Open Access
Review Article
Issue
Parasite
Volume 27, 2020
Article Number 52
Number of page(s) 13
DOI https://doi.org/10.1051/parasite/2020048
Published online 29 September 2020

© B. do Vale et al., published by EDP Sciences, 2020

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Members of the genus Thelazia (Spirurida, Thelaziidae) dwell the orbital cavity and associated tissues of several mammals and birds [1], and at least 16 species have been identified in different hosts [49, 75]. However, only Thelazia callipaeda Railliet & Henry, 1910, Thelazia californiensis Price, 1930 and Thelazia gulosa Railliet & Henry, 1910 have been found to affect humans [24, 19].

Thelazia callipaeda is also known as “the oriental eyeworm” because of its distribution throughout the former Soviet Union and East Asia [1, 59, 70]. Nevertheless, at the end of the 20th century, autochthonous cases were reported in Italy [50, 52] and, since then, T. callipaeda has increasingly been reported in some European countries both in animals and humans [75]. In Europe, the intermediate host of this eyeworm is the male drosophilid fruit fly Phortica variegata Fallén, 1823 (Drosophilidae, Steganinae), which feeds on lachrymal secretions of mammals [53, 55, 58, 60].

There are reported cases of thelaziosis in companion animals (dogs and cats), lagomorphs such as hares (Lepus europaeus) and wild rabbits (Oryctolagus cuniculus), but also in wild carnivores, especially red foxes (Vulpes vulpes), which appear to play an important role in the introduction and geographical dispersion of this eyeworm in non-endemic European regions [15, 23, 32, 44, 51, 57].

The importance of studying and investigating thelaziosis lies in the fact that T. callipaeda has a broad spectrum of hosts and the number of infected hosts, including humans, in Europe has been increasing since the beginning of the 21st century. Taking into account that thelaziosis is an expanding disease, it becomes necessary to identify the characteristics of all the cases reported, in order to profile this zoonosis. Therefore, the objective of the present study was to carry out a qualitative and quantitative analysis based on a systematic review of the scientific literature. Consequently, it is expected that this compilation of all reported cases will be useful in future investigations on understanding the evolution of thelaziosis by T. callipaeda.

Materials and methods

Study design

The present study consisted of a systematic review of the literature in order to answer the following research question: “What are the epidemiological and clinical features as well as the prevalence of thelaziosis by T. callipaeda reported in companion animals, wildlife and humans in Europe in the 21st century?” This study was conducted based on the methodological recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [46].

Article eligibility

Articles published in indexed journals cited in PubMed, ScienceDirect and Web of Science were considered eligible if they consisted of case reports or cross-sectional studies describing clinical and epidemiological features (including species, prevalence, gender, age, country, geographical area, affected eye, and ocular signs). There were other restrictions regarding the eligibility criteria. Only studies published between 1 January 2001 and 10 July 2020, and written in the languages of Western Europe (comprising English, French, German, Italian, Portuguese and Spanish) were included.

The types of publications included original articles, short communications and case reports that addressed issues within the following criteria: (i) information on the clinical presentation of thelaziosis by T. callipaeda in companion animals, wild animals and humans; and (ii) prevalence of the disease in canine, feline and red fox populations.

Reviews of the literature, research notes, editorials, experimental essays, textbook chapters, posters, abstracts, articles with no primary data and dissertations along with unpublished studies and data were excluded.

Information sources and search strategies

The process of identifying articles in indexed journals was developed using the PubMed, ScienceDirect and Web of Science databases. The combination of search terms in English applied included: {Europe AND (Thelazia callipaeda OR thelaziosis OR thelaziasis OR thelazi*)}. To prevent missing data, references of retrieved publications were also checked in order to identify additional papers. The searches were conducted between March and July 2020.

Selection of studies and data extraction

After a comprehensive systematic searching, a bibliographic manager tool (Zotero version 5.0.88) [65] was used to exclude duplicate records. Then, two independent reviewers selected articles based on their titles and abstracts, followed by a full reading of the text when the title or abstract met the inclusion criteria or could not be rejected with certainty. Any disagreements or divergences were resolved by discussion and consensus.

Two researchers extracted the required data and added the information on an electronic spreadsheet, dividing them into three groups: (i) companion animals (dog, cat, and domestic rabbit), (ii) wildlife, and (iii) humans. The qualitative data about companion animals comprised references (country, authors and year of publication), case report data (host species, breed, age, gender, lifestyle, and affected eye), number of infected animals, number of adult nematodes and ocular signs (Table 1). With regard to wildlife, information was extracted about the authors, year of publication, country, case report (species, gender and affected eye), number of infected animals, number of adult nematodes and ocular signs (Table 2). For cases of human thelaziosis, references (country, region, data on authors and year of publication), gender, age, affected eye, number of infected hosts, number of adult nematodes and ocular symptoms were collected (Table 3). In turn, the quantitative data extracted from the second group of articles (cross-sectional studies) comprised the references (authors and year of publication), country where the study was conducted, species (dogs, cats and red foxes) and their identification, sample size, number of positive animals, and prevalence (%).

Table 1

Features of the studies included in the qualitative analysis regarding T. callipaeda infection in companion animals in Europe.

Table 2

Features of the studies included in the qualitative analysis regarding T. callipaeda infection in wildlife in Europe.

Table 3

Features of the studies included in the qualitative analysis regarding T. callipaeda infection in humans.

Data analysis

The data collected were analysed using IBM SPSS Statistics 26 statistical software [30]. A Chi-square test was used to test associations between the parameters. Statistical significance was considered if p value was < 0.05.

Results

The identification and study selection are represented in Figure 1. Articles that did not meet the inclusion criteria, as well as duplicates and incomplete articles or studies not available online or in other sources, were excluded. Thus, out of the 363 studies searched, 56 met the eligibility criteria and were divided according to the subject they addressed: epidemiological and clinical characteristics of thelaziosis (n = 44), which were included in the qualitative analysis; studies with relevant data to both qualitative and quantitative analysis (n = 4); or the prevalence of thelaziosis by T. callipaeda in dogs, cats and red foxes (n = 8), which were considered to be cross-sectional (prevalence) studies with data for quantitative analysis.

thumbnail Figure 1

Flow chart of the search, selection and inclusion process for studies in the systematic review based on PRISMA guidelines.

