epidemiologyЭпидемиология и ВакцинопрофилактикаEpidemiology and Vaccinal Prevention2073-30462619-0494«Numicom» LLC10.31631/2073-3046-2024-23-6-83-103epidemiology-2125Research ArticleПРАКТИЧЕСКИЕ АСПЕКТЫ ЭПИДЕМИОЛОГИИ И ВАКЦИНОПРОФИЛАКТИКИPRACTICAL ASPECTS OF EPIDEMIOLOGY AND VACCINE PREVENTIONРаспространенность и факторы риска колонизации карбапенемрезистентными микроорганизмами у пациентов, поступающих в многопрофильный стационарPrevalence and Risk Factors for Colonization with Carbapenem-Resistant Microorganisms in Patients Admitted to a Multidisciplinary Hospitalhttps://orcid.org/0000-0003-0994-0579НиО. Г.NiO. G.

Оксана Геннадьевна Ни – заведующая отделением клинической фармакологии – врач–клинический фармаколог

Москва

+7 (918) 182–20–27

Oksana G. Ni – Head of the Department of Clinical Pharmacology – Clinical Pharmacologist

+7 (918) 182–20–27

ni.oksana@gmail.comhttps://orcid.org/0000-0002-5758-5703БелоцерковскийБ. З.BelotserkovskiyB. Z.

Борис Зиновьевич Белоцерковский – заведующий отделением реанимации и интенсивной терапии №5 – врач–анестезиолог–реаниматолог; доцент кафедры анестезиологии и реаниматологии

Москва

+7 (916) 266–99–01

Boris Z. Belotserkovskiy – Head of the Intensive Care Unit No. 5 – Anesthesiologist–Intensivist; Associate Professor of the Department of Anesthesiology and Intensive Care at the Faculty of Continuing Professional Education of the Institute of Lifelong Learning and Professional Development

+7 (916) 266–99–01

belotserkovskii@mail.ruhttps://orcid.org/0000-0001-6849-0008КругловА. Н.KruglovA. N.

Александр Николаевич Круглов – заведующий лабораторией клинической микробиологии – врач–бактериолог

Москва

+7 (910) 460–33–56

Aleksander N. Kruglov – Head of the Clinical Microbiology Laboratory – Medical Bacteriologist

+7 (910) 460–33–56

kruglov_a_n@mail.ruhttps://orcid.org/0009-0004-0764-4658МатяшМ. И.MatyashM. I.

Максим Игоревич Матяш – врач-анестезиолог–реаниматолог

Москва

+7 (905) 656–69–38

Maksim Ig. Matyash – Anesthesiologist-Intensivist

+7 (905) 656–69–38

https://orcid.org/0000-0001-5244-7769БыковА. О.BykovA. O.

Андрей Олегович Быков – врач-анестезиолог–реаниматолог; ассистент кафедры анестезиологии и реаниматологии

Москва

+7 (925) 634–22–24

Andrey O. Bykov – Anesthesiologist–Intensivist; Assistant Professor of the Department of Anesthesiology and Intensive Care at the Faculty of Continuing Professional Education of the Institute of Lifelong Learning and Professional Development

+7 (925) 634–22–24

bykoff-87@mail.ruhttps://orcid.org/0000-0001-7606-8608ЯковлевС. В.YakovlevS. V.

Сергей Владимирович Яковлев – профессор кафедры госпитальной терапии №2; врач-клинический фармаколог

Москва

+7 (916) 681–91–92

Sergey V. Yakovlev– Professor of the Department of Hospital Therapy No. 2; Clinical Pharmacologist

+7 (916) 681–91–92

antimicrob@yandex.ruhttps://orcid.org/0000-0002-6113-8498ШифманЕ. М.ShifmanE. M.

Ефим Муневич Шифман – профессор кафедры анестезиологии и реаниматологии; профессор кафедры анестезиологии и реаниматологии

Москва

+7 (925) 072–60–75

Efim M. Shifman – Professor of the Department of Anesthesiology and Intensive Care at the Faculty of Continuing Professional Education of the Institute of Lifelong Learning and Professional Development; Professor of the Department of Anesthesiology and Intensive Care at the Faculty for Postgraduate Training of Physicians

+7 (925) 072–60–75

eshifman@mail.ruhttps://orcid.org/0000-0002-5166-3280ПроценкоД. Н.ProtsenkoD. N.

Денис Николаевич Проценко – директор, ГБУЗ города Москвы; заведующий кафедрой анестезиологии и реаниматологии

Москва

+7 (909) 901–30–30

Denis N. Protsenko – Director; Head of the Department of Anesthesiology and Intensive Care at the Faculty of Continuing Professional Education of the Institute of Lifelong Learning and Professional Development

+7 (909) 901–30–30

drprotsenko@gmail.comГБУЗ г. Москвы «Московский многопрофильный клинический центр «Коммунарка» Департамента здравоохранения города Москвы»РоссияMoscow City Multi-field Clinical Center «Kommunarka»Russian FederationГБУЗ г. Москвы «Московский многопрофильный клинический центр «Коммунарка» Департамента здравоохранения города Москвы»; ФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н. И. Пирогова» Минздрава РоссииРоссияMoscow City Multi-field Clinical Center «Kommunarka»; Pirogov National Research Medical UniversityRussian FederationГБУЗ г. Москвы «Московский многопрофильный клинический центр «Коммунарка» Департамента здравоохранения города Москвы»; ФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н. И. Пирогова» Минздрава РоссииРоссияMoscow City Multi-field Clinical Center «Kommunarka»; Pirogov National Research Medical UniversityRussian FederationФГАОУ ВО «Первый МГМУ им. И. М. Сеченова» Минздрава России (Сеченовский Университет); ГБУЗ г. Москвы «Городская клиническая больница имени С. С. Юдина Департамента здравоохранения города Москвы»РоссияSechenov University; City clinical hospital named after S. S. YudinRussian FederationФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н. И. Пирогова» Минздрава России; ГБУЗ МО МОНИКИ им. М. Ф. ВладимирскогоРоссияPirogov National Research Medical University; Moscow Regional Research Clinical InstituteRussian Federation20241401202523683103Copyright © Ни О.Г., Белоцерковский Б.З., Круглов А.Н., Матяш М.И., Быков А.О., Яковлев С.В., Шифман Е.М., Проценко Д.Н., 20252025Ни О.Г., Белоцерковский Б.З., Круглов А.Н., Матяш М.И., Быков А.О., Яковлев С.В., Шифман Е.М., Проценко Д.Н.Ni O.G., Belotserkovskiy B.Z., Kruglov A.N., Matyash M.I., Bykov A.O., Yakovlev S.V., Shifman E.M., Protsenko D.N.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.epidemvac.ru/jour/article/view/2125

