PEDIATRICS Vol. 120 No. 2 August 2007, pp. e382-e390 (doi:10.1542/peds.2006-3712)
ARTICLE |
Reduction of Health Care–Associated Infection Risk in Neonates by Successful Hand Hygiene Promotion
a Infection Control Program, Department of Internal Medicine
b Department of Pediatrics, Children's Hospital, University of Geneva Hospitals, Geneva, Switzerland
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVES. Hand hygiene promotion interventions rarely result in sustained improvement, and an assessment of their impact on individual infection risk has been lacking. We sought to measure the impact of hand hygiene promotion on health care worker compliance and health care–associated infection risk among neonates.
METHODS. We conducted an intervention study with a 9-month follow-up among all of the health care workers at the neonatal unit of the Children's Hospital, University of Geneva Hospitals, between March 2001 and February 2004. A multifaceted hand hygiene education program was introduced with compliance assessed during successive observational surveys. Health care–associated infections were prospectively monitored, and genotypic relatedness of bloodstream pathogens was assessed by pulsed-field gel electrophoresis. A comparison of observed hand hygiene compliance and infection rates before, during, and after the intervention was conducted.
RESULTS. A total of 5325 opportunities for hand hygiene were observed. Overall compliance improved gradually from 42% to 55% across study phases. This trend remained significant after adjustment for possible confounders and paralleled the measured increase in hand-rub consumption (from 66.6 to 89.2 L per 1000 patient-days). A 9-month follow-up survey showed sustained improvement in compliance (54%), notably with direct patient contact (49% at baseline vs 64% at follow-up). Improved compliance was independently associated with infection risk reduction among very low birth weight neonates. Bacteremia caused by clonally related pathogens markedly decreased after the intervention.
CONCLUSIONS. Hand hygiene promotion, guided by health care workers' perceptions, identification of the dynamics of bacterial contamination of health care workers' hands, and performance feedback, is effective in sustaining compliance improvement and is independently associated with infection risk reduction among high-risk neonates.
Key Words: neonatal care • very low birth weight • NICU • health care–associated infection • cross-infection • hand hygiene • hand-washing • alcohol-based hand rubbing • behavioral sciences • hand contamination • molecular epidemiology • Staphylococcus epidermidis • prospective study • intervention
Abbreviations: HCW—health care worker • CRIB—Clinical Risk Index for Babies • VLBW—very low birth weight
Health care–associated infection is the leading, preventable adverse event in acutely ill patients and is associated with considerable morbidity, mortality, and additional use of resources.1,2 Hand hygiene is recognized as the single most important preventive measure,3 but compliance with recommendations is particularly difficult to achieve when caring for critically ill neonates.4 Average hospital-wide compliance with hand hygiene significantly improved at the University Hospitals of Geneva during a sustained multimodal promotion campaign including increased recourse to alcohol-based hand rub from 1995 through 2001.5,6 However, compliance averaged only 40% in the neonatal unit in 2001.
Successful promotion interventions have used different approaches including system changes, education, performance feedback, reminders, and motivation, yet sustained improvement has rarely been achieved.5,7 Furthermore, it has been suggested that the lack of scientific evidence showing the extent to which hand hygiene can impact on health care–associated infection risk in intensive care is a concern.8 Hand hygiene prevents cross-infection,9 and several studies observed a reduction in health care–associated infection rates that paralleled compliance improvement.4,5,10–13 The purpose of this study was to evaluate the impact of successful hand hygiene promotion on individual infection risk reduction among neonates.
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METHODS |
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Setting and Participants
The study was conducted from March 1, 2001, to February 29, 2004, in the neonatal unit of the University of Geneva Hospitals, a large referral center that provides primary and tertiary medical care for residents of Geneva, Switzerland, and the surrounding area (
800000 population).
Approximately 700 neonates (5200 patient-days) are admitted annually to the 20-bed unit. Hand-washing facilities are conveniently located throughout, with 1 sink in each of the 3 wards. The use of an alcohol-based hand rub (Hopirub; B Braun, Sempach, Switzerland) has been the primary agent for hand hygiene since 19955 and is widely available. All health care workers (HCWs) in the neonatal unit during the study period were eligible for inclusion in hand hygiene compliance surveys. All of the neonates hospitalized for 
48 hours were included in the surveillance of health care–associated infections. The average patient-to-nurse ratio was 3:2 and 1:1 in the intermediate and intensive care sections, respectively. Clinical staff included 17 physicians and 84 registered nurses. The study was approved by the institutional review board, and all of the participating HCWs provided oral consent.
Study Design
The study was conducted in 3 phases. The baseline phase (phase 1, 9 months) consisted of studies on the dynamics of HCW hand contamination during routine care14 and the evaluation of HCWs' beliefs and perceptions toward hand hygiene using concepts derived from the behavioral sciences.15,16 Baseline compliance with hand hygiene was also assessed during this phase. The intervention (phase 2, 18 months) was based on the results of studies conducted during phase 1. Follow-up (9 months) was conducted in phase 3, where no active intervention was performed. Hand hygiene observation surveys were conducted at months 1, 5, and 9 during phase 3. Continuous prospective surveillance of health care–associated infections was performed throughout the entire study period.
Baseline Studies (Phase 1)
From March 26 to April 9, 2001, structured observation sessions were conducted to evaluate the dynamics of bacterial contamination of HCWs' hands during neonatal care as described previously.14 A sequence of care began when the HCW performed hand hygiene and ended when the activity changed or hand hygiene was performed again; 149 sequences of care were observed. An imprint of the 5 fingertips of the dominant hand was taken before and after hand hygiene action and at the end of a sequence of care. The study results have been published elsewhere.14 In brief, all types of contact, including contact with the patient surroundings, were associated with significant contamination.14 The data confirm that hands become progressively contaminated with commensal flora and potential pathogens during neonatal care and identify activities at higher risk for hand contamination.14 They also reinforce the need for hand hygiene after a sequence of care, before starting a different task, and after glove removal.
In May 2001, an anonymous self-report questionnaire (75 items) based on the theory of planned behavior15,16 was distributed to 80 neonatal HCWs to assess intention to comply, attitude toward hand hygiene, behavioral and subjective norm perceptions, and perception of difficulty to comply.15 Seventy-five percent of responders believed that they could improve their compliance with hand hygiene. The only variables independently associated with intention to comply were the individual's perception of the difficulty or ease in performing hand hygiene and a positive perception of how superiors valued hand hygiene.15 These results highlight the importance of the opinion of superiors and a strong perceived control over the difficulty to comply with hand hygiene as possible internal factors that may influence compliance.
In June 2001, compliance with hand hygiene was measured (see below).5,14,17 Overall compliance was 42% but only 33% in the case of contact with patient surroundings.
Intervention (Phase 2)
The intervention included reminders in the workplace (posters), focus group sessions, and feedback on hand hygiene performance and infection rates. Assessment of HCWs' beliefs and perceptions toward hand hygiene was used to guide focus group sessions (groups of 8–12 HCWs) with the participation of superiors (head nurse and head physician). The first group of sessions was held from November 2001 to January 2002 and in November 2002 and January 2003 for HCWs employed after January 2002. These sessions included education on hand hygiene indications and technique, hand hygiene performance feedback, and discussion of the previous evaluation of the dynamics of bacterial contamination of HCWs' hands during routine care,14 as well as feedback and discussion of the previous assessment of HCWs' beliefs toward hand hygiene.15 The second group of sessions was held in May 2003 and included hand hygiene performance feedback, discussion of observed risk factors for noncompliance with hand hygiene, and hand hygiene compliance and its possible impact on infection rates. Emphasis was placed on identifying solutions to overcome difficulties to comply with hand hygiene. In particular, during the first group of sessions, we addressed the need to reduce unnecessary contact with the patient's immediate surroundings during interruptions in patient care through a reorganization of the care process (ie, review of the organization of all of the necessary material before starting procedures, thus requiring less interruptions in care to procure missing material, as described previously and based on previous experience at our institution18). The intervention activities triggered discussion among the nursing staff on the review and improvement of neonatal care procedures, and 1 member of the research team (Ms Touveneau) was regularly solicited across phase 2 to provide advice on clean care.
