Onchocerca jakutensis ocular infection in Poland: a new vector-borne human health risk?

Abstract

Background: Zoonotic onchocerciasis is a vector-borne disease, which involves many animal species, including large ungulates, boars, dogs, and sporadically, humans. So far, 39 cases of zoonotic onchocerciasis have been reported worldwide, 30 of which have been found in the last 20 years. Onchocerca nematodes are transmitted to humans by blood-sucking vectors during a blood meal. The following species have been responsible for zoonotic infections: Onchocerca cervicalis, O. dewittei japonica, O. gutturosa, O. jakutensis and O. lupi. In humans, the worms have usually been found in the subcutaneous tissues where they form subcutaneous nodules, induce inflammation of musculature, or penetrate the eye. Thirteen ocular zoonotic onchocerciasis cases have been reported so far. In the eye, nematodes were localized in the subconjunctival space, anterior chamber and within the vitreous body. Methods:In a 39-year-old male patient, a writhing worm in the vitreous body of the left eye was detected and surgically removed. Laboratory identification of the worm was based on macroscopic and molecular identification, based on sequencing of the cytochrome c oxidase subunit 1 gene (cox1). Phylogenetic analysis of the first 250 nucleotide sequences showing the highest levels of similarity with the present isolate in a BLAST analysis was performed.Results: Here, we report the first case worldwide of human ocular infection with O. jakutensis, a natural parasite of red deer. By exploiting a PCR assay, we detected the sequence almost identical to O. jakutensis (GenBank: KT001213.1; positions 1-650) with a single mismatch G/A at position 622. The sequence reported in this paper was deposited in the GenBank database under the accession number MK491767. Conclusions:Our case together with the previous case reports indicate that zoonotic Onchocerca worms exhibit no tissue specificity and an eye infection has been described in over one third of human zoonotic onchocerciasis cases. In terms of the growing number of cases of zoonotic onchocerciasis in Europe, the USA and Japan, attention should be paid to the diagnosis of subcutaneous nodules and eye infestations.

Zoonotic Implications of Onchocerca Species on Human Health

“…Description of the most common Onchocerca species identified parasitizing animals and humans, related to their main vectors, hosts, and geographical distribution. [58], humans [68] Some authors emphasize that knowing the evolutionary history of a parasite and its spread among its hosts is crucial to control the disease it causes [104]. The origin of the genus Onchocerca and its principal evolution may have been started in Africa.…”

“…So far, 40 cases of Onchocerca species infecting animals have been described in humans worldwide, and all of them are within the Holarctic region [68,96,[118][119][120][121][122][123][124][125][126] (Figure 2). Among these cases in humans, O. lupi was the most prevalent species identified, followed by O. dewittei japonica and, to lesser extent, O. jakutensis, O. gutturosa, and O. cervicalis.…”

“…Since 2015, 12 reports of Onchocerca species infecting animals have been described in humans [68,96,118,119,[121][122][123][124][125][126]. Five of them were caused by O. lupi, which was found in the upper cervical spinal cord, conjunctiva, head, and forearm of five individuals diagnosed in the United States [121,122].…”

“…Six more cases were reported in Japan, caused by O. dewittei japonica, which was isolated from the upper extremities in five individuals [123][124][125][126] or from the head of one person [96]. The most recent case was caused by O. jakutensis and was found in the vitreous body of the eye of a man from Poland [68]. These cases were generally caused by immature adult female worms, most of them with no evidence of fertile adult worms, and thus no microfilariae seemed to be produced [39].…”

“…These cases were generally caused by immature adult female worms, most of them with no evidence of fertile adult worms, and thus no microfilariae seemed to be produced [39]. However, to determine the fertile status of these worms, it was important to remove them intact from the nodules or tissues where they were located [68]. Sometimes, the worms were damaged during their extraction, and therefore, the chances of obtaining a good quality sample for morphological identification were reduced [68].…”