Nosocomial Pneumonia After Acute Stroke

Implications for Neurological Intensive Care Medicine

Ruediger Hilker, MD; Carsten Poetter, MD; Nahide Findeisen, MD; Jan Sobesky, MD;
Andreas Jacobs, MD; Michael Neveling, MD; Wolf-Dieter Heiss, MD

Background and PurposePneumonia has been estimated to occur in about one third of patients after acute stroke. Only
limited data are available on stroke-associated pneumonia (SAP) in specialized neurological intensive care units
(NICUs).
MethodsWe enrolled 124 patients with acute stroke who were treated at our university hospital NICU in a prospective
observational study. Incidence rates and risk factors of SAP and long-term clinical outcome were determined.
ResultsSAP incidence was 21% with a spectrum of pathogens, which is comparable to previously published data on
general ICU patients. Mechanical ventilation, multiple location, and vertebrobasilar stroke, as well as dysphagia and
abnormal chest x-ray findings, were identified as risk factors for the disease. SAP patients showed higher mortality rates
than nondiseased subjects (acute, 26.9% versus 8.2%; long-term, 35.3% versus 14.3%) and a significantly poorer
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017

long-term clinical outcome (Barthel Index, 50.542.4 versus 81.527.8; Rankin Scale, 3.51.7 versus 2.21.6).
ConclusionsOur data underline the considerable epidemiological and prognostic impact of SAP for the treatment of
acute stroke patients in a specialized NICU setting. They demonstrate that the occurrence of SAP deteriorates clinical
outcome in these patients. Our results allow us to identify high-risk stroke patients at time of NICU admission in whom
the use of preventive treatment strategies is most promising. (Stroke. 2003;34:975-981.)
Key Words: intensive care units pneumonia stroke

T he overall prognosis of patients with acute ischemic brain

infarction is crucially dependent on the occurrence of
medical complications in the course of the disease that have
stroke and stroke-associated pneumonia (SAP) in patients
treated in an NICU in a university hospital setting.

been found to occur in 59% of stroke patients, leading to
death in up to 23% during the hospital stay.1 Among them,
nosocomial infections have been estimated to develop in
about one third of patients with acute stroke, most commonly
affecting the urinary tract and the lungs.2,3
As a result of recent advances in stroke treatment, an
increasing number of patients are treated nowadays in spe-
cialized wards, eg, stroke units or neurological intensive care
units (NICUs). Note that the highest incidence and mortality
rates of pneumonia are observed in ICUs, where 10% to
25% of patients develop the disease.4 6 Therefore, these
treatment settings imply certain infectious risks that are
closely associated with intensive care medicine in general,5,7
despite their undoubted benefits for stroke patients.
Only limited data are currently available on infection after
acute ischemic stroke8 and incidence rates of nosocomial
infections in NICUs.9,10 A prospective study investigating the
association of pneumonia and acute stroke as the infectious
and neurological diseases with highest prevalence rates is still
lacking. Therefore, we focused on the coincidence of acute
Subjects and Methods
Study Population
We performed a prospective observational study of consecutive
patients with acute stroke who were admitted to the NICU of the
Neurology Department at Cologne University Hospital over a 1-year
period. The NICU has 9 beds and an annual inpatient count of 500
patients with 1200 ventilator days per year. The presence of acute
stroke was defined in all patients in whom the time interval between
symptom onset and NICU treatment was 24 hours and in whom the
ischemic brain lesion was clearly visible in cerebral CT or MRI. Data
on all acute stroke patients with an NICU stay of at least 24 hours
were collected.
Surveillance and Data Collection
A daily surveillance of the study subjects was performed by 4 trained
and experienced clinicians (R.H., J.S., M.N., A.J.) from time of
admission to 48 hours after NICU discharge. Each patient was
followed up by the same observer over the entire study period. One
infection control practitioner (C.P.) attended the NICU every 1 to 2
weeks for supervision. Study records were kept on distinct data
sheets. On admission, history of lung and heart diseases and
cerebrovascular risk factors were recorded. Clinical scores for
general disease severity (Acute Physiology and Chronic Health

Received May 3, 2002; final revision received October 18, 2002; accepted November 4, 2002.
From the Departments of Neurology (R.H., N.T., J.S., A.J., M.N., W.-D.H.) and Hospital Infection Control (C.P.), University Hospital, Cologne,
Germany.
Correspondence to Prof Dr Wolf-Dieter Heiss, Department of Neurology, University Hospital, Joseph-Stelzmann-Strasse 9, D-50924 Cologne,
Germany. E-mail wdh@pet.mpin-koeln.mpg.de
2003 American Heart Association, Inc.
Stroke is available at http://www.strokeaha.org DOI: 10.1161/01.STR.0000063373.70993.CD

975
 976 Stroke April 2003

TABLE 1. SAP Risk Factors and Stroke Location in 124 Patients With and
Without SAP Who Have Been Treated in an NICU
SAP* Non-SAP*
Patient characteristics (n26) (n98) RR 95% CI P
SAP risk factors
Dysphagia 14 (53.8) 22 (22.4) 4.74 1.8012.45 0.000
MV 14 (53.8) 3 (3.1) 7.34 4.1313.07 0.000
Abnormal chest x-ray 18 (69.2) 29 (29.6) 4.05 1.838.95 0.001
Stroke location
MCA I (33%) 3 (11.5) 43 (43.9) 0.22 0.070.70 0.002
MCA II (3366%) 2 (7.7) 18 (19.4) 0.43 0.111.69 0.188
MCA III (66%) 8 (30.8) 15 (15.3) 1.95 0.973.93 0.071
ACA 0 (0.0) 2 (2.0) N/A N/A 0.460
PCA 1 (3.8) 7 (7.1) 0.58 0.903.75 0.543
Brain stem 2 (7.7) 6 (6.1) 1.21 0.354.23 0.772
Cerebellum 1 (3.8) 4 (4.1) 0.95 0.165.69 0.957
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017

Multiple hemispheric stroke 4 (15.4) 3 (3.1) 3.04 1.446.39 0.016

Multiple vertebrobasilar stroke 5 (19.2) 0 (0.0) 5.67 3.848.35 0.000
Vertebrobasilar stroke 8 (30.8) 10 (10.2) 3.91 1.3611.28 0.008
ACA indicates anterior cerebral artery; PCA, posterior cerebral artery.
*Data are expressed as total number (percentage proportion) of all stroke patients in that group.
Between-group comparison between SAP and non-SAP subjects with 2 test or Fishers exact test
(ACA) (significant values of P0.05 in bold).
More than 1 vascular hemispheric territory (MCA, ACA, PCA) affected by the ischemic lesion.
Brain stem and cerebellum simultaneously affected by the ischemic lesion.

Evaluation [APACHE II] index),11 severity of neurological deficit
(National Institute of Health Stroke Scale [NIHSS]),12 and impair-
ment of consciousness (Glasgow Coma Scale [GCS])13 were mea-
sured on each of the first 3 days after admission. In the same time
window, the presence of dysphagia was screened in all study subjects
by the study clinicians. In case of swallowing dysfunction, a
definitive examination was performed by trained speech-language
therapists comprising subtle clinical examination and additional
water swallowing or pharyngeal sensation test.14 Dysphagia was
diagnosed if positive clinical signs were accompanied by patholog-
ical findings in either additional test. Only dysphagia diagnosed
before SAP manifestation was included in the risk factor analysis.
The need for mechanical ventilation (MV) was decided in patients
with severe impairment of consciousness, respiratory failure (sus-
tained arterial PaO2 65 mm Hg, PaCO2 50 mm Hg), and severe
swallowing dysfunction. Respirator FiO2 levels were kept below 60%
in all cases to avoid oxygen-related damage of lung tissue. Patho-
logical findings in the initial chest x-ray after admission were
recorded. Cerebral CT- or MRI-documented ischemic infarctions
were classified according to the affected vascular territory. Infarc-
tions in the territory of the middle cerebral artery (MCA) were
further subdivided according to the size of the ischemic lesion (I,
33%; II, 33% to 66%; III, 66% of the MCA territory affected).
Radiological examinations were evaluated and documented by
trained radiologists.
Definition of SAP
SAP was diagnosed by the study clinician team in close collaboration
with the infection control practitioner according to Centers for
Disease Control and Prevention (CDC) criteria15 with clinical (lung
auscultation and percussion, presence of fever, purulent tracheal
secretion), microbiological (tracheal specimens, blood cultures), and
chest x-ray findings. The date of onset of the first incident per patient
was recorded. Infections occurring within the first 72 hours of NICU
treatment were defined as early-onset pneumonia (EOP).16 All
infections in mechanically ventilated patients were assigned as
ventilator-associated pneumonia (VAP).
Estimation of Clinical Outcome
By means of a follow-up survey undertaken with a mean time
interval of 14.63.7 months after NICU discharge, the long-term
clinical outcome could be measured in 70 stroke patients (10 with
SAP, 60 without SAP; 15 patients died during NICU treatment; 16
died after NICU discharge; 23 patients had no follow-up data).
Telephone interviews with the patients or their caregivers were
performed, and the Barthel Index17 and Rankin Scale18 were used as
outcome measures.
Statistical Analysis
Values are expressed as meanSD. Categorical data were analyzed
by 2 test or Fishers exact test estimating relative risk (RR) factors
for SAP development with corresponding 95% confidence intervals
(CIs). Subsequently, a multivariable logistic regression model, con-
trolling for possible confounding covariates, was fitted by forward
stepwise selection (for inclusion, 5%; for exclusion, 10%) from the
7 categorical variables found to be significant for SAP development
at the 5% level in the univariate analysis (Table 1). A repeated-
measures analysis of variance with posthoc Bonferroni-adjusted
contrasts was used on clinical scores (NIHSS, GCS, APACHE II),
with the occurrence of SAP as a between-subjects factor and time
(days 1 to 3 after NICU admission) as a within-subjects factor. All
probability values are 2 sided, and the level of significance was set
at P0.05. Statistical analyses were performed with SPSS 10.0 for
Windows (SPSS Inc).
Results
Study Population and Epidemiological Data
Over the 12-month study period, a total of 124 patients with
a mean age of 63.811.9 years were included (82 men; mean
age, 6510 years; 42 women; mean age, 6214 years). The
mean duration of NICU treatment was 7.67.3 days (range,
1 to 46 days).
 Hilker et al Pneumonia After Acute Stroke in an NICU 977

TABLE 2. Physiological Parameters Monitored in an NICU in 26 Patients With SAP Over 5 Days From Time
of SAP Diagnosis (Day 0)
Days After Diagnosis of SAP

0 1 2 3 4 Measurements, n
Mean arterial blood pressure* 106.7 (11.5) 110.9 (12.1) 108.1 (13.6) 114.2 (14.8) 116.0 (10.0) 105 (18)
Heart rate 86.6 (14.3) 85.9 (17.2) 85.7 (17.9) 85.7 (16.7) 84.0 (18.9) 105 (18)
Body temperature 38.5 (0.4) 38.3 (0.6) 38.3 (0.7) 38.3 (0.8) 38.1 (0.7) 105 (18)
Arterial PaO2 101.9 (6.2) 102.8 (10.1) 107.4 (7.5) 103.3 (13.3) 103.0 (12.6) 34 (12)
Venous PaO2 41.7 (3.5) 41.7 (4.6) 41.6 (5.8) 42.2 (5.5) 43.5 (3.6) 18 (8)
O2 saturation 96.9 (1.7) 96.8 (1.8) 96.3 (2.1) 96.2 (1.8) 96.0 (1.9) 105 (18)
Serum glucose 158.3 (55.0) 158.9 (35.8) 159.9 (43.4) 160.3 (50.8) 149.1 (43.5) 25 (12)
Data are presented as group means (SD) calculated from individual values that were averaged for each day (last column gives mean
number (SD) of individual measurements over the entire 5-day period).
*Obtained with arterial (radialis) catheter (n9) or by Riva-Rocci method (n17). Continuous intravenous catecholamine application
was needed in 14 of 26 patients: dopamine (n8), dopaminedobutamine (n3), dopaminenoradrenaline (n2), and
dopamineadrenaline (n1).
Measured with urinary catheter (n21) or intraoral (n5).
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017

Obtained from arterial blood samples from radialis cannula (n9).

Obtained from venous or capillary blood samples (n17).
Obtained from arterial (n9) or venous and capillary blood samples (n17). Continuous intravenous insulin (27 IU/h) application
was needed in 10 of 26 patients.

