NDFLIES ON THE ISLAND OF CORFU, GREECE

(1)

S

a

NDFLIES ON THE ISLAND OF CORFU, GREECE

PAPADOPOULOS B.* & TSELENTIS Y.*

Summary :

The island of Corfu is an endemic area of human leishmaniasis, mainly visceral and secondly cutaneous. In August 1996, a survey of phlebotomine sandflies was conducted throughout the whole island. Using castor-oil paper traps, a total of 2 ,6 1 5 sandflies were caught. The following species were identified: 4 5 0 (17.21 %) Phlebotomus neglectus, 213 (8.15% ) P. tobbi, 129 (4.93% ) P. perfiliewi, 12 (0.46% ) P. sergenti, 1 1 (0.42% ) P. simici, 4 (0.15% ) P. papatasi, 9 9 9 (38.20% ) Sergentomyia minuta and 7 9 7 (30.48%) S. dentata. Among the potential vectors of Leishmania spp., P. neglectus, P. tobbi and P.

perfiliewi, were the most widespread species on the island.

However, a decrease of the population density of sandflies compared to previous entomological studies was observed.

R é s u m é : Le s p h l é b o t o m e s d e l'î l e d e Co r f u, Gr è c e

L'île de Corfu est une région endémique de leishmaniose humaine viscérale et secondairement de leishmaniose cutanée. En août

1996, une étude sur les phlébotomes a été entreprise dans toute l'île. Au total, 2 6 1 5 phlébotomes ont été capturés par la méthode des pièges adhésifs. Les espèces suivantes ont été identifiées: 4 5 0 ( 17,21 %) Phlebotomus neglectus, 2 1 3 (8, 15 %) P. tobbi, 129 (4 ,9 3 %) P. perfiliewi, 12 (0,4 6 %) P. sergenti, 1 1 (0,42 %) P. simici, 4 (0,15% ) P. papatasi, 9 9 9 (38,20% ) Sergentomyia minuta et 7 9 7 (3 0 ,4 8 %) S. dentata. Parmi les vecteurs potentiels de Leishmania spp., P. neglectus, P. tobbi et P. perfiliewi sont les espèces les plus répandues. Toutefois, une baisse de la densité des populations de phlébotomes par rapport aux études entomologiques précédentes a été observée.

KEY WORDS : Sandflies, Greece. MOTS CLÉS : Phlébotomes, Grèce.

T

he prefecture1 o f Corfu, consisting o f the island o f Corfu and som e surrounding small islands, is one o f the four pre fectures o f the Ionian

Islands lying to the w est o f mainland G reece. It is an endem ic area o f human leishmaniasis, mainly visce ral

and secondly cutaneous. According to the data o f the G reek Ministry o f Health, during the period 1951- 1995, 56 cases o f visce ral leishmaniasis (VL) and 22 cases (12 o f them in 1951) o f cutaneous leishmaniasis (CL) w ere recorded in this pre fecture. The incidence o f leishmaniasis in dogs, considered to be the domestic reservoir host o f VL in the M editerranean region, is m uch higher. During the last nine years (1988-1996) for w hich detailed statistics are available from the O ffice o f Animal Health o f the G reek Ministry o f Agri

culture, 297 canine cases w ere reported by the local Veterinarian Services.

L e is h m a n ia in fan tu m , the causative agent o f zoonotic VL and sporadic cases o f CL, has been isolated in Corfu

1 Prefecture : administrative division o f the country.

* Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, Faculty of Medicine, University of Crete, P.O.

B ox 1393, Iraklion Crete, Greece.

Correspondence: Dr. B. Papadopoulos.

Tel.: 081 394076-394743-394801 - Fax: 081 394408.

E-mail: byron@edu.uch.gr

from a human, a dog and a sandfly. In 1981, Tza- mouranis et a l. (1984) su cceed ed in isolating and typing L. in fa n tu m from a human and a dog that had overt leishmaniasis, while in 1987, Léger et al. (1988) isolated a parasite from P h leb o to m u s n eg lectu s, which was found by isoenzym e characterization to be indis- tin gu ishable from L. in fa n t u m zym odem e MON1 (= LON49).

In an early study conducted before the second World War, Stephanides (1940) observed that P. p a p a t a s i was the most abundant sandfly species in the human habitations o f Corfu. Later, during the period 1979- 1981, in a large scale entom ological survey conducted on the island by the team o f Prof. N. Léger, sandflies o f eight diffe rent sp ecies w ere captured (Madulo- Leblond, 1983; Pesson et al., 1984).

In this paper w e present the results o f a massive sam- pling o f sandflies throughout the island o f Corfu conducted in August 1996.

STUDY AREA _____________________

T

he island o f Corfu (592 km2, 104,781 inhabi

tants) is the northernmost large island o f the Ionian sea. In terms o f administration, this island with other surrounding small islands form the Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1998054387

(2)

Fig. 1. - The island o f Corfu with the stations in which the entomological survey was carried out ( O ) and sites from where human VL ( * ) and CL ( * ) cases were reported during the period 1951-1995.

3 8 8 Note de recherche Parasite, 1998, 5, 387-391

(3)

SANDFLIES ON THE ISLAND OF CORFU

pre fecture o f Corfu (642 km2, 107,592 inhabitants). Its capital is the city o f Corfu (31,359 inhabitants) situated on the west coast o f the island. The island o f Corfu is situated in the north-west part o f G reece, opposite the re gion o f Hepirus in the G reek mainland and Albania, betw een 39° 22’ and 39° 4 9 ’ north latitude and 19° 3 8 ’ and 20° 0 8 ’ east longitude (Fig. 1). The island is about 62 km long and 28 km w ide in its northern part, reduced to 3 5 km in its narrowest Southern part. Most o f the island is o f low altitude (< 100 m). Mount Pan- tocrator, 906 m in altitude, in the north is its highest point. There is also a mountain ridge, with a maximum altitude o f 576 m, in the central-southern region. The rest o f the island is flat to hilly. The w hole island belongs to the attenuated m esom editerranean type o f the mediterranean bioclim ate (Mavrommatis, 1980). It is located on th e January isotherm o f 10 °C and the July isotherm o f 25.5 °C. The relative humidity is relatively high during the entire year (6 5 -7 5 % ) and the mean annual pre cipitation is 1,150 mm.

The entom ological survey was conducted along transects at 72 stations, mainly in the north and the cen tral part o f the island (Fig. 1). The stations were located at points w hose altitude ranged from 20 to 680 m.

MATERIALS AND METHO D S ________________

T

he entom ological survey was carried out bet

w een August 16 and August 23, 1996, in 72 sta

tions on transects throughout the island (Fig. 1).

Sandflies w ere caught using castor-oil treated paper sheets (A4 format photocopy papers). A total o f 1,170 castor-oil treated paper sheets w ere set and 1,125 o f them w ere recovered (losses 3.85% ).

The sticky traps (10 to 30 traps/station) w ere placed into any potential sandfly breeding or resting site (holes or cracks in dry walls or rocks; spaces in stone walls; pipes o f buildings or gardens). The papers were left in place for four days. The specim ens w ere then picked up with a fine paint-brush, w ashed in 9 0 % ethanol, cleared and mounted in Marc-André solution for identification, w hich was made according to the descriptions o f Léger et al. (1986).

In order to estimate the relative densities o f the sandfly species in the different stations, the number o f sand

flies collected per 100 paper traps (sf/100 pt) per sta

tion was calculated. Stations with < 2 5 sf/100 pt are considered o f low density for the species in question, stations with 25-100 sf/100 pt o f middle density and stations with > 100 sf/100 pt o f high density.

RESULTS

A total o f 2,615 sandflies w ere collected during August 1996. Table I shows the species identified, their total number, their relative density (num ber o f sandflies per 100 paper traps), their percent o f total, the num ber o f m ales and females and the proportion o f females for each species, as well as the num ber o f localities in w hich they w ere found and their percent o f total.

All but nine stations w ere positive for sandflies. About 1/3 o f the captures w ere P h leb otom u s spp. and the rest 2/3 S erg en to m y ia spp. (Table I). Almost all samples of P h leb o to m u s spp. belong to the subgenus L arrou ssiu s, P. n eglectu s being the most abundant and widespread.

For S erg en to m y ia spp. almost equal numbers o f m ales and females were captured, while for P h lebotom u s spp.

the se x ra tio was strongly in favor o f m ales.

No of sf, number of sandflies; No o f sf/100 pt, number of sandflies per 100 paper traps; % o f total sf, percentage o f the total number of collected specimens; o o , number o f m ales ; 9 9, number o f females ; 9 9 / o o + 9 9 , proportion o f females ; No o f localities, number of localities in which they were found; % o f localities, percentage of the total number of localities.

Table I. - Sandfly species on the island o f Corfu.

(4)

No o f localities, number of localities; % o f localities, percentage o f the total number o f localities.

Table II. - Distribution o f the localities the sandfly species were found according to their relative density (number of sf/100 pt).

Table II shows the distribution o f localities w here the différent sandfly species were found according to their relative density. Most o f the species w ere found in low (< 2 5 sf/100 pt) or medium (25-100 sf/100 pt) densities.

DISCUSSION _________

O

ur entom ological results are generally in agreem ent with those obtained by Madulo- Leblond (1983) about 15-17 years earlier.

However, the relative density o f almost ail sandfly spe

cies was low er in our survey. This is probably due to the drop in the num ber o f most sandfly species during August (Madulo-Leblond, 1983; Papadopoulos & Tse- lentis, 1994) and the extensive use o f insecticides, especially against the crop pests, during the last years.

Ail three P h leb o to m u s spp. belonging to the subgenus Larroussius, P. n eglectus, P. to b b i and P. p erfiliew i, are co n sid e re d p o te n tial v ecto rs o f L. in fa n t u m . P.

n eglectus, the most com m on P h leb o to m u s sp. on the island, is still the only sandfly species from w hich a L. in fa n tu m has been isolated in the Ionian islands (Léger et al., 1988; Garifallou et al., 1989). P. p e r filiew i has been found infected with viscerotropic L. in fan tu m in Italy (M a ro li e t a l ., 1 9 8 8 ) an d d e rm o tro p ic L. in fa n tu m in Algeria (Izri & Belazzoug, 1993), while P. to b b i has been infected experim entally by feeding on infected hamsters (Adler &d Theodor, 1935).

The rarity o f P. p a p a ta si, vector o f L. m a jo r and sandfly fever, in our captures is noteworthy. This species was considered by far the most abundant species in Corfu in human habitations (Stephanides, 1940). The scarcity observed may be due to the low num ber o f domestic

sites explored with the m ethod o f transects using castor-oil paper traps, as discussed in a previous article (Papad opou los & Tselentis, 1994). This sp ecies is nowadays found to be abundant only in Eastern Crete, Karpathos and Athens (Pesson et al., 1993; Papado

poulos & Tselentis, 1994; Chaniotis et al., 1994).

P. sergenti, w hich was long suspected (Adler et al., 1938) but only recently proved to be a vector o f L. tro- p i c a (Al-Zahrani e t a l., 1989; Guilvard e t a l., 1991), was rare in Corfu, w here only few cases o f CL have been recorded. This species is relatively abundant in the w armer and drier Southern Ionian Islands and esp e

cially in Zakynthos (Pesson et al., 1984), the principal focus o f CL in the région. It should be noted that P.

sergenti, as well as P. sim ici, b ecom e very rare late in the season (Madulo-Leblond, 1983).

The sandflies o f the genus S ergen tom yia, captured in high numbers during our study, feed on reptiles and therefore have no epidem iological interest as vectors for human and canine leishmaniasis.

REFERENCES

Ad l e rS. & Th e o d o r O . Investigations on Mediterranean kala azar. IX. Feeding experiments with Phlebotom us p em i- ciosus and other species on animais infected with Leish

m an ia infantum. Proceedings o f the Royal Society (B), 1935, 116, 516-542.

Ad l e r S., Th e o d o r O . & Wit e n b e r g G . Investigations on Mediterranean kala azar. XI. A study of leishmaniasis in Canea (Crete). Proceedings o f the Royal Society (B), 1938,

125, 491-516.

Al- Za h r a n i M . A ., Pe t e r s W ., Ev a n s D .A ., Sm it h V . & Ch in g Ch in I. Leishm ania infecting man and wild animais in Saudi Arabia. 6. Cutaneous leishmaniasis of man in the

390 Note de recherche Parasite, 1998, 5, 387-391

(5)

SANDFLIES ON THE ISLAND OF CORFU

south-west. Transactions o f the Royal Society o f Tropical M edicine a n d Hygiene, 1989, 83, 621-628.

Ch a n io t is B ., Go z a l o- Ga r c ia G . & Ts e l e n t is Y . Leishmaniasis in the large urban area of Athens, Greece. Entomological studies. Annals o f Tropical M edicine a n d Parasitology,

1994, 88 (6), 659-663.

