AN OUTBREAK OF SIMULIUM ERYTHROCEPHALUM (DE GEER, 1776) IN THE REGION OF NOVI SAD (SERBIA) IN 2006

At entomologi seri, Supplement, 2006, 97-114 UDC 595.771 (497.113 Novi Sd) : 616.98 AN OUTBREAK OF SIMULIUM ERYTHROCEPHALUM (DE GEER, 1776) IN THE REGION OF NOVI SAD (SERBIA) IN 2006 ALEKSANDRA IGNJATOVIĆ-ĆUPINA 1, MARIJA ZGOMBA 1, LJUBA VUJANOVIĆ 2, ALEKSANDRA KONJEVIĆ 1, DUŠAN MARINKOVIĆ 1, AND DUŠAN PETRIĆ 1 1 University of Novi Sd, Fulty of Agriulture, Deprtment of Environment nd Plnt Protetion, Lortory of Medil nd Veterinry Entomology, 21000 Novi Sd, Seri 2 Clinil Center of Vojvodin, Deprtment for Dermtology nd Venereology, 21000 Novi Sd, Seri ABSTRACT During the pst dedes, Simulium (Boophthor) erythroephlum (De Geer, 1776) proved to e n extremely ggressive nthropophili lkfly speies in the provine of Vojvodin, Seri. Prior to 2006, lst outreks in Vojvodin oured fter severe flooding of the Dnue nd the Tisz River in the springs of 1965 nd 1970. The extremely elevted level of the Dnue in the spring of 2006 (whih exeeded the verge perennil vlues for the lst sixty yers) nd old wether t the time reted suitle onditions for nother outrek of S. erythroephlum. Situted on oth nks of the Dnue, the ity of Novi Sd with numerous villges in the viinity represents prtiulrly endngered region. The undne of dult popultions of lkflies ws reorded on weekly sis y dry ie-ited trps. Positive ptures were reorded t 26 out of 28 lolities during the seson of the outrek. Estimtion of the iting risk ws lulted for eh trpping result. The presene of dult S. erythroephlum femles ws ontinully reorded in trps during the seson from April to mid July. Periods with frequent ses of elevted iting risks extended from April to the end of June. Reorded linil ses of ptients suffering from ites were in orreltion with the periods of elevted risk of eing itten y S. erythroephlum. The mjority of ites were reorded elow the knees, whih reflets the typil iting hit of this speies. KEY WORDS: Simuliide, lk flies, Simuliium erythroephlum, outrek, linil ses

