Peritoneal Dialysis–Related Peritonitis: Atypical and

Resistant Organisms

Yeoungjee Cho, PhD,* and Dirk Gijsbert Struijk, PhD†

Summary: Peritoneal dialysis (PD)-related peritonitis remains to be one of the most frequent and serious
complications of PD. In this study, existing literature has been reviewed on PD peritonitis caused by atypical
organisms and antibiotic resistant organisms and their impact on patient outcomes. Although uncommon, delay
in recognition of PD peritonitis caused by atypical organisms can lead to poor patient outcomes if there is a delay
in diagnosis and implementation of appropriate treatment. There is also a large difference in prevalence of
antibiotic-resistant infections across the world with variable impact on reported patient-level outcomes.
Semin Nephrol 37:66-76 C 2017 Elsevier Inc. All rights reserved.
Keywords: Antibiotic resistance, atypical, peritoneal dialysis, peritonitis

R
epeated exposures to conventional peritoneal
dialysis (PD) solutions have been associated
with an impairment in host cell defense,1
reduction in peritoneal mesothelial cell viability,2 and
progressive peritoneal membrane injury.3 In conse-
quence, PD-related peritonitis is one of the most
frequent and serious complications of PD, which
directly contributes to approximately 20% of technique
failures4 and up to 6% of deaths.5,6 Reported rates of PD
peritonitis range widely from 0.06 to 1.66 episodes per
patient-year across different centers and countries.7 The
first part of this article reviews the peritonitis caused by
atypical organisms, with particular focus on risk factors,
presence of any variation in clinical presentations, and
diagnostic and treatment strategies. The second part
reviews the development of antibiotic resistance over
time and its impact on treatment outcomes.
is a group of fungi that grows readily in routine cultures).
Although they are rare, a delay in the diagnosis and
implementation of appropriate treatment can result in
adverse patient outcomes, including death.
PERITONITIS CAUSED BY MYCOBACTERIA
The genus Mycobacterium contains several species, many
of which have caused human illnesses. Mycobacterium
tuberculosis causes tuberculous disease and form M tuber-
culosis complex with three other closely related mycobac-
terial species (Mycobacterium bovis, Mycobacterium
africanum, and Mycobacterium microti) (Table 1). Myco-
bacteria other than those that make up the M tuberculosis
complex are called nontuberculous or atypical mycobac-
teria. Patients with end-stage renal disease have relative
defects in cell-mediated immunity,9 which may predispose
them to develop infections from these organisms.

PERITONITIS CAUSED BY ATYPICAL Tuberculous Peritonitis

MICROORGANISMS
The most common micro-organisms responsible for peri-
tonitis are aerobic bacteria, such as Staphylococcus aureus,
coagulase-negative Staphylococcus, and Pseudomonas aer-
uginosa.4 Culture-negative peritonitis accounts for up to
12% of all peritonitis episodes,8 which may be owing to
peritonitis caused by atypical organisms, including myco-
bacteria and fungi (other than the Candida species, which
*Department of Nephrology, University of Queensland at Princess
Alexandra Hospital, Brisbane, Australia.
†
Division of Nephrology, Department of Medicine, Academic
Medical Center and Dianet, Amsterdam, The Netherlands.
Financial disclosure and conflict of interest statements: none.
Address reprint requests to Yeoungjee Cho, PhD, Department of
Nephrology, Level 2, ARTS Building, Princess Alexandra Hospi-
tal, Ipswich Rd, Woolloongabba, Brisbane, QLD 4102 Australia.
E-mail: Yeoungjee.cho@health.qld.gov.au
0270-9295/ - see front matter
& 2017 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.semnephrol.2016.10.008
The risk of active tuberculosis is increased dramatically by
many factors that affect the innate and adaptive immune
systems,10 including older age, presence of diabetes
mellitus, and human immunodeficiency virus (HIV) infec-
tion11 (Table 2). Although the relative risk for developing
active tuberculosis in patients with end-stage renal disease
is 5 to 15 times greater than in the general population,12-16
the reported incidence of tuberculous peritonitis is low
(o3%),11 with a higher prevalence in Asian countries.17
The diagnosis is challenging and often delayed, with fewer
than half of all cases diagnosed before 6 weeks after the
initial presentation.11,17 For reasons that are unclear, the
classic finding of peritoneal fluid containing a predomi-
nance of lymphocytes with peritoneal tuberculosis (not
specifically related to PD) is uncommon in PD-associated
tuberculous peritonitis, in which neutrophils usually pre-
dominate (460% of cases).11,17,18 A case of eosinophilic
peritonitis caused by M tuberculosis also has been
observed.19 Timely diagnosis is compromised further by
extremely low sensitivity of a smear for acid-fast bacilli

