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Fatima Zahra Adil Department of Bacteriology, Mohammed V Military Teaching Hospital, Rabat, Morocco
Faculty of Medicine and Pharmacy, Mohammed V University, Rabat, Morocco

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Elmostafa Benaissa Department of Bacteriology, Mohammed V Military Teaching Hospital, Rabat, Morocco
Research Team of Epidemiology and Bacterial Resistance, Faculty of Medicine and Pharmacy, Mohammed V University, Rabat, Morocco

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Yassine Benlahlou Department of Bacteriology, Mohammed V Military Teaching Hospital, Rabat, Morocco
Research Team of Epidemiology and Bacterial Resistance, Faculty of Medicine and Pharmacy, Mohammed V University, Rabat, Morocco

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Hicham Bakkali Department of Anesthesiology and Critical Care, Military Teaching Hospital Mohammed V, Rabat, Morocco

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Nawfal Doghmi Department of Anesthesiology and Critical Care, Military Teaching Hospital Mohammed V, Rabat, Morocco

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Hicham Balkhi Department of Anesthesiology and Critical Care, Military Teaching Hospital Mohammed V, Rabat, Morocco

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Adil Maleb Research Team of Epidemiology and Bacterial Resistance, Faculty of Medicine and Pharmacy, Mohammed V University, Rabat, Morocco
Laboratory of Microbiology, Faculty of Medicine and Pharmacy of Oujda, Mohammed the First University, Oujda, Morocco

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Mostafa Elouennass Department of Bacteriology, Mohammed V Military Teaching Hospital, Rabat, Morocco
Research Team of Epidemiology and Bacterial Resistance, Faculty of Medicine and Pharmacy, Mohammed V University, Rabat, Morocco

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Abstract

Introduction

Bacteremia is responsible for high rates of morbidity and mortality. The increasing prevalence of multidrug-resistant (MDR) bacteria in intensive care units (ICU) is a growing concern. Hence, prior knowledge of bacterial epidemiology and resistance phenotypes is required to optimize these infections' management. The objective of this study was to determine the epidemiological profile of bacteremia in ICU settings, as well as the place occupied by MDR bacteria in these infections.

Methods

It is a prospective study carried out over 10 months on episodes of bacteremia in the ICU of Mohammed V Military Teaching Hospital (Rabat, Morocco). Microorganism growth was detected using fluorescent technology, species identification was based on morphological and biochemical characteristics. Antimicrobial susceptibility testing was performed following the recommendations of the Antibiogram Committee of the French Society of Microbiology (CA-SFM) and the European Committee on Antimicrobial Susceptibility Testing (EUCAST).

Results

Among 504 hospitalized patients, sixty-one (12.1%) presented at least one episode of bacteremia. Forty patients (65.6% of bacteremic patients) presented at least one episode of bacteremia due to MDR bacteria. Male gender, cardiovascular diseases, diabetes and previous hospitalization were significant risk factors for the acquisition of MDR bacteremia. Isolated bacteria were mainly Gram-negative bacilli (GNB) (n = 62; 68.9%) dominated by Acinetobacter baumannii (n = 19; 21.1%) and Klebsiella pneumoniae (n = 16; 17.8%). MDR bacteria were represented by multi-resistant Acinetobacter baumannii (n = 19; 44.2%), extended-spectrum beta-lactamases-producing Enterobacterales (n = 9; 20.9%) and carbapenem-resistant Enterobacterales (n = 7; 16.3%). Carbapenems (n = 40; 65.6%), Aminoglycosides (n = 32; 52.5%) and Polypeptides (n = 24; 39.3%) were the most used antimicrobials. Mortality rates were 66.6% (n = 40) and 85% (n = 43) in patients with non MDR bacteremia and MDR bacteremia respectively.

Conclusion

Limiting the spread of MDR bacteria and improving the management of bacteremic patients require continuous monitoring of bacteremia as well as adapting the therapeutic and preventive strategy.

Abstract

Introduction

Bacteremia is responsible for high rates of morbidity and mortality. The increasing prevalence of multidrug-resistant (MDR) bacteria in intensive care units (ICU) is a growing concern. Hence, prior knowledge of bacterial epidemiology and resistance phenotypes is required to optimize these infections' management. The objective of this study was to determine the epidemiological profile of bacteremia in ICU settings, as well as the place occupied by MDR bacteria in these infections.

Methods

It is a prospective study carried out over 10 months on episodes of bacteremia in the ICU of Mohammed V Military Teaching Hospital (Rabat, Morocco). Microorganism growth was detected using fluorescent technology, species identification was based on morphological and biochemical characteristics. Antimicrobial susceptibility testing was performed following the recommendations of the Antibiogram Committee of the French Society of Microbiology (CA-SFM) and the European Committee on Antimicrobial Susceptibility Testing (EUCAST).

Results

Among 504 hospitalized patients, sixty-one (12.1%) presented at least one episode of bacteremia. Forty patients (65.6% of bacteremic patients) presented at least one episode of bacteremia due to MDR bacteria. Male gender, cardiovascular diseases, diabetes and previous hospitalization were significant risk factors for the acquisition of MDR bacteremia. Isolated bacteria were mainly Gram-negative bacilli (GNB) (n = 62; 68.9%) dominated by Acinetobacter baumannii (n = 19; 21.1%) and Klebsiella pneumoniae (n = 16; 17.8%). MDR bacteria were represented by multi-resistant Acinetobacter baumannii (n = 19; 44.2%), extended-spectrum beta-lactamases-producing Enterobacterales (n = 9; 20.9%) and carbapenem-resistant Enterobacterales (n = 7; 16.3%). Carbapenems (n = 40; 65.6%), Aminoglycosides (n = 32; 52.5%) and Polypeptides (n = 24; 39.3%) were the most used antimicrobials. Mortality rates were 66.6% (n = 40) and 85% (n = 43) in patients with non MDR bacteremia and MDR bacteremia respectively.

Conclusion

Limiting the spread of MDR bacteria and improving the management of bacteremic patients require continuous monitoring of bacteremia as well as adapting the therapeutic and preventive strategy.

Introduction

Bacteremia is the presence of viable bacteria in the circulating blood [1]. It is responsible for organ dysfunctions such as sepsis and septic shock that are associated with high morbidity and mortality [2, 3]. This infection's incidence variates depending on demographic characteristics, risk factors, and the number of blood cultures performed [4]. The frequent use of invasive devices in the intensive care unit (ICU) makes it a high-risk area for bacteremia [5].

Multidrug-resistant (MDR) isolates are defined as microorganisms with acquired resistance to at least one agent in three or more antimicrobial classes. This acquisition can either be endogenous with selection of resistant strains from the patient's own body flora, or exogenous from skin contact mainly hand related [6, 7]. MDR Gram-negative bacilli (GNB) including Extended-Spectrum Beta-Lactamase (ESBL) producing or Carbapenem-Resistant Enterobacterales (CRE) and non-fermenters such as Acinetobacter baumannii, are widely reported as causing bloodstream infections (BSI) in critical care units [3, 7–9]. This is mainly related to the predominance of healthcare-associated bacteremia whose source is usually pulmonary or urinary in ventilated patients or those with urinary catheters. In addition, the massive use of broad-spectrum antimicrobials like third-generation cephalosporins and carbapenems leads to the selection of these microorganisms [9].

The increasing prevalence of MDR bacteria, is a challenge, as treating infected patients becomes difficult with a pejorative prognosis [7]. Therefore, an updated knowledge of bacterial epidemiology and resistance phenotypes is required [8].

In Morocco, studies concerning bacteremia and MDR bacteria are relatively rare despite the high mortality rates related to these infections, which is concerning, especially in the ICU settings. This study aims to determine the epidemiological profile of bacteremia in ICU as well as the role of MDR bacteria in these infections.

Methods

This is a prospective study carried out for over ten months (May 2019 to February 2020), on blood samples and episodes of bacteremia in the medical and surgical intensive care units (10 beds each) of Mohammed V Military Teaching Hospital in Rabat (Morocco). Bacteremia was defined by at least one positive blood culture. Regarding commensal microorganisms such as coagulase-negative Staphylococci (CoNS), at least two different sets of positive blood culture were required, in addition to clinical features and at least one of the following parameters: White blood cells (WBC) > 10,000/mm3, C-reactive protein (CRP) > 5 mg L−1, procalcitonin (PCT) > 0.5 ng mL−1. Excluded were sterile, contaminated blood cultures, as well as duplicates (the same isolates with the same susceptibility profile isolated several times from the same patient for less than five days).

In patients with two or more episodes of bacteremia, an episode was considered new either after identifying a different microorganism or when isolating the same microorganism after more than seven days under appropriate antibiotic therapy.

In the case of multiple ICU stays, we only considered those in which the patients presented an episode of bacteremia. Bacteremia occurring within the first 48 h of admission to the ICU was considered community-acquired, otherwise, it was considered healthcare-associated.

Bacteremia was defined as secondary when the same microorganism was isolated in both blood culture and the first site of infection within a maximum of 17 days. For this purpose, the patient's bacteriological record was taken into consideration, including respiratory, urinary, catheter, skin, and other samples. The source of the infection was considered unknown if no other bacteriological samples were taken, or if the germ isolated in the blood culture was not found elsewhere.

Antibiotic therapy was considered adequate when the isolated bacteria were sensitive in vitro to at least one of the prescribed antibiotics. It was considered probabilistic in the absence of microbiological documentation and documented when an antibiogram was available. Favorable evolution was based on clinical improvement and normalization of the biological parameters.

In case of suspected bacteremia, blood samples were collected, usually in pairs of aerobic/anaerobic bottles (Becton Dickinson Bactec Plus Aerobic medium and Becton Dickinson Bactec Lytic Anaerobic medium, Becton Dickinson, Winnersh Triangle, Wokingham, Berkshire, United Kingdom), and incubated at 37°C in the Becton Dickinson BACTEC 9240 (Becton Dickinson, Winnersh Triangle, Wokingham, Berkshire, United Kingdom) Blood Culture System. We made subcultures in adequate growth medium from each positive bottle. We also performed smears for direct examination and Gram staining, and the results were immediately communicated to initiate or adjust antibiotic therapy. Species identification was based on morphological and biochemical characteristics (API gallery, bio-Mérieux SA, Marcy l'Étoile/France). Antimicrobial susceptibility testing was performed following the recommendations of the Antibiotic susceptibility Committee of the French Society of Microbiology (CA-SFM) and the European Committee on Antimicrobial Susceptibility Testing (EUCAST) [10].

Statistical analysis was performed using the software SPSS v23.0. Categorical variables were compared using the Chi-square test. Quantitative variables were compared using the Mann-Whitney U Test. For all statistical tests, results were considered significant when P < 0.01.

Ethics statement

The agreement of the data exploitation was obtained via consent forms that the patients or their parents signed.

Results

During this study, five hundred and four patients were admitted to the medical and surgical ICU. Sixty-eight episodes of bacteremia were recorded in 61 patients, relating to an incidence of 12.1% of hospitalized patients. Forty-one episodes of bacteremia due to MDR bacteria were recorded in 40 patients, corresponding to 65.5% of bacteremic patients. Table 1 demonstrates a comparison of demographic and clinical data, risk factors, as well as nonspecific biological markers of patients with non MDR and MDR bacteremia.

Table 1.

Comparison of demographic and clinical data, risk factors, and non-specific biological markers of non MDR bacteremic patients and MDR bacteremic patients (MDR: Multi-Drug Resistant, CRP: C-Reactive Protein, PCT: Procalcitonin, WBC: White Blood Cells, NS: Non-Significant)

Non MDR bacteremia MDR bacteremia P value
n = 21 % n = 40 %
Age <20 1 4.8 4 10
20–39 4 19 5 12.5
40–59 5 23.9 14 35
60–79 8 38 14 35
≥80 3 14.3 3 7.5
Median age [minimum – maximum] 56 [18–85] 57 [14–95] NS
Gender Male 17 80.9 31 77.5 P < 0.01
Female 4 19.1 9 22.5
Gender ratio 4.25 3.44
Comorbidities Cardiovascular disease 15 71.4 7 17.5 P < 0.01
Diabetes mellitus 13 62 7 17.5 P < 0.01
Cancer 8 38 9 22.5 NS
Chronic renal failure 7 33.3 6 15 NS
Respiratory disease 1 4.7 2 5 NS
Liver disease 5 23.8 5 12.5 NS
Other 3 14.3 2 5
Mean length of stay ± Standard Deviation 28.1 ± 23.7 16.6 ± 19.5 NS
Risk factors Mechanical ventilation 19 90.4 33 82.5 NS
Urinary catheterization 18 85.7 30 75 NS
Central venous catheterization 15 71.4 31 77.5 NS
Hemodialysis 5 23.8 12 30 NS
Inadequate probabilistic antibiotic therapy 10 47.6 27 67.5 NS
Previous hospitalization (3 months) 2 9.5 21 52.5 P < 0.01
Previous antibiotic therapy (3 months) 2 9.5 17 42.5 NS
Clinical features Fever (≥38 °C) 17 80.9 21 52.5
Sepsis 12 57.1 19 47.5
Septic shock 5 23.8 20 50
Non-specific biological markers CRP > 5 mg L−1 21 100 40 100
PCT > 0.5 ng mL−1 21 100 40 100
WBC > 10,000 mm 3 14 66.6 23 57.5

Fifty-four (88.5%) of bacteremic patients presented a single episode of bacteremia. Sixty-five (95.6%) of bacteremia episodes were healthcare-associated, and fifty-four (79.4%) were monomicrobial. Sources of non MDR bacteremia and MDR bacteremia, when identified, were principally respiratory and urinary tract infections (Table 2). In the 68 episodes of bacteremia included in this study, ninety microorganisms were isolated, among which forty-three (47.7%) were MDR. GNB was predominant (n = 62; 68.9%), Enterobacterales and non-fermenting GNB represented 38.9% (n = 35) and 30% (n = 27) respectively. The most encountered species were Acinetobacter baumannii followed by Klebsiella pneumoniae (Table 2). Antimicrobial resistance rates are shown in Table 3.

Table 2.

Microorganisms responsible of bacteremia and different sources of infection (n = 90) (MDR: Multi-Drug Resistant, UN: Unknown, R: Respiratory tract, U: Urinary tract, CVC: Central venous catheterization)

Family Bacteria Total (%) Non MDR bacteremia (%) Source of infection (%) MDR bacteremia (%) Source of infection (%)
UN R U CVC Other UN R U CVC Other
Enterobacterales (n = 35; 38.9%) Escherichia coli 5 (5.6%) 3 (60%) 1 (33.3%) 0 2 (66.7%) 0 0 2 (40%) 0 0 1 (50%) 0 1 (50%)
Klebsiella pneumoniae 16 (17.8%) 6 (37.5%) 2 (33.3%) 2 (33.3%) 1 (16.7%) 1 (16.7%) 0 10 (62.5%) 4 (40%) 3 (30%) 2 (20%) 0 1 (10%)
Enterobacter cloacae 5 (5.6%) 3 (60%) 1 (33.3%) 0 1 (33.3%) 1 (33.3%) 0 2 (40%) 2 (100%) 0 0 0 0
Enterobacter aerogenes 2 (2.2%) 0 2 (100%) 1 (50%) 1 (50%) 0 0 0
Proteus mirabilis 3 (3.3%) 3 (100%) 2 (66.7%) 0 1 (33.3%) 0 0 0
Serratia liquefaciens 1 (1.1%) 1 (100%) 1 (100%) 0 0 0 0 0
Morganella morganii 1 (1.1%) 1 (100%) 1 (100%) 0 0 0 0 0
Providencia stuartii 1 (1.1%) 1 (100%) 1 (100%) 0 0 0 0 0
Citrobacter freundii 1 (1.1%) 1 (100%) 1 (100%) 0 0 0 0 0
non-fermenting Gram-negative bacilli (n = 27; 30%) Acinetobacter baumannii 19 (21.1%) 0 19 (100%) 11 (57.9%) 7 (36.8%) 0 1 (5.3%) 0
Pseudomonas aeruginosa 8 (8.9%) 5 (62.5%) 1 (20%) 3 (60%) 1 (20%) 0 0 3 (37.5%) 1 (33.3%) 1 (33.3%) 1 (33.3%) 0 0
Staphylococci (n = 9; 10%) Staphylococcus aureus 6 (6.7%) 5 (83.3%) 2 (40%) 2 (40%) 0 1 (20%) 0 1 (16.7%) 1 (100%) 0 0 0 0
Coagulase-negative staphylococci 3 (3.3%) 3 (100%) 3 (100%) 0 0 0 0 0
Streptococci (n = 2; 2.2%) Streptococcus pneumonia 1 (1.1%) 1 (100%) 1 (100%) 0 0 0 0 0
Streptococcus pyogenes 1 (1.1%) 1 (100%) 1 (100%) 0 0 0 0 0
Enterococci (n = 15; 16.7%) Enterococcus faecalis 7 (7.8%) 6 (85.7%) 3 (50%) 0 3 (50%) 0 0 1 (14.3%) 0 0 0 0 1 (100%)
Enerococcus faecium 8 (8.9%) 5 (62.5%) 4 (80%) 0 0 1 (20%) 0 3 (37.5%) 2 0 0 1 0
Yeasts Source of infection
UN P U CVC Other
Candida (n = 2; 2.2%) Candida glabrata 1 (1.1%) 0 0 1 (100%) 0 0
Candida sphaerica 1 (1.1%) 1 (100%) 0 0 0 0
Table 3.

Resistance rates (3GC: Third-generation cephalosporins, FQ: Fluoroquinolones, AMK: Amikacin, IMP: Imipenem, COL: Colistin, TZP: Tazobactam-Piperacillin, FOX: Cefoxitin, LZD: Linezolid, VAN: Vancomycin, TEI: Teicoplanin)

Enterobacterales 3GC FQ AMK IMP
Klebsiella pneumoniae (n = 16) 62% 62% 12% 37%
Escherichia coli (n = 5) 40% 40% 0% 0%
Enterobacter sp. (n = 7) 57% 28% 28% 14%
Non fermenters GNB 3GC FQ AMK IMP COL TZP
Acinetobacter baumannii (n = 19) 100% 100% 79% 100% 0%
Pseudomonas aeruginosa (n = 8) 25% 12% 12% 25% 25%
Staphylococci FOX LZD
Staphylococcus aureus (n = 6) 17% 0%
CoNS (n = 3) 100% 0%
Enterococci LZD VAN TEI
Enterococcus faecalis (n = 7) 0% 14% 14%
Enterococcus faecium (n = 8) 0% 37% 25%

In 41 episodes of MDR bacteremia, forty-three MDR bacteria were isolated. MDR A cinetobacter baumannii, Extended-Spectrum Beta-Lactamase producing Enterobacterales (ESBL-E), and Carbapenem-Resistant Enterobacterales (CRE) were the most frequently isolated MDR bacteria. In MDR Enterobacterales, Klebsiella pneumoniae was predominant (Fig. 1). Regarding MDR rates per species, all A cinetobacter baumannii isolates (n = 19; 100%) were MDR, nine (25.7%) of Enterobacterales isolates were ESBL-E while seven (20%) were CRE, three (37.5%) of Pseudomonas aeruginosa isolates were MDR. In Gram-positive cocci, glycopeptide resistance was observed in four (26.6%) of Enterococcus isolates, while one (16.6%) Staphylococcus aureus was Methicillin-resistant.

Fig. 1.
Fig. 1.

MDR bacteria responsible of bacteremia (n = 43) (ESBL-E: Extended-Spectrum Beta-Lactamase producing Enterobacterales, CRE: Carbapenem-Resistant Enterobacterales, MDR: Multi-Drug Resistant, MRSA: Methicillin-resistant Staphylococcus aureus, GRE: Glycopeptide-resistant Enterococci)

Citation: European Journal of Microbiology and Immunology 12, 2; 10.1556/1886.2022.00010

Antibiotic therapy was documented in 31 (45.6%) episodes of bacteremia, and empiric in 30 (48.5%). Carbapenems (n = 40; 65.6%), Aminoglycosides (n = 32; 52.5%) and Polypeptides (n = 24; 39.3%) were the most used antibiotics. In terms of antibiotic combination, dual therapy was widely used (n = 35; 57.4%) especially the association of Imipenem with Amikacin or Colistin.

Fourteen (66.6%) patients with non MDR bacteremia and 34 (85%) with MDR bacteremia died. Table 4 shows MDR species responsible for mortality.

Table 4.

Mortality rate of MDR bacteremic patients by species (MDR: Multi-Drug Resistant, GNB: Gram Negative Bacilli, GPC: Gram-positive cocci, ESBL-E: Extended-Spectrum Beta-Lactamase producing Enterobacterales, CRE: Carbapenem-Resistant Enterobacterales, MRSA: Methicillin-resistant Staphylococcus aureus, GRE: Glycopeptide-resistant Enterococci)

MDR bacteria n %
GNB MDR Acinetobacter baumannii 14 29 41.2 85.3
ESBL-E 6 17.7
CRE 6 17.7
MDR Pseudomonas aeruginosa 3 8.8
GPC MRSA 3 4 8.8 11.8
GRE 1 3

Discussion

ICU stay is associated with a high risk of infection owing to the patients' critical condition and the use of invasive devices. However, bacteremia rates are widely variable because of inconsistent diagnosis criteria and therapeutic intervention measures, as well as adherence to hand hygiene protocols [11–14].

The incidence of bacteremia in our study was 12.1%, it remains the highest when compared to those of El Kettani et al. (5.1%), Merzougui et al. (11.3%) and Kallel et al. (9.5%) [11, 12, 14]. Our demographic data demonstrates that patients over the age of 55 years are prone to develop bacteremia, in agreement with Lachhab et al. and Tabah et al. [38], this could be explained by the weakening of the immune system in the elderly. Male patients were predominant in our study, the same result was found by Kallel et al. (67,3%) and Lachhab et al. (62%) [8, 14]. It is related to differences in lifestyle, access to health care, sex hormones, and genetic variability between males and females [15]. In addition, according to the analysis of our statistical data, male gender was a significant risk factor for MDR bacteremia.

The comorbidities found in our patients with non MDR bacteremia and MDR bacteremia were mainly diabetes, cardiovascular diseases and cancer, in agreement with other studies [8, 14]. The statistical analysis data showed that cardiovascular disease and diabetes are significant risk factors for MDR bacteremia. In fact, diabetic patients are immunocompromised. On the other hand, cardiovascular diseases may not be directly related to these infections but they are common worldwide, and the age of their occurrence corresponds to the patients' median age in our study.

Furthermore, we showed that patients with MDR bacteremia have a shorter ICU stay compared to patients with non MDR bacteremia, which is in contrast to a study by Kallel et al., who demonstrated longer stay in patients with ESBL-E bacteremia [14]. This may be explained by the early mortality of patients with MDR bacteremia in our case, which is closely related to late initiation of appropriate therapeutic intervention.

Apart from cases where the source of infection remained unknown, respiratory and urinary tracts were predominant in our study for both non MDR bacteremia and MDR bacteremia cases which was also reported by Lachhab et al. [8]. This can be related to the important use of mechanical ventilation and urinary catheters in ICU. However, the major causes of bacteremia reported in a French study were ventilator-associated pneumonia and catheters [14]. The low rate of catheter-related bacteremia would be linked to Coagulase-negative staphylococci (CoNS), often considered as commensal agents, hence, an underestimation of these infections would be possible.

Several studies showed that prior hospitalization and previous or inadequate antibiotic therapy could be considered as risk factors for MDR bacteremia [16–19]. This was also observed in our study. In addition, our statistical data analysis showed that hospitalization in the previous three months is a predisposing factor for MDR bacteremia.

The most frequently isolated bacteria were Gram-negative bacilli (68.9%), as reported in other studies [8, 9, 14]. A cinetobacter  baumannii and K lebsiella pneumoniae were predominant, which reflect the important rates of healthcare-associated bacteremia in our study. The isolated microorganisms were MDR in 47.7% of cases, which agrees with a multicenter study (47.8%) carried out by Tabah et al. [3]. Antibiotic resistance rates were compared with those of two other studies conducted at the same facility as ours (Table 5); Increased rates were observed in GNB especially in third-generation Cephalosporins (3GC), Fluoroquinolones (FQ), Amikacin (AMK) and Imipenem (IMP), which would be the consequence of the bacteria capacity to rapidly accumulate resistance factors, the selection pressure of antibiotics, as well as the difficulty of controlling hygiene conditions.

Table 5.

Comparison of antibiotic resistance rates (MDR: Multi-Drug Resistant, ESBL: Extended-Spectrum Beta-Lactamase, 3GC: Third-generation cephalosporins, FQ: Fluoroquinolones, AMK: Amikacin, IMP: Imipene, TZP: Tazobactam-Piperacillin)

MDR bacteria Antibiotic Elouennass et al. [9] Lachhab et al. [8] Our study
MDR Acinetobacter baumannii 3GC 68.7% 100% 100%
FQ 77.8% 100% 100%
AMK 27% 50% 79%
IMP 31.4% 100% 100%
ESBL producing Klebsiella pneumoniae 3GC 40% 60% 62%
FQ 40% 70% 62%
AMK 0% 0% 12%
Carbapenem-resistant Klebsiella pneumoniae IMP 0% 0% 37%
MDR Pseudomonas aeruginosa TZP 22.2% 20% 25%
3GC 16.6% 20% 25%
FQ 26% 20% 12%
AMK 0% 20% 12%
IMP 10.5% 20% 25%
Glycopeptide-resistant Enterococci Glycopeptides _ 0% 27%
Methicillin-resistant Staphylococcus aureus Methicillin 52.94% 20% 17%

The frequency of use of Imipenem, Amikacin, and Colistin in our study reflects the burden of MDR GNB in invasive infections in the ICU setting. Although prognosis and mortality are largely influenced by the choice of antibiotic therapy, the use of a therapeutic regimen against MDR bacteria is necessary, with all the consequences that it may have, including selection pressure of antibiotics and increased management costs.

Mortality rates in our study exceed those observed in other series, whether in non MDR or in MDR bacteremia [14, 20, 21]. This is probably related to the heterogeneity of age groups and comorbidities. On the other hand, the variability of diagnosis methods and therapeutic management of bacteremia would influence the mortality rate. Moreover, the increasing emergence of MDR bacteria, leading sometimes to therapeutic impasses, closely affects the patients' prognosis.

Like all studies, ours has many limitations. It is a monocentric study carried out on a limited number of cases. Moreover, the patients' outcome outside the ICU was not taken into consideration, this could therefore affect the data's exhaustivity. Concerning the techniques used in the laboratory of bacteriology, the molecular identification of resistance genes was not carried out, the resistant character was retained based only on the antibiograms.

Conclusion

This study highlights the important place occupied by GNB in bacteremia in ICUs. Acinetobacter baumanni and K lebsiella  pneumoniae were most commonly isolated pathogens, reflecting the healthcare-associated nature of these infections and, consequently, the difficulties of hygiene control in ICU settings. The use of broad spectrum antimicrobials cannot be avoided given the increase in the rates of MDR GNB and the resulting infections. This makes it essential to establish an epidemiological surveillance system, in addition to actions on selection pressure, hand hygiene, and optimization of cleaning practices in the ICU.

Funding sources

No financial support was received for this study.

Authors' contribution

Fatima Zahra Adil: acquisition of clinical and biological data, data analysis and interpretation, statistical analysis.

Elmostafa Benaissa: data analysis and interpretation.

Yassine Benlahlou: data analysis and interpretation.

Hicham Bakkali: acquisition of clinical and therapeutic data.

Nawfal Doghmi: acquisition of clinical and therapeutic data.

Hicham Balkhi: acquisition of clinical and therapeutic data.

Adil Maleb: manuscript correction and linguistic review.

Mostafa Elouennass: study concept and design, data analysis and interpretation, manuscript correction and linguistic review.

All authors read and approved the final version of the manuscript.

Conflict of interest

The authors declare no conflict of interest.

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    El Kettani A , Zerouali K , Diawara I , Ouhadous M , Harrar N , Belabbes H , et al. Les bactériémies associées aux soins en réanimation au centre hospitalier universitaire Ibn Rochd, casablanca, Maroc. Santé publique. 2017;29(2):209–13.

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    Ting SW , Lee CH , Liu JW . Risk factors and outcomes for the acquisition of carbapenem-resistant Gram-negative bacillus bacteremia: a retrospective propensity-matched case control study. J Microbiol Immunol Infect. 2018;51(5):621–8.

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    Zhou H , Yao Y , Zhu B , Ren D , Yang Q , Fu Y , et al. Risk factors for acquisition and mortality of multidrug-resistant Acinetobacter baumannii bacteremia: a retrospective study from a Chinese hospital. Medicine. 2019;98(13).

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    Lye DC , Earnest A , Ling ML , Lee T-E , Yong H-C , Fisher DA , et al. The impact of multidrug resistance in healthcare-associated and nosocomial Gram-negative bacteraemia on mortality and length of stay: cohort study. Clin Microbiol Infect. 2012;18(5):502–8.

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    Komori A , Abe T , Kushimoto S , Ogura H , Shiraishi A , Saitoh D , et al. Characteristics and outcomes of bacteremia among ICU-admitted patients with severe sepsis. Scientific Rep. 2020;10(1):18.

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    Michalopoulos A , Falagas ME , Karatza DC , Alexandropoulou P , Papadakis E , Gregorakos L , et al. Epidemiologic, clinical characteristics, and risk factors for adverse outcome in multiresistant gram-negative primary bacteremia of critically ill patients. Am J Infect Control. 2011;39(5):396400.

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    Leal HF , Azevedo J , Silva GEO , Amorim AML , de Roma LRC , Arraes ACP , et al. Bloodstream infections caused by multidrug-resistant gram-negative bacteria: epidemiological, clinical and microbiological features. BMC Infect Dis 2019;19(1):111.

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    Tabah A , Koulenti D , Laupland K , Misset B , Valles J , Bruzzi de Carvalho F , et al. Characteristics and determinants of outcome of hospital-acquired bloodstream infections in intensive care units: the EUROBACT International Cohort Study. Intensive Care Med. 2012;38(12):1930–45.

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    Silago V , Kovacs D , Msanga DR , Seni J , Matthews L , Oravcová K , et al. Bacteremia in critical care units at Bugando Medical Centre, Mwanza, Tanzania: the role of colonization and contaminated cots and mothers’ hands in cross-transmission of multidrug resistant Gram-negative bacteria. Antimicrob Resist Infect Control 2020;9(1):114.

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    Lachhab Z , Frikh M , Maleb A , Kasouati J , Doghmi N , Ben Lahlou Y , et al. Bacteraemia in intensive care unit: clinical, bacteriological, and prognostic prospective study. Can J Infect Dis Med Microbiol. 2017;2017.

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    Elouennass M , Sahnoun I , Zrara A , Bajjou T , Elhamzaoui S . Epidemiology and susceptibility profile of blood culture isolates in an intensive care unit (2002–2005). Médecine et maladies infectieuses. 2007;38(1):1824.

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    CA-SFM-EUCAST . Recommandations. Comité de l’Antibiogramme-Société Française de Microbiologie and European Commitee on Antimicrobial Susceptibility Testing standards, V 1.0, Janvier; 2019, p. 144.

    • Search Google Scholar
    • Export Citation
  • 11.

    El Kettani A , Zerouali K , Diawara I , Ouhadous M , Harrar N , Belabbes H , et al. Les bactériémies associées aux soins en réanimation au centre hospitalier universitaire Ibn Rochd, casablanca, Maroc. Santé publique. 2017;29(2):209–13.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Merzougui L , Barhoumi T , Guizani T , Barhoumi H , Hannachi H , Turki E , et al. Les infections nosocomiales en milieu de réanimation: incidence annuelle et aspects cliniques au Service de Réanimation Polyvalente, Kairouan, Tunisie, 2014. The Pan Afr Med J. 2018;30.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Nasa P , Juneja D , Singh O , Dang R , Arora V , Saxena S . Incidence of bacteremia at the time of ICU admission and its impact on outcome. Indian J Anaesth. 2011;55(6):594.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Kallel H , Houcke S , Resiere D , Roy M , Mayence C , Mathien C , et al. Epidemiology and prognosis of intensive care unit–acquired bloodstream infection. The Am J Trop Med Hyg. 2020;103(1):508.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Mege JL , Bretelle F , Leone M . Sex and bacterial infectious diseases. New microbes and new infections 2018;26:S100–3.

  • 16.

    Patolia S , Abate G , Patel N , Frey S . Risk factors and outcomes for multidrug-resistant Gram-negative bacilli bacteremia. Ther Adv Infect Dis. 2018;5(1):1118.

    • Search Google Scholar
    • Export Citation
  • 17.

    Ting SW , Lee CH , Liu JW . Risk factors and outcomes for the acquisition of carbapenem-resistant Gram-negative bacillus bacteremia: a retrospective propensity-matched case control study. J Microbiol Immunol Infect. 2018;51(5):621–8.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Zhou H , Yao Y , Zhu B , Ren D , Yang Q , Fu Y , et al. Risk factors for acquisition and mortality of multidrug-resistant Acinetobacter baumannii bacteremia: a retrospective study from a Chinese hospital. Medicine. 2019;98(13).

    • Search Google Scholar
    • Export Citation
  • 19.

    Lye DC , Earnest A , Ling ML , Lee T-E , Yong H-C , Fisher DA , et al. The impact of multidrug resistance in healthcare-associated and nosocomial Gram-negative bacteraemia on mortality and length of stay: cohort study. Clin Microbiol Infect. 2012;18(5):502–8.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Komori A , Abe T , Kushimoto S , Ogura H , Shiraishi A , Saitoh D , et al. Characteristics and outcomes of bacteremia among ICU-admitted patients with severe sepsis. Scientific Rep. 2020;10(1):18.

    • Search Google Scholar
    • Export Citation
  • 21.

    Michalopoulos A , Falagas ME , Karatza DC , Alexandropoulou P , Papadakis E , Gregorakos L , et al. Epidemiologic, clinical characteristics, and risk factors for adverse outcome in multiresistant gram-negative primary bacteremia of critically ill patients. Am J Infect Control. 2011;39(5):396400.

    • Crossref
    • Search Google Scholar
    • Export Citation
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The author instruction is available in PDF.
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Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita

Editor(s)-in-Chief: Heimesaat, Markus M.

Vice Editor(s)-in-Chief: Fuchs, Anja

Editorial Board

Chair of the Editorial Board:
Jeffrey S. Buguliskis (Thomas Jefferson University, USA)

  • Jörn Albring (University of Münster, Germany)
  • Stefan Bereswill (Charité - University Medicine Berlin, Germany)
  • Dunja Bruder (University of Megdeburg, Germany)
  • Jan Buer (University of Duisburg, Germany)
  • Jeff Buguliskis (Thomas Jefferson University, USA)
  • Edit Buzas (Semmelweis University, Hungary)
  • Charles Collyer (University of Sydney, Australia)
  • Renato Damatta (UENF, Brazil)
  • Ivelina Damjanova (Semmelweis University, Hungary)
  • Maria Deli (Biological Research Center, HAS, Hungary)
  • Olgica Djurković-Djaković (University of Belgrade, Serbia)
  • Jean-Dennis Docquier (University of Siena, Italy)
  • Anna Erdei (Eötvös Loránd University, Hungary)
  • Zsuzsanna Fabry (University of Washington, USA)
  • Beniam Ghebremedhin (Witten/Herdecke University, Germany)
  • Nancy Guillen (Institute Pasteur, France)
  • Georgina L. Hold (University of Aberdeen, United Kingdom)
  • Ralf Ignatius (Charité - University Medicine Berlin, Germany)
  • Zsuzsanna Izsvak (MDC-Berlin, Germany)
  • Achim Kaasch (University of Cologne, Germany)
  • Tamás Laskay (University of Lübeck, Germany)
  • Oliver Liesenfeld (Roche, USA)
  • Shreemanta Parida (Vaccine Grand Challenge Program, India)
  • Matyas Sandor (University of Wisconsin, USA)
  • Ulrich Steinhoff (University of Marburg, Germany)
  • Michal Toborek (University of Miami, USA)
  • Mary Jo Wick (University of Gothenburg, Sweden)
  • Susanne A. Wolf (MDC-Berlin, Germany)

 

Dr. Dunay, Ildiko Rita
Magdeburg, Germany
E-mail: ildikodunay@gmail.com

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2021  
Web of Science  
Total Cites
WoS
790
Journal Impact Factor not applicable
Rank by Impact Factor not applicable
Impact Factor
without
Journal Self Cites
not applicable
5 Year
Impact Factor
not applicable
Journal Citation Indicator 0,64
Rank by Journal Citation Indicator Microbiology 81/157
Scimago  
Scimago
H-index
not indexed
Scimago
Journal Rank
not indexed
Scimago Quartile Score not indexed
Scopus  
Scopus
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Scopus
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  not indexed
Scopus
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2020  
CrossRef Documents 23
WoS Cites 708
Wos H-index 27
Days from submission to acceptance 219
Days from acceptance to publication 176
Acceptance Rate 70%

2019  
WoS
Cites
558
CrossRef
Documents
24
Acceptance
Rate
92%

 

European Journal of Microbiology and Immunology
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European Journal of Microbiology and Immunology
Language English
Size A4
Year of
Foundation
2011
Volumes
per Year
1
Issues
per Year
4
Founder Akadémiai Kiadó
Founder's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 2062-509X (Print)
ISSN 2062-8633 (Online)

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