Leishmaniasis in Central Morocco: Seasonal Fluctuations of ...

Research ArticleLeishmaniasis in Central MoroccoSeasonal Fluctuations of Phlebotomine Sand Fly inAichoun Locality from Sefrou Province

Fatima Zahra Talbi12 Abdelhakim El Ouali Lalami3 Abdellatif Janati Idrissi1

Faiza Sebti4 and Chafika Faraj2

1Analysis and Modelisation of Continental Ecosystems Laboratory Faculty of Sciences Dhar El MehrazSidi Mohamed Ben Abdellah University 30000 Fes Morocco2Laboratory of Medical Entomology National Institute of Hygiene 27 Avenue Ibn Battuta Agdal 11400 Rabat Morocco3Regional Diagnostic Laboratory Epidemiological and Environmental Health Regional Health Directorate EL Ghassani Hospital30000 Fes Morocco4National Reference Laboratory of Leishmaniasis National Institute of Hygiene 27 Avenue Ibn Battuta Agdal 11400 Rabat Morocco

Correspondence should be addressed to Abdelhakim El Ouali Lalami eloualilalamiyahoofr

Received 27 August 2014 Accepted 9 January 2015

Academic Editor Shahid Pervez

Copyright copy 2015 Fatima Zahra Talbi et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Cutaneous leishmaniases (CL) are endemic in Morocco They are common in the human population in different localities suchas Aichoun in Sefrou province Morocco This study was carried out in Aichoun locality from April to October 2012 in order tostudy the spatiotemporal trends of the main Leishmania phlebotomine vectors in this focus Overall 1171 sand flies belonging tofour species were collected by sticky traps Phlebotomus sergenti was the predominant species (784) followed by Ph perniciosus(105) Ph papatasi (794) and Ph longicuspis (316) Sandflies were active during 6 months (MayndashOctober) Ph sergenti Phperniciosus and Ph papatasi displayed a bimodal distribution with a first peak in July and a second peak in September while Phlongicuspis showed amonophasic trend with a peak in AugustThe high abundance and the lengthy period of activity of Ph sergentiand Ph perniciosus vectors of L tropica and L infantum respectively are a cause for concern as they indicate the high potentialrisk of Leishmania transmission in the studied areas

1 Introduction

Cutaneous Leishmaniasis (CL) is an increasingly publichealth problem inMoroccoThree forms are present anthro-ponotic leishmaniasis caused by Leishmania tropica andzoonotic leishmaniasis caused by L major and less frequentlyby Leishmania infantum [1] The parasites are transmittedby phlebotomine sand flies namely Phlebotomus sergenti forACL and Ph papatasi and phlebotomines from Larrousiussubgenus for L major and L infantum respectively for ZCL[2] The main reservoir host for L major is considered to bethe rodentMeriones shawi [1]

CL caused byL tropica is themostwidespread in semiaridareas in central and south-western Morocco This disease

was reported for the first time in Azilal province in 1989[3] then in other focus in central and southern areas of thecountry such as Guelmim Agadir Essaouira [4] and Taza[5] CL due to L infantumwas reported in Taounate provincein 1996 within an active focus of visceral leishmaniasis[6] L infantum is also responsible for widespread visceralleishmaniasis in the north-eastern slope of the Rif Mountainswhen dog is the main domestic reservoir of the parasite [7]

Each year we witness the emergence of new foci extend-ing the disease distribution and increasing its total impact In2011 and 2012 the Ministry of Health recorded respectively4426 and 2990 cases with 492 and 719 in the region ofFes-Boulmane [8 9] The region of Fes-Boulmane recordedthe first outbreak ofCL in 2001with 1600 cases in the province

Hindawi Publishing CorporationPathology Research InternationalVolume 2015 Article ID 438749 4 pageshttpdxdoiorg1011552015438749

2 Pathology Research International

Table 1 Sandflies collected in Aichoun locality 2012

Subgenus (R Ab ) Species Mal Female Total R Ab ()

Larroussius (1374) Phlebotomus longicuspis 13 24 37 316Phlebotomus perniciosus 113 10 123 1050

