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REVIEW ARTICLE
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Abstract
The Candida parapsilosis family has emerged as a major opportunistic and nosocomial pathogen. It causes
multifaceted pathology in immuno-compromised and normal hosts, notably low birth weight neonates.
Its emergence may relate to an ability to colonize the skin, proliferate in glucose-containing solutions, and
adhere to plastic. When clusters appear, determination of genetic relatedness among strains and identification of a common source are important. Its virulence appears associated with a capacity to produce biofilm
and production of phospholipase and aspartyl protease. Further investigations of the host-pathogen interactions are needed. This review summarizes basic science, clinical and experimental information about
C. parapsilosis.
Keywords: Candida parapsilosis, epidermiology, strain differentiation, clinical aspects, pathogenesis,
antifungal susceptibility
Introduction
Candida bloodstream infections (BSI) remain an
exceedingly common life-threatening fungal disease
and are now recognized as a major cause of hospitalacquired infection (Douglas 2003; Tortorano etal. 2006;
Tortorano etal. 2004). It is now the fourth most common
organism recovered from blood cultures among hospitalized patients in the USA (Hobson 2003; Pfaller etal.
1998b, Rangel-Frausto etal. 1999; Schaberg etal. 1991).
Some years ago Candida albicans accounted for
7080% of the Candida isolates recovered from infected
patients (Banerjee et al. 1991; Beck-Sague & Jarvis
1993; Fidel et al. 1999). However, infections due to
non-albicans species have emerged over the past two
decades, and a shift from C. albicans to species such as
Candida glabrata, Candida parapsilosis, and Candida
tropicalis has occurred (Fidel et al. 1999; San Miguel
et al. 2005). C. parapsilosis is now the second or third
most common cause of candidiasis, behind C. albicans.
Address for Correspondence: Karl V. Clemons, Ph.D., Division of Infectious Diseases, Santa Clara Valley Medical Center, 751 South Bascom Ave., San Jose,
CA 95128. Tel: (408) 9984557, Fax: (408) 9982723. E-mail:clemons@cimr.org
(Received 17 March 2009; revised 23 June 2009; accepted 02 July 2009)
ISSN 1040-841X print/ISSN 1549-7828 online 2009 Informa UK Ltd
DOI: 10.3109/10408410903213393
http://www.informahealthcare.com/mby
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Epidemiology
C. parapsilosis is a ubiquitous microorganism in the
natural environment. It is not only isolated easily from
soil, seawater, and plants, but also can be isolated from
mucosal surfaces, skin and nails, where it belongs to the
benign commensal flora of humans and mammals (De
Bernardis etal. 1999; Kuhn etal. 2004; Sanchez etal. 1993;
Weems 1992). The epidemiology of C. parapsilosis in the
hospital environment is unique among Candida species,
because it is frequently isolated from physical surfaces.
It is a frequent cause of opportunistic infection, associated with high morbidity and mortality rates in hospitalized immuno-compromised patients (Girmenia etal.
1996; Jarvis 1995). Although C. parapsilosis is an opportunistic pathogen, the majority of patients who develop
disseminated candidiasis due to C. parapsilosis are not
immunosuppressed in the classical sense (Spellberg &
Edwards 2002). Rather, the predominant risk factors for
disseminated candidiasis due to C. parapsilosis, which
are held in common among afflicted patients, are iatrogenic and/or nosocomial factors (Spellberg etal. 2006).
This species has been particularly associated with BSI
in very low birth weight neonates (Campbell etal. 2000;
da Silva etal. 2001; Damjanovic etal. 1993; Huang etal.
1998; Huang etal. 1999; Sarvikivi etal. 2005; Saxen etal.
1995; Solomon etal. 1986; Welbel etal. 1996), but is also
seen frequently in patients with catheter-associated
candidemia and/or with intravenous hyperalimentation
(Cano et al. 2005; Huang et al. 2004; Levin et al. 1998;
Levy etal. 1998; Marais etal. 2004).
