deep fungal and higher bacterial skin infections in thailand: clinical manifestations and treatment...
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Deep fungal and higher bacterial skin infections in Thailand:clinical manifestations and treatment regimens
Punkae Mahaisavariya, MD, Angkana Chaiprasert, Dr.rer.nat., Apichati Sivayathorn, MD,and Supakan Khemngern, MABS
From the Departments of AbstractDermatology and Microbiology, Background Deep fungal and higher bacterial skin infections occur fairly frequently inFaculty of Medicine, Siriraj Hospital, Thailand.Mahidol University, Bangkok, Thailand
Methods Cases with a provisional diagnosis of deep fungal and higher bacterial
infections were prospectively collected from 1994 to 1997 in the Granuloma Clinic,CorrespondencePunkae Mahaisavariya, MD Department of Dermatology, Faculty of Medicine, Siriraj Hospital, Mahidol University,Siriraj Hospital, 2 Prannok Rd Bangkok, Thailand. Demographic data, clinical manifestations, causative organisms,Bangkoknoi, Bangkok 10700 histologic features, treatment, and outcome were investigated.Thailand
Results The total cases in a 4-year period numbered 27. The male to female ratio was
approximately 1 : 1. Mycetoma was most common, followed by chromoblastomycosis.Supported by Siriraj-China Medical
Actinomycetoma was similar in incidence to eumycetoma. The only causative organismBoard, Faculty Research Grant,
that could be identified among the mycetoma cases was Cladosporium carrionii, whichFaculty of Medicine, Siriraj Hospital,caused mycetoma of the buttock of an aplastic anemia patient at the site of bone marrowMahidol University, Bangkok, Thailand
aspiration. Surgical treatment was recommended for eumycetoma. Chromoblastomycosis
was caused by C. carrionii and F. compactum and responded well with itraconazole orally.
Mycotic abscesses were found in four cases, basidiobolomycosis in two cases, and
cutaneous nocardiosis in one case. Cotrimoxazole was recommended in the treatment of
actinomycetoma, cutaneous nocardiosis, and basidiobolomycosis.
Conclusions Localized, chronic, slow, progressive, and usually asymptomatic were the
main cutaneous manifestations of deep fungal and higher bacterial skin infections. A skin
biopsy for histologic study and culture identification should be performed in every
suspected case. The causative organisms were found in the histologic sections of every
case, but only about one-third were found by culture.
Introduction
Deep fungal and higher bacterial skin infections occur
primarily in tropical and subtropical regions. The etiologic
agents are traumatically introduced into tissue, usually
through occupational exposure. The skin lesions enlarge
slowly and often asymptomatically so that it may be a
long time, months to years, before treatment is sought.
Mycetoma and chromoblastomycosis are the well-known
entities of this group, but a variety of cutaneous mani-
festations can also occur. The diagnosis is confirmed by
histopathologic study and culture identification from skin
lesions. Surgical and/or medical treatment is chosen accord-
ing to the etiologic agent and clinical lesion.
In this series, cases were collected with a provisional
diagnosis of deep fungal infections primarily or by referral
© 1999 Blackwell Science Ltd International Journal of Dermatology 1999, 38, 279–284
279
from other physicians. The demographic data, clinical
manifestations, causative organisms, and treatment regi-
mens were investigated.
Materials and methods
Twenty-seven patients, 13 men and 14 women, were examined
in the Granuloma Clinic, Department of Dermatology, Faculty of
Medicine, Siriraj Hospital, Mahidol University, Bangkok,
Thailand, during the years 1994–1997, with chronic, mostly
asymptomatic, slow, progressive skin lesions suspicious of
deep fungal and higher bacterial infections. Skin biopsy was
taken from the lesions for histopathologic study and culture
identification of the causative organisms. Special staining for
fungal identification, Gomori–Methenamine Silver (GMS) and
Periodic Acid–Schiff (PAS), and acid fast staining were
280 Report Deep fungal and higher bacterial skin infections in Thailand Mahaisavariya et al.
performed in addition to hematoxylin and eosin staining. For
mycologic and higher bacterial culture, each biopsy specimen
was cut into very small pieces using a sterile technique and
then inoculated on four slants of Sabouraud dextrose agar
(SDA) and SDA plus chloramphenicol (50 µg/mL). All tubes
were incubated at room temperature and examined for visible
colonies every week until 6 weeks. The fungi or bacteria were
identified by macroscopic morphology, microscopic morphology,
staining properties, and some biochemical characteristics.
Demographic data, character of the skin lesion (site, size,
number, morphology), histologic findings, microbiologic
findings, and treatment modalities were recorded.
Results
Demographic dataFrom a total of 27 cases, 13 were men and 14 were women
(age 15–67 years; mean, 46.85 6 16.19 years). Thirteen
cases were field workers, eight housewives, two factory
employees, and one each a teacher, soldier, shop-keeper,
and clerk. Seventeen cases came from rural areas and ten
cases lived in big cities. Only two cases were immunocom-
promised from their underlying diseases: one had nephrotic
syndrome and was being treated with corticosteroid (Case
3, Table 1) and one had aplastic anemia (Case 7).
Clinical manifestations and causative organismsThe main causative organisms were found in two groups:
filamentous higher bacteria and true fungi. Filamentous
higher bacteria caused actinomycotic mycetoma and cuta-
neous nocardiosis. The cutaneous lesions caused by true
fungi were of four types: mycetoma, chromoblastomycosis,
mycotic abscesses, and basidiobolomycosis (Table 2).
Mycetoma, which is characterized by a firm, usually
painless, tumor-like mass with a sinus tract discharging
pus that contains granules or grains of the causal agent,
was found in 14 cases. Half of the mycetoma cases were
caused by filamentous higher bacteria and the other half
were caused by true fungi, dematiaceous fungi (four cases),
and hyaline molds (three cases). Only a single lesion was
found in each patient and the common site was the foot
(ten cases) (Table 1). The other four skin lesions were
found on the thigh (Cases 3 and 14), left chest wall without
history of previous trauma (Case 12), and at the site of
bone marrow aspiration on the left buttock of an aplastic
anemia patient (Case 7). The causative organism was
found as sulfur granules for actinomycotic mycetoma or
eumycotic grains, either black or hyaline fungi, for
mycetoma in the histologic section of every case, but culture
identification was performed in only 10 cases. Two cases
of actinomycotic mycetoma and two cases of eumycotic
mycetoma were not cultured (Table 2). Five actinomycotic
cases that were cultured revealed no growth. Five eumycotic
International Journal of Dermatology 1999, 38, 279–284 © 1999 Blackwell Science Ltd
cases showed no growth in two cases, and a fungal colony
in three specimens. Cladosporium carrionii was identified
from one specimen and the other two specimens were
nonsporulate septate hyaline fungi.
Chromoblastomycosis was found in six cases. The char-
acteristic verrucous hyperkeratotic plaque with a black
dot was found in three cases. Another three cases were
violaceous hyperkeratotic annular plaque (Case 16), hyper-
keratotic nodule (Case 19), and subcutaneous nodule (Case
20). C. carrionii was identified from three specimens,
F. compactum from one specimen, and the other two cases
were not cultured.
Mycotic abscesses, which are characterized by a soft,
cystic mass without or with a very slight sign of inflamma-
tion, were found in four cases: as a single lesion in three
cases and multiple lesions in one case. Disseminated mycotic
abscesses were caused by Penicillium marneffei (Case 24).
In three patients who had single lesions the causative
organisms were found in the abscess in histologic section
as hyaline septate hyphae in one case, which was identified
as Acremonium species (Case 23), and as brown septate
hyphae in the other two cases, which grew nonsporulate
septate black mold in one case (Case 22) and the other
case was not cultured (Case 21).
Basidiobolomycosis, which is the rare form of deep
fungal infection caused by nonseptate fungi, characterized
by a slow-growing, asymptomatic, plate-like lump, was
found in two cases (Cases 25 and 26). The causative
organism was identified as Basidiobolus ranarum in both
cases.
Cutaneous nocardiosis was found in one case (Case 27)
which manifested as a single hyperkeratotic nodule on the
dorsum of the hand. The causative organism was identified
as Nocardia asteroides.
Histologic findings
Suppurative granuloma was the main histopathologic find-
ing in all lesions. Pseudoepitheliomatous hyperplasia of the
epidermis was the associated feature in chromoblasto-
mycosis. Mycotic abscesses were found in the deep dermis
with granuloma formation surrounded by fibrous capsules
at the wall of the abscess. Dematiaceous fungi were easily
seen in hematoxylin and eosin stained sections. Hyaline
fungi were detected by special stains (GMS and PAS).
Actinomycotic grains, sulfur granules, which appeared as
round to oval bodies up to 300 µm in diameter, composed
of clumped colonies of bacteria with peripherally radiating
club-shaped filaments (Splendore–Hoeppli phenomenon),
were found within microabscesses in suppurative granul-
oma in hematoxylin and eosin stained and specially
stained sections.
Mahaisavariya et al. Deep fungal and higher bacterial skin infections in Thailand Report 281
Table 1 Character of the patients, treatment, and outcome
No. Sex Age Site Diagnosis Histology Culture Treatment Outcome/follow-up
(years) (months) (months)
1 F 33 Foot Eumycetoma Hyaline eumycotic grain Nonsporulate Itraconazole (48) Not improved
septate mold
2 F 27 Foot Eumycetoma Hyaline eumycotic grain NG† Itraconazole (36) Not improved (36)
3 F 35 Thigh Eumycetoma Hyaline eumycotic grain Nonsporulate Excision Cure (12)
septate mold
4 M 44 Foot Eumycetoma Black eumycotic grain ND* No treatment Loss to follow-up
5 F 42 Foot Eumycetoma Black eumycotic grain ND Excision Cure (12)
6 M 52 Buttock Eumycetoma Black eumycotic grain NG Itraconazole (24) Slightly improved (24)
7 M 52 Buttock Eumycetoma Suppurative granuloma C. carrionii Amphotericin B Cure (24)
8 F 22 Foot Actinomycetoma Sulfur granule NG Cotrimoxazole (8) Cure (12)
9 F 60 Foot Actinomycetoma Sulfur granule NG Cotrimoxazole (8) SCC on top scar (14)
10 M 41 Foot Actinomycetoma Sulfur granule ND Cotrimoxazole (3) Cure (18)
11 M 43 Foot Actinomycetoma Sulfur granule NG Cotrimoxazole (3) Loss to follow-up
12 F 61 Chest wall Actinomycetoma Sulfur granule ND Cotrimoxazole (9) Cure (12)
13 F 23 Foot Actinomycetoma Sulfur granule ND Cotrimoxazole (9) Cure (12)
14 M 63 Thigh Actinomycetoma Sulfur granule NG Cotrimoxazole (2) Improved (still follow-up)
15 M 49 Leg Chromoblastomycosis Medlar body F. compactum Itraconazole (18) Cure (18)
16 M 57 Forearm Chromoblastomycosis Pseudoepitheliomatous C. carrionii Itraconazole Cure (24)
hyperplasia with mixed cell
granuloma
17 M 67 Leg Chromoblastomycosis Medlar body C. carrionii Itraconazole (8) Cure (14)
18 M 65 Arm Chromoblastomycosis Pseudoepitheliomatous C. carrionii Itraconazole (2) Improved (2)
hyperplasia with mixed cell
granuloma
19 F 63 Wrist Chromoblastomycosis Medlar body ND Excision Cure (6)
20 F 62 Foot Chromoblastomycosis Suppurative granuloma with ND Excision Cure (12)
brown hyphae
21 F 42 Buttock Pheohyphomycosis Clump of black hyphae ND Excision Cure (24)
22 F 80 Foot Pheohyphomycosis Brown hyphae Nonsporulate Excision Cure (24)
septate mold
23 M 67 Shin Mycotic abscess Hyaline hyphae Acremonium Excision Cure (23)
24 F 57 Disseminate Penicilliosis Abscess with yeast-like organism P. marneffei Itraconazole (15) Not improved (24)
25 F 38 Arm Basidiobolomycosis Broad, nonseptate hyphae with B. ranarum Cotrimoxazole (3) Cure (24)
Splendore–Hoeppli phenomenon
26 F 15 Abdomen Basidiobolomycosis Broad, nonseptate hyphae with B. ranarum Cotrimoxazole (24) Much improved (24)
and thigh Splendore–Hoeppli phenomenon
27 M 62 Finger Nocardiosis Mixed cell granuloma N. asteroides Cotrimoxazole (2) Improved (2)
*ND, not done. †NG, no growth.
Treatment regimensActinomycotic mycetoma, cutaneous nocardiosis, and
basidiobolomycosis were treated with cotrimoxazole, two
tablets twice daily orally, with a favorable response. The
patients were treated until the skin lesions were completely
resolved. The duration of treatment ranged from 3 to 8
months. For eumycotic cases, mycetoma, mycotic abscesses,
and chromoblastomycosis, surgical excision was the curat-
ive treatment. In cases where surgical treatment could not
be performed easily or complete surgical excision could
not be carried out, antifungal drugs, i.e. itraconazole and
amphotericin B, were tried. Most cases were cured after a
single surgical procedure, except for one case with a deep
mycotic abscess on the buttock which was excised three
© 1999 Blackwell Science Ltd International Journal of Dermatology 1999, 38, 279–284
times. Itraconazole was tried at a dosage of 200 mg daily
with a favorable result for chromoblastomycosis, but not
for mycetoma and disseminated mycotic abscesses caused
by P. marneffei. The duration of treatment for chromoblas-
tomycosis caused by C. carrionii and F. compactum ranged
from 5 to 18 months. Amphotericin B was tried in one
case of mycetoma with aplastic anemia with a cumulative
dose of 1 g. The patient responded quite well and the
lesion healed completely after 3 months of treatment
without relapse during 2 years of follow-up.
Discussion
Thailand is an agricultural country in a subtropical region
with hot and humid weather all year round. Both the
282 Report Deep fungal and higher bacterial skin infections in Thailand Mahaisavariya et al.
Table 2 Summary of causative organisms, treatment, and outcome
Diagnosis ( n) Organisms ( n) Treatment ( n) Outcome ( n)
Mycetoma (14)Eumycetomic (7) C. carrionii (1) Itraconazole (3) Cure (3)Hyaline (3) Nonsporulate (2) Amphotericin B (1) Not cured (3)Dematiaceous (4) NG* (2), ND† (2) Excision (2)‡ Loss to follow-up (1)Actinomycotic (7) NG (5) Cotrimoxazole (7) Cure (5)
ND (2) Improved (2)Chromoblastomycosis (6) F. compactum (1) Itraconazole (4) Cure (6)
C. carrionii (3) Excision (2)ND (2)
Mycotic abscess (4) Acremonium (1) Excision (3) Cure (3)Single (3) P. marneffei (1) Itraconazole (1) Not cured (1)Multiple (1) Nonsporulate (1)
ND (1)Basidiobolomycosis (2) B. ranarum (2) Cotrimoxazole (2) Cure (1)
Much improved (1)Nocardiosis (1) N. asteroides (1) Cotrimoxazole (1) Cure (1)
*NG, no growth. †ND, not done. ‡One case was lost to follow-up. n, number of cases.
geography and the way of life are important factors in
acquiring deep fungal and higher bacterial skin infections.
Our patients came from all parts of the country, both
urban and rural areas. Middle-aged farmers predominated.
The sites of predilection were the extremities, especially
the hands and feet, as previously reported,1–4 which might
support traumatic inoculations as the route of entry of the
organism although most of them could not be recognized.
Uncommon locations, such as the head and neck,3,5,6 back,
and perineum,3 were not found in our series. Mycetoma
was most common, followed by chromoblastomycosis. The
causative organisms were found in al histologic sections,
but not in all cultures.
The mycetoma cases in our series were caused by actino-
mycetes and fungi, in equal number, which was different
from the report from Brazil4 stating that actinomycetoma
was about twice as common as the eumycotic form. The
most common organism of eumycetoma are Madurellagrisea,3,4 M. mycetomatis,3,4 Scedosporium apiospermum,4
Acremonium kiliense,3 A. falciforme,3,7 and Pyrenochaetaromeroi.3 Rare species that have been reported include
Arthrographis kalrae8 and Microsporum audouinii.6 In our
series, only three cases could be cultured. The only single
case was identified as C. carrionii and was successfully
treated with amphotericin B. The other two cases could
not be identified due to nonsporulation. Surgical treatment
was more effective than itraconazole for eumycetoma cases
in our series. A combination of medical and surgical
treatment was recommended in previous reports.1,9,10
Encouraging improvement was reported in the treatment
of eumycetoma due to M. grisea8 and A. falciforme7 with
itraconazole. Oral ketoconazole at a dosage of 400 mg
International Journal of Dermatology 1999, 38, 279–284 © 1999 Blackwell Science Ltd
daily for 8 to 24 months was tired in 10 eumycetoma cases
due to M. grisea, M. mycetomatis, P. romeroi, A. kiliense,
and A. falciforme with favorable results.3 Cotrimoxazole
was recommended for the treatment of actino-
mycetoma.1,5,9–12 In severe and recalcitrant cases, amikacin,
either alone or in combination with cotrimoxazole,13 and
amoxycillin plus clavulanic acid14 were recommended.
The causative organisms of chromoblastomycosis in our
series were C. carrionii and F. compactum which were the
common species in previous reports.15–19 The patients
responded well with itraconazole as well as surgical
treatment.
Mycotic abscess has seldom been reported in the litera-
ture. Both hyaline and dematiaceous fungi, as well as
higher bacteria (Nocardia species), could be the causative
organisms. The species that have been reported include
Exophiala jeanselmei,20 Phialaphora gougerotii,21
Pseudallescheria boydii,22 and Nocardia otitidiscaviarum.23
Our cases were caused by both hyaline and dematiaceous
fungi. Only hyaline fungi were identified as Acremoniumspecies and P. marneffei. Disseminated penicilliosis caused
by P. marneffei is one of the most common opportunistic
infections in AIDS patients in northern Thailand.24,25 The
cutaneous manifestations that have been reported include
multiple umbilicated papules,24,26 predominantly on the
face and upper extremities, palatal papules,24 and chronic
genital ulcer.24 Bamboo rat is the only known nonhuman
host of P. marneffei, but a history of exposure to or
consumption of bamboo rat was not a risk factor for
infection in AIDS patients.27 In addition, it occurs more
commonly in the rainy season.25 Chariyalertsak et al.25
suggested that an environmental reservoir of organisms in
Mahaisavariya et al. Deep fungal and higher bacterial skin infections in Thailand Report 283
the soil may be associated with P. marneffei infections.
Our patient who had disseminated penicilliosis manifested
differently from the previous report. She was an HIV-
negative patient and did not have any underlying disease
which would cause an immunodeficiency state. P. marneffeiwas cultured from the skin lesions, which were multiple,
large, cystic masses, and from the bone marrow aspiration.
She lived in the central part of Thailand and her neighbor
raised bamboo rat for sale. Amphotericin B,25,28 ketocona-
zole,25 and itraconazole25,29 were reported to yield success-
ful treatment of penicilliosis. Our patient responded to
initial itraconazole therapy, but she had many recurrences
during a 2-year follow-up period. She was lost to follow-
up until 1 year later when we were informed that she had
died from this illness.
Basidiobolomycosis is an uncommon deep mycosis in
the entomophthoromycosis group which has been
reported from Africa and Latin America. The reported
species include Basidiobolus haptosporus30–33 and
B. meristosporus, which is a saprophyte of amphibians
and reptiles.34 The causative organism in our cases was
B. ranarum which is now the correct name for the species
described in the previous reports. The clinical manifestation
was characterized by a hard, deep, non-tender, infiltrating,
slowly progressive plaque, which can simulate deep sclero-
derma,35 a tumoral disease,35 or elephantiasis.36 The correct
diagnosis can be made by histologic study and culture.
The diagnostic histologic features were broad, nonseptate
hyphae surrounded by eosinophilic material (Splendore–
Hoeppli phenomenon) in mixed cell granuloma with
numerous eosinophils. The sites reported include the
trunk,34,35 buttock,35 shoulder,34 and upper part of the
limbs.35,36 They have been successfully treated by potassium
iodide, either alone32,33 or in combination with ketocona-
zole,30 itraconazole,35 and cotrimoxazole.32,36 Our cases
responded well with cotrimoxazole without any side-
effects.
Nocardia species can cause a variety of cutaneous mani-
festations that include mycetoma,38,39 lymphocutaneous
syndrome (sporotrichoid),38,39 superficial skin infections
such as pyoderma,38–40 pustules,41 cellulitis,39 subcutane-
ous nodules,42 and abscess.23 The reported species include
Nocardia brasiliensis,39,41 N. asteroides,39,42 and
N. caviae43 (N. otitidiscaviarum).23 The patients were
successfully treated with sulfur drugs, such as sulfon-
amide,39 cotrimoxazole,39,41 and dapsone, either alone or
in combination with other drugs, such as amikacin41
or minocycline.40 Our case presented with a hyperkeratotic
nodule caused by N. asteroides and responded well to
cotrimoxazole.
Conclusions
Deep fungal and higher bacterial infections are localized,
chronic, and slowly progressive skin diseases which are
© 1999 Blackwell Science Ltd International Journal of Dermatology 1999, 38, 279–284
rarely fatal but disfigure the affected parts. The causative
organisms can be found by histologic study and culture.
Mycetoma was the most common form in this group, with
the feet most commonly affected. Mycotic abscess and
basidiobolomycosis were the uncommon types. The extra-
ordinary case in our series was an HIV-negative woman who
had multiple disseminated abscesses caused by P. marneffei.Surgical treatment was recommended for the therapy of
eumycetoma and single mycotic abscess. Itraconazole was
effective for chromoblastomycosis caused by F. compactumand C. carrionii. Cotrimoxazole was effective for actinomy-
cotic mycetoma, cutaneous nocardiosis, and basidiobolo-
mycosis.
Acknowledgment
Professor Visanu Thamlikithul, MD, Chief of Clinical
Epidemiology Unit, Office for Research and Development,
Faculty of Medicine, Siriraj Hospital, Mahidol University,
assisted in the project.
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