Strategies for Scientific and Practicall Search: is There Any Correlation Between the Development of the Gut-Brain Axis and the Sleep Characteristics in Infants?

The review provides the analysis of modern publications on the topic of correlation between development of intestinal microbiota and maturation of neurophysiological activity patterns (on the example of sleep age structure development). The importance of the stage maturation of intestinal microbiota in the concept of the gut-brain axis is presented. Mechanisms and mediators involved in this axis are described, and its ontogenetic significance is justified. The main stages of sleep function development in a child as an important component of the general mental health maturation in relation to environmental factors and family features are presented. Recommendations on sleep periods duration and estimation of sleep onset and sleep structure are also given. Direct and reverse correlations of quantitative and qualitative microbiota parameters with sleep efficiency are shown. Positive correlation was identified between sleep consolidation, number and diversity of Bacteroidetes species in intestinal microbiota, and composition of bacterial metabolites. The presence of such correlations is theoretical justification for further development of methods of pathogenetic therapy of both microbiota and sleep disorders. Keywords: sleep, diet, nutrition, sleeping schedule, infant, development, intestinal microbiota.

1. Stiemsma LT, Michels KB. The role of the microbiome in the developmental origins of health and disease. Pediatrics. 2018;141(4):e20172437. doi: 10.1542/peds.2017-2437

2. Underwood MA, Mukhopadhyay S, Lakshminrusimha S, et al. Neonatal intestinal dysbiosis. J Perinatol. 2020;40(11):1597–1608. https://doi.org/10.1038/s41372-020-00829-2

3. Walker RW, Clemente JC, Peter I, Loos RJF. The prenatal gut microbiome: are we colonized with bacteria in utero? Pediatr Obes. 2017;12(1):3–17. doi: 10.1111/ijpo.12217

4. Nagpal R, Tsuji H, Takahashi T, et al. Sensitive Quantitative Analysis of the Meconium Bacterial Microbiota in Healthy Term Infants Born Vaginally or by Cesarean Section. Front Microbiol. 2016;7:1997. doi: 10.3389/fmicb.2016.01997

5. Nagpal R, Tsuji H, Takahashi T, et al. Ontogenesis of the Gut Microbiota Composition in Healthy, Full-Term, Vaginally Born and Breast-Fed Infants over the First 3 Years of Life: A Quantitative Bird’s-Eye View. Front Microbiol. 2017;8:1388. doi: 10.3389/fmicb.2017.01388

6. Lyons KE, Ryan CA, Dempsey EM, et al. Breast Milk, a Source of Beneficial Microbes and Associated Benefits for Infant Health. Nutrients. 2020;12(4):1039. doi: 10.3390/nu12041039

7. Fujimura KE, Sitarik AR, Havstad S, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med. 2016;22(10):1187–1191. doi: 10.1038/nm.4176

8. Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30(6): 492–506. doi:10.1038/s41422-020-0332-7

9. Carabotti M, Scirocco A, Maselli MA, et al. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol. 2015;28(2):203.

10. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837–848. doi: 10.1016/j.cell.2006.02.017

11. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125(3):926–938. doi: 10.1172/JCI76304

12. Feitong L, Jie L, Fan W, et al. Altered composition and function of intestinal microbiota in autism spectrum disorders: a systematic review. Transl Psychiatry. 2019;9(1):43. doi: 10.1038/s41398-019-0389-6

13. Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–141. doi: 10.1016/j.cell.2014.03.011

14. Zelante T, Iannitti RG, Cunha C, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity. 2013;39(2): 372–385. doi: 10.1016/j.immuni.2013.08.003

15. Rosser EC, Oleinika K, Tonon S, et al. Regulatory B cells are induced by gut microbiota–driven interleukin-1β and interleukin-6 production. Nat Med. 2014;20(11):1334. doi: org/10.1038/nm.3680

16. Brett BE, de Weerth C. The microbiota-gut-brain axis: A promising avenue to foster healthy developmental outcomes. Dev Psychobiol. 2019;61(5):772–782. doi: 10.1002/dev.21824

17. Zhu X, Han Y, Du J, et al. Microbiota-gut-brain axis and the central nervous system. Oncotarget. 2017;8(32):53829–5338. doi: 10.18632/oncotarget.17754

18. Cani PD, Knauf C. How gut microbes talk to organs: The role of endocrine and nervous routes. Mol Metab. 2016;5(9):743–752. doi: 10.1016/j.molmet.2016.05.011

19. Cani PD, Possemiers S, Van de Wiele T, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58(8):1091–1103. doi: 10.1136/gut.2008.165886

20. Braniste V, Al-Asmakh M, Kowal C, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Trans Med. 2014;6(263):263ra158–263ra158. doi: 10.1126/scitranslmed.3009759

21. Gobin CM, Banks JB, Fins AI, et al. Poor sleep quality is associated with a negative cognitive bias and decreased sustained attention. J Sleep Res. 2015;24(5):535–542. doi: 10.1111/jsr.12302

22. Sun W, Li SX, Jiang Y, et al. A community-based study of sleep and cognitive development in infants and toddlers. J Clin Sleep Med. 2018;14(6):977–984 doi: 10.5664/jcsm.7164

23. Super CM, Blom MJM, Harkness S, et al. Culture and the organization of infant sleep: A study in the Netherlands and the U.S.A. Infant Behav Dev. 2021;64:101620. doi: 10.1016/j.infbeh.2021.101620

24. Öztürk M, Boran P, Ersu R, Peker Y. Possums-based parental education for infant sleep: cued care resulting in sustained breastfeeding. Eur J Pediatr. 2021;180(6):1769–1776. doi: 10.1007/s00431-021-03942-2

25. Besedovsky L, Lange T, Haack M. The sleep-immune crosstalk in health and disease. Physiol Rev. 2019;99(3):1325–1380. doi: 10.1152/physrev.00010.2018

26. Mindell JA, Leichman ES, Composto J, et al. Development of infant and toddler sleep patterns: real-world data from a mobile application. J Sleep Res. 2016;25(5):508–516. doi: 10.1111/jsr.12414

27. Byars KC, Yolton K, Rausch J, et al. Prevalence, patterns, and persistence of sleep problems in the first 3 years of life. Pediatrics. 2012;129(2):e276–e284. doi: 10.1542/peds.2011-0372

28. Bruni O, Baumgartner E, Sette S, et al. Longitudinal study of sleep behavior in normal infants during the first year of life. J Clin Sleep Med. 2014;10(10):1119–1127. doi: 10.5664/jcsm.4114

29. Pacheco D. Babies and Sleep. In: Sleep Foundation. Available online: https://www.sleepfoundation.org/baby-sleep. Accessed on December 2, 2021.

30. Henderson JM, France KG, Owens JL, et al. Sleeping through the night: the consolidation of self-regulated sleep across the first year of life. Pediatrics. 2010 infants’ nocturnal sleep across the first year of life. Sleep Med Rev. 2011;15(4):211–220. doi: 10.1016/j.smrv.2010.08.003

31. Hirshkowitz M, Whiton K, Albert SM, et al. National Sleep Foundation’s updated sleep duration recommendations: final report. Sleep Health. 2015;1(4):233–243. doi: 10.1016/j.sleh.2015.10.004

32. Shepard-Ohta R. Consolidated Sleep for Infants: Is it Necessary to Healthy Brain Development? Hey Sleepy Baby, LLC; 2021 May 27. Available online: https://heysleepybaby.com/blog/consolidated-sleep-for-infants-is-it-necessary-to-healthy-brain-development. Accessed on December 2, 2021.

33. Walker M. Why We Sleep: Unlocking the Power of Sleep and Dreams. New York, NY: Scribner; 2017. 359 p.

34. Pennestri MH, Laganière C, Bouvette-Turcot AA, et al. Uninterrupted Infant Sleep, Development, and Maternal Mood. Pediatrics. 2018;142(6):e20174330. doi: 10.1542/peds.2017-4330

35. Tham EK, Schneider N, Broekman BF. Infant sleep and its relation with cognition and growth: a narrative review. Nat Sci Sleep. 2017;9:135–149. doi: 10.2147/NSS.S125992

36. Jiang F. Sleep and Early Brain Development. Ann Nutr Metab. 2019;75:(1):44–54. doi: 10.1159/000508055

37. Roffwarg HP, Muzio JN, Dement WC. Ontogenetic development of the human sleep-dream cycle. Science. 1966;152(3722):604–619. doi: 10.1126/science.152.3722.604

38. Kryger MH, Roth T, Dement WC. Principle and practice of sleep medicine. 5th ed. Philadelphia: Saunders/Elsevier; 2011.

39. Sheldon SH, Sateia MJ, Carskadon MA. Sleep in infants and children. In: Sleep Medicine. Lee-Chiong TL, Sateia MJ, Carskadon MA, eds. Philadelphia (PA): Hanley and Belfus Inc; 2002. pp. 99–103.

40. Chaput JP, Dutil C, Sampasa-Kanyinga H. Sleeping hours: what is the ideal number and how does age impact this? Nat Sci Sleep. 2018;10:421–430. doi: 10.2147/NSS.S163071

41. Hirshkowitz M, Whiton K, Albert SM, et al. National Sleep Foundation’s sleep time duration recommendations: methodology and results summary. Sleep Health. 2015;1(1):40–43. doi: 10.1016/j.sleh.2014.12.010

42. Lin QM, Spruyt K, Leng Y, et al. Cross-cultural disparities of subjective sleep parameters and their age-related trends over the first three years of human life: A systematic review and meta-analysis. Sleep Med Rev. 2019;48:101203. doi: 10.1016/j.smrv.2019.07.006

43. Cubero J, Valero V, Sánchez J, et al. The circadian rhythm of tryptophan in breast milk affects the rhythms of 6-sulfatoxymelatonin and sleep in newborn. Neuro Endocrinol Lett. 2005; 26(6):657–661.

44. Hagan JF, Shaw JS, Duncan PM. Bright Futures: Guidelines for Health Supervision of Infants, Children, and Adolescents. Elk Grove Village (IL): American Academy of Pediatrics; 2008.

45. Smith RP, Lyle SM, et al. Gut microbiome diversity is associated with sleep physiology in humans. PLoS One. 2019;14(10):e0222394. doi: 10.1371/journal.pone.0222394

46. Poroyko VA, Carreras A, Khalyfa A, et al. Chronic sleep disruption alters gut microbiota, induces systemic and adipose tissue inflammation and insulin resistance in mice. Sci Rep. 2016;6:35405. doi: 10.1038/srep35405

47. Anderson JR, Carroll I, Azcarate-Peril MA, et al. A preliminary examination of gut microbiota, sleep, and cognitive flexibility in healthy older adults. Sleep Med. 2017;38:104–107. doi: 10.1016/j.sleep.2017.07.018

48. Smith RP, Easson C, Lyle SM, et al. Gut microbiome diversity is associated with sleep physiology in humans. PLoS One. 2019; 14(10):e0222394. doi: 10.1371/journal.pone.0222394

49. Parkar SG, Kalsbeek A, Cheeseman JF. Potential Role for the Gut Microbiota in Modulating Host Circadian Rhythms and Metabolic Health. Microorganisms. 2019;7(2):41. doi: 10.3390/microorganisms7020041

50. Singh RK, Chang H-W, Yan D, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med. 2017;15(1):73 doi: 10.1186/s12967-017-1175-y

51. Heath А-LМ, Haszard JJ, Galland BC, et al. Association between the faecal short-chain fatty acid propionate and infant sleep. Eur J Clin Nutr. 2020;74(9):1362–1365. doi: 10.1038/s41430-019-0556-0

52. Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569–573. doi: 10.1126/science.1241165

53. Strandwitz P, Kim KH, Terekhova D, et al. GABA-modulating bacteria of the human gut microbiota. Nat Microbiol. 2019;4(3):396. doi: 10.1038/s41564-018-0307-3

54. Yunes R, Poluektova E, Dyachkova M, et al. GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strains from human microbiota. Anaerobe. 2016;42:197–204. doi: 10.1016/j.anaerobe.2016.10.011

55. Todd N, Zhang Y, Power Ch, et al.Modulation of brain function by targeted delivery of GABA through the disrupted blood-brain barrier. Neiroimage. 2019;189:267-275.

56. Gottesmann C. GABA mechanisms and sleep. Neuroscience. 2002;111(2):231–239. doi: 10.1016/s0306-4522(02)00034-9

57. Ursin R. Serotonin and sleep. Sleep Med Rev. 2002;6(1):55–67. doi: 10.1053/smrv.2001.0174

58. Frey DJ, Fleshner M, Wright KP Jr. The effects of 40 hours of total sleep deprivation on inflammatory markers in healthy young adults. Brain Behav Immun. 2007;21(8):1050–1057. doi: 10.1016/j.bbi.2007.04.003

59. Miller AH, Maletic V, Raison CL. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry. 2009;65(9):732–741. doi: 10.1016/j.biopsych.2008.11.02

60. Nicolaides NC, Vgontzas AN, Kritikou I, et al. HPA Axis and Sleep. [Updated 2020 Nov 24]. In: Endotext [Internet]. Feingold KR, Anawalt B, Boyce A, et al., eds. South Dartmouth (MA): MDText.com, Inc.; 2000. Available online: https://www.ncbi.nlm.nih.gov/books/NBK279071./ Accessed on December 4, 2021.

61. Pannaraj PS, Li F, Cerini C, et al. Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr. 2017;171(7): 647–654. doi: 10.1001/jamapediatrics.2017.0378

62. Brown A, Harries V. Infant sleep and night feeding patterns during later infancy: association with breastfeeding frequency, daytime complementary food intake, and infant weight. Breastfeed Med. 2015;10(5):246–252. doi: 10.1089/bfm.2014.0153

63. Ball HL, Taylor CE, Thomas V, Douglas PS. Development and evaluation of ‘Sleep, Baby & You’ — An approach to supporting parental well-being and responsive infant caregiving. PLoS One. 2020;15(8):e0237240. doi: 10.1371/journal.pone.0237240

64. Cubero J, Chanclón B, Sánchez S, et al. Improving the quality of infant sleep through the inclusion at supper of cereals enriched with tryptophan, adenosine-5’-phosphate, and uridine-5’-phosphate. Nutr Neurosci. 2009;12(6):272–280. doi: 10.1179/147683009X423490

65. Krol KM, Grossmann T. Psychological effects of breastfeeding on children and mothers. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2018;61(8):977–985. doi: 10.1007/s00103-018-2769-0

66. Vandeputte D, Falony G, Vieira-Silva S, et al. Prebiotic inulin-type fructans induce specific changes in the human gut microbiota. Gut. 2017;66(11):1968–1974. doi: 10.1136/gutjnl-2016-313271