Mycotoxin Exposure and Early Life Gut Microbiome Development in Nigerian Neonates and Infants

Certain molds found in foodstuffs such as grains, nuts and dried fruit produce mycotoxins that, when consumed, can have devastating short- and long-term effects on our health. The interaction between mycotoxins and the gut microbiome is complex and can also contribute to the impact they have. A study from the University of Vienna, published in Environmental Science and Technology, delves into this relationship. Using advanced methods including liquid chromatography-tandem mass spectrometry (LC-MS/MS), the researchers recruited mother–infant dyads from Babcock University Teaching Hospital in Nigeria and local households to investigate the potential influence of mycotoxins' on the gut microbiota during early development.

Exploring the hidden hazards of early mycotoxin exposure

Knowledge gaps persist in our understanding of how mycotoxin exposure influences the development of the gut microbiota (GM) in neonates and infants (NIs). Given the pivotal role of the gut microbiome in various physiological functions, including digestion and immune modulation, better understanding this bidirectional relationship during the neonatal period is crucial. The current study investigated mycotoxin exposure patterns in NIs, utilizing an extensive analysis of three biospecimens—breast milk, stool and urine—across an 18-month postdelivery timeframe in Sub-Saharan Africa (SSA). Through this examination of GM composition in a mycotoxin-exposed cohort, this study explored potential longitudinal associations between mycotoxin exposure and GM development. This research illuminated critical aspects of early gut health, particularly within the first 500 days of life, in this vulnerable population.

Microbial shifts: Tracking changes in mycotoxin levels and neonatal gut composition

In this pilot longitudinal biomonitoring study, 14 mother–infant dyads were recruited to participate. Samples of breast milk, complementary/solid foods, stool and urine were collected from neonates and infants at 3-month intervals up to 18 months postdelivery. Stool samples, collected by mothers, were divided into two batches for mycotoxin and microbiota analysis. Mycotoxin analysis employed LC-MS/MS methods, while microbial analysis utilized 16S rRNA gene amplicon sequencing. Statistical analyses including PERMANOVA, redundancy analysis (RDA) and MaAsLin2 were employed to investigate associations between mycotoxin exposure and gut microbiota composition.

The key findings of the paper were:

• Breast milk and stool samples indicated exposure to multiple mycotoxins; 13 out of the 34 mycotoxins tested for were detected in breast milk samples, including aflatoxin B₁ (AFB₁), aflatoxin M₁ (AFM₁), ochratoxin A (OTA) and citrinin (CIT).
• Despite evidence of high aflatoxin exposure through complementary foods, aflatoxins were not detected in stool samples, possibly due to biotransformation or metabolism.
• Urine samples showed recent exposure to mycotoxins, emphasizing the importance of monitoring for potential health impacts. Ten mycotoxins were detected in urine samples, including AFM₁, AFB₂, FB₁, deoxynivalenol (DON), OTA and CIT.
• Mycotoxins were detected in NIs’ stools, primarily coinciding with increased cofeeding with complementary foods. Fumonisin B₁ (FB₁), FB₂ and alternariol monomethyl ether (AME) were quantifiable in stools between months 6 and 18, indicating continuous exposure during critical developmental periods.
• The diversity of gut microbiota increased significantly over time, with mycotoxin presence associated with alterations in microbial composition, particularly with the genus Clostridioides.

Mycotoxins may influence neonates' gut composition and immune responses

Through a longitudinal biomonitoring approach, the researchers identified several mycotoxins, including aflatoxins, fumonisins, ochratoxin A and others, in the participants’ biospecimens. Notably, some mycotoxins found in complementary foods were also detected in stool samples, indicating the potential for a link between mycotoxin exposure and the composition of the gut microbiome in Nigerian infants. Firmicutes, Proteobacteria, Actinobacteriota and Bacteroidota were the dominant GM phyla observed overall. The study unveiled dynamic shifts in GM composition over time, with notable increases in diversity as the infants aged. These findings underscore the delicate balance of bacterial levels within the gut microbiome, which plays a key role in protecting against harmful agents and maintaining overall equilibrium. The correlation between dietary mycotoxin exposure and changes in GM composition highlights potential implications for neonatal and infant health.

Despite the sparse detection of quantifiable individual mycotoxins, a significant association was found between the presence of mycotoxins in stool samples and GM composition. While the specific bacteria contributing to this variation remain unclear, taxa such as Clostridioides difficile were notably associated with mycotoxin presence. These findings suggest a potential link between mycotoxin exposure and shifts in GM composition, which could have immunomodulatory implications with potential adverse consequences. The study underscores the need for further research to elucidate the causal relationship between mycotoxin exposure and GM alterations in early development.

This study has several limitations that warrant consideration. To begin with, the small sample size of 14 participants, compounded by challenges in cohort recruitment and incomplete sample collection at all time points, may limit the generalizability of the findings. Secondly, the study did not include a control group as it was unable to obtain microbiome data from a similar cohort that consumed a mycotoxin-free diet. Additionally, the dichotomous categorization of mycotoxin presence (detected vs. non-detected) oversimplifies the complex nature of mycotoxin presence and exposure, which can vary in its mode of action. Lastly, only mycotoxins were analyzed in the biospecimens, but other factors may influence the NIs’ gut microbiome. It is important to consider the potential influence of other environmental toxicants on the gut microbiota, increasing food diversity and overall exposure to the environment as infants age, as well as the impact of a maturing immune system. Despite these limitations, this study represents a crucial step towards understanding the interplay between chemical exposome and microbiome interactions in early life, particularly in regions like sub-Saharan Africa where such research is still in its infancy.

Advancing our understanding of chemical−microbial interactions for early life gut health

Future studies should explore wider chemical interactions and investigate the prevalence of specific bacterial taxa in early life stools, while also examining in vitro models to understand species interactions with mycotoxins more comprehensively. This research sets the stage for larger-scale studies across different geographical regions to deepen our understanding of these complex dynamics.

Reference:  Ayeni KI, Seki D, Pjevac P, et al. Biomonitoring of dietary mycotoxin exposure and associated impact on the gut microbiome in Nigerian infants. Environ Sci Technol. 2024;58(5):2236–2246. doi:10.1021/acs.est.3c07786

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