Development of the nasopharyngeal microbiota in infants with cystic fibrosis

American Journal of Respiratory and Critical Care Medicine

Volumn 193, Issue 5, 2016, Pages 504-515

  Prevaes, Sabine M P J ^a   De Winter De Groot, Karin M ^a   Janssens, Hettie M ^b   De Steenhuijsen Piters, Wouter A A ^a   Tramper Stranders, Gerdien A ^a   Wyllie, Anne L ^a   Hasrat, Raiza ^a   Tiddens, Harm A ^b   Van Westreenen, Mireille ^c   Van Der Ent, Cornelis K ^a   Sanders, Elisabeth A M ^a   Bogaert, Debby ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Cystic fibrosis; Healthy controls; Longitudinal; Microbiota; Nasopharynx

Indexed keywords

AMOXICILLIN; ANTIBIOTIC AGENT; CLAVULANIC ACID; COTRIMOXAZOLE; RNA 16S; ANTIINFECTIVE AGENT; BACTERIAL DNA;

ACINETOBACTER; ACTINOMYCES; AGE; ANTIBIOTIC PROPHYLAXIS; ANTIBIOTIC THERAPY; ARTICLE; BACILLI; BACTERIAL COLONIZATION; BENEFICIAL ORGANISM; BOSEA; BREAST FEEDING; CLINICAL ARTICLE; COHORT ANALYSIS; COMMENSAL; CONTROLLED STUDY; CORYNEBACTERIUM; CORYNEBACTERIUM ACCOLENS; CORYNEBACTERIUM PROPINQUUM; CORYNEBACTERIUM PSEUDODIPHTERICUM; CYSTIC FIBROSIS; DOLOSIGRANULUM; ENTEROBACTERIACEAE; FEMALE; HAEMOPHILUS; HAEMOPHILUS INFLUENZAE; HELCOCOCCUS; HUMAN; HUMAN TISSUE; INFANT; INFANT DISEASE; LACHNOSPIRACEAE; MALE; MICROBIAL COMMUNITY; MICROFLORA; MORAXELLA; NASOPHARYNX; NEISSERIACEAE; PASTEURELLACEAE; PORPHYROMONAS; PREVOTELLA; PREVOTELLAE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEOBACTERIA; PSEUDOMONAS; QUESTIONNAIRE; RESPIRATORY TRACT DISEASE; RNA SEQUENCE; SPECIES DOMINANCE; STAPHYLOCOCCACEAE; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS; STREPTOCOCCUS MITIS; STREPTOCOCCUS PNEUMONIAE; VEILLONELLA; BURKHOLDERIA; BURKHOLDERIA INFECTIONS; CASE CONTROL STUDY; CORYNEBACTERIUM INFECTIONS; ENTEROBACTERIACEAE INFECTIONS; GENETICS; HAEMOPHILUS INFECTIONS; HETEROZYGOTE; MICROBIOLOGY; MORAXELLACEAE INFECTIONS; NEWBORN; REAL TIME POLYMERASE CHAIN REACTION; STAPHYLOCOCCAL INFECTIONS; STREPTOCOCCAL INFECTIONS;

ANTI-BACTERIAL AGENTS; BURKHOLDERIA; BURKHOLDERIA INFECTIONS; CARRIER STATE; CASE-CONTROL STUDIES; COHORT STUDIES; CORYNEBACTERIUM; CORYNEBACTERIUM INFECTIONS; CYSTIC FIBROSIS; DNA, BACTERIAL; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; FEMALE; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HUMANS; INFANT; INFANT, NEWBORN; MALE; MICROBIOTA; MORAXELLA; MORAXELLACEAE INFECTIONS; NASOPHARYNX; PROSPECTIVE STUDIES; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS MITIS;

EID: 84979097475     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201509-1759OC     Document Type: Article

References (49)

