Effects of Mediterranean Diet or Mindfulness-Based Stress Reduction during Pregnancy on Fetal Brain Development Detected by Neurosonography: A Secondary Analysis of a Randomized Clinical Trial (IMPACT BCN)

2.

Marshall

NE

,

Abrams

B

,

Barbour

LA

,

Catalano

P

,

Christian

P

,

Friedman

JE

, et al.

The importance of nutrition in pregnancy and lactation: lifelong consequences

.

Am J Obstet Gynecol

.

2022

;

226

(

5

):

607

–

32

.

3.

Edlow

AG

.

Maternal obesity and neurodevelopmental and psychiatric disorders in offspring: maternal obesity and offspring neurodevelopmental disorders

.

Prenat Diagn

.

2017

;

37

(

1

):

95

–

110

.

4.

Steenweg-de Graaff

J

,

Tiemeier

H

,

Steegers-Theunissen

RPM

,

Hofman

A

,

Jaddoe

VWV

,

Verhulst

FC

, et al.

Maternal dietary patterns during pregnancy and child internalising and externalising problems. The Generation R Study

.

Clin Nutr

.

2014

;

33

(

1

):

115

–

21

.

5.

Urbonaite

G

,

Knyzeliene

A

,

Bunn

FS

,

Smalskys

A

,

Neniskyte

U

.

The impact of maternal high-fat diet on offspring neurodevelopment

.

Front Neurosci

.

2022

;

16

:

909762

.

6.

Bordeleau

M

,

Fernández de Cossío

L

,

Chakravarty

MM

,

Tremblay

M-È

.

From maternal diet to neurodevelopmental disorders: a story of neuroinflammation

.

Front Cell Neurosci

.

2020

;

14

:

612705

.

7.

Motoki

N

,

Inaba

Y

,

Shibazaki

T

,

Misawa

Y

,

Ohira

S

,

Kanai

M

, et al.

Insufficient maternal gestational weight gain and infant neurodevelopment at 12 months of age: the Japan Environment and Children’s Study

.

Eur J Pediatr

.

2022

;

181

(

3

):

921

–

31

.

8.

Van den Bergh

BRH

,

Mulder

EJH

,

Mennes

M

,

Glover

V

.

Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review

.

Neurosci Biobehav Rev

.

2005

;

29

(

2

):

237

–

58

.

9.

Bock

J

,

Wainstock

T

,

Braun

K

,

Segal

M

.

Stress in utero: prenatal programming of brain plasticity and cognition

.

Biol Psychiatry

.

2015

;

78

(

5

):

315

–

26

.

10.

Wu

Y

,

Espinosa

KM

,

Barnett

SD

,

Kapse

A

,

Quistorff

JL

,

Lopez

C

, et al.

Association of elevated maternal psychological distress, altered fetal brain, and offspring cognitive and social-emotional outcomes at 18 months

.

JAMA Netw Open

.

2022

;

5

(

4

):

e229244

.

11.

Anifantaki

F

,

Pervanidou

P

,

Lambrinoudaki

I

,

Panoulis

K

,

Vlahos

N

,

Eleftheriades

M

.

Maternal prenatal stress, thyroid function and neurodevelopment of the offspring: a mini review of the literature

.

Front Neurosci

.

2021

;

15

:

692446

.

12.

Marques

AH

,

Bjørke-Monsen

A-L

,

Teixeira

AL

,

Silverman

MN

.

Maternal stress, nutrition and physical activity: impact on immune function, CNS development and psychopathology

.

Brain Res

.

2015

;

1617

:

28

–

46

.

13.

Crovetto

F

,

Crispi

F

,

Casas

R

,

Martín-Asuero

A

,

Borràs

R

,

Vieta

E

, et al.

Effects of mediterranean diet or mindfulness-based stress reduction on prevention of small-for-gestational age birth weights in newborns born to at-risk pregnant individuals: the IMPACT BCN randomized clinical trial

.

JAMA

.

2021

;

326

(

21

):

2150

–

60

.

14.

Crovetto

F

,

Nakaki

A

,

Arranz

A

,

Borras

R

,

Vellvé

K

,

Paules

C

, et al.

Effect of a mediterranean diet or mindfulness-based stress reduction during pregnancy on child neurodevelopment: a prespecified analysis of the IMPACT BCN randomized clinical trial

.

JAMA Netw Open

.

2023

;

6

(

8

):

e2330255

.

15.

Nakaki

A

,

Crovetto

F

,

Urru

A

,

Piella

G

,

Borras

R

,

Comte

V

, et al.

