Do Different LED Colours Influence Sand Fly Collection by Light...
8
Research Article Do Different LED Colours Influence Sand Fly Collection by Light Trap in the Mediterranean? Gabriella Gaglio , Ettore Napoli, Francesca Arfuso, Jessica Maria Abbate, Salvatore Giannetto, and Emanuele Brianti Dipartimento di Scienze Veterinarie, University of Messina, Messina, Italy Correspondence should be addressed to Gabriella Gaglio; [email protected] Received 19 April 2018; Accepted 4 June 2018; Published 27 June 2018 Academic Editor: Stephen Munga Copyright © 2018 Gabriella Gaglio et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Light traps represent the most used attractive system to collect and monitor phlebotomine sand flies. Recent studies have suggested that light traps can be easily upgraded by the use of light-emitting diode (LED) with positive effects on trap design, weight, and battery life. However, scant data on the effect of different LED colours on the attractiveness to phlebotomine sand fly species are available in literature. In this study, the capture performances of light traps equipped with different LED colours on phlebotomine sand fly species indigenous in the Mediterranean area were evaluated. Phlebotomine sand fly collections were performed using a classical light trap (CLT), equipped with a traditional incandescent lamp, and five Laika 4.0 light traps supplied, each with LED of different colours and wavelengths: (i) white; (ii) red; (iii) green; (iv) blue; (v) UV. Light traps were set for three consecutive nights fortnightly from May to October 2017 and climate data recorded using a meteorological station. A total of 411 phlebotomine sand flies (191 males and 220 females), belonging to three different species, namely, Phlebotomus perniciosus (n= 298, 141 males and 157 females), Sergentomyia minuta (n=110, 48 males and 62 females), and Phlebotomus neglectus (n=3, 2 males and 1 females) were collected. Abundance of capture was influenced by colours of LED and time. e highest number of phlebotomine sand flies was captured on June (P<0.01) and by UV LED (P<0.01). As regard to species, P. perniciosus was mainly captured by UV LED on June (P<0.01). No effect of time (P>0.05) or LED colour (P>0.05) was recorded for S. minuta and P. neglectus. According to the results of the present study light trap equipped with UV LED can represent an effective tool for the capture of sand fly species in the Mediterranean area. 1. Introduction Phlebotomine sand flies (Diptera: Psychodidae) are small nocturnal insects that act as vectors of various infectious and parasitic agents including canine and human Leishmaniosis. ese insects play a crucial role in the epidemiology of relevant diseases being some of great veterinary and medical importance; their monitor and control are, therefore, of pivotal importance. e system for trapping phlebotomine sand flies can be categorized into attractive (e.g., light traps and CO 2 ) or pas- sive (e.g., sticky traps) traps, and the different methods may influence the capture outcomes including specific attraction to sand fly species in a given area [1]. Although phlebotomine sand flies are nocturnal/crepuscular insects and their flight activity increases in relation to the decrease of the daily light intensity [2], they are contemporarily attracted by artificial light; thus, light traps are largely employed for the collection of these insects. Interestingly, insects are attracted by light of different colours and intensity relating to their retina struc- ture and to the presence of photoreceptors. Honeybees, for instance, have three photoreceptors (i.e., ultraviolet, blue, and green); in butterfly the retinas have six or more photoreceptor classes [3]. It has been demonstrated that the eyes of the adult sand fly Lutzomyia longipalpis reacted maximally to light in the ultraviolet region (at 340 nm) with a secondary peak in the blue-green-yellow region at 520-546 nm [4]. Light trap methods have recently been improved by the use of light-emitting diode (LED) [5–8]. LED light traps have some advantages compared to traditional light trap models including the low electric consumption resulting in a longer battery life and in a longest lifetime of the lamp. e LED technology allows easily customizing the colour and the intensity of the light. Some authors showed that LED Hindawi BioMed Research International Volume 2018, Article ID 6432637, 7 pages https://doi.org/10.1155/2018/6432637
Transcript of Do Different LED Colours Influence Sand Fly Collection by Light...
Research ArticleDo Different LED Colours Influence Sand Fly Collection byLight Trap in the Mediterranean
Gabriella Gaglio Ettore Napoli Francesca Arfuso Jessica Maria AbbateSalvatore Giannetto and Emanuele Brianti
Dipartimento di Scienze Veterinarie University of Messina Messina Italy
Correspondence should be addressed to Gabriella Gaglio ggagliounimeit
Received 19 April 2018 Accepted 4 June 2018 Published 27 June 2018
Academic Editor Stephen Munga
Copyright copy 2018 Gabriella Gaglio et alThis is an open access article distributed under the Creative CommonsAttribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited
Light traps represent the most used attractive system to collect andmonitor phlebotomine sand flies Recent studies have suggestedthat light traps can be easily upgraded by the use of light-emitting diode (LED) with positive effects on trap design weight andbattery life However scant data on the effect of different LED colours on the attractiveness to phlebotomine sand fly species areavailable in literature In this study the capture performances of light traps equipped with different LED colours on phlebotominesand fly species indigenous in the Mediterranean area were evaluated Phlebotomine sand fly collections were performed using aclassical light trap (CLT) equipped with a traditional incandescent lamp and five Laika 40 light traps supplied each with LED ofdifferent colours and wavelengths (i) white (ii) red (iii) green (iv) blue (v) UV Light traps were set for three consecutive nightsfortnightly from May to October 2017 and climate data recorded using a meteorological station A total of 411 phlebotomine sandflies (191 males and 220 females) belonging to three different species namely Phlebotomus perniciosus (n= 298 141 males and 157females) Sergentomyia minuta (n=110 48 males and 62 females) and Phlebotomus neglectus (n=3 2 males and 1 females) werecollected Abundance of capture was influenced by colours of LED and time The highest number of phlebotomine sand flies wascaptured on June (Plt001) and by UV LED (Plt001) As regard to species P perniciosus was mainly captured by UV LED on June(Plt001) No effect of time (Pgt005) or LED colour (Pgt005) was recorded for S minuta and P neglectus According to the resultsof the present study light trap equipped with UV LED can represent an effective tool for the capture of sand fly species in theMediterranean area
1 Introduction
Phlebotomine sand flies (Diptera Psychodidae) are smallnocturnal insects that act as vectors of various infectious andparasitic agents including canine and human LeishmaniosisThese insects play a crucial role in the epidemiology ofrelevant diseases being some of great veterinary and medicalimportance their monitor and control are therefore ofpivotal importance
The system for trapping phlebotomine sand flies can becategorized into attractive (eg light traps and CO
2) or pas-
sive (eg sticky traps) traps and the different methods mayinfluence the capture outcomes including specific attractionto sand fly species in a given area [1] Although phlebotominesand flies are nocturnalcrepuscular insects and their flightactivity increases in relation to the decrease of the daily lightintensity [2] they are contemporarily attracted by artificial
light thus light traps are largely employed for the collectionof these insects Interestingly insects are attracted by light ofdifferent colours and intensity relating to their retina struc-ture and to the presence of photoreceptors Honeybees forinstance have three photoreceptors (ie ultraviolet blue andgreen) in butterfly the retinas have six ormore photoreceptorclasses [3] It has been demonstrated that the eyes of the adultsand fly Lutzomyia longipalpis reacted maximally to light inthe ultraviolet region (at 340 nm) with a secondary peak inthe blue-green-yellow region at 520-546 nm [4]
Light trap methods have recently been improved by theuse of light-emitting diode (LED) [5ndash8] LED light trapshave some advantages compared to traditional light trapmodels including the low electric consumption resulting ina longer battery life and in a longest lifetime of the lampThe LED technology allows easily customizing the colour andthe intensity of the light Some authors showed that LED
HindawiBioMed Research InternationalVolume 2018 Article ID 6432637 7 pageshttpsdoiorg10115520186432637
2 BioMed Research International
(a) (b)
Figure 1 Classical light trap (CLT) and five Laika traps equipped with red green white UV and blue LEDs placed in the study area (a)Diurnal vision (b) nocturnal vision
of different colours could have different power of attractiondemonstrating for instance that Phlebotomus papatasi ismore attracted by red LED [9] while Nyssomyia whitmaniand Lutzomyia longipalpis seem to be more attracted by blueand green LED respectively [10] However no data on theeffect of different LED colours on other Phlebotomus speciespresent in Mediterranean area are available in the literatureTherefore the aim of the present study is to evaluate thecapture performances of light traps equipped with differentLED colours to phlebotomine sand fly species endemic in theMediterranean area
2 Materials and Methods
21 Study Area and Collection Procedures The study wasconducted from May to October 2017 which corresponds tothe sand fly season in the study area [11] in the municipalityof Messina an area highly endemic for canine leishmaniosiswhere the presence of competent sand fly species has beenpreviously reported [11 12] The traps were placed in asuburban area nearby the horse stables of the Department ofVeterinary Sciences of theUniversity ofMessina (38∘1310158405910158401015840N15∘321015840489910158401015840E 263 m asl)
Sand fly collection was performed using both a clas-sical light trap (named CLT) equipped with a traditionalincandescent lamp (12V 8W) and five Laika 40 light trapssupplied eachwith LEDof different colours andwavelengths(i) white455 nm (ii) red620 nm (iii) green530 nm (iv)blue470 nm (v) UV395 nmThe six traps were set oppositeto a stonewall at 50 cm above the ground [11] and at about3 meters apart from each other (Figures 1(a) and 1(b)) BothCLT and LED traps were placed for three consecutive daystwice a month (six days per month) from May to October2017 Traps were switched-on before sunset (1800) and leftworking for 13 hours (up to 700 am) Net-bags of traps werecollected and replaced after each day of collection Tempera-ture (∘C) relative humidity (RH) and wind intensity (WI)were recorded using a meteorological station placed in thesame area of traps
22 SandFly Identification Phlebotomine sandflies collectedwere initially separated from other insects differentiated bysex and stored in vials containing 70 ethanol For species
identification the external genitalia of males and the headand posterior last tergites of females were dissected clearedand slide-mounted as described elsewhere [8] Identificationwas performed using morphological keys [13]
23 Data Analysis Due to the limited number of phle-botomine sand flies collected in each sampling session thedata were merged according to the month of capture Two-way analysis of variance (ANOVA) was applied in order toevaluate the effect of time (ie month) and traps (ie CLTor LED traps) on abundance and sand fly species Whensignificant differences were found Bonferronirsquos post hoccomparison was applied
