Nurse staffing levels and the incidence of mortality and morbidity in the adult intensive care unit: A literature review

Nurse staffing levels and the incidence of mortality and morbidity in the adult intensive care unit: A literature review

Australian Critical Care (2012) 25, 64—77 LITERATURE REVIEW Nurse staffing levels and the incidence of mortality and morbidity in the adult intensive...

281KB Sizes 0 Downloads 81 Views

Australian Critical Care (2012) 25, 64—77

LITERATURE REVIEW

Nurse staffing levels and the incidence of mortality and morbidity in the adult intensive care unit: A literature review Matthew McGahan BN, Grad Cert Intensive Care Nursing, RN a,∗, Geraldine Kucharski BN, Dip App Sc (Nursing Management), MHA, RN a,c, Fiona Coyer MSc Nursing, PGCEA, PhD, RN b,d , Winner ACCCN Best Nursing Review Paper 2011 sponsored by Elsevier a Department of Intensive Care Medicine, Royal Brisbane & Women’s Hospital, Butterfield St, Herston QLD 4006, Australia b School of Nursing and Midwifery, Queensland University of Technology, Victoria Park Rd, Kelvin Grove, QLD 4059, Australia

Received 28 June 2011 ; received in revised form 28 February 2012; accepted 13 March 2012

KEYWORDS Intensive care; Review; Adverse; Client—staff ratios; Mortality; Infection

Summary Background: Studies have shown that nurse staffing levels, among many other factors in the hospital setting, contribute to adverse patient outcomes. Concerns about patient safety and quality of care have resulted in numerous studies being conducted to examine the relationship between nurse staffing levels and the incidence of adverse patient events in both general wards and intensive care units. Aim: The aim of this paper is to review literature published in the previous 10 years which examines the relationship between nurse staffing levels and the incidence of mortality and morbidity in adult intensive care unit patients. Methods: A literature search from 2002 to 2011 using the MEDLINE, Cumulative Index to Nursing and Allied Health Literature (CINAHL), PsycINFO, and Australian digital thesis databases was undertaken. The keywords used were: intensive care; critical care; staffing; nurse staffing; understaffing; nurse—patient ratios; adverse outcomes; mortality; ventilator-associated pneumonia; ventilator-acquired pneumonia; infection; length of stay; pressure ulcer/injury; unplanned extubation; medication error; readmission; myocardial infarction; and renal failure. A total of 19 articles were included in the review. Outcomes of interest are patient mortality and morbidity, particularly infection and pressure ulcers. Results: Most of the studies were observational in nature with variables obtained retrospectively from large hospital databases. Nurse staffing measures and patient



Corresponding author. Tel.: +61 4 0764 1048; fax: +61 7 3818 7775. E-mail addresses: [email protected] (M. McGahan), Geraldine [email protected] (G. Kucharski), [email protected] (F. Coyer). c Tel.: +61 7 3636 5966; fax: +61 7 3636 3542. d Tel.: +61 7 3138 3895; fax: +61 7 3138 3814. 1036-7314/ $ — see front matter © 2012 Australian College of Critical Care Nurses Ltd. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.

doi:10.1016/j.aucc.2012.03.003

The incidence of mortality and morbidity

65

outcomes varied widely across the studies. While an overall statistical association between increased nurse staffing levels and decreased adverse patient outcomes was not found in this review, most studies concluded that a trend exists between increased nurse staffing levels and decreased adverse events. Conclusion: While an overall statistical association between increased nurse staffing levels and decreased adverse patient outcomes was not found in this review, most studies demonstrated a trend between increased nurse staffing levels and decreased adverse patient outcomes in the intensive care unit which is consistent with previous literature. While further more robust research methodologies need to be tested in order to more confidently demonstrate this association and decrease the influence of the many other confounders to patient outcomes; this would be difficult to achieve in this field of research. © 2012 Australian College of Critical Care Nurses Ltd. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.

Introduction Adequate nurse staffing levels are indistinguishably linked to positive patient outcomes in both general ward settings and in critical care areas, including the intensive care unit (ICU).1,2 However, determining what is considered adequate nurse staffing levels is an area of contention in hospitals worldwide. The increasing need for critical care beds, combined with decreasing budgets and nurse shortages may lead to situations whereby nurse staffing adequacy is suboptimal and patient safety is compromised. Professional bodies such as the Australian College of Critical Care Nurses (ACCCN),3 British Association of Critical Care Nurses (BACCN),4 and American Association of Critical Care Nurses (AACN)5 have set minimum standards on nurse staffing levels in order to overcome staffing inadequacy and to provide safe patient care focused on quality and desired patient outcomes. The state of California in the United States mandated minimum nurse-to-patient ratios in 2004 in the general hospital population, to assess its effect on key measures of nursing quality. A study performed two years after regulation found that while the amount of licensed nursing staff increased due to this mandate, significant improvements in the incidence of falls and prevalence of hospital-acquired pressure ulcers were not seen.6 Over the past 10 years, numerous studies have been conducted to examine the relationship between nurse staffing levels and patient outcomes such as mortality,7—16 failure-to-rescue and complications,7—10,14,16—18 infection rates,10,11,16—19 pressure ulcer development,10,11,16,18 falls,11,18—20 length of stay,16,21 and medication errors11,19 ; with varying degrees of results. These studies either focused on outcomes at a general ward level or aggregated their results at a hospital level, hence not

providing a clear insight into the relationship between nurse staffing levels and patient outcomes in the intensive care environment. Nurse staffing levels in the intensive care environment vary from that of wards and other hospital services for many reasons. In the Australian context, the nurse-to patient ratio is significantly higher in the intensive care unit as the ACCCN have mandated a 1:1 nurse—patient ratio due to the increased acuity of the patients, the need for continuous monitoring and observations, and the management of technological life supporting equipment. The use of float nurses or access nurses is required to support the nurse in tasks which require more than one nurse to complete. An access nurse may also be quarantined to accept an emergency admission, reduce entry block to the ICU or be a contingency for unexpected staff absence or education requirements.3 In addition, the total amount of ‘staff per bed’ employed in the intensive care unit is also higher as the same amount of patient care staff is required to be rostered on around the clock as opposed to decreasing staff numbers on night shifts as often occurs in the ward setting. Given these unique staffing requirements, it is necessary to review the literature which explores the relationship between nurse staffing levels and patient outcomes specific to the intensive care area.

Background The relationship between nurse staffing levels and the incidence mortality and morbidity in the intensive care setting has been extensively examined in the literature. Two recently published reviews22,23 examining this relationship failed to find an overall significant association between nurse staffing levels and the incidence of mortality and adverse events in the intensive care setting. Numata et al.22

66 conducted a meta-analysis of five included studies and found a positive relationship between higher nurse staffing levels and lower mortality; however after adjusting for various co-variates within each study, the individually reported associations between high nurse staffing levels and low hospital mortality became non-significant in all but one study. Similarly, West et al.23 examined 15 studies in their review and found that only 2 studies reported a statistical association between nursing resources and both mortality and adverse events; one reported an association to mortality only; seven studies reported they could not reject the null hypothesis of no relationship to mortality; and 10 studies reported a relationship to adverse events. The difficulty in ascertaining an association between nurse staffing levels and mortality and morbidity is thoroughly discussed in both of these reviews. The majority of the studies in these two reviews were observational and retrospective in nature making fully adjusting for confounding factors difficult. West et al.23 noted that the majority of studies in their review were cross-sectional in design, which causes difficulties in inferring causal relationships due to data being collected at one point in time. The potential for inaccurate coding of patient characteristics and nurse staffing measures in administrative databases may distort the actual relationship between nurse staffing levels and adverse outcomes. Numata et al.22 also discussed a possible lack of sensitivity between mortality and nurse staffing levels due to the nature and severity of patient diagnosis; lack of standardised nurse staffing and outcome measures; minimal variation in staffing levels in the ICU; skill mix; and the contribution of other staff as potential factors which may make documenting an association between nurse staffing levels and mortality difficult. While the reviews by Numata et al.22 and West et al.23 have only been recently published, the included studies in these reviews are not as contemporary, dating from 1994 to 2004 and 1993 to 2002 respectively. As numerous studies have been published in the six years since 2004, another review of this topic was deemed appropriate.

M. McGahan et al. event or outcome are considered eligible for inclusion into this review under the term morbidity.

Search methods Electronic databases were searched along with manual searches of reference lists from selected electronic articles, and Internet search engines to find relevant literature on the effect of nurse staffing levels on patient mortality and morbidity in the intensive care setting. The MEDLINE, CINAHL, PsycINFO, and Australian digital thesis databases were searched; along with Google Scholar search engine with the terms: intensive care; critical care; staffing; nurse staffing; understaffing; nurse—patient ratios; adverse outcomes; mortality; ventilator-associated pneumonia; ventilatoracquired pneumonia; infection; length of stay; pressure ulcer/injury; unplanned extubation; medication error; readmission; myocardial infarction; and renal failure. The search included only articles written in the English language from the previous 10 years (January 2002 to March 2011). Articles were included if they were: (1) quantitative studies; (2) studies which measured nurse staffing levels against patient outcomes; (3) studies of adult patients; and (4) studies specific to the intensive care environment; or the study contained a subanalysis of results specific to the intensive care setting. Articles were excluded if they were: (1) specifically studying the paediatric or neonatal population; (2) studies focusing on nurse staffing levels at the ward level; and (3) studies which only displayed results at a hospital level. A total of 95 articles were retrieved from the initial search; of which 51 were excluded as they were: (1) systematic reviews; (2) literature reviews; (3) reports; and (4) expert opinion papers. Articles which met the initial search criteria but upon perusal did not relate to the aim of this paper were also excluded. All abstracts of the remaining 44 original study articles were reviewed and a further 25 were excluded as they did not meet the above inclusion criteria. A total of 19 articles were included in this review (see Fig. 1).

Aims Results The aim of this paper is to review literature to examine the relationship between nurse staffing levels and the incidence of mortality and morbidity in adult intensive care unit patients. Studies which examine the relationship between nurse staffing levels and any adverse patient

Among the articles that met the inclusion criteria, seven studies observed the incidence of mortality (see Table 1); 13 studies observed the incidence of infection (see Table 2); and three studies observed the incidence of pressure ulcer

Studies examining nurse staffing levels and mortality.

Author, year of publication Cho et al.,

28

2008

Cho and Yun,29 2009

Stone et al.,24 2007

Population studied

Study method

Nurse staffing measure

Findings

n = 27,372; 42 tertiary and 194 secondary hospital ICUs in Korea

Retrospective study from a large administrative database

Every additional patient per RN associated with increased risk of death

n = 6957; stroke patients admitted to ICUs of 185 Korean hospitals n = 15,846; elderly patients in 51 ICUs of 31 American hospitals

Cross sectional design of survey and administrative data Observational data from NNIS and Medicare files, administrative data, American Hospital Association annual survey, and RN survey Observational, single-centre, prospective study

Ratio of average daily census to total number of RN fulltime equivalent (FTE) Bed-to-nurse ratio (total beds: total FTE RN)

Kiekkas et al.,30 2008

n = 396; medical—surgical ICU patients in 1 Greek hospital

Van den Heede et al.,27 2009

n = 9054; cardiac surgery patients in 58 Belgian ICUs and 75 general nursing units n = 129,579; patients from 453 nursing units (171 ICU and 282 non-ICU) in 123 Veteran Health Administration hospitals n = 26,186; general patients admitted to 31 ICUs in Austria

Sales et al.,31 2008

Metnitz et al.,32 2004

RN hours per patient day (RN HPPD)

Therapeutic Intervention Scoring System (TISS-28) to nurse ratio

Better ICU staffing levels associated with lower mortality Higher staffing levels significantly associated with lower mortality

The incidence of mortality and morbidity

Table 1

Clinically significant trend in increased mortality with increased workload; however not statistically significant ICU staffing levels were not significantly associated with mortality

Observational study using administrative data

Nursing hours per patient day (NHPPD)

Retrospective observational study using administrative data

RN hours per patient day (RNHPPD)

Nil significant association found between ICU staffing levels and mortality

Prospective multi-centre cohort study

Nurse-to-patient ratio; work-to-utilisation ratio

Nil significant association between ICU nurse staffing levels and mortality

67

68

Table 2

Studies examining nurse staffing levels and infection.

Author, year of publication Population studied

Study method

Nurse staffing method

Findings

Dancer et al.,33 2006

Retrospective study using hospital databases Single centre cohort study

Nursing workload (TISS)

Increased MRSA acquisition with nurse understaffing Staff deficit associated with MRSA transmission MRSA transmission when nurses are overloaded by 25% Understaffing associated with transmission of all pathogens Higher nurse-to-patient ratio associated with lower risk of late on-set VAP Lower nurse-to-patient ratio associated with VAP and other complications

Grundmann et al.,34 2002 Blatnik and Lesnicar,35 2006 Halwani et al.,36 2006 Hugonnet et al.,37 2007 Dang et al.,42 2002

Stone et al.,24 2007

Blot et al.,38 2011

Shuldham et al.,25 2009

n = 174; patients admitted to one ICU in Scotland n = 782; all patients admitted to one ICU in UK n = 297; patients admitted to surgical ICU in Slovenia n = 430; adult ICU in United Kingdom n = 2470; ventilated ICU patients in Switzerland n = 2606; all ICU patients undergoing abdominal aortic surgery in 52 hospitals in Maryland n = 15,846; elderly patients in 51 ICUs of 31 American hospitals

n = 1658; ICU patients treated for pneumonia or received mechanical ventilation in 27 ICUs in 9 European countries n = 23,192 adults admitted to two hospitals in England

