is 1.00, the slope of the line is 45"and the specific growth rates of x (the abscissa1 value) and of y (the ordi- + 143 FETAL CRrZNIAL BONE THICKNESS la lb lc Id @ : O S S I F I C A T I O N CENTER (OC) El : M I D D L E POINT (M PI V :VERTICAL ARC LENGTH T :TRANSVERSE ARC LENGTH Fig. 1 Schematic rcpresentation of the vertical and transverse arc lengths measured for each bone: frontal (la], parietal (lbl,occipital (lc) and temporal (Id).OC is the ossification center. MP is the middle point between the ossification center and the highest point of squamo-occipital of occipital bone (Ic),and that between porion and the highest point of squamo-temporalis of temporal bone (Id), respectively. FH, Frankfort horizontal plane. nate value) are equal, that is, isometry. by sides and the bilateral differences When the value of a is less than 1.00,the tested in the frontal, parietal and temporal slope of the line is less than 45" and the bones. No statistical significance could be ratio favors the abscissa1value (XI, negative found, namely, a's in the regression equaallometry; when the value of a is greater tion, y = ax+b, taking C-R length as than 1.00, the slope of the line is greater abscissa, of the right and left frontal bones than 45" and the ratio favors the ordinate are 0.27 and 0.28, of parietal bones both value (y), positive allometry. 0.29 and temporal bones 0.27 and 0.28, respectively (table 1). RESULTS To investigate the specific growth rate of Dry bone series each cranial bone thickness, allometric The data of dry bone series were pooled analyses were carried out (table 2). (The 144 FUHIO OHTSUKI TABLE 1 a- and b-values in the regression equation, y = ax+b, C-R length being represented by x and the others by y ltems Side a1 11 R L R L R L 0.27+ 0.06 - 35.61 - 37.02 - 23.47 - 25.31 - 42.65 - 46.90 Frontal bone thickness (OC) Parietal bone thickness (OC) Temporal bone thickness (MP) I 0.28 f 0.07 0.29k 0.08 0.292 0.09 0.272 0.08 0.28+ 0.09 Significant difference wrisriot toiu~dbetween right and left ndes TABLE 2 a- and log b - d u e s in the regression eqwtion, log y = a log x + log b, C-R length being represented by x and the others by y Side a log b F-test 2.052 0.45 Parietal hone thickness (OC) R L R Temporal bone thickness (MP) R - 3.43 - 3.23 - 2.07 - 4.55 - 4.55 - 4.77 P P P P P P Items Frontal bone thickness (OC) 1.96+ 0.46 1.56_+0.44 1.61i 0.25 2.452 0.75 2.54+ 0.64 L L OC and hlP are the abbreviations as identified in figure 1. ,'l positive allometry procedure of analysis by this technique will be given later.) The a values approximate 2 in all the cases. The a's of right and left frontal bones are 2.05 and 1.96,of parietal bones 1.56 and 1.61 and of temporal bones 2.45 and 2.54, respectively. The results here obtained were not immediately accepted, since no other study of skeletal growth shows such an exceedingly positive allometry. This required us to study another material, i.e. fresh bone series. Fresh bone series Absolute growth Table 3 presents the mean and standard deviation of arc length for each bone by fetal age in months. For the frontal bone, transverse length exceeds vertical length in the fetuses of four to five months; however, this relation is reversed at six months and thereafter vertical length is greater than transverse length in an absolute value. For the parietal bone, vertical length leads throughout the latter half of fetal period. The two dimensions grow proportionally keeping the same difference as that at the initial age in this study. In the occipital bone, contrary to the parietal bone, transverse length is greater than vertical length throughout the period studied. Even though not strictly the same measurement, the results here obtained are in agreement with those of Misaki ('59a) in the frontal bone, of Koura and Yokota ('60) in the parietal bone, of Nishida ('59) in the occipital bone and of Misaki ('59b) in the temporal bone. Table 4 presents the mean and standard deviation of cranial bone thickness by fetal age in months. At the age of four to five months, the order of thickness among cranial bones is as follows; occipital bone at ossification center, occipital bone at midpoint, parietal bone at ossification center, frontal bone at ossification center and temporal bone at midpoint. This ranking is nearly constant until the tenth month, except that the position of the occipital bone at midpoint and parietal bone at ossification center are reversed at seven months. 