Peritoneal dialysis-associated peritonitis in Scotland (19992002)
David Kavanagh,
Gordon J. Prescott and
Robert A. Mactier on behalf of the Scottish Renal Registry
The Scottish Renal Registry, Royal Infirmary, Castle Street, Glasgow G4 0SF, UK
Correspondence and offprint requests to: David Kavanagh, The Scottish Renal Registry, Royal Infirmary, Castle Street, Glasgow G4 0SF, UK. Email: David.Kavanagh{at}newcastle.ac.uk
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Abstract
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Background. Peritonitis is a major complication of peritoneal dialysis (PD). We have performed a national study of all patients on PD in Scotland over a 3.5 year period examining the causes of technique failure, rates of peritonitis, causative organisms, clinical outcomes and differences between automated peritoneal dialysis (APD) and continuous ambulatory peritoneal dialysis (CAPD).
Methods. All 10 adult renal units in Scotland participated in the study and the data include all 1205 patients who were on PD in Scotland from January 1999 to June 2002. The data were collected prospectively by the PD nurses and reported to the Scottish Renal Registry every 6 months.
Results. Refractory or recurrent peritonitis was the cause of technique failure in 167 patients (42.6% of all cases of technique failure). There were 928 cases of peritonitis in 1487 patient-years, which equates to an overall peritonitis rate of one episode every 19.2 months. The peritonitis rates for APD and CAPD were similar at one episode every 20.3 months and one episode every 18.6 months, respectively. These results include 88 cases of peritonitis due to relapse or re-infection. There was a statistically significant difference (P = 0.012) in peritonitis rates between units using nasal mupiricin (one episode every 21.9 months) and those that did not (one episode every 18.3 months). Coagulase-negative Staphylococcus was the most common cause of peritonitis (29%), although this rate is lower than in historic studies. The overall initial cure rate was 75%. The initial cure rate for APD was 77.2% and for CAPD was 73.7%. No causative organism was isolated in 17% of cases.
Conclusion. PD-associated peritonitis is the leading cause of technique failure in Scotland. We validate previous studies showing a decrease in the proportion of peritonitis episodes that are caused by coagulase-negative staphylococci. APD peritonitis rates are not significantly better than CAPD peritonitis rates in Scotland, and the initial cure rates for APD and CAPD are similar.
Keywords: patient outcome; peritoneal dialysis; peritonitis; quality assurance; technique failure
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Introduction
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As a result of the introduction of the flush before fill twin bag system and the emergence of improved connection systems, the incidence rates of peritonitis have decreased substantially [1]. Despite this, peritonitis remains one of the major complications of peritoneal dialysis (PD) and peritonitis is the most common reason why patients switch from PD to haemodialysis [2].
In view of the adverse effect of peritonitis on patient outcomes on PD, standards for the management of peritonitis have been established in some countries. The Renal Association (the national society of renal physicians in the UK) has published Recommended Standards for the Treatment of Adult Patients with Renal Failure [3]. These standards were derived from clinical results in historic cohorts of PD patients [4]. The second edition of the Renal Association standards document [5] was used for clinical audit during the time of this study and stated that:
- Peritonitis rates should be less than one episode per 18 months.
- The negative peritoneal fluid culture rate in patients with clinical peritonitis should be <10%.
- The initial cure rate of peritonitis should be >80% (without the necessity of removing the peritoneal catheter).
This study reports the incidence, causative organisms and outcome of all episodes of PD-associated peritonitis in Scotland during a 3.5 year period. The influence on technique failure was assessed. All results were compared with the Renal Association standards [5], historical cohorts of patients listed in the Cochrane Renal Group review [1] and a US national survey [6].
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Methods
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This study was conducted in all 10 adult renal units in Scotland. A twin bag disconnect system was the standard connectology used for continuous ambulatory peritoneal dialysis (CAPD) in all of the units, and a luer lock method was used for automated peritoneal dialysis (APD). The empiric antibiotics used in the units after the initial diagnosis of peritonitis were an aminoglycoside and vancomycin in six units, and ceftazidime and vancomycin in four units (Table 1). Two units changed from the former to the latter regime during the study period. Only two units (units 7 and 10) continued the patients on APD during episodes of peritonitis. Four units used nasal mupiricin for 5 days after the time of catheter insertion in nasal carriers of Staphylococcus aureus, and one of these units (unit 5) used recurrent courses of nasal mupiricin in such patients. The PD nurses from each of the 10 renal units in Scotland reported the following data from their unit every 6 months from January 1999 to June 2002:
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Table 1. Comparison of the initial cure rate with the empiric antibiotic regime and the number of days of intraperitoneal antibiotic treatment used by the individual dialysis units for different causative organisms
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- number of prevalent patients and patient-months on PD
- number, causative organism and outcome of all episodes of peritonitis that occurred in their unit
- number of patients beginning and stopping PD
- the stated cause of technique failure in patients stopping PD
- type of PD.
Identification of the centres is possible from the number of PD patients in each unit. To maintain anonymity, therefore, the results are given as average number of months between episodes of peritonitis. The number of patients in each centre at any time during the study ranged from 12 to 98. PD-associated peritonitis was defined if the peritoneal effluent contained >100 white cells/µl with >50% polymorphonuclear leukocytes. Recurrent peritonitis was defined as a further episode of peritonitis within 4 weeks of stopping antibiotics, and this definition includes all episodes of peritonitis due to either a relapse or re-infection. A relapse of peritonitis was defined as a further episode of infection with either the same organism or a sterile peritonitis within 4 weeks of stopping antibiotics. A re-infection was defined as a further episode of peritonitis within 4 weeks of stopping antibiotics due to a different organism. Refractory peritonitis is defined as peritonitis that does not respond to antibiotic treatment and results in catheter removal. The standard operating procedure for culture of PD fluid was obtained from the microbiology departments. All departments cultured at 37°C but used different culture media and times for culture (Table 2).
Peritonitis rates were calculated as the number of infections for all patients in a group divided by the number of patient-months on PD for the group and expressed as months between episodes. We use the number of months between episodes of peritonitis to fit in with the Renal Association standards [5], to account for all episodes of infection and to allow comparisons among units with relatively small numbers of episodes of peritonitis. An actuarial analysis of time free of peritonitis is an alternative method that requires a larger number of peritonitis episodes to detect a specified difference in peritonitis rates [6,7]. Outcome was classified as initial cure, catheter removal or patient death. Initial cure was defined as resolution of evidence of peritonitis with antimicrobial therapy and without the need for catheter removal. Patient deaths included patients who died within 4 weeks of presentation of peritonitis even if the effluent white cell count had cleared.
Although the results are presented as person-months per episode of peritonitis, this was converted to the number of events per person-time of exposure for Poisson regression analysis. Poisson regression analysis of events per person-month of exposure was performed in STATA to compare peritonitis rates between units and between CAPD and APD.
2 comparisons were performed in SPSS to compare the initial cure rates in the different units and in the groups of different causative organisms or between CAPD and APD.
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Results
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The 1205 patients who were on PD during January 1999 [8] to June 2002 had a total of 1487 patient-years on PD. At the start of the study, there were 435 PD patients in Scotland of whom 116 (26.7%) were on APD. During the 3.5 year study period, 770 patients began PD (491 new end-stage renal failure patients, 205 patients transferring from haemodialysis, 63 failed transplants and 11 patients transferring from other centres) and 815 patients discontinued PD (396 patients transferred to haemodialysis, 216 died, 178 were transplanted, 16 recovered native renal function and nine transferred to other centres). Refractory or recurrent peritonitis accounted for 167 (42.2%) of the 396 technique failures, making peritonitis still the most common reason for stopping PD. Other causes of technique failure were: poor dialysis, 17.9%; failed peritoneal access, 13.6%; wish to transfer to haemodialysis, 9.3%; complications of high intraperitoneal pressure, 7.9%; poor ultrafiltration, 5.8%; and discontinuation of dialysis; 3.3%. At the end of the study period, 186 (47.7%) of the 390 patients were on APD.
Nine hundred and twenty-eight episodes of peritonitis occurred over the 3.5 year period. The peritonitis rate for CAPD was one episode every 18.6 months and the peritonitis rate for APD was one episode every 20.3 months. This gave a total peritonitis rate of one episode every 19.2 patient months (Table 3). Only one unit (unit 9) met the Renal Association standard of less than one episode of peritonitis every 18 months during each 6 months of the study period. There was no statistically significant difference between the rates of events per person-month between CAPD and APD (P = 0.21). Peritonitis rates for the individual units are shown in Table 3. In order to avoid exaggerating differences between units, the unit with the largest number of overall person-months of peritoneal dialysis, unit 2, was selected as the reference group. Total peritonitis rates were significantly lower in units 7 and 9 compared with unit 2 (P<0.0001). CAPD peritonitis events were significantly less frequent in unit 9 and significantly more frequent in unit 6 compared with the reference group (P = 0.0008). APD peritonitis events were significantly less frequent in unit 7 than in the reference group (P = 0.0044). Peritonitis rates in all other units were similar to those of unit 2.
The differences in the number of PD patients per centre, nurse staffing rates and unit protocols and procedures were analysed to try to explain the lower peritonitis rates in units 7 and 9 (Table 4). There was no correlation between the total number of patient-months on PD in each centre and the total, APD or CAPD peritonitis rates in each unit. There was no relationship between the number of PD patients per nurse or average training time and the unit peritonitis rate. The use of nasal mupiricin in 5 of the 10 units was associated with significantly reduced rates of peritonitis per person-month in these units (Table 5) (P = 0.012). Peritonitis events were 15% less frequent in the units using mupiricin [95% confidence interval (CI) 426%]. When the rates of S.aureus peritonitis were examined (Table 5), the units using mupiricin had a lower incidence (one episode every 106 months) compared with those that did not use mupiricin (one episode every 96.2 months), but the difference was not statistically significant (P = 0.52). Furthermore, since four of the units used intranasal mupirocin only at the start of PD, we performed a subanalysis of the incident patients to assess if the use of mupiricin may have delayed the first presentation of S.aureus peritonitis in patients in this study. There were 41 first episodes of S.aureus peritonitis in the 410 incident patients who did not receive mupirocin and 36 first episodes of S.aureus peritonitis in the 360 incident patients in the mupirocin group. The median time interval until the first episode of S.aureus peritonitis was 155 days for the mupirocin group and 156 days for those who did not receive mupirocin. There was therefore no evidence of a delayed presentation of S.aureus peritonitis in the patients in this study who were treated with mupirocin.
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Table 4. Comparison of the peritonitis rate, use of nasal mupiricin, the nurse to patient ratio and average patient training times in the individual units during the study period
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The national initial cure rate over the 3.5 year study period was 75%. The initial cure rates in each of the individual units during the study period are shown in Table 1. The overall culture-negative rate was 17%. The culture-negative rates for the individual units are shown in Table 2. In one of the units, which supervises PD patients who live on islands that are remote from the mainland centre, empiric antibiotics were started before peritoneal dialysate was sent to the laboratory for culture (unit 1). Nevertheless this unit had a culture-negative rate of only 11%.
Coagulase-negative Staphylococcus was the most common causative organism and accounted for 274 (29%) of the episodes of peritonitis. The next most common cause of peritonitis was S.aureus, and this organism accounted for 19.2% of infections. Twenty-four (13.5%) of the 178 S.aureus peritonitis episodes were due to methicillin-resistant S.aureus (MRSA). The other causative organisms are listed in Table 6. The Gram-negative organisms isolated were Escherichia coli, 33; Klebsiella, 22; Pseudomonas, 12; Proteus, nine; Enterobacter, six; Serratia, four; Acinetobacter, three; and Campylobacter, one. In a further 56 cases, the Gram-negative organism was classified simply as a coliform. The other organisms isolated were streptococci species, 75; diphtheroids, 11; Corynebacterium, eight; Nisseria, five; lactobacilli, 3; mixed growth 25; and eight other organisms. There was only one case of vancomycin-resistant Enterococcus (VRE) peritonitis reported during the 3.5 year study period. The culture-negative episodes of peritonitis exclude 14 cases of Extraneal®-associated peritonitis from four units during the last 6 months of the study. Extraneal®-associated peritonitis was defined as culture-negative peritonitis which resolved after stopping the use of Extraneal® dialysis fluid and without treatment with antibiotics.
The spectrum of organisms causing peritonitis in APD and CAPD is described in Table 6. Staphylococcus aureus peritonitis was 49% more frequent in CAPD than APD (P = 0.016; 95% CI 8105%) although caution is required in interpretation of this finding since the number of cases is not large. Whilst there were more episodes of peritonitis due to coagulase-negative staphylococci and Gram negatives in APD, this was not statistically significant in this study. The clinical outcomes of peritonitis caused by different organisms are also shown in Table 6. The prognosis for coagulase-negative staphylococcal peritonitis was the most favourable, with an initial cure rate of 89.8%. In contrast, fungal peritonitis always resulted in technique failure as the failure to respond promptly to antifungal therapy was considered by all units as an indication to remove the catheter. Gram-negative bacilli and S.aureus peritonitis episodes also had a poor prognosis. The initial overall cure rate for APD is 77.2% compared with 73.7% for CAPD, which is not statistically significant (P = 0.13). Only Gram-negative episodes of peritonitis showed any significant difference in cure rate between CAPD (45.3%) and APD (71.7%) (P = 0.003). There were 25 (2.7%) deaths associated with the 928 peritonitis episodes.
Seventy-four relapses of peritonitis are included in the 928 episodes of peritonitis. Table 7 shows a comparison between the spectrum of organisms causing relapses of peritonitis and the organisms causing the initial episodes of peritonitis. Coagulase-negative Staphylococcus was the most common organism causing a relapse of peritonitis, and 2 of the 17 S.aureus relapse infections were due to MRSA. There were also 14 cases of re-infection in the 928 episodes of peritonitis. Fungal peritonitis was the most common, causing 42.9% of re-infections, whilst coagulase-negative staphylococci, Gram negatives and other organisms caused 14.3, 14.3 and 28.6% of relapses of peritonitis, respectively.
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Table 7. Comparison of the causative organisms in initial episodes and relapses of peritonitis in Scotland from January 1999 to June 2002
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Discussion
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This study shows that PD-related peritonitis remains the most common cause of technique failure despite advances in PD systems. Peritonitis was the stated reason for 42.2% of patient transfers to haemodialysis, and therefore peritonitis continues to be the most important complication of PD.
The overall peritonitis rate in Scotland was one episode every 19.2 months. This meets the Renal Association standard of one episode of peritonitis every 18 months. The peritonitis rate in CAPD was higher than in APD, as has been described in previous studies [911], but this was not statistically significant in our national study. In a national census in the USA, Port et al. found that centres with >21 PD patients had lower peritonitis rates than smaller centres [6]. Our data show wide variation in the peritonitis rates between units (Table 3) and over time in individual units (data not shown) at least in part due to the small number of patients in some centres. There was no correlation between the unit peritonitis rate and the number of patient-months per unit, the nurse to patient ratio, use of home visits or the average number of days for patient training. The five units using nasal mupiricin had a significantly lower peritonitis rate than those that did not, although there was no significant difference in S.aureus peritonitis rates between the two groups. The time interval until the first episode of S.aureus peritonitis also was not different in a subanalysis of incident patients in the mupirocin and the non-mupirocin groups. It is therefore unclear whether the lower peritonitis rates in the mupirocin group reflect an effect of mupirocin or confounding factors. Unit 9, which had the lowest peritonitis rate (Table 4), was one of the units using nasal mupiricin prophylactically and was the only unit where the PD nurses were present in the operating theatre when peritoneal catheters were inserted. No other difference in unit procedures and policies was observed which may explain the lower rates of peritonitis in units 7 and 9.
The Cochrane Renal Group has reviewed [1] several studies showing superior peritonitis rates with the twin bag and the older Y-sets to that in this study of all PD patients in Scotland (Table 8). These studies have small numbers of patients and are performed in hospitals interested in undertaking PD research. There were also patient exclusion criteria in some of these studies since their aim was to compare peritonitis rates using different connection devices and not to give an accurate representation of population-based peritonitis rates. This illustrates the potential problem of publication bias if short-term results from centres with low peritonitis rates tend to be reported. We use the entire PD population of Scotland over a 3.5 year period to report the peritonitis rate in this national study, reflecting actual practice in a large, unselected population rather than in patients in research institutions considered eligible for trials. This may account for the poorer overall peritonitis rates compared with some of the trials listed in Table 8. Similarly, a national sample of all incident CAPD patients in the USA during the first 6 months of 1989 also showed poorer peritonitis rates [6] compared with studies using the same connection devices (Table 8). The large sample size lends weight to its validity as a report of actual clinical practice in the USA. The time interval between the first and second episodes of peritonitis was similar to the time interval until the first episode of peritonitis after starting PD [6]. This observation is supportive of using inverse peritonitis rates (average number of months between episodes of peritonitis) to report the incidence of peritonitis in large studies. In his review of the different methods of reporting peritonitis rates in PD patients, Vonesh has concluded that the method using the total number of peritonitis episodes/treatment time is preferred when there are <100 incident patients per group, especially if peritonitis rates continue to decline [7]. Unit 2 was the only centre that had >100 incident patients over the 3.5 year study period.
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Table 8. Comparison of peritonitis rates (months between episodes of peritonitis) reported in studies of peritoneal dialysis patients using standard, Y-set and twin bag connection devices
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There are no comparable data on the incidence of peritonitis in Scotland from the pre-Y-set era. The largest data set in the UK in this period was reported by the Working Party of the British Society for Antimicrobial Chemotherapy [12]. In comparison with this descriptive report of the isolated organisms in 250 culture-positive cases of peritonitis, our data show a large fall in the percentage of episodes of peritonitis due to coagulase-negative staphylococci counterbalanced by a rise in the proportion of cases of S.aureus peritonitis. There are also smaller rises in the proportion of fungal and Gram-negative cases in the modern era. The dramatic decrease in infections caused by coagulase-negative staphylococci when compared with historical data corresponds to other data sets, suggesting that Y-set and twin bag systems protect against coagulase-negative staphylococcal peritonitis, but not S.aureus peritonitis [13,14].
