The zoonotic parasites of the genus Dirofilaria are on the increase as an accidental finding or as a cause of disease in humans worldwide. Human dirofilariasis usually manifests as either subcutaneous infiltrates or lung parenchymal dis- ease, in many cases asymptomatically. We report the case of a 77-year old female patient presenting with irritation and pain in her left eye. Ophthalmologic examination of the temporal part of her left eye revealed motile and threadlike or- ganism, which was surgically extracted and morphologically identified as Dirofilaria. Further molecular diagnostics with polymerase chain reaction (PCR) confirmed that the isolated organism is Dirofilaria repens. Due to already recog- nized autochthonous occurrence of human dirofilariasis in Croatia, human dirofilariasis must be included in the differ- ential diagnosis of patients presenting with subcutaneous nodules, eye affection and other potential manifestations of this disease

Gordana Mlinarić Galinović

Katarina Palko Bartulović

Khalil Nemer

Mario Sviben

Robert Škara

Tomislav Meštrović

English

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Coll. Antropol. 37 (2013) 3: 995–997Short communicationDirofilaria Repens as a Cause of SubconjunctivalInfection in a 77-Years Old Female Patient fromCroatia – A Case ReportMario Sviben1, Tomislav Me{trovi}2, Khalil Nemer3, Katarina Palko Bartulovi}3, Robert [kara3and Gordana Mlinari} Galinovi}11 Microbiology Service, Croatian National Institute of Public Health, Zagreb, Croatia2 Clinical Microbiology and Parasitology Laboratory, Polyclinic »Dr. Zora Profozi}«, Zagreb, Croatia3 General Hospital »dr. Ivo Pedi{i}«, Sisak, CroatiaA B S T R A C TThe zoonotic parasites of the genus Dirofilaria are on the increase as an accidental finding or as a cause of disease inhumans worldwide. Human dirofilariasis usually manifests as either subcutaneous infiltrates or lung parenchymal dis-ease, in many cases asymptomatically. We report the case of a 77-year old female patient presenting with irritation andpain in her left eye. Ophthalmologic examination of the temporal part of her left eye revealed motile and threadlike or-ganism, which was surgically extracted and morphologically identified as Dirofilaria. Further molecular diagnosticswith polymerase chain reaction (PCR) confirmed that the isolated organism is Dirofilaria repens. Due to already recog-nized autochthonous occurrence of human dirofilariasis in Croatia, human dirofilariasis must be included in the differ-ential diagnosis of patients presenting with subcutaneous nodules, eye affection and other potential manifestations ofthis disease.Key words: dirofilariasis, nematode, subconjunctival infection, ophthalmology, parasitologyIntroductionRepresentatives of the nematode, genus Dirofilaria,particularly Dirofilaria immitis, Dirofilaria repens, Di-rofilaria tenuis and Dirofilaria ursi, are becoming acommon finding either as an accidental discovery or dur-ing diagnostic assessment of patients around the worldpresenting with certain symptoms1. Dirofilariae are nat-ural parasites of a great variety of animals and, with theexception of D. immitis, they live in the subcutaneoustissue of their definitive host producing circulating mi-crofilariae which can be transmitted by various arthro-pods.Humans are accidental hosts for Dirofilaria genuswith patient symptomatic infections being extremely ra-re. Most documented human cases of infections with thisgenus are attributed to D. repens. As domestic and wildcanids are definitive hosts of D. repens, the dog is