Clinical course of peritonitis due to Pseudomonas species comtor. complicating peritoneal dialysis: A review of 104 cases

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1 Kidney International, Vol. 59 (2001), pp Clinical course of peritonitis due to Pseudomonas species complicating peritoneal dialysis: A review of 104 cases CHEUK-CHUN SZETO, KAI-MING CHOW, CHI-BON LEUNG, TERESA YUK-HWA WONG, ALAN KA-LUN WU, ANGELA YEE-MOON WANG, SIU-FAI LUI, and PHILIP KAM-TAO LI Department of Medicine and Therapeutics, Prince of Wales Hospital, The Chinese University of Hong Kong, Shatin, Hong Kong, China Clinical course of peritonitis due to Pseudomonas species comtor Conclusions. Recent antibiotic therapy is the major risk facplicating peritoneal dialysis: A review of 104 cases. for peritonitis due to the Pseudomonas species. Exit site Background. Peritonitis due to Pseudomonas species is a infection and recent antibiotic therapy are associated with poor serious complication in continuous ambulatory peritoneal dialsponse therapeutic response to antibiotics. When the therapeutic re- ysis (CAPD) patients. The clinical course of peritonitis due to is suboptimal, early Tenckhoff catheter removal may Pseudomonas complicating CAPD remains unclear. help preserve the peritoneum for further peritoneal dialysis. Methods. All of the Pseudomonas species episodes of peritoperitoneal Elective Tenckhoff catheter exchange after clearing up the nitis in our dialysis unit were studied from 1995 to During dialysis effluent may also reduce the likelihood of this period, there were 859 episodes of peritonitis recorded, relapse. It is desirable to use third-generation cephalosporin 113 of which were caused by the Pseudomonas species. Nine in the initial antibiotic regimen for peritonitis treatment in episodes were excluded because they were mixed growth. The localities with a high incidence of peritonitis due to the Pseuremaining 104 episodes in 68 patients were reviewed. domonas species. Results. The underlying renal diagnosis and prevalence of comorbid conditions of the 68 patients were similar to those found in our entire dialysis population. There was a history of antibiotic therapy within 30 days of the onset of peritonitis due Peritonitis due to the Pseudomonas species is a serious to the Pseudomonas species in 69 episodes (66.3%). In 47 complication in continuous ambulatory peritoneal dial- episodes (45.2%) there was a concomitant exit site infection. ysis (CAPD) patients [1 3], and is one of the most impor- The overall primary response rate was 60.6% and the complete tant causes of technique failure in CAPD [3, 4]. A guidecure rate was 22.1%. The presence of exit site infection was associated with a lower primary response rate (22 in 47 vs. line for the management of CAPD peritonitis by the Ad 41 in 57 episodes, P 0.01) and a lower complete cure rate Hoc Advisory Committee on Peritonitis Management (5 in 47 vs. 18 in 57 episodes, P 0.02). The episodes that [the International Society of Peritoneal Dialysis (ISPD) had received recent antibiotic therapy had a significantly lower protocol] recommends double antibiotic therapy, which complete cure rate than the de novo cases (8 in 69 vs. 15 in may include a third-generation cephalosporin, aminogly- 35 episodes, P 0.001). Episodes receiving third-generation cephalosporin as part of the initial antibiotic regimen had a coside, or quinolone drugs [4, 5]. However, this recom- significantly higher primary response rate than the ones that mendation was based on a series of small clinical studies initially received aminoglycoside (54 in 81 episodes vs. 8 in 22 [1, 2, 6 9]. The clinical course of this notorious complicaepisodes, P 0.05), but their complete cure rates were similar. tion remains unclear. Twenty-four cases failed to respond to antibiotics and the In our locality, CAPD is the first-line renal replace- Tenckhoff catheter was removed. The chance of returning to CAPD was higher when the Tenckhoff catheter was removed ment therapy for all end-stage renal disease patients on day 10 than on day 15 (9 in 14 cases vs. 5 in 10 cases), although [3, 10]. Patients are switched to long-term hemodialysis the result was not statistically significant. The Tenckhoff only when they have ultrafiltration failure or peritoneal catheter was removed and replaced at another site simultane- sclerosis. This policy has provided an excellent opportuously in another 14 cases after the effluent cleared up. None nity to examine the clinical outcome of peritonitis due of these patients had a relapse of peritonitis within three months. to Pseudomonas species with contemporary therapy in a large unselected group of CAPD patients in a retro- Key words: renal failure, CAPD, antibiotics, bacterial infection, Tenck- spective study. hoff catheter, cephalosporin therapy, exit site infection. Received for publication September 28, 2000 and in revised form December 12, 2000 Accepted for publication December 26, by the International Society of Nephrology METHODS All episodes of CAPD peritonitis in our unit from January 1995 to December 1999 were reviewed. The diagnosis 2309

