Next Article in Journal
Effect of Powder from Different Jackfruit (Artocarpus heterophyllus Lam.) Sections on Performance, Blood Indices, Carcass Characteristics, and Meat Quality of Rabbits
Previous Article in Journal
Patellar Shape Variation in Cats and Dogs: Implications for Orthopedic Surgical Planning
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 15
Issue 11
10.3390/ani15111606
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Oxyspirura petrowi Causing Ocular Parasitism in a Free-Ranging Common Buzzard (Buteo buteo) in Romania and a Review of the Potential Zoonotic Implications as Cutaneous Larval Migrans

by
Călin Mircea Gherman
1,
Angela Monica Ionică
2,*,
Katarzyna Anna Hołówka
1,
Vlad Dan Cotuțiu
1,
Carla Andreea Culda
1,
Georgiana Iulia Lupu
1 and
Andrei Daniel Mihalca
1
1
Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăștur 3-5, 400372 Cluj-Napoca, Romania
2
Clinical Hospital of Infectious Diseases of Cluj-Napoca, 23 Iuliu Moldovan, 400348 Cluj-Napoca, Romania
*
Author to whom correspondence should be addressed.
Animals 2025, 15(11), 1606; https://doi.org/10.3390/ani15111606
Submission received: 25 April 2025 / Revised: 19 May 2025 / Accepted: 22 May 2025 / Published: 30 May 2025
(This article belongs to the Section Wildlife)
Browse Figures
Versions Notes

Simple Summary

Birds are equally affected by thelaziid eyeworms as mammals are. Thelazia species, common in birds, are mainly distributed in the Neotropics, while Oxyspirura spp. are spread worldwide. Raptors are among the most affected species by eyeworms. This study aimed to morphologically and molecularly characterize two eyeworm specimens collected from common buzzards (Buteo buteo) in Romania. One of the 92 examined birds revealed eye parasitism (1/92; 1.08%). Morphologically, collected specimens resembled Oxyspirura petrowi and sequencing showed a 98.36% similarity to the same species. To our knowledge, this is the first report of O. petrowi in the common buzzard.

Abstract

Bird eyes are more neglected organs in studies targeting the structure of the helminth fauna, which are instead mainly focused on the digestive and respiratory systems. In an extended study aimed at identifying helminths in the common buzzard (Buteo buteo), the eyes of 92 birds were also examined. Morphological characteristics and molecular analyses were used to identify the collected specimens. Eyeworms were found in only one bird, a juvenile male (1/92; 1.08%). Two nematodes were collected, a female and a fourth-stage larva. This is the first report of Oxyspirura petrowi in the common buzzard. The results highlight the need for careful examination of raptors’ eyes as ocular parasitism can affect their vision.

Graphical Abstract

1. Introduction

The common buzzard, Buteo buteo, is a diurnal bird of prey and partial migrant that is spread almost throughout Europe, up to central Asia, and is present on several islands in the eastern Atlantic [1]. The species’ world population is estimated at 2,170,000–3,690,000 individuals [2], while European pairs range between 882,000 and 1,230,000 pairs [3]. In Romania, the evaluated population is 20,000–50,000 pairs, with an unknown, albeit likely, increasing trend [2].
The species is a generalist predator with an opportunistic feeding strategy. Its diet includes mammals, birds, reptiles, amphibians, arthropods, and fish, with predominance of the order Rodentia [4,5,6]. This varied diet exposes birds to the risk of contamination with a wide variety of helminths belonging to different taxa, Platyhelminthes, Nematoda, or Acanthocephala, confirmed by numerous studies [7,8,9,10]. These helminths most frequently affect the digestive system, with the respiratory system being less often parasitized. Other organs (kidneys, eyes, and brain) represent rare locations of metazoan parasites.
The eye is among one of birds’ rarely affected organs. Still, bird eyeworms belonging to the family Thelaziidae are well documented. The family includes two subfamilies, Oxyspirurinae and Thelaziinae, both containing genera and species that are ocular parasites of birds. Species from the subgenera Thelaziella and Oxyspirura are reported in diurnal raptors [11,12] and other bird orders, while Ceratospira and Hempelia species affect Columbiformes and Passeriformes [13,14]. While members of the family Thelaziidae are notorious, from a public health perspective, for transmitting the oriental eyeworm (Thelazia callipaeda), species reported in birds have yet to infect human eyes.
Given this context, this study aimed to confirm ocular parasitism with nematodes in common buzzards (B. buteo) from Romania by morphological and molecular characterization of the collected specimens.

2. Materials and Methods

2.1. Sample Collection, Origin, and Necropsy

The collected birds’ eyes were examined as part of a more extensive study to determine the structure of the common buzzard’s helminth fauna. The birds originated from all over the country and were found either as roadkill or died from other causes in various rehabilitation centers located in southern (Bucharest), northeastern (Piatra Neamț), western (Oradea), or central Romania (Tg. Mureș).
After collection, the birds were sent to the Parasitic Diseases Department of the Faculty of Veterinary Medicine in Cluj-Napoca. Initially, they were frozen at −18 °C. Subsequently, all birds were postmortem examined, and the eyeball and the appendages in the orbital cavity were individually collected. Afterward, the eyes and annexes were subjected to a parasitological search by opening them, flushing them with saline solution into Petri dishes, and checking under a stereomicroscope (Olympus SZ, Olympus Corporation, Tokyo, Japan). All nematodes were collected, washed with saline, morphologically identified, and later preserved in 70% ethanol for molecular identification.
The age of the birds was determined using a specific guide. Four age groups were recognized: juvenile, 2nd year autumn/3rd year spring, 3rd year autumn/4th year spring, and adults [15]. The sex was identified by genitalia visualization during the necropsy. The frequency (F), prevalence (P), geographical, and sex distribution of the eyeworm infections were assessed.

