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CAPD-Related Peritonitis due to Salmonella enteritidis in a Patient With SLE
CASE REPORT
CAPD-Related Peritonitis due to Salmonella enteritidis in a Patient With SLE Yen-Ling Chiu, MD, Jenq-Wen Huang, MD, Po-Ren Hsueh, MD, Kwan-Dun Wu, MD, PhD, and Tzong-Shinn Chu, MD, PhD ● Patients with systemic lupus erythematosus are prone to various infections, often associated with high mortality. Salmonella species are a rare cause of continuous ambulatory peritoneal dialysis (CAPD) peritonitis, but patients with lupus are susceptible to infection caused by Salmonella species. A 47-year-old woman who had systemic lupus erythematosus with end-stage renal disease and was undergoing CAPD presented with fever, watery diarrhea, abdominal pain, and turbid dialysate effluent. The effluent culture yielded Salmonella enteritidis. Although she was administered antibiotics to which the organism was susceptible in vitro, peritonitis was not cured. Her clinical condition stabilized after removal of the Tenckhoff catheter and prolonged antibiotic use. In Salmonellarelated CAPD peritonitis, early catheter removal may be necessary to achieve complete treatment. Am J Kidney Dis 46:E21-E23. © 2005 by the National Kidney Foundation, Inc. INDEX WORDS: Continuous ambulatory peritoneal dialysis (CAPD); peritonitis; systemic lupus erythematosus (SLE); Salmonella enteritidis.
P
ERITONITIS IS THE MAIN infectious complication in patients undergoing continuous ambulatory peritoneal dialysis (CAPD). Systemic lupus erythematosus (SLE) nephritis is one of the important causes of end-stage renal disease in young adults in Taiwan. Our previous study showed that patients with SLE comprised up to 8.5% of patients receiving CAPD in National Taiwan University Hospital (Taipei, Taiwan), and these patients had a shorter interval to first infectious complications and poorer technique survival than patients without SLE or diabetes receiving CAPD.1 Infection also was the major cause of dropout and mortality in patients with SLE undergoing CAPD. Salmonella is an intracellular pathogen that is difficult to eradicate. Patients with SLE are unusually susceptible to infection caused by Salmonella species2; however, Salmonella is a rare cause of CAPD peritonitis. We report a patient with SLE undergoing CAPD who experienced an episode of peritonitis caused by Salmonella species. This is the first case report of Salmonellarelated CAPD peritonitis in a patient with SLE. CASE REPORT A 47-year-old woman was admitted to our hospital with a 3-day history of fever and chills. She had been receiving CAPD for end-stage renal disease caused by lupus nephritis for 4 years without peritonitis episodes. The patient regularly was administered 10 mg of prednisolone twice daily for lupus, but the dose had been increased to 50 mg/d 3 weeks before this admission because of arthritis.
After a 3-day course of diarrhea and abdominal pain followed by fever and chills, she visited the emergency department, where fever of 38.5°C, diffuse abdominal tenderness, and turbid dialysate effluent were noted. White blood cell count was 3.24 ⫻ 103/L (⫻ 109/L), with 95.6% neutrophils, 1.9% monocytes, and 2.5% lymphocytes. The peritoneal effluent study showed a white blood cell count of 2.5 ⫻ 103/L (⫻ 109/L), with 97% neutrophils, 2% mesothelial cells, and 1% lymphocytes. Gram stain showed no pathogen. Her serum high-sensitivity C-reactive protein concentration was 12.77 mg/dL (normal, ⬍0.8 mg/dL). Cefamezine, 1 g/d, and ceftazidime, 1 g/d, were administered intraperitoneally. Dialysate culture yielded a Salmonella species on day 5 of admission. Isolates were identified as Salmonella enteritidis on the basis of serotyping of O antigen (1, 9, 12) and H antigen (g, m), according to the Kauffman and White scheme that uses somatic and flagellar antigens (Becton Dickinson, Cockeysville, MD) and conventional biochemical identification methods and the Phoenix System (Becton Dickinson).3 The 16S ribosomal RNA partial sequencing analysis with a pair of universal primers (DG74 and RW01)
From the Departments of Internal Medicine and Laboratory Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine, Taipei, Taiwan. Received February 23, 2005; accepted in revised form April 18, 2005. Originally published online as doi:10.1053/j.ajkd.2005.04.021 on June 16, 2005. Supported in part by the Ta-Tung Kidney Foundation. Address reprint requests to Tzong-Shinn Chu, MD, PhD, Department of Internal Medicine, National Taiwan University Hospital, No 7 Chung-Shan South Rd, Taipei 100, Taiwan. E-mail: [email protected] © 2005 by the National Kidney Foundation, Inc. 0272-6386/05/4602-0029$30.00/0 doi:10.1053/j.ajkd.2005.04.021
American Journal of Kidney Diseases, Vol 46, No 2 (August), 2005: E21-E23
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CHIU ET AL
identified the isolate as having an identity of 99.7% (1,441 of 1,445 nucleotides) with Salmonella typhimurium (GenBank accession no. AE008893.1), 99.4% (1,436 of 1,445 nucleotides) with Salmonella typhi (accession no. AL627279.1), and 98.1% (1,417 of 1,445 nucleotides) with S enteritidis (accession no. SEU90318).4 The isolate was susceptible to cefotaxime, ceftriaxone, co-trimoxazole, chloramphenicol, and ciprofloxacin, but resistant to ampicillin, with standard disk diffusion susceptibility testing. The stool culture was negative. Antibiotic therapy was shifted to ceftriaxone, 1 g/d, intraperitoneally according to the susceptibility test. However, fever, abdominal pain, and turbid effluent persisted during the next week. Serum C-reactive protein concentration decreased to 4.30 mg/dL on day 12 of admission. Day 13 of admission, the Tenckhoff catheter was removed and the patient was shifted for temporary hemodialysis therapy. The fever and abdominal tenderness subsided 2 days later. The antibiotic was switched to intravenous administration and continued for 4 weeks, and serum C-reactive protein level finally decreased to 0.95 mg/dL. Whole-body gallium scanning showed no other foci of inflammation. She received a second Tenckhoff catheter, but it was improperly positioned and drained poorly, so the patient switched to long-term hemodialysis therapy.
DISCUSSION
Peritonitis is the most frequently encountered infectious complication of CAPD, but Salmonella is a rare pathogen in this infection. S enteritidis is the principal pathogen in salmonellosis in Taiwan.5 According to the literature, only Salmonella hadar6 and S enteritidis phage type 47 have caused CAPDrelated peritonitis before. In the first case report, a 67-year-old man experienced 1 episode of S hadar– related CAPD peritonitis, which resolved with amoxicillin therapy for 3 weeks. However, a second episode of S hadar–related CAPD peritonitis occurred 1 month later. As a result, ciprofloxacin was administered for 3 months to eliminate the presumed carrier status. Although the Tenckhoff catheter was not removed at that time, the follow-up course of this patient was not reported. In the second case report, S enteritidis–related CAPD peritonitis developed in a 23-year-old woman. Antibiotic therapy initially was successful, but peritonitis recurred, so the Tenckhoff catheter was removed and the patient abandoned CAPD therapy. Our case is similar to this one except that the stool culture was negative. All patients, including ours, had watery diarrhea before the episode of peritonitis and were administered prolonged antibiotic treatment with or without catheter removal. Patients with lupus are prone to various infections, especially those caused by Salmonella spe-
cies, because of their suppressed cellular immunity and steroid treatment. An epidemiological study showed that as much as 10% of infection caused by Salmonella choleraesuis in Taiwan is related to lupus.8 In our patient, lupus activity flared up, and the increase in steroid dosage might have made her more susceptible to infection caused by Salmonella species. Previous studies suggested that treatment for salmonellosis should be prolonged in patients with lupus because bacteremia frequently recurs and carries a high mortality rate2; therefore, the patient was administered ceftriaxone for 4 weeks. Although lupus activity tends to decrease after a patient enters end-stage renal disease, sometimes the diagnosis of CAPD peritonitis may be confounded by increased lupus activity.9 The outcome of patients with lupus with CAPD peritonitis has not been studied before. However, 1 study found that patients with lupus may have an increased risk for sclerosing peritonitis after peritonitis episodes.10 Immune-mediated serositis may represent a risk factor for the development of this condition. In the present case, despite the absence of direct examination with laparoscopy, it was clear that the second Tenckhoff catheter was malpositioned, and its malfunction might have been related to adhesions in the peritoneal cavity. Infection caused by Salmonella species can cause intestine adhesions, lymphatic invasion, and sepsis. Our patient and the 2 reported cases experienced a preceding episode of gastroenteritis. The route of inoculation of the pathogen thus might have been contamination of the connection devices by the patient’s hands or transmural translocation. In conclusion, Salmonella-related peritonitis in CAPD patients is very rare. Clinically, it usually is preceded by watery diarrhea. Despite use of antibiotics to which the causative organism is susceptible in vitro, peritonitis frequently relapses or cannot be cured. Early removal of the Tenckhoff catheter and prolonged antibiotic use may be necessary. REFERENCES 1. Huang JW, Hung KY, Yen CJ, Wu KD, Tsai TJ: Systemic lupus erythematosus and peritoneal dialysis: Outcomes and infectious complications. Perit Dial Int 21:143147, 2001 2. Shahram F, Akbarian M, Davatchi F: Salmonella infection in systemic lupus erythematosus. Lupus 2:5559, 1993
SALMONELLA IN AN SLE PATIENT ON CAPD
3. Hsueh PR, Teng LJ, Tseng SP, et al: Ciprofloxacinresistant Salmonella enterica typhimurium and choleraesuis from pigs to humans, Taiwan. Emerg Infect Dis 10:60-68, 2004 4. Hsu CC, Chen WJ, Chen SY, Chiang WC, Hsueh PR: Fatal septicemia and pyomyositis caused by Salmonella typhi. Clin Infect Dis 39:1547-1549, 2004 5. Chen YH, Chen TP, Tsai JJ, et al: Epidemiological study of human salmonellosis during 1991-1996 in southern Taiwan. Kaohsiung J Med Sci 15:127-136, 1999 6. Hirsch DJ, Jindal KK: Recurrent Salmonella peritonitis in a patient on CAPD. Perit Dial Int 13:163, 1993
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7. Orr KE, Wilkinson R, Gould FK: Salmonella enteritidis causing CAPD peritonitis. Perit Dial Int 13:164, 1993 8. Chen YH, Chen TP, Lu PL, et al: Salmonella choleraesuis bacteremia in southern Taiwan. Kaohsiung J Med Sci 15:202-208, 1999 9. Jalil NS, Lee J, Hoffman B, Soloway S: Lupus masquerading as CAPD peritonitis. Adv Perit Dial 9:152155, 1993 10. Odama UO, Shih DJ, Korbet SM: Sclerosing peritonitis and systemic lupus erythematosus: A report of two cases. Perit Dial Int 19:160-164, 1999
CAPD-Related Peritonitis due to Salmonella enteritidis in a Patient With SLE Yen-Ling Chiu, MD, Jenq-Wen Huang, MD, Po-Ren Hsueh, MD, Kwan-Dun Wu, MD, PhD, and Tzong-Shinn Chu, MD, PhD ● Patients with systemic lupus erythematosus are prone to various infections, often associated with high mortality. Salmonella species are a rare cause of continuous ambulatory peritoneal dialysis (CAPD) peritonitis, but patients with lupus are susceptible to infection caused by Salmonella species. A 47-year-old woman who had systemic lupus erythematosus with end-stage renal disease and was undergoing CAPD presented with fever, watery diarrhea, abdominal pain, and turbid dialysate effluent. The effluent culture yielded Salmonella enteritidis. Although she was administered antibiotics to which the organism was susceptible in vitro, peritonitis was not cured. Her clinical condition stabilized after removal of the Tenckhoff catheter and prolonged antibiotic use. In Salmonellarelated CAPD peritonitis, early catheter removal may be necessary to achieve complete treatment. Am J Kidney Dis 46:E21-E23. © 2005 by the National Kidney Foundation, Inc. INDEX WORDS: Continuous ambulatory peritoneal dialysis (CAPD); peritonitis; systemic lupus erythematosus (SLE); Salmonella enteritidis.
P
ERITONITIS IS THE MAIN infectious complication in patients undergoing continuous ambulatory peritoneal dialysis (CAPD). Systemic lupus erythematosus (SLE) nephritis is one of the important causes of end-stage renal disease in young adults in Taiwan. Our previous study showed that patients with SLE comprised up to 8.5% of patients receiving CAPD in National Taiwan University Hospital (Taipei, Taiwan), and these patients had a shorter interval to first infectious complications and poorer technique survival than patients without SLE or diabetes receiving CAPD.1 Infection also was the major cause of dropout and mortality in patients with SLE undergoing CAPD. Salmonella is an intracellular pathogen that is difficult to eradicate. Patients with SLE are unusually susceptible to infection caused by Salmonella species2; however, Salmonella is a rare cause of CAPD peritonitis. We report a patient with SLE undergoing CAPD who experienced an episode of peritonitis caused by Salmonella species. This is the first case report of Salmonellarelated CAPD peritonitis in a patient with SLE. CASE REPORT A 47-year-old woman was admitted to our hospital with a 3-day history of fever and chills. She had been receiving CAPD for end-stage renal disease caused by lupus nephritis for 4 years without peritonitis episodes. The patient regularly was administered 10 mg of prednisolone twice daily for lupus, but the dose had been increased to 50 mg/d 3 weeks before this admission because of arthritis.
After a 3-day course of diarrhea and abdominal pain followed by fever and chills, she visited the emergency department, where fever of 38.5°C, diffuse abdominal tenderness, and turbid dialysate effluent were noted. White blood cell count was 3.24 ⫻ 103/L (⫻ 109/L), with 95.6% neutrophils, 1.9% monocytes, and 2.5% lymphocytes. The peritoneal effluent study showed a white blood cell count of 2.5 ⫻ 103/L (⫻ 109/L), with 97% neutrophils, 2% mesothelial cells, and 1% lymphocytes. Gram stain showed no pathogen. Her serum high-sensitivity C-reactive protein concentration was 12.77 mg/dL (normal, ⬍0.8 mg/dL). Cefamezine, 1 g/d, and ceftazidime, 1 g/d, were administered intraperitoneally. Dialysate culture yielded a Salmonella species on day 5 of admission. Isolates were identified as Salmonella enteritidis on the basis of serotyping of O antigen (1, 9, 12) and H antigen (g, m), according to the Kauffman and White scheme that uses somatic and flagellar antigens (Becton Dickinson, Cockeysville, MD) and conventional biochemical identification methods and the Phoenix System (Becton Dickinson).3 The 16S ribosomal RNA partial sequencing analysis with a pair of universal primers (DG74 and RW01)
From the Departments of Internal Medicine and Laboratory Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine, Taipei, Taiwan. Received February 23, 2005; accepted in revised form April 18, 2005. Originally published online as doi:10.1053/j.ajkd.2005.04.021 on June 16, 2005. Supported in part by the Ta-Tung Kidney Foundation. Address reprint requests to Tzong-Shinn Chu, MD, PhD, Department of Internal Medicine, National Taiwan University Hospital, No 7 Chung-Shan South Rd, Taipei 100, Taiwan. E-mail: [email protected] © 2005 by the National Kidney Foundation, Inc. 0272-6386/05/4602-0029$30.00/0 doi:10.1053/j.ajkd.2005.04.021
American Journal of Kidney Diseases, Vol 46, No 2 (August), 2005: E21-E23
e21
e22
CHIU ET AL
identified the isolate as having an identity of 99.7% (1,441 of 1,445 nucleotides) with Salmonella typhimurium (GenBank accession no. AE008893.1), 99.4% (1,436 of 1,445 nucleotides) with Salmonella typhi (accession no. AL627279.1), and 98.1% (1,417 of 1,445 nucleotides) with S enteritidis (accession no. SEU90318).4 The isolate was susceptible to cefotaxime, ceftriaxone, co-trimoxazole, chloramphenicol, and ciprofloxacin, but resistant to ampicillin, with standard disk diffusion susceptibility testing. The stool culture was negative. Antibiotic therapy was shifted to ceftriaxone, 1 g/d, intraperitoneally according to the susceptibility test. However, fever, abdominal pain, and turbid effluent persisted during the next week. Serum C-reactive protein concentration decreased to 4.30 mg/dL on day 12 of admission. Day 13 of admission, the Tenckhoff catheter was removed and the patient was shifted for temporary hemodialysis therapy. The fever and abdominal tenderness subsided 2 days later. The antibiotic was switched to intravenous administration and continued for 4 weeks, and serum C-reactive protein level finally decreased to 0.95 mg/dL. Whole-body gallium scanning showed no other foci of inflammation. She received a second Tenckhoff catheter, but it was improperly positioned and drained poorly, so the patient switched to long-term hemodialysis therapy.
DISCUSSION
Peritonitis is the most frequently encountered infectious complication of CAPD, but Salmonella is a rare pathogen in this infection. S enteritidis is the principal pathogen in salmonellosis in Taiwan.5 According to the literature, only Salmonella hadar6 and S enteritidis phage type 47 have caused CAPDrelated peritonitis before. In the first case report, a 67-year-old man experienced 1 episode of S hadar– related CAPD peritonitis, which resolved with amoxicillin therapy for 3 weeks. However, a second episode of S hadar–related CAPD peritonitis occurred 1 month later. As a result, ciprofloxacin was administered for 3 months to eliminate the presumed carrier status. Although the Tenckhoff catheter was not removed at that time, the follow-up course of this patient was not reported. In the second case report, S enteritidis–related CAPD peritonitis developed in a 23-year-old woman. Antibiotic therapy initially was successful, but peritonitis recurred, so the Tenckhoff catheter was removed and the patient abandoned CAPD therapy. Our case is similar to this one except that the stool culture was negative. All patients, including ours, had watery diarrhea before the episode of peritonitis and were administered prolonged antibiotic treatment with or without catheter removal. Patients with lupus are prone to various infections, especially those caused by Salmonella spe-
cies, because of their suppressed cellular immunity and steroid treatment. An epidemiological study showed that as much as 10% of infection caused by Salmonella choleraesuis in Taiwan is related to lupus.8 In our patient, lupus activity flared up, and the increase in steroid dosage might have made her more susceptible to infection caused by Salmonella species. Previous studies suggested that treatment for salmonellosis should be prolonged in patients with lupus because bacteremia frequently recurs and carries a high mortality rate2; therefore, the patient was administered ceftriaxone for 4 weeks. Although lupus activity tends to decrease after a patient enters end-stage renal disease, sometimes the diagnosis of CAPD peritonitis may be confounded by increased lupus activity.9 The outcome of patients with lupus with CAPD peritonitis has not been studied before. However, 1 study found that patients with lupus may have an increased risk for sclerosing peritonitis after peritonitis episodes.10 Immune-mediated serositis may represent a risk factor for the development of this condition. In the present case, despite the absence of direct examination with laparoscopy, it was clear that the second Tenckhoff catheter was malpositioned, and its malfunction might have been related to adhesions in the peritoneal cavity. Infection caused by Salmonella species can cause intestine adhesions, lymphatic invasion, and sepsis. Our patient and the 2 reported cases experienced a preceding episode of gastroenteritis. The route of inoculation of the pathogen thus might have been contamination of the connection devices by the patient’s hands or transmural translocation. In conclusion, Salmonella-related peritonitis in CAPD patients is very rare. Clinically, it usually is preceded by watery diarrhea. Despite use of antibiotics to which the causative organism is susceptible in vitro, peritonitis frequently relapses or cannot be cured. Early removal of the Tenckhoff catheter and prolonged antibiotic use may be necessary. REFERENCES 1. Huang JW, Hung KY, Yen CJ, Wu KD, Tsai TJ: Systemic lupus erythematosus and peritoneal dialysis: Outcomes and infectious complications. Perit Dial Int 21:143147, 2001 2. Shahram F, Akbarian M, Davatchi F: Salmonella infection in systemic lupus erythematosus. Lupus 2:5559, 1993
SALMONELLA IN AN SLE PATIENT ON CAPD
3. Hsueh PR, Teng LJ, Tseng SP, et al: Ciprofloxacinresistant Salmonella enterica typhimurium and choleraesuis from pigs to humans, Taiwan. Emerg Infect Dis 10:60-68, 2004 4. Hsu CC, Chen WJ, Chen SY, Chiang WC, Hsueh PR: Fatal septicemia and pyomyositis caused by Salmonella typhi. Clin Infect Dis 39:1547-1549, 2004 5. Chen YH, Chen TP, Tsai JJ, et al: Epidemiological study of human salmonellosis during 1991-1996 in southern Taiwan. Kaohsiung J Med Sci 15:127-136, 1999 6. Hirsch DJ, Jindal KK: Recurrent Salmonella peritonitis in a patient on CAPD. Perit Dial Int 13:163, 1993
e23
7. Orr KE, Wilkinson R, Gould FK: Salmonella enteritidis causing CAPD peritonitis. Perit Dial Int 13:164, 1993 8. Chen YH, Chen TP, Lu PL, et al: Salmonella choleraesuis bacteremia in southern Taiwan. Kaohsiung J Med Sci 15:202-208, 1999 9. Jalil NS, Lee J, Hoffman B, Soloway S: Lupus masquerading as CAPD peritonitis. Adv Perit Dial 9:152155, 1993 10. Odama UO, Shih DJ, Korbet SM: Sclerosing peritonitis and systemic lupus erythematosus: A report of two cases. Perit Dial Int 19:160-164, 1999