Prospective study Prospective longitudinal Prospective, observational, single-centre cohort Secondary analysis of hospital discharge data; surveys

Observational data from NNIS and Medicare files, administrative data, American Hospital Association annual survey, and RN survey Prospective, observational survey

Case study using retrospective hospital data

n = 4535; all patients in eight ICUs of six hospitals in United States

Prospective, observational, multi-centre, cohort study

Whitman et al.,26 2002

n = 95 patient care units across ten acute care hospitals in United States n = 366; medical ICU in Switzerland; Length of stay >7 days

Secondary analysis of prospective, observational data Comparison of case-crossover, cohort, and case-time-control designs; prospective surveillance Observational, single-centre, prospective cohort study

Hugonnet et al.,40 2007

Hugonnet et al.,41 2007

n = 1883; medical ICU in Switzerland

Number of staff and number of patients daily Nurse-to-patient ratio (NPR) Nurse-to-patient ratio (NPR)

RN hours per patient day Higher staffing levels significantly (RN HPPD) associated with lower incidence of VAP and CLBSI

Patient-to nurse ratio (NPR)

Higher incidence of VAP when increased patient-to-nurse ratio. Not significant following adjustments

Nursing hours per patient No statistically significant association day between increased nursing hours and decreased incidence of VAP Nurse-to-patient ratio; No significant association with float nurse care nurse-to-patient ratio and CLBSI; increased CLBSI when 60% care by float nurse Worked hours per Trend towards lower staffing levels patient day increasing CLBSI although no significant association Daily nurse-to-patient Lower nurse staffing levels associated ratio with increased risk of nosocomial infection Daily nurse-to-patient ratio

Higher nurse-to-patient ratio associated with decreased infection risk

M. McGahan et al.

Alonso-Echanove et al.,39 2003

Nurse-to-patient ratio (NPR) Nursing workload (TISS)

The incidence of mortality and morbidity

69

Search Methods: MEDLINE CINAHL PsychINFO Google Scholar Reference Lists Australian digital thesis database Total articles: 95

44 articles eligible for review

51 papers excluded on abstract review: • • •

25 excluded due to not meeting inclusion criteria • 4 qualitative studies • 2 medical staffing studies • 15 studies at ward level • 4 studies with results aggregated at hospital level

5 systematic reviews 10 literature reviews 36 reports, expert opinion papers, and articles which upon perusal did not relate to the aim of this paper

19 original study articles included in this review

Figure 1 Flow diagram of search strategy.

(see Table 3) in relation to nurse staffing levels in the intensive care setting. Three of the studies24—26 included multiple outcomes of interest in relation to this paper. No studies examining outcomes such as errors, unplanned extubation, increased length of stay, readmission, myocardial infarction or acute renal failure met the inclusion criteria.

Nurse staffing levels and mortality Six of the included studies exclusively measured mortality as the independent variable27—32 ; while one other study measured mortality as one of a number of variables.24 Table 1 provides an overview of the year of publication, setting, population, study method, nurse staffing measure and results of each of these studies. The results on the impact of nurse staffing levels and mortality are mixed, with three studies24,28,29 showing a statistically significant association with increased nurse staffing levels on reduced mortality; and four studies27,30—32 not

finding a statistically significant association. Cho et al.28 found a significant association between patient—nurse ratios and mortality in secondary hospitals (secondary level of care as opposed to tertiary referral hospital) (OR 1.43, p = 0.001); indicating that every additional patient per registered nurse (RN) was associated with a 9% increase in the risk of patient death occurring (OR 1.09, 95% CI 1.04—1.14). An additional two or three patients allocated to a RN would be accompanied by an 18% and 29% increased risk in patient mortality, respectively. The authors, in their cohort, calculated that by adding one, two and three patients to a RN workload would result in 15, 28, and 44 excess deaths per 1000 patient admissions, respectively. Further, the association between patient—nurse ratio and mortality in tertiary hospitals was not significant (OR 0.54, 95% CI 0.22—1.33). Cho and Yun29 examined nurse staffing levels as it relates to the provision of basic nursing care and mortality of intensive care patients. Their study found that intensive care units with ‘number of beds per nurse’ of one or less were more likely to fully provide basic care to their patients (OR

n = 23,192 adults admitted to two hospitals in England

n = 95 patient care units across ten acute care hospitals in United States

Shuldham et al.,25 2009

Whitman et al.,26 2002

Secondary analysis of prospective, observational data

Worked hours per patient day

No statistically significant association. Trend towards increased nursing hours and increased incidence of pressure sores Trend towards lower staffing levels increasing pressure ulcer rates although no significant association Nursing hours per patient day

RN hours per patient day (RN HPPD)

Observational data from NNIS and Medicare files, administrative data, American Hospital Association annual survey, and RN survey Case study using retrospective hospital data

Nurse staffing method Study method Population studied

n = 15,846; elderly patients in 51 ICUs of 31 American hospitals 2007 Stone et al.,

24

Author, year of publication

Studies examining nurse staffing levels and pressure ulcers. Table 3

Higher staffing levels significantly associated with lower incidence of decubitus ulcers

M. McGahan et al.

Findings

70

3.94, 95% CI 1.22—12.7) compared to the control group of ‘greater than one and a half beds per nurse’ (OR 1.0). This same group of intensive care units also had lower likelihood of both in-hospital mortality (OR 0.26, 95% CI 0.09—0.80; p = 0.019) and 30-day mortality (OR 0.23, 95% CI 0.07—0.78; p = 0.018) compared to the same control group (OR 1.0); indicating that lower patient—nurse ratios lead to the provision of better nursing care and subsequently lower mortality (p value trend 0.030 and 0.001 respectively). Stone et al.24 also found that patients admitted to an ICU with more RN hours per patient day had a significantly lower incidence of 30-day mortality (OR 0.81, 95% CI 0.69—0.95; p = ≤0.05 for the third quartile compared to the first). While the study by Kiekkas et al.30 found the risk of mortality increased for both medical and surgical ICU patients as their exposure to periods of peak nursing workload increased, it did not reach statistical significance; however the results were clinically significant. In the group of ‘median patient exposure to nursing workload’, all patient mortality increased from 22% in the low exposure group (control) to 25% in the medium exposure group (OR 1.22, 95% CI 0.69—2.17) and further to 28% in the high exposure group (OR 1.39, 95% CI 0.79—2.44). With regard to the group of ‘peak patient exposure to nursing workload’, all patient mortality increased from 20.4% in the low exposure group (control) to 25.8% in the medium exposure group (OR 1.37, 95% CI 0.77—2.45) and reached 31.1% in the high exposure group (OR 1.74, 95% CI 0.98—3.08). Van den Heede et al.27 in their study set in 75 cardiac surgical general care units and 58 cardiac surgical intensive care units found a significant statistical and clinical association between increased nursing hours per patient day (NHPPD) and decreased in-hospital mortality at the general care level, however were unable to replicate the results in intensive care units. Similarly, Sales et al.31 found that increasing RN hours per patient day was significantly associated with decreased inhospital mortality in patients without an ICU stay (OR 0.91, 95% CI 0.86—0.96; p = <0.001); however RN staffing was not significantly associated with in-hospital mortality in patients who had an ICU stay (OR 1.01, 95% CI 0.99—1.03; p = 0.45). The study by Metnitz et al.32 primarily focused on ICU type and size and its effect on mortality; however a multivariate linear regression analysis of nurse staffing factors found no significant association with mortality (statistical results not provided in the publication).