66 Seminars in Nephrology, Vol 37, No 1, January 2017, pp 66–76

Peritonitis: atypical & resistant organisms 67

Table 1. List of Atypical Microorganisms Causing Peritoneal
Dialysis–Related Peritonitis
Group Species
Tuberculous Mycobacterium tuberculosis19,*
peritonitis
Atypical Mycobacterium abscessus37
mycobacterial Mycobacterium avium complex34
peritonitis Mycobacterium chelonae37
Mycobacterium fortuitum37
Mycobacterium gastri34
Mycobacterium gordonae34
Mycobacterium heckeshornense34
Mycobacterium kansasii34
Mycobacterium phlei102
Mycobacterium porcinum34
Mycobacterium rhodesiae34
Mycobacterium smegmatis34
Mycobacterium trivale34
Mycobacterium xenopi34
Fungal Aspergillus species (Aspergillus
peritonitis fumigatus, Aspergillus niger,
(non- Aspergillus thermomutatus)50,53,56
Candida) Bipolaris spicifera50
Cryptococcosis (Cryptococcosis
neoformans)50,103
Fusarium104
Histoplasma capsulatum50
Hormonema dematiodes50
Lecythophora mutabilis50
Mucormycosis (Rhizopus, Absidia,
Mucor, and other Zygomycetes)50
Paecilomyces species (Paecilomyces
variotii, Paecilomyces taitungiacus)50
Penicillium species50
Roseomonas gilardii50
Trichosporon species50
*Forms a tuberculosis complex with M bovis, M africanum, or M
microti.
(3% positive smear in culture-confirmed or pathologically
confirmed cases), and relatively low yield (30%) from
culture of peritoneal dialysate, which may take more than
4 weeks before results are known.20 The gold standard for
the diagnosis of tuberculous peritonitis is laparoscopy,
which has the best diagnostic yield (sensitivity, 84%-
100%), but is an invasive procedure that may not be
readily available.21 There are several newer, relatively
noninvasive tests and more rapid investigations that can
confirm M tuberculosis, including polymerase chain reac-
tion (PCR) assay,22 and measurement of adenosine deam-
inase (ADA) in the peritoneal dialysate.23 ADA is a purine-
degrading enzyme that catalyzes the deamination of
adenosine in an irreversible manner, which results in the
production of inosine. An increase in ADA activity has
been reported to relate to the intensity of stimulation and
the maturation state of the lymphocyte, owing to an
immune cellular response against M tuberculosis.24-26
Table 2. Risk Factors for Peritoneal Dialysis–Related Peritonitis
From Atypical Microorganisms
Type of Risk factors
organism
Tuberculous Compromise in innate and adaptive
peritonitis immune systems,10,11 including
Older age
Diabetes mellitus
HIV infection
End-stage renal disease
Residence in Asia17
Atypical Immunosuppression, including34-36
mycobacter- Autoimmune diseases (eg, systemic
ial peritonitis lupus erythematosus)
Diabetes mellitus
HIV infection
Bone marrow transplantation
History of frequent bacteria peritonitis11,36
History of concomitant bacterial/fungal
infections
Unknown number. Use of prophylactic
exit-site gentamicin cream37,38
Fungal Recent history of antibiotic use47,50,51
peritonitis Use of immunosuppressive therapy56,57
Immunosuppressive condition (eg, HIV
infection, multiple myeloma)53,58
Low adherence to antifungal
chemoprophylaxis59-63
ADA levels in body fluids can be measured rapidly, and
its level in ascitic fluid has been reported to be a sensitive
(0.93; 95% confidence interval, 0.89-0.95) test for the
diagnosis of tuberculous peritonitis based on a meta-
analysis.23 However, it is a nonspecific test and is
considered at best a useful screening test in high-risk
patients or in countries with a high incidence of tuber-
culosis.27 In contrast, PCR is a specific test to detect M
tuberculosis, which can be performed directly on the
obtained tissue samples. Uzunkoy et al22 also have reported
reliable diagnoses by performing PCR analyses on ascitic
fluid, with their outcomes similarly replicated by
others.28,29 Upon confirmation of diagnosis, timely initia-
tion of antituberculous therapy is necessary. Before decid-
ing on the regimen, the possibility of drug resistance should
be considered. Risk factors for drug-resistant tuberculosis
include a previous episode of tuberculosis, exposure to a
person with drug-resistant tuberculosis, and residence in an
area with a high prevalence of multidrug-resistant or
extensively drug-resistant organisms. Once drug regimen
is determined, its pharmacokinetics in relation to dialysis
also needs to be evaluated (eg, pyrazinamide is cleared by
dialysis and should be administered after hemodialysis).
The International Society for Peritoneal Dialysis guideline
recommends combination of four drugs: rifampicin, iso-
niazid, pyrazinamide, and ofloxacin.30 Treatment with
68
pyrazinamide and ofloxacin can be ceased after 3 months,
whereas rifampicin and isoniazid are continued for a total
of 12 to 18 months. The optimal duration of treatment of
multidrug-resistant tuberculous peritonitis is not defined
clearly and implementation of therapy in consultation with
local infectious diseases unit is recommended.
Nontuberculous Peritonitis: Atypical Mycobacteria
To date, more than 100 species of atypical mycobac-
teria have been described, which can be found in the
natural environment, including soil, dust, rivers, and
streams.31 Municipal water supplies and tap water can
harbor these organisms and potentially pose a threat to
exposed PD patients. These organisms are even found
in medical equipment, including disinfectant solutions
and hemodialysis fluids.32 The first reported case of
atypical mycobacteria peritonitis was in 1982,33 and
since then there have been more than 50 cases reported
in the literature.34 Unlike tuberculous peritonitis, atyp-
ical mycobacteria peritonitis has been reported pre-
dominantly in the United States (57.9%), followed by
Asia (26.3%) and Europe (10.5%).34 However, this
distributional difference may be a consequence of
publication bias or variations in accurate diagnoses
rather than a true regional disparity.34
The majority of reported cases of patients diagnosed
with atypical mycobacteria peritonitis have been those
who are immunosuppressed, including a history of
autoimmune diseases (eg, systemic lupus erythemato-
sus), or other immunosuppressive conditions such as
diabetes mellitus, HIV infection,34 and bone marrow
transplantation35 (Table 2). A frequent history of
bacterial peritonitis episodes (66.7%) or concomitant
bacterial/fungal infections in these patients has been
attributed to their immunosuppressed states. However,
exposure to multiple courses of broad-spectrum anti-
biotics for treatment of infections11,36 could have
promoted an overgrowth of nonsusceptible microor-
ganisms, such as atypical mycobacteria. In fact, several
studies have reported cases of atypical mycobacterial
exit-site infections and peritonitis in PD patients
receiving prophylactic exit-site gentamicin cream.37,38
Lo et al37 reported an almost 20-fold (2.71% versus
0.102%) greater incidence of atypical mycobacterial
infections in patients receiving topical gentamicin
cream compared with those who received alternative
exit-site care. Although these results are alarming,
this outcome was based on retrospective observational
data, which was at risk of indication bias and residual
confounding. Furthermore, previous double-blind,
randomized, controlled trial of 133 PD patients comparing
topical mupirocin against gentamicin cream over a 12-
month follow-up duration did not observe any episodes of
atypical mycobacteria peritonitis or significant differences
in culture-negative peritonitis incidence (P ¼ .71).39
Y. Cho and D.G. Struijk
Similar to tuberculous peritonitis, the time from
initial presentation to diagnosis and initiation of
appropriate treatment is long and averages 4 weeks.34
The presenting features are indistinguishable from
other causes of peritonitis.11,17 Timely diagnosis again
is challenged by frequent occurrence of smear-negative
diseases (33.3%).34 Furthermore, the smear results will
not distinguish between M tuberculosis and atypical
mycobacteria. Therefore, if there is a suspicion of
atypical mycobacteria peritonitis (ie, in culture-
negative peritonitis with failing empiric antibacterial
therapy, especially in patients with additional risk
factors of immunosuppression), the treating physician
should consider performing additional investigations
with more rapid detection capability, such as commer-
cial DNA probes, high-performance liquid chromato-
graphy, DNA sequencing, or PCR restriction endonu-
clease assay.40,41 The optimal treatment regimen or
duration has not been defined clearly. In general, a
prolonged course of antibiotics is required, and the
majority of reported cases have required a treatment
duration longer than 1 month in 93.7% of patients.34
The choice of therapy should be in accordance to
antimicrobial susceptibility testing and patient
response. Similar to the treatment of tuberculous
peritonitis, the majority of reported cases of atypical
mycobacteria peritonitis have required removal of the
PD catheter as part of treatment (92.9%), with an
85.7% reported recovery rate.34
FUNGAL PERITONITIS
Fungal peritonitis accounts for 1% to 15% of perito-
nitis episodes,42-45 and is a serious complication
associated with significant morbidity and up to a
50% mortality rate.45-49 One of the contributors to
poor outcomes from fungal peritonitis has been a delay
in the time to diagnosis, which is particularly relevant
for non-Candida species (accounts for  10% of
fungal peritonitis), such as Aspergillus, Cryptococco-
sis, and Mucormycosis,50 which are not detectable
using the Gram stain of smears from the peritoneal
dialysate.44-49,51,52 Recognition of fungal peritonitis is
hindered further by comparable presenting clinical
features with that of bacterial peritonitis.47,49-51 Some
cases of fungal peritonitis may show predominance of
lymphocytes and/or mononuclear cells in the peritoneal
dialysate, which should flag the possibility of its
diagnosis. Some cases in which culture results
remained negative or were delayed have used newer
molecular techniques successfully, such as PCR53 and
18S ribosomal RNA gene sequencing,54 to confirm
diagnosis. These investigations certainly are not part of
routine clinical practice, but should be considered in
patients who are not responding to empiric treatment,
Peritonitis: atypical & resistant organisms
especially in the presence of risk factors for fungal
peritonitis (Table 2).
One of the recognized risk factors includes a recent
history of antibiotic use, especially in the context of
bacterial peritonitis. Wang et al51 conducted one of the
largest case series of fungal peritonitis to date (n ¼ 70),
