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      Enteric parasitic infections in children and dogs in resource-poor communities in northeastern Brazil: Identifying priority prevention and control areas

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          Abstract

          The aim of this study was to determine the prevalence and risk factors of the main enteric parasitic infections that affect children and dogs in the municipality of Ilhéus, Bahia, Brazil; and to identify the geopolitical areas that should receive priority interventions to combat them. Between March and November 2016, fecal samples of 143 dogs and 193 children aged 1 month to 5 years were collected in 40 rural and semirural communities using a systematic sampling approach, stratified by district. Samples were collected by legal guardians of the children and / or dog owners. Eggs, larvae, cysts and oocysts of parasites were concentrated by centrifugal-flotation and centrifugal-sedimentation, and acid-resistant staining was used to visualize parasites. One hundred and thirty-two children (68.4%), 111 dogs (77.6%) and 199 (73.7%) dog fecal samples collected from streets were parasitized. Giardiasis, cryptosporidiosis, amoeba infections and hookworm were the most frequent infections in all studied populations, in addition to trichuriasis in dogs and ascaridiasis in children. A predominance of Giardia and hookworms was observed in children and dogs, respectively. The coastal districts of Aritaguá, Olivença and the main district had a higher parasitic diversity and overlapping of important potential zoonotic infections. Age over one year (p<0.001), adjusted OR = 3.65; 95% CI = 1.86–7.16) and income below the minimum monthly salary (p = 0.02, adjusted OR = 2.78, 95% CI = 1.17–6.59) were the main factors associated with intestinal parasitic infections in children and dogs, respectively. The coastal districts of Aritaguá and Olivença and the main district should be prioritized through enteric disease control programs, and the factors associated with infections must be considered in the design of health interventions in these districts. The integration between affirmative income actions and investments to improve the health infrastructure of these communities may work more effectively than current preventive measures to combat enteric parasites.

          Author summary

          The maintenance of high prevalence of enteric parasitic diseases in human and animal populations is an indisputable fact in the current scientific context. Despite all the advances in ecology, pathology, epidemiology and treatment, the control of these diseases remains ineffective and is a major problem in public health management. New control strategies should be tested in order to optimize the actions of current preventive programs and thus reduce prevalence. These strategies should include identification and mapping of geopolitical areas experiencing a greater frequency and overlap of enteric parasitic infections, and they must include the prevalence in both canine and human populations. This study indicates that poverty is strongly associated with the parasite's frequency. In a One Health approach, it demonstrates that affirmative actions of citizenship and income can be preventive health measures, and it also demonstrates the areas in which deworming actions must be a priority through control actions based on risk.

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          Most cited references39

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          Zoonotic potential and molecular epidemiology of Giardia species and giardiasis.

          Molecular diagnostic tools have been used recently in assessing the taxonomy, zoonotic potential, and transmission of Giardia species and giardiasis in humans and animals. The results of these studies have firmly established giardiasis as a zoonotic disease, although host adaptation at the genotype and subtype levels has reduced the likelihood of zoonotic transmission. These studies have also identified variations in the distribution of Giardia duodenalis genotypes among geographic areas and between domestic and wild ruminants and differences in clinical manifestations and outbreak potentials of assemblages A and B. Nevertheless, our efforts in characterizing the molecular epidemiology of giardiasis and the roles of various animals in the transmission of human giardiasis are compromised by the lack of case-control and longitudinal cohort studies and the sampling and testing of humans and animals living in the same community, the frequent occurrence of infections with mixed genotypes and subtypes, and the apparent heterozygosity at some genetic loci for some G. duodenalis genotypes. With the increased usage of multilocus genotyping tools, the development of next-generation subtyping tools, the integration of molecular analysis in epidemiological studies, and an improved understanding of the population genetics of G. duodenalis in humans and animals, we should soon have a better appreciation of the molecular epidemiology of giardiasis, the disease burden of zoonotic transmission, the taxonomy status and virulences of various G. duodenalis genotypes, and the ecology of environmental contamination.
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            Zoonotic potential of Giardia.

            Giardia duodenalis (syn. Giardia lamblia and Giardia intestinalis) is a common intestinal parasite of humans and mammals worldwide. Assessing the zoonotic transmission of the infection requires molecular characterization as there is considerable genetic variation within G. duodenalis. To date eight major genetic groups (assemblages) have been identified, two of which (A and B) are found in both humans and animals, whereas the remaining six (C to H) are host-specific and do not infect humans. Sequence-based surveys of single loci have identified a number of genetic variants (genotypes) within assemblages A and B in animal species, some of which may have zoonotic potential. Multi-locus typing data, however, has shown that in most cases, animals do not share identical multi-locus types with humans. Furthermore, interpretation of genotyping data is complicated by the presence of multiple alleles that generate "double peaks" in sequencing files from PCR products, and by the potential exchange of genetic material among isolates, which may account for the non-concordance in the assignment of isolates to specific assemblages. Therefore, a better understanding of the genetics of this parasite is required to allow the design of more sensitive and variable subtyping tools, that in turn may help unravel the complex epidemiology of this infection. Copyright © 2013. Published by Elsevier Ltd.
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              Human behaviour and the epidemiology of parasitic zoonoses.

              The behaviour of Homo sapiens has a pivotal role to play in the macro and microepidemiology of emerging or re-emerging parasitic zoonoses. Changing demographics and the concomitant alterations to the environment, climate, technology, land use and changes in human behavior, converge to favour the emergence and spread of parasitic zoonoses. The recent unprecedented movements of people, their animals and their parasites around the world, introduce and mix genes, cultural preferences, customs, and behavioral patterns. The increasing proclivity for eating meat, fish, crabs, shrimp, molluscs raw, undercooked, smoked, pickled or dried facilitates a number of protozoan (Toxoplasma), trematode (Fasciola sp., Paragonimus spp., Clonorchis sp., Opisthorchis spp., Heterophyes sp., Metagonimus sp., Echinostoma spp., Nanophyetus sp.) cestode (Taenia spp, Diphyllobothrum sp.) and nematode (Trichinella spp., Capillaria spp., Gnathostoma spp., Anisakis sp., Parastrongylus spp.) caused zoonoses. The increasing world population and the inability to keep pace with the provision of adequate sanitation and clean, safe drinking water, has led to an increased importance of waterborne zoonoses, such as those caused by Giardia, Cryptosporidium and Toxoplasma. Our close relationship with and the numerous uses to which we put companion animals and their ubiquitous distribution has resulted in dogs and cats unwitting participation in sharing over 60 parasite species including: Giardia, Cryptosporidium, Toxoplasma, most foodborne trematode species, Diphyllobothrum, Echinococcus spp., Ancylostoma and Toxocara. Changing human behaviour through education, to encourage the proper cooking of food, which may have cultural and social significance, will remain as challenging as controlling stray and feral pet populations, improving hygiene levels and the provision of safe drinking water and the proper use of sanctuary facilities. Long pre-patent periods and the normally insidious sub-clinical nature of most zoonoses makes advice requiring behavioural change for their control a difficult task. Our clearer understanding of the heterogeneity of susceptibility to infection, the complex genetic variations of people and parasite species and the development of molecular epidemiological tools is shedding more light on transmission routes and the spectrum of disease that is observed. Improved and new serological, molecular and imaging diagnostic tests and the development of broad spectrum chemotherapeutic agents has led to the attenuation of morbidity and mortality due to parasitic zoonoses in economically advantaged regions. Such advancements, in partnership with supportive behavioural change, has the potential for a sustainable global reduction in the burden of ill health due to parasitic zoonoses. Whether this will materialise is a challenge for us all.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draft
                Role: Formal analysis
                Role: Formal analysisRole: Writing – review & editing
                Role: Methodology
                Role: Formal analysis
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                9 June 2020
                June 2020
                : 14
                : 6
                : e0008378
                Affiliations
                [1 ] Departamento de Ciências Agrárias e Ambientais, Programa de Pós-Graduação em Ciência Animal, Universidade Estadual de Santa Cruz—UESC, Ilhéus, Bahia, Brasil
                [2 ] Department of Public Health & Community Medicine, School of Medicine, Tufts University, Boston, Massachusetts, United States of América
                [3 ] Departamento de Medicina Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo–USP, São Paulo, São Paulo, Brasil
                [4 ] Departamento de Ciências Agrárias e Ambientais, Faculdade de Medicina Veterinária, Universidade Estadual de Santa Cruz—UESC, Ilhéus, Bahia, Brasil
                [5 ] Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz -UESC, Ilhéus, Bahia, Brasil
                [6 ] Departamento de Medicina Veterinária, Universidade Federal de Lavras—UFLA, Lavras, Minas Gerais, Brasil
                [7 ] Departamento de Apoio, Produção e Saúde Animal, Universidade Estadual Paulista, Faculdade de Medicina Veterinária, Araçatuba, SP, Brasil
                University of Queensland School of Veterinary Science, AUSTRALIA
                Author notes

                The authors have declared that no competing interests exist.

                [¤]

                Current address: Departamento de Ciências Agrárias e Ambientais, Programa de Pós-Graduação em Ciência Animal, Universidade Estadual de Santa Cruz—UESC, Ilhéus, Bahia, Brasil

                ‡ ADPS and CMBMDR also contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-8118-7713
                Article
                PNTD-D-19-01494
                10.1371/journal.pntd.0008378
                7282628
                32516309
                c4d10c1f-367a-4de6-9700-bacdef406de8
                © 2020 Harvey et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 September 2019
                : 8 May 2020
                Page count
                Figures: 3, Tables: 5, Pages: 19
                Funding
                This investigation was supported in part by the Coordination for the Improvement of Higher Education Personnel – CAPES ( www.capes.gov.br) - Finance Code 001 and by the Bahia Research Foundation (FAPESB) – (APP0043/2016). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Medicine and Health Sciences
                Parasitic Diseases
                Medicine and Health Sciences
                Parasitic Diseases
                Parasitic Intestinal Diseases
                Medicine and Health Sciences
                Health Care
                Socioeconomic Aspects of Health
                Medicine and Health Sciences
                Public and Occupational Health
                Socioeconomic Aspects of Health
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                People and Places
                Population Groupings
                Age Groups
                Children
                People and Places
                Population Groupings
                Families
                Children
                People and places
                Geographical locations
                South America
                Brazil
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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