Services on Demand
Print version ISSN 0365-0596
On-line version ISSN 1806-4841
An. Bras. Dermatol. vol.77 no.6 Rio de Janeiro Nov./Dec. 2002
CLINICAL, LABORATORY AND THERAPEUTIC INVESTIGATION
Tegumentary leishmaniasis distribution by satellite remote sensing imagery, in Paraná State, Brazil*
Airton Pereira LimaI; Lorivaldo MinelliII; Ueslei TeodoroIII; Éder ComunelloIV
of Dermatology, Medicine Department - DMD/UEM
IIAssociate Professor of Dermatology. Health Science Center, "Universidade Estadual de Londrina"
IIIAssociate Professor of Parasitology at the Clinical Analysis Department - DAC/UEM
IVPostgraduate Student, Environmental Multi-Disciplinary Group of Studies - UEM
The epidemiology of tegumentary leishmaniasis (TL) is poorly known in the State
OBJECTIVES: To verify the geographical distribution of TL cases in four municipalities in the State of Paraná and correlate the notified TL cases with the presence of the remaining vegetation and water streams, using images by satellite monitoring.
METHODS: The distribution of 4,416 cases of TL in the State of Paraná, from 1993 to 1998, was done according to the notification records used by the State of Paraná Health Secretariat. The distribution of 231 cases of TL and the correlation between these cases and the remaining forest, as well as the extent to which man has influenced the environment in Cianorte, Japurá, Jussara and São Tomé municipalities was verified using satellite monitoring.
RESULTS: The geographical distribution showed a higher concentration of cases in the northern and western regions of Paraná. The satellite monitored images show that there is a close relationship between TL and modified native forest areas, gallery forest areas or the remainder of both.
CONCLUSION: It is possible that the areas with higher incidence of TL in Paraná are similar to the ones in Cianorte, Japurá, Jussara and São Tomé municipalities.
Key words: ecology; epidemiology; leishmaniasis, mucocutaneous.
Leishmanioses are diseases caused by protozoa of the genus Leishmania, Ross 1903, transmitted primitively from wild mammals (reservoirs) to Man (host) through the bite of phlebotomines (vectors). The disease is endemic in tropical areas of America, Africa and India, as well as in the subtropics of southwest Asia and the Mediterranean.1
Up to the mid 20th Century, approximately 40 thousand cases of Leishmaniasis were recorded in countless points of the Brazilian national territory.2 There was then a brief period of quiescence, but in the last two decades the number of cases has been increasing considerably, according to notifications from all of the states.3,4 In Brazil, from 1980 to 1988, 107,412 cases of tegumentary Leishmaniasis were notified, representing 11,935 new cases per year.3 There was a marked growth from 1989 to 1999, reaching 310,767 cases, or a mean of 28,252 cases per year.3,4 In the South Region, in the last 20 years, 6,277 cases were registered, representing 2% of the total occurrences in Brazil and, of these, 6,264 (99.8%) were in Paraná State.3,4
Until the decade of the 1940's, tegumentary Leishmaniasis in Brazil was intimately related to Man's penetration into forested areas, since deforestation to make way for planting, construction of highways and railroads, hydroelectric power stations and implantation of towns favored human contact with the reservoirs and vectors of Leishmania.5,6 In the Amazonian region, one can still observe an epidemic pattern of transmission based on the settlers'contact with the wild environment, such that the disease prevails in adult male individuals.
The persistence of tegumentary Leishmaniasis in an endemic form within areas of long-standing colonization is related to modification of the remaining forests.7-10 In these areas there has been an evident adaptation of phlebotomines and wild reservoirs of Leishmania, propitiating the formation of the cycle of this parasite in the peridomicile, both in rural areas and in the periphery of urban centers.11-16
In Paraná State, American tegumentary Leishmaniasis has been registered since the beginning of the last century, with cases reported up until 1958.2,17,18 The disease was then only notified officially in Paraná as of 1980 and has remained endemic in several municipal districts, despite the abusive deforestation that occurred within this State.19
The vegetation associated to water courses is an ecological factor that has been aiding studies into the distribution of Leishmaniasis and identification of areas of infection risk, through an analysis of the topography. Linthicum et al.20 used analysis of topography by orbital satellite monitoring for the delimitation of areas of occurrence of Rift valley fever in Kenya, Africa. While in Brazil, Miranda et al.,7,8used images obtained by orbital satellite monitoring, to determine an association of tegumentary Leishmaniasis with areas of bush vegetation and the presence of streams.