The incidence of mortality and morbidity

Nurse staffing levels and infections Nine of the included studies focused exclusively on the outcome of infection as the independent variable33—41 ; while four other studies measured infectious outcomes as one of a number of variables.24—26,42 Table 2 provides an overview of the year of publication, setting, population, study method, nurse staffing measure and result of each of these studies. Three studies33—35 focused specifically on the transmission of MRSA and nurse staffing levels in the intensive care unit; while one article36 examined the transmission of numerous pathogens with regard to nurse staffing levels. All four studies reported an association between decreased staffing levels and increased spread of MRSA and other pathogens. Dancer et al.33 found that new cases of MRSA in the intensive care unit were more likely to occur during periods where a deficit of trained nurses exists. The authors found that 10 of 12 new cases of MRSA originated during a week when there was a deficit of trained nurses on day duty. The authors then calculated that the odds ratio of MRSA being acquired by patients was 6.9 (95% CI 0.49—310) during a period of staff shortage compared with an excess of staff (p = 0.16). While Dancer et al.33 concluded that epidemiologic analysis suggested that the acquisition of MRSA was seven times more likely during periods of nurse understaffing, this is an incorrect interpretation of the statistical result. Grundmann et al.34 found that patient exposure to relative staff deficit (adjusted rate ratio 1.05, 95% CI 1.02—1.09) was significantly associated with potential transmission of MRSA (p = 0.001). Blatnik and Lesnicar35 used the Therapeutic Intervention Scoring System (TISS) to examine the effect of nurses’ workload on the spread of MRSA in the intensive care unit. The TISS is a set of selected therapeutic activities that nurses perform daily in the ICU; and is used to compare the use of nursing manpower between groups of patients.43 It is assumed that 40—50 TISS points corresponds to the work of one nurse per eight hour shift35,43 ; therefore in this ICU setting with four staff per shift the target TISS is approximately 160. The authors found that nurses in this setting are overloaded by an average of 57%, with MRSA transmission occurring during periods where nurses were overloaded by more than 25%. At TISS scores over 250 the daily rate of MRSA transmission was 0.15; at a TISS score of 201—250 the daily rate was 0.05; and at a TISS score of 151—200 the daily rate was 0.01; while there was no MRSA transmission at a TISS score of less than 150. The difference between these mean values was found to be

71 statistically significant (p = <0.001). Halwani et al.36 found that patients who spent their entire ICU stay in an understaffed environment were more than three times more likely to receive a pathogen compared to those who spent no time in an understaffed environment (OR 3.28, 95% CI 1.43—7.53). Five studies addressed the association between the incidence of VAP and nurse staffing levels. Three studies24,37,42 demonstrated a statistically significant association between decreased nurse staffing levels and increased risk for VAP; while another two studies25,38 demonstrated no significant difference. Hugonnet et al.37 reported that higher nurse-to-patient ratios was associated with a reduced risk for late-onset VAP (hazard ratio 0.42, 95% CI 0.18—0.99); however it did not influence the occurrence of early-onset VAP. Similarly, Dang et al.42 found that patients cared for on units with ‘low intensity staffing’ (1:3 or greater on day and night shift) were more than twice as likely to develop respiratory complications such as VAP (OR 2.33, 95% CI 1.5—3.6) than patients cared for on units with ‘high intensity staffing’ (1:2 or fewer on day and night shift; control, OR 1.0). The study by Stone et al.24 concluded that patients admitted to an ICU with more RN hours per patient day had a significantly lower incidence of VAP (OR 0.21, 95% CI 0.08—0.53; p = ≤0.05 for the fourth quartile compared to the first). Blot et al.38 found that VAP rates in units with patient-to-nurse ratios of 1:1, 2:1, 2.5:1, and 3:1 were 9.3%, 25.7%, 18.7%, and 24.2%, respectively (p = 0.003); demonstrating a statistically significant association between lower nurse staffing levels and higher VAP rates. However, following adjustment for confounding covariates, patient—nurse ratios of more than 1:1 were no longer significantly associated with an increased risk of VAP (3:1 OR 1.74, 95% CI 0.76—4.99; p = 0.19). The study by Shuldham et al.25 also failed to find a significant association between increased staffing levels and decreased rates of VAP (incidence rate ratio 1.002, 95% CI 0.954—1.052; p = 0.950) in the critical care setting. Three studies investigated the association between nurse staffing levels and central line associated blood stream infection (CLBSI). Only one study24 showed a significant association between decreased nurse staffing levels and increased CLBSI; while the other two studies26,39 showed no significant association. As shown with other variables, Stone et al.24 found that patients admitted to an ICU with more RN hours per patient day had a significantly lower incidence of CLBSI (OR 0.32, 95% CI 0.15—0.70; p = ≤0.05 for the third quartile compared to the first). Alonso-Echanove et al.39 found no significant association between nurse-to-patient

72 ratio and CLBSI even after stratifying for Total Parenteral Nutrition (TPN) use or antimicrobialimpregnated CVC (statistical result not provided in the publication). However, the risk of acquiring CLBSI was 2.6 times higher in patients who are looked after by a float nurse more than 60% of the time (hazard ratio 2.75, 95% CI 1.45—5.22; p = 0.019). Whitman et al.26 also found no significant association between CLBSI and nurse staffing levels across critical care areas (statistical results not provided in the publication), however reported that the relationship is inversely related, with lower nurse staffing levels resulting in higher rates of CLBSI. Two studies40,41 focused on the association of nurse staffing levels and risk of nosocomial infection in general; both with significant results. Hugonnet et al.40 used three different methodological approaches to assess the relationship between nurse staffing levels and nosocomial infection and found that a nurse-to-patient ratio below 1.9 was associated with an approximately 50% increased infection risk in both case-crossover (OR 1.53, 95% CI 1.05—2.24) and cohort designs (OR 1.5, 95% CI 1.06—2.14); and a slightly less risk found in the case-time control design (OR 1.24, 95% CI 1.02—1.49). Another study by Hugonnet et al.41 found that after controlling for central venous catheter, mechanical ventilation, urinary catheter and antibiotic use, higher staffing levels were associated with a greater than 30% infection risk reduction (incidence rate ratio 0.69, 95% CI 0.50—0.95). The authors argued that if the nurseto-patient ratio was maintained above 2.2:1, 26.7% (95% CI 0.5—9.7) or 183 infections would have been prevented in their cohort.

Nurse staffing levels and pressure ulcers There were no studies which exclusively measured pressure ulcer development as the independent variable; however three of the included studies in this review examined pressure ulcer development as one of a number of outcome variables.24—26 Table 3 provides an overview of the year of publication, setting, population, study method, nurse staffing measure and results of each of these studies. Only the study by Stone et al.24 found a significant association between nurse staffing levels and pressure ulcer; with the studies by Shuldham et al.25 and Whitman et al.26 showing no significant association. Stone et al.24 reported that patients admitted to an intensive care unit with more RN hours per patient day had a significantly lower incidence of decubitus ulcer (OR 0.69, 95%

M. McGahan et al. CI 0.49—0.98; p = ≤0.01 for the third quartile compared to the first). In contrast, Shuldham et al.25 found no significant difference between higher nurse staffing levels and decreased incidence of decubitus ulcer (incidence rate ratio 0.986, 95% CI 0.941—1.034; p = 0.564); however the authors report some evidence of a relationship between increased nurse staffing levels and increased rates of pressure injury in the critical care area. Whitman et al.26 found no significant relationship between nurse staffing levels and pressure ulcer rates (statistical results not provided in the publication), however concluded that the relationship between these variables is inversely related with lower nurse staffing levels resulting in higher rates of pressure ulcer development..

Discussion While an overall statistically significant association between increased nurse staffing levels and decreased incidences of mortality and morbidity in adult intensive care patients was not found in this review, most studies concluded that a positive relationship does exists between these variables. The findings in this review are largely consistent with findings in earlier literature related to both intensive care and general ward nurse staffing levels and its effect on adverse patient outcomes.1,2,22,23,44

Methodological issues While the results in this review may well be consistent with prior literature, interpreting the association between nurse staffing levels and the incidence of mortality and morbidity needs to be treated with caution by authors and readers alike.2 The methodological designs of the studies examined in this review include retrospective, cross sectional, prospective cohort, longitudinal and case-crossover; which are all observational in nature45 (see Tables 1—3). It is important to note that observational studies make demonstrating an association difficult due to many unrecognised and uncontrolled variables such as illness trajectory, age, co-morbidities and individual nurse factors; which ultimately confound the true relationship between nurse staffing levels and adverse outcomes.12,22,23,45 Ideally, in order to be more confident in demonstrating an association, experimental studies such as randomised controlled trials would need to be performed; however this study design is unlikely to be employed to test this relationship due to logistical complexities and ethical

The incidence of mortality and morbidity concerns.1,22 A number of studies used administrative databases and medical records to examine variables. Databases and records are historical archives which may vary in accuracy and completeness and consequently distort findings between different hospital settings.1 For example, the incidence of adverse events may be under-reported where nurse staffing levels are low.16 In addition, large datasets include variables measured at different levels (nursing and patient characteristics, unit and hospital type, geographical location) often leading to outcomes being aggregated at the institutional level rather than at the level of interest.11 This review used a variety of measures to describe nurse staffing levels across the studies (nursing hours per patient day, RN hours per patient day, nurse-to-patient ratio, nursing workload). These impact on the ability to collate and analyse the outcome data for statistical purposes. In an attempt to standardise these variables, Van den Heede et al.46 developed a panel of experts in this field to gain consensus on the most appropriate nurse staffing and patient characteristic measures using a Delphi survey. Nursing hours per patient day received the highest consensus score as a valid measure of the number of nursing staff; while both age and co-morbidities were rated as the most important patient variables by all respondents. Interestingly, only two of the included studies in this review which were published following the Delphi survey conducted by Van den Heede et al.46 have used nursing hours per patient day as their nurse staffing measure. The fact that the majority of studies recruited a small population sample; included a small number of centres; or examined a group of geographically homogeneous hospitals makes generalising the results across the whole population inappropriate.47 Unfortunately, the methodological issues identified in the majority of included studies in this review are consistent with the issues presented in reviews by Numata et al.22 and West et al.23 The lack of improvement in study design, data collection techniques, consistency of nurse staffing measure, and sample size and range fail to provide a new perspective or understanding beyond what is already known. These methodological issues limit the ability to counteract confounders and assess the true association between nurse staffing levels and the incidence of mortality and morbidity in the intensive care setting.

Nurse staffing levels and mortality Most studies in this review found some association between nurse staffing levels and patient mortality.

73 While all studies adjusted their results to counteract certain patient characteristics, interpretation of the findings must be heeded with caution due to the influence of these characteristics on the outcome. Possibly the most significant factors contributing to mortality is the type and severity of the patient’s presenting illness, existing co-morbidities and age. While Cho et al.28 found that nurse staffing levels was associated with mortality in secondary hospitals, they found no association in tertiary hospitals; possibly due to increased severity of illness and risk of death on admission to tertiary hospitals. Similarly, Sales et al.31 found that patients had better odds of survival in lower complexity units possibly due to decreased severity of illness in that facility. The study by Cho and Yun29 only included stroke patients in their study so ruling out the effects of other presenting illnesses in their findings. Van den Heede et al.27 only examined cardiac surgical patients and noted that the resulting relationship between nurse staffing levels and mortality may be different to that of the general ICU population. Kiekkas et al.30 noted that patients admitted to the ICU post surgery are generally expected to be healthy enough to sustain an operation and have a reversible condition, therefore having a lower risk of mortality. They also noted that their medical subjects were younger, had higher APACHE scores, stayed longer in the ICU and had a higher mortality rate. Based on this finding, Kiekkas et al.30 highlighted that nurse staffing levels should be based on patient care needs rather than nurse-to-patient ratios. The study by Stone et al.24 focused on elderly patients which could influence the rate of mortality independent of other factors. Surgical performance may also influence mortality rates in some hospitals especially where a ‘volume effect’ is present such as in cardiac surgical units, hence reducing mortality.27 The effect of medical staff performance also appears to play a large part in the risk of mortality. Cho et al.28 found that patients in tertiary hospitals that had no board-certified physician attending for four or more hours per day had a 56% increased risk in the odds of death. Differences in ICU admission criteria across hospitals may influence inclusion and exclusion of patients in the study samples, posing the problems of selection and referral bias.29 The definition of mortality (all mortality, in-hospital mortality, 30day mortality) varies across included studies, not allowing a genuine comparison to occur between studies. Also, the use of in-hospital mortality as an end-point may bias the association between ICU nurse staffing levels and mortality as the care the patient receives on the ward following discharge from ICU will influence this result.

