Geospatial and Transmission Evidences of the Human Fascioliasis Cases
(2012-2017) in South Bahia, Brazil
Evidências Geoespaciais e de Transmissão de Casos de Fasciolíase
Humana (2012-2017) no Sul da Bahia, Brasil
DOI:10.34117/bjdv6n3-298
Recebimento dos originais: 29/02/2020 Aceitação para publicação: 19/03/2020
Tiago Santos de Oliveira
Biomedical. Laboratory of Human Parasitology Department of Biological Sciences State University of Santa Cruz, BR-415, km 16 - Salobrinho, Ilhéus, Bahia, Brazil
E-mail: tiagobiomed28@gmail.com
Júllyan Mendes Silva da Silva
Biomedical. Laboratory of Human Parasitology. Department of Biological Sciences, State University of Santa Cruz, BR-415, km 16 - Salobrinho, Ilhéus, Bahia, Brazil
E-mail: jullyanmendes@hotmail.com
Raquel Moraes Ramos Silva
Nurse, Master in Health Sciences. Postgraduate Program in Health Sciences State University of Santa Cruz, BR-415, km 16 - Salobrinho, Ilhéus, Bahia, Brazil
E-mail: raquel_moraes@outlook.com
Maurício Santana Moreau
PhD in Agronomy (Soils and Plant Nutrition) from the Federal University of Viçosa Full Professor at the Department of Agricultural Sciences
State University of Santa Cruz, BR-415, km 16 - Salobrinho, Ilhéus, Bahia, Brazil E-mail: mmoreau@uesc.br
Ana Paula Melo Mariano
PhD in Public Health from the University of São Paulo. Adjunct Professor at the Center of Environmental Health - Department of Biological Sciences
State University of Santa Cruz, BR-415, km 16 - Salobrinho, Ilhéus, Bahia, Brazil. Email: apm.mariano@hotmail.com
Marcelo Fernandes da Silva
PhD in Sciences from the University of São Paulo. Professor of the Postgraduate Program in Health Sciences and Full Professor of the Center of Environmental Health
State University of Santa Cruz, BR-415, km 16 - Salobrinho, Ilhéus, Bahia, Brazil E-mail: mfsilva@uesc.br
ABSTRACT
Human fascioliasis, despite suspected cases, is rarely confirmed in the Northeast of Brazil. Unfortunately, it is still possible to diagnose the presence of the eggs of Fasciola hepatica in the feces samples of children and adults; in addition, previous studies have already demonstrated the presence of the intermediate host Lymnaea spp. in the state of
Bahia. A parasitological survey with inhabitants of an urban conglomerate in the city of Ilhéus, South Bahia, Brazil, revealed new cases (n=7) of human facioliasis (2012-2016), with a significant (p<0,01) prevalence (P = 0,036) affecting mainly children (n=5 or 71.43% of the cases). In addition, the mollusks captured among households were of the species Lymnea spp (n= 20) Neritina zebra (n = 15) and Physa acuta (n = 133). The analysis of geospatial data revealed that the collection sites in the Teotônio Vilela neighborhood gathered evidences that favor unusual human cases of fascioliasis, nonetheless, not notified by the municipal health system. It includes the topography with floods along the water courses where the Lymnaea spp. snails were found besides to the poor sanitation in the marginal housing with inadequate sewage.
