Effect of Probiotics and Prebiotics on Gut-Brain Axis

Yıl 2019, Cilt 17, Sayı 2, 269 - 280, 02.09.2019

Merve ÖZER Gonca ÖZYURT Şebnem TELLİOĞLU HARSA

https://doi.org/10.24323/akademik-gida.613637

Cited By: 3

Öz

People have been started to consume functional foods that promote health with changing nutritional dynamics all over the world. Psychological signs such as level of daily stress and emotional changes affect the microbiota negatively. Neuropsychiatric disorders cause irregular release of neurotransmitters like gamma-aminobutyric acid; therefore, functional food ingredients can be used as therapeutic agents. The purpose of this study is to review the positive impacts of prebiotics, and probiotics, and functional foods containing these ingredients on the gut-brain axis through the health of microbiota. The definition of probiotics and prebiotics and their neurotransmitters secreted, the effects on neuropsychological health, the role of intestinal metabolic disorders in the formation of neuropsychiatric diseases, the importance of gut-brain axis on this mechanism are presented in the light of scientific researches and current literature. In this study, the contribution of food biosciences into this interdisciplinary area is highlighted.

Anahtar Kelimeler

Psychobiotics, Functional foods, Nutrition, Neuropsychiatric disorders, Neurotransmitter

Probiyotik ve Prebiyotiklerin Bağırsak-Beyin Aksına Etkisi

Öz

Tüm dünyada değişen beslenme dinamikleri ile insanlar, sağlıklı yaşamı destekleyecek fonksiyonel besinler tüketmeye yönelmektedir. Günümüz yaşam koşullarında yaşanan stres düzeyi ve duygu değişimleri gibi psikolojik belirtilerin bağırsak mikrobiyotasını olumsuz yönde etkilemektedir. Bireylerde görülen nöropsikiyatrik bozukluklar, gama-amino bütirik asit vb. nörotransmitterlerin salınımındaki değişimlerde rol oynarken, fonksiyonel gıda bileşenleri terapötik ürün olarak bu nöropsikiyatrik bozuklar üzerinde etkili olabilmektedir. Derlemenin amacı, prebiyotik ve probiyotiklerin ve bunları içeren fonksiyonel gıdaların mikrobiyota sağlığı, dolayısıyla bağırsak-beyin aksı üzerindeki olumlu katkılarının incelenmesidir. Probiyotik ve prebiyotik tanımı, sentezledikleri nörotransmiterler, nöropsikolojik sağlık üzerindeki etkileri, bağırsaklardaki metabolik bozuklukların nöropsikiyatrik rahatsızlıkların meydana gelmesindeki rolü, bağırsak-beyin ekseninin bu mekanizmadaki önemi bilimsel araştırmalar ve güncel literatür ışığında sunulmaktadır, bu disiplinlerarası alanda gıda biyobilimlerinin katkısının ve öneminin altı çizilmektedir.

Anahtar Kelimeler

Psikobiyotik, Fonksiyonel Gıda, Beslenme, Nöropsikiyatrik bozukluklar, Nörotransmitter

