Decreased incidence of peritoneal dialysis-associated peritonitis in young children

doi:10.21203/rs.3.rs-3222827/v1

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Decreased incidence of peritoneal dialysis-associated peritonitis in young children

https://doi.org/10.21203/rs.3.rs-3222827/v1

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Background

Peritonitis is the most common complication of peritoneal dialysis (PD). This study aimed to investigate changes in the incidence, risk factors, microbiology, and clinical outcomes of PD-associated peritonitis in the past decades.

Methods

This was a retrospective study that included children who initiated chronic PD at Seoul National University Children’s Hospital between 2000 and 2017. The patients were divided into two groups according to the year of initiation: those who initiated PD between 2000 and 2008 and those who initiated PD between 2009 and 2017. The follow-up data until PD cessation, death, or June 30, 2023, were reviewed. The incidence and characteristics of peritonitis were compared between the groups.

Results

A total of 184 patients (107 males and 77 females) with a median age of 10.2 years were included in this study. Of the patients, 92 experienced 210 episodes of peritonitis. Automated PD was the dominant PD modality in the later period. The incidence rate of peritonitis decreased from 0.35 to 0.21 episodes/patient year during the study period (P = 0.001). No changes were observed in the distribution of causative organisms. Subgroup analysis showed an increase in the 2-year peritonitis-free rate from 26.9–93.3% in children under 2 years of age. No significant difference in the 2-year peritonitis-free rate was observed among different age groups since 2009.

Conclusions

The incidence of PD-associated peritonitis decreased, particularly in children under 2 years of age. Thus, younger age is no longer a risk factor for PD-associated peritonitis.

Peritonitis

Incidence

Retrospective study

Peritoneal dialysis

Peritoneal dialysis (PD) is a preferred dialysis modality of kidney replacement therapy for children with kidney failure (KF) due to its ease of implementation and better preservation of residual kidney function [1, 2]. Although PD has several benefits, it is associated with various complications. PD-related peritonitis is the most common complication observed in children receiving PD, occurring more frequently in children than in adults [3–5]. In 2007, the International Pediatric Peritonitis Registry reported 548 episodes of PD-related peritonitis in 392 children from 44 centers, whereas in 2011, the North American Pediatric Renal Transplant Cooperative Study (NAPRTCS) reported a peritonitis rate of 0.64 episodes/patient year [4, 6]. Recent studies have reported a relatively lower peritonitis rate, as low as 0.23 episodes/patient year. However, peritonitis remains the most significant complication for children receiving chronic PD [7]. In South Korea, many studies have examined the incidence and outcomes of PD-associated peritonitis and reported peritonitis incidence rates of 0.28–0.43 episodes/patient year in 57–110 children before 2012 [8–10].

As PD-associated peritonitis remains a major cause of morbidity in children receiving PD, efforts have been made to lower its incidence, including the development of adequate prevention and treatment guidelines. In 2022, the International Society of PD developed consensus guidelines [11]. The guidelines recommend periodic reevaluation of peritonitis characteristics. However, few long-term studies have been conducted to investigate changes in peritonitis characteristics, despite the frequently reported cross-sectional studies on peritonitis incidence [4, 12–14]. In North America, the NAPRTCS evaluated changes in peritonitis occurrence over time and demonstrated a decline in the incidence rates of peritonitis from 0.79 episodes/patient year in the 1992–1996 period to 0.44 episodes/patient year in the 2007–2010 period [6]. In the United States, the Standardizing Care to Improve Outcomes in Pediatric End-Stage Kidney Disease Collaborative, focusing on implementing care bundles of catheter insertion, training, and follow-up, reported a decrease in annualized monthly peritonitis rates from 0.63 to 0.42 after the implementation of the care bundle in 2011 [15, 16]. However, no long-term studies have been conducted in different regions or centers, and this may be due to the inadequate number of cases available for analysis.

This study aimed to evaluate the incidence, risk factors, microbiology, clinical outcomes, and trends of peritonitis over time in Korean children. Considering that our institution is the largest children’s dialysis center in South Korea, with about 10 children initiating PD annually, we anticipate that this study would provide informative results in terms of sequential changes in peritonitis characteristics.