For the best represented species Pearsonrsquos chi-squareanalysis was applied to evaluate statistically significant differ-ence in the number of male and female specimens
Statistical significant values were set for 119875 values lt 005The statistical analyses were performed using the STATIS-TICA software package (STATISTICA 7 for Windows StatSoftware Inc Tulsa Oklahoma)
3 Results
A total of thirty-six sampling days were carried out through-out the study but no phlebotomine sandflieswere captured inthe first four (May) and in the last six capture days (October)The number of captured phlebotomine sand flies along withenvironmental parameters recorded during the samplingdays are summarized in Table 1 Overall 411 specimensbelonging to three different species namely Phlebotomusperniciosus (n= 298 141 males and 157 females) Sergentomyiaminuta (n=110 48 males and 62 females) and Phleboto-mus neglectus (n=3 2 males and 1 females) were collected(Table 2) A statistically significant effect of time (month)and trap model found that the highest number of specimenswas collected in the month of June and by blue LED UVLED and CLT (Figure 2) Similarly in regard to species Pperniciosus was mainly captured in June (Plt001) and by UVLED (Figure 3) no differences in the number of male andfemale specimens of P perniciosus captured by the threemoreefficient traps (ie blue LED UV LED and CLT traps) wereobserved (Figure 4) Neither effect of sampling period norof trap model was found on the number of S minuta and Pneglectus captured during the study
BioMed Research International 3
Table 1 Number of phlebotomine sand flies captured in the study along with environmental parameters recorded during the trapping daysEnvironmental parameters are provided as means of values recorded during each trapping day (ie from 6 pm to 7 am)
Month Sampling day Sand fly number Temperature(∘C)
RelativeHumidity ()
Wind Intensity(kmh)
May
15 0 23 46 2316 0 24 64 1817 0 22 58 2024 0 23 63 2425 15 21 57 1726 13 25 49 12
June
13 41 24 57 2114 29 25 49 2815 46 24 61 2627 61 28 55 1028 12 29 50 1330 24 28 63 14
July
11 10 31 45 1712 10 33 36 1913 15 30 60 2625 3 25 73 2526 7 25 67 1927 4 27 54 22
August
1 7 33 30 192 6 33 28 213 3 34 27 2729 9 25 87 1730 39 23 84 1131 12 24 74 10
September
11 14 24 73 1912 8 22 84 2013 2 27 50 1825 8 22 62 1526 10 22 64 927 3 21 82 9
October
9 0 17 88 810 0 19 96 1011 0 26 68 1316 0 20 57 917 0 20 65 918 0 21 61 18
4 Discussions
The advent of LED technology has substantially improvedlight trap performances Despite the fact that previous sur-veys have demonstrated how light trap using LED tech-nologies can be valid alternative to classical models theattractiveness of different colours LED has not been exploredin deep so far The present study investigated the captureperformances of light trap equipped with LED of differentcolour and wavelength on sand fly species endemic in the
Mediterranean area According to the herein results itmay bespeculated that light trap equipped with UV LED of 395 nmhas a higher attractiveness compared to other coloured LEDtrapsThis is particularly evident for the species P perniciosuswhich is one of the main vectors of leishmaniosis by Linfantum to both humans and dogs [14]
The species captured in the present survey are the samereported in other previous investigations performed in thesame area [11 12 15] where P perniciosus and S minuta werethe most abundant species Though the well-known role of
4 BioMed Research International
Table2Num
bera
ndpercentageso
fphlebotom
ines
andfly
speciesc
apturedby
each
trap
mod
elin
thes
tudy
Traps
Species
Stud
yperiod
May
ntotal()
June
ntotal()
July
ntotal()
Augu
stntotal()
Septem
ber
ntotal()
blue
LED
Phleb
otom
usperniciosus
15(20)
2030(667)
311(273
)918
(50)
46(667)
Sergentomyiaminuta
45(80)
1030(333)
811(727)
918
(50)
26(333)
Phleb
otom
usnegle
ctus
05(0)
030
(0)
011(0)
018
(0)
06(0)
UVLE
DPh
lebotom
usperniciosus
1011
(909)
104116
(897
)89(971)
1418
(778
)610
(60)
Sergentomyiaminuta
111(91
)1211
6(103)
19(29)
418
(222)
410
(40)
Phleb
otom
usnegle
ctus
011(0)
0116
(0)
09(0)
018
(0)
010
(0)
whiteLE
DPh
lebotom
usperniciosus
22(100)
915
(60)
04(0)
912
(75)
11(100)
Sergentomyiaminuta
02(0)
515
(333)
44(100)
312
(25)
01(0)
Phleb
otom
usnegle
ctus
02(0)
115(67)
04(0)
012
(0)
01(0)
greenLE
DPh
lebotom
usperniciosus
13(333)
24(50)
310
(30)
05(0)
45(80)
Sergentomyiaminuta
23(667)
24(50)
710
(70)
55(100)
05(0)
Phleb
otom
usnegle
ctus
03(0)
04(0)
010
(0)
05(0)
15(20)
redLE
DPh
lebotom
usperniciosus
12(50)
1014
(714
)06(0)
05(0)
25(40)
Sergentomyiaminuta
12(50)
414
(286)
66(100)
55(100)
25(40)
Phleb
otom
usnegle
ctus
02(0)
014
(0)
06(0)
05(0)
15(20)
CLT
Phleb
otom
usperniciosus
55(100)
3334(971)
59(556)
1518
(833)
1718
(971)
Sergentomyiaminuta
05(0)
134(29)
49(444)
318
(167)
118(29)
Phleb
otom
usnegle
ctus
05(0)
034
(0)
09(0)
018
(0)
018
(0)
Legend
blueL
EDU
VLE
Dw
hiteLE
Dgreen
LEDred
LED=Laikatraps
equipp
edwith
blueU
Vwhitegreen
andredLE
Dsrespectively
CLT
=Classic
allight
trap
equipp
edwith
incand
escent
lamp
BioMed Research International 5
Figure 2 Total number of phlebotomine sand flies captured byclassical light trap (CLT) and five Laika traps equipped with redgreen white UV and blue LEDs
Figure 3 Total number of Phlebotomus perniciosus captured byclassical light trap (CLT) and blue and UV Laika traps
P perniciosus is being competent vector of L infantum thatof S minuta is still unclear and needs further investigationsRecently [16] reported the first molecular detection of Linfantum in S minuta in southern Portugal and the firstisolation of human blood as meal source in an engorgedfemale of S minuta These findings opened a debate on thepotential role of this species in the transmission of leish-maniosis and its involvement in the epidemiology deservesfurther researches including but not limited to protozoanisolation from engorged specimens as well as experimentaltransmission
The limited presence of P neglectus here observed isconsistent with previous reports in southern Italy [11 17]and justified by the higher abundance of this species innorthern Italian regions which are featured by cooler climate[18 19]
The attractiveness of different light technologies andcolours could bias the estimation of sand fly populationin a specific area In fact as demonstrated by a studythat compared the attractiveness of different LED coloursPhlebotomus papatasi was attracted four times more by redLED compared to blue and green and twice with respectto incandescent lamp [9] A study performed in Brazil
demonstrated that Hoover Pugedo light traps equipped withgreen or blue LED or incandescent lamps showed the sameattractiveness power for Nyssomyia whitmani and Lutzomyialongipalpis [10] In another study the CDC and Disney trapswere respectively more efficient in the capture of Lutzomyiaovallesi and Lutzomyia olmeca olmeca compared to LED lighttrap [20] In a previous study conducted by our group [8] theattractiveness of a Laika trap equipped with both white andUV LED was compared to CLT no significant differences inthe trapping performance of the two traps were recorded inthat study Here the Laika model equipped with UV LEDshowed the best capture performances in general and to Pperniciosus in particular These findings suggest that the eyesof P perniciosus react maximally to light in the ultravioletregion as already observed for Lutzomyia longipalpis [4]However spectral sensitivities using electroretinograms needto be determined in order to clarify whether the greaterattractiveness of the UV LED for this species is linked to ahigher sensitivity of the eyes to wavelength of the ultravioletregion (395 nm) or to the low brightness emitted by this LEDcolour
In addition to trapping methods sand fly abundance andrichness may be influenced considerably by other variablesincluding animalsrsquo presence and environmental and climatevariables [21] In particular the environmental factors havebeen used to predict and elucidate the distribution of diseasestransmitted by vectors [22] The climatic factors includingtemperature humidity wind and rainfall could influence thedistribution of vectors including sand fly species [22 23]A previous study conducted in the same area recorded twopeaks of sand fly collection on August and September [11]in the present study instead only one peak was observed inthe month of June Moreover phlebotomine sand flies werecaptured earlier in the here survey compared to the aforemen-tioned study in which the first positive trapping session wasobserved in late June In regard to this difference it is inter-esting to notice that the summer season in which the presentstudy was conducted was featured by very hot temperatureespecially in July (286 plusmn 32∘C) and August (288 plusmn 50) andhigh humidity in September (693 plusmn 131) and October (725plusmn 156) caused by intense rains These particular climaticconditions may explain the decline in the number of sandflies during the hottest months and their complete absence inOctober
In conclusion this study showed how light trap equippedwith UV LED of 395 nm has superior performances toother LED traps equipped with blue or green or white orred lamps for the capture of sand flies including importantLeishmania vector species such as P perniciosus By virtueof their performances and technology UV LED trap mayrepresent a highly efficient alternative to CLT for the captureand monitoring of the sand fly species endemic in theMediterranean
Data Availability
Data supporting the findings of this study is included withinthe article
6 BioMed Research International
Figure 4 Number of males and females of Phlebotomus perniciosus captured by classical light trap (CLT) and blue and UV Laika trap alongwith results of Pearsonrsquos chi-square test
Conflicts of Interest
The authors declare that they have no conflicts of interest
Authorsrsquo Contributions
Ettore Napoli and Francesca Arfuso contributed equally tothis paper
Acknowledgments
The authors thank Eng Leonardo Spacone of Laika Lab forproviding the traps and the meteorological station used inthis study
References
[1] B Alexander ldquoSampling method for phlebotomine sandfliesrdquoMedical and Veterinary Entomology vol 14 pp 109ndash122 2000
[2] B N Chaniotis M A Correa R B Tesh and K M John-son ldquoDaily and seasonal man-biting activity of phlebotomine
sandflies in Panamardquo Journal of Medical Entomology vol 8 no4 pp 415ndash420 1971
[3] K Arikawa ldquoThe eyes and vision of butterfliesrdquo The Journal ofPhysiology vol 595 no 16 pp 5457ndash5464 2017
[4] H E Mellor J G C Hamilton and M Anderson ldquoSpectralsensitivity in the eyes of male and female Lutzomyia longipalpissandfliesrdquoMedical and Veterinary Entomology vol 10 no 4 pp371ndash374 1996
[5] L W Cohnstaedt J I Gillen and L E Munstermann ldquoLight-emitting diode technology improves insect trappingrdquo Journal ofthe American Mosquito Control Association vol 24 no 2 pp331ndash334 2008
[6] R S Mann P E Kaufman and J F Butler ldquoLutzomyia spp(Diptera Psychodidae) response to olfactory attractant- andlight emitting diode-modified mosquito magnet X (MM-X)trapsrdquo Journal of Medical Entomology vol 46 no 5 pp 1052ndash1061 2009
[7] G C Muller J A Hogsette D L Kline J C Beier E E Revayand R-D Xue ldquoResponse of the sand fly Phlebotomus papatasito visual physical and chemical attraction features in the fieldrdquoActa Tropica vol 141 pp 32ndash36 2015
BioMed Research International 7
[8] G Gaglio E Napoli L Falsone S Giannetto and E BriantildquoField evaluation of a new light trap for phlebotomine sandfliesrdquo Acta Tropica vol 174 pp 114ndash117 2017
[9] D F Hoel J F Butler E Y Fawaz N Watany S S El-Hossaryand J Villinski ldquoResponse of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egyptrdquo Journalof Vector Ecology vol 32 no 2 pp 302ndash307 2007