13 13 10 10 10 N 22.50 34.38 43.90 50.70 55.00 h.1 SD 23.25 29.31 36.80 41.80 45.00 M N 13 13 10 10 10 M 6.75 14.31 24.90 29.30 39.60 oc SD 3.40 7.03 6.60 5.70 9.52 Frontal Abhseviations are as identified in table 3. 7 8 9-10 6 4-5 Age in months 38.50 45.62 57.30 70.00 76.30 M SD TABLE 4 35.75 45.00 56.20 67.40 73.70 M 4.50 4.85 6.88 5.10 5.54 SD Parietal bone Tsansv. 5.20 4.43 4.83 5.73 4.16 Vert. SD 24.00 3.92 29.77 5.59 41.50 3.59 50.60 3.92 57.10 3.76 M M 9.50 21.69 41.70 49.60 54.30 SD 1.73 9.47 9.23 12.19 13.46 Parietal OC M 30.00 67.08 135.90 157.20 165.40 oc SD 19.92 30.10 42.56 26.98 26.32 Occipital M 14.50 34.80 39.90 51.70 66.20 MP 3.70 12.17 15.99 9.33 13.52 SD 30.00 36.15 46.50 57.60 60.60 M 4.83 5.01 4.45 4.62 2.68 SD Occipital hone Vest. Transv. Numbers of materials, means and standard deviations of cranial bone thickness by fetal uge in months 10-2 mm 1.50 3.33 3.19 3.05 2.71 SD Frontal bone Tsansv 9.29 3.28 3.78 3.40 3.53 Vest. N, numl,rrs of' the rnatrrials (sexes comhinedl. M, rneans. SD, standard deviations. 4-5 6 7 8 9-10 Age in months Numbers of materials, means and standard deoiutions of arc length bv fetal age in months mm TABLE 3 M 3.75 9.85 17.60 21.00 32.80 SD 1.26 1.93 2.36 2.11 2.35 2.22 4.74 5.19 4.71 12.20 SD Temporal MP 9.25 11.31 16.70 19.00 24.20 M Temporal bone Vert. 146 FUMIO OHTSUKJ The thickness of occipital bone at ossification center is distinguished above all others. As far as the author is aware, other data for the cranial thickness in fetuses are not available. distinguished among them, gentle and steep ones. The slopes are generally gentle for arc length and rather steep for bone thickness, which means a differing specific growth rate predominated by the thickness of cranial bone. This trend, apparent from the figures, is more reliable by the result of the F-test for a values given in table 5, namely, the difference between each a value and 1.00. Where the a value is significantly greater than 1.00, it is categorized as positive allometry and vice versa as negative one. On the other hand, when a is not significantly different from 1.00, it is isometry (Huxley and Tessier, '36). Graphic representation of a values are given in figure 6. RelatiGe growth Analysis of allometry was undertaken in the following way. The values for arc length and bone thickness were plotted on log-log papers by each cranial bone with crown-rump length as abscissa. Subsequently the usual methods of allometric technique were utilized (Sholl, '48, '50; Sagami, '69). Table 5 presents the results of analysis by this technique for vertical arc length, transverse arc length and thickness by each cranial bone. The results of external head measurements are additionally presented. In table 5, a is the allometric growth coefficient or the slope of the regression line, and log b is the initial growth coefficient considered only the y intercept of the regression line. Then, the lines were drawn on each plot (figs. 2-51 and two kinds of slope may be DISCUSSION Growth The skull may be regarded as a complex of relatively separate functional components such as cerebral capsule, ear capsule, orbit, etc. (Van der Klaauw, '48-'52). Furthermore, within a given cranial bone are three functionally independent compo- TABLE 5 a und log b-values in regression equation, log y = a log x + log b, C-R length being represented h y x and the others by y Item Frontal bone Thickness (OC) Vertical arc Transverse arc Parietal bone Thickness (OC) Vertical arc Transverse arc Occipital bone Thickness (OC) Thickness (MP) Vertical arc Transverse arc Temporal bone Thickness (MP) Vertical arc Head length Head breadth Head circumference a loe b F-te5t 2.48 & 0.47 1.13+ 0.17 0.97 f 0.08 - - 4.48 1.02 - 0.68 P I I 2.38k 0.39 1.0810.08 1.08f 0.10 - 4.05 - 0.77 - 0.78 P I I 2.492 0.53 2.03i 0.36 1.37k 0.14 1.12r 0.12 - 3.83 - 3.18 P 2.65+ 0.51 1.48r 0.14 1.06? 0.09 1.02+ 0.08 1.10+ 0.08 - 5.02 P - 2.27 P - 0.59 - 0.59 - 0.21 P OC and MP are as identified in figure 1. F-test, significant at the level of 0.01; P, positive allonietry, I, isometry. 1.60 - 0.96 - P P I 1' P FETAL CRAKIAL BONE THICKNESS 1 o-hmw 60 - FRONTAL / BONE 50 - 40 . . . .. . .. 30 - - 20 - 15 - 60 50 40 - 25 Ohm 30 80 1 0;m 90 80 70 70 60 60 50 50 40 40 30 30 25 25 20 20 1 fm,r 90 25 20 15 Thickness 15 10 8 147 - 10 T/ 6 - mm 50 40 20 "F mm - 90 80 70 60 30 Transverse A r c 25 20 50 30 40 40 20 I I , 125 150 I 200 ( 1 30 , 250 300350 C-R L E N G T H mm Fig. 2 Logarithmic plots of arc length and thickness for the frontal bone against C-R length. Fitting lines are drawn on each item. 125 150 200 250 300350 L E N G T H mm Fig. 3 Logarithmic plots of arc length and thickness for the parietal bone against C-R length. Fitting lines are drawn on each item. nents: an outer plate, a diploe and an inner plate. Growth of the outer plate is correlated with the increasing demands of the scalp tissues in general and of cranial muscles in particular. The inner plate on the other hand is sensitive to alterations in cerebral morphology, that is, the state of adjacent soft tissues (Dyke et al., '33; Ross, '41; Noback, '45; Noetzel, '49; Fischgold and Metzger, '51; Lefebvre, '51; Lefebvre et al., '53; Kehre, '55; Lefebvre et al., '55; Schiffer, '56; Schiffer and Korn, '56; Kimura et al., '69). Dissociated by the result of this osseous differentiation of the two bony plates, an intervening diploe appears. Kawarada ('68) suggested that the time of formation of three components within the parietal bone is at about two years of age. From the viewpoint of functional anatomy, the time of diploe formation and any connection between it and high allometric coefficients in the thickness of cranial bone are of great concern to us. The allometric analysis of thickness in fresh bone series of fetuses (table 5 ) fundamentally coincides with that in dry bone series (table 2). This confirms both the results as not artificially obtained. C-R 148 FUMIO OHTSUW 10;1rnr OCCIPITAL 250 BONE / I QXllIl 250 1 fhm Oj:II?? 60 TEMPORAL BONE 50 200 - 200 150 - .I 60 50 40 40 30 30 150 25 25 100 90 80 - 100 90 80 20 20 70 60 - 70 15 15 60 50 - 50 40 - 40 30 - /-' J 10 8 25 20 15 - mm 6 70 60 5 50 mm 15 40 mm i ! 70 60 50 40 Transverse Arc 30 25 I ' 0 1 30 o m 30 lo I. 1 I 25 0 0 B"o0 Vertical Arc 125 150 200 250 300350 C - R L E N G T H mm Fig. 5 Logarithmic plots of arc length and thickness for the temporal bone against C-H length. Fitting lines are drawn on each item. weight and areal growth of fetal parietal bone (Ohtsuki, unpublished) and the a values in table 3 for one dimension, head length, breadth and circumference aplines are drawn on each item. proximate 1, or isometry. Taking this into consideration, the present results are In a previous report, a values were 3.21 peculiar as one-dimensional outcomes. for body volume and 3.17 for body weight Something must be taking place in the in the human fetuses (Morita and Hattori, growth of individual bone. '69). However, a values approximating 3 The following outline of the growth are generally for volumetric or weight process of cranial bone in the fetal period growth, 2 for areal growth, and 1 for the is useful for consideration of the cause of growth of one dimension. For example, the high a values obtained: Ossification of 3.74 and 2.20 are found for the a values of membrane bones commences as a thin net1 2 5 150 C-R 200 250 300350 LENGTH mm Fig. 4 Logarithmic plots of arc length and thickness for the occipital bone against C-R length. Fitting 149 FFTAI> CII4NI.4L RONE 'l~HI(:KNESS GRAPHIC REPRESENTATION OF 08 ITEMS 1 I FRDNlAl Vertiral 25 I I iOC) Arc BONE tOC1 Thickness 0 Arc VprtiLal I Transverse 0 Arc -------. BONE OCCIPITAL Thickness (OCI ThicknPss (MF) Arc Vertical Transverse Arc BONE Thickness Vertical 2 Arc Transverse TEMPORAL 15 I -VALUES BdbF Thickness PARIETAL ___- Q iMPi Arc HEAD LENGlH HEAD RREADlH HE A U C I P C IJ M F E R F N L E 0 : Positive Ailornetry 0 : Isometry Fig. 6 Graphic reprcwntation of allornetry coefficients. Numerals indicated in the first row of the figure are allorrietric coefficients. Note that all the a values of the thickness at OC and MP deviatcr far from the vertical line of the figure, i.e. extremely positive ;illoinetr). Thea values of arc lrngth and external head dirrtrmsion locate new this line. i.e. isometry. work of bone in the region of the future eminence. Growth o c c ~ mby the formation of the long thin bony trabeculae laid down radially from the primary ossification center. Later a few secondary trabeculae arise, fuse with each other and increase the size of the original bony network. Thus, in a cross-section of any individual cranial bone, a comparatively large unossified or vacant area is observed among bony trabeculae (fig. 7 ) . The behavior of this area rnay hold a key to interpreting the present a values of cranial bone thickness, that is, any high speed extension of vacant area, not of bone s~il~stance itself. is presumably in the dynamic growing process within an individual bone. The quantitative