Long-Term Implicit Epigenetic Stress Information in the Enteric Nervous
System and its Contribution to Developing and Perpetuating IBS

Császár-Nagy      Noemi; Petr      Bob; István      Bókkon
doi:10.2174/1570159X22666240507095700
Abstract

Psychiatric and mood disorders may play an important role in the development and persistence of irritable bowel syndrome (IBS). Previously, we hypothesized that stress-induced implicit memories may persist throughout life via epigenetic processes in the enteric nervous system (ENS), independent of the central nervous system (CNS). These epigenetic memories in the ENS may contribute to developing and perpetuating IBS. Here, we further elaborate on our earlier hypothesis. That is, during pregnancy, maternal prenatal stresses perturb the HPA axis and increase circulating cortisol levels, which can affect the maternal gut microbiota. Maternal cortisol can cross the placental barrier and increase cortisol-circulating levels in the fetus. This leads to dysregulation of the HPA axis, affecting the gut microbiota, microbial metabolites, and intestinal permeability in the fetus. Microbial metabolites, such as short-chain fatty acids (which also regulate the development of fetal ENS), can modulate a range of diseases by inducing epigenetic changes. These mentioned processes suggest that stress-related, implicit, long-term epigenetic memories may be programmed into the fetal ENS during pregnancy. Subsequently, this implicit epigenetic stress information from the fetal ENS could be conveyed to the CNS through the bidirectional microbiota-gut-brain axis (MGBA), leading to perturbed functional connectivity among various brain networks and the dysregulation of affective and pain processes.
Keywords: ENS, Implicit epigenetic long-term memory, IBS, Microbiota-gut-brain axis, stress, short-chain fatty acids.
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[1]
Chen, J.; Barandouzi, Z.A.; Lee, J.; Xu, W.; Feng, B.; Starkweather, A.; Cong, X. Psychosocial and sensory factors contribute to self-reported pain and quality of life in young adults with irritable bowel syndrome. Pain Manag. Nurs.,  2022, 23(5), 646-654.
 [http://dx.doi.org/10.1016/j.pmn.2021.12.004] [PMID: 35074280]

[2]
Tripathi, R.; Mehrotra, S. Irritable bowel syndrome and its psychological management. Ind. Psychiatry J.,  2015, 24(1), 91-93.
 [http://dx.doi.org/10.4103/0972-6748.160947] [PMID: 26257492]

[3]
van Tilburg, M.A.L.; Palsson, O.S.; Whitehead, W.E. Which psychological factors exacerbate irritable bowel syndrome? Development of a comprehensive model. J. Psychosom. Res.,  2013, 74(6), 486-492.
 [http://dx.doi.org/10.1016/j.jpsychores.2013.03.004] [PMID: 23731745]

[4]
Sharkey, K.A.; Mawe, G.M. The enteric nervous system. Physiol. Rev.,  2023, 103(2), 1487-1564.
 [http://dx.doi.org/10.1152/physrev.00018.2022] [PMID: 36521049]

[5]
Furness, J.B. Comparative and evolutionary aspects of the digestive system and its enteric nervous system control. Adv. Exp. Med. Biol.,  2022, 1383, 165-177.
 [http://dx.doi.org/10.1007/978-3-031-05843-1_16] [PMID: 36587156]

[6]
Green, S.A.; Uy, B.R.; Bronner, M.E. Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest. Nature,  2017, 544(7648), 88-91.
 [http://dx.doi.org/10.1038/nature21679] [PMID: 28321127]

[7]
Furness, J.B.; Stebbing, M.J. The first brain: Species comparisons and evolutionary implications for the enteric and central nervous systems. Neurogastroenterol. Motil.,  2018, 30(2), e13234.
 [http://dx.doi.org/10.1111/nmo.13234] [PMID: 29024273]

[8]
Császár-Nagy, N.; Bókkon, I. Hypnotherapy and IBS: Implicit, long-term stress memory in the ENS? Heliyon,  2023, 9(1), e12751.
 [http://dx.doi.org/10.1016/j.heliyon.2022.e12751] [PMID: 36685398]

[9]
Mao, C.P.; Chen, F.R.; Huo, J.H.; Zhang, L.; Zhang, G.R.; Zhang, B.; Zhou, X.Q. Altered resting‐state functional connectivity and effective connectivity of the habenula in irritable bowel syndrome: A cross‐sectional and machine learning study. Hum. Brain Mapp.,  2020, 41(13), 3655-3666.
 [http://dx.doi.org/10.1002/hbm.25038] [PMID: 32488929]

[10]
Weng, Y.; Qi, R.; Liu, C.; Ke, J.; Xu, Q.; Wang, F.; Zhang, L.J.; Lu, G.M. Disrupted functional connectivity density in irritable bowel syndrome patients. Brain Imaging Behav.,  2017, 11(6), 1812-1822.
 [http://dx.doi.org/10.1007/s11682-016-9653-z] [PMID: 27848148]

[11]
Bhatt, R.R.; Gupta, A.; Labus, J.S.; Zeltzer, L.K.; Tsao, J.C.; Shulman, R.J.; Tillisch, K. Altered brain structure and functional connectivity and its relation to pain perception in girls with irritable bowel syndrome. Psychosom. Med.,  2019, 81(2), 146-154.
 [http://dx.doi.org/10.1097/PSY.0000000000000655] [PMID: 30615602]

[12]
Nisticò, V.; Rossi, R.E.; D’Arrigo, A.M.; Priori, A.; Gambini, O.; Demartini, B. Functional neuroimaging in irritable bowel syndrome: A systematic review highlights common brain alterations with functional movement disorders. J. Neurogastroenterol. Motil.,  2022, 28(2), 185-203.
 [http://dx.doi.org/10.5056/jnm21079] [PMID: 35189600]

[13]
Qi, R.; Liu, C.; Weng, Y.; Xu, Q.; Chen, L.; Wang, F.; Zhang, L.J.; Lu, G.M. Disturbed interhemispheric functional connectivity rather than structural connectivity in irritable bowel syndrome. Front. Mol. Neurosci.,  2016, 9, 141.
 [http://dx.doi.org/10.3389/fnmol.2016.00141] [PMID: 27999530]

[14]
Li, J.; He, P.; Lu, X.; Guo, Y.; Liu, M.; Li, G.; Ding, J. A resting-state functional magnetic resonance imaging study of whole-brain functional connectivity of voxel levels in patients with irritable bowel syndrome with depressive symptoms. J. Neurogastroenterol. Motil.,  2021, 27(2), 248-256.
 [http://dx.doi.org/10.5056/jnm20209] [PMID: 33795543]

[15]
Martinou, E.; Stefanova, I.; Iosif, E.; Angelidi, A.M. Neurohormonal changes in the gut-brain axis and underlying neuroendocrine mechanisms following bariatric surgery. Int. J. Mol. Sci.,  2022, 23(6), 3339.
 [http://dx.doi.org/10.3390/ijms23063339] [PMID: 35328759]

[16]
Carabotti, M.; Scirocco, A.; Maselli, M.A.; Severi, C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol.,  2015, 28(2), 203-209.
 [PMID: 25830558]

[17]
Muhammad, F.; Fan, B.; Wang, R.; Ren, J.; Jia, S.; Wang, L.; Chen, Z.; Liu, X.A. The molecular gut-brain axis in early brain development. Int. J. Mol. Sci.,  2022, 23(23), 15389.
 [http://dx.doi.org/10.3390/ijms232315389] [PMID: 36499716]

[18]
Sarubbo, F.; Cavallucci, V.; Pani, G. The influence of gut microbiota on neurogenesis: Evidence and hopes. Cells,  2022, 11(3), 382.
 [http://dx.doi.org/10.3390/cells11030382] [PMID: 35159192]

[19]
Song, J.G.; Yu, M.S.; Lee, B.; Lee, J.; Hwang, S.H.; Na, D.; Kim, H.W. Analysis methods for the gut microbiome in neuropsychiatric and neurodegenerative disorders. Comput. Struct. Biotechnol. J.,  2022, 20, 1097-1110.
 [http://dx.doi.org/10.1016/j.csbj.2022.02.024] [PMID: 35317228]

[20]
Wachsmuth, H.R.; Weninger, S.N.; Duca, F.A. Role of the gut–brain axis in energy and glucose metabolism. Exp. Mol. Med.,  2022, 54(4), 377-392.
 [http://dx.doi.org/10.1038/s12276-021-00677-w] [PMID: 35474341]

[21]
Chakrabarti, A.; Geurts, L.; Hoyles, L.; Iozzo, P.; Kraneveld, A.D.; La Fata, G.; Miani, M.; Patterson, E.; Pot, B.; Shortt, C.; Vauzour, D. The microbiota-gut-brain axis: Pathways to better brain health. Perspectives on what we know, what we need to investigate and how to put knowledge into practice. Cell. Mol. Life Sci.,  2022, 79(2), 80.
 [http://dx.doi.org/10.1007/s00018-021-04060-w] [PMID: 35044528]

[22]
Rutsch, A.; Kantsjö, J.B.; Ronchi, F. The gut-brain axis: How microbiota and host inflammasome influence brain physiology and pathology. Front. Immunol.,  2020, 11, 604179.
 [http://dx.doi.org/10.3389/fimmu.2020.604179] [PMID: 33362788]

[23]
Karl, J.P.; Hatch, A.M.; Arcidiacono, S.M.; Pearce, S.C.; Feliciano, P.I.G.; Doherty, L.A.; Soares, J.W. Effects of psychological, environmental and physical stressors on the gut microbiota. Front. Microbiol.,  2018, 9, 2013.
 [http://dx.doi.org/10.3389/fmicb.2018.02013] [PMID: 30258412]

[24]
Gebrayel, P.; Nicco, C.; Al Khodor, S.; Bilinski, J.; Caselli, E.; Comelli, E.M.; Egert, M.; Giaroni, C.; Karpinski, T.M.; Loniewski, I.; Mulak, A.; Reygner, J.; Samczuk, P.; Serino, M.; Sikora, M.; Terranegra, A.; Ufnal, M.; Villeger, R.; Pichon, C.; Konturek, P.; Edeas, M. Microbiota medicine: Towards clinical revolution. J. Transl. Med.,  2022, 20(1), 111.
 [http://dx.doi.org/10.1186/s12967-022-03296-9] [PMID: 35255932]

[25]
Afzaal, M.; Saeed, F.; Shah, Y.A.; Hussain, M.; Rabail, R.; Socol, C.T.; Hassoun, A.; Pateiro, M.; Lorenzo, J.M.; Rusu, A.V.; Aadil, R.M. Human gut microbiota in health and disease: Unveiling the relationship. Front. Microbiol.,  2022, 13, 999001.
 [http://dx.doi.org/10.3389/fmicb.2022.999001] [PMID: 36225386]

[26]
Chidambaram, S.B.; Essa, M.M.; Rathipriya, A.G.; Bishir, M.; Ray, B.; Mahalakshmi, A.M.; Tousif, A.H.; Sakharkar, M.K.; Kashyap, R.S.; Friedland, R.P.; Monaghan, T.M. Gut dysbiosis, defective autophagy and altered immune responses in neurodegenerative diseases: Tales of a vicious cycle. Pharmacol. Ther.,  2022, 231, 107988.
 [http://dx.doi.org/10.1016/j.pharmthera.2021.107988] [PMID: 34536490]

[27]
Carding, S.; Verbeke, K.; Vipond, D.T.; Corfe, B.M.; Owen, L.J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis.,  2015, 26, 26191.
 [PMID: 25651997]

[28]
Scriven, M.; Dinan, T.; Cryan, J.; Wall, M. Neuropsychiatric disorders: Influence of gut microbe to brain signalling. Diseases,  2018, 6(3), 78.
 [http://dx.doi.org/10.3390/diseases6030078] [PMID: 30200574]

[29]
Sandhu, K.V.; Sherwin, E.; Schellekens, H.; Stanton, C.; Dinan, T.G.; Cryan, J.F. Feeding the microbiota-gut-brain axis: Diet, microbiome, and neuropsychiatry. Transl. Res.,  2017, 179, 223-244.
 [http://dx.doi.org/10.1016/j.trsl.2016.10.002] [PMID: 27832936]

[30]
Socała, K.; Doboszewska, U.; Szopa, A.; Serefko, A.; Włodarczyk, M.; Zielińska, A.; Poleszak, E.; Fichna, J.; Wlaź, P. The role of microbiota-gut-brain axis in neuropsychiatric and neurological disorders. Pharmacol. Res.,  2021, 172, 105840.
 [http://dx.doi.org/10.1016/j.phrs.2021.105840] [PMID: 34450312]

[31]
Zang, Y.; Lai, X.; Li, C.; Ding, D.; Wang, Y.; Zhu, Y. The role of gut microbiota in various neurological and psychiatric disorders-an evidence mapping based on quantified evidence. Mediators Inflamm.,  2023, 2023, 1-16.
 [http://dx.doi.org/10.1155/2023/5127157] [PMID: 36816743]

[32]
Suganya, K.; Koo, B.S. Gut-brain axis: Role of gut microbiota on neurological disorders and how probiotics/prebiotics beneficially modulate microbial and immune pathways to improve brain functions. Int. J. Mol. Sci.,  2020, 21(20), 7551.
 [http://dx.doi.org/10.3390/ijms21207551] [PMID: 33066156]

[33]
Abo-Shaban, T.; Sharna, S.S.; Hosie, S.; Lee, C.Y.Q.; Balasuriya, G.K.; McKeown, S.J.; Franks, A.E.; Yardin, H.E.L. Issues for patchy tissues: Defining roles for gut-associated lymphoid tissue in neurodevelopment and disease. J. Neural Transm.,  2023, 130(3), 269-280.
 [http://dx.doi.org/10.1007/s00702-022-02561-x] [PMID: 36309872]

[34]
Agustí, A.; Pardo, G.M.P.; Almela, L.I.; Campillo, I.; Maes, M.; Pérez, R.M.; Sanz, Y. Interplay between the gut-brain axis, obesity and cognitive function. Front. Neurosci.,  2018, 12, 155.
 [http://dx.doi.org/10.3389/fnins.2018.00155] [PMID: 29615850]

[35]
Rudzki, L.; Maes, M. The microbiota-gut-immune-glia (MGIG) axis in major depression. Mol. Neurobiol.,  2020, 57(10), 4269-4295.
 [http://dx.doi.org/10.1007/s12035-020-01961-y] [PMID: 32700250]

[36]
Clapp, M.; Aurora, N.; Herrera, L.; Bhatia, M.; Wilen, E.; Wakefield, S. Gut microbiota’s effect on mental health: The gut-brain axis. Clin. Pract.,  2017, 7(4), 987.
 [http://dx.doi.org/10.4081/cp.2017.987] [PMID: 29071061]

[37]
Berk, M.; Williams, L.J.; Jacka, F.N.; O’Neil, A.; Pasco, J.A.; Moylan, S.; Allen, N.B.; Stuart, A.L.; Hayley, A.C.; Byrne, M.L.; Maes, M. So depression is an inflammatory disease, but where does the inflammation come from? BMC Med.,  2013, 11(1), 200.
 [http://dx.doi.org/10.1186/1741-7015-11-200] [PMID: 24228900]

[38]
Maes, M.; Vasupanrajit, A.; Jirakran, K.; Klomkliew, P.; Chanchaem, P.; Tunvirachaisakul, C.; Plaimas, K.; Suratanee, A.; Payungporn, S. Adverse childhood experiences and reoccurrence of illness impact the gut microbiome, which affects suicidal behaviours and the phenome of major depression: Towards enterotypic phenotypes. Acta Neuropsychiatr.,  2023, 35(6), 328-345.
 [http://dx.doi.org/10.1017/neu.2023.21] [PMID: 37052305]

[39]
Maes, M.; Yirmyia, R.; Noraberg, J.; Brene, S.; Hibbeln, J.; Perini, G.; Kubera, M.; Bob, P.; Lerer, B.; Maj, M. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab. Brain Dis.,  2009, 24(1), 27-53.
 [http://dx.doi.org/10.1007/s11011-008-9118-1] [PMID: 19085093]

[40]
Rudzki, L.; Maes, M. From “Leaky Gut” to impaired glia-neuron communication in depression. Adv. Exp. Med. Biol.,  2021, 1305, 129-155.
 [http://dx.doi.org/10.1007/978-981-33-6044-0_9] [PMID: 33834399]

[41]
Martínez, R.S.; Real, S.L.; García, G.A.P.; Cruz, T.E.; Jonapa, C.L.A.; Amedei, A.; García, A.M.M. Neuroinflammation, microbiota-gut-brain axis, and depression: The vicious circle. J. Integr. Neurosci.,  2023, 22(3), 65.
 [http://dx.doi.org/10.31083/j.jin2203065] [PMID: 37258450]

[42]
Qin, H.Y.; Cheng, C.W.; Tang, X.D.; Bian, Z.X. Impact of psychological stress on irritable bowel syndrome. World J. Gastroenterol.,  2014, 20(39), 14126-14131.
 [http://dx.doi.org/10.3748/wjg.v20.i39.14126] [PMID: 25339801]

[43]
Belei, O.; Basaca, D.G.; Olariu, L.; Pantea, M.; Bozgan, D.; Nanu, A.; Sîrbu, I.; Mărginean, O.; Enătescu, I. The interaction between stress and inflammatory bowel disease in pediatric and adult patients. J. Clin. Med.,  2024, 13(5), 1361.
 [http://dx.doi.org/10.3390/jcm13051361] [PMID: 38592680]

[44]
Howland, R.H. Vagus nerve stimulation. Curr. Behav. Neurosci. Rep.,  2014, 1(2), 64-73.
 [http://dx.doi.org/10.1007/s40473-014-0010-5] [PMID: 24834378]

[45]
Berthoud, H.R.; Neuhuber, W.L. Functional and chemical anatomy of the afferent vagal system. Auton. Neurosci.,  2000, 85(1-3), 1-17.
 [http://dx.doi.org/10.1016/S1566-0702(00)00215-0] [PMID: 11189015]

[46]
Forsythe, P.; Bienenstock, J.; Kunze, W.A. Vagal pathways for microbiome-brain-gut axis communication. Adv. Exp. Med. Biol.,  2014, 817, 115-133.
 [http://dx.doi.org/10.1007/978-1-4939-0897-4_5] [PMID: 24997031]

[47]
Latorre, R.; Sternini, C.; Giorgio, D.R.; Meerveld, G.V.B. Enteroendocrine cells: A review of their role in brain–gut communication. Neurogastroenterol. Motil.,  2016, 28(5), 620-630.
 [http://dx.doi.org/10.1111/nmo.12754] [PMID: 26691223]

[48]
Kanai, T.; Teratani, T. Role of the vagus nerve in the gut-brain axis: Development and maintenance of gut regulatory T cells via the liver-brain-gut vago-vagal reflex. Brain Nerve,  2022, 74(8), 971-977.
 [PMID: 35941793]

[49]
Han, Y.; Wang, B.; Gao, H.; He, C.; Hua, R.; Liang, C.; Zhang, S.; Wang, Y.; Xin, S.; Xu, J. Vagus nerve and underlying impact on the gut microbiota-brain axis in behavior and neurodegenerative diseases. J. Inflamm. Res.,  2022, 15, 6213-6230.
 [http://dx.doi.org/10.2147/JIR.S384949] [PMID: 36386584]

[50]
Chang, L.; Wei, Y.; Hashimoto, K. Brain–gut–microbiota axis in depression: A historical overview and future directions. Brain Res. Bull.,  2022, 182, 44-56.
 [http://dx.doi.org/10.1016/j.brainresbull.2022.02.004] [PMID: 35151796]

[51]
Garg, K.; Mohajeri, M.H. Potential effects of the most prescribed drugs on the microbiota-gut-brain-axis: A review. Brain Res. Bull.,  2024, 207, 110883.
 [http://dx.doi.org/10.1016/j.brainresbull.2024.110883] [PMID: 38244807]

[52]
Vich Vila, A.; Collij, V.; Sanna, S.; Sinha, T.; Imhann, F.; Bourgonje, A.R.; Mujagic, Z.; Jonkers, D.M.A.E.; Masclee, A.A.M.; Fu, J.; Kurilshikov, A.; Wijmenga, C.; Zhernakova, A.; Weersma, R.K. Impact of commonly used drugs on the composition and metabolic function of the gut microbiota. Nat. Commun.,  2020, 11(1), 362.
 [http://dx.doi.org/10.1038/s41467-019-14177-z] [PMID: 31953381]

[53]
Karakan, T.; Ozkul, C.; Akkol, K.E.; Bilici, S.; Sánchez, S.E.; Capasso, R. Gut-brain-microbiota axis: Antibiotics and functional gastrointestinal disorders. Nutrients,  2021, 13(2), 389.
 [http://dx.doi.org/10.3390/nu13020389] [PMID: 33513791]

[54]
Maier, L.; Pruteanu, M.; Kuhn, M.; Zeller, G.; Telzerow, A.; Anderson, E.E.; Brochado, A.R.; Fernandez, K.C.; Dose, H.; Mori, H.; Patil, K.R.; Bork, P.; Typas, A. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature,  2018, 555(7698), 623-628.
 [http://dx.doi.org/10.1038/nature25979] [PMID: 29555994]

[55]
Essmat, N.; Karádi, D.Á.; Zádor, F.; Király, K.; Fürst, S.; Khrasani, A.M. Insights into the current and possible future use of opioid antagonists in relation to opioid-induced constipation and dysbiosis. Molecules,  2023, 28(23), 7766.
 [http://dx.doi.org/10.3390/molecules28237766] [PMID: 38067494]

[56]
Bernabè, G.; Shalata, M.E.M.; Zatta, V.; Bellato, M.; Porzionato, A.; Castagliuolo, I.; Brun, P. Antibiotic treatment induces long-lasting effects on gut microbiota and the enteric nervous system in mice. Antibiotics,  2023, 12(6), 1000.
 [http://dx.doi.org/10.3390/antibiotics12061000] [PMID: 37370319]

[57]
Caparrós-Martín, J.A.; Lareu, R.R.; Ramsay, J.P.; Peplies, J.; Reen, F.J.; Headlam, H.A.; Ward, N.C.; Croft, K.D.; Newsholme, P.; Hughes, J.D.; O’Gara, F. Statin therapy causes gut dysbiosis in mice through a PXR-dependent mechanism. Microbiome,  2017, 5(1), 95.
 [http://dx.doi.org/10.1186/s40168-017-0312-4] [PMID: 28793934]

[58]
Doestzada, M.; Vila, A.V.; Zhernakova, A.; Koonen, D.P.Y.; Weersma, R.K.; Touw, D.J.; Kuipers, F.; Wijmenga, C.; Fu, J. Pharmacomicrobiomics: A novel route towards personalized medicine? Protein Cell,  2018, 9(5), 432-445.
 [http://dx.doi.org/10.1007/s13238-018-0547-2] [PMID: 29705929]

[59]
Crişan, I.M.; Dumitraşcu, D.L. Irritable bowel syndrome: Peripheral mechanisms and therapeutic implications. Clujul Med.,  2014, 87(2), 73-79.
 [PMID: 26528001]

[60]
Saha, L. Irritable bowel syndrome: Pathogenesis, diagnosis, treatment, and evidence-based medicine. World J. Gastroenterol.,  2014, 20(22), 6759-6773.
 [http://dx.doi.org/10.3748/wjg.v20.i22.6759] [PMID: 24944467]

[61]
Weaver, K.R.; Melkus, G.D.E.; Henderson, W.A. Irritable bowel syndrome. Am. J. Nurs.,  2017, 117(6), 48-55.
 [http://dx.doi.org/10.1097/01.NAJ.0000520253.57459.01] [PMID: 28541989]

[62]
Lee, Y.J.; Park, K.S. Irritable bowel syndrome: Emerging paradigm in pathophysiology. World J. Gastroenterol.,  2014, 20(10), 2456-2469.
 [http://dx.doi.org/10.3748/wjg.v20.i10.2456] [PMID: 24627583]