Kaynakça

• [1] Kılıç, C. (2017). Ruhsal Hastalıklara Bağlı Hastalık Yükü. HÜTF Ulusal Hastalık Yükü Çalışması Sonuçları ve Çözüm Önerileri. Ruh Sağlığı ve Hastalıkları Anabilim Dalı, Nisan 18, 2017, Ankara, 3p.
• [2] Anderson, H.D., Pace, W.D., Libby, A.M., West, D.R., Valuck, R.J. (2012). Rates of 5 common antidepressant side effects among new adult and adolescent cases of depression: a retrospective US claims study. Clinical Therapeutics, 34(1), 113-123.
• [3] Foster, J.A., McVey, K.A. 2013. Gut-brain axis: how the microbiome influences anxiety and depression. Trends in Neurosciences, 36(5), 305-312.
• [4] Jiang, H., Ling, Z., Zhang, Y., Mao, H., Ma, Z., Yin, Y., Wang, W., Tang, W., Tan, Z., Shi, J., Li, L., Ruan, B. (2015). Altered fecal microbiota composition in patients with major depressive disorder. Brain, Behavior, and Immunity, 48, 186-194.
• [5] Kelly, J.R., Borre, Y., O' Brien, C., Patterson, E., El Aidy, S., Deane, J., Kennedy, P.J., Beers, S., Scott, K., Moloney, G., Hoban, A.E., Scott, L., Fitzgerald, P., Ross, P., Stanton, C., Clarke, G., Cryan, J.F. ve Dinan, T.G. (2016). Transferring the blues: Depression-associated gut microbiota induces neurobehavioural changes in the rat. Journal of Psychiatr Research, 82, 109-118.
• [6] Walker, E.A., Katon, W.J., Jemelka, R.P., Roy-Bryne, P.P. (1992). Comorbidity of gastrointestinal complaints, depression, and anxiety in the Epidemiologic Catchment Area (ECA) Study.The American Journal of Medicine, 92(1A), 26-30.
• [7] Mangiola, F., Ianiro, G, Franceschi, F.,Fagiuoli, S., Gasbarrini, G., Gasbarrini, A. (2016). Gut microbiota in autism and mood disorders. World Journal of Gastroenterology, 22(1), 361-368.
• [8] Petra, A.I., Panagiotidou, S., Hatziagelaki, E., Stewart, J.M., Conti, P., Theoharides, T.C. (2015). Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clinical Therapeutics, 37(5), 984-995.
• [9] Goodrich, J.K., Waters, J.L., Poole, A.C., Sutter, J.L., Koren, O., Bleckham, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J.T., Spector, T.D., Clark, A.G., Ley, R.E. (2014). Human genetics shape the gut microbiome. Cell, 159(4), 789-799.
• [10] Yatsunenko, T., Rey, F.E., Manary, M.J., Trehan, I., Dominguez-Bello, M.G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R.N., Anokhin, A.P., Heath, A.C., Warner, B., Reeder, J., Kuczynski, J., Caporaso, J.G., Lozupone, C.A., Lauber, C., Clemente, J.C., Kinghts, D., Knight, R., Gordon, J.I. (2012). Human gut microbiome viewed across age and geography. Nature, 486(7402), 222-227.
• [11] Markle, J.G., Frank, D.N., Mortin-Toth, S., Robertson, C.E., Feazel, L.M., Rolle-Kampczyk, U., von Bergen, M., McCoy, K.D., Macpherson, A.J., Danska, J.S. (2013). Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science, 339(6123), 1084-1088.
• [12] David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E., Ling, A.V., Devlin, A.S., Varma, Y., Fischbach, M.A., Biddinger, S.B., Dutton, R.J., Turnbaugh, P.J. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505(7484), 559-63.
• [13] O'Mahony, S.M., Marchesi, J.R., Scully, P., Codling, C., Ceolho, A.M., Quigley, E.M., Cryan, J.F., Dinan, T.G. (2009). Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biological Psychiarty, 65(3), 263-267.
• [14] Logan, A.C., Jacka, F.N. (2014). Nutritional psychiatry research: an emerging discipline and its intersection with global urbanization, environmental challenges and the evolutionary mismatch. Journal of Physiological Anthropology, 33(1), 22.
