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Metformin Is Associated with Higher Relative Abundance of Mucin

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Metformin Is Associated with Higher Relative Abundance of Mucin 54 Diabetes Care Volume 40, January 2017 Jacobo de la Cuesta-Zuluaga,1 Metformin Is Associated With Noel T. Mueller,2 Vanessa Corrales-Agudelo,1 Higher Relative Abundance of Eliana P. Velasquez-Mej´ ´ıa,1 Jenny A. Carmona,3 Jose´ M. Abad,4 and Mucin-Degrading Akkermansia Juan S. Escobar1 muciniphila and Several Short- Chain Fatty Acid–Producing Microbiota in the Gut Diabetes Care 2017;40:54–62 | DOI: 10.2337/dc16-1324 OBJECTIVE Recent studies suggest the beneficial effects of metformin on glucose metabolism may be microbially mediated. We examined the association of type 2 diabetes, metformin, and gut microbiota in community-dwelling Colombian adults. On the basis of previous research, we hypothesized that metformin is associated with higher levels of short-chain fatty acid (SCFA)–producing and mucin-degrading microbiota. RESEARCH DESIGN AND METHODS Participants were selected from a larger cohort of 459 participants. The present analyses focus on the 28 participants diagnosed with diabetesd14 taking metformind and the 84 participants without diabetes who were matched (3-to-1) to participants with diabetes by sex, age, and BMI. We measured de- mographic information, anthropometry, and blood biochemical parameters and EMERGING TECHNOLOGIES AND THERAPEUTICS collected fecal samples from which we performed 16S rRNA gene sequencing to 1VidariumdNutrition, Health and Wellness Re- analyze the composition and structure of the gut microbiota. search Center, Grupo Empresarial Nutresa, Me- dellin, Colombia RESULTS 2Department of Epidemiology, Johns Hopkins fi Bloomberg School of Public Health, Baltimore, We found an association between diabetes and gut microbiota that was modi ed MD by metformin use. Compared with participants without diabetes, participants 3Dinamica´ I.P.S.dEspecialista en Ayudas Diag- with diabetes taking metformin had higher relative abundance of Akkermansia nosticas,´ Medellin, Colombia 4 muciniphila, a microbiota known for mucin degradation, and several gut micro- EPS y Medicina Prepagada Suramericana S.A., Medellin, Colombia biota known for production of SCFAs, including Butyrivibrio, Bifidobacterium fi Corresponding author: Juan S. Escobar, jsescobar@ bi dum, Megasphaera, and an operational taxonomic unit of Prevotella.In serviciosnutresa.com. contrast, compared with participants without diabetes, participants with Received 20 June 2016 and accepted 27 Septem- diabetes not taking metformin had higher relative abundance of Clostridiaceae ber 2016. 02d06 and a distinct operational taxonomic unit of Prevotella and a lower This article contains Supplementary Data online abundance of Enterococcus casseliflavus. at http://care.diabetesjournals.org/lookup/ suppl/doi:10.2337/dc16-1324/-/DC1. CONCLUSIONS © 2017 by the American Diabetes Association. Our results support the hypothesis that metformin shifts gut microbiota compo- Readers may use this article as long as the work sition through the enrichment of mucin-degrading A. muciniphila as well as sev- is properly cited, the use is educational and not for profit, and the work is not altered. More infor- eral SCFA-producing microbiota. Future studies are needed to determine if these mation is available at http://www.diabetesjournals shifts mediate metformin’s glycemic and anti-inflammatory properties. .org/content/license. care.diabetesjournals.org de la Cuesta-Zuluaga and Associates 55 Microbial communities (microbiota) and (11–13), a mucin-degrading bacteria to enrollment, and individuals diagnosed their associated genes (microbiome) that has been shown to reverse meta- with Alzheimer disease, Parkinson dis- constitute the interface of our environs bolic disorders (1,12). In humans, partic- ease, or any other neurodegenerative dis- and our cells, and their composition is ipants with diabetes taking metformin eases; current or recent cancer (,1year); believed to play a deterministic role in had similar abundance of Subdoligranu- and gastrointestinal diseases (Crohn dis- human health and disease. In particular, lum and, to some extent, Akkermansia ease, ulcerative colitis, short bowel syn- the development of type 2 diabetes, a compared with control subjects without drome, diverticulosis, or celiac disease). disease rising in prevalence around the diabetes, suggesting that metformin This study was conducted in accor- globe, has been linked in nonhuman (1) may help ameliorate a type 2 diabetes– dance with the principles of the Decla- and human (2–5) studies to imbalances associated gut microbiome (6). It has also ration of Helsinki, as revised in 2008, and in microbiota of the intestinal tract been shown that people with diabetes had minimal risk according to the (gut). However, the most recent human taking metformin had a higher relative Colombian Ministry of Health (Resolution study on this topic found that the asso- abundance of Adlercreutzia (17), and 008430 of 1993). All of the partici- ciation was modulated in a potent- metagenomic functional analyses dem- pants were thoroughly informed about ially beneficial manner by metformin onstrated significantly enhanced butyrate the study and procedures. Participants treatment (6). and propionate production in people with were assured of anonymity and confi- Metformin (1,1-dimethylbiguanide diabetes using metformin (6). In contrast, dentiality. Written informed consent was hydrochloride) is the most frequent people with diabetes who were not treat- obtained from all the participants before medication used to treat type 2 diabetes ed with metformin had a higher abun- beginning the study. The Bioethics (7), and findings from recent studies dance of Eubacterium and Clostridiaceae Committee of Sede de Investigacion´ suggest it may also prevent cancer (7) SMB53 (17) and lower levels of short- UniversitariadUniversity of Antioquia re- and cardiovascular events (8). Metfor- chain fatty acid (SCFA) producers, such viewed the protocol and the consent min has pleiotropic effects, yet the as Roseburia, Subdoligranulum,anda forms and approved the procedures de- majority of mechanistic studies have cluster of butyrate-producing Clostri- scribed here (approbation act 14–24–588 focused on changes in liver function diales (6). These findings provide evi- dated 28 May 2014). (7,9,10). Although metformin certainly dence that gut microbes may contribute Anthropometric, Clinical, and Dietary alters hepatic glucose production via to the antidiabetes effects of metformin Evaluations effects on AMPK, there is growing evi- through pathways that include mucin We calculated BMI as weight (kg)/height dence that the genesis of its action is in degradation and SCFA production. squared (m2) to classify participants as the gut (11–15). In this study we aimed to test the gen- lean (18.5 # BMI , 25.0 kg/m2), over- Metformin is ;50% bioavailable, al- eralizability of previous observations con- weight (25.0 # BMI , 30.0 kg/m2), or lowing for near-equal intestinal and cerning the influence of metformin on the obese (BMI $30 kg/m2). In addition, val- plasma exposure, but intestinal accumu- association of type 2 diabetes and gut ues of HDL, LDL, VLDL, total cholesterol, lation of metformin is 300 times that of dysbiosis in a Colombian adult popula- triglycerides, apolipoprotein B, fasting the plasma (16), making the gut the pri- tion. Given the considerable variation in glucose, glycated hemoglobin (HbA ), mary reservoir for metformin in humans. the microbiota associated with type 2 di- 1c fasting insulin, adiponectin, and hs-CRP Unlike oral administration, intravenous abetes and that the gut microbiota of Co- were obtained (collection and measure- administration of metformin in humans lombians is different to that of other ment explained in Supplementary Data). does not improve glycemia (14). More- populations (18), we hypothesized that Dietary intake was evaluated through over, in mice, oral administration of a the microbial taxa involved in the type 2 24-h dietary recalls (see Supplementary broad-spectrum antibiotic cocktail with diabetes dysbiosis of Colombians are dif- Data). oral metformin abrogates metformin’s ferent to those observed in Chinese and glucose-lowering effect (12). Providing European populations (2,3) but that the DNA Extraction and Sequence yet further evidence that the glucose- effect of metformin is similar, i.e., through Analysis lowering effect of metformin may originate enrichment of mucin-degrading and SCFA- Each participant collected their own fe- in the lower bowel, a delayed-release oral producing microbiota. cal sample in a hermetically sealed, ster- metformin, which targets the ileum, ile receptacle provided by the research had a similar or greater glucose-lowering RESEARCH DESIGN AND METHODS team. Samples were immediately refrig- effect than immediate-release or extended- Study Design erated in household freezers and brought release metformin, despite the delayed- Between July and November 2014, we en- to an EPS SURA facility in each city within release metformin having lower systemic rolled 459 men and women 18–62 years 12 h; receipt of samples occurred exclu- 2 exposure than the other metformin for- old, with BMI $18.5 kg/m , living in sively in the morning (6 A.M.–12 P.M.). As mulations (15). the Colombian cities of Medellin, Bogota, such, stools were collected between the Recent studies in animals (11,12,13) Barranquilla, Bucaramanga, and Cali. All evening of the day before and the morn- and humans (6,17) provide evidence participants enrolled in the study were in- ing of the day of sample receipt. Fecal that metformin may partially
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