Skip to content

Advertisement

  • Research article
  • Open Access
  • Open Peer Review

Low incidence of multidrug-resistant bacteria and nosocomial infection due to a preventive multimodal nosocomial infection control: a 10-year single centre prospective cohort study in neurocritical care

BMC NeurologyBMC series – open, inclusive and trusted201818:23

https://doi.org/10.1186/s12883-018-1031-6

  • Received: 6 November 2017
  • Accepted: 28 February 2018
  • Published:
Open Peer Review reports

Abstract

Background

Nosocomial infection (NI) control is an important issue in neurocritical care due to secondary brain damage and the increased morbidity and mortality of primary acute neurocritical care patients. The primary aim of this study was to determine incidence of nosocomial infections and multidrug-resistant bacteria and seek predictors of nosocomial infections in a preventive multimodal nosocomial infection protocol in the neurointensive care unit (NICU). The secondary aim focused on their impact on stay, mortality and cost in the NICU.

Methods

A10-year, single-centre prospective observational cohort study was conducted on 3464 acute brain disease patients. There were 198 (5.7%) patients with nosocomial infection (wound 2.1%, respiratory 1.8%, urinary 1.0%, bloodstream 0.7% and other 0.1%); 67 (1.9%) with Extended spectrum beta-lactamase (ESBL); 52 (1.5%) with Methicillin-resistant Staphylococcus aureus (MRSA), nobody with Vancomycin-resistant enterococcus (VRE). The protocol included hygienic, epidemiological status and antibiotic policy. Univariate and multivarite logistic regression analysis was used for identifying predictors of nosocomial infection.

Results

From 198 NI patients, 153 had onset of NI during their NICU stay (4.4%; wound 1.0%, respiratory 1.7%, urinary 0.9%, bloodstream 0.6%, other 0.1%); ESBL in 31 (0.9%) patients, MRSA in 30 (0.9%) patients. Antibiotics in prophylaxis was given to 63.0% patients (59.2 % for operations), in therapy to 9.7% patients. Predictors of NI in multivariate logistic regression analysis were airways (OR 2.69, 95% CI 1.81-3.99, p<0.001), urine catheters (OR 2.77, 95% CI 1.00-7.70, p=0.050), NICU stay (OR 1.14, 95% CI 1.12-1.16, p<0.001), transfusions (OR 1.79, 95% CI 1.07-2.97, p=0.025) antibiotic prophylaxis (OR 0.50, 95% CI 0.34-0.74, p<0.001), wound complications (OR 2.30, 95% CI 1.33-3.97, p=0.003). NI patients had longer stay (p<0.001), higher mortality (p<0.001) and higher TISS sums (p<0.001) in the NICU.

Conclusions

The presented preventive multimodal nosocomial infection control management was efficient; it gave low rates of nosocomial infections (4.2%) and multidrug-resistant bacteria (ESBL 0.9%, MRSA 0.9% and no VRE). Strong predictors for onset of nosocomial infection were accesses such as airways and urine catheters, NICU stay, antibiotic prophylaxis, wound complications and transfusion. This study confirmed nosocomial infection is associated with worse outcome, higher cost and longer NICU stay.

Keywords

  • Neurocritical care
  • Nosocomial infections
  • Multidrug-resistant bacteria
  • Outcome
  • Preventive protocol

Background

Nosocomial infections (NI) are still an important issue in neurocritical care due to secondary brain damage and the increased morbidity and mortality of primary acute neurocritical care patients [15]. NI is associated with higher antibiotic consumption, thereby worsening the epidemiological situation in the intensive care unit by increasing the occurrence of multidrug-resistant bacteria [6]. For these reasons, they have a significant economic impact because they prolong stay [710] in the neurointensive care unit (NICU) and the higher frequency of diagnostic and therapeutic processing significantly raises healthcare costs.

Nosocomial infections can be caused by many risk factors, not all of which have been fully investigated. However, keeping a hygienic and epidemiological regime of critical care [1113] and the rational use of antibiotics makes a significant impact [14, 15].

The primary aim of this study was to determine incidence of nosocomial infections and multidrug-resistant bacteria and seek predictors of nosocomial infections in a preventive multimodal nosocomial infection protocol in our neurocritical care. The secondary aim focused on their impact on stay, mortality and cost in the NICU.

Method

Study design and setting

A monocentric 10-year observation prospective cohort study was conducted in the entire population of 3464 patients with acute brain disease, admitted to an eight-bed, adult neurological and neurosurgical intensive care unit in the Neurocenter of the 900-bed Regional Hospital with a catchment area of approximately half a million people. The study was performed in the NICU, which consists of four different rooms: one room with one bed, two rooms with two beds and one room with three beds. The study was approved by the Liberec hospital Ethics Committees for Multicentric Clinical Trials.

We prospectively examined the following determined demographic and clinical parameters in our local NICU: brain diagnosis, type of admission (primary, secondary to 24 hours and after 24 hours; acute or planned; rehospitalisation), admission and overall Therapeutic Intervention Scoring System (TISS), admission Glasgow Coma Scale (GCS), admission Acute Physiology and Chronic Health Evaluation (APACHE) II score, length of stay in the NICU, mortality in the NICU, Glasgow Outcome Scale (GOS) upon discharge from the NICU, C-reactive protein (CRP), operations (amount, day of hospital and NICU hospitalisation, acute or planned, reoperation, time and type of operation), American Society of Anesthesiologists (ASA) Score, drainage, airways, mechanical ventilation, catheters (artery, central venous, urine) and tubes, administration of corticoids, transfusions, ulcer prophylaxis and diabetes mellitus.

Preventive multimodal nosocomial infection protocol

In the preventive multimodal nosocomial infection protocol, we categorised hygienic and epidemiological status and antibiotic policy.

Hygienic and epidemiological regime

The basis of the hygienic and epidemiological regime in our preventive multimodal protocol consisted of cleanliness, disinfection, sterilisation, barrier patient care techniques, the separation of clean and contaminated procedures and the regular monthly exchange of disinfectants. We categorised principles for staff, patients and facilities.

1/Staff and visitors

The foremost part of this protocol was maintaining the hygiene and disinfection of all staff members’ hands before and after care for each patient, enabled by the bottled disinfectant provided at each entrance and each bed. This rule was also required for visitors. Staff members were not allowed to wear jewellery or watches on their hands and had to keep their fingernails cut short. Internal staff had to wear new, clean, special NICU clothing every day, a protective coat when outside the NICU, and masks, surgical caps and gowns when caring for isolated patients or during invasive medical procedures. Aprons were worn while washing patients. External staff as well as visitors wore surgical gowns, but not overshoes, and only 2 family members were allowed in the patient’s room at a time.

2/Patients

Care of the patient was performed on the principle of barrier care techniques. Tools for individual patients including disinfection, stethoscopes, thermometers and washing aids were available by each bed. Patients were washed twice a day with liquid soap. Disinfection soap was used only before entering the operating theatre. Oral hygiene included cleaning teeth with our special toothbrushes with chlorhexidine and subglottic secretion drainage, after washing, the patient’s body was rubbed with a non-allergic cream. Patients’ clothes and bedding were changed twice a day. Dirty laundry was put in special sacks rather than dropped freely on the floor.

Basic principles of care for drainage, catheters, infusion, suction from the airway, breathing circuit sets, tubes included: 1/single-use products, 2/closed systems, 3/the minimum necessary duration, 4/minimal and only necessary disconnection, using the port system, 5/the regular (peripheral venous catheters, all infusion sets, connecting tubes and ports) and irregular (central venous catheters, endotracheal tubes and tracheostomy) exchange of all these tubes and catheters was made according to the exchange protocol. Invasive procedures included the sterile insertion of systems and regularly exchanged, fully covering and constantly dry sterile wound covers. Furthermore, the protocol included the hourly monitoring of residual gastric volume.

The protocol included the regular microbiological screening of nose, throat, trachea, skin, urine and rectum from admission and then every three days, as well as every catheter except the peripheral venous for the timely detection of multidrug-resistant bacteria extended spectrum beta-lactamases (ESBL) or methicillin-resistant Staphylococcus aureus (MRSA) or Vancomycin-resistant enterococcus (VRE).

Patients with an infection or with multidrug-resistant bacteria ESBL and MRSA were completely isolated.

3/Facilities

Daily cleaning with disinfection of surfaces including the bed, monitors, and other equipment around the bed, door handles and floors was conducted three times a day. Walls were cleaned once a day for the isolated patients, otherwise once a week. Each room had its own bucket for surfaces and walls. The floors were mopped using a system of two buckets and a cloth, with each room having its own. All cupboards containing materials and medical equipment were cleaned with disinfectant once a week. Waste was sorted and disposed of using specially marked plastic containers and sacks. After the patient was discharged, the bed was completely disinfected. The room was painted with a washable coating once a year.

Antibiotic policy

The protocol included the monitoring of antibiotics in a local computer database. Antibiotic policy was implemented in close cooperation with the antibiotic centre and intended to keep the rational antibiotic policy aim of eliminating the overuse of antibiotics, especially those not used during bacterial pathogeny colonisation. The indications for using prophylactic antibiotics were surgical procedures (operation, external ventricular and lumbar drainage, intracranial sensors), liquorrhoea and aspiration. The protocol required maintaining dose and timing before the operation, perioperative administration for lengthy operations, and the non-prolongation of antibiotic administration after the operation or drainage or implantation of sensors. Empiric antibiotic therapy was to start after samples were taken for microbiological examination to enable their administration according to culture and sensitivity.

Nosocomial infection

Infections were identified according to clinical symptoms such as fever, bacterial pathogens from secretions, liquor, urine, wounds, catheters, haemoculture with a defined microbiology colony count, imaging methods, biochemical and haematological laboratory tests. Nosocomial infections were defined as infections starting after two calendar days in the hospital. We identified nosocomial infections in 198 patients (5.7%). There were more wound infections (2.1%), than respiratory (1.8%), urinary (1.0%), bloodstream (0.7%) and others (0.1%).

Statistical analysis

Parametric t-tests or non-parametric Mann-Whitney U tests were used for comparison of continuous variables. Comparison of categorical parameters was carried out using Chi-square or Fisher tests as appropriate. Univariate logistic regression was used for identifying prognostic factors of NI. Factors from univarite analysis with level of significance defined as p <0.1 were used for multivarite regression analysis, factors with p value <0.1 were left in the model. P–values of less than 0.05 were considered significant. STATISTICA 13.2 (TIBCO Software Inc., Palo Alto, CA, USA) software was used for statistical analyses. The control group was defined as patients without nosocomial infections.

Results

We did not find any demographic differences such as age, gender, weight or body mass index between the NI group and the control group, as can be seen in Table 1. However, there was a difference in diagnosis, more patients with stroke and hydrocephalus had more NI than those with other diagnoses. According to the scoring system, patients with nosocomial infection upon admission had significantly lower GCS scale and higher APACHE II. Prognostic parameters were also significantly higher in the NI patients group. They stayed in the NICU longer, had higher mortality and worse Glasgow Coma Scale upon discharge. They were also more expensive economically, and had significantly higher total TISS.
Table 1

Demographic and clinical data of population of patients with acute brain disease, with or without nosocomial infection

Parameter

Unit

Total population

NI group

Control group

p value

Number total

pts

3464 (100%)

198 (5.7%)

3266 (94.3%)

 

January

pts

327 (9.4%)

7 (3.6%)

310 (9.5%)

 

February

pts

249 (7.2%)

19 (9.6%)

230 (7.0%)

 

March

pts

267 (7.7%)

19 (9.6%)

248 (7.6%)

 

April

pts

305 (8.8%)

13 (6.6%)

292 (8.9%)

 

May

pts

269 (7.8%)

21 (10.6%)

248 (7.6%)

 

June

pts

290 (8.4%)

17 (8.6%)

273 (8.4%)

0.660

July

pts

310 (8.9%)

19 (9.6%)

291 (8.9%)

 

August

pts

274 (7.98%)

12 (6.1%)

262 (8.0%)

 

September

pts

307 (8.9%)

14 (7.1%)

293 (9.0%)

 

October

pts

280 (8.1%)

13 (6.6%)

267 (8.2%)

 

November

pts

291 (8.4%)

17 (8.6%)

274 (8.4%)

 

December

pts

295 (8.5%)

17 (8.6%)

278 (8.5%)

 

Age

pts

 

57.2±15.6

56.3±15.6

0.416

Male

pts

2004 (57.9%)

117 (59.1%)

1887 (57.8%)

0.716

Weight

kg

 

78.7±17.1

77.6±15.8

0.423

BMI

  

26.8±5.0

26.8±4.9

0.966

NICU stay

day

 

15.3±11.7

4.8±5.4

<0.001

Admission

     

 Primary

pts

746 (21.5%)

47 (23.7%)

699 (21.4%)

 

 Secondary to 24 h

pts

739 (21.3%)

51 (25.8%)

688 (21.1%)

0.134

 Secondary after 24 h

pts

1979 (57.1%)

100 (50.5%)

1879 (57.5%)

 

Acute admission

pts

1020 (29.4%)

70 (35.4%)

950 (29.1%)

<0.001

Rehospitalisation

pts

40 (1.22%)

4 (2.0%)

44 (1.3%)

0.331

Diagnoses

     

 Stroke

pts

1498 (43.2%)

110 (55.6%)

1388 (42.5%)

 

 Trauma

pts

472 (13.6%)

27 (13.6%)

445 (13.6%)

 

 Tumour

pts

1078 (31.1%)

33 (16.7%)

1045 (32.0%)

<0.001

 Epilepsy

pts

133 (3.8%)

3 (1.5%)

130 (4.0%)

 

 Hydrocephalus

pts

119 (3.4%)

13 (6.6%)

106 (3.2%)

 

 Infection

pts

88 (2.5%)

11 (5.6%)

77 (2.4%)

 

 Others

pts

75 (2.2%)

1 (0.5%)

74 (2.3%)

 

 Stroke

pts

   

<0.001

  Ischemic

pts

580 (16.7%)

21 (10.6%)

559 (17.1%)

  ICH

pts

471 (13.6%)

49 (24.7%)

422 (12.9%)

  SAH

pts

447 (12.9%)

40 (20.2%)

407 (12.5%)

TISS on admission

  

54.7±1.9

56.0±1.7

<0.001

TISS total

  

270632.8±231533.1

60415.1±92140..3

<0.001

GCS on admission

  

11.5±3.5

13.1±3.0

<0.001

APACHE II on admission

  

15.1±5.5

11.8±5.8

<0.001

GOS on NICU discharge

  

3.1±1.1

3.9±1.1

<0.001

Mortality in NICU

pts

152 (4.4%)

21 (10.6%)

131 (4.0%)

<0.001

Mortality in NICU

day

 

16.2±10.4

7.5±5.7

<0.001

CRP on admission

  

31.7±45.6

17.5±39.1

<0.001

CRP postoperative

  

30.0±44.4

14.0±33.0

<0.001

CRP 1 day after operation

  

59.8±56.9

31.6±39.6

<0.001

CRP highest in NICU stay

  

228.0±122.5

66.1±80.3

<0.001

BMI body mass index, NICU neurointensive care unit, ICH intracerebral haemorrhage, SAH subarachnoid haemorrhage, TISS Therapeutic Intervention Scoring System, GCS Glasgow Coma Scale, APACHE Acute Physiology and Chronic Health Evaluation, GOS Glasgow Outcome Scale, CRP C-reactive protein

Characteristics of brain operations can be seen in Table 2. Patients who had undergone operations and drainage had significantly higher nosocomial infection. These patients had more endotracheal tubes and tracheostomies, mechanical ventilations (Table 3), artery and central venous catheters (Table 4), urine and gastrointestinal tubes (Table 5).
Table 2

Characteristics of brain operations

Operation

Unit

Total population N=2231

NI group N=151

Control group N=2080

p value

Operation

pts

2231(64.4%)

151(76.3%)

2080 (63.7%)

<0.001

More than 1 operation

pts

214(9.6%)

42(27.8%)

172(8.3%)

<0.001

ASA score

  

3.8±1.0

3.1±1.1

<0.001

Day of hospitalisation

day

 

5.5±9.8

7.1±17.1

0.430

Day of NICU

  

1.6±1.3

1.3±1.1

0.535

Acute operation

pts

905(40.6%)

106(70.2%)

799(38.4%)

<0.001

Reoperation

pts

479(21.5%)

58(38.4%)

421(20.2%)

<0.001

Time of operation

minutes

 

151.9±108.4

137.7±89.4

0.080

Craniotomy

pts

1361(61.0%)

82(54.3%)

1279(61.5%)

0.080

Craniectomy

pts

363(16.3%)

50(33.1%)

313(15.0%)

<0.001

Trepanation

pts

227(10.2%)

23(15.2%)

204(9.8%)

0.033

Hypophysis

pts

85(3.8%)

0(0.0%)

85(4.1%)

0.011

Shunt

pts

108(4.8%)

12(7.9%)

96(4.6%)

0.066

Others

pts

99(4.4%)

9(6.0%)

90(4.3%)

0.347

Drainage

pts

1678(75.2%)

131(86.8%)

1547(74.4%)

<0.001

 Redon

pts

858(38.5%)

49(32.5%)

809(38.9%)

0.001

 Time overall

day

 

2.0±0.9

1.8±1.3

0.395

 Gravity drainage

pts

807(36.2%)

75(49.7%)

732(35.2%)

0.029

  Time overall

day

 

3.5±2.1

2.7±2.2

0.004

 Lumbar

pts

218(9.8%)

36(23.8%)

182(8.8%)

<0.001

  Day overall

day

 

7.7±5.5

5.1±3.2

<0.001

 Ventricular

pts

138(6.2%)

21(13.9%)

117(5.6%)

<0.001

  Day overall

day

 

13.4±9.9

5.9±4.3

<0.001

ASA American Society of Anesthesiologists, NICU neurointensive care unit

Table 3

Characteristics of respiratory procedures

Parameter

Unit

Total population N=3646

NI group N=198

Control group

N=3266

p value

Airways

pts

710 (20.5%)

112 (56.6%)

598 (18.3%)

<0.001

 ETT

pts

327(46.1%)

15(13.4%)

312(52.2%)

 

 TSK

pts

161(22.7%)

29(25.9%)

132(22.1%)

<0.001

 ETT/TST

pts

222(31.3%)

68(60.7%)

154(25.8%)

 

 ETK time NICU

day

 

4.2±2.1

2.9±2.2

<0.001

 ETK time

day

 

4.4±2.1

2.9±2.3

<0.001

 TSK time NICU

day

 

14.2±10.2

8.4±7.8

<0.001

 TSK time

day

 

21.8±34.6

21.6±62.2

0.980

 TSK type Classic

pts

43(11.2%)

9(9.3%)

34(11.9%)

0.456

 TSK NICU made

pts

250(65.3%)

75(77.3%)

175(61.2%)

0.006

Mechanical ventilation

pts

543(15.7%)

87(43.9%)

456(14.0%)

<0.001

 Invasive

pts

539(99.3%)

87(100.0%)

452(99.1%)

<0.001

 Time

day

 

14.1±9.9

5.6±5.9

<0.001

Indication

 Neuro

pts

414(76.2%)

54(62.1%)

360(78.9%)

0.161

 Respiratory

pts

32(5.9%)

7(8.0%)

25(5.5%)

ETT endotracheal tube, TST tracheostomy tube, NICU neurointensive care unit

Table 4

Characteristics of vascular catheters

Parameter

Unit

Total population N=3464

NI group N=198

Control group N=3266

p value

Artery catheter

pts

907(26.2%)

90(45.5%)

817(25.0%)

<0.001

Time

day

 

9.5±6.6

7.5±3.7

0.018

Number of artery catheters

 

923(100.0%)

91(100.0%)

832(100.0%)

 

 Radialis

pts

873(94.6%)

89(97.8%)

784(94.2%)

0.165

 Brachialis

pts

14(1.5%)

0(0.0%)

14(1.7%)

0.211

 Femoralis

pts

36(3.9%)

2(2.2%)

34(4.1%)

0.371

 Left

pts

598(64.8%)

64(70.3%)

534(64.2%)

0.275

 Time in NICU

day

 

8.27±5.45

4.10±3.36

0.094

 Time all

day

 

8.41±5.40

4.41±3.43

0.377

 Made in NICU

pts

216(23.4%)

47(51.6%)

169(20.3%)

<0.001

 Made in operation theatre

pts

607(65.8%)

46(50.5%)

561(67.4%)

0.001

 Cultivation of catheter

pts

691(74.9%)

74(81.3%)

617(74.2%)

0.157

  Positive

pts

113(16.4%)

18(24.3%)

95(15.4%)

0.050

  STSP

pts

100(88.5%)

13(72.2%)

87(91.6%)

0.018

 Haemoculture cultivation

pts

164(17.8%)

31(34.1%)

133(16.0%)

<0.001

  Positive

pts

34(20.7%)

9(29.0%)

25(18.8%)

0.206

  STSP

pts

18(52.9%)

3(33.3%)

15(60.0%)

0.169

Central venous catheter

pts

372(10.7%)

64(32.3%)

308(9.4%)

<0.001

Time overall

day

 

9.9±7.4

7.5±3.7

0.077

Number of venous catheter

 

378(100%)

66(100%)

312(100%)

 

 Subclavia

pts

336(88.9%)

60(90.9%)

276(88.5%)

0.308

 Jugularis

pts

19(5.0%)

1(1.5%)

18(5.8%)

0.157

 Femoralis

pts

16(4.2%)

4(6.1%)

12(3.8%)

0.398

 Axilaris

pts

7(1.9%)

1(1.5%)

6(1.9%)

0.836

 Right

pts

323(85.4%)

59(89.4%)

264(84.6%)

0.164

 Type one-line

pts

75(19.8%)

10(15.2%)

65(20.8%)

 

 Type two-line

pts

192(50.8%)

39(59.1%)

153(49.0%)

0.214

 Type three-line

pts

64(16.9%)

8(12.1%)

56(17.9%)

 

 Time in NICU

day

 

8.20±7.31

4.70±4.92

<0.001

 Time all

day

 

11.19±8.70

7.24±5.50

<0.001

 Made in NICU

pts

162(42.9%)

41(62.1%)

121(38.8%)

<0.001

 Made in operation theatre

pts

14(3.7%)

1(1.5%)

13(4.2%)

0.309

 Cultivation of catheter

pts

261(69.0%)

45(68.2%)

216(69.2%)

0.977

  Positive

pts

52(19.9%)

16(35.6%)

36(16.7%)

0.004

  STSP

pts

40(76.9%)

10(62.5%)

30(83.3%)

0.010

 Haemoculture cultivation

pts

72(19.0%)

16(24.2%)

56(17.9%)

0.090

  Positive

pts

15(20.8%)

2(12.5%)

13(23.2%)

0.352

  STSP

pts

13(86.7%)

2(100.0%)

11(84.6%)

0.551

NICU neurointensive care unit, STSP Staphylococcus species

Table 5

Characteristics of urine and gastrointestinal procedures

Parameter

Unit

Total population N=3464

NI group N=198

Control group N=3266

p value

Urine catheter

pts

3166(91.4%)

189(95.5%)

2927(89.6%)

0.008

 Epicystostomy

pts

6(0.2%)

1(0.5%)

5(0.2%)

0.247

 Time

day

 

15.5±11.6

4.7±5.5

<0.001

 Time overall

day

 

22.6±13.1

12.8±9.7

<0.001

Gastrointestinal tube

pts

904(26.1%)

128(64.6%)

776(23.8%)

<0.001

 Nasogastric tube

pts

882(25.5%)

125(63.1%)

757(23.2%)

<0.001

 Time

day

 

15.4±11.2

6.2±6.9

<0.001

 Time overall

day

 

19.6±12.6

10.7±9.4

<0.001

We confirmed transfusions (p<0.001), ulcer prophylaxis (p<0.001) and corticoids (p=0.002) as further parameters influencing nosocomial infection, but we did not see more nosocomial infection in patients with diabetes mellitus (p=0.203), (Table 6).
Table 6

Further monitored parameters influencing onset of nosocomial infection

Parameter

Unit

Total population N=3464

NI group N=198

Control group N=3266

p value

Corticoids

pts

1172(33.8%)

47(23.7%)

1125(34.4%)

0.002

 Dexamethasone

pts

944(27.3%)

31(15.7%)

913(28.0)

<0.001

 Methylprednisolone

pts

35(1.0%)

5(2.5%)

30(0.9%)

0.028

 Hydrocortisone

pts

241(7.0%)

12(6.1%)

229(7.0%)

0.610

 Time

day

 

6.37±8.78

3.58±2.56

<0.001

Transfusions

pts

176(5.1%)

41(20.7%)

135(4.1%)

<0.001

 Number

  

2.46±8.78

2.57±2.56

0.695

 Blood loss

ml

 

523.77±668.07

380.74±478.76

0.019

 Haemoglobin

  

93.35±21.03

115.34±21.62

<0.001

Ulcer prophylaxis

pts

1838(53.1%)

134(67.7%)

1704(52.2%)

<0.001

 One medicine

pts

1669(48.2%)

119(60.1%)

1550(47.5%)

0.406

 Sucralfate

pts

758(21.9%)

26(13.1%)

732(22.4%)

0.002

 H2 antagonist

pts

196(5.7%)

27(13.6%)

169(5.2%)

<0.001

 Omeprazole

pts

1062(30.7%)

97(49.0%)

965(29.5%)

<0.001

Diabetes Mellitus

pts

491(14.2%)

22(11.1%)

469(14.4%)

0.203

Op. wound complication

pts

133(3.8%)

35(17.7%)

98(3.0%)

<0.001

Liquorrhoea

pts

81(2.3%)

23(11.6%)

58(1.8%)

<0.001

ESBL occurred in 1.9% and MRSA in 1.5% of the total population, without differences between NI group patients and the control group (Table 7). We did not have any case of vancomycin-resistant enterococcus.
Table 7

Multidrug-resistant bacteria ESBL and MRSA in NICU

Parameter

Unit

Total population N=3464

NI group N=198

Control group N=3266

p value

Multidrug-resistant

pts

116(3.3%)

12(6.1%)

104(3.2%)

0.029

ESBL

pts

67(1.9%)

6(3.0%)

61(1.9%)

0.566

 On admission

pts

36(1.0%)

4(2.0%)

32(1.0%)

0.249

  Nose

pts

11(0.3%)

1(0.5%)

10(0.3%)

0.986

  Throat

pts

21(0.6%)

4(2.0%)

17(0.5%)

0.051

  Trachea

pts

15(0.4%)

1(0.5%)

14(0.4%)

0.725

  Urine

pts

19(0.5%)

0(0.0%)

19(0.6%)

0.106

  Rectum

pts

31(0.9%)

3(1.5%)

28(0.9%)

0.848

  Brain

pts

2(0.1%)

1(0.5%)

1(0.0%)

0.039

  Others

pts

5(0.1%)

1(0.5%)

4(0.1%)

0.369

MRSA

pts

52(1.5%)

7(3.5%)

45(1.4%)

0.320

 On admission

pts

22(0.6%)

0(0.0%)

22(0.7%)

0.015

  Nose

pts

27(0.8%)

4(2.0%)

23(0.7%)

0.766

  Throat

pts

11(0.3%)

1(0.5%)

10(0.3%)

0.632

  Trachea

pts

14(0.4%)

2(1.0%)

12(0.4%)

0.916

  Brain

pts

5(0.1%)

1(0.5%)

4(0.1%)

0.652

  Haemoculture

pts

1(0.0%)

0(0.0%)

1(0.0%)

0.690

  Others

pts

5(0.1%)

0(0.0%)

5(0.2%)

0.354

NICU neurointensive care unit, ESBL Extended spectrum beta-lactamase, MRSA Methicillin-resistant Staphylococcus aureus

Antibiotics policy is shown in Table 8. Antibiotic prophylaxis was given to 63% of the total population, mostly (59.2%) in association with operations. In 33.4% of the patients it was only administered in the operating theatre. Prolonged administration in the NICU was associated with more NIs (p=0.017). Antibiotic therapy was given to 9.7% of the total population.
Table 8

Administration of antibiotics in NICU

Parameter

Unit

Total population N=3464

NI group N=198

Control group N=3266

p value

Antibiotic prophylaxis

pts

2183(63.0%)

127(64.1%)

2056(63.0%)

0.736

 One prophylaxis

pts

1931(55.7%)

91(46.0%)

1840(56.3%)

<0.001

 Operation

pts

2049(59.2%)

116(58.6%)

1933(59.2%)

0.222

  Only operation theatre

pts

1157(33.4%)

61(30.8%)

1096(33.6%)

 

  Operation 1 dose

pts

924(26.7%)

42(21.2%)

882(27.0%)

 

  Operation 2 doses

pts

191(5.5%)

14(7.1%)

177(5.4%)

0.006

  Operation 3 doses

pts

40(1.2%)

4(2.0%)

36(1.1%)

 

  Operation 4 doses

pts

2(0.1%)

1(0.5%)

1(0.0%)

 

  NICU

day

 

4.96±5.69

3.31±2.88

0.017

Others

 Aspiration

pts

51(1.5%)

5(2.5%)

46(1.4%)

0.218

 Suspected infection

pts

49(1.0%)

2(1.0%)

47(1.4%)

0.600

 Trauma

pts

30(1.4%)

2(1.0%)

28(0.9%)

0.844

 Liquorrhoea

pts

46(0.9%)

6(3.0%)

40(1.2%)

0.034

 Drainage

pts

35(1.3%)

6(3.0%)

29(0.9%)

0.004

 Others

pts

31(1.0%)

4(2.0%)

27(0.8%)

0.090

 NICU

Day

 

7.75±4.61

4.54±3.33

<0.001

Type of antibiotic

 Cefazolin

pts

1733(50.0%)

106(53.5%)

1627(49.8%)

0.242

 Amoxicillin clavulanate

pts

362(10.5%)

30(15.2%)

332(10.2%)

0.028

 Clindamycin

pts

127(3.7%)

5(2.5%)

122(3.7%)

0.351

Antibiotic therapy

pts

335(9.7%)

169(85.4%)

166(5.1%)

<0.001

One infection

pts

326(9.4%)

161(81.3%)

165(5.1%)

0.019

One antibiotic

pts

220(6.4%)

100(50.5%)

120(3.7%)

0.061

Two antibiotics

pts

78(2.3%)

44(22.2%)

34(1.0%)

 

NICU start

pts

224(6.5%)

151(76.3%)

73(2.2%)

<0.001

Empirical therapy

pts

201(5.8%)

101(51.0%)

100(3.1%)

0.929

According to cultivation

pts

189(5.5%)

106(53.5%)

83(2.5%)

0.019

Days of ATB all

day

 

8.82±6.89

6.09±4.95

<0.001

Type of antibiotic

 Ceftriaxone

pts

34(1.0%)

9(4.5%)

25(0.8%)

0.003

 Ceftazidime

pts

6(0.2%)

3(1.5%)

3(0.1%)

0.982

 Meropenem

pts

75(2.2%)

48(24.2%)

27(0.8%)

0.008

 Penicillin

pts

13(0.4%)

5(2.5%)

8(0.2%)

0.378

 Oxacillin

pts

23(0.7%)

17(8.6%)

6(0.2%)

0.020

 Ciprofloxacin

day

84(2.4%)

57(28.8%)

27(0.8%)

<0.001

 Trimethoprim

pts

17(0.5%)

10(5.1%)

7(0.2%)

0.478

Gentamicin

pts

25(0.7%)

15(7.6%)

10(0.3%)

0.321

Others

pts

71(2.0%)

29(14.6%)

42(1.3%)

0.068

NICU neurointensive care unit, ATB antibiotic

We compared patients with NI onset in the NICU (77.3%) with NI present on admission (22.7%), (Table 9). We identified 153 (4.4%; wound 1.0%, respiratory 1.7%, urinary 0.9%, bloodstream 0.6% and other 0.1%) patients with NI onset in the NICU. Patients with NI onset in the NICU stayed in the NICU significantly longer, and were more expensive, but these patients did not have higher mortality. Multivariate logistic regression analysis seeking significant predictors for onset of NI in the NICU can be seen in Table 10. Our results showed that strong predictors on onset of NI in our neurocritical care were accesses such as airways and urine catheters, NICU stay, antibiotic prophylaxis, wound complications and transfusion. This analysis did not find the multidrug-resistant bacteria as ESBL and MRSA to be a predictor of NI.
Table 9

Nosocomial infections on admission and onset in the NICU

Parameter

Unit

NI total

NI on admission

NI onset in NICU

p value

Number total

pts

198 (100%)

45 (22.7%)

153 (77.3%)

 

Age

pts

57.2±15.6

53.7±16.9

58.3±15.1

0.086

Male

pts

117(59.1%)

18(40.0%)

63(41.2%)

<0.001

NICU stay

day

15.3±11.7

6.9±7.2

17.7±11.6

<0.001

Diagnoses

 Stroke

pts

110(55.6%)

13(28.9%)

97(63.4%)

 

 Trauma

pts

27(13.6%)

3(6.7%)

24(15.7%)

 

 Tumour

pts

33(16.7%)

13(28.9%)

20(13.1%)

 

 Epilepsy

pts

3(1.5%)

0(0.0%)

3(2.0%)

<0.001

 Hydrocephalus

pts

13(6.6%)

7(15.6%)

6(3.9%)

 

 Infection

pts

11(5.6%)

9(20.0%)

2(1.3%)

 

 Others

pts

1(0.5%)

0(0.0%)

1(0.7%)

 

TISS on admission

 

54.7±1.9

56.0±179

54.3±1.8

<0.001

TISS total

 

270632.8±231533.1

111173.7±231533.1

309492.6±234698.9

<0.001

GCS on admission

 

11.5±3.5

12.0±3.3

11.3±3.5

0.234

APACHE II on admission

 

15.1±5.5

13.6±5.4

15.4±5.5

0.099

GOS on NICU discharge

 

3.1±1.1

3.5±1.2

3.0±1.1

0.015

Mortality in NICU

pts

21(10.6%)

3(6.7%)

18(11.8%)

0.329

Operation

pts

151(76.3%)

37(82.2%)

114(74.5%)

0.285

Airways

pts

112(56.6%)

16(35.6%)

96(62.7%)

0.001

Mechanical ventilation

pts

87(43.9%)

7(15.6%)

80(52.3%)

<0.001

Artery catheter

pts

90(45.5%)

6(13.3%)

84(54.9%)

<0.001

Central venous catheter

pts

64(32.3%)

11(24.4%)

53(34.6%)

0.199

Lumbar drainage

pts

36(18.2%)

5(11.1%)

31(20.3%)

0.162

Ventricular drainage

pts

21(10.6%)

3(6.7%)

18(11.8%)

0.329

Corticoids

pts

47(23.7%)

11(24.4%)

36(23.5%)

0.899

Transfusions

pts

41(20.7%)

5(11.1%)

36(23.5%)

0.071

Ulcer prophylaxis

pts

134(67.7%)

27(60.0%)

107(69.9%)

0.210

Diabetes Mellitus

pts

22(11.1%)

3(6.7%)

19(12.4%)

0.280

Antibiotic prophylaxis

pts

127(64.1%)

23(51.1%)

104(68.0%)

0.038

Antibiotic therapy

pts

169(85.4%)

28(62.2%)

141(92.2%)

<0.001

ESBL

pts

6(3.0%)

1(2.2%)

5(3.3%)

0.719

MRSA

pts

7(3.5%)

1(2.2%)

6(3.9%)

0.587

One infection

pts

189(95.5%)

45(100.0%)

144(94.1%)

 

Two infections

pts

8(4.0%)

0(0.0%)

8(5.2%)

0.250

Three infections

pts

1(0.5%)

0(0.0%)

1(0.7%)

 

 Bloodstream

pts

23(11.6%)

1(2.2%)

22(14.4%)

0.025

   Vascular catheter

pts

14(7.1%)

1(2.2%)

13(8.5%)

0.149

 Respiratory

pts

63(31.8%)

3(6.7%)

60(39.2%)

< 0.001

  VAP

pts

34(17.2%)

1(2.2%)

33(21.6%)

0.002

 Urinary

pts

35(17.7%)

5(11.1%)

30(19.6%)

0.189

  Urinary catheter

pts

33(16.7%)

5(11.1%)

25(16.3%)

0.255

 Wound without operation

pts

2(1.0%)

1(2.2%)

1(0.7%)

0.355

 Wound with operation

pts

70(35.4%)

35(77.8%)

35(22.9%)

<0.001

  Wound complication

   Liquorrhoea

pts

14(7.1%)

7(15.6%)

7(4.6%)

0.012

   Dehiscence

pts

11(5.6%)

9(20.0%)

2(1.3%)

<0.001

   Fistula

pts

6(3.6%)

3(6.7%)

3(2.0%)

0.105

NICU neurointensive care unit, TISS Therapeutic Intervention Scoring System, GCS Glasgow Coma Scale, APACHE Acute Physiology and Chronic Health Evaluation, GOS Glasgow Outcome Scale, ESBL Extended spectrum beta-lactamase, MRSA Methicillin-resistant Staphylococcus aureus, VAP ventilator associated pneumonia

Table 10

Multivariate logistic regression analysis of nosocomial infection onset in NICU

Multivariate analysis

    

Nosocomial infections predictors

Odds Ratio

Lower CL 95%

Upper CL 95%

p value

NICU stay (per day)

1.14

1.12

1.16

< 0.001

Airways

2.69

1.81

3.99

< 0.001

Urine catheter

2.77

1.00

7.70

0.050

Transfusions

1.79

1.07

2.97

0.025

Wound complications

2.30

1.33

3.97

0.003

Antibiotic prophylaxis

0.50

0.34

0.74

< 0.001

NICU neurointensive care unit, CL confidence limit

Discussion

Maintaining nosocomial infection control management is one marker of quality in neurocritical care. Its target is to improve clinical outcomes and decrease costs in the neurocritical care unit. Preventions of nosocomial infections are an important issue in all medical or surgical critical care units, but in neurocritical care they have an additional risk as a cause of secondary brain damage, which affects the morbidity and mortality of primary brain diseases [15]. As the aim of neurocritical care is to avoid all insults causing secondary brain damage, preventive management of nosocomial infections is a challenge for neurointensivists. Incidence of nosocomial infections can be reduced by keeping a hygienic and epidemiological regime and rational antibiotic policy. Nosocomial infection management demands constant maintenance and stable teamwork while maintaining standard procedures. We present our preventive multimodal nosocomial infection protocol, which we implemented in our NICU. The first phase involves imposing hygienic principles and the antibiotics policy. The second phase, actually keeping to this protocol, is a much more difficult task in our experience, as a vital component for its success is the participation of the whole team, from doctors and nurses to cleaners working in the neurocritical care unit and even visitors. The use of standard procedures and meticulous checks are an important part of the regime.

Here we present the impact of our preventive nosocomial infection management on the incidence of nosocomial infections in all the patients admitted to our NICU with acute brain disease. The results show that our preventive protocol was not sufficient to completely eliminate all nosocomial infections, but it did lead to a relatively low nosocomial infection incidence of 4.4%. We did not observe differences between various seasons of the year, either among primary or secondary admissions, but we did among acute admissions, acute operations and reoperations. Infections were more frequently associated with strokes than other brain diagnoses. There were significantly more infections in airways, mechanical ventilations and catheters, but only airways and urine catheters were strong predictors in multivariate logistic regression analysis. These are still risk factors which remained despite the maintenance of the preventive strategy. Further predictors were confirmed to be the well-known factors of NICU stay, wound complications, antibiotic prophylaxis and transfusion.

The increasing colonisation of multidrug-resistant bacteria ESBL and MRSA is a big problem among critically ill patients and this situation is getting worse. At present, many patients already have these bacteria on admission and this colonization constitutes a risk of nosocomial infections [1618]. We deal with this by completely isolating these patients using barrier care techniques in order to prevent the transmission of these multidrug-resistant ESBL and MRSA to other, uncolonised patients. This was reflected in our results, which showed that we had newly occurred ESBL in only in 31 (0.9%) patients and MRSA in 30 (0.9%) patients. In this study we did not find that multidrug-resistant bacteria were a predictor of nosocomial infections.

Antibiotics policy, predominantly the overuse of antibiotics, is another big issue in preventive multimodal nosocomial infection protocol. From our results, we see that antibiotic prophylaxis is mainly used in association with operations and only 9.7% of the total population received antibiotic therapy. Unindicated use of antibiotics contributes to the emergence and spread of multidrug-resistant bacteria, which are becoming a growing problem in healthcare facilities. Antibiotics should only be given during operations and their administration should not be prolonged in the NICU. During the prophylactic use of antibiotics it is essential not only to keep to the indication, but also to maintain the time of administration. However, this study confirmed that antibiotic prophylaxis policy is an important task, because antibiotic prophylaxis was found to be a predictor of nosocomial infection in the neurocritical care population. While using antibiotics, it is essential to maintain the correct administration and not use antibiotics during the colonisation of the patient, but only for the infection. Timing, dosage and tissue penetration are important in their administration.

Our microbiological screening was the same for all patients, who can therefore be compared easily. The unified system included nose, throat, trachea, skin, urine and rectum tests from admission, so that we would know what the patient was admitted with, and then regularly every three days. This means that this microbiological screening sometimes fell on the weekend, which at first was difficult to implement in the microbiological department. Regular microbiological screening from admission took place every three days, giving us an overview of the microbiological state of the patient and allowing us to find colonization of multidrug-resistant bacteria [18] and further perform the targeted antibiotic treatment of nosocomial infections.

Although it would be better to have single-patient boxes, the lay-out of four divided rooms provides some of the benefits and enables the isolation of patients with multidrug-resistant bacteria ESBL and MRSA, as it is very important to isolate these patients so that these bacteria do not spread to the rest of the NICU and the other patients. Our results show that over a ten-year period we did not have a large incidence of the multidrug-resistant bacteria ESBL and MRSA, while there was not a single case of VRE. This is in contrast to the Minhas [19] study, where he mentioned 2.5% of VRE in the neurosurgical and neurological intensive care unit.

This study confirmed that accesses are still a risk factor for nosocomial infection. Due to increasing numbers of invasive medical procedures in neurocritical care, local preventive infection control management has an important task. Although preventive multimodal strategy is widely known to reduce nosocomial infection and multidrug resistant bacteria, it is sometimes difficult to maintain. Nonetheless, the results of this study show the importance of this maintenance. We present our 10 year prospective infection control management, which was efficient, as it led to a rate of 4.4% nosocomial infections in acute neurological and neurosurgical care patients. Due to multiple testing, there is a higher probability of family-wise error. On the other hand, the results must be read in context, not every p-value below 0.05 is commented on as a finding.

This study showed prospective infection control management in 3464 neurocritically care patients. Although they all came from a single neurocentre, which is a limitation of this study, there are already many more epidemiologic studies regarding nosocomial infection control and multi-drug resistant bacteria from the medical and surgery intensive care units than from neurocritical care units, whether neurosurgical or neurological, and very few studies concerned with neurological-neurosurgical critical care units [19, 20]. In this area, more studies focus on specific diagnoses [1, 2, 7, 21, 22] than whole neurocritical care populations.

Conclusions

This study showed that this preventive multimodal nosocomial infection control management was efficient, because it gave low rates of nosocomial infections (4.2%), both ESBL and MRSA in a mere 0.9% of patients each and not a single case of VRE. Strong predictors for the onset of nosocomial infections were accesses such as airways and urine catheters, NICU stay, antibiotic prophylaxis, wound complications and transfusion. This study confirmed the well-known fact that nosocomial infections are associated with worse outcome, higher cost and longer NICU stay.

Abbreviations

APACHE: 

Acute Physiology and Chronic Health Evaluation

ASA: 

American Society of Anesthesiologists

ATB: 

antibiotic

BMI: 

body mass index

CRP: 

C-reactive protein

ESBL: 

Extended spectrum beta-lactamase

ETT: 

endotracheal tube

GCS: 

Glasgow Coma Scale

GOS: 

Glasgow Outcome Scale

ICH: 

intracerebral haemorrhage

MRSA: 

Methicillin-resistant Staphylococcus aureus

NI: 

nosocomial infection

NICU: 

neurointensive care unit

SAH: 

subarachnoid haemorrhage

STSP: 

Staphylococcus species

TISS: 

Therapeutic Intervention Scoring System

TST: 

tracheostomy tube

VRE: 

Vancomycin-resistant enterococcus

Declarations

Acknowledgement

We thank the translator and native English speaker Henry Morgan (BA honours) for the correction of the English text. This study was published as an abstract of the 23rd annual congress of the European Society of Intensive Care Med Experimental 2016;4(S1):426.

Funding

This study was supported by grants from the Scientific Board of the hospital, number VR 140312.

Availability of data and materials

The datasets obtained during this study are available from the corresponding author on reasonable request.

Authors’ contributions

VS, OB, DF, ZB, PS: revising it critically for important intellectual content, final approval of the manuscript, read and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. VS: conception and design, acquisition of data, interpretation of data; drafting the manuscript, OB: statistical analysis, interpretation of data, DF, ZB: acquisition of data, interpretation of data. PS: conception.

Ethics approval and consent to participate

The study was approved by the Liberec hospital Ethics Committees for Multicentric Clinical Trials (č.j. EK27/2008). All participants gave written informed consent prior to all measurements and agreed upon publication.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Neurocenter, Neurointensive Care Unit, Regional Hospital, Husova 357/10, Regional Hospital, 46063 Liberec, Czech Republic
(2)
Department of Neurosurgery, Military University Hospital and First Medical School, Charles University, Prague, Czech Republic
(3)
Department of Clinical microbiology and immunology, Antibiotic Centre, Regional Hospital, Liberec, Czech Republic
(4)
Neurocenter, Department of Neurosurgery, Regional Hospital, Liberec, Czech Republic

References

  1. Zygun DA, Zuege DJ, Boiteau PJ, Laupland KB, Henderson EA, Kortbeek JB, Doig CJ. Ventilator-associated pneumonia in severe traumatic brain injury. Neurocrit Care. 2006;5:108–14.View ArticlePubMedGoogle Scholar
  2. Murthy SB, Moradiya Y, Shah J, Merkler AE, Mangat HS, Iadacola C, et al. Nosocomial Infections and Outcomes after Intracerebral Hemorrhage: A Population-Based Study. Neurocrit Care. 2016;25:178–84.View ArticlePubMedGoogle Scholar
  3. Foreman PM, Chua M, Harrigan MR, Fisher WS 3rd, Vyas NA, Lipsky RH, Walters BC, Tubbs RS, Shoja MM, Griessenauer CJ. Association of nosocomial infections with delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2016;125:1383–9.View ArticlePubMedGoogle Scholar
  4. Westendorp WF, Nederkoorn PJ, Vermeij JD, Dijkgraaf MG, van de Beek D. Post-stroke infection: a systematic review and meta-analysis. BMC Neurol. 2011;11:110.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Bronchard R, Albaladejo P, Brezac G, Geffroy A, Seince PF, Morris W, et al. Early onset pneumonia: risk factors and consequences in head trauma patients. Anesthesiology. 2004;100:234–9.View ArticlePubMedGoogle Scholar
  6. Bassetti M, De Waele JJ, Eggimann P, Garnacho-Montero J, Kahlmeter G, Menichetti F, et al. Preventive and therapeutic strategies in critically ill patients with highly resistant bacteria. Intensive Care Med. 2015;41:776–95.View ArticlePubMedGoogle Scholar
  7. Ohwaki K, Yano E, Nagashima H, Nakagomi T, Tamura A. Impact of infection on length of intensive care unit stay after intracerebral hemorrhage. Neurocrit Care. 2008;8:271–5.View ArticlePubMedGoogle Scholar
  8. Josephson SA, Moheet AM, Gropper MA, Nichols AD, Smith WS. Ventilator-associated pneumonia in a neurologic intensive care unit does not lead to increased mortality. Neurocrit Care. 2010;12:155–8.View ArticlePubMedGoogle Scholar
  9. Chen YY, Chou YC, Chou P. Impact of nosocomial infection on cost of illness and length of stay in intensive care units. Infect Control Hosp Epidemiol. 2005;26:281–7.View ArticlePubMedGoogle Scholar
  10. Higgins TL, McGee WT, Steingrub JS, Rapoport J, Lemeshow S, Teres D. Early indicators of prolonged intensive care unit stay: impact of illness severity, physician staffing, and pre-intensive care unit length of stay. Crit Care Med. 2003;31:45–51.View ArticlePubMedGoogle Scholar
  11. Halperin JJ, Moran S, Prasek D, Richards A, Ruggiero C, Maund C. Reducing Hospital-Acquired Infections Among the Neurologically Critically Ill. Neurocrit Care. 2016;25:170–7.View ArticlePubMedGoogle Scholar
  12. Traa MX, Barboza L, Doron S, Snydman DR, Noubary F, Nasraway SA Jr. Horizontal infection control strategy decreases methicillin-resistant Staphylococcus aureus infection and eliminates bacteremia in a surgical ICU without active surveillance. Crit Care Med. 2014;42:2151–7.View ArticlePubMedGoogle Scholar
  13. Morgan DJ, Rogawski E, Thom KA, Johnson JK, Perencevich EN, Shardell M, et al. Transfer of multidrug-resistant bacteria to healthcare workers' gloves and gowns after patient contact increases with environmental contamination. Crit Care Med. 2012;40:1045–51.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Kollef MH, Micek ST. Antimicrobial stewardship programs: mandatory for all ICUs. Crit Care. 2012;16:179.View ArticlePubMedPubMed CentralGoogle Scholar
  15. Rimawi RH. Just Say "Stop": Avoiding Prolonged Empiric Antibiotics. Crit Care Med. 2015;43:2675–6.View ArticlePubMedGoogle Scholar
  16. Ziakas PD, Anagnostou T, Mylonakis E. The prevalence and significance of methicillin-resistant Staphylococcus aureus colonization at admission in the general ICU Setting: a meta-analysis of published studies. Crit Care Med. 2014;42:433–44.View ArticlePubMedGoogle Scholar
  17. Ziakas PD, Zacharioudakis IM, Zervou FN, Mylonakis E. Methicillin-resistant Staphylococcus aureus prevention strategies in the ICU: a clinical decision analysis*. Crit Care Med. 2015;43:382–93.View ArticlePubMedGoogle Scholar
  18. Sarikonda KV, Micek ST, Doherty JA, Reichley RM, Warren D, Kollef MH. Methicillin-resistant Staphylococcus aureus nasal colonization is a poor predictor of intensive care unit-acquired methicillin-resistant Staphylococcus aureus infections requiring antibiotic treatment. Crit Care Med. 2010;38:1991–5.View ArticlePubMedGoogle Scholar
  19. Minhas P, Perl TM, Carroll KC, Shepard JW, Shangraw KA, Fellerman D, et al. Risk factors for positive admission surveillance cultures for methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci in a neurocritical care unit. Crit Care Med. 2011;39:2322–9.View ArticlePubMedGoogle Scholar
  20. Dettenkofer M, Ebner W, Els T, Babikir R, Lucking C, Pelz K, et al. Surveillance of nosocomial infections in a neurology intensive care unit. J Neurol. 2001;248:959–64.View ArticlePubMedGoogle Scholar
  21. Divani AA, Hevesi M, Pulivarthi S, Luo X, Souslian F, Suarez JI, et al. Predictors of nosocomial pneumonia in intracerebral hemorrhage patients: a multi-center observational study. Neurocrit Care. 2015;22:234–42.View ArticlePubMedGoogle Scholar
  22. Hilker R, Poetter C, Findeisen N, Sobesky J, Jacobs A, Neveling M, et al. Nosocomial pneumonia after acute stroke: implications for neurological intensive care medicine. Stroke. 2003;34:975–81.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s). 2018

Advertisement