Genomic epidemiology of penicillin- nonsusceptible pneumococci with nonvaccine serotypes causing invasive disease in the United States

Journal of Clinical Microbiology

Volumn 55, Issue 4, 2017, Pages 1104-1115

  Andam, Cheryl P ^a   Mitchell, Patrick K ^a   Callendrello, Alanna ^a   Chang, Qiuzhi ^a   Corander, Jukka ^b   Chaguza, Chrispin ^c,d   McGee, Lesley ^e   Beall, Bernard W ^e   Hanage, William P ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

^c QUEEN ELIZABETH CENTRAL HOSPITAL   (Malawi)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

^e NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

Genomic epidemiology; Nonvaccine serotype; Penicillin; Vaccine

Indexed keywords

PENICILLIN DERIVATIVE; TRANSCRIPTION FACTOR RELA;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GENOME; BACTERIUM ISOLATE; CLONAL VARIATION; CONTROLLED STUDY; GENE LOCUS; GENE SWITCHING; GENETIC EPIDEMIOLOGY; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; MOLECULAR CLONING; MOLECULAR PHYLOGENY; NONHUMAN; POPULATION GENETIC STRUCTURE; RELA GENE; STREPTOCOCCUS PNEUMONIAE; UNITED STATES; ADOLESCENT; ADULT; AGED; CHILD; CLASSIFICATION; DNA SEQUENCE; DRUG EFFECTS; EPIDEMIOLOGICAL MONITORING; FEMALE; HUMAN; INFANT; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY; MIDDLE AGED; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; NEWBORN; PENICILLIN RESISTANCE; PNEUMOCOCCAL INFECTIONS; PRESCHOOL CHILD; SEROTYPE; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CHILD; CHILD, PRESCHOOL; EPIDEMIOLOGICAL MONITORING; EVOLUTION, MOLECULAR; FEMALE; GENOME, BACTERIAL; GENOTYPE; HUMANS; INFANT; INFANT, NEWBORN; MALE; MIDDLE AGED; MOLECULAR EPIDEMIOLOGY; PENICILLIN RESISTANCE; PNEUMOCOCCAL INFECTIONS; SEQUENCE ANALYSIS, DNA; SEROGROUP; STREPTOCOCCUS PNEUMONIAE; UNITED STATES; YOUNG ADULT;

EID: 85016103517     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.02453-16     Document Type: Article

References (56)

1. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E, Collins M, Donohoe K, Harris D, Murphy L, Quail MA, Samuel G, Skovsted IC, Kaltoft MS, Barrell B, Reeves PR, Parkhill J, Spratt BG. 2006. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2:e31. https://doi.org/10.1371/journal.pgen.0020031.
2. Hausdorff WP, Feikin DR, Klugman KP. 2005. Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis 5:83-93. https://doi.org/10.1016/S1473-3099(05)70083-9.
3. Hsu KK, Pelton SI. 2003. Heptavalent pneumococcal conjugate vaccine: current and future impact. Expert Rev Vaccines 2:619-631. https://doi.org/10.1586/14760584.2.5.619.
4. Pilishvili T, Lexau C, Farley MM, Hadler J, Harrison LH, Bennett NM, Reingold A, Thomas A, Schaffner W, Craig AS, Smith PJ, Beall BW, Whitney CG, Moore MR, Active Bacterial Core Surveillance/Emerging Infections Program Network. 2010. Sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J Infect Dis 201:32-41. https://doi.org/10.1086/648593.
5. Hanage WP, Finkelstein JA, Huang SS, Pelton SI, Stevenson AE, Kleinman K, Hinrichsen VL, Fraser C. 2010. Evidence that pneumococcal serotype replacement in Massachusetts following conjugate vaccination is now complete. Epidemics 2:80-84. https://doi.org/10.1016/j.epidem.2010.03.005.
6. Pichon B, Ladhani SN, Slack MPE, Segonds-Pichon A, Andrews NJ, Waight PA, Miller E, George R. 2013. Changes in molecular epidemiology of streptococcus pneumoniae causing meningitis following introduction of pneumococcal conjugate vaccination in England and Wales. J Clin Microbiol 51:820-827. https://doi.org/10.1128/JCM.01917-12.
7. Gladstone RA, Jefferies JM, Tocheva AS, Beard KR, Garley D, Chong WW, Bentley SD, Faust SN, Clarke SC. 2015. Five winters of pneumococcal serotype replacement in UK carriage following PCV introduction. Vaccine 33:2015-2021. https://doi.org/10.1016/j.vaccine.2015.03.012.
8. Gertz RE, Li Z, Pimenta FC, Jackson D, Juni BA, Lynfield R, Jorgensen JH, Carvalho Mda G, Beall BW, Active Bacterial Core Surveillance Team. 2010. Increased penicillin nonsusceptibility of nonvaccine-serotype invasive pneumococci other than serotypes 19A and 6A in post-7-valent conjugate vaccine era. J Infect Dis 201:770-775. https://doi.org/10.1086/650496.
9. Hanage WP, Fraser C, Tang J, Connor TR, Corander J. 2009. Hyperrecombination, diversity, and antibiotic resistance in pneumococcus. Science 324:1454-1457. https://doi.org/10.1126/science.1171908.
10. Brueggemann AB, Pai R, Crook DW, Beall B. 2007. Vaccine escape recombinants emerge after pneumococcal vaccination in the United States. PLoS Pathog 3:e168. https://doi.org/10.1371/journal.ppat.0030168.
11. 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 18:343-345. https://doi.org/10.1128/CVI.00383-10.
12. Golubchik T, Brueggemann AB, Street T, Gertz RE, Jr, Spencer CCA, Ho T, Giannoulatou E, Link-Gelles R, Harding RM, Beall B, Peto TEA, Moore MR, Donnelly P, Crook DW, Bowden R. 2012. Pneumococcal genome sequencing tracks a vaccine escape variant formed through a multifragment recombination event. Nat Genet 44:352-355. https://doi.org/10.1038/ng.1072.
13. Wyres KL, Lambertsen LM, Croucher NJ, McGee L, von Gottberg A, Liñares J, Jacobs MR, Kristinsson KG, Beall BW, Klugman KP, Parkhill J, Hakenbeck R, Bentley SD, Brueggemann AB. 2013. Pneumococcal capsular switching: a historical perspective. J Infect Dis 207:439-449. https://doi.org/10.1093/infdis/jis703.
14. Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. 2013. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 30:1224-1228. https://doi.org/10.1093/molbev/mst028.
15. Serrano I, Melo-Cristino J, Carriço JA, Ramirez M. 2005. Characterization of the genetic lineages responsible for pneumococcal invasive disease in Portugal. J Clin Microbiol 43:1706-1715. https://doi.org/10.1128/JCM.43.4.1706-1715.2005.
16. McGee L, McDougal L, Zhou J, Spratt BG, Tenover FC, George R, Hakenbeck R, Hryniewicz W, Lefévre JC, Tomasz A, Klugman KP. 2001. Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiology network. J Clin Microbiol 39:2565-2571. https://doi.org/10.1128/JCM.39.7.2565-2571.2001.
17. Beall B, McEllistrem MC, Gertz RE, Boxrud DJ, Besser JM, Harrison LH, Jorgensen JH, Whitney CG, Active Bacterial Core Surveillance/Emerging Infections Program Network. 2002. Emergence of a novel penicillinnonsusceptible, invasive serotype 35B clone of Streptococcus pneumoniae within the United States. J Infect Dis 186:118-122. https://doi.org/10.1086/341072.
18. Kapatai G, Sheppard CL, Al-Shahib A, Litt DJ, Underwood AP, Harrison TG, Fry NK. 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. https://doi.org/10.7717/peerj.2477.
19. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, McGee L, von Gottberg A, Song JH, Ko KS, Pichon B, Baker S, Parry CM, Lambertsen LM, Shahinas D, Pillai DR, Mitchell TJ, Dougan G, Tomasz A, Klugman KP, Parkhill J, Hanage WP, Bentley SD. 2011. Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430-434. https://doi.org/10.1126/science.1198545.
20. Croucher NJ, Finkelstein JA, Pelton SI, Mitchell PK, Lee GM, Parkhill J, Bentley SD, Hanage WP, Lipsitch M. 2013. Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 45: 656-663. https://doi.org/10.1038/ng.2625.
21. Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P, Cheng L, Pessia A, Aanensen DM, Mather AE, Page AJ, Salter SJ, Harris D, Nosten F, Goldblatt D, Corander J, Parkhill J, Turner P, Bentley SD. 2014. Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 46:305-309. https://doi.org/10.1038/ng.2895.
22. Brown DR, Barton G, Pan Z, Buck M, Wigneshweraraj S. 2014. Nitrogen stress response and stringent response are coupled in Escherichia coli. Nat Commun 5:4115. https://doi.org/10.1038/ncomms5115.
23. Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K. 2015. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol 13:298-309. https://doi.org/10.1038/nrmicro3448.
24. Li Y, Croucher NJ, Thompson CM, Trzciński K, Hanage WP, Lipsitch M. 2015. Identification of pneumococcal colonization determinants in the stringent response pathway facilitated by genomic diversity. BMC Genomics 16:369. https://doi.org/10.1186/s12864-015-1573-6.
25. Mostowy R, Croucher NJ, Hanage WP, Harris SR, Bentley S, Fraser C. 2014. Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution. PLoS Genet 10:e1004300. https://doi.org/10.1371/journal.pgen.1004300.
26. Metcalf BJ, Gertz RE, Gladstone RA, Walker H, Sherwood LK, Jackson D, Li Z, Law C, Hawkins PA, Chochua S, Sheth M, Rayamajhi N, Bentley SD, Kim L, Whitney CG, McGee L, Beall B, Active Bacterial Core Surveillance Team. 2016. Strain features and distributions in pneumococci from children with invasive disease before and after 13-valent conjugate vaccine implementation in the USA. Clin Microbiol Infect 22: 60.e9-60.e29. https://doi.org/10.1016/j.cmi.2015.08.027.
27. Olarte L, Kaplan SL, Barson WJ, Romero JR, Lin PL, Tan TQ, Hoffman JA, Bradley JS, Givner LB, Mason EO, Hultén KG. 9 November 2016. Emergence of multidrug-resistant pneumococcal serotype 35B among U.S. Children. J Clin Microbiol https://doi.org/10.1128/JCM.01778-16.
28. Clinical and Laboratory Standards Institute. 2008. Performance standards for antimicrobial susceptibility testing,16th informational supplement M100-S16. Clinical and Laboratory Standards Institute, Wayne, PA.
29. Weinstein MP, Klugman KP, Jones RN. 2009. Rationale for revised penicillin susceptibility breakpoints versus Streptococcus pneumoniae: coping with antimicrobial susceptibility in an era of resistance. Clin Infect Dis 48:1596-1600. https://doi.org/10.1086/598975.
30. Venkateswaran PS, Stanton N, Austrian R. 1983. Type variation of strains of Streptococcus pneumoniae in capsular serogroup 15. J Infect Dis 147:1041-1054. https://doi.org/10.1093/infdis/147.6.1041.
31. van Selm S, van Cann LM, Kolkman MAB, van der Zeijst BAM, van Putten JPM. 2003. Genetic basis for the structural difference between Streptococcus pneumoniae serotype 15B and 15C capsular polysaccharides. Infect Immun 71:6192-6198. https://doi.org/10.1128/IAI.71.11.6192-6198.2003.
32. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ, Tomita T, Zobel J, Holt KE. 2014. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 6:90. https://doi.org/10.1186/s13073-014-0090-6.