[10] F S Silva J M Brito B M Costa-Neta and S E P D LoboldquoEvaluation of light-emitting diodes as attractant for sandflies(Diptera Psychodidae Phlebotominae) in northeastern BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 110 no 6 pp 801ndash8032015
[11] G Gaglio E Brianti E Napoli et al ldquoEffect of night time-intervals height of traps and lunar phases on sand fly collectionin a highly endemic area for canine leishmaniasisrdquoActa Tropicavol 133 no 1 pp 73ndash77 2014
[12] E Brianti G Gaglio E Napoli et al ldquoEfficacy of a slow-releaseimidacloprid (10)flumethrin (45) collar for the preventionof canine leishmaniosisrdquo Parasites amp Vectors vol 7 no 1 article327 2014
[13] F Dantas-Torres V D Tarallo and D Otranto ldquoMorphologicalkeys for the identification of Italian phlebotomine sand flies(Diptera Psychodidae Phlebotominae)rdquo Parasites amp Vectorsvol 7 no 1 article 479 2014
[14] M Maroli M D Feliciangeli L Bichaud R N Charrel andL Gradoni ldquoPhlebotomine sand flies and the spreading ofleishmaniases and other diseases of public health concernrdquoMedical and Veterinary Entomology vol 27 no 2 pp 123ndash1472013
[15] O Lisi V DrsquoUrso V Vaccalluzzo et al ldquoPersistence of phle-botomine Leishmania vectors in urban sites of Catania (SicilyItaly)rdquo Parasites amp Vectors vol 7 no 1 article 560 2014
[16] S Pereira D Pita-Pereira T Araujo-Pereira et al ldquoFirstmolecular detection of Leishmania infantum in Sergentomyiaminuta (Diptera Psychodidae) in Alentejo southern PortugalrdquoActa Tropica vol 174 pp 45ndash48 2017
[17] F Dantas-Torres V D Tarallo M S Latrofa A Falchi R PLia and D Otranto ldquoEcology of phlebotomine sand flies andLeishmania infantum infection in a rural area of southern ItalyrdquoActa Tropica vol 137 pp 67ndash73 2014
[18] M Signorini M Drigo F Marcer et al ldquoComparative fieldstudy to evaluate the performance of three different traps forcollecting sand flies in northeastern Italyrdquo Journal of VectorEcology vol 38 no 2 pp 374ndash378 2013
[19] M Maroli L Rossi R Baldelli et al ldquoThe northward spread ofleishmaniasis in Italy evidence from retrospective and ongoingstudies on the canine reservoir and phlebotomine vectorsrdquoTropical Medicine amp International Health vol 13 no 2 pp 256ndash264 2008
[20] J J Rodrıguez-Rojas W Arque-Chunga I Fernandez-Salasand E A Rebollar-Tellez ldquoComparative field evaluation ofdifferent traps for collecting adult phlebotomine sand flies(Diptera Psychodidae) in an endemic area of cutaneous leish-maniasis in Quintana Roo Mexicordquo Journal of the AmericanMosquito Control Association vol 32 no 2 pp 103ndash116 2016
[21] J Ghrab A Rhim D Bach-Hamba et al ldquoPhlebotomi-nae (Diptera Psychodidae) of human leishmaniosis sites inTunisiardquo Parasite vol 13 no 1 pp 23ndash33 2006
[22] A Y M Abdullah A Dewan M R I Shogib M M Rahmanand M F Hossain ldquoEnvironmental factors associated withthe distribution of visceral leishmaniasis in endemic areas of
Bangladesh modeling the ecological nicherdquo Tropical Medicineand Health vol 45 no 1 article 13 2017
[23] L Chamaille A Tran A Meunier G Bourdoiseau P Readyand J-P Dedet ldquoEnvironmental risk mapping of canine leish-maniasis in Francerdquo Parasites amp Vectors vol 3 no 1 article 312010
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2 BioMed Research International
(a) (b)
Figure 1 Classical light trap (CLT) and five Laika traps equipped with red green white UV and blue LEDs placed in the study area (a)Diurnal vision (b) nocturnal vision
of different colours could have different power of attractiondemonstrating for instance that Phlebotomus papatasi ismore attracted by red LED [9] while Nyssomyia whitmaniand Lutzomyia longipalpis seem to be more attracted by blueand green LED respectively [10] However no data on theeffect of different LED colours on other Phlebotomus speciespresent in Mediterranean area are available in the literatureTherefore the aim of the present study is to evaluate thecapture performances of light traps equipped with differentLED colours to phlebotomine sand fly species endemic in theMediterranean area
2 Materials and Methods
21 Study Area and Collection Procedures The study wasconducted from May to October 2017 which corresponds tothe sand fly season in the study area [11] in the municipalityof Messina an area highly endemic for canine leishmaniosiswhere the presence of competent sand fly species has beenpreviously reported [11 12] The traps were placed in asuburban area nearby the horse stables of the Department ofVeterinary Sciences of theUniversity ofMessina (38∘1310158405910158401015840N15∘321015840489910158401015840E 263 m asl)
Sand fly collection was performed using both a clas-sical light trap (named CLT) equipped with a traditionalincandescent lamp (12V 8W) and five Laika 40 light trapssupplied eachwith LEDof different colours andwavelengths(i) white455 nm (ii) red620 nm (iii) green530 nm (iv)blue470 nm (v) UV395 nmThe six traps were set oppositeto a stonewall at 50 cm above the ground [11] and at about3 meters apart from each other (Figures 1(a) and 1(b)) BothCLT and LED traps were placed for three consecutive daystwice a month (six days per month) from May to October2017 Traps were switched-on before sunset (1800) and leftworking for 13 hours (up to 700 am) Net-bags of traps werecollected and replaced after each day of collection Tempera-ture (∘C) relative humidity (RH) and wind intensity (WI)were recorded using a meteorological station placed in thesame area of traps
22 SandFly Identification Phlebotomine sandflies collectedwere initially separated from other insects differentiated bysex and stored in vials containing 70 ethanol For species
identification the external genitalia of males and the headand posterior last tergites of females were dissected clearedand slide-mounted as described elsewhere [8] Identificationwas performed using morphological keys [13]
23 Data Analysis Due to the limited number of phle-botomine sand flies collected in each sampling session thedata were merged according to the month of capture Two-way analysis of variance (ANOVA) was applied in order toevaluate the effect of time (ie month) and traps (ie CLTor LED traps) on abundance and sand fly species Whensignificant differences were found Bonferronirsquos post hoccomparison was applied
For the best represented species Pearsonrsquos chi-squareanalysis was applied to evaluate statistically significant differ-ence in the number of male and female specimens
Statistical significant values were set for 119875 values lt 005The statistical analyses were performed using the STATIS-TICA software package (STATISTICA 7 for Windows StatSoftware Inc Tulsa Oklahoma)
3 Results
A total of thirty-six sampling days were carried out through-out the study but no phlebotomine sandflieswere captured inthe first four (May) and in the last six capture days (October)The number of captured phlebotomine sand flies along withenvironmental parameters recorded during the samplingdays are summarized in Table 1 Overall 411 specimensbelonging to three different species namely Phlebotomusperniciosus (n= 298 141 males and 157 females) Sergentomyiaminuta (n=110 48 males and 62 females) and Phleboto-mus neglectus (n=3 2 males and 1 females) were collected(Table 2) A statistically significant effect of time (month)and trap model found that the highest number of specimenswas collected in the month of June and by blue LED UVLED and CLT (Figure 2) Similarly in regard to species Pperniciosus was mainly captured in June (Plt001) and by UVLED (Figure 3) no differences in the number of male andfemale specimens of P perniciosus captured by the threemoreefficient traps (ie blue LED UV LED and CLT traps) wereobserved (Figure 4) Neither effect of sampling period norof trap model was found on the number of S minuta and Pneglectus captured during the study
BioMed Research International 3
Table 1 Number of phlebotomine sand flies captured in the study along with environmental parameters recorded during the trapping daysEnvironmental parameters are provided as means of values recorded during each trapping day (ie from 6 pm to 7 am)
Month Sampling day Sand fly number Temperature(∘C)
RelativeHumidity ()
Wind Intensity(kmh)
May
15 0 23 46 2316 0 24 64 1817 0 22 58 2024 0 23 63 2425 15 21 57 1726 13 25 49 12
June
13 41 24 57 2114 29 25 49 2815 46 24 61 2627 61 28 55 1028 12 29 50 1330 24 28 63 14
July
11 10 31 45 1712 10 33 36 1913 15 30 60 2625 3 25 73 2526 7 25 67 1927 4 27 54 22
August
1 7 33 30 192 6 33 28 213 3 34 27 2729 9 25 87 1730 39 23 84 1131 12 24 74 10
September
11 14 24 73 1912 8 22 84 2013 2 27 50 1825 8 22 62 1526 10 22 64 927 3 21 82 9
October
9 0 17 88 810 0 19 96 1011 0 26 68 1316 0 20 57 917 0 20 65 918 0 21 61 18
4 Discussions
The advent of LED technology has substantially improvedlight trap performances Despite the fact that previous sur-veys have demonstrated how light trap using LED tech-nologies can be valid alternative to classical models theattractiveness of different colours LED has not been exploredin deep so far The present study investigated the captureperformances of light trap equipped with LED of differentcolour and wavelength on sand fly species endemic in the
Mediterranean area According to the herein results itmay bespeculated that light trap equipped with UV LED of 395 nmhas a higher attractiveness compared to other coloured LEDtrapsThis is particularly evident for the species P perniciosuswhich is one of the main vectors of leishmaniosis by Linfantum to both humans and dogs [14]
The species captured in the present survey are the samereported in other previous investigations performed in thesame area [11 12 15] where P perniciosus and S minuta werethe most abundant species Though the well-known role of
4 BioMed Research International
Table2Num
bera
ndpercentageso
fphlebotom
ines
andfly
speciesc
apturedby
each
trap
mod
elin
thes
tudy
Traps
Species
Stud
yperiod
May
ntotal()
June
ntotal()
July
ntotal()
Augu
stntotal()
Septem
ber
ntotal()
blue
LED
Phleb
otom
usperniciosus
15(20)
2030(667)
311(273
)918
(50)
46(667)
Sergentomyiaminuta
45(80)
1030(333)
811(727)
918
(50)
26(333)
Phleb
otom
usnegle
ctus
05(0)
030
(0)
011(0)
018
(0)
06(0)
UVLE
DPh
lebotom
usperniciosus
1011
(909)
104116
(897
)89(971)
1418
(778
)610
(60)
Sergentomyiaminuta
111(91
)1211
6(103)
19(29)
418
(222)
410
(40)
Phleb
otom
usnegle
ctus
011(0)
0116
(0)
09(0)
018
(0)
010
(0)
whiteLE
DPh
lebotom
usperniciosus
22(100)
915
(60)
04(0)
912
(75)
11(100)
Sergentomyiaminuta
02(0)
515
(333)
44(100)
312
(25)
01(0)
Phleb
otom
usnegle
ctus
02(0)
115(67)
04(0)
012
(0)
01(0)
greenLE
DPh
lebotom
usperniciosus
13(333)
24(50)
310
(30)
05(0)
45(80)
Sergentomyiaminuta
23(667)
24(50)
710
(70)
55(100)
05(0)
Phleb
otom
usnegle
ctus
03(0)
04(0)
010
(0)
05(0)
15(20)
redLE
DPh
lebotom
usperniciosus
12(50)
1014
(714
)06(0)
05(0)
25(40)
Sergentomyiaminuta
12(50)
414
(286)
66(100)
55(100)
25(40)
Phleb
otom
usnegle
ctus
02(0)
014
(0)
06(0)
05(0)
15(20)
CLT
Phleb
otom
usperniciosus
55(100)
3334(971)
59(556)
1518
(833)
1718
(971)
Sergentomyiaminuta
05(0)
134(29)
49(444)
318
(167)
118(29)
Phleb
otom
usnegle
ctus
05(0)
034
(0)
09(0)
018
(0)
018
(0)
Legend
blueL
EDU
VLE
Dw
hiteLE
Dgreen
LEDred
LED=Laikatraps
equipp
edwith
blueU
Vwhitegreen
andredLE
Dsrespectively
CLT
=Classic
allight
trap
equipp
edwith
incand
escent
lamp
BioMed Research International 5
Figure 2 Total number of phlebotomine sand flies captured byclassical light trap (CLT) and five Laika traps equipped with redgreen white UV and blue LEDs
Figure 3 Total number of Phlebotomus perniciosus captured byclassical light trap (CLT) and blue and UV Laika traps
