Gastrointestinal tract microbiome changes in intensive care units patients: review

REVIEWS

  • Ivan A. Lisitsa Saint Petersburg State Pediatric Medical University. 2 Lithuania, Saint Petersburg 194100 Russian Federation
  • Yurii S. Aleksandrovich Saint Petersburg State Pediatric Medical University. 2 Lithuania, Saint Petersburg 194100 Russian Federation
  • Anna N. Zavyalova Saint Petersburg State Pediatric Medical University. 2 Lithuania, Saint Petersburg 194100 Russian Federation
  • Irina V. Aleksandrovich North-Western State Medical University named after I.I. Mechnikov. 41 Kirochnaya str., Saint Petersburg 191015 Russian Federation
  • Oleg V. Lisowskii Saint Petersburg State Pediatric Medical University. 2 Lithuania, Saint Petersburg 194100 Russian Federation
  • Polina D. Ignatova Saint Petersburg State Pediatric Medical University. 2 Lithuania, Saint Petersburg 194100 Russian Federation
  • Maria N. Kachalova Saint Petersburg State Budgetary Inpatient Institution of Social Services for the Population, the “House of Social Services “Vmeste””, Saint Petersburg, Russia
Keywords:
желудочно-кишечный тракт микробиом отделения интенсивной терапии microbiome gastrointestinal tract intensive care units

Abstract

Hospitalization in the intensive care unit (ICU) changes the adaptive mechanisms of the patient, which affects his microbiome. Important triggers of microbiome disorders are the severity of the patient’s condition, the lack of oral nutrition and/or artificial nutrition, as well as the duration of stay in the ICU. Intestinal dysbiosis with the development of pathobionts increases the risk of complications and the outcome of the disease. The review includes articles describing changes in the microbiome of the gastrointestinal tract in patients hospitalized in ICU departments. The main changes in the microbiome occurring in different parts of the gastrointestinal tract in patients hospitalized in the ICU are analyzed. Changes in the intestinal microbiome of the oral cavity were detected in patients from the first day of stay in the ICU with an increase in microbial contamination and the release of pathogens of nosocomial infections in the plaque. A direct relationship has been established between the duration of the patient’s stay in the ICU and the depth of changes in the microbiome with the development of pathobiont dominance, regardless of the age and pathology profile of patients. An established risk factor for the development of complications and the onset of an unfavorable outcome is a decrease in the diversity of Firmicutes and the ratio of Firmicutes and Bacteroidetes. The influence of disorders of the functional activity of the intestinal microbiome and metabolism of certain bacterial species on the severity and prognosis of the disease has been determined. The factors influencing changes in the microbiota of newborns and their clinical significance are described. The positive effect of pre-, pro-, synbiotics, and fecal transplantation on the correction of microbiome disorders has been shown. In patients hospitalized in the ICU, pronounced changes in the gastrointestinal microbiome are diagnosed, while there is a relationship between the severity of the condition and a decrease in bacterial diversity and an increased risk of developing multiple organ failure and nosocomial infection. The greatest clinical significance in predicting a fatal outcome is the depletion of Firmicutes and a decrease in the ratio of Firmicutes/Bacteroidetes. The study of changes in the microbiome can be useful in the early diagnosis of nosocomial infection in critically ill patients and in predicting the risk of outcome.

References

Александрович Ю.С., Иванов Д.О., Павловская Е.Ю. и др. Особенности микробиоты у новорожденных в критическом состоянии при поступлении в ОРИТ специализированного стационара. Вестник анестезиологии и реаниматологии. 2022;19(2):56–63. DOI: 10.21292/2078-5658-2022-19-2-56-63.

Ахмедов В.А., Кашева К.А., Гаус О.В. Микробиота кишечника и критические состояния. Медицинский алфавит. 2020;(37):16–20. DOI: 10.33667/2078-5631-2020-37-16-20.

