Abstract
Background
Previous studies have linked gestational diabetes (GDM) with allergies in offspring. However, the effect of specific glucose metabolism metrics was not well characterized, and the role of polyunsaturated fatty acids (PUFAs), a modifier of metabolism and the immune system, was understudied. We aimed to investigate the association between maternal GDM and allergic diseases in children and the interaction between glucose metabolism and PUFAs on allergic outcomes.
Methods
This prospective cohort study included 706 mother–child dyads from Guangzhou, China. Maternal GDM was diagnosed via a 75-g oral glucose tolerance test (OGTT), and dietary PUFAs were assessed using a validated food frequency questionnaire. Allergic disease diagnoses and the age of onset were obtained from medical records of children within three years old.
Results
Approximately 19.4% of women had GDM, and 51.3% of children had any allergic diseases. GDM was positively associated with any allergic diseases (hazard ratio [HR] 1.40; 95% confidence interval (CI) 1.05–1.88) and eczema (HR 1.44; 95% CI 1.02–1.97). A unit increase in OGTT after two hours (OGTT-2 h) glucose was associated with an 11% (95% CI 2%–21%) higher risk of any allergic diseases and a 17% (95% CI 1–36%) higher risk of food allergy. The positive associations between OGTT-2 h glucose and any allergic diseases were strengthened with decreased dietary a-linolenic acid (ALA) and increased n-6 PUFAs, linoleic acid (LA), LA/ALA ratio, and n-6/n-3 PUFA ratio.
Conclusions
Maternal GDM was adversely associated with early-life allergic diseases, especially eczema. We were the first to identify OGTT-2 h glucose to be more sensitive in inducing allergy risk and that dietary PUFAs might modify the associations.
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Data availability statement
The datasets generated during and/or analyzed during the current study are not publicly available due to individual privacy, but are available from the corresponding author on reasonable request.
References
World Allergy Organization. World Allergy Organization (WAO) White Book on Allergy: Update 2013. 2013. https://www.worldallergy.org/wao-white-book-on-allergy. Accessed 17 Feb 2023.
Wang S, Jiang JX, Wang Y, Wang ZH, Wang T, Wang HS. Survey on prevalence of allergic symptoms among 0–24 months old children in Chinese cities. Chin J Child Heal Care. 2016;24:119–22.
Abuabara K, Ye M, Margolis DJ, McCulloch CE, Mulick AR, Silverwood RJ, et al. Patterns of atopic eczema disease activity from birth through midlife in 2 British birth cohorts. JAMA Dermatol. 2021;157:1191–9.
Montalbano L, Ferrante G, Montella S, Cilluffo G, Di Marco A, Bozzetto S, et al. Relationship between quality of life and behavioural disorders in children with persistent asthma: a multiple indicators multiple causes (MIMIC) model. Sci Rep. 2020;10:6957.
Schmitt J, Schwarz K, Baurecht H, Hotze M, Folster-Holst R, Rodriguez E, et al. Atopic dermatitis is associated with an increased risk for rheumatoid arthritis and inflammatory bowel disease, and a decreased risk for type 1 diabetes. J Allergy Clin Immunol. 2016;137:130–6.
Schans JV, Cicek R, de Vries TW, Hak E, Hoekstra PJ. Association of atopic diseases and attention-deficit/hyperactivity disorder: a systematic review and meta-analyses. Neurosci Biobehav Rev. 2017;74:139–48.
Warner JA, Jones CA, Jones AC, Warner JO. Prenatal origins of allergic disease. J Allergy Clin Immunol. 2000;105:S493–8.
Hui JW, Leung DYM. Origins of allergic disease: maternal and early childhood factors. Ann Allergy Asthma Immunol. 2020;125:501–2.
North ML, Ellis AK. The role of epigenetics in the developmental origins of allergic disease. Ann Allergy Asthma Immunol. 2011;106:355–61 (quiz 62).
Garcia-Larsen V, Ierodiakonou D, Jarrold K, Cunha S, Chivinge J, Robinson Z, et al. Diet during pregnancy and infancy and risk of allergic or autoimmune disease: a systematic review and meta-analysis. PLoS Med. 2018;15:e1002507.
Feleszko W, Ruszczynski M, Jaworska J, Strzelak A, Zalewski BM, Kulus M. Environmental tobacco smoke exposure and risk of allergic sensitisation in children: a systematic review and meta-analysis. Arch Dis Child. 2014;99:985–92.
