Exposure of dogs and wild carnivores to canine distemper virus, canine parvovirus, Leishmania infantum, and Toxoplasma gondii in the Xingu River basin, Brazilian Amazon: Prevalence, spatial distribution, and association with land cover types

ABSTRACT

Infectious diseases transmitted by domestic dogs can have important consequences for wildlife health. This study aimed to investigate the exposure to four selected pathogens in dogs and wild carnivores in six municipalities in the Xingu River Basin (Pará state, Brazil). The prevalence of positive animals, their spatial distribution, and the association with land cover types were analyzed. Blood samples from 298 dogs and 11 free-ranging wild carnivores were tested through serological diagnoses. The seroprevalence to canine distemper virus, canine parvovirus, Leishmania infantum, and Toxoplasma gondii was 68.6, 75.4, 14.8, and 47.1%, respectively. The seroprevalence to canine distemper virus and T. gondii was significantly higher in dogs than in wild carnivores. Spatial analyses revealed a broad distribution of seropositive animals, except for animals seropositive to L. infantum, which were concentrated in the southern region close to the margins of the Xingu River. Spatial clusters of seropositive animals were detected for all tested pathogens, indicating areas with a greater risk of exposure. Positive results for canine distemper virus, T. gondii, and L. infantum were associated with different types of land cover, and thus were considered risk factors for pathogen exposure. The high seroprevalence of dogs to canine distemper virus and to canine parvovirus are concerning, suggesting risks of transmission to wild species inhabiting areas close to the surveyed communities.

KEYWORDS:
epidemiology; wildlife; risk factor; spatial analysis; zoonosis

RESUMO

Doenças infecciosas transmitidas por cães domésticos podem ter consequências importantes na saúde de animais silvestres. Este estudo objetivou investigar a exposição a quatro patógenos em cães e carnívoros silvestres em seis municípios da bacia do Rio Xingu (Pará, Brasil). A prevalência de animais positivos, sua distribuição espacial e a associação com tipos de cobertura do solo foram analisados. Amostras de sangue de 298 cães e 11 carnívoros silvestres de vida livre foram testados por diagnósticos sorológicos. As soroprevalências para o vírus da cinomose canina, vírus da parvovirose canina, Leishmania infantum e Toxoplasma gondii foram 68,6, 75,4, 14,8 e 47,1%, respectivamente. As soroprevalências para o vírus da cinomose canina e T. gondii foram significativamente maiores em cães do que em carnívoros silvestres. Análises espaciais revelaram uma ampla distribuição de animais soropositivos, exceto aqueles soropositivos para L. infantum, os quais se concentraram na região sul próximo às margens do Rio Xingu. Clusters espaciais de animais soropositivos foram detectados para todos os patógenos estudados, indicando áreas com maiores risco de exposição. Resultados positivos para o vírus da cinomose canina, T. gondii e L. infantum estiveram associados a diferentes tipos de cobertura do solo, que, portanto, foram considerados fatores de risco para a exposição aos patógenos. As elevadas soroprevalências de cães para o vírus da cinomose canina e para o vírus da parvovirose canina são preocupantes, sugerindo riscos de transmissão para espécies silvestres que habitam áreas próximas das comunidades investigadas.

PALAVRAS-CHAVE:
epidemiologia; animais selvagens; fatores de risco; análise espacial; zoonose

INTRODUCTION

Infectious diseases transmitted from domestic dogs to wild animals occur worldwide and have important implications for biodiversity conservation (Woodroffe et al. 2012). Infections do not necessarily cause host death but also symptoms that lead to a decline in populations, directly or indirectly, due to reduced competition capacity for hunting or escape from predators, infertility, altered secondary sex ratios and movement patterns, morbidity, and increased susceptibility to other infectious diseases (Preece et al. 2017). Canine distemper virus (CDV) in lions, Panthera leo (Linnaeus, 1758) (Mourya et al. 2019), canine parvovirus (CPV) in wolves, Canis lupus (Linnaeus, 1758) (Mech et al. 2008), and the rabies virus in African wild dogs, Lycaon pictus (Temminck, 1820) (Canning et al. 2019) are examples of pathogens that can cause diseases with substantial mortality rates in wildlife, including endangered species. These diseases are called the “Big Three” due to strongly negative impact on wild carnivores (Knobel et al. 2014). Wild canids are particularly susceptible to diseases carried by dogs since both animal groups are closely related (Woodroffe et al. 2004). The transmission routes of these events are difficult to elucidate (Blasio et al. 2019), but they most likely occur through direct contact between dogs and wildlife (Curi et al. 2010).

