The purpose of this study was to explore whether prenatal gut microbiota (GM) and its functions predict the development of offspring temperament. A total of 53 mothers with a 1-year-old child and 41 mothers with a 2-year-old child were included in this study using a mother-infant cohort from central China. Maternal fecal samples collected during the third trimester were analyzed using 16S rRNA V3-V4 gene sequences. Temperament of the child was measured by self-reported data according to the primary caregiver. The effects of GM in mothers on offspring’s temperament were evaluated using multiple linear regression models. The results demonstrated that the alpha diversity index Simpson of prenatal GM was positively associated with the activity level of offspring at 1 year (adj. P = .036). Bifidobacterium was positively associated with high-intensity pleasure characteristics of offspring at 1 year (adj. P = .031). Comparatively, the presence of Bifidobacterium found in the prenatal microbiome was associated with low-intensity pleasure characteristics in offspring at 2 years (adj. P = .031). There were many significant associations noted among the functional pathways of prenatal GM and temperament of offspring at 2 years. Our findings support the maternal-fetal GM axis in the setting of fetal-placental development with subsequent postnatal neurocognitive developmental outcomes, and suggest that early childhood temperament is in part associated with specific GM in the prenatal setting.
AatsinkiA. K.LahtiL.UusitupaH. M.MunukkaE.KeskitaloA.NolviS.O’MahonyS.PietiläS.EloL. L.EerolaE.KarlssonH.KarlssonL. (2019). Gut microbiota composition is associated with temperament traits in infants. Brain, Behavior, and Immunity, 80, 849–858. https://doi.org/10.1016/j.bbi.2019.05.035
2.
AokiR.OnukiM.HattoriK.ItoM.YamadaT.KamikadoK.KimY. G.NakamotoN.KimuraI.ClarkeJ. M.KanaiT.HaseK. (2021). Commensal microbe-derived acetate suppresses NAFLD/NASH development via hepatic FFAR2 signalling in mice. Microbiome, 9(1), 188. https://doi.org/10.1186/s40168-021-01125-7
BhardwajR. D.CurtisM. A.SpaldingK. L.BuchholzB. A.FinkD.Björk-ErikssonT.NordborgC.GageF. H.DruidH.ErikssonP. S.FrisénJ. (2006). Neocortical neurogenesis in humans is restricted to development. Proceedings of the National Academy of Sciences of the United States of America, 103(33), 12564–12568. https://doi.org/10.1073/pnas.0605177103
6.
BiT.ZhangL.ZhanL.FengR.ZhaoT.RenW.HangT.ZhouW.LuX. (2022). Integrated analyses of microbiomics and metabolomics explore the effect of gut microbiota transplantation on diabetes-associated cognitive decline in zucker diabetic fatty rats. Frontiers in Aging Neuroscience, 14, 913002. https://doi.org/10.3389/fnagi.2022.913002
7.
BufferdS. J.LevinsonC. A.OlinoT. M.DoughertyL. R.DysonM. W.CarlsonG. A.KleinD. N. (2022). Temperament and psychopathology in early childhood predict body dissatisfaction and eating disorder symptoms in adolescence. Behaviour Research and Therapy, 151, 104039. https://doi.org/10.1016/j.brat.2022.104039
8.
BuffingtonS. A.Di PriscoG. V.AuchtungT. A.AjamiN. J.PetrosinoJ. F.Costa-MattioliM. (2016). Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell, 165(7), 1762–1775. https://doi.org/10.1016/j.cell.2016.06.001
9.
ChetcutiL.UljarevićM.Ellis-DaviesK.HardanA. Y.WhitehouseA. J. O.HedleyD.PutnamS.HudryK.PriorM. R. (2021). Temperament in individuals with autism spectrum disorder: A systematic review. Clinical Psychology Review, 85, 101984. https://doi.org/10.1016/j.cpr.2021.101984
10.
ChristianL. M.GalleyJ. D.HadeE. M.Schoppe-SullivanS.Kamp DushC.BaileyM. T. (2015). Gut microbiome composition is associated with temperament during early childhood. Brain, Behavior, and Immunity, 45, 118–127. https://doi.org/10.1016/j.bbi.2014.10.018
11.
CowanC. S. M.DinanT. G.CryanJ. F. (2020). Annual research review: Critical windows - the microbiota-gut-brain axis in neurocognitive development. The Journal of Child Psychology and Psychiatry and Allied Disciplines, 61(3), 353–371. https://doi.org/10.1111/jcpp.13156
12.
CryanJ. F.DinanT. G. (2012). Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nature Reviews Neuroscience, 13(10), 701–712. https://doi.org/10.1038/nrn3346
13.
CurranE. A.O’NeillS. M.CryanJ. F.KennyL. C.DinanT. G.KhashanA. S.KearneyP. M. (2015). Research review: Birth by caesarean section and development of autism spectrum disorder and attention-deficit/hyperactivity disorder: A systematic review and meta-analysis. The Journal of Child Psychology and Psychiatry and Allied Disciplines, 56(5), 500–508. https://doi.org/10.1111/jcpp.12351
De FilippisF.PasolliE.ErcoliniD. (2020). Newly explored Faecalibacterium diversity is connected to age, lifestyle, geography, and disease. Current Biology: CB, 30(24), 4932–4943.e4. https://doi.org/10.1016/j.cub.2020.09.063
16.
DingsdaleH.GarayS. M.TysonH. R.SavoryK. A.SumptionL. A.KelleherJ. S.LangleyK.Van GoozenS.JohnR. M. (2022). Cord serum brain-derived neurotrophic factor levels at birth associate with temperament outcomes at one year. Journal of Psychiatric Research, 150, 47–53. https://doi.org/10.1016/j.jpsychires.2022.03.009
17.
EicherT. P.MohajeriM. H. (2022). Overlapping mechanisms of action of brain-active bacteria and bacterial metabolites in the pathogenesis of common brain diseases. Nutrients, 14(13), 2661. https://doi.org/10.3390/nu14132661
18.
EinzigerT.LeviL.Zilberman-HayunY.AuerbachJ. G.Atzaba-PoriaN.ArbelleS.BergerA. (2018). Predicting ADHD symptoms in adolescence from early childhood temperament traits. Journal of Abnormal Child Psychology, 46(2), 265–276. https://doi.org/10.1007/s10802-017-0287-4
19.
FoxM.LeeS. M.WileyK. S.LagishettyV.SandmanC. A.JacobsJ. P.GlynnL. M. (2022). Development of the infant gut microbiome predicts temperament across the first year of life. Development and Psychopathology, 34, 1–12. https://doi.org/10.1017/S0954579421000456
20.
GagneJ. R.GoldsmithH. H. (2020). Development of temperament in infancy and childhood. In SaudinoK. J.GanibanJ. M. (Eds.), Behavior genetics of temperament and personality (pp. 3–39). Springer.
21.
GalleyJ. D.Mashburn-WarrenL.BlalockL. C.LauberC. L.CarrollJ. E.RossK. M.HobelC.Coussons-ReadM.Dunkel SchetterC.GurT. L. (2023). Maternal anxiety, depression and stress affects offspring gut microbiome diversity and bifidobacterial abundances. Brain, Behavior, and Immunity, 107, 253–264. https://doi.org/10.1016/j.bbi.2022.10.005
22.
GartsteinM. A.RothbartM. K. (2003). Studying infant temperament via the revised infant behavior questionnaire. Infant Behavior and Development, 26(1), 64–86. https://doi.org/10.1016/s0163-6383(02)00169-8
23.
GuoC.WangY.ZhangS.ZhangX.DuZ.LiM.DingK. (2021). Crataegus pinnatifida polysaccharide alleviates colitis via modulation of gut microbiota and SCFAs metabolism. International Journal of Biological Macromolecules, 181, 357–368. https://doi.org/10.1016/j.ijbiomac.2021.03.137
24.
GustafssonH. C.NolviS.SullivanE. L.RasmussenJ. M.GyllenhammerL. E.EntringerS.WadhwaP. D.O'ConnorT. G.KarlssonL.KarlssonH.KorjaR.BussC.GrahamA. M.NiggJ. T. (2021). Early development of negative and positive affect: Implications for ADHD symptomatology across three birth cohorts. Development and Psychopathology, 33(5), 1837–1848. https://doi.org/10.1017/s0954579421001012
25.
GuzzardiM. A.EderveenT. H. A.RizzoF.WeiszA.ColladoM. C.MuratoriF.GrossG.AlkemaW.IozzoP. (2022). Maternal pre-pregnancy overweight and neonatal gut bacterial colonization are associated with cognitive development and gut microbiota composition in pre-school-age offspring. Brain, Behavior, and Immunity, 100, 311–320. https://doi.org/10.1016/j.bbi.2021.12.009
26.