Qualitative analysis of the epidemiological and clinical aspects of T. callipaeda infection in companion animals

The 31 studies included in the qualitative analysis of thelaziosis in companion animals had been conducted in 19 different countries (Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Czech Republic, France, Germany, Greece, Hungary, Moldova, Portugal, Romania, Serbia, Slovakia, Spain, Switzerland, Turkey and the United Kingdom) (Table 1). They reported occurrence of T. callipaeda infection in dogs (n = 1343), cats (n = 20), and a rabbit (n = 1), in a total of 1364 animals (Table 1).

The studies reported the gender of 206 dogs, of which 76 were female (36.9%) and 130 were male (63.1%); 16 cats, of which six were female (37.5%) and 10 were male (62.5%); and the rabbit, which was male.

It was possible to obtain the age of 161 dogs (161/1343, 12.0%), one of which was less than 1 year old (1/161, 0.6%), 113 dogs were 1–8 years old (113/161, 70.2%) and 47 dogs were more than 8 years old (47/161, 29.2%); of the 16 cats whose age was reported (16/20, 80.0%), one cat was more than 8 years old (1/16, 6.3%) and the remaining 15 cats were 1–8 years old (15/16, 93.8%). The rabbit was more than 8 years old.

Of the 58 dogs whose breed was reported, 38 dogs were purebred (38/58; 65.5%) and 20 were crossbred (20/58; 34.5%). The main represented purebred was Labrador Retriever (n = 5; 13.5%), followed by Collie, German Shepherd and Golden Retriever (n = 4 each; 10.5% each), Portuguese Podengo and Transmontano Mastiff (n = 2 each; 5.3% each), Beagle, Borzoi, Dalmatian, Brittany, Greek Hound, Hungarian Vizla, Jack Russel Terrier, Large Münsterländer, Patterdale Terrier, Rottweiler, Samoyed, Scottish Terrier, Sharplanina, Siberian Husky, Spitz, West White Highland Terrier and Wirehaired Slovakian Pointer (n = 1 each; 2.6% each). In cats, the main represented breed was European shorthair (11/15; 73.3%), followed by Greek shorthair (3/15; 20%) and Brown Tabby European (1/15; 6.7%).

It was possible to collect data on body size of 134 dogs (134/1343; 10.0%), most of which fitted in the large category (n = 100; 74.6%), followed by medium (n = 20; 14.9%) and small (n = 14; 10.4%).

The lifestyle of 179 dogs was reported (179/1343, 13.3%), 50 of which lived strictly outdoors (50/179, 27.9%) and 129 lived between inside and outside the house (129/179, 72.1%); regarding the ten cats with information about their lifestyle (10/20, 50.0%), five lived between indoors and outdoors (5/10, 50.0%) and five lived exclusively outdoors (5/10, 50.0%). The domestic rabbit had an exclusively outdoor lifestyle.

In dogs (n = 45; 3.4%), the most affected eye was the right one (n = 19; 42.2%) followed by both eyes (n = 14; 31.1%) and the left eye (n = 12; 26.7%). In turn, the most affected eye in cats was the left one (n = 6; 66.7%) followed by the right eye (n = 3; 33.3%) (Table 1).

The number of specimens of T. callipaeda was counted in 65 dogs (65/1343, 4.8%) and 14 cats (14/20, 70.0%), making a total of 79 animals (79/1363, 5.8%). In both host species, the number of female nematodes (dogs: n = 600; cats: n = 43) was higher than the number of male nematodes (dogs: n = 265; cat: n = 18). The gender of parasitic specimens collected from both domestic species was determined for 89.2% (931/1044).

The 28 articles reporting canine thelaziosis referred to clinical manifestations such as conjunctivitis (n = 21), epiphora (n = 10), purulent discharge (n = 6), blepharospasm (n = 4), conjunctival hyperemia (n = 5), keratitis (n = 3), blepharitis (n = 2), chemosis (n = 2), corneal ulceration (n = 2), follicular conjunctivitis (n = 3), follicular hyperplasia of the 3rd eyelid, (n = 2), ocular discharge (n = 3), anterior uveitis, conjunctival edema, corneal abrasions, increased blink rate, indolent corneal ulcer, lacrimation, mild and proliferative lesions of the inferior conjunctival sac, mucoid discharge, mucoid or mucopurulent discharge, ocular pruritus, periocular alopecia and erosions and serous discharge (n = 1 in each study). The 12 studies reporting feline thelaziosis described ocular signs, including conjunctival oedema (n = 5), conjunctivitis (n = 4), conjunctival hyperaemia (n = 3), blepharospasm (n = 2), epiphora (n = 2), photophobia (n = 2), chemosis, infra-orbital abscess, mucopurulent or purulent or serous discharge, periocular alopecia and erosions and wound on the 3rd eyelid (n = 1 each) (Table 1). The domestic rabbit had conjunctivitis and mucoid ocular discharge (Table 1).

Qualitative analysis of the epidemiological and clinical aspects of T. callipaeda infection in wildlife

The 11 studies included in the qualitative analysis of thelaziosis in wildlife were conducted in five different countries (i.e. Italy, Portugal, Romania, Serbia and Spain) (Table 2). They reported occurrences of thelaziosis by T. callipaeda in beech martens (Martes foina) (n = 5), brown hares (Lepus europaeus) (n = 3), European badger (Meles meles) (n = 1), golden jackal (Canis aureus) (n = 1), red foxes (Vulpes vulpes) (n = 8), wild rabbits (Oryctolagus cuniculus) (n = 2), wildcats (Felis silvestris) (n = 4) and gray wolves (Canis lupus) (n = 14), in a total of 38 animals (Table 2).

The studies reported the gender of all animals, except five red foxes. Out of the five beech martens, three were female (3/5, 60%) and two were male (2/5, 40%); the three brown hares were female, the European badger was female and the golden jackal was male; of the three red foxes whose gender was reported, one was female (1/3, 33.3%) and two were male (2/3, 66.7%); one wild rabbit was female and the other one was male; out of the four wildcats, one was female (1/4; 25%) and three were male (3/4; 75%); out of the 14 wolves, four were female (4/14; 28.6%) and the remaining 10 were male (10/14; 71.4%).