98 A. IGNJATOVIĆ-ĆUPINA ET AL. INTRODUCTION On the sis of the numer of speies with the potentil for mssive reprodution, the frequeny of outreks of different lkfly speies, nd onsequent enormous dmge during the lst entury, Seri nd espeilly the provine of Vojvodin n e onsidered s one of the most endngered prts of Europe (ŽKOVIĆ, 1970; ŽKOVIĆ AND BURÁNY, 1972). Outreks of Simulium (Simulium) olomshense (Sopoli, 1780) were reorded severl times during the lst entury in Seri, in 1923, 1934, nd 1950, these outreks using out 2300, 11000, nd 800 deths, respetively, mong domesti nimls (mostly ttle) (SIMIĆ AND ŽKOVIĆ, 1958). Simulium (Byssodon) multum (Meigen, 1804) used nuisne nd the loss of severl hundred hikens in the distrit of Bnt (Vojvodin) in 1958 (ŽKOVIĆ, 1958). During the outreks of Simulium (Boophthor) erythroephlum (De Geer,1776) in 1965 nd 1970 in the provine of Vojvodin, numer of people suffered from ite onsequenes, prtiulrly in 1970, when more thn 2000 linil ses were reorded (ŽKOVIĆ, 1967; ŽKOVIĆ AND BURÁNY, 1972; BURÁNY ET AL., 1972). Erlier studies in the ountry onfirmed tht mong 16 lkfly tx tht suk the lood of domesti nimls, the following ones ite humns s well: S. multum, Simulium orntum (s.l.) [proly Simulium (Simulium) orntum Meigen, 1818 (omplex)], Simulium (Simulium) reptns (Linneus, 1758), S. olomshense nd S. erythroephlum (ŽKOVIĆ, 1970). Reent studies showed tht the most undnt speies in the region of Novi Sd (provine of Vojvodin) re S. orntum (omplex), S. erythroephlum, nd Simulium (Wilhelmi) lnium (Enderlein, 1924) (IGNJATOVIĆ-ĆUPINA ET AL., 2003). In ll of these speies nthropophili preferene hs een reognized (IGNJATOVIĆ-ĆUPINA ET AL., 2006). Extensive investigtion of lkfly reeding sites in the region onfirmed tht the lrgest reeding sites of S. erythroephlum nd S. lnium re in the Dnue River (IGNJATOVIĆ-ĆUPINA, 2003). Their immture stges were found only osionlly in smller wter ourses of the region. On the other hnd, S. orntum (omplex) represents the dominnt lkfly txon in strems of the Frušk Gor Hills, ut it hs never een found in the Dnue. Simulium erythroephlum ws desried s highly ggressive speies, one with remrkle nthropophili preferene (ŽKOVIĆ, 1970; ROSECCHI, 1978). Although femles of this speies ttk in mssive swrms nd the list of hosts inludes rnge of irds nd mmmls, deths of domesti nimls were not reorded in the pst (ŽKOVIĆ, 1971). Femles of S. erythroephlum generlly ite prts of the ody poorly overed y hir (usully the hed nd ventrl ody prts) in ttle nd unovered ody prts, mostly the legs, in humns (ŽKOVIĆ, 1967, 1970). Consequenes of ites n e very severe, depending on the numer of ites nd individul sensitivity of the host (KRSTIĆ, 1966; BURÁNY ET AL., 1972). In some ses, itten people required speil medil re. The onsequenes of ites re prtiulrly pinful nd irritting, expressed s serious dermtitis with utneous hemorrhgi lesions, edem, nd ithing tht n persist for rther long period. These symptoms re sometimes followed y ferile onditions, exhustion, or other less serious onsequenes (KRSTIĆ, 1966; ŽKOVIĆ AND BURÁNY, 1972; BURÁNY ETAL., 1972; ROSECCHI, 1978). Lowlnd rivers with muddy or sndy ottoms, low or moderte urrent veloity, nd low oxygen ontent hve een desried s typil reeding sites of S. erythroephlum (ŽKOVIĆ, 1971; ROSECCHI, 1978). Within the frontiers of former Yugoslvi, reeding sites of this speies were deteted in the Drv River in Croti nd in the Dnue nd its triutries (the Tisz, Tmiš,

Outrek of Simulium erythroephlum 99 Krš, nd Krši Rivers) nd few smll wter ourses in Seri (ŽKOVIĆ, 1967, 1969). Despite frequent reords of S. erythroephlum, the popultion density of immture stges in the prt of the Dnue pssing through the Pnnonin plin ws usully lower thn in some other smller wter ourses. It ws lso reorded tht the speies is of lesser undne ompred to some other speies tht reed in the Dnue (ŽKOVIĆ, 1967; 1971). Reent extensive studies of lkfly reeding sites demonstrted tht S. erythroephlum is the dominnt lkfly speies in the setion of the Dnue River flowing through the region of Novi Sd. Highly undnt popultions of immture stges of this speies hve een reently deteted in the Dnue, ut immture stges were lso found in smll ffluent strem, outside the min reeding sites (IGNJATOVIĆ-ĆUPINA, 2003). High nd onstntly rising wter levels nd old riny wether during the spring nd first hlf of summer represent suitle eologil preonditions for outreks of S. erythroephlum. Coinidene of suh hydrologil nd eologil ftors ourred in Seri fter severe flooding of the Dnue nd Tisz Rivers in 1965 nd 1970. Mssive pperne of dults of this speies nd ggressive iting of humns were then reorded in settlements long those rivers (ŽKOVIĆ, 1967, 1971; ŽKOVIĆ AND BURÁNY, 1972). Suitle hydrologil nd eologil onditions reppered during the spring of 2006, entiling enhning new outrek of this lkfly speies. Approximtely 122,500 hetres of lnd in Seri were flooded, 112,000 h were ffeted y high levels of underground wter, nd 5,500 h were ffeted y lndslides. With 50,000 h of flooded lnd, the southern prt of the Bčk distrit (where the region of Novi Sd is loted) represented one of the most endngered prts of the provine of Vojvodin. Until the spring of 2006 our ttempts to otin offiil moridity dt of lkfly ites on humns were unsuessful, sine no reords of the kind were kept y medil institutions in the region. An inresing numer of itten ptients seeking medil help ws reorded in the region of Novi Sd strting from April 2006. Suh sitution imposed the need for more reful pproh to the identifition of ite symptoms nd loser ollortion etween entomologists nd medil experts. MATERIAL AND METHODS The region of the ity of Novi Sd (ltitude: 45 o 18 N; longitude: 19 o 51 E; ltitude: 76-84 m) is situted on the nks of the Dnue River, whih divides it into two prts: the flt northern prt on the left nk of the Dnue nd the rolling southern prt on the slopes of the Frušk Gor Hills on the river s right nk. Smples of dult lkflies were olleted using dry ie-ited trps of the NS-2 type (PETRIĆ ET AL., 2000). This type of trp, sed on ron dioxide s non-speifi ttrtnt for loodsuking insets, hs een employed for more thn dede in monitoring dult mosquito popultions nd hs proved effetive in monitoring lkfly popultions s well (ĆUPINA ET AL., 2002). The trps were employed t weekly intervls during the seson from April to Septemer of 2006, strting when the verge dily temperture exeeded 10 o C for ontinul period of 10 dys.

