Medical Mycology Advance Access published October 18, 2015

Medical Mycology, 2015, 00, 18

doi: 10.1093/mmy/myv075
Advance Access Publication Date: 0 2015
Original Article

Original Article

Emergence of Magnusiomyces capitatus

infections in Western Nepal

Department of Microbiology, Manipal College of Medical Sciences, Pokhara, Nepal and 2 Department of
Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India.

*To whom correspondence should be addressed. Hosuru Subramanya Supram, Lecturer, Dept. of Microbiology, Manipal
College of Medical Science, Pokhara, Nepal. Tel: +9779816642697; E-mail: supram.gowda@gmail.com
Received 28 February 2015; Revised 13 July 2015; Accepted 15 July 2015

Abstract
Magnusiomyces capitatus is an emerging opportunistic yeast in the Mediterranean region. We report from Nepal one case of M. capitatus infection and six other cases of
colonization/probable infection due to M. capitatus at a tertiary care center. Majority of
the patients were immunocompromised, at extreme age, associated with comorbidities,
and had history of close contact with livestock and poultry. The isolates were identified
by phenotypic and genotypic (ITS and D1/D2 region of 26S rDNA sequence) methods.
Molecular typing of the isolates was carried out by amplified fragment length polymorphism. Minimum inhibitory concentration (MIC) of the isolates for amphotericin B,
caspofungin, fluconazole, itraconazole, voriconazole, posaconazole, anidulafungin, and
micafungin were 2, 0.14, 2, 0.120.5, 0.120.5, 0.25, 14, and 14 g/ml, respectively.
Presence of M. capitatus infection was not known in Nepal, and the study should alert
the clinicians and infectious disease specialists.
Key words: Magnusiomyces capitatus, Blastoschizomyces capitatus, immunocompromised, emerging fungal
infection.

Introduction
Magnusiomyces capitatus1 is isolated from soil, beach sand,
poultry feces, and wood pulp.2,3 This saprobe can colonize
human skin, mucosa of respiratory tracts and gastrointestinal system. Magnusiomyces belong to Saccharomycetales.
Dipodascus and its anamorph Geotrichum are considered
as sister genera to the genus Magnusiomyces.4 The genus
Magnusiomyces currently contains fourteen species and its
anamorphic state is placed under genera Saprochaete. Magnusiomyces capitatus is an emerging opportunistic fungal
pathogen. Patients with neutropenia, hematologic malig-

nancies undergoing chemotherapy, on corticosteroids or

broad spectrum antibiotics therapy are at high risk of acquiring this infection. Surgery, drug abuse, catheters, and
low dose azole treatment have also been reported as predisposing factors.3 M. capitatus colonization may precede
invasive infection and hematogenous dissemination, often
giving rise to a wide and diverse spectrum of infections. The
mortality rate with this infection is quite high regardless of
antifungal treatment. Both superficial and systemic infections due to M. capitatus have been reported in immunocompetent hosts as well.5,6 The term emerging infection


C The Author 2015. Published by Oxford University Press on behalf of The International Society for Human and Animal Mycology.

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Hosuru Subramanya Supram1, , Shishir Gokhale1 ,

Arunaloke Chakrabarti2 , Shivaprakash M Rudramurthy2 ,
Sunita Gupta2 and Prasanna Honnavar2

may be used to denote an infection that has newly appeared

in the population or one that is rapidly increasing in incidence or geographic range.7 M. capitatus infection is well
documented to restricted areas with Mediterranean climate
like Italy, Spain, and France.8 Only few case reports have
been published from India and other Asian countries.5,9,10
Here, we report a series of seven cases with M. capitatus
isolation, one proven infection, and the other six as colonization/probable infections.

