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The Impact of Probiotic Intervention during Developmental Cafeteria Diet Consumption on Social Behavior in Adulthood

Year 2024, , 67 - 74, 27.10.2024
https://doi.org/10.5281/zenodo.13996497

Abstract

This study examines the ramifications of consuming a cafeteria diet during developmental stages and subsequent probiotic therapy on social behavior in adult male Wistar rats. The investigation involves four experimental groups: a control group, a probiotics-only group, a cafeteria diet group, and a cafeteria diet with probiotics supplementation group. From day 21 (weaning) today 56 (the end of the developmental period), the treatments were administered. Social behavior was assessed using a three-chambered apparatus to evaluate the time spent interacting with unfamiliar rats. The results displayed that consuming a cafeteria diet during development significantly altered social behaviors, as demonstrated by decreased interaction times with unfamiliar animals, which suggests increased anxiety or diminished sociability. Conversely, the probiotics-supplemented group, which consumed the cafeteria diet, displayed social behaviors that were more comparable to the cafeteria diet group. These findings indicate that a poor diet during critical growth periods can have detrimental effects on social interaction and suggest that probiotic supplementation may be able to mitigate these negative consequences. The study emphasizes the importance of early dietary interventions and gut microbiota modulation in maintaining social health and reducing the long-term consequences of an unhealthy diet.

Ethical Statement

The study was approved by the Bingöl University Animal Experiments Local Ethics Committee (meeting date: 29.06.2021, approval number: 2021/03).

