OBJECTIVE: We aimed to reduce late-onset bacterial infections in infants born at 22 to 29 weeks' gestation by using collaborative quality-improvement methods to implement evidence-based catheter care. We hypothesized that these methods would result in a 50% reduction in nosocomial infection.
PATIENTS AND METHODS: We conducted an interrupted time-series study among 24 Ohio NICUs. The intervention began in September 2008 and continued through December 2009. Sites used the Institute for Healthcare Improvement Breakthrough Series quality-improvement model to facilitate implementation of evidence-based catheter care. Data were collected monthly for all catheter insertions and for at least 10 observations of indwelling catheter care. NICUs also submitted monthly data on catheter-days, patient-days, and episodes of infection. Data were analyzed by using statistical process control methods.
RESULTS: During the intervention, NICUs submitted information on 1916 infants. Of the 242 infections reported, 69% were catheter associated. Compliance with catheter-insertion components was >90% by April 2009. Compliance with components of evidence-based indwelling catheter care reached 80.4% by December 2009. There was a significant reduction in the proportion of infants with at least 1 late-onset infection from a baseline of 18.2% to 14.3%.
CONCLUSIONS: There was a 20% reduction in the incidence of late-onset infection after the intervention, but the magnitude was less than hypothesized, perhaps because compliance with components of evidence-based care of indwelling catheters remained <90%. Because nearly one-third of infections were not catheter associated, improvement may require attention to other aspects of care such as skin integrity and nutrition.
WHAT'S KNOWN ON THIS SUBJECT:
Late-onset infections cause significant morbidity and mortality in preterm infants. Quality-improvement interventions focused on catheter care have reduced nosocomial infections in adult and pediatric patients but have yet to be proven effective in preterm neonates.
WHAT THIS STUDY ADDS:
This study extended previous work, and the results showed that increased application of evidence-based catheter care as part of a state-based quality-improvement collaborative can reduce infections in preterm neonates. It also highlights the important role of reliability principles in evidence implementation.
Late-onset (>72 hours of life) bacterial bloodstream infections occur in 15% to 30% of preterm infants and are a significant source of morbidity, mortality, and added health care costs.1,2 A majority of these infections are believed to be associated with the use of indwelling vascular catheters.3,4 Quality-improvement (QI) interventions focused on catheter care have reduced nosocomial infection rates in adult and PICUs. Among 108 adult ICUs participating in a QI intervention, attention to evidence-based catheter care resulted in a 66% reduction in catheter-associated bloodstream infections.5 Similarly, use of evidence-based catheter care practices resulted in a 43% reduction in catheter-associated bloodstream infections among a group of PICUs.6 Strategies that result in decreased infection rates in adults and older children may have similar effects in preterm infants. However, preterm infants present special challenges related to relative immunologic immaturity, compromised skin integrity, long lengths of hospital stay, and long duration of catheter use.
Our objective was to reduce the incidence of late-onset infections in infants born at 22 to 29 weeks' gestation in 24 NICUs in Ohio by using collaborative QI methods designed to increase the use of evidence-based central catheter care. We hypothesized that reliable, simultaneous implementation of multiple aspects of catheter care (>90% of opportunities) would result in an aggregate 50% reduction in the incidence of nosocomial infections.
We conducted a multisite, interrupted time-series study. Historical comparison (baseline) data were obtained for the period from April 2006 through August 2008. The intervention began September 2008 and continued for 15 consecutive months. The study was approved by the institutional review board (IRB) of the Cincinnati Children's Hospital Medical Center. All participating NICUs received either IRB approval or were classified as exempt from IRB review. Templates used by teams to prepare their IRB submission and to execute agreements for data sharing are available on the Ohio Perinatal Quality Collaborative (OPQC) Web site (www.opqc.net/toolkit).
Ohio Perinatal Quality Collaborative
The OPQC is a state-based network of Ohio perinatal care clinicians, hospitals, professional organizations, and state agencies with a mission to reduce preterm births and improve outcomes of preterm infants. Participating hospitals and clinicians are supported by a central staff with QI expertise and an administrative and data management infrastructure.7
NICU Participants and Patient Population
All Ohio NICUs that were members of the Vermont Oxford Network (VON) very low birth weight registry were eligible to participate (n = 26). Senior administrators at hospitals with eligible NICUs were required to approve participation. The 24 NICUs that elected to participate include all Ohio NICUs designated by the Ohio Department of Health as level 3 neonatal programs.
