nogrЭкспериментальная и клиническая гастроэнтерологияExperimental and Clinical Gastroenterology1682-8658«Global Media Technologies»nogr-437Research ArticleЭКСПЕРИМЕНТАЛЬНАЯ ГАСТРОЭНТЕРОЛОГИЯEXPERIMENTAL GASTROENTEROLOGYДИСБИОЗ КИШЕЧНИКА ПРИ ЯЗВЕННОМ КОЛИТЕ И ЦЕЛИАКИИ И ЕГО ТЕРАПЕВТИЧЕСКАЯ КОРРЕКЦИЯ С ПОМОЩЬЮ МАСЛЯНОЙ КИСЛОТЫ В КОМБИНАЦИИ С ИНУЛИНОМDYSBIOSIS IN ULCERATIVE COLITIS AND CELIAC DISEASE AND ITS THERAPEUTIC CORRECTION BY BUTYRIC ACID PLUS INULINСиткинС. И.SitkinS. I.drsitkin@gmail.comВахитовТ. Я.VakhitovT. Ya.noemail@neicon.ruТкаченкоЕ. И.TkachenkoE. I.noemail@neicon.ruОрешкоЛ. С.OreshkoL. S.noemail@neicon.ruЖигаловаТ. Н.ZhigalovaT. N.noemail@neicon.ruРадченкоВ. Г.RadchenkoV. G.noemail@neicon.ruСеливерстовП. В.SeliverstovP. V.noemail@neicon.ruАвалуеваЕ. Б.AvaluevaE. B.noemail@neicon.ruСувороваМ. А.SuvorovaM. A.noemail@neicon.ruУтсальВ. А.UtsalV. A.noemail@neicon.ruСЗГМУ им. И. И. Мечникова; Гос. НИИ ОЧБ ФМБА РоссииРоссияState Research Institute of Highly Pure Biopreparations; North-Western State Medical University named after I. I. MechnikovRussian FederationГос. НИИ ОЧБ ФМБА РоссииРоссияState Research Institute of Highly Pure BiopreparationsRussian FederationВоенно-медицинская академия имени С. М. КироваРоссияKirov Military Medical AcademyRussian FederationСЗГМУ им. И. И. МечниковаРоссияNorth-Western State Medical University named after I. I. MechnikovRussian FederationИнститут экспериментальной медициныРоссияInstitute of Experimental MedicineRussian FederationИнститут токсикологии ФМБА РоссииРоссияInstitute of Toxicology of FMBARussian Federation201720062017067798Copyright © Ситкин С.И., Вахитов Т.Я., Ткаченко Е.И., Орешко Л.С., Жигалова Т.Н., Радченко В.Г., Селиверстов П.В., Авалуева Е.Б., Суворова М.А., Утсаль В.А., 20172017Ситкин С.И., Вахитов Т.Я., Ткаченко Е.И., Орешко Л.С., Жигалова Т.Н., Радченко В.Г., Селиверстов П.В., Авалуева Е.Б., Суворова М.А., Утсаль В.А.Sitkin S.I., Vakhitov T.Y., Tkachenko E.I., Oreshko L.S., Zhigalova T.N., Radchenko V.G., Seliverstov P.V., Avalueva E.B., Suvorova M.A., Utsal V.A.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.nogr.org/jour/article/view/437

Цель исследования: оценить динамику количественных показателей микробиоты толстой кишки, метаболома сыворотки крови и некоторых клинико-лабораторных показателей у больных язвенным колитом (ЯК) и пациентов с целиакией (Ц) на фоне перорального приема масляной кислоты в комбинации с инулином (Закофальк NMX). Материалы и методы: В исследование было включено 40 пациентов с активным язвенным колитом (левостороннее поражение, легкая и среднетяжелая атаки) и 43 пациента с целиакией в фазе ремиссии на фоне безглютеновой диеты. Для количественного определения микроорганизмов ДНК, выделенную из образцов кала, подвергали полимеразной цепной реакции (ПЦР) в режиме реального времени. Состав метаболома сыворотки крови определялся с помощью метода газовой хроматографии - масс-спектрометрии (ГХ-МС). Дизайн исследования: открытое рандомизированное исследование в параллельных группах. Пациенты с язвенным колитом были рандомизированы в группы A1 и A2, больные целиакией - в группы B 1 и B 2. Пациенты, вошедшие в группы A1 (ЯК) и B 1 (Ц), в течение 28 дней получали Закофальк NMX в дополнение к базисной терапии пероральным месалазином (ЯК) или безглютеновой диете (Ц). Пациенты из группы A2 (ЯК) в течение 28 дней получали только базисную терапию, пациенты из группы B 2 (Ц) - безглютеновую диету. Результаты: На фоне дополнительного применения масляной кислоты в комбинации с инулином в течение 28 дней выявлено значимое увеличение численности всего пула бутират-продуцирующих бактерий, имеющих ген бутирил-КоA: ацетат-КоA-трансферазы (but), как у пациентов с язвенным колитом, так и у больных целиакией. Бутират также значимо снижал исходно повышенное отношение Bacteroides fragilis spp. к Faecalibacterium prausnitzii в обеих группах (A1 и B 1) до значений, характерных для здоровых лиц. Значимые изменения микробиоценоза толстой кишки у пациентов с язвенным колитом и больных целиакией сопровождались изменениями концентраций метаболитов микробного происхождения в сыворотке крови (снижение уровня противовоспалительных капроновой и гликолевой кислот, повышение уровня провоспалительных метаболитов - молочной, 2-гидроксиизовалериановой, янтарной, фумаровой, бензойной, парагидроксифенилуксусной и индолуксусной кислот). На фоне дополнительного применения масляной кислоты в комбинации с инулином отмечалось значимое понижение сывороточных концентраций провоспалительных метаболитов микробного происхождения - янтарной кислоты (как у больных язвенным колитом, так и у пациентов с целиакией) и 2-гидроксиизовалериановой кислоты (у больных целиакией). У значимо большего числа пациентов (85 %) из группы A1, получавших Закофальк NMX, по сравнению с 55 % пациентов из группы A2 (p = 0,048; точный критерий Фишера) через 14 дней наблюдалось клиническое улучшение (урежение частоты стула и уменьшение ректального кровотечения). У пациентов с целиакией из группы B 1, получавших Закофальк NMX, наблюдалось значимое улучшение субпоказателей синдрома диспепсии и синдрома абдоминальной боли шкалы GSRS через 28 дней (снижение с 3,8 до 2,1 и с 3,2 до 1,7; p < 0,05). Дополнительный прием масляной кислоты в комбинации с инулином снижал интенсивность вздутия живота у 73 % пациентов из группы B 1, в то время как улучшение этого симптома наблюдалось только у 29 % пациентов в группе B 2 (p = 0,006; точный критерий Фишера). Выводы: Помимо противовоспалительных и иммуномодулирующих эффектов, масляная кислота способна оказывать пребиотическое (бутирогенное) действие, восстанавливая пул бутират-продуцирующих микроорганизмов при дисбиотических состояниях, связанных с хроническим воспалением в толстой кишке (ВЗК) или обусловленных снижением потребления пищевых волокон (при безглютеновой диете). Значимое снижение отношения Bacteroides fragilis к Faecalibacterium prausnitzii на фоне дополнительного применения масляной кислоты в комбинации с инулином свидетельствует об эффективном купировании таксономического дисбиоза кишечника провоспалительного типа, а снижение уровня провоспалительных метаболитов микробного происхождения в сыворотке крови - о возможности эффективной коррекции метаболического дисбиоза с помощью метабиотиков как при язвенном колите, так и при целиакии. Клинические данные также позволяют рекомендовать назначение масляной кислоты в комбинации с инулином в дополнение к базисной терапии при язвенном колите и безглютеновой диете при целиакии с целью более быстрого купирования основных симптомов заболеваний.

