1887

Abstract

The nasopharyngeal microbiome is a dynamic microbial interface of the aerodigestive tract, and a diagnostic window in the fight against respiratory infections and antimicrobial resistance. As its constituent bacteria, viruses and mycobacteria become better understood and sampling accuracy improves, diagnostics of the nasopharynx could guide more personalized care of infections of surrounding areas including the lungs, ears and sinuses. This review will summarize the current literature from a clinical perspective and highlight its growing importance in diagnostics and infectious disease management.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001368
2021-06-24
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/jmm/70/6/jmm001368.html?itemId=/content/journal/jmm/10.1099/jmm.0.001368&mimeType=html&fmt=ahah

References

  1. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Beck JM et al. Spatial variation in the healthy human lung microbiome and the adapted Island model of lung biogeography. Ann Am Thorac Soc 2015; 12:821–830 [View Article]
    [Google Scholar]
  2. Boeck D, Wittouck S, Martens K, Claes J, Jorissen M et al. Anterior nares diversity and pathobionts represent sinus microbiome in chronic rhinosinusitis. mSphere 2019; 4: [View Article]
    [Google Scholar]
  3. Rawlings B, Higgins T, Han J. Bacterial pathogens in the nasopharynx, nasal cavity, and osteomeatal complex during wellness and viral infection. Am J Rhinol Allergy 2013; 27:39–42 [View Article]
    [Google Scholar]
  4. Lappan R, Imbrogno K, Sikazwe C, Anderson D, Mok D et al. A microbiome case-control study of recurrent acute otitis media identified potentially protective bacterial genera. BMC Microbiol 2018; 18: [View Article]
    [Google Scholar]
  5. Ending Preventable Child Deaths from Pneumonia and Diarrhoea by 2025 The integrated Global Action Plan for Pneumonia and Diarrhoea (GAPPD) WHO Press; 2013
    [Google Scholar]
  6. Dekker A, Verheij T, van der Velden A. Inappropriate antibiotic prescription for respiratory tract indications: most prominent in adult patients. Fam Pract 2015; 32:401–407 [View Article]
    [Google Scholar]
  7. Grijalva CG, Nuorti JP, Griffin MR. Antibiotic prescription rates for acute respiratory tract infections in US ambulatory settings. JAMA 2009; 302:758–766 [View Article]
    [Google Scholar]
  8. Köser CU, Ellington MJ, Peacock SJ. Whole-genome sequencing to control antimicrobial resistance. Trend Genet 2014; 30:401–407 [View Article]
    [Google Scholar]
  9. Flynn M, Hooper G. Antimicrobial stewardship though FeverPAIN score: Successes and challenges in secondary care. Clin Infect Practice 20207–8 [View Article]
    [Google Scholar]
  10. Huxley E, Viroslav J, Gray W, Pierce A. Pharyngeal aspiration in normal adults and patients with depressed consciousness. Survey Anesthesiol 1979; 23:203 [View Article]
    [Google Scholar]
  11. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 2011; 184:957–963 [View Article]
    [Google Scholar]
  12. Wang H, Dai W, Feng X, Zhou Q, Wang H et al. Microbiota composition in upper respiratory tracts of healthy children in Shenzhen, China, differed with respiratory sites and ages. Biomed Res Int 2018; 2018:6515670 [View Article]
    [Google Scholar]
  13. Stearns JC, Davidson CJ, McKeon S, Whelan FJ, Fontes ME et al. Culture and molecular-based profiles show shifts in bacterial communities of the upper respiratory tract that occur with age. ISME J 2015; 9:1246–1259 [View Article]
    [Google Scholar]
  14. Man WH, Clerc M, de Steenhuijsen Piters WAA, van Houten MA, Chu MLJN et al. Loss of microbial topography between oral and nasopharyngeal microbiota and development of respiratory infections early in life. Am J Respir Crit Care Med 2019; 200:760–770 [View Article]
    [Google Scholar]
  15. Man W, van Houten M, Mérelle M, Vlieger A, Chu M et al. Bacterial and viral respiratory tract microbiota and host characteristics in children with lower respiratory tract infections: a matched case-control study. Lancet Respir Med 2019; 7:417–426 [View Article]
