Hemodialysis International 2019

CASE REPORT

Outbreak of nonfermentative Gram-negative

bacteria (Ralstonia pickettii
and Stenotrophomonas maltophilia)
in a hemodialysis center

May K. THET,1 Ma. Lourdes F. PELOBELLO,1 Milton DAS,1 Mohammed M. ALHAJI,2

Vui Heng CHONG,3 Muhammad Abdul Mabood KHALIL,1 Terence CHINNIAH4,
Jackson TAN2
1
Department of Renal Medicine, RIPAS Hospital, Bandar Seri Begawan, Brunei Darussalam; 2PAPRSB
Institute of Health Sciences, Universiti Brunei Darussalam, Brunei Darussalam; 3Department of Medicine,
RIPAS Hospital, Bandar Seri Begawan, Brunei Darussalam; 4Department of Microbiology, RIPAS Hospital,
Bandar Seri Begawan, Brunei Darussalam

Abstract
We report a case series of seven patients with nonfermentative Gram-negative bacteria infections in a
single dialysis center; four patients with Ralstonia pickettii and three patients with Stenotrophomonas
maltophilia. Two of the seven patients were admitted to hospital for intravenous antibiotic treatment,
while the rest were treated with oral antibiotics at home. Both the admitted patients had temporary vas-
cular catheter infections from the aforementioned pathogens. We conclude that the outbreak is due to
colonization of treated reverse osmosis water, presumably through contamination via polluted filters
and compounded by the usage of reprocessed dialysers in the dialysis center. This is especially relevant
because contaminated treated water is directly introduced into the blood compartment of the dialysers
during reprocessing. In addition, there seems to be a propensity for both organisms to cause prolonged
febrile reactions in patients with temporary vascular catheters, likely through the early development of
biofilm. Intensification of general sterilization procedures, servicing and replacement of old decrepit
components of the water treatment system and temporary cessation of dialyser reuse practice seem to
have halted the outbreak. Due to the virulent nature and difficult resistant profile of nonfermentative
Gram-negative bacteria, we strongly recommend meticulous vigilance in the surveillance of culture iso-
lates in routine microbiological specimens from dialysis centers, especially if there is a senescent water
treatment system and a practice of reprocessing dialysers.

Keywords: Outbreak, hemodialysis, Ralstonia Pickettii, Stenotrophomonas maltophilia

INTRODUCTION reported to be present in up to 5% of water sources in hos-

Nonfermentative Gram-negative bacteria (NFGNB) is an
emerging and threatening problem in hospitals. It is
Correspondence to: M. A. M. Khalil, Department of Renal
Medicine, RIPAS Hospital, Bandar Seri Begawan BA1710,
Brunei Darussalam. E-mail: doctorkhalil1975@hotmail.com
Conflict of Interest: All authors have declared no competing interest.
Disclosure of grants or other funding: None.
pital wards and more than half the isolates showed anti-
biotic resistance.1 Most are opportunistic pathogens that
cause infections in debilitated and immunosuppressed hos-
pital patients. Previous reports have focused on Pseudomo-
nas spp. and Acinetobacter spp. because of their higher
isolation rates in microbiological specimens.2 Rarer bacteria
like Ralstonia pickettii and Stenotrophomonas maltophilia have
recently generated greater interests because of their flourish-
ing prevalence and difficult resistant profiles. Nosocomial

© 2019 International Society for Hemodialysis

DOI:10.1111/hdi.12722

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K. Thet et al.

Table 1 Summary of cases

Duration
Dialysis on dialysis
Gender Age Etiology of ESRD access (years) Culture results Outcome
F 39 Glomerulonephritis Vascular 6 Ralstonia Pickettii Admitted to hospital and dialysis catheter
catheter removed. Empirical treatment with
ceftazidime. Catheter tip did not grow any
organism.
Arteriovenous fistula usage commenced.
F 63 Diabetes mellitus Fistula 20 Stenotrophomonas No admission required. A course of oral
maltophilia antibiotics were given.
Resolved after corrective measures were
performed on water system
M 61 Diabetes mellitus Fistula 5 Stenotrophomonas No admission required. Patient declined oral
maltophilia antibiotics.
Resolved after corrective measures were
performed on water system
M 52 Diabetes mellitus Fistula 4 Ralstonia pickettii No admission required. A course of oral
antibiotics were given.
Resolved after corrective measures were
performed on water system
F 71 Unknown Fistula 13 Ralstonia pickettii No admission required. A course of oral
antibiotics were given.
Resolved after corrective measures were
performed on water system
F 59 Diabetes mellitus Vascular 1 Ralstonia pickettii Admitted to hospital and dialysis catheter
catheter removed. Treatment with intravenous
meropenem for 5 days. Catheter tip grew
R. picketti.
M 39 Diabetes mellitus Fistula 4 Stenotrophomonas No admission required. A course of oral
maltophilia antibiotics were given.
Resolved after corrective measures were
performed on water system

infections among susceptible individuals are more fre- CASE REPORT

quently reported and there has been a few documented
outbreaks in the literature, particularly relating to contami-
nation of pharmaceutical solutions3–5 and in varied settings
including oncology outpatients,6,7 pediatric emergency
department,8 hematology inpatient ward,9 and neonatal
intensive care unit.9,10 Reports of outbreaks came from
diverse countries including Taiwan,3,4 China,11 Italy,10
India,12 Bulgaria,13 Germany,14 and United States.15 Due to
its heighten profile, soaring prevalence, evolving resistance,
and virugenic potential, early reporting and identification of
infections are necessary to curtail the serious challenges
pose by the bacteria in the future.
We report an outbreak of seven patients with either
R. pickettii and S. maltophilia from a single center. Case
histories of every patients were briefly summarized and
presented. A literature review of all cases of infections
relating to both pathogens was also described.
Rigors were reported in three patients by nursing staff of a
dialysis center. All the patients were dialysed from the same
morning shift and had no complaints of recent infections or
hospitalizations. Blood cultures were taken from all the
patients but only one set grew R. picketti. That patient was
admitted for observation because the pyrexia did not sub-
side after dialysis. Biomedical engineers were alerted to the
problem and given immediate instructions to flush the dial-
ysis water system. Subsequent to that rigors were reported
in six other patients during different shifts over the next
24 hours. Only one patient who subsequently grew R. pick-
ettii, required hospitalization because of hemodynamic
compromise and persistent pyrexia. This patient, who is
diabetic and has a temporary vascular catheter, dropped
her blood pressure from 140/90 to 100/60 mmHg during
the hemodialysis session. Six sets of blood cultures were

2 Hemodialysis International 2019

 Gram-negative bacteria outbreak in hemodialysis unit

Table 2 Summary of reported cases of Ralstonia pickettii and Stenotrophomonas maltophilia infections in hemodialysis patients
Reference Ralstonia pickettii Stenotrophomonas maltophilia
Tan et al. 4 patients from same HD center; 2 patients 3 patients from same HD center; none of the
were admitted. The first patient who patient was admitted
dialysed with a permanent dialysis catheter,
was admitted with septicemic shock. Blood
culture and catheter tip culture grew
R. picketti. Infection resolved after removal of
catheter and treatment with intravenous
meropenem. The second admitted patient
also had a temporary dialysis catheter and
was discharged after 5 days of intravenous
antibiotics and removal of catheter.
Strateva et al.13 1 patient with permanent vascular catheter was
treated with intravenous ceftriaxone after
being febrile for a few days. Blood and
dialysis fluid culture grew R. pickettii.
Tajera et al.29 2 patients from different dialysis centers. The
first patient developed septic shock during
dialysis treatment necessitating admission to
intensive care unit. R. pickettii was identified
from blood and dialysis water culture. He
responded to intravenous meropenem.
The second patient developed intermittent
febrile illnesses over a period of 20 days in a
dialysis center. His clinical condition
deteriorated and was admitted to intensive
care unit for supportive treatment. Blood
cultures and dialysis water cultures grew
R. picketti and the patient responded to
piperacillin-tazobactam.
Edens et al.36 8 definite cases of S. maltophilia were reported
from a cluster of 3 clinics managed by the
same dialysis organization in United States.
When compared to controls, it was concluded
that patients were more likely to be reusing
dialysers and receiving nocturnal
hemodialysis.
Ganadu et al.38 S. maltophilia-related septicemia was reported in
a hemodialysis patient with a tunneled central
venous catheter. The patient responded to
intravenous ciprofloxacin and the removal of
the catheter.
Korzets et al.39 Two cases of dialysis catheter-related
bacteremia successfully treated with
trimethoprim-sulfamethoxazole. Both
patients had catheter removed and suffered
from transient pancytopenia during the
course of the treatment.
Kara et al.40 A hemodialysis patient with long-term central
venous catheter and S. maltophilia septicemia
was successfully treated with a combination of
trimethoprim-sulfamethoxazole and
ciprofloxacin and catheter removal.

Hemodialysis International 2019 3

K. Thet et al.
Table 2 Continued
Reference Ralstonia pickettii
Shah and
Feinfeld41
Kataria et al.42
Total affected 7 19
patients
sent off for all the affected patients; three grew R. Picketti
and another three isolated S. maltophilia. A summary of all
the affected patients is presented in Table 1.
The first admitted patient who grew R. pickettii
remained pyrexial in the ward for 3 days but subse-
quently made an unremarkable recovery after removal of
her tunneled dialysis catheter. No other source of sepsis
was identified. She was treated with intravenous merope-
nem and was discharged after 5 days. The catheter tip
also grew R. picketti, which was sensitive to meropenem,
imipenem, piperacillin-tazobactam, and ceftazidime but
resistant to ceftriazxone, cefuroxime, and amoxicillin/cla-
vulanic acid. The second admitted patient was observed
in the ward for 1 day. She was given an empirical treat-
ment of intravenous ceftazidime. The temporary tunneled
dialysis catheter was removed and fortunately, she
already had a mature fistula. Catheter tip did not grow
any organism but blood cultures showed R. picketti that
was sensitive to ceftazidime. Dialysis was commenced
through the arteriovenous fistula thenceforth. The rest of
the patients who were not warded were offered an oral
prescription of amoxicillin/clavulanic acid. Subsequent
blood culture reports confirmed sensitivity to the antibi-
otics and four patients completed the course of antibi-
otics whilst one patient declined. All the patients had
uncomplicated recovery at home and were not admitted
for further treatment.
Given the extent of the problem and the failure of resolu-
tion after flushing and disinfection, a decision was under-
taken to physically examine the water system and it was
found that the valve from the reverse osmosis outlet was
decrepit and rusty. There was also a built up of rust in the
valve of reprocessing machine. Water was sent for analysis
4 Hemodialysis International 2019
Stenotrophomonas maltophilia
A case of S. maltophilia infection in a
hemodialysis patient with a tunneled central
venous catheter which did not respond to
ceftazidime and ciprofloxacin. Long-term
daily locked-in therapy with ceftazidime was
able to save both the catheter and the
patient.
Catheter-related bacteremia was reported in
three hemodialysis patients that as
successfully treated by dialysis catheter
removal and antibiotic therapy. It is unclear
from the report whether the patients dialyse
in the same center.
in our scientific laboratory and this confirmed high aerobic
bacterial count from various check points. Immediate and
decisive actions were taken to flush, disinfect, and sterilize
the water system and to replace the valves of the reverse
osmosis outlet and reprocessing machine. Rigorous decon-
tamination and cleansing procedures were put in place to
minimize risks of cross-infection. We temporarily ceased
the use of reprocessing machines to recycle dialysis filters
because there were concerns of cross-infections and the
introduction of contaminated treated water during the rins-
ing procedure. In addition, we were also worried about
residual particulate biologic materials within dialysers that
may not have been removed completely despite rinsing and
disinfection. As we instigate the changes, there were no
reported cases of new infections.
DISCUSSION
Ralstonia pickettii is a nonfermenting Gram-negative bacilli
that is ubiquitous in the environment.15,16 The bacterium
is often found in moist hospital environment, particularly
from water sources including dental water supplies,17 hos-
pital water supplies,7,18 and industrial ultrapure/high
purity water.19–21 In addition, R. picketti has the propen-
sity to form and maintain biofilm in plastic industrial
water piping.22 The pathogen is now commonly recog-
nized and implicated in septicemia in immunocompro-
mised and debilitated hospitalized patients.18 Outbreaks
have occurred due to contaminated solutions causing
respiratory illnesses,23 endopthalmitis,12 otitis media,24
meningitis,25 prosthetic joint infections,26 and nonspecific
bacteremic symptoms.3,4,27

Ralstonia pickettii has also been described in patients with
renal failure. Wertheim and Markovitz28described a case of
osteomyelitis in a 71-year-old man suffering from chronic
kidney disease. Strateva et al.13 reports an incidental case of
R. picketti sepsis in a 75-year-old lady undergoing hemodial-
ysis in Bulgaria. A report from Uruguay documented two
cases of R. pickettii bacteremia in patients on chronic hemo-
dialysis linked to contamination of dialysis water.29
Stenotrophomonas maltophilia is another nonfermenting
Gram-negative bacterium that is of emerging importance as
a pathogen in dialysis units.30 Like R. picketti, it propagates
in moist environments (water and medical equipment) and
colonizes medical devices.31,32 Only a few studies have
described its colonization in dialysis units. Arvanitidou
et al.33 reported that S. maltophilia accounted for 13.5% of
treated water and dialysate sample isolates in a Greek
hemodialysis unit. Flaherty et al.34 and Bland et al.35
described S. maltophilia sepsis in patients from the use of
reprocessed high-flux membranes with contaminated
O-rings inside the dialyser. Most recently in 2017, Edens
et al.36 reported eight cases of S. maltophilia from three dif-
ferent dialysis clinics managed by the same dialysis organi-
zation. The article concluded that dialyser reuse and
reprocessing equipment contributed to the risk of infection.
There were also reports of multiorganisms infections that
feature S. maltophilia causing septicemia and pneumonia,
although it was difficult to ascertain which pathogen was
directly responsible for clinical infection.37 The same study
reported that 12 out of 18 patients with co-existing
S. maltophilia died from the infection. Table 2 showed a
summary of case reports of hemodialysis patients directly
affected by R. pickettii and S. maltophilia.
We hypothesize that this outbreak is due to colonization
of treated water, presumably through contamination via the
polluted filters and compounded by the usage of repro-
cessed dialysers in our center. In addition, there seems to be
a propensity of both organisms to cause prolonged febrile
reactions in patients with temporary dialysis catheters, likely
through the early development of biofilm. Intensification of
general sterilization procedures and servicing and replace-
ment of old decrepit components of the water system seems
to have halted the outbreak.
We believe that this is the first reported outbreak of
R. pickettii from a dialysis center. Previous case reports have
reported isolated cases of R. pickettii infection from different
dialysis centers.29 There were also reports of multiorganisms
outbreaks in hemodialysis patients, where S. maltophilia was
identified concurrently with other pathogens36,37 In our
case report, water from dialysis treatment plant has been
infected by the two pathogens and was transmitted to the
patients during the dialysis procedure. Vincenti et al. also
reported the co-existence of these two pathogens in water
Hemodialysis International 2019
Gram-negative bacteria outbreak in hemodialysis unit
sources (tap water and water used for hemodialysis and
bronchoscopy flushings) in a tertiary care hospital but there
were no direct consequence of infection to patients.1 Indeed
these organisms have many common features with other
more common opportunistic premise plumbing pathogens
like Legionella pneumophilia, Mycobacterium avium, and
Pseudomonas aeroginosa which exhibit characteristics like
disinfection resistant and growth in biofilms.43 The antibi-
otic resistance is primarily mediated through beta-lactamase
production, drug efflux pumps, and decreased permeabil-
ity.44,45 There are growing concerns regarding the evolving
resistance of the bacteria to new antimicrobial compounds
and it has been advocated that combination therapy may be
the solution to improving the long-term utility of new drugs
in the treatment of patients with NFGNB.46