Paraphlebotomus (7828) Phlebotomus sergenti 845 73 918 784Phlebotomus (798) Phlebotomus papatasi 63 30 93 794R Ab Relative Abundance

of Moulay Yacoub alone [10 11] The outbreak was rapidlystopped by insecticides use but the disease has persisted sincethat under endemic and epidemic forms in other provinces ofthe regionwithmore than 100 cases each year despite a strongmonitoring plan

The control of the disease is mainly based on case detec-tion and treatment of human cases and on vector controlThisis based essentially on environmental management includingpromotion of improved solid waste disposal practices Theuse of bed nets and local residual indoor spraying withsynthetic pyrethroids are often applied in newly emergedepidemic foci Nevertheless few data are available on thevector Ph sergenti especially seasonal fluctuations of itsabundance This information is essential for the success ofvector control In this context we have conducted this studyfor the first time in a village belonging to the region of Sefrouprovince in center of Morocco

This study also allows a better understanding of thedynamics of the transmission of leishmaniasis in the area ofAichoun and therefore contributes to the future design ofsurveillance strategies

2 Materials and Methods

21 Study Area and Environment The entomological studywas conducted in the locality of Aichoun (33∘391015840N 04∘381015840W)situated in the northwest of theMoroccanMiddleAtlas a partof the province of Sefrou that belongs to the territory pastoralvillage of Tazouta with a cold semiarid climate The meanaltitude is 750m The average annual rainfall is 400mm themain minimum of the coldest month is 2∘C and maximumof the hottest month is 40∘C

The locality of Aichoun is characterized by the presenceof cowsheds caves and accumulation of animal waste thatcreates an environment favorable to the biological cycle ofsand flies The vegetation is characterized by a covering moreor less degraded because of overgrazing and overexploitationfor domestic uses (Tetraclinis articulata Pistacia lentiscusOlea oleaster Olea europaea and Juniperus phoenicea)

22 Sand Fly Collection and Identification Sand flies werecollected bimonthly during their optimum developmentperiod inMorocco betweenMay andOctober Five collectingsites were chosen in Aichoun locality Collections wereperformed by using sticky papers (21 times 273 cm) coated withcastor oil We used 40 traps in each trapping campaignThe traps were installed in different habitats during the dayand were removed the next day Collected sand flies were

transferred in glass tubes containing a solution of ethanolat 70∘ After sex determination all sand flies collected wereidentified by examining the morphology of the pharyngealarmature and spermathecae of female flies and the externalgenitalia of males using the morphological key [12 13]Morphological differentiation of the two sympatric speciesPh longicuspis and Ph perniciosus was made according todescription of Berchi et al [14]

3 Results

31 Taxonomic Inventory of Sand Flies This study has estab-lished a faunal inventory of Aichoun revealing the presenceof four species belonging to the genus Phlebotomus Thesex ratio indicated that more males were collected themalefemale ratio was 754

The collections accounted for 1171 sand fly specimensPh sergenti was the predominant and the most frequentlycollected species with 918 individuals (784) In secondplace comes Ph perniciosus Newstead with 123 (1050)followed by Ph papatasi Scopoli with 93 individuals (794)Ph longicuspisNitzulescu was represented by 316 (Table 1)

32 Seasonal Fluctuations of Sand Flies Species Seasonalactivity of sandflies extended fromMay to the end ofOctoberwith variation in the monthly evolution according to speciesPh sergenti Ph Perniciosus and Ph papatasi displayed abimodal distribution with a first peak in July where Phsergenti dominates (2946) and a second peak in Septemberwith 1383 while Ph longicuspis showed a monophasictrend with a slight peak in August (111) (Figure 1)

4 Discussion

Over the last years incidence of L tropica CL has contin-uously increased in the province of Sefrou [15] Between1997 and 2011 1242 cases were declared [16] The majority ofcases were reported mainly in El Menzel Sefrou AghbalouTazouta Sidi Lahcen and Ain Chegag communes [17]

Ph sergenti is confirmed as vector ofL tropica in northernAfrica Middle East and Central Asia [18 19] the same inMorocco [4] It dominates in arid and semiarid areas [20]In this study area Ph sergenti was largely widespread it waspresent throughout the whole period of our surveys showinga biphasic course evolution with two peaks in July andSeptember respectively Its activity period was investigatedin Taza a semiarid area in northern Morocco where itwas collected from June to November showing two density

Pathology Research International 3

0

5

10

15

20

25

30

35

May June July August September October

Ph perniciosusPh sergenti

Ph papatasiPh longicuspis

Month

Abun

danc

e of s

andfl

ies (

)

Figure 1 Seasonal variation of sand flies collected in Aichoun bysticky paper traps

peaks [21]Ph sergentiwas the dominant species compared toother species which confirms the results obtained in 2011 [22]and with a maximum activity in July confirming the resultsobtained in Marrakech province [23]

Ph perniciosus one of the most competent L infantumvectors in the Mediterranean foci [24] was present duringall the period of our study This species showed a biphasicactivity and dominating in September (529) This is inline with the results obtained by Guernaoui et al [25] in theprovince of Chichaoua southwest of Morocco

Ph papatasi was also present in our study even if it isconsidered to be adapted to arid climate [26] Ph papatasipopulations were present from May to October with twopeaks These results are in accordance with the data obtainedin Marrakech area in southwestern Morocco [27]

Ph longicuspis was collected in Aichoun locality Thehighest density of this species was observed in AugustThis result is in accordance with Guernaoui et al [28] inChichaoua province where this species showed amonophasiccycle with one density peak in August-September

In the region of Fez Boulmane one similar study ofthe species inventory sand flies in a focus of cutaneousleishmaniasis nominated Ouled aid and belonging to aneighboring province than that Sefrou was realized in 2011during a year between April 2011 and March 2012 [29 30] Ifwe compare our results with those found in this study we caninfer that the same species were encountered but not in thesame abundance Indeed the most abundant species foundwere respectively Phlebotomus papatasi (5052) Phleboto-mus sergenti (247) Phlebotomus perniciosus (969) andPhlebotomus longicuspis (554) [29]

According Lahouiti et al [30] the destruction of vectorsrsquohabitats the improvement of human habitats the treatmentof scraps animal drop-pings dung and the separationbetween animal and human dwellings could be an efficientway to get rid of sand flies and consequently diminish therisks of contamination

In addition to means mentioned above we mustremember that the companions of information-education-communication and the process of integrated management

of vector control piloted together by the health services arevery efficient tools to prevent cases of leishmaniasis

Also these means will be very efficient not only to fightthe mosquito sand fly vector of such diseases but also tocombat the parasite tanks such as rats and stray dogs who areincreasingly responsible formany emerging zoonoses [31 32]

5 Conclusion

This study conducted in Aichoun locality during the monthsof April to October 2012 was aimed at studying the spatialand temporal trends of the main vectors of Leishmania insand flies in this focus 1171 sand flies belonging to thefour species were collected by sticky traps Phlebotomussergentiwas the predominant species (784) followed by Phperniciosus (105) Ph papatasi (794) and Ph longicuspis(316) Sand flies were active during 6 months (MayndashOctober)

The large distribution and the long activity period of Phsergenti and species of the subgenus Larroussius in Aichounlocality indicate the high potential risk of L tropica and Linfantum transmission in this area

Conflict of Interests

The authors declare that they have no conflict of interests

Acknowledgments

The authors thank Mr El Kohli Mohamed M Adlaoui ElBachir Lakraa Lhoussine El Rhazi Mohamed and OuahabiSouad Laboratory Medical Entomology for the constantsupport made during this study Likewise the authors thankthe regional direction of the Fes-Boulemane Health provin-cial delegate of Ministry of Health Sefrou province andstaff of Aichoun locality for their cooperation assistanceinformation and help

References

[1] J A Rioux F Petter O Akalay et al ldquoMeriones shawi (Duver-noy 1842) (Rodentia Gerbillidae) reservoir of Leishmaniamajor Yakimoff and Schokhor 1914 in South Moroccordquo Ren-dered Accounts of Meetings of the Academy of Sciences Series IIILife Sciences vol 294 pp 515ndash517 1982

[2] E Guilvard J A Rioux M Gallego et al ldquoLeishmania tropicainMorocco IIImdashthe vector of Phlebotomus sergenti Apropos of89 isolatesrdquo Annales de Parasitologie Humaine et Comparee vol66 no 3 pp 96ndash99 1991

