Association between Gut Microbiota and Infant’s Temperament in the First Year of Life in a Chinese Birth Cohort

Microorganisms - Tập 8 Số 5 - Trang 753
Ying Wang1, Xiaoli Chen1, Yun Yu1, Yanqun Liu1, Qing Zhang1, Jinbing Bai2
1School of Health sciences, Wuhan University, Wuhan 430071, China
2Nell Hodgson Woodruff School of Nursing, Emory University, Atlanta, GA, 30322, USA

Tóm tắt

Infant temperament characteristics play a critical role in children’s developmental pathways and can predict adulthood psychopathology. The diversity and composition of the gut microbiota are associated with human temperament in both adults and young children. However, the relationship between the gut microbiota and temperament in 12-month-old infants is rarely studied; this developmental period is when temperament reaches a relatively stable stage. We used high-throughput sequencing methods to explore whether temperament characteristics were associated with gut microbiota diversity and composition. Infants’ fecal samples were collected at 12 months of age for the gut microbiota analysis. Based on the primary caregivers’ reports, infants’ temperaments were measured using the Infant Behavior Questionnaire-revised (IBQ-R). This study included 51 infants, including 20 boys and 31 girls, with a mean age of 12.25 months. Results showed that soothability was positively correlated with maternal education level (β = 0.29, p = 0.043, adjust p = 0.025) and the abundance of Bifidobacterium genera (β = 0.62, p = 0.004, adjust p = 0.002). Conversely, cuddliness was negatively correlated with the abundance of Hungatella genera. There was no significant difference in temperament based on gender. This study demonstrated that gut microbiota composition was associated with temperament in 12-month-old infants. These results point to the importance of gut microbiota balance. Future studies on the mechanisms behind the gut microbiota affecting temperament are warranted.

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Tài liệu tham khảo

Rothbart, 1981, Measurement of Temperament in Infancy, Child Dev., 52, 569, 10.2307/1129176

Gartstein, 2003, Studying infant temperament via the Revised Infant Behavior Questionnaire, Infant Behav. Dev., 26, 64, 10.1016/S0163-6383(02)00169-8

Cozzi, 2013, Studying cross-cultural differences in temperament in toddlerhood: United States of America (US) and Italy, Infant Behav. Dev., 36, 480, 10.1016/j.infbeh.2013.03.014

Enlow, 2016, The Infant Behavior Questionnaire-Revised: Factor structure in a culturally and sociodemographically diverse sample in the United States, Infant Behav. Dev., 43, 24, 10.1016/j.infbeh.2016.04.001

de Lauzon-Guillain, B., Wijndaele, K., Clark, M., Acerini, C.L., Hughes, I.A., Dunger, D.B., Wells, J.C., and Ong, K.K. (2012). Breastfeeding and Infant Temperament at Age Three Months. PLoS ONE, 7.

Gartstein, 2006, Studying Cross-cultural Differences in the Development of Infant Temperament: People’s Republic of China, the United States of America, and Spain, Child Psychiatry Hum. Dev., 37, 145, 10.1007/s10578-006-0025-6

Gartstein, 2015, Stability of temperament in South Korean infants from 6 to 12 to 18 months: Moderation by age, gender, and birth order, Infant Behav. Dev., 40, 103, 10.1016/j.infbeh.2015.05.002

Turkheimer, 2000, Nonshared environment: A theoretical, methodological, and quantitative review, Psychol. Bull., 126, 78, 10.1037/0033-2909.126.1.78

Keightley, 2015, Gut feelings 1. Mind, mood and gut in irritable bowel syndrome: Approaches to psychiatric care, Australas. Psychiatry, 23, 403, 10.1177/1039856215590033

Keightley, 2015, Gut feelings 2. Mind, mood and gut in inflammatory bowel disease: Approaches to psychiatric care, Australas. Psychiatry, 23, 407, 10.1177/1039856215590034

Dinan, 2017, The Microbiome-Gut-Brain Axis in Health and Disease, Gastroenterol. Clin. N. Am., 46, 77, 10.1016/j.gtc.2016.09.007

Kennedy, P.J., Cryan, J.F., Dinan, T.G., and Clarke, G. (2016). Kynurenine pathway metabolism and the microbiota-gut-brain axis. Neuropharmacology.

Foster, 2014, Gut-brain axis: How the microbiome influences anxiety and depression, Int. J. Neuropsychopharmacol., 17, 27

Steenbergen, 2015, A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood, Brain Behav. Immun., 48, 258, 10.1016/j.bbi.2015.04.003

Messaoudi, 2011, Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers, Gut Microbes, 2, 256, 10.4161/gmic.2.4.16108

Hsiao, 2013, Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders, Cell, 155, 1451, 10.1016/j.cell.2013.11.024

Tillisch, 2013, Consumption of fermented milk product with probiotic modulates brain activity, Gastroenterology, 144, 1394, 10.1053/j.gastro.2013.02.043

Gao, W., Salzwedel, A.P., Carlson, A.L., Xia, K., Azcarate-Peril, M.A., Styner, M.A., Thompson, A.L., Geng, X., Goldman, B.D., and Gilmore, J.H. (2019). Gut microbiome and brain functional connectivity in infants-a preliminary study focusing on the amygdala. Psychopharmacology.

Kim, 2017, The Association between Temperament and Microbiota in Healthy Individuals: A Pilot Study, Psychosom. Med., 79, 898, 10.1097/PSY.0000000000000459

Christian, 2015, Gut microbiome composition is associated with temperament during early childhood, Brain Behav. Immun., 45, 118, 10.1016/j.bbi.2014.10.018

Putnam, 2008, Homotypic and heterotypic continuity of fine-grained temperament during infancy, toddlerhood, and early childhood, Infant Child Dev., 17, 387, 10.1002/icd.582

Li, Y., Faden, H.S., and Zhu, L. (2020). The Response of the Gut Microbiota to Dietary Changes in the First Two Years of Life. Front. Pharmacol., 11.

Wang, Y., Liu, Y., Bai, J., and Chen, X. (2019). The Effect of Maternal Postpartum Practices on Infant Gut Microbiota: A Chinese Cohort Study. Microorganisms, 7.

Yu, 2017, Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer, Gut, 66, 70, 10.1136/gutjnl-2015-309800

R Core Team (2019). A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Available online: https://www.R-project.org/.

Lerner, R.M. (2015). Handbook of Child Psychology and Developmental Science, WILEY.

Coll, 1992, Stability and Correlates of Change of Early Temperament in Preterm and Full-Term Infants, Infant Behav. Dev., 15, 137, 10.1016/0163-6383(92)80020-U

Fuller, 2010, Commands, competence, and carino: Maternal socialization practices in Mexican American families, Dev. Psychol., 46, 566, 10.1037/a0018016

Friend, 2017, Developmental changes in maternal education and minimal exposure effects on vocabulary in English- and Spanish-learning toddlers, J. Exp. Child Psychol., 164, 250, 10.1016/j.jecp.2017.07.003

Lai, J. (2013). The Effects of Socioeconomic Status and Parent-Infant Interactions on Early Lexical Development of 12-to 24-Month-Old Infants. [Ph.D. Thesis, Zhejiang University].

Kuchirko, 2014, Why Is Infant Language Learning Facilitated by Parental Responsiveness?, Curr. Dir. Psychol. Sci., 23, 121, 10.1177/0963721414522813

Meyrose, 2018, Benefits of maternal education for mental health trajectories across childhood and adolescence, Soc. Sci. Med., 202, 170, 10.1016/j.socscimed.2018.02.026

Thompson, 2013, Maternal Characteristics and Perception of Temperament Associated With Infant TV Exposure, Pediatrics, 131, E390, 10.1542/peds.2012-1224

Deanda, 2016, Minimal second language exposure, SES, and early word comprehension: New evidence from a direct assessment, Biling.-Lang. Cogn., 19, 162, 10.1017/S1366728914000820

Patra, 2016, Maternal Education Level Predicts Cognitive, Language, and Motor Outcome in Preterm Infants in the Second Year of Life, Am. J. Perinatol., 33, 738, 10.1055/s-0036-1572532

Putnam, 2006, Measurement of fine-grained aspects of toddler temperament: The early childhood behavior questionnaire, Infant Behav. Dev., 29, 386, 10.1016/j.infbeh.2006.01.004

Ruiz, 2017, Bifidobacteria and Their Molecular Communication with the Immune System, Front. Microbiol., 8, 2345, 10.3389/fmicb.2017.02345

Kondo, 2013, Bifidobacterium breve B-3 exerts metabolic syndrome-suppressing effects in the liver of diet-induced obese mice: A DNA microarray analysis, Benef. Microbes, 4, 247, 10.3920/BM2012.0019

Wang, 2013, Meta-analysis of the efficacy and safety of Lactobacillus-containing and Bifidobacterium-containing probiotic compound preparation in Helicobacter pylori eradication therapy, J. Clin. Gastroenterol., 47, 25, 10.1097/MCG.0b013e318266f6cf

Kondo, 2013, Modulatory effects of Bifidobacterium longum BB536 on defecation in elderly patients receiving enteral feeding, World J. Gastroenterol., 19, 2162, 10.3748/wjg.v19.i14.2162

Sampson, 2015, Control of Brain Development, Function, and Behavior by the Microbiome, Cell Host Microbe, 17, 565, 10.1016/j.chom.2015.04.011

Savignac, 2014, Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice, Neurogastroenterol. Motil., 26, 1615, 10.1111/nmo.12427

Messaoudi, 2011, Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects, Br. J. Nutr., 105, 755, 10.1017/S0007114510004319

Kobayashi, 2017, Therapeutic potential of Bifidobacterium breve strain A1 for preventing cognitive impairment in Alzheimer’s disease, Sci. Rep., 7, 13510, 10.1038/s41598-017-13368-2

Inoue, T., Kobayashi, Y., Mori, N., Sakagawa, M., Xiao, J.Z., Moritani, T., Sakane, N., and Nagai, N. (2018). Effect of combined bifidobacteria supplementation and resistance training on cognitive function, body composition and bowel habits of healthy elderly subjects. Benef. Microbes, 1–12.

Allen, 2016, Bifidobacterium longum 1714 as a translational psychobiotic: Modulation of stress, electrophysiology and neurocognition in healthy volunteers, Transl. Psychiatry, 6, e939, 10.1038/tp.2016.191

Ohara, T. (2019). Identification of the microbial diversity after fecal microbiota transplantation therapy for chronic intractable constipation using 16s rRNA amplicon sequencing. PLoS ONE, 14.

Kaur, 2014, Hungatella effluvii gen. nov., sp. nov., an obligately anaerobic bacterium isolated from an effluent treatment plant, and reclassification of Clostridium hathewayi as Hungatella hathewayi gen. nov., comb. nov, Int. J. Syst. Evol. Microbiol., 64, 710, 10.1099/ijs.0.056986-0

Huang, 2017, Structure analysis of the gut microbiota in chronic functional constipation patients, Chin. J. Colorectal Dis., 6, 121

Zao, A.B. (2018). Analysis of Gut Microbiota in Patients with Parkinson’s Disease. [Ph.D. Thesis, Nanjing Medical University].

Wei, L. (2017). Diversity of Gut Flora in Navy Officers and Soldiers Involved in Long Voyage. [Ph.D. Thesis, The Second Military Medical University].