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Avian and Emerging Human Oxyspirura Species Compared by Morphology, Pathogenicity, Intermediate Host, and Sequence Homology

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Abstract

Based on sequence homology and phylogenetic tree results, the first report of eyeworm Oxyspirura species larvae has been confirmed in a human patient from Vietnam. However, important information related to Oxyspirura larvae was not presented in the case study. This comment provides a more detailed comparison of the Oxyspirura larvae found in the human case study to the avian eyeworm Oxyspirura petrowi.
Avian and Emerging Human Oxyspirura Species
Compared by Morphology, Pathogenicity, Intermediate
Host, and Sequence Homology
Authors: Kalyanasundaram, Aravindan, Bastille, Maya O., Lukashow-
Moore, Shannon P., and Kendall, Ronald J.
Source: Journal of Parasitology, 106(4) : 623-624
Published By: American Society of Parasitologists
URL: https://doi.org/10.1645/20-106
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Published 2 October 2020
DOI: 10.1645/20-106
Contents and archives available through www.bioone.org or www.jstor.org
Journal of Parasitology
journal homepage: www.journalofparasitology.org
CRITICAL COMMENT . .....
AVIAN AND EMERGING HUMAN OXYSPIRURA SPECIES COMPARED BY MORPHOLOGY,
PATHOGENICITY, INTERMEDIATE HOST, AND SEQUENCE HOMOLOGY
Aravindan Kalyanasundaram, Maya O. Bastille, Shannon P. Lukashow-Moore, and Ronald J. Kendall
The Wildlife Toxicology Laboratory, Texas Tech University, Lubbock, Texas 79409-3290.
Correspondence should be sent to Ronald J. Kendall (https://orcid.org/0000-0003-0527-5399) at: ron.kendall@ttu.edu
KEY WORDS ABSTRACT
Bobwhite
Eyeworm
Human
Intermediate
Oxyspirura
Parasite
Paratenic
Based on sequence homology and phylogenetic tree results, the first report of eyeworm Oxyspirura
species larvae has been confirmed in a human patient from Vietnam. However, important
information related to Oxyspirura larvae was not presented in the case study. This comment provides
a more detailed comparison of the Oxyspirura larvae found in the human case study to the avian
eyeworm Oxyspirura petrowi.
We read with interest the recent article reporting the first
documented case of human infection with Oxyspirura species
larvae (Dung et al., 2020). We published the sequence of the avian
eyeworm Oxyspirura petrowi (accession no. LC316613) that was
found to have high similarity (96.6%) in sequence analysis, as well
as high bootstrap value (93%) in the phylogenetic tree, to the 18S
rRNA sequence of the human patient in Vietnam (Kalyanasun-
daram et al., 2018; Dung et al., 2020). With the above noteworthy
similarity, we provide additional evidence comparing morpholo-
gy, pathogenicity, and information about the intermediate host to
support that the Oxyspirura species of the human case is very
closely related to the avian O. petrowi.
Morphological observations of the recent case study were
similar to third-stage O. petrowi recovered from experimentally
infected house crickets (Acheta domesticus). The Oxyspirura sp.
matched in terms of larvae length (~700–850 lm), nerve ring
distance, papilla (anterior end), and buccal cavity (clear with 6
lobes) and matured anus (Kalyanasundaram et al., 2019b; Dung
et al., 2020), indicating the larvae specimen found in the human
patient was in its third developmental stage. Additionally, we
found embryonated eggs in the fecal samples of Northern
bobwhites (Colinus virginianus), which was not detected in the
human case, indicating humans may be a paratenic host to
Oxyspirura sp. larvae. Paratenic hosts that contain high
accumulations of the parasite in the larval stage without showing
further development in the life cycle are most likely incidental
transporters rather than serving as the parasite’s intermediate
host. This stage was observed in the human case of Oxyspirura
infection.
Pathogenicity findings revealed disseminated pruritic erythema
in the skin of the infected humans (Dung et al., 2020). Northern
bobwhites infected with O. petrowi also showed signs of
inflammation, along with distinct petechial hemorrhaging, corneal
scarring, conjunctivitis, and keratitis was observed in the lacrimal
ducts, eyelid, nictitating membrane, and in the conjunctival sac
(Dunham et al., 2014; Bruno et al., 2015). Our recent O. petrowi
glycoprotein challenge study using host cytokines showed a
measurable immune reaction in experimental bobwhites (Kalya-
nasundaram et al., 2019a). Although the localization of infection
from the Oxyspirura species differed between human and avian
subjects, the parasitic infection ultimately induced a similar lesion
and inflammatory response in both cases.
In the Vietnam case study, the patient and his neighbors
reported that had regularly consumed grasshoppers and crickets
as a part of their diet for more than a year (Dung et al., 2020).
Our recent studies (Kistler et al., 2016; Kalyanasundaram et al.,
2018) experimentally demonstrated that the grasshopper (Bra-
chystola magna) and house cricket (A. domesticus) serve as
intermediate hosts for O. petrowi, indicating that L3 infective
larvae are transmitted to the avian definitive host when ingested.
A recent study (Gałecki and Soko
´ł, 2019), evaluating the
relationship of regularly consumed insects and their role in the
transmission of parasitic diseases to humans and animals, further
supports the theory that frequently consumed insects may serve as
the most significant vector for these parasites. The authors from
the Vietnam study (Dung et al., 2020) also stated that further
investigation of maturated Oxyspirura in poultry in the patient’s
community was needed. However, this might be counterintuitive,
Journal of Parasitology 2020 106(5) 623–624
ÓAmerican Society of Parasitologists 2020
623
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as previous evidence reported the chicken eyeworm O. mansoni
transmits through its single intermediate host, the burrowing
cockroach Pycnoscelus surinamensis (Schwabe, 1951).
In conclusion, the similarities in sequence homology, morphol-
ogy, pathogenicity, and intermediate hosts indicate the Oxyspi-
rura sp. found in the human patient as an emerging pathogen is
very closely related to O. petrowi, and further research is
necessary to determine the extent of the relation by species-level
confirmation.
LITERATURE CITED
BRUNO, A., A. M. FEDYNICH,A.SMITH-HERRON,AND D. ROLLINS.
2015. Pathological response of northern bobwhites to
Oxyspirura petrowi infections. Journal of Parasitology 101:
364–368.
DUNG, D. T., N. T. HOP,H.TRAN,T.H.THO,Y.NAWA,AND P.
N. DOANH. 2020. Pruritic cutaneous nematodiasis caused by
avian eyeworm Oxyspirura larvae,Vietnam.Emerging
Infectious Diseases 4: 786–788.
DUNHAM, N. R., L. A. SOLIZ,A.M.FEDYNICH,D.ROLLINS,AND
R. J. KENDALL. 2014. Evidence of an Oxyspirura petrowi
epizootic in northern Bobwhites (Colinus virginianus), Texas,
USA. Journal of Wildlife Disease 50: 552–588.
GAłECKI, R., AND R. A. SOKO
´ł. 2019. Parasitological evaluation of
edible insects and their role in the transmission of parasitic
diseases to humans and animals. PLoS ONE 7: e0219303.
doi:10.1371/journal.pone.0219303.
KALYANASUNDARAM, A., K. BLANCHARD,C.HENRY,M.BRYM,
AND R. J. KENDALL. 2018. Phylogenetic analysis of eyeworm
(Oxyspirura petrowi) in northern bobwhite (Colinus virgin-
ianus) based on the nuclear 18S rDNA and mitochondrial
cytochrome oxidase 1 gene (COX1). Parasitology Open 4: e7.
doi:10.1017/pao.2018.2.
KALYANASUNDARAM, A., K. R. BLANCHARD,B.J.HENRY,C.
HENRY,M.Z.BRYM,AND R. J. KENDALL. 2019a. Quantitative
analysis of Northern bobwhite (Colinus virginianus) cytokines
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tology Research 118: 2909–2918.
KALYANASUNDARAM, A., M. Z. BRYM,K.R.BLANCHARD,C.
HENRY,K.SKINNER,B.J.HENRY,J.HERZOG,A.HAY,AND R.
J. KENDALL. 2019b. Life-cycle of Oxyspirura petrowi (Spiru-
rida: Thelaziidae), an eyeworm of the northern bobwhite
quail (Colinus virginianus). Parasites & Vectors 2: 555. doi:10.
1186/s13071-019-3802-3.
KISTLER, W. M., S. HOCK,B.HERNOUT,E.BRAKE,N.WILLIAMS,
C. DOWNING,N.R.DUNHAM,N.KUMAR,U.TURAGA,J.A.
PARLOS,ET AL. 2016. Plains lubber grasshopper (Brachystola
magna) as a potential intermediate host for Oxyspirura
petrowi in northern bobwhites (Colinus virginianus). Parasi-
tology Open 2: e7. doi: 10.1017/pao.2016.5.
SCHWABE, C. W. 1951. Studies on Oxyspirura mansoni, the tropical
eyeworm of poultry. II. Life history. Pacific Science 5: 18–35.
624 THE JOURNAL OF PARASITOLOGY, VOL. 106, NO. 5, OCTOBER 2020
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