MRSA acquisition in an intensive care unit

Article Outline

• Abstract
• Methods
• Results
• Discussion
• Acknowledgment
• References
• Copyright

Background

This paper describes a retrospective investigation of methicillin-resistant Staphylococcus aureus (MRSA) acquisition in an 8-bed intensive care unit (ICU) over a 5-month period.

Methods

Clinical and microbiologic data were collected from the ICU, including MRSA detection dates, patient dependency scores, standardized environmental screening data, weekly bed occupancies, number of admissions, and nurse staffing levels. MRSA acquisition weeks were defined as weeks during which initial delivery of MRSA occurred before sampling and laboratory confirmation. Weekly workloads were plotted against staffing levels and modelled against MRSA acquisition weeks and hygiene failures.

Results

Of 174 patients admitted into the ICU, 28 (16%) were found to have MRSA; 12 of these (7%) acquired MRSA on the ICU within 7 of the 23 weeks studied. Six of these 7 weeks were associated with a deficit of trained nurses during the day and 5 with hygiene failures (data unavailable for 2). Pulsed-field gel electrophoresis (PFGE) profiles demonstrated relationships between staphylococci from staff hands, hand-touch sites, and patients' blood.

Conclusion

MRSA acquisition in the ICU was temporally associated with reduced numbers of trained nurses and hygiene failures predominantly involving hand-touch sites. Epidemiologic analysis suggested that patient acquisitions were 7 times more likely to occur during periods of nurse understaffing.

Methicillin-resistant Staphylococcus aureus (MRSA) is endemic in most United Kingdom hospitals and is particularly associated with severely compromised patients, including those in intensive care units (ICU).¹ The epidemiology of MRSA in ICUs is complex, but the main vehicle of transmission is likely to be staff hands.² Staff members will pick up and propagate MRSA from one patient to another in the absence of effective hand hygiene. It is also possible that the environment serves as an inanimate reservoir because MRSA can survive desiccation and has been demonstrated on a variety of surfaces and medical equipment in hospitals.³, ⁴, ⁵

To investigate the microbiologic component of the hospital environment, we performed a standardized 4-month screening programme on 3 wards, including the ICU.⁶ The aim was to examine organisms from different sites in clinical areas and compare bacterial resistances in association with antimicrobial consumption for these wards. We found that antibiotic resistance was the only significant difference between environmental organisms from different wards and appeared to reflect ward-based prescribing pressures.⁶

It was during this study that we noticed that there were certain weeks on the ICU during which patients were more likely to acquire MRSA. These acquisitions appeared to be linked in that they occurred within a few days of each other. Staff members told us that these periods were particularly busy. We wondered whether increased workload in our ICU might be a risk factor for MRSA acquisition because it has been previously described.⁷, ⁸ This prompted a retrospective analysis on MRSA acquisition, using the results from the environmental screening study, and incorporating other data that might affect workload and infection control practices in the ICU.

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Methods 

Standardized screening of surface level hygiene in an 8-bed ICU was performed weekly at different times and at different intervals over a 16-week period for a previous study.⁶ This period was contained within the 5-month analysis for the current report. A “surprise” visit was included 2 weeks after the screening period had finished. Dipslides (Biotrace; Bridgend, United Kingdom) were applied against 10 sites to include both hand-touch and nonhand-touch sites, eg, floor, sinks, handles, beds, curtains, and computer keyboards.⁶ Hand-touch sites were defined as those places more frequently touched by human hands during routine clinical activities. Microbial growth was quantitatively and qualitatively assessed, with hygiene failures ascribed according to the recent proposal of microbiologic standards for surface hygiene in hospitals.⁹ These suggest that finding an indicator organism such as S aureus or MRSA or >5 cfu/cm² of any organisms from a hand-touch site in a clinical area constitutes a lapse in surface level cleanliness.⁹

Microbiologic data were extracted from the laboratory database for all ICU patients admitted from 3 weeks before to 4 weeks after the environmental screening period. We were able to retrieve staphylococcal isolates from patients producing positive blood cultures within the study period, but isolates from other clinical specimens were unobtainable because this was a retrospective analysis. Staphylococci were identified in accordance with standard operating procedures, namely, culture on blood agar, Gram's stain, and catalase and coagulase testing (slide and tube). API Staph biochemical identification kits (bioMérieux UK Limited, Basingstoke, UK) were utilized for blood culture isolates. MRSA screening swabs were plated onto mannitol salt agar and incubated at 37°C for 24 to 48 hours; mannitol-fermenting colonies were tested for catalase and coagulase production as before. A laboratory database supplied extended antibiotic resistance spectra for all staphylococcal isolates from ICU patients. Apart from meticillin, vancomycin, and teicoplanin, isolates were tested against trimethoprim, mupirocin, rifampicin, fusidic acid, gentamicin, tobramycin, and neomycin in accordance with Clinical and Laboratory Standard Institute (CLSI) guidelines.

Formal staff screening was not performed during this study, although we did obtain opportunistic fingertip cultures from 18 members of staff at different times during the 16-week environmental screening period.⁶ All fingertips were voluntarily pressed onto a blood agar plate and returned to the laboratory for culture at 37°C for 24 to 48 hours. Suspicious colonies were identified using the methods previously described and tested against the same range of antibiotics. Feedback to staff was offered on a confidential basis.

Pulsed-field gel electrophoresis (PFGE) typing was performed on coagulase-negative staphylococci (CNS) obtained from the environment, staff hands, and patients' blood. We had originally intended to genotype the MRSA isolates collected, but the environmental screen only produced 1 isolate, and there were none from staff fingertips or from the blood of patients who had acquired MRSA on the ICU. PFGE was performed according to the method described by Neumeister et al with minor modifications, using SmaI as discriminative enzyme.¹⁰ Antibiogram similarities were used to select and group isolates for typing.

Because all patients are screened on admission and alternate days thereafter, the criteria for acquisition of MRSA on the ICU were negative swabs on admission and for the first 48 hours in the ICU.¹¹ Patients who were MRSA positive on arrival, or identified within the first 48 hours, were therefore excluded from the analysis. MRSA colonization pressures included all positive patients and were calculated weekly as the total number of MRSA-positive patient-days per week divided by the total number of patients in the ICU for that week per 1000 patient-days.¹²

Since primary acquisition must have occurred a few days before the identification of MRSA from a clinical specimen, we were interested in the period between acquisition and sufficient quantity of bacterial growth to enable routine laboratory detection. After considering previous work on staphylococcal incubation, we chose 4 days as an average time interval between first acquisition of a few colony forming units of MRSA and laboratory isolation from a clinical sample.¹³, ¹⁴

Clinical data, including Therapeutic Intervention Scores (TIS) for each patient, were retrieved from the ICU database.¹⁵ Weekly workloads were calculated by adding the number of patients in the ICU for a particular week multiplied by their dependency level (1, 2, or 3) according to individual TIS⁷ and then by the number of days they were in ICU (see Table 1). The number of admissions for that week was then added to this sum to represent a total weekly workload or modified weekly TIS. Weekly bed occupancies and nurse staffing levels for trained, agency, and auxiliary nurses (both day and night duties) were obtained from the senior nurse. Day shift sessions ran from 8 am until 8 pm.

Table 1. Calculation of weekly workload using a modified total Therapeutic Intervention Score (TIS)⁷, ¹⁵

There were no outbreaks in the ICU during the study period, and no changes in disinfection policies, infection control policies, cleaning schedules, or staffing policies. Other than routine informal audits organized by the infection control nurses, we did not formally monitor hand hygiene compliance. Statistical analyses were performed between all variables: linear regression analysis between workload and number of staff and Fisher exact test for association between staffing levels and MRSA acquisition.

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Results 

Of 174 admissions during the 23-week period studied, 28 (16%) patients were found to have MRSA at some time during their stay on the ICU. Sixteen (9%) patients were admitted either colonized or infected with MRSA; 2 of these produced positive blood cultures. Twelve (7%) of 174 patients acquired MRSA while on the ICU, but none became bacteraemic (Table 2). The average length of time between admission and laboratory detection of MRSA was 10 days (range, 4-30; median, 6 days). MRSA isolates were first identified from upper respiratory sites in 9 of 12 patients. Four discrete clusters were observed, each involving 3 patients within a 5-day period and occurring within 7 of the 23 weeks studied (Table 2, Fig 1). Clusters were defined by temporal relationships between new ICU acquisitions, ie, cases occurring within a 5-day period, and not by any other clinical, microbiologic, or typing criteria.

Table 2. Weekly nurse staffing, number of admissions, bed occupancy rates, workload, MRSA colonization pressures, cleaning failures, and new MRSA patients over a 5-month period on an ICU

MRSA acquisition weeks, 1, 2, 4, 5, 13, 18, 19; Pt, patient; ND, not done; TIS, Therapeutic Intervention Scores; U, unknown.

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• Fig 1. 

  Total workload, MRSA acquisition weeks, number of nurses on day duty, and hygiene assessment over a 5-month period on the ICU.

There were no significant trends between workload, nurse staffing levels, number of admissions, or MRSA colonization pressure and either the occurrence of a cluster or a patient acquisition of MRSA. As expected, there is a link between the number of trained nurses on day shift and total workload (correlation coefficient, 0.669) (Fig 2). We took the best-fit line from Fig 2 to illustrate the boundary between an excess number of trained nurses and a deficit of nurses on day duty for an estimated workload in the ICU. This showed that 10 of 12 new cases of MRSA originally acquired the organism during a week when there was a deficit of trained nurses on day duty. The odds ratio of MRSA being acquired by patients was 6.9 (95% CI: 0.49-310) if there were a deficit of trained nurses during the day compared with an excess (P = .16) (Table 3). This suggests that patient acquisitions of MRSA were 7 times more likely during periods of understaffing.

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• Fig 2. 

  Relationship between workload (modified TIS) and the number of trained nurses on day duty per week.

Table 3. Weeks in which MRSA acquisition occurred versus adequacy^∗ of trained nurse staffing during the day over a 5-month period^†

There were other weeks from Fig 2 during which there was a deficit of trained nurses for the workload during the day (weeks 3, 8, 15, and 17). It was of interest that new acquisitions of MRSA were not associated with these weeks. Weeks 8 and 15, however, saw many more patient admissions, most of who did not stay in the ICU for more than 2 or 3 days (Table 2). A shorter length of stay would have reduced the risk of acquiring MRSA as well as excluding the patient from the definition of ICU-acquired MRSA. Some of these patients may have become positive for MRSA following discharge, but we had no system in place for detecting these. In addition, week 15 is unique regarding the environmental screening results in that it was the only week within the screening study when the ICU did not fail the cleaning standards (Fig 1). There is no explanation for a lack of new MRSA cases in weeks 3 and 17, although their positions in Fig 2 would suggest that there was less risk from MRSA than during weeks 8 and 15. In contrast, week 4, which was an MRSA acquisition week, is close to the boundary for adequate nurse staffing and therefore should have been at lower risk for MRSA acquisition. Within that week, however, we identified the highest number of hygiene failures and also found MRSA in the environment–the only week when it was found (Table 2, Table 4).

Week 5 is the real issue because the association between a deficit in nursing staff and MRSA acquisition would have achieved statistical significance (P = .048) if week 5 had not been implicated as an MRSA acquisition week (Fig 2). We presume that the complexities of staphylococcal epidemiology are at work here in that there are several ways that a patient could ultimately acquire MRSA, including air transmission, environmental contamination, or delivery from a carrier. These are not necessarily affected by short staffing of nurses.

Antimicrobial susceptibility testing of MRSA isolates suggested that at least 2 strains from each cluster were related in that they demonstrated identical antibiograms (Table 4). The third strain from 3 of the clusters appeared similar by susceptibility testing to strains from neighboring clusters. We suspect that unique strains were introduced into the unit by patients from other hospitals and then transmitted to others at a later date (data not shown). This occurred despite the fact that the original patient was no longer a resident on the unit.

Table 4. Isolation dates and selected antibiotic susceptibilities of MRSA isolates^∗ acquired in the ICU

Fus, fusidic acid; Neo, neomycin; Tob, tobramycin; Gen, gentamicin; Rif, rifampicin; Mup, mupirocin; Tmp, trimethoprim; S, susceptible; R, resistant; U, unknown.

^∗Only first isolate susceptibilities are shown. Isolates with similar antibiotic susceptibilities are identified with the same symbol, eg, ^†patients 1, 2, 3, and 6; ^‡patients 4, 5, 9, and an environmental isolate; ^§patients 7, 8, and 10; and ^¶patients 11 and 12. Thus, at least 2 patients within each cluster have similar antibiotic susceptibilities, and the remainder are similar to isolates from a neighboring cluster.

Of 160 environmental sites screened, 37 (23%) produced either the presence of an indicator organism (S aureus; MRSA, or other) or quantitative growth of >5 cfu/cm².⁹ Twenty-six of these 37 (70%) were from hand-touch sites, and most furnished large quantities of coagulase-negative staphylococci (CNS).⁶ The number of cleaning failures each week ranged from none to 4 throughout the screening period, with an average of 1.8 failures (Table 2).⁶, ⁹ MRSA was isolated during week 4, 3 days before a sample from patient 4 was shown to be positive. It shared a unique antibiogram with isolates from patients 4 and 5 (Table 4). The unit demonstrated above average numbers of cleaning failures before 9 of 12 acquisitions, the first 3 occurring prior to the environmental screening program and therefore the cleaning status before these MRSA acquisitions remains unknown (Fig 1).

MRSA was not found from any of 18 fingertip cultures, although one doctor had methicillin-susceptible S aureus on his fingers. All cultures demonstrated variable quantities of CNS, and these were subjected to antimicrobial susceptibility testing to group isolates with CNS from other sources. PFGE typing of CNS from environment, staff hands, and patient blood cultures produced several different patterns, but indistinguishable strains from all 3 sources were found on 2 occasions (Fig 3).⁶, ¹⁶ The only environmental strains exhibiting similar profiles to isolates from patients and staff originated from hand-touch sites, ie, bed frame, door handle, and computer keyboard, suggesting dynamic transmission between these sites, staff hands, and patients.

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• Fig 3. 

  Indistinguishable PFGE patterns demonstrated by coagulase-negative staphylococci from staff members' hands, patient blood, and the ICU environment.

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Discussion 

This analysis suggests that new cases of MRSA in the ICU were more likely to occur following a deficit of trained nurses on day duty. There were also environmental hygiene failures during 5 of the 7 MRSA acquisition weeks. Other studies have shown that staff shortages contribute toward hospital-acquired infection rates.⁷, ⁸, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹ The assumption is that staff members do not adhere to basic hand hygiene when they are busy. One study defined nursing workload using dependency calculations, as we did, but did not address the potential role of the environment and its reservoirs of hardy hospital organisms.⁷ Although an infected or colonized patient provides an immediate risk to others in the vicinity, dispersed MRSA can survive long after that patient is discharged.²² This complicates the investigation of an MRSA incident or outbreak. Staff deficiencies, combined with MRSA in the environment, increase the risk of hospital-acquired infection.²¹ Conversely, a heavier workload imposed on a fixed nursing complement results in less attention to basic infection control practices.¹⁷, ¹⁸, ²⁰

The precise timing of initial MRSA delivery can never be ascertained, only the sampling date of swabs taken on which later grow MRSA in the laboratory. Other studies have elicited the interval between MRSA colonization and infection.²³ We had to estimate the interval between first acquisition of MRSA, from whichever source, and laboratory confirmation from a clinical specimen. A few colony-forming units of MRSA delivered to a vulnerable site may not necessarily be detectable from a clinical sample for several days. It was important to decide when the hygiene lapses might have occurred, facilitating acquisition, in relation to laboratory detection. Because specimens were sent every other day, we were confident that established colonization/infection was identified promptly, given the inoculum required to produce growth on mannitol salt agar. There were factors influencing this interval, however, that we could not measure–patient vulnerability, tissue viability, original inoculum, exact timing of screening, and effects of antimicrobial chemotherapy.

We chose 4 days as a best estimate for MRSA incubation in this setting. There is some evidence to support this, from early work performed on staphylococcal infection. Noble found that cotton threads placed in superficial wounds in mice accelerated the development of an abscess, with visible pyogenic lesions elicited in 1 to 4 days.¹³ Human studies vary in their estimates of incubation period, ranging from 1 to 6 days, and none are directly analogous to our patients.¹⁴ Experimental induction produced infection in 24 to 48 hours in human skin, but the inoculum required for this was 4 to 8 million staphylococci.²⁴ It is reasonable to assume that the incubation period is inversely proportional to the original inoculum, but we doubt that our patients received this magnitude of dose at first acquisition. A clinical study in surgical patients found a median interval of 6 days, but the end point was determined by diagnosing the clinical features of established infection.¹⁴ We were routinely screening patients, actively seeking MRSA colonization. The latter study also discussed the effects of antibiotics, which not only prolonged the interval between acquisition and infection but also increased the chance of infection with resistant staphylococci.¹⁴ Our patients were all receiving antibiotics, none of which were clinically appropriate for MRSA. We therefore decided on a 4-day interval between acquisition and laboratory detection for our ICU patients. This incubation period then cast suspicion on events occurring during the week prior to 7 of the cases and for the actual week of detection for the remainder (Table 2).

This was a retrospective study, and MRSA strains from superficial sites were discarded by the laboratory and therefore unavailable for genotyping. None of the patients who acquired MRSA while a resident on the ICU produced positive blood cultures. Given phenotypic limitations therefore, we were cautious about analyzing strain relatedness. Examination of extended antibiogram, however, allowed speculation within the relevant time frame (Table 4). Within each cluster, at least 2 of 3 patients produced first MRSA isolates with identical antibiograms, and some resistance patterns were identical to strains identified weeks before. Staphylococci easily survive in the hospital environment, although their exact location is not readily identifiable.³, ⁴, ⁵, ⁶, ²², ²⁵

Some of the resistance patterns from the MRSA isolates were sufficiently different, given the overall series of 28 strains, to justify transmission hypotheses. We suspect that patients transferred from other hospitals introduce “new” strains into the ICU environment. These are then identified from other patients at a later date. Our “clusters,” however, did not depend on genotyping similarities to demonstrate a breakdown in hygiene; each new acquisition of MRSA, whether clustered or not, results from a lapse in infection control for a variety of reasons. The fact that 4, 3-patient clusters occurred at discrete and irregular intervals in our ICU provided the impetus for us to launch this investigation.

We examined colonization pressure as a potential factor that might be associated with MRSA acquisition on the ICU. No association was found, which contrasts with previous findings.¹² Although an understanding of staphylococcal epidemiology would lead one to believe that more patients with MRSA in an ICU should increase the risk to other patients, we would question the effect of the denominator (total number of patients in the ICU) in reducing this risk as bed occupancy rises. Given the same number of MRSA patient-days within the same length of time, we think that a unit with 100% occupancy is more at risk than one that is only half full. Yet the colonization pressure from a unit that is full is deemed to be less than the latter, using this denominator. It appears that the complexity of staphylococcal acquisition does not easily fit into a simple equation–as well as confounding attempts to identify the most important factors in MRSA transmission (cf, week 5).

