Matias Szabo
Universidade Federal de Uberlândia, Pathology, Faculty Member
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This study addresses a meta-analysis of the distribution of Rickettsia spp. in the Neotropical region, as well as their associations with ticks and vertebrates. A total of 219 published reports on Rickettsia in ticks in the target region... more
This study addresses a meta-analysis of the distribution of Rickettsia spp. in the Neotropical region, as well as their associations with ticks and vertebrates. A total of 219 published reports on Rickettsia in ticks in the target region were compiled, providing 599 records of 31 species of Rickettsia recorded in 50 species of Ixodidae. The aim is to capture the phylogenetic relationships between rickettsiae and the ticks carrying them in the target region, with a focus on the co-speciation ticks-rickettsiae. We compared the phylogeny of ticks, the records of rickettsiae, the environmental gradients colonized by ticks and the effect of the phylogenetic composition of vertebrates feeding ticks on the detection of Rickettsia in ticks. Results show that differences in rickettsial composition in ticks do not depend on the vertebrate's blood-source. This is the first time this result is demonstrated. This study pinpoints that some Neotropical rickettsial organisms are associated with well-defined phylogenetical clusters of ticks. Secondarily, and probably only in a few cases, rickettsiae share species of phylogenetically distant ticks distributed along a gradient of environmental traits in which the ticks overlap (i.e., the different strains of Rickettsia parkeri sensu lato). We outline the importance of some ticks that share hosts and habitat: these ticks may act as "bridges" for the circulation of rickettsial species. There are also many species of Rickettsia that have been detected so far in only one tick species, pointing to a tight relationship or to the lack of data preventing conclusions about the detection of these bacteria in other ticks. Two species, namely Rickettsia amblyommatis and Rickettsia bellii have been recorded in the majority of ticks in the region (mainly Amblyomma spp.) and seem to be not associated with definite tick species because they may be an essential symbiont of the ticks. We conclude that an adequate analysis of rickettsiae-ticks-habitat is necessary to address the human health issues derived from the infections by rickettsiae.
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We herein describe exposure and tick attachment to researchers and field staff within the greatest preserved inland Atlantic rainforest, located in Brazil, over a non-consecutive period of five years. Overall, 433 ticks from five species... more
We herein describe exposure and tick attachment to researchers and field staff within the greatest preserved inland Atlantic rainforest, located in Brazil, over a non-consecutive period of five years. Overall, 433 ticks from five species were collected, Amblyomma coelebs (n = 281), Amblyomma brasiliense (n = 79), Amblyomma incisum (n = 43), Amblyomma ovale (n = 4), Haemaphysalis juxtakochi (n = 4). Clusters of larvae belonged to the genus Amblyomma (n = 21) and Haemaphysalis (n = 1). Both Haemaphysalis and Amblyomma species were observed crawling on humans but only ticks from the latter genus were found attached. Most recovered ticks (59%) were found attached and, whereas A. brasiliense was the main host-seeking tick species in the forest, A. coelebs nymphs were the ones that overwhelmingly attached to humans (70% of all attachments). At the same time only 0.4% of human bites were of A. ovale, the Rickettsia parkeri strain Atlantic rainforest vector tick in Brazil. Tick attachment sites were recorded for 132 ticks and lower/upper limbs and the trunk were more parasitized than the head/neck. Tick bites were recorded throughout the year; while larvae did not show an evident seasonal pattern, nymphs attached to humans mainly in autumn and winter and the few adult bites were recorded in spring. Our results highlighted A. coelebs nymphs as major human-biters and evidenced the necessity of studies that discern human tick bites that occur after exposure to host-seeking ticks from those that occur after tick displacement from hosts that carry ticks to human dwellings.
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This expert opinion revisits the factors affecting the on- and off-host ecology of Rhipicephalus microplus in the context of climate change. It also highlights how the negative effects of heat stress caused by climate change on animal... more
This expert opinion revisits the factors affecting the on- and off-host ecology of Rhipicephalus microplus in the context of climate change. It also highlights how the negative effects of heat stress caused by climate change on animal welfare, productivity and health of cattle will likely become more of an issue in the future if the Earth's climate continues to warm as predicted.
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An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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Leptospirosis is a zoonotic disease of world importance, and its transmission depends on the interaction between humans and animals. Given the necessity to investigate potential hosts of Leptospira spp., this study verified the prevalence... more
Leptospirosis is a zoonotic disease of world importance, and its transmission depends on the interaction between humans and animals. Given the necessity to investigate potential hosts of Leptospira spp., this study verified the prevalence of different serovars in the species of Rhipidomys spp., a widespread sigmodont rodent in Brazil. The studied population originates from a semi-evergreen forest located in the county of Uberlândia, in the state of Minas Gerais. The microscopic agglutination test (MAT) was performed with 14 serovars. Thirteen out of the 43 wild rodents captured showed a positive agglutination reaction, with a greater prevalence of the serovars Pyrogenes, Copenhageni, and Canicola. This study found a prevalence of 30.3% anti-Leptospira spp. antibodies; all positive animals were reactive to more than one serovar.
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M. B. Castro, DVM, MS, M. P. J. Szab6, DVM, PhD, Veterinary Pathology Diagnostic Service, M. A. Romano, DVM, PhD, Veterinary Reproduction Service, University of Franca, Av Dr Armando Salles de Oliveira 201, CEP 14404-600, Franca, SP,... more
M. B. Castro, DVM, MS, M. P. J. Szab6, DVM, PhD, Veterinary Pathology Diagnostic Service, M. A. Romano, DVM, PhD, Veterinary Reproduction Service, University of Franca, Av Dr Armando Salles de Oliveira 201, CEP 14404-600, Franca, SP, Brazil H. K. Hokamura, DVM, PhD, Veterinary Radiology Service, Bandeirantes University, Sao Paulo, Brazil PEROSOMUS elumbis is a rare congenital anomaly of unknown aetiology. It is characterised by a series of malformations, which include agenesis of vertebrae and the lumbar segment of the spinal cord. Arthrogrypotic hindlegs, associated with muscle malformation, are also frequently seen (Hiraga and Abe 1987, Jubb and Huxtable 1993, Jones 1999). This partial agenesis of the spinal cord and the lack of vertebrae in the lumbar, sacral and coccygeal regions lead to the shortening of the animal's body and atrophy of its posterior end, especially the hindlimbs (Kitt and others 1954). Perosomus elumbis has been previously described in Holstein-Friesian calves (Jones 1999), sheep (Dennis 1975) and pigs (Kitt and others 1954). Ingestion of the plant Veratrum californicum by Merino sheep has been considered as one of the causes of this malformation in their offspring (Dennis 1975). This short communication describes a case of perosomus elumbis in a two-day-old female Holstein-Friesian calf which was presented to Franca University Veterinary Hospital, Sao Paulo, Brazil, in March 2001. The animal was dead on presentation and presented with atrophy and paralysis of the hindlimbs, arthrogryposis, a laterally dislocated anus and vulva, and its tail was absent (Fig 1). Radiological examination of the vertebral axis revealed the presence of only two lumbar vertebrae and a severe conformational deformity of the calf's body in that region. The diameter of the vertebral conduit was reduced and dislodged from its dorsoventral axis, and injected contrast medium comprising 30 ml of lohexol (Omnipaque; Searle) (300 mg I/ml) did not fill the vertebral canal at the level of the lumbar vertebrae. At postmortem examination, apart from the external morphological malformations described above, severe atrophy of the distal portions of the lumbar muscles and of the hindlimbs was observed. Examination of the pelvis revealed that the pubic bone was absent, as were the sacral and coccygeal vertebrae. The lumbar segment of the incomplete vertebral axis ended abruptly (Fig 2). The animal's hindquarters were linked to the rest of its body only by soft tissues. The caudal portion of the spinal cord ended in a structure morphologically similar to the medullary cone, but the cauda equina was absent. The adjacent dura mater was quite fibrous and thickened, and was continuous to an anomalous fibrocartilaginous structure of approximately 1 x 2 cm. Fragments of spinal cord were collected and fixed in 10 per cent buffered formalin (pH 7-0) for miscroscopic examination. Paraffinembedded sections at 5 Mim were stained with haematoxylin and eosin. Histopathological examination of the spinal cord revealed myelodysplasia with malformation of the grey matter and abnormal multiplicity of the central canal. Perosomus elumbis is a rare disorder among cattle. To the authors' knowledge, the malformation has not been previously reported in Brazil. Its aetiology is unknown and it represents less than 1 per cent of the observed congenital malformations in the species. Congenital defects can occur as a result of aberrations in the complex transition from the embryonic to the fetal phase of development. Malformation or improper migration of the neural tube during the tail-bud stage, accompanied by partial agenesis of the caudal spinal cord, may be the cause of this abnormality (Jones 1999). Another possible explanation is that it may result from nonclosure of the neural tube near the middle of the neural tube FIG 1: Atrophy of the hindlimbs, arthrogryposis and absence of the tail of a two-day-old Holstein-Friesian calf with perosomus elumbis
Research Interests: Brazil, Medicine, Female, Animals, Cattle, and 3 moreVeterinary Sciences, lumbar vertebrae, and Arthrogryposis
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Basic knowledge of species, ecological preferences and behavior of ticks in preserved rainforests are scanty. We herein describe species richness, seasonal activity, altitude influence and questing height of ticks along 3375 m of animal... more
Basic knowledge of species, ecological preferences and behavior of ticks in preserved rainforests are scanty. We herein describe species richness, seasonal activity, altitude influence and questing height of ticks along 3375 m of animal trails within the largest remain of inland Atlantic rainforest in Brazil, the Iguaçu National Park (INP). Altogether, 2954 ticks from nine tick species were collected; Amblyomma brasiliense Aragão (49.09% of the specimens), Amblyomma coelebs Neumann (29.08%), Amblyomma incisum Neumann (12.49%), Haemaphysalis juxtakochi Cooley (5.21%), Amblyomma ovale Koch (2.64%), Amblyomma longirostre Koch (0.20%), Ixodes fuscipes Fonseca (0.17%), Ixodes loricatus Neumann (0.07%) and Amblyomma dubitatum Neumann (0.03%) (Ixodida: Ixodidae). There was an evident seasonal influence on tick host-questing activity, with each tick stage prevailing in a season before the following one, and a general trend of one tick generation per year. Adult tick questing height mode on vegetation showed a correspondence between tick species and preferred host size and height. Adult ticks quested higher than immatures, but several larval clusters were found high enough to seek for large-sized hosts as well. Nymphal and adult tick questing height increased significantly at higher altitudes within the park. Amblyomma incisum and A. coelebs were more abundant at higher and lower altitudes, respectively. The knowledge on tick species richness, ecological preferences and behavior herein obtained provides baseline information to understand tick-borne disease epidemiology occurring at landscapes under a strong anthropogenic impact.
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Rickettsia rickettsii infection causes the highest human fatality rate among all Rickettsia species of the world and is endemic in Southeast Brazil. In this part of the country most human spotted fever cases are related to unnaturally... more
Rickettsia rickettsii infection causes the highest human fatality rate among all Rickettsia species of the world and is endemic in Southeast Brazil. In this part of the country most human spotted fever cases are related to unnaturally high populations of ticks, usually a mix of two species, Amblyomma dubitatum Neumann and Amblyomma sculptum Berlese and their local host, capybara ( Hydrochoerus hydrochaeris ). At the same time, an increase in the number of SF notifications as well as its urbanization was observed, and a better characterization of disease epidemiology is mandatory for control measures and to halt its expansion. It was recently noticed in southeast Brazil that SF endemic areas were characterized by overgrowth populations of A. sculptum and decreased populations of A. dubitatum . Hence, characterization of areas with potential to endemicity, eco-epidemiological studies and control measures may rely on the evaluation of A. sculptum / A. dubitatum rate. However, in potentially endemic scenarios, discriminating the two tick species, particularly the nymphs considered the main vector stage, is a challenge in face of several hundreds to thousands of ticks that should be examined for quantitative studies. We herein present additional morphological features to an existing identification key for Amblyomma nymphs that considerably diminishes the labor to distinguish nymphs of these two tick species. Specifically, the oval-shaped scutum of A. dubitatum and a conspicuous scapula of A. sculptum are prominent discriminating features.
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Abstract We evaluated the role of communities of small mammals from three distinct areas in a region of Cerrado mixed with Atlantic Forest remains for maintenance of tick fauna. Thirty-nine marsupials (Gracilinanus agilis, n = 34; Marmosa... more
Abstract We evaluated the role of communities of small mammals from three distinct areas in a region of Cerrado mixed with Atlantic Forest remains for maintenance of tick fauna. Thirty-nine marsupials (Gracilinanus agilis, n = 34; Marmosa paraguaiana, n = 4; Didelphis albiventris, n = 1) and 33 rodents (Oecomys cleberi, n = 10; Nectomys squamipes, n = 4; Calomys tener, n = 4; Hylaeamys megacephalus, n = 4; Akodon sp., n = 3; Rattus rattus, n = 3; Cerradomys subflavus, n = 2; Mus musculus, n = 2; Rhipidomys macrurus, n = 1) were captured. Solely G. agilis and the four rodent species (N. squamipes, R. macrurus, C. subflavus and Akodon sp.) were infested. Four tick species were collected (Amblyomma dubitatum, Amblyomma sculptum, Ixodes loricatus and Ornithodoros mimon). A. dubitatum was the most abundant tick species on hosts. Capture success was higher in the dry season, but the infestation was similar in both seasons. Forested habitats, particularly riparian forests, resulted in higher number of hosts and ticks collected (from hosts and from vegetation), compared to pastures and anthropized sites. The association between C. subflavus and I. loricatus and between A. dubitatum and N. squamipes observed here is the first recorded in Cerrado biome. Areas with more patches of forest, including the Atlantic Forest fragments, tend to present a richest community of small mammals and associated ticks.
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Research Interests: Zoology, Veterinary Medicine, Biology, Brazil, Medicine, and 15 moreWildlife Diseases, Phylogeny, Deer, Female, Animals, Male, Polymerase Chain Reaction, National Park, Prevalence, Mycoplasma, Phylogenetic Tree, Veterinary Sciences, Species Specificity, Amino Acid Sequence, and Molecular Sequence Data
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This work investigated microorganisms responsible for the contamination and death of ticks from natural reserves and wild animals and later kept in the Laboratory of Ixodology in the Veterinary School of the Federal University of... more
This work investigated microorganisms responsible for the contamination and death of ticks from natural reserves and wild animals and later kept in the Laboratory of Ixodology in the Veterinary School of the Federal University of Uberlândia. Such investigation aimed prevention of tick death in the laboratory but also search for microorganisms to be used in the biological control of ticks. From four tick samples of Amblyomma genus, the following agents were isolated: Staphylococus sp, Gram positive bacillus, filamentous fungi of the genera Aspergillus and Penicillium , and a yeast identified as Non- albicans Candida and Cryptococcus sp. Even though the source of contamination of these ticks is uncertain, this study displayed the necessity of to better evaluating the spread of pathogens by ticks, as well as those known to be transmitted solely during tick feeding.
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We studied communities of small mammals and their ticks in endemic (E) and non-endemic (NE) areas for Brazilian spotted fever (BSF), aiming to infer if diversity parameters of parasites and hosts could be related to occurrence and... more
We studied communities of small mammals and their ticks in endemic (E) and non-endemic (NE) areas for Brazilian spotted fever (BSF), aiming to infer if diversity parameters of parasites and hosts could be related to occurrence and prevalence of rickettsial infection, especially Rickettsia rickettsii. We compared E and NE areas in human-modified landscapes (HMLs) and natural areas (BIO) with no report of BSF cases. Composition and equitability were important components of diversity explaining differences among areas. The marsupial Didelphis albiventris was dominant in HMLs, but not in natural areas, and this opossum was the main host for the tick Amblyomma sculptum, principal vector of R. rickettsii, especially in E areas. Communities of ticks were dominated by A. sculptum, followed by Amblyomma dubitatum in E areas. In NE areas, this dominance was inverted, with more A. dubitatum than A. sculptum infesting small mammals, but the numbers of ticks were much lower than in E areas. Composition and abundance of ticks in natural areas were very dissimilar from HMLs, with the lowest tick burdens. Didelphis albiventris in E areas presented higher seroprevalence and endpoint titres against R. rickettsii than in other areas. At least three Rickettsia species, non-pathogenic to humans, were detected in natural areas (Rickettsia bellii, Rickettsia amblyommatis and 'Candidatus Rickettsia andeanae'), and only one non-pathogenic species in HMLs (R. bellii). Our results suggest that higher diversity of ticks, hosts and rickettsiae could be relevant factors in buffering the effect in BSF occurrence. Particularly for D. albiventris, its importance has to be quantified in further studies considering the epidemiological scenario of BSF.