Белобородова Н.В., Черневская Е.А. Перспективы микробиота-ориентированной терапии в нейрореабилитологии. Физическая и реабилитационная медицина, медицинская реабилитация. 2020;2(1):79–85. DOI: 10.36425/rehab19432.

Гостимский А.В., Гавщук М.В., Завьялова А.Н., Барсукова И.М., Найденов А.А., Карпатский И.В., Петросян А.А., Лисовский О.В. Особенности нутритивной поддержки и ухода за пациентами с гастростомой. Медицина: теория и практика. 2018;3(2):3–10.

Завьялова А.Н., Новикова В.П., Игнатова П.Д. Ось «микробиота–мышцы». Экспериментальная и клиническая гастроэнтерология. 2022;207(11):60–69. DOI: 10.31146/1682-8658-ecg-207-11-60-69.

Завьялова А.Н., Новикова В.П., Кузнецова Ю.В. и др. База данных «Секвенирование 16SrRNK микробиома из трех биотопов у гастростомированного пациента детского возраста». Заявка № 2023620378 от 13.02.2023. Дата государственной регистрации в Реестре баз данных 22.03.2023.

Завьялова А.Н., Новикова В.П., Орел В.И. и др. Организация питания стомированного пациента. Выбор пищевого субстрата. Педиатр. 2023;14(2);93–104. DOI: 10.17816/PED14293-104.

Кузнецова Ю.В., Завьялова А.Н., Давлетова Л.А. и др. Микробиом ротовой полости у детей, питающихся через гастростому. Forcipe. 2022;5(S2):285–286.

Кузнецова Ю.В., Завьялова А.Н., Лисовский О.В. и др. Мик­робиом ротовой полости у пациентов, питающихся через гастростому. Профилактическая и клиническая медицина. 2023;87(2):68–76. DOI: 10.47843/2074-9120_2023_2_68.

Кузнецова Ю.В., Завьялова А.Н., Лисовский О.В. и др. Особенности микробного пейзажа желудка у детей, питающихся через гастростому или назогастральный зонд. Педиатр. 2023;14(2):17–27. DOI: 10.17816/PED14217-27.

Лисица И.А., Александрович Ю.С., Завьялова А.Н. и др. Дисфагия у пациентов педиатрических отделений реанимации и интенсивной терапии (обзор литературы). Вестник анестезиологии и реаниматологии. 2023;20(6):97–105. DOI: 10.24884/2078-5658-2022-20-6-97-105.

Лисица И.А., Завьялова А.Н., Игнатова П.Д., Макарова Т.Ю. Микробиом пациентов в отделении реанимации и интенсивной терапии. Обзор литературы. Университетский терапевтический вестник. 2024;6(3):5–18. DOI: 10.56871/UTJ.2024.67.59.001

Марковская И.Н. Микробиом ребенка первого года жизни, длительно находящегося в условиях ОРИТ, по данным секвенирования 16S rRNA. Тезисы X общеросс. конф. с междунар. участием «FLORES VITAE. Поликлиническая педиатрия». 2022:16–17.

Набока Ю.Л., Рымашевский А.Н., Свирава Э.Г. и др. Становление микробиоты толстого кишечника новорожденных при различных способах родоразрешения. Педиатр. 2014;5(3):22–29. DOI: 10.17816/PED5322-29.

Новикова В.П., Гурова М.М., Хавкин А.И. Кишечная микробиота как регулятор работы органов и систем человека. М.: ГЭОТАР-Медиа; 2024. DOI: 10.33029/9704-8174-5-IMR-2024-1-352.

Новикова В.П., Хавкин А.И., Горелов А.В. и др. Ось «легкие–кишечник» и COVID- инфекция. Инфекционные болезни. 2021;19(1):91–96. DOI: 10.20953/1729-9225-2021-1-91-96.

