Association between use of hand hygiene products and rates ... - CCIH

Association between use of hand
hygiene products and rates of health
care–associated infections in a large
university hospital in Norway
Trine Herud, RN, a Roy M. Nilsen, MSc, a,b Kjersti Svendheim, RN, c and Stig Harthug, MD, PHD a,d
Bergen, Norway
Background: An association between use of hand hygiene products and health care–associated infection rates was investigated in
a large Norwegian university hospital.
Methods: We conducted an ecologic study by combining data from purchasing and admission systems with data from 32 point
prevalence surveys (27,248 patients) in 1998-2005. Data on purchase of hand disinfectants and soap, and patient-days, were collected
for 20 bed wards similar to those of the prevalence surveys.
Results: The prevalence of infections was 7.1%. We found no significant decline in overall infections (P 5 .19), but use of hand
hygiene products significantly increased from 28.5 L per 1000 patients-days in 1998 to 43.3 L per 1000 patient-days in 2005 (P ,
.001). After examining a linear dose-response relation between use and infection rates, we observed a borderline significant decline
in infections from 8% to 6% with increased use of hand hygiene products (P 5 .05). This association appeared stronger for wards
that were registered with infections .9% at study start in 1998 (P , .001).
Conclusion: These data suggests that infection rates may be reflected by amount of hand hygiene products used. Quantification of
such products over time may serve as an indicator for hand hygiene performance in hospitals.
Copyright ª 2009 by the Association for Professionals in Infection Control and Epidemiology, Inc.
(Am J Infect Control 2009;37:311–17.)
The benefits of hand hygiene in reducing the risk of
cross contamination and health care–associated infections
in hospitals are well established. 1,2 For that reason,
performance of hand hygiene among health care
workers in many hospitals worldwide is mandatory. 3-5
The guidelines from the Centers for Disease Control
and Prevention (CDC) state that both handwashing and
use of hand disinfection should be practiced. 6 In Norway,
the official guideline from 2004 emphasizes the use of
hand disinfection to be the primary choice of method. 7,8
Numerous studies have examined the relation between
compliance with hand hygiene guidelines and infection
rates. 9-14 It is widely accepted that compliance
remains an important factor in controlling infection
From the Centre of Infection Control, Haukeland University Hospital, a
Department of Public Health and Primary Health Care, University of
Bergen, b The Blood Bank, Haukeland University Hospital, c and Institute
of Medicine, University of Bergen, Bergen, Norway. d
Address correspondence to Trine Herud, RN, Department of Infection
Control, Haukeland University Hospital, N-5021 Bergen, Norway.
E-mail: trine.herud@helse-bergen.no.
Conflicts of interest: All authors report no conflicts of interest.
0196-6553/$36.00
Copyright ª 2009 by the Association for Professionals in Infection
Control and Epidemiology, Inc.
doi:10.1016/j.ajic.2008.06.006
rates, but that high compliance have to be maintained
over time to effectively reduce infection rates. 15-18
An interesting question is whether hand hygiene
compliance and infection rates may be reflected by
the amount of hand hygiene products used in a hospital.
19 If so, the data of hand hygiene products used may
serve as a simple indicator of hand hygiene performance
and thereby as a tool for hospital infection control.
As we are aware, there are few epidemiologic
studies that have evaluated this possibility.
Repeated point prevalence surveys are well-established
methods for measuring various health careassociated
infections during a long-term period. 20-23
In the present study, we used data from a large Norwegian
university hospital during the years 1998-2005 to
examine an association between amount of hand disinfectants
and soaps used and the prevalence of health
care–associated infections.
MATERIALS AND METHODS
Setting
The study was conducted at Haukeland University
Hospital in Bergen, which is one of the 2 largest acute
care hospitals in Norway. The hospital provides approximately
1100 beds with a number of specialties,
except organ transplantations. Wards are organized after
a primary nursing design, in which the health care
311

312 Herudetal. American Journal of Infection Control
May 2009
workers are divided into teams treating the same set of
patients every day. One team may involve a wide spectre
of different health care workers, basically including
registered nurses, nursing assistants, and doctors.
Data
This was an ecologic study in which information from
3 different data sources was compared. Information on
product labels and amount of hand soap and disinfectant
were abstracted from the hospital"s purchasing database
system, whereas information on a patient’s length
of hospital stay (ie, patient-days) was abstracted from
the patient admission database system. If a patient was
admitted and discharged on the same day, we defined
his or her length of hospital stay as 1 day.
From point prevalence surveys, we collected information
on a patient’s infection status. In brief, repeated
point prevalence surveys have been conducted by the
Centre of Infection Control at the hospital 4 times a
year since 1994. They were normally conducted on
1 day for each of the following time intervals: (1) January
to March, (2) April to June, (3) July to October, and
(4) November to December. Infection data were collected
and registered at each ward by dedicated senior
nurses and physicians on the day of collection. Each
patient was inspected between 8:00 and 9:00 AM and
examined with respect to infection status. Whether
an infection started outside or during the hospital admission
or at another hospital stay was assessed by interviewing
the patient and reading the patients journal.
Ahead of a data collection, an announcement was
made on the hospital’s Intranet. Detailed instructions
and guidelines were sent by e-mail to those who
were responsible for the data collection. All infection
data were registered on-line and stored in a single infection
database system. Generally, response rates
were over 95%.
All types of hospital infections were registered and
CDC definitions of nosocomial infections, with minor
modifications, were used throughout the surveillance
period. 24,25 The CDC’s National Nosocomial Infections
Surveillance system defines nosocomial infections as
a localized or systemic condition that results from adverse
reaction to the presence of an infectious agent(s)
or its toxin(s) and that was not present or incubating at
the time of admission to the hospital. 26
Initially, our study comprised a total of 25 wards during
the period 1998 to 2005. We excluded 1 ward because
infection rates were unusually high (burn
patients, .50%) and an additional 4 wards because information
on hospital stay (ie, not bed wards) or use of
hand hygiene products was unknown, leaving data on
27,248 patients from 32 prevalence surveys for
analysis.
Hand hygiene performance
Hand hygiene was defined as any use of hand soap
or hand disinfection. All hand disinfectants from dispensers
or pocket bottles were waterless and contained
ethyl alcohol 70% and glycerine #2%. The dispensers
for soap or hand disinfectants provided the same dose,
#2 mL. Hand disinfectants were not used for cleaning
surfaces or medical instruments. For these purposes,
technical alcohol without glycerine was required.
In our hospital, sinks with dispensers for hand soap
and paper towels are available in every patient room
and located near the door. Furthermore, hand disinfection
has been placed between the beds and on the respirators
and in the staff rooms, the disinfection rooms,
the kitchens, the wardrobes, and the corridors in addition
to locations at which the health care workers have
found it convenient. The availability of hand soap and
disinfectant has increased over the years. Until 2004,
pocket bottles of hand disinfection were generally
not available for the attending health personnel.
Hand hygiene campaigns
In 2000 and 2005, large hand hygiene campaigns
were performed at the hospital. The campaign in 2000
was conducted during 1 day (October 25) by the infection
control personnel at the hospital. Four weeks before
the campaign day, several posters about hand
hygiene methods and interventions to increase compliance
were distributed around the entire hospital together
with the campaign program. During the
campaign day, different lectures were given, not only
emphasizing hand hygiene but also pointing at the hospital’s
infection control program, which was published
as an electronic handbook on the hospital’s Intranet
during the spring 2001. The campaign also focused on
standard precautions and on the health care workers attitude
and behavior with respect to hand hygiene.
The campaign in 2005 was conducted for 8 months,
from February to September, and was organized by the
Norwegian Institute of Public Health, which invited all
hospitals and nursing homes in Norway to participate.
The main focus of the campaign was compliance of
hand hygiene. Prior to the campaign, in 2004, the
new national guideline for hand hygiene for health
care settings was released. According to this guideline,
the recommended use of hand hygiene products is
hand disinfection for 15 to 30 seconds. If hands are visible
dirty, they should be washed with water and soap
for 30 to 60 seconds.
Statistical analyses
All analyses were performed by using Statistical
Analysis System (SAS) version 9.1 for Windows (SAS

www.ajicjournal.org
Vol. 37 No. 4
Institute, Inc., Cary, NC). All P values were 2-sided, and
values ,.05 were considered statistically significant.
We quantified use of hand hygiene products as the total
amount (sum liters) of hand disinfections and soap purchased
during the whole study period, as well as by year,
and by time periods for which the 32 point prevalence
surveys were conducted. Use was further standardized
by dividing the amount of use by the corresponding
sum of patientsÕ days for the relevant time periods (liters/1000
patient-days). Bootstrap method was used to
estimate the standard error of mean (SEM) of use by
the standard deviation (SD) of estimates found by resampling
from the observed data 200 times. 27 We used
unadjusted linear regression analysis to test whether infection
rates and use of hand hygiene products changed
over time (ie, a test for trend). Similarly, we used unadjusted
linear regression analysis to examine a dose-response
association between infection rates and
amount of hand hygiene products used.
In Norwegian hospitals, infection rates above 9% are
regarded as high. 28-30 Using this basis, we categorized
wards into 2 groups: whether their infection rates
were above or under 9% on average during the first
study year in 1998. We then performed separate linear
regression analyses to examine whether the associations
differed in magnitude between the 2 groups (9
and 11 wards, respectively). Notably, 3 of the wards
studied were established later than 1998 but were included
in the latter group because they were registered
with infection rates #9% during their first study year.
RESULTS
Characteristics of the 27,248 patients in the present
study with infection status are shown in Table 1. Mean
patient age was 51.8 (SD, 27.1) years. Approximately
55% of the patients were women, over 25% had undergone
a surgical operation, and 12% of the patients
were using a urinary tract catheter. The proportion of
patients registered was evenly distributed across the 4
time intervals for which the prevalence studies were
conducted (25%). Mean number of patients per year
was 3406 (SD, 236.1).
The overall prevalence of health care-associated infections
in 1998-2005 was estimated to be 7.1% (Table
2). We observed no significant decline in infection rates
during these years (Table 2; P 5 .19). The lowest infection
rate (5.7%) was observed in 2001.
The overall mean use of hand hygiene products in
1998-2005 was 35.5 L per 1000 patient-days (Table 2).
The use of hand hygiene products increased from 28.5
L per 1000 patients-days in 1998 to 43.3 L per 1000 patient-days
in 2005 (Table 2; P , .001). Linear regression
analysis further showed a significant increase in the use
of hand disinfectants and a significant decline in the use
Table 1. Characteristics of 27,248 patients with infection
status at Haukeland University Hospital, Norway, 1998
2005
Characteristics No. %
Survey time interval
January-March 6951 25.5
April-June 6553 24.0
July-October 6762 24.8
November-December 6982 25.6
Age
Unknown 29 0.1
,15 Yr 3486 12.8
15-34 Yr 4141 15.2
35-54 Yr 4912 18.0
55-74 Yr 7775 28.5
.74 Yr 6905 25.3
Gender
Woman 14,664 53.8
Man 12,584 46.2
Surgical operation
No 20,033 73.5
Yes 7215 26.5
Urinary tract catheter
No 23,949 87.9
Yes 3299 12.1
of hand soaps (Table 2; P , .001 and P 5 .003, respectively).
There was a strong increase in the use of hand
disinfectants in 2005 and a top in the use of both hand
soap and disinfectants in 2001.
We examined the dose-response relation between
overall infection rates (from 32 prevalence surveys)
and amount of hand hygiene products used (Fig 1).
We observed a 25% decline on average of health
care-associated infections (from approximately 8% to
6%) with increased use of hand hygiene products
from approximately 26 to 47 L per 1000 patient-days
(P 5 .05). We also examined whether this association
was different between wards with initially high and
low infection rates at study start (Fig 2). We observed
a strong inverse relation between use of hand hygiene
products and infection rates for wards with infection
rates .9% and a nonsignificant relation for wards
with rates below this cut point (P , .001 and P 5 .75,
respectively).
Finally, we tested the association between use of
hand disinfectants alone and rates of health care-associated
infections among all study wards (data not
shown). There was a significant inverse relation between
use of alcohol-based hand products and infection
rates after adjusting for use of hand soap
(adjusted, P 5 .04).
DISCUSSION
Herud et al. 313
In this study, we examined prevalence of health
care–associated infection in relation to the use of

314 Herudetal. American Journal of Infection Control
May 2009
Table 2. Prevalence of health care–associated infections and use of hand soap and disinfectants at Haukeland University
Hospital, Norway, 1998-2005
Year
No. of subjects
with infection status
Health care-associated
infections
hand hygiene products in a large university hospital in
Norway from 1998 through 2005. Using linear dose-response
analysis, we found that the percentage of hospital
infection declined by 25% on average (ie, from 8%
to 6%) with increased use of hand hygiene products
from 26 to 47 L per 1000 patient-days. This association
was borderline significant but appeared to be stronger
for wards that were registered with initially high infection
rates (.9%) at study start in 1998.
The strength of the present study is that it was hospital
based, comprising 27,248 patients from 32 pointprevalence
surveys during 8 years. Information on infection
status was reported by trained health personnel
using a standardized electronic form for all wards. In
addition, the criteria for health care-associated infections
were the same for each survey during the study
period.
There are, however, some limitations of the present
study. There are many factors that may have contributed
to the changes in both infection rates and in use
of hand hygiene products, including education, compliance,
and frequency of use. However, because we
do not have exact measures about such factors, they
had to be assumed rather than tested in statistical
models. Furthermore, we cannot exclude the possibility
of bias in prevalence estimates for the entire hospital
because several wards are not included in the study.
In addition, we only had information on purchase of
hand hygiene products and not the actual amount of
use. However, because of the limitations of storage capacity
at our hospital, the products are purchased in
small scales and are being continuously used.
Few studies have reported both prevalence of hospital
infections and amount of hand hygiene products
used over a long-term period. A hospital-based study
Use of hand
hygiene products (liters/1000 patient-days)*
No. % Any Soap Disinfectant
All 27,248 1947 7.1 6 0.16 y
35.5 6 0.16 z
23.4 6 0.21 12.2 6 0.18
1998 3171 250 7.9 6 0.48 28.5 6 0.93 25.5 6 0.89 2.9 6 0.27
1999 3373 257 7.6 6 0.46 31.1 6 0.93 23.8 6 0.84 7.3 6 0.45
2000 3052 245 8.0 6 0.49 31.9 6 0.96 22.7 6 0.84 9.2 6 0.52
2001 3612 207 5.7 6 0.39 36.8 6 1.07 25.1 6 0.88 11.7 6 0.57
2002 3386 236 7.0 6 0.44 35.6 6 1.06 23.1 6 0.90 12.5 6 0.54
2003 3465 258 7.4 6 0.46 36.2 6 1.10 22.0 6 0.86 14.2 6 0.66
2004 3381 222 6.6 6 0.43 39.8 6 1.08 23.1 6 0.88 16.7 6 0.66
2005 3808 272 7.1 6 0.42 43.3 6 1.02 21.8 6 0.76 21.5 6 0.78
P trend §
.19 ,.001 .003 ,.001
*Based on sum of liters of hand hygiene products used and sum of patient-days from 20 study wards similar to those registered for patients with infection status.
y
Percent 6 SEM.
z
Liters/1000 patient-days 6 SEM: bootstrap method was used to estimate SEM by the standard deviation of estimates found by resampling from the original data 200 times.
§
P trend was estimated by incorporating year as a linear predictor in an unadjusted linear regression model: the linear predictor was negative for health care-associated infections
and use of soap but positive for use of disinfectants as well as for the overall use of hand hygiene products.
Infections (%)
15
12
9
6
3
0
24 29 34 39 44 49
Hand hygiene products (litres/1,000 patient days)
Fig 1. Prevalence of health care–associated
infections from 32 point prevalence surveys by use
of hand disinfectants and soap (liters/1000 patientdays)
at Haukeland University Hospital, Norway,
1998-2005. Dots represent infection rates; solid line
represents predicted infection rate based on
unadjusted linear regression analysis.
from Switzerland reported a 41% decrease (ie, from
17% to 10%) in health care–associated infections during
a 4-year period. 19 During the same period, the overall
use of alcohol-based handrub increased from
approximately 4 to 15 L per 1000 patient-days. The observed
rate changes in that study may be explained by
the comprehensive information campaign that was
conducted during the 4-year period. Notably, the campaign
involved all staff members at the hospital, including
senior members from all wards and departments.
In addition, 2 unit-specific studies have reported decreased
infection rates with increased use of hand

www.ajicjournal.org
Vol. 37 No. 4
Infections (%)
15
12
9
6
3
0
24 29 34 39 44 49
Hand hygiene products (litres/1,000 patient days)
Fig 2. Ward-specific prevalence of health careassociated
infections from 32 point prevalence
surveys by use of hand disinfectants and soap (liters/
1000 patient-days) at Haukeland University Hospital,
Norway, 1998-2005. Triangles and segmented line
represent infection rates and predicted infection
rate, respectively, for wards with infection rates
.9% in 1998; dots and solid line represent infection
rates and predicted infection rates, respectively, for
wards with infection rates #9% in 1998. Prediction
of infection rates was based on unadjusted linear
regression analysis.
hygiene products. In an intervention study, use of handrub
in a neonatal unit increased from 67 to 89 L per
1000 patient-days after implementing a hand hygiene
education program, while infection rates decreased
by 38% (ie, from 13% to 8%). 31 In another intervention
study, there was a 30% reduction in the infection rates
in the units of a health care facility in which alcoholbased
hand sanitizer was used, compared with units
in which no such sanitizer was used. 32
We observed that the use of hand soap slightly decreased
from 26 to 22 L per 1000 patient-days from
1998 to 2005 but that the use of hand disinfectants
strongly increased from 3 to 22 L per 1000 patientdays.
It is likely that the strong increase in hand disinfection
may be due to a gradual shift in the practice of
hand hygiene performance, accompanied by better
compliance, more frequent education, and increased
availability of hand hygiene products. A small portion
of the increase in hand disinfectants may also be related
to the number of staff. From 2000 to 2005, there
was an overall 8% increase in health care personnel at
our hospital. The relative increase in the use of hand
disinfectants was 135% (Table 2).
Interestingly, we observed a strong linear doseresponse
relation between use of hand hygiene products
and infection rates for wards with infection rates
.9% (P , .001) at study start in 1998 but found no
Herud et al. 315
significant relation when analysis was restricted to
wards with prevalence #9% at study start. This may indicate
that excessive use of hand hygiene products is
not an efficient way of reducing infections in low-prevalence
wards in hospitals. Notably, the volume range of
use of hand hygiene products was the same for the 2
categorized groups (see Fig 2); however, they differed
slightly with respect to patient characteristics (see Appendix
1). Our study should be repeated, preferably
by intervention studies, for example, by comparing different
amount of use in 2 low-prevalence hospital
wards. However, in case of similarity, the need of other
strategies, such as implementing and using Standard
Precautions, in addition to hand hygiene performance
is necessary to prevent infections in both low- and
high-prevalence wards.