[3] P Marty Y Le Fichoux F Pratlong J A Rioux G Rostainand J P Lacour ldquoCutaneous leishmaniasis due to Leishmaniatropica in a young Moroccan child observed in Nice FrancerdquoTransactions of the Royal Society of TropicalMedicineampHygienevol 83 no 4 p 510 1989

[4] F Pratlong J A Rioux J Dereure et al ldquoLeishmania tropicain Morocco IVmdashIntrafocal enzyme diversityrdquo Annales de Para-sitologie Humaine et Comparee vol 66 no 3 pp 100ndash104 1991


[5] N Guessous-Idrissi A Hamdani A Rhalem et al ldquoEpidemi-ology of human visceral leishmaniasis in Taounate a northernprovince of Moroccordquo Parasite vol 4 no 2 pp 181ndash185 1997

[6] J A Rioux JMahjoubMGallego et al ldquoLeishmaniose cutaneehumaine a Leishmania infantumMon-24 auMarocrdquo Bulletin dela Societe Francaise de Parasitologie vol 14 pp 179ndash183 1996

[7] R Nejjar M Lemrani A Malki S Ibrahimy H Amarouchand A Benslimane ldquoCanine leishmaniasis due to Leishmaniainfantum MON-1 in northern Moroccordquo Parasite vol 5 no 4pp 325ndash330 1998

[8] DELM 2011 Department of Planning and Financial ResourcesDirectorate of Planning and Research Services Research andHealth Information Health Digit Edit 2012


[10] H Fellah M Rhajaoui S Ouahabi D Belghiti and MLyagoubi ldquoOccurrence of human cutaneous leishmaniasis inZouaghaMyYacoubprovince (Morocco)rdquo International Journalof Agriculture and Biology vol 9 no 1 pp 197ndash198 2007

[11] M Rhajaoui ldquoHuman leishmaniases in Morocco a nosogeo-graphical diversityrdquo Pathologie Biologie vol 59 no 4 pp 226ndash229 2011

[12] D J Lewis ldquoThephlebotomine sandflies (Diptera Psychodidae)of the Oriental Regionrdquo Bulletin of the British Museum (NaturalHistory) (Entomology) vol 37 pp 217ndash343 1978

[13] Ministry of Health (MS) Fight against Leishmaniasis ActivityGuide Ministry of Health (MS) Rabat Morocco 2010

[14] S Berchi A Bounamous K Louadi and B Pesson ldquoMorpho-logical distinction between two sympatric species Phlebotomuspernlciosus and Phlebotomus longicuspis (Diptera Psychodi-dae)rdquoAnnales de la Societe Entomologique de France vol 43 no2 pp 201ndash203 2007

[15] DELM and Directorate of Epidemiology and Disease ControlldquoEco epidemiology of leishmaniasis in Moroccordquo Epidemiolog-ical Bulletin no 65ndash68 pp 1ndash15 2006

[16] Moroccan Ministry of Health Etat drsquoAvancement des Pro-grammes de Lutte Contre les Maladies Parasitaires Directionde lrsquoEpidemiologie et de Lutte Contre les Maladies RabatMorocco 2011

[17] H Asmae A Fatima F Hajiba et al ldquoCoexistence of Leish-mania tropica and Leishmania infantum in Sefrou provinceMoroccordquo Acta Tropica vol 130 no 1 pp 94ndash99 2014

[18] M A Al-ZahraniW Peters D A Evans C Chin V Smith andR P Lane ldquoPhlebotomus sergenti a vector of Leishmania tropicain Saudi Arabiardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 82 no 3 article 416 1988

[19] A Tabbabi N Bousslimi A Rhim K Aoun andA BouratbineldquoFirst report on natural infection of Phlebotomus sergenti withLeishmania promastigotes in the cutaneous leishmaniasis focusin southeastern Tunisiardquo The American Journal of TropicalMedicine and Hygiene vol 85 no 4 pp 646ndash647 2011

[20] J A Rioux ldquoEco-epidemiology of leishmaniasis in Moroccoreview of 30 years of cooperation DELMrdquo EpidemiologicalBulletin vol 37 pp 2ndash10 1999

[21] N Guessous-Idrissi S Chiheb A Hamdani et al ldquoCutaneousleishmaniasis an emerging epidemic focus of Leishmania trop-ica in north Moroccordquo Transactions of the Royal Society ofTropical Medicine and Hygiene vol 91 no 6 pp 660ndash663 1997

