• 1

    Gramiccia M, Bettini S, Yasarol S, 1984. Isoenzyme characterization of Leishmania isolates from human cases of cutaneous leishmaniasis in Urfa, south-east Turkey. Trans R Soc Trop Med Hyg 78 :568–568.

    • Search Google Scholar
    • Export Citation
  • 2

    Akman L, Aksu HSZ, Wang RQ, Ozensoy S, Ozbel Y, Alkan Z, Ozcel MA, Culha G, Ozcan K, Uzun S, Memisoglu HR, Chang K-P, 2000. Multi-site DNA polymorphism analyses of Leishmania isolates define their genotypes predicting clinical epidemiology of leishmaniasis in a specific region. J Eukaryot Microbiol 47 :545–554.

    • Search Google Scholar
    • Export Citation
  • 3

    Lepont F, Bayazit Y, Konyar M, Demirhindi H, 1996. Dermal leishmaniasis in the urban focus of Sanliurfa (Turquey). Bull Soc Pathol Exot 89 :274–275.

    • Search Google Scholar
    • Export Citation
  • 4

    Alptekin D, Kasap M, Luleyap U, Kasap H, Aksoy S, Wilson ML, 1999. Sandflies (Diptera : Psychodidae) associated with epidemic cutaneous leishmaniasis in Sanliurfa, Turkey. J Med Entomol 36 :277–281.

    • Search Google Scholar
    • Export Citation
  • 5

    Akkafa F, Tasci S, 1999. Phlebotomus Fauna of the City of Sanliurfa in Southeastern Turkey. T Parazitol Derg 23 :417–422.

  • 6

    Volf P, Ozbel Y, Akkafa F, Svobodova M, Votypka J, Chang K-P, 2002. Sand flies (Diptera: Phlebotominae) in Sanliurfa, Turkey: relationship of Phlebotomus sergenti with the epidemic of anthroponotic cutaneous leishmaniasis. J Med Entomol 39 :12–15.

    • Search Google Scholar
    • Export Citation
  • 7

    Harrison DL, Bates PM, 1991.The Mammals of Arabia. Harrison Zoological Museum Publications, Sevenoaks, UK.

  • 8

    Tesh RB, Chaniotis BN, Aronson MD, Johnson KM, 1971. Natural host preferences of Panamanian phlebotomine sandflies as determined by precipitin test. Am J Trop Med Hyg 20 :150–156.

    • Search Google Scholar
    • Export Citation
  • 9

    de Colmenares M, Portus M, Botet J, Dobano C, Gallego M, Wolff M, Segui G, 1995. Identification of blood meals of Phlebotomus perniciosus (Diptera: Psychodidae) in Spain by a competitive enzyme-linked immunosorbent assay biotin-avidin method. J Med Entomol 32 :229–233.

    • Search Google Scholar
    • Export Citation
  • 10

    Morrison AC, Ferro C, Tesh RB, 1993. Host preferences of the sand fly Lutzomyia longipalpis at an endemic focus of American visceral leishmaniasis in Colombia. Am J Trop Med Hyg 49 :68–75.

    • Search Google Scholar
    • Export Citation
  • 11

    Zivkovic V, Movsesijan M, Miscevic Z, Borojevic D, 1971. Detection of the origin of blood meals in sandflies (Diptera, Psychodidae). Acta Vet Beograd 21 :129–134.

    • Search Google Scholar
    • Export Citation
  • 12

    Guy MW, Killickkendrick R, Gill GS, Rioux JA, Bray RS, 1984. Ecology of leishmaniasis in the south of France.19. Determination of the hosts of Phlebotomus ariasi Tonnoir, 1921 in Cevennes by bloodmeal analyses. Ann Parasitol Hum Comp 59 :449–458.

    • Search Google Scholar
    • Export Citation
  • 13

    Edman JD, Webber LA, Schmidt AA, 1973. Effect of host defenses on the feeding pattern of Culex nigripalpus when offered a choice of blood sources. J Parasitol 60: 874–883. 14. Lane RP, 1986. Chicken house reservoirs of sandflies. Parasitol Today 2 :248–249.

    • Search Google Scholar
    • Export Citation
  • 15

    Schlein Y, Warburg A, Schnur LF, Shlomai J, 1983. Vector compatibility of Phlebotomus papatasi dependent on differentially induced digestion. Acta Trop 40 :65–70.

    • Search Google Scholar
    • Export Citation
  • 16

    Girginkardesler N, Balcioglu IC, Yereli K, Ozbilgin A, Ozbel Y, 2001. Cutaneous leishmaniasis infection in BALB/c mice using a Leishmania tropica strain isolated from Turkey. J Parasitol 87 :1177–1178.

    • Search Google Scholar
    • Export Citation
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

SHORT REPORT: DISTRIBUTION AND FEEDING PREFERENCE OF THE SAND FLIES PHLEBOTOMUS SERGENTI AND P. PAPATASI IN A CUTANEOUS LEISHMANIASIS FOCUS IN SANLIURFA, TURKEY

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  • 1 Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic; Department of Microbiology/ Immunology, University of the Health Sciences/Chicago Medical School, North Chicago, Illinois

Sand flies (Diptera: Psychodidae) and rodents were collected in the endemic focus of urban cutaneous leishmaniasis in Sanliurfa, Turkey. Phlebotomus sergenti and P. papatasi represented 99% of the sand fly population. These flies were trapped in highest numbers in animal sheds, followed by cellars. However, P. sergenti was relatively more abundant in rooms. An enzyme-linked immunosorbent assay of the gut contents from blood-fed females detected immunoglobulins specific to birds and mammals, suggesting that both species are opportunistic feeders, although poultry is a frequent blood source of P. sergenti. Blood sources include black rats (Rattus rattus) and house mice (Mus domesticus); these rodents are abundant inside houses, and might have a role in parasite circulation.

Phlebotomine sand flies (Diptera: Phlebotominae) are vectors of leishmaniasis, a disease caused by several species of the genus Leishmania (Kinetoplastida: Trypanosomatidae). Different species of the parasite are transmitted by specific sand fly vectors. Sanliurfa, located in southeastern Turkey on the border with Syria, is an endemic focus of anthroponotic cutaneous leishmaniasis (ACL) caused by genetically homogeneous Leishmania tropica.1,2 Phlebotomus sergenti, a vector of ACL, and P. papatasi, a vector of zoonotic CL, are the two most abundant sand fly species at this site.36

We report here more detailed studies of these sand flies in Sanliurfa to further understand aspects of their ecology by recording their spatial distribution in houses, the temperature and humidity in the sand fly habitats, and sources of blood for females. Small mammals that may serve as blood source and potential reservoirs of CL were trapped in this focus.

Sand flies were collected in five districts in the old part of the city during September 1999. Centers for Disease Control and Prevention (Atlanta, GA) miniature light traps were placed in different locations (yards, cellars, rooms, sheds, and roof tops) of the houses of patients with active or previous ACL. Typically, nine traps were set every night (three traps in each house) for 11 consecutive days. Traps were set before sunset and collected the next morning. Humidity and/or temperature were recorded using Bionaire Climate Check (Bionaire, Montreal, Canada) and a maximal-minimal thermometer (Exatherm, Železný Brod, Czech Republic) placed near the traps. Species of live and dead fly specimens were identified as described elsewhere.6

Dissected guts from blood-fed females were smeared onto filter paper (No. 3; Whatman, Newton, MA), air-dried and stored at -20°C before use. The degree of blood digestion in the fly guts was graded into three levels: 1) fresh blood (bright red content in the midgut with intact erythrocytes visible under the microscope), 2) partially digested blood (dark red), and 3) extensively digested blood (brown).

The blood meals in fly guts were screened for their sources of origin by an enzyme-linked immunosorbent assay (ELISA) using commercially available antisera specific to different animal immunoglobulins. Filter papers containing blood meals from individual flies were eluted overnight at 4°C in 800 μl of Tris-buffered saline (TBS, 20 mM Tris, 150 mM NaCl, 0.05% Tween 20, 0.1 mM Nα-tosyl-lysine-chloromethylketone, pH 7.6). Samples were homogenized mechanically and centrifuged at 9,000 × g for 10 minutes at 4°C to collect the supernatant. Microtitration plates (Gama, České Budějovice, Czech Republic) were coated for one hour with primary antibodies against immunoglobulins of seven host species representing the readily available blood sources. Primary antibodies (swine anti-human, swine anti-bovine, swine anti-mouse, swine anti-rat, swine anti-goat, rabbit anti-chicken, and rabbit anti-horse immunoglobulins; Sevac, Prague, Czech Republic) were diluted in coating buffer (1 μg/ml of IgG in 20 mM TBS, pH 9). Plates were subsequently blocked by adding 3% rabbit serum for 15 minutes, then incubated with blood meal samples (100 μl/well) in TBS for two hours. The wells were then washed and incubated for one hour with peroxidase-conjugated anti-IgG antibodies (swine anti-human, swine anti-bovine, swine anti-mouse, swine anti-rat [Sevac], rabbit anti-chicken [A-9043; Sigma, St. Louis, MO], rabbit anti-horse [A-6917; Sigma], and monoclonal rabbit anti-goat/sheep [A-9452; Sigma]) at dilutions of 1:500-1: 2,000 in TBS. Wells without blood meals served as negative controls. The substrate buffer contained o-phenylenediamine in phosphate-citrate (0.11 M NaHPO4, 0.5 M citric acid, pH 5.5) and 0.03% hydrogen peroxide. The reaction was stopped with 10% sulfuric acid. Plates were read on Multiscan reader (Labsystems, Helsinki, Finland) at 492 nm using Multiscan Transmit software. In all experiments, the lower limit of a positive reaction was taken as 2-3 mean values of the negative samples.

The anti-immunoglobulin antisera were prescreened to verify their antigenic specificity by reactions with blood samples from different animals. These samples were prepared exactly as described for the sand fly blood meals, including the steps of smearing on filter paper, storage, and elution. Cross-reactions were noted only between closely related animals, i.e., anti-chicken antibody cross-reacted with turkey (Meleagris gallopavo) blood, anti-goat antibody with sheep blood, and anti-rat (Rattus norvegicus) antibody with black rat (Rattus rattus) blood. The anti-rat antiserum did not cross-react with mouse blood. This specificity was further verified with the gut contents of Lutzomyia longipalpis fed on mice or black rats. The anti-rat antibodies showed a positive reaction with black rat blood, but not with mouse blood in the fly guts and vice versa. Statistical tests were performed using Statistica 6.0 (STATSoft, Tulsa, OK) and Statgraphics 4.2 (StatPoint, Englewood Cliffs, NJ) software.

Rodents and insectivores were collected at the same sites for fly collections in August 1998. Snap traps (n = 130 trap-nights) with standard baits (pieces of wick fried in fat with flour), and wooden and live traps (Tomahawk Live Trap Co., Tomahawk, WI) (n = 155 trap-nights) were set in kitchens, basements, and cellars of houses where sand fly collection was under way. Traps were also set in fig orchards and small fields in the vicinity of the town (70 snap traps). Biopsy samples were obtained from the ears, tail, lymph nodes, liver, and spleen of trapped animals for culture in SNB-9 blood agar at 25°C to check for the presence of Leishmania. The specimens were weighed and measured; species were identified according to Harrison and Bates monograph.7 These collections are now kept in the Department of Zoology at Charles University (Prague, Czech Republic).