In most Norwegian hospitals, hand disinfectants
were introduced during the 1990s, but information as
to whether this has improved the rates of health careassociated
infections in Norway or in other countries
is limited. We tested this hypothesis and found that
use of alcohol-based hand products was significantly
associated with decreased infection rates at our hospital,
after controlling for use of hand soap. In particular,
we found a strong increase in the use of hand disinfectants
during the campaign in 2005 and a top in the use
of both hand soap and disinfectants after the campaign
in 2000. Although information and education seem to
have increased the use of hand disinfectants, we did
not see an immediate reduction in infection rates for
2005. A closer examination, however, revealed an infection
rate of 6.5% during the campaign months
April-June 2005, which was approximately 1% lower
than other prevalences this year (data not shown).
There are several strategies for infection control. It is
well-known that high level of hand hygiene compliance
lowers the risk of hospital infections. 19 Compliance
can be improved through education, motivation,
information campaigns, and audits, coaching, or feedback
to health personnel. 33-40 However, to maintain
high compliance over time, such interventions have
to be repeated regularly. Although extensive hand hygiene
performance is effective for disease control, a
simpler but more indirect control method is surveillance
and statistic process control of hospital infections.
Whenever infection rates are unacceptable
high, interventions may be directed at single wards or
health personnel. 41,42 Given the observed inverse association
between use of hand hygiene products and infection
rates in the present study, we believe that also
screening the use of hand hygiene products may be a
tool for infection control. Whenever use of hand disinfectants
is decreasing, specific interventions may be
performed to increase use, which may in turn lead to
lower infection rates.

316 Herudetal. American Journal of Infection Control
May 2009
In conclusion, by using data from a low-prevalence
hospital in Norway, we observed a modest inverse association
between use of hand hygiene products and
rates of infections. Quantifying use of such products
over time along with surveillance of hospital infections
may serve as an indicator for hand hygiene performance
in hospitals.
The authors thank Anne Dalheim at the Centre for Infection Control for administering
the point prevalence surveys at our hospital and to Ketil Kvernerod for providing
staff numbers.
References
1. Boyce J. It is time for action: improving hand hygiene in hospitals. Ann
Intern Med 1999;130:153-5.
2. Pittet D, Boyce JM. Hand hygiene and patient care: pursuing the Semmelweis
legacy. Lancet 2001;5(Suppl):9-20.
3. Pittet D, Simon A, Hugonnet S, Pessoa-Silva CL, Sauvan V, Perneger
TV. Hand hygiene among physicians: performance, beliefs and perceptions.
Ann Intern Med 2004;141:1-8.
4. Voss A, Widmer AF. No time for handwashing! Handwashing versus
alcohol rub: can we afford 100% compliance?. Infect Control Hosp Epidemiol
1997;18:205-8.
5. Whitby M, Pessoa-Silva CL, McLaws ML, Allegranzi B, Sax H, Larson E,
et al. Behavioural considerations for hand hygiene practices: the basic
building blocks. J Hosp Infect 2007;65:1-8.
6. Boyce JM, Pittet D. Guideline for hand hygiene in health-care settings.
Healthcare Infection Control Practices Advisory Committee, recommendations.
CDC. MMWR 2002;51(RR-16):1-44.
7. The Norwegian Institute of Public Health: (in Norwegian) Nasjonal veileder
for ha˚ndhygiene. Smittevern 2004; :11.fhi, NO-0403 Oslo, Norway.
8. The Norwegian Institute of Public Health: (in Norwegian) Evaluering.
Ren omsorg. Rapport 2006; 1.fhi, NO-0403 Oslo, Norway.