    [Google Scholar]
  16. Little P, Hobbs FD, Moore M, Mant D, Williamson I et al. Clinical score and rapid antigen detection test to guide antibiotic use for sore throats: randomised controlled trial of PRISM (primary care streptococcal management). BMJ 2013; 10:f5806 [View Article]
    [Google Scholar]
  17. Teo SM, Mok D, Pham K, Kusel M, Serralha M et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe 2015; 17:704–715 [View Article]
    [Google Scholar]
  18. de Steenhuijsen Piters WA, Sanders EA, Bogaert D. The role of the local microbial ecosystem in respiratory health and disease. Phil Trans R Soc Lond B Biol Sci 2015; 370:20140294 [View Article]
    [Google Scholar]
  19. Man WH, Clerc M, de Steenhuijsen Piters WAA, van Houten MA, Chu MLJN et al. Loss of microbial topography between oral and nasopharyngeal microbiota and development of respiratory infections early in life. Am J Respir Crit Care Med 2019; 200:760–770 [View Article]
    [Google Scholar]
  20. Bosch A, Piters W, van Houten M, Chu M, Biesbroek G et al. Maturation of the Infant Respiratory Microbiota, Environmental Drivers, and Health Consequences. A Prospective Cohort Study. Am J Respir Crit Care Med 2017; 196:1582–1590 [View Article]
    [Google Scholar]
  21. Perez GF, Pérez-Losada M, Isaza N, Rose MC, Colberg-Poley AM et al. Nasopharyngeal microbiome in premature infants and stability during rhinovirus infection. J Invest Med 2017; 65:984–990 [View Article]
    [Google Scholar]
  22. Bogaert D, Keijser B, Huse S, Rossen J, Veenhoven R et al. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis. PLoS One 2011; 6:e17035 [View Article]
    [Google Scholar]
  23. Stearns JC, Davidson CJ, McKeon S, Whelan FJ, Fontes ME et al. Culture and molecular-based profiles show shifts in bacterial communities of the upper respiratory tract that occur with age. ISME J 2015; 9:1246–1259 [View Article]
    [Google Scholar]
  24. de Steenhuijsen Piters WAA, Huijskens EGW, Wyllie AL, Biesbroek G, van den Bergh MR et al. Dysbiosis of upper respiratory tract microbiota in elderly pneumonia patients. ISME J 2016; 10:97–108 [View Article]
    [Google Scholar]
  25. Liu C, Price L, Hungate B, Abraham A, Larsen L et al. Staphylococcus aureus and the ecology of the nasal microbiome. Sci Advance 2015; 1:e1400216 [View Article]
    [Google Scholar]
  26. Whelan F, Verschoor C, Stearns J, Rossi L, Luinstra K. The loss of topography in the microbial communities of the upper respiratory tract in the elderly. Annal Am Thoracic Soc 2014; 11:513–521 [View Article]
    [Google Scholar]
  27. Man W, Clerc M, de Steenhuijsen Piters W, van Houten M, Chu M et al. Loss of microbial topography between oral and nasopharyngeal microbiota and development of respiratory infections early in life. Am J Respir Crit Care Med 2019; 200:760–770 [View Article]
    [Google Scholar]
  28. Biesbroek G, Bosch A, Wang X, Keijser B, Veenhoven R et al. The impact of breastfeeding on nasopharyngeal microbial communities in infants. Am J Respir Crit Care Med 2014140612135546007 [View Article]
    [Google Scholar]
  29. Teo SM, Mok D, Pham K, Kusel M, Serralha M et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe 2015; 17:704–715 [View Article]
    [Google Scholar]
  30. Aksoy F, Demirhan H, Bayraktar G, Yıldırım Y, Özturan O et al. Effect of nasal mometasone furoate on the nasal and nasopharyngeal flora. Auris Nasus Larynx 2012; 39:180–185 [View Article]
    [Google Scholar]
  31. Brook I, Gober A. Recovery of potential pathogens in the nasopharynx of healthy and otitis media—prone children and their smoking and nonsmoking parents. Ann Otol, Rhinol Laryngol 2008; 117:727–730 [View Article]
    [Google Scholar]
  32. Brook I, Gober AE. Effect of smoking cessation on the microbial flora. Arch Otolaryngol Head Neck Surg 2007; 133:135–138 [View Article]
    [Google Scholar]
  33. Jourdain S, Smeesters P, Denis O, Dramaix M, Sputael V et al. Differences in nasopharyngeal bacterial carriage in preschool children from different socio-economic origins. Clin Microbiol Infect 2011; 17:907–914 [View Article]
    [Google Scholar]
  34. Principi N, Marchisio P, Schito G, Mannelli S. Risk factors for carriage of respiratory pathogens in the nasopharynx of healthy children. Ped Infect Dis J 1999; 18:517–523 [View Article]
    [Google Scholar]
  35. Kraemer JG, Ramette A, Aebi S, Oppliger A, Hilty M. Influence of pig farming on the human nasal microbiota: Key role of airborne microbial communities. Appl Environ Microbiol 2018; 84: [View Article]
    [Google Scholar]
  36. Berger D, Rakhamimova A, Pollack A, Loewy Z. Oral biofilms: development, control, and analysis. High Throughput 2018; 7:24 [View Article]
    [Google Scholar]
  37. Winther B, Gross BC, Hendley JO, Early SV. Location of bacterial biofilm in the mucus overlying the adenoid by light microscopy. Arch Otolaryngol Head Neck Surg 2009; 135:1239–1245 [View Article]
    [Google Scholar]
  38. Coticchia J, Zuliani G, Coleman C, Carron M, Gurrola J II et al. Biofilm surface area in the pediatric nasopharynx. Arch Otolaryngol Head Neck Surg 2007; 133:110 [View Article]
    [Google Scholar]
  39. Flemming H, Wingender J, Szewzyk U, Steinberg P, Rice S et al. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 2016; 14:563–575 [View Article]
    [Google Scholar]
  40. Subtil J, Bajanka-Lavado M, Rodrigues J, Duarte A, Reis L et al. Cross-sectional study of adenoidal biofilms in a paediatric population and its clinical implications. Otolar Polska 2018; 72:1–5 [View Article]
    [Google Scholar]
  41. Pawlowski B, Nowak J, Borkowska B, Drulis-Kawa Z. Human body morphology, prevalence of nasopharyngeal potential bacterial pathogens, and immunocompetence handicap principal. Am J Human Biol 2014; 26:305–310 [View Article]
    [Google Scholar]
  42. Bergman P, Norlin A, Hansen S. Vitamin D3 supplementation in patients with frequent respiratory tract infections: a randomised and double-blind intervention study. BMJ Open 2012; 2:e001663 [View Article]
    [Google Scholar]
  43. Olliver M, Spelmink L, Hiew J, Meyer-Hoffert U, Henriques-Normark B et al. Immunomodulatory effects of vitamin D on innate and adaptive immune responses to Streptococcus pneumoniae. J Infect Dis 2013; 208:1474–1481 [View Article]
    [Google Scholar]
  44. Pérez-Losada M, Alamri L, Crandall K, Freishtat R. Nasopharyngeal microbiome diversity changes over time in children with asthma. PLOS ONE 2017; 12:e0170543 [View Article]
    [Google Scholar]
  45. See xvi, Grindle K, Johnston SL, Gern JE, Sly PD. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe 2015; 17:704–715 [View Article]
    [Google Scholar]
  46. Donkor ES. Understanding the pneumococcus: transmission and evolution. Front Cell Infect Microbiol 2013; 3:7 [View Article]
    [Google Scholar]
  47. Mechergui A, Achour W, Baaboura R, Ouertani H, Lakhal A et al. Case report of bacteremia due to Neisseria mucosa. APMIS 2013; 122:359–361 [View Article]
    [Google Scholar]
  48. Cleary D, Devine V, Morris D, Osman K, Gladstone R et al. Pneumococcal vaccine impacts on the population genomics of non-typeable Haemophilus influenzae. Microb Genomics 2018; 4: [View Article]
    [Google Scholar]
  49. Gladstone R, Devine V, Jones J, Cleary D, Jefferies J et al. Pre-vaccine serotype composition within a lineage signposts its serotype replacement – a carriage study over 7 years following pneumococcal conjugate vaccine use in the UK. Microb Genomics 2017; 3: [View Article]
    [Google Scholar]
  50. Murphy T, Parameswaran G. Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis 2009; 49:124–131 [View Article]
    [Google Scholar]
  51. Vuononvirta J, Toivonen L, Gröndahl-Yli-Hannuksela K, Barkoff A, Lindholm L et al. Nasopharyngeal bacterial colonization and gene polymorphisms of mannose-binding lectin and toll-like receptors 2 and 4 in infants. PLOS ONE 2011; 6:e26198 [View Article]
    [Google Scholar]
  52. Reiss-Mandel A, Regev-Yochay G. Staphylococcus aureus and Streptococcus pneumoniae interaction and response to pneumococcal vaccination: Myth or reality?. Hum Vaccin Immunother 2016; 12:351–357 [View Article]
    [Google Scholar]
  53. Bosch AA, Biesbroek G, Trzcinski K, Sanders EA, Bogaert D. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 2013; 9:e1003057 [View Article] [PubMed]
    [Google Scholar]
  54. Wylie K, Mihindukulasuriya K, Sodergren E, Weinstock G, Storch G. Sequence analysis of the human virome in Febrile and Afebrile Children. PLOS ONE 2012; 7:e27735 [View Article] [PubMed]
    [Google Scholar]
  55. Cai X, Wang Q, Lin G, Cai Z, Lin C et al. Respiratory virus infections among children in South China. J Med Virol 2014; 86:1249–1255 [View Article]
    [Google Scholar]
  56. Hause A, Avadhanula V, Maccato M, Pinell P, Bond N et al. A cross-sectional surveillance study of Acute Respiratory Illness (ARI) in pregnant women. Open Forum Infect Dis 2017; 4:S573 [View Article]
    [Google Scholar]
  57. Wylie KM, Mihindukulasuriya KA, Sodergren E, Weinstock GM, Storch GA. Sequence analysis of the human Virome in febrile and afebrile children. PLOS ONE 2012; 7:e27735 [View Article]
    [Google Scholar]
  58. Wang Y, Zhu N, Li Y, Lu R, Wang H et al. Metagenomic analysis of viral genetic diversity in respiratory samples from children with severe acute respiratory infection in China. Clin Microbiol Infect 2016; 22:458 [View Article]
    [Google Scholar]
  59. Annamalay AA, Khoo SK, Jacoby P, Bizzintino J, Zhang G et al. Prevalence of and risk factors for human rhinovirus infection in healthy aboriginal and non-aboriginal Western Australian children. Ped Infect Dis J 2012673–679 [View Article]
    [Google Scholar]
  60. Moore H, Jacoby P, Taylor A, Harnett G, Bowman J. The interaction between respiratory viruses and pathogenic bacteria in the upper respiratory tract of asymptomatic aboriginal and non-aboriginal children. Ped Infect Dis J 2010; 29:540–545 [View Article]
    [Google Scholar]
  61. Ederveen THA, Ferwerda G, Ahout IM, Vissers M, de Groot R et al. Haemophilus is overrepresented in the nasopharynx of infants hospitalized with RSV infection and associated with increased viral load and enhanced mucosal CXCL8 responses. Microbiome 2018; 6:10 [View Article]
    [Google Scholar]
  62. Mansbach JM, Hasegawa K, Piedra PA, Avadhanula V, Petrosino JF et al. Haemophilus-dominant nasopharyngeal microbiota is associated with delayed clearance of respiratory syncytial virus in infants hospitalized for bronchiolitis. J Infect Dis 2019; 219:1804–1808 [View Article]
    [Google Scholar]
  63. Wang X, Tan L, Wang X, Liu W, Lu Y et al. Comparison of nasopharyngeal and oropharyngeal swabs for SARS-CoV-2 detection in 353 patients received tests with both specimens simultaneously. Int J Infect Dis 2020; 94:107–109 [View Article]
    [Google Scholar]
  64. Dai W, Wang H, Zhou Q, Feng X, Lu Z et al. The concordance between upper and lower respiratory microbiota in children with Mycoplasma pneumoniae pneumonia. Emerg Microb Infect 2018; 7:92 [View Article]
    [Google Scholar]
  65. Lu Y, Wang S, Liou M, Shen T, Lu Y et al. Microbiota dysbiosis in fungal rhinosinusitis. J Clin Med 2019; 8:11 [View Article]
    [Google Scholar]
  66. Dickson RP, Erb-Downward JR, Huffnagle GB. The role of the bacterial microbiome in lung disease. Expert Rev Respir Med 2013; 7:245–257 [View Article]
    [Google Scholar]
  67. Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L et al. Analysis of the lung microbiome in the “healthy” smoker and in COPD. PLOS One 2011; 6:e16384 [View Article]
    [Google Scholar]
  68. Charlson ES, Bittinger K, Chen J, Diamond JM, Li H et al. Assessing bacterial populations in the lung by replicate analysis of samples from the upper and lower respiratory tracts. PLOS One 2012; 7:e42786 [View Article]
    [Google Scholar]
  69. Man W, de Steenhuijsen Piters W, Bogaert D. The microbiota of the respiratory tract: gatekeeper to respiratory health. Nat Rev Microbiol 2017; 15:259–270 [View Article]
    [Google Scholar]