100 A. IGNJATOVIĆ-ĆUPINA ET AL. They were set up from the fternoon to the following morning. The hosen sites were usully shded ples round trees or shrus out 1,5 m ove the ground nd lwys in the sme predetermined position. Lotion of the trps ws 28 sites ll over the region of Novi Sd: 15 trps were situted t sites long the right nk of the Dnue inluding the villges on the slopes of the Frušk Gor Hills, nd 13 were loted on the left nk of the Dnue, inluding the urn re. All trps were set up in the sme ples s during three previous sesons of monitoring. Cptured dults were preserved nd identified on the sis of their morphologil fetures. Speimens were ompred with dults rered from immture stges nd identified ording to desriptions given in ville identifition keys (KNOZ, 1965; DAVIES, 1968; ROSECCHI, 1978; YANKOVSKY, 2000). Aundne of dult popultions of S. erythroephlum during the lst four sesons (2003-2006) ws ompred nd disussed in reltion to ir temperture nd flutution of the level of the Dnue River. Offiil dt were provided y the RHSS [Repuli Hydrometeorologil Servie of Seri (http://www.hidmet.sr.gov.yu)]. Estimtion of the risk to humns of eing itten ws sed on pture results for eh lolity, ording to the previously proposed sle (IGNJATOVIĆ-ĆUPINA ET AL., 2006). Critil vlues for the numer of S. erythroephlum femles in trp were defined for eh tegory of iting risk. The risk of eing itten y this lkfly speies ws deemed moderte if 3-9 femles were trpped, high if 10-21 femles were trpped, very high if 22-40 femles were trpped, nd extremely high if 41 or more femles were ught in the trp, representing 1-2, 3-5, 6-10, nd 11 or more possile ites on humns during five hours of fternoon exposure, respetively. Clinil ses of lkfly ites on humns were reorded t the Clinil Center of Vojvodin, Deprtment of Dermtology nd Venereology during the 2006 seson. Aville dt for eh ptient onsisted of the dte of ptient reeption, the ple (lolity within the region) where ites possily ourred, the numer of ites, nd the ody prt itten. The reorded dt of linil ses were ompred with the expeted sitution estimted on the sis of trp smple size. The results were sttistilly proessed nd nlyzed using the SPSS sttistil pkge, version 10, for ANOVA nlysis. RESULTS AND DISCUSSION Adults of the following three lkfly speies with previously onfirmed mmmophili ehvior were ught in dry ie-ited trps in the region of Novi Sd during the 2006 seson: S. orntum (omplex), S. erythroephlum, nd S. lnium. Adults of other speies Simulium (Eusimulium) velutinum (Sntos Areu, 1922), Simulium (Eusimulium) ureum (Freis, 1824) Simulium (Nevermnni) lundstromi (Enderlein, 1921) nd Simulium (Wilhelmi) equinum (Linneus, 1758) were ptured rrely nd in signifintly lower numers. Simulium erythroephlum ws the most undnt speies in the region of Novi Sd in 2006 (Fig. 1). Femles of this typilly Dnuin speies were ontinully ught in trps from the eginning of April to mid-july. After this period, the presene of dults ws not reorded until the end of Septemer, when only few speimens were ptured in trps.

Outrek of Simulium erythroephlum 101 Signifintly higher numers of femles were reorded in the first nd seond week of April, third nd fourth week of My, nd seond nd third week of June, inditing mssive emergene of three genertions in the spring of 2006. 550 500 450 Numer of femles in trps 400 350 300 250 200 150 100 50 0 April I I My I I June I I Simulium (Wilhelmi) lnium (Enderlein, 1824) July I I August I I Septemer I Simulium (Simulium) orntum Meigen, 1818 (omplex) Simulium (Boophthor) erythroephlum (De Geer, 1776) I Figure 1. Sesonl ourrene of most undnt mmmophili lkfly speies ught in dry ieited trps in the region of Novi Sd during the 2006 seson. Sesonl tivity of S. lnium ws similr to tht of S. erythroephlum, ut the former speies ws reorded in signifintly lower numers, inditing tht eologil onditions during the 2006 seson were not quite dequte for its reprodution. Simulium orntum (omplex) ws reorded from the first dys of April until the eginning of August. The low popultion density of this usully very undnt speies in the region ws onsequene of well trgeted lrviide tretments of their reeding sites. Compring ir tempertures during the lst four yers (Fig. 2), we notied tht during the period from Mrh to July 2006, when mssive emergene of dults of S. erythroephlum ourred, verge monthly tempertures were not signifintly different from those reorded in the sme months during the two previous yers (2004 nd 2005). At the sme time, the verge monthly tempertures in 2006 were quite similr to the perennil vlues lulted for the period 1961-1990.

102 A. IGNJATOVIĆ-ĆUPINA ET AL. 30 2003 temperture ( oc ) 25 20 15 10 2004 2005 2006 verge 1961-1990 5 0-5 -10 Jnury Ferury Mrh April My June July August Septemer Otoer Novemer Deemer,, Dunn s multiple rnge test (p=0.05) Figure 2. Averge monthly tempertures in Novi Sd during the yers 2003-2006 nd verge vlues for the period 1961-1990 (dt soure: RHSS). During the spring nd summer of 2003, signifintly higher verge monthly tempertures thn those reorded in the following yers (2004-2006) were oserved in My, June nd August. Sine temperture dt for the spring of 2006 nd the period 1961-1990, do not differ signifintly, it n e stted tht ir temperture during the ongoing 2006 seson ws not n exlusive ftor induing the mssive pperne of S. erythroephlum, eing not signifintly different from those reorded during previous sesons, when no outreks of this lkfly speies were reorded. Permnently high levels of the Dnue River nd onseutive periods of severe flooding hrterized the spring of 2006. During the period from Mrh to June, the verge monthly levels of the Dnue signifintly exeeded the perennil vlues nd those reorded during the previous three yers (Fig. 3). At wter level ove 250 m, the Dnue egins to flood in the region of Novi Sd. In view of this ft, the period from Mrh to July of the lst three yers (2004-2006) n generlly e onsidered s period of high floods. A prtiulrly high wter level hrterized the spring nd erly summer of 2006. Flutution of the Dnue proved to hve n importnt influene on the popultion density of S. erythroephlum, s ws demonstrted over the lst four sesons of our reserh (Figs. 4 nd 5). In onditions of low wter in 2003, the popultion density of S. erythroephlum ws generlly low thoroughout the entire seson (Fig. 4). The highest numer of femles (42) ws reorded

I Outrek of Simulium erythroephlum 103 800 700 d 2003 2004 2005 2006 verge 1946-2000 600 500 d d wter level (m) 400 300 200 100 d d 0 Jnury Ferury Mrh April My June July August Septemer Otoer Novemer Deemer,,,d Dunn s multiple rnge test (p=0.05) Figure 3. Averge monthly levels of the Dnue t Novi Sd during the yers 2003-2006 nd verge vlues for the period 1946-2000 (dt soure: RHSS). 800 100 wter level (m) 700 600 500 400 300 200 100 90 80 70 60 50 40 30 20 10 totl numer of femles in trps totl numer of speimens in 2003 totl numer of speimens in 2004 wter level in 2003 wter level in 2004 0 0 Jnury I I Ferury I VI Mrh I I April I I My I VI June I I July I I August I VI Septemer I I Otoer I VI Novemer I I Deemer I V Figure 4. Sesonl flututions in the level of the Dnue River t Novi Sd (dt soure: RHSS) nd trpping of Simulium erythroephlum in 2003 nd 2004.

I 104 A. IGNJATOVIĆ-ĆUPINA ET AL. in mid-my, while lter in the seson the permnently low wter level diminished the popultion density of susequent genertions. Only 76 speimens of S. erythroephlum were ught in trps in 2003, representing only 2.56% of the totl numer of speimens of S. erythroephlum ptured over the lst four yers (2003-2006). wter level (m) 800 700 600 500 400 300 200 600 550 500 450 400 350 300 250 200 150 totl numer of femles in trps totl numer of speimens in 2005 totl numer of speimens in 2006 wter level in 2005 wter level in 2006 100 0 100 50 0 Jnury I I Ferury I VI Mrh I I April I I My I VI June I I July I I August I VI Septemer I I Otoer I VI Novemer I I Deemer I V Figure 5. Sesonl flututions in the level of the Dnue River t Novi Sd (dt soure: RHSS) nd trpping of Simulium erythroephlum in 2005 nd 2006. Wter level onditions on the Dnue were more suitle for the development of S. erythroephlum in 2004 thn in 2003, ut despite frequent ptures, no more thn 40 speimens of S. erythroephlum were ptured t ny of the smpling times (Fig. 4). The wter level ws permnently higher thn 250 m thoroughout lsting long period from the 21st of Mrh to the 3rd of August, nd higher numers of ptured femles were reorded, in June nd July. The reltively smll numer of femles ptured in 2004 ws onsequene of low popultion density of S. erythroephlum in 2003 nd the time needed for reovery of the popultion. The orretness of suh n ssertion is supported y results otined in monitoring of immture stges t the reeding sites. However, the numer of speimens of S. erythroephlum in ptured trps ws higher in 2004 thn in 2003. A totl of 130 femles were ught in 2004, representing 4.37 % of speimens reorded during the period 2003-2006. Sesonl vlues of the Dnue s wter level in 2005 were signifintly higher thn in 2004 nd 2003 (Fig. 5). The solute sesonl mximum (570 m) ws reorded on the 6th of April, while severl peks of levels higher thn 400 m were registered lter during the seson. Cptures in trps were reorded from the end of April, the pek eing reorded during the seond hlf of My, fter period with wter levels ove 450 m. The highest pture results were otined on the 24th of My (145 femles in trps). Higher pture vlues were hieved gin t the eginning of August, fter the flooding tht ourred in July.

Outrek of Simulium erythroephlum 105 It ws ovious tht suitle wter level onditions in 2005 enhned the development of S. erythroephlum, s is indited y the higher numer of speimens ught in trps during tht yer (398 speimens or 13.39% of the totl numer of ptured speimens in the period 2003-2006) thn during the two previous yers. The high survivl rte of the overwintering genertion, together with optiml sesonl onditions (espeilly high wter levels) during the following seson, led to the outrek of S. erythroephlum in 2006 (Fig. 5). An extremely high level of the Dnue ws reorded from the 9th to the 19th of April, when threshold of 700 m (defined s the seond flood lert level for the ity of Novi Sd) ws exeeded. The solute monthly mximum for April for the period 1946-2000 (654 m) ws surpssed for period of 19 dys (from the 8th to the 26th of April 2006). Prtiulrly high numers of femles in trps were reorded fter the wter level of 450 m ws exeeded in April, My, nd June. The highest numer of ptured femles (548 speimens) ws reorded on the 25th of My, in the sme period s in the previous yer. The inrese in the level of the Dnue tht ourred in August hd no influene on prodution of undnt popultions. Altogether, 2,369 speimens of S. erythroephlum were ught in trps during the 2006 seson, whih represented 79,68% of the totl numer of individuls ptured over the lst four sesons. Correltion etween high levels of the Dnue nd Tisz Rivers nd mssive pperne of S. erythroephlum ws reported y previous reserhers (ŽKOVIĆ, 1967; BURANY ET AL., 1972; ŽKOVIĆ AND BURANY, 1972), ut it ws not possile on the sis of their results to estlish the pproximte threshold wter level ple of induing lmitous outrek on the setion of the Dnue flowing thorough the region of Novi Sd. Comprison of sesonl flututions in the level of the Dnue in the region of Novi Sd during the sesons of 2003 to 2006 demonstrted tht the inresingly frequent ourene of wter level ove 250 m during spring nd erly summer led to the pperne of higher popultion density of S. erythroephlum. If the period of high wter levels ove 450 m persists during spring nd erly summer, undnt dult popultions n e expeted in the following period. Lter inrese of the wter level, s reorded in August nd Septemer of 2005 nd 2006, hd no influene on inrese in the numer of dults of this speies. Cpture of dults of S. erythroephlum in trps during the 2006 seson ws reorded t 26 of the 28 investigted lolities: t 14 lolities situted on the right nk nd 12 on the left nk of the Dnue (Fig. 6). In 2006, lolities situted on oth the right nd left nks of the Dnue were sujeted to elevted iting risk: moderte, high, very high, or extremely high (Tle 1). Higher numers of femles nd onsequent higher iting risk were, s rule, lwys reorded in the prt of the region situted on the right nk of the Dnue. Elevted risk to humns of eing itten ws judged to exist t 22 lolities: t ll lolities on the right side of the river nd eight out of 12 on the left side. Cpture results vried depending on the period of the seson nd the position of the trp. Numerous ses of elevted iting risk were reorded in the period from the first week of April to the seond week of July, while lter on only few speimens were ught in trps. The highest sesonl numer of femles in trp (336 speimens) ws reorded t the Ledini villge 1 lolity