2.2. Morphological Identification and Characterization of Parasites

Morphological identification was based on the keys described by Addison and Anderson [16] and Pence [17]. Measurements were performed using an Olympus BX61 microscope (Olympus Corporation, Tokyo, Japan), with its dedicated software (Cell F version 3.1). Due to the reduced number of nematode specimens collected, limited morphometry was attempted, mainly targeting buccal capsule dimensions, esophagus length, striation length, and anal pore and vulva distance from tail end.

2.3. Molecular Characterization of Parasites

DNA was isolated from two specimens using a DNeasy Blood and Tissue kit (QIAGEN, Heildberg, Germany), and a ~700 bp fragment of the cytochrome c oxidase subunit 1 (cox1) was amplified using universal primers [18] and bilaterally sequenced using an external service (Macrogen Europe, Amsterdam, The Netherlands). The attained consensus sequences were compared to each other and to other isolates from the GenBank® database by means of basic local alignment search tool (BLAST) analysis (https://blast.ncbi.nlm.nih.gov/Blast.cgi?PROGRAM=blastn&PAGE_TYPE=BlastSearch&LINK_LOC=blasthome, accessed on 10 April 2025).
The phylogenetic analysis was conducted in MEGA X software (version 10.2.6) [19]. The evolutionary history was inferred by the maximum likelihood method, using the Tamura–Nei model [20]. A discrete Gamma distribution was used to model evolutionary rate differences among sites (+G, parameter = 0.3697).

3. Results

A total of 92 specimens of common buzzards were collected between 2017 and 2025, from all over Romania. In terms of age, the fewest birds examined were juveniles (3/92; 3.3%), whilst at the opposite pole the age group from the second autumn year/third spring year (57/92; 62.0%), with intermediate values recorded for the other age categories (Table 1). Regarding the sex of examined birds, 55 were males (55/92; 59.8%) and 37 females (37/92; 40.2%).
Depending on the origin, 2 birds (2/92; 2.2%) were collected from the Alpine ecoregion and 82 from the Continental ecoregion (82/92; 89.1%), both situated in central Romania (Figure 1). Another three birds originated in Pannonian (west of the country) (3/92; 3.25%), two buzzards from Pontic (2/92; 2.2%), and the last three from the Steppic one (3/92; 3.25%), with the last two ecoregions both located in southeastern Romania. Ocular parasitism was revealed in only one specimen, meaning there was a prevalence of 1.08% (1/92). The bird was a juvenile male from the Pannonian ecoregion.

3.1. Morphological Description

Two nematodes were recovered during sampling, one adult female and one L4 larva (Figure 2). While the L4 stage was intact, the female anterior end was sectioned off at the lower third of the esophagus. Therefore, the buccal capsule and some esophagus measurements could not be performed in the affected specimen (Table 2). Eggs within the female specimen’s uterus appeared unembryonated (Figure 2A).

3.2. Molecular Identification

The two sequences were identical to each other and showed a 98.36% similarity to the only Oxyspirura petrowi cox1 sequence available in GenBank® (Accession No. LC333364), with an overlap of 420/427 bp. The subsequent BLAST results include Spirocerca sp. (Accession No. KJ605486, KJ605489), with a similarity of 85.93% (586/661 bp overlap), followed by Thelazia callipaeda (Accession No. AM042550, AM042556, and MN719909), with a similarity of 85.17% (563/661 bp overlap). The currently attained sequence was deposited in GenBank® under the Accession Number PV203592. Our sequence clustered together with the other O. petrowi isolate, forming a sister group of T. callipaeda (Figure 3).

