Abstract
Background and objectives The Standardizing Care to Improve Outcomes in Pediatric ESRD Collaborative is a quality improvement initiative that aims to reduce peritoneal dialysis–associated infections in pediatric patients on chronic peritoneal dialysis. Our objectives were to determine whether provider compliance with peritoneal dialysis catheter care bundles was associated with lower risk for infection at the individual patient level and describe the epidemiology, risk factors, and outcomes for peritonitis in the Standardizing Care to Improve Outcomes in Pediatric ESRD Collaborative.
Design, setting, participants, & measurements We collected peritoneal dialysis characteristics, causative organisms, compliance with care bundles, and outcomes in children with peritonitis between October of 2011 and September of 2014. Chi-squared tests, t tests, and generalized linear mixed models were used to assess risk factors for peritonitis.
Results Of 734 children enrolled (54% boys; median age =9 years old; interquartile range, 1–15) from 29 centers, 391 peritonitis episodes occurred among 245 individuals over 10,130 catheter-months. The aggregate annualized peritonitis rate was 0.46 episodes per patient-year. Rates were highest among children ≤2 years old (0.62 episodes per patient-year). Gram-positive peritonitis predominated (37.8%) followed by culture-negative (24.7%), gram-negative (19.5%), and polymicrobial (10.3%) infections; fungal only peritonitis accounted for 7.7% of episodes. Compliance with the follow-up bundle was associated with a lower rate of peritonitis (rate ratio, 0.49; 95% confidence interval, 0.30 to 0.80) in the multivariable model. Upward orientation of the catheter exit site (rate ratio, 4.2; 95% confidence interval, 1.49 to 11.89) and touch contamination (rate ratio, 2.22; 95% confidence interval, 1.44 to 3.34) were also associated with a higher risk of peritonitis. Infection outcomes included resolution with antimicrobial treatment alone in 76.6%, permanent catheter removal in 12.2%, and catheter removal with return to peritoneal dialysis in 6% of episodes.
Conclusions Lower compliance with standardized practices for follow-up peritoneal dialysis catheter care in the Standardizing Care to Improve Outcomes in Pediatric ESRD Collaborative was associated with higher risk of peritonitis. Quality improvement and prevention strategies have the potential to reduce peritoneal dialysis–associated peritonitis.
- peritoneal dialysis
- children
- peritonitis
- catheter-related infections
- Follow-Up Studies
- Humans
- Kidney Failure, Chronic
- Patient Care Bundles
- Quality Improvement
- renal dialysis
- risk factors
Introduction
Peritoneal dialysis (PD) is the dialysis modality used by 44% of children receiving chronic dialysis in the United States (1) and the primary modality used to provide dialysis to children around the globe (2–4). Peritonitis remains the most significant complication among patients on PD (5), which can result in substantial morbidity and permanent technique failure (3).
The Children’s Hospital Association’s Standardizing Care to Improve Outcomes in Pediatric ESRD (SCOPE) Collaborative is a multicenter quality transformation effort with the primary aim to minimize exit site infection and peritonitis rates among pediatric patients on chronic PD (6). Quality improvement methods are used to increase implementation of standardized practices for PD catheter care, with the goal to test whether these practices can affect infection rates (6). In its first 3 years, the SCOPE Collaborative showed a significant increase in implementation of standardized follow-up care and a significant decrease in average monthly peritonitis rates across the participating centers (7).
The analysis focused on changes in compliance with the PD catheter care bundles and infection rates over time at the collaborative and center levels. The aims of this study were to evaluate whether provider compliance with the care bundles for follow-up and training was associated with risk for infection at the patient level rather than center level. In addition, the objectives were to describe the epidemiology of peritonitis during the first 3 years of the SCOPE Collaborative, identify risk factors for peritonitis, and describe the outcomes after treatment of peritonitis.