[22] C Faraj A El Bachir S Ouahabi et al ldquoDistribution andbionomic of sand flies in five ecologically different cutaneous

Leishmaniasis foci in Moroccordquo ISRN Epidemiology vol 2012Article ID 145031 8 pages 2012

[23] S Boussaa S Guernaoui and A Boumezzough ldquoPeriodicitypf phlebotomine sand flies (h) in an urban area of MarrakechMoroccordquo in Proceedings of the European Multicolloquium ofParasitology pp 18ndash23 2004

[24] R Benikhlef Z Harrat M Toudjine A Djerbouh S Bendali-Braham and M Belkaid ldquoDetection of Leishmania infantumMON-24 in the dogrdquo Medecine Tropicale Revue du Corps deSante Colonial vol 64 no 4 pp 381ndash383 2004

[25] S Guernaoui A Boumezzough and A Laamrani ldquoAltitudinalstructuring of sand flies (Diptera Psychodidae) in the High-Atlas mountains (Morocco) and its relation to the risk ofleishmaniasis transmissionrdquoActaTropica vol 97 no 3 pp 346ndash351 2006

[26] J A Rioux O Akalay J Perieres et al ldquoThe ecoepidemiolog-ical evolution of risk leishmanien Moroccan Atlantic SaharaHeuristic interest bioclimates sandflies relationshiprdquo Mediter-ranean School vol 23 pp 73ndash92 1997

[27] S Boussaa S Guernaoui B Pesson and A BoumezzoughldquoSeasonal fluctuations of phlebotomine sand fly populations(Diptera Psychodidae) in the urban area of MarrakechMoroccordquo Acta Tropica vol 95 no 2 pp 86ndash91 2005

[28] S Guernaoui A Boumezzough B Pesson and G PichonldquoEntomological investigations in Chichaoua an emerging epi-demic focus of cutaneous leishmaniasis in Moroccordquo Journal ofMedical Entomology vol 42 no 4 pp 697ndash701 2005

[29] K Lahouiti A El Ouali Lalami H Hmamouch and K BakhtldquoPhototropism of sand flies species (Diptera Psychodidae)collected in a rural locality in Central Moroccordquo Journal ofParasitology and Vector Biology vol 6 no 5 pp 66ndash74 2014

[30] K Lahouiti A El Ouali Lalami S Maniar and K BekhtildquoSeasonal fluctuations of phlebotomines sand fly populations(Diptera Psychodidae) in the Moulay Yacoub province centreMorocco effect of ecological factorsrdquo African Journal of Envi-ronmental Science and Technology vol 7 no 11 pp 1028ndash10362013

[31] K T Wong and K C Ong ldquoPathology of acute henipavirusinfection in humans and animalsrdquo Pathology Research Interna-tional vol 2011 Article ID 567248 12 pages 2011

[32] H I Al-Sadi and S S Al-Mahmood ldquoPathology of experi-mental Encephalitozoon cuniculi infection in immunocompe-tent and immunosuppressed mice in Iraqrdquo Pathology ResearchInternational vol 2014 Article ID 857036 6 pages 2014

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014


MEDIATORSINFLAMMATION

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Behavioural Neurology

EndocrinologyInternational Journal of



Disease Markers


BioMed Research International

OncologyJournal of



Oxidative Medicine and Cellular Longevity


PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of



Computational and Mathematical Methods in Medicine

OphthalmologyJournal of


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Research and TreatmentAIDS


Gastroenterology Research and Practice


Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom


Table 1 Sandflies collected in Aichoun locality 2012

Subgenus (R Ab ) Species Mal Female Total R Ab ()

Larroussius (1374) Phlebotomus longicuspis 13 24 37 316Phlebotomus perniciosus 113 10 123 1050

Paraphlebotomus (7828) Phlebotomus sergenti 845 73 918 784Phlebotomus (798) Phlebotomus papatasi 63 30 93 794R Ab Relative Abundance

of Moulay Yacoub alone [10 11] The outbreak was rapidlystopped by insecticides use but the disease has persisted sincethat under endemic and epidemic forms in other provinces ofthe regionwithmore than 100 cases each year despite a strongmonitoring plan