  70. Dinwiddie D, Schwalm K, Hardin O, Stoner A, Denson J et al. The nasopharyngeal microbiome is perturbed during respiratory viral infections and asthmatic exacerbations. Sequencing, finishing, and analysis in the future meeting [Internet]; 2017 http://programme.exordo.com/sfaf2017/delegates/presentation/96/
  71. Verhagen LM, Rivera-Olivero IA, Clerc M, Chu MLJN, van Engelsdorp Gastelaars J et al. Nasopharyngeal microbiota profiles in rural venezuelan children are associated with respiratory and gastrointestinal infections. Clin Infect Dis 2021; 72:212–221 [View Article]
    [Google Scholar]
  72. Fokkens W, Lund V, Mullol J, Bachert C, Alobid I et al. European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinol J 2012; 50:1–12 [View Article]
    [Google Scholar]
  73. Santee CA, Nagalingam NA, Faruqi AA, DeMuri GP, Gern JE et al. Nasopharyngeal microbiota composition of children is related to the frequency of upper respiratory infection and acute sinusitis. Microbiome 2016; 4:34 [View Article]
    [Google Scholar]
  74. Rawlings BA, Higgins TS, Han JK. Bacterial pathogens in the nasopharynx, nasal cavity, and osteomeatal complex during wellness and viral infection. Am J Rhinol Allergy 2013; 27:39–42 [View Article]
    [Google Scholar]
  75. Hauser LJ, Ir D, Kingdom TT. Investigation of bacterial repopulation after sinus surgery and perioperative antibiotics. Int Forum Allergy Rhinol 2016; 6:34–40 [View Article]
    [Google Scholar]
  76. Shibao S, Toda M, Tomita T, Ogawa K, Yoshida K. Analysis of the bacterial flora in the nasal cavity and the sphenoid sinus mucosa in patients operated on with an endoscopic endonasal transsphenoidal approach. Neurol Med-Chir 2014; 54:1009–1013 [View Article]
    [Google Scholar]
  77. Bluestone C, Stephenson J, Martin L. Ten-year review of otitis media pathogens. Ped Infect Dis J 1992; 11:S7–11 [View Article]
    [Google Scholar]
  78. Hendolin P, Markkanen A, Ylikoski J, Wahlfors J. Use of multiplex PCR for simultaneous detection of four bacterial species in middle ear effusions. J Clin Microbiol 1997; 35:2854–2858 [View Article]
    [Google Scholar]
  79. Harimaya A, Takada R, Hendolin P, Fujii N, Ylikoski J et al. High incidence of Alloiococcus otitidis in children with otitis media, despite treatment with antibiotics. J Clin Microbiol 2006; 44:946–949 [View Article]
    [Google Scholar]
  80. de Barre T, Hollants J, Waetens A, Huyghe J, Cuvelier C et al. Otitis media microbes: culture, PCR, and confocal laser scanning microscopy. B-ENT 1990; 5:65–72
    [Google Scholar]
  81. De Baere T, Vaneechoutte M, Deschaght P, Huyghe J, Dhooge I. The prevalence of middle ear pathogens in the outer ear canal and the nasopharyngeal cavity of healthy young adults. Clin Microbiol Infect 2010; 16:1031–1035 [View Article]
    [Google Scholar]
  82. Stroman D, Roland P, Dohar J, Burt W. Microbiology of normal external auditory canal. Laryngoscope 2001; 111:2054–2059 [View Article]
    [Google Scholar]
  83. Coleman A, Wood A, Bialasiewicz S, Ware R, Marsh R et al. The unsolved problem of otitis media in indigenous populations: a systematic review of upper respiratory and middle ear microbiology in indigenous children with otitis media. Microbiome 2018; 6: [View Article]
    [Google Scholar]
  84. Smith-Vaughan HC, Binks MJ, Marsh RL, Kaestli M, Ward L et al. Dominance of Haemophilus influenzae in ear discharge from Indigenous Australian children with acute otitis media with tympanic membrane perforation. BMC Ear Nose Throat Disord 2013; 13:12 [View Article]
    [Google Scholar]
  85. Lappan R, Imbrogno K, Sikazwe C, Anderson D, Mok D et al. A microbiome case-control study of recurrent acute otitis media identified potentially protective bacterial genera. BMC Microbiol 2018; 18:13 [View Article]
    [Google Scholar]
  86. Martínez-Martínez L, Pascual A, Bernard K, Suárez AI. Antimicrobial susceptibility pattern of Corynebacterium striatum. Antimicrob Agent Chemother 1996; 40:2671–2672 [View Article]
    [Google Scholar]