The occurrence of tegumentary Leishmaniasis has been notified in various municipal districts in Paraná State,10,19 however no relationship has been established with the level of anthropic activity nor other environmental variables within the areas covered by these municipal districts.
The objective of this work was to establish: i) a correlation between the notified cases of tegumentary Leishmaniasis, in the period from 1993 to 1998, in the municipal districts of Cianorte, Japurá, Jussara and San Tome, Paraná State, with the presence of remaining native vegetation and water courses in the places with a higher infection probability, using images obtained by orbital satellite monitoring; ii) the geographical distribution of the cases of tegumentary Leishmaniasis notified in Paraná State, in the period from 1993 to 1998, correlating this with the environmental and meteorological characteristics (remaining native vegetation, annual rainfall and temperature) in the various regions of Paraná.
MATERIAL AND METHODS
1. General description of Paraná State
Paraná State is located in the South Region of Brazil, between 22°30'58" and 26°43'00" latitude South and 48°05'37" and 54°37'08" longitude West.21
The climatic maps of 1994, elaborated by Iapar [Agronomic Institute of Paraná]22 mshow that there are three climatic types in the State, according to Köppen's classification: 1) Af, tropical superhumid climate, without a dry station, with a mean temperature in all months greater than 18°C (megathermic), mean precipitation in the driest month over 60mm and free from frosts; 2) Cfa, subtropical climate; mean temperature in the coldest month less than 18°C (mesothermic) and mean temperature in the hottest month above 22°C, with hot summers, infrequent frosts and a tendency for a concentration of rainfall in the summer months, however without a defined dry station; and 3) Cfb, temperate climate; mean temperature in the coldest month below 18°C (mesothermic), with cool summers, mean temperature in the hottest month below 22°C and without a defined dry station.
The primitive vegetation of Paraná was constituted by several types of forests, which at the beginning of the XX century began to be destroyed for the extraction of wood, expansion of coffee plantations and production of charcoal. In less than half a century, the primitive forest covering had practically disappeared. In 1980, there only remained 5% and, in 1990, a mere 2.6% of the original vegetation, mostly in parks and areas of protection and conservation of the remaining forests.23
2. General description of the Municipal districts of Cianorte, Japurá, Jussara and San Tome
The municipal districts of Cianorte, Jussara, Japurá and San Tome are located in the mesoregion of northwest Paraná, between 52°20' and 52°50' longitude West and 23°20' and 23°60' latitude South (Figure 1). These municipal districts belong to the geomorphological unit of the central plateau of the Paraná Basin,24 which is part of the third Paraná plateau25 or sandstone-basaltic plateau. The relief is of lowered plateaus, with flat and little dissected tops, with convex slopes, between 250 and 600m of altitude. The local base of which is constituted by the thalweg of the mid river Ivaí that forms one of the main hydrographic basins of northwest Paraná. The original covering comprised semidecidual seasonal forest.26The climate type is tropical subhot, superhumid with subdry station.27 NIn the subdry winter station the mean temperatures are under 18°C. The mean rainfall is 1,700mm/year.
In the municipal districts of Cianorte, Japurá, Jussara and San Tome the original forest was extensively altered or eliminated, to provide land for cultivation and reforestation. There still persists remnants of dense ciliary and intricate forest, with many woody lianas and bamboos along the course of the River Ivaí, besides small strips of secondary forest of variable breadth. There are also some secondary forests, that uninterruptedly follow the water courses constituting the Ivaí hydrographic basin. These primary or secondary forest formations favor the occurrence of phlebotomines and thus are one of the important environmental factors in the epidemiology of tegumentary Leishmaniasis within the region.28
Local fauna of native mammals and possible reservoirs of Leishmania is sparse with little variety. The areas reforested with exotic species and internally thinned forests attract few animal species. The ciliary forests can shelter rodents, skunks, deer and rare felines. These formations present, however, a numerous and varied fauna of birds.28
The main economic activity in the municipal districts of Cianorte, Japurá, Jussara and San Tome is agriculture, mainly for cultivation of soy bean, sugarcane, corn and cassava with a tendency to temporary plantations.
The distribution of the cases of tegumentary Leishmaniasis notified in the various municipal districts of Paraná State, information regarding age group, sex, occupation, residential zone (urban/rural) and clinical form of the disease was obtained from the Report of Patients with Leishmaniasis Registered in the State of Paraná from 1993 to 1996. Part of the data for 1997 were obtained from this report and the remainder from Sinan [System of Information of Offences of Notification], since irregularities were detected in the information from these registration sources. Data for 1998 were obtained entirely from Sinan. The aforementioned report and data from Sinan were supplied by the General Secretary of Health of Paraná State. Besides these, notification records and registration books from the Regional Health Services of Cianorte, Londrina, Maringá and Umuarama, of the General Secretary of Health of Paraná State, were used for rectification of information regarding the notifications. The notifications of tegumentary Leishmaniasis in Paraná State from 1993 to 1998 were analyzed on a one-to-one basis, thereby eliminating a great number of cases with double registration and correcting their origin.
The geographical distribution of the cases of tegumentary Leishmaniasis in the various areas of Paraná State was made according to the patients' municipal districts of origin and notification. Furthermore, the correlation was established between the distribution of Leishmaniasis cases and temperatures, annual precipitation and especially location of forests.
In the Regional Health Service of Cianorte, files were used with complementary information regarding 231 cases of tegumentary Leishmaniasis from a total of 382 cases notified in the municipal districts of Cianorte, Japurá, Jussara and San Tome, from 1993 to 1998. These cases were selected according to the locations with a probability of occurrence of infections, and these places were defined with the aid of maps showing the hydrography, road networks, rural lots of each of the municipal districts, including the streets and blocks in the urban zone of Cianorte.
The cases identified were transferred to the System of Geographical Information -SGI/Sitim 2.5,29 together with other aspects of relevance for the study in question, such as hydrography and the urban and municipal limits. The classification of the use and occupation of the soil from the orbital satellite monitoring, regarding orbit-point 223-076, with date of passage on October 16, 1996 was also done using the SGI / Sitim.
The image, produced by the TM multiple sensor of the Landsat satellite, was acquired in digital format, with correction level PL-4 (Processing Level-4), necessitating georeferencing to determine properties of scale and projection.
The preliminary studies used planimetric maps of Umuarama (SF-22-Y-C) and Londrina (SF-22-Y-D) in the scale 1:250,000, produced by IBGE [Brazilian Institute of Geography and Statistics] as the cartographic basis. After geometric correction, the image was classified using the Maxver algorithm.30
At this point, the SGI was used to cross-reference information regarding the location of the cases with the various related aspects (classifications for the use and occupation of the soil and hydrography), thereby generating a preliminary map of the study area, starting from which it was possible to define some sub-areas for investigation, with a view to delimiting those environments with a greater number of Leishmaniasis cases, which could therefore be appropriate habitats for mammals (reservoirs) and vectors (phlebotomines) of Leishmania. In this manner, seven quadrants of 64km2 (8 x 8km) each were selected and denominated A to G. The area of each quadrant was defined in such a way as to facilitate the observation of the most probable places of occurrence of infections (Figure 2).
Having defined the quadrants A to G, quadrants A, E, F and G were selected, of which some areas were visited in loco to confirm the presence of vegetation and determine the necessity for the elaboration of new classes for the use and occupation of the soil or correction of the preexistent classifications.
In the search for greater precision the quadrants were rectified, using as a basis cartographic sheets in the scale 1:100,000 from the Department of Geographical Services of the Army (SF-22-Y-C-III and VI) and 1:50,000 of the IBGE (SF-22-Y-D-I and IV). In this manner a new classification of the image was made, assisted by the verification in loco of localities within the area under study.
At the end of the above mentioned steps, the data were transferred to the Spring 3.3 software, which generated the final maps of the quadrants, presenting the demarcation of the cases in the places of greater probability for occurrence of infections and the geographical relationship with elements of the landscape: such as streams and vegetation.
To ascertain the anthropic activity level, the patterns of soil usage and influence of these factors in the occurrence of the tegumentary Leishmaniasis in Paraná State, the region was georeferenced with classification of fractions of orbital images from the TM Landsat sensor of the north areas (Scene 221-076 taken on 12/24/97) and west (Scene 223-078, 06/10/96), highlighting the municipal districts with greater occurrence of cases.
As shown in table 1, there was a greater occurrence of Leishmaniasis in Paraná State in 1994, during the period from 1993 to 1998. It was observed that of the 4,416 patients with tegumentary Leishmaniasis 2,808 (63.6%) were male. For both sexes the age group most affected was 21 to 50 years old, accounting for 2,306 (52.2%) cases. The age group of patients' between 0 and 10 years was the least involved.
Figure 3 shows that the distribution of tegumentary Leishmaniasis, from 1993 to 1998, occurred especially in the north and west areas of Paraná State.
Approximately 94% of the tegumentary Leishmaniasis cases in the State occurred in those areas with a Cfa type climate and more than 96% in areas with annual medium temperature above 18°C. There was a prevalence of Leishmaniasis in areas in which the annual means of the minimum and maximum temperatures were over 14°C and above 25°C, respectively, which includes the areas in the north and west of Paraná State (Figure 3).
The largest number of notifications of the disease (above 90% of the cases) originated in those areas in which the annual average of relative humidity of the air oscillated between 70 and 75%, and practically all the registered cases occurred in areas with mean annual precipitation from 1,300 to 2,000mm.
The mentioned cases of tegumentary Leishmaniasis were distributed in 276 municipal districts in the State of Paraná, as follows: in 173 (62.8%) one to nine cases were notified; in 62 (22.5%) from 10 to 24; in 23 (8.3%) from 25 to 49; in 11 (4%) from 50 to 99; and in seven (2.5%) 100 or more.
In the quadrants of A to G (Figure 2), including the municipal districts of Cianorte, Japurá, Jussara and San Tome, 60, 22, 82 and 17 cases of tegumentary Leishmaniasis were recorded, respectively.
In the urban area of Cianorte (Figure 4) 37 cases were registered in the places with highest probability of occurrence of infection by Leishmania, as well as another five cases outside the limits of the urban area.
In Figures 5 and 6 it can be seen that there were 59 and 27 cases, respectively, with three demarcated within the area of intersection of these figures and one in the Municipal district of Cianorte, totaling 82 cases in the Municipal district of Jussara and demarcated in the places or areas with the highest probability of infection.
In the fractions of orbital images from the TM Landsat sensor it was observed that in the municipal districts in which there were numerous notifications of tegumentary Leishmaniasis, from 1993 to 1998, in the north area of Paraná, there had occurred an extreme devastation of the environment, with only small areas or traces of native forests remaining. The same is also true for the municipal districts in the west of Paraná.