in which antibiotic use within the preceding 3 months
was noted in 94% of the patients with fungal peritonitis
(compared with 61% with de novo fungal peritonitis).
It has been postulated that antibiotics may destroy the
normal skin and bowel flora and allow fungal prolif-
eration and overgrowth, leading to an environment
conducive to fungal colonization and infection.47,50 In
bacterial peritonitis episodes, gram-negative or poly-
microbial peritonitis episodes have been associated
with a greater risk of subsequent fungal peritonitis
(22% and 42.1%, respectively, compared with 4.7%
after gram-positive and 5.8% after culture-negative
peritonitis; P o .0001).55 Other risk factors include
the use of immunosuppressive therapy (eg, eculizumab
for treatment of atypical hemolytic uremic syn-
drome),56,57 HIV infection,58 and underlying diseases
such as multiple myeloma).53 As soon as the diagnosis
is confirmed, the PD catheter should be removed30 and
antifungal treatment should be commenced. Failure to
remove the catheter has been associated with a greater
mortality risk (31% versus 91%; P ¼ .0006).51
Although the overall probability of the patient’s ability
to resume PD after the catheter removal after fungal
peritonitis is low, patients with early catheter removal
are more likely to resume PD (68%)52 compared with
patients with a catheter left in situ.51 There is no
uniform recommendation with regard to drug selection
or doses and combinations of antifungal therapy.30
Choice of therapy is based on case series, anecdotal
reports, and opinions. In general, a combination
amphotericin B and flucytosine or fluconazole is
recommended for non-Candida species until the sus-
ceptibility results are known.50 Other treatment options
include an echinocandin (eg, caspofungin), flucona-
zole, posaconzaole, or voriconazole instead of ampho-
tericin B. Therapy should be continued for at least 10
days after catheter removal, but typically is continued
for 4 to 6 weeks in the majority of cases.50 There is no
consensus on the timing of catheter reinsertion after an
episode of fungal peritonitis. Given the adverse out-
comes associated with an episode of fungal peritonitis,
including higher rates of hospitalization, catheter
removal, transfer to hemodialysis, and death, the
prevention should take precedence.42 Although there
are conflicting outcomes on the use of antifungal
prophylaxis largely based on observational studies,59-
62
a randomized controlled trial conducted by Lo et al63
comparing nystatin tablets with a placebo during
the antibiotic treatment showed a reduction in
the incidence of Candida peritonitis with use of
69
chemoprophylaxis (1.39 versus 3.19 episodes/100 peri-
tonitis episodes).
In summary, PD peritonitis caused by atypical
organisms is uncommon, but important to consider
because a delay in diagnosis and implementation of
appropriate treatment can lead to poor patient out-
comes. Until we develop diagnostic strategies that
reliably can identify PD peritonitis caused by atypical
microorganisms, one needs to remain vigilant,
especially in patients with risk factors for atypical PD
peritonitis, including recent exposure to antimicrobial
treatment for infections that may or may not be
related to PD.
DEVELOPMENT OF ANTIMICROBIAL RESISTANCE
OVER TIME IN THE PD POPULATION
Antibiotics are essential in the treatment of infectious
diseases. However, their abundant use in medicine as
well as their widespread abuse outside human medicine
has resulted in the development of (multi)drug resist-
ance. The frequency of resistance varies between
countries, but overall still is increasing according to
the European Centre For Disease Prevention and
Control website (available: www.ecdc.europe.eu).
European data can be obtained from the database on
the same website, data on resistance in the United
States can be obtained from the Centers For Disease
Control and Prevention website (available: www.cdc.
gov/narms/). Unfortunately, when high resistance has
been established in a community, it is unlikely to be
reduced by restrictive use policies.64 The development
of resistance limits the treatment options, increases the
risk of treatment failure, and imposes an extra health
care cost burden and productivity loss.64
The development of resistance is dependent on the
exposure of the microorganism to the drug. Only a few
studies in PD patients have analyzed time frames
longer than 10 years. That the time period is important
can be shown by the data from a single center, where
the first report over a 6-year time frame showed no
increase in resistance, whereas during a longer period
diminished antibiotic susceptibility rates over time
were found.65,66
In this second part of the review we focus on the
development of antibiotic resistance in the adult PD
population and its impact on the outcomes of perito-
nitis episodes. With Australia and New Zealand as
exceptions, almost all available data were derived from
retrospective single-center studies. Case histories were
not included in this review.
As mentioned earlier, both place and time frame of
the study are essential in the interpretation of the data
on the development of antibiotic resistance. Therefore,
in the description of the published results, both country
70 Y. Cho and D.G. Struijk

