Abstract
Objectives
Hyperglycaemia first detected in pregnancy (HFDP), on the rise in urban sub-Saharan Africa (SSA), may negatively impact foetal neurodevelopment, with potential long-term cognitive consequences for the child. Data on this association from SSA is lacking, and we aimed to investigate the association in 3- to 6-year-old children in Soweto, South Africa.
Methods
In this comparative study, we compared cognitive skills measured with the Herbst Early Childhood Development Criteria test in 95 children born to mothers with HFDP and 99 participants unexposed to maternal HFDP. Fine and gross motor skills were secondary outcomes. Ordinal regression analysis with known confounders was performed for children born at-term.
Results
Of children exposed to HFDP born at-term, 24.3% scored ‘high’ and 25.7% scored ‘low’ in the cognitive subsection of the test, as opposed to 37.7% and 12.9% in the HFDP-unexposed group, respectively. In ordinal regression, exposed participants had a significantly lower odds of scoring in a higher cognitive category when adjusting for maternal confounders and socio-economic status (OR 0.33, 95% CI 0.15–0.74, p = 0.007). No difference was found in gross motor development between the two groups; differences in fine motor development were attenuated after adjustment for maternal pregnancy factors and household socioeconomic status (OR 0.62, 95% CI 0.28–1.37, p = 0.239).
Conclusions for Practice
Exposure to HFDP was negatively associated with cognitive development at preschool age. Optimising maternal (preconception) health and early childhood cognitive stimulation could help more children reach their developmental potential.
Similar content being viewed by others
Data Availability
Data is available upon request to the corresponding author.
Code Availability
Not applicable.
References
Adane, A. A., Mishra, G., & Tooth, L. (2018). Maternal preconception weight trajectories, pregnancy complications and offspring’s childhood physical and cognitive development. Journal of Developmental Origins of Health and Disease, 9(6), 653–660. https://doi.org/10.1017/S2040174418000570
Adane, A. A., Mishra, G. D., & Tooth, L. R. (2016). Diabetes in pregnancy and childhood cognitive development: A systematic review. Review Article Pediatrics. https://doi.org/10.1542/peds.2015-4234
Bhutta, A. T., Cleves, M. A., Casey, P. H., Cradock, M. M., & Anand, K. J. S. (2002). Cognitive and behavioral outcomes of school-aged children who were born preterm: A meta-analysis. Journal of the American Medical Association, 288(6), 728–737. https://doi.org/10.1001/jama.288.6.728
Black, M. M., Walker, S. P., Fernald, L. C., Andersen, C. T., DiGirolamo, A. M., Lu, C., McCoy, D. C., Bhutta, Z. A., Britto, P. R., Daelmans, B., Darmstadt, G. L., Dua, T., Gertler, P., Heymann, J., Lombardi, J., Lopez Boo, F., Lye, S. J., MacMillan, H., Perez-Escamilla, R., … Grantham-McGregor, S. (2017). Early childhood development coming of age: Science through the life course Early Childhood Development Series Steering Committee HHS Public Access. Lancet, 389, 77–90. https://doi.org/10.1016/S0140-6736(16)31389-7
Chatfield, A., Caglia, J., Dhillon, S., Hirst, J., Cheikh Ismail, L., Abawi, K., Kac, G., Al Dhaheri, A., Villar, J., Kennedy, S., & Langer, A. (2013). Translating research into practice: The introduction of the INTERGROWTH-21st package of clinical standards, tools and guidelines into policies, programmes and services. BJOG, 120(Supplement 2), 139–142. https://doi.org/10.1111/1471-0528.12416
Clausen, T. D., Mortensen, E. L., Schmidt, L., Mathiesen, E. R., Hansen, T., Jensen, D. M., & Damm, P. (2013). Cognitive function in adult offspring of women with gestational diabetes—The role of glucose and other factors. PLoS ONE. https://doi.org/10.1371/journal.pone.0067107
Cook, C. J., Howard, S. J., Scerif, G., Twine, R., Kahn, K., Norris, S. A., & Draper, C. E. (2019). Associations of physical activity and gross motor skills with executive function in preschool children from low-income South African settings. Developmental Science, 22(5), 1–13. https://doi.org/10.1111/desc.12820
de Sousa, R. A. L., Torres, Y. S., Figueiredo, C. P., Passos, G. F., & Clarke, J. R. (2018). Consequences of gestational diabetes to the brain and behavior of the offspring. Anais Da Academia Brasileira De Ciencias, 90(2), 2279–2291. https://doi.org/10.1590/0001-3765201720170264
