{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,9,9]],"date-time":"2025-09-09T21:56:31Z","timestamp":1757454991136,"version":"3.37.3"},"reference-count":42,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2022,10,12]],"date-time":"2022-10-12T00:00:00Z","timestamp":1665532800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100009947","name":"Merck Sharp and Dohme","doi-asserted-by":"publisher","award":["60164"],"award-info":[{"award-number":["60164"]}],"id":[{"id":"10.13039\/100009947","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>Data related to carriage of <jats:italic>Streptococcus pneumoniae<\/jats:italic> (Spn) and antimicrobial resistance patterns in middle-aged and older adults are limited. We assessed the carriage of Spn, and its antibiotic resistance patterns, among participants \u226550 years of age living in the city of Novi Sad during the second year of COVID-19 pandemic.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>Analysis of prospectively collected data among participants with or without symptoms of upper respiratory tract infection who visited their elected physicians in the Primary Health Care Centre of Novi Sad (outpatient facility) was conducted from May 18, 2021 to December 7, 2021. Both nasopharyngeal (NP) and oropharyngeal (OP) samples from each participant were collected.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>A total of 1042 samples from 521 study subjects (1 NP and 1 OP sample from each person) were collected. Sixteen samples from the same number of persons (3.1%, 95% confidence interval: 1.76%-4.94%) were culture positive for the presence of Spn. Overall, the median age of study participants was 71 years (range, 50\u201393 years; 90th percentile, 77 years), and most (197\/521, 37.8%) of them were 70\u201379 years of age. A majority of the study subjects were: females (324\/521; 62.2%), sampled during May and June 2021 (376\/521, 72.2%), those who did not have contact with children aged 0\u201310 years in the family (403\/521; 77.4%), without smokers in the household (443\/521; 85.0%), and those who did not receive vaccine against Spn (519\/521; 99.6%). Out of 16 Spn positive samples, for six participants, Spn carriage serotypes were obtained and there were four vaccine (6A, 11A, 15B, and 18C) serotypes, and two (6C and 35F) non-vaccine serotypes. Remaining 10 (62.50%) samples were non-typeable isolates of pneumococci. Among four vaccine serotypes, two (6A and 18C) were represented in PCV13, and 18C along with the other two (11A and 15B) in PPSV23 vaccine. The highest level of resistance of Spn isolates was observed for erythromycin, (10 or 62.50%), and tetracycline, (7 or 43.75%), one isolate showed resistance to penicillin, ampicillin, and amoxicillin\/amoxicillin-clavulanic acid, while none of them were resistant to ceftriaxone, trimethoprim\/sulfamethoxazole and levofloxacin. There were three multi-drug resistant isolates; one was identified as 6C (non-vaccine serotype), and two other were non-typeable isolates of Spn.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusions<\/jats:title>\n<jats:p>In this first study conducted in Serbia on Spn carriage in adults \u226550 years of age, we found low prevalence of Spn carriage and identified 6 serotypes of Spn, four of which were represented in vaccines. These results may support future Spn colonization studies among middle-aged and older adults.