Occurrence of alert pathogens in patients hospitalised in the department of lung diseases

Michał Zieliński1, Szymon Dworniczak2, Anna Dworniczak2, Jerzy Kozielski1

1School of Medicine with the Division of Dentistry in Zabrze, Department of Lung Diseases and Tuberculosis, Medical University of Silesia in Katowice, Poland

2NZOZ ATOMED Chorzów, Poland

 

 

Occurrence of alert pathogens in patients hospitalised in the department of lung diseases

Występowanie patogenów alarmowych u chorych hospitalizowanych na oddziale chorób płuc

The authors declare no finacial disclosure

 

 

ABSTRACT

Introduction: Infections caused by multiple drug-resistant pathogens represent an increasingly often encountered challenge in clinical practice. The problem particularly applies to patients with chronic lung diseases resulting in multiple hospitalisations. The aim of this paper was to analyse the incidence of alert pathogens isolated from patients hospitalised in the department of lung diseases, who were divided into three groups: patients qualified for lung transplantation, patients treated for neoplastic diseases and patients with chronic lung diseases.

Materials and methods: Analysis involved microbiological test results of 3950 samples obtained from 3521 patients divided into: 200 patients being qualified for lung transplantation, 1292 patients treated for neoplastic diseases and 2029 patients with chronic lung diseases.

Results: Infection with alert pathogen was found in 155 of 3521 patients (4.4%). Most often isolated infectious agent was P. aeruginosa, which accounted for 27% of infections. Other pathogens were as follows A. baumanii ESBL(−) (13%), S. pneumoniae (12%), E. cloacae ESBL(+) (10%), K. pneumoniae ESBL(+) (10%), S. aureus MRSA (8%), E. faecalis (7%), E. coli ESBL(+) (6%), S. maltophilia ESBL(+) (5%) and E. kobei ESBL(+) (2%). Alert pathogens were found in 31 (15%) of 200 patients being qualified for lung transplantation, 89 (4.4%) of 2029 patients with chronic lung diseases and 35 (2.7%) of 1292 patients treated for neoplastic diseases. Difference between infection frequency in patients being qualified for lung transplantation and the remaining groups was statistically significant (p < 0.01). P. aeruginosa infection was the most frequent in all groups. It constituted 35% in patients being qualified for lung transplantation, 29% in patients treated for neoplastic diseases and 22% in patients with chronic lung diseases.

Conclusions: Infections caused by alert pathogens were found in more than 4% of patients hospitalised in the department of lung diseases between 2007 and 2011. Their frequency was significantly higher in patients being qualified for lung transplantation than in other analysed groups. In all examined groups the most frequently isolated bacteria was P. aeruginosa (27% of all isolates).

Key words: alert pathogens, lung diseases, antibiotic resistance, lung transplantation, lung cancer

Pneumonol Alergol Pol 2015; 83: 101–108

 

STRESZCZENIE

Wstęp: Zakażenia spowodowane przez patogeny wielolekooporne stają się coraz częściej wyzwaniem terapeutycznym dla klinicystów. Problem ten dotyczy również pacjentów z przewlekłymi chorobami płuc wymagających wielokrotnych hospitalizacji. Celem pracy była analiza częstości występowania patogenów alarmowych wyizolowanych od chorych oddziału chorób płuc, w podziale na trzy grupy: kwalifikowanych do przeszczepienia płuca, leczonych z powodu choroby nowotworowej oraz leczonych z powodu przewlekłych chorób płuc.

Materiał i metody: Analiza dotyczyła wyników badań mikrobiologicznych 3950 materiałów pochodzących od 3521 chorych: w tym 200 chorych — kwalifikowanych do przeszczepienia płuca, 1292 — leczonych z powodu choroby nowotworowej i 2029 — leczonych z powodu przewlekłej choroby płuc.

Wyniki: Zakażenia patogenem alarmowym stwierdzono u 155 spośród 3521 chorych (4.4%). Najczęściej izolowanym czynnikiem infekcyjnym był P. aeruginosa, który stanowił 27% wszystkich zakażeń, kolejno to A. Baumanii ESBL(−) (13%), S. pneumoniae (12%), E. cloacae ESBL(+) (10%), K. pneumoniae ESBL(+) (10%), S. aureus MRSA (8%), E. faecalis (7%), E. coli ESBL(+) (6%), S. maltophilia ESBL(+) (5%) i E. kobei ESBL(+) (2%). Patogeny alarmowe stwierdzono u 31 (15%) spośród 200 chorych kwalifikowanych do przeszczepienia płuc, 89 (4,4%) spośród 2029 chorych na przewlekłe choroby płuc i 35 (2.7%) spośród 1292 chorych leczonych z powodu choroby nowotworowej. Różnica pomiędzy częstością zakażeń w grupie chorych kwalifikowanych do przeszczepienia a pozostałymi grupami chorych była istotna statystycznie (p < 0.01). We wszystkich grupach chorych dominowało zakażenia P. aeruginosa. Stanowiło ono: w grupie chorych kwalifikowanych do przeszczepienia — 35%, w grupie chorych leczonych z powodu nowotworu — 29%, w grupie chorych z przewlekłą chorobą płuc — 22%.

Wnioski: Zakażenie bakteriami alarmowymi dotyczyło ponad 4% chorych hospitalizowanych na oddziale chorób płuc w latach 2007−2011. Występowało ono istotnie częściej u chorych kwalifikowanych do przeszczepienia płuc niż w pozostałych dwóch grupach analizowanych chorych. We wszystkich grupach najczęściej izolowaną bakterią alarmową była pałeczka ropy błękitnej (27% wszystkich zakażeń).

Słowa kluczowe: patogeny alarmowe, choroby płuc, antybiotykooporność, przeszczepienie płuca, rak płuca

Pneumonol Alergol Pol 2015; 83: 101–108

 

Introduction

Infections caused by drug-resistant bacterial strains constitute a significant problem in patients hospitalised in the pulmonology departments. The necessity of frequent use of antibiotics and chemotherapeutic drugs in this group of patients increases resistance of microorganisms to the used drugs and consequently, leads to the appearance of multidrug-resistant strains [1−3]. Furthermore, it should be emphasised that there are more and more people with reduced resistance, who are exposed to infectious complications. It is related to an increased number of older patients with chronic diseases, who undergo lung transplantation and cytostatic treatment [4, 5]. Drug resistance of bacterial strains contributes to limited therapeutic possibilities, prolonged hospitalisations and consequently, a higher probability of failure of the applied treatment [5–8], and a considerable increase in hospitalisation costs [8, 9]. Supervisory programmes that control infections with alert pathogens focus on rapid methods of pathogens identification, implementation of correct procedures for the patient isolation and preparation of specialised therapeutic algorithms [5, 7, 10].

The aim of the study was to analyse the prevalence of alert pathogens isolated from patients of the department of lung diseases divided into three groups: patients qualified for lung transplantation, patients treated for neoplastic diseases and patients treated for chronic lung diseases.

 

Material and methods

3950 clinical specimens were analysed (85% sputum, 3% urine, 2% blood) from 3521 patients of the pulmonology department, the Third Independent Public Teaching Hospital in Zabrze-Biskupice, hospitalised between 2007−2011.

Basing on clinical characteristics, patients were divided into three groups:

— patients qualified for lung transplantation,

— patients treated for neoplastic lung diseases,

— patients treated for chronic lung diseases.

Microbiological diagnosis was conducted basing on applicable standards, collected material was cultured on proper solid or liquid media with their consecutive identification in semi-automatic system manufactured by BioMerieux Polska-Vitek; tests for drug resistance and identification of resistance mechanisms were carried out basing on standards defined in the guidelines of the European Committee on Antimicrobial Susceptibility Testing (EUCAST).

200 specimens from the patients qualified for lung transplantation (5.7% of all specimens), 1292 specimens from patients with neoplasms (36.7% of all specimens) and 2029 from patients with chronic lung diseases (57.6% of all specimens).

The obtained data were analysed statistically. The significance of proportion differences was examined using z test. Significance of differences between the results was assumed at p < 0.05.

 

Results

During the analysed 5-year period 155 drug-resistant bacterial strains were isolated. In all groups of patients, most frequently isolated pathogen was P. aeruginosa, which accounted for 27% of all infections. Other pathogens in accordance with their prevalence were as follows: A. baumanii ESBL(−) (13%), S. pneumoniae (12%), E. cloacae ESBL(+) (10%), K. pneumoniae ESBL(+) (10%), S. aureus MRSA (8%), E. faecalis (7%), E. coli ESBL(+) (6%), S. maltophilia ESBL(+) (5%) and E. kobei ESBL(+) (2%). The results of analysis of the prevalence of particular strains during a 5-year period were presented in Figure 1.

 

Rycina 1. Frequency of the particular bacterial strain isolates in the 5-year period (2007−2012)

 

Patients qualified for lung transplantation

In this group, the results of microbiological tests of 200 patients were analysed. Infection with resistant pathogen was diagnosed in 31 subjects (15.5%). 6 strains were identified: P. aeruginosa, A. baumanii ESBL(−), E. cloacae ESBL(+), K. pneumoniae ESBL(+), S. aureus MRSA and E. kobei ESBL(+). Among the isolated strains, most frequently were found: P. aeruginosa (35.5%), then Gram (−) bacilli: A. baumanii ESBL(−) — the strain that does not produce beta lactamases, with a wide substrate spectrum (29% of all isolates), the third pathogen was methicillin-resistant Staphylococcus aureus (MRSA), which made up over 16% of all isolated bacteria in the group (Table 1). The proportion of fermenting bacilli from the Enterobacteriacae did not exceed 20%, and most frequently isolated was K. pneumoniae ESBL(+), which constituted nearly 10% of all isolates in the group.

 

Table 1. Patients qualified for lung transplantation (n = 200 SPECIMENS)

The name of the strain

2007

n = 55

2008

n = 49

2009

n = 37

2010

n = 30

2011

n = 29

Total

(percentage)

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

Pseudomonas aeruginosa

1

4.30%

3

12.50

3

7.14

2

5.40

2

6.89

11

35.48

Acinetobacter baumanii ESBL(–)

4

17.40%

2

8.30

1

2.38

1

2.7

1

3.44

9

29

Streptococcus pneumoniae

Enterobacter cloacae ESBL(+)

1

4.20

1

2.70

2

6.45

Klebsiella pneumoniae ESBL(+)

1

4.20

2

4.76

3

9.68

Staphylococcus aureus MRSA

1

4.20

1

2.38

2

5.40

1

3.44

5

16.13

Enterococcus faecalis

Escherichia coli ESBL(+)

Stenotrophomonas maltophilia ESBL(+)

Enterobacter kobei ESBL(+)

1

3.44

1

3.23

Entrobacter aerogenes ESBL(+)

 

Patients treated for lung neoplasms

In the group of 1292 patients treated for lung neoplasms, 35 alert pathogens were isolated (2.7%). Except for bacteria mentioned in the previous group of patients, there were also resistant strains of E. coli ESBL(+) and Gram (+) cocci, i.e. E. faecalis and S. pneumoniae (Table 2). Similarly as in the first analysed group, the most frequent pathogen was P. aeruginosa, which was isolated from 28.6% of specimens. The proportion of fermenting bacilli from the Enterobacteriacae family was distinctly larger and it exceeded 31%, the most often isolated was Enterobacter cloacae ESBL(+), which constituted 14% of all isolates in the group. It should be emphasised that the proportion of Gram (+) cocci, including the proportion of pneumococci — S. pneumoniae, which is sensitive to penicillins, was clearly higher, compared to the previous group (1/3 of all isolated bacteria) and accounted for 14%. The proportion of MRSA was lower (8.5%).

 

Table 2. Patients treated for lung neoplasm (n = 1292 SPECIMENS)

The name of the strain

2007

n = 225

2008

n = 267

2009

n = 288

2010

n = 253

2011

n = 259

Total

(percentage)

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

Pseudomonas aeruginosa

2

8.70

4

16.60

2

4.76

2

5.40

10

28.6

Acinetobacter baumanii ESBL(−)

2

8.70

1

4.20

3

8.57

Streptococcus pneumoniae

1

4.30

1

4.20

1

2.38

1

2.70

1

3.44

5

14.29

Enterobacter cloacae ESBL(+)

1

4.20

1

2.38

3

8.10

5

14.29

Klebsiella pneumoniae ESBL(+)

2

8.30

1

2.38

1

3.44

4

11.43

Staphylococcus aureus MRSA

1

4.30

1

2.70

1

3.44

3

8.57

Enterococcus faecalis

1

4.30

1

2.70

1

3.44

3

8.57

Escherichia coli ESBL(+)

1

4.30

1

2.38

2

5.71

Stenotrophomonas maltophilia ESBL(+)

Enterobacter kobei ESBL(+)

Entrobacter aerogenes ESBL(+)

 

Patients treated for chronic diseases of the respiratory system

In the group of patients treated for chronic diseases of the respiratory system, in 89 (4.4%) subjects out of 2029 hospitalised patients, at least one alert pathogen was isolated. In this group of patients, diverse species of isolated pathogens were found, with dominant P. aeruginosa, which was an aetiological factor of more than every fifth infection (22.5%), and S. pneumoniae, which is sensitive to penicillins (14.6%) (Table 3). The prevalence of the remaining pathogens in the group was well-balanced. A lower proportion of MRSA (5.6%), compared to the two previous groups was observed.

 

Table 3. Patients treated for chronic lung diseases (n = 2029 SPECIMENS)

The name of the strain

2007

n = 403

2008

n = 369

2009

n = 410

2010

n = 428

2011

n = 419

Total

(percentage)

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

No of infected patients

%

Pseudomonas aeruginosa

3

13.04

1

4.20

9

21.42

6

16.21

1

3.44

20

22.5

Acinetobacter baumanii ESBL(−)

3

13.04

3

12.50

1

2.38

1

3.44

8

8.99

Streptococcus pneumoniae

5

11.90

5

13.50

3

10.39

13

14.61

Enterobacter cloacae ESBL(+)

2

8.70

1

4.20

3

7.14

3

8.10

9

10.11

Klebsiella pneumoniae ESBL(+)

2

8.70

2

4.76

1

2.70

3

10.39

8

8.99

Staphylococcus aureus MRSA

1

2.38

2

5.40

2

6.89

5

5.62

Enterococcus faecalis

2

4.76

2

5.40

3

10.39

7

7.87

Escherichia coli ESBL(+)

1

4.20

3

7.14

3

8.10

1

3.44

8

8.99

Stenotrophomonas maltophilia ESBL(+)

3

7.14

1

2.70

4

13.79

8

8.99

Enterobacter kobei ESBL(+)

2

6.89

2

2.25

Entrobacter aerogenes ESBL(+)

1

4.20

1

1.12

 

In the analysed groups, resistant strains were isolated significantly more often in patients qualified for transplantation (p < 0.01), compared to the remaining subjects. The group of patients with neoplasms and the group with chronic diseases of the respiratory system did not differ significantly in respect of proportions of patients infected with alert microorganisms.

 

Discussion

Alert pathogens made up a significant proportion of bacteria isolated from biological material of patients of the department of lung diseases. Among the isolated pathogens, P. aeruginosa prevailed. Currently, this pathogen is becoming the most frequent cause of infections worldwide, it is also changing into more and more resistant to the drugs such as quinolones, carbapenems and aminiglycosides [1]. P. aeruginosa is an aetiological factor of exacerbations of chronic lung diseases causing progressive impairment of functioning of the respiratory system expressed in lowered forced expiratory volume in 1 second (FEV1) [11, 12]. Among patients with lowered immunity after lung transplantation, this pathogen is an aetiological factor of pneumonia, contributing to higher mortality in the early post-transplant period and at long-term follow-up. According to the authors who conducted the studies in Spain, approximately 24% of pneumonia cases after lung transplantation is caused by this pathogen [13−16]. Moreover, P. aeruginosa is frequently isolated in patients with neutropenic fever in the course of lung cancer chemotherapy [17, 18].

The consecutive, in respect of frequency, pathogen isolated among patients qualified for lung transplantation was A. baumanii, which occurred comparably as often as P. aeruginosa (29% and 35% of infections respectively). The results of the published studies have shown that the colonisation of the airways with A. baumanii, and infection with this pathogen in the post-transplant period, constitute a risk factor of prolonged pneumonia in the group of patients after lung transplantation, and consequently, lead to pulmonary fibrosis with compensatory hyperinflation of a native lung [19, 20]. The recent studies have clearly shown that A. baumanii play a crucial role in the increase in mortality among patients infected with this pathogen [4].

In the presented material, in the group of patients with chronic diseases of the respiratory system and patients with neoplasms, infection with A. baumanii occurred more rarely than infection with S. pneumoniae: 8.57% and 14.29%, and 8.99% and 14.61% respectively. These results correspond with the researches carried out by other authors [11, 18, 21].

Infection with S. pneumoniae was not found in the group of patients qualified for lung transplantation. Presumably, it is related to relatively lower resistance of the species to antibiotics [5, 10]. Gram (+) cocci — E. faecalis were not found in this group of patients either [18].

Among the analysed pathogens, the Enterobacteriaceae were represented by: E. cloacae ESBL(+), K. pneumoniae ESBL(+), E. kobei ESBL(+) and E. coli ESBL(+) present in the material in the largest numbers in the group of patients with lung neoplastic diseases and in patients with chronic pulmonary pathology (31% and 30% respectively). Resistance of Enterobacteriaceae to antibiotics is a significant risk factor of prolonged hospitalisation [22]. In the analysed material, in patients qualified for lung transplantation, infections with pathogens from the Enterobacteriaceae family constituted 19%. According to the literature, K. pneumoniae is a pathogen that frequently constitutes an infectious agent in the early post-transplant period [23].

According to the agency of the federal government of the United States — Centers for Disease Control and Prevention — methicillin-resistant S. aureus is becoming more and more frequently recognised infectious agent and the cause of deaths. In the United States, infections with MRSA cause more deaths than tuberculosis and AIDS combined [1]. Next to P. aeruginosa, MRSA is the most frequent factor of pneumonia and bronchitis among patients who underwent immunosuppression due to lung transplantation [16, 24], which is in accordance with the results of the present study.

The last analysed pathogen was S. maltophilia ESBL(+). This non-fermenting Gram-negative bacillus is phylogenetically close to P. aeruginosa and it often colonises the airways of the patients with chronic lung diseases, in immunosuppression or treated for neoplasms. COPD patients and the persons who repeatedly undergo therapy with antibiotics, are at risk of colonisation with this bacterium. Its presence is associated with prolonged hospitalisation and increased patients’ mortality and longer time of mechanical ventilation [6, 25].

To sum up, alert pathogens constitute a vital problem in the group of patients of the department of lung diseases. According to our data, the group most exposed to infections with these bacteria are patients qualified for lung transplantation. For infections influence long-term prognosis, their efficient therapy is crucial in all groups of patients. It should be emphasised that in the analysed material, there were no pathogens of most dangerous resistance mechanisms, i.e. K. pneumoniae KPC (+) producing beta lactamases active to carbapenems, Pseudomonas and Acinetobacter MBL(+) strains producing metallo beta lactamases or OXA-48 (+) producing oxacillinases that hydrolise carbapenems or vancomycin-resistant Enterococcus strains (VRE) or penicillin-resistant pneumococci.

 

Conclusions

Infection with alert pathogens affected 4% of patients hospitalised in the department of lung diseases. It occurred significantly more often in patients qualified for lung transplantation, compared to the remaining subjects. The pathogen that occurred in all study groups was P. aeruginosa (27% of all infections).

 

Acknowledgements

the late Danuta Frankiewicz

The authors thank to for her assistance in collecting the material.

 

Conflict of interest

The authors declare no conflict of interest.

 

Address for correspondence: dr hab. n. med. Michał Zieliński, Katedra i Klinika Chorób Płuc i Gruźlicy SUM, ul. Ks. Koziołka 1, 41–803 Zabrze Biskupice, Poland, tel.: +48 32 373 22 35, e-mail: michal.zielinski1@interia.pl

 

DOI: 10.5603/PiAP.2015.0017

Received: 25.04.2014

 

References:

  1. Boucher HW, Talbot GH, Bradley JS. et al. Bad bugs, no drugs: no ESKAPE! An Update from the Infectious Diseases Society of America. Clin Infect Dis 2009; 48: 1–12.

  2. Urban C, Segal-Maurer S, Rahal JJ. Considerations in control and treatment of nosocomial infections due to multidrug resistant acinetobacter baumannii. Clin Infect Dis 2003; 36: 1268–1274.

  3. Jiun-Nong L, Yen-Hsu Ch, Lin-Li Ch, Chung-Hsu L, Hsing-Lin L, Hsi-Hsun L. Clinical characteristics and outcomes of patients with extended-spectrum b-lactamase-producing bacteremias in the emergency department. Intern Emerg Med. 2011; 6: 547–555.

  4. Falagas ME, Rafailidis PI. Attributable mortality of Acinetobacter baumannii: no longer a controversial issue. Crit Care 2007; 11: 134−136.

  5. Niederman MS. Use of broad-spectrum antimicrobials for the treatment of pneumonia in seriously ill patients: Maximizing Clinical Outcomes and Minimizing Selection of Resistant Organisms. Clin Infect Dis 2006; 42 (Suppl. 2) S72–S81.

  6. Saad Nseir, Di Pompeo C, Brisson H. et al. Intensive care unit-acquired Stenotrophomonas maltophilia: incidence, risk factors, and outcome. Crit Care 2006; 10: R143−151.

  7. Sacha P, Jaworowska J, Ojdana D, Wieczorek P, Czaban S, Tryniszewska E. Occurrence of the aacA4gene among multidrug resistant strains of Pseudomonas aeruginosa isolated from bronchial secretions obtained from the Intensive Therapy Unit at University Hospital in Bialystok, Poland. Folia Histochem Cytobiol 2012; 50: 322–324.

  8. Evanset HL, Lefrac SN, Lyman J. et al. Cost of gram-negative resistance. Crit Care Med 2007; 35: 89−95.

  9. Niederman MS. Impact of antibiotic resistance on clinical outcomes and the cost of care. Crit Care Med 2001; 29 (Suppl. 4) N114-N120.

  10. De Pascale G, Bello G, Tumbarello M, Antonelli M. Severe pneumonia in intensive care: cause, diagnosis, treatment and management: a review of the literature. Curr Opin Pulm Med 2012; 18: 213–221.

  11. Miravittles M, Espinosa C, Fernandez-Laso E. et al. Relationship between bacterial flora in sputum and functional impairment in patients with acute exacerbations of COPD. Chest 1999; 116: 40–46.

  12. Ferrer M, Ioanas M, Arancibia F, Marco MA, de la Bellacasa JP, Torres A. Microbial airway colonization is associated with noninvasive ventilation failure in exacerbation of chronic obstructive pulmonary disease. Crit Care Med 2005; 33: 2003−2009.

  13. Sang Young K, Jung Ar S, Eun Na C. et al. Late respiratory infection after lung transplantation. Tuberc Respir Dis 2013; 74: 63−69.

  14. Zander DS, Baz MA, Visner GA. et al. Analysis of early deaths after isolated lung transplantation. Chest 2001; 120: 225–232.

  15. Domenig C. Continuous Beta-lactam antibiotic therapy in a double-lung transplanted patient with a multidrug resistant Pseudomonas Aeruginosa infection. Transplantation 2001; 71: 744–745.

  16. Aguilar-Guisado M, Givalda J, Ussetti P. et al. Pneumonia after lung transplantation in the resitra cohort: a multicenter prospective study. Am J Transplant 2007; 7: 1989–1996.

  17. Oppenheim BA. The changing pattern of infection in neutropenic patients. J Antimicrob Chemother 1998; 41: 7−11.

  18. Lanoix JP, Pluquet E, Lescure FX. et al. Bacterial infection profiles in lung cancer patients with febrile neutropenia. BMC Infect Dis 2011; 11: 183.

  19. Nunley DR, Bauldoff GS, Mangino JE, Pope-Harman AL. Mortality associated with Acinetobacter baumannii infections experienced by lung transplant rRecipients. Lung 2010; 188: 381–385.

  20. Sopirala MM, Pope-Herman A, Nunley DR. et al. Multidrug-resistant Acinetobacter baumannii pneumonia in lung transplant recipients. J Heart Lung Transplant 2008; 27: 804–807.

  21. Saad Nseir, Di Pompeo C, Cavestri B. 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.

  22. Salgado D, O’Grady N, Farr BM. Prevention and control of antimicrobial-resistant infections in intensive care patients. Crit Care Med 2005; 33: E388−E394.

  23. Raviv Y, Shitrit D, Amital A. et al. Multidrug-resistant Klebsiella pneumoniae acquisition in lung transplant recipients. Clin Transplant 2012: 26: E388–E394.

  24. Maurer JR, Tulliss DE, Grossman RF, Vellend H, Winton TL, Patterson GA. Infectious complications following isolated lung transplantation. Chest 1992; 101: 1056−1059.

  25. Senol E. Stenotrophomonas maltophilia: the significance and role as a nosocomial pathogen. J Hosp Infect 2004, 57: 1−7.

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

Czasopismo Pneumonologia i Alergologia Polska dostęne jest również w Ikamed - księgarnia medyczna

Wydawcą serwisu jest "Via Medica sp. z o.o." sp.k., ul. Świętokrzyska 73, 80–180 Gdańsk

tel.:+48 58 320 94 94, faks:+48 58 320 94 60, e-mail: viamedica@viamedica.pl