Прокопьева Н.Э., Новикова В.П., Хавкин А.И. Ось «кишечная микробиота–почки». Особенности при заболеваниях мочевыделительной системы и урогенитального тракта. Медицина: теория и практика. 2022;7(4):68–77. DOI: 10.56871/MTP.2022.51.41.008.

Хавкин А.И., Завьялова А.Н., Новикова В.П. Влияние нутриентов на микробиоту кишечника. Вопросы детской диетологии. 2023;21(1):66–75. DOI: 10.20953/1727-5784-2023-1-66-75.

Черневская Е.А., Белобородова Н.В. Микробиота кишечника при критических состояниях (обзор). Общая реаниматология. 2018;14(5):96–119. DOI: 10.15360/1813-9779-2018-5-96-119.

Шаповалова Н.С., Новикова В.П. Ось «кишечник–мозг» и ее роль в развитии функциональных гастроинтестинальных ­расстройств. Children’s Medicine of the North-West. 2021;9(4):33–51.

Aardema H., Lisotto P., Kurilshikov A. et al. Marked changes in gut microbiota in cardio-surgical intensive care patients: a longitudinal cohort study. Front. Cell. Infect. Microbiol. 2020;9:467. DOI: 10.3389/fcimb.2019.00467.

Akrami K., Sweeney D.A. The microbiome of the critically ill patient. Curr. Opin. Crit. Care. 2018;24(1):49–54. DOI: 10.1097/MCC.0000000000000469.

Bansal S., Nguyen J.P., Leligdowicz A. et al. Rectal and naris swabs: practical and informative samples for analyzing the mic­robiota of critically ill patients. mSphere. 2018;3(3):e00219-18. DOI: 10.1128/mSphere.00219-18.

Bender J.M., Li F., Purswani H. et al. Early exposure to antibiotics in the neonatal intensive care unit alters the taxonomic and functional infant gut microbiome. J Matern Fetal Neonatal Med. 2021;34(20):3335–3343. DOI: 10.1080/14767058.2019.1684466.

Buelow E., Bello González T.D.J., Fuentes S. et al. Comparative gut microbiota and resistome profiling of intensive care patients receiving selective digestive tract decontamination and healthy subjects. Microbiome. 2017;5(1):88. DOI: 10.1186/s40168-017-0309-z.

Caldarelli M., Franza L., Rio P. et al. Gut-kidney-heart: a novel trilogy. Biomedicines. 2023;11(11):3063. DOI: 10.3390/biomedicines11113063.

Chanderraj R., Baker J.M., Kay S.G. et al. In critically ill patients, anti-anaerobic antibiotics increase risk of adverse clinical outcomes. Eur Respir J. 2023;61(2):2200910. DOI: 10.1183/13993003.00910-2022.

Chapple L.A., Deane A. From dysmotility to virulent pathogens: implications of opioid use in the ICU. Curr Opin Crit Care. 2018;24(2):118–123. DOI: 10.1097/MCC.0000000000000487.

Chapple L.S., Plummer M.P., Chapman M.J. Gut dysfunction in the ICU: diagnosis and management. Curr Opin Crit Care. 2021;27(2):141–146. DOI: 10.1097/MCC.0000000000000813.

D'Agata A.L., Wu J., Welandawe M.K.V. et al. Effects of early life NICU stress on the developing gut microbiome. Dev Psychobiol. 2019;61(5):650–660. DOI: 10.1002/dev.21826.

Dahlgren A.F., Pan A., Lam V. et al. Longitudinal changes in the gut microbiome of infants on total parenteral nutrition. Pediatr Res. 2019;86(1):107–114. DOI: 10.1038/s41390-019-0391-y.

Elfiky S.A., Mahmoud Ahmed S., Elmenshawy A.M. et al. Study of the gut microbiome as a novel target for prevention of hospital-associated infections in intensive care unit patients. Acute Crit Care. 2023;38(1):76–85. DOI: 10.4266/acc.2022.01116.

