Objective. Six neonatal intensive care units (NICUs) that are members of the Vermont Oxford National Evidence-Based Quality Improvement Collaborative for Neonatology collaborated to reduce infection rates. There were 7 centers in the original focus group, but 1 center left the collaborative after 1 year. Nosocomial infection is a significant area for improvement in most NICUs.
Methods. Six NICUs participating in the Vermont Oxford Network made clinical changes to address 3 areas of consensus: handwashing, line management, and accuracy of diagnosis. The summary statements were widely communicated. Review of the literature, internal assessments, and benchmarking visits all contributed to ideas for change.
Results. The principle outcome was the incidence of coagulase-negative staphylococcus bacteremia. There was an observed reduction from 24.6% in 1997 to 16.4% in 2000.
Conclusions. The collaborative process for clinical quality improvement can result in effective practice changes.
- nosocomial infection
- line management
- blood cultures
- collaborative quality improvement
- NIC/Q 2000
KEY POINTS OF ARTICLE
All participating sites began with hand hygiene improvements.
Vascular line management was recognized as another key element in reducing infection.
Improved accuracy of infection diagnosis is needed because of problems with contaminated blood culture.
It was helpful to quantify the impact of infections including impact on length of stay and cost.
APPLYING LESSONS LEARNED TO PRACTICE
Multiple issues may require resolution before program changes can be initiated.
Ongoing evaluation is an important component of the change process.
Public relations is an important aspect of the education process around new practices.
Nosocomial bacteremia is a significant contributor to neonatal morbidity and mortality.1 The frequency of this complication varies among neonatal units and seems to be related, at least in part, to management decisions and practice style.2 Investigations have suggested that selected interventions could lower the risk of nosocomial infections (NIs).3,4
As described in an earlier report, 6 institutions participating in the Vermont Oxford Network (VON) entered into a 2-year collaborative with the goal of reducing by 50% coagulase-negative staphylococcus (CONS) bacteremia for infants <1500 g birth weight.5 Bacteremic events caused by CONS were targeted because this organism is known to be the most frequent cause of neonatal NI.1 To accomplish this objective, multidisciplinary teams representing each of the 6 institutions collaborated to develop lists of potentially better practices (PBPs) thought to be related to lowering infection rates. The PBPs were prioritized. As appropriate, PBPs were joined together into larger perspectives referred to as “summary statements.” The summary statements addressed hand hygiene, line management, and accuracy of diagnosis. The participating institutions implemented and documented their changed practices. This article describes the implementation at different institutions, obstacles that were encountered, and the effects on clinical processes and NI rates.
Each participating institution made clinical changes to address the 3 areas of consensus: hand hygiene, line management, and accuracy of diagnosis. As shown in Table 1, not all PBPs were undertaken by every institution. Some practices had previously been incorporated as routine care at several hospitals. PBPs were given different priority at different hospitals. All recognized the importance of handwashing and either were already performing or changed to the PBPs in this area. “Hub care” practices were implemented eventually in all 6 participating units, although in 1, implementation was delayed until after this project was completed.
Line standardization was assessed and adopted in 5 of the 6 units. However, in most units, implementation of “closed system” access was deferred or was only partially implemented. At 3 hospitals, closed access was implemented for deep venous lines. Only 2 hospitals implemented closed access with their umbilical lines. One group described inadequate hardware as a barrier, forcing several product changes and delays in implementation. The “accuracy of diagnosis” was variably addressed by the units and depended on the perception of need for changes in this area. Not all units seemed to have the same level of difficulty with contaminated blood cultures and overuse of antibiotics. The 2 units that implemented most of these changes had identified differences in the frequency of sepsis evaluations between themselves and the benchmark hospitals. Although a specialized phlebotomy team was developed as a PBP based on benchmarking, this was not implemented in any unit. This may be explained in part by the fact that the PBP would have required large changes in residency training and use of bedside nursing personnel that were not considered warranted. See Table 1 for details.
Implementation of Specific Summary Statements
Handwashing (mechanical removal of organisms from hands) is considered a key aspect of hand hygiene (elimination of organisms from hands). Because spread of organisms by hand contact is universally accepted as the leading means of dissemination of infectious agents, hand hygiene was adopted by the group as a first priority in lowering infection rates.6 Both the Centers for Disease Control and Prevention and the American Hospital Association recommend routine handwashing before and after each patient contact, although compliance with this recommendation has always been problematic.7 The PBP on hand hygiene emphasized the importance of vigorously washing hands 10 to 15 seconds before and after all patient contacts, after using gloves during patient care, and when in contact with patient equipment.
