Rhipicephalus (Boophilus) microplus (Arachnida: Ixodidae) larvae infestation of human eyelids. A rare case

An 82-year-old female patient with painful, watery, and itchy eyes was admitted for examination at the Sri Guru Ramdas Institute of Medical Sciences and Research. During the examination, a number of tick larvae were found attached to the patient’s upper and lower eyelid margins. The ticks were manually removed and the patient was treated with topical ciprofloxacin eye ointment. Microscopic studies revealed that all specimens belonged to a single species Rhipicephalus (Boophilus) microplus Canestrini (Acari: Ixodidae) which parasitizes livestock. Although other cases of ocular infestations have been reported, this is the first in North India involving R. (B.) microplus. It is speculated that the patient’s occupation, surrounding conditions and living propensities made her susceptible to contamination by ticks.


Introduction
Ticks are hematophagous ectoparasites that infest amphibians, birds, mammals, and reptiles (Black and Piesman, 1994). Ticks rank second only after the mosquitoes in transmitting human infectious diseases worldwide (de la Fuente et al., 2008).
Ocular infestations by ticks are unusual in humans, but cases have been reported in different areas of the world (e.g., Mentz et al., 2016;Uzun et al., 2016 andLin et al., 2016). Presented herein, is a case of ocular infestation by R. (B.) microplus larvae on the eyelids of an elderly female patient, a condition which has not been previously reported from North India.
Rhipicephalus (Boophilus) microplus is a single-host tick belonging to the family Ixodidae. Out of 106 reported tick species from India, R. (B.) microplus is considered the most important tick economically because of its impacts on livestock production (Ghosh et al., 2007). As a vector of babesiosis (caused by the protozoan parasites Babesia bovis and B. bigemina) and anaplasmosis (caused by Anaplasma marginale) R. microplus adversely affects cattle health in tropical and subtropical areas of the world (Connell, 1974 andOliveira-Sequeira et al., 2005). The life cycle of R. (B.) microplus includes four developmental stages: egg, larva, nymph and adult. The newly hatched larvae crawl upon plants or grass to access the host. Larvae usually seek soft skin like inside flanks, thighs and forelegs for attachment (Estrada-Pena et al., 2006). On a typical host, the rest of the life cycle continues, using the same host individual for all subsequent blood meals; only the engorged female will leave the host to lay her eggs on the ground.

Case Report
An 82-year-old female with itchy, red, and watery eyes was admitted to the Sri Guru Ramdas Institute of Medical Sciences and Research, Amritsar, Punjab. Slit lamp examination revealed that a large number of ticks adhered to the upper and lower eyelid margins of both eyes (Fig. 1). All ticks were manually removed with blunt forceps and preserved in 70% alcohol. After removal of the ticks, attachment sites were cleaned thoroughly with antiseptic solution (povidone-iodine solution). Ciprofloxacin 0.3% ointment was prescribed to be applied to the affected area twice daily for a week. On examination, the patient revealed that she was engaged in dairy farming and had close contact with domestic livestock. To find out the source of infestation, we visited patient's home with our co-fellows and observed that her livestock were heavily infested with the tick R. (B.) microplus. Despite of being aware about the infestation of their livestock, the patient's family had taken no action to control the ticks. They were advised to treat the animals with acaricides to avoid further infestations. For identification, specimens were submitted to the Acarology laboratory of the Department of Zoology and Environmental Sciences, Punjabi University Patiala, Punjab (India). After clearing the specimens in 60% lactic acid, permanent slides were prepared using Hoyer's medium. Photographs of the slides were taken in the Sophisticated Instrumentation Centre at Punjabi University Patiala, Punjab (India). The species identity of each specimen was determined based on morphology, following the descriptions and keys given by Walker and colleagues (Walker et al., 2003). All the specimens were identified as larvae of Rhipicephalus (Boophilus) microplus (Fig. 2).

Discussion
Eyelid infestation with hematophagous ticks is a rare condition. Ticks infest humans in the absence of their natural host and/or when in close proximity to the natural hosts. Other cases of human eye infestation by Ixodes ricinus in the U.K. (McLeod, 1986;Bowes et al., 2015) and by larvae of Amblyomma americanum in the U.S.A. (Bode et al., 2006;Holak et al., 2006) have been reported .In Turkey, Keklikci and co-workers reported Ixodes ricinus on the upper eyelid margin of a three-year-old girl and advised removing such ticks as soon as possible via mechanical procedures to prevent disease transmission (Keklikci et al., 2009). Sakalar et al. reported a four-year-old girl with cellulitis due to infestation by nymphal forms of Ixodes sp. (Sakalar et al., 2010). Celebi and Orkun presented a case report of tick infestation on the lower eyelid of a 71-year-old male with a nymph of Dermacentor marginatus (Celebi and Orkun, 2016).
A few instances of human eye infestation with ticks have been reported from India. In 1977, a case of Rhipicephalus sp. pervasion on the lower eyelid of a 22-year-old man was reported from Karela, India (Ittyerah and Fernandez, 1977). In the Chennai hospital, a 20-year-old male was admitted with painful swelling of the left lower eyelid that had been slowly progressing for 5 days. He was found to be infested with the tick Rhipicephalus sanguineus (Kumaran, 2015). Ticks belonging to genera Haemaphysalis were also reported infesting the lower eyelid of a male from Uttrakhand who had cattle and was sleeping at ground the night before the infestation (Kumar and Chhangte, 2015).
Severe disease associated with human tick infestations have been reported from India (Vasudevan andChatterjee, 2013 andCelik et al., 2013) including those transmitted by R. ( B.) microplus such as babesiosis, and anaplasmosis (Ghosh and Nagar, 2014). To reduce the probability of transmission, ticks should be removed as soon as possible from patients; studies have shown that the risk of disease transmission increases after 24 hours of attachment and is even higher after 48 hours (Gammons and Salam, 2002). For tick removal, chemical and mechanical methods have been suggested, but mechanical removal is considered as the most safe, quick, and effective method.
In the current case, larvae of R. (B.) microplus were found attached to the eyelids of the patient. The patient lived in close proximity to dairy cattle and other domestic animals increasing her potential for tick infestation. Clean surroundings, controlling infestation levels on animals, good personal hygiene, and avoiding prolonged direct contact with domestic animals can reduce the risk of tick infestation.