Abstract
Purposes
The objectives of this study were to investigate differences in gut microbiota (GM) composition after high dairy intake (HD) compared to adequate dairy intake (AD) and to correlate GM composition variations with the change in glycemic parameters in hyperinsulinemic subjects.
Methods
In this crossover study, 10 hyperinsulinemic adults were randomized to HD (≥ 4 servings/day) or AD (≤ 2 servings/day) for 6 weeks, separated by a 6-week washout period. Fasting insulin and glucose levels were measured after each intervention. Insulin resistance was calculated with the homeostasis model assessment of insulin resistance (HOMA-IR). GM was determined with 16S rRNA-based high-throughput sequencing at the end of each intervention. Paired t test, correlations and machine learning analyses were performed.
Results
Endpoint glycemic parameters were not different between HD and AD intake. After HD compared with AD intake, there was a decrease in the abundance of bacteria in Roseburia and Verrucomicrobia (p = 0.04 and p = 0.02, respectively) and a trend for an increase abundance in Faecalibacteria and Flavonifractor (p = 0.05 and p = 0.06, respectively). The changes in abundance of Coriobacteriia, Erysipelotrichia, and Flavonifractor were negatively correlated with the change in HOMA-IR between the AD and HD phases. Furthermore, a predictive GM signature, including Anaerotruncus, Flavonifractor, Ruminococcaceae, and Subdoligranulum, was related to HOMA-IR.
Conclusion
Overall, these results suggest that HD modifies the abundance of specific butyrate-producing bacteria in Firmicutes and of bacteria in Verrucomicrobia in hyperinsulinemic individuals. In addition, the butyrate producing bacteria in Firmicutes phylum correlate negatively with insulin resistance.
Similar content being viewed by others
References
Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14:e1002533
Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Reddy DN (2015) Role of the normal gut microbiota. World J Gastroenterol 21:8787
Rajoka MSR, Shi J, Mehwish HM, Zhu J, Li Q, Shao D, Huang Q, Yang H (2017) Interaction between diet composition and gut microbiota and its impact on gastrointestinal tract health. Food Sci Hum Wellness 6:121–130
Liang D, Leung RKK, Guan W, Au WW (2018) Involvement of gut microbiome in human health and disease: brief overview, knowledge gaps and research opportunities. Gut pathog 10:3
Bo T, Shao S, Wu D, Niu S, Zhao J, Gao L (2017) Relative variations of gut microbiota in disordered cholesterol metabolism caused by high-cholesterol diet and host genetics. Microbiol Open 6:e00491
Valle Gottlieb MG, Closs VE, Junges VM, Schwanke CHA (2018) Impact of human aging and modern lifestyle on gut microbiota. Crit Rev Food Sci Nutr 58:1557–1564
Navab-Moghadam F, Sedighi M, Khamseh ME, Alaei-Shahmiri F, Talebi M, Razavi S, Amirmozafari N (2017) The association of type II diabetes with gut microbiota composition. Microbial Pathog 110:630–636
Azcarate-Peril MA, Ritter AJ, Savaiano D, Monteagudo-Mera A, Anderson C, Magness ST, Klaenhammer TR (2017) Impact of short-chain galactooligosaccharides on the gut microbiome of lactose-intolerant individuals. Proc Natl Acad Sci 114:E367–E375
Ferrocino I, Ponzo V, Gambino R, Zarovska A, Leone F, Monzeglio C, Goitre I, Rosato R, Romano A, Grassi G (2018) Changes in the gut microbiota composition during pregnancy in patients with gestational diabetes mellitus (GDM). Sci Rep 8:12216
Liu H, Zhang H, Wang X, Yu X, Hu C, Zhang X (2018) The family Coriobacteriaceae is a potential contributor to the beneficial effects of Roux-en-Y gastric bypass on type 2 diabetes. Surg Obes Relat Dis 14:584–593
Wang Y, Luo X, Mao X, Tao Y, Ran X, Zhao H, Xiong J, Li L (2017) Gut microbiome analysis of type 2 diabetic patients from the Chinese minority ethnic groups the Uygurs and Kazaks. PLoS ONE 12:e0172774
Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490:55
Aydin Ö, Nieuwdorp M, Gerdes V (2018) The gut microbiome as a target for the treatment of type 2 diabetes. Curr Diabetes Rep 18:55
Gao D, Ning N, Wang C, Wang Y, Li Q, Meng Z, Liu Y, Li Q (2013) Dairy products consumption and risk of type 2 diabetes: systematic review and dose-response meta-analysis. PLoS ONE 8:e73965
Aune D, Norat T, Romundstad P, Vatten LJ (2013) Dairy products and the risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies. Am J Clin Nutr 98:1066–1083
Smith-Brown P, Morrison M, Krause L, Davies P (2016) Dairy and plant based food intakes are associated with altered faecal microbiota in 2 to 3 year old Australian children. Sci Rep 6:32385
Suzuki Y, Ikeda K, Sakuma K, Kawai S, Sawaki K, Asahara T, Takahashi T, Tsuji H, Nomoto K, Nagpal R (2017) Association between yogurt consumption and intestinal microbiota in healthy young adults differs by host gender. Front Microbiol 8:847
Li X, Yin J, Zhu Y, Wang X, Hu X, Bao W, Huang Y, Chen L, Chen S, Yang W (2018) Effects of whole milk supplementation on gut microbiota and cardiometabolic biomarkers in subjects with and without lactose malabsorption. Nutrients 10:1403
Chen EA et al (2018) Dairy intake and mucosa-associated gut microbiome in healthy individuals: Presidential Poster Award:235. Am J Gastroenterol 113:S37