Although C. albicans continues to predominate,
several surveillance programs report the emergence
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Clinical aspects
C. parapsilosis is an important opportunistic pathogen
that causes infections ranging from thrush to invasive
disease such as fungemia, endocarditis, endophthalmitis, arthritis, and peritonitis, all of which usually occur
in association with invasive procedures or prosthetic
devices. We will describe only the most frequent infections caused by C. parapsilosis.
Superficial Infections
Frequent isolation of C. parapsilosis from pathological
lesions of nails and skin, with a distal subungual type
of onychomycosis often occurs with this organism (De
Bernardis etal. 1999; Figueiredo etal. 2007; Mujica etal.
2004; Pfaller et al. 1995; Segal et al. 2000; Strausbaugh
et al. 1994). Risk factors significantly associated with
colonization in patients are prolonged antibiotic
therapy, parenteral nutrition, duration of stay in the
hospital, surgery, indwelling devices, diabetes, obesity, malignancy, elderly, and neonates of very low birth
weight (Bendel 2003; Dorko etal. 2005; Figueiredo etal.
2007; Jautova etal. 2001).
C. parapsilosis is second to C. albicans as the most
common Candida causing onychomycosis (Brilhante
et al. 2005; Dorko et al. 2002a; Khosravi & Mansouri
2001). However, some studies observed an even higher
prevalence of onychomycosis caused by C. parapsilosis. Segal et al. (2000) reported a high prevalence of
C. parapsilosis among onychomycosis patients obtained
from two different centers in Israel. C. parapsilosis was
the predominant Candida species, recovered from both
fingernail and toenail infections (Segal et al. 2000).
Figueiredo etal. (2007) reported 41% of the 200 samples
recovered from fingernails of Candida species were
C. parapsilosis, which is in agreement with RodriguesSoto et al. (1993), who identified C. parapsilosis as
the prevalent species in onychomycosis involving the
fingernails. In addition, Oliveira et al. (2006) reported
C. parapsilosis as the Candida species most frequently
isolated from onychomycosis lesions. Recently, in a
study among Algerian military personnel, C. parapsilosis
was the predominant yeast species causing both superficial fungal infection and onychomycosis of the foot
(Djeridane et al. 2006; Djeridane et al. 2007). In addition, C. parapsilosis was the most common yeast causing
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two decades fungal endocarditis has increased in incidence, carrying with it a high risk of mortality (Garzoni
etal. 2007; Lopez-Ciudad etal. 2006); this is one of the
most serious manifestations of candidiasis. A long duration of illness has been reported in patients suffering
non-albicans endocarditis, so prolonged treatment is
required to avoid grave consequences (Khan etal. 2007).
Among yeast-related endocarditis, C. parapsilosis is the
most important non-albicans species isolated (Garzoni
etal. 2007; Khan etal. 2007).
Clusters of cases involving prosthetic valves have
been reported (Diekema et al. 1997). Garzoni et al.
(2007) described intraoperative contamination (e.g.
cardiac bypass equipment, tears in surgical gloves) to
be the most common source of infection in outbreaks of
C. parapsilosis infective endocarditis (Diekema et al.
1997; Johnston et al. 1994). The most prevalent predisposing factors for fungal endocarditis caused by
C. parapsilosis are prosthetic valves, then, in this order,
intravenous drug use, parenteral nutrition, antibiotic
therapy, preexisting valvular heart disease, prior episode of endocarditis and reconstructive cardiovascular
surgery (Brandstetter & Brause 1980; Garzoni etal. 2007;
Khan etal. 2007; Rubinstein etal. 1975; San Miguel etal.
2006; Tonomo etal. 2004; Weems 1992). Abdominal surgery and immunosuppression have also been described
as risk factors. The aortic valve is the first, and mitral valve
the second, most commonly involved valve in infection
of native valves (Garzoni etal. 2007; Weems 1992), with
intravenous drug use the most common predisposing
factor (Garzoni etal. 2007). The overall mortality of these
patients was high (42%). Among those treated with conventional antifungals and adjunctive surgery, mortality
was lower (Johnston etal. 1994). Peripheral embolic and
hemorrhagic events are the most common complications (44%) of C. parapsilosis endocarditis (Garzoni etal.
