Influence of Ward Environments on External Ventricular Drain Infections: A Retrospective Risk Factor Analysis

Abstract

Background:

Ventriculostomy-related infection (VRI) is one of the most severe and common complications of external ventricular drains (EVD). Ward environment is closely related to hospital-acquired infection, but its role in EVD infection is unclear. For some other recognized risk factors, clinical evidence also remains complicated and undetermined. We aimed to evaluate ward environment including multi-bed accommodation and intensive care unit (ICU) stay as potential risk factors for VRI, as well as to confirm those already known factors.

Methods:

We reviewed EVDs retrospectively in our center between January 2012 and January 2017. Univariable and logistic regression analysis were performed to identify risk factors for EVD-related infection.

Results:

A total of 284 patients who underwent EVD procedure were included. Thirty-six (12.7%) developed EVD-related infection. Univariable analysis revealed that the infection group had longer intensive care unit (ICU) stay (6.81 vs. 3.65 days, p = 0.045) but multi-bed accommodation showed no statistical difference between the two groups (p = 0.404). Univariable analysis also showed VRI patients had lower pre-operational Glasgow Coma Scale (6.89 vs. 9.32, p = 0.001), longer drainage placement duration (11.4 vs. 8.30 days, p < 0.001), greater numbers of cerebrospinal fluid (CSF) sampling (3.89 vs. 1.73, p < 0.001), higher percentage of pre-operational artificial airway status (50.0% vs. 18.1%, p < 0.001), and higher percentage of intracranial hemorrhage diagnosis (88.9% vs. 73.8%, p = 0.048). Logistic regression analysis demonstrated longer post-operational ICU stay (>5 days, odds ratio [OR] = 3.21, p = 0.026) as independent risk factor for EVD-related infection. Other independent risk factors included CSF sampling counts (>3, OR = 5.14, p <0.001), EVD duration (>7 days, OR = 3.85, p = 0.028), and pre-operational artificial airway status (OR = 2.85, p = 0.038).

Conclusions:

Longer post-operational ICU stay, frequent CSF sampling, longer duration of EVD placement, and pre-operational intubation are independent risk factors for EVD infection. Multi-bed accommodation and bilateral EVD placement have no substantial influence on VRI risk.

External ventricular drains are used commonly in neurosurgical practices. External ventricular drain (EVD) placement is often lifesaving but can also cause complications. One of the most severe and common complications of EVD is ventriculostomy-related infection (VRI). Reported VRI rates vary from 0% to more than 40% based on different diagnosis criteria [1,2].

The risk of VRI has been followed with interest for decades. Recognized risk factors include duration of EVD placement, and prophylactic options include one dose of antimicrobial agents prior to EVD insertion, antimicrobial-impregnated catheters, avoiding routine cerebrospinal fluid (CSF) sampling, early removal, and limiting manipulation of the closed system [3]. However, there are still potential factors lacking enough research such as bilateral EVDs and ward environments [4,5].

Ward environments rarely had been taken into consideration. In our country, up to six patients could share the same room. Multi-bed accommodation often means more care providers and visitors in a given area, and might increase hospital-acquired infection risk [6,7]. When it came to VRI events, only one study specifically discussed multi-bed bays (up to four-bed bays) to the best of our knowledge [5]. Moreover, post-surgery ICU stay is often required for neurosurgical patients. Compared with a common ward, whether prolonged ICU stay could be a potential risk factor also remains unclear and evidence is inconsistent [5,8]. Therefore, in this study, we analyzed ward environments including multi-bed accommodation and prolonged ICU stay as well as other known risk factors to provide novel and further clinical evidence for the prevention of VRI events.

Patients and Methods

Patient population

This retrospective study included patients who had EVDs in The First Affiliated Hospital, College of Medicine, Zhejiang University, from January 2012 to January 2017. Exclusion criteria included: age of younger than 18 years old; already diagnosed as intracranial infection before the surgery; and died, auto-discharged, or transferred to other hospitals within 72 hours after the surgery. The study was in keeping with the ethical standards of the 1964 Declaration of Helsinki and its later amendments.

Auto-discharged here means when the patient is entering the terminal stage, the patient or his/her legal representative (if the patient is unconscious) decides to transfer to a local terminal care facility and gives up further active and invasive treatment. Because of traditional culture and religious reasons, many people in our district would insist that their beloved ones spend their last days in their hometown.

External ventricular drain procedure details

In this study, plain catheters (not silver or antibiotic impregnated) were used in all cases, and short tunnel procedure were followed [9,10]. All operations were done in operating theaters. Antibiotic agents were given only perioperatively for prevention purposes, unless VRI or other infections were suspected. In concordance with our hospital infection control policy, cefuroxime would be given once before the surgery and continued for 24 to 48 hours after the surgery. The exact duration was decided by the primary neurosurgeon team. When contraindications (such as allergy) existed, alternative antibiotic agents would be utilized. Post-operatively patients went to either the ICU or neurosurgical wards, which include four different environments: six-bed bays, three-bed bays, two-bed bays, or single rooms. Patients were isolated by curtains installed on the ceiling in multi-bed rooms.

Cerebrospinal fluid sampling was performed only when infection was suspected, or CSF oncology tests were required for patients with tumors. The catheters would be clamped temporarily during the process. Hygiene procedure of the hands was followed before and after handling the drainage. Gloves, masks, and hats were used for the process. Daily dressings were performed; povidone iodine and alcoholic chlorhexidine were used for the cleansing of the incision area. Catheters would be replaced only if violation of drainage integrity was confirmed.

Definition of infection

Based on U.S. Centers for Disease Control and Infection/National Healthcare Safety Network (CDC/NHSN) surveillance definitions and previous reviews [2,11,12], we defined VRI as: organisms cultured from CSF or at least one sign or symptom of ventriculitis plus increased white cells (>300*10⁹/L, with higher apocyte ratio than monocyte ratio), elevated protein, and decreased glucose in CSF. All VRI patients in this study were diagnosed independtly by both neurosurgeons and infectious disease specialists.

Data collection

Collected data included age, gender, height, weight, medical history, American Society of Anesthesiologists (ASA) Score [13], pre-operative diagnosis, best Glasgow Coma Scale (GCS) within 24 hours of the procedure, pre-operational airway status, operation duration and category (bilateral or unilateral EVD placement), post-operational accommodation, ICU stay duration, EVD duration, total sampling count, duration intubation or tracheotomy, CSF chemistry, and CSF culture results.

Statistical analysis

Statistical analysis was performed with SPSS version 19.0 (IBM Corp, Armonk, NY). Continuous variables are given as means and standard deviations. Student t-test was performed to compare continuous variables if they were normally distributed and Mann-Whitney U test was performed if the distribution was not normal. Categorical variables are given as numbers and percentages (with 95% confidence intervals [CI]). To compare categorical variables, χ² tests were used. Based on the univariable analysis results, marginal (p < 0.10) or statistically significant factors were included in binary logistic regression analysis to identify risk factors for VRI events. Statistical significance was determined when p < 0.05.

Results

Baseline characteristics

We screened a total of 390 patients who had EVDs and included 284 (Fig. 1). Baseline data are summarized in Table 1. Among all 284 patients, 19 (6.7%) were admitted to single-bed rooms after surgery; 22 (7.7%) were admitted to two-bed rooms; 106 (37.3%) were admitted to three-bed rooms; and 137 (48.2%) were admitted to six-bed rooms. There were 166 (58.5%, 95% CI = 52.7%–64.2%) male patients. Mean age was 55.0 ± 15.7 years. Two hundred fifteen patients (75.7%, 95% CI = 70.7%–80.7%) had EVDs for intracranial hemorrhage (ICH). The most common medical issues were hypertension (126 patients, 44.4%, 95% CI = 38.6%–50.2%) and cerebrovascular disease (73 patients, 25.7%, 95% CI = 20.6%-30.8%). There were 149 patients (52.5%, 95% CI = 46.6%–58.3%) with GCS ≤8. Sixty-three patients (22.2%, 95% CI = 17.3%–27.0%) had already been intubated prior to the EVD placement. Seventy-eight patients (27.5%, 95% CI = 22.2%–32.7%) underwent bilateral EVD procedures. The mean operative duration was 1.01 ± 0.87 hours for the 136 patients (47.9%, 95% CI = 42.0%–53.7%) who underwent isolated EVD procedures. The other 148 patients (52.1%, 95% CI = 46.3%–58.0%) underwent combined procedures with mean operation durations of 5.06 ± 2.06 hours. After EVDs were placed, the mean drainage duration was 8.70 ± 4.75 days and the total counts of CSF sampling were 2.00 ± 1.98 times. The mean duration of ICU stay was 4.05 ± 6.85 days.

FIG. 1.

Flow chart showing the recruitment of patients with external ventricular drains (EVDs). We screened a total of 390 patients with EVDs from 2012 to 2017. Three patients underwent EVD procedures before being admitted to our center; 103 patients met the exclusion criteria. A total of 284 patients were finally included in the study.

Table 1.

Patient Characteristics

Characteristic	Value
Number of patients	284
Gender, n (%)
Male	166 (58.5%)
Female	118 (41.5%)
Age, mean ± SD (y)	55.0 ± 15.7
Pre-operational diagnosis included, n (%)
ICH	215 (75.7%)
TBI	31 (10.9%)
Intracranial tumor	60 (21.1%)
Cerebral infarction	13 (4.6%)
Medical history, n (%)
Hypertension	126 (44.4%)
Diabetes mellitus	22 (7.7%)
Cardiovascular disease	19 (6.7%)
Cerebrovascular disease	73 (25.7%)
Pre-operational GCS, mean ± SD	8.99 ± 4.72
GCS ≤8, n (%)	149 (52.5%)
Pre-operational artificial airway status, n (%)	63 (22.2%)
ASA score, mean ± SD	3.71 ± 1.72
EVD procedure, n (%)
Unilateral	206 (72.5%)
Bilateral	78 (27.5%)
Combined surgery, n (%)
EVD placement only	136 (47.9%)
Combined surgery	148 (52.1%)
Surgery duration, mean ± SD (h)
EVD placement only	1.01 ± 0.87
Combined surgery	5.06 ± 2.06
All cases	3.15 ± 2.56
Drainage duration, mean ± SD (d)	8.70 ± 4.75
CSF sampling, mean ± SD (times)	2.00 ± 1.98
ICU stay, mean ± SD (d)	4.05 ± 6.85
Post-surgery artificial airway status, mean ± SD (d)	9.68 ± 17.3
Accommodation, n (%)
One-bed room	19 (6.7%)
Two-bed room	22 (7.7%)
Three-bed room	106 (37.3%)
Six-bed room	137 (48.2%)
Patients developed VRI, n (%)	36 (12.7%)

SD = standard deviation; TBI = traumatic brain injury; ICH = intracranial hemorrhage; GCS = Glasgow Coma Scale; EVD = external ventricular drain;

VRI = ventriculostomy-related infection; ASA = American Society of Anesthesiologists.

General information for EVD-related infection

Thirty-six patients (12.7%) had confirmed VRIs. Among them, 14 had positive CSF culture results (Table 2). The most common pathogen was Acinetobacter baumanii, which was found in five CSF samples.

Table 2.

Responsible Pathogens for EVD-Related Infection

Pathogen	n
Acinetobacter baumanii	5
Staphylococcus spp.
MRSA	1
Staphylococcus epidermidis	2
Streptococcus spp.
Viridans streptococci	2
Streptococcus sanguinis	1
Pseudomonas aeruginosa	2
Blastomyces dermatitidis	1
Total	14^a

The number of patients with positive culture results is 14 and the rest 22 VRI patients had negative CSF culture results.

EVD = external ventricular drain; MRSA = methicillin-resistant Staphylococcus aureus; VRI = ventriculostomy-related infection; CSF = cerebrospinal fluid.

Risk factors for EVD infection

To evaluate the influence of ward environments on EVD infection, we compared the percentage of different ward types between infection and non-infected groups (11.1% vs. 6.0% for one-bed room, 5.6% vs. 8.1% for two-bed room, 27.8% vs. 38.7% for three-bed room, and 55.6% vs. 47.2% for three-bed room), and the overall data showed no statistical difference (p = 0.404). On the other hand, the ICU stay of the infection group was much longer in univariable analysis (6.81 vs. 3.65 days, p = 0.045) as presented in Table 3. Furthermore, after including marginal (p < 0.10) or statistically significant factors in univariable analysis into logistic regression model, it was demonstrated that longer post-operational ICU stay (>5 days, OR = 3.21, p = 0.026) should be considered as an independent risk factor for EVD infection. Logistic regression analysis is shown in Table 4.

Table 3.

Influence of Ward Environments on EVD-Related Infection

Characteristic	EVD infection	No EVD infection	p
Number of patients	36	248
ICU stay, mean ± SD (d)	6.81 ± 8.79	3.65 ± 6.44	0.045
Accommodation, n (%)			0.404
One-bed room	4 (11.1%)	15 (6.0%)
Two-bed room	2 (5.6%)	20 (8.1%)
Three-bed room	10 (27.8%)	96 (38.7%)
Six-bed room	20 (55.6%)	117 (47.2%)

EVD = external ventricular drain; ICU = intensive care unit; SD = standard deviation.

Table 4.

Logistic Regression Analysis of Risk Factors for EVD-Related Infection

Factors	β	Standard error	p	OR	95% CI
Pre-operational artificial airway status	1.048	0.506	0.038	2.851	1.057–7.688
Pre-operational GCS (≤8)	0.113	0.538	0.834	1.119	0.390–3.214
Drainage duration (>7 d)	1.349	0.612	0.028	3.854	1.161–12.797
CSF sampling (>3 times)	1.637	0.433	<0.001	5.140	2.200–12.008
ICU stay (>5 d)	1.166	0.525	0.026	3.209	1.147–8.980
ICH positive	0.308	0.622	0.621	1.360	0.402–4.604
ASA score (>3)	0.144	0.545	0.792	1.155	0.396–3.363
Post-operational artificial airway status (≥7 d)	−0.550	0.558	0.324	0.577	0.193–1.722

EVD = external ventricular drain; GCS = Glasgow Coma Scale; CSF = cerebrospinal fluid; ICU = intensive care unit; ICH = intracranial hemorrhage; ASA = American Society of Anesthesiologists.

Other univariable analysis results are presented in Table 5. The infected group had lower pre-operational GCS (6.89 vs. 9.32, p = 0.001), longer drainage placement duration (11.4 vs. 8.30 days,p <0.001) and higher CSF sample counts (3.89 vs. 1.73,p <0.001). More VRI patients were at artificial airway status (50.0% vs. 18.1%, p < 0.001) or diagnosed as ICH (88.9% vs. 73.8%, p = 0.048) before the surgery.

Table 5.

Univariable Analysis of Risk Factors for EVD-Related Infection

Characteristic	EVD infection	No EVD infection	p
Number of patients	36	248
Gender, n (%)			0.729
Male	22 (61.1%)	144 (58.1%)
Age, mean ± SD (y)	53.1 ± 14.7	55.2 ± 15.9	0.448
Pre-operational GCS, mean ± SD	6.69 ± 3.87	9.32 ± 4.75	0.001
ASA score, mean ± SD	4.00 ± 0.99	3.67 ± 1.14	0.068
Pre-operational diagnosis included, n (%)
ICH	32 (88.9%)	183 (73.8%)	0.048
TBI	4 (11.1%)	27 (10.9%)	0.968
Intracranial tumor	4 (11.1%)	56 (22.6%)	0.115
Cerebral infarction	1 (2.8%)	12 (4.8%)	0.580
Medical history, n (%)
Hypertension	13 (36.1%)	113 (45.6%)	0.286
Diabetes mellitus	3 (8.3%)	19 (7.7%)	0.888
Cardiovascular disease	1 (2.8%)	18 (7.3%)	0.315
Cerebrovascular disease	8 (22.2%)	65 (26.2%)	0.609
Tumor of other systems	2 (5.6%)	17 (6.9%)	0.771
Pre-operational artificial airway status, n (%)	18 (50.0%)	45 (18.1%)	< 0.001
Surgery duration, mean ± SD (h)	3.10 ± 2.09	3.15 ± 2.62	0.902
Unilateral or bilateral EVD procedure, n (%)			0.964
Unilateral	26 (72.2%)	180 (72.6%)
Drainage duration, mean ± SD (d)	11.4 ± 4.50	8.30 ± 4.67	< 0.001
CSF sampling, mean ± SD (times)	3.89 ± 2.14	1.73 ± 1.80	< 0.001
Post-surgery artificial airway status, mean ± SD (d)	14.7 ± 19.3	8.95 ± 16.9	0.062
Combined surgery or EVD placement only, n (%)			0.932
EVD placement only	17 (47.2%)	119 (48.0%)

EVD = external ventricular drain; SD = standard deviation; GCS = Glasgow Coma Scale; ASA = American Society of Anesthesiologists; ICH = intracranial hemorrhage; TBI = traumatic brain injury. CSF = cerebrospinal fluid.

Bilateral operations, combined surgery and operation duration showed no association with infection rate. There were no differences in age, gender, medical history (hypertension, diabetes mellitus, cardiovascular or cerebrovascular disease, and tumor of other system), ASA score, or post-operational artificial airway status between VRI and non-VRI groups.

Apart from prolonged ICU stay, logistic regression analysis also demonstrated that frequent CSF sampling (>3, OR = 5.14, p < 0.001), longer duration of EVD placement (>7 days, OR = 3.85, p = 0.028) and pre-operational artificial airway status (OR = 2.85, p = 0.038) could be independent risk factors for EVD-related infection. Lower GCS (GCS ≤8, p = 0.843), higher ASA score (> 3, p = 0.792), longer post-operational artificial airway status (≥ 7 days, p = 0.324), and diagnosis of ICH (p = 0.621) showed no statistical significance in logistic regression model. These logistic regression analysis results are presented in Table 4.

Discussion

Our overall incidence of EVD infection was 12.7%. Given the broad definition of infection used and the fact that neither silver nor antimicrobial-impregnated catheters [14] were available in our district of China, our rate was reasonable and comparable with previous studies [3,5,15 –17].

Ward environment is regularly mentioned in hospital-acquired infection control discussion, but clinical data of specific infection type such as VRI are limited. Multi-bed accommodation is common worldwide and six-bed bays or even more crowded ward environments can be found in developing countries. Our data showed multi-bed bays did not contribute to VRI risk. This result is similar to the previous study in 2014, which mentioned the influence of multi-bed accommodation, and found no substantial difference in the VRI rate [5]. These results indicate that with valid prevention measures, multi-bed bays may not increase the risk of EVD infection events.

Compared with multi-bed accommodation, evidence related to ICU stay is easier to find but remains inadequate and inconsistent. Kim et al. [11] listed 17 studies from 2000 to 2008 among which three mentioned ICU stay [18 –20]. Hagel et al. [5] reported substantially longer ICU stay in VRI patients (21 days vs. 11 days, p < 0.01), however, another study found no differences in ICU stay or ward stay between the VRI and non-infected groups [8]. Our study identified ICU stay duration longer than five days as an independent risk factor. Naturally, longer ICU stay is often considered as an outcome of infection and given the retrospective nature of our study, a causal inference should not be drawn from this result.

Apart from ward environments, we also examined CSF sampling count, EVD duration, GCS, pre-operative airway status, bilateral EVD placement, and ICH diagnosis as potential risk factors. Cerebrospinal fluid sampling count has been repeatedly studied and its role remains uncertain. The 2016 consensus statement suggested avoiding routine CSF sampling but did not hold the practice unreasonable [3]. In 2014, Williamson et al. [21] reported higher risk of VRI for each CSF sample. More recently Thompson et al. [16] found increased sampling did not raise the risk of infection. In another recent study, Champey et al. [22] suggested that an EVD care bundle including routine daily CSF sampling could lower the risk of infection. In our study, higher sample counts were identified to be related to increase VRI risk.

Duration of EVD placement has been well accepted to be a risk factor for EVD-related infection although cause-and-effect relation has not been determined [3]. The consensus statement suggested removing EVD device as soon as possible. The different studies used non-uniformed definitions of VRI and methodologies that undoubtedly contributed to the heterogeneity of results [18,19,23]. Our study showed an increased infection risk with longer duration of EVD placement. It should be noted that studies showing unchanged or lower risk after seven days also exist [3].

Intracranial hemorrhage is one of the most common indications for EVDs. Some previous studies had reported subarachnoid or intraventricular hemorrhage as risk factors whereas others failed to confirm subarachnoid cases [24 –27]. In a more recent study, Dos Santos et al. [28] reported a 36.2% overall EVD infection rate in spontaneous intracerebral hemorrhage patients that was much higher than typical EVD infection rates. Our study found no influence of intracerebral hemorrhage on VRI infection.

Glasgow Coma Scale and pre-operative intubation are both correlated with patients' general state. The GCS has rarely been used to predict EVD-related infection. Muttaiyah et al. [29] reported in 2008 that GCS did not allow early prediction of VRI events. Our data did not support pre-operative GCS as VRI risk factor either. Pre-operative intubation status closely correlates to GCS, but to our knowledge, there were no previous studies looking at intubation status. We performed logistic regression analysis and identified pre-operational intubation as an independent risk factor, which reminded us that pre-operational intubation status might indicate an even worse basal condition of the patient.

Bilateral EVD placement is another possible risk factor for VRI. A recent study found that among patients with low modified Graeb scores, bilateral EVDs could contribute to higher VRI risk [4]. In contrast, our data showed similar risk between the bilateral and unilateral procedures. Because the present study is single-center and retrospective, selection bias as well as limited generalizability and sample volume might potentially affect the effectiveness of the data.

Conclusions

Longer post-operational ICU stay, frequent CSF sampling, longer duration of EVD placement, and pre-operational intubation are independent risk factors for EVD infection. Multi-bed accommodations and bilateral EVD placement have no substantial influence on VRI risk.

Footnotes

Funding Information

No funding was received for this research.

Author Disclosure Statement

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest, or non-financial interest in the subject matter or materials discussed in this article.

Formal consent was not required for this study. The study was in keeping with the ethical standards of the 1964 Declaration of Helsinki and its later amendments.

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