Актуальность. В последнее десятилетие возрастает распространенность антибиотикорезистентных микроорганизмов во внебольничной среде. Колонизация и бессимптомное носительство продуцентов бета-лактамаз расширенного спектра и карбапенемаз могут быть предпосылкой к развитию инфекционного процесса и существенным фактором патогенеза инфекций, связанных с оказанием медицинской помощи. Понимание факторов риска внебольничной колонизации антибиотикорезистентными микроорганизмами необходимо для проведения целенаправленного скрининга и своевременного принятия мер по предотвращению распространения резистентности в стационаре.Цель. Определить значимые факторы риска колонизации антибиотикорезистентными грамотрицательными микроорганизмами и носительства генов устойчивости к карбапенемам у пациентов, поступающих в многопрофильный стационар.Материалы и методы. Проспективное одноцентровое исследование методом поперечных срезов проводилось в Московском многопрофильном клиническом центре «Коммунарка» с 15.09.2022 г. по 15.08.2023 г. Включены 733 пациента в возрасте от 18 до 94 лет. Образцы биоматериала брались из прямой кишки, верхних и нижних дыхательных путей. Полученный биоматериал исследовали методом полимеразной цепной реакции с гибридизационно-флуоресцентной детекцией продуктов амплификации (ПЦР в реальном времени) для выявления генов карбапенемаз и культуральным методом для определения колонизации карбапенемрезистентными бактериями. Идентификацию выделенных микроорганизмов проводили с помощью метода времяпролетной масс-спектрометрии с матрично-активированной лазерной десорбцией/ионизацией (MALDI-TОF MS), чувствительность к антибактериальным препаратам определяли методом диск-диффузии в агар на среде Мюллер-Хинтон по Кирби-Бауэру. Результаты определения чувствительности выделенных возбудителей интерпретировали на основании критериев EUCAST v12.0, v13.0, v13.1.Результаты и обсуждение. Носительство генов карбапенемаз выявлено у 12,6% пациентов, поступивших в стационар, колонизация карбапенемрезистентными бактериями – у 2,7%. У большинства пациентов (66,7%) единственным локусом носительства генов была прямая кишка. При этом лишь у 18,1% из них была выявлена колонизация прямой кишки бактериями, устойчивыми к карбапенемам. Указанное несовпадение, вероятно, обусловлено большей чувствительностью молекулярно-генетических методов по сравнению с культуральными, а с позиций клинической медицины определение нуклеиновых кислот методом ПЦР может служить эквивалентом обнаружения возбудителя в биоматериале. Многофакторный анализ выявил 5 независимых предикторов колонизации: прием цитостатиков, перевод из другого стационара, потребность в вазопрессорной поддержке, прием антибиотиков в предшествующие 3 месяца и мужской пол.Выводы. Выявленные факторы риска позволяют выделить когорту пациентов высокого риска для целенаправленного скрининга с целью своевременного назначения адекватной антибактериальной терапии и принятия мер по профилактике распространения карбапенемрезистентности в стационаре.

Relevance. In the last decade, there has been an increase in the isolation of antibiotic-resistant microorganisms in community settings. Colonization and asymptomatic carriage of extended-spectrum beta-lactamase and carbapenemase producers can be a precursor to the development of an infectious process and a significant factor in the pathogenesis of healthcare-associated infections. Understanding the risk factors for community-acquired colonization with antibiotic-resistant microorganisms is necessary for targeted screening and timely implementation of measures to prevent the spread of resistance in hospitals.The aim. To determine significant risk factors for colonization with antibiotic-resistant gram-negative microorganisms and carriage of carbapenem resistance genes in patients admitted to a multidisciplinary hospital.Materials & Methods. A prospective single-center crosssectional study was conducted at the Moscow Multidisciplinary Clinical Center «Kommunarka» from 15.09.2022 to 15.08.2023. The study included 733 patients aged 18 to 94 years. Biological samples were taken from the rectum, upper and lower respiratory tract. The obtained samples were examined by real-time polymerase chain reaction (PCR) with hybridization-fluorescent detection of amplification products to identify carbapenemase genes and by culture method to determine colonization with carbapenemresistant bacteria. Identification of isolated microorganisms was performed using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS), and antibiotic susceptibility was determined by the Kirby-Bauer disk diffusion method on Mueller-Hinton agar. The results of susceptibility testing were interpreted based on EUCAST v12.0, v13.0, and v13.1 criteria.Results. Carriage of carbapenemase genes was detected in 12.6% of patients admitted to the hospital, while colonization with carbapenem-resistant bacteria was found in 2.7%. In the majority of patients (66.7%), the rectum was the only site of gene carriage. However, only 18.1% of these patients showed rectal colonization with carbapenem-resistant bacteria. This discrepancy is likely due to the higher sensitivity of molecular genetic methods compared to culture-based techniques. From a clinical perspective, the detection of nucleic acids by PCR can serve as an equivalent to pathogen detection in biological material. Multivariate analysis identified 5 independent predictors of colonization: cytostatic therapy, transfer from another hospital, need for vasopressor support, antibiotic use in the previous 3 months, and male gender.Conclusion. The identified risk factors allow for the identification of a highrisk patient cohort for targeted screening, enabling timely administration of appropriate antibiotic therapy and implementation of measures to prevent the spread of carbapenem resistance in the hospital.

карбапенемрезистентностьколонизацияэпидемиологиякарбапенемазыантибиотикорезистентностьфакторы риска Конфликт интересов не заявленcarbapenem-resistanceсolonizationepidemiologycarbapenemasesantimicrobial resistancerisk factors No conflict of interest to declareReferencesWorld Health Organization. WHO publishes list of bacteria for which new antibiotics are urgently needed. [Internet] Available at: https://www.who.int/news/item/27–02–2017–who–publishes–list–of–bacteria–for–which–new–antibiotics–are–urgently–needed. Accessed: 5 Aug 2024.World Health Organization. WHO publishes list of bacteria for which new antibiotics are urgently needed. [Internet] Available at: https://www.who.int/news/item/27–02–2017–who–publishes–list–of–bacteria–for–which–new–antibiotics–are–urgently–needed. Accessed: 5 Aug 2024.Козлов Р. С., Кузьменков А. Ю., Виноградова А. Г. Антибиотикорезистентность как медицинская проблема. Вестник Российской академии наук. 2024. – Т. 94. – №1. – C. 11–18.Kozlov RS, Kuzmenkov AY, Vinogradova AG. Antibiotic resistance as a medical problem. Vestnik Rossijskoj akademii nauk. 2024;94(1):11–18 (In Russ). doi: 10.31857/S0869587324010033Falagas ME, Tansarli GS, Karageorgopoulos DE, et al. Deaths Attributable to Carbapenem–Resistant Enterobacteriaceae Infections. Emerging Infectious Diseases. 2014;20(7):1170–1175. doi:10.3201/eid2007.121004.Falagas ME, Tansarli GS, Karageorgopoulos DE, et al. Deaths Attributable to Carbapenem–Resistant Enterobacteriaceae Infections. Emerging Infectious Diseases. 2014;20(7):1170–1175. doi:10.3201/eid2007.121004.Otter JA, Burgess P, Davies F, et al. Counting the cost of an outbreak of carbapenemase–producing Enterobacteriaceae: an economic evaluation from a hospital perspective. Clin Microbiol Infect. 2017;23(3):188–196. doi:10.1016/j.cmi.2016.10.005Otter JA, Burgess P, Davies F, et al. Counting the cost of an outbreak of carbapenemase–producing Enterobacteriaceae: an economic evaluation from a hospital perspective. Clin Microbiol Infect. 2017;23(3):188–196. doi:10.1016/j.cmi.2016.10.005Cerceo E, Deitelzweig SB, Sherman BM, et al. Multidrug–Resistant Gram–Negative Bacterial Infections in the Hospital Setting: Overview, Implications for Clinical Practice, and Emerging Treatment Options. Microb Drug Resist. 2016;22(5):412–431. doi:10.1089/mdr.2015.0220Cerceo E, Deitelzweig SB, Sherman BM, et al. Multidrug–Resistant Gram–Negative Bacterial Infections in the Hospital Setting: Overview, Implications for Clinical Practice, and Emerging Treatment Options. Microb Drug Resist. 2016;22(5):412–431. doi:10.1089/mdr.2015.0220Devi LS, Broor S, Rautela RS, et al. Increasing Prevalence of Escherichia coli and Klebsiella pneumoniae Producing CTX–M–Type Extended–Spectrum Beta–Lactamase, Carbapenemase, and NDM–1 in Patients from a Rural Community with Community Acquired Infections: A 3–Year Study. Int J Appl Basic Med Res. 2020;10(3):156–163. doi:10.4103/ijabmr.IJABMR_360_19Devi LS, Broor S, Rautela RS, et al. Increasing Prevalence of Escherichia coli and Klebsiella pneumoniae Producing CTX–M–Type Extended–Spectrum Beta–Lactamase, Carbapenemase, and NDM–1 in Patients from a Rural Community with Community Acquired Infections: A 3–Year Study. Int J Appl Basic Med Res. 2020;10(3):156–163. doi:10.4103/ijabmr.IJABMR_360_19Dickstein Y, Edelman R, Dror T, et al. Carbapenem–resistant Enterobacteriaceae colonization and infection in critically ill patients: a retrospective matched cohort comparison with non–carriers. J Hosp Infect. 2016;94(1):54–59. doi:10.1016/j.jhin.2016.05.018Dickstein Y, Edelman R, Dror T, et al. Carbapenem–resistant Enterobacteriaceae colonization and infection in critically ill patients: a retrospective matched cohort comparison with non–carriers. J Hosp Infect. 2016;94(1):54–59. doi:10.1016/j.jhin.2016.05.018McConville TH, Sullivan SB, Gomez–Simmonds A, et al. Carbapenem–resistant Enterobacteriaceae colonization (CRE) and subsequent risk of infection and 90–day mortality in critically ill patients, an observational study. PLoS One. 2017;12(10):e0186195. doi:10.1371/journal.pone.0186195McConville TH, Sullivan SB, Gomez–Simmonds A, et al. Carbapenem–resistant Enterobacteriaceae colonization (CRE) and subsequent risk of infection and 90–day mortality in critically ill patients, an observational study. PLoS One. 2017;12(10):e0186195. doi:10.1371/journal.pone.0186195Emmanuel Martinez A, Widmer A, Frei R, et al. ESBL–colonization at ICU admission: impact on subsequent infection, carbapenem-consumption, and outcome. Infect Control Hosp Epidemiol. 2019;40(4):408–413. doi:10.1017/ice.2019.5Emmanuel Martinez A, Widmer A, Frei R, et al. ESBL–colonization at ICU admission: impact on subsequent infection, carbapenem-consumption, and outcome. Infect Control Hosp Epidemiol. 2019;40(4):408–413. doi:10.1017/ice.2019.5Golzarri MF, Silva–Sánchez J, Cornejo–Juárez P, et al. Colonization by fecal extended–spectrum β-lactamase–producing Enterobacteriaceae and surgical site infections in patients with cancer undergoing gastrointestinal and gynecologic surgery. Am J Infect Control. 2019;47(8):916–921. doi:10.1016/j.ajic.2019.01.020Golzarri MF, Silva–Sánchez J, Cornejo–Juárez P, et al. Colonization by fecal extended–spectrum β-lactamase–producing Enterobacteriaceae and surgical site infections in patients with cancer undergoing gastrointestinal and gynecologic surgery. Am J Infect Control. 2019;47(8):916–921. doi:10.1016/j.ajic.2019.01.020Massart N, Camus C, Benezit F, et al. Incidence and risk factors for acquired colonization and infection due to extended-spectrum beta–lactamase–producing Gram–negative bacilli: a retrospective analysis in three ICUs with low multidrug resistance rate. Eur J Clin Microbiol Infect Dis. 2020;39(5):889–895. doi:10.1007/s10096–019–03800–yMassart N, Camus C, Benezit F, et al. Incidence and risk factors for acquired colonization and infection due to extended-spectrum beta–lactamase–producing Gram–negative bacilli: a retrospective analysis in three ICUs with low multidrug resistance rate. Eur J Clin Microbiol Infect Dis. 2020;39(5):889–895. doi:10.1007/s10096–019–03800–yEUCAST. Clinical breakpoints – breakpoints and guidance. Archive of EUCAST tables and documents. [Internet]. Available at: https://www.eucast.org/ast_of_bacteria/previous_versions_of_documents. Accessed: 5 Aug 2024.EUCAST. Clinical breakpoints – breakpoints and guidance. Archive of EUCAST tables and documents. [Internet]. Available at: https://www.eucast.org/ast_of_bacteria/previous_versions_of_documents. Accessed: 5 Aug 2024.About Carbapenem–resistant Enterobacterales. [Internet]. Available at: https://www.cdc.gov/cre/about/index.html. Accessed: 5 Aug 2024.About Carbapenem–resistant Enterobacterales. [Internet]. Available at: https://www.cdc.gov/cre/about/index.html. Accessed: 5 Aug 2024.Эйдельштейн М. В. Выявление β лактамаз расширенного спектра у грамотрицательных бактерий с помощью фенотипических методов. Клиническая Микробиология-Антимикробная Химиотерапия. 2001. Т.3, № 2. С. 183–189.Edelstein MV. Detection of Extended Spectrum β–lactamases by Phenotypic Methods in Gram–negative Bacteria. Kliniceskaa Mikrobiologia i Antimikrobnaa Himioterapia. 2001;3(2): 183–189. (In Russ).Hu Y, Qing Y, Chen J, et al. Prevalence, Risk Factors, and Molecular Epidemiology of Intestinal Carbapenem–Resistant Pseudomonas aeruginosa. Microbiol Spectr. 2021;9(3):e0134421. doi:10.1128/Spectrum.01344–21Hu Y, Qing Y, Chen J, et al. Prevalence, Risk Factors, and Molecular Epidemiology of Intestinal Carbapenem–Resistant Pseudomonas aeruginosa. Microbiol Spectr. 2021;9(3):e0134421. doi:10.1128/Spectrum.01344–21Программа СКАТ (Стратегия контроля антимикробной терапии) при оказании стационарной медицинской помощи. Российские клинические рекомендации. С. В. Яковлев, Н. И. Брико, С. В. Сидоренко и др., ред. М.: Перо; 2018.Ed.: Yakovlev S.V., Briko N.I., Sidorenko S.V., et al. AMS program (Strategy for the Control of Antimicrobial Therapy) in the provision of inpatient medical care. Russian clinical guidelines. Moscow: Pero; 2018 (In Russ).Yan L, Sun J, Xu X, Huang S. Epidemiology and risk factors of rectal colonization of carbapenemase–producing Enterobacteriaceae among high risk patients from ICU and HSCT wards in a university hospital. Antimicrob Resist Infect Control. 2020;9(1):155. doi:10.1186/s13756–020–00816–4Yan L, Sun J, Xu X, Huang S. Epidemiology and risk factors of rectal colonization of carbapenemase–producing Enterobacteriaceae among high risk patients from ICU and HSCT wards in a university hospital. Antimicrob Resist Infect Control. 2020;9(1):155. doi:10.1186/s13756–020–00816–4Kim HJ, Hyun J, Jeong HS, et al. Epidemiology and Risk Factors of Carbapenemase–Producing Enterobacteriaceae Acquisition and Colonization at a Korean Hospital over 1 Year. Antibiotics (Basel). 2023;12(4):759. doi:10.3390/antibiotics12040759Kim HJ, Hyun J, Jeong HS, et al. Epidemiology and Risk Factors of Carbapenemase–Producing Enterobacteriaceae Acquisition and Colonization at a Korean Hospital over 1 Year. Antibiotics (Basel). 2023;12(4):759. doi:10.3390/antibiotics12040759Rodríguez–Villodres Á, Martín–Gandul C, Peñalva G, et al. Prevalence and Risk Factors for Multidrug–Resistant Organisms Colonization in Long–Term Care Facilities Around the World: A Review. Antibiotics (Basel). 2021;10(6):680. doi:10.3390/antibiotics10060680Rodríguez–Villodres Á, Martín–Gandul C, Peñalva G, et al. Prevalence and Risk Factors for Multidrug–Resistant Organisms Colonization in Long–Term Care Facilities Around the World: A Review. Antibiotics (Basel). 2021;10(6):680. doi:10.3390/antibiotics10060680Kajova M, Khawaja T, Kantele A. European hospitals as source of multidrug–resistant bacteria: analysis of travellers screened in Finland after hospitalization abroad. J Travel Med. 2022;29(4):taac022. doi:10.1093/jtm/taac022Kajova M, Khawaja T, Kantele A. European hospitals as source of multidrug–resistant bacteria: analysis of travellers screened in Finland after hospitalization abroad. J Travel Med. 2022;29(4):taac022. doi:10.1093/jtm/taac022Heinemann M, Kleinjohann L, Rolling T, et al. Impact of antibiotic intake on the incidence of extended–spectrum β-lactamase-producing Enterobacterales in sub-Saharan Africa: results from a community based longitudinal study. Clin Microbiol Infect. 2023;29(3):340–345. doi:10.1016/j.cmi.2022.09.008Heinemann M, Kleinjohann L, Rolling T, et al. Impact of antibiotic intake on the incidence of extended–spectrum β-lactamase-producing Enterobacterales in sub-Saharan Africa: results from a community based longitudinal study. Clin Microbiol Infect. 2023;29(3):340–345. doi:10.1016/j.cmi.2022.09.008Bar Ilan M, Kjerulf A. Who should be screened for carbapenemase–producing Enterobacterales and when? A systematic review. J Hosp Infect. 2023;142:74–87. doi:10.1016/j.jhin.2023.09.018Bar Ilan M, Kjerulf A. Who should be screened for carbapenemase–producing Enterobacterales and when? A systematic review. J Hosp Infect. 2023;142:74–87. doi:10.1016/j.jhin.2023.09.018Мониторинг антибиотикорезистентности с использованием платформы AMRcloud. Практическое руководство. Козлов Р. С., Виноградов А. Г., Кузьменков А. Ю. и др., ред. Смоленск: СГМУ; 2021.Kozlov RS, Vinogradov AG, Kuzmenkov AYu, et al., editors. Monitoring antibiotikorezistentnosti s ispol’zovaniem platformy AMRcloud. Prakticheskoe rukovodstvo. Smolensk: SGMU;2021 (In Russ).Kelly AM, Mathema B, Larson EL. Carbapenem–resistant Enterobacteriaceae in the community: a scoping review. Int J Antimicrob Agents. 2017;50(2):127–134. doi:10.1016/j. ijantimicag.2017.03.012Kelly AM, Mathema B, Larson EL. Carbapenem–resistant Enterobacteriaceae in the community: a scoping review. Int J Antimicrob Agents. 2017;50(2):127–134. doi:10.1016/j. ijantimicag.2017.03.012Garrido A, Seral C, Gude MJ, et al. Characterization of plasmid–mediated β–lactamases in fecal colonizing patients in the hospital and community setting in Spain. Microb Drug Resist. 2014;20(4):301–304. doi:10.1089/mdr.2013.0109Garrido A, Seral C, Gude MJ, et al. Characterization of plasmid–mediated β–lactamases in fecal colonizing patients in the hospital and community setting in Spain. Microb Drug Resist. 2014;20(4):301–304. doi:10.1089/mdr.2013.0109Alexopoulou A, Papadopoulos N, Eliopoulos DG, et al. Increasing frequency of gram–positive cocci and gram–negative multidrug–resistant bacteria in spontaneous bacterial peritonitis. Liver Int. 2013;33(7):975–981. doi:10.1111/liv.12152Alexopoulou A, Papadopoulos N, Eliopoulos DG, et al. Increasing frequency of gram–positive cocci and gram–negative multidrug–resistant bacteria in spontaneous bacterial peritonitis. Liver Int. 2013;33(7):975–981. doi:10.1111/liv.12152Lohiya A, Kant S, Kapil A, et al. Pattern of Antibiotic Resistance Among Community Derived Isolates of Enterobacteriaceae Using Urine Sample: A Study From Northern India. J Clin Diagn Res. 2015;9(7):LC15–LC19. doi:10.7860/JCDR/2015/14230.6254Lohiya A, Kant S, Kapil A, et al. Pattern of Antibiotic Resistance Among Community Derived Isolates of Enterobacteriaceae Using Urine Sample: A Study From Northern India. J Clin Diagn Res. 2015;9(7):LC15–LC19. doi:10.7860/JCDR/2015/14230.6254Henderson J, Ciesielczuk H, Nelson SM, et al. Community prevalence of carbapenemase–producing organisms in East London. J Hosp Infect. 2019;103(2):142–146. doi:10.1016/j.jhin.2019.04.014Henderson J, Ciesielczuk H, Nelson SM, et al. Community prevalence of carbapenemase–producing organisms in East London. J Hosp Infect. 2019;103(2):142–146. doi:10.1016/j.jhin.2019.04.014van den Bunt G, van Pelt W, Hidalgo L, et al. Prevalence, risk factors and genetic characterisation of extended–spectrum beta–lactamase and carbapenemase–producing Enterobacteriaceae (ESBL–E and CPE): a community–based cross–sectional study, the Netherlands, 2014 to 2016. Euro Surveill. 2019;24(41):1800594. doi:10.2807/1560–7917. ES.2019.24.41.1800594van den Bunt G, van Pelt W, Hidalgo L, et al. Prevalence, risk factors and genetic characterisation of extended–spectrum beta–lactamase and carbapenemase–producing Enterobacteriaceae (ESBL–E and CPE): a community–based cross–sectional study, the Netherlands, 2014 to 2016. Euro Surveill. 