theprincipal reservoir for infection with this species. Mos-quitoes of the genus Aedes, Anopheles and Culex serve asintermediate hosts and vectors, and some species ofticks, lice and flies are suggested as possible vectors aswell1,2.D. repens infection in humans is usually manifestedas skin or subconjunctival infiltrates. These nematodesdo not normally reach sexual maturity in the human or-ganism. Consequently microfilaremia is not expected todevelop in humans. However, one case of subcutaneousD. repens infection with microfilariae in the circulationhas been described in the literature3.Clinical importance of this infection lies in the factthat dirofilariasis in humans is commonly misdiagnosedas tumour or some other granulomatous disease, whichcan lead to unnecessary and often invasive diagnostictests and procedures. It was decided to present in thisshort report a case of a female patient with conjunctivalform of this disease.995Received for publication October 28, 2011Case ReportA 77-year-old female patient was admitted to theophthalmology ward of General Hospital dr. Ivo Pedi{i}in Sisak for intermittent sensation of scratching, rubbingand sharp, thrusting pain in her left eye. She also experi-enced a sensation of movement in her eye, which laterbecame visible.Medical history revealed that the patient is in chargeof a large rural estate with a lot of dogs and cats present.An epidemiologically important detail was frequent pre-vious mosquito bites, through the patient had never trav-elled or resided outside Croatia.Ophthalmologic examination of the temporal part ofher left eyeball revealed a motile, threadlike structure.Biomicroscopy of the eye performed temporally presen-ted a long and thin live parasite under the chemotic andinjected bulbar conjunctiva, showing occasional serpen-tine movement. Light stimulus applied to the eye elicitedresponse from the organism in the sense of squatting andslowly calming down. Cornea was clear, and anterior eyechamber had normal content and depth. Further eyefindings were normal in accordance with age of the pa-tient. After clinical suspicion of dirofilariasis was estab-lished, operation was indicated. Upon surgical extirpa-tion of the parasite under local anaesthesia, the motilelarva about 10 centimetres (4 inches) in length wasplaced in a sterile test tube containing saline solutionand sent to the Parasitology Department of the CroatianNational Institute of Public Health in Zagreb. On the ba-sis of morphologic characteristics, it was confirmed thatthe extirpated larva belongs to the Dirofilaria genus.Polymerase chain reaction (PCR) confirmed that the or-ganism is Dirofilaria repens.Postoperative ultrasound of the patient’s left eye sho-wed normal findings.Materials and MethodsExtraction of the parasitic DNA was done using com-mercial Blood and Tissue Kit (QIAGEN) system, accord-ing to manufacturer’s instructions. Molecular identifica-tion of the parasite was conducted using DIDR-F1 (5’ –AGT GCG AAT TGC AGA CGC ATT GAG – 3’) andDIDR-R1 (5’ – AGC GGG TAA TCA CGA CTG AGT TGA– 3’) primers. Reaction mixture consisted of 1 x PCRbuffer, 1.5 mM MgCl2, 10 pmol of each primer, 200 mMdNTP and 1.5 U GoTaq polymerase (Promega). Amplifi-cation was carried out using a method developed byRinshiw and co-authors4. Primers were used to amplifyInternal transcribed spacer region 2 (ITS2) for D. im-mitis (542 bp), D. reconditum (578 bp) and D. repens (484bp) on Real Time PCR, Applied Biosystems Veriti ma-chine.DiscussionHuman infection with Dirofilaria can be manifestedin various forms. The majority of