Relationship between the milk bacterial phyla and the amount of dietary macronutrients and micronutrients intake in lactating mothers with high body mass index compared to the normal: a case-control study

Document Type : Original Article

Authors

1 Department of Microbiology, Zanjan Branch, Islamic Azad University, Zanjan, Iran

2 Department of Nutrition, School of Public Health, Zanjan University of Medical Sciences, Zanjan, Iran

3 Department of Microbiology and Virology, School of Medicine, Zanjan University of Medical Sciences, Zanjan, Iran

Abstract

Objective: In the present study, the amount of the four main phyla in obese lactating mothers and mothers with a normal body mass index was evaluated and their relationship with the amount of macro- and micronutrient’s intake was investigated.
Materials and Methods: 30 mothers with high BMI (greater-equal to 23 kg/m2) and 30 mothers with normal BMI (between 18.5-24.9 kg/m2) who were in the fourth month of breastfeeding were selected from the health centers of Zanjan city. The milk sample was collected under completely sterile conditions. Bacterial DNA was extracted and amplification of 16S rRNA gene was done by qPCR method using universal bacterial primers. Dietary information was collected using a food frequency questionnaire (FFQ) and validated by a three-day food diary.
Results: Adjusting for all parameters, mothers with a normal body mass index had 1.41 times more Actinobacteria gene in milk (p=0.04). The amount of iron and vitamin C intake showed a significant negative relationship with the Actinobacteria and Firmicutes population in milk, respectively (OR=-2.3, p=0.04, OR=-0.96, p=0.02). Also, the amount of dietary cholesterol showed a significant relationship with the Bacteroidetes population (OR=0.81, p=0.04).
Conclusion: Actinobacteria gene presence, as a beneficial phylum, was higher in lactating mothers with normal than the high body mass index. Dietary Iron and vitamin C were inversely related to the Actinobacteria and Firmicutes population.