Cases

Methods
All clinical specimens were processed as per standard
procedures.11 The fungal isolates were identified as M.
capitatus by phenotypic characteristics and further confirmed by amplifying the 26S rDNA12 and ITS region of the rDNA13 at National Culture Collection of
Pathogenic Fungi (NCCPF), Postgraduate Institute of Medical Education and Research, Chandigarh, India. Amplified gene products were purified by a gel extraction kit
(QIAquick; Qiagen, Bengaluru, India). Sequencing polymerase chain reaction (PCR) was performed using the
Big Dye Terminator Cycle Sequencing kit, version 3.1
(Applied Biosystems, Foster City, CA). Purified PCR
products were analyzed on an ABI 3130 Genetic Analyzer (Applied Biosystems). The sequences were compared
with sequences in the CBS-KNAW Fungal Biodiversity
Centre database (http://www.cbs.knaw.nl/) and GenBank
DNA database (http://www.ncbi.nlm.nih.gov/Genbank/
index.html). Neighbor-joining method was used to infer the evolutionary history.14 The evolutionary distances
were computed using the maximum composite likelihood

method.15 MEGA5 package was used to perform evolutionary analyses.16

Molecular typing of M. capitatus strains was performed
by amplified fragment length polymorphism (AFLP) as
described earlier with some modification.17 EcoRI and
HindIII restriction enzymes (New England Biolabs, Ipswich, MA, USA) and corresponding adapters were used.
After pre-selective amplification, selective primers were
used [EcoRI (6-FAM labeled)] with two selective residues
(5 - GACTGCGTACCAATTCAC-3 ) and HindIII with
one selective residue (5 - GACTGCGTACCAGCTTT-3 )].
Capillary electrophoresis was performed in an ABI automated DNA Sequencer 3130. The similarity coefficient was
determined by Pearson correlation with negative similarities cliped to zero. Cluster analysis was performed by unweighted pair group method with arithmetic mean using
Bionumerics software version 7.1 (Applied Maths, Ghent,
Belgium).
In vitro antifungal susceptibility testing of M. capitatus isolates against fluconazole, itraconazole, voriconazole, posaconazole, caspofungin, anidulafungin, micafungin, and amphotericin B, were performed by micro titer
broth dilution method based on the Clinical and
Laboratory Standards Institute M27-A3 standard18 at
NCCPF, PGIMER, Chandigarh, India. Briefly, the susceptibility testing included RPMI supplemented with 2% glucose
as assay medium, inoculum size of 105 CFU/ml, flat-bottom
trays, and spectrophotometric reading. All microplates were
wrapped with a film sealer (to prevent dehydration of the
medium), and incubated at 30 C for 48 h. Candida parapsilosis ATCC 22019 and Candida krusei ATCC 6258 were
used as quality control strains.
One blood culture positive case was determined as confirmed invasive infection. The rest of the six cases were considered as probable cases (Table 1). The criteria for defining
invasive fungal disease (IFD) and probable IFD were in accordance with the revised definition of IFD from European
Organization for Research and Treatment of Cancer/ Invasive Fungal Infections Cooperative Group and the National
Institute of Allergy and Infectious Diseases Mycoses Study
Group (EORTC/MSG) Consensus Group.19

Results
The Gram stain of sputum, endotracheal aspirate, bronchial
aspirate, and pus from different cases revealed pus cells and
Gram positive septate hyphae and few yeast cells. Presence
of thin, septate, hyaline hyphae with narrow angle branching and pleomorphic yeast-like cells were seen in 10% KOH
wet mount. Periodic acid schiff (PAS) stain of the lung aspirate showed the presence of small fragments of hyphae with

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Case 1 was a 68 year-old man with type 2 diabetes mellitus, hypertension, and ischemic stroke. He had history
of recurrent lower respiratory tract infections for the past
three years. He was admitted with chief complaints of fever,
cough with expectoration, and dyspnoea for four days.
Based on clinical and radiological features, he was diagnosed as left lower zone community acquired pneumonia.
Sputum, bronchial aspirate and blood specimens collected
on the fifth and seventh days of admission yielded M. capitatus. The patient improved with fluconazole 400 mg per
day for two weeks and was discharged after 21 days of
admission.
The six other cases of varying clinical presentations were
observed to have M. capitatus colonization. The clinical and
microbiological profile of all the patients is summarized in
Table 1.

Medical Mycology, 2015, Vol. 00, No. 00

Subramanya Supram et al.

Table 1. Clinicomicrobiological profile of 7 patients from where Magnusiomyces capitatus was isolated.
1

Age (years)
and Gender

68
M

72
M

82
M

15
M

77
F

48
M

80
M

Department
and Ward

Medicine
ward

Medical ICU

Medicine
ward

Medicine
OPD

Medical ICU

Neurology
ICU

Medical ICU

Underlying
disease

CAP, DM-2,
hypertension,
ischemic CVA

Acute gastroenteritis,
bilateral lower
zone
pneumonia,
DM-2,
hypertension,
parkinsonism,
BPH

COPD

CAP

Aspiration
pneumonitis,
UTI, sepsis,
hypertension,
Alzheimers
disease

Traffic
accident, skull
bone fracture,
rib facture,
scalp injury,
perichondritis

COPD,
hypertension,
CAP, septic
shock

Total WBC
count ,
103 /l

14.5

13.5

8.3

12

13

20

14

Neutrophil at
diagnosis ,
(%)
Lymphocyte ,
(%)

89

78

82

80

75

94

90

11

22

18

20

25

06

10

Days of
persistent
fungemia

16

NA

NA

NA

NA

NA

NA

Immunosuppression
(With primary
reason)

No

No

Steroids
(COPD)

No

No

No

Steroids
(COPD)

Specimen
whence M.
capitatus was
isolated

Sputum,
bronchial
aspirate,
blood

Bronchial
aspirate, lung
aspirate (post
mortem)

Sputum,
endotracheal
aspirate

Sputum

Endotracheal
aspirate,

Pus

Sputum,
broncheal
aspirate

Concomitant
microorganisms isolated
(site of
isolation)

Nil

E. coli - ESBL
producer
(bronchial
aspirate)

Nil

Nil

Flavobacter
spp.
(endotracheal
aspirate)

Candida
alibicans and
Klebsiella
pneumoniae,
(pus)

Nil

Broad
spectrum
antibiotics

Yes

Yes

No

No

Yes

Yes

Yes

Antifungal
therapy

Fluconazole
(400mg/day
for 2 weeks)

No antifungal
therapy

Fluconazole
(400mg/day
for 2 weeks)

No antifungal
therapy

No antifungal
therapy

Clotrimazole
(topical)

Fluconazole
(400mg/day
for 4 days)

Days from
collection of
first positive
sample to
start of
antifungal
treatment

5 days

NA

3 days

NA

NA

NA

3 days

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Case No.

Medical Mycology, 2015, Vol. 00, No. 00

Table 1. Continued.
1

Outcome
(cause of
death)

Alive, no
relapse

Died on 5th
day of
admission
(cardiorespiratory
failure)

Alive, no
relapse

Not known
(lost on
follow up)

Died on 6th
day of
admission,
(aspiration
pneumonitis,
septic shock,
UTI)

Alive, no
relapse

Died on 7 th
day of
admission
(CPA, septic
shock)

Travel history
to foreign
country
(endemic area)

None

None

None

None

None

None

None

History of
animal
contact

Yes1

Not known

Yes 2

Yes 2

No contact
since past 2
years

Yes 2

Yes 2

Etiological
significance of
M capitatus

Confirmed

Probable

Probable

Probable

Probable

Probable

Probable

Clearance of
fungus after
treatment

Cleared

NA

Cleared

NA

NA

NA

NA

Note: CAP: community acquired pneumonia, ICU: intensive care unit, DM: diabetes mellitus, COPD: chronic obstructive pulmonary disorder, CVA: cerebrovascular
accident, NA: not applicable, UTI: urinary tract infection, ESBL: extended spectrum beta lactamase, BPH: benign prostatic hypertrophy.
1
Contact with poultry.
2
Contact with poultry and farm animals.

Counts at the time of etiological diagnosis.

a few yeast cells. Pure growth of rapidly growing white to

cream colored yeastlike colonies were grown on SDA with
chloramphenicol and SDA with cycloheximide incubated
at 27 C and 37 C for 48 hours. Blood culture from case
number 1, revealed pure growth of dry, white to cream colored yeast like colonies after 4 days of incubation at 37 C,
which was morphologically similar to bronchial aspirate
culture isolate. Microscopic characterization of the fungal
isolates was carried out by Gram stain and Lactophenol
cotton blue [LPCB] mount. It showed true hyphae, pseudohyphae and annelloconidia resembling arthroconidia. The
organism grew at 45 C as well. The isolates assimilated glucose and galactose but did not hydrolyse urea. Sequences of
the 26S rDNA and the ITS region of rDNA showed 99%
identity with the sequences of the M. capitatus (U40084 and
KP13240220 respectively). The phylogenetic relationship of
M. capitatus is shown in Fig. 1.
All the sequences of M. capitatus have been deposited in the GenBank database (http://www.ncbi.nlm.nih.
gov/Genbank/index.html) with the accession numbers
KT005305 to KT005311 (26S region of rDNA) and
KT005312 to KT005317 (ITS region of rDNA). The isolates have been deposited at NCCPF, PGIMER, Chandigarh, India as NCCPF480014NCCPF480020.

