Parental autoimmune and autoinflammatory disorders as multiple risk factors for common neurodevelopmental disorders in offspring: a systematic review and meta-analysis.
Journal
Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664
Informations de publication
Date de publication:
18 03 2022
18 03 2022
Historique:
received:
06
09
2021
accepted:
07
02
2022
revised:
04
02
2022
entrez:
19
3
2022
pubmed:
20
3
2022
medline:
5
4
2022
Statut:
epublish
Résumé
Epidemiological studies have raised concerns about the risk of neurodevelopmental disorders (NDD) in children of patients with autoimmune or inflammatory disorders (AID). The pathophysiological pathways underlying this association are still unknown and little is known about the specific and distinct risk of each AID. To explore these questions, we investigated the association between the occurrences of several NDD in the offspring of mothers or fathers with different IDA. We conducted a meta-analysis-PROSPERO (CRD42020159250)-examining the risk of NDD in the offspring of mothers or fathers with AID. We performed specific analyses separately in fathers or mothers of NDD patients as well as subgroup analyses for each NDD and AID. We searched MEDLINE, Embase, PsycINFO, Cochrane Central Register of Controlled Trials, and Web of Science Core Collection published until December 2021. From an initial pool of 2074 potentially relevant references, 14 studies were included, involving more than 1,400,000 AID and 10,000,000 control parents, 180,000 children with NDD and more than 14,000,000 control children. We found AID in mothers (Adjusted OR 1.27 [95% CI 1.03; 1.57] p = 0.02, [I
Identifiants
pubmed: 35304436
doi: 10.1038/s41398-022-01843-y
pii: 10.1038/s41398-022-01843-y
pmc: PMC8933391
doi:
Types de publication
Meta-Analysis
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
112Informations de copyright
© 2022. The Author(s).
Références
Thapar A, Cooper M, Rutter M. Neurodevelopmental disorders. Lancet Psychiatry. 2017;4:339–46.
pubmed: 27979720
doi: 10.1016/S2215-0366(16)30376-5
Diagnostic and statistical manual of mental disorders: DSM-5. 5th edn. Washington: American psychiatric association; 2013.
Lichtenstein P, Carlström E, Råstam M, Gillberg C, Anckarsäter H. The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. Am J Psychiatry. 2010;167:1357–63.
pubmed: 20686188
doi: 10.1176/appi.ajp.2010.10020223
Thapar A, Cooper M. Attention deficit hyperactivity disorder. Lancet Lond Engl. 2016;387:1240–50.
doi: 10.1016/S0140-6736(15)00238-X
Lord C, Elsabbagh M, Baird G, Veenstra-Vanderweele J. Autism spectrum disorder. Lancet Lond Engl. 2018;392:508–20.
doi: 10.1016/S0140-6736(18)31129-2
Robertson MM, Eapen V, Singer HS, Martino D, Scharf JM, Paschou P, et al. Gilles de la Tourette syndrome. Nat Rev Dis Prim. 2017;3:16097.
pubmed: 28150698
doi: 10.1038/nrdp.2016.97
Stein DJ, Costa DLC, Lochner C, Miguel EC, Reddy YCJ, Shavitt RG, et al. Obsessive-compulsive disorder. Nat Rev Dis Prim. 2019;5:52.
pubmed: 31371720
doi: 10.1038/s41572-019-0102-3
Gustavson K, Ask H, Ystrom E, Stoltenberg C, Lipkin WI, Surén P, et al. Maternal fever during pregnancy and offspring attention deficit hyperactivity disorder. Sci Rep. 2019;9:9519.
pubmed: 31266998
pmcid: 6606630
doi: 10.1038/s41598-019-45920-7
Croen LA, Qian Y, Ashwood P, Zerbo O, Schendel D, Pinto-Martin J, et al. Infection and fever in pregnancy and autism spectrum disorders: findings from the study to explore early development. Autism Res J Int Soc Autism Res. 2019;12:1551–61.
doi: 10.1002/aur.2175
Atladóttir HÓ, Henriksen TB, Schendel DE, Parner ET. Autism after infection, febrile episodes, and antibiotic use during pregnancy: an exploratory study. Pediatrics. 2012;130:e1447–1454.
pubmed: 23147969
doi: 10.1542/peds.2012-1107
Smith SEP, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci. 2007;27:10695–702.
pubmed: 17913903
pmcid: 2387067
doi: 10.1523/JNEUROSCI.2178-07.2007
Wu W-L, Hsiao EY, Yan Z, Mazmanian SK, Patterson PH. The placental interleukin-6 signaling controls fetal brain development and behavior. Brain Behav Immun. 2017;62:11–23.
pubmed: 27838335
doi: 10.1016/j.bbi.2016.11.007
Rudolph MD, Graham AM, Feczko E, Miranda-Dominguez O, Rasmussen JM, Nardos R, et al. Maternal IL-6 during pregnancy can be estimated from newborn brain connectivity and predicts future working memory in offspring. Nat Neurosci. 2018;21:765–72.
pubmed: 29632361
pmcid: 5920734
doi: 10.1038/s41593-018-0128-y
Wang L, Wang F-S, Gershwin ME. Human autoimmune diseases: a comprehensive update. J Intern Med. 2015;278:369–95.
pubmed: 26212387
doi: 10.1111/joim.12395
Bennabi M, Gaman A, Delorme R, Boukouaci W, Manier C, Scheid I, et al. HLA-class II haplotypes and autism spectrum disorders. Sci Rep. 2018;8:7639.
pubmed: 29769579
pmcid: 5955937
doi: 10.1038/s41598-018-25974-9
Dendrou CA, Petersen J, Rossjohn J, Fugger L. HLA variation and disease. Nat Rev Immunol. 2018;18:325–39.
pubmed: 29292391
doi: 10.1038/nri.2017.143
Wu S, Ding Y, Wu F, Li R, Xie G, Hou J, et al. Family history of autoimmune diseases is associated with an increased risk of autism in children: a systematic review and meta-analysis. Neurosci Biobehav Rev. 2015;55:322–32.
pubmed: 25981892
doi: 10.1016/j.neubiorev.2015.05.004
Chen S-W, Zhong X-S, Jiang L-N, Zheng X-Y, Xiong Y-Q, Ma S-J, et al. Maternal autoimmune diseases and the risk of autism spectrum disorders in offspring: A systematic review and meta-analysis. Behav Brain Res. 2016;296:61–69.
pubmed: 26327239
doi: 10.1016/j.bbr.2015.08.035
Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.
pubmed: 19622551
pmcid: 2714657
doi: 10.1136/bmj.b2535
Eurofever Project—Home. 2021. https://www.printo.it/eurofever/index . Accessed 19 February 2021.
Autoimmune Disease List. AARDA. AARDA. 2016. https://www.aarda.org/diseaselist/ . Accessed 19 February 2021.
Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25:603–5.
pubmed: 20652370
doi: 10.1007/s10654-010-9491-z
Cullen AE, Holmes S, Pollak TA, Blackman G, Joyce DW, Kempton MJ, et al. Associations between non-neurological autoimmune disorders and psychosis: a meta-analysis. Biol Psychiatry. 2019;85:35–48.
pubmed: 30122288
pmcid: 6269125
doi: 10.1016/j.biopsych.2018.06.016
Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.
pubmed: 12958120
pmcid: 192859
doi: 10.1136/bmj.327.7414.557
Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol. 2008;61:991–6.
pubmed: 18538991
doi: 10.1016/j.jclinepi.2007.11.010
Egger M, Smith GD, Phillips AN. Meta-analysis: principles and procedures. BMJ. 1997;315:1533–7.
pubmed: 9432252
pmcid: 2127925
doi: 10.1136/bmj.315.7121.1533
Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA (editors). Cochrane Handbook forSystematic Reviews of Interventions. 2nd Edition. Chichester (UK): John Wiley & Sons, 2019.