Dionne, G., Boivin, M., Séguin, J. R., Pérusse, D., & Tremblay, R. E. (2008). Gestational diabetes hinders language development in offspring. Pediatrics, 122(5), e1073–e1079. https://doi.org/10.1542/peds.2007-3028
Draper, C. E., Achmat, M., Forbes, J., & Lambert, E. V. (2012). Impact of a community-based programme for motor development on gross motor skills and cognitive function in preschool children from disadvantaged settings. Early Child Development and Care, 182(1), 137–152. https://doi.org/10.1080/03004430.2010.547250
Ford, N. D., & Stein, A. D. (2016). Risk factors affecting child cognitive development: A summary of nutrition, environment, and maternal-child interaction indicators for sub-Saharan Africa. Journal of Developmental Origins of Health and Disease, 7(2), 197–217. https://doi.org/10.1017/S2040174415001427
Fraser, A., Nelson, S. M., Macdonald-Wallis, C., & Lawlor, D. A. (2012). Associations of existing diabetes, gestational diabetes, and glycosuria with offspring IQ and educational attainment: The Avon longitudinal study of parents and children. Experimental Diabetes Research, 2012, 1–7. https://doi.org/10.1155/2012/963735
French, B., Outhwaite, L. A., Langley-Evans, S. C., & Pitchford, N. J. (2020). Nutrition, growth, and other factors associated with early cognitive and motor development in Sub-Saharan Africa: A scoping review. Journal of Human Nutrition and Dietetics, 33(5), 644–669. https://doi.org/10.1111/JHN.12795
Grantham-McGregor, S., Cheung, Y. B., Cueto, S., Glewwe, P., Richter, L., Strupp, B., The International Child Development Steering Group. (2007). Developmental potential in the first 5 years for children in developing countries. Lancet, 369(9555), 60–70. https://doi.org/10.1016/S0140-6736(07)60032-4
Harris, P. A., Taylor, R., Thielke, R., Payne, J., Gonzalez, N., & Conde, J. G. (2009). Research electronic data capture (REDCap)—A metadata-driven methdology and workflow process for providing translational research informatics support. Journal of Biomedical Informatics, 42(2), 377–381.
Herbst, I., & Huysamen, G. K. (2000). The construction and validation of developmental scales for environmentally disadvantaged preschool children. South African Journal of Psychology, 30(3), 19–24.
Koning, S. H., Hoogenberg, K., Lutgers, H. L., van den Berg, P. P., & Wolffenbuttel, B. H. R. (2016). Gestational diabetes mellitus: Current knowledge and unmet needs. Journal of Diabetes. https://doi.org/10.1111/1753-0407.12422
Kristenson, M., Eriksen, H. R., Sluiter, J. K., Starke, D., & Ursin, H. (2004). Psychobiological mechanisms of socioeconomic differences in health. Social Science and Medicine, 58(8), 1511–1522. https://doi.org/10.1016/S0277-9536(03)00353-8
Lake, A., & Chan, M. (2015). Putting science into practice for early child development. The Lancet, 385(9980), 1816–1817. https://doi.org/10.1016/S0140-6736(14)61680-9
Macaulay, S., Ngobeni, M., Dunger, D. B., & Norris, S. A. (2018). The prevalence of gestational diabetes mellitus amongst black South African women is a public health concern. Diabetes Research and Clinical Practice, 139, 278–287. https://doi.org/10.1016/j.diabres.2018.03.012
Márquez-Valadez, B., Valle-Bautista, R., García-López, G., Díaz, N. F., & Molina-Hernández, A. (2018). Maternal diabetes and fetal programming toward neurological diseases: Beyond neural tube defects. Frontiers in Endocrinology, 9(664), 1–10. https://doi.org/10.3389/fendo.2018.00664
Nomura, Y., Marks, D. J., Grossman, B., Yoon, M., Loudon, H., Stone, J., & Halperin, J. M. (2012). Exposure to gestational diabetes mellitus and low socioeconomic status: Effects on neurocognitive development and risk of attention-deficit/hyperactivity disorder in offspring. Archives of Pediatrics & Adolescent Medicine, 166(4), 337–343. https://doi.org/10.1001/archpediatrics.2011.784
Nozyce, M. L., Huo, Y., Williams, P. L., Kapetanovic, S., Hazra, R., Nichols, S., Hunter, S., Smith, R., Seage, G. R., & Sirois, P. A. (2014). Safety of in utero and neonatal antiretroviral exposure: Cognitive and academic outcomes in HIV-exposed, uninfected children 5–13 years of age. Pediatric Infectious Disease Journal, 33(11), 1128–1133. https://doi.org/10.1097/INF.0000000000000410
Ornoy, A. (2005). Growth and neurodevelopmental outcome of children born to mothers with pregestational and gestational diabetes. Pediatric Endocrinology Reviews, 3(2), 104–113.