Improving compliance with hand hygiene presented unique challenges to participating institutions. When performed correctly before and after each patient contact, appropriate handwashing involves as many as 100 actions throughout the day. Even if everyone is supremely motivated, high workloads can generate a need for handwashings that, if conducted for the recommended duration, can exceed the time available for patient care.8 The activity also involves participation of personnel from multiple disciplines, who work throughout the institution and have varying exposure to NICU goals and policy.
After review of the literature, the participating institutions recognized that improved compliance with current protocols was the first and most important goal. It was hypothesized that education, monitoring, and feedback to staff would modify behavior, resulting in improved compliance and effectiveness. At each institution, the first step was to conduct a baseline assessment of compliance with existing policy. All NICUs in the country have standing policies on handwashing with varying adherence to the policy. All units in the group to assess baseline compliance, which was universally reported as low by group members, used audit tools designed locally.
The second step was a campaign of education, using the documented incidence of poor compliance as a motivator to help staff adopt a higher level of commitment. The results of the baseline studies were disseminated through educational in-service sessions, e-mails, handouts, and demonstrations. At this stage, participating institutions not only reinforced the rationale for complying with existing policies but also capitalized on the discussions generated by negative results to introduce changes in policy. Most changes were directed at techniques to improve the frequency of handwashing while addressing concerns regarding skin breakdown and sensitivity to antisepsis agents.
The third phase involved repeated assessments of compliance after the initial campaign, usually in the form of small audits performed publicly to serve as reminders for staff, who became aware that they were being observed. In other cases, units devised methods using new personnel or rotating residents to obtain objective information without observational bias.
The fourth phase was feedback to staff on the data from these intermediate assessments. This was usually given as periodic updates on progress or lack of improvement. The feedback also involved exchange of information and processing of successful and unsuccessful strategies to introduce change.
The audits of handwashing compliance were the most common and perhaps the most important tools for changing behavior. Units initially developed their own audit tools. The rapid deployment of these tools enabled units to identify quickly the areas where improvement was necessary and provide feedback in a timely manner to staff. The downside to this decentralized approach was the inability to measure compliance for the group as a whole, because data were not obtained uniformly. In an attempt to achieve uniformity, at the end of the 18-month collaboration, a single tool was adopted by the group9 and used by all participating institutions (Fig 1). This audit tool was administered during the first quarter of 2001 at the 5 institutions that remained in the collaborative. In using the tool, observations were made anonymously by a single untrained observer in the NICU. Compliance was defined as appropriate use of antiseptic agent at handwashing opportunities, before and after each contact with a patient. Results of the audit showed 78% to 100% compliance (Fig 2). Preintervention baseline data were not available at all units for comparison.
The handwashing changes incorporated by group members were the result of a literature review and discussion among the groups. Most units adopted similar changes in the following areas: 1) initial wash, 2) interval wash, and 3) elimination of jewelry and artificial nails.
The traditional practice was to perform a 3- to 5-minute scrub using a brush on entry to the unit. When evidence that discouraged this practice was disseminated, this was an important step in improving compliance. It provided better credibility for handwashing “enthusiasts,” because they were less likely to be seen as advocates of policies that were unpopular, unenforceable, or ineffective. An initial wash of 15 to 60 seconds replaced the former practice. Brushes were recommended only for parents or staff who had heavily soiled hands.
This became the primary focus because it represented the area with the greatest noncompliance and potential for improvement. Barriers to compliance included skin breakdown from repeated friction and application of antisepsis agents, lack of time, involvement of multiple disciplines, and human nature. Strategies to overcome these barriers included introduction of new antisepsis agents: 2% chlorhexidine instead of 4% chlorhexidine, the addition of 3% triclosan at the sinks for staff with chlorhexidine-sensitive skin, and use of lotions that were compatible with the antibacterial agents.
Some units added waterless alcohol gels at the bedside to enhance compliance when sinks were not readily accessible and time between patients was limited.10 One unit performed 5 simultaneous PDSA cycles to evaluate different alcohol products before making a decision. Once the new agents had been introduced, ongoing educational efforts were made using posters, e-mail messages, newsletters, instructional pamphlets, and videos. A novel product used by several units was Glo Germ, a substance that when applied to hands of staff demonstrates the efficacy of handwashing. This product clearly showed staff the effects of improper handwashing techniques. As mentioned above, serial audits with feedback to the staff were an important strategy for enhancing compliance.
