Kronik enteropatili kedilerde bağırsak mikrobiyota analizleri ile kısa dönem rektal enema probiyotik sağaltımı

Year 2023, , 16 - 30, 31.03.2023

Kerem Ural , Hasan Erdoğan , Songül Erdoğan , Serdar Paşa , Tuğba Aslan , Cansu Balıkçı , Gamze Gökçay

https://doi.org/10.30607/kvj.1177247

Abstract

Bağırsak mikrobiyotasındaki bir dengesizlik, kedilerdeki kronik enteropatide olduğu gibi gastrointestinal sistemdeki kronik inflamasyon oluşumu için hazırlayıcı bir faktör olarak hizmet ettiği tespit edilmiştir. Probiyotik uygulamasının gastrointestinal rahatsızlıkları azaltabileceği varsayımı göz önüne alındığında, ülkemizde kronik enteropatili kedilerde rektal yoldan etkileri hiç araştırılmamıştır. Bu nedenle bu çalışmanın amacı, kedilerde Bifidobacterium kombinasyonu [Bifidobacterium longum, Bifidobacterium bifidum, Bifidobacterium animalis], Lactobacillus suşları [Lactobacillus rhamnosus, Lactobacillus gastrikus, Lactobacillus acidophilus], Bacillus suşları [Bacillus clausii, Bacillus subtilis] ve yeni nesil bir probiyotik Akkermansia muciniphilia'yı içeren çok zincirli bir probiyotik tedavisinin terapötik etkinliğini kedilerde rektal yoldan (enema) değerlendirmektir. Teşhis, a) klinik, b) hematolojik ve serum biyokimyasal analizlerinin yanı sıra Feline Kronik Enteropati Aktivite İndeksi'ne (FCEAI) göre puanlamaya dayanıyordu. Her kedi muayene edildi ve analiz edildi/yeniden değerlendirildi ve 10 günlük indüksiyon dönemi için tedavinin başlangıcında ve sonunda bir FCEAI puanı verildi. Rektal lavman probiyotik tedavisi, yorumlamaya tabi tutulmuş kompozit FCEAI skoru (p<0.01) ve laboratuvar parametreleri yeniden değerlendirme değerleri (p<0.01) anlamlı derecede azalmıştır. Herhangi bir yan etkisi olmayan bu tedavi yöntemi, tekrarlayan ve dejeneratif etkileri olan diğer ilgili tedavi yöntemlerinin yerini almalıdır.

Keywords

disbiyoz, ; Gİ inflamasyon, mikrobiyom analizi, probiyoterapi

Short-Term Rectal Enema Probiotic Treatment with Intestinal Microbiota Analysis in Cats with Chronic Enteropathy

Abstract

An imbalance in gut microbiota detected to serve as a predisposing factor for existence of chronic inflammation of the gastrointestinal tract, such as chronic enteropathy among cats. Given the postulation that probiotic administration might mitigate gastrointestinal disorders, its effects via rectal route have never been explored in our country among cats with chronic enteropathy. Thus the purpose of the present study was to evaluate the therapeutical efficacy of an multiple chain probiotic treatment involving Bifidobacterium combination [Bifidobacterium longum, Bifidobacterium bifidum, Bifidobacterium animalis], Lactobacillus strains [Lactobacillus rhamnosus, Lactobacillus gastricus, Lactobacillus acidophilus, Lactobacillus plantarum], Bacillus strains [Bacillus clausii, Bacillus subtilis] and a next generation probiotic Akkermansia muciniphilia via rectal route (enema)in cats with cEnT. Diagnosis was based on a) clinical, b) hematological and serum biochemical analysis along with scoring to those of Feline Chronic Enteropathy Activity Index (FCEAI). Each cat was inspected and analyzed/reevaluated and assigned a FCEAI score at the start and end of treatment for 10 day induction period. Rectal enema probiotic treatment resulted with significantly decreased composite FCEAI score (p<0.01) and laboratory parameters re-evaluation values (p<0.01) subjected to interpretation. This treatment modality without any side effects, should be subtitute other relevant treatment modalities with relapsing and degenerative effects.

Keywords

dysbiosis, GI inflammation, Microbiome analysis, Probiotheraphy

References

• Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nature reviews immunology, 2008;8(6):411-420.
• Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. Bacteria and host interactions in the gut epithelial barrier. Nature chemical biology, 2012;8(1):36-45.
• Ashrafian F, Keshavarz Azizi Raftar , Shahryari, A, Behrouzi A, Yaghoubfar R, Lari A, Siadat SD. Comparative effects of alive and pasteurized Akkermansia muciniphila on normal diet-fed mice. Scientific reports, 2021;11(1):1-13.
• Bernstein CN. Treatment of IBD: where we are and where we are going. Official journal of the American College of Gastroenterology. ACG. 2015;110(1):114-126.
• Canani RB, Di Costanzo M, Leone L, Pedata M, Meli R, Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World journal of gastroenterology: WJG. 2011;17(12):1519.
• Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet–induced obesity and diabetes in mice. Diabetes. 2008;57(6):1470-1481.
• Cresci GA, Bush K, Nagy LE. Tributyrin supplementation protects mice from acute ethanol‐induced gut injury. Alcoholism: Clinical and Experimental Research. 2014;38(6): 1489-1501.
• de La Serre CB, Ellis CL, Lee J, Hartma AL, Rutledge JC, Raybould HE. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2010;299(2):G440-G448.
• Dennis JS, Kruger JM, Mullaney TP. Lymphocytic/plasmacytic colitis in cats: 14 cases (1985-1990). Journal of the American Veterinary Medical Association. 1993;202(2): 313-318.
• Dennis JS, Kruger JM, Mullaney TP. Lymphocytic/plasmacytic gastroenteritis in cats: 14 cases (1985-1990). Journal of the American Veterinary Medical Association. 1992;200(11):1712-1718.
• Depommier C, Everard A, Druart C, Plovier H, Van Hul M, Vieira-Silva S, Cani PD. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nature medicine. 2019;25(7):1096-1103.
• Everard A, Belzer C, Geurts, L, Ouwerkerk JP, Druart C, Bindels LB, Cani PD. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proceedings of the national academy of sciences. 2013;110(22):9066-9071.
• Falony G, De Vuyst L. Ecological interactions of bacteria in the human gut. Prebiotics and probiotics science and technology. 2009;639.
• Falony G, Vlachou A, Verbrugghe K, Vuyst LD. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Applied and environmental microbiology. 2006;72(12):7835-7841.
• Garcia-Mazcorro JF, Minamoto Y, Kawas JR, Suchodolski JS, de Vos WM. Akkermansia and microbial degradation of mucus in cats and dogs: implications to the growing worldwide epidemic of pet obesity. Veterinary sciences. 2020;7(2):44.
• Geerlings SY, Kostopoulos I, De Vos WM, Belzer C. Akkermansia muciniphila in the human gastrointestinal tract: when, where, and how?. Microorganisms. 2018;6(3):75.
• Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. The Journal of nutrition. 1995;125(6):1401-1412.
• Hajela N, Ramakrishna BS, Nair GB, Abraham P, Gopalan S, Ganguly NK. Gut microbiome, gut function, and probiotics: Implications for health. Indian Journal of Gastroenterology. 2015;34(2):93-107.
• Halfvarson J, Brislawn CJ, Lamendella R, Vázquez-Baeza Y, Walters WA, Bramer LM, Jansson JK. Dynamics of the human gut microbiome in inflammatory bowel disease. Nature microbiology. 2017;2(5):1-7.
• Hall EJ, German AJ. Diseases of the small intestine. In: Ettinger SJ, Feldman EC., eds. Textbook of Veterinary Internal Medicine, 6th ed. Philadelphia, PA: Saunders. 2004; pp.1332–1378.
• Hamer HM, Jonkers DMAE, Venema K, Vanhoutvin SALW, Troost FJ, Brummer RJ. The role of butyrate on colonic function. Alimentary pharmacology & therapeutics. 2008;27(2):104-119.
• Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, Suchodolski JS. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS microbiology ecology. 2011;76(2):301-310.
• Hart JR, Shaker E, Patnaik AK, Garvey MS. Lymphocytic-plasmacytic enterocolitis in cats: 60 cases (1988-1990). American Animal Hospital Association (USA). 1994.
• Jergens AE, Crandell JM, Evans R, Ackermann M, Miles KG, Wang C. A clinical index for disease activity in cats with chronic enteropathy. Journal of veterinary internal medicine. 2010;24(5):1027-1033.
• Jergens AE, Moore FM, Haynes JS, Miles KG. Idiopathic inflammatory bowel disease in dogs and cats: 84 cases (1987-1990). Journal of the American Veterinary Medical Association. 1992;201(10):1603-1608.
• Jha PN, Gomaa AB, Yanni YG, El-Saadany AEY, Stedtfeld, TM, Stedtfeld RD, Dazzo FB. Alterations in the endophyte-enriched root-associated microbiome of rice receiving growth-promoting treatments of urea fertilizer and Rhizobium biofertilizer. Microbial ecology. 2020;79(2):367-382.
• Jugan MC, Rudinsky AJ, Gordon A, Kramer DL, Daniels JB. Paliy O, Gilor C. Effects of oral Akkermansia muciniphila supplementation in healthy dogs following antimicrobial administration. American journal of veterinary research. 2018);79(8):884-892.
• Klijn A, Mercenier A, Arigoni F. Lessons from the genomes of bifidobacteria. FEMS Microbiology Reviews. 2005;29(3):491-509.
• Kusumo PD, Maulahela H, Utari AP, Surono IS, Soebandrio A, Abdullah M. Probiotic Lactobacillus plantarum IS 10506 supplementation increase SCFA of women with functional constipation. Iranian Journal of Microbiology. 2019;11(5):389.
• Larrosa M, Luceri C, Vivoli E, Pagliuca C, Lodovici M, Moneti G, Dolara P. Polyphenol metabolites from colonic microbiota exert anti‐inflammatory activity on different inflammation models. Molecular nutrition & food research. 2009;53(8):1044-1054.
• Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837-848.
• Li J, Butcher J, Mack D, Stintzi A. Functional impacts of the intestinal microbiome in the pathogenesis of inflammatory bowel disease. Inflammatory bowel diseases. 2015;21(1):139-153.
• Macfarlane GT. The colonic flora, fermentation and large bowel digestive function. The large intestine: physiology, pathophysiology and disease.1991;51-92.
• Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Vermeire S. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63(8):1275-1283.
• Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A, Gordon JI. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proceedings of the National Academy of Sciences. 2009;106(14):5859-5864.
• Makras L, Falony G, Van der Meulen R, De Vuyst L. Production of organic acids from fermentation of mannitol, fructooligosaccharides and inulin by a cholesterol removing Lactobacillus acidophilus strain. Journal of applied microbiology. 2006;100(6):1388-1390.
• Makras L, Van Acker G, De Vuyst L. Lactobacillus paracasei subsp. paracasei 8700: 2 degrades inulin-type fructans exhibiting different degrees of polymerization. Applied and Environmental Microbiology. 2005;71(11):6531-6537. Marsilio S, Pilla R, Sarawichitr B, Chow B, Hill SL, Ackermann MR, Suchodolski JS. Characterization of the fecal microbiome in cats with inflammatory bowel disease or alimentary small cell lymphoma. Scientific reports. 2019;9(1):1-11.
• Morrison DJ, Mackay WG, Edwards CA, Preston T, Dodson B, Weaver LT. Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate?. British Journal of Nutrition. 2006;96(3):570-577.
