Canine visceral leishmaniasis: perception, prevalence, and spatial distribution in municipality of Nossa Senhora do Livramento, Mato Grosso, Brazil

Leishmaniose visceral canina: percepção, prevalência e distribuição espacial em Nossa Senhora do Livramento, Mato Grosso, Brazil

Matheus Roberto Carvalho Álvaro Felipe de Lima Ruy Dias Arleana do Bom Parto Ferreira de Almeida Mário Ribeiro Alves Adilson Santos Paes Valéria Régia Franco Sousa About the authors

Abstract

The midwest region of Brazil has witnessed an increase in the number of cases of human (HVL) and canine visceral leishmaniasis (CVL). The aim of the present study was to evaluate the population’s perception of these diseases, factors associated with CVL, its spatial distribution, and the prevalence of anti-Leishmania spp. in 385 dogs, determined using a commercially available immunochromatographic rapid test and confirmed using enzyme-linked immunosorbent assay (ELISA). Of the 385 samples, 54 were positive for CVL and confirmed by ELISA, corresponding to a prevalence of 14%. Knowledge of signs of CVL by tutors (p = 0.038); previous occurrence of CVL in the vicinity (p = 0.022); symptomatic dog(s) (p = 0.014), splenomegaly (p = 0.055), and ear ulcer(s) (p = 0.059) were significantly associated with CVL. The results revealed a significant prevalence of CVL spatially distributed in rural and urban contexts. The association between environmentally related variables and perception and the occurrence of CVL underscores the importance of implementing control and prevention strategies primarily focused on environmental management and health education activities.

Keywords:
Epidemiology; associated factors; Leishmania infantum

Resumo

No Brasil, a região Centro-Oeste tem apresentado aumento no número de casos de leishmaniose visceral humana (LVH) e canina (LVC). Com isso, o objetivo deste estudo foi avaliar a percepção da população em relação à doença, aos fatores associados a LVC, à distribuição espacial e à prevalência de anticorpos anti-Leishmania spp. em 385 cães, a partir do teste rápido imunocromatográfico e ensaio imunoenzimático (ELISA). Das 385 amostras, 54 foram reagentes para LVC e confirmadas no ELISA, correspondendo a prevalência de 14%. O conhecimento dos sinais da LVC pelos tutores (p = 0,038), a ocorrência prévia da LVC na vizinhança (p = 0,022), o cão sintomático (p = 0,014), esplenomegalia (p = 0,055) e apresentar úlcera em ponta de orelha (p = 0,059) foram significativamente associados à LVC. Os resultados demonstram expressiva prevalência de LVC, distribuídas espacialmente no contexto rural e urbano, e a associação de variáveis relacionadas ao ambiente e à percepção com a ocorrência da LVC ressaltam a importância da implementação de estratégias de controle e prevenção, focadas principalmente no manejo ambiental e em atividades de educação em saúde.

Palavras-chave:
Epidemiologia; fatores associados; Leishmania infantum

Introduction

Visceral leishmaniasis (VL) is a potentially fatal anthropozoonosis, with an estimated incidence of 50,000 to 90,000 new human cases worldwide each year (WHO, 2019World Health Organization – WHO. Epidemiological situation [online]. Geneva: WHO; 2019 [cited 2019 Mar 15]. Available from: http://www.who.int/leishmaniasis/burden
http://www.who.int/leishmaniasis/burden...
). The canine form of VL (CVL) is recognized by the World Organisation for Animal Health (OIE) as an important disease due to its clinical characteristics, transmissibility and zoonotic potential, and the number of regions becoming Leishmania endemic has grown significantly in recent years (OIE, 2020Word Organisation for Animal Health – OIE. Leishmaniosis [online]. Paris: OIE; 2020 [cited 2020 Feb 20]. Available from: https://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/3.01.11_LEISHMANIOSIS.pdf
https://www.oie.int/fileadmin/Home/eng/H...
).

In the Americas, Brazil accounts for approximately 96% of cases of human VL (HVL), which continues to experience geographic expansion, mainly in the Northeast, Southeast, and Midwest (OPAS, 2018aOrganização Pan-Americana da Saúde – OPAS. Leishmanioses: informe epidemiológico das Américas. 6. ed. Brasilia: OMS; 2018a.) regions. Moreoever, most cases of CVL are also reported in Brazil (WHO, 2019World Health Organization – WHO. Epidemiological situation [online]. Geneva: WHO; 2019 [cited 2019 Mar 15]. Available from: http://www.who.int/leishmaniasis/burden
http://www.who.int/leishmaniasis/burden...
), with Leishmania infantum (Kinetoplastida, Trypanosomatidae) being the etiological agent (Ready, 2014Ready PD. Epidemiology of visceral leishmaniasis. Clin Epidemiol 2014; 6: 147-154. http://dx.doi.org/10.2147/CLEP.S44267.
http://dx.doi.org/10.2147/CLEP.S44267...
), which is transmitted to vertebrate hosts mainly by two species of Phlebotominae, Lutzomyia longipalpis and Lutzomyia cruzi (Missawa & Lima, 2006Missawa NA, Lima GBM. Distribuição espacial de Lutzomyia longipalpis (Lutz & Neiva, 1912) e Lutzomyia cruzi (Mangabeira, 1938) no estado de Mato Grosso. Rev Soc Bras Med Trop 2006; 39(4): 337-340. http://dx.doi.org/10.1590/S0037-86822006000400004. PMid:17119747.
http://dx.doi.org/10.1590/S0037-86822006...
).

