Bacterial Etiology of Lower Respiratory Tract Infections in Turkey: A Systematic Review

authors:

avatar Elmas Pinar Kahraman Kilbas ORCID 1 , * , avatar Imdat Kilbas ORCID 2 , avatar Ihsan Hakki Ciftci ORCID 2

Fenerbahçe University, Vocational School of Health Services, Medical Laboratory Techniques, İstanbul, Turkey
Sakarya University Faculty of Medicine, Department of Clinical Microbiology, Sakarya, Turkey
Journal of Kermanshah University of Medical Sciences: Vol.25, issue 2; e113798
published online: July 11, 2021
article type: Systematic Review
received: February 14, 2021
revised: April 19, 2021
accepted: April 20, 2021
DOI: https://doi.org/10.5812/jkums.113798

how to cite: Kahraman Kilbas E P, Kilbas I, Ciftci I H. Bacterial Etiology of Lower Respiratory Tract Infections in Turkey: A Systematic Review. J Kermanshah Univ Med Sci. 2021;25(2):e113798. https://doi.org/10.5812/jkums.113798.

Abstract

Context:

Lower respiratory tract infections (LRTIs) are prevalent diseases and a major cause of referral to primary healthcare centers. The present study aimed to identify the bacterial etiology of LRTIs to determine the trend changes within the past three decades and help ascertain the new scenarios of empirical LRTI therapy in Turkey.

Methods:

This systematic review was conducted by searching various electronic databases based on specified criteria. In total, 2,670 articles were identified, which had been published during 1990 - 2020 and could be potentially used, and 46 scientific studies that met the eligibility criteria were selected for the review.

Results:

The most frequently isolated bacteria in the reviewed studies were Acinetobacter spp. (31.68%), P. aeruginosa (16.59%), H. influenzae (14.30%), and S. pneumoniae (13.80%). Data analysis also indicated that the most frequent reports of LRTI agents were in Aegean region in Turkey during 2014-2020.

Conclusions:

This systematic review reflected the changes in LRTI agents over the past three decades in Turkey. Knowledge of the frequency of LRTI bacterial agents specific to each country could help healthcare professionals in reporting laboratory results and prescribing/selecting the most effective antibiotics for the treatment of the disease.

1. Context

Lower respiratory tract infections (LRTIs) are prevalent diseases and a major cause of referral to primary healthcare centers. Antibiotics are mostly prescribed for the treatment of these disorders as bacterial pathogens are considered to be the most common etiological factors that induce LRTIs (1, 2).

The diagnosis and treatment of LRTIs require a multidisciplinary approach that integrates current clinical, microbiological, and immunological data. Such an approach is essential due to the large number of the etiological factors that cause these infections, the unfavorable symptoms caused by particular pathogens, the increasing number of antibiotic-resistant bacteria, and limited microbiological diagnostic capabilities (3). Physicians may not routinely opt for etiologic diagnoses and prefer a therapeutic approach based on the distribution of pathogens and previous epidemiological findings (4).

The early and accurate identification of etiological agents is the most effective approach to avoiding inappropriate antibiotic use (5). The first-line treatment for LRTIs should be planned in accordance with national recommendations on appropriate antibiotics, as well as the spectrum of the common pathogens and resistance patterns in a specific region (6).

2. Objective

The present study aimed to identify the bacterial etiology of LRTIs, determine the trend of changes within the past three decades, and help ascertain the new empirical LRTI therapy scenarios in Turkey.

3. Methods

This systematic review was conducted in four phases of data sources and keywords, qualitative analysis of studies, determination of eligibility criteria, and data analysis.

3.1. Data Sources and Keywords

A systematic review was performed via searching in databases such as PubMed, Turkish Medline, Scopus, EBSCO, Google Scholar, and other indexed journals using keywords such as lower respiratory tract infections, lower respiratory tract infections in Turkey, respiratory tract infections in Turkey, and alt solunum yolu enfeksiyonları Türkiye.

3.2. Eligibility Criteria

The eligibility criteria of the articles were the scientific studies conducted in Turkish or English language, studies performed in Turkey, and studies presenting consistent data. The exclusion criteria were unavailable full texts, data on lower respiratory tract infections, data on the infections between upper/lower respiratory tracts without distinction, assessment of fewer than 10 specimens, and lack of detailed description. Based on the screening criteria, 46 studies were selected for our systematic review. Figure 1 depicts the flowchart of the systematic review.

Flowchart of systematic review
Flowchart of systematic review
Figure 1.

Flowchart of systematic review

3.3. Data Analysis

Data were divided into five groups based on the publication year of the selected studies, including 1990 - 1995, 1996 - 2001, 2002 - 2007, 2008 - 2013, and 2014 - 2020. Two independent researchers analyzed the data, and disagreements were resolved unanimously in line with the eligibility criteria. Data were collected on the name of the first author, study area, total number of isolates, methodologies, characteristics of the patient population, and prevalence of LRTI agents. In addition, tables were drawn to demonstrate the prevalence data in terms of numbers, so that the selected studies could be assessed by a common unit.

4. Results

The literature search based on the eligibility criteria resulted in 2,670 articles, which had been published during 1990 - 2020 and could be potentially used, and 46 scientific studies meeting the eligibility criteria were selected for the final review (Table 1). Frequencies were determined by the analysis of the data on LRTI agents reported in different studies.

Table 1.

Data of Reviewed Studies

AuthorYearCityNBacterial SpeciesComorbiditiesClinics
Kurt et al. (7)1990Ankara16H. influenzae, S. pneumoniae1 LA, 6 pneumonia, 5 bronchiectasis, 4 bronchiectasis + COPD -
Saka et al. (8)1994Ankara85S. pneumoniae24 COPD, 3 COPD + 13 DM, COPD + CP, 8 bronchiectasis, 2 APT, 2 IPT, 11 pneumonia, 1 pneumonia + PE, 1 LA, 18 LC, 1 LC + DM, 5 BA, 2 DIF, 1 DL -
Berkiten et al. (9)1994-1997İstanbul291H. influenzae--
Koseoglu et al. (10)1996Ankara24S. pneumoniae, H. influenzae, B. catarrhalis27 COPD, 13 BA, 7 bronchiectasis, 7 CB, 2 LC, 1 emphysema
Ceylan et al. (11)1996İzmir60P. aeruginosa, K. pneumoniae, Enterobacter spp.29 COPD, 25 CAP, 12 HAP
Berkiten et al. (12)1997İstanbul34S. pyogenes-
Yurdakul et al. (13)1997Ankara514S. pneumoniae, P. aeruginosa, S. aureus, K. pneumoniae, M. catarrhalis-ICU
Senol et al. (14)1999İzmir365S. pneumoniae, H. influenzae, M. catarrhalis-ICU, Outpatient
Aydın et al. (15)1999Sivas35S. pneumoniae35 COPD-
Coplu et al. (16)1999Ankara64H. influenzae33 CFOutpatient
Aktepe et al. (17)2000Ankara288H. influenzae, P. aeruginosa, S. aureus288 CF-
Ünel et al. (18)2000İstanbul100H. influenzae, M. catarrhalis, S. pneumoniae, Pseudomonas spp.100 COPD-
Berkiten et al. (19)2001İstanbul102S. pyogenes--
Erdogan et al. (20)2001-2002İstanbul466H. influenzae, H. parainfluenzae, S. pneumoniae, M. catarrhalis, MSSA--
Talay et al. (21)2002İstanbul41S. pneumoniae, K. pneumoniae, P. aeruginosa, E. coli17 COPD, 25 pneumoniainpatient
Ciragil et al. (22)2002İstanbul59P. aeruginosa59 CFICU, inpatient
Azap et al. (23)2002Ankara77S. pneumoniaeCOPD, CAPICU, inpatient, Outpatient
Gonlugur et al. (24)2004Sivas355Klebsiella spp., E. coli, Proteus spp., Enterobacter spp., A. baumannii, Serratia spp.NRIICU, inpatient, Outpatient
Gurol et al. (25)2004İstanbul44S. pneumoniae--
Arikan Akan et al. (26)2005-2007Ankara25A. baumannii, K. pneumoniae-ICU, inpatient,
Atasever et al. (27)2006İzmir837S. aureus, M. catarrhalis, H. influenzae, P. aeruginosa, S. pneumoniae, K. pneumoniae, E. coli, Acinetobacter baumannii, Enterobacter spp.837 LC, 535 pneumonia, 515 COPDICU, inpatient, Outpatient
Komus et al. (28)2006İzmir16P. aeruginosa16 bronchiectasis-
Uncu et al. (29)2007Ankara82S. pneumoniae, H. influenzae--
Demir et al. (30)2007-2010Trabzon78P. aeruginosa-inpatient
Bayram et al. (31)2007-2010Van191A. baumannii-ICU, inpatient
Gazi et al. (32)2008Manisa835Pseudomonas spp., Acinetobacter spp., Klebsiella spp., E. coli, S. maltophilia, Enterobacter spp., S. marcescens-ICU, inpatient
Eksi et al. (33)2008Gaziantep116S. pneumoniae-ICU, inpatient, Outpatient
Kume et al. (34)2008-2010İzmir175Acinetobacter spp., Pseudomonas spp.33 pneumonia, 40 COPD, 12 LCICU,
Akin et al. (35)2009Konya62S. pneumoniae, H. influenzae, M. catarrhalis62 COPD-
Ince et al. (36)2009Duzce98M. catarrhalis, S. pneumoniae, H. influenzae, P. aeruginosa, E. coli98 COPDICU, inpatient, Outpatient
Bacakoglu et al. (37)2009İzmir37A. baumannii8 COPD, 10 CAP, 1, pyopneumothorax, 1 LCICU,
Beşli et al. (38)2012-2014İstanbul586S. pneumoniae, H. influenzae--
Özer et al. (39)2012-2014Hatay1516A. baumannii, P. aeruginosa, K. pneumoniae, E. coli, S. aureus, Enterobacter cloacae, Streptococcus pneumoniae, Stenotrophomonas marcescens-ICU, inpatient,
Akkoyun Bilgi et al. (40)2013İstanbul163H. influenzae, S. pneumoniae, P. aeruginosa-ICU, inpatient, Outpatient
Bayramoglu et al. (41)2014Trabzon67S. pneumoniae, M. catarrhalis, H. influenzae--
Direkel et al. (42)2015Mersin277A. baumanniii
Savcı et al. (43)2015Ankara67A. baumanniii--
Alışkan et al. (44)2016Adana184S. Pneumoniae,H. İnfluenzae--
Eroğlu et al. (45)2016Samsun1183A. baumanniii-ICU, inpatient, Outpatient
Aydemir et al. (46)2016Sakarya130A. baumannii, K. pneumoniae, E. coli, S. aureus, E. cloacae, P. aeruginosa-ICU
Maçin et al. (47)2017Ankara130P. aeruginosa--
Sagmak-Tartar et al. (48)2017Elazığ535A. baumanniii, P. aeruginosa, K. pneumoniae-ICU
Kahraman et al. (49)2017Sakarya71K. pneumoniae--
Altun et al. (50)2018Ankara52S. pneumoniae--
Tanriverdi et al. (51)2019Samsun330H. influenzae, M. catarrhalis, M. catarrhalis, S. Pneumoniae-ICU, inpatient, Outpatient
Altay Koçak et al. (52)2019Adana181A. baumannii, Klebsiella spp., P. aeruginosa, E. coli, H. influenzae, S. aureus, S. pneumoniae-ICU, inpatient

