Microbiological monitoring of the respiratory tract in patients with primary ciliary dyskinesia complicated by bronchiectasis
Objective. Analysis of the etiology and epidemiology of respiratory tract infections in patients with primary ciliary dyskinesia (PCD) complicated by bronchiectasis.Domblides E.A., Chernukha M.Yu., Avetisyan L.R., Voronkova A.Yu., Kiyan T.A., Zhukhovitsky V.G., Polyakov N.B., Kuznetsova N.A., Shidlovskaya E.V., Gushchin V.A., Kondratyeva E.I.
Materials and methods. Data from 83 patients from 37 regions of the Russian Federation with a confirmed diagnosis of PCD and a complication of bronchiectasis were analyzed. The study was conducted between 2022 and 2025. The material for the study included sputum, throat and nasal swabs. Microorganisms were identified using bacteriological methods, as well as MALDI-TOF mass spectrometry analysis (UltrafleXtreme (Bruker Daltonics, Germany) and PCR for MRSA detection. Antibiotic susceptibility was assessed using the disk diffusion method, and a serial dilution method was used to determine susceptibility to a number of drugs.
Results. 36 different species and genera of clinically significant bacteria and 2 genera of fungi were isolated. Staphylococcus aureus (45.8%) and Pseudomonas aeruginosa (38.5%) were the most prevalent bacteria. Most species belonged to the group of non-fermenting gram-negative bacteria (NFGB) and the order Enterobacterales. When studying the antibiotic susceptibility of P. aeruginosa, multiresistant strains were found in 51.6% of cases, and among S. aureus isolates, in 45.7%. The greatest diversity of microbes were identified in children: 28 bacterial species were isolated, compared to 22 species identified in adult patients (18 years and older). P. aeruginosa was the dominant bacteria in adults (52.3%), while S. aureus was the most common (64.1%) in children (18 years and younger). Among adolescents aged 13–17, S. aureus was isolated in 73.7% of cases, and in the subgroup of children under 12 - in 55% of cases.
Conclusion. When studying the respiratory microflora in patients with PCD and bronchiectasis, it is important to note the need for microbiological monitoring in these patients, especially those with a history of bronchiectasis.
Keywords
primary ciliary dyskinesia
bronchiectasis
bacterial lung infections
References
- Lucas J.S.A., Walker W.T., Kuehni C.E., Lazor R. Primary ciliary dyskinesia. In.: Cordier J.F. (ed.) Orphan Lung Diseases. European Respiratory Society Monograph 2011; 201–217. DOI: 10.1183/1025448x.10008310
- Новак А.А., Мизерницкий Ю.Л. Первичная цилиарная дискинезия: состояние проблемы и перспективы. Медицинский совет 2021; (1): 276–285. [Novak A.A., Mizernitskiy Yu.L. Primary ciliary dyskinesia: state of the problem and prospects. Medical Council 2021; (1): 276–285. (In Russ.)]. DOI: 10.21518/2079-701X-2021-1-276-285
- Богорад А.Е., Дьякова С.Э., Мизерницкий Ю.Л. Первичная цилиарная дискинезия: современные подходы к диагностике и терапии. Российский вестник перинатологии и педиатрии 2019; 64(5): 123–133. [Bogorad A.E., Diakova S.E., Mizernitsky Yu.L. Primary ciliary dyskinesia: modern approaches to the diagnostics and treatment. Russian Bulletin of Perinatology and Pediatrics 2019; 64(5): 123–133. (In Russ.)]. DOI: 10.21508/1027-4065-2019-64-5-123-133
- Wee W.B., Kinghorn B., Davis S.D., Ferkol T.W., Shapiro A.J. Primary Ciliary Dyskinesia. Pediatrics 2024; 153(6): e2023063064. DOI: 10.1542/peds.2023-063064
- Kuehni C.E., Lucas J.S. Diagnosis of primary ciliary dyskinesia: summary of the ERS Task Force report. Breathe (Sheff.) 2017; 13(3): 166–178. DOI: 10.1183/20734735.008517
- Knowles M.R., Zariwala M., Leigh M. Primary Ciliary Dyskinesia. Clin. Chest Med. 2016; 37(3): 449–461. DOI: 10.1016/j.ccm.2016.04.008