Study design, data collection, and definitions

This was a retrospective study reviewing the electronic medical records of children who initiated chronic PD between January 1, 2000, and December 31, 2017, at Seoul National University Hospital, Seoul, South Korea. The inclusion criteria included patients who were under the age of 18 years at the initiation of PD and who received PD for a minimum duration of 3 months. If the children underwent more than two courses of PD involving other kidney replacement therapy modalities, such as kidney transplantation or hemodialysis, for a period exceeding 2 months between PD courses, only the first PD course was evaluated. The children were followed-up until the cessation of PD, death, or June 30, 2023, whichever came first. This study was approved by the Institutional Review Board of Seoul National University Hospital (IRB No. H-1808-137-967).

Data were collected, including age, sex, cause of KF (glomerulonephritis, congenital anomalies of the kidney and urinary tract, and other specified or unspecified causes), year of PD initiation, dominant PD modality (continuous ambulatory PD or automated PD [APD]), PD duration, and information about catheter insertion surgery, such as catheter type (straight or coiled), usage of laparoscopy, and concomitant omentectomy. In addition, peritoneal fluid analysis data were collected, including cell count and culture results, peritonitis symptoms, and outcomes such as catheter removal.

According to the 2022 International Society of Peritoneal Dialysis guidelines [11], PD-related peritonitis was defined as the presence of two of the following three criteria: (1) abdominal pain and/or cloudy dialysis effluent, (2) peritoneal fluid containing 100 or more white blood cells per mm³ with at least 50% polymorphonuclear cells, and (3) positive culture results of dialysis effluent. Relapsing peritonitis was defined as an episode of peritonitis with the same organism or a sterile episode within 4 weeks post the completion of antibiotic treatment. Recurrent peritonitis was defined as an episode of peritonitis with a different organism within 4 weeks after the completion of antibiotic treatment. Each episode was considered separately in patients experiencing multiple episodes of peritonitis, except for relapsing peritonitis.

Outcomes and statistical analysis

The incidence of peritonitis was calculated as episodes/patient year and stratified by age (subdivided by 0–1 year, 2–5 years, 6–12 years, and more than 13 years), cause of KF, year of PD initiation, and dominant PD modality. The year of PD initiation was divided into two periods: 2000–2008 and 2009–2017. All peritonitis episodes were analyzed to determine microbiological findings (gram-positive, gram-negative, fungal, coinfection with gram-positive and gram-negative organisms, and culture-negative results) and complications, such as relapsing peritonitis, recurrent peritonitis, and catheter removal.

Continuous variables were presented as median with interquartile range (IQR), and categorical variables were expressed as frequencies and percentages. The characteristics of patient demographics and peritonitis were compared using the Chi-squared or Mann–Whitney U tests as appropriate. Sequential changes in peritonitis-free survival were assessed using the Kaplan–Meier survival analysis according to the age group and year of PD initiation. In addition, the risk factors for the peritonitis-free survival period were analyzed using a multivariate Cox proportional hazard model. Statistical analysis was performed using R-project version 4.2.1. A P value of < 0.05 was considered statistically significant.

Patient characteristics and sequential changes

A total of 191 patients initiated PD during the study period at our institution. Among them, 184 patients (107 males and 77 females) who were under the age of 18 years at the initiation of PD and who received PD for more than 3 months were included in this study. The median age at the initiation of PD was 10.2 years (IQR: 4.8–13.8), and the median duration of receiving PD was 40.9 months (IQR: 23.5–63.3). Table 1 shows the sequential changes in patient characteristics. The proportion of patients using APD significantly increased from 53.6% in the 2000–2008 period to 86.2% in the 2009–2017 period. No patients underwent laparoscopic PD catheter insertion in the 2000–2008 period. However, it was the predominant modality in the 2009–2017 period (80.5%).

Table 1

Baseline characteristics of the patients
Characteristics	2000–2008 (n = 97)	2009–2017 (n = 87)	P value	All patients (n = 184)
Male sex	54 (55.7)	53 (60.9)	0.568	107 (58.2)
Age, years	9.5 (5.5–13.1)	10.6 (3.0–14.3)	0.603	10.2 (4.8–13.8)
Age group			0.086
0–1 years	13 (13.4)	15 (17.2)		28 (15.2)
2–5 years	15 (15.5)	15 (17.2)		30 (16.3)
6–12 years	44 (45.4)	24 (27.6)		68 (37.0)
More than 13 years	25 (25.8)	33 (37.9)		58 (31.5)
Duration of PD, months	44.1 (25.1–64.3)	37.7 (19.6–59.5)	0.214	40.9 (23.5–63.3)
Cause of KF			0.156
CAKUT	20 (20.6)	20 (23.0)		40 (21.7)
Glomerulonephritis	46 (47.4)	50 (57.5)		96 (52.2)
Others	31 (32.0)	17 (19.5)		48 (26.1)
Automated PD	52 (53.6)	75 (86.2)	< 0.001	127 (69.0)
Coiled PD catheter (n = 185)¹	16 (16.5)	23 (26.7)	0.131	39 (21.3)
Laparoscopic catheter insertion (n = 185)¹	0 (0.0)	66 (80.5)	< 0.001	66 (40.5)
Concomitant omentectomy at the time of catheter insertion (n = 164)¹	43 (53.8)	57 (69.5)	0.057	100 (61.7)
Peritonitis occurred	58 (59.8)	34 (39.1)	0.008	92 (50.0)
Abbreviations: PD, peritoneal dialysis; KF, kidney failure; CAKUT, congenital anomalies in kidney and urinary tract
Values are presented as numbers (%) or median (interquartile range).
¹Types of PD catheter, usage of laparoscopy, and concomitant omentectomy were unavailable in some patients due to the lack of operation record