Leishmania infantum transmission control measures recommended by the Brazilian Ministry of Health are focused on the diagnosis and treatment of human cases, reduction of the phlebotomine population, and measures to combat the reservoir, including diagnosis and euthanasia of seroreactive dogs (Brasil, 2014Brasil. Ministério da Saúde. Manual de vigilância e controle da Leishmaniose Visceral. Brasília: Ministério da Saúde; 2014. 122 p.). According to Alemu et al. (2013)Alemu A, Alemu A, Esmael N, Dessie Y, Hamdu K, Mathewos B, et al. Knowledge, attitude and practices related to visceral leishmaniasis among residents in Addis Zemen town, South Gondar, Northwest Ethiopia. BMC Public Health 2013; 13(1): 382. http://dx.doi.org/10.1186/1471-2458-13-382. PMid:23617595.
http://dx.doi.org/10.1186/1471-2458-13-3...
, the effectiveness of VL control and prevention programmes depend on active participation of the population because there is a relationship between environmental variables and vector density. Therefore, it is important to understand the population’s level of information about this disease, as well as its attitudes and practices regarding prevention. In addition, the use of spatial analysis tools makes it possible to understand the disease expansion process, including spatial patterns of distribution and identification of risk areas (Silva et al., 2017Silva TAM, Coura-Vital W, Barbosa DS, Oiko CSF, Morais MHF, Tourinho BD, et al. Spatial and temporal trends of visceral leishmaniasis by mesoregion in a southeastern state of Brazil, 2002-2013. PLoS Negl Trop Dis 2017; 11(10): e0005950. http://dx.doi.org/10.1371/journal.pntd.0005950. PMid:28985218.
http://dx.doi.org/10.1371/journal.pntd.0...
).

Widely accepted in the scientific community, the occurrence of HVL is associated with poor socioeconomic, environmental, and housing conditions (Belo et al., 2013Belo VS, Werneck GL, Barbosa DS, Simões TC, Nascimento BW, da Silva ES, et al. Factors associated with visceral leishmaniasis in the Americas: a systematic review and meta-analysis. PLoS Negl Trop Dis 2013; 7(4): e2182. http://dx.doi.org/10.1371/journal.pntd.0002182. PMid:23638203.
http://dx.doi.org/10.1371/journal.pntd.0...
; Bruhn et al., 2018Bruhn FRP, Morais MHF, Bruhn NCP, Cardoso DL, Ferreira F, Rocha CMBM. Human visceral leishmaniasis: factors associated with deaths in Belo Horizonte, Minas Gerais state, Brazil from 2006 to 2013. Epidemiol Infect 2018; 146(5): 565-570. http://dx.doi.org/10.1017/S0950268818000109. PMid:29463341.
http://dx.doi.org/10.1017/S0950268818000...
; Diniz et al., 2018Diniz LFB, Souza CDF, Carmo RF. Epidemiology of human visceral leishmaniasis in the urban centers of the lower-middle São Francisco Valley, Brazilian semiarid region. Rev Soc Bras Med Trop 2018; 51(4): 461-466. http://dx.doi.org/10.1590/0037-8682-0074-2018. PMid:30133628.
http://dx.doi.org/10.1590/0037-8682-0074...
). In this sense, studies assessing the prevalence of CVL seek to highlight factors associated with canine infection, especially those intrinsic to dogs, as well as environmental aspects (Coura-Vital et al., 2011Coura-Vital W, Marques MJ, Veloso VM, Roatt BM, Aguiar-Soares RDO, Reis LES, et al. Prevalence and factors associated with Leishmania infantum infection of dogs from an urban area of brazil as identified by molecular methods. PLoS Negl Trop Dis 2011; 5(8): e1291. http://dx.doi.org/10.1371/journal.pntd.0001291. PMid:21858243.
http://dx.doi.org/10.1371/journal.pntd.0...
; Dias et al., 2017Dias AFLR, Almeida ABPF, Cruz FACS, Silva RR, Rodrigues JY, Otsubo AAF, et al. Seroprevalence and spatial analysis of canine visceral Leishmaniasis in the Pantanal Region, Mato Grosso State, Brazil. J Zoonotic Dis Public Health 2017; 1: 3.; Leal et al., 2018Leal GGA, Carneiro M, Pinheiro ADC, Marques LA, Ker HG, Reis AB, et al. Risk profile for Leishmania infection in dogs coming from an area of visceral leishmaniasis reemergence. Prev Vet Med 2018; 150: 1-7. http://dx.doi.org/10.1016/j.prevetmed.2017.11.022. PMid:29406075.
http://dx.doi.org/10.1016/j.prevetmed.20...
) and the association between the population’s level of knowledge and the occurrence of CVL (Margonari et al., 2012Margonari C, Menezes JA, Rocha MN, Maia KN, Oliveira ME, Fonseca AL, et al. Public knowledge about and detection of canine visceral leishmaniasis in urban Divinópolis, Brazil. J Trop Med 2012; 2012: 429586. http://dx.doi.org/10.1155/2012/429586. PMid:22991521.
http://dx.doi.org/10.1155/2012/429586...
; Menezes et al., 2016Menezes JA, Luz TCB, Sousa FF, Verne RN, Lima FP, Margonari C. Peridomiciliary risk factors and knowledge concerning visceral leishmaniasis in the population of Formiga, Minas Gerais, Brazil. Rev Bras Epidemiol 2016; 19(2): 362-374. http://dx.doi.org/10.1590/1980-5497201600020013. PMid:27532759.
http://dx.doi.org/10.1590/1980-549720160...
).

