Influence of the Infant Feeding on the Taxonomy of the Gut Microbiome and the Trefoil Factors Level in Children and Adolescents

Capa

Citar

Texto integral

Acesso aberto Acesso aberto
Acesso é fechado Acesso está concedido
Acesso é fechado Somente assinantes

Resumo

Changes in the gut microbiome are recognized as an important component of obesity in both adults and children. One factor in the gut microbiome formation is the infant feeding type, which may also have a prolonged effect on the microbial community. Breast milk contributes to the formation of mucosal tolerance to the intestinal microbiota. In turn, trefoil factors (TFF2 and TFF3) are important components of the mucosal barrier. The aim was to study the composition of the gut microbiota and the trefoil factors level in the blood of children and adolescents with obesity, depending on the infant feeding type. The study included 93 non-obese children (Group 1) and 92 obese children (Group 2). Serum TFF2 and TFF3 levels were determined by enzyme immunoassay in each study participant. The taxonomic composition of the fecal microbiome was determined by metagenomic sequencing of the 16S rRNA gene. In general, the taxonomic composition of the gut microbiota in Groups 1 and 2 was similar. However, Group 2 had less by [Prevotella], Epulopiscium and Haemophilus and more by Clostridium and Catenibacterium. Neither obesity nor the infant feeding type of influenced the serum concentration of TFF2 and TFF3. However, the infant feeding has a prolonged effect on the gut microbiota, and in Group 2 this effect was less pronounced. In Group 1, breastfeeding led to the formation of a complete mucosal tolerance to the microbiome, which did not occur with mixed and bottle feeding. In Group 2, most of the “TFFs–gut microbiome” associations were positive, indicating an unfavorable interaction between intestinal wall and microbiome in obese children and adolescents. Thus, infant feeding type seems to be a weak but significant factor in the gut microbiome formation in children and adolescents, which also affects the formation of mucosal tolerance to the intestinal microbiota.

Sobre autores

A. Shestopalov

Pirogov Russian National Research Medical University; Center for Molecular Health; Dmitry Rogachev National Medical Research Center of Pediatric Hematology,
Oncology and Immunology

Email: ir.max.kolesnikova@gmail.com
Russia, Moscow; Russia, Moscow; Russia, Moscow

I. Kolesnikova

Pirogov Russian National Research Medical University

Autor responsável pela correspondência
Email: ir.max.kolesnikova@gmail.com
Russia, Moscow

D. Savchuk

Rostov State Medical University; Children’s City Hospital № 1 in Rostov-on-Don

Email: ir.max.kolesnikova@gmail.com
Russia, Rostov-on-Don; Russia, Rostov-on-Don

E. Teplyakova

Rostov State Medical University

Email: ir.max.kolesnikova@gmail.com
Russia, Rostov-on-Don

V. Shin

Rostov State Medical University

Email: ir.max.kolesnikova@gmail.com
Russia, Rostov-on-Don

T. Grigoryeva

Kazan (Volga Region) Federal University

Email: ir.max.kolesnikova@gmail.com
Russia, Kazan

Yu. Naboka

Rostov State Medical University

Email: ir.max.kolesnikova@gmail.com
Russia, Rostov-on-Don

A. Gaponov

Center for Molecular Health; Negovsky Research Institute of General Reanimatology, Federal Research and Clinical
Center of Intensive Care Medicine and Rehabilitology

Email: ir.max.kolesnikova@gmail.com
Russia, Moscow; Russia, Moscow

S. Roumiantsev

Pirogov Russian National Research Medical University; Center for Molecular Health

Email: ir.max.kolesnikova@gmail.com
Russia, Moscow; Russia, Moscow

Bibliografia

  1. Lobstein T, Jackson-Leach R, Moodie ML, Hall KD, Gortmaker SL, Swinburn BA, James WPT, Wang Y, McPherson K (2015) Child and adolescent obesity: part of a bigger picture. Lancet (London, England) 385: 2510–2520. https://doi.org/10.1016/S0140-6736(14)61746-3
  2. Singer-Englar T, Barlow G, Mathur R (2019) Obesity, diabetes, and the gut microbiome: an updated review. Expert Rev Gastroenterol Hepatol 13: 3–15. https://doi.org/10.1080/17474124.2019.1543023
  3. Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG (2014) Minireview: Gut microbiota: the neglected endocrine organ. Mol Endocrinol 28: 1221–1238. https://doi.org/10.1210/me.2014-1108
  4. Шестопалов АВ, Шатова ОП, Комарова ЕФ, Румянцев СА (2020) Особенности метаболического сопряжения в системе “СУПЕРОРГАНИЗМА” (хозяин–микробиота). Крымск журн экспер клин мед 10: 95–103. [Shestopalov AV, Shatova OP, Komarova EF, Rumyantsev SA (2020) Features of metabolic coupling in the “SUPERORGANISM” system (host–microbiota) Krymsk J Exper Klin Med 10: 95–103. (In Russ)]. https://doi.org/10.37279/2224-6444-2020-10-2-95-103
  5. Шестопалов АВ, Дворников АС, Борисенко ОВ, Тутельян АВ (2019) Трефоиловые факторы – новые маркеры мукозального барьера желудочно-кишечного тракта. Инфекция и иммунитет 9: 39–46. [Shestopalov AV, Dvornikov AS, Borisenko OV, Tutelyan AV (2019) Trefoil factors – new markers of gastrointestinal mucosal barrier. Infekciya i immunitet 9: 39–46. (In Russ)]. https://doi.org/10.15789/2220-7619-2019-1-39-46
  6. Шестопалов АВ, Трофименко ОВ, Шестопалова МА (2012) Уровень трефоиловых пептидов (TFF-1 и TFF-2) у детей с хроническими гастродуоденитами. Фундамент исследов 10: 363–366. [Shestopalov AV, Trofimenko OV, Shestopalova MA (2012) Level trefoil peptides (TFF-1 and TFF-2) in children with chronic gastroduodenitis. Fundament Issledovan 10: 363–366. (In Russ)].
  7. Шестопалов АВ, Мирошниченко ЮА, Рымашевский АН (2013) Содержание муцинов (MUC 5 AC, MUC 6) и трефоилового пептида-3 (TFF-3) в эндометрии и цервико-вагинальном секрете у женщин с физиологической беременностью. Фундамент исследов 12: 104–106. [Shestopalov AV, Miroshnichenko YA, Rymashevskiy AN (2013) The concentration of mucin (MUC 5 ac, MUC 6) and trefoil peptide-3 (TFF-3) in the endometrium and cervico-vaginal secretions of women with physiological pregnancy. Fundament Issledovan 12: 104–106. (In Russ)].
  8. Шестопалов АВ, Румянцев СА, Шестопалова МА, Сапрыкина ЕА, Шумилов ПВ (2014) Влияние H. pylori на уровень трефоиловых факторов и адипокинов у детей с гастродуоденитами. Педиатрия. Журн им ГН Сперанского 93: 6–10. [Shestopalov AV, Rumyantsev SA, Shestopalova MA, Saprykina EA, Shumilov PV (2014) Effect of H. pylori on the level of trefoil factors and adipokines in children with gastroduodenitis. Pediatriya. Zhurn im GN Speranskogo 93: 6–10. (In Russ)].
  9. Ford SL, Lohmann P, Preidis GA, Gordon PS, O’Donnell A, Hagan J, Venkatachalam A, Balderas M, Luna RA, Hair AB (2019) Improved feeding tolerance and growth are linked to increased gut microbial community diversity in very-low-birth-weight infants fed mother’s own milk compared with donor breast milk. Am J Clin Nutr 109: 1088–1097. https://doi.org/10.1093/ajcn/nqz006
  10. Le Doare K, Holder B, Bassett A, Pannaraj PS (2018) Mother’s Milk: A Purposeful Contribution to the Development of the Infant Microbiota and Immunity. Front Immunol 9: 361. https://doi.org/10.3389/fimmu.2018.00361
  11. Donald K, Petersen C, Turvey SE, Finlay BB, Azad MB (2022) Secretory IgA: Linking microbes, maternal health, and infant health through human milk. Cell Host Microbe 30: 650–659. https://doi.org/10.1016/j.chom.2022.02.005
  12. Eshriqui I, Viljakainen HT, Ferreira SRG, Raju SC, Weiderpass E, Figueiredo RAO (2020) Breastfeeding may have a long-term effect on oral microbiota: results from the Fin-HIT cohort. Int Breastfeed J 15: 42. https://doi.org/10.1186/s13006-020-00285-w
  13. Peterkova VA, Bezlepkina OB, Bolotova NV, Bogova EA, Vasyukova OV, Girsh YV, Kiyaev AV, Kostrova IB, Malievskiy OA, Mikhailova EG, Okorokov PL, Petryaykina EE, Taranushenko TE, Khramova EB (2021) Clinical guidelines “Obesity in children”. Probl Endocrinol 67: 67–83. https://doi.org/https://doi.org/10.14341/probl12802
  14. Chen X, Sun H, Jiang F, Shen Y, Li X, Hu X, Shen X, Wei P (2020) Alteration of the gut microbiota associated with childhood obesity by 16S rRNA gene sequencing. Peer J 8: e8317. https://doi.org/10.7717/peerj.8317
  15. Zeng Q, Li D, He Y, Li Y, Yang Z, Zhao X, Liu Y, Wang Y, Sun J, Feng X, Wang F, Chen J, Zheng Y, Yang Y, Sun X, Xu X, Wang D, Kenney T, Jiang Y, Gu H, Li Y, Zhou K, Li S, Dai W (2019) Discrepant gut microbiota markers for the classification of obesity-related metabolic abnormalities. Sci Rep 9: 13424. https://doi.org/10.1038/s41598-019-49462-w
  16. Гапонов АМ, Волкова НИ, Ганенко ЛА, Набока ЮЛ, Маркелова МИ, Синягина МН, Харченко АМ, Хуснутдинова ДР, Румянцев СА, Тутельян АВ, Макаров ВВ, Юдин СМ, Шестопалов АВ (2021) Особенности микробиома толстой кишки у пациентов с ожирением при его различных фенотипах (оригинальная статья). Журн микробиол, эпидемиол и иммунобиол 98: 44–155. [Gaponov AM, Volkova NI, Ganenko LA, Naboka YL, Markelova MI, Sinyagina MN, Kharchenko AM, Khusnutdinova DR, Rumyantsev SA, Tutelyan AV, Makarov VV, Yudin SM, Shestopalov AV (2021) Features of the colon microbiome in obese patients with its various phenotypes (original article). Zhurn microbiol, epidemiol and immunobiol 98: 44–155. https://doi.org/10.36233/0372-9311-66
  17. Heuer F, Stürmer R, Heuer J, Kalinski T, Lemke A, Meyer F, Hoffmann W (2019) Different Forms of TFF2, A Lectin of the Human Gastric Mucus Barrier: In Vitro Binding Studies. Int J Mol Sci 20(23): 5871. https://doi.org/10.3390/ijms20235871
  18. Hoffmann W (2015) TFF2, a MUC6-binding lectin stabilizing the gastric mucus barrier and more (Review). Int J Oncol 47: 806–816. https://doi.org/10.3892/ijo.2015.3090
  19. Hoffmann W (2020) Trefoil Factor Family (TFF) Peptides and Their Diverse Molecular Functions in Mucus Barrier Protection and More: Changing the Paradigm. Int J Mol Sci 21(12): 4535. https://doi.org/10.3390/ijms21124535
  20. Yang Y, Lin Z, Lin Q, Bei W, Guo J (2022) Pathological and therapeutic roles of bioactive peptide trefoil factor 3 in diverse diseases: recent progress and perspective. Cell Death Dis 13: 62. https://doi.org/10.1038/s41419-022-04504-6
  21. Roa JB, Tortolero GS, Gonzalez E (2013) Trefoil factor 3 (TFF3) expression is regulated by insulin and glucose. J Heal Sci 3: 1–12. https://doi.org/10.17532/jhsci.2013.26
  22. De Giorgio MR, Yoshioka M, Riedl I, Moreault O, Cherizol R-G, Shah AA, Blin N, Richard D, St-Amand J (2013) Trefoil factor family member 2 (Tff2) KO mice are protected from high-fat diet-induced obesity. Obesity (Silver Spring) 21: 1389–1395. https://doi.org/10.1002/oby.20165
  23. Paone P, Cani PD (2020) Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut 69: 2232–2243. https://doi.org/10.1136/gutjnl-2020-322260
  24. Heitkemper MM, Cain KC, Shulman RJ, Burr RL, Ko C, Hollister EB, Callen N, Zia J, Han CJ, Jarrett ME (2018) Stool and urine trefoil factor 3 levels: associations with symptoms, intestinal permeability, and microbial diversity in irritable bowel syndrome. Benef Microbes 9: 345–355. https://doi.org/10.3920/BM2017.0059
  25. Kaakoush NO (2015) Insights into the Role of Erysipelotrichaceae in the Human Host. Front Cell Infect Microbiol 5: 84. https://doi.org/10.3389/fcimb.2015.00084
  26. Palmas V, Pisanu S, Madau V, Casula E, Deledda A, Cusano R, Uva P, Vascellari S, Loviselli A, Manzin A, Velluzzi F (2021) Gut microbiota markers associated with obesity and overweight in Italian adults. Sci Rep 11: 5532. https://doi.org/10.1038/s41598-021-84928-w
  27. Scheiman J, Luber JM, Chavkin TA, MacDonald T, Tung A, Pham L-D, Wibowo MC, Wurth RC, Punthambaker S, Tierney BT, Yang Z, Hattab MW, Avila-Pacheco J, Clish CB, Lessard S, Church GM, Kostic AD (2019) Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med 25: 1104–1109. https://doi.org/10.1038/s41591-019-0485-4
  28. Lee H, An J, Kim J, Choi D, Song Y, Lee C-K, Kong H, Kim SB, Kim K (2022) A Novel Bacterium, Butyricimonas virosa, Preventing HFD-Induced Diabetes and Metabolic Disorders in Mice via GLP-1 Receptor. Front Microbiol 13: 858192. https://doi.org/10.3389/fmicb.2022.858192
  29. Conway de Macario E, Macario AJL (2009) Methanogenic archaea in health and disease: a novel paradigm of microbial pathogenesis. Int J Med Microbiol 299: 99–108. https://doi.org/10.1016/j.ijmm.2008.06.011
  30. Yuan X, Zhang Y, Lin X, Yang X, Chen R (2023) Association of gut microbiota and glucose metabolism in children with disparate degrees of adiposity. Pediatr Obes 18(4): e13009. https://doi.org/10.1111/ijpo.13009
  31. Waters JL, Ley RE (2019) The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol 17: 83. https://doi.org/10.1186/s12915-019-0699-4
  32. Tavella T, Rampelli S, Guidarelli G, Bazzocchi A, Gasperini C, Pujos-Guillot E, Comte B, Barone M, Biagi E, Candela M, Nicoletti C, Kadi F, Battista G, Salvioli S, O’Toole PW, Franceschi C, Brigidi P, Turroni S, Santoro A (2021) Elevated gut microbiome abundance of Christensenellaceae, Porphyromonadaceae and Rikenellaceae is associated with reduced visceral adipose tissue and healthier metabolic profile in Italian elderly. Gut Microbes 13: 1–19. https://doi.org/10.1080/19490976.2021.1880221
  33. Xu Y, Wang N, Tan HY, Li S, Zhang C, Feng Y (2020) Function of Akkermansia muciniphila in Obesity: Interactions With Lipid Metabolism, Immune Response and Gut Systems. Front Microbiol 11: 1–12. https://doi.org/10.3389/fmicb.2020.00219
  34. Yan J, Liu L, Zhu Y, Huang G, Wang PP (2014) The association between breastfeeding and childhood obesity: a meta-analysis. BMC Public Health 14: 1267. https://doi.org/10.1186/1471-2458-14-1267
  35. Verduci E, Giannì ML, Vizzari G, Vizzuso S, Cerasani J, Mosca F, Zuccotti GV (2021) The Triad Mother-Breast Milk-Infant as Predictor of Future Health: A Narrative Review. Nutrients 13(2): 486. https://doi.org/10.3390/nu13020486