- Кондратьева Е.И., Авдеев С.Н., Мизерницкий Ю.Л., Поляков А.В., Чернуха М.Ю., Кондратенко О.В. и др. Первичная цилиарная дискинезия: обзор проекта клинических рекомендаций 2022 года. Пульмонология 2022; 32 (4): 517–538. [Kondratyeva E.I., Avdeev S.N., Mizernitskiy Yu.L., Polyakov A.V., Chernukha M.Yu., Kondratenko O.V. et al. Primary ciliary dyskinesia: review of the draft clinical guidelines, 2022. Pulmonologiya 2022; 32(4): 517–538. (In Russ.)]. DOI: 10.18093/0869-0189-2022–32-4-517-538
- Shah A., Shoemark A., MacNeill S.J., Bhaludin B., Rogers A., Bilton D. et al. A longitudinal study characterising a large adult primary ciliary dyskinesia population. Eur. Respir. J. 2016; 48(2): 441–450. DOI: 10.1183/13993003.00209-2016
- Чернуха М.Ю., Кондратьева Е.И., Домблидес Э.А., Аветисян Л.Р., Воронкова А.Ю., Киян Т.А. и др. Микробный пейзаж дыхательных путей у пациентов с первичной цилиарной дискинезией: пилотное исследование. Пульмонология 2025; 35(3): 351–358. [Chernukha M. Yu., Kondratyeva E.I., Domblides E.A., Avetisyan L.R., Voronkova A. Yu., Kyian T.A. et al. Airway microbial landscape in patients with primary ciliary dyskinesia – a pilot study. Pulmonologiya 2025; 35(3): 351–358. (In Russ.)]. DOI: 10.18093/0869-0189-2024-4446
- Alanin M.C., Nielsen K.G., von Buchwald C., Skov M., Aanaes K., Høiby N. et al. A longitudinal study of lung bacterial pathogens in patients with primary ciliary dyskinesia. Clin. Microbiol. Infect. 2015; 21(12): 1093-e1 DOI: 10.1016/j.cmi.2015.08.020
- Чернуха М.Ю., Шагинян И.А., Жуховицкий В.Г., Аветисян Л.Р., Кулястова Д.Г., Сиянова Е.А. и др. Применение системы MALDI Biotyper и алгоритма микробиологической диагностики для идентификации неферментирующих микроорганизмов, выделенных из дыхательных путей у больных муковисцидозом. Клиническая микробиология и антимикробная xимиотерапия. 2017; 19(4): 327–334. [Chernukha M.Yu., Shaginyan I.A., Zhukhovitskiy V.G. et al. Use of the MALDI Biotyper system and the microbiological diagnosis algorithm for identification of nonfermenting bacteria isolated from respiratory tract in cystic fibrosis patients. Clinical Microbiology and Antimicrobial Chemotherapy. 2017; 19(4): 327–334. (In Russ.)].
- Wijers C.D., Chmiel J.F., Gaston B.M. Bacterial infections in patients with primary ciliary dyskinesia: Comparison with cystic fibrosis. Chron. Respir. Dis. 2017; 14(4): 392–406. DOI:10.1177/1479972317694621
- Шагинян И.А., Аветисян Л.Р., Чернуха М.Ю., Сиянова Е.А., Бурмистров Е.М., Воронкова А.Ю. и др. Эпидемиологическая значимость молекулярной изменчивости генома изолятов Pseudomonas aeruginosa, вызывающих хроническую инфекцию легких у больных муковисцидозом. Клиническая микробиология и антимикробная химиотерапия 2019; 21(4): 340–351. [Shaginyan I.A., Avetisyan L.R., Chernukha M.Yu. et al. Epidemiological significance of genome variations in Pseudomonas aeruginosa causing chronic lung infection in patients with cystic fibrosis. Clinical Microbiology and Antimicrobial Chemotherapy 2019; 21(4): 340–351. (In Russ.)]. DOI: 10.36488/cmac.2019.4.340-351
- Saiman L., Siegel J. Infection Control Recommendations for Patients With Cystic Fibrosis: Microbiology, Important Pathogens, and Infection Control Practices to Prevent Patient-to-Patient Transmission. Infect. Control. Hosp. Epidemiol. 2003; 24(5): 6–52. DOI: 10.1086/503485
- Шагинян И.А., Капранов Н.И., Чернуха М.Ю., Алексеева Г.В., Семыкин С.Ю., Каширская Н.Ю. и др. Микробный пейзаж нижних дыхательных путей у различных возрастных групп детей, больных муковисцидозом. Журнал микробиологии, эпидемиологии и иммунобиологии 2010; (1): 15–20. [Shaginyan I.A., Kapranov N.I., Chernukha M. Yu. et al. [Microbial landscape of the lower respiratory tract in different age groups of children with cystic fibrosis. Journal of microbiology, epidemiology and immunobiology 2010; 87(1): 15–20. (In Russ.)].