4. Discussion

Eyeworm primarily refers to thelaziid nematodes that infect the orbital cavities, conjunctival sacs, and lacrimal ducts of mammals and birds, which are typical members of the Thelaziidae family. However, the eyes can also be affected by other parasites, such as Philophthalmus trematodes [21], tapeworm larvae [22], and spirurid nematodes like Onchocerca lupi, Setaria sp., and Aprocta sp. [23,24,25], or the protozoan Toxoplasma gondii [26]. Two genera of Thelaziidae, Oxyspirura and Thelazia, each divided into two subgenera, of which Oxyspirura and Thelaziella [27] are significant for bird eye parasitism.
Species of the subgenus Thelaziella Travassos, 1918 differ morphologically from Thelazia spp. through the presence of gubernaculum and differ ecologically due to their specificity for birds. Moreover, they have a restricted geographical distribution to the Neotropical realm, specifically South America, but have also reported in India [28], Japan [29], and Russia [30]. In South America, mainly in Brazil, 15 Thelaziella species were reported [11,14,31], but according to the newest nematode classification [27] only 7 species are recognized within the subgenus. However, the restricted distribution of Thelaziella species in birds, which is particularly limited to Brazil, is intriguing. Generally, thelaziid species are vectored by muscid and drosophilid flies [32,33,34] that take first-stage larvae and will later transmit infective third-stage larvae to a new host. In contrast, no information is available about the intermediate hosts of Thelaziella spp. It is possible that the restricted distribution can be explained by the intervention of intermediate hosts belonging to taxa similar to those of other thelaziids but having, in turn, a restricted geographical distribution. Another explanation could be the neglected nature of parasitological examination of the eyes in wild birds, thus underestimating eyeworm distribution.
In contrast, of the subgenus Oxyspirura Drasche in Stossich, 1897 contains 35 recognized species [27] with a cosmopolitan geographical spread. They parasitize a large variety of bird species belonging to approximately one-third of the bird orders, namely Accipitriformes [35], Bucerotiformes [35], Caprimulgiformes [31,36], Cariamiformes [37], Charadriiformes [35], Coraciiformes [38,39], Cuculiformes [31,40], Falconiformes [12,41], Galliformes [42,43], Gruiformes [40,44], Passeriformes [45], Pelecaniformes [40], Piciformes [40,46], Psittaciformes [47], Ralliformes [48], Strigiformes [49,50], and Trogoniformes [51]. This wide distribution and the polyspecific host–parasite relationships are favored by the biological cycle in which arthropods, predominantly from the Orthoptera and Blattodea orders, act as intermediate hosts [52]. These arthropods are part of the preferred regular diet of many bird species, including nocturnal and diurnal raptors [53]. The birds will be more easily contaminated by consuming arthropods compared to feeding-flies inoculation of Thelaziella larvae, especially when irritated birds become restless and flies’ feeding and larvae transfer can be consecutively interrupted. Two species of the subgenus are significant for birds’ parasitism, namely O. mansoni, found mainly in tropical and subtropical regions of America, Asia, and the Pacific Ocean, and O. petrowi predominantly spread in America, Europe, and Asia [54]. They are reported in various bird species, including multiple species of owls and other raptors [12,41,49].
Here, we report, to the best of our knowledge, for the first time, ocular parasitism with O. petrowi in the common buzzard. Still, apart from North America, the main geographic distribution of the species O. petrowi is reported in different passerines from Europe [55,56] and Asia [57,58]. Within the Buteo genus, there is only one report from Turkey, where O. mansoni was identified in a long-legged buzzard (Buteo rufinus) [12]. In the two specimens isolated in the current study, all measurements were consistent with findings from other recent studies [59], thus confirming the species is O. petrowi.
For animal parasitic nematodes, sequencing of mitochondrial genes such as cytochrome c oxidase subunit 1 (cox1) is widely used to determine lower taxonomic levels and resolve species-level phylogenies due to their high degree of variation [60]. A recent study evaluated six markers for representatives of three families of nematodes of veterinary and medical importance (30 species) and concluded that cox1 is a useful marker for diagnostic or metabarcoding purposes, firstly due to its high interspecific resolution and secondly due to the higher number of sequences available in databases [61]. However, in the present case, cox1 sequences for ocular parasites of birds in general were limited to a single entry of O. petrowi, isolated from a Northern Bobwhite quail, Colinus virginianus, in the USA [62]. The geographic distancing of the two specimens may account for the noted genetic divergence between them (seven SNPs, representing 1.64% of total overlap region). Due to the comparable variation in inter- and intra-specific distances among different lineages, there is no universal similarity ‘cut-off’ characteristic for the interspecific level [63]. Instead, several sister-species pairs would need to be used to determine the minimum level of genetic distance characteristic of species for that particular clade [64]. Nevertheless, in the present case, the species determination was based firstly on morphological determination, while the evolutionary analysis placed our specimen within the same clade as the American isolate.
In addition to affecting vision in parasitized vertebrate animals, the zoonotic potential of the species in the Thelaziidae family is significant. In this background, the transmission of the Thelazia callipaeda from wild and domestic canids, the primary definitive host, to humans by secretophagous flies is well known [65]. However, little is known about the zoonotic nature of the thelaziids parasitizing the birds. While there are no reports of Thelaziella species affecting people, human parasitism has recently been reported for the Oxyspirura genus in Vietnam [66]. Specifically, molecularly identified O. petrowi larvae caused a systemic cutaneous larval nematodiasis, clinically characterized by disseminated pruritic erythema, in a 41-year-old man from Son La Province, northern Vietnam. Since the patient’s neighbors also had the same condition, it was suggested that Oxyspirura sp. larval infection could be a public health concern. The lack of Thelaziella spp. reports in humans is strange since these species are more easily transmitted by flies compared with the orthopterans–oral transmission of O. petrowi. Food habits vary worldwide, including, in some areas, the consumption of arthropods [67]: the Vietnamese patient admitted to having eaten grasshoppers and crickets. Consecutively to this report, larval Oxyspirura spp. infection has been included in the possible etiology of cutaneous larval migrans (CLM) [68]. However, it cannot definitively include bird eyeworms in the list of potentially zoonotic nematodes. Still, a more precise diagnosis of CLM will be required, especially among farm workers in whom such cases were previously attributed to hookworms [69]. Furthermore, a more thorough molecular description of the genus Oxyspirura could provide much needed clarity into its phylogenetics.

5. Conclusions

This study reported eyeworm infection with O. petrowi for the first time in the common buzzard and for the first time in Romania. One adult female and a fourth-stage larva were collected from 1 juvenile male out of 92 examined birds, meaning a prevalence of 1.08%. Morphologically and molecularly, the species O. petrowi was confirmed. The results showed that this eyeworm can also affect raptors which are distant from a wide variety of other bird species. This emphasizes the need for careful eye examination in these birds to highlight such parasitism as the examination of the eyeball is often neglected.

Author Contributions

Conceptualization, C.M.G. and A.M.I.; methodology, C.M.G., A.M.I., V.D.C., C.A.C. and G.I.L.; investigation: all authors; software, A.M.I. and V.D.C.; validation, C.M.G. and A.D.M.; formal analysis, A.M.I.; writing—original draft preparation, C.M.G., A.M.I. and V.D.C.; writing—review and editing, K.A.H., C.A.C., G.I.L. and A.D.M.; visualization, A.D.M.; supervision, C.M.G. and A.D.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Ethical review and approval were waived for this study because it was conducted on dead birds collected from roadsides or humanely euthanized in private vet clinics before sending them to the Parasitic Diseases Department of the Faculty of Veterinary Medicine in Cluj-Napoca due to the impossibility of rescuing them.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data may be shared and should be requested from the corresponding author.

Acknowledgments

We would like to thank everyone involved in providing the dead birds.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Orta, J.; Boesman, P.F.D.; Marks, J.S.; Garcia, E.F.J. Common Buzzard (Buteo buteo), version 1.0. In Birds of the World; del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A., de Juana, E., Eds.; Cornell Lab of Ornithology: Ithaca, NY, USA, 2020. [Google Scholar] [CrossRef]
  2. Societatea Ornitologică Română. Available online: https://pasaridinromania.sor.ro/specii/246/sorecar-comun-buteo-buteo (accessed on 28 February 2025).
  3. BirdLife DataZone. Available online: https://datazone.birdlife.org/species/factsheet/eurasian-buzzard-buteo-buteo (accessed on 28 February 2025).
  4. Sidorovich, A.A.; Ivanovskij, V.V.; Sidorovich, V.E.; Solovej, I.A. Landscape-related variation in the diet composition of the common buzzard (Buteo buteo) in Belarus. Slovak. Raptor J. 2016, 10, 65–74. [Google Scholar] [CrossRef]
  5. Selås, V.; Tveiten, R.; Aanonsen, O.M. Diet of Common Buzzards Buteo buteo in southern Norway determined from prey remains and video recordings. Ornis Fenn. 2007, 84, 97–104. [Google Scholar]
  6. Tapia, L.; Domínguez, J.; Romeu, M. Diet of Common buzzard (Buteo buteo) (Linnaeus, 1758) in an area of Northwestern Spain as assessed by direct observation from blinds. Nova Acta Científica Compostel. Ser. Biol. 2007, 16, 145–149. [Google Scholar]
  7. Hołówka, K.A.; Ionică, A.M.; Ilea, M.; Poșa, A.C.; Cotuțiu, V.D.; Bulacu, A.; Sitko, J.; Vasiliu, O.C.; Mihalca, A.D.; Gherman, C.M. Platyhelminthes of common buzzard (Buteo buteo): Checklist of species in Europe and new parasite-host associations in Romania. Int. J. Parasitol. Parasites Wildl. 2024, 25, 101007. [Google Scholar] [CrossRef] [PubMed]
  8. Santoro, M.; Kinsella, J.M.; Galiero, G.; degli Uberti, B.; Aznar, F.J. Helminth community structure in birds of prey (Accipitriformes and Falconiformes) in southern Italy. J. Parasitol. 2012, 98, 22–29. [Google Scholar] [CrossRef]
  9. Komorová, P.; Sitko, J.; Špakulová, M.; Hurníková, Z.; Sałamatin, R.; Chovancová, G. New data on helminth fauna of birds of prey (Falconiformes, Accipitriformes, Strigiformes) in the Slovak Republic. Helminthologia 2017, 54, 314–321. [Google Scholar] [CrossRef]
  10. Tezel, M.; Girişgin, A.O.; Birlik, S.; Yildirimhan, H.S.; Şenlik, B. Helminths of the digestive tract in Buteo buteo (Falconiformes: Falconidae) in Bursa Province of Northwest Turkey. Turk. J. Zool. 2015, 39, 323–327. [Google Scholar] [CrossRef]
  11. Fagundes-Moreira, R.; Bezerra-Santos, M.A.; Lia, R.P.; Daudt, C.; Wagatsuma, J.T.; de Carmo, E.C.O.; Berger, L.; Chaves da Silva, F.R.; Soares, J.F.; Otranto, D. Eyeworms of wild birds and new record of Thelazia (Thelaziella) aquilina (Nematoda: Spirurida). Int. J. Parasitol. Parasites Wildl. 2024, 23, 100910. [Google Scholar] [CrossRef]
  12. Zerek, A.; Erdem, İ. The first report of Oxyspirura mansoni (Spirurida: Thelaziidae) in a Long-legged buzzard (Buteo rufinus) in Türkiye. Antakya Vet. Bil. Derg. 2024, 3, 16–17. [Google Scholar]
  13. Suedmeyer, W.K.; Smith, T.; Moore, C.; Greiner, E. Ceratospira inglisi Ocular Infestation in a Wompoo Fruit-Dove (Ptilinopus magnificus). J. Avian Med. Surg. 1999, 13, 261–264. [Google Scholar]
  14. Rodrigues, H.O. Espécies de Thelaziinae (Skrjabin) Baylis & Daubney (Nematoda, Thelazioidea) Referidas Para o Brasil. Rev. Bras. Zool. 1996, 13, 343–350. [Google Scholar]
  15. Blasco-Zumeta, J.; Heinze, G.M. Identification Atlas of the Continental Birds of Southwestern Europe; Tundra Ediciones: Toronto, ON, Canada, 2023; p. 574. [Google Scholar]
  16. Addison, E.M.; Anderson, R.C. A review of eyeworms of the genus Oxyspirura (Nematoda: Spirurodidea). J. Wildl. Dis. 1969, 55, 1–8. [Google Scholar]
  17. Pence, D.B. The genus Oxyspirura (Nematoda: Thelaziidae) from birds in Louisiana. Proc. Helminthol. Soc. Wash. 1972, 39, 23–28. [Google Scholar]
  18. Casiraghi, M.; Anderson, T.; Bandi, C.; Bazzocchi, C.; Genchi, C. A phylogenetic analysis of filarial nematodes: Comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 2001, 122, 93–103. [Google Scholar] [CrossRef]
  19. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
  20. Tamura, K.; Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10, 512–526. [Google Scholar]
  21. Somma, A.T.; Steuernagel, A.; Pulido-Murillo, E.A.; Pinto, H.A.; Reifur, L.; Moore, B.A.; Montiani-Ferreira, F. Ocular disease caused by the trematode Philophthalmus lachrymosus in free-living kelp gulls (Larus dominicanus) of Brazil. J. Vet. Med. Sci. 2022, 84, 1447–1452. [Google Scholar] [CrossRef] [PubMed]
  22. Rama, K.; Jahagirdar, V.; Ginnaram, A.R.R.; Pottabathini, R.; Mandapalli, V. Worm in the Eye: A Case Report of Ocular Neurocysticercosis with Adherent Retinal Cyst. Cureus 2023, 15, e50194. [Google Scholar] [CrossRef]
  23. Otranto, D.; Sakru, N.; Testini, G.; Gürlü, V.P.; Yakar, K.; Lia, R.P.; Dantas-Torres, F.; Bain, O. Case report: First evidence of human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). Am. J. Trop. Med. Hyg. 2011, 84, 55–58. [Google Scholar] [CrossRef]
  24. Marzok, M.A.; Desouky, A.R. Ocular infection of donkeys (Equus asinus) with Setaria equina. Trop. Anim. Health Prod. 2009, 41, 859–863. [Google Scholar] [CrossRef]
  25. Beckmann, K.M.; Harris, E.; Pocknell, A.M.; John, S.K.; Macgregor, S.K.; Cunningham, A.A.; Lawson, B. Aprocta cylindrica (Nematoda) infection in a European Robin (Erithacus rubecula) in Britain. J. Wildl. Dis. 2014, 50, 986–989. [Google Scholar] [CrossRef] [PubMed]
  26. Kalogeropoulos, D.; Sakkas, H.; Mohammed, B.; Vartholomatos, G.; Malamos, K.; Sreekantam, S.; Kanavaros, P.; Kalogeropoulos, C. Ocular toxoplasmosis: A review of the current diagnostic and therapeutic approaches. Int. Ophthalmol. 2022, 42, 295–321. [Google Scholar] [CrossRef]
  27. Hodda, M. Phylum Nematoda: A classification, catalogue and index of valid genera, with a census of valid species. Zootaxa 2022, 5114, 1–289. [Google Scholar]
