endokrynologia pediatryczna pediatric endocrinology · 2015. 2. 26. · rodki matek chorujących na...

35

Dawid G. i inni: Infants of Diabetic Monthers: Morphological Heart Parameters, Cord Blood Insulin, Glucose Concentration at Birth and Echocardiographic...

Vol. 8/2009 Nr 4(29)

Endokrynologia PediatrycznaPediatric Endocrinology

ABSTRACT/STRESZCZENIE

Objective. One of the well known disturbances in infants of diabetic mothers (IDM) is hypertrophic cardiomyopathy (HCM). We analyzed the relationship between morphological heart parameters and cardiac function, cord blood insu-lin, fructosamine and glucose concentration at birth and the natural history of echocardiographic findings during the first year of life. Material and methods. 77 infants: 44 infants of diabetic mothers (IDM) and 30 control subjects from birth to the age of 12 months were prospectively evaluated by echocardiography. The diabetic group covered 7 prege-stational diabetes mothers (PGDM) and 37 gestational diabetes mothers (GDM), 18 treated with diet only (G-1) and 19 with insulin (G-2). 18.2% of IDM were born as large for gestational age (LGA), while in the control group all but one neonates were appropriate for gestational age (AGA). In IDM venous cord blood samples were collected at deli-very and analyzed for insulin and fructosamine level, while glycemia was analyzed in capillary blood. Results. Cord blood insulin (Ic) level was significantly higher in PGDM (p < 0.01) than in both GDM groups (G-1 and G-2). In the G-2 group a significant positive association was found between Ic level and blood flow through mitral valve (MV). In-terventricular septum (IVS) diameter was significantly higher (p < 0.01) in diabetic, especially in G-2 group. In 38.6% of IDM, the enlargement of the IVS was noticed. The ratio of IVS/LVPW in the control group was 1.03 ± 0.14, while

Infants of Diabetic Mothers: Morphological Heart Parameters, Cord Blood Insulin, Glucose Concentration at Birth and Echocardiographic Findings During the First Year of Life

Niemowlęta urodzone przez matki z cukrzycą ciężarnych: stężenia insuliny we krwi pępowinowej, stężenia glukozy, ocena echokardiograficzna serca przeprowadzona po urodzeniu oraz w pierwszym roku życia

1Dawid Grażyna, 1Horodnicka-Józwa Anita, 1Biczysko-Mokosa Agnieszka, 1Petriczko Elżbieta, 2Engel Karina

1Department of Pediatrics, Endocrinology, Diabetology, Metabolic Diseases and Cardiology of Developmental Age, Pomeranian Medical University, Szczecin, Poland,2Department of Maternal – Fetal Medicine, Pomeranian Medical University, Szczecin, Poland

Corresponding author: Grażyna Dawid MD, PhD, Department of Pediatrics, Endocrinology, Diabetology, Metabolic Diseases and Cardiology of Developmental Age Pomeranian Medical University, Szczecin, Poland, 71-252 Szczecin, Poland, ul. Unii Lubelskiej 1, phone + 48 (91) 425 31 66, fax + 48 (91) 425 31 67, e-mail address: [email protected]

Key words: gestational diabetes, infant of diabetic mother, hypertrophic cardiomyopathySłowa kluczowe: cukrzyca ciężarnych, noworodek matki chorującej na cukrzycę, kardiomiopatia przerostowa

36

Praca oryginalne Endokrynol. Ped., 8/2009;4(29):35-44

37


in IDM it was significantly (p < 0.001) higher – 1.32 ± 0.52. During 12-month observation the resolution of HCM was confirmed. Conclusions. Infants born to mothers with diabetes first recognized during pregnancy and treated with in-sulin (G-2) are at high risk of developing HCM. The Resolution of HCM to normality was confirmed during 12 mon-ths. Pediatr. Endocrinol. 8/2009;4(29):35-44.

