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Parasitol Res
https://doi.org/10.1007/s00436-017-5675-8
ORIGINAL PAPER
Phlebotomine sandflies and factors associated with their
abundance in the leishmaniasis endemic area of Attiki, Greece
Sofia Boutsini 1 & Labrini V. Athanasiou 2 & Gregory Spanakos 3 & Dimitra Ntousi 1 &
Eleni Dotsika 4 & Marina Bisia 2 & Elias Papadopoulos 5
Received: 22 May 2017 / Accepted: 5 November 2017
# Springer-Verlag GmbH Germany, part of Springer Nature 2017
Abstract Leishmaniasis is a parasitic disease of animals and
humans caused by several Leishmania species and transmitted
by phlebotomine sandflies. The aim of the present study was
to identify the species of field collected phlebotomine
sandflies in the endemic area of the Attiki during 4 consecutive years, to isolate the Leishmania parasites from the
infected sandflies, and identify possible factors associated
with sandfly abundance in the area. A total of 542 trappings were made in 46 collection sites, in purely urban
areas, periurban areas, and purely rural areas in Attiki.
Out of the 3254 sandflies trapped, 1448 (44.43%) were
female and 241 (16.64%) of the females were blood fed
while Leishmania infantum DNA was detected in the
0.41% of them. Regarding sandfly species, the most prevalent
was Phlebotomus tobbi (41.52%) followed by Sergentomyia
minuta (27.44%), P. neglectus (14.83%), P. simici (11.08%),
P. papatasi (3.68%), P. similis (0.89%), and P. alexandri
* Labrini V. Athanasiou
lathan@vet.uth.gr
1
National Reference Laboratory for Parasites, Directory of Veterinary
Centre of Athens, Ministry of Rural Development and Food,
Athens, Greece
2
Faculty of Veterinary Medicine, University of Thessaly,
43100 Karditsa, Greece
3
National School of Public Health, 196 Alexandras Ave,
11521 Athens, Greece
4
Laboratory of Cellular Immunology, Department of Microbiology,
Hellenic Pasteur Institute, Athens, Greece
5
Laboratory of Parasitology and Parasitic Diseases, Faculty of
Veterinary Sciences, Aristotle University of Thessaloniki, University
Campus, GR-54124 Thessaloniki, Greece
(0.56%). Periurban areas were found to have the highest density of sandfly populations.
Keywords Attiki . Environmental . Leishmania .
Phlebotomus . Sand flies
Introduction
Leishmaniases is a group of human and animal diseases with
distribution in all continents, including previously unaffected
Australia (Dereure and Dedet 1999; Rose et al. 2004) and
except Antarctica and the islands of Pacific Ocean. Although
infection and/or disease has been reported in many different
species, canids are considered as the main reservoirs of
Leishmania infantum, the causative agent of canine leishmaniasis and zoonotic visceral leishmaniasis in the Mediterranean
Area, Asia, North Africa, and South Africa (Dantas-Torres
2007). Incidence of zoonotic human leishmaniasis in Greece
for the last decade is relatively stable with small fluctuations
and an average of 0.36 cases per 100,000 population with
almost half of the reported visceral leishmaniasis cases reported in Attiki (Gkolfinopoulou et al. 2013).
Seroprevalence of canine leishmaniasis in Greece ranged
from 1.6 to 24% in various studies conducted in different
geographic regions and seasons of the year, employing different diagnostic methods, samples, and sampling schemes
(Boutsini et al. 2002), while a seropositivity of 30.12% has
been reported in Attiki (Athanasiou et al. 2012).