• [15] Sánchez-Villegas, A., Delgado-Rodríguez, M., Alonso, A., Schlatter, J., Lahortiga, F., Serra Majem, L., Martínez-González, M.A. (2009). Association of the Mediterranean dietary pattern with the incidence of depression: the Seguimiento Universidad de Navarra/University of Navarra follow-up (SUN) cohort. Archives of General Psychiatry, 66(10), 1090-1098.
• [16] Akbaraly, T.N., Brunner, E.J., Ferrie, J.E., Marmot, M.G., Kivimaki, M., Singh-Manoux, A. (2009). Dietary pattern and depressive symptoms in middle age. The British Journal of Psychiarty:The Journal of Mental Science, 195(5), 408-13.
• [17] Parvez, S., Malik, K.A., Ah Kang, S., Kim, H.Y. (2006). Probiotics and their fermented food products are beneficial for health. Journal of Applied Microbiology, 100(6), 1171-85..
• [18] Logan, A.C., Katzman, M. (2005). Major depressive disorder: probiotics may be an adjuvant therapy. Medical Hypotheses, 64(3), 533-538.
• [19] Burgain, J., Gaiani, C.,Linder, M., Scher, J. (2011). Encapsulation of probiotic living cells: From laboratory scale to industrial applications. Journal of Food Engineering, 104(4), 467-483.
• [20] Kopp-Hoolihan, L. (2001). Prophylactic and therapeutic uses of probiotics: a review. Journal of American Dietetic Association, 101(2), 229-238.
• [21] Şengün, İ.Y. (2011). Fermente gıdaların üretiminde kullanılan laktik asit bakterileri. Biological Diversity and Conservation, 4(1), 42-53.
• [22] Ranadheera, R.D., Baines, S.K., Adams, M.C. (2010). Importance of food in probiotic efficacy. Food Research International, 43(1), 1-7.
• [23] Douglas, C.L., Sanders, M.E. (2008). Probiotics and prebiotics in dietetics practice. Journal of The American Dietetic Association, 108(3), 510-521.
• [24] Lourens-Hattingh, A., Viljoen, B.C. (2001). Yogurt as probiotic carrier food. International Dairy Journal, 11(1-2), 1-17.
• [25] Akan, E., Kınık, Ö. (2015). Gıda üretimi ve depolanması sırasında probiyotiklerin canlılıklarını etkileyen faktörler. Celal Bayar Üniversitesi Fen Bilimleri Dergisi, 11(2), 155-166.
• [26] Anal, A.K., Singh, H. (2007). Recent advances in microencapsulation of probiotics for industrial applications and targeted delivery. Trends in Food Science & Technology, 18(5), 240-251.
• [27] Vinderola, C.G., Reinheimer, J.A. (2003). Lactic acid starter and probiotic bacteria: a comparative “in vitro” study of probiotic characteristics and biological barrier resistance. Food Research International, 36(9-10), 895-904.
• [28] FAO/WHO (2001). Health and nutritional properties of in food including powder milk with live lactic acid bacteria. Food and Agricultural Organization of the United Nations and World Health Organization Expert Consultation Report. Ocak, 1-4, 2001, Cordoba, Argentina, 30p.
• [29] Tripathi, M.K., Giri, S.K. (2014). Probiotic functional foods: Survival of probiotics during processing and storage. Journal of Functional Foods, 9, 225-241.
• [30] Çakır, İ. (2006). Mikroenkapsülasyon Tekniğinin Probiyotik Gıda Üretiminde Kullanımı. Türkiye 9. Gıda Kongresi, Mayıs 24-26, Bolu,Türkiye, 693-696p.
• [31] Kerry, R.G., Patra, J.K., Gouda, S.,Park, Y., Shin, H.S., Das, G. (2018). Benefaction of probiotics for human health: A review. Journal of Food and Drug Analysis, 26, 927-939.
• [32] Thomas, L.V. (2016). Probiotics– the journey continues. International Journal of Dairy Technology, 69(4), 469-480.
• [33] Ramchandran, L., Shah, N.P. (2010). Characterization of functional, biochemical and textural properties of synbiotic low-fat yogurts during refrigerated storage. LWT - Food Science and Technology, 43(5), 819-827.
• [34] Dülger, D., Sahan, Y. (2011). Diyet lifin özellikleri ve sağlık üzerindeki etkileri. Uludağ Üniversitesi Ziraat Fakültesi Dergisi, 25(2), 147-157.
• [35] Causey, J.L., Feirtag, J.M., Gallaher, D.D. Tungland, B.C., Slavin J.L. (2000). Effects of dietary inulin on serum lipids, blood glucose and the gastrointestinal environment in hypercholesterolemic men. Nutrition Research, 20(2), 191-201.
• [36] Roberfroid, M., Gibson, G.R., Hoyles, L., McCartney, A.L., Rastall, R., Rowland, I., Wolvers, D., Watzl, B., Szajewska, H., Stahl, B., Guarner, F., Respondek, F., Whelan, K., Coxam, V., Davicco, M.J., Leotoing, L., Wittrant, Y., Delzenne, N.M., Cani, P.D., Neyrinck, A.M., Meheust, A. (2010). Prebiotic effects: metabolic and health benefits. The British Journal of Nutrition, 104(52), 1-63.
• [37] Yoo, J.Y., Kim, S.S. (2016). Probiotics and prebiotics: present status and future perspectives on metabolic disorders. Nutrients, 8(3), 173.
• [38] García-Peris, P., Velasco, C., Lozano, M.A., Moreno, Y., Paron, L., de la Cuerda, C., Breton, I., Camblor, M., García-Hernández, J., Guarner, F., Hernández, M. (2012). Effect of a mixture of inulin and fructo-oligosaccharide on Lactobacillus and Bifidobacterium intestinal microbiota of patients receiving radiotherapy: a randomised, double-blind, placebo-controlled trial. Nutricion Hospitalaria, 27(6), 1908- 1915.
• [39] Gutierrez-Gomez, V., Fournier, C., Sauvage, C.,Vilain, A.C., Just, N., Wallaert, B. (2005). Réactions anaphylactiques induites par l'inulineAnaphylactic reactions to inulin. Revue Française d'Allergologie et d'Immunologie Clinique, 45(6), 493-495.
• [40] Sarkar, A., Lehto, S.M.,Harty, S.,Dinan, T.G.,Cryan, C.F., Burnet, P.W.J. (2016). Psychobiotics and the Manipulation of Bacteria–Gut–Brain Signals. Trends in Neurosciences, 39(11), 763-781.
• [41] Pinto-Sanchez, M.I., Hall, G.B., Ghajar, K., Nardelli, A., Bolino, C., Lau, J.T., Martin, F.P., Cominetti, O., Welsh, C., Rieder, A., Traynor, J., Gregory, C., De Palma, G., Pigrau, M., Ford, A.C., Marci, J., Berger, B., Bergonzelli, G., Surette, M.G., Collins, S.M., Moayyedi, P., Bercik, P. (2017). Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology, 153(2), 448-459.
• [42] Evrensel, A., Ceylan, M.E. (2015). Bağırsak beyin ekseni:Psikiyatrik bozukluklarda bağırsak mikrobiyotasının rolü. Psikiyatride Güncel Yaklaşımlar, 7(4), 461-472.
• [43] Lee, K.N., Lee, O.Y. (2014). Intestinal microbiota in pathophysiology and management of irritable bowel syndrome. World Journal of Gastroenterology, 20(27), 8886-8897.
• [44] Li, J., Butcher, J., Mack, D., Stintzi, A. (2015). Functional impacts of the intestinal microbiome in the pathogenesis of inflammatory bowel disease. Inflammatory Bowel Diseases, 21(1), 139-153.
• [45] Erbay-Gönenir, L., Seçkin, Y. (2016). Yeme bozuklukları. Güncel Gastroenteroloji, 20(4), 473-477.
• [46] Fooks, L.J., Gibson, G.R. (2002). In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS Microbiology Ecology, 39(1), 67-75.
• [47] Borre, Y.E., Moloney, R.D., Clarke, G., Dinan, T.G., Cryan, J.F. (2014). The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Advances in Experimental Medicine and Biology, 817, 373-403.
• [48] Hornig, M. (2013). The role of microbes and autoimmunity in the pathogenesis of neuropsychiatric illness. Current Opinion in Rheumatology, 25(4), 488-795.
• [49] Önal, D., Beyatlı, Y., Aslım, B. (2005). Probiyotik Bakterilerin Epitel Yüzeylere Yapışması. Orlab On-Line Mikrobiyoloji Dergisi, 3(9), 1-10.
• [50] Ouwehand, A.C., Tuomola, E.M., Tölkkö, S., Salminen, S. (2001). Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. International Journal of Food Microbiology, 64(1-2), 119-126.
• [51] Cani, P.D., Lecourt, E., Dewulf, E.M., Sohet, F.M., Pachikian, B.D., Naslain, D., De Backer, F., Neyrinck, A.M., Delzenne, N.M. (2009). Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. American Journal of Clinical Nutrition, 90(5), 1236-1243.
• [52] Mayer, E.A. (2011). Gut feelings: the emerging biology of gut-brain communication. Nature Reviews Neuroscience, 12(8), 453-466.
• [53] Yıldırım, A.E., Altun, R. (2014). Obezite ve Mikrobiyota. Güncel Gastroenteroloji, 18(1), 106-111.
• [54] Everard, A., Cani, P.D. (2013). Diabetes, obesity and gut microbiota. Best Practice & Research. Clinical Gastroenterology, 27(1), 73-83.
• [55] Cani, P., Everard, A., Duparc, T. (2013). Gut microbiota, enteroendocrine functions and metabolism. Current Opinion in Pharmacology, 13(6), 935-940.
• [56] Macfarlane, S., Macfarlane, G.T. (2003). Regulation of short-chain fatty acid production. The Proceedings of The Nutrition Society, 62(1), 62-72.
• [57] Wang, X., Wang, B.R., Zhang, X.J., Xu, Z., Ding, Y.Q., Ju, G. (2002). Evidences for vagus nerve in maintenance of immune balance and transmission of immune information from gut to brain in STM-infected rats. World Journal of Gastroenterology, 8(3), 540-545.
• [58] Borovikova, L.V., Ivanova, S., Zhang, M., Yang, H., Botchkina, G.I., Watkins, L.R., Wang, H., Abumrad, N., Eaton, J.W., Tracey, K.J. (2000). Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature, 405, 458-462.
• [59] Perez-Burgos, A., Wang, B., Mao, Y.K., Mistry, B., Mcvey Neufeld, K.A., Bienenstock, J., Kunze, W. (2013). Psychoactive bacteria Lactobacillus rhamnosus (JB-1) elicits rapid frequency facilitation in vagal afferents. American Journal of Physiology. Gastrointestinal and Liver Physiology, 304(2), G211-220.
• [60] Dinan, T.G., Cryan, J.F. (2012). Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology, 37(9), 1369-1378.
• [61] Miller, A.H., Maletic, V., Raison, C.L. (2009). Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biological Psychiatry, 65(9), 732-741.
• [62] Chiu, I.M., Heesters, B.A., Ghasemlou, N.,Von Hehn, C.A., Zhao, F., Tran, J., Wainger, B., Strominger, A., Muralidharan, S., Horswill, A.R., Bubeck Wardenburg, J., Hwang, S.W., Carroll, M.C., Woolf, C.J. (2013). Bacteria activate sensory neurons that modulate pain and inflammation. Nature, 501(7465), 52-57.
• [63] Tamam, L., Zeren, T. (2002). Depresyonda Serotonerjik Düzenekler. Klinik Pskiyatri Dergisi, 5(4),11-18.
• [64] Philips, J.G.P. (1910). The treatment of melancholia by the lactic acid bacillus. Journal of Mental Science, 56(234), 422-430.
• [65] Barrett, E., Ross, R.P., O'Toole, P.W., Fitzgerald, G.F., Stanton, C. (2012). γ-Aminobutyric acid production by culturable bacteria from the human intestine. Journal of Applied Microbiology, 113(2), 411-417.
