Epidemiology of toxoplasmosis in felids and canids in Brazil: A brief One Health overview

Epidemiologia da toxoplasmose em felídeos e canídeos no Brasil: uma breve visão geral em Saúde Única

ABSTRACT:

Toxoplasmosis is a disease caused by the obligate intracellular protozoan Toxoplasma gondii, which infects animals and humans worldwide. Felids are definitive hosts that eliminate oocysts, contaminating the environment, food, and water. Among carnivores, cats are the most important hosts for the epidemiology of the disease since a single individual can shed millions of oocysts. Wild canids are considered sentinels and play an essential role in the epidemiology of toxoplasmosis due to tissue cysts in muscle cells, representing a source of infection for carnivores through predation, while environmental contamination is mainly due to oocyst shedding by felids. Free-ranging felids are more likely to be infected by T. gondii than felids living in captivity. The free-living wild canids have lower seropositivity compared to canids in captivity. This review article presents epidemiological data on toxoplasmosis in domestic and wild carnivores in Brazil, targeting professionals in clinical practice, veterinary pathology, diagnostics, and One Health. Therefore, we understand the importance of disseminating diagnoses, epidemiological investigations and animal health programs to control, prophylaxis and treat toxoplasmosis in domestic and wild carnivores.

INDEX TERMS:
Epidemiology; wildlife conservation; wildlife medicine; veterinary pathology; toxoplasmosis; carnivore; Apicomplexa; Toxoplasma gondii

RESUMO:

A toxoplasmose é uma doença causada pelo protozoário intracelular obrigatório Toxoplasma gondii, responsável por infectar animais e seres humanos em todo o mundo. Os felinos são hospedeiros definitivos e eliminam oocistos que contaminam o ambiente, alimentos e água. Dentre os carnívoros, os felinos são os hospedeiros mais importantes para a epidemiologia da doença, visto que um único indivíduo é capaz de excretar milhões de oocistos. Canídeos selvagens são considerados sentinelas e desempenham um papel essencial na epidemiologia da toxoplasmose, pois os cistos teciduais presentes nas células musculares representam uma fonte de infecção para carnívoros por meio da predação, enquanto a contaminação ambiental ocorre principalmente pela eliminação de oocistos por felídeos. Os felinos de vida livre têm maior probabilidade de serem infectados por T. gondii do que os felinos mantidos sob cuidados humanos. Os canídeos silvestres de vida livre apresentam menor soropositividade em comparação aos canídeos em cativeiro. Este artigo de revisão apresenta dados sobre a epidemiologia da toxoplasmose em carnívoros domésticos e silvestres no Brasil focado para profissionais da área clínica, patologia veterinária, diagnóstico e Saúde Única. Portanto entendemos a importância de divulgação de métodos de diagnósticos, investigações epidemiológicas e programas de saúde animal para contribuir com o controle, profilaxia e tratamento da toxoplasmose em carnívoros domésticos e silvestres.

TERMOS DE INDEXAÇÃO:
Epidemiologia; conservação da natureza; medicina de animais silvestres; patologia veterinária; toxoplasmose; carnívoro; Apicomplexa; Toxoplasma gondii

INDEX TERMS:
Epidemiology; wildlife conservation; wildlife medicine; veterinary pathology; toxoplasmosis; carnivore; Apicomplexa; Toxoplasma gondii

TERMOS DE INDEXAÇÃO:
Epidemiologia; conservação da natureza; medicina de animais silvestres; patologia veterinária; toxoplasmose; carnívoro; Apicomplexa; Toxoplasma gondii

INDEX TERMS:
Epidemiology; wildlife conservation; wildlife medicine; veterinary pathology; toxoplasmosis; carnivore; Apicomplexa; Toxoplasma gondii

TERMOS DE INDEXAÇÃO:
Epidemiologia; conservação da natureza; medicina de animais silvestres; patologia veterinária; toxoplasmose; carnívoro; Apicomplexa; Toxoplasma gondii

Introduction

Toxoplasma gondii infects all warm-blooded animal species. Toxoplasmosis continues to be a worldwide public health problem (Aguirre et al. 2019, Dubey 2022). The epidemiological scenario of toxoplasmosis in Brazil is impressive since it accounted for 35% of human toxoplasmosis outbreaks worldwide over the last decade (Dubey 2022). Felids (domestic and wild cats) are the only definitive hosts of Toxoplasma gondii and are capable of shedding environmentally resistant oocysts in their feces (Dubey et al. 2020a). However, skeletal muscle cells contain tissue cysts, representing an essential source of infection for omnivorous and carnivorous hosts and maintenance of the protozoans’ biological cycle.

The carnivorous hosts of T. gondii are affected by a catastrophic environmental scenario, besides threats to human urban areas and diseases (Gering et al. 2021). An increasing number of wild carnivores have been attracted to urban or suburban areas due to easy access to food or safe shelter, and wild animals have become urban residents (Kornacka-Stackonis 2022). Currently, in Brazil, wildfire receives significant importance as an agent that implies the migration of wildlife populations, which could drive mortality across vast areas (Magioli et al. 2024), exerting intense selective pressure on disease occurrence (Tomas et al. 2021).

The species from the order Carnivora are mammals that feed by preying on other animals. Carnivores comprise around 280 species spread across the planet (Hudson et al. 2022). About 64% of carnivores species are threatened, and 80% have declining populations due to habitat loss and fragmentation, persecution by humans, and often livestock-related conflicts (Ubiali et al. 2018, Wolf & Ripple 2018). There are 28 wild carnivore species of mammals in the Brazilian fauna, comprising five taxonomic families, including 10 Felidae and six Canidae species (Instituto Pró-Carnívoros 2024). This order includes the most popular domestic species, including pets, dogs, and cats. Our affection for domestic carnivores reflects the number of domestic dogs and cats, quantified as 55.9 million canines and 25.6 million domestic felines in Brazil (Instituto Pet Brasil 2021). Otherwise, the Earth’s large terrestrial carnivores are charismatic, highly endangered groups of species like jaguars and maned wolves. Most of these wild species have experienced major geographical range contractions, causing risk of extinction or becoming ecologically nonviable (Van Valkenburgh & Wayne 2010).

