|
Memórias do Instituto Oswaldo Cruz
Fundação Oswaldo Cruz, Fiocruz
ISSN: 1678-8060 EISSN: 1678-8060
Vol. 91, Num. 5, 1996, pp. 555-560
|
Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(5), 555-560,
Sep/Oct 1996,
A Two Years Study on Vectors of Cutaneous Leishmaniasis.
Evidence for Sylvatic Transmission Cycle in the State of
Campeche, Mexico
Eduardo A Rebollar-Tellez^+, Alejandro Ramirez-Fraire,
Fernando J Andrade-Narvaez
Departamento de Inmunologia, CIR "Dr. Hideyo Noguchi",
Universidad Autonoma de Yucatan, Apdo. Postal 2-1277, Merida,
Yucatan 97240, Mexico
^+Corresponding author. Current address: Department of
Biological Sciences, Keele University, Staffordshire ST5 5BG,
United Kingdom. Fax: 44-1782-630007
Received 20 November 1995
Accepted 20 May 1996
Code Number: OC96102
Size of Files:
Text: 28.7K
Graphics: No associated graphics files
[TABLES AND FIGURES AT END OF TEXT]
Vectors of cutaneous leishmaniasis in the State of Campeche
were studied in relation to the transmission cycle of
Leishmania (Le.) mexicana. To determine how
transmission of leishmaniasis occurs, we collected
phlebotomine sand flies for two years. In the first year
(October 1990 to November 1991) the collections were made with
CDC light traps, Shannon traps and direct captures at natural
shelters around the village (<200 m) of La Libertad. In the
second year (February 1993 to January 1994) the catches were
performed at 8 km southeast of La Libertad in the forest.
Female sand flies were examined for Leishmania. During
the first year, 347 sand flies of nine species were collected,
most of which were Lutzomyia deleoni (61.3%). When all
nine species were considered, more females than males were
captured. Low densities of anthropophillic species of sand
flies around the village indicated that sylvatic transmission
was taking place. For the second year, 1484 sand flies of 16
species were caught. The most common were L. olmeca
olmeca (21.7%), L. cruciata (19.2%) and L.
ovallesi (14.1%). Similarly, more females were caught than
males. Thirty-five females of five species were found infected
with flagellates believed to be Leishmania sp. The
highest infection rate was found in L. olmeca olmeca
(7.1%) followed by L. cruciata (4.5%) and L.
ovallesi (1.1%). These data plus other evidence on the
epidemiology of human cases and results from reservoir studies
are discussed in relation to the sylvatic transmission cycle.
Key words: leishmaniasis - transmission cycle - vector
ecology - Lutzomyia - Mexico
Cutaneous leishmaniasis was first reported in Mexico by
Seidelin (1912) who named it "chiclero's ulcer". Later, it was
reported as an endemic disease on the peninsula of Yucatan,
constituting an occupational hazard among forest labourers
(Beltran & Bustamante 1942). Biagi (1953) identified the
causative parasite as a subspecies of Leishmania
tropica, but Garham (1962) identified the parasite as
Le. mexicana. Recently, Grimaldi et al. (1987)
confirmed that Le. (Leishmania) mexicana
was the most common parasite responsible for chiclero's ulcer
based on monoclonal antibody studies. However Perez-Motul et
al. (1994) demonstrated that Le. (Viannia)
braziliensis is also present on the peninsula of
Yucatan, but at a very low prevalence. The distribution of
cases of leishmaniasis corresponds to the distribution of
forests in Quintana Roo, Campeche and the southern region of
the State of Yucatan. In the State of Campeche the annual
incidence rate of leishmaniasis is 5.08 per 1000 inhabitants
(Andrade-Narvaez et al. 1990). The population at high risk are
males between 14-45 years old who frequently travel deep into
the forest for agricultural activities (Andrade-Narvaez et al.
1992).