More than 99% (2,129) of the sand flies trapped were P. sergenti and P. papatasi, with the former species twice as abundant (1,388) and representing 65% of the total. Phlebotomus sergenti predominated in the sand fly fauna sampled from 1998 to 2000.5,6 The male:female ratio was 1.34 (χ2 = 29, P < 0.0001) for P. sergenti and 0.94 for P. papatasi2 = 0.7, P = 0.4).

Sand flies of both species were most abundant in sheds, followed by cellars, and less so in rooms, yards, and roof tops (F = 5.7, P = 0.0004, by analysis of variance [ANOVA]; Table 1). However, the ratio of P. sergenti to P. papatasi differed significantly in these locations (χ2 = 231, P < 0.0001). Phlebotomus papatasi was more abundant in sheds, representing 56% of trapped flies, while P. sergenti was more abundant in rooms (82%). This difference was even more pronounced for females (χ2 = 200, P < 0.0001). Phlebotomus sergenti females represented only 32% of the females trapped in sheds, but they represented 88% of 130 females trapped in rooms. Previously, P. sergenti was also found to be more abundant in houses than in stables;3 thus, this behavior may enhance the probability of its feeding on humans, thereby increasing the transmission of L. tropica in this focus.

Trapping sites differed with regard to humidity and temperature. Evening and morning humidities were highest in sheds and cellars (F = 7.0, P = 0.0001 and F = 6.2, P = 0.002, by ANOVA) where sand flies were trapped in the greatest numbers. Minimal temperature was most predominant in sheds, rooms, and cellars (F = 12.2, P < 0.0001), while maximal temperature was not significantly different between the trapping sites (F = 2.1, P = 0.09). Closed habitats with higher humidity and temperature seem to be preferred by sand flies, at least in September, which is the temperate season in Turkey. However, the relative efficacy of trapping in yards and roofs might be influenced by background light. The presence of domestic animals serving as a blood source for females is probably another factor influencing the higher incidence of sand flies in the shelters.

Of the 588 dissected females, 120 were found to contain blood in their guts. Of these, the percentage of fed P. papatasi was significantly higher (43 of 157, 27%) than that of fed P. sergenti (76 of 430, 18%; χ2 = 6.7, P = 0.01). One fed female was identified as P. brevis. Blood meal samples were tested by ELISA for their sources of origin from different animals with seven different antisera. Sixty-four samples (53%) were positive with at least one antiserum. Identifiable blood meals relative to the total samples examined were proportionally similar for both species (58% in P. sergenti and 46% in P. papatasi; χ2 = 1.43, P = 0.23). However, the efficacy of the ELISA differed significantly for the two fly species in relation to the levels of blood digestion (Table 2). This efficacy did not affect the identification in P. papatasi2 = 2.0, P = 0.37), but did so in P. sergenti2 = 39.1, P < 0.00001). In fact, the origin of the blood meals could not be identified in the latter species beyond level three of digestion. Likewise, Lu. longipalpis blood meals could no longer be identified when they turned dark.8 Our sandwich ELISA is comparable in sensitivity to the competitive ELISA previously used for P. perniciosus, in which 59% of the blood meals are identifiable.9 However, only freshly engorged females may have been tested in this study because they were not dissected, as in other previous studies.10,11 This finding, together with the use of different detection methods (microplate precipitin test, Ouchterlony’s double diffusion test), makes comparison of these results difficult. In samples with level 1 blood digestion, we were able to identify 73% of the blood meals tested, similar to the 83% and 74% of positive rates reported in previous studies.10,11 Countercurrent immuno-electrophoresis, which was used in another study with P. ariasi,12 identified 89% of the blood meals, which was comparable to our results for freshly engorged P. sergenti. The results of our experiments showed that the ELISA used is simple and sensitive, yielding a high percentage of positive identifications even in females with partially digested blood, and after the guts have been checked microscopically for the presence of promastigotes.

Both dominant sand fly species in Sanliurfa feed on domestic animals and wild rodents (Table 3). Poultry is the predominant source of blood found for P. sergenti, representing 65% of the identified blood meals. This source represents only 18% of the blood meals for P. papatasi2 = 16.3, P = 0.00005).

We detected two different blood sources in nine P.sergenti and five P. papatasi, and three blood sources in one P. sergenti and one P. papatasi. Of these, we found mouse and poultry blood in five P. sergenti, rat and poultry blood in two P. sergenti and one P. papatasi, rat and goat/sheep blood in one P. sergenti and one P. papatasi, mouse and rat blood in one P. sergenti and one P. papatasi, and horse and rat blood in one P. papatasi. The triple meals contained cow, horse, and goat/ sheep blood in one P. papatasi, and mouse, rat, and chicken blood in one P. sergenti. These results were not due to cross-reactivity with antisera of closely related species, and they were not influenced by the degree of blood digestion (χ2 = 3.0, P = 0.55). Of the 15 samples with multiple blood meals, 14 contained either mouse or rat blood. Rodents have been shown to display efficient defensive behavior against Culex nigripalpus mosquitoes,13 and we believe that this behavior is also displayed against sand flies, which interrupts their feeding and causes them to feed consecutively on another host. The presence of domestic animals and wild rodents at the same sites than explains 23% frequency of multiple meals. Other sand fly species were also shown to feed on multiple hosts, e.g., 16% of P. perniciosus and 5% of P. ariasi tested.9,12

Our results suggest that the local population of P. sergenti is highly ornithophilic. However, the host-feeding pattern described refers only to the relative frequency of blood source detection in the blood meal samples, which does not necessarily imply a higher preference for a particular host. Phlebotomus sergenti was abundant in cellars where poultry was kept; chicken were shown to display the lowest defensive behavior among several avian and mammalian species.13 Its availability and low irritability affects frequent feeding on poultry; however, the role of poultry as a risk factor in the local focus of ACL is not clear. Poultry kept in cellars represent a rich source of blood for P. sergenti females to sustain their high population numbers. The abundance of sand flies increases vector-host contact and thus the chance for transmission. In addition, we suspect that these chicken cellars may serve as an important breeding place for sand flies in Sanliurfa as they do for other sand fly species.14 Conversely, certain components of bird blood, namely, nucleated turkey erythrocytes, were shown to inhibit the development of L. major in P. papatasi.15 Therefore, a negative effect of chicken blood on L. tropica in P. sergenti cannot be excluded.

Four species of small mammals were trapped, with black rats and house mice being especially abundant (Table 4). Tristram’s jirds were also trapped near human settlements, representing potential reservoir host for zoonotic CL. Results of ELISAs for the blood meals from collected flies showed that they feed on mice and rats. Phlebotomus sergenti and P. papatasi originating in Sanliurfa and raised in laboratory colonies feed on various mammals, including mice and black rats. Moreover, both laboratory mice16 and feral black rats (Svobodová M, unpublished data) are susceptible to L. tropica from the same site. The potential role of these rodents in the transmission of L. tropica is thus suggested, although none of those caught in the field was positive for Leishmania, as assessed by cultivation.

Table 1

Numbers of sand fly collected, and temperature and humidity in different trapping sites*

Mean ± SD number of sand flies per trapMean ± SD number of females per trapMean ± SD temperature (°C)Mean ± SD relative humidity
Trapping site (No. of traps)Total ±SDP. sergenti (%)TotalP. sergenti (% females)MinimalMaximalEveningMorning
*Centers for Disease Control and Prevention light traps were set in houses with cases of cutaneous leishmaniasis. Sand fly numbers represent the average per trap.
Shed (8)95 ± 17642 ± 69 (44)47 ± 8815 ± 21 (32)27 ± 232 ± 247 ± 851 ± 6
Cellar (23)40 ± 4330 ± 32 (75)16 ± 1612 ± 12 (76)25 ± 230 ± 446 ± 658 ± 11
Room (28)10 ± 148 ± 13 (82)5 ± 64 ± 5 (88)26 ± 231 ± 442 ± 440 ± 8
Yard (31)5 ± 54 ± 5 (76)3 ± 22 ± 2 (73)23 ± 330 ± 439 ± 548 ± 12
Roof (8)4 ± 63 ± 5 (77)2 ± 32 ± 3 (79)22 ± 231 ± 241 ± 541 ± 18
Table 2

Percentage of identified blood meals according to the level of blood digestion in Phlebotomus sergenti and P. papatasi

No. (%) of identified blood meals
Level of digestionP. sergentiP. papatasi
113 (93)9 (56)
231 (74)4 (31)
307 (50)
No. not identified32 (42)23 (53)
Table 3

Sources of origin for Phlebotomus sand fly blood meals determined by enzyme-linked immunosorbent assay*

Sand fly hostP. sergentiP. papatasi
* Gut contents from fed females were each screened with seven different antisera specific to potential hosts.
Chicken355
Mouse71
Rat66
Horse04
Sheep/goat22
Cattle34
Human16
Table 4

Small mammals trapped in Sanliurfa, Turkey, 1998

SpeciesNo.
Live and snap traps were placed in the patient’s houses, or in nearby small fields and orchards. All specimens were culture-negative for Leishmania.
Rattus rattus (black rat)28
Mus domesticus (house mouse)25
Meriones cf. tristrami (Tristram’s jird)2
Crocidura suaveolens (lesser white-toothed shrew)4

Acknowledgments: We thank Feridun Akkafa (Harran University, Sanliurfa, Turkey), Seray Ozensoy and Yusuf Ozbel (Ege University, Izmir, Turkey), Jan Votýpka, Eva Dvoráková (Charles University, Prague, Czech Republic), and Kadri Bulut (Harrankapi Health Center, Sanliurfa, Turkey) for assistance in the field.

Financial support: This work was supported by the Ministry of Education of the Czech Republic (grants GAUK 78/1998/BBio and J13/ 981131-B4) to Petr Volf and Milena Svobodová, and by an anonymous source to K.-P. Chang.

REFERENCES

  • 1

    Gramiccia M, Bettini S, Yasarol S, 1984. Isoenzyme characterization of Leishmania isolates from human cases of cutaneous leishmaniasis in Urfa, south-east Turkey. Trans R Soc Trop Med Hyg 78 :568–568.

    • Search Google Scholar
    • Export Citation
  • 2

    Akman L, Aksu HSZ, Wang RQ, Ozensoy S, Ozbel Y, Alkan Z, Ozcel MA, Culha G, Ozcan K, Uzun S, Memisoglu HR, Chang K-P, 2000. Multi-site DNA polymorphism analyses of Leishmania isolates define their genotypes predicting clinical epidemiology of leishmaniasis in a specific region. J Eukaryot Microbiol 47 :545–554.

    • Search Google Scholar
    • Export Citation
  • 3

    Lepont F, Bayazit Y, Konyar M, Demirhindi H, 1996. Dermal leishmaniasis in the urban focus of Sanliurfa (Turquey). Bull Soc Pathol Exot 89 :274–275.

    • Search Google Scholar
    • Export Citation
  • 4

    Alptekin D, Kasap M, Luleyap U, Kasap H, Aksoy S, Wilson ML, 1999. Sandflies (Diptera : Psychodidae) associated with epidemic cutaneous leishmaniasis in Sanliurfa, Turkey. J Med Entomol 36 :277–281.

    • Search Google Scholar
    • Export Citation
  • 5

    Akkafa F, Tasci S, 1999. Phlebotomus Fauna of the City of Sanliurfa in Southeastern Turkey. T Parazitol Derg 23 :417–422.