The greater number of cases of Leishmaniasis involving male adults is probably related to rural work close to forests and to leisure activities (mainly fishing) along the margins of rivers and streams with ciliary forests that, although altered, still maintain the enzootic cycle of Leishmania. Of 147 individuals with the disease and resident in Maringá, 44 (39 men) referred to the margins of the river Ivaí, where they fish, as being the most probable place in which they acquired the infection. The results of the present investigation confirm previous studies that demonstrated the males sex bias in tegumentary Leishmaniasis,31,32 including those focussing Paraná State.10,33
The cases relative to women and male children, although in a smaller proportion (40.1%), are expressive and most probably due to rural activities undertaken by female labor, as well as the common habit of building houses and shelters for domestic animals alongside modified native forests, where the atmosphere is fresher and more agreeable.10 Usually the houses are built close to the banks of rivers and streams with ciliary forests, in order to facilitate the provision of water for human consumption and domestic animals.10 The infection of women and children is a strong indication of domiciliary and/or peridomiciliary transmission of Leishmania, which has been reinforced by the verification of high densities of phlebotomines in the home and especially in shelters for domestic animals in the peridomicile of endemic areas in the states of Pernambuco,34 Espírito Santo,14 São Paulo,35,36 and Paraná.28,37
Leishmaniasis was notified in 276 municipal districts of Paraná. However, it is known that there is a tendency to concentrate notification of the disease in the municipal districts that serve as head offices for the regional health services of the General Secretary of Health of the State of Paraná, since treatment is provided, as a rule, in the dermatology services of these municipal districts. Rectification of information regarding notifications from the municipal districts of Cianorte, Londrina, Maringá and Umuarama enabled the conclusion that several cases of people resident in other municipal districts were erroneously notified as being resident in these municipal districts. And even among the patients resident in the above-mentioned municipal districts many were not autochthonous. In the case of Curitiba, it was found that, in spite of the high number of notified cases, there were no reports of autochthonous cases. These facts demonstrate the existence of flaws in the notification of the disease in Paraná.
The majority of the municipal districts with occurrence of tegumentary Leishmaniasis are in the area with a Cfa climate, according to Köeppen's classification (subtropical climate), with bands of annual mean temperature predominantly over 18°C, while the municipal districts with the highest number of cases (above 100 in the period considered) are located in the bands of annual mean isotherms between 20 and 22°C.
Approximately 94% of the cases of tegumentary Leishmaniasis in Paraná State occurred in areas with a Cfa climate, and more than 96% in areas with annual mean temperature above 18°C. There was a prevalence of Leishmaniasis in areas in which the annual mean minimum temperature is over 14°C, and the annual mean maximum temperature above 25°C, which includes areas in the north and west of Paraná State (Figure 1). In São Paulo State, from 1986 to 1995, Camargo-Neves9 observed that 76% of the municipal districts notifying Leishmaniasis were in the band of annual mean isotherms from 19 to 23°C, with the highest incidence of coefficients in the temperature band between 21 and 23°C. In Corte de Pedra, Bahia, an area with occurrence of Leishmaniasis, the temperature varied from 16 to 37°C, with an annual mean of 22°C,38 corroborating the data of this work.
In the areas with the highest number of notifications of tegumentary Leishmaniasis it was observed that the relative humidity of the air (annual mean) was between 70 and 75%. It was also noted that almost all the cases occurred in areas with a mean annual precipitation that oscillated from 1,300 to 1,900mm. The municipal districts with the highest number of registrations of the disease were located in areas with rainfall from 1,500 to 1,800mm. In the endemic area of Corte de Pedra, Bahia,38 an annual average of 1,300mm of rainfall and mean humidity of 78% was observed. Camargo-Neves,9 found a higher coefficient of incidence of tegumentary Leishmaniasis in areas of São Paulo State with annual rainfall greater than 1,500mm, although the majority of municipal districts with notification of the disease were located in the band with 1,300 to 1,500mm of rainfall.
Figure 2 shows the locations in quadrants A to G of the patients' homes in the municipal districts of Japurá, Cianorte and San Tomé. It can be seen that the areas with the highest probability of infection coincide with proximity to water courses with shrub ciliary forests or remnants of primary forests.
The cases of Leishmaniasis notified in the urban area of Cianorte (Figure 4) revealed the home and peridomicile be the places with the greatest probability of infection, since the houses are generally located close to or alongside the margins of modified native forests. The largest concentration of cases occurred where the forest presents the greatest degree of alteration, within the area denominated the Green Belt of Cianorte.