2007).
Peritonitis
Fungal peritonitis is an uncommon but potentially lifethreatening complication of continuous ambulatory
peritoneal dialysis (CAPD) (Amici etal. 1994; Bren 1998;
Chen etal. 2004; Chen etal. 2006; Johnson etal. 1985;
Kaitwatcharachai 2002). C. parapsilosis has become the
most prevalent pathogen of fungal peritonitis (Chen
etal. 2006). This organism, which is a common skin and
subungual colonizer, has the ability, in high glucose
concentrations, to adhere easily to prosthetic material
by extensive biofilm formation on the surface of the
plastic catheter. The high glucose content of dialysate,
and catheter implantation in peritoneal dialysis patients
causes this high prevalence of fungal peritonitis caused
by C. parapsilosis (Chen etal. 2006). The mechanism of C.
parapsilosis infections is considered to be transmission
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albicans the most frequent subspecies (30%). C. parapsilosis accounted for 21% of all Candida endophthalmitis infections.
A few cases of keratitis have been reported, with risk
factors such as corticosteroid use, corneal transplantation and laser in situ keratomileusis (LASIK) (Bourcier
et al. 2003; Muallem et al. 2003; Solomon et al. 2004).
Since treatment, such as surgery and antifungal therapy,
can save vision, evidence of intraocular infection should
be recognized as early as possible (Feman etal. 2002).
Joint diseases
Candida arthritis is most commonly seen among intravenous drug users (Vasquez et al. 2002). Nosocomial
C. parapsilosis arthritis has been reported in only a few
cases, involving the knee, shoulder and wrist (De Clerck
et al. 1988; Diekema et al. 1997; Legout et al. 2006;
Salo et al. 1990; Smith et al. 1987; Vasquez et al. 2002;
Yarchoan et al. 1979) Arthritis caused by C. parapsilosis is associated with joint prostheses, probably due to
the increased ability of this micro-organism to adhere
to plastic (Brooks & Pupparo 1998; Cushing & Fulgenzi
1997; Hennessy 1996; Wada et al. 1998). Arthritis, produced by C. parapsilosis, can result through direct inoculation of the fungus at arthrocentesis and is sporadic
in older individuals (Cuende et al. 1993). Risk factors
for these sporadic incidents include diabetes mellitus,
intravenous drug use, and immunosuppression (Cuende
etal. 1993).
Pancreatitis
There are a growing number of reports of pancreatic
infections due to Candida species, most commonly
C. albicans, mainly with previous abdominal manipulation, such as previous pancreatic drainage procedures
(percutaneous or surgical) (Robbins etal. 1996). Fungal
pancreatitis due to non-albicans species has increased
in incidence and is attributed to several factors, such
as the use of broad-spectrum antibiotics, parenteral
nutrition as well as the increase in use of immunosuppressive agents (Robbins etal. 1996). Only a few cases of
pancreatic infections (infected pancreatic necrosis and
pancreatic abscesses) due to C. parapsilosis have been
described (Ibanez & Serrano-Heranz 1999; Kull et al.
1999; Gautret etal. 1998).
Meningitis
Up to 1992, in the review article by Weems (1992) one
case of meningitis caused by C. parapsilosis was reported
(Faix 1983). Several cases of meningitis caused by this
organism have since been described, especially among
neonates (Dorko et al. 2002b; Huttova et al. 1998b).
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Pathogenesis
Although very little on this subject has been studied,
in this section we will discuss what is currently known
about virulence factors of C. parapsilosis and host
defense against this organism.
Virulence
C. parapsilosis accounts for a significant proportion of
nosocomial infections, with an increasing prevalence.
As with other Candida species, invasion of C. parapsilosis can result in severe disease, particularly in hosts with
a suppressed immune system. For the development of
more effective containment measures it is necessary to
understand the mechanisms that underlie pathogenicity. The lack of knowledge of virulence factors that play
a role in the pathogenicity of C. parapsilosis may in part
be due to the exclusive use of type-collection strains in
most experiments (Cassone etal. 1995). The paucity of
data on clinical isolates needs to be corrected.
