Application of psychobiotics in clinical treatment of mental disorders: Neurodevelopmental disorders, neurodegenerative diseases, depression and anxiety

Abstract

Psychobiotics are a distinct category of probiotics known for their beneficial effects on human health, particularly in influencing mental well-being. Typical psychobiotics include genera such as Lactobacillus, Streptococcus, and Bifidobacterium. The gut microbiota influences bidirectional communication between the brain and the gastrointestinal (GI) system. Neurons in the enteric nervous system directly interact with neurotransmitters, short-chain fatty acids (SCFAs), gut hormones, and anti-inflammatory cytokines produced by the gut microbiota, thereby affecting signal transmission in the central nervous system. Unlike traditional probiotics, psychobiotics have the capacity to generate or stimulate the host to produce neurotransmitters, SCFAs, gut hormones, and anti-inflammatory cytokines. It is precisely this potential that has led to the widespread use of psychobiotics over the past decade to improve and treat mental disorders. This article briefly reviews the clinical applications of psychobiotics in improving and treating conditions such as neurodevelopmental disorders, neurodegenerative diseases, depression and anxiety. It is proposed that the novel therapeutic approach of using Bacillus licheniformis as an adjuvant treatment for patients with depression shows a certain degree of feasibility. Finally, this review suggests that the current evidence regarding the improvement and treatment of mental and neurological disorders with psychobiotics is still limited. Further in-depth research is needed to clarify their effectiveness and mechanisms of action in the clinical management of various mental disorders.

Keywords

depression / gut microbiota / mental disorders / probiotics / psychobiotics

References

[1] Evaluation, I.O.H.M. Global health data exchange (GHDx). 2021.

[2] Evidence as a catalyst for policy and societal change: towards more equitable, resilient and sustainable global health. World Health Organization 2022.

[3] H.Herrman, V.Patel, C.Kieling, M. Berk, C.Buchweitz, P.Cuijpers, T. A.Furukawa, R. C.Kessler, B. A.Kohrt, M.Maj, P.McGorry, C. F. Reynolds, III, M. M.Weissman, D.Chibanda, C.Dowrick, L. M.Howard, C. W.Hoven, M.Knapp, H. S.Mayberg, B. W. J. H.Penninx, S.Xiao, M.Trivedi, R.Uher, L.Vijayakumar, M.Wolpert, Lancet 2022, 399, 957.

[4] R.Atun, Lancet 2015, 386, 721.

[5] J.Lu, X.Xu, Y.Huang, T. Li, C.Ma, G.Xu, H.Yin, X.Xu, Y.Ma, L.Wang, Z. Huang, Y.Yan, B.Wang, S.Xiao, L.Zhou, L. Li, Y.Zhang, H.Chen, T.Zhang, J.Yan, H. Ding, Y.Yu, C.Kou, Z.Shen, L.Jiang, Z. Wang, X.Sun, Y.Xu, W.Guo, L.Jiang, S. Li, W.Pan, Y.Wu, G.Li, F.Jia, J. Shi, Z.Shen, N.Zhang, Lancet Psychiatry 2021, 8, 981.

[6] E. A.Grice, J. A.Segre, Annu. Rev. Genom. Hum. Genet. 2012, 13, 151.

[7] S.Crompton, Sci. Focus 2019.

[8] K.Rea, T. G.Dinan, J. F.Cryan, Neurobiol. Stress 2016, 4, 23.

[9] X.Kong, J.Liu, J.Li, K.Kwong, M.Koh, P. Sukijthamapan, J. J.Guo, Z. J.Sun, Y. Song, Pilot Feasibility Stud. 2020, 6, 20.

[10] B.Lu, L.Lin, X.Su, J. Affect. Disord. 2024, 354, 553.

[11] O.Gawlik-Kotelnicka, M. Polguj, D.Strzelecki, Psychiatr. Pol. 2018, 52, 1023.

[12] C.Long-Smith, K. J.O’Riordan, G.Clarke, C.Stanton, T. G.Dinan, J. F.Cryan, Annu. Rev. Pharmacol. Toxicol. 2020, 60, 477.

[13] S.Qu, Z.Yu, Y.Zhou, S. Wang, M.Jia, T.Chen, X.Zhang, Microbiol. Res. 2024, 287, 127858.

[14] E.Aizawa, H.Tsuji, T.Asahara, T. Takahashi, T.Teraishi, S.Yoshida, M.Ota, N.Koga, K. Hattori, H.Kunugi, J. Affect. Disord. 2016, 202, 254.

[15] R.Huang, K.Wang, J.Hu, Nutrients 2016, 8, 483.

[16] C. J. KWallace, R.Milev, Ann. Gen. Psychiatry 2017, 16, 14.

[17] N. M.Vogt, R. L.Kerby, K. ADill-McFarland, S. J.Harding, A. P.Merluzzi, S. C.Johnson, C. M.Carlsson, S.Asthana, H.Zetterberg, K.Blennow, B. B.Bendlin, F. E.Rey, Sci. Rep. 2017, 7, 13537.

[18] A.Keshavarzian, S. J.Green, P. A.Engen, R. M. Voigt, A.Naqib, C. B.Forsyth, E.Mutlu, K. M.Shannon, Mov. Disord. 2015, 30, 1351.

[19] D.Kang, J. G.Park, Z. E.Ilhan, G. Wallstrom, J.LaBaer, J. B.Adams, R.Krajmalnik-Brown, PLoS One 2013, 8, e68322.

[20] M.Sucksdorff, L.Lehtonen, R.Chudal, A.Suominen, P.Joelsson, M.Gissler, A.Sourander, Pediatrics 2015, 136, e599.

[21] M. C.Cenit, I. C.Nuevo, P.Codoñer-Franch, T. G.Dinan, Y.Sanz, Eur. Child Adolesc. Psychiatry 2017, 26, 1081.

[22] T. G.Dinan, C.Stanton, J. F.Cryan, Biol. Psychiatry 2013, 74, 720.

[23] A.Bambury, K.Sandhu, J. F.Cryan, T. G.Dinan, Br. J. Pharmacol. 2018, 175, 4430.

[24] J. R.Kelly, A. P.Allen, A.Temko, W. Hutch, P. J.Kennedy, N.Farid, E.Murphy, G.Boylan, J.Bienenstock, J. F.Cryan, G.Clarke, T. G. Dinan, Brain Behav. Immun. 2017, 61, 50.

[25] R.Sharma, D.Gupta, R.Mehrotra, P. Mago, Curr. Microbiol. 2021, 78, 449.

[26] J.Żakowicz, A. Bramorska, W.Zarzycka, A.Kovbasiuk, K.Kuć, A.Brzezicka, Kopernika 2020, 69, 45.

[27] K.Skowron, A.Budzyńska, N.Wiktorczyk-Kapischke, K.Chomacka, K.Grudlewska-Buda, M.Wilk, E.Wałecka-Zacharska, M.Andrzejewska, E.Gospodarek-Komkowska, Int. J. Mol. Sci. 2022, 23, 7820.

[28] A. M.Mincic, M.Antal, L.Filip, D. Miere, Clin. Nutr. 2024, 43, 1832.

[29] A.Mehra, G.Arora, G.Sahni, M. Kaur, H.Singh, B.Singh, S.Kaur, J. Tradit. Complement. Med. 2023, 13, 135.

[30] W. M.Wierzchanowska, T. Iwanicki, Kosmos 2020, 69, 301.

[31] C. P.Johnson, S. M.Myers, Pediatrics 2007, 120, 1183.

[32] Y. S.Kim, B. L.Leventhal, Y. J.Koh, E.Fombonne, E.Laska, E. C.Lim, K. A. Cheon, S. J.Kim, H.Lee, D. H.Song, R. R.Grinker, Am. J. Psychiatry 2011, 168, 904.

[33] B. L.Teng, V. D.Nikolova, N. V.Riddick, K. L.Agster, J. J.Crowley, L. K.Baker, B. H.Koller, C. A.Pedersen, M. B.Jarstfer, S. S.Moy, Neuropharmacology 2016, 105, 61.

