{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T21:40:04Z","timestamp":1790286004367,"version":"4.1.0"},"reference-count":37,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,8,29]],"date-time":"2022-08-29T00:00:00Z","timestamp":1661731200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81671985"],"award-info":[{"award-number":["81671985"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2018ZX10712001 007"],"award-info":[{"award-number":["2018ZX10712001 007"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2019SKLID403"],"award-info":[{"award-number":["2019SKLID403"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Science and Technology Major Project of China","award":["81671985"],"award-info":[{"award-number":["81671985"]}]},{"name":"National Science and Technology Major Project of China","award":["2018ZX10712001 007"],"award-info":[{"award-number":["2018ZX10712001 007"]}]},{"name":"National Science and Technology Major Project of China","award":["2019SKLID403"],"award-info":[{"award-number":["2019SKLID403"]}]},{"name":"Science Foundation for the State Key Laboratory for Infectious Disease Prevention and Control of China","award":["81671985"],"award-info":[{"award-number":["81671985"]}]},{"name":"Science Foundation for the State Key Laboratory for Infectious Disease Prevention and Control of China","award":["2018ZX10712001 007"],"award-info":[{"award-number":["2018ZX10712001 007"]}]},{"name":"Science Foundation for the State Key Laboratory for Infectious Disease Prevention and Control of China","award":["2019SKLID403"],"award-info":[{"award-number":["2019SKLID403"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>(1) Background: M. catarrhalis can ascend into the middle ear, where it is a prevalent causative agent of otitis media in children, or enter the lower respiratory tract, where it is associated with community-acquired pneumonia (CAP). In this study, we aimed to provide an overview of the prevalence of M. catarrhalis in preschool children. (2) Methods: M. catarrhalis strains were isolated from samples. All isolates were characterized in terms of serotypes (STs), virulence genes, multilocus sequence type, and antibiotic susceptibility. (3) Results: The percentages of strains expressing lipooligosaccharides (LOSs), serotype A, B, C, or unknown were 67.61%, 15.71%, 4.28%, and 12.38%, respectively. Among the strains, 185 (88.10%) carried ompB2, 207 (98.57%) carried ompE, and 151 (71.90%) carried ompCD. The most frequently identified STs were ST449 (n = 13), ST64 (n = 11), and ST215 (n = 10). The resistance rates to the antibiotics cefuroxime, azithromycin, and erythromycin were 43.33%, 28.10%, and 39.05%, respectively. (4) Conclusions: High prevalence of some-specific ST types and high rates of antibiotic resistance indicate the necessity for an increased vigilance of resistant strains, a rational use of antibiotics in preschool children, and most importantly, the surveillance of healthy asymptomatic participants preschool children with M. catarrhalis. Our findings provide a platform for the development of novel M. catarrhalis vaccines.<\/jats:p>","DOI":"10.3390\/pathogens11090984","type":"journal-article","created":{"date-parts":[[2022,8,29]],"date-time":"2022-08-29T22:53:42Z","timestamp":1661813622000},"page":"984","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Genotypic and Phenotypic Characteristics of Moraxella catarrhalis from Patients and Healthy Asymptomatic Participants among Preschool Children"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2396-2483","authenticated-orcid":false,"given":"Na","family":"Zhao","sequence":"first","affiliation":[{"name":"Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102211, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongyu","family":"Ren","sequence":"additional","affiliation":[{"name":"Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102211, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianping","family":"Deng","sequence":"additional","affiliation":[{"name":"Zigong Center for Disease Control and Prevention, Control and Prevention of Zigong City, Zigong 643002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yinju","family":"Du","sequence":"additional","affiliation":[{"name":"Disease Control and Prevention of Liaocheng City, Liaocheng 252001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qun","family":"Li","sequence":"additional","affiliation":[{"name":"Zigong Center for Disease Control and Prevention, Control and Prevention of Zigong City, Zigong 643002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pu","family":"Zhou","sequence":"additional","affiliation":[{"name":"Disease Control and Prevention of Liaocheng City, Liaocheng 252001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haijian","family":"Zhou","sequence":"additional","affiliation":[{"name":"Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102211, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangkun","family":"Jiang","sequence":"additional","affiliation":[{"name":"Disease Control and Prevention of Liaocheng City, Liaocheng 252001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tian","family":"Qin","sequence":"additional","affiliation":[{"name":"Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102211, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1086\/599375","article-title":"Moraxella catarrhalis, a Human Respiratory Tract Pathogen","volume":"49","author":"Murphy","year":"2009","journal-title":"Clin. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.meegid.2017.11.018","article-title":"Multilocus sequence typing-based analysis of Moraxella catarrhalis population structure reveals clonal spreading of drug-resistant strains isolated from childhood pneumonia","volume":"56","author":"Du","year":"2017","journal-title":"Infect. Genet. Evol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1128\/MMBR.00007-09","article-title":"Molecular Aspects of Moraxella catarrhalis Pathogenesis","volume":"73","author":"Bootsma","year":"2009","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1128\/CMR.15.1.125-144.2002","article-title":"Moraxella catarrhalis: From emerging to established pathogen","volume":"15","author":"Verduin","year":"2002","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1089\/mdr.2014.0217","article-title":"High-Level Macrolide-Resistant Moraxella catarrhalis and De-velopment of an Allele-Specific PCR Assay for Detection of 23S rRNA Gene A2330T Mutation: A Three-Year Study at a Chi-nese Tertiary Hospital","volume":"21","author":"Liu","year":"2015","journal-title":"Microb. Drug Resist."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"35711","DOI":"10.1038\/srep35711","article-title":"Use of next generation sequence to investigate potential novel macrolide resistance mechanisms in a population of Moraxella catarrhalis isolates","volume":"6","author":"Liu","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_7","first-page":"707","article-title":"Prevalence of Moraxella catarrhalis in the nasopharyngeal specimen from 1\u2009082 hospitalized children with respiratory infection and the drug resistance of the isolates","volume":"18","author":"Tang","year":"2016","journal-title":"Zhongguo Dang Dai Er Ke Za Zhi"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1136\/archdischild-2013-305550","article-title":"The diagnosis and management of acute otitis media: American Academy of Pediatrics Guide-lines 2013","volume":"100","author":"Siddiq","year":"2015","journal-title":"Arch. Dis. Child Educ. Pract. Ed."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Liu, Y., Chen, M., Zhao, T., Wang, H., Wang, R., Cai, B., Cao, B., Sun, T., Hu, Y., and Xiu, Q. (2009). Causative agent distribution and antibiotic therapy assessment among adult patients with community acquired pneumonia in Chinese urban population. BMC Infect. Dis., 9.","DOI":"10.1186\/1471-2334-9-31"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Shi, W., Wen, D., Chen, C., Yuan, L., Gao, W., Tang, P., Cheng, X., and Yao, K. (2018). \u03b2-Lactamase production and antibiotic susceptibility pattern of Moraxella catarrhalis isolates collected from two county hospitals in China. BMC Microbiol., 18.","DOI":"10.1186\/s12866-018-1217-5"},{"key":"ref_11","first-page":"30","article-title":"Antimicrobial susceptibility of community-acquired respiratory tract pathogens isolated from class B hospitals in China during 2013 and 2014","volume":"39","author":"Sun","year":"2016","journal-title":"Zhonghua Jie He He Hu Xi Za Zhi"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Kov\u00e1cs, E., Sahin-T\u00f3th, J., T\u00f3thp\u00e1l, A., Van Der Linden, M., Tirczka, T., and Dobay, O. (2020). Co-carriage of Staphylococcus aureus, Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis among three different age categories of children in Hungary. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0229021"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"630.e1","DOI":"10.1016\/j.cmi.2020.04.033","article-title":"Decreased prevalence of Moraxella catarrhalis in addition to Streptococcus pneumoniae in children with upper respiratory tract infection after introduction of conjugated pneumococcal vaccine: A retrospective cohort study","volume":"27","author":"Littorin","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1099\/mic.0.042929-0","article-title":"Colonization of healthy children by Moraxella catarrhalis is characterized by genotype heterogeneity, virulence gene diversity and co-colonization with Haemophilus influenzae","volume":"157","author":"Verhaegh","year":"2011","journal-title":"Microbiology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1556\/1886.2020.00010","article-title":"The incidence of anaerobic bacteria in adult patients with chronic sinusitis: A prospective, single-centre microbiological study","volume":"10","author":"Torkos","year":"2020","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"110848","DOI":"10.1016\/j.ijporl.2021.110848","article-title":"Nasopharyngeal cultures in children with AOM\u2014A retrospective study on bacteriological findings and impact on management","volume":"149","author":"Jinhage","year":"2021","journal-title":"Int. J. Pediatr. Otorhinolaryngol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1016\/j.vaccine.2015.11.060","article-title":"Nasopharyngeal carriage of Streptococcus pneumoniae and other bacteria in the 7th year after implementation of the pneumococcal conjugate vaccine in the Netherlands","volume":"34","author":"Bosch","year":"2016","journal-title":"Vaccine"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Pan, H., Cui, B., Huang, Y., Yang, J., and Ba-Thein, W. (2016). Nasal carriage of common bacterial pathogens among healthy kindergarten children in Chaoshan region, southern China: A cross-sectional study. BMC Pediatr., 16.","DOI":"10.1186\/s12887-016-0703-x"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1099\/jmm.0.040584-0","article-title":"Nasal colonization by four potential respiratory bacteria in healthy children attending kindergarten or elementary school in Seoul, Korea","volume":"61","author":"Bae","year":"2012","journal-title":"J. Med. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"450","DOI":"10.7883\/yoken.JJID.2020.824","article-title":"Study of Normal Flora in the Pharynx of Healthy Children","volume":"74","author":"Oishi","year":"2021","journal-title":"Jpn. J. Infect. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1567","DOI":"10.1007\/s40121-021-00472-0","article-title":"Epidemiology of Respiratory Pathogens Among Children Hospitalized for Pneumonia in Xiamen: A Retrospective Study","volume":"10","author":"Sun","year":"2021","journal-title":"Infect. Dis. Ther."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e18504","DOI":"10.1097\/MD.0000000000018504","article-title":"Clinical significance of viral\u2013bacterial codetection among young children with respiratory tract infections: Findings of RSV, influenza, adenoviral infections","volume":"99","author":"Jung","year":"2020","journal-title":"Medicine (Baltimore)"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1159\/000504541","article-title":"The Suppressive Role of Streptococcus pneumoniae Colonization in Acute Exacerbations of Childhood Bronchial Asthma","volume":"181","author":"Kama","year":"2019","journal-title":"Int. Arch. Allergy Immunol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1016\/j.arcmed.2010.10.003","article-title":"Distribution of genes encoding virulence factors ompB2, ompCD, ompE, \u03b2-lactamase and serotype in pathogenic and colonizing strains of Moraxella catarrhalis","volume":"41","author":"Mitov","year":"2010","journal-title":"Arch. Med. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1906","DOI":"10.1128\/IAI.72.4.1906-1913.2004","article-title":"The Moraxella catarrhalis porin-like outer mem-brane protein CD is an adhesin for human lung cells","volume":"72","author":"Holm","year":"2004","journal-title":"Infect. Immun."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"6250","DOI":"10.1128\/IAI.68.11.6250-6256.2000","article-title":"Antigenic structure of outer membrane protein E of Moraxella catarrh-alis and construction and characterization of mutants","volume":"68","author":"Murphy","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Ren, D., Xie, H., Zhang, W., Hassan, F., Petralia, R.S., Yu, S., Lim, D.J., and Gu, X.-X. (2011). Intranasal immunization of the combined lipooligosaccha-ride conjugates protects mice from the challenges with three serotypes of Moraxella catarrhalis. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0029553"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2790","DOI":"10.1128\/IAI.73.5.2790-2796.2005","article-title":"Synthesis and Characterization of Lipooligosaccharide-Based Conjugate Vaccines for Serotype B Moraxella catarrhalis","volume":"73","author":"Yu","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2974","DOI":"10.1128\/IAI.01915-06","article-title":"Biological and immunological characteristics of lipooligosaccharide-based conjugate vaccines for sero-type C Moraxella catarrhalis","volume":"75","author":"Yu","year":"2007","journal-title":"Infect. Immun."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5982","DOI":"10.1128\/IAI.70.11.5982-5989.2002","article-title":"Specific Immune Responses and Enhancement of Murine Pulmonary Clearance of Moraxella catarrhalis by Intranasal Immunization with a Detoxified Lipooligosaccharide Conjugate Vaccine","volume":"70","author":"Jiao","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"151357","DOI":"10.1016\/j.ijmm.2019.151357","article-title":"Genotypic differences in CC224, CC363, CC449 and CC446 of Moraxella catarrhalis isolates based on whole genome SNP, MLST and PFGE typing","volume":"310","author":"Liu","year":"2019","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_32","first-page":"201","article-title":"Moraxella catarrhalis Macrolide-Resistant Isolates Are Highly Concentrated in Two MLST Clonal Complexes -CCN10 and CC363","volume":"8","author":"Liu","year":"2017","journal-title":"Front Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.diagmicrobio.2012.06.005","article-title":"Spectrum and potency of ceftaroline tested against leading pathogens causing community-acquired respiratory tract infections in Europe (2010)","volume":"75","author":"Farrell","year":"2013","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1099\/jmm.0.000076","article-title":"Prevalence and molecular analysis of macro-lide-resistant Moraxella catarrhalis clinical isolates in Japan, following emergence of the highly macrolide-resistant strain NSH1 in 2011","volume":"64","author":"Kasai","year":"2015","journal-title":"J. Med. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.diagmicrobio.2012.06.007","article-title":"Macrolide and tetracycline resistance among Moraxella catarrhalis isolates from 2009 to 2011","volume":"74","author":"Flamm","year":"2012","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1086\/383067","article-title":"Manual of clinical microbiology, 8th edition","volume":"38","author":"Murray","year":"2004","journal-title":"Clin. Infect. Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1178","DOI":"10.1099\/mic.0.2007\/015057-0","article-title":"Age-related genotypic and pheno-typic differences in Moraxella catarrhalis isolates from children and adults presenting with respiratory disease in 2001\u20132002","volume":"154","author":"Verhaegh","year":"2008","journal-title":"Microbiology (Reading)"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/9\/984\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:19:33Z","timestamp":1760141973000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/9\/984"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,29]]},"references-count":37,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["pathogens11090984"],"URL":"https:\/\/doi.org\/10.3390\/pathogens11090984","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,29]]}}}