Soil-transmitted helminth infection in pregnancy and long-term child neurocognitive and behavioral development: A prospective mother-child cohort in Benin.
Journal
PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
30
06
2020
accepted:
21
02
2021
entrez:
19
3
2021
pubmed:
20
3
2021
medline:
6
7
2021
Statut:
epublish
Résumé
An estimated 30% of women in Sub-Saharan Africa suffer from soil-transmitted helminth infection during pregnancy (SHIP), which has been shown to increase risk of pre-term birth, low birth weight, and maternal anemia. A previous study in Benin found that SHIP was associated with impaired cognitive and gross motor development scores in 635 one-year-old children. The objective of the present study was to follow children prospectively to investigate whether the association between SHIP and child neurocognitive and behavioral development persisted at age six. Our prospective child cohort included 487 live-born singletons of pregnant women enrolled in the Malaria in Pregnancy Preventive Alternative Drugs clinical trial in Allada, Benin. SHIP was assessed at three antenatal visits (ANVs) through collection and testing of stool samples. Neurocognitive and behavioral development was assessed in six-year-old children by trained investigators using the Kaufman Assessment Battery for Children 2nd edition and the parent-reported Strengths and Difficulties Questionnaire (SDQ). Multiple linear regression models generated coefficients and 95% confidence intervals and potential mediating factors were tested. Prevalence of SHIP was 13% at the 1st ANV, 9% at the 2nd ANV, and 1% at delivery. SHIP was not associated with low neurocognitive scores in children at six years. Higher SDQ internalizing scores, indicating increased emotional impairments in children, were associated with helminth infection at the 2nd ANV/delivery 1.07 (95% CI 0.15, 2.00) and at least once during pregnancy 0.79 (95% CI 0.12, 1.46) in adjusted models. Mediation analysis did not reveal significant indirect effects of several mediators on this association. Our study shows that while SHIP is not associated with impaired long-term neurocognitive development, infections may have significant negative impacts on emotional development in six-year-old children. SHIP remains a critical public health issue, and adequate prevention and treatment protocols should be enforced in low- and middle-income countries.
Sections du résumé
BACKGROUND
An estimated 30% of women in Sub-Saharan Africa suffer from soil-transmitted helminth infection during pregnancy (SHIP), which has been shown to increase risk of pre-term birth, low birth weight, and maternal anemia. A previous study in Benin found that SHIP was associated with impaired cognitive and gross motor development scores in 635 one-year-old children. The objective of the present study was to follow children prospectively to investigate whether the association between SHIP and child neurocognitive and behavioral development persisted at age six.
PRINCIPAL FINDINGS
Our prospective child cohort included 487 live-born singletons of pregnant women enrolled in the Malaria in Pregnancy Preventive Alternative Drugs clinical trial in Allada, Benin. SHIP was assessed at three antenatal visits (ANVs) through collection and testing of stool samples. Neurocognitive and behavioral development was assessed in six-year-old children by trained investigators using the Kaufman Assessment Battery for Children 2nd edition and the parent-reported Strengths and Difficulties Questionnaire (SDQ). Multiple linear regression models generated coefficients and 95% confidence intervals and potential mediating factors were tested. Prevalence of SHIP was 13% at the 1st ANV, 9% at the 2nd ANV, and 1% at delivery. SHIP was not associated with low neurocognitive scores in children at six years. Higher SDQ internalizing scores, indicating increased emotional impairments in children, were associated with helminth infection at the 2nd ANV/delivery 1.07 (95% CI 0.15, 2.00) and at least once during pregnancy 0.79 (95% CI 0.12, 1.46) in adjusted models. Mediation analysis did not reveal significant indirect effects of several mediators on this association.
CONCLUSIONS
Our study shows that while SHIP is not associated with impaired long-term neurocognitive development, infections may have significant negative impacts on emotional development in six-year-old children. SHIP remains a critical public health issue, and adequate prevention and treatment protocols should be enforced in low- and middle-income countries.
Identifiants
pubmed: 33739991
doi: 10.1371/journal.pntd.0009260
pii: PNTD-D-20-01184
pmc: PMC7978343
doi:
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0009260Subventions
Organisme : NICHD NIH HHS
ID : R21 HD060524
Pays : United States
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
BMC Public Health. 2016 Nov 23;16(1):1185
pubmed: 27881115
J Dev Behav Pediatr. 2013 Sep;34(7):486-93
pubmed: 23899660
Infect Immun. 2011 Mar;79(3):1254-61
pubmed: 21149589
Trans R Soc Trop Med Hyg. 2019 Apr 1;113(4):169-182
pubmed: 30551211
PLoS Pathog. 2015 Sep 24;11(9):e1005140
pubmed: 26402732
Brain Behav Immun. 2015 Feb;44:100-5
pubmed: 25218900
Am J Trop Med Hyg. 2005 Oct;73(4):783-9
pubmed: 16222026
Biol Reprod. 2014 Jun;90(6):129
pubmed: 24759787
BMC Infect Dis. 2016 Feb 13;16:78
pubmed: 26874788
Struct Equ Modeling. 2018;25(1):121-136
pubmed: 29910595
Curr Probl Pediatr Adolesc Health Care. 2015 Nov;45(11):325-64
pubmed: 26476880
Int J Gynaecol Obstet. 2015 Jun;129(3):199-202
pubmed: 25733444
PLoS Negl Trop Dis. 2018 Jan 12;12(1):e0005523
pubmed: 29329288
Biol Psychiatry. 2018 Jan 15;83(2):109-119
pubmed: 28754515
Neurosci Biobehav Rev. 2009 Jul;33(7):1061-79
pubmed: 19442688
Am J Trop Med Hyg. 2012 Sep;87(3):418-24
pubmed: 22826498
Psychiatry Res. 2017 Nov;257:102-110
pubmed: 28750213
Transl Psychiatry. 2014 Feb 18;4:e363
pubmed: 24548878
Afr Health Sci. 2018 Sep;18(3):542-551
pubmed: 30602986
PLoS One. 2013 Sep 18;8(9):e74643
pubmed: 24058614
Am J Trop Med Hyg. 2013 Feb;88(2):292-300
pubmed: 23296448
Pediatrics. 2012 Nov;130(5):e1326-44
pubmed: 23118140
J Psychiatr Res. 2019 Apr;111:96-103
pubmed: 30690329
PLoS Med. 2012 Jan;9(1):e1001162
pubmed: 22291577
J Int Neuropsychol Soc. 2012 Nov;18(6):1019-30
pubmed: 23158229
Pan Afr Med J. 2017 Jun 06;27:88
pubmed: 28819509
Neurotoxicol Teratol. 2004 May-Jun;26(3):359-71
pubmed: 15113598
Eur Child Adolesc Psychiatry. 2016 Dec;25(12):1361-1367
pubmed: 27165339
Lancet. 2006 May 6;367(9521):1521-32
pubmed: 16679166
Parasit Vectors. 2014 Jan 21;7:37
pubmed: 24447578
J Neurosci. 2007 Oct 3;27(40):10695-702
pubmed: 17913903
Am J Clin Nutr. 2001 Dec;74(6):814-26
pubmed: 11722965
J Parasitol Res. 2015;2015:641602
pubmed: 26161265
Am J Trop Med Hyg. 2016 Oct 5;95(4):856-863
pubmed: 27573634
PLoS One. 2019 May 2;14(5):e0216468
pubmed: 31048855
PLoS Negl Trop Dis. 2015 Mar 10;9(3):e0003463
pubmed: 25756357
Brain Res Bull. 2019 Feb;145:129-135
pubmed: 29630997
Parasit Vectors. 2018 Jan 31;11(1):65
pubmed: 29382360
PLoS Med. 2019 Oct 1;16(10):e1002914
pubmed: 31574087
Am J Hum Biol. 2020 Mar;32(2):e23337
pubmed: 31642576
Int J Dev Neurosci. 2005 Apr-May;23(2-3):299-305
pubmed: 15749254
PLoS Negl Trop Dis. 2018 Dec 6;12(12):e0006758
pubmed: 30522129
J Pediatr Infect Dis. 2018 Sep;13(3):185-201
pubmed: 30100780
J Child Psychol Psychiatry. 1997 Jul;38(5):581-6
pubmed: 9255702
Front Microbiol. 2019 Aug 22;10:1924
pubmed: 31507551
PLoS Med. 2014 Sep 23;11(9):e1001733
pubmed: 25247709
PLoS One. 2012;7(12):e50325
pubmed: 23236367
J Clin Invest. 2008 Apr;118(4):1311-21
pubmed: 18382743
Neurotoxicol Teratol. 2016 Sep - Oct;57:54-59
pubmed: 27343815
AIDS Care. 2020 Apr;32(4):411-419
pubmed: 31280587
BMC Infect Dis. 2016 Sep 30;16(1):530
pubmed: 27716099
J Autism Dev Disord. 2010 Dec;40(12):1423-30
pubmed: 20414802
Eur Child Adolesc Psychiatry. 2006 Aug;15(5):292-9
pubmed: 16583124