Guido S. (PDF) meta: An R Package for Meta-Analysis. 2012. https://www.researchgate.net/publication/285729385_meta_An_R_Package_for_Meta-Analysis . Accessed 28 December 2018.
Ji J, Chen T, Sundquist J, Sundquist K. Type 1 diabetes in parents and risk of attention deficit/hyperactivity disorder in offspring: a population-based study in Sweden. Diabetes Care. 2018;41:770–4.
pubmed: 29374069
doi: 10.2337/dc17-0592
Rom AL, Wu CS, Olsen J, Jawaheer D, Hetland ML, Mørch LS. Parental rheumatoid arthritis and autism spectrum disorders in offspring: a Danish nationwide cohort study. J Am Acad Child Adolesc Psychiatry. 2018;57:28–32.e1.
pubmed: 29301665
doi: 10.1016/j.jaac.2017.10.002
Andersen ABT, Ehrenstein V, Erichsen R, Frøslev T, Sørensen HT. Autism spectrum disorders in children of parents with inflammatory bowel disease—a nationwide cohort study in Denmark. Clin Exp Gastroenterol. 2014;7:105–10.
pubmed: 24855384
pmcid: 4019630
doi: 10.2147/CEG.S59360
Comi AM, Zimmerman AW, Frye VH, Law PA, Peeden JN. Familial clustering of autoimmune disorders and evaluation of medical risk factors in autism. J Child Neurol. 1999;14:388–94.
pubmed: 10385847
doi: 10.1177/088307389901400608
Sweeten TL, Bowyer SL, Posey DJ, Halberstadt GM, McDougle CJ. Increased prevalence of familial autoimmunity in probands with pervasive developmental disorders. Pediatrics. 2003;112:e420.
pubmed: 14595086
doi: 10.1542/peds.112.5.e420
Mouridsen SE, Rich B, Isager T, Nedergaard NJ. Autoimmune diseases in parents of children with infantile autism: a case-control study. Dev Med Child Neurol. 2007;49:429–32.
pubmed: 17518928
doi: 10.1111/j.1469-8749.2007.00429.x
Atladóttir HO, Pedersen MG, Thorsen P, Mortensen PB, Deleuran B, Eaton WW, et al. Association of family history of autoimmune diseases and autism spectrum disorders. Pediatrics. 2009;124:687–94.
pubmed: 19581261
doi: 10.1542/peds.2008-2445
Keil A, Daniels JL, Forssen U, Hultman C, Cnattingius S, Söderberg KC, et al. Parental autoimmune diseases associated with autism spectrum disorders in offspring. Epidemiol Camb Mass. 2010;21:805–8.
doi: 10.1097/EDE.0b013e3181f26e3f
Nielsen PR, Benros ME, Dalsgaard S. Associations between autoimmune diseases and attention-deficit/hyperactivity disorder: a nationwide study. J Am Acad Child Adolesc Psychiatry. 2017;56:234–.e1.
pubmed: 28219489
doi: 10.1016/j.jaac.2016.12.010
Mataix-Cols D, Frans E, Pérez-Vigil A, Kuja-Halkola R, Gromark C, Isomura K, et al. A total-population multigenerational family clustering study of autoimmune diseases in obsessive-compulsive disorder and Tourette’s/chronic tic disorders. Mol Psychiatry. 2018;23:1652–8.
pubmed: 29133949
doi: 10.1038/mp.2017.215
Croen LA, Qian Y, Ashwood P, Daniels JL, Fallin D, Schendel D, et al. Family history of immune conditions and autism spectrum and developmental disorders: findings from the study to explore early development. Autism Res J Int Soc Autism Res. 2019;12:123–35.
doi: 10.1002/aur.1979
Spann MN, Timonen-Soivio L, Suominen A, Cheslack-Postava K, McKeague IW, Sourander A, et al. Proband and familial autoimmune diseases are associated with proband diagnosis of autism spectrum disorders. J Am Acad Child Adolesc Psychiatry. 2019;58:496–505.
pubmed: 30975444
pmcid: 6631342
doi: 10.1016/j.jaac.2018.09.444
Hegvik T-A, Chen Q, Kuja-Halkola R, Klungsøyr K, Butwicka A, Lichtenstein P, et al. Familial co-aggregation of attention-deficit/hyperactivity disorder and autoimmune diseases: a cohort study based on Swedish population-wide registers. Int J Epidemiol. 2021:dyab151.
Lee H, Hsu J-W, Tsai S-J, Huang K-L, Bai Y-M, Su T-P, et al. Risk of attention deficit hyperactivity and autism spectrum disorders among the children of parents with autoimmune diseases: a nationwide birth cohort study. Eur Child Adolesc Psychiatry. 2021. https://doi.org/10.1007/s00787-021-01860-0 .
Khan MF, Wang H. Environmental exposures and autoimmune diseases: contribution of gut microbiome. Front Immunol. 2019;10:3094.
pubmed: 31998327
doi: 10.3389/fimmu.2019.03094
Shelton JF, Geraghty EM, Tancredi DJ, Delwiche LD, Schmidt RJ, Ritz B, et al. Neurodevelopmental disorders and prenatal residential proximity to agricultural pesticides: the CHARGE study. Environ Health Perspect. 2014;122:1103–9.
pubmed: 24954055
pmcid: 4181917
doi: 10.1289/ehp.1307044
von Ehrenstein OS, Ling C, Cui X, Cockburn M, Park AS, Yu F, et al. Prenatal and infant exposure to ambient pesticides and autism spectrum disorder in children: population based case-control study. BMJ. 2019;364:l962.
doi: 10.1136/bmj.l962
Minatoya M, Araki A, Itoh S, Yamazaki K, Kobayashi S, Miyashita C, et al. Prenatal tobacco exposure and ADHD symptoms at pre-school age: the Hokkaido Study on Environment and Children’s Health. Environ Health Prev Med. 2019;24:74.
pubmed: 31812162
pmcid: 6898952
doi: 10.1186/s12199-019-0834-4
Kim B, Ha M, Kim YS, Koh Y-J, Dong S, Kwon H-J, et al. Prenatal exposure to paternal smoking and likelihood for autism spectrum disorder. Autism Int J Res Pract. 2021;25:1946–59.
doi: 10.1177/13623613211007319
Altink ME, Slaats-Willemse DIE, Rommelse NNJ, Buschgens CJM, Fliers EA, Arias-Vásquez A, et al. Effects of maternal and paternal smoking on attentional control in children with and without ADHD. Eur Child Adolesc Psychiatry. 2009;18:465–75.
pubmed: 19288168
pmcid: 2718195
doi: 10.1007/s00787-009-0001-3
Zengeler KE, Lukens JR. Innate immunity at the crossroads of healthy brain maturation and neurodevelopmental disorders. Nat Rev Immunol. 2021;21:454–68.
pubmed: 33479477
doi: 10.1038/s41577-020-00487-7
Katsarou A, Gudbjörnsdottir S, Rawshani A, Dabelea D, Bonifacio E, Anderson BJ, et al. Type 1 diabetes mellitus. Nat Rev Dis Primer. 2017;3:1–17.