References

  • [1] Zenardini, B., Amir, M., Silveira, D., et al., “Cafeteria diet and obesity: Mutagenicity in Wistar rats and consequences on female offspring”, 2017, Vol. 7, Pages 16016–16019.
  • [2] Maeda Júnior, A.S., Constantin, J., Utsunomiya, K.S., et al., “Cafeteria diet feeding in young rats leads to hepatic steatosis and increased gluconeogenesis under fatty acids and glucagon influence”, Nutrients, Vol. 10, Pages 1–25, 2018.
  • [3] Heden, T.D., Morris, E.M., Kearney, M.L., et al., “Differential effects of low-fat and high-fat diets on fed-state hepatic triacylglycerol secretion, hepatic fatty acid profiles, and DGAT-1 protein expression in obese-prone Sprague-Dawley rats”, Applied Physiology, Nutrition, and Metabolism, Vol. 39, Pages 472–479, 2014.
  • [4] Buyukdere, Y., Gulec, A., Akyol, A., “Cafeteria diet increased adiposity in comparison to high fat diet in young male rats”, PeerJ, Vol. 7, Article e7068, 2019.
  • [5] Srinivasan, M., Katewa, S.D., Palaniyappan, A., et al., “Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood”, American Journal of Physiology - Endocrinology and Metabolism, Vol. 291, Pages 792–799, 2006.
  • [6] Moeckli, B., Delaune, V., Prados, J., et al., “Impact of maternal obesity on liver disease in the offspring: A comprehensive transcriptomic analysis and confirmation of results in a murine model”, Biomedicines, Vol. 10, Pages 1–19, 2022.
  • [7] Lambertz, J., Weiskirchen, S., Landert, S., et al., “Fructose: A dietary sugar in crosstalk with microbiota contributing to the development and progression of non-alcoholic liver disease”, Frontiers in Immunology, Vol. 8, Article 1153, 2017.
  • [8] Si, J., Vázquez-Castellanos, J.F., Gregory, A.C., et al., “Long-term life history predicts current gut microbiome in a population-based cohort study”, Nature Aging, Vol. 2, Pages 885–895, 2022.
  • [9] Ceylani, T., Teker, H.T., “The effect of young blood plasma administration on gut microbiota in middle-aged rats”, Archives of Microbiology, Vol. 204, Article 541, 2022.
  • [10] Teker, H.T., Ceylani, T., “Intermittent fasting supports the balance of the gut microbiota composition”, International Microbiology, Vol. 25, Pages 1–9, 2022.
  • [11] Ceylani, T., Allahverdi, H., Teker, H.T., “Role of age-related plasma in the diversity of gut bacteria”, Archives of Gerontology and Geriatrics, Vol. 111, Article 105003, 2023.
  • [12] Pan, Y., Zhang, X., “Diet and gut microbiome in fatty liver and its associated liver cancer”, Journal of Gastroenterology and Hepatology, Vol. 37, Pages 7–14, 2022.
  • [13] Ritze, Y., Bárdos, G., Claus, A., et al., “Lactobacillus rhamnosus GG protects against non-alcoholic fatty liver disease in mice”, PLoS ONE, Vol. 9, Article e86011, 2014.
  • [14] Le Barz, M., Anhê, F.F., Varin, T.V., et al., “Probiotics as complementary treatment for metabolic disorders”, Diabetes and Metabolism Journal, Vol. 39, Pages 291–303, 2015.
  • [15] Bourebaba, Y., Marycz, K., Mularczyk, M., et al., “Postbiotics as potential new therapeutic agents for metabolic disorders management”, Biomedicine & Pharmacotherapy, Vol. 153, Article 113138, 2022.
  • [16] Ceylani, T., “Effect of SCD probiotics supplemented with tauroursodeoxycholic acid (TUDCA) application on the aged rat gut microbiota composition”, Journal of Applied Microbiology, Vol. 135, Issue 1, Pages 92-102, 2023.
  • [17] Leclercq, S., Mian, F.M., Stanisz, A.M., et al., “Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior”, Nature Communications, Vol. 8, Article 15062, 2017.
  • [18] Cryan, J.F., Dinan, T.G., “Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour”, Nature Reviews Neuroscience, Vol. 13, Pages 701–712, 2012.
  • [19] Ceylani, T., Teker, H.T., “The combined use of SCD probiotics and tauroursodeoxycholic acid (TUDCA) is more effective in controlling anxiety-like behavior in aged rats”, Bitlis Eren Fen Bilimleri Dergisi, Vol. 12, Issue 1, Pages 242–246, 2023.
  • [20] Guo, M., Li, M., Zhang, C., et al., “Dietary administration of Bacillus subtilis enhances immune responses and disease resistance in chickens”, Frontiers in Microbiology, Vol. 11, Article 1768, 2020.
  • [21] Kalamara, M., Spacapan, M., Mandic-Mulec, I., et al., “Social behaviours by Bacillus subtilis: quorum sensing, kin discrimination and beyond”, Molecular Microbiology, Vol. 110, Pages 863–878, 2018.
  • [22] Ceylani, T., Jakubowska Doğru, E., Gurbanov, R., Teker, H.T., Gözen, A.G., “The effects of repeated antibiotic administration to juvenile BALB/c mice on the microbiota status and animal behavior at the adult age”, Heliyon, Vol. 4, Issue 6, Article e00644, 2018.
  • [23] Cryan, J.F., O’Mahony, S.M., “The microbiome-gut-brain axis: From bowel to behavior”, Neurogastroenterology & Motility, Vol. 23, Pages 187–192, 2011.
  • [24] Tian, P., O’Riordan, K.J., Lee, Y.K., et al., “Towards a psychobiotic therapy for depression: Bifidobacterium breve CCFM1025 reverses chronic stress-induced depressive symptoms and gut microbial abnormalities in mice”, Neurobiology of Stress, Vol. 12, Article 100216, 2020.
  • [25] Bravo, J.A., Forsythe, P., Chew, M.V., et al., “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, Vol. 108, Pages 16050–16055, 2011.
  • [26] Zhu, X., Sakamoto, S., Ishii, C., et al., “Dectin-1 signaling on colonic γδ T cells promotes psychosocial stress responses”, Nature Immunology, Vol. 24, Pages 625–636, 2023.
  • [27] Ait-Belgnaoui, A., Durand, H., Cartier, C., et al., “Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats”, Psychoneuroendocrinology, Vol. 37, Pages 1885–1895, 2012.
  • [28] Falkenstein, M., Simon, M.C., Mantri, A., et al., “Impact of the gut microbiome composition on social decision-making”, PNAS Nexus, Vol. 3, Issue 5, Article pgae166, 2024.
  • [29] Mazzone, L., et al., “Precision microbial intervention improves social behavior but not autism severity: A pilot double-blind randomized placebo-controlled trial”, Cell Host & Microbe, Vol. 32, Pages 106–116.e6, 2024.
  • [30] Weber, K.T., Varian, B.J., Erdman, S.E., “The gut microbiome and sociability”, Frontiers in Neuroscience, Vol. 18, Article 1372274, 2024.

Gelişim Döneminde Kafeterya Diyeti ile Probiyotik Kullanımının Ergin Bireyde Sosyal Davranış Üzerindeki Etkisi

