Alcaligenes xylosoxidans Cholecystitis and Meningitis Acquired during Bathing Procedures in a Burn Unit: A Case Report

The information in this article was presented at the 37th Annual Meeting of the Japan Society of Burn, Nagoya, Japan, June 7–8, 2008. Alcaligenes xylosoxidans, a nonfermentative, Gram-negative rod often found in aqueous environments, has been isolated from respirators, incubators, and disinfectant solutions in the hospital environment. It is known to cause disease in immunocompromised (eg, burn) patients and represents a cross-contamination risk related to wound care. In the authors’ burn unit, two patients, admitted with deep dermal burns during a 1-month time period, acquired serious A. xylosoxidans infections. The first involved A. xylosoxidans-associated cholecystitis in an adult with 32% total body surface area (TBSA) burns and the second involved A. xylosoxidans meningitis in an adult with 30% TBSA burns. Both patients received hydrotherapy (bathing) in the same bathing tub, one patient after the other. Culture from environmental sources isolated A. xylosoxidans from the bathing mattress. Bacterial analysis of the isolates, including antimicrobial susceptibility testing and pulsed-field gel electrophoresis, suggested the patients had been infected by the same strain — ie, cross-contaminated — probably during treatment of their burns. The isolated strains were resistant not only to broad-spectrum penicillins and cephalosporins, but also to imipenem, to which past A. xylosoxidans strains have been susceptible. These findings underscore the need for strict infection control to prevent cross-contamination and disease outbreak.

   In the hospital environment, Alcaligenes xylosoxidans has been isolated from respirators, incubators, and disinfectant solutions.^1,2 A. xylosoxidans infection is thought to occur mostly in immunocompromised patients and those with severe underlying disease conditions. ^3,4 The majority of A. xylosoxidans strains are multidrug-resistant; thus, strict infection control is required to prevent spread of disease. ^3,4 Two cases (one unusual because of the rarity of A. xylosoxidans-related cholecystitis) occurred within a 1-month period in patients who had sustained severe burns and had been treated in the burn unit of the authors’ facility.

Case Reports

   Case 1. Mr. B, a 78-year-old man, sustained flame burns when his trousers accidentally caught fire in May 2007. He was immediately taken to the authors’ burn unit. On initial examination, it was noted that Mr. B had sustained deep burn (DB) to both lower legs, comprising 8% of the total body surface area (BSA); deep dermal burn (DDB) to both thighs, comprising 14% of the total BSA; and superficial dermal burn (SDB) to both forearms and the face, comprising 10% of the total BSA (see Figure 1). A decompression incision was made in both lower legs. The next day, all DB and DDB tissue was surgically removed from the legs and skin grafting was performed. Seven days after surgery, Mr. B underwent hydrotherapy in a hospital bathing tub — 10 days later, he developed a high fever and severe infection in both lower legs. Below-the-knee amputation was performed emergently for both legs due to life-threatening sepsis. Mr. B’s general condition improved over the next 2 weeks and he underwent bathing treatment every other day. Forty days after the injury, A. xylosoxidans was isolated from the residual wound, prompting immediate culture of environmental surfaces. A. xylosoxidans was isolated from the bathing mattress (see Figure 2). Clinical systemic and local inflammatory symptoms were not observed and the entire wound was resurfaced with free skin grafting.

   Mr. B was discharged from the burn unit 10 weeks after admission but 1 week later, he developed a temperature of 39.1° C and stomach pain. An abdominal CT scan detected a swollen gallbladder and expanded bile duct (see Figure 3). Hematological studies revealed a white blood cell (WBC) count of 11.9×109/L and increases in C-reactive protein (CRP) (9.9 mg/dL), alkaline phosphatase (485 IU/L), and gamma-glutamyl transpeptidase (87 IU/L) levels, indicating severe inflammation of the gallbladder (cholecystitis). Percutaneous transhepatic biliary drainage was performed and the remaining bile was drained continuously though a drainage tube. A. xylosoxidans was isolated from the bile and treatment with imipenem was initiated but subsequently changed to tazobactam/pippracillin following the results of antimicrobial susceptibility testing. Mr. B’s general condition improved over the next 3 weeks and he was discharged 3 months after the injury.

   Case 2. At the end of May 2007, 66-year-old Ms. K sustained scald burns when she accidentally fell over a bowl filled with boiling water. She was taken immediately to the authors’ emergency unit. On initial examination, Ms. K had sustained DDB to the back and right upper arm, comprising 20% of the total BSA; and SDB to both thighs, comprising 10% of the total BSA (see Figure 4). Initial surgery was performed the next day to remove all DDB tissue on the back along with free skin grafting. Seven days after surgery, Ms. K received hydrotherapy in the hospital’s bathing tub. Her general condition improved and she was discharged from the burn unit 2 weeks after the injury. The entire wound was resurfaced 10 weeks after the injury with another free skin graft.

