Yak thelaziasis in the Orenburg Oblast: Musca autumnalis (De Geer, 1776) as a vector and Thelazia rhodesi (Desmarest, 1827) as the causative agent of infestation

INTRODUCTION

Thelaziasis, caused by “eyeworms”, is a seasonal parasitic keratoconjunctivitis spread across both Europe (England, Italy, Spain, France, Croatia, Serbia, Germany, Romania, Poland) and Asia (India, Korea, Taiwan, Thailand, Bangladesh, Mongolia, Indonesia, China, Myanmar, Japan) [1][2][3][4][5][6][7][8][9][10]. Sporadically, the invasion was noted in Africa, Australia, North and South America [2][10].

According to the literature, bovine thelaziasis in the Russian Federation occurs in the Northwestern, Volga, West Siberian, and Far Eastern regions, as well as in the Middle and Southern Urals [11][12][13]. In the Orenburg Oblast, bovine thelaziasis is registered everywhere, the causative agent is Thelazia rhodesi (Desmarest, 1827) [1][12][14].

Currently, 16 Thelazia species have been described [10], the most common are:

– Th. callipaeda (Railliet et Henry, 1910) – oriental eye worm;

– Th. californiensis (Price, 1930) – California eye worm;

– Th. gulosa (Railiet et Henry, 1910) – cattle eye worm;

– Th. lacrymalis (Gurlt, 1831) – eyeworm in horses;

– Th. rhodesi (Desmarest, 1827) parasitic nematode of cattle;

– Th. leesei (Railliet et Henry, 1910);

– Th. alfortensis (Railliet et Henry, 1910);

– Th. skrjabini (Erschov, 1928);

– Th. ershowi (Oserskaja, 1931);

– Th. bubalis (Ramanujachari et Alwar, 1952);

– Th. anolabiata (Molin, 1860).

Nematodes of the genus Thelazia parasitize cattle, domestic horses, Przewalski’s horses, donkeys, mules, and European bison [2][3][4][6][7][8][15]. The infection also affects small ruminants, pigs, cats, dogs, foxes, and rabbits [1][5][9]. Reports in the literature describe infection in deer, badgers, monkeys, and wolves [10]. Several cases of avian infestation have been described [1][2][16].

Thelaziasis in yaks has been confirmed in the Kabardino-Balkarian Republic. The extent of invasion (EI) was 2.7%, and the causative agent was Thelazia gulosa [17][18]. There is evidence that Th. skrjabini can infest yaks [1].

In disadvantaged socioeconomic environments, humans can also become an accidental host of Th. californiensis, Th. gulosa or Th. callipaeda. Thus, thelaziasis is a parasitic zoonosis, which is consistent with the literature data [1][10][19][20][21].

The role of Musca autumnalis (De Geer, 1776) as an intermediate host for nematodes of the genus Thelazia has been extensively described in both Russian [11][12][16] and international literature [2][3][4][10][22].

The aim of this work was to study the vector (Musca autumnalis) and the causative agent (Thelazia rhodesi) of thelaziasis in yaks from the Orenburg Oblast. It is the first time a thelaziasis clinical case in yaks from the Orenburg Oblast is described and it is of significant interest to a broad range of specialists.

MATERIALS AND METHODS

The studies were carried out at the Orenburg Tarpania Steppe Field Station (Institute оf Steppe оf the Urаl Branch оf the Russian Academy of Sciences, Orenburg Federal Research Center оf the Urаl Branch оf the Russian Academy of Sciences) in the Belyayevsky Raion of the Orenburg Oblast. This location is home to an assembled collection of ungulates: in addition to domestic yaks, the site supports populations of Przewalski’s horses, Tibetan kiangs, Bactrian camels and wool goats.

In 2021–2023, yak were clinically examined to assess pathological lesions and inflammation degree in the eyes and conjunctiva.

Parasitic secretophagous dipterans (flies) from the ocular region were collected and counted, and their abundance, species and sex ratios were determined. Collection and counting of insects from the suborder Brachycera Orthorrhapha were carried out throughout the entire flight period of imago using an entomological sweep net directly on the animals, following standard methods for collecting Diptera [23]. Insects were identified using taxonomic keys [24][25][26].