The involvement of sandflies in the ecology of the disease
in the Mediterranean region as well as in the rest of the world
has been long reported (Adler 1947; Lanotte et al. 1979;
Rioux et al. 1972, 1973; Theodorides 1997). Until now,
several different species of sandflies have been reported
in Greece such as Phlebotomus perfiliewi, P. neglectus,
Parasitol Res
P. tobbi, P. balcanicus, P. simici, P. papatasi, P. sergenti,
P. similis, P. alexandri, P. mascittii, Sergentomyia dentata,
and S. minuta with important differences regarding spatial
distribution and biological habits (Aransay et al. 1999;
Chaskopoulou et al. 2016; Ivovic et al. 2007; Xanthopoulou
et al. 2011).
Endemicity of leishmaniasis by Leishmania infantum is
associated with the distribution and abundance of vectors
(Antoniou et al. 2013; Killick-Kendrick 1999), mainly of
sandfly species of the subgenus Phlebotomus (Larroussius)
as well as Lutzomyia species (L. longipalpis and closely related species) that have been reported to transmit L. infantum in
South America. Furthermore, the role of some Sergentomyia
is also discussed (Maia and Depaquit 2016). On the other
hand, climatic conditions may favor or not the survival and
the activity of the sandfly vectors and therefore influence the
force of the infection. Environmental temperature affects the
biological cycle of the vector, and there is a positive correlation between high temperatures and the infection rate of
sandflies, the rate of promastigote multiplication in their midgut, the movement of promastigotes towards their thoracic
midgut, and the attachment of the flagellates to the wall of
the stomodaeal valve (Rioux et al. 1985).
Furthermore, deforestation, irrigation, and urbanization in a
constantly endemic area of leishmaniasis such as Attiki may
have contributed in widening the geographical distribution of
sandflies and consequently of the parasites.
The aim of the present study was to identify the species of
field collected Phlebotomine sandflies in the endemic area of
the Attiki during 4 consecutive years, to isolate the
Leishmania parasites from the infected sandflies, and identify
possible factors associated with sandfly abundance in the area.
Materials and methods
Sandflies were collected for 4 consecutive years in the
Prefecture of Attiki. Located on the eastern edge of Central
Greece, the study area of Attiki covers about 427 km2 and has
a roughly estimated population of 5,000,000 inhabitants. The
greater area of Attica includes Athens and Piraeus along with
62 other cities and settlements. To the east, south, and south
west, it is bordered by the sea, while four mountains—Egaleo,
Parnitha, Penteli, and Hymettus delineate the hilly plain and
may act as natural barriers that determine the distribution of
phlebotomines in the area.
Sites for collection were primarily selected based on the
reported presence of dogs with leishmaniasis. Secondarily,
attention was paid so that assigned areas represented (a) purely
urban areas; (b) suburban areas, densely populated areas on
the outskirts of the mountains Hymettus, Penteli, and Parnitha,
previously semi-rural and recently urbanized; and (c) purely
rural areas. Εnvironmental conditions (temperature, sunshine,
winds) and coordinates of each site were recorded for every
labeled sand fly trap. A total of 542 trappings were made by
means of Onderstepoort-type traps in the 46 collection sites
after sunset and collected before sunrise, and they were used
as previously described (Venter and Meiswinkel 1994). The
plastic container with the trapped insects was filled with 70%
alcohol and transported to the Laboratory of Parasitology.
Containers were kept at 2–4 °C until sand flies were separated
from other insects.
Initially, the contents of the plastic container were filtered
through a mesh into a conical flask followed by 4–5 washes
with tap water so as to remove impurities such as dust. The
remaining insects held on the filter were transferred to a petri
dish with an equivalent amount of water and the insects were
separated by sex, using a stereoscope. Female sand flies with
blood in their gut were stored in vials with absolute alcohol for
detection and identification of Leishmania spp. by nested PCR
(n-PCR).
The reference strains used for that purpose were (a)
L. infantum MON-1 MCAN/PT/98/IMT244, (b) L. tropica
MON-60 MHOM/SU/74/SAF-K27, and (c) L. major
MRHO/SU/59/P. DNA was extracted using a commercially
available kit (Qiamp DNA mini kit, Qiagen), and it was stored
in vials at − 20 °C pending a n-PCR assay as previously described (Athanasiou et al. 2013; Spanakos et al. 2008).