[34] S.Liu, E.Li, Z.Sun, D. Fu, G.Duan, M.Jiang, Y.Yu, L.Mei, P. Yang, Y.Tang, P.Zheng, Sci. Rep. 2019, 9, 287.

[35] J.Pulikkan, A.Maji, D. B.Dhakan, R. Saxena, B.Mohan, M. M.Anto, N.Agarwal, T.Grace, V. K.Sharma, Microb. Ecol. 2018, 76, 1102.

[36] D.Kang, Z. E.Ilhan, N. G.Isern, D. W. Hoyt, D. P.Howsmon, M.Shaffer, C. A.Lozupone, J.Hahn, J. B.Adams, R.Krajmalnik-Brown, Anaerobe 2018, 49, 121.

[37] L. E.Arnold, https://clinicaltrials.gov/ct2/show/NCT02903030 (accessed:5 March 2018).

[38] E.Santocchi, L.Guiducci, F.Fulceri, L.Billeci, E.Buzzigoli, F.Apicella, S.Calderoni, E.Grossi, M. A.Morales, F.Muratori, BMC Psychiatry 2016, 16, 183.

[39] S. D.Simmons, C.Brugaletta, A. V.Emmanuel, Res. Autism Spectr. Disord. 2024, 114, 102406.

[40] S. Y.Shaaban, Y. G.El Gendy, N. S.Mehanna, W. MEl-Senousy, H. S. A. El-Feki, K.Saad, O. MEl-Asheer, Nutr. Neurosci. 2018, 21, 676

[41] J.Marc Rhoads, Combination Probiotic: BB-12 With LGG (Different Doses) in Treating Children With Autism Spectrum Disorder. https://ClinicalTrials.gov/show/NCT03514784

[42] RCT of Autism spectrum disorder and probiotics. (UMIN000033113). 2018.

[43] L.Zhang, Y.Xu, H.Li, B.Li, G.Duan, C. Zhu, PLoS One 2022, 17, e0263109.

[44] Y.Wang, J. J.Yang, D. M.Zhao, B. Chen, G. Q.Zhang, S.Chen, R. F.Cao, H.Yu, C. Y.Zhao, L.Zhao, Y. S. Ge, Y.Liu, L. H.Zhang, W.Hu, L.Zhang, Z. T. Gai, Pharmacol. Res. 2020, 157, 104784.

[45] E.Santocchi, L.Guiducci, M.Prosperi, S.Calderoni, M.Gaggini, F.Apicella, R.Tancredi, L.Billeci, P.Mastromarino, E.Grossi, A.Gastaldelli, M. A.Morales, F.Muratori, Front. Psychiatry 2020, 11, 550593.

[46] C.Guidetti, E.Salvini, M.Viri, F.Deidda, A.Amoruso, A.Visciglia, L.Drago, M.Calgaro, N.Vitulo, M.Pane, A. C.Caucino, J. Clin. Med. 2022, 11, 5263.

[47] S. E.Erdman, T.Poutahidis, Int. Rev. Neurobiol. 2016, 131, 91.

[48] Y. W.Liu, W. H.Liu, C. C.Wu, Y. C. Juan, Y. C.Wu, H. P.Tsai, S.Wang, Y. C.Tsai, Brain Res. 2016, 1631, 1.

[49] Y.Liu, M. T.Liong, Y. C. E.Chung, H. Y.Huang, W. S.Peng, Y. F.Cheng, Y. S. Lin, Y. Y.Wu, Y. C.Tsai, Nutrients 2019, 11, 820.

[50] W.Liu, H. L.Chuang, Y. T.Huang, C. C.Wu, G. T.Chou, S.Wang, Y. C. Tsai, Behav. Brain Res. 2016, 298, 202.

[51] R. L.Pobbe, B. L.Pearson, E. B.Defensor, V. J.Bolivar, W. S.Young, III, H. J.Lee, D. C.Blanchard, R. J.Blanchard, Horm. Behav. 2012, 61, 436.