Abbreviations: LA, lung abscess; DM, diabetes mellitus; CP, cor pulmonale; APT, active pulmonary tuberculosis; IPT, inactive pulmonary tuberculosis; PE, pleural effusion; LC, lung cancer; BA, bronchial asthma; DIF, diffuse interstitial fibrosis; DL, destroyed lung; CB, chronic bronchiectasis; CAP, community-acquired pneumonia; HAP, hospital-acquired pneumonia; CF, cystic fibrosis; NRI, nosocomial respiratory infections; ICU, intensive care unit.

According to the findings, the most commonly isolated bacteria were Acinetobacter spp. (31.68%), P. aeruginosa (16.59%), H. influenzae (14.30%), and S. pneumoniae (13.80%). Table 2 shows the frequency of the isolated bacterial species by years. Accordingly, S. pneumoniae was the most common bacterial species isolated during 1990 - 1995, M. catarrhalis was mostly frequently isolated during 1996 - 2001, S. aureus was most commonly isolated during 2002 - 2007 and 2008 - 2013, and A. baumannii was most frequently isolated during 2014 - 2020.

Table 2.

Total Frequencies of Bacterial Isolates by Year (N)

Interval
1990 - 19951996 - 20012002 - 20072008 - 20132014 - 2020
Acinetobacter spp.00818722,024
B. catarrhalis03000
E. coli059814278
Enterobacter spp.04943212
H. influenzae4227298380435
K. pneumoniae025152147318
M. catarrhalis03450560
P. aeruginosa0220270760308
Proteus spp.001000
S. aureus0703153755
S. maltophilia000420
S. pneumoniae112290118288489
Serratia spp.006210
Total1161,1891,4422,7773,719

The findings of the current review indicated significant changes in the reported LTRI data over time, which could be associated with the increased prevalence of A. baumannii infections. Furthermore, a three-fold increase was observed in the data of A. baumannii infections, especially within the past seven years. On the other hand, the reports on P. aeruginosa infections have decreased (Table 2).

Sputum, tracheal aspirate (TA), endotracheal aspiration (ETA), and bronchoalveolar lavage (BAL) have been the most commonly used samples in the diagnosis of LRTI. Table 3 shows the frequency of bacterial isolation and the clinical sample table correlations. In terms of isolation frequency, A. baumannii has been isolated from TA, sputum, BAL, and ETA samples, P. aeruginosa and K. pneumoniae have been isolated from BAL and sputum samples, and S. pneumoniae and H. influenzae have been the most frequently isolated agents from sputum samples.

Table 3.

Total Frequencies of Bacterial Isolates by Sample Type (N)

Sample Type
TASBALDTAETAPFUSBATSPE
A. baumannii1,339536330115319206129030
B. catarrhalis0300000000
E. coli5996780362923000
Enterobacter spp.112310028619000
H. influenzae2566801866018203400
H. parainfluenzae01700000000
K. pneumoniae9521899170121640016
M. catarrhalis11311236001350300
P. aeruginosa200787102948719882000
Proteus spp.01000000000
S. aureus521051332901580000
S. maltophilia00000042000
S. pneumoniae173533170610167067960
S. pyogenes2341000000000
Serratia spp.02700000000
Total2,3003,1811,2443224701,2573491049916

Abbreviations: TA, tracheal aspirate; S, sputum; PF, pleural fluid; BAL, bronchoalveolar lavage; DTA, deep tracheal aspiration; ETA, endotracheal aspiration; BA, bronchial aspiration; TS, throat swab; PE, pleural effusion; US, unspecified.

Table 4 shows the distribution of the isolated infectious agents by geographical regions. Data are scarce on nosocomial LRTI agents in the Black Sea region. Moreover, sufficient data could not be found regarding LRTI agents in the Southeastern Anatolia region. The Aegean region has also been the geographical area with the highest number of notifications on LRTI agents. S. pneumoniae and H. influenzae are community-acquired LRTI agents detected in all regions. Furthermore, nosocomial agents such as A. baumannii, P. aeruginosa, K. pneumoniae, and S. aureus have been frequently reported. The overall analysis of data indicated that LRTI agents were most commonly reported in the Aegean region during 2014 - 2020.

Table 4.

Total Frequencies of Bacterial Isolates by Geographical Region in Turkey (N)

MarmaraMediterraneanCentral AnatoliaEastern AnatoliaSoutheastern AnatoliaAegeanBlack Sea
A. baumannii123717611,76403120
B. catarrhalis0030000
E. coli2114118001403
Enterobacter spp.18161000980
H. influenzae457161151300265280
K. pneumoniae1301724910101900
M. catarrhalis410240028155
P. aeruginosa1512962861270597101
Proteus spp.00100000
S. aureus387252003150
S. maltophilia00000420
S. pneumoniae2741925065521137130
Serratia spp.09600120
Total1,2531,7761,1762,077212,389569

5. Discussion

The etiological diagnosis of LRTIs, which is a major cause of mortality and morbidity, is essential to the treatment of the disease. The distribution of LRTI etiological agents may vary depending on the geographical region, season, age, ethnicity, and underlying diseases (53). LRTIs have changed during the COVID-19 outbreak, which is currently the most pressing public health concern. Consequently, community-acquired and nosocomial LRTI bacterial agents have been extensively investigated due to the risk of developing secondary infections and the essential differences between the treatment of the viral and bacterial agents that cause LRTIs. Therefore, determining possible LRTI pathogens through large-scale studies is of utmost importance in the planning of empirical treatments (54).

According to the studies evaluated in our systematic review, the most common community-acquired LRTI agents were S. pneumoniae and H. influenzae, while the most common nosocomial LRTI agents were A. baumannii, P. aeruginosa, K. pneumoniae, and S. aureus. Changes in the frequency of LRTI agents may be affected by factors such as the identification method, type of isolation samples, waiting times/conditions of sampling, healthcare professionals collecting the samples from the patients, interpretation of the results, and the principles of the automated devices.

Our observations indicated that researchers' trends are one of the critical factors affecting the distribution and frequency of LRTI pathogens (Table 4). The regional distribution of the studies showed that they were mostly performed in the Aegean region, and limited data were provided on the Southeastern Anatolia, as well as on the nosocomial LRTI pathogens in the Black Sea region. On the other hand, the distribution of these factors may be attributed to the used antibiotics, pathogen resistance, accompanying diseases, diagnostic techniques used in hospitals, and hospitals' development, climate, and sanitation state.