   However, 12 weeks after the injury, the patient developed a mental disorder (agitated and compromised ability to communicate) with a fever of 38.8° C and a slight headache. A CT scan detected a swollen ventricle (see Figure 5). Hematological studies revealed a WBC count of 13.3×109/L, and an increased CRP level (2.9 mg/dL), indicating bacterial meningitis. Ventricular drainage was performed, and A. xylosoxidans was isolated from the cerebrospinal fluid (CSF). Treatment with amikacin and ceftazidime was initiated and subsequently changed to tazobactam/pippracillin and ceftazidime after antimicrobial susceptibility testing. Four weeks later, recognizing the absence of A. xylosoxidans in the CSF, a ventriculo-peritoneal shunt was inserted. Ms. K’s general condition improved and she was discharged 5 months after the injury.

   Figure 6 shows the clinical course of both patients.

Bacterial Isolate Analysis

   Three isolates of A. xylosoxidans, including those from the wound and bile of case 1, the CSF of case 2, and environmental sources, were subjected to antimicrobial susceptibility testing and pulsed-field gel electrophoresis (PFGE) and the results were found to be similar (see Table 1 and Figure 7). The isolates were resistant to almost all antibiotics, including ceftriaxone, cefpodoxime proxetil, cefepime, cefozopran, flomoxef sodium, imipenem, meropenem, aztreonam, entamicin, tobramycin, amikacin, minocycline, and ciprofloxacin; the only antibiotics to which all isolates were uniformly susceptible was tazobactam/pippracillin.

   Three isolates from the environmental sources — the CSF of case 2 and the bile of case 1 — were subjected to PFGE of Xba I-genomic DNA to determine their clonal homology (see Figure 7). The PFGE fingerprints of two isolates (Lane 1, environmental sources; and Lane 3, bile of case 1) showed identical patterns. Also, their PFGE fingerprints were closely related to that of Lane 2 (CSF of case 2).

Discussion

   A. xylosoxidans is a nonfermentative, Gram-negative rod often isolated from aqueous environments and known to cause disease in immunocompromised patients. Little has been reported about its pathogenicity in humans, except in cases involving children. ^2,5 Reports of CSF infection by A. xylosoxidans are even rarer. ⁶ In case studies, Kumar et al⁴ reported that two strains of A. xylosoxidans were isolated from CSF, Boukadida et al⁷ documented a case of A. xylosoxidans-associated neonatal meningitis transmitted by aqueous eosin, and D’Amato et al⁸ reported a case of A. xylosoxidans meningitis related to a gunshot wound. No case reports describing cholecystitis due to A. xylosoxidans were found in the literature.

   Burn wound infection is common and difficult to control because cutaneous surfaces are without protective barriers; thus, burn patients may easily acquire bacterial infection, including Staphylococcus aureus, Pseudomonas aeruginosa, Escherichia coli, Legionella pneumophila, Aerobacter aerogenes, Proteus vulgaris, and A. xylosoxidans. ^9-11 Several investigators have reported A. xylosoxidans in patients with underlying diseases, including malignancies, cardiac disease, and immunosuppression. ^4,5,12 Burn patients also have a high risk of infection because severe burns lead to a compromised immune system, which may cause life-threatening general infections, including sepsis, meningitis, and cholecystitis from common burn wound infections. The results of the susceptibility tests and PFGE patterns of all isolates were similar, suggesting that both patients acquired the organism due to cross-contamination of the same strains of A. xylosoxidans from the hospital environment — specifically, from the bathing mattress.

   Results of in vitro susceptibility studies of the isolates have found that A. xylosoxidans is a multidrug-resistant organism. Legrand et al⁵ studied susceptibility in 26 blood cultures from 10 patients with A. xylosoxidans infections between 1983 and 1988 and reported that the isolates were susceptible to trimethoprim-sulfamethoxazole, as well as the antipseudomonal penicillins, ceftazidime, cefoperazone, and imipenem. In 1996, Duggan et al¹² performed susceptibility studies in 11 cases of A. xylosoxidans bacteremia and found that all were susceptible to broad-spectrum penicillins, imipenem, ceftazidime, and trimethoprim-sulfamethoxazole. Aisenberg et al13 investigated 46 patients with hematogenous A. xylosoxidans infection between 1989 and 2003, reporting that most isolates exhibited susceptibility to carbapenems, antipseudomonal penicillins, and trimethoprim-sulfamethoxazole. In 2003, Gomem-Cerezo et al¹⁴ reviewed 44 cases of A. xylosoxidans bacteremia diagnosed over a 10-year period and concluded that antibiotic therapy with antipseudomonal penicillins or carbapenems would be a reasonable choice. Based on the authors’ review of current drug-susceptibility data, A. xylosoxidans appears to have become resistant to novel antibiotics to varying degrees, reducing the number of effective antimicrobial agents. Antipseudomonal penicillins and carbapenems have maintained their effectiveness against the organism until recently. However, strains of A. xylosoxidans isolated from the authors’ patients were found to be resistant not only to almost all antibiotics, including broad-spectrum penicillins and cephalosporins, but also to imipenem, to which past A. xylosoxidans strains were susceptible. Only tazobactam/pippracillin maintained their effectiveness against strains of A. xylosoxidans isolated from the authors’ patients and could improve their conditions.