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The objective of this work was to evaluate the relationship between the populations of the ticks Amblyomma triste Koch, 1844, Rhipicephalus microplus (Canestrini, 1888), Amblyomma sculptum Berlese, 1888, the pathogenic bacteria Rickettsia... more
The objective of this work was to evaluate the relationship between the populations of the ticks Amblyomma triste Koch, 1844, Rhipicephalus microplus (Canestrini, 1888), Amblyomma sculptum Berlese, 1888, the pathogenic bacteria Rickettsia parkeri and a marsh deer (Blastocerus dichotomus) population after its removal from a pristine environment. For this purpose, ticks were collected from the cervical region of deer at the Marsh Deer Conservation Center in Promissão, São Paulo State, Brazil for nine consecutive years (2000 - 2008). Deer in captivity at the Center were kept in 2,000 m² paddocks surrounded by two-meter-high fences in the Tiete-river marsh. In total, 1,012 ticks of 26 deer were collected. Prevalence of the species A. triste among tick-infested hosts was the highest in the first triennium but decreased to the second and further to the third triennium. In contrast, the R. microplus prevalence amidst infested host population, increased from the first to the third triennium and was the species that attained the highest infestation intensity. Amblyomma sculptum was the tick with the lowest infestation prevalence and intensity throughout the period. The change in the proportion between the two most prevalent species was attributed to the new environment, specifically its restricted size and within it a dry area more suitable for R. microplus. DNA of 424 ticks processed in 276 pools was tested for Rickettsia genetic material by polymerase chain reactions (PCR). Twenty samples of the study were positive for the rickettsial gltA gene. Of these, 18 were from A. triste ticks and revealed the presence of the ompA spotted fever group gene as well. Eleven samples were sequenced and showed 100% identity with R. parkeri sensu stricto. Two samples from R. microplus did not amplify ompA gene neither yielded product in a PCR specific for Rickettsia bellii. Sequencing of the gltA gene in the DNA of these two ticks was also 100% identical with R. parkeri s.s. In conclusion, the changes in the deer environment modified the tick populations but maintained, at least temporary, R. parkeri bacteria in A. triste ticks. Rhipicephalus microplus was refractory to the R. parkeri infection and bacterial DNA in this tick species indicated DNA spill over from other tick species. It was demonstrated that captive marsh deer may sustain cattle tick populations on its own. This would hardly occur under pristine conditions because of the inadequacy the marsh deer´s naturally humid habitat for the cattle tick. However, deer transportations of R. microplus ticks from one farm to another may occur whenever habitat loss pushes this wild animal towards farms.
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Rondônia is the only state in the North Region of Brazil to have registered confirmed cases of Brazilian Spotted Fever (BSF). The present study investigated the epidemiological cycle of Rickettsia spp. by surveying free-living ixodofauna... more
Rondônia is the only state in the North Region of Brazil to have registered confirmed cases of Brazilian Spotted Fever (BSF). The present study investigated the epidemiological cycle of Rickettsia spp. by surveying free-living ixodofauna and tick parasitism of dogs in the municipality of Porto Velho, Rondônia State. Ticks and dogs were tested for the presence of Rickettsia spp. DNA and dog serum was tested for reactivity to anti-Rickettsia spp. antibodies. Tick collection and dog blood sampling were performed in peri-urban and rural environments at 11 locations. Eight free-living Amblyomma species and one Haemaphysalis species were collected: A. scalpturatum, A. naponense, A. oblongoguttatum, A. coelebs, A. latepunctatum, A. pacae, A. ovale, Amblyomma sp., and H. juxtakochi. Three tick species were found parasitizing dogs: Rhipicephalus sanguineus sensu lato, A. oblongoguttatum and A. ovale. Molecular analysis did not identify the presence of the gltA gene fragment in any tick specimen. Results from an indirect immunofluorescent assay (IFA) showed that 20.8% of peri-urban and 15.4% of rural dog sera exhibited reactivity to Rickettsia rhipicephali, Rickettsia amblyommatis, Rickettsia bellii and Rickettsia parkeri antigens. Antibody prevalence in dogs was 16.4%. This study is the first to describe the prevalence of Rickettsia spp. infection in dogs from Porto Velho municipality. Our findings enhance current knowledge of Rickettsia spp. circulation in the Western Amazon.
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Human activities are changing landscape structure and function globally, affecting wildlife space use, and ultimately increasing human-wildlife conflicts and zoonotic disease spread. Capybara (Hydrochoerus hydrochaeris) is a conflict... more
Human activities are changing landscape structure and function globally, affecting wildlife space use, and ultimately increasing human-wildlife conflicts and zoonotic disease spread. Capybara (Hydrochoerus hydrochaeris) is a conflict species that has been implicated in the spread and amplification of the most lethal tick-borne disease in the world, the Brazilian spotted fever (BSF). Even though essential to understand the link between capybaras, ticks and the BSF, many knowledge gaps still exist regarding the effects of human disturbance in capybara space use. Here, we analyzed diurnal and nocturnal habitat selection strategies of capybaras across natural and human-modified landscapes using resource selection functions (RSF). Selection for forested habitats was high across human- modified landscapes, mainly during day- periods. Across natural landscapes, capybaras avoided forests during both day- and night periods. Water was consistently selected across both landscapes, during day- ...