Johnson WG, Buyske S, Mars AE, Sreenath M, Stenroos ES, Williams TA, et al. HLA-DR4 as a risk allele for autism acting in mothers of probands possibly during pregnancy. Arch Pediatr Adolesc Med. 2009;163:542–6.
pubmed: 19487610
doi: 10.1001/archpediatrics.2009.74
Lee L-C, Zachary AA, Leffell MS, Newschaffer CJ, Matteson KJ, Tyler JD, et al. HLA-DR4 in families with autism. Pediatr Neurol. 2006;35:303–7.
pubmed: 17074598
doi: 10.1016/j.pediatrneurol.2006.06.006
Tong J, Furukawa Y, Sherwin A, Hornykiewicz O, Kish SJ. Heterogeneous intrastriatal pattern of proteins regulating axon growth in normal adult human brain. Neurobiol Dis. 2011;41:458–68.
pubmed: 21029775
doi: 10.1016/j.nbd.2010.10.017
Hendrickx DAE, van Eden CG, Schuurman KG, Hamann J, Huitinga I. Staining of HLA-DR, Iba1 and CD68 in human microglia reveals partially overlapping expression depending on cellular morphology and pathology. J Neuroimmunol. 2017;309:12–22.
pubmed: 28601280
doi: 10.1016/j.jneuroim.2017.04.007
Enz LS, Zeis T, Schmid D, Geier F, van der Meer F, Steiner G, et al. Increased HLA-DR expression and cortical demyelination in MS links with HLA-DR15. Neurol Neuroimmunol Neuroinflammation. 2020;7.
Sharp SA, Weedon MN, Hagopian WA, Oram RA. Clinical and research uses of genetic risk scores in type 1 diabetes. Curr Opin Genet Dev. 2018;50:96–102.
pubmed: 29702327
pmcid: 6089633
doi: 10.1016/j.gde.2018.03.009
Leppert B, Havdahl A, Riglin L, Jones HJ, Zheng J, Davey Smith G, et al. Association of maternal neurodevelopmental risk alleles with early-life exposures. JAMA Psychiatry. 2019;76:834–42.
pubmed: 31042271
pmcid: 6495368
doi: 10.1001/jamapsychiatry.2019.0774
Nordsletten AE, Larsson H, Crowley JJ, Almqvist C, Lichtenstein P, Mataix-Cols D. Patterns of nonrandom mating within and across 11 major psychiatric disorders. JAMA Psychiatry. 2016;73:354–61.
pubmed: 26913486
pmcid: 5082975
doi: 10.1001/jamapsychiatry.2015.3192
Meyer U. Neurodevelopmental resilience and susceptibility to maternal immune activation. Trends Neurosci. 2019. https://doi.org/10.1016/j.tins.2019.08.001 .
Choi GB, Yim YS, Wong H, Kim S, Kim H, Kim SV, et al. The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science. 2016;351:933–9.
pubmed: 26822608
pmcid: 4782964
doi: 10.1126/science.aad0314
Kim S, Kim H, Yim YS, Ha S, Atarashi K, Tan TG, et al. Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature. 2017;549:528–32.
pubmed: 28902840
pmcid: 5870873
doi: 10.1038/nature23910
Tsai PT, Greene-Colozzi E, Goto J, Anderl S, Kwiatkowski DJ, Sahin M. Prenatal rapamycin results in early and late behavioral abnormalities in wildtype C57BL/6 mice. Behav Genet. 2013;43:51–59.
pubmed: 23229624
doi: 10.1007/s10519-012-9571-9
Coscia LA, Constantinescu S, Davison JM, Moritz MJ, Armenti VT. Immunosuppressive drugs and fetal outcome. Best Pract Res Clin Obstet Gynaecol. 2014;28:1174–87.
pubmed: 25175414
doi: 10.1016/j.bpobgyn.2014.07.020
Motta M, Tincani A, Meroni PL, Cimaz R. Follow-up of children exposed antenatally to immunosuppressive drugs. Rheumatol Oxf Engl. 2008;47:iii32–34.
doi: 10.1093/rheumatology/ken149
Nulman I, Sgro M, Barrera M, Chitayat D, Cairney J, Koren G. Long-term neurodevelopment of children exposed in utero to ciclosporin after maternal renal transplant. Paediatr Drugs. 2010;12:113–22.
pubmed: 20095652
doi: 10.2165/11316280-000000000-00000