Adult Thelazia nematodes were recovered by irrigating the conjunctival sacs of the yaks. The animal’s head was secured, the eyelids were retracted, and the third eyelid and conjunctival cavity were flushed with a 3% boric acid solution. Strong jets of fluid were produced using a rubber bulb syringe to ensure thorough flushing. Next, contents of the conjunctival cavities were collected [16]. The nematode species were identified morphologically.

The study assessed both the extent of invasion, defined as the percentage of infected animals out of the total examined, and the intensity of invasion, defined as the number of parasite specimens recovered from an individual host.

Photographs were obtained using a Canon 760D camera (Japan) and a Nikon Eclipse E200 microscope (Japan).

RESULTS AND DISCUSSION

Musca autumnalis (the face fly) belongs to the family Muscidae (Latreille, 1802), which includes house flies and stable flies. It belongs to the superfamily Muscoidea, section Calyptratae, suborder Brachycera (Cyclorrhapha), order Diptera [26]. M. autumnalis is widespread in the Palearctic region, throughout Western Europe (Sweden, Norway, Spain, Italy), the Caucasus and Central Asia. These flies inhabit steppe, semi-desert, forest-steppe, and forest landscapes, and are a component of pasture fauna [1].

Fifty-eight species of Diptera – Brachycera from the synbovine complex have been identified in the Orenburg Cis-Urals, 40 of which are capable of mechanically transmitting helminths of medical and veterinary importance (including pinworms, ascarids, whipworms, tapeworms, hookworms, Drascheia megastoma, Habronema, Parabronema, Parafilaria, Setaria, Stephanofilaria, and Thelazia) [27]. M. autumnalis was found to be active throughout the flight period, from early spring to late autumn, confirming its status as a thermophilic species. Figure 1 shows the pronounced sexual dimorphism in eye color and structure between male and female flies. Holoptic eyes in males are adapted for swarming and mating in flight. The male exhibits symmetrical, translucent dark yellow spots located on the third and fourth abdominal tergites. The female has an abdomen entirely covered in a grayish bloom with iridescent spots; setae are developed on the first sternite [26].

Females constituted the overwhelming majority of the insects captured. The ratio of females to males collected from the head region was 83 and 17%, respectively, confirming the data of G. A. Kotelnikov [16] and F. Gregor et al. [22] regarding the leading role of females from an ecological and veterinary perspective. M. autumnalis serves as a transmission agent for various pathogens, particularly nematodes of the genus Thelazia.

Musca autumnalis is a typical representative of the synbovine, zoophilic fauna. In the imaginal stage, for example, members of the family Muscidae frequently feed on secretions from wounds and the ocular, nasal, and oral mucosa of grazing animals [26].

Nartshuk E. P. [26] and Ageeva T. Yu. [27] regard female M. autumnalis as facultative hematophages, a characterization that does not contradict the data obtained in the present study. M. autumnalis lacks a piercing proboscis capable of actively penetrating the skin of mammals. However, females possess prestomal teeth, with which they can damage healing wounds and mucous membranes, thereby sustaining inflammatory processes and obtaining nourishment.

Larvae of M. autumnalis are specialized saprophages that develop in and feed on vertebrate dung, exhibiting a coprophagous habit specific to the Muscidae [11][26].

During the summer, the animals under study were kept together as a single herd, managed under semi-wild conditions on natural pasture. The general condition of the experimental animals was satisfactory; appetite and movement were normal. Water was provided from an open source, the Sazan stream. In winter, the animals were maintained under covered shelters. No antiparasitic drugs were administered to the animals.

Profuse lacrimation was recorded as one of the clinical signs of thelaziasis in the yaks. The animals presented with chronic recurrent keratoconjunctivitis and exhibited visual impairment, which is consistent with the findings of D. F. L. Djungu et al. [7].

Other clinical signs associated with thelaziasis are photophobia, blepharospasm, and ulcerative as well as non-ulcerative keratitis. Reported complications include granulomas and corneal perforations, inflammation of the lens, ectropion of the eyeball, corneal opacity (leukoma) resulting from nematode migration through the cornea, fibrohemorrhagic iridocyclitis, and blindness [1][9][10][11]. The clinical course of thelaziasis is frequently complicated by secondary infections, further compromising the animals’ health [10][11][12][13][14].

In the overwhelming majority of cases, thelaziasis-associated keratoconjunctivitis in yaks was observed to be bilateral. No age- or sex-related differences were observed, which contrasts with the findings of D. M. Tweedle et al. [8] that cattle aged 21 to 38 months were more commonly affected.

The intensity of invasion was determined to be 5, and the extent of invasion was 100%; this contrasts with the findings of A. K. Oshkhunov et al. [17]. In conclusion, yaks introduced into the natural and climatic conditions of the Orenburg steppes acquired the infection during the process of acclimatization.

Thelaziasis clinical signs were observed throughout the entire M. autumnalis flight period, thereby determining the disease seasonality. This finding is consistent with the data reported by D. M. Tweedle et al. [8], E. Kim et al. [9], and R. R. Kasarla et al. [10].

Nematodes were isolated from the conjunctival sacs of yaks during helminthoscopic examination by flushing, followed by collection and microscopic analysis. The parasites were identified as belonging to the species Th. rhodesi, and all nematodes recovered were female. Figure 2 illustrates that the females were approximately 20 mm long. They were highly motile, whitish in color, and barely visible to the naked eye within the conjunctival sac. The nematodes were most visible in the medial canthus (inner corner) of the yaks’ eyes.

The species Th. rhodesi belongs to the genus Thelazia, the order Spirurida, the family Thelaziidae, the type Nematoda, nematodes, or roundworms. Microscopically, the head end of Th. rhodesi has a cross-striations, as shown in Figure 3. The serrated cuticle of the nematodes inflicts mechanical damage to the corneal and conjunctival surfaces, resulting in inflammation.

Excessive lacrimation is a response to damage to the eye tissues. The blood-feeding fly M. autumnalis, acting as a facultative hematophage, induces profuse lacrimation in animals both through mechanical trauma to the cornea and by transmitting Thelazia infestation. In addition to the mechanical effects caused by the nematodes, there is also evidence (Glazunova L. A. et al. [1]) of their allergic and toxic pathological influence on the host. Khristianovsky P. I. et al. describe the phenomenon of parasite carriage by definitive hosts as a cause of annual infection in animals [12].

Larvae of Thelazia are excreted from the bodies of afflicted yaks through the lacrimal passages, namely from the lacrimal gland ducts, the conjunctival cavity, and the area under the third eyelid. M. autumnalis consumes the secretion of the lacrimal glands together with Thelazia larvae, thereby acting as a specific thelaziasis intermediate host. The nematodes reach the final stage of their development within the host organism over a period of approximately one month. Transmission of infective larvae to the definitive host occurs when flies ingest (take up) the larvae while feeding on yaks’ tears and mucous secretions with their proboscises.

CONCLUSION

As a vector-borne parasitic zoonosis, thelaziasis continues to be of considerable importance in both human and veterinary medicine, necessitating continued research.

Thelaziasis in yaks is documented for the first time in the Belyayevsky Raion of the Orenburg Oblast, contributing both theoretical and practical value to the understanding of this disease.

The isolated nematodes were identified as Th. rhodesi. M. autumnalis, a species ubiquitous in the steppe ecosystems of Orenburg, served as the vector for Thelazia transmission. The chronic nature of the disease is linked to pathogen carriage over the winter stall period. Clinical manifestations and disease progression in yaks were driven by the mechanical, allergic, and toxic effects of Th. rhodesi, combined with a relatively low infestation intensity.

No distinct differences in clinical signs, diagnostic methods, prevention, or treatment were observed between thelaziasis in yaks and that in cattle. Preventive and therapeutic measures against thelaziasis in yaks should include seasonal applications of repellents and insecticides, as well as scheduled anthelmintic treatments. To control the incidence of thelaziasis, it is necessary to manage the population size of vector flies and maintain proper zoohygienic conditions on farms.

Contribution of the author: Kuzmina E. N. – study concept and design, data collection, manuscript preparation and editing.

Вклад автора: Кузьмина Е. Н. – разработка концепции, проведение исследования, подготовка и редактирование текста рукописи.