BACKGROUND: Sand fly species of the genus Sergentomyia are proven vectors of reptilian Leishmania that are non-pathogenic to humans. However, a consideration of the role of Sergentomyia spp. in the circulation of mammalian leishmaniasis appears repeatedly in the literature and the possibility of Leishmania transmission to humans remains unclear. Here we studied the susceptibility of colonized Sergentomyia schwetzi to Leishmania donovani and two other Leishmania species pathogenic to humans: L. infantum and L. major. METHODS: Females of laboratory-reared S. schwetzi were infected by cultured Leishmania spp. by feeding through a chicken membrane, dissected at different time intervals post bloodmeal and examined by light microscopy for the abundance and location of infections. RESULTS: All three Leishmania species produced heavy late stage infections in Lutzomyia longipalpis or Phlebotomus duboscqi sand flies used as positive controls. In contrast, none of them completed their developmental cycle in Sergentomyia females; Leishmania promastigotes developed within the bloodmeal enclosed by the peritrophic matrix (PM) but were defecated together with the blood remnants, failing to establish a midgut infection. In S. schwetzi, the PM persisted significantly longer than in L. longipalpis and it was degraded almost simultaneously with defecation. Therefore, Leishmania transformation from procyclic to long nectomonad forms was delayed and parasites did not attach to the midgut epithelium. CONCLUSIONS: Sergentomyia schwetzi is refractory to human Leishmania species and the data indicate that the crucial aspect of the refractoriness is the relative timing of defecation versus PM degradation.

Department of Parasitology Faculty of Science Charles University Vinicna 7 Prague 2 Czech Republic

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Elnaiem DE. Ecology and control of the sand fly vectors of Leishmania donovani in East Africa, with special emphasis on Phlebotomus orientalis. J Vector Ecol. 2011;36(Suppl 1):S23–S31. PubMed

Elnaiem DA, Hassan HK, Ward RD. Associations of Phlebotomus orientalis and other sandflies with vegetation types in the eastern Sudan focus of kala-azar. Med Vet Entomol. 1999;13:198–203. doi: 10.1046/j.1365-2915.1999.00182.x. PubMed DOI

Gebre-Michael T, Malone JB, Balkew M, Ali A, Berhe N, Hailu A, Herzi AA. Mapping the potential distribution of Phlebotomus martini and P-orientalis (Diptera : Psychodidae), vectors of kala-azar in East Africa by use of geographic information systems. Acta Trop. 2004;90:73–86. doi: 10.1016/j.actatropica.2003.09.021. PubMed DOI

Lewis DJ, Ward RD. In: The Leishmaniases in Biology and Medicine. Volume 1: Biology and Epidemiology. Peters W, Killick-Kendrick R, editor. Academic Press; 1987. Transmission and vectors; pp. 235–261.

Zijlstra EE, El-Hassan AM. Leishmaniasis in Sudan 3. Visceral leishmaniasis. Trans R Soc Trop Med Hyg. 2001;95:S27–S58. PubMed

Gebre-Michael T, Balkew M, Alamirew T, Gudeta N, Reta M. Preliminary entomological observations in a highland area of Amhara region, northern Ethiopia, with epidemic visceral leishmaniasis. Ann Trop Med Parasitol. 2007;101:367–370. doi: 10.1179/136485907X176382. PubMed DOI

Hailu A, Balkew M, Berhe N, Meredith SE, Gemetchu T. Is Phlebotomus (Larroussius) orientalis a vector of visceral leishmaniasis in south-west Ethiopia? Acta Trop. 1995;60:15–20. doi: 10.1016/0001-706X(95)00093-T. PubMed DOI

Gebre-Michael T, Balkew M, Berhe N, Hailu A, Mekonnen Y. Further studies on the phlebotomine sandflies of the kala-azar endemic lowlands of Humera-Metema (north-west Ethiopia) with observations on their natural blood meal sources. Parasit Vectors. 2010;3:6. doi: 10.1186/1756-3305-3-6. PubMed DOI PMC

Hoogstraal H, Heyneman D. Leishmaniasis in the Sudan republic. Am J Trop Med Hyg. 1969;18:1091–1210.

Elnaiem DE, Hassan HK, Osman OF, Maingon RD, Killick-Kendrick R, Ward RD. A possible role for Phlebotomus (Anaphlebotomus) rodhaini (Parrot, 1930) in transmission of Leishmania donovani. Parasit Vectors. 2011;4:238. doi: 10.1186/1756-3305-4-238. PubMed DOI PMC

Elnaiem DA, Hassan HK, Ward RD. Phlebotomine sandflies in a focus of visceral leishmaniasis in a border area of eastern Sudan. Ann Trop Med Parasitol. 1997;91:307–318. doi: 10.1080/00034989761157. PubMed DOI

Senghor MW, Faye MN, Faye B, Diarra K, Elguero E, Gaye O, Banuls AL, Niang AA. Ecology of phlebotomine sand flies in the rural community of Mont Rolland (Thies region, Senegal): area of transmission of canine leishmaniasis. PLoS One. 2011;6:e14773. doi: 10.1371/journal.pone.0014773. PubMed DOI PMC

Lainson R, Shaw JJ. In: The leishmaniases in biology and medicine. Peters W, Killick-Kendrick R, editor. London: Academic Press; 1987. Evolution, classification and geographical distribution; pp. 1–120.

Bates PA. Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. Int J Parasitol. 2007;37:1097–1106. doi: 10.1016/j.ijpara.2007.04.003. PubMed DOI PMC

Zhang LM, Leng YJ. Eighty-year research of phlebotomine sandflies (Diptera: Psychodidae) in China (1915–1995). II. Phlebotomine vectors of leishmaniasis in China. Parasite. 1997;4:299–306. PubMed

Mutinga MJ, Massamba NN, Basimike M, Kamau CC, Amimo FA, Onyido AE, Omogo DM, Kyai FM, Wachira DW. Cutaneous leishmaniasis in Kenya: Sergentomyia garnhami (Diptera Psychodidae), a possible vector of Leishmania major in Kitui District: a new focus of the disease. East Afr Med J. 1994;71:424–428. PubMed

Mutinga MJ, Kyai FM, Omogo DM. Investigations on the Epidemiology of Leishmaniases in Kenya .1. Studies on Vectors of Leishmania-Major in Marigat, Baringo District, Kenya. Insect Sci. Applic. 1986;7:181–189.

Gebremichael T, Lane RP. The roles of Phlebotomus martini and P-celiae (Diptera: Phlebotominae) as vectors of visceral leishmaniasis in the Aba Roba focus, southern Ethiopia. Med Vet Entomol. 1996;10:53–62. doi: 10.1111/j.1365-2915.1996.tb00082.x. PubMed DOI

Lambert M, Dereure J, El-Safi SH, Bucheton B, Dessein A, Boni M, Feugier E, Dedet JP. The sandfly fauna in the visceral-leishmaniasis focus of Gedaref, in the Atbara-River area of eastern Sudan. Ann Trop Med Parasitol. 2002;96:631–636. doi: 10.1179/000349802125001474. PubMed DOI

Volf P, Volfova V. Establishment and maintenance of sand fly colonies. J Vector Ecol. 2011;36(Suppl 1):S1–S9. PubMed

Myskova J, Votypka J, Volf P. Leishmania in sand flies: Comparison of quantitative polymerase chain reaction with other techniques to determine the intensity of infection. J Med Entomol. 2008;45:133–138. doi: 10.1603/0022-2585(2008)45[133:LISFCO]2.0.CO;2. PubMed DOI

Sadlova J, Yeo M, Seblova V, Lewis MD, Mauricio I, Volf P, Miles MA. Visualisation of Leishmania donovani fluorescent hybrids during early stage development in the sand fly vector. PLoS One. 2011;6:e19851. doi: 10.1371/journal.pone.0019851. PubMed DOI PMC

Benkova I, Volf P. Effect of temperature on metabolism of Phlebotomus papatasi (Diptera : Psychodidae) J Med Entomol. 2007;44:150–154. doi: 10.1603/0022-2585(2007)44[150:EOTOMO]2.0.CO;2. PubMed DOI

Killick-Kendrick R. Phlebotominae vectors of the leishmaniases: a review. Med Vet Entomol. 1990;4:1–24. doi: 10.1111/j.1365-2915.1990.tb00255.x. PubMed DOI

Kaddu JB, Mutinga MJ, Nyamori MP. Leishmania in Kenyan Phlebotomine Sandflies .4. Artificial Feeding and Attempts to Infect 6 Species of Laboratory-Reared Sandflies with Leishmania-donovani. Insect Sci Applic. 1986;7:731–735.

Lawyer PG, Ngumbi PM, Anjili CO, Odongo SO, Mebrathu YM, Githure JI, Koech DK, Roberts CR. Development of Leishmania major in Phlebotomus duboscqi and Sergentomyia schwetzi (Diptera: Psychodidae) Am J Trop Med Hyg. 1990;43:31–43. PubMed

Bates PA, Rogers ME. New insights into the developmental biology and transmission mechanisms of Leishmania. Curr Mol Med. 2004;4:601–609. doi: 10.2174/1566524043360285. PubMed DOI

Dostalova A, Volf P. Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors. 2012;5:276. doi: 10.1186/1756-3305-5-276. PubMed DOI PMC

Strelkova MV. Intergeneric and individual differences in the character of blood digestion by gnats of the genera Phlebotomus and Sergentomyia. Parazitologiia. 1974;8:126–132. PubMed

Reznik EP, Kuznetsova LA. Some peculiarities of digestion and peritrophic membrane formation in sand flies Sergentomyia arpaklensis. Parazitologiya. 1987;21:16–21.

Pimenta PFP, Modi GB, Pereira ST, Shahabuddin M, Sacks DL. A novel role for the peritrophic matrix in protecting Leishmania from the hydrolytic activities of the sand fly midgut. Parasitology. 1997;115:359–369. doi: 10.1017/S0031182097001510. PubMed DOI

Sadlova J, Volf P. Peritrophic matrix of Phlebotomus duboscqi and its kinetics during Leishmania major development. Cell Tissue Res. 2009;337:313–325. doi: 10.1007/s00441-009-0802-1. PubMed DOI PMC

Charlab R, Ribeiro JMC. Cytostatic Effect of Lutzomyia longipalpis Salivary Gland Homogenates on Leishmania Parasites. Am J Trop Med Hyg. 1993;48:831–838. PubMed

Charlab R, Tesh RB, Rowton ED, Ribeiro JMC. Leishmania amazonensis: Sensitivity of different promastigote morphotypes to salivary gland homogenates of the sand fly Lutzomyia longipalpis. Exp Parasitol. 1995;80:167–175. doi: 10.1006/expr.1995.1021. PubMed DOI

Wilson R, Bates MD, Dostalova A, Jecna L, Dillon RJ, Volf P, Bates PA. Stage-specific adhesion of Leishmania promastigotes to sand fly midguts assessed using an improved comparative binding assay. PLoS Negl Trop Dis. 2010;4:e816. doi: 10.1371/journal.pntd.0000816. PubMed DOI PMC

Shatova SM, Saf’ianova VM, Ovezmukhammedov A. An experimental study of the interrelations of Leishmania (Sauroleishmania) gymnodactyli and the sandfly Sergentomyia arpaklensis (Diptera: Phlebotominae) Parazitologiia. 1991;25:110–115. PubMed

Kaddu JB. Leishmania in Kenyan Phlebotomine Sandflies .3. Advances in the Investigations of Vectorial Capacity and Vector Parasite Relationships of Various Species of Sandflies in Kenya. Insect Sci Applic. 1986;7:207–212.

Berdjane-Brouk Z, Kone AK, Djimde AA, Charrel RN, Ravel C, Delaunay P, Del GP, Diarra AZ, Doumbo S, Goita S, Thera MA, Depaquit J, Marty P, Doumbo OK, Izri A. First detection of Leishmania major DNA in Sergentomyia (Spelaeomyia) darlingi from cutaneous leishmaniasis foci in Mali. PLoS One. 2012;7:e28266. doi: 10.1371/journal.pone.0028266. PubMed DOI PMC

Parvizi P, Amirkhani A. Mitochondrial DNA characterization of Sergentomyia sintoni populations and finding mammalian Leishmania infections in this sandfly by using ITS-rDNA gene. Iranian J Vet Res. 2008;9:9–18.

Mukherjee S, Hassan MQ, Ghosh A, Ghosh KN, Bhattacharya A, Adhya S. Short report. Leishmania DNA in Phlebotomus and Sergentomyia species during a kala-azar epidemic. Am J Trop Med Hyg. 1997;57:423–425. PubMed

Seblova V, Sadlova J, Carpenter S, Volf P. Development of Leishmania parasites in Culicoides nubeculosus (Diptera: Ceratopogonidae) and implications for screening vector competence. J Med Entomol. 2012;49:967–970. doi: 10.1603/ME12053. PubMed DOI

Rogers ME, Bates PA. Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. PLoS Pathog. 2007;3:818–825. PubMed PMC

Stamper LW, Patrick RL, Fay MP, Lawyer PG, Elnaiem DE, Secundino N, Debrabant A, Sacks DL, Peters NC. Infection parameters in the sand fly vector that predict transmission of Leishmania major. PLoS Negl Trop Dis. 2011;5:e1288. doi: 10.1371/journal.pntd.0001288. PubMed DOI PMC

Deribe K, Meribo K, Gebre-Michael T, Hailu A, Ali A, Aseffa A, Davey G. The burden of neglected tropical diseases in Ethiopia, and opportunities for integrated control and elimination. Parasit Vectors. 2012;5:240. doi: 10.1186/1756-3305-5-240. PubMed DOI PMC

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Phlebotomine sand flies (Diptera: Psychodidae) of the Maghreb region: A systematic review of distribution, morphology, and role in the transmission of the pathogens

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Refractoriness of Sergentomyia schwetzi to Leishmania spp. is mediated by the peritrophic matrix

Leishmania mortality in sand fly blood meal is not species-specific and does not result from direct effect of proteinases

Lutzomyia migonei is a permissive vector competent for Leishmania infantum

A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies

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