O'Connor S, Weisnagel SJ, Gagnon C, Rudkowska I (2019) Impact of a high intake of dairy product on insulin sensitivity in hyperinsulinemic adults: a cross-over randomized controlled trial. Curr Dev Nutr 3:nzz083
Passey RB, Gillum RL, Fuller JB, Urry FM, Giles ML (1977) Evaluation and comparison of 10 glucose methods and the reference method recommended in the proposed product class standard (1974). Clin Chem 23:131–139
Kirk RE, Othmer Donald F, Standen A, Scott JD (1947) Encyclopedia of chemical technology. The Interscience Encyclopedia, Inc., New York
Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J (2017) Microbiome analyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188
De Candia P, Spinetti G, Specchia C, Sangalli E, La Sala L, Uccellatore A, Lupini S, Genovese S, Matarese G, Ceriello A (2017) A unique plasma microRNA profile defines type 2 diabetes progression. PLoS ONE 12:e0188980
Alexander WM, Ficarro SB, Adelmant G, Marto JA (2017) multiplierz v2. 0: A Python-based ecosystem for shared access and analysis of native mass spectrometry data. Proteomics 17:1700091
Healey GR, Murphy R, Brough L, Butts CA, Coad J (2017) Interindividual variability in gut microbiota and host response to dietary interventions. Nutr Rev 75:1059–1080
Fujio-Vejar S, Vasquez Y, Morales P, Magne F, Vera-Wolf P, Ugalde JA, Navarrete P, Gotteland M (2017) The gut microbiota of healthy chilean subjects reveals a high abundance of the phylum verrucomicrobia. Front Microbiol 8:1221
Zhang X, Shen D, Fang Z, Jie Z, Qiu X, Zhang C, Chen Y, Ji L (2013) Human gut microbiota changes reveal the progression of glucose intolerance. PLoS ONE 8:e71108
Chen E, Ajami N, Chen L, Plew S, White D, Wang Z, El-Serag H, Petrosino J, Jiao L (2018) Dairy intake and mucosa-associated gut microbiome in healthy individuals: Presidential Poster Award. Am J Gastroenterol 113:S137
Burton KJ, Rosikiewicz M, Pimentel G, Bütikofer U, Von Ah U, Voirol M-J, Croxatto A, Aeby S, Drai J, McTernan PG (2017) Probiotic yogurt and acidified milk similarly reduce postprandial inflammation and both alter the gut microbiota of healthy, young men. Br J Nutr 117:1312–1322
Saeb AT, Al-Rubeaan KA, Aldosary K, Raja GU, Mani B, Abouelhoda M, Tayeb HT (2019) Relative reduction of biological and phylogenetic diversity of the oral microbiota of diabetes and pre-diabetes patients. Microb Pathogenesis 128:215–229
Nuli R, Cai J, Kadeer A, Zhang Y, Mohemaiti P (2019) Integrative analysis towards different glucose tolerance-related gut microbiota and diet. Front Endocrinol 10:295
Larsen N, Vogensen FK, Van Den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5:e9085
Schoefer L, Mohan R, Schwiertz A, Braune A, Blaut M (2003) Anaerobic degradation of flavonoids by Clostridium orbiscindens. Appl Environ Microbiol 69:5849–5854
Lv Y, Zhao X, Guo W, Gao Y, Yang S, Li Z, Wang G (2018) The relationship between frequently used glucose-lowering agents and gut microbiota in type 2 diabetes mellitus. J Diabetes Res
Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J (2009) Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58:1509–1517
Shumar SA (2019) Determining the role of Nudt7 in the regulation of cellular CoA levels and metabolism. Dissertation, West Virginia University
Zeevi D, Korem T, Zmora N, Israeli D, Rothschild D, Weinberger A, Ben-Yacov O, Lador D, Avnit-Sagi T, Lotan-Pompan M (2015) Personalized nutrition by prediction of glycemic responses. Cell 163:1079–1094
Acknowledgements
The authors thank Andréa Taschereau-Charron, Sarah Chouinard-Castonguay, Élise Cant, Valérie-Ève Julien, and Camille Lambert for their precious help with the visits with participants. They thank Andréa Taschereau-Charron for her support with the synthesis of the literature.
Funding
This study was funded by the Canadian Institutes of Health Research (CIHR). L. K. received a scholarship from CHU de Québec-Laval University Research Center; S. O. received a scholarship from the Canadian Institutes of Health Research (CIHR) and Diabète Québec; C. G. and I. R. hold a Junior two research Scholar from the Fonds de recherche du Québec—Santé (FRQ-S); C. G. holds a Diabetes Canada New Investigator Award; A. D. is funded by the L’Oréal research and innovation chair in digital biology of Université Laval. Food Isolation bags for dairy product transportation were given by the Dairy Farmers of Canada.
Author information
Authors and Affiliations
Contributions
PJ, JW, CG, and IR were involved in the conceptualization of the study and resources; IR was responsible for methodology; SOC conducted the study; LK and IR were responsible for data analyses; ML and AD performed machine learning analyses; LK and IR wrote the original draft; all the authors were involved in reviewing and editing the manuscript; and IR was responsible for supervision and funding acquisition.
Corresponding author
Ethics declarations
Conflicts of interest
On behalf of all the authors, the corresponding author states that there is no conflict of interest. The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Khorraminezhad, L., Leclercq, M., O’Connor, S. et al. Dairy product intake modifies gut microbiota composition among hyperinsulinemic individuals. Eur J Nutr 60, 159–167 (2021). https://doi.org/10.1007/s00394-020-02226-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-020-02226-z