Ga r if a l l o u A., ^Ha d jl a n t o n io u M., ^S^{c h n u r}L.F., ^Y^{u v a l}B., ^W^{a r}^-

b u r g A., ^Ja c o b s o n R.L., ^Pa t e r a k iE., ^Pa t r ik o u s s isM., ^S^{c h l ein}

Y . & Se r ie C. Epidemiology of human and canine leish

maniasis of the island of Zakinthos. In: D . T . Hart (Editor), Leishmaniasis. Plénum Publishing Corporation, 1989, pp. 1011-1015.

Gu il v a r d E., Rioux J.-A., Ga l l e g o M ., Pr a t l o n g F., Ma h jo u r

J., Ma r t in e z- Or t e g a E., De r e u r eJ., Sa d d ik iA. & Ma r t in iA.

Leishm ania tropica au Maroc. III. Rôle vecteur de Phle

botomus sergenti. A propos de 89 isolats. Annales d e Parasitologie H um aine et Comparée, 1991, 6 6 (3 ), 96-99.

Iz r i M.A. & Be l a z z o u gS. Phlebotomus (Larroussius) perfiliewi naturally infected with dermotropic Leishm ania infantum at Tenes, Algeria. Transactions o f the Royal Society o f Tro

p ic a l M edicine a n d Hygiene, 1993, 87, 399-

Lé g e rN., Gr a m ic ia M ., Gr a d o n i L ., Ma d u l o-Le b l o n d G ., Pe s s o n B . , Fe r t é H., ^Bo u l a n g e r N., ^K^{il l ic k}^{- K}e n d r ic k R. & ^K^{il l ic k}^-

Ke n d r ic k M . Isolation and typing of Leishm ania infantum from Phlebotomus neglectus on the island of Corfu, Greece.

Transactions o f the Royal Society o f Tropical M edicine a n d Hygiene, 1988, 82, 419-420.

Lé g e r N., ^P^{e s s o n} B. & ^M^{a d u l o}^-Le b l o n d G. Les phlébotomes de Grèce. Biologia Gallo-Hellenica, 1986, 11 (2), 165-192.

Ma d u l o- Le b l o n d G . L e s phlébotomes des îles Ioniennes.

Thèse Doc. Sci. Pharm., Université de Reims, 1983, 218 p.

Ma v r o m m a t is G. Le bioclimat de la Grèce. Relations entre le climat et la végétation naturelle. Cartes bioclimatiques (in Greek, with French summary). Dasiki Erevna, 1980, 1, 63 p. + 3 maps.

Pa p a d o p o u l o s B. & Ts e l e n t is Y . Sandflies in the Greater Athens région. Parasite, 1994, 1 (2), 131-140.

Pe s s o n B., Lé g e r N. & Ma d u l o-Le b l o n d G. La leishmaniose en Grèce : Les phlébotomes des îles ioniennes et de la mer Egée. Annales d e Parasitologie H um aine et Com

parée, 1984, 5 9 (3), 277-296,

Pe s s o n B., Lé g e r N., Ma d u l o-Le b l o n d G . , Fe r t é H., Ts e l e n t is I ., Pa p a d o p o u l o s B. & Pé r ie r e sJ. S p é c i a t i o n e t v i c a r i a n c e c h e z l e s p h l é b o t o m e s d e s î l e s g r e c q u e s . P r o c . 6 t h I n t.

C o n g r . Z o o g e o g r a p h y a n d E c o l o g y o f G r e e c e a n d t h e A d ja c e n t R é g i o n s , T h e s s a l o n i k i , 1993. Bios, 1994, 2, 233- 243.

St e p h a n id e s T. Corfu Phlebotom us (Dipt. Psychod.) found in human habitations. Bulletin o f Entom ological Research, 1940, 30, 303-304.

Tz a m o u r a n is N., Sc h n u r L. F ., Ga r if a l l o u A ., Pa t e r a k i E . &

Se r ie C. Leishmaniasis in Greece. I. Isolation and identifi

cation of the parasite causing human and canine viscéral leishmaniasis. Annals o f Tropical M edicine a n d Parasito- logy, 1984, 78 (4), 363-368.

Reçu le 2 décembre 1998 Accepté le 25 juin 1998

E rratum

Pa p a d o p o u l o s B. & ^Ts e l e n t is Y . Sandflies in the Greater Athens région. Parasite, 1994, 1 (2), 131-140.

Table I. - Nbr sf, number o f sandflies; %, percentage o f the total number of collected specim ens; KK, number of m ales ; AA, number of females; AA/KK + AA, proportion o f females; Nbr local., number o f localities they were found.