• Nagao-Kitamoto H, Kamada N. Host-microbial cross-talk in inflammatory bowel disease. Immune network. 2017;17(1):1-12.
• Paturi G, Mandimika T, Butts CA, Zhu S, Roy NC, McNabb WC, Ansell J. Influence of dietary blueberry and broccoli on cecal microbiota activity and colon morphology in mdr1a−/− mice, a model of inflammatory bowel diseases. Nutrition. 2012;28(3):324-330.
• Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. The Journal of nutrition. 2009;139(9):1619-1625.
• Roberfroid MB, Van Loo JA, Gibson GR. The bifidogenic nature of chicory inulin and its hydrolysis products. The Journal of nutrition. 1998;128(1):11-19.
• Scheppach W, Weiler F. The butyrate story: old wine in new bottles?. Current Opinion in Clinical Nutrition & Metabolic Care. 2004;7(5):563-567.
• Siavoshian S, Segain JP, Kornprobst M. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease. Gut. 2000;47:397-403.
• Tsukahara T, Iwasaki Y, Nakayama K, Ushida K. Stimulation of butyrate production in the large intestine of weaning piglets by dietary fructooligosaccharides and its influence on the histological variables of the large intestinal mucosa. Journal of nutritional science and vitaminology. 2003;49(6):414-421.
• Turner JR. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. The American journal of pathology. 2006;169(6):1901-1909.
• Ural K, Erdoğan H, Erdoğan S, Camkerten İ, Şahin N. Circulating Serum Zonulin Levels Before and After Probiotic Enema Treatment in Dogs with Atopic Dermatitis: Randomized Clinical Study Turkiye Klinikleri J Vet Sci. 2021a;12(2):70-8
• Ural K, Erdoğan S, Balıkçı C, Erdoğan H. Inovatif Gastroentero-Dermatoloji Kapsamında Muhtelif Yöntem Geliştirme I: Lactobacillus plantarum ve Lactobacillus paracasei ile Probiyotik Eneması Atopik Dermatitli Köpeklerde Anti-Pruritik Etkinlik Sağlar Mı? Van Vet J. 2021b;32(2):74-81
• Ural K, Gültekin M, Erdoğan H, Erdoğan S, Gul G, Türk E. Kısa Dönem Değişmeli Takvim Probiyotik Sağaltımıyla Atopik Dermatitli Köpeklerde Kaşıntı Giderilebilir mi? Turkiye Klinikleri J Vet Sci. 2020a;11(1):1-8
• Ural K. Küçük hayvan hekimliğinde dermatoloji alanında yeni dönem: bağırsak-beyin-deri ekseni-I ve II. Uluslararası Vetexpo Veteriner Bilimleri Kongresi Sözlü sunumları. 20-22.09.2019. İstanbul. 2019a.
• Ural K. Veteriner İç Hastalıklarında Probiyotikler: Probiyotik Kullanımı rehber Kitabı ve Olgu Atlası. Atalay konf. ve Matb., Ankara. 2020b; pp. 200.
• Van der Meulen R, Avonts L, De Vuyst L. Short fractions of oligofructose are preferentially metabolized by Bifidobacterium animalis DN-173 010. Applied and environmental microbiology. 2004;70(4):1923-1930.
• Walker AW, Lawley TD. Therapeutic modulation of intestinal dysbiosis. Pharmacological research. 2013;69(1):75-86.
• Wang J, Ji H, Wang S, Liu H, Zhang W, Zhang D, Wang Y. Probiotic Lactobacillus plantarum promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Frontiers in microbiology. 2018;9:1953.
• Williams S. Observations on the flora of the alimentary tract of animals and factors affecting its composition. Journal of Pathology and Bacteriology. 1965;89(1):95-122.
• Wong JM, De Souza R, Kendall CW, Emam A, Jenkins, DJ. Colonic health: fermentation and short chain fatty acids. Journal of clinical gastroenterology. 2006;40(3):235-243.
• Wult M, Hagslatt MLJ, Odenholt I, Berggren A. Lactobacillus planatarum 299v enhances the concentrations of fecal short chain fatty acids in patients with recurrent clostridium difficile associated diarrhea. Dig Dis Sci. 2007;52:2082-2086.
• Xiao L, Feng Q, Liang S, Sonne S B, Xia Z, Qiu X, Kristiansen K. A catalog of the mouse gut metagenome. Nature biotechnology. 2015;33(10):1103-1108.