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Memórias do Instituto Oswaldo Cruz
Fundação Oswaldo Cruz, Fiocruz
ISSN: 1678-8060 EISSN: 1678-8060
Vol. 95, Num. s1, 2000, pp. 133-139
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Untitled Document
Mem. Inst. Oswaldo
Cruz vol.95 s.1 Rio de Janeiro 2000 pp. 133-139
Microsporidia
and Acquired Immunodeficiency Syndrome
J Schottelius, SC Gonçalves
da Costa*/+
Section of Parasitology, Bernhard-Nocht-Institute
for Tropical Medicine, D-20359 Hamburg, Germany *Laboratório de Imunomodulação,
Departamento de Protozoologia, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900
Rio de Janeiro, RJ, Brasil
+Corresponding
author. Fax: +55-21-598.4323. E-mail: sycosta@gene.dbbm.fiocruz.br
Received 7 August 2000
Accepted 4 September 2000
Code Number: OC00170
Microsporidia is a common
term that has been used to refer to a group of eukaryotic, obligate intracellular
protozoan parasites belonging to the phylum Microspora. They are important agricultural
parasites, contaminating commercial insects; they are also important by infecting
laboratory rodents, rabbits and primates. Ever since the early cases found by
Magarino Torres, who reported the presence of Encephalitozoon in a patient suffering
of a meningoencephalomyelitis, some human pathology caused by microsporidia
has been described. However, only after the acquired immunodeficiency syndrome
outbreak have these organisms appeared as significant etiological agents in
different pathologies. Even so, they remain underestimated. In the present article,
the importance of microsporidia for the human pathology in immunocompromised
host has been stressed.
Key words: microsporidia -
immunocompromised host - pathology - acquired immunodeficiency syndrome-Aids
Parasites belonging to the
phylum microspo-ridia Balbiani 1882 (Sprague & Becnel 1998) are spore-forming,
small, obligate intracellular living eukaryotes with a unique morphology (Vavra
& Larsson 1999). These parasites are distributed by spores which contain
a characteristic polar tube apparatus which is necessary for the transfer of
the "the parasite" sporoplasm, from the spore to a host cell. The
mature spores are Gram positive. The spore wall is composed of a protein-rich
exospore, an electron-dense surface coat, and a structure-less layer below this
coat, the electron-transparent endospore which contains chitin. The internal
surface of the endospore is covered by a plasma membrane which limits the cytoplasma
of the spore. The life cycle of these parasites comprise three distinct phases:
the infective phase, the proliferative, vegetative phase or schizogonie and
the spore-forming phase or sporogony. Microsporidia are world-wide distributed
in invertebrates and vertebrates including man. More than 140 genera including
more than 1,000 species are known (Wittner & Weiss 1999).
The first mammalian infection
was reported by Wright and Craighead (1922) in rabbits. The first human case
was described by Magarinos Torres in 1927. Some years later Matsubayashi et
al. (1959) described another case of a 9-year old Japanese boy with headache,
recurrent fever, seizures, among other symptoms. Margileth et al. (1973) described
an human case proven by autopsy of a 4-month old immunocompromised infant with
thymic aplasia and disseminated nosematosis. Ashton and Wirashina (1973) mentioned
a case of ocular microsporidiosis in a 11- year old boy from Sri Lanka. Pinnolis
et al. (1981) described the case of an African woman with a perforated corneal
ulcer. The parasite was identified as Nosema.
Up to the beginning of the
acquired immunodeficiency syndrome (Aids) pandemie in 1981, only single cases
of microsporidia infections in men and animals were reported because these microorganisms
were not routinely diagnosed. Since this time, the microsporidia are increasingly
recognized as cause of severe infections with a wide range of clinicopathologic
findings especially in immuno-compromised patients. At present, seven genera:
Enterocytozoon, Encephalitozoon, Nosema, Pleistophora,
Trachipleistophora, Vittaforma, Brachiola, with 12 species
are known as pathogens in humans plus the collective group of Microsporidium
with uncertain taxonomic status. The spores of these genera can morphologically
be distinguished in regard of the combination of the number of their nuclei
(one or two), the number and arrangement of the coils of the polar filament
inside the spores and whether the spore is envolved by a parasitophoric vacuole
or not in the cytoplasm of the host cell.
From the mentioned microsporidia,
only the species E. bieneusi, E. hellem, E. intestinalis,
E. cuniculi, Pleistophora sp., T. hominis, T. anthropopthera,
N. connori, B. vessicularum, V. vesicularum were diagnosed
in patients with human immunodeficiency virus (HIV) together with a Thelohania/Pleistophora-like
parasite. From patients without HIV were described E. cuniculi, E. intestinalis,
E. bieneusi, N. ocularum, V. coneae, M. ceylonensis and M. africanum.
In both groups of patients special attention should be paid to ocular microsporidial
infections. In patients without HIV such infections were found with Nosema,
Vittaforma and Microsporidium; in patients with HIV E. cuniculi-like,
E. hellem and E. intestinalis plus some cases without analysis of the genera
and species (Kotler & Orenstein 1999).
GENERA AND SPECIES
ENCEPHALITOZOON
The genus Encephalitozoon
contains the species E. cuniculi, E. hellem and E. intestinalis.
These pathogens are morphologically indistinguishable. The development of the
spores takes place in the cytoplasm of the host cell inside of a parasito-phorous
vacuole. In the longitudinally sectioned spores, the polar filament can be seen
in form of five to six coils arranged regularly in a single row. The mature
spores have only one nucleus. This pathogen has a reservoir in different mammals
(Canning 1998). This agent was also found in HIV patients (Deplazes et al. 1996,
Didier et al. 1996a, Weber et al. 1997). Human infections with this microorganism
can not be discussed without a side-glance on animal pathogenic strains. Up
to now three groups have been identified: group I was originally isolated from
rabbits and also described from HIV patients (Deplazes 1996). The group II was
isolated from a mouse and is able to infect blue foxes but was not found in
humans, until now (Didier 1995). Group III was isolated from domestic dogs and
identified in Aids patients (Didier et al. 1996b). These examples demonstrate
that in some cases human infections can trace back to animal reservoirs. The
importance of these strain variations and whether E. cuniculi strains
exist pathogen only for animals should furtherhin be observed.
Spores of E. cuniculi
- Have been found in a patient with cytomegalovirus adrenalitis. The spores
were seen in epithelium and endothelial cells of the adrenal glands. De Groote
et al. (1995) described three pathogens in the soft tissue of a tongue ulcer
in a patient with Aids with a disseminated E. cuniculi infection. These
protozoa were also described by Belcher et al. (1997) as infection of the mandible
of an Aids patient. Weber et al. (1997) reported that E. cuniculi infection
in Aids patients was associated with keratoconjunctivitis, hepatitis, peritonitis,
encephalititis, urinary tract infections and respiratory tract infections. A
case of E. cuniculi infection of duodenal mucosa was described by Franzen
et al. (1995). This patient has had no gastrointestinal symptoms. Franzen et
al. (1996) analyzed this species as pathogen for a chronic rhinosinusitis in
patients with Aids. Zender et al. (1989) mentioned a case of peritonitis in
an immunocompromised patient. Experimentally infections with E. cuniculi
and E. hellem could be transferred to healthy and immunocompromised rhesus
monkeys Macaca mulatta (Didier et al. 1994).
E. hellem - This microsporidia
was found in immunocompromised patients. The first isolation and characterization
was made from Aids patients with keratoconjunctivitis. This pathogen was also
diagnosed in cases of chronic rhinosinusitis (Eeftinck-Schattenkerk et al. 1992),
disseminated microsporidiosis (Schwartz et al. 1992), keratoconjunctivitis (Schwartz
et al. 1993a), bronchiolitis (Schwartz et al. 1993b), isolated out
of a prostatic abcess (Schwartz et al. 1994), pulmonary and intestinal microsporidiosis
(Weber et al. 1992), in an Aids patient with pulmonary colonization, microhematuria,
and mild conjunctivitis (Weber et al. 1993). This pathogen could be identified
in cases of superficial keratitis in Aids patients (Didier et al. 1991). Cases
of ocular microsporidiosis are described by Diesenhouse et al. (1993), Rosberger
et al. (1993), Schwartz et al. (1993a), Didier et al. (1996a) and Silverstein
et al. (1997). Until today, E. hellem was found in immunocompetent humans
(Weber et al. 1999) and could be transferred to M. mulatta (Didier et
al. 1994). Furthermore, this infection was detected in wild parrot (Suter et
al. 2000).
E. intestinalis (formerly
Septata intestinalis) - this pathogen was first described by Cali et
al. (1991b) found in patients with chronic diarrhea, by Orenstein et al. (1992)
in a case of disseminated microsporidiosis and from humans infecting enterocytes,
macrophages and associated with diarrhea in an Aids patient. This result was
underlined by the analysis of Baker et al. (1995) who suggest that S. intestinalis
should be designated as E. intestinalis on the basis of the phylogenetic
analysis of the small subunit ribosomal DNA. This parasite was found associated
with chronic diarrhea and dissemination in Aids patients (Cali et al. 1993),
small intestinal microsporidiosis (Field et al. 1993). Orenstein et al. (1993)
reported about four cases of S. intestinalis infection in Aids patients
with intestinal and disseminated microsporidiosis. This microsporidia species
was not only found in immunocompromised persons but also in immunocompetent
humans. Enriquez et al. (1997) described such infections in children and adults
with diarrhea and in travelers with chronic diarrhea (Raynaud et al. 1998).
This pathogen was found in dogs, pigs, cows, goats and donkeys (Bornay-Llinares
et al. 1998) and SCID mice could be infected (Achbaron et al. 1996, Enriquez
et al. 1997). Therefore, it can not be excluded that by an oral-fecal infection
these pathogens can be transferred from animals to humans. Patients with E.
intestinalis infection have the tendency to develop disseminated infection
(Molina et al. 1995). A consequence of E. intestinalis infection can
be the break-down of the renal function. The infection of the kidneys can result
in urethritis (Corcoran et al. 1996, Soule et al. 1997). E. intestinalis
can infect the biliary tract (Schwartz & Bryan 1997). Ocular infections
with E. intestinalis were reported by Lowder et al. (1990).
E. bieneusi - this
pathogen was first described by Desportes Livage et al. (1985). It is found
in enterocytes of the small intestine of HIV patients with chronic diarrhea
(Orenstein et al. 1997). Furtherhin this agent was identified, in pulmonary
and intestinal microsporidiosis (Weber et al. 1992), and in the biliary tree,
gall bladder the biliary tract and nonparachymal liver cells (Beangerie et al.
1992, Pol et al. 1992). The spores and their electron microscopical morphology
can be distinguished from the spores and their morphology of the species of
the genus Encephalitozoon. The spores of E. bieneusi are formed
in direct contact with the cytoplasma of the host cell and not enveloped by
a parasitophoric vacuole. The mature spores have one nucleus and the polar filament
has five to six coils forming two rows (Vavra & Larsson 1999). E. bieneusi
was found as cause of self-limited diarrhea in immunonocompetent persons (Weber
et al. 1994, Bryan et al. 1997). Bertange et al. (1993) described that this
microsporidia was found in 1% of African children with diarrhea. Furtherhin
it was found that this opportunistic protozoa was diagnosed in patients with
bone-marrow, liver, and heart-lung transplantation (Weber et al. 1994, Rabodonirina
et al. 1996).
E. bieneusi was first
described as animal infection in a pig by Deplazes et al. (1996). This microsporidia
species could also be detected in macaques which had been experimentally infected
with simian immunodeficiency virus (SIV) (Mansfield et al. 1998), in contrast
to human infections where these pathogens were found in the small intestine,
in the macaques the parasites were found in the gallbladder. Carville et al.
(1997) have found this agent in immunocompetent macaques which were not infected
by SIV.
Tzipori et al. (1997) were
successful to transfer an infection of E. bieneusi from an Aids patient
to SIV infected macaques.
PLEISTOPHORA TRACHIPLEISTOPHORA
Pleistophora
spp. was found in three immuno-deficient patients: first in an immunodeficient
but HIV negative man, then in Aids patients (Ledford et al. 1985, Macher et
al. 1988, Grau et al. 1996) suffering in myositis. These microsporidia are serious
muscle parasites of fishes (Canning & Lom 1986, Lom & Dykova 1992).
These are the only publications of these microsporidia species in mammals.
In another case of myositis
of an Aids patient, biopsy material from the skeletmuscle was transferred to
tissue culture and athymic mice (Hollister et al. 1996). This patient has had
an additional infection in the corneal epithelium. The development and ultrastructure
of these parasites differ from the genus Pleistophora and give rise to
nomination of the genus and species T. hominis. Field et al. (1996) reported
about a second case of human Aids with myositis and infection with T. hominis.
Vavra et al. (1998) described the second species T. anthropopthera found
in the brain of one and in the kidneys, brain, heart, liver, spleen, lymph nodes
bone marrow, pancreas, thyroid and parathyroid of a second Aids patient. Both
species differ in their development.
The mature spores of Pleistophora
and Trachipleistophora have 9 to 12 coils, only one nucleus and develop
inside of a parasitophoric vacuole. Pleistophora spp. form in merogonic
and sporogonic proliferation multinucleate plasmidia while Trachipleistophora
spp. has division of meronts and sporonts by a binary fission.
VITTAFORMA
Davis et al. (1990) have given
a case report about a corneal microsporidiosis. This pathogen was named N.
corneum by Shadduck et al. (1990). The investigation of the ultrastructure
of the developmental forms in athymic mice (Silveira & Canning 1995) gave
rise to the denomination of this agent as V. corneae. Later, this microsporidia
was found in the urinary tract of an Aids patient (Deplazes et al. 1997). The
mature spores are diplokaryotic with a polar filament of six coils. The development
of the parasite takes place in direct contact with host cell cytoplasma. The
mature spore is enclosed in several membranous layers (Vavra & Larsson 1999).
An animal host of this parasite is not known.
BRACHIOLA
The species B. vesicularum
was found in a patient with Aids associated with myositis (Cali et al. 1998).
In the mature spores of the diplokaryotic B. vesicularum, the polar tube
forms two rows of coils, each row with 8 to 10 coils, but they can also be arranged
in single and triple rows of coils. This pathogen seems only to be infective
for muscle cells. The development of the spores takes place in direct contact
with the cytoplasm of the host cell. The formerly described B. connori
(Sprague 1974) is a synonym for N. connoris (Sprague 1974, Cali et al.
1998).
MICROSPORIDIUM
The collective group of microsporidium
includes microsporidia species of which the genetic position is unclear, the
developmental cycle unknown. Two human pathogenic microsporidia are placed in
this group: M. ceylonensis and M. africanum. Ashton and Wirasinha
(1973) described the case of an 11-year old Tamil boy with a corneal ulcera.
Sprague (1977) described this parasite as Nosema sp. Canning and Lom
(1986) transferred this pathogen to the collective group of microsporidium and
denominated this agent as M. ceylonensis. Pinnolis et al. (1981) presented
a second case of a 36 year old woman from Botswana with a perforated corneal
ulcer. This parasite was identified as Nosema sp. Canning and Lom (1986)
transferred this agent to the collective group of microsporidum and named it
M. africanum.
NOSEMA
Microsporidia of the genus
Nosema normally parasites in invertebrates. One case of a disseminated
infection with this pathogen was found in a athymic infant (Margileth et al.
1973, Canning & Lom 1986). This microorganism was described as N. connori.
In a second case, ocular microsporidiosis was diagnosed in a patient without
immunodeficiency with keratitis. The parasite was named N. ocularum (Cali
et al. 1991a). The development of these protozoa occur in direct contact with
the host cell cytoplasma. The mature spore has paired nuclei and contain a polar
filament with 11 coils.
The clinical manifestations
of human microsporidial infections include systemic, intestinal, muscular and
ocular diseases in immunocompromised and immunocompetent humans. Not all mentioned
microsporidia species have been found in both groups of patients. The question
can not be answered whether microsporidia species exist which are able to infect
only one of both patient groups. We do not know how many of these opportunistic
protozoa are pathogens for humans. But the clinical manifestations are so manifold
and so grave, especially for immunocompromised patients, that these microorganisms
should be included in the routine diagnosis of such patients.
REFERENCES
- Achbaron A, Mazier D, Desportes-Livage
I, Renia L, Charlotte F, Gneragbe T, Onbrouck C 1996. Experiment model for
human intestinal microsporidiosis in interferon gamma receptor knockout mice
infected by Encephalitozoon intestinalis. Parasite Immunol 18:
387-392.
- Ashton N, Wirashina PA
1973. Encephalitozoonosis (nosematosis) of the cornea. Br J Ophthalmol
57: 669-674.
- Baker MD, Vossbrinck CR,
Didier ES, Maddox JV, Shadduck JA 1995. Small subunit ribosomal DNA phylogenic
of various microsporidia with emphasis on AIDS related forms. J Eukaryot
Microbiol 42: 564-570.
- Beangerie L, Teilhac MF,
Deluol AM, Fritsch J, Girard PM, Rozembaum W, Lequintrec Y, Chatelet FP 1992.
Cholangiopathy associated with Microsporidia infection of the common
bile duct mucosa in a patient with HIV infection. Ann Intern Med 117:
401-402.
- Belcher JW, Guttenberg
SA, Schmooker BM 1997. Microsporidiosis of the mandible in a patient with
acquired immunodeficiency syndrome. J Oral Maxillofac Surg 55:
424-426.
[ Medline ]
- Bertange S, Foulet F, Alkassoum
W, Fleury-Feith J, Develoux M 1993. Prevalence des spores d´Enterocytozoon
bieneusi dans les selles de patient sideens et d'enfants Africains non
infectes par le VIH. Bull Soc Pathol Exot 86: 531.
- Bornay-Llinares FJ, Da
Silva AJ, Moura H, Schwartz DA, Visvesvara GS, Pieniazek NJ, Cruz-Lopez A,
Hernandez-Jauregui P, Guerrero J, Enriquez FJ 1998. Immunologic, microscopic,
and molecular evidence of Encephalitozoon intestinalis (Septata
intestinalis) infection in mammals other than humans. J Infect Dis
178: 820-826.
[ Medline ]
- Bryan RT, Schwartz DA,
Weber R 1997. Mi-crosporidiosis in patients who are not infected with human
immunodeficiency virus. Clin Infect Dis 24: 534-535.
- Cali A, Kotler DP, Orenstein
JM 1993. Septata intestinalis n.g., n.sp., an intestinal microsporidian
associated with chronic diarrhea and dissemination in AIDS patients. J
Protozool 40: 101-112.
- Cali A, Meisler DM, Lowder
CY, Lembal R, Ayers L, Takvorian PM, Rutherford I, Long-worth DL, McMahon
J, Bryan RT 1991a. Corneal microsporidiosis. Characterization and identification.
J Protozool 38: 215S-217S.
- Cali A, Orenstein JM, Kotler
DP, Owen RL 1991b. A comparison of two microsporidian parasites in enterocytes
of AIDS patients with chronic diarrhea. J Protozool 38: 96S-98S.
[ Medline ]
- Cali A, Takvorian PM, Lewin
S, Rendel M, Sian CS, Wittner M, Tanowitz HB, Keohane E, Weiss LM 1998. Brachiola
vesicularum, n.g., n.sp., a new mi-crosporidium associated with AIDS and
myositis. J Eukaryot Microbiol 45: 240-251.
- Canning EU 1998. Microsporidiosis.
In SR Palmer, Lord Soulsby, DIH Simpson (eds), Zoonoses, Biology, Clinical
Practice, and Public Health Control, Oxford Univ. Press, Oxford, p. 603-623.
- Canning EU, Lom J 1986.
The Microsporidia of Vertebrates, Hartcourt Brace Jovanowich, Publ.,
London, New York, 289 pp.
- Carville A, Meansfield
K, Link KC, McKay J, Chalifoux L, Lackner A 1997. Genetic and ultrastructural
characterization of Encephalitozoon bieneusi in simian immunodeficiency
virus infected and immunocompetent rhesus macaques. Vet Pathol 34:
515.
- Corcorsan GD, Chiodini
PL, Daniels C, Isaacson JM 1996. Urethritis associated with disseminated microsporidiosis:
clinical response to albendazole. Clin Inf Dis 22: 592-593.
- Davis RM, Font RL, Keisler
MS, Shadduck JA 1990. Corneal microsporidiosis. A case report including ultrastructural
observations. Ophthalmology 97: 953-957.
[ Medline ]
- De Groote MA, Visvesvara
GS, Wilson ML, Pieniazek NJ, Slemenda SB, Da Silva AJ, Letch GJ, Bryan RT,
Reves R 1995. Polymerase chain reaction and culture confirmation of disseminated
Encephalitozoon cuniculi infection in a patient with Aids. Successful
therapy with albendazole. J Infect Dis 171: 1375-1378.
[ Medline ]
- Deplazes P, Mathis A, Muller
C, Weber R 1996. Molecular epidemiology of Encephalitozoon cuniculi
and first detection of Enterocytozoon bieneusi in faecal samples of
pigs. J Eukaryot Microbiol 43: 93S.
- Deplazes P, Saanen van
M, Iten A, Mathis A, Keller R, Tanner I, Weber R, Canning EU 1997. Double
infection with Vittaforma corneae and Encephalitozoon hellem
in an AIDS patient. In Program and Abstract, 10th Intern Congress of Protozoology,
Sydney, Australia, p. 75.
- Desportes-Livage I, Charpentier
Le A, Galian A, Bernard F, Cochand-Priollet B, Lavergne A, Ravisse P, Modiglian
R 1985. Occurrence of a new microsporidian Enterocytozoon bieneusi
n.g., n.sp., in the enterocytes of a human patient with AIDS. J Protozool
32: 250-254.
- Didier ES 1995. Reactive
mitogen intermediates implicated in the inhibition of Encephalitozoon cuniculi
(phylum Microspora) replication in murine peritoneal macrophages. Parasite
Immunol 17: 406-412.
- Didier E, Didier P, Friedberg
D, Stenson S, Orenstein J, Yee R, Tio F, Davis R, Vossbrinck C, Millichamp
N, Shadduck J 1991. Isolation and characterization of a new human microsporidian,
Encephalitozoon hellem (n. sp.), from three AIDS patients with kerato-conjunctivitis.
J Infect Dis 163: 617-621.
[ Medline ]
- Didier ES, Rogers LB, Brush
AD, Wong S, Traina-Dosge V, Bertuccci D 1996a. Diagnosis of disseminated microsporidian
Encephalitozoon hellem infection by PCR-Southern analysis and successful
treatment with albendazol and fumagillin. J Clin Microbiol 34:
947-952.
[ Medline ]
- Didier ES, Varner PU, Didier
PJ, Aldras AM, Millichamp NJ, Murphey-Corb M, Bohm R, Shadduck JA 1994. Experimental
microsporidiosis in immunocompetent and immunodeficent mice and monkey. Folia
Parasitol 41: 1-11.
- Didier ES, Visvesvara GS,
Baker MD, Rogers LB, Bertucci DC, De Groote MA, Vossbrinck CR 1996b. A microsporidian
isolated from an Aids patient corresponds to Encephalitozoon cuniculi
III, originally isolated from domestic dogs. J Clin Microbiol 43:
2835-2837.
[ Medline ]
- Diesenhouse M, Wilson L,
Corrent G, Visvesvara G, Grossniklaus H, Bryan R 1993. Treatment of microsporidial
keratoconjunctivitis with topical fumagillin. Am J Ophthalmol
115: 293-298.
[ Medline ]
- Eeftinck-Schattenkerck
JKM, Gool van T, Schot LS, van den Bergh Weerman M, Dankert J 1992. Chronic
rhinosinusitis, a new clinical syndrome in HIV infected patients with microsporidiosis.
Workshop on intestinal microsporidia in HIV infection, Paris , Abstract.
- Enriquez FJ 1997. Microsporidia:
immunity and immunodiagnosis. In Abstract 2nd Workshop on Microsporidiosis
and Cryptosporidiosis in Immunodeficient Patients, Ceske Budejovice, Czech
Republic.
- Enriquez FJ, Cruz-Lopez
AP, Palting JD, Cruz-Lopez P, Hernandez-Janregui P, Tellez C, Guerrero J,
Curran B 1997. Prevalence of microsporidial infection in children and adults
with diarrhea. In Abstracts of the 97th General Meeting of the American Society
for Microbiology. Washington DC, Abstr. C-216, p. 158.
- Field AS, Hing MC, Marriott
DJ 1993. Small intestinal microsporidiosis in HIV infected patients in Sydney,
Australia. In Abstract 1st Workshop on Microsporidiosis and Cryptosporidiosis
in Immunodeficient Patients, Ceske Budejovice, Czech Republic.
- Field AS, Marriott DJ,
Milliken ST, Brew BJ, Canning EU, Keuch JG, Darveniza P, Harkness JL 1996.
Myositis associated with a newly described microsporidian, Trachipleistophora
hominis, in a patient with AIDS. J Clin Microbiol 34: 2803-2811.
[ Medline ]
- Franzen C, Diehl V, Mahrle
G, Hartmann P, Fatkenheuer G, Salzberger B, Schwenk A, Müller A, Visvesvara
GS, Schwartz DA 1995. Immunologically confirmed disseminated, asymptomatic
Encephalitozoon cuniculi infection of the gastrointestinal tract in
a patient with Aids. Clin Infect Dis 21: 1480-1484.
[ Medline ]
- Franzen C, Müller A, Salzberger
B, Fatkenheuer G, Diehl V, Schrappe R 1996. Chronic rhinosinusitis in patients
with Aids: potential role of microsporidia. AIDS 10: 687-688.
[ Medline ]
- Friedberg D, Stenson S,
Orenstein J, Tierno D, Charles N 1990. Microsporidial keratoconjunctivitis
in acquired immunodeficiency syndrome. Arch Ophthalmol 108:
504-508.
[ Medline ]
- Grau A, Valls ME, Williams
JE, Ellis DS, Muntane MJ, Nadal C 1996. Miotis por Pleistophora en
un paciente con SIDA. Med Clin Barcelona 107: 779-781.
- Hollister WS, Canning EU,
Weidner E, Field AS, Keuch J, Marriott DJ 1996. Development and ultrastructure
of Trachipleistophora hominis ng., n. sp. after in vitro isolation
from an Aids patient and inoculation into athymic mice. Parasitology 112:
143-154.
[ Medline ]
- Kotler DP, Orenstein JM
1999. Clinical syndromes associated with microsporidiosis. In M Wittner, LM
Weiss (eds), The Microsporidia and Micro-sporidiosis, American Society
of Microbiology, Washington DC, p. 258-292.
- Ledford DK, Overman MD,
Gonzalvo A, Cali A, Mesler SW, Lockey RF 1985. Microsporidian myositis in
a patient with acquired immunodeficiency syndrome. Ann Intern Med 102:
628-630.
- Lom J, Dykova I 1992. Protozoan
Parasites of Fishes. Developments in Aquaculture and Fisheries Sciences,
Elsevier, Amsterdam, London, New York, Tokyo, 314 pp.
- Lowder CY, Meisler DM,
McMahon JT, Longworth DL, Rutherford I 1990. Microsporidia infection of the
cornea in a man seropositive for human immunodeficiency virus. Am J
Ophthalmol 109: 242-244.
[ Medline ]
- Macher AM, Neafie R, Angritt
P, Tuus SM 1988. Microsporidial myositis and the acquired im-munodeficiency
syndrome Aids: a four-year follow-up. Ann Intern Med 109: 343.
- Mansfield KG, Carville
A, Hebert D, Chalifoux L, Shvetz D, Tzipori LS, Lackner AA 1998. Localization
of persistent Enterocytozoon bieneusi infection in normal Rhesus
macaques (Macaca mulatta) to the Hepatobiliary Tree. J Clin
Microbiol 36: 2336-2338.
[ Medline ]
- Magarinos Torres C 1927.
Adffinités de l'Encephalitozoon chagasi, agent étilogique d`une ménigo-encéphalo-myélite
congénitale avec myocardite e myosite chez l'homme. Comptes reudus des
séances de la Société de Biologie: 1787-1789.
- Margileth AM, Strano AJ,
Chandro R, Neafie R, Blum M, McCully RM 1973. Disseminated nosematosis in
an immunologically compromised infant. Arch Pathol 95: 145-150.
[ Medline ]
- Matsubayashi H, Koike T,
Mikata T, Hagiwara S 1959. A case of Encephalitozoon like body infection
in man. Arch Pathol 67: 181-187.
- Molina JM, Modai J, Derouin
F, Jaccard A, Sarfati C, Beanvais B, Oksenhendler E 1995. Disseminated microsporidiosis
due to Septata intestinalis in patients with Aids: clinical features
and response to albendazole therapy. J Infect Dis 171: 245-249.
[ Medline ]
- Orenstein JM, Dieterich
DT, Kotler DP 1993. Albendazole as a treatment for intestinal and disseminated
microsporidiosis due to Septata intestinalis in Aids patients: a report
for four cases. Aids 7 (Suppl. 3): S40-S42.
- Orenstein JM, Gaetz HG,
Yachnis AT, Frankel SS, Mertens RB, Didier ES 1997. Disseminated microsporidiosis
in Aids. Are any organs spared? AIDS 11: 385-386.
[ Medline ]
- Orenstein JM, Tenner M,
Cali A, Kotler DP 1992. A microsporidian previously undescribed in humans,
infecting enterocytes and macrophages, and associated with diarrhea in an
acquired immunodeficiency syndrome patient. Human Pathol 23:
722-728.
[ Medline ]
- Pinnolis M, Egbert PR,
Font RL, Winter FC 1981. Nosematosis of the cornea: case report including
electron microscopic studies. Arch Ophthalmol 99: 1044-1014.
[ Medline ]
- Pol S, Romano C, Richard
S, Carnot F, Dumont JL, Bouche H, Pialonx G, Stern M, Pays JF, Berthelot P
1992. Enterocytozoon bieneusi infection in acquired immunodeficiency
syndrome - related sclerosing cholangitis. Gastroenterology 102: 1778-1781.
- Rabodonirina M, Bertocchi
M, Desportes-Livage I, Cotte L, Levrey H, Piens MA, Momeret G, Colard M, Mornex
JF, Mogou M 1996. Enterocytozoon bieneusi as a cause of chronic diarrhea
in a heart-lung transplantat recipient who was seronegative for human immunodeficiency
virus. Clin Infect Dis 23: 114-117.
[ Medline ]
- Raynaud L, Delbac F, Broussolle
V, Rabodonirina M, Girault V, Wallon M, Cozon G, Vivares CP, Peyron F 1998.
Identification of Encephalitozoon intestinalis in travelers with chronic
diarrhea by specific PCR amplification. J Clin Microbiol 36:
37-40.
[ Medline ]
- Rosberger D, Serdarevic
G, Erlandson R, Bryan R, Schwartz D, Visvesvara G, Keenan PC 1993. Successful
treatment of microsporidial kera-toconjunctivitis with topical fumagillin
in a patient with Aids. Cornea 12: 261-265.
- Schwartz DA, Bryan RT 1997.
Microsporidia. In CR Horsburgh, AM Nelson (eds), Pathology of Emerging
Infections, American Society for Microbiology, Washington DC, p. 61-93.
- Schwartz DA, Bryan RT,
Hewan-Lowe KW, Visvesvara GS, Weber R, Cali A, Angritt P 1992. Disseminated
microsporidiosis (Encephalitozoon hellem) and acquired immunodeficiency
syndrome. Arch Pathol Lab Med 116: 660-666.
[ Medline ]
- Schwartz DA, Visvesvara
GS, Diesenhouse MC, Weber R, Font RL, Wilson LA, Corrent G, Rosberger DF,
Keenen PJ, Grossniklaus H, Hewan-Lowe K, Bryan RT 1993a. Ocular paphology
of microsporidiosis: role of immunofluorescent antibody for diagnosis of Encephalitozoon
hellem in biopsies, smears, and intact globes from seven Aids patients.
Am J Ophthalmol 115: 285-292.
- Schwartz DA, Visvesvara
GS, Leitch GJ, Tashjian L, Pollack M, Holden J, Bryan RT 1993b. Pathology
of symtomatic microsporidial (Encephalitozoon hellem) bronchiolitis
in Aids: a new respiratory pathogen diagnosed from lung biopsy broncho alveolar
lavage, sputum, and tissue culture. Human Pathol 24: 937-943.
- Schwartz DA, Visvesvara
GS, Weber R, Bryan RT 1994. Male genital tract microsporidiosis and Aids:
prostatic abcess due to Encephalitozoon hellem. J Eukaryot Microbiol
41: 61S.
- Shadduck JA, Meccoli RA,
Davis R, Font RL 1990. Isolation of a microsporidian from a human patient.
J Infect Dis 162: 772-776.
- Silveira H, Canning EU
1995. Vittaforma corneae N. Comb. for the human microsporidium Nosema
corneum Shadduck, Meccoli, Davis & Font, 1990, based on ist ultrastructure
in the liver of experimentally infected athymic mice. J Eukaryot Microbiol
42: 158-165.
[ Medline ]
- Silverstein B, Cunningham
EJ, Margolis T, Cavallos V, Wong I 1997. Microsporidial keratoconjunctivitis
in a patient without human immunodeficiency virus infection. Am J Ophthal
Mol 124: 395-396.
- Soule JB, Orenstein JM,
Pistole MC, Becker RB, Helverson AL 1997. A patient with acquired immunodeficiency
syndrome and untreated Encephalitozoon (Septata) intestinalis micro-sporidiosis
leading to small bowel perforation: response to albendazole. Arch Pathol
Lab Med 121: 880-887.
[ Medline ]
- Sprague V 1974. Nosema
connori n. sp., microsporidian parasite in man. Trans Amer Microsc
Soc 93: 400-403.
[ Medline ]
- Sprague V 1977. Annoted
host of species of microsporidia. In LA Bulla, TC Chang (eds), Comparative
Pathology, 2 Systematics of the Microsporidia, Plenum Press New York,
London.
- Sprague V, Becnel JJ 1998.
Note on the name-author-date combination for the taxon Microsporidies Balbiani
1882, when ranked as a phylum. J Invertebr Pathol 71: 91-94.
- Suter C, Mathis A, Hoop
R, Deplazes P 2000. Imported Encephalitozoon hellem infection in a
wild parrot (Chalopsitta sciutillata) from Indonesia. Vet Res,
in press.
- Tzipori S, Carville A,
Widmer G, Kotler D, Mansfield K, Lackner A 1997. Transmission and establishment
of a persistent infection of Enterocytozoon bieneusi, derived from
a human with Aids, in simian immunodeficiency virus infected rhesus monkey.
J Infect Dis 175: 1016-1020.
[ Medline ]
- Vavra J, Larsson JTR 1999.
Structure of the microsporidia. In M Wittner, LM Weiss (eds),The Microsporidia
and Microsporidiosis, American Society for Microbiology, Washington
DC, p.7-84.
- Vavra J, Yachnis AT, Shadduck
JA, Orenstein JM 1998. Microsporidia of the genus Trachipleistophora -
causative agent of human microsporidiodid. Description of Trachipleistophora
anthropopthera n. sp., (Protozoa, Microsporidia). J Eukaryot Microbiol
45: 273-283.
- Weber R, Bryan RT, Schwartz
DA, Owen RL 1994. Human microsporidial infection. Clin Microbiol
Reviews 7: 426-461.
- Weber R, Deplazes P, Flepp
M, Mathis A, Baumann R, Sauer B, Kuster H, Luethy R 1997. Cerebral microsporidiosis
due to Encephalitozoon cuniculi in a patient with human immunodeficiency
virus infection. N Engl J Med 336: 474-478.
[ Medline ]
- Weber R, Kuster H, Keller
R, Baechi T, Spycher MA, Briner J, Russi E, Luethy R 1992. Pulmonary and intestinal
microsporidiosis in a patient with the acquired immunodeficiency syndrome.
Am Rev Respir Dis 146: 1603-1605.
[ Medline ]
- Weber R, Kuster H, Visvesvara
GS, Bryan RT, Schwartz DA, Luethy R 1993. Disseminated microsporidiosis due
to Encephalitozoon hellem: pulmonary colonization, microtic hematurie
and mild conjubctivitis in a patient with Aids. Clin Infect Dis 17:
415-419.
[ Medline ]
- Weber R, Schwartz DA, Deplazes
P 1999. Laboratory Diagnosis. In M Wittner, LM Weiss (eds), The Microsporidia
and Microsporidiosis, American Society for Microbiology, Washington DC,
p. 315-362.
- Wittner M, Weiss LM 1999.
The Microsporidia and Microsporidiosis, American Society for Microbiology,
Washington DC, USA, 553 pp.
- Wright JH, Craighead EM
1922. Infectious motor paralysis in young rabbits. J Exp Med 36:
135-149.
- Zender HO, Arrigoni E,
Eckert J, Kapanci Y 1989. A case of Encephalitis cuniculi peritonitis
in a patient with Aids. Am J Clin Pathol 92: 352-356.
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