Ornoy, A., Ratzon, N., Greenbaum, C., Wolf, A., & Dulitzky, M. (2001). School-age children born to diabetic mothers and to mothers with gestational diabetes exhibit a high rate of inattention and fine and gross motor impairment. Journal of Pediatric Endocrinology and Metabolism, 14(Supplement 1), 681–689. https://doi.org/10.1515/jpem.2001.14.s1.681
Robles, M. C., Campoy, C., Garcia Fernandez, L., Lopez-Pedrosa, J. M., Rueda, R., & Martin, M. J. (2015). Maternal diabetes and cognitive performance in the offspring: A systematic review and meta-analysis. PLoS ONE, 10(11), e0142583. https://doi.org/10.1371/journal.pone.0142583
Silverman, B. L., Rizzo, T. A., Cho, N. H., & Metzger, B. E. (1998). Long-term effects of the intrauterine environment. Diabetes Care, 21(Supplement 2), B142.
Spaull, N., & Kotze, J. (2015). Starting behind and staying behind in South Africa. The case of insurmountable learning deficits in mathematics. International Journal of Educational Development, 41, 13–24. https://doi.org/10.1016/j.ijedudev.2015.01.002
StataCorp. (2013). Stata statistical software: Release 13 (No. 13). StataCorp.
Statistics South Africa. (2016). Statistics South Africa. Retrieved October 4, 2020 from http://www.statssa.gov.za/?page_id=4286&id=11317
Steyn, N. P., & Mchiza, Z. J. (2014). Obesity and the nutrition transition in Sub-Saharan Africa. Annals of the New York Academy of Sciences, 1311(1), 88–101. https://doi.org/10.1111/nyas.12433
Tomaz, S. A., Hinkley, T., Jones, R. A., Twine, R., Kahn, K., Norris, S. A., & Draper, C. E. (2020). Objectively measured physical activity in South African children attending preschool and grade R: Volume, patterns, and meeting guidelines. Pediatric Exercise Science, 32(3), 150–156. https://doi.org/10.1123/pes.2019-0216
Van Rie, A., Mupuala, A., & Dow, A. (2008). Impact of the HIV/AIDS epidemic on the neurodevelopment of preschool-aged children in Kinshasa, democratic Republic of the Congo. Pediatrics, 122(1), e123. https://doi.org/10.1542/peds.2007-2558
Walker, S. P., Wachs, T. D., Gardner, J. M., Lozoff, B., Wasserman, G. A., Pollitt, E., Carter, J. A., International Child Development Steering Group. (2007). Child development: risk factors for adverse outcomes in developing countries. Lancet, 369(9556), 145–157. https://doi.org/10.1016/S0140-6736(07)60076-2
West, N. S., Schwartz, S. R., Yende, N., Schwartz, S. J., Parmley, L., Gadarowski, M. B., Mutunga, L., Bassett, J., & Van Rie, A. (2019). Infant feeding by South African mothers living with HIV: Implications for future training of health care workers and the need for consistent counseling. International Breastfeeding Journal, 14(1), 11. https://doi.org/10.1186/s13006-019-0205-1
World Health Organization. (2006). The WHO child growth standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. World Health Organization.
World Health Organisation. (2013). Diagnostic criteria and classification of hyperglycaemia first detected in pregnancy. World Health Organization.
Funding
This study was supported through SAN by the South African Medical Research Council, and SAN is also supported by the DST-NRF Centre of Excellence in Human Development at the University of the Witwatersrand, Johannesburg.
Author information
Authors and Affiliations
Contributions
SAN, KKG, NSL, VN, CED and LMS contributed to research conceptualization and planning. VN and LMS contributed to the study project coordination and data collection. CD advised on the use of the Herbst test. LMS performed data analysis and wrote the initial manuscript version. All the authors contributed to interpretation of data and revising the manuscript. All authors approved the final submitted version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors have no conflict of interest to declare.
Ethical Approval
Ethical approval for this study was obtained from the Human Research Ethics Committee of the University of the Witwatersrand (ref: M180317), and the study was therefore performed in accordance with the 1964 Declaration of Helsinki and its amendments.
Consent to Participate
Written informed consent was obtained from the participants’ parent or guardian prior to participation in the study. Any details that might disclose the identity of the participants were omitted.
Consent for Publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Soepnel, L.M., Nicolaou, V., Draper, C.E. et al. Cognitive and Motor Development in 3- to 6-Year-Old Children Born to Mothers with Hyperglycaemia First Detected in Pregnancy in an Urban African Population. Matern Child Health J 26, 1328–1338 (2022). https://doi.org/10.1007/s10995-021-03331-z
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10995-021-03331-z