The question of when handwashing was necessary came under scrutiny during this project. It was clearly necessary to wash between patient contacts, but it was not clear why it was required when a provider touched the top of the incubator or side of the ventilator. Discussion of these issues led to the concept of a “clean touch” zone that surrounds an infant’s incubator or crib. Providers were asked to practice hand hygiene when contacting or leaving the areas contiguous to the infant. A PDSA cycle implementing the “clean touch” policy is provided for illustration in Fig 3.
Elimination of jewelry and artificial nails
Eliminating use of hand and arm jewelry and artificial nails met with opposition in all units. These practices represent personal lifestyles of NICU staff, and changes in them extend beyond the workplace (eg, elimination of stylish nails or switching to a simple wedding band). In some areas of the country, acrylic nails are an especially popular accessory worn by many members of NICU staff. The infection control officers and nurse managers provided evidence linking NI with these practices. This was an important first step in achieving buy-in. In 1 unit, however, staff were willing to accept elimination of artificial nails only after several occurrences of pseudomonas NIs.11 In some units, unequivocal unit policies created and enforced by the unit manager became the last resort in achieving compliance with elimination of jewelry and artificial nails. This is the least desirable strategy because authoritative enforcement of policies in 1 area often leads to a negative and subversive reaction in other areas and undermines staff’s positive attitude toward responsible individual behavior in reducing infection.
Epidemiologic studies indicate that neonatal NIs, particularly those as a result of CONS, are frequently associated with indwelling catheters.12 Organisms that colonize catheter hubs are often the same as those isolated from the catheter tips or blood of infants who have a diagnosis of catheter-related sepsis.13 The frequency of line entry affects the incidence of catheter-related sepsis.14 Decontaminating hubs at the time of entry or connection with rubbing (friction) and alcohol will decrease colonization15 and result in lower rates of bacteremia.16 Because the evidence strongly suggests that the design and management of vascular lines can play a significant role in lowering the risk of nosocomial bacteremia, the PBP included several PBPs directed at these issues.
The summary statement5 recommended that line setups should provide access using the minimum number of ports. Breaks into the line should be reduced by adhering to recommendations that lipid infusions be changed only once every 24 hours. Parenteral fluids with amino acids should be changed once every 48 to 72 hours. Connectors and hubs need not be changed at other times unless there is breakdown or signs of residue. Finally, the most important PBP relates to antisepsis maneuvers surrounding hub entry or disconnection. At the time of entry, the operator, after first properly performing hand hygiene and establishing a sterile field, should rub the hub vigorously with alcohol. Implementation suggestions included provision of adequate supplies, a training program, and evaluation and monitoring tools.
The vascular line setup and care objectives required units to address several complex and ubiquitous components of medical and nursing practice. These included standardization of line setups, ways to implement “closed” vascular systems (including umbilical lines), and line entry techniques (termed “hub care process”). The tasks related to implementing these PBPs were particularly daunting because current intravenous hardware and procedures for neonatal use are not standardized.
Each unit noted that it was time consuming and challenging to review, clarify, and then modify their many existing practices in light of the summary statement. These challenges were compounded when units sought to address the mechanics and processes necessary to implement “closed vascular access systems” for umbilical catheters. In addition, material management issues relating to hardware availability, product compatibility, stocking procedures, and communication required resolution. When access to a new provider was required, units had to overcome prohibitions against buying materials not provided by the hospital’s buying consortia.
Significant efforts were required to develop (or revise) policies and procedures, staff education modules, skills teaching laboratories, competency tests (usually also requiring incorporation into the nurses’ and respiratory therapists’ annual performance evaluation processes, see Fig 4), and visual cues to reinforce the desired process (note the “hub care” logo in Fig 5). A PDSA cycle to address “closed access” is shown in Fig 6. Figure 7 shows the audit tool for line standardization and management.
The first unit to adopt these changes distributed its materials electronically. As units made additional improvements and refinements, materials were recirculated back among the members.
The units rolled out new practices after announcements and other attention-getting events. Different communication styles were used by each of the units, reflecting local conditions and “unit cultures.”
