A rare case of tick infestation of the eyelid : case report and literature review

E ste artigo apresenta um caso de infestação por carrapatos da pálpebra inferior por um a espécie previam ente não declarada. U m hom em de 71 anos de idade apresentou-se com um carrapato grudado na pálpebra inferior. O carrapato foi identificado m orfologicam ente, e, em seguida, um a estrutura m olecular através de reacção em cadeia da polim erase (PC R ) e a sequenciação do seu D N A . A lém disso, um a análise da literatura pertinente aos gêneros de carrapatos associados à infestação do olho hum ano é fornecido. O carrapato, que estava em fase de desenvolvim ento das ninfas, foi identificado pela prim eira vez de acordo com chaves taxonôm icas com o D erm acentor sp. Para identificação de espécies com pleta, gene 16S rD N A PC R e sequenciam ento foram realizadas, que m ostrou que o carrapato foi D . m arginatus. Sistem atizando espécie de carrapato poderia ajudar os m édicos a determ inar o potencial de transm issão de doenças hum anas transm itidas por carrapatos. D escritores: Infestações por carrapato/parasitologia; Infecções oculares parasitarias; Pálpebras/patologia; R eação em cadeia da polym erase; Sequência de bases; D erm acentor/parasitologia; M ordeduras e picadas; R elatos de casos A BSTRA C T


A BSTRA C T T his article presents a case of tick infestation of the low er eyelid by a previously unreported species. A 71-year-old m ale presented w ith a tick attached to the low er eyelid. T he tick w as identified m orphologically, and then m olecularly via polym erase chain reaction (P C R )
and sequencing of its D N A .In addition, a review of the literature relevant to the genera of ticks associated w ith infestation of the hum an eye is provided.T he tick, w hich w as in the nym phal developm ental stage, w as first identified according to taxonom ic keys as D erm acentor sp.For com plete species identification, 16s rD N A gene P C R and sequencing w ere perform ed, w hich show ed that the tick w as D .m arginatus.System atizing tick species could assist physicians in determ ining the potential for transm ission of tick-borne hum an diseases.

T
icks are acarine ectoparasites, and are among the most important vectors of human and animal diseases.Tickborne diseases are a significant threat to public health.Ticks infected with microbiological agents (primarily viruses, bacteria, and protozoa) transmit diseases to vertebrate hosts while feeding on their blood 1,2 .In Turkey, numerous tick species attached to humans have been reported 3,4 , and they transmit very serious diseases, including Crimean-Congo hemorrhagic fever, tick-borne rickettsiosis, and Lyme disease [5][6][7] .Tick infestation of the eyelid is a rare condition.Herein we report on a 71-yearold man with a tick attached to the right lower eyelid that was identified morphologically and molecularly, and a review of the literature relevant to the genera of ticks associated with infestation of the human eye.

CASE PRESENTATION
A 71-year-old man with a two-day history of a small gray lesion on the medial aspect of the lower right eyelid presented to Nigde State Hospital, Ophthalmology Clinic with itching and localized redness caused by tick infestation.He was a farmer from a rural region and had contact with farm animals, which we considered was the likely source of tick infestation.Ophthalmologic examination showed a two millimeter elevated light gray lesion compatible with a tick on the medial aspect of the right lower eyelid (Figure 1).The head of the tick was embedded in the skin of the eyelid and its body moved during manipulation with tweezers.The remainder of the eye examination, including visual acuity and anterior segment examination, was normal.The patient did not have any systemic symptoms at presentation.
The tick was successfully removed using tweezers.The patient's blood was drawn to screen for thrombocytopenia; the platelet count was normal at presentation and one month later.During follow-up, one week post presentation, erythema of the lower eyelid was found to have subsided without the use of topical medication.The tick was sent to the laboratory of the School of Veterinary Medicine, Protozoology and Entomology at Ankara University for further investigation and identification.The tick, which was in the nymphal developmental stage, was identified according to taxonomic keys 8 as Dermacentor sp.For complete species identification16s rDNA gene PCR and sequencing were performed 9 , which showed that the tick was D. marginatus.

DISCUSSION
Ticks embedded in the meibomian gland orifice or in the eyelash margin generally manifest as a mass on the eyelid margin.The most frequent symptomatic eye manifestations are conjunctivitis, uveitis, keratitis, and vasculitis 10 .The genera of ticks that have attached to human eyelids have been described previously: the nymphal form of D. auratus was the first documented tick embedded in the human eyelid 11  Bodé et al. reported that in addition to human eyelids, tick infestation can occur in conjunctival tissue; they identified a tick embedded in the conjunctiva as the larval form of Amblyomma americanum 15 .Singh et al. reported an 11-year-old girl living in an urban region of Singapore with Ixodessp.infestation of the upper eyelid; however, despite the fact that ticks are more common in rural environments, they reported that tick infestation of the eyelid can occur in urban regions 16 .Liolios et al. reported a 40year-old female in England with a tick of the Ixodesgenus on her left lower eyelid, without any other ophthalmological findings 17 .
Ticks must be removed as soon as possible, as animal and human studies have shown that the risk of disease transmission increases after 24 hours of attachment and increases significantly after 48 hours 18 .Holak et al. reported Lyme borreliosis in 1 of 5 patients diagnosed with left abducens nerve palsy following Ixodes genus infestation of the eyelid region 19 .Keklikci et al. reported another tick described as I. ricinusin in a three-yearold girl's right upper eyelid margin.They advised removing such ticks as soon as possible via mechanical procedures to prevent disease transmission 20 .While a tick is attached, or after its removal, an inflammatory reaction leading to abscess formation or secondary infections may occur 18 .Sakalaret al. reported on a four-year-old girl with cellulitis due to infestation by the nymphal form of a tick of the Ixodes genus 21 .
It is important to know that ticks can produce one or more toxins that cause tick paralysis by blocking the neuromuscular system.Symptoms can be local, such as facial nerve paralysis, or systemic.Commonly, there is an ascending flaccid motor paralysis that occurs within hours or up to a few days after tick bites.The paralysis usually progresses to respiratory failure and even death.Almeida et al. described tick paralysis in a 28-year-old male due to immature stages of ticks, probably of the Amblyomma genus.Their patient had shown loss of muscle strength, decreased reflexes, and marked palpebral ptosis.The ticks were removed individually, and the patient's ptosis improved six hours after the last tick was removed.The following day there was near total regression of manifestations.The researchers recommended that all cases of suspected tick paralysis should be promptly diagnosed and treated 22 .
Tick paralysis has been described in Turkey: Gürbüz et al. reported a three-year-old girl with facial palsy caused by Hyalomma marginatum 23 ; Engin et al. described tick paralysis with atypical upper trunk involvement of the brachial plexus in a 66 year-old male farmer 24 ; and Doðan et al. reported a case with peripheral facial nerve paralysis due to a tick of the genus A rare case of tick infestation of the eyelid: case report and literature review Hyalomma attached to the external auditory canal 25 .It is also important to know that D. marginatus can also cause tick paralysis: Abdigoudarzi et al. described tick paralysis in a 48-year-old female in Iran caused by D. marginatus 26 .
In Turkey, D. marginatus ticks are known to transmit the following disease pathogens to humans: Rickettsia slovaca and R. raoultii, which cause TIBOLA/DEBONEL (tick-borne lymphadenopathy/ Dermacentor-borne necrosis erythema and lymphadenopathy) 7 , and Crimean-Congo hemorrhagic fever virus 27 .In addition, Coxiellabrunetti, Omsk hemorrhagic fever virus, R. sibirica subsp.sibirica, and Francisellatularensis are transmitted by D. marginatus ticks, but such transmission has yet to be observed in Turkey.
Tick infestation of the human eyelid is rare.Systematizing the species of ticks that attach to the eyelid can alert physicians to the potential for transmission of the above-mentioned disease pathogens.Timely mechanical removal of ticks is an easy, safe, and effective method of preventing tick-associated systematic and local ocular complications.

Figure 1 :
Figure 1: D. marginatus attached to the medial aspect of the patient's right lower eyelid.
DOI 10.5935/0034-7280.20160030 ; E ye infections, parasitic; E yelids/pathology; P olym erase chain reaction; B ase sequence; D erm acentor/parasitology; B ites and stings; C ase reports R ev B ras O ftalm ol.2016; 75 (2): 144-6 ; Hara et al. reported Ixodesovatus Neumann in a 30-year-old female's right superior eyelid 12 ; Santos-Bueso et al. reported Rhipicephalus sanguineus for the first time in a 21-year-old female's right upper eyelid 10 ; Samaha et al. reported a nymphal stage tick of the genus Hyalomma, but of an unspecified species in a 58-year-old female's left upper eyelid margin 13 ; and McLeod described I. ricinus in an 11-month-old girl and reported that I. ricinus was the most common tick in Scotland, Wales and the West of England 14 .