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Alkhuzaie, M. M., & Jasim, N. O. (2022). Filamentous fungi associated with COVID-19 and
its susceptibility to some antifungals.
International Journal of Health Sciences
,
6
(S6), 1448–
1462. https://doi.org/10.53730/ijhs.v6nS6.9753
Filamentous fungi associated with COVID-19
and its susceptibility to some antifungals
Mohammed Mudhafar Alkhuzaie
Department of Biology, College of Science, University of Al-Qadisiyah, Iraq
*Corresponding author email: scie.bio.mas.20.30@qu.edu.iq
Neeran Obied Jasim
Department of Biology, College of Science, University of Al-Qadisiyah, Iraq
Abstract
---
The purpose of this study was to conduct a survey of the
fungal species associated with COVID-19 viral infection in 150 patients
who were admitted to the intensive care unit (ICU) in Al- Diwaniyah
Teaching Hospital in Al-Diwaniyah City, Iraq, for a period of five
months beginning in October 2021 and ending in February 2022.
According to the findings, yeasts were more prevalent than any of the
other detected fungal species, accounting for 98 of the total isolates
(65.33 percent). While filamentous fungus accounted for 19 isolates
(12.33 percent), including the predominance of Aspergillus flavus with
6 isolates (40 percent) in comparison to the Aspergillus spp. ratio,
these fungi were found to be rather uncommon. In light of the fact that
this publication provided evidence of the isolation of Aspergillus
sydowii from COVID19 patients for the first time globally. In addition,
we drew attention to the outstanding activity of the antifungal
medications amphotericin B, itraconazole, and voriconazole, all of
which have a high susceptibility rate.
Keywords
---
COVID-19, yeast, filamentous fungi, antifungal,
AmphotericinB, Itraconazole, Voriconazole.
Introduction
World Health Organization (WHO) labeled the new coronavirus (COVID-19)
outbreak a worldwide pandemic on March 11, 2020 (WHO, 2020). It is a
respiratory condition that has a negative impact on the overall health of the
individual (Singh & Singh, 2020). Fever, dry cough, weariness, dyspnea, anosmia,
ageusia, or a combination of these symptoms are the most often reported clinical
symptoms in patients (Huang
et al
., 2020). COVID-19 infection symptoms may
International Journal of Health Sciences ISSN 2550-6978 E-ISSN 2550-696X © 2022.
Manuscript submitted: 9 March 2022, Manuscript revised: 27 May 2022, Accepted for publication: 18 June 2022
1448
1449
appear 2–14 days after exposure (based on the incubation period of COVID-19
virus). Clinical symptoms in SARS-CoV-2 infected patients are often various,
ranging from no symptoms to severe sickness. These clinical symptoms can be
further classified into four groups, which are as follows: asymptomatic; mild;
moderate; severe; and critical illness (Raoult
et al
., 2020). Critically sick COVID-
19 patients had increased pro-inflammatory (IL-1, IL-2, IL-6, TNF-α) and anti-
inflammatory (IL-4, IL-10) cytokine levels, fewer CD4 interferon-gamma
countenance, and less CD4 and CD8 cells. This acute clinical state raises the
hazard of deadly fungal infections (Pemán
et al
., 2020).
There was an increase in the number of re-infections due to the severe
immunomodulation and lymphocyte depletion generated by the virus and its
treatment. Incidence and mortality of (CAPA) are on the rise (David
et al
., 2022).
CAPA has been recorded in between 5% and 10% of severely unwell individuals
with COVID-19 (coronavirus disease 2019). Hospitals' rates of occurrence range
from zero to three-thirds of one percent (Clancy & Nguyen, 2022). As a
consequence of the SARS-CoV-2 pandemic, mucormycosis has become a major
problem for the worldwide pandemic, particularly in Asian countries (Pushparaj
et
al
., 2022). Several hypotheses relate mucormycosis to serious COVID-19 patients
who are immunocompromised and/or have concomitant co-morbidities, as an
example, Covid has been linked to diabetes, which in turn has been linked to an
increased risk of mucormycosis. (Bhatia, 2022). The purpose of our research is to
carry out a survey of the fungal species that are linked to COVID-19 especially the
filamentous fungi, and the activity of some antifungals against it.
Materials and Methods
Collection of the specimens and data
During the research period beginning in October 2021 and continuing through
February 2022, a total of 150 clinical samples were collected from patients who
were confirmed to be infected with COVID-19 by using PCR. These patients were
hospitalized in the intensive care unit (ICU) at Al-Shifa Center of Al-Diwaniyah
Teaching Hospital, which is located in the Al-Diwaniyah governorate of Iraq. Oral
swabs, pharyngeal swabs, nasal swabs, and sputum samples were all included in
the collection of samples. When it came to the swabs, sterile cotton swabs were
rotated inside the oral cavity of the patient, and then they were stored in plastic
containers until they were needed. During the process of collecting sputum
samples, a container with a diameter of 5 centimeters was used. After rinsing the
mouth with water to reduce the number of germs present in the mouth and to
dilute the saliva, samples were obtained. It is important to avoid swallowing
sputum and instead spit it out into a clean container as fast as possible.