In all host species, with the exception of red foxes, both eyes were the most affected (beech marten: 3/5, 60%; brown hare: 3/3, 100%; European badger: 1/1, 100%; golden jackal: 1/1, 100%; wild rabbit: 2/2, 100%; wildcat: 3/4, 75%; wolf: 11/13, 84.6%), followed by the left eye (beech marten: 1/5, 20%; red fox: 3/6, 50%; wildcat: 1/4, 25%; wolf: 1/13, 7.7%) and the right eye (beech marten: 1/5, 20%; red fox: 1/6, 16.7%; wolf: 1/13, 7.7%). There were no reports on this topic for two red foxes and one wolf (Table 2).

A total of 615 specimens of T. callipaeda were collected from the wildlife mentioned in the studies, and the gender of the nematodes was identified in 610 specimens (610/ 615; 99.2%). The number of female nematodes (beech marten: 10/17, 58.8%; brown hare: 14/17, 82.4%; golden jackal: 21/29, 72.4%; red fox: 35/54, 64.8%; wild rabbit: 5/6, 83.3%; wolf: 313/441, 71.0%) was higher than the number of male nematodes (beech marten: 7/17, 41.2%; brown hare: 3/17, 17.7%; golden jackal: 8/29, 27.6%; red fox: 14/54, 25.9%; wild rabbit: 1/6, 16.7%; wolf: 128/441, 29.0%) in all species, with the exception of wildcats, in which the number of female and male nematodes was equal (9 female and 9 male) and the European badger, in which more males than females were counted (female: 10/33, 30.3%; male: 23/33, 69.7%).

Out of the 11 studies reporting thelaziosis in wildlife, only one study described ocular signs (conjunctivitis) on red foxes (Table 2).

Qualitative analysis of the epidemiological and clinical aspects of T. callipaeda infection in humans

The seven studies included in the qualitative synthesis of T. callipaeda infection in humans reported 11 cases in six different countries: Croatia (n = 1), France (n = 1), Germany (n = 1), Italy (n = 3), Serbia (n = 1) and Spain (n = 4).

Out of the 11 cases, nine were male hosts (81.8%) and two were female hosts (18.2%), with ages between 15 and 35 years (n = 3), 35 and 55 years (n = 4), 55 and 75 years (n = 3) and over 75 years (n = 1).

Out of the nine cases whose affected eyes were reported, four cases occurred in the right eye (4/9, 44.4%), four in the left eye (4/9, 44.4%), and one case in both eyes (1/9, 11.1%).

A total of 17 specimens of T. callipaeda were collected from the human cases mentioned in five out of the seven studies. However, the gender of nematodes was only identified in eight specimens, in which four were female (4/8, 50.0%) and four were male (4/8, 50.0%).

All studies reported ocular signs in the affected humans, including lacrimation (n = 8), foreign body sensation (n = 7), exudative conjunctivitis (n = 5), conjunctival hyperaemia (n = 4), itching (n = 2), ocular pain and discomfort (n = 2), tarsal reaction (n = 2), conjunctival and ciliary infection (n = 1), corneal abscess (n = 1), and redness (n = 2) (Table 3).

Quantitative analysis of the epidemiological and clinical aspects of T. callipaeda infection in dogs, cats and red foxes

Regarding canine thelaziosis, seven studies were carried out in Italy, Portugal, Serbia, Spain and Switzerland (Table 4). Of a total of 659 positive dogs, the gender of 366 animals is known (females: 163, 44.5%; and males: 203, 55.5%).

Table 4

Quantitative analysis regarding the main features of the studies about T. callipaeda infection in dogs, cats and red foxes in Europe.

To date, there are only two cross-sectional studies referring to thelaziosis by T. callipaeda in cats. These studies were conducted in Portugal and Switzerland and their prevalences were 23.5% and 0.8%, respectively (Table 4). They reported the occurrence of T. callipaeda infection in 21 cats (females: 5, 23.8%; males: 16, 76.2%).

Regarding wildlife, five cross-sectional studies have already been carried out in order to determine the prevalence of T. callipaeda infection in red foxes. These studies took place in Bosnia and Herzegovina, Italy, Romania, Slovakia and Switzerland (Table 4). Most red foxes came from legal hunts during rabies-monitoring programmes, so their eye examination occurred post-mortem at necropsy. Two hundred and fifty-three positive red foxes were reported, of which 105 were female (105/252, 41.7%) and 147 were male (147/252, 58.3%) (the gender of one red fox was unknown).

Thelazia-positive dogs from quantitative analysis (cross-sectional studies) indicated a significantly higher occurrence in male dogs (p = 0.0365). The same scenario was observed in cats (p = 0.0164) and red foxes (p = 0.0082).

It was possible to obtain the age of 86 dogs (86/659, 13.1%), having significant differences between young, adult and senior dogs (p < 0.0001), since 16 of which were less than 1 year old (16/86, 18.6%), 55 dogs were 1–8 years old (55/86, 64.0%), and 15 dogs were more than 8 years old (15/86, 17.4%); of the 17 cats whose age was reported, one cat was less than 1 year old (1/17, 5.9%), 14 cats were 1–8 years old (14/17, 82.4%), and two cats were more than 8 years old (2/17, 11.8%).

In dogs, there were statistically significant differences regarding the breed (p = 0.0095), with crossbred dogs (30/43, 69.8%) being more infected than purebred dogs (13/43, 30.2%). The breed of 17 cats was known, all of which were crossbred.

Regarding the body size effect, there were statistically significant differences between positive dogs (p < 0.0001). Small-sized dogs (47/307, 15.3%) have been found to be less infected than medium-sized dogs (122/307, 39.7%), followed by large-sized dogs (138/307, 45.0%).

The lifestyle of 515 dogs was reported, and those that lived strictly outdoors (482/515, 93.6%) were found to be significantly more infected than those that lived inside and outside the house (33/515, 6.4%) (p < 0.0001). Regarding the 17 cats with information about their lifestyle, all of them lived between indoors and outdoors.

Taking into account the information available for the “infected eye”, it was found that in 33 dogs both eyes were infected (33/178, 18.5%), while 145 dogs harboured unilateral infection (145/178, 81.5%). Including the 33 dogs that harboured bilateral infection, the left eye (108/211, 51.2%) was more frequently infected than the right eye (103/211, 48.8%), but without statistical significance (p = 0.7307). The same scenario was observed in cats (left eye: 11/18, 61.1%; right eye: 7/18, 38.9%; p = 0.3458) and in red foxes (left eye: 202/403, 50.1%; right eye: 201/403, 49.9%; p = 0.9603).

The number of female nematodes (dogs: 676/940, 71.9%; cats: 11/17, 64.7%; red foxes: 2428/3534, 68.7%) was higher than the number of male nematodes (dogs: 264/940, 28.1%; cats: 6/17, 35.3%; red foxes: 1106/3534, 31.3%) (Table 5). Dogs and red foxes involved in these cross-sectional studies harboured significantly more female than male nematodes (p < 0.0001), whereas in cats this difference was not statistically significant (p = 0.2253). It is important to note that the gender of all parasitic specimens collected from red foxes was not determined (total: 391/3925, 10.0%).

Table 5

Gender identification and intensity of T. callipaeda infection in the eyes of dogs, cats and red foxes from the cross-sectional studies.

All studies reported a sex ratio in favour of females. Also, the intensity of infection with adult forms of T. callipaeda per study shows high variability, as indicated in Table 5.

Discussion

The occurrence of T. callipaeda infection was significantly higher in male dogs, cats and red foxes from cross-sectional studies, and an equal outcome was observed in the qualitative analysis. In addition, there is no evidence of a host sex predisposition, but there are contradictory results concerning this, as has been shown in previous reports [40, 45, 52]. In relation to cats, it is known that in the samples from the study by Motta et al. [47] all the hosts were male and had outdoor access, which could be risk factors for T. callipaeda infection, possibly due to their territorial and hunting behaviour, but also because of a wider roaming area. Perhaps a similar situation regarding the possible male predisposition in red foxes may be assumed, given that the quantitative analysis has shown that male foxes were significantly more affected than female foxes.

It was observed that the age group corresponding to the adult phase (1–8 years old) was the most affected, having significant differences between the three age groups of dogs. This may be due to the fact that adults potentially had more access to outdoor spaces than juvenile and elderly dogs, a circumstance that predisposed them to contact with P. variegata. This result is in line with that observed in cats [47], as well as in the qualitative analysis of the present study. Nevertheless, some studies have not reported significant differences in infected animals when ages were compared [45, 52].

In relation to the possible breed effect, on the quantitative analysis, there were statistical significant differences regarding the breed, with crossbred dogs being more frequently infected than purebred dogs. Nonetheless, given that the sample consisted of only 43 dogs, it is not possible to confirm that crossbred dogs are more susceptible to infection than purebred dogs. In addition, there is no article that points out in that direction and whose qualitative analysis shows a different perspective. Likewise, in previous reports, no effect of breed was detected [45, 52]. Nevertheless, when it comes to aptitude/management, there seems to be a greater tendency for crossbred or purebred dogs, whose aptitude is shepherd or hunting, being infected by T. callipaeda, since they have a higher possibility for physical contact with the vector while outside in the forest environment [5, 8, 39].

Another feature that appears to play an important role in infection with Thelazia is body size. Small-sized dogs have been found to be less frequently infected than medium-sized dogs, followed by large-sized dogs. This can be explained by the fact that most large-sized dogs are usually housed outdoors, a circumstance that increases their exposure to the intermediate hosts [40, 45, 75]. Additionally, it is accepted that a larger body surface also favours physical contact with P. variegata [40]. In contrast, the lower prevalence in small-sized dogs and in cats may be due to their small body mass index, which apparently makes them less attractive to the intermediate host. Moreover, cats eliminate eye discharges through their intensive cleaning habits, therefore losing their decoy to flies [40, 47, 52]. In addition, feline infection seems to be underestimated because of difficulties experienced by veterinarians inspecting cats’ eyes [15, 47].

As already reported, lifestyle seems to be an important feature in the occurrence of Thelazia infection. In fact, animals that frequently (or exclusively) live outdoors are more highly exposed to P. variegata flies. Similarly, places where there is physical contact between animals, which are potential hosts, seem to attract the intermediate host [39, 45].

In the three species submitted to a quantitative analysis, it was found that the left eye was the most frequently affected. However, these results come from few sources and represent a small sample [6, 25, 28, 31, 40, 47, 57]. Consequently, it is not possible to compare or infer about eye predisposition. Moreover, to the best of our knowledge, there is no scientific article that has identified the existence of a pattern with respect to the most affected eye by T. callipaeda.

Thelaziosis has already been described, based on cases reports and prevalence studies, in several European countries, having as the common denominator the zoophilic fruit fly P. variegata, which is the intermediate host of T. callipaeda. All cases reported have occurred in regions characterised by similar altitude (800–1000 a.s.l) and climate and habitat conditions: continental Mediterranean climate, and cultivated areas and deciduous woods, which fall within the geoclimatic model for the distribution of P. variegata [54].

A higher prevalence of T. callipaeda infection, especially in dogs and red foxes, as described in Spain [41, 45] or Italy [57], suggests a stable endemic condition [42] (Table 4). A lower prevalence of T. callipaeda, such as in Portugal [39] or Slovakia [6], could be associated with the recent emergence of the infection at the local level [42] (Table 4). However, this outcome is expected to be underdiagnosed and/or underreported. The number of companion animals and wildlife (not only red foxes) positive to T. callipaeda might be considerably higher in the mentioned countries, but also in other European countries that have not yet performed prevalence studies. It is important to raise awareness about the need to perform these studies in order to understand the European reality of this zoonosis.

Canine thelaziosis was firstly reported in southern Europe, in Italy, and then in western Europe and the Balkan area. Subsequently, more and more cases appeared in eastern Europe, and it is evident that this zoonosis is already established in Central Europe [5, 10, 29, 34, 35, 38, 51]. The spread of thelaziosis in endemic regions in Europe, but also to previously non-endemic areas, has been linked to the migration of infected wild animals, especially red foxes as well as wolves, jackals and other wildlife. This demonstrates the role of free-ranging wild carnivores as reservoirs of T. callipaeda and highlights the importance of the sylvatic cycle, especially in rural areas, where transmission to humans and domestic animals is facilitated [6, 28, 34, 44, 57]. However, the role of pets, especially dogs, in spreading the disease, should not be neglected [35, 36]. The movement of pets when traveling with their owners within the European Union, but also the adoption and import of dogs from shelters from endemic regions are a crucial driver of Thelazia, but also for other pathogenic agents and their vectors [16, 34]. Undoubtedly, these risk factors highlight the importance of preventive programmes [35, 36] and surveillance polices to restrict cross-border spread of the nematode [34, 75].

Conclusions

In this work, isolated cases of thelaziosis were summarized and an in-depth analysis of all cross-sectional studies was conducted. The reduced number of prevalence studies and the small sample per study were the main disadvantages found, as this made it difficult or even impossible to infer or determine the situation for certain features. However, this work shows the expansion potential of T. callipaeda and the urgent need for additional large-scale studies in order to provide information on the current situation in the European Union. Given the scarcity of papers on human health, the need to stress the importance of the One Health approach is sustained. Only through updated epidemiological data, knowledge improvement, and awareness can correct diagnosis and appropriate treatment and prevention of thelaziosis be ensured.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Author contributions

Beatriz do Vale: conceptualisation; investigation; methodology; writing – original draft; writing – review & editing. Ana Patrícia Lopes: writing – review & editing. Maria da Conceição Fontes: writing – review & editing. Mário Silvestre: writing – review & editing. Luís Cardoso: supervision, writing – review & editing. Ana Cláudia Coelho: supervision; writing – review & editing.

Acknowledgments

This research was supported by the project UIDB/CVT/00772/2020 funded by the Fundação para a Ciência e Tecnologia (FCT, Portugal).

References

  1. Anderson RC. 2000. Nematode parasites of vertebrates: their development and transmission, 2nd edn. Guilford, UK: CABI Publishing. p. 672. [Google Scholar]
  2. Beugnet F, Halos L, Guillot J. 2018. Internal non-gastrointestinal parasitoses – thelaziosis, in Textbook of clinical parasitology in dogs and cats, 2nd edn. Zaragoza, Spain: Servet. p. 200–202. [Google Scholar]
  3. Bradbury RS, Breen KV, Bonura EM, Hoyt JW, Bishop HS. 2018. Case report: conjunctival infestation with Thelazia gulosa: a novel agent of human thelaziasis in the United States. American Journal of Tropical Medicine and Hygiene, 98, 1171–1174. [CrossRef] [Google Scholar]
  4. Burnett HS, Parmelee WE, Lee RD, Wagner ED. 1957. Observations on the life cycle of Thelazia californiensis Price, 1930. Journal of Parasitology, 43, 433. [CrossRef] [Google Scholar]
  5. Čabanová V, Kocák P, Víchová B, Miterpáková M. 2017. First autochthonous cases of canine thelaziosis in Slovakia: a new affected area in Central Europe. Parasites & Vectors, 10, 179. [CrossRef] [PubMed] [Google Scholar]
  6. Čabanová V, Miterpáková M, Oravec M, Hurníková Z, Jerg S, Nemčíková G, Červenská MB. 2018. Nematode Thelazia callipaeda is spreading across Europe. The first survey of red foxes from Slovakia. Acta Parasitologica, 63, 160–166. [CrossRef] [PubMed] [Google Scholar]
  7. Calero-Bernal R, Otranto D, Pérez-Martín JE, Serrano FJ, Reina D. 2013. First report of Thelazia callipaeda in wildlife from Spain. Journal of Wildlife Diseases, 49, 458–460. [CrossRef] [PubMed] [Google Scholar]
  8. Calero-Bernal R, Sánchez-Murillo JM, Alarcón-Elbal PM, Sánchez-Moro J, Latrofa MS, Dantas-Torres F, Otranto D. 2014. Resolution of canine ocular thelaziosis in avermectin-sensitive Border Collies from Spain. Veterinary Parasitology, 200, 203–206. [CrossRef] [PubMed] [Google Scholar]
  9. Caron Y, Premont J, Losson B, Grauwels M. 2013. Thelazia callipaeda ocular infection in two dogs in Belgium. Journal of Small Animal Practice, 54, 205–208. [CrossRef] [Google Scholar]
  10. Colella V, Kirkova Z, Fok É, Mihalca AD, Tasić-Otašević S, Hodžić A, Dantas-Torres F, Otranto D. 2016. Infections in Eastern Europe. Emerging Infectious Diseases, 22, 3. [Google Scholar]
  11. Deltell JG, Calderón SR, Vidal MIP, Iglesias MF. 2019. A propósito de dos casos de thelaziosis ocular humana. Revista Española de Quimioterapia, 32, 286–287. [Google Scholar]
  12. Diakou A, Di Cesare A, Tzimoulia S, Tzimoulias I, Traversa D. 2015. Thelazia callipaeda (Spirurida: Thelaziidae): first report in Greece and a case of canine infection. Parasitology Research, 114, 2771–2775. [CrossRef] [PubMed] [Google Scholar]
  13. Dolff S, Kehrmann J, Eisermann P, Dalbah S, Tappe D, Rating P. 2020. Case report: Thelazia callipaeda eye infection: the first human case in Germany. American Journal of Tropical Medicine and Hygiene, 102, 350–351. [CrossRef] [Google Scholar]
  14. Dorchies Ph, Chaudieu G, Siméon LA, Cazalot G, Cantacessi C, Otranto D. 2007. First reports of autochthonous eyeworm infection by Thelazia callipaeda (Spirurida, Thelaziidae) in dogs and cat from France. Veterinary Parasitology, 149, 294–297. [CrossRef] [PubMed] [Google Scholar]
  15. Dumitrache MO, Györke A, Mircean M, Benea M, Mircean V. 2018. Ocular thelaziosis due Thelazia callipaeda (Spirurida: Thelaziidae) in Romania: first report in domestic cat and new geographical records of canine cases. Parasitology Research, 117, 4037–4042. [CrossRef] [PubMed] [Google Scholar]
  16. Dumitrache MO, Ionică AM, Voinițchi E, Chavdar N, D’Amico G. 2019. First report of canine ocular thelaziosis in the Republic of Moldova. Parasites & Vectors, 12, 505. [CrossRef] [PubMed] [Google Scholar]
