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 Table of Contents  
CASE REPORT
Year : 2020  |  Volume : 32  |  Issue : 3  |  Page : 293-296

Ocular dirofilariasis in bosnia and herzegovina: A case report and review of the literature


1 Department of Ophthalmology, University Clinical Centre Tuzla, Tuzla, Bosnia and Herzegovina
2 Institute of Microbiology, Polyclinic for Laboratory Diagnostics, University Clinical Centre Tuzla, Tuzla, Bosnia and Herzegovina

Date of Submission26-Oct-2019
Date of Decision16-Dec-2019
Date of Acceptance11-Apr-2020
Date of Web Publication04-Jul-2020

Correspondence Address:
Jasmin Zvornicanin
Department of Ophthalmology, University Clinical Centre Tuzla, Trnovac bb, Tuzla 75000
Bosnia and Herzegovina
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/JOCO.JOCO_143_20

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  Abstract 


Purpose: To report a rare occurrence of ocular dirofilariasis in Bosnia and Herzegovina and provide a short overview on clinical characteristics and treatment options for ocular dirofilariasis.
Methods: A 75-year-old woman was admitted to the University Clinical Centre Tuzla with pain and redness in her left eye. A live, white, coiled, and active worm was noticed in subconjunctival space of bulbar conjunctiva.
Results: After successful surgical extraction, the parasite was identified as the adult form of Dirofilaria repens. There were no signs of intraocular or systemic inflammation.
Conclusion: Ophthalmologists should have in mind a possible infestation, especially in cases with repeated inflammatory reactions and swelling of the ocular region, which does not respond to conventional therapy.

Keywords: Conjunctiva, Dirofilaria, Eye, Zoonosis


How to cite this article:
Zvornicanin J, Zvornicanin E, Numanovic F, Delibegovic Z, Husic D, Gegic M. Ocular dirofilariasis in bosnia and herzegovina: A case report and review of the literature. J Curr Ophthalmol 2020;32:293-6

How to cite this URL:
Zvornicanin J, Zvornicanin E, Numanovic F, Delibegovic Z, Husic D, Gegic M. Ocular dirofilariasis in bosnia and herzegovina: A case report and review of the literature. J Curr Ophthalmol [serial online] 2020 [cited 2020 Aug 13];32:293-6. Available from: http://www.jcurrophthalmol.org/text.asp?2020/32/3/293/288936




  Introduction Top


Human dirofilariasis is a vector-borne zoonotic disease caused by nematodes of the superfamily Filarioidea and transmitted by blood-feeding mosquitoes from animals to man. Humans are the accidental hosts, and these worms are not capable to reproduce in human body.[1],[2],[3] The clinical picture of dirofilariasis depends on the type and location of the parasite in the human body. Ocular dirofilariasis is rare and can affect the orbit and periorbital region, the skin of the eyelids, the conjunctiva, the Tenon membrane, a retrobulbar space, or have intrabulbar localization.[3],[4]

The distribution of Dirofilaria repens is limited to the Old World, with highly prevalent areas (prevalence in dogs of >10%) in southern and eastern Europe, Asia Minor, Central Asia, and Sri Lanka.[5],[6],[7] In recent years, an increasing number of ocular dirofilariasis cases has been reported from neighboring countries Croatia[8],[9],[10] and Serbia,[11],[12],[13] but rarely from Bosnia and Herzegovina.[1],[3],[4],[14]

The purpose of this article is to present a rare case of ocular dirofilariasis from Bosnia and Herzegovina and to give an overview on clinical characteristics and treatment options for ocular dirofilariasis.


  Case Report Top


A 75-year-old woman had been presented to the Department of Ophthalmology of the University Clinical Centre Tuzla with a history of ocular redness, irritation, and foreign-body sensation in her left eye for the past 10 days. The patient was treated with topical antibiotics, gentamicin 0.3% eye drops, and chloramphenicol 1.0% ointment, prescribed by a local ophthalmologist. However, the symptoms worsened, and the patient was referred to the University Clinical Centre Tuzla. The patient was of a good socioeconomic status with no history of preceding ocular trauma, previous travel, or any animal contact. She had her cataract successfully operated in both eyes 6 years ago.

Clinical examination revealed visual acuity of 20/20 in both eyes. Slit-lamp examination was normal in the right eye with regular pseudophakia. The left eye demonstrated significantly hyperemic but transparent conjunctiva, with the extremely active and mobile white worm, wrapped in concentric circles in the subconjunctival space on the temporal side of bulbar conjunctiva [Figure 1]. The anterior segment also presented regular pseudophakia, and there were no signs of intraocular inflammation. The fundus examination in both eyes was normal, with measured intraocular pressure of 15.0 mmHg bilaterally. The pupil reaction was normal, and extraocular movements were full in both eyes.
Figure 1: External photograph of subconjunctival dirofilariasis before extraction

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Informed consent was obtained and immediate surgical intervention in topical anesthesia was performed. An incision of approximately 3 mm in the temporal part of the bulbar conjunctiva was made. Immediately, a part of the parasite emerged from the incision, and filaria was gently pulled out with the pair of tweezers [Figure 2]. The wound and surrounding subconjunctival space were cleaned with povidone-iodine 0.5% and vancomycin 1 mg/0.1 mL solutions.
Figure 2: Surgical removal of the parasite

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The parasite was put into formalin and sent to the Institute of Microbiology of the University Clinical Centre Tuzla for identification. Morphological examination showed that the specimen was a mature female worm of D. repens, with 11.5 cm in length and the maximum width of 600 μm [Figure 3]. Laboratory tests, including the inflammatory markers, were normal, and peripheral blood smear presented no signs of microfilariae. Stool and chest X-ray findings were also normal. The patient was treated postoperatively with topical moxifloxacin 0.5% eye drops and a combination of neomycin 0.3%/polymyxin B sulfate/dexamethasone 0.1% eye drops and ointment for 2 weeks. Since the parasite was already identified early the next day, systemic antibiotics and anti-helminths were not used. Control examination one and six months after the intervention revealed a completely normal anterior segment of the left eye, with discrete conjunctival scaring in the temporal conjunctiva, while all systemic and inflammatory parameters were normal.
Figure 3: Top: photograph of Dirofilaria following subconjunctival removal. Bottom left: anterior end of the adult female. Bottom right: longitudinal striations in the form of ridges on the surface of the cuticle

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  Discussion Top


According to the classification of the genus Dirofilaria, there are more than 40 described species, but only a few of them cause human infections: immitis, tenuis, repens, inermis, and ursi.[1],[2],[3],[4] Human ocular dirofilariasis is typically caused by D. repens, while reports of Dirofilaria immitis as an agent of ocular dirofilariasis are extremely rare.[2],[3] Human infections due to D. repens appear to be increasing throughout the world, and it should be considered an emerging zoonosis.[1],[3] More than 1500 cases of human subcutaneous or ocular dirofilariasis caused by this pathogen have been documented worldwide.[6] It is important to note that the published reports of human Dirofilaria infections are based on clinically manifest disease, and it is likely that the infections are much more frequent considering the serological data.[1],[3],[4]

Cases of D. repens in dogs are reported in the whole Balkan region, with high variations of prevalence in different countries.[1],[3] Two neighboring countries of Bosnia and Herzegovina, Croatia, and Serbia reported prevalence up to 47.3% and 49%, respectively, while in Bosnia and Herzegovina it is 1.9%.[1] In the Balkan Peninsula, only a few studies have presented risk areas in Romania, Serbia, and Albania, although, from published data, it is difficult to obtain a clear idea where the infection is endemic in the canine population.[1],[4] Several factors including climate changes with the global rise of the temperatures, introduction of new competent vectors, and relocation of infected microfilaremic dogs, which are the main reservoirs of infection, have allowed the spread of Dirofilaria infections from the endemic areas.[1],[3],[15]

A detailed analysis of the literature in English has been performed. The following keywords: filariasis, zoonosis, Dirofilaria, eye, ocular, conjunctiva, Bosnia and Herzegovina, and the following Medical Subject Headings: ophthalmology, microbiology, parasitosis, and eye were used for literature review. The analysis revealed a total of two cases describing ocular filariasis in patients from Bosnia and Herzegovina. The first case was reported from our institution, while the second one was reported in Austria on a patient that had previously traveled to our country [Table 1].[16],[17]
Table 1: Summary of reported cases of ocular dirofilariasis in Bosnia and Herzegovina

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In recent years, an increasing number of human subcutaneous and especially human ocular dirofilariasis cases with different clinical presentations has been reported from the neighboring countries of Croatia[8],[9],[10] and Serbia.[11],[12],[13] On the other hand, in the majority of recent reports, Bosnia and Herzegovina is still a country with no epidemiologic data about human dirofilariasis.[1],[3],[4],[14] Although we have found two cases of ocular dirofilariasis, considering the above-mentioned facts, the estimated number of unreported cases in Bosnia and Herzegovina is probably much higher.[1],[3],[7] The main reason for under-reporting of dirofilariasis in Bosnia and Herzegovina may be due to the poor knowledge and still low awareness of possible infestation among health workers.[3]

Presenting symptoms are variable, depending on the worm location, including orbit and periorbital region, the eyelids skin, the conjunctiva, the Tenon membrane, a retrobulbar space, or intrabulbar localization.[4] In most cases with ophthalmic infection, the patient presents with ocular pain, eyelid and conjunctival redness and swelling, sometimes blurred vision, and rarely proptosis and diplopia.[8],[18] It is also important to note that most of these patients had been previously unsuccessfully treated with local antibiotics and corticosteroids, just like in our case.

There are no valid diagnostic blood tests for ocular dirofilariasis. In these cases, serological fluorescent antibody test, enzyme-linked immunosorbent assay technique, and the polymerase chain reaction are negative.[2],[3],[4],[8],[18] Peripheral blood smears, as in our case, are mostly negative for microfilaria, and only one case of circulating diromicrofilaremia in humans has been reported.[19] Eosinophilia occurs in < 15% of cases with D. immitis and rarely with D. repens.[18] The diagnosis is most commonly made by clinical presentation depending on the ocular localization. However, the only proper diagnosis can be made by the microbiologist and pathologist after an excisional biopsy. The species identification of Dirofilaria is based on morphological characteristics of the helminthic cross-section. D. repens is identified by the presence of external longitudinal cuticular ridges and transverse striations, which are absent in D. immitis.[4],[18]

Surgical removal of the worm is the treatment of choice in cases with ocular dirofilariasis. Depending on the parasite localization, different surgical approaches can be used. In cases of subconjunctival or localization in the lacrimal gland, surgery is technically simple with good results. During the surgery, it is possible to paralyze the parasite's movements by application of the local anesthetic.[13] The recovery after surgical intervention is generally good without severe ocular complications. However, in cases of intraocular localization, the surgical approach is more challenging and might require surgery in general anesthesia with the use of vitreoretinal surgical procedures.[18] In addition, these patients require longer follow-up due to possible postoperative complications such as endophthalmitis, cataract, and glaucoma.[18],[20]

Oral anti-helminthic drugs are considered ineffective in the management of ocular dirofilariasis.[2],[20] Thus, D. repens cases must be differentiated from D. immitis, which requires the use of anti-helminthic agents. Furthermore, in a small number of cases of D. repens, ivermectin and/or diethylcarbamazine have been tried with good results. Oral therapy with diethylcarbamazine 2 mg/kg destroys others not yet visible worms although human dirofilariasis is usually regarded as an infection by a single worm.[4],[18]

We present a rare case of ocular dirofilariasis in Bosnia and Herzegovina. It is important to note that in our country as an endemic area, we can expect an increasing number of patients with dirofilariasis. Therefore, ophthalmologists should have in mind a possible infestation, especially in cases with repeated inflammatory reactions and swelling of the ocular region, which does not respond to conventional therapy.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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1.
Tasić-Otašević SA, Trenkić Božinović MS, Gabrielli SV, Genchi C. Canine and human Dirofilaria infections in the Balkan Peninsula. Vet Parasitol 2015;209:151-6.  Back to cited text no. 1
    
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Capelli G, Genchi C, Baneth G, Bourdeau P, Brianti E, Cardoso L, et al. Recent advances on Dirofilaria repens in dogs and humans in Europe. Parasit Vectors 2018;11:663.  Back to cited text no. 3
    
