Opportunistic Candida Infections in Critical COVID-19 Patients

Variable	Groups			p^†
Variable	Group 1 (n = 78)	Group 2 (n = 189)	Group 3 (n = 57)	p^†
Gender (male)	54 (69.2)^a	87 (46)^b	29 (50.9)^b	0.002
Age (year)	71.33 ± 13.67^ab	73.42 ± 11.34^a	68.51 ± 15.74^b	0.035
APACHE II score	12 (7–19)	12 (7–19)	14 (9–19)	0.485
SOFA score	4 (2–6)	4 (2–6)	4 (3–6)	0.334
Hospital stay (day)	27 (18–43)^a	22 (15–32)^b	18 (13–26)^b	< 0.001
ICU stay (day)	19 (10–27)^a	14 (8–22)^ab	10 (7–15)^b	< 0.001
PCR (positive)	50 (64.1)	128 (67.7)	36(63.1)	0.889
Comorbidities	66 (84.6)^a	162 (85.7)^a	28(49.1)^b	< 0.001
DM	23 (29.4)	70 (37)	16(28)	0.305
HT	30 (38.4)^ab	97( 49.7)^a	17 (29.8)^b	0.008
COPD	14 (17.9)^a	35 (18.5)^a	3 (5.2)^b	0.049
CAD	23 (29.4)	40 (21.1)	8 (14)	0.093
Malignancy	10 (12.8)^a	15 (7.9)^a	0 (0.0)^b	0.022
Goitre	6 (7.7)^a	2 (1.0)^b	1 (1.7)^ab	0.010
Kidney transplantation	0 (0.0)	2 (1.0)	0 (0.0)	0.487
Immunological disease	3 (3.8)	2(1.0)	0 (0.0)	0.142
Neurological disease	13 (16.6)^a	30 (15.8)^a	2 (3.5)^b	0.044
CKF/AKF	14 (17.9)	26 (13.7)	6 (10.5)	0.226
Mortality	54 (69.2)	133 (60.4)	33 (57.8)	0.208
Intubation	49 (62.8)^a	107 (85.2)^a	21 (36.8)^b	0.008
Central Catheter	42 (53.9)^a	58 (30.7)^b	7 (12.2)^c	< 0.001
Juguler	13 (30.9)	18 (31.0)	4 (57.1)	0.139
Femoral	23 (54.7)	31 (53.4)	2 (28.5)	< 0.001
Dialysis	6 (14.2)	9 (15.5)	1 (14.2)	0.286
BSA	75 (96.1)^a	178 (94.1)^a	12 (21.0)^b	< 0.001
Corticosteroid	49 (62.8)^a	142 (75.1)^b	15 (26.3)^c	< 0.001
IL-6 receptor inhibitors	7 (9.0)	7 (3.7)	3 (5.2)	0.214
TPN	24 (30.8)^a	59 (31.2)^a	5 (8.7)^b	0.003
AF	34 (43.5)	95 (50.2)	–	0.192
AF+/mortality	20 (58.8)	56 (58.9)	–	0.511
AF–/mortality	34 (77.2)	76 (80.8)	–	0.803
p^‡	0.080	< 0.001

[i] Values are expressed as n (%), mean ± SD or median (1^st–3^rd quartiles). Different superscripts among groups indicate a statistically significant difference between groups. Significant results are shown in bold.

p^† – significance value for the between-group comparisons, p^‡ – significance value for the within-group comparisons

TPN – total parenteral nutrition, BSA – broad-spectrum antibiotic, DM – diabetes mellitus,

HT – hypertension, COPD – chronic obstructive pulmonary disease, CAD – coronary artery disease,

CKF/AKF – chronic kidney failure/acute kidney failure, AF – antifungal, AF+ – antifungal use,

AF– – no antifungal use, APACHE II score – acute physiology and chronic health evaluation score,

SOFA – sequential organ failure assessment score, ICU – intensive care unit, IL-6 – interleukin-6

Table II

Univariate and multiple binary logistic regression analysis in identifying candidemia in Covid-19 patients.

Variable	Univariate		Multiple
Variable	OR (95% CI)	p	OR (95% CI)	p
Gender (female/male)	2.17 (1.07–4.41)	0.032	–	–
Age (year)	1.01 (0.99–1.04)	0.269	–	–
APACHE II score	0.97 (0.93–1.02)	0.181	–	–
SOFA score	0.93 (0.83–1.05)	0.224	–	–
Hospital stay (day)	1.04 (1.02–1.07)	0.002	–	–
ICU stay (day)	1.05 (1.02–1.09)	0.002	1.06 (1.01–1.11)	0.025
Comorbidities	5.70 (2.55–12.74)	< 0.001	6.94 (2.01–23.90)	0.002
DM	1.07 (0.50–2.28)	0.858	–	–
HT	1.47 (0.71–3.05)	0.299	–	–
COPD	3.94 (1.08–14.43)	0.039	–	–
CAD	2.56 (1.05–6.25)	0.039	–	–
Goitre	4.67 (0.55–39.89)	0.159	–	–
Neurological disease	4.52 (0.96–21.24)	0.056	–	–
CKF/AKF	1.86 (0.67–5.18)	0.235	–	–
Intubation	2.90 (1.43–5.88)	0.003	–	–
Central Catheter	8.33 (3.36–20.65)	< 0.001	–	–
BSA	93.75 (25.09–350.24)	< 0.001	90.68 (21.84–376.53)	< 0.001
Corticosteroid	4.73 (2.24–9.99)	< 0.001	–	–

[i] Significant results are shown in bold.