Lutzomyia longipalpis vector has been reported in Mato Grosso, in the city of Nossa Senhora do Livramento, Brazil (Missawa & Lima, 2006Missawa NA, Lima GBM. Distribuição espacial de Lutzomyia longipalpis (Lutz & Neiva, 1912) e Lutzomyia cruzi (Mangabeira, 1938) no estado de Mato Grosso. Rev Soc Bras Med Trop 2006; 39(4): 337-340. http://dx.doi.org/10.1590/S0037-86822006000400004. PMid:17119747.
http://dx.doi.org/10.1590/S0037-86822006...
) and, in the triennium of 2015, 2016 and 2017, the mean incidence of HVL was 8.26% (OPAS, 2018bOrganização Pan-Americana da Saúde – OPAS. Relatório de índice composto de leishmaniose visceral por 2º nível, análise: País: triênio. Brasilia: OMS; 2018b.). The municipality has a medium index of human development (IBGE, 2018Instituto Brasileiro de Geografia e Estatística – IBGE. Panorama da cidade de Nossa Senhora do Livramento em 2018 [online]. Brasília: IBGE; 2018 [cited 2019 Mar 15]. Available from: https://cidades.ibge.gov.br/brasil/mt/nossa-senhora-do-livramento/panorama
https://cidades.ibge.gov.br/brasil/mt/no...
), and human occupation is associated with agricultural activities and mineral extraction. Thus, the present study aimed to investigate the population’s perception of VL, the prevalence of anti-Leishmania species (spp.) antibodies in dogs, associated factors, and the spatial distribution of canine disease in Nossa Senhora do Livramento.

Material and Methods

Study area

The present cross-sectional study was conducted between July and August 2018 in the municipality of Nossa Senhora do Livramento, Mato Grosso (15°46’30” S and 56° 20’44” W [232 m in altitude]). It is 32 km from the capital, Cuiabá, and belongs to the physiographic zone of the Pantanal, located in the central-south mesoregion of Mato Grosso and Cuiabá microregion, with a warm and humid tropical climate, and an average temperature of 24 °C (IBGE, 2018Instituto Brasileiro de Geografia e Estatística – IBGE. Panorama da cidade de Nossa Senhora do Livramento em 2018 [online]. Brasília: IBGE; 2018 [cited 2019 Mar 15]. Available from: https://cidades.ibge.gov.br/brasil/mt/nossa-senhora-do-livramento/panorama
https://cidades.ibge.gov.br/brasil/mt/no...
).

Sampling and description of animals

Considered the equation n=Zα22p1pd2 (zα22 is a tabulated value of the normal distribution, p is the proportion of successes or prevalence and d2 is the estimate margin of error), the calculated sample size was 385 dogs, which considered the ratio of dogs to humans in the area of 7:1 and a population estimated in 2017 to be 12.484 inhabitants in a territorial extension of 4.934.713 km2 (IBGE, 2018Instituto Brasileiro de Geografia e Estatística – IBGE. Panorama da cidade de Nossa Senhora do Livramento em 2018 [online]. Brasília: IBGE; 2018 [cited 2019 Mar 15]. Available from: https://cidades.ibge.gov.br/brasil/mt/nossa-senhora-do-livramento/panorama
https://cidades.ibge.gov.br/brasil/mt/no...
), with a confidence level of 95%, acceptable error of 5%, and prevalence of 50% (Brasil, 2014Brasil. Ministério da Saúde. Manual de vigilância e controle da Leishmaniose Visceral. Brasília: Ministério da Saúde; 2014. 122 p.), using the software EpiInfo (7.1.4). Domiciled dogs of both sexes, of different breeds, and ≥ 6 months of age were included (CDC, 2014Centers for Disease Control and Prevetion – CDC. EPI INFO™ 7. Version 7.1.4 [online]. Atlanta: CDC; 2014 [cited 2018 June 14]. Available from: http://www.cdc.gov/epiinfo
http://www.cdc.gov/epiinfo...
).

Clinical evaluation and sample collection

Dogs were examined and classified according to the method described by Solano-Gallego et al. (2009)Solano-Gallego L, Koutinas A, Miró G, Cardoso L, Pennisi MG, Ferrer G, et al. Directions for the diagnosis, clinical staging, treatment and prevention of canine leishmaniosis. Vet Parasitol 2009; 165(1-2): 1-18. http://dx.doi.org/10.1016/j.vetpar.2009.05.022. PMid:19559536.
http://dx.doi.org/10.1016/j.vetpar.2009....
in symptomatic and asymptomatic animals. Initially, local asepsis of the skin was performed with 70% ethyl alcohol and, with sterile syringe, approximately 10 mL of blood was collected by puncture of the external or cephalic jugular vein. Serum was separated by centrifugation and stored at -20 °C until processing.

The present study was approved by the Animal Ethics Committee of the Federal University of Mato Grosso (CEUA-UFMT; Number 23108.942583/2018-82), and all procedures were performed only after written consent was provided by the tutors of the animals.

Serological diagnosis

Serological diagnosis was performed using a commercially available immunochromatographic test (Dual Path Platform [DPP], ChemBio Diagnostic Systems Inc., Medford, NJ, USA) that uses the recombinant protein k28 (fragments k26, k39 and k9) as antigen, isolated from L. (L.) donovani, for screening. The enzyme-linked immunosorbent assay (ELISA), wich uses the soluble and lysate antigen of Leishmania major-like, as a confirmatory test (Brasil, 2011Brasil. Ministério da Saúde. Nota técnica conjunta nº 01/2011- CGDT/DEVIT/SUS/MS: esclarecimento sobre a substituição do protocolo diagnóstico da leishmaniose visceral canina (LVC). Brasília: Ministério da Saúde; 2011.), according to manufacturer’s instuctions (Bio-Manguinhos/Fiocruz, Brazil).

Epidemiological and perception analysis

Information regarding the living environment (proximity to areas of vegetation, rivers or bays, presence of other domestic animals, presence of trees, vegetable gardens or livestock in the backyard of houses, and whether there was public garbage collection), as well as dog population characteristics (breed, sex, age, house function, and presence of clinical signs) were obtained using an epidemiological questionnaire. Perception was assessed by interviews querying guardians’ knowledge of the disease (etiological agent, vector, and hosts), and prevention and control measures.