Rusconi F, Galassi C, Forastiere F, Bellasio M, De Sario M, Ciccone G, et al. Maternal complications and procedures in pregnancy and at birth and wheezing phenotypes in children. Am J Respir Crit Care Med. 2007;175:16–21.
International Association of Diabetes and Pregnancy Study Groups Consensus Panel, Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, et al. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care. 2010;33:676–82.
Taricco E, Radaelli T, Rossi G, Nobile-de-Santis MS, Bulfamante GP, Avagliano L, et al. Effects of gestational diabetes on fetal oxygen and glucose levels in vivo. BJOG. 2009;116:1729–35.
Newsholme P, Cruzat VF, Keane KN, Carlessi R, de Bittencourt Jr. PI. Molecular mechanisms of ROS production and oxidative stress in diabetes. Biochem J. 2016;473:4527–50.
Nelson SM, Sattar N, Freeman DJ, Walker JD, Lindsay RS. Inflammation and endothelial activation is evident at birth in offspring of mothers with type 1 diabetes. Diabetes. 2007;56:2697–704.
Martinez MP, Lin J, Chow T, Chung J, Wang X, Xiang AH. Maternal gestational diabetes and type 2 diabetes during pregnancy and risk of childhood asthma in offspring. J Pediatr. 2020;219:e1.
Azad MB, Becker AB, Kozyrskyj AL. Association of maternal diabetes and child asthma. Pediatr Pulmonol. 2013;48:545–52.
Nasreen S, Wilk P, Mullowney T, Karp I. The effect of gestational diabetes mellitus on the risk of asthma in offspring. Ann Epidemiol. 2021;57:7–13.
Liu X, Agerbo E, Li J, Dharmage SC, Thomsen RW, Olsen J, et al. Maternal pregestational or gestational diabetes and childhood wheezing: a population-based cohort study. Allergy. 2018;73:2247–50.
Adgent MA, Gebretsadik T, Reedus J, Graves C, Garrison E, Bush N, et al. Gestational diabetes and childhood asthma in a racially diverse US pregnancy cohort. Pediatr Allergy Immunol. 2021;32:1190–6.
Li Z, Yu M, Wang P, Qian H, Fan Y, Li X, et al. Association between maternal diabetes mellitus and allergic diseases in children—a systematic review and meta-analysis. Pediatr Allergy Immunol. 2021;32:880–91.
World Health Organization. WHO Recommendations on Antenatal Care for a Positive Pregnancy Experience, 2016. https://www.who.int/publications/i/item/9789241549912. Accessed 3 Jul 2022.
Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W, et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell. 2010;142:687–98.
Cai L, Wu W, Lin L, Chen Y, Gao R, Shi B, et al. Association between plasma irisin and glucose metabolism in pregnant women is modified by dietary n-3 polyunsaturated fatty acid intake. J Diabetes Investig. 2020;11:1326–35.
Peng S, Du Z, He Y, Zhao F, Chen Y, Wu S, et al. Association of maternal erythrocyte PUFA during pregnancy with offspring allergy in the Chinese population. Nutrients. 2022;14:2312.
Wu W, Lin L, Shi B, Jing J, Cai L. The effects of early life polyunsaturated fatty acids and ruminant trans fatty acids on allergic diseases: a systematic review and meta-analysis. Crit Rev Food Sci Nutr. 2019;59:1802–15.
Imamura F, Micha R, Wu JH, de Oliveira Otto MC, Otite FO, Abioye AI, et al. Effects of saturated fat, polyunsaturated fat, monounsaturated fat, and carbohydrate on glucose-insulin homeostasis: a systematic review and meta-analysis of randomised controlled feeding trials. PLoS Med. 2016;13:e1002087.
Venter C, Meyer RW, Nwaru BI, Roduit C, Untersmayr E, Adel-Patient K, et al. EAACI position paper: influence of dietary fatty acids on asthma, food allergy, and atopic dermatitis. Allergy. 2019;74:1429–44.
Mallol J, Crane J, von Mutius E, Odhiambo J, Keil U, Stewart A, et al. The International Study of Asthma and Allergies in Childhood (ISAAC) phase three: a global synthesis. Allergol Immunopathol (Madr). 2013;41:73–85.
Sherwani SI, Khan HA, Ekhzaimy A, Masood A, Sakharkar MK. Significance of HbA1c test in diagnosis and prognosis of diabetic patients. Biomark Insights. 2016;11:95–104.
Zhang CX, Ho SC. Validity and reproducibility of a food frequency Questionnaire among Chinese women in Guangdong province. Asia Pac J Clin Nutr. 2009;18:240–50.