TPN – total parenteral nutrition, BSA – broad-spectrum antibiotic, DM – diabetes mellitus,

HT – hypertension, COPD – chronic obstructive pulmonary disease, CAD – coronary artery disease,

CKF/AKF – chronic kidney failure/acute kidney failure,

APACHE II score – acute physiology and chronic health evaluation score,

SOFA – sequential organ failure assessment score, ICU – intensive care unit,

OR – Odds ratio, CI – Confidence interval

Table III

Candida species distribution and frequency of antifungal use in the study groups.

	Total	FLC	CAS	ANI	MIC	AMB
Group 1
n	78	12	11	3	3	5
C. albicans	43 (55.1)	6 (50.0)	5 (45.5)	0 (0.0)	1 (33.3)	3 (60.0)
C. dubliniensi	1 (1.3)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)
C. glabrata	7 (9.0)	1 (8.3)	1 (9.1)	1 (33.3)	0 (0.0)	0 (0.0)
C. krusei	3 (3.8)	1 (8.3)	0 (0.0)	0 (0.0)	2 (66.7)	1 (20.0)
C. lusitaniae	1 (1.3)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)
C. parapsilosis	14 (17.9)	3 (25.0)	3 (27.3)	1 (33.3)	0 (0.0)	0 (0.0)
C. tropicalis	9 (11.5)	1 (8.3)	2 (18.2)	1 (33.3)	0 (0.0)	1 (20.0)
Group 2
n	189	46	32	9	4	4
C. albicans	123 (65.1)	34 (73.9)	22 (68.8)	7 (77.8)	3 (75.0)	0 (0.0)
C. glabrata	9 (4.7)	1 (2.2)	1 (3.1)	1 (11.1)	1 (25.0)	1 (25.0)
C. kefyr	2 (1.1)	2 (4.3)	0 (0.0)	0 (0.0)	0 (0.0)	1 (25.0)
C. krusei	2 (1.1)	0 (0.0)	1 (3.1)	0 (0.0)	0 (0.0)	0 (0.0)
C. lusitaniae	1 (0.5)	0 (0.0)	1 (3.1)	0 (0.0)	0 (0.0)	0 (0.0)
C. parapsilosis	29 (15.3)	4 (8.7)	3 (9.4)	0 (0.0)	0 (0.0)	1 (25.0)
C. tropicalis	22 (11.6)	5 (10.9)	4 (12.5)	1 (11.1)	0 (0.0)	1 (25.0)
Group 4 (53.8% of candidemia)
n	42	9	6	1	0	3
C. albicans	26 (61.9)	5 (55.6)	4 (66.7)	0 (0.0)	0 (0.0)	3 (100.0)
C. parapsilosis	10 (23.8)	3 (33.3)	2 (33.3)	0 (0.0)	0 (0.0)	0 (0.0)
C. glabrata	1 (2.4)	0 (0.0)	0 (0.0)	1 (100.0)	0 (0.0)	0 (0.0)
C. tropicalis	3 (7.1)	1 (11.1)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)
C. krusei	1 (2.4)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)
C. duplensie	1 (2.4)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)

[i] Values are expressed as n (%).

FLC – fluconazole, CAS – caspofungin, ANI – anidulafungin, MIC – micafungin, AMB – amphotericin B

Table IV

Antifungal results against Candida species, reproduced in blood.

	VRC μg/ml			FLC μg/ml			CAS μg/ml			AMB μg/ml
Species	GM	MIC₅₀	MIC₉₀	GM	MIC₅₀	MIC₉₀	GM	MIC₅₀	MIC₉₀	GM	MIC₅₀	MIC₉₀
C. albicans (n = 42)	0.42	0.25	0.75	2.42	2	4	0.74	0.75	1	0.59	0.25	1.5
C. parapsilosis (n = 13)	0.39	0.25	0.5	4.07	4	8	1.46	1	2	0.84	0.75	1.5
C. glabrata (n = 7)	0.42	0.47	0.5	22.5	16	48	1.02	1.5	1.5	0.53	0.5	0.75
C. tropicalis (n = 9)	0.35	0.38	0.5	3.22	2	4	0.75	0.5	2	0.91	0.38	2
C. krusei (n = 3)	0.21	0.25	0.38	74.6	64	128	0.75	0.75	1	0.59	0.75	1

[i] VRC – voriconazole, FLC – fluconazole, CAS – caspofungin, AMB – amphotericin B,

GM – geometric mean, MIC – minimal inhibitory concentration

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DOI: https://doi.org/10.33073/pjm-2022-036 | Journal eISSN: 2544-4646 | Journal ISSN: 1733-1331

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Language: English

Page range: 411 - 419

Submitted on: May 23, 2022

Accepted on: Jul 19, 2022

Published on: Sep 24, 2022

Published by: Polish Society of Microbiologists

In partnership with: Paradigm Publishing Services

Publication frequency: 4 issues per year

Keywords:

opportunistic Candida infections,

COVID-19,

critical care

Related subjects:

Life sciences,

Microbiology and virology

© 2022 Mıne Altinkaya Çavuş, Hafıze Sav, published by Polish Society of Microbiologists
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Volume 71 (2022): Issue 3 (September 2022)

Opportunistic Candida Infections in Critical COVID-19 Patients

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Table I

Table II

Table III

Table IV

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