74 The consistency of nurse staffing levels in the ICU across studies make finding an association difficult. The studies conducted by Van den Heede et al.27 and Sales et al.31 found an association between increased nurse staffing levels and decreased mortality in the ward setting, however were unable to replicate their results in the ICU setting possibly due to lack of variation in ICU staffing levels across shifts in the hospitals examined. Similarly, Cho et al.,28 while finding a strong association between patient—nurse ratio and mortality in secondary hospital ICUs, only found a weak association in tertiary hospital ICUs; once again possibly due to higher, more consistent staffing levels and a higher proportion of RNs in tertiary hospitals than that is seen in secondary hospitals. Upon discharge from the ICU, critically ill patients are likely to spend a significant time in hospital, possibly being cared for in numerous units throughout the hospital. Nurse staffing levels vary widely in different units within the hospital, hence confounding the effect of nurse staffing levels on mortality in the intensive care unit. While difficult to achieve, the reviewed studies did not attempt to account for the effect of varying nurse staffing levels on mortality in other parts of the hospital.

Nurse staffing levels and infections The incidence of infection was associated with decreased nurse staffing levels in the majority of the studies. However, determining whether nurse staffing levels directly influence infection rates is complex, as there are many other contributing factors to consider. Periods of increased workload during the shift have been linked to the spread of MRSA due to inadequate time to adhere to effective hand hygiene interventions and disinfection techniques.33,36 However, determining the exact transmission time is difficult, thus making it impossible to link transmission of a pathogen to increased workload and demonstrating causality. Hugonnet et al.37 in their study investigating VAP also hypothesised that increased workload results in hygiene practice failures and furthers the spread of pathogens. As a large proportion of early onset VAP stems from aspiration,37 inadequate time, resources and knowledge in providing sufficient oral and airway care to the intubated patient would influence the occurrence of late-onset VAP possibly more than nurse staffing levels alone. AlonsoEchanove et al.39 found that while risk of central line infection was not related to nurse-to-patient ratio, the risk of infection increased when patients were looked after by a ‘float’ nurse. This highlights the fact that the care of patients is undertaken by

M. McGahan et al. many other health care professionals, besides ICU trained nurses, who could spread infection due to lack of adequate hand hygiene practices or education in infection control practices and unit policies. This emphasises the point that global staff training in infection control practices is vital in preventing nosocomial infection. The ‘5 Moments for Hand Hygiene’ developed by the World Health Organisation (WHO)48 is one initiative designed to educate all hospital staff worldwide on the importance of effective hand hygiene practices and prevention of nosocomial infections. Halwani et al.36 discovered that patients who underwent repeated bronchoscopy were five times more likely to be the recipient of a transmittable pathogen. Grundmann et al.34 found a significant association between tracheostomy and renal replacement therapy and the acquisition of MRSA. However, determining whether nurse staffing levels alone affect infection rates in these patients is difficult to determine as medical staff usually perform these procedures with nursing staff performing the subsequent care. Regularly accessing invasive devices such as arterial and central venous lines and frequency of invasive procedures also appear to increase the risk of pathogen acquisition regardless of the actual amount of nurses present on shift. Interestingly, the study by Hugonnet et al.41 concluded that overstaffing does not influence the incidence of infection; however what seems important is to define a minimum nurse-to-patient ratio below which infections rise dramatically. Cross transmission of pathogens may be reduced by eliminating unnecessary procedures, keeping patient contact to a minimum, providing infection control education and enforcing proper hand hygiene techniques, in addition to adequate nurse staffing levels.

Nurse staffing levels and pressure ulcer Increased nurse staffing levels were associated with decreased pressure ulcer development in only one24 of the included studies in this review. The study by Stone et al.24 found that higher nurse staffing levels were associated with a lower incidence of pressure ulcers (with statistical significance). A study conducted by Unrah18 also found a similar trend with a 10% increase in staff numbers decreasing pressure ulcers by two percent. However, in contrast, the study conducted by Shuldham et al.25 found that a greater number of nursing hours was associated with a higher probability of pressure ulcer development; a similar result to the one found by Cho et al.11 in an earlier ward based study. This result is assumed to be due to higher staffing levels promoting more thorough patient assessments

The incidence of mortality and morbidity and ultimately more accurate reporting. Another possible reason for this outcome is that increased nurse staffing levels promoted miscommunication between staff on what pressure ulcer care had been performed; hence these interventions were being omitted, causing pressure ulcer rates to actually rise. The effect of nurse staffing levels on pressure ulcers in the intensive care unit could also be distorted due to inaccurate documentation of preexisting pressure ulcers on admission to the unit. While adequate nurse staffing levels are necessary for the prevention of pressure ulcers; vigilant skin assessment, accurate and timely documentation, and effective communication also influences this outcome in the intensive care setting.

Individual nurse factors The studies in this review focused on nurse staffing levels and its effect on mortality and morbidity, particularly infection and pressure ulcer development. However, even despite adequate nurse staffing levels, individual nurse factors such as knowledge, skills, and physical and mental wellness may impact on the incidence of mortality and morbidity in the critically ill patient. Although not included in this review, three studies conducted in the last decade found that better educated nursing workforces are associated with a lower 30-day patient mortality.15,49,50 In contrast, the studies by Cho et al.,28 Van den Heede et al.,27 and Sales et al.31 in this review did not find an association between nurse education levels and mortality. Hugonnet et al.41 failed to find an association between nurse education levels and infection transmission. Fatigue due to long working hours is detrimental to staff health and may contribute to nurse performance and patient outcomes. Rogers et al.51 found that nurses who worked more than 12.5 h per shift were three times more likely to make errors compared to nurses who only worked an eight hour shift. Similarly, Scott et al.52 found that the risk for making an error almost doubled when nurses worked 12.5 or more consecutive hours. In this review, the study by Stone et al.24 found a trend between increased overtime and increased adverse outcomes; with a significant association found between increased overtime and increased pressure injury development. Also, hospital care environments where nursing staff reported more positive job experiences had significantly lower risks of mortality and failure-to rescue.53 Cho et al.28 tended to agree but stated that more research on this topic is required to fully assess its effect. Surprisingly, Stone et al.24 found a significant association between organisational climate

75 and CLBSI. Hugonnet et al.41 also believe that job satisfaction and positive organisational support may lead to better outcomes, including those of healthcare associated infections.

