Fetal Myocardial Function as Assessed by N-Terminal Fragment Brain Natriuretic Protein in Premature Fetuses Exposed to Intra-amniotic Inflammation

Roxanna A. Irani; Catalin S. Buhimschi; Sarah N. Cross; Guomao Zhao; Joshua A. Copel; Vineet Bhandari; Irina A. Buhimschi; Mert Ozan Bahtiyar

doi:10.1055/s-0039-1688909

American Journal of Perinatology, Inhaltsverzeichnis

Am J Perinatol 2020; 37(07): 745-753
DOI: 10.1055/s-0039-1688909

Original Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Fetal Myocardial Function as Assessed by N-Terminal Fragment Brain Natriuretic Protein in Premature Fetuses Exposed to Intra-amniotic Inflammation

Roxanna A. Irani

¹Department of Obstetrics, Gynecology, and Reproductive Sciences, Division of Maternal-Fetal Medicine, University of California San Francisco, San Francisco, California

,

Catalin S. Buhimschi

²Department of Obstetrics & Gynecology, University of Illinois at Chicago College of Medicine, Chicago, Illinois

,

Sarah N. Cross

³Department of Obstetrics, Gynecology, and Women's Health, Division of Maternal-Fetal Medicine, University of Minnesota, Minneapolis, Minnesota

,

Guomao Zhao

²Department of Obstetrics & Gynecology, University of Illinois at Chicago College of Medicine, Chicago, Illinois

,

Joshua A. Copel

⁴Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, Connecticut

⁵Department of Pediatrics, Yale School of Medicine, New Haven, Connecticut

,

Vineet Bhandari

⁶Department of Pediatrics, Drexel University College of Medicine, Philadelphia, Pennsylvania

,

Irina A. Buhimschi

²Department of Obstetrics & Gynecology, University of Illinois at Chicago College of Medicine, Chicago, Illinois

,

Mert Ozan Bahtiyar

⁴Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, Connecticut

› Institutsangaben

Abstract

Objective This study aimed to determine the relationship between fetal exposure to intra-amniotic infection/inflammation (IAI) and fetal heart ventricular function as assessed by circulatory levels of N-terminal fragment brain natriuretic protein (NT-proBNP) and the Tei index.

Study Design We analyzed 70 samples of paired amniotic fluid (AF) and cord blood retrieved from mothers who delivered preterm at <34 weeks as follows: Yes-IAI (n = 36) and No-IAI (n = 34). IAI was diagnosed by amniocentesis and AF mass spectrometry. Fetal exposure to inflammation was determined through the evaluation of cord blood haptoglobin (Hp) switch-on status and level, and interleukin (IL)-6 levels by Western blotting and enzyme-linked immunosorbent assay, respectively. Fetal heart function was assessed by cord blood NT-proBNP immunoassay and fetal echocardiogram (Tei index).

Results IAI was characterized by significantly higher levels of AF (p < 0.001) and umbilical cord IL-6 (p = 0.004). Cord blood Hp levels and frequency of switch-on status were higher in fetuses exposed to IAI (p < 0.001, both). Fetuses exposed to IAI did not have higher levels of NT-proBNP. Following correction for gestational age and race, neither cord blood NT-proBNP nor the Tei index was significantly different in fetuses with Hp switched-on status (p > 0.05, both).

Conclusion Fetal myocardial left ventricular function does not seem to be significantly impaired in fetuses born alive due to IAI if delivery of the fetus occurs immediately following the diagnosis of IAI.

Keywords

fetal echocardiogram - BNP - inflammation - infection - cardiac

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Referenzen

References
1 Buhimschi CS, Dulay AT, Abdel-Razeq S. , et al. Fetal inflammatory response in women with proteomic biomarkers characteristic of intra-amniotic inflammation and preterm birth. BJOG 2009; 116 (02) 257-267
2 Buhimschi CS, Bhandari V, Dulay AT. , et al. Proteomics mapping of cord blood identifies haptoglobin “switch-on” pattern as biomarker of early-onset neonatal sepsis in preterm newborns. PLoS One 2011; 6 (10) e26111
3 Archabald KL, Buhimschi IA, Bahtiyar MO. , et al. Limiting the exposure of select fetuses to intrauterine infection/inflammation improves short-term neonatal outcomes in preterm premature rupture of membranes. Fetal Diagn Ther 2017; 42 (02) 99-110
4 Gotsch F, Romero R, Kusanovic JP. , et al. The fetal inflammatory response syndrome. Clin Obstet Gynecol 2007; 50 (03) 652-683
5 Letti Müller AL, Barrios PdeM, Kliemann LM, Valério EG, Gasnier R, Magalhães JA. Tei index to assess fetal cardiac performance in fetuses at risk for fetal inflammatory response syndrome. Ultrasound Obstet Gynecol 2010; 36 (01) 26-31
6 Di Naro E, Cromi A, Ghezzi F, Giocolano A, Caringella A, Loverro G. Myocardial dysfunction in fetuses exposed to intraamniotic infection: new insights from tissue Doppler and strain imaging. Am J Obstet Gynecol 2010; 203 (05) 459.e1-459.e7
7 Romero R, Espinoza J, Gonçalves LF. , et al. Fetal cardiac dysfunction in preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2004; 16 (03) 146-157
8 Cameron VA, Ellmers LJ. Minireview: natriuretic peptides during development of the fetal heart and circulation. Endocrinology 2003; 144 (06) 2191-2194
9 Schwachtgen L, Herrmann M, Georg T, Schwarz P, Marx N, Lindinger A. Reference values of NT-proBNP serum concentrations in the umbilical cord blood and in healthy neonates and children. Z Kardiol 2005; 94 (06) 399-404
10 Pudil R, Tichy M, Andrys C, Drahosova M, Blaha V, Vojacek J. The use of plasma NT-pro BNP, interleukin 6, TNF alpha and sCD40L in assessment of acute heart failure severity in emergency department. J Mol Cell Cardiol 2006; 40: 951
11 Lee SM, Jun JK, Kim SA. , et al. N-terminal pro-B-type natriuretic peptide and cardiac troponin T in non-immune hydrops. J Obstet Gynaecol Res 2016; 42 (04) 380-384
12 Girsen A, Ala-Kopsala M, Mäkikallio K, Vuolteenaho O, Räsänen J. Cardiovascular hemodynamics and umbilical artery N-terminal peptide of proB-type natriuretic peptide in human fetuses with growth restriction. Ultrasound Obstet Gynecol 2007; 29 (03) 296-303
13 Committee opinion no 611: method for estimating due date. Obstet Gynecol 2014; 124 (04) 863-866
14 Higgins RD, Saade G, Polin RA. , et al; Chorioamnionitis Workshop Participants. Evaluation and management of women and newborns with a maternal diagnosis of chorioamnionitis: summary of a workshop. Obstet Gynecol 2016; 127 (03) 426-436
15 Committee on Practice Bulletins—Obstetrics, The American College of Obstetricians and Gynecologists. Practice bulletin no. 130: prediction and prevention of preterm birth. Obstet Gynecol 2012; 120 (04) 964-973
16 Buhimschi CS, Bhandari V, Hamar BD. , et al. Proteomic profiling of the amniotic fluid to detect inflammation, infection, and neonatal sepsis. PLoS Med 2007; 4 (01) e18
17 Rodwell RL, Leslie AL, Tudehope DI. Early diagnosis of neonatal sepsis using a hematologic scoring system. J Pediatr 1988; 112 (05) 761-767
18 Rychik J, Ayres N, Cuneo B. , et al. American Society of Echocardiography guidelines and standards for performance of the fetal echocardiogram. J Am Soc Echocardiogr 2004; 17 (07) 803-810
19 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 normals and dilated cardiomyopathy. J Cardiol 1995; 26 (06) 357-366
20 Friedman D, Buyon J, Kim M, Glickstein JS. Fetal cardiac function assessed by Doppler myocardial performance index (Tei Index). Ultrasound Obstet Gynecol 2003; 21 (01) 33-36
21 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 (03) 227-232
22 Tei C, Dujardin KS, Hodge DO. , et al. Doppler echocardiographic index for assessment of global right ventricular function. J Am Soc Echocardiogr 1996; 9 (06) 838-847