  28. Majumdar, N.; Sarkar, S.D. On four new species of avian nematodes from Orissa, India. Rec. Zool Surv. India 1989, 85, 467–480. [Google Scholar] [CrossRef]
  29. Murata, K.; Asakawa, M. First report of Thelazia sp. from a captive Oriental white stork (Ciconia boyciana) in Japan. J. Vet. Med. Sci. 1999, 61, 93–95. [Google Scholar] [CrossRef]
  30. Daiya, G.G. Nematode fauna of diurnal predatory birds and owls in the Yakutsk region. Tr. Gel’mintol Lab. 1968, 19, 73–82. [Google Scholar]
  31. Strachan, A.A. Eye worms of the family Thelaziidae from Brazilian birds. Can. J. Zool. 1957, 35, 179–187. [Google Scholar] [CrossRef]
  32. Otranto, D.; Traversa, D. Thelazia eyeworm: An original endo- and ecto-parasitic nematode. Trends Parasitol. 2005, 21, 1–4. [Google Scholar] [CrossRef]
  33. Otranto, D.; Cantacessi, C.; Testini, G.; Lia, R.P. Phortica variegata as an intermediate host of Thelazia callipaeda under natural conditions: Evidence for pathogen transmission by a male arthropod vector. Int. J. Parasitol. 2006, 36, 1167–1173. [Google Scholar] [CrossRef]
  34. Otranto, D.; Lia, R.P.; Cantacessi, C.; Testini, G.; Troccoli, A.; Shen, J.L.; Wang, Z.X. Nematode biology and larval development of Thelazia callipaeda (Spirurida, Thelaziidae) in the drosophilid intermediate host in Europe and China. Parasitology 2005, 131 Pt 6, 847–855. [Google Scholar] [CrossRef]
  35. Mehdi, A.S. On Some New Species of the Genus Oxyspirura from Birds in Hyderabad, Andhra Pradesh, India. J. Helminthol. 1960, 34, 221. [Google Scholar] [CrossRef] [PubMed]
  36. Drago, F.; Amigo, M.; Podesta, T.; Draghi, R.; Núñez, V. Eyes wide open: First record of eyeworms of genus Oxyspirura (Nematoda-Thelaziidae) in Argentina. Rev. Arg. Parasitol. 2024, 13, 25–29. [Google Scholar]
  37. Vicente, J.J.; Rodrigues, H.O.; Corrêa-Gomes, D.; Pinto, R.M. Nematóides do Brasil. Parte IV: Nematóides de aves. Rev. Bras. Zool. 1995, 12 (Suppl. 1), 1–273. [Google Scholar] [CrossRef]
  38. Muniz-Pereira, L.C.; Vieira, F.M.; Luque, J.L. Checklist of helminth parasites of threatened vertebrate species from Brazil. Zootaxa 2009, 2123, 1–45. [Google Scholar] [CrossRef]
  39. Jairapuri, D.S.; Siddiqi, A.H. A Review of the Genus Oxyspirura Drasche in Stossich, 1897 (Nematoda: Thelaziidae) with Descriptions of Fourteen New Species. J. Helminthol. 1967, 41, 337–363. [Google Scholar] [CrossRef]
  40. Sultana, A. Some new eye-worms from birds in India. Z. Parasitenk 1964, 23, 532–547. [Google Scholar] [CrossRef]
  41. Pinto, R.M.; Vicente, J.J.; Noronha, D. Nematode parasites of brazilian accipitrid and falconid birds (falconiformes). Mem. Inst. Oswaldo Cruz 1994, 89, 359–362. [Google Scholar] [CrossRef]
  42. Dunham, N.R.; Soliz, L.A.; Fedynich, A.M.; Rollins, D.; Kendall, R.J. Evidence of an Oxyspirura petrowi epizootic in northern bobwhites (Colinus virginianus), Texas, USA. J. Wildl. Dis. 2014, 50, 552–558. [Google Scholar] [CrossRef]
  43. Dunham, N.R.; Peper, S.T.; Baxter, C.E.; Kendall, R.J. The parasitic eyeworm Oxyspirura petrowi as a possible cause of decline in the threatened lesser prairie-chicken (Tympanuchus pallidicinctus). PLoS ONE 2014, 9, e108244. [Google Scholar] [CrossRef]
  44. Yeh, L.S. A collection of Helminths from a Great Bustard, Otis tarda from Spain, with a description of a new species of Oxyspirura (Nematoda). Proc. Zool. Soc. Lond. 1957, 128, 279–286. [Google Scholar]
  45. Dunham, N.R.; Kendall, R.J. Evidence of Oxyspirura petrowi in migratory songbirds found in the rolling plains of West Texas, USA. J. Wildl. Dis. 2014, 50, 711–712. [Google Scholar] [CrossRef]
  46. Pinto, R.M.; Vicente, J.J.; Noronha, D. Nematode parasites of brazilian piciformes birds: A general survey with description of Procyrnea anterovulvata n. sp. (Habronematoidea, Habronematidae). Mem. Inst. Oswaldo Cruz 1996, 91, 479–487. [Google Scholar] [CrossRef]
  47. Lee, A.R.; Irving, A.C.; Pomroy, W.E. Oxyspirura sp. in the eye of a New Zealand Kaka (Nestor meridionals). N. Z. J. Zool. 2001, 28, 227–231. [Google Scholar]
  48. Okulewicz, A.; Okulewicz, J.; Hildebrand, J.; Zaleśny, G. New data on straggled eyeworm Oxyspirura chabaudi (Baruš, 1965) (Nematoda, Thelaziidae) in Europe. Acta Parasit. 2007, 52, 292–294. [Google Scholar] [CrossRef]
  49. Niedringhaus, K.D.; Dumbacher, J.P.; Dunker, F.; Medina, S.; Lawson, B.; Fenton, H.M.A.; Higley, J.M.; Haynes, E.; Yabsley, M.J. Apparent Prevalence, Diversity, and Associated Lesions of Periorbital Nematodes in a Population of Barred Owls (Strix varia) from Northern California, USA. J. Wildl. Dis. 2023, 59, 299–309. [Google Scholar] [CrossRef]
  50. Rodriguez-Tovar, L.E.; Casas-Martínez, A.; Ramírez-Romero, R.; Nevárez-Garza, A.M.; Zarate-Ramos, J.J. First report of Oxyspirura sp. from a captive fulvous owl (Strix fulvescens) in Mexico. J. Parasitol. 2008, 94, 1430–1431. [Google Scholar] [CrossRef] [PubMed]
  51. Vicente, J.J.; Pinto, R.M.; Noronha, D.; Goulart de Carvalho, P. Nematode Parasites of Brazilian Pelecaniformes and Trogoniformes Birds: A General Survey with New Records for the Species. Rev. Bras. Zool. 1996, 13, 891–901. [Google Scholar] [CrossRef]
  52. Almas, S.; Gibson, A.G.; Presley, S.M. Molecular detection of Oxyspirura larvae in arthropod intermediate hosts. Parasitol. Res. 2018, 117, 819–823. [Google Scholar] [CrossRef]
  53. Mwansat, G.S.; Turshak, L.G.; Okolie, M.O. Insects as important delicacy for birds: Expanding our knowledge of insect food ecology of birds in the Tropics. J. Int. Sci. Publ. Ecol. Saf. 2015, 9, 434–441. [Google Scholar]
  54. Yazwinski, T.A.; Tucker, C.A. Nematodes. In Diseases of Poultry, 12th ed.; Saif, Y.M., Fadly, A.M., Glisson, J.R., McDougald, L.R., Nolan, L.K., Swayne, D.E., Eds.; Blackwell Publishing Professional: Ames, IA, USA, 2008; Section IV: Parasitic Diseases; pp. 1025–1056. [Google Scholar]
  55. Barus, V. On Some Species of the Genus Oxyspirura (Nematoda, Thelaziidae) from Birds in Czechoslovakia. J. Helminthol. 1965, 39, 117–124. [Google Scholar] [CrossRef]
  56. Skrjabin, K.I. Nematoden der Gattung Oxyspirura Drasche aus den Augen der Vogel. Soliaznoi Gel’mintol. Ekspeditsii Sib. Krai 1929, 5, 213–234. [Google Scholar]
  57. Skrjabin, K.I. Neue Nematoden der Gattung Oxyspirura Drasche aus dem Vogelauge. Z. Parasitenkunde 1931, 3, 726–740. [Google Scholar] [CrossRef]
  58. Ahmed, A. The eyeworm, Oxyspirura petrowi Skrjabin, 1929 (Nematoda, Thelaziidae) in the Masked Shrike Lanius nubicus Lichtenstein, 1823 (Passeriformes, Laniidae) collected in Baghdad City, Central Iraq. Int. J. Recent. Sci. Res. 2013, 4, 1126–1128. [Google Scholar]
  59. Kalyanasundaram, A.; Brym, M.; Blanchard, K.; Henry, C.; Skinner, K.; Henry, B.; Herzog, J.; Hay, A.; Kendall, R. Life-cycle of Oxyspirura petrowi (Spirurida: Thelaziidae), an eyeworm of the northern bobwhite quail (Colinus virginianus). Parasites Vectors 2019, 12, 555. [Google Scholar] [CrossRef] [PubMed]
  60. Hwang, U.W.; Kim, W. General properties and phylogenetic utilities of nuclear ribosomal DNA and mitochondrial DNA commonly used in molecular systematics. Korean J. Parasitol. 1999, 37, 215–228. [Google Scholar] [CrossRef]
  61. Mejías-Alpízar, M.J.; Porras-Silesky, C.; Rodríguez, E.J.; Quesada, J.; Alfaro-Segura, M.P.; Robleto-Quesada, J.; Gutiérrez, R.; Rojas, A. Mitochondrial and ribosomal markers in the identification of nematodes of clinical and veterinary importance. Parasit. Vectors 2024, 17, 77. [Google Scholar] [CrossRef]
  62. Kalyanasundaram, A.; Blanchard, K.R.; Henry, C.; Brym, M.Z.; Kendall, R.J. Phylogenetic analysis of eyeworm (Oxyspirura petrowi) in northern bobwhite (Colinus virginianus) based on the nuclear 18S rDNA and mitochondrial cytochrome oxidase 1 gene (COX1). Parasitol. Open 2018, 4, e7. [Google Scholar] [CrossRef]
  63. Goldstein, P.Z.; DeSalle, R.; Amato, G.; Vogler, A.P. Conservation genetics at the species boundary. Conserv. Biol. 2000, 14, 12–31. [Google Scholar] [CrossRef]
  64. Nadler, S.A.; Pérez-Ponce DE León, G. Integrating molecular and morphological approaches for characterizing parasite cryptic species: Implications for parasitology. Parasitology 2011, 138, 1688–1709. [Google Scholar] [CrossRef]
  65. Otranto, D.; Dantas-Torres, F. Transmission of the eyeworm Thelazia callipaeda: Between fantasy and reality. Parasites Vectors 2015, 8, 273. [Google Scholar] [CrossRef]
  66. Dung, D.T.; Hop, N.T.; Tho, T.H.; Nawa, Y.; Doanh, P.N. Pruritic Cutaneous Nematodiasis Caused by Avian Eyeworm Oxyspirura Larvae, Vietnam. Emerg. Infect. Dis. 2020, 26, 786–788. [Google Scholar] [CrossRef] [PubMed]
  67. Magara, H.J.O.; Niassy, S.; Ayieko, M.A.; Mukundamago, M.; Egonyu, J.P.; Tanga, C.M.; Kimathi, E.K.; Ongere, J.O.; Fiaboe, K.K.M.; Hugel, S.; et al. Edible Crickets (Orthoptera) Around the World: Distribution, Nutritional Value, and Other Benefits-A Review. Front. Nutr. 2021, 7, 537915. [Google Scholar] [CrossRef] [PubMed]
  68. Mathison, B.A.; Bradbury, R.S.; Pritt, B.S. Medical Parasitology Taxonomy Update, January 2018 to May 2020. J. Clin. Microbiol. 2021, 59, e01308-20. [Google Scholar] [CrossRef] [PubMed]
  69. Stufano, A.; Foti, C.; Lovreglio, P.; Romita, P.; De Marco, A.; Lia, R.P.; Otranto, D.; Iatta, R. Occupational risk of cutaneous larva migrans: A case report and a systematic literature review. PLoS Negl. Trop. Dis. 2022, 16, e0010330. [Google Scholar] [CrossRef]
Animals 15 01606 g001
Figure 1. Ecoregional origin of the common buzzards collected from Romania.
Figure 1. Ecoregional origin of the common buzzards collected from Romania.
Animals 15 01606 g001
Animals 15 01606 g002
Figure 2. Morphological appearance and morphometric data of the identified eyeworms in a common buzzard from Romania. (A) Mid-section of the female specimen featuring eggs and striation measurements. B-D, buccal capsule and esophagus (B), overview (C), and tail end (D) of the L4 stage.
Figure 2. Morphological appearance and morphometric data of the identified eyeworms in a common buzzard from Romania. (A) Mid-section of the female specimen featuring eggs and striation measurements. B-D, buccal capsule and esophagus (B), overview (C), and tail end (D) of the L4 stage.
Animals 15 01606 g002
Animals 15 01606 g003
Figure 3. Bootstrap consensus tree inferred from 1000 replicates. The tree with the highest log likelihood is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches (values below 50 not shown). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. This analysis involved 13 nucleotide sequences. There were a total of 413 positions in the final dataset.
Figure 3. Bootstrap consensus tree inferred from 1000 replicates. The tree with the highest log likelihood is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches (values below 50 not shown). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. This analysis involved 13 nucleotide sequences. There were a total of 413 positions in the final dataset.
Animals 15 01606 g003
Table 1. Age, gender, and ecoregion distribution of the common buzzards collected from Romania.
Table 1. Age, gender, and ecoregion distribution of the common buzzards collected from Romania.
DescriptorFrequency
(n/total)		Distribution (%)
ageJuvenile3/923.3
2nd-year autumn/3rd-year spring57/9262.0
3rd-year autumn/4th-year spring20/9221.7
Adults12/9213.0
sexMales55/9259.8
Females37/9240.2
ecoregionAlpine2/922.2
Continental82/9289.1
Pannonian3/923.25
Pontic2/922.2
Steppic3/923.25
Table 2. Morphometry (in µm) of recovered Oxyspirura petrowi specimens.
Table 2. Morphometry (in µm) of recovered Oxyspirura petrowi specimens.
Morphological TraitFemaleL4
Total body length 14,4046010
Buccal capsuleWidth-10.77
Depth-17.01
EsophagusLength-621.31
Maximum width101.4560.7
Anal poreDistance from tail end290284.87
VulvaDistance from tail end480
Nerve ringFrom anterior end of esophagus-140
Striations 6.24.5
EggsLength30.94-
Width16.37-
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Gherman, C.M.; Ionică, A.M.; Hołówka, K.A.; Cotuțiu, V.D.; Culda, C.A.; Lupu, G.I.; Mihalca, A.D. Oxyspirura petrowi Causing Ocular Parasitism in a Free-Ranging Common Buzzard (Buteo buteo) in Romania and a Review of the Potential Zoonotic Implications as Cutaneous Larval Migrans. Animals 2025, 15, 1606. https://doi.org/10.3390/ani15111606