9. Tvedt C, Bukholm G. Alcohol-based hand disinfection: a more robust
hand-hygiene method in an intensive care unit. J Hosp Infect 2005;59:
229-34.
10. Pittet D. Compliance with hand disinfection and its impact on hospitalacquired
infections. J Hosp Infect 2001;48(Suppl A):S40-6.
11. Gordin FM, Schultz ME, Huber RA, Gill JA. Reduction in nosocomial
transmission of drug-resistant bacteria after introduction of an alcohol-based
handrub. Infect Control Hosp Epidemiol 2005;26:650-3.
12. Larson EL, Cimiotti J, Haas J, Parides M, Nesin M, Della-Latta PH, et al.
Effect of antiseptic handwashing vs alcohol sanitizer on health care-associated
infections in neonatal intensive care units. Arch Pediatr Adolesc
Med 2005;159:377-83.
13. Girou E, Loyeau S, Legrand P, Oppein F, Brun-Buisson Chr. Efficacy of
hand rubbing with alcohol-based solution versus standard handwashing
with antiseptic soap: randomised clinical trial. BMJ 2002;325:362.
14. Kac G, Podglajen I, Gueneret M, Vaupré S, Bissery A, Meyer G. Microbiological
evaluation of two hand hygiene procedures achieved by
healthcare workers during routine patient care: a randomized study.
J Hosp Infect 2005;60:32-9.
15. Lam BCC, Lee J, Lau YL. Hand hygiene practices in a neonatal intensive
care unit: a multimodal intervention and impact on nosocomial infection.
Pediatrics 2004;114:e565-71.
16. Rosenthal VD, Guzman S, Safdar N. Reduction in nosocomial infection
with improved hand hygiene in intensive care units of a tertiary care
hospital in Argentina. Am J Infect Control 2005;33:392-7.
17. Pittet D. Improving adherence to hand hygiene practice: a multidisciplinary
approach. Emerg Infect Dis 2001;7:234-40.
18. Gould DJ, Drey NS, Maralejo D, Grimshaw J, Chudleigh J. Interventions
to improve hand hygiene compliance in patient care. J Hosp Infect
2008;68:193-202.
19. Pittet D, Hugonnet S, Harbarth S, Mourouga Ph, Sauvan V, Touveneau
S, et al. Effectiveness of a hospital-wide programme to improve compliance
with hand hygiene. Lancet 2000;356:1307-12.
20. Haley RW, Culver D, White JW, Morgan WM, Emori TG, Munn P,
et al. The efficacy of infection surveillance and control programs in
preventing nosocomial infections in us hospitals. Am J Epidemiol
1984;121:182-205.
21. Sartor C, Delchambre A, Pascal L, Drancourt M, De Micco P, Sambuc
R. Assessment of the value of repeated point-prevalence surveys for
analyzing the trend in nosocomial infections. Infect Control Hosp Epidemiol
2005;26:369-73.
22. Gastmeier P, Geffers C, Brandt C, Zuschneid I, Sohr D, Schwab F, et al.
Effectiveness of a nationwide nosocomial infection surveillance system
for reducing nosocomial infections. J Hosp Infect 2006;64:16-22.
23. Orsi GB, Scorzolini L, Franchi C, Mondillo V, Rosa G, Venditti M. Hospital-acquired
infection surveillance in a neurosurgical intensive care
unit. J Hosp Infect 2006;64:23-9.
24. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions
for nosocomial infections. Am J Infect Control 1988;16:128-40.
25. Public health focus: surveillance, prevention, and control of nosocomial
infections. MMWR 1992;41:783-7.
26. Horan TC, Gaynes RP. Surveillance of nosocomial infections. In: Mayhall
CG, editor. Hospital epidemiology and infection control. 3rd ed.
Philadelphia: Lippincott Williams & Wilkins; 2004. p. 1659-702.
27. Davison AC, Hinkley DV. Bootstrap methods and their application.
New York: Cambridge University Press; 1997.
28. Aavitsland P, Stormark M, Lystad A. Hospital-acquired infections in
Norway: a national prevalence survey in 1991. Scand J Infect Dis
1992;24:477-83.
29. Scheel O, Stormark M. National prevalence survey on hospital infections
in Norway. J Hosp Infect 1999;41:331-5.
30. Eriksen HM, Iversen BG, Aavitsland P. Prevalence of nosocomial infections
in hospitals in Norway, 2002 and 2003. J Hosp Infect 2005;60:
40-5.
31. Pessoa-Silva CL, Hugonnet S, Pfister R, Touveneau S, Dharan S, Posfay-
Barbe K, et al. Reduction of health care-associated infection risk in neonates
by successful hand hygiene promotion. Pediatrics 2007;120:
e382-90.
32. Fendler EJ, Ali Y, Hammond BS, Lyons MK, Kelley MB, Vowell NA. The
impact of alcohol hand sanitizer use on infection rates in an extended
care facility. Am J Infect Control 2002;30:226-33.
33. Rykkje L, Heggelund A, Harthug S. Improved hand hygiene through
simple interventions. Tidsskr Nor Laegeforen 2007;127:861-3.
34. King S. Provision of alcohol hand rub at the hospital bedside: a case
study. J Hosp Infect 2004;56:S10-2.
35. Duerink DO, Farida H, Nagelkerke NJ, Wahyono H, Keuter M, Lestari
ES, et al. Preventing nosocomial infections: improving compliance with
standard precautions in an Indonesian teaching hospital. J Hosp Infect
2006;64:36-43.
36. Creedon SA. Healthcare workersÕ hand decontamination practices:
compliance with recommended guidelines. J Adv Nurs 2005;51:
208-16.
37. Kampf G. The six golden rules to improve compliance in hand hygiene.
J Hosp Infect 2004;56:S3-5.
38. Larson E. A tool to assess barriers to adherence to hand hygiene
guideline. Am J Infect Control 2004;32:48-51.
39. Scott AA, Hughes J, Hall D. Views and understanding of senior nursing
staff in relation to infection control. Br J Infect Control 2005;6:23-6.
40. Lankford M, Zembower TR, Trick WE, Hacek DM, Noskin GA, Peterson
LR. Influence of role models and hospital design on hand hygiene
of health care workers. Emerg Infect Dis 2003;9:217-33.
41. Randle J, Clarke M, Storr J. Hand hygiene compliance in healthcare
workers. J Hosp Infect 2006;64:205-9.
42. Pittet D. Infection control and quality health care in the new millennium.
Am J Infect Control 2005;33:258-67.

www.ajicjournal.org
Vol. 37 No. 4
Appendix 1 Characteristics of 27,248 patients
with infection status at Haukeland University Hospital,
Norway, 1998-2005, among wards with infections
rates .9% and wards with infection rates #9% at
study start in 1998.
Prevalence .9% Prevalence #9%
Characteristics No. % No. %
All 14,287 100.0 12,961 100.0
Survey time interval
January-March 3555 24.9 3396 26.2
April-June 3398 23.8 3155 24.3
July-October 3617 25.3 3145 24.3
November-December 3717 26.0 3265 25.2
Age
Unknown 12 0.1 17 0.1
,15 Yr 3087 21.6 399 3.1
15-34 Yr 2650 18.5 1491 11.5
35-54 Yr 2075 14.5 2837 21.9
55-74 Yr 3252 22.8 4523 34.9
.74 Yr 3211 22.5 3694 28.5
Gender
Woman 8510 59.6 6154 47.5
Man 5777 40.4 6807 52.5
Surgical operation
No 9827 68.8 10,206 78.7
Yes 4460 31.2 2755 21.3
Urinary tract catheter
No 12,500 87.5 11,449 88.3
Yes 1787 12.5 1512 11.7
Herud et al. 317