In the last few decades, the apparently more frequent occurrence of
zoonotic helminth infections in man have attracted the attention of parasitologists.1 In particular have been those brought about by
the genus Dirofilaria, which has been reported to
cause more than 900 cases of human infection. Most of them were due to Dirofilaria repens and Dirofilaria immitis. Therefore, it is worth reporting on a recent human case caused by Macacanema formosana, a filarial parasite of the catarrhine
monkeys (Macaca cyclopsis), that came to our attention
and apparently has never been reported in humans.
The patient was a 19-year-old woman who had been living in an urban
area of northern Taiwan since childhood. She visited the Department of Ophthalmology,
Taipei Veterans General Hospital in November 1999 owing to sudden pain and
redness in her left eye. Mild swelling of the left lower eyelid was noted
for 1 month and several episodes of severe left periorbital pain happened
within these few months. She had never traveled outside Taiwan and never had
animals as pets. Her family had a routine annual picnic at the riverside of
the Hsin-Tien Shi in northern Taiwan until 3 years previously. She could not
recall any unusual insect bite or any contact with monkeys during these picnics.
Complete ophthalmologic examination was performed. Best-corrected visual
acuity was 6/4 OU with Snellen distance chart. Slitlamp examination disclosed
a subconjunctival active worm at the nasal side of her left eye with marked
conjunctival congestion (Figure 1).
Indirect ophthalmoscopic examination revealed a normal fundus. Findings on
examination of the right eye were unremarkable. The results of blood and biochemical
tests, including the eosinophil count, were normal. No microfilaria was found
in blood and urine samples. No lesion was seen on chest radiographs or brain
computed tomographic scans.
The subconjunctival worm under
slitlamp biomicroscope. It was motile and active.
Under local anesthesia, the conjunctiva was incised and dissected. The
worm was removed alive and intact and preserved in 5% formaldehyde for identification.
Histological sections were prepared for further study of the parasite. Periorbital
pain and conjunctival congestion resolved after the surgery. There was no
sign of recurrent infection after 2 years' follow-up.
The parasite was sent to the Department of Public Veterinary Health
and Animal Pathology, University of Bologna, Bologna, Italy, and the Department
of Tropical Medicine, Tulane University Medical Center, New Orleans, La, for
identification. It was later sent to the Museum of Natural History, Paris,
France, for further confirmation of the identity. It was threadlike and approximately
7.5 cm long with a maximum diameter of 510 µm (Figure 2). The anterior extremity (Figure 3) was subconical with a small, round oral opening without
lips and surrounded by 2 pairs of circumoral papillae. The cuticle was thin
with fine transverse striations. The tail (Figure 4) was short with 2 spicules of unequal length. The longer
one (on the worm's left side) measured 512 µm and the shorter (on the
worm's right side) one, partially protruding from the cloaca, was about 120
µm long. There was a row of approximately 7 caudal papillae, asymmetrically
arranged, on either side of the cloaca.
The whole nematode measured 7.5
× 0.5 cm.
The cephalic end of the nematode
(original magnification ×60).
The caudal end of the nematode
where the 2 asymmetrical spicules (S) and some papillae (P) can be seen (original
The esophagus could be visualized through the semitransparent body wall.
It was divided into a short muscular portion and a much longer glandular portion.
The lateral chords contained dark, granular material that could be seen throughout
the length of the chords (Figure 5).
The detail of a segment of Macacanema formosana where the scattered brownish granules
within the lateral chords (L) can be seen (original magnification ×60).
In the transverse section of the worm (Figure 6), the multilayered structure of the cuticle was evident
as was the underlying thin hypodermis. The large lateral chords displayed
clusters of pigmented granules that were scattered in the hypodermis as well.
The muscle cells were coelomyarian and numerous in each quadrant of the body.
The pseudocoele was virtually filled with the large genital tube packed with
developing spermatozoa (spermatocytes). The digestive tube was small and round
and lined with a relatively thick endothelium. On the basis of these morphological
characteristics, the nematode can be identified as an adult male of Macacanema formosana (Nematoda, Onchocercidae, Dirofilariinae).
The morphological characteristics to differentiate M formosana from other nematodes (Filarioidea, Ascaridoid, Oxyuroidea, Strongylid,
Spirurid, Strongyloid, Rhabditoid, and Trichinellae)
were well described by Orihel and Ash.1
Schad and Anderson2 had reported the differential
diagnosis of M formosana with other Onchocercidae,
in particular with Edesonfilaria malayensis, the
nematode most similar to M formosana.
