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New Insights into the Role of Oral Microbiota Dysbiosis in the Pathogenesis of Inflammatory Bowel Disease

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Abstract

Inflammatory bowel disease (IBD) is a group of chronic intestinal inflammatory disorders with a prolonged duration characterized by recurrent relapse and remission. The exact etiology of IBD remains poorly understood despite the identification of relevant risk factors, including individual genetic susceptibility, environmental triggers, and disruption of immune homeostasis. Dysbiosis of the gut microbiota is believed to exacerbate the progression of IBD. Recently, increasing evidence has also linked oral microbiota dysbiosis with the development of IBD. On the one hand, IBD patients show significantly unbalanced composition and function of the oral microbiota known as dysbiosis. On the other, overabundances of oral commensal bacteria with opportunistic pathogenicity have been found in the gut microbiota of IBD patients. Herein, we review the current information on the causative factors of IBD, especially recent evidence of IBD-associated oral microbiota dysbiosis, which has seldom been covered in the previous literature review, highlighting the pathogenic mechanisms of specific oral bacteria in the development of IBD. Ectopic colonization of several oral bacteria, including a subset of Porphyromonas gingivalis, Streptococcus mutans, Fusobacterium nucleatum, Campylobacter concisus, and Klebsiella pneumoniae, may lead to destruction of the intestinal epithelial barrier, excessive secretion of inflammatory cytokines, disruption of the host immune system, and dysbiosis of gut microbiota, consequently aggravating chronic intestinal inflammation. Studying oral microbiota dysbiosis may open future horizons for understanding IBD pathogenesis and provide novel biomarkers for IBD. This review also presents the current treatment and new perspectives for IBD treatment.

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Abbreviations

APC:

Antigen-presenting cell

CBP:

Collagen-binding protein

Cc:

Campylobacter concisus

CCK:

Cholecystokinin

CD:

Crohn’s disease

CDI:

Clostridioides difficile infection

CPS:

Capsular polysaccharide

Cr:

Campylobacter rectus

Cu:

Campylobacter ureolyticus

EEN:

Exclusive enteral nutrition

EIMs:

Extra-intestinal manifestations

EPS:

Extracellular polymeric substances

FMT:

Fecal microbiota transplant

Fn:

Fusobacterium nucleatum

GI:

Gastrointestinal

HCs:

Healthy controls

IBD:

Inflammatory bowel disease

IC:

Indeterminate colitis

IECs:

Intestinal epithelial cells

IL:

Interleukin

Kp:

Klebsiella pneumoniae

LPS:

Lipopolysaccharides

MACs:

Microbiota-accessible carbohydrates

MAMP:

Microbe-associated molecular pattern

Pg:

Porphyromonas gingivalis

PN:

Parenteral nutrition

PRR:

Pattern recognition receptor

SCD:

Specific carbohydrate diet

SCFAs:

Short-chain fatty acids

S-ECC:

Severe early childhood caries

Sm:

Streptococcus mutans

TLR:

Toll-like receptors

TNF-α:

Tumor necrosis factor alpha

UC:

Ulcerative colitis

WSD:

Westernized diet

Zot:

Zonula occludens toxin

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Acknowledgments

We acknowledge Prof. Yonghe Luo at Jinling Hospital and Xuwen Liu at Middlebury Institute of International Studies at Monterey for their linguistic assistance.

Funding

This review was funded by the National Natural Science Foundation of China, grant nos. 81873559 and 81570506.

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Authors and Affiliations

  1. Department of Gastroenterology and Hepatology, Jinling Hospital, Medical School of Nanjing University, Zhongshan East Road 305, Nanjing, 210002, China

    Ying Qi, Hui-min Wu, Zhao Yang, Yi-fei Zhou, Miao-fang Yang & Fang-yu Wang

  2. Department of Stomatology, Jinling Hospital, Medical School of Nanjing University, Nanjing, China

    Lei Jin

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  1. Ying Qi
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Contributions

Conceptualization, FYW and YQ; writing: original draft preparation and figure design, YQ; writing: review and editing, HMW, ZY, and YFZ; revision, LJ and MFY; final revision: FYW. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Fang-yu Wang.

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Qi, Y., Wu, Hm., Yang, Z. et al. New Insights into the Role of Oral Microbiota Dysbiosis in the Pathogenesis of Inflammatory Bowel Disease. Dig Dis Sci 67, 42–55 (2022). https://doi.org/10.1007/s10620-021-06837-2

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