Disease transmission by dogs to wild species can be high under particular circumstances. Isolated communities of low socioeconomic status may have fewer healthy dogs that can become major reservoirs for the transmission of diseases to humans and sympatric wildlife (Fung et al. 2014). Factors associated with this condition may include limited resources to seek veterinary care services (including deworming and immunization), low access to transportation, lack of awareness and information regarding animal welfare, poor-quality food provided to dogs, and cultural habits. In addition, these threats to wildlife can have greater impacts in areas that are biodiversity hotspots, where diverse and numerous species occur. The Amazon region perfectly illustrates the abovementioned situation, with thousands of impoverished communities living in remote areas in one of the most biodiverse ecosystems in the world.

Among the diverse pathogens found in dogs, CDV is one of the most important that impairs wildlife health (Knobel et al. 2014). Several cases and outbreaks have been reported among diverse animal species worldwide, making canine distemper probably the most threatening disease of dog origin affecting wild carnivores (Knobel et al. 2014; Mourya et al. 2019). In Brazil, CDV outbreaks of large magnitude have not been described. However, severe cases have occasionally been reported, including in a hoary fox, Lycalopex vetulus (Lund, 1842), a lesser grison, Galictis cuja (Molina, 1758), coatis, Nasua nasua (Linnaeus, 1766), and felids (Puma concolor Linnaeus, 1771, Leopardus wiedii Schinz, 1821, and Herpailurus yagouaroundi Geoffroy Saint-Hilaire, 1803) (Megid et al. 2010; Megid et al. 2013; Michelazzo et al. 2020; Viana et al. 2020).

The present study was part of a project on the control of endemic diseases transmissible to wildlife, conducted during the construction of the Belo Monte Hydroelectric Dam (BMHD) in Pará state, Brazil. This project targeted communities that inhabit areas near the BMHD, and aimed to assess the level of exposure of domestic and wild animals to the following pathogens: CDV, CPV, Leishmania infantum (Nicolle, 1908) (synonym to Leishmania chagasi), and Toxoplasma gondii (Nicolle & Manceaux, 1908). Other goals included the spatial distribution of positive and negative animals and their association with different land cover types.

MATERIAL AND METHODS

Study area

Six municipalities located in the lower Xingu River were surveyed between November 2011 and September 2015: Altamira, Porto de Moz, Senador José Porfírio, Anapu, Brasil Novo, and Vitória do Xingu (Figure 1). The geographical characteristics of the region are typical of the Amazon biome, with dense tropical forests, equatorial climate, high precipitation levels, low population density, and high deforestation levels. At the time of our survey, most communities were of low socioeconomic status with inadequate sanitary conditions.

Figure 1
Map of the study region where dogs and wild carnivores were sampled for diagnosis of infectious diseases in the lower Xingu River basin, Pará state, Brazil. This figure is in color in the electronic version.

Animals and samples

Blood samples were collected from 298 dogs and transported to the BMHD station for storage (-20^oC) until laboratory diagnosis. Most dogs were apparently healthy, but several showed clinical abnormalities of multiple origins, including malnutrition, ectoparasites, apathy, dermatitis, old bone fractures, and pelvic paralysis. Vaccination status was reported by the owners of 107 dogs but only against rabies. Most dogs roamed freely and had access to the forest environment and surrounding community areas.

Eleven free-ranging wild carnivores were captured from wildlife rescue activities during vegetation suppression in the areas destined for the water reservoir (Table 1). The animals that required captive management actions for biometric data collection, tagging, and translocation were sampled for this study. Blood samples were collected when the animals were chemically restrained.

Table 1
Data from wild carnivores surveyed in the lower Xingu River basin (Pará state, Brazil) and results of serological tests for canine distemper virus (CDV), canine parvovirus (CPV), Leishmania infantum, and Toxoplasma gondii.

Species	Common name	Family	Sampling date	Age class	Sex	Weight (kg)	Author id code	Laboratory diagnosis (serological titer)
								CDV	CPV	L. infantum	T. gondii*
Cerdocyon thous (Linnaeus, 1766)	Crab-eating fox	Canidae	10 Sep 2012	Adult	M	5.16	203	Negative	Positive (40)	Negative	Negative
Speothos venaticus (Lund, 1842)	Bush dog	Canidae	14 Jan 2012	Adult	M	4.98	31	Positive (40)	Positive (40)	Negative	Negative
			14 Jan 2014	Subadult	M	3.2	451	Negative	Negative	Negative	Positive
Eira barbara (Linnaeus, 1758)	Tayra	Mustelidae	21 Oct 2011	Young	F	2.18	97	Negative	Negative	Negative	Negative
			21 Oct 2011	Young	F	2.15	98	Negative	Negative	Negative	Negative
			17 May 2014	Subadult	M	2.9	502	Positive (40)	Positive (40)	Negative	Negative
Lontra longicaudis (Olfers, 1818)	Neotropical otter	Mustelidae	09 Nov 2012	Young	F	4.3	369	Negative	Positive (40)	Negative	Negative
			03 Sep 2013	Young	M	3.73	441	Negative	Positive (40)	Negative	Negative
Potos flavus (Schreber, 1774)	Kinkajou	Procyonidae	10 Apr 2013	Adult	F	1.66	330	Negative	Positive (40)	Negative	Negative
			02 Jun 2015	Adult	F	1.5	666	Negative	Negative	Negative	Negative
Procyon cancrivorus (G. Cuvier, 1798)	Crab-eating raccoon	Procyonidae	27 Dec 2014	Cub	M	0.3	595	Negative	Negative	Negative	Negative

• *Endpoint titer could not be performed (32 was used as the cutoff point)

The location of the wild carnivores and dogs was georeferenced using a GPS device for later spatial analyses. All procedures were approved by the Brazilian Institute of Environmental and Renewable Natural Resources (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis - IBAMA, process 02001.001848/2006-75).

Laboratory diagnosis of pathogens

Exposure to CDV, CPV, L. infantum, and T. gondii was assessed through antibody detection using serological tests performed by the TECSA^® laboratory (Belo Horizonte, Minas Gerais state, Brazil). Detailed information on the laboratory tests and protocols are protected by the laboratory’s privacy policy and cannot be published. Because of the limited sample availability for laboratory tests, diagnosis of CDV, CPV, and T. gondii could not be performed in 44 domestic dogs.

Diagnosis of CDV and CPV was performed by the detection of IgG antibodies using immunochromatography tests with a dilution 1:40 as the cut-off titer. Exposure to L. infantum was investigated using indirect immunofluorescent antibody tests (IFATs) and enzyme-linked immunosorbent assays (ELISA) to detect IgG. For IFATs, a dilution of 1:40 was considered the cut-off point, whilst the ELISA is a qualitative test that yields negative or positive results. Exposure to L. infantum was considered when an animal tested positive in at least one of the two tests. Exposure to T. gondii was assessed using IFATs to detect IgM and IgG antibodies with a dilution of 1:32 as the cut-off point. Exposure to T. gondii was considered when an animal tested positive in at least one of the two tests. Dogs and wild carnivores were tested using the same diagnostic techniques, which employed anti-dog conjugates. Except for T. gondii, the endpoint titers of seropositive samples were determined. Standardized serological tests for different wild species are extremely scarce; therefore, we used laboratory tests that employed conjugates against the immunoglobulins of domestic dogs, which are phylogenetically close to wild carnivores, as in previous epidemiological studies (Clifford et al. 2006; Brandão et al. 2020).

Spatial analysis

Cluster analyses were performed independently for each pathogen to assess the spatial prevalence of seropositive animals and identify areas with high risk of exposure. The animals were classified as cases (seropositive) and controls (seronegative), and the rates of pathogen prevalence within circles of various sizes were calculated using statistical modeling and the Bernoulli distribution. This test compares the hypothesis that the risk of being positive is greater within the circle with the hypothesis that the risk is equal inside and outside the circle, and significance was set at 5%. The scan statistics method was applied as described by Kulldorff and Nagarwalla (1995) using the SaTScan^TM 9.5 software. Prevalence inside and outside the clusters was compared using the chi-square test or Fisher’s exact test using R v.3.6.1. The circle with the maximum value of the likelihood ratio was considered the most probable cluster (Kulldorff 1997; Wheeler 2007; Pfeiffer et al. 2008) and was represented on the map using the QGIS v.3.8 software.

Association with land cover types

The habitat of each animal’s origin was explored as risk factors for pathogen exposure and were investigated by comparing with laboratory tests results. The analyzed variables consisted of the types of land cover and soil use (LCSU) present in the studied region, such as forest formation, tree farming, floodplain, pasture, agriculture (soybean, sugar cane, and rice), urban infrastructure, and water bodies. Data were retrieved from the MapBiomas v.5.0 platform (as raster image of 30 m resolution, 4.0 collection), which makes the catalog of images of Brazil with different categories of LCSU publicly available (MAPBIOMAS 2022). QGIS v.3.8 software was used to create a 3 km radius buffer area around each animal’s origin (28.3 km²), which was assumed to be their home range (Jesus et al. 2023). The proportion of each LCSU type of in the raster image within the buffer area of each animal was calculated. The variables were compared with the laboratory tests results (seropositive or seronegative) for each disease. The normality of data was analyzed using the Shapiro-Wilk test, followed by the non-parametric Mann-whitney U test, both performed in R v.3.6.1.

RESULTS

The seroprevalence of CDV, CPV, L. infantum, and T. gondii was 68.6, 75.4, 14.8, and 47.1%, respectively. Seroprevalence for CDV and T. gondii was significantly higher in dogs than in wild carnivores. CPV was the pathogen with the highest prevalence in all specimens tested and in each animal group (Table 2).

Table 2
Results of serological tests for canine distemper virus (CDV), canine parvovirus (CPV), Leishmania infantum, and Toxoplasma gondii in dogs and wild carnivores in six municipalities of the lower Xingu River basin (Pará state, Brazil).

Pathogens	Dogs				Wild carnivores			Difference between prevalence*	Total
	N	Positive	% (CI 95%)		N	Positive	% (CI 95%)		N	Positive	% (CI 95%)
CDV	254	180	70.8 (64.8 - 76.3)		11	2	18.2 (2.3 - 51.7)	< 0.001	265	182	68.6 (62.7 - 74.2)
CPV	254	194	76.3 (70.6 - 81.4)		11	6	54.5 (23.4 - 83.2)	0.19	265	200	75.4 (69.8 - 80.5)
L. infantum	298	46	15.4 (11.5 - 20.0)		11	0	0 (0.0 - 28.5)	0.25	309	46	14.8 (11.1 - 19.3)
T. gondii	254	124	48.8 (42.5 - 55.1)		11	1	9.1 (0.2 - 41.3)	0.023	265	125	47.1 (41.0 - 53.3)

• N: Number of animals tested. % (CI 95%): confidence interval. *p value.

Thirty-nine dogs were seropositive to L. infantum using both ELISA and IFAT, whereas four dogs were seropositive using ELISA and three using IFAT. Regarding the IFAT for T. gondii, 122 seropositive animals were reactive to IgG antibodies, and two (dogs) were reactive to both IgM and IgG. Among dogs, the serological titers for CDV were 40 (n = 97), 80 (n = 21), 160 (n = 30), and ≥ 320 (n = 32); for CPV, they were 40 (n = 64), 80 (n = 28), 160 (n = 44), and ≥ 320 (n = 58); and for L.infantum (IFAT), they were 40 (n = 15), 80 (n = 26), and 160 (n = 1).

