Gut microbiota and changes in cytokine profile in animals with experimental acute disseminated peritonitis on the background of diabetes
Keywords:
microbiological monitoring; pathogens; interleukins; peritonitis; hyperglycemia
Abstract
In the pathogenesis of acute widespread peritonitis and accompanying diabetes, a vital link is an endogenous intoxication caused by the translocation of microorganisms and their toxins from the intestine into the blood, metabolic changes, and immunological reactivity of the body. Our work aimed to investigate the microbial composition in the parietal intestinal biotope and the features of the blood cytokine profile in animals with acute disseminated peritonitis on the background of streptozotocin-induced diabetes. The study was conducted on 56 sexually mature non-linear white male rats. Diabetes mellitus was modeled by a single intraperitoneal injection of streptozotocin (60 mg/kg). On the 14th day of the development of streptozotocin-induced diabetes mellitus, a 10% filtered fecal suspension (0.5 mL) was injected into the abdominal cavity of animals, and acute generalized peritonitis was initiated. Sowing on nutrient media was carried out for bacteriological research to isolate a pure culture of microorganisms and their identification. The concentration of TNF-α, IL-1β, and IL-6 was studied by solid-phase enzyme immunoassay. The research results demonstrate an imbalance of cytokines in the dynamics of experimental acute disseminated peritonitis against the background of diabetes and quantitative and qualitative changes in the microbiota of the parietal intestinal biotope. A decrease in the number of Escherichia coli strains isolated in monoculture and an increase in the number of two-component and three-component microbial associations were revealed, among which Enterobacter aerogenes, Escherichia coli, Bacteroides spp., Proteus mirabilis, Klebsiella spp. and Candida species prevailed.References
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Giesbrecht, K., Förmer, S., Sähr, A., Heeg, K., & Hildebrand, D. (2019). Streptococcal pyrogenic exotoxin a-stimulated monocytes mediate regulatory T-cell accumulation through PD-L1 and kynurenine. International Journal of Molecular Sciences, 20(16), 3933.
Gilmore, W. J., Johnston, E. L., Bitto, N. J., Zavan, L., O'Brien-Simpson, N., Hill, A. F., & Kaparakis-Liaskos, M. (2022). Bacteroides fragilis outer membrane vesicles preferentially activate innate immune receptors compared to their parent bacteria. Frontiers in Immunology, 13, 970725.
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Karpenko, Y., Hunchak, Y., Gutyj, B., Hunchak, A., Parchenko, M., & Parchenko, V. (2022). Advanced research for physico-chemical properties and parameters of toxicity piperazinium 2-((5-(furan-2-YL)-4-phenyl-4H-1,2,4-triazol-3-yl)thio)acetate. ScienceRise: Pharmaceutical Science, 36, 18–25.
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Kotsar, O. V., & Kochnieva, O. V. (2021). Antimicrobial resistance of Escherichia coli strains isolated from patients with purulent peritonitis. Infectious Diseases, 2, 53–57.
Kukhtyn, M., Malimon, Z., Salata, V., Rogalskyy, I., Gutyj, B., Kladnytska, L., Kravcheniuk, K., & Horiuk, Y (2022). The effects of antimicrobial residues on microbiological content and the antibiotic resistance in frozen fish. World’s Veterinary Journal, 12(4), 374–381.
Lazarenko, V. A., Lipatov, V. A., Blinkov, J. J., & Skorikov, D. V. (2008). Eksperimental’naja model’ rasprostranennogo kalovogo peritonita [Experimental model of disseminated fecal peritonitis]. Kurskij Nauchno-Prakticheskij Vestnik “Chelovek i ego Zdorov’e”, 4, 128–132 (in Russian).
Lobo, L. A., Benjamim, C. F., & Oliveira, A. C. (2016). The interplay between microbiota and inflammation: Lessons from peritonitis and sepsis. Clinical and Translational Immunology, 5(7), e90.
Lykhman, V. M., Shevchenko, O. M., Merkulov, A. O., Myroshnychenko, D. O., Tkach, S. V., Bilodid, Y. O., Bitiak, S. Y., & Tokarev, A. V. (2020). Sanatsija cherevnoj porozhnyny pry poshyrenomu perytoniti [Sanitation of the abdominal cavity in widespread peritonitis]. Kharkivs’ka Khirurhichna Shkola, 103, 37–42 (in Ukrainian).
Moganti, K., Li, F., Schmuttermaier, C., Riemann, S., Klüter, H., Gratchev, A., Harmsen, M. C., & Kzhyshkowska, J. (2017). Hyperglycemia induces mixed M1/M2 cytokine profile in primary human monocyte-derived macrophages. Immunobiology, 222(10), 952–959.