Conclusion

   From the authors’ experience, including the two case studies presented, as well as information in the literature, A. xylosoxidans isolates should be considered as a possible etiology of infection in patients with extensive burn injuries. Various isolates were found to be multidrug-resistant but tazobactam/pippracillin still appear to be effective against the organism. Strict infection control practices are required to prevent cross-contamination and disease outbreaks in acute care facilities because, in addition to the case reported here, the organism has been cultured from several aqueous environments and needs to be monitored.

Dr. Fujioka is Director and Drs. Oka, Kitamura, and Yakabe are staff surgeons, Department of Plastic and Reconstructive Surgery, National Hospital Organization, Nagasaki Medical Center, Ohmura City, Japan. Dr. Chikaaki is on staff at the Department of Intensive Care Unit and Infection Control Center, Nagasaki Medical Center. Please address correspondence to: Masaki Fujioka, MD, PhD, Department of Plastic and Reconstructive Surgery, National Hospital Organization, Nagasaki Medical Center, 1001-1 Kubara 2, Ohmura City, Japan 856-8562; email: mfujioka@nmc.hosp.go.jp.

1. Vu-Thien H, Darbord JC, Moissenet D, et al. Investigation of an outbreak of wound infections due to Alcaligenes xylosoxidans transmitted by chlorhexidine in a burns unit. Eur J Clin Microbiol Infect Dis. 1998;17(10):724–726.

2. Reverdy ME, Freney J, Fleurette J, et al. Nosocomial colonization and infection by Achromobacter xylosoxidans. J Clin Microbiol. 1984;19(2):140–143.

3. Tsay RW, Lin LC, Chiou CS, et al. Alcaligenes xylosoxidans bacteremia: clinical features and microbiological characteristics of isolates. J Microbiol Immunol Infect. 2005;38(3):194–199.

4. Kumar A, Ray P, Kanwar M, Sethi S, Narang A. Investigation of hospital-acquired infections due to Achromobacter xylosoxidans in a tertiary care hospital in India. J Hosp Infect. 2006;62(2):248–250.

5. Legrand C, Anaissie E. Bacteremia due to Achromobacter xylosoxidans in patients with cancer. Clin Infect Dis. 1992;14(2):479–484.

6. Shigeta S, Yasunaga Y, Honzumi K, Okamura H, Kumata R, Endo S. Cerebral ventriculitis associated with Achromobacter xylosoxidans. J Clin Pathol. 1978;31(2):156–161.

7. Boukadida J, Monastiri K, Snoussi N, Jeddi M, Berche P. Nosocomial neonatal meningitis by Alcaligenes xylosoxidans transmitted by aqueous eosin. Pediatr Infect Dis J. 1993;12(8):696–697.

8. D’Amato RF, Salemi M, Mathews A, Cleri DJ, Reddy G. Achromobacter xylosoxidans (Alcaligenes xylosoxidans subsp. xylosoxidans) meningitis associated with a gunshot wound. J Clin Microbiol. 1988;26(11):2425–2426.

9. Breiman RF, Fields BS, Sanden GN, Volmer L, Meier A, Spika JS. Association of shower use with Legionnaires’ disease. Possible role of amoebae. JAMA. 1990;263(21):2924–2926.

10. Weber JM, Sheridan RL, Schulz JT, Tompkins RG, Ryan CM. Effectiveness of bacteria-controlled nursing units in preventing cross-colonization with resistant bacteria in severely burned children. Infect Control Hosp Epidemiol. 2002;23(9):549–551.

11. Haynes BW Jr, Hench ME. Hospital isolation system for preventing cross-contamination by staphylococcal and pseudomonas organisms in burn wounds. Ann Surg. 1965;162(4):641–649.

12. Duggan JM, Goldstein SJ, Chenoweth CE, Kauffman CA, Bradley SF. Achromobacter xylosoxidans bacteremia: report of four cases and review of the literature. Clin Infect Dis. 1996;23(3):569–576.

13. Aisenberg G, Rolston KV, Safdar A. Bacteremia caused by Achromobacter and Alcaligenes species in 46 patients with cancer (1989–2003). Cancer. 2004;101(9):2134–2140.

14. Gomem-Cerezo J, Suárez I, Ríos JJ, et al. Achromobacter xylosoxidans bacteremia: a 10-year analysis of 54 cases. Eur J Clin Microbiol Infect Dis. 2003;22(6):360–363.