Leishmaniasis in Morocco: Diseases and Vectors

Home , Al Haouz Province, Chichaoua Province

Asian Pac J Trop Dis 2014; 4(Suppl 2): S530-S534 S530

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1* 1,2 3 1 4 1* Kholoud Kahime , Samia Boussaa , Lahouari Bounoua , Ouanaimi Fouad , Mohammed Messouli , Ali Boumezzough 1Laboratory of Ecology and Environment, (URAC 32, CNRST; ERACNERS 06), Faculty of Sciences Semlalia, Cadi Ayyad University, Marrakesh, Morocco 2Institut Supérieur des Professions Infirmières et des Techniques de Santé, Marrakesh, Morocco 3Biospheric Sciences Laboratory, NASA’s Goddard Space Flight Center, Maryland, USA 4Laboratory of Hydrobiology, Ecotoxicology and Sanitation, Faculty of Sciences Semlalia, Cadi Ayyad University, Marrakesh, Morocco

ARTICLE INFO ABSTRACT

Article history: Leishmaniasis, a highly neglected disease, currently presents a significant health problem Received 23 Apr 2014 throughout Africa. This review presents a summarized analysis of its epidemiology in Moroccan Received in revised form 28 Jul 2014 context, a Mediterranean location in which leishmaniasis is prevalent and where both cutaneous Accepted 2 Aug 2014 and visceral leishmaniasis have been reported. Available online 15 Aug 2014 This study aims to determine the current leishmaniasis epidemiological situation in Morocco and the distribution of its different forms throughout the country. During the past 20 years, this disease Keywords: has emerged as a major public health threat in Morocco. So, we gave a particular attention to vectorial status of Moroccan sandflies (Diptera: Psychodidae, Phlebotominae) in view of its major L eishmaniasis role in diseases spreading. E pidemiology It seems clear that the risk of spread of the disease is rising in Morocco. Ecological characteristic V ector of proven and potential vectors, according to climate and environmental changes, should be S andfly regarded as good marker to anticipate leishmaniasis distribution in Morocco. Morocco

1. Introduction Phlebotomus papatasi P. papatasi I M ( ) n Phlebotomusorocco, the sergenti P. sergenti ( ) and L. major are L.th tropicae most I M n orocco, leishmaniases are endemic diseases posing a common vectorPhlebotomuss for the spre ariasiad of P. ariasi anPhlebotomusd , I 2011 M M [3] ( ) major threat to public health. n , oroccan inistry of rperniciosusespectively P.. perniciosus , Phlebotomus H 4 319 (CL) ( ) ealth reported cases of cutaneous leishmaniasis longicuspis P. longicuspis , and potentially 107 (VL)[1] ( ) and cases of visceral leishmaniasis . Leishmania L. infantum are reported to be the vectors of CL M [3] P is cLeishmaniaaused by th majorree cl inL.ic majorally impLeishmaniaortant tropica in editerranean countries . revious studies ( ) M sL.pe ctropicaies [ Leishmania infantum, L. infantum in orocco showed that the distribution of sandflies was ( ), and ( )], a due, in great part, to the bioclimate[4]. T I M flagellate protozoL.a infantumof the family rypanosomitidae, while, n orocco, both zoonotic and anthroponotic forms were VL is caused by . Recently, the mucocutaneous reported. The main reservoirs are dogs for zoonotic VL (ZVL), form was also reported in Morocco, but remains rare[2]. rodents for zoonotic CL (ZCL) and human for anthroponotic Leishmania infection is transmitted to human host as CL (ACL). (D a result of a bite by an infected female sanPhlebotomusdfly iptera: ) Psychodidae, Phlebotominae of the genus . 2. Epidemiology

C K K A B L E * orresponding author: holéoud ahime and li oumezzoughé, aboratoire cologie Due to its geographical position, Morocco possesses and Environnement L2E, Facult des Sciences Semlalia, Universit Cadi Ayyad, BP 2390, Marrakech 40000, Morocco. different ecological and climatic conditions, which are Tel: +212 (0) 662 130 564 important factors in the repartition and epidemiology E-mail: [email protected], [email protected] Foundation Project: Supported by Laboratory of Ecology and Environment (CNRST, of endemic neglected diseases such as leishmaniasis. URAC 32; ERA-CNERS 06) and the National Centre for Studies and Research on the According to Moroccan Ministry of Health, CL caused S CNERS P (C N 06 ERACNERS) L. major ahara, roject ontract . / . by is the most dominant form (Figure 1), with Kholoud Kahime et al./Asian Pac J Trop Dis 2014; 4(Suppl 2): S530-S534 S531