The spatial analysis revealed a wide geographical distribution of animals seropositive to CDV, CPV, and T. gondii. All animals seropositive to L. infantum were concentrated in the southern region of the study area, in localities close to the margins of the Xingu River (Figure 2). Significant clusters of seropositive animals were detected for all pathogens tested. L. infantum was the only pathogen with three clusters, with one cluster (Cluster 1) presenting the highest relative risk (9.1) among all tested pathogens (Table 3). This result indicates a 9.1-fold higher risk of becoming exposed inside the cluster than outside, despite the prevalence inside the cluster being only 24.1%. The prevalence in CDV and CPV clusters was 100 and 97.8%, respectively.

Figure 2
Spatial clusters of dogs and wild carnivores seropositive to canine distemper virus, canine parvovirus, Leishmania infantum, and Toxoplasma gondii in the lower Xingu River basin, Pará state, Brazil. This figure is in color in the electronic version.

Table 3
Data from spatial clusters of dogs and wild carnivores seropositive to canine distemper virus (CDV), canine parvovirus (CPV), Leishmania infantum, and Toxoplasma gondii in six municipalities of the lower Xingu River basin (Pará state, Brazil).

Clusters data	CDV	CPV	L. infantum			T. gondii
			Cluster 1	Cluster 2	Cluster 3
Prevalence inside the cluster	100% (23/23)	97,8% (44/45)	24,1% (35/145)	28,8% (23/80)	37,8% (14/37)	62,1% (77/124)
Expected cases	15.8	34	19.2	10.6	4.9	58
Relative risk	1.5	1.4	9.1	3.9	3.9	1.9
Log likelihood ratio	9.1	10.2	16.6	10.3	8.6	11.1
P-value	0.014	0.003	<0.001	0.003	0.016	0.001
Prevalence outside the cluster	65.7% (159/242)	88.6% (156/176)	26.7% (4/15)	8.3% (16/192)	10.2% (25/244)	73.4% (47/64)

Animals seropositive to CDV were associated with areas of pasture (p = 0.015) and a few water bodies (p < 0.03), but not with floodplains and forest formations (Figure 3; Table 4). Seropositivity to L. infantum was positively associated with areas of floodplains (p < 0.001) and forest formations (p < 0.001) and negatively associated with pastures (p < 0.001); the only variable that did not reach statistical significance was water bodies. Seropositivity to T. gondii was positively associated with pasture areas (p < 0.001) and negatively associated with floodplains (p < 0.001), forest formations (p < 0.001), and water bodies (p < 0.001). Seropositivity to CPV did not show significant association with floodplains, pastures, forest formations or agricultural areas. Agricultural areas, urban infrastructure, and tree farming areas showed a median of 0% at the buffers of seropositive and seronegative dogs; thus, they were not considered in the analysis. It is important to note that LCSU types such as urban infrastructure, agriculture, and tree farming are rare in the studied region, and their median area around seropositive and seronegative dogs for all pathogens was equal to zero (Table 4). Thus, although some types were significant (p < 0.05) in the analysis, we did not consider them as representative.

Figure 3
Correlation between the occurrence of dogs seropositive to canine distemper virus with three land cover types in the lower Xingu River basin, Pará state, Brazil. The results of the remaining land cover types are omitted. This figure is in color in the electronic version.

Table 4
Association of the type of land cover with serological tests for canine distemper virus (CDV), canine parvovirus (CPV), Leishmania infantum, and Toxoplasma gondii in dogs and wild carnivores in six municipalities of the Xingu River basin (Pará state, Brazil).

Coverage	CDV					CPV					L. infantum					T. gondii
	Median of area (%)		MW-U	p-value		Median of area (%)		MW-U	p-value		Median of area (%)		MW-U	p-value		Median of area (%)		MW-U	p-value
	+	-				+	-				+	-				+	-
River floodplain	0.3	0.86	7468	0.883		0.89	0.285	6197	0.572		5.17	0.57	1593	< 0.001		0.57	1.73	6417	< 0.001
Pasture	36.7	28.4	6149	0.015		32.7	33.8	6357	0.790		9.16	35.1	1419	< 0.001		43.6	22.6	5037	< 0.001
Forest formation	43.2	42.7	7059	0.393		43.9	39.6	6346	0.774		54.5	40.9	1503	< 0.001		38.5	45.3	6635	< 0.001
Water bodies	14.9	24.1	6308	0.031		16.6	20.7	6156	0.521		30.5	16.2	3049	0.148		6.49	28.6	6176	<0.001
Agriculture	0	0	8306	0.006		0	0	6929	0.26		0	0	4098	0.0818		0	0	8689	0.906
Urban	0	0	9279	<0.001		0	0	7701	0.002		0	0	2821	0.005		0	0	10653	<0.001
Tree farming	0	0	7311	0.133		0	0	6460	0.791		0	0	4130	<0.001		0	0	8308	0.012

