Emerg Infect DisEmerging Infect. DisEIDEmerging Infectious Diseases1080-60401080-6059Centers for Disease Control and Prevention21529397332176910-130910.3201/eid1705.101309DispatchDispatchHuman Intraocular Filariasis Caused by Pelecitus sp.
Nematode, BrazilFilariasis Caused by
Pelecitus sp. NematodeBainOdileOtrantoDomenicoDinizDaniel G.Nascimento dos SantosJeanniePinto de OliveiraNorimarFrota de AlmeidaIzabela NegrãoFrota de AlmeidaRafael NegrãoFrota de AlmeidaLuciana NegrãoDantas-TorresFilipeSobrinhoEdmundo Frota de AlmeidaAuthor affiliations: Muséum National d’Histoire
Naturelle, Paris, France (O. Bain);Università degli Studi di Bari, Valenzano, Italy (D. Otranto,
F. Dantas-Torres);Universidade Federal do Pará, Belém, Brazil (D.G.
Diniz, J. Nascimento dos Santos, I.N. Frota de Almeida, R.N. Frota de Almeida,
L.N. Frota de Almeida, E. Frota de Almeida Sobrinho);Instituto de Medicina do Olho de Tucuruí, Tucuruí,
Brazil (N. Pinto de Oliveira)Address for correspondence: Domenico Otranto, Dipartimento di
Sanità Pubblica e Zootecnia, Facoltà di Medicina Veterinaria,
Università degli Studi di Bari, Strada Provinciale per Casamassima Km 3,
70010 Valenzano, Bari, Italy; email: d.otranto@veterinaria.uniba.it52011175867869
A male nematode was extracted from iris fibers of a man from the Brazilian Amazon
region. This nematode belonged to the genus Pelecitus but was
distinct from the 16 known species in this genus. Similarities with
Pelecitus spp. from neotropical birds suggested an avian
origin for this species.
Filarial nematodes have been found in the eyes and periorbital region of humans worldwide
(1–4). However, rarely have the worms been removed and
morphologically described. The main human filarial parasites are Wuchereria
bancrofti and Brugia malayi, whose adults live in the
lymphatic system, and Loa loa, which infects subcutaneous tissues. In
addition, some filarioids have an animal origin, either from domestic mammals, such as
for Dirofilaria spp., or from wild mammals, including
Onchocerca, Molinema, and Loaina
spp (1,2,5).
Nematode identification at the species level might be supported by anamnestic
information, such as host and geographic location. However, for a reliable, definitive,
species identification, proper morphologic or molecular diagnosis is needed. Clinical
reports may provide a useful database for better understanding of the zoonotic potential
of little-known filarioids infecting wild animals. We report a case of human intraocular
filariasis caused by a Pelecitus sp., briefly describe the main
morphologic features for nematode identification, and suggest the origin of this
zoonotic infection.
The Study
On August 2007, a 29-year-old man from Tucuruí in northern Brazil, who worked
in power grid maintenance in a forested area, came to his ophthalmologist with an
intraocular larva in the left eye. There was no familial history of ophthalmologic
disorders, and ophthalmologic examinations showed that the patient had visual acuity
and corrected vision of 20/25 in both eyes. Biomicroscopy showed a transparent
cornea in the right eye without lesions or edema, an anterior cavity without an
inflammatory reaction, and an anterior subcapsular cataract of +/4+. The cornea in
the left eye was transparent and did not have lesions or edema, and the anterior
chamber did not show an inflammatory reaction. No funduscopic alterations were found
in either eye by direct and indirect ophthalmoscopic examination.
An ≈4-mm worm with undulating movements was observed between the muscular
fibers of the iris (Figure 1, panel A). The
patient underwent surgery 1 day after the consultation, and he consented to the
publication of this clinical case. After peribulbar anesthesia, a 2-mm corneal
incision was made at the 11 o’clock position. The nematode was extracted by
aspiration (Video) and placed in saline
solution. No surgical complications occurred (Figure
1, panel B), and the patient did not have ocular symptoms during the 6
months after surgery.
Eye of the patient, a 29-year-old man from Brazil. A) Nematode (n) between
muscle fibers of the iris. B) Iris after surgery, showing a mild residual
scar (cr) in the region where the nematode had been located.
Surgical removal of aPelecitus sp. nematode
from the left eye of a 29-year-old man, Brazil. A portion of the material in
this video was previously published in the journal Parasites and Vectors
(http://www.parasitesandvectors.com/content/pdf/1756-3305-4-41.pdf).
