Vol 54, No 3 (2023)
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Invasive fungal disease presenting as septic shock in immunocompromised pediatric and adult patients: summary of reported cases

Tomasz Styczyński12, Jagoda Sadlok12, Monika Richert-Przygońska1, Robert Dębski1, Jan Syczyński1, Krzysztof Czyżewski1
Acta Haematol Pol 2023;54(3):154-160.

Abstract

Introduction: Septic shock is a very rare presentation of invasive fungal disease (IFD) in immunocompromised patients. The objective of this paper was to summarize reported cases of pediatric and adult patients with IFD presenting as septic shock in non-Candida infections. Literature data describing etiology, age, and outcome of septic shock as a presentation of IFD, is summarized. Material and methods: The available pediatric data included 23 patients, most of them with underlying non-hematological disease. Results: Only 6/23 (26.1%) were reported to survive this infection. Respective data in adults with invasive fungal disease presenting as septic shock were reported in 28 patients. Most of these patients were treated for acute leukemias (including three patients after hematopoietic cell transplantation); only 5/28 (17.9%) survived the infection. Conclusion: Invasive fungal disease presenting as septic shock in immunocompromised patients is a highly unusual presentation.

ORIGINAL RESEARCH ARTICLE

Acta Haematologica Polonica 2023

Number 3, Volume 54, pages 154–160

DOI: 10.5603/AHP.a2023.0030

ISSN 0001–5814

e-ISSN 2300–7117

Invasive fungal disease presenting as septic shock in immunocompromised pediatric and adult patients: summary of reported cases

Tomasz Styczyński12Jagoda Sadlok12Monika Richert-Przygońska 1Robert Dębski 1Jan Styczyński 1Krzysztof Czyżewski 1*
1Department of Pediatric Hematology and Oncology, Collegium Medicum, Nicolaus Copernicus University in Toruń,Jurasz University Hospital 1, Bydgoszcz, Poland
2Student Scientific Society, Collegium Medicum, Nicolaus Copernicus University in Toruń, Jurasz University Hospital 1,Bydgoszcz, Poland

*Address for correspondence: Krzysztof Czyżewski, Department of Pediatric Hematology and Oncology, Nicolaus Copernicus University in Toruń, Collegium Medicum, Skłodowskiej-Curie 9, 85–094 Bydgoszcz, Poland, phone +48 52 585 48 03, e-mail: k.czyzewski@cm.umk.pl

Received: 29.03.2023 Accepted: 13.04.2023 Early publication date: 09.06.2023

Abstract
Introduction: Septic shock is a very rare presentation of invasive fungal disease (IFD) in immunocompromised patients. The objective of this paper was to summarize reported cases of pediatric and adult patients with IFD presenting as septic shock in non-Candida infections. Literature data describing etiology, age, and outcome of septic shock as a presentation of IFD, is summarized.
Material and methods: The available pediatric data included 23 patients, most of them with underlying non-hematological disease.
Results: Only 6/23 (26.1%) were reported to survive this infection. Respective data in adults with invasive fungal disease presenting as septic shock were reported in 28 patients. Most of these patients were treated for acute leukemias (including three patients after hematopoietic cell transplantation); only 5/28 (17.9%) survived the infection.
Conclusion: Invasive fungal disease presenting as septic shock in immunocompromised patients is a highly unusual presentation.
Key words: invasive fungal disease, septic shock, hematopoietic cell transplantation, leukemia
Acta Haematologica Polonica 2023; 54, 3: 154–160

Introduction

Patients after allogeneic hematopoietic cell transplantation (allo-HCT) belong to a high-risk group of invasive fungal disease (IFD) [1]. The distribution of pathogens in an allo-HCT setting include aspergillosis in 55–60%, candidiasis in 25–30%, mycormycosis in 7–8%, and rare species e.g. fusariosis, scedosporiosis, geotrichosis in 2–3% [2]. With the widespread introduction of antifungal prophylaxis with azoles, this epidemiology is tending to change, with the rise of rare and sporadic species. No major differences in etiology between children and adults have been reported [3–6], although in one study the incidence of IFD after allo-HCT was significantly higher in children than in adults [6]. Regardless of age, patients in the following groups are considered high-risk for IFD: acute myeloblastic leukemia (AML); recurrent acute leukemia; allogeneic hematopoietic stem cell transplantation; and high risk acute lymphoblastic leukemia (ALL) [4, 5, 7–9]. Coexisting cytomegalovirus replication increases the risk of fungal complications [9].

