Paper - Fetal growth in man
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Schultz AH. Fetal growth in man. (1923) Amer. J of Physical Anthropology 6(4): 389-
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Fetal Growth in Man
Adolph H. Schultz
Carnegie Institution of Washington, Department of Embryology
This article is a summarized preliminary report of the author's extensive investigations on this subject. These will appear in detail in the near future in Contributions to Embryology, published by the Carnegie Institution of Washington.
Our knowledge of human growth after birth is well advanced, but comparatively little study has been made of growth in utero, and what has been published does not deal with the subject in a comprehensive manner, being either based upon insufiicient material or restricted to some special problem.
From a collection of over 5,000 human embryos and fetuses in the Carnegie Laboratory of Embryology the author selected for study 623 of the best of the normal and well—preserved specimens, both white and negro, ranging in age from the ninth week to term. Of the results of the anthropological investigations of this material the more important general conclusions will be mentioned first.
These exist as early in development as the human form can be recognized; many of them become more marked with advancing growth, but some are as pronounced in fetuses of three months as in the newborn or even in the adult stage. These differences are essentially the same as those which distinguish adult whites from adult negroes. No racial differences in any part of the body were found to diminish with advance in growth; they all seem to develop in diverging directions. In many instances the greatest divergence is reached early in fetal life and growth thereafter proceeds in parallel directions. It seems hardly necessary to point out that this speaks strongly in favor of a monophyletic origin for at least these two human races. However, the author cannot agree with the view, repeatedly expressed to him, that the presence of racial differences so early in development can be interpreted as an indication of great antiquity of the races of man. Ontogeny furnishes no proof in this problem, since the recapitulation theory cannot be applied to time; i. e., the time of first appearance of racial characters in prenatal development does not necessarily depend on the phylogenetic age of races. The author found, for instance, that the very recent races of pug—nosed and long—snouted dogs have their respective peculiarities indicated long before birth.
Clear and unquestionable secondary sexual differences could not be demonstrated in any of the body proportions; the general size, however, is slightly greater in the male than in the female during the last two months of prenatal life.
Individual differences in fetuses are very considerable; in other words, variability before birth is at least as pronounced as in adult life. This not only holds true for measurements but can be shown in even the smallest details. Individual characteristics in facial expression, for instance, can be readily recognized, after some experience, even in very young fetuses. The coefficients and relative ranges of variation for the proportions on the fetal body in specimens of approximately equal ages are in general about the same as for the corresponding proportions in adults; indeed, not infrequently they are even higher. As a rule, the variability is slightly greater in the first than in the second part of fetal development, and is certainly as fully pronounced in the smallest embryos as in fetuses. The variability in fetuses does not seem to be correlated with rapidity of growth, since the latter undergoes very marked changes. Here it may also be mentioned that the variability in the total length of the upper, as well as of the lower extremity, was found to be less than that of the single components of an extremity, which signifies that the parts of a limb show a tendency to compensate each other in their variations in length. For instance, in fetuses of equal ages the relative ranges of variation for the total length of the upper limb average 8.48; for the upper arm, 9.88; for the forearm, 9.20; and for the hand, 11.23.
Differences between the two halves of the body do not begin to develop in childhood, as is commonly supposed, but appear early in fetal life. They could be clearly demonstrated from the beginning of the fourth month on, and, with an especially precise technique, some asymmetries could no doubt be found even earlier. In fetuses from the fourth month to term the humerus, for instance, was longer on the right side in 57.6 per cent, longer on the left in 18.2 per cent, and equal on the two sides in 24.2 per cent of the cases. The difference in length of the two humeri amounted on an average to nearly 1 per cent of the smaller measurement.
From these general results it seems most probable that racial and individual differences, as well as asymmetries, are very closely dependent upon heredity. They certainly make their appearance very early in development, long before environment or function could exert any noteworthy inﬂuence. Secondary sexual differences, only, develop comparatively late, and then under the stimulation of the sex glands.
One of the most interesting problems regarding absolute measurements exists in their relative increments, particularly in the changes in these during the course of growth. These relative increments for all measurements on fetuses are greatest during the third month, whereafter they decrease rapidly up to the ninth month in case of measurements on the trunk, up to the eighth month in case of measurements on the limbs, and up to the eighth, ninth, or tenth month in case of the various measurements on the head. From these stages of fetal life to birth the relative increments increase again quite noticeably, which indicates a certain fluctuation in the rate of growth. This is exemplified in the accompanying table, which gives the averages of the relative weekly increments, within each month, of the anterior height of the trunk and of the biacromial diameter.
Month 3rd 4th 5th 6th 7th 8th 9th 10th
Ant. trunk ht . . . . . . . . . . . . . . .. 29.2 18.0 9.5 8.2 5.7 5.0 1.6 5.4
Biacrom.diarn, . . . . . . . . . . . . . .. 24.3 19.3 11.1 6.2 4.8 3.5 2.4 6.2
These figures decrease up to the ninth month and increase again in the tenth month. In addition they show that in the third month the rate of growth is greater in the height than in the width. In the fourth and fifth months this condition is reversed, only to change back again in the sixth, seventh, and eighth months. and to change a third time in the ninth and tenth months to a preponderance in rate of growth of the width diameter over the height diameter. Alternations such as that between growth rate of height and of width, or of extremity and of trunk, can be demonstrated in many measurements on the fetal body. It is well known that these ﬂuctuations, as well as alternations, in rate of growth occur during postnatal development, and it is of great interest to find them also during growth in utero.
The alternations in relative increments naturally lead to changes in proportions, and it is to such changes, particularly those occurring in fetal life, that special attention has been given by the author. Only the more general ones can be outlined in this paper; the trunk will be considered first, next the extremities, and lastly the head. Wherever the proportions differ in the two races this will be mentioned and an occasional comparison be made with conditions of growth in other primates. The author has examined a considerable number of these, representing various species, at different fetal stages as well as at older stages of development.
In general, the trunk becomes more and more slender as development advances, as evidenced by the fact that the circumference of the chest (at nipple height) amounts to 238 per cent of the trunk height (symphysion-suprasternale) in fetuses of 9 weeks, decreasing to 178 per cent in newborns and to 168, or slightly more, in adults. The width between the hips increases faster than the biacromial width. In white fetuses of 9 weeks the former constitutes only 58 per cent of the latter, but this percentage increases to 84 at birth and to 91 in adults. In negroes these figures are less than in whites at all stages of development; i. e., negroes have slightly narrower hips in relation to the shoulders. Analogous ontogenetic changes in this proportion between upper and lower breadth of the trunk take place also in other primates. The chest becomes relatively broader with advancing development; at 9 weeks its transverse and sagittal diameters are still practically alike, but very soon afterwards the former surpasses the latter. The umbilicus shifts to a relatively higher position on the trunk in the course of fetal as well as postnatal growth, a rule which seems to hold true also for all monkeys and apes. Man has the lowest placed nipples of any of the primates; this extreme position is not reached, however, until growth is completed, the nipples being situated higher in the fetus than in the adult. In relation to the ribs, the nipples overlie the second intercostal space in young fetuses, but have shifted down to the fourth intercostal space in adults. In fetuses of monkeys and apes the nipples occupy a relative position on the trunk similar to that in human fetuses, but in contrast to man, they shift upward in the course of growth, so that these d’ifierent specializations in man and monkey in regard to the position of the nipples are not attained until relatively late in life. In the human fetus the shoulders lie rather high above the suprasternal notch, so that the lateral ends of the clavicles stand much higher than their medial ends. In adult whites the clavicles, when in a position of rest, are horizontally posed, but in adults of primitive races they have descended less from their fetal position.
In relation to the height of the trunk, the total length of the upper extremity undergoes marked changes throughout the entire growth period; these consist of alternating increases and decreases. At nine weeks of intrauterine life the upper limb is still slightly shorter than the trunk; at ten weeks it has surpassed the latter, growing at a rapid rate up to the end of the fifth month, when its length is one and a half times the height of the trunk. For the whites measured by the author, this is the greatest relative length of the upper arm reached anywhere during growth. After the fifth month until birth a considerable decrease takes place in this relative measurement, but during postnatal life the upper extremity in general again surpasses the trunk height in rate of growth. The fact that the upper limb reaches a maximum relative length in the middle of fetal development may be regarded as lending support to the theory that at some time in the evolution of man his arms were longer than they are in recent human races.
The upper arm—forearm index increases during fetal life; in other words, the forearm grows faster than the upper arm. This stands in direct opposition to the claims made by Hamy, and more recently by Mendes Corréa, that the relative length of the forearm decreases in the course of intrauterine growth. These authors had measured only 22 and 10 specimens respectively, and these series are too small to reveal the typical age changes. As in man, the upper ann—forearm index in apes and monkeys is smaller in the fetus than in the adult; but of all primates man has the relatively shortest forearm. Adult negroes have longer forearms in relation to their upper arms than adult whites. This racial distinction appears early in fetal life and can be demonstrated at all subsequent stages of growth. A typical example for the alternations in growth rate in different parts of the body is furnished by the proportion between the length of the hand and that of the forearm. At 9 weeks of fetal life the former is nearly one—fifth longer than the latter; during the third and fourth months the forearm grows much more rapidly than the hand, so that the corresponding index drops in this short interval to less than 73; from the beginning of the fifth month to birth the hand again becomes relatively longer; i. e., the index rises steadily to about 95. finally, in postnatal life the index drops a second time to a considerable extent, the hand length in adults forming only 75 per cent of the forearm length. With advancing growth the hand becomes more and more slender, but is always slightly broader in whites than in negroes. The thumb, when measured from the styloid process of the radius to the tip of the digit, becomes steadily shorter, in relation to the greatest hand length, from the third month to birth and is, at all stages of growth, somewhat longer in whites than in negroes. The same ontogenetic reduction of the relative length of the thumb was found in other primates also, but here the final shortening goes much farther than in man. The place of attachment of the free thumb to the hand shifts more and more proxirnally in the course of development; in a fetus of 9 weeks the thumb branches off immediately beneath the base of the index finger, while in adults this branching occurs relatively much closer to the wrist. In fetuses of 8 weeks the transverse axis of the thumb, as determined by its nail anlage, forms a very small angle with the transverse axis of the other fingers; soon afterwards, however, the thumb rotates to nearly the extent of a right angle, assuming the typical position of opposability which it occupies in adult man. In all monkeys and apes the fourth finger is longer than the second; this relation holds true also for most negroes, but in the whites these two fingers, in over half _of all cases observed, were of equal length, and in more than 10 per cent of the cases the second finger even surpassed the fourth in length. These relations change but little throughout prenatal and postnatal development.
The proportion between the total length of the lower extremity (from the great trochanter to the sole of foot) and the height of the trunk changes very considerably during ontogeny. At 9 weeks of fetal life the length of the lower limb constitutes only 72 per cent of the trunk height; at the end of the third month the two measurements are alike; at the end of the fifth and during the sixth month the maximum in relative limb length of the entire fetal period is reached, being at one time 140 per cent of the trunk height. In the following months this index decreases again down to 116 in newborn whites. During postnatal life there takes place a second increase, which brings the index to 175 in male adult whites. This tremendous development of the lower limb in man is entirely unparalleled in other primates. However, this human distinction does not come about until comparatively late in growth, since at birth the relative length of the lower extremity in most monkeys and apes is fully as great as, if not greater than in the human newborn.
The thigh-leg index, like the corresponding index on the upper limb, increases in general with advancing growth; in fetuses of 9 weeks this index in the white race amounts to only 65, at birth it is 79, and in adults 84. Negroes have slightly higher values for this index from the end of the third prenatal month to adult life. It can be stated, therefore, that on both the upper and lower extremities the more distal parts, radius and tibia, grow faster than the proximal parts, humerus and femur, and are relatively longer in the negro than in the white. The foot, like the hand, becomes relatively narrower in the course of growth and, likewise, is relatively less broad in the negro than in the white fetus. Very early in fetal life the soles of the feet stand parallel to the midsagittal plane and thus face inward; during ontogeny the feet rotate until the soles face downward and occupy a horizontal position. This initial supinatorial position of the feet is not caused by conditions of space or pressure within the uterus, as has been assumed by some Writers, but is the result of an inherent law of fetal growth, causing many changes in at least the tarsal region, such as a slight rotation of the tuber calcanei and a shifting of the tarsus from the fibular to the tibial side. Typical for the negro, well marked even in small fetuses, is the prominence of the heel, which, as a rule, is due to a very thick layer of subcutaneous fat overlying the calcaneus.