Cel pracy. Kardiomiopatia przerostowa częściej występuje u noworodków matek chorujących na cukrzycę. Celem pracy była ocena zmian echokardiograficznych u noworodków matek chorujących na cukrzycę a także ustalenia dyna-miki ustępowania zmian w trakcie 12-miesięcznej obserwacji oraz ocena korelacji między zmianami występującymi w sercu a poziomem insuliny, fruktozaminy i glukozy u noworodka w momencie urodzenia. Materiał i metody. Pro-spektywnymi badaniami echokardiograficznymi od urodzenia do 12 miesiąca życia objęto 74 noworodki: 44 nowo-rodki matek chorujących na cukrzycę (IDM) i 30 noworodków matek zdrowych. Grupę matek chorujących na cukrzy-cę stanowiło: 7 noworodków matek z cukrzycą przedciążową (PGDM) i 37 noworodków matek z cukrzycą ciężarnych (GDM), w tym 18 leczonych dietą (G1) i 19 leczonych insuliną (G2). 18,2% of IDM stanowiły noworodki z cecha-mi makrosomii (LGA) a w grupie kontrolnej wszystkie z wyjątkiem jednego były urodzone z masą ciała odpowied-nią do wieku ciążowego. U noworodków matek cukrzycowych poziom insuliny i fruktozaminy był oznaczony z krwi pępowinowej a poziom glukozy z krwi włośniczkowej. Wyniki. Poziom insuliny we krwi pępowinowej był istotnie statystycznie wyższy w grupie noworodków matek z cukrzycą przedciążową (p < 0,01) w porównaniu z grupą nowo-rodków matek z cukrzycą rozpoznaną w trakcie ciąży (G-1 and G-2). W grupie G-2 stwierdzono istotną statystycznie korelację między poziomem insuliny we krwi pępowinowej a prędkością przepływu przez zastawkę mitralną (MV). Średni wymiar przegrody międzykomorowej IVS był istotnie statystycznie wyższy w grupie noworodków matek cu-krzycowych, szczególnie w grupie G2. U 38,6% noworodków matek cukrzycowych stwierdzono przerost przegro-dy międzykomorowej. Stosunek wymiaru przegrody międzykomorowej do tylnej ściany lewej komory (IVS/LVPW) w grupie kontrolnej wynosiło 1,03 ± 0,14 a w grupie noworodków matek chorujących na cukrzycę było istotnie staty-stycznie wyższe (p < 0,001) i wynosiło – 1,32 ± 0,52. Podczas 12-miesięcznej obserwacji zmiany ustąpiły. Wnioski. Noworodki matek chorujących na cukrzycę rozpoznaną po raz pierwszy w trakcie ciąży i leczonych insuliną znajdują się w grupie zwiększonego ryzyka występowania kardiomiopatii przerostowej, zmiany w sercu miały charakter przej-ściowy i ustąpiły podczas pierwszego roku życia. Endokrynol. Ped. 8/2009;4(29):35-44.

Introduction

The term cardiomyopathy refers to a variety of myocardial abnormalities. Among them, hypertrophic cardiomyopathy observed in infants born to diabetic mothers was described [1–4]. This asymmetric septal enlargement with disproportional hypertrophy septum is an anabolic result of fetal hyperinsulinemia caused by maternal hyperglycemia during the third trimester [5–7]. In the patients with HCM the M-mode echocardiography shows hypertrophy of the left ventricle (LV), usually with much more striking involvement of the ventricular septum (IVS). That may result in dynamic and clinically significant left ventricular outflow obstruction. It was described that in IDM, the ratio of the ventricular septal thickness to the left ventricular posterior wall thickness in diastole (IVS/LVPW ratio) greatly exceeds the upper limit of normality, which means the value of 1.3 [1, 6, 7]. Left-ventricular end-diastolic dimension is normal or decreased and shortening fraction (SF%) is normal or supranormal [5, 7]. The severity of cardiomyopathy can vary from an incidental finding on echocardiography to an infant with severe symptoms of congestive heart failure. All symptoms

spontaneously regress within a few weeks. The resolution of septal hypertrophy occurred during the first two to twelve months of life [5].

It is believed that careful management of diabe-tes with a well glycemic control during pregnancy may reduce the severity of hypertrophic cardiomy-opathy [6–12]. It was also noticed that cardiac sep-tum hypertrophy in IDM correlates with high le-vels of fetal insulin better than with macrosomia [13, 7].

The aim of this study was to analyze the relation-ship between morphological heart parameters and cardiac function assessed during echocardiography examination in infants of diabetic mothers, cord blo-od insulin, and fructosamine concentration at birth as well as to follow the natural history of echocardio-graphic findings during the first year of life.

Material

The total of 74 infants (30 of healthy mothers and 44 infants born to diabetic mothers) were pro-spectively evaluated in the study. The diabetic gro-up covered 7 infants born to insulin-dependent PGDM, and 37 born to GDM.

36


37


Gestational diabetes mellitus was recognized on the basis of oral glucose tolerance test (OGTT) per-formed between 24–28 week of pregnancy with load of 75 g glucose. In 18 pregnant women diabetes was treated only with diet and classified as G-1; in 19 others treated with insulin it was classified as G-2.

Gestational age was in the range between 35 to 40 week of pregnancy in the diabetic group and be-tween 30 to 41 in the control group. However, the rate of pre-term deliveries in the diabetic group (43.3%) was significantly higher (p < 0.01) than in the control one (20.4%).

Birth weight was in the range from 1950 g to 4450 g in the diabetic group, and between 1000 g to 4300 g in control subjects. The Comparison of the birth weight between the diabetic and control group is shown in Figure 1. The mean birth weight in the diabetic groups was significantly higher than

in the control group. Furthermore, macrosomia de-fined by a birth weight above the 90th percentile was recognized in 9 neonates. In the diabetic group 8 (18.2%) out of 44 IDM were born as large for gesta-tional age (LGA), and 35 as appropriate for gesta-tional age (AGA). In the control group all but one neonates were born as appropriate for gestational age (AGA).

Methods

In offsprings of diabetic mothers venous cord blood samples were collected at the delivery and analyzed for insulin and fructosamine level; next, one hour after delivery glucose level was measured in capillary blood. Fructosamine and insulin levels served as indirect markers of maternal glycemic control during the last days before delivery.

Fig. 1. The Comparison of the birth weight [g] in the analyzed groupsRyc. 1. Porównanie masy urodzeniowej ciała (g) w analizowanych grupach

birth weigh: ANOVA Kruskal-Wallis H(3, n = 72) = 13.55, p = 0.004;F(3.68) = 5.91, p = 0.001

(a)" tBF(45) = −4.42, p = 0.00006;UMW = 100 (Z = −3.52), p = 0.0004

(b)" tBF(45) = −2.25, p = 0.03;UMW = 166 (Z = −2.08), p = 0.04

(c) t(34) = 2.37, p = 0.02heteroscedasticity

11 2 F = 3.64, p = 0.007;Levene (45) = 8.11, p = 0.007;Brown-Forsyth(45) = 7.03, p = 0.01

11 3 F = 2.60 p = 0.04

[g]

38


39


Electrochemiluminescency method “Eclia” ana-lyzer Cobas 6000 Roches Company was used to measure insuline levels. Colorimetric method Inte-gra 400 analyzer was used for the determination of fructosamine level and enzymatic method based on hexokinase with Cobas 6000 Roches Company was used for glucose levels.

Echocardiography was performed in all patients over the period of one year; first measurements were done at the age of the first 48 hours of life and next at every 2–4 months up to 12 months of life. The values obtained after the delivery and at the age of 12 months were compared between diabetic and control group, and analyzed statistically.

Echocardiography measurements were done according to the recommendations of The American Society of Echocardiography. Morphological para-meters were determined using M-mode echo-cardiography, and two-dimensional and Doppler techniques were used to diagnose congenital heart disease [14]. Echocardiography was performed with the patient at rest in the partial left decubitus position utilizing standard parasternal, short axis and apical views. M-mode echocardiographic view of the left ventricular cavity was recorded under two-dimensional control. Measurements or calculation of the following parameters: end diastolic dimension of interventricular septal thickness (IVSd), left ventricular posterior wall thickness (LVPW), left ventricular end diastolic dimension (LVDd), left ventricular end systolic dimension (LVDs), left atrium diastolic dimension (LAD), aortic diameter on the level of aortic valve (vAo) were carried out. In addition, blood flow through mitral valve (MV), tricuspid valve (TV), aortic valve (Ao), pulmonary artery valve (PA) was measured. All measurements were done according to the recommendations of The American Society of Echocardiography [15, 16]. Fractional shortening (SF%) was also calculated according to the rule [16, 17]:

The Data were analyzed using Statistica 6.0 com-puter software. The Shapiro–Wilk test was used to assess distribution normality for each variable. The Data were compared between groups using ANOVA procedures and Mann–Withney U-test. Depending on the normality the data were expressed as mean ± standard deviation or median and ranges (mini-mum, maximum). Moreover, to compareg the fre-quency between the analyzed groups, χ2 and Yates χ2 were used. P values less than 0.05 were conside-red significant.

Results

The values of insulin, fructosamine and glucose level evaluated at birth are presented in Table 1.