The fragments ranging from 30 to 475 bp were included

for AFLP analysis. Except the strain NCCPF480020, all the
remaining M. capitatus strains formed a tight cluster with
85% similarity coefficient (Fig. 2).
The minimum inhibitory concentrations (MIC) results for different antifungal agents are summarized in
Table 2. Clinical breakpoints values for M. capitatus are
not available.21,22 A short range of MIC for each antifungal agent was observed. The MIC of amphotericin B and
fluconazole for all seven isolates was 2 g/ml. Cases 1 and
3 responded to empirical treatment with fluconazole, and
clearance of fungus was documented. All isolates were likely
to be resistant to amphotericin B (MIC = 2 g/ml).23 Low
MIC values ranging from 0.12 to 0.5 g/ml were noted for
itraconazole, voriconazole, and posaconazole. The MIC of
the echinocandins: caspofungin, micafungin and anidulafungin were similar for all isolates (1 to 4 g/ml), except
case 5, where low MIC for caspofungin (0.12 g/ml) was
seen.
Specimens from case number one and three were collected a week after administration of antifungals and at the
end of the treatment regime, M. capitatus was not detected
by microscopic examination and culture in any of those
specimens, indicating a successful treatment.

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Case No.

Subramanya Supram et al.

Figure 2. UPGMA dendrogram showing the comparison of AFLP fingerprints of M. capitatus strains.

Table 2. In vitro antifungal susceptibility profile by micro titer broth dilution.

Antifungal agent

Case 1

Amphotericin B
Fluconazole
Itraconazole
Voriconazole
Posaconazole
Caspofungin
Anidulafungin
Micafungin

2
2
0.12
0.12
0.25
1
1
1

MIC (g/ml) for Magnusiomyces capitatus isolates

Case 2
Case 3
Case 4
2
2
0.5
0.12
0.25
1
1
1

2
2
0.5
0.5
0.25
4
4
4

2
2
0.5
0.25
0.25
1
1
1

Case 5

Case 6

Case 7

2
2
0.5
0.25
0.25
0.12
2
2

2
2
0.5
0.12
0.25
1
1
1

2
2
0.5
0.12
0.25
2
2
2

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Figure 1. The phylogram of all the M. capitatus isolates were generated using maximum composite likelihood method with 1000 bootstrap (a) D1/D2
regions of the 26S rDNA; (b) ITS5.8S rDNA

Discussion

in six of our cases, as the fungus was isolated from nonsterile sites. Histopathology of deep tissue though important
to confirm invasive infection, it is difficult to perform in
immunosuppressed patients.
Mortality from emerging fungal infections in the immunocompromised patients remains alarmingly high due
to lack of clinical suspicion and delay in diagnosis. Clinicians and microbiologists must recognize the potential risk
for these emerging fungal infections, as well as the risk factors involved therein. In our cases, the mortality may be
due to the fungal infection or comorbidities as the patients
were immunocompromised, and at the extremes of ages.
The antifungal susceptibility reports in our patients were
not available before commencement of therapy. The decision to start empirical antifungal therapy was arrived at
after discussion between the treating physician and the microbiologist. The clinical profile, risk factors, Gram stain
and culture findings contributed to the decision making.
Early appropriate therapy may improve clinical outcome.
At present the treatment of this rare infection is not clearly
defined.4,22,25,31 The MIC breakpoints for interpretation of
in vitro susceptibility results have not been defined but antifungal susceptibility testing of the isolated organism is
highly recommended.16 MIC values of fluconazole were
low compared to other studies (MIC between 16 and
32 mg/L).22,24 Among the azoles, voriconazole, posaconazole and itraconazole appear to be more active in vitro
than fluconazole.32,33 M. capitatus is considered intrinsically resistant to echinocandins.31 Few authors have suggested M. capitatus breakthrough infections in neutropenic
patients receiving echinocandins.34,35 Treatment decisions
need careful consideration of the institutional epidemiological factors and the immune status of the population at risk.

Conclusion
Emergence of M. capitatus infection in Nepal should alert
clinicians and infectious disease specialists. All fungi recovered from immunocompromised patients should be identified and reported, to establish their clinical and epidemiological significance.

Acknowledgments
We thank Dr. Shankar Baral, resident, Internal medicine, Manipal
Teaching Hospital, for clinical evaluation of cases and specimen collection. We also appreciate the assistance of the entire laboratory staff
and faculty, Department of Microbiology and Pathology, MCOMS,
Pokhara. We also extended special thanks to Dr. P Y Prakash,
In-charge Medical Mycology Laboratory, KMC, Manipal University, India for his valuable suggestions. We also thank the Indian
Council of Medical Research for their financial help for sequencing,

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M. capitatus is an emerging opportunistic fungal pathogen

especially in immunosuppressed individuals. It can colonize
the skin, bronchial and intestinal tract of healthy people and
produce serious opportunistic infections in patients with
hematological malignancies undergoing chemotherapy, especially with acute leukemia.2426 This fungus was previously considered as normal flora or harmless colonizer,
but recently it has been gaining importance as an emerging opportunistic pathogen. Progressive increase in number
of cases with M. capitatus infections from new geographical areas indicates the possibility of silent spreading of the
disease from endemic areas to non-endemic areas,5,9,23 or
is being identified now with better diagnostic tools.
Tissue invasion by this fungus could be proven only in
one case in this series. Other six patients probably had
colonization. Though the case 2 describes a positive postmortem lung aspirate and the patient had pulmonary infection, it could not rule out postmortem bronchial tree colonization. Most of the patients in this study were elderly;
six were more than 60 years while one was 16 years of
age. Extreme of age associated with comorbidities is additional risk for the opportunistic emerging fungal infections.
Most of patients in this study had close contact with poultry and/or farm animals, but no strong evidence regarding
transmission of the fungus from the animals to humans is
established.
The emergence of M. capitatus infection in nonendemic areas has been attributed to local effects of global
warming.27,28 The present series does not support this hypothesis, as our cases were recorded during August 2013
to April 2014, when the environmental temperature varies
widely at Pokhara. The cases in this report can represent a
cluster as they were noted over short period of time. In the
literature common hospital source has been advocated for
several clusters29 and more recently, it has been confirmed
by sequencing that this fungus in milk vacuum flasks was
the origin of an outbreak in four patients in Barcelona.30 In
our isolates no single nucleotide variation was observed in
405 bp and 469 bp nucleotides in 26S rDNA and ITS region
respectively. All the isolates were having 80% similarity
in AFLP profile. Therefore, the sequence results and tight
cluster formation in AFLP profile indicate that our isolates
had clonal origin.
This is the first study where M. capitatus was isolated as
a pathogen in Nepal. Isolation of M. capitatus from clinical
specimens is technically not difficult, but it does not necessarily indicate invasion unless the fungus is isolated from
deep tissue. The lack of specific clinical, radiographic, and
histological features and the absence of surrogate markers
hamper proper diagnosis. The infection could not be proven

Medical Mycology, 2015, Vol. 00, No. 00

Subramanya Supram et al.

molecular typing and antifungal susceptibility testing at PGIMER,

Chandigarh.

Authors contributions

Funding Information
This work was supported by the Indian Council of Medical Research,
New Delhi for performing molecular characterization and antifungal
susceptibility testing under two different projects.

Declaration of interest
The authors report no conflicts of interest. The authors alone are
responsible for the content and the writing of the paper.

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H S Supram observed the incidence and cases, collected specimens, performed the phenotyping, followed the cases and wrote the
manuscript. P Honnavar performed molecular identification and typing; S M Rudramurthy performed molecular analysis, S Gupta performed phenotypic characterization and antifungal susceptibility. In
addition to supervision of all activities related to this manuscript
at PGIMER, A Chakrabarti also interpreted the antifungal susceptibility, taxonomy and did critical evaluation of the manuscript. S.
Gokhale contributed toward providing clinical relevance, distilling
the material, and manuscript preparation.

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