Effects of mediterranean diet or mindfulness-based stress reduction on fetal and neonatal brain development A secondary analysis of a randomized clinical trial (IMPACT BCN)

.

Am J Obstet Gyneocol

.

2023

;

MFM

:

101188

.

16.

Malinger

G

,

Paladini

D

,

Haratz

KK

,

Monteagudo

A

,

Pilu

GL

,

Timor‐Tritsch

IE

.

ISUOG Practice Guidelines (updated): sonographic examination of the fetal central nervous system. Part 1: performance of screening examination and indications for targeted neurosonography

.

Ultrasound Obstet Gynecol

.

2020

;

56

(

3

):

476

–

84

.

17.

Paladini

D

,

Malinger

G

,

Birnbaum

R

,

Monteagudo

A

,

Pilu

G

,

Salomon

LJ

, et al.

ISUOG Practice Guidelines (updated): sonographic examination of the fetal central nervous system. Part 2: performance of targeted neurosonography

.

Ultrasound Obstet Gynecol

.

2021

;

57

(

4

):

661

–

71

.

18.

Malinger

G

,

Paladini

D

,

Pilu

G

,

Timor-Tritsch

IE

.

Fetal cerebral magnetic resonance imaging, neurosonography and the brave new world of fetal medicine

.

Ultrasound Obstet Gynecol

.

2017

;

50

(

6

):

679

–

80

.

19.

Hahner

N

,

Puerto

B

,

Perez-Cruz

M

,

Policiano

C

,

Monterde

E

,

Crispi

F

, et al.

Altered cortical development in fetuses with isolated nonsevere ventriculomegaly assessed by neurosonography

.

Prenat Diagn

.

2018

;

38

(

5

):

365

–

75

.

20.

Pérez‐Cruz

M

,

Gómez

O

,

Gibert

M

,

Masoller

N

,

Marimon

E

,

Lip‐Sosa

D

, et al.

Corpus callosum size by neurosonography in fetuses with congenital heart defect and relationship with expected pattern of brain oxygen supply

.

Ultrasound Obstet Gynecol

.

2022

;

59

(

2

):

220

–

5

.

21.

Egaña-Ugrinovic

G

,

Savchev

S

,

Bazán-Arcos

C

,

Puerto

B

,

Gratacós

E

,

Sanz-Cortés

M

.

Neurosonographic assessment of the corpus callosum as imaging biomarker of abnormal neurodevelopment in late-onset fetal growth restriction

.

Fetal Diagn Ther

.

2015

;

37

(

4

):

281

–

8

.

22.

Paules

C

,

Miranda

J

,

Policiano

C

,

Crovetto

F

,

Youssef

L

,

Hahner

N

, et al.

Fetal neurosonography detects differences in cortical development and corpus callosum in late‐onset small fetuses

.

Ultrasound Obstet Gynecol

.

2021

;

23592

.

23.

Basso

A

,

Youssef

L

,

Nakaki

A

,

Paules

C

,

Miranda

J

,

Casu

G

, et al.

Fetal neurosonography at 31‐35 weeks reveals altered cortical development in pre‐eclampsia with and without small‐for‐gestational‐age fetus

.

Ultrasound Obstet Gyne

.

2022

;

24853

.

24.

Boutet

ML

,

Eixarch

E

,

Ahumada‐Droguett

P

,

Nakaki

A

,

Crovetto

F

,

Cívico

MS

, et al.

Fetal neurosonography and infant neurobehavior in assisted reproductive technologies following fresh and frozen embryo transfer

.

Ultrasound Obstet Gyne

.

2022

;

24920

.

25.

Pooh

RK

,

Machida

M

,

Nakamura

T

,

Uenishi

K

,

Chiyo

H

,

Itoh

K

, et al.

Increased Sylvian fissure angle as early sonographic sign of malformation of cortical development

.

Ultrasound Obstet Gynecol

.

2018

;

9

.

26.

Crowley

T

.

The investigation and management of the small–for–gestational–age fetus

.

2014

; p.

1

–

34

.

27.

Figueras

F

,

Meler

E

,

Iraola

A

,

Eixarch

E

,

Coll

O

,

Figueras

J

, et al.

Customized birthweight standards for a Spanish population

.

Eur J Obstet Gynecol Reprod Biol

.

2008

;

136

(

1

):

20

–

4

.

28.

Estruch

R

,

Ros

E

,

Salas-Salvadó

J

,

Covas

M-I

,

Corella

D

,

Arós

F

, et al.

Primary prevention of cardiovascular disease with a mediterranean diet supplemented with extra-virgin olive oil or nuts

.

N Engl J Med

.

2018

;

378

(

25

):

e34

–

14

.

29.

Crovetto

F

,

Crispi

F

,

Borras

R

,

Paules

C

,

Casas

R

,

Martín-Asuero

A

, et al.

Mediterranean diet, Mindfulness-Based Stress Reduction and usual care during pregnancy for reducing fetal growth restriction and adverse perinatal outcomes: IMPACT BCN (Improving Mothers for a better PrenAtal Care Trial BarCeloNa): a study protocol for a randomized controlled trial

.

Trials

.

2021

;

22

(

1

):

362

.

30.

Juton

C

,

Castro-Barquero

S

,

Casas

R

,

Freitas

T

,

Ruiz-León

AM

,

Crovetto

F

, et al.

Reliability and concurrent and construct validity of a food frequency questionnaire for pregnant women at high risk to develop fetal growth restriction

.

Nutrients

.

2021

;

13

(

5

):

1629

.

31.

Castro-Barquero

S

,

Crovetto

F

,

Estruch

R

,

María Ruiz-León

A

,

Larroya

M

,

Sacanella

E

, et al.

Validation of a pregnancy-adapted Mediterranean diet Adherence Screener (preg-MEDAS): a validation study nested in the IMPACT BCN trial

.

Am J Clin Nutr

.

2024

;

S0002916524005197

.

32.

Bech

P

,

Olsen

LR

,

Kjoller

M

,

Rasmussen

NK

.

Measuring well-being rather than the absence of distress symptoms: a comparison of the SF-36 Mental Health subscale and the WHO-Five well-being scale

.

Int J Method Psychiat Res

.

2003

;

12

(

2

):

85

–

91

.

33.

Marcos

J

,

Renau

N

,

Casals

G

,

Segura

J

,

Ventura

R

,

Pozo

OJ

.

Investigation of endogenous corticosteroids profiles in human urine based on liquid chromatography tandem mass spectrometry

.

Anal Chim Acta

.

2014

;

812

:

92

–

104

.

34.

Braithwaite

EC

,

Pickles

A

,

Sharp

H

,

Glover

V

,

O’Donnell

KJ

,

Tibu

F

, et al.

Maternal prenatal cortisol predicts infant negative emotionality in a sex-dependent manner

.

Physiol Behav

.

2017

;

175

:

31

–

6

.

35.

Glover

V

,

Bergman

K

,

Sarkar

P

,

O’Connor

TG

.

Association between maternal and amniotic fluid cortisol is moderated by maternal anxiety

.

Psychoneuroendocrinology

.

2009

;

34

(

3

):

430

–

5

.

36.

Mairesse

J

,

Lesage

J

,

Breton

C

,

Bréant

B

,

Hahn

T

,

Darnaudéry

M

, et al.

Maternal stress alters endocrine function of the feto-placental unit in rats

.

Am J Physiol Endocrinol Metab

.

2007

;

292

(

6

):

E1526

–

33

.

37.

Egaña-Ugrinovic

G

,

Sanz-Cortes

M

,

Figueras

F

,

Bargalló

N

,

Gratacós

E

.

Differences in cortical development assessed by fetal MRI in late-onset intrauterine growth restriction

.

Am J Obstet Gynecol

.

2013

;

209

(

2

):

126.e1

–

8

.

38.

Alonso

I

,

Borenstein

M

,

Grant

G

,

Narbona

I

,

Azumendi

G

.

Depth of brain fissures in normal fetuses by prenatal ultrasound between 19 and 30 weeks of gestation

.

Ultrasound Obstet Gynecol

.

2010

;

36

(

6

):

693

–

9

.

39.

Vinkesteijn

ASM

,

Mulder

PGH

,

Wladimiroff

JW

.

Fetal transverse cerebellar diameter measurements in normal and reduced fetal growth: cerebellar growth

.

Ultrasound Obstet Amp Gyne

.

2000

;

15

(

1

):

47

–

51

.

40.

Cignini

P

,

Padula

F

,

Giorlandino

M

,

Brutti

P

,

Alfò

M

,

Giannarelli

D

, et al.

Reference charts for fetal corpus callosum length: a prospective cross-sectional study of 2950 fetuses

.

J Ultrasound Med

.

2014

;

33

(

6

):

1065

–

78

.

41.

Sanz-Cortes

M

,

Egaña-Ugrinovic

G

,

Zupan

R

,

Figueras

F

,

Gratacos

E

.