Once the COVID-19 pandemic is over, new discussions may arise regarding LRTI pathogens. It is assumed that the samples used for the detection of pathogens will change drastically. In the reviewed studies, most of the samples to isolate LRTI agents were collected from sputum, TA, pleural effusion, and BAL. However, the lack of rapid, inexpensive, and easily applicable diagnostic methods and/or tools for these samples remains a critical challenge in this regard. Currently, gram-staining is considered to be the only effective option although its value remains controversial (55). Unfortunately, suggestions on rapid conventional and/or automated diagnostic tools were not proposed in the reviewed studies.

A notable finding on this systematic review was that studies regarding LRTI were more abundant during 2010-2020 within the past three decades, which could be attributed to several factors, such as the progress achieved in identification and antimicrobial susceptibility technologies of pathogens.

The main conclusions of the reviewed studies have been summarized below:

- LRTIs are two major causes of global mortality. In addition, hospital-acquired infections are the leading cause of mortality and morbidity in intensive care units (ICUs). The use of broad-spectrum antibiotics leads to the development of more resistant strains. With increased bacterial resistance, appropriate and effective antibiotic treatment may be delayed, which in turn leads to higher sepsis frequency and mortality rates (52).

- Evidently, the resistance rate of gram-negative microorganisms to various antibiotics has increased over the years due to the continuous or long-term use of antibiotics in hospitals. P. aeruginosa is a typical example in this regard, which remains an important pathogen in terms of nosocomial infections, especially in ICUs (52).

- No significant change has been reported in the short-term antimicrobial susceptibility of LRTI agents, and the antibiotics to be used in empirical treatments should be selected meticulously. Additionally, it is essential to evaluate the long-term effectiveness of empirical treatment approaches to plan for the necessary changes (38).

- It is essential to periodically determine the pathogens that cause LRTIs, as well as sensitivity to the antibiotics used in empirical treatment protocols (44).

5.1. Strengths and Limitations

To the best of our knowledge, this is the first study to compile the reports on bacterial LRTI agents. One of the limitations of this systematic review was that we could not review the studies providing data on fewer than 10 patients and did not discriminate between upper respiratory tract infections and LRTIs. In addition, errors are possible due to the differences in the identification methods and the experts who evaluate culture results. Therefore, the generalization of the results should be further discussed.

5.2. Conclusions

Since the disease course of bacterial LRTIs is generally mild, uncomplicated, and similar to non-bacterial LRTIs, physicians should not prescribe antibiotics to the patients without the detection of LRTI agents even if they are bacterial. This systematic review was focused on the reported data on the 30-year frequency of LRTI agents. As the frequency of LRTI bacterial factors is specific to each country, healthcare professionals may be able to report cultures and prescribe/select antibiotics. These findings could contribute to the prevention and reduction of antibiotic resistance, which is a major health issue today. It is recommended that further investigations be conducted on homogeneous samples to discuss the frequency of LRTI agents more generally. Furthermore, periodic evaluations could largely contribute to the current literature and treatment guidelines in this regard.

References

  • 1.

    Loeb M, McGeer A, McArthur M, Peeling RW, Petric M, Simor AE. Surveillance for outbreaks of respiratory tract infections in nursing homes. CMAJ. 2000;162(8):1133-7. [PubMed ID: 10789627]. [PubMed Central ID: PMC1232363].

  • 2.

    NNIS. Intensive care antimicrobial resistance epidemiology (ICARE) surveillance report, data summary from January 1996 through December 1997: A report from the National Nosocomial Infections Surveillance (NNIS) System. Am J Infect Control. 1999;27(3):279-84. [PubMed ID: 10358233]. https://doi.org/10.1053/ic.1999.v27.a98878.

  • 3.

    Couriel J. Assessment of the child with recurrent chest infections. Br Med Bull. 2002;61:115-32. [PubMed ID: 11997302]. https://doi.org/10.1093/bmb/61.1.115.

  • 4.

    Milucky J, Pondo T, Gregory CJ, Iuliano D, Chaves SS, McCracken J, et al. The epidemiology and estimated etiology of pathogens detected from the upper respiratory tract of adults with severe acute respiratory infections in multiple countries, 2014-2015. PLoS One. 2020;15(10). e0240309. [PubMed ID: 33075098]. [PubMed Central ID: PMC7571682]. https://doi.org/10.1371/journal.pone.0240309.

  • 5.

    Lalezari J, Campion K, Keene O, Silagy C. Zanamivir for the treatment of influenza A and B infection in high-risk patients: a pooled analysis of randomized controlled trials. Arch Intern Med. 2001;161(2):212-7. [PubMed ID: 11176734]. https://doi.org/10.1001/archinte.161.2.212.

  • 6.

