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Developmental age estimated by bone-length measurement in human fetuses.

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THE ANATOMICAL RECORD 209547-552 (1984)
Developmental Age Estimated by Bone-Length
Measurement in Human Fetuses
ENDRE KELEMEN, MARGIT JANOSSA, WENCESLAO CALVO, AND
THEODOR M. FLIEDNER
First Department of Medicine, Semmelweis University, Koranyi u 2/A, 1083
Budapest, Hungary E K . , M.J.1 and Department of Clinical Physiology and
Occupational Medicine, Uniuersity of Ulm, 7900 U l d D o n a u , Federal
Republic of Germany (H?C., l7M.F)
ABSTRACT
The lengths of 491 long bones of the extremities derived from
193 freshly delivered human fetuses of 7 to 22 weeks fertilization age were
measured. Fetuses delivered after spontaneous abortion, twin pregnancy, or
known maternal disease were excluded. The correlation between fetal age
(measured by crown-rump length) and bone length was linear. The term “developmental age” was used for bone length-derived age values. Developmental
age can be determined from the length of even a single bone, i.e., when
mechanical injury of the delivered fetus inhibits crown-rump length measurement. The results could aid researchers dealing with human embryology,
clinicians performing fetal tissue transplantation, and could be applied in
forensic medicine as well.
Diaphyseal lengths for dried material of Streeter (6.O’Rahilly, 1973), whereas Patfetal skeletons from the third to the tenth ten’s values (1968bused in our work-were
lunar month of pregnancy had already been remarkably close to their sonar curve.
investigated in a forensic series (F‘azekas and
In the course of a n investigation of human
Kosa, 1978). Earlier literature on the subject hemopoietic development (Kelemen et al.,
can be found in that monograph.
1979), we measured the lengths of long bones
Recently, ultrasonography of the normal of the extremities. During this study we had
intrauterine fetal skeleton has furnished im- several samples in which the fetus was not
portant information (Jeanty et al., 1981; intact and the well-known CR length, otherBowie and Andreotti, 1982; Pedersen, 1982, wise used to determine the age of fetus (cf.
specimens for 7-14 menstrual weeks; O’Brien Patten, 1968),was not measurable.’ In these
and Queenan, 1982, specimens for 14-27 cases we used bone length as a n alternative
menstrual weeks [menstrual age is 2 weeks indication of developmental stage.
Having 491 bone length values between 7
more than fertilization age]). O’Brien et al.
(1981) reported on diaphyseal femur length and 22 weeks fertilization age, we thought it
derived from measurement of the calcified would be useful to publish details of this
portion in utero. Filly and Globus (1982) work, and now we propose to use bone length
noted that the lengths of the humerus and measurement as a simple method of estimatfemur of normal fetuses younger than 22 ing the developmental age of delivered hupostmenstrual weeks were virtually identi- man fetuses, at least in the indicated range.
cal by ultrasonography. On the other hand,
Seeds and Cefalo (19821, investigating the
‘Seventy-four out of 193 samples (38.3%), originating from
relationship of fetal limb lengths to gesta- fetuses
older than 8 weeks, were not intact, i.e., not suitable for
tional age, emphasized that there is a natu- exact CR length measurement. Ninety values belong to these
samples:
29, humeri 24, tibiae 20, and radii 17. Values
ral break a t 25 (menstrual) weeks, i.e., the belongingfemora
to these samples did not differ from the values belongcurve becomes more flattened after this age. ing to uninjured fetuses. CR lengths for these samples have been
determined either by reconstruction or by calculation as given
In a critical evaluation of sonar crown- in
Patten (1968).
rump (CR) length measurements, Robinson
Received April 4, 1983; accepted January 31,1984.
and Fleming (1975) raised some doubts as to
Address reprint requests to Dr. Endre Kelemen, I. Belklinika,
the accuracy of the values originating from Koranyi u ZiA, 1083 Budapest, Hungary.
0 1984 ALAN R. LISS, INC.
548
E. KELEMEN, M. JANOSSA, W. CALVO, AND T.M. FLIEDNER
Our results could serve as assistance to
human embryologists as well as clinicians
performing fetal tissue transplantation and
could have application in forensic medicine.
MATERIALS AND METHODS
Four hundred ninety-one long bones from
193 human fetuses were investigated. Most
of these specimens were obtained from the
2nd Department of Obstetrics and Gynecology of the Semmelweis University of Budapest. Mothers were all Caucasians.