106 A. IGNJATOVIĆ-ĆUPINA ET AL. 1 2 15 3 4 5 16 17 20 7 6 21 18 19 9 8 22 10 23 11 12 13 14 24 25 26 Right Dnue nk: 1. Sremski Krlovi 2. Bukov 3. Petrovrdin Sdovi 4. Petrovrdin villge 5. Petrovrdin Dnue 6. Sremsk Kmeni 7. Popovi 8. Ledini villge 1 9. Ledini villge 2 10. Šndrov 11. Rkov villge 12. Rkov Dnue 13. Beočin villge 14. Beočin Dnue Left Dnue nk: 15. Kovilj Mrsh 16. Suić 17. Novi Sd Dunvski Prk 18. Novi Sd Futoški Prk 19. Novi Sd Jugovićevo 20. Novi Sd quy 21. Novi Sd Rirsko ostrvo islnd 22. Novi Sd Kmeničk d 23. Veternik 24. Futog 25. Begeč villge 26. Begeč Dnue Fig. 6. Lotion of sites in the region of Novi Sd where femles of Simulium erythroephlum were trpped during the 2006 seson. during the first week of April, while the highest numer of lolities sujeted to elevted iting risk (15 lolities) ws reorded during the third week of My. A totl of 71 ses of elevted iting risk were judged to exist estimted during the seson (56 ses on the right side of the Dnue nd 15 on the left side). During the lst four sesons (2003-2006), n inrese ws registered in the numer of lolities with positive pture results (Tle 2). Lolities situted on the right nk of the Dnue were onstntly exposed to higher iting risk thn those situted on the left nk. The numer of lolities with elevted iting risk s indited y the numer of estimted ses of risk for eh defined tegory peked in 2006. Sttistil nlysis of dt otined t 26 lolities over four sesons of monitoring demonstrted tht the verge numer of femles ptured in trp ws signifintly higher in April, My,

Tle 1. Numer of femles of Simulium erythroephlum ptured in dry ie-ited trps nd estimted risk to humns of eing itten t different lolities in the region of Novi Sd during the 2006 seson. Outrek of Simulium erythroephlum 107

108 A. IGNJATOVIĆ-ĆUPINA ET AL. Tle 2. Resume of distriution of lolities with positive trpping results in reltion to iting risk tegory nd numer of estimted ses of elevted risk to humns of eing itten y Simulium erythroephlum during the sesons of 2003-2006. NUMBER OF LOCALITIES NUMBER OF CASES OF ELEVATED BITING RISK YEAR POSITION OF LOCALITIES with positive pture results with elevted iting risk Ctegory of iting risk Moderte High Very high Extremely high Moderte High Very high Extremely high Totl 2003 2004 2005 2006 Right nk 5 2 2 1 1 0 4 1 1 0 6 Left nk 0 0 0 0 0 0 0 0 0 0 0 TOTAL 5 2 2 1 1 0 4 1 1 0 6 Right nk 10 5 4 2 1 0 7 2 1 0 10 Left nk 3 1 1 0 0 0 1 0 0 0 1 TOTAL 13 6 5 2 1 0 8 2 1 0 11 Right nk 13 11 9 5 0 2 14 5 0 2 21 Left nk 5 4 4 0 1 0 8 0 1 0 9 TOTAL 18 15 13 5 1 2 22 5 1 2 30 Right nk 14 14 12 8 5 8 26 11 7 12 56 Left nk 12 8 8 3 1 0 10 4 1 0 15 TOTAL 26 22 20 11 6 8 36 15 8 12 71 nd June of 2006 thn in the sme months of the previous three sesons (Fig. 7). Despite vrition of trpping results, the highest verge vlue of femles in trp ws reorded in April of 2006, fter the period with the highest level of the Dnue (15.92 femles per trp with four expeted ites on humns per dy). Lower, ut still high vlues were oserved in My nd June (9.99 nd 6.75 femles per trp; high nd moderte iting risk; three nd two expeted ites on humns per dy). Averge vlues of the numer of femles in trp for July, August nd Septemer of 2006 were s low s in the previous three sesons. Medil experts t the Deprtment for Dermtology nd Venereology of the Clinil Center of Vojvodin reported n inresed numer of exmined ptients with symptoms of inset ites strting from April of 2006. By the end of July, the numer of ptients inresed to 30,27 of whih were inhitnts of the region of Novi Sd. In ll ses the ites were loted on the extremities, mostly the legs (elow the knees). Two ptients were itten eqully elow nd ove the knees,

Outrek of Simulium erythroephlum 109 30 25 2003 2004 2005 2006 Averge numer of femles in trp 20 15 10 5 0 April My June July August Septemer, Dunn's multiple rnge test (p = 0,05) Figure 7. Averge monthly numer of femles of Simulium erythroephlum ught in dry ie-ited trp in the region of Novi Sd during the sesons of 2003-2006. only one on the forerms. The linil piture vried in different ptients depending on the numer of ites nd individul sensitivity, ut usully strted with hemorrhgi, edem, nd pinful ithing of the re surrounding the itten point (Figs. 8-11). The symptoms usully persisted for rther long period of more thn week to severl weeks. In more serious ses, erythemtous hnges spred over lrger prt of the skin surrounding the ite. In the sene of ny informtion out the ustive gent t the initil hek-up, ll ptients were dignosed s Itus inseti (inset ite). Soon fter relizing the inresing frequeny of suh symptoms nd due to the reports of interviewed ptients, it eme ler to exminers tht the ustive inset gents were lk flies. The symptomtology of suh ites ompletely orresponded to the linil piture of ites used y S. erythroephlum s desried erlier y KRSTIĆ (1966) AND BURÁNY ET AL. (1972) fter outreks of this speies in 1965 nd 1972. Suh frequeny of ite ses ws unusul in the long-term prtie of this medil institution. It hs to e emphsized tht the Deprtment for Dermtology nd Venereology is medil institution of tertiry protetion grde, where only the most serious ptients re hospitlized. Before eing epted in this institution, ptients re usully exmined t two less speilized medil institutions. It ould therefore e presumed tht the numer of ptients suffering from ites used y this lkfly speies ws muh higher ut not dequtely identified nd registered y generl prtitioners. However, the numer of 30 ptients in 2006 ws very lose to the numer of 37 ptients exmined nd ured t the Clini for Dermtology nd Venereology of the ity of Zemun s reorded y KRSTIĆ (1966) fter the first reported outrek of S. erythroephlum in the ountry in 1965.

110 A. IGNJATOVIĆ-ĆUPINA ET AL. Figs. 8-11. Consequenes of lkfly ites. Suspeted gent: Simulium erythroephlum (photo Vujnović, 2006). All ite ses in 2006 were reorded during the period from April to July, when positive pture results indited the existene of elevted risks of eing itten y S. erythroephlum t mny of the investigted lolities in the region of Novi Sd. Among 27 ptients who were residents of the region, 25 were suspeted of hving reeived their ites in ples where ptures of S. erythroephlum in trps were reorded (Tle 3). Furthermore, 13 ptients were residents of lolities on the right nk of the Dnue (Sremski Krlovi, Petrovrdin, Sremsk Kmeni, nd Beočin). In ll of these lolities, elevted iting risk ws judged to exist severl times during the seson. Seven ptients were suspeted of hving reeived their ites t lolities on the left nk of the river (Begeč nd Novi Sd). Five ptients, residents of the Jugovićevo lolity (severl kilometers from the Dnue s left nk), were itten even though only one pture in trp ws otined. A similr disrepny ws oserved in ptients suspeted of hving suffered lkfly ttks within the urn re of Novi Sd, ut they ould not preisely indite lotion tht ould e ompred with trpping results. Finlly, two reported ite ses ourred t lolities whih were not inluded in the monitoring progrm. The numer of ites per ptient rnged from one to more thn 10. Ptients epted in April hd only two or three ites, while most of those epted during the following months hd high-