2019;24(41):1800594. doi:10.2807/1560–7917. ES.2019.24.41.1800594Turnidge JD, Gottlieb T, Mitchell DH, et al. Australian Group on Antimicrobial Resistance Community–onset Gram–negative Surveillance Program annual report, 2010. Commun Dis Intell Q Rep. 2013;37(3):E219–E223.Turnidge JD, Gottlieb T, Mitchell DH, et al. Australian Group on Antimicrobial Resistance Community–onset Gram–negative Surveillance Program annual report, 2010. Commun Dis Intell Q Rep. 2013;37(3):E219–E223.Sheng WH, Badal RE, Hsueh PR; et al. Distribution of extended–spectrum β–lactamases, AmpC β–lactamases, and carbapenemases among Enterobacteriaceae isolates causing intra-abdominal infections in the Asia–Pacific region: results of the study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother. 2013;57(7):2981–2988. doi:10.1128/AAC.00971–12Sheng WH, Badal RE, Hsueh PR; et al. Distribution of extended–spectrum β–lactamases, AmpC β–lactamases, and carbapenemases among Enterobacteriaceae isolates causing intra-abdominal infections in the Asia–Pacific region: results of the study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother. 2013;57(7):2981–2988. doi:10.1128/AAC.00971–12Tang HJ, Hsieh CF, Chang PC, et al. Clinical Significance of Community– and Healthcare–Acquired Carbapenem–Resistant Enterobacteriaceae Isolates. PLoS One. 2016;11(3):e0151897. doi:10.1371/journal.pone.0151897Tang HJ, Hsieh CF, Chang PC, et al. Clinical Significance of Community– and Healthcare–Acquired Carbapenem–Resistant Enterobacteriaceae Isolates. PLoS One. 2016;11(3):e0151897. doi:10.1371/journal.pone.0151897Miller BM, Johnson SW. Demographic and infection characteristics of patients with carbapenem–resistant Enterobacteriaceae in a community hospital: Development of a bedside clinical score for risk assessment. Am J Infect Control. 2016;44(2):134–137. doi:10.1016/j.ajic.2015.09.006Miller BM, Johnson SW. Demographic and infection characteristics of patients with carbapenem–resistant Enterobacteriaceae in a community hospital: Development of a bedside clinical score for risk assessment. Am J Infect Control. 2016;44(2):134–137. doi:10.1016/j.ajic.2015.09.006Guh AY, Bulens SN, Mu Y, et al. Epidemiology of Carbapenem–Resistant Enterobacteriaceae in 7 US Communities, 2012–2013. JAMA. 2015;314(14):1479–1487. doi:10.1001/jama.2015.12480Guh AY, Bulens SN, Mu Y, et al. Epidemiology of Carbapenem–Resistant Enterobacteriaceae in 7 US Communities, 2012–2013. JAMA. 2015;314(14):1479–1487. doi:10.1001/jama.2015.12480Thaden JT, Lewis SS, Hazen KC, et al. Rising rates of carbapenem–resistant enterobacteriaceae in community hospitals: a mixed–methods review of epidemiology and microbiology practices in a network of community hospitals in the southeastern United States. Infect Control Hosp Epidemiol. 2014;35(8):978–983. doi:10.1086/677157Thaden JT, Lewis SS, Hazen KC, et al. Rising rates of carbapenem–resistant enterobacteriaceae in community hospitals: a mixed–methods review of epidemiology and microbiology practices in a network of community hospitals in the southeastern United States. Infect Control Hosp Epidemiol. 2014;35(8):978–983. doi:10.1086/677157Brennan BM, Coyle JR, Marchaim D, et al. Statewide surveillance of carbapenem–resistant enterobacteriaceae in Michigan. Infect Control Hosp Epidemiol. 2014;35(4):342– 349. doi:10.1086/675611Brennan BM, Coyle JR, Marchaim D, et al. Statewide surveillance of carbapenem–resistant enterobacteriaceae in Michigan. Infect Control Hosp Epidemiol. 2014;35(4):342– 349. doi:10.1086/675611Li K, Jiang S, Fu H, et al. Risk Factors and Prognosis of Carbapenem–Resistant Organism Colonization and Infection in Acute Cholangitis. Infect Drug Resist. 2022;15:7777–7787. doi:10.2147/IDR.S398581Li K, Jiang S, Fu H, et al. Risk Factors and Prognosis of Carbapenem–Resistant Organism Colonization and Infection in Acute Cholangitis. Infect Drug Resist. 2022;15:7777–7787. doi:10.2147/IDR.S398581Tian F, Li Y, Wang Y, et al. Risk factors and molecular epidemiology of fecal carriage of carbapenem resistant Enterobacteriaceae in patients with liver disease. Ann Clin Microbiol Antimicrob. 2023;22(1):10. doi:10.1186/s12941–023–00560–8Tian F, Li Y, Wang Y, et al. Risk factors and molecular epidemiology of fecal carriage of carbapenem resistant Enterobacteriaceae in patients with liver disease. Ann Clin Microbiol Antimicrob. 2023;22(1):10. doi:10.1186/s12941–023–00560–8Satlin MJ, Chen L, Gomez–Simmonds A, et al. Impact of a Rapid Molecular Test for Klebsiella pneumoniae Carbapenemase and Ceftazidime–Avibactam Use on Outcomes After Bacteremia Caused by Carbapenem–Resistant Enterobacterales. Clin Infect Dis. 2022;75(12):2066–2075. doi:10.1093/cid/ciac354Satlin MJ, Chen L, Gomez–Simmonds A, et al. Impact of a Rapid Molecular Test for Klebsiella pneumoniae Carbapenemase and Ceftazidime–Avibactam Use on Outcomes After Bacteremia Caused by Carbapenem–Resistant Enterobacterales. Clin Infect Dis. 2022;75(12):2066–2075. doi:10.1093/cid/ciac354Recio R, Villa J, Viedma E, et al. Bacteraemia due to extensively drug–resistant Pseudomonas aeruginosa sequence type 235 high–risk clone: Facing the perfect storm. Int J Antimicrob Agents. 2018;52(2):172–179. doi:10.1016/j.ijantimicag.2018.03.018Recio R, Villa J, Viedma E, et al. Bacteraemia due to extensively drug–resistant Pseudomonas aeruginosa sequence type 235 high–risk clone: Facing the perfect storm. Int J Antimicrob Agents. 2018;52(2):172–179. doi:10.1016/j.ijantimicag.2018.03.018Baier C, Beck M, Panagiota V, et al. Infection control management and surveillance of carbapenem–resistant Gram–negative bacteria in hematopoietic stem cell recipients. Antimicrob Resist Infect Control. 2019;8:160. doi:10.1186/s13756–019–0606–3Baier C, Beck M, Panagiota V, et al. Infection control management and surveillance of carbapenem–resistant Gram–negative bacteria in hematopoietic stem cell recipients. Antimicrob Resist Infect Control. 2019;8:160. doi:10.1186/s13756–019–0606–3Cattaneo C, Di Blasi R, Skert C, et al. Bloodstream infections in haematological cancer patients colonized by multidrug–resistant bacteria. Ann Hematol. 2018;97(9):1717–1726. doi:10.1007/s00277–018–3341–6Cattaneo C, Di Blasi R, Skert C, et al. Bloodstream infections in haematological cancer patients colonized by multidrug–resistant bacteria. Ann Hematol. 2018;97(9):1717–1726. doi:10.1007/s00277–018–3341–6Jiang Y, Ding Y, Wei Y, Jian C, Liu J, Zeng Z. Carbapenem–resistant Acinetobacter baumannii: A challenge in the intensive care unit. Front Microbiol. 2022;13:1045206. doi:10.3389/fmicb.2022.1045206Jiang Y, Ding Y, Wei Y, Jian C, Liu J, Zeng Z. Carbapenem–resistant Acinetobacter baumannii: A challenge in the intensive care unit. Front Microbiol. 2022;13:1045206. doi:10.3389/fmicb.2022.1045206Hu H, Wang Y, Sun J, et al. Risk factors and molecular epidemiology of intestinal colonization by carbapenem–resistant Gram–negative bacteria in patients with hematological diseases: a multicenter case‒control study. Microbiol Spectr. 2024;12(7):e0429923. doi:10.1128/spectrum.04299–23Hu H, Wang Y, Sun J, et al. Risk factors and molecular epidemiology of intestinal colonization by carbapenem–resistant Gram–negative bacteria in patients with hematological diseases: a multicenter case‒control study. Microbiol Spectr. 2024;12(7):e0429923. doi:10.1128/spectrum.04299–23Кузьменков А. Ю., Виноградова А. Г., Трушин И. В. и др. AMRmap – система мониторинга антибиотикорезистентности в России. Клиническая микробиология и антимикробная химиотерапия. 2021. Т.23, №2. С.198–204.Kuzmenkov AYu., Vinogradova AG., Trushin IV., et al. AMRmap – antibiotic resistance surveillance system in Russia. Kliniceskaa Mikrobiologia i Antimikrobnaa Himioterapia. 2021; 23(2):198–204 (In Russ). doi:10.36488/cmac.2021.2.198–204Lautenbach E, Mosepele M, Smith RM, et al. Risk Factors for Community Colonization With Extended–Spectrum Cephalosporin–Resistant Enterobacterales (ESCrE) in Botswana: An Antibiotic Resistance in Communities and Hospitals (ARCH) Study. Clin Infect Dis. 2023;77(Suppl 1):S89–S96. doi:10.1093/cid/ciad259Lautenbach E, Mosepele M, Smith RM, et al. Risk Factors for Community Colonization With Extended–Spectrum Cephalosporin–Resistant Enterobacterales (ESCrE) in Botswana: An Antibiotic Resistance in Communities and Hospitals (ARCH) Study. Clin Infect Dis. 2023;77(Suppl 1):S89–S96. doi:10.1093/cid/ciad259Caudell MA, Castillo C, Santos LF, et al. Risk factors for colonization with extended–spectrum cephalosporin–resistant and carbapenem–resistant Enterobacterales among hospitalized patients in Guatemala: An Antibiotic Resistance in Communities and Hospitals (ARCH) study. IJID Reg. 2024;11:100361. doi:10.1016/j.ijregi.2024.100361Caudell MA, Castillo C, Santos LF, et al. Risk factors for colonization with extended–spectrum cephalosporin–resistant and carbapenem–resistant Enterobacterales among hospitalized patients in Guatemala: An Antibiotic Resistance in Communities and Hospitals (ARCH) study. IJID Reg. 2024;11:100361. doi:10.1016/j.ijregi.2024.100361Moghnieh R, Abdallah D, Jadayel M, et al. Epidemiology, risk factors, and prediction score of carbapenem resistance among inpatients colonized or infected with 3rd generation cephalosporin resistant Enterobacterales. Sci Rep. 2021;11(1):14757. doi:10.1038/s41598–021–94295–1Moghnieh R, Abdallah D, Jadayel M, et al. Epidemiology, risk factors, and prediction score of carbapenem resistance among inpatients colonized or infected with 3rd generation cephalosporin resistant Enterobacterales. Sci Rep. 2021;11(1):14757. doi:10.1038/s41598–021–94295–1Park SH, Yi Y, Suh W, Ji SK, Han E, Shin S. The impact of enhanced screening for carbapenemase–producing Enterobacterales in an acute care hospital in South Korea. Antimicrob Resist Infect Control. 2023;12(1):62. doi:10.1186/s13756–023–01270–8Park SH, Yi Y, Suh W, Ji SK, Han E, Shin S. The impact of enhanced screening for carbapenemase–producing Enterobacterales in an acute care hospital in South Korea. Antimicrob Resist Infect Control. 2023;12(1):62. doi:10.1186/s13756–023–01270–8Клясова Г. А., Коробова А. Г., Фролова И. Н. и др. Детекция энтеробактерий с продукцией бета–лактамаз расширенного спектра у больных острыми миелоидными лейкозами и лимфомами при поступлении в стационар // Гематология и трансфузиология. 2016. Т.61, №1. С. 25–32.Klyasova GA, Korobova AG, Frolova IN, et al. Detection of extended–spectrum β-lactamase producing Enterobacteriaceae (ESBL–E) among patients with acute myeloid leukemia and lymphoma upon admission to hospital. Russian journal of hematology and transfusiology. 2016;61(1):25–32 (In Russ.). https://doi.org/10.18821/0234–5730–2016–61–1–25–32Segagni Lusignani L, Presterl E, Zatorska B, et al. Infection control and risk factors for acquisition of carbapenemase producing enterobacteriaceae. A 5 year (2011–2016) case–control study. Antimicrob Resist Infect Control. 2020;9(1):18. doi:10.1186/s13756–019–0668–2Segagni Lusignani L, Presterl E, Zatorska B, et al. Infection control and risk factors for acquisition of carbapenemase producing enterobacteriaceae. A 5 year (2011–2016) case–control study. Antimicrob Resist Infect Control. 2020;9(1):18. doi:10.1186/s13756–019–0668–2Salomão MC, Freire MP, Boszczowski I, et al. Increased Risk for Carbapenem–Resistant Enterobacteriaceae Colonization in Intensive Care Units after Hospitalization in Emergency Department. Emerg Infect Dis. 2020;26(6):1156–1163. doi:10.3201/eid2606.190965Salomão MC, Freire MP, Boszczowski I, et al. Increased Risk for Carbapenem–Resistant Enterobacteriaceae Colonization in Intensive Care Units after Hospitalization in Emergency Department. Emerg Infect Dis. 2020;26(6):1156–1163. doi:10.3201/eid2606.190965Callejón Fernández M, Madueño Alonso A, Abreu Rodríguez R, et al. Risk factors for colonization by carbapenemase–producing bacteria in Spanish long–term care facilities: a multicentre point–prevalence study. Antimicrob Resist Infect Control. 2022;11(1):163. doi:10.1186/s13756–022–01200–0Callejón Fernández M, Madueño Alonso A, Abreu Rodríguez R, et al. Risk factors for colonization by carbapenemase–producing bacteria in Spanish long–term care facilities: a multicentre point–prevalence study. Antimicrob Resist Infect Control. 2022;11(1):163. doi:10.1186/s13756–022–01200–0Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol. 2011;62(6):591–599.Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol. 2011;62(6):591–599.van Duin D, Paterson DL. Multidrug–Resistant Bacteria in the Community: An Update. Infect Dis Clin North Am. 2020;34(4):709–722. doi:10.1016/j.idc.2020.08.002van Duin D, Paterson DL. Multidrug–Resistant Bacteria in the Community: An Update. Infect Dis Clin North Am. 2020;34(4):709–722. doi:10.1016/j.idc.2020.08.002Shrestha R, Luterbach CL, Dai W, et al. Characteristics of community–acquired carbapenem–resistant Enterobacterales. J Antimicrob Chemother. 2022;77(10):2763–2771. doi:10.1093/jac/dkac239Shrestha R, Luterbach CL, Dai W, et al. Characteristics of community–acquired carbapenem–resistant Enterobacterales. J Antimicrob Chemother. 2022;77(10):2763–2771. doi:10.1093/jac/dkac239Salomão MC, Guimarães T, Duailibi DF, et al. Carbapenem–resistant Enterobacteriaceae in patients admitted to the emergency department: prevalence, risk factors, and acquisition rate. J Hosp Infect. 2017;97(3):241–246. doi:10.1016/j.jhin.2017.08.012Salomão MC, Guimarães T, Duailibi DF, et al. Carbapenem–resistant Enterobacteriaceae in patients admitted to the emergency department: prevalence, risk factors, and acquisition rate. J Hosp Infect. 2017;97(3):241–246. doi:10.1016/j.jhin.2017.08.012Barbadoro P, Bencardino D, Carloni E, et al. Carriage of Carbapenem–Resistant Enterobacterales in Adult Patients Admitted to a University Hospital in Italy. Antibiotics (Basel). 2021;10(1):61. doi:10.3390/antibiotics10010061Barbadoro P, Bencardino D, Carloni E, et al. Carriage of Carbapenem–Resistant Enterobacterales in Adult Patients Admitted to a University Hospital in Italy. Antibiotics (Basel). 2021;10(1):61. doi:10.3390/antibiotics10010061van Loon K, Voor In ‘t Holt AF, Vos MC. A Systematic Review and Meta–analyses of the Clinical Epidemiology of Carbapenem–Resistant Enterobacteriaceae. Antimicrob Agents Chemother. 2017;62(1):e01730–17. doi:10.1128/AAC.01730–17van Loon K, Voor In ‘t Holt AF, Vos MC. A Systematic Review and Meta–analyses of the Clinical Epidemiology of Carbapenem–Resistant Enterobacteriaceae. Antimicrob Agents Chemother. 2017;62(1):e01730–17. doi:10.1128/AAC.01730–17

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