Up to the 12th week of pregnancy, samples
were obtained by curettage, while older ones
were derived from prostaglandin-induced
abortion. Fetuses delivered after spontaneous abortion or from twin pregnancies or
cases of known’ maternal disease were
excluded.
Each sample was investigated within 1
hour after delivery. Femora (128), humeri
(1371, tibiae (117), and radii (109)were cleaned
of soft tissue by scissors and were measured
with a millimeter caliper under a stereomicroscope. The maximal length of the bone,
including its cartilage, was determined by
two measurements. Laterality was not considered. The size of the fetus was measured
as crown-rump length a t least twice. Fertilization age was taken from Figure VII-2 and
p. 142 of Patten (1968).
RESULTS
Table 1contains the measurements of four
long bones and their corresponding fertilization age. Because a linear correlation exists
between CR length and gestational age
(either fertilization or menstrual: Patten,
1968) on the one hand, and between CR
length and the length of long bones of the
extremities on the other (at least in the time
period of development that we investigated),
the correlation between fetal age and the
length of bones can be considered linear.
Formulae €or calculating the age of a fetus
in weeks (x), knowing the size of a bone in
millimeters (y) are:
y + 24.6
y + 21.8
Femur x = ___ Humerus x = ___
3.85
3.85
and bone length measurements on the other
hand, were < .5 week 76.0%; .5-< 1 week
15.6%; 1-< 1.5 weeks 5.9%; 1.5-< 2 weeks
2.5%. This means that the differences between the two methods amounted to less than
1 week in 91.6% of cases. We may add that
when differences surpassed 1 week, CR
length values tended to be the higher ones.
The largest difference in length of any bone
at a single time point was 6.5 mm, whereas
the largest deviation for identical bone length
at different age values was 2.5 weeks above
18 weeks of age, while under 18 weeks of
fertilization it was scarcely over 2 weeks.
DISCUSSION
Although knowledge of gestational age
forms the standard against which other
measures are evaluated for normalcy, different types of measurements are applied in
different publications, and, sometimes, one is
uncertain as to the measurement employed
in estimating gestational age. Most clinicians prefer the menstrual age, whereas research workers tend to use fertilization age.
There are some difficulties with the widely
used CR length measurement, especially over
150 mm length as well as in cases in which
the fetus is not intact (cf. Patten, 1968). The
measurement of biparietal diameter has been
recommended by Little and Campbell (1982).
Direct bone length measurement appears to
be a very simple and accurate method. Given
the actual numerical information in Table 1,
the formulae that we include are dispensable.
The main advantage of measurement of
the length of the long bones of extremities is
that the age of even severely damaged fetuses can be readily determined with acceptable accuracy up to the 22nd week of
fertilization. In fact, a t least one long bone
was available in every case, whereas exact
CR length measurement was impossible to
ascertain in 38.3% of 193 samples. On the
basis of our observations on 491 fresh, intact
bone samples investigated shortly after delivery, we propose the use of that method,
and to call it “measurement of developmental age” (expressed either in fertilization
or in postmenstrual weeks).
ACKNOWLEDGMENTS
Tibia x
+ 24.8
= ___
y
3.48
y + 15.3
Radius x = ___
2.58
Estimated age differences between intrasample CR length measurements on the one,
This work was supported by the Scientific
Research Council, Ministry of Health, Budapest (13/1-31/311). Statistical evaluation of
results and calculations were carried out by
Peter Vargha, Department of Biometry, Semmelweis University, Budapest.
549
DEVELOPMENTAL AGE MEASURED BY BONE LENGTH
TABLE 1. Length of long bones of extremities and fertilization age in healthy, delivered human fetuses
Fertil.
age
(weeks)
Bone
length
(mm)
Fertil.
age
(weeks)
Bone
length
(mm)
Fertil.
age
(weeks)
Bone
length
(mm)
12 314
13
13 112
24.0
27.5
25.0
26.0
27.5
28.5
31.3
31.5
32.0
32.0
28.0
28.5
31.5
32.5
33.0
34.0
34.1
35.0
36.5
37.0
34.0
36.0
37.0
36.0
37.2
38.0
37.5
38.0
40.0
41.0
42.0
42.0
38.5
41.0
43.0
40.4
44.0
43.0
41.0
45.0
51.0
46.0
46.5
47.0
50.3
51.0
47.5
50.0
50.0
51.0
52.5
52.2
19 112
48.5
50.0
52.0
52.0
53.0
50.2
52.0
53.0
54.0
54.0
51.3
51.0
54.0
52.6
54.0
55.0
55.5
57.0
58.5
59.5
59.0
57.0
Femora
7
7 114
7 112
7 314
3.0
3.5
3.7
3.5
3.7
4.0
3.6
4.0
3.7
13 314
14
5.0
8
4.0
4.5
5.0
5.0
8 114
8 112
8 314
9
9 114
9 112
9 314
10
10 112
10 314
11
11 114
11 112
11 314
12
12 112
6.0
7.0
7.2
6.0
7.5
7.0
8.0
9.0
9.0
9.5
10.0
10.5
11.5
12.0
12.5
15.0
16.0
15.0
15.5
16.2
17.0
19.0
19.0
19.5
20.0
22.0
17.9
18.5
19.3
20.0
20.0
21.0
21.4
22.0
19.5
21.0
22.0
21.0
22.0
22.5
14 114
14 314
15
15 112
15 314
16
16 114
16 112
16 314
17
17 114
17 112
17 314
18
18 114
18 112
18 314
19
19 114
Humeri
7
7 114
7 112
7 314
8
3.0
3.2
3.1
3.5
3.5
4.0
4.5
3.7
4.0
4.5
4.6
11 112
11 314
12
12 112
17.5
18.0
19.8
20.0
18.0
20.0
18.5
19.0
20.0
20.5
21.0
19 314
20
20 114
20 112
20 314
21
21 114
21 112
22
22 114
17
17 114
17 112
17 314
18
35.5
39.5
36.0
38.0
39.0
42.0
37.5
42.0
44.0
41.4
42.0
Continued
TABLE 1. (Continued) Length of long bones ofextremities and fertilization age i n healthy, delivered human fetuses
Fertil.
age
(weeks)
8 114
8 112
8 314
9
9 114
9 112
9 314
10
10 114
10 112
10 314
11
11 114
Tibiae
7 112
8
8 112
8 314
9
9 114
9 112
9 314
10
10 114
10 112
10 314
11
11 114
Bone
length
(mm)
5.3
5.5
5.5
5.0
6.0
6.5
7.1
7.0
7.0
7.5
7.5
7.2
7.5
7.5
8.0
8.2
8.5
9.5
10.0
10.0
11.0
11.0
11.5
12.0
12.5
12.0
12.0
12.5
13.5
14.0
14.5
15.0
16.5
15.0
18.0
17.0
17.5
18.3
17.4
20.5
3.5
3.3
3.5
3.7
4.1
5.5
6.0
6.0
6.5
6.0
6.2
7.0
7.0
5.9
8.5
9.0
8.0
8.5
9.0
12.0
12.1
12.3
11.5
11.0
13.0
15.0
16.0
16.5
14.8
17.0
17.5
Fertil.
age
(weeks)
12 314
13 114
13 112
13 314
14
14 114
14 112
14 314
15
15 112
15 314
16
16 114
16 112
16 314
14
14 114
14 112
15
15 114
15 314
16
16 114
16 112
16 314
17
17 114
17 112
Bone
length
(mm)
23.0
23.5
24.5
25.0
23.0
24.0
25.5
24.0
27.0
27.9
28.0
30.5
28.5
27.0
30.0
26.7
28.0
28.3
29.0
29.5
28.5
29.0
31.3
31.5
32.0
32.0
34.0
35.0
32.5
33.0
35.5
35.0
37.0
37.8
39.5
37.0
39.0
38.5
40.0
40.5
23.5
26.0
22.5
23.5
24.0
22.0
23.0
25.0
25.7
26.0
27.5
26.0
27.0
28.0
27.0
29.0
30.5
31.5
32.0
32.0
33.0
34.0
34.3
36.0
32.0
34.2
35.0
32.0
34.4
35.0
35.5
Fertil.
age
(weeks)
18 114
18 1.2
18 314
19
19 114
19 112
20
20 112
21
21 114
21 112
22
22 114
20
20 114
20 314
21
21
21
21
22
22
114
112
314
114
Bone
length
(mm)
41.0
45.0
42.5
43.0
47.0
42.0
46.0
46.5
45.3
44.0
45.0
48.5
47.0
47.0
48.0
46.5
51.0
47.0
50.0
51.5
52.0
52.0
54.6
56.0
44.5
48.0
48.0
47.5
43.6
46.0
46.0
46.5
52.0
48.0
51.7
52.0
49.0
Continued
TABLE 1. (Continued) Length of long bones of extremities and fertilization age in healthy, delivered human fetuses
Fertil.
age
(weeks)
11 112
11 314
12
12 112
12 314
13
13 1/4
13 112
Radii
7 112
8
8 112
8 314
9
9 114
9 112
9 314
10
10 112
10 314
11
11 114
11 112
11 314
12
12
12
12
13
13
114
112
314
112
13 3/4
14
14 114
14 112
Bone
length
(mm)
15.0
16.2
17.0
17.2
18.0
15.0
16.5
17.0
18.0
15.4
17.0
18.0
18.5
21.0
19.0
22.0
21.0
19.0
21.0
22.0
22.0
3.4
3.6
3.8
3.5
3.7
4.5
5.5
5.0
6.7
5.5
5.5
7.0
7.5
7.5
8.0
10.0
10.0
9.5
10.0
11.0
13.0
13.5
14.5
15.0
13.8
14.0
15.0
15.2
14.0
16.0
17.0
15.5
17.5
16.5
16.8
16.5
17.5
17.7
20.0
20.0
21.0
21.5
22.0
23.0
22.5
20.5
21.5
21.0
21.0
Ferti 1.
age
(weeks)
17 314
18
18 112
18 314
19
19 114
19 112
15
15 112
15 314
16
16 114
16 112
16 314
17
17 114
17 112
17 314
18
18 114
18 112
18 314
19
19 114
19 112
19 314
Bone
length
(mm)
38.0
35.7
39.5
35.0
41.5
35.0
37.0
37.5
38.0
41.5
43.2
44.0
46.0
48.0
41.3
42.5
48.0
42.0
47.5
48.0
48.5
21.5
23.0
23.5
23.5
24.5
24.5
25.0
27.0
28.5
24.9
28.0
25.0
26.0
28.0
29.0
27.5
27.5
29.0
29.0
29.5
30.6
27.5
30.0
32.0
27.3
29.0
30.0
30.0
31.5
32.5
31.5
32.7
35.5
32.0
31.5
32.0
30.5
31.5
32.4
35.0
36.0
37.1
33.0
33.9
33.0
34.0
34.5
37.0
Fertil.
age
(weeks)
20
20 112
20 314
21
2 1 112
21 314
22
22 114
Bone
length
(mm)
35.0
35.5
36.0
38.5
35.3
38.0
39.0
42.0
43.0
46.0
552
E. KELEMEN, M. JANOSSA, W. CALVO, AND T.M. FLIEDNER
LITERATURE CITED
Bowie, J.D., and R.F. Andreotti (1982) Estimating gestational age in utero. Radiol. Clin. North Am., 20r325334.
Fazekas, I.G., and F. KQa (1978) Forensic Fetal Osteology. Akad. Kiado, Budapest, pp. 232-277.
Filly, R.A., and M.S. Globus (1982) Ultrasonography of
the normal and pathological fetal skeleton. Radiol.
Clin. North Am., 20:311-323.
Jeanty, P., C. Kirkpatrick, M. Dramaix-Wilwet, et al.
(1981)Ultrasonic evaluation of fetal limb growth. Radiology, 140:165-168.
Kelemen, E., W. Calvo, and T.M. Fliedner (1979)Atlas of
Human Hemopoietic Development. Springer-Verlag,
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Berlin, p. 14.
Little. D.. and S. Camubell (1982)Ultrasound evaluation
of intrauterine gro&h retardation. Radiol. Clin. North
Am. 20:335-351.
O’Brien, G.B., and J.T. Queenan (1982)Ultrasound fetal
femur length in relation to intrauterine growth retardation. Part 11. Am. J. Obstet. Gynecol., 144:35-39.
O’Brien, G.B., J.T. Queenan, and S. Campbell (1981)
Assessment of gestation age in the second trimester by
real-time ultrasound measurement of the femur length.
Am. J. Obstet. Gynecol., 139:540-545.
O’Rahilly, R. (1973) Developmental Stages in Human
Embryos. Carnegie Institute, Publ. 631, Washington,
D.C., p. 3.
Patten, B.M. (1968) Human Embryology, 3rd ed. McGraw-Hill, New York, pp. 142-145.
Pedersen, J.F. (1982) Fetal crown-rump length measurement by ultrasound in normal pregnancy. Br. J. Obstet. Gynaecol., 89:926-930.
Robinson, H.P., and J.E.E. Fleming (1975) A critical
evaluation of sonar “CR length” measurements. Br. J.
Obstet. Gynaecol., 82.702-710.
Seeds, J.W., and R.C. Cefalo (1982)Relationship of fetal
limb lengths to both biparietal diameter and gestational age. Obstet. Gynecol., 60:680-685.
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