Cord blood insulin (Ic) level was significantly higher in PGDM (p < 0.01) than in both GDM gro-up (G-1 and G-2) (Fig. 2). A tendency to positive association between LVDd and Ic levels was noti-ced, however the relationship did not reach a signi-ficant level (p < 0.08). No significant correlation be-tween Ic levels and IVS, IVS/LVPW ratio, and SF% was observed.

Cord blood fructosamine levels did not differ si-gnificantly between the diabetic groups (Table 1). In the G-2 group a significant positive association was found between Ic level and LAD, and blood flow through mitral valve (MV). Yet, any signifi-cant correlation between cord blood fructosamine levels and IVS, and IVS/LVPW ratio, and SF% was not found. Similarly, no significant correlations be-tween cord blood fructosamine levels and IVS, and IVS/LVPW ratio and SF% were found.

There was no significant difference of glycemia levels between the diabetic groups and in all groups glycemia levels were in a normal range (Table 1).

During echocardiography examinations some anatomic abnormalities were found in 11 newborns. 8 heart abnormalities were recognized in IDM and 3 in control subjects. In the diabetic group, 4 cases of ventricular septum defect (VSD) were recogni-zed. Furthermore, one newborn had an atrio-ven-tricular septum defect and 3 others displayed atrial septum defect (ASD). In the control group 2, VSD and 1 ASD were noticed. During one year of echo-cardiography and cardiology observation, none of the examined IDM needed pharmacology or surgi-cal treatment.

The echocardiographic results found in diabetic group are compared with normal values obtained in matched age and birth weight newborns from the

LVDd – LVDsLVDd( (x 100%

Furthermore, the ratio of the left ventricular septal thickness to the left ventricular posterior wall thickness in diastole (IVS/LVPW ratio) was calculated. Echocardiography examination was per-formed using HDI Phillips model with either a 3.5 or 5.0 mHz transducer. All echocardiographic measurements were carried out by the same observer (G. David).

38


39


insulin: ANOVA Kruskal-Wallis H(2, n = 36) = 9.68, p = 0.008;(a)"UMW = 1.00 (Z = −3.22), p = 0.001(b)"UMW = 9.00 (Z = −2.49), p = 0.001

Fig. 2. The Comparison of the cord blood insulin levels [µU/ml] between the analyzed groups of neonates from diabetic mothersRyc. 2. Porównanie poziomu insuliny we krwi pępowinowej [µU/ml] w analizowanych grupach noworodków matek chorujących na cukrzycę

Table 1. Cord blood insulin, fructosamine and newborns’ glycemia in the analyzed groups of infants of diabetic mothersTabela 1. Poziom insuliny, fruktozaminy we krwi pępowinowej i glikemia noworodkowa w analizowanych grupach noworod-ków matek chorujących na cukrzycę

G1 G2 PGDM

N

Mea

n±

SD

Med

ian±

qua

rtile

rang

e

Min

imum

Max

imum

N

Mea

n±

SD

Med

ian±

qua

rtile

rang

e

Min

imum

Max

imum

N

Mea

n±

SD

Med

ian±

qua

rtile

rang

e

Min

imum

Max

imum

Fructosamine/Fruktozamina [µmol/L]

11207.15 204.00 183.00

12197.30 203.25 144.00

5213.00 222.00 181.00

22.69 16.00 261.00 29.63 24.68 243.00 29.25 19.50 251.00Glycemia/Glikemia [mg%]

1659.19 54.00 42.00

1756.35 59.00 38.00

661.17 60.50 51.00

18.82 2.50 122.00 10.42 6.00 75.00 9.66 7.50 76.00Insulin/Insulina [µU/ml]

164.03 4.05 0.20

159.71 3.60 0.30

527.22 15.00 7.60

2.65 1.73 10.80 5.70 9.05 72.00 21.02 14.60 55.50

40


41


control group in the first 48 hours of life. Interven-tricular septum (IVS) diameter was significantly hi-gher (p < 0.01) in diabetic, especially in G-2 group, than in control newborns (Figure 3). In the group of neonates born to diabetic mothers, in 17 out of 44 evaluated cases, the enlargement of the ventricular septum was noticed. In 15 out of 17 cases, asymme-trical septal hypertrophy was observed, and in two cases symmetrical hypertrophy was noticed. Thick-ness of the ventricular septum was found in the nor-mal range in all newborns from the control group.