23 McCarthy ME, Buhimschi CS, Hardy JT. , et al. Identification of haptoglobin switch-on status in archived placental specimens indicates antenatal exposure to inflammation and potential participation of the fetus in triggering preterm birth. Placenta 2018; 62: 50-57
24 Salafia CM, Weigl C, Silberman L. The prevalence and distribution of acute placental inflammation in uncomplicated term pregnancies. Obstet Gynecol 1989; 73 (3 Pt 1): 383-389
25 Ghidini A, Salafia CM, Kirn V, Doria V, Spong CY. Biophysical profile in predicting acute ascending infection in preterm rupture of membranes before 32 weeks. Obstet Gynecol 2000; 96 (02) 201-206
26 Mannarino S, Garofoli F, Mongini E. , et al. BNP concentrations and cardiovascular adaptation in preterm and fullterm newborn infants. Early Hum Dev 2010; 86 (05) 295-298
27 Mannarino S, Ciardelli L, Garofoli F. , et al. Correlation between cord blood, perinatal BNP values and echocardiographic parameters in healthy Italian newborns. Early Hum Dev 2009; 85 (01) 13-17
28 Sutton MS, Gill T, Plappert T, Saltzman DH, Doubilet P. Assessment of right and left ventricular function in terms of force development with gestational age in the normal human fetus. Br Heart J 1991; 66 (04) 285-289
29 Cameron VA, Aitken GD, Ellmers LJ, Kennedy MA, Espiner EA. The sites of gene expression of atrial, brain, and C-type natriuretic peptides in mouse fetal development: temporal changes in embryos and placenta. Endocrinology 1996; 137 (03) 817-824
30 Siegel JH, Greenspan M, Del Guercio LR. Myocardial failure, vascular tone, and oxygen transport in septic shock in a human being. Surg Forum 1966; 17: 5-6
31 Merx MW, Weber C. Sepsis and the heart. Circulation 2007; 116 (07) 793-802
32 Parrillo JE, Burch C, Shelhamer JH, Parker MM, Natanson C, Schuette W. A circulating myocardial depressant substance in humans with septic shock. Septic shock patients with a reduced ejection fraction have a circulating factor that depresses in vitro myocardial cell performance. J Clin Invest 1985; 76 (04) 1539-1553
33 Yanowitz TD, Jordan JA, Gilmour CH. , et al. Hemodynamic disturbances in premature infants born after chorioamnionitis: association with cord blood cytokine concentrations. Pediatr Res 2002; 51 (03) 310-316
34 Tare M, Bensley JG, Moss TJ. , et al. Exposure to intrauterine inflammation leads to impaired function and altered structure in the preterm heart of fetal sheep. Clin Sci (Lond) 2014; 127 (09) 559-569
35 Seehase M, Gantert M, Ladenburger A. , et al. Myocardial response in preterm fetal sheep exposed to systemic endotoxinaemia. Pediatr Res 2011; 70 (03) 242-246
36 Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 1989; 298 (6673): 564-567
37 Duygu B, Poels EM, da Costa Martins PA. Genetics and epigenetics of arrhythmia and heart failure. Front Genet 2013; 4: 219
38 Lock MC, Botting KJ, Tellam RL, Brooks D, Morrison JL. Adverse intrauterine environment and cardiac miRNA expression. Int J Mol Sci 2017; 18 (12) E2628
39 Olson EN, Backs J, McKinsey TA. Control of cardiac hypertrophy and heart failure by histone acetylation/deacetylation. Novartis Found Symp 2006; 274: 3-12
40 Mathiyalagan P, Chang L, Du XJ, El-Osta A. Cardiac ventricular chambers are epigenetically distinguishable. Cell Cycle 2010; 9 (03) 612-617
41 Tsutsumi T, Ishii M, Eto G, Hota M, Kato H. Serial evaluation for myocardial performance in fetuses and neonates using a new Doppler index. Pediatr Int 1999; 41 (06) 722-727
42 Bahtiyar MO, Copel JA. Cardiac changes in the intrauterine growth-restricted fetus. Semin Perinatol 2008; 32 (03) 190-193
43 Dulay AT, Buhimschi IA, Zhao G. , et al. Compartmentalization of acute phase reactants interleukin-6, C-reactive protein and procalcitonin as biomarkers of intra-amniotic infection and chorioamnionitis. Cytokine 2015; 76 (02) 236-243
44 Damas P, Ledoux D, Nys M. , et al. Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg 1992; 215 (04) 356-362
45 Mäkikallio K, Rounioja S, Vuolteenaho O, Paakkari J, Hallman M, Räsänen J. Fetal cardiac natriuretic peptide expression and cardiovascular hemodynamics in endotoxin-induced acute cardiac dysfunction in mouse. Pediatr Res 2006; 59 (02) 180-184