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Pediatrics and Neonatology (2016) xx, 1e5

Available online at www.sciencedirect.com

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ORIGINAL ARTICLE

Complications in Infants of Diabetic Mothers

Related to Glycated Albumin and
Hemoglobin Levels During Pregnancy
Daisuke Sugawara*, Asami Maruyama, Toshiyuki Imanishi,
Yohei Sugiyama, Ko Ichihashi

Department of Pediatrics, Saitama Medical Center Jichi Medical University, Saitama, Japan

Received Aug 21, 2015; received in revised form Dec 3, 2015; accepted Feb 5, 2016
Available online - - -

Key Words Background: This study was conducted to investigate whether glycated albumin is a useful gly-
gestational diabetes; cemic marker from the point of view of infant complications for monitoring glycemic control in
glycosylated pregnant women with diabetes or gestational diabetes mellitus.
hemoglobin A; Methods: We retrospectively studied 42 Japanese infants of diabetic mothers and their mothers
infant; at our facility between May 2010 and July 2013. The mean glycated albumin and glycated hemo-
serum albumin globin levels were compared between mothers of infants with complications and those without
complications. We used 15.8% as the cutoff value of glycated albumin and calculated the sensi-
tivity and specificity of items that were significantly different between the two groups.
Results: Glycated albumin was significantly higher in mothers of infants with hypoglycemia
(15.5
1.8 vs. 13.8
1.2%, p Z 0.001), respiratory disorders (15.6
1.8 vs. 13.9
1.2%,
p < 0.001), hypocalcemia (15.7
2.1 vs. 14
1.2%, p Z 0.004), myocardial hypertrophy
(15.2
1.9 vs. 13.7
1%, p Z 0.007), and large-for-date status (15.8
1.9 vs. 14
1.3%,
p Z 0.002). By contrast, considering hypoglycemia, glycated hemoglobin was not significantly
different between the two groups. The sensitivity and specificity with 15.8% as the cutoff value
of glycated albumin were as follows: hypoglycemia (70% and 81.2%), respiratory disorders (61.5%
and 82.8%), hypocalcemia (62.5% and 84.4%), myocardial hypertrophy (87.5% and 79.4%), and
large-for-date status (75% and 85.3%).
Conclusion: Glycated albumin is a useful marker of glycemic control considering infant complica-
tions during pregnancy. This study also suggests that evaluating both glycated hemoglobin and gly-
cated albumin levels can lead to better glycemic control in pregnant women.
Copyright ª 2016, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/
by-nc-nd/4.0/).

* Corresponding author. Department of Pediatrics, Saitama Medical Center Jichi Medical University, 1e847 Amanuma-cho, Saitama 330-
8503, Japan.
E-mail address: d.sugawara@jichi.ac.jp (D. Sugawara).

http://dx.doi.org/10.1016/j.pedneo.2016.02.003
1875-9572/Copyright ª 2016, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Sugawara D, et al., Complications in Infants of Diabetic Mothers Related to Glycated Albumin and
Hemoglobin Levels During Pregnancy, Pediatrics and Neonatology (2016), http://dx.doi.org/10.1016/j.pedneo.2016.02.003
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2 D. Sugawara et al
1. Introduction
Infants of diabetic mothers (IDMs) often have complications
associated with fetal hyperinsulinemia induced by maternal
hyperglycemia.1 In the first trimester, maternal hypergly-
cemia can cause diabetic embryopathy, which results in
major birth defects and spontaneous abortions. In the
second and third trimesters, maternal hyperglycemia can
cause fetal hyperglycemia, hyperinsulinemia, hypocalce-
mia, polycythemia, hyperbilirubinemia, myocardial hyper-
trophy, delayed lung maturation, and large-for-date
status.2
Glycated hemoglobin (HbA1c), the current gold standard
marker for glycemic control, reflects blood glucose levels
over the previous 2e3 months. However, the HbA1c level is
affected by an abnormal erythrocyte life span, which may
occur in iron deficiency anemia.3 Pregnant women with
diabetes mellitus or gestational diabetes mellitus (GDM)
often develop iron deficiency anemia; therefore, HbA1c
may be insufficient for assessing glycemic control in these
women.
Recent reports have advocated the use of glycated al-
bumin as a marker of glycemic control.4e7 Compared with
HbA1c, glycated albumin reflects shorter-term blood
glucose levels (the previous 2e3 weeks as opposed to the
previous 2e3 months) and is unaffected by the erythrocyte
life span.8 Therefore, glycated albumin may be a useful
marker for glycemic control during pregnancy. However,
few studies have examined the association between gly-
cated albumin in diabetic mothers and complications in
IDMs.9 Therefore; we investigated whether glycated albu-
min is a useful glycemic marker for monitoring glycemic
control in pregnant women with diabetes or gestational
diabetes.
2. Methods
2.1. Study design and participants
We performed a retrospective study of 59 Japanese IDMs
and their mothers (including women with GDM), who were
admitted to our facility between May 2010 and July 2013.
Seventeen cases were excluded because the mother’s gly-
cated albumin level was not measured or because of the
presence of hepatic disease, renal disease, or obesity [body
mass index (BMI)  30]; therefore, 42 IDMs were included in
the final analysis.
We retrieved the mother’s age, gestational week, num-
ber of previous pregnancies, BMI (prior to the pregnancy),
glycated albumin level, HbA1c, diabetes type, family his-
tory of diabetes mellitus, systolic and diastolic blood
pressure, infant birth weight, and infant complications. The
glycated albumin and HbA1c values measured within 1
month prior to birth were used in the analyses. The com-
plications assessed were hypoglycemia, respiratory disor-
ders, hypocalcemia, polycythemia, hyperbilirubinemia,
myocardial hypertrophy, and large-for-date status. Malfor-
mations were excluded from the analysis owing to their
occurrence prior to the 7th gestational week.10 Maternal
diabetes mellitus was diagnosed according to the Japan
Diabetes Society (JDS) criteria.11 Mothers with preexisting
Please cite this article in press as: Sugawara D, et al., Complications in Infants of Diabetic Mothers Related to Glycated Albumin and
Hemoglobin Levels During Pregnancy, Pediatrics and Neonatology (2016), http://dx.doi.org/10.1016/j.pedneo.2016.02.003
diabetes mellitus were treated with insulin subcutaneous
injections. GDM was diagnosed according to the criteria of
the International Association of Diabetes and Pregnancy
Study Groups.12 Infant complications were defined as fol-
lows: hypoglycemia Z blood glucose < 1.9 mmol/L; respi-
ratory disorders Z infants that required oxygenation;
hypocalcemia Z serum calcium levels < 2.0 mmol/L;
polycythemia Z serum hematocrit levels > 0.65/L;
hyperbilirubinemia Z infants that required phototherapy;
myocardial hypertrophy Z interventricular septum thick-
ness > 5 mm on ultrasound; and large-for-date
status Z birth weight > 90th percentile for gestational age.
2.2. Laboratory analysis
HbA1c (%) was measured by high-performance liquid chro-
matography and was calibrated using JDS Lot 2. HbA1c was
estimated as the National Glycated Hemoglobin Standard
Program (NGSP) equivalent value and the estimated Inter-
nal Federation of Clinical Chemistry (IFCC) equivalent value
using the following formulae: HbA1c Z HbA1c (JDS) þ 0.4
(%) and NGSP Z (0.9148  IFCC) þ 2.152, respectively.11,13
Glycated albumin was measured enzymatically using keto-
amine oxidase, an albumin-specific proteinase, and albu-
min assay reagent (Lucica GA-L; Asahi Kasai Pharma Co.,
Tokyo, Japan).14
2.3. Statistical analysis
We checked whether any factors (mother’s age, BMI,
gestational week, systolic blood pressure, diastolic blood
pressure, or type of delivery) were significantly different in
IDMs with and without complications (hypoglycemia, res-
piratory disorders, hypocalcemia, polycythemia, hyper-
bilirubinemia, myocardial hypertrophy, and large-for-date
status). Then, multivariable regression analysis was per-
formed to determine whether glycated albumin is an in-
dependent predictor of neonatal complications of IDM. We
compared the mean glycated albumin and HbA1c values
between IDMs with and without complications. We con-
ducted the post hoc test to calculate the sample power of
adequate equations by adopting an error probability of 5%
for the sample size used. The sample power (1 e b error
probability) was 0.831. We used 15.8% as the cutoff value
for glycated albumin and calculated the sensitivity and
specificity of items that were significantly different be-
tween the two groups. We also calculated the odds ratios
and 95% confidence intervals for the prevalence of each
complication at the determined cutoff value. All data are
presented as mean
standard deviation. The Kolmogor-
oveSmirnov goodness-of-fit test was performed to deter-
mine whether data were normally distributed. Two-sided
Student t tests or Welch t tests were used to determine
possible differences between the two groups. Sample
power calculations were performed using the G*Power
software version 3.0.10 (Franz Faul, University of Kiel, Kiel,
Germany),15 and other statistical analyses were performed
using EZR 1.10 software (Saitama Medical Center, Jichi
Medical University, Saitama, Japan).16 The level of signifi-
cance was set at p < 0.05 in all analyses. This study was
approved by the Ethics Review Board of our facility.
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Glycemic control markers during pregnancy 3

3. Results respiratory disorders, hypocalcemia, polycythemia, hyper-

Baseline characteristics of the study population are shown
in Table 1. Glycated albumin and HbA1c were significantly
different between cases and controls (15.3
1.6 vs.
13.3
1.1%, p < 0.01 and 5.9
0.3 vs. 5.6
0.4%,
p Z 0.03, respectively). Twenty-five IDMs presented with
complications; 17 (40.4%) had myocardial hypertrophy; 13
(30.9%) had hypoglycemia; 11 (26.1%) had respiratory dis-
orders; nine (21.4%) had hypocalcemia; eight (19%) were
large for date; six (14.2%) had hyperbilirubinemia; and four
(9.5%) had polycythemia. There were no cases of myocar-
dial hypertrophy combined with heart failure. All infants
with hypoglycemia improved following intravenous glucose
infusion. One infant required ventilation after the diagnosis
of respiratory distress syndrome. None of the infants had
hypoglycemia-induced convulsions. All of the infants with
hyperbilirubinemia and polycythemia showed improve-
ments following phototherapy and intravenous glucose
infusion, respectively.
We checked whether any factors (mother’s age, BMI,
gestational week, systolic blood pressure, diastolic blood
pressure, or type of delivery) were significantly different in
IDMs with and without each complication (hypoglycemia,
bilirubinemia, myocardial hypertrophy, and large-for-date
status), and there were no significant differences between
these two groups. Multivariable regression analysis
revealed glycated albumin to be a significant independent
predictor of neonatal complications of IDMs (R2 Z 0.572,
standard error Z 0.15%, t Z 3.8, p < 0.01). We compared
mean glycated albumin and HbA1c values for each
complication between IDMs with and without complications
(Table 2). Glycated albumin differed significantly between
the mothers of infants with versus without hypoglycemia
(15.5
1.8 vs. 13.8
1.2%, p Z 0.001), respiratory disor-
ders (15.6
1.8 vs. 13.9
1.2%, p < 0.001), hypocalcemia
(15.7
2.1 vs. 14
1.2%, p Z 0.004), myocardial hyper-
trophy (15.2
1.9 vs. 13.7
1%, p Z 0.007), and large-for-
date status (15.8
1.9 vs. 14
1.3%, p Z 0.002). By
contrast, HbA1c differed significantly between mothers of
infants with respiratory disorders (6.4
0.8 vs. 5.7
0.4%,
p Z 0.002), myocardial hypertrophy (6.2
0.7 vs.
5.7
0.4%, p Z 0.009), and large-for-date status (6.6
0.8
vs. 5.7
0.4%, p < 0.001). As for hypoglycemia, HbA1c was
not significantly different between the two groups
(6.1
0.4 vs. 5.8
0.6%, p Z 0.2).

Table 1 Baseline characteristics.

Case Control p
Number of mothers, n 25 17
Age, y
SD 35.1
4.6 34.9
3.5 0.78
BMI prior to 22.8
2.4 23.8
2.8 0.69
pregnancy, kg/
m2
SD
Gestational week, 38.2
1.4 38.1
1.0 0.85
wk
SD
Previous pregnancy 6 4
Baby’s birth weight, 3211
434 2977
463 0.11
g
SD
Systolic blood 113.7
9.7 109.3
8.3 0.2
pressure,
mmHg
SD
Diastolic blood 75.1
8.4 74.2
8.2 0.72
pressure,
mmHg
SD
Glycated albumin, 15.3
1.6 13.3
1.1 <0.01
%
SD
HbA1c, %
SD (NGSP) 5.9
0.3 5.6
0.4 0.03
HbA1c, mmol/ 40.8
3.7 37.8
4.5 0.03
mol
SD (IFCC)
Family history of 6 9
diabetes mellitus
Type of mother’s
diabetes mellitus
Type 1 diabetes 4 2
mellitus
Type 2 diabetes 1 0
mellitus
Gestational diabetes 19 16
mellitus
BMI Z body mass index; HbA1c Z glycated hemoglobin; IDMs Z infants of diabetic mothers; IFCC Z Internal Federation of Clinical
Chemistry; NGSP Z National Glycated Hemoglobin Standard Program; SD Z standard deviation.

Please cite this article in press as: Sugawara D, et al., Complications in Infants of Diabetic Mothers Related to Glycated Albumin and
Hemoglobin Levels During Pregnancy, Pediatrics and Neonatology (2016), http://dx.doi.org/10.1016/j.pedneo.2016.02.003
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4 D. Sugawara et al

Table 2 Comparison of glycated albumin and HbA1c in complication of IDMs.

Case Control p
Glycated albumin (%
SD)
Hypoglycemia 15.5
1.8 13.8
1.2 0.001y
Respiratory disorder 15.6
1.8 13.9
1.2 <0.001*
Hypocalcemia 15.7
2.1 14.0
1.2 0.004y
Hypervolemia 15.0
2.3 14.3
1.5 0.4y
Hyperbilirubinemia 14.4
1.5 14.3
1.6 0.9*
Myocardial hypertrophy 15.2
1.9 13.7
1.0 0.007y
Large for date 15.8
1.9 14.0
1.3 0.002*
HbA1c (%
SD, mmol/mol)
Hypoglycemia 6.1
0.4 (43.5
1.5) 5.8
0.6 (40.5
1.3) 0.2y
Respiratory disorder 6.4
0.8 (46.6
1.5) 5.7
0.4 (39.6
4.9) 0.002y
Hypocalcemia 6.2
0.5 (45.0
6.1) 5.8
0.6 (40.4
6.9) 0.08*
Hypervolemia 6.2
0.5 (45.2
5.6) 5.9
0.6 (41.0
7.0) 0.2*
Hyperbilirubinemia 5.7
0.5 (39.1
5.6) 5.9
0.6 (41.8
7.0) 0.3*
Myocardial hypertrophy 6.2
0.7 (45.2
8.3) 5.7
0.4 (39.4
4.4) 0.009y
Large for date 6.6
0.8 (49.3
9.2) 5.7
0.4 (39.5
4.7) <0.001y
HbA1c Z glycated hemoglobin; IDMs Z infants of diabetic mothers; SD Z standard deviation.
* Student’s t test.
y
Welch’s t test.

The sensitivity, specificity, and odds ratios for the gly- There were several cases in this study in which HbA1c levels
cated albumin cutoff values (15.8%) are shown in Table 3. The were within the normal range, but glycated albumin levels
odds ratios for all parameters were statistically significant, were high. This might have been caused by glycated albu-
and the sensitivity and specificity were relatively high. min reflecting more short-term glycemic control. Second,
glycated albumin is unaffected by iron metabolism. Iron
deficiency anemia is often observed in late pregnancy
4. Discussion because of increased iron demand, and HbA1c levels are
higher relative to the actual glycemic state in patients with
The results of the present study showed that glycated al- iron deficiency anemia. Because glycated albumin is not
bumin was a useful glycemic marker from the point of view correlated with hemoglobin, it is not affected by iron
of infant complications for monitoring glycemic control in deficiency anemia.5,18 There were several cases in this
pregnant women with diabetes or gestational diabetes. It study in which HbA1c levels were high but glycated albumin
was recently reported in Japan that glycated albumin is a levels were within the normal range. Thus, we can better
more useful marker for glycemic control during pregnancy determine the blood sugar status of pregnant women by
than HbA1c. Glycated albumin is a ketoamine formed by evaluating both HbA1c and glycated albumin levels. Hir-
nonenzymatic glycation of serum albumin.14 Glycated al- amatsu et al19 reported that glycated albumin levels in
bumin is a more useful marker than HbA1c for several healthy pregnant Japanese women ranged from 11.5% to
reasons. First, the half-life of albumin is approximately 15 15.7%. Meanwhile, Shimizu et al9 reported that hypoglyce-
days; therefore, glycated albumin increases in the presence mia, respiratory disorders, and polycythemia were signifi-
of hyperglycemia and reflects mean glycemia over a period cantly more frequent in infants of mothers (including those
of approximately 2 to 3 weeks.17 Thus, glycated albumin is with GDM) with a glycated albumin level 15.8% than in
a better index of short-term glycemic control than HbA1c. infants of mothers with a glycated albumin level <15.8%.9
They also reported that the frequency of complications
did not differ significantly between infants whose mothers
Table 3 Sensitivity, specificity, and odds ratio at a gly- (including those with GDM) had an HbA1c level 5.8%
cated albumin cutoff value of 15.8%. (40 mmol/mol) and those with HbA1c levels <5.8%
Sensitivity Specificity Odds ratio p (40 mmol/mol).9 Our study results confirmed that glycated
(%) (%) (95% CI) albumin is useful from the point of view of infant compli-
cations for monitoring glycemic control in pregnant women
Hypoglycemia 70 81.2 3.7 (1.6e8.5) 0.001 with diabetes or gestational diabetes, consistent with the
Respiratory 61.5 82.8 3.5 (1.4e8.3) 0.01 results reported by Shimizu et al.9
disorder This study has several limitations. First, this was a
Hypocalcemia 62.5 84.4 4 (1.5e7.2) 0.02 single-center study, so the number of participants was
Myocardial 87.5 79.4 4.2 (2e8.6) 0.001 small. Larger studies are recommended to confirm our re-
hypertrophy sults. Second, we studied only Japanese IDMs and their
Large for date 75 85.3 5.1 (2e12.5) 0.002 mothers. There might be ethnic differences in glycated
CI Z confidence interval. albumin, but the reference range of glycated albumin in an

Please cite this article in press as: Sugawara D, et al., Complications in Infants of Diabetic Mothers Related to Glycated Albumin and
Hemoglobin Levels During Pregnancy, Pediatrics and Neonatology (2016), http://dx.doi.org/10.1016/j.pedneo.2016.02.003
 + MODEL
Glycemic control markers during pregnancy
American population is 11.9e15.8%, which is close to the
reference range for Japanese women.20
Furthermore, glycated albumin is affected by albumin
metabolism. Glycated albumin is artificially low relative to
glycemic status in conditions associated with increased al-
bumin metabolism, such as hyperthyroidism, nephrotic
syndrome, steroid use, and obesity.7 We must be aware of
the limitations of this test in those patients. There were no
patients with hyperthyroidism, nephrotic syndrome, or
steroid use in our study, and we excluded obese patients. In
conclusion, our study has shown that glycated albumin is a
useful marker of glycemic control in pregnant diabetic
women. Because the glycated albumin level can be
measured easily and accurately using an enzymatic
method, it can be measured without pretreatment along-
side common biological markers, such as glucose, which
should encourage wider use. This study also suggests that
evaluating both HbA1c and glycated albumin levels can lead
to better glycemic control in pregnant women. Neverthe-
less, further studies are required to confirm the utility of
glycated albumin as a marker of glycemic control during
pregnancy.
Conflict of interest
The authors declare no conflict of interest. The authors
received no support for this work in the form of grants,
equipment, or drugs.
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