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  1. Hanson M, Aagaard-Hansen J. Developmental Origins of Health and Disease: Towards a combined bio-social life-course perspective. Acta Pediatrica 2021; 110: 2306-2309.
  2. Carroll X, Liang X, Zhang W, Zhang W, Liu G, Turner N, et al. Socioeconomic, environmental and lifestyle factors associated with gestational diabetes mellitus: a matched case-control study in Beijing, China. Scientific Reports 2018; 8:8103–
  3. Chiefari E, Arcidiacono B, Foti D, Brunetti A. Gestational diabetes mellitus: an updated overview. Journal of Endocrinological Investigation 2017;40:899–
  4. Chatzakis C, Eleftheriades A, Demertzidou E, Dinas K, Vlahos N, Sotiriadis A, Eleftheriades M. Pregnancy outcomes in the different phenotypes of gestational diabetes mellitus based on the oral glucose tolerance test. A systematic review and meta-analysis. Diabetes Research and Clinical Practice 2023;204:110913.
  5. Metzger BE, Buchanan TA, Coustan DR, de Leiva A, Dunger DB, Hadden DR, et al. Summary and recommendations of the fifth international workshop-conference on gestational diabetes mellitus. Diabetes Care 2007;30(Supplement 2):S251–
  6. Wei JLX, Gao J. Insulin secretion and tolerance of women with different gestational glucose regulation one year postpartum. International Journal of Clinical and Experimental Medicine 2015;8: 6384–
  7. Sheiner E. Gestational Diabetes Mellitus: Long-Term Consequences for the Mother and Child Grand Challenge: How to Move on Towards Secondary Prevention?. Frontiers in Clinical Diabetes and Healthcare 2020;1:546256.
  8. Damm P, Houshmand-Oeregaard A, Kelstrup L, Lauenborg J, Mathiesen ER, Clausen TD. Gestational diabetes mellitus and long-term consequences for mother and offspring: a view from Denmark. Diabetologia 2016;59:1396–
  9. Agha-Jaffar R, Oliver N, Johnston D, Robinson S. Gestational diabetes mellitus: does an effective prevention strategy exist? Endocrinology 2016;12:533-546.
  10. Eyupoglu ND, Caliskan Guzelce E, Acikgoz A, Uyanik E, Bjørndal B, Berge RK, et al. Circulating gut microbiota metabolite trimethylamine N-oxide and oral contraceptive use in polycystic ovary syndrome. Clinical Endocrinology (Oxford) 2019;91:810–
  11. Zhou L , Xiao X , Zhang Q , Zheng J , Li M , Wang X , et al. Gut microbiota might be a crucial factor in deciphering the metabolic benefits of perinatal genistein consumption in dams and adult female offspring. Food and Function 2019;10:4505.
  12. Simpson SSL, Bowe J. Placental peptides regulating islet adaptation to pregnancy: clinical potential in gestational diabetes mellitus. Current Opinion in Pharmacology 2018;43:59–
  13. Kalra SGY, Kumar A. Prevention of gestational diabetes mellitus (GDM). Journal of the Pakistan Medical Association 2016;66(9 Suppl 1):S107-S109.
  14. DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, et al. Temporal and spatial variation of the human microbiota during pregnancy. Proceedings of the National Academy of Sciences 2015;112:11060-11065.
  15. Vaiserman A, Romanenko M, Piven L, Moseiko V, Lushchak O, Kryzhanovska N, et al. Differences in the gut Firmicutes to Bacteroidetes ratio across age groups in healthy Ukrainian population. BMC Microbiology 2020;20:221.
  16. Liu C, Song Y, McTeague M, Vu AW, Wexler H, Finegold SM. Rapid identification of the species of the Bacteroides fragilis group by multiplex PCR assays using group- and species-specific primers. FEMS Microbiology Letters 2003;222:9-16.
  17. Notarbartolo V, Giuffrè M, Montante C, Corsello G, Carta M. Composition of Human Breast Milk Microbiota and Its Role in Children's Health. Journal of Pediatric Gastroenterology and Nutrition 2022; 25(3):194-210.
  18. Stach JE, Maldonado LA, Ward AC, Goodfellow M, Bull AT. New primers for the class Actinobacteria: application to marine and terrestrial environments. Environmental Microbiology 2003 ;5:828-841.
  19. Blackwood CB, Oaks A, Buyer JS. Phylum- and class-specific PCR primers for general microbial community analysis. Applied Environmental Microbiology 2005;71:6193-6198.
  20. Rinninella E, Raoul P, Cintoni M, Franceschi F, Donato Miggiano G, Gasbarrini A, et al. What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms 2019;7(1):14.
  21. Dridi L, Altamura F, Gonzalez E, Lui O, Kubinski R, Pidgeon R, et al. Identifying glycan consumers in human gut microbiota samples using metabolic labeling coupled with fluorescence-activated cell sorting. Nature Communications 2023; 14:662.
  22. Archambaud C, Derre-Bobillot A, Lapaque N, Rigottier-Gois L, Serror P. Intestinal translocation of enterococci requires a threshold level of enterococcal overgrowth in the lumen. Scientific Reports 2019;9(1):8926.
  23. Pareek S, Kurakawa T, Das B, Motooka D, Nakaya S, Rongsen-Chandola T. Comparison of Japanese and Indian intestinal microbiota shows diet-dependent interaction between bacteria and fungi. NPJ Biofilms Microbiomes 2019;5:37.
  24. Zeng H., Umar S., Rust B., Lazarova D., Bordonaro M. Secondary bile acids and short chain fatty acids in the colon: a focus on colonic microbiome, cell proliferation, inflammation, and cancer. International Journal of Molecular Sciences 2019;20.
  25. Santhanam S, Alvarado D.M, Ciorba M.A. Therapeutic targeting of inflammation and tryptophan metabolism in colon and gastrointestinal cancer. Translational Research 2016;167:67–
  26. Kaur A, Chen T, Green S.J, Mutlu E, Martin B.R, Rumpagaporn P, et al. Physical Inaccessibility of a Resistant Starch Shifts Mouse Gut Microbiota to Butyrogenic Firmicutes. Molecular Nutrition and Food Research 2019; 63: e1801012.
  27. Murata Ch , Gutiérrez-Castrellón P, Pérez-Villatoro F, García-Torres I, Enríquez-Flores, S, Mora I, et al. Delivery mode-associated gut microbiota in the first 3 months of life in a country with high obesity rates: A descriptive study. Medicine 2020; 99: e22442.
  28. Binda C, Lopetuso LR, Rizzatti G, Gibiino G, Cennamo V, Gasbarrini A. Actinobacteria: A relevant minority for the maintenance of gut homeostasis. Digestive and Liver Disease 2018;50(5):421-428.
  29. Lai S, Yan Y, Pu Y, Lin Sh, Qiu J, Jiang B, et al. Enterotypes of the human gut mycobiome. Microbiome 2023; 11, 179.
  30. Zhang P. Influence of Foods and Nutrition on the Gut Microbiome and Implications for Intestinal Health. International Journal of Molecular Sciences 2022;23(17):9588.