P perniciosus is being competent vector of L infantum thatof S minuta is still unclear and needs further investigationsRecently [16] reported the first molecular detection of Linfantum in S minuta in southern Portugal and the firstisolation of human blood as meal source in an engorgedfemale of S minuta These findings opened a debate on thepotential role of this species in the transmission of leish-maniosis and its involvement in the epidemiology deservesfurther researches including but not limited to protozoanisolation from engorged specimens as well as experimentaltransmission
The limited presence of P neglectus here observed isconsistent with previous reports in southern Italy [11 17]and justified by the higher abundance of this species innorthern Italian regions which are featured by cooler climate[18 19]
The attractiveness of different light technologies andcolours could bias the estimation of sand fly populationin a specific area In fact as demonstrated by a studythat compared the attractiveness of different LED coloursPhlebotomus papatasi was attracted four times more by redLED compared to blue and green and twice with respectto incandescent lamp [9] A study performed in Brazil
demonstrated that Hoover Pugedo light traps equipped withgreen or blue LED or incandescent lamps showed the sameattractiveness power for Nyssomyia whitmani and Lutzomyialongipalpis [10] In another study the CDC and Disney trapswere respectively more efficient in the capture of Lutzomyiaovallesi and Lutzomyia olmeca olmeca compared to LED lighttrap [20] In a previous study conducted by our group [8] theattractiveness of a Laika trap equipped with both white andUV LED was compared to CLT no significant differences inthe trapping performance of the two traps were recorded inthat study Here the Laika model equipped with UV LEDshowed the best capture performances in general and to Pperniciosus in particular These findings suggest that the eyesof P perniciosus react maximally to light in the ultravioletregion as already observed for Lutzomyia longipalpis [4]However spectral sensitivities using electroretinograms needto be determined in order to clarify whether the greaterattractiveness of the UV LED for this species is linked to ahigher sensitivity of the eyes to wavelength of the ultravioletregion (395 nm) or to the low brightness emitted by this LEDcolour
In addition to trapping methods sand fly abundance andrichness may be influenced considerably by other variablesincluding animalsrsquo presence and environmental and climatevariables [21] In particular the environmental factors havebeen used to predict and elucidate the distribution of diseasestransmitted by vectors [22] The climatic factors includingtemperature humidity wind and rainfall could influence thedistribution of vectors including sand fly species [22 23]A previous study conducted in the same area recorded twopeaks of sand fly collection on August and September [11]in the present study instead only one peak was observed inthe month of June Moreover phlebotomine sand flies werecaptured earlier in the here survey compared to the aforemen-tioned study in which the first positive trapping session wasobserved in late June In regard to this difference it is inter-esting to notice that the summer season in which the presentstudy was conducted was featured by very hot temperatureespecially in July (286 plusmn 32∘C) and August (288 plusmn 50) andhigh humidity in September (693 plusmn 131) and October (725plusmn 156) caused by intense rains These particular climaticconditions may explain the decline in the number of sandflies during the hottest months and their complete absence inOctober
In conclusion this study showed how light trap equippedwith UV LED of 395 nm has superior performances toother LED traps equipped with blue or green or white orred lamps for the capture of sand flies including importantLeishmania vector species such as P perniciosus By virtueof their performances and technology UV LED trap mayrepresent a highly efficient alternative to CLT for the captureand monitoring of the sand fly species endemic in theMediterranean
Data Availability
Data supporting the findings of this study is included withinthe article
6 BioMed Research International
Figure 4 Number of males and females of Phlebotomus perniciosus captured by classical light trap (CLT) and blue and UV Laika trap alongwith results of Pearsonrsquos chi-square test
Conflicts of Interest
The authors declare that they have no conflicts of interest
Authorsrsquo Contributions
Ettore Napoli and Francesca Arfuso contributed equally tothis paper
Acknowledgments
The authors thank Eng Leonardo Spacone of Laika Lab forproviding the traps and the meteorological station used inthis study
References
[1] B Alexander ldquoSampling method for phlebotomine sandfliesrdquoMedical and Veterinary Entomology vol 14 pp 109ndash122 2000
[2] B N Chaniotis M A Correa R B Tesh and K M John-son ldquoDaily and seasonal man-biting activity of phlebotomine
sandflies in Panamardquo Journal of Medical Entomology vol 8 no4 pp 415ndash420 1971
[3] K Arikawa ldquoThe eyes and vision of butterfliesrdquo The Journal ofPhysiology vol 595 no 16 pp 5457ndash5464 2017
[4] H E Mellor J G C Hamilton and M Anderson ldquoSpectralsensitivity in the eyes of male and female Lutzomyia longipalpissandfliesrdquoMedical and Veterinary Entomology vol 10 no 4 pp371ndash374 1996
[5] L W Cohnstaedt J I Gillen and L E Munstermann ldquoLight-emitting diode technology improves insect trappingrdquo Journal ofthe American Mosquito Control Association vol 24 no 2 pp331ndash334 2008
[6] R S Mann P E Kaufman and J F Butler ldquoLutzomyia spp(Diptera Psychodidae) response to olfactory attractant- andlight emitting diode-modified mosquito magnet X (MM-X)trapsrdquo Journal of Medical Entomology vol 46 no 5 pp 1052ndash1061 2009
[7] G C Muller J A Hogsette D L Kline J C Beier E E Revayand R-D Xue ldquoResponse of the sand fly Phlebotomus papatasito visual physical and chemical attraction features in the fieldrdquoActa Tropica vol 141 pp 32ndash36 2015
BioMed Research International 7
[8] G Gaglio E Napoli L Falsone S Giannetto and E BriantildquoField evaluation of a new light trap for phlebotomine sandfliesrdquo Acta Tropica vol 174 pp 114ndash117 2017
[9] D F Hoel J F Butler E Y Fawaz N Watany S S El-Hossaryand J Villinski ldquoResponse of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egyptrdquo Journalof Vector Ecology vol 32 no 2 pp 302ndash307 2007
[10] F S Silva J M Brito B M Costa-Neta and S E P D LoboldquoEvaluation of light-emitting diodes as attractant for sandflies(Diptera Psychodidae Phlebotominae) in northeastern BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 110 no 6 pp 801ndash8032015
[11] G Gaglio E Brianti E Napoli et al ldquoEffect of night time-intervals height of traps and lunar phases on sand fly collectionin a highly endemic area for canine leishmaniasisrdquoActa Tropicavol 133 no 1 pp 73ndash77 2014
[12] E Brianti G Gaglio E Napoli et al ldquoEfficacy of a slow-releaseimidacloprid (10)flumethrin (45) collar for the preventionof canine leishmaniosisrdquo Parasites amp Vectors vol 7 no 1 article327 2014
[13] F Dantas-Torres V D Tarallo and D Otranto ldquoMorphologicalkeys for the identification of Italian phlebotomine sand flies(Diptera Psychodidae Phlebotominae)rdquo Parasites amp Vectorsvol 7 no 1 article 479 2014
[14] M Maroli M D Feliciangeli L Bichaud R N Charrel andL Gradoni ldquoPhlebotomine sand flies and the spreading ofleishmaniases and other diseases of public health concernrdquoMedical and Veterinary Entomology vol 27 no 2 pp 123ndash1472013
[15] O Lisi V DrsquoUrso V Vaccalluzzo et al ldquoPersistence of phle-botomine Leishmania vectors in urban sites of Catania (SicilyItaly)rdquo Parasites amp Vectors vol 7 no 1 article 560 2014
[16] S Pereira D Pita-Pereira T Araujo-Pereira et al ldquoFirstmolecular detection of Leishmania infantum in Sergentomyiaminuta (Diptera Psychodidae) in Alentejo southern PortugalrdquoActa Tropica vol 174 pp 45ndash48 2017
[17] F Dantas-Torres V D Tarallo M S Latrofa A Falchi R PLia and D Otranto ldquoEcology of phlebotomine sand flies andLeishmania infantum infection in a rural area of southern ItalyrdquoActa Tropica vol 137 pp 67ndash73 2014
[18] M Signorini M Drigo F Marcer et al ldquoComparative fieldstudy to evaluate the performance of three different traps forcollecting sand flies in northeastern Italyrdquo Journal of VectorEcology vol 38 no 2 pp 374ndash378 2013
[19] M Maroli L Rossi R Baldelli et al ldquoThe northward spread ofleishmaniasis in Italy evidence from retrospective and ongoingstudies on the canine reservoir and phlebotomine vectorsrdquoTropical Medicine amp International Health vol 13 no 2 pp 256ndash264 2008
[20] J J Rodrıguez-Rojas W Arque-Chunga I Fernandez-Salasand E A Rebollar-Tellez ldquoComparative field evaluation ofdifferent traps for collecting adult phlebotomine sand flies(Diptera Psychodidae) in an endemic area of cutaneous leish-maniasis in Quintana Roo Mexicordquo Journal of the AmericanMosquito Control Association vol 32 no 2 pp 103ndash116 2016
[21] J Ghrab A Rhim D Bach-Hamba et al ldquoPhlebotomi-nae (Diptera Psychodidae) of human leishmaniosis sites inTunisiardquo Parasite vol 13 no 1 pp 23ndash33 2006
[22] A Y M Abdullah A Dewan M R I Shogib M M Rahmanand M F Hossain ldquoEnvironmental factors associated withthe distribution of visceral leishmaniasis in endemic areas of
Bangladesh modeling the ecological nicherdquo Tropical Medicineand Health vol 45 no 1 article 13 2017
[23] L Chamaille A Tran A Meunier G Bourdoiseau P Readyand J-P Dedet ldquoEnvironmental risk mapping of canine leish-maniasis in Francerdquo Parasites amp Vectors vol 3 no 1 article 312010
Hindawiwwwhindawicom
International Journal of
Volume 2018
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Hindawiwwwhindawicom Volume 2018
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Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
BioinformaticsAdvances in
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Hindawiwwwhindawicom Volume 2018
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Hindawiwwwhindawicom Volume 2018
BioMed Research International
Cell BiologyInternational Journal of
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Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
ArchaeaHindawiwwwhindawicom Volume 2018
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Genetics Research International
Hindawiwwwhindawicom Volume 2018
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Hindawiwwwhindawicom Volume 2018
International Journal of
MicrobiologyHindawiwwwhindawicom
Nucleic AcidsJournal of
Volume 2018
Submit your manuscripts atwwwhindawicom
BioMed Research International 3
Table 1 Number of phlebotomine sand flies captured in the study along with environmental parameters recorded during the trapping daysEnvironmental parameters are provided as means of values recorded during each trapping day (ie from 6 pm to 7 am)
Month Sampling day Sand fly number Temperature(∘C)
RelativeHumidity ()
Wind Intensity(kmh)
May
15 0 23 46 2316 0 24 64 1817 0 22 58 2024 0 23 63 2425 15 21 57 1726 13 25 49 12
June
13 41 24 57 2114 29 25 49 2815 46 24 61 2627 61 28 55 1028 12 29 50 1330 24 28 63 14
July
11 10 31 45 1712 10 33 36 1913 15 30 60 2625 3 25 73 2526 7 25 67 1927 4 27 54 22
August
1 7 33 30 192 6 33 28 213 3 34 27 2729 9 25 87 1730 39 23 84 1131 12 24 74 10
September
11 14 24 73 1912 8 22 84 2013 2 27 50 1825 8 22 62 1526 10 22 64 927 3 21 82 9
October
9 0 17 88 810 0 19 96 1011 0 26 68 1316 0 20 57 917 0 20 65 918 0 21 61 18
4 Discussions
The advent of LED technology has substantially improvedlight trap performances Despite the fact that previous sur-veys have demonstrated how light trap using LED tech-nologies can be valid alternative to classical models theattractiveness of different colours LED has not been exploredin deep so far The present study investigated the captureperformances of light trap equipped with LED of differentcolour and wavelength on sand fly species endemic in the
Mediterranean area According to the herein results itmay bespeculated that light trap equipped with UV LED of 395 nmhas a higher attractiveness compared to other coloured LEDtrapsThis is particularly evident for the species P perniciosuswhich is one of the main vectors of leishmaniosis by Linfantum to both humans and dogs [14]
The species captured in the present survey are the samereported in other previous investigations performed in thesame area [11 12 15] where P perniciosus and S minuta werethe most abundant species Though the well-known role of
4 BioMed Research International
Table2Num
bera
ndpercentageso
fphlebotom
ines
andfly
speciesc
apturedby
each
trap
mod
elin
thes
tudy
Traps
Species
Stud
yperiod
May
ntotal()
June
ntotal()
July
ntotal()
Augu
stntotal()
Septem
ber
ntotal()
blue
LED
Phleb
otom
usperniciosus
15(20)
2030(667)
311(273
)918
(50)
46(667)
Sergentomyiaminuta
45(80)
1030(333)
811(727)
918
(50)
26(333)
Phleb
otom
usnegle
ctus
05(0)
030
(0)
011(0)
018
(0)
06(0)
UVLE
DPh
lebotom
usperniciosus
1011
(909)
104116
(897
)89(971)
1418
(778
)610
(60)
Sergentomyiaminuta
111(91
)1211
6(103)
19(29)
418
(222)
410
(40)
Phleb
otom
usnegle
ctus
011(0)
0116
(0)
09(0)
018
(0)
010
(0)
whiteLE
DPh
lebotom
usperniciosus
22(100)
915
(60)
04(0)
912
(75)
11(100)
Sergentomyiaminuta
02(0)
515
(333)
44(100)
312
(25)
01(0)
Phleb
otom
usnegle
ctus
02(0)
115(67)
04(0)
012
(0)
01(0)
greenLE
DPh
lebotom
usperniciosus
13(333)
24(50)
310
(30)
05(0)
45(80)
Sergentomyiaminuta
23(667)
24(50)
710
(70)
55(100)
05(0)
Phleb
otom
usnegle
ctus
03(0)
04(0)
010
(0)
05(0)
15(20)
redLE
DPh
lebotom
usperniciosus
12(50)
1014
(714
)06(0)
05(0)
25(40)
Sergentomyiaminuta
12(50)
414
(286)
66(100)
55(100)
25(40)
Phleb
otom
usnegle
ctus
02(0)
014
(0)
06(0)
05(0)
15(20)
CLT
Phleb
otom
usperniciosus
55(100)
3334(971)
59(556)
1518
(833)
1718
(971)
Sergentomyiaminuta
05(0)
134(29)
49(444)
318
(167)
118(29)
Phleb
otom
usnegle
ctus
05(0)
034
(0)
09(0)
018
(0)
018
(0)
Legend
blueL
EDU
VLE
Dw
hiteLE
Dgreen
LEDred
LED=Laikatraps
equipp
edwith
blueU
Vwhitegreen
andredLE
Dsrespectively
CLT
=Classic
allight
trap
equipp
edwith
incand
escent
lamp
BioMed Research International 5
Figure 2 Total number of phlebotomine sand flies captured byclassical light trap (CLT) and five Laika traps equipped with redgreen white UV and blue LEDs
Figure 3 Total number of Phlebotomus perniciosus captured byclassical light trap (CLT) and blue and UV Laika traps
P perniciosus is being competent vector of L infantum thatof S minuta is still unclear and needs further investigationsRecently [16] reported the first molecular detection of Linfantum in S minuta in southern Portugal and the firstisolation of human blood as meal source in an engorgedfemale of S minuta These findings opened a debate on thepotential role of this species in the transmission of leish-maniosis and its involvement in the epidemiology deservesfurther researches including but not limited to protozoanisolation from engorged specimens as well as experimentaltransmission
The limited presence of P neglectus here observed isconsistent with previous reports in southern Italy [11 17]and justified by the higher abundance of this species innorthern Italian regions which are featured by cooler climate[18 19]
The attractiveness of different light technologies andcolours could bias the estimation of sand fly populationin a specific area In fact as demonstrated by a studythat compared the attractiveness of different LED coloursPhlebotomus papatasi was attracted four times more by redLED compared to blue and green and twice with respectto incandescent lamp [9] A study performed in Brazil
demonstrated that Hoover Pugedo light traps equipped withgreen or blue LED or incandescent lamps showed the sameattractiveness power for Nyssomyia whitmani and Lutzomyialongipalpis [10] In another study the CDC and Disney trapswere respectively more efficient in the capture of Lutzomyiaovallesi and Lutzomyia olmeca olmeca compared to LED lighttrap [20] In a previous study conducted by our group [8] theattractiveness of a Laika trap equipped with both white andUV LED was compared to CLT no significant differences inthe trapping performance of the two traps were recorded inthat study Here the Laika model equipped with UV LEDshowed the best capture performances in general and to Pperniciosus in particular These findings suggest that the eyesof P perniciosus react maximally to light in the ultravioletregion as already observed for Lutzomyia longipalpis [4]However spectral sensitivities using electroretinograms needto be determined in order to clarify whether the greaterattractiveness of the UV LED for this species is linked to ahigher sensitivity of the eyes to wavelength of the ultravioletregion (395 nm) or to the low brightness emitted by this LEDcolour
In addition to trapping methods sand fly abundance andrichness may be influenced considerably by other variablesincluding animalsrsquo presence and environmental and climatevariables [21] In particular the environmental factors havebeen used to predict and elucidate the distribution of diseasestransmitted by vectors [22] The climatic factors includingtemperature humidity wind and rainfall could influence thedistribution of vectors including sand fly species [22 23]A previous study conducted in the same area recorded twopeaks of sand fly collection on August and September [11]in the present study instead only one peak was observed inthe month of June Moreover phlebotomine sand flies werecaptured earlier in the here survey compared to the aforemen-tioned study in which the first positive trapping session wasobserved in late June In regard to this difference it is inter-esting to notice that the summer season in which the presentstudy was conducted was featured by very hot temperatureespecially in July (286 plusmn 32∘C) and August (288 plusmn 50) andhigh humidity in September (693 plusmn 131) and October (725plusmn 156) caused by intense rains These particular climaticconditions may explain the decline in the number of sandflies during the hottest months and their complete absence inOctober
In conclusion this study showed how light trap equippedwith UV LED of 395 nm has superior performances toother LED traps equipped with blue or green or white orred lamps for the capture of sand flies including importantLeishmania vector species such as P perniciosus By virtueof their performances and technology UV LED trap mayrepresent a highly efficient alternative to CLT for the captureand monitoring of the sand fly species endemic in theMediterranean
Data Availability
Data supporting the findings of this study is included withinthe article
6 BioMed Research International
Figure 4 Number of males and females of Phlebotomus perniciosus captured by classical light trap (CLT) and blue and UV Laika trap alongwith results of Pearsonrsquos chi-square test
Conflicts of Interest
The authors declare that they have no conflicts of interest
Authorsrsquo Contributions
Ettore Napoli and Francesca Arfuso contributed equally tothis paper
Acknowledgments
The authors thank Eng Leonardo Spacone of Laika Lab forproviding the traps and the meteorological station used inthis study
References
[1] B Alexander ldquoSampling method for phlebotomine sandfliesrdquoMedical and Veterinary Entomology vol 14 pp 109ndash122 2000
[2] B N Chaniotis M A Correa R B Tesh and K M John-son ldquoDaily and seasonal man-biting activity of phlebotomine
sandflies in Panamardquo Journal of Medical Entomology vol 8 no4 pp 415ndash420 1971
[3] K Arikawa ldquoThe eyes and vision of butterfliesrdquo The Journal ofPhysiology vol 595 no 16 pp 5457ndash5464 2017
[4] H E Mellor J G C Hamilton and M Anderson ldquoSpectralsensitivity in the eyes of male and female Lutzomyia longipalpissandfliesrdquoMedical and Veterinary Entomology vol 10 no 4 pp371ndash374 1996
[5] L W Cohnstaedt J I Gillen and L E Munstermann ldquoLight-emitting diode technology improves insect trappingrdquo Journal ofthe American Mosquito Control Association vol 24 no 2 pp331ndash334 2008
[6] R S Mann P E Kaufman and J F Butler ldquoLutzomyia spp(Diptera Psychodidae) response to olfactory attractant- andlight emitting diode-modified mosquito magnet X (MM-X)trapsrdquo Journal of Medical Entomology vol 46 no 5 pp 1052ndash1061 2009
[7] G C Muller J A Hogsette D L Kline J C Beier E E Revayand R-D Xue ldquoResponse of the sand fly Phlebotomus papatasito visual physical and chemical attraction features in the fieldrdquoActa Tropica vol 141 pp 32ndash36 2015
BioMed Research International 7
[8] G Gaglio E Napoli L Falsone S Giannetto and E BriantildquoField evaluation of a new light trap for phlebotomine sandfliesrdquo Acta Tropica vol 174 pp 114ndash117 2017
[9] D F Hoel J F Butler E Y Fawaz N Watany S S El-Hossaryand J Villinski ldquoResponse of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egyptrdquo Journalof Vector Ecology vol 32 no 2 pp 302ndash307 2007
[10] F S Silva J M Brito B M Costa-Neta and S E P D LoboldquoEvaluation of light-emitting diodes as attractant for sandflies(Diptera Psychodidae Phlebotominae) in northeastern BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 110 no 6 pp 801ndash8032015
[11] G Gaglio E Brianti E Napoli et al ldquoEffect of night time-intervals height of traps and lunar phases on sand fly collectionin a highly endemic area for canine leishmaniasisrdquoActa Tropicavol 133 no 1 pp 73ndash77 2014
[12] E Brianti G Gaglio E Napoli et al ldquoEfficacy of a slow-releaseimidacloprid (10)flumethrin (45) collar for the preventionof canine leishmaniosisrdquo Parasites amp Vectors vol 7 no 1 article327 2014
[13] F Dantas-Torres V D Tarallo and D Otranto ldquoMorphologicalkeys for the identification of Italian phlebotomine sand flies(Diptera Psychodidae Phlebotominae)rdquo Parasites amp Vectorsvol 7 no 1 article 479 2014
[14] M Maroli M D Feliciangeli L Bichaud R N Charrel andL Gradoni ldquoPhlebotomine sand flies and the spreading ofleishmaniases and other diseases of public health concernrdquoMedical and Veterinary Entomology vol 27 no 2 pp 123ndash1472013
[15] O Lisi V DrsquoUrso V Vaccalluzzo et al ldquoPersistence of phle-botomine Leishmania vectors in urban sites of Catania (SicilyItaly)rdquo Parasites amp Vectors vol 7 no 1 article 560 2014
[16] S Pereira D Pita-Pereira T Araujo-Pereira et al ldquoFirstmolecular detection of Leishmania infantum in Sergentomyiaminuta (Diptera Psychodidae) in Alentejo southern PortugalrdquoActa Tropica vol 174 pp 45ndash48 2017
[17] F Dantas-Torres V D Tarallo M S Latrofa A Falchi R PLia and D Otranto ldquoEcology of phlebotomine sand flies andLeishmania infantum infection in a rural area of southern ItalyrdquoActa Tropica vol 137 pp 67ndash73 2014
[18] M Signorini M Drigo F Marcer et al ldquoComparative fieldstudy to evaluate the performance of three different traps forcollecting sand flies in northeastern Italyrdquo Journal of VectorEcology vol 38 no 2 pp 374ndash378 2013
[19] M Maroli L Rossi R Baldelli et al ldquoThe northward spread ofleishmaniasis in Italy evidence from retrospective and ongoingstudies on the canine reservoir and phlebotomine vectorsrdquoTropical Medicine amp International Health vol 13 no 2 pp 256ndash264 2008
[20] J J Rodrıguez-Rojas W Arque-Chunga I Fernandez-Salasand E A Rebollar-Tellez ldquoComparative field evaluation ofdifferent traps for collecting adult phlebotomine sand flies(Diptera Psychodidae) in an endemic area of cutaneous leish-maniasis in Quintana Roo Mexicordquo Journal of the AmericanMosquito Control Association vol 32 no 2 pp 103ndash116 2016
[21] J Ghrab A Rhim D Bach-Hamba et al ldquoPhlebotomi-nae (Diptera Psychodidae) of human leishmaniosis sites inTunisiardquo Parasite vol 13 no 1 pp 23ndash33 2006
[22] A Y M Abdullah A Dewan M R I Shogib M M Rahmanand M F Hossain ldquoEnvironmental factors associated withthe distribution of visceral leishmaniasis in endemic areas of
