Original Article - Springer Link

Original Article Wien Klin Wochenschr (2008) 120/3–4: 96–102 DOI 10.1007/s00508-008-0928-2

WIENER KLINISCHE WOCHENSCHRIFT The Middle European Journal of Medicine Printed in Austria

Human dirofilariosis in Hungary: an emerging zoonosis in central Europe Zsuzsanna Szénási1, András Hári Kovács2, Silvio Pampiglione3, Maria Letizia Fioravanti3, István Kucsera1, Balázs Tánczos1, and László Tiszlavicz4 Department of Parasitology, National Center for Epidemiology, Budapest, Hungary 2 Department of Ophthalmology, University of Szeged, Hungary 3 Dipartimento di Sanitá Pubblica Veterinaria e Patologia Animale, Universitá degli Studi, Bologna, Italy 4 Department of Pathology, University of Szeged, Szeged, Hungary 1

Received June 13, 2007, accepted after revision January 14, 2008 © Springer-Verlag 2008

Humane Dirofilariose in Ungarn: eine in Zentraleuropa neu auftretende Zoonose Zusammenfassung. Einleitung: In den gemäßigten Regionen Europas, vorwiegend in Italien, Frankreich und Griechenland, und in den letzten Jahren auch in Ungarn, führte ein spezieller Wurm, die Dirofilaria (Nochtiella) repens, zu Infektionen beim Menschen und verursacht eine autochthone humane Dirofiariose. D. repens ist ein Parasit von Hunden, Katzen und einigen anderen Raubtieren, und wird durch Mücken übertragen. Wir berichten über einen weiteren Fall und fassen die bisher in Ungarn beobachteten Fälle zusammen. Patienten und Methoden: Die Autoren präsentieren einen Fall einer humanen Dirofilariose bei einem 56-jährigen Patienten mit Jucken und brennendem Gefühl in seinem rechtem Auge. Ein sich langsam bewegender, weißlicher, Zwirn-ähnlicher Wurm wurde durch Spaltlampenuntersuchung entdeckt. Die parasitologische Unter suchung identifizierte ihn als junge männliche Dirofilaria repens. Eine aktualisierte Übersicht über die ungarischen Fälle von 1880–2002 wird vorgestellt und zusätzlich 16 neuen Fälle analysiert, die in der Periode von 2001 zu 2006 diagnostiziert wurden. Das Durchschnittsalter dieser 16 neuen Patienten war 60 Jahre, acht Patienten hatten eine okulare, sieben eine subkutane Lokalisation. Bei einem Patienten mit akuter lymphatischer Leukämie wurde histopatologisch aus einem axillärem Lymphknoten diagnostiziert. Keiner der Patienten hatte sich im Ausland aufgehalten. Konklusion: Die Mehrheit der in Urgarn beobachteten Fälle von Dirofilariasis muss als autochthon aquiriert angesehen werden. Die zunehmende Zahl an diagnostizierten Fällen spricht dafür, dass diese Zoonose auch in Zentraleuropa Verbreitung erlangt. Summary. Introduction: In the temperate regions of Europe, mainly Italy, France, Greece, and in recent years Hungary, a specific filarioid worm, Dirofilaria (Nochtiella)

repens, a parasite of dogs, cats and some other carnivores, transmitted by mosquitoes, has occasionally been contracted, causing dirofilariosis in humans. We report a case of dirofilariosis and review all previously observed cases in Hungary. Materials, methods and results: The authors present a case of human subconjunctival dirofilariosis in a 56year-old man with mild itching and a burning sensation in his right eye. A slow-moving, whitish, thread-like worm was detected by slit-lamp examination. The worm was surgically removed and parasitological examination identified it as an immature male Dirofilaria repens. A review of Hungarian cases from 1880 to 2000 is presented, with updates of earlier reports. In addition, 16 new cases (8 men; 8 women) diagnosed between 2001 and 2006 are reviewed. The mean age of these 16 patients was 60 years; eight cases had ocular localization, seven were subcutaneous and one was diagnosed in a histopathological section of removed axillary lymph node in a patient with lymphoid leukemia. Twelve of the 16 identified Dirofilariae were females, four were males. According to their recorded histories the patients had not traveled internationally. Conclusion: Most of the above cases of dirofilariosis are certainly autochthonous infections. The increasing number of diagnosed cases suggests that this zoonosis is becoming more important in central Europe and that the incidence may increase with the improvement of clinical diagnosis. Key words: Dirofilaria repens, dirofilariosis, human, autochthony, subconjunctival, central Europe.

Introduction Zoonotic filarioidoses are common in humans. The majority of cases are caused by Dirofilaria spp. (Filarioidea, Onchocercidae), most frequently by Dirofilaria immitis, D. repens, D. tenuis and D. ursi. All the filariae known to have caused zoonotic infections have been

Szénási et al., Human dirofilariosis in Hungary

found to be natural parasites of mammals [1]. Dirofilaria (Nochtiella) repens is a habitual parasite of dogs, cats and other carnivores. Most frequently, it lives in the subcutaneous tissue (sometimes in the internal organs) of its host and is transmitted by mosquitoes (Culicidae). D. repens has only been found in the Old World, notably in some parts of southern Europe, Africa and Asia [2, 3]. The most affected countries are Italy, Sri Lanka and Russia, where more than a third of cases have been detected [3]. In Europe, dirofilariosis is definitely autochthonous in the Mediterranean countries [2–5]. Until 2006 it had not been detected in northern European countries, with the exception of extraordinary imported cases. The first obviously autochthonous dog dirofilariosis case in Germany was described by Hermosilla and coworkers in 2006 [6], proving that dirofilariosis is on the increase in Europe. Autochthony of human dirofilariosis in Hungary has long been suspected [7–9], although it has not been confirmed. We consider our first case of D. repens infection [10, 11] to be worth reporting in detail because it is the first human case in Hungary in which an intact, living specimen has been recovered and identified during thorough macroscopic and microscopic examinations. Furthermore, its autochthonous origin was traced and verified. We also offer a critical review of Hungarian cases up to the year 2000 that updates earlier reports [7, 8, 12]. In addition, 16 new cases were reported between 2001 and 2006, two of which were published [13, 14]. An increasing number of Dirofilaria cases described in recent medical and veterinary reports [15, 16], and also newly diagnosed cases at the Department of Parasitology, National Center for Epidemiology, support our opinion that dirofilariosis is an emerging zoonosis in Hungary and potentially in central Europe.

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Fig. 1. Subconjunctival nodule containing a whitish threadlike worm. Conjunctiva is injected

Presentation of a case In 2000, a 56-year-old man was referred to the Department of Ophthalmology at Szeged University Hospital with the diagnosis of “conjunctival tumor”. He had experienced a mild itching and burning sensation in his right eye for two or three days, but without severe pain, visual loss or other vision related symptoms. The man was a farmer living in close proximity to dogs, cats, pigs and also to stagnant water where mosquitoes were frequent during hot weather. He had not traveled abroad, except for a short trip to Vienna ten years previously. He did not have any history of visual disorder or complaints regarding his vision. During examination of the right eye, “red eye” was found without eyelid edema. The left eye was normal. The visual acuity of both his eyes was 1.0. Slit-lamp examination revealed a smooth transparent cornea, clear anterior chamber and lens. The nasal area of the conjunctiva of the right eye was injected. A subconjunctival nodule of approximately 4 x 3 x 2 mm in size was found in which a slow moving, whitish, thread-like worm was discerned. Brighter illumination resulted in more intense movements of the worm (Fig. 1). Ophthalmoscopy revealed clear transparent vitreous space and normal fundus. Ultrasonography (B scan) also

Fig. 2. A living whitish worm was removed intact from the nodule

showed clear vitreous space, normal thickness of the ocular wall and normal orbit echogram. Laboratory investigations: ESR and blood cell count were normal (no eosinophilia). No microfilariae were detected using the Knott concentration technique on blood samples taken and tested in the morning, at noon and in the evening. Radiologic and dermatologic examinations did not reveal other localization of nodules. The subconjunctival nodule was surgically excised under local anesthesia with cocaine. The living, moving helminth was removed intact and put first into physiological saline to make macroscopic observations and then into 70% ethyl alcohol. The wound was washed with povidone iodine and closed with 8/0 sutures. Wound healing was uneventful and perfect. Macroscopic examination revealed an intact, living, whitish, thread-like worm (Fig. 2), 45 mm in length, with a maximum thickness of 390 µm. The body was cylindrical with conoid ends and a corkscrew-like tail. The spec-

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Review of cases of human dirofilariosis in Hungary between 2001 and 2006

Fig. 3. Caudal part of D. repens. Two unequal spicula, caudal alae and cloaca are shown (Blue-lactophenol, x 100)

We diagnosed 16 cases (8 men; 8 women) of dirofilariosis caused by D. repens at the Department of Parasitology, National Center for Epidemiology (Budapest, Hungary) in the period 2001–06. The mean age of the men was 64 years; the women had a mean age of 57 years. Patients’ data and measured parameters of the Dirofilaria are summarized in Tables 1 and 2. D. repens was identified on the basis of the morphological characteristics and measured microscopic parameters of the intact worm and in the histopathological section. Eight of the 16 cases had ocular localization, seven were subcutaneous and one case was diagnosed in a histopathological section of removed axillary lymph node with lymphoid leukemia. Eosinophilia was found in one case. We used the Knott concentration technique for detection of microfilariae in ten cases, which yielded negative results. The epidemiological data of four patients was unavailable. Eight of the other 12 patients were living in close or general proximity to dogs and/or cats; four patients had no evident contact with animals. In their history no trips abroad had been recorded, except for patient ID No 69/01, who had traveled to the Ukraine (in 2000) and to Germany, Belgium and the Netherlands (in 2001). Analyses of the territorial distribution of these 16 cases showed that they were localized on the watershed of the Danube and Tisza River, and in one case in close proximity to Lake Balaton. Twelve of the 16 identified Dirofilariae were females and four were males.

Human dirofilariosis in Hungary between 1879 and 2000 Fig. 4. Transverse section of D. repens: external cuticular ridges (CR), lateral cords (LC), muscle fibers (M), testicule (T) and intestine (I) are evident (Periodic acid Schiff, x 350)

imen was made transparent with lactophenol. Microscopic examination revealed that the cuticle had external longitudinal ridges over the entire length of the body. A small apical mouth without lips was observed. Cephalic papillae were not visible. The length of the esophagus was 86 µm. Two unequal spicula, 145 and 450 µm long, were found. Pre- and post-cloacally, outlines of some caudal papillae were visible. The distance from the cloaca to the caudal end was 95 µm (Fig. 3). In transverse sections of the helminth, the big tubule (testicle) and the small tubule (intestine) were stained with periodic acid Schiff stain and Masson–Goldner trichromic stain, respectively. Cuticular ridges and muscle fibers were well evident. The ridges were separated from each other by 3–7 µm. The thickness of the cuticle was 12–14 µm. Lateral cords were also visible (Fig. 4). On the basis of the above data, it can be stated with certainty that a living immature male D. repens specimen was found in the subconjunctival nodule of our patient.

The autochthonous occurrence of D. repens infections in Hungary has long been suspected [7–9, 16] but has not been confirmed for several reasons: first, the identification of the parasite was somewhat uncertain, as either rigorous macroscopic and histological examinations were omitted or the veracity of their analysis was hindered by the necrotic condition of the parasite specimen; second, patients were not asked about their travel history and therefore the imported origin of the infection was not or could not have been excluded; third, criteria used for the classification of filarial species were not elaborated upon and the macroscopic and microscopic characteristics of the various filarial species were not properly determined. According to current scientific literature, Addario’s Filaria conjunctivae [5, 17] is considered to be D. repens, at least in the Old World. However, we may suppose that the helminth described as Filaria peritonei hominis by Babes [18, 19] in Budapest might also belong to the Dirofilaria species. This reasoning can be accepted on the basis of the drawings reported by Babes and on the interpretation of Desportes [20, 21]. Babes’ case was reported in 1879 and 1880, and preceded Addario’s paper by six years. Thus, we propose that Babes’ findings should be reconsidered and taken as the very first scientific report to document an infection due to D. repens in Hungary. In 1920, some four decades later, Béla Johan presented to Sándor Kotlán a worm that had been removed


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Table 1. Data of 16 Dirofilaria repens – positive patients diagnosed at the Department of Parasitology, NCE in the period 2001–2006 Year

Identification No.

Patients’ data Age (years)

Sex Locality/County

Describer/Author(s)/ [Reference]

Localization of the lesion, clinical symptoms

57

82

f

Adács/Heves

Pampiglione et al./ Kucsera et al. [33]

subconjunctival, left eye

69

50

m

Békéscsaba/Békés

Pampiglione et al.

subconjunctival

77

27

f

Szeged/Csongrád

Pampiglione et al.

subcutaneous, forearm

2002

45

56

m

Cegléd/Pest

Pampiglione et al.

subconjunctival

2003

No case

2004

2

61

m

Budapest

Kucsera et al.

subconjunctival

14

41

f

Tiszasas/JászNagykun-Szolnok

Kucsera et al.

subcutaneous, left axillary region

15

51

f

Vác/Pest

Kucsera/Pónyai et al. [14]

subcutaneous, intermittent, right forearm edema, urticaria

3499

81

m

Budapest

Kucsera et al.

subconjunctival

271

72

m

Szeged/Csongrád

Kucsera et al.

subconjunctival

1581

56

f

Kisköre/Heves

Kucsera et al.

subcutaneous, right forearm (st. post mammectomy)

3038

62

m

Budapest

Kucsera/Salomváry et al. [13]

ocular, left upper eyelid, edema

2291

62

f

Kaposvár/Somogy

Kucsera et al.

subcutaneous, right upper arm

3550

73

f

Felso´´göd/Pest

Kucsera et al.

subconjunctival

3953

78

m

Apaj/Pest

Kucsera/Kucsera et al. [34]

subcutaneous, forearm

4197

63

f

Békéscsaba/Békés

Kucsera et al.

axillary lymph-node, leukemia

6798

48

m

Hódmezo´´vásárhely/ Csongrád

Kucsera et al.

subcutaneous, upper arm

2001

2005

2006

m male; f female; NCE National Center for Epidemiology, Budapest.

from a woman’s subcutaneous nodule at a Budapest hospital. Kotlán pathologically and morphologically determined the specimen as belonging to the group Filaria conjunctivae [7]. This was the second possible instance of dirofilariasis in Hungary. In 1930 and 1935 Neuber described respective cases as bancroftian filariasis [22–24]. “Microfilariae” were identified, although Wuchereria bancrofti was not indisputably determined in these cases, as underlined by Kotlán [7]. Filarioid worms and “micro filariae” were identified in two further cases [25, 26] but the recognition of helminths was once again inconclusive. These latter four cases can in all probability be fairly excluded from the list of dirofilariases. In 1941, Anda [27] reported the first supposed incidence of “onchocercosis” in Hungary, although Makara and Mihályi [28] later doubted this diagnosis, asserting that the worm was not Onchocerca but rather Dirofilaria, possibly D. conjunctivae, an opinion accepted by Kotlán [7]. This case was possibly the third D. repens infection in Hungary. Kettesy observed the fourth probable case in the conjunctiva of a patient detailed by Makara and Mihályi [28]. The helminth was identified as D. immitis,

although the possibility of its being D. repens was not discounted. Case five was found by Ko´´hegyi and described by Kotlán [7] as Dirofilaria sp., and case six was described by Németh and Kugler [8], who in 1968 identified a helminth in the conjunctiva of a patient as D. repens. Case seven was described by Pampiglione et al. [12] in 1999, when a female D. repens was found in the spermatic cord of a rail worker, who had most likely contracted the infection in Italy. Case eight was described by Parlagi et al. [9], in which histological sections from the nodule of the right lower eyelid revealed cross sections of a male D. repens. A further four Hungarian cases, in which subcutaneous nodules were removed from a different part of the body of each patient, were reported by Elek et al. [29] in 2000. Histological examination of the nodules identified D. repens in all four cases. The subconjunctival case we reported in 2000 [10, 11] is the thirteenth D. repens infection in Hungary and the first in which a living D. repens was surgically removed intact. The autochthony of this case is indisputable on the basis of the morphology of the parasite and of the patient’s statement regarding his travels; namely, that he

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Szénási et al., Human dirofilariosis in Hungary Table 2. Parameters of the identified Dirofilaria

Identification No./year

Examined material

Sex

Length (cm)

Thickness Distance: (µm) anterior endvulva (µm)

57/2001 69/2001 77/2001 45 /2002 2/2004 14/2004 15/2004 3499/2004 271/2005 1581/2005 3038/2005 2291/2006 3550/2006 3953/2006 4197/2006 6796/2006

Worm Worm HP section HP section Worm HP section HP section Worm Worm HP section Worm HP section Worm Worm HP section HP section

f f f f f m f f f m f m m f f f

11.5 10.5

600 490 500 375 500 250 450 350 525 536 328 500 340 540 475 463

10.5

11 9.5 5 10

Distance: cloaca-caudal end (µm)

1900 1500

2050

Thickness of the cuticle (µm)

Cuticular ridges separated from each other (µm)

16–21 15–22 13–18 13–16

8–12 8–12 8–12 9–15 9–10 5–7 9–10 10–14 11–15 10–14 12–18 7–11 8–10 8–12 10–12 20

60 13–15 11–14

1700 2250

70 75

1900

87

2000

88 44

15–19 15–16

15–18 18–22

m male; f female; HP histopathological.

had never left the country, except for a short trip to Vienna ten years previously. The specimen was an immature male D. repens. Accordingly, the infection must have been acquired a few months earlier, in the summer of 2000, and therefore could not have been an imported case. A review of (more or less) confirmed human dirofilariosis in Hungary between 1879 and 2000 is given in Table 3. We have noted six probable but not confirmed cases of Dirofilaria (repens?) infection during the more than one hundred years that followed the first of Babes’ cases [18, 19]. In contrast, seven cases have been published [9–12, 29] between 1999 and 2000, all of them confirmed as D. repens infections. In addition, 16 other dirofilariosis cases were diagnosed at the Department of Parasitology, National Center for Epidemiology, Budapest, in the period 2001–06; the mean age of these 16 patients was 60 years. This higher incidence in the elderly corresponds to data in the literature [21]. We used the Knott concentration technique for detection of microfilariae in ten cases, and the results were negative. Microfilariae are not usually present in the peripheral blood of patients: they have only once been reported in the peripheral blood of a patient with a history of previous malignant neoplasia [2, 13]. Twelve out of 16 identified Dirofilariae were female and four were male. This marked prevalence of females corresponds to data in the literature [2]. The differential diagnosis from the other filaria species that occur in humans is not required in these cases, since the patients’ histories do not contain any data to indicate such a possibility. Based on the available epidemiological data, it can be concluded that most of these cases are autochthonous infections (Tables 1, 2).

Dirofilariosis of dogs in Hungary In relation to canine infections with Dirofilaria spp., out of approximately 35,000 autopsies on dogs since 1958, not one case has been found (pers. comm. F. Vetési, 1998). The first autochthonous D. repens infection of a dog was described in Hungary in 1998 by Fok et al. [30]. This was rapidly followed by a report [31] of two further canine cases associated with D. repens. The autochthony of these cases was stated by their authors, who screened 101 dogs from the relevant catchment areas. Screenings revealed that 9% of the dogs were infected with D. repens. Preliminary results of the epidemiological surveys started in 2005 by Fok et al. [16, 32] showed that 116 of 826 (14%) samples of dog blood and 2 of 29 (7%) samples of cat blood tested positive for D. repens microfilariae. Territorial distribution showed that most of the animals that tested positive were found on the watershed of the Danube and Tisza River, with the exception of one animal found in close proximity to Lake Balaton. This result closely corresponds with our findings in human dirofilariosis cases. Visiting or living near riverbanks where mosquitoes are abundant appears to be a significant risk factor in contracting the infection. These veterinary reports complete and confirm our opinion that dirofilariosis is an emerging zoonosis in Hungary.

Conclusion Several factors may contribute to the apparent increase in observed cases of human and canine dirofilariosis recently reported in Hungary and in other European countries: better knowledge of distinctive features of the parasite in microscopical sections and of its clinical as-


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Table 3. Human dirofilariosis in Hungary between 1879 and 2000 No.

Date

Patients’ data Age (in years)

Sex

Locality/County

Describer/Author (s)/ [Reference] Babes [18, 19]

1

1879

–

f

Budapest

2 3

1920 1941

– 41

f f

Budapest –

4 5

1942 1951

– –

m –

Debrecen/Hajdú-Bihar –

6 7 8 9 10 11

1968 1999 2000 2000 2000 2000

21 37 57 52 48 64

m m f f m f

12 13

2000 2000

76 56

f m

Budapest Budapest Budapest Budapest Hódmezo´´vásárhely/Csongrád Szegilong/Borsód-AbaújZemplén Csobaj/Borsód-Abaúj-Zemplén Elek et al. [29] Szeged/Csongrád Szénási et al. [10], Hári Kovács et al. [11]

Localization of the lesion

ligamentum gastrosplenicum Kotlán [7] subcutaneous Anda [27], Makara, subcutaneous, temporal Mihályi [28] region Kettesy/Makara, Mihályi [28] subconjunctival Ko´´hegyi/Kotlán [7] subcutaneous, temporal region Németh, Kugler [8] subconjunctival Pampiglione et al. [12] spermatic cord Parlagi et al. [9] ocular, right lower eyelid Elek et al. [29] eyelid Elek et al. [29] subcutaneous, brow Elek et al. [29] subcutaneous, back subcutaneous, upper arm subconjunctival

m male; f female.

pects; increased tourism with pets; increased number of dogs and cats kept as pets; a significant number of recent publications drawing the attention of the medical community to the diagnostic probability of dirofilariosis; and climatic change, the spread of the “greenhouse effect” leading to the extension of the Mediterranean climatic belt to the north, giving better opportunity for both vectors (mosquitoes) and filarias to thrive and spawn infection. The increasing number of diagnosed cases suggests that direct attention must be paid to this zoonosis, since its incidence may rise with the improvement of clinical diagnosis.

References 1. Orihel TC, Eberhard ML (1998) Zoonotic filariosis. Clin Microbiol Rev 11: 366–381 2. Pampiglione S, Canestri Trotti G, Rivasi F (1995) Human dirofilariosis due to Dirofilaria (Nochtiella) repens: a review of world literature. Parassitologia 37: 149–193 3. Pampiglione S, Rivasi F (2000) Human dirofilariosis due to Dirofilaria (Nochtiella) repens: an update of world literature from 1995 to 2000. Parassitologia 42: 231– 254 4. Muro A, Genchi C, Cordero M, Simón F (1999) Human dirofilariosis in the European Union. Parasitol Today 15: 386–389 5. Auer H (2004) Die Dirofilariose des Menschen – Epidemiologie und Nosologie einer gar nicht so seltenen Parasitose in Österreich. Denisia 13: 463–471 6. Hermosilla C, Pantchev N, Dyachencko V, Gutmann M, Bauer C (2006) First autochthonous case of canine ocular Dirofilaria repens infection in Germany. Veterinary Record 158: 134–135

7. Kotlán A (1951) On a new case of human filarioidosis in Hungary. Acta Vet Acad Sci Hung 1: 69–79 8. Németh B, Kugler S (1968) Ophthalmo-filariosis (Ophthalmo-filariosis). Orvosi Hetilap 109: 195–197 9. Parlagi G, Sumi Á, Elek G, Varga I (2000) Orbital dirofilariosis (Szemüregi dirofilariosis). Szemészet 137: 105– 107 10. Szénási Z, Hári Kovács A, Tiszlavicz L, Kolozsvári L, Nagy E (2000) Human ophthalmo-filarioidosis (Humán ophthalmo-filarioidosis). A Magyar Zoonózis Társaság Kiadványa, pp 124–130 11. Hári Kovács A, Szénási Z, Tiszlavitz L, Kolozsvári L, Pampiglione S, Fioravanti ML (2002) A new case of ocular filarioidosis in Hungary (Ophthalmo-filarioidosis újabb esete Magyarországon). Szemészet 139: 87–90 12. Pampiglione S, Elek G, Pálfi P, Vetési F, Varga I (1999) Human Dirofilaria repens infection in Hungary: a case in the spermatic cord and a review of the literature. Acta Vet Hung 47: 77–83 13. Salomváry B, Korányi K, Kucsera I, Szénási Z, Czirják S (2005) A new case of ocular dirofilariosis in Hungary (Szemüregi dirofilariosis újabb esete Magyarországon). Szemészet 142: 31–35 14. Pónyai K, Wikonkál N, Bottlik G, Hársing J, Kucsera I, Horváth A, et al (2006) Dirofilaria repens infection case in Hungary: a case report. J Dtsch Dermatol Ges 4: 1051– 1053 15. Farkas R (2003) Dirofilariosis in Hungary (Abstract). Helminthologische Fachgespräche – Helminthological Colloquium, Klinisches Institut für Hygiene und Medizinische Mikrobiologie, Wien, November 2003, Abstract book p 13 16. Fok É (2007) The importance of dirofilariosis in carnivores and humans in Hungary, past and present. Dirofi-

102


laria immitis and D. repens in dog and cat and human infections. Mappe parassitologiche 8: 181–188 17. Addario C (1885) About an ocular nematode in human (Su di un nematode dell’occhio umano). Ann Ottalmol 14: 135–147 18. Babes V (1879) Ueber einen neuen Parasiten des Menschen. Med Chir Centralblatt Wien 14: 554 19. Babes V (1880) Ueber einen im menschlichen Peritonäum gefundenen Nematoden. Arch Pathol Anat Physiol Klin Med (Hrsg R Virchow) 81: 158–165 20. Desportes C (1939/1940) Filaria conjuntivae Addario, 1885, parasite accidental de l’homme, est un Dirofilaria. Ann Parasitol Hum Comp 17: 380–404, 515–532 21. Pampiglione S, Rivasi F, Angeli G, Boldorini R, Incensati RM, Pastormerlo M, et al (2001) Dirofilariosis due to Dirofilaria repens in Italy, an emergent zoonosis: report of 60 new cases. Histopathology 38: 344–354 22. Neuber E (1930) Data to the pathology and epidemiology of Filaria sanguinis hominis (Adatok a Filaria sanguinis hominis pathologiájához és epidemiologiájához). Orvosi Hetilap 74: 53–59 23. Neuber E (1930) A case of filariosis healed to gold- and malaria-therapy (Arany-és maláriatherapiára gyógyult filariosis). Orvosi Hetilap 74: 862–864 24. Neuber E (1935) Data to the diagnostics, epidemiology, and therapy of filariasis (Filaria bancrofti), in connection with two cases [A filariasis (Filaria bancrofti) kórhatározásához, járványtanához és gyógykezeléséhez, két eset kapcsán]. Orvosképzés 25: 205–216 25. Bokrétás A (1932) Filariasis (A filariasisról). Orvosi Hetilap 76: 813–815 26. Szél J (1942) A case of Filaria sanguinis (Filaria sanguinis esete). Orvosi Hetilap 86: 502–503 27. Anda T (1941) The first case of onchocercosis in Hungary (Az onchocerkózis elso´´ esete Magyarországon). Orvosi Hetilap 85: 331–333

28. Makara G, Mihályi F (1943) Insects and Diseases (Rovarok és betegségek). Magyar Orvosi Könyvkiadó Társulat Budapest, pp 157–159 29. Elek G, Minik K, Pajor L, Parlagi G, Varga I, Vetési F, et al (2000) New human dirofilarioses in Hungary. Path Oncol Res 6: 141–145 30. Fok É, Szabó Z, Farkas R (1998) First Hungarian case of Dirofilaria repens infection diagnosed during surgical action in dog (Dirofilaria repens ferto´´zöttség elso´´ hazai diagnosztizálása kutyában sebészeti beavatkozás során). Kisállatorvoslás 4: 218–219 31. Széll Z, Sréter T, Csikós K, Kátai Z, Dobos-Kovács M, Vetési F, et al (1999) Autochthonous Dirofilaria repens infection in dogs (Autochton Dirofilaria repens ferto´´zöttség kutyákban). Magyar Állatorvosok Lapja 121: 100–104 32. Fok É, Kiss G, Majoros G, Jacsó O, Farkas R, Gyurkov szky M (2007) Preliminary results of an epidemiological survey on dirofilariosis of dogs and cats in Hungary. Dirofilaria immitis and D. repens in dog and cat and human infections. Mappe parassitologiche 8: 195–196 33. Kucsera I, Elek I, Danka J, Fok É, Varga EB, Birnbaum I, et al (2004) Ocular filarioidosis – case report. Meeting of the Hungarian Society of Microbiology, October 8–10, 2002, Balatonfüred, Hungary; Abstract, Acta Microbiol Immunol Hung 51: 185 34. Kucsera I, Szénási Zs, Danka J (2007) Review of human dirofilariosis diagnosed at the Department of Parasitology, National Center for Epidemiology, Budapest, Hungary. Dirofilaria immitis and D. repens in dog and cat and human infections. Mappe parassitologiche 8: 197 Correspondence: Zsuzsanna Szénási, Dr. Biol, PhD, Department of Parasitology, National Center for Epidemiology, P.O.Box 64, 1966 Budapest, Hungary, E-mail: szenasizs@oek. antsz.hu