Shifting pattern of gut microbiota in pregnant women two decades apart – an observational study

ABSTRACT

Background:

Past decades have witnessed a decrease in environmental biodiversity. We hypothesized a similar decrease in indigenous gut microbiota diversity, which may have contributed to the obesity epidemic.

Objective:

To investigate the changes in the composition and function of the gut microbiota in pregnant women over a period of 20 years.

Study design:

Altogether 124 pregnant women (41 overweight and matched 83 normal weight) pregnant in 1997, 2007 or 2017 were included in the study. The gut microbiota composition was assessed from fecal samples obtained at 32 weeks of gestation by 16S rRNA gene sequencing. Fecal short chain fatty acid (SCFA) profiles were measured by gas chromatography mass spectrometry (GC-MS).

Results:

Distinct gut microbiota profiles were detected in pregnant women from 1997, 2007 and 2017 (PERMANOVA Bray-Curtis R² = 0.029, p = 0.001). The women pregnant in 1997 exhibited significantly higher microbiota richness and diversity as compared to those pregnant in 2007 and 2017. The total concentration of fecal SCFAs was significantly higher in the pregnant women in 1997 compared to those in 2007 and 2017. Significant differences in gut microbiota composition between normal weight and overweight women were manifest in 1997 but not in 2007 or 2017.

Conclusions:

The decrease in intestinal microbiota richness and diversity over two decades occurred in parallel with the decline in biodiversity in our natural surroundings. It appears that the gut microbiota of pregnant women has changed over time to a composition typical for overweight individuals.

Plain Language Summary

The composition of the indigenous gut microbiota was investigated in pregnant women from three different time periods (1997, 2007 and 2017) in the same geographical and cultural area in Southwest Finland. Distinct gut microbiota profiles were evident in the women from the different time periods. The women pregnant in 1997 exhibited significantly higher microbiota richness and diversity as compared to the pregnant women from 2007 to 2017. The cause of the loss of gut microbiota richness and diversity over time remains obscure, since no major changes in the population, dietary practices or antibiotic use occurred in the area during the course of the study periods. Gut microbiota composition has been suggested to play a causal role in the development of overweight and obesity. In line with this notion, significant differences in the gut microbiota composition between normal weight and overweight were detectable in women pregnant in 1997. However, no such differences were manifest in women pregnant in 2007 or 2017 and the gut microbiota of these individuals resembled that of overweight pregnant women from 1997. The results of the study provide direct evidence for a decline in gut microbiota diversity over time in the same geographical area and the same population. It furthermore appears that the gut microbiota of pregnant women has changed over time to a composition typical for overweight individuals. The gut microbiota profiles may thus provide insight into the development and intergenerational transfer of overweight.

KEYWORDS:

• Fecal short-chain fatty acids
• gut microbiota
• obesity
• overweight
• pregnancy

Abbreviations

BMI	=	Body Mass Index
FDR	=	False Discovery Rate
CCA	=	Canonical Correspondence Analysis
GC-MS	=	Gas Chromatography-Mass Spectrometry
LDA	=	Linear Discriminant Analysis
PERMANOVA	=	Permutational Multivariate Analysis Of Variance
SCFAs	=	Short Chain Fatty Acids

Acknowledgments

Professor Seppo Salminen, PhD, from the University of Turku is acknowledged for his contribution to the original intervention studies and valuable comments regarding the results of the present study. Dr. Hanna Lagström, PhD, from the University of Turku is acknowledged for providing expert views regarding dietary changes in Finland during the study period. We thank the technical support from Erika Cortés-Macías and Julian Beltrán, IATA-CSIC, Valencia. Finally, Prof. Maria Carmen Collado, PhD, and Dr. Marta Selma-Royo, PhD, acknowledge the support by the research grant (ref. PID2022-139475OB-I00) from the Spanish Ministry of Science and Innovation (MCIN) and also, the award of the Spanish government MCIN/AEI to the IATA-CSIC as Center of Excellence Accreditation Severo Ochoa (reference: CEX2021-001189-S/MCIN/AEI/10.13039/501100011033).

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

EI, SR conceptualized the study. MSR, MCC performed the microbiota and SCFA analyses. SR, MSR, TO, MCC, SS and EI contributed to the collection and assembly of data. SR, MSR, MCC, EI contributed to the writing and/or data interpretation. SR, MSR, MCC, EI wrote the manuscript and edit the manuscript. All authors read and approved the final manuscript.

Data availability statement

The 16S rRNA gene sequence data generated is available through NCBI Sequence Read Archive Database under project accession number BioProject ID PRJNA844901 is available from National Center for Biotechnology Information (NCBI) repository (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA844901). All supporting data are included in the manuscript.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2023.2234656

Additional information

Funding

The study was funded by The Academy of Finland (project 348914). The funding source had no involvement in study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication.