Linguatula Serrata (pentastomida Linguatulidae) Infection In Dog

Linguatula serrata (Pentastomida: Linguatulidae) infection in dog, : a case report

Mariana ioniȚă, Ioan Liviu MITREA

1 University of Agronomic Sciences and Veterinary Medicine of Bucharest, Faculty of Veterinary Medicine, Department of Parasitology and Parasitic Diseases & Animal Biology, 105 Spl. Independentei, 050097, Bucharest, Romania

Corresponding author email: [anonimizat]

Abstract

Linguatula serrata (Pentastomida: order Porocephalida, family Linguatulidae),a cosmopolitan parasite, inhabits as adults the nasal passages and frontal sinuses of wild and domestic canids (dogs, foxes), which serve as definitive hosts. Cattle, sheep, goats, camels, rabbits, and other animals serve as intermediate hosts, in which fully developed nymphs, the parasitic stage infective for carnivores, are found encysted mainly in the mesenteric lymph nodes, lungs, liver, or serous membranes). Although man is accidental/aberrant host, the reports of human infection with this parasite, as visceral or nasopharyngeal (“Halzoun” or “Marrara syndrome”) linguatulosis is not uncommon, particularly in the where high infection rates are registered. Here we report a case of Linguatula serrata infection in a dog rescued from a suburban area, in southern . The dog was an approximately 6-months-old male of mixed breed, which had a history of free-roaming life, and which had been rescued by the dog owner in late November, 2012. Several months later, on March 2013, about two days after a treatment with a macrocylic lactone (ivermectine), the dog had expelled by sneezing several worm-like parasites. The parasite specimens were morphologically identified as adults of L. serrata. The epidemiological aspects of linguatulosis and potential risks of public health and veterinary concern are discussed.

Key words: Linguatula serrata, dog, .

introduction

Linguatula serrata is a cosmopolitan parasitic species of the phylum Pentastomida (order Porocephalida, family Linguatulidae).

The Phylum Pentastomida comprises a group of obligatory endoparasites of the respiratory tract and other organs / body cavities of tetrapod (particularly reptiles) vertebrates (Soulsby, 1982). Most pentastomids have an indirect life cycle: reptiles, amphibians and mammals, also fish or insects, serve as intermediate hosts in which the primary larvae develop through several molts to the infective stage (nymphs) in different organs and associated lymph nodes. The definitive hosts – wild and domestic carnivorous become infected by eating tissues from the intermediate hosts containing encysted infective stages (Christoffersen and De Assis, 2013).

L. serrata, commonly called tongue worm, inhabits as adults the nasal passages and frontal sinuses of wild and domestic canids (dogs, foxes), which serve as definitive hosts. Various

mammalian herbivores, such as cattle, sheep, goats, camels, rabbits serve as intermediate host, in which fully developed nymphs, the parasitic stage infective for carnivores, are found encysted in the lymph nodes, liver, lungs and serous membranes (Riley, 1986).

Although man is accidental host, the reports of human infection to this parasite is not uncommon, particularly in the (Yagi et al., 1996; Siavashi et al., 2002) where high infection rates in dogs are registered. (Oryan et al., 2008).

Humans become infected either by ingesting the eggs of parasite, resulting encapsulated larvae in internal organs, causing visceral linguatulosis (Tappe and Büttner, 2009), or eating infective nymphs contained in raw or undercooked viscera of infected intermediate hosts, causing nasopharyngeal linguatulosis (Yagi et al., 1996; Siavashi et al., 2002)

Here we report a case of L. serrata infection in a dog rescued from a suburban area, in southern .

MATERIAL AND METHODS

A male dog, mixed breed, approximately 6-months-old, with a history of free-rooming life had been rescued by the dog owner form a non-living rural area, outside of (), in late November 2012. Several months later, on March, 2013, the dog was presented in a veterinary clinic for consultation, due to a persistent nasal pruritus and skin lesions (depilation) observed on the head (around the mouth, nose, and eyes). Subsequently to the clinical examination, the dog was diagnosed with sarcoptic mange and treated by the vet with a macrocylic lactone (ivermectine), as the dog owner recalled.

About two days after the treatment, the dog had expelled by sneezing several worm-like parasites and the dog owner asked the authors for help with its identification.

The parasite specimens (n=4) were preserved in formalin and subjected for morphological examination and species identification.

Additionally, the owner was asked to bring also fecal samples from the dog for parasitological examination.

RESULTS AND DISCUSSIONS

At the clinical examination, the dog presented no any clinical signs, but minor skin lesions, such as depilations were still present around the nose and the mouth.

The parasite specimens were microscopically examined. Light microscopy examination of the parasites revealed specific features of L. serrata (Soulsby, 1982):

body whitish, transparent, elongate, with a tongue-like shape, slightly convex, and ventrally flattened body, with a rounded anterior and pointed (narrow) posterior end; length from ~4 cm to 6 cm (Figure 1);

the cuticle showed rings and spicules (Figure 2);

on the anterior, ventral side were noticed curved hooks with sharp tips (Figure 3).

All four specimens were females.

The fecal examination was negative for parasitic stages, including for L. serrata eggs.

Figure 1. Linguatula serrata: macroscopical view

Figure 2A. Linguatula serrata: cuticle with rings and spicules (x6, by stereomicroscopy)

Figure 2B. Linguatula serrata: [B] ventral anterior end:

mouth (black arrow); 4 hooks (double red arrows)

(x6, by stereomicroscopy)

DISCUSSIONS

Here we report a case of adult L. serrata infection in a dog with a history of a free-roaming live and then rescued by the dog owner. Considering the free-roaming life history of the dog (stray dog rescued from a suburban area), it is assumed that the infection was by eating infected viscera very likely from animals found dead on the field; as well, the dog might had been fed with infected animal viscera.

In favour of this assumption, the life cycle of L. serrata will be briefly described.

Dogs are the typical definitive hosts of L. serrata, while a wide range of mammals act as intermediate hosts; of them, herbivores, mainly ruminants such as cattle, sheep, goats, camels, are frequent the best hosts for the nymphal stage development (causing visceral linguatulosis) of the parasite (Riley, 1986).

The adults are large parasites, ranging in length from 1.8-2 cm in males to 3 – 13 cm in females (Taylor et al., 2007), that firmly attach to the mucosa of the nasal passages, causing nasal obstruction and chronic rhinitis (nasal discharge, sneezing) (Bonagura and Twedt, 2013). Females excrete per day thousands embryonated eggs (up to 5,000,000) (Mehlborn, 2008). The eggs are expelled by the definitive host (dog) either with nasal secretions (by coughing or sneezing) or in the faeces. Eggs, ingested by the herbivorous intermediate host, accidentally by humans, pass into gut where they hatch; then, the larvae migrate to the mesenteric lymph nodes and different viscera (lung, liver, etc.,), where after a number of moults (lasting up to five – six months), reached to nymphal stage. The nymphs encysted, become encapsulated, and may stay alive in the intermediate host for at least two to three years, (Soulsby, 1982). In the intermediate host, nymphal stages grow up to 6 mm; they have four hooks, mouth, annular rings, and spines (Riley, 1986). The definitive host becomes infected by consuming the infected viscera from intermediate hosts (Soulsby, 1982). Following ingestion, the nymphs migrate to the nasal passages where the final moult occur and reach maturity within six-seven months; their longevity is about 15 months (Taylor et al., 2007).

Therefore, in this report, the absence of the parasite eggs from the dog faeces might be

explained by the fact that the parasites had no reached the reproduction maturity, since the age of the dog was about 5-6 months.

The geographical range of L. serrata is almost global, but predominantly prevalent in warm tropical, and subtropical regions, where high infection rates are registered. Prevalence studies of L. serrata in different herbivorous have reported high infection rates in goats (50.75%), sheep (42.69%), cattle (36.62%), and buffaloes (26.6%), in North West of Iran (Rezaei et al., 2011); 10% in sheep in Turkey (Aldemir et al., 2014). Similar studies showed that 37.45% of client owned dogs in Nigeria were infected with L. serrata (Oluwasina et al., 2014), and from 27.83% to 76.2% of dogs in different parts of Iran (Rezaei et al., 2011; Oryan et al., 2008). The close contact between dogs and livestock explains the greater rates of infection in intermediate hosts (herbivorous, mainly ruminants) (Rezaei et al., 2011).

It is known that also close contact to L. serrata infected dogs and their secretions predispose humans to infection. As mentioned before, man might serve as accidental intermediate hosts (visceral linguatulosis), when ingesting the eggs (Tappe and Büttner, 2009). Intraocular infections, caused by L. serrata tongue worms, even extremely rare, have been described, including in Europe, such as one from Portugal and one, recently from Austria (Koehsler et al., 2011).

Humans can also serve as aberrant final hosts (nasopharyngeal linguatulosis) after ingesting raw or under-cooked viscera (liver, lungs, trachea) of infected intermediate hosts. The nasopharyngeal linguatulosis appears to be prevalent throughout the Middle East, where it is known as “Halzoun syndrome” (Siavashi et al., 2002) or as “Marrara” in Sudan. It is states that, in some areas of Sudan, up to 20% of the population may be affected (Yagi et al, 1996). These syndromes are associated with some popular, local or traditional dishes prepared from raw offal/raw meat.

In Romania, high prevalence rates for L. serrata nymphs infection in the mesenteric lymph nodes of slaughtered domestic ruminants from Transilvania region have been reported, of 60.5% in goats, 47.4% in cattle; 40.7% in sheep; 25.5% in buffaloes (Negrea et al., 2010).

However, in dogs, only sporadic clinical cases, or accidental findings during of necropsy are reported (Negrea, 2008). Therefore, the overall prevalence of L. serrata in Romanian dogs is very likely to be underestimated.

Considering the medical history of the dog in the present case, it may be assumed that the parasites were expelled subsequently to the ivermectin (a systemic macrocyclic lactone) treatment. However, when searching in the literature, information is scarce about treatment of linguatulosis. Usually, physical/surgical removal of the parasites is recommended for heavily infected dogs. Although, the sneezing may also provoke expelling of the worms, systemic insecticides could be also considered (Taylor et al (2007; Bonagura and Twedt, 2013). In this respect, a field study showed that ivermectin is an effective agent against, a related species, L. arctica in reindeer (and possibly against other pentastomids because of their similar arthopodal nerve system) (Haugerud et al., 1993). However, treatment of cattle, sheep or other livestock with parasiticides against tongue worms is usually not practiced, as they cause no economic damage. Therefore, management of linguatulosis relies mostly in preventative measures. So, prevalence studies on L. serrata infection in the definitive (dogs) and intermediate hosts (especially ruminant animals) are of epidemiological relevance, and could represent a basis for developing and applying control program and measurements.

CONCLUSIONS

This case report indicates that dogs with free-roaming life, having access to infected animal offal, have a higher risk for L. serrata infection. Subsequently, an infected dog become a potential source of infection and pose a public health and veterinary concern, mainly in endemic areas.

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