of origin and time frame of the study are always given.
When possible, the number of included patients also
was noted. Furthermore, the studies were divided into
those that provided data on all microorganisms
observed during the study period and those that
analyzed only individual microorganisms or subgroups
of microorganisms. This approach was chosen to
reduce overlap in the text.
First, the data on the development of antibiotic
resistance over time is discussed. Some, but not all,
microorganisms listed in Table 3 are reviewed. Then,
the impact on resistance of antibiotic-containing exit-site
creams is described. Finally, the impact of antimicrobial
resistance in the outcomes of the treatment per micro-
organism is reviewed, followed by a brief summary.
Studies With Data Not Restricted to a Single
Microorganism
In The Netherlands (1979-2010; 2,234 episodes), 731
patients were treated at a university hospital.66 Only
few data were provided on antibiotic resistance. No
changes in the resistance of S aureus to flucloxacillin
were observed and only a modest increase in cefradine
(and thus methicillin) resistance by coagulase-negative
Staphylococcus (CNS) was observed (from 0.8% to
5.8%). Resistance of Pseudomonas to aminoglycosides
also remained stable. In Germany (1979-2014; 487
episodes), extensive data were provided on the sensi-
tivity to various antibiotics.67 Although over time some
methicillin-resistant S aureus as well as vancomycin-
resistant enterococci were detected, these findings were
not significant. In Staphylococcus epidermidis, methi-
cillin resistance increased from 5% to 19%. In gram-
positive organisms cefazolin susceptibility decreased
over time from 93% to 58%. Although third-gener-
ation, cephalosporin-resistant, gram-negative rods
appeared only recently, this finding was not significant.
In Canada (1991-1998; 546 episodes) S epidermidis
resistance developed to ciprofloxacin (5%-48%) and
oxacillin (19%-74%).68 In the other microorganisms,
higher but stable resistance rates were observed only in
Escherichia coli for ampicillin (36%) and piperacillin
(31%). In Brazil (1995-2009; 402 episodes), an
increase in the resistance of oxacillin-resistant CNS
(26%-44%) and amikacin-resistant, nonfermentive,
gram-negative bacilli (26.9%-40%).69 In Turkey
(2000-2006; 620 episodes), the percentage of
methicillin-resistant CNS increased from 5% to
13%.70 The percentage of extended-spectrum β-lacta-
mase (ESBL)-producing E coli was constant over time
and on average 19%. In India (2002-2011; 303

