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Pulmonary vein pulsatility in fetuses of diabetic mothers: prenatal Doppler echocardiographic study

Abstracts

OBJECTIVE: To verify the hypothesis that the pulmonary vein pulsatility index is higher in fetuses of diabetic mothers than it is in normal fetuses of nondiabetic mothers. METHODS: Twenty-four fetuses of mothers with either gestational or previous diabetes (cases), and 25 normal fetuses of mothers without systemic disease (control) were examined. Fetuses were examined through prenatal Doppler and color flow mapping. The pulmonary vein pulsatility index was obtained by placing the pulsed Doppler sample volume over the right superior pulmonary vein and applying the formula (systolic velocity - presystolic velocity)/mean velocity. RESULTS: The mean gestational age of the study fetuses was 30.3±2.7 weeks, and gestational age of the controls was 29±3.3 weeks, with no significant difference in gestational age between groups (p=0.14). Fetuses of diabetic mothers had a mean pulmonary vein pulsatility index of 1.6±1, and those of the control group had an index of 0.86±0.27. CONCLUSION: Fetuses of diabetic mothers had pulmonary vein pulsatility indexes (parameter easily obtained through Doppler echocardiography that may be related to fetal diastolic function) higher than those in fetuses of mothers with normal glycemia.

fetal echocardiography; fetal diastolic function; fetal pulmonary venous flow; diabetes; pulmonary vein pulsatility index


OBJETIVO: Testar a hipótese de que o índice de pulsatilidade da veia pulmonar é maior em fetos de mães diabéticas do que em fetos normais. MÉTODOS: Examinados 24 fetos de mães com diabetes prévio ou gestacional (casos) e 25 fetos normais de mães sem doença sistêmica (controles). Os fetos foram examinados pela ecocardiografia pré-natal com Doppler e mapeamento de fluxo em cores. O índice de pulsatilidade da veia pulmonar foi obtido colocando-se a amostra volume do Doppler pulsado sobre a veia pulmonar superior direita e aplicando-se a fórmula (velocidade sistólica-velocidade pré-sistólica)/velocidade média. RESULTADOS: Os casos apresentaram idade gestacional média de 30,3 ± 2,7 semanas, e os controles, de 29, ± 3,3 semanas, sem diferença significativa entre as idades gestacionais nos dois grupos (p = 0,14). Os fetos de mães diabéticas apresentaram índice de pulsatilidade da veia pulmonar médio de 1,6 ± 1 e os fetos do grupo controle 0,86 ± 0,27. CONCLUSÃO: Fetos de mães diabéticas apresentam índice de pulsatilidade da veia pulmonar (parâmetro Doppler-ecocardiográfico de fácil obtenção, que pode estar relacionado com a função diastólica fetal) maior do que os de mães com glicemia normal.

ecocardiografia fetal; função diastólica fetal; fluxo venoso pulmonar fetal; diabetes; índice de pulsatilidade da veia pulmonar


ORIGINAL ARTICLE

Pulmonary vein pulsatility in fetuses of diabetic mothers. Prenatal Doppler echocardiographic study

Paulo Zielinsky; Antonio L. Piccoli Jr; Lucas Teixeira; Eduardo I. Gus; João L. Mânica; Fabíola Satler; Humberto Vaz; Luiz H. Nicoloso; Stelamaris Luchese; Marlui Sheid; Silvana Marcantonio; Domingos Hatém

Instituto de Cardiologia do Rio Grande do Sul - Fundação Universitária de Cardiologia. Porto Alegre, RS - Brazil

Correspondence Correspondence to Paulo Zielinsky Unidade de Cardiologia Fetal do IC/FUC Av. Princesa Isabel, 395 Cep 90620-001 - Porto Alegre, RS E-mail: zielinsky@cardiol.br / pesquisa@cardnet.tche.br

ABSTRACT

OBJECTIVE: To verify the hypothesis that the pulmonary vein pulsatility index is higher in fetuses of diabetic mothers than it is in normal fetuses of nondiabetic mothers.

METHODS: Twenty-four fetuses of mothers with either gestational or previous diabetes (cases), and 25 normal fetuses of mothers without systemic disease (control) were examined. Fetuses were examined through prenatal Doppler and color flow mapping. The pulmonary vein pulsatility index was obtained by placing the pulsed Doppler sample volume over the right superior pulmonary vein and applying the formula (systolic velocity - presystolic velocity)/mean velocity.