Fida M., Wolf M.J., Hamdi A. et al. Detection of pathogenic bacteria from septic patients using 16S ribosomal RNA gene-targeted metagenomic sequencing. Clin Infect Dis. 2021;73(7):1165–1172. DOI: 10.1093/cid/ciab349.

Freedberg D.E., Zhou M.J., Cohen M.E. et al. Pathogen colonization of the gastrointestinal microbiome at intensive care unit admission and risk for subsequent death or infection. Intensive Care Med. 2018;44(8):1203–1211. DOI: 10.1007/s00134-018-5268-8.

Haak B.W., Argelaguet R., Kinsella C.M. et al. Integrative Trans­kingdom analysis of the gut microbiome in antibiotic pertur­bation and critical illness. mSystems. 2021;6(2):e01148–20. DOI: 10.1128/mSystems.01148-20.

Howard B.M., Kornblith L.Z., Christie S.A. et al. Characterizing the gut microbiome in trauma: significant changes in microbial diversity occur early after severe injury. Trauma Surg Acute Care Open. 2017;2(1):e000108. DOI: 10.1136/tsaco-2017-000108.

Iapichino G., Callegari M.L., Marzorati S. et al. Impact of antibio­tics on the gut microbiota of critically ill patients. J Med Microbiol. 2008;57(Pt 8):1007–1014. DOI: 10.1099/jmm.0.47387-0.

Kuznetsova Yu.V., Zavyalova A.N., Dudurich V.V. The microbiome of the stomach in children fed through a gastrostomy. World of Microbiome. Vienna: Kenes group; 2022: 104.

Lamoureux C., Surgers L., Fihman V. et al. Prospective comparison between shotgun metagenomics and sanger sequencing of the 16S rRNA gene for the etiological diagnosis of infections. Front Microbiol. 2022;13:761873. DOI: 10.3389/fmicb.2022.761873.

Lankelma J.M., van Vught L.A., Belzer C. et al. Critically ill patients demonstrate large interpersonal variation in intestinal microbiota dysregulation: a pilot study. Intensive Care Med. 2017;43(1):59-68. DOI: 10.1007/s00134-016-4613-z.

Limketkai B.N., Hendler S., Ting P.S. et al. Fecal microbiota transplantation for the critically ill patient. Nutr Clin Pract. 2019;34(1):73–79. DOI: 10.1002/ncp.10228.

Liu W., Cheng M., Li J. et al. Classification of the gut microbiota of patients in intensive care units during development of sepsis and septic shock. Genomics Proteomics Bioinformatics. 2020;18(6):696–707. DOI: 10.1016/j.gpb.2020.06.011.

McDonald D., Ackermann G., Khailova L. et al. Extreme dysbiosis of the microbiome in critical illness. mSphere. 2016;1(4):e00199-16. DOI: 10.1128/mSphere.00199-16.

Mustansir Dawoodbhoy F., Patel B.K., Patel K. et al. Gut microbiota dysbiosis as a target for improved post-surgical outcomes and improved patient care: a review of current literature. Shock. 2021;55(4):441–454. DOI: 10.1097/SHK.0000000000001654.

Ojima M., Motooka D., Shimizu K. et al. Metagenomic analysis reveals dynamic changes of whole gut microbiota in the acute phase of intensive care unit patients. Dig Dis Sci. 2016;61(6):1628–1634. DOI: 10.1007/s10620-015-4011-3.

Ojima M., Shimizu K., Motooka D. et al. Gut dysbiosis associated with antibiotics and disease severity and its relation to mortality in critically ill patients. Dig Dis Sci. 2022;67(6):2420–2432. DOI: 10.1007/s10620-021-07000-7.

Paul B. Concatenated 16S rRNA sequence analysis improves bacterial taxonomy. F1000Res. 2023;11:1530.DOI: 10.12688/f1000research.128320.3.