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0274674","type":"journal-article","created":{"date-parts":[[2022,10,12]],"date-time":"2022-10-12T17:33:50Z","timestamp":1665596030000},"page":"e0274674","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["Pneumococcal carriage in adults aged 50 years and older in outpatient health care facility during pandemic COVID-19 in Novi Sad, 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adults and children in community and family settings","volume":"38","author":"G Regev-Yochay","year":"2004","journal-title":"Clin Infect Dis"},{"issue":"5","key":"pone.0274674.ref008","doi-asserted-by":"crossref","first-page":"1851","DOI":"10.1128\/JCM.40.5.1851-1853.2002","article-title":"Household transmission of Streptococcus pneumoniae among siblings with acute otitis media","volume":"40","author":"J Shimada","year":"2002","journal-title":"J Clin Microbiol"},{"issue":"10","key":"pone.0274674.ref009","doi-asserted-by":"crossref","first-page":"2094","DOI":"10.1111\/jgs.13651","article-title":"Pneumococcal Carriage and Vaccine Coverage in Retirement Community Residents","volume":"63","author":"S Becker-Dreps","year":"2015","journal-title":"J Am Geriatr Soc"},{"issue":"1","key":"pone.0274674.ref010","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s40121-014-0025-y","article-title":"Epidemiology of pneumococcal disease in a national cohort of older adults","volume":"3","author":"HJ Morrill","year":"2014","journal-title":"Infect Dis Ther"},{"issue":"6","key":"pone.0274674.ref011","doi-asserted-by":"crossref","first-page":"e364","DOI":"10.1016\/j.ijid.2013.01.004","article-title":"Regional epidemiology of invasive pneumococcal disease in Asian adults: epidemiology, disease burden, serotype distribution, and antimicrobial resistance patterns and prevention","volume":"17","author":"IF Hung","year":"2013","journal-title":"Int J Infect Dis"},{"issue":"9\u201310","key":"pone.0274674.ref012","doi-asserted-by":"crossref","first-page":"521","DOI":"10.2298\/SARH1610521P","article-title":"Streptococcus pneumoniae serotype distribution in Vojvodina before the introduction of pneumococcal conjugate vaccines into the National Immunization Program","volume":"144","author":"V Petrovi\u0107","year":"2016","journal-title":"Srp Arh Celok Lek"},{"issue":"1","key":"pone.0274674.ref013","doi-asserted-by":"crossref","first-page":"3509","DOI":"10.1038\/s41598-018-21837-5","article-title":"Nasopharyngeal Pneumococcal Carriage in Nigeria: a two-site, population-based survey","volume":"8","author":"IMO Adetifa","year":"2018","journal-title":"Sci Rep"},{"key":"pone.0274674.ref014","unstructured":"Pravilnik o imunizaciji i na\u010dinu za\u0161tite lekovima, Slu\u017ebeni glasnik Republike Srbije br. 88\/2017, 11\/2018, 14\/2018, 45\/2018, 48\/2018, 58\/2018, 104\/2018. Available from: https:\/\/www.paragraf.rs\/propisi\/pravilnik_o_imunizaciji_i_nacinu_zastite_lekovima.html. Serbian. [accessed December 10, 2021]."},{"key":"pone.0274674.ref015","unstructured":"Zakon o za\u0161titi stanovni\u0161tva od zaraznih bolesti, Slu\u017ebeni glasnik Republike Srbije br. 15\/2016. Available from: http:\/\/www.paragraf. rs\/propisi\/zakon_o_zastiti_stanovnistva_od_zaraznih_bolesti.html. Serbian. [accessed December 15, 2021]."},{"key":"pone.0274674.ref016","unstructured":"Institut za javno zdravlje Srbije \u201eDr Milan Jovanovi\u0107 Batut\u201c. Stru\u010dno-metodolo\u0161ko uputstvo za sprovo\u0111enje obavezne i preporu\u010dene imunizacije stanovni\u0161tva za 2021. godinu. 2021. Available from: https:\/\/dzgm.rs\/dokumenta\/SMU%20za%202021.%20godinu%20(1).pdf Serbian. [accessed December 20, 2021]."},{"key":"pone.0274674.ref017","first-page":"9","article-title":"Practical Issues in Calculating the Sample Size for Prevalence Studies","volume":"1","author":"L Naing","year":"2006","journal-title":"Archives of Orofacial Sciences"},{"issue":"1","key":"pone.0274674.ref018","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.vaccine.2013.08.062","article-title":"Standard method for detecting upper respiratory carriage of Streptococcus pneumoniae: updated recommendations from the World Health Organization Pneumococcal Carriage Working Group","volume":"32","author":"C Satzke","year":"2013","journal-title":"Vaccine"},{"issue":"2","key":"pone.0274674.ref019","first-page":"229","article-title":"Study of the ability of two swab transport systems to maintain viability of clinically important bacteria","volume":"46","author":"AL Horacio","year":"2012","journal-title":"Acta bioqu\u00edmica cl\u00ednica latinoamericana"},{"key":"pone.0274674.ref020","unstructured":"CDC. Fast Extraction of DNA for Streptococcal culture isolates. Available from: https:\/\/www.cdc.gov\/streplab\/downloads\/pcr-dna-extraction-culture-may2009.pdf [accessed December 25, 2021]."},{"issue":"8","key":"pone.0274674.ref021","doi-asserted-by":"crossref","first-page":"2460","DOI":"10.1128\/JCM.02498-06","article-title":"Evaluation and improvement of real-time PCR assays targeting lytA, ply, and psaA genes for detection of pneumococcal DNA","volume":"45","author":"G Carvalho Mda","year":"2007","journal-title":"J Clin Microbiol"},{"issue":"6","key":"pone.0274674.ref022","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1093\/jac\/48.6.915","article-title":"Evaluation of PCR primers to screen for Streptococcus pneumoniae isolates and beta-lactam resistance, and to detect common macrolide resistance determinants","volume":"48","author":"K Nagai","year":"2001","journal-title":"J Antimicrob Chemother"},{"issue":"3","key":"pone.0274674.ref023","first-page":"156","article-title":"Detection of lytA, pspC, and rrgA genes in Streptococcus pneumoniae isolated from healthy children","volume":"7","author":"T Gholamhosseini-Moghaddam","year":"2015","journal-title":"Iran J Microbiol"},{"issue":"5","key":"pone.0274674.ref024","doi-asserted-by":"crossref","first-page":"1611","DOI":"10.1128\/JCM.02243-09","article-title":"Revisiting pneumococcal carriage by use of broth enrichment and PCR techniques for enhanced detection of carriage and serotypes","volume":"48","author":"M da Gloria Carvalho","year":"2010","journal-title":"J Clin Microbiol"},{"key":"pone.0274674.ref025","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1186\/1471-2334-11-100","article-title":"Sequential multiplex PCR assay for determining capsular serotypes of colonizing S. pneumoniae","volume":"11","author":"S Jourdain","year":"2011","journal-title":"BMC Infect Dis"},{"issue":"8","key":"pone.0274674.ref026","doi-asserted-by":"crossref","first-page":"2470","DOI":"10.1128\/JCM.00484-09","article-title":"Simple, accurate, serotype-specific PCR assay to differentiate Streptococcus pneumoniae serotypes 6A, 6B, and 6C","volume":"47","author":"P Jin","year":"2009","journal-title":"J Clin Microbiol"},{"issue":"1","key":"pone.0274674.ref027","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1128\/JCM.44.1.124-131.2006","article-title":"Sequential multiplex PCR approach for determining capsular serotypes of Streptococcus pneumoniae isolates","volume":"44","author":"R Pai","year":"2006","journal-title":"J Clin Microbiol"},{"key":"pone.0274674.ref028","unstructured":"The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 11.0, 2021. Available from: http:\/\/www.eucast.org [accessed December 22, 2021]."},{"issue":"9","key":"pone.0274674.ref029","doi-asserted-by":"crossref","first-page":"1590","DOI":"10.1093\/infdis\/jiaa558","article-title":"Dynamics of Pneumococcal Carriage in Adults: A New Look at an Old Paradigm","volume":"223","author":"ST Almeida","year":"2021","journal-title":"J Infect Dis"},{"issue":"6","key":"pone.0274674.ref030","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1086\/319246","article-title":"Pneumococcal carriage and otitis media induce salivary antibodies to pneumococcal surface adhesin a, pneumolysin, and pneumococcal surface protein a in children","volume":"183","author":"B Simell","year":"2001","journal-title":"J Infect Dis"},{"issue":"5","key":"pone.0274674.ref031","doi-asserted-by":"crossref","first-page":"e38271","DOI":"10.1371\/journal.pone.0038271","article-title":"A longitudinal study of