Fazenda Jussara, in the Municipal district of Jussara, was indicated as the most probable place of infection among the 37 cases marked in figure 5. Of these, 11 occurred in the area with the greatest risk of infection known as the horto florestal [forest reserve], constituted by a nucleus of houses (colony) beside the Encontro stream; plus two cases in the distillery and two in the main gate of the farm. The 22 remaining cases in Fazenda Jussara certainly occurred within its limits, although it was not possible to determine the probable site of infection more specifically. The other cases (22) shown in Figure 5 refer to the location of domiciles close to water courses with remnants or traces of forests or beside the larger forests of Fazenda Jussara.
The 21 cases contained in Figure 6 refer to a possible site of infection called Olaria Andirá. Most of the infections very probably occurred in the home or peridomicile.
It should be underscored that in Fazenda Jussara and Olaria Andirá, where there was a great concentration of cases, there are extensive areas of forest that, although modified, still preserve many of the characteristics of the native forest that existed in the region.
In São Paulo State, using images obtained by orbital satellite monitoring, Miranda et al.7,8 showed the presence of shrub vegetation close to the places in which people notified with Leishmaniasis lived and/or worked. Also in São Paulo State Camargo-Neves0 demonstrated that the natural vegetation types of capoeira (tall, dense grasslands), residual forest and preserved forest occurred in the areas in which they verified the highest coefficients of incidence of tegumentary leishmaniasis.
The images from orbital satellite monitoring show that regarding tegumentary Leishmaniasis in the municipal districts of Cianorte, Japurá, Jussara and San Tome, there is a very close relationship between areas of modified native forest, small ciliary forests or remnants of which and the home and/or peridomicile.
Most of the cases of tegumentary Leishmaniasis in Paraná State were notified in municipal districts of the north and west areas, coinciding with the areas in which there was intense destruction of the native vegetation. It is possible that the environments in which infection by Leishmania is occurring in the above mentioned areas resemble those observed in the municipal districts of Cianorte, Japurá, Jussara and San Tome.
1. Tegumentary Leishmaniasis in Paraná State has an extensive and irregular geographical distribution, with concentration of cases in municipal districts of the north and west regions, coinciding with areas marked by a high degree of destruction of the native vegetation, due to agricultural exploration by monoculture, especially corn, soy bean, sugarcane, and also pastures; in those areas the annual mean temperature is above 18°C, relative humidity of the air varies between 70 and 75%, and the annual mean rainfall varies from 1,300 to 1,900mm.
2. Images from orbital satellite monitoring show that in the municipal districts of Cianorte, Japurá, Jussara and San Tome tegumentary Leishmaniasis has a very close relationship with areas of modified native forest, small ciliary forests or remnants of these.
1. Modabber F. Leishmaniasis. In: UNDP. World Bank. WHO. Special programme for tesearch and training in tropical diseases (TDR). Tropical Desease Research: progress 1991-92, Geneva: World Health Organization 1993;77-87. [ Links ]