Vectors of New World leishmaniasis are small haematophagous
Diptera of the genus Lutzomyia (Young & Arias 1991).
Apart from some taxonomical or distributional reports on sand
flies (e. g., Vargas & Diaz-Najera 1953, Biagi et al. 1966a),
relatively few entomological studies have been performed on
the Yucatan peninsula. However, Biagi et al. (1965) studied
sand flies in the State of Quintana Roo, where they found
seven females of L. olmeca (5.9%) naturally infected
with flagellates. They also proved that experimentally-
infected females of L. olmeca could transmit the
parasite to humans during bloodfeeding.
Despite their findings, there remains little knowledge in
Mexico about important aspects of the transmission cycle
including vector population, seasonal distribution, and vector
capacity of other species of sand flies as vectors.
In our two year study, the main objective was to determine
whether transmission of cutaneous leishmaniasis in the State
of Campeche was peridomestic or sylvatic. This included
studies on anthropophillic species and natural infection
rates.
Materials and methods
Study area -
The first year study was carried out in the village of La
Libertad (18 34' N, 90 31' W), Campeche, Mexico. Population of
this village is presently 922 inhabitants. From 1987 to 1995,
48 cases of cutaneous leishmaniasis have been well-documented.
The second year study was conducted 8 km southeast of La
Libertad, elevation (150 m a.s.l.). Due to the Mayan
agricultural practices, some areas within the forest are
cleared and planted with crops, mainly corn. These areas are
used only for a few years and then abandoned, so at present
the original forest has been mostly destroyed and only a few
large trees remain e.g., gum-trees (Malnikara sapota),
chaka-trees (Bursera simaruba), punab-trees
(Swetenia macrophylla) and ramon-trees (Brosimun
alicastrum). Farmers usually go to these places to work in
their cornfields. We selected a representative site which
included some areas of old forest (>12 years old), areas of
dense bushes and cornfields, all of which were close one to
another.
The weather in the area is classified as dry-humid, the dry
season occurring from May to July. December and January are
the coolest and most humid months of the year (Flores &
Espejel 1994).
Sand fly collections -
During the first year, sand flies were captured around the
village (<200 m) from October 1990 to September 1991 during
three nights every month. Three CDC light traps (Sudia &
Chamberlain 1962) were set from 18:00 to 21:00 hr and at 100 m
interval and a triangular arrangement. A Shannon trap (Shannon
1939), 1.6 x 2.5 x 1.6 m, was placed at 30 cm above the
ground. Inside the Shannon trap, two persons attracted the
flies, but they were protected from bites by their long-
sleeves shirts, long slacks, and a fine mosquito screen-net
covering the head (Perez et al. 1987). All sand flies landing
on either the collectors or walls of the trap were collected.
Collections were made every 30 min from 17:00 to 7:00 hr.
During the day, two persons searched in the holes of dead logs
for resting sand flies, the flies were collected using a mouth
aspirator. All sand flies caught from all three sampling
methods, were preserved dry between layers of tissue paper in
a small pillbox.
During the second year, from February 1993 to January 1994
catches were performed in the forest, monthly during four
nights. Three CDC light traps were set at 1 m height above
ground level at intervals of about 50 m and from 17:00 to
23:00 hr. The Shannon trap was used in the same way as the
previous year, except that it was operated from 17:00 to 23:00
hr. All flies caught from either CDC light traps or Shannon
trap were placed in small vials containing saline solution
(0.65%), gentamicine sulphate (1 mg/ml) and glycerol (10%).
Later at the laboratory of Immunology of the Regional Research
Centre "Dr. Hideyo Noguchi" of the University of Yucatan, the
flies were dissected, and their the guts were checked for
leishmanial infection.
Identification of sand flies and parasite -
The flies collected in the first year study were processed for
slide mounting following the technique of Young and Perkins
(1984). The keys of Forattini (1973), Young (1979), Murillo
and Zeledon (1985) were followed to identify the sand flies.
Dissected female sand flies from the second year, were
identified using the shape of the spermatheca and number of
cibarial teeth. Positive slides of infected sand flies were
stained with Giemsa and parasites were examined under light-
microscope using 40 and 100X objectives. No attempts to
isolate the parasite were made.
Results
During the first year, 347 sand flies of nine species were
collected, the majority being L. deleoni (61.3%) and
L. cruciata (13.7%) (Table I). More females were
captured than males (t test= 14.14; df=8, P<0.01). However,
when sample size of the known anthropophillic species, such as
L. cruciata, L. ovallesi, L.
panamensis, L. shannoni and the proven vector L.
o. olmeca, the number of females was only 83, constituting
23.2% of the catches. Only 50 females (14.0%) of L.
cruciata (40), L. o. olmeca (5) and L.
panamensis (5) were collected in the Shannon trap.
Anthropophillic species were caught mainly between the months
of December and March. The nightly peak of catches was between
19:00 to 20:00 hr. The highest number of sand flies was
obtained with CDC traps (46.5%) followed by direct searching
in natural shelters (37.0%) and in the Shannon trap (16.5%).
These results indicated that near La Libertad, densities of
anthropophillic species of sand flies were very low.
During the second year, 1484 sand flies of 16 species were
caught. The most abundant species were L. o. olmeca
(21.7%), L. cruciata (19.2%) and L. ovallesi
(14.1%) (Table II). More females were captured than males (t
test= 55.4; df=15, P<0.01). The three former species, plus
L. panamensis and L. shannoni, (the
anthropophillic subset), represented 68.9% of all sand flies
collected. Of these five anthropophillic sand flies, 35
females (Table II) were found infected with Leishmania
sp. Although anthropophillic species were collected
throughout the year, infected females of the five species were
found only between November 1993 and February 1994. Twenty
five of these flies had promastigote flagellates in their
midguts. One female of L. ovallesi was found with both
promastigote and amastigote forms of Leishmania sp.,
indicating that it had had a very recent bloodmeal.
The seasonal abundance for these five anthropophillic species
was similar, except that L. o. olmeca had the highest
peak in October. The maximum catches of flies in the Shannon
trap was between 18:00 to 19:00 hr.
Discussion
The low numbers of sand flies captured at La Libertad could be
due to deforestation. Only small bushes remain around the
village, therefore favourable conditions for sand fly breeding
sites, such as shaded areas and soil with high content of
organic matter, is limited. The most common species collected
around the village was L. deleoni, a non-
anthropophillic species (Forattini 1973), and its presence
could be used as an indication that the risk of leishmaniasis
transmission is low. This sand fly species might be more
associated with opossums or armadillos living nearby the
village (Rebollar-Tellez unpublished data). Moreover, L.
deleoni has never been incriminated as vector of
leishmanaisis.
Results from the second year were consistent with the results
of Biagi et al. (1966b). Who found a peak of biting activity
between 18:00 to 19:00 hr for the anthropophillic species of
sand flies in the county of Escarcega, Campeche, Mexico. On
the other hand, Biagi et al. (1965) incriminated L.
olmeca as a proven vector of cutaneous leishmaniasis in
Quintana Roo. In this two-year study, females of L. o.
olmeca had the highest infection rate (7.1%) of all the
species of sand flies collected in the forest. Females of
L. o. olmeca and other members of the L.
flaviscutellata complex, are mainly zoophillic, feeding on
ground-dwelling rodents (Shaw & Lainson 1968), but sometimes
biting humans who enter the forest. Our results support Biagi
et al. (1965) who showed that L. o. olmeca is
relatively anthropophillic. The same species has been reported
as a vector of Le. mexicana transmission in Belize at
an infection rate of 0.5% (Disney 1968).
The second highest species infected was L. cruciata
which has been suspected to be a vector due to its highly
anthropophillic habit (Biagi et al. 1966b). Also, Disney
(1968) found a 0.5% infection rate of females collected in
Belize. Transmission of parasite to human from experimentally-
infected females has been proved (Williams 1970). In
Guatemala, a 0.20% infection rate was reported by Rowton et
al. (1991). In Quintana Roo, Mexico, L. cruciata was by
far the most anthropophillic species of sand flies collected
on human bait (Cruz-Ruiz et al. 1994). Whilst, in a subsequent
study of the present work, Rebollar-Tellez et al. (1996a)
reported L. cruciata in Campeche as the only species
collected on human bait catches re-confirming the highly
anthropophillic behaviour of this species. Additionally,
Rebollar-Tellez et al. (1996b) reported a survival rate of
0.68 per gonotrophic cycle for L. cruciata population
in Campeche, indicating that L. cruciata females could
survive long enough to acquire the parasite during the first
blood-meal and subsequent transmission in the following
cycle.
These two species, L. o. olmeca and L. cruciata,
can be associated with transmission of cutaneous leishmaniasis
caused by Le. (Le.) mexicana in the
Peninsula of Yucatan. Data recorded in the program "Study,
Surveillance and Control of Leishmaniasis, Mexico" (1987-1995)
indicated that the number of human cases at La Libertad
reached a peak from January to April constituting
approximately 70% of all cases reported each year. Men aged 14
or more years, were most commonly infected (A.-Vargas-
Gonzalez, University of Yucatan, per. com.). Also, most
patients believed that they had been bitten by sand flies and
presumably infected with Leishmania in fields located
far from the village. The main transmission period of new
cases of leishmaniasis is correlated with high population
densities of L. o. olmeca in October. The number
of infected females of both L. o. olmeca and L.
cruciata was found mainly during the months of November,
December and January. Rebollar-Tellez et al. (1996a) reported
that population of L. cruciata in Campeche, Mexico, had
peak from December to March. Furthermore, in the same study
area, and since November 1993, small rodents of the species
Oryzomys melanotis, Ototylomys phyllotis and
Sigmodon hispidus were found infected with Le.
(Le.) mexicana. These strains were identical
to those isolates from humans (Chable-Santos et al. 1995).
These data suggest that densities of L. o. olmeca and
L. cruciata with a high infected rate, appearance of
infected reservoirs, and human activities in the forest at
this time, seem to result in seasonal transmission from
November to March each year.
On the other hand, the two infected flies of L.
ovallesi might be associated with transmission of
cutaneous leishmaniasis caused by Le. (V.)
braziliensis. L. ovallesi has been found
naturally infected with Le. (V.)
braziliensis in Guatemala (Rowton et al. 1992). In
Venezuela, unidentified flagellates were also detected in
L. ovallesi females (0.08%) (Feliciangeli et al. 1988).
In the same country, 21 females (0.5%) of L. ovallesi
were infected with flagellates in their midgut and
hindgut, indicating Le. (V.) braziliensis
(Bonfante-Garrido et al. 1991). In our study, we found
flagellates in the midgut of L. ovallesi, but, we were
not able to establish if parasites were also present in the
hindgut, which would have suggested they were Le.
(V.) braziliensis.
In the Yucatan Peninsula seven isolates from human cases of
leishmaniasis caused by Le. (V.)
braziliensis have been identified by isoenzymes and by
indirect immunoflourescence with monoclonal antibodies (MAbs)
(Canto-Lara et al. 1996). Three isolates of Le.
(V.) braziliensis were confirmed by kDNA
hybridization technique (Perez-Motul et al. 1994). Since L.
ovallesis seems to be the natural vector of Le.
(V.) braziliensis, the unidentified flagellates
found in L. ovallesi may have been conspecific with
Le. (V.) braziliensis. However, the
isolation and correct identification and characterization of
Le. (V.) braziliensis from wild-caught
females of L. ovallesi are needed to confirm our
suggestion.
Regarding the role played by L. permira, it is not
possible to evaluate its vector potential, since it was
collected at a very low density (33 females/ year).
In summary, the evidence supports the hypothesis of sylvatic
transmission in the State of Campeche, but more studies are
needed to fully confirm our conclusions.
Acknowledgements
To many people at La Libertad, Campeche, for their help and
facilities in conducting this research. To the Parasitology
team of the Department of Immunology. The senior writer
acknowledges the help of Alberto Vargas-Gonzalez, Nelly E
Albertos-Alpuche and N Van Wynsberghe, University of Yucatan
for reading an early draft of this paper.
This investigation received financial support from UNDP/WORLD
BANK/ WHO Special Programme for Research and Training in
Tropical Diseases (TDR) ID 900248.
References
Andrade-Narvaez FJ, Simmonds-Diaz E, Rico-Aguilar S, Andrade-
Narvaez M, Palomo-Cetina M, Canto-Lara S, Garcia Miss MR,
Madera-Sevilla M, Albertos-Alpuche NE 1990. Incidence of
localized cutaneous leishmaniasis (chiclero's ulcer) in
Mexico. Trans Soc Trop Med Hyg 84: 219-220.
Andrade-Narvaez FJ, Albertos-Alpuche NE, Canto-Lara SB,
Vargas-Gonzalez A, Valencia-Pacheco G, Palomo-Cetina A,
Ramirez-Fraire A, Loria-Lara J, Ceron-Espinosa J, Madera-
Sevilla M, Escalante-Cervantes M, Esquivel-Vinas R, Cardenas-
Marrufo MF, Damian-Centeno AG 1992. Risk factors associated
with cutaneous leishmaniasis infection and disease in the
state of Campeche, Peninsula of Yucatan, Mexico, p. 193-205.
In P Wijeyaratne, T Goodman, C Espinal (eds). Leishmaniasis
Control Strategies: A Critical Evaluation of IDRC-
Supported Research.
Beltran E, Bustamante ME 1942. Datos epidemiologicos acerca de
la "ulcera de los chicleros" (Leishmaniasis Americana) en
Mexico. Rev Inst Salub Enf Trop 3: 1-28.
Biagi F 1953. Algunos comentarios sobre leishmaniasis y sus
agentes etiologicos, Leishmania tropica mexicana, nueva
sub-especies. Medicina (Mex) 33: 385-396.
Biagi AM de, Beltran F, Biagi F 1966a. Nuevos conocimientos
sobre los flebotomos del area endemica de leishmaniasis
cutanea en Yucatan. Rev Invest Salud Publ 26: 139-
153.
Biagi F, Biagi AM de, Beltran F 1965. Phlebotomus
flaviscutellatus, transmisor natural de Leishmania
mexicana. Prensa Med Mex 30: 267-272.
Biagi F, Biagi AM de, Beltran F 1966b. Actividad horaria de
Phlebotomus antropofilicos en la Peninsula de Yucatan.
Rev Inst Salud Publ 26: 73-77.
Bonfante-Garrido R, Urdaneta R, Urdaneta I, Alvarado J 1991.
Natural infection of Lutzomyia ovallesi (Diptera:
Psychodidae) with Leishmania in Duaca, Lara State,
Venezuela. Trans R Soc Trop Med Hyg 85: 61
Canto-Lara SB, Cardenas-Marrufo MF, Vargas-Gonzalez A,
Andrade-Narvaez FJ 1996. Isoenzyme characterization of
Leishmania isolated from human cases with localized
cutaneous leishmaniasis from the state of Campeche, Mexico.
Am J Trop Med Hyg (submitted).
Chable-Santos JB, Van Wynsberghe N, Canto-Lara SB, Andrade-
Narvaez FJ 1995. Isolation of Leishmania (L.)
mexicana from wild rodents and their possible role in
the transmission of localized cutaneous leishmaniasis in the
state of Campeche, Mexico. Am J Trop Med Hyg 53: 141-
145.
Cruz-Ruiz AL, Garcia-Rejon J, Manrique-Saide P, Perez-Motul J
1994. Taxonomical identification of anthropophilic species of
Lutzomyia in Quintana Roo, Peninsula of Yucatan,
Mexico. Rev Biomed 5: 127-131.
Disney RH 1968. Observations on a zoonosis: Leishmaniasis in
British Honduras. J Appl Ecol 5: 1-59.
Feliciangeli MD, Reyes RM, Limongi JE 1988. Natural infection
of Lutzomyia ovallesi (Diptera: Psychodidae) with
parasites of the Leishmania braziliensis complex in a
restricted focus of cutaneous leishmaniasis in northern
Venezuela. Mem Inst Oswaldo Cruz 83: 393-394.
Flores JS, Espejel I 1994. Tipos de vegetacion en la
Peninsula de Yucatan. Etnoflora Yucatanense. Fasciculo 3,
135 pp.
Forattini OP 1973. Entomologia Medica IV. Psychodidae.
Phlebotominae. Leishmanioses. Bartonelose. Edgar Bulcher,
S o Paulo, 658 pp.
Garham PCC 1962. Cutaneous leishmaniasis in the New World with
special reference to Leishmania mexicana. Scientific
Reports of Instituto Superiore di Sanita 2: 76-
82.
Grimaldi G, David JR, McMahon-Pratt D 1987. Identification and
distribution of New World Leishmania species
characterized by serodeme analysis using monoclonal
antibodies. Am J Trop Med Hyg 36: 270-287.
Murillo CM, Zeledon R 1985. Flebotomos de Costa Rica.
Brenesia No. 23. 137 pp.
Navarro-Correa N 1995. Especies de Lutzomyia spp. como
vectores potenciales de leishmaniasis cutanea localizada en
una region selvatica del estado de Campeche, Mexico. Thesis
Biologist, School of Medical Veterinary, University of Yucatan
(unpublished)
Perez-Motul J, Balam-Tzeek L, Canto-Lara S 1994.
Identification de protozoarios del genero Leishmania
con sondas biotinadas de kDNA en la Peninsula de Yucatan,
Mexico. Rev Biomed 5: 60-69.
Perez JE, Villaseca P, Llanos-Cuentas A, Campos M, Guerra H
1987. Tecnicas para colectar "titiras" (Lutzomyia spp.,
Diptera: Psychodidae) en ambientes altoandinos peruanos.
Rev Peru Ent 30: 77-80.
Rebollar-Tellez EA, Reyes-Villanueva F, Fernandez-Salas I,
Andrade-Narvaez FJ 1996a. Population dynamics and biting
rhythm of the anthropophilic sand fly Lutzomyia
cruciata (Diptera: Psychodidae) in Southeast Mexico.
Rev Inst Med Trop S o Paulo (In press).
Rebollar-Tellez, EA, Reyes-Villanueva F, Fernandez-Salas I,
Andrade-Narvaez FJ 1996b. Abundance and parity rate of
Lutzomyia cruciata (Diptera: Psychodidae) in an endemic
focus of localized cutaneous leishmaniasis in Southern Mexico.
J Med Entomol (In press).
Rowton E, de Mata M, Rizzo N, Navin T, Porter C 1991. Vectors
of Leishmania braziliensis in the Peten, Guatemala.
Parassitologia 33 (Suppl. 1) 501-504.
Rowton E, de Mata M, Rizzo N, Porter CH, Navin TR 1992.
Isolation of Leishmania braziliensis from Lutzomyia
ovallesi (Diptera: Psychodidae) in Guatemala. Am J Trop
Med Hyg 46: 465-468.
Seidelin H 1912. Leishmaniasis and babesiasis in Yucatan.
Ann Trop Med Parasitol 6: 295-299.