33. Enright MC, Spratt BG. 1998. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144(Part 11):3049-3060. https://doi.org/10.1099/00221287-144-11-3049.
34. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455-477. https://doi.org/10.1089/cmb.2012.0021.
35. Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068-2069. https://doi.org/10.1093/bioinformatics/btu153.
36. Contreras-Moreira B, Vinuesa P. 2013. GET-HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol 79:7696-7701. https://doi.org/10.1128/AEM.02411-13.
37. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, Fookes M, Keane JA, Parkhill J. 2015. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31:3691-3693. https://doi.org/10.1093/bioinformatics/btv421.
38. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059-3066. https://doi.org/10.1093/nar/gkf436.
39. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. https://doi.org/10.1093/bioinformatics/btu033.
40. Tavaré S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences, p 57-86. In Miura R (ed), Lectures on mathematics in the life sciences. American Mathematical Society, Providence, RI.
41. Corander J, Marttinen P, Sirén J, Tang J. 2008. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539. https://doi.org/10.1186/1471-2105-9-539.
42. Castillo-Ramírez S, Corander J, Marttinen P, Aldeljawi M, Hanage WP, Westh H, Boye K, Gulay Z, Bentley SD, Parkhill J, Holden MT, Feil EJ. 2012. Phylogeographic variation in recombination rates within a global clone of methicillin-resistant Staphylococcus aureus. Genome Biol 13:R126. https://doi.org/10.1186/gb-2012-13-12-r126.
43. Willems RJL, Top J, van Schaik W, Leavis H, Bonten M, Sirén J, Hanage WP, Corander J. 2012. Restricted gene flow among hospital subpopulations of Enterococcus faecium. mBio 3:e00151-12. https://doi.org/10.1128/mBio.00151-12.
44. McNally A, Cheng L, Harris SR, Corander J. 2013. The evolutionary path to extraintestinal pathogenic, drug-resistant Escherichia coli is marked by drastic reduction in detectable recombination within the core genome. Genome Biol Evol 5:699-710. https://doi.org/10.1093/gbe/evt038.
45. Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M, Carriço JA. 2012. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 13:87. https://doi.org/10.1186/1471-2105-13-87.
46. Simpson EH. 1949. Measurement of diversity. Nature 163:688. https://doi.org/10.1038/163688a0.
47. Grundmann H, Hori S, Tanner G. 2001. Determining confidence intervals when measuring genetic diversity and the discriminatory abilities of typing methods for microorganisms. J Clin Microbiol 39:4190-4192. https://doi.org/10.1128/JCM.39.11.4190-4192.2001.
48. Jolley KA, Wilson DJ, Kriz P, McVean G, Maiden MCJ. 2005. The influence of mutation, recombination, population history, and selection on patterns of genetic diversity in Neisseria meningitidis. Mol Biol Evol 22: 562-569. https://doi.org/10.1093/molbev/msi041.
49. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, Parkhill J, Harris SR. 2014. Rapid phylogenetic analysis of large samples of recombinant bacterial whole-genome sequences using Gubbins. Nucleic Acids Res 43:e15. https://doi.org/10.1093/nar/gku1196.
50. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079. https://doi.org/10.1093/bioinformatics/btp352.
51. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group. 2011. The variant call format and VCFtools. Bioinformatics 27:2156-2158. https://doi.org/10.1093/bioinformatics/btr330.
52. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain J-M. 2014. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58:212-220. https://doi.org/10.1128/AAC.01310-13.
53. R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
54. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214.
55. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969-1973. https://doi.org/10.1093/molbev/mss075.
56. Croucher NJ, Klugman KP. 2014. The emergence of bacterial "hopeful monsters". mBio 5:e01550-14. https://doi.org/10.1128/mBio.01550-14.