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Linguatula serrata Tongue Worm in Human Eye, Austria

Article  in  Emerging Infectious Diseases · May 2011

DOI: 10.3201/eid1705.100790 · Source: PubMed

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Linguatula serrata advanced Porocephalida. All species infecting humans are

currently classified as Porocephalida; the species L. serrata
Tongue Worm in and Armillifer armillatus are responsible for most human
cases of infection.
Human Eye,
Austria
The Study
A 14-year-old girl was referred to the eye clinic at the
Medical University of Vienna with an unknown parasite
Martina Koehsler, Julia Walochnik, detected during ophthalmologic examination. The girl
Michael Georgopoulos, Christian Pruente, had redness, pain, and progressive visual loss in the right
Wolfgang Boeckeler, Herbert Auer, eye. Her medical history was unremarkable except that
and Talin Barisani-Asenbauer she had reported regular contact with domestic animals:
2 dogs, cats, and 1 turtle. She had no history of bites or
Linguatula serrata, the so-called tongue worm, is other infestations, and neither she nor any of her animals
a worm-like, bloodsucking parasite belonging to the had been abroad.
Pentastomida group. Infections with L. serrata tongue
Vision was reduced to 0.1 Snellen. Slit lamp
worms are rare in Europe. We describe a case of ocular
linguatulosis in central Europe and provide molecular data
examination revealed a mobile parasite swimming like a fish
on L. serrata tongue worms. in the anterior chamber of the eye (online Appendix Video,
www.cdc.gov/EID/content/17/5/870-appV.htm); signs of
local inflammation with cells and Tyndall phenomena

T he species Linguatula serrata belongs to the

Pentastomida, a still-enigmatic group of worm-like,
bloodsucking parasites that inhabit the upper respiratory
were present. The pupil was round and reactive, the lens
was clear, and a slight iridodonesis was observed. Fundus
examination through a constricted pupil showed no
tract of terrestrial, carnivorous vertebrates, mostly reptiles abnormalities. On general examination, the patient’s heart,
and birds; L. serrata, commonly called tongue worms, lungs, abdomen, and extremities also had no abnormalities.
typically inhabit canids and felids. The intermediate hosts Her nose and throat were examined carefully for additional
of these parasites are usually sheep, cattle, or rodents. parasites. Serologic data including serum chemistry,
The hosts ingest the eggs, and the first instar larva hatches C-reactive protein, fasting blood glucose, erythrocyte
within their intestines, penetrates the mucosa, and retreats sedimentation rate, creatinine, and blood urea nitrogen
into the tissue, where it encysts and molts to the third levels were within normal limits. Her complete blood count
larval stage. Humans can serve as aberrant final hosts after revealed cell differentiation within normal limits without
ingesting raw or poorly cooked viscera (i.e., liver, lungs, eosinophilia. Her chest and sinus radiographs showed
and trachea) of intermediate hosts. This nasopharyngeal no abnormalities. Surgical removal of the parasite was
infection is known as Halzoun syndrome in the Middle complicated because of high mobility of the parasite inside
East or as Marrara in Sudan (1,2). Humans can also serve the anterior chamber. The worm escaped into the posterior
as accidental intermediate hosts, when ingesting the eggs segment of the eye where it was found, after lens removal
(visceral infection) (3). Intraocular infection is extremely and complete vitrectomy, in a recess of the ciliary body. A
rare; only 5 cases caused by L. serrata tongue worms have viable parasite was extracted and transferred to physiologic
been described: 2 from the southern United States (4–5), 1 saline. One month later, the eye was completely free of
from Portugal (6), 1 from Israel (7), and 1 from Ecuador (8). irritation, and 3 months later an artificial intraocular lens
The phylogenetic position of the pentastomids is (ARTISAN; OPHTEC BV, Groningen, the Netherlands)
still not fully resolved. A position as the sister group of was implanted. Final visual acuity was 1.0 Snellen.
branchiurian crustaceans (Maxillopoda) is supported by The surgically extracted parasite was examined
molecular data and sperm morphology (9–11) and is widely microscopically and then subjected to DNA isolation with
accepted today; however, sound evidence also exists for the QIAGEN tissue kit (QIAGEN, Hilden, Germany). The
other classifications (12). The group itself is divided into 18S rDNA was amplified and sequenced stepwise by using
2 orders, the more primitive Cephalobaenida and the more 6 internal primers (P1fw, P1rev, P2fw, P2rev, P3fw, P3rev)
(13) and a 310 ABI PRISM automated sequencer (Applied
Author affiliations: Medical University of Vienna, Vienna, Austria
Biosystems, Darmstadt, Germany); 3 sequences each were
(M. Koehsler, J. Walochnik, M. Georgopoulos, C. Pruente, H. Auer,
obtained from both strands. Fragments were combined to a
T. Barisani-Asenbauer); and University of Kiel, Kiel, Germany (W.
consensus sequence with the GENEDOC sequence editor
Boeckeler)
(www.nrbsc.org/gfx/genedoc), and deposited in GenBank
DOI: 10.3201/eid1705.100790 (accession no. FJ528908). For cluster analysis, primer sites,

870 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 5, May 2011
 L. serrata Tongue Worm

Figure 1. Morphology of Linguatula serrata tongue worm. A) Ventral anterior end with hooks. B) Posterior end laterally with primordial
uterus, genital porus, and intestine (note peristalsis). C) Dorsal anterior end with cuticular structures of apical papillae, chitinoid oral clasp,
and insertions of oral muscles. D) Rows of spicules. Original magnification ×50 (A–C) or ×100 (D) .

unique gaps, and ambiguously aligned sites were excluded, tongue worm (14). Two of the other 5 ocular linguatulosis
resulting in a dataset of ≈1,560 aligned sites. Cluster analysis case-patients mentioned earlier had a recent history of
was performed by using the PHYLIP 3.63 package (www. ocular trauma but whether trauma was related to infection
phylip.com), with neighbor joining, maximum parsimony,
and maximum likelihood as evolutionary models and
100 bootstrap replicates generated for each model. Trees
were rooted with 4 branchiurian sequences (GenBank nos.
DQ925818, DQ925819, AF436004, and DQ925842).
The parasite was 4.5 mm long, appeared whitish, and
had a flattened (tongue-like) body shape with a rounded
anterior (0.9 mm wide) and pointed posterior end (0.35
mm). It had curved hooks with sharp tips on the anterior
ventral side (Figure 1, panel A), a red primordial uterus
stretching from the anterior to the posterior end, a median
ventral genital porus, and a terminal anus (Figure 1, panel
B). The anterior end had apical papillae and a chitinoid
oral clasp (Figure 1, panel C). The cuticle showed 94 rings
and conspicuous spicules (Figure 1, panel D). Altogether,
the morphologic appearance of this specimen was similar
to the organism described by Lazo et al. (8) and could thus
be identified as a third instar larva of L. serrata tongue
worm. The cuticular rings and the spicules at the posterior
margins of the cuticle rings are also characteristic for this
parasite (14).
We assumed the mode of infection to be ingestion
or direct eye contact with L. serrata eggs and the source
of infection to be 1 of the patient’s 2 pet dogs. Dogs are
Figure 2. Rectangular cladogram based on 18S rRNA gene
the typical final hosts of L. serrata tongue worms, and sequences of 6 pentastomid species. The tree was rooted with
children generally tend to have carefree contact with pet 4 branchiura sequences as an outgroup. The numbers at nodes
animals. Unfortunately, neither dog could be investigated represent bootstrap values based on 100 replicates (neighbor
for potential infection. Infection rates of dogs in Austria are joining/maximum likelihood/maximum parsimony). Both subgroups
unknown; only 1 case has been reported, and it occured in of the Pentastomida, the Cephalobaenida (Reighardia sternae,
Hispania vulturis, and Raillietiella spp.) and the Porocephalidae
a dog imported from the United States (15). The girl also (Porocephalus crotali and Armillifer agkistrodontis) are well
had cats and a turtle, but cats are not primary hosts and supported. The choice of outgroup had no effect on tree topology
turtles are never hosts for the life cycle of the L. serrata but did in some cases reduce bootstrap values.

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 5, May 2011 871
 DISPATCHES

remains unknown. In the case reported here, no eye injury 2. Yagi H, el Bahari S, Mohamed HA, Ahmed el-R S, Mustafa B, Mah-
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tb00391.x
The authors thank Christopher Kiss for help with producing 14. Doucet J. Contribution á l’etude anatomique, histologique et his-
the video and Jacek Pietrzak for excellent technical assistance. tochimique des Pentastomes (Pentastomida). Paris: Office de la re-
cherché scientifique et technique Outre–Mer (O.R.S.T.O.M.); 1965.
This work was supported by the Medical University of 15. Leschnik M, Löwenstein M, Edelhofer R, Kirtz G. Imported non-
Vienna, Austria. endemic, arthropod-borne and parasitic infectious diseases in Aus-
trian dogs. Wien Klin Wochenschr. 2008;120:59–62. doi:10.1007/
Dr Koehsler is a postdoctoral researcher at the Department s00508-008-1077-3
of Specific Prophylaxis and Tropical Medicine of the University
of Vienna. Her research interests focus on the molecular biology Address for correspondence: Julia Walochnik, Molecular Parasitology,
of parasites. Institute for Specific Prophylaxis and Tropical Medicine, Centre for
Pathophysiology, Infectiology and Immunology, Medical University
of Vienna, Kinderspitalgasse 15, 1090 Vienna, Austria; email: julia.
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