Infants were included if they were born between 22 and 29 weeks' gestational age inclusive and were admitted to a participating NICU before 28 days after birth.
Interventions: Catheter Care
On the basis of local unpublished data, we determined that >75% of late-onset infections were associated with catheters. Therefore, the OPQC chose to focus on catheter care during insertion and thereafter (maintenance) until the catheter was removed. On the basis of suggestions from the Centers for Disease Control and Prevention (CDC)8 and existing toolkits,6,9 2 compilations of recommendations for standardized catheter care (bundles) were developed, 1 for care during catheter insertion and 1 for ongoing care (maintenance) (Table 1).
The OPQC used standardized collaborative QI methods based on the Breakthrough Series Collaborative Model of the Institute for Healthcare Improvement.10 Participating NICUs identified multidisciplinary teams that participated in 3, day-long, face-to-face learning sessions (September 2008, January 2009, and October 2009). NICUs were asked to create a team that consisted of a physician, a nurse, a data manager, and as many as 3 additional members. Between learning sessions, teams participated in monthly Web-based seminars, which were used to share aggregate and site-specific results and strategies for change.
Data were analyzed by OPQC staff and provided to teams in a monthly progress report that included their individual site results, aggregate collaborative results, and deidentified comparison results for other participating NICUs.
During the 15-month intervention period, each team was counseled to use the “plan-do-study-act” method11 to implement components of the catheter bundles.
Data Source and Measures
OPQC used 2 data sources: (1) VON registry data; and (2) project-specific local data. For VON data, hospitals used an OPQC-developed, Microsoft Access (Microsoft Corporation, Redmond, WA) query to create a data file from the VON registry that was transmitted monthly for analysis. VON data were available for 13 sites for the entire baseline period. Two sites had baseline data for 20 months before the intervention. The remaining 9 sites reported baseline data for 6 to 8 months before the intervention. After a 1-month run-in period, teams submitted data monthly on bundle compliance for all catheter insertions and for at least 10 observations of indwelling-catheter care. NICU teams also submitted data monthly on total days of catheter use, NICU patient-days, and selected characteristics of each infection. These data were collected by NICU teams by using forms that were pilot tested and refined on the basis of feedback from several sites and were entered into the OPQC Internet-based data-entry system. The Internet-based data-entry system was designed with specific validation rules to improve data quality. In addition, data were reviewed monthly for potential errors (eg, catheter-days equal to patient-days, increases in reported values for a given month compared with previous months, etc). Teams were contacted and asked to resolve any data concerns. External audits of source data were not conducted.
Process measures included compliance with the specified care bundles. Use of each bundle component was analyzed separately. An all-or-none measure of the percentage of observations during which all bundle components were used was also calculated.12
Because it was the only measure for which baseline data were available, the primary outcome, obtained from the VON registry, was the proportion of eligible infants with at least 1 late-onset nosocomial infection. Nosocomial infection was defined according to the VON manual of operations to include: (1) a positive bacterial culture of blood or cerebrospinal fluid (CSF) obtained 72 hours or more after birth, or (2) a positive blood or CSF culture for coagulase-negative Staphylococcus (CONS) obtained 72 hours or more after birth and associated with generalized symptoms of illness and for which the infant received antibiotics for ≥5 days.13 For monthly graphic evaluation of the primary outcome, infants were plotted according to their month of discharge, which means that improvements noted on the control charts may reflect changes in care instituted in earlier months. An infection was labeled as catheter-associated if there was a catheter in place or the catheter was removed <48 hours before the positive blood culture results were obtained.
In the primary analyses we examined whether there were changes in aggregate results summed over the 24 participating NICUs. Statistical process control (SPC) was the primary method used to detect changes in processes and outcomes.14 For the primary outcome, baseline mean and control limits were calculated and displayed for the period from April 2006 through August 2008. The upper and lower control limits reflected the inherent variation in the data and were calculated at ±3 SEs of the mean (based on the binomial distribution). The baseline mean was carried forward and displayed throughout the intervention period. Data values were added monthly and monitored for evidence of significant change by using standard SPC rules, including the presence of (1) 1 point outside the upper or lower control limits, (2) 2 of 3 successive points in the outer third of the control limit, (3) 8 successive points above or below the center line, or (4) 6 consecutive points increasing or decreasing.14 We determined a priori that if 1 of these criteria were met, we would conclude that a significant change occurred.
On the basis of the results of the PICU collaborative,6 we posited that maintenance-bundle compliance would be directly related to reduction in infection. Therefore, we planned a subgroup analysis to determine if there was an association between maintenance-bundle compliance and infection incidence. Infection rates among NICUs that failed to achieve an average of 90% compliance with the maintenance bundle for the last 3 months of the intervention period were compared with NICUs that achieved ≥90% compliance. Because baseline comparison data were not available, process-of-care measures were plotted monthly without mean or control limits, so that we could observe general patterns.
Twenty-four NICUs participated in the study. Of these, 20 were maternity hospitals and 4 were freestanding children's hospitals. All hospitals were located in urban areas. Sixteen (66.6%) of the participating NICUs trained residents and 13 (54.2%) trained fellows. According to birth certificate data, these hospitals care for >90% of Ohio infants born at 22 to 29 weeks' gestation. During the intervention period, 1916 eligible infants were discharged from OPQC NICUs. The range among hospitals was 209 infants in the largest hospital and 10 infants in the smallest hospital. The average baseline prevalence of late-onset nosocomial infection in infants 22 to 29 weeks' gestation among the 24 NICUs (in aggregate) was 18.2%. During the intervention period, NICUs submitted information on 125 150 days of patient care including 42 612 days (34%) with indwelling catheters. There were 242 infections of which 69% were catheter associated and 121 (50%) were caused by bacteria other than CONS, most frequently Staphylococcus aureus (26%), Klebsiella species (14%), Escherichia coli (14%), and Enterococcus species (12%).
Improvements in Processes of Care and Outcomes
Aggregate compliance with all catheter-insertion components was >90% by April 2009 (Fig 1A). For the last 3 months of the intervention period, among sites that submitted at least 30 maintenance-bundle observations (n = 17), maintenance-bundle compliance among NICUs ranged from 8% to 100%. Nine sites (53%) achieved maintenance-bundle compliance of ≥90% by the end of the intervention period. Aggregate compliance with all components of the maintenance bundle reached 80.4% by the end of the intervention period (Fig 1B). Daily documentation of assessment of catheter necessity, use of prefilled flush syringes, and use of a closed system were the slowest bundle components to improve (Fig 1C).
In the postintervention period, there was a reduction in the proportion of infants with infection (Fig 2A). In the 3-month period from April through June 2009, the proportion of infants with infections was consistently low, in the outer third of the control limits, which indicated a significant change based on a priori SPC rules. On the basis of these findings and the concurrent improvements in our processes of care, we adjusted the baseline mean and control limits for the period from April 2006 through December 2008 (average infection rate of 18.2%) and from January 2009 through December 2009 (average infection rate of 14.0%). In the period immediately before significant improvement was documented (April 2009), January 2009 was the first month during which the infection rate was consistently below the historical baseline.
Significant change (8 points below the mean) was seen in the 9 sites with high maintenance-bundle compliance (Fig 2B). There was also improvement in the sites with lower maintenance-bundle compliance (Fig 2C), although this improvement occurred later in the intervention period and was of a smaller magnitude. When we examined the reduction in the proportion of infants with infections related to bacterial pathogens other than CONS versus infections related to CONS, it seems that there were greater reductions in CONS infections (Fig 3).
The OPQC has extended the findings of other investigators by showing that a state-based, improvement collaborative that includes all Ohio level 3 NICUs can be used to reduce NICU-associated infections. This finding confirms conclusions drawn from similar efforts in adult and PICUs.5,6 It is also consistent with findings from improvement efforts that focused on the application of evidence-based catheter-care principles and infection reduction in preterm infants.9,15,–,17 Thirteen California NICUs collaboratively demonstrated a 25% reduction in catheter-associated infection rates from 4.3 to 3.2 per 1000 line days.9 Similarly, 6 VON NICUs collaboratively reduced the proportion of infants with nosocomial infections from 26.3% to 20.9% and the rate of CONS infections from 22% to 16.6%.17 The OPQC achieved a similar 20% reduction in the overall incidence of infection, likely driven by reductions in infections caused by CONS.