Spatial analysis

Geographical locations were identified using global positioning equipment (Monterra, Garmin, Olathe, Kansas, USA), with each household visited represented by a mark. Thus, dogs residing in the same household were registered at the same geographical point.

For spatial visualisation of the point pattern, the dogs’ location was plotted using the geographical coordinates to construct a point map. The kernel intensity estimate was then calculated to evaluate the density of the points. All of these procedures were performed in the ArcGIS 10.3 software.

Statistical analysis

Prevalence values and corresponding 95% confidence intervals were calculated. The association between the prevalence of anti-Leishmania spp. antibodies in dogs and independent variables was performed by two-step logistic regression (i.e., univariate and multivariate analysis). Variables with p ≤ 0.20 in the chi-squared test were selected for multivariate analysis, and differences with p ≤ 0.05 were considered to be statistically significant.

The chi-squared test was used to assess perception, as a means of comparing the statistical differences between the responses obtained for each variable and assessing the association between respondents’ responses and CVL serology. All analyses were performed using the R statistical package version 3.4.4 (R Core Team, 2018R Core Team. R: a language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing; 2018 [cited 2018 Nov 2]. Available from: https://www.R-project.org/
https://www.R-project.org/...
).

Ethics statement

In this study, all procedures using animals complied with the Ethical Principles in Animal Research adopted by the College of Animal Experimentation (COBEA) and were approved (protocol number 23108.942583/2018-82) by the Animal Research Ethics Committee of the Federal University of Mato Grosso, Brazil.

Results

Of the 385 dogs analysed, 54 were TR-DPP reagent-positive in the screening test and confirmed by ELISA, corresponding to a prevalence of 14% for CVL in the municipality of Nossa Senhora do Livramento. Considering reactive dogs, no significant differences were observed according to sex and breed (only two reactive purebred dogs, Boxer and American Pitbull were detected) (Table 1).

Table 1
Univariate and multivariate analyses between dog characteristics and the prevalence of canine visceral leishmaniasis in Nossa Senhora do Livramento, Mato Grosso, Brazil.

Regarding age distribution, the population consisted mainly of dogs between 1 and 3 years of age, followed by those 3 to 7 years of age, thus characterizing a young adult population. When considering the home function performed by the reactant dogs, most were considered guard and companion dogs (48.1%), which was not statistically different from animals that were guard only (20.3%) or companion only (31.4%).

Regarding the clinical evaluation of reactant dogs, a large proportion consisted of symptomatic animals and an asymptomatic minority, with a statistical difference between the groups (Table 1). Among dogs with CVL, the most frequent clinical signs included localized lymphadenopathy (38.8%), splenomegaly (35.1%), skin lesions (35.1%), and generalized lymphadenopathy (25.9%). There were significant differences in the univariate analysis for skin lesions (p = 0.001) and, in multivariate analysis, ear ulcer (p = 0.059) and splenomegaly (p = 0.055). Regarding the body score of reactive dogs, 57.4% were classified as normal, 38.8% as thin, and 3.7% as very thin.

When considering the location of residence, a statistical difference was observed in the univariate analysis for dogs that lived in the urban area compared with the rural area (Table 2). These residences were mostly located near forests, followed by rivers/streams, with higher risks for the occurrence of the disease in both contexts (Table 2), and a smaller portion was located in urban areas without proximity to forests and/or rivers/streams. Most of the backyards of these residences consisted of land and cemented areas (61.1%), land only (37%), and lawn only (1.8%).

Table 2
Univariate and multivariate analyzes to assess the association between environmental characteristics and the occurrence of canine visceral leishmaniasis in Nossa Senhora do Livramento, Mato Grosso, Brazil.

There were plantations in 70.3% of these backyards and, in 29.6%, no practices of vegetable cultivation were observed. Other environmental and demographic factors associated with canine positivity in the univariate analysis included the following: presence of chicken coop(s); small rodents/marsupials; practice of dedetization in the house; and lack of public garbage collection. On multivariate analysis, knowledge of the occurrence of CVL in the vicinity was associated with canine positivity (Table 2).

Owners’ perception of VL

A total of 167 interviews were conducted with the guardians of the 385 dogs evaluated in the study and, of these, 68.9% of individuals had heard about VL, and 31% were unaware of the disease. Of those who had heard about VL, 68.4% knew that the disease can also affect humans, and only 19.1% reported knowing at least one clinical sign of VL in humans, and the most cited clinical sign was injuries (12.3%).

Most respondents were unaware of routes of transmission (Table 3), and 15.3% reported that mosquitoes were the disease vectors, but could not specify which species, 9.1% reported they were by direct contact with a positive dog, 3% answered “straw mosquito”, 2% reported “dengue mosquito”, 2% reported tick, and 2% associated transmission with a bite from a sick dog.

Table 3
Perception of the interviewed population regarding canine visceral leishmaniasis and univariate analysis for evaluation between responses and disease occurrence in Nossa Senhora do Livramento, Mato Grosso, Brazil.

The variable “knows the clinical signs of CVL” was related to the occurrence of the disease (Table 3), being the most cited by the interviewees: large nails, wounds, hair loss, itching, and weight loss. Approximately 86.5% of respondents answered that there is no cure for the canine form of the disease (i.e., CVL) and 24.7% reported that there was treatment; however, 75.2% of these did not know about treatment.

When asked how to prevent CVL, most respondents were completely unaware of the existence of preventive measures (Table 3). Maintenance of a clean yard was mentioned by 4.2% of tutors, euthanasia of reactive dogs by 3%, avoidance of contact with the vector by 2.4%, vaccination by 2.4%, and 1.8% responded with avoiding contact with a positive dog.

Spatial visualisation

Based on the point map, cases of CVL were scattered throughout practically all sampled areas of the municipality. However, through the kernel density estimator (Figure 1), it was possible to visualize a greater intensity of CVL cases recorded in the northeast region of Nossa Senhora do Livramento.