[52] X.-J.Kong, J.Liu, K.Liu, M. Koh, H.Sherman, S.Liu, R.Tian, P.Sukijthamapan, J.Wang, M.Fong, L.Xu, C.Clairmont, M. S.Jeong, A.Li, M.Lopes, V.Hagan, T. Dutton, S. T. P.Chan, H.Lee, A.Kendall, K.Kwong, Y.Song, Nutrients 2021, 13, 1552.

[53] M. R.Sanctuary, J. N.Kain, S. Y.Chen, K. Kalanetra, D. G.Lemay, D. R.Rose, H. T.Yang, D. J.Tancredi, J. B.German, C. M.Slupsky, P.Ashwood, D. A.Mills, J. T.Smilowitz, K.Angkustsiri, PLoS One 2019, 14, e0210064.

[54] D.Kang, J. B.Adams, D. M.Coleman, E. L.Pollard, J.Maldonado, S.McDonough-Means, J. G.Caporaso, R.Krajmalnik-Brown, Sci. Rep. 2019, 9, 5821.

[55] D.Kang, J. B.Adams, A. C.Gregory, T.Borody, L.Chittick, A.Fasano, A.Khoruts, E.Geis, J.Maldonado, S. McDonough-Means, E. L.Pollard, S.Roux, M. J.Sadowsky, K. S.Lipson, M. B.Sullivan, J. G.Caporaso, R.Krajmalnik-Brown, Microbiome 2017, 5, 1.

[56] A.Tomova, V.Husarova, S.Lakatosova, J.Bakos, B.Vlkova, K.Babinska, D.Ostatnikova, Physiol. Behav. 2015, 138, 179.

[57] M.Roy, W.Dillo, H. M.Emrich, M. D. Ohlmeier, Dtsch. Arztebl. Int. 2009, 106, 59.

[58] M.Rajaprakash, M. L.Leppert, Pediatr. Rev. 2022, 43, 135.

[59] H.Huang, H. M.Xu, Y. D.Liu, D. W. Shou, H. T.Chen, Y. Q.Nie, Y. Q.Li, Y. J.Zhou, Front. Psychiatry 2022, 13, 695481.

[60] R. W.Lee, M. J.Corley, A.Pang, G.Arakaki, L.Abbott, M.Nishimoto, R.Miyamoto, E.Lee, S.Yamamoto, A. K. Maunakea, A.Lum-Jones, M.Wong, Physiol. Behav. 2018, 188, 205.

[61] G.Polanczyk, M. S.de Lima, B. L.Horta, J.Biederman, L. A.Rohde, Am. J. Psychiatry 2007, 164, 942.

[62] V.Simon, P.Czobor, S.Bálint, Á.Mészáros, I.Bitter, Br. J. Psychiatry 2009, 194, 204.

[63] A.Pärtty, M.Kalliomäki, P.Wacklin, S.Salminen, E.Isolauri, Pediatr. Res. 2015, 77, 823.

[64] J. J.Rucklidge, Adv. Mind Body Med. 2013, 27, 14.

[65] H. G.Kumperscak, A. Gricar, I.Ülen, D.Micetic-Turk, Front. Psychiatry 2020, 11, 181.

[66] R. M.Elhossiny, H. H.Elshahawy, H. M.Mohamed, R. I.Abdelmageed, BMC Psychiatry 2023, 23, 823.

[67] Z.Sepehrmanesh, A.Shahzeidi, M.Mansournia, A.Ghaderi, Int. Arch. Health Sci. 2021, 8, 90.

[68] M.Ghanaatgar, S.Taherzadeh, S.Ariyanfar, S.Razeghi Jahromi, F. Martami, J.Mahmoudi Gharaei, A.Teimourpour, Z.Shahrivar, Nutr. Food Sci. 2022, 53, 19.

[69] L.Wang, C. S.Tsai, W. J.Chou, H. C. Kuo, Y. H.Huang, S. Y.Lee, H. Y.Dai, C. Y.Yang, Y. T. Yeh, Nutrients 2024, 16, 226.

[70] D.Seo, D. M.Holtzman, Exp. Mol. Med. 2024, 56, 86.

[71] KumarA., J.Sidhu, A.Goyal, J. W. Tsao, C.Doerr, Alzheimer disease (nursing), StatPearls Publishing, Treasure Island (FL) 2021.