analysis of the cross-sectional tissue of cranial bone is requisite to the next step. Finally the positive allometry in the vertical arc length for temporal and occipital bone? is of' interest for the one-dimensional outcomes. Nishida ('59) and Ohtawa ('67) also described a relatively high growth rate in the latter half of the fetal period for vertical arc length in temporal and oc- 150 FUMIO Olf'SUKI Fig. 7 Saniples of parietal lmne tissue of a fetus cross-sectioned at ossification center, 7a of the sixth month and 7t)of the seventh month, respectively. Note the vacant area in proportion to that filled with bone substance. x 50. FETAL CRANIAL BONE THICKNESS cipital bones respectively, which supports the present results. It is common knowledge that the cranial bones are of dual origin, membranous and endochondral; occipital and temporal bones have a complicated structure composed of both parts. Moss ('55) demonstrated the singular behavior of the cartilagenous part in occipital bone growing relatively faster than any cranial and postcranial bone. Since his series of human fetuses are from 14 mm to 175 mm C-R (55 to 133 days of menstrual age), earlier in growth stage than the present materials, some alternative or compensatory changes in the growth rate favoring the membranous portion may have been possible in the later fetal period in response to the rapid growth of underlying soft tissues. However, it is hasty to present any conclusion based on fragmentary information; estimating the whole from knowledge of a part is also dangerous here. The study of the growing process for a membranous portion in close connection to a cartilagenous portion is certainly necessary for clearer analysis of the present results. 151 more active metabolism in the brain and makes the left inner plate narrower than the right side by a strong inner pressure upon it adjusting to the expansion of the intra-cranial contents. Attention may be called thereby to the functional independence of inner and outer plates in cranial bones (Van der Klaauw, '46; Delattre and Fennart, '54; Simon, '55; Kimura et al., '69); that is, the inner plate responds primarily to the underlying brain. No difference b y side in the thickness of cranial bone for postnatal preadults (Roche, '53) and prenatal samples (the present study) would not thoroughly refute the hypothesis of Hackl ('661, because it is presumably taking a long term until any changes of soft tissue (brain) bring corresponding changes in the cranial bone. It seems, however, scientifically unsound to take two morphological and/or behavioral events, e.g., cerebral dominance and bone thickness changes and assign a causal relationship between them. There should be some intermediate steps which need to be considered before jumping from brain morphology to bone shape or thickness. Bilateral d gference Besides, few studies on the growth of Studies of the bilateral difference in the brain are decisive for the validity of thickness of cranial bone are rare. Roche Hackl's interpretation. The anatomic dif('53)investigated a postnatal subadult sam- ference between the dominant and the ple (3-21 years) and found no significant minor cerebral hemisphere is uncertain exbilateral difference at euryon. Hackl ('661, cept that the occipital horn of the lateral on the other hand, observed adult crania ventricle is usually larger and the sulcus (under 50 years) and found asymmetry in lunatus more prominent on the left side the thickness near stephanion. His sexes (Adams and Mohr , '70). Whether heredity or learning is responcombined data showed that 71 out of 100 cases dominant in the right side, 16 cases sible for hand preference is still controversial. left side and 13 c a e s were symmetric, ACKNOWLEDGMENTS Of the general population, the ratio of right-sided dominance in the upper limbs The author is deeply indebted to Profesis approximately 90-95%, the remainder sor S . Morita, the director of the Departleft-sided and 10-2096 partially left- ment of Anatomy, The Jikei University handed, that is, preferring neither hand School of Medicine, for his cordial direccompletely but favoring one hand for more tion throughout the study, without whom complicated tasks (Adams and Mohr, '70). this study would not have been possible. These numerals coincide well with the reLITERATURE CITED sults of Hackl ('66). He presumed that the increasing demand on the left cerebral Adam, R. D., and J. P. 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