Brainstem and cerebellar differences and their association with neurobehavior in term small-for-gestational-age fetuses assessed by fetal MRI

.

Am J Obstet Gynecol

.

2014

;

210

(

5

):

452.e1

–

8

.

42.

Sonographic examination of the fetal central nervous system: guidelines for performing the “basic examination” and the “fetal neurosonogram”

..

Ultrasound Obstet Gynecol

.

2007

;

29

(

1

):

109

–

16

.

43.

Koo

TK

,

Li

MY

.

A guideline of selecting and reporting intraclass correlation coefficients for reliability research

.

J Chiropr Med

.

2016

;

15

(

2

):

155

–

63

.

44.

Duggan

C

,

Irvine

AD

,

O’B Hourihane

J

,

Kiely

ME

,

Murray

DM

.

ASQ-3 and BSID-III’s concurrent validity and predictive ability of cognitive outcome at 5 years

.

Pediatr Res

.

2023

;

94

(

4

):

1465

–

71

.

45.

Sheldrick

RC

,

Marakovitz

S

,

Garfinkel

D

,

Carter

AS

,

Perrin

EC

.

Comparative accuracy of developmental screening questionnaires

.

JAMA Pediatr

.

2020

;

174

(

4

):

366

–

74

.

46.

Squires

J

,

Twombly

E

,

Bricker

D

,

Potter

L

.

ASQ-3 technical report. ASQ-3 User’s Guide

.

Brookes Publishing

;

2009

. Available from: https://agesandstages.com/wp-content/uploads/2017/05/ASQ-3-Technical-Appendix_web.pdf

47.

Morel

B

,

Bertault

P

,

Favrais

G

,

Tavernier

E

,

Tosello

B

,

Bednarek

N

, et al.

Automated brain MRI metrics in the EPIRMEX cohort of preterm newborns: correlation with the neurodevelopmental outcome at 2 years

.

Diagn Interv Imaging

.

2021

;

102

(

4

):

225

–

32

.

48.

Han

VX

,

Patel

S

,

Jones

HF

,

Dale

RC

.

Maternal immune activation and neuroinflammation in human neurodevelopmental disorders

.

Nat Rev Neurol

.

2021

;

17

(

9

):

564

–

79

.

49.

Bergdolt

L

,

Dunaevsky

A

.

Brain changes in a maternal immune activation model of neurodevelopmental brain disorders

.

Prog Neurobiol

.

2019

;

175

:

1

–

19

.

50.

Estes

ML

,

McAllister

AK

.

Maternal immune activation: implications for neuropsychiatric disorders

.

Science

.

2016

;

353

(

6301

):

772

–

7

.

51.

Maldonado-Ruiz

R

,

Garza-Ocañas

L

,

Camacho

A

.

Inflammatory domains modulate autism spectrum disorder susceptibility during maternal nutritional programming

.

Neurochem Int

.

2019

;

126

:

109

–

17

.

52.

Lindsay

KL

,

Buss

C

,

Wadhwa

PD

,

Entringer

S

.

The interplay between nutrition and stress in pregnancy: implications for fetal programming of brain development

.

Biol Psychiatry

.

2019

;

85

(

2

):

135

–

49

.

53.

Limperopoulos

C

,

Wu

Y

.

Association of prenatal maternal psychological distress with fetal brain growth, metabolism, and cortical maturation

.

JAMA Netw Open

.

2020

;

3

(

1

):

e1920030

-

16

.

54.

Lu

Y-C

,

Kapse

K

,

Andersen

N

,

Quistorff

J

,

Lopez

C

,

Fry

A

, et al.

Association between socioeconomic status and in utero fetal brain development

.

JAMA Netw Open

.

2021

;

4

(

3

):

e213526

.

55.

Niculescu

MD

,

Lupu

DS

.

High fat diet‐induced maternal obesity alters fetal hippocampal development

.

Int J Dev Neurosci

.

2009

;

27

(

7

):

627

–

33

.

56.

Madore

C

,

Leyrolle

Q

,

Morel

L

,

Rossitto

M

,

Greenhalgh

AD

,

Delpech

JC

, et al.

Essential omega-3 fatty acids tune microglial phagocytosis of synaptic elements in the mouse developing brain

.

Nat Commun

.

2020

;

11

(

1

):

6133

.

57.

Schwingshackl

L

,

Morze

J

,

Hoffmann

G

.

Mediterranean diet and health status: active ingredients and pharmacological mechanisms

.

Br J Pharmacol

.

