A Polymicrobial Perspective of Pulmonary Infections Exposes an Enigmatic Pathogen in Cystic Fibrosis Patients

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2008 Sep 25

PMID 18812504

Citations 175

Authors

Christopher D Sibley

Michael D Parkins

Harvey R Rabin

Kangmin Duan

Jens C Norgaard

Michael G Surette

Affiliations

Soon will be listed here.

Abstract

Lung disease is the leading cause of morbidity and mortality in cystic fibrosis (CF) patients. A modest number of bacterial pathogens have been correlated with pulmonary function decline; however, microbiological and molecular evidence suggests that CF airway infection is polymicrobial. To obtain a more complete assessment of the microbial community composition and dynamics, we undertook a longitudinal study by using culture-independent and microbiological approaches. In the process, we demonstrated that within complex and dynamic communities, the Streptococcus milleri group (SMG) can establish chronic pulmonary infections and at the onset of 39% of acute pulmonary exacerbations, SMG is the numerically dominant pathogen. We report the comprehensive polymicrobial community dynamics of a CF lung infection in a clinically relevant context. If a given organism, such as Pseudomonas aeruginosa, becomes resistant to antibiotic therapy, an alternative treatment avenue may mediate the desired clinical response by effectively managing the composition of the microbial community.

Citing Articles

Effect of cell-free culture on bacterial pathogens isolated from cystic fibrosis patients: and studies.

Aban C, Orosco S, Arganaraz Aybar J, Albarracin L, Venecia A, Perret L Front Microbiol. 2024; 15:1440090.

PMID: 39351305 PMC: 11439784. DOI: 10.3389/fmicb.2024.1440090.

Practical Guidance for Clinical Microbiology Laboratories: Updated guidance for processing respiratory tract samples from people with cystic fibrosis.

Saiman L, Waters V, LiPuma J, Hoffman L, Alby K, Zhang S Clin Microbiol Rev. 2024; 37(3):e0021521.

PMID: 39158301 PMC: 11391703. DOI: 10.1128/cmr.00215-21.

Dpr-mediated HO resistance contributes to streptococcus survival in a cystic fibrosis airway model system.

Rogers R, Kesthely C, Jean-Pierre F, El Hafi B, OToole G J Bacteriol. 2024; 206(7):e0017624.

PMID: 38940597 PMC: 11270861. DOI: 10.1128/jb.00176-24.

Exploring the microbiota difference of bronchoalveolar lavage fluid between community-acquired pneumonia with or without COPD based on metagenomic sequencing: a retrospective study.

Wang B, Tan M, Li W, Xu Q, Jin L, Xie S BMC Pulm Med. 2024; 24(1):278.

PMID: 38867204 PMC: 11167785. DOI: 10.1186/s12890-024-03087-6.

Association between oral microbiome and five types of respiratory infections: a two-sample Mendelian randomization study in east Asian population.

He J, Mao N, Lyu W, Zhou S, Zhang Y, Liu Z Front Microbiol. 2024; 15:1392473.

PMID: 38659993 PMC: 11039966. DOI: 10.3389/fmicb.2024.1392473.

References

Shain H, Homer K, Beighton D . Degradation and utilisation of chondroitin sulphate by Streptococcus intermedius. J Med Microbiol. 1996; 44(5):372-80. DOI: 10.1099/00222615-44-5-372. View

Ball J, Malhotra R, Leong P, BACON A . The importance of recognising Streptococcus milleri as a cause of orbital cellulitis. Eye (Lond). 2000; 14 Pt 5:814-5. DOI: 10.1038/eye.2000.226. View

Eisen M, Spellman P, Brown P, Botstein D . Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998; 95(25):14863-8. PMC: 24541. DOI: 10.1073/pnas.95.25.14863. View

PARKER M, Ball L . Streptococci and aerococci associated with systemic infection in man. J Med Microbiol. 1976; 9(3):275-302. DOI: 10.1099/00222615-9-3-275. View

Hardwick R, Taylor A, Thompson M, Jones E, Roe A . Association between Streptococcus milleri and abscess formation after appendicitis. Ann R Coll Surg Engl. 2000; 82(1):24-6. PMC: 2503455. View

Parkins M, Sibley C, Surette M, Rabin H . The Streptococcus milleri group--an unrecognized cause of disease in cystic fibrosis: a case series and literature review. Pediatr Pulmonol. 2008; 43(5):490-7. DOI: 10.1002/ppul.20809. View

Ong E, Ellis M, Webb A, Neal K, Dodd M, Caul E . Infective respiratory exacerbations in young adults with cystic fibrosis: role of viruses and atypical microorganisms. Thorax. 1989; 44(9):739-42. PMC: 462055. DOI: 10.1136/thx.44.9.739. View

Whiley R, Beighton D, Winstanley T, Fraser H, Hardie J . Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus (the Streptococcus milleri group): association with different body sites and clinical infections. J Clin Microbiol. 1992; 30(1):243-4. PMC: 265033. DOI: 10.1128/jcm.30.1.243-244.1992. View

Yamamoto N, Kubota T, Tohyama M, Kanamori S, Shinzato T, Higa F . Trends in antimicrobial susceptibility of the Streptococcus milleri group. J Infect Chemother. 2002; 8(2):134-7. DOI: 10.1007/s101560200023. View

10.

Smith E, Buckley D, Wu Z, Saenphimmachak C, Hoffman L, DArgenio D . Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A. 2006; 103(22):8487-92. PMC: 1482519. DOI: 10.1073/pnas.0602138103. View

11.

Rajan S, Saiman L . Pulmonary infections in patients with cystic fibrosis. Semin Respir Infect. 2002; 17(1):47-56. DOI: 10.1053/srin.2002.31690. View

12.

Tunney M, Field T, Moriarty T, Patrick S, Doering G, Muhlebach M . Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Respir Crit Care Med. 2008; 177(9):995-1001. DOI: 10.1164/rccm.200708-1151OC. View

13.

Smith J, Travis S, Greenberg E, Welsh M . Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell. 1996; 85(2):229-36. DOI: 10.1016/s0092-8674(00)81099-5. View

14.

Bourgault A, Wilson W, Washington 2nd J . Antimicrobial susceptibilities of species of viridans streptococci. J Infect Dis. 1979; 140(3):316-21. DOI: 10.1093/infdis/140.3.316. View

15.

CADE A, Denton M, Brownlee K, Todd N, Conway S . Acute bronchopulmonary infection due to Streptococcus milleri in a child with cystic fibrosis. Arch Dis Child. 1999; 80(3):278-9. PMC: 1717868. DOI: 10.1136/adc.80.3.278. View

16.

Van der Auwera P . Clinical significance of Streptococcus milleri. Eur J Clin Microbiol. 1985; 4(4):386-90. DOI: 10.1007/BF02148688. View

17.

Rogers G, Carroll M, Serisier D, Hockey P, Jones G, Kehagia V . Use of 16S rRNA gene profiling by terminal restriction fragment length polymorphism analysis to compare bacterial communities in sputum and mouthwash samples from patients with cystic fibrosis. J Clin Microbiol. 2006; 44(7):2601-4. PMC: 1489498. DOI: 10.1128/JCM.02282-05. View

18.

Hartmann M, Widmer F . Reliability for detecting composition and changes of microbial communities by T-RFLP genetic profiling. FEMS Microbiol Ecol. 2008; 63(2):249-60. DOI: 10.1111/j.1574-6941.2007.00427.x. View

19.

Ball L, PARKER M . The cultural and biochemical characters of Streptococcus milleri strains isolated from human sources. J Hyg (Lond). 1979; 82(1):63-78. PMC: 2130127. DOI: 10.1017/s002217240002547x. View

20.

Jacobs J, Stobberingh E . Hydrolytic enzymes of Streptococcus anginosus, Streptococcus constellatus and Streptococcus intermedius in relation to infection. Eur J Clin Microbiol Infect Dis. 1995; 14(9):818-20. DOI: 10.1007/BF01691002. View