2 2310 Szeto et al: Peritonitis due to Pseudomonas in CAPD Table 1. Loading and maintenance doses of antibiotics terium, either the Tenckhoff catheter was removed imfor peritonitis mediately or the antibiotics were changed (the salvage Maintenance antibiotics group), as judged clinically by the individual Drug Loading IP dose a IP dose a nephrologist. The salvage antibiotic regimens were gen- Vancomycin 1000 mg b erally two of the following: amikacin, ciprofloxacin, or Netromycin 150 mg if body weight 50 kg 15 mg 200 mg if body weight 50 kg piperacillin. Cephalosporin c 1000 mg 250 mg Tenckhoff catheters were removed and patients were a Per 2-liter dialysate; antibiotics were given intravenously when the patient put on temporary hemodialysis when peritonitis failed was septic or required rapid cycle dialysis for other reasons b to resolve with antibiotics. Tenckhoff catheter reinser- Loading dose was given every five days as a maintenance dose c Cephalosporins included cefazolin, ceftazidime, cefepime, and cefaperazone tion was attempted in all cases. As described in our plus sulbactam; cefazolin was used for the coverage of gram-positive organisms previous study [10], in our locality patients were switched to long-term hemodialysis only when attempts at Tenck- hoff catheter reinsertion failed because of peritoneal adhesion, or when there was ultrafiltration failure caused by peritoneal sclerosis. In selected cases as judged by [4]; the loading dose of cefepime was 2000 mg IP when the drug was used as a monotherapy (that is, without vancomycin) [12] of peritonitis was based on at least two of the following the individual nephrologist, the Tenckhoff catheter was [11]: (1) abdominal pain or cloudy peritoneal dialysis removed and a new catheter was reinserted simultaneeffluent (PDE); (2) leukocytosis in PDE [white blood ously at a different site after the antibiotic treatment cells (WBC) 100/mL]; and (3) positive Gram stain or for the peritonitis episode was completed (the catheter culture from PDE. Episodes with peritoneal eosinophilia exchange group). Early relapse was defined as recurbut negative bacterial culture were excluded. A bacterial rence of peritonitis by the same organism within 30 days culture of PDE was performed using BacTAlert bottles of completion of the antibiotic treatment [13]. Late re- (Organon Teknika Corp., Durham, NC, USA). Isolation lapse was defined as recurrence of peritonitis by the same and identification were performed by standard tech- organism within 120 days of completion of antibiotics. nique. Antibiotic sensitivity was determined by the com- Complete cure was defined as complete resolution of parative disc-diffusion method. peritonitis by antibiotics alone within 120 days without Over the five-year study period, 859 episodes of perito- relapse, salvage antibiotics, or catheter exchange. All of nitis were recorded. One hundred thirteen episodes the patients were monitored for at least three months (13.2%) were caused by the Pseudomonas species and after their treatment was completed. nine episodes were excluded from analysis because the Statistical analysis was performed using SYSTAT 7.0 PDE cultures showed mixed bacterial growth. The case for Windows (SPSS Inc., Chicago, IL, USA). All data RESULTS From 1995 to 1999, 859 episodes of peritonitis were recorded in our unit. The overall peritonitis rate was 18.2 patient months per episode. One hundred thirteen episodes (13.2%) were caused by the Pseudomonas spe- cies. Nine of these episodes were excluded from analysis because the PDE culture showed mixed bacterial growth. The remaining 104 episodes of peritonitis from Pseudomonas species were reviewed in 68 patients. Their demographic and baseline clinical data are summarized in Table 2. The species of Pseudomonas isolated from PDE are summarized in Figure 1. Most of the episodes were caused by Pseudomonas aeruginosa. The isolated bacteria were resistant to netilmicin in seven cases (6.7%). In two of them, the patient had received netilmicin within 30 days of the onset of the peritonitis episode. The bacteria iso- records of the remaining 104 episodes in 68 patients were reviewed. The demographic characteristics, underlying medical conditions, previous peritonitis episodes, recent antibiotic therapy, antibiotic regimen for the peritonitis episode, requirement of Tenckhoff catheter removal, and clinical outcome were examined. Recent antibiotics were defined as antibiotic therapy within 30 days of the onset of peritonitis from the Pseudomonas species. Episodes without recent antibiotics were called de novo cases. Peritonitis episodes were treated with our center s standard antibiotic protocol, which was changed systemically over time. Initial antibiotics for peritonitis generally consisted of intraperitoneal administration of a third- or fourth-generation cephalosporin, plus or minus vancomycin, or cefazolin plus netilmicin. Antibiotic regimens for individual patients were modified when culture results became available. The antibiotic dosing regimens are summarized in Table 1. In general, patients received two antibiotics to which the isolated bacterium was sensitive in vitro for at least 21 days [4]. Primary response was defined as resolution of abdominal pain, clearing of dialysate, and PDE neutrophil count of less than 100 per ml on day 10 with antibiotics alone. If the PDE did not clear up on day 10 despite in vitro sensitivity of the bac- were expressed in mean SD unless otherwise specified. Data were compared by the chi-square test, Fisher exact test, and Student t-test as appropriate. A P value of less than 0.05 was considered significant. All probabilities were two tailed.

