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Seasonal and weather-mediated

variation in hospital pathogens:


opportunities for prevention
Eli N. Perencevich, MD MS
Professor of Medicine
University of Iowa, Carver College of Medicine
Iowa City, Iowa
Friday, 1 July 2011 17:15
Overview
MDR-Acinetobacter
Some early epidemiological work around
Acinetobacter
Seasonality
Background studies
First UMMC study
132-hospital study
Acinetobacter
Gram-negative coccobacillus
Was often viewed as a colonizer
HAS ARRIVED as a nosocomial pathogen
Acinetobacter baumannii is the most common
Outbreak of imipenem-resistant Acinetobacter in
New York
Difficult to eradicate colonized state
Emergence in returning troops from the Middle
East

Reference Clinical Setting Cases Attributable
Mortality
Acinetobacter Infections Compared to Matched Un-infected Controls
Grupper (2007) Nosocomial BSI
ICU, Israel
52 BSI 36.5%
Blot (2003) Nosocomial BSI
ICU, Belgium
45 BSI 7.8%
Acinetobacter Infections Compared to Matched Controls with Klebsiella Infection
Robenshtok (2006) Nosocomial BSI
Israel
112 BSI 22.7%
Multidrug-Resistant Acinetobacter Infections Compared to Matched Susceptible Controls
Kwon (2007) CR-BSI
3* Care, Korea
40 CR- Infections 25-30%
Sunenshine (2007) MDR-Infections
3* Care; Baltimore
96 MDR-Infections 8.4%
Lee (2007) MRD-Infections
3* Care, Taiwan
48 MDR-BSI 21.8%
Multidrug-Resistant Acinetobacter Infections Compared to Matched Un-infected Controls
Sunenshine (2007) MDR-Infections
3* Care, Baltimore
96 MDR-Infections 14.8%
Playford (2007) CR-Infection/Colonization
ICU, Australia
66 CR-Infections or
Colonization
20%
Bacteria CLABSI
(%
imipenem
resistant)
VAP
(%
imipenem
resistant)
CAUTI
(%
imipenem
resistant)
Pooled
(%
imipenem
resistant)
Pseudomonas 23.0% 25.1% 26.4% 25.3%
Klebsiella 10.8% 10.1 3.6
Acinetobacter 29.2 25.6 36.8
NHSN: impenem-resistance
Why do I care about AB?
July 2002, MICU
Everyone on vacation, except
5 patients with MDR-AB bacteremia in July
4 in August
Control plan
Shut MICU
Press
Ban artificial nails
0
1
2
3
4
5
What happened?
Universal gown/glove instituted in MICU
and SICU

Active surveillance on all transfers from
outside hospitals; isolated until cultures
return

Statewide AB surveillance (2010)
The Source!
180-bed, UMMC-afilliated LTAC
1
147 patient point prevalence survey (12/05)
28% AB+ (41 patients)
Sensitivity by site 22% peri-rectal,
68% sputum, 22% wound
2010 Survey of 57 Maryland Facilities
2
1. Furuno J et al, Am J Infect Control 2008
2. Thom K (unpublished)
Transmissibility and Protection
Organism
HCW
Room
Entries
Hand +
Before
(%)
Gown
and/or
Glove +
After %
Hands +
After
Removal
Effectiveness
of PPE
A. baumannii
1
202 1.5% 38.7% 4.5% 88%
P. aeruginosa
1
133 0% 8.2% 0.7% 90%
VRE
2
94 0% 9% 0% 100%
MRSA
2
81 2% 19% 2.6% 85%
1. Morgan D, et al, Infect Control Hosp Epidemiol July 2010; 31(7):716-21.
2. Snyder G, et al, Infect Control Hosp Epidemiol July 2008; 29(7):584-589
FOR MORE INFO...
Add in local hand hygiene
adherence rates
0
36% 20% 17% 14% 11% 8% 5%
50%
18% 10% 9% 7% 5% 4% 2%
60%
15% 8% 7% 6% 4% 3% 2%
70%
11% 6% 5% 4% 3% 2% 1%
80%
7% 4% 3% 3% 2% 2% 1%
90%
4% 2.% 2% 1% 1% 1% 1%
100%
0 0 0 0 0 0 0
0 50% 60% 70% 80% 90% 100%
Compliance with Gloves (patients on contact precautions)

C
o
m
p
l
i
a
n
c
e

w
i
t
h

H
a
n
d
-
H
y
g
i
e
n
e

Environmental Sampling
Percent of rooms with positive
environmental cultures for organism
known to be colonizing patient (PFGE)
78% Acinetobacter
35% VRE
28% MRSA
22% P. aeruginosa
15% KPC
1. Morgan D, et al, Society for Healthcare Epidemiology of America (SHEA) 2010
FOR MORE INFO...
What else?
Outbreak in summer
Vets returning from Iraq had high
incidence of infection with Acinetobacter
Tropical climates with more AB infections

Could weather or season play a role?
If found, could this alter our infection
prevention practices?
Seasonal variation
Certain infections have seasonal variation
Influenza, RSV, Legionella*
Seasonal variation in hospital pathogens?
Previous studies limited given combined data
Seattle summer added to Houston summer
Did not look at temperature specifically
FOR MORE INFO...
Fisman DN, J Infect Dis 2005 Dec 15;192(12):2066-73
Seasonal Variation AB
CDC NNIS 1974-1977 hospital-wide data
1
2x increase in late summer vs early winter
CDC NNIS 1987-1996, 3447 ICU isolates
2

54% higher during JulyOctober than during
NovemberJune (8.0 vs. 5.2 per 10,000
patientdays, p<0.01)
Did not control for location, year, temp etc.
No variation in Pseudomonas spp
1. Retailliau HF, et al. J Infect Dis 1979;139:37152.
2. McDonald LC et al. Clin Infect Dis 1999;1133-7.
FOR MORE INFO...
Monthly incidence density of acinetobacter infections: intensive care unit
surveillance component, National Nosocomial Infection Surveillance
System, 19871996 (white bars, A. baumannii; black bars, all other
Acinetobacter species)
McDonald LC et al. Clin Infect Dis 1999;1133-7.
FOR MORE INFO...
Monthly incidence density of Pseudomonas aeruginosa infections: intensive
care unit surveillance component, National Nosocomial Infection
Surveillance System, 19871996.
McDonald LC et al. Clin Infect Dis 1999;1133-7.
FOR MORE INFO...
Seasonal Variation of Season
2008
FOR MORE INFO...
http://www.ncdc.noaa.gov/sotc/index.php?report=national&year=2008&month=ann
Study
Aim: Assess for seasonal variation in
Pseudomonas aeruginosa, Acinetobacter
baumannii, Enterobacter cloacae, Escherichia
coli, Staphylococcus aureus, and enterococci
8-years of clinical culture data, UMMC
Summer: July-September
Community-associated <48 hours, HA>48 hours
Time-series analysis; Poisson GLM
FOR MORE INFO...
Perencevich et al. Infect Control Hosp Epidemiol Dec 2008:1124-31
Additional Methods
Adjusted for long-term trends
Assessed for temperature, humidity and
rainfall effects
Adjusted for non-weather seasonality
>48 hour and <48 hour for community vs.
hospital strains
r/o intern effects

Cultures and Sources
218,594 admissions
26,624 unique cultures (one per pt / year)
3,373 Pseudomonas aeruginosa (34% urine)
1,444 Acinetobacter baumannii (35% sputum)
1,823 Enterobacter cloacae (27% urine)
6,035 Escherichia coli (74% urine)
7,162 Staphylococcus aureus (39% wound)
6,787 enterococci (51% urine)
Community-associated
Species
% Community-associated
(<48 hours)
Pseudomonas aeruginosa 37%
Acinetobacter baumannii 33%
Enterobacter cloacae 33%
Escherichia coli 56%
Staphylococcus aureus 62%
enterococci 39%
Seasonal Variation in GNR
Seasonal GPC
Summer Peaks
Additional Studies
E. coli BSI in N. Israel
Single medical center (HaEmek)
8 years (2001-2008)
Winter (Dec-Feb) Transition (Mar, Apr, Nov)
and Summer (May-Oct)
983 BSIs, 72% community, 70% UTI
IRR summer vs winter 1.21 (95% CI 1.16-1.28)
IRR summer vs trans 1.19 (95% CI 1.12-1.26)
Within seasons no temperature association
FOR MORE INFO...
Chazan B. et al. Clin Micro Infect 2010
E. coli BSI in N. Israel
FOR MORE INFO...
Chazan B. et al. Clin Micro Infect 2010
E. coli BSI in Olmsted County,
MN
Single county
Mayo Med Center and Olmsted Med Center
1998-2007
Summer: June-Sept
461 BSI, 59% community, 80% 1 Urine
IRR summer vs other 1.35 (1.12-1.66)
7% increase for each 10 degree rise in temp
Did not adjust for month in temp analysis
FOR MORE INFO...
Al-Hasan et al. Clin Micro Infect 2009;15:947-950
E. coli BSI in Olmsted County,
MN
FOR MORE INFO...
Chazan B. et al. Clin Micro Infect 2010
Repeated analysis in Enterobacter (only 38 isolates) and reported no seasonality
Bacteremia England 2004-2008
FOR MORE INFO...
Wilson J. et al. Clin Micro Infect 2010 (in press)
Klebsiella BSI
4 sites (Durham, NC; Marseille, France;
Melbourne, Australia and Taipei, Taiwan)
2001-2006
1189 BSI, ? % community
IRR 4 warmest months 1.46 (1.04-2.06)
Ranged from 1.41 to 1.49 at 4 sites, all p<0.05
Enterobacter IRR = 1.22 (0.92-1.63)
Serratia IRR = 1.23 (0.86-1.77)
FOR MORE INFO...
Anderson D, et al. J Infect Dis 2008; 197:752-6
Klebsiella, 4 Countries
A=Duke
B=Marseille
C=Melbourne
D=Taipei
FOR MORE INFO...
Anderson D, et al. J Infect Dis 2008; 197:752-6
Klebsiella, 4 Countries Combined
FOR MORE INFO...
Anderson D, et al. J Infect Dis 2008; 197:752-6
What about
MRSA?
Rhode Island Hospital
All clinical MRSA
isolates
January 2001 to
March 2010
48-hour rule
Poisson regression
Offset log # admits
or ED visits
FOR MORE INFO...
Mermel LA et al. PLoS One, March 2011;6(3):e17925
Seasonality CA-MRSA
Pediatric patients
1.85 times (95%CI 1.45-2.36, p<0.01)
in quarters 3-4
Adult patients
1.14 times (95%CI 1.01-1.29, p=0.03)
in quarters 3-4

FOR MORE INFO...
Mermel LA et al. PLoS One, March 2011;6(3):e17925
Seasonality HA-MRSA
Pediatric patients
2.94 times (95%CI 1.39-6.21, p=0.015)
in quarters 3-4
Adult patients
1.00 times (95%CI 0.89-1.12, p=0.97)
in quarters 3-4
FOR MORE INFO...
Mermel LA et al. PLoS One, March 2011;6(3):e17925
FOR MORE INFO...
Mermel LA et al. PLoS One, March 2011;6(3):e17925
FOR MORE INFO...
Mermel LA et al. PLoS One, March 2011;6(3):e17925
Seasonality and S. aureus Mixed Infections, Bacteremia, and Upper Extremity Infections
FOR MORE INFO...
Mermel LA et al. PLoS One, March 2011;6(3):e17925
Seasonality and Staphylococcus aureus Skin Infections
FOR MORE INFO...
Mermel LA et al. PLoS One, March 2011;6(3):e17925
Seasonal and temperature-
associated increases in
gram-negative bacterial
bloodstream infections
among hospitalized patients


Seasonality GNR, US 1999-2006
132 US Hospitals, TSN Database
Jan 1, 1999 - Sept 30, 2006
Acinetobacter spp, E. coli, K. pneumoniae,
P. aeruginosa Enterococcus spp and S.
aureus
Monthly climate data: National Climactic
Data Centers Climate Data Online system
ZIP code: mean temp, mean dew point,
total precipitation
BSI isolates
211,697 BSIs
9,423 hospital-months
S. aureus: median 976 BSI/month
Acinetobacter: median 67 BSI/month

FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
Distribution of Hospitals by Region
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
Seasonally adjusted Change in BSI
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
* Controlling for long-term trends, census region
BSI and Temperature
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
* Controlling for long-term trends, census region, precipitation and mean relative humidity

BSI and Humidity or
Precipitation
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
Mean Acinetobacter BSI by Month
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
Mean E. coli BSI by Month
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
Mean K. pneumonia BSI by Month
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
Mean P. aeruginosa BSI by Month
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9):e25298. Epub 2011 Sep 26.
Mean BSI by Month for GPC
FOR MORE INFO...
Eber M et al. PLoS One. 2011;6(9)
High-Impact Journal Associate Editor
Even if there is seasonality of admissions, and even if
such seasonality were deemed to be of practical
importance, why should the correlation with temperature
be of value?
What is the practical public health significance of
knowing such correlation (beyond the general idea that
number of cases is greater in summer compared to
winter)
Surely just increasing surveillance of tap water quality in
summer is sufficient guidance, regardless of exact
atmospheric temperature
Even if we faced a new ice age, surely populations
would be at risk to these pathogens?
Q1: Why would temperature
data be of value?
Seasons are associated with many changes
including staffing changes (new interns),
vacations and weather. If temperature was not
associated with seasonal peaks, we would want
to look at other modifiable factors
If higher-temperatures are predicted,
surveillance could be altered
Data on temperature and increased infections
could inform the global climate change debate

Q2: Public health significance of knowing
such seasonal correlation?
Alter surveillance strategies
Cost-effectiveness could target GNR
surveillance more intensively in summer
Alter empirical therapy decisions
Begin other investigations to determine the
source of each GNR in summer time
Surveillance
Source control
Q3: Just increase surveillance
of tap water quality
None of these pathogens have been
detected in increased frequency in our tap
water
Association could be through prolonged
environmental contamination of hospitals,
colonization of HCW hands or fomites
E. coli could be from summer barbecue
cookouts or increase sexual activity - UTI
Q4: Even if we faced a new ice age, surely
populations would be at risk to these pathogens?
I have submitted my grant to do a quasi-
experimental study of infections before
and after an ice age
It appears that only eliminating a risk
factor and all associated infections is
worthwhile then?
I disagree!
Acknowledgments
Anthony Harris
Jon Furuno
Mary-Claire Roghmann
Daniel Morgan
Kerri Thom
Richard Venezia
Kristie Johnson
Colin Stine
Atlisa Young
Lisa Pinelis
Michelle Shardell

Marin Schweizer
Hannah Day
Kristen Kreisel
Mary Warren
Gwen Smith
Mike Eber
Jessina McGregor
Ramanan Laxminarayan