Finally, the means to monitor compliance and complications were addressed. Each unit included individual competency testing as part of their line and hub care program, both in the initial training phase and later as part of a collaborative-wide, postimplementation assessment. Usually, an aggregate score was calculated and displayed after postimplementation testing. Later, using a common “hub care” indicator, 5 collaborating units tested a majority of their staff from 1 month to 1 year after implementation. Four units reported aggregate competency scores between 90% and 100% for their staffs. The remaining unit found only a 57% competency score. Some units adopted a targeted approach to their reinforcement efforts, such as monitoring line setups daily for all infants with birth weights <1000 g (see Fig 6 “Act-Cycle” and Fig 7). This enabled reinforcement of compliance and education in real time (“one-on-one” process control) and also enabled the collection and distribution of aggregate trending data.
Accuracy of Diagnosis
The objective of this collaborative was to decrease the incidence of CONS bacteremia. CONS, as a component of normal skin flora, may contaminate blood cultures and lead to a false-positive identification of bacteremia. The definition of CONS infection was that of the VON. It requires a positive culture from blood or cerebral spinal fluid, signs of generalized infection, and treatment with 5 days or more of antibiotics.5 Because considerable variation occurs in blood-drawing practices and clinical interpretation of the significance of positive blood cultures, measured rates of CONS bacteremia may include both true CONS infections and false positives (contaminated blood cultures).
False-negative interpretation may occur when an inadequate specimen of blood is obtained.17 Therefore, the participating units developed a PBP to assist in more accurately defining “true” infection. This PBP emphasized the site and number of blood cultures, preparing for blood culture, personnel performing blood cultures, volume of blood for culture, discontinuation of antibiotics, and ancillary tests.1 It was recognized that a more accurate diagnosis of CONS bacteremia might not decrease the incidence of true bacteremia, but it would lower the reported rate by decreasing inclusion of false positives. This was considered desirable because the subsequent overtreatment of these infants may lead to secondary morbidity.18,19
The first PBP implemented in this area related to obtaining 2 blood cultures with each nosocomial sepsis evaluation. Objections to implementation primarily related to excessive blood removal and skin punctures for extremely low birth weight infants. These concerns had to be addressed at the outset (Fig 8). The approach had to be flexible to allow for limited blood drawing for the most fragile newborns. However, for most infants, obtaining dual cultures was an acceptable risk. Feedback to nurses and physicians led to routine implementation of the practice as nurse phlebotomists and physicians observed that the results of the double cultures were used to make better antibiotic treatment decisions. Five units implemented policies on obtaining double blood cultures. Some of the policies emphasized that the second blood culture should be obtained from a central line, to avoid the issue of multiple skin punctures. Two units designed decision trees that called for central line cultures and protocols for dealing with positive cultures, including line removal with repeated positive cultures.20
Improved skin preparation before drawing a blood culture was addressed by 2 units in new policies that changed the manner of skin preparation. The other units reviewed and reinvigorated existing phlebotomy procedures. The consensus reached was that the precise technique of preparing the skin was not as important as the rigor with which the chosen technique was used. Data suggest that 1 mL is the optimal sample volume for maximizing the yield when culturing blood. The major objections to obtaining this volume were the actual volume of blood that had to be removed and the technical difficulties of obtaining 1 mL of blood with every peripheral phlebotomy. Four units initiated policies regarding drawing this volume of blood. Two units conducted PDSAs to facilitate implementation (Fig 9). After the PDSA cycles, 1 unit noted that 92% of cultures had a volume of 1 mL or greater.
The discontinuation of antibiotics at 48 hours when blood cultures were negative was considered important in limiting antibiotic exposure and decreasing the need for vascular access to deliver antibiotics. Most of the units reported that their previous practice was compatible with this PBP, but 3 reemphasized this practice with new policies and the development of the decision trees discussed above. Ancillary tests, such as C-reactive protein 21 and various white blood cell indices, were implemented in 1 unit to aid diagnosis and treatment decisions. Other units reported that these tests were already being used.
The practice of having a specialized team draw blood cultures was not implemented in any unit, despite evidence that such a team reduces the rate of contaminated blood cultures.22 The major reasons for nonimplementation were cost and the requirement for substantial change in unit culture.
Multidisciplinary staff in all 6 units considered and discussed the PBPs. The response of each unit depended on its existing practices and culture. Some of the PBPs had already been established and required no action or perhaps only reinforcement of existing policies. Most of the units, however, developed more comprehensive policies or decision trees that contained several of the PBPs (Fig 10).
The principal outcome measure was the incidence of CONS bacteremia. In 1997, the last year before the initiation of the cooperative, the mean incidence of CONS bacteremia for the collaborating institutions was 24.6%. For the 6-month period ending in December 2000, the mean incidence was 16.4% (relative risk: 0.67; 95% confidence interval: 0.51–0.87). Figure 11 shows the changes in incidence of CONS bacteremia in the 6 participating institutions.
This quality improvement collaborative resulted in the development of evidence-based summary statements directed at lowering rates of NI in NICUs. The statements were widely communicated and became the basis for multiple changes in clinical practices in the collaborating institutions. Review of the literature, internal assessments, and benchmarking all contributed ideas for change and identified practice options, with levels of evidence for each. Through small change cycles, involving monitored implementations, subsequent analysis, and shared experiences, collaborators quickly clarified priorities and began to understand the obstacles that needed to be addressed for success. Often, the data generated from trials at 1 institution became the strongest evidence available for making change decisions at the others.
Each unit began PDSA changes with hand hygiene practices. All addressed this issue, and approximately 80% of the hand hygiene PBPs were implemented throughout the focus group. Unit handwashing policies were recognized as the cornerstone for reducing nosocomial bacteremia. Because of the ubiquitous nature of handwashing, units with successful implementation of a handwashing policy were observed to have a philosophy of accountability, embodied in the statement that “nosocomial infection is not an entitlement in our unit.” Thus, the occurrence of an infection represented a failure, not a natural event, in the hospital course of a preterm infant. The group observed this commitment in several of the benchmark hospitals where avoidance of NI and almost ritualistic handwashing were a part of the unit culture.
The collaborating institutions also recognized the importance of vascular line management in altering the rate of nosocomial bacteremia in the NICU. Each unit addressed hub care. The reduction of vascular line entry points was investigated by all, although not successfully accomplished by all. Interinstitutional collaboration was made difficult by lack of standardization of nomenclature and hardware for vascular access devices. Supply issues emerged with the hospitals’ unique purchasing contracts, which limited the availability of some equipment.
At the same time, the situation in California was confounded by the requirement to implement “needleless” access systems, without provision of the means to do that in neonatal settings (eg, umbilical lines). In addition, this aspect of clinical care has not been widely investigated in randomized trials that provide clear evidence of which practices are efficacious in lowering infection rates, particularly in neonatal care. Thus, the experiences of this collaborative often represent the best available evidence.
The third PBP addressed improved accuracy of diagnosis. Members of the collaborative recognized that some CONS bacteremia may represent contaminated blood cultures. Improved techniques to obtain specimens were reviewed by all units, some of which adopted changes even without PDSA involvement. When collaborating units shared information regarding the frequency of contaminated cultures, those with the fewest identified false positives were noted to have the highest antibiotic usage. This suggested that at some units, clinicians were reluctant to label a positive blood as false, thus perhaps unnecessarily “treating” some infants with antibiotics. In these units, practices to improve clarification of CONS bacteremia were given high priority. In other units, PBPs about diagnosis accuracy were not targeted for initial changes.
Although many of the PBPs were unique, the implementation processes for all navigated a similar course. All had to overcome similar challenges, following the pattern described by Geertsma23 in his assessment of practice behavior changes. Before the PDSA cycles were initiated, it was necessary to educate unit staff about high NI rates. It quickly became evident that if staff did not see the importance of making change, then introduction of new procedures would not be possible. The impact of NIs on patient outcomes, including length of stay and costs, and the importance of staff behavior in lowering the risks of infection were emphasized early in the process. A large number of providers were involved in almost all of the targeted behavior changes. With hand hygiene practices and line management issues, all of the staff nurses, many physician providers, and personnel who frequented but were not directly assigned to the NICU needed to become aware of the altered practice.
Once the unit was primed for change, multiple issues often required resolution before a program could be initiated. For example, line setup needed to be understood, hub care needed to be defined, and alternatives needed to be described and evaluated before the simultaneous change of so many integrated practices was begun. The PDSA cycle model allowed for division of the task into many discrete components. In each unit, groups of 4 or more people addressed each of these components of the change agenda and worked simultaneously.
Involvement of so many staff facilitated participation in the change process and developed advocates of change among the staff. Change would not have been possible without the commitment of all disciplines working in the nursery. Everyone interfacing with the infants needed to participate actively in the new hand hygiene procedures. Observational tools to assess compliance had to apply to both the physician and the nursing staff. It was important that all staff felt a part of the team fighting to lower the risk of infection. Although hub and line care were primarily provided by nurses, medical leadership participated. Physicians emphasized the importance of these changes and provided positive feedback when procedures were done well.