The control of the disease is mainly based on case detec-tion and treatment of human cases and on vector controlThisis based essentially on environmental management includingpromotion of improved solid waste disposal practices Theuse of bed nets and local residual indoor spraying withsynthetic pyrethroids are often applied in newly emergedepidemic foci Nevertheless few data are available on thevector Ph sergenti especially seasonal fluctuations of itsabundance This information is essential for the success ofvector control In this context we have conducted this studyfor the first time in a village belonging to the region of Sefrouprovince in center of Morocco

This study also allows a better understanding of thedynamics of the transmission of leishmaniasis in the area ofAichoun and therefore contributes to the future design ofsurveillance strategies

2 Materials and Methods

21 Study Area and Environment The entomological studywas conducted in the locality of Aichoun (33∘391015840N 04∘381015840W)situated in the northwest of theMoroccanMiddleAtlas a partof the province of Sefrou that belongs to the territory pastoralvillage of Tazouta with a cold semiarid climate The meanaltitude is 750m The average annual rainfall is 400mm themain minimum of the coldest month is 2∘C and maximumof the hottest month is 40∘C

The locality of Aichoun is characterized by the presenceof cowsheds caves and accumulation of animal waste thatcreates an environment favorable to the biological cycle ofsand flies The vegetation is characterized by a covering moreor less degraded because of overgrazing and overexploitationfor domestic uses (Tetraclinis articulata Pistacia lentiscusOlea oleaster Olea europaea and Juniperus phoenicea)

22 Sand Fly Collection and Identification Sand flies werecollected bimonthly during their optimum developmentperiod inMorocco betweenMay andOctober Five collectingsites were chosen in Aichoun locality Collections wereperformed by using sticky papers (21 times 273 cm) coated withcastor oil We used 40 traps in each trapping campaignThe traps were installed in different habitats during the dayand were removed the next day Collected sand flies were

transferred in glass tubes containing a solution of ethanolat 70∘ After sex determination all sand flies collected wereidentified by examining the morphology of the pharyngealarmature and spermathecae of female flies and the externalgenitalia of males using the morphological key [12 13]Morphological differentiation of the two sympatric speciesPh longicuspis and Ph perniciosus was made according todescription of Berchi et al [14]

3 Results

31 Taxonomic Inventory of Sand Flies This study has estab-lished a faunal inventory of Aichoun revealing the presenceof four species belonging to the genus Phlebotomus Thesex ratio indicated that more males were collected themalefemale ratio was 754

The collections accounted for 1171 sand fly specimensPh sergenti was the predominant and the most frequentlycollected species with 918 individuals (784) In secondplace comes Ph perniciosus Newstead with 123 (1050)followed by Ph papatasi Scopoli with 93 individuals (794)Ph longicuspisNitzulescu was represented by 316 (Table 1)

32 Seasonal Fluctuations of Sand Flies Species Seasonalactivity of sandflies extended fromMay to the end ofOctoberwith variation in the monthly evolution according to speciesPh sergenti Ph Perniciosus and Ph papatasi displayed abimodal distribution with a first peak in July where Phsergenti dominates (2946) and a second peak in Septemberwith 1383 while Ph longicuspis showed a monophasictrend with a slight peak in August (111) (Figure 1)

4 Discussion

Over the last years incidence of L tropica CL has contin-uously increased in the province of Sefrou [15] Between1997 and 2011 1242 cases were declared [16] The majority ofcases were reported mainly in El Menzel Sefrou AghbalouTazouta Sidi Lahcen and Ain Chegag communes [17]

Ph sergenti is confirmed as vector ofL tropica in northernAfrica Middle East and Central Asia [18 19] the same inMorocco [4] It dominates in arid and semiarid areas [20]In this study area Ph sergenti was largely widespread it waspresent throughout the whole period of our surveys showinga biphasic course evolution with two peaks in July andSeptember respectively Its activity period was investigatedin Taza a semiarid area in northern Morocco where itwas collected from June to November showing two density


0

5

10

15

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Month

Abun

danc

e of s

andfl

ies (

)











5 Conclusion





Acknowledgments


References








































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of

















0

5

10

15

20

25

30

35




Month

Abun

danc

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andfl

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5 Conclusion





Acknowledgments


References








































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of



















































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of
















Leishmaniasis in Central Morocco: Seasonal Fluctuations of ...

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