Yang Y. China food composition. Beijing: Beijing Peking University Medical Press; 2002.
Willett WC, Howe GR, Kushi LH. Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr. 1997;65:1220S–31.
Moreno MA. JAMA pediatrics patient page. Atopic diseases in children. JAMA Pediatr. 2016;170:96.
Haataja P, Korhonen P, Ojala R, Hirvonen M, Paassilta M, Gissler M, et al. Asthma and atopic dermatitis in children born moderately and late preterm. Eur J Pediatr. 2016;175:799–808.
Kumar R, Ouyang F, Story RE, Pongracic JA, Hong X, Wang G, et al. Gestational diabetes, atopic dermatitis, and allergen sensitization in early childhood. J Allergy Clin Immunol. 2009;124:e1–4.
Cave AJ, Atkinson LL. Asthma in preschool children: a review of the diagnostic challenges. J Am Board Fam Med. 2014;27:538–48.
Sifnaios E, Mastorakos G, Psarra K, Panagopoulos ND, Panoulis K, Vitoratos N, et al. Gestational diabetes and T cell (Th1/Th2/Th17/Treg) immune profile. In Vivo. 2019;33:31–40.
Sert UY, Ozgu-Erdinc AS. Gestational diabetes mellitus screening and diagnosis. Adv Exp Med Biol. 2021;1307:231–55.
Hicks WB, Nageotte CG, Wegienka G, Havstad S, Johnson CC, Ownby DR, et al. The association of maternal prenatal IgE and eczema in offspring is restricted to non-atopic mothers. Pediatr Allergy Immunol. 2011;22:684–7.
Gao XL, Yang HX, Zhao Y. Variations of tumor necrosis factor-alpha, leptin and adiponectin in mid-trimester of gestational diabetes mellitus. Chin Med J (Engl). 2008;121:701–5.
Lewandowski KC, Stojanovic N, Press M, Tuck SM, Szosland K, Bienkiewicz M, et al. Elevated serum levels of visfatin in gestational diabetes: a comparative study across various degrees of glucose tolerance. Diabetologia. 2007;50:1033–7.
Shore SA. Obesity and asthma: possible mechanisms. J Allergy Clin Immunol. 2008;121:1087–93 (quiz 94–5).
Marin-Juez R, Jong-Raadsen S, Yang S, Spaink HP. Hyperinsulinemia induces insulin resistance and immune suppression via Ptpn6/Shp1 in zebrafish. J Endocrinol. 2014;222:229–41.
Das UN. Essential fatty acids: biochemistry, physiology and pathology. Biotechnol J. 2006;1:420–39.
Wei Y, Meng Y, Li N, Wang Q, Chen L. The effects of low-ratio n-6/n-3 PUFA on biomarkers of inflammation: a systematic review and meta-analysis. Food Funct. 2021;12:30–40.
Li N, Yue H, Jia M, Liu W, Qiu B, Hou H, et al. Effect of low-ratio n-6/n-3 PUFA on blood glucose: a meta-analysis. Food Funct. 2019;10:4557–65.
Acknowledgements
We thank all the participating families and the research assistants involved with our study.
Funding
This research was supported by the Key-Area Research and Development Program of Guangdong Province (2019B030335001), the Natural Science Foundation of Guangdong Province, China (2023A1515030192), and the “Nutrition and Care of Maternal & Child Research Fund Project” of Biostime Institute of Nutrition & Care (2021BINCMCF053).
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LC: conceptualizaion, methodology, investigation, data curation, formal analysis, resource, supervision. YC: conceptualizaion, methodology, investigation, data curation, formal analysis, visualization, writing–original draft. LL: conceptualizaion, methodology, writing–review and editing. SP, BJ, XL, NL: investigation, data curation, formal analysis. YW: visualization. SK, XW, ZL: writing–review and editing. JJ: writing–review and editing, resource, supervision.
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No financial or non-financial benefits have been received or will be received from any party related directly or indirectly to the subject of this article.
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This study was approved by the ethics committee of the School of Public Health, Sun Yat-sen University (approval number: SYSUSPH2021121). Informed consent to participate in the study have been obtained from participants.
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Chen, YJ., Lin, LZ., Liu, ZY. et al. Association between maternal gestational diabetes and allergic diseases in offspring: a birth cohort study. World J Pediatr 19, 972–982 (2023). https://doi.org/10.1007/s12519-023-00710-0
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DOI: https://doi.org/10.1007/s12519-023-00710-0