Keywords: Environmental Parasitology, Fascioliasis, Geospatial, Trematoda. RESUMO
A fasciolíase humana, apesar dos casos suspeitos, raramente é confirmada no Nordeste do Brasil. Infelizmente, ainda é possível diagnosticar a presença dos ovos de Fasciola hepatica nas amostras de fezes de crianças e adultos; além disso, estudos anteriores já demonstraram a presença do hospedeiro intermediário Lymnaea spp. no estado da Bahia. Um levantamento parasitológico com habitantes de um dos bairro da cidade de Ilhéus, sul da Bahia, Brasil, revelou novos casos (n = 7) de faciolíase humana (2012-2016), com prevalência significativa (p <0,01) (P = 0,036) afetando principalmente crianças (n = 5 ou 71,43% dos casos). Além disso, os moluscos capturados na proximidade dos domicílios eram da espécie Lymnea spp (n = 20) Neritina zebra (n = 15) e Physa acuta (n = 133). A análise dos dados geoespaciais incluiu a topografia com inundações ao longo dos cursos d'água onde foram encontrados Lymnaea spp. além de saneamento inadequado nas habitações marginais com esgoto nos locais de coleta no bairro de Teotônio Vilela, reunindo evidências que favoreceram os achados de casos humanos incomuns de fasciolíase, não notificados pelo sistema municipal de saúde.
Palavras-chave: Parasitologia Ambiental, Fasciolíase Geoespacial, Trematoda.
1 INTRODUÇÃO
Fascioliasis is a neglected zoonotic disease that accidentally affects humans. Contamination occurs by ingestion of water and raw foods containing the metacercaria (Esteban et al., 2002; Guimarães, 2003), an infective form of Fasciola hepatica trematode. Although it stills a little-known disease, it is estimated that about 750 million people worldwide are at risk of infection (Elelu & Eisler, 2017). An estimative of the cases in Brazil would be imprecise, since the number of cases has an unofficial picture (Igreja et al., 2004; Mezzari et al., 2000; Oliveira et al., 2007; Pile et al., 2000). More recently, however, a systematic review of literature from 1950 to 2016 by Pritsch and Molento (2018) affirmed the prevalence of 48 cases in Brazil, two of them in the South of Bahia.
The cycle of Facioliasis depends on the availability of fresh water, which is the environment of the intermediate host, the mollusks of the genus Lymnaea (Brasil, 2008), is also the means of dispersing the infective forms of Fasciola hepatica. Studies have been shown that the combination of global climate changes and anthropogenic activities directly interfere with the cycle of parasitic diseases (Bilac & Alves, 2014; Kalinda et al., 2017; Maia, 2013; Patz et al., 2000) compromising the balance of ecosystems, as they affect land cover and water quality. In addition, the lack of urban infrastructure and poor sanitation contribute to the spread of infectious agents (WHO, 2014), threatening, for example, leisure and adventure tourism activities with activities in rivers, waterfalls, and lagoons (Barreto et al, 2016).
An important resource for monitoring these conditions is the geospatial methods, which allows biological, environmental and sociopolitical information to be combined to elucidate the health-disease process and to develop more effective control actions (Bennema, et al., 2014; Chen et al., 2013; Dutra, 2011; Nardi et al., 2013). Based on these findings, this study proposed to analyze by using geospatial tolls, the evidences involved in the occurrence of fascioliasis cases in a neighborhood in the municipality of Ilhéus, South Bahia, Brazil.
2 MATERIAL AND METHODS Study population
The study was conducted in the Teotônio Vilela neighborhood, located in the municipality of Ilhéus, a coastal tourist town in the south state of Bahia, Brazil from 2014 to 2017. The study area was divided into three subareas, based on the census division of the Brazilian Institute of Geography and Statistics (IBGE, 2016). Considering the resident population in the locality, with a confidence interval of 90%, a sample error of 10% and a random loss of 30% of the questionnaires, a participation of n= 137 individuals was calculated. As exclusion criteria were considered: no consent, absence of the signature in the consent form and/or response on the questionnaire or absence of at least one fecal sample delivery and moving out of the study area.
The first stage of the research considered families vulnerable to parasitic diseases, according to the indication of health community agents of the local Family Health Unit. During the home visit, upon understanding the study, the volunteers who agreed to participate signed the consent/assent term and responded to the socio-epidemiological
and socio-health questionnaires. This instrument contained questions about gender, age, racial, schooling, family income, life and most common habits associated with Fasciola contamination, such as consumption of vegetables and their origin, and origin of ingested water (Chen et al, 2013). In the second stage, a parasitological survey was carried out, collecting three fecal samples on previously combined schedule. The material was processed by the methods Mariano & Carvalho and Kato-Katz (Mariano et al., 2007; Barbosa et al., 2017). Therefore, mollusks were searched in the field and caught in swamps and streams in the research area. The animals were identified and kept under simulated conditions to investigate the occurrence of cercarial burden at laboratory.
Research on molluscs and induction to the experimental release of cercariae
The study area is bathed by important rivers of Ilhéus hydrographic network: Fundão, Itacanoeira and Cachoeira rivers. Thus, the collection of mollusks was concentrated in crowded points on the banks of the rivers, where the local population reported the presence of snails similar to the intermediate host species, and in areas of flooding during periods of heavy rainfall. The snails were captured directly with the aid of metal tweezers or by scraping with a shell or nylon net with an expandable mitt, making it possible to reach a distance of more than one meter from the margin and to efficiently scrape the substrate in the depth of the banks of rivers and streams.
The captured snails were taken in plastic collectors and kept in some water from the bed of the river of origin or in a volume of dechlorinated water. After collection, the animals were kept under dechlorinated water with exchange every two days. In order to avoid accidents, the containers were always kept closed with perforated covers, with a nylon protection to prevent the animals from reaching out the container. Handling the animals was done with gloves and tweezers. The dead individuals were removed from the container and their shells stored and cataloged. Samples of the vegetation closer to the water source on the collection sites were also taken to further investigation in the laboratory in order to identify metacercarial structures.
Two mollusks were put in 24-well cell culture dish well containing previously aerated distilled water and lined with cellophane paper; in a 6-well plate, 8 snails were placed in each well lined with specimens of raw vegetables (Nasturtium spp. and Lactuca sativa). After 5 days of photostimulation and heat (alternating exposure to direct sunlight and incandescent lamp 40W at 27-32cm distance from the plates). The collected
vegetables were sectioned with a stylet and crushed between glass plates to identify the metacercariae at the stereomicrocope and microscope, as well as the sheets of cellophane paper.
Geospatial of thematic maps
The collection areas were georeferenced using the Garmin® digital reader equipment, eTrex10 model, using the SIRGAS 2000 UTM 24s coordinate system, as well as the altimetry feature of the digital reader. The points of the participating households were mapped, sites of snail collection, and interest in communities (areas of greater movement, social facilities); possible flooding variations were also demarcated, based on the visual findings of field researchers and community residents; as well as demarcation of strategic points for visual representation of the topography by means of the IDW interpolation method. In addition, the public databases of the IBGE, Department of Informatics of the National Health System (DATASUS), Instituto Nossa Ilhéus web page and the State Institute of the Environment (INEMA) were accessed to obtain data from the city of Ilhéus, as data tracts of the 2010 Census, digital cartographic base, social data and hydrographic network. All the data processing, scenarios and maps were elaborated in the GIS software QGIS 2.18.11.
3 RESULTS AND DISCUSSION
A characterization of volunteers is showed in the Table 1. The effective population of Area 02 was lower than expected, however, considering the total number of volunteers (n= 225), it was obtained the necessary number of volunteers to validate the results obtained in the research (Table 1). The summarizing of socio-health aspects of the studied population reveals distinct characteristics in each Area. As for the general water supply, there was a variation among areas, being 85.5% of the households located of in Area 01 (230 households in the total of 269 in the census sector), 93.72% in Area 02 (224 of the 239 households), and 95.7% in Area 03 (204 out of 213 households in total). As for native well water, the occurrence of in 24 households in Area 01, in 11 households in Area 02 , and in 4 residences in Area 03 (1.8%). Regarding sanitation and general sewage, Area 01 presents the lowest coverage index of sanitation network, with 158 households in this condition (58.7%) then the Area 02 (87.4%) and 163 (76.5%).
Table 1: Characterization of the studied population
Total Area 01 Area 02 Area 03
Population
Resident * 2482 939 751 792
Expected population (calculated) 137 49 40 48
Invited to participate 100 n.d. 43 57
Exclusion of the study** 30 n.d. 21 9
Volunteers 225 155 22# 48
Fecal sample delivered
Sample 1 215 145 22 48
Sample 2 175 116 17 42
Sample 3 126 80 14 32
Total 516 341 53 122
* as defined in the last demographic census sectorization; ** as defined by exclusion criteria; # number below of the expected; n.d. not determined.
Therefore, there is accumulation of garbage in 40 households in Area 01 (14%), 2 vacant lots in Area 03 (0.9%). This is an important risk factor, since the disposal of household waste in inadequate environment attracts insects, potential vectors for various diseases, increases the possibility of water contamination, besides contributing to the flooding of urban roads.
According to the parasitological investigation, it was observed that at least half of the studied population in all the areas was diagnosed with two or more parasites, such as helminthiases or protozoooses (Table 2). Thus, there were six individuals with positive (F=6/225 = 0,026) diagnostic of Fascioliasis since a typical Fasciola spp ellipsoidal and operculated eggs seen in the coproparasitological examination and diagnosed by specific morphological aspects not observed in Ascaris lumbricoides, Ancylostoma spp or Paragonimus westermani (not shown). Also the potential misdiagnoses were avoided by having the participants abstained from eating liver before stool examination schedule having at least five different samples. The initial cases occurred in the Area 01 in the year of 2012. In addition, it was possible to detect the occurrence of a new case in the Area 03 (F= 1/48 = 0,020). The overall (2012-2016) prevalence of the Fascioliasis in the present study was 0,031 (F=7/225). Despite the efforts, it was not possible to confirm the diagnosis of the disease with more precise techniques, such as immunological or molecular tests.
Table 2: Overview of the parasitological survey
Total Area 01 Area 02 Area 03 n = 225 n = 155 % n = 22 % n = 48 % Negative 28 17 17,5 2 9 5 10,4 Positive 191 128 82,5 20 91 43 89,6 Monoparasitism 51 38 24,6 6 27,2 7 14,6 Poliparasitism 140 90 75,4 14 63,6 36 75 Main protozooa Entamoeba coli 14 63,6 23 47,9 Entamoeba histolytica 5 22,7 15 31,2 Giardia lamblia 9 40,9 16 33,3 Main helminthes Ascaris lumbricoides 39 25,2 2 9,1 9 18,7 Trichuris trichiura 29 18,7 3 13,6 11 22,9 Ancylostoma spp. 3 13,6 11 22,9 Fasciola hepatica 7 6 3,8 - - 1 2,8
As for the research of snails, we observed in the Areas 01 and 03 the presence of small water shafts that compose the hydrography of the rivers of the Teotônio Vilela. Especially in Area 01, there are two water courses one having 165 and another with 200 meters of extension, where were targeted by 16 collection points, alternating with a distance of approximately 15 meters. Nonetheless, none was infected by cercareas or even release cercarial forms after experimental induction. None of the vegetables collected did exhibit metacercaria strucutures (not shown).
During the first visits to the community, it was possible to find mollusks of the genus Lymnaea in the swampy areas of the stream (Fig. 1), where there was little deposition of residential or other types of garbage. However, in order to contain the recurrent floods, the community requested the deposition of the landfill debris of a large construction site in the neighborhood, making the first collection points disappear. The Figure 2 shows the comparison of the site before and after the ground. After this event, the only species found in the bank of the streams was Physa acuta, along with shells of other species.
Figure 1: Typical snail of mollusks collected in the Area 01 identified as Lymnaea sp. (first three snails right to left) and Physa acuta (last two).
Figure 2: Map of the collection sites in Area 01 before (A) and after (B) grounding. Image A was kindly provided by Dr. Maurício Santana Moreau. The image B was taken from Google Earth®. Note: In A (2014) the marsh and stream bed with evident vegetation are observed (arrows), while in B (2015) the same area after grounding.
Figure 3: Representatives of altimetry and water course alteration before (A) and after (B) grounding within the prevalence of snail’s distribution in the Area 1. Grayish hot-spots mean difference (in meters) in ground elevation (altimetry). Species of mollusks are identified in the diamonds (darker =Lymnae sp.; clearer =
Physa acuta)
In addition to an impressive visual effect, the deposition of material in the swamp area also altered the altimetry in the environment, according to the Figures 3. Previously, the highest altitude was 6.70 m above sea level (upstream of the narrow water course) and the lowest, 5.42 m (central part of the stream), with a difference greater than 1 meter. The altimetry of the stream was about 6.1 m to 6.3 m, with a difference of about 1 m in relation to the central part. After the alteration (Fig.3b) turned the terrain more plan thus reducing the water flow and the floodings. It was possible to localize precisely the inhabitants with positive diagnostic of fascioliasis (5 of the 6) on the map (solid square) showed in Figure 3A. It was possible to note a combination of snails, the water course proximity and the emergence of the human cases of fascioliasis in the Area 01.
Through geospatial tolls it was possible to find significant associations regarding the spatial distribution of the socioeconomic, demographic and health data of the population with exposure to the snails of the genus Lymnaea sp. and Physa acuta, despite the mollusks were not infected with F. hepatica larvae (not shown). It is possible that some of the animals analyzed were infected, but unable to release cercariae during the
experiment. The species Physa acuta is capable to be infect with miracids of Fasciola hepatica, however, the natural infection rate is very low, due to some kind of deleterious action on miracidium, mainly caused by mucus substances produced, as well as the maladaptability of parasite for the development of larval forms in the tissues of the mollusk (Chen et al., 2013; Gomes & Serra-Freire, 2001).
Considering that most of the positive cases in Area 01 laid in the swamp area, it is possible to speculate if that the infection might have been autochthonous. In the periods of heavy rain, water was dammed in the central part of the stream (Fig. 3A), reaching homes and the school where the children diagnosed were studying. According to locals, mollusks were easily found in the streets and homes, within of reach of the children. It is noteworthy that despite the grounding of the site, the condition of inadequate disposal of domestic sewage remained.
Nevertheless, considering the spatial overlap of the diagnosed cases of human fascioliasis and the location where the snails were found, it is possible to argue that there was a potential risk of transmission of the disease. Regarding the influence of climate on the prevalence of fascioliasis, the data obtained in this research agree with several authors in recent publications on the association between the presence of snails and diseased animals in places with hot weather and with higher rainfall, such as in the municipality of Ilhéus, and lower altimetry. Studies indicate that the major influences in the prevalence of bovine fascioliasis are temperature variation, seasonality of temperature, and increase of rainfall volume, especially in the hottest months of the year (Bennema et al., 2017; Bosco et al., 2015; Selemetas, Waal, 2015).
According to data from the National Institute of Meteorology (INMET), in 2016 due to the low intensity of El Niño, accumulated rainfall in the Northeast region was below oh the average. In Bahia, however, rainfall was higher than expected during the month of January. In addition, in the same year the temperatures were above the usual. Thus, when considering the climatic variables (temperature variations and precipitation) to the risk maps developed, it is possible to include the South of the State of Bahia in the areas at risk for fascioliasis. Maps produced using geoprocessing tools can then be used to subsidize activities of public and animal health programs, even in areas without notification of fascioliasis (Bennema et al., 2017).
A GIS study for the mapping of the risk of fascioliasis was developed for the southern part of the state of Espírito Santo, Brazil. The determinants investigated were
precipitation, temperature, elevation, slope, soil type and land use. The weights and values were attributed to the determinants and their categories according to their relevance in relation to animal fascioliasis. The thematic maps that describe the spatial distribution of the areas of greater risk indicate that more than 50% of the south of Espírito Santo is in a high risk of fascioliasis. These areas were characterized by a comparatively high temperature, but a relatively low slope, low rainfall and low elevation, corresponding to periodically flooded pastures or soils that promote water retention. (Martins et al., 2012)
One of the first contributions in the study of fascioliasis and the geographic and climatic conditions was Freitas' master's dissertation (2013). In it, the author aimed to use GIS to facilitate the understanding and visualization of the disease in cattle, delimiting possible risk areas in the state of Espírito Santo. Thus, risk maps were developed for F. hepatica based on environmental and climatic variables considered fundamental for the maintenance of the disease and maps of bioclimatological zoning and prevalence using GIS.
Freitas (2013) stated that the results of the mapping showed that high risk areas accounted for a total of 35.42% and tended to decrease with increases of 1 ° C to 5 ° C in temperature to 33.84%. The zoning map showed that 52.24% of the state's areas were in areas considered suitable for the development of the disease. The elegant combination of maps generated by zoning and prevalence showed a higher prevalence in the municipalities located in the South. Thus, it was evident that epidemiological data allied to GIS can be considered a valuable tool for decision making aimed at minimizing and prioritize strategies for the prevention and control of fascioliasis in Espírito Santo.
The epidemiological studies carried out in cattle by Freitas (2013) and Bennema et al. (2017) are extremely important for a better description and understanding of the biological cycle of human fascioliasis in Ilhéus, since there is a predictable and measurable risk that fascioliasis has crossed the southern border of the State of Bahia. Martins (2012) states that although bovine fascioliasis has a recent incidence in the south of Espírito Santo, there are reports of bovine mortality by Fasciola also in the north of the state. As the states of the Espírito Santo and Minas Gerais border the extreme south of Bahia and that in both states there are cases of bovine fascioliasis, the risk that infected animals have entered the region of Ilhéus, or even infected people, is a a probable hypothesis that can be confirmed.
Other authors have shown that intestinal parasitoses were strongly associated with the socioeconomic status of the population, thus allowing identification of socially vulnerable areas. The geospatial distribution by GIS of the detected intestinal parasitic infections were not random or homogeneous, but significantly influenced by socioeconomic conditions, since participants classified in higher levels of deprivation had a higher risk of having intestinal parasites (Faria et al., 2017). Data on the education of Teotônio Vilela's population indicates that almost 15% of the population (15 years of age or older) are not literate, suggesting that the population may not recognize, from a cognitive point of view, the risks they are exposed to contact with the waters of rivers, streams and sewage. The analysis of socio-sanitary indicators shows unfavorable conditions, since sanitation and garbage collection services are not done in their entirety in the proper way, causing residents to seek alternatives that increase their exposure to risk factors, use of river water for consumption and personal hygiene. The investigation of the epidemiological profile of biohelminthiases in the region under study was fundamental for the knowledge of the mode of distribution, its evolution and the development of interventions necessary for its prevention. Based on the results presented in this dissertation it is possible to affirm that the prevalence ranged from 3, 87% (6/155) in 2014 to 2.08% (1/48) in 2016 in relation to cases of human fascioliasis diagnosed in Ilhéus, confirming earlier findings (Santos, 1967). Despite the innovative nature of this research, using georeferencing and geoprocessing resources associated with laboratory diagnostics and environmental conditions, methodological fragility is recognized, given the small sample size considered. In addition, a detailed evaluation of climatic conditions during the period of the study, in addition to the use of diagnostic techniques, using immunoenzymatic methods and imaging tests would be opportune for a better clinical characterization of the diagnosed volunteers.
4 CONCLUSION
This study demonstrated the presence of intermediate hosts of the genus Lymnaea that can transmit fascioliasis in regions where cases were diagnosed in the Teotônio Vilela, Ilhéus, Bahia. In addition, it was observed that climatic and sociodemographic conditions of the investigated areas, especially in Area 01 and 03, contribute to the transmission of enteroparasitoses, as observed by other authors in other places with similar characteristics. The anthropogenic alterations, especially the unplanned garbage
disposal and debris mobilization in the floodplain areas revealed by the geospatial analysis, indicated that the alteration of the terrain altimetry of the Area 01 interfered in the pattern of flooding and the spatial distribution of the intermediate hosts in consecutive years.
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