Clinical symptoms of IFD in immunocompromised patients are dependent on the localization of the infection, which in most cases involves the lungs, abdomen, paranasal sinuses, skin or brain. In most cases, general symptoms occur including fever, followed by other systemic symptoms and laboratory markers of severe infection (e.g. C-reactive protein, procalcitonin). Fungemia or fungal sepsis might occur in a case of bloodstream infection with Candida; nonetheless septic shock is an infrequent presentation [10]. The objective of this paper was to analyze a series of cases of pediatric and adult patients with non-Candida IFD presenting as septic shock.

Material and methods

Studies and case reports regarding non-Candida invasive fungal disease presenting as septic shock in pediatric and adult patients were searched for in ‘PubMed’. Search queries included ‘invasive fungal disease’ OR ‘invasive fungal infection’ AND ‘septic shock’. The following data was retrieved from these reports: number of patients, age, gender, underlying disease, identification of fungal etiology, antifungal therapy, and treatment outcome.

Papers were included into analysis according to the diagnosis made by the respective authors. No additional judgment of sepsis and/or septic shock was made. According to the Third International Consensus Definitions for Sepsis and Septic Shock, sepsis was defined as ‘life-threatening organ dysfunction caused by a dysregulated host response to infection’ [11]. Septic shock was defined as ‘a subset of sepsis in which particularly profound circulatory, cellular, and metabolic abnormalities are associated with a greater risk of mortality than with sepsis alone’. Patients with septic shock can be clinically identified by the presence of two factors: the need to use a vasopressor and increased serum lactate concentration despite adequate volume resuscitation [11].

Results

Literature data describing etiology, age and outcome is very limited. The available pediatric data includes 22 patients, most of them with an underlying non-hematological disease (Table I) [12–22]. Only 6/22 (27.3%) are reported to have survived this infection, including 2/4 with acute leukemia. Etiology of the infection was highly variable, however infection with Saprochaete spp. (formerly Geotrichum spp., now proposed as Magnusiomyces spp.) presenting as septic shock was reported in four children, all with acute leukemias. Only two of them survived the infection. IFD-related non-Candida septic shock was reported also in 28 adults (Table II) [21, 23–40]. Among them, high mortality has been observed, with only 5/28 (17.9%) patients survival.

Table I. Literature data on septic shock in children with invasive fungal disease

Source

Age

Primary disease

Etiology

Treatment

Outcome

Zeng et al., 2021 [12]

Median age
22 months;
age range:
3–44 months
in 12 children

Various

Talaromyces marneffei

Amphotericin B 7/11

Itraconazole 2/11

Fluconazole 2/11

Voriconazole 3/11

Caspofungin 3/11

Died 9/12

Cured 3/12

Romanio et al., 2017 [13]

1-year-old boy

Down’s syndrome in postoperative period of congenital cardiac disease correction

Saccharomyces cerevisiae

Amphotericin B

Alive

Watson et al., 2016 [14]

12-year-old girl

Juvenile idiopathic arthritis

Blastomyces

Amphotericin B, adjunctive inhaled amphotericin; liposomal amphotericin B was changed to amphotericin B lipid complex

Died

El Dib et al., 2014 [15]

5-year-old boy

Coccidioidomycosis

Patient died before receiving required antifungal therapy

Died

Cavalcante et al., 2014 [16]

10-year-old girl

JSLE

Cryptococcus neoformans

Amphotericin B (liposomal)
(3 mg/kg)

Died

França et al., 2012 [17]

14-year-old girl

JSLE

Histoplasma capsulatum

Amphotericin B (liposomal)
(1 mg/kg)

Died

Pereira et al., 2004 [18]

2-year-old girl

Lymphoproliferative syndrome

Paracoccidioides brasiliensis

Intravenous sulfamethoxazole-trimethoprim (10 mg/kg trimethoprim)

Died

Hsu et al., 1998 [19]

23-month-old boy

AML

Trichosporon beigelii

Amphotericin B

Died

Wee et al., 2019 [20]

13-year-old boy

ALL

Saprochaete clavata

Amphotericin B and voriconazole (10 weeks)

Alive

17-year-old boy

AML

Saprochaete clavata

Amphotericin B (60 mg/d)

Died

Parahym et al., 2015 [21]

15-year-old boy

AML

Saprochaete
capitata

Caspofungin, amphotericin B
(lipid) (5 mg/kg) (24 days), and voriconazole (400 mg/d)