24 000 [1] more than cases reported duL.ri nmajorg the last decade . dichotomy between visceral and cutaneous leishmaniasiL.s, E (F 2) A pidemiological data show that dominated in rinfantumespectively L. itropicagure . n overlap of foci, including 1990 2000 the s,L. h otropicawever startL.in ginfantum in , the apparition and and bL.eg ainfantumn then to emerge. (F C VL growth of L. major and L. tropica is noticeable igure urrently, due to is distributed mainly 1). Including and , the highest CL cases in Northern Morocco Rif and pre-Rif region (Figure 2A), 2000 2010 W VL were noted between and . hile cases remains geographically separated from other areas by mL.o utropicantains comparatively stable (Figure 1). which constitute a natural barrier[12]. The ACL has the widest geographic distribution with large foci in thL.e 6 C W M (F 2B) ZCL majorentral and estern orocco igure , while, the is dispersed in the south and south-east of the Atlas

0 5

伊 ( ) 1 Mountain Figure 2C where the disease is located in the [10] 4 steppe fringes of the Sahara desert . H owever, for the extremeet s al.outh, there are no available 3 epidemiological data. Rioux have led an entomological survey carried out in the littoral zone of the Western Saharan

u m b e r o f c a s 2 N region of Morocco, namely in Tan-Tan, Tarfaya, Layoun, B D [13] T 1 oujdour and akhla . he authors noted the scarcit’y of vector species and absence of leishmaniasis cases. It s 0 necessary to update theses entomological data and assess 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 the current status of human leishmaniasis in the entire L.tropica L.infantum L.major S M Figure 1. L. major L. tropica L. extreme outhern orocco. Evolution of cutaneous ( + ) and visceral ( infantum ) leishmaniasis cases between 1990-2010 in Morocco. 3. ZCL According to the same source, all ages are affected by the different forms of disease, with a high incidence for youth. In the pre-Saharan area, ZCL has been identified since S VL [5] 1914[11] O T CL imilar to thL.e tropica case , young childL.re majorn are at high risk for , in the palm grove of ued ata where a major both CL by [6,7] and CL by [8]. In the same epidemic manifested during the late 1970s. Currently, foci of way, leishmaniasis affects both genders almost equally ZCL are basically linked to palm groves, rural and periurban [7,8] T with a slight increase in women . he large Leishmanianumbers of areas with degraded environmental and socio-economic women and children infected, indicates that conditions like poor housing and hygiene[8]. It is widespread transmission may have occurred in the peridomiciliar from the Atlantic coast, south of the Anti-Atlas mountains habitat[6]. to the north-east, crossing Saharan areas south of the Anti- T A H A M A here is evidence that changes in climate contribute to tlas and igh tlas mounL.ta imajorns, and east of the iddle tlas [14] C some extent to the incidence and expansion of the range of mountaP.in spapatasi. aused byMeriones shawi, this grandisform is transmitted the CL[9,10], but the absence of leishmaniasis epidemiological by the , with as the main information collection system pre-1993 did not allow reservoir host[10]. All strains isolated from the host, human to accurately describe the epidemiological situation in and vector are iL.de nmajortical and are identified biochemically Morocco[11] or to establish correlations between dynamics of as being due to MON-25[15]. The same results were the disease and global changes. found on skin smears in 2007, in the provinces of Ouarzazate S 1993 E [16] ince , various studies of leishmaniasis foci together andP. papatasirrachidia . with the national incidence statistics confirmed the change was reported in Morocco as early as 1916[17]. in geographical distribution of leishmaniasis in Morocco, This species is very common and has a significant ecological marked by the disappearance of the traditional North-South plasticity. It can be found in various biotopes, including

Tetouan N Tetouan N T ador Taownate ador Larache aounale Berkane Taza Berkane C Taza Ouazane F hefchaouen Fes es Guerclf J Sale Guercif Settat erada Boulemane Boulem ane B M A ElkelaaBeni Mellai Midelt eni ellal zilal Chichoua M Tinghir Azilal Errachidia Figuig arr akech Alh aouz Essaouira T Aihaouz inghir Tinghir Essaouira Zagora Taroudannt Quarzazate Inzgane Zagora Tiznit Chtouka ait baha Tata Guelmim

Number of VL cases Number of ZCL cases Number of ACL cases 1-6 16-146 1-42 146 295 6-17 42-199 - 199-447 295-587 C A B Figure 2. L. infantum L. tropica L. major Geographical distribution of VL due to (A), ACL cases due to (B) and ZCL cases due to (C) in Morocco (cases recorded in 2011). Kholoud Kahime et al./Asian Pac J Trop Dis 2014; 4(Suppl 2): S530-S534 S532

[17,18] E T [34] W N hou-ses, animal sheds and caves , and is most frequent at ssaouira and aza . hen its populations from orthern 400 800 [19] S M P. papatasi m above sea level . and oP.u tsergentihern orocco were investigated by isoenzymatic is well adapted to arid climate and its density tools, did not present genetic characteristics of a increases with the aridity[10]. In Marrakech City, its seasonal single species[35]. A fluctuation shows two peaks, the first inP. s upapatasimmer and the s closely related vectors, other endemic sandP.fl ysergenti species [20] T D second in fall . he establishment of in the are also present. Phlebotomusepending on alexandri the regionPhlebotomus, [19] T city appears to have been favoured by urbanization . he chabaudiis sympatrPhlebotomusic with kezeruni Phlebotomus, riouxi, disease progresses as small localized epidemics and cases , and/or are diagnosed between late fall and late winter. Then, lull however the vectorial status of all these species is still not periods occur as the aboriginal population is protected well unknown in Morocco. E [10] by acquired immunity, as in P.th epapatasi rrachidia region . G enetically and phenotypically, populations are 5. VL and CL due to L. infantum supposed to be highly homogeneous[21], but this assumption [22-25] B L.sti lmajorl requires morP.e ipapatasinvestigations Phlebotomus. eside sbergeroti this proven L. infantum vector, and are The first human CL case caused by in Morocco M A E S E R T 1996 sympatric in orocco, lgeria, gypt,Phlebotomus udan, and bergerotithiopia was detected in the central if region of aounate in , [26] VL[11] I VL with possibility of cross-breeding L.. major within an active focus of . n contrast, was detected may play a role in transmission of , like in Iran[27] many years before. The first case of infantile kala-azar has which suggests that future studies should include other been described in 1921 in the region of Tanger with a single M 1922[15] factors related to this suspected vector and its vectorial adL.ul infantumt case reported for one nurse in eknes in . competence/capacity in Morocco. CL is a rare condition with a few sporadic cases T in the north of the country. he enzL.ym infantumatic identification of MON 24[36] 4. ACL the parasite showed that it is the - . Molecular investigations, conducted in 2007 in the province S K L. tropica of L.id iinfantum acem showed the existence of skin lesions caused ACL P. sergenti is caused by and transmitted by the sandfly bP.y ariasi , with domestic dogs as reservoir host and [3] D [16] R S P with humans as thL.e tropicaonly reservoir . omestic as vecL.to rtropica. ecentlyL., ininfantum efrou rovince, the dogs were found infected with in some rural areas, coexistence of and by species- ITS1 PCR RFLP [37] A however these are not regarded as animal reservoirs and the specificL. tropica- - assay was noted . nthroponotic [15] CL F T transmission cycL.le tropica is still considered to be anthroponotic . foci of are found around es and aza in the In Morocco, was isolated, for the first time in eastern central parts of Morocco, not far from VL foci[29]. 