We suspect that the lower virulence of C. parapsilosis
compared to C. albicans and some other non-albicans
Candida species is a reason for the lower mortality and
morbidity rates observed in adults and neonates (Faix
1992; Sullivan et al. 1995; Weems 1992). Comparing
C. parapsilosis with C. albicans has made it possible to
define some putative virulence factors. These virulence
factors, present in both species, include adherence to
epithelial and endothelial cells, proteinase production
(Cassone et al. 1987; Ross et al. 1990), pseudohypha
formation (Sobel etal. 1984), phospholipase production
(Ibrahim et al. 1995) and phenotypic switching (Soll
1992).
The lower virulence of C. parapsilosis compared
to C. albicans can also be attributed to the lack of formation of hyphae. Most Candida species, including
C. parapsilosis (Laffey & Butler 2005) exist as spherical to
ovoid blastospores or yeast cells. Many Candida species
are capable, to various degrees, of producing chains of
elongated blastospores termed pseudohyphae, both in
vivo, and under certain conditions, in vitro. The hyphal
forms are more difficult to ingest, and the cell walls may
be more resistant to digestion. In addition, hyphal forms
have been defined as more adhesive than pseudohyphae
(Hostetter 1994).
The ability of a micro-organism to adhere to
mucosal surfaces is the critical first step for successful
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identified, smooth phenotypes produce the least biofilm. The molecular mechanisms that regulate phenotypic switching in C. parapsilosis are not yet understood
(Laffey & Butler 2005).
Another enzyme that seems to play an important
role in the pathogenesis of C. parapsilosis is phospholipase. This group of enzymes affect adhesion to
and penetration of host cells. Phospholipase activity
was detected in 51% of C. parapsilosis strains in a study
done by Ghannoum et al. (2000). Dagdeviren et al.
(2005) described phospholipase activity among 26% of
the blood isolates. As with C. albicans, C. parapsilosis
isolated from blood cultures were found to be stronger
phospholipase producers than isolates from other body
sites (Ibrahim etal. 1995). One study indicated no statistical difference between phospholipase production
and adherence, possibly due to the small sample size
(Dagdeviren etal. 2005).
The enzyme lipase seems to be another important
virulence factor. These enzymes affect adhesion and may
deny the host nutrients. Gacser etal. (2007a) showed that
lipase inhibitors significantly reduce tissue damage during infection of reconstituted human tissues. Recently,
Gacser etal. (2007b) studied targeted gene deletion on
the lipase genes CpLIP1 and CpLIP2. Their data support
the idea that lipase, secreted by C. parapsilosis, is involved
in disease pathogenesis. Extracellular lipase proteins
are important for optimal growth of C. parapsilosis in
lipid solutions, such as lipid-rich total parenteral nutrition, frequently used for very low birth weight neonates.
Another finding of the study was the correlation between
biofilm formation and lipase. Biofilm formation of the
C. parapsilosis lipase-negative mutant was decreased
dramatically (Gacser etal. 2007b). This enzyme seems to
be involved in survival of C. parapsilosis after phagocytosis by macrophages. Lipase-negative mutants were more
readily phagocytosed and killed by macrophages, compared to the parental strain and reconstituted mutants
(mutants of C. parapsilosis showing lipase activity). The
lipase negative strain of C. parapsilosis was tested in a
murine intraperitoneal infection model and showed less
virulence compared to the parental and reconstituted
strains (Gacser etal. 2007b).
Cassone etal. (1995) reported that C. parapsilosis is
markedly heterogeneous in experimental pathogenicity
and made a ranking of biotype. They assessed the various differential characteristics of colony morphology
(morphotype), resistance to various chemicals (resistotype), and correlated these with virulence in a systemic
murine infection model. These authors were able to
place isolates into groups on the basis of these traits,
although virulence in murine models showed a wide
range within a group. In addition, these authors found
no correlation of virulence in systemic infection with
Sap production (Cassone etal. 1995).
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pathogenic fungi, such as C. albicans, Blastomyces dermatitidis and Paracoccidioides brasiliensis (Brummer
et al. 1991). The mechanism of killing C. parapsilosis
by peritoneal macrophages, activated in vitro by
lymphokines or recombinant gamma-interferon was
studied by Brummer etal. (Brummer & Stevens 1989).
They observed killing of C. parapsilosis by non-activated peritoneal macrophages. Superoxide dismutase
blocked and dimethyl sulfoxide partially blocked this
killing, which suggested a mechanism depending on
the presence of superoxide anion is involved in the
killing of C. parapsilosis by macrophages. Killing by
activated macrophages was not inhibited by superoxide dismutase or dimethyl sulfoxide, suggesting
that activated macrophages probably depend on the
myeloperoxidase systems. In addition, Brummer etal.
(1991) observed no inhibition of killing of C. parapsilosis by the macrophages by the use of cycloheximide
and hydrocortisone.
Takoa etal. (1996) examined the role of reactive oxygen metabolites in phagocytosis and killing by murine
peritoneal macrophages incubated with C. parapsilosis,
by the use of a fluorochromatic vital staining technique.
The relative contribution of reactive oxygen metabolites,
depending on NADPH oxidase or xanthine oxidase,
was determined using selective inhibition of each of
these enzyme systems. Generation of reactive oxygen
metabolites by xanthine oxidase and NADPH oxidasedependent pathways were found to be important for
phagocytic killing by murine peritoneal macrophages.
Although there is a difference in pathogenicity of
the species C. albicans and C. parapsilosis, Marodi
et al. (1991b) found no difference in the biochemical
basis of phagocytosis by human monocytes or monocyte derived macrophages between these two Candida
species. In a separate study, C. parapsilosis was killed
significantly better by human monocytes than was
C. albicans; however monocyte derived macrophages
did not require the yeast to be opsonized, and killed
both species to an equivalent extent (Marodi et al.
1991a). The greater killing of C. parapsilosis by monocytes may be due to the sensitivity of the yeast to
toxic oxygen metabolites, hypochlorite, etc., which
is required for the killing of Candida species (Marodi
et al. 1991a). In addition, opsonization was required
for phagocytosis by monocytes for both C. albicans and
C. parapsilosis, and used both the classical pathway
and alternative pathway (Marodi etal. 1991b). Potoka
etal. (1998) studied phagocytosis and phagocytic killing of C. parapsilosis by rat Kupffer cell alone and by
Kupffer cells in coculture with hepatic endothelial
cell-enriched fraction of non-parenchymal cells. They
also reported both the NAPD oxidase and the xanthine
oxidase dependent pathways are important in Kupffer
cell killing of C. parapsilosis.
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was unable to cause disease in either normal or cyclophosphamide immunosuppressed mice. In contrast,
Arendrup etal. (2002) using immunocompetent mice in
a similar study, reported C. parapsilosis did show some
virulence, with parameters such as weight loss, kidney
weight, inflammation and infection and number of eyes
infected. Like C. krusei and C. guilliermondii, C. parapsilosis showed less virulence compared to the species
C. albicans, C. tropicalis, C. glabrata, C. kefyr, and
C. lusitaniae. In other studies, Andriole and Hasenclever
(1962) found mortality of diabetic mice infected with
C. albicans, C. tropicalis, or C. parapsilosis.
A recent report of Nett et al. (2007) proposed -1,3
glucan as a marker for C. albicans, C. parapsilosis, and
C. glabrata biofilm using a central venous catheter
(CVC) biofilm rat model. This model closely mimics a
patient with CVC infection. This model has been used for
diagnostic purposes, where animals with experimental
CVC infection showed significantly higher serum levels
of -1,3 glucan in C. parapsilosis and C. albicans biofilm
infections, compared with a model of systemic disease
using tail-vein infection, representing disseminated or
nonbiofilm disease.