1. Stick SM, Brennan S, Murray C, Douglas T, von Ungern-Sternberg BS, Garratt LW, Gangell CL, De Klerk N, Linnane B, Ranganathan S, et al.; Australian Respiratory Early Surveillance Team for Cystic Fibrosis (AREST CF). Bronchiectasis in infants and preschool children diagnosed with cystic fibrosis after newborn screening. J Pediatr 2009;155:623-628.e1.
2. Cantin A. Cystic fibrosis lung inflammation: early, sustained, and severe. Am J Respir Crit Care Med 1995;151:939-941.
3. Stoltz DA, Meyerholz DK, Welsh MJ. Origins of cystic fibrosis lung disease. N Engl J Med 2015;372:351-362.
4. Goss CH, Muhlebach MS. Review: Staphylococcus aureus and MRSA in cystic fibrosis. J Cyst Fibros 2011;10:298-306.
5. Tiddens HAWM, Stick SM, Davis S. Multi-modality monitoring of cystic fibrosis lung disease: the role of chest computed tomography. Paediatr Respir Rev 2014;15:92-97.
6. Sermet-Gaudelus I, Mayell SJ, Southern KW; European Cystic Finrosis Society (ECFS), Neonatal Screening Working Group. Guidelines on the early management of infants diagnosed with cystic fibrosis following newborn screening. J Cyst Fibros 2010;9:323-329.
7. Smyth AR, Walters S. Prophylactic anti-staphylococcal antibiotics for cystic fibrosis. Cochrane Database Syst Rev 2012;12:CD001912.
8. Stick SM. Clinical trials in infants with cystic fibrosis detected following newborn screening. Paediatr Respir Rev 2008;9:176-180.
9. Stutman HR, Lieberman JM, Nussbaum E, Marks MI. Antibiotic prophylaxis in infants and young children with cystic fibrosis: a randomized controlled trial. J Pediatr 2002;140:299-305.
10. Rogers GB, Hoffman LR, Whiteley M, Daniels TWV, Carroll MP, Bruce KD. Revealing the dynamics of polymicrobial infections: implications for antibiotic therapy. Trends Microbiol 2010;18:357-364.
11. Rogers GB, Shaw D, Marsh RL, Carroll MP, Serisier DJ, Bruce KD. Respiratory microbiota: addressing clinical questions, informing clinical practice. Thorax 2015;70:74-81.
12. Taylor L, Corey M, Matlow A, Sweezey NB, Ratjen F. Comparison of throat swabs and nasopharyngeal suction specimens in nonsputum-producing patients with cystic fibrosis. Pediatr Pulmonol 2006;41:839-843.
13. Mainz JG, Naehrlich L, Schien M, Käding M, Schiller I, Mayr S, Schneider G, Wiedemann B, Wiehlmann L, Cramer N, et al. Concordant genotype of upper and lower airways P aeruginosa and S aureus isolates in cystic fibrosis. Thorax 2009;64:535-540.
14. Prevaes SMPJ, de Winter-de Groot KM, Janssens HM, de Steenhuijsen Piters WAA, Tramper-Stranders GA, Wyllie AL, Hasrat R, Tiddens HA, van Westreenen M, van der Ent CK, et al. Development of the nasopharyngeal microbiome in CF infants and healthy controls [abstract]. J Cyst Fibros 2015;14(Suppl 1):S77.
15. Satzke C, Turner P, Virolainen-Julkunen A, Adrian PV, Antonio M, Hare KM, Henao-Restrepo AM, Leach AJ, Klugman KP, Porter BD, et al.; WHO Pneumococcal Carriage Working Group. Standard method for detecting upper respiratory carriage of Streptococcus pneumoniae: updated recommendations from the World Health Organization Pneumococcal Carriage Working Group. Vaccine 2013;32:165-179.
16. Pillet S, Lardeux M, Dina J, Grattard F, Verhoeven P, Le Goff J, Vabret A, Pozzetto B. Comparative evaluation of six commercialized multiplex PCR kits for the diagnosis of respiratory infections. PLoS One 2013;8:e72174.
17. van Gils EJM, Hak E, Veenhoven RH, Rodenburg GD, Bogaert D, Bruin JP, van Alphen L, Sanders EAM. Effect of seven-valent pneumococcal conjugate vaccine on Staphylococcus aureus colonisation in a randomised controlled trial. PLoS One 2011;6: e20229.
18. van Gils EJM, Veenhoven RH, Rodenburg GD, Hak E, Sanders EAM. Effect of 7-valent pneumococcal conjugate vaccine on nasopharyngeal carriage with Haemophilus influenzae and Moraxella catarrhalis in a randomized controlled trial. Vaccine 2011;29: 7595-7598.
19. Wyllie AL, Chu MLJN, Schellens MHB, van Engelsdorp Gastelaars J, Jansen MD, van der Ende A, Bogaert D, Sanders EAM, Trzciński K. Streptococcus pneumoniae in saliva of Dutch primary school children. PLoS One 2014;9:e102045.
20. Biesbroek G, Sanders EAM, Roeselers G, Wang X, Caspers MPM, Trzciński K, Bogaert D, Keijser BJF. Deep sequencing analyses of low density microbial communities: working at the boundary of accurate microbiota detection. PLoS One 2012;7:e32942.
21. Biesbroek G, Bosch AATM, Wang X, Keijser BJF, Veenhoven RH, Sanders EAM, Bogaert D. The impact of breastfeeding on nasopharyngeal microbial communities in infants. Am J Respir Crit Care Med 2014;190:298-308.
22. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-336.
23. Carvalho MdaG, Tondella ML, McCaustland K, Weidlich L, McGee L, Mayer LW, Steigerwalt A, Whaley M, Facklam RR, Fields B, et al. Evaluation and improvement of real-time PCR assays targeting lytA, ply, and psaA genes for detection of pneumococcal DNA. J Clin Microbiol 2007;45: 2460-2466.
24. Regev-Yochay G, Dagan R, Raz M, Carmeli Y, Shainberg B, Derazne E, Rahav G, Rubinstein E. Association between carriage of Streptococcus pneumoniae and Staphylococcus aureus in children. JAMA 2004;292:716-720.
25. Lay JO Jr. MALDI-TOF mass spectrometry of bacteria. Mass Spectrom Rev 2001;20:172-194.
26. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001;98:5116-5121.
27. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O?Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. Ordination methods, diversity analysis and other functions for community and vegetation ecologists (vegan: community ecology package version 2.3.1) [accessed 2015 Nov 2]. Available from: http://CRANRprojectorg/package=vegan.
28. Letunic I, Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 2011;39 (Web server issue):W475-W478.
29. Faust K, Raes J. Microbial interactions: from networks to models. Nat Rev Microbiol 2012;10:538-550.
30. Tang AC, Turvey SE, Alves MP, Regamey N, Tümmler B, Hartl D. Current concepts: host-pathogen interactions in cystic fibrosis airways disease. Eur Respir Rev 2014;23:320-332.
31. Stick SM. The first 2 years of life: implications of recent findings. Curr Opin Pulm Med 2009;15:615-620.
32. Madan JC, Koestler DC, Stanton BA, Davidson L, Moulton LA, Housman ML, Moore JH, Guill MF, Morrison HG, Sogin ML, et al. Serial analysis of the gut and respiratory microbiome in cystic fibrosis in infancy: interaction between intestinal and respiratory tracts and impact of nutritional exposures. MBio 2012; 3:e00251-12.
33. Stoltz DA, Meyerholz DK, Pezzulo AA, Ramachandran S, Rogan MP, Davis GJ, Hanfland RA, Wohlford-Lenane C, Dohrn CL, Bartlett JA, et al. Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci Transl Med 2010;2: 29ra31.
34. Hurley MN, Forrester DL, Smyth AR. Antibiotic adjuvant therapy for pulmonary infection in cystic fibrosis. Cochrane Database Syst Rev 2013;6:CD008037.