2. Pessôa SB, Barreto MP. Leishmaniose tegumentar americana. Rio de Janeiro: Ministério da Educação e Saúde. Imprensa Nacional, 1948. [ Links ]
3. Ministério da Saúde. Fundação Nacional de Saúde. Série histórica de casos de agravos e doenças infecciosas e parasitárias-Brasil-1980 a 1996. Informe Epidemiológico do SUS 1997, anoVI(1):59-60. [ Links ]
4. Ministério da Saúde (Fundação Nacional de Saúde). Manual de controle da leishmaniose tegumentar americana. Brasília, 2000. 62p. [ Links ]
5. Forattini OP. Entomologia médica. São Paulo: E. Blücher/EDUSP, 1973:4v.658p. [ Links ]
6. Souza AM, Geller M. Abordagem epidemiológica, clínica e laboratorial da leishmaniose tegumentar americana. Folha Médica 1994;108(3):53-7. [ Links ]
7. Miranda C, Massa JL, Marques CCA. Análise da ocorrência de leishmaniose tegumentar americana através de imagem obtida por sensoriamento remoto orbital em localidade urbana da região Sudeste do Brasil. Rev Saúde Públ 1996;30(5):433-7. [ Links ]
8. Miranda C, Massa JL, Marques CCA. Sensoriamento remoto orbital como recurso para análise da ocorrência da leishmaniose tegumentar americana em localidade urbana da região Sudeste do Brasil. Rev Saúde Públ 1998;32(5):455-63. [ Links ]
9. Camargo-Neves, VLFC. Características da transmissão da leishmaniose tegumentar americana no Estado de São Paulo, Brasil. Dissertação. São Paulo: USP, 1999. [ Links ]
10. Roberto ACBS, Lima AP, Peixoto PR, et al. Avaliação da terapia com antimoniato de N-metil glucamina e de notificação de leishmaniose tegumentar. An bras Dermatol 1997;72(2):129-3. [ Links ]
11. Barros GC, Sessa PA, Mattos EA, Carias VRD, Mayrink W, Alencar JTA, Falqueto A, Jesus AC. Foco de leishmaniose tegumentar americana nos municípios de Viana e Cariacica, Estado do Espírito Santo, Brasil. Rev Saúde Públ 1985;19:146-53. [ Links ]
12. Lima LCR, Marzochi MCA, Sabroza PC. Flebotomíneos em área de ocorrência de leishmaniose tegumentar no bairro de Campo Grande, Rio de Janeiro, Brasil. Rev bras Malar 1981;33:64-74. [ Links ]
13. Lima LCR, Marzochi MCA, Sobroza PC, Souza MA. Observações sobre a leishmaniose tegumentar cinco anos após profilaxia. Rev Saúde públ 1988;22(1):73-7. [ Links ]
14. Mattos EA. Bionomia dos flebotomíneos de Perobas, município de Viana (ES), área endêmica de leishmaniose tegumentar americana. Dissertação. Belo Horizonte: Universidade Federal de Minas Gerais, 1981. [ Links ]
15. Souza MA, Sabroza PCT, Marzochi MCA, Coutinho SG, Souza WJS. Leishmaniose visceral no Rio de Janeiro. 1. Flebotomíneos da área de procedência de caso humano autóctone. Mem Inst Oswaldo Cruz 1981;76(2):161-68. [ Links ]
16. Teodoro U, Kühl JB, Thomaz-Soccol V, et al. Environmental sanitation and peridomiciliar organization as auxiliary practices for the control of phlebotomines in Paraná State, Southern Brazil. Brazilian Archives of Biology and Tecnology 1999;42(3):307-14. [ Links ]
17. Lima EC, Luz E, Souza LA. Leishmaniose tegumentar americana no município de Foz do Iguaçu. Rev. Méd. Paraná 1958;27(2):53-8. [ Links ]
18. Silveira TGV, Teodoro U, Arraes SMAA, et al. An autochthonous case of cutaneous Leishmaniasis caused by Leishmania (Leishmania) amazonensis Laison & Shaw, 1972 from the North Paraná State, Brazil. Mem Inst Oswaldo Cruz 1990;85(4):475-6. [ Links ]
19. Teodoro U, La Salvia Fº V, Lima EM, Mizuta NM, Verzignassi TG, Ferreira MEMC. Leishmaniose tegumentar americana: flebotomíneos de área de transmissão no Norte do Paraná - Brasil. Rev Saúde Públ 1991b;25(2):129-33. [ Links ]
20. Linthicum KJ, Bailey CL, Davies FG, Tucker CJ. Detection of rift valley fever viral activity in Kenya by satellite remote sensing imagery. Science 1987;235:1656-9. [ Links ]
21. Camargo JB. Geografia física, humana e econômica do Paraná. 2th ed. Paranavaí: Clichetec, 1998. [ Links ]
22. Instituto Agronômico do Paraná. Cartas climáticas do Estado do Paraná - 1994. Londrina: IAPAR, 1994. [ Links ]
23. Cigolini A, Mello L, Lopes N. Paraná - quadro natural, transformações territoriais e economia. Curitiba: Renascer, 1998:128p. [ Links ]
24. Hermann MLP & Rosa RO. Relevo. In: Geografia do Brasil - Região Sul. Rio de Janeiro: IBGE, 1990. [ Links ]
25. Maack R. Geografia física do Estado do Paraná. 2 ed. Rio de Janeiro/J. Olímpio/Curitiba: Secretaria da Cultura e do Esporte, 1981;450p. [ Links ]
26. Leite PF & Klein RM. Vegetação. In: Geografia do Brasil - Região Sul. Rio de Janeiro: IBGE, 1990. [ Links ]
27. Nimer E. Clima. In: Geografia do Brasil - Região Sul. Rio de Janeiro: IBGE, 1990. [ Links ]
28. Teodoro U. Características ecológicas de flebotomíneos (Diptera, Psychodidae) em habitats antrópicos, município de Jussara, Paraná, Brasil. Tese. Curitiba: Universidade Federal do Paraná, 1995. [ Links ]
29. Engespaço. Sistema de informações geográficas SGI/INPE: Manual do usuário versão 2.5. São José dos Campos, 1990. [ Links ]
30. Jensen JR. Introductory Digital Image Processing: a Remote Sensing Perspective. New Jersey: Prentice-Hall, 1986p.379. [ Links ]
31. Cavalcante JEA, Oliveira MF, Rios AA, Freitas CEJ. Prevalência da leishmaniose tegumentar americana no Estado do Ceará no ano de 1991 e suas variações nos últimos dez anos. Rev Bras Anál Clín 1992;24(4):121-3. [ Links ]
32. Gomes AC. Perfil epidemiológico da leishmaniose tegumentar no Brasil. An bras Dermatol 1992;67 (2):55-60. [ Links ]
33. Silveira TGV, Teodoro U, Lonardoni MVC, et al. Aspectos epidemiológicos da leishmaniose tegumentar em área endêmica do Estado do Paraná, Brasil. Cad Saúde Pública 1996;12(2):37-45. [ Links ]
34. Brandão-Filho SP, Carvalho FG, Brito MEF, Almeida FA, Nascimento LA American cutaneous Leishmaniasis in Pernambuco, Brazil: eco-epidemiological aspects in "Zona da Mata" region. In: research and control of Leishmaniasis in Brazil. Proceedings of National Workshop. Recife, Fiocruz, 1993:51-7. [ Links ]
35. Forattini OP, Rabello EX, Serra OP, Cotrim MD, Galati EAB, Barata JMS. Observações sobre a transmissão da leishmaniose tegumentar no Estado de São Paulo, Brasil. Rev Saúde públ 1976;10:31-43. [ Links ]
36. Gomes AC, Santos JLF, Galati EAB. Ecological aspectos of american cutaneos Leishmaniasis. 4. Observations on the endophilic behavior of the sandfly and the vectorial role of psychodopygus intermedius in the Ribeira Valley region of the S. Paulo State, Brasil. Rev Saúde públ 1986;20(4):280-7. [ Links ]
37. Teodoro U, La Salvia Fº V, Lima EM, et al. Observações sobre o comportamento de flebotomíneos em ecótopos florestais e extraflorestais, em área endêmica de leishmaniose tegumentar americana, no norte do Estado do Paraná, sul do Brasil. Rev Saúde Públ 1993b;27(4):242-9. [ Links ]
38. França F, Lago EL, Tada S, et al. An outbreak of human Leishmania (Viannia) brasiliensis infection. Men Inst Oswaldo Cruz 1991;86(2):169-74. [ Links ]
Airton Pereira Lima
Rua Humaitá, 456
Cianorte PR 87200-000
Tel: (44) 629-1915
Received in October,
10th of 2001.
Approved by the Consultive Council and accepted for publication in May, 22nd of 2002.
* Work conducted at the Department of Medicine and the Department of Clinical Analysis of the "Universidade Estadual de Maringá (DMD/UEM; DAC/UEM)".