infestations are causedby D. repens species, which usually leads to developmentof subcutaneous nodules anywhere in the body, with apossibility of eye invasion5.Dirofilariasis is an endemic parasitic disease in theMediterranean Basin and territories of Ukraine andsouth Russia6. Review of literature on this topic suggestthat Italy is a European country with the highest preva-lence of human dirofilariasis, followed by France, Greeceand Spain5,7,8. Global warming and hot summers are im-portant contributing factors to the spread of Dirofilaria.Consequently, this parasite can be expected to appear inpreviously unaffected areas of Europe9. The first humancase of autochthonous D. repens infection in Hungarywas described in 200810. Autochthonous occurrence ofhuman dirofilariasis has been confirmed in Ukraine andRussia as well, with more and more diagnosed cases ev-ery year11,12. As an endemic organism, this parasite hasbeen found in the territories of Asia Minor, central Asiaand Sri Lanka13.About ten cases of human dirofilariasis have been de-scribed in Croatia to date, with nematode D. repens con-firmed as the sole causative agent. In the first describedcase from the year 1996, the affected region was the eyeand conjunctiva14, while in 2003, the first cases of subcu-taneous form of human dirofilariasis in Croatia werepublished15. From the clinical point of view, one of themost interesting cases was an infection manifested assubcutaneous, motile and painless nodule located in theleft breast of a 52-year-old woman, initially suggestive ofa malignant process16. All these examples of human sub-cutaneous dirofilariasis were described in patients fromthe Mediterranean part of Croatia17. In 2007, a rare caseof lacrimal gland dirofilariasis from inland Croatia wasdescribed, the second of its kind in the literature18. Thepatient’s general and ophthalmic condition was good,and infection clinically manifested as disfiguring swell-ing in the lateral part of the left upper eyelid, withoutany pain or loss of vision. Two more cases of subcutane-ous dirofilariasis were described in the same year, in pa-tients who neither travelled to endemic parts of Croatianor abroad2. Recently, one new case of ocular dirofilaria-sis in Croatia has been published, clinically similar to ourreport19.Key elements for accurate diagnosis of human diro-filariasis are clinical presentation of infection, as well asmacroscopic and histopathologic examinations of biopticmaterial. Due to unspecific results, serologic diagnosticsof dirofilariasis is not routinely used20, while PCR is typi-cally applied as the confirmatory test. The number of re-ported cases of human dirofilariasis and affected coun-tries has increased in the last decades, which is suppor-ted by a growing number of studies and case reports. Sev-eral contributing factors might be responsible, includingchanges in people’s lifestyle, greater medical awarenessin larger number of countries, increased travel to en-demic areas, global warming and climatic changes thatfacilitate the introduction of competent vectors into newgeographic areas, as well as a lack of adequate controlmeasures in animal reservoirs21.M. Sviben et al.: Dirofilaria Repens as a Cause of Subconjunctival Infection, Coll. Antropol. 