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1.
Bull Environ Contam Toxicol ; 112(6): 82, 2024 Jun 01.
Article in English | MEDLINE | ID: mdl-38822880

ABSTRACT

Mercury contamination has been aggravated by emerging environmental issues, such as climate change. Top predators present concerning Hg concentrations once this metal bioaccumulates and biomagnifies. This study evaluated total mercury (THg) concentrations in tissues of 43 franciscanas (Pontoporia blainvillei) from two populations: the Franciscana Management Area (FMA) IIb and FMA IIIa. Animals from FMA IIIa showed mean concentration 5-times and 2.5-times higher in the liver and kidney (4.73 ± 6.84 and 0.52 ± 0.51 µg.g-1, w.w., respectively) than individuals from FMA IIb (0.89 ± 1.04 and 0.22 ± 0.15 µg.g-1, w.w., respectively). This might be due to: (I) individuals sampled from FMA IIIa being larger and older, and/or (II) the area near FMA IIIa presents environmental features leading to higher THg availability. Coastal contamination can affect franciscanas' health and population maintenance at different levels depending on their life history and, therefore, it should be considered to guide specific conservation actions.


Subject(s)
Dolphins , Endangered Species , Environmental Monitoring , Mercury , Water Pollutants, Chemical , Animals , Mercury/analysis , Mercury/metabolism , Water Pollutants, Chemical/analysis , Water Pollutants, Chemical/metabolism , Atlantic Ocean , Dolphins/metabolism , Liver/metabolism , Kidney/metabolism
2.
Mar Pollut Bull ; 182: 114002, 2022 Sep.
Article in English | MEDLINE | ID: mdl-35939933

ABSTRACT

A global movement towards decreases in elasmobranch overfishing has been noted in the last decades. However, discussion concerning the effects of POP contamination on the health and survival of these organisms is still recent. These compounds can affect the immune and endocrine systems of both sharks and batoids, impairing reproduction and impacting species recruitment, acting synergistically alongside overfishing effects. In this context, this study investigated the concentration of organochlorine compounds in liver of 29 individuals of Rioraja agassizii, a commercially exploited skate classified as Vulnerable by IUCN and as Endangered in Brazil. Contaminant concentrations were higher in adults compared to juveniles. Distinct contamination profiles were observed, suggesting different groups within the investigated population and revealing contaminants as a potential tool to assess population ecology. PCB levels were considered a concern as they resemble concentrations in ecosystems from the northern hemisphere, where deleterious effects on elasmobranchs have been observed.


Subject(s)
Sharks , Skates, Fish , Animals , Brazil , Conservation of Natural Resources , Ecosystem , Endangered Species , Fisheries
3.
Environ Pollut ; 306: 119370, 2022 Aug 01.
Article in English | MEDLINE | ID: mdl-35526646

ABSTRACT

On November 5th, 2015, the Fundão dam collapsed in Minas Gerais, southeastern Brazil, releasing millions of cubic meters of mud containing mining residue into the Doce River. Two weeks later, the mud arrived to the marine environment, triggering changes in franciscana dolphin habitat, Pontoporia blainvillei, from Franciscana Management Area Ia. This is an isolated population of the most endangered cetacean species in the South Atlantic Ocean. Organohalogen compounds (OHCs) may pose a threat to this endangered population because of their endocrine disrupting properties. Hence, this study sought to determine if there were differences in the bioaccumulation profile of OHC (PCBs, DDTs, Mirex, HCB, HCHs, PBDEs, PBEB, HBBZ and MeO-BDEs) in franciscana dolphins before and after dam collapse and to build a temporal trend. Blubber of 33 stranded individuals was collected in Espírito Santo state for organohalogen assessment between 2003 and 2019. Differences were found between franciscana dolphins collected prior to and after the disaster. Additionally, significant temporal trends for organochlorine pesticides and natural and anthropogenic organobromine were detected. The increase in pesticide concentrations after 2015 is suggestive of their reavailability in the environment. The decline in organobromine over time could be due to their debromination in the marine environment and alterations in the composition of their natural producers. PCBs remained stable during the period of the study. Our findings show an increase in endocrine disruptor concentrations, which is of great concern for this endangered population.


Subject(s)
Disasters , Dolphins , Pesticides , Polychlorinated Biphenyls , Water Pollutants, Chemical , Animals , Brazil , Environmental Monitoring , Mining , Polychlorinated Biphenyls/analysis , Water Pollutants, Chemical/analysis
4.
Chemosphere ; 299: 134331, 2022 Jul.
Article in English | MEDLINE | ID: mdl-35339524

ABSTRACT

Sea turtles face several threats and pollution has become a major concern for their conservation worldwide. We analyzed samples of the liver, muscles, and kidneys of 38 Chelonia mydas stranded along the Potiguar Basin, northeastern Brazil, between 2015 and 2018 to determine the total Hg concentration (THg), as well as the concentrations of Cu, Cd, Ag, and Se. The relation between turtle size and element concentrations revealed a negative correlation for THg and Se (liver, muscles, and kidneys), Cu and Cd (liver and kidneys) and a positive correlation for Ag in the three organs analyzed. Concentrations of THg, Cu, Ag, and Se were high in the liver, highlighting the Cu concentration (median = 25.1150 µg g-1 w.w.), while the kidneys had the highest Cd levels (median = 12.2200 µg g-1 w.w.). There was significant difference between element concentrations and the three organs analyzed, except for Ag and Se concentrations in the muscle and kidney samples. Our study showed that green turtles found in Potiguar Basin, northeastern Brasil, have bioaccumulated inorganic elements which indicate the need of further investigations on the environmental quality of the region.


Subject(s)
Mercury , Selenium , Turtles , Water Pollutants, Chemical , Animals , Bioaccumulation , Brazil , Cadmium , Copper , Silver , Water Pollutants, Chemical/analysis
5.
Environ Sci Technol ; 55(22): 15149-15161, 2021 11 16.
Article in English | MEDLINE | ID: mdl-34726395

ABSTRACT

Rough-toothed dolphins, Steno bredanensis, are closely associated with coastal waters in the Southwestern Atlantic Ocean, increasing the exposure to multiple stressors, such as chemical pollution. Persistent organic pollutants (POPs) are known to affect the health of cetacean species. To comprehend the potential impacts of POPs on populations' viability, it is necessary to distinguish populations and predict their risk of long-term exposure. Blubbers of rough-toothed dolphins (n = 28) collected along the southeastern (SE) and southern (S) Brazilian coast were screened for polychlorinated biphenyls (PCBs) and pesticides in a gas chromatograph coupled to a mass spectrometer. Based on the contamination profile, a discriminant function analysis separated the rough-toothed dolphins into three ecological populations: two coastal and one offshore. POP concentrations were the highest reported for the species worldwide and highest among the delphinids in Brazilian waters, reaching 647.9 µg g-1 lw for PCBs. The SE population presented 212.9 ± 163.0, S population presented 101.0 ± 96.7, and OCS/S population presented 183.3 ± 85.3 µg g-1 lw (mean ± SD) of PCBs. The potential risk of effects triggered by elevated PCB concentrations was assessed in an individual-based model. A risk of severe decline in population size is projected for the three populations in the next 100 years, especially in SE Brazil, varying between 67 and 99%.


Subject(s)
Dolphins , Environmental Pollutants , Polychlorinated Biphenyls , Animals , Atlantic Ocean , Environmental Monitoring , Polychlorinated Biphenyls/analysis
6.
J Acoust Soc Am ; 148(5): EL420, 2020 11.
Article in English | MEDLINE | ID: mdl-33261388

ABSTRACT

Atlantic spotted dolphins were recorded on the coastal area of Rio de Janeiro with equipment of 192 kHz sampling rate. The animals produced an average of 33 whistles/min. The repertoire was balanced among four contour categories, with the occurrence of a stereotyped whistle. Frequency parameters were measured between 1.3 and 29 kHz, which represents an increase in the frequency range previously reported for this species in the southwestern Atlantic Ocean. With the use of a higher sampling rate, the acoustic parameters of S. frontalis whistles have changed significantly and became more similar to those reported for North Atlantic populations.


Subject(s)
Dolphins , Stenella , Animals , Atlantic Ocean , Brazil , Sound Spectrography , Vocalization, Animal
7.
Vet Pathol ; 57(6): 845-857, 2020 11.
Article in English | MEDLINE | ID: mdl-32964811

ABSTRACT

Cetacean morbillivirus (CeMV; Paramyxoviridae) is the most significant pathogen of cetaceans worldwide. The novel "multi-host" Guiana dolphin (Sotalia guianensis; GD)-CeMV strain is reported in South American waters and infects Guiana dolphins and southern right whales (Eubalaena australis). This study aimed to describe the pathologic findings, GD-CeMV viral antigen distribution and detection by RT-PCR (reverse transcriptase polymerase chain reaction), and infectious comorbidities in 29 Guiana dolphins that succumbed during an unusual mass-mortality event in Rio de Janeiro state, Brazil, between November 2017 and March 2018. The main gross findings were lack of ingesta, pulmonary edema, ascites, icterus, hepatic lipidosis, multicentric lymphadenomegaly, as well as pneumonia, polyserositis, and multiorgan vasculitis caused by Halocercus brasiliensis. Microscopically, the primary lesions were bronchointerstitial pneumonia and multicentric lymphoid depletion. The severity and extent of the lesions paralleled the distribution and intensity of morbilliviral antigen. For the first time in cetaceans, morbilliviral antigen was detected in salivary gland, optic nerve, heart, diaphragm, parietal and visceral epithelium of glomeruli, vulva, and thyroid gland. Viral antigen within circulating leukocytes suggested this as a mechanism of dissemination within the host. Comorbidities included disseminated toxoplasmosis, mycosis, ciliated protozoosis, and bacterial disease including brucellosis. These results provide strong evidence for GD-CeMV as the main cause of this unusual mass-mortality event.


Subject(s)
Dolphins , Morbillivirus Infections , Morbillivirus , Animals , Brazil , Dolphins/virology , Female , Morbillivirus Infections/pathology , Morbillivirus Infections/veterinary
8.
Front Immunol ; 10: 485, 2019.
Article in English | MEDLINE | ID: mdl-30936878

ABSTRACT

Cetacean morbillivirus (CeMV; Paramyxoviridae) causes epizootic and interepizootic fatalities in odontocetes and mysticetes worldwide. Studies suggest there is different species-specific susceptibility to CeMV infection, with striped dolphins (Stenella coeruleoalba), bottlenose dolphins (Tursiops truncatus), and Guiana dolphins (Sotalia guianensis) ranking among the most susceptible cetacean hosts. The pathogenesis of CeMV infection is not fully resolved. Since no previous studies have evaluated the organ-specific immunopathogenetic features of CeMV infection in tissues from infected dolphins, this study was aimed at characterizing and comparing immunophenotypic profiles of local immune responses in lymphoid organs (lymph nodes, spleen), lung and CNS in CeMV-molecularly (RT-PCR)-positive cetaceans from Western Mediterranean, Northeast-Central, and Southwestern Atlantic. Immunohistochemical (IHC) analyses targeted molecules of immunologic interest: caspase 3, CD3, CD20, CD57, CD68, FoxP3, MHCII, Iba1, IFNγ, IgG, IL4, IL10, lysozyme, TGFß, and PAX5. We detected consistent CeMV-associated inflammatory response patterns. Within CNS, inflammation was dominated by CD3+ (T cells), and CD20+ and PAX5+ (B cells) lymphocytes, accompanied by fewer Iba1+, CD68+, and lysozyme+ histiocytes, mainly in striped dolphins and bottlenose dolphins. Multicentric lymphoid depletion was characterized by reduced numbers of T cells and B cells, more pronounced in Guiana dolphins. Striped dolphins and bottlenose dolphins often had hyperplastic (regenerative) phenomena involving the aforementioned cell populations, particularly chronically infected animals. In the lung, there was mild to moderate increase in T cells, B cells, and histiocytes. Additionally, there was a generalized increased expression of caspase 3 in lymphoid, lung, and CNS tissues. Apoptosis, therefore, is believed to play a major role in generalized lymphoid depletion and likely overt immunosuppression during CeMV infection. No differences were detected regarding cytokine immunoreactivity in lymph nodes, spleen, and lung from infected and non-infected dolphins by semiquantitative analysis; however, there was striking immunoreactivity for IFNγ in the CNS of infected dolphins. These novel results set the basis for tissue-specific immunophenotypic responses during CeMV infection in three highly susceptible delphinid species. They also suggest a complex interplay between viral and host's immune factors, thereby contributing to gain valuable insights into similarities, and differences of CeMV infection's immunopathogenesis in relation to body tissues, CeMV strains, and cetacean hosts.


Subject(s)
Dolphins/immunology , Morbillivirus Infections/veterinary , Morbillivirus/immunology , Animals , Atlantic Ocean , Central Nervous System/immunology , Central Nervous System/pathology , Cytokines/biosynthesis , Cytokines/genetics , Female , Immunohistochemistry , Lung/immunology , Lung/pathology , Lymphoid Tissue/immunology , Lymphoid Tissue/pathology , Male , Mediterranean Sea , Morbillivirus Infections/immunology , Morbillivirus Infections/pathology , Paraffin Embedding , Species Specificity , Tissue Fixation
9.
Dis Aquat Organ ; 130(3): 177-185, 2018 09 27.
Article in English | MEDLINE | ID: mdl-30259870

ABSTRACT

The poxviruses identified in cetaceans are associated with characteristic tattoo or ring skin lesions. However, little is known regarding the prevalence and progression of these lesions and the molecular characterization of cetacean poxviruses in the Southern Hemisphere. This manuscript describes the progression of poxvirus-like skin lesions in 5 free-ranging Guiana dolphins Sotalia guianensis. Additionally, 151 skin samples from 113 free-ranging cetaceans from Brazil, including 4 animals with tattoo skin lesions, were selected for poxvirus testing. Poxviral DNA polymerase gene PCR amplification was used to detect the virus in ß-actin-positive samples (145/151). DNA topoisomerase I gene PCR was then used in Cetaceanpoxvirus (CePV)-positive cases (n = 2), which were further evaluated by histopathology and electron microscopy. Based on photo-identification, adult Guiana dolphins presented regressing or healed poxvirus-like lesions (2/2), while juveniles presented persistent (2/3) or healed and progressive lesions (1/3). CePV DNA was amplified in a common bottlenose dolphin Tursiops truncatus and in a Guiana dolphin. Intracytoplasmic inclusion bodies and viral particles consistent with poxvirus were identified by histology and electron microscopy, respectively. CePV-specific amino acid motifs were identified through phylogenetic analysis. Our findings corroborate previous studies that suggest the placement of poxviruses from cetaceans within the novel CePV genus. This is the first molecular identification of poxvirus in South American odontocetes.


Subject(s)
Bottle-Nosed Dolphin , Phylogeny , Poxviridae Infections , Poxviridae , Animals , Bottle-Nosed Dolphin/virology , Brazil , Poxviridae/isolation & purification , Poxviridae Infections/veterinary
10.
Emerg Infect Dis ; 24(7): 1349-1354, 2018 07.
Article in English | MEDLINE | ID: mdl-29912687

ABSTRACT

During November-December 2017, a mass die-off of Guiana dolphins (Sotalia guianensis) began in Rio de Janeiro, Brazil. Molecular and pathologic investigations on 20 animals indicated that cetacean morbillivirus played a major role. Our findings increase the knowledge on health and disease aspects of this endangered species.


Subject(s)
Animal Diseases/epidemiology , Animal Diseases/virology , Dolphins/virology , Morbillivirus Infections/veterinary , Morbillivirus , Animals , Brazil/epidemiology , Disease Outbreaks , Female , Male , Phylogeny , Population Density , RNA, Viral
11.
PLoS One ; 13(5): e0194872, 2018.
Article in English | MEDLINE | ID: mdl-29768405

ABSTRACT

This study describes the pathologic findings of 24 humpback whales (Megaptera novaeangliae) found stranded along the Brazilian coast from 2004 to 2016. Eighteen (75%) animals evaluated were found stranded alive. From these, 13 died naturally on shore and five were euthanized. Six died at sea and were washed ashore. Of the 24, 19 (79.2%) were calves, four (16.7%) were juveniles, and one (4.2%) was an adult. The most probable cause of stranding and/or death (CSD) was determined in 23/24 (95.8%) individuals. In calves, CSD included neonatal respiratory distress (13/19; 68.4%), infectious disease (septicemia, omphaloarteritis and urachocystitis; 3/19; 15.8%), trauma of unknown origin (2/19; 10.5%), and vehicular trauma (vessel strike; 1/19; 5.3%). In juveniles and adult individuals, CSD was: emaciation (2/5; 40%), sunlight-thermal burn shock (1/5; 20%); and discospondylitis (1/5; 20%). In one juvenile, the CSD was undetermined (1/5; 20%). This study integrates novel findings and published case reports to delineate the pathology of a South-western Atlantic population of humpback whales. This foundation will aid in the assessment of the population health and establish a baseline for development of conservation policies.


Subject(s)
Bone Diseases/veterinary , Cause of Death , Communicable Diseases/veterinary , Humpback Whale/abnormalities , Respiratory Insufficiency/veterinary , Animals , Bone Diseases/mortality , Bone Diseases/pathology , Brazil , Communicable Diseases/mortality , Communicable Diseases/pathology , Respiratory Insufficiency/mortality , Respiratory Insufficiency/pathology
12.
Environ Sci Technol ; 51(3): 1176-1185, 2017 02 07.
Article in English | MEDLINE | ID: mdl-28055195

ABSTRACT

To catalog the diversity and abundance of halogenated organic compounds (HOCs) accumulating in high trophic marine species from the southwestern Atlantic Ocean, tissue from bottlenose dolphins (Tursiops truncatus) stranded or incidentally captured along the coast of Rio de Janeiro, Brazil, were analyzed by a nontargeted approach based on GC×GC/TOF-MS. A total of 158 individual HOCs from 32 different structural classes were detected in the blubber of 4 adult male T. truncatus. Nearly 90% of the detected compounds are not routinely monitored in the environment. DDT-related and mirex/dechlorane-related compounds were the most abundant classes of anthropogenic origin. Methoxy-brominated diphenyl ethers (MeO-BDEs) and chlorinated methyl- and dimethyl bipyrroles (MBPs and DMBPs) were the most abundant natural products. Reported for the first time in southwestern Atlantic cetaceans and in contrast to North American marine mammals, chlorinated MBPs and DMBPs were more abundant than their brominated and/or mixed halogenated counterparts. HOC profiles in coastal T. truncatus from Brazil and California revealed a distinct difference, with a higher abundance of MeO-BDEs, mirex/dechloranes and chlorinated bipyrroles in the Brazilian dolphins. Thirty-six percent of the detected HOCs had an unknown structure. These results suggest broad geographical differences in the patterns of bioaccumulative chemicals found in the marine environment and indicate the need to develop more complete catalogs of HOCs from various marine environments.


Subject(s)
Bottle-Nosed Dolphin , Environmental Monitoring , Animals , Brazil , Dolphins , Organic Chemicals , Water Pollutants, Chemical
13.
Sci Total Environ ; 572: 352-360, 2016 Dec 01.
Article in English | MEDLINE | ID: mdl-27509073

ABSTRACT

Organic compounds, in particular organochlorines, are highly persistent compounds which accumulate in biotic and abiotic substrates. Marine mammals bioaccumulate and biomagnify persistent organic pollutants (POPs) through diet. ∑PCB (26 PCB congeners), ∑DDT (pp-DDT, pp-DDD, pp-DDE), ∑HCH (α-HCH, ß-HCH, γ-HCH, δ-HCH), HCB and mirex were analyzed from samples of subcutaneous adipose tissue of common dolphins, Delphinus delphis, and Fraser's dolphins, Lagenodelphis hosei, obtained in 1999 and 2012. The aim of this study was to determine the concentrations of POPs to get baseline information on the current state of pollution by these compounds in these two species in South Atlantic. At the same time, to assess concentrations of POPs in relation to age, the total length and sexual maturity in common dolphins. Organochlorine pesticides dominated Fraser's dolphins, DDT being the most abundant, while PCBs were mostly present in common dolphins. In both species, the distributions of isomers or metabolites followed the order: ß-HCH>δ-HCH>γ-HCH>α-HCH and pp-DDE>pp-DDD>pp-DDT. As for ∑PCB, the largest contribution was given by congeners of high molecular weight, particularly by hexa and hepta - CBs. Common dolphins did not show effects on sexual maturity, age and standard length in the concentration of organochlorines. The mean concentrations found in this study are lower compared to those reported in other studies performed in dolphins elsewhere. This study provides new information regarding levels of organochlorines in common dolphins for the Southwestern Atlantic.


Subject(s)
Dolphins/metabolism , Hydrocarbons, Chlorinated/metabolism , Pesticides/metabolism , Water Pollutants, Chemical/metabolism , Age Factors , Animals , Argentina , Atlantic Ocean , Body Size , Common Dolphins/metabolism , Female , Male , Sexual Maturation
14.
Sci Total Environ ; 472: 194-203, 2014 Feb 15.
Article in English | MEDLINE | ID: mdl-24291562

ABSTRACT

Organochlorine compounds are highly persistent in the environment, causing bioaccumulation and biomagnification through the marine food chain. To verify the bioaccumulation pattern of DDT and its metabolites, as well as PCBs, Mirex, HCHs and HCB, samples of subcutaneous adipose tissue from 25 Guiana dolphins (Sotalia guianensis), two Fraser's dolphins (Lagenodelphis hosei), two spinner dolphins (Stenella longirostris), one spotted dolphin (Stenella frontalis), and one striped dolphin (Stenella coeruleoalba) were analyzed. The collected specimens were found stranded in northeastern Brazil between 2005 and 2011. The concentrations were reported in µg·g(-1) lip, varying from 0.02 to 17.3 for ΣPCB, from 0.003 to 5.19 for ΣDDT, from 0.005 to 0.16 for ΣHCH, from 0.002 to 0.16 for HCB, and from 0.02 to 2.38 for Mirex. The PCBs dominated the bioaccumulation pattern for both the Guiana and spinner dolphins; for the other species, DDT was the major compound. A discriminant function analysis revealed the differences in the organochlorine accumulation patterns between the Guiana dolphin (S. guianensis) and the continental shelf/oceanic dolphins (S. frontalis and S. longirostris). The results also show that the concentrations of organochlorine compounds found in the delphinids in northeastern Brazil were lower than the delphinids found in other regions of Brazil, as well as other locations worldwide with intense agroindustrial development and/or a larger population.


Subject(s)
Dolphins/metabolism , Environmental Monitoring , Hydrocarbons, Chlorinated/metabolism , Water Pollutants, Chemical/metabolism , Animals , Brazil , DDT/metabolism , Female , Hexachlorobenzene/metabolism , Hexachlorocyclohexane/metabolism , Male , Mirex/metabolism , Polychlorinated Biphenyls/metabolism
15.
Article in English | LILACS-Express | VETINDEX | ID: biblio-1494000

ABSTRACT

It was evaluated the influence of the weight in the effect of the anesthetic eugenol for juveniles of matrinxã and tambaqui. For that, it was used a total of 69 matrinxãs and 49 tambaquis. The animals were anesthetized individually, weighed and observed during the induction and the recover of the anesthesia. For the induction it was used the concentration of the anesthetic"s 50 mg/L, previously diluted in alcohol. The obtained weights were gathered in five classes and no difference statistics was observed for the times of induction and recovery among them.


Foi avaliada a influência do peso de juvenis de matrinxã e tambaqui sobre a ação do anestésico eugenol. Para isso, foram utilizados 69 matrinxãs e 49 tambaquis. Os animais foram individualmente anestesiados, pesados e observados durante a indução e a recuperação da anestesia. Para a indução foi utilizada a concentração de 50 mg/L do anestésico, previamente diluído em álcool. Os pesos obtidos foram reunidos em cinco classes, não sendo observada diferença estatística para os tempos de indução e de recuperação entre elas.

16.
Article in English | VETINDEX | ID: vti-711661

ABSTRACT

It was evaluated the influence of the weight in the effect of the anesthetic eugenol for juveniles of matrinxã and tambaqui. For that, it was used a total of 69 matrinxãs and 49 tambaquis. The animals were anesthetized individually, weighed and observed during the induction and the recover of the anesthesia. For the induction it was used the concentration of the anesthetic"s 50 mg/L, previously diluted in alcohol. The obtained weights were gathered in five classes and no difference statistics was observed for the times of induction and recovery among them.


Foi avaliada a influência do peso de juvenis de matrinxã e tambaqui sobre a ação do anestésico eugenol. Para isso, foram utilizados 69 matrinxãs e 49 tambaquis. Os animais foram individualmente anestesiados, pesados e observados durante a indução e a recuperação da anestesia. Para a indução foi utilizada a concentração de 50 mg/L do anestésico, previamente diluído em álcool. Os pesos obtidos foram reunidos em cinco classes, não sendo observada diferença estatística para os tempos de indução e de recuperação entre elas.

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