Altered dietary behaviour during pregnancy impacts systemic metabolic phenotypes

Charlotte E Rowley; Samantha Lodge; Siobhon Egan; Catherine Itsiopoulos; Claus T Christophersen; Desiree Silva; Elizabeth Kicic-Starcevich; Therese A O'Sullivan; Julien Wist; Jeremy Nicholson; Gary Frost; Elaine Holmes; Nina D'Vaz

doi:10.3389/fnut.2023.1230480

Altered dietary behaviour during pregnancy impacts systemic metabolic phenotypes

Front Nutr. 2023 Dec 4:10:1230480. doi: 10.3389/fnut.2023.1230480. eCollection 2023.

Authors

Charlotte E Rowley¹, Samantha Lodge¹, Siobhon Egan¹, Catherine Itsiopoulos², Claus T Christophersen^{3

4}, Desiree Silva^{5

6}, Elizabeth Kicic-Starcevich⁵, Therese A O'Sullivan⁴, Julien Wist^{1

7}, Jeremy Nicholson^{1

8

9}, Gary Frost^{1

9}, Elaine Holmes^{1

8

9}, Nina D'Vaz⁵

Affiliations

¹ Australian National Phenome Centre, and Centre for Computational and Systems Medicine, Health Futures Institute, Murdoch University, Perth, WA, Australia.
² Health and Biomedical Sciences, RMIT University, Melbourne, VIC, Australia.
³ WA Human Microbiome Collaboration Centre, Curtin University, Bentley, WA, Australia.
⁴ School of Medical and Health Sciences, Edith Cowan University, Joondalup, WA, Australia.
⁵ Telethon Kids Institute, Perth Children's Hospital, Nedlands, WA, Australia.
⁶ Joondalup Health Campus, Joondalup, WA, Australia.
⁷ Chemistry Department, Universidad del Valle, Cali, Colombia.
⁸ Faculty of Medicine, Imperial College London, Institute of Global Health Innovation, London, United Kingdom.
⁹ Section of Nutrition Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, United Kingdom.

Abstract

Rationale: Evidence suggests consumption of a Mediterranean diet (MD) can positively impact both maternal and offspring health, potentially mediated by a beneficial effect on inflammatory pathways. We aimed to apply metabolic profiling of serum and urine samples to assess differences between women who were stratified into high and low alignment to a MD throughout pregnancy and investigate the relationship of the diet to inflammatory markers.

Methods: From the ORIGINS cohort, 51 pregnant women were stratified for persistent high and low alignment to a MD, based on validated MD questionnaires. ¹H Nuclear Magnetic Resonance (NMR) spectroscopy was used to investigate the urine and serum metabolite profiles of these women at 36 weeks of pregnancy. The relationship between diet, metabolite profile and inflammatory status was investigated.

Results: There were clear differences in both the food choice and metabolic profiles of women who self-reported concordance to a high (HMDA) and low (LMDA) Mediterranean diet, indicating that alignment with the MD was associated with a specific metabolic phenotype during pregnancy. Reduced meat intake and higher vegetable intake in the HMDA group was supported by increased levels of urinary hippurate (p = 0.044) and lower creatine (p = 0.047) levels. Serum concentrations of the NMR spectroscopic inflammatory biomarkers GlycA (p = 0.020) and GlycB (p = 0.016) were significantly lower in the HDMA group and were negatively associated with serum acetate, histidine and isoleucine (p < 0.05) suggesting a greater level of plant-based nutrients in the diet. Serum branched chain and aromatic amino acids were positively associated with the HMDA group while both urinary and serum creatine, urine creatinine and dimethylamine were positively associated with the LMDA group.

Conclusion: Metabolic phenotypes of pregnant women who had a high alignment with the MD were significantly different from pregnant women who had a poor alignment with the MD. The metabolite profiles aligned with reported food intake. Differences were most significant biomarkers of systemic inflammation and selected gut-microbial metabolites. This research expands our understanding of the mechanisms driving health outcomes during the perinatal period and provides additional biomarkers for investigation in pregnant women to assess potential health risks.

Keywords: Mediterranean diet; fibre; hippurate; inflammation; metabolic phenotype; pregnancy; α-1-acid glycoprotein.

Grants and funding

The ORIGINS Project has received core funding support from the Telethon Perth Children’s Hospital Research Fund, Joondalup Health Campus, the Paul Ramsay Foundation and the Commonwealth Government of Australia through the Channel 7 Telethon Trust. Substantial in-kind support has been provided by Telethon Kids Institute and Joondalup Health Campus. The authors thank the Science Sceptics of WA for the funding for this project, as well as Bruker Corporation, United States and the Channel 7 Telethon Trust, Western Australia. In addition the MRFF for funding the Australian National Phenome Centre for this and related work. They also thank Bruker and the Cooperative Research Centre Future Food Systems funding for CR, and MRFF Frontier Health and Medical Research, the Australian Research Council for Laureate Fellowship funding for EH, and the NHMRC MRFF grant (2014349). We thank Drew Hall and Philipp Nitschke for advice on the technical aspects of the NMR spectroscopic analysis.