Arch Gynecol Obstet
DOI 10.1007/s00404-016-4219-2
MATERNAL-FETAL MEDICINE
The effects of gestational transient thyrotoxicosis on the perinatal
outcomes: a case–control study
Satoko Kinomoto-Kondo1 • Nagayoshi Umehara1 • Shiori Sato1 • Kohei Ogawa1
Takeo Fujiwara2 • Naoko Arata1 • Haruhiko Sago1
Received: 5 July 2016 / Accepted: 13 October 2016
Ó Springer-Verlag Berlin Heidelberg 2016
Abstract
Purpose To study the effects of gestational transient thy-
rotoxicosis (GTT) on pregnancy outcomes.
Methods This case–control study retrospectively analyzed
7976 women with singleton pregnancies whose thyroid
function was measured before 16 weeks of gestation and
who delivered at C22 weeks of pregnancy. GTT was
defined as hyperthyroidism (free thyroxine [FT4]
level: C95th percentile) in the early pregnancy, which
normalized in mid-pregnancy without thyroid-stimulating
hormone receptor antibodies. Using data extracted from
electronic records, we examined the association between
GTT and the pregnancy outcomes (preterm delivery, ges-
tational age at delivery, pregnancy induced hypertension
(PIH), preeclampsia, placental abruption, caesarian section,
birth weight, low birth weight, Apgar score, cord pH,
stillbirth at gestational week C22, and neonatal death). We
classified the cases into quartiles according to their FT4
values during the early pregnancy and investigated the
association with the gestational age at delivery.
Results Two hundred and eight cases of GTT and 6317
cases with normal thyroid assessments were reviewed.
GTT was associated with hyperemesis gravidarum, but not
with stillbirth, preterm delivery, PIH, preeclampsia, pla-
cental abruption, or low birth weight. The gestation period
& Nagayoshi Umehara
umehara-n@ncchd.go.jp
1
Center of Maternal-Fetal, Neonatal and Reproductive
Medicine, National Center for Child Health and
Development, 2-10-1 Okura, Setagaya-ku, Tokyo 157-8535,
Japan
2 The clinical manifestations of GTT are not always
Department of Social Medicine, National Center for Child
Health and Development, 2-10-1 Okura, Setagaya-ku,
Tokyo 157-8535, Japan
•
was shorter in patients with GTT than in those with a
normal thyroid function (38.69 ± 1.79 vs. 39.07 ±
1.64 weeks, p \ 0.01). Higher FT4 levels during the early
pregnancy were associated with earlier delivery
(p = 0.02).
Conclusions GTT was associated with a lower gestational
age at delivery but not with adverse pregnancy outcomes.
There was a negative correlation between the FT4 values in
the early pregnancy and the gestational period.
Keywords Gestational thyrotoxicosis
Free T4

Hyperemesis gravidarum
Preterm delivery
Gestational
period
Introduction
Gestational transient thyrotoxicosis (GTT) is a condition in
which transient hyperthyroidism occurs due to the thyroid-
stimulating effect of human chorionic gonadotropin (hCG),
which is secreted from the placenta during the early
pregnancy [1–4]. GTT is diagnosed when there is an
increase in thyroid hormone levels during the early preg-
nancy and normalization in mid-pregnancy, in women who
have no history of hyperthyroidism, no physical findings,
such as thyroid gland enlargement or exophthalmos, and no
detection of thyroid autoantibodies [1, 5]. GTT has been
reported to be associated with a higher frequency of
hyperemesis gravidarum and it is often accompanied by
symptoms of hyperthyroidism, such as tachycardia and
weight loss [1–3]. However, GTT has not been reported to
be associated with unfavorable perinatal outcomes [6–9].
apparent [1]. GTT is not easily detected without an
assessment of the thyroid function [1]. Thus, few studies
123

have so far investigated the association between GTT and
perinatal outcomes. In addition, most of the existing studies
are small in scale, with less than 100 cases [6, 7, 9]. The
objective of this study was to clarify the effects of GTT on
the perinatal outcomes in a large study population.
Methods
We performed a retrospective case–control study on
women with singleton pregnancies whose thyroid function
was measured before 16 weeks of gestation and who
delivered at C22 weeks of pregnancy at the Center of
Maternal-Fetal, Neonatal and Reproductive Medicine,
National Center for Child Health and Development
(Tokyo, Japan), from October 2004 to November 2012.
Hyperthyroxinemia during the early pregnancy (before
16 weeks of gestation) was defined by a free thyroxine
(FT4) value that was the 95th percentile or over. Women
with a history of thyroid disease were excluded from this
study. The patients whose FT4 values normalized during
mid-pregnancy without receiving any anti-thyroid drugs,
excluding the patients who demonstrated a positive finding
for thyroid-stimulating hormone receptor antibodies
(TRAb), were defined as GTT. We also excluded any
women who had maternal complications that could affect
the perinatal outcome (kidney disease, heart disease,
essential hypertension, and diabetes). The normal group
consisted of women with normal thyroid function (FT4
value: 6th to 94th percentile); women with a history of
thyroid disease, maternal complications, and subclinical
hypothyroidism (FT4 value, normal; thyroid-stimulating
hormone [TSH], C95th percentile) were excluded. The
second-generation human TRAb was measured by an
electrochemiluminescence immunoassay. Values
of \1.0 IU/L were considered to be negative. The TSH and
FT4 measurements were obtained by a chemiluminescence
immunoassay using an IMMULYZE device (LSI Medience
Corporation, Tokyo; n = 5488) until February 2010 and a
LUMIPULSE device (Fujirebio Inc., Tokyo; n = 2591)
from March 2010.
The maternal background [age, parity, smoking, weight,
height, assisted reproductive technology (ART), and severe
hyperemesis gravidarum] and pregnancy outcomes (pre-
term delivery, gestational age at delivery, PIH,
preeclampsia, placental abruption, caesarian section, birth
weight, the Z score of the birth weight by the week of
gestational age, low birth weight infants, placental weight,
Apgar score, cord pH, stillbirth after 22 weeks, and
neonatal death) were extracted from the patients’ electronic
records. We used the maternal weight at the time of the first
examination. Hyperemesis gravidarum was considered to
be severe if hospitalization was required. The Z score of the
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Arch Gynecol Obstet
birth weight, according to the week of gestational age,
parity, and sex, was calculated using the standard curve of
birth weights according to the distribution of birth weights
for gestational age in Japan [10].
Statistical analysis
Categorical variables were investigated by the Chi-square
test or Fisher’s exact test, while continuous variables were
evaluated using the t test. A multivariate analysis was
performed using a logistic regression model that was
adjusted for maternal background factors (age, parity,
smoking, height, body mass index (BMI), and ART). The
multivariate analysis of the birth weight included the
background above-mentioned factors as well as the gesta-
tional age at delivery. A portion of the data was missing for
two factors: maternal height and weight. We, therefore,
performed two analyses: in the first analysis, we used the
average value in place of the missing data; in the second
analysis, we excluded the cases with missing data. As a
secondary analysis, we classified all GTT and normal cases
into quartiles according to the FT4 value during the early
pregnancy and investigated the association with the ges-
tational age at delivery. Furthermore, we divided the GTT
cases into quartiles in the same manner as mentioned above
and investigated the association with the gestational age at
delivery. P values of \0.05 were considered to indicate
statistical significance. The data are represented as
numerical values or percentages for categorical variables,
and as the average value ± standard deviation for contin-
uous variables.
Results
The 5th and 95th percentiles for FT4 that were measured
using the IMMULYZE device were 1.10 and 1.73 ng/dl,
respectively. The 95th percentile for TSH was 2.94 lIU/ml.
The corresponding values, as measured by the LUMI-
PULSE device, were 0.75, 1.22 ng/dl, and 2.85 lIU/ml,
respectively. At the time of the early pregnancy examina-
tion, 411 participants had hyperthyroxinemia
(FT4: C95th), 7135 had normothyroxinemia (FT4: 6th to
94th percentile), and 430 had hypothyroxinemia
(FT4: B5th percentile). Of the 411 cases with hyperthy-
roxinemia, 369 had no history of thyroid disease, 146 did
not have follow-up evaluations for FT4, and 223 demon-
strated normal FT4 values in subsequent examinations.
After excluding the TRAb-positive cases (n = 2) and those
with maternal complications (n = 13), there were 208
participants (2.61 %) in the GTT group. Among the 7135
participants with normothyroxinemia, 6317 (79.20 %)
remained after excluding the cases with a history of thyroid
Arch Gynecol Obstet
disease (n = 301), maternal complications (n = 232), and
subclinical hypothyroidism (TSH: C95th percentile,
n = 285) (Fig. 1).
The background of the study population is shown in
Table 1. No significant differences were detected with
regard to the maternal age, parity, smoking, or the ART
between the GTT and normal groups. The maternal weight
in the GTT group was slightly lower than that in the normal
group (50.51 ± 6.53 vs 52.19 ± 7.15 kg; p \ 0.01), as
was the maternal height (158.78 ± 5.26 vs 159.52 ±
5.19 cm; p = 0.04). The maternal BMI in the GTT group
was also slightly lower than that in the normal group
(20.00 ± 2.28 vs 20.49 ± 2.39; p \ 0.01). The maternal
weight and height data were missing for 732 (11.21 %) and
213 (3.26 %) patients, respectively. The proportion of
participants who experienced severe hyperemesis gravi-
darum was significantly higher in the GTT group than in
the normal group [6 patients (2.88 %) vs 45 patients
(0.71 %); odds ratio (OR) 4.19; 95 % CI 1.77–9.93;
p \ 0.01]. The average FT4 values determined using the
IMMULYZE and LUMIPULSE devices were 2.22 ± 0.34
(range 1.77–3.47) ng/dl and 1.63 ± 0.32 (range 1.28–2.92)
ng/dl, respectively, in the GTT group, and 1.35 ± 0.16 and
Fig. 1 Flow chart illustrating the selection of singletons in this study. SCH subclinical hypothyroidism
0.95 ± 0.13 ng/dl, respectively, in the normal group. Both
values were significantly higher in the GTT group. Fur-
thermore, the average TSH values determined using the
IMMULYZE and LUMIPULSE devices were significantly
lower in the GTT group (0.06 ± 0.16 and 0.04 ± 0.08
lIU/ml, respectively) in comparison to those in the normal
group (0.91 ± 0.71 and 0.80 ± 0.63 lIU/ml, respectively).
Table 2 shows the pregnancy outcomes. The frequency
of preterm delivery before 37 weeks of gestation in the
GTT group (7.21 %) did not differ to a statistically sig-
nificant extent from that in the normal group (5.75 %) (OR
1.27; 95 % CI 0.75–2.18; p = 0.37). However, the gesta-
tional age at delivery was significantly lower in the GTT
group in comparison to that in the normal group
(38.69 ± 1.79 vs 39.07 ± 1.64 weeks; p \ 0.01). There
were no significant differences between the two groups in
terms of the incidence of PIH, preeclampsia, placental
abruption, and risk of caesarian section.
A univariate analysis of birth weight demonstrated a
slight, but significant difference in the weights of the
newborns in the two groups: the newborns in the GTT
group were smaller than those in the normal group
(2909.4 ± 427.5 vs 2992.6 ± 411.9 g; p \ 0.01);
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 Arch Gynecol Obstet

Table 1 Maternal
GTT group (n = 208) Normal group (n = 6317) P value
characteristics of the study
population Age, years 34.44 ± 4.19 34.75 ± 4.22 0.30
Multiparous 99 (47.60) 2857 (45.23) 0.50
Smoking
Current 8 (3.85) 145 (2.30) 0.23
Past 2 (0.96) 32 (0.51)
Body weight, kg 50.51 ± 6.53 52.19 ± 7.15 \0.01
Height, cm 158.78 ± 5.26 159.52 ± 5.19 0.04
Body mass index 20.00 ± 2.28 20.49 ± 2.39 \0.01
ART 17 (8.17) 733 (11.60) 0.13
FT4 IMMULYZE, ng/dl 2.22 ± 0.34 1.35 ± 0.16 \0.01
FT4 LUMIPULSE, ng/dl 1.63 ± 0.32 0.95 ± 0.13 \0.01
TSH IMMULYZE, lIU/ml 0.06 ± 0.16 0.91 ± 0.71 \0.01
TSH LUMIPULSE, lIU/ml 0.04 ± 0.08 0.80 ± 0.63 \0.01
Hyperemesis gravidarum 6 (2.88) 45 (0.71) \0.01
The values are expressed as the mean ± standard deviation or N (%)
ART assisted reproductive technology, SD standard deviation

Table 2 Pregnancy outcomes

GTT group (n = 208) Normal group (n = 6317) Crude Adjusted
P value OR (95 % CI) P value OR (95 % CI)

Preterm delivery \37 weeks 15 (7.21) 363 (5.75) 0.37 1.27 (0.75–2.18) 0.38a 1.27
Gestational age of delivery, weeks 38.69 ± 1.79 39.07 ± 1.64 \0.01 \0.01a (0.71–2.10)a
PIH 3 (1.44) 136 (2.15) 0.63 0.67 (0.21–2.11)
Preeclampsia 1 (0.48) 65 (1.03) 0.72 0.46 (0.06–3.36)
Placental abruption 3 (1.44) 76 (1.20) 0.74 1.20 (0.38–3.84)
Cesarean section 60 (28.9) 1614 (25.6) 0.28 1.18 (0.87–1.60)
Birth weight, g 2909.4 ± 427.5 2992.6 ± 411.9 \0.01 0.82b
Z score of birth weight 0.02 ± 0.91 0.09 ± 0.96 0.30
Low birth weight (\2500 g) 20 (9.62) 542 (8.58) 0.60 1.13 (0.71–1.81)
Placental weight, g 533.9 ± 95.8 546.8 ± 103.9 0.08
Male 101 (48.6) 3320 (52.6) 0.26 1.17 (0.89–1.55)
Apgar score 5 min: B7 7 (3.37) 114 (1.81) 0.10 1.89 (0.87–4.11)
Apgar score 5 min: B4 0 (0) 15 (0.24) –
Cord pH 7.198 ± 0.734 7.200 ± 0.728 0.96
Stillbirth 0 (0) 11 (0.17) –
Neonatal death 0 (0) 2 (0.03) –
The values are expressed as the mean ± standard deviation or N (%)
95 % CI 95 % confidence interval, OR odds ratio, PIH pregnancy induced hypertension
a
Adjusted for maternal age, parity, smoking, height, BMI, and ART
b
Adjusted for maternal age, parity, smoking, height, BMI, ART, and gestational age at delivery

however, when the Z scores for birth weight by gestational
age were compared, no significant differences were
observed (0.02 ± 0.91 vs 0.09 ± 0.96; p = 0.30). Twenty
participants (9.62 %) in the GTT group and five hundred
and forty two (8.58 %) participants in the normal group
gave birth to low birth weight infants; the difference was
not statistically significant (p = 0.60). Although the pla-
cental weight was slightly lower in the GTT group
(533.9 ± 95.8 g) in comparison to the normal group
(546.8 ± 103.9 g), the difference was not significant
(p = 0.08). In addition, no significant differences were
observed in terms of newborn gender, the proportion of

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patients with Apgar scores (5 min) of B7 and B4, cord
blood pH, stillbirths, and neonatal death. The numbers of
unusable data points (percent) for the placental weight,
Apgar score, and cord blood pH were 8 (0.12 %), 17
(0.26 %), and 547 (8.40 %), respectively.
In the multivariate analysis with adjustment for maternal
age, parity, smoking, height, BMI, and ART, the incidence
of severe hyperemesis gravidarum was found to be sig-
nificantly higher in the GTT group (OR 4.05; 95 % CI
1.53–8.94; p \ 0.01). The rate of preterm delivery before
37 weeks of gestation did not differ between the two
groups (OR 1.27; 95 % CI 0.71–2.10; p = 0.38); however,
the gestational age at delivery was still significantly lower
in the GTT group (p \ 0.01). A multivariate analysis of
newborn birth weight using the background factors men-
tioned above with adjustment for the gestational age at
delivery revealed no significant difference between the two
groups (p = 0.82). Similar results were obtained when the
missing data values were replaced by the average values or
excluded altogether in the multivariate analysis.
Although GTT did not increase the risk of preterm
delivery, the gestational age at delivery was lower than that
in the normal group. To investigate the association between
the FT4 values in the early pregnancy and the gestational
age at delivery, we grouped all of the study participants
(n = 6525) according to their FT4 quartile and compared
the gestational age at delivery (Table 3). The FT4(ng/dl)
quartiles were defined as follows: Q1 (n = 1684),
1.05–1.23 (IMMULYZE), or 0.71–0.86 (LUMIPULSE);
Q2 (n = 1662), 1.24–1.34 (IMMULYZE), or 0.87–0.94
(LUMIPULSE); Q3 (n = 1591), 1.35–1.47 (IMMULYZE)
or 0.95–1.05 (LUMIPULSE); and Q4 (n = 1588),
1.48–3.47 (IMMULYZE) or 1.06–2.92 (LUMIPULSE),
respectively. The corresponding gestational ages at deliv-
ery were 39.12 ± 1.51 weeks for Q1, 39.09 ± 1.61 weeks
for Q2, 39.01 ± 1.85 weeks for Q3, and
39.00 ± 1.58 weeks for Q4. This suggests a negative
correlation between the FT4 values in the early pregnancy
and the gestational age at delivery (p = 0.02). However,
there was no significant association between the FT4 value
in the early pregnancy and the gestational age at delivery
among the GTT cases (Table 4).
Table 3 FT4 quartiles and the gestational age at delivery (n = 6525)
Q1 (n = 1684): Q2 (n = 1662):
FT4 IMMULYZE, ng/dl 1.05–1.23 1.24–1.34
FT4 LUMIPULSE, ng/dl 0.71–0.86 0.87–0.94
GA at delivery, weeks 39.12 ± 1.51 39.09 ± 1.61
The values are expressed as the mean ± standard deviation
GA gestational age
Discussion
We investigated the pregnancy outcomes in mothers with
GTT and a normal thyroid function, and found that
although GTT increased the likelihood of onset of hyper-
emesis gravidarum, it did not increase the likelihood of
adverse pregnancy outcomes. Although the gestational age
at delivery was lower in the GTT group, GTT did not
increase the risk of preterm delivery. In addition, we found
a negative correlation between the FT4 values in the early
pregnancy and the gestational age at delivery.
In 1990, Glinoer et al. noted that the incidence of GTT
in Europe was 2–3 % [1]; this closely matched the results
of our study, in which the incidence was 2.6 %. Several
studies have examined the association between hyper-
emesis gravidarum and both GTT and hyperthyroidism,
including Graves’s disease [1, 3, 7–9]. In this study, the
rate of hyperemesis gravidarum in the GTT group was
significantly higher than that in the normal group (OR 4.19;
95 % CI 1.77–9.93; p \ 0.01), with similar results in the
multivariate analysis (OR 4.05; 95 % CI 1.53–8.94;
p \ 0.01). The mechanisms of hyperemesis gravidarum are
poorly understood and the role of hyperthyroidism in
hyperemesis gravidarum has not been determined. How-
ever, hCG is suspected to play some role in the patho-
genesis of both GTT and hyperemesis gravidarum, since
increased hCG levels are found in both conditions [8, 11].
Abortions, preterm births, stillbirths, PIH, preeclampsia,
gestational diabetes mellitus, fetal growth restriction, and
low birth weight are known to occur more frequently in
pregnancies complicated by hyperthyroidism [12–16].
GTT is not considered to be associated with adverse
pregnancy outcomes [6–9]; however, few studies have
investigated this issue. We conducted a large-scale inves-
tigation of the association between GTT and pregnancy
outcomes, and demonstrated that GTT does not increase
the risk of stillbirth, preterm birth, PIH, preeclampsia, or
low birth weight, indicating that GTT is not associated with
adverse pregnancy outcomes.
Medici et al. reported that in cases in which the FT4
values during the early pregnancy were within the normal
range, higher FT4 values increased the proportion of low
Q3 (n = 1591): Q4 (n = 1588): P for trend
1.35–1.47 1.48–3.47
0.95–1.05 1.06–2.92
39.01 ± 1.85 39.00 ± 1.58 0.02
123

Table 4 FT4 quartiles and the
gestational age at delivery in the
GTT group (n = 208) FT4 IMMULYZE, ng/dl
FT4 LUMIPULSE, ng/dl
GA at delivery, weeks
The values are expressed as the mean ± standard deviation
GA gestational age
birth weight or small for gestational age infants [17]. Leon
et al. reported similar findings [18]. Our study demon-
strated that the birth weight was significantly lower and
that the gestational age at delivery was lower in the GTT
group. The difference in the birth weight disappeared when
the analysis was adjusted for the gestational age at deliv-
ery. In addition, a comparison of the Z scores according to
birth weight revealed no significant differences. Thus, the
low birth weight was likely to have been caused by the
lower gestational age.
The previous studies have suggested that there is no
association between the FT4 values in the early pregnancy
and the gestational age at delivery or the frequency of
preterm delivery [17, 18]; however, Chin et al. suggested a
weak but a significant negative correlation between the
second trimester FT4 values and the gestational age at
delivery, but not between the thyroid hormone levels and
the birth weight [19]. Our study revealed that GTT was
associated with a shorter gestational period. Furthermore,
regardless of the presence of GTT, a negative correlation
was observed between the FT4 values in the early preg-
nancy and the gestational period. Notably, even at the
highest FT4 quartile, the average gestational period
(38.98 ± 1.60 weeks) was well within the full-term limits.
Furthermore, there was no association between the FT4
value in the early pregnancy and the gestational age at
delivery among the GTT cases. These observations support
the conclusion that GTT does not adversely affect preg-
nancy outcomes.
The mechanism through which hyperthyroidism
increases the incidence of preterm delivery and low birth
weight is unclear. It is possible that changes in maternal
metabolism due to hyperthyroidism affect the development
of the placenta and the fetus [20]. Similarly, in this study,
the high FT4 values in the GTT group during the early
pregnancy may have affected the maternal metabolism
during the formation of the placenta, leading to a shorter
gestational period.
One of the limitations of this study is its retrospective
design. There were many participants with high FT4 values
during the early pregnancy who we could not be followed-
up, which may mean that many cases of GTT were thus
potentially undetected. Moreover, although the subjects’
FT4 levels were measured before 16 weeks of gestation,
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Arch Gynecol Obstet
Q1 (n = 55) Q2 (n = 53) Q3 (n = 49) Q4 (n = 51) P for trend
1.77–1.99 2.00–2.14 2.16–2.34 2.35–3.47
1.28–1.39 1.40–1.51 1.53–1.80 1.81–2.92
38.50 ± 1.82 38.70 ± 2.30 38.90 ± 1.59 38.70 ± 1.28 0.54
the variability in the measurement dates means that the
blood tests may have been performed before or after the
peak hCG levels were reached. Thus, it is possible that
there were cases of undetected GTT within the normal
group.
In conclusion, although the proportion of patients with
hyperemesis gravidarum was higher in the GTT group,
GTT was not associated with adverse pregnancy outcomes.
Although GTT led to a shorter gestational period, it did not
increase the risk of preterm delivery. Moreover, it was
shown that higher FT4 values in the early pregnancy led to
a shorter gestational period.
Acknowledgments We would like to thank Dr. Julian Tang of the
Department of Education for Clinical Research, National Center for
Child Health and Development, for proofreading, editing, and
rewriting parts of this manuscript.
Compliance with ethical standards
Funding The authors received no funding for this study.
Conflict of interest All of the authors declare that they have no
conflicts of interest.
Ethical approval All procedures performed in studies involving
human participants were in accordance with the ethical standards of
the institutional and/or national research committee and with the 1964
Helsinki declaration and its later amendments or comparable ethical
standards.
This article does not contain any studies with animals performed by
any of the authors.
Informed consent Data were collected without any personal iden-
tifiers of the study participants, so individual informed consent was
considered not necessary and was not obtained. All data were anon-
ymized and de-identified prior to analysis. If the study participants
disagreed with this study, they could choose an opt-out. The institu-
tion review boards of National Center for Child Health and Devel-
opment approved this study protocol (No. 80, approved at November
27, 2014).
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