Outrek of Simulium erythroephlum 111 Tle 3. Ptients from the region of Novi Sd with dignosed inset ites during the 2006 seson. Suspeted gent: Simulium erythroephlum. Dt soure: Clinil Center of Vojvodin, Deprtment of Dermtology nd Venereology. Month April My June July Lolities of ite report Numer of exmined ptients Dte of reeption Numer of ites per ptient Lotion of ites Novi Sd 1 April 19th 2006 3 elow the knees Sremsk Kmeni 1 April 29th.2006 2 elow the knees Petrovrdin 1 April 30th 2006 3 forerms Novi Sd 1 My 12th.2006 1 elow the knee Sremski Krlovi 1 My 20th 2006 5 elow the knees Beočin 1 My 20th 2006 5 elow the knees Petrovrdin 1 My 23rd 2006 2 elow the knees Jugovićevo 2 My 27th 2006 8 elow the knees My 27th 2006 2 elow the knees Sremski June17th 2006 6 elow the knees 2 Krlovi June 23rd 2006 6 elow the knees Begeč 2 June 20th 2006 8 elow the knees June 23rd 2006 7 elow the knees June 20th 2006 7 elow the knees Jugovićevo 3 June 20th 2006 4 elow nd ove the knees June 23rd 2006 4 elow the knees Bnoštor 1 June 23rd 2006 > 10 elow nd ove the knees Petrovrdin 1 June 31st 2006 2 elow the knees July 4th 2006 5 elow the knees Sremski 3 Krlovi July 17th 2006 7 elow the knees July 31st 2006 3 elow the knees Petrovrdin 2 July 9th 2006 8 elow the knees July 18th 2006 9 elow the knees July 10th 2006 6 elow the knees Novi Sd 3 July 17th.2006 5 elow the knees July 24th 2006 8 elow the knees Bčki Jrk 1 July 15th.2006 4 elow the knees er numer of ites: up to eight ites in My, more thn 10 ites in June, nd up to nine ites in July. The inrese in the numer of itten ptients nd numer of ites per ptient n e ttriuted to the ft tht the dily period of feeding tivity of dult femles of S. erythroephlum oinides with humn outdoor tivity. The ft is tht memers of the lol popultion usully spend muh more time outside during lte spring nd summer, therey inresing the time of exposure to lkfly ites. Estimtion of the iting risk to humns in this study ws lulted on the sis of hypothetil five-hour period of exposure in the fternoon efore sunset. However, sine no ext informtion out the durtion of ptient exposure is ville, n dequte omprison of the estimted nd reorded ite ses ould not e hieved. It hs to e emphsized tht the dt otined t the lini were relted to the dte when ptients were epted for exmintion, not to the dte when ites ourred. Mny of the ptients

112 A. IGNJATOVIĆ-ĆUPINA ET AL. reported tht the ites ourred lte in the fternoon, one or few dys efore medil exmintion. Lk of this informtion n explin why some of the ite ses were reorded lter thn the estimte of elevted iting risk. The results of this study indite tht higher iting risk existed t lolities long the nks of the Dnue, espeilly ones lose to the undnt reeding sites on the right nk, in rurl or semirurl lolities, where the mjority of ptients were itten. In suh hitts, the iting risk to humns n e estimted quite urtely. Aording to ŽKOVIĆ (1971), S. erythroephlum hs firly high potentil for flight in serh of lood mel, whih ws defined within the rnge of 20-30 km from the reeding sites. It is still unler when the spreding of femles ours in lol eologil onditions. Our results indite tht femles n rpidly invde lolities t short distnes (up to 5 km) from the reeding sites in serh of lood mel. This hypothesis ws onfirmed y our reords of femles in trps positioned lose to the Dnue nd t sites within the urn re or in the surrounding hills. The sptil distriution of dults t urn lolities distnt from the min reeding sites ws irregulr, nd the iting risk ould not e predited with stisftory onfidene there. CONCLUSIONS Suitle eologil nd hydrologil onditions, espeilly the extremely high level of the Dnue River during the spring of 2006, provoked the mssive pperne of dults of S. erythroephlum in the region of Novi Sd, reting sitution tht ould e hrterized s n outrek. Compring the level of the Dnue nd the undne of dult popultions in the region during lst four yers, we were le to demonstrte tht one to two months of wter level ove 450 m in the spring nd erly summer n inrese size of the S. erythroephlum popultion. On the other hnd, high wter level during the seond hlf of summer hs no influene on size of the dult popultion. Mssive emergene of three genertions of S. erythroephlum ws reorded during the seson from April to June: during the first nd seond week of April, third nd fourth week of My nd seond nd third week of June, respetively. The numer of lolities where femles of S. erythroephlum were ptured nd the numer of lolities with ses of elevted iting risk were signifintly higher in 2006 thn during the three previous yers. Signifintly more ses of elevted iting risk in eh tegory from moderte to extremely high were lso reorded in 2006. The prt of the region lose to reeding sites on the right nk of the Dnue generlly ws more endngered y lkflies thn lolities on the opposite nk. Despite high vrition of trpping results t different lolities, the verge monthly numers of femles reorded in April, My, nd June of 2006 were signifintly higher thn in the previous three sesons. High popultion density of S. erythroephlum used frequent pperne of symptoms typil of the ite of this speies during the period from April to July of 2006. The mjority of ptients were residents of the Novi Sd region, where elevted iting risk hd een estimted erlier. In order to otin more detiled piture of the flight ehvior of this speies, the reserh progrm should e ontinued nd rried out t greter distnes from the reeding sites.

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