  17. Eser M, Miman Ö, Acar A. 2018. Thelazia callipaeda (Railliet and Henry, 1910) case in a dog: first record in Turkey. Kafkas Universitesi Veteriner Fakultesi Dergisi, 25, 131–134. [Google Scholar]
  18. Farkas R, Takács N, Gyurkovszky M, Henszelmann N, Kisgergely J, Balka G, Solymosi N, Vass A. 2018. The first feline and new canine cases of Thelazia callipaeda (Spirurida: Thelaziidae) infection in Hungary. Parasites & Vectors, 11, 338. [CrossRef] [PubMed] [Google Scholar]
  19. Faust EC. 1928. Studies on Thelazia callipaeda Railliet and Henry, 1910. Journal of Parasitology, 15, 75. [CrossRef] [Google Scholar]
  20. Fuentes I, Montes I, Saugar JM, Latrofa S, Gárate T, Otranto D. 2012. Thelaziosis in humans, a zoonotic infection, Spain, 2011. Emerging Infectious Diseases, 18, 2073–2075. [CrossRef] [PubMed] [Google Scholar]
  21. Gajić B, Bogunović D, Stevanović J, Kulišić Z, Simeunović P, Stanimirović Z. 2014. Canine and feline thelaziosis caused by Thelazia callipaeda in Serbia. Acta Veterinaria, 64, 447–455. [Google Scholar]
  22. Gajić B, Bugarski-Stanojević V, Penezić A, Kuručki M, Bogdanović N, Ćirović D. 2019. First report of eyeworm infection by Thelazia callipaeda in gray wolf (Canis lupus) from Serbia. Parasitology Research, 118, 3549–3553. [CrossRef] [PubMed] [Google Scholar]
  23. Gama A, Pires I, Canado M, Coutinho T, Lopes AP, Latrofa MS, Cardoso L, Dantas-Torres F, Otranto D. 2016. First report of Thelazia callipaeda infection in wild European rabbits (Oryctolagus cuniculus) in Portugal. Parasites & Vectors, 9, 236. [CrossRef] [PubMed] [Google Scholar]
  24. Graham-Brown J, Gilmore P, Colella V, Moss L, Dixon C, Andrews M, Arbeid P, Barber J, Timofte D, McGarry J, Otranto D, Williams D. 2017. Three cases of imported eyeworm infection in dogs: a new threat for the United Kingdom. Veterinary Record, 181, 346–346. [CrossRef] [Google Scholar]
  25. Hadži-Milić M, Ilić T, Stepanović P, Đorđević J, Dimitrijević S. 2016. Serbia: another endemic region for canine ocular thelaziosis. Medycyna Weterynaryjna, 72, 558–563. [Google Scholar]
  26. Hammond A. 2018. Thelazia callipaeda in a travelled dog in England. Veterinary Record, 183, 477. [Google Scholar]
  27. Hermosilla C, Bauer C, Herrmann B. 2004. First case of Thelazia callipaeda infection in a dog in Germany. Veterinary Record, 154, 568–569. [CrossRef] [Google Scholar]
  28. Hodžić A, Latrofa M, Annoscia G, Alić A, Beck R, Lia R, Dantas-Torres F, Otranto D. 2014. The spread of zoonotic Thelazia callipaeda in the Balkan area. Parasites & Vectors, 7, 352. [CrossRef] [PubMed] [Google Scholar]
  29. Hodžić A, Payer A, Duscher G. 2019. The first autochthonous case of feline ocular thelaziosis in Austria. Parasitology Research, 118, 1321–1324. [CrossRef] [PubMed] [Google Scholar]
  30. IBM Corp. 2019. IBM SPSS Statistics for Windows version 26.0. New York, USA: Armonk. [Google Scholar]
  31. Ionică AM, Deak G, Matei IA, D’Amico G, Cotuţiu VD, Gherman CM, Mihalca AD. 2018. Thelazia callipaeda, an endemic parasite of red foxes (Vulpes vulpes) in Western Romania. Journal of Wildlife Diseases, 54, 829–833. [CrossRef] [PubMed] [Google Scholar]
  32. Ionică AM, Deak G, D’Amico G, Stan GF, Chișamera GB, Constantinescu IC, Adam C, Lefkaditis M, Gherman CM, Mihalca AD. 2019. Thelazia callipaeda in mustelids from Romania with the European badger, Meles meles, as a new host for this parasite. Parasites & Vectors, 12, 370. [CrossRef] [PubMed] [Google Scholar]
  33. Ioniţă M, Mitrea IL, Ionică AM, Morariu S, Mihalca AD. 2016. New cases of Thelazia callipaeda haplotype 1 in dogs suggest a wider distribution in Romania. Vector-Borne and Zoonotic Diseases, 16, 172–175. [CrossRef] [Google Scholar]
  34. Jirků M, Kuchta R, Gricaj E, Modry D, Pomajbikova KJ. 2020. Canine thelaziosis in the Czech Republic: the northernmost autochthonous occurrence of the eye nematode Thelazia callipaeda Railliet et Henry, 1910 in Europe. Folia Parasitologica, 67, 10. [Google Scholar]
  35. Lebon W, Guillot J, Álvarez M-J, Antonio Bazaga J, Cortes-Dubly M-L, Dumont P, Eberhardt M, Gómez H, Pennant O, Siméon N, Beugnet F, Halos L. 2019. Prevention of canine ocular thelaziosis (Thelazia callipaeda) with a combination of milbemycin oxime and afoxolaner (Nexgard Spectra®) in endemic areas in France and Spain. Parasite, 26, 1. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  36. Lechat C, Siméon N, Pennant O, Desquilbet L, Chahory S, Lesueur C, Guillot J. 2015. Comparative evaluation of the prophylactic activity of a slow-release insecticide collar and a moxidectin spot-on formulation against Thelazia callipaeda infection in naturally exposed dogs in France. Parasites & Vectors, 8, 93. [CrossRef] [PubMed] [Google Scholar]
  37. López-Medrano R, Guerra Calleja G, Díez Morrondo C, Panadero Fontán R. 2015. Ocular thelaziosis, an emergent zoonosis in Spain. Medicina Clínica (English Edition), 145, 317–318. [CrossRef] [Google Scholar]
  38. Magnis J, Naucke TJ, Mathis A, Deplazes P, Schnyder M. 2010. Local transmission of the eye worm Thelazia callipaeda in southern Germany. Parasitology Research, 106, 715–717. [CrossRef] [PubMed] [Google Scholar]
  39. Maia C, Catarino AL, Almeida B, Ramos C, Campino L, Cardoso L. 2016. Emergence of Thelazia callipaeda infection in dogs and cats from East-Central Portugal. Transboundary and Emerging Diseases, 63, 416–421. [CrossRef] [PubMed] [Google Scholar]
  40. Malacrida F, Hegglin D, Bacciarini L, Otranto D, Nägeli F, Nägeli C, Bernasconi C, Scheu U, Balli A, Marenco M, Togni L, Deplazes P, Schnyder M. 2008. Emergence of canine ocular thelaziosis caused by Thelazia callipaeda in southern Switzerland. Veterinary Parasitology, 157, 321–327. [CrossRef] [PubMed] [Google Scholar]
  41. Marino V, Gálvez R, Colella V, Sarquis J, Checa R, Montoya A, Barrera JP, Domínguez S, Lia RP, Otranto D, Miró G. 2018. Detection of Thelazia callipaeda in Phortica variegata and spread of canine thelaziosis to new areas in Spain. Parasites & Vectors, 11, 195. [CrossRef] [PubMed] [Google Scholar]
  42. Marino V, Gálvez R, Montoya A, Mascuñán C, Hernández M, Barrera JP, Domínguez I, Zenker C, Checa R, Sarquis J, Miró G. 2020. Spain as a dispersion model for Thelazia callipaeda eyeworm in dogs in Europe. Preventive Veterinary Medicine, 175, 104883. [CrossRef] [PubMed] [Google Scholar]
  43. Mihalca AD, D’Amico G, Scurtu I, Chirilă R, Matei I, Ionică A. 2015. Further spreading of canine oriental eyeworm in Europe: first report of Thelazia callipaeda in Romania. Parasites & Vectors, 8, 48. [CrossRef] [PubMed] [Google Scholar]
  44. Mihalca AD, Ionică AM, D’Amico G, Daskalaki AA, Deak G, Matei IA, Șimonca V, Iordache D, Modrý D, Gherman CM. 2016. Thelazia callipaeda in wild carnivores from Romania: new host and geographical records. Parasites & Vectors, 9, 350. [CrossRef] [PubMed] [Google Scholar]
  45. Miró G, Montoya A, Hernández L, Dado D, Vázquez MV, Benito M, Villagrasa M, Brianti E, Otranto D. 2011. Thelazia callipaeda: infection in dogs: a new parasite for Spain. Parasites & Vectors, 4, 148. [CrossRef] [PubMed] [Google Scholar]
  46. Moher D, Liberati A, Tetzlaff J, Altman DG. 2009. The PRISMA Group preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine, 6, e1000097. [CrossRef] [PubMed] [Google Scholar]
  47. Motta B, Nägeli F, Nägeli C, Solari-Basano F, Schiessl B, Deplazes P, Schnyder M. 2014. Epidemiology of the eye worm Thelazia callipaeda in cats from southern Switzerland. Veterinary Parasitology, 203, 287–293. [CrossRef] [PubMed] [Google Scholar]
  48. Nájera F, Lucas-Veguillas J, Vela Á, López-Fernández M, Martínez-Martínez P, Mata-Huete M, Cáceres-Urones J, Annoscia G, Otranto D, Calero-Bernal R. 2020. First report of Thelazia callipaeda in a free-ranging Iberian wolf (Canis lupus signatus) from Spain. Parasitology Research, 119, 2347–2350. [CrossRef] [PubMed] [Google Scholar]
  49. Otranto D, Traversa D. 2005. Thelazia eyeworm: an original endo- and ecto-parasitic nematode. Trends in Parasitology, 21, 1–4. [CrossRef] [PubMed] [Google Scholar]
  50. Otranto D, Dutto M. 2008. Human thelaziasis, Europe. Emerging Infectious Diseases, 14, 647–649. [CrossRef] [PubMed] [Google Scholar]
  51. Otranto D, Dantas-Torres F. 2015. Transmission of the eyeworm Thelazia callipaeda: between fantasy and reality. Parasites & Vectors, 8, 273. [CrossRef] [PubMed] [Google Scholar]
  52. Otranto D, Ferroglio E, Lia RP, Traversa D, Rossi L. 2003. Current status and epidemiological observation of Thelazia callipaeda (Spirurida, Thelaziidae) in dogs, cats and foxes in Italy: a “coincidence” or a parasitic disease of the Old Continent? Veterinary Parasitology, 116, 315–325. [CrossRef] [PubMed] [Google Scholar]
  53. Otranto D, Lia RP, Cantacessi C, Testini G, Troccoli A, Shen JL, Wang ZX. 2005. Nematode biology and larval development of Thelazia callipaeda (Spirurida, Thelaziidae) in the drosophilid intermediate host in Europe and China. Parasitology, 131, 847. [CrossRef] [PubMed] [Google Scholar]
  54. Otranto D, Brianti E, Cantacessi C, Lia RP, Máca J. 2006. The zoophilic fruitfly Phortica variegata: morphology, ecology and biological niche. Medical and Veterinary Entomology, 20, 358–364. [CrossRef] [PubMed] [Google Scholar]
  55. Otranto D, Cantacessi C, Testini G, Lia RP. 2006. Phortica variegata as an intermediate host of Thelazia callipaeda under natural conditions: evidence for pathogen transmission by a male arthropod vector. International Journal for Parasitology, 36, 1167–1173. [CrossRef] [PubMed] [Google Scholar]
  56. Otranto D, Cantacessi C, Mallia E, Lia RP. 2007. First report of Thelazia callipaeda (Spirurida, Thelaziidae) in wolves in Italy. Journal of Wildlife Diseases, 43, 508–511. [CrossRef] [PubMed] [Google Scholar]
  57. Otranto D, Dantas-Torres F, Mallia E, DiGeronimo PM, Brianti E, Testini G, Traversa D, Lia RP. 2009. Thelazia callipaeda (Spirurida, Thelaziidae) in wild animals: report of new host species and ecological implications. Veterinary Parasitology, 166, 262–267. [CrossRef] [PubMed] [Google Scholar]
  58. Otranto D, Cantacessi C, Lia RP, Kadow ICG, Purayil SK, Dantas-Torres F, Máca J. 2012. First laboratory culture of Phortica variegata (Diptera, Steganinae), a vector of Thelazia callipaeda. Journal of Vector Ecology, 37, 458–461. [CrossRef] [Google Scholar]
  59. Otranto D, Mendoza-Roldan JA, Dantas-Torres F. 2020. Thelazia callipaeda. Trends in Parasitology, S1471-4922(20)30127-6. [Google Scholar]
  60. Papadopoulos E, Komnenou A, Thomas A, Ioannidou E, Colella V, Otranto D. 2018. Spreading of Thelazia callipaeda in Greece. Transboundary and Emerging Diseases, 65, 248–252. [Google Scholar]
  61. Paradžik MT, Samardžić K, Živičnjak T, Martinković F, Janjetović Ž, Miletić-Medved M. 2016. Thelazia callipaeda – first human case of thelaziosis in Croatia. Wiener Klinische Wochenschrift, 128, 221–223. [CrossRef] [PubMed] [Google Scholar]
  62. Pavlović I, Jakić-Dimić D, Kureljušić B, Ćirović D, Jezdimirović N, Drobnjak M. 2017. First occurence of Thelazia callipaeda in foxes (Vulpes vulpes L.) in Serbia. Balkan Journal of Wildlife Research, 4, 1–5. [Google Scholar]
  63. Pimenta P, Cardoso L, Pereira MJ, Maltez L, Coutinho T, Alves MS, Otranto D. 2013. Canine ocular thelaziosis caused by Thelazia callipaeda in Portugal. Veterinary Ophthalmology, 16, 312–315. [CrossRef] [PubMed] [Google Scholar]
  64. Rodrigues FT, Cardoso L, Coutinho T, Otranto D, Diz-Lopes D. 2012. Ocular thelaziosis due to Thelazia callipaeda in a cat from northeastern Portugal. Journal of Feline Medicine and Surgery, 14, 952–954. [CrossRef] [PubMed] [Google Scholar]
  65. Roy Rosenzweig Center for History and New Media. 2020. Zotero version 5.0.88. Fairfax, Virginia, USA: George Mason University. [Google Scholar]
  66. Ruytoor P, Déan E, Pennant O, Dorchies P, Chermette R, Otranto D, Guillot J. 2010. Ocular thelaziosis in dogs, France. Emerging Infectious Diseases, 16, 1943–1945. [CrossRef] [PubMed] [Google Scholar]
  67. Sargo R, Loureiro F, Catarino AL, Valente J, Silva F, Cardoso L, Otranto D, Maia C. 2014. First report of Thelazia callipaeda in red foxes (Vulpes vulpes) from Portugal. Journal of Zoo and Wildlife Medicine, 45, 458–460. [CrossRef] [Google Scholar]
  68. Schottstedt T. 2009. Okuläre thelaziose bei einem Hund. Kleintierpraxis, 54, 160–163. [Google Scholar]
  69. Seixas F, Travassos P, Coutinho T, Lopes AP, Latrofa MS, Pires M dos A, Cardoso LOtranto D. 2018. The eyeworm Thelazia callipaeda in Portugal: current status of infection in pets and wild mammals and case report in a beech marten (Martes foina). Veterinary Parasitology, 252, 163–166. [CrossRef] [PubMed] [Google Scholar]
  70. Shen J, Gasser RB, Chu D, Wang Z, Yuan X, Cantacessi C, Otranto D. 2006. Human thelaziosis – a neglected parasitic disease of the eye. Journal of Parasitology, 92, 872–876. [CrossRef] [Google Scholar]
  71. Silva LMR, Spoerel S, Wiesner L, Klein M, Pantchev N, Taubert A, Hermosilla C. 2020. Ophthalmic Thelazia callipaeda infections: first feline and new canine imported cases in Germany. Parasitology Research, 119, 3099–3104. [CrossRef] [PubMed] [Google Scholar]
  72. Soares C, Sousa SR, Anastácio S, Matias MG, Marquês I, Mascarenhas S, Vieira MJ, de Carvalho LM, Otranto D. 2013. Feline thelaziosis caused by Thelazia callipaeda in Portugal. Veterinary Parasitology, 196, 528–531. [CrossRef] [PubMed] [Google Scholar]
  73. Tasić-Otašević S, Gabrielli S, Trenkić-Božinović M, Petrović A, Gajić B, Colella V, Momčilović S, Cancrini G, Otranto D. 2016. Eyeworm infections in dogs and in a human patient in Serbia: a One Health approach is needed. Comparative Immunology, Microbiology and Infectious Diseases, 45, 20–22. [CrossRef] [PubMed] [Google Scholar]
  74. Tudor P, Bădicu A, Mateescu R, Tudor N, Mateescu C, Ionaşcu I. 2016. First report of canine ocular thelaziosis in the Muntenia Region, Romania. Parasitology Research, 115, 1741–1744. [CrossRef] [PubMed] [Google Scholar]
  75. Vale B do, Lopes AP, da Conceição Fontes M, Silvestre M, Cardoso L, Coelho AC. 2019. Thelaziosis due to Thelazia callipaeda in Europe in the 21st century – a review. Veterinary Parasitology, 275, 108957. [CrossRef] [PubMed] [Google Scholar]
  76. Vieira L, Rodrigues FT, Costa Á, Diz-Lopes D, Machado J, Coutinho T, Tuna J, Latrofa M, Cardoso L, Otranto D. 2012. First report of canine ocular thelaziosis by Thelazia callipaeda in Portugal. Parasites & Vectors, 5, 124. [CrossRef] [PubMed] [Google Scholar]

Cite this article as: do Vale B, Lopes AP, da Conceição Fontes M, Silvestre M, Cardoso L & Coelho AC. 2020. Systematic review on infection and disease caused by Thelazia callipaeda in Europe: 2001–2020. Parasite 27, 52.

All Tables

Table 1

Features of the studies included in the qualitative analysis regarding T. callipaeda infection in companion animals in Europe.

Table 2

Features of the studies included in the qualitative analysis regarding T. callipaeda infection in wildlife in Europe.

Table 3

Features of the studies included in the qualitative analysis regarding T. callipaeda infection in humans.

Table 4

Quantitative analysis regarding the main features of the studies about T. callipaeda infection in dogs, cats and red foxes in Europe.

Table 5

Gender identification and intensity of T. callipaeda infection in the eyes of dogs, cats and red foxes from the cross-sectional studies.

All Figures

thumbnail Figure 1

Flow chart of the search, selection and inclusion process for studies in the systematic review based on PRISMA guidelines.

In the text

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.