[72] J. A.Bravo, P.Forsythe, M. V.Chew, E.Escaravage, H. M.Savignac, T. G.Dinan, J.Bienenstock, J. F.Cryan, Proc. Natl. Acad. Sci. USA 2011, 108, 16050.

[73] L.Cheng, Y. W.Liu, C. C.Wu, S. Wang, Y. C.Tsai, J. Food Drug Anal. 2019, 27, 632.

[74] F.Leblhuber, K.Steiner, B.Schuetz, D.Fuchs, J. M.Gostner, Curr. Alzheimer Res. 2018, 15, 1106.

[75] E.Akbari, Z.Asemi, R.Daneshvar Kakhaki, F.Bahmani, E.Kouchaki, O. R.Tamtaji, G. A.Hamidi, M.Salami, Front. Aging Neurosci. 2016, 8, 256.

[76] Y.Kobayashi, T.Kinoshita, A.Matsumoto, K.Yoshino, I.Saito, J.-Z.Xiao, J. Prev. Alzheimer’s Dis. 2019, 6, 70.

[77] Y.Kobayashi, T.Kuhara, M.Oki, J. Z.Xiao, Benef. Microbes 2019, 10, 511.

[78] A.Agahi, G. A.Hamidi, R.Daneshvar, M.Hamdieh, M.Soheili, A.Alinaghipour, S. M.Esmaeili Taba, M. Salami, Front. Neurol. 2018, 9, 662.

[79] B. R.Bloem, M. S.Okun, C.Klein, Lancet 2021, 397, 2284.

[80] W.Poewe, K.Seppi, C. M.Tanner, G. M. Halliday, P.Brundin, J.Volkmann, A. E.Schrag, A. E.Lang, Nat. Rev. Dis. Primers 2017, 3, 17013.

[81] L.Hirsch, N.Jette, A.Frolkis, T. Steeves, T.Pringsheim, Neuroepidemiology 2016, 46, 292.

[82] A. J.Akki, S. A.Patil, S.Hungund, R. Sahana, M. M.Patil, R. V.Kulkarni, K.Raghava Reddy, F.Zameer, A. V.Raghu, Int. Immunopharm. 2024, 139, 112758.

[83] R.Roy, D.Kumar, P.Bhattacharya, A.Borah, Neurochem. Int. 2024, 178, 105803.

[84] O. R.Tamtaji, M.Taghizadeh, R.Daneshvar Kakhaki, E.Kouchaki, F.Bahmani, S.Borzabadi, S.Oryan, A.Mafi, Z.Asemi, Clin. Nutr. 2019, 38, 1031.

[85] S.Borzabadi, S.Oryan, A.Eidi, Z. Asemi, Arch. Iran. Med. 2018, 21, 289.

[86] A.Ibrahim, R. A. R. Ali, M. R. A.Manaf, N.Ahmad, F. W.Tajurruddin, W. Z.Qin, S. H. M.Desa, N. M.Ibrahim, PLoS One 2020, 15, e0244680.

[87] A. H.Tan, S. Y.Lim, K. K.Chong, M. A. A. AManap, J. W.Hor, J. L.Lim, S. C. Low, C. W.Chong, S.Mahadeva, A. E.Lang, Neurology 2021, 96, e772.

[88] M.Barichella, C.Pacchetti, C.Bolliri, E.Cassani, L.Iorio, C.Pusani, G. Pinelli, G.Privitera, I.Cesari, S. A.Faierman, R.Caccialanza, G.Pezzoli, E.Cereda, Neurology 2016, 87, 1274.

[89] D.Georgescu, O.Ancusa, L.Georgescu, I.Ionita, D.Reisz, Clin. Interv. Aging 2016, 11, 1601.

[90] E.Cassani, G.Privitera, G.Pezzoli, C.Pusani, C.Madio, L.Iorio, M. Barichella, Minerva Gastroenterol. Dietol. 2011, 57, 117.

[91] J. W.Tiller, Med. J. Aust. 2012, 1, 28.

[92] H.Taipale, J.Reutfors, A.Tanskanen, L.Brandt, J.Tiihonen, A.DiBernardo, E.Mittendorfer-Rutz, P. Brenner, BMC Psychiatry 2020, 20, 232.

[93] C.Wang, R.Pan, X.Wan, Y. Tan, L.Xu, R. C.Ho, Int. J. Environ. Res. Publ. Health 2020, 17, 1729.

[94] L.Cui, S.Li, S.Wang, X. Wu, Y.Liu, W.Yu, Y.Wang, Y.Tang, M. Xia, B.Li, Signal Transduct. Targeted Ther. 2024, 9, 30.

[95] L.Liu, H.Wang, X.Chen, Y. Zhang, H.Zhang, P.Xie, eBioMedicine 2023, 90, 104527.

[96] V. M.Merkulov, T. I.Merkulova, N. P.Bondar, Biochem. Mosc. 2017, 82, 351.

[97] A.Ait-Belgnaoui, H. Durand, C.Cartier, G.Chaumaz, H.Eutamene, L.Ferrier, E.Houdeau, J.Fioramonti, L.Bueno, V.Theodorou, Psychoneuroendocrinology 2012, 37, 1885.

[98] S.Davari, S. A.Talaei, H.Alaei, M.salami, Neuroscience 2013, 240, 287.

[99] J.Arseneault-Bréard, I.Rondeau, K.Gilbert, S. A.Girard, T. A.Tompkins, R.Godbout, G.Rousseau, Br. J. Nutr. 2012, 107, 1793.

[100] E.Merkouris, T.Mavroudi, D.Miliotas, D.Tsiptsios, A.Serdari, F.Christidi, T. K.Doskas, C.Mueller, K.Tsamakis, Microorganisms 2024, 12, 411.

[101] F.Guida, F.Turco, M.Iannotta, D. De Gregorio, I.Palumbo, G.Sarnelli, A.Furiano, F.Napolitano, S.Boccella, L.Luongo, M.Mazzitelli, A.Usiello, F.De Filippis, F.Iannotti, F.Piscitelli, D.Ercolini, V.de Novellis, V.Di Marzo, R.Cuomo, S.Maione, Brain Behav. Immun. 2018, 67, 230.

[102] A. V.Rao, A. C.Bested, T. M.Beaulne, M. A.Katzman, C.Iorio, J. M.Berardi, A. C.Logan, Gut Pathog. 2009, 1, 6.

[103] C.Yang, Y.Fujita, Q.Ren, M.Ma, C.Dong, K.Hashimoto, Sci. Rep. 2017, 7, 45942.

[104] R. C.Robertson, C.Seira Oriach, K.Murphy, G. M.Moloney, J. F.Cryan, T. G.Dinan, R. Paul Ross, C.Stanton, Brain Behav. Immun. 2017, 59, 21.

[105] Z.Hao, W.Wang, R.Guo, H. Liu, Psychoneuroendocrinology 2019, 104, 132.

[106] B.Chahwan, S.Kwan, A.Isik, S. van Hemert, C.Burke, L.Roberts, J. Affect. Disord. 2019, 253, 317.

[107] E. Z.Reininghaus, M. Platzer, A.Kohlhammer-Dohr, C.Hamm, S.Mörkl, S. A.Bengesser, F. T.Fellendorf, T. Lahousen-Luxenberger, B.Leitner-Afschar, H.Schöggl, D.Amberger-Otti, W. Wurm, R.Queissner, A.Birner, V. S.Falzberger, A.Painold, W.Fitz, M.Brunnmayr, A.Rieger, J.Wagner-Skacel, A. Maget, R.Unterweger, K.Schwalsberger, B. Reininghaus, M.Lenger, T. F. S.Bastiaanssen, N. Dalkner, Nutrients 2020, 12, 3422.

[108] A.Kazemi, A. A.Noorbala, K.Azam, M. H.Eskandari, K.Djafarian, Clin. Nutr. 2019, 38, 522.

[109] H.Karakula-Juchnowicz, J. Rog, D.Juchnowicz, I.Łoniewski, K. Skonieczna-Żydecka, P.Krukow, M.Futyma-Jedrzejewska, M.Kaczmarczyk, Nutr. J. 2019, 18, 1.

[110] R. F.Slykerman, F.Hood, K.Wickens, J. Thompson, C.Barthow, R.Murphy, J.Kang, J.Rowden, P. Stone, J.Crane, T.Stanley, P.Abels, G.Purdie, R. Maude, E.Mitchell, eBio-Medicine 2017, 24, 159.

[111] A. P.Allen, W.Hutch, Y. E.Borre, P. J. Kennedy, A.Temko, G.Boylan, E.Murphy, J. F.Cryan, T. G.Dinan, G.Clarke, Transl. Psychiatry 2016, 6, e939.

[112] G.Akkasheh, Z.Kashani-Poor, M.Tajabadi-Ebrahimi, P.Jafari, H.Akbari, M.Taghizadeh, M. R.Memarzadeh, Z. Asemi, A.Esmaillzadeh, Nutrition 2016, 32, 315.

[113] M.Messaoudi, R.Lalonde, N.Violle, H.Javelot, D.Desor, A.Nejdi, J. F. Bisson, C.Rougeot, M.Pichelin, M.Cazaubiel, J. M.Cazaubiel, Br. J. Nutr. 2011, 105, 755.

[114] M.Messaoudi, N.Violle, J. F.Bisson, D.Desor, H.Javelot, C.Rougeot, Gut Microb. 2011, 2, 256.

[115] H.Chen, P. H.Kuo, C. Y.Hsu, Y. H. Chiu, Y. W.Liu, M. L.Lu, C. H.Chen, Nutrients 2021, 13, 3731.

[116] A.Marotta, E.Sarno, A.Del Casale, M.Pane, L.Mogna, A.Amoruso, G. E. Felis, M.Fiorio, Front. Psychiatry 2019, 10, 164.

[117] P.Tian, Y.Chen, H.Zhu, L. Wang, X.Qian, R.Zou, J.Zhao, H.Zhang, L. Qian, Q.Wang, G.Wang, W.Chen, Brain Behav. Immun. 2022, 100, 233.

[118] R.Zhu, Y.Fang, H.Li, Y.Liu, J.Wei, S. Zhang, L.Wang, R.Fan, L.Wang, T.Chen, Front. Immunol. 2023, 14, 1158137.

[119] R. F.Slykerman, E.Li, E. A.Mitchell, PLoS One 2022, 17, e0267778.

[120] C. J.Wallace, J.Foster, C.Soares, R.Milev, Neuropsychobiology 2020, 79, 108.

[121] A.Bartos, J.Weinerova, S.Diondet, Front. Aging Neurosci. 2023, 15, 1163727.

[122] T.Wu, Chin. J. Microecol. 1990, 2, 1.

[123] P.Shariat, W. J.Mitchell, A.Boyd, F. G.Priest, Microbiology 1995, 141, 1117.

[124] P.Wang, Q.Wu, X.Jiang, Z. Wang, J.Tang, Y.Xu, Int. J. Food Microbiol. 2017, 250, 59.

[125] E. N.Salo, A.Novero, Trop. Life Sci. Res. 2020, 31, 57.

[126] H.Ramirez-Olea, B.Reyes-Ballesteros, R. AChavez-Santoscoy, Front. Microbiol. 2022, 13, 993451.

[127] F. C.Belton, G. M.Hills, J. F.Powell, Microbiology 1949, 3, 400.

[128] H. I.Haavik, Microbiology 1974, 84, 321.

[129] C.Meng, S.Feng, Z.Hao, C. Dong, H.Liu, Psychoneuroendocrinology 2022, 136, 105620.

[130] S.Feng, C.Meng, Z.Hao, H. Liu, Nutrients 2022, 14, 1642.

[131] S.Feng, C.Meng, Y.Liu, Y. Yi, A.Liang, Y.Zhang, Z.Hao, Appl. Microbiol. Biotechnol. 2023, 107, 4355.

RIGHTS & PERMISSIONS

2025 The Author(s). Interdisciplinary Medicine published by Wiley-VCH GmbH on behalf of Nanfang Hospital, Southern Medical University.