Incidence of peritonitis

Of the 184 patients, 92 experienced 210 episodes of peritonitis. The overall incidence rate was 0.28 episodes/patient year (95% confidence interval, 0.25–0.33), and the median time from the initiation of PD to the first peritonitis episode was 9.9 months (IQR: 3.5–24.7 months). The incidence rate of peritonitis decreased from 0.35 episodes/patient year in the 2000–2008 period to 0.21 episodes/patient year in the 2009–2017 period (P = 0.001). When stratified by age, the incidence rate of peritonitis was the lowest in patients 2–5 years of age (0.19 episodes/patient year) and the highest in patients 0–1 year of age (0.39 episodes/patient year). In addition, no significant difference in the incidence rate was observed between the two dominant PD modalities (Table 2).

Table 2

Incidence of peritonitis
	No. of episodes	Total duration of PD (months)	Incidence (95% CI)
All patients	211	739	0.29 (0.25–0.33)
Age
0–1 years	37	96	0.39 (0.28–0.54)
2–5 years	14	73	0.19 (0.11–0.33)
6–12 years	64	238	0.27 (0.21–0.34)
More than 13 years	96	332	0.29 (0.24–0.35)
Cause of KF
CAKUT	47	167	0.28 (0.21–0.38)
Glomerulonephritis	114	406	0.28 (0.23–0.34)
Others	50	166	0.3 (0.23–0.4)
Year of initiation
2000–2008	141	398	0.35 (0.3–0.42)
2009–2017	70	341	0.21 (0.16–0.26)
Dominant PD modality
CAPD	70	238	0.29 (0.23–0.37)
APD	141	501	0.28 (0.24–0.33)
Abbreviations: KF, kidney failure; CAKUT, congenital anomalies in kidney and urinary tract; PD, peritoneal dialysis; APD, automated PD; CAPD, continuous ambulatory PD; CI, confidence interval

Peritonitis-free survival

The overall peritonitis-free survival rates were 82.0% at 6 months, 70.8% at 1 year, and 60.5% at 2 years (Table 3). Figure 1 shows Kaplan–Meier curves stratified by age and year of PD initiation. The peritonitis-free survival rate significantly differed based on the year of PD initiation (P = 0.020). However, no significant difference was observed among the age groups (P = 0.381). Subgroup analysis was performed, and Kaplan–Meier curves stratified by age for patients who initiated PD in the 2000–2008 and 2009–2017 periods were presented (Table 3 and Fig. 2). Interestingly, patients under 2 years of age at the initiation of PD showed the most drastic change in the peritonitis-free survival rate over time. The 2-year peritonitis-free survival rates for patients 0–1 years of age were 26.9% in the 2000–2008 period and 93.3% in the 2009–2017 period. In the 2000–2008 period, the 2-year peritonitis-free survival rate was significantly lower for patients 0–1 years of age than for other age groups (P = 0.004). In the 2009–2017 period, the 2-year peritonitis-free survival rate for patients 0–1 years of age was higher than for other age groups. However, no statistically significant difference was observed. The multivariable Cox proportional hazard model showed that patients under 2 years of age had a significantly higher risk of developing peritonitis than the adolescent group in the 2000–2007 period. However, this was not evident in the 2008–2017 period (Supplementary Table 1).

Table 3

The 6-month, 1-year, and 2-year peritonitis-free survival stratified by year of initiation and age at the initiation of peritoneal dialysis
	6-month peritonitis-free survival (%)	1-year peritonitis-free survival (%)	2-year peritonitis-free survival (%)
Overall	82.0	70.8	60.5
2000–2008	80.3	68.7	56.1
0–1 years	53.8	53.8	26.9
2–5 years	80.0	80.0	80.0
6–12 years	88.6	69.7	61.5
More than 13 years	80.0	68.0	51.7
2009–2017	83.8	73.1	65.5
0–1 years	93.3	93.3	93.3
2–5 years	86.7	66.7	57.1
6–12 years	87.5	82.9	82.9
More than 13 years	75.8	60.6	47.8

Peritonitis characteristics

Table 4 shows the characteristics of peritonitis episodes. Of the 211 episodes of peritonitis, 109 episodes (51.7%) were caused by gram-positive organisms (51.7%), whereas 21 (10.0%) were classified as sterile episodes. No change in the proportion of gram-positive and -negative organisms as causative pathogens was observed throughout the study period. Methicillin-resistant organisms were found in 30% (6 out of 20) of S. aureus episodes and 49% (22 out of 45) of coagulase-negative Staphylococcus episodes. Relapsing peritonitis occurred in 26 episodes (12.3%), and recurrent peritonitis occurred in 16 episodes (7.6%). Catheter removal was necessary for 20 (9.5%) patients due to fungal peritonitis (n = 6), relapsing peritonitis (n = 6), refractory peritonitis (n = 6), and exit site infection (n = 1). No significant differences in the complications were observed between the two periods.

Table 4

Peritonitis characteristics according to the year of PD catheter insertion
	2000–2008 (n = 141)	2009–2017 (n = 70)	P value	Overall (n = 211)
Culture result			0.171
Fungus	6 (4.3)	0 (0.0)		6 (2.8)
Gram negative	50 (35.5)	25 (35.7)		75 (35.5)
Gram positive	74 (52.5)	35 (50.0)		109 (51.7)
Sterile	11 (7.8)	10 (14.3)		21 (10.0)
Complications
Recurrent peritonitis	13 (9.2)	3 (4.3)	0.318	16 (7.6)
Relapsing peritonitis	17 (12.1)	9 (12.9)	> 0.999	26 (12.3)
Catheter removal	13 (9.2)	7 (10.0)	> 0.999	20 (9.5)
Age at the time of peritonitis			0.001
0–1 years	14 (9.9)	1 (1.4)		15 (7.1)
2–5 years	25 (17.7)	11 (15.7)		36 (17.1)
6–12 years	29 (20.6)	4 (5.7)		33 (15.6)
More than 13 years	73 (51.8)	54 (77.1)		127 (60.2)
Abbreviations: PD, peritoneal dialysis
Values are presented as numbers (%).

This study showed that the incidence of peritonitis declined gradually in recent years. Interestingly, this decline was most significant in young children under 2 years of age. Contrary to previous studies, this finding suggests that younger age may not be associated with a higher risk of infectious complications in pediatric patients on PD. Several previous studies have also shown a steady decline in the incidence of peritonitis in children over the past several decades. This decline may be attributed to improved adherence to quality improvement strategies [11]. Auron et al. reported a decline in the incidence rate of peritonitis from 0.56 episodes/patient year in 1997–2000 to 0.19 episodes/patient year in 2001–2004 in the United States with the application of an adequate combination of prophylactic measures [3]. In addition, the NAPRTCS, which included 3,363 children on PD from 1992 to 2010, reported a gradual decline in the incidence of peritonitis [6]. More recently, the Standardizing Care to Improve Outcomes in Pediatric End-Stage Kidney Disease Collaborative reported a significant decline in the incidence of peritonitis by implementing standardized care [15]. Furthermore, researchers in Turkey have reported a reduction in the peritonitis rate among children from 0.13 episodes/patient year during the 1998–2008 period to 0.09 episodes/patient year during the 2009–2018 period [17]. To the best of our knowledge, this is the first study to present comprehensive findings regarding the decline in the trends of peritonitis incidence in East Asia.

The cause of improvement in peritonitis over time may be multifactorial. The enhancement of training and follow-up practices may be one of the most important factors. However, this study could not include measurable values in standardized care, such as the compliance rate. In addition, the widespread use of APD in recent years may have contributed to this improvement. In Korea, the use of APD has dramatically increased since the Korean Ministry of Health and Welfare provided insurance benefits to patients with KF in 2008. Although a consensus has not been reached on this matter, many international and Korean studies favor APD over continuous ambulatory PD in terms of peritonitis [6, 8]. However, this study did not find a significant difference in the peritonitis-free survival rates between the two modalities. Moreover, laparoscopic catheter insertion or omentectomy has recently become more common. Previous studies on adult patients have shown no significant difference in peritonitis rates between laparoscopy and laparotomy [18, 19]. However, laparoscopy may be beneficial for children due to the smaller surgical incisions. Nevertheless, no studies have compared surgical methods and their impact on peritonitis outcomes in pediatric patients receiving PD.

This study showed a novel finding that children under 2 years of age showed a significant decline in the rate of peritonitis compared with adolescents. This finding is inconsistent with the findings of previous studies that showed an inverse relationship between age and the rate of peritonitis in children [4, 7]. Moreover, during the 2009–2017 period, patients under 2 years of age showed the highest rate of peritonitis-free survival. Extensive caregiver education may be beneficial for younger children, as patients 0–1 years of age have limited interactions with people other than their primary caregivers at school or daycare centers. In addition, APD may have a more apparent positive impact on younger children due to fewer connections and favorable outcomes of performing flush procedures [20]. Laparoscopic surgery with small surgical incisions might also offer advantages for younger children [21]. However, establishing conclusive evidence is challenging because no prior studies have assessed changes in the trend of peritonitis with respect to age groups. Compared with younger children, adolescents have demonstrated the lowest rate of peritonitis-free survival in recent years. Furthermore, adolescents’ poor adherence may result in elevated morbidity rates and an increased risk of complications. This resembles the common nonadherence observed in adolescents with kidney transplants [22].

Many previous studies have evaluated peritonitis-free survival rates in children in recent years. Bordador et al. analyzed the data of 167 children and reported a 2-year peritonitis-free survival rate of 36%, whereas Ponce et al. investigated 491 Brazilian children and reported a 2-year survival rate of 58.9% [12, 13]. The findings of Ponce et al.’s study are similar to those observed in our study. The most recent annual report of the NAPRTCS revealed an overall peritonitis-free survival rate of 49% at 2 years [6]. However, no direct comparisons were made with similar regions because no similar studies have conducted survival analysis in Eastern Asia. The incidence rates of PD-associated peritonitis in children vary from region to region [23]. The incidence rate of PD-associated peritonitis in Eastern Asia has been reported to be lower than that in other regions, with a rate as low as 0.19 episodes/patient year, as reported from Japan [24]. Nevertheless, peritonitis remains the most common complication and the primary cause of PD failure. Thus, it is important to collect regional epidemiological data to better plan for treatment and prevention options for peritonitis [7, 25].

Furthermore, in contrast to the results observed in North America, gram-positive bacteria, such as Staphylococcus, were found to be the most prevalent in South Korea, and this pattern remained consistent regardless of the period of PD initiation [6]. Furthermore, the sensitivity to methicillin of Staphylococcus has not changed significantly since the early 2000s, which is consistent with previous studies conducted in Eastern Asia [8, 25, 26].

This study has a limitation. This was a single-center retrospective medical chart review study. Thus, it was difficult to collect important data, including patient adherence, risk factors such as ostomy presence, in-depth details about peritonitis, such as specific antibiotic dosage, and the status of exit site care. These missing data might affect our overall understanding of peritonitis cases. Nevertheless, this study has important strengths as we collected data over a long period and showed changes in peritonitis characteristics, which were scarcely reported in children.

In conclusion, the incidence of peritonitis significantly decreased, mainly in young children, whereas the incidence has not changed significantly in adolescents. Further large-scale studies investigating peritonitis characteristics, including the incidence rate in relation to patients’ ages, microbiology, and outcomes, are needed to establish adequate center- and region-based guidelines for proper treatment and prevention of peritonitis.

Funding: No funds, grants, or other support was received.

Competing interests: All authors declare that they do not have competing interests.

Ethics approval: This study was approved by the Institutional Review Board of Seoul National University Hospital.

Consent to participate: Informed consent was waived due to the retrospective nature of this study.

Consent for publication: Not applicable.

Data availability: The datasets analyzed during the current study are available from the corresponding author upon reasonable request.

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Peong Gang Park and Yo Han Ahn. The first draft of the manuscript was written by Peong Gang Park and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Code availability: Not applicable.

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Decreased incidence of peritoneal dialysis-associated peritonitis in young children

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Abstract

Background

Methods

Results

Conclusions

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Introduction

Methods

Study design, data collection, and definitions

Outcomes and statistical analysis

Results

Patient characteristics and sequential changes

Incidence of peritonitis

Peritonitis-free survival

Peritonitis characteristics

Discussion

Declarations

References

Supplementary Files

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