• [66] Thomas, C.M., Hong, T., van Pijkeren, J.P., Hemarajata, P., Trinh, D.V., Hu, W., Britton, R.A., Kalkum, M., Versalovic, J. (2012). Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PloS one, 7(2), e31951.
• [67] Umbrello, G., Esposito, S. (2016). Microbiota and neurologic diseases: potential effects of probiotics. Journal of Translational Medicine, 14, 298.
• [68] Flint, H.J. (2012). The impact of nutrition on the human microbiome. Nutrition Reviews, 70(1), 10-13.
• [69] Carabotti, M., Scirocco, A., Maselli, M.A., Severi, C. (2015). The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Annals of Gastroenterology, 28(2), 203-209.
• [70] Martinez, I., Lattimer, J.M., Hubach, K.L., Case, J.A., Yang, J., Weber, C.G., Louk, J.A., Rose, D.J., Kyureghian, G., Peterson, D.A., Haub, M.D., Walter, J. (2013). Gut microbiome composition is linked to whole grain-induced immunological improvements. The ISME Journal, 7(2), 269-280.
• [71] Bäckhed, F., Manchester, J.K., Semenkovich, C.F., Gordon, I.J. (2007). Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. PNAS, 104(3), 979-984.
• [72] Tarr, A.J., Galley, J.D., Fisher, S.E., Chichlowski, M., Berg, B.M., Bailey, M.T. (2015). The prebiotics 3'Sialyllactose and 6'Sialyllactose diminish stressor-induced anxiety-like behavior and colonic microbiota alterations: Evidence for effects on the gut-brain axis. Brain, Behaviour, and Immunity, 50,166-77.
• [73] Burokas, A., Arboleya, S., Moloney, R.D., Peterson, V.L., Murphy, K.,Clarke, G., Stanton, C., Dinan, T.G., Cryan, J.F. (2017). Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biological Psychiatry, 82(7), 472-487.
• [74] Tillisch, K. (2014). The effects of gut microbiota on CNS function in humans. Gut Microbes, 5(3), 404-410.
• [75] Kunze, W.A., Mao, Y.K., Wang, B.,Huizinga, J.D., Ma, X., Forsythe, P., Bienenstock, J. (2009). Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. Journal of Cellular and Molecular Medicine, 13(8B), 2261-2270.
• [76] Davis, M., Walker, D.L., Miles, L., Grillon, C. (2010). Phasic vs sustained fear in rats and humans: Role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology, 35(1), 105-135.
• [77] Cowan, C.S.M., Hoban, A.E., Ventura-Silva, A.P., Dinan, T.G., Clarke, G., Cryan, J.F. (2018). Gutsy moves: The amygdala as a critical node in microbiota to brain signaling. BioEssays, 40(1), 1-12.
• [78] O'mahony, L., Mccarthy, J., Kelly, P.,Hurley, G., Luo, F., Chen, K., O'sullivan, G.C., Kıely, B.,Collins, K., Shanahan, F., Quigley, E.M.M. (2005). Lactobacillus and Bifidobacterium in irritable bowel syndrome:symptom responses and relationship to cytokine profiles. Gastroenterology, 128(3), 541-551.
• [79] Luo, J., Wang, T., Shan, L., Xu, H., Wei, L. ve Feng, J. (2014). Ingestion of Lactobacillus strain reduces anxiety and improves cognitive function in the hyperammonemia rat. Sciences CHINA Life Sciences, 57(3), 327–35.
• [80] Savignac, H.M., Couch, Y.,Stratford, M., Bannerman, D.M., Tzortzis, G., Anthony, D.C., Burnet, P.W.J. (2016). Prebiotic administration normalizes lipopolysaccharide (LPS)-induced anxiety and cortical 5-HT2A receptor and IL1-β levels in male mice. Brain, Behavior, and Immunity, 52, 120-131.
• [81] Williams, S., Chen, L., Savignac, H.M., Tzortzis, G., Anthony, D.C., Burnet P.W.J. (2016). Neonatal prebiotic (BGOS) supplementation increases the levels of synaptophysin, GluN2A-subunits and BDNF proteins in the adult rat hippocampus. Synapse, 70(3), 121-125.
• [82] Davari, S., Talaei, S.A., Alaei, H., Salamı, M. (2013). Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome-gut-brain axis. Neuroscience, 240, 287-296.
• [83] Mackos, A.R., Galley, J.D., Eubank, T.D., Easterling, R.S., Parry, N.M., Fox, J.G., Lyte, M., Bailey M.T. (2016). Social stress-enhanced severity of Citrobacter rodentium induced colitis is CCL2-dependent and attenuated by probiotic Lactobacillus reuteri. Mucosal Immunol, 9(2), 515-526.
• [84] Jia, S., Lu, Z., Gao, Z., An, J., Wu, X., Li, X., Dai, X., Zheng, Q., Sun, Y. (2016). Chitosan oligosaccharides alleviate cognitive deficits in an amyloid-β1-42-induced rat model of Alzheimer's disease. International Journal of Biological Macromolecules, 83, 416-25.
• [85] Bartosch, S., Woodmansey, E.J., Paterson, J.C., McMurdo, M.E., Macfarlane, G.T. (2005). Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis, and oligofructose in elderly persons, determined by real-time polymerase chain reaction and counting of viable bacteria. Clinical Infectious Diseases, 40(1), 28-37.
• [86] Kałużna-Czaplińska, J., Błaszczyk, S. (2012). The level of arabinitol in autistic children after probiotic therapy. Nutrition, 28(2), 124-126.
• [87] Yamamura, S., Morishima, H., Kumano-go, T., Suganuma, N., Matsumoto, H., Adachi, H., Sigedo, Y., Mikami, A., Kai, T., Masuyama, A., Takano, T., Sugita, Y., Takeda, M. (2009). The effect of Lactobacillus helveticus fermented milk on sleep and health perception in elderly subjects. European Journal of Clinical Nutrition, 63(1), 100-105.
• [88] Benton, D., Williams, C., Brown, A. (2007). Impact of consuming a milk drink containing a probiotic on mood and cognition. European Journal of Clinical Nutrition, 61(3), 355-361.
• [89] Haskey, N., Dahl, W.J. (2009). Synbiotic Therapy Improves Quality of Life and Reduces Symptoms in Pediatric Ulcerative Colitis. ICAN: Infant, Child, & Adolescent Nutrition, 1(2), 88-93.
• [90] Diop, L., Guillou, S., Durand, H. (2008). Probiotic food supplement reduces stress-induced gastrointestinal symptoms in volunteers: a double-blind, placebo-controlled, randomized trial. Nutrition Research, 28(1),1-5.
• [91] Kannampalli, P., Pochiraju, S., Chichlowski, M., Berg, B.M., Rudolph, C., Bruckert, M., Miranda, A., Sengupta, J.N. (2014). Probiotic Lactobacillus rhamnosus GG (LGG) and prebiotic prevent neonatal inflammation-induced visceral hypersensitivity in adult rats. Neurogastroenterol Motil, 26,1694-1704.
• [92] Zareie, M., Johnson‐Henry, K., Jury, J., Yang, P.C., Ngan, B.Y., McKay, D.M., Soderholm, J.D., Perdue, M.H., Sherman, P.M. (2006). Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut, 55(11), 1553-1560.
• [93] Gareau, M.G., Wine, E, Rodrigues, D.M., Cho, J.H., Whary, M.T., Philpott, D.J., Macqueen, G., Sherman, P.M. (2011). Bacterial infection causes stress-induced memory dysfunction in mice. Gut, 60(3), 307-317.
• [94] Rodrigues, D.M., Sousa, A.J., Johnson-Henry, K.C., Sherman, P.M., Gareau, M.G. (2012). Probiotics are effective for the prevention and treatment of Citrobacter rodentium-induced colitis in mice. The Journal of Infectious Diseases, 206(1), 99-109.
• [95] Pärtty, A., Kalliomäki, M., Wacklin, P., Salminen, S., Isolauri, E. (2015). A possible link between early probiotic intervention and the risk of neuropsychiatric disorders later in childhood: a randomized trial. Pediatric Research, 77(6), 823-828.
• [96] Kalliomäki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., Isolauri, E. (2001). Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet, 357(9262), 1076-1079.
• [97] Pessi, T., Sütas, Y., Hurme, M., Isolauri, E. (2000). Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clinical and Experimental Allergy, 30(12), 1804-1808.
• [98] Ait-Belgnaoui, A., Payard, I., Rolland, C., Harkat, C., Braniste, V., Théodorou, V., Tompkins, T.A. (2018). Bifidobacterium longum and Lactobacillus helveticus synergistically suppress stress-related visceral hypersensitivity through hypothalamic-pituitary-adrenal axis modulation. Journal of Neurogastroenterology and Motility, 24(1), 138-146.
• [99] Messaoudi, M., Lalonde, R.,Violle, N., Javelot, H., Desor, D., Nejdi, A., Bisson, J.F., Rougeot, C., Pichelin, M., Cazaubiel, M., Cazaubiel, J.M. (2011). Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. The British Journal of Nutrition, 105(5), 755-764.
• [100] Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain-Raspaud, S., Trotin, B., Naliboff, B., Mayer, E.A. (2013). Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology, 144(7), 1394-401.
• [101] Parracho, H., Gibson, G.R., Knott, F., Bosscher, D.,Kleerebezem, M., McCartney, A.L. (2010). A double-blind, placebo-controlled, crossover-designed probiotic feeding study in children diagnosed with autistic spectrum disorders. International Journal of Probiotics and Prebiotics, 5(2), 69-74.
• [102] Ohland, C.L., Kish, L., Bell, H., Thiesen, A., Hotte, N., Pankiv, E., Madsen, K.L. (2013). Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology, 38(9), 1738-47.
• [103] Liang, S., Wang, T., Hu, X., Luo, J., Li, W., Wu, X., Duan, Y., Jin, F. (2015). Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience, 310, 561-77.
• [104] Savignac, H.M., Tramullas, M., Kiely, B., Dinan, T.G., Cryan, J.F. (2015). Bifidobacteria modulate cognitive processes in an anxious mouse strain. Behavioural Brain Research, 287, 59-72.
• [105] Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J.A., Colzato, L.S. (2015). A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain, Behavior, and Immunity, 48, 258-264.
• [106] Desbonnet, L., Garrett, L., Clarke, G., Bienenstock, J., Dinan, T.G. (2008). The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. Journal of Psychiatric Research, 43(2), 164-174.
• [107] Bravo, J.A., Forsythe, P., Chew, M.V., Escaravage, E., Savignac, H.M., Dinan, T.G., Bienenstock, J., Cryan, J.F. (2011). Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of The National Academy of Sciences of the United States of America, 108(38), 6050-6055.
• [108] Gibson, E.L. (2006). Emotional influences on food choice: sensory, physiological and psychological pathways. Physiology & Behavior, 89(1), 53-61.
• [109] Greeno, G.G., Wing, R.R. (1994). Stress-induced eating. Psychological Bulletin, 115(3), 444-464.
• [110] Gonzalez-Bono, E., Rohleder, N.,Helhammer, D.H.,Salvador, A., Kirschbaum, C. (2002). Glucose but not protein or fat load amplifies the cortisol response to psychosocial stress. Hormones and Behavior, 41(3), 328-333.
• [111] Robbins, T.W., Fray, P.J. (1980). Stress-induced eating: Fact, fiction or misunderstanding? Appetite, 1(2), 103-133.
• [112] Benton, D., Donohoe, R.T. (1999). The effects of nutrients on mood. Public Health Nutrition, 2(3A), 403-409.