35. Pillarisetti N, Williamson E, Linnane B, Skoric B, Robertson CF, Robinson P, Massie J, Hall GL, Sly P, Stick S, et al.; Australian Respiratory Early Surveillance Team for Cystic Fibrosis (AREST CF). Infection, inflammation, and lung function decline in infants with cystic fibrosis. Am J Respir Crit Care Med 2011; 184:75-81.
36. Wolter DJ, Emerson JC, McNamara S, Buccat AM, Qin X, Cochrane E, Houston LS, Rogers GB, Marsh P, Prehar K, et al. Staphylococcus aureus small-colony variants are independently associated with worse lung disease in children with cystic fibrosis. Clin Infect Dis 2013;57:384-391.
37. Kahl BC. Impact of Staphylococcus aureus on the pathogenesis of chronic cystic fibrosis lung disease. Int J Med Microbiol 2010;300: 514-519.
38. Melter O, Radojevič B. Small colony variants of Staphylococcus aureus-review. Folia Microbiol (Praha) 2010;55:548-558.
39. van den Bergh MR, Biesbroek G, Rossen JWA, de Steenhuijsen Piters WAA, Bosch AATM, van Gils EJM, Wang X, Boonacker CWB, Veenhoven RH, Bruin JP, et al. Associations between pathogens in the upper respiratory tract of young children: interplay between viruses and bacteria. PLoS One 2012;7: e47711.
40. Ramsey KA, Ranganathan S, Park J, Skoric B, Adams A-M, Simpson SJ, Robins-Browne RM, Franklin PJ, de Klerk NH, Sly PD, et al.; AREST CF. Early respiratory infection is associated with reduced spirometry in children with cystic fibrosis. Am J Respir Crit Care Med 2014;190:1111-1116.
41. Jacoby P, Carville KS, Hall G, Riley TV, Bowman J, Leach AJ, Lehmann D; Kalgoorlie Otitis Media Research Project Team. Crowding and other strong predictors of upper respiratory tract carriage of otitis media-related bacteria in Australian Aboriginal and non-Aboriginal children. Pediatr Infect Dis J 2011;30: 480-485.
42. Santagati M, Scillato M, PatanèF, Aiello C, Stefani S. Bacteriocinproducing oral streptococci and inhibition of respiratory pathogens. FEMS Immunol Med Microbiol 2012;65:23-31.
43. Tano K, Olofsson C, Grahn-Hakansson E, Holm SE. In vitro inhibition of S. pneumoniae, nontypable H. influenzae and M. catharralis by a-hemolytic streptococci from healthy children. Int J Pediatr Otorhinolaryngol 1999;47:49-56.
44. Whiley RA, Fleming EV, Makhija R, Waite RD. Environment and colonisation sequence are key parameters driving cooperation and competition between Pseudomonas aeruginosa cystic fibrosis strains and oral commensal streptococci. PLoS One 2015;10: e0115513.
45. Biesbroek G, Tsivtsivadze E, Sanders EAM, Montijn R, Veenhoven RH, Keijser BJF, Bogaert D. Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am J Respir Crit Care Med 2014;190:1283-1292.
46. Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM, Wolfgang MC. The adult cystic fibrosis airway microbiota is stable over time and infection type, and highly resilient to antibiotic treatment of exacerbations. PLoS One 2012;7:e45001.
47. Price KE, Hampton TH, Gifford AH, Dolben EL, Hogan DA, Morrison HG, Sogin ML, O?Toole GA. Unique microbial communities persist in individual cystic fibrosis patients throughout a clinical exacerbation. Microbiome 2013;1:27.
48. Rogers GB, Hoffman LR, Döring G. Novel concepts in evaluating antimicrobial therapy for bacterial lung infections in patients with cystic fibrosis. J Cyst Fibros 2011;10:387-400.
49. Mouquet N, Gravel D, Massol F, Calcagno V. Extending the concept of keystone species to communities and ecosystems. Ecol Lett 2013; 16:1-8.