During the study the ratio of the ventricular septum thickness to the left ventricular posterior wall thickness in diastole (IVSd/LVPW) was calculated. In the control group the ratio of IVSd/LVPW was 1.03 ± 0.14, while in newborns of diabetic mothers the ratio was significantly (p < 0.001) higher 1.32 ± 0.52. The highest ratio of IVS/LVPW was found in the G-2 group (Figure 4). The Analysis of

IVS: ANOVA Kruskal-Wallis H(3, n = 70) = 8.76, p = 0.03;F(3.66) = 3.82, p = 0.01(a)"t(43) = −3.41, p = 0.001; UMW = 120 (Z = −2.92), p = 0.004(b)"t(42) = −1.78, p = 0.08; heteroscedasticity41 1 F = 7.99, p = 0.0001; Levene (31) = 15.49, p = 0.0004; Brown-Forsyth(31) = 9.83, p = 0.00441 2 F = 4.47 p = 0.01 Levene (23) = 6.35, p = 0.02;41 3 F = 4.71, p = 0.001; Levene (24) = 7.04, p = 0.01; Brown-Forsyth(24) = 4.25, p = 0.05

Fig. 3. Comparison of the IVS [mm] diameter between the analyzed groupsRyc. 3. Porównanie średniego wymiaru IVS [mm] w analizowanych grupach

variance indicates significant differences of the ratio of IVSd/LVPW between all groups.

The results of echocardiographic evaluation performed after 12 months of age are presented in Table 3. In contrast to on early postnatal period, the IVS thickness in diabetic group did not differ significantly at that time, in comparison to control subjects. Furthermore, during one–year observation the ratio of IVS/LVPW significantly decreased for about 0.17 and reached normal values of – 1.13 in comparison to neonatal period.

Discussion

The risk of congenital anomalies is increased in in-fants of diabetic mothers with an over-representation of congenital heart defects. Cardiac abnormalities occur in approximately 2.5% – 4.0% of babies born to mothers with insulin-dependent pregestational

40


41


diabetes mellitus [18, 19]. That fact was also con-firmed in our study, although most of IDM were born to GDM mothers. It may prove the some cases of GDM were recognized too late. Ventricular and atrial septal defect were the most frequent cardiac anomalies recognized in our neonates.

Most of the examined infants born to diabetic mothers were not large for gestational age. Thesefindings suggest that their mothers were probably well controlled during pregnancy and their infants did not experience maternal hyperglycemia or fe-tal hyperinsulinemia late in gestation. On the other hand, cord blood hyperinsulinemia, especially in neonates born to insulin treated mothers (PGDM and G-2 group), was detected during our study. It is a generally accepted opinion that newborns of dia-betic mothers are at high risk of hypoglycemia due to transient hyperinsulinemia in a few days after de-livery [18]. However, despite increasing levels of cord blood insulin, hypoglycemia in the examined neonates was not detected.

Infants of diabetic mothers are ata high risk of developing hypertrophic cardiomyopathy. The hy-pertrophy occurs primarily in the interventricu-lar septum but can affect any portion of the ven-tricular walls [7, 8]. Features of IVS hypertrophywere found in 17 out of 44 examined by us neona-tes born to diabetic mothers. Most of the neonateswith HCM were born by GDM mothers, especial-ly from G-2 group. Newborns from the last group had significantly higher IVS diameters and valu-es of IVS/LVPW ratio compare to control subjects. These findings indicate that unrecognized mater-nal diabetes onset before 24–28 weeks of pregnan-cy (time of OGTT) may be responsible for develo-ping HCM. Furthermore our findings indicate that good metabolic control of gestational diabetes from recognition until delivery is not sufficient to norma-lize some cardiac diameter size, e.g. IVS enlarge-ment. Next few months out of maternal hyperglyce-mic environment are reguired to achieve there solu-tion of HCM feature.