Materials and Methods
The SCOPE Collaborative
The design of the SCOPE Collaborative has been previously described in detail (6). Briefly, quality improvement methods were used at 29 pediatric centers throughout the United States to increase implementation of three standardized PD catheter care bundles (catheter insertion bundle, patient and caregiver training bundle, and catheter/exit site follow-up care bundle). Components of the bundles were on the basis of expert opinion and published guidelines. All patients with ESRD on chronic PD cared for by the pediatric centers were eligible. Patients were enrolled at the time of catheter placement, even if chronic care had not yet been established as an outpatient (i.e., patients who started chronic PD as an inpatient and remained hospitalized). All catheters associated with patients enrolled during the study period, including prevalent catheters and new catheter insertions, were evaluated; therefore, a single patient could have contributed multiple catheters. Data on peritonitis episodes and compliance with the bundles were collected prospectively. The Declaration of Helsinki was followed, and the collaborative protocol was approved by the Institutional Review Board at each participating center. Informed consent was obtained where required by the institution’s Institutional Review Board.
Data Collection
Data pertaining to patient and catheter characteristics, causative organisms of peritonitis, provider compliance with care bundles, and peritonitis outcomes were collected between October 1, 2011 and September 30, 2014. Peritonitis was defined as PD effluent white blood cell count >100 and differential of >50% polymorphonuclear cells (8). Relapsing peritonitis, defined as recurrence of peritonitis with the same causative organism within 4 weeks of a previous peritonitis episode, was excluded from analysis (8). Treatment of peritonitis was per each center’s practice, but centers were advised to follow the International Society for Peritoneal Dialysis (ISPD) guidelines (8). Compliance with the follow-up bundle was scored for the visit before infection for patients with peritonitis and at last follow-up for those without peritonitis. Compliance with the training bundle was only scored for the initial training session associated with the initial catheter placement in incident patients. Prevalent patients, who had initial training before the start of the SCOPE Collaborative, received training on hand hygiene, exit site care, and aseptic technique at a follow-up visit. Compliance was assessed as all or none, meaning that each patient’s follow-up event or training session had to comply with all of the elements of the respective bundle to be considered compliant. The provider present at the follow-up visit/training recorded compliance with bundle elements. The components of the care bundles are outlined in Table 1. Compliance with the insertion bundle and its association with peritonitis in the first 3 postoperative months are being analyzed separately and will be published elsewhere.
The Standardizing Care to Improve Outcomes in Pediatric ESRD Collaborative peritoneal dialysis catheter care bundles
Statistical Analyses
For the purposes of statistical analysis, the unit of interest was the PD catheter. The time at risk for infection was calculated from catheter insertion for incident patients or the start of the collaborative for prevalent patients to catheter removal or last follow-up. For patients who contributed multiple catheters to the analysis, patient characteristics at the time of enrollment and clinical characteristics at the time of each catheter insertion were included in the analyses. Descriptive analyses included means, SDs, medians, interquartile ranges (IQRs), ranges of continuous variables, and distributions of categorical variables. Univariate comparisons of clinical variables between catheters with peritonitis and those without peritonitis were made using chi-squared test, t test, and Wilcoxon rank sum test as appropriate. The annualized peritonitis rate was calculated as follows: peritonitis rate = ([no. of events]/[count of patient-month]) ×12. Generalized linear mixed models assuming an underlying Poisson distribution were used to assess the association of potential risk factors and the peritonitis rate ratio (RR). Variables were first tested in crude models. Subsequently, a multivariable model was fit that included only factors for which the crude model yielded significant results. The multivariable model also included sex and a random patient within center effect to account for clustering of insertions within patients and clustering of patients within center. Generalized linear mixed models were assessed for the presence of overdispersion. Models in which the presence of overdispersion was detected were refit assuming an underlying negative binomial distribution.
All analyses were conducted using SAS, version 9.4 (SAS Institute Inc., Cary, NC). Tests with a P value <0.05 were considered statistically significant.
Results
Patient Population and Peritonitis
There were 734 children enrolled in the SCOPE Collaborative during the study period, representing 10,130 catheter-months. Among this group, 54% were boys, and 17.1% were black. The median age at enrolment into the SCOPE Collaborative was 9 years old (IQR, 1–15 years old; mean =7.9±6.6 years old; range =0–24 years old). Children <2 years old represented 32.4% of the cohort. Congenital anomalies of the kidney and urinary tract was the underlying diagnosis in 39.1% of the cohort. There were 857 PD catheters evaluated during the study period, consisting of 499 new catheter insertions and 358 prevalent catheters (from patients enrolled with a functioning catheter).