1987 [28] S F , from cutaneous lesion in a young child . ince then, urL.th etropicarmore, several cases of canine leishmaniasis caused many eco-epidemiological studies were carried out in by have been reported in regions where canine L. infantum[16] central and southern areaL.s tropicaof the country with the aim to leishmaniasis is caused by . detect CL foci caused by . Several foci have been The VL form is widespread throughout the country. It reported in the rural areas of Azilal, Essaouira, Chichaoua is more frequent in the northern part with sporadic cases and Al Haouz[6,28] and the urban and peri-urban regions of observed in other regions, particularly in the south[15]. T Z M Y [29] A VL 1999 aza and ouagL.ha tropica oulay aacoub . ctually, the situation remained quasi-static since I M A n orocco, is characterizeL.d tropicaby high enzymatic with hundreds of cases reported each year. lmost all of S ( MON 102 polymorphism. even zymodemes - , these cases originated in tradL.iti oinfantumnal northern foci, where MON 107 MON 109 MON 112 MON 113 MON 122 [38] - , - , - , - , - , anP.d this disease is sporadic . is transmitted MON 123) L sergenti- were detected in human, dogs andL. thtropicae sandfly by sandflies belonging to the subgenus arroussius with [30]. In addition, a new zymodeme ( MON- dogs being the main host reservoir. Within this subgenus, 279) VL A H , responsible for canine , was detected in l oceima little is known about Phlebotomusthe distributi omariaen and/o r Phlebotomusthe vectorial [29] A ACL ( in the north of country . ctually, the is widespread in rchadlii,ole of iPhlebotomusts species perfiliewi, Phlebotomus, langeroni, P. C S M the semi-arid regions of entral and outh-westeP.rn sergentiorocco perniciosus P. longicuspis P. ariasi ) M where it is transmitted anthroponotically by . , P. ariasi or P. perniciosus in orocco. T [31,32] N his vector has an extensive geographical distribution . evertheless, and aP.re longicuspisthe proven Its role as vector was identified in Tanant-Azilal region, vectors in Mediterranean countries[33,36], while [39] howe‘ver it was a’lso reported in all biocliP.m asergentitic zones is a suspected one . P. ariasi with preferences for semi-arid regions[19]. is The vectorial role of has been described in endophilic in Morocco, where it is abundant in rural as well Northern Morocco in Taounate Province, where, one [18] P. sergenti P. ariasi L. infantum[11] P. as urban population habitats . was collected up fariasiemale was found infected by et. al 1 400 800 G to m with the highest densities recorded between - distP.ri bariasiution is limited to mountain. uernaoui . 999 [33] 1 000 1 400 m abovL.e stropicaea levelP. .sergenti collected in altitude ranging between and As the , shows considerable genetic m[33]. However, in Morocco, VL is not limited to mountain M T DNA variation in orocco. hP.ree sergenti mitochondrial- haplotypes and is mainly located in the northern regions and at different were identified among populations of Azilal, altitudes (Nador, 62 m; Al Hoceima, 14 m; Tetouan, 1 m; Taza, Kholoud Kahime et al./Asian Pac J Trop Dis 2014; 4(Suppl 2): S530-S534 S533 Acknowledgements 1 100 m; Taounate, 567 m; Sidi Kacem, 55 m; Fez, 300 m and M 560 ) [36,38] eknes, m with sporadic cases in the sP.ou tperniciosush . I M T n north of orocco, typicalL. m oinfantumrphs of are he authors would like to appreciate the kind [39] A D E D the most abundant foP.rm perniciosuss of . lthough in collaboration of irectorate of pidemiology and isease C M H R 10010 M W the southerP.n rlongicuspisegions, , mainly as an atypical ontrol, inistry of ealth, abat , orocco. arm form, and are sympatric, particularly in the thanks are due to Mr. A. El. Laamrani and Mr. N. Haddou for [11] H S T mP.o ulongicuspisntainous regions . oLarroussisuswever, in pre- aharan regions, help with the epidemiological data. his article is supported is the only species sufficiently by Laboratory of Ecology and Environment, (CNRST, URAC VL[39] 32 ERA CNERS 06) N C S abundant to be credibly suspected of transP.m itperniciosusting . ; - and the ational entre for tudies and F R S CNERS P (C N 06 urthermoP.re , perniciosusthe taxonomP.ic longicuspisstatus of the esearch on the ahara, roject ontract . / complex ( , and a potential ERACNERS). cryptic species) should be confirmed as well as its vectorial capacity and competence of its species. References

6. Conclusion [1] M oroccan Ministry of Health. [A report on progress of control programs against parasitic diseases]. Rabat: Directorate of CL VL Epidemiology and Disease Control, Ministry of Health; 2013. and are still significant public healLeishmaniath issues in Morocco. The increase in transmission of French. [Online] Available from: http://www.sante.gov.ma/ appears to be linked to changes in environment and departements/delm/index-delm.htm [Accessed on 15th July, disruption of its natural balance by ways of urbanization, 2014] rural exodus, unhealthy habitats and precarity, all of which [2] I guermia S, Harmouche T, Mikou O, Amarti A, Mernissi FZ. [Mucocutaneous leishmaniasis in Morocco, evidence of the promote settlement of the insect vector and/or reservoir that ’ Med Mal Infect 41 could exacerbate the epidemiological situation[8]. parasite s ecological evolution?]. 2011; (1): 47- Significant attention and priority must be given to 48. French. the studies of eco-epidemiology and spatio-temporal [3] W orld Health Organization. Control of the leishmaniasis: report distribution of vectors, reservoirs as well as the diseases they of a meeting of the WHO Expert Committee on the Control transmit and their relationships to changes in climate. Only of Leishmaniases. Geneva: World Health Organization; 2010. an integrated approach can give us a better understanding [Online] Available from: http://whqlibdoc.who.int/trs/WHO_ of these relationships and allow us to predict the associated TRS_949_eng.pdf [Accessed on 15th July, 2014] risk level. Use of geographical information systems and [4] P rudhomme J, Gunay F, Rahola N, Ouanaimi F, Guernaoui S, Boumezzough A, et al, Wing size and shape variation of remote sensing can help in investigations of large-scale Phlebotomus papatasi (Diptera: Psychodidae) populations from distributions and geographical risk assessment of the J the south and north slopes of the Atlas Mountains in Morocco. disease, but so far such investigations on leishmaniasis have Vector Ecol 37 been absent or rare partly because of the complexity of the 2012; (1): 137-147. disease transmission cycle. [5] H ouda T. The infantile visceral leishmaniasis (about 73 cases) An health-ecosystemic approach seems prominent to allow [dissertation]. Fez City: Sidi Mohammed Ben Abdellah University; for propose realistic and effective strategies for prevention, 2011. control and monitoring. Thus it is necessary to create a [6] R amaoui K, Guernaoui S, Boumezzough A. Entomological and epidemiological study of a new focus of cutaneous leishmaniasis regional network in order to share information, and direct a Parasitol Res 103 - collaborative programme of combined health education, risk in Morocco. 2008; : 859 863. [7] Z ougaghi L, Bouskraoui M, Amine M, Akhdari N, Amal S. assessment and mass screening of both infections in order to Leishmania tropica [Cutaneous leishmaniasis due to in the area help early diagnosis and treatment. In order to be proactive, Revue Francophone I of Marrakech (Morocco): a rebellious focus!]. t •is needed to: des Laboratoires Improvement of the awareness and preparedness of the 2011; doi: 10.1016/S1773-035X(11)70765-1. French. [8] K ahime K, Bounoua B, Messouli M, Boussaa S, Ouanaimi p o •pulation to health problems such as leishmaniasis; Reappraisal of current plans to improve the robustness of F, Boumezzough A. Evaluation of eco-adaptation strategies design standards in those infrastructures which are usually of health to climate change: case of zoonotic cutaneous leishmaniasis (ZCL) as vulnerability indicator in pre-Saharan r u •dimentary; Environmental change region of Morocco. In: Behnassi M, editor. Creating a strong partnership between the health sector and human security and other sectors, an essential step in effective epidemic . Berlin: Springer; 2014. combat and control and orienting and charting the transverse [9] T oumi A, Chlif S, Bettaieb J, Alaya NB, Boukthir A, Ahmadi ZE, measures. et al. Temporal dynamics and impact of climate factors on the cases of zoonotic cutaneous leishmaniasis in Central Tunisia. PLoS Negl Trop Dis 6 2012; (5): e1633. Conflict of interest statement [10] B ounoua L, Kahime K, Houti L, Blakey T, Ebi KL, Zhang P, et al. Linking climate to incidence of zoonotic cutaneous leishmaniasis L. major Int J Environ Res Public We declare that we have no conflict of interest. ( ) in pre-Saharan North Africa. Kholoud Kahime et al./Asian Pac J Trop Dis 2014; 4(Suppl 2): S530-S534 S534 Health 10 Phlebotomus papatasi 2013; (8): 3172-3191. as revealed by microsatellite variation. Med Vet Entomol 23 [11] B oussaa, S. [Epidemiology of leishmaniasis in the region 2009; : 69-77. of Marrakesh, Morocco: impact of urbanization on the [25] D antas-Torres F, Latrofa MS, Otranto D. Occurrence and genetic Phlebotomus Phlebotomus papatasi spatio-temporal distribution of and molecular variability of in an urban area of Southern Parasit Vectors 3 characterization of their populations]. Strasbourg: University of Italy. 2010; : 77. Strasbourg; 2008. French. [Online] Available from: http://scd- [26] F ryauff D, Hanaffi H. Demonstration of hybridization between Phlebotomus papatasi Phlebotomus bergeroti theses.u-strasbg.fr/1494/01/BOUSSAA_Samia_2008.pdf [Accessed (Scopoli) and Parrot. Parassitoligia 33 on 15th July, 2014] 1991; : 237-243. [12] Boudrissa A, Cherif K, Kherrachi I, Benbetka S, Bouiba L, [27] P arvizi P, Alaeenovin E, Kazerooni PA, Ready PD. Low diversity Leishmania major Leishmania Boubidi SC, et al. [Spread of to the north of of parasites in sandflies and the absence of the Bull Soc Pathol Exot 105 Algeria]. 2012; (1): 30-35. French. great gerbil in foci of zoonotic cutaneous leishmaniasis in Fars é è é Trans R Soc Trop Med Hyg 107 [13] R ioux JA, Akalay O, P ri res J, Dereure J, Mahjour J, Le Hou rou Province, Southern Iran. 2013; (6): ‘ HN, et al. [Evolution of eco-epidemiological of leishmaniasis 356-362. ’ risk at Atlantic Moroccan Sahara. Heuristic interest of the [28] R hajaoui M, Sebti F, Fellah H, Alam MZ, Nasereddin A, Abbasi ‘ ’ Ecol Mediterr 23 - relationship sandflies bioclimates ]. 1997; : 73 I, et al. Identification of the causative agent of cutaneous . Parasite 92. French. leishmaniasis in Chichaoua Province, Morocco 2012; 19 [14] R iyad M, Chiheb S, Soussi-Abdallaoui M. Cutaneous (1): 81-84. Leishmania major leishmaniasis caused by in Morocco: still a [29] R hajaoui M, Fellah H, Pratlong F, Dedet JP, Lyagoubi M. East Mediterr Health J 19 Leishmania tropica topical question. 2013; (5): 495-501. Leishmaniasis due to MON-102 in a new Trans R Soc Trop Med Hyg 98 - [15] R hajaoui M . [H uman leishmaniases in M orocco: a Moroccan focus. 2004; : 299 301. Pathol Biol (Paris) 59 ç nosogeographical diversity]. 2011; : 226-229. [30] T lam ani Z, Er-Rami M. The current status of cutaneous Turkiye Parazitol Derg 38 French. leishmaniasis in Morocco. 2014; : 5-8. ó í á á [16] R hajaoui M, Abedelmajed N, Fellah H, Azmi K, Amrir F, [31] B ar n S, Mart n-S nchez J, G llego M, Morales-Yuste M, á Al-jawabreh A, et al. New clinico-epidemiologic profile of Boussaa S, Morillas-M rquez F. Intraspecific variability (rDNA Emerg Infect Dis 13 Phlebotomus sergenti cutaneous leishmaniasis, Morocco. 2007; (9): ITS and mtDNA Cyt b) of in Spain and - Acta Trop 107 1358 1360. Morocco. 2008; : 259-267. Ö ğ Ö Ş ö Ö [17] G uernaoui S, Ramaoui K, Rahola N, Barnabe C, Sereno D, [32] zbel Y, Balcio lu IC, lgen MK, imsek FM, T z S , Ertabaklar Boumezzough A. Malformations of the genitalia in male H, et al. Spatial distribution of phlebotomine sand flies in the Phlebotomus papatasi J Vector (Scopoli) (Diptera: Psychodidae). Aydin Mountains and surroundings: the main focus of cutaneous Ecol 35 J Vector Ecol 36 2010; (1): 13-19. leishmaniasis in Western Turkey. 2011; (Suppl 1): [18] G uernaoui S, Boumezzough A. Habitat preferences of 99-105. phlebotomine sand flies (Diptera: Psychodidae) in Southwestern [33] G uernaoui S, Boumezzough A, Laamrani A. Altitudinal J Med Entomol 46 Morocco. 2009; (5): 1187-1194. structuring of sand flies (Diptera: Psychodidae) in the High-Atlas [19] B oussaa S, Neffa M, Pesson B, Boumezzough A. Phlebotomine mountains (Morocco) and its relation to the risk of leishmaniasis Acta Trop 97 - sandflies (Diptera: Psychodidae) of Southern Morocco: results transmission. 2006; : 346 351. - of entomological surveys along the Marrakech Ouarzazat and [34] Y ahia H, Ready PD, Hamdani A, Testa JM, Guessous-Idrissi N. - Ann Trop Med Parasitol 104 Phlebotomus sergenti Marrakech Azilal roads. 2010; (2): Regional genetic differentiation of in three - Leishmania 163 170. Moroccan foci of cutaneous leishmaniasis caused by tropica Parasite 11 [20] B oussaa S, Guernaoui S, Pesson B, Boumezzough A. Seasonal . 2004; : 189-199. fluctuations of phlebotomine sand fly populations (Diptera: [35] B oussaa S, Pesson B, Boumezzough A. Faunistic study of Acta Trop Psychodidae) in the urban area of Marrakech, Morocco. the sandflies (Diptera: Psychodidae) in an emerging focus of 95 - Ann 2005; : 86 91. cutaneous leishmaniasis in Al Haouz Province, Morocco. Trop Med Parasitol 103 - [21] B oussaa S, Perrotey S, Boumezzough A, Harrak R, Hilali S, 2009; (1): 73 83. Phlebotomus papatasi Pesson B. Isoenzymatic characterization of [36] A mro A, Hamdi S, Lemrani M, Idrissi M, Hida M, Rhajaoui M, J Med Leishmania infantum (Diptera: Psychodidae) of the Marrakech Area, Morocco. et al, Moroccan : genetic diversity and Entomol 45 2008; (3): 370-374. population structure as revealed by multi-locus microsatellite é PLoS One 8 [22] D epaquit J, Lienard E, Verzeaux-Griffon A, Fert H, Bounamous typing. 2013; (10): e77778. A, Gantier JC, et al. Molecular homogeneity in diverse [37] A smae H, Fatima A, Hajiba F, Mbarek K, Khadija B, Mohamed Phlebotomus papatasi Leishmania tropica Leishmania geographical populations of (Diptera, R, et al. Coexistence of and infantum Acta Trop 130 - Psychodidae) inferred from ND4 and mtDNA and ITS2 rDNA: in Sefrou Province, Morocco. 2014; : 94 Infect Genet Evol 8 epidemiological consequences. 2008; : 159-170. 99. A report on progress of control [23] H amarsheh O, Presber W, Al-Jawabreh A, Abdeen Z, Amro [38] M oroccan Ministry of Health. ö Phlebotomus papatasi programs against parasitic diseases, annual activity report. A, Sch nian G. Molecular markers for Rabat: - (Diptera: Psychodidae) and their usefulness for population genetic Moroccan Ministry of Health; 2010, p. 34 49. Trans R Soc Trop Med Hyg 103 analysis. 2009; : 1085-1086. [39] B oussaa S, Boumezzough A, Remy PE, Glasser N, Pesson B. Phlebotomus [24] H amarsheh O, Presber W, Yaghoobi-Ershadi MR, Amro A, Morphological and isoenzymatic differentiation of perniciosus Phlebotomus longicuspis Al-Jawabreh A, Sawalha S, et al. Population structure and and (Diptera: Psychodidae) Leishmania major Acta Trop 106 - geographical subdivision of the vector in Southern Morocco. 2008; : 184 189.