-
Rise of multidrug-resistant non-vaccine serotype 15A Streptococcus pneumoniae in the United Kingdom, 2001 to 2014
- Carmen Sheppard1 , Norman K. Fry1 , Shazad Mushtaq2 , Neil Woodford2 , Rosy Reynolds4,5 , Regina Janes6 , Rachel Pike2 , Robert Hill2 , Maimuna Kimuli2 , Peter Staves2 , Michel Doumith2 , Timothy Harrison2 , David M Livermore2,3
-
View Affiliations Hide AffiliationsAffiliations: 1 Respiratory and Vaccine Preventable Bacteria Reference Unit, Public Health England, London, United Kingdom 2 Antimicrobial Resistance and Healthcare Associated Infections Reference Unit, Public Health England, London, United Kingdom 3 Norwich Medical School, University of East Anglia, Norwich, United Kingdom 4 Southmead Hospital, Bristol, United Kingdom 5 British Society for Antimicrobial Chemotherapy, Birmingham, United Kingdom 6 LGC, Fordham, United KingdomDavid Livermored.livermore uea.ac.uk
-
View Citation Hide Citation
Citation style for this article: Sheppard Carmen, Fry Norman K., Mushtaq Shazad, Woodford Neil, Reynolds Rosy, Janes Regina, Pike Rachel, Hill Robert, Kimuli Maimuna, Staves Peter, Doumith Michel, Harrison Timothy, Livermore David M. Rise of multidrug-resistant non-vaccine serotype 15A Streptococcus pneumoniae in the United Kingdom, 2001 to 2014. Euro Surveill. 2016;21(50):pii=30423. https://doi.org/10.2807/1560-7917.ES.2016.21.50.30423 Received: 19 Mar 2016; Accepted: 17 Aug 2016
Abstract
Conjugate vaccines have reduced pneumococcal disease in vaccinated children and unvaccinated adults, but non-vaccine serotypes are of concern, particularly if antibiotic resistant. We reviewed Streptococcus pneumoniae collected via: (i) the British Society for Antimicrobial Chemotherapy (BSAC) surveillances from 2001–2014; (ii) Public Health England’s (PHE) invasive isolate surveillance from 2005–2014 and (iii) referral to PHE for resistance investigation from 2005–2014. Serotype 15A increased in all series, with many representatives showing triple resistance to macrolides, tetracyclines and penicillin. 15A was consistently among the 10 most prevalent serotypes from 2011 in PHE and BSAC invasive isolate/bacteraemia surveillance but never previously; 26–33% of these invasive 15A isolates had triple resistance. BSAC respiratory isolates were only serotyped in 2013/14 and 2014/15 (October to September); 15A was most prevalent serotype in both periods, comprising 9–11% of isolates, 38–48% of them with triple resistance. Serotype 15A represented 0–4% of S. pneumoniae referred to PHE for reference investigation annually until 2008 but rose to 29% (2013) and 32% (2014). Almost all multidrug-resistant 15A isolates were sequence type (ST) 63 variants, whereas susceptible 15A isolates were clonally diverse. The rise of serotype 15A suggests that pneumococcal conjugate vaccines will need ongoing adaptation.

Article metrics loading...

-
From This Site
/content/10.2807/1560-7917.ES.2016.21.50.30423dcterms_title,dcterms_subject,pub_keyword-contentType:Journal -contentType:Contributor -contentType:Concept -contentType:Institution105 -
PubMed
-
Google Scholar

Full text loading...