    Hryniewicz W, Grzesiowski P, Kozielski J. Recommendations for diagnostics and treatment of respiratory tract infections. Warszawa: National Program of Antibiotic Protection; 2008. p. 5-7.

  • 7.

    Kurt B, Kalac N, Alin H. Ceftazidime in the treatment of lower respiratory tract infections. ANKEM Journal. 1990;4:56-61.

  • 8.

    Saka D, Berberoglu Ulubas B, Alpar S. Penicillin resistance in patients with Streptococcus pneumoniae development in sputum culture and response to treatment of susceptibility. Balgam Respiratory Diseases. 2000;11(144-147).

  • 9.

    Berkiten R, Bal C, Gurol DS. In vitro antibiotic susceptibilities of Haemophilus influenzae strains isolated from respiratory tract infections. ANKEM Journal. 1998;12:20-5.

  • 10.

    Koseoglu O, Gunalp A. The incidence and antimicrobial susceptibility of Branhamella catarrhalis isolated from adults with lower respiratory tract infection. Bulletin of Microbiology. 1997;31:315-24.

  • 11.

    Ceylan E, İtil O, Ari G. Factors affecting mortality and morbidity in patients followed in medical intensive care unit. Turkish Thoracic Journal. 2001;2:6-12.

  • 12.

    Berkiten R, Erkan-Krause F. Streptococcus pneumoniae isolates from respiratory tract infections, belonging to years 1987-1996. Klimik Journal. 1999;11:9-12.

  • 13.

    Yurdakul AS, Calisir HC, Atasever M. Antibiotic susceptibilities of bacteria isolated from the respiratory sites. Respiratory Diseases. 2001;12:289-93.

  • 14.

    Senol G, Eris F. Haemophilus influenzae, Moraxella catarrhalis and Streptoccus pneumoniae strains isolated from respiratory infections and their resistance to antibiotics. Turkish Thoracic Journal. 2000;1:46-9.

  • 15.

    Aydin BE, Bakir M, Dokmetas İ. The resistance rate of Streptococcus pneumoniae strains to some antibiotics in our region. Klimik Journal. 1999;12:13-5.

  • 16.

    Coplu N, Aktepe OC, Uluutku S. In-vitro antibiotic susceptibilities of Haemophilus influenzae isolates. ANKEM Journal. 1999;13:87-91.

  • 17.

    Aktepe OC, Ozcelik U, Coplu N. Haemophilus influenzae in cystic fibrosis cases: A lower respiratory tract infection agent. Flora. 2000;5:44-8.

  • 18.

    Unel N, Oltan N, Ak O, Sarac G, Ozer S. Incidence of Moraxella catarrhalis in acute exacerbations of chronic obstructive pulmonary disease. Klimik Journal. 2000;13:51-3.

  • 19.

    Berkiten R, Gurol SD. Respiratory tract isolates of Haemophilus influenzae and their resistance to various antimicrobials. ANKEM Journal. 2001;15:718-23.

  • 20.

    Erdogan H, Ongen B, Oksuz L. Antibiotic resistance and phenotypes of macrolide resistance in Streptococcus pyogenes. ANKEM Journal. 2003;17:85-7.

  • 21.

    Talay F, Cetinkaya E, Gencoglu A, Safak G, Tas I, Altin S, et al. Nonspecific culture and antibiogram results of hospitalized patients because of lower respiratory tract infection and empiric treatment approach. Abant Medical Journal. 2014;3(1):21-6. https://doi.org/10.5505/abantmedj.2014.95867.

  • 22.

    Ciragil P, Soyletir G, Sener B. Susceptibilitiy of Pseudomonas aeruginosa strains isolated from cystic fibrosis and other lower respiratory tract infections against various antibiotics. Journal of Turkish Society of Microbiology. 2002;32:197-202.

  • 23.

    Azap A, Altunsoy A, Memikoglu KO. In-vitro susceptibility of Streptococcus pneumoniae strains isolated from lower respiratory tract infections. Ankara Üniversitesi Tıp Fakültesi Mecmuası. 2004;57(2). https://doi.org/10.1501/Tipfak_0000000104.

  • 24.

    Gonlugur U, Bakici MZ, Akkurt I, Efeoglu T. Antibiotic susceptibility patterns among respiratory isolates of Gram-negative bacilli in a Turkish university hospital. BMC Microbiol. 2004;4:32. [PubMed ID: 15320954]. [PubMed Central ID: PMC515300]. https://doi.org/10.1186/1471-2180-4-32.

  • 25.

    Gurol Y, Bertiken R, Georgopoulos A. The Serotyping of Streptococcus pneumoniae strains isolated from lower respiratory tract infections. ANKEM Journal. 2004;18:213-5.

  • 26.

    Arikan Akan O, Uysal S. In vitro activity of tigecycline against multiple resistant Acinetobacter baumannii and carbapenem resistant Klebsiella pneumoniae isolates. Bulletin of Microbiology. 2008;42:209-21.

  • 27.

    Atasever A, Goksel T, Aysan T. Lower respiratory tract infections in patients with lung cancer. Turkish Thoracic Journal. 2006;7:79-83.

  • 28.

    Komus N, Tertemiz KC, Akkoclu A. Pseudomonas aeruginosa colonisation in bronchiectatic patients and clinical reflections. Tuberculosis and Thorax. 2006;54:355-62.

  • 29.

    Uncu H, Colakoglu S, Turunc T. Short communication: In vitro resistance rates of Streptococcus pneumoniae and Haemophilus influenzae clinical isolates to the antibiotics used in therapy. Bulletin of Microbiology. 2007;41:441-6.

  • 30.

    Demir N, Yazıcı Y, Çınarka H, Yılmaz H, Şengül C, Babalık M. Antibiotic resistance profiles of Pseudomonas aeruginosa strains isolated from patients with acute exacerbation of chronic obstructive pulmonary disease. Turkish Bulletin of Hygiene and Experimental Biology. 2014;71(4):179-86. https://doi.org/10.5505/TurkHijyen.2014.16768.

  • 31.

    Bayram Y, Gultepe B, Bektas A, Parlak M, Guducuoglu H. Evaluation of antibiotic resistance in Acinetobacter baumannii strains isolated from various clinical samples. Klimik Dergisi/Klimik Journal. 2015;26(2):49-53. https://doi.org/10.5152/kd.2013.17.

  • 32.

    Gazi H, Ecemis T, Kurutepe S, Gursev N, Surucuoglu S. Antimicrobial resistance of gram-negative bacteria isolated from lower respiratory tract specimens of hospitalized patients. Klimik Dergisi/Klimik Journal. 2011;24(2):112-5. https://doi.org/10.5152/kd.2011.27.

  • 33.

    Eksi F, Gayyurhan ED, Bayram A. Antimicrobial susceptibility of Staphylococcus aureus strains isolated in Gaziantep University Hospital. ANKEM Journal. 2008;22:203-8.

  • 34.

    Kume G, Demirci M. Antimicrobial susceptibilities of non-fermantative gram-negative bacilli isolated from lower respiratory tracts specimens of intensive care units patients and associated risc factors of lower respiratory tract infections. Medical Faculty Journal. 2012;26:37-44.

  • 35.

    Akin B, Tulek B, Arslan U, Sutcu L, Findik D, Suerdem M. Quantitative detection of Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis on sputum in exacerbations of chronic obstructive pulmonary disease by real-time PCR. Solunum. 2011;13(1):32-40. https://doi.org/10.5505/solunum.2011.88156.

  • 36.

    Ince N, Sirmatel F. Frequency and antibiotic susceptibility of Moraxella catarrhalis isolated from sputum in acute exacerbation of chronic obstructive pulmonary disease. ANKEM Dergisi. 2014;28(2):44-9. https://doi.org/10.5222/ankem.2014.044.

  • 37.

    Bacakoglu F, Korkmaz Ekren P, Tasbakan MS. Multidrug-resistant Acinetobacter baumannii infection in respiratory intensive care unit. Bulletin of Microbiology. 2009;43:575-85.

  • 38.

    Beşli Y, Karatuna O, Akyar I. Evaluation of antimicrobial susceptibility in Streptococcus pneumoniae and Haemophilus influenzae strains isolated from lower respiratory tract samples between 2012 and 2014 according to years and age groups. ANKEM Journal. 2015. https://doi.org/10.5222/ankem.2015.0114.

  • 39.

    Özer B, Babayiğit C, Çolak S, Önlen C, Çimen F, Boyacıgil İ, et al. Microorganisms isolated from lower respiratory tract specimens and their antimicrobial resistance. Mustafa Kemal Üniversitesi Tıp Dergisi. 2016;7(27). https://doi.org/10.17944/mkutfd.42522.

  • 40.

    Akkoyun Bilgi E, Gonullu N, Kucukbasmaci O, Altinkum S, Mamal Torun M, Kiraz N. Antibiotic resistance of bacteria isolated from upper and lower respiratory tract infections of children. J Acad Res Med. 2014;3(3):103-7. https://doi.org/10.5152/jarem.2013.1590.

  • 41.

    Bayramoglu G, Koksal I. Spiramycin sensitivity in respiratory tract pathogens. Nobel Medicus. 2014;10:25-31.

  • 42.

    Direkel S, Uzunoglu E, Keles S, Yapar K. Antibiotic resistance rates of Acinetobacter baumannii strains isolated from various clinical samples in giresun Prof. Dr. Atilla Ilhan Ozdemir State Hospital. Gazi Medical Journal. 2015;26(3). https://doi.org/10.12996/gmj.2015.29.

  • 43.

    Savcı Ü, Özveren G, Yenişehirli G, Bulut Y, Özdaş S. In-vitro susceptibility of Acinetobacter baumannii strains isolated from clinical specimens. Turkish Journal of Clinics and Laboratory. 2015;6(1). https://doi.org/10.18663/tjcl.42209.

  • 44.

    Alışkan HE, Çolakoğlu Ş, Göçmen JS. Antibiotic resistance of streptococcus pneumoniae and haemophilus influenzae isolated from respiratory tract specimens. Cukurova Medical Journal. 2016;41(2). https://doi.org/10.17826/cutf.196127.

  • 45.

    Eroğlu C, Ünal N, Karadağ A, Yılmaz H, Acuner İÇ, Günaydın M. Acinetobacter species isolated from various clinical specimens between 2006-2011 years and their susceptibilities against antibiotics. Turkish Bulletin of Hygiene and Experimental Biology. 2016;73(1):25-32. https://doi.org/10.5505/TurkHijyen.2016.68915.

  • 46.

    Aydemir O, Demiray T, Koroglu M. Microbiological evaluation of the pathogens isolated from the endotracheal aspirate samples of the patients followed in the Intensive care units. Online Turkish Journal of Health Sciences. 2016;1:1-8.

  • 47.

    Maçin S, Akdoğan Kıttana FN, Yılmaz YA. Investigation of virulence factors of pseudomonas aeruginosa strains isolated from various clinical samples. Cukurova Medical Journal (Çukurova Üniversitesi Tıp Fakültesi Dergisi). 2017;42(2):308. https://doi.org/10.17826/cutf.322935.

  • 48.

    Sagmak-Tartar A, Ozer AB, Ulu R, Akbulut A. Microbiological evaluation of the pathogens isolated from the endotracheal aspirate samples of the patients followed in the intensive care units: A one-year retrospective analysis. Klimik Dergisi/Klimik Journal. 2018:56-60. https://doi.org/10.5152/kd.2018.14.

  • 49.

    Kahraman EP, Karakeçe E, Erdoğan F, Uluyurt H, Köroğlu M, Çiftci İH. The evaluation of antibiotic resistance status of Klebsiella pneumoniae. Ortadoğu Tıp Dergisi. 2017;9(1):12-8. https://doi.org/10.21601/ortadogutipdergisi.291133.

  • 50.

    Altun B, Sancak B, Gür D. Serotype distribution and antibiotic susceptibility patterns of respiratory isolates of Streptococcus pneumoniae from Hacettepe University Adult Hospital. Türk Mikrobiyoloji Cemiyeti Dergisi. 2018. https://doi.org/10.5222/tmcd.2018.228.

  • 51.

    Tanriverdi Y, Avan T, Bilgin K, Birinci A. Evaluation of antibiotic susceptibility of Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis isolated from lower respiratory tract specimens. Turk J Clin Lab. 2019;10:277-82.

  • 52.

    Altay Koçak A, Yayla B, Üsküdar Güçlü A, Mirza HC, Hortaç İştar E, Alışkan HE, et al. Evaluation of respiratory pathogens isolated in a university hospital in adana and their antibiotic resistance profiles. Turk Mikrobiyol Cemiy Derg. 2019. https://doi.org/10.5222/tmcd.2019.226.

  • 53.

    Sonoda S, Gotoh Y, Bann F, Nakayama T. Acute lower respiratory infections in hospitalized children over a 6 year period in Tokyo. Pediatr Int. 1999;41(5):519-24. [PubMed ID: 10530065]. [PubMed Central ID: PMC7167942].

  • 54.

    Woodhead M, Blasi F, Ewig S, Huchon G, Ieven M, Ortqvist A, et al. Guidelines for the management of adult lower respiratory tract infections. Eur Respir J. 2005;26(6):1138-80. [PubMed ID: 16319346]. https://doi.org/10.1183/09031936.05.00055705.

  • 55.

    Erturan S. Diagnosis of lower respiratory tract infections. Respiratory Tract Infections Symposium. 21 January; Istanbul. IU Cerrahpasa Faculty of Medicine Continuous Medical Education Activities; 2000. p. 141-6.