Skip to main content

Acute exacerbations of chronic obstructive pulmonary disease: etiological bacterial pathogens and antibiotic resistance in Upper Egypt



Previous data on etiologic bacteria in acute exacerbations of chronic obstructive pulmonary disease (AECOPD) in Upper Egypt are limited.


The aim of this study was to identify the causative bacteria in AECOPD and to determine the antibiotic resistance patterns for AECOPD in Upper Egypt.

Settings and design

The study design was a prospective one and was conducted in a University Hospital.

Materials and methods

Patients who were admitted in Assiut University Hospital with AECOPD were prospectively enrolled. Sputum specimens were investigated using culture. Susceptibilities of the isolated bacterial strains to different antibiotics were determined using the disk diffusion method.


During 18 months, 156 patients who experienced 218 AECOPD were enrolled. A significant bacterial growth was found in 77% of patients during 81% of exacerbations. The most commonly detected bacteria were Haemophilus influenzae (18%), Streptococcus pneumoniae (15%), and Klebsiella pneumoniae (14%). The majority of the isolated strains showed high resistance rates to most groups of antibiotics; 63% of the isolated strains were multidrug resistant, 29% were extensively drug resistant, and 5% were pandrug resistant. High resistance rates were observed against penicillins and cephalosporins, moderate rates against fluoroquinolones, and lowest rates against the carbapenems. All gram-positive bacteria were sensitive to linezolid. Increased severity of chronic obstructive pulmonary disease was related to increased prevalence of antibiotic resistance.


The predominant bacterial pathogens for AECOPD in Upper Egypt are H. influenzae, S. pneumoniae, and K. pneumoniae. Bacterial resistance rates were the highest against penicillins and cephalosporins, moderate against fluoroquinolones, and least against carbapenems. Increased severity of chronic obstructive pulmonary disease is related to an increased prevalence of antibiotic resistance.


  1. Perera WR, Hurst JR, Wilkinson TM, Sapsford RJ, Müllerova H, Donaldson GC, Wedzicha JA. Inflammatory changes, recovery and recurrence at COPD exacerbation. Eur Respir J 2007; 29:527–534.

    Article  CAS  Google Scholar 

  2. Global Initiative for Chronic Obstructive Lung Disease. Global strategy for the diagnosis, management and prevention of COPD, updated 2015. Available at:

  3. Donaldson GC, Seemungal TA, Bhowmik A, Wedzicha JA. Relationship between exacerbation frequency and lung function decline in chronic obstructive pulmonary disease. Thorax 2002; 57:847–852.

    Article  CAS  Google Scholar 

  4. Kyd JM, McGrath J, Krishnamurthy A. Mechanisms of bacterial resistance to antibiotics in infections of COPD patients. Curr Drug Targets 2011; 12:521–530.

    Article  CAS  Google Scholar 

  5. Agmy G, Mohamed S, Gad Y, Farghally E, Mohammedin H, Rashed H. Bacterial profile, antibiotic sensitivity and resistance of lower respiratory tract infections in Upper Egypt. Mediterr J Hematol Infect Dis 2013; 5: e2013056.

    Article  Google Scholar 

  6. Indrayan A, Kumar R, Dwivedi S. “A simple index of smoking” (November 2008). COBRA Preprint Series. Working Paper 40. Available at:

  7. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. ATS/ERS Task Force General considerations for lung function testing. Eur Respir J 2005; 26:153–161.

    Article  CAS  Google Scholar 

  8. Henig NR, Tonelli MR, Pier MV, Burns JL, Aitken ML. Sputum induction as a research tool for sampling the airways of subjects with cystic fibrosis. Thorax 2001; 56:306–311.

    Article  CAS  Google Scholar 

  9. Holt JG, Krieg NR, Sneath PHA, Staley H, Williams ST. Bergeys manual of determinative bacteriology. 9th ed. Baltimore, MD: Lippincott Williams and Wilkins; 1994.

    Google Scholar 

  10. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk susceptibility tests. 9th ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2006.

    Google Scholar 

  11. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pan drug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281.

    Article  CAS  Google Scholar 

  12. White AJ, Gompertz S, Stockley RA. Chronic obstructive pulmonary disease. 6: the aetiology of exacerbations of chronic obstructive pulmonary disease. Thorax 2003; 58:73–80.

    Article  CAS  Google Scholar 

  13. Wedzicha JA, Donaldson GC. Exacerbations of chronic obstructive pulmonary disease. Respir Care 2003; 48:1204–1213 discussion 1213–1215.

    PubMed  Google Scholar 

  14. Zalacain R, Sobradillo V, Amilibia J, Barrón J, Achótegui V, Pijoan JI, Llorente JL. Predisposing factors to bacterial colonization in chronic obstructive pulmonary disease. Eur Respir J 1999; 13:343–348.

    Article  CAS  Google Scholar 

  15. Hill AT, Campbell EJ, Hill SL, Bayley DL, Stockley RA. Association between airway bacterial load and markers of airway inflammation in patients with stable chronic bronchitis. Am J Med 2000; 109:288–295.

    Article  CAS  Google Scholar 

  16. Nakou A, Papaparaskevas J, Diamantea F, Skarmoutsou N, Polychronopoulos V, Tsakris A. A prospective study on bacterial and atypical etiology of acute exacerbation in chronic obstructive pulmonary disease. Future Microbiol 2014; 9:1251–1260.

    Article  CAS  Google Scholar 

  17. White AJ, Gompertz S, Bayley DL, Hill SL, O’Brien C, Unsal I, Stockley RA. Resolution of bronchial inflammation is related to bacterial eradication following treatment of exacerbations of chronic bronchitis. Thorax 2003; 58:680–685.

    Article  CAS  Google Scholar 

  18. Hunter MH, King DE. COPD: management of acute exacerbations and chronic stable disease. Am Fam Physician 2001; 64:603–612.

    CAS  PubMed  Google Scholar 

  19. Nowiński A, Kamiński D, Korzybski D, Stokłosa A, Górecka D. The impact of comorbidities on the length of hospital treatment in patients with chronic obstructive pulmonary disease. Pneumonol Alergol Pol 2011; 79:388–396.

    PubMed  Google Scholar 

  20. Mohan A, Premanand R, Reddy LN, Rao MH, Sharma SK, Kamity R, Bollineni S. Clinical presentation and predictors of outcome in patients with severe acute exacerbation of chronic obstructive pulmonary disease requiring admission to intensive care unit. BMC Pulm Med 2006; 6:27.

    Article  Google Scholar 

  21. Ko FW, Ng TK, Li TS, Fok JP, Chan MC, Wu AK, Hui DS. Sputum bacteriology in patients with acute exacerbations of COPD in Hong Kong. Respir Med 2005; 99:454–460.

    Article  Google Scholar 

  22. Molyneaux PL, Mallia P, Cox MJ, Footitt J, Willis-Owen SA, Homola D, et al. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2013; 188:1224–1231.

    Article  Google Scholar 

  23. Bogaert D, van der Valk P, Ramdin R, Sluijter M, Monninkhof E, Hendrix R, et al. Host-pathogen interaction during pneumococcal infection in patients with chronic obstructive pulmonary disease. Infect Immun 2004; 72:818–823.

    Article  CAS  Google Scholar 

  24. Groenewegen KH, Wouters EF. Bacterial infections in patients requiring admission for an acute exacerbation of COPD: a 1-year prospective study. Respir Med 2003; 97:770–777.

    Article  Google Scholar 

  25. González-Castillo J, Cenci C, Rodriguez-Adrada E, Candel FJ, de la Torre-Misiego F, Fernández C, Martín-Sánchez FJ. Staphylococcus aureus infections and factors associated with resistance to methicillin in a hospital emergency department. Rev Esp Quimioter 2013; 26:337–345.

    PubMed  Google Scholar 

  26. Falagas ME, Karveli EA, Kelesidis I, Kelesidis T. Community-acquired Acinetobacter infections. Eur J Clin Microbiol Infect Dis 2007; 26:857–868.

    Article  CAS  Google Scholar 

  27. Li XJ, Li Q, Si LY, Yuan QY. Bacteriological differences between COPD exacerbation and community-acquired pneumonia. Respir Care 2011; 56:1818–1824.

    Article  Google Scholar 

  28. Madhavi S, Rama Rao MV, Janardhan Rao R. Bacterial etiology of acute exacerbations of chronic obstructive pulmonary disease. J Microbiol Biotech Res 2012; 2:440–444.

    CAS  Google Scholar 

  29. Lode H, Eller J, Linnhoff A, Ioanas M, Evaluation of Therapy-Free Interval in COPD Patients Study Group. Levofloxacin versus clarithromycin in COPD exacerbation: focus on exacerbation-free interval. Eur Respir J 2004; 24:947–953.

    Article  Google Scholar 

  30. Thwaites GE. The management of Staphylococcus aureus bacteremia in the United Kingdom and Vietnam: a multicentre evaluation. PLoS One 2010; 5:14170.

    Article  Google Scholar 

  31. Borg MA, de Kraker M, Scicluna E, van de Sande-Bruinsma N, Tiemersma E, Monen J, Grundmann H, ARMed Project Members and Collaborators. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in invasive isolates from southern and eastern Mediterranean countries. J Antimicrob Chemother 2007; 60:1310–1315.

    Article  CAS  Google Scholar 

  32. Johnson AP, Warner M, Livermore DM. Activity of linezolid against multiresistant gram-positive bacteria from diverse hospitals in the United Kingdom. J Antimicrob Chemother 2000; 45:225–230.

    Article  CAS  Google Scholar 

  33. El-Korashy RI, El-Sherif RH. Gram negative organisms as a cause of acute exacerbation of COPD. EJCDT 2014; 63:345–349.

    Google Scholar 

  34. Ye F, He LX, Cai BQ, Wen FQ, Chen BY, Hadiarto M, et al. Spectrum and antimicrobial resistance of common pathogenic bacteria isolated from patients with acute exacerbation of chronic obstructive pulmonary disease in mainland of China. Chin Med J (Engl) 2013; 126:2207–2214.

    Google Scholar 

  35. Nseir S, Di Pompeo C, Cavestri B, Jozefowicz E, Nyunga M, Soubrier S, et al. Multiple-drug-resistant bacteria in patients with severe acute exacerbation of chronic obstructive pulmonary disease: prevalence, risk factors, and outcome. Crit Care Med 2006; 34:2959–2966.

    Article  CAS  Google Scholar 

  36. Fogarty CM, Kohno S, Buchanan P, Aubier M, Baz M. Communityacquired respiratory tract infections caused by resistant pneumococci: clinical and bacteriological efficacy of the ketolide telithromycin. J Antimicrob Chemother 2003; 51:947–955.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations


Corresponding author

Correspondence to Sherif A. A. Mohamed.

Additional information

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

Rights and permissions

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hassan, A.T., Mohamed, S.A.A., Mohamed, M.S.E. et al. Acute exacerbations of chronic obstructive pulmonary disease: etiological bacterial pathogens and antibiotic resistance in Upper Egypt. Egypt J Bronchol 10, 283–290 (2016).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: