Difference between revisions of "Paper - Fetal age assessment by centers of ossification"

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==Introduction==
 
==Introduction==
  
This study was undertaken to extend into fetal life the
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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
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.
 
' Study made under (‘rile Scholarship Grant, summer 1934.
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251
 
251
  
A.\u‘.IucAx~’ JOURNAL or PHYSICAL AN‘l‘HROP0u)0Y. voL. xxiv. so. 8
+
A.\u‘.IucAx~’ JOURNAL or PHYSICAL AN‘l‘HROP0u)0Y. voL. xxiv. so. 8 JANUARY-MARC!-I. 1939 252 ALFRED H. HILL
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
+
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.
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
+
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.
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
+
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.
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.
+
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
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
+
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.
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
+
TABLE 1 Specimens studied. Length of pregnancy in lunar months
Specimens studied. Length of pregnancy in lunar months
 
  
stat“; “,9 White Negro
+
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
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.’
 
' Including all those whose stated age was ‘term.’
  
’ Spina. bifida, anencephaly, clubfoot, achondroplasia, and certain other anomalies
+
’ Spina. bifida, anencephaly, clubfoot, achondroplasia, and certain other anomalies excluded from tables.
excluded from tables.
 
  
 
  
Table 2 gives the distribution according to crown-rump
+
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
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
+
found only in the early months of fetal life where our values tend to be higher than Mall ’s. 254 ALFRED H. HILL
tend to be higher than Mall ’s.
 
254 ALFRED H. HILL
 
  
Sex difl’erences in maturity appear in our records during
+
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
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
+
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
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
+
‘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.
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
+
‘This is the earliest age at which there is a distinguishable sex difference in C-R length.
C-R length.
 
  
in the tables or the graphs. This uniformity in maturity
+
in the tables or the graphs. This uniformity in maturity progress is harmonious with that found by Todd in postnatal life (’33). RECORDS
progress is harmonious with that found by Todd in postnatal
 
life (’33).
 
RECORDS
 
  
It was decided, after a preliminary survey, to chart the
+
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
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
+
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.
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
+
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.
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
 
TABLE 3
Line 211: Line 91:
 
Visualization of semicircular canals
 
Visualization of semicircular canals
  
0-]? age Numbar in Oanala Per cent
+
0-]? age Numbar in Oanala Per cent (montha) group avidam incidence 2 3 0 0 3 19 12 63 4 32 32 100
(montha) group avidam incidence
 
2 3 0 0
 
3 19 12 63
 
4 32 32 100
 
  
 
Obsouratian of semicircular canals
 
Obsouratian of semicircular canals
  
0,}; am, Numb“. ,-,, Percentage obncurad Percentage obacurad
+
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
(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
+
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.
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
+
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
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
+
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
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
 
Vertebral column. N umber of centra
  
Gestation age Per cent
+
Gestation age Per cent in lunar Extremes Average flodal frequency months in number number number of mode
in lunar Extremes Average flodal frequency
 
months in number number number of mode
 
  
2 17-26 20.3
+
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
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
 
10 28-31 29.3 29 58
  
Vertebral components. Upper cervical region transverse processes ossified but
+
Vertebral components. Upper cervical region transverse processes ossified but not centra
not centra
 
  
2 4
+
2 4 3 0-3 2.1 3 44 4 0-3 1.4 1 50 5 0-2 0.4 0 63
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
 
Sacral region. Centra ossified but not transverse processes
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2 3
 
2 3
  
3 0-3 2 2 50
+
3 0-3 2 2 50 4 0-2 1 .1 1 50 5 0-4 0.6 0 63
4 0-2 1 .1 1 50
 
5 0-4 0.6 0 63
 
  
The vertebral column undergoes rapid ossification during
+
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
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
+
shape particularly in centra. Neural arches are difficult of interpretation in anteroposterior View but ossified portions of the transverse processes progressively approximate the centra.
interpretation in anteroposterior View but ossified portions
 
of the transverse processes progressively approximate the
 
centra.
 
  
The earliest embryo studied shows ossification points in
+
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
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
+
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
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
 
Inferior extremity
  
2 X-rays not clear
+
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
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
+
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.
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
+
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
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
+
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.
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
+
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.
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
+
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
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
+
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
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
+
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
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
+
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).
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
+
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).
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
+
The calcaneus is followed scarcely a month later by the talus which should show an ossific center when the fetus has
talus which should show an ossific center when the fetus has
 
  
reached 6 lunar months and a C-R length of about 235 mm.
+
reached 6 lunar months and a C-R length of about 235 mm. (table 7 ). 260 ALFRED H. HILL
(table 7 ).
 
260 ALFRED H. HILL
 
  
Sexual diflerence in the time of appearance of centers up
+
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.
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
+
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.).
birth. It ossifies somewhat more frequently in female than in
 
male fetuses of each age group (table 7.).
 
  
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
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
+
5 54 0 0 6 74 2 3 7 67 1 2 8 62 7 11 36 M 1 3
6 74 2 3
 
7 67 1 2
 
8 62 7 11
 
36 M 1 3
 
  
 
26 F 6 24
 
26 F 6 24
  
9 48 11 23
+
9 48 11 23 27 M 3 11
27 M 3 11
 
  
 
21 F 8 38
 
21 F 8 38
  
10 85 41 48
+
10 85 41 48 50 M 23 46
50 M 23 46
 
  
 
35 F 18 51
 
35 F 18 51
  
When development has proceeded to the point Where the
+
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
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
+
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
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
+
5 54 0 0 6 7 4 1 1 41 M 1 2
6 7 4 1 1
 
41 M 1 2
 
  
 
33 F 0 0
 
33 F 0 0
  
7 67 3 4
+
7 67 3 4 48 M 2 4
48 M 2 4
 
  
 
19 F 1 5
 
19 F 1 5
  
8 62 23 37
+
8 62 23 37 36 M 7 19
36 M 7 19
 
  
 
26 F 16 62
 
26 F 16 62
  
9 50 42 84
+
9 50 42 84 28 M 22 79
28 M 22 79
 
  
 
22 F 20 91
 
22 F 20 91
  
10 85 82 96
+
10 85 82 96 50 M 47 94
50 M 47 94
 
  
 
35 F 35 100
 
35 F 35 100
Line 504: Line 199:
 
Proximal tibial epiphysis
 
Proximal tibial epiphysis
  
7 67 0 0
+
7 67 0 0 8 62 6 10 36 M 1 3
8 62 6 10
 
36 M 1 3
 
  
 
26 F 5 19
 
26 F 5 19
  
9 50 16 32
+
9 50 16 32 28 M 5 18
28 M 5 18
 
  
 
22 F 11 50
 
22 F 11 50
  
10 84 57 68
+
10 84 57 68 49 M 32 65
49 M 32 65
 
  
 
35 F 25 71
 
35 F 25 71
  
cally all fetuses at birth have an ossified femoral epiphysis,
+
cally all fetuses at birth have an ossified femoral epiphysis, less than 75% show a bony center for upper tibial epiphysis.
less than 75% show a bony center for upper tibial epiphysis.
 
  
The curves of ossification of cuboid and of epiphyses for
+
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
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
+
month in duration and as there is no constitutional handicap present to prolong its duration all trace is lost before birth.
present to prolong its duration all trace is lost before birth.
 
  
There is an obvious contrast in the curves for coracoid
+
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
process and humeral head. The center for the coracoid process
 
of the scapula appears before birth in a limited percentage
 
  
 
TABLE 9
 
TABLE 9
Line 539: Line 223:
 
Coracoid process
 
Coracoid process
  
0-R age Number in Center Per cent
+
0-R age Number in Center Per cent (months) aroup present inchicnco
(months) aroup present inchicnco
 
  
6 67 0 0
+
6 67 0 0 7 66 1 2 47 M 1 2
7 66 1 2
 
47 M 1 2
 
  
 
19 F 0 0
 
19 F 0 0
  
8 62 3 5
+
8 62 3 5 36 M 0 0
36 M 0 0
 
  
 
26 F 3 12
 
26 F 3 12
  
9 50 6 12
+
9 50 6 12 28 M 3 11
28 M 3 11
 
  
 
22 F 3 14
 
22 F 3 14
  
10 86 12 14
+
10 86 12 14 51 M 6 12
51 M 6 12
 
  
 
35 F 6 17
 
35 F 6 17
Line 565: Line 243:
 
Humeral head
 
Humeral head
  
7 67 0 0
+
7 67 0 0 8 62 2 3 36 M 1 3
8 62 2 3
 
36 M 1 3
 
  
 
26 F 1 4
 
26 F 1 4
  
9 50 6 12
+
9 50 6 12 28 M 1 4
28 M 1 4
 
  
 
22 F 5 23
 
22 F 5 23
  
10 84 23 27
+
10 84 23 27 49 M 11 22
49 M 11 22
 
  
 
35 F 12 34
 
35 F 12 34
  
of male fetuses against a somewhat greater percentage of
+
of male fetuses against a somewhat greater percentage of female fetuses (tables 9, 11).
female fetuses (tables 9, 11).
 