3 Szeto et al: Peritonitis due to Pseudomonas in CAPD 2311 Table 2. Demographic and baseline clinical data N of patients (%) Total 68 Sex male:female 35:33 Age a years Duration on dialysis a months Renal diagnosis Glomerulonephritis 23 (33.8%) Diabetic nephropathy 16 (23.5%) Polycystic kidney 4 (5.9%) Hypertensive nephrosclerosis 4 (5.9%) Obstructive uropathy 2 (2.9%) Others/unknown 19 (27.9%) Disconnect system a 58 (55.8%) a Data of all 104 episodes were included because some patients had more than one episode of peritonitis due to Pseudomonas species Fig. 1. Prevalence of the identified Pseudomonas species. lated were resistant to ceftazidime in five cases (4.8%), to piperacillin in five cases (4.8%), and to amikacin in three cases (2.9%). None of the patients had received Twelve patients (11.5%) died within three months the corresponding antibiotic recently. In 47 episodes after the onset of peritonitis caused by Pseudomonas spe- (45.2%), there was a concomitant exit site infection. Howcies. The causes of death were peritonitis from Pseudoever, the same Pseudomonas species was isolated in only monas species per se (4 cases), fungal peritonitis (1 case), 21 episodes (20.2%). cardiovascular disease (4 cases), termination of dialysis Clinical outcome (because of severe coexisting medical illnesses; 2 cases), The clinical outcome is summarized in Figure 2. The and unrelated malignancy (1 case). overall primary response rate was 60.6% and the complete cure rate was 22.1%. The initial antibiotic regimen, Recent antibiotic therapy primary response rate, and complete cure rate of the There was a history of antibiotic therapy within 30 days individual regimens are summarized in Figure 3. Epi- of the onset of peritonitis due to Pseudomonas species sodes that received third-generation cephalosporin as in 69 episodes (66.3%; the post-antibiotic cases). Among part of the initial antibiotic regimen had significantly the 746 episodes of peritonitis not from the Pseudomonas higher primary response rates than the episodes where species, 147 episodes (19.7%) had a history of antibiotic aminoglycoside was the initial therapy (54 of 81 episodes therapy within 30 days of the onset of peritonitis (P vs. 8 of 22 episodes, P 0.05). However, there was no dif ). ference in their complete cure rates (19 of 81 episodes vs. For the peritonitis episodes due to Pseudomonas spe- 3 of 22 episodes, P 0.39). The primary response rate and complete cure rate were not associated with age, cies, antibiotics had been given in 29 cases (27.9%) to sex, duration of dialysis, underlying renal diagnosis, or treat recent peritonitis by other organisms, in 28 cases diabetic status (details not shown). (26.9%) due to exit site infection, and in 11 cases (10.6%) Thirty-four cases showed no clearing of PDE on day for unrelated medical reasons. The antibiotics given to 10. The Tenckhoff catheter was immediately removed these patients are summarized in Figure 4. Thirty-two in 14 cases, and 9 of them (64.3%) could return to CAPD patients (30.8%) had received two or more antibiotics after a period of temporary hemodialysis. In the 20 cases within 30 days of the onset of peritonitis due to Pseudothat received salvage antibiotic therapy, 10 cases responded monas species. within another five days (Fig. 2). There was no clinical Episodes receiving recent antibiotic therapy had a sigresponse in the other 10 cases, and the Tenckhoff cathe- nificantly lower complete cure rate than the de novo cases ter was removed. Only five cases (50%) could return to (8 of 69 vs. 15 of 35 episodes, P 0.001). Their primary CAPD afterward. The presence of exit site infection of response rate also tended to be lower (38 of 60 vs. 25 of any origin was associated with a lower primary response 35 episodes, P 0.11), but the result was not statistically rate (22 in 47 vs. 41 in 57 episodes, P 0.01) and lower complete cure rate (5 in 47 vs. 18 in 57 episodes, P significant. Of the 20 cases that received salvage-antibi- 0.02). Exit site infection from Pseudomonas species was otic therapy (Fig. 2), 13 had received recent antibiotics. also associated with a lower primary response rate (9 in Only 3 of the 13 cases that had received recent antibiotics 21 vs. 54 in 83 episodes, P 0.063) and a lower complete responded to salvage antibiotics. On the other hand, all cure rate (2 in 21 vs. 21 in 83 episodes, P 0.15), but seven de novo cases responded to salvage antibiotics the result was not statistically significant. (P 0.005).