Table 3. Simplified Classification of Microorganisms Initially Based on Gram Stain

Division Group Family Species
Gram positive Cocci Staphylococcaceae Coagulase positive
Staphylococcus aureus
Coagulase negative
Staphylococcus epidermidis
Staphylococcus saprophyticus

Streptococcaceae Streptococcus pyogenes

Streptococcus pneumoniae
Streptococcus faecalis
Enterococcaceae Enterococcus faecalis
Enterococcus faecum
Rods Corynebacterium Corynebacterium dipheriae
Bacillaceae Bacillus antracis
Gram negative Cocci Neisseriaceae Neisseria gonorrhea
Rods Enterobacteraceae Lactose fermenters
Escherichia coli
Citrobacter freundii
Enterobacter aerogenes
Klebsiella pneumoniae
Lactose nonfermenters
Proteus mirabilis
Serratia marcescens

Pseudomonadaceae Pseudomonas aeruginosa

Moraxellaceae Acinetobacter baumannii
Bacteriodaceae Bacteroides fragilis
Peritonitis: atypical & resistant organisms
episodes), methicillin resistance for S aureus and CNS
was 29% and 21%, respectively.71 Resistance to
vancomycin existed in 15% of the enterococci. Fifty-
five percent of the Enterobacteriacea species were
resistant to third-generation cephalosporins, and all of
them were ESBL producers. Nonfermentive, gram-
negative bacilli had an even higher resistance to
third-generation cephalosporins. In Korea (1992-
2001; 1,108 episodes), methicillin resistance in CNS
increased from 18% to 42%, although it remained
stable with 35% in S aureus.72 The incidence of
vancomycin-resistant enterococci was low (8%), but
all Enterococcus faecalis strains were resistant to
ampicillin. In Argentina (1991-2005; 96 episodes),
methicillin resistance occurred in 38% of all Staph-
ylococcus isolates, mostly in CNS.73 Resistance to
gram-negative bacteria was low, and vancomycin
resistance was not observed. In Spain (1988-2007;
832 episodes), the overall incidence of peritonitis with
methicillin-resistant S aureus and ESBL-producing E
coli was low.74 Vancomycin resistance was not
observed. Ciprofloxacin resistance, which was given
as the initial treatment, remained low, except for an
increase in CNS (13%-30%). Strains resistant to
ciprofloxacin also more frequently were resistant to
amoxicillin-clavulanic acid, cefotaxime, ceftazidime,
imipenem/cilastin, and gentamicin. The proportion of
gram-positive bacteria resistant to cefazolin increased
over time from 24% to 49%. In Western Australia
(2008-2013; 1,319 episodes, multicenter), methicillin
resistance in S aureus and CNS remained low (2% and
18%), as well as the resistance to gentamicin and
vancomycin (8% and 2%), the combination that was
chosen as the initial antibiotic treatment.75 Multidrug
resistance (isolate with resistance to at least one
agent in three or more categories of antimicrobial
agents) occurred in 37% of all isolates, 71% of these
strains were gram negative and 29% were gram
positive. In Portugal (1985-2010; 588 episodes),
overall methicillin resistance in S epidermidis (7%)
and S aureus (2%) was low.76 Vancomycin resistance
was not found. In India (2006-2008; 90 episodes),
a high degree of resistance to third-generation
cephalosporins was found in Enterobacteriaceae
(73%) and other gram-negative bacilli (57%).77
No vancomycin resistance for gram-positive cocci
was found.
STUDIES FOCUSED ON A SINGLE SPECIES
S aureus
In China (1994-2005; 245 episodes), methicillin resist-
ance was approximately 18%.78 In Brazil (1996-2010;
62 episodes), oxacillin resistance was approximately
11% and stable over time.79 In Australia (2003-2006;
71
936 episodes, multicenter study), methicillin resistance
was approximately 22%.80
Coagulase-Negative Staphylococci
In Canada (1993-1999; 93 episodes); methicillin resist-
ance increased over time and overall was 68%.81 In
Brazil (1994-2011; 115 episodes), oxacillin resistance
was found in 70%, with a trend over time to increase
(63% to 71%).82 In England (1988-1991), the intro-
duction of ciprofloxacin resulted in an increase in
ciprofloxacin-resistant carriers from 0% to 33%.83
Thirty-eight percent of these carriers became infected
with these resistant strains. In China (1995-2006; 232
episodes), methicillin resistance remained stable during
the study period at approximately 50%.84 In Australia
(2003-2006; 355 episodes), methicillin resistance was
approximately 68%.85
Enterococci
In the United States (1993-1996; 24 episodes), vanco-