Aim: to investigate changes in the composition of fecal microbiota, serum metabolome and some clinical parameters following oral calcium butyrate plus inulin (Zacofalk NMX) in patients with ulcerative colitis (UC) and celiac disease (CD). Methods: 40 mild-to-moderate active left-sided UC patients and 43 CD patients in remission on a gluten-free diet were enrolled in the study. The quantitative real-time polymerase chain reaction (qRT-PCR) was used for fecal microbiota assessment. Serum metabolomic assays were conducted using the GC-MS. Study design: an open, randomized, parallel-group study. UC patients were randomized into A1 and A2 groups and CD patients were randomized into B 1 and B 2 groups. Patients enrolled in the groups A1 (UC) and B 1 (CD) received Zacofalk NMX (Dr. Falk Pharma GmbH, 3 tablets per day) for 28 days as supplement to oral mesalazine (standard treatment) in UC or gluten-free diet (GFD) in CD. Patients from group A2 (UC) received standard treatment for 28 days. Patients from group B 2 (CD) were on a gluten-free diet. Results: Oral butyrate plus inulin (as supplement for 28 days) significantly enhanced fecal butyrate-producing bacteria (with a butyryl coenzyme A: acetate-CoA transferase gene, but) and significantly reduced elevated baseline Bacteroides fragilis / Faecalibacterium prausnitzii ratio in both (A1 and B 1) groups. Significant changes in gut microbiota in both UC and CD were accompanied by changes in serum levels of some microbial metabolites (reduced levels of anti-inflammatory caproate and glycolate, elevated levels of pro-inflammatory metabolites such as lactate, 2-hydroxyisovalerate, succinate, fumarate, benzoate, p-hydroxyphenylacetate and 3-indoleacetate). Butyrate plus inulin significantly lowered serum levels of pro-inflammatory succinic acid (in both UC and CD patients) and 2-hydroxyisovaleric acid (in CD). In total, 85 % of UC patients in group A1 (Zacofalk NMX) demonstrated significant improvement in both rectal bleeding and stool frequency by day 14, compared to 55 % in group A2 (p=0.048; Fisher’s exact test). Consumption of Zacofalk NMX for 28 days in CD patients (group B 1) improved perception of some clinical syndromes (indigestion and abdominal pain) evaluated by the GSRS: there was a significant decrease in related subscores (from 3.8 to 2.1 for indigestion; from 3.2 to 1.7 for abdominal pain; p<0.05 for both). Butyrate plus inulin significantly improved bloating in CD patients (group B 1) compared with those from group B 2 with GFD only (73 % vs. 29 %; p = 0.006; Fisher’s exact test). Conclusions: In addition to anti-inflammatory and immunomodulatory effects, butyric acid is probably able to exert a prebiotic (butyrogenic) effect, restoring butyrate-producing bacteria in patients with gut dysbiosis associated with chronic inflammation (IBD) or in patients with dysbiosis due to a decrease in dietary fiber intake (GFD). A significant reduction in the Bacteroides fragilis / Faecalibacterium prausnitzii ratio and the lowering of serum level of pro-inflammatory microbial metabolites confirm the effectiveness of metabiotics such as butyrate plus inulin in UC- or CD-associated taxonomic/metabolic dysbiosis. Clinical data also support the use of butyrate plus inulin as supplement to standard treatment in UC or gluten-free diet in CD patients to more rapid improvement in gastrointestinal symptoms.

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The authors declare that there are no conflicts of interest present.