A

Macdt(IsV©

K

1

oSsroeri

Vi

0d

Available online at www.sciencedirect.com

Acta Tropica 105 (2008) 55–61

Seasonal variation of Lutzomyia longipalpis (Lutz & Neiva, 1912)(Diptera: Psychodidae: Phlebotominae) in endemic area of visceralleishmaniasis, Campo Grande, state of Mato Grosso do Sul, Brazil

Alessandra Gutierrez Oliveira a,∗, Eunice Aparecida Bianchi Galati c,Carlos Eurico Fernandes a, Maria Elizabeth Cavalheiros Dorval a, Reginaldo Pecanha Brazil b

a Departamento de Patologia, Laboratorio de Parasitologia, UFMS, Caixa Postal 549, CEP 79070-900 Campo Grande, MS, Brazilb Departamento de Bioquımica e Biologia Molecular, Instituto Oswaldo Cruz-FIOCRUZ, Av. Brasil, 4365, CEP 21040-900 Rio de Janeiro, RJ, Brazil

c Departamento de Epidemiologia, Faculdade de Saude Publica, USP, Av. Doutor Arnaldo, 715, CEP 01246-904 Sao Paulo, SP, Brazil

Received 5 March 2007; received in revised form 31 May 2007; accepted 26 September 2007Available online 7 October 2007

bstract

The seasonal distribution of Lutzomyia longipalpis was studied in two forested and five domiciliary areas of the urban area of Campo Grande;S, from December 2003 to November 2005. Weekly captures were carried out with CDC light traps positioned on ground and in the canopy insideresidual forest and on the edge (ground) of a woodland and in at least one of the following ecotopes in peridomiciles—a cultivated area, a chickenoop, a pigsty, a kennel, a goat and sheep shelter and an intradomicile. A total of 9519 sand flies were collected, 2666 during the first year and 6853uring the second. L. longipalpis was found throughout the 2-year period, presenting smaller peaks at intervals of 2–3 months and two greater peaks,he first in February and the second in April 2005, soon after periods of heavy rain. Only In one of the woodlands was a significant negative correlation

p < 0.05) between the number of insects and temperature during the first year and the climatic factors (temperature, RHA and rain) was observed.n the domiciliary areas in four domiciles some positive correlations (p ≤ 0.05) occurred in relation to one or more climatic factors; however, thepecies shows a clear tendency to greater frequency (72%) in the rainy season than in the dry (28%). Thus, we recommend an intensification of theL control measures applied in Campo Grande, MS, during the rainy season with a view to reducing the risk of the transmission of the disease.2007 Elsevier B.V. All rights reserved.

rosso

ctttt2

ttd

eywords: Phlebotominae; Lutzomyia longipalpis; Seasonal variation; Mato G

. Introduction

In Campo Grande, MS, visceral leishmaniasis (VL) is a seri-us public health problem. Data supplied by the Epidemiologicalurveillance Department of the Municipal Health Secretariat,hows that there has been an increase in the number of caseseported since 2002, when the first human autochthonous casesf VL (total of 19) were diagnosed. In subsequent years, the dis-ase has spread throughout the municipality with, a total of 490egistered cases, up to and including 2005 and thus confirmingts endemic nature.

The presence of Lutzomyia longipalpis, the main vector ofL in Brazil, was reported in Campo Grande for the first time

n 2000, when it was the most common species collected in the

∗ Corresponding author. Tel.: +55 67 3345 7369.E-mail address: agoliveira@nin.ufms.br (A.G. Oliveira).

2

2

to

001-706X/$ – see front matter © 2007 Elsevier B.V. All rights reserved.oi:10.1016/j.actatropica.2007.09.008

do Sul; Brazil

entral area of the city. L. longipalpis was found to be presenthroughout the year, with the greatest density being recorded inhe period following that of the heaviest rainfall, in peridomes-ic/domestic environments, suggesting its potential relevance tohe transmission of VL in the municipality (Oliveira et al., 2000,003).

Given that VL and L. longipalpis are widely distributed inhe Campo Grande urban area the purpose of this study waso determine if there was a relationship between climate andensity of L. longipalpis in Campo Grande.

. Material and methods

.1. General characteristics of Campo Grande

The municipality of Campo Grande is located in the cen-ral part of Mato Grosso do Sul State. Covering 8118.4 km2, itccupies 2.27% of the total area of the state and according to

5 ta Tro

at((a

dAwatat

2

cisfi

2

ltoovsiiwt

oSs

Fa

6 A.G. Oliveira et al. / Ac

n estimate by the Brazilian Institute of Geography and Statis-ics for 2004, it has an urban population of 734,164 inhabitantsInstituto Municipal de Planejamento Urbano de Campo GrandePLANURB), 2006). The center of the municipality is situatedt 20◦26′34′′S and 54◦38′47′′W.

According to the classification of Koppen (1948), the pre-ominant climate is of the tropical rainy type of Savanna, subtypeW, characterized by the irregular annual distribution of rain,ith a well defined dry period from April to September andrainy season from October to March. The average annual

emperature is around 23 ◦C, December is the hottest month,t approximately 25 ◦C and June the coldest, with an averageemperature of 18 ◦C.

.2. Area of study

The captures were carried out in three regions of the city

hosen because of the density and diversity of sand flies reportedn a previous study (Oliveira et al., 2003) (Fig. 1). In total sevenites were sampled including two areas of residual forest andve domiciliary environments.

BCG

ig. 1. Area of study where the captures were carried out in three regions of the citynd domiciles 1 and 2; B, domiciles 3 and 4; C, Chacara Wood and domicile 5.

pica 105 (2008) 55–61

.3. Sand fly captures

Simultaneously, in each of the seven selected sites, ateast one automatic light trap (Natal et al., 1991) was posi-ioned inside the forest (on the ground and in the canopy)n the edge of the woodland (on the ground) and in at leastne of the following peridomiciliary environments—a culti-ated area, a chicken coop, a pigsty, a kennel, a goat andheep shelter and an intradomiciliary environment. The trapsnstalled in the canopy were placed at a height of approx-mately 5 m and those on the ground at 1 m. The capturesere made weekly dusk to dawn regardless of official summer

ime.The sand flies captured were transported to the Laboratory

f Parasitology of the Federal University of Mato Grosso doul (UFMS) for species identification. The nomenclature of thepecies adopted was that of Galati (2003).

The meteorological data was supplied by the Empresarasileira de Pesquisa Agropecuaria, EMBRAPA (CNPGC-entro Nacional de Pesquisa de Gado de Corte) in Camporande, Mato Grosso do Sul, Brazil.

of Campo Grande, Mato Grosso do Sul State, Brazil. A, Ze Pereira woodland

A.G. Oliveira et al. / Acta Tropica 105 (2008) 55–61 57

Table 1Frequencies of Lutzomyia longipalpis by ecotope, in urban Campo Grande, December 2003 to November 2005

First year (December 2003–November 2004) Second year (December 2004–November 2005) Total

M F Total Percentage M F Total Percentage

Ze Pereira 50 39 89 3.3 175 167 342 5.0 431Chacara Wood 49 11 60 2.3 157 43 200 2.0 260Domicile 1 230 72 302 11.3 54 25 79 1.2 381Domicile 2 154 47 201 7.5 43 23 66 1.0 267Domicile 3 1,339 392 1,731 64.9 4,229 1,434 5,663 82.6 7,394Domicile 4 85 45 130 4.9 160 144 304 4.4 434Domicile 5 128 25 153 5.7 170 29 199 2.9 352

T

2

omblmaa

3

moo

mt

2ahGm

otas

FD

otal 2,035 631 2,666 100.0

.4. Data analysis

The frequency of capture of each species per month wasbtained by Williams’ geometric mean (Haddow, 1960). Theethod of Spearmann was used to estimate any correlations

etween climatic variables and the number of specimens of L.ongipalpis. The comparisons of the frequencies in terms of cli-

ate as between the sand fly populations for the various periodsnd climatic seasons were made by the Chi-square (χ2) test forbsolute frequencies.

. Results

A total of 9519 specimens of L. longipalpis, 7023 (73.78%)ales and 2496 (26.22%) females, were captured. The number

f insects (by sex) collected in each season of each of the 2 yearsf study is presented in Table 1, which shows that about 2.5 times

lws

ig. 2. Monthly distribution of Lutzomyia longipalpis captured in the urban area ofecember 2003 to November 2004 (first year) and December 2004 to November 200

4,988 1,865 6,853 100.0 9,519

ore specimens were collected in the second year compared tohe first year.

The monthly distribution of L. longipalpis during each of theyears obtained from the total number of specimens captured

t all the sites are represented in Fig. 2. The rainfall, the relativeumidity of the air, the average monthly temperature in Camporande, from November 2003 to December 2005, and Williams’onthly geometric average for L. longipalpis are shown in Fig. 3.In the first 6 months of 2004, small peaks of fly density were

bserved in March, April and June and from October onwardshere was continuous growth culminating in a peak in Februarynd another small one in April 2005. These last events occurredoon after a rainy season of about 4 consecutive months.

In the Ze Pereira woodland the monthly distribution of L.ongipalpis was more uniform in the second year, as comparedith the first; however, the population density was greater in the

econd half of each year. There was a statistically significant

Campo Grande, MS, in accordance with climatic variation during the period5 (second year). *χ2 = 38.9, GL = 1, p < 0.001; **χ2 = 344.7, GL = 1, p < 0.001.

58 A.G. Oliveira et al. / Acta Tropica 105 (2008) 55–61

Fig. 3. Monthly rainfall (mm), average monthly temperature (◦C) and monthlydpN

dgitync

cgs

Table 2Distribution of the frequencies of Lutzomyia longipalpis in the urban area ofCampo Grande, MS, by season and intra or peridomicile of the dwellingssampled, during the period December 2003 to November 2005

Season

Dry Rainy

Intra Peri Total Intra Peri Total

Domicile 1 110* 36 146 177*,a 58b 235c

Domicile 2 38 75* 113 63d 91**,e 154f

Domicile 3 86 2647* 2733 139a 4522*,g 4661c

Domicile 4 39 127* 166 111a 157* 268c

Domicile 5 15 127* 142 20h 190*,g 210c

a p < 0.01 (Intra × Intra).b p < 0.05 (Peri × Peri).c p < 0.01 (Total × Total).d p < 0.05 (Intra × Intra).e p > 0.05 (Peri × Peri).f p < 0.05 (Total × Total).g p < 0.01 (Peri × Peri).h

t2

bS

Ft

istribution (Williams’ average, Xw) of the total specimens Lutzomyia longi-alpis captured in all the ecotopes during the period December 2003 toovember 2005. Campo Grande, Mato Grosso do Sul, Brazil.

ifference between the 2 years (p < 0.001) when the numbers ofrounds level catches (χ2 = 81.9; GL = 1) in the woodland andts edge (χ2 = 72.9; GL = 1) were compared. In Chacara Wood,he number of insects captured was also greater in the secondear and there was a significantly difference (p < 0.001) in theumber of sand flies captured in the canopy (χ2 = 15.0; GL = 1)ompared to the edge (χ2 = 69.0; GL = 1) (Fig. 4).

The monthly distribution of specimens in intra and peridomi-ile locations within the residential areas, demonstrated the sameeneral tendency, there being significantly a greater number ofand flies in the hot, rainy seasons (p < 0.05) of the 2 years, with

ttt(

ig. 4. Monthly distribution of Lutzomyia longipalpis captured on the ground, in the co November 2005, in urban Campo Grande, MS, Brazil.

p > 0.05 (Intra × Intra).* p < 0.01 (Intra × Peri, same season).

** p < 0.05 (Intra × Peri, same season).

he exception of the peridomicile and intradomicile of dwellingsand 5, respectively (p > 0.05) (Fig. 5 and Table 2).The association between the climatic factors and the num-

er of L. longipalpis collected was analyzed for each ecotope.ignificant statistical correlations were found in some of the eco-

opes as between each of the three climatic variables (rainfall,emperature and humidity) and the number of specimens cap-ured for each of the three ecotopes, as observed in domicile 1p < 0.05), as shown in Table 3.

anopy and on the edge of the two woodlands during the period December 2003

A.G. Oliveira et al. / Acta Tropica 105 (2008) 55–61 59

Fig. 5. Monthly distribution of Lutzomyia longipalpis, by intra and peridomicilie in the dwellings sampled from December 2003 to November 2005. Campo Grandec

4

twoo

yo(

ity, Mato Grosso do Sul state, Brazil.

. Discussion

Specimens of L. longipalpis were captured every month in

he urban area of Campo Grande during the 2 study years,ith increases in number caught occurring at intervals of 2r 3 months (Fig. 3). It was observed that two of these peaksccurred in the winter months (June and August) of the first

ihec

ear and two others in the autumn (March and April) of the sec-nd year. These data corroborate those obtained by Galati et al.2003) in Bonito, also in the State of Mato Grosso do Sul, where

ncreases in population were reported in similar periods. Thisad not observed in a previous study carried out by Oliveirat al. (2003) in Campo Grande, probably due to the atypicallimatic conditions prevailing that year.

60 A.G. Oliveira et al. / Acta Tropica 105 (2008) 55–61

Table 3Associations among the climatic variables (temperature, relative humidity air and rain) and the respective ecotopes for the specimens of Lutzomyia longipalpiscaptured in urban Campo Grande, MS, December 2003 to November 2005

First year (December 2003–November 2004) Second year (December 2004–November 2005)

Temperature (◦C) RHA (%) Rain (mm) Temperature (◦C) RHA (%) Rain (mm)

Ze Pereira ns ns ns ns ns nsChacara Wood −0.53** ns ns ns −0.61** −0.55**

Domicile 1 ns ns ns 0.59** 0.66** 0.60**

Domicile 2 ns ns ns ns ns nsDomicile 3 ns ns ns 0.63** ns nsDomicile 4 0.75* ns ns ns ns nsDomicile 5 ns 0.73* ns ns ns ns

T **

*

biaCawdavmr(

ow2stepieasMRtdMp2

ttptbict

hwom

iphee

trVaro

A

ittCaft

4

R

A

otal ns ns ns

p < 0.001; **p < 0.05; ns, not significant.

No great differences were observed in the monthly distri-ution profile of specimens captured either in the forested orn residential areas. In the interior of the Ze Pereira woodland,t ground level, and at the edge of the residual forest of thehacara Wood, the highest densities had occurred in the autumnnd winter months, whereas, in the residential areas specimensere captured in similar numbers practically every month. Thisifferential behavior is probably due to the differences in rainfallnd not to the other climatic factors which show no significantariation during the year. Therefore, in Campo Grande, the cli-atic seasons should not be defined by the habitual standard but

ather as the rainy season (October–March) and the dry seasonApril–September).

The highest densities of L. longipalpis occurred during peri-ds following heavy rainfall, as observed in February 2005,hen a population explosion occurred immediately after themonths with the heaviest rain (a total of 498 mm). The

ignificant increase on the numbers of insects captured inhe intradomiciles during the rainy periods perhaps may bexplained by the inadequate condition of the resting sites in theeridomiciles. This tendency of L. longipalpis to predominaten the rainy season has already been observed in the North-ast, West-Central and Southeast Brazilian regions, which arereas that have a significant occurrence of visceral leishmania-is (Barata et al., 2004; Deane, 1956; Galati et al., 2003, 2006;

argonari et al., 2004; Oliveira et al., 2003; Rebelo, 2001;esende et al., 2006; Sherlock and Guitton, 1969). However,

his high density profile has already been shown to occur inrier areas of Costa Rica (Zeledon et al., 1984) as well as inato Grosso do Sul, in periods of drought, there being some

eaks in the autumn and winter (the dry season) (Galati et al.,003).

Despite the importance of the rainfall and the humidity inhe data obtained from Campo Grande, the overall analysis ofhe correlations between the climatic factors and the L. longi-alpis population density did not present significant results inhe majority of the ecotopes, as had already been demonstrated

y Margonari et al. (2004) in Belo Horizonte, MG. Nonetheless,n dwelling 1, each of the three climatic variables had a positiveorrelation (p < 0.05) with density, though on the other hand, inhe forested area of Chacara Wood, the rainfall and the relative

A

B

0.63 ns ns

umidity of the air presented a negative correlation (p < 0.05)ith density, corroborating the comment of Barata et al. (2004)n their study in Porteirinha, MG, that the use of a mathematicalodel demonstrated this correlation.The great frequencies of L. longipalpis in the residence 3

s mainly attributed to the presence of chicken-house in itseridomicile, demonstrating the role of chicken as promoter ofigh densities of this sand fly. This fact corroborates the prefer-nce of L. longipalpis by domestic chickens observed by Lainsont al. (1983), Aguiar et al. (1987) and Alexander et al. (2002).

The high seasonal fluctuation in numbers of L. longipalpishroughout the year, predominating in Campo Grande in theainy season which occurs with the presence of the endemicL, demonstrate the need for the development of a permanent

wareness based on continued health education together withigorous epidemiological surveillance to maintain the reductionf the risks of VL transmission (Desjeux, 2001).

cknowledgements

We wish to thank Mr. Orcy de Oliveira for his assistancen both field and laboratory activities and the maintenance ofhe equipment, as also the inhabitants of the studied areas forheir patience and kindness. To Dr. J. Gordon Hamilton and Dr.laudio Barros for reviewing the manuscript. Thanks are duelso to our colleagues in the Laboratory of Parasitology (UFMS)or their help and to the administrative staff of the UCDB forheir logistic support.

Financial support: FUNDECT 498/02, DECIT/FUNDECT1/100208/2003.

eferences

guiar, G.M., Vilela, M.L., Lima, R.B., 1987. Ecology of the sandflies of Itaguai,an area of cutaneous leishmaniasis in the state of Rio de Janeiro. Food pref-erences (Diptera, Psychodidae, Phlebotominae). Mem. Inst. Oswaldo Cruz.82, 583–584.

lexander, B., de Carvalho, R.L., McCallum, H., Pereira, M.H., 2002. Role ofthe domestic chicken (Gallus gallus) in the epidemiology of urban visceralleishmaniasis in Brazil. Emerg. Infect. Dis. 8, 1480–1485.

arata, R.A., Franca-Silva, J.C., Fortes-Dias, C.L., Costa, R.T., Silva, J.C.,Vieira, E.P., Prata, A., Michalsky, E.M., Dias, E.S., 2004. Phlebotomines

ta Tro

D

D

G

G

G

H

I

KL

M

N

O

O

R

R

S

missor. Rev. Bras. Malariol. Doencas Trop. 21, 541–548.

A.G. Oliveira et al. / Ac

sand flies in Porteirinha, an endemic area of American visceral leishma-niasis in the state of Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz. 99,481–487.

eane, L.M., 1956. Leishmaniose visceral no Brasil. Estudos sobre Reser-vatorios e Transmissores no Estado do Ceara. Servico Nacional de EducacaoSanitaria, Rio de Janeiro, 162 pp.

esjeux, P., 2001. The increase in risk factors for leishmaniasis worldwide.Trans. R. Soc. Trop. Med. Hyg. 95, 239–243.

alati, E.A.B., 2003. Classificacao de Phlebotominae. In: Rangel, E.F., Lainson,R. (Eds.). Flebotomıneos do Brasil. Fiocruz, Rio de Janeiro, pp. 23–51.

alati, E.A.B., Nunes, V.L., Cristaldo, G., Rocha, H.C., 2003. Aspectos docomportamento da fauna flebotomınea (Diptera: Psychodidae) em foco deleishmaniose visceral e tegumentar na Serra da Bodoquena e area adjacente,Estado de Mato Grosso do Sul, Brasil. Rev. Patol. Trop. 32, 235–261.

alati, E.A.B., Nunes, V.L., Boggiani, P.C., Dorval, M.E.C., Cristaldo, G.,Rocha, H.C., Oshiro, E.T., Damasceno-Junior, G.A., 2006. Phlebotomines(Diptera: Psychodidae) in forested areas of the Serra da Bodoquena, state ofMato Grosso do Sul, Brazil. Mem. Inst. Oswaldo Cruz. 101, 175–193.

addow, A.J., 1960. Studies on the biting-habits and medical importance ofEast African mosquitos in the genus Aedes. I. Subgenera Aedimorphus,Banksinella and Nunnius. Bull. Entomol. Res. 50, 759–779.

nstituto Municipal de Planejamento Urbano de Campo Grande (PLANURB),2006. Perfil Socioeconomico de Campo Grande. Retrieved on May 21, 2007,from http://www.pmcg.ms.gov.br/PLANURB/downloads/capitulo 02.pdf.

oppen, W., 1948. Climatologia. Fondo de Cultura Economica, Mexico.ainson, R., Shaw, J.J., Silveira, F.T., Fraiha, H., 1983. Leishmaniasis in Brazil.

XIX. Visceral leishmaniasis in the Amazon Region, and the presence ofLutzomyia longipalpis on the Island of Marajo, Para State. Trans. R. Soc.Trop. Med. Hyg. 77, 323–330.

Z

pica 105 (2008) 55–61 61

argonari, C.S., Pessanha, J.E., Barata, R.A., Monteiro, E.M., Costa, D.C.,Dias, E.S., 2004. Study on phlebotomine sand fly (Diptera: Psychodidae)fauna in Belo Horizonte, State of Minas Gerais, Brazil. Mem. Inst. OswaldoCruz. 99, 795–803.

atal, D., Marucci, D., Reis, I.M., Galati, E.A.B., 1991. Modificacao daarmadilha CDC com testes para coletas de flebotomıneos (Diptera). Rev.Bras. Entomol. 35, 697–700.

liveira, A.G., Falcao, A.L., Brazil, R.P., 2000. Primeiro encontro de Lutzomyialongipalpis (Lutz & Neiva, 1912) na area urbana de Campo Grande, MS,Brasil. Rev. Saude Publica 34, 654–655.

liveira, A.G., Andrade Filho, J.D., Falcao, A.L., Brazil, R.P., 2003. Estudode flebotomıneos (Diptera, Psychodidae, Phlebotominae) na zona urbana dacidade de Campo Grande, Mato Grosso do Sul, Brasil, 1999–2000. Cad.Saude Publica 19, 933–944.

ebelo, J.M.M., 2001. Frequencia horaria e sazonalidade de Lutzomyialongipalpis (Diptera: Psychodidae: Phlebotominae) na Ilha de Sao Luis,Maranhao, Brasil. Cad. Saude Publica 17, 221–227.

esende, M.C., Camargo, M.C.V., Vieira, J.R.M., Nobi, R.C.A., Porto, N.M.N.,Oliveira, C.D.L., Pessanha, J.E., Cunha, M.C.M., Brandao, S.T., 2006. Sea-sonal variation of Lutzomyia longipalpis in Belo Horizonte, State of MinasGerais. Rev. Soc. Bras. Med. Trop. 39, 51–55.

herlock, I.A., Guitton, N., 1969. Observacoes sobre Calazar em Jacobina,Bahia. III. Alguns dados sobre o Phlebotomus longipalpis, o principal trans-

eledon, R., Murillo, J., Gutierrez, H., 1984. Observaciones sobre la ecologia deLutzomyia longipalpis (Lutz & Neiva, 1912) y possibilidades de existenciade leishmaniasis visceral em Costa Rica. Mem. Inst. Oswaldo Cruz. 79,455–459.