HanfordL. C.SchmithorstV. J.PanigrahyA.LeeV.RidleyJ.BonarL.VersaceA.HipwellA. E.PhillipsM. L. (2018). The impact of caregiving on the association between infant emotional behavior and resting state neural network functional topology. Frontiers in Psychology, 9, 1968. https://doi.org/10.3389/fpsyg.2018.01968
27.
HaydenE. P.KleinD. N.DurbinC. E.OlinoT. M. (2006). Positive emotionality at age 3 predicts cognitive styles in 7-year-old children. Development and Psychopathology, 18(2), 409–423. https://doi.org/10.1017/S0954579406060226
28.
HoppeM. M.SundarR.TanD. S. P.JeyasekharanA. D. (2018). Biomarkers for homologous recombination deficiency in cancer. Journal of the National Cancer Institute, 110(7), 704–713. https://doi.org/10.1093/jnci/djy085
29.
HuangL.DuanC.XiaX.WangH.WangY.ZhongZ.WangB.DingW.YangY. (2021). Commensal microbe-derived propionic acid mediates juvenile social isolation-induced social deficits and anxiety-like behaviors. Brain Research Bulletin, 166, 161–171. https://doi.org/10.1016/j.brainresbull.2020.12.001
30.
JiangH. Y.ZhouY. Y.ZhouG. L.LiY. C.YuanJ.LiX. H.RuanB. (2018). Gut microbiota profiles in treatment-naïve children with attention deficit hyperactivity disorder. Behavioural Brain Research, 347, 408–413. https://doi.org/10.1016/j.bbr.2018.03.036
31.
JosephH. M.LorenzoN. E.FisherN.NovickD. R.GibsonC.RothenbergerS. D.FoustJ. E.Chronis-TuscanoA. (2023). Research review: A systematic review and meta-analysis of infant and toddler temperament as predictors of childhood attention-deficit/hyperactivity disorder. The Journal of Child Psychology and Psychiatry and Allied Disciplines, 64(5), 715–735. https://doi.org/10.1111/jcpp.13753
32.
KaiserR. H.Andrews-HannaJ. R.WagerT. D.PizzagalliD. A. (2015). Large-scale network dysfunction in major depressive disorder: A meta-analysis of resting-state functional connectivity. JAMA Psychiatry, 72(6), 603–611. https://doi.org/10.1001/jamapsychiatry.2015.0071
33.
KarF.HaciogluC.KarE.DonmezD. B.KanbakG. (2022). Probiotics ameliorates LPS induced neuroinflammation injury on Aβ 1-42, APP, γ-β secretase and BDNF levels in maternal gut microbiota and fetal neurodevelopment processes. Metabolic Brain Disease, 37(5), 1387–1399. https://doi.org/10.1007/s11011-022-00964-z
34.
KelseyC. M.PrescottS.McCullochJ. A.TrinchieriG.ValladaresT. L.DreisbachC.AlhusenJ.GrossmannT. (2021). Gut microbiota composition is associated with newborn functional brain connectivity and behavioral temperament. Brain, Behavior, and Immunity, 91, 472–486. https://doi.org/10.1016/j.bbi.2020.11.003
35.
KimS.KimH.YimY. S.HaS.AtarashiK.TanT. G.LongmanR. S.HondaK.LittmanD. R.ChoiG. B.HuhJ. R. (2017). Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature, 549(7673), 528–532. https://doi.org/10.1038/nature23910
36.
KoflerM. J.RapportM. D.SarverD. E.RaikerJ. S.OrbanS. A.FriedmanL. M.KolomeyerE. G. (2013). Reaction time variability in ADHD: A meta-analytic review of 319 studies. Clinical Psychology Review, 33(6), 795–811. https://doi.org/10.1016/j.cpr.2013.06.001
37.
KomsiN.RäikkönenK.PesonenA. K.HeinonenK.KeskivaaraP.JärvenpääA. L.StrandbergT. E. (2006). Continuity of temperament from infancy to middle childhood. Infant Behavior and Development, 29(4), 494–508. https://doi.org/10.1016/j.infbeh.2006.05.002
38.
KorenO.GoodrichJ. K.CullenderT. C.SporA.LaitinenK.BäckhedH. K.GonzalezA.WernerJ. J.AngenentL. T.KnightR.BäckhedF.IsolauriE.SalminenS.LeyR. E. (2012). Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell, 150(3), 470–480. https://doi.org/10.1016/j.cell.2012.07.008
39.
Kostyrka-AllchorneK.WassS. V.Sonuga-BarkeE. J. S. (2020). Research review: Do parent ratings of infant negative emotionality and self-regulation predict psychopathology in childhood and adolescence? A systematic review and meta-analysis of prospective longitudinal studies. The Journal of Child Psychology and Psychiatry and Allied Disciplines, 61(4), 401–416. https://doi.org/10.1111/jcpp.13144
40.
LebovitzY.KowalskiE. A.WangX.KellyC.LeeM.McDonaldV.WardR.CreaseyM.MillsW.Gudenschwager BassoE. K.HazyA.HrubecT.TheusM. H. (2019). Lactobacillus rescues postnatal neurobehavioral and microglial dysfunction in a model of maternal microbiome dysbiosis. Brain, Behavior, and Immunity, 81, 617–629. https://doi.org/10.1016/j.bbi.2019.07.025
41.
LeveL. D.DeGarmoD. S.BridgettD. J.NeiderhiserJ. M.ShawD. S.HaroldG. T.NatsuakiM. N.ReissD. (2013). Using an adoption design to separate genetic, prenatal, and temperament influences on toddler executive function. Developmental Psychology, 49(6), 1045–1057. https://doi.org/10.1037/a0029390
42.
LiF.FengY.LiuH.KongD.HsuehC. Y.ShiX.WuQ.LiW.WangJ.ZhangY.DaiC. (2022). Gut microbiome and metabolome changes in mice with acute vestibular deficit. Frontiers in Cellular and Infection Microbiology, 12, 821780. https://doi.org/10.3389/fcimb.2022.821780
43.
LiuC.MooreG. A.BeekmanC.Pérez-EdgarK. E.LeveL. D.ShawD. S.GanibanJ. M.NatsuakiM. N.ReissD.NeiderhiserJ. M. (2018). Developmental patterns of anger from infancy to middle childhood predict problem behaviors at age 8. Developmental Psychology, 54(11), 2090–2100. https://doi.org/10.1037/dev0000589
44.
LiuC.ZhengY.GanibanJ. M.SaudinoK. J. (2023). Genetic and environmental influences on temperament development across the preschool period. The Journal of Child Psychology and Psychiatry and Allied Disciplines, 64(1), 59–70. https://doi.org/10.1111/jcpp.13667
45.
MansfieldM. J.TremblayB. J.ZengJ.WeiX.HodginsH.WorleyJ.BryL.DongM.DoxeyA. C. (2020). Phylogenomics of 8,839 Clostridioides difficile genomes reveals recombination-driven evolution and diversification of toxin A and B. PLoS Pathogens, 16(12), Article e1009181. https://doi.org/10.1371/journal.ppat.1009181
46.
MartínR.Bermúdez-HumaránL. G.LangellaP. (2018). Searching for the bacterial effector: The example of the multi-skilled commensal bacterium Faecalibacterium prausnitzii. Frontiers in Microbiology, 9, 346. https://doi.org/10.3389/fmicb.2018.00346
47.
MaslowskiK. M.VieiraA. T.NgA.KranichJ.SierroF.YuD.SchilterH. C.RolphM. S.MackayF.ArtisD.XavierR. J.TeixeiraM. M.MackayC. R. (2009). Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature, 461(7268), 1282–1286. https://doi.org/10.1038/nature08530
48.
MassraliA.AdhyaD.SrivastavaD. P.Baron-CohenS.KotterM. R. (2022). Virus-induced maternal immune activation as an environmental factor in the etiology of autism and schizophrenia. Frontiers in Neuroscience, 16, 834058. https://doi.org/10.3389/fnins.2022.834058
49.
MitchellR. H.GoldsteinB. I. (2014). Inflammation in children and adolescents with neuropsychiatric disorders: A systematic review. Journal of the American Academy of Child and Adolescent Psychiatry, 53(3), 274–296. https://doi.org/10.1016/j.jaac.2013.11.013
50.
MurrayK. T.KochanskaG. (2002). Effortful control: Factor structure and relation to externalizing and internalizing behaviors. Journal of Abnormal Child Psychology, 30(5), 503–514. https://doi.org/10.1023/a:1019821031523
51.