- Чернуха М.Ю., Аветисян Л.Р., Шагинян И.А., Алексеева Г.В., Авакян Л.В., Каширская Н.Ю. и др. Алгоритм микробиологической диагностики хронической инфекции легких у больных муковисцидозом. Клиническая микробиология и антимикробная химиотерапия 2014; 16(4): 312–324. [Chernukha M.Yu., Avetisyan L.R., Shaginyan I.A., Alekseeva G.V., Avakyan L.V., Kashirskaya N. Yu. et al. Microbiological diagnosis algorithm for chronic lung infection in patients with cysticfibrosis. Clinical Microbiology and Antimicrobial Chemotherapy. 2014; 16(4): 312–324. (In Russ.)].
- Аветисян Л.Р., Чернуха М.Ю., Шагинян И.А., Медведева О.С., Бурмистров Е.М., Русакова Е.В. и др. Применение современных методов в микробиологической диагностике хронической инфекции легких у больных муковисцидозом. Сибирское медицинское обозрение 2019; 2(116): 70–79. [Avetisyan L.R., Chernukha M. Yu., Shaginyan I.A., Medvedeva O.S., Burmistrov E.M., Rusakova E.V. et al. Application of modern methods in microbiological diagnosis of chronic infec tion of lungs in patients with cystic fibrosis. Siberian Medical Review 2019; (2): 70–79. (In Russ.)]. DOI: 10.20333/2500136-2019-2-70-79
- Ender M., McCallum N., Berger-Bächi B. Impact of mecA promoter mutations on mecA expression and β-lactam resistance levels. International Journal of Medical Microbiology 2008; 298(7–8): 607–617. DOI: 10.1016/j.ijmm.2008.01.015.
- Аzzam A., Khaled H., Mosa M., Refaey N., Alsaifi M.S., Elsisi S. et al. Epidemiology of clinically isolated methicillin-resistant Staphylococcus aureus (MRSA) and its susceptibility to linezolid and vancomycin in Egypt: a systematic review with meta-analysis. BMC Infect. Dis. 2023; 23(1): 263. DOI: 10.1186/s12879-023-08202-2
- Dacco V., Alicandro G., Consales A., Rosazza C., Sciarrabba C.S., Cariani L. et al. Cepacia syndrome in cystic fibrosis: a systematic review of the literature and possible new perspectives in treatment. Pediatr. Pulmonol. 2023; 58(5): 1337–1343. DOI: 10.1002/ppul.26359
- Шагинян И.А., Чернуха М.Ю., Капранов Н.И., Кондратьева Е.И., Каширская Н.Ю., Амелина Е.Л. и др. Консенсус «Муковисцидоз: определение, диагностические критерии, терапия», раздел «Микробиология и эпидемиология хронической респираторной инфекции при муковисцидозе». Педиатр 2016; 7(1): 80–96. [Shaginyan I.A., Chernukha M.Y., Kapranov N.I., Kondratyeva E.I., Kashirskaya N.Y., Amelina E.L. et al. Consensus «Cystic Fibrosis: definition, diagnostic criteria, treatment», Section «Microbiology and Epidemiology of chronic respiratory infections in cystic fibrosis». Pediatrician 2016; 7(1): 80–96. (In Russ.)]. DOI: 10.17816/PED7180-96
About the Authors
Edward A. Domblides, Junior Researcher, Laboratory of Molecular Epidemiology of Nosocomial Infections, N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology. Ministry of Health of the Russia, Moscow, Russia; domblides@mail.ru; https://orcid.org/0009-0005-7835-8891Marina Yu. Chernukha, МD, Head, Laboratory of Molecular Epidemiology of Nosocomial Infections, N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology. Ministry of Health of the Russia, Chief Researcher, Research and Clinical Institute of Childhood, Ministry of Health of the Moscow Region, Moscow, Russia; chernukha@gamaleya.org; https://orcid.org/0000-0002-2349-8556