Specimens’ cultivation
For each sputum sample, 0.1 mL of the specimen was removed and streaked onto
Sabouraud dextrose agar medium (Pashley
et al
., 2012)
.
The swabs streaked
directly onto SDA; three replications of the culture were made to ensure that the
fungal growth was not contaminated during the culture process. The dishes were
incubated at a temperature of 37°C for 24 hours (Atlas, 1995). Then for
1450
subculture we used another culture media like, Czapiks dox agar, and Potato
Dextrose Agar for diagnostic reasons.
Identification of Fungal species
Depending on the culture and microscopic properties of the fungus as stated in
(Kidd
et al
., 2016).
Antifungal susceptibility test
Antifungal susceptibility testing using disk diffusion was carried out on non-
supplemented MHA in accordance with the procedure outlined in the CLSI M 51-
A publication (CLSI, 2010). To summarize, the mold stock inoculum suspension
was applied to the whole surface of the MHA using a non-toxic cotton swab. This
was done so that the mold would not be diluted. On the surface of each of the
MHA plates that had been infected, disks containing antifungals were inserted.
After 24 and 48 hours of incubation at 35°C, the plates were examined for their
results. The CLSI M51-A standard was followed in order to interpret the zone
diameter. The antifungal disks that tested are AmphotericinB (AMB) 20 µg/ml,
Itraconazole (IT) 10 µg/ml, Ketoconazole (KT) 10 µg/ml, Fluconazole (FLC) 25
µg/ml, Voriconazole (VRC) 1 µg/ml. (the antifungal disks manufactured by
Liophilcm, Italy)
Statistical analysis
Statistical analysis of the data was carried out using one-way ANOVA with the
least significance difference (LSD) using the statistical analysis software program
(Special Package for Statistical Science SPSS version 26), with a significant value
P ≤ 0.05.
Results and Discussion
Isolation and Diagnosis
A number of the agronomic and microscopic characteristics were investigated in
order to demonstrate the yield of dangerous fungus isolates that were isolated
from COVID19 patients. The following are some of the characteristics that were
investigated:
Aspergillus
spp
Cultural Characteristics
The colonies growing on Czapik’s dox agar and Sabouraud Dextrose Agar (SDA)
appeared in the form of Cottony fluffy to velvety white mycelium growth, shortly
coated with copious amounts of spores quickly change to green, yellow, orange,
black, or brown, could be seen in all of the petri dishes after three days to five
days. It's possible to see different shades of the same hue at different places.
1451
Microscopic Characteristics
In order to carry out microscopic characterization of the fungal isolate, a
lactophenol cotton blue mount of the growth was prepared. This was done from
the growth. They were predominantly made up of upright conidiophores. The
conidiophores branched out into vesicles that were coated in phialides at their
tips (biseriate).
Diagnosed isolates
An assessment of their morphology (both macroscopic and microscopic), as in
Figure (1), was performed using a reference guide (Kidd
et al
., 2016; Sciortino, 2017).
In order to make the best guess as to the species to which they belonged; we
identified the following:
•
A. niger
(n=5) isolates, on culture medium the basal felt of the colonies is
either white or yellow in color, and it is covered with a thick coating of
darkish brown to black conidial heads. Under microscope the walls of
conidiophore stipes are smooth and hyaline, or they begin to darken as they
approach the vesicle. The conidial heads are biseriate, and the phialides are
born on brown metulae that are often septate. The conidia range in size from
globose to sub globose and have rough walls. Their color ranges from dark
brown to black.
•
A. flavus
(n=6) isolate, on culture media yellow colonies with radial channels
become brilliant to dark yellow-green with age. Under microscope some
conidial heads have phialides carried directly on the vesicle (uniseriate).
Near the vesicle, conidiophore stipes are hyaline and rough. Pale green,
globose, echinulate conidia.
•
A. fumigatus
(n= 3) isolates, on culture media blue-green colonies have a
suede-like. Microscopic examination revealed conidiophore-covered surface.
Columnar conidial heads are commonly shorter and uniseriate. Short,
smooth-walled conidiophore stipes with conical-shaped terminal vesicles with
one row of phialides. Conidia are globose to sub globose, green, and coarsely
roughened.
•
A. sydowii
(n=1) isolate. on culture media circle with brown to orange
margins colonies have a suede-like The isolated fungus had conidiophores,
and one could discern conidia globose in shape, metulae, and phialides.
Regarding this point, Banu
et al
. (2013) indicate that the
Aspergillus
colonies
exhibit several phenotypic traits when grown on SDA, and this outcome is in line
with what De Carolis
et al
. (2012) mentioned in their study that
Aspergillus
Colony morphology and microscopic features are presently used in clinical
mycology laboratories to identify filamentous fungus.
1452
a
b
c
d
Fig.1.
Aspergillus
sp. Culture on Czapik’s dox agar medium at 37°C for 5 days,
and microscopic morphology (40X), a.
A. niger, b. A. flavus, c.
A. fumigatus, d. A. sydowii
Rhizopus oryzae
Cultural Characteristics
The initial color of
R. oryzae
colonies is white, cottony on SDA and PDA at 37
o
C,
but they mature to a brownish color and rapidly can reach a thickness of around
1 centimeter. With this respect, Kwon
et al
. (2011) indicates that the
R. oryzae
colonies initially white and cotton-like eventually became brownish-grey to black
due to the heavy accumulation of sporangia, and the mycelial growth was optimal
at 30
o
C, although good growth was also seen at 37
o
C on PDA. and this result is
consistent with what Manghwar
et al
. (2015) mentioned about the appearance of
R. oryzae
mycelium SDA was initially white but gradually turned grayish black
with a web-like texture.
as in Figure (2a)
1453
Microscopic Characteristics
a
b
Hyphae are hyaline, varying in size and nonseptate. Sporangiophores are dark
brown, unbranched, and rhizoids are abundantly produced from the foot cells.
Foot cells are often seen at the end opposite the sporangium. Sporangia are
round, dark brown to grayish black, with a flattened base, and contain many
spores. This finding is consistent with what was presented by Manghwar
et al
.
(2015) in their study that sporangia, apophysis, sporangiophores, and rhizoids
made up the bulk of
R. oryzae
microscopic structure.
as in Figure (2b)
Fig.2.
R. oryzae
a)Culture on SDA medium at 37°C for 3 days, and b)
microscopic morphology (40X)
Talaromyces marneffei
Cultural Characteristics
A colony's color might range from green, blue, gray, white, yellow, or even pink,
depending on the stage of development and the incubation period, so after three
days of incubation on SDA at 25
o
C, the colony's surface is covered with a fine
green, powdery or velvety layer,
T.
marneffei
that generate red pigment in the agar in
the fifth day of incubation. this result is in accordance with findings reported by
Sethuraman
et al
. (2020) who demonstrated that in 72 hours of growth on SDA at
25
o
C, greenish velvety mycelial colonies formed, which, after two more days of
incubation, developed a diffuse red color,
as in Figure (3a,3b).
Microscopic Characteristics
A mount of lactophenol cotton blue showed Phialides are generated on primary
conidiophores that are short branching or unbranched. Branching can be
achieved by forming metulae, which provide the impression of a brush. Chains of
phialides generate conidia, which can be flat, elliptical, cylindrical, or spindle- shaped.
This finding in line with Hart
et al
. (2012) there are septate hyphae with smooth-
walled hyaline conidiophores that have bi-vertical ends with 3–5 metulae and 4–5
phialides on each,as in figure (3c).
1454
a
b
c
a
b
Fig.3: a)
T. marneffei
Culture on SDA medium at 25°C for 3 days, b) Culture on
SDA medium at 25°C for 7days, c) microscopic morphology (40X),
Coccidioides immitis
Cultural Characteristics
C. immitis
colonies start off white and may develop cottony. then become white
and fluffy. As colonies age, they may become gray-white this result in line with
Kantarcioglu
et al
. (2014) who demonstrated that in 4–5 days at 30° C and 37° C,
SDA cultures developed glabrous colonies surrounding tissue biopsy specimens.
After 2–3 weeks, colonies were white, floccose, and in consistent with findings by
Cordeiro
et al
. (2006) that the Coccidioides colony was macromorphologically
examined in PDA and SDA, revealing the apiculated, velvety, white or cream-
colored,
as in figure (4)
Fig.4.a)
C. immitis
Culture on SDA medium at 37°C for 3 days.
b) microscopic
morphology (40X)
Isolated Fungi
In the present study, it was discovered that 102 patients out of 150 had a fungal co-
infection Table 1. A total of 117 distinct fungal isolates were retrieved from patients,
which brings the total number of fungal isolates from this study to 117. As is
evident by looking at Table 2, several of the isolates consisted of yeasts and molds:
TABLE 1: Percentage of Infection type
infection type covid19 only covid19+fungi* Total
1455
number 48 102 150
Percentage% 32 68 100
*There are S. D. LSD= 26.172 P VALUE=0.04719
Table 2
Fungal species isolates
Fungi Species Number of
Isolates
Percentage to
isolates 117
Percentage to
Samples 150
yeast 98 83.76 65.33
filamentous 19 16.24 12.66
There are no significant differences between fungi species
Aspergillus spp. Frequency
The recent study found that
Aspergillus
is the second prevalent fungi identified
from Covid-19 patients, with a 10 % frequency
.
As seen in the table (1),
A. flavus
was the most common (40%) than the other isolated
Aspergillus
species (
A. niger
33.33%
, A. fumigatus
20% and
A. sydowii
6.67%
.
