Paper - Fetal age assessment by centers of ossification

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Hill AH. Fetal age assessment by centers of ossification. (1939) Amer. J Phys. Anthropol. 24(3): 251-264.

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This 1939 paper by Hill attempts to age fetuses based upon their bone ossification. Modern Pages: Musculoskeletal Links: Introduction | mesoderm | somitogenesis | limb | cartilage | bone | bone timeline | bone marrow | shoulder | pelvis | axial skeleton | skull | joint | skeletal muscle | muscle timeline | tendon | diaphragm | Lecture - Musculoskeletal | Lecture Movie | musculoskeletal abnormalities | limb abnormalities | developmental hip dysplasia | cartilage histology | bone histology | Skeletal Muscle Histology | Category:Musculoskeletal Historic Embryology - Musculoskeletal   1853 Bone | 1885 Sphenoid | 1902 - Pubo-femoral Region | Spinal Column and Back | Body Segmentation | Cranium | Body Wall, Ribs, and Sternum | Limbs | 1901 - Limbs | 1902 - Arm Development | 1906 Human Embryo Ossification | 1906 Lower limb Nerves and Muscle | 1907 - Muscular System | Skeleton and Limbs | 1908 Vertebra | 1908 Cervical Vertebra | 1909 Mandible | 1910 - Skeleton and Connective Tissues | Muscular System | Coelom and Diaphragm | 1913 Clavicle | 1920 Clavicle | 1921 - External body form | Connective tissues and skeletal | Muscular | Diaphragm | 1929 Rat Somite | 1932 Pelvis | 1940 Synovial Joints | 1943 Human Embryonic, Fetal and Circumnatal Skeleton | 1947 Joints | 1949 Cartilage and Bone | 1957 Chondrification Hands and Feet | 1968 Knee

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Hill AH. Fetal age assessment by centers of ossification. (1939) Amer. J Phys. Anthropol. 24(3): 251-264.

VOL. XXIV, N0. 3 264 ALFRED H. HILL

Fetal Age Assessment By Centers Of Ossification

Alfred H. Hill

Anatomical Laboratory and Associated Foundations, Western Reserve University, Cleveland, Ohéo

OONTENTS Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251 Records . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254 Comparison of methods of age determination . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266 Summary and timetable . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268

Introduction

This study was undertaken to extend into fetal life the principles of maturity assessment devised for postnatal life by Dr. Wingate Todd and elaborated by him in the Atlas of Skeletal Maturation (’37). The basis of this maturity assessment is, first, that symbols of progressive maturation are to be found in the connective tissues of the bodily framework and, secondly, that owing to its radio-opaque mineral the symbols are most readily deciphered in the skeleton. It has been pointed out however that, owing to interferences in the process of mineralization, skeletal symbols of maturation may be obscured or the objective record of their progress inhibited. This is the more striking when the record depends upon the appearance of a center of ossification and that appearance is delayed owing to failure of mineralization, a failure Particularly liable to occur between 3 and 12 months after birth. Fortunately the secondary centers tend to appear in sheaves so that if one is delayed the others in the sheaf carry on the consecutive record. In fetal life the record of maturity must

' Study made under (‘rile Scholarship Grant, summer 1934.

251

A.\u‘.IucAx~’ JOURNAL or PHYSICAL AN‘l‘HROP0u)0Y. voL. xxiv. so. 8 JANUARY-MARC!-I. 1939 252 ALFRED H. HILL

depend largely on the appearance of centers since subepiphysial surfaces are not yet defined and therefore cannot assist the identification. Because of the protection against nutritional deficiency and intercurrent maladies afforded by prenatal existence it may be expected that variability in date of appearance of the several centers will not be as marked as in infancy.

The material upon which this study is made, some 500 fetuses, was obtained in the routine manner, most being spontaneous abortions or miscarriages of dispensary mothers. A few are from the private ward service. All were received within 48 hours of delivery. Measurements and roentgenograms were made immediately upon receipt and before fixation.

Data were obtained by direct record from the roentgenograms, the observations being classified both by stated age from the clinical records and by crown-rump length. All observations on monsters and any questionable data on the several centers are eliminated from the final results recorded in the tables. Data from certain fetuses of which the crownrump length was not measured until after fixation are also eliminated from the final consideration.

Table 1 gives the distribution upon the basis of stated age. In practice this resulted in certain irregularities of the maturation curves for the several centers. For this reason as well as its incompatibility with other studies of fetal anatomy in the literature it was abandoned though a complete file of records and curves constructed upon this basis is preserved in the laboratory. It is not however certain that the standards determining fetal age by crown-rump length made by Mall many years ago ('08) hold good now. In the interval the establishment of prenatal dispensaries and other aids to the more appropriate nourishment and prenatal care of expectant mothers may easily have modified the fetal growth curve. Moreover, as Doctor Dodge has shown, there is a marked racial difference in size of newborn babies, the Irish and the Russian Jews being the heaviest and the Negroes the lightest in Cleveland records (to be published). Babies born of small FETAL AGE BY CENTERS or OSSIFICATION 253

sized parents may themselves be smaller than average. At what date in fetal life this distinction first appears we do not know. It may well be first evident in the seventh fetal month for it is then that we find recognizable differences in size between male and female fetuses (table 2). Even with this reservation upon crown-rump length in later fetal life it is unquestionably the most reliable indicator of age.

TABLE 1 Specimens studied. Length of pregnancy in lunar months

stat“; “,9 White Negro tmontha) Male Female Male Female Total 2 1 0 1 1 3 3 9 2 2 1 14 4 9 3 3 1 16 5 27 20 9 11 67 6 30 21 12 3 71 7 48 24 21 16 109 8 10 I 1 11 5 37 9 5 2 1 4 12 10 ‘ 55 33 20 16 124 Total 194 116 80 63 Grand total 310 143 -453Terata ’ 5 7 3 2 17

' Including all those whose stated age was ‘term.’

’ Spina. bifida, anencephaly, clubfoot, achondroplasia, and certain other anomalies excluded from tables.

Table 2 gives the distribution according to crown-rump length computed from our own series in the following manner. An average was struck on the crown-rump lengths of all fetuses whose stated age was 2% or 3 months and set down as the mean value for the third fetal month. Mean values were calculated for each succeeding fetal month and from these the ranges were computed. Thereafter any fetus of crown-rump length falling within a given range was allocated to the age defined by that range without regard to stated age. These mean crown-rump lengths conform rather well with those established by Mall (’08), practical discrepancies being

found only in the early months of fetal life where our values tend to be higher than Mall ’s. 254 ALFRED H. HILL

Sex difl’erences in maturity appear in our records during the seventh fetal month and are set forth in the tables and graphs: diflerences in dimensions are evident also in the seventh month. Differences between racial stocks were not found and hence no discrimination of race or stock is made

TABLE 2 Crown-rump length classification S03 and Moan 0-R 0-)? «ye number in Length range length (months) group (millimeters) (millimeters) 2 3 Up to so 69 3 19 81-135 115 ‘ 4 32 136-175 157 5 54 176-215 194 6 74 216-255 233 41 M 33 F 7 ’ 67 256-285 272 48 M 274 19 F 268 8 62 286-315 298 36 M 298 26 F 298 9 50 316-340 332 28 M 333 22 F 332 10 86 340-up 348 51 M 349 35 F 346 Total 1147

‘This is the average C-R length of all fetuses whose stated age was 29 or 3 months and indicates the basis for setting up the grouping in GR age.

‘This is the earliest age at which there is a distinguishable sex difference in C-R length.

in the tables or the graphs. This uniformity in maturity progress is harmonious with that found by Todd in postnatal life (’33). RECORDS

It was decided, after a preliminary survey, to chart the appearance of the various centers over their period of development and graph the results. From the groupings in the FETAL AGE By cmrrnss or ossrrrcmrron 255

graphs it would then be possible to focus the attention of an investigator upon a few critical points in any age range for determination of status of the fetus in question.

The semicircular canals become visualized through mineralization of their ensheathing tissue early in the embryo, and should be evident by the end of the third lunar month of development (table 3). During the ossification of their ensheathing tissue they stand out rather clearly due to the light mineralization of petrous and squamous temporal bone.

TABLE 3

Visualization of semicircular canals

0-]? age Numbar in Oanala Per cent (montha) group avidam incidence 2 3 0 0 3 19 12 63 4 32 32 100

Obsouratian of semicircular canals

0,}; am, Numb“. ,-,, Percentage obncurad Percentage obacurad (months) group Slightly Partly Almost Wholly 4 32 0 0 0 0 5 54 1 2 0 0 6 74 5 7 1 1 7 67 21 31 1 2 8 62 31 50 3 5 9 49 32 65 1 1 22 10 86 31 36 44 5 1

They stand out much more obtrusively than one would anticipate from their adult dimensions for their extraordinarily early attainment of practically adult size is strikingly disproportionate to the development of surrounding structures at this age.

With increasing mineralization of the squamous and petrous temporal the semicircular canals become less clearly defined. The canal walls share in the deficient mineralization of a saltpoor fetus and hence the relative obscurity of the canals does not seem to be much affected by the level of mineral health. The relative obscurity of the canals has seemed to 256 ALFRED H. HILL

us to be some index of the development of the fetus. We have classified canals as slightly, partly, almost and wholly obscured. The first two and last two characterizations have been grouped and computed in table 3. From the table it is seen that from the eighth month to birth they are almost invariably barely or partly obscured: at birth they tend to lose their definition in the increasing mineralization of envelop ing tissue. TABLE 4

Vertebral column. N umber of centra

Gestation age Per cent in lunar Extremes Average flodal frequency months in number number number of mode

2 17-26 20.3 3 23-29 25.2 25 35 4 22-28 26.3 27 31 5 26-29 28.1 28 39 6 27-30 28.5 29 59 7 27-30 28.9 29 71 3 28-31 29.1 29 73 9 28-30 29.1 29 75

10 28-31 29.3 29 58

Vertebral components. Upper cervical region transverse processes ossified but not centra

2 4 3 0-3 2.1 3 44 4 0-3 1.4 1 50 5 0-2 0.4 0 63

Sacral region. Centra ossified but not transverse processes

2 3

3 0-3 2 2 50 4 0-2 1 .1 1 50 5 0-4 0.6 0 63

The vertebral column undergoes rapid ossification during the early months of prenatal life. From the fifth month onward it is rather stable in number of components. One or two ossified segments may be added at the caudal end in later months. Table 4, drawn up in lunar months for convenience of interpretation, indicates the mode, the average number and the extremes found in each age group. The changes produced by time are more strikingly those of form, size and FETAL AGE BY CENTERS or OSSIFICATION 257

shape particularly in centra. Neural arches are difficult of interpretation in anteroposterior View but ossified portions of the transverse processes progressively approximate the centra.

The earliest embryo studied shows ossification points in both transverse processes and centra of the lower thoracic and upper lumbar regions. Upward of this area transverse processes alone are ossified; downward from it are several

TABLE 5 Phalanyes. Superior extremity Ranga Per cent 0-R (lot number Average Modal /requnury (months) unified number number of mode 2 9-12 10.5 None 3 11-14 13.5 14 75 4 14 14 14 100

Inferior extremity

2 X-rays not clear 3 9-11 9.6 9 80 4 9-13 10.3 10 48 5 9-13 11.3 11 48 6 9-14 11.7 11 32 7 10-14 12.1 13 45 8 10-14 12.2 13 35 10-14 M 11.9 13 34 11-14 F 12.5 13 36 9 10-14 12.6 13 49 10-14 M 12.5 13 56 11-14 F 12.8 13 41 10 9-14 12.6 13 56 11-14 M 12.6 13 59 9-14 F 12.6 13 53

centra but no transverse processes. By the fifth month this asymmetrical progress of ossification has come to an end (table 4). It is noted that at 3 lunar months the modal vertebral column presents ossification centers in the transverse processes alone of cervical segments 1, 2 and 3 and in the centra only of sacral segments 3 and 4.

The centers for phalanges of the hand appear rather early and their number should be complete in an embryo of the third month with a C-R length of 155 mm. (table 5). The phalanges 258 ALFRED H. HILL

of the foot, however, ossify much more erratically, and are usually incomplete in number at term. The percentage incidence of the modal number does not increase as fetal age progresses. This , of course must mean that whatever phalanges do not ossify by the end of the fourth month have very little, though some, chance of ossifying. The order of appearance in the hand digits, I-V proximal, I-V terminal, then II to V middle in ascending order, holds for the lower extremity with V middle phalanx lacking in a majority of the specimens examined at birth. In a few embryos terminal phalanx V was lacking and the middle phalanx of this digit present (table 5). The failure of middle phalanx of digit V to ossify, and the less frequent failure of terminal phalanx V and middle phalanx IV, is in conformity with the findings recorded in the Atlas of Skeletal Maturation (Todd, ’37) and the observations made by Francis and Werle on the appearance of centers after birth (’39). The occasional absence of an ossific center for terminal phalanx V must not blind the reader to the fact that records of the vagaries in ossification of phalanges and their epiphyses plainly demonstrate the vestigial nature of the middle phalanges of the toes, more especially IV and V.

The ilium is the first element of the os coxae to ossify and is present in every embryo of this series as well as in the fetuses. It must certainly ossify during the second month. The ischium appears during the third or fourth month with little variation as evidenced by the curve of its incidence. It should be bilaterally present at the end of the third or early in the fourth fetal month (table 6). Five months of development suflice to bring the pubis into the x-ray picture. It apparently is more subject to delay than the ischium (table 6) and its percentage curve of presence therefore shows a more oblique incline with a refractory termination.