References
-
Isaacman DJ, Fletcher MA, Fritzell B, Ciuryla V, Schranz J. Indirect effects associated with widespread vaccination of infants with heptavalent pneumococcal conjugate vaccine (PCV7; Prevnar). Vaccine. 2007;25(13):2420-7. https://doi.org/10.1016/j.vaccine.2006.09.011 PMID: 17049677
-
Rodrigo C, Bewick T, Sheppard C, Greenwood S, Macgregor V, Trotter C, et al. Pneumococcal serotypes in adult non-invasive and invasive pneumonia in relation to child contact and child vaccination status. Thorax. 2014;69(2):168-73. https://doi.org/10.1136/thoraxjnl-2013-203987 PMID: 24048505
-
Myint TT, Madhava H, Balmer P, Christopoulou D, Attal S, Menegas D, et al. The impact of 7-valent pneumococcal conjugate vaccine on invasive pneumococcal disease: a literature review. Adv Ther. 2013;30(2):127-51. https://doi.org/10.1007/s12325-013-0007-6 PMID: 23397399
-
Isaacman DJ, Strutton DR, Kalpas EA, Horowicz-Mehler N, Stern LS, Casciano R, et al. The impact of indirect (herd) protection on the cost-effectiveness of pneumococcal conjugate vaccine. Clin Ther. 2008;30(2):341-57. https://doi.org/10.1016/j.clinthera.2008.02.003 PMID: 18343273
-
Song JH, Dagan R, Klugman KP, Fritzell B. The relationship between pneumococcal serotypes and antibiotic resistance. Vaccine. 2012;30(17):2728-37. https://doi.org/10.1016/j.vaccine.2012.01.091 PMID: 22330126
-
Dagan R, Klugman KP. Impact of conjugate pneumococcal vaccines on antibiotic resistance. Lancet Infect Dis. 2008;8(12):785-95. https://doi.org/10.1016/S1473-3099(08)70281-0 PMID: 19022193
-
Miller E, Andrews NJ, Waight PA, Slack MP, George RC. Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: an observational cohort study. Lancet Infect Dis. 2011;11(10):760-8. https://doi.org/10.1016/S1473-3099(11)70090-1 PMID: 21621466
-
Henderson KL, Muller-Pebody B, Blackburn RM, Johnson AP. Reduction in erythromycin resistance in invasive pneumococci from young children in England and Wales. J Antimicrob Chemother. 2010;65(2):369-70. https://doi.org/10.1093/jac/dkp442 PMID: 20007730
-
Clarke SC, Scott KJ, McChlery SM. Erythromycin resistance in invasive serotype 14 pneumococci is highly related to clonal type. J Med Microbiol. 2004;53(Pt 11):1101-3. https://doi.org/10.1099/jmm.0.45737-0 PMID: 15496387
-
Reinert R, Jacobs MR, Kaplan SL. Pneumococcal disease caused by serotype 19A: review of the literature and implications for future vaccine development. Vaccine. 2010;28(26):4249-59. https://doi.org/10.1016/j.vaccine.2010.04.020 PMID: 20416266
-
Liñares J, Ardanuy C, Pallares R, Fenoll A. Changes in antimicrobial resistance, serotypes and genotypes in Streptococcus pneumoniae over a 30-year period. Clin Microbiol Infect. 2010;16(5):402-10. https://doi.org/10.1111/j.1469-0691.2010.03182.x PMID: 20132251
-
van Hoek AJ, Sheppard CL, Andrews NJ, Waight PA, Slack MP, Harrison TG, et al. Pneumococcal carriage in children and adults two years after introduction of the thirteen valent pneumococcal conjugate vaccine in England. Vaccine. 2014;32(34):4349-55. https://doi.org/10.1016/j.vaccine.2014.03.017 PMID: 24657717
-
Waight PA, Andrews NJ, Ladhani SN, Sheppard CL, Slack MP, Miller E. Effect of the 13-valent pneumococcal conjugate vaccine on invasive pneumococcal disease in England and Wales 4 years after its introduction: an observational cohort study. Lancet Infect Dis. 2015;15(5):535-43. https://doi.org/10.1016/S1473-3099(15)70044-7 PMID: 25801458
-
Ozawa D, Yano H, Endo S, Hidaka H, Kakuta R, Okitsu N, et al. Impact of the Seven-valent Pneumococcal Conjugate Vaccine on Acute Otitis Media in Japanese Children: Emergence of Serotype 15A Multidrug-resistant Streptococcus pneumoniae in Middle Ear Fluid Isolates. Pediatr Infect Dis J. 2015;34(9):e217-21. https://doi.org/10.1097/INF.0000000000000776 PMID: 26083590
-
Suga S, Chang B, Asada K, Akeda H, Nishi J, Okada K, et al. Nationwide population-based surveillance of invasive pneumococcal disease in Japanese children: Effects of the seven-valent pneumococcal conjugate vaccine. Vaccine. 2015;33(45):6054-60. https://doi.org/10.1016/j.vaccine.2015.07.069 PMID: 26235372
-
Ho PL, Chiu SS, Law PY, Chan EL, Lai EL, Chow KH. Increase in the nasopharyngeal carriage of non-vaccine serogroup 15 Streptococcus pneumoniae after introduction of children pneumococcal conjugate vaccination in Hong Kong. Diagn Microbiol Infect Dis. 2015;81(2):145-8. https://doi.org/10.1016/j.diagmicrobio.2014.11.006 PMID: 25483278
-
Richter SS, Diekema DJ, Heilmann KP, Dohrn CL, Riahi F, Doern GV. Changes in pneumococcal serotypes and antimicrobial resistance after introduction of the 13-valent conjugate vaccine in the United States. Antimicrob Agents Chemother. 2014;58(11):6484-9. https://doi.org/10.1128/AAC.03344-14 PMID: 25136018
-
Golden AR, Adam HJ, Gilmour MW, Baxter MR, Martin I, Nichol KA, et al. Assessment of multidrug resistance, clonality and virulence in non-PCV-13 Streptococcus pneumoniae serotypes in Canada, 2011-13. J Antimicrob Chemother. 2015;70(7):1960-4. PMID: 25761605
-
Steens A, Bergsaker MA, Aaberge IS, Rønning K, Vestrheim DF. Prompt effect of replacing the 7-valent pneumococcal conjugate vaccine with the 13-valent vaccine on the epidemiology of invasive pneumococcal disease in Norway. Vaccine. 2013;31(52):6232-8. https://doi.org/10.1016/j.vaccine.2013.10.032 PMID: 24176490
-
Mameli C, Fabiano V, Daprai L, Bedogni G, Faccini M, Garlaschi ML, et al. A longitudinal study of streptococcus pneumoniae carriage in healthy children in the 13-valent pneumococcal conjugate vaccine era. Hum Vaccin Immunother. 2015;11(4):811-7. https://doi.org/10.1080/21645515.2015.1010945 PMID: 25751237
-
Strachan JE, Rowe SL, Dunne EM, Hogg GG. Emergence of Streptococcus pneumoniae serotype 15A after the introduction of the conjugate vaccine in Victoria. Med J Aust. 2013;199(7):461-3. https://doi.org/10.5694/mja13.10420 PMID: 24099202
-
British Society for Antimicrobial Chemotherapy (BSAC) Resistance Surveillance Project. [Accessed 15 July 2016]. Available from: http://www.bsacsurv.org/
-
Reynolds R, Hope R, Williams LBSAC Working Parties on Resistance Surveillance. Survey, laboratory and statistical methods for the BSAC Resistance Surveillance Programmes. J Antimicrob Chemother. 2008;62(Suppl 2):ii15-28. https://doi.org/10.1093/jac/dkn349 PMID: 18819976
-
Farrell DJ, Felmingham D, Shackcloth J, Williams L, Maher K, Hope R, et al. BSAC Working Parties on Resistance Surveillance. Non-susceptibility trends and serotype distributions among Streptococcus pneumoniae from community-acquired respiratory tract infections and from bacteraemias in the UK and Ireland, 1999 to 2007. J Antimicrob Chemother. 2008;62(Suppl 2):ii87-95. https://doi.org/10.1093/jac/dkn355 PMID: 18819983
-
European Antimicrobial Resistance Surveillance Network (EARS-Net). [Accessed 15 July 2016]. Available from: http://ecdc.europa.eu/en/healthtopics/antimicrobial-resistance-and-consumption/antimicrobial_resistance/EARS-Net/Pages/EARS-Net.aspx
-
Lund E, Henrichsen J. Laboratory diagnosis, serology and epidemiology of Streptococcus pneumoniae. In: T. Bergan and J. R. Norris, editors. Methods in Microbiology. London: Academic Press; 1978. p. 241-262.
-
[No authors listed]. A guide to sensitivity testing. Report of the Working Party on Antibiotic Sensitivity Testing of the British Society for Antimicrobial Chemotherapy. J Antimicrob Chemother 1991;27 Suppl D:1-50.
-
The European Committee on Antimicrobial Susceptibility Testing - EUCAST. [Accessed Accessed 15 July 2016]. Available from: http://www.eucast.org/
-
Public databases for molecular typing and microbial genome diversity (PubMLST). Streptococcus pneumonia MLST Databases. Oxford: Department of Zoology, University of Oxford. [Accessed 27 Feb 2016]. Available from: http://pubmlst.org/spneumoniae/
-
Inouye M, Conway TC, Zobel J, Holt KE. Short read sequence typing (SRST): multi-locus sequence types from short reads. BMC Genomics. 2012;13(1):338. https://doi.org/10.1186/1471-2164-13-338 PMID: 22827703
-
Arguedas A, Soley C, Abdelnour A. Prevenar experience. Vaccine. 2011;29(Suppl 3):C26-34. https://doi.org/10.1016/j.vaccine.2011.06.104 PMID: 21896350
-
Koshy E, Murray J, Bottle A, Sharland M, Saxena S. Impact of the seven-valent pneumococcal conjugate vaccination (PCV7) programme on childhood hospital admissions for bacterial pneumonia and empyema in England: national time-trends study, 1997-2008. Thorax. 2010;65(9):770-4. https://doi.org/10.1136/thx.2010.137802 PMID: 20805169
-
Ansaldi F, Sticchi L, Durando P, Carloni R, Oreste P, Vercelli M, et al. Decline in pneumonia and acute otitis media after the introduction of childhood pneumococcal vaccination in Liguria, Italy. J Int Med Res. 2008;36(6):1255-60. https://doi.org/10.1177/147323000803600612 PMID: 19094434
-
Fortanier AC, Venekamp RP, Boonacker CW, Hak E, Schilder AG, Sanders EA, et al. Pneumococcal conjugate vaccines for preventing otitis media. Cochrane Database Syst Rev. 2014;4(4):CD001480. PMID: 24696098
-
Bonten MJ, Huijts SM, Bolkenbaas M, Webber C, Patterson S, Gault S, et al. Polysaccharide conjugate vaccine against pneumococcal pneumonia in adults. N Engl J Med. 2015;372(12):1114-25. https://doi.org/10.1056/NEJMoa1408544 PMID: 25785969
-
Naito S, Tanaka J, Nagashima K, Chang B, Hishiki H, Takahashi Y, et al. The impact of heptavalent pneumococcal conjugate vaccine on the incidence of childhood community-acquired pneumonia and bacteriologically confirmed pneumococcal pneumonia in Japan. Epidemiol Infect. 2016;144(3):494-506. https://doi.org/10.1017/S0950268815001272 PMID: 26122538
-
van der Linden M, Perniciaro S, Imöhl M. Increase of serotypes 15A and 23B in IPD in Germany in the PCV13 vaccination era. BMC Infect Dis. 2015;15(1):207. https://doi.org/10.1186/s12879-015-0941-9 PMID: 25940580
-
Frazão N, Hiller NL, Powell E, Earl J, Ahmed A, Sá-Leão R, et al. Virulence potential and genome-wide characterization of drug resistant Streptococcus pneumoniae clones selected in vivo by the 7-valent pneumococcal conjugate vaccine. PLoS One. 2013;8(9):e74867. https://doi.org/10.1371/journal.pone.0074867 PMID: 24069360
-
Ardanuy C, de la Campa AG, García E, Fenoll A, Calatayud L, Cercenado E, et al. Spread of Streptococcus pneumoniae serotype 8-ST63 multidrug-resistant recombinant Clone, Spain. Emerg Infect Dis. 2014;20(11):1848-56. https://doi.org/10.3201/eid2011.131215 PMID: 25340616
-
Sanz JC, Cercenado E, Marín M, Ramos B, Ardanuy C, Rodríguez-Avial I, et al. Multidrug-resistant pneumococci (serotype 8) causing invasive disease in HIV+ patients. Clin Microbiol Infect. 2011;17(7):1094-8. https://doi.org/10.1111/j.1469-0691.2011.03495.x PMID: 21463396

Data & Media loading...
