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Altered gut microbiota ameliorates bone pathology in the mandible of obese–insulin-resistant rats

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Abstract

Purpose

The chronic consumption of a high-fat diet (HFD) induces obese–insulin resistance and impairs jawbone health via gut dysbiosis-stimulated inflammatory process. Our previous studies demonstrated that the probiotic Lactobacillus paracasei HII01, prebiotic xylooligosaccharide (XOS), and synbiotics improved several vital organ functions by reducing gut dysbiosis in HFD-induced obese rats. However, the impacts on the cellular level of jawbone microarchitecture have not been examined. Here, we hypothesized that the supplementation of L. paracasei HII01, XOS, and synbiotics ameliorated the bone microarchitectural pathology in HFD-fed rats by reducing systemic inflammation and other metabolic parameters.

Methods

The dietary regimes (normal or high-fat diet) were provided to 48 male Wistar rats throughout 24-week experiment. After week 12, rats were given either a vehicle, pro-, pre-, or synbiotic for an additional 12 weeks before being killed. Then, blood analyses and bone histomorphometry of the jawbones were performed.

Results

The HFD-fed rats developed obese–insulin resistance with significantly elevated systemic inflammation. Bone histomorphometry of these rats showed a decrease in trabecular thickness with increased osteoclasts and active erosion surfaces. Mineral apposition and bone-formation rates were also remarkably diminished. The treatment with pro-, pre-, and synbiotics equally improved metabolic disturbance, reduced systemic inflammation, increased trabecular thickness, decreased osteoclasts and active erosion surfaces and restored mineral apposition and bone-formation rates.

Conclusion

The probiotic L. paracasei HII01, prebiotic XOS, and the synbiotics had similarly beneficial effects to improve jawbone microarchitecture in HFD-fed rats by possibly ameliorating osteoclast-related bone resorption and potentiating bone-formation activities.

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Acknowledgements

This work was supported by Thailand Research Fund (TRF) Grants: TRF-Senior Research Scholar RTA6080003 (to SCC), RTA6080007 (to N. Charoenphandhu), IRN60W0001 (to N. Charoenphandhu) and MRG6180187 (to PT); Mahidol University (to N. Charoenphandhu); a CMU 50th Anniversary Grant by Chiang Mai University (PHD/014/2557 SE&SCC); a NSTDA Research Chair Grant from the National Science and Technology Development Agency Thailand (N. Chattipakorn) and a Chiang Mai University Center of Excellence Award (N. Chattipakorn).

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Authors and Affiliations

  1. Department of Orthodontics and Pediatric Dentistry, Faculty of Dentistry, Chiang Mai University, Chiang Mai, 50200, Thailand

    Sathima Eaimworawuthikul

  2. Department of Oral Biology and Diagnostic Sciences, Faculty of Dentistry, Chiang Mai University, Chiang Mai, 50200, Thailand

    Sathima Eaimworawuthikul & Siriporn C. Chattipakorn

  3. Neurophysiology Unit, Center of Excellence in Cardiac Electrophysiology Research and Training Center, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand

    Sathima Eaimworawuthikul, Wannipa Tunapong, Titikorn Chunchai, Nipon Chattipakorn & Siriporn C. Chattipakorn

  4. Department of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand

    Parameth Thiennimitr

  5. Center of Calcium and Bone Research (COCAB), Faculty of Science, Mahidol University, Bangkok, 10400, Thailand

    Panan Suntornsaratoon & Narattaphol Charoenphandhu

  6. Department of Physiology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand

    Panan Suntornsaratoon & Narattaphol Charoenphandhu

  7. Institute of Molecular Biosciences, Mahidol University, Nakhon Pathom, 73170, Thailand

    Narattaphol Charoenphandhu

  8. The Academy of Science, The Royal Society of Thailand, Dusit, Bangkok, 10300, Thailand

    Narattaphol Charoenphandhu

Authors
  1. Sathima Eaimworawuthikul
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  2. Wannipa Tunapong
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  3. Titikorn Chunchai
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  4. Panan Suntornsaratoon
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  5. Narattaphol Charoenphandhu
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  6. Parameth Thiennimitr
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  7. Nipon Chattipakorn
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  8. Siriporn C. Chattipakorn
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Contributions

The authors’ responsibilities were as follows—SE, PT, and NC and SCC: designed the research; SE, WT, and TC: conducted the research; PS, NC, and PT: provided essential materials; SE, NC, and SCC: analyzed the data; SE, NC, NC, and SCC: wrote the manuscript; SCC: had primary responsibility for the final content; and all authors: read and approved the final manuscript.

Corresponding author

Correspondence to Siriporn C. Chattipakorn.

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Eaimworawuthikul, S., Tunapong, W., Chunchai, T. et al. Altered gut microbiota ameliorates bone pathology in the mandible of obese–insulin-resistant rats. Eur J Nutr 59, 1453–1462 (2020). https://doi.org/10.1007/s00394-019-02002-8

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  • DOI: https://doi.org/10.1007/s00394-019-02002-8

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