Implications for practice While the majority of results in this review indicate that a relationship exists between increased nurse staffing levels and decreased adverse patient outcomes, an exact nurse-to-patient ratio or exact number of staff needed per shift to optimise outcomes remains unknown. Nurse managers and leaders responsible for staffing must be constantly aware of patient acuity and workload issues in the intensive care unit and respond appropriately as these change throughout the shift. Decisions on staffing levels should also be made in consultation with medical staff, taking into consideration predicted workload for the shift ahead. In addition, skill mix and patient allocation need to be aligned with patient acuity and workload demands, as these factors impact on care delivery and outcome.54 Lastly, nurse managers must ensure their staff avoid overtime and excessive continuous hours as these not only affect patient care and outcomes; but also staff health, satisfaction, and retention.

Conclusion While an overall statistical association between increased nurse staffing levels and decreased adverse patient outcomes was not found in this review, most studies demonstrated a trend between increased nurse staffing levels and decreased adverse patient outcomes in the intensive care unit. These results are consistent with previous studies over the past few decades in both the critical care and ward setting. In order to facilitate a statistical analysis of the topic to ascertain the exact relationship between nurse staffing levels and mortality and morbidity a more robust study design would need to be employed. The authors believe that this may be unachievable if one considers the multitude of potential confounders that complicate this area of research. However, future studies on this topic should aim to collect data prospectively, standardise nurse staffing and outcome measure definitions, and conduct large heterogeneous multicentre trials in order to be able to collate data for statistical analysis. Nonetheless, the results found in this review are thought-provoking for nurse managers and staff nurses when faced with the complex

76 task of decision making regarding appropriate nurse staffing levels. Identified limitations of this review include that no meta-analysis was able to be undertaken; a small number of included studies; and the homogeneity of included studies makes generalising the results across the whole population inappropriate.

References 1. Kane RL, Shamliyan TA, Mueller C, Duval S, Wilt TJ. The association of registered nurse staffing levels and patient outcomes: systematic review and meta-analysis. Med Care 2007;45(12):1195—204. 2. Lankshear AJ, Sheldon TA, Maynard A. Nurse staffing and healthcare outcomes: a systematic review of the international research evidence. Adv Nurs Sci 2005;28(2):163—74. 3. ACCCN: Australian College of Critical Care Nurses. ACCCN ICU staffing position statement (2003) on intensive care nursing staffing. Melbourne: Workforce Advisory Panel Australian College of Critical Care Nurses; 2002—2011, 2003 Jan [cited 2011 May 10]; 2 pp. [Internet]. Available from: http://www.acccn.com.au/images/stories/downloads/ staffing intensive care nursing.pdf. 4. BACCN: British Association of Critical Care Nurses. BACCN Standards for nurse staffing in critical care. Newcastle upon Tyne: British Association of Critical Care Nurses; 2007—2011 [revised 2010 Jan; cited 2011 May 10]; p. 1—38 [Internet]. Available from: http://www.baccn.org.uk/ downloads/BACCN Staffing Standards.pdf. 5. AACN: American Association of Critical-Care Nurses. Establishing criteria for 1:1 staffing ratios. Aliso Viejo: American Association of Critical-Care Nurses; 2010, 2000 Apr [cited 2011 May 10]; 1 p. [Internet]. Available from: http://www. aacn.org/wd/certifications/content/synpract8.pcms?menu= practice. 6. Burnes Bolton L, Aydin CE, Donaldson N, Storer Brown N, Sandhu M, Fridman M, et al. Mandated nurse staffing ratios in California: a comparison of staffing and nursing-sensitive outcomes pre- and postregulation. Policy Polit Nurs Pract 2007;8(4):238—50. 7. Halm M, Peterson M, Kandels M, Sabo J, Blalock M, Braden R, et al. Hospital nurse staffing and patient mortality, emotional exhaustion, and job satisfaction. Clin Nurse Specialist 2005;19(5):241—51. 8. Rafferty AM, Clarke SP, Coles J, Ball J, James P, McKee M, et al. Outcomes of variation in hospital nurse staffing in English hospitals: cross-sectional analysis of survey data and discharge records. Int J Nurs Stud 2007;44:175—82. 9. Sochalski J, Tamara Konetzka R, Zhu J, Volpp K. Will mandated minimum nurse staffing ratios lead to better patient outcomes? Med Care 2008;46(6):606—13. 10. Van den Heede K, Sermeus W, Diya L, Clarke SP, Lesaffre E, Vleugels A, et al. Nurse staffing and patient outcomes in Belgian acute hospitals: cross-sectional analysis of administrative data. Int J Nurs Stud 2009;46:928—39. 11. Cho SH, Ketefian S, Barkauskas VH, Smith DG. The effects of nurse staffing on adverse events, morbidity, mortality and medical costs. Nurs Res 2003;52(2):71—9. 12. Needleman J, Buerhaus P, Shane Pankratz V, Leibson CL, Stevens SR, Harris M. Nurse staffing and inpatient hospital mortality. N Engl J Med 2011;364(11):1037—45.

M. McGahan et al. 13. Sasichay-Akkadechanunt T, Scalzi CC, Jawad AF. The relationship between nurse staffing and patient outcomes. J Nurs Adm 2003;33(9):478—85. 14. Aitken LH, Clarke SP, Sloane DM, Sochalski J, Silber JH. Hospital nurse staffing and patient mortality, nurse burnout, and job satisfaction. J Am Med Assoc 2002;288(16):1987—93. 15. Tourangeau AE, Doran DM, McGillis Hall L, O’Brien Pallas L, Pringle D, Tu JV, et al. Impact of hospital nursing care on 30-day mortality for acute medical patients. J Adv Nurs 2006;57(1):32—44. 16. Needleman J, Buerhaus P, Mattke S, Stewart M, Zelevinsky K. Nurse-staffing levels and the quality of care in hospitals. N Engl J Med 2002;346(22):1715—22. 17. Needleman J, Buerhaus PI, Stewart M, Zelevinsky K, Mattke S. Nurse staffing in hospitals: is there a business case for quality? Health Aff 2006;25(1):204—11. 18. Unrah L. Licensed nurse staffing and adverse events in hospitals. Med Care 2003;41(1):142—52. 19. McGillis Hall L, Doran D, Pink GH. Nurse staffing models, nursing hours, and patient safety outcomes. J Nurs Adm 2004;34(1):41—5. 20. Dunton N, Gajewski B, Taunton RL, Moore J. Nurse staffing and patient falls on acute care hospital units. Nurs Outlook 2004;52:53—9. 21. Tschannen D, Kalisch BJ. The effect of variations in nurse staffing on patient length of stay in the acute care setting. West J Nurs Res 2009;31(2):153—70. 22. Numata Y, Schulzer M, van der Wal R, Globerman J, Semenuik P, Balka E, et al. Nurse staffing levels and hospital mortality in critical care settings: literature review and meta-analysis. J Adv Nurs 2006;55(4):435—48. 23. West E, Mays N, Rafferty AM, Rowan K, Sanderson C. Nursing resources and patient outcomes in intensive care: a systematic review of the literature. Int J Nurs Stud 2009;46:993—1011. 24. Stone PW, Mooney-Kane C, Larson EL, Horan T, Glance LG, Zwanziger J, et al. Nurse working conditions and patient safety outcomes. Med Care 2007;45(6):571—8. 25. Shuldham C, Parkin C, Firouzi A, Roughton M, LauWalker M. The relationship between nurse staffing and patient outcomes: a case study. Int J Nurs Stud 2009;46: 986—92. 26. Whitman GR, Kim Y, Davidson LJ, Wolf GA, Wang SL. The impact of staffing on patient outcomes across specialty units. J Nurs Adm 2002;32(12):633—9. 27. Van den Heede K, Lesaffre E, Diya L, Vleugels A, Clarke SP, Aitken LH, et al. The relationship between inpatient cardiac surgery mortality and nurse numbers and educational level: analysis of administrative data. Int J Nurs Stud 2009;46:796—803. 28. Cho SH, Hwang JH, Kim J. Nurse staffing and patient mortality in intensive care units. Nurs Res 2008;57(5): 322—30. 29. Cho SH, Yun SC. Bed-to-nurse ratios, provision of basic nursing care, and in-hospital and 30-day mortality among acute stroke patients admitted to an intensive care unit: cross sectional analysis of survey and administrative data. Int J Nurs Stud 2009;46:1092—101. 30. Kiekkas P, Sakellaropoulos GC, Brokalaki H, Manolis E, Samios A, Skartsani C, et al. Association between nursing workload and mortality of intensive care unit patients. J Nurs Scholarsh 2008;40(4):385—90. 31. Sales A, Sharp N, Li YF, Lowy E, Greiner G, Liu CF, et al. The association between nursing factors and patient mortality in the veterans health administration: the view from the nursing unit level. Med Care 2008;46(9): 938—45.

