125
REVIEW ARTICLES
Infection Due to Penicillium marneffei, an Emerging Pathogen: Review of 155
Reported Cases
Tuan Anh Duong
From the Department of Medical Microbiology and Immunology,
University of Wisconsin, Madison, Wisconsin
A disseminated and progressive infection, penicilliosis marneffei is the third most common opportunistic infection in human immunodeficiency virus (HIV)-infected patients in certain parts of
Southeast Asia. Penicillium marneffei is endemic in Southeast Asia and the southern part of China.
Cases have been reported from both Eastern and Western countries. This review discusses the
history, epidemiology, mycology, clinical manifestations, diagnosis, and treatment of penicilliosis
marneffei, on the basis of 155 cases of the infection. About 80% of the patients are immunocompromised. P. marneffei can infect various organs, particularly the lung, liver, and skin. The most
common clinical features include fever, weight loss, and anemia. The organism has been isolated
most commonly from skin, blood, and bone marrow. Immunologic identification of fungal isolates
can be done with exoantigen tests and immunohistochemical methods. Treatment of disseminated
penicilliosis marneffei in HIV -infected patients with parenteral amphotericin Band itraconazole is
relatively effective and safe.
Penicilliosis marneffei is a disseminated and progressive infection caused by Penicillium marneffei, a facultative intracellular pathogen and the only thermally dimorphic fungus of the
genus Penicillium [1-3]. It is the third most common opportunistic infection in HIV-infected patients in certain parts of
Southeast Asia, following extrapulmonary tuberculosis and
cryptococcosis [3]. Areas in which the organism is highly endemic include Southeast Asia [4-6] and the southern part of
China [1, 7]. The infection has been widely suggested to be
included in the list of indicator diseases for differential diagnosis of AIDS in HIV-infected patients who are visitors to or
natives or residents of the areas of endemicity [2, 8-15].
Although most patients with penicilliosis marneffei are immunocompromised, some researchers have recommended that
P. marneffei be considered as a primary pathogen in all humans,
because in certain areas of endemicity most of the infections
have occurred in persons with normal immunity [1, 16]. Without early diagnosis and proper treatment, the disease is associated with a high mortality rate, regardless of whether HIV
infection is involved [1, 3, 5, 14, 16].
Many cases of penicilliosis marneffei have been misdiagnosed as tuberculosis, which is epidemic in regions where the
fungal disease is prevalent [2, 5, 17- 23]. Both infections have
similar symptomology [5, 8, 15, 18,23]. Unfortunately, antitu-
Received 13 September 1995; revised 15 March 1996,
Reprints or correspondence: Tuan Anh Duong, 205 South Henry Unit 2,
Madison, Wisconsin 53703,
Clinical Infectious Diseases 1996;23:125-30
© 1996 by The University of Chicago. All rights reserved.
1058-4838/96/2301-0017$02.00
berculosis agents are not effective against P. marneffei [5, 21,
22]. Because of similar clinical manifestations, penicilliosis
mameffei in HIV-infected patients can be easily misdiagnosed
as other fungal infections, such as histoplasmosis and cryptococcosis [1,2,8,15, 17,21,24].
The incidence of penicilliosis marneffei has risen markedly
during the past 5 years. From ~ 30 cases reported from 1973
to 1990, the number increased to a total of > 160 by 1995.
These figures, however, do not include cases reported in languages other than English. This review discusses the history,
epidemiology, mycology, clinical manifestations, diagnosis,
and treatment of penicilliosis marneffei, on the basis of 155
cases of the infection that have been described in the Englishlanguage literature. This review also introduces recent findings
from research on serology for better diagnosis and from epidemiologic studies of penicilliosis mameffei.
History
Capponi et al. [4] first isolated P. marneffei in 1956 from the
liver of a bamboo rat (Rhizomys sinensis) in Vietnam. Pathogenicity of the organism in mice, hamsters, and guinea pigs was
established. The organism was named after Dr. Mameffe, director of the Institut Pasteur in Indochina and Paris [25].
In 1959, Segretain [6] reported the first infection in humans.
After the researcher accidentally inoculated the fungi into his
finger, auxiliary lymphadenopathy developed and a nodule appeared at the inoculated site 9 days later. P. marneffei was isolated
from the nodule. Segretain successfully treated himself with oral
nystatin-a drug other researchers later found to be ineffective
in treating natural P. marneffei infection in humans [1].