Acute Ischemic Brain Infarction and
Concomitant Diseases
Hemispheric infarction was documented in 106 patients with
1 hemispheric territory affected in 7 of 106 subjects.
Eighteen patients suffered from vertebrobasilar stroke with
simultaneous lesions in the brain stem and cerebellum in 5 of
18 subjects. There was no overlap between stroke locations;
ie, simultaneous acute infarctions in hemispheric and verte-
brobasilar territories were not found. The percentage distri-
bution of infarct sites is presented in Table 1 for the SAP and
non-SAP groups.
SAP: Epidemiology, Microbiological Monitoring,
and Treatment Response
The overall incidence rate of SAP was 26 of 124 (21%) with
a mean latency between NICU admission and disease mani-
festation of 1.81.9 days (range, 0 to 6 days). There was no
significant difference between the SAP and non-SAP groups
with regard to age and sex. SAP developed in 15 of 26
patients (58%) within the first 48 hours and in 19 of 26
patients within the first 72 hours of NICU treatment (73%
fulfilling EOP criteria). From blood and/or tracheal speci-
mens, a single pathogen (Staphylococcus aureus, n3; Kleb-
siella oxytoca, n2; Enterobacter species, n1; Escherichia
coli, n1) was isolated in 7 of 26 patients, whereas 2
pathogens (Escherichia coli and Candida albicans, n1;
Klebsiella oxytoca and Enterobacter species, n1; Candida
albicans and Candida glabrata; n1) were found in 3 of 26
cases. With the exception of 1 patient (monoinfection with
Klebsiella oxytoca), all positive cultures were found in stroke
patients with VAP (pathogen verification in 9 of 14 or 65% of
VAP cases). At the time of SAP diagnosis, a clear pulmonary
infiltrate in chest x-rays was diagnosed in 7 of 10 culture-
positive and in 11 of 16 culture-negative patients, whereas
only atelectasis was noted in 3 of 10 culture-positive and 5 of
16 culture-negative SAP subjects. However, all patients
without definite infiltrate fulfilled the CDC criteria by the
presence of fever, pathological findings in clinical lung
examination, and purulent tracheal secretion. Immediately
after NICU admission, chest x-ray infiltrate was noted in 4 of
26 SAP patients (3 culture negative, 1 culture positive),
suggesting prior aspiration. Several days after SAP diagnosis,
additional urinary tract infection was found in 4 of 26 SAP
patients (2 culture negative, 2 culture positive) and 1 epidid-
ymitis in a culture-negative SAP subject.
All SAP patients were treated with intravenous antibiotics,
leading to subsequent fever reduction. However, elevated
mean serum glucose levels and body temperatures over the
first 5 days after SAP manifestation were found despite
symptomatic therapeutic interventions (Table 2). Patients
with SAP stayed significantly longer in the NICU compared
with the non-SAP group (12.39.5 versus 6.36.0 days;
P0.001, unpaired t test).
Risk Factors for SAP
Results of the univariate SAP risk factor analysis are sum-
marized in Table 1 and Figure 1. Patients with vertebrobasilar
stroke had a significantly higher risk of developing SAP than
subjects with a hemispheric lesion (RR, 3.9; P0.05, 2 test).
Furthermore, patients with 1 infarcted vascular territory
were at higher risk (multiple lesion stroke: vertebrobasilar,
RR, 5.7; P0.001; hemispheric, RR, 3.0; P0.05, 2 test). In
case of small MCA infarction (type I), the risk of SAP was
significantly lower compared with other infarction sites (RR,
0.22; P0.05, 2 test).
MV was needed in 17 patients. The mean length of MV
was 9.39.4 days. VAP occurred in 14 of 17 patients
(82.4%), with a mean latency between endotracheal intuba-
tion and VAP occurrence of 1.11.8 days. Thus, the need for
MV led to a significantly increased RR for pneumonia of 7.3
(P0.001, 2 test).
 978 Stroke April 2003
Dysphagia was present in 36 of 124 patients and was
associated with a significantly increased risk for SAP (RR,
4.7; P0.01, 2 test). Pathological findings in the initial chest
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017
x-ray were found in 47 of 124 subjects (51% cardiomegaly,
30% pulmonal congestion, 7% atelectasis, 5% pleural effu-
sion, 4% pulmonal infiltrate, 3% emphysema). They were
also related to a significantly increased SAP incidence (RR,
4.1; P0.001, 2 test). In contrast, this relationship was not
detected for the presence of concomitant cardial and pulmo-
nal diseases and other cerebrovascular risk factors (data not
shown).
A multivariable logistic regression analysis with forward
stepwise factor selection yielded the following variables as
independent risk factors for SAP in acute stroke patients: MV
(P0.001; odds ratio [OR], 35.7; 95% CI, 6.5 to 194.7),
abnormal chest x-ray on admission (P0.005; OR, 7.3; 95%
CI, 1.8 to 29.2), and dysphagia (P0.064; OR, 3.3; 95% CI,
0.9 to 11.7). The logistic regression model reached a 97.4%
sensitivity and a lower 45.5% specificity for individual SAP
occurrence prediction (cutpoint, 0.5).
Clinical Scores
SAP patients scored significantly worse with respect to
general disease severity, neurological deficit, and conscious-
ness over the first 3-day period of NICU treatment (APACHE
II, F81.8; NIHSS, F42.6; GCS, F65.4; P0.001 for
each subscore). The occurrence of SAP significantly inter-
acted with the time course of all subscores (APACHE II,
Wilks-Lambda F8.3, P0.001; NIHSS, Wilks-Lambda
F8.2, P0.001; GCS, Wilks-Lambda F4.9, P0.001),
leading to an increase in general disease severity and neuro-
logical deficit over time exclusively in the SAP group.
Moreover, consciousness deteriorated more in SAP than in
non-SAP patients (Figure 2).
Clinical Outcome
The overall mortality rate of the study population during the
NICU treatment period was 15 of 124 (12.1%) with a
significantly higher mortality in the SAP (7 of 26, 26.9%)
compared with the non-SAP (8 of 98, 8.2%) group, resulting
in an RR of 3.3 to die from acute stroke in the presence of
SAP (P0.05, 2 test). During the poststroke follow-up
period, the mortality rate was significantly higher in the SAP
Figure 1. Factors with significantly
increased RR for development of SAP.
Vertical lines refer to 95% CIs. MLS-V
indicates multiple location stroke, verte-
brobasilar; MLS-H, multiple location
stroke, hemispheric. *P0.05,
**P0.001.
group (6 of 17, 35.3%; causes of death: 2 cardiac arrhythmia,
1 heart failure, 1 second pneumonia, 2 unknown) compared
with non-SAP subjects (10 of 60, 14.3%; RR, 2.5; 95% CI,
1.0 to 5.9; P0.05, 2 test; causes of death: 3 pulmonary
embolism; 2 second ischemic stroke, 1 cerebral hemorrhage,
1 pharyngeal carcinoma, 1 cardiac arrhythmia, 2 unknown).
At time of the follow-up survey, SAP patients had a signifi-
cantly higher Rankin Scale score (3.51.7 versus 2.2 in
non-SAP patients; P0.05, unpaired t test) and a lower
Barthel Index (50.542.4 versus 81.527.8; P0.05, un-
paired t test), indicating impaired clinical outcome in pneu-
monia subjects (Figure 3).
Discussion
The overall SAP incidence of 21.4% in our study population
is near the upper limit of the 10% to 25% incidence rates
found in large multicenter studies on medical and surgical
ICU patients.19,20 Thus, NICU-treated patients with acute
stroke have to be considered a high-risk group for the
development of pneumonia. The criteria of EOP were ful-
filled in 75% of cases, and 58% developed the disease
within the first 48 hours of NICU treatment. Therefore, a
considerable number of SAP cases are presumably commu-
nity acquired soon after stroke onset.
The spectrum of pathogens found in our study is in line
with previously published data on pneumonia in neurosurgi-
cal ICU patients.21 Etiological agents for bacterial pneumonia
vary by type of hospital, patient population at risk, diagnostic
methods, and the microbial flora in the ICU.6 In general,
Gram-negative bacilli have been implicated in 40% to 60%,
Staphylococcus aureus in 20% to 40%, and anaerobic bacte-
ria in 0% to 35% of cases.4,6 The high frequency of aerobic
Gram-negative pathogens found in our SAP population may
point to endogenous lung colonization after aspiration of
oropharynx secretions. Otherwise, Gram-negative bacteria
and Staphylococcus aureus may be acquired by exogenous
sources such as the hands of hospital personnel.
The mean length of NICU stay was 6 days longer in
patients with SAP compared with nondiseased subjects.
Furthermore, we found a significantly increased risk of death
in SAP patients during both the NICU treatment and the
poststroke follow-up period. These data are in line with
previous results on pneumonia lethality in general ICUs.22,23
 Hilker et al Pneumonia After Acute Stroke in an NICU 979
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017

Figure 2. Comparison of NIHSS (a), GCS (b), and APACHE II scale (c) values obtained during the first treatment days after NICU
admission in acute stroke patients with () and without () SAP. Data are presented as mean (circles) and SD (vertical lines). Repeated-
measures analysis of variance revealed significantly worse clinical scores in SAP patients over the entire observation period (each
P0.001) and significant differences between individual time points for NIHSS day 2 versus 3 (P0.035), GCS day 1 versus 2 and day
1 versus 3 (each P0.001), and APACHE II scale day 1 versus 2 (P0.001) and day 1 versus 3 (P0.005).

They clearly indicate that the occurrence of SAP is respon-
sible for prolonged ICU stay, excess mortality, and extra
treatment costs. Moreover, we found that long-term clinical
outcome is impaired in stroke patients who suffered from
SAP during their acute illness. This finding may be explained
by more extended cerebral infarctions and subsequent more
pronounced poststroke deficits in SAP patients. Otherwise,
we found elevated mean serum glucose levels and body
temperatures after SAP manifestation despite symptomatic
therapeutic interventions. Therefore, these SAP-induced dys-
regulations of body homeostasis might also deteriorate the
ability of functionally impaired but morphologically pre-
served tissue (ischemic penumbra)24 to recover from ischemia
because hyperglycemia, fever, and impaired oxygen supply
are known to deteriorate clinical outcome in patients with
acute stroke.25,26
We demonstrated that MV is an independent risk factor for
SAP in acute stroke patients. Thus, the need for endotracheal
intubation is highly predictive of SAP development, which is
in agreement with previous findings.27 There is ongoing
debate as to whether MV is suitable for improving overall
prognosis in patients with severe stroke.28,29 Steiner and
colleagues29 found that clinical outcome of ventilated stroke
patients is better than previously reported. Several studies
have shown that MV exposes ICU patients to a significantly
increased risk of ventilator-associated pneumonia.6,30 In our
study, early-onset VAP developed in 83% of intubated
stroke patients, which is even more frequent than the 70%
VAP incidence reported in a previous study on general ICU
patients.31 Hsieh et al32 found a comparable incidence of
early-onset VAP within the first 4 days of MV in comatose
patients, particularly those with head injury.
Significantly decreased GCS values at the time of admis-
sion in SAP patients, along with the identification of dyspha-
gia as a distinct risk factor, underline the pathophysiological
significance of silent aspiration in the absence of sufficient
protective reflexes in the development of SAP. Pathological
findings in the initial chest x-ray were additionally associated
with an increased SAP incidence. We propose that these are
early indicators of either aspiration and ongoing SAP or a
susceptibility state for the disease, eg, lung congestion in case
of cardiac failure. Moreover, the extent and location of the
 980 Stroke April 2003
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017
Figure 3. Rankin Scale (a) and Barthel Index (b) as a measure of
clinical outcome in 70 stroke patients at time of the follow-up
survey 142 months after NICU discharge. Absolute numbers
of patients with good (Rankin, 0 to 1; Barthel, 100 to 95), mod-
erate (Rankin, 2 to 3; Barthel, 90 to 55), and poor (Rankin, 4 to
5; Barthel, 50 to 0) clinical outcome are given for 10 patients
with and 60 patients without SAP.
ischemic lesion were found to be predictive of the develop-
ment of SAP because patients with vertebrobasilar and
multiple location infarction had a significantly higher risk of
acquiring the disease. Both are often associated with impaired
consciousness and are believed to have a cumulative effect on
the deterioration of swallowing with a high frequency of
aspiration.33 Several studies have shown that swallowing
difficulties and aspiration are common within 2 weeks after
stroke34,35 and are of pathogenetic relevance for the develop-
ment of pneumonia in these patients.36 However, it should be
noted that dysphagia and aspiration are not limited to verte-
brobasilar or bilateral hemispheric stroke but may also be
present after unilateral hemispheric infarction.37
In conclusion, our data underline the remarkable epidemi-
ological and prognostic impact of SAP on treatment and
outcome of acute stroke patients in a specialized NICU
setting. The considerably high coincidence rate of acute
stroke and pneumonia indicates a close pathophysiological
link between the diseases. Furthermore, our findings indicate
a high SAP risk in patients with multiple location and
vertebrobasilar stroke who also show considerable general
disease severity, a need for MV, impaired consciousness,
dysphagia, and pathological chest x-ray findings at time of
NICU admission. Because case fatality rates of 20% to 50%
have been reported in nosocomial pneumonia,7 intensive care
neurologists are urged to make prevention of SAP a treatment
priority. We conclude that dedicated standard precautions
following the CDC guidelines for pneumonia prevention4 and
surveillance of pneumonia38 are minimal requirements for
infection control in acute stroke patients treated in the NICU
setting.
Acknowledgments
We wish to express our gratitude to all healthcare workers at the
Neurological Intensive Care Unit at Cologne University Hospital for
their helpful cooperation. We also thank Dr Martin Hellmich,
Department of Medical Statistics, Informatics and Epidemiology,
Cologne University, for statistical advice.
References
1. Davenport RJ, Dennis MS, Wellwood I, Warlow CP. Complications after
acute stroke. Stroke. 1996;27:415 420.
2. Silver F, Norris J, Lewis A, Hachinski V. Early mortality following
stroke: a prospective review. Stroke. 1984;15:492 496.
3. Walker AE, Robins M, Weinfeld FD. Clinical findings: the National
Survey of Stroke. Stroke. 1981;12(suppl 1):1337.
4. Tablan OC, Anderson LJ, Arden NH, Breiman RF, Butler JC, McNeil
MM. Guidelines for prevention of nosocomial pneumonia: the Hospital
Infection Control Practices Advisory Committee, Centers for Disease
Control and Prevention. Infect Control Hosp Epidemiol. 1994;15:
587 627.
5. Vincent JL, Bihari DJ, Suter PM, Bruining HA, White J, Nicolas-Chanoin
MH, Wolff M, Spencer RC, Hemmer M. The prevalence of nosocomial
infection in intensive care units in Europe: results of the European
Prevalence of Infection in Intensive Care (EPIC) study. JAMA. 1995;274:
639 644.
6. Craven DE, Steger KS. Hospital-acquired pneumonia: perspectives for
the healthcare epidemiologist. Infect Control Hosp Epidemiol. 1997;18:
783795.
7. Craven DE, Kunches L, Lichtenberg DA, Kollisch NR, Barry A, Heeren
TC, McCabe WR. Nosocomial infections and fatality in medical and
surgical intensive care unit patients. Arch Intern Med. 1988;148:
11611168.
8. Grau AJ, Buggle F, Schnitzler P, Spiel M, Lichy C, Hacke W. Fever and
infection early after ischemic stroke. J Neurol Sci. 1999;171:115120.
9. Dettenkofer M, Ebner W, Els T, Babikir R, Lucking C, Pelz K, Rueden
H, Daschner F. Surveillance of nosocomial infections in a neurology
intensive care unit. J Neurol. 2001;248:959 964.
10. Heckmann JG, Kraus J, Niedermeier W, Erbguth F, Druschky A,
Schoerner C, Neundrfer B. Nosokomiale Pneumonien auf einer neurolo-
gischen Intensivstation. Dtsch Med Wochenschr. 1999;124:919 924.
11. Knaus WA, Wagner DP, Draper EA, Zimmermann JE. APACHE II: a
severity of disease classification system. Crit Care Med. 1985;13:
818 829.
12. Brott T, Adams HP, Olinger CP, Marler JR, Barsan WG, Biller J, Spilker
J, Holleran R, Eberle R, Hertzberg V. Measurements of acute cerebral
infarction: a clinical examination scale. Stroke. 1989;20:864 870.
13. Teasdale G, Jennet B. Assessment of coma and impaired consciousness:
a practical scale. Lancet. 1974;2:81 83.
14. Kidd D, Lawson J, Nesbitt R, MacMahon J. Aspiration in acute stroke: a
clinical study with videofluoroscopy. Q J Med. 1993;86:825 829.
15. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC defi-
nitions for nosocomial infections, 1988. Am J Infect Control. 1988;16:
128 140.
16. Langer M, Mosconi P, Cigada M, Mandelli M. Long-term respiratory
support and risk of pneumonia in critically ill patients: Intensive Care
Unit Group of Infection Control. Am Rev Respir Dis. 1989;140:302305.
17. Mahoney FI, Barthel DW. Functional evaluation: the Barthel Index. Md
Med J. 1965;14:61 65.
18. Van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJA, van Gijn
J. Interobserver agreement for the assessment of handicap in stroke
patients. Stroke. 1988;19:604 607.
19. Barsic B, Beus I, Marton E, Himbele J, Klinar I. Nosocomial infections
in critically ill infectious disease patients: results of a 7-year focal sur-
veillance. Infection. 1999;27:16 22.
20. Chevret S, Hemmer M, Carlet J, Langer M. Incidence and risk factors of
pneumonia acquired in intensive care units: results from a multicenter
prospective study on 996 patients: European Cooperative Group on Nos-
ocomial Pneumonia. Intensive Care Med. 1993;19:256 264.
21. Dettenkofer M, Ebner W, Hans FJ, Forster D, Babikir R, Zentner J, Pelz
K, Daschner FD. Nosocomial infections in a neurosurgery intensive care
unit. Acta Neurochir (Wien). 1999;141:13031308.
22. Fagon JY, Chastre J, Vuagnat A, Trouillet JL, Novara C, Gilbert C.
Nosocomial pneumonia and mortality among patients in intensive care
units. JAMA. 1996;275:866 869.
 Hilker et al
23. Valls J, Lon C, Alvarez-Lerma F. Nosocomial bacteriemia in critically
ill patients: a multicenter study evaluating epidemiology and prognosis.
Clin Infect Dis. 1997;24:387395.
24. Heiss WD, Graf R. The ischemic penumbra. Curr Opin Neurol. 1994;7:
1119.
25. Reith J, Jorgensen HS, Pedersen PM, Nakayama H, Raaschou HO,
Jeppesen LL, Olsen TS. Body temperature in acute stroke: relation to
stroke severity, infarct size, mortality, and outcome. Lancet. 1996;347:
422 425.
26. Weir CJ, Murray GD, Dyker AG, Lees KR. Is hyperglycemia an inde-
pendent predictor of poor outcome after stroke? BMJ. 1997;314:
13031306.
27. Salemi C, Morgan JW, Kelleghan SI, Hiebert-Crape B. Severity of illness
classification for infection control departments: a study in nosocomial
pneumonia. Am J Infect Control. 1993;21:117126.
28. El-Ad B, Bornstein NM, Fuchs P, Korczyn AD. Mechanical ventilation in
stroke patients: is it worthwhile? Neurology. 1996;47:657 659.
29. Steiner T, Mendoza G, De Georgia M, Schellinger P, Holle R, Hacke W.
Prognosis of stroke patients requiring mechanical ventilation in a neuro-
logical critical care unit. Stroke. 1997;28:711715.
30. Craven DE, Steger KS. Nosocomial pneumonia in mechanically ven-
tilated adult patients: epidemiology and prevention. Semin Respir Infect.
1996;11:3253.
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017
Pneumonia After Acute Stroke in an NICU 981
31. Torres A, Aznar R, Gatell JM, Jimenz P, Gonzlez J, Ferrer A, Celis R,
Rodriguez-Roisin R. Incidence, risk and prognosis factors of nosocomial
pneumonia in mechanically ventilated patients. Am Rev Respir Dis. 1990;
142:523528.
32. Hsieh AH, Bishop MJ, Kubilis PS, Newell DW, Pierson DJ. Pneumonia
following closed head injury. Am Rev Respir Dis. 1992;146:290 294.
33. Gordon C, Hewer R, Wade D. Dysphagia in acute stroke. BMJ. 1987;
295:411 414.
34. Schmidt J, Holas M, Halvorson K, Reding M. Videofluoroscopic
evidence of aspiration predicts pneumonia and death but not dehydration
following stroke. Dysphagia. 1994;9:711.
35. Kidd D, Lawson J, Nesbitt R, MacMahon J. The natural history and
clinical consequences of aspiration in acute stroke. Q J Med. 1995;88:
409 413.
36. Daniels SK, Brailey K, Priestly DH, Herrington LR, Weisberg LA,
Foundas AL. Aspiration in patients with acute stroke. Arch Phys Med.
1998;79:14 19.
37. Meadows JC. Dysphagia in unilateral cerebral lesions. J Neurol Neu-
rosurg Psychiatry. 1973;36:853 860.
38. Lemmen SW, Zolldann D, Gastmeier P, Luetticken R. Implementing and
evaluating a rotating surveillance system and infection control guidelines
in 4 intensive care units. Am J Infect Control. 2001;29:89 93.
 Nosocomial Pneumonia After Acute Stroke: Implications for Neurological Intensive Care
Medicine
Ruediger Hilker, Carsten Poetter, Nahide Findeisen, Jan Sobesky, Andreas Jacobs, Michael
Neveling and Wolf-Dieter Heiss
Downloaded from http://stroke.ahajournals.org/ by guest on June 13, 2017

Stroke. 2003;34:975-981; originally published online March 13, 2003;

doi: 10.1161/01.STR.0000063373.70993.CD
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright 2003 American Heart Association, Inc. All rights reserved.
Print ISSN: 0039-2499. Online ISSN: 1524-4628

The online version of this article, along with updated information and services, is located on the
World Wide Web at:
http://stroke.ahajournals.org/content/34/4/975

Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published
in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office.
Once the online version of the published article for which permission is being requested is located, click
Request Permissions in the middle column of the Web page under Services. Further information about this
process is available in the Permissions and Rights Question and Answer document.

Reprints: Information about reprints can be found online at:

http://www.lww.com/reprints

Subscriptions: Information about subscribing to Stroke is online at:

http://stroke.ahajournals.org//subscriptions/