• +: positive. -: negative. MW-U: Mann Whitney U statistic.

DISCUSSION

The high seroprevalence of CDV and CPV in dogs was surprising and indicates the broad circulation of these pathogens. The small number of wild carnivores sampled hinders major conclusions at the population level; thus, the following discussion focuses mainly on dogs. Seroprevalence studies in Brazil are scarce, especially in the Amazon region, which limits comparisons with our results. The lack of data is particularly noticeable in the case of spatial analyses and risk factor assessments. This is one of the first studies to explore diverse pathogens in a large sample size of domestic dogs in the Brazilian Amazon.

Severe cases of CDV infection in free-ranging carnivores have been described in Brazil (Megid et al. 2010; Megid et al. 2013; Michelazzo et al. 2020; Viana et al. 2020). Antibodies against CDV in unvaccinated dogs have been reported with prevalence rates of 66 and 71.4% in Goiás and Minas Gerais states, respectively (Curi et al. 2010; Furtado et al. 2016), indicating high exposure levels and the presence of infected animals as potential sources of infection. The reported rates are very similar to the seroprevalence detected in the present study (70.8%). Such a high frequency of exposure is alarming, suggesting recurrent infections in the population and their possible role as a source of infection for wild species. One of the few assessments in the Brazilian Amazon detected 27% (27/101) of dogs seropositive to CDV in Pará state (Whiteman et al. 2007). In the Bolivian Amazon, Fiorello et al. (2004) found an expressive seroprevalence of 92% in dogs from the borders of Madidi National Park. Comparison of prevalence rates between studies should be cautious due to methodological differences. Nonetheless, studies have shown that CDV is widely distributed in Brazil and other South American countries and should be the focus of great concern for wildlife conservation. Although CDV seroprevalence was higher in dogs than in wild carnivores, we should also consider that wild carnivores can maintain enzootic cycles of CDV and transmit it to susceptible dogs (Prager et al. 2012).

Although CPV is less life-threatening to wildlife than CDV, carnivores have been affected by CPV in southeastern Brazil and northeastern Argentina (Bucafusco et al. 2019; Spera et al. 2020, Spera et al. 2021). The detected 75.4% seroprevalence corroborates the results of previous studies, demonstrating that CPV is highly prevalent in Brazilian dog populations. In southeastern Brazil, seroprevalences as high as 100 and 97% were found in dogs living close to environmentally protected areas (Curi et al. 2010; Curi et al. 2016). Studies on CPV in the Brazilian Amazon region are rare. Courtenay et al. (2001) reported that 13% (3/23) of dogs from Marajó, Pará state, Brazil, were seropositive; and a seroprevalence of over 90% was found in the Bolivian Amazon (Fiorello et al. 2004, Fiorello et al. 2006). Therefore, CPV is a common pathogen in dogs in Brazil, with evidence of particularly high exposure rates in some areas at the interface between domestic and wild species.

Leishmania infantum is the etiological agent of visceral leishmaniasis (VL), a zoonotic disease of great concern to human and animal health worldwide, with domestic dogs acting as the main reservoir. Brazil is endemic for VL, with varying levels of endemism across its immense territory. VL is expanding geographically in the Amazon biome, especially in Pará state. The 14.8% seroprevalence that we detected corroborates previous investigations in dogs from Pará, which reported 23.3 and 43% seropositivity (Valadas et al. 2010; Silveira et al. 2012). Additionally, among the six municipalities surveyed, two