Peritonitis Caused by Haemophilus parainfluenzae,Leifsonia aquatica,and Gordonia spp. in a Patient Undergoing Continuous Ambulatory Peritoneal Dialysis

Abstract

Background:

Peritonitis has remained the most common serious complication of continuous ambulatory peritoneal dialysis (CAPD). In most cases, these infections are monomicrobial, and the pathogens involved most commonly are Staphylococci. Recently, polymicrobial infections with rare organisms have been reported more often.

Case Report:

We describe a patient who developed recurrent episodes of CAPD-associated peritonitis with a total of four pathogens: Methicillin-resistant S. aureus, Haemophilus parainfluenzae, Leifsonia aquatica, and Gordonia spp. The infection most likely was acquired when the patient used tap water for dialysis during a camping trip. All episodes were treated successfully with antibiotics. Finally, the device was removed, and later, a new catheter was implanted, which still is in use.

Conclusion:

Peritoneal dialysis-associated peritonitis may be caused by rare organisms. Antibiotics may be able to treat disease temporarily, but removal of contaminated catheters usually is required.

Approximately 500,000 individuals in the United States require renal replacement therapy, and more than 80,000 are on the waiting list for a kidney transplant at the United Network for Organ Sharing [1]. Renal replacement using hemodialysis is associated with multiple problems as well as the inconvenience of visits to a dialysis center three times each week. Continuous ambulatory peritoneal dialysis (CAPD) is accepted widely by patients, mainly because they are able to become independent of dialysis centers. The main complication of this technology is infection [2 –4]. It is estimated that the overall incidence of peritonitis for the average patient is one bout every two years [5]. In many cases, the catheter must be removed to clear the infection and then be replaced at a later date if the peritoneal cavity has not been closed by adhesions. Indications for catheter removal include relapsing peritonitis within four weeks of completing antibiotic therapy, peritonitis refractory to treatment for longer than five days, refractory catheter infections, and fungal peritonitis [6].

Unlike surgical peritonitis, CAPD-associated peritonitis usually is caused by a single organism; polymicrobial infections are found in only 1% of cases, although recently this number has increased substantially [5,7]. In the case of recurrent infection, the pathogens cultured initially are isolated again commonly during subsequent episodes of peritonitis [8]. Historically, the spectrum of responsible pathogens included coagulase-negative staphylococci (CoNS), Staphylococcus aureus, and streptococci, with other microorganisms occurring much less frequently [6]. Kim et al. reported that recently, the development of disconnect systems has decreased the incidence of peritonitis to less than half of its previous value [5]. The decrease has affected the incidence of CoNS peritonitis disproportionately, which, although the most common, is among the least virulent and easiest to treat. Overall, from 1992 to 2001, the proportion of peritonitis caused by gram-positive organisms decreased from 87% to 70% and the proportion caused by single gram-negative species increased from 7% to 28%, which is worrisome given that the corresponding mortality rates for these infections are 1.4% and 3.7%, respectively [5].

Increasingly, CAPD-associated peritonitis is being caused by more virulent bacteria, and many recent reports describe CAPD-associated peritonitis with rare pathogens, sometimes representing a first case of a thus far unknown human pathogen [5]. We herein report on a patient who developed recurrent episodes of CAPD-associated peritonitis with a total of four pathogens: methicillin-resistant S. aureus (MRSA), Haemophilus parainfluenzae, Leifsonia aquatica, and Gordonia spp. Pleomorphic infections of any kind are rare in CAPD-associated peritonitis. Furthermore, this is, to our knowledge, the first reported case of Gordonia peritonitis and the first case in which a single CAPD patient suffered recurrent infections with such an unusual combination of rare pathogens. It is thought that this unusual situation developed because of the improper use of tap water as dialysate while the patient was on a camping trip.

Case Report

A 50-year-old female with an allergy to sulfonamide drugs and a history of reflux necessitating urethral dilatation at age 3, ureteral reimplantation at ages 13 and 15, ultimately leading to chronic kidney disease, began hemodialysis and joined the transplant list. However, after she was found to have intraductal breast cancer necessitating a right mastectomy, radiation, and chemotherapy. Thereafter, she was considered unsuitable for transplantation and decided to transition to CAPD four years after she began renal replacement therapy to obtain more independence. She was initially in good health and tolerated CAPD well; however, she developed peritonitis with MRSA. She was treated with intravenous vancomycin, but presented subsequently with abdominal pain, cloudy peritoneal fluid, and low-grade fever. She had leukocytosis of 10,000/mm³; peritoneal fluid demonstrated 400 leukocytes/mm³ and grew pleomorphic gram-negative bacilli that eventually proved to include H. parainfluenzae. She was treated with ciprofloxacin, and an MRSA eradication protocol was administered for numerous skin lesions. A peritoneal fluid culture the following month grew L. aquatica. Disk diffusion testing tentatively showed susceptibility to amoxicillin-clavulanic acid, trimethoprim-sulfamethoxazole, and vancomycin. Nine days later, after acute worsening of her abdominal pain, re-emergence of low-grade fever, and the development of cloudy peritoneal fluid, she was readmitted to the hospital. Blood tests revealed 4,333 leukocytes/mm³ with an 80% neutrophil predominance. A culture of peritoneal fluid demonstrated a Gordonia species that essentially was pan-sensitive, including amoxicillin-clavulanic acid with a minimum inhibitory concentration (MIC) of <2 mcg/mL, a sensitivity to ciprofloxacin with a MIC of <0.125 mcg/mL, a sensitivity to trimethoprim-sulfamethoxazole of 0.5 mcg/mL, and a sensitivity to ceftriaxone with a MIC of 4 mcg/mL. Treatment consisted of a three-week course of amoxicillin-clavulanic acid, and her peritoneal catheter was removed; she was switched back to hemodialysis. Her infection resolved quickly with this intervention, and she remained asymptomatic for the next several months with the exception of a long-standing rash. The skin lesions were suspected to be the source of the infection, and a computed tomography scan was performed to exclude any intra-abdominal source. It was at this time that the patient revealed that prior to the first episode of peritonitis, she had gone camping in Yellowstone National Park and may have used tap water for dialysate, although she insisted that when she used this water, she had no acute onset of complications with her CAPD. Despite her unfortunate experience, she maintained a great preference for CAPD over hemodialysis, and another catheter was placed, which is still in use after three years without any complications.

Discussion

This series of CAPD-associated peritonitis episodes involved three pathogens that thus far have not been described in this setting. This infection most likely was acquired when the patient used contaminated water in Yellowstone National Park. Although we have no environmental sample to prove this conclusion, the patient's history and the resolution of the recurrent infection after removal of the dialysis device strongly support it. The pathogens encountered in this patient are most unusual causes of peritonitis, but luckily, they proved not to be especially virulent. Still, this situation could have been avoided with proper technique for CAPD and the use of sterile dialysate solution. Despite the decrease in the overall incidence of CAPD-associated infection, the use of properly treated, properly sealed dialysate is crucial to avoiding peritonitis. Once the catheter was removed, the infection cleared quickly and completely with antibiotics, and, ultimately, her abdomen was suitable for insertion of a new CAPD catheter.

The mortality rate from CAPD-associated peritonitis can be as high as 6% [9]. The majority of CAPD-related peritonitis can be managed with out-patient antibiotics, and 75% are cured, but each case puts the patient's life at risk with increasingly virulent and unfamiliar pathogens [10]. A low threshold for the use of broad-spectrum antibiotics should be applied if the cultures are not immediately conclusive. Different culture techniques may aid in proper identification of under diagnosed pathogens and lead to more focused therapies.

Haemophilus parainfluenzae is a gram-negative coccobacillus that has been reported to cause peritonitis in only a few cases [11 –16]. Betriu et al., who reported the first patient with CAPD-associated H. parainfluenzae peritonitis in 1999, noted that although the organism is a commensal of the upper respiratory tract, it occasionally colonizes the gastrointestinal tract. Those authors believed that the source of peritoneal infection may have been touch contamination or transmural migration from the gastrointestinal lumen, as has been recorded with Escherichia coli. Haemophilus parainfluenzae may be under-diagnosed because of its slow growth and strict requirement for nicotinamide adenine dinucleotide or factor V, which rarely are provided in laboratory culture media [11]. Proper microbial nutrition could be provided by including peritoneal fluid in the culture medium. This bacterium is difficult to culture and with modification of culture practice may be found more often in cases of polymicrobial peritonitis than is the case currently.

Until 1962, the actinomycete L. aquatica was known as Cornybacterium aquaticum, and it still is reported occasionally under this name. There are four reports of this bacterium causing peritonitis. Interestingly, all cases seem to have been dialysis-dependent patients [17 –22]. Leifsonia aquatica is a motile, catalase-positive, oxidase-positive, gram-positive bacillus. Leifsonia spp. are pathogens of plants more frequently than of human beings, the targets include sugar cane [23]. Still, Leifsonia is a resilient organism that has been recovered from many water habitats, including Himalayan glaciers and filtered Antarctic ice [24,25]. As Sulpher et al. noted, they can tolerate low temperatures and alkaline water and can pass through polycarbonate filters [21]. Leifsonia aquatica has been found in tap water on multiple occasions, illustrating the importance of ensuring the purity of all water used as dialysate. To be used as dialysate, water must be treated with an array of filters, deionizers, and reverse osmosis [21]. The American Association for the Advancement of Medical Instrumentation recommends that dialysate microbial counts be <2,000 colony-forming units/mL [21]. The importance of using properly treated and tightly sealed water is emphasized by the postulated mechanism of infection in our patient.

Our patient is the first recorded case of peritonitis caused by Gordonia spp. Gordonia, a family of actinomycetes that was, until 20 years ago, classified as rhodococci, is a group of aerobic, weakly acid-fast, gram-positive bacilli that rarely produce infections in human beings [26,27]. There are numerous accounts of bacteremia caused by Gordonia, mostly in immunocompromised patients, including a recent case in which a rubber-degrading species from a rotting automobile tire became transferred to a central venous catheter [28 –31]. However, the infection probably is under-diagnosed, as laboratories without molecular sequencing can easily misidentify the bacteria as related Cornybacterium or Nocardia species. Gene sequencing using 16S rRNA and high-performance liquid chromatography have become widely accepted tools in identifying rare pathogens [32,33]. In our patient, the culture and sensitivity results did not return until 32 days after our culture, by which time, our treatment regimen of amoxicillin-clavulanic acid had eradicated the weakly virulent infection.

The spectrum of pathogens involved in CAPD peritonitis is ever-expanding, and the most unusual pathogens are being isolated at an increasing frequency. Given this rising prevalence of unusual and difficult-to-culture bacteria, there is a great need for more sophisticated microbiologic techniques; and there will be an increasing need to treat infections without timely conclusive cultures, as identification may require an unusually long time, as in our patient. If recurrence or refractory infection is encountered, removing the catheter with concurrent antibiotic therapy can greatly reduce the mortality rate [6,34]. Insertion of a new CAPD catheter may be feasible in many cases after successful treatment of peritonitis.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

References

Leichtman

, Cohen

, Keith

et al. Kidney and pancreas transplantation in the United States, 1997–2006: The HRSA Breakthrough Collaboratives and the 58 DSA Challenge. Am J Transplant, 2008; 8:946–957.

Port

, Held

, Nolph

et al. Risk of peritonitis and technique failure by CAPD connection technique: A national study. Kidney Int, 1992; 42:967–974.

Al-Allak

, Jones

, Stiff

et al. Long-term outcome of continuous ambulatory peritoneal dialysis (CAPD) peritonitis: Surgery can be avoided. Ann R Coll Surg Engl, 2009; 91:118–122.

Davenport

. Peritonitis remains the major clinical complication of peritoneal dialysis: The London, UK, peritonitis audit 2002–2003. Perit Dial Int, 2009; 29:297–302.

Kim

, Yoo

, Ryu

et al. Changes in causative organisms and their antimicrobial susceptibilities in CAPD peritonitis: A single center's experience over one decade. Perit Dial Int, 2004; 24:424–432.

Boeschoten

, Ter Wee

, Divino

. Peritoneal dialysis-related infections recommendations 2005—An important tool for quality improvement. Nephrol Dial Transplant, 2006; 21,Suppl 2:ii31–ii33.

Kim

, Korbet

. Polymicrobial peritonitis in continuous ambulatory peritoneal dialysis patients. Am J Kidney Dis, 2000; 36:1000–1008.

Finkelstein

, Jekel

, Troidle

et al. Patterns of infection in patients maintained on long-term peritoneal dialysis therapy with multiple episodes of peritonitis. Am J Kidney Dis, 2002; 39:1278–1286.

Perez Fontan

, Rodriguez-Carmona

, Garcia-Naveiro

et al. Peritonitis-related mortality in patients undergoing chronic peritoneal dialysis. Perit Dial Int, 2005; 25:274–284.

10.

von Graevenitz

, Amsterdam

. Microbiological aspects of peritonitis associated with continuous ambulatory peritoneal dialysis. Clin Microbiol Rev, 1992; 5:36–48.

11.

Betriu

, Coronel

, Martin

, Picazo

. Peritonitis caused by Haemophilus parainfluenzae in a patient undergoing continuous ambulatory peritoneal dialysis. J Clin Microbiol, 1999; 37:3074–3075.

12.

Brautbar

, Esayag

, Breuer

et al. Spontaneous bacterial peritonitis caused by Haemophilus parainfluenzae. Isr Med Assoc J, 2007; 9:175–176.

13.

Frankard

, Rodriguez-Villalobos

, Struelens

, Jacobs

. Haemophilus parainfluenzae: An underdiagnosed pathogen of biliary tract infections? Eur J Clin Microbiol Infect Dis, 2004; 23:46–48.

14.

Gallant

, Malinak

, Gump

, Mead

. Haemophilus parainfluenzae peritonitis associated with an intrauterine contraceptive device. Am J Obstet Gynecol, 1977; 129:702–703.

15.

Mayer

, Schweizer

. Primary peritonitis in a child caused by Haemophilus parainfluenzae. Pediatr Surg Int, 2002; 18:728–729.

16.

Riahi

, Hansen

, Bjerre

, Kragsbjerg

. ERCP complicated by a retroperitoneal abscess caused by Haemophilus influenzae and Haemophilus parainfluenzae. Gastrointest Endosc, 1998; 47:417–418.

17.

D'Amico

, Mangano

, Spinelli

et al.

[From the Mailing List SIN: Epidemic of infections caused by “aquatic” bacteria in patients undergoing hemodialysis via central venous catheters] (Ita)

G Ital Nefrol, 2005; 22:508–513.

18.

Fujinaga

, Ohtomo

, Hirano

et al. Relapsing peritonitis with Corynebacterium aquaticum in a boy receiving automated peritoneal dialysis. Pediatr Nephrol, 2009; 24:1253–1254.

19.

Kwon

, Lee

. Corynebacterium aquaticum peritonitis in a patient on CAPD. Perit Dial Int, 1997; 17:98–99.

20.

Levitski-Heikkila

, Ullian

. Peritonitis with multiple rare environmental bacteria in a patient receiving long-term peritoneal dialysis. Am J Kidney Dis, 2005; 46:e119–e124.

21.

Sulpher

, Desjardins

, Lee

. Central venous catheter-associated Leifsonia aquatica bacteremia in a hemodialysis-dependent patient. Diagn Microbiol Infect Dis, 2008; 61:64–66.

22.

Morris

, Henderson

, Bremner

, Collins

. Relapsing peritonitis in a patient undergoing continuous ambulatory peritoneal dialysis due to Corynebacterium aquaticum. J Infect, 1986; 13:151–156.

23.

Monteiro-Vitorello

, Camargo

, Van Sluys

et al. The genome sequence of the gram-positive sugarcane pathogen Leifsonia xyli subsp. xyli. Mol Plant Microbe Interact, 2004; 17:827–836.

24.

Reddy

, Prabagaran

, Shivaji

. Leifsonia pindariensis sp. nov., isolated from the Pindari glacier of the Indian Himalayas, and emended description of the genus Leifsonia. Int J Syst Evol Microbiol, 2008; 58:2229–2234.

25.

Pindi

, Kishore

, Reddy

, Shivaji

. Description of Leifsonia kafniensis sp. nov. and Leifsonia antarctica sp. nov. Int J Syst Evol Microbiol, 2009; 59:1348–1352.

26.

McNeil

, Brown

. The medically important aerobic actinomycetes: Epidemiology and microbiology. Clin Microbiol Rev, 1994; 7:357–417.

27.

Brust

, Whittier

, Scully

et al. Five cases of bacteraemia due to Gordonia species. J Med Microbiol, 2009; 58:1376–1378.

28.

Blaschke

, Bender

, Byington

et al. Gordonia species: Emerging pathogens in pediatric patients that are identified by 16S ribosomal RNA gene sequencing. Clin Infect Dis, 2007; 45:483–486.

29.

Grisold

, Roll

, Hoenigl

et al. Isolation of Gordonia terrae from a patient with catheter-related bacteraemia. J Med Microbiol, 2007; 56:1687–1688.

30.

Gupta

, Prasad

, Khara

, Alcid

. A rubber-degrading organism growing from a human body. Int J Infect Dis, 2010; 14:e75–e76.

31.

Jannat-Khah

, Halsey

, Lasker

et al. Gordonia araii infection associated with an orthopedic device and review of the literature on medical device-associated Gordonia infections. J Clin Microbiol, 2009; 47:499–502.

32.

Blanc

, Dalle

, Markarian

et al.

Gordonia terrae: A difficult-to-diagnose emerging pathogen?

J Clin Microbiol, 2007; 45:1076–1077.

33.

Gil-Sande

, Brun-Otero

, Campo-Cerecedo

et al. Etiological misidentification by routine biochemical tests of bacteremia caused by Gordonia terrae infection in the course of an episode of acute cholecystitis. J Clin Microbiol, 2006; 44:2645–2647.

34.

Piraino

, Bailie

, Bernardini

et al. Peritoneal dialysis-related infections recommendations: 2005 update. Perit Dial Int, 2005; 25:107–131.