Bangladesh modeling the ecological nicherdquo Tropical Medicineand Health vol 45 no 1 article 13 2017
[23] L Chamaille A Tran A Meunier G Bourdoiseau P Readyand J-P Dedet ldquoEnvironmental risk mapping of canine leish-maniasis in Francerdquo Parasites amp Vectors vol 3 no 1 article 312010
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
Hindawiwwwhindawicom Volume 2018
Anatomy Research International
PeptidesInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Neuroscience Journal
Hindawiwwwhindawicom Volume 2018
BioMed Research International
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Genetics Research International
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y Stem Cells International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Enzyme Research
Hindawiwwwhindawicom Volume 2018
International Journal of
MicrobiologyHindawiwwwhindawicom
Nucleic AcidsJournal of
Volume 2018
Submit your manuscripts atwwwhindawicom
4 BioMed Research International
Table2Num
bera
ndpercentageso
fphlebotom
ines
andfly
speciesc
apturedby
each
trap
mod
elin
thes
tudy
Traps
Species
Stud
yperiod
May
ntotal()
June
ntotal()
July
ntotal()
Augu
stntotal()
Septem
ber
ntotal()
blue
LED
Phleb
otom
usperniciosus
15(20)
2030(667)
311(273
)918
(50)
46(667)
Sergentomyiaminuta
45(80)
1030(333)
811(727)
918
(50)
26(333)
Phleb
otom
usnegle
ctus
05(0)
030
(0)
011(0)
018
(0)
06(0)
UVLE
DPh
lebotom
usperniciosus
1011
(909)
104116
(897
)89(971)
1418
(778
)610
(60)
Sergentomyiaminuta
111(91
)1211
6(103)
19(29)
418
(222)
410
(40)
Phleb
otom
usnegle
ctus
011(0)
0116
(0)
09(0)
018
(0)
010
(0)
whiteLE
DPh
lebotom
usperniciosus
22(100)
915
(60)
04(0)
912
(75)
11(100)
Sergentomyiaminuta
02(0)
515
(333)
44(100)
312
(25)
01(0)
Phleb
otom
usnegle
ctus
02(0)
115(67)
04(0)
012
(0)
01(0)
greenLE
DPh
lebotom
usperniciosus
13(333)
24(50)
310
(30)
05(0)
45(80)
Sergentomyiaminuta
23(667)
24(50)
710
(70)
55(100)
05(0)
Phleb
otom
usnegle
ctus
03(0)
04(0)
010
(0)
05(0)
15(20)
redLE
DPh
lebotom
usperniciosus
12(50)
1014
(714
)06(0)
05(0)
25(40)
Sergentomyiaminuta
12(50)
414
(286)
66(100)
55(100)
25(40)
Phleb
otom
usnegle
ctus
02(0)
014
(0)
06(0)
05(0)
15(20)
CLT
Phleb
otom
usperniciosus
55(100)
3334(971)
59(556)
1518
(833)
1718
(971)
Sergentomyiaminuta
05(0)
134(29)
49(444)
318
(167)
118(29)
Phleb
otom
usnegle
ctus
05(0)
034
(0)
09(0)
018
(0)
018
(0)
Legend
blueL
EDU
VLE
Dw
hiteLE
Dgreen
LEDred
LED=Laikatraps
equipp
edwith
blueU
Vwhitegreen
andredLE
Dsrespectively
CLT
=Classic
allight
trap
equipp
edwith
incand
escent
lamp
BioMed Research International 5
Figure 2 Total number of phlebotomine sand flies captured byclassical light trap (CLT) and five Laika traps equipped with redgreen white UV and blue LEDs
Figure 3 Total number of Phlebotomus perniciosus captured byclassical light trap (CLT) and blue and UV Laika traps
P perniciosus is being competent vector of L infantum thatof S minuta is still unclear and needs further investigationsRecently [16] reported the first molecular detection of Linfantum in S minuta in southern Portugal and the firstisolation of human blood as meal source in an engorgedfemale of S minuta These findings opened a debate on thepotential role of this species in the transmission of leish-maniosis and its involvement in the epidemiology deservesfurther researches including but not limited to protozoanisolation from engorged specimens as well as experimentaltransmission
The limited presence of P neglectus here observed isconsistent with previous reports in southern Italy [11 17]and justified by the higher abundance of this species innorthern Italian regions which are featured by cooler climate[18 19]
The attractiveness of different light technologies andcolours could bias the estimation of sand fly populationin a specific area In fact as demonstrated by a studythat compared the attractiveness of different LED coloursPhlebotomus papatasi was attracted four times more by redLED compared to blue and green and twice with respectto incandescent lamp [9] A study performed in Brazil
demonstrated that Hoover Pugedo light traps equipped withgreen or blue LED or incandescent lamps showed the sameattractiveness power for Nyssomyia whitmani and Lutzomyialongipalpis [10] In another study the CDC and Disney trapswere respectively more efficient in the capture of Lutzomyiaovallesi and Lutzomyia olmeca olmeca compared to LED lighttrap [20] In a previous study conducted by our group [8] theattractiveness of a Laika trap equipped with both white andUV LED was compared to CLT no significant differences inthe trapping performance of the two traps were recorded inthat study Here the Laika model equipped with UV LEDshowed the best capture performances in general and to Pperniciosus in particular These findings suggest that the eyesof P perniciosus react maximally to light in the ultravioletregion as already observed for Lutzomyia longipalpis [4]However spectral sensitivities using electroretinograms needto be determined in order to clarify whether the greaterattractiveness of the UV LED for this species is linked to ahigher sensitivity of the eyes to wavelength of the ultravioletregion (395 nm) or to the low brightness emitted by this LEDcolour
In addition to trapping methods sand fly abundance andrichness may be influenced considerably by other variablesincluding animalsrsquo presence and environmental and climatevariables [21] In particular the environmental factors havebeen used to predict and elucidate the distribution of diseasestransmitted by vectors [22] The climatic factors includingtemperature humidity wind and rainfall could influence thedistribution of vectors including sand fly species [22 23]A previous study conducted in the same area recorded twopeaks of sand fly collection on August and September [11]in the present study instead only one peak was observed inthe month of June Moreover phlebotomine sand flies werecaptured earlier in the here survey compared to the aforemen-tioned study in which the first positive trapping session wasobserved in late June In regard to this difference it is inter-esting to notice that the summer season in which the presentstudy was conducted was featured by very hot temperatureespecially in July (286 plusmn 32∘C) and August (288 plusmn 50) andhigh humidity in September (693 plusmn 131) and October (725plusmn 156) caused by intense rains These particular climaticconditions may explain the decline in the number of sandflies during the hottest months and their complete absence inOctober
In conclusion this study showed how light trap equippedwith UV LED of 395 nm has superior performances toother LED traps equipped with blue or green or white orred lamps for the capture of sand flies including importantLeishmania vector species such as P perniciosus By virtueof their performances and technology UV LED trap mayrepresent a highly efficient alternative to CLT for the captureand monitoring of the sand fly species endemic in theMediterranean
Data Availability
Data supporting the findings of this study is included withinthe article
6 BioMed Research International
Figure 4 Number of males and females of Phlebotomus perniciosus captured by classical light trap (CLT) and blue and UV Laika trap alongwith results of Pearsonrsquos chi-square test
Conflicts of Interest
The authors declare that they have no conflicts of interest
Authorsrsquo Contributions
Ettore Napoli and Francesca Arfuso contributed equally tothis paper
Acknowledgments
The authors thank Eng Leonardo Spacone of Laika Lab forproviding the traps and the meteorological station used inthis study
References
[1] B Alexander ldquoSampling method for phlebotomine sandfliesrdquoMedical and Veterinary Entomology vol 14 pp 109ndash122 2000
[2] B N Chaniotis M A Correa R B Tesh and K M John-son ldquoDaily and seasonal man-biting activity of phlebotomine
sandflies in Panamardquo Journal of Medical Entomology vol 8 no4 pp 415ndash420 1971
[3] K Arikawa ldquoThe eyes and vision of butterfliesrdquo The Journal ofPhysiology vol 595 no 16 pp 5457ndash5464 2017
[4] H E Mellor J G C Hamilton and M Anderson ldquoSpectralsensitivity in the eyes of male and female Lutzomyia longipalpissandfliesrdquoMedical and Veterinary Entomology vol 10 no 4 pp371ndash374 1996
[5] L W Cohnstaedt J I Gillen and L E Munstermann ldquoLight-emitting diode technology improves insect trappingrdquo Journal ofthe American Mosquito Control Association vol 24 no 2 pp331ndash334 2008
[6] R S Mann P E Kaufman and J F Butler ldquoLutzomyia spp(Diptera Psychodidae) response to olfactory attractant- andlight emitting diode-modified mosquito magnet X (MM-X)trapsrdquo Journal of Medical Entomology vol 46 no 5 pp 1052ndash1061 2009
[7] G C Muller J A Hogsette D L Kline J C Beier E E Revayand R-D Xue ldquoResponse of the sand fly Phlebotomus papatasito visual physical and chemical attraction features in the fieldrdquoActa Tropica vol 141 pp 32ndash36 2015
BioMed Research International 7
[8] G Gaglio E Napoli L Falsone S Giannetto and E BriantildquoField evaluation of a new light trap for phlebotomine sandfliesrdquo Acta Tropica vol 174 pp 114ndash117 2017
[9] D F Hoel J F Butler E Y Fawaz N Watany S S El-Hossaryand J Villinski ldquoResponse of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egyptrdquo Journalof Vector Ecology vol 32 no 2 pp 302ndash307 2007
[10] F S Silva J M Brito B M Costa-Neta and S E P D LoboldquoEvaluation of light-emitting diodes as attractant for sandflies(Diptera Psychodidae Phlebotominae) in northeastern BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 110 no 6 pp 801ndash8032015
[11] G Gaglio E Brianti E Napoli et al ldquoEffect of night time-intervals height of traps and lunar phases on sand fly collectionin a highly endemic area for canine leishmaniasisrdquoActa Tropicavol 133 no 1 pp 73ndash77 2014
[12] E Brianti G Gaglio E Napoli et al ldquoEfficacy of a slow-releaseimidacloprid (10)flumethrin (45) collar for the preventionof canine leishmaniosisrdquo Parasites amp Vectors vol 7 no 1 article327 2014
[13] F Dantas-Torres V D Tarallo and D Otranto ldquoMorphologicalkeys for the identification of Italian phlebotomine sand flies(Diptera Psychodidae Phlebotominae)rdquo Parasites amp Vectorsvol 7 no 1 article 479 2014
[14] M Maroli M D Feliciangeli L Bichaud R N Charrel andL Gradoni ldquoPhlebotomine sand flies and the spreading ofleishmaniases and other diseases of public health concernrdquoMedical and Veterinary Entomology vol 27 no 2 pp 123ndash1472013
[15] O Lisi V DrsquoUrso V Vaccalluzzo et al ldquoPersistence of phle-botomine Leishmania vectors in urban sites of Catania (SicilyItaly)rdquo Parasites amp Vectors vol 7 no 1 article 560 2014
[16] S Pereira D Pita-Pereira T Araujo-Pereira et al ldquoFirstmolecular detection of Leishmania infantum in Sergentomyiaminuta (Diptera Psychodidae) in Alentejo southern PortugalrdquoActa Tropica vol 174 pp 45ndash48 2017
[17] F Dantas-Torres V D Tarallo M S Latrofa A Falchi R PLia and D Otranto ldquoEcology of phlebotomine sand flies andLeishmania infantum infection in a rural area of southern ItalyrdquoActa Tropica vol 137 pp 67ndash73 2014
[18] M Signorini M Drigo F Marcer et al ldquoComparative fieldstudy to evaluate the performance of three different traps forcollecting sand flies in northeastern Italyrdquo Journal of VectorEcology vol 38 no 2 pp 374ndash378 2013
[19] M Maroli L Rossi R Baldelli et al ldquoThe northward spread ofleishmaniasis in Italy evidence from retrospective and ongoingstudies on the canine reservoir and phlebotomine vectorsrdquoTropical Medicine amp International Health vol 13 no 2 pp 256ndash264 2008
[20] J J Rodrıguez-Rojas W Arque-Chunga I Fernandez-Salasand E A Rebollar-Tellez ldquoComparative field evaluation ofdifferent traps for collecting adult phlebotomine sand flies(Diptera Psychodidae) in an endemic area of cutaneous leish-maniasis in Quintana Roo Mexicordquo Journal of the AmericanMosquito Control Association vol 32 no 2 pp 103ndash116 2016
[21] J Ghrab A Rhim D Bach-Hamba et al ldquoPhlebotomi-nae (Diptera Psychodidae) of human leishmaniosis sites inTunisiardquo Parasite vol 13 no 1 pp 23ndash33 2006
[22] A Y M Abdullah A Dewan M R I Shogib M M Rahmanand M F Hossain ldquoEnvironmental factors associated withthe distribution of visceral leishmaniasis in endemic areas of
Bangladesh modeling the ecological nicherdquo Tropical Medicineand Health vol 45 no 1 article 13 2017
[23] L Chamaille A Tran A Meunier G Bourdoiseau P Readyand J-P Dedet ldquoEnvironmental risk mapping of canine leish-maniasis in Francerdquo Parasites amp Vectors vol 3 no 1 article 312010
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
Hindawiwwwhindawicom Volume 2018
Anatomy Research International
PeptidesInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Neuroscience Journal
Hindawiwwwhindawicom Volume 2018
BioMed Research International
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Genetics Research International
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y Stem Cells International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Enzyme Research
Hindawiwwwhindawicom Volume 2018
International Journal of
MicrobiologyHindawiwwwhindawicom
Nucleic AcidsJournal of
Volume 2018
Submit your manuscripts atwwwhindawicom
BioMed Research International 5
Figure 2 Total number of phlebotomine sand flies captured byclassical light trap (CLT) and five Laika traps equipped with redgreen white UV and blue LEDs
Figure 3 Total number of Phlebotomus perniciosus captured byclassical light trap (CLT) and blue and UV Laika traps
P perniciosus is being competent vector of L infantum thatof S minuta is still unclear and needs further investigationsRecently [16] reported the first molecular detection of Linfantum in S minuta in southern Portugal and the firstisolation of human blood as meal source in an engorgedfemale of S minuta These findings opened a debate on thepotential role of this species in the transmission of leish-maniosis and its involvement in the epidemiology deservesfurther researches including but not limited to protozoanisolation from engorged specimens as well as experimentaltransmission
The limited presence of P neglectus here observed isconsistent with previous reports in southern Italy [11 17]and justified by the higher abundance of this species innorthern Italian regions which are featured by cooler climate[18 19]
The attractiveness of different light technologies andcolours could bias the estimation of sand fly populationin a specific area In fact as demonstrated by a studythat compared the attractiveness of different LED coloursPhlebotomus papatasi was attracted four times more by redLED compared to blue and green and twice with respectto incandescent lamp [9] A study performed in Brazil
demonstrated that Hoover Pugedo light traps equipped withgreen or blue LED or incandescent lamps showed the sameattractiveness power for Nyssomyia whitmani and Lutzomyialongipalpis [10] In another study the CDC and Disney trapswere respectively more efficient in the capture of Lutzomyiaovallesi and Lutzomyia olmeca olmeca compared to LED lighttrap [20] In a previous study conducted by our group [8] theattractiveness of a Laika trap equipped with both white andUV LED was compared to CLT no significant differences inthe trapping performance of the two traps were recorded inthat study Here the Laika model equipped with UV LEDshowed the best capture performances in general and to Pperniciosus in particular These findings suggest that the eyesof P perniciosus react maximally to light in the ultravioletregion as already observed for Lutzomyia longipalpis [4]However spectral sensitivities using electroretinograms needto be determined in order to clarify whether the greaterattractiveness of the UV LED for this species is linked to ahigher sensitivity of the eyes to wavelength of the ultravioletregion (395 nm) or to the low brightness emitted by this LEDcolour
In addition to trapping methods sand fly abundance andrichness may be influenced considerably by other variablesincluding animalsrsquo presence and environmental and climatevariables [21] In particular the environmental factors havebeen used to predict and elucidate the distribution of diseasestransmitted by vectors [22] The climatic factors includingtemperature humidity wind and rainfall could influence thedistribution of vectors including sand fly species [22 23]A previous study conducted in the same area recorded twopeaks of sand fly collection on August and September [11]in the present study instead only one peak was observed inthe month of June Moreover phlebotomine sand flies werecaptured earlier in the here survey compared to the aforemen-tioned study in which the first positive trapping session wasobserved in late June In regard to this difference it is inter-esting to notice that the summer season in which the presentstudy was conducted was featured by very hot temperatureespecially in July (286 plusmn 32∘C) and August (288 plusmn 50) andhigh humidity in September (693 plusmn 131) and October (725plusmn 156) caused by intense rains These particular climaticconditions may explain the decline in the number of sandflies during the hottest months and their complete absence inOctober
In conclusion this study showed how light trap equippedwith UV LED of 395 nm has superior performances toother LED traps equipped with blue or green or white orred lamps for the capture of sand flies including importantLeishmania vector species such as P perniciosus By virtueof their performances and technology UV LED trap mayrepresent a highly efficient alternative to CLT for the captureand monitoring of the sand fly species endemic in theMediterranean
Data Availability
Data supporting the findings of this study is included withinthe article
6 BioMed Research International
Figure 4 Number of males and females of Phlebotomus perniciosus captured by classical light trap (CLT) and blue and UV Laika trap alongwith results of Pearsonrsquos chi-square test
Conflicts of Interest
The authors declare that they have no conflicts of interest
Authorsrsquo Contributions
Ettore Napoli and Francesca Arfuso contributed equally tothis paper
Acknowledgments
The authors thank Eng Leonardo Spacone of Laika Lab forproviding the traps and the meteorological station used inthis study
References
[1] B Alexander ldquoSampling method for phlebotomine sandfliesrdquoMedical and Veterinary Entomology vol 14 pp 109ndash122 2000
[2] B N Chaniotis M A Correa R B Tesh and K M John-son ldquoDaily and seasonal man-biting activity of phlebotomine
sandflies in Panamardquo Journal of Medical Entomology vol 8 no4 pp 415ndash420 1971
[3] K Arikawa ldquoThe eyes and vision of butterfliesrdquo The Journal ofPhysiology vol 595 no 16 pp 5457ndash5464 2017
[4] H E Mellor J G C Hamilton and M Anderson ldquoSpectralsensitivity in the eyes of male and female Lutzomyia longipalpissandfliesrdquoMedical and Veterinary Entomology vol 10 no 4 pp371ndash374 1996
[5] L W Cohnstaedt J I Gillen and L E Munstermann ldquoLight-emitting diode technology improves insect trappingrdquo Journal ofthe American Mosquito Control Association vol 24 no 2 pp331ndash334 2008
[6] R S Mann P E Kaufman and J F Butler ldquoLutzomyia spp(Diptera Psychodidae) response to olfactory attractant- andlight emitting diode-modified mosquito magnet X (MM-X)trapsrdquo Journal of Medical Entomology vol 46 no 5 pp 1052ndash1061 2009
[7] G C Muller J A Hogsette D L Kline J C Beier E E Revayand R-D Xue ldquoResponse of the sand fly Phlebotomus papatasito visual physical and chemical attraction features in the fieldrdquoActa Tropica vol 141 pp 32ndash36 2015
BioMed Research International 7
[8] G Gaglio E Napoli L Falsone S Giannetto and E BriantildquoField evaluation of a new light trap for phlebotomine sandfliesrdquo Acta Tropica vol 174 pp 114ndash117 2017
[9] D F Hoel J F Butler E Y Fawaz N Watany S S El-Hossaryand J Villinski ldquoResponse of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egyptrdquo Journalof Vector Ecology vol 32 no 2 pp 302ndash307 2007
[10] F S Silva J M Brito B M Costa-Neta and S E P D LoboldquoEvaluation of light-emitting diodes as attractant for sandflies(Diptera Psychodidae Phlebotominae) in northeastern BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 110 no 6 pp 801ndash8032015
[11] G Gaglio E Brianti E Napoli et al ldquoEffect of night time-intervals height of traps and lunar phases on sand fly collectionin a highly endemic area for canine leishmaniasisrdquoActa Tropicavol 133 no 1 pp 73ndash77 2014
[12] E Brianti G Gaglio E Napoli et al ldquoEfficacy of a slow-releaseimidacloprid (10)flumethrin (45) collar for the preventionof canine leishmaniosisrdquo Parasites amp Vectors vol 7 no 1 article327 2014
[13] F Dantas-Torres V D Tarallo and D Otranto ldquoMorphologicalkeys for the identification of Italian phlebotomine sand flies(Diptera Psychodidae Phlebotominae)rdquo Parasites amp Vectorsvol 7 no 1 article 479 2014
[14] M Maroli M D Feliciangeli L Bichaud R N Charrel andL Gradoni ldquoPhlebotomine sand flies and the spreading ofleishmaniases and other diseases of public health concernrdquoMedical and Veterinary Entomology vol 27 no 2 pp 123ndash1472013
[15] O Lisi V DrsquoUrso V Vaccalluzzo et al ldquoPersistence of phle-botomine Leishmania vectors in urban sites of Catania (SicilyItaly)rdquo Parasites amp Vectors vol 7 no 1 article 560 2014
[16] S Pereira D Pita-Pereira T Araujo-Pereira et al ldquoFirstmolecular detection of Leishmania infantum in Sergentomyiaminuta (Diptera Psychodidae) in Alentejo southern PortugalrdquoActa Tropica vol 174 pp 45ndash48 2017
[17] F Dantas-Torres V D Tarallo M S Latrofa A Falchi R PLia and D Otranto ldquoEcology of phlebotomine sand flies andLeishmania infantum infection in a rural area of southern ItalyrdquoActa Tropica vol 137 pp 67ndash73 2014
[18] M Signorini M Drigo F Marcer et al ldquoComparative fieldstudy to evaluate the performance of three different traps forcollecting sand flies in northeastern Italyrdquo Journal of VectorEcology vol 38 no 2 pp 374ndash378 2013
[19] M Maroli L Rossi R Baldelli et al ldquoThe northward spread ofleishmaniasis in Italy evidence from retrospective and ongoingstudies on the canine reservoir and phlebotomine vectorsrdquoTropical Medicine amp International Health vol 13 no 2 pp 256ndash264 2008
[20] J J Rodrıguez-Rojas W Arque-Chunga I Fernandez-Salasand E A Rebollar-Tellez ldquoComparative field evaluation ofdifferent traps for collecting adult phlebotomine sand flies(Diptera Psychodidae) in an endemic area of cutaneous leish-maniasis in Quintana Roo Mexicordquo Journal of the AmericanMosquito Control Association vol 32 no 2 pp 103ndash116 2016
[21] J Ghrab A Rhim D Bach-Hamba et al ldquoPhlebotomi-nae (Diptera Psychodidae) of human leishmaniosis sites inTunisiardquo Parasite vol 13 no 1 pp 23ndash33 2006
[22] A Y M Abdullah A Dewan M R I Shogib M M Rahmanand M F Hossain ldquoEnvironmental factors associated withthe distribution of visceral leishmaniasis in endemic areas of
Bangladesh modeling the ecological nicherdquo Tropical Medicineand Health vol 45 no 1 article 13 2017
[23] L Chamaille A Tran A Meunier G Bourdoiseau P Readyand J-P Dedet ldquoEnvironmental risk mapping of canine leish-maniasis in Francerdquo Parasites amp Vectors vol 3 no 1 article 312010
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
Hindawiwwwhindawicom Volume 2018
Anatomy Research International
PeptidesInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Neuroscience Journal
Hindawiwwwhindawicom Volume 2018
BioMed Research International
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Genetics Research International