We only found MRSA once from the environment and none at all from staff members' hands. Finding indistinguishable strains of CNS from hand-touch sites, staff members' hands, and patient blood cultures suggest dynamic transmission between these sites in this ICU (Fig 3).⁶, ¹⁶ This strengthens the transmission hypotheses but does not determine the origin of strains or direction of delivery. Given the epidemiologic relatedness of staphylococcal species, however, such a transmission cycle could occur with coagulase-positive staphylococci, including MRSA.⁵

In conclusion, we believe that understaffing of trained nurses is a risk factor for MRSA acquisition in this ICU. The risk may be enhanced by hygiene failures in the ICU environment, which would allow persistence of resilient pathogens. Prospective studies are now required to demonstrate the dynamic relationships of bacterial transmission between staff, patients, and the environment and confirm the exact mechanism by which patients ultimately acquire MRSA. Such evidence will then allow us to intervene in a timely and cost-effective manner.

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The authors thank Barbara Nolan, all ICU staff, the Department of Health (London) for funding the environmental screening, Dr. John Cowden for epidemiologic advice, Professor Chris Robertson and Robert Hill for statistical analyses, and Dr. Donald Morrison from the Scottish Staphylococcal reference laboratory for helping us with the PFGE typing.

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References 

1. Weber DJ, Raasch R, Rutala WA. Nosocomial infections in the ICU: the growing importance of antibiotic-resistant pathogens. Chest. 1999;115:S34–S41
   • View In Article
2. Bauer TM, Ofner E, Just HM, Just H, Daschner FD. An epidemiological study assessing the relative importance of airborne and direct contact transmission of microorganisms in the medical intensive care unit. J Hosp Infect. 1990;15:301–309
   • View In Article
   • Abstract
   • Full-Text PDF (559 KB)
   • CrossRef
3. Boyce JM, Potter-Bynoe G, Chenevert C, King T. Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect Control Hosp Epidemiol. 1997;18:622–627
   • View In Article
   • MEDLINE
4. Lemmen SW, Hafner H, Zolldan D, Stanzel S, Lutticken R. Distribution of multi-resistant gram-negative versus gram-positive bacteria in the hospital inanimate environment. J Hosp Infect. 2004;56:191–197
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (166 KB)
   • CrossRef
5. Bhalla A, Pultz N, Gries DM, Ray A, Eckstein EC, Aron DC, et al. Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalised patients. Infect Control Hosp Epidemiol. 2004;25:164–167
   • View In Article
   • MEDLINE
   • CrossRef
6. Dancer SJ, Coyne M, Robertson C, Thomson A, Guleri A, Alcock S. Antibiotic use is associated with resistance of environmental organisms in a teaching hospital. J Hosp Infect. In press.
   • View In Article
7. Vicca AF. Nursing staff workload as a determinant of methicillin-resistant Staphylococcus aureus spread in an adult intensive therapy unit. J Hosp Infect. 1999;43:109–113
   • View In Article
   • Abstract
   • Full-Text PDF (231 KB)
   • CrossRef
8. 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;185:481–488
   • View In Article
   • MEDLINE
   • CrossRef
9. Dancer SJ. How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals. J Hosp Infect. 2004;56:10–15
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (79 KB)
   • CrossRef
10. Neumeister B, Kastner S, Conrad S, Klotz G, Bartmann P. Characterization of coagulase-negative staphylococci causing nosocomial infections in preterm infants. Eur J Clin Microbiol Infect Dis. 1995;14:856–863