IVS/LVPW: ANOVA Kruskal-Wallis H(3, n = 68) = 10.27, p = 0.02;(a)"UMW = 96.5 (Z = −3.28), p = 0.001(b)"UMW = 97.5 (Z = −1.83), p = 0.07;

Fig. 4. The Comparison of the IVS/LVPW ratio between the analyzed groupsRyc. 4. Porównanie stosunku przegrody międzykomorowej do tylnej ściany lewej komory w analizowanych grupach

42


43


Waldman and co-workers [1] described that HCM is the most common cardiac abnormality seen in IDM. This is thought to be related to high insu-lin levels in the fetus, an increased number of insu-lin receptors in the fetal heart, and increased pro-tein and fat synthesis resulting in myocardial cell hyperplasia and hypertrophy as well as glycogen deposition [6, 8]. Cooper et al. [20] found a strict correlation between the appearance and degree of HCM with metabolic control during the third tri-mester. Conversedy, Rizzo et al. [13] found an ac-celerated increase in the cardiac size in fetuses of diabetic mothers, in spite of a careful metabolic control. We did not detect any significant correlation between cord blood fructosamine level, IVSd dia-meter, LVPW diameter and IVS/LVPW ratio either. Also, We did not found any significant correlation between cord blood insulin levels, and IVSd diame-ter, LVPW diameter as well as IVS/LVPW ratio. On the other hand, the observed levels of fructosami-ne and the lack of hypoglycemia in the examined newborns allows to assume that maternal diabetes was well controlled during the last days before deli-very. However, cord blood insulin levels in exami-ned IDM were increased, especially in PGDM and G-2 groups. In the last group a positive correlation between cord blood insulin and LAD, and between LADd blood flow through MV and abdominal aorta was found. Furthermore, all but LADd relationship were statistically significant. That allows assuming that hyperinsulinemia may lead to the enlargement of left heart size and function. Waldman [1] repor-ted that in IDM with HCM, Doppler may show high velocity from the left ventricle into the aorta and co-lour flow Doppler often reveals turbulence.

According to the data described by Waldman [1],left ventricular shortening fraction may be normal or increased in infants with HCM. A tendency to a positive correlation between SF% and cord blo-od fructosamine and insulin levels in neonates from G-2 group was observed in our study. However, the values of correlation coefficient have not reached si-gnificant levels. It is not possible to compare our re-sults with other authors’ findings because up to now such relationship has not been analyzed.

In our study, the ratio of IVSd/LVPW evaluated in neonates born to diabetic mothers during the first

48 hours was found to be significantly higher, espe-cially in G-2 group, in comparison to control sub-jects. As it is described in literature, macrosomic infants of diabetic mothers may face circulatory fa-ilure due to hypertrophic cardiomyopathy. Howe-ver, the observed HCM was generally mild and did not affect cardiac function.

The significant difference of the IVSd/LVPW ratio between diabetic and control patients detec-ted at birth was not demonstrated after 12 months of age. This means that features of HCM disappe-ared without any treatment during the first months of life. Our results confirmed findings concerning infants born to insulin-dependent diabetes mothers by Akcoral et al. [5], and Waldman et al. [1]. It is generally believed that PGDM is a main risk factor for developing fetal macrosomia and hypertrophic cardiomyopathy [6, 7, 20, 21]. Our results show ho-wever that the highest risk for both these abnormali-ties is present in neonates born to mothers with dia-betes first recognized during pregnancy, especially type G-2.

According to the excess of frequency of gesta-tional diabetes [22, 23], diabetes-related obstetrical complications as well as problems in IDM will in-crease in next generations.

Conclusions

1. Infants born to mothers with diabetes first recognized during pregnancy and treated with insulin (G-2) are at a high risk of developing hypetrophic cardiomyopathy.

2. Cord blood insulin and fructosamine levels present no significant association with IVS and IVS/LVPW ratio in infants of diabetic mothers.

3. Fetal hyperinsulinemia may lead to the increased left heart diastolic diameter and to the increased blood flow through mitral valve, and abdominal aorta in neonates born to gestational diabetic mothers treated with insulin.

4. Resolution to normality of echocardiographic findings noticed in the newborns born to diabetic mothers (HCM) was confirmed during 12-month echocardiography observation.

42


43


[1] Waldman D.J., Plowden J., Clericuzio C. In: Skinner J., Alverson D., Hunter S., (editors) Echocardiography for the neonatologist. Edinburgh, Churchill Livingstone 2000; 225-237.

[2] Ferencz C., Neil C.A.: Cardiomyopathy in infancy: observations In an epidemiologic study. Pediatr. Cardiol., 1992:3, 65-71.[3] Schwartz R., Teramo K.A.: Effects of diabetic pregnancy on the fetus and newborn. Semin. Perinatol, 2000:24, 120-135.[4] Ullmo S., Vial Y., Di Bernardo S. et al.: Pathologic ventricular hypertrophy in the offspring of diabetic mothers: a retrospective study.

