Association of Breastfeeding for the First Six Months of Life and Autism Spectrum Disorders: A National Multi-Center Study in China
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population and Overall Design
2.2. Procedure of ASD Screening and Diagnosis
2.3. Covariates
2.4. Breastfeeding
2.5. Statistical Analysis
3. Results
3.1. Demographic Information and Maternal Risk Factors during Pregnancy
3.2. Prevalence of ASD Associated with Breastfeeding
3.3. Associations of Breastfeeding in the First Six Months of Life with ASD among Toddlers
3.4. Subgroup Analysis
3.5. Sensitivity Analyses
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Collaborators, G.M.D. Global, regional, and national burden of 12 mental disorders in 204 countries and territories, 1990–2019: A systematic analysis from the Global Burden of Disease Study 2019. Lancet Psychiatry, 2020; in press. Available online: https://www.healthdata.org/research-article/global-regional-and-national(accessed on 19 December 2021).
- Lord, C.; Brugha, T.S.; Charman, T.; Cusack, J.; Dumas, G.; Frazier, T.; Jones, E.J.H.; Jones, R.M.; Pickles, A.; State, M.W.; et al. Autism spectrum disorder. Nat. Rev. Dis. Primers 2020, 6, 5. [Google Scholar] [CrossRef]
- Zhou, H.; Xu, X.; Yan, W.; Zou, X.; Wu, L.; Luo, X.; Li, T.; Huang, Y.; Guan, H.; Chen, X.; et al. Prevalence of Autism Spectrum Disorder in China: A Nationwide Multi-center Population-based Study Among Children Aged 6 to 12 Years. Neurosci. Bull. 2020, 36, 961–971. [Google Scholar] [CrossRef]
- Shi, B.; Wu, W.; Dai, M.; Zeng, J.; Luo, J.; Cai, L.; Wan, B.; Jing, J. Cognitive, Language, and Behavioral Outcomes in Children With Autism Spectrum Disorders Exposed to Early Comprehensive Treatment Models: A Meta-Analysis and Meta-Regression. Front. Psychiatry 2021, 12, 691148. [Google Scholar] [CrossRef] [PubMed]
- Leventakou, V.; Roumeliotaki, T.; Koutra, K.; Vassilaki, M.; Mantzouranis, E.; Bitsios, P.; Kogevinas, M.; Chatzi, L. Breastfeeding duration and cognitive, language and motor development at 18 months of age: Rhea mother-child cohort in Crete, Greece. J. Epidemiol. Community Health 2015, 69, 232–239. [Google Scholar] [CrossRef]
- Smith, J.M. Breastfeeding and language outcomes: A review of the literature. J. Commun. Disord. 2015, 57, 29–40. [Google Scholar] [CrossRef]
- Bar, S.; Milanaik, R.; Adesman, A. Long-term neurodevelopmental benefits of breastfeeding. Curr. Opin. Pediatr. 2016, 28, 559–566. [Google Scholar] [CrossRef]
- Belfort, M.B.; Anderson, P.J.; Nowak, V.A.; Lee, K.J.; Molesworth, C.; Thompson, D.K.; Doyle, L.W.; Inder, T.E. Breast Milk Feeding, Brain Development, and Neurocognitive Outcomes: A 7-Year Longitudinal Study in Infants Born at Less Than 30 Weeks’ Gestation. J. Pediatr. 2016, 177, 133–139.e131. [Google Scholar] [CrossRef] [Green Version]
- Deoni, S.; Dean, D.; Joelson, S.; O’Regan, J.; Schneider, N. Early nutrition influences developmental myelination and cognition in infants and young children. Neuroimage 2018, 178, 649–659. [Google Scholar] [CrossRef]
- Lopez, D.A.; Foxe, J.J.; Mao, Y.; Thompson, W.K.; Martin, H.J.; Freedman, E.G. Breastfeeding Duration Is Associated With Domain-Specific Improvements in Cognitive Performance in 9-10-Year-Old Children. Front. Public Health 2021, 9, 657422. [Google Scholar] [CrossRef]