    • View In Article
    • MEDLINE
    • CrossRef
11. Emori TG, Culver DH, Horan TC, Jarvis WR, Olson DR, Banerjee S, et al. National nosocomial infections surveillance (NNIS): description of surveillance methods. Am J Infect Control. 1991;19:19–35
    • View In Article
    • Abstract
    • Full-Text PDF (1667 KB)
    • CrossRef
12. Merrer J, Santoli F, Appere de Vecchi, Tran B, De Jonghe B, Outin H. “Colonization pressure” and risk of acquisition of methicillin-resistant Staphylococcus aureus in a medical intensive care unit. Infect Control Hosp Epidemiol. 2000;21:718–723
    • View In Article
    • MEDLINE
    • CrossRef
13. Noble WC. The production of subcutaneous staphylococcal skin lesions in mice. Br J Exp Pathol. 1965;46:254–262
    • View In Article
    • MEDLINE
14. Minchew BH, Cluff LE. Studies of the epidemiology of staphylococcal infection. 1. Infection in hospitalised patients. J Chron Dis. 1961;13:354–373
    • View In Article
15. Pirret AM. Utilizing TISS to differentiate between intensive care and high dependency patients and to identify nursing skill requirements. Intensive Crit Care Nurs. 2002;18:19–26
    • View In Article
    • Abstract
    • Full-Text PDF (132 KB)
    • CrossRef
16. Dancer SJ. How antibiotics can make us sick: the less obvious adverse effects of antimicrobial chemotherapy. Lancet Infect Dis. 2004;4:611–619
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (1945 KB)
    • CrossRef
17. Borg MA. Bed occupancy and overcrowding as determinant factors in the incidence of MRSA infections within general ward settings. J Hosp Infect. 2003;54:316–318
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (170 KB)
    • CrossRef
18. Bignardi GE, Askew C. Workload may be related to the spread of MRSA and other infections. J Hosp Infect. 2000;45:78–80
    • View In Article
    • Abstract
    • Full-Text PDF (116 KB)
    • CrossRef
19. Russell B, Ehrenkranz NJ, Hyams PJ, Gribble CA. An outbreak of Staphylococcus aureus surgical wound infection associated with excess overtime employment of operating room personnel. Am J Infect Control. 1983;11:63–67
    • View In Article
    • Full-Text PDF (603 KB)
    • CrossRef
20. Fridkin SK, Pear SM, Williamson TH, Galgiani JM, Jarvis WR. The role of understaffing in central venous catheter-associated bloodstream infections. Infect Control Hosp Epidemiol. 1996;17:150–158
    • View In Article
    • MEDLINE
21. Arnow P, Allyn PA, Nichols EM, Hill DL, Pezzlo M, Bartlett RH. Control of methicillin-resistant Staphylococcus aureus in a burns unit: the role of nurse staffing. J Trauma. 1982;22:954–959
    • View In Article
    • MEDLINE
22. Wagenvoort JH, Sluijsmans W, Penders RJ. Better environmental survival of outbreak vs. sporadic MRSA isolates. J Hosp Infect. 2000;45:231–234
    • View In Article
    • Abstract
    • Full-Text PDF (78 KB)
    • CrossRef
23. Truffault A, Mimoz O, Karim A, Edouard A, Nordmann P, Samii K. Colonization by methicillin-resistant Staphylococcus aureus is a predictive factor for the resistance phenotype of an infectious strain of S. aureus. Ann Fr Anesth Reanim. 2000;19:151–155
    • View In Article
    • MEDLINE
    • CrossRef
24. Elek SD, Conen PE. The virulence of Staphylococcus pyogenes for man: a study of the problems of wound infection. Br J Exper Pathol. 1957;38:573
    • View In Article
25. Low DE, Schmidt BK, Kirpalani HM, Moodie R, Kreiswirth B, Matlow A, et al. An endemic strain of Staphylococcus haemolyticus colonizing and causing bacteraemia in neonatal intensive care unit patients. Pediatrics. 1992;89:696–700
    • View In Article
    • MEDLINE