[63]
Chong, P.P.; Chin, V.K.; Looi, C.Y.; Wong, W.F.; Madhavan, P.; Yong, V.C. The microbiome and irritable bowel syndrome - A review on the pathophysiology, current research and future therapy. Front. Microbiol.,  2019, 10, 1136.
 [http://dx.doi.org/10.3389/fmicb.2019.01136] [PMID: 31244784]

[64]
Oka, P.; Parr, H.; Barberio, B.; Black, C.J.; Savarino, E.V.; Ford, A.C. Global prevalence of irritable bowel syndrome according to Rome III or IV criteria: A systematic review and meta-analysis. Lancet Gastroenterol. Hepatol.,  2020, 5(10), 908-917.
 [http://dx.doi.org/10.1016/S2468-1253(20)30217-X] [PMID: 32702295]

[65]
Camilleri, M. Diagnosis and treatment of irritable bowel syndrome: A review. JAMA,  2021, 325(9), 865-877.
 [http://dx.doi.org/10.1001/jama.2020.22532] [PMID: 33651094]

[66]
Dinic, R.B.; Rajkovic, T.S.; Grgov, S.; Petrovic, G.; Zivkovic, V. Irritable bowel syndrome - From etiopathogenesis to therapy. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub.,  2018, 162(1), 1-9.
 [http://dx.doi.org/10.5507/bp.2017.057] [PMID: 29358788]

[67]
Rodiño-Janeiro, B.K.; Vicario, M.; Cotoner, A.C.; García, P.R.; Santos, J. A review of microbiota and irritable bowel syndrome: Future in therapies. Adv. Ther.,  2018, 35(3), 289-310.
 [http://dx.doi.org/10.1007/s12325-018-0673-5] [PMID: 29498019]

[68]
Black, C.J.; Thakur, E.R.; Houghton, L.A.; Quigley, E.M.M.; Moayyedi, P.; Ford, A.C. Efficacy of psychological therapies for irritable bowel syndrome: Systematic review and network meta-analysis. Gut,  2020, 69(8), 1441-1451.
 [http://dx.doi.org/10.1136/gutjnl-2020-321191] [PMID: 32276950]

[69]
Grundmann, O.; Yoon, S.L. Irritable bowel syndrome: Epidemiology, diagnosis and treatment: An update for health‐care practitioners. J. Gastroenterol. Hepatol.,  2010, 25(4), 691-699.
 [http://dx.doi.org/10.1111/j.1440-1746.2009.06120.x] [PMID: 20074154]

[70]
Staudacher, H.M.; Walus, M.A.; Ford, A.C. Common mental disorders in irritable bowel syndrome: pathophysiology, management, and considerations for future randomised controlled trials. Lancet Gastroenterol. Hepatol.,  2021, 6(5), 401-410.
 [http://dx.doi.org/10.1016/S2468-1253(20)30363-0] [PMID: 33587890]

[71]
Juruena, M.F.; Eror, F.; Cleare, A.J.; Young, A.H. The role of early life stress in HPA axis and anxiety. Adv. Exp. Med. Biol.,  2020, 1191, 141-153.
 [http://dx.doi.org/10.1007/978-981-32-9705-0_9] [PMID: 32002927]

[72]
Distrutti, E.; Monaldi, L.; Ricci, P.; Fiorucci, S. Gut microbiota role in irritable bowel syndrome: New therapeutic strategies. World J. Gastroenterol.,  2016, 22(7), 2219-2241.
 [http://dx.doi.org/10.3748/wjg.v22.i7.2219] [PMID: 26900286]

[73]
Occhipinti, K.; Smith, J. Irritable bowel syndrome: A review and update. Clin. Colon Rectal Surg.,  2012, 25(1), 046-052.
 [http://dx.doi.org/10.1055/s-0032-1301759] [PMID: 23449495]

[74]
Kano, M.; Muratsubaki, T.; Van Oudenhove, L.; Morishita, J.; Yoshizawa, M.; Kohno, K.; Yagihashi, M.; Tanaka, Y.; Mugikura, S.; Dupont, P.; Ly, H.G.; Takase, K.; Kanazawa, M.; Fukudo, S. Altered brain and gut responses to corticotropin-releasing hormone (CRH) in patients with irritable bowel syndrome. Sci. Rep.,  2017, 7(1), 12425.
 [http://dx.doi.org/10.1038/s41598-017-09635-x] [PMID: 28963545]

[75]
Tarar, Z.I.; Farooq, U.; Zafar, Y.; Gandhi, M.; Raza, S.; Kamal, F.; Tarar, M.F.; Ghouri, Y.A. Burden of anxiety and depression among hospitalized patients with irritable bowel syndrome: A nationwide analysis. Ir. J. Med. Sci.,  2023, 192(5), 2159-2166.
 [http://dx.doi.org/10.1007/s11845-022-03258-6] [PMID: 36593438]

[76]
Eijsbouts, C.; Zheng, T.; Kennedy, N.A.; Bonfiglio, F.; Anderson, C.A.; Moutsianas, L.; Holliday, J.; Shi, J.; Shringarpure, S.; Agee, M.; Aslibekyan, S.; Auton, A.; Bell, R.K.; Bryc, K.; Clark, S.K.; Elson, S.L.; Brant, K.; Fontanillas, P.; Furlotte, N.A.; Gandhi, P.M.; Heilbron, K.; Hicks, B.; Hinds, D.A.; Huber, K.E.; Jewett, E.M.; Jiang, Y.; Kleinman, A.; Lin, K-H.; Litterman, N.K.; Luff, M.K.; McCreight, J.C.; McIntyre, M.H.; McManus, K.F.; Mountain, J.L.; Mozaffari, S.V.; Nandakumar, P.; Noblin, E.S.; Northover, C.A.M.; O’Connell, J.; Petrakovitz, A.A.; Pitts, S.J.; Poznik, G.D.; Sathirapongsasuti, J.F.; Shastri, A.J.; Shelton, J.F.; Tian, C.; Tung, J.Y.; Tunney, R.J.; Vacic, V.; Wang, X.; Zare, A.S.; Voda, A-I.; Kashyap, P.; Chang, L.; Mayer, E.; Heitkemper, M.; Sayuk, G.S.; Kulka, R.T.; Ringel, Y.; Chey, W.D.; Eswaran, S.; Merchant, J.L.; Shulman, R.J.; Bujanda, L.; Etxebarria, G.K.; Dlugosz, A.; Lindberg, G.; Schmidt, P.T.; Karling, P.; Ohlsson, B.; Walter, S.; Faresjö, Å.O.; Simren, M.; Halfvarson, J.; Portincasa, P.; Barbara, G.; Satta, U.P.; Neri, M.; Nardone, G.; Cuomo, R.; Galeazzi, F.; Bellini, M.; Latiano, A.; Houghton, L.; Jonkers, D.; Kurilshikov, A.; Weersma, R.K.; Netea, M.; Tesarz, J.; Gauss, A.; Stengel, G.M.; Andresen, V.; Frieling, T.; Pehl, C.; Schaefert, R.; Niesler, B.; Lieb, W.; Hanevik, K.; Langeland, N.; Wensaas, K-A.; Litleskare, S.; Gabrielsen, M.E.; Thomas, L.; Thijs, V.; Lemmens, R.; Van Oudenhove, L.; Wouters, M.; Farrugia, G.; Franke, A.; Hübenthal, M.; Abecasis, G.; Zawistowski, M.; Skogholt, A.H.; Jensen, N.E.; Hveem, K.; Esko, T.; Laving, T.M.; Zhernakova, A.; Camilleri, M.; Boeckxstaens, G.; Whorwell, P.J.; Spiller, R.; McVean, G.; D’Amato, M.; Jostins, L.; Parkes, M. Genome-wide analysis of 53,400 people with irritable bowel syndrome highlights shared genetic pathways with mood and anxiety disorders. Nat. Genet.,  2021, 53(11), 1543-1552.
 [http://dx.doi.org/10.1038/s41588-021-00950-8] [PMID: 34741163]

