Download PDF
Ultraschall Med 2023; 44(02): e99-e107
DOI: 10.1055/a-1499-7265
Review

Third Trimester Myocardial Performance Index in Fetuses from Women with Hyperglycemia in Pregnancy: A Systematic Review and Meta-Analysis

Fetaler myokardialer Performance-Index im dritten Trimester bei Schwangeren mit Hyperglykämie: Systematische Übersicht und Metaanalyse
Angelo Sirico 
1   Obstetrics and High-Risk Pregnancy Unit, Fondazione Policlinico A. Gemelli IRCCS, Rome, Italy
2   Gynecology and Obstetrics Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, School of Medicine, University of Naples Federico II, Naples, Italy
,
Antonio Raffone 
2   Gynecology and Obstetrics Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, School of Medicine, University of Naples Federico II, Naples, Italy
,
Giuseppe Maria Maruotti
2   Gynecology and Obstetrics Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, School of Medicine, University of Naples Federico II, Naples, Italy
,
Antonio Travaglino
3   Anatomic Pathology Unit, Department of Advanced Biomedical Sciences, School of Medicine, University of Naples Federico II, Naples, Italy
,
Carmela Paciullo
1   Obstetrics and High-Risk Pregnancy Unit, Fondazione Policlinico A. Gemelli IRCCS, Rome, Italy
,
Alice Diterlizzi
1   Obstetrics and High-Risk Pregnancy Unit, Fondazione Policlinico A. Gemelli IRCCS, Rome, Italy
,
Antonio Mollo
4   Gynecology and Obstetrics Unit, Department of Medicine, Surgery and Dentistry “Schola Medica Salernitana”, University of Salerno, 84081 Baronissi, Italy
,
Giuseppe Rizzo
5   Division of Maternal and Fetal Medicine, Ospedale Cristo Re - University of Rome Tor Vergata, Rome, Italy
6   Department of Obstetrics and Gynecology The First I.M. Sechenov Moscow State Medical University
,
Fulvio Zullo
2   Gynecology and Obstetrics Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, School of Medicine, University of Naples Federico II, Naples, Italy
,
Antonio Lanzone
1   Obstetrics and High-Risk Pregnancy Unit, Fondazione Policlinico A. Gemelli IRCCS, Rome, Italy
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

Introduction The myocardial performance index (MPI) has been proposed to evaluate cardiac dysfunction in newborns from diabetic mothers. Although MPI is routinely assessed in newborns, its role in the evaluation of fetuses from women with hyperglycemia in pregnancy (HIP) is still under evaluation. We aimed to evaluate the differences in third trimester fetal MPI in pregnant women with hyperglycemia compared to healthy controls.

Materials and Methods Seven electronic databases were searched for all studies assessing women with HIP who underwent evaluation of fetal left MPI during pregnancy compared to a control group. The summary measures were reported as mean differences (MD) in the mean fetal left MPI between women with HIP and healthy controls, with a 95 % confidence interval (CI). A post hoc subgroup analysis based on the type of HIP – pregestational diabetes, GDM, or gestational impaired glucose tolerance (GIGT) – was performed as an additional analysis.

Results 14 studies assessing 1326 fetuses (580 from women with HIP and 746 from controls) were included. Women with HIP had a significantly higher mean left fetal MPI compared to controls (MD 0.08; 95 %CI: 0.05 to 0.11; p < 0.00 001). Subgroup analysis according to the type of HIP concurred with the overall analysis for women with DM (MD 0.07; 95 %CI: 0.01 to 0.13; p = 0.02) and for women with GDM (MD 0.012; 95 %CI: 0.07 to 0.17; p < 0.00 001) but not for women with GIGT (MD –0.01, 95 % CI –0.28 to 0.27; p = 0.96).

Conclusion Fetal left MPI is increased in pregnancies with HIP appearing as a potential marker of cardiac dysfunction.

Zusammenfassung

Ziel Der myokardiale Performance-Index (MPI) wurde vorgeschlagen, um die kardiale Dysfunktion bei Neugeborenen von Müttern mit Diabetes zu beurteilen. Obwohl der MPI routinemäßig bei Neugeborenen bestimmt wird, ist seine Rolle bei der Beurteilung von Föten von Schwangeren mit Hyperglykämie (HIP) noch in der Evaluierung. Unser Ziel war es, die Unterschiede im fetalen MPI im dritten Trimester bei schwangeren Frauen mit Hyperglykämie im Vergleich zu gesunden Kontrollen zu bewerten.

Material und Methoden Sieben elektronische Datenbanken wurden nach allen Studien durchsucht, in denen Frauen mit HIP untersucht wurden, bei denen während der Schwangerschaft eine Bewertung des fetalen linken MPI im Vergleich zu einer Kontrollgruppe durchgeführt wurde. Die zusammenfassenden Messungen wurden als mittlere Differenzen (MD) des mittleren fetalen linken MPI zwischen Frauen mit HIP und gesunden Kontrollen mit einem 95 %-Konfidenzintervall (KI) angegeben. Eine Post-hoc-Subgruppenanalyse basierend auf dem HIP-Typ – präkonzeptioneller Diabetes, Gestationsdiabetes mellitus (GDM) oder Gestations-bedingte Glukosetoleranzstörung (GIGT) – wurde als zusätzliche Analyse durchgeführt.

Ergebnisse 14 Studien mit 1326 Föten (580 von Frauen mit HIP und 746 von Kontrollpersonen) wurden eingeschlossen. Frauen mit HIP hatten einen signifikant höheren mittleren linken fetalen MPI im Vergleich zu den Kontrollen (MD 0,08; 95 %-KI 0,05–0,11; p < 0,00 001). Die Subgruppenanalyse nach dem HIP-Typ stimmte mit der Gesamtanalyse für Frauen mit DM (MD 0,07; 95 %-KI 0,01–0,13; p = 0,02) und für Frauen mit GDM (MD 0,012; 95 %-KI 0,07–0,17; p < 0,00 001) überein, nicht aber für Frauen mit GIGT (MD –0,01; 95 %-KI –0,28–0,27; p = 0,96).

Schlussfolgerung Der fetale linke MPI ist bei Schwangerschaften mit HIP erhöht und könnte sich somit als potenzieller Marker für die kardiale Dysfunktion erweisen.

Key words

hyperglycemia - pregnancy - fetal ultrasound - fetus - echocardiography

Supplement



Publication History

Received: 22 October 2020

Accepted: 09 April 2021

Article published online:
23 August 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 McIntyre HD, Metzger BE, Coustan DR. et al Counterpoint: Establishing consensus in the diagnosis of GDM following the HAPO study. Curr Diab Rep 2014; 14: 497
    CrossrefPubMedGoogle Scholar
  • 2 International Association of Diabetes and Pregnancy Study Groups Consensus Panel. International Association of Diabetes and Pregnancy Study Groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 2010; 33: 676-682
    CrossrefPubMedGoogle Scholar
  • 3 McIntyre D, Desoye G, Dunne F. et al FIGO analysis of research priorities in hyperglycemia in pregnancy. Diabetes Res Clin Pract 2018; 145: 5-14 DOI: 10.1016/j.diabres.2018.03.026.
    CrossrefPubMedGoogle Scholar
  • 4 Mitanchez D, Yzydorczyk C, Siddeek B. et al The offspring of the diabetic mother – short- and long-term implications. Best Pract Res Clin Obstet Gynaecol 2015; 29: 256-269
    CrossrefPubMedGoogle Scholar
  • 5 Barker DJ, Eriksson JG, Fors'en T. et al Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 2002; 31: 235-239
    CrossrefPubMedGoogle Scholar
  • 6 Agarwal P, Morriseau TS, Kereliuk SM. et al Maternal obesity, diabetes during pregnancy and epigenetic mechanisms that influence the developmental origins of cardiometabolic disease in the offspring. Crit Rev Clin Lab Sci 2018; 55: 71-101 DOI: 10.1080/10408363.2017.1422109.
    CrossrefPubMedGoogle Scholar
  • 7 Corrigan N, Brazil DP, McAuliffe F. Fetal cardiac effects of maternal hyperglycemia during pregnancy. Birth Defects Res A Clin Mol Teratol 2009; 85: 523-530
    CrossrefPubMedGoogle Scholar
  • 8 Rizzo G, Arduini D, Capponi A. et al Cardiac and venous blood flow in fetuses of insulin-dependent diabetic mothers: evidence of abnormal hemodynamics in early gestation. Am J Obstet Gynecol 1995; 173: 1775-1781
    CrossrefPubMedGoogle Scholar
  • 9 Pauliks LB. The effect of pregestational diabetes on fetal heart function. Expert Rev Cardiovasc Ther 2015; 13: 67-74 DOI: 10.1586/14779072.2015.988141.
    CrossrefPubMedGoogle Scholar
  • 10 Dervisoglu P, Kosecik M, Kumbasar S. Effects of gestational and pregestational diabetes mellitus on the foetal heart: a cross-sectional study. J Obstet Gynaecol 2018; 38: 408-412 DOI: 10.1080/01443615.2017.1410536.
    CrossrefPubMedGoogle Scholar
  • 11 Garcia-Flores J, Jañez M, Gonzalez MC. et al Fetal myocardial morphological and functional changes associated with well-controlled gestational diabetes. Eur J Obstet Gynecol Reprod Biol 2011; 154: 24-26 DOI: 10.1016/j.ejogrb.2010.08.002.
    CrossrefPubMedGoogle Scholar
  • 12 Tei C, Ling LH, Hodge DO. et al New index of combined systolic and diastolic myocardial performance: A simple and reproducible measure of cardiac function – a study in normal and dilated cardiomyopathy. J Cardiol 1995; 26: 357-366
    PubMedGoogle Scholar
  • 13 Tei C, Dujardin KS, Hodge DO. et al Doppler index combining systolic and diastolic myocardial performance: clinical value in cardiac amyloidosis. J Am Coll Cardiol 1996; 28: 658-664 DOI: 10.1016/0735-1097(96)00202-1. . PMID: 8772753
    CrossrefPubMedGoogle Scholar
  • 14 Tsutsumi T, Ishii M, Eto G. et al Serial evaluation for myocardial performance in fetuses and neonates using a new Doppler index. Pediatr Int 1999; 41: 722-727
    CrossrefPubMedGoogle Scholar
  • 15 Hernandez-Andrade E, López-Tenorio J, Figueroa-Diesel H. et al A modified myocardial performance (Tei) index based on the use of valve clicks improves reproducibility of fetal left cardiac function assessment. Ultrasound Obstet Gynecol 2005; 26: 227-232 DOI: 10.1002/uog.1959. . PMID: 16116562
    CrossrefPubMedGoogle Scholar
  • 16 Hernandez-Andrade E, Figueroa-Diesel H, Kottman C. et al Gestational-age-adjusted reference values for the modified myocardial performance index for evaluation of fetal left cardiac function. Ultrasound Obstet Gynecol 2007; 29: 321-325 DOI: 10.1002/uog.3947. . PMID: 17290412
    CrossrefPubMedGoogle Scholar
  • 17 Moher D, Liberati A, Tetzlaff J. et al Preferred reporting items for syste matic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62: 1006-1012
    CrossrefPubMedGoogle Scholar
  • 18 Slim K, Nini E, Forestier D. et al Methodological index for non-randomized studies (MINORS). Development and validation of a new instrument. ANZ J Surg 2003; 73: 712-716
    CrossrefPubMedGoogle Scholar
  • 19 Moher D, Liberati A, Tetzlaff J. et al Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62: 1006-1012
    CrossrefPubMedGoogle Scholar
  • 20 Diagnostic criteria and classification of hyperglycaemia first detected in pregnancy: a World Health Organization Guideline. Diabetes Res Clin Pract 2014; 103: 341-363 DOI: 10.1016/j.diabres.2013.10.012. . PMID: 24847517
    CrossrefPubMedGoogle Scholar
  • 21 Wong ML, Wong WH, Cheung YF. Fetal myocardial performance in pregnancies complicated by gestational impaired glucose tolerance. Ultrasound Obstet Gynecol 2007; 29: 395-400 DOI: 10.1002/uog.3957.
    CrossrefPubMedGoogle Scholar
  • 22 Russell NE, Foley M, Kinsley BT. et al Effect of pregestational diabetes mellitus on fetal cardiac function and structure. Am J Obstet Gynecol 2008; 199: 312e1-312e7
    CrossrefPubMedGoogle Scholar
  • 23 Garcia-Flores J, Janez M, Gonzalez MC. et al Fetal myocardial morphological and functional changes associated with well-controlled gestational diabetes. Eur J Obstet Gynecol Reprod Biol 2011; 154: 24-26
    CrossrefPubMedGoogle Scholar
  • 24 Chu C, Gui YH, Ren YY. et al The impacts of maternal gestational diabetes mellitus (GDM) on fetal hearts. Biomed Environ Sci 2012; 25: 15-22
    PubMedGoogle Scholar
  • 25 Figueroa H, Silva MC, Kottmann C. et al Fetal evaluation of the modified-myocardial performance index in pregnancies complicated by diabetes. Prenat Diagn 2012; 32: 943-948 DOI: 10.1002/pd.3937.
    CrossrefPubMedGoogle Scholar
  • 26 Balli S, Pac FA, Ece I. et al Assessment of cardiac functions in fetuses of gestational diabetic mothers. Pediatr Cardiol 2014; 35: 30-37
    CrossrefPubMedGoogle Scholar
  • 27 Bhorat IE, Bagratee JS, Pillay M. et al Use of the myocardial performance index as a prognostic indicator of adverse fetal outcome in poorly controlled gestational diabetic pregnancies. Prenat Diagn 2014; 34: 1301-1306 DOI: 10.1002/pd.4471.
    CrossrefPubMedGoogle Scholar
  • 28 Gonzalez AB, Young L, Doll JA. et al Elevated neonatal insulin-like growth factor I is associated with fetal hypertrophic cardiomyopathy in diabetic women. Am J Obstet Gynecol 2014; 211: 290.e1-290.e7
    CrossrefPubMedGoogle Scholar
  • 29 Pilania R, Sikka P, Rohit MK. et al Fetal Cardiodynamics by Echocardiography in Insulin Dependent Maternal Diabetes and Its Correlation with Pregnancy Outcome. J Clin Diagn Res 2016; 10: QC01-QC04 DOI: 10.7860/JCDR/2016/17993.8079.
    CrossrefPubMedGoogle Scholar
  • 30 Sanhal CY, Daglar HK, Kara O. et al Assessment of fetal myocardial performance index in women with pregestational and gestational diabetes mellitus. J Obstet Gynaecol Res 2017; 43: 65-72 . doi:10.1111/jog.13174
    CrossrefPubMedGoogle Scholar
  • 31 Bhorat I, Pillay M, Reddy T. Determination of the fetal myocardial performance index in women with gestational impaired glucose tolerance and to assess whether this parameter is a possible prognostic indicator of adverse fetal outcome. J Matern Fetal Neonatal Med 2018; 31: 2019-2026 DOI: 10.1080/14767058.2017.1334047.
    CrossrefPubMedGoogle Scholar
  • 32 Moodley S, Arunamata A, Stauffer KJ. et al Maternal arterial stiffness and fetal cardiovascular physiology in diabetic pregnancy. Ultrasound Obstet Gynecol 2018; 52: 654-661 DOI: 10.1002/uog.17528.
    CrossrefPubMedGoogle Scholar
  • 33 Bhorat I, Pillay M, Reddy T. Assessment of the Fetal Myocardial Performance Index in Well-Controlled Gestational Diabetics and to Determine Whether It Is Predictive of Adverse Perinatal Outcome. Pediatr Cardiol 2019; 40: 1460-1467 DOI: 10.1007/s00246-019-02158-4.
    CrossrefPubMedGoogle Scholar
  • 34 Moghadam EA, Zeinaloo A, Danaeian M. et al The diagnosis of early fetal cardiacchanges of the gestational diabetic mothers: Presenting the preload index. Iranian Journal of Pediatrics 2019; 29: e86450 DOI: 10.5812/ijp.86450.
    CrossrefPubMedGoogle Scholar
  • 35 Patey O, Carvalho JS, Thilaganathan B. Perinatal changes in fetal cardiac geometry and function in diabetic pregnancy at term. Ultrasound Obstet Gynecol 2019; 54: 634-642 DOI: 10.1002/uog.20187.
    CrossrefPubMedGoogle Scholar
  • 36 Oncel Alanyali M, Alkan F, Artunc Ulkumen B. et al Use of the modified myocardial performance index for evaluating fetal cardiac functions in pregestational diabetic pregnancy babies. J Obstet Gynaecol 2020; 1-6 DOI: 10.1080/01443615.2020.
    CrossrefPubMedGoogle Scholar
  • 37 Eidelman AI, Samueloff A. The pathophysiology of the fetus of the diabetic mother. Semin Perinatol 2002; 26: 232-236 DOI: 10.1053/sper.2002.34215. . PMID: 12099314
    CrossrefPubMedGoogle Scholar
  • 38 Garcia Carrapato MR. The offspring of gestational diabetes. J Perinat Med 2003; 31: 5-11 . PMID: 12661138 DOI: 10.1515/JPM.2003.001.
    CrossrefPubMedGoogle Scholar
  • 39 Sirico A, Sarno L, Zullo F. et al Pregestational diabetes and fetal heart rate in the first trimester of pregnancy. Eur J Obstet Gynecol Reprod Biol 2019; 232: 30-32 . Epub 2018 Nov 5. PMID: 30465928 DOI: 10.1016/j.ejogrb.2018.11.003.
    CrossrefPubMedGoogle Scholar
  • 40 Sirico A, Lanzone A, Mappa I. et al The role of first trimester fetal heart rate in the prediction of gestational diabetes: A multicenter study. Eur J Obstet Gynecol Reprod Biol 2019; 243: 158-161 DOI: 10.1016/j.ejogrb.2019.10.019. . Epub 2019 Oct 22. PMID: 31706055
    CrossrefPubMedGoogle Scholar
  • 41 Asoglu MR, Gabbay-Benziv R, Turan OM. et al Exposure of the developing heart to diabetic environment and early cardiac assessment: A review. Echocardiography 2018; 35: 244-257 DOI: 10.1111/echo.13811. . Epub 2018 Jan 21. PMID: 29356088
    CrossrefPubMedGoogle Scholar
  • 42 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: 1319-1325 DOI: 10.1093/eurheartj/ehl416. . Epub 2006 Dec 11. PMID: 17158827
    CrossrefPubMedGoogle Scholar
  • 43 Lynch TA, Westen E, Li D. et al Stillbirth in women with diabetes: a retrospective analysis of fetal autopsy reports. J Matern Fetal Neonatal Med 2020; 1-8 DOI: 10.1080/14767058.2020.1779213.
    CrossrefPubMedGoogle Scholar
  • 44 Sirico A, Diemert A, Glosemeyer P. et al Prediction of adverse perinatal outcome by cerebroplacental ratio adjusted for estimated fetal weight. Ultrasound Obstet Gynecol 2018; 51: 381-386 . Epub 2018 Feb 7. PMID: 28294442 DOI: 10.1002/uog.17458.
    CrossrefPubMedGoogle Scholar
  • 45 Vollgraff Heidweiller-Schreurs CA, van Osch IR, Heymans MW. et al Cerebroplacental ratio in predicting adverse perinatal outcome: a meta-analysis of individual participant data. BJOG 2020; DOI: 10.1111/1471-0528.16287. . Epub ahead of print. PMID: 32363701
    CrossrefPubMedGoogle Scholar
  • 46 Gordon EE, Reinking BE, Hu S. et al Maternal Hyperglycemia Directly and Rapidly Induces Cardiac Septal Overgrowth in Fetal Rats. J Diabetes Res 2015; 2015: 479565 . Epub 2015 May 7. PMID: 26064981; PMCID: PMC4439465 DOI: 10.1155/2015/479565.
    CrossrefPubMedGoogle Scholar
  • 47 Maruotti GM, Rizzo G, Sirico A. et al Are there any relationships between umbilical artery Pulsatility Index and macrosomia in fetuses of type I diabetic mothers?. J Matern Fetal Neonatal Med 2014; 27: 1776-1781 . Epub 2014 Feb 3. PMID: 24397275 DOI: 10.3109/14767058.2013.879706.
    CrossrefPubMedGoogle Scholar
  • 48 Rizzo G, Capponi A, Pietrolucci ME. et al First trimester placental volume and three dimensional power doppler ultrasonography in type I diabetic pregnancies. Prenat Diagn 2012; 32: 480-484 DOI: 10.1002/pd.3848. . Epub 2012 Apr 16. PMID: 22504827
    CrossrefPubMedGoogle Scholar
  • 49 Rizzo G, Pietrolucci ME, Mappa L. et al Fetal cardiac remodelling in pregnancies complicated by gestational diabetes mellitus: a prospective cohort study. Prenat Cardiol 2020; DOI: 10.5114/pcard.2020.94558.
    CrossrefPubMedGoogle Scholar
  • 50 Depla AL, de Wit L, Steenhuis TJ. et al Effects of maternal diabetes on fetal heart function at echocardiography: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2020; DOI: 10.1002/uog.22163. . Epub ahead of print. PMID: 32730637
    CrossrefPubMedGoogle Scholar