AMA Style

Gherman CM, Ionică AM, Hołówka KA, Cotuțiu VD, Culda CA, Lupu GI, Mihalca AD. Oxyspirura petrowi Causing Ocular Parasitism in a Free-Ranging Common Buzzard (Buteo buteo) in Romania and a Review of the Potential Zoonotic Implications as Cutaneous Larval Migrans. Animals. 2025; 15(11):1606. https://doi.org/10.3390/ani15111606

Chicago/Turabian Style

Gherman, Călin Mircea, Angela Monica Ionică, Katarzyna Anna Hołówka, Vlad Dan Cotuțiu, Carla Andreea Culda, Georgiana Iulia Lupu, and Andrei Daniel Mihalca. 2025. "Oxyspirura petrowi Causing Ocular Parasitism in a Free-Ranging Common Buzzard (Buteo buteo) in Romania and a Review of the Potential Zoonotic Implications as Cutaneous Larval Migrans" Animals 15, no. 11: 1606. https://doi.org/10.3390/ani15111606

APA Style

Gherman, C. M., Ionică, A. M., Hołówka, K. A., Cotuțiu, V. D., Culda, C. A., Lupu, G. I., & Mihalca, A. D. (2025). Oxyspirura petrowi Causing Ocular Parasitism in a Free-Ranging Common Buzzard (Buteo buteo) in Romania and a Review of the Potential Zoonotic Implications as Cutaneous Larval Migrans. Animals, 15(11), 1606. https://doi.org/10.3390/ani15111606

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop