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The human fetal thyroid I. Its weight in relation to body weight crown-rump length foot length and estimated gestation age

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The Human Fetal Thyroid
I. ITS WEIGHT IN RELATION TO BODY WEIGHT, CROWN-RUMP
LENGTH, FOOT LENGTH AND ESTIMATED GESTATION AGE'
THOMAS H . SHEPARD, HENNING J. ANDERSEN AND
HELGE ANDERSEN
Department of Pediatrics, University of Washington, Seattle, Washington,
Fetal Laboratory, Department of Pediatrics, University o f Copenhagen,
Denmark and Laboratory of Cyto- and Histochemistry, Department of
Human Anatomy, University of Copenhagen, Copenhagen, Denmark
The weights of 75 human fetal thyroids were analyzed in relation to
ABSTRACT
crown-rump length, foot length, weight, and estimated gestation age. The ratio of
thyroid weight to body weight was lower in the smaller fetuses and gradually increased
until the fetus was 7&90 m m in crown-rump length when the ratio attained a value
close to that found in the newborn and adult. This period of development when the
relative weight of the thyroid becomes constant coincides with the time of appearance of colloid and the onset of ability to concentrate iodine.
A comparison of estimated age of fetuses in the Danish material and the fomalinfixed fetuses from the Carnegie Collection shows the Danish fetuses under 40 m m i n
crown-rump length to be four to six days older than the average given by Streeter.
Streeter may have made his average too low and probably the relative ages of the
two groups are comparable.
There are very few records of the weight
of the normal human fetal thyroid during
the first half of pregnancy. Jackson ('09)
reported 11 thyroid weights in fetuses under 150 mm but only four of these were
from fetuses of less than 100 mm in crownrump length. Seven fetal thyroid weights
were given by Pulaska ('29) for human
fetuses of 115 to 145 mm in crown-rump
length and Lucien and George ('27) also
reported two thyroid weights.
In addition, a thorough analysis of the
relation of the fetal age to the crown-rump
length of the non-pathological fresh fetus
has not been reported. The majority of
the previous crown-rump measurements
have been obtained from spontaneous abortions and in most cases the determinations
were made after fixation. (Retzius, '04;
Jackson, '09; Mall, '18; Streeter, '20; Scammon and Calkins, '29; Arey, '47; and Trolle,
'48).
The purpose of this report is to relate
the weights of developing thyroids to
crown-rump length, foot length, body
weight, and estimated gestation age. A
comparison is made also between the fresh
crown-rump lengths of the Danish material and those from Streeter's fixed fetuses.
MATERIAL AND METHODS
The material consisted of 22 fetuses
from the collection of the Carnegie Institution, Department of Embryology, and 57
fetuses from the laboratory located in the
Department of Human Anatomy at the
University of Copenhagen. If the fetal period is defined as beginning after Streeter's
horizon XXIII (27-31 mm crown-rump
length) five of our studied specimens
would be embryos. In this paper they all
have been placed in the fetal group for the
sake of continuity. Eighteen of the fetuses
from the Carnegie Collection were fixed in
4% formaldehyde, and four were fixed in
other types of fixative.
All the Danish material was obtained
within one-half to two hours after elective
operative removal of the fetus by Cesarean
or lower cervical section.
Seventeen thyroids were weighed after
fixation in Lillie's acetic-alcohol-formalin
solution' ('54), 35 after fixation in 4%
1 This work was performed in the Fetal Laboratory
at the Department of Human Anatomy University of
Copenhagen and in the Department df Embryology
Carnegie Institution of Washington Baltimore Mary:
land, and was supported by the fiational In'stitutes
of Health (grant AM06799-01HED) and by the
Association for Aid of Crippled Children, New York.
2 Lillie's fixative contains: 85 parts absolute ethyl
alcohol, five garts glacial acetic acid, and ten parts
4% formalde yde.
123
124
T. H. SHEPARD, H . J. ANDERSEN AND H. ANDERSEN
formaldehyde (10% formalin), and 19
were weighed in the fresh state. Four of
the thyroids were fixed in other types of
fixative. Some of those fixed in formalin
were transferred to 70% ethyl alcohol
after an undetermined number of months.
The thyroid glands were removed under
a dissecting microscope and the anterior
approach was used in order to determine
the presence of the pyramidal lobe; in most
cases both lobes and the isthmus were removed intact. Some difficulty was encountered in the removal of unfixed glands in
specimens of less than 50 mm crown-rump
length. The glands were kept in a moist
state with isotonic saline solution and
weighed immediately on a microanalytical
balance. To study the changes in weight
due to fixation, six glands of 20 to 106 mg
were reweighed at intervals of days or
weeks after being blotted free of any surface fixative. The fetuses were weighed to
the nearest 0.1 g. The whole fetus and the
thyroid were always in a similar state;
namely both fixed in the same fixative or
both fresh.
In the Carnegie group of specimens, the
crown-rump length was measured two
weeks after fixation but in the fresh Danish
material, over 35 mm in length, the vertebral column was straightened fmt by laying the fetus on a flat surface. Fresh
specimens 35 mm or under were not
straightened and were measured in their
natural curved position. The foot length
was measured according to Streeter (’20).
The estimated gestation age for the
Danish fetuses was obtained by subtracting
14 days from the menstrual age which was
the period from the first day of the last
menses to the day of operation. If the
mother was unable to give the gynecologist
a specific date for the time of onset of her
last menstrual period, the age was not calculated. All available data on ovulation
age from the Danish laboratory was
plotted. The gestation ages for the fetuses
from the Carnegie Collection were obtained by subtracting 14 days from the
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125
HUMAN FETAL THYROID WEIGHT
menstrual age but in some cases where the
date of last menses was unknown the menstrual age was assigned by using Streeter's
average sitting height.
The sex of the Danish fetuses of less
than 50 mm in length was determined by
the presence or absence of the nuclear sex
chromatin body of Ban.
RESULTS
The increase in thyroid weight with respect to crown-rump and foot length is
illustrated in figures 1 and 2. There was
a tendency for the glands fixed in Lillie's
solution to be lighter while the weight of
those fixed in formalin corresponded to the
freshly weighed specimens. There were no
differences noted in gland weights of male
and female fetuses.
As the fetus increased in length from 29
to 80 mm the thyroid weight in relation to
body weight also increased (fig. 3). After
80 mm there was no apparent change in
this ratio. The correlation coefficient between the thyroid to body weight ratio and
the crown-rump length was 0.704 (p <
+
0
wr
THYROID
VS
FOOT L€NGTH
a
0
0
I
5
..
I
I
1
1
10
15
20
25
fOOT LlrNGTH mm.
Fig. 2 Thyroid weight in mg plotted against the foot length in mm. The symbols are
the same as in figure 1. One point could not be plotted because it was above the scale.
126
T. H. SHEPARD, H. J. ANDERSEN AND H. ANDERSEN
.4
0
BODY
W Z x100
0
0
0
0
\
2
.03L
a
I
i5 .@.Of-
CROWN-RUMP LENGTH rnrn.
Fig. 3 The ratio of the thyroid weight to body weight is plotted against crown-rump
lengths in mm. The symbols are the same as in figure 1.
CROWN-RUMP LENGTH mm.
Fig. 4 Estimated gestation age is plotted against the crown-rump length in mm.
Gestation was assumed to begin 14 days after the first day of the last menstrual period.
The connected line is taken from Streeter's material and the dotted line from this study.
x - Carnegie Collertion embryos used in this study. * - all available material from the
Danish collection of fetuses.
127
HUMAN FETAL THYROID WEIGHT
TH Y R 0 l B W € l G H T CHANGES
A F T E R f I X A T I ON
I
0
I
2
3
4
5
6
7
8
9
WEEKS
Fig. 5 Thyroid weight changes after fixation in 10% neutral formalin (crosses, X ) and
in Lillie's fixative (dots, .).
0.001) for the group below 80 mm whereas
above 80 mm it was 0.002 which is not
st atistically significant.
The plots of gestation age and crownrump length of the Danish material were
compared in figure 4 to Streeter's average
which is a widely accepted standard in the
United States. Below 40 mm all of the
Danish ages are equal to or more than
Streeter's average. Along this segment of
the line (below 40 mm) 15 of the Danish
specimens fall above, one on the line and
none below. It is very unlikely that such
a distribution could occur by chance.
The thyroid weight changes during a
seven week period following fixation are
shown in figure 5 and it may be noted that
there was a decrease with Lillie's fixative
whereas with formaldehyde the reverse
was usually seen.
Thirty per cent of the glands had a pyramidal lobe; in eight it was in the midline, in six it was on the right side and in
nine it was on the left side.
The exact figures for the plotted measurements may be obtained from the senior
author.
+
DISCUSSION
The most striking finding is that the
relative weights of the thyroid gland gradually increase until fetuses attain a crownrump length of 80 mm. This length represents an age of 80 days gestation and a
developmental period which is functionally
and histologically very significant. This
period (75-85 days of gestation) is when
the human thyroid first develops the ability
to concentrate iodine (Chapman et al.,
'48; Hodges et al., '55; Andersen, '60). Although small amounts of colloid are present earlier there is also a very sharp increase in amount between 75 and 85 days
(Norris, '16; Shepard et al., '64). After
the 80 mm period the thyroid weight averages 0.0458% of body weight and this
average is close to that of the newborn
(0.049, Potter, '61) and adult (0.036).
These findings do not agree with the few
thyroid to body weight ratios reported by
Lucien and George ('22) who observed an
increase between the fourth and fifth
months. However, they report only one
thyroid weight for each month and do not
clearly define their time periods.
128
T. H. SHEPARD, H. J. ANDERSEN AND H. ANDERSEN
LITERATURE CITED
The incidence of pyramidal lobes does
J. 1960 Studies of hypothyroidAndersen,
H.
not seem to differ with age. The incidence
ism in children. Acta Paed. Scand., Suppleof 40% in adults (Huber, ’30) is fairly
ment, 125: 106-111.
close to the 30% observed in this study. Arey, L. B. 1947 A new rule for correlating the
age of human fetuses with size indices. Am. J.
