Longitudinal Doppler Assessments in Late Preterm Fetal Growth Restriction

Bronacha Mylrea-Foley; Hans Wolf; Tamara Stampalija; Christoph Lees; B. Arabin; A. Berger; E. Bergman; A. Bhide; C. M. Bilardo; A. C. Breeze; J. Brodszki; P. Calda; I. Cetin; E. Cesari; J. Derks; C. Ebbing; E. Ferrazzi; W. Ganzevoort; T. Frusca; S. J. Gordijn; W. Gyselaers; K. Hecher; P. Klaritsch; L. Krofta; P. Lindgren; S. M. Lobmaier; N. Marlow; G. M. Maruotti; F. Mecacci; K. Myklestad; R. Napolitano; F. Prefumo; L. Raio; J. Richter; R. K. Sande; J. Thornton; H. Valensise; G. H. A. Visser; L. Wee; On behalf of the Truffle-2 Group; TRUFFLE 2 Authors:; TRUFFLE-2 GROUP AND COLLABORATING AUTHORS; C. Brezinka, Department of Obstetrics and Gynecology, Medical University of Innsbruck, Innsbruck, Austria; D. Casagrandi, University College London Hospitals NHS Foundation Trust, London, UK; A. Cerny, Department of Obstetrics and Gynaecology, GeneralUniversity Hospital and First Faculty of Medicine, Charles University, Prague, Czech Republic; A. Dall’Asta, Department of Obstetrics and Gynecology, University of Parma, Parma, Italy; R. DeVlieger, Department of Gynecology and Obstetrics, UZ Leuven, Leuven and Department of Regeneration and Development, KU Leuven, Leuven, Belgium; J. Duvekot, Department of Obstetrics and Gynecology, Erasmus Academic Centre Rotterdam, Rotterdam, The Netherlands; T. M. Eggebo, St Olav’s Hospital, Trondheim, Norway; I. Fantasia, Unit of Fetal Medicine and Prenatal Diagnosis, Institute for Maternal and Child Health, IRCCS Burlo Garofolo, Trieste, Italy; F. Ferrari, Obstetrics & Gynecology, Policlinico University Hospital of Modena, Modena, Italy; N. Fratelli, Department of Obstetrics and Gynecology, ASST Spedali Civili di Brescia and University of Brescia, Brescia, Italy; T. Ghi, Department of Obstetrics and Gynecology, University of Parma, Parma, Italy; O. Graupner, Department of Obstetrics and Gynecology, Klinikum Rechts Der Isar, Technical University of Munich, Munich, Germany; P. Greimel, Department of Obstetrics and Gynecology, Medical University of Graz, Graz, Austria; C. Hofstaetter, Department of Obstetrics & Gynecology, University Hospital of Bern, Bern, Switzerland; D. Lo Presti, Department of Surgery, Division of Obstetrics and Gynecology, Tor Vergata University, Policlinico Casilino Hospital, Rome, Italy; M. Georg, Helsinki University Central Hospital, Helsinki, Finland; F. Macsali, Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway; K. Marsal, Department of Obstetrics and Gynecology, Lund University, Skåne University Hospital, Lund, Sweden; P. Martinelli, Department of Neurosciences, Reproductive and Dentistry Sciences, University of Naples ‘Federico II’, Naples, Italy; E. Ostermayer, Department of Obstetrics and Gynecology, Klinikum Rechts Der Isar, Technical University of Munich, Munich, Germany; A. Papageorghiou, Fetal Medicine Unit, St George’s University Hospitals NHS Foundation Trust and Molecular & Clinical Sciences Research Institute, St George’s, University of London, London, UK; R. Peasley, Fetal Medicine Unit, University College London Hospitals NHS Foundation Trust, London, UK; A. Ramoni, Department of Obstetrics and Gynecology, Medical University of Innsbruck, Innsbruck, Austria; L. Sarno, Department of Neurosciences, Reproductive and Dentistry Sciences, University of Naples ‘Federico II’, Naples, Italy; L. Seikku, Helsinki University Central Hospital, Helsinki, Finland; S. Simeone, Department of Health Sciences, University of Florence, Obstetrics and Gynecology, Careggi University Hospital, Florence, Italy; B. Thilaganathan, Fetal Medicine Unit, St George’s University Hospitals NHS Foundation Trust and Molecular & Clinical Sciences Research Institute, St George’s, University of London, London, UK; G. Tiralongo, Department of Surgery, Division of Obstetrics and Gynecology, Tor Vergata University, Policlinico Casilino Hospital, Rome, Italy; A. Valcamonico, Department of Obstetrics and Gynecology, ASST Spedali Civili di Brescia and University of Brescia, Brescia, Italy; C. Van Holsbeke, Department of Obstetrics & Gynaecology,  Ziekenhuis Oost-Limburg, Genk, Belgium; A. Vietheer, Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway

doi:10.1055/a-1511-8293

Ultraschall in der Medizin - European Journal of Ultrasound, Table of Contents

Ultraschall Med 2023; 44(01): 56-67
DOI: 10.1055/a-1511-8293

Original Article

Longitudinal Doppler Assessments in Late Preterm Fetal Growth Restriction

Longitudinale Doppler-Bewertungen bei später fetaler Wachstumsrestriktion

Authors

Bronacha Mylrea-Foley

¹Institute for Reproductive and Developmental Biology, Department of Metabolism, Digestion and Reproduction, Imperial College London, UK

²Queen Charlotteʼs and Chelsea Hospital, Imperial College Healthcare NHS Trust, London W12 0HS
Hans Wolf^*

³Department of Obstetrics and Gynecology, Amsterdam University Medical Center (Location AMC), University of Amsterdam, Amsterdam, The Netherlands
Tamara Stampalija

⁴Unit of Fetal Medicine and Prenatal Diagnosis, Institute for Maternal and Child Health, IRCCS Burlo Garofolo, Trieste, Italy

⁵Department of Medicine, Surgery and Health Sciences, University of Trieste, Trieste, Italy
Christoph Lees^*

¹Institute for Reproductive and Developmental Biology, Department of Metabolism, Digestion and Reproduction, Imperial College London, UK

²Queen Charlotteʼs and Chelsea Hospital, Imperial College Healthcare NHS Trust, London W12 0HS

³³Department of Gynecology and Obstetrics, UZ Leuven and Department of Regeneration and Development, KU Leuven, Leuven, Belgium

On behalf of the Truffle-2 Group

TRUFFLE 2 Authors:

B. Arabin

⁶Department of Obstetrics Charite, Humboldt University Berlin and Clara Angela Foundation, Berlin, Germany
A. Berger

⁷Department of Obstetrics and Gynecology, Medical University of Innsbruck, Innsbruck, Austria
E. Bergman

⁸Department of Women’s and Children’s Health, Uppsala University, Uppsala, Sweden
A. Bhide

⁹Fetal Medicine Unit, St George’s University Hospitals NHS Foundation Trust and Molecular & Clinical Sciences Research Institute, St George’s, University of London, London, UK
C. M. Bilardo

¹⁰Department of Obstetrics and Gynecology, Amsterdam University Medical Centers, University of Amsterdam, location VUMC, Amsterdam, The Netherlands
A. C. Breeze

¹¹Fetal Medicine Unit, Leeds General Infirmary, Leeds Teaching Hospitals NHS Trust, Leeds, UK
J. Brodszki

¹²Department of Pediatric Surgery and Neonatology, Lund University, Skane University Hospital, Lund, Sweden
P. Calda

¹³Department of Obstetrics and Gynaecology, General University Hospital and First Faculty of Medicine, Charles University, Prague, Czech Republic
I. Cetin

¹⁴Department of Obstetrics and Gynecology, Vittore Buzzi Children’s Hospital, University of Milan, Milan, Italy
E. Cesari

¹⁴Department of Obstetrics and Gynecology, Vittore Buzzi Children’s Hospital, University of Milan, Milan, Italy
J. Derks

¹⁵Department of Perinatal Medicine, University of Utrecht, Utrecht, The Netherlands
C. Ebbing

¹⁶Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway
E. Ferrazzi

¹⁷Department of Obstetrics and Gynecology, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico and Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Milan, Italy
W. Ganzevoort

³Department of Obstetrics and Gynecology, Amsterdam University Medical Center (Location AMC), University of Amsterdam, Amsterdam, The Netherlands
T. Frusca

¹⁸Department of Obstetrics and Gynecology, University of Parma, Parma, Italy
S. J. Gordijn

¹⁹Department of Obstetrics and Gynaecology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
W. Gyselaers

²⁰Faculty of Medicine and Life Sciences, Hasselt University, Agoralaan, Diepenbeek, Belgium, Department of Obstetrics & Gynaecology, Ziekenhuis Oost-Limburg, Genk and Department Physiology, Hasselt University, Diepenbeek, Belgium
K. Hecher

²¹Department of Obstetrics and Fetal Medicine, University Medical Centre Hamburg-Eppendorf, Hamburg, Germany
P. Klaritsch

²²Department of Obstetrics and Gynecology, Medical University of Graz, Graz, Austria
L. Krofta

²³Institute for the Care of Mother and Child, Prague, Czech Republic and Third Medical Faculty, Charles University, Prague, Czech Republic
P. Lindgren

²⁴Center for Fetal Medicine, Karolinska University Hospital, Stockholm, Sweden
S. M. Lobmaier

²⁵Department of Obstetrics and Gynecology, Klinikum Rechts Der Isar, Technical University of Munich, Munich, Germany
N. Marlow

²⁶UCL Elizabeth Garrett Anderson Institute for Women’s Health, University College London, London, UK
G. M. Maruotti

²⁷Department of Neurosciences, Reproductive and Dentistry Sciences, University of Naples ‘Federico II’, Naples, Italy
F. Mecacci

²⁸Department of Health Sciences, University of Florence, Obstetrics and Gynecology, Careggi University Hospital, Florence, Italy
K. Myklestad

²⁹St Olav’s Hospital, Trondheim, Norway
R. Napolitano

²⁶UCL Elizabeth Garrett Anderson Institute for Women’s Health, University College London, London, UK

³⁰Fetal Medicine Unit, University College London Hospitals NHS Foundation Trust, London, UK
F. Prefumo

³¹Department of Obstetrics and Gynecology, ASST Spedali Civili di Brescia and University of Brescia, Brescia, Italy
L. Raio

³²Department of Obstetrics & Gynecology, University Hospital of Bern, Bern, Switzerland
J. Richter

³³Department of Gynecology and Obstetrics, UZ Leuven and Department of Regeneration and Development, KU Leuven, Leuven, Belgium
R. K. Sande

³⁴Department of Obstetrics and Gynecology, Stavanger University Hospital, Stavanger and Department of Clinical Science, University of Bergen, Bergen, Norway
J. Thornton

³⁵School of Clinical Sciences, University of Nottingham, Division of Obstetrics and Gynaecology, Maternity Department, City Hospital, Nottingham, UK
H. Valensise

³⁶Department of Surgery, Division of Obstetrics and Gynecology, Tor Vergata, University, Policlinico Casilino Hospital, Rome, Italy
G. H. A. Visser

¹⁶Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway
L. Wee

³⁷The Princess Alexandra Hospital NHS Trust, Harlow, UK

TRUFFLE-2 GROUP AND COLLABORATING AUTHORS

C. Brezinka, Department of Obstetrics and Gynecology, Medical University of Innsbruck, Innsbruck, Austria

D. Casagrandi, University College London Hospitals NHS Foundation Trust, London, UK

A. Cerny, Department of Obstetrics and Gynaecology, GeneralUniversity Hospital and First Faculty of Medicine, Charles University, Prague, Czech Republic

A. Dall’Asta, Department of Obstetrics and Gynecology, University of Parma, Parma, Italy

R. DeVlieger, Department of Gynecology and Obstetrics, UZ Leuven, Leuven and Department of Regeneration and Development, KU Leuven, Leuven, Belgium

J. Duvekot, Department of Obstetrics and Gynecology, Erasmus Academic Centre Rotterdam, Rotterdam, The Netherlands

T. M. Eggebo, St Olav’s Hospital, Trondheim, Norway

I. Fantasia, Unit of Fetal Medicine and Prenatal Diagnosis, Institute for Maternal and Child Health, IRCCS Burlo Garofolo, Trieste, Italy

F. Ferrari, Obstetrics & Gynecology, Policlinico University Hospital of Modena, Modena, Italy

N. Fratelli, Department of Obstetrics and Gynecology, ASST Spedali Civili di Brescia and University of Brescia, Brescia, Italy

T. Ghi, Department of Obstetrics and Gynecology, University of Parma, Parma, Italy

O. Graupner, Department of Obstetrics and Gynecology, Klinikum Rechts Der Isar, Technical University of Munich, Munich, Germany

P. Greimel, Department of Obstetrics and Gynecology, Medical University of Graz, Graz, Austria

C. Hofstaetter, Department of Obstetrics & Gynecology, University Hospital of Bern, Bern, Switzerland

D. Lo Presti, Department of Surgery, Division of Obstetrics and Gynecology, Tor Vergata University, Policlinico Casilino Hospital, Rome, Italy

M. Georg, Helsinki University Central Hospital, Helsinki, Finland

F. Macsali, Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway

K. Marsal, Department of Obstetrics and Gynecology, Lund University, Skåne University Hospital, Lund, Sweden

P. Martinelli, Department of Neurosciences, Reproductive and Dentistry Sciences, University of Naples ‘Federico II’, Naples, Italy

E. Ostermayer, Department of Obstetrics and Gynecology, Klinikum Rechts Der Isar, Technical University of Munich, Munich, Germany

A. Papageorghiou, Fetal Medicine Unit, St George’s University Hospitals NHS Foundation Trust and Molecular & Clinical Sciences Research Institute, St George’s, University of London, London, UK

R. Peasley, Fetal Medicine Unit, University College London Hospitals NHS Foundation Trust, London, UK

A. Ramoni, Department of Obstetrics and Gynecology, Medical University of Innsbruck, Innsbruck, Austria

L. Sarno, Department of Neurosciences, Reproductive and Dentistry Sciences, University of Naples ‘Federico II’, Naples, Italy

L. Seikku, Helsinki University Central Hospital, Helsinki, Finland

S. Simeone, Department of Health Sciences, University of Florence, Obstetrics and Gynecology, Careggi University Hospital, Florence, Italy

B. Thilaganathan, Fetal Medicine Unit, St George’s University Hospitals NHS Foundation Trust and Molecular & Clinical Sciences Research Institute, St George’s, University of London, London, UK

G. Tiralongo, Department of Surgery, Division of Obstetrics and Gynecology, Tor Vergata University, Policlinico Casilino Hospital, Rome, Italy

A. Valcamonico, Department of Obstetrics and Gynecology, ASST Spedali Civili di Brescia and University of Brescia, Brescia, Italy

C. Van Holsbeke, Department of Obstetrics & Gynaecology, Ziekenhuis Oost-Limburg, Genk, Belgium

A. Vietheer, Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway

Abstract

Purpose To assess the longitudinal variation of the ratio of umbilical and cerebral artery pulsatility index (UCR) in late preterm fetal growth restriction (FGR).

