Mycopathologia DOI 10.1007/s11046-015-9859-4

Fungemia Caused by Yarrowia lipolytica H. Trabelsi • K. Chtara • N. Khemakhem • S. Ne´ji • F. Cheikhrouhou • H. Sellami • R. Guidara • F. Makni • M. Bouaziz • A. Ayadi

Received: 4 September 2014 / Accepted: 6 January 2015 Ó Springer Science+Business Media Dordrecht 2015

Abstract Yarrowia lipolytica is weakly pathogenic yeast, which is rarely isolated from the blood. We report unusual cases of Y. lipolytica fungemia occurred between October 2012 and June 2014 in the intensive care unit (ICU) of the UH Habib Bourguiba Sfax. During this period, 55 cases of Y. lipolytica septicemia were diagnosed. There were 44 men and 11 women (sex ratio = 4).The median age was 43 years. The broadspectrum antibiotics (100 %), the catheterization (96 %), and the prolonged hospitalization in ICU (91 %) were the main risk factors. Patients were hospitalized in ICU, mostly, for polytraumatism (45.4 %), pneumopathy (9 %), and post-operative complications (7 %). Fever unresponsive to broadspectrum antibacterial therapy was the predominant sign of infection (83.6 %). Y. lipolytica was isolated in one or several blood cultures (14.5 %) and in the catheter tip culture of nine patients (16.3 %).Treatment was based on intravenous amphotericin B (58.2 %), fluconazole (45.4 %) and/or removal catheter (69 %).

H. Trabelsi  N. Khemakhem  S. Ne´ji  F. Cheikhrouhou  H. Sellami  R. Guidara  F. Makni  A. Ayadi (&) Fungal and Parasitic Molecular Biology Laboratory, School of Medicine-Sfax, Sfax University, 3029 Sfax, Tunisia e-mail: [email protected] K. Chtara  M. Bouaziz Intensive Care Unit, CHU Habib Bourguiba Sfax, Sfax, Tunisia

Apyrexia or blood cultures sterilization was obtained for 34 patients (61.8 %). Y. lipolytica candidemia is an opportunistic and emerging human yeast pathogen. It can reach to the bloodstream of immunocompromised or critically ill patients during hospitalization through intravascular catheterization. Further clinical data need to be evaluated for formulating management strategies of seriously ill patients infected with uncommon fungal agents. Keywords Yarrowia lipolytica  Emergent yeast  Candidemia  Intensive care unit

Introduction Yarrowia lipolytica is the only known species in the teleomorph genus Yarrowia and its anamorph is Candida lipolytica. It is a strictly aerobic and ubiquitous in the environment and having been isolated from refrigerated meat products, petroleum products, agricultural processing plants, and soil [1]. It, also, inhabits the mouth, pulmonary tree and intestines of healthy individuals [2]. It has a high lipolytic and proteolytic activity, and it is widely used in the detergent, food and pharmaceutics industries. Y. lipolytica has rarely been reported as a human pathogen [2, 3]. Y. lipolytica infection was first reported by Wehrspann and Fu¨llbrandt [4] in 1985. Since then, Y. lipolytica candidemia has been

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increasingly reported. It was isolated in four cases (0.07 %) among 6,082 yeast isolates collected from bloodstream infections in 250 medical centers distributed over 32 countries [5]. How such a yeast microorganism invades human hosts, even causing severe bloodstream infections is an interesting issue that is yet to be elucidated [6]. We report 55 cases of fungemia caused by Y. lipolytica. We sought to deepen our understanding of the clinical characteristics and management of Y. lipolytica fungemia.