Of the 734 children enrolled with a median follow-up of 349 days (range =0–1095 days), 391 peritonitis episodes occurred among 245 individuals (33.3%), with a median of one (range =1–9) episode per patient (mean =1.4±1.1 episodes). The aggregate annualized peritonitis rate over the entire first 3 years of the collaborative was 0.46 infections per patient-year (PPY). The peritonitis rate was highest in children <2 years of age at the time of catheter insertion (0.62 infections PPY; 95% confidence interval [95% CI], 0.55 to 0.69) followed by the rates in those ≥18 years old (0.59 infections PPY; 95% CI, 0.40 to 0.87), 2–5 years old (0.50 infections PPY; 95% CI, 0.39 to 0.64), 6–12 years old (0.38 infections PPY; 95% CI, 0.32 to 0.44), and 13–17 years old (0.37 infections PPY; 95% CI, 0.32 to 0.42). Table 2 compares the demographic and clinical characteristics of children with peritonitis with those without peritonitis.
Demographic and clinical characteristics of children with and without peritonitis
Organism Distribution
Culture results were reported for 389 of 391 peritonitis episodes. Gram-positive peritonitis predominated (37.8%) followed by culture-negative infections (24.7%). Seventy-six episodes (19.5%) were attributed to gram-negative organisms, and 40 (10.3%) were polymicrobial. Fungal organisms were the sole cause of peritonitis in 30 (7.7%) episodes; however, two fungal organisms were also cultured as part of a polymicrobial infection, thus giving a total of 32 fungal infections. Staphylococcus epidermidis (11.3%) was the most common gram–positive organism identified, and Pseudomonas (7.2%) was the most common gram–negative organism identified. Figure 1 shows the distribution of peritonitis organisms.
Organisms cultured from patients with peritonitis. Gram-positive organisms were the predominant bacteria in peritonitis (n=389 cultures; missing two cultures; may have more than one pathogen per peritonitis episode). E. coli, Escherichia coli; MRSA, Methicillin-resistant Staphylococcus aureus; Staph, Staphylococcus; Staph A, Staphylococcus aureus; Staph Epi, Staphylococcus epidermidis.
Compliance with Bundle Elements
Provider compliance with the SCOPE Collaborative training and follow-up bundles at the patient level was evaluated as a risk factor for peritonitis. Among 734 individuals enrolled during the study period, there were 370 initial training sessions completed in incident patients and a total of 8985 follow-up encounters. Overall compliance with the training bundle did not significantly differ between those with peritonitis and the group without peritonitis (64.5% versus 70.3%, respectively; P=0.26). When examining the individual components of the bundle, compliance with a home visit by a registered nurse after outpatient PD therapy initiation (73.4% versus 77.6%, respectively; P=0.36) and compliance with teaching about hand washing (100.0% versus 99.6%, respectively; P=0.48) and the exit site care procedure (97.6% versus 99.2%, respectively; P=0.21) were also not significantly different between groups.
In contrast, there was significantly lower provider compliance with the follow-up bundle in the peritonitis group compared with the group without peritonitis (67.2% versus 71.0%, respectively; P<0.001). Compliance with the individual elements of review of hand washing (84.1% versus 88.8%, respectively), exit site care (86.1% versus 89.4%, respectively), and aseptic technique (82.1% versus 87.3%, respectively) was significantly lower in those patients with peritonitis compared with the no peritonitis group (all P<0.001). Compliance with exit site scoring was high in both groups (96.1% versus 96.1%, respectively; P=0.95). Compliance with administration of a repeat demonstration and concept test in the past 6 months was lower than the other individual bundle elements and was not significantly different between groups (76.2% versus 76.7%, respectively; P=0.61).
Risk Factors for Peritonitis
The patient and PD catheter characteristics associated with peritonitis were analyzed (Table 3). In univariate analysis, the peritonitis group had a significantly higher proportion of patients with a gastrostomy tube, incontinence (e.g., in diapers), and report of touch contamination in the month before infection or at last follow-up compared with the group without peritonitis. Comparison of PD catheter characteristics revealed that the peritonitis group had significantly more catheters with an upward (rather than downward or lateral) orientation of the catheter exit site and use of a plastic rather than titanium adapter at the distal end of the dialysis catheter.