4 2312 Szeto et al: Peritonitis due to Pseudomonas in CAPD Fig. 2. Summary of clinical outcome. *One patient died of myocardial infarct two months later. **One patient died of malignancy six weeks later. Fig. 3. Initial antibiotic regimen for the peritonitis episodes and their relationship to the clinical response. Symbols are: ( ) complete cure; ( ) clearing by day 10; ( ) no primary response. Peritonitis rate over five years The overall peritonitis rate and percentage of peritoni- tis episodes caused by Pseudomonas species in our unit from 1995 to 1999 are summarized in Figure 5. During this period, the peritonitis rate in our unit improved from 14.2 to 21.8 patient-months per episode. However, there was a parallel rise in the percentage of peritonitis caused by Pseudomonas species, from 7.1% in 1995 to 16.7% in Further examination showed that the incidence of de novo peritonitis from the Pseudomonas species remained similar over five years, but the incidence of cases that had received recent antibiotics rose progressively from 1995 to 1999 (Fig. 6). DISCUSSION In this case series, we examined 104 consecutive epi- sodes of peritonitis due to Pseudomonas species in our unit from 1995 to To the best of our knowledge, this is the largest study to date of CAPD peritonitis

5 Szeto et al: Peritonitis due to Pseudomonas in CAPD 2313 Fig. 5. Overall peritonitis rate ( ) and percentage of peritonitis episodes caused by Pseudomonas species ( ) during the five-year study period. Fig. 4. Recent antibiotic therapy prior to the onset of peritonitis due to the Pseudomonas species. (A) Incidence of individual antibiotic treatment and (B) number of antibiotics prescribed. caused by this notorious organism. Although this is a retrospective study, most of the cases were managed according to contemporary guidelines [4, 14]. The clinical course of our cases is therefore representative of cases that have received modern, state-of-the-art treatment. Peritonitis from the Pseudomonas species accounted for 13.2% of all CAPD peritonitis in the present study. This incidence was substantially higher than many reported series [1, 2, 6 9], which might be partly explained by the low incidence of Gram-positive peritonitis after widespread utilization of disconnect peritoneal dialysis systems [15 17]. Pseudomonas species accounted for 2.9% of the positive blood cultures and 6.3% of the positive urinary cultures in our hospital during the same period. We do not believe the high incidence of peritonitis due to the Pseudomonas species in this study is the result of a high overall rate of Pseudomonas species infection in our hospital. It is interesting to note that another group from Hong Kong has also reported a high incidence of exit site Fig. 6. Incidence of de novo peritonitis from Pseudomonas species ( ) and of episodes in patients who had recent antibiotic therapy ( ). infection due to Pseudomonas species in peritoneal dialysis patients [18]. It is possible that some unique local factors exist that could account for our high rate of infection by Pseudomonas species in this region. Although our cases were not confined to summer, we believe the warm and humid climate of Hong Kong, which favors the accumulation of sweat and dirt around catheter exit sites and contributes to the growth and colonization of bacteria such as Pseudomonas species, was probably an important factor. In fact, almost half of our cases had pre-existing exit site infections. During the study period, we worked vigorously to try to reduce the incidence of peritonitis from Pseudomonas species. Although infection by the Pseudomonas species can occur from contaminated water taps or bathing water, we do not think that explains our high prevalence of peritonitis due to Pseudomonas species. Furthermore, as outlined in our previous series of peritonitis due to Xanthomonas, almost all of our patients lived in an urban area and received the usual domestic water supply [19]. In 1997, we performed bacterial cultures of the antiseptic

6 2314 Szeto et al: Peritonitis due to Pseudomonas in CAPD solution and other peritoneal dialysis utilities for seven higher primary response rate with cephalosporin is certainly cases of peritonitis due to Pseudomonas species, and a desirable effect because the peritoneum as dialcases none of the facilities proved to be contaminated (unpub- ysis membrane is expected to be better preserved [25, 26]. lished data). Before 1998, povidone-iodine painting was In localities with a high incidence of peritonitis due to used for exit site care in all of the cases at our center, Pseudomonas, we suggest the use of third-generation which might have encouraged the growth of resistant cephalosporin as one of the initial antibiotics for treat- organisms. Nevertheless, the incidences of exit site infec- ment of CAPD peritonitis. Interestingly, the recent ISPD tion and peritonitis due to Pseudomonas species did not recommendation of peritonitis treatment also favors decrease despite the adoption of soap and water for exit third-generation cephalosporin, although for different site cleansing in mid-1998 (Figs. 5 and 6). We typically reasons [5]. treated exit site infections with chlorhexidine or hydro- Because of practical difficulties, immediate Tenckhoff gen peroxide dressing, together with oral cloxacillin or catheter removal was not possible and salvage antibiotics cefuroxime. Ciprofloxacin was used in cases of exit site were used in 20 cases when PDE failed to clear up on infection due to Pseudomonas species because of its high day 10. Although half the cases responded, most of these efficiency [20]. (7 out of 10) were de novo cases. Furthermore, of the In this case series, recent antibiotic therapy was an patients whose Tenckhoff catheter removal was delayed important risk factor for a poor response to treatment. (that is, because they failed to respond to salvage antibiotics), No other risk factor for developing peritonitis from Pseudomonas half could not return to CAPD, mostly because species was identified; the patients in the pres- of failed Tenckhoff catheter reinsertion. On the other ent study had a similar prevalence of diabetes, cardiovascular hand, when catheters were removed on day 10, two thirds disease, and chronic hepatitis when compared with of the patients could return to CAPD after a period the entire peritoneal dialysis population as reported in of temporary hemodialysis. Our finding highlights the our previous studies [3, 10, 21]. importance of early Tenckhoff catheter removal once There are two possible explanations for our observation. the response to antibiotics is suboptimal. First, use of antibiotics alters body flora and pro- As recommended by several small-scale studies [27 29], vokes the development of resistant bacterial strains we performed Tenckhoff catheter exchange after PDE [22, 23]. Although in vitro resistance to antibiotics was cleared up if the patient had persistent exit site infection not common in the bacterial strains isolated from our (not necessarily caused by the Pseudomonas species). patients (in 93 cases the isolated bacteria were sensitive We found this approach to be highly effective, and none to all the anti-pseudomonal species antibiotics tested), of the 14 cases had a relapse of peritonitis after the it was probably not the Pseudomonas species itself that catheter exchange. This observation suggests that relapse was resistant, but rather that the use of antibiotics had peritonitis is mostly caused by the persistence of bacterial removed the normal bacterial flora and perhaps given biofilm on the peritoneal catheter, which has been shown the Pseudomonas species a relative survival advantage. by many other groups [30, 31]. Liberal prescription of antibiotics was common among In summary, peritonitis due to the Pseudomonas spefamily physicians in Hong Kong [24]. cies is a notorious complication of peritoneal dialysis. Second, recent antibiotic therapy was a surrogate Recent antibiotic therapy is the major risk factor. Exit marker of recent peritonitis or exit site infection (in over site infection and recent antibiotic therapy are associated 80% of cases, antibiotics had recently been prescribed with poor therapeutic response to antibiotics. In localifor either of these indications), either of which could ties with a high incidence of peritonitis from Pseudomoexplain the poor clinical response. Peritonitis can spe- nas species, it is desirable to include third-generation cifically alter local peritoneal defenses, and a thickened cephalosporin in the initial antibiotic regimen for CAPD peritoneum may be more vulnerable to further peritoni- peritonitis. When the therapeutic response is suboptimal, tis episodes. In our series, exit site infection from Pseu- early Tenckhoff catheter removal may help preserve the domonas species alone was only marginally correlated peritoneum for further peritoneal dialysis. Elective Tenckwith clinical response. hoff catheter exchange after PDE has cleared may also Most of the episodes in the present study were treated reduce subsequent relapse. with netilmicin plus a third-generation cephalosporin. However, we found that the primary response rate of ACKNOWLEDGMENT the cases initially treated with third-generation cephalo- This study was supported in part by the CUHK research account sporin (that is, netilmicin had been added when peritoni- # tis due to Pseudomonas species was confirmed) was higher than for episodes initially treated with netilmicin Reprint requests to Dr. Cheuk-Chun Szeto, Department of Medicine and Therapeutics, Prince of Wales Hospital, The Chinese University of (with cephalosporin added subsequently). Although the Hong Kong, Shatin, Hong Kong, China. complete cure rates were not statistically different, the ccszeto@cuhk.edu.hk

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