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y Stem Cells International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Enzyme Research
Hindawiwwwhindawicom Volume 2018
International Journal of
MicrobiologyHindawiwwwhindawicom
Nucleic AcidsJournal of
Volume 2018
Submit your manuscripts atwwwhindawicom
6 BioMed Research International
Figure 4 Number of males and females of Phlebotomus perniciosus captured by classical light trap (CLT) and blue and UV Laika trap alongwith results of Pearsonrsquos chi-square test
Conflicts of Interest
The authors declare that they have no conflicts of interest
Authorsrsquo Contributions
Ettore Napoli and Francesca Arfuso contributed equally tothis paper
Acknowledgments
The authors thank Eng Leonardo Spacone of Laika Lab forproviding the traps and the meteorological station used inthis study
References
[1] B Alexander ldquoSampling method for phlebotomine sandfliesrdquoMedical and Veterinary Entomology vol 14 pp 109ndash122 2000
[2] B N Chaniotis M A Correa R B Tesh and K M John-son ldquoDaily and seasonal man-biting activity of phlebotomine
sandflies in Panamardquo Journal of Medical Entomology vol 8 no4 pp 415ndash420 1971
[3] K Arikawa ldquoThe eyes and vision of butterfliesrdquo The Journal ofPhysiology vol 595 no 16 pp 5457ndash5464 2017
[4] H E Mellor J G C Hamilton and M Anderson ldquoSpectralsensitivity in the eyes of male and female Lutzomyia longipalpissandfliesrdquoMedical and Veterinary Entomology vol 10 no 4 pp371ndash374 1996
[5] L W Cohnstaedt J I Gillen and L E Munstermann ldquoLight-emitting diode technology improves insect trappingrdquo Journal ofthe American Mosquito Control Association vol 24 no 2 pp331ndash334 2008
[6] R S Mann P E Kaufman and J F Butler ldquoLutzomyia spp(Diptera Psychodidae) response to olfactory attractant- andlight emitting diode-modified mosquito magnet X (MM-X)trapsrdquo Journal of Medical Entomology vol 46 no 5 pp 1052ndash1061 2009
[7] G C Muller J A Hogsette D L Kline J C Beier E E Revayand R-D Xue ldquoResponse of the sand fly Phlebotomus papatasito visual physical and chemical attraction features in the fieldrdquoActa Tropica vol 141 pp 32ndash36 2015
BioMed Research International 7
[8] G Gaglio E Napoli L Falsone S Giannetto and E BriantildquoField evaluation of a new light trap for phlebotomine sandfliesrdquo Acta Tropica vol 174 pp 114ndash117 2017
[9] D F Hoel J F Butler E Y Fawaz N Watany S S El-Hossaryand J Villinski ldquoResponse of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egyptrdquo Journalof Vector Ecology vol 32 no 2 pp 302ndash307 2007
[10] F S Silva J M Brito B M Costa-Neta and S E P D LoboldquoEvaluation of light-emitting diodes as attractant for sandflies(Diptera Psychodidae Phlebotominae) in northeastern BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 110 no 6 pp 801ndash8032015
[11] G Gaglio E Brianti E Napoli et al ldquoEffect of night time-intervals height of traps and lunar phases on sand fly collectionin a highly endemic area for canine leishmaniasisrdquoActa Tropicavol 133 no 1 pp 73ndash77 2014
[12] E Brianti G Gaglio E Napoli et al ldquoEfficacy of a slow-releaseimidacloprid (10)flumethrin (45) collar for the preventionof canine leishmaniosisrdquo Parasites amp Vectors vol 7 no 1 article327 2014
[13] F Dantas-Torres V D Tarallo and D Otranto ldquoMorphologicalkeys for the identification of Italian phlebotomine sand flies(Diptera Psychodidae Phlebotominae)rdquo Parasites amp Vectorsvol 7 no 1 article 479 2014
[14] M Maroli M D Feliciangeli L Bichaud R N Charrel andL Gradoni ldquoPhlebotomine sand flies and the spreading ofleishmaniases and other diseases of public health concernrdquoMedical and Veterinary Entomology vol 27 no 2 pp 123ndash1472013
[15] O Lisi V DrsquoUrso V Vaccalluzzo et al ldquoPersistence of phle-botomine Leishmania vectors in urban sites of Catania (SicilyItaly)rdquo Parasites amp Vectors vol 7 no 1 article 560 2014
[16] S Pereira D Pita-Pereira T Araujo-Pereira et al ldquoFirstmolecular detection of Leishmania infantum in Sergentomyiaminuta (Diptera Psychodidae) in Alentejo southern PortugalrdquoActa Tropica vol 174 pp 45ndash48 2017
[17] F Dantas-Torres V D Tarallo M S Latrofa A Falchi R PLia and D Otranto ldquoEcology of phlebotomine sand flies andLeishmania infantum infection in a rural area of southern ItalyrdquoActa Tropica vol 137 pp 67ndash73 2014
[18] M Signorini M Drigo F Marcer et al ldquoComparative fieldstudy to evaluate the performance of three different traps forcollecting sand flies in northeastern Italyrdquo Journal of VectorEcology vol 38 no 2 pp 374ndash378 2013
[19] M Maroli L Rossi R Baldelli et al ldquoThe northward spread ofleishmaniasis in Italy evidence from retrospective and ongoingstudies on the canine reservoir and phlebotomine vectorsrdquoTropical Medicine amp International Health vol 13 no 2 pp 256ndash264 2008
[20] J J Rodrıguez-Rojas W Arque-Chunga I Fernandez-Salasand E A Rebollar-Tellez ldquoComparative field evaluation ofdifferent traps for collecting adult phlebotomine sand flies(Diptera Psychodidae) in an endemic area of cutaneous leish-maniasis in Quintana Roo Mexicordquo Journal of the AmericanMosquito Control Association vol 32 no 2 pp 103ndash116 2016
[21] J Ghrab A Rhim D Bach-Hamba et al ldquoPhlebotomi-nae (Diptera Psychodidae) of human leishmaniosis sites inTunisiardquo Parasite vol 13 no 1 pp 23ndash33 2006
[22] A Y M Abdullah A Dewan M R I Shogib M M Rahmanand M F Hossain ldquoEnvironmental factors associated withthe distribution of visceral leishmaniasis in endemic areas of
Bangladesh modeling the ecological nicherdquo Tropical Medicineand Health vol 45 no 1 article 13 2017
[23] L Chamaille A Tran A Meunier G Bourdoiseau P Readyand J-P Dedet ldquoEnvironmental risk mapping of canine leish-maniasis in Francerdquo Parasites amp Vectors vol 3 no 1 article 312010
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
Hindawiwwwhindawicom Volume 2018
Anatomy Research International
PeptidesInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Neuroscience Journal
Hindawiwwwhindawicom Volume 2018
BioMed Research International
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Genetics Research International
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y Stem Cells International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Enzyme Research
Hindawiwwwhindawicom Volume 2018
International Journal of
MicrobiologyHindawiwwwhindawicom
Nucleic AcidsJournal of
Volume 2018
Submit your manuscripts atwwwhindawicom
BioMed Research International 7
[8] G Gaglio E Napoli L Falsone S Giannetto and E BriantildquoField evaluation of a new light trap for phlebotomine sandfliesrdquo Acta Tropica vol 174 pp 114ndash117 2017
[9] D F Hoel J F Butler E Y Fawaz N Watany S S El-Hossaryand J Villinski ldquoResponse of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egyptrdquo Journalof Vector Ecology vol 32 no 2 pp 302ndash307 2007
[10] F S Silva J M Brito B M Costa-Neta and S E P D LoboldquoEvaluation of light-emitting diodes as attractant for sandflies(Diptera Psychodidae Phlebotominae) in northeastern BrazilrdquoMemorias do Instituto Oswaldo Cruz vol 110 no 6 pp 801ndash8032015
[11] G Gaglio E Brianti E Napoli et al ldquoEffect of night time-intervals height of traps and lunar phases on sand fly collectionin a highly endemic area for canine leishmaniasisrdquoActa Tropicavol 133 no 1 pp 73ndash77 2014
[12] E Brianti G Gaglio E Napoli et al ldquoEfficacy of a slow-releaseimidacloprid (10)flumethrin (45) collar for the preventionof canine leishmaniosisrdquo Parasites amp Vectors vol 7 no 1 article327 2014
[13] F Dantas-Torres V D Tarallo and D Otranto ldquoMorphologicalkeys for the identification of Italian phlebotomine sand flies(Diptera Psychodidae Phlebotominae)rdquo Parasites amp Vectorsvol 7 no 1 article 479 2014
[14] M Maroli M D Feliciangeli L Bichaud R N Charrel andL Gradoni ldquoPhlebotomine sand flies and the spreading ofleishmaniases and other diseases of public health concernrdquoMedical and Veterinary Entomology vol 27 no 2 pp 123ndash1472013
[15] O Lisi V DrsquoUrso V Vaccalluzzo et al ldquoPersistence of phle-botomine Leishmania vectors in urban sites of Catania (SicilyItaly)rdquo Parasites amp Vectors vol 7 no 1 article 560 2014
[16] S Pereira D Pita-Pereira T Araujo-Pereira et al ldquoFirstmolecular detection of Leishmania infantum in Sergentomyiaminuta (Diptera Psychodidae) in Alentejo southern PortugalrdquoActa Tropica vol 174 pp 45ndash48 2017
[17] F Dantas-Torres V D Tarallo M S Latrofa A Falchi R PLia and D Otranto ldquoEcology of phlebotomine sand flies andLeishmania infantum infection in a rural area of southern ItalyrdquoActa Tropica vol 137 pp 67ndash73 2014
[18] M Signorini M Drigo F Marcer et al ldquoComparative fieldstudy to evaluate the performance of three different traps forcollecting sand flies in northeastern Italyrdquo Journal of VectorEcology vol 38 no 2 pp 374ndash378 2013
[19] M Maroli L Rossi R Baldelli et al ldquoThe northward spread ofleishmaniasis in Italy evidence from retrospective and ongoingstudies on the canine reservoir and phlebotomine vectorsrdquoTropical Medicine amp International Health vol 13 no 2 pp 256ndash264 2008
[20] J J Rodrıguez-Rojas W Arque-Chunga I Fernandez-Salasand E A Rebollar-Tellez ldquoComparative field evaluation ofdifferent traps for collecting adult phlebotomine sand flies(Diptera Psychodidae) in an endemic area of cutaneous leish-maniasis in Quintana Roo Mexicordquo Journal of the AmericanMosquito Control Association vol 32 no 2 pp 103ndash116 2016
[21] J Ghrab A Rhim D Bach-Hamba et al ldquoPhlebotomi-nae (Diptera Psychodidae) of human leishmaniosis sites inTunisiardquo Parasite vol 13 no 1 pp 23ndash33 2006
[22] A Y M Abdullah A Dewan M R I Shogib M M Rahmanand M F Hossain ldquoEnvironmental factors associated withthe distribution of visceral leishmaniasis in endemic areas of
Bangladesh modeling the ecological nicherdquo Tropical Medicineand Health vol 45 no 1 article 13 2017
[23] L Chamaille A Tran A Meunier G Bourdoiseau P Readyand J-P Dedet ldquoEnvironmental risk mapping of canine leish-maniasis in Francerdquo Parasites amp Vectors vol 3 no 1 article 312010
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
Hindawiwwwhindawicom Volume 2018
Anatomy Research International
PeptidesInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Neuroscience Journal
Hindawiwwwhindawicom Volume 2018
BioMed Research International
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Genetics Research International
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y Stem Cells International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Enzyme Research
Hindawiwwwhindawicom Volume 2018
International Journal of
MicrobiologyHindawiwwwhindawicom
Nucleic AcidsJournal of
Volume 2018
Submit your manuscripts atwwwhindawicom
Hindawiwwwhindawicom
International Journal of
Volume 2018
Zoology
Hindawiwwwhindawicom Volume 2018
Anatomy Research International
PeptidesInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Journal of Parasitology Research
GenomicsInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom
The Scientific World Journal
Volume 2018
Hindawiwwwhindawicom Volume 2018
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Neuroscience Journal
Hindawiwwwhindawicom Volume 2018
BioMed Research International
Cell BiologyInternational Journal of
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Biochemistry Research International
ArchaeaHindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Genetics Research International
Hindawiwwwhindawicom Volume 2018
Advances in
Virolog y Stem Cells International
Hindawiwwwhindawicom Volume 2018
Hindawiwwwhindawicom Volume 2018
Enzyme Research
Hindawiwwwhindawicom Volume 2018
International Journal of
MicrobiologyHindawiwwwhindawicom
Nucleic AcidsJournal of
Volume 2018
Submit your manuscripts atwwwhindawicom