RESULTS: The mean gestational age of the study fetuses was 30.3±2.7 weeks, and gestational age of the controls was 29±3.3 weeks, with no significant difference in gestational age between groups (p=0.14). Fetuses of diabetic mothers had a mean pulmonary vein pulsatility index of 1.6±1, and those of the control group had an index of 0.86±0.27.

CONCLUSION: Fetuses of diabetic mothers had pulmonary vein pulsatility indexes (parameter easily obtained through Doppler echocardiography that may be related to fetal diastolic function) higher than those in fetuses of mothers with normal glycemia.

Key words: fetal echocardiography, fetal diastolic function, fetal pulmonary venous flow, diabetes, pulmonary vein pulsatility index

The incidence of insulin-dependent diabetes mellitus is about 0.8%, and gestational diabetes is 3-5%. Both are evidence of the metabolic disturbances of carbohydrates during pregnancy1. The incidence of congenital malformation is 3 to 4 times greater in children from diabetic mothers than in the general population 2. Among those malformations, 50% are congenital cardiac diseases 3. Maternal diabetes is a risk factor for congenital heart disease and an indication for fetal echocardiography4-12.

Maternal hyperglycemia and the excess of glucose transferred to the fetus encourage fetal pancreatic islets to increase the production of insulin, leading to hyperinsulinism, which is responsible for fetal complications. Fetal myocardial hypertrophy is the most frequent abnormality found in newborns from diabetic mothers, and it may be found in up to 35% of these newborns 13. The interventricular septum is particularly rich in insulin receptors 14, which would justify increased hypertrophy in this segment, secondary to myocardial cell hyperplasia and hypertrophy due to the increased synthesis of fat and proteins.

Fetal Doppler echocardiography has increased our knowledge about the cardiocirculatory changes in the prenatal period. Recent studies have shown significant changes in the cardiovascular flow of fetuses from diabetic mothers, especially in pregnancies with inadequate glycemic control 15.

With the introduction of echocardiography, several clinical studies have demonstrated normal patterns of pulmonary venous flow in children and adults through transesophageal and transthoracic echocardiography 16,17. The use of the pulmonary vein pulsatility index as a parameter for diastolic function evaluation during fetal life has not yet been reported. Thus, we have tested the hypothesis that the pulmonary vein pulsatility index in fetuses from diabetic mothers is greater than that in fetuses from nondiabetic mothers, based on the idea that a less complacent left ventricle would increase presystolic flow impedance in the pulmonary vein, corresponding to the atrial contraction phases. Consequently, it would increase the pulsatility index in this vessel.

Methods

Pregnant women with a gestational age between 25 weeks to term were selected and sent to the Unidade de Cardiologia Fetal - Instituto de Cardiologia do RS/Fundação Universitária de Cardiologia (Fetal Cardiology Unit - Cardiology Institute of RS/University Foundation of Cardiology) by several obstetric centers in the city.

Twenty-four fetuses with a gestational age between 25 weeks to term whose mothers had previous or gestational diabetes were examined. The control group was formed by 25 normal fetuses between 25 weeks to term, whose mothers did not have diabetes, also examined sequentially. Fetuses were included in the study when the images obtained were of adequate quality and when cardiac abnormalites apart from septal hypertrophy were excluded.

Fetuses with a gestational age less than 25 weeks, with any other congenital malformation, or those whose mother had a systemic disease other than diabetes mellitus were excluded.

The diagnosis of gestational diabetes was made based on the principles proposed by O'Sullivan and Mahan 18.

The equipment used was an Acuson ASPEN echocardiography system with a convex transducer 4 to 7MHz or a 2.25 to 4MHz phased array transducer, with the capacity to perform bidimensional imaging, M-mode, Doppler and color mapping. Fetal echocardiographic examinations were comprehensive, following the segmental sequential approach 19, starting in the maternal umbilical region and searching as anatomical referentials the dorsal spine, the liver, and the fetal septum primum. Determination of the atrial situs, the position of the heart in the thorax, the type and mode of atrioventricular and ventriculoarterial connections, the aortic arch, and any associated defects was then performed. Flow analysis was performed with pulsed Doppler and color flow mapping, considering that the pulmonary vein flow has systolic, diastolic, and presystolic phases. The pulmonary vein pulsatility index was obtained by placing the pulsed Doppler sample volume over the right superior pulmonary vein (fig. 1), as near as possible to its junction with the left atrium, applying the formula (systolic velocity - presystolic velocity)/mean velocity. To obtain adequate flow velocity curves, 0-2m/s scales and 50 to 100MHZ filters were used. The measures performed in fetal apnea and those corresponding to the average of 3 assessments were considered. All fetal echocardiograms were recorded on magnetic tape.


Data were compared with the 2-tailed Student t test for independent variables. The statistical significance level was established as 0.05.

Results

Mean gestational age of the study fetuses was 30.3 ±2.7 weeks, and of the controls was 29±3.3 weeks. The difference between gestational ages in the 2 groups was not significant, with p=0.14. Mean septal thickening in the study fetuses was 3.6±1mm, and in the control group it was 2.38±0.83mm. In the study fetuses, mean systolic, diastolic, and presystolic velocities were, respectively, 0.29±0.07m/s, 0.21±0.07m/s, and -0.02±0.12m/s, whereas in the controls they were, respectively, 0.27±0.05m/s (NS), 0.22±0.05m/s (NS), and 0.10±0.03m/s (P=0.001). The mean pulmonary vein pulsatility index in the fetuses of diabetic mothers was 1.6±1 (fig. 2) and in the controls, it was 0.86 ± 0.27 (fig. 3) with a significant difference (p=0.001) (fig. 4).




Discussion

The classical approach to the study of ventricular filling function in the fetus is the analysis of atrioventricular flow velocities. We are proposing an alternative method to evaluate fetal diastolic function.

Keren et al 20 suggested that pulmonary venous flow is influenced by dynamic changes in left atrial pressure created by contraction and relaxation of the atrium and ventricle. The pulmonary vein flow pattern is mainly determined by the events that occur in the left side of the heart 20. Pulmonary venous flow patterns in fetuses and newborns have been studied. Hong and Choi 21 reported that pulmonary venous flow was continuous from the pulmonary vein to the left atrium in all cardiac cycles and had biphasic peaks: one during systole and the other during diastole. Fetuses have a pulmonary vein pattern similar to that described in the postnatal period, apart from the absence of reverse atrial flow. As the lungs are collapsed in the fetus, the flow is reduced and, additionally, lower velocities may reflect the decreased pulmonary flow volume. Hong and Choi 22 verified that the pattern of pulmonary vein flow in fetuses results from the low pulmonary flow and the reduced capacity of the pulmonary system. The pattern of the pulmonary venous waveform was also described by Laudy et al 23, and reinforces that it has a biphasic flow profile with a systolic and a diastolic component. The nature of the fetal pulmonary venous flow waveform pattern suggests positive pressures towards the left atrium thorough the cardiac cycle.

The pattern of pulmonary venous flow velocity, may be altered in many physiologic and pathologic situations, such as heart rate 24, cardiac output 25, absolute pulmonary flow 26, left atrial pressure 22 and function, mitral valve function, left ventricle pressure and function 22. Talbert and Johnson 27 suggested that the change of shape of the pulmonary venous flow waveform reflects the changes in the pressure waveform of the left atrium and represent the atrial pressure response to both intracardiac and systemic vascular status.

The present study has demonstrated that fetuses from diabetic mothers have a higher pulmonary vein pulsatility index than fetuses from mothers with normal glycemia. It is suggested that this alteration is due to the involvement of fetal diastolic function secondary to previous or gestational maternal diabetes, with left ventricular hypertrophy, and an increase in muscle mass and a consequent decrease in ventricular compliance. The increase in left atrial pressure leads to a restriction of pulmonary venous emptying, resulting in a decrease in presystolic velocity in pulmonary vein or reverse flow in presystole. The marker of this retrograde transmission of pressure would be the increase in pulmonary vein pulsatility index, because this index reflects the correlation between systolic and presystolic velocities, and the mean pulmonary venous flow velocity.

The pulmonary vein pulsatility index is an easily obtained echocardiographic Doppler parameter, which may add information about fetal circulatory dynamics in fetuses from diabetic mothers.

Received for publication: 11/19/02

Accepted for publication 4/29/03

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  • Correspondence to
    Paulo Zielinsky
    Unidade de Cardiologia Fetal do IC/FUC
    Av. Princesa Isabel, 395
    Cep 90620-001 - Porto Alegre, RS
    E-mail:
  • Publication Dates

    • Publication in this collection
      10 Feb 2004
    • Date of issue
      Dec 2003

    History

    • Received
      19 Nov 2002
    • Accepted
      29 Apr 2003
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