[77]
Aziz, M.; Kumar, J.; Nawawi, M.K.; Ali, R.R.; Mokhtar, N. Irritable bowel syndrome, depression, and neurodegeneration: A bidirectional communication from gut to brain. Nutrients,  2021, 13(9), 3061.
 [http://dx.doi.org/10.3390/nu13093061] [PMID: 34578939]

[78]
Midenfjord, I.; Polster, A.; Sjövall, H.; Törnblom, H.; Simrén, M. Anxiety and depression in irritable bowel syndrome: Exploring the interaction with other symptoms and pathophysiology using multivariate analyses. Neurogastroenterol. Motil.,  2019, 31(8), e13619.
 [http://dx.doi.org/10.1111/nmo.13619] [PMID: 31056802]

[79]
Ng, Q.X.; Soh, A.Y.S.; Loke, W.; Venkatanarayanan, N.; Lim, D.Y.; Yeo, W.S. Systematic review with meta‐analysis: The association between post‐traumatic stress disorder and irritable bowel syndrome. J. Gastroenterol. Hepatol.,  2019, 34(1), 68-73.
 [http://dx.doi.org/10.1111/jgh.14446] [PMID: 30144372]

[80]
Creed, F. Risk factors for self-reported irritable bowel syndrome with prior psychiatric disorder: The lifelines cohort study. J. Neurogastroenterol. Motil.,  2022, 28(3), 442-453.
 [http://dx.doi.org/10.5056/jnm21041] [PMID: 35799238]

[81]
Fadgyas-Stanculete, M.; Buga, A.M.; Popa-Wagner, A.; Dumitrascu, D.L. The relationship between irritable bowel syndrome and psychiatric disorders: From molecular changes to clinical manifestations. J. Mol. Psychiatry,  2014, 2(1), 4.
 [http://dx.doi.org/10.1186/2049-9256-2-4] [PMID: 25408914]

[82]
Lydiard, R.B.; Falsetti, S.A. Experience with anxiety and depression treatment studies: implications for designing irritable bowel syndrome clinical trials. Am. J. Med.,  1999, 107(5), 65-73.
 [http://dx.doi.org/10.1016/S0002-9343(99)00082-0] [PMID: 10588175]

[83]
Tao, E.; Long, G.; Yang, T.; Chen, B.; Guo, R.; Ye, D.; Fang, M.; Jiang, M. Maternal separation induced visceral hypersensitivity evaluated via novel and small size distention balloon in post-weaning mice. Front. Neurosci.,  2022, 15, 803957.
 [http://dx.doi.org/10.3389/fnins.2021.803957] [PMID: 35153662]

[84]
Ge, L.; Liu, S.; Li, S.; Yang, J.; Hu, G.; Xu, C.; Song, W. Psychological stress in inflammatory bowel disease: Psychoneuroimmunological insights into bidirectional gut–brain communications. Front. Immunol.,  2022, 13, 1016578.
 [http://dx.doi.org/10.3389/fimmu.2022.1016578] [PMID: 36275694]

[85]
Sun, Y.; Xie, R.; Li, L.; Jin, G.; Zhou, B.; Huang, H.; Li, M.; Yang, Y.; Liu, X.; Cao, X.; Wang, B.; Liu, W.; Jiang, K.; Cao, H. Prenatal maternal stress exacerbates experimental colitis of offspring in adulthood. Front. Immunol.,  2021, 12, 700995.
 [http://dx.doi.org/10.3389/fimmu.2021.700995] [PMID: 34804005]

[86]
Császár-Nagy, N.; Bókkon, I. Mother-newborn separation at birth in hospitals: A possible risk for neurodevelopmental disorders? Neurosci. Biobehav. Rev.,  2018, 84, 337-351.
 [http://dx.doi.org/10.1016/j.neubiorev.2017.08.013] [PMID: 28851575]

[87]
Bradford, K.; Shih, W.; Videlock, E.J.; Presson, A.P.; Naliboff, B.D.; Mayer, E.A.; Chang, L. Association between early adverse life events and irritable bowel syndrome. Clin. Gastroenterol. Hepatol.,  2012, 10(4), 385-390.e1.
 [http://dx.doi.org/10.1016/j.cgh.2011.12.018]

[88]
Chitkara, D.K.; van Tilburg, M.A.L.; Martin, B.N.; Whitehead, W.E. Early life risk factors that contribute to irritable bowel syndrome in adults: A systematic review. Am. J. Gastroenterol.,  2008, 103(3), 765-774.
 [http://dx.doi.org/10.1111/j.1572-0241.2007.01722.x] [PMID: 18177446]

[89]
Videlock, E.J.; Chang, L. Latest insights on the pathogenesis of irritable bowel syndrome. Gastroenterol. Clin. North Am.,  2021, 50(3), 505-522.
 [http://dx.doi.org/10.1016/j.gtc.2021.04.002] [PMID: 34304785]

[90]
Tang, H.Y.; Jiang, A.J.; Wang, X.Y.; Wang, H.; Guan, Y.Y.; Li, F.; Shen, G.M. Uncovering the pathophysiology of irritable bowel syndrome by exploring the gut-brain axis: A narrative review. Ann. Transl. Med.,  2021, 9(14), 1187.
 [http://dx.doi.org/10.21037/atm-21-2779] [PMID: 34430628]

[91]
Salhy, E.M. Irritable bowel syndrome: Diagnosis and pathogenesis. World J. Gastroenterol.,  2012, 18(37), 5151-5163.
 [http://dx.doi.org/10.3748/wjg.v18.i37.5151] [PMID: 23066308]

[92]
Gieryńska, M.; Szulc-Dąbrowska, L.; Struzik, J.; Mielcarska, M.B.; Zboroch, G.K.P. Integrity of the intestinal barrier: the involvement of epithelial cells and microbiota-a mutual relationship. Animals,  2022, 12(2), 145.
 [http://dx.doi.org/10.3390/ani12020145] [PMID: 35049768]

[93]
Gritz, E.C.; Bhandari, V. The human neonatal gut microbiome: A brief review. Front Pediatr.,  2015, 3, 17.
 [PMID: 25798435]

[94]
Wu, H.J.; Wu, E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes,  2012, 3(1), 4-14.
 [http://dx.doi.org/10.4161/gmic.19320] [PMID: 22356853]

[95]
Ng, Q.X.; Soh, A.Y.S.; Loke, W.; Lim, D.Y.; Yeo, W.S. The role of inflammation in irritable bowel syndrome (IBS). J. Inflamm. Res.,  2018, 11, 345-349.
 [http://dx.doi.org/10.2147/JIR.S174982] [PMID: 30288077]

[96]
Shi, N.; Li, N.; Duan, X.; Niu, H. Interaction between the gut microbiome and mucosal immune system. Mil. Med. Res.,  2017, 4(1), 14.
 [http://dx.doi.org/10.1186/s40779-017-0122-9] [PMID: 28465831]

[97]
Lazaridis, N.; Germanidis, G. Current insights into the innate immune system dysfunction in irritable bowel syndrome. Ann. Gastroenterol.,  2018, 31(2), 171-187.
 [http://dx.doi.org/10.20524/aog.2018.0229] [PMID: 29507464]

[98]
Akiho, H.; Ihara, E.; Nakamura, K. Low-grade inflammation plays a pivotal role in gastrointestinal dysfunction in irritable bowel syndrome. World J. Gastrointest. Pathophysiol.,  2010, 1(3), 97-105.
 [http://dx.doi.org/10.4291/wjgp.v1.i3.97] [PMID: 21607147]

[99]
El-Hakim, Y.; Bake, S.; Mani, K.K.; Sohrabji, F. Impact of intestinal disorders on central and peripheral nervous system diseases. Neurobiol. Dis.,  2022, 165, 105627.
 [http://dx.doi.org/10.1016/j.nbd.2022.105627] [PMID: 35032636]

[100]
Lu, S.; Jiang, H.; Shi, Y. Association between irritable bowel syndrome and Parkinson’s disease: A systematic review and meta‐analysis. Acta Neurol. Scand.,  2022, 145(4), 442-448.
 [http://dx.doi.org/10.1111/ane.13570] [PMID: 34908158]

[101]
Yoon, S.Y.; Shin, J.; Heo, S.J.; Chang, J.S.; Sunwoo, M.K.; Kim, Y.W. Irritable bowel syndrome and subsequent risk of Parkinson’s disease: A nationwide population-based matched-cohort study. J. Neurol.,  2022, 269(3), 1404-1412.
 [http://dx.doi.org/10.1007/s00415-021-10688-2] [PMID: 34255181]

[102]
Alvino, B.; Arianna, F.; Assunta, B.; Antonio, C.; Emanuele, D.; Giorgia, M.; Leonardo, S.; Daniele, S.; Renato, D.; Buscarinu, M.C.; Massimiliano, M.; Crisafulli, S.G.; Aurora, Z.; Nicoletti, G.C.; Marco, S.; Viola, B.; Francesco, P.; Marfia, A.G.; Grazia, S.; Valentina, S.; Davide, O.; Giovanni, S.; Gioacchino, T.; Gallo, A. Prevalence and predictors of bowel dysfunction in a large multiple sclerosis outpatient population: An Italian multicenter study. J. Neurol.,  2022, 269(3), 1610-1617. [Erratum in: Prevalence and predictors of bowel dysfunction in a large multiple sclerosis outpatient population: An Italian multicenter study. J. Neurol., 2022; 269(5): 2824-2825.

[103]
Lee, Y.T.; Hu, L.Y.; Shen, C.C.; Huang, M.W.; Tsai, S.J.; Yang, A.C.; Hu, C.K.; Perng, C.L.; Huang, Y.S.; Hung, J.H. Risk of psychiatric disorders following irritable bowel syndrome: A nationwide population-based cohort study. PLoS One,  2015, 10(7), e0133283.
 [http://dx.doi.org/10.1371/journal.pone.0133283] [PMID: 26222511]

[104]
Meade, E.; Garvey, M. The Role of neuro-immune interaction in chronic pain conditions; Functional somatic syndrome, neurogenic inflammation, and peripheral neuropathy. Int. J. Mol. Sci.,  2022, 23(15), 8574.
 [http://dx.doi.org/10.3390/ijms23158574] [PMID: 35955708]

[105]
Frauches, B.A.C.; Boesmans, W. The enteric nervous system: The hub in a star network. Nat. Rev. Gastroenterol. Hepatol.,  2020, 17(12), 717-718.
 [http://dx.doi.org/10.1038/s41575-020-00377-2] [PMID: 33087897]

[106]
Holland, A.M.; Frauches, B.A.C.; Keszthelyi, D.; Melotte, V.; Boesmans, W. The enteric nervous system in gastrointestinal disease etiology. Cell. Mol. Life Sci.,  2021, 78(10), 4713-4733.
 [http://dx.doi.org/10.1007/s00018-021-03812-y] [PMID: 33770200]

[107]
Nagy, N.; Goldstein, A.M. Enteric nervous system development: A crest cell’s journey from neural tube to colon. Semin. Cell Dev. Biol.,  2017, 66, 94-106.
 [http://dx.doi.org/10.1016/j.semcdb.2017.01.006] [PMID: 28087321]

[108]
Gershon, M.D.; Ratcliffe, E.M. Developmental biology of the enteric nervous system: Pathogenesis of Hirschsprung’s disease and other congenital dysmotilities. Semin. Pediatr. Surg.,  2004, 13(4), 224-235.
 [http://dx.doi.org/10.1053/j.sempedsurg.2004.10.019] [PMID: 15660316]

[109]
Torroglosa, A.; Alves, M.M.; Fernández, R.M.; Antiñolo, G.; Hofstra, R.M.; Borrego, S. Epigenetics in ENS development and Hirschsprung disease. Dev. Biol.,  2016, 417(2), 209-216.
 [http://dx.doi.org/10.1016/j.ydbio.2016.06.017] [PMID: 27321561]

[110]
de Jonge, W.J. The gut’s little brain in control of intestinal immunity. ISRN Gastroenterol.,  2013, 2013, 1-17.
 [http://dx.doi.org/10.1155/2013/630159] [PMID: 23691339]

[111]
Yang, X.; Lou, J.; Shan, W.; Ding, J.; Jin, Z.; Hu, Y.; Du, Q.; Liao, Q.; Xie, R.; Xu, J. Pathophysiologic role of neurotransmitters in digestive diseases. Front. Physiol.,  2021, 12, 567650.
 [http://dx.doi.org/10.3389/fphys.2021.567650] [PMID: 34194334]

[112]
Spencer, N.J.; Travis, L.; Wiklendt, L.; Costa, M.; Hibberd, T.J.; Brookes, S.J.; Dinning, P.; Hu, H.; Wattchow, D.A.; Sorensen, J. Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice. Commun. Biol.,  2021, 4(1), 955.
 [http://dx.doi.org/10.1038/s42003-021-02485-4] [PMID: 34376798]

[113]
Annahazi, A.; Schemann, M. The enteric nervous system: “A little brain in the gut”. Neuroforum,  2020, 26(1), 31-42.
 [http://dx.doi.org/10.1515/nf-2019-0027]

[114]
Schemann, M.; Frieling, T.; Enck, P. To learn, to remember, to forget—How smart is the gut? Acta Physiol.,  2020, 228(1), e13296.
 [http://dx.doi.org/10.1111/apha.13296] [PMID: 31063665]

[115]
Furness, J.B.; Clerc, N.; Kunze, W.A. Memory in the enteric nervous system. Gut,  2000, 47(S4), 60-62.
 [http://dx.doi.org/10.1136/gut.47.suppl_4.iv60]

[116]
Cheng, L. Progress on the regulation of DNA methylation in the development of the enteric nervous system. Int. J. Pediatr.,  2018, 6, 756-760.

[117]
Jaroy, E.G.; Acosta-Jimenez, L.; Hotta, R.; Goldstein, A.M.; Emblem, R.; Klungland, A.; Ougland, R. “Too much guts and not enough brains”: (epi)genetic mechanisms and future therapies of Hirschsprung disease — A review. Clin. Epigenetics,  2019, 11(1), 135.
 [http://dx.doi.org/10.1186/s13148-019-0718-x] [PMID: 31519213]

[118]
Uribe, R.A. Genetic regulation of enteric nervous system development in zebrafish. Biochem. Soc. Trans.,  2024, 52(1), 177-190.
 [http://dx.doi.org/10.1042/BST20230343] [PMID: 38174765]

[119]
Kenny, S.E.; Tam, P.K.H.; Barcelo, G.M. Hirschsprung’s disease. Semin. Pediatr. Surg.,  2010, 19(3), 194-200.
 [http://dx.doi.org/10.1053/j.sempedsurg.2010.03.004] [PMID: 20610192]

[120]
Diposarosa, R.; Bustam, N.A.; Sahiratmadja, E.; Susanto, P.S.; Sribudiani, Y. Literature review: Enteric nervous system development, genetic and epigenetic regulation in the etiology of Hirschsprung’s disease. Heliyon,  2021, 7(6), e07308.
 [http://dx.doi.org/10.1016/j.heliyon.2021.e07308] [PMID: 34195419]

[121]
Brosens, E.; Burns, A.J.; Brooks, A.S.; Matera, I.; Borrego, S.; Ceccherini, I.; Tam, P.K.; Barceló, G.M.M.; Thapar, N.; Benninga, M.A.; Hofstra, R.M.W.; Alves, M.M. Genetics of enteric neuropathies. Dev. Biol.,  2016, 417(2), 198-208.
 [http://dx.doi.org/10.1016/j.ydbio.2016.07.008] [PMID: 27426273]

[122]
Torroglosa, A.; Villalba-Benito, L.; Toro, L.B.; Fernández, R.M.; Antiñolo, G.; Borrego, S. Epigenetic mechanisms in hirschsprung disease. Int. J. Mol. Sci.,  2019, 20(13), 3123.
 [http://dx.doi.org/10.3390/ijms20133123] [PMID: 31247956]

[123]
Heanue, T.A.; Shepherd, I.T.; Burns, A.J. Enteric nervous system development in avian and zebrafish models. Dev. Biol.,  2016, 417(2), 129-138.
 [http://dx.doi.org/10.1016/j.ydbio.2016.05.017] [PMID: 27235814]

[124]
Kuil, L.E.; Chauhan, R.K.; Cheng, W.W.; Hofstra, R.M.W.; Alves, M.M. Zebrafish: A model organism for studying enteric nervous system development and disease. Front. Cell Dev. Biol.,  2021, 8, 629073.
 [http://dx.doi.org/10.3389/fcell.2020.629073] [PMID: 33553169]

[125]
Ganz, J.; Melancon, E.; Wilson, C.; Amores, A.; Batzel, P.; Strader, M.; Braasch, I.; Diba, P.; Kuhlman, J.A.; Postlethwait, J.H.; Eisen, J.S. Epigenetic factors Dnmt1 and Uhrf1 coordinate intestinal development. Dev. Biol.,  2019, 455(2), 473-484.
 [http://dx.doi.org/10.1016/j.ydbio.2019.08.002] [PMID: 31394080]

[126]
Feng, G.; Sun, Y. The Polycomb group gene rnf2 is essential for central and enteric neural system development in zebrafish. Front. Neurosci.,  2022, 16, 960149.
 [http://dx.doi.org/10.3389/fnins.2022.960149] [PMID: 36117635]

[127]
Liu, J.; Tan, Y.; Cheng, H.; Zhang, D.; Feng, W.; Peng, C. Functions of gut microbiota metabolites, current status and future perspectives. Aging Dis.,  2022, 13(4), 1106-1126.
 [http://dx.doi.org/10.14336/AD.2022.0104] [PMID: 35855347]

[128]
Fujisaka, S.; Watanabe, Y.; Tobe, K. The gut microbiome: A core regulator of metabolism. J. Endocrinol.,  2023, 256(3), e220111.
 [http://dx.doi.org/10.1530/JOE-22-0111] [PMID: 36458804]

[129]
Ansari, M.H.R.; Saher, S.; Parveen, R.; Khan, W.; Khan, I.A.; Ahmad, S. Role of gut microbiota metabolism and biotransformation on dietary natural products to human health implications with special reference to biochemoinformatics approach. J. Tradit. Complement. Med.,  2023, 13(2), 150-160.
 [http://dx.doi.org/10.1016/j.jtcme.2022.03.005] [PMID: 36970455]

[130]
Swer, N.M.; Venkidesh, B.S.; Murali, T.S.; Mumbrekar, K.D. Gut microbiota-derived metabolites and their importance in neurological disorders. Mol. Biol. Rep.,  2023, 50(2), 1663-1675.
 [http://dx.doi.org/10.1007/s11033-022-08038-0] [PMID: 36399245]

[131]
Yeramilli, V.; Cheddadi, R.; Shah, J.; Brawner, K.; Martin, C. A Review of the impact of maternal prenatal stress on offspring microbiota and metabolites. Metabolites,  2023, 13(4), 535.
 [http://dx.doi.org/10.3390/metabo13040535] [PMID: 37110193]

[132]
Mepham, J.; McGee, N.T.; Andrews, K.; Gonzalez, A. Exploring the effect of prenatal maternal stress on the microbiomes of mothers and infants: A systematic review. Dev. Psychobiol.,  2023, 65(7), e22424.
 [http://dx.doi.org/10.1002/dev.22424] [PMID: 37860905]

[133]
Yang, H.; Guo, R.; Li, S.; Liang, F.; Tian, C.; Zhao, X.; Long, Y.; Liu, F.; Jiang, M.; Zhang, Y.; Ma, J.; Peng, M.; Zhang, S.; Ye, W.; Gan, Q.; Zeng, F.; Mao, S.; Liang, Q.; Ma, X.; Han, M.; Gao, F.; Yang, R.; Zhang, C.; Xiao, L.; Qin, J.; Li, S.; Zhu, C. Systematic analysis of gut microbiota in pregnant women and its correlations with individual heterogeneity. NPJ Biofilms Microbiomes,  2020, 6(1), 32.
 [http://dx.doi.org/10.1038/s41522-020-00142-y] [PMID: 32917878]

[134]
Gorczyca, K.; Obuchowska, A.; Trojnar, K.Ż.; Opoka, W.M.; Gorzelak, L.B. Changes in the gut microbiome and pathologies in pregnancy. Int. J. Environ. Res. Public Health,  2022, 19(16), 9961.
 [http://dx.doi.org/10.3390/ijerph19169961] [PMID: 36011603]

[135]
Srinivasan, K.; Satyanarayana, V.A.; Lukose, A. Maternal mental health in pregnancy and child behavior. Indian J. Psychiatry,  2011, 53(4), 351-361.
 [http://dx.doi.org/10.4103/0019-5545.91911] [PMID: 22303046]

[136]
Tuovinen, S.; Pulkkinen, L.M.; Girchenko, P.; Heinonen, K.; Lahti, J.; Reynolds, R.M.; Hämäläinen, E.; Villa, P.M.; Kajantie, E.; Laivuori, H.; Raikkonen, K. Maternal antenatal stress and mental and behavioral disorders in their children. J. Affect. Disord.,  2021, 278, 57-65.
 [http://dx.doi.org/10.1016/j.jad.2020.09.063] [PMID: 32950844]

[137]
Van den Bergh, B.R.H.; van den Heuvel, M.I.; Lahti, M.; Braeken, M.; de Rooij, S.R.; Entringer, S.; Hoyer, D.; Roseboom, T.; Räikkönen, K.; King, S.; Schwab, M. Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neurosci. Biobehav. Rev.,  2020, 117, 26-64.
 [http://dx.doi.org/10.1016/j.neubiorev.2017.07.003] [PMID: 28757456]

[138]
Sulkowska, S.E.M. The impact of maternal gut microbiota during pregnancy on fetal gut-brain axis development and life-long health outcomes. Microorganisms,  2023, 11(9), 2199.
 [http://dx.doi.org/10.3390/microorganisms11092199] [PMID: 37764043]

[139]
Rusch, J.A.; Layden, B.T.; Dugas, L.R. Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis. Front. Endocrinol.,  2023, 14, 1130689.
 [http://dx.doi.org/10.3389/fendo.2023.1130689] [PMID: 37404311]

[140]
Misiak, B.; Łoniewski, I.; Marlicz, W.; Frydecka, D.; Szulc, A.; Rudzki, L.; Samochowiec, J. The HPA axis dysregulation in severe mental illness: Can we shift the blame to gut microbiota? Prog. Neuropsychopharmacol. Biol. Psychiatry,  2020, 102, 109951.
 [http://dx.doi.org/10.1016/j.pnpbp.2020.109951] [PMID: 32335265]

[141]
Turroni, F.; Rizzo, S.M.; Ventura, M.; Bernasconi, S. Cross-talk between the infant/maternal gut microbiota and the endocrine system: A promising topic of research. Microbiome Res Rep.,  2022, 1(2), 14.
 [http://dx.doi.org/10.20517/mrr.2021.14] [PMID: 38045647]

[142]
Garzoni, L.; Faure, C.; Frasch, M.G. Fetal cholinergic anti-inflammatory pathway and necrotizing enterocolitis: The brain-gut connection begins in utero. Front. Integr. Nuerosci.,  2013, 7, 57.
 [http://dx.doi.org/10.3389/fnint.2013.00057] [PMID: 23964209]

[143]
Zijlmans, M.A.C.; Korpela, K.; Walraven, R.J.M.; de Vos, W.M.; de Weerth, C. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology,  2015, 53, 233-245.
 [http://dx.doi.org/10.1016/j.psyneuen.2015.01.006] [PMID: 25638481]

[144]
Gur, T.L.; Palkar, A.V.; Rajasekera, T.; Allen, J.; Niraula, A.; Godbout, J.; Bailey, M.T. Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring. Behav. Brain Res.,  2019, 359, 886-894.
 [http://dx.doi.org/10.1016/j.bbr.2018.06.025] [PMID: 29949734]

[145]
Silva, Y.P.; Bernardi, A.; Frozza, R.L. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front. Endocrinol.,  2020, 11, 25.
 [http://dx.doi.org/10.3389/fendo.2020.00025] [PMID: 32082260]

[146]
Dalile, B.; Vervliet, B.; Bergonzelli, G.; Verbeke, K.; Oudenhove, V.L. Colon-delivered short-chain fatty acids attenuate the cortisol response to psychosocial stress in healthy men: A randomized, placebo-controlled trial. Neuropsychopharmacology,  2020, 45(13), 2257-2266.
 [http://dx.doi.org/10.1038/s41386-020-0732-x] [PMID: 32521538]

[147]
Zhang, D.; Jian, Y.P.; Zhang, Y.N.; Li, Y.; Gu, L.T.; Sun, H.H.; Liu, M.D.; Zhou, H.L.; Wang, Y.S.; Xu, Z.X. Short-chain fatty acids in diseases. Cell Commun. Signal.,  2023, 21(1), 212.
 [http://dx.doi.org/10.1186/s12964-023-01219-9] [PMID: 37596634]

[148]
Chen, B.; Sun, L.; Zhang, X. Integration of microbiome and epigenome to decipher the pathogenesis of autoimmune diseases. J. Autoimmun.,  2017, 83, 31-42.
 [http://dx.doi.org/10.1016/j.jaut.2017.03.009] [PMID: 28342734]

[149]
Li, L.; Zhao, S.; Xiang, T.; Feng, H.; Ma, L.; Fu, P. Epigenetic connection between gut microbiota-derived short-chain fatty acids and chromatin histone modification in kidney diseases. Chin. Med. J.,  2022, 135(14), 1692-1694.
 [http://dx.doi.org/10.1097/CM9.0000000000002295] [PMID: 36193977]

[150]
Stein, R.A.; Riber, L. Epigenetic effects of short-chain fatty acids from the large intestine on host cells. Microlife,  2023, 4, uqad032.

[151]
Woo, V.; Alenghat, T. Epigenetic regulation by gut microbiota. Gut Microbes,  2022, 14(1), 2022407.
 [http://dx.doi.org/10.1080/19490976.2021.2022407] [PMID: 35000562]

[152]
Yang, L.L.; Millischer, V.; Rodin, S.; MacFabe, D.F.; Villaescusa, J.C.; Lavebratt, C. Enteric short‐chain fatty acids promote proliferation of human neural progenitor cells. J. Neurochem.,  2020, 154(6), 635-646.
 [http://dx.doi.org/10.1111/jnc.14928] [PMID: 31784978]

[153]
Kimura, I.; Miyamoto, J.; Kitano, O.R.; Watanabe, K.; Yamada, T.; Onuki, M.; Aoki, R.; Isobe, Y.; Kashihara, D.; Inoue, D.; Inaba, A.; Takamura, Y.; Taira, S.; Kumaki, S.; Watanabe, M.; Ito, M.; Nakagawa, F.; Irie, J.; Kakuta, H.; Shinohara, M.; Iwatsuki, K.; Tsujimoto, G.; Ohno, H.; Arita, M.; Itoh, H.; Hase, K. Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice. Science,  2020, 367(6481), eaaw8429.
 [http://dx.doi.org/10.1126/science.aaw8429] [PMID: 32108090]

[154]
Liu, R.T. Childhood adversities and depression in adulthood: Current findings and future directions. Clin. Psychol. Sci. Pract.,  2017, 24(2), 140-153.
 [http://dx.doi.org/10.1111/cpsp.12190] [PMID: 28924333]

[155]
Garcia-Rizo, C.; Bitanihirwe, B.K.Y. Implications of early life stress on fetal metabolic programming of schizophrenia: A focus on epiphenomena underlying morbidity and early mortality. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2020, 101, 109910.
 [http://dx.doi.org/10.1016/j.pnpbp.2020.109910] [PMID: 32142745]

[156]
Kwon, E.J.; Kim, Y.J. What is fetal programming?: A lifetime health is under the control of in utero health. Obstet. Gynecol. Sci.,  2017, 60(6), 506-519.
 [http://dx.doi.org/10.5468/ogs.2017.60.6.506] [PMID: 29184858]

[157]
Gluckma, P.D.; Hanson, M.A. Predictive adaptive responses and human disease. In: The fetal matrix. Evolution, development and disease Cambridge; Cambridge Universiy Press: UK, 2005; pp. 78-102.

[158]
Zietlow, A.L.; Nonnenmacher, N.; Reck, C.; Ditzen, B.; Müller, M. Emotional stress during pregnancy - Associations with maternal anxiety disorders, infant cortisol reactivity, and mother-child interaction at pre-school age. Front. Psychol.,  2019, 10, 2179.
 [http://dx.doi.org/10.3389/fpsyg.2019.02179] [PMID: 31607996]

[159]
Howerton, C.L.; Bale, T.L. Prenatal programing: At the intersection of maternal stress and immune activation. Horm. Behav.,  2012, 62(3), 237-242.
 [http://dx.doi.org/10.1016/j.yhbeh.2012.03.007] [PMID: 22465455]

[160]
Van den Bergh, B.R.H.; Van Calster, B.; Smits, T.; Van Huffel, S.; Lagae, L. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology,  2008, 33(3), 536-545.
 [http://dx.doi.org/10.1038/sj.npp.1301450] [PMID: 17507916]

[161]
Begum, N.; Mandhare, A.; Tryphena, K.P.; Srivastava, S.; Shaikh, M.F.; Singh, S.B.; Khatri, D.K. Epigenetics in depression and gut-brain axis: A molecular crosstalk. Front. Aging Neurosci.,  2022, 14, 1048333.
 [http://dx.doi.org/10.3389/fnagi.2022.1048333] [PMID: 36583185]

[162]
Li, D.; Li, Y.; Yang, S.; Lu, J.; Jin, X.; Wu, M. Diet-gut microbiota-epigenetics in metabolic diseases: From mechanisms to therapeutics. Biomed. Pharmacother.,  2022, 153, 113290.
 [http://dx.doi.org/10.1016/j.biopha.2022.113290] [PMID: 35724509]

[163]
O’Riordan, K.J.; Collins, M.K.; Moloney, G.M.; Knox, E.G.; Aburto, M.R.; Fülling, C.; Morley, S.J.; Clarke, G.; Schellekens, H.; Cryan, J.F. Short chain fatty acids: Microbial metabolites for gut-brain axis signalling. Mol. Cell. Endocrinol.,  2022, 546, 111572.
 [http://dx.doi.org/10.1016/j.mce.2022.111572] [PMID: 35066114]

[164]
Walker, R.W.; Clemente, J.C.; Peter, I.; Loos, R.J.F. The prenatal gut microbiome: Are we colonized with bacteria in utero? Pediatr. Obes.,  2017, 2017(12 (S1)), 3-17.
 [http://dx.doi.org/10.1111/ijpo.12217]

[165]
Nuriel-Ohayon, M.; Neuman, H.; Koren, O. Microbial changes during pregnancy, birth, and infancy. Front. Microbiol.,  2016, 7, 1031.
 [http://dx.doi.org/10.3389/fmicb.2016.01031] [PMID: 27471494]

[166]
Aagaard, K.; Ma, J.; Antony, K.M.; Ganu, R.; Petrosino, J.; Versalovic, J. The placenta harbors a unique microbiome. Sci. Transl. Med.,  2014, 6(237), 237ra65.
 [http://dx.doi.org/10.1126/scitranslmed.3008599] [PMID: 24848255]

[167]
Miko, E.; Csaszar, A.; Bodis, J.; Kovacs, K. The maternal-fetal gut microbiota axis: Physiological changes, dietary influence, and modulation possibilities. Life,  2022, 12(3), 424.
 [http://dx.doi.org/10.3390/life12030424] [PMID: 35330175]
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DOI https://dx.doi.org/10.2174/1570159X22666240507095700	Print ISSN 1570-159X
Publisher Name Bentham Science Publisher	Online ISSN 1875-6190
Current Neuropharmacology

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