126
Duong
Fourteen years after the report of laboratory-acquired infection, DiSalvo and colleagues [25] reported the first natural
infection of P. marneffei in a human. The patient was a 61year-old man living in North Carolina. A minister who had
worked in Vietnam and traveled in Southeast Asia, he had
undergone radiation therapy and splenectomy for Hodgkin's
disease. P. marneffei was unexpectedly isolated from his enlarged and infarcted spleen. The isolate's susceptibility to amphotericin B was tested, but the author did not mention whether
the patient was treated with amphotericin B and, if so, whether
the treatment was successful.
Deng and colleagues [1] claimed that they identified the first
patient with penicilliosis mameffei in Guangxi, China, in 1964.
However, they were unable to publish their findings until 1985
because of suppression of academic endeavors during the Cultural Revolution (1966-1976) [16].
When DiSalvo described the first case of penicilliosis
marneffei, it was thought to be an isolated incident, until in
1984 Jayanetra et al. [5] reported on five cases in Bangkok,
Thailand. Two of the patients had normal immunity. They
were successfully treated with amphotericin B. The others had
underlying conditions: tuberculosis, lymphopro1iferative disorder, or pregnancy complicated by systemic lupus erythematosus. They died as a result of misdiagnosis of the condition as
tuberculosis; isolates of P. marneffei from their tissues were
discounted as contaminants.
In 1988, Piehl and colleagues [26] in the United States reported the first case of penicilliosis marneffei associated with
HIV infection. Subsequently, additional cases of the opportunistic mycosis in persons with AIDS were reported. The most
significant report of disseminated P. marneffei infection in
AIDS patients was published in 1994 by Supparatpinyo and
colleagues [3] in Chiang Mai, Thailand, where P. marneffei is
endemic. Within 2 years, 86 patients with AIDS at one hospital
were found to have the mycosis.
Recognizing the prevalence of the mycosis in patients with
AIDS, the Thai Ministry of Public Health has allowed penicilliosis mameffei to be considered as an AIDS-indicating disease
in Thailand since 1992, according to Imwidthaya [27]. A number of mycologists researching the fungal disease expect that
the same measure will be taken by other countries in Southeast
Asia, since P. marneffei is endemic throughout this area [2, 3,
8, 10, 13, 14, 22, 28].
A recent report by Wong et al. [29] indicates that in Hong
Kong, another area where P. marneffei is endemic, the fungal
disease has become not only the sixth known cause of death
of patients with AIDS but also the second major fungal infection (after cryptococcosis) in these patients. In fact, the infection has been included as an AIDS-defining disease in the area.
Mycology
The mycologic features of P. marneffei have been very well
characterized [1, 3, 5, 11, 12, 15, 20, 21, 25, 30-33]. It is the
em
1996;23 (July)
only dimorphic fungus of the genus Penicillium. The fungus
grows as a mold at 25°C on Sabouraud glucose agar medium.
After 2 days, the mold colony is grayish white and downy or
woolly. A unique characteristic of the P. marneffei mold is the
presence of a soluble red pigment that diffuses into the agar.
The reverse side therefore appears either pink or red. As it
ages, the colony becomes more rugose while the aerial mycelia
become pinkish. The fungus has a fast growth rate. Within 2
days the mold colony grows up to 5 mm in diameter and may
further grow to 40 mm after 2 weeks. After 10 days the color
of the colony changes from white to light brown and finally
to light green.
Microscopically, P. marneffei as a mold has typical penicillial features. The hyphae are short, hyaline, septate, and
branched. The conidiophores are located laterally and terminally. The verticils have 3-5 penicilli, which bear phialides in
a verticillate fashion. The phialides give rise to curved chains
of ellipsoidal and smooth-walled phialoconidia of 2-4 X 23 mm in size. The phialoconidia have prominent disjunctors.
Spirals are occasionally present.
After 2 days' incubation at 37°C, P. marneffei grows as a
yeast on Sabouraud glucose agar, cotton-seed agar, blood agar,
or brain-heart infusion agar medium. The colony surface has
been described as cerebriform, convoluted, and smooth. No
soluble, diffusing red pigment is produced. The colony is light
tan, resembling the color of Blastomyces dermatitidis [25].
Microscopically, P. marneffei yeast cells are unicellular and
3-6 X 1.5-2 mm in size. The cells are mixed with hyphaelike elements. Investigators have described them as round [25],
ellipsoidal [1], or rectangular [5]. A unique characteristic of
the yeastlike cells is that they divide by fission, not budding,
and have an easily seen white central septum.
Epidemiology
More than 155 cases of penicilliosis marneffei have been
described in the English-language literature. The organism's
ecological characteristics and geographic distribution are still
unknown. The organism has been isolated from bamboo rats
in various parts of Southeast Asia, particularly in Vietnam [6]
and Thailand [27]. The organism is also endemic in Guangxi
Province of China [1, 7] and in some areas of Hong Kong [14].
