Volume 5 - 2024 | https://doi.org/10.3389/fitd.2024.1501710
This article is part of the Research TopicFoodborne Zoonotic Parasites and ParasitosesView all 5 articles
Background: Nematodes of the genus Trichinella are foodborne zoonotic pathogens that are widespread globally
These parasites have two epidemiological cycles
with the latter having wild carnivores as the main reservoirs of the parasite
have been increasingly detected in wild carnivores in Argentina and Chile
Although the disease is absent in domestic animals in Brazil
there is serological evidence that the agent is circulating in wild boars in some areas
This study aimed to diagnose Trichinella spp
infection through artificial tissue digestion and histopathology of selected tissues of wild carnivores from São Paulo state
and tongue) from 53 wild carnivores (21 Canidae
along with a retrospective study of the slide bank
considering samples from the period 2010 to 2021
totaling 89 free-living carnivores (42 Canidae
Results: Either artificial digestion or histopathological analyses did not reveal any larvae suggestive of Trichinella spp.
indicating that the nematode was not circulating within the target population
there is no direct evidence of nematode circulation in wild carnivores in the study area
studies in other South American countries are scarce or absent
hindering the proper comprehension of the epidemiology of human trichinellosis in this region
Considering the importance of wild carnivores in the epidemiology of trichinellosis
this study aimed to investigate Trichinella spp
infection in free-living wild carnivores in the state of São Paulo
03 Procyonidae) were collected from animals hit by cars on highways in 17 municipalities of São Paulo state
These carcasses were sent by the Environmental Police
Fire Brigade and highway concessionaires to the Wild Animal Pathology Service (SEPAS) at FCAV/Unesp Jaboticabal/SP
Santa Rita do Passa Quatro and Luis Antônio experimental stations of the São Paulo Forest Foundation
the “Quinzinho de Barros” Municipal Zoological Park and the Center for Wild Animal Medicine and Research (CEMPAS) - UNESP/FMVZ and kept in freezers at -20°C until processing
and tongue were taken for histopathological analysis and artificial digestion
histological slides were selected from 89 free-living wild carnivores (42 Canidae
02 Procyonidae) deposited in the collection of the Wild Animal Pathology Service (SEPAS) at FCAV/UNESP
Animals with histological sections of at least one of the abovementioned tissues were included in the study
These animals selected came from 39 municipalities in São Paulo and were necropsied between November 2010 and December 2021
The municipalities of origin of the animals studied are in Figure 1 showing the road killed animals’ origins and Figure 2 showing the slide bank samples’ origins. Table 1 compiles all the animals used in the study
Cities and species from São Paulo State where the road killed carcasses were obtained (Assis
Tambaú) between April 2022 and July 2023
Cities and species from São Paulo State where the slide bank carcasses were obtained (Araraquara
Uchôa and Vista Alegre do Alto) between November 2010 to December 2021
Species of carcasses and collection of slides of wild carnivorous mammals used in the study
Fifty grams of forearm, tongue and diaphragm muscles were collected (17, 18)
The samples were stored at -20°C in plastic bags labeled with the species
date and collection place until processing
a 1 cm3 fragment of these tissues was fixed in a 10% buffered formalin solution for histological processing
The tissue samples were subjected to the Artificial Digestion Technique (AD) based on the magnetic stirrer method according to European regulation EC 2075/2005
which is used for the surveillance of Trichinella spp
The samples (20 g) were crushed and digested using 400 ml of artificial digestive fluid (20 ml for each gram of muscle) consisting of 1% pepsin (1:10,000 US National Formulary) and 1% hydrochloric acid (HCl)
The digested tissue was stirred for 60 min or more at 44-46°C in a 600 ml glass beaker using a heated magnetic stirrer plate
the fluid was sieved through a 180 μm mesh sieve into the separatory funnel and left to stand for 30 minutes
40 ml of the sediment sample was quickly released from the funnel into a 50 ml beaker and sedimented again for 10 minutes
30 ml of supernatant was removed from the 50 ml beaker and the 10 ml of sediment was poured into a Petri dish
the 50 ml beaker was rinsed with 10 ml of water and the liquid was added to the Petri dish
The sample was analyzed under a stereomicroscope (Leica EZ4 HD
Leica Microsystems© Limited) at 15 to 40x magnification
The tissues collected after 24 to 48 hours in 10% phosphate-buffered formalin (pH 7.4) were processed according to routine
cut at 3μm and mounted on histological slides stained with hematoxylin and eosin
Readings were made using an Olympus BX-51® optical microscope equipped with a Q-color3® camera at 10x and 40x magnification
Another factor that makes it difficult to carry out serologies on the carcasses of animals that have been road killed is the coagulation and autolysis of the blood
Direct methods are more suitable for diagnosing Trichinella spp
using the carcasses of road killed animals is a non-invasive way of performing epidemiological surveillance of several pathogens
maximizing the use of biological samples and reducing the risk to both humans and animals
Despite not being the gold standard for diagnosing this nematode
histopathology is an alternative for confirming infection and diagnosis
Access to samples of wild carnivores, especially endangered animals protected by law, can be hampered by various factors. Therefore, the necropsy of carcasses of animals that have already died, as well as not interfering with conservation or causing stress to the animals, provides us with a lot of information (40)
It is possible to observe places of occurrence
among other ways of using them for educational purposes
It is also possible to monitor numerous diseases of human and animal importance
due to the logistics of the distance between the laboratory and the institutions that collected the carcasses
freezing is the best alternative of accessing a greater number and diversity of carnivore species
The epidemiological surveillance of trichinellosis in wild boars is already being carried out in Brazil, as these animals are important hosts for the nematode (46). Wild animals, especially carnivores, are natural hosts of Trichinella spp. and the parasite develops better in these animals than in domestic animals (39)
Given the way trichinellosis is transmitted and the fact that these animals are at the top of the food chain
epidemiological surveillance of wild carnivores and wild boars is essential to understanding the epidemiology of the disease in Brazil
there is no direct evidence of Trichinella spp
nematodes circulating in wild carnivores in São Paulo state
The original contributions presented in the study are included in the article/supplementary material
Further inquiries can be directed to the corresponding author
The animal study was approved by FCAV/Unesp Ethics Committee for the Use of Animals
The study was conducted in accordance with the local legislation and institutional requirements
All the procedures adopted in this study are in accordance with current international standards
This work was authorized by the Chico Mendes Institute for Biodiversity Conservation (ICMBio/Sisbio #82767-4)
by the Ethics Committee for the Use of Animals (CEUA) at UNESP/FCAV (proc
#2729/22) and by the Environmental Research Institute of the Secretariat for the Environment
Infrastructure and Logistics of the São Paulo State Government (#2180/2023)
The author(s) declare financial support was received for the research
Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Funding code 001 partially funded this study
EL is a researcher for CNPQ (National Council for Scientific and Technological Development); productivity grant no
Forestry Foundation (Experimental Station of: São Simão
Santa Rita do Passa Quatro and Luiz Antônio)
“Quinzinho de Barros” Municipal Zoological Park
Wild Animal Medicine and Research Center (CEMPAS) - UNESP/FMVZ
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest
The author(s) declare that no Generative AI was used in the creation of this manuscript
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations
Any product that may be evaluated in this article
or claim that may be made by its manufacturer
is not guaranteed or endorsed by the publisher
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Received: 25 September 2024; Accepted: 16 December 2024;Published: 07 January 2025
Copyright © 2025 Andrade, Perin, Arias-Pacheco, Amorim, Lefort, Pereira, Soares-Neto, Bordignon Fernandes, Oliveira, Ichikawa, da Costa, Ruffino, Werther and Lux Hoppe. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY)
distribution or reproduction in other forums is permitted
provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited
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distribution or reproduction is permitted which does not comply with these terms
*Correspondence: Estevam Guilherme Lux Hoppe, bHV4LmhvcHBlQHVuZXNwLmJy
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Mario Tomazello Filho 1 , Claudio S. Lisi 1 , Norbert Hansen 2
Wood samples of 41 tree species from seven different sites (Savanna and Atlantic forest) in the State of São Paulo were analysed macro- and microscopically for occurrence of increment zones
Distinct increment zones were found in Bombax grandiflorum Cav.
The anatomical features of increment zones of those nine species is described
increment zones were marked by thick-walled and radially flattened latewood versus thin-walled earlywood fibres
marginal parenchyma bands were found to mark the boundaries
Tree species with a ring-porous or semi-ring-porous structure could not be found within the 41 trees species investigated
Distinct increment zones could be found in all leaf-fall categories
the occurrence of distinct increment zones seems to be more common in deciduous and semi-deciduous tree species
Tree ring research on tropical species nowadays is a known field of research
the knowledge about the existence of annual tree rings in tropical trees
which was already found at the beginning of the last century
was ignored by many scientists for a long time (Worbes 1989)
During the last two to three decades different researchers doubtlessly demonstrated the existence of annual tree rings in many different tree species throughout the tropics (Vetter & Botosso 1989
it is also well known that tree ring analysis in the tropics is more difficult than in the temperated climate zones or in the boreal climate zone
From different investigations it is known that species with distinct increment zones can be found directly beside species with scarcely distinct or indistinct increment zones (Worbes 1999)
every tropical tree species has its own growth rhythm and reacts different to seasonal variations
The high variability of sites concerning climatic
edaphic and mechanic site factors and the complex anatomical structure of tropical woods are also reasons for the varying distinctness of increment zones
The periodicity of increment zones in tropical trees
which does not have to be annual (Alvim 1964
also makes tree ring analysis more difficult
The occurrence of distinct increment zones in tropical trees is the first prerequisite for tree ring anylsis
knowledge about the periodicity of the increment zones is absolutelly essentiell
Different methods to proof the annual periodicity of increment zones are described in Worbes (1995)
we investigated 41 tree species of different forests in the state of São Paulo
Aim of the investigation was to examine the wood anatomy in order to find tree species with distinct increment zones
The anatomy of the increment zones of those 9 tree species which showed distinct increment zones is described
Forthy-one tree species belonging to 22 families were sampled in 7 differents forests reserves and forest plantations in the State of São Paulo
The locations of the different areas under investigation are shown in Map 1
All species are native in the State of São Paulo and grow either in the forest formations Savanna (Cerrado) or Atlantic forest (Mata Atlântica)
Climate diagrams in all regions samples were collected
precipitation is well distributed throughout the year with an distinct dry season from June to August
Monthly precipitation in that time is less than 60 mm in all regions
mean annual precipitation for the 1975-2001 period was 1357 mm
mean annual air-temperature was 21.8 °C
June and July were the coldest months with an average air-temperature around 17.7°C
The climate diagram of Piracicaba (1981-90 period) is shown in Fig
Wood samples were taken at breast height by a specially developed motorized borer (Cury 2002)
For each of the 41 tree species investigated
three individuals were found and one sample collected out of each tree
Blocks of approximatelly 2 x 1 x 1 cm were cut out of one sample per species and softened by boiling in distilled water and glycerine
tangential and radial sections (15 µm thick) were cut of the blocks using a sliding microtome and stained with safranin
Mikrofotographs of the transverse sections were made using a ZEISS Axioskop light microscope
one or two samples were polished with sand paper (150 - 1200 grains per cm 2 ) and observed with the naked eye
The leaf fall pattern of the species investigated were divided into deciduous
based on the literature (Lorenzi 1992 & 1998
Morellato 1991) and phenological observations which were carried out monthly from January 1999 to Dezember 2001
9 of the 41 tree species investigated showed distinct increment zones
10 more species showed scarcly distinct increment zones
13 species showed indistinct increment zones
while the remaining 9 species showed no increment zones
Distinct increment zones were found in all leaf-fall categories
whereas in each of the two categories deciduous and semi-deciduous 4 tree species with distinct increment zones could be found
in the categorie evergreen only one species showed distinct increment zones
15 semi-deciduous and 11 evergreen species
Species with scarcely distinct and indistinct increment zones were found in all leaf-fall categories
The structure of the increment zones of those nine tree species which showed distinct increment zones is described below:
Both species of the familie Bombacaceae studied in the scope of this investigation had distinct increment zones
The increment zones in Bombax grandiflorum Cav
3) were marked by marginal parenchyma bands and thick-walled and radially flattened latewood versus thin-walled earlywood fibres
in both species the increment zones showed distended rays
The two Ocotea species investigated (Ocotea puberula (Reich.) Nees (Fig
4) and Ocotea porosa (Nus & Mart.) Barroso (Fig
marked by thick-walled and radially flattened latewood versus thin-walled earlywood fibres
From the six species of the family Leguminosae-Caesalpiniaceae investigated
and Schizolobium parahyba (Vell.) Blake had distinct increment zones
showed indistinct increment zones while Bauhinia forficata Link showed no increment zones
The increment zones in Schizolobium parahyba (Vell.) Blake (Fig
6) were marked by thick-walled and radially flattened latewood versus thin-walled earlywood fibres
8) had increment zones marked by marginal parenchyma bands
9) showed the most distinct increment zones
They were marked by thick-walled and radially flattened latewood versus thin-walled earlywood fibres
We investigated four tree species of the family Euphorbiaceae
10) was the only one were the increment zones were found to be distinct
showed scarcely distinct increment zones while Croton sp
The increment zones in Alchornea sidifolia were marked by thick-walled and radially flattened latewood versus thin-walled earlywood fibres
Nine out of the 41 tree species investigated showed distinct increment zones
Four species belonged to the leaf-fall categorie deciduous
four to the categorie semi-deciduous and one to the categorie evergreen
It is known that evergreen tree species also can show distinct increment zones (Alvim 1964
The increment zones in the two Ocotea species (Lauraceae) were marked by thick-walled and radially flattened latewood versus thin-walled earlywood fibres
that this type of increment zone is common in species of the family Lauraceae
He also mentioned that terminal parenchyma bands are common in species of the family Leguminosae
which can be confirmed with the results of this study
Tree species with a ring-porous or semi-ring-porous structure
as can be found for example in Cedrela fissilis (Boninsegna et al
could not be found within the 41 trees species investigated
that this type of increment zone does not occur in tree species from the Central Amazonian inundation forests
it looks like that this type of increment zone is not very common
(2000) investigated 491 tree species of the 22 most representative families of the Brazilian flora
Hymenaea courbaril and Centrolobium tomentosum showed increment zones
the formation of increment zones in woody plants in general can be induced by seasonally changing favourable and unfavourable growth conditions
dry seasons and inundations were found to be triggering climate factors (Jacoby 1989
The relationship between precipitation and the formation of increment zones in tropical trees was found early
At the beginning of the last century Coster (1927 & 1928) recognized that trees of the same species showed distinct increment zones when they were grown under seasonal monsun climate
whereas individuals of the everwet climate only showed indistinct increment zones
a dry season width a length of two to three months and monthly precipitation with less than 60 mm can induce the formation of increment zones in tropical trees
In all areas under investigation in which trees were sampled in the scope of this study
precipitation is well distributed throughout the year with an distinct dry season of 3 months and monthly precipitation with less than 60 mm
Luchi (1998) investigated the growth periodicity of Hymenaea courbaril in the State of São Paulo
using the method of cambial wounding (Wolter 1968
Marcati (2000) investigated the growth rhythm of Copaifera langsdorfii
that the cambial activity during the rainy season was higher and that an terminal parenchyma band was formed during the dry season
The results of those two investigations already indicate that tree ring analysis in the eastern parts of the State of São Paulo
where precipitation is well distributed throughout the year
even when it seems to be highly likely that the periodicity of the increment zones in other tree species which show distinct increment zones also will found to be annual
it should be proofed in further investigations
The results of this investigation indicate
are species which should be further investigated in terms of their potential for tree ring analysis
We thank the Estação Experimental de Santa Rita do Passa Quatro
Estação Ecológica de Ibicatu
Estação Experimental de Tupi
Reserva Florestal Mata de Santa Genebra and the Sitio São Luiz for the samples
The financially supported by a research fellowship from the DAAD and FAPESP
Ecological trends in the wood anatomy of some Brazilian species
Tree growth periodicity in tropical climates
Zur Anatomie und Physiologie der Zuwachszonen- und Jahresringbildung in den Tropen
Descrição da estrutura anatômica do lenho e sua aplicação na identificação de espécies arbóreas do Cerrado e da Mata Atlântica do estado de São Paulo
Manual de Identificação e Cultivo de Plantas Arbóreas do Brasil
Manual de Identificação e Cultivo de Plantas Arbóreas do Brasil Vol
Periodicidade de crescimento em Hymenaea courbaril L
e anatomia ecológica do lenho de espécies de Mata Ciliar
Sazonalidade cambial em espécies tropicais
Growth Periodicity in Tropical Trees - Foreword
fenologia e relação com a atividade cambial de espécies arbóreas tropicais de florestas estacionais semideciduais
Earth's biologically richest and most endangered terrestrial ecoregions
arbustos e lianas de uma floresta semidecidua no Sudeste do Brasil
A method to measure radial increment in tropical trees
Remarks on age and growth rate determination of Amazonian trees
Vegetação e zonas climáticas: tratado de ecologia global
increment and age of trees in inundation forests
savannas and a mountain forest in the neotropics
How to measure growth dynamics in tropical trees - a review
rainfall-dependent growth and long-term growth patterns of tropical trees from the Caparo Forest Reserve in Venezuela
Dating tropical trees by means of 14 C from bomb tests
Location of the seven research areas in the State of São Paulo
the map also gives an idea about where the ecosystems savanna and Atlantic forest occur
- 3 : Chorisia speciosa (Bombacaceae)
Figures named with the letter a are macrographs
Figures named with the letter b are micrographs (magnification 100x)
- 6: Schizolobium parahyba (Leguminosae-Caesalpiniaceae)
- 7 : Hymenaea courbaril (Leguminosae-Caesalpiniaceae)
- 8: Copaifera langsdorfii (Leguminosae-Caesalpiniaceae)
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