Ortega, M. A., Fraile-Martínez, O., Naya, I., García-Honduvilla, N., Álvarez-Mon, M., Buján, J., Asúnsolo, Á., & de la Torre, B. (2020). Type 2 diabetes mellitus associated with obesity (diabesity). The central role of gut microbiota and its translational applications. Nutrients, 12(9), 2749.
Peregudov, S. I., & Khanevich, M. D. (1996). The small intestine as the origin of bacteremia in acute diffuse peritonitis. Nutricion Hospitalaria, 11(6), 317–320.
Piccioni, A., Rosa, F., Mannucci, S., Manca, F., Merra, G., Chiloiro, S., Candelli, M., Covino, M., Gasbarrini, A., & Franceschi, F. (2023). Gut microbiota, LADA, and type 1 diabetes mellitus: An evolving relationship. Biomedicines, 11(3), 707.
Popejoy, M. W., Long, J., & Huntington, J. A. (2017). Analysis of patients with diabetes and complicated intra-abdominal infection or complicated urinary tract infection in phase 3 trials of ceftolozane/tazobactam. BMC Infectious Diseases, 17(1), 316.
Prasad, K. N., Singh, K., Rizwan, A., Mishra, P., Tiwari, D., Prasad, N., & Gupta, A. (2014). Microbiology and outcomes of peritonitis in Northern India. Peritoneal Dialysis International, 34(2), 188–194.
Qiu, D., Zhang, L., Zhan, J., Yang, Q., Xiong, H., Hu, W., Ji, Q., & Huang, J. (2020). Hyperglycemia decreases epithelial cell proliferation and attenuates neutrophil activity by reducing ICAM-1 and LFA-1 expression levels. Frontiers in Genetics, 11, 616988.
Raeeszadeh, M., Hosseini, S., Khanmohammadi, M., Manoochehry, S., & Rasouli, H. R. (2017). Comparison of peritoneal lavage with normal saline and normal saline plus antibiotic in acute peritonitis. Trauma Monthly, 22(5), e58188.
Ramos-Lobo, A. M., Buonfiglio, D. C., & Cipolla-Neto, J. (2015). Streptozotocin-induced diabetes disrupts the body temperature daily rhythm in rats. Diabetology and Metabolic Syndrome, 7, 39.
Riga, A., Boyko, V., & Grirorov, Y. (2019). Serum interleukin-8 in patients with different origin of intra-abdominal infections in perioperative period. Medical Sciences, 7(9), 94.
Ross, J. T., Matthay, M. A., & Harris, H. W. (2018). Secondary peritonitis: Principles of diagnosis and intervention. British Medical Journal, 361, k1407.
Sameliuk, Y., Kaplaushenko, A., Nedorezanıuk, N., Ostretsova, L., Diakova, F., & Gutyj, B. (2022). Prospects for the search for new biologically active compounds among the derivatives of the heterocyclic system of 1,2,4-triazole. Hacettepe University Journal of the Faculty of Pharmacy, 42(3), 175–186.
Seo, S. U., Kamada, N., Muñoz-Planillo, R., Kim, Y. G., Kim, D., Koizumi, Y., Hasegawa, M., Himpsl, S. D., Browne, H. P., Lawley, T. D., Mobley, H. L., Inohara, N., & Núñez, G. (2015). Distinct commensals induce interleukin-1β via NLRP3 inflammasome in inflammatory monocytes to promote intestinal inflammation in response to injury. Immunity, 42(4), 744–755.
Sharma, R., Anuradha, & Nandini, D. (2017). Bacteriological profile and antimicrobial sensitivity pattern in sterile body fluids from a tertiary care hospital. Journal of Applied Microbiology and Biochemistry, 1, 1.
Tai, H., Zhu, Z., Mei, H., Sun, W., & Zhang, W. (2020). Albumin-to-fibrinogen ratio independently predicts 28-day mortality in patients with peritonitis-induced sepsis. Mediators of Inflammation, 2020, 7280708.
Tessaro, F. H. G., Ayala, T. S., Nolasco, E. L., Bella, L. M., & Martins, J. O. (2017). Insulin influences LPS-induced TNF-α and IL-6 release through distinct pathways in mouse macrophages from different compartments. Cellular Physiology and Biochemistry, 42(5), 2093–2104.