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Trenkić-Božinović M, Otašević S, Stanković-Babić G, Tasić A, Trenkić M. Human ocular dirofilariosis: Clinical and epidemiological features. Acta Med Medianae 2014;53:80-4.  Back to cited text no. 4
    
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Simón F, Siles-Lucas M, Morchón R, González-Miguel J, Mellado I, Carretón E, et al. Human and animal dirofilariasis: The emergence of a zoonotic mosaic. Clin Microbiol Rev 2012;25:507-44.  Back to cited text no. 5
    
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Fuehrer HP, Auer H, Leschnik M, Silbermayr K, Duscher G, Joachim A. Dirofilaria in humans, dogs, and vectors in Austria (1978-2014)-from imported pathogens to the endemicity of Dirofilaria repens. PLoS Negl Trop Dis 2016;10:e0004547.  Back to cited text no. 6
    
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Otranto D, Eberhard ML. Zoonotic helminths affecting the human eye. Parasit Vectors 2011;4:41.  Back to cited text no. 7
    
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Juri J, Kuzman T, Stiglmayer N, Tojagić M. A case of lacrimal gland dirofilariasis. Ophthalmologica 2007;221:204-6.  Back to cited text no. 8
    
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Janjetović Z, Arar ZV, Paradzik MT, Sapina L, Bitunjac M, Lojen G, et al. [Ocular dirofilariasis: A case report]. Acta Med Croatica 2010;64:41-5.[Article in Croatian]  Back to cited text no. 9
    
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Sviben M, Mestrović T, Nemer K, Bartulović KP, Skara R, Galinović GM. Dirofilaria repens as a cause of subconjunctival infection in a 77-years old female patient from Croatia – A case report. Coll Antropol 2013;37:995-7.  Back to cited text no. 10
    
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Dujic MP, Mitrovic BS, Zec IM. Orbital swelling as a sign of live Dirophilaria repens in subconjunctival tissue. Scand J Infect Dis 2003;35:430-1.  Back to cited text no. 11
    
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Dzamić AM, Arsić-Arsenijević V, Radonjić I, Mitrović S, Marty P, Kranjcić-Zec IF. Subcutaneous Dirofilaria repens infection of the eyelid in Serbia and Montenegro. Parasite 2004;11:239-40.  Back to cited text no. 12
    
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Jaksic V, Mitic N, Pavlovic I, Vitosevic Z, Mirkovic M, Zoric Z, et al. Discrete eyelid swelling caused by live subconjunctival Dirofilaria repens. Cent Eur J Med 2011;6:177-80.  Back to cited text no. 13
    
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Otranto D, Dantas-Torres F, Brianti E, Traversa D, Petrić D, Genchi C, et al. Vector-borne helminths of dogs and humans in Europe. Parasit Vectors 2013;6:16.  Back to cited text no. 14
    
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Boss JD, Sosne G, Tewari A. Ocular dirofilariasis: Ophthalmic implication of climate change on vector-borne parasites. Am J Ophthalmol Case Rep 2017;7:9-10.  Back to cited text no. 15
    
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Nurkic M, Sarajlic D, Cickusic E, Tihic N, Numanovic F, Delibegovi Z, et al. Dirofilariasis conjuctivae: The first case in bosnia and herzegovina. Acta Med Sal 2008;37:88-92.  Back to cited text no. 16
    
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Ritter A, Egger S, Emesz M. Dirofilariosis: Subconjunctival infection with Dirofilaria repens. Ophthalmologe 2012;109:788-90.  Back to cited text no. 17
    
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Patel R, Singh S, Bhavsar S. A rare case of subconjunctival dirofilariasis by Dirofilaria repens in rural Gujarat. Indian J Ophthalmol 2014;62:649-51.  Back to cited text no. 18
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Argy N, Sabou M, Billing A, Hermsdorff C, Candolfi E, Abou-Bacar A. A first human case of ocular dirofilariosis due to Dirofilaria repens in Northeastern France. J Trop Med 2011;2011:698647.  Back to cited text no. 19
    
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