Eur. Heart. J., 2007:28(11), 1319-1325.[5] Akcoral A., Oran B., Tavli V. et al.: Transient right hypertrophic cardiomyopathy in an infant born to a diabetic mother. Indian. J. Pe-

diatr., 1996:63, 700-703.[6] Reller M.D., Tsang R.C., Meyer R.A., Braun C.P.: Relationship of prospective diabetes control in pregnancy to neonatal cardiorespira-

tory function. J. Pediatr., 1985:106, 86-90.[7] Sheehan P.Q., Rowland T.W., Shah B.L. et al.: Maternal diabetic control and hypertrophic cardiomyopathy in infants of diabetic moth-

ers. Clin. Pediatr., 1986:25, 266-271.[8] Weber H.S., Botti J.J., Baylen B.G.: Sequential longitudinal evaluation of cardiac growth and ventricular diastolic filling in fetuses of

well controlled diabetic mothers. Pediatr. Cardiol., 1994:15, 184-189.[9] American Diabetes Association. Preconception Care of Women with Diabetes Diabetes Care, vol. 27 supp. 1, January 2004.[10] Penney G.C., Mair G., Pearson D.W.: Scottish diabetes in pregnancy group. Outcomes of pregnancy in women with type I diabetes

in Scotland: a national population – based study. BJOG, 2003:110, 315-318.[11] Leipold H., Worda C., Schwindt J. et al.: Severe diabetic fetopathy despite strict metabolic control. Wien. Klin. Wochenschr., 2005:

117, 561-564.[12] Jensen D.M., Damm P., Moelsted-Pedersen L. et al.: Outcomes in type 1 diabetic pregnancies. Diabetes. Care., 2004:27, 2819-

2823. [13] Rizzo G., Arduini D., Romanini C.: Accelerated cardiac growth and abnormal cardiac flow in fetuses of type 1 diabetic mothers. Ob-

stet Gynecol, 1992:80, 369-376.[14] Skinner J.: Normal Doppler ultrasound measurements in the newborn. In: Echocardiography for the neonatologist. Skinner J., Alver-

son D., Hunter S., (editors): Edinburgh, Churchill Livingstone 2000, 73-86.[15] Madar J., Hunter S., Skinner J.: Obtaining the standard echocardiographic views. In: Skinner J, Alverson D, Hunter S, editors.

Echocardiography for the neonatologist. Edinburgh, Churchill Livingstone 2000, 39-50.[16] Madar J.: M-mode echocardiography. In: Skinner J., Alverson D., Hunter S. (editors). Echocardiography for the neonatologist. Edin-

burgh, Churchill Livingstone 2000, 51-57.[17] Wyllie J.P.: Ventricular function. In: Skinner J., Alverson D., Hunter S. (editors). Echocardiography for the neonatologist. Edinburgh,

Churchill Livingstone 2000, 113-120.[18] Wu P.Y. Infant of diabetic mother: a continuing challenge for perinatal-neonatal medicine. Chung Hua Min Kuo Hsiao Erh Ko Ihsueh

Hui Tsa Chin, 1996; 37(5):312-319.[19] Loffredo C., Wilson P.D., Ferencz C.: Maternal diabetes: An independent risk factor for major cardiovascular malformation with

increased mortality of affected infants. Teratology, 2001:64, 98-106. [20] Cooper M.J., Enderlein M.A., Tarnoff H., Roge C.L.: Asymmetric septal hypertrophy in infants of diabetic mothers. Am. J. Dis. Child.,

1992:146, 226-229.[21] Franzese A., Valerio G., Ciccarelli N.P. et al.: Severe hypertrophic cardiomyopathy in an infant of a diabetic mother. Diabetes Care,

1997:20, 676-677.[22] McLean M., Chipps D., Wah Cheung N.: Mother to child transmission of diabetes mellitus: does gestational diabetes program Type

2 diabetes in the next generation? Diabet. Med., 2006:23, 1213-1215.[23] Feig D.S., Razzaq A., Sykora K. et al.: Trends in Deliveries, Prenatal Care, and Obstetrical Complications in Women with Pregestatio-

nal Diabetes. Diabetes Care, vol. 29, No 2, Feb 2006.

PIŚMIENNICTWO/REFERENCES

endokrynologia pediatryczna pediatric endocrinology · 2015. 2. 26. · rodki matek chorujących na...

Documents