Patient and peritoneal dialysis characteristics of children with and without peritonitis
Clinical and PD catheter variables that were significant in the unadjusted model to predict the peritonitis RR were entered into a multivariable model (Table 4). In the final model, compliance with the overall follow-up bundle in the month before infection or at last follow-up for those without infection was independently associated with a lower risk of peritonitis (RR, 0.49; 95% CI, 0.30 to 0.80). Additionally, a history of touch contamination in the previous month (RR, 2.22; 95% CI, 1.44 to 3.34) and upward orientation of the exit site (RR, 4.2; 95% CI, 1.49 to 11.89) were associated with a higher risk of infection.
Rate ratio models for peritonitis
Outcomes of Infection
Of the 391 peritonitis episodes (five missing data), 76.6% of infections resolved with antimicrobial treatment alone, 12.2% required permanent removal of the catheter, and 6% resulted in catheter removal with subsequent catheter replacement and reinstitution of PD (other outcomes =5.2%). Figure 2 displays the outcomes of peritonitis by organism. Fungal infections most commonly resulted in permanent catheter removal (66.7%). There were 33 episodes of relapsing peritonitis. Hospitalization was required in 59.6% of peritonitis episodes and varied by organism (gram negative =71.1%; fungal =66.7%; gram positive =62.3%; polymicrobial =57.5%; culture negative =44.7%; P<0.01). Polymicrobial infections resulted in the longest hospital stays (median =12 days; IQR, 6–30 days) followed by fungal infections (median =6 days; IQR, 6–16 days). Among the 734 participants, 32 (4.4%) patients died during the study period. The cause of death was known in 22 patients; however, data were not available on whether peritonitis was present at the time of death. One death was attributed to sepsis. No significant difference in mortality was observed between those with and without peritonitis (6.1% versus 3.5%, respectively; P=0.10).
Outcomes of peritonitis by organism.
Discussion
In this large cohort of pediatric patients receiving chronic PD, one third ultimately developed one or more episodes of peritonitis. Rates of peritonitis were highest in children <2 years of age and lowest in those 13–17 years of age. As reported in prior studies, touch contamination and upward orientation of the catheter were identified as risk factors for infection (3). At the patient level, lower provider compliance with the follow-up care bundle was associated with a higher risk of peritonitis. This novel finding suggests that improved compliance with standardized care practices during a clinic encounter could reduce the rate of catheter-associated infections.
Quality improvement practices implemented by the SCOPE Collaborative have been shown to influence the rate of peritonitis. Neu et al. (7) previously reported that there was a reduction in the monthly annualized peritonitis rate from 0.63 pre-SCOPE Collaborative to 0.42 at 36 months post-SCOPE Collaborative as center-specific compliance with the follow-up bundle increased. That analysis focused on compliance and infection over time at the collaborative and center levels. This analysis sought to build on those findings by identifying risk factors for infection, including patient level compliance with the care bundles. Our findings reveal that provider compliance with the follow-up bundle at the patient level was associated with a significantly lower risk of peritonitis. When evaluating the individual components of the bundle, compliance with the review of hand washing, exit site care, and aseptic technique was significantly associated with a lower risk for peritonitis. Exit site scoring was not associated with a lower risk of peritonitis, but compliance with this bundle element was >96% in patients with and without a history of peritonitis. Interestingly, compliance with the demonstration and concept test every 6 months was not associated with the risk for peritonitis. Compliance with this bundle element was relatively low in both groups, and it must be emphasized that, for this analysis, follow-up compliance was measured at one visit only: the visit immediately before infection in the peritonitis group and at last follow-up in the group without peritonitis. In fact, analyses at the collaborative level suggest that the significant reduction in peritonitis rates over time was associated with increased compliance with the entire follow-up bundle, including the requirement for a repeat of the demonstration and concept test every 6 months (7). It will be important to repeat these analyses with additional follow-up time to more clearly evaluate associations between compliance with this specific care bundle and peritonitis risk.
It is also interesting to note that we were not able to show an association between compliance with the training bundle and the risk for peritonitis. The relatively low numbers of training events may explain the lack of a relationship, and a stronger effect may emerge as the numbers increase. It should be noted that the overall low compliance with the training bundle was because of low compliance with the home visit, and compliance with the other components of the bundle was high in both groups. Nevertheless, it is possible that the review of key aspects of catheter care and the dialysis procedure at each follow-up visit may minimize the effect of the initial training compliance beyond the first few weeks after that training. This is supported by the association between low compliance with review of these protocols and risk for peritonitis among all patients, including prevalent patients who would have received training on these bundles during a follow-up session rather than during their initial training, which occurred before the start of the SCOPE Collaborative.