The transverse section of the
nematode (partial). C indicates cuticle; I, intestine; M, muscular fibers;
T, testicle; and arrowheads, brownish granules in the lateral chord (trichrome-Masson-Goldner
stain, original magnification ×250).
Macacanema formosana was first identified and
described by Schad and Anderson in 1963.2
It was a nematode of new genus and species of the family Onchocercidae, subfamily
Dirofilariinae. They found the filaria in the peritracheal tissue and diaphragm
of Macaca cyclopsis, a monkey native to Formosa (Taiwan).
Like all filariae, the microfilariae were found in the blood of the host.
Little was known about this parasite except for a report published in 1968
by Bergner and Jachowski.3 They found the
parasite in the peritracheal and mandibular intermuscular connective tissues.
There was no subconjunctival infection reported in the monkey. The prevalence
rate of M formosana in the Taiwanese monkey was reported
to be as high as 42% in northern Taiwan where the patient had picnicked. Culicoides (Insecta, Diptera, Ceratopogonidae), a cosmopolitan
genus of biting midges often causing great annoyance to man and animals, was
proposed as the most probable transmitting vector of the parasite. Many species
of Culicoides were identified in northern Taiwan.
This large reservoir of the parasite and the existence of the vectors made
human infection possible. To our knowledge, this is the first case of human
infection caused by M formosana to be reported worldwide.
However, other cases in the same area may well have taken place, but unobserved,
as seemed to happen with D repens in endemic zones.4 The prepatent period of the worm has not yet been
determined. Based on the size of the worm, the patient would have been infected
for at least 1 year and symptoms appeared only after the worm migrated into
the subconjunctival space. The reported human Dirofilaria infections usually consisted of a single worm,5
and treatment for the soreness consisted of the worm's surgical removal. There
was no evidence of recurrent infection in our patient after 2 years' follow-up.
Cases of subconjunctival D repens infection
occur widely throughout European, African, Middle Eastern, and Asian countries.
However, it has never been reported in Taiwan. From the cases reported and
our observation, subconjunctival D repens and M formosana infections shared the characteristics of sudden
onset and were treated solely by surgical removal of the worm. From the size
of the worms recovered, they might have been migrating in subcutaneous space
for a period of time and caused symptoms only when they appeared in the subconjunctiva.
The episodic periorbital pain preceding subconjunctival infection in our patient
could be caused by the worm's migration within this area.
The presence of brownish granules in the lateral chords is a phenomenon
that has been observed on other occasions both in other nematodes, such as Mansonella perstans and Edesonfilaria species, and in the selfsame M formosana.
Their origin is obscure and further studies are necessary to understand their
This is, to our knowledge, the first case report of human infection
caused by M formosana although other cases may have
gone by unobserved or unidentified. Since the Taiwan monkeys (Macaca cyclopsis) have been largely involved in laboratory studies
and have close contact with human beings, possible zoonotic infection should
be kept in mind.
We would like to thank Shyh-Haw Tsay, MD, Department of Pathology, Taipei
Veterans General Hospital, and F. Rivasi, PhD, histopathologist at Modena
University, Emilia, Italy, for preparing the histological sections of the
parasite; and Kin-Mu Lee, PhD, Department of Parasitology, National Yang Ming
University, Taipei, and Odile Bain, PhD, Museum of Natural History, Paris,
France, for their kind suggestions on the identity of the parasite.
Presented as a poster at the 18th Congress of the Asia-Pacific Academy
of Ophthalmology, Taipei, Taiwan, March 10-14, 2001.
Corresponding author: Fenq-Lih Lee, MD, Department of Ophthalmology,
Taipei Veterans General Hospital, No. 201, Section 2, Shih-Pai Road, Shih-Pai,
Taipei 11217, Taiwan (e-mail address: email@example.com).
Reprints: Ling-Ing Lau, MD, Department of Ophthalmology, Taipei Veterans
General Hospital, No. 201, Section 2, Shih-Pai Road, Taipei 11217, Taiwan
Lau L, Lee F, Hsu W, Pampiglione S, Fioravanti ML, Orihel TC. Human Subconjunctival Infection of Macacanema formosana: The First Case of Human Infection Reported Worldwide. Arch Ophthalmol. 2002;120(5):643-646. doi: