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These infections are often relegated to medical curiosities as a result of the small number of cases. However, there is a need to recognize the nature of the infection, identify the worm, report the finding, and where possible, identify reservoir and intermediate hosts. Microscopic characterization and identification of the worm is crucial in this process and increases our knowledge of the biology and importance of filarial parasites, especially in the developing world where the facilities for such studies are non-existent or minimal because of limited personnel and resources.
We report our findings on two patients in whom we identified zoonotic filarial worms. These cases follow two initial reports of zoonotic Dirofilaria infection in 1994 from Kuwait and bring to four the recognized cases from the Arabian Peninsula.2,3
Case 1. A 12-year old Kuwaiti woman was seen initially for ocular complaints. During the course of clinical follow-up, the patient had recently reported a firm-to-hard swelling in the middle of the suprapubic region 5 cm from the symphysis pubis. Ultrasound examination showed a subcutaneous swelling that was not attached to the muscles.
A 1 x 1 cm mass was excised, sectioned, and stained with hematoxylin and eosin. A single, coiled, non-gravid, well-preserved female worm, with a maximum diameter of approximately 225 µm, was observed in fibofatty tissue (Figure 1A
). The cuticle had prominent circular ridges that were readily evident in longitudinal sections (Figure 1B
). Also evident was an inner layer of striae, with one under each ridge and one between each ridge (Figure 1B
). In cross section, the cuticle was thick when cut through an external ridge but relatively thin when cut between the ridges. The hypodermis was prominent and underlined the muscle layer. There were a few somatic muscle cells (meromyarian) that were weak and poorly developed, lateral chords were well developed, and an intestine and two uterine tubes were recognized (Figure 1C
). Only nonfertilized ova were present in the reproductive tube, and no microfilariae were seen in the uteri or in the surrounding tissue. The worm was identified as an Onchocerca spp. The patient had visited Najran in Saudi Arabia on the border with Yemen, approximately three months earlier, where she had stayed for approximately two months.
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A physical examination showed no nodules or any other abnormalities. The hematologic profile was normal and there was no eosinophilia. Results of liver and kidney function tests were in normal ranges.
The worm was placed in saline and immediately preserved in 70% ethanol and glycerol. It was cleared in glycerin, mounted, and examined microscopically. The worm was approximately 9 cm long and had a maximum diameter of 500 µm. Prominent longitudinal ridges were clearly visible; at mid-body level there were approximately 100 of them, and the distance between ridges was approximately 8–15 µm (Figure 2
). Other features that aided identification were the lance-shaped anterior end, mouth without lips, small head papillae, and a relatively short esophagus. The posterior end, which had a short tail, was blunt and rounded. The vulva, ovijector, and looped vagina were all readily evident. The uterus, which was paired with coiled uterine tubes, had no microfilariae. On the basis of these features, this worm was identified as a well-preserved, immature, infertile, female Dirofilaria spp. Based on the ocular location in the host, residence in Kuwait but with travel history to India, and, size and cuticular ornamentation of the worm, it was identified as Dirofilaria (Nochtiella) spp., most likely D. (N.) repens, a natural parasite of dogs that is endemic in Kuwait and India.
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Coincidentally, this patient had a concurrent diagnosis of ophthalmic toxoplasmosis. We were aware from the outset that the ocular complaint the patient reported was not related to the Onchocerca spp. infection; during several eye examinations to evaluate toxoplasmosis, no microfilariae were seen. Furthermore, sections also confirmed that the worm was immature; there were no microfilariae in the uteri or in the surrounding tissue. However, as a precaution, ivermectin was administrated with no adverse effects. Ocular complaints of toxoplasmosis and zoonotic onchocerciasis are interesting, not merely as a peculiarity, but add to the pool of knowledge on the subject in this geographic area where there is a paucity of such information.
Zoonotic Onchocerca cases are rare; 13 previous cases have been reported from the United States, Canada, Switzerland, Hungary, Russia, and Japan.1–4 The species involved in these infections were tentatively identified as O. gutturosa, O. cervicalis, O. reticulate, and O. dewittei japonica on the basis of morphologic features. A recent report (case 14) identified O. jakutensis by molecular techniques in a patient from the United States who had traveled throughout Europe.5
In case 2, the worm was observed in the conjunctiva of the patient and identified as a Dirofilaria spp. The genus Dirofilaria has two subgenera. The first subgenus is Dirofilaria, which is characterized by a smooth cuticle. The most widely recognized species in this group is D. immitis, the dog heart-worm, which is a common cause of zoonotic infection. The second subgenus is Dirofilaria (Nochtiella). Members of this group are characterized by having pronounced longitudinal ridges on the external surface of the cuticle, and as adults, the worms typically reside in subcutaneous tissues.1 The two most widely recognized species in this group that cause zoonotic infections are D. tenuis of raccoons in North America and D. repens of dogs in most other areas of the world.6,7 These two species account for most zoonotic human infections. Dirofilaria tenuis and D. repens take 6–9 months to develop to maturity. On the basis of the residence of case 2 in Kuwait, her recent visit to India, and the morphologic features of the worm, the specific diagnosis in this case was infection with an immature female D. repens. It is unclear in which country she acquired this infection. However, the size and development of the worm suggest that it was more than one month of age, which suggests that the infection was actually in Kuwait before her visit to India.
The number of cases of zoonotic dirofilariasis continues to increase. Identification and/or confirmation of the species are closely correlated with the areas where the infection was surmised to have taken place.
We have described two zoonotic filariasis cases in Kuwait caused by Onchocerca spp. and Dirofilaria spp. and have speculated on the most probable species responsible for these infections. The case of onchocerciasis is the first reported in Kuwait and the Arabian Peninsula. The case of dirofilariasis is the second case reported from Kuwait and the third from the Arabian Peninsula. We believe that continued interest in such infections is needed to document not only where they are occurring, but also to identify the responsible species. Although identification may be incomplete, even partial identification is essential and needs to be recorded so that these cases can be tracked.
Received June 11, 2008. Accepted for publication August 6, 2008.
Acknowledgment: We thank the physicians and surgeons of the district general hospitals for helpful discussions.
Financial support: This study was supported by Kuwait University (Project MI 03/03).
* Address correspondence to Parsotam R. Hira, Department of Microbiology, Faculty of Medicine, Kuwait University, PO Box 24923, 13110 Safat, Kuwait. E-mail: hira{at}hsc.edu.kw ![]()
Authors addresses: Parsotam R. Hira, Nabila Khalid, and Jamshaid Iqbal, Department of Microbiology, Faculty of Medicine, Kuwait University, PO Box 24923, 13110 Safat, Kuwait. Adel Al-Buloushi, Al-Bahar Eye Hospital, Kuwait. Odile Bain, Muséum National dHistoire Naturelle, USM 307, Parasitologie Comparée et Modèles Expérimentaux, Paris, France. Mark L. Eberhard, Division of Parasitic Diseases, Centers for Disease Control and Prevention, 4770 Buford Highway, Mailstop F13, Chamblee, GA 30341-3724.
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