Publication Cover
Archives of Physiology and Biochemistry
The Journal of Metabolic Diseases
Volume 129, 2023 - Issue 3
908
Views
11
CrossRef citations to date
0
Altmetric
Review Articles

A comprehensive systematic review of the effectiveness of Akkermansia muciniphila, a member of the gut microbiome, for the management of obesity and associated metabolic disorders

, , , , , , ORCID Icon, , ORCID Icon & ORCID Icon show all
Pages 741-751 | Received 11 Sep 2020, Accepted 30 Dec 2020, Published online: 15 Jan 2021

References

  • Abdelaal, M., le Roux, C.W., and Docherty, N.G., 2017. Morbidity and mortality associated with obesity. Annals of translational medicine, 5 (7), 161.
  • Afshin, A., et al., 2017. Health effects of overweight and obesity in 195 Countries over 25 years. The New England journal of medicine, 377 (1), 13–27.
  • Alard, J., et al., 2016. Beneficial metabolic effects of selected probiotics on diet-induced obesity and insulin resistance in mice are associated with improvement of dysbiotic gut microbiota. Environmental microbiology, 18 (5), 1484–1497.
  • Anhê, F.F., et al., 2019. Treatment with camu camu (Myrciaria dubia) prevents obesity by altering the gut microbiota and increasing energy expenditure in diet-induced obese mice. Gut, 68 (3), 453–464.
  • Anhê, F.F., et al., 2018. Arctic berry extracts target the gut-liver axis to alleviate metabolic endotoxaemia, insulin resistance and hepatic steatosis in diet-induced obese mice. Diabetologia, 61 (4), 919–931.
  • Anoop, S., et al., 2017. High circulating plasma dipeptidyl peptidase-4 levels in non-obese Asian Indians with type 2 diabetes correlate with fasting insulin and LDL-C levels, triceps skinfolds, total intra-abdominal adipose tissue volume and presence of diabetes: a case–control study. BMJ open diabetes research and care, 5, bmjdrc-2017-000393.
  • Arias, M., et al., 2017. Gut microbiota and systemic inflammation changes after bread consumption: the ingredients and the processing influence. Journal of functional foods, 32, 98–105.
  • Ashrafian, F., et al., 2019. Akkermansia muciniphila-derived extracellular vesicles as a mucosal delivery vector for amelioration of obesity in mice. Frontiers in microbiology, 10, 2155.
  • Baboota, R.K., et al., 2014. Capsaicin-induced transcriptional changes in hypothalamus and alterations in gut microbial count in high fat diet fed mice. Journal of Nutritional Biochemistry , 25 (9), 893–902.
  • Backhed, F., et al., 2004. The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the national academy of sciences of the United States of America, 101 (44), 15718–15723.
  • Baldwin, J., et al., 2016. Table grape consumption reduces adiposity and markers of hepatic lipogenesis and alters gut microbiota in butter fat-fed mice. The journal of nutritional biochemistry, 27, 123–135.
  • Bang, S.-J., et al., 2019. Effect of raw potato starch on the gut microbiome and metabolome in mice. International journal of biological macromolecules, 133, 37–43.
  • Bekiares, N., et al., 2018. Effect of sweetened dried cranberry consumption on urinary proteome and fecal microbiome in healthy human subjects. Omics: A journal of integrative biology, 22 (2), 145–153.
  • Bohan, R., et al., 2019. Gut microbiota: a potential manipulator for host adipose tissue and energy metabolism. The journal of nutritional biochemistry, 64, 206–217.
  • Burokas, A., et al., 2017. Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biological psychiatry, 82 (7), 472–487.
  • Caesar, R., et al., 2015. Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell metabolism, 22 (4), 658–668.
  • Cani, P.D., et al., 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes, 56 (7), 1761–1772.
  • Cani, P.D., and de Vos, W.M., 2017. Next-generation beneficial microbes: the case of Akkermansia muciniphila. Frontiers in microbiology, 8, 1765.
  • Cani, P.D., et al., 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut, 58 (8), 1091–1103.
  • Cani, P.D., et al., 2019. Microbial regulation of organismal energy homeostasis. Nature metabolism, 1 (1), 34–46.
  • Chelakkot, C., et al., 2018. Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Experimental & molecular medicine, 50 (2), e450.
  • Cooper, D.N., et al., 2017. The effects of moderate whole grain consumption on fasting glucose and lipids, gastrointestinal symptoms, and microbiota. Nutrients, 9 (2), 173.
  • Cowan, S.F., et al., 2020. Effect of whole foods and dietary patterns on markers of subclinical inflammation in weight-stable overweight and obese adults: a systematic review. Nutrition reviews, 78 (1), 19–38.
  • d’Hennezel, E., et al., 2017. Total lipopolysaccharide from the human gut microbiome silences toll-like receptor signaling. mSystems, 2 (6), e00046–00017.
  • Depommier, C., et al., 2019. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nature medicine, 25 (7), 1096–1103.
  • Derrien, M., et al., 2004. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. International journal of systematic and evolutionary microbiology, 54 (Pt 5), 1469–1476.
  • Everard, A., et al., 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proceedings of the national academy of sciences of the United States of America, 110 (22), 9066–9071.
  • Everard, A., et al., 2011. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes, 60 (11), 2775–2786.
  • Everard, A., et al., 2014. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. The ISME Journal, 8 (10), 2116–2130.
  • Everard, A., et al., 2019. Intestinal epithelial N-acylphosphatidylethanolamine phospholipase D links dietary fat to metabolic adaptations in obesity and steatosis. Nature communications, 10 (1), 17.
  • Flint, H.J., et al., 2008. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature reviews microbiology, 6 (2), 121–131.
  • Fujio-Vejar, S., et al., 2017. The Gut microbiota of healthy chilean subjects reveals a high abundance of the Phylum Verrucomicrobia. Frontiers in microbiology, 8, 1221.
  • Gaggia, F., Mattarelli, P., and Biavati, B., 2010. Probiotics and prebiotics in animal feeding for safe food production. International journal of food microbiology, 141, S15–S28.
  • Gao, X., et al., 2017. Polyphenol-and caffeine-rich postfermented pu-erh tea improves diet-induced metabolic syndrome by remodeling intestinal homeostasis in mice. Infection and immunity, 86 (1), e00601–00617.
  • Ghezzal, S., et al., 2020. Palmitic acid damages gut epithelium integrity and initiates inflammatory cytokine production. Biochimica et Biophysica Acta (BBA)–Molecular and cell biology of lipids, 1865, 158530.
  • Gowd, V., et al., 2019. Dietary fibers as emerging nutritional factors against diabetes: focus on the involvement of gut microbiota. Critical reviews in biotechnology, 39 (4), 524–540.
  • Hansson, G.C., 2012. Role of mucus layers in gut infection and inflammation. Current opinion in microbiology, 15 (1), 57–62.
  • Henao-Mejia, J., et al., 2012. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature, 482 (7384), 179–185.
  • Henning, S.M., et al., 2017. Pomegranate ellagitannins stimulate the growth of Akkermansia muciniphila in vivo. Anaerobe, 43, 56–60.
  • Hooda, S., et al., 2012. 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. The journal of nutrition, 142 (7), 1259–1265.
  • Johansen, O.E., et al., 2012. Cardiovascular safety with linagliptin in patients with type 2 diabetes mellitus: a pre-specified, prospective, and adjudicated meta-analysis of a phase 3 programme. Cardiovascular diabetology, 11 (1), 3.
  • Karlsson, C.L., et al., 2012. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity, 20 (11), 2257–2261.
  • Katiraei, S., et al., 2019. Akkermansia muciniphila exerts lipid-lowering and immunomodulatory effects without affecting neointima formation in hyperlipidemic APOE* 3-Leiden. CETP Mice. Molecular nutrition & food research, 64 (15), 1900732.