The incidence of mortality and morbidity 32. Metnitz PG, Reiter A, Jordan B, Lang T. More interventions do not necessarily improve patient outcome in critically ill patients. Intensive Care Med 2004;30:1586—93. 33. Dancer SJ, Coyne M, Speekenbrink A, Samavedam S, Kennedy J, Wallace PG. MRSA acquisition in an intensive care unit. Am J Infect Control 2006;34:10—7. 34. Grundmann H, Hori S, Winter B, Tami A, Austin DJ. Risk factors for the transmission of methicillin-resistant Staphylococcus aureus in an adult intensive care unit: fitting a model to the data. J Infect Dis 2002;185:481—8. 35. Blatnik J, Lesnicar G. Propagation of methicillin-resistant Staphylococcus aureus due to the overloading of medical nurses in intensive care units. J Hosp Infect 2006;63:162—6. 36. Halwani M, Solaymani-Dodaran M, Grundmann H, Coupland C, Slack R. Cross-transmission of nosocomial pathogens in an adult intensive care unit: incidence and risk factors. J Hosp Infect 2006;63:39—46. 37. Hugonnet S, Uckay I, Pittet D. Staffing level: a determinant of late onset ventilator-associated pneumonia. Crit Care 2007;11(4.):7. 38. Blot SI, Llaurado Serra M, Koulenti D, Lisboa T, Deja M, Myrianthefs P, et al. Patient to nurse ratio and risk of ventilator-associated pneumonia in critically ill patients. Am J Crit Care 2011;20:e1—9. 39. Alonso-Echanove J, Edwards JR, Richards MJ, Brennan P, Venezia RA, Keen J, et al. Effect of nurse staffing and antimicrobial-impregnated central venous catheters on the risk for bloodstream infections in intensive care units. Infect Control Hosp Epidemiol 2003;24(12):916—25. 40. Hugonnet S, Villaveces A, Pittet D. Nurse staffing level and nosocomial infections: empirical evaluation of the casecrossover and case-time-control designs. Am J Epidemiol 2007;165:1321—7. 41. Hugonnet S, Chevrolet JC, Pittet D. The effect of workload on infection risk in critically ill patients. Crit Care Med 2007;35(1):76—81. 42. Dang D, Johantgen ME, Provonost PJ, Jenckes MW, Bass EB. Postoperative complications: does intensive care unit staff nursing make a difference? Heart Lung 2002;31(3):219—28.

77 43. Reis Miranda D, de Rijk A, Schaufeli W. Simplified Therapeutic Intervention Scoring System: the TISS-28 items—–results from a multicenter study. Crit Care Med 1996;24(1):64—73. 44. Lang TA, Hodge M, Olsen V, Romano PS, Kravitz RL. Nurse—patient ratios: a systematic review on the effects of nurse staffing on patient, nurse employee, and hospital outcomes. J Nurs Adm 2004;34(7/8):326—37. 45. Oleckno WA. Epidemiology: concepts and methods. 1st ed. Long Grove (IL): Waveland Press, Inc.; 2008, 649 pp. 46. Van den Heede K, Clarke SP, Sermeus W, Vleugels A, Aitken LH. International experts’ perspective on the state of the nurse staffing and patient outcomes literature. J Nurs Scholarsh 2007;39(4):290—7. 47. Heinz D. Hospital nurse staffing and patient outcomes: a review of current literature. Dim Crit Care Nurs 2004;23(1):44—50. 48. WHO: World Health Organisation. Guidelines: hand hygiene in healthcare (advanced draft). Geneva: WHO; 2011, 2006 Oct [cited 2011 June 18] [Internet]. Available from: http://www.who.int/gpsc/tools/Five moments/en/index. html. 49. Aitken LH, Clarke SP, Cheung RB, Sloane DM, Silber JH. Educational levels of hospital nurses and surgical patient mortality. J Am Med Assoc 2003;290(12):1617—23. 50. Estabrooks CA, Midodzi WK, Cummings GG, Ricker KL, Giovannetti P. The impact of hospital nursing characteristics on 30-day mortality. Nurs Res 2005;54(2):74—84. 51. Rogers AE, Hwang WT, Scott LD, Aitken LH, Dinges DF. The working hours of hospital staff nurses and patient safety. Health Aff 2004;23(4):202—12. 52. Scott LD, Rogers AE, Hwang WT, Zhang Y. Effects of critical care nurses’ work hours on vigilance and patients’ safety. Am J Crit Care 2006;15(1):30—7. 53. Aitken LH, Clarke SP, Sloane DM, Lake ET, Cheney T. Effects of hospital care environment on patient mortality and nurse outcomes. J Nurs Adm 2008;38(5):223—9. 54. Rischbieth A. Matching nurse skill with patient acuity in the intensive care units: a risk management mandate. J Nurs Manag 2006;14:397—404.

Available online at www.sciencedirect.com