Alive

Trabelsi et al., 2015 [22]

17-year-old boy

AML

Saprochaete
capitata

Amphotericin B (60 mg/d)

Died

Table II. Literature data on septic shock in adults with invasive fungal disease

Source

Age

Primary disease

Etiology

Treatment

Outcome

Caldas et al., 2022 [23]

43-year-old woman

Crohn’s disease on treatment
with infliximab and azathioprine

Saprochaete clavata, Legionella pneumo­phila serogroup 1

Amphotericin B
(liposomal)

Died

Duarte et al., 2021 [24]

66-year-old woman

AML

Saprochaete capitata

Amphotericin B (liposomal)
and flucytosine

Died

Lo Cascio et al., 2020 [25]

20-year-old woman

ALL

Saprochaete clavata

Caspofungin

Died

Buchta et al., 2019 [26]

Patient 1 — 45-year-old man

Patient 2 — 61-year-old woman

Patient 3 — 58-year-old woman

Patient 4 — 50-year-old woman

Patient 5 — 66-year-old woman

1 — AML after
allo-HCT

2 — AML

3 — AML after
allo-HCT

4 — AML after auto-HCT

5 — DLBCL

1 — Saprochaete clavata

2 — Saprochaete clavata

3 — Saprochaete clavata

4 — Saprochaete clavate (+ Candida albicans were cultivated from nasopharyngeal swab)

5 — Saprochaete clavata + Candida glabrata

1 — amphotericin B
(1 mg/kg)

2 — amphotericin B
(1 mg/kg), amphotericin B
(lipid) (5 mg/kg)

3 — amphotericin B
(0.7–1 mg/kg), amphotericin B (lipid)
(5 mg/kg), voriconazole
(2 × 200 mg)

4 — amphotericin B
(0.7–1 mg/kg)

5 — micafungin (100 mg), voriconazole (2 × 200 mg)

1 — died

2 — survived (but died from early relapse of AML later)

3 — died

4 — died

5 — died

Ben Neji et al., 2019 [27]

39-year-old man

AML

Saprochaete capitata

Amphotericin B
(deoxycholate)

Died

Alobaid et al., 2019 [28]

67-year-old woman

Diabetes, hypertension, ischemic heart disease, left ventricular failure, peripheral vascular disease, bronchial asthma and obstructive sleep apnea

Saprochaete capitata

No antifungal therapy

Died

Bansal et al., 2018 [29]

29-year-old woman

AML

Saprochaete capitata

Amphotericin B (liposomal)

Died

Hajar et al., 2018 [30]

82-year-old man

Kidney transplant recipient

Saprochaete capitata

Amphotericin B
(liposomal)

Died

Pamidimukkala et al., 2017 [31]

48-year-old woman

Biphenotypic acute leukemia

Saprochaete capitata concomitant

Enterococcus gallinarum

Died

Fernández-Ruiz et al., 2017 [32]

55-year-old man

Refractory acute leukemia

Saprochaete capitata

Amphotericin B
and voriconazole

Died

Del Principe
et al., 2016 [33]

50-year-old woman

Mantle cell lymphoma

Saprochaete clavate

Amphotericin B (liposomal)
(3 mg/kg), 47 days

Died on day 60 from chemotherapy initiation because of lymphoma progression

Subramanya Supram et al., 2016 [34]

Patient 1 — 77-year-old woman

Patient 2 — 80-year-old man

Patient 1 — hypertension, Alzheimer’s disease

Patient 2 — COPD, hypertension

Patient 1 — Saprochaete capitata +
+ Flavobacter spp. (endotracheal aspirate)

Patient 2 — Saprochaete capitata

Patient 1 — no antifungal therapy

Patient 2 — fluconazole (400 mg/day for 4 days)

Patient 1 — died

Patient 2 — died

Trabelsi et al., 2015 [22]

Patient 1 — 25-year-old woman

Patient 2 — 57-year-old man

AML

Saprochaete capitata

Patient 1 — amphotericin B
(60 mg/d)

Patient 2 — amphotericin B
(80 mg/d) + voriconazole (2 × 200 mg)

Patient 1 — died

Patient 2 — died

Picard et al., 2014 [35]

Patient 1 — 46-year-old woman

Patient 2 — 70-year-old man

Patient 3 — 63-year-old woman

AML

Saprochaete clavata

Patient 1 — amphotericin B
(liposomal) and voriconazole

Patient 2 — caspofungin

Patient 3 — amphotericin B
(liposomal) and voriconazole

Patient 1 — survived septic shock, died because of hemorrhage

Patient 2 — died

Patient 3 — died

García-Ruiz
et al., 2013 [36]

55-year-old man

ALL

Saprochaete capitata

Amphotericin B (liposomal)
(4 mg/kg/d) + voriconazole

Died

Saghrouni
et al., 2012 [37]

47-year-old man

AML

Saprochaete capitata

Amphotericin B (1 mg/kg)
for 14 days followed by voriconazole 2 × 200 mg

Died

Avelar Rodriguez et al., 2017 [38]

28-year-old man

Cocaine abuse and Child-Pugh class C alcoholic liver cirrhosis

Rhinocerebral
mucormycosis
,
Candida glabrata

Amphotericin B (liposomal)
3 mg/kg

Died

Fernández-
-Ruiz et al., 2017 [32]

56-year-old man

Solid cancer, abdominal surgery, prolonged ICU stay

Wickerhamomyces anomalus

Amphotericin B for 9 days followed by fluconazole for 5 days)

Alive

Taniguchi
et al., 2009 [39]

18-year-old man

Mitochondrial encephalomyopathy accompanied by refractory anemia and chronic renal failure

Lecythophora mutabilis

Micafungin 5 mg/kg,
amphotericin B
(liposomal) (3 mg/kg)

Died

Hennequin
et al., 2000 [40]

47-year-oldman

Adenocarcinoma of lower esophagus

Saccharomyces boulardii

Fluconazole (100 mg/d) initiated on day 35 for six weeks

Alive

Discussion

Invasive fungal infections represent a serious medical problem worldwide and are a major cause of morbidity and mortality in patients with hematological malignancies. Other immunocompromised patients are also at high risk of IFD mainly because of the increased use of immunosuppressive and cytotoxic therapies, as well as improved diagnostic techniques. Candida and Aspergillus spp. are major causative agents.

However, with the new prevention strategies, new species are increasingly being reported as agents of bloodstream infections (BSI) or disseminated fungal disease. While Candida spp. is the most common etiology of fungal BSI and septic shock, such presentation is rare in case of other fungal pathogens.

Septic shock is the most dangerous presentation of infection, bringing the risk of poor prognosis. In this paper, we have searched for patients with non-Candida invasive fungal infection presenting as septic shock. We have found a limited number of reports, both in children and adults.

Septic shock is always a medical emergency. It requires the immediate administration of antimicrobials. Usually, bacterial etiology is suspected and adequate empirical treatment broadly covering the most probable pathogens is promptly started. In immunocompromised patients, in the presence of severe infection with symptoms of septic shock, atypical agents including fungal etiology should also be considered. One should also be aware of mixed etiology of septic shock in patients.

The most striking finding of our analysis is the low survival of patients, as only 26.1% of children and 17.9% of adults survived fungal infection with septic shock. Even with the long time period of inclusion, this survival rate was low in comparison with the outcome of IFD seen in leukemic patients both in the first [3, 41] and second [42, 43] decades of this century.

Immunocompromised patients, especially those with hematological malignancy who develop septic shock caused by fungal infection, are at very high risk of mortality. There are two options to improve therapeutic effect. Firstly, starting the empirical antifungal therapy as soon as possible is essential to increase the chance of survival in these patients. Secondly, it is recommended that early source control, including catheter removal, is a key factor influencing the outcome of leukemic or transplant patients with septic shock or sepsis of fungal etiology [4, 8].

The limitation of this study was the heterogenous population in terms of primary diagnosis, primary treatment, and etiology of fungal infection. We also limited the analysis to non-Candida etiology, because the symptoms of sepsis are relatively more frequent in Candida bloodstream infection.

Conclusion

Septic shock is a very rare presentation of fungal infection in immunocompromised patients, but the mortality is very high both in children and adults.

Authors’ contributions

KC, JS — design of study. RD, MRP, KC — provision of clinical data. All authors — analysis of clinical data. TS, JS — literature search and analysis of data. TS, JS — writing manuscript. All authors — critical revision and final approval.

Conflict of interest

The authors declare no conflict of interest.

Financial support

None.

Ethics

The work described in this article has been carried out in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans; EU Directive 2010/63/EU for animal experiments and uniform requirements for manuscripts submitted to biomedical journals.

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