37 (2013) 3: 995–997996Albeit rare, both clinicians and parasitologists shouldconsider and include dirofilariasis in the differential di-agnosis of patients presenting with subcutaneous nod-ules, eye affection and other potential manifestations ofthis disease.AcknowledgementThe authors thank Relja Beck, dr.vet.med. for kindhelp in molecular diagnostic of dirofilaria.R E F E R E N C E S1. PAMPIGLIONE S, RIVARSI F, Parassitologia, 42 (2000) 231. — 2.VICKOVI] N, GRANI] J, DESNICA B, MAKEK N, BALEN-TOPI] M,Infektolo{ki glasnik, 27 (2007) 135. — 3. NOZAIS JP, BAIN O, GENTI-LINI M, Bull Soc Path Exot, 87 (1994) 183. — 4. RISHNIW M, BARR SC,SIMPSON KW, FRONGILLO MF, FRANZ M, DOMINGUEZ ALPIZARJL, Vet Parasitol, 135 (2006) 303. — 5. PAMPIGLIONE S, RIVASI F, AN-GELI G, BOLDORINI R, INCENSATI RM, PASTORMERLO M, PAVESIM, RAMPONI A, Histopathology, 38 (2001) 344. — 6. MARU[I] Z, STAS-TNY T, KIRAC I, STOJ^EVI] D, KRU[LIN B, TOMAS D, Acta Derma-tovenerol Croat, 16 (2008) 222. — 7. MURO A, GENCHI C, CORDEROM, SIMON F, Parasitol Today, 15 (1999) 386. — 8. RACCURT CP, (1999)Dirofilariasis, an emerging and underestimated zoonosis in France, MedTrop (Mars), 59 (1999) 389. — 9. GENCHI C, RINALDI L, MORTARINOM, GENCHI M, CRINGOLI G, Vet Parasitol 163 (2009), 286. — 10. SZE-NASI Z, KOVACS AH, PAMPIGLIONE S, FIORAVANTI ML, KUCSERAI, TÁNCZOS B, TISZLAVICZ L, Wien Klin Wochenschr, 120 (2008) 96, —11. KRAMER LH, KARTASHEV VV, GRANDI G, MORCHÓN R, NA-GORNII SA, KARANIS P, SIMÓN F, Emerg Infect Dis, 13 (2007) 150. —12. DARCHENKOVA NN, SUPRIAGA VG, GUZEEVA MV, MOROZOVEN, ZHUKOVA LA, SERGIEV VP, Med Parazitol (Mosk), 2 (2009) 3. —13. DISSANAIKE AS, ABEYEWICKREME W, WIJESUNDERA MD,WEERASOORIYA MV, ISMAIL MM, Parassitologia, 39 (1997) 375. — 14.BUJGER Z, EKERT M, TOJAGI] M, ^A^I] M, GRANI] J, Ophthalmo-logica Croatica, 5 (1996) 63. — 15. PUIZINA-IVI] N, \AKULA N, BEZI]J, PUNDA-POLI] V, SARDELI] S, KUZMI]-PRUSAC I, Parasite, 10(2003) 382. — 16. BEZI] J, VRBI^I] B, GUBERINA P, ALFIER V, PRO-JI] P, MAROVI] Z, Ann Saudi Med, 26 (2006) 403. — 17. BEZI] J, ActaDermatovenerol Croat, 17 (2009) 82. — 18. JURI J, KUZMAN T, STIGL-MAYER N, TOJAGI] M, Ophthalmologica, 221 (2007) 204. — 19. JA-NJETOVI] Z, ARAR ZV, PARADZIK MT, SAPINA L, BITUNJAC M, LO-JEN G, MARINCULI] A, Acta Med Croatica, 64 (2010) 41. — 20. THEISJH, Vet Parasitol, 133 (2005) 157. — 21. GENCHI C, RINALDI L, CAS-CONE C, MORTARINO M, CRINGOLI G, Vet Parasitol, 133 (2005) 137.M. SvibenMicrobiology Service, Croatian National Institute of Public Health, Rockefellerova 7, 10000 Zagreb, Croatiae-mail: mario.sviben@hzjz.hrDIROFILARIA REPENS KAO UZRO^NIK SUBKONJUNKTIVALNE INFEKCIJE U 77-GODI[NJEPACIJENTICE IZ HRVATSKE – PRIKAZ SLU^AJAS A @ E T A KZoonotski paraziti iz roda Dirofilaria u porastu su kao slu~ajan nalaz ili kao uzrok bolesti u ljudi diljem svijeta.Ljudska dirofilarijaza obi~no se manifestira u vidu potko`nih ~vori}a ili kao bolest plu}nog parenhima, u velikom brojuslu~ajeva potpuno asimptomatski. Prikazujemo slu~aj 77-godi{nje pacijentice s pojavom iritacije i boli u lijevom oku.Oftalmolo{kim pregledom sljepoo~nog dijela njenog lijevog oka otkriven je pokretni organizam nalik kon~i}u, koji jekirur{ki odstranjen i morfolo{ki identificiran kao parazit iz roda Dirofilaria. Daljnja molekularna dijagnostika lan~a-nom reakcijom polimeraze (PCR) potvrdila je da se radi o vrsti Dirofilaria repens. Zbog ve} opisane autohtone ljudskedirofilarijaze u Hrvatskoj, dirofilarijaza se mora diferencijalno-dijagnosti~ki razmotriti kod pacijenata s potko`nim ~vo-ri}ima, zahva}anjem oka i drugim potencijalnim manifestacijama ove bolesti.M. Sviben et al.: Dirofilaria Repens as a Cause of Subconjunctival Infection, Coll. Antropol. 37 (2013) 3: 995–997997

Dirofilaria Repens as a Cause of Subconjunctival Infection in a 77-Years Old Female Patient from Croatia – A Case Report

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