Lusine R. Avetisyan, MD, Head, Laboratory of Epidemiology of Opportunistic Infections; Leading Researcher, Laboratory of Molecular Epidemiology of Nosocomial Infections, ,N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology, Ministry of Health of the Russia, Moscow, Russia; lusavr@mail.ru; https://orcid.org/0000-0002-9053-2515
Lusine R. Avetisyan, MD, Head, Laboratory of Opportunistic Infections Epidemiology; Leading Researcher, Laboratory of Molecular Epidemiology of Nosocomial Infections, N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology. Ministry of Health of the Russia, Moscow, Russia; lusavr@mail.ru; https://orcid.org/0000-0002-9053-2515
Anna Yu. Voronkova, Cand. Med. Sci., Leading Researcher, Scientific and Clinical Department of Cystic Fibrosis, Academician N.P. Bochkov Medical Genetic Research Center, Ministry of Science and Higher Education of the Russian Federation, Moscow, Russia; voronkova111@yandex.ru; https://orcid.org/0000-0002-8183-7990
Tatiana A. Kyian, Cand. Med. Sci., Senior Researcher, Scientific and Clinical Department of Cystic Fibrosis, Academician N.P. Bochkov Medical Genetic Research Center, Ministry of Science and Higher Education of the Russian Federation, Moscow, Russia; bogdanovatata87@gmail.com; https://orcid.org/0000-0001-8281-1162
Vladimir G. Zhukhovitsky, Cand. Med. Sci., Head, Laboratory of Indication and Ultrastructural Analysis of Microorganisms, N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology, Ministry of Health of the Russia, Moscow, Russia; Associate Professor, Department Сlinical Laboratory Diagnostics with a Course in Laboratory Immunology, Russian Medical Academy of Continuous Professional Education, Ministry of Health of Russia, Moscow, Russia; zhukhovitsky@rambler.ru; https://orcid.org/0000-0002-4653-2446
Nikita B. Polyakov, Researcher, Laboratory of Indication and Ultrastructural Analysis of Microorganisms,N.F. Gamaleya Federal Research Center for Epidemiology and Microbioof Health of the Russia, Moscow, Russia; polyakovnb@gmail.com; https://orcid.org/0000-0002-1647-5815logy, Ministry
Nadezhda A. Kuznetsova, Cand. Bio. Sci., Research Associate, Head, Laboratory of Infection Vectors, N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology, Ministry of Health of the Russia, Moscow, Russia; a-myznikova@list.ru; 0000–0001–5299–3081
Elena V. Shidlovskaya, Research Associate, Laboratory of Mechanisms of Population Variability of Pathogenic Microorganisms, N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology, Ministry of Health of the Russia, Moscow, Russia; lenitsa@gmail.com
Vladimir A. Gushchin, BD, Associate Professor, Head, Epidemiology Department; Head, Laboratory of Mechanisms of Population Variability of Pathogenic Microorganisms, N.F. Gamaleya Federal Research Center for Epidemiology and Microbiology, Ministry of Health of the Russia; Head, Department of Medical Genetics, I.M. Sechenov First Moscow State Medical University, Ministry of Health of the Russia (Sechenov University). Moscow, Russia; wowaniada@yan-dex.ru; 0000–0002–9397–3762
Professor Elena I. Kondratieva, MD, Head, Scientific and Clinical Department of Cystic Fibrosis; Head, Department of Genetics of Respiratory System Diseases, Academician N.P. Bochkov Medical Genetics Research Center, Ministry of Science and Higher Education of the Russian Federation; Head of the Center, Research and Clinical Institute of Childhood, Ministry of Health of the Moscow Region, Moscow, Russia;elenafpk@mail.ru; http://orcid.org/0000-0001-6395-0407