  • Kim, S., et al., 2020. Akkermansia muciniphila prevents fatty liver disease, decreases serum triglycerides, and maintains gut homeostasis. Applied and environmental microbiology, 86 (7), 19.
  • Lawenius, L., et al., 2020. Pasteurized Akkermansia muciniphila protects from fat mass gain but not from bone loss. American journal of physiology-endocrinology and metabolism, 318 (4), E480–E491.
  • Li, Z., et al., 2015. Pomegranate extract induces ellagitannin metabolite formation and changes stool microbiota in healthy volunteers. Food & function, 6 (8), 2487–2495.
  • Li, J., et al., 2016. Akkermansia muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in Apoe–/– Mice. Circulation, 133 (24), 2434–2446.
  • Li, X., Watanabe, K., and Kimura, I., 2017. Gut microbiota dysbiosis drives and implies novel therapeutic strategies for diabetes mellitus and related metabolic diseases. Frontiers in immunology, 8, 1882.
  • Macchione, I.G., et al., 2019. Akkermansia muciniphila: key player in metabolic and gastrointestinal disorders. European review for medical and pharmacological sciences , 23 (18), 8075–8083.
  • Mannucci, E., et al., 2005. Hyperglycaemia increases dipeptidyl peptidase IV activity in diabetes mellitus. Diabetologia, 48 (6), 1168–1172.
  • Meng, X., et al., 2019. A purified aspartic protease from Akkermansia muciniphila plays an important role in degrading Muc2. International journal of molecular sciences, 21 (1), 72.
  • Monk, J.M., et al., 2016. Navy bean supplementation in obesity increases Akkermansia muciniphila abundance and attenuates obesity related impairments in gut barrier function. The FASEB journal, 30, 421.422.
  • Ndisang, J.F., Vannacci, A., and Rastogi, S., 2014. Oxidative stress and inflammation in obesity, diabetes, hypertension, and related cardiometabolic complications. Oxidative medicine and cellular longevity, 2014, 1–3.
  • Organization, W. H. 2016. World Health Organization obesity and overweight fact sheet.
  • Pahlavani, N., et al., 2020a. Molecular and cellular mechanisms of the effects of Propolis in inflammation, oxidative stress and glycemic control in chronic diseases. Nutrition & metabolism, 17 (1), 12.
  • Pahlavani, N., et al., 2020b. Nuts effects in chronic disease and relationship between walnuts and satiety: review on the available evidence. Obesity medicine, 17, 100173.
  • Pahlavani, N., et al., 2019. Possible molecular mechanisms of glucose-lowering activities of Momordica charantia (Karela) in diabetes. Journal of cellular biochemistry, 120 (7), 10921–10929.
  • Payahoo, L., et al., 2019. Investigation the effect of oleoylethanolamide supplementation on the abundance of Akkermansia muciniphila bacterium and the dietary intakes in people with obesity: a randomized clinical trial. Appetite, 141, 104301.
  • Peng, G.C., and Hsu, C.H., 2005. The efficacy and safety of heat-killed Lactobacillus paracasei for treatment of perennial allergic rhinitis induced by house-dust mite. Pediatric allergy and immunology, 16 (5), 433–438.
  • Plovier, H., et al., 2017. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nature medicine, 23 (1), 107–113.
  • Ramnani, P., et al., 2010. Prebiotic effect of fruit and vegetable shots containing Jerusalem artichoke inulin: a human intervention study. British journal of nutrition, 104 (2), 233–240.
  • Roopchand, D.E., et al., 2015. Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet-induced metabolic syndrome. Diabetes, 64 (8), 2847–2858.
  • Roshanravan, N., et al., 2018. The effects of sodium butyrate and high-performance inulin supplementation on the promotion of gut bacterium Akkermansia muciniphila growth and alterations in miR-375 and KLF5 expression in type 2 diabetic patients: a randomized, double-blind, placebo-controlled trial. European journal of integrative medicine, 18, 1–7.