  • 6

    Volf P, Ozbel Y, Akkafa F, Svobodova M, Votypka J, Chang K-P, 2002. Sand flies (Diptera: Phlebotominae) in Sanliurfa, Turkey: relationship of Phlebotomus sergenti with the epidemic of anthroponotic cutaneous leishmaniasis. J Med Entomol 39 :12–15.

    • Search Google Scholar
    • Export Citation
  • 7

    Harrison DL, Bates PM, 1991.The Mammals of Arabia. Harrison Zoological Museum Publications, Sevenoaks, UK.

  • 8

    Tesh RB, Chaniotis BN, Aronson MD, Johnson KM, 1971. Natural host preferences of Panamanian phlebotomine sandflies as determined by precipitin test. Am J Trop Med Hyg 20 :150–156.

    • Search Google Scholar
    • Export Citation
  • 9

    de Colmenares M, Portus M, Botet J, Dobano C, Gallego M, Wolff M, Segui G, 1995. Identification of blood meals of Phlebotomus perniciosus (Diptera: Psychodidae) in Spain by a competitive enzyme-linked immunosorbent assay biotin-avidin method. J Med Entomol 32 :229–233.

    • Search Google Scholar
    • Export Citation
  • 10

    Morrison AC, Ferro C, Tesh RB, 1993. Host preferences of the sand fly Lutzomyia longipalpis at an endemic focus of American visceral leishmaniasis in Colombia. Am J Trop Med Hyg 49 :68–75.

    • Search Google Scholar
    • Export Citation
  • 11

    Zivkovic V, Movsesijan M, Miscevic Z, Borojevic D, 1971. Detection of the origin of blood meals in sandflies (Diptera, Psychodidae). Acta Vet Beograd 21 :129–134.

    • Search Google Scholar
    • Export Citation
  • 12

    Guy MW, Killickkendrick R, Gill GS, Rioux JA, Bray RS, 1984. Ecology of leishmaniasis in the south of France.19. Determination of the hosts of Phlebotomus ariasi Tonnoir, 1921 in Cevennes by bloodmeal analyses. Ann Parasitol Hum Comp 59 :449–458.

    • Search Google Scholar
    • Export Citation
  • 13

    Edman JD, Webber LA, Schmidt AA, 1973. Effect of host defenses on the feeding pattern of Culex nigripalpus when offered a choice of blood sources. J Parasitol 60: 874–883. 14. Lane RP, 1986. Chicken house reservoirs of sandflies. Parasitol Today 2 :248–249.

    • Search Google Scholar
    • Export Citation
  • 15

    Schlein Y, Warburg A, Schnur LF, Shlomai J, 1983. Vector compatibility of Phlebotomus papatasi dependent on differentially induced digestion. Acta Trop 40 :65–70.

    • Search Google Scholar
    • Export Citation
  • 16

    Girginkardesler N, Balcioglu IC, Yereli K, Ozbilgin A, Ozbel Y, 2001. Cutaneous leishmaniasis infection in BALB/c mice using a Leishmania tropica strain isolated from Turkey. J Parasitol 87 :1177–1178.

    • Search Google Scholar
    • Export Citation

Footnotes

Authors’ addresses: Milena Svobodová, Jovana Sádlová, and Petr Volf, Department of Parasitology, Faculty of Science, Charles University, Vinicná 7, CZ-128 43 Prague 2, Czech Republic. K.-P. Chang Department of Microbiology/Immunology, University of Health Sciences/Chicago Medical School, North Chicago, IL 60064.

Author Notes

Reprint requests: Milena Svobodová, Department of Parasitology, Charles University, Faculty of Science, Vinicná 7, CZ-128 43 Prague 2, Czech Republic, Telephone: 420-2-2195-1814, Fax: 420-2-2491-9704, E-mail: milena@natur.cuni.cz
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