The OPQC effort provides support for the important role of reliability principles in improving the application of evidence in practice.18 The initial theory driving OPQC interventions was that to reduce infections, evidence-based catheter care would need to be applied consistently in >90% of care opportunities. Although a cutoff of 90% still means that there is a 1 in 10 chance that suboptimal care will be provided, the achievement of 90% reliability indicates that a specific common process exists for the application of evidence in practice.18 Subgroup analysis in which sites with compliance of ≥90% with the maintenance bundle components were compared to those with compliance of <90% supports this theory in that it shows greater improvement among the NICUs with higher compliance. NICUs that achieved high reliability moved beyond educational strategies and focused on changes such as the institution of specific protocols to standardize the timing of catheter removal and the addition of questions about catheter necessity to templates in the medical record.
Another unique contribution was the attention paid to the reduction of both catheter-associated and non–catheter-associated infections. Although the intervention focused initially on the implementation of evidence-based catheter care, the participating NICUs had a high degree of belief that a comprehensive approach to infection was necessary. The adoption of the proportion of infants with at least 1 bacterial infection (catheter associated or non–catheter associated) as the primary outcome measure, although perhaps a less sensitive measure of catheter-associated infection, allows the OPQC to continue to test subsequent interventions related to other portals of entry for invasive infections, including the skin, respiratory tract, and gastrointestinal tract. A similar approach may be useful to other QI collaborative groups that have successfully reduced catheter-associated infections and are now poised to tackle other key processes unrelated to catheter care.
Our study design did not include a contemporaneous control group. Thus alternative explanations for the change in infection rates cannot be excluded. At the start of the OPQC intervention, participating NICUs had an aggregate nosocomial infection rate lower than that reported for the entire VON network. This lower baseline rate may indicate that many of the OPQC NICUs were already actively working on infection reduction. However, additional reductions were seen during the OPQC intervention. Infections among comparable infants discharged from hospitals participating in the VON network have declined minimally over a similar time period. Unpublished data from the VON Nightingale Web site indicates that the incidence of late-onset nosocomial infection decreased from 27.3% to 24.7% from 2006 to 2008.
We chose to use the VON measure of late-onset nosocomial infection as the primary outcome measure because participating NICUs had processes in place to collect these data and considerable baseline data were available. Some collaborative groups have used measures defined by the CDC National Health Care Safety Network to monitor changes in infection rates.6,9 The OPQC/VON definition focuses on bloodstream and CSF infections regardless of the source, whereas the CDC definition allows for exclusion of infections in which the organism may have been related to infection at another site and therefore tends to identify infections that can be more directly attributed to the presence of an indwelling catheter. In addition, the CDC definition requires isolation of bacteria from 2 blood cultures along with generalized signs of illness to classify an infection as being related to organisms that are generally considered skin contaminants. According to the OPQC/VON definition, an infection is related to a skin contaminant when it is associated with a single positive culture, generalized symptoms of illness, and treatment with antibiotics for ≥5 days. We believe that the CDC definition captures a subset of all NICU-associated infections; however, direct comparisons of results obtained by use of these 2 definitions have not been performed. Among transferred infants, before January 2009, VON data did not differentiate between infections that occurred at the transferring hospital and those that occurred subsequent to admission at the accepting hospital. Although this lack of differentiation may have had a significant impact on the rates of infection calculated for individual hospitals, particularly for those hospitals with mainly outborn infants, in aggregate this effect was unlikely to have led to variation in results calculated for the baseline and intervention periods. OPQC used various methods to promote data quality including using established data sources (eg, VON registry data) and building data quality checks into the Internet-based data collection system. Although we did not conduct site audits, we believe our other data quality processes and efforts to create a culture where sharing results (even negative ones) and learning from data were the norm, serve to reduce the likelihood that sites were systematically under-reporting infections.
The magnitude of the reduction experienced by the OPQC was less than the hypothesized reduction. We believed that evidence-based catheter care must be applied in ≥90% of instances to achieve significant improvements in outcomes. However, by the end of the intervention period, maintenance-bundle compliance had reached only 80%. It is possible that NICUs must achieve higher reliability before more significant reductions in infection can be seen. In addition, because NICUs that participated in the OPQC started with a lower infection rate than that seen in previous collaborative group efforts17, and only 69% of infections were reported to be catheter associated, the magnitude of the effect attributable to improved catheter care may have been smaller than initially hypothesized.
The use of collaborative QI methods that focus primarily on the implementation of evidence-based catheter care can lead to significant reductions in late-onset infections in infants born at 22 to 29 weeks' gestation across an entire state. Future work should continue to focus on application of reliability principles to improve compliance with evidence-based care. Attention to other care practices unrelated to catheters may be needed to effect larger decreases in infections. Future research should explore the impact of evidence-based nutrition (eg, human milk) and skin care practices applied to further reduce the incidence of infection.
This work was supported in part by grant 1U0CMS030227/01 from the Center for Medicare and Medicaid Services administered by the Ohio Department of Job and Family Services.
OPQC participating hospitals and key improvement team members included Akron Children's Hospital, Akron: Kim Firestone, Anand Kantak, and Judy Ohlinger; St Elizabeth Health Center, Youngstown: Linda Beilstein, Carrie Cannon, Patricia Hray, Diane L. Pitts, and Elena Rossi; Aultman Hospital, Canton: Corena Albert, Brenda Douglass, Fran Kessler, and Jamie Mosnot; Cincinnati Children's Hospital Medical Center, Cincinnati: Pattie Bondurant, Claire Burkhart, Cathy Grisby, Beth Haberman, and Debbie Hershberger; Cleveland Clinic, Cleveland: John Baker, Carol Bennett, Marita DiNetto, Rita Eakins, Greg Gagliano, and Amy Toth; Dayton Children's Medical Center, Dayton: Karen Beekman, Lisa Jasin, Alicia Link, Jennifer Morris, and Jerod Rone; Fairview Hospital, Cleveland: Laura Bobek, Louana Dickey, Patricia Kaser, Jeffrey Pietz, and Denise Speer; Good Samaritan Hospital, Cincinnati: Juanita Dudley, Laura Harris, Amy Nathan, Cheri Potts, Kurt Schibler, and Janet Sherrod; Hillcrest Hospital, Mayfield: Sue Levar, Jeffrey Schwersenski, Susan Shirey, and Christine Walton; MetroHealth Medical Center, Cleveland: Marc Collin, Monica Fundzak, and Maroun Mhanna; Miami Valley Hospital, Dayton: Marc Belcastro, Sue Mackey, and Tracy Morrison; Mount Carmel East Hospital, Columbus: Ehab Ahmed, Marcia Garrett, Debbie LaJeunesse, Theresa Lombardo, Jennifer Notestine, and Kathy Sturges; Mount Carmel St Ann's Hospital, Westerville: Jill Beverly, Sandy Conte, Martha Meyers, Randy Miller, Ann Peeples, and Gary Snyder; Mount Carmel West Hospital, Columbus: Marcia Garrett, Barry Halpern, Mickey Johnson, and Laura Shade; Nationwide Children's Hospital, Columbus: Gail Bagwell, Al Gest, John Hitchner, Tami Kelly, Jodi Lowe, Renee Miller, Joanna Sutton, and Rick Taylor; Doctor's Hospital, Columbus: Dan Malleske and Stephanie Stafford; Grant Hospital, Columbus: Margaret Holston, Brandon Kuehne, and Apurwa Naik; Riverside Hospital, Columbus: Carol Jaeger, Kari Kennedy, and Pat Wall; St Vincent Mercy Medical Center, Toledo: Moustafa M. Aouthmany, Jennifer Roe, Paula Samples, and Joan Zolla Bold; Summa Health Systems, Akron: Theresa Flohr, Karen Frantz, Jennifer Grow, and Debbie Seiber; Ohio State University Medical Center, Columbus: Shelly Biggs, Leandro Cordero, Cynthia Jenkins, Michael Popa, Michele Sweet, and David Taylor; Toledo Children's Hospital, Toledo: Barbara Chappell, Debbie Fritz, Vicky Gall, Judy Gresky, Mary Moore, Joan Ruff, and Howard Stein; University Hospital, Cincinnati: Linda Croop, Vivek Narendran, and Emily Rosenberg; University Hospital Case Medical Center and Rainbow Babies & Children, Cleveland: Beverly Capper, Kathleen Deakins, Jonathan Fanaroff, Kathleen Haas, Elie Abu Jawdeh, Tina Lewis, Ann Reitenbach, Amy Seekely, and Michele Walsh; OPQC Executive Committee: Mary Applegate, Gail Bagwell, Jennifer Bailit, Marc Belcastro, Jo Bouchard, Barbara Chappell, Ronda Christopher, Lori Deacon, Ed Donovan, Kelly Friar, Al Gest, Pat Heinrich, Karen Hughes, Jay Iams, Anand Kantak, Heather Kaplan, Karen Keller, Carole Lannon, Michael Marcotte, Rick McClead, Dave McKenna, Brian Mercer, Barbara Rose, Craig Strafford, Mary Ann Swank, and Michele Walsh; for the Ohio Department of Health: Jo Bouchard, Lori Deacon, Kelly Friar, Karen Hughes, Mark Kassouf, John Paulson, and Bev Wargo; for the Ohio Department of Job and Family Services: Mary Applegate, Karen Keller, Debbie Clement Saxe, and Michael Wiggins; for the VON: Joseph Carpenter, Nancy Cloutier, Jeffrey Horbar, Ted Krieder, Kathy Leahy, A. Lynn Stillman, and Pete Warner; project directors and staff, Ohio Department of Health Regional Perinatal Center Program Grants, Region I, Cincinnati: Kathy Hill; Region II, Dayton: Mary Ann Swank; Region III, Toledo: Debbie Fritz; Region IV, Columbus: Corey F. Ferguson; Region V, Cleveland: Marilyn Benjamin; Region VI, Akron: Judy Orosz and Connie Teal; OPQC Central Administration: Harry Atherton, John Besl, Ronda Christopher, Diana McClendon, Barbara Rose, Tim Salvage, Sang Sam, Kenneth Matthew Short, and Mariea Taylor.
- Accepted November 19, 2010.
- Address correspondence to Heather C. Kaplan, MD, MSCE, Cincinnati Children's Hospital Medical Center, 3333 Burnet Ave, MLC 7009, Cincinnati, OH 45229. E-mail: .
Preliminary results of this study were presented as a platform at the Pediatric Academic Societies meeting; May 3, 2010; Vancouver, British Columbia, Canada.
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
- QI =
- quality improvement •
- IRB =
- institutional review board •
- OPQC =
- Ohio Perinatal Quality Collaborative •
- VON =
- Vermont Oxford Network •
- CDC =
- Centers for Disease Control and Prevention •
- CSF =
- cerebrospinal fluid •
- CONS =
- coagulase-negative Staphylococcus •
- SPC =
- statistical process control
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LIVING LONGER: The other night, we had my parents over for dinner. After they left, a friend of mine remarked, “Your parents don't make getting old look easy.” My father, whose mind is razor sharp, has had a heart attack and because of joint problems and being overweight, can sometimes hardly walk. He has, however, lived longer than any other member of his family. My mother, whose cognitive function is not as sharp, carries with her at all times a remarkably large pill box for her various chronic medical conditions and can hardly use her hands because of arthritis. A day that does not involve a physician or therapist visit for one of them is considered a great day and seen as a rare event. As reported in The New York Times (December 27, 2010: Health) Americans, like my parents, are indeed living longer than ever, but the added years are more likely to include living with conditions such as heart disease, stroke, cancer, diabetes and significant physical disability. According to the article, researchers combing published US morbidity and mortality data from the last decade and a half concluded that people live longer not because they are less likely to get sick, but because they survive longer with disease. Their data suggest that 20-year-old men today can expect to live about a year longer than men who were 20-years-old in 1998. However, today's 20-year-old men will spend approximately one more year with disease and two years without full mobility. While I am thrilled that I still get to see my parents, and hope I can continue to have dinners with them for many more years to come, I can't help but be reminded a tiny bit of Tithonus, the lover of Eos, whom Zeus granted immortality but not eternal youth. So, when I have dinner with my own 20-year-old son, I counsel him that asking for immortality has always been a bad request. Putting practices that improve and ensure better long term health into place at an early age seems to be the way to go.
Noted by WVR, MD
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