Initial successes were reinforced so that other staff who were less open to change became more excited about the process. Public relations became an important aspect of the project, particularly in making change “fun.” Posters emphasizing hand hygiene or “hub care” were colorful and usually in cartoon form. When Glo Germ was used to teach about handwashing, it was not used punitively. It allowed staff to laugh at their colorful hands, emphasizing the need to be more complete in rubbing with the next attempt.
Although these efforts worked well for limited issues, widespread staff involvement and buy-in were possible only with clear and frequent communications. Information was disseminated through e-mail, in-service sessions, regularly scheduled meetings, newsletters, open discussions, and posters. No 1 approach was successful for all institutions because cultures and structures differed. At 1 hospital with a personal computer available at each bedside, staff nurses routinely accessed e-mail notices. At another, e-mails were largely ignored and written memos and meeting announcements were much more widely used.
In addition to changing staff attitudes and knowledge base, interventions sometimes required structural change. For instance, 1 institution modified a computer order entry screen to facilitate the phlebotomist’s entry on the site and quantity of the blood draw, data necessary for assessing the diagnostic accuracy of blood cultures. As noted above, when addressing line management, lack of standardization of equipment made interinstitutional collaboration difficult. In some cases, the changes could not occur until new products were purchased. However, change was aided by the free communication between institutions, usually involving administrative as well as medical personnel.
Evaluation was an important component of the change process. The PDSA cycle methodology reinforced the need to evaluate the impact of each intervention trial and readjust it as required. Intermediary process goals were used, and both individual and group feedback were provided to motivate continuous improvement. Unit-wide feedback was also a common feature of successfully implemented practice changes.
On the basis of the currently available data, this quality improvement collaborative seems to have been a success. Certainly, clinical processes were successfully changed in the 6 units. Hand hygiene compliance measures showed improvement. Line setups were reevaluated and standardized, and nursing competency scores relating to line management improved. More rigorous criteria for the diagnosis of CONS infections were adopted in several units. Perhaps most important, preliminary data suggest an overall decline in nosocomial bacteremia in the participating units, from 26% to 16%. The differing improvement rates for CONS bacteremia between units might reflect unit differences in the commitment of personnel and the time available for implementing changes. However, the differences may also reflect that the cause of NIs is related to many processes and practices of care, which vary among units. This collaborative may have addressed predominant factors in some units but not in all.
The collaborative involved collectively thousands of hours of work. Initially, development and prioritization of the PBPs was done. Subsequently, implementation of the changes on the various services had to be completed. Associated with this investment has come an apparent decline in CONS NIs in the 6 collaborating NICUs. It has not been proved which, if any, of the interventions is responsible for the decreased rate of infection. In 1 institution, the decline in the infection rate may be related to more focused diagnosis, with less contamination and overtreatment of false positives. However, for most of the NICUs, it seems that the actual risk of NI from CONS decreased during the project period. This experience supports the importance of multi-institutional, multidisciplinary collaboration for quality improvement in neonatal care.
- ↵Gaynes RP, Edwards JR, Jarvis WR, et al. Nosocomial infections among neonates in high-risk nurseries in the United States. Pediatrics.1996;98 :357– 361
- ↵Kilbride HW, Powers R, Wirtschafter DD, et al. Evaluation and development of potentially better practices to prevent neonatal nosocomial bacteremia. Pediatrics.2003;111(suppl) :e504– e518
- ↵Mueller-Premru M, Gubina M, Kaufmann ME, et al. Use of semi-quantitative and quantitative culture methods and typing for studying the epidemiology of central venous catheter-related infections in neonates on parenteral nutrition. J Med Microbiol.1999;48 :451– 460
- ↵McCarthy MC, Shives JK, Robison RJ, et al. Prospective evaluation of single and triple lumen catheters in total parenteral nutrition. J Parenter Enteral Nutr.1987;11 :259– 262
- ↵Salzman MB, Isenberg HD, Rubin LG. Use of disinfectants to reduce microbial contamination of hubs of vascular catheters. J Clin Microbiol.1993;31 :475– 479
- ↵Calil R, Marba ST, von Nowakonski A, Tresoldi AT. Reduction in colonization and nosocomial infection by multiresistant bacteria in a neonatal unit after institution of educational measures and restriction in the use of cephalosporins. Am J Infect Control.2001;29 :133– 138
- Copyright © 2003 by the American Academy of Pediatrics