The characteristic curves of commencing ossification in the ilium, ischium and pubis offer significant information on the progress of development. During the second month when the ilium ossifies the rate is great. Precision extends from FETAL AGE BY CENTERS OF OSSIFICATION

time to substance and each stage must be completed 011 schedule: there is no lag evidenced in ossification of ilium. The curve of ischium is like that of ilium, steep and abrupt in termination though its slope is more obliquely inclined. Pubis, however, in which ossification begins in the fourth month when ossification of isehium has already reached 100%, shows a more sloping curve consistent with a rate of development slower in fetal than in embryonic life. The refractory termination on the pubic curve extending over 7 and 8 months is an early example of lag in a symbol of maturity. Failure of

TABLE 6 I schium Per cent 0~R ape Number in Center frequency (months) group present of mode 2 3 0 0 3 19 9 47 4 32 32 100 Pubis 3 19 0 0 4 32 7 22 5 53 32 60 6 7 4 63 85 7 67 66 99 8 62 61 98 9 50 50 100

ossific centers to appear on time is far more typical of postnatal than of fetal life. Its interpretation is therefore more fully considered in the publications of Todd (’37) and of Francis and Werle (’39).

The calcaneus is the first of the tarsals to ossify and is visible in a well«developed embryo of 5 lunar months whose C-R length approximates 195 mm. (table 7).

The calcaneus is followed scarcely a month later by the talus which should show an ossific center when the fetus has

reached 6 lunar months and a C-R length of about 235 mm. (table 7 ). 260 ALFRED H. HILL

Sexual diflerence in the time of appearance of centers up to and through 6 lunar months is not appreciable and therefore is not evident in ossification of talus.

The cuboid is not to be expected until or shortly before birth. It ossifies somewhat more frequently in female than in male fetuses of each age group (table 7.).

TABLE 7 Caloaneus 0-R ag¢ N umber in Canter Per cent (months) group present incidence 3 19 0 0 4 31 8 26 5 52 30 58 6 73 66 90 7 66 66 100 Talus 3 19 0 0 4 32 1 3 5 54 3 6 6 72 40 55 7 67 64 96 8 62 62 100 Cuboid

5 54 0 0 6 74 2 3 7 67 1 2 8 62 7 11 36 M 1 3

26 F 6 24

9 48 11 23 27 M 3 11

21 F 8 38

10 85 41 48 50 M 23 46

35 F 18 51

When development has proceeded to the point Where the distal femoral epiphysis is beginning to ossify, sexual-differences are evident so that mineralization may be expected 4- to 1 month later in the male than in the female fetus. At 8 C-R fetal months an ossific center should be present in the female and a month later in the male (table 8). FETAL AGE BY CENTERS or OSSIFICATION 261

About 1 month after the distal femoral epiphysis ossifies the proximal tibial center appears, a comparable difierence existing between the date of appearance in the two sexes (table 8). However, in contrast with the fact that practi TABLE 8 Distal femoral epiphysis 0-1? we Number in Center Per cent (months) group present incidence

5 54 0 0 6 7 4 1 1 41 M 1 2

33 F 0 0

7 67 3 4 48 M 2 4

19 F 1 5

8 62 23 37 36 M 7 19

26 F 16 62

9 50 42 84 28 M 22 79

22 F 20 91

10 85 82 96 50 M 47 94

35 F 35 100

Proximal tibial epiphysis

7 67 0 0 8 62 6 10 36 M 1 3

26 F 5 19

9 50 16 32 28 M 5 18

22 F 11 50

10 84 57 68 49 M 32 65

35 F 25 71

cally all fetuses at birth have an ossified femoral epiphysis, less than 75% show a bony center for upper tibial epiphysis.

The curves of ossification of cuboid and of epiphyses for lower femur and upper tibia illustrate quite vividly the sexlinked lag in the male with the obscuration of the lag which rapidly occurs in constitutional health. The lag is of but 1 262 ALFRED 11. HILL

month in duration and as there is no constitutional handicap present to prolong its duration all trace is lost before birth.

There is an obvious contrast in the curves for coracoid process and humeral head. The center for the coracoid process of the scapula appears before birth in a limited percentage

TABLE 9

Coracoid process

0-R age Number in Center Per cent (months) aroup present inchicnco

6 67 0 0 7 66 1 2 47 M 1 2

19 F 0 0

8 62 3 5 36 M 0 0

26 F 3 12

9 50 6 12 28 M 3 11

22 F 3 14

10 86 12 14 51 M 6 12

35 F 6 17

Humeral head

7 67 0 0 8 62 2 3 36 M 1 3

26 F 1 4

9 50 6 12 28 M 1 4

22 F 5 23

10 84 23 27 49 M 11 22

35 F 12 34

of male fetuses against a somewhat greater percentage of female fetuses (tables 9, 11).