  • Salguero, M.V., et al., 2019. Dysbiosis of Gram-negative gut microbiota and the associated serum lipopolysaccharide exacerbates inflammation in type 2 diabetic patients with chronic kidney disease. Experimental and therapeutic medicine, 18, 3461–3469.
  • Sarkar, J., et al., 2019. Increased plasma dipeptidyl peptidase-4 (DPP4) activity is an obesity-independent parameter for glycemic deregulation in type 2 diabetes patients. Frontiers in endocrinology, 10, 505.
  • Schneeberger, M., et al., 2015. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Scientific reports, 5 (1), srep16643.
  • Shin, J., et al., 2019. Elucidation of akkermansia muciniphila probiotic traits driven by mucin depletion. Frontiers in microbiology, 10, 1137.
  • Stengel, A., et al., 2014. Obese patients have higher circulating protein levels of dipeptidyl peptidase IV. Peptides, 61, 75–82.
  • Tamboli, C.P., et al., 2004. Dysbiosis in inflammatory bowel disease. Gut, 53 (1), 1–4.
  • Verhoog, S., et al., 2019. Dietary factors and modulation of bacteria strains of Akkermansia muciniphila and Faecalibacterium prausnitzii: a systematic review. Nutrients, 11 (7), 1565.
  • Vreugdenhil, A.C., et al., 1999. Lipopolysaccharide binding protein and serum amyloid A secretion by human intestinal epithelial cells during the acute phase response. Journal of immunology, 163 (5), 2792–2798.
  • Wallace, T.C., et al., 2011. Human gut microbiota and its relationship to health and disease. Nutrition reviews, 69 (7), 392–403.
  • Wang, J.-H., et al., 2015. Fermented Rhizoma Atractylodis macrocephalae alleviates high fat diet-induced obesity in association with regulation of intestinal permeability and microbiota in rats. Scientific reports, 5 (1), 8391.
  • Wronkowitz, N., et al., 2014. Soluble DPP4 induces inflammation and proliferation of human smooth muscle cells via protease-activated receptor 2. Biochimica et Biophysica Acta (Bba) – Molecular basis of disease, 1842 (9), 1613–1621.
  • Wu, F., et al., 2020. An Akkermansia muciniphila subtype alleviates high-fat diet-induced metabolic disorders and inhibits the neurodegenerative process in mice. Anaerobe, 61, 102138.
  • Xu, Y., et al., 2020. Function of Akkermansia muciniphila in obesity: interactions with lipid metabolism, immune response and gut systems. Frontiers in microbiology., 11, 219.
  • Yang, J., and Xiao, Y.Y., 2013. Grape phytochemicals and associated health benefits. Critical reviews in food science and nutrition, 53 (11), 1202–1225.
  • Yang, Y., et al., 2019. Early-life high-fat diet-induced obesity programs hippocampal development and cognitive functions via regulation of gut commensal Akkermansia muciniphila. Neuropsychopharmacology: official publication of the American College of neuropsychopharmacology, 44 (12), 2054–2064.
  • Zhang, Z., et al., 2019. Impact of fecal microbiota transplantation on obesity and metabolic syndrome–a systematic review. Nutrients, 11, 2291.
  • Zhao, S., et al., 2017. Akkermansia muciniphila improves metabolic profiles by reducing inflammation in chow diet-fed mice. Journal of molecular endocrinology, 58 (1), 1–14.
  • Zhong, Y., Nyman, M., and Fåk, F., 2015. Modulation of gut microbiota in rats fed high-fat diets by processing whole-grain barley to barley malt. Molecular nutrition & food research, 59 (10), 2066–2076.
  • Zhong, J., Rao, X., and Rajagopalan, S., 2013. An emerging role of dipeptidyl peptidase 4 (DPP4) beyond glucose control: potential implications in cardiovascular disease. Atherosclerosis, 226 (2), 305–314.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.