  87. Laclaire L, Facklam R. Antimicrobial susceptibility and clinical sources of Dolosigranulum pigrum cultures. Antimicrob Agent Chemother 2000; 44:2001–2003 [View Article]
    [Google Scholar]
  88. National Institute for Clinical Excellence. Otitis media (acute): antimicrobial prescribing. Public Health England 2018
    [Google Scholar]
  89. Wiertsema SP, Chidlow GR, Kirkham LAS, Corscadden KJ, Mowe EN et al. High detection rates of nucleic acids of a wide range of respiratory viruses in the nasopharynx and the middle ear of children with a history of recurrent acute otitis media. J Med Virol 2011; 83:2008–2017 [View Article]
    [Google Scholar]
  90. Hasegawa K, Mansbach JM, Ajami NJ, Espinola JA, Henke DM et al. Association of nasopharyngeal microbiota profiles with bronchiolitis severity in infants hospitalised for bronchiolitis. Eur Respir J 2016; 48:1329–1339 [View Article]
    [Google Scholar]
  91. Hasegawa K, Mansbach JM, Ajami NJ, Petrosino JF, Freishtat RJ et al. The relationship between nasopharyngeal CCL5 and microbiota on disease severity among infants with bronchiolitis. Allergy 2017; 72:1796–1800 [View Article]
    [Google Scholar]
  92. Luna PN, Hasegawa K, Ajami NJ, Espinola JA, Henke DM et al. The association between anterior nares and nasopharyngeal microbiota in infants hospitalized for bronchiolitis. Microbiome 2018; 6:2 [View Article]
    [Google Scholar]
  93. Hasegawa K, Linnemann RW, Mansbach JM, Ajami NJ, Espinola JA et al. Nasal airway microbiota profile and severe bronchiolitis in infants: A case-control study. Pediatr Infect Dis J 2017; 36:1044–1051 [View Article]
    [Google Scholar]
  94. Stewart CJ, Mansbach JM, Wong MC, Ajami NJ, Petrosino JF et al. Associations of nasopharyngeal metabolome and microbiome with severity among infants with bronchiolitis. A multiomic analysis. Am J Respir Crit Care Med 2017; 196:882–891 [View Article]
    [Google Scholar]
  95. van den Bergh MR, Biesbroek G, Rossen JW, de Steenhuijsen Piters WA, Bosch AA et al. Associations between pathogens in the upper respiratory tract of young children: interplay between viruses and bacteria. PLOS One 2012; 7:10e47711 [View Article]
    [Google Scholar]
  96. Man W, van Houten M, Mérelle M, Vlieger A, Chu M et al. Bacterial and viral respiratory tract microbiota and host characteristics in children with lower respiratory tract infections: a matched case-control study. Lancet Respir Med 2019; 7:417–426 [View Article]
    [Google Scholar]
  97. Dubourg G, Edouard S, Raoult D. Relationship between nasopharyngeal microbiota and patient’s susceptibility to viral infection. Exp Rev Anti-infect Ther 2019; 17:437–447 [View Article]
    [Google Scholar]
  98. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, JH H et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A 2011; 108:5354–5359 [View Article]
    [Google Scholar]
  99. Thapa S, Runge J, Venkatachalam A, Denne C, Luna R. The nasopharyngeal and gut microbiota in children in a pediatric otolaryngology practice. Ped Infect Dis J 2020; 39:e226 [View Article]
    [Google Scholar]
  100. Manenzhe RI, Moodley C, Abdulgader SM, Robberts FJL, Zar HJ et al. Nasopharyngeal carriage of antimicrobial-resistant pneumococci in an intensively sampled south african birth cohort. Front Microbiol 2019; 10:610 [View Article]
    [Google Scholar]
  101. Moodley D, Reddy L, Mahungo W, Masha R. Factors associated with coverage of cotrimoxazole prophylaxis in HIV-exposed children in South Africa. PLOS ONE 2013; 8:e63273 [View Article]
    [Google Scholar]
  102. Miao Q, Ma Y, Wang Q, Pan J, Zhang Y et al. Microbiological diagnostic performance of metagenomic next-generation sequencing when applied to clinical practice. Clin Infect Dis 2018; 67:S231–S240S240 [View Article]
    [Google Scholar]
  103. Mellmann A, Bletz S, Böking T, Kipp F, Becker K et al. Real-time genome sequencing of resistant bacteria provides precision infection control in an institutional setting. J Clin Microbiol 2016; 54:2874–2881 [View Article]
    [Google Scholar]
  104. World Health Organisation WHO guidelines for the collection of human specimens for laboratory diagnosis of avian influenza infection; 2005 https://www.who.int/influenza/human_animal_interface/virology_laboratories_and_vaccines/guidelines_collection_h5n1_humans/en/
  105. Marty FM, Chen K, Verrill KA. How to Obtain a Nasopharyngeal Swab Specimen. N Engl J Med 2020; 382:e76 [View Article]
    [Google Scholar]
  106. Hiebert N, Chen B, Sowerby L. Variability in instructions for performance of nasopharyngeal swabs across Canada in the era of COVID-19 – what type of swab is actually being performed?. J Otolaryngol - Head Neck Surg 2021; 50: [View Article]
    [Google Scholar]
  107. Nwaokorie K, Woods R, Crowley J, Walsh M, de Barra E et al. Analysing the accuracy of healthcare proffesionals’ nasopharyngeal swab technique in SARS-COV-2 specimen collection. Academic Meeting of the Irish Otorhinolaryngology / Head and Neck Society 20207
    [Google Scholar]
  108. Flynn M, Kelly M, Dooley J. Nasopharyngeal aspirates vs. nasal swabs for the detection of respiratory pathogens: results of a rapid review protocol. MedRxiv 2020
    [Google Scholar]
  109. Hiebert N, Chen B, Sowerby L. Variability in instructions for performance of nasopharyngeal swabs across Canada in the era of COVID-19 – what type of swab is actually being performed?. J Otolaryngol - Head Neck Surg 2021; 50: [View Article]
    [Google Scholar]
  110. Pérez-Losada M, Crandall KA, Freishtat RJ. Two sampling methods yield distinct microbial signatures in the nasopharynges of asthmatic children. Microbiome 2016; 4:25 [View Article]
    [Google Scholar]
  111. Yan M, Pamp S, Fukuyama J, Hwang P, Cho D et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe 2013; 14:631–640 [View Article]
    [Google Scholar]
  112. Wang H, Dai W, Feng X, Zhou Q, Wang H. Microbiota composition in upper respiratory tracts of healthy children in Shenzhen, China, differed with respiratory sites and ages. BioMed Res Int 2018; 2018:1–8 [View Article]
    [Google Scholar]
  113. Lieberman D, Shleyfer E, Castel H, Terry A, Harman-Boehm I et al. Nasopharyngeal versus oropharyngeal sampling for isolation of potential respiratory pathogens in adults. J Clin Microbiol 2006; 44:525–528 [View Article]
    [Google Scholar]
  114. Gritzfeld JF, Roberts P, Roche L, El Batrawy S, Gordon SB. Comparison between nasopharyngeal swab and nasal wash, using culture and PCR, in the detection of potential respiratory pathogens. BMC Res Notes 2011; 4:122 [View Article]
    [Google Scholar]
  115. Pérez-Losada M, Alamri L, Crandall KA, Freishtat RJ. Nasopharyngeal microbiome diversity changes over time in children with asthma. PLOS ONE 2017; 12:e0170543 [View Article]
    [Google Scholar]
  116. Kinloch NN, Shahid A, Ritchie G, Dong W, Lawson T et al. Evaluation of nasopharyngeal swab collection techniques for nucleic acid recovery and participant experience: Recommendations for COVID-19 diagnostics. Open Forum Infect Dis 2020; 7:ofaa488 [View Article]
    [Google Scholar]
  117. Lu Y, Wang S, Liou M, Shen T, Lu Y-C et al. Microbiota dysbiosis in fungal rhinosinusitis. J Clin Med 2019; 8:11 [View Article]
    [Google Scholar]
  118. Carver C, Jones N. Comparative accuracy of oropharyngeal and nasopharyngeal swabs for diagnosis of COVID-19 - CEBM [Internet]. CEBM; 2020 https://www.cebm.net/covid-19/comparative-accuracy-of-oropharyngeal-and-nasopharyngeal-swabs-for-diagnosis-of-covid-19/
  119. Leven M, Vercauteren E, Descheemaeker P, van Laer F, Goossens H. Comparison of direct plating and broth enrichment culture for the detection of intestinal colonization by glycopeptide-resistant enterococci among hospitalized patients. J Clin Microbiol 1999 [View Article]
    [Google Scholar]
  120. Choo JM, Leong LE, Rogers GB. Sample storage conditions significantly influence faecal microbiome profiles. Sci Rep 2015; 5:16350 [View Article]
    [Google Scholar]
  121. Shaikh N, Hoberman A, Colborn D, Kearney D, Jeong J. Are nasopharyngeal cultures useful in diagnosis of acute bacterial sinusitis in children. Clin Ped 2013; 52:1118–1121 [View Article]