More than 90% of bamboo rats in Guangxi are infected with
the fungus and carry it in their internal organs [7]. Information
from the 155 reported cases indicates that infected patients
have either visited or lived in Vietnam [6, 25], Laos [2, 33],
Singapore [19, 22], Malaysia [2, 11], Burma [2, 8], Thailand
[2, 3, 5, 9, 15, 20, 26, 34, 35], Indonesia [2], Guangxi [1, 16],
or Hong Kong [13, 14, 19, 23].
Animal hosts for P. marneffei include humans and bamboo
rats (R. sinensis and Rhizomys pruinous senex) [4, 6, 7]. The
organism has been isolated from the feces, liver, lungs, and
spleen of bamboo rats [1, 7], as well as from soil from the
rats' burrows [1]. It is believed that both humans and bamboo
em 1996;23 (July)
127
Penicillium marneffei: An Emerging Pathogen
rats are infected with P. marneffei from a common source, as
opposed to humans being infected from the rats [1, 7].
No definitive route of transmission has been determined. It
has been suggested that the organism is acquired via ingestion
and inhalation [5, 27, 36]. Inoculation via skin can cause the
infection as well [6]. In an interesting case, a 61-year-old immunocompetent patient from an area of nonendemicity in Hong
Kong had P. marneffei infection without having ever been to
an area where such infection is endemic [18]. However, the
patient had daily working contact with Vietnamese refugees.
Chan and Woo [18] speculate that P. marneffei was carried by
these refugees or in their belongings and transmitted to the
patient.
Approximately 90% of patients with penicilliosis marneffei
have been male. Their ages have ranged from 3 months to 72
years. As a whole, > 80% of the patients are immunocompromised. In their reports, Supparatpinyo et al. [3] and Sirisanthana
[37] demonstrated a correlation between the increase in incidence of AIDS in northern Thailand and that of penicilliosis
mameffei. Within two years, 86 cases of P. marneffei infection
associated with AIDS were diagnosed at Chiang Mai University
Hospital [3]. Among the first 400 patients with AIDS at the
hospital, 140 cases of penicilliosis marneffei were identified
[37]. (Not all of these case reports are published in English.)
Many of these patients had no other opportunistic infection at
the time of admission [3]. It is important to note that, as presented in figure 1, a small number of the patients were not
HIV-positive.
In contrast to the Thai cases of P. marneffei infection, almost
all of the cases (14 of 15) reported from Guangxi involved
patients with normal immunity [1, 16, 31]. However, the reports
did not mention whether malnutrition, which may be considered to be an immunocompromising factor, was involved. It is
surprising that the mortality rate was very high (13 patients
died). According to the authors, this was partially due to the
lack of treatment and to incorrect diagnosis.
A number of cases of P. marneffei infection have involved
individuals from Western countries such as Italy [15], Britain
[32], Canada [33, 38], France [2], Netherlands [9, 39], Switzerland [17], and the United States [21, 25, 26]. All of these
patients had traveled to various parts of Southeast Asia and
southern China. It has been suggested that the HIV-infected
patients in the United States who are at risk of penicilliosis
marneffei include Southeast Asian immigrants, immigrants
from southern China, Vietnam War veterans, and those who
have traveled to Southeast Asia, Guangxi, and certain parts of
Hong Kong [21].
Pathology
Histopathologically, penicilliosis marneffei can lead to three
distinct tissue reactions [1]. The granulomatous reaction involves infection of the reticuloepithelial system, often seen in
immunocompetent patients. The yeast cells invade macrophages and survive and multiply intracellularly. The cell-mediated response to the fungi leads to formation of granulomas.
Multinucleated giant cells, lymphocytes, and neutrophils
participate in the reaction. As a result, centers of the granuloma
become necrotic and the yeast cells are released. The reaction
can occur in any organs of the mononuclear phagocytic system
[1, 14].
Commonly, a suppurative reaction occurs in immunocompetent patients with P. marneffei infection [1]. An inflammatory
response invoking neutrophils and fibrin results in abscesses
in various organs, especially the lung, skin, liver, and subcutaneous tissues.
An anergic and necrotizing reaction is often seen in patients
with compromised immune function [1]. Organs involved include the lung, liver, and skin. Many of the reports indicate
observation of diffuse infiltration of macrophages engorged
with proliferating yeast cells in tissues [1, 2, 5, 12, 34]. This
12
10
Figure 1. Number of patients
with P. marneffei infection seen at
Chiang Mai University Hospital
and time of diagnosis. The number
of HIV-infected patients (open
bars) and HIV-noninfected patients (solidbars) is indicated. (Reproduced with permission from
[3].)
8
6
4
2
O-L,-........................I.r-r'T'"r'rT"'I-r'IITrT"T"1r-T'"T"T"'T"T'I"-I""T
Jan 1988
Jan 1989
Jan 1987
Jan 1990
Month of diagnosis
Jan 1991
Jan 1992
Duong
128
Table 1. Sitesof culture-positive infection in the 155 reported cases
of penicilliosis mameffei.
Site of infection
Skin
Blood
Bone marrow
Lymph nodes
Liver
Lung
Bone
Spleen
Nasopharynx
Bowel
Kidney
Pericardium
Finger*
Meninges
No. (%) of patients
96 (61.9)
85 (54.8)
44 (28.4)
35 (22.6)
26 (16.8)
21 (13.5)
12 (7.7)
8 (5.2)
5 (3.2)
3 (1.9)
3 (1.9)
3 (1.9)
1 (0.6)
1 (0.6)
* Laboratory-acquired infection.
stage signals initiation of a progressive and disseminated infection with P. marnefJei [1].
Immunocompromised patients have a greater chance of having disseminated penicilliosis marneffei [14] involving a number of organs as listed in table 1.
em
1996;23 (July)
mocystis carinii infection [11], and cryptococcosis [27]. Its
nonspecific symptoms and signs and great similarities to the
manifestations of other HIV-related opportunistic infections
may make diagnosis of P. marnefJei infection more difficult
[3, 9]. Common clinical findings in the 155 reported cases of
penicilliosis mameffei are presented in table 2.
Immunity
Because P. marnefJei is a facultative intracellular pathogen,
cell-mediated immunity is important in helping to eradicate the
organism from a host [1, 2, 14,20, 34]. This is consistent with
the observation that dissemination of the infection is much
more common in patients with AIDS. Formation of granulomas
helps localize and prevent the dissemination of the infection.
Although a humoral reaction may be induced by presence
of the fungi, antibody-mediated immunity appears to be of little
importance against the fungal infection. Yuen and colleagues
[40] reported an increase in titer of IgG (specific for
P. marnefJei antigens originating from the germinating conidia
and yeast hyphae) in patients with penicilliosis mameffei, as
compared with the titer in healthy individuals. The information
may be useful serologically for rapid detection of the fungal
infection.
Diagnosis
Clinical Manifestations
The most common clinical features observed in patients with
penicilliosis mameffei include fever, weight loss, and anemia.
Dissemination of the disease is characterized by skin lesions,
most often on the face, upper trunk, pinnae, and arms [12,
27]. Many patients have painful, nonproductive cough [1,27].
Generalized lymphadenopathy is commonly observed. Hepatosplenomegaly is noted in many patients, especially children
with AIDS [28]. In some patients pulmonary infiltrates occur
and can be evidenced on roentgenographs showing densities,
abscesses, and cavitations [3]. Hilar node calcification is not
commonly reported [5].
Many cases of penicilliosis mameffei also involve fungemia,
diarrhea (especially in children with AIDS [28]), necrotic papules, and nodules or pustules of the skin and subcutaneous
tissues [3, 12,34]. In addition, bone marrow infection, leukocytosis [1, 21, 32], and genital ulcer [12] have been reported.
Pericarditis [1, 5,22] and pleurisy [31] have been observed in
a few cases. Osteolytic lesions or osteomyelitis [18], arthritis
[34], and retropharyngeal purulent abscess causing upper-airway obstruction [19] are rare.
The clinical manifestations observed in cases of penicilliosis
marneffei may closely resemble those of other systemic fungal
infections, such as histoplasmosis and cryptococcosis in HIVinfected patients [2, 9, 14, 17]. Moreover, cases of AIDS have
been reported in which penicilliosis occurred with other opportunistic infections, such as salmonellal septicemia [12], Pneu-
The first important step in diagnosis of penicilliosis
mameffei involves determination of whether the patient has
been to an area of endemicity [8, 9, 13, 22]. Chest roentgenography may be able to show cavities present in the lung [3].
A presumptive diagnosis can be established with use of any of
a number of different staining/direct examination techniques,
such as with Wright's [3], Giemsa [2], hematoxylin and eosin
[17], Grocott-Gomori methenamine - silver nitrate [1], and periodic acid-Schiff stains [1]. Samples for direct examination can
Table 2. Common clinical characteristics reported in the 155 reported cases of penicilliosis mameffei.
Clinical characteristic
Fever
Anemia
Weight loss
Skin lesions
Fungemia
Lymphadenopathy
Cough
Hepatomegaly
Diarrhea
Splenomegaly
Pericarditis
Osteolytic lesions
Arthritis
No. (%) of patients
152
116
III
108
84
81
(98.0)
(74.8)
(71.6)
(69.7)
(54.2)
(52.3)
77 (49.7)
68 (43.9)
36 (23.2)
21 (13.5)
7 (4.5)
6 (3.9)
6 (3.9)
em
1996;23 (July)
Penicillium marneffei: An Emerging Pathogen
be obtained from bone marrow aspirate [2, 3], lymph nodes
[3], and skin scrapings [17, 34].
Intracellular and extracellular basophilic, elliptical yeastlike
organisms can be seen in these specimens. P. marneffei yeasts
have clear central septation. The organism can be cultured from
specimens of blood, bone marrow, skin and palatal papule
scrapings, liver tissue, draining abscesses, lymph nodes, sputum, and ulcers. Cultures of stool [2, 10, 13, 14, 22], urine [2,
9, 32], bronchial washings [17, 33], fluid from knee joints [5],
and CSF [34] have been reported to yield P. marneffei colonies.
Differentiation between P. marneffei and Histoplasma capsulatum is important because of the great morphological resemblance between the two organisms [1, 2, 8, 15, 17, 21, 24].
Both are intracellular pathogens. However, H. capsulatum yeast
divides by budding, not fission. Immunologic identification of
P. marneffei by means of an immunohistochemical approach
[41] and exoantigen tests [2] has been reported. More important, differentiation between tuberculosis and P. marneffei
infection must be accurate for proper antifungal therapy [5].
Recently, Yuen and colleagues [40] experimented with serodiagnosis of penicilliosis mameffei. They used an indirect immunofluorescent antibody test to evaluate the increase in IgG
titer, and they found that patients with P. marneffei infection
have a much higher titer of antibody against antigens in yeast
hyphae and germinating conidia than do control groups (healthy
persons and patients with diseases of which the symptoms are
similar to those of penicilliosis mameffei). The clinical utility
of serodiagnosis on the basis of IgG titers remains to be proven.
LoBuglio and Taylor [24] developed oligonucleotide primers
from nucleotide sequences unique to the fungus. They used the
primers to selectively amplify DNA from six isolates of
P. marneffei and exclude the other species tested, including
Penicillium subgenus Biverticillium, Talaromyces species, Aspergillus fumigatus, Coccidioides immitis, H. capsulatum, and
P. carinii. The researchers believe that these primers can be
used to create a PCR identification system, potentially leading
to faster diagnosis of P. marnefJei.
Treatment
It is relatively effective and safe to treat disseminated penicilliosis mameffei in HIV-infected patients with parenteral amphotericin B (for 2 weeks) followed by itraconazole (for 6
weeks) [2, 27, 42]. Supparatpinyo and colleagues found that
this combination did not lead to serious adverse effects in any
of their patients with HIV infection who had culture-proven
penicilliosis mameffei [42]. Clinical improvements were seen
in all of them after 2 weeks. In immunocompetent patients,
amphotericin B yields a very good outcome if the condition is
diagnosed early.
Relapse can occur. In one of Supparatpinyo's reports [3],
the treatment-response rate was 59%. The conditions of 77%
of patients responded well to amphotericin B; most responses
to itraconazole and some to fluconazole were good.
129
Conclusions
In summary, P. marneffei has emerged as an opportunistic
pathogen in immunocompromised patients. Immunocompetent
persons living in areas of endemicity are also at risk of the
fungal disease. Successful treatment of the disease requires
early diagnosis and administration of the proper antifungal
drugs. Diagnosis is difficult because of similarities between
penicilliosis mameffei and tuberculosis and other AIDS-related
opportunistic infections, such as histoplasmosis and cryptococcosis.
Currently, the environmental niche of P. marneffei is unknown. Serological tests, as well as epidemiologic investigations, may be useful for diagnosis. Given the increase in incidence of the mycosis in patients with AIDS in Southeast Asia,
penicilliosis mameffei is a potential AIDS-indicating disease
in this area.
Acknowledgments
The author thanks Dr. Edward Balish, Professor of Medical
Microbiology and Immunology (University of Wisconsin, Madison), for his cooperation, preparation advice, and review of the
manuscript and thanks Kevin McIntyre, M.S.S.W., Jon Woods,
M.D., Ph.D., and Thira Sirisanthana, M.D., for also reviewing the
manuscript.
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