- Burd, L.; Fisher, W.; Kerbeshian, J.; Vesely, B.; Durgin, B.; Reep, P. A comparison of breastfeeding rates among children with pervasive developmental disorder, and controls. J. Dev. Behav. Pediatr. 1988, 9, 247–251. [Google Scholar] [CrossRef] [PubMed]
- Tanoue, Y.; Oda, S. Weaning time of children with infantile autism. J. Autism Dev. Disord. 1989, 19, 425–434. [Google Scholar] [CrossRef] [PubMed]
- Schultz, S.T.; Klonoff-Cohen, H.S.; Wingard, D.L.; Akshoomoff, N.A.; Macera, C.A.; Ji, M.; Bacher, C. Breastfeeding, infant formula supplementation, and Autistic Disorder: The results of a parent survey. Int. Breastfeed. J. 2006, 1, 16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dodds, L.; Fell, D.B.; Shea, S.; Armson, B.A.; Allen, A.C.; Bryson, S. The role of prenatal, obstetric and neonatal factors in the development of autism. J. Autism Dev. Disord. 2011, 41, 891–902. [Google Scholar] [CrossRef] [PubMed]
- Shamberger, R.J. Autism rates associated with nutrition and the WIC program. J. Am. Coll. Nutr. 2011, 30, 348–353. [Google Scholar] [CrossRef] [PubMed]
- Al-Farsi, Y.M.; Al-Sharbati, M.M.; Waly, M.I.; Al-Farsi, O.A.; Al-Shafaee, M.A.; Al-Khaduri, M.M.; Trivedi, M.S.; Deth, R.C. Effect of suboptimal breast-feeding on occurrence of autism: A case-control study. Nutrition 2012, 28, e27–e32. [Google Scholar] [CrossRef]
- Brown, C.M.; Austin, D.W.; Busija, L. Observable essential fatty acid deficiency markers and autism spectrum disorder. Breastfeed. Rev. 2014, 22, 21–26. [Google Scholar] [PubMed]
- Field, S.S. Interaction of genes and nutritional factors in the etiology of autism and attention deficit/hyperactivity disorders: A case control study. Med. Hypotheses 2014, 82, 654–661. [Google Scholar] [CrossRef]
- George, B.; Padmam, M.S.; Nair, M.K.; Leena, M.L.; Russell, P.S. CDC Kerala 14: Early child care practices at home among children (2–6 y) with autism—A case control study. Indian J. Pediatr. 2014, 81, S138–S141. [Google Scholar] [CrossRef]
- Shafai, T.; Mustafa, M.; Hild, T.; Mulari, J.; Curtis, A. The association of early weaning and formula feeding with autism spectrum disorders. Breastfeed. Med. 2014, 9, 275–276. [Google Scholar] [CrossRef]
- Husk, J.S.; Keim, S.A. Breastfeeding and Autism Spectrum Disorder in the National Survey of Children’s Health. Epidemiology 2015, 26, 451–457. [Google Scholar] [CrossRef]
- Ravi, S.; Chandrasekaran, V.; Kattimani, S.; Subramanian, M. Maternal and birth risk factors for children screening positive for autism spectrum disorders on M-CHAT-R. Asian J. Psychiatry 2016, 22, 17–21. [Google Scholar] [CrossRef]
- Say, G.N.; Karabekiroglu, K.; Babadagi, Z.; Yuce, M. Maternal stress and perinatal features in autism and attention deficit/hyperactivity disorder. Pediatr. Int. 2016, 58, 265–269. [Google Scholar] [CrossRef] [PubMed]
- Boucher, O.; Julvez, J.; Guxens, M.; Arranz, E.; Ibarluzea, J.; Sanchez de Miguel, M.; Fernandez-Somoano, A.; Tardon, A.; Rebagliato, M.; Garcia-Esteban, R.; et al. Association between breastfeeding duration and cognitive development, autistic traits and ADHD symptoms: A multicenter study in Spain. Pediatr. Res. 2017, 81, 434–442. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bittker, S.S.; Bell, K.R. Acetaminophen, antibiotics, ear infection, breastfeeding, vitamin D drops, and autism: An epidemiological study. Neuropsychiatr. Dis. Treat. 2018, 14, 1399–1414. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lemcke, S.; Parner, E.T.; Bjerrum, M.; Thomsen, P.H.; Lauritsen, M.B. Early Regulation in Children Who Are Later Diagnosed with Autism Spectrum Disorder. A Longitudinal Study within the Danish National Birth Cohort. Infant Ment. Health J. 2018, 39, 170–182. [Google Scholar] [CrossRef]