Shannon R 1939. Methods for collecting and feeding mosquitoes
in jungle yellow fever studies. Am J Trop Med 19: 131-
140.
Shaw JJ, Lainson R 1968. Leishmaniasis in Brazil: II.
Observations on enzootic rodent leishmaniasis in the lower
amazon region. The feeding habits of the vector, Lutzomyia
flaviscutellata in reference to man, rodents and other
animals. Trans R Soc Trop Med Hyg 62: 396-405.
Sudia W, Chamberlain M 1962. Battery operated light trap: An
improved model. Mosq News 22: 126-129.
Vargas L, Diaz-Najera A 1953. Lista de flebotomos mexicanos y
su distribucion geografica (Diptera: Psychodidae). Rev Inst
Salubr Enfer Trop 13: 309-314.
Williams P 1970. Phlebotomine sand flies and leishmaniasis in
British Honduras (Belize).Trans R Soc Trop Med Hyg 64:
317-368.
Young DG 1979. A review of the bloodsucking psychodid flies
of Colombia (Diptera: Phlebotominae and Sycoracinae). Inst
Food Agric Sci Tech. Bull 806, University of Florida,
Gainesville, 266 pp.
Young DG, Arias JR 1992. Phlebotomine sandflies in the
Americas. Pan American Health Organization/ WHO, technical
paper No. 33, 28 pp.
Young DG, Perkins PV 1984. Phlebotomine sand flies of North
America (Diptera: Psychodidae). Mosq News 44: 263-
304.
--------------------------------------------------------------
TABLE I Total number of sand flies species collected in
the first year (October 1990- September 1991) at La Libertad,
Campeche, Mexico
--------------------------------------------------------------
Sampling method
--------------------------------------- Relative
Species NS CDC ST F Total abundance %
--------------------------------------------------------------
L. carpenteri -- 26 1 27 41 11.5
L. cayennensis 5 -- -- 5 11 3.1
L. cruciata^a 4 4 39 47 49 13.7
L. deleoni 14 96 5 115 219 61.3
L. gomezi -- 2 -- 2 3 0.8
L. o. olmeca^b -- 1 5 6 6 1.7
L. ovallesi^a -- -- -- -- 2 0.6
L. panamensis^a -- 3 3 6 15 4.2
L. shannoni^a 3 1 -- 4 11 3.1
NS= natural shelters, CDC= light trap, ST= Shannon trap, F=
female, a: anthropophilic. b: proven vector, L: Lutzomyia
--------------------------------------------------------------
TABLE II Total number of sand flies collected and examined
for flagellates. Flies were captured with CDC light-traps and
Shannon trap in the second year (February 1993-January 1994)
in a forest 8 km southeast of Libertad, Campeche, Mexico
----------------------------------------------------------
Species No. collected No. dissected No. + (%)
--------------------------------------------------------------
L. aclydifera 10 7 ---(0.0)
L. cayennensis 30 30 ---(0.0)
L. carpenteri 116 116 ---(0.0)
L. cratifera 20 20 ---(0.0)
L. cruciata^a 269 269 12(4.5)
L. deleoni 91 91 ---(0.0)
L. dodgei 3 1 ---(0.0)
L. gomezi 65 65 ---(0.0)
L. o. olmeca^b 282 282 20(7.1)
L. ovallesi^a 186 186 2(1.1)
L. panamensis^a 69 69 ---(0.0)
L. permira 33 33 1(3.0)
L. serrana 18 15 ---(0.0)
L. shannoni^a 82 82 1(1.2)
L. trinidadensis 11 9 ---(0.0)
L. undulata 17 13 ---(0.0)
Total 1299 1288 36(16.9)
^a: anthropophilic species, ^b: proven vector, + No. females
with flagellates; L: Lutzomyia; Results of this Table were
taken from Navarro-Correa (1995).
--------------------------------------------------------------
Copyright 1996 Fundacao Oswaldo Cruz
|