Toniolo, A., Cassani, G., Puggioni, A., Rossi, A., Colombo, A., Onodera, T., & Ferrannini, E. (2019). The diabetes pandemic and associated infections: Suggestions for clinical microbiology. Reviews in Medical Microbiology, 30(1), 1–17.
Vergadi, E., Vaporidi, K., & Tsatsanis, C. (2018). Regulation of endotoxin tolerance and compensatory anti-inflammatory response syndrome by non-coding RNAs. Frontiers in Immunology, 9, 2705.
Zaporozhan, S. Y., Tkach, V. O., & Dombrovskyi, O. A. (2020). Efektyvnist’ likuvannia poshyrenoho vtorynnoho hniinoho perytonitu iz zastosuvanniam relaparotomiji [Treatment efficacy of widespread secondary purulent peritonitis with the use of relaparotomy]. Shpytal’na Khirurhiia, 3, 50–54 (in Ukrainian).
Zhou, Z., Sun, B., Yu, D., & Zhu, C. (2022). Gut microbiota: An important player in type 2 diabetes mellitus. Frontiers in Cellular and Infection Microbiology, 12, 834485.
Arango Duque, G., & Descoteaux, A. (2014). Macrophage cytokines: Involvement in immunity and infectious diseases. Frontiers in Immunology, 5, 491.
Armbruster, C. E., Mobley, H. L. T., & Pearson, M. M. (2018). Pathogenesis of Proteus mirabilis infection. EcoSal Plus, 8(1), 9.
Bashchenko, M. I., Boiko, О. V., Honchar, О. F., Gutyj, B. V., Lesyk, Y. V., Ostapyuk, A. Y., Kovalchuk, І. І., & Leskiv, K. Y. (2020). The effect of milk thistle, metiphen, and silimevit on the protein-synthesizing function of the liver of laying hens in experimental chronic cadmium toxicosis. Ukrainian Journal of Ecology, 10(6), 164–168.
Boiko, T. I. (2010). Klinichni laboratorni doslidzhennia [Clinical laboratory diagnostics]. Medytsyna, Kyiv (in Ukrainian).
Clements, T. W., Tolonen, M., Ball, C. G., & Kirkpatrick, A. W. (2021). Secondary peritonitis and intra-abdominal sepsis: An increasingly global disease in search of better systemic therapies. Scandinavian Journal of Surgery, 110(2), 139–149.
Craciun, C. I., Neag, M. A., Catinean, A., Mitre, A. O., Rusu, A., Bala, C., Roman, G., Buzoianu, A. D., Muntean, D. M., & Craciun, A. E. (2022). The relationships between gut microbiota and diabetes mellitus, and treatments for diabetes mellitus. Biomedicines, 10(2), 308.
Fu, Y. L., & Harrison, R. E. (2021). Microbial phagocytic receptors and their potential involvement in cytokine induction in macrophages. Frontiers in Immunology, 12, 662063.
Giesbrecht, K., Förmer, S., Sähr, A., Heeg, K., & Hildebrand, D. (2019). Streptococcal pyrogenic exotoxin a-stimulated monocytes mediate regulatory T-cell accumulation through PD-L1 and kynurenine. International Journal of Molecular Sciences, 20(16), 3933.
Gilmore, W. J., Johnston, E. L., Bitto, N. J., Zavan, L., O'Brien-Simpson, N., Hill, A. F., & Kaparakis-Liaskos, M. (2022). Bacteroides fragilis outer membrane vesicles preferentially activate innate immune receptors compared to their parent bacteria. Frontiers in Immunology, 13, 970725.
Grotelüschen, R., Heidelmann, L. M., Lütgehetmann, M., Melling, N., Reeh, M., Ghadban, T., Dupree, A., Izbicki, J. R., & Bachmann, K. A. (2020). Antibiotic sensitivity in correlation to the origin of secondary peritonitis: A single center analysis. Scientific Reports, 10(1), 18588.
Grynchuk, F. V., Polianskiy, I. Y., Grynchuk, A. F., Sheremet, M., Maksymyuk, V. V., Tarabanchuk, V. V., & Vasylovych, V. S. (2021). Characteristics of cytokine status in intra-abdominal infection with underlying diabetes mellitus: An experimental study. Romanian Journal of Diabetes Nutrition and Metabolic Diseases, 28(3), 255–260.
Hugon, P., Dufour, J.-C., Colson, P., Fournier, P.-E., Sallah, K., & Raoult, D. (2015). A comprehensive repertoire of prokaryotic species identified in human beings. The Lancet Infectious Diseases, 15, 1211–1219.