We also believed that the practice of reusing and repro-
cessing dialysers may have contributed or compounded the
outbreak. An internal investigation of our practice reveals
that there was poor adherence to the standard operating
procedure (SOP) for reprocessing dialysers. In addition,
header caps of dialyser used in the center are nonremovable
and this makes the sterilization and cleaning process more
difficult than for those with removable caps, often needing
multiple rinsing cycles to remove biologic material. As a
result, we are working on audits to implement more rigor-
ous quality control especially in relation to the disinfection,
reprocessing and storage of dialysers. Even though there is a
routine practice of daily heat disinfection of the water sys-
tem and bi-monthly cultures and endotoxin testing, many
staff have not received proper training on handling of speci-
mens, interpretation of results and implementation of cor-
rective measures. We have instigated regular educational
sessions with doctors, nurses, and biomedical engineers to
familiarize them with SOP and protocols for sterilization of
water treatment and dialyser reprocessing systems. Special
attention and considerations were given to revision of pro-
tocol for dialyser reprocessing and references were particu-
larly made to the American National Standards Institute
(ANSI)/Advancing Safety in Medical Technology (AAAMI)
RD47 document on reuse of hemodialysers. Changes were
made specifically to record keeping, personnel training,
hemodialyser labeling, and storage and disposition of
rejected dialyzers.47
Early communication with our microbiologists had led to
rapid actions being taken to identify affected patients from
the hemodialysis center. Biomedical engineers and public
health doctors also played important roles in identifying
source of infection and implementing measures to investi-
gate and curtail the outbreak and hopefully, forestall future
infections. Current measures to control these pathogens
include manipulation of chemistry and microbiome of water,
employment of bio-film discouraging pipes (antimicrobial
5
K. Thet et al.
coated or impregnated) or pretreatment with disinfectant
and reduction of organic carbon.43 Simple and effective mea-
sures like raising temperature of flushing water and increas-
ing maintenance frequency of treatment facilities should
remain the mainstay for prevention of infections.
CONCLUSION
We hope to increase awareness of the pathogenicity and
virulence of NFGNB, particularly in patients with end
stage renal disease. Meticulous and vigilant monitoring of
isolates from culture specimens can help to identify an
outbreak. Adequate maintenance and repair of dialysis
water system and adherence to disinfection guidelines
can prevent accumulation of endotoxins and reduce like-
lihood of biofilm formation. Particular attention must be
given to adherence to SOP in reprocessing dialysers and
surveillance of water quality for endotoxins and bacterial
growth, especially as treated water is directly introduced
into the blood compartment of the dialysers during
reprocessing. Identification of unusual organisms like
NFGNB in dialysis patients requires prompt investigation
to locate source of infection, particularly in shared water
source in community or institutionalized facilities. Delay
in identification can lead to rapid outbreaks and fatal
outcomes. In light of its challenging resistance profile,
imperative actions must be taken to tackle infections at
the outset and prevent potentiation of resistance. More
studies are urgently needed to identify the best ways to
utilize existing antibiotic therapy to combat the up
growth of these proliferating infections.
ETHICS
Informed consent was obtained from the patients in this
case report.
Manuscript received July 2018; revised October 2018;
accepted November 2018.
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