Materials and Methods A prospective European multicenter observational study included women with a singleton pregnancy, 32^+ 0–36^+ 6, at risk of FGR (estimated fetal weight [EFW] or abdominal circumference [AC] < 10^th percentile, abnormal arterial Doppler or fall in AC from 20-week scan of > 40 percentile points). The primary outcome was a composite of abnormal condition at birth or major neonatal morbidity. UCR was categorized as normal (< 0.9) or abnormal (≥ 0.9). UCR was assessed by gestational age at measurement interval to delivery, and by individual linear regression coefficient in women with two or more measurements.

Results 856 women had 2770 measurements; 696 (81 %) had more than one measurement (median 3 (IQR 2–4). At inclusion, 63 (7 %) a UCR ≥ 0.9. These delivered earlier and had a lower birth weight and higher incidence of adverse outcome (30 % vs. 9 %, relative risk 3.2; 95 %CI 2.1–5.0) than women with a normal UCR at inclusion. Repeated measurements after an abnormal UCR at inclusion were abnormal again in 67 % (95 %CI 55–80), but after a normal UCR the chance of finding an abnormal UCR was 6 % (95 %CI 5–7 %). The risk of composite adverse outcome was similar using the first or subsequent UCR values.

Conclusion An abnormal UCR is likely to be abnormal again at a later measurement, while after a normal UCR the chance of an abnormal UCR is 5–7 % when repeated weekly. Repeated measurements do not predict outcome better than the first measurement, most likely due to the most compromised fetuses being delivered after an abnormal UCR.

Zusammenfassung

Ziel Beurteilung der longitudinalen Variation der umbilikozerebralen Ratio (UCR) der Pulsatilitätsindizes bei später fetaler Wachstumsrestriktion (FGR).

Material und Methoden Eine prospektive europäische multizentrische Beobachtungsstudie schloss Frauen mit Einlingsschwangerschaft (32^+ 0–36^+ 6) und Risiko für FGR ein (geschätztes fetales Gewicht (EFW) oder Abdomenumfang (AU) < 10. Perzentile, abnormaler arterieller Doppler oder Absinken der AU-Perzentile um > 40 Punkte im US in der 20. SSW). Der primäre Outcome war kombiniert aus auffälligen Geburtsparametern oder schwerer neonataler Morbidität. Die UCR wurde als normal (< 0,9) oder abnormal (≥ 0,9) eingestuft. Die UCR wurde im Messintervall bis zur Entbindung mittels SSW und mittels individuellen linearen Regressionskoeffizienten bei Frauen mit 2 oder mehr Messungen bewertet.

Ergebnisse 856 Frauen hatten 2770 Messungen; 696 (81 %) hatten mehr als eine Messung (Median 3, IQR 2–4). Bei Einschluss hatten 63 (7 %) eine UCR ≥ 0,9. Diese entbanden früher und hatten ein niedrigeres Geburtsgewicht und eine höhere Inzidenz für einen unerwünschten Outcome (30 % vs. 9 %, relatives Risiko 3,2; 95 %-KI 2,1–5,0) im Vergleich zu Frauen mit normaler UCR bei Einschluss. Wiederholte Messungen nach abnormaler UCR bei Einschluss waren in 67 % (95 %-KI 55–80) erneut abnormal, aber nach einer normalen UCR betrug die Wahrscheinlichkeit, eine abnormale UCR zu finden, 6 % (95 %-KI 5–7 %). Das Risiko für einen kombinierten unerwünschten Outcome war ähnlich, wenn man den ersten oder den nachfolgenden UCR-Wert verwendete.

Schlussfolgerung Eine abnormale UCR ist wahrscheinlich bei einer späteren Messung wieder abnormal, während nach einer normalen UCR die Wahrscheinlichkeit einer abnormalen UCR bei wöchentlicher Wiederholung 5–7 % beträgt. Wiederholte Messungen sagen das Ergebnis nicht besser voraus als die erste Messung, was höchstwahrscheinlich darauf zurückzuführen ist, dass die am stärksten gefährdeten Föten nach einer abnormalen UCR entbunden werden.

Key words

late fetal growth restriction - Doppler - middle cerebral artery - brain sparing - adverse outcome

Full Text

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