Compliance With Hand Hygiene
Eight surveys on hand hygiene compliance were performed as previously described.5,17 Each survey lasted 2 to 3 weeks. A previously trained and validated5,14,17 single observer (Ms Touveneau) conducted most (65%) observation sessions across the 3 study phases. A second observer (Dr Pessoa-Silva) participated; cross-validation between the 2 observers was performed before the beginning of the study as reported previously.5,17 Overall compliance with hand hygiene was monitored during neonatal care using 20-minute structured overt observation sessions randomly distributed over all of the weekday shifts. Potential opportunities for hand hygiene and the actual number of episodes of hand washes/hand rubs performed were recorded according to established criteria.3,5,17 Hand-washing referred to washing hands with either unmedicated or medicated soap and water, and hand-rubbing to the use of the alcohol-based solution. Indications for hand hygiene were defined according to international standards.3,7 Direct patient contact included contact with skin, respiratory tract secretions, secretions other than respiratory (mucous and oral), vascular access line (ie, blood sampling and intravenous set connections), and change of diapers. Contact with the patient's immediate surroundings was defined as contact with equipment in close proximity to the neonate (ie, incubator, monitoring device, and ventilator). Alcohol-based hand-rub consumption was measured as a process indicator.
Surveillance of Neonatal Infections
An infection control nurse (Ms Touveneau) visited the unit 3 times a week (Monday, Wednesday, and Friday) and conducted prospective on-site surveillance of health care–associated infections. All of the neonates were followed up from admission to discharge. Identification of infections was obtained by means of chart review, participation in ward rounds, information from physicians and nursing staff, direct observation of neonates, and review of laboratory reports.18,19 The infection control nurse also held regular meetings with a neonatologist (Dr Pfister) and a pediatric infectious disease specialist (Dr Pessoa-Silva) to review all of the subjects with suspected infection. Standard definitions for health care–associated infections were used.19 Isolates were defined as bloodstream pathogens if signs of infection were present at the time of collection.19 All of the infections, except those known or proven to have been acquired transplacentally (eg, herpes simplex, toxoplasmosis, rubella, cytomegalovirus, and syphilis) were considered health care associated. The definition of conjunctivitis was broadened to include eye discharge with empiric antibiotic treatment. Health care–associated infections that developed within 48 hours of life were considered of maternal origin; later infections were considered of hospital origin.20 Device-associated infection was defined as an infection with a device (ie, ventilator or central vascular catheter) used within 48 hours before infection onset.21 Variables recorded included birth weight; gestational age; and daily exposure to mechanical ventilation, short-term central vascular catheterization (including umbilical and peripherally inserted central venous catheters), or other invasive devices (ie, thoracic drain, abdominal drain, arterial catheter, totally implanted, long-term venous catheter, urinary catheter, dialysis catheter, and suprapubic catheter); parenteral nutrition; antibiotic use; and the Clinical Risk Index for Babies (CRIB)22 score for very low birth weight (VLBW) infants (<1500 g).
Microbiologic Studies
Blood samples were inoculated using Bactec-Peds Plus (BD Diagnostics, Franklin Lakes, NJ) pediatric blood culture bottles and incubated for 120 hours. Strains were identified using the Vitek GNI card for Gram-negative bacteria and Vitek GP card for Staphylococcus species (Vitek system, bioMérieux, Hazelwood, MO).
Genotyping of bloodstream pathogens was conducted by pulsed field gel electrophoresis.23 The restriction enzymes, XbaI for Escherichia coli and SmaI for Staphylococcus epidermidis, were used according to manufacturer's instructions (Roche Applied Science, Roche Diagnostics (Schweiz) AG, Rotkreuz, Switzerland). Macrorestriction patterns were compared both visually24 and by using the Bionumerics software 3.5 (Applied Maths, Kortrijk, Belgium).