The relation in length between the first three toes undergoes some important changes during development. In all monkeys and apes the middle toe surpasses all others in length, and it is interesting to note that man occasionally also conforms to this rule, although only for a very short transitory stage in his ontogeny, since in a fair percentage of fetuses from the end of the second and the beginning of the third month the middle toe is the longest. Very soon afterward the second toe becomes the longest in the large majority of cases; not until the fourth month does the great toe project farther than any of the other toes, and then only in a small minority of cases. The frequency of instances in which the great toe is shorter than toe II decreases in both races with advance in fetal development, but such cases always remain much more common in the negro than in the white. The human foot is very diﬂerent from the feet of other primates in adult life; however, early in intrauterine development this distinction is not nearly as pronounced. At this stage the hallux is markedly abduced and all metatarsals are divergent instead of parallel, as in the adult. Furthermore, in all primates, including man, the great toe at the beginning of fetal life is considerably shorter than the second toe, but in the course of growth the former approaches or even surpasses the latter in man, whereas in the other primates it becomes progressively shorter. The phalanges of the lateral toes are shorter than the corresponding metatarsals in young fetuses, both human and ape; but during development they become relatively still shorter in man and just the opposite, relatively much longer, in other primates. In some human fetuses of 8 weeks it was observed that the hallux was slightly rotated toward the other toes, and this in the sense of opposability; very soon afterwards, however, the transverse axis of the great toe runs in the same direction as the transverse axis of the lateral toes.
Relation Between Total Upper and Total Lower Extremity
This interrelation is best demonstrated in the intermembral index, which expresses the length of the former in percentage of the length of the latter. From 133 in fetuses of 9 weeks, this index in whites drops to 104 at the end of the sixth month; thereafter to birth the averages remain about the same. During postnatal life a second drop takes place in whites, reducing the index to 82.5 in the adult. From this it can be stated that the lower extremity grows faster than the upper during the first part of fetal development, and again during life after birth, and not until early infancy does the length of the lower limb surpass that of the upper. Negroes at all stages of growth have higher indices than whites; i. e., the upper extremity of the negro is slightly more developed in relation to the lower extremity, and this constantly from early fetal to adult life. The variability of the intermembral index is very small; in fact, there exists a surprisingly close correlation between the length of the upper and the length of the lower limb throughout growth, so that hardly any other two measurements on the body show such a constant proportion. Among all adult primates man has the longest lower limb, not only in relation to the trunk, as shown above, but also in relation to the upper limb. Only in man and some of the lower primates, the prosimiae, does the intermembral index sink below 100 when growth is completed; and even in the prosimiae the index never decreases to the extent shown in the human adult. This distinction between man and apes and monkeys, however, does not exist in earlier stages of development; inhuman fetuses the proportional lengths of the limbs are well within the range of variation of this proportion in fetuses or adults of other primates. In all the monkeys, in gorilla, and in man the interrnembral index is smaller in adults than in fetuses, a difference most pronounced in man. Only in chimpanzee, orang, and gibbon is a definite age change in this regard missing, due, most likely, to the specialized over-development of the arms in these apes.
Alongside of many striking resemblances in conditions of growth in the upper and lower extremities, a certain well-defined difference was found; i. e., the lower limb for a long period is a step behind the upper limb in development. This retardation of the lower, or acceleration of the upper limb, can be best recognized by means of the time of first appearance of (1) ossification centers in certain skeletal elements of the extremities, (2) cutaneous ridges on palm and sole, and (3) lanugo on arm and leg. All these features develop slightly later in the lower than in the upper extremity.
It remains to consider brieﬂy growth changes in the head. By measuring the greatest length, greatest width, and the height of the head, and dividing the total of these measurements by 3, the average head diameter is obtained. This diameter is expressed in percentage of the trunk height, thus giving a sensitive index for the relative size of the head. This index averages 95 in fetuses of 9 weeks; it decreases throughout growth, reaching 57 at birth and 31 in adults. In fetuses this relative head size was found to be slightly less in negroes than in whites, but in adults slightly greater. As in man, the index in all other primates decreases with advance in growth and the size of the index in monkeys and apes differs in general but little from that in man at corresponding stages of growth. For example, at birth man, With an index of 57, stands lower than orang and gibbon, with indices of 61 each, and is not far from chimpanzee, with an index of 50. At adult life man's index of 31 is equalled by such forms as the macaque and surpassed by Cebus, with its index of 39. Of the various head diameters the width is considerably more variable than the length or height. The cephalic index decreases during fetal life; in the third month it amounts on an average to 87 and may be as high as 98. The index which expresses the face height in percentage of the head height averages 48 in white fetuses of 9 weeks and increases to 59 in white newborns and to 85 in white adults. This indicates that the face grows in height at a more rapid rate than the cranial part of the head. In negroes this index is at all stages of development considerably larger than in whites. Likewise, a proportionally greater height of the negro face in fetuses, as well as in adults, is obtained when the upper face height (naso-buccal diameter) is brought into relation to the circumference of the head. This index increases during growth in most primates, just as in man. The face itself changes its general shape but little during fetal development, since the proportion between height and width remains about stationary from the third month to birth; only in postnatal growth does facial height increase more rapidly than facial width.
During development the eyes of man and of other primates move constantly closer together. This is best demonstrated when the interocular width is expressed in percentage of the bizygomatic width. This percentage relation averages 51.8 in human fetuses of 9 weeks but only 25 in white newborns and 23 in adult whites. The most rapid decrease occurs during the third and fourth fetal months. In orang-utan this relative interocular width amounted to 29.3 in a specimen from the middle of fetal development, to 19.1 in a newborn, and to 12.2 in a juvenile. In some primates, such as orang, baboon and Cebus, the relative narrowing of the distance between the eyes goes much farther than in man.
In relation to the upper facial height, the height of the nose decreases in general during prenatal growth, but increases again in postnatal life. In negroes this relative nasal height is constantly smaller than in whites. This is an indication, also, that the upper lip is lower in the latter than in the former. The nasal breadth in percentage of the bizygomatic breadth decreases very markedly during fetal growth; at 9 weeks it amounts to 36, while in white newborns it is only 24.7. In all negro fetuses, as well as in adults, the relative nasal breadth is very much greater than in whites of corresponding ages. From the foregoing it can be anticipated that the nasal index, also, must show a marked racial difference, with the larger values in the negroes. This index decreases from 145.1 in white fetuses of 9 weeks to 100.6 in newborns and to 62.1 in adults. The negro nose is not only relatively shorter and much broader than the white nose, but also considerably blunter and less prominent. All these differences become apparent as early as the third month of fetal life. Up to the end of the fourth month the nostrils are closed by epidermal plugs and are circular in form; after that time they become elongated, with their longitudinal axes in whites converging forward or, later on, even running parallel, while in negroes they usually occupy a transverse position.
In relation to the size of the head, the ear size increases with advance in fetal growth in all primates. The index used to express this relative ear size rises from an average of 1.3 in human (white) fetuses of 9 weeks to one of 5.9 in newborns, but decreases again thereafter to an average of 4.7 in adults. Man and orang-utan possess by far the relatively smallest ears of all the primates, and it is only in these two that the relative ear size was found to diminish again during postnatal growth. This can most likely be interpreted as an indication that in the evolution of man, as well as of orang, the ear has become smaller.
Many more growth changes and racial differences in fetuses could be enumerated, even from a study of the outer form alone. These examples, however, suffice to show that with anthropological investigations on ample fetal material, especially of different races, one enters an almost entirely untrod field, from which important additions to our knowledge of human growth may be expected. Itis also highly probable that systematic studies in this field, in connection with those on the ontogeny of primates other than man, will eventually shed new light on man’s evolution.
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