Considerably higher in its percentage of incidence is the center for humeral head though its presence at birth can be expected in a third or less of full term babies. FETAL AGE BY CENTERS or ossnvrcacrron 263

By the time of birth there is a distinct tendency for centers to appear in the female earlier than in the male though this preponderance in favor of the female is neither very great nor very stable until far on in childhood as is clearly shown in the Atlas (Todd, ’37). In fetal life at least the sex difference seems much more pronounced in earlier miscarriages than in those which occur nearer full term. This point is worthy of careful consideration. The distinction is evident in ossification of the cuboid (table 7) a center better suited for this inquiry than lower femoral or upper tibial epiphysis where there seems simply to be a short lag in the male. For the cuboid, on the contrary, scarcely 50% of full term babies of either sex show a bony center, but in the eighth and ninth lunar months (C-R basis) an overwhelming preponderance of those which show the center are females. Now the crownrump basis obscures features like this by assuming that small fetuses are necessarily young fetuses. Doubtless this is so for all but those approaching term when, as we have indicated, differences in size linked with stock, race, family strain and sex begin to show themselves. It is probably in fetuses of crown-rump designation 9 and 10 months that an unnecessary confusion is injected into the problem. Nevertheless, as the curves for cuboid show, the fact, though obscured, is still evident. We have set up graphs for coracoid process, humeral head, capitate and hamate constructed on length of pregnancy in addition to those on the C-R basis in order to emphasize our contention that the more extremely divergent examples of humanity tend to elimination. The deaths which occur at or about full term show, as do the living infants of the Inquiry, relatively little sex distinction in the skeletal roentgenograms (Todd, ’37).

The hamate and capitate centers appear in a few well-advanced fetuses of 10 lunar months gestation which have reached a C-R length of near 350 mm. (tables 10, 11).

Centers for the alar processes of the sacrum appear rather early in the developmental period (table 12). Two centers should appear on each side in the eighth month. Failing this

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY, VOL. XXIV, N0. 3 264 ALFRED H. HILL

the lagging centers may be long delayed. The third center on each side, if it occurs at all, is not present till after birth. One must remember, however, that the iliac articulation usually covers only two and a half sacral vertebrae and that even so much is of phylogenetically recent development, for the anthropoid apes usually possess an articulation involving no more than two sacral vertebrae.

Centers for lateral cuneiform and proximal femoral epiphysis appear in but 2% and 1%, respectively, of term fetuses.

TABLE 10

Capitate 0-1? and Number in Canter Per cent (months) yroup present fncidonce

8 62 0 0

9 50 1 2 28 M 0 0

22 F 1 5

10 86 9 10 51 M 5 10

35 F 4 11

Hamate

8 62 0 0

9 50 2 4 28 M 0 0

22 F 2 9

10 86 10 12 51 M 5 10

35 F 5 14

No sexual difierence exists between the incidence of the hyoid center in males and females and its incidence in any age group can be but hesitantly predicted. It is present in well-developed babies at birth, but its absence should cause no suspicion of delayed development. Table 13 illustrates its incidence in the various groups.

Another pair of centers frequently met with (60% in the oldest group) should be noted in passing. The centers are plainly homologous with those of the ribs and appear opposite 07. To this group must be added the true cervical

TABLE 11

Coracoid process

Gestation ago, lunar Number in Center _Pe_r cent

month: group prount mmdenco

6 71

7 108 69 M 39 F

8 36 20 M 16 F

9 12 6M 6F 10 121 1 73 M 48F

H wmeral head

71

7 109 69 M 40 F

8 37 21 M 16 F

9 12 6M 6F

10 122 32 26 73 M 18 25 49 F 14 29

Capitate

G [0010 NON I-H-‘MO KIQUI 03°10 MON D-‘I-‘KOO

6 71

109 69 M 40 F

8 37 21 M 16 F

9 12 6M 6F

10 123 75 M 48 F

Hamate

G3 *1 O3|&\l|-‘OD-II-‘OI-IO!-H-‘O G5OI¢>‘lO® @009 00-19-10

71

109 69 M 40 F

1 21M 16F

6M 6F

10 122 74 M 48 F

UHk® I-‘OI-I D-‘OI-I O0-H-‘ O B-5 I-0 OUINI ‘IOQ 93060 Oi-H-‘ O

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