Figure 1
Spatial distribution of dogs sampled and Visceral Leishmaniasis reagents in the municipality of Nossa Senhora do Livramento - MT.

Discussion

Results of the present study revealed a CVL prevalence of 14% in the municipality of Nossa Senhora do Livramento, Brazil. In a state context, lower prevalence rates have been observed in other cities of Mato Grosso – 7.8% in Poxoréo (Azevedo et al., 2008Azevedo MÁA, Dias AKK, Paula HB, Perri SHV, Nunes CM. Avaliação da leishmaniose visceral canina em Poxoréo, Estado do Mato Grosso, Brazil. Rev Bras Parasitol Vet 2008; 17(3): 123-127. http://dx.doi.org/10.1590/S1984-29612008000300001. PMid:19245756.
http://dx.doi.org/10.1590/S1984-29612008...
) and 4.2% in Barão de Melgaço (Dias et al., 2017Dias AFLR, Almeida ABPF, Cruz FACS, Silva RR, Rodrigues JY, Otsubo AAF, et al. Seroprevalence and spatial analysis of canine visceral Leishmaniasis in the Pantanal Region, Mato Grosso State, Brazil. J Zoonotic Dis Public Health 2017; 1: 3.) – and the highest prevalences were reported by Duarte (2010)Duarte JLS. Aspectos epidemiológicos da Leishmaniose visceral no Município de Rondonópolis, Mato Grosso, 2003- 2008 [dissertação]. São Paulo: Faculdade de Ciências Médicas da Santa Casa de São Paulo; 2010.: 48.4% in Rondonópolis, and 22.1% in the state capital Cuiabá (Almeida et al., 2012Almeida ABPF, Sousa VRF, Cruz FACS, Dahroug MAA, Figueiredo FB, Madeira MF. Canine visceral leishmaniasis: seroprevalence and risk factors in Cuiabá, Mato Grosso, Brazil. Rev Bras Parasitol Vet 2012; 21(4): 359-365. http://dx.doi.org/10.1590/S1984-29612012005000005. PMid:23184322.
http://dx.doi.org/10.1590/S1984-29612012...
).

Different prevalences were also observed in other regions of Brazil (Barbosa et al., 2010Barbosa DS, Rocha AL, Santana AA, Souza CSF, Dias RA, Costa-Júnior LM, et al. Soroprevalência e variáveis epidemiológicas associadas à leishmaniose visceral canina em área endêmica no município de São Luís, Maranhão, Brasil. Cienc Anim Bras 2010; 11(3): 653-659. http://dx.doi.org/10.5216/cab.v11i3.5933.
http://dx.doi.org/10.5216/cab.v11i3.5933...
; D'Andrea et al., 2015D’Andrea LAZ, da Silva Fonseca E, Prestes-Carneiro LE, Guimarães RB, Yamashita RC, Soares CN, et al. The shadows of a ghost: a survey of canine leishmaniasis in Presidente Prudente and its spatial dispersion in the western region of São Paulo state, an emerging focus of visceral leishmaniasis in Brazil. BMC Vet Res 2015; 11(1): 273. http://dx.doi.org/10.1186/s12917-015-0583-6. PMid:26503368.
http://dx.doi.org/10.1186/s12917-015-058...
), and may be due to different diagnostic methods used, with variations in specificity and sensitivity, as well as size and selection of the sampled population, the type of study, and local environmental characteristics (Solano-Gallego et al., 2009Solano-Gallego L, Koutinas A, Miró G, Cardoso L, Pennisi MG, Ferrer G, et al. Directions for the diagnosis, clinical staging, treatment and prevention of canine leishmaniosis. Vet Parasitol 2009; 165(1-2): 1-18. http://dx.doi.org/10.1016/j.vetpar.2009.05.022. PMid:19559536.
http://dx.doi.org/10.1016/j.vetpar.2009....
).

Regarding age, although univariate analysis was significant for dogs > 7 years of age, age was not a factor associated with canine infection in the multivariate analysis. Results regarding the age variable have been inconsitent among studies. For example, there are many reports of a higher prevalence of the disease in young dogs (Dantas-Torres et al., 2006Dantas-Torres F, Brito MEF, Brandão-Filho SP. Seroepidemiological survey on canine leishmaniasis among dogs from an urban area of Brazil. Vet Parasitol 2006; 140(1-2): 54-60. http://dx.doi.org/10.1016/j.vetpar.2006.03.008. PMid:16621286.
http://dx.doi.org/10.1016/j.vetpar.2006....
; Figueiredo et al., 2014Figueiredo MJFM, Souza NF, Figueiredo HF, Meneses AMC, Filho ES, Nascimento GG. Fatores de risco e classificação clínica associados à soropositividade para leishmaniose visceral canina. Cienc Anim Bras 2014; 15(1): 102-106. http://dx.doi.org/10.5216/cab.v15i1.25097.
http://dx.doi.org/10.5216/cab.v15i1.2509...
), which may be associated with immunological immaturity. In other studies, higher prevalences were observed in adult to elderly animals (Coura-Vital et al., 2011Coura-Vital W, Marques MJ, Veloso VM, Roatt BM, Aguiar-Soares RDO, Reis LES, et al. Prevalence and factors associated with Leishmania infantum infection of dogs from an urban area of brazil as identified by molecular methods. PLoS Negl Trop Dis 2011; 5(8): e1291. http://dx.doi.org/10.1371/journal.pntd.0001291. PMid:21858243.
http://dx.doi.org/10.1371/journal.pntd.0...
), which would be associated with the longer incubation period of the parasite, as well as longer exposure time to the vector (Gállego, 2004Gállego M. Zoonosis emergentes por patógenos parásitos: las leishmaniosis. Rev Sci Tech Off Int Epiz 2004; 23(2): 661-676. http://dx.doi.org/10.20506/rst.23.2.1512.
http://dx.doi.org/10.20506/rst.23.2.1512...
). There is also the possibility of a bimodal distribution of seroprevalence in relation to age, with a peak being observed among young animals, and a second, more significant peak among older animals (Gálvez et al., 2010Gálvez R, Miró L, Descalzo MA, Nieto J, Dado D, Martin O, et al. Emerging trends in the seroprevalence of canine leishmaniosis in the Madrid region (central Spain). Vet Parasitol 2010; 169(3-4): 327-334. http://dx.doi.org/10.1016/j.vetpar.2009.11.025. PMid:20031330.
http://dx.doi.org/10.1016/j.vetpar.2009....
).