Ravi A., Halstead F.D., Bamford A. et al. Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients. Microb Genom. 2019;5(9):e000293. DOI: 10.1099/mgen.0.000293.

Reis A.M.D., Fruchtenicht A.V., Loss S.H. et al. Use of die­tary ­fibers in enteral nutrition of critically ill patients: a systematic review. Rev Bras Ter Intensiva. 2018;30(3):358–365. DOI: 10.5935/0103-507X.20180050.

Sachdev M., Ready D., Brealey D. et al. Changes in dental plaque following hospitalisation in a critical care unit: an observational study. Crit Care. 2013;17(5):R189. DOI: 10.1186/cc12878.

Sanschagrin S., Yergeau E. Next-generation sequencing of 16S ribosomal RNA gene amplicons. J Vis Exp. 2014;90:51709. DOI: 10.3791/51709.

Seifi N., Jafarzadeh Esfahani A., Sedaghat A. et al. Effect of gut mic­robiota modulation on feeding tolerance of enterally fed critically ill adult patients: a systematic review. Syst Rev. 2021;10(1):95. DOI: 10.1186/s13643-021-01633-5.

de Sire A., de Sire R., Curci C. et al. Role of dietary supplements and probiotics in modulating microbiota and bone health: the gut-bone axis. Cells. 2022;11(4):743. DOI: 10.3390/cells11040743.

Shimizu K., Yamada T., Ogura H. et al. Synbiotics modulate gut microbiota and reduce enteritis and ventilator-associated pneumonia in patients with sepsis: a randomized controlled trial. Crit Care. 2018;22(1):239. DOI: 10.1186/s13054-018-2167-x.

Tauchi H., Yahagi K., Yamauchi T. et al. Gut microbiota development of preterm infants hospitalised in intensive care units. Benef Microbes. 2019;10(6):641–651. DOI: 10.3920/BM2019.0003.

Watts G.S., Youens-Clark K., Slepian M.J. et al. 16S rRNA gene sequencing on a benchtop sequencer: accuracy for identification of clinically important bacteria. J Appl Microbiol. 2017;123(6):1584–1596. DOI: 10.1111/jam.13590.

Wei R., Chen X., Hu L. et al. Dysbiosis of intestinal microbiota in critically ill patients and risk of in-hospital mortality. Am J Transl Res. 2021;13(3):1548–1557.

Wijeyesekera A., Wagner J., De Goffau M. et al. Multi-com- partment profiling of bacterial and host metabolites identifies intestinal dysbiosis and its functional consequences in the critically ill child. Crit Care Med. 2019;47(9):e727–e734. DOI: 10.1097/CCM.0000000000003841.

Wischmeyer P.E., McDonald D., Knight R. Role of the microbiome, probiotics, and 'dysbiosis therapy' in critical illness. Curr Opin Crit Care. 2016;22(4):347–353. DOI: 10.1097/MCC.0000000000000321.

Xu R., Tan C., He Y. et al. Dysbiosis of gut microbiota and short-chain fatty acids in encephalitis: a chinese pilot study. Front Immunol. 2020;11:1994. DOI: 10.3389/fimmu.2020.01994.

Xu R., Tan C., Zhu J. et al. Dysbiosis of the intestinal microbiota in neurocritically ill patients and the risk for death. Crit Care. 2019;23(1):195. DOI: 10.1186/s13054-019-2488-4.

Yap P.S.X., Chong C.W., Ahmad Kamar A. et al. Neonatal intensive care unit (NICU) exposures exert a sustained influence on the progression of gut microbiota and metabolome in the first year of life. Sci Rep. 2021;11(1):1353. DOI: 10.1038/s41598-020-80278-1.

Zanza C., Romenskaya T., Thangathurai D. et al. Microbiome in critical illness: an unconventional and unknown ally. Curr Med Chem. 2021;29(18):3179–3188. DOI: 10.2174/0929867328666210915115056.