Direct Link: http://streaming.cdc.gov/vod.php?id=bec4b66c4804f440dce5072b04eeba0c20110426172737138
The worm was fixed in 2% acetic acid, 3% formaldehyde, and 95% ethanol; mounted in
glycerine jelly; and later transferred into lactophenol. The specimen was preserved
in absolute alcohol at the National Museum of Natural History (Paris, France)
(accession no. 138 YU). This male nematode (length 4.5 mm, width 300 µm at
mid-body) had a coiled and twisted body that tapered at both extremities (Figure 2, panel A). The cuticle (thickness 6
µm) showed 2 rounded, lateral, cuticular alae (thickness 20 μm) along
the body and postdeirids 530 µm from the posterior extremity (Figure 2, panel B). The head was bluntly rounded
and contained 4 externolabial papillae, 4 cephalic papillae, 2 amphids, and a buccal
cavity (length 5 µm, width 4.5 µm) with a tiny cuticular ring. The
nerve ring was 165 µm from the anterior end. The esophagus was 765 µm
long, increased slightly in diameter in the posterior half, and did not have a
distinct glandular part. The large caudal alae had 2 granular inclusions on each
lateral side. The tail was 48 µm long. Five pairs of caudal papillae (2
pedunculated, precloacal, lateral; 1 small subventral closely posterior to the
cloacal opening; and 2 pedunculated lateral pairs on posterior half of the tail)
were observed, and the 2 phasmids were subterminal. The 2 spicules (length 66
µm and 82 µm) (Figure 2, panels
C, D) were dissimilar. The larger left spicule had a typical beveled extremity.
Parasitic nematode isolated from the eye of the patient, a 29-year-old man
from Brazil. A) Nematode that was removed from the iris, showing anterior
(ae) and posterior (pe) extremities. Scale bar = 200 µm. B) Caudal
region, subdorsal view, showing lateral alae, spicules, and the 2
postdeirids. Scale bar = 150 µm. C) Left spicule; D) right spicule.
Scale bars = 20 µm.
Many morphologic characteristics of the filarial worm resembled those of
Pelecitus spp (6). (coiled and twisted body that was attenuated at
both extremities; lateral alae from the cervical region to distal tip of body;
postdierids within alae in the posterior half of body; and a delicate,
preesophageal, cuticular ring). Pelecitus spp. include mainly
parasites of birds and a few mammals, some of which have been identified as
Loaina spp (6,7).
The specimen from the patient was compared with the 16 known species of
Pelecitus described (6,8,9), but the specimen did not match any of them. The
worm differed from the only 2 species found in lagomorphs (P.
scapiceps and P. meridionaleporinus) (9) in North America and Mexico,
which had a beveled extremity on the right spicule (8,9) instead of the left spicule.
A small male filaria was recovered from the anterior chamber of a human eye in
Colombia (5). This filaria
was originally assigned to the genus Loaina but was later
identified as a species of Pelecitus (6). Like the nematode specimen we describe, it
was morphologically similar to some species that infect birds.
Conclusions
We assigned the worm found in the anterior chamber of the eye of the patient to the
genus Pelecitus (6). The species of Pelecitus that
infected the eyes of 2 humans (reported here and in Colombia) (5) remains unidentified. These cases were found
in the tropical Amazon region (Pará, Brazil) and the Department of Antioquia
(northwestern Colombia). The male specimen of Pelecitus sp.
described here and the species that infected a human in Colombia are similar but
distinct. However, in both cases, a mammalian origin of these zoonotic agents seems
unlikely because of differences identified by comparing these worms with parasitic
species infecting lagomorphs (8,9). Both cases of human infection with
Pelecitus spp. more likely have an avian origin. Vectors of
Pelecitus spp. are mosquitoes, chewing lice, and tabanids, as
shown with the 3 cycles elucidated (10–12).
Although infection of birds in South America by Pelecitus spp. has
been reported (13,14), information on this taxon is scant. Many
nematode species have not been identified because of lack of basic information on
filarial fauna of animals. This dearth of information is particularly true for
regions, such as the Amazon rain forest in Brazil, where wide biodiversity and many
unidentified animal and plant species are found (15). Consequently, species identification of
filarioid nematodes that infect human eyes is difficult if not impossible. However,
our identification of this filarid should help clarify the zoonotic role of
filarioid infections in humans in tropical regions and increase awareness of
physicians and ophthalmologists of the variety of nematodes that may be found in the
human eye.
Suggested citation for this article: Bain O, Otranto D, Diniz
DG, Nascimento dos Santos J, Pinto de Oliveira N, Frota de Almeida IN, et al.
Human intraocular filariasis caused by Pelecitus sp. nematode,
Brazil. Emerg Infect Dis [serial on the Internet]. 2011 May [date
cited]. http://dx.doi.org/10.3201/eid1705.101309
Acknowledgment
We thank R.P. Lia for assistance with the laboratory work.
This study was supported by European Community grant INCO-CT-2006-032321 and by
Muséum National d’ Histoire Naturelle grant ATM (Taxonomie
moléculaire: DNA barcode et gestion des collections).
Dr Bain is curator of Zooparasitic Nematodes at the Muséum National
d’Histoire Naturelle, Parasitologie Comparée, Paris, France. Her
research interests include taxonomy and biology of nematodes, in particular
filarioids, infecting animals and humans.
ReferencesBeaverPC. Intraocular
filariasis: a brief review.Am J Trop Med Hyg.
1989;40:40–52644857OrihelTC,
EberhardML. Zoonotic
filariasis.Clin Microbiol Rev.
1998;11:366–819564568SalloF,
EberhardML,
FokE,
BaskaF,
HatvaniI. Zoonotic
intravitreal Onchocerca in Hungary.Ophthalmology.
2005;112:502–410.1016/j.ophtha.2004.10.03615745781PampiglioneS,
RivasiF,
GustinelliA. Dirofilarial
human cases in the Old World, attributed to Dirofilaria
immitis: a critical analysis.Histopathology.
2009;54:192–20410.1111/j.1365-2559.2008.03197_a.x19207944BoteroD,
AguledoLM,
UribeFU,
EsslingerJH,
BeaverPC. Intraocular
filaria, a Loaina species, from man in
Colombia.Am J Trop Med Hyg.
1984;33:578–826476200BartlettCM,
GreinerEC. A revision of
Pelecitus Railliet & Henry, 1910 (Filarioidea,
Dirofilariinae) and evidence for the “capture” by mammals of
filarioids from birds.Bulletin du Muséum National d’Histoire Naturelle
(Paris).
1986;8:47–99EberhardML,
OrihelTC.
Loaina gen. n. (Filarioidea:
Onchocercidae) for the filariae parasitic in rabbits in North
America.Proceedings of the Helminthological Society of Washington.1984;51:49–53BartlettCM. Zoogeography and
taxonomy of Dirofilaria scapiceps (Leidy, 1886) and
D. uniformis Price, 1957 (Nematoda: Filarioidea) of
lagomorphs in North America.Can J Zool.
1983;61:1011–2210.1139/z83-135Jiménez-RuizFA,
GardnerSL,
CervantesFA,
LorenzoC. A new species of
Pelecitus (Filarioidea: Onchocercidae) from the
endangered Tehuantepec jackrabbit Lepus
flavigularis.J Parasitol.
2004;90:803–710.1645/GE-213R115357073BartlettCM. Development of
Dirofilaria scapiceps (Leidy, 1886) (Nematoda:
Filarioidea) in Aedes spp. and Mansonia
perturbans (Walker) and responses of mosquitoes to
infection.Can J Zool.
1984;62:112–2910.1139/z84-019BartlettCM,
AndersonRC.
Pelecitus fulicaeatrae (Nematoda:
Filarioidea) of coots (Gruiformes) and grebes (Podicipediformes):
skin-inhabiting microfilariae and development in Mallophaga.Can J Zool.
1987;65:2803–1210.1139/z87-423SprattDM. Natural
occurrence, histopathology and developmental stages of Dirofilaria
roemeri in the intermediate host.Int J Parasitol.
1972;2:201–810.1016/0020-7519(72)90007-04652607PintoRM,
VicenteJJ,
NoronhaD. Nematode
parasites of Brazilian psittacid birds, with emphasis on the genus
Pelecitus Railliet & Henry, 1910.Mem Inst Oswaldo Cruz.
1993;88:279–8410.1590/S0074-02761993000200016OnikiY,
KinsellaJM,
WillisEO.
Pelecitus helicinus Railliet &
Henry, 1910 (Filarioidea, Dirofilariinae) and other nematode parasites of
Brazilian birds.Mem Inst Oswaldo Cruz.
2002;97:597–810.1590/S0074-0276200200040002712118298BarlowJ,
GardnerTA,
AraujoIS,
Avila-PiresTC,
BonaldoAB,
CostaJE, Quantifying the biodiversity value of tropical primary,
secondary, and plantation forests.Proc Natl Acad Sci U S A.
2007;104:18555–6010.1073/pnas.070333310418003934