Leishmania genome amplification was performed using the
primers LBL, 5′– GCAATACAGGTGATCGGACA-3′ and
LBR, 5′-TGCGTTCTTCAACGAAATAGG-3′. PCR products were separated by electrophoresis on a 2% agarose gel
in 1 × TAE (Tris-Acetate-EDTA) buffer. Digestion of the PCR
products with the restriction enzyme Apo I allowed the unequivocal differentiation and identification of Leishmania
species.
The remaining insects were placed into 1.5–2 ml
microvials with 97% ethyl alcohol and were subsequently
stored at 4 °C pending further testing. After removal of soft
tissue with potassium hydroxide, specimens (5–8 sandflies)
were placed on slides and mounted in Hoyer’s medium
(Lewis 1969). For species identification, the external genitalia
of males and the morphological features of the pharynx and
spermathecae of females were examined as previously described (Leger et al. 1986; Lewis 1987) using a microscope
(NICON SMZ-U).
Percentages of the phlebotomine species found in the different areas (urban, periurban, and rural), different meteorological conditions (rain, sunshine, overcast), and different
months of the year were compared using Pearson’s chisquare test.
Furthermore, the effect of temperature and wind on the
different phlebotomine species was assessed with the
Analysis of Variance with Bonferroni correction for multiple
comparisons. All statistical analyses were performed using
SPSS v.15.0 for Windows (IBM Corp., Armonk, NY, USA).
Parasitol Res
Results
Throughout the 4 years of the study, a total of 3254
phlebotomine sand flies were collected from 42 of the 46 sites,
1448 of which were females (44.49%) and 1806 (55.51%)
males. Out of 1448 female sand flies collected, 241
(16.64%) contained blood in their gut and were not identified
at species level. The majority (72.56%) of the remaining
sandflies (3013) were found to belong to the genus
Phlebotomus while 827 insects (27.44%) belonged to the genus Sergentomyia. Six of the identified species (P. neglectus,
P. tobbi, P. simici, P. papatasi, P. alexandri, and P. similis)
belonged to the genus Phlebotomus and one species
(S. minuta) belonged to the genus Sergentomyia.
The 241 female sand flies that contained blood in their gut
were subsequently examined by means of n-PCR for the detection of parasite DNA. Only one reaction (0.41%) yielded a
n-PCR product of 350 bp. Digestion with the restriction enzyme Apo I determined that it belonged to the Leishmania
infantum species.
Most of the sandflies were collected from June to
September with small fluctuations among years of collection
and collected species. The numbers of each sand fly species
per month of the year they had been collected is displayed in
Fig. 1.
Most of sand flies were collected in moderate (31–34 °C) to
high (> 34 °C) environmental temperature and wind force less
than 7 in the Beaufort scale with P. tobbi as the prevailing
species collected.
Correlation between collection sites and sand fly species
demonstrated that P. tobbi was the prevailing species in urban
(38.4%), periurban (43.5%), and rural (39.8%) areas. The percentages for the rest of the species in all areas are shown in
Table 1. A significant correlation is observed between the sites
of collection and the sand fly species: X2 (8) = 20.072,
p < 0.05.
Association of the frequency of the prevailing
phlebotomine species with the meteorological conditions
and the altitude of collection sites is depicted in Tables 2
and 3, respectively.
Discussion
In recent years, epidemiologic distribution of leishmaniasis
has been altered, and newly affected areas indicate that both
Phlebotomus hosts and the disease are spreading, probably
due to climate change. According to a study in Attiki, occurrence of canine and human Leishmaniasis is in line with the
geographical expansion of the sand fly species. Cases tend to
spread in parallel with the urbanization of the hilly plains and
low-range mountains (Antoniou et al. 2013).
This is the first extensive study on the vector species of
Leishmania parasites, for four consecutive sand fly activity
periods in urban, periurban, and rural areas of Attiki.
Out of the 3254 sand flies that were collected in total, seven
species of phlebotomines were identified, in agreement with
previous studies in the same area (Chaniotis et al. 1994;
Papadopoulos and Tselentis 1994). P. perfiliewi was reported
for the first time in Attica by Ivovic et al. (2007) but was not
among the identified species in our study. It should be mentioned that P. perfiliewi is a species encountered mainly in
Northern Greece, where humidity is comparatively higher
than in Attiki (Chaskopoulou et al. 2016; Xanthopoulou
et al. 2011).
The prevalent species identified in this study was
Phlebotomus (Larroussius) tobbi, one of the three species belonging to subgenus Larroussius that have been reported in
our country (Leger et al. 1986). This species is a proven vector
of L. infantum in Cyprus (Leger et al. 2000). P. tobbi is involved in transmitting L. infantum, the cause of visceral
Leishmaniasis in the Mediterranean basin (Lane et al. 1984).
Fig. 1 Number of sandflies of each species collected per month of 4 consecutive years in Attiki, Greece
Parasitol Res
Table 1 Count and percentage of
sand fly species per type of area of
collection
Sand fly species
P. neglectus
P. tobbi
Area
Total
Urban count % within
species % within area
Periurban count % within
species % within area
Rural count % within
species % within area
41
9.1%a
23.2%
68
274
60.8%b
136
30.2%c
451
100.0%
14.5%
823
65.4%b
14.8%
367
29.2%c
15.1%
1258
100.0%
43.5%
39.8%
42.1%
195
57.7%b
122
36.1%c
338
100.0%
10.3%
80
70.8%b
13.2%
28
24.8%c
11.3%
113
100.0%
4.2%
520
62.6%b
27.5%
3.0%
269
32.4%c
29.2%
3.8%
831
100.0%
27.8%
5.4%a
38.4%
P. simici
P. papatasi
21
6.2%a
11.9%
5
S. minuta
4.4%a
2.8%
42
5.1%a
23.7%
a,b,c
Percentages with different superscripts are statistical significantly different
In Northern Greece, Chalkidiki and Xanthi, P. tobbi along
with P. neglectus, and P. perfiliewi are the prevailing species
of the genus Phlebotomus (Karanis et al. 2000). Even though
P. tobbi has not been identified as a vector for L. infantum in
Greece, it does belong to the subgenus Larroussius (exclusive
vectors of L. infantum) and is closely related to P. perniciosus,
the vector of L. infantum in Italy, France, and Spain. However,
Table 2 Sandfly species and
meteorological conditions at the
sites of collection
Sand fly species
P. neglectus
P. tobbi
P. simici
P. papatasi
S. minuta
a,b,c
it appears that P. tobbi transmits the parasite mostly among
dogs (Chaniotis et al. 1994).
According to our study, P. neglectus was third in frequency
(14.83%), followed by P. tobbi and S. minuta. P.neglectus and
P. tobbi are the two species that belong to the subgenus
Larroussius that are most probably implicated in the transmission of L. infantum in humans and dogs in the Mediterranean
Meteorological conditions
Total
Rainy count % within
species % within area
Sunshine count % within
species % within area
Overcast count % within
species % within area
25
7.2%a
10.9%
116
10.5%a
50.4%
210
60.7%b
13.2%
700
63.1%b
43.9%
111
32.1%c
16.1%
294
26.5% c
42.7%
346
100.0%
13.8%
1110
100.0%
44.2%
34
13.0%a
14.8%
6
6.2%a
2.6%
49
7.0%a
21.3%
153
58.6%b
9.6%
64
66.0%b
4.0%
468
66.9%b
29.3%
74
28.4%c
10.7%
27
27.8%c
3.9%
183
26.1%c
26.6%
261
100.0%
10.4%
97
100.0%
3.9%
700
100.0%
27.8%
Percentages with different superscripts are statistical significantly different
Parasitol Res
Table 3 Sand fly species and
altitude at the sites of collection
Altitude (m)
Sand fly species
P. neglectus
P. tobbi
P. papatasi
P. simici
S. minuta
0–100
21 (9.25%)
4.71a
101–200
147 (17.11%)
32.96b
278 (14.76%)
62.33c
446
84 (37%)
6.71a
339 (39.46%)
27.10b
828 (43.97%)
66.19c
1251
8 (3.52%)
7.21a
25 (2.91%)
22.52b
78 (4.14%)
70.27c
111
47 (20.7%)
14.07a
96 (11.17%)
28.74b
191 (10.14%)
57.19c
334
67 (29.53%)
8.10a
252 (29.35%)
30.47b
508 (26.99%)
61.43c
827
201–429
Total
a,b,c
Total
227
859
1883
Percentages with different superscripts are statistical significantly different
(Chaniotis et al. 1994). Its presence in Attiki has been reported
in the past by many investigators (Chaniotis et al. 1994;
Chaniotis and Tselentis 1996; Hadjinicolaou 1958; Hertig
1949; Papadopoulos and Tselentis 1994; Tselentis et al.
1994). Interestingly Ivovic et al. (2007) found only 8
P. neglectus out of the 23 that they had collected, too small a
number for any conclusions to be drawn.
Different investigations performed in Attiki record a decline
of the P. neglectus populations over the years (Chaniotis et al.
1994; Ivovic et al. 2007; Papadopoulos and Tselentis 1994). A
possible explanation may be the expansion of the outer limits
of the city of Athens over the last decade, disrupting any potential breeding sites of P. neglectus, where populations were
much higher in the past, such as in quarries (Tselentis et al.
1994) and wells (Chaniotis and Tselentis 1996).
More of P. neglectus sand flies were collected in periurban
than in urban or rural areas, as concurred by other investigations in Attiki (Chaniotis et al. 1994; Chaniotis and Tselentis
1996) or elsewhere (Bosnic et al. 2006).
P. papatasi was fifth in frequency and is the main vector of
L. major (which has never been isolated from dogs in Greece)
and responsible for the three-day fever. Similarly, low ratios
for P. papatasi are reported in some investigations performed
in mainland Greece (Ivovic et al. 2007; Karanis et al. 2000)
and the islands of the Aegean and the Ionian Sea (Pesson et al.
1984). However, they differ from others carried out in Attiki
(Aransay et al. 2000; Chaniotis et al. 1994; Papadopoulos and
Tselentis 1994). Selection of different collection sites and trapping methods could explain these inconsistent results. In addition, these investigations did not incorporate many houses,
despite the fact that P. papatasi is commonly found within
dwellings.
Phlebotomus (Adlerius) simici was fourth in frequency in
our study. It can enter houses and can potentially transmit
L. infantum. Its percentage is higher than the one
Papadopoulos and Tselentis (1994) recorded in an investigation from the same area, but is in agreement with studies in
Attiki (Aransay et al. 2000; Chaniotis et al. 1994).
Disagreement with another study (Papadopoulos and
Tselentis 1994) could be attributed to the different sand fly
collection method (use of castor oil paper and not light traps).
P. simici, as opposed to the other sand fly species, is found
more frequently in rural areas and slightly less often in
periurban areas. It seems to avoid high temperatures while
no preference was observed regarding sunny, cloudy, or rainy
weather, in contrast with the rest of the species that favor
sunshine.
P. (Paraphlebotomus) similis was found in very small numbers in this study, in agreement with other investigations for
the same area (Aransay et al. 2000; Chaniotis et al. 1994;
Chaniotis and Tselentis 1996; Papadopoulos and Tselentis
1994), while others reported none at all (Aransay et al. 1999;
Ivovic et al. 2007). The small numbers of P. similis did not
allow for any conclusions to be drawn. Phlebotomus
(Paraphlebotomus) alexandri was extremely uncommon (only 17 phlebotomines were found), making any data assessment pointless. Previous studies in Attiki report its appearance
in small percentages (Aransay et al. 1999, 2000; Chaniotis
et al. 1994; Papadopoulos and Tselentis 1994), or none at all
(Chaniotis and Tselentis 1996; Ivovic et al. 2007).
Sergentomyia minuta is one of the three species that
belong to the genus Sergentomyia, reported in Greece. It
was second in frequency in this study, following P. tobbi.
This is the only species of the genus Sergentomyia that is
reported not only in Attiki (Aransay et al. 1999, 2000;
Chaniotis et al. 1994; Chaniotis and Tselentis 1996;
Ivovic et al. 2007; Papadopoulos and Tselentis 1994) but
also throughout Greece (Ivovic et al. 2007; Karanis et al.
2000; Leger et al. 1988).
Our study found S. minuta second in frequency, following
P. tobbi, in agreement with all other studies that showed similar high ratios. Most populations were located in rural areas,
where they are able to encounter lizards that said areas abound
with.
Because of the implication of sandflies in the transmission
of Leishmania, accurate identification of parasites found inside the vectors becomes indispensable for epidemiological
studies in order to identify control measures. Identification
Parasitol Res
of the parasite is based on morphological features, location of
promastigotes inside the intestinal tract of the vector, or on
culture results (Paiva et al. 2006). Furthermore, molecular
methods for detecting Leishmania-DNA in vectors offer greater sensitivity and specificity. In this study, only one of the 241
sandflies was found positive for L. infantum (0.41%). An investigation in Corfu showed a percentage of 0.12%, using
culture as an identification method (Aransay et al. 2000;
Leger et al. 1988). In another study (Aransay et al. 2000), a
greater percentage (5.4%) was detected in Attiki, using a seminested PCR assay, possibly due to the fact that all sand flies
were collected from the same stable and may have fed on the
same host. This fairly low percentage of Leishmania-DNA
positive phlebotomines in our study may be attributed to the
trapping and preservation methods employed (CDC light
traps—live insects, Onderstepoort light traps—dead insects
in water) and to the high percentages of infected humans
and dogs that other investigators report in the endemic areas
they studied, even though infection rates in Attiki may very
well be equally high, and finally to the unknown sand fly
species found in our study that perhaps do not transmit
L. infantum, L. tropica, or L. major.
Seasonal changes and climatic conditions are expected to
have an impact on sand fly populations. A 2-year study in
Italy, on the seasonality of sand flies, showed that variation
in numbers of the sand flies collected was attributed to the
changing climatic conditions (Rossi et al. 2008). P. tobbi
was found in 41 of the 46 sand fly traps, a fact indicating its
remarkable survivability in urbanized environments, densely
inhabited, periurban, or purely rural areas. Sand flies seem to
prefer (36.2%) former rural areas that have later been urbanized, with shady, humid environments with ample organic
matter to rest and reproduce.
Local climate (temperature, wind, rain, and altitude) is also
an influencing factor on sand fly distribution. Temperature is
one of the main factors that has an effect in the expansion of
either visceral or cutaneous human leishmaniasis (Kuhn 1999)
and canine leishmaniasis (Athanasiou et al. 2012). In our
study, it has been determined that sand flies favor sunshine
over rainy or cloudy weather.
In our study, no traps were installed in very high altitudes,
with the highest at 429 m, in Penteli area. Our results agree
with other studies in which P. tobbi is found predominantly
(96.4%) at low (0–400 m) altitudes (Simsek et al. 2007).
In our study, sandflies were found to be more abundant in
periurban areas, from June to September, in sunshine areas
with moderate to high temperatures and up to the highest
altitude of 429 m collected. Preventive measures such as
the use of insect repellants should be intensified during the
sand fly activity periods in areas with these characteristics
in order to minimize the risk of Leishmania transmission to
dogs, the primary reservoirs of the parasite and immunocompromised humans.
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