Although in humans C. parapsilosis is associated with
endophthalmitis Edwards et al. (1977) were unable to
recover C. parapsilosis from the eyes in a rabbit model
of haematogenous Candida endopthalmitis. They studied ocular pathogenicities of species of Candida (e.g.,
C. krusei, C. parapsilosis, C. guilliermondii, C. tropicalis,
C. stellateoidea, and C. albicans) and found a relative
resistance of ocular tissues to haematogenous Candida
infections with species other than C. albicans. Thus, this
model would not appear useful for the study of endophthalmitis due to C. parapsilosis.
An alternative nonmammalian model has been
described by Chamilos etal. (2006b), who developed a
model of candidiasis of Toll (Tl)-deficient Drosophila
melanogaster. In agreement with mammalian animal
model studies, C. parapsilosis was less virulent than
C. albicans when injected into Tl mutant flies. This alternative model using D. melanogaster is promising for
large-scale studies of virulence mechanisms of candidiasis (Chamilos etal. 2006b).
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The emergence of yeast species with decreased susceptibility to contemporary antifungal regimens demonstrates the need for new antifungal agents (Capoor
et al. 2005, Nguyen et al. 1996). The echinocandin
class of antifungals offers an alternative to the standard regimens of azole or polyene agents and provides
additional advantages of reduced toxicity (Messer etal.
2004). Caspofungin, micafungin and anidulafungin,
echinocandin antifungal agents, compromise cell wall
structural integrity through non-competitive inhibition of the synthesis of 1,3--D-glucan (Cappelletty
& Eiselstein-McKitrick 2007; Denning 2003; Pfaller
et al. 2006b). Compared to other Candida species,
C. parapsilosis tends to be associated with a higher MIC
of echinocandins (Cappelletty & Eiselstein-McKitrick
2007; Fleck etal. 2007; Laverdiere etal. 2007; Marco etal.
1998; Messer et al. 2004; Nakamura & Takahashi 2006;
Ostrosky-Zeichner etal. 2003; Pfaller 2004; Pfaller etal.
2005a; Pfaller et al. 2006a; Pfaller et al. 2006b; Reboli
et al. 2007). The meaning of these higher MICs is still
being investigated, but changes in the glucan synthase
subunit Fks1 might explain the reduced activity of echinocandins against C. parapsilosis (Park etal. 2005; Reboli
etal. 2007). A recent report indicated the C. parapsilosis complex has a naturally occurring polymorphism
resulting in the substitution of alanine at position 660
for a conserved proline, which is present in other fungal
Fks1 (Garcia-Effron etal. 2008). The unique mitochondrial respiratory network of C. parapsilosis might play
an important role for its decreased susceptibility to the
echinocandins (Chamilos etal. 2006a). Chamilos etal.
(2006a) observed a decrease in caspofungin MICs after
simultaneous inhibition of all respiratory pathways.
From early studies, anidulafungin was demonstrated
to have a minimal inhibitory concentration range for
90% of C. parapsilosis strains [MIC90] of <2-4mg/L
(Arevalo etal. 2003; Marco etal. 2003; Marco etal. 1998;
Ostrosky-Zeichner etal. 2003; Pfaller etal. 1997). Marco,
etal. (1998) reported a discrepancy between caspofungin and anidulafungin susceptibility for C. parapsilosis.
Anidulafungin showed less activity against C. parapsilosis than did caspofungin (MIC90, >2 versus 1g/mL).
Messer, etal. (2004) reported only 36% of 106 C. parapsilosis strains tested were inhibited by anidulafungin
at<1mg/L; however, nearly all isolates were inhibited
at4mg/L. Reboli et al. (2007) directly compared the
efficacy of anidulafungin with that of fluconazole for the
treatment of candidemia and other forms of invasive
candidiasis. In that study, anidulafungin showed higher
MICs for C. parapsilosis compared to other species of
Candida, and patients with a C. parapsilosis infection
treated with fluconazole showed a somewhat better
response rate compared to anidulafungin. However,
the absolute difference in rate of successful response
against C. parapsilosis was not significant. Recently, a
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