The first study characterizing the respiratory microbiome in cystic fibrosis patients in Jordan

Main Article Content

Ahmad R Alsayed https://orcid.org/0000-0002-1324-7884
Anas Abed https://orcid.org/0000-0003-4938-0756
Malek Zihlif https://orcid.org/0000-0002-8005-3908
Mahmoud S Abu-Samak https://orcid.org/0000-0002-6980-7895
Rana Ahmad Almuhur https://orcid.org/0000-0002-8628-8660
Mohammad Alkhatib https://orcid.org/0000-0002-3160-0637

Keywords

Cystic fibrosis, Respiratory, Microbiome , Jordan, Epidemiology

Abstract

Cystic fibrosis (CF) is most commonly seen in Caucasians and is uncommon in the Middle East. This study, based in Jordan, aimed to describe the association between lung exacerbation in CF patients and the respiratory microbiome composition. Using the 16S rRNA marker-gene sequencing, we investigated the microbiota in sputa during exacerbation (E1) and 14 days after the exacerbation (E2) of two CF patients admitted to the hospital. Detected genera with high abundance in the E1-related sputa of the first patient included Achromobacter and Streptococcus. At E2, Achromobacter and Staphylococcus were the highest abundant genera. Regarding the second patient, Veillonella and Streptococcus, were the highest abundant genera at E1. Whereas, Streptococcus and Veillonella were the highest abundant genera. This is the first study, based in Jordan, to report and describe the respiratory microbiome during and after the exacerbation of CF patients. This study suggests that pulmonary exacerbation in CF patients can result in alterations in their respiratory microbiome. A better knowledge of this link could allow more focused use of antibiotics, especially during exacerbations, improving clinical efficacy and patient outcomes 

Abstract 263 | PDF Downloads 335

References

1. O’Sullivan BP, Freedman SD. Cystic fibrosis. Lancet. 2009;373(9678):1891-1904. https://doi.org/10.1016/s0140-6736(09)60327-60335
2. Alsayed AR, Abed A, Khader HA, et al. Molecular Accounting and Profiling of Human Respiratory Microbial Communities: Toward Precision Medicine by Targeting the Respiratory Microbiome for Disease Diagnosis and Treatment. Int J Mol Sci. 
2023;24(4):4086. https://doi.org/10.3390/ijms24044086
3. Lipuma JJ. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev. 2010;23(2):299-323. https://doi.org/10.1128/cmr.00068-09
4. Surette MG. The cystic fibrosis lung microbiome. Ann Am Thorac Soc. 2014;11(Suppl 1):S61-S65. https://doi.org/10.1513/AnnalsATS.201306-159MG
5. Sanders DB, Bittner RC, Rosenfeld M, et al. Failure to recover to baseline pulmonary function after cystic fibrosis pulmonary exacerbation. Am J Respir Crit Care Med. 2010;182(5):627-32. https://doi.org/10.1164/rccm.200909-1421OC
6. Klepac‐Ceraj V, Lemon KP, Martin TR, et al. Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environmental Microbiology. 2010;12(5):1293-1303. https://doi.
org/10.1111/j.1462-2920.2010.02173.x
7. Zhao J, Schloss PD, Kalikin LM, et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proceedings of the National Academy of Sciences. 2012;109(15):5809-5814. https://doi.org/10.1073/pnas.1120577109
8. Flanagan J, Brodie E, Weng L, et al. Loss of bacterial diversity during antibiotic treatment of intubated patients colonized with Pseudomonas aeruginosa. Journal of Clinical Microbiology. 2007;45(6):1954-1962. https://doi.org/10.1128/JCM.02187-06
9. Cox MJ, Allgaier M, Taylor B, et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PloS One. 2010;5(6):e11044. https://doi.org/10.1371/journal.pone.0011044
10. Rawashdeh M, Manal H. Cystic fibrosis in Arabs: a prototype from Jordan. Ann Trop Paediatr. 2000;20(4):283-286. https://doi.org/10.1080/02724936.2000.11748148
11. Nazer HM. Early diagnosis of cystic fibrosis in Jordanian children. J Trop Pediatr. 1992;38(3):113-115. https://doi.org/10.1093/tropej/38.3.113
12. Comeau AM, Accurso FJ, White TB, et al. Guidelines for implementation of cystic fibrosis newborn screening programs: Cystic Fibrosis Foundation workshop report. Pediatrics. 2007;119(2):e495-e518. https://doi.org/10.1542/peds.2006-1993
13. Farrell PM, Rosenstein BJ, White TB, et al. Guidelines for diagnosis of cystic fibrosis in newborns through older adults: Cystic Fibrosis Foundation consensus report. The Journal of Pediatrics. 2008;153(2):S4-s14. https://doi.org/10.1016/j.
jpeds.2008.05.005
14. De Boeck K, Wilschanski M, Castellani C, et al. Cystic fibrosis: terminology and diagnostic algorithms. Thorax. 2006;61(7):627-635. https://doi.org/10.1136/thx.2005.043539
15. Flume PA, Mogayzel Jr PJ, Robinson KA, et al. Cystic fibrosis pulmonary guidelines: treatment of pulmonary exacerbations. American Journal of Respiratory and Critical Care Medicine. 2009;180(9):802-808. https://doi.org/10.1164/rccm.200812-
1845PP
16. Al-Dulaimi A, Alsayed AR, Maqbali MA, et al. Investigating the human rhinovirus co-infection in patients with asthma exacerbations and COVID-19. Pharm Pract (Granada). 2022;20(2):2665. https://doi.org/10.18549/PharmPract.2022.2.2665
17. Alsayed AR, Talib W, Al-Dulaimi A, et al. The first detection of Pneumocystis jirovecii in asthmatic patients post-COVID-19 in Jordan. Bosn J Basic Med Sci. 2022;22(5):784-790. https://doi.org/10.17305/bjbms.2022.7335
18. Alsayed AR, Hasoun L, Khader HA, et al. Co‑infection of COVID-19 patients with atypical bacteria: A study based in Jordan. Pharmacy Practice. 2023;21(1):1-5. https://doi.org/10.18549/PharmPract.2023.1.2753
19. Alsayed A, Al-Doori A, Al-Dulaimi A, et al. Influences of bovine colostrum on nasal swab microbiome and viral upper respiratory tract infections - A case report. Respir Med Case Rep. 2020;31:101189. https://doi.org/10.1016/j.rmcr.2020.101189
20. Alsayed AR, Abed A, Jarrar YB, et al. Alteration of the Respiratory Microbiome in Hospitalized Patients with Asthma–COPD Overlap during and after an Exacerbation. Journal of Clinical Medicine. 2023;12(6):2118. https://doi.org/10.3390/jcm12062118
21. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nature methods. 2010;7(5):335-336. https://doi.org/10.1038/nmeth.f.303
22. Edgar RC, Haas BJ, Clemente JC, et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194-2200. https://doi.org/10.1093/bioinformatics/btr381
23. Caporaso JG, Bittinger K, Bushman FD, et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2009;26(2):266-267. https://doi.org/10.1093/bioinformatics/btp636
24. Wang Q, Garrity GM, Tiedje JM, et al. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology. 2007;73(16):5261-5267. https://doi.org/10.1128/AEM.00062-07
25. Fodor AA, Klem ER, Gilpin DF, et al. 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(9):e45001. https://doi.org/10.1371/journal.pone.0045001
26. van der Gast CJ, Walker AW, Stressmann FA, et al. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. Isme J. 2011;5(5):780-791. https://doi.org/10.1038/ismej.2010.175
27. Han MK, Huang YJ, Lipuma JJ, et al. Significance of the microbiome in obstructive lung disease. Thorax. May 2012;67(5):456-463. https://doi.org/10.1136/thoraxjnl-2011-201183
28. Madan JC, Koestler DC, Stanton BA, 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(4): e00251-12. https://
doi.org/10.1128/mBio.00251-12
29. O’Neill K, Bradley JM, Johnston E, et al. Reduced bacterial colony count of anaerobic bacteria is associated with a worsening in lung clearance index and inflammation in cystic fibrosis. PloS One. 2015;10(5):e0126980. https://doi.org/10.1371/journal.
pone.0126980
30. Sherrard LJ, Graham KA, McGrath SJ, et al. Antibiotic resistance in Prevotella species isolated from patients with cystic fibrosis. Journal of Antimicrobial Chemotherapy. 2013;68(10):2369-2374. https://doi.org/10.1093/jac/dkt191
31. Hurst JR, Wilkinson TM, Perera WR, et al. Relationships among bacteria, upper airway, lower airway, and systemic inflammation in COPD. CHEST Journal. 2005;127(4):1219-1226. https://doi.org/10.1378/chest.127.4.1219
32. Rogers G, Carroll M, Serisier D, et al. 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. Journal of 
Clinical Microbiology. 2006;44(7):2601-2604. https://doi.org/10.1128/JCM.02282-05
33. Patel I, Seemungal T, Wilks M, et al. Relationship between bacterial colonisation and the frequency, character, and severity of COPD exacerbations. Thorax. 2002;57(9):759-764. https://doi.org/10.1136/thorax.57.9.759
34. Wilkinson TM, Patel IS, Wilks M, et al. Airway bacterial load and FEV1 decline in patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine. 2003;167(8):1090-1095. https://doi.org/10.1164/
rccm.200210-1179OC
35. Tunney MM, Field TR, Moriarty TF, et al. Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. American Journal of Respiratory and Critical Care Medicine. 2008;177(9):995-1001. https://doi.org/10.1164/
rccm.200708-1151oc

Most read articles by the same author(s)