Year 2024, , 67 - 74, 27.10.2024
https://doi.org/10.5281/zenodo.13996497

Abstract

Bu çalışma, gelişim dönemlerinde tüketilen bir cafeteria diyetinin ve ardından uygulanan probiyotik tedavisinin yetişkin erkek Wistar sıçanlarında sosyal davranışlar üzerindeki etkilerini incelemektedir. Araştırma, dört deneysel grup içermektedir: bir kontrol grubu, yalnızca probiyotik verilen bir grup, cafeteria diyeti grubu ve probiyotik ile takviye edilmiş cafeteria diyeti grubu. Tedaviler, gün 21'den (sütten kesilme) gün 56'ya (gelişim döneminin sonu) kadar uygulanmıştır. Sosyal davranışlar, deney hayvanlarının yabancı sıçanlarla etkileşimde bulundukları zamanı değerlendirmek için üç bölmeli bir düzenek kullanılarak değerlendirilmiştir. Sonuçlar, gelişim döneminde tüketilen cafeteria diyetinin sosyal davranışları önemli ölçüde değiştirdiğini ve yabancı hayvanlarla etkileşim sürelerinin azalmasıyla kendini gösterdiğini ortaya koymuştur; bu durum artan kaygı veya azalan sosyallik olarak yorumlanabilir. Buna karşın, probiyotik takviyesi yapılan ve cafeteria diyeti tüketen grup, sosyal davranışlarda cafeteria diyeti grubuna daha benzer davranışlar sergilemiştir. Bu bulgular, kritik büyüme dönemlerinde kötü bir diyetin sosyal etkileşimler üzerinde olumsuz etkileri olabileceğini ve probiyotik takviyesinin bu olumsuz sonuçları hafifletebileceğini göstermektedir. Çalışma, erken dönem diyet müdahalelerinin ve bağırsak mikrobiyotasının düzenlenmesinin sosyal sağlığı korumada ve sağlıksız bir diyetin uzun vadeli sonuçlarını azaltmada önemini vurgulamaktadır.

References

  • [1] Zenardini, B., Amir, M., Silveira, D., et al., “Cafeteria diet and obesity: Mutagenicity in Wistar rats and consequences on female offspring”, 2017, Vol. 7, Pages 16016–16019.
  • [2] Maeda Júnior, A.S., Constantin, J., Utsunomiya, K.S., et al., “Cafeteria diet feeding in young rats leads to hepatic steatosis and increased gluconeogenesis under fatty acids and glucagon influence”, Nutrients, Vol. 10, Pages 1–25, 2018.
  • [3] Heden, T.D., Morris, E.M., Kearney, M.L., et al., “Differential effects of low-fat and high-fat diets on fed-state hepatic triacylglycerol secretion, hepatic fatty acid profiles, and DGAT-1 protein expression in obese-prone Sprague-Dawley rats”, Applied Physiology, Nutrition, and Metabolism, Vol. 39, Pages 472–479, 2014.
  • [4] Buyukdere, Y., Gulec, A., Akyol, A., “Cafeteria diet increased adiposity in comparison to high fat diet in young male rats”, PeerJ, Vol. 7, Article e7068, 2019.
  • [5] Srinivasan, M., Katewa, S.D., Palaniyappan, A., et al., “Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood”, American Journal of Physiology - Endocrinology and Metabolism, Vol. 291, Pages 792–799, 2006.
  • [6] Moeckli, B., Delaune, V., Prados, J., et al., “Impact of maternal obesity on liver disease in the offspring: A comprehensive transcriptomic analysis and confirmation of results in a murine model”, Biomedicines, Vol. 10, Pages 1–19, 2022.
  • [7] Lambertz, J., Weiskirchen, S., Landert, S., et al., “Fructose: A dietary sugar in crosstalk with microbiota contributing to the development and progression of non-alcoholic liver disease”, Frontiers in Immunology, Vol. 8, Article 1153, 2017.
  • [8] Si, J., Vázquez-Castellanos, J.F., Gregory, A.C., et al., “Long-term life history predicts current gut microbiome in a population-based cohort study”, Nature Aging, Vol. 2, Pages 885–895, 2022.
  • [9] Ceylani, T., Teker, H.T., “The effect of young blood plasma administration on gut microbiota in middle-aged rats”, Archives of Microbiology, Vol. 204, Article 541, 2022.
  • [10] Teker, H.T., Ceylani, T., “Intermittent fasting supports the balance of the gut microbiota composition”, International Microbiology, Vol. 25, Pages 1–9, 2022.
  • [11] Ceylani, T., Allahverdi, H., Teker, H.T., “Role of age-related plasma in the diversity of gut bacteria”, Archives of Gerontology and Geriatrics, Vol. 111, Article 105003, 2023.
  • [12] Pan, Y., Zhang, X., “Diet and gut microbiome in fatty liver and its associated liver cancer”, Journal of Gastroenterology and Hepatology, Vol. 37, Pages 7–14, 2022.
  • [13] Ritze, Y., Bárdos, G., Claus, A., et al., “Lactobacillus rhamnosus GG protects against non-alcoholic fatty liver disease in mice”, PLoS ONE, Vol. 9, Article e86011, 2014.
  • [14] Le Barz, M., Anhê, F.F., Varin, T.V., et al., “Probiotics as complementary treatment for metabolic disorders”, Diabetes and Metabolism Journal, Vol. 39, Pages 291–303, 2015.
  • [15] Bourebaba, Y., Marycz, K., Mularczyk, M., et al., “Postbiotics as potential new therapeutic agents for metabolic disorders management”, Biomedicine & Pharmacotherapy, Vol. 153, Article 113138, 2022.
  • [16] Ceylani, T., “Effect of SCD probiotics supplemented with tauroursodeoxycholic acid (TUDCA) application on the aged rat gut microbiota composition”, Journal of Applied Microbiology, Vol. 135, Issue 1, Pages 92-102, 2023.
  • [17] Leclercq, S., Mian, F.M., Stanisz, A.M., et al., “Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior”, Nature Communications, Vol. 8, Article 15062, 2017.
  • [18] Cryan, J.F., Dinan, T.G., “Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour”, Nature Reviews Neuroscience, Vol. 13, Pages 701–712, 2012.
  • [19] Ceylani, T., Teker, H.T., “The combined use of SCD probiotics and tauroursodeoxycholic acid (TUDCA) is more effective in controlling anxiety-like behavior in aged rats”, Bitlis Eren Fen Bilimleri Dergisi, Vol. 12, Issue 1, Pages 242–246, 2023.
  • [20] Guo, M., Li, M., Zhang, C., et al., “Dietary administration of Bacillus subtilis enhances immune responses and disease resistance in chickens”, Frontiers in Microbiology, Vol. 11, Article 1768, 2020.
  • [21] Kalamara, M., Spacapan, M., Mandic-Mulec, I., et al., “Social behaviours by Bacillus subtilis: quorum sensing, kin discrimination and beyond”, Molecular Microbiology, Vol. 110, Pages 863–878, 2018.
  • [22] Ceylani, T., Jakubowska Doğru, E., Gurbanov, R., Teker, H.T., Gözen, A.G., “The effects of repeated antibiotic administration to juvenile BALB/c mice on the microbiota status and animal behavior at the adult age”, Heliyon, Vol. 4, Issue 6, Article e00644, 2018.
  • [23] Cryan, J.F., O’Mahony, S.M., “The microbiome-gut-brain axis: From bowel to behavior”, Neurogastroenterology & Motility, Vol. 23, Pages 187–192, 2011.
  • [24] Tian, P., O’Riordan, K.J., Lee, Y.K., et al., “Towards a psychobiotic therapy for depression: Bifidobacterium breve CCFM1025 reverses chronic stress-induced depressive symptoms and gut microbial abnormalities in mice”, Neurobiology of Stress, Vol. 12, Article 100216, 2020.
  • [25] Bravo, J.A., Forsythe, P., Chew, M.V., et al., “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, Vol. 108, Pages 16050–16055, 2011.
  • [26] Zhu, X., Sakamoto, S., Ishii, C., et al., “Dectin-1 signaling on colonic γδ T cells promotes psychosocial stress responses”, Nature Immunology, Vol. 24, Pages 625–636, 2023.
  • [27] Ait-Belgnaoui, A., Durand, H., Cartier, C., et al., “Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats”, Psychoneuroendocrinology, Vol. 37, Pages 1885–1895, 2012.
  • [28] Falkenstein, M., Simon, M.C., Mantri, A., et al., “Impact of the gut microbiome composition on social decision-making”, PNAS Nexus, Vol. 3, Issue 5, Article pgae166, 2024.
  • [29] Mazzone, L., et al., “Precision microbial intervention improves social behavior but not autism severity: A pilot double-blind randomized placebo-controlled trial”, Cell Host & Microbe, Vol. 32, Pages 106–116.e6, 2024.
  • [30] Weber, K.T., Varian, B.J., Erdman, S.E., “The gut microbiome and sociability”, Frontiers in Neuroscience, Vol. 18, Article 1372274, 2024.
There are 30 citations in total.

Details

Primary Language English
Subjects Neural Engineering
Journal Section Research Article
Authors

Hikmet Taner Teker 0000-0002-6621-3071

Gizem Hazan Akçay 0000-0002-5885-7934

Şeyma Nur Çetiner This is me 0000-0002-8609-521X

Aydoğan Bora This is me 0000-0003-1979-8692

Taha Ceylani 0000-0002-3041-6010

Publication Date October 27, 2024
Submission Date August 5, 2024
Acceptance Date October 20, 2024
Published in Issue Year 2024

Cite

APA Teker, H. T., Akçay, G. H., Çetiner, Ş. N., Bora, A., et al. (2024). The Impact of Probiotic Intervention during Developmental Cafeteria Diet Consumption on Social Behavior in Adulthood. Hendese Teknik Bilimler Ve Mühendislik Dergisi, 1(2), 67-74. https://doi.org/10.5281/zenodo.13996497