Patients and Methods We report unusual cases of Y. lipolytica fungemia occurred between October 2012 and June 2014 in the intensive care unit (ICU) of the UH Habib Bourguiba Sfax (Tunisia). For each patient, we collected epidemiological (age, sex, underlying disease, and risk factors), clinical characteristics, treatment, and outcome. Prospective surveillance cultures (oral, nasal, urine, anal, and catheters tip cultures) were also taken in an attempt to further isolate Y. lipolytica from our patients. We collected samples from environmental sources (intravascular injection fluids, floors, tap water supply system, infusion pumps, and other hospital equipment). The hands of all healthcare workers in the unit were sampled using the broth-bag technique [7] and sterile premoistened swabs, respectively. All the blood specimens from the patients were inoculated into Bactec PED bottles (Becton–Dickinson, USA), which were incubated in the BactecÒ 9050 automated culturing system (BD diagnostic Systems 9050, Oxford, UK) at 37 °C for 15 days or until the bottles were positive by the colorimetric detection of CO2. Bottles proven to contain Candida spp. by direct examination were selected and subcultured in Sabouraud dextrose agar (SDA) at 25 °C. Yeasts grown on SDA plates were identified according to their morphological characteristics and biochemical profiles. Biochemical tests were performed by using ID32C (BioMerieux, France). The same methods were used for the others specimens (culture on SDA and identification by using ID32C). Identification of isolates was confirmed by DNA sequence analysis of the intergenic spacer (ITS) region (primers: ITS-1: 50 -TCCGTAGGTGAACCTGCGG-

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30 and ITS-4: 50 -TCCTCCGCTTATTGATATGC-30 ). These primers were designated by White et al. [8]. For antifungal drug susceptibility testing, a microtiter broth dilution method based on the Clinical and Laboratory Standards Institute M27-A2 standard (the sensititre yeast one; TREK Diagnostic Systems, East Grimstead, UK) was performed.

Results During our period of study, 55 cases of Y. lipolytica septicemia were diagnosed among 77 cases of positive yeast blood culture (71.4 %). There were 44 men and 11 women (sex ratio = 4).The median age was 43 years. The broad-spectrum antibiotics (100 %), the catheterization (96 %), and the prolonged hospitalization in ICU (91 %) were the main risk factors. The other risk factors were as follows: surgery (38 %), parenteral nutrition (36 %), yeast colonization (36 %), and diabetes (29 %). Only 9 % of cases received antifungal prophylaxis, and in all cases, the infection was acquired C48 h after hospitalization. Patients were hospitalized in ICU, mostly, for polytraumatism (45.4 %), pneumopathy (9 %), and post-operative complications (7 %). Fever unresponsive to broad-spectrum antibacterial therapy was the predominant sign of infection (83.6 %) followed by respiratory distress (20 %) and septic shock (20 %). Y. lipolytica was isolated in one or several blood cultures (14.5 %) and in the catheter tip culture of nine patients (16.3 %). All epidemiological and clinical characteristics of our patients were summarized in Table 1. The examination of the hands of healthcare workers, intravenous injection samples, other hospital equipment and environment source samples documented colonization by Y. lipolytica in the hands of one worker and in the infusions pumps of three patients. Y. lipolytica was also, isolated in the catheter tip culture of 11 patients who did not have an associated fungemia. On SDA after 3 days at 25 °C, the yeasts formed distinctive cerebriform, convoluted and firm white colonies. Microscopic examination showed ellipsoidal yeasts, single, paired, or single in small clusters. The API ID32C system yielded a 2300011011 code with excellent identification of the genus C. lipolytica.

Mycopathologia Table 1 Epidemiological and clinical characteristics of patients with Y. lipolytica candidemia No.

Age (y)/ sex

Underlying disease

Isolement of Y. lipolytica

Risk factors

Clinical failures

Therapy/ outcome

1

21/M

Polytraumatism

1 blood culture catheter

Antibiotics

Fever

AMB (13 d)

Catheter

Hemoperitonia

FLZ (17 d)

Parenteral nutrition

Pneumoperitoneum

CT removal Remission

Abdominal surgery 2

3

39/M

60/F

Polytraumatism

Diabetes

1 blood culture

1 blood culture

Ischemic cerebrovascular accident 4

5

48/F

32/F

Polytraumatism

Diabetes

1 blood culture

1 blood culture

Status epilepticus 6

15/F

Acute anemia

1 blood culture

Menometrorrhagia

7

8

78/M

50/M

Chronic obstructive pulmonary disease

1 blood culture

Rectosigmoid tumor

1 blood culture

Antibiotics

Fever

CT removal

Catheter Cerebral surgery

Sub-dural hematoma

Remission

Antibiotics

Hypothermia

FLZ (3 d)

Catheter

Pneumonia

AMB (6 d)

Parenteral nutrition

Septic shock

CT removal/dead

Antibiotics

Fever

FLZ (7 d)

Catheter

Pneumonia

CT removal

Cerebral surgery

Meningeal bleeding Fever

Remission

Antibiotics

FLZ (3 d)

Catheter

Respiratory distress

AMB (1 d)/dead

Antibiotics

Fever

FLZ (9 d)

Catheter

Chills

CT removal

Abdominal surgery

Multi visceral failure

Dead

Antibiotics

Fever

FLZ (7 d)

Catheter

Respiratory distress

Remission

Antibiotics

Fever

FLZ (6 d)

Catheter

Abdominal pain

AMB (17 d)

Parenteral nutrition

Peritonitis

Dead

Antibiotics

Hypothermia

AMB (2 d)

Catheter

Septic shock

Dead

Abdominal surgery 9

60/M

Diabetes

1 blood culture

Chronic renal failure

Respiratory distress 10

11

47/M

27/M

Polytraumatism

Thoracic traumatism

1 blood culture

2 blood culture

Antibiotics

Fever

AMB (10 d)

Catheter

Pneumonie

CT removal

Abdominal surgery

Extradural hematoma

Remission

Antibiotics

Fever Hemothorax

FLZ(23 d) CT removal

Catheter Abdominal surgery

Remission

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Mycopathologia Table 1 continued No.

Age (y)/ sex

Underlying disease

Isolement of Y. lipolytica

12

43/M

Polytraumatism

3 blood culture

13

52/M

Renal failure

1 blood culture

Cerebrovascular accident

Risk factors

Clinical failures

Therapy/ outcome

Antibiotics

Fever

FLZ

Catheter

Sub-dural hematoma

CT removal/ remission

Antibiotics

Infectious pneumopathy

AMB (7 d)

Catheter

FLZ(2 d) CT removal/dead

14

68/M

Chronic obstructive pulmonary disease

1 blood culture

Antibiotics

Respiratory distress

FLZ

15

36/M

Polytraumatism

1 blood culture

Antibiotics Catheter

Fever Respiratory distress

FLZ AMB Dead

Multiple surgery

Cerebral hemorrhage

Parenteral nutrition 16

17

18

18/M

51/M

46/M

Polytraumatism

Polytraumatism

Polytraumatism

1 blood culture

1 blood culture

1 blood culture catheter

20

62/F

20/M

Acute pancreatitis

Polytraumatism

1 blood culture

1 blood culture

CT removal

Antibiotics

Fever

AMB (8 d)

Catheter

Pneumopathy

CT removal/ remission

Antibiotics

Fever

FLZ (14 d)

Catheter

Septic shock

AMB(6 d) CT removal/ remission

Antibiotics

Fever

AMB (14 d)

Catheter

Extra dural hematoma

CT removal

Parenteral nutrition 19

Remission

Multiple surgery

Infectious pneumopathy

Remission

Antibiotics

Fever

AMB (2 d)

Catheter Parenteral nutrition

Septic shock

Dead

Antibiotics

Fever

FLZ ((25 d)

Catheter

Meningeal hemorrhage

CT removal

Parenteral nutrition

Dead

Pneumothorax

Cerebral surgery 21

73/M

Diabetes

1 blood culture

Renal failure Myocardial infarction 22

74/M

Polytraumatism

3 blood culture

Diabetes

Antibiotics

Fever

ablation

Catheter

Septic shock Pulmonary edema

catheter Dead

Antibiotics

Fever

FLZ (13 d)

Catheter

Septic shock

AMB (2 d) CT removal/dead

23

14/F

123

Status epilepticus

2 blood culture

Antibiotics

Fever

FLZ (16 d)

Catheter

Pneumopathy

CT removal

Parenteral nutrition

Epileptic seizure

Remission

Mycopathologia Table 1 continued No.

Age (y)/ sex

24

57/M

Underlying disease

Isolement of Y. lipolytica

Polytraumatism

1 blood culture

26

27

35/F

16/M

58/F

Clinical failures

Therapy/ outcome CT removal

Antibiotics

Fever

Catheter

Pneumopathy

Dead

1 blood culture catheter

Antibiotics

Fever

FLZ

Catheter Surgery(cesarian)

Pneumopathy Hemorrhagic shock

CT removal Remission

1 blood culture

Antibiotics

Fever

FLZ (11 d)

Catheter

Pneumopathy

AMB (16 d)

Multiple surgery

Extra dural hematoma

CT removal/ remission

Antibiotics

Fever

FLZ

Heart failure

Catheter

Pneumopathy

AMB

Cardiomyopathy

Parenteral nutrition

Diabetes 25

Risk factors

Post-operative shock

Polytraumatism

Diabetes

6 blood culture

CT removal Dead

Surgery 28

50/M

Guillain Barre´ syndrome

1 blood culture

Pneumopathy

Antibiotics

Fever

CT removal

Catheter

Respiratory distress

Dead

Parenteral nutrition 29 30

36/M 45/F

Polytraumatism Pneumonia

1 blood culture 1 blood culture catheter

Fever

Catheter

Pneumopathy

Remission

Antibiotics Catheter

Fever Respiratory distress

AMB (6 d) CT removal

Parenteral nutrition 31 32

21/M 61/M

Polytraumatism Polytraumatism

1 blood culture 2 blood culture catheter

Septic shock

Antibiotics

26/M

Polytraumatism

1 blood culture

34

78/M

Polytraumatism

1 blood culture

35

36

27/M

83/M

Polytraumatism

Thoracic trauma Heart failure

1 blood culture

1 blood culture catheter

Dead

Antibiotics

Fever

AMB

Catheter

Pneumopathy

Remission

Antibiotics

Fever

AMB

Catheter

Pneumopathy

CT removal/ remission

Antibiotics Catheter

Fever

CT removal Remission

Parenteral nutrition 33

AMB

Antibiotics

Fever



Catheter

Septic shock

Dead

Abdominal surgery

Splenic infarct

Antibiotics

Fever

AMB (14 d)

Catheter

Pneumopathy

CT removal/ remission

Antibiotics Catheter

Fever Pneumothorax

– Dead

Parenteral nutrition

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Mycopathologia Table 1 continued No.

Age (y)/ sex

37

42/M

Underlying disease

Isolement of Y. lipolytica

Polytraumatism

1 blood culture

Diabetes 38

30/M

Polytraumatism Diabetes

1 blood culture catheter

Risk factors

Clinical failures

Therapy/ outcome

Antibiotics

Fever

AMB

Catheter

Pneumonia

CT removal

Pneumothorax

Remission

Antibiotics

Fever

CT removal

Catheter

Pneumopathy

Remission

Parenteral nutrition 39

45/M

Polytraumatism

1 blood culture

Antibiotics

Fever

FLZ

40

50/M

Diabetes Pharyngeal cancer

2 blood culture

Catheter Antibiotics

Pneumonia Fever

AMB/dead AMB (2 d)

41

61/M

Diabetes

1 blood culture

Acute colitis

Surgery

Pneumopathy

Dead

Antibiotics

Hypothermia

FLZ (7 d)

Catheter

Severe sepsis

Remission

Hypothermia Thrombophlebitis

AMB (1 d) Dead

CT removal

Parenteral nutrition Abdominal surgery 42

52/M

Hemorrhagic rectocolitis

1 blood culture

Antibiotics Catheter Parenteral nutrition Abdominal surgery

43

36/F

Diabetes

1 blood culture

Chronic renal failure 44

25/F

Diabetes

1 blood culture

Epilepsy Caustic oesophagitis 45

38/M

Thoracic and abdominal trauma

1 blood culture

diabetes 46

29/M

Abdominal trauma

Antibiotics

Hypothermia

Catheter

Septic shock

Remission

Antibiotics

Fever

AMB (4 d)

Catheter Parenteral nutrition

Pneumonia Respiratory distress

CT removal Dead

Antibiotics

Pneumopathy

AMB

Catheter

Renal failure

CT removal

Parenteral nutrition 1 blood culture

Dead

Antibiotics

Fever

AMB

Catheter

Pneumonia

FLZ

Parenteral nutrition

Septic shock

Dead

Abdominal surgery 47

48

30/M

46/M

Thoracic trauma

Diabetes Bronchopneumopathy

123

1 blood culture

Antibiotics

Fever

CT removal

Catheter

Catheter

Dead

Surgery

Hemorrhagic shock Pulmonary abscess

Antibiotics

Septic shock

FLZ

Catheter

Respiratory distress

Dead

1 blood culture

Mycopathologia Table 1 continued No.

Age (y)/ sex

Underlying disease

Isolement of Y. lipolytica

49

32/M

Nosocomial pneumopathy

1 blood culture

50

34/M

Polytraumatism

1 blood culture

51

64/M

Hemorrhagic

1 blood culture

Cerebrovascular accident

52

60/M

53

4/M

Diabetes Acute pulmonary edema

1 blood culture

Soda intoxication

1 blood culture

Caustic oesophagitis 54

40/M

Polytraumatism

1 blood culture

55

18/M

Polytraumatism

1 blood culture

Risk factors

Clinical failures

Therapy/ outcome AMB

Antibiotics

Fever

Catheter

Septic shock

CT removal

Antibiotics

Fever

FLZ

Catheter

Pneumopathy

Remission

Antibiotics

Fever

AMB

Catheter

Pneumonia

FLZ

Cerebral surgery

Cerebral edema

CT removal/ Dead

Antibiotics Catheter

Fever Pneumopathy

FLZ CT removal/ remission CT removal

Antibiotics

Fever

Catheter

Septic shock

Dead

Antibiotics

Fever

CT removal

Catheter

Pneumopathy

Dead

Antibiotics

Fever

AMB

Catheter

Pneumonia

CT removal/ remission

Y year, M male, F female, AMB amphotericin B, FLZ fluconazole, d day, CT catheter

The isolates were confirmed to be Y. lipolytica using a sequence analysis (GenBank accession no. KC254114.1) of the amplified ITS region using the BLAST program 9. The length of the query sequence was 358 bp. A 99 % identity with Y. lipolytica genes was obtained. Treatment was based on intravenous amphotericin B (1 mg/kg/day) (58.2 %), fluconazole (400 mg/day) (45.4 %) and/or the removal catheter (69 %). Apyrexia or blood cultures sterilization was obtained for 34 patients (61.8 %). In vitro susceptibility testing of the strains showed that: the MICs of amphotericin B was B1 lg/ml for 94.5 % of strains; the MICs of fluconazole was \8 lg/ml for 87.2 % of strains; the MICs of VRZ was B1 lg/ml for 98 % of strains; the MICs of caspofungin was B28 lg/ml for 96.3 % of strains and the MICs of 5-flucytosine was B4 lg/ml for 20 % of strains.

Discussion Despite the fact that Candida albicans remained the most common species causing invasive candidiasis

worldwide (overall, 66 % of all Candida spp.), we noted a decreasing trend in the isolation of C. albicans, proportionately, due to widespread prophylactic use of fluconazole. Non-albicans Candida species are being reported more commonly as these are resistant to fluconazole [3, 9]. Y. lipolytica candidemia is a rare but an emerging pathogenic yeast infection in humans [2, 3, 10]. It was not included in the long list in Hazen’s [11] careful 1995 review of emerging yeast pathogens. Y. lipolytica infection was first reported by Wehrspann and Fu¨llbrandt [4] in 1985. Since then, Y. lipolytica candidemia has been increasingly reported and strongly associated with intravascular catheterization. In the multicenter study of Pfaller and Diekema [12], his incidence crossed from 0 % in 1997 to 0.8 % in 2003. In the literature, 55 cases of human infections due to Y. lipolytica have been described [2–5, 13–21]. Recently, Liu et al. [10] found 16 cases by reviewing relevant studies in English from PubMed. This first report documents 55 cases of Y. lipolytica fungemia that occurred in the same department (ICU). No previous isolate of Y. lipolytica from clinical, surveillance, or environmental samples has been

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reported at our hospital. The isolation of several cases of such an uncommon species in a hospital ward suggested an outbreak. The 55 patients involved were hospitalized in adjacent units and cared sometimes for by the same healthcare workers. Although the source of the outbreak was not, certainly, identified, positive cultures of vascular catheters tips from some patients in the absence of other potential sources of infection were very suggestive of vascular catheter-associated candidemia. In the literature, contaminated infusions or the hands of healthcare workers are considered potential exogenous sources of Candida spp, such as Candida parapsilosis [22]. Shin et al. have reported the ability of this fungus to cause epidemic transmission but deep visceral infections and mortality have not been documented [3, 14]. It seems that the virulence of Y. lipolytica is weak. Neither deep visceral infections nor profound febrile reactions developed in the experimental cases. In almost cases, the patients were immunocompromised and received parenteral nutrition or antibiotic treatment via a catheter [23]. Documented infections of candidemia due to Y. lipolytica have been described in persons with hematological disorders such as leukemias, bone marrow transplant recipients, traumatic ocular infections, chronic sinusitis, and vascular catheter-related infections [6]. Indwelling catheter devices, especially central venous catheters, were strongly correlated in almost all cases of Y. lipolytica candidemia. In addition, D’Antonio et al. [6] claimed that Y. lipolytica produced large amounts of viscous slime materials, which are responsible for its capacity to adhere to and to colonize the central catheter. These catheters could introduce the yeast pathogen into the blood stream easily. Therefore, C. lipolytica might be considered one of the causative agents of catheter-related candidemia. In the present case, fever unresponsive to broadspectrum antibacterial therapy was the predominant sign of infection. In line with other studies, the clinical feature of Y. lipolytica septicemia is often non specific and frequently resembles those of invasive candidiasis. Appropriate management of Y. lipolytica candidemia is still controversial. Some suggest a stand back or a wait-and-watch approach without catheter removal or antifungal therapy [6]. Others suggest that although the yeast may colonize in the catheter and be seeded

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into the bloodstream, removal of catheter alone resolves fungemia [2, 14]. Consistent with the current guideline for the management of candidiasis, most studies suggest systemic antifungal therapy as well as the removal of the potentially infected vascular catheter as the best treatment [24]. Importantly, almost all infections due to Y. lipolytica were catheter related. Removal of the catheter or its replacement, in some cases combined with antifungal therapy, resulted invariably in clearance of the pathogen [15, 17, 18]. Our results showed that most Y. lipolytica isolates are susceptible to fluconazole and amphotericin B. In vitro susceptibility tests revealed that Y. lipolytica is susceptible to amphotericin B, ketoconazole, fluconazole, itraconazole, voriconazole, and caspofungin [2, 6, 18, 21], whereas in some isolates resistance has been reported to 5-flucytosine (5FC) and itraconazole [21]. Decreased susceptibilities of Y. lipolytica isolates to fluconazole, the triazoles posaconazole and voriconazole were also observed [23].

Conclusion Though Y. lipolytica is an environmental contaminant, the increasing evidence of catheter-related Y. lipolytica infections suggests that Y. lipolytica should be included in any list of emerging yeast pathogens and also poses the problem of defining the best strategy of patient management, given the current controversy on the most appropriate approach.

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Fungemia caused by Yarrowia lipolytica.

Yarrowia lipolytica is weakly pathogenic yeast, which is rarely isolated from the blood. We report unusual cases of Y. lipolytica fungemia occurred be...
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