In the present study, symptomatic dogs, more specifically, those with at least one clinical sign associated with CVL, were three times more likely to be seroreactive compared with asymptomatic dogs, which is consitent with the observations of other studies (Figueiredo et al., 2014Figueiredo MJFM, Souza NF, Figueiredo HF, Meneses AMC, Filho ES, Nascimento GG. Fatores de risco e classificação clínica associados à soropositividade para leishmaniose visceral canina. Cienc Anim Bras 2014; 15(1): 102-106. http://dx.doi.org/10.5216/cab.v15i1.25097.
http://dx.doi.org/10.5216/cab.v15i1.2509...
; Dias et al., 2017Dias AFLR, Almeida ABPF, Cruz FACS, Silva RR, Rodrigues JY, Otsubo AAF, et al. Seroprevalence and spatial analysis of canine visceral Leishmaniasis in the Pantanal Region, Mato Grosso State, Brazil. J Zoonotic Dis Public Health 2017; 1: 3.). According to Coura-Vital et al. (2013)Coura-Vital W, Reis AB, Fausto MA, Leal GGA, Marques MJ, Veloso VM, et al. Risk factors for seroconversion by Leishmania infantum in a cohort of dogs from an endemic area of Brazil. PLoS One 2013; 8(8): e71833. http://dx.doi.org/10.1371/journal.pone.0071833. PMid:23990996.
http://dx.doi.org/10.1371/journal.pone.0...
, the association between clinical signs and positivity is due to seroconversion, mainly because symptomatic sick dogs exhibit higher levels of anti-Leishmania spp. antibodies.

Splenomegaly and skin lesions, especially ear ulcers, were clinical signs that were positively related to canine infection, corroborating clinical findings from other epidemiological studies (Rondon et al., 2008Rondon FC, Bevilaqua CML, Franke CR, Barros RS, Oliveira FR, Alcântara AC, et al. Cross-sectional serological study of canine Leishmania infection in Fortaleza, Ceará state, Brazil. Vet Parasitol 2008; 155(1-2): 24-31. http://dx.doi.org/10.1016/j.vetpar.2008.04.014. PMid:18565676.
http://dx.doi.org/10.1016/j.vetpar.2008....
; Queiroz et al., 2009Queiroz PVS, Monteiro GRG, Macedo VPS, Rocha MA, Batista LMM, Queiroz JW, et al. Canine visceral leishmaniasis in urban and rural areas of Northeast Brazil. Res Vet Sci 2009; 86(2): 267-273. http://dx.doi.org/10.1016/j.rvsc.2008.07.014.
http://dx.doi.org/10.1016/j.rvsc.2008.07...
; Islam et al., 2017Islam A, Rahman MD, Islam S, Debnath P, Alam M, Hassan MM. Sero-prevalence of visceral leishmaniasis (VL) among dogs in VL endemic areas of Mymensingh district, Bangladesh. J Adv Vet Anim Res 2017; 4(3): 241-248. http://dx.doi.org/10.5455/javar.2017.d217.
http://dx.doi.org/10.5455/javar.2017.d21...
). However, an important factor in maintaining the epidemiological cycle of VL is asymptomatic reagent-positive dogs, which has been reported in different studies (Dantas-Torres et al., 2006Dantas-Torres F, Brito MEF, Brandão-Filho SP. Seroepidemiological survey on canine leishmaniasis among dogs from an urban area of Brazil. Vet Parasitol 2006; 140(1-2): 54-60. http://dx.doi.org/10.1016/j.vetpar.2006.03.008. PMid:16621286.
http://dx.doi.org/10.1016/j.vetpar.2006....
; Coura-Vital et al., 2011Coura-Vital W, Marques MJ, Veloso VM, Roatt BM, Aguiar-Soares RDO, Reis LES, et al. Prevalence and factors associated with Leishmania infantum infection of dogs from an urban area of brazil as identified by molecular methods. PLoS Negl Trop Dis 2011; 5(8): e1291. http://dx.doi.org/10.1371/journal.pntd.0001291. PMid:21858243.
http://dx.doi.org/10.1371/journal.pntd.0...
) because they remain in the environment with the potential to infect the vectors (Molina et al., 1994Molina R, Amela C, Nieto J, San-Andrés H, González F, Castillo JA, et al. Infectivity of dogs naturally infected with Leishmania infantum to colonized Phlebotomus perniciosus. Trans R Soc Trop Med Hyg 1994; 88(4): 491-493. http://dx.doi.org/10.1016/0035-9203(94)90446-4. PMid:7570854.
http://dx.doi.org/10.1016/0035-9203(94)9...
) and maintain the transmission cycle.

Considering the results of univariate analysis in the municipality studied, the prevalence of seroreactive dogs was higher in the rural zone and differed from the urban zone. This high prevalence in the rural area was associated with the presence of chicken coops and rodents/marsupials in the households visited.

According to Ávila et al. (2018)Ávila MM, Brilhante AF, Souza CF, Bevilacqua PD, Galati EAB, Brazil RP. Ecology, feeding and natural infection by Leishmania spp. of phlebotomine sand flies in an area of high incidence of American tegumentary leishmaniasis in the municipality of Rio Branco, Acre, Brazil. Parasit Vectors 2018; 11(1): 64. http://dx.doi.org/10.1186/s13071-018-2641-y. PMid:29373995.
http://dx.doi.org/10.1186/s13071-018-264...
, the environmental context facilitates maintenance and dispersion of the vector.Thus, the observation of high prevalence of CVL in dogs living in rural environments serves as a warning indicator of higher risk for infection in the rural population, because in this municipality (IBGE, 2010Instituto Brasileiro de Geografia e Estatística – IBGE. Censo populacional Nossa Senhora do Livramento 2010 [online]. Brasília: IBGE; 2010 [cited 2019 Mar 10]. Available from: https://cidades.ibge.gov.br/brasil/mt/nossa-senhora-do-livramento/pesquisa/23/25207
https://cidades.ibge.gov.br/brasil/mt/no...
), as in the study by Dias et al. (2017)Dias AFLR, Almeida ABPF, Cruz FACS, Silva RR, Rodrigues JY, Otsubo AAF, et al. Seroprevalence and spatial analysis of canine visceral Leishmaniasis in the Pantanal Region, Mato Grosso State, Brazil. J Zoonotic Dis Public Health 2017; 1: 3., the largest proportion of the human population lived in rural areas.

Continuing with environmental variables, the univariate analysis revealed that the lack of public garbage collection was a risk factor for CVL. Such a result was also reported to contribute to a higher risk for canine and human disease in a previous study (Dias et al., 2018Dias RCF, Thomaz-Soccol V, Pasquali AKS, Alban SM, Fendrich RC, Pozzolo EM, et al. Variables associated with the prevalence of anti-Leishmania spp. antibodies in dogs on the tri-border of Foz do Iguaçu, Paraná, Brazil. Rev Bras Parasitol Vet 2018; 27(3): 338-347. http://dx.doi.org/10.1590/s1984-296120180055. PMid:30184001.
http://dx.doi.org/10.1590/s1984-29612018...
; Lima et al., 2018Lima ID, Lima ALM, Mendes-Aguiar CO, Coutinho JFV, Wilson ME, Pearson RD, et al. Changing demographics of visceral leishmaniasis in northeast Brazil: lessons for the future. PLoS Negl Trop Dis 2018; 12(3): e0006164. http://dx.doi.org/10.1371/journal.pntd.0006164. PMid:29509765.
http://dx.doi.org/10.1371/journal.pntd.0...
). According to Oliveira & Araújo (2003)Oliveira SS, Araújo TM. Avaliação das ações de controle da leishmaniose visceral (calazar) em uma área endêmica do Estado da Bahia, Brasil (1995-2000). Cad Saude Publica 2003; 19(6): 1681-1690. http://dx.doi.org/10.1590/S0102-311X2003000600012. PMid:14999334.
http://dx.doi.org/10.1590/S0102-311X2003...
, residues in the peridomicile can serve as a shelter and breeding ground for vectors, which may explain why previous occurrence of CVL in the neighborhood in our study was a risk factor for infection. Therefore, households with previous occurrence of CVL represent an obvious risk for infection of other dogs in the house, aside from offering favorable environmental conditions for the vector(s), thus favoring new cases of the disease (Dereure et al., 2003Dereure J, El-Safi SH, Bucheton B, Boni H, Kheir MM, Davoust B, et al. Visceral leishmaniasis in eastem Sudan: parasite identification in humans and dogs; host-parasite relationships. Microbes Infect 2003; 5(12): 1103-1108. http://dx.doi.org/10.1016/j.micinf.2003.07.003. PMid:14554251.
http://dx.doi.org/10.1016/j.micinf.2003....
).

To reduce the risk for CVL in Brazil, the leishmaniasis control and prevention programme recommends actions on different fronts and encourages action from the population in disease control measures. In this study, when we assessed the perception of the guardians of dogs sampled, 86.58% were unaware of the existence of preventive measures for the disease. Margonari et al. (2012)Margonari C, Menezes JA, Rocha MN, Maia KN, Oliveira ME, Fonseca AL, et al. Public knowledge about and detection of canine visceral leishmaniasis in urban Divinópolis, Brazil. J Trop Med 2012; 2012: 429586. http://dx.doi.org/10.1155/2012/429586. PMid:22991521.
http://dx.doi.org/10.1155/2012/429586...
also reported superficial knowledge and low participation of the population in the control and prevention of VL. Menezes et al. (2016)Menezes JA, Luz TCB, Sousa FF, Verne RN, Lima FP, Margonari C. Peridomiciliary risk factors and knowledge concerning visceral leishmaniasis in the population of Formiga, Minas Gerais, Brazil. Rev Bras Epidemiol 2016; 19(2): 362-374. http://dx.doi.org/10.1590/1980-5497201600020013. PMid:27532759.
http://dx.doi.org/10.1590/1980-549720160...
commented that this fragmented perception of VL does not permit a deep understanding or recognition of all components of the epidemiological chain of the disease.

In this sense, the relationship between seroreactive dogs and the variables, “have heard about VL” and “know the symptoms of CVL”, can be understood as measures of previous exposure to the disease, explaining, for example, the risk for occurrence of CVL being almost six times higher in homes that have already been sprayed with insecticides. Similar results were reported by Coura-Vital et al. (2011)Coura-Vital W, Marques MJ, Veloso VM, Roatt BM, Aguiar-Soares RDO, Reis LES, et al. Prevalence and factors associated with Leishmania infantum infection of dogs from an urban area of brazil as identified by molecular methods. PLoS Negl Trop Dis 2011; 5(8): e1291. http://dx.doi.org/10.1371/journal.pntd.0001291. PMid:21858243.
http://dx.doi.org/10.1371/journal.pntd.0...
, who observed that dogs whose owners knew the vector was associated with a higher risk for infection compared with dog owners who were unaware of this information.

Regarding spatial assessment, several studies focused on the geographical distribution of HVL (Silva et al., 2017Silva TAM, Coura-Vital W, Barbosa DS, Oiko CSF, Morais MHF, Tourinho BD, et al. Spatial and temporal trends of visceral leishmaniasis by mesoregion in a southeastern state of Brazil, 2002-2013. PLoS Negl Trop Dis 2017; 11(10): e0005950. http://dx.doi.org/10.1371/journal.pntd.0005950. PMid:28985218.
http://dx.doi.org/10.1371/journal.pntd.0...
; Galgamuwa et al., 2018Galgamuwa LS, Dharmaratne SD, Iddawela D. Leishmaniasis in Sri Lanka: spatial distribution and seasonal variations from 2009 to 2016. Parasit Vectors 2018; 11(1): 60. http://dx.doi.org/10.1186/s13071-018-2647-5. PMid:29370864.
http://dx.doi.org/10.1186/s13071-018-264...
) and CVL (Ursine et al., 2016Ursine RL, Dias JVL, Morais HA, Pires HHR. Human and canine visceral leishmaniasis in an emerging focus in Araçuaí, Minas Gerais: spatial distribution and socio-environmental factors. Mem Inst Oswaldo Cruz 2016; 111(8): 505-511. http://dx.doi.org/10.1590/0074-02760160133.
http://dx.doi.org/10.1590/0074-027601601...
; Lana et al., 2018Lana RS, Michalsky EM, Lopes LO, Lara-Silva FO, Nascimento JL, Pinheiro LC, et al. Ecoepidemiological aspects of visceral leishmaniasis in an endemic area in the Steel Valley in Brazil: an ecological approach with spatial analysis. PLoS One 2018; 13(10): e0206452. http://dx.doi.org/10.1371/journal.pone.0206452.
http://dx.doi.org/10.1371/journal.pone.0...
). To our knowledge, however, the present study was the first to use a spatial approach to canine disease in Nossa Senhora do Livramento, although the municipality has annually reported cases of HVL since 2015 (Mato Grosso, 2019Mato Grosso. Secretaria de Estado de Saúde. Data WareHouse [online]. Cuiabá: SES-MT; 2019 [cited 2019 Oct 1]. Available from: http://appweb3.saude.mt.gov.br/dw/pesquisa/detalhe
http://appweb3.saude.mt.gov.br/dw/pesqui...
).

Despite the point map demonstrating a wide distribution of reactant dogs in the assessed areas, the fact that several dogs resided at the same coordinates made it difficult to identify patterns of infection. However, with the intensity map (Figure 2), it was possible to see that the urban area (of a smaller territorial extension), represented by the black color, indicated a higher intensity of reactive dogs. More specifically, despite a lower prevalence of CVL in relation to rural areas, the urban population is also at risk for infection, which further supports the process of urbanisation of the disease described in several previous studies (Duarte, 2010Duarte JLS. Aspectos epidemiológicos da Leishmaniose visceral no Município de Rondonópolis, Mato Grosso, 2003- 2008 [dissertação]. São Paulo: Faculdade de Ciências Médicas da Santa Casa de São Paulo; 2010.; Gálvez et al., 2010Gálvez R, Miró L, Descalzo MA, Nieto J, Dado D, Martin O, et al. Emerging trends in the seroprevalence of canine leishmaniosis in the Madrid region (central Spain). Vet Parasitol 2010; 169(3-4): 327-334. http://dx.doi.org/10.1016/j.vetpar.2009.11.025. PMid:20031330.
http://dx.doi.org/10.1016/j.vetpar.2009....
; Pimentel et al., 2015Pimentel DS, Ramos RAN, Santana MA, Maia CS, Carvalho GA, Silva HP, et al. Prevalence of zoonotic visceral leishmaniasis in dogs in an endemic area of Brazil. Rev Soc Bras Med Trop 2015; 48(4): 491-493. http://dx.doi.org/10.1590/0037-8682-0224-2014. PMid:26132498.
http://dx.doi.org/10.1590/0037-8682-0224...
).

Figure 2
Kernel map, identifying low to high density regions of Canine Visceral Leishmaniasis in Nossa Senhora do Livramento - MT.

Considering the data obtained in this study, a significant prevalence of CVL was observed in Nossa Senhora do Livramento, which should raise awareness to the risk for new human cases, given that canine disease precedes human disease. Factors inherent to dogs, the environment, and population perception were associated with the occurrence of CVL, observed spatially in both rural and urban contexts.

Thus, these data reaffirm the classification of VL as a neglected disease, where endemics are observed in low-income populations in poor or developing countries with poor infrastructure and emphasizes the importance of epidemiological surveillance and the need to implement control and prevention strategies for CVL focused mainly on environmental management and health education activities.

Acknowledgements

We thank the Ministry of Health for providing the Dual Path Platform (DPP®) and enzyme-linked immunosorbent assay (ELISA) tests used in this research. We are also grateful to the Secretary of Health of the State of Mato Grosso and the Secretariat of Health of the municipality of Nossa Senhora do Livramento (Locimar Bispo da Silva). To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for grating the scholarship.

  • How to cite: Carvalho MR, Dias AFLR, Almeida ABPF, Alves MR, Paes AS, Sousa VRF. Canine visceral leishmaniasis: perception, prevalence, and spatial distribution in municipality of Nossa Senhora do Livramento, Mato Grosso, Brazil. Braz J Vet Parsitol 2020; 29(2): e021019. https://doi.org/10.1590/S1984-29612020017

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Publication Dates

  • Publication in this collection
    18 May 2020
  • Date of issue
    2020

History

  • Received
    11 Nov 2019
  • Accepted
    19 Feb 2020
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br