Multiple reports have established an inverse correlation between rates of peritonitis and age (3). In this cohort, the highest rates of infection were seen in the youngest patients, although age was not a risk factor for peritonitis in the multivariable model. However, we did confirm several modifiable risk factors for peritonitis, including upward orientation of the catheter and a history of touch contamination. Consensus guidelines published by the ISPD in 2012 recommended placement of catheters with downward or lateral tunnel configuration to decrease the risk of infection (8). Despite these recommendations, 30 children in this study cohort had catheters placed with an upward–directed exit site, and more than one half of these children developed an infection. These data suggest that better adherence to the existing guideline on exit site orientation has the potential to reduce the frequency of peritonitis episodes in children. Interestingly, the presence of a gastrostomy tube at catheter insertion did not increase the risk of infection (9). Additional analyses to evaluate if risk for infection is associated with the timing of placement of the gastrostomy tube relative to placement of the PD catheter are planned.
The relative distribution of gram-positive, gram-negative, and culture-negative peritonitis in this cohort was similar to that of other recent reports (10–12). Common skin flora, including S. epidermidis, other coagulase–negative staphylococci, and Staphylococcus aureus, were the most common gram–positive pathogens isolated, consistent with the importance of touch contamination as a risk factor for infection. No pathogen was able to be identified in 25% of patients with peritonitis. The ISPD guidelines recommend that the rate of culture-negative peritonitis should not exceed 20% of episodes in any single center, with a goal of <10% (8). According to data from the International Pediatric Peritonitis Registry, the culture–negative peritonitis rate reported from 13 North American centers was only 11%, although there was substantial variability worldwide (12). Additional evaluation of the relatively high rate of culture-negative peritonitis is planned, including collecting center–specific culture techniques.
Fungal peritonitis has historically accounted for <5% of all episodes in children, but it is associated with significant morbidity, including technique failure (13). The rate of fungal peritonitis in the SCOPE Collaborative was higher than rates reported in the literature (3,12,14). Potential risk factors for fungal peritonitis, including prior antibiotic use and prior bacterial peritonitis, in addition to treatment and outcome data are currently being analyzed and will be published separately.
There are several limitations of this study that should be considered. Selection bias is a possible limitation, because centers voluntarily enroll patients and enter data in the SCOPE Collaborative database. However, the substantial number of centers and patients in the collaborative makes it likely that the data obtained are reflective of the pediatric PD population in general. Additionally, although the collaborative recommends that centers follow international guidelines for diagnosis and treatment of peritonitis (8), there may be variation in treatment of peritonitis by center, which may affect outcomes and hospitalization rates. Another limitation is that there was no central adjudication of infection events; peritonitis was reported by center but in accordance with the ISPD recommendations. Lastly, because the mission of the SCOPE Collaborative is to reduce infection rates by implementing quality initiatives, the rates of peritonitis and outcomes reported here may differ from centers that are not involved in the collaborative.
In summary, this study reveals that lower provider compliance with standardized practices for follow-up PD catheter care in the SCOPE Collaborative was associated with higher risk of peritonitis. In addition, orientation of the catheter exit site and touch contamination were identified as additional risk factors for peritonitis. These data support the hypotheses that repeated review of key aspects of PD catheter care and the aseptic technique required to perform the dialysis procedure and prevention strategies, such as avoidance of an upward orientation of the PD catheter exit site and prophylactic treatment of touch contamination episodes, may have the potential to reduce PD-associated peritonitis. The results from the SCOPE Collaborative may provide direction to guide best practice development for the care of children on chronic PD.
Disclosures
B.A.W. has received research support from Baxter Healthcare.
Acknowledgment
A complete list of SCOPE collaborators given in the Supplemental Material.
Footnotes
Published online ahead of print. Publication date available at www.cjasn.org.
This article contains supplemental material online at http://cjasn.asnjournals.org/lookup/suppl/doi:10.2215/CJN.02540316/-/DCSupplemental.
- Received March 7, 2016.
- Accepted May 21, 2016.
- Copyright © 2016 by the American Society of Nephrology