2020

;

177

(

6

):

1241

–

57

.

58.

Gu

Y

,

Brickman

AM

,

Stern

Y

,

Habeck

CG

,

Razlighi

QR

,

Luchsinger

JA

, et al.

Mediterranean diet and brain structure in a multiethnic elderly cohort

.

Neurology

.

2015

;

85

(

20

):

1744

–

51

.

59.

Staubo

SC

,

Aakre

JA

,

Vemuri

P

,

Syrjanen

JA

,

Mielke

MM

,

Geda

YE

, et al.

Mediterranean diet, micronutrients and macronutrients, and MRI measures of cortical thickness

.

Alzheimers Dement

.

2017

;

13

(

2

):

168

–

77

.

60.

Rodrigues

B

,

Coelho

A

,

Portugal-Nunes

C

,

Magalhães

R

,

Moreira

PS

,

Castanho

TC

, et al.

Higher adherence to the mediterranean diet is associated with preserved white matter integrity and altered structural connectivity

.

Front Neurosci

.

2020

;

14

:

786

.

61.

Li

M

,

Francis

E

,

Hinkle

SN

,

Ajjarapu

AS

,

Zhang

C

.

Preconception and prenatal nutrition and neurodevelopmental disorders: a systematic review and meta-analysis

.

Nutrients

.

2019

;

11

(

7

):

1628

.

62.

Morton

SU

,

Vyas

R

,

Gagoski

B

,

Vu

C

,

Litt

J

,

Larsen

RJ

, et al.

Maternal dietary intake of omega-3 fatty acids correlates positively with regional brain volumes in 1-month-old term infants

.

Cereb Cortex

.

2020

;

30

(

4

):

2057

–

69

.

63.

Ogundipe

E

,

Tusor

N

,

Wang

Y

,

Johnson

MR

,

Edwards

AD

,

Crawford

MA

.

Randomized controlled trial of brain specific fatty acid supplementation in pregnant women increases brain volumes on MRI scans of their newborn infants

.

Prostaglandins Leukot Essent Fatty Acids

.

2018

;

138

:

6

–

13

.

64.

House

JS

,

Mendez

M

,

Maguire

RL

,

Gonzalez-Nahm

S

,

Huang

Z

,

Daniels

J

, et al.

Periconceptional maternal mediterranean diet is associated with favorable offspring behaviors and altered CpG methylation of imprinted genes

.

Front Cell Dev Biol

.

2018

;

6

:

107

.

65.

Witek Janusek

L

,

Tell

D

,

Mathews

HL

.

Mindfulness based stress reduction provides psychological benefit and restores immune function of women newly diagnosed with breast cancer: a randomized trial with active control

.

Brain Behav Immun

.

2019

;

80

:

358

–

73

.

66.

Saban

KL

,

Collins

EG

,

Mathews

HL

,

Bryant

FB

,

Tell

D

,

Gonzalez

B

, et al.

Impact of a mindfulness-based stress reduction program on psychological well-being, cortisol, and inflammation in women veterans

.

J Gen Intern Med

.

2022

;

37

(

Suppl 3

):

751

–

61

.

67.

Galante

J

,

Friedrich

C

,

Dawson

AF

,

Modrego-Alarcón

M

,

Gebbing

P

,

Delgado-Suárez

I

, et al.

Mindfulness-based programmes for mental health promotion in adults in nonclinical settings: a systematic review and meta-analysis of randomised controlled trials

.

PLoS Med

.

2021

;

18

(

1

):

e1003481

.

68.

Guo

P

,

Zhang

X

,

Liu

N

,

Wang

J

,

Chen

D

,

Sun

W

, et al.

Mind–body interventions on stress management in pregnant women: a systematic review and meta‐analysis of randomized controlled trials

.

J Adv Nurs

.

2021

;

77

(

1

):

125

–

46

.

69.

Tamayo y Ortiz

M

,

Téllez-Rojo

MM

,

Trejo-Valdivia

B

,

Schnaas

L

,

Osorio-Valencia

E

,

Coull

B

, et al.

Maternal stress modifies the effect of exposure to lead during pregnancy and 24-month old children’s neurodevelopment

.

Environ Int

.

2017

;

98

:

191

–

7

.

70.

Noroña-Zhou

AN

,

Coccia

M

,

Epel

E

,

Vieten

C

,

Adler

NE

,

Laraia

B

, et al.

The effects of a prenatal mindfulness intervention on infant autonomic and behavioral reactivity and regulation

.

Psychosom Med

.

2022

;

84

(

5

):

525

–

35

.