    [Google Scholar]
  122. Stępińska M, Olszewska-Sosińska O, Lau-Dworak M, Zielnik-Jurkiewicz B, Trafny E. Identification of Intracellular Bacteria in Adenoid and Tonsil Tissue Specimens: The Efficiency of Culture Versus Fluorescent In Situ Hybridization (FISH). Curr Microbiol 2013; 68:21–29 [View Article]
    [Google Scholar]
  123. Tokman H, Aslan M, Kalayci F, Demir T, Kocazeybek B. Microorganisms in respiratory tract of patients diagnosed with atypical pneumonia: Results of a research based on the use of reverse transcription polymerase chain reaction (RT-PCR) DNA. Clin Lab 2014; 60:06 [View Article]
    [Google Scholar]
  124. Arevalo-Rodriguez I, Buitrago-Garcia D, Simancas-Racines D, Zambrano-Achig P, del Campo R et al. False-negative results of initial RT-PCR assays for COVID-19: A systematic Review. medRxiv Pre-print 2020 [View Article]
    [Google Scholar]
  125. Rutebemberwa E, Mpeka B, Pariyo G, Peterson S, Mworozi E et al. High prevalence of antibiotic resistance in nasopharyngeal bacterial isolates from healthy children in rural Uganda: A cross-sectional study. Ups J Med Sci 2015; 120:249–256 [View Article]
    [Google Scholar]
  126. Mika M, Maurer J, Korten I, Allemann A, Aebi S et al. Influence of the pneumococcal conjugate vaccines on the temporal variation of pneumococcal carriage and the nasal microbiota in healthy infants: a longitudinal analysis of a case–control study. Microbiome 2017; 5: [View Article]
    [Google Scholar]
  127. Glück U, Gebbers J. Ingested probiotics reduce nasal colonization with pathogenic bacteria (Staphylococcus aureus, Streptococcus pneumoniae, and β-hemolytic streptococci. Am J Clin Nut 2003; 77:517–520 [View Article]
    [Google Scholar]
  128. Uehara Y, Nakama H, Agematsu K, Uchida M, Kawakami Y et al. Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J Hosp Infect 2000; 44:127–133 [View Article]
    [Google Scholar]
  129. Kanmani P, Clua P, Vizoso-Pinto MG, Rodriguez C, Alvarez S et al. Respiratory commensal bacteria Corynebacterium pseudodiphtheriticum improves resistance of infant mice to respiratory syncytial virus and Streptococcus pneumoniae superinfection. Front Microbiol 2017; 8:1613 [View Article]
    [Google Scholar]
  130. Quainoo S, Coolen JPM, van Hijum SAFT, Huynen MA, Melchers WJG et al. Whole-genome sequencing of bacterial pathogens: the future of nosocomial outbreak analysis. Clin Microbiol Rev 2017; 30:1015–1063 [View Article]
    [Google Scholar]
  131. Meredith L, Hamilton W, Warne B, Houldcroft C, Hosmillo M et al. Rapid implementation of SARS-CoV-2 sequencing to investigate cases of health-care associated COVID-19: a prospective genomic surveillance study. Lancet Infect Dis 2020; 20:1263–1271 [View Article]
    [Google Scholar]
  132. Couturier M, Bard J. Direct-from-specimen pathogen identification. Clin Lab Med 2019; 39:433–451 [View Article]
    [Google Scholar]
  133. van Belkum A, Rochas O. Laboratory-based and point-of-care testing for MSSA/MRSA detection in the age of whole genome sequencing. Front Microbiol 2018; 9:1437 [View Article]
    [Google Scholar]
  134. Abramson M, Wolfe R. Prediction models in respiratory medicine. Respirology 2020; 25:666–667 [View Article]
    [Google Scholar]
  135. Lamarche D, Johnstone J, Zytaruk N, Clarke F, Hand L et al. Microbial dysbiosis and mortality during mechanical ventilation: a prospective observational study. Respir Res 2018; 19: [View Article]
    [Google Scholar]
  136. Xu Z, Xie Z, Sun J, Huang S, Chen Y et al. Gut microbiome reveals specific dysbiosis in primary osteoporosis. Front Cell Infect Microbiol 2020; 10:160 [View Article]
    [Google Scholar]
  137. Kwak S, Choi J, Hink T, Reske K, Blount K et al. Impact of investigational microbiota therapeutic RBX2660 on the gut microbiome and resistome revealed by a placebo-controlled clinical trial. Microbiome 2020; 8: [View Article]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001368
Loading
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error