Table 1
Aspergillus spp.
Isolates
Aspergillus sp. isolates Percentage to
Aspergillus sp. Isolates
A. flavus
6 40
A. niger
5 33.33
A. fumigatus
3 20.00
A. sydowii
1 6.67
total 15 100.00
There are no significant differences between the species
In view of the information presented above on the percentage of Aspergillus
isolates, we observe that
A. flavus
and
A. niger
are the most prevalent species.
Generally, this is a sign that non-fumigatus Aspergillus species are in dominance.
This result lends credence to the conclusions drawn by previous researchers in
this field Al-Wathiqi
et al
. (2013); Taghizadeh-Armaki
et al
. (2017); Zarrinfar
et al
.
(2012) who have found that non-fumigatus Aspergillus species, such as the A.
flavus, are the most common cause of IPA in tropical and subtropical climatic
zones. This finding in line with Abdalla
et al
. (2020) who reported that
A. terreus
or
A. niger
was suspected of causing CAPA in COVID-19 patients in Qatar, to
substantiate the claim that Middle Eastern and South Asian non fumigatus
Aspergillus species are more prevalent than in Europe and North America.
The yields and the percentage of Aspergillus in our study were higher compared to
those of other studies by Schein
et al
. (2020) from France and Yang
et al
. (2020)
from China, which reported an incident rate with 2.4% and 5.8% respectively
.
on
the other hand, our finding is lower to what find by Rutsaert
et al
. (2020) from the
1456
Netherlands and Alanio
et al
. (2020) from France Koehler
et al
. (2020) from
Germany with
(
35%, 33%, 26.3% respectively) and indicate the prevalence of
A.
fumigatus
,
while Nasir
et al
. (2020) from Pakistan record 21.7% and
A. flavus
has
the higher rate of isolation than other
Aspergillus sp.
.The mentioned studies
reflect a wide-ranging incident and another indication for the variation in
dominant of
Aspergillus sp
. as causing for Aspergillosis between different
geographical zones. In our study we record an intriguing finding which is the first
isolation globally of
A. sydowii
from COVID-19 patient based to the available
literatures.
Rhizopus oryzae
According to our findings,
R. oryzae
(which causes Mucormycosis) came in at
position three on the incidence scale with (1.33%) and percent of (1.71%) when
compared to the remaining fungal isolates that were recovered and diagnosed as
having originated from COVID-19 patients, as shown in table (2).
Table 2
Rhizopus sp.
Isolates
Rhizopus sp.
isolates Percentage to
Rhizopus sp
. Isolates
Percentage to fungal isolates
(117)
R. oryzae
2 100 1.71
This pattern of results is consistent with the finding of Masci and Wormser
(2005); Nazir
et al
. (2021) that
R. Oryzae
strains account for sixty percent of the
cases of human mucormycosis, and
R. Oryzae
makes up ninety percent of rhino
orbital brain (ROCM), this is consistent with A meta-analysis of 851 instances of
mucormycosis by Jeong
et al
. (2019), which indicated that the species
Rhizopus
was
the most prevalent one to be isolated. And in consistent with Prakash
et al
.
(2019) work that deals with mucormycosis at India's four largest tertiary care
facilities, they found that
R. oryzae
(n = 124, 51.9 percent ) was the major agent
found, followed by
R. microsporus
(n = 30,
12.6 percent ),
Apophysomyces variabilis
(n = 22, 9.2 percent ) and
R. homothallicus
(n
= 6, 2.5 percent )
.
Also
,
we isolate
R. Oryzae
from a nasal swab
,
which indicate the colonization of
this genus to the nasal sinuses
,
this finding in line with Uddin (2021) who point
out that nose
,
sinuses are the mostly affected parts of the body. Satish
et al
.
(2021) have stated that Mucormycosis linked to COVID-19 has been identified in
both Europe and the United States (CAM). According to reports from Iran,
Pakistan, Bangladesh, and Iraq (and other countries), CAM instances have been
reported.
Talaromyces marneffei
According to our findings,
T. marneffei
(which causes Talaromycosis) on the
incidence scale with (0.67%) and a percent of (0.85%) when compared to the
remaining fungal isolates that were recovered and diagnosed as having originated
from COVID-19 patients, as shown in table (3).
1457
Talaromyces sp.
isolates
Percentage to
Percentage to fungal
Talaromyces sp
. Isolates
isolates (117)
T. marneffei
1
100
0.85
Coccidiodes sp.
isolates
Percentage to
Percentage to fungal
Coccidiodes sp
. Isolates
isolates (117)
Coccidioides immitis
1
100
0.85
Table 3
Talaromyces sp.
Isolates
(Narayanasamy
et al
., 2021) Death and morbidity rates from acute and chronic
pulmonary mycoses, notably endemic diseases like Talaromycosis, remain
alarmingly high despite breakthroughs in antifungal therapy (Maitre
et al
., 2021).