Statistical Analysis
Two periods were compared to evaluate the impact of the hand hygiene promotion intervention on compliance and health care–associated infections: the period before the intervention started (phase 1) and the period after the initiation of the intervention (pooled phases 2 and 3). Categorical variables were compared using the 
2 test or Fisher's exact test and continuous variables using Student's t test or nonparametric methods when appropriate. We used Stata 7 (Stata Corp, College Station, TX) for all of the analyses. All of the tests were 2-tailed, and P < .05 was considered statistically significant.
Compliance With Hand Hygiene
Compliance with hand hygiene before (phase 1) and after (phases 2 and 3) the intervention had started was compared. The dependent variable was compliance with hand hygiene, and the explanatory variable was the intervention. Adjustment for potential confounders included the following: professional category (physician or nurse), time of day, patient location, type of contact, and activity index (defined as the number of hand hygiene opportunities per hour of care during each observation period).5,17 Logistic regression models were used for multivariate analysis. To account for interdependence of observations performed within the same 20-minute observation session, we used robust estimates of variance (generalized estimating equations) by including each session as a cluster.5,17,25
Health Care–Associated Infections
Health care–associated infection rates per 1000 patient-days were calculated using only infections of hospital origin (after 48 hours of life).26 The occurrence of patients with health care–associated infection before (phase 1) and after (phases 2 and 3) the intervention started was compared. Patients admitted before the beginning of the intervention but still present in the unit were excluded from the analysis (n = 13). We used logistic regression to assess the association between the first episode of infection and the intervention. In models for VLBW neonates, potential confounders included severity index (CRIB), infection of maternal origin, Apgar score at 5 minutes of life, and duration of parenteral nutrition, device exposure, and antibiotic use before the infection. Length of stay was not included in the model because of a strong correlation with the duration of the exposure to invasive devices. Variables with P < .25 in the bivariate analysis were tested in the multivariate analysis, and those associated with the outcome with a P < .05 were kept in the final model.27
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RESULTS |
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Patient and Unit Characteristics
Of 1127 neonates housed in the unit for
2 days during the study period, 1114 were included in the analysis for a total of 17066 patient-days. Thirteen patients were excluded because of admission before the beginning of the intervention. Patient and unit characteristics are described in Table 1. Case mix as estimated by birth weight, gestational age, and CRIB score was stable over the study period. The average bed occupancy rate was slightly higher during the follow-up period (P < .001). Median length of stay was comparable across the study phases (phase 1: 6 days; phase 2: 8 days; phase 3: 8 days; P = .15). However, length of stay among VLBW neonates was significantly longer in phase 1 as compared with phases 2 and 3 (phase 1: 46 days; phase 2: 28 days; phase 3: 22 days; P = .008).
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Compliance With Hand Hygiene and Hand-Rub Consumption
Of 5325 opportunities for hand hygiene, 3555 were related to direct patient contact and 1770 to contact with equipment in the patient's immediate surroundings (Table 2). Hand-rubbing was used in 91% (2315 of 2550) of all hand hygiene episodes. Overall compliance improved significantly across the 3 study phases and paralleled the increase in hand-rub consumption (Table 2). Hand-rub use increased in phase 2 (intervention period) versus phase 1 (P = .025) and continued to increase in phase 3 (follow-up) versus phase 2 (P = .037). Because of a decrease in contact with patient surroundings, the median activity index decreased markedly between phases 1 and 2 and remained stable in phase 3 (Table 2). Compliance with hand hygiene after contact with surroundings remained stable across the study (phase 1: 33%; phase 2: 39%; phase 3: 37%). Whereas 51% of opportunities for hand hygiene were related to direct patient contact in phase 1, this rose to 66% in phase 2 and 75% in phase 3 (Table 2). Compliance improvement with direct patient contact was sustained over time (49% at baseline vs 64% at last follow-up survey; P < .001). The impact of the intervention remained significant after adjustment for possible confounders (Table 3).
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Impact of Hand Hygiene Promotion on Health Care–Associated Infection
Although 73 neonates had an infection of maternal origin, 99 acquired a total of 150 episodes of health care–associated infections after >48 hours of life. Table 2 shows the number of infected patients and the distribution of health care–associated infections across the 3 study phases. The overall rates of health care–associated infection per 1000 patient-days across the study phases were 11.1 (48 of 4322), 7.9 (70 of 8846), and 8.2 (32 of 3898) in phases 1, 2, and 3, respectively. VLBW infants represented only 19.2% (214 of 1114) of the study population but acquired most of the later infections (103 of 150 [69%]). Overall, 28.5% of VLBW neonates had
1 health care–associated infection as compared with only 4.2% of heavier infants (P < .001). Among the 150 infections, 100 were considered severe, and 80% occurred among VLBW neonates. Among VLBW neonates, the rates of health care–associated infection per 1000 patient-days across the study phases were 15.5 (42 of 2718), 10.7 (47 of 4381), and 8.8 (14 of 1599) in phases 1, 2, and 3, respectively. After adjustment for possible confounders for the risk of acquiring health care–associated infection, an independent protective effect of the intervention was observed among VLBW neonates (Table 4).
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Distribution of Genetically Related Bloodstream Pathogens
During the study period, 37 episodes (37 of 57 [65%]) of bloodstream infection of hospital origin were laboratory confirmed; of these, 89% (33 of 37) developed in VLBW neonates. Nineteen of the 37 bloodstream isolates were distributed in genetically related genotypes: 1 E coli genotype (3 isolates) and 5 distinct genotypes of S epidermidis (Fig 1). A clear cluster of E coli was observed during the baseline period, and 7 of 16 genetically related genotypes of S epidermidis also occurred in this study phase. All but 1 genetically related genotype were recovered from VLBW neonates. The incidence of bloodstream infections caused by genetically related genotypes was much higher (2.3 per 1000 patient-days) before than after the intervention started (0.7 per 1000 patient-days; incidence density ratio: 3.3; P = .012).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Most studies assessing the impact of hand hygiene on health care–associated infection4,5,10,12,13,28–35 show a temporal relation between improved practices and reduced infection rates. However, none of these studies could determine a causal relation because of the lack of statistical significance, presence of confounding factors, or the absence of randomization. To the best of our knowledge, this study is the first to evaluate the impact of hand hygiene promotion on the infection risk adjusted for individual patient's characteristics that might confound the occurrence of infection. Successful hand hygiene promotion was independently associated with a 60% decrease in the risk of health care–associated infection among VLBW neonates.
Consistent with health care–associated risk reduction, the occurrence of genetically related clones decreased after the intervention. S epidermidis species contributed to most cases of genetically related isolates. Indeed, S epidermidis, the most common infectious pathogen of hospital origin among neonates,36 may become established in neonatal units for several years and be cross-transmitted between infants.36–40 Strategies to improve infection control practices, such as hand hygiene, should impact on cross-transmission and occurrence of epidemic clones.40
Three particular aspects contribute to the uniqueness of the current intervention. The first is the use of behavioral sciences to evaluate HCWs' cognitive determinants associated with intention to perform hand hygiene15 and to model interventions accordingly. Hand hygiene behavior varies significantly among HCWs within the same institution or ward,17 thus suggesting that individual features could play a crucial role in determining behavior. Social cognitive models have been applied to evaluate HCWs' cognitive determinants toward hand hygiene behavior41–43 and to promote hand hygiene.44 Behavioral sciences offer tools to help understand individual determinants of behavior16 and may provide additional insight.45–47
The second aspect particular to this intervention was the evaluation of the dynamics of bacterial contamination of HCWs' hands during routine neonatal care,14 discussion of the results during focus group sessions, and the resulting reorganization of the work process. Discussions highlighted the types of contact significantly associated with hand contamination and emphasized the need to reduce all unnecessary contact. Few studies support current guidelines on indications for hand hygiene7,48 and, more importantly, opportunities for an optimal timing of hand cleansing in the neonatal setting have never been defined. The feedback on the evaluation of the dynamics of hand contamination may have had an impact on the process of care with a subsequent reduction of the number of contacts with the patient's immediate surroundings. Subsequently, this intentional decrease in the number of hand hygiene opportunities allowed us to achieve a sustained increase in compliance.
The third aspect was staff feedback on hand hygiene performance and predictors of compliance in conjunction with feedback on the impact on health care–associated infection rates. These provided an additional opportunity to discuss means to overcome barriers to compliance and to reinforce HCWs' positive attitude toward hand hygiene.
The intervention improved hand hygiene, and its effect remained significant after adjustment for possible confounders. Interestingly, compliance with hand hygiene at time of direct patient contact remained stable in phase 2 compared with phase 1 but increased in phase 3. This can be explained by the fact that the various components of the intervention were implemented sequentially during phase 2, and their measurable effect on compliance became apparent only later. Previous studies have evaluated the possible impact of hand hygiene promotion in the neonatal setting.4,12,49–52 Among these, 3 included a follow-up period,4,12,52 but only 1 evaluated the impact of the intervention on hand hygiene compliance adjusted for possible confounders.50 Our intervention was independently associated with sustained hand hygiene improvement.
The main limitation of the present study is the lack of randomization. Methodologic and ethical concerns make it difficult to conduct randomized, controlled trials with an appropriate sample size that could establish the relative importance of hand hygiene in the prevention of health care–associated infections. Because the intervention was multimodal, it is therefore impossible to assess the relative efficacy of each component. In particular, despite the fact that the reorganization of procedures occurred after focus group discussion, a systematic monitoring of changes in practices was beyond our capacity. However, this deserves additional research in different patient populations, considering the critical importance of timely performed hand hygiene in the complex sequence of patient care.7 Newly developed tools for hand hygiene promotion should consider clear-cut indications for action and the reorganization of care procedures.53 Finally, some bias may have influenced the observed effect of the intervention. The baseline studies might have affected compliance and infection rates measured during phase 1 in the direction of higher compliance and lower infection rates. If this occurred, then the observed effect of the intervention would be underestimated. We are consequently confident about the validity of the results. In addition, the overt observation might have distorted the observed compliance. However, the steady increase in hand-rub–solution consumption over the study period rules out this phenomenon as the reason for improved compliance.
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Although it remains important to generate additional scientific and causal evidence for the impact of enhanced adherence with hand hygiene on infection rates in health care settings, these results indicate that improved practices reduce the risk of pathogen cross-transmission and health care–associated infection. Recently, new technologies have guaranteed the survival of neonates who would have died previously, and more premature infants now succeed to overcome the challenging start of life. Almost half a century after the first steps of neonatal special intensive care, infectious complications are still a paradigm to defeat. This study disclosed that hand hygiene promotion was independently associated with a significant decrease in infection risk among the most fragile pediatric population, VLBW neonates, and represents a step forward toward improved neonatal care.
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ACKNOWLEDGMENTS |
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Dr Pessoa-Silva is a postdoctoral fellow from the Universidade Federal do Rio de Janeiro (Rio de Janeiro, Brazil). She received a grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (200694/99–5). She was also recipient of a grant from the University of Geneva Faculty of Medicine (PRD-02-11-05). Dr Hugonnet was the recipient of a research grant from the Swiss National Science Foundation (32–68164.02).
We thank the HCWs of the neonatal unit of the University of Geneva Hospitals for adherence to the project and support. We are indebted to Nadia Colaizzi for data management and Rosemary Sudan for providing editorial assistance.
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FOOTNOTES |
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Accepted Apr 3, 2007.
Address correspondence to Didier Pittet, MD, MS, Infection Control Program, Department of Internal Medicine, University of Geneva Hospitals, 24 Rue Micheli-du-Crest, 1211 Geneva 14, Switzerland. E-mail: didier.pittet{at}hcuge.ch
The authors have indicated they have no financial relationships relevant to this article to disclose.
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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics
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