  
Considerably higher in its percentage of incidence is the
+
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
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
+
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).
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
+
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).
a C-R length of near 350 mm. (tables 10, 11).
 
  
Centers for the alar processes of the sacrum appear rather
+
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
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
+
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY, VOL. XXIV, N0. 3 264 ALFRED H. HILL
264 ALFRED H. HILL
 
  
the lagging centers may be long delayed. The third center
+
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.
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.
 
Centers for lateral cuneiform and proximal femoral epiphysis appear in but 2% and 1%, respectively, of term fetuses.
Line 639: Line 273:
 
TABLE 10
 
TABLE 10
  
Capitate
+
Capitate 0-1? and Number in Canter Per cent (months) yroup present fncidonce
0-1? and Number in Canter Per cent
 
(months) yroup present fncidonce
 
  
 
8 62 0 0
 
8 62 0 0
  
9 50 1 2
+
9 50 1 2 28 M 0 0
28 M 0 0
 
  
 
22 F 1 5
 
22 F 1 5
  
10 86 9 10
+
10 86 9 10 51 M 5 10
51 M 5 10
 
  
 
35 F 4 11
 
35 F 4 11
Line 659: Line 289:
 
8 62 0 0
 
8 62 0 0
  
9 50 2 4
+
9 50 2 4 28 M 0 0
28 M 0 0
 
  
 
22 F 2 9
 
22 F 2 9
  
10 86 10 12
+
10 86 10 12 51 M 5 10
51 M 5 10
 
  
 
35 F 5 14
 
35 F 5 14
  
No sexual difierence exists between the incidence of the
+
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.
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
+
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
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
 
TABLE 11
Line 684: Line 305:
 
Coracoid process
 
Coracoid process
  
Gestation
+
Gestation ago, lunar Number in Center _Pe_r cent
ago, lunar Number in Center _Pe_r cent
 
  
 
month: group prount mmdenco
 
month: group prount mmdenco
Line 691: Line 311:
 
6 71
 
6 71
  
7 108
+
7 108 69 M 39 F
69 M
 
39 F
 
  
8 36
+
8 36 20 M 16 F
20 M
 
16 F
 
  
9 12
+
9 12 6M 6F 10 121 1 73 M 48F
6M
 
6F
 
10 121 1
 
73 M
 
48F
 
  
 
H wmeral head
 
H wmeral head
Line 710: Line 321:
 
71
 
71
  
7 109
+
7 109 69 M 40 F
69 M
 
40 F
 
  
8 37
+
8 37 21 M 16 F
21 M
 
16 F
 
  
9 12
+
9 12 6M 6F
6M
 
6F
 
  
10 122 32 26
+
10 122 32 26 73 M 18 25 49 F 14 29
73 M 18 25
 
49 F 14 29
 
  
 
Capitate
 
Capitate
  
G
+
G [0010 NON I-H-‘MO KIQUI 03°10 MON D-‘I-‘KOO
[0010 NON I-H-‘MO KIQUI 03°10 MON D-‘I-‘KOO
 
  
 
6 71
 
6 71
  
109
+
109 69 M 40 F
69 M
 
40 F
 
  
8 37
+
8 37 21 M 16 F
21 M
 
16 F
 
  
9 12
+
9 12 6M 6F
6M
 
6F
 
  
10 123
+
10 123 75 M 48 F
75 M
 
48 F
 
  
 
Hamate
 
Hamate
  
G3 *1
+
G3 *1 O3|&\l|-‘OD-II-‘OI-IO!-H-‘O G5OI¢>‘lO® @009 00-19-10
O3|&\l|-‘OD-II-‘OI-IO!-H-‘O
 
G5OI¢>‘lO® @009 00-19-10
 
  
 
71
 
71
  
109
+
109 69 M 40 F
69 M
+
 
40 F
+
1
 +
21M 16F
  
*1
+
6M 6F
  
21M
+
10 122 74 M 48 F
16F
 
  
6M
+
UHk® I-‘OI-I D-‘OI-I O0-H-‘ O B-5 I-0 OUINI ‘IOQ 93060 Oi-H-‘ O
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
 
 
{{Footer}}
 
{{Footer}}
 
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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.



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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



Cite this page: Hill, M.A. (2020, September 26) Embryology Paper - Fetal age assessment by centers of ossification. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Fetal_age_assessment_by_centers_of_ossification

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