Eyeworm infections in dogs and in a human patient in Serbia: A One Health approach is needed
Introduction
Nematodes of the genus Thelazia (Spirurida, Thelaziidae) inhabit the orbital cavity and associated tissues of several species of warm-blooded animals, for a long time commonly being referred to as eyeworms [1]. In particular, Thelazia callipaeda parasitizes the eyes of domestic and wild carnivores, lagomorphs and humans [2] and is vectored in Europe by Phortica variegata, a drosophilid displaying zoophilic behaviour [3]. Male flies of P. variegata come into contact with first-stage larvae whilst feeding on animal ocular secretions and, in 2–3 weeks, third-stage larvae are released into the eye of a new host through a subsequent meal [3]. Clinical manifestations of thelaziosis are ascribed to be due to mechanical damage of the conjuctival and corneal epithelia associated to the number of parasites and the lateral serrations of the nematode cuticle [4]. Humans may display a range of clinical signs and lesions (e.g. conjunctivitis, lachrymation, corneal ulcers), also dependent on the parasite load, including severe problems such as corneal perforation and blindness [5]. Human case reports are mainly from China and the Far East, in children and elderly people living in or visiting rural communities of low socio-economic standards, and those in close contact with infected animals [4]. In Europe human thelaziosis occurs occasionally in areas where the infection is prevalent in dogs and in other wild canids [5], [6].
This parasite was originally identified in Far Eastern Countries (e.g. China, Japan and Thailand) and, therefore, for long time was known as the “oriental eyeworm”. However, T. callipaeda was subsequently identified in dogs, cats and foxes in Italy [7], [8] and, later on, in many other European countries [9]. Indeed, since the early 90s when canine thelaziosis was first reported in Italy as an occasional finding, studies on the aetiology, ecology and biology of the vector of this spirurid allowed the identification of large areas of Europe as suitable for the occurrence of the infection [10]. Later on, the presence of the infection in France, Germany, Switzerland, Spain and Portugal confirmed the accuracy of that predictive model and indicated that canine thelaziosis was spreading in animal populations throughout Europe [9].
Only recently T. callipaeda has been detected in the Balkans, parasitizing 27.71% of the 184 red foxes examined [11]. The high prevalence of the infection in red foxes indicates the status of hyperendemicity of eyeworm infection in these regions [11]. Nonetheless, although >1000 cases of human thelaziosis have been reported in Asia, only 8 human cases have been documented in Europe (i.e., Italy, France and Spain) [12]. Based on data available on the prevalence of thelaziosis in red foxes from Croatia and Bosnia Herzegovina [11], infection in dogs and humans is most likely unreported in the Balkans.
In this study, we describe the first human case of ocular thelaziosis, along with two cases in dogs living in the same region of Serbia and discuss the findings from a One Health perspective.
Section snippets
Materials and methods
A 36-year-old man, living in a small village near Medveđa in the Southern part of Serbia, required medical assistance because of redness, itching and ocular discomfort in his left eye, lasting for 25 days. The patient reported that while picking mushrooms in the vicinity of his home, he noticed the presence of swarming insects. Due to the ocular discomfort and continual rubbing of the eye, the patient removed a very motile parasite from his eye and delivered the specimen to the ophthalmologist.
Results
Clinical examination of the human patient revealed conjunctivitis, whilst standard laboratory haematological and biochemical tests were within normal ranges. Any other parasite was found in the eye of the patient. After repeated examinations, visual acuity, intraocular pressure and fundus examination displayed standard results. Although poorly preserved, the worm was 9.2 mm in length, 330 μm in width with a cylindrical, serrated cuticle and whitish in colour. Based on morphological, anamnestic
Discussion
The first case of human thelaziosis herein reported in Serbia and the Balkans indicates that the infection is endemic in that area. This is further supported by the detection of two infected animals in the same region where the parasite was previously found in dogs and cats [15]. Furthermore, T. callipaeda infection, recently detected in the Balkans (i.e., Bosnia and Herzegovina and Croatia) in foxes, cats and dogs [11], suggests that the infection has most likely recently expanded in animal
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Update on the treatment and prevention of ocular thelaziosis (Thelazia callipaeda) in naturally infected dogs from Spain
2021, International Journal for ParasitologyCitation Excerpt :This term is no longer appropriate because cases of T. callipaeda infection have been described in dogs and/or cats in many European countries including Italy, France, Germany, Switzerland, Spain, Portugal, Belgium, Bosnia and Herzegovina, Croatia, Serbia, Romania, Greece, Bulgaria, Hungary, Slovakia, United Kingdom, Turkey, Austria, Czech Republic, Republic of Moldova, and Andorra (Colella et al., 2016; do Vale et al., 2019; Dumitrache et al., 2019; Hofmannová et al., 2019; Marino et al., 2020). In humans, thelaziosis has been reported in Italy and France (Otranto and Dutto, 2008), Spain (Fuentes et al., 2012; López Medranoet al., 2015; Deltell et al., 2019) and, more recently, in Croatia, Serbia and Germany (Paradžik et al., 2016; Tasić-Otašević et al., 2016; Dolff et al., 2020), and has accordingly been described as a public health concern (Otranto and Dutto, 2008). The therapeutic and prophylactic efficacy of different drugs against canine thelaziosis has been a topic of recent investigation.
Spain as a dispersion model for Thelazia callipaeda eyeworm in dogs in Europe
2020, Preventive Veterinary MedicineCitation Excerpt :To date, ocular thelaziosis has been detected in red foxes (Vulpes vulpes), gray wolves (Canis lupus), beech martens (Martes foina), brown hares (Lepus europaeus), wild cats (Felis silvestris) (Otranto et al., 2009), wild European rabbits (Oryctolagus cuniculus) (Gama et al., 2016; Papadopoulos et al., 2017) and golden jackals (Canis aureus) (Mihalca et al., 2016). Human cases of thelaziosis have been mainly documented in people living in East Asian countries (e.g., Japan, Korea, China, India) (reviewed by Colwell et al., 2011) though reports of human eye infection have also emerged from Italy, France (Otranto and Dutto, 2008), Spain (Fuentes et al., 2012; Gomez-Couso et al., 2013; López Medrano et al., 2015), Serbia (Tasić-Otašević et al., 2016) and Croatia (Paradžik et al., 2016). Today, the spread and increasing reports of the eyeworm especially in animals but also in humans, means it is classed as an emergent vector-borne pathogen in Europe (Otranto et al., 2013).
Thelaziosis due to Thelazia callipaeda in Europe in the 21st century—A review
2019, Veterinary ParasitologyCitation Excerpt :Thelazia callipaeda is also known as “the oriental eyeworm” because of its distribution through the former Soviet Union, other countries of Asia, including China, India, Indonesia, Japan, South Korea and Thailand (Anderson, 2000; Shen et al., 2006; Otranto and Dutto, 2008; Colwell et al., 2011; Sharma et al., 2019), and also Bangladesh (Hossain et al., 2011; Akhanda et al., 2013), Nepal (Sah et al., 2018) and Vietnam (De et al., 2012). Nevertheless, recent decades have witnessed its increasing presence in some European countries both in animals and humans (Motta et al., 2014), such as in Italy (Lia et al., 2000; Otranto et al., 2003, 2007, 2009; Otranto and Dutto, 2008), France (Chermette et al., 2004; Dorchies et al., 2007; Otranto and Dutto, 2008; Ruytoor et al., 2010), Germany (Hermosilla et al., 2004; Magnis et al., 2010), Switzerland (Malacrida et al., 2008; Motta et al., 2014), Spain (Miró et al., 2011; Fuentes et al., 2012; Calero-Bernal et al., 2013; López Medrano et al., 2015; Marino et al., 2018; Deltell et al., 2019), Portugal (Rodrigues et al., 2012; Vieira et al., 2012; Pimenta et al., 2013; Soares et al., 2013; Sargo et al., 2014; Gama et al., 2016; Maia et al., 2016; Seixas et al., 2018), Belgium (Caron et al., 2013), Bosnia and Herzegovina (Hodžić et al., 2014), Croatia (Hodžić et al., 2014; Paradžik et al., 2016), Serbia (Gajić et al., 2014; Tasić-Otašević et al., 2016; Pavlović et al., 2017), Romania (Mihalca et al., 2015; Ioniţă et al., 2016; Mihalca et al., 2016; Tudor et al., 2016; Dumitrache et al., 2018; Ionică et al., 2018, 2019), Greece (Diakou et al., 2015; Papadopoulos et al., 2018), Bulgaria (Colella et al., 2016), Hungary (Colella et al., 2016; Farkas et al., 2018), Slovakia (Čabanová et al., 2017, 2018), the United Kingdom (UK) (Graham-Brown et al., 2017; Hammond, 2018), Turkey (Eser et al., 2018) and Austria (Hodžić et al., 2019) (Fig. 1). The present article reviews the eyeworm itself and reported European ocular thelaziosis cases, underlining the importance of prevention based on the One Health paradigm.
Zoonotic nematodes of wild carnivores
2019, International Journal for Parasitology: Parasites and WildlifeQuestionnaire-based survey on distribution of canine ocular thelaziosis in southwestern France
2018, Veterinary ParasitologyCitation Excerpt :During the last decade, the knowledge about the distribution of T. callipaeda in Europe has been greatly improved. To date, ocular thelaziosis is widespread among dogs (and to a lesser extent among cats) from northern (Aosta valley) to southern (Calabria region) Italy (Rossi and Bertaglia, 1989; Lia et al., 2000; Otranto et al., 2003), southern Switzerland (Ticino) (Malacrida et al., 2008), southwestern France (Dordogne) (Dorchies et al., 2007), central western Spain (Miró et al., 2011), central and northern Portugal (Vieira et al., 2012; Pimenta et al., 2013), Bosnia and Herzegovina (Hodžić et al., 2014), Serbia (Tasić-Otašević et al., 2016), Romania (Ionita et al., 2016) and Hungary (Colella et al., 2016). Very recently, autochthonous cases of thelaziosis have been reported in dogs, cats and in one rabbit from northern and central parts of Greece (Papadopoulos et al., 2017) and in four dogs from Slovakia (Cabanova et al., 2017).