The pathology of schistosomiasis mansoni, a neglected tropical disease of great clinical and socioeconomic importance, results from the parasite eggs that become trapped in host tissues, particularly in the liver and intestines. Continuous antigenic stimulation from these eggs leads to recruitment of inflammatory cells to the sites of infection with formation of periovular granulomas. These complex structures have variable size and composition and are the most striking histopathological feature of schistosomiasis mansoni. However, evaluation of granulomas by conventional microscopy methods is time-consuming and limited, especially in large-scale studies. Here, we used high resolution Whole Slide Imaging (WSI), which allows fast scanning of entire histological slides, and multiple morphometric evaluations, to assess the granulomatous response elicited in target organs (liver, small and large intestines) of two models of schistosomiasis mansoni. One of the advantages of WSI, also termed virtual microscopy, is that it generates images that simultaneously offer high resolution and a wide field of observation. By using a model of natural (Nectomys squamipes, a wild reservoir captured from endemic areas in Brazil) and experimental (Swiss mouse) infection with Schistosoma mansoni, we provided the first detailed WSI characterization of granulomas and other pathological aspects. WSI and quantitative analyses enabled a fast and reliable assessment of the number, evolutional types, frequency and areas of granulomas and inflammatory infiltrates and revealed that target organs are differentially impacted by inflammatory responses in the natural and experimental infections. Remarkably, high-resolution analysis of individual eosinophils, key cells elicited by this helminthic infection, showed a great difference in eosinophil numbers between the two infections. Moreover, features such as the intestinal egg path and confluent granulomas were uncovered. Thus, WSI may be a suitable tool for detailed and precise histological analysis of granulomas and other pathological aspects for clinical and research studies of schistosomiasis.
Schistosomiasis is a neglected tropical disease of a significant public health impact. The water rat Nectomys squamipes is one of the most important non-human hosts in the schistosomiasis mansoni transmission in Brazil, being considered a wild reservoir. Cellular mechanisms that contribute to the physiological adaptation of this rodent to the Schistosoma mansoni parasite are poorly understood. Here we identified, for the first time, that a hepatic steatosis, a condition characterized by excessive lipid accumulation with formation of lipid droplets (LDs) within hepatocytes, occurs in response to the natural S. mansoni infection of N. squamipes, captured in an endemic region. Significant increases of LD area in the hepatic tissue and LD numbers/hepatocyte, detected by quantitative histopathological and ultrastructural analyses, were paralleled by increased serum profile (total cholesterol and triglycerides) in infected compared to uninfected animals. Raman spectroscopy showed high content of polyunsaturated fatty acids (PUFAs) in the liver of both groups. MALDI-TOFF mass spectroscopy revealed an amplified pool of omega-6 PUFA arachidonic acid in the liver of infected animals. Assessment of liver functional activity by the levels of hepatic transaminases (ALT and AST) did not detect any alteration during the natural infection. In summary, this work demonstrates that the natural infection of the wild reservoir N. squamipes with S. mansoni elicits hepatic steatosis in the absence of liver functional harm and that accumulation of lipids, markedly PUFAs, coexists with low occurrence of inflammatory granulomatous processes, suggesting that lipid stores may be acting as a protective mechanism for dealing with the infection.
Rattus norvegicus has attracted much attention because of its role as a reservoir of zoonotic pathogens. This work aimed to identify the intestinal helminth species in R. norvegicus and to analyse the effects of temperature, rainfall, host age and sex on the helminth community structure. Moreover, this study investigated the possible associations among helminth species in an urban population of R. norvegicus in São Gonçalo, Rio de Janeiro, sampled during the rainy and dry seasons over a span of 2 years. A total of 112 rats were infected by six species of helminths. The nematode Nippostrongylus brasiliensis was the most prevalent and abundant species, with high mean intensity in both seasons, followed by Strongyloides venezuelensis, Heterakis spumosa, Raillietina sp., Hymenolepis nana and Moniliformis moniliformis. Co-occurrence was found between N. brasiliensis and S. venezuelensis and between N. brasiliensis and H. spumosa. The occurrence of S. venezuelensis was related to rainfall. The understanding of the helminth community structure in this synanthropic rat provides basic information on parasites of public health importance, as two helminth species (H. nana and M. moniliformis) recovered from rats in the urban area studied can infect humans.
Small mammals are found naturally infected by Schistosoma mansoni, becoming a confounding factor for control programs of schistosomiasis in endemic areas. The aims of this study were: to investigate the infection rates by S. mansoni on the water-rat Nectomys squamipes during four years in endemic areas of Sumidouro, state of Rio de Janeiro, using mark-recapture technique; to compare two diagnostic methods for schistosomiasis; and to evaluate the effects of the chemotherapy in the human infected population on the rodent infection rates. The rodent infection rates of S. mansoni increased when rodent population sizes were lower. Coprology and serology results presented the same trends along time and were correlated. Serology could detect recent infection, including the false negatives in the coprology. The chemotherapy in the humans could not interrupt the rodent infection. Rodents can increase the schistosomiaisis transmission where it already exists, they probably maintain the transmission cycle in the nature and can be considered as biological indicators of the transmission sites of this parasite since they are highly susceptible to infection. The water-rats may present different levels of importance in the transmission dynamics of S. mansoni infection cycle for each area, and can be considered important wild-reservoirs of this human disease.Key words: diagnostic methods -population ecology -rodents -schistosomiasis Small mammals are found naturally infected by Schistosoma mansoni, becoming a confounding factor for control programs of schistosomiasis in endemic areas (Barbosa et al. 1958, Antunes et al. 1971, Rey 1993. Among the extra-human definitive hosts of this parasite, rodents of the genera Nectomys and Holochilus are the most probable wild reservoirs taking into account: (1) their semiaquatic habits (Ernest & Mares 1986), which make them highly exposed to infection; (2) their wide geographic distribution (Bonvicino 1994) coincident with the distribution of schistosomiasis in Brazil; (3) presence of infected individuals in most of the endemic areas where they were investigated, despite of the low human prevalence -rodents frequently showing higher infection rates in relation to human populations (Rey 1993); (4) rodent tolerance to human presence, occurring near human dwellings. Several experimental studies also support the hypothesis that water-rats are probable wild reservoirs of S. mansoni, showing high susceptibility to infection (Borda 1972, Souza et al. 1992, Maldonado Jr. et al. 1994, Ribeiro et al. 1998, somatic development hypertrophy of adult worms , elimination of viable eggs with high infectivity potential (Picot 1992), high infection persistence , low pathogenicity with efficient peri-ovular modulation and low tissue aggression (Silva & Andrade 1989), and ability to close the transmission cycle in semi-natural conditions (Antunes et al. 1973, Carvalho et al. 1976, Kawazoe & Pinto 1983. Infection of small mammals other than Nectomys and Holochilus by S. mansoni occurs only occasionally, especial...
ABSTRACT. The Atlantic Forest is one of the most disturbed Brazilian biomes, with 183 out of 298 species of mammals occurring in the state of Rio de Janeiro. In this study, we aimed to characterize the diversity, community structure, and habitat use of small mammals in the FIOCRUZ Atlantic Forest Campus (CFMA), including areas of Pedra Branca State Park (PBSP, subunit Pau da Fome), state of Rio de Janeiro. We also compared species diversity and composition between two moments 15 years apart (2001 and 2012-2015) and analyzed the population dynamics of the marsupial Didelphis aurita (Wied-Neuwied, 1826). Small mammal captures were made in different habitats: sylvatic-urban interface areas near human dwellings, disturbed forest, and preserved forest areas. Five marsupial species and four rodent species were captured in both periods. There was a reduction in species richness and β diversity between the two periods, indicating that disturbances in the environment over the years may have affected the small mammal community structure. The most altered environment showed the greatest species richness and abundance, while the forest areas showed the smallest values, which may be explained by the loss of mammal species, mainly specialist species in forested areas. We identified three groups of species according to habitat preferences: one related to environments with a higher density of vegetation in upper strata -Marmosa paraguayana (Tate, 1931) and Monodelphis americana (Müller, 1776), another related to a higher density in lower forest strata -Akodon cursor (Winge, 1887), and another with no association with the investigated habitat variables -D. aurita and Oligoryzomys nigripes (Olfers, 1818). The small mammal community structure showed a low level of nestedness in both sampling periods. This study is the first report to evaluate the community structure of small mammals in the sylvatic-urban interface area of Pedra Branca State Park, the largest forest reserve within an urban area in Brazil. The surveys indicate that the small mammal diversity was low in both sampling periods and in both areas, and a species loss in the Pau da Fome locality was observed, despite it is a conservation unit. The greater species abundance and richness in the most disturbed areas suggest an increase of factors favoring the occurrence of synanthropic and opportunistic species.
Among the Brazilian marsupials, the species of the genus Didelphis are the most parasitized by helminths. This study aimed to describe the species composition and to analyse the helminth communities of the Atlantic Forest common opossum Didelphis aurita at infracommunity and component community levels using the Elements of Metacommunity Structure Analysis, considering peri-urban, sylvatic and rural environments in the state of Rio de Janeiro, Brazil. Seventy-three specimens of D. aurita were captured during the study. Fourteen species of helminths were collected: nine of the phylum Nematoda (Trichuris minuta, Trichuris didelphis, Globocephalus marsupialis, Heterostrongylus heterostrongylus, Travassostrongylus orloffi, Viannaia hamata, Aspidodera raillieti, Cruzia tentaculata and Turgida turgida); four of the phylum Platyhelminthes (three species of Trematoda, Duboisiella proloba, Brachylaima advena and Rhopalias coronatus, and one species of the class Cestoda); and one species of the phylum Acanthocephala (Oligacanthorhynchus microcephalus). More than 95% of the animals were infected with parasites. The most abundant parasite species were V. hamata, T. turgida, C. tentaculata and T. orloffi. The nematodes T. turgida, C. tentaculata and A. raillieti were the most dominant species in the three environments. The analysis of the metacommunity structure indicated a structured pattern as a function of the environmental gradient, but only when all localities were considered together. At the infracommunity and component community levels, quasi-nested and nested structures with stochastic species loss were observed, respectively. The results indicate that the settlement of helminth species in the opossums can be attributed to the heterogeneity among individual hosts in relation to their exposure to parasites and to extrinsic factors, which vary among habitats, considering a regional scale. On a local scale, the characteristics of this host species may promote homogenization among individual hosts in terms of their exposure to the helminths. This study constitutes a new host record for the species G. marsupialis and T. didelphis and represents a pioneering investigation of the helminth metacommunity of a Neotropical marsupial.
Long-term monitoring of small mammal populations is very important to understand the variations in temporal abundance on a large time scale, which are related to ecological, economic and epidemiological phenomena. The aim of this study is to monitor the populations of the marsupials Didelphis aurita and Philander frenatus and the rodents Nectomys squamipes, Akodon cursor and Oligorysomys nigripes in a locality of typical Brazilian rural landscape, Sumidouro Municipality, Rio de Janeiro State, Brazil. A mark-recapture study was conducted during five years. We analyzed the population dynamics, the reproduction and age structure of these species. Both marsupials presented higher population sizes in the end of wet period and beginning of the dry period, which can be explained by the seasonal reproduction which begins in the middle of the dry period and ends in the last months of the wet period. N. squamipes reproduced throughout the year but mostly during rainy periods, due to the close association of this rodent to resources found in the water. Higher survivorship and recruitment rates were in the end of the wet season. The rodent A. cursor had an opportunist reproduction, resulting in high turnover rates. Survivorship increased with the effects of the dry periods. O. nigripes showed a clear annual pattern of population cycle with peaks during the dry season. The rodents did not show potential to present outbreaks and become agricultural pests. The annual population cycles of O. nigripes and the unique peak of A. cursor population during five years highlight attention to their importance as wild reservoirs of the hantavirus disease. Their ecological characteristics associated to their opportunistic behavior make these species prone to be good reservoirs of zoonoses.
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