Pulaska (’29) found eight pyramidal lobes
of Obst. and Gyn., 54: 872-873.
out of a total of 64 fetal glands.
Chapman, E. M., G. W. Corner, D. Robinson and
The discrepancy between the gestational
R. D. Evans 1948 Collection of radioiodine
by the human fetal thyroid. J. Clin. Endocrinol.,
age of the Danish fetuses and Streeter’s
8: 717-720.
“average” can be explained by the fact that Hodges,
R. E., T. C. Evans, J. T. Bradbury and
Streeter’s “average” up to 40 mm length
W. C. Keettel 1955 The accumulation of
radioactive iodine by human fetal thyroids. J.
was calculated from timed monkey matClin. Endocrinol. and Metab., 15: 661-667.
ings rather than human (Streeter, ’20;
Huber, G. C., editor 1930 Piersol’s Human
Streeter et al., ’51). If Streeter’s 11 plotted
Anatomy. Ninth edition, Pages 1790,J. B. Lipspecimens under 40 mm are scrutinized it
pincott, Philadelphia.
can be seen that eight were above the Jackson, C. M. 1909 On the prenatal growth of
the human body and the relative growth of the
average line actually giving a distribution
various organs and parts. Am. J. Anat., 9:
quite similar to those of the Danish fetuses.
119-166.
Scammon and Calkins (’29) and Schultz Lillie, R. D. 1954 Histopathologic Technic and
Practical Histochemistry, page 35. McGraw
(’19) have thoroughly discussed factors
Hill Book Company, New York.
which may alter the measurements of Lucien, M., and A. George 1927 A propos de
l’evolution ponderale de quelques organes endofetuses.
criniens chez le foetus humain. Compt. rendus
Thyroid weights calculated from Jackde l’Ass. des Anatomistes, 22: 176-183, Lndres.
son’s data (’09) are heavier and fit poorly, Mall, F. P. 1918 On the age of human embryos.
if at all the data reported in figure 1.
Am. J. Anat., 23: 397-422.
Pulaska’s thyroid weights (‘29) determined Norris, E. H. 1916 The morphogenesis of the
follicles in the human thyroid gland. Am. J.
on fetuses from Hamburg fit the data on
Anat., 20: 411-448.
figure 1 but the three fetuses from Bern Potter, E. L. 1961 Pathology of the Fetus and
the Infant, 2nd edition, page 14, Year Book
had lighter thyroid glands.
Medical Publishers Inc., Chicago, Ill.
The weights of fetal thyroids from the Pulaska,
Alfred 1929 Vergleichende histologische
Danish and Carnegie group were found to
Untersuchungen a n fotalen Schilddriisen aus
Hamburg und Bern. Frankfurter Zeitschrift
be comparable when the fixation was in
fur Pathologie, 38: 29-63.
formalin. In fact, the formalin fixed ma- Retzius,
G. 1904 Zur Kenntnis der Entwicklung
terial was quite similar in weight to the
der Korperformen des Menschen wahrend der
fotalen Lebensstufen. Biol. Untersuchungen,
fresh glands from embryos of the same
11: (N.F.) 33-76.
length. Unfortunately the data in figure 5
R. E.,and L. A. Calkins 1929 Growth
does not answer the question of what Scammon,
in the Fetal Period. Part I, pages 1-55, part 111,
happens to the weight of the gland after
pages 75-91. University of Minnesota Press,
Minneapolis.
the ninth week of fixation.
Schultz, A. H. 1919 Changes in fetuses due to
formalin fixation. Am. J. of Phys. Anthropol.,
ACKNOWLEDGMENTS
Gratitude is expressed to the Chief
Physicians: A. Christensen, M.D., Dept. of
Gynecology, Bispebjerg Hospital, A. Fuchs,
M.D., Dept. of Gynecology, Municipal Hospital of Copenhagen, V. Madsen, M.E.,
Dept. of Gynecology, Gentofte Amts Sygehus, and S. Stamer, M.D., Dept. of Gynecology, Sonderbro Hospital for the valuable
cooperation in supplying the Danish fetal
material. The senior author appreciates
help given by Drs. James Ebert, Mary
Rawles and Elizabeth Ramsev.
2: 35-41.
Shepard, T. H., Helge Andersen and Henning
Andersen 1964 The human fetal thyroid. 11.
Histochemical studies during the first half of
fetal life. To be published.
Streeter, G. L. 1920 Weight, sitting height,
head size, foot length and menstrual age of
human embryos. Carnegie Inst. Wash., Pub.
274, Contributions to Embryology no. 55, vol.
11, 143-170.
Streeter, G. L., C. H. Heuser and G. W. Corner
1951 Developmental horizons in human embryos. Contributions to Embryology no. 230,
Reprint vol., 11s 166-186.
Trolle, Dyre 1948 Age of foetuses determined
from their measures. Acta Obst. et Gyn. Scand.,
27: 327-337.
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