Environmental enrichment with nylon gnaw sticks introduces variation in Sprague Dawley rat immune and lower gastrointestinal parameters with differences between sexes

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Abstract

Background

Environmental enrichment (EE) is commonly included as an important component of animal housing to promote well being of laboratory animals; however, much remains to be learned about the impact of chewable forms of EE on experimental outcomes in the context of nutritional and microbiome-related studies, and whether outcomes differ between sexes. In the present study, nylon chew bones (gnaw sticks, GS) were evaluated for their effects on fermentation profiles, microbial community structure, and cytokine profiles of gastrointestinal and systemic tissues in pair-housed female and male Sprague Dawley (SD) rats.

Results

Food consumption and weight gain were not significantly altered by access to GS. Cecal short-chain fatty acid and branched-chain fatty acid profiles significantly differed between sexes in rats with access to GS, and alpha diversity of the microbiome decreased in females provided GS. Sex-related tissue cytokine profiles also significantly differed between rats with and without access to GS.

Conclusions

These findings indicate that including GS can influence microbiota and immune-related parameters, in a sex dependent manner. This shows that environmental enrichment strategies need to be clearly reported in publications to properly evaluate and compare experimental results, especially with respect to the use of chewable EE in the context of studies examining diet, microbiome and immune parameters.

Supplementary Information

The online version contains supplementary material available at 10.1186/s42523-024-00369-6.

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Most cited references 69

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Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform.

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Rapid advances in sequencing technology have changed the experimental landscape of microbial ecology. In the last 10 years, the field has moved from sequencing hundreds of 16S rRNA gene fragments per study using clone libraries to the sequencing of millions of fragments per study using next-generation sequencing technologies from 454 and Illumina. As these technologies advance, it is critical to assess the strengths, weaknesses, and overall suitability of these platforms for the interrogation of microbial communities. Here, we present an improved method for sequencing variable regions within the 16S rRNA gene using Illumina's MiSeq platform, which is currently capable of producing paired 250-nucleotide reads. We evaluated three overlapping regions of the 16S rRNA gene that vary in length (i.e., V34, V4, and V45) by resequencing a mock community and natural samples from human feces, mouse feces, and soil. By titrating the concentration of 16S rRNA gene amplicons applied to the flow cell and using a quality score-based approach to correct discrepancies between reads used to construct contigs, we were able to reduce error rates by as much as two orders of magnitude. Finally, we reprocessed samples from a previous study to demonstrate that large numbers of samples could be multiplexed and sequenced in parallel with shotgun metagenomes. These analyses demonstrate that our approach can provide data that are at least as good as that generated by the 454 platform while providing considerably higher sequencing coverage for a fraction of the cost.

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An Analysis of Transformations

G. BOX, D R Cox (1964)

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Gut/brain axis and the microbiota.

Emeran Mayer, Kirsten Tillisch, Arpana Gupta (2015)

Tremendous progress has been made in characterizing the bidirectional interactions between the central nervous system, the enteric nervous system, and the gastrointestinal tract. A series of provocative preclinical studies have suggested a prominent role for the gut microbiota in these gut-brain interactions. Based on studies using rodents raised in a germ-free environment, the gut microbiota appears to influence the development of emotional behavior, stress- and pain-modulation systems, and brain neurotransmitter systems. Additionally, microbiota perturbations by probiotics and antibiotics exert modulatory effects on some of these measures in adult animals. Current evidence suggests that multiple mechanisms, including endocrine and neurocrine pathways, may be involved in gut microbiota-to-brain signaling and that the brain can in turn alter microbial composition and behavior via the autonomic nervous system. Limited information is available on how these findings may translate to healthy humans or to disease states involving the brain or the gut/brain axis. Future research needs to focus on confirming that the rodent findings are translatable to human physiology and to diseases such as irritable bowel syndrome, autism, anxiety, depression, and Parkinson's disease.

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Author and article information

Contributors

Sandra T. Clarke: sandra.clarke2@agr.gc.ca

Journal

Journal ID (nlm-ta): Anim Microbiome

Journal ID (iso-abbrev): Anim Microbiome

Title: Animal Microbiome

Publisher: BioMed Central (London )

ISSN (Electronic): 2524-4671

Publication date (Electronic): 31 January 2025

Publication date PMC-release: 31 January 2025

Publication date Collection: 2025

Volume: 7

Electronic Location Identifier: 12

Affiliations

[1 ]Applied Bioscience Graduate Program, Faculty of Science, Ontario Tech University, ( https://ror.org/016zre027) Oshawa, ON Canada

[2 ]Bureau of Nutritional Sciences, Health Canada, ( https://ror.org/05p8nb362) Ottawa, ON Canada

[3 ]Kentville Research and Development Centre, Agriculture and Agri-Food Canada, ( https://ror.org/051dzs374) Kentville, NS Canada

[4 ]Guelph Research and Development Centre, Agriculture and Agri-Food Canada, ( https://ror.org/051dzs374) Guelph, ON Canada

Article

Publisher ID: 369

DOI: 10.1186/s42523-024-00369-6

PMC ID: 11786542

PubMed ID: 39891232

SO-VID: 647ea603-892d-4b43-907a-64e8efb51c3b

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 27 August 2024

Date accepted : 18 December 2024

Funding

Funded by: A-base funding at Health Canada

Award ID: SPJB

Funded by: Natural Sciences and Engineering Research Council of Canada Grant

Award ID: RGPIN-2017-05237

Custom metadata

Keywords: gnaw sticks,environmental enrichment,rat,gut microbiome,cytokines,nutrition,immune system,short chain fatty acids,sex-based differences

Data availability:

Keywords: gnaw sticks, environmental enrichment, rat, gut microbiome, cytokines, nutrition, immune system, short chain fatty acids, sex-based differences

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Environmental enrichment with nylon gnaw sticks introduces variation in Sprague Dawley rat immune and lower gastrointestinal parameters with differences between sexes

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Abstract

Background

Results

Conclusions

Supplementary Information

Related collections

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Most cited references 69

Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform.

An Analysis of Transformations

Gut/brain axis and the microbiota.

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Most referenced authors 663