- Manohar, H.; Pravallika, M.; Kandasamy, P.; Chandrasekaran, V.; Rajkumar, R.P. Role of Exclusive Breastfeeding in Conferring Protection in Children At-Risk for Autism Spectrum Disorder: Results from a Sibling Case-control Study. J. Neurosci. Rural Pract. 2018, 9, 132–136. [Google Scholar] [CrossRef]
- Soke, G.N.; Maenner, M.; Windham, G.; Moody, E.; Kaczaniuk, J.; DiGuiseppi, C.; Schieve, L.A. Association Between Breastfeeding Initiation and Duration and Autism Spectrum Disorder in Preschool Children Enrolled in the Study to Explore Early Development. Autism Res. 2019, 12, 816–829. [Google Scholar] [CrossRef]
- Chen, J.; Strodl, E.; Huang, L.H.; Chen, J.Y.; Liu, X.C.; Yang, J.H.; Chen, W.Q. Associations between Prenatal Education, Breastfeeding and Autistic-Like Behaviors in Pre-Schoolers. Children 2021, 8, 124. [Google Scholar] [CrossRef]
- Bawono, K.D.; Herini, E.S.; Wandita, S. Breastfeeding as a protective factor against autism. J. Gizi Klin. Indones. 2012, 8, 166–171. [Google Scholar] [CrossRef]
- Kim, J.H.; Lee, S.W.; Lee, J.E.; Ha, E.K.; Han, M.Y.; Lee, E. Breastmilk Feeding during the First 4 to 6 Months of Age and Childhood Disease Burden until 10 Years of Age. Nutrients 2021, 13, 2825. [Google Scholar] [CrossRef]
- Ghozy, S.; Tran, L.; Naveed, S.; Quynh, T.T.H.; Helmy Zayan, A.; Waqas, A.; Sayed, A.K.H.; Karimzadeh, S.; Hirayama, K.; Huy, N.T. Association of breastfeeding status with risk of autism spectrum disorder: A systematic review, dose-response analysis and meta-analysis. Asian J. Psychiatry 2020, 48, 101916. [Google Scholar] [CrossRef] [PubMed]
- Guo, C.; Luo, M.; Wang, X.; Huang, S.; Meng, Z.; Shao, J.; Zhang, X.; Shao, Z.; Wu, J.; Robins, D.L.; et al. Reliability and Validity of the Chinese Version of Modified Checklist for Autism in Toddlers, Revised, with Follow-Up (M-CHAT-R/F). J. Autism Dev. Disord. 2019, 49, 185–196. [Google Scholar] [CrossRef] [PubMed]
- von Elm, E.; Altman, D.G.; Egger, M.; Pocock, S.J.; Gøtzsche, P.C.; Vandenbroucke, J.P. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies. BMJ 2007, 335, 806–808. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, B.; Coorperative Meta-Analysis Group Of China Obesity Task Force. Predictive values of body mass index and waist circumference to risk factors of related diseases in Chinese adult population. Chin. J. Epidemiol. 2002, 23, 5–10. [Google Scholar]
- Dewey, K.G. Indicators for Assessing Infant and Young Child Feeding Practices. Ann. Nutr. Metab. 2009, 55, 10. [Google Scholar]
- Puhr, R.; Heinze, G.; Nold, M.; Lusa, L.; Geroldinger, A. Firth’s logistic regression with rare events: Accurate effect estimates and predictions? Stat. Med. 2017, 36, 2302–2317. [Google Scholar] [CrossRef]
- Purdy, I.B. Social, cultural, and medical factors that influence maternal breastfeeding. Issues Ment. Health Nurs. 2010, 31, 365–367. [Google Scholar] [CrossRef]
- Brion, M.J.; Lawlor, D.A.; Matijasevich, A.; Horta, B.; Anselmi, L.; Araujo, C.L.; Menezes, A.M.; Victora, C.G.; Smith, G.D. What are the causal effects of breastfeeding on IQ, obesity and blood pressure? Evidence from comparing high-income with middle-income cohorts. Int. J. Epidemiol. 2011, 40, 670–680. [Google Scholar] [CrossRef] [Green Version]
- Linde, K.; Lehnig, F.; Nagl, M.; Kersting, A. The association between breastfeeding and attachment: A systematic review. Midwifery 2020, 81, 102592. [Google Scholar] [CrossRef]
- Vivanti, G.; Nuske, H.J. Autism, attachment, and social learning: Three challenges and a way forward. Behav. Brain Res. 2017, 325, 251–259. [Google Scholar] [CrossRef]
- Rutgers, A.H.; Bakermans-Kranenburg, M.J.; van Ijzendoorn, M.H.; van Berckelaer-Onnes, I.A. Autism and attachment: A meta-analytic review. J. Child Psychol. Psychiatry 2004, 45, 1123–1134. [Google Scholar] [CrossRef] [PubMed]
- Ooi, Y.P.; Weng, S.J.; Kossowsky, J.; Gerger, H.; Sung, M. Oxytocin and Autism Spectrum Disorders: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Pharmacopsychiatry 2017, 50, 5–13. [Google Scholar] [CrossRef] [PubMed]
- Vanya, M.; Szucs, S.; Vetro, A.; Bartfai, G. The potential role of oxytocin and perinatal factors in the pathogenesis of autism spectrum disorders—Review of the literature. Psychiatry Res. 2017, 247, 288–290. [Google Scholar] [CrossRef] [Green Version]
- Sharma, S.R.; Gonda, X.; Dome, P.; Tarazi, F.I. What’s Love Got to do with it: Role of oxytocin in trauma, attachment and resilience. Pharmacol. Ther. 2020, 214, 107602. [Google Scholar] [CrossRef] [PubMed]
- John, S.; Jaeggi, A.V. Oxytocin levels tend to be lower in autistic children: A meta-analysis of 31 studies. Autism 2021, 25, 2152–2161. [Google Scholar] [CrossRef] [PubMed]
- Grote, V.; Verduci, E.; Scaglioni, S.; Vecchi, F.; Contarini, G.; Giovannini, M.; Koletzko, B.; Agostoni, C.; European Childhood Obesity Project. Breast milk composition and infant nutrient intakes during the first 12 months of life. Eur. J. Clin. Nutr. 2016, 70, 250–256. [Google Scholar] [CrossRef] [Green Version]
- Martins, B.P.; Bandarra, N.M.; Figueiredo-Braga, M. The role of marine omega-3 in human neurodevelopment, including Autism Spectrum Disorders and Attention-Deficit/Hyperactivity Disorder—A review. Crit. Rev. Food Sci. Nutr. 2020, 60, 1431–1446. [Google Scholar] [CrossRef]
- Steinman, G.; Mankuta, D. Breastfeeding as a possible deterrent to autism—A clinical perspective. Med. Hypotheses 2013, 81, 999–1001. [Google Scholar] [CrossRef]
- Mazahery, H.; Stonehouse, W.; Delshad, M.; Kruger, M.C.; Conlon, C.A.; Beck, K.L.; von Hurst, P.R. Relationship between Long Chain n-3 Polyunsaturated Fatty Acids and Autism Spectrum Disorder: Systematic Review and Meta-Analysis of Case-Control and Randomised Controlled Trials. Nutrients 2017, 9, 155. [Google Scholar] [CrossRef] [Green Version]
- Andersson, Y.; Hammarstrom, M.L.; Lonnerdal, B.; Graverholt, G.; Falt, H.; Hernell, O. Formula feeding skews immune cell composition toward adaptive immunity compared to breastfeeding. J. Immunol. 2009, 183, 4322–4328. [Google Scholar] [CrossRef] [Green Version]
- UNICEF. UNICEF Data|Optimal Feeding Practices are Fundamental to a Child’s Survival, Growth and Development, but Too Few Children Benefit. Available online: https://data.unicef.org/topic/nutrition/infant-and-young-child-feeding/ (accessed on 23 November 2021).
- Fang, J.; Qiu, Y.; Wang, X.; Li, J. Report on National Survey into Factors Influencing Breastfeeding (Conference Version); China Development Research Fundation: Beijing, China, 2019. [Google Scholar]
- Institute for Health Metrics and Evaluation. GBD Compare|Data Visualizations. Available online: https://vizhub.healthdata.org/gbd-compare/ (accessed on 23 November 2021).
- Kang, L.; Liang, J.; He, C.; Miao, L.; Li, X.; Dai, L.; Li, Q.; Liu, Z.; Zhu, J.; Wang, Y.; et al. Breastfeeding practice in China from 2013 to 2018: A study from a national dynamic follow-up surveillance. BMC Public Health 2021, 21, 329. [Google Scholar] [CrossRef] [PubMed]
- Tseng, P.T.; Chen, Y.W.; Stubbs, B.; Carvalho, A.F.; Whiteley, P.; Tang, C.H.; Yang, W.C.; Chen, T.Y.; Li, D.J.; Chu, C.S.; et al. Maternal breastfeeding and autism spectrum disorder in children: A systematic review and meta-analysis. Nutr. Neurosci. 2019, 22, 354–362. [Google Scholar] [CrossRef] [PubMed]
Variables | Means (Standard Deviation)/No. (%) | |
---|---|---|
Child’s age (Month) | 22.7 (4.1) | |
Child’s sex | Boy | 3364 (55.6) |
Girl | 2685 (44.4) | |
Only child | Yes | 4277 (70.7) |
No | 1772 (29.3) | |
Preterm birth | Yes | 507 (8.4) |
No | 5542 (91.6) | |
Maternal age | ≤24 years | 1045 (17.3) |
25–29 years | 3188 (52.7) | |
30–34 years | 1407 (23.3) | |
≥35 years | 409 (6.8) | |
Maternal education | Primary school and below | 677 (11.2) |
Middle school | 1289 (21.3) | |
College degree | 3768 (62.3) | |
Advanced degree | 315 (5.2) | |
Yearly household income | ≤¥100,000 | 2153 (35.6) |
¥100,000–¥300,000 | 2314 (38.3) | |
≥¥300,000 | 464 (7.7) | |
Not available | 1118 (18.5) | |
Ethnic background | Han | 5674 (93.8) |
Minority | 375 (6.2) | |
Complications during pregnancy | Yes | 860 (14.2) |
No | 5189 (85.8) | |
Depression during pregnancy | Yes | 1486 (24.6) |
No | 4563 (75.4) | |
Pre-pregnancy overweight/obesity | Yes | 472 (7.8) |
No | 5577 (92.2) | |
Second-hand smoke during pregnancy | Yes | 843 (13.9) |
No | 5206 (86.1) |
Crude Model a | Adjusted Model 1 b | Adjusted Model 2 c | ||||
---|---|---|---|---|---|---|
OR (95% CI) | p Value | OR (95% CI) | p Value | OR (95% CI) | p Value | |
Exclusive breastfeeding | 1 [Reference] | 1 [Reference] | 1 [Reference] | |||
Partial breastfeeding | 2.05 (1.21, 3.57) | 0.01 | 1.59 (0.93, 2.80) | 0.10 | 1.55 (0.90, 2.74) | 0.12 |
Not breastfeeding | 3.39 (1.64, 6.73) | <0.001 | 2.19 (1.04, 4. 46) | 0.03 | 2.34 (1.10, 4.82) | 0.02 |
Odd Ratios (95% CI) | Breastfeeding Status under the First Six Month | Pinteraction | ||
---|---|---|---|---|
Exclusive Breastfeeding | Partial Breastfeeding | Not Breastfeeding | ||
Children with ASD or without ASD | ||||
Stratified by child sex | 0.66 | |||
Boy | 1 [Reference] | 1.42 (0.76, 2.07) | 2.27 (1.39, 3.14) | |
Girl | 1 [Reference] | 2.92 (1.30, 4.53) | 2.57 (0.15, 4.99) | |
Stratified by only child | 0.75 | |||
No | 1 [Reference] | 1.16 (0.14, 2.18) | 1.78 (0.38, 3.18) | |
Yes | 1 [Reference] | 1.88 (1.12, 2.64) | 2.70 (1.69, 3.72) | |
Stratified by maternal age | 0.45 | |||
<30 years | 1 [Reference] | 1.93 (1.20, 2.66) | 3.03 (2.08, 3.99) | |
≥30 years | 1 [Reference] | 0.97 (−0.15, 2.08) | 1.06 (−0.58, 2.69) | |
Stratified by maternal education | 0.79 | |||
Middle school and below | 1 [Reference] | 1.27 (0.37, 2.16) | 1.93 (0.86, 3.01) | |
Bachelor degree or above | 1 [Reference] | 1.92 (1.08, 2.76) | 2.84 (1.60, 4.07) | |
Stratified by yearly household income | 0.42 | |||
≤¥100,000 | 1 [Reference] | 1.57 (0.74, 2.39) | 1.43 (0.21, 2.65) | |
>¥100,000 | 1 [Reference] | 1.59 (0.71, 2.48) | 3.73 (2.64, 4.83) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Huang, S.; Wang, X.; Sun, T.; Yu, H.; Liao, Y.; Cao, M.; Cai, L.; Li, X.; Lin, L.; Su, X.; et al. Association of Breastfeeding for the First Six Months of Life and Autism Spectrum Disorders: A National Multi-Center Study in China. Nutrients 2022, 14, 45. https://doi.org/10.3390/nu14010045
Huang S, Wang X, Sun T, Yu H, Liao Y, Cao M, Cai L, Li X, Lin L, Su X, et al. Association of Breastfeeding for the First Six Months of Life and Autism Spectrum Disorders: A National Multi-Center Study in China. Nutrients. 2022; 14(1):45. https://doi.org/10.3390/nu14010045
Chicago/Turabian StyleHuang, Saijun, Xin Wang, Tao Sun, Hong Yu, Yanwei Liao, Muqing Cao, Li Cai, Xiuhong Li, Lizi Lin, Xi Su, and et al. 2022. "Association of Breastfeeding for the First Six Months of Life and Autism Spectrum Disorders: A National Multi-Center Study in China" Nutrients 14, no. 1: 45. https://doi.org/10.3390/nu14010045
APA StyleHuang, S., Wang, X., Sun, T., Yu, H., Liao, Y., Cao, M., Cai, L., Li, X., Lin, L., Su, X., & Jing, J. (2022). Association of Breastfeeding for the First Six Months of Life and Autism Spectrum Disorders: A National Multi-Center Study in China. Nutrients, 14(1), 45. https://doi.org/10.3390/nu14010045