PaulusF. W.MöhlerE.FestagL.JoasJ. (2022). Preschool temperament as a factor of risk and protection for later childhood psychopathology. Frontiers in Psychiatry, 13, 803959. https://doi.org/10.3389/fpsyt.2022.803959
PutnamS. P.GartsteinM. A.RothbartM. K. (2006). Measurement of fine-grained aspects of toddler temperament: The early childhood behavior questionnaire. Infant Behavior and Development, 29(3), 386–401. https://doi.org/10.1016/j.infbeh.2006.01.004
54.
QuévrainE.MaubertM. A.MichonC.ChainF.MarquantR.TailhadesJ.MiquelS.CarlierL.Bermúdez-HumaránL. G.PigneurB.LequinO.KharratP.ThomasG.RainteauD.AubryC.BreynerN.AfonsoC.LavielleS.GrillJ. P.SeksikP. (2016). Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut, 65(3), 415–425. https://doi.org/10.1136/gutjnl-2014-307649
RossiO.KhanM. T.SchwarzerM.HudcovicT.SrutkovaD.DuncanS. H.StolteE. H.KozakovaH.FlintH. J.SamsomJ. N.HarmsenH. J.WellsJ. M. (2015). Faecalibacterium prausnitzii strain HTF-F and its extracellular polymeric matrix attenuate clinical parameters in DSS-induced colitis. PLoS One, 10(4), Article e0123013. https://doi.org/10.1371/journal.pone.0123013
57.
RothbartM. K.EllisL. K.RuedaM. R.PosnerM. I. (2003). Developing mechanisms of temperamental effortful control. Journal of Personality, 71(6), 1113–1143. https://doi.org/10.1111/1467-6494.7106009
58.
SayalK.HeronJ.MaughanB.RoweR.RamchandaniP. (2014). Infant temperament and childhood psychiatric disorder: Longitudinal study. Child: Care, Health and Development, 40(2), 292–297. https://doi.org/10.1111/cch.12054
59.
TeerikangasO. M.AronenE. T.MartinR. P.HuttunenM. O. (1998). Effects of infant temperament and early intervention on the psychiatric symptoms of adolescents. Journal of the American Academy of Child and Adolescent Psychiatry, 37(10), 1070–1076. https://doi.org/10.1097/00004583-199810000-00017
60.
VatanenT.JabbarK. S.RuohtulaT.HonkanenJ.Avila-PachecoJ.SiljanderH.StražarM.OikarinenS.HyötyH.IlonenJ.MitchellC. M.YassourM.VirtanenS. M.ClishC. B.PlichtaD. R.VlamakisH.KnipM.XavierR. J. (2022). Mobile genetic elements from the maternal microbiome shape infant gut microbial assembly and metabolism. Cell, 185(26), 4921–4936.e15. https://doi.org/10.1016/j.cell.2022.11.023
61.
VijayakumarN.WhittleS.DennisonM.YücelM.SimmonsJ.AllenN. B. (2014). Development of temperamental effortful control mediates the relationship between maturation of the prefrontal cortex and psychopathology during adolescence: A 4-year longitudinal study. Developmental Cognitive Neuroscience, 9, 30–43. https://doi.org/10.1016/j.dcn.2013.12.002
62.
VuongH. E.PronovostG. N.WilliamsD. W.ColeyE. J. L.SieglerE. L.QiuA.KazantsevM.WilsonC. J.RendonT.HsiaoE. Y. (2020). The maternal microbiome modulates fetal neurodevelopment in mice. Nature, 586(7828), 281–286. https://doi.org/10.1038/s41586-020-2745-3
63.
WangH.BraunC.MurphyE. F.EnckP. (2019a). Bifidobacterium longum 1714™ strain modulates brain activity of healthy volunteers during social stress. American Journal of Gastroenterology, 114(7), 1152–1162. https://doi.org/10.14309/ajg.0000000000000203
64.
WangW.HaoZ.WuZ.CuiJ.LiuH. (2023). Long-term artificial/natural daytime light affects mood, melatonin, corticosterone, and gut microbiota in rats. Applied Microbiology and Biotechnology, 107(7–8), 2689–2705. https://doi.org/10.1007/s00253-023-12446-y
65.
WangY.ChenX.YuY.LiuY.ZhangQ.BaiJ. (2020). Association between gut microbiota and infant’s temperament in the first year of life in a Chinese birth cohort. Microorganisms, 8(5), 753. https://doi.org/10.3390/microorganisms8050753
66.
WangY.LiuY.BaiJ.ChenX. (2019b). The effect of maternal postpartum practices on infant gut microbiota: A Chinese cohort study. Microorganisms, 7(11), 511. https://doi.org/10.3390/microorganisms7110511
67.
WittigS. M. O.RodriguezC. M. (2019). Emerging behavior problems: Bidirectional relations between maternal and paternal parenting styles with infant temperament. Developmental Psychology, 55(6), 1199–1210. https://doi.org/10.1037/dev0000707
68.
WongM. L.InserraA.LewisM. D.MastronardiC. A.LeongL.ChooJ.KentishS.XieP.MorrisonM.WesselinghS. L.RogersG. B.LicinioJ. (2016). Inflammasome signaling affects anxiety- and depressive-like behavior and gut microbiome composition. Molecular Psychiatry, 21(6), 797–805. https://doi.org/10.1038/mp.2016.46
XieT.WangY.ZouZ.WuY.FanX.DaiJ.LiuY.BaiJ. (2022). Relationship between the gut microbiota and temperament in children 1-2 years old in Chinese birth cohort. Journal of Psychiatric Research, 148, 52–60. https://doi.org/10.1016/j.jpsychires.2022.01.041
71.
YassourM.JasonE.HogstromL. J.ArthurT. D.TripathiS.SiljanderH.SelveniusJ.OikarinenS.HyötyH.VirtanenS. M.IlonenJ.FerrettiP.PasolliE.TettA.AsnicarF.SegataN.VlamakisH.LanderE. S.HuttenhowerC.KnipM.XavierR. J. (2018). Strain-level analysis of mother-to-child bacterial transmission during the first few months of life. Cell Host & Microbe, 24(1), 146–154.e4. https://doi.org/10.1016/j.chom.2018.06.007
72.
YinH.WangZ.LiuJ.LiY.LiuL.HuangP.WangW.ShanZ.SunR.ShenJ.DuanL. (2023). Dysregulation of immune and metabolism pathways in maternal immune activation induces an increased risk of autism spectrum disorders. Life Sciences, 324, 121734. https://doi.org/10.1016/j.lfs.2023.121734
73.
YuX.JiangW.KosikR. O.SongY.LuoQ.QiaoT.TongJ.LiuS.DengC.QinS.LvZ.LiD. (2021). Gut microbiota changes and its potential relations with thyroid carcinoma. Journal of Advanced Research, 35, 61–70. https://doi.org/10.1016/j.jare.2021.04.001
74.
ZengY.NieC.MinJ.LiuX.LiM.ChenH.XuH.WangM.NiT.LiY.YanH.ZhangJ. P.SongC.ChiL. Q.WangH. M.DongJ.ZhengG. Y.LinL.QianF.VaupelJ. W. (2016). Novel loci and pathways significantly associated with longevity. Scientific Reports, 6, 21243. https://doi.org/10.1038/srep21243
75.
ZentnerM.BiedermannV.TafernerC.da CudanH.MöhlerE.StraußH.SeveckeK. (2021). Early detection of temperament risk factors: A comparison of clinically referred and general population children. Frontiers in Psychiatry, 12, 667503. https://doi.org/10.3389/fpsyt.2021.667503
76.
ZhangL.WongL. R.WongP.ShenW.YangS.HuangL.LimY. A.HoP. C. (2023). Chronic treatment with baicalein alleviates behavioural disorders and improves cerebral blood flow via reverting metabolic abnormalities in a J20 transgenic mouse model of alzheimer’s disease. Brain, Behavior, & Immunity - Health, 28, 100599. https://doi.org/10.1016/j.bbih.2023.100599
77.
ZhouL.ZhangM.WangY.DorfmanR. G.LiuH.YuT.ChenX.TangD.XuL.YinY.PanY.ZhouQ.ZhouY.YuC. (2018). Faecalibacterium prausnitzii produces butyrate to maintain Th17/Treg balance and to ameliorate colorectal colitis by inhibiting histone deacetylase 1. Inflammatory Bowel Diseases, 24(9), 1926–1940. https://doi.org/10.1093/ibd/izy182
78.
ZhuangZ.YangR.WangW.QiL.HuangT. (2020). Associations between gut microbiota and alzheimer’s disease, major depressive disorder, and schizophrenia. Journal of Neuroinflammation, 17(1), 288. https://doi.org/10.1186/s12974-020-01961-8
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