Serologic prevalence data are also important for determining the epidemiologic significance of T. gondii infection in cats because oocysts are rarely found in the feces of cats (Dubey et al. 1995). The definitive hosts eliminate oocysts and contribute to the perpetuation of the disease (Dubey 2022). Cats can eliminate rapidly around 20 million oocysts during the first infection (Dubey 1995). Experimentally reinfected cats could eliminate T. gondii oocysts years after the first infection (Zulpo et al. 2018), especially when the cat has been infected with different strains (Dubey 2022). Cats infected with Feline Immunodeficiency Virus (FIV) or Feline Leukemia Virus (FeLV) may be more susceptible to T. gondii infection due to immunosuppression (Munhoz et al. 2017, Pena et al. 2017). The human-animal bond, recognized as a special relationship between people and companion animals, has led to the hypothesis that humans and animals living in the same household, sometimes sharing a bed, may be closely related from an epidemiological perspective (Paul et al. 2010, Benitez et al. 2017).

The population of domestic felines in Brazil has grown, and the seropositivity of the populations varies from 19% to 50%, demonstrating, as definitive hosts, at some point, that these felines eliminate oocysts in their feces, increasing high environmental contamination. (Dubey 2022, Carvalho-Alves et al. 2024). In Brazilian wildlife, 10 species of felids are distributed into five biomes (Instituto Pró-Carnívoros 2024). Interactions of wild felids could contaminate the food of many species and cause abortion due to toxoplasmosis in ruminants (Caldeira et al. 2011, Roman et al. 2024). Under other conditions, birds could be hunted by felids. Birds are susceptible to T. gondii infection and serve as intermediate hosts in the protozoan’s life cycle. Consequently, birds are essential sources of infection for wildlife carnivores (Alves et al. 2022).

The present review provides information on the epidemiology of toxoplasmosis in domestic and wild carnivores in Brazil, targeting One Health professionals. In this context, a literature review was conducted on epidemiologic investigations of domestic and wild carnivores to identify toxoplasmosis and host-protozoan interactions.

Materials and Methods

Ethical approval. All data were obtained from database literature searches; we did not perform animal sampling or experiments for the present study.

Peer-reviewed scientific papers (original research, case reports, and reviews) on toxoplasmosis were searched in electronic databases: BASE, Google Scholar, Latindex, Medline, PubMed, SciELO, Scopus, Web of Science and WorldWideScience. We searched for carnivores, cats, dogs, wild carnivores, toxoplasmosis and Toxoplasma gondii. The title, abstract, materials and methods, and results from researches found in online database searches up to December 2024 were screened for relevance to inclusion in our review. This review is divided into toxoplasmosis epidemiology in domestic cats and domestic dogs, wild carnivores, wild felids and wild canids in Brazil; afterward, we prepare a Discussion section and the Conclusions.

The reported research spatial data on toxoplasmosis cases in domestic and wild carnivores were analyzed using ArcGIS ^TM v. 10.6.1 licensed software to elaborate epidemiological maps.

Domestic Cats

The prevalence of Toxoplasma gondii infection varies depending on the habits and housing of domestic cats. In general, it is higher in wild cats that hunt for food than in domestic cats without outdoor access. The availability of food sources is directly linked to high seroprevalence rates in domestic cats (Dubey et al. 2020a). Brazil is highlighted as one of the countries with the highest number of reports, emphasizing domestic cats’ significant role in toxoplasmosis epidemiology. The frequency of T. gondii infection in Brazilian pet animal populations can vary from 0 to 92% in cats (Fig. 1 and Table 1).

Fig. 1.
Mapping toxoplasmosis in domestic cats and dogs, wild felids and canids in Brazil based on literature reports and research.

Table 1.
Seroepidemiological survey for toxoplasmosis in domestic cats in Brazil

State	N	Reactive (%)	Test	Dilution	Author and year
Acre	89	24.7	IFAT	1:64	Souza et al. (2015)
Bahia	231	45.4	IFAT	1:64	Munhoz et al. (2017)
	28	50.0	IFAT	1:64	Oliveira et al. (2019)
	20	35.0	IHA	1:64	Deiró et al. (2021)
Espírito Santo	79	15.2 7.6	ELISA IFAT	NM	Fux et al. (2020)
Maranhão	200	50.5	IFAT	1:40	Braga et al. (2012)
Mato Grosso do Sul	14	57.14	MAT	1:25	Marques et al. (2009)
	50	4.0	IFAT	1:40	Braga et al. (2014)
	151	32.5	IFAT	1:16	Souza et al. (2014)
Minas Gerais	209	19.6 21.0	IFAT ELISA	1:16	Sebastiani (2021)
Pará	447	21.92	IFAT	1:16	Rocha et al. (2020)
Paraíba	201	43.8	IFAT	1:16	Feitosa et al. (2014)
	103	53.4	IFAT	1:16	Feitosa et al. (2021)
	267	17.22	IFAT	1:16	Fernandes et al. (2024a)
Paraná	282	16.3	IFAT	1:16	Cruz et al. (2011)
	171	28.7	IFAT	1:16	Andrade et al. (2015)
	2	100.0	IFAT	1:24	Ferreira Neto et al. (2018)
Pernambuco	118	59.3	MAT	1:25	Costa et al. (2012)
	35	25.7	IFAT	1:16	Arraes-Santos et al. (2016)
	348	71.2	IFAT	1:16	Magalhães et al. (2017)
	31	58.0	IFAT	1:16	Melo et al. (2016)
Piauí	102	0	ELISA	NM	Teixeira et al. (2016)
Rio de Janeiro	41	24.4	ELISA	NM	Gonçalves Netto et al. (2003)
	75	92.0	HAI	1:16	Mendes-de-Almeida et al. (2007)
	108	5.6	HAI	1:16	Bastos et al. (2014)
	213	6.6	IFAT	1:64	Barros et al. (2015)
	372	9.7	MAT	1:25	Bolais et al. (2017)
	86	29.0	IFAT	1:16	Freitas (2017)
	433	21.9	IFAT	1:64	Pereira et al. (2018)
	272	8.1	IFAT	1:64	Arruda et al. (2021)
	91	18.7	MAT	1:25	Carvalho-Alves et al. (2024)
Rio Grande do Norte	53	52.8	MAT	1:25	Fournier et al. (2014)
	120	25.8	IFAT	1:16	Bezerra et al. (2023)
Rio Grande do Sul	100	37.0	HAI	1:64	Araújo et al. (2003)
	245	37.9	IFAT	1:64	Pinto et al. (2009)
	180	21.6	IFAT	1:64	Oliveira et al. (2014)
	112	38.0	IFAT	1:16	Fernandes et al. (2024b)
Rondônia	63	87.3	MAT	1:25	Cavalcante et al. (2006)
	100	26.0	IFAT	1:16	Silva et al. (2023)
Santa Catarina	300	14.3	IFAT	1:64	Rosa et al. (2010)
	60	50.0	IFAT	NM	Faria et al. (2018)
São Paulo	248	17.7	IFAT	1:40	Lucas et al. (1999)
	400	25.0	IFAT	1:64	Bresciani et al. (2007)
	237	35.4	MAT	1:25	Pena et al. (2006)
	59	78.0	ELISA	NM	Duarte et al. (2010)
	70	15.7	IFAT	1:64	Coelho et al. (2011)
	251	20.3	IFAT	1:16	Vicente Sobrinho et al. (2012)
	386	16.3	IFAT	1:64	Cardia et al. (2013)

• IFAT = Indirect fluorescent antibody test, IHA = indirect hemagglutination, ELISA = enzyme-linked immunosorbent assay, MAT = modified agglutination test, NM = not mentioned.

The Brazilian domestic cats seropositivity to T. gondii shows remarkable variation, a key epidemiological feature. One study found a seroprevalence of just 5.6% in domestic cats. At the same time, other analyses indicate seropositivity between 61% and 92% in a free-living feline population in urban areas of the State of Rio de Janeiro (Mendes-de-Almeida et al. 2007). This variation was also attributed to these animals’ eating habits and lifestyle since domesticated felines have more access to industrialized food, sanitary litter boxes, and reduced access to hunting small rodents or other possible intermediate hosts of the protozoan.

Studies on the detection of anti-T. gondii and assessment of risk factors for infection are common. A current report evaluated the risk factors in Rio de Janeiro and observed that cats over ten years have a high probability of disease (Carvalho-Alves et al. 2024). An investigation by Fernandes et al. (2024a) in João Pessoa, Paraíba, also observed the cat’s age and where they live (urban area) as risk factors. Domestic cats that eat offal and homemade food are more likely to become infected, as male cats become more infected than females (Arruda et al. 2021). This factor may be related to exploratory behavior, possibly associated with outside physical activities and high energy requirements (Miró et al. 2004).

The Southeast region has the highest number of seroepidemiological investigations in domestic cats and, consequently, a high prevalence. It is worth highlighting the State of Rio de Janeiro, which is endemic for toxoplasmosis in cats, with the most significant number of studies and, therefore, the one with the most important variation in seroprevalence: 8.1% to 92%. São Paulo comes next with seven studies in which a variation of 15% to 70% in seroprevalence is observed. Minas Gerais and Espírito Santo have few analyses, just one of each, with seroprevalence of 7% and 20%, respectively. From the Northeast, in the state of Piauí, no seropositive cats were detected in the only study, unlike Pernambuco, where seroprevalence reached up to 70%. Bahia, Maranhão, Paraíba, and Rio Grande do Norte had an average of 50% of cats presenting anti-T. gondii antibodies. In the North region, studies were conducted only in Acre, Rondônia and Pará, with the percentage varying from 20% to 50%, demonstrating the need for further investigations to better understand toxoplasmosis in this region. Although one of the most significant outbreaks of human toxoplasmosis ever recorded occurred in the South region (Minuzzi et al. 2021), the seroprevalence of cats in this region averaged 30%.

A meta-analysis of published articles on T. gondii prevalence in cats in Brazil conducted by Lugoch et al. (2018) showed a seroprevalence of 35.9% for toxoplasmosis in cats in Brazil. Regarding the age group, it was found that adult cats are 2.84 times more likely to be seropositive than young cats. The seroprevalence of cats from the North-Northeast-Center region was 50.5% and 29.9% in the South-Southeast region, except for some studies in which the seroprevalence was higher.

A research group from Pará focused on applying an epidemiological questionnaire on toxoplasmosis to the owner, regardless of their level of education. Owners knew little about how the protozoan is transmitted to humans and animals (Rocha et al. 2020). This finding highlights the need for improved public awareness and education regarding the pathways of toxoplasmosis transmission. As a widely distributed zoonosis, toxoplasmosis must involve guidance and joint research within the scope of One Health. Therefore, it is essential to reinforce information on prophylaxis and monitor the profile of the epidemiological analysis of the animal population (Fernandes et al. 2024a).

Control and prophylaxis measures effectively reduce the incidence of infections and shed environmental oocysts. Feline infection risk depends on access to infected prey, reflecting their hunting behavior. Furthermore, methods such as castration and placing screens in homes so that animals do not have access to the streets are alternatives for control, as well as the presence of a litter box to defecate in an appropriate place (Dubey 2022). Controlling the food supply is also a protective measure and must be provided. In natural feeding, it is essential to freeze and cook meat before offering it (Arruda et al. 2021). Water is also a source of infection. Adequately treated and filtered water is recommended, as water treatment does not provide protection (England et al. 2018). The filtration efficiently retains T. gondii oocysts and prevents infection, instead of oocyst resistance to the most popular chlorination water treatment technique (Minuzzi et al. 2021, Dubey 2022).

Our review identified 47 Brazilian studies on anti-T. gondii seroprevalence in domestic cats (Table 1). In these studies, we observed variation in the serological tests used, with the Indirect Fluorescent Antibody Test (IFAT) being the most frequently used, followed by the Modified Agglutination Test (MAT), Enzyme-Linked Immunosorbent Assay (ELISA) and Indirect Hemagglutination Test (IHAT). When we look at the percentage of seropositive domestic cats, we notice that the country has a high prevalence. More than half of the analyses demonstrated a prevalence of 50% or higher, but depending on the region, this level reached only 20%. All reported studies were carried out after 1999 and cover the country’s five regions: six in the North, 11 in the Northeast, three in the Midwest, eight in the South, and 18 in the Southeast.

Concerning the presented data, we found that toxoplasmosis affects domestic cats throughout the national territory, warning of possible environmental contamination, considering that felines, when infected, can shed millions of environment-resistant oocysts, which survive for years. In other regions, especially in the North and Midwest of Brazil, further research is needed to increase understanding of the epidemiology and possible spillover between human and wild species, given the scarcity of reports.

Domestic Dogs

Toxoplasma gondii strain isolates in dogs in Brazil revealed high recombination, being highly pathogenic to animals (Silva et al. 2017). Seropositivity for anti-T. gondii antibodies in dogs has epidemiological significance and indicates the circulation of the protozoan in the environment (Dubey et al. 2020b). The seropositivity of free-ranging dogs means sentinel animals for toxoplasmosis and indicates environmental contamination by T. gondii oocysts. Monitoring seroprevalence can offer a strategy for evaluating exposure and geographical distribution of protozoan circulation (Dini et al. 2024).

Although toxoplasmosis has typically been considered a foodborne disease, socioeconomic factors such as low household income can impact human seroprevalence. An example is that yards containing garbage affect canine seroprevalence (Benitez et al. 2017). Contact with oocysts can led consequences beyond infection of the dog, as it has been demonstrated that dogs can act as mechanical transporters of T. gondii oocysts from the surface of the body, hair, mouth and paws. Furthermore, in coprophagia cases, after ingesting infected feline feces and during the oocyst elimination phase, dogs are not definitive hosts of T. gondii and do not biologically shed oocysts in their feces. However, they may contribute to environmental dissemination by mechanically excreting viable oocysts in their feces after ingesting cat feces during coprophagy. Additionally, oocysts may be transported on their fur, paws, or oral cavity after contact with contaminated environments (Dubey et al. 2020b, Dini et al. 2024).

Ingestion of homemade food and water is the leading risk factor associated with T. gondii infection in dogs. Meireles et al. (2004) pointed out that dogs are more susceptible to ingesting one of the infectious forms of T. gondii, such as tissue cysts in raw or undercooked meat or oocysts in contaminated food. More recent studies have also identified food as the leading risk factor for infection in domestic dogs (Cunha et al. 2020, Arruda et al. 2021, Freitas et al. 2022, Dini et al. 2024). Mixed-breed dogs are more likely to be infected with T. gondii than purebred dogs (Arruda et al. 2021).

The environment in which the dog has access is strongly related to a risk factor for T. gondii infection. Dini et al. (2024) associated the high prevalence of anti-T. gondii with cohabitation with domestic cats; this factor was highly significant in this study. The author pointed out that environmental contamination and the coprophagy behavior of dogs are associated with the presence of felines in the same environment. On the other hand, Freitas et al. (2022) did not find an association between the infection and the presence of cats in the environment in their research. This research found an association between high disease prevalence in dogs and owners having anti-T. gondii, demonstrating that animals are prone to becoming infected through contaminated food or water.

The low socioeconomic level of the population and poor infrastructure are directly associated as risk factors for dog infection (Carlos 2010, Benitez et al. 2017, Olbera et al. 2020, Belaz et al. 2023, Remor-Sebolt et al. 2024). Toxoplasmosis in dogs is associated with precarious sanitary conditions and environmental conditions of intense social inequality and low economic power. The presence of stray small animals as reservoirs and the close relationship between humans and dogs are also factors that contribute to the spread of the protozoan (Belaz et al. 2023). Arruda et al. (2021) raised the hypothesis that the habit of domestic dogs walking on the streets and their owners may be a factor for the high prevalence.

In Brazil, 60 seroprevalence analyses of this species were recorded in the most diverse states (Fig. 1 and Table 2). In these studies, they investigated anti-T. gondii in domiciled, non-domesticated dogs and those living in peridomicile and the type of residence, in addition to the presence of different eating habits and water intake that are provided to each animal by each responsible family, who proposed to participate in the work by answering forms. The most used serological test was the IFAT, which is known to be reliable but not as sensitive as the MAT (Desmonts & Remington 1980, Dubey 1997), followed by IHAT and ELISA. The percentage of seropositive dogs varied from 6% to 85%, depending on the region of the country. However, Table 2 shows that more than half of the country’s analyses demonstrated a prevalence of more than 50% of dogs.

Table 2.
Seroepidemiological survey for toxoplasmosis in domestic dogs in Brazil

State	N	Reactive (%)	Test	Dilution	Author and year
Several	157	31.2	IFAT	1:16	Machado et al. (2019)
Amazonas	325	52.0	IFAT	1:16	Minervino et al. (2012)
	154	12.3	IFAT	1:16	Campos et al. (2022)
Bahia	529	36.5	IHA	1:16	Carlos (2010)
	21	33.3	IHA	1:16	Silva et al. (2017)
	61	44.3	IFAT	1:16	Oliveira et al. (2019)
Espírito Santo	187	47.0	IFAT	1:16	Acosta et al. (2016)
Mato Grosso	61	88.5	NM	NM	Santos et al. (2009)
	248	43.1	IFAT	1:16	Rodrigues et al. (2016)
	386	6.7	IFAT	1:16	Strital et al. (2016)
Minas Gerais	163	33.0	IFAT	1:16	Mineo et al. (2001)
	218	60.7	IFAT	1:16	Guimarães et al. (2009)
	72	70.8	IFAT	1:16	Valadas et al. (2010)
Pará	57	68.4	IFAT	1:16	Paz et al. (2019)
	88	36.4
	16	18.7
	31	61.3
	128	35.9
Paraíba	286	45.1	IFAT	1:16	Azevedo et al. (2005)
	384	9.6	IFAT	1:50	Brasil et al. (2018)
	1043	22.1	IFAT	1:64	Fernandes et al. (2018)
Paraná	649	51.3	IFAT	1:16	Garcia et al. (1999)
	134	34.4	MAT	1:20	Souza et al. (2003)
	61	70.5	IFAT	1:16	Ruffolo et al. (2016)
	24	20.8	IFAT	1:16	Romanelli et al. (2007)
	127	18.1	IFAT	1:50	Plugge et al. (2011)
	120	40.0
	175	70.8	IFAT	1:16	Dreer et al. (2013)
	26	30.7	IFAT	1:20	Constantino et al. (2016)
	598	43.3	IFAT	1:16	Ferreira et al. (2016)
	729	16.3	IFAT	1:16	Benitez et al. (2017)
	649	51.3	ELISA	1:16	Pinto-Ferreira et al. (2019)
	364	48.0 29.67	IFAT MAT	1:16 1:25	Almeida et al. (2016)
	264	7.95	IFAT	1:16	Cunha et al. (2020)
	283	23.3	IFAT	1:16	Freitas et al. (2022)
	133	9.8	IFAT	1:16	Sohn-Hausner et al. (2024)
Pernambuco	170	57.6	IFAT	1:16	Figueredo et al. (2008)
	60	40.0	MAT	1:25	Costa et al. (2012)
	320	48.7	IFAT	1:16	Magalhães et al. (2017)
	241	9.5	IFAT	1:16	Souza et al. (2019)
Piauí	530	18.8	IFAT	1:16	Lopes et al. (2011)
Rio de Janeiro	651	46.8	ELISA	1:16	Cunha et al. (2016)
	14	28.6	IFAT	1:16	Oliveira et al. (2017)
	400	34.0	IFAT	1:16	Arruda et al. (2021)
Rio Grande do Sul	2245	16.0	IFAT	1:16	Mortari et al. (2023)
Rio Grande do Norte	476	11.5	IFAT	1:64	Dantas et al. (2013)
Santa Catarina	102	12.7	IFAT	1:16	Lopes et al. (2015)
	400	22.3	IFAT	1:64	Moura et al. (2009)
São Paulo	110	19.7	MAT	1:25	Souza et al. (2003)
	205	25.4	IFAT	1:16	Silva et al. (2010)
	21	38.1	IFAT	1:64	Aguiar et al. (2012)
	50	22.0	IFAT	1:16	Langoni et al. (2012)
	93	47.3	IFAT	1:16	Paulan et al. (2013)
	10	50.0	IFAT	1:16	Zanette et al. (2014)
São Paulo	300	24.3	IFAT	1:16	Seabra et al. (2015)
	133	27.0	MAT	1:25
	369	15.1	IFAT	1:16	Olbera et al. (2020)
	331	27.2	IFAT	1:16	Sevá et al. (2020)
	371	22.5
	348	43.9
	28	17.8	NM	NM	Gonçalves et al. (2022)
	336	52.9	MAT	1:25	Belaz et al. (2023)
	1194	10.5	IFAT	1:16	Santos et al. (2023)
	73	85.0	IFAT	1:16	Perin et al. (2024)
	238	23.1	IFAT	1:64	Remor-Sebolt et al. (2024)
São Paulo/Paraná	253	38.0	IFAT	1:16	Doline et al. (2023)
Tocantins	99	70.7	ELISA	1:20	Raimundo et al. (2015)

• IFAT = indirect fluorescent antibody test, IHA = indirect hemagglutination, NM = not mentioned, MAT = modified agglutination test, ELISA = enzyme-linked immunosorbent assay.

All domestic dog toxoplasmosis studies were conducted after 1999, demonstrating research covering the country’s five regions. According to the survey, the Southeast region of the country concentrates the most significant number of reports, totaling 20 studies with results ranging from 10% to 85% of dogs that present anti-T. gondii antibodies. They were followed by the South region, with 17 reports with seroprevalence ranging from 7 to 70%. We found 14 investigations in the Northeast with a seropositivity rate ranging from 9% to 60% of the dog population. The North and Midwest regions have the lowest number of reports, three and five, respectively, with seropositivity rates ranging from 6% to 70%. The number of dog investigations represents a level below 10% prevalence; they are lower than those that present a prevalence above 50%, indicating that toxoplasmosis is endemic in Brazil; this is also an indication of environmental contamination in the five regions of the country. The rate of positive dog studies varies, reflecting multifactorial factors such as different geographical scenarios, assay methodologies, sampling design, laboratory tests and study location (Olbera et al. 2020).

Control and prophylaxis measures lead to a low prevalence associated with the low prevalence of T. gondii in domestic dogs. Providing adequate food and filtered water is the primary measure to avoid infection. In cases where natural food is necessary, guidance on pre-freezing meat and adequate cooking is crucial. Furthermore, adequate hygiene of fruits and vegetables offered to the animal is recommended (Dubey 2022). Adopting practices such as restricting animals’ access to places possibly contaminated by oocysts or cohabited by potential infective definitive hosts can minimize dogs’ exposure to T. gondii. Veterinarians have an essential role in clinical work and guiding those responsible for disseminating prophylactic information that contributes to public health.

Wild Carnivores

The order Carnivora comprises approximately 280 species (Hudson et al. 2022). Brazil has 28 native species of carnivores, 10 from the Felidae and six from the Canidae family. Felidae from Brazil are Geoffroy’s cat (Leopardus geoffroyi), southern tiger cat (Leopardus guttulus), northern tiger cat (Leopardus tigrinus), margay (Leopardus wiedii), Pampas cat (Leopardus braccatus), Uruguayan pampas cat (Leopardus munoai), ocelot (Leopardus pardalis), jaguarundi (Herpailurus yagouaroundi), mountain lion (Puma concolor), jaguar (Panthera onca) (Instituto Pró-Carnívoros 2024). Canidae from Brazil are crab-eating fox (Cerdocyon thous), short-eared dog (Atelocynus microtis), bush dog (Speothos venaticus), Pampas fox (Lycalopex gymnocercus), maned wolf (Chrysocyon brachyurus), hoary fox (Lycalopex vetulus) (ICMBio 2024, Instituto Pró-Carnívoros 2024). These wild species play an essential ecological role, such as controlling herbivores and smaller carnivorous populations, dispersing seeds and maintaining local flora (Lial et al. 2022).

Brazil’s vast biodiversity is under threat due to increasing urbanization and agricultural activities. These human interventions bring domestic animal populations closer to wild animals, spreading infectious agents like Toxoplasma gondii to new species and areas (Padilha et al. 2021). Climate change has caused devastating changes in ecosystems and facilitated the emergence and expansion of pathogens. Understanding the complex reasons behind these phenomena is crucial for preventing and mitigating diseases in various hosts (Zhu et al. 2023). Emerging infectious diseases are considered a serious threat to biodiversity (Sacristán et al. 2021). The dependence of wild carnivores on large landscapes for shelter, reproduction, and hunting makes these species vulnerable to habitat loss, modification, and fragmentation. Furthermore, landscape transformation favors the spread of various pathogens (Lial et al. 2022). Wildlife is directly related to the stability of the entire ecosystem, playing a fundamental role throughout the biological world (Wei et al. 2021).

The circulation of various pathogens in wild nature is a topic that has been highlighted under the One Health approach. Therefore, carnivores are essential in this sense, as they are considered examples of biomagnification and bioaccumulation of pathogens, potentially acting as sentinel hosts and environmental indicators (Padilha et al. 2021). Regarding the T. gondii protozoan, these animals are considered sentinels for contamination of the environment (Dubey 2022).

In wild animal populations, observing healthy animals suggests that asymptomatic or subclinical infections may occur. Wild populations’ infection routes include consuming animals infected with T. gondii, especially when dealing with carnivores through predation or direct ingestion of oocysts shed by the definitive host, contaminating the environment. Another form of transmission is the transplacental form, in which tachyzoites cross the transplacental barrier, infecting the fetus (Aguirre et al. 2019, Dubey 2022).

Diagnosing and preventing toxoplasmosis in wild animals is challenging, especially from free-ranging origin (Padilha et al. 2021). The detection of anti-T. gondii in wild animals is extremely difficult, and for this surveillance to become part of the routine, much human and financial effort is required (González-Barrio et al. 2024).

Wild Felids

Wild felids are definitive hosts of Toxoplasma gondii, capable of shedding oocysts to the environment when infected (Dubey 2022). In Brazil, there are few reports of seroprevalence in wild felids, most carried out in captive animals (Fig. 1 and Table 3). Ten seroepidemiological studies were carried out to detect anti-T. gondii in 13 different species of free-ranging or captive neotropical felids. Various serological tests, predominantly the MAT, were used due to the highest sensitivity and specificity for T. gondii antibody detection (Dubey 2022).

Table 3.
Seroepidemiological survey for toxoplasmosis in wild (native and exotic) felids in Brazil

Species	State	Origin	N	Reactive (%)	Test	Dilution	Reference
Tiger (Panthera tigris)	Distrito Federal/São Paulo/Mato Grosso	Under human care	6	66.7	IFAT	1:40	André et al. (2010)
Lion (Panthera leo)	Distrito Federal/São Paulo/Mato Grosso	Under human care	9	55.5	IFAT	1:40	André et al. (2010)
	São Paulo	Under human care	3	100.0	MAT	1:64	Marujo et al. (2017)
Leopard (Panthera pardus)	Distrito Federal/São Paulo/Mato Grosso	Under human care	1	100.0	IFAT	1:40	André et al. (2010)
Jaguar (Panthera onca)	Several	Under human care	212	83.0	MAT	1:25	Silva et al. (2007)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	13	84.6	IFAT	1:40	André et al. (2010)
	Mato Grosso	Wildlife	10	90.9	IFAT	1:16	Onuma et al. (2014)
	São Paulo	Under human care	3	100.0	MAT	1:64	Marujo et al. (2017))
	Sergipe	Under human care	1	100.0	MAT	1:25	Pimentel et al. (2009)
Common genet (Genetta genetta)	Distrito Federal/São Paulo/Mato Grosso	Under human care	1	100.0	IFAT	1:40	André et al. (2010)
Puma (Puma concolor)	Several	Under human care	172	48.0	MAT	1:25	Silva et al. (2007)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	18	77.8	IFAT	1:40	André et al. (2010)
	São Paulo	Wildlife	2	50.0	MAT	1:40	Silva et al. (2014)
	São Paulo	Under human care	3	33.3	MAT	1:64	Marujo et al. (2017)
Oncila (Leopardus tigrinus)	Several	Under human care	131	50.0	MAT	1:25	Silva et al. (2007)
	Paraná	Under human care	22	68.1	MAT	1:16	Ullmann et al. (2010)
	São Paulo	Under human care	15	37.0	MAT	1:64	Marujo et al. (2017)
Geoffroy’s cat (Leopardus geoffroyi)	Several	Under human care	168	58.0	MAT	1:25	Silva et al. (2007)
	Paraná	Under human care	1	100.0	MAT	1:16	Ullmann et al. (2010)
Ocelot (Leopardus pardalis)	Several	Under human care	168	58.0	MAT	1:25	Silva et al. (2007)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	42	66.7	IFAT	1:40	André et al. (2010)
	Pará/Rio Grande do Norte	Under human care	3	100.0	MAT	1:25	Minervino et al. (2010)
	Paraná	Under human care	14	71.4	MAT	1:16	Ullmann et al. (2010)
	Rio de Janeiro	Under human care	2	50.0	MAT	1:16	Villar-Echarte et al. (2021)
	São Paulo	Under human care	4	50.0	MAT	1:64	Marujo et al. (2017)
Northern tiger cat (Leopardus tigrinus)	Distrito Federal/São Paulo/Mato Grosso	Under human care	35	62.8	IFAT	1:40	André et al. (2010)
	Paraná	Under human care	22	68.1	MAT	1:16	Ullmann et al. (2010)
Margay (Leopardus wiedii)	Several	Under human care	63	54.0	MAT	1:25	Silva et al. (2007)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	4	100.0	IFAT	1:40	André et al. (2010)
	Paraná	Under human care	17	58.8	MAT	1:16	Ullmann et al. (2010)
Pampas cat (Oncifelis colocolo)	Several	Under human care	72	48.0	MAT	1:25	Silva et al. (2007)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	3	33.3	IFAT	1:40	André et al. (2010)
Jaguarundi (Herpailurus yagouaroundi)	Several	Under human care	99	46.0	MAT	1:25	Silva et al. (2007)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	25	40.0	IFAT	1:40	André et al. (2010)
	Paraná	Under human care	3	66.6	MAT	1:16	Ullmann et al. (2010)

• IFAT = indirect fluorescent antibody test, MAT = modified agglutination test.

Considering Brazilian territory, a concentration of wild felid studies on toxoplasmosis was observed in decreasing order in the Midwest, Southeast, Northeast, South and North regions. The Midwest region comprises the Pantanal wetland, a critical biome for jaguar conservation, as it harbors the second-largest population in the world. The average seroprevalence of free-living populations with values above 50%, reaching up to 100%, demonstrates the circulation of T. gondii in wild felid populations in Brazil. In felids living in captivity, seroprevalence ranged from 30% to 100%, showing that, even in captivity, they had contact with the protozoan at some point (Ullmann et al. 2010). Felids are excellent predators, and carnivory is the main route of T. gondii infection within the food chain (Dubey 2022). However, the possibility of infection by ingesting oocysts that can contaminate the environment, and water cannot be ruled out. The infection occurs in all species of wild felids. A study carried out by Ullmann et al. (2010) concluded that free-ranging felids are more likely to be infected than animals living in zoos, indicating that the ingestion of oocysts or cyst tissue occurs in nature.

Based on existing reports, T. gondii circulates widely among neotropical and exotic felid populations in zoos and conservation centers. Serological, molecular and biological studies on various wild animal species have documented the protozoan circulation at different trophic levels (Cañón-Franco et al. 2013). Although laboratory studies investigate the route of infection and elimination of oocysts when dealing with wild felids, many questions require further investigation. It is necessary to understand the frequency and amount of oocyst shedding, as oocysts in the environment are also a source of infection and can impact bradyzoite transmission by ingesting tissue cysts (Zhu et al. 2022).

Prophylactic measures to prevent infection of felids living in captivity, such as zoos, can be carried out. These measures include protecting the facilities to prevent contact between domestic cats, rodents, and birds and the animals’ enclosure, as well as preventing owners from carrying oocysts on their shoes, thus providing disposable boot covers as a protective measure (Spriggs et al. 2020, Dubey 2022). Other forms of prophylaxis, such as veterinary care, monitoring the quality of the water offered, and drainage control to prevent rainwater from running off and carrying oocysts to the enclosures, are also effective. However, the essential way to prevent toxoplasmosis in felids in captivity is to control their diet. Under no circumstances should these animals be fed fresh meat or raw bones. Ideally, frozen meat should be offered, as it is less infectious, and beef should be preferred over lamb or pork (Dubey 2022).

Attention must be paid to the reproduction of felids in captivity. Basso et al. (2005) reported T. gondii infection in puppies that ingested oocysts that were present in the female’s feces. It is suggested that feline feces be removed from the enclosure daily to prevent the oocyst from being able to sporulate in the enclosure (Spriggs et al. 2020). Furthermore, the female must be monitored during pregnancy to ensure that transplacental transmission does not occur (Dubey 2022).

Wild Canids

The reports of toxoplasmosis in wild canid species are still limited. Reports on seroprevalence listed 14 surveys from seven species of wild canids in Brazil (Fig. 1 and Table 4). Around five research studies were carried out on captives, eight on free-ranging canids, and one on captives and free-ranging canids. Considering all studies, canids’ seropositivity varies from 7.6% to 75%. Considering the environment, research on captive animals is almost 50% greater than on free-ranging canines. Reports on captive animals are more frequent due to the efficient collection of samples. However, free-living wild canids have lower seropositivity rates than captive ones. It is highlighted that Toxoplasma gondii is widely disseminated in these populations, and that at some point, these canids had contact with the protozoan through environmental contamination, contaminated water, or even through their eating habits, depending on the species, such as contaminated fruit and infected meat (Dubey 2022).

Table 4.
Seroepidemiological survey of toxoplasmosis in wild (native and exotic) canids in Brazil

Species	State	Habitat	N	Reactive (%)	Test	Dilution	Reference
Bush dog (Speothos venaticus)	Distrito Federal/São Paulo/Mato Grosso	Under human care	27	63.0	IFAT	1:40	André et al. (2010)
Crab-eating fox (Cerdocyon thous)	Several	Wildlife	15	60.0	IFAT	1:16	Gennari et al. (2004)
	Several	Under human care	25	36.0	IFAT	1:50	Mattos et al. (2008)
	Distrito Federal	Wildlife	7	71.4	MAT	1:25	Proença et al. (2013)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	39	35.9	IFAT	1:40	André et al. (2010)
	Minas Gerais	Wildlife	10	70.0	MAT	1:25	Curi et al. (2010)
	Goiás	Wildlife	13	7.6	MAT	1:16	Carneiro et al. (2014)
	Northeast	Under human care and wildlife	25	36.0	MAT	1:25	Almeida et al. (2018)
	São Paulo	Under human care	52	19.2	MAT/IFAT	1:16	Catenacci et al. (2014)
	São Paulo	Wildlife	3	33.3	MAT	1:10	Silva et al. (2014)
	São Paulo	Under human care	11	27.2	MAT	1:16	Marujo et al. (2017)
	Rio Grande do Sul	Wildlife	30	13.0	IHA	1:64	Padilha et al. (2021)
Hoary Fox (Lycalopex vetulus)	Distrito Federal/São Paulo/Mato Grosso	Under human care	7	71.4	IFAT	1:40	André et al. (2010)
	São Paulo	Wildlife	6	16.6	MAT	1:10	Silva et al. (2014)
	São Paulo	Under human care	7	14.2	MAT	1:16	Marujo et al. (2017)
Pampas fox (Lycalopex gymnocercus)	Several	Wildlife	12	91.7	IFAT	1:16	Gennari et al. (2004)
	Several	Under human care	5	60.0	IFAT	1:50	Mattos et al. (2008)
	Rio Grande do Sul	Wildlife	22	36.4	IHA	1:64	Padilha et al. (2021)
Maned wolf (Chrysocyon brachyurus)	Several	Under human care	14	71.4	IFAT	1:50	Mattos et al. (2008)
	Bahia	Wildlife	11	54.0	IFAT	1:32	Gomes et al. (2024)
	Brasília	Under human care	7	100	ELISA	1:64	Vitaliano et al. (2004)
	Distrito Federal/São Paulo/Mato Grosso	Under human care	21	54.2	IFAT	1:40	André et al. (2010)
	Minas Gerais	Under human care	35	80.0	ELISA	1:64	Vitaliano et al. (2004)
	Gerais	Wildlife	7	85.0	MAT	1:25	Curi et al. (2010)
	Minas Gerais	Wildlife	8	75.0	MAT	1:25	Curi et al. (2012)
	São Paulo		17	88.2	IFAT	1:16	Oliveira et al. (2016)
	São Paulo	Under human care	3	100.0	MAT	1:64	Marujo et al. (2017)

• IFAT = indirect fluorescent antibody test, MAT = modified agglutination test, ELISA = enzyme-linked immunosorbent assay.

Data are predominant from the Southeast region in the reports. The state of São Paulo demonstrates a high prevalence in this region, followed by the Northeast, Midwest, and South regions of Brazil with high prevalence rates, proving that toxoplasmosis is widely disseminated in Brazil (Pinto-Ferreira et al. 2019). Further investigation into these canid populations is needed, as they are considered sentinels (Dubey 2022). Wild canids have a close genetic relationship with domestic dogs, and intense contact with urban environments can favor the potential transmission of pathogens (Padilha et al. 2021). The role of T. gondii in the Brazilian Biomes has still not been explored.

Studies indicate that the increased fragmentation of environments may influence the occurrence of fatal accidents in wild animals, which, in general, may be linked to the development of infectious diseases (Souza et al. 2022). Disseminated toxoplasmosis in wild canines is rarely reported; these animals present non-specific clinical signs when it occurs concomitantly with immunosuppressive diseases, such as canine distemper (Pepper et al. 2019). In a study with maned wolves in Brazil, T. gondii infection was identified concomitantly with the canine distemper virus (Souza et al. 2022) as occurs in domestic dogs, demonstrating that the population of wild canines, although not know a lot about the pathogenesis of toxoplasmosis in these species, it is also subject to disseminated infection caused by the protozoan. Identifying highly recombinant T. gondii genotypes in Brazil (Dubey 2022), which have been associated with increased virulence, may alter the epidemiological dynamics and clinical outcomes in both domestic and wild hosts.

Whereas the effects of T. gondii infection in most intermediate hosts are known, these effects have been little studied in wild canid populations. Research demonstrated that gray wolves infected by T. gondii showed changes in their behavior, becoming more “courageous”, thus dispersing and more likely to become pack leaders than seronegative wolves. T. gondii infection can affect behavior and decision-making in wild intermediate host species (Gering et al. 2021). One of Brazil’s most significant concerns regarding the preservation of wild canids is the high incidence of motor vehicle collisions involving these species on highways. It was noted that wolves that tested anti-T. gondii-positive were more inclined to make poor decisions, and these decisions impacted the animal’s fitness. However, there was a lack of correlation when they associated seropositivity with motor vehicle collisions (Gering et al. 2021, Dini et al. 2024).

Regarding wild canid toxoplasmosis prophylaxis, it is challenging to control the diet and environment of these carnivores. In this sense, preserving the biodiversity of natural habitats is an indirect focus to prevent disease transmission (Padilha et al. 2021). Controlling the access of cats near the enclosures and the water source offered is possible in canids from zoological gardens. In this way, some measures such as protection of enclosures, freezing of meat for at least three days before offering, cleaning of fruits that are part of the diet of some species, control of water quality and guidance to owners can be carried out to avoid contamination of the environment and consequent infection of canids.

Discussion

The seroprevalence of anti-Toxoplasma gondii in domestic cats in many Brazilian regions is high. We hypothesize that the cat’s and the owner’s habits can justify this result. It is widespread for owners to think that the cat is an animal that must live “free”. This behavior is harmful, as there is no control over what the animal is hunting and ingesting outside, and if it becomes infected, it will contaminate the environment, shedding millions of oocysts. Another fact is that raw or undercooked meat and unfiltered water are provided for cats, which is very common among owners in Brazil (Benitez et al. 2017, Dubey 2022). As in domestic cats, seroprevalence in domestic dogs is also high. Many dog owners still let their dogs go for a “walk” without supervision, which increases the chances of infection, precisely due to the behavior of accessing trash and ingesting some infected meat or other contaminated food. Dogs are sentinels of environmental contamination by T. gondii; therefore, the high seroprevalence indicates an environment widely contaminated with oocysts. Providing unfiltered water and unsanitized food or raw meat is a risk factor for exposing the dog to the protozoan, as well as the infrequent cleaning of yards in which many of these pets are housed.

One of the challenging questions in conservation medicine is diagnosing diseases in wildlife-free-ranging individuals (Corrêa & Passos 2001). Reporting complete data on fatal cases of animal toxoplasmosis should be systematically investigated using techniques such as physical examination, necropsy, histopathology, immunohistochemistry, Polymerase Chain Reaction (PCR), microsatellite techniques, genotyping and cytological examination of cerebrospinal fluid (Pena et al. 2017, Dubey 2022).

Discussing the epidemiological maps from this review, we suggest that regions presenting significant toxoplasmosis diagnoses in both wild and domestic carnivores are associated with greater diagnostic capacity or research. Veterinary Diagnostic Laboratories have contributed fundamentally to diagnosing animal diseases. Even so, there are large areas of the country where information regarding animal health is limited (Riet-Correa et al. 2025).

The major highlight of this review was the different occurrences of seropositivity of free-ranging felids and canids. Free-ranging felids are more likely to be infected by T. gondii than felids living in captivity. Free-ranging wild canids have lower seropositivity rates compared to those in captivity. Many studies should verify these issues to contribute to conservation medicine. The literature data compiled in this review allow us to hypothesize that habits of free-ranging wild felid species, such as feeding on small rodents, increase the chance of consuming prey infected with T. gondii, besides contact with other felid species’ feces. The low prevalence of captive felids can be explained by good hygiene and management practices in the zoos where they live, thereby reducing contact with T. gondii. The high seropositivity in wild canids in captivity seems to have a high frequency of contamination with oocysts in the zoo environment due to the proximity of felid enclosures (Dubey et al. 2020a, Dubey 2022).

Conclusions

Toxoplasma gondii infections are widespread among domestic and wild carnivores across all Brazilian regions. We suppose that regions presenting significant occurrence fit with greater diagnostic capacity or research in both domestic and wild carnivores. We agree on continuing diagnosis efforts by health and educational institutions to draw an epidemiologic scenario representing sampling from the whole country. The diagnosis of toxoplasmosis in carnivores must be established with serology, clinical findings, necropsy, histopathology and laboratory tests that confirm the presence of the protozoan in tissues with inflammatory and necrotizing lesions. Only serological tests for detecting antibodies indicate an immune response instead of clinical diseases.

Free-ranging felids are more likely to be infected by T. gondii than felids living in captivity. The free-living wild canids have lower seropositivity compared to the canids in captivity. Researching wildlife-free-ranging animals in Brazil is challenging due to logistical issues. The role of T. gondii in the Brazilian biomes should be better investigated.

This review brought relevant and updated information to understand the epidemiology of toxoplasmosis in Brazil’s domestic and wild carnivores, linking human, animal, and ecosystem health. Toxoplasmosis demands integrative approaches that break disciplinary boundaries to generate new approaches to managing and controlling the disease. Practitioners and researchers from medical and wildlife sciences could join in applying their expertise on One Health, aiming for public health authorities to raise awareness and implement prophylaxis measures.

Acknowledgment

To “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES) for granting scholarships, financing code 001. The authors thank Niriele B. Rodrigues from UFRuralRJ for elaborating on the maps. This publication was supported by resources from the approved Project related to the Basic Research Support Notice (APQ1) - 2023” (SEI-260003/003363/2023) from “Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro” (FAPERJ).

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• Data Availability
  Scientific literature was consulted to prepare the present review article. No datasets were generated or analyzed during the current study.

Data availability

Scientific literature was consulted to prepare the present review article. No datasets were generated or analyzed during the current study.

Publication Dates

• Publication in this collection
  06 Oct 2025
• Date of issue
  2025

History

• Received
  14 Mar 2025
• Accepted
  25 May 2025