Coccidioides immitis
According to our findings,
C. immitis
(which causes Coccidiomycosis) on the
incidence scale with (0.67%) and a percent of (0.85%) when compared to the
remaining fungal isolates that were recovered and diagnosed as having originated
from COVID-19 patients, as shown in table (4).
Table 4
Coccidiodes sp.
Isolates
Consistent findings with Shah
et al
. (2020) who gave a description of the first
instance of Coccidiomycosis coinfection with CoV-2 that has ever been
documented, this is in line with Chang
et al
. (2020) who report identification of
Coccidiomycosis with COVID19 in a female (48 y) and stated the health care
system is on the verge of collapsing under the strain of the COVID-19 pandemic,
which is why screening, triaging, and treatment efforts need to be stepped up
immediately. It is simple to forget about endemic illnesses like
C. immitis
or to
incorrectly believe that they are part of a pandemic.
1458
Antifungal susceptibility test
Table 5
Antifungal susceptibility for filamentous fungi (disc diffusion)
Antifungal agents
Fungi
. (n)
AMB
20µg/ml
FLC
25µg/ml
KT
10µg/ml
IT
10µg/ml
VRC
1µg/ml
Aspergillus fla vus (6)
Aspergillus fumigatus (3)
Aspergillus niger (5)
Aspergillus sydowii (1)
Coccidioides immitis (1)
Talaromyces marneffei (1)
Rhizopus oryzae (2)
S 6 4 3 6 6
S-DD
R 2 3
S 3 2 2 3 3
S-DD
R 1 1
S 5 4 3 5 5
S-DD
R 1 2
S 1 1 1 1 1
S-DD
R
S 1 1 1 1
S-DD
R 1
S 1 1 1 1
S-DD
R 1
S 2 2 2 2 2
S-DD
R
Total`19
S
(%)
S-DD
R
(%)
100 14
73.7
5
26.3
13
68.4
6
31.6
100 100
It is clear from observing the table (5) that the antifungal that was tested had a
definite degree of sensitivity when put up against the filamentous fungus. AmB,
IT, VRC obtained sensitivity with 100%, while FLC, KT get an obvious resistance
with (26.3, 31.6) % respectively. These results in accordance with Kumar et al.
(2010) who reported that the disc diffusion technique was used for measuring the
susceptibility of antifungals toward
A. flavus
, and the results indicated that not a
single strain was fluconazole sensitive. In addition, ketoconazole demonstrated a
sensitivity of sixty percent at Against itraconazole, 100 percent strains were
sensitive. Amphotericin B had a 96 percent inhibition rate. The findings of the
study by Thompson
et al
. (2017), which are consistent with our findings, indicate that
C. immitis
has evolved a resistance to the antifungal medication fluconazole. Our
findings for
T. marneffei
are consistent with those of Lei
et al
. (2018) who stated
that their study results of antifungals against
T. marneffei
support the use of
Amphotericin B, Itraconazole, Voriconazole, and Posaconazole in the clinical care of
Talaromycosis but raise concerns about fluconazole resistance.
Conclusion
Fungal co-infection poses a significant health risk in patients infected with
coronavirus (COVID-19). Aspergillus sp. that causes Aspergillosis and Rhizopus
sp., which causes Mucormycosis, is becoming increasingly common as the globe
Sensitiv
ity
1459
continues to fight COVID-19 due to immunological issues that weaken the
defenses of the body against opportunistic and true pathogenic fungi.
Furthermore, the antifungals AmphotericinB, Itraconazole, and Voriconazole have
good activity with a high susceptibility ratio. Lastly, this study found that COVID-
19 is linked to a high number of fungal infections. Because of this, patients with
COVID-19 should be tested for fungal infections as soon as possible to reduce the
chance of getting a more serious illness. This is because early detection is key to
treating fungal co-infections.
Acknowledgment
We would like to extend our gratitude to the administration of Al-Diwaniyah
Teaching Hospital as well as the workers of Al-Shifa Center.
References
Abdalla, S., Almaslamani, M. A., Hashim, S. M., Ibrahim, A. S., & Omrani, A. S.
(2020). Fatal Coronavirus Disease 2019-associated Pulmonary Aspergillosis; A
Report of Two Cases and Review of the Literature.
IDCases
,
22
, e00935-
e00935.
https://doi.org/10.1016/j.idcr.2020.e00935
Al-Wathiqi, F., Ahmad, S., & Khan, Z. (2013). Molecular identification and
antifungal susceptibility profile of Aspergillus flavus isolates recovered from
clinical specimens in Kuwait.
BMC Infectious Diseases
,
13
(1).
https://doi.org/10.1186/1471-2334-13-126
Alanio, A., Dellière, S., Fodil, S., Bretagne, S., & Mégarbane, B. (2020). Prevalence
of putative invasive pulmonary aspergillosis in critically ill patients with
COVID-19.