  36. Lv Y, Qin X, Jia H, Chen S, Sun W, Wang X (2019) The association between gut microbiota composition and BMI in Chinese male college students, as analysed by next-generation sequencing. Br J Nutr 122: 986–995. https://doi.org/10.1017/S0007114519001909
  37. Hiippala K, Kainulainen V, Kalliomäki M, Arkkila P, Satokari R (2016) Mucosal Prevalence and Interactions with the Epithelium Indicate Commensalism of Sutterella spp. Front Microbiol 7: 1706. https://doi.org/10.3389/fmicb.2016.01706
  38. Wang C, Zhang H, Liu H, Zhang H, Bao Y, Di J, Hu C (2020) The genus Sutterella is a potential contributor to glucose metabolism improvement after Roux-en-Y gastric bypass surgery in T2D. Diabetes Res Clin Pract 162: 108116. https://doi.org/10.1016/j.diabres.2020.108116
  39. Chatterton DEW, Nguyen DN, Bering SB, Sangild PT (2013) Anti-inflammatory mechanisms of bioactive milk proteins in the intestine of newborns. Int J Biochem Cell Biol 45: 1730–1747. https://doi.org/10.1016/j.biocel.2013.04.028
  40. Hiippala K, Barreto G, Burrello C, Diaz-Basabe A, Suutarinen M, Kainulainen V, Bowers JR, Lemmer D, Engelthaler DM, Eklund KK, Facciotti F, Satokari R (2020) Novel Odoribacter splanchnicus Strain and Its Outer Membrane Vesicles Exert Immunoregulatory Effects in vitro. Front Microbiol 11: 575455. https://doi.org/10.3389/fmicb.2020.575455
  41. Hoffmann W (2021) Trefoil Factor Family (TFF) Peptides and Their Links to Inflammation: A Re-evaluation and New Medical Perspectives. Int J Mol Sci 22(9): 4909. https://doi.org/10.3390/ijms22094909
  42. Lima SF, Gogokhia L, Viladomiu M, Chou L, Putzel G, Jin W-B, Pires S, Guo C-J, Gerardin Y, Crawford CV, Jacob V, Scherl E, Brown S-E, Hambor J, Longman RS (2022) Transferable Immunoglobulin A-Coated Odoribacter splanchnicus in Responders to Fecal Microbiota Transplantation for Ulcerative Colitis Limits Colonic Inflammation. Gastroenterology 162: 166–178. https://doi.org/10.1053/j.gastro.2021.09.061
  43. Pereira FC, Wasmund K, Cobankovic I, Jehmlich N, Herbold CW, Lee KS, Sziranyi B, Vesely C, Decker T, Stocker R, Warth B, von Bergen M, Wagner M, Berry D (2020) Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization. Nat Commun 11: 5104. https://doi.org/10.1038/s41467-020-18928-1
  44. Налетов АВ, Пушкарук ВВ (2022) Состояние кишечной микробиоты у детей с ожирением. Child Med North-West 10: 70–74. [Nalyotov AV, Pushkaruk VV (2022) The state of the intestinal microbiota in obese children. Child Med North-West 10: 70–74. (In Russ)].
  45. Dong TS, Luu K, Lagishetty V, Sedighian F, Woo S-L, Dreskin BW, Katzka W, Chang C, Zhou Y, Arias-Jayo N, Yang J, Ahdoot A, Li Z, Pisegna JR, Jacobs JP (2020) A High Protein Calorie Restriction Diet Alters the Gut Microbiome in Obesity. Nutrients 12(10): 3221. https://doi.org/10.3390/nu12103221

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML
2.

Baixar (621KB)
3.

Baixar (91KB)
4.

Baixar (150KB)

Declaração de direitos autorais © А.В. Шестопалов, И.М. Колесникова, Д.В. Савчук, Е.Д. Теплякова, В.А. Шин, Т.В. Григорьева, Ю.Л. Набока, А.М. Гапонов, С.А. Румянцев, 2023

Este site utiliza cookies

Ao continuar usando nosso site, você concorda com o procedimento de cookies que mantêm o site funcionando normalmente.

Informação sobre cookies