Huttenhower, C., Gevers, D., Knight, R., Abubucker, S., Badger, J. H., Chinwalla, A. T., Creasy, H. H., Earl, A. M., & Fitzgerald, M. G., The Human Microbiome Project Consortium et al. (2012). Structure, function and diversity of the healthy human microbiome. Nature, 486, 207–214.
Kaneko, N., Kurata, M., Yamamoto, T., Morikawa, S., & Masumoto, J. (2019). The role of interleukin-1 in general pathology. Inflammation and Regeneration, 39, 12.
Karpenko, Y., Hunchak, Y., Gutyj, B., Hunchak, A., Parchenko, M., & Parchenko, V. (2022). Advanced research for physico-chemical properties and parameters of toxicity piperazinium 2-((5-(furan-2-YL)-4-phenyl-4H-1,2,4-triazol-3-yl)thio)acetate. ScienceRise: Pharmaceutical Science, 36, 18–25.
Kiani, D., Santus, W., Kiernan, K. A., & Behnsen, J. (2021). Proteus mirabilis employs a contact-dependent killing system against competing Enterobacteriaceae. mSphere, 6(4), e0032121.
Kim, J. W., Park, J. H., Kim, D. J., Choi, W. H., Cheong, J. C., & Kim, J. Y. (2017). The delta neutrophil index is a prognostic factor for postoperative mortality in patients with sepsis caused by peritonitis. PloS One, 12(8), e0182325.
Kotsar, O. V., & Kochnieva, O. V. (2021). Antimicrobial resistance of Escherichia coli strains isolated from patients with purulent peritonitis. Infectious Diseases, 2, 53–57.
Kukhtyn, M., Malimon, Z., Salata, V., Rogalskyy, I., Gutyj, B., Kladnytska, L., Kravcheniuk, K., & Horiuk, Y (2022). The effects of antimicrobial residues on microbiological content and the antibiotic resistance in frozen fish. World’s Veterinary Journal, 12(4), 374–381.
Lazarenko, V. A., Lipatov, V. A., Blinkov, J. J., & Skorikov, D. V. (2008). Eksperimental’naja model’ rasprostranennogo kalovogo peritonita [Experimental model of disseminated fecal peritonitis]. Kurskij Nauchno-Prakticheskij Vestnik “Chelovek i ego Zdorov’e”, 4, 128–132 (in Russian).
Lobo, L. A., Benjamim, C. F., & Oliveira, A. C. (2016). The interplay between microbiota and inflammation: Lessons from peritonitis and sepsis. Clinical and Translational Immunology, 5(7), e90.
Lykhman, V. M., Shevchenko, O. M., Merkulov, A. O., Myroshnychenko, D. O., Tkach, S. V., Bilodid, Y. O., Bitiak, S. Y., & Tokarev, A. V. (2020). Sanatsija cherevnoj porozhnyny pry poshyrenomu perytoniti [Sanitation of the abdominal cavity in widespread peritonitis]. Kharkivs’ka Khirurhichna Shkola, 103, 37–42 (in Ukrainian).
Moganti, K., Li, F., Schmuttermaier, C., Riemann, S., Klüter, H., Gratchev, A., Harmsen, M. C., & Kzhyshkowska, J. (2017). Hyperglycemia induces mixed M1/M2 cytokine profile in primary human monocyte-derived macrophages. Immunobiology, 222(10), 952–959.
Ortega, M. A., Fraile-Martínez, O., Naya, I., García-Honduvilla, N., Álvarez-Mon, M., Buján, J., Asúnsolo, Á., & de la Torre, B. (2020). Type 2 diabetes mellitus associated with obesity (diabesity). The central role of gut microbiota and its translational applications. Nutrients, 12(9), 2749.
Peregudov, S. I., & Khanevich, M. D. (1996). The small intestine as the origin of bacteremia in acute diffuse peritonitis. Nutricion Hospitalaria, 11(6), 317–320.
Piccioni, A., Rosa, F., Mannucci, S., Manca, F., Merra, G., Chiloiro, S., Candelli, M., Covino, M., Gasbarrini, A., & Franceschi, F. (2023). Gut microbiota, LADA, and type 1 diabetes mellitus: An evolving relationship. Biomedicines, 11(3), 707.
Popejoy, M. W., Long, J., & Huntington, J. A. (2017). Analysis of patients with diabetes and complicated intra-abdominal infection or complicated urinary tract infection in phase 3 trials of ceftolozane/tazobactam. BMC Infectious Diseases, 17(1), 316.
Prasad, K. N., Singh, K., Rizwan, A., Mishra, P., Tiwari, D., Prasad, N., & Gupta, A. (2014). Microbiology and outcomes of peritonitis in Northern India. Peritoneal Dialysis International, 34(2), 188–194.
Qiu, D., Zhang, L., Zhan, J., Yang, Q., Xiong, H., Hu, W., Ji, Q., & Huang, J. (2020). Hyperglycemia decreases epithelial cell proliferation and attenuates neutrophil activity by reducing ICAM-1 and LFA-1 expression levels. Frontiers in Genetics, 11, 616988.
Raeeszadeh, M., Hosseini, S., Khanmohammadi, M., Manoochehry, S., & Rasouli, H. R. (2017). Comparison of peritoneal lavage with normal saline and normal saline plus antibiotic in acute peritonitis. Trauma Monthly, 22(5), e58188.
Ramos-Lobo, A. M., Buonfiglio, D. C., & Cipolla-Neto, J. (2015). Streptozotocin-induced diabetes disrupts the body temperature daily rhythm in rats. Diabetology and Metabolic Syndrome, 7, 39.
Riga, A., Boyko, V., & Grirorov, Y. (2019). Serum interleukin-8 in patients with different origin of intra-abdominal infections in perioperative period. Medical Sciences, 7(9), 94.
Ross, J. T., Matthay, M. A., & Harris, H. W. (2018). Secondary peritonitis: Principles of diagnosis and intervention. British Medical Journal, 361, k1407.
Sameliuk, Y., Kaplaushenko, A., Nedorezanıuk, N., Ostretsova, L., Diakova, F., & Gutyj, B. (2022). Prospects for the search for new biologically active compounds among the derivatives of the heterocyclic system of 1,2,4-triazole. Hacettepe University Journal of the Faculty of Pharmacy, 42(3), 175–186.
Seo, S. U., Kamada, N., Muñoz-Planillo, R., Kim, Y. G., Kim, D., Koizumi, Y., Hasegawa, M., Himpsl, S. D., Browne, H. P., Lawley, T. D., Mobley, H. L., Inohara, N., & Núñez, G. (2015). Distinct commensals induce interleukin-1β via NLRP3 inflammasome in inflammatory monocytes to promote intestinal inflammation in response to injury. Immunity, 42(4), 744–755.
Sharma, R., Anuradha, & Nandini, D. (2017). Bacteriological profile and antimicrobial sensitivity pattern in sterile body fluids from a tertiary care hospital. Journal of Applied Microbiology and Biochemistry, 1, 1.
Tai, H., Zhu, Z., Mei, H., Sun, W., & Zhang, W. (2020). Albumin-to-fibrinogen ratio independently predicts 28-day mortality in patients with peritonitis-induced sepsis. Mediators of Inflammation, 2020, 7280708.
Tessaro, F. H. G., Ayala, T. S., Nolasco, E. L., Bella, L. M., & Martins, J. O. (2017). Insulin influences LPS-induced TNF-α and IL-6 release through distinct pathways in mouse macrophages from different compartments. Cellular Physiology and Biochemistry, 42(5), 2093–2104.
Toniolo, A., Cassani, G., Puggioni, A., Rossi, A., Colombo, A., Onodera, T., & Ferrannini, E. (2019). The diabetes pandemic and associated infections: Suggestions for clinical microbiology. Reviews in Medical Microbiology, 30(1), 1–17.
Vergadi, E., Vaporidi, K., & Tsatsanis, C. (2018). Regulation of endotoxin tolerance and compensatory anti-inflammatory response syndrome by non-coding RNAs. Frontiers in Immunology, 9, 2705.
Zaporozhan, S. Y., Tkach, V. O., & Dombrovskyi, O. A. (2020). Efektyvnist’ likuvannia poshyrenoho vtorynnoho hniinoho perytonitu iz zastosuvanniam relaparotomiji [Treatment efficacy of widespread secondary purulent peritonitis with the use of relaparotomy]. Shpytal’na Khirurhiia, 3, 50–54 (in Ukrainian).
Zhou, Z., Sun, B., Yu, D., & Zhu, C. (2022). Gut microbiota: An important player in type 2 diabetes mellitus. Frontiers in Cellular and Infection Microbiology, 12, 834485.
Published
2023-08-23
How to Cite
Verveha, B. M., Gutyj, B. V., Holubiev, M. I., Kondro, M. M., & DatsІ. V. (2023). Gut microbiota and changes in cytokine profile in animals with experimental acute disseminated peritonitis on the background of diabetes . Regulatory Mechanisms in Biosystems, 14(3), 506-510. https://doi.org/10.15421/10.15421/022372
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