The Lancet. Respiratory medicine
,
8
(6), e48-e49.
https://doi.org/10.1016/S2213-2600(20)30237-X
Atlas, R. M. (1995). Principles of Microbiology. Mosby-Year Book.
Inc., St-Louis,
USA
.
Banu, A., Anand, M., & Eswari, L. (2013). A rare case of onychomycosis in all 10
fingers of an immunocompetent patient.
Indian Dermatology Online Journal
,
4
(4).
https://doi.org/10.4103/2229-5178.120649
Bhatia, M. (2022). The rise of mucormycosis in Covid-19 patients in India.
Expert
Review of Anti-infective Therapy
,
20
(2), 137-138.
https://doi.org/10.1080/14787210.2021.1960822
Chang, C. C., Senining, R., Kim,
J.,
& Goyal, R. (2020). An Acute Pulmonary
Coccidioidomycosis Coinfection in a Patient Presenting With Multifocal
Pneumonia With COVID-19.
Journal of Investigative Medicine High Impact Case
Reports
,
8
, 2324709620972244.
https://doi.org/10.1177/2324709620972244
Clancy, C.
J.,
& Nguyen, M. H. (2022). Coronavirus Disease 2019-Associated
Pulmonary Aspergillosis: Reframing the Debate.
Open Forum Infect Dis
,
9
(5),
ofac081.
https://doi.org/10.1093/ofid/ofac081
CLSI. (2010). Performance Standards for Antifungal Disk Diffusion Susceptibility
Testing of Filamentous Fungi; Informational Supplement CLSI document M51-
S1. In: Clinical and Laboratory Standards Institute Wayne.
Cordeiro, R. A., Brilhante, R. S. N., Rocha, M. F. G., Fechine, M. A. B., Camara, L.
M. C., Camargo, Z. P., & Sidrim,
J. J.
C. (2006). Phenotypic characterization
and ecological features of Coccidioides spp. from Northeast Brazil.
Medical
mycology
,
44
(7), 631-639.
https://doi.org/10.1080/13693780600876546
1460
David, F., Morais,
J.
R., Beires, F., Greenfield, H., & Fernandes, G. L. (2022).
Invasive Pulmonary Aspergillosis after COVID-19 Pneumonia.
Eur J Case Rep
Intern Med
,
9
(3), 003209.
https://doi.org/10.12890/2022_003209
De Carolis, E., Posteraro, B., Lass-Flörl, C., Vella, A., Florio, A. R., Torelli, R.,
Girmenia, C., Colozza, C., Tortorano, A. M., Sanguinetti, M., & Fadda, G.
(2012). Species identification of Aspergillus, Fusarium and Mucorales with
direct surface analysis by matrix-assisted laser desorption ionization time-of-
flight mass spectrometry.
Clinical Microbiology and Infection
,
18
(5), 475-484.
https://doi.org/https://doi.org/10.1111/j.1469-0691.2011.03599.x
Hart,
J.,
Dyer,
J.
R., Clark, B. M., McLellan, D. G., Perera, S., & Ferrari, P. (2012).
Travel-related disseminated Penicillium marneffei infection in a renal
transplant patient.
Transplant Infectious Disease
,
14
(4), 434-439.
https://doi.org/10.1111/j.1399-3062.2011.00700.x
Huang,
C.,
Wang, Y., Li, X., Ren, L., Zhao,
J.,
Hu, Y., Zhang, L., Fan,
G.,
Xu,
J.,
&
Gu, X. (2020). Clinical features of patients infected with 2019 novel
coronavirus in Wuhan, China.
The lancet
,
395
(10223), 497-506.
Jeong, W., Keighley, C., Wolfe, R., Lee, W. L., Slavin, M. A., Kong, D. C. M., &
Chen, S. C. (2019). The epidemiology and clinical manifestations of
mucormycosis: a systematic review and meta-analysis of case reports.
Clin
Microbiol Infect
,
25
(1), 26-34.
https://doi.org/10.1016/j.cmi.2018.07.011
Kantarcioglu, A. S., Sandoval-Denis, M., Aygun, G., Kiraz, N., Akman, C.,
Apaydin, H., Karaman, E., Guarro,
J.,
de Hoog, G. S., & Gurel, M. S. (2014).
First imported coccidioidomycosis in Turkey: A potential health risk for
laboratory workers outside endemic areas.
Medical mycology case reports
,
3
,
20-25.
https://pubmed.ncbi.nlm.nih.gov/24567896
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3930961/
Kidd, S., Halliday, C. L., Alexiou, H., & Ellis, D. H. (2016).
Descriptions of Medical
Fungi
. CutCut Digital.
https://books.google.iq/books?id=G95gjwEACAAJ
Koehler, P., Cornely, O. A., Böttiger, B. W., Dusse, F., Eichenauer, D. A., Fuchs,
F., Hallek, M., Jung, N., Klein, F., & Persigehl, T. (2020). COVID
‐
19 associated
pulmonary aspergillosis.
Mycoses
,
63
(6), 528-534.
Kumar, R., Shrivastava, S. K., & Chakraborti, A. (2010). Comparison of Broth
Dilution and Disc Diffusion Method for the Antifungal Susceptibility Testing of
Aspergillus flavus.
American Journal of Biomedical Sciences
, 202-208.
https://doi.org/10.5099/aj100300202
Kwon,
J.-H.,
Kim,
J.,
& Kim, W.-I. (2011). First Report ofRhizopus oryzaeas a
Postharvest Pathogen of Apple in Korea.
Mycobiology
,
39
(2).
Lei, H. L., Li, L. H., Chen, W. S., Song, W. N., He, Y., Hu, F. Y., Chen, X.
J.,
Cai,
W. P., & Tang, X. P. (2018). Susceptibility profile of echinocandins, azoles and
amphotericin B against yeast phase of Talaromyces marneffei isolated from
HIV-infected patients in Guangdong, China.
European Journal of Clinical
Microbiology & Infectious Diseases
,
37
(6), 1099-1102.
https://doi.org/10.1007/s10096-018-3222-x
Maitre,
T.,
Cottenet,
J.,
Godet,
C.,
Roussot,
A.,
Abdoul Carime,
N.,
Ok,
V.,
Parrot,
A.,
Bonniaud,
P.,
Quantin,
C.,
& Cadranel,
J.
(2021). Chronic Pulmonary
Aspergillosis: Prevalence, favouring pulmonary diseases and prognosis.
European Respiratory Journal
,
2003345.
https://doi.org/10.1183/13993003.03345-2020
1461
Manghwar, H., Naz, S., Gul, S., Chaudhary, H., & Munis, M. F. H. (2015). First
report of Rhizopus oryzae causing fruit rot of citrus medica L. in Pakistan.
JOURNAL OF PLANT PATHOLOGY
,
93
, 209-220.
Masci,
J.
R., & Wormser, G. P. (2005). Mandell, Douglas, and Bennett's Principles
and Practice of Infectious Diseases, 6th Edition Edited by Gerald L. Mandell,
John E. Bennett, and Raphael Dolin Philadelphia: Elsevier Churchill
Livingstone, 2005. 3661 pp., illustrated. $329 (cloth).
Clinical Infectious
Diseases: An Official Publication of the Infectious Diseases Society of America
,
41
(2), 277-277.
https://doi.org/10.1086/431221
Narayanasamy, S., Dougherty,
J.,
van Doorn, H. R., & Le, T. (2021). Pulmonary
Talaromycosis: A Window into the Immunopathogenesis of an Endemic
Mycosis.
Mycopathologia
,
186
(5), 707-715.
https://doi.org/10.1007/s11046-
021-00570-0
Nasir, N., Farooqi,
J.,
Mahmood, S. F., & Jabeen, K. (2020). COVID
‐
19
‐
associated
pulmonary aspergillosis (CAPA) in patients admitted with severe COVID
‐
19
pneumonia: an observational study from Pakistan.
Mycoses
,
63
(8), 766-770.
Nazir, S., Khan, A., Noor, A., Rehman, R., & Khalid, B. (2021). Mucormycoses in
Covid-19 Patients.
Pakistan Journal of Medical and Health Sciences
,
15
(9),
2837-2840.
https://doi.org/10.53350/pjmhs211592837
Pashley,
C. H.,
Fairs,
A.,
Morley,
J. P.,
Tailor,
S.,
Agbetile,
J.,
Bafadhel,
M.,
Brightling,
C. E.,
& Wardlaw,
A. J.
(2012). Routine processing procedures for
isolating filamentous fungi from respiratory sputum samples may
underestimate fungal prevalence.
Medical mycology
,
50
(4), 433-438.
Pemán,
J.,
Ruiz-Gaitán, A., García-Vidal, C., Salavert, M., Ramírez, P., Puchades,
F., García-Hita, M., Alastruey-Izquierdo, A., & Quindós, G. (2020). Fungal co-
infection in COVID-19 patients: Should we be concerned?
Revista
Iberoamericana
de
Micología
,
37
(2),
41-46.
https://doi.org/https://doi.org/10.1016/j.riam.2020.07.001
Prakash, H., Ghosh, A. K., Rudramurthy, S. M., Singh, P., Xess, I., Savio,
J.,
Pamidimukkala, U., Jillwin,
J.,
Varma, S., Das, A., Panda, N. K., Singh, S.,
Bal, A., & Chakrabarti, A. (2019). A prospective multicenter study on
mucormycosis in India: Epidemiology, diagnosis, and treatment.
Medical
mycology
,
57
(4), 395-402.
https://doi.org/10.1093/mmy/myy060
Pushparaj, K., Kuchi Bhotla, H., Arumugam, V. A., Pappusamy, M., Easwaran,
M., Liu, W. C., Issara, U., Rengasamy, K. R. R., Meyyazhagan, A., &
Balasubramanian, B. (2022). Mucormycosis (black fungus) ensuing COVID-19
and comorbidity meets - Magnifying global pandemic grieve and catastrophe
begins.
Sci Total Environ
,
805
,
150355.
https://doi.org/10.1016/j.scitotenv.2021.150355
Raoult, D., Zumla, A., Locatelli, F., Ippolito, G., & Kroemer, G. (2020).
Coronavirus infections: Epidemiological, clinical and immunological features
and hypotheses.
Cell stress
,
4
(4), 66.
Rutsaert, L., Steinfort, N., Van Hunsel, T., Bomans, P., Naesens, R., Mertes, H.,
Dits, H., & Van Regenmortel, N. (2020). COVID-19-associated invasive
pulmonary aspergillosis.
Ann Intensive Care
,
10
(1), 71.
https://doi.org/10.1186/s13613-020-00686-4
Satish, D., Joy, D., & Ross, A. B. (2021). Mucormycosis co-infection associated
with global COVID-19: A case series from India.
Int. J. Otorhinolaryngol. Head
Neck Surg
,
7
, 815-820.
1462
Schein,
F.,
Munoz-Pons,
H.,
Mahinc,
C.,
Grange,
R.,
Cathébras,
P.,
& Flori,
P.
(2020). Fatal aspergillosis complicating severe SARS-CoV-2 infection: A case
report.
Journal de mycologie medicale
,
30
(4), 101039.
https://doi.org/10.1016/j.mycmed.2020.101039
Sethuraman, N., Thirunarayan, M. A., Gopalakrishnan, R., Rudramurthy, S.,
Ramasubramanian, V., & Parameswaran, A. (2020). Talaromyces marneffei
Outside Endemic Areas in India: an Emerging Infection with Atypical Clinical
Presentations and Review of Published Reports from India.
Mycopathologia
.
Shah, A. S., Heidari, A., Civelli, V. F., Sharma, R., Clark, C. S., Munoz, A. D.,
Ragland, A. S., & Johnson, R. H. (2020). The Coincidence of 2 Epidemics,
Coccidioidomycosis and SARS-CoV-2: A Case Report.
Journal of Investigative
Medicine High Impact Case Reports
,
8
, 2324709620930540.
https://doi.org/10.1177/2324709620930540
Singh,
J.,
& Singh,
J.
(2020). COVID-19 and its impact on society.
Electronic
Research Journal of Social Sciences and Humanities
,
2
.
Taghizadeh-Armaki,
M.,
Hedayati,
M. T.,
Moqarabzadeh,
V.,
Ansari,
S.,
Mahdavi
Omran,
S.,
Zarrinfar,
H.,
Saber,
S.,
Verweij,
P. E.,
Denning,
D. W.,
&
Seyedmousavi,
S.
(2017). Effect of involved Aspergillus species on
galactomannan in bronchoalveolar lavage of patients with invasive
aspergillosis.
J
Med Microbiol
,
66
(7),
898-904.
https://doi.org/10.1099/jmm.0.000512
Thompson, G. R., 3rd, Barker, B. M., & Wiederhold, N. P. (2017). Large-Scale
Evaluation of In Vitro Amphotericin B, Triazole, and Echinocandin Activity
against Coccidioides Species from U.S. Institutions.
Antimicrobial agents and
chemotherapy
,
61
(4), e02634-02616.
https://doi.org/10.1128/AAC.02634-16
Uddin, K. N. (2021). Black fungus: a new threat.
BIRDEM Medical Journal
,
11
(3),
164-165.
WHO. (2020). World Health Organization Director-General opening remarks at the
media briefing on COVID-19-11 March 2020. In: Geneva, Switzerland.
Yang, X., Yu, Y., Xu,
J.,
Shu, H., Liu, H., Wu, Y., Zhang, L., Yu, Z., Fang, M., &
Yu, T. (2020). Clinical course and outcomes of critically ill patients with SARS-
CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective,
observational study.
The Lancet respiratory medicine
,
8
(5), 475-481.
Zarrinfar, H., Saber, S., Kordbacheh, P., Makimura, K., Fata, A., Geramishoar,
M., & Mirhendi, H. (2012). Mycological Microscopic and Culture Examination
of 400 Bronchoalveolar Lavage (BAL) Samples.
Iranian journal of public health
,
41
(7), 70-76.
https://pubmed.ncbi.nlm.nih.gov/23113213
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3469012/
Rinartha, K., & Suryasa, W. (2017). Comparative study for better result on
query suggestion of article searching with MySQL pattern matching and
Jaccard similarity. In
2017 5th International Conference on Cyber and IT
Service Management (CITSM)
(pp. 1-4). IEEE.
Widana, I.K., Sumetri, N.W., Sutapa, I.K., Suryasa, W. (2021). Anthropometric
measures for better cardiovascular and musculoskeletal health.
Computer
Applications in Engineering Education
,
29
(3), 550–561.
https://doi.org/10.1002/cae.22202