Streptococcus pneumoniae carriage in a cohort of infants and their mothers on the Thailand-Myanmar border","volume":"7","author":"P Turner","year":"2012","journal-title":"PLoS One"},{"issue":"1","key":"pone.0274674.ref032","doi-asserted-by":"crossref","first-page":"e79578","DOI":"10.1371\/journal.pone.0079578","article-title":"Nasopharyngeal carriage and transmission of Streptococcus pneumoniae in American Indian households after a decade of pneumococcal conjugate vaccine use","volume":"9","author":"JF Mosser","year":"2014","journal-title":"PLoS One"},{"issue":"3","key":"pone.0274674.ref033","doi-asserted-by":"crossref","first-page":"e60520","DOI":"10.1371\/journal.pone.0060520","article-title":"Superiority of trans-oral over trans-nasal sampling in detecting Streptococcus pneumoniae colonization in adults","volume":"8","author":"K Trzci\u0144ski","year":"2013","journal-title":"PLoS One"},{"issue":"1","key":"pone.0274674.ref034","doi-asserted-by":"crossref","first-page":"8373","DOI":"10.1038\/s41598-020-65399-x","article-title":"Re-evaluation of Streptococcus pneumoniae carriage in Portuguese elderly by qPCR increases carriage estimates and unveils an expanded pool of serotypes","volume":"10","author":"ST Almeida","year":"2020","journal-title":"Sci Rep"},{"issue":"3","key":"pone.0274674.ref035","first-page":"172","article-title":"Nasopharyngeal carriage of Streptococcus pneumoniae and serotypes indentified among nursing home residents in comparison to the elderly and patients younger than 65 years living in domestic environment","volume":"56","author":"M Kol\u0161ek-\u0160u\u0161ter\u0161i\u010d","year":"2017","journal-title":"Zdr Varst"},{"issue":"8","key":"pone.0274674.ref036","doi-asserted-by":"crossref","first-page":"e0221525","DOI":"10.1371\/journal.pone.0221525","article-title":"Nasopharyngeal carriage of Streptococcus pneumoniae, Haemophilus influenzae, and Staphylococcus aureus in a Brazilian elderly cohort","volume":"14","author":"RC Zanella","year":"2019","journal-title":"PLoS One"},{"issue":"5","key":"pone.0274674.ref037","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s40266-013-0060-5","article-title":"Preventing pneumococcal disease in the elderly: recent advances in vaccines and implications for clinical practice","volume":"30","author":"A Vila-Corcoles","year":"2013","journal-title":"Drugs Aging"},{"issue":"12","key":"pone.0274674.ref038","doi-asserted-by":"crossref","first-page":"O1145","DOI":"10.1111\/1469-0691.12752","article-title":"Density and duration of experimental human pneumococcal carriage","volume":"20","author":"JF Gritzfeld","year":"2014","journal-title":"Clin Microbiol Infect"},{"issue":"7","key":"pone.0274674.ref039","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1586\/erv.12.53","article-title":"The fundamental link between pneumococcal carriage and disease","volume":"11","author":"Pneumococcal Carriage Group","year":"2012","journal-title":"Expert Rev Vaccines"},{"issue":"5","key":"pone.0274674.ref040","doi-asserted-by":"crossref","first-page":"1802","DOI":"10.1073\/pnas.1812388116","article-title":"Unraveling the seasonal epidemiology of pneumococcus","volume":"116","author":"M Domenech de Cell\u00e8s","year":"2019","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1","key":"pone.0274674.ref041","doi-asserted-by":"crossref","first-page":"e0246122","DOI":"10.1371\/journal.pone.0246122","article-title":"Streptococcus pneumoniae carriage and antibiotic susceptibility among Indonesian pilgrims during the Hajj pilgrimage in 2015","volume":"16","author":"K Harimurti","year":"2021","journal-title":"PLoS One"},{"key":"pone.0274674.ref042","unstructured":"Institute of Public Health of Vojvodina. [Actual epidemiological situation of COVID-19 in Vojvodina]. Novi Sad: Institute of Public Health of Vojvodina; 2021. 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