The Emergence of Invasive Streptococcus pneumoniae Serotype 24F in Lebanon: Complete Genome Sequencing Reveals High Virulence and Antimicrobial Resistance Characteristics
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
33746930
PubMed Central
PMC7967862
DOI
10.3389/fmicb.2021.637813
Knihovny.cz E-resources
- Keywords
- Lebanon, Streptococcus pneumoniae, antibiotic resistance, serotype 24F, whole-genome sequencing,
- Publication type
- Journal Article MeSH
BACKGROUND: Invasive pneumococcal disease (IPD) remains a global health problem. IPD incidence has significantly decreased by the use of pneumococcal conjugate vaccines (PCV). Nevertheless, non-PCV serotypes remain a matter of concern. Eight Streptococcus pneumoniae serotype 24F isolates, belonging to a non-PCV serotype, were detected through the Lebanese Inter-Hospital Pneumococcal Surveillance Program. The aim of the study is to characterize phenotypic and genomic features of the 24F isolates in Lebanon. METHODS: WGS using long reads sequencing (PacBio) was performed to produce complete circular genomes and to determine clonality, antimicrobial resistance and virulence determinants. RESULTS: The sequencing results yielded eight closed circular genomes. Three multilocus sequence typing (MLST) types were identified (ST11618, ST14184, ST15253). Both MLST and WGS analyses revealed that these isolates from Lebanon were genetically homogenous belonging to clonal complex CC230 and clustered closely with isolates originating from Canada, United States of America, United Kingdom and Iceland. Their penicillin binding protein profiles correlated with both β-lactam susceptibility patterns and MLST types. Moreover, the isolates harbored the macrolide and tetracycline resistance genes and showed a similar virulence gene profile. To our knowledge, this study represents the first report of complete phenotypic and genomic characterization of the emerging Streptococcus pneumoniae, serotype 24F, in the Middle East and North Africa region.
Department of Laboratory and Blood Makassed General Hospital Beirut Lebanon
Department of Microbiology Nini Hospital Tripoli Lebanon
El Youssef Hospital Center Department of Clinical Laboratory Halba Lebanon
See more in PubMed
Aguiar S. I., Pinto F. R., Nunes S., Serrano I., Melo-Cristino J., Sa-Leao R., et al. (2010). Denmark14-230 clone as an increasing cause of pneumococcal infection in Portugal within a background of diverse serotype 19A lineages. J. Clin. Microbiol. 48(1), 101–108. 10.1128/JCM.00665-09 PubMed DOI PMC
Akdogan Kittana F. N., Mustak I. B., Hascelik G., Saricam S., Gurler N., Diker K. S. (2019). Erythromycin-resistant Streptococcus pneumoniae: phenotypes, genotypes, transposons and pneumococcal vaccine coverage rates. J. Med. Microbiol. 68(6), 874–881. 10.1099/jmm.0.000995 PubMed DOI
Alcock B. P., Raphenya A. R., Lau T. T. Y., Tsang K. K., Bouchard M., Edalatmand A., et al. (2020). CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucl. Acids Res. 48 D517–D525. 10.1093/nar/gkz935. PubMed DOI PMC
Al-Sheikh Y. A., Gowda K. L., Mohammed Ali M. M., John J., Khaled Homoud Mohammed D., Chikkabidare Shashidhar P. (2014). Distribution of serotypes and antibiotic susceptibility patterns among invasive pneumococcal diseases in Saudi Arabia. Ann. Lab. Med. 34 210–215. 10.3343/alm.2014.34.3.210. PubMed DOI PMC
Ansaldi F., Canepa P., de Florentiis D., Bandettini R., Durando P., Icardi G. (2011). Increasing incidence of Streptococcus pneumoniae serotype 19A and emergence of two vaccine escape recombinant ST695 strains in Liguria, Italy, 7 years after implementation of the 7-valent conjugated vaccine. Clin. Vaccine Immunol. 18(2), 343–345. 10.1128/CVI.00383-10 PubMed DOI PMC
Arbique J. C., Poyart C., Trieu-Cuot P., Quesne G., Carvalho Mda G., Steigerwalt A. G., et al. (2004). Accuracy of phenotypic and genotypic testing for identification of Streptococcus pneumoniae and description of Streptococcus pseudopneumoniae sp. nov. J. Clin. Microbiol. 42 4686–4696. 10.1128/JCM.42.10.4686-4696.2004 PubMed DOI PMC
Bahy R. H., Hamouda H. M., Shahat A. S., Yassin A. S., Amin M. A. (2016). Emergence of Neoteric Serotypes Among Multidrug Resistant Strains of Streptococcus pneumoniae Prevalent in Egypt. Jundishapur. J. Microbiol. 9:e30708. 10.5812/jjm.30708 PubMed DOI PMC
Balsells E., Dagan R., Yildirim I., Gounder P. P., Steens A., Munoz-Almagro C., et al. (2018). The relative invasive disease potential of Streptococcus pneumoniae among children after PCV introduction: A systematic review and meta-analysis. J. Infect. 77 368–378. 10.1016/j.jinf.2018.06.004 PubMed DOI
Balsells E., Guillot L., Nair H., Kyaw M. H. (2017). Serotype distribution of Streptococcus pneumoniae causing invasive disease in children in the post-PCV era: A systematic review and meta-analysis. PLoS One 12:e0177113. 10.1371/journal.pone.0177113 PubMed DOI PMC
Bentley S. D., Aanensen D. M., Mavroidi A., Saunders D., Rabbinowitsch E., Collins M., et al. (2006). Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2:e31. 10.1371/journal.pgen.0020031 PubMed DOI PMC
Brettin T., Davis J. J., Disz T., Edwards R. A., Gerdes S., Olsen G. J., et al. (2015). RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci. Rep. 5:8365. 10.1038/srep08365 PubMed DOI PMC
Calatayud L., Ardanuy C., Tubau F., Rolo D., Grau I., Pallares R., et al. (2010). Serotype and genotype replacement among macrolide-resistant invasive Pneumococci in adults: mechanisms of resistance and association with different transposons. J. Clin. Microbiol. 48(4), 1310–1316. 10.1128/JCM.01868-09 PubMed DOI PMC
Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., et al. (2009). BLAST+: architecture and applications. BMC Bioinform. 10:421. 10.1186/1471-2105-10-421 PubMed DOI PMC
Carattoli A., Zankari E., Garcia-Fernandez A., Voldby Larsen M., Lund O., Villa L., et al. (2014). In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58 3895–3903. 10.1128/AAC.02412-14 PubMed DOI PMC
Chan W. Y., Entwisle C., Ercoli G., Ramos-Sevillano E., McIlgorm A., Cecchini P., et al. (2019). A Novel, Multiple-Antigen Pneumococcal Vaccine Protects against Lethal Streptococcus pneumoniae Challenge. Infect. Immun. 87 846–818. 10.1128/IAI.00846-18 PubMed DOI PMC
Clinical and Laboratory Standards Institute [CLSI] (2019). Performance standards for antimicrobial susceptibility testing; twenty-third informational supplement. M100-S29. Weinstein, MP: Clinical and Laboratory Standards Institute.
Croucher N. J., Finkelstein J. A., Pelton S. I., Mitchell P. K., Lee G. M., Parkhill J., et al. (2013). Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat. Genet. 45 656–663. 10.1038/ng.2625 PubMed DOI PMC
Daniels C. C., Rogers P. D., Shelton C.M. (2016). A Review of Pneumococcal Vaccines: Current Polysaccharide Vaccine Recommendations and Future Protein Antigens. J. Pediatr. Pharmacol. Ther. 21 27–35. 10.5863/1551-6776-21.1.27 PubMed DOI PMC
Dewe T. C. M., D’Aeth J. C., Croucher N. J. (2019). Genomic epidemiology of penicillin-non-susceptible Streptococcus pneumoniae. Microb. Genom. 5:305. 10.1099/mgen.0.000305 PubMed DOI PMC
El Garch F., Lismond A., Piddock L. J., Courvalin P., Tulkens P. M., Van Bambeke F. (2010). Fluoroquinolones induce the expression of patA and patB, which encode ABC efflux pumps in Streptococcus pneumoniae. J. Antimicrob. Chemother. 65 2076–2082. 10.1093/jac/dkq287 PubMed DOI
El Moujaber G., Osman M., Rafei R., Dabboussi F., Hamze M. (2017). Molecular mechanisms and epidemiology of resistance in Streptococcus pneumoniae in the Middle East region. J. Med. Microbiol. 66 847–858. 10.1099/jmm.0.000503 PubMed DOI
Francisco A. P., Bugalho M., Ramirez M., Carrico J. A. (2009). Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinform. 10:152. 10.1186/1471-2105-10-152 PubMed DOI PMC
Gamez G., Castro A., Gomez-Mejia A., Gallego M., Bedoya A., Camargo M., et al. (2018). The variome of pneumococcal virulence factors and regulators. BMC Genomics 19:10. 10.1186/s12864-017-4376-0 PubMed DOI PMC
Ganaie F., Saad J. S., McGee L., van Tonder A. J., Bentley S. D., Lo S. W., et al. (2020). A New Pneumococcal Capsule Type, 10D, is the 100th Serotype and Has a Large cps Fragment from an Oral Streptococcus. mBio 11 937–20. 10.1128/mBio.00937-20. PubMed DOI PMC
Garcia-Suarez Mdel M., Vazquez F., Mendez F.J. (2006). Streptococcus pneumoniae virulence factors and their clinical impact: An update. Enferm. Infecc. Microbiol. Clin. 24 512–517. 10.1157/13092469 PubMed DOI
Global Burden of Disease Study (2018). Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect. Dis. 18 1191–1210. 10.1016/S1473-3099(18)30310-4 PubMed DOI PMC
Hanage W. P., Kaijalainen T. H., Syrjanen R. K., Auranen K., Leinonen M., Makela P. H., et al. (2005). Invasiveness of serotypes and clones of Streptococcus pneumoniae among children in Finland. Infect. Immun. 73 431–435. 10.1128/IAI.73.1.431-435.2005 PubMed DOI PMC
Hanna-Wakim R., Chehab H., Mahfouz I., Nassar F., Baroud M., Shehab M., et al. (2012). Epidemiologic characteristics, serotypes, and antimicrobial susceptibilities of invasive Streptococcus pneumoniae isolates in a nationwide surveillance study in Lebanon. Vaccine 30 G11–G17. 10.1016/j.vaccine.2012.07.020 PubMed DOI
Hausdorff W. P., Feikin D. R., Klugman K. P. (2005). Epidemiological differences among pneumococcal serotypes. Lancet Infect. Dis. 5 83–93. 10.1016/S1473-3099(05)01280-6 PubMed DOI
Hicks L. A., Harrison L. H., Flannery B., Hadler J. L., Schaffner W., Craig A. S., et al. (2007). Incidence of pneumococcal disease due to non-pneumococcal conjugate vaccine (PCV7) serotypes in the United States during the era of widespread PCV7 vaccination, 1998-2004. J. Infect. Dis. 196 1346–1354. 10.1086/521626 PubMed DOI
Isturiz R. E., Hall-Murray C., McLaughlin J. M., Snow V., Schmoele-Thoma B., Webber C., et al. (2018). Pneumococcal conjugate vaccine use for the prevention of pneumococcal disease in adults <50 years of age. Exp. Rev. Vacc. 17 45–55. 10.1080/14760584.2018.1411196 PubMed DOI
Janoir C., Lepoutre A., Gutmann L., Varon E. (2016). Insight Into Resistance Phenotypes of Emergent Non 13-valent Pneumococcal Conjugate Vaccine Type Pneumococci Isolated From Invasive Disease After 13-valent Pneumococcal Conjugate Vaccine Implementation in France. Open Forum. Infect. Dis. 3:ofw020. 10.1093/ofid/ofw020 PubMed DOI PMC
Kapatai G., Sheppard C. L., Al-Shahib A., Litt D. J., Underwood A. P., Harrison T. G., et al. (2016). Whole genome sequencing of Streptococcus pneumoniae: development, evaluation and verification of targets for serogroup and serotype prediction using an automated pipeline. PeerJ 4:e2477. 10.7717/peerj.2477 PubMed DOI PMC
Kavalari I. D., Fuursted K., Krogfelt K. A., Slotved H. C. (2019). Molecular characterization and epidemiology of Streptococcus pneumoniae serotype 24F in Denmark. Sci. Rep. 9:5481. 10.1038/s41598-019-41983-8 PubMed DOI PMC
Kawabata T., Tenokuchi Y., Yamakuchi H., Sameshima H., Katayama H., Ota T., et al. (2020). Concurrent Bacteremia Due to Non-vaccine Serotype 24F Pneumococcus in Twins: A Rapid Increase in Serotype 24F-invasive Pneumococcal Disease and its High Invasive Potential. Pediatr. Infect. Dis. J. 39 85–87. 10.1097/INF.0000000000002508 PubMed DOI
Kleinheinz K. A., Joensen K. G., Larsen M. V. (2014). Applying the ResFinder and VirulenceFinder web-services for easy identification of acquired antibiotic resistance and E. coli virulence genes in bacteriophage and prophage nucleotide sequences. Bacteriophage 4:e27943. 10.4161/bact.27943 PubMed DOI PMC
Larsen M. V., Cosentino S., Rasmussen S., Friis C., Hasman H., Marvig R. L., et al. (2012). Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50 1355–1361. 10.1128/JCM.06094-11 PubMed DOI PMC
Li Y., Metcalf B. J., Chochua S., Li Z., Gertz R. E., Jr., Walker H., et al. (2016). Penicillin-Binding Protein Transpeptidase Signatures for Tracking and Predicting beta-Lactam Resistance Levels in Streptococcus pneumoniae. mBio 7 756–16. 10.1128/mBio.00756-16. PubMed DOI PMC
Liu B., Zheng D., Jin Q., Chen L., Yang J. (2019). VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 47 D687–D692. 10.1093/nar/gky1080. PubMed DOI PMC
Lo S. W., Gladstone R. A., van Tonder A. J., Du Plessis M., Cornick J. E., Hawkins P. A., et al. (2020). A mosaic tetracycline resistance gene tet(S/M) detected in an MDR pneumococcal CC230 lineage that underwent capsular switching in South Africa. J. Antimicrob. Chemother. 75 512–520. 10.1093/jac/dkz477 PubMed DOI PMC
Lo S. W., Gladstone R. A., van Tonder A. J., Lees J. A., du Plessis M., Benisty R., et al. (2019). Pneumococcal lineages associated with serotype replacement and antibiotic resistance in childhood invasive pneumococcal disease in the post-PCV13 era: an international whole-genome sequencing study. Lancet Infect. Dis. 19 759–769. 10.1016/S1473-3099(19)30297-X PubMed DOI PMC
Matanock A., Lee G., Gierke R., Kobayashi M., Leidner A., Pilishvili T. (2019). Use of 13-Valent Pneumococcal Conjugate Vaccine and 23-Valent Pneumococcal Polysaccharide Vaccine Among Adults Aged >/=65 Years: Updated Recommendations of the Advisory Committee on Immunization Practices. MMWR Morb. Mortal. Wkly. Rep. 68 1069–1075. 10.15585/mmwr.mm6846a5 PubMed DOI PMC
Mayanskiy N., Savinova T., Alyabieva N., Ponomarenko O., Brzhozovskaya E., Lazareva A., et al. (2017). Antimicrobial resistance, penicillin-binding protein sequences, and pilus islet carriage in relation to clonal evolution of Streptococcus pneumoniae serotype 19A in Russia, 2002-2013. Epidemiol. Infect. 145 1708–1719. 10.1017/S0950268817000541 PubMed DOI PMC
Moghnieh R., Awad L., Abdallah D., Sleiman R., Jisr T., Tamim H., et al. (2018). Epidemiology of pneumococcal infections in hospitalised adult patients in Lebanon with a highlight on non-invasive disease. J. Infect. Dev. Ctries 12:20S. 10.3855/jidc.10106. PubMed DOI
Moghnieh R., Tamim H., Awad L., Abdallah D., Sleiman R., Jisr T., et al. (2020). Epidemiology of invasive and non-invasive pneumococcal infections in hospitalised adult patients in a Lebanese medical centre, 2006-2015. J. Infect. Public Health 13 2092–2100. 10.1016/j.jiph.2019.03.003 PubMed DOI
Mokaddas E., Albert M. J. (2012). Impact of pneumococcal conjugate vaccines on burden of invasive pneumococcal disease and serotype distribution of Streptococcus pneumoniae isolates: an overview from Kuwait. Vaccine 30 G37–G40. 10.1016/j.vaccine.2012.10.061 PubMed DOI
Munoz-Almagro C., Ciruela P., Esteva C., Marco F., Navarro M., Bartolome R., et al. (2011). Serotypes and clones causing invasive pneumococcal disease before the use of new conjugate vaccines in Catalonia, Spain. J. Infect. 63(2), 151–162. 10.1016/j.jinf.2011.06.002 PubMed DOI
Namkoong H., Ishii M., Funatsu Y., Kimizuka Y., Yagi K., Asami T., et al. (2016). Theory and strategy for Pneumococcal vaccines in the elderly. Hum. Vaccin. Immunother. 12 336–343. 10.1080/21645515.2015.1075678 PubMed DOI PMC
Ouldali N., Levy C., Varon E., Bonacorsi S., Bechet S., Cohen R., et al. (2018). Incidence of paediatric pneumococcal meningitis and emergence of new serotypes: a time-series analysis of a 16-year French national survey. Lancet Infect. Dis. 18 983–991. 10.1016/S1473-3099(18)30349-9 PubMed DOI
Pitsiou G. G., Kioumis I. P. (2011). Pneumococcal vaccination in adults: does it really work? Respir. Med. 105 1776–1783. 10.1016/j.rmed.2011.07.008 PubMed DOI
Price M. N., Dehal P. S., Arkin A. P. (2010). FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. 10.1371/journal.pone.0009490 PubMed DOI PMC
Principi N., Di Cara G., Bizzarri I., Isidori C., Borgia P., Mignini C., et al. (2018). Prevention of Invasive Pneumococcal Disease: Problems Emerged After Some Years of the 13-Valent Pneumococcal Conjugate Vaccine Use. Curr. Infect. Dis. Rep. 20:1. 10.1007/s11908-018-0607-z PubMed DOI
Reinert R. R., Ringelstein A., van der Linden M., Cil M. Y., Al-Lahham A., Schmitz F. J. (2005). Molecular epidemiology of macrolide-resistant Streptococcus pneumoniae isolates in Europe. J. Clin. Microbiol. 43 1294–1300. 10.1128/JCM.43.3.1294-1300.2005 PubMed DOI PMC
Sadowy E., Kuch A., Gniadkowski M., Hryniewicz W. (2010). Expansion and evolution of the Streptococcus pneumoniae Spain9V-ST156 clonal complex in Poland. Antimicrob. Agents Chemother. 54(5), 1720–1727. 10.1128/AAC.01340-09 PubMed DOI PMC
Schroeder M. R., Stephens D. S. (2016). Macrolide Resistance in Streptococcus pneumoniae. Front. Cell Infect. Microbiol. 6:98. 10.3389/fcimb.2016.00098 PubMed DOI PMC
Taha N., Araj G. F., Wakim R. H., Kanj S. S., Kanafani Z. A., Sabra A., et al. (2012). Genotypes and serotype distribution of macrolide resistant invasive and non-invasive Streptococcus pneumoniae isolates from Lebanon. Ann. Clin. Microbiol. Antimicrob. 11:2. 10.1186/1476-0711-11-2 PubMed DOI PMC
Treangen T. J., Ondov B. D., Koren S., Phillippy A. M. (2014). The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 15:524. 10.1186/s13059-014-0524-x PubMed DOI PMC
Varon E., Cohen R., Bechet S., Doit C., Levy C. (2015). Invasive disease potential of pneumococci before and after the 13-valent pneumococcal conjugate vaccine implementation in children. Vaccine 33 6178–6185. 10.1016/j.vaccine.2015.10.015 PubMed DOI
Vestrheim D. F., Steinbakk M., Aaberge I. S., Caugant D. A. (2012). Postvaccination increase in serotype 19A pneumococcal disease in Norway is driven by expansion of penicillin-susceptible strains of the ST199 complex. Clin. Vaccine Immunol. 19 443–445. 10.1128/CVI.05563-11 PubMed DOI PMC
Weinberger D. M., Malley R., Lipsitch M. (2011). Serotype replacement in disease after pneumococcal vaccination. Lancet 378 1962–1973. 10.1016/S0140-6736(10)62225-8 PubMed DOI PMC
World Health Organization (2007). Pneumococcal conjugate vaccine for childhood immunization — WHO position paper. Weekly Epidemiological Record = Relevé épidémiologique hebdomadaire, Geneva: World Health Organization, 82ı, 93–104. PubMed
Zankari E., Hasman H., Cosentino S., Vestergaard M., Rasmussen S., Lund O., et al. (2012). Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67 2640–2644. 10.1093/jac/dks261 PubMed DOI PMC