The empiric antibiotics used by the renal units in this study were reported to provide initial cure rates of 8090% in the review of studies from the pre-Y-set era by Millikin et al. [4]. The initial cure rate for PD-related peritonitis in this study was only 75%. This fails to meet the Renal Association's standard for an initial cure rate greater than 80% based on these historic studies. Only one unit managed to achieve this standard during the study (unit 10). When the initial cure rates for individual organisms are analysed, the reason becomes apparent. The initial cure rate for coagulase-negative staphylococci was 89.8%, whereas the combined initial cure rate for organisms associated with a poor prognosis (S.aureus, fungi and Gram-negative bacilli) was only 56%. As already described, the Y-set and twin bag systems have preferentially reduced the rate of peritonitis caused by the more easily treated coagulase-negative staphylococci. The poor initial cure rate can therefore be attributed to a higher proportion of episodes of peritonitis due to organisms with a poor prognosis. This is also the most likely reason why the reduction in peritonitis incidence has failed to impact significantly upon the high technique failure rate due to refractory or recurrent peritonitis. There is great concern that potential delay in the discovery of peritonitis in APD might be harmful for the peritoneal membrane [15]. Yishak et al. have reported a poorer outcome of peritonitis with APD compared with CAPD [16]. However, in this study, the initial cure rate for CAPD was 74% and for APD was 77%, concurring with the study of Rodriguez-Carmona et al. which showed no difference in clinical outcomes between peritonitis episodes in CAPD and APD [10]. Whilst the initial cure rate in this study is low, the death rate associated with peritonitis is also low at 2.7%. It may be postulated that these low initial cure and death rates indicate that the renal units were following the guidelines on the management of peritonitis of the International Society of Peritoneal Dialysis [17] that advocate early removal of the peritoneal catheter to prevent further injury to the peritoneal membrane and improve patient survival.
It is interesting to note that all renal units in Scotland independently have continued to use vancomycin as the empiric antibiotic of choice to cover Gram-positive organisms, despite the guidelines issued by the advisory committee of the International Society for Peritoneal Dialysis discouraging its use [17]. The ideal empiric treatment has been the subject of much debate, but the antimicrobial sensitivity patterns in this study may justify the continuing use of vancomycin in PD centres in Scotland. The prevalence of MRSA is high whilst there was only one case of VRE peritonitis in the 3.5 year period. Khairullah et al. have reported no cases of VRE in a recent 2 year study of also using empiric vancomycin for peritonitis in an out-patient setting [18].
The culture-negative rate was 17.2%. This is higher than the Renal Association standard, which stated that <10% of all episodes of PD peritonitis should be culture negative. All units failed to meet this target and the culture-negative rate ranged from 10 to 29%. There was a wide range of standard operating procedures for dialysate culture in the microbiology laboratories serving the 10 units (Table 2) and there is no obvious reason for the variation in culture-negative rates. The culture-negative rate of first episodes of peritonitis in a national survey in the USA was also relatively high at 20% [6]. The latest edition of the Recommended Standards for the Treatment of Adult Patients with Renal Failure has revised the standard for culture-negative rates upwards to <15% of all episodes of peritonitis [3]. Coagulase-negative staphylococcal peritonitis was the most common cause of recurrent peritonitis due to relapse after an apparent initial cure. Gram-negative organisms and fungi are under-represented as causes of relapse of peritonitis because of their lower initial cure rates. Fungal peritonitis is the leading cause of re-infection, presumably due to fungal overgrowth following treatment of an initial episode of bacterial peritonitis with antibiotics.
In summary, we confirm PD-associated peritonitis as the leading cause of technique failure of PD in Scotland. We confirm previous studies showing a decrease in the proportion of peritonitis episodes that are caused by coagulase-negative staphylococci. We show that Scotland does not meet the Renal Association Standards for initial cure and culture-negative rates. We propose that the fall in the proportion of episodes due to coagulase-negative staphylococci and the setting of standards based upon historic studies of selected patient populations may explain the failure to meet the current standards set by the Renal Association for initial cure and culture-negative rates in PD-associated peritonitis. We show no significant difference in the incidence of peritonitis between CAPD and APD, and we find no evidence for a worse outcome for peritonitis in patients on APD than CAPD. Units using nasal mupiricin have significantly lower peritonitis rates than those that do not.
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Acknowledgments
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The authors wish to thank the nursing staff for forwarding the data from each unit and participating in this national audit.
Conflict of interest statement. None declared.
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References
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Received for publication: 29. 5.03
Accepted in revised form: 2. 6.04