mycin resistance was found in 37.5% of the peritonitis
episodes.86 In China (1995-2009, 210 episodes), the
ampicillin resistance in episodes with a single organ-
ism was 42%.87 High-level gentamicin resistance and
streptomycin resistance was found in 21% and 14%,
respectively. Vancomycin resistance was not seen.
Enterobacteriacae
In China (1995-2006), a gradual increase in antibiotic
resistance to commonly used antibiotics (cephalotin,
ampicillin, and cefuroxime) was seen over the years.88
Recent antibiotic treatment was associated with resist-
ance to cefotaxime (57.1%), ceftazidime (75.0%),
cefoperazone/sulbactam (66.7%), and piperacillin/tazo-
bactam (80.0%). In another center in China (1994-
2003), on average 13% of the episodes of E coli
peritonitis were caused by ESBL-producing E coli.89
The resistance increased over time from approximately
10% to 20%. In Brazil (1998-2007; 95 episodes), a low
resistance to gentamicin, ceftazodime, cefepime,
oxfloxacin, and imipenem (o5%) was found, which
also remained stable over time.90 Nonfermentive gram-
negative bacilli on the other hand had a higher
resistance to these bacteria, with a significant increase
over time for cefepime (33.1% versus 62.0%). In China
(2006-2011; 90 episodes) ESBL E coli was found in
36% of all strains and fluctuated over the years.91
These strains remained highly sensitive to carbape-
nems, furadantin, amikacin, cefmetazole, and cefoper-
azone/sulbactam. However, a high proportion of
these isolates were resistant to ampicillin, cefazolin,
and ceftazidime, and together with cefepime showed
an increase in resistance over time. In Taiwan
72
(1990-2010; 11 episodes), all Citrobacter isolates were
susceptible to ceftazidime, cefepime, carbapenem, and
aminoglycosides, but 64% were resistant to ampicillin,
55% were resistant to cefazolin, and 27% were
resistant to cefmetazole.92
Other Gram-Negative Microorganisms
In Taiwan (1985-2012; 26 episodes), all isolates of
Acinetobacter species were susceptible to cefepime,
fluoroquinolones, and aminoglycosides, with a low
ceftazidime-resistance rate (16%).93
ANAEROBIC MICROORGANISMS
In Taiwan (1990-2010; 328 patients), only 10 episodes
of peritonitis were encountered. Penicillin resistance
was found in 40%, and ampicillin/sulbactam resistance
in 20%.94 All strains were susceptible to clindamycin
and metronidazole.
DEVELOPMENT OF MUPIROCIN/GENTAMICIN
RESISTANCE
In Spain (1990–2008; 155 patients and 62 dialysis
partners), the sensitivity of S aureus to mupirocin
significantly decreased over time.95 Mupirocin resist-
ance resulted in a higher incidence of exit-site infec-
tions. In the United States (1991-2000 and 2004-2013;
444 patients), during the first time period the prophy-
lactic strategy consisted of treatment in case of nasal
carriers of S aureus with rifampicin orally, cyclic oral
rifampicin, or daily mupirocin on the exit site.96
During the second time period, gentamicin cream
was applied in all patients. In both periods only 3
gentamicin-resistant infections occurred. In Canada
(2001; 149 patients with three swabs: anterior nares,
axilla/inguinal areas, and exit site), patients using
mupirocin prophylaxis were analyzed.97 After 4 years
of mupirocin use, mupirocin-resistant S aureus
appeared in 3%, whereas methicillin resistance disap-
peared in S aureus (8% to 0%). In Canada (2003-2004;
147 patients); 16 S aureus carriers were identified.
In 4 patients (25%), mupirocin resistance was
found, whereas methicillin resistance occurred in
2 patients (13%).98 Compared with their previous
study 3 years earlier, no changes were found
in the prevalence of mupirocin resistance. In the
United States (2004-2006 and 2007-2009; 377
patients), no significant differences were found
between two periods in which mupirocin cream
(first period) and gentamicin cream (second period)
were used in the prevalence of resistance to gentamicin
for S aureus, CNS, Pseudomonas species, and
Enterobacteriaceae.99
Y. Cho and D.G. Struijk
In Spain (2009-2011; unknown number of
patients), no increase in the resistance to microorgan-
isms was seen with the exception of S epidermidis in
2009 and 2010.100 In Turkey (unknown time frame;
36 patients), during a mean follow-up period of
2.2 years, mupirocin resistance was investigated using
swabs (anterior nares, axilla/inguinal areas, and
exit site).101 In CNS isolates, mupirocin resistance
was found in 66% and methicillin resistance was
found in 39%. None of the S aureus isolates showed
methicillin resistance and only one (1%) showed
mupirocin resistance.
TREATMENT OUTCOME
The impact of antibiotic resistance on parameters of
treatment outcome is provided in this section. Because
the treatment itself in most publications was based on
the antibiotic susceptibility data and the clinical
response, the individual treatment strategies are not
included in the review.
Studies With Data Not Restricted to a Single
Microorganism
In The Netherlands, resistance to cefradine resulted in a
3-day longer treatment time.66 In Brazil, oxacillin
resistance was an independent predictor of resolu-
tion.69 In India, mortality was significantly higher in
peritonitis as a result of VRS, and ESBL and metallo-
β-lactamase producers.71 In Korea, episodes with
methicillin-resistant CNS showed a higher catheter
removal rate (8.2% versus 1.0%).72 In Spain, resistance
to ciprofloxacin for both gram-positive and gram-
negative infections was a strong marker of poor out-
come.74 This held true for hospital admissions (61%
versus 5%), relapse (31% versus 12%), re-infection
(11% versus 3%), catheter removal (32% versus 7%),
PD dropout (7% versus 2%), and death (18%
versus 2%).
S aureus
In Australia, methicillin-resistant peritonitis episodes
generally were more severe in terms of frequency and
duration of hospitalization, higher rate of catheter loss,
permanent HD transfer, and death.85 In China,
methicillin-resistant peritonitis episodes had a lower
primary response rate (64.4% versus 93.0%) and
complete cure rate (60.0% versus 77.5%).78 Adjuvant
rifampicin treatment was associated with a lower rate
for relapse or repeat peritonitis (21.4% versus 42.8%).
In Brazil, no correlation was found between resistance
and outcome.79
Peritonitis: atypical & resistant organisms
Coagulase-Negative Staphylococci
In Canada, the occurrence of resistance did not
influence patient outcome.81 Also in China, resistance
did not influence outcome.84 In Brazil, oxacillin
resistance was an independent predictor of poor reso-
lution owing to a high rate of catheter removal (21%)
and relapse (18%).82
Enterococcus
In a single-center study in the United States,
vancomycin-resistant peritonitis resulted in high mor-
bidity and mortality rates because the catheter had to
be removed in 6 of 9 patients and death occurred in
5 of these 9 patients.86 In China, ampicillin resistance
was not associated with a worse outcome.87
Enterobacteriacae
In China, recent antibiotic resistance and a lower
treatment response rate was associated with previous
antibiotic use (49.3% versus 62.8%).88 In 39.0% of the
peritonitis episodes the peritonitis did not respond to
single-antibiotic treatment despite sensitivity in vitro.
In a second center in China more cases in the ESBL E
coli group developed treatment failure (45.5% versus
13.0%) and died of sepsis (27.3% versus 3.9%).89
However, in another center in China, no relation was
found between the presence of ESBL E coli and
outcome.91 In a study in Taiwan, peritonitis episodes
caused by Citrobacter species, the relapse rate (9%
versus 0%), mortality rate (18% versus 7%), and
technique failure (89% versus 59%) were worse
compared with other Enterobacteriaceae peritonitis
episodes.92
SUMMARY
After reviewing the data in the literature on the
presence and development over time of antibiotic
Figure 1. Methicillin resistance (%) in coagulase-negative
Staphylococci in various countries, combined with the year of
the last reported data.
73
resistance in microorganisms, it is obvious that large
differences exist between the various countries
throughout the world. This is shown Figure 1, which
summarizes the data on methicillin-resistant CNS. In
addition, the impact of resistance of microorganisms
differs between the various publications. Some studies
reported no effects on outcome, whereas other studies
reported that it negatively influenced treatment dura-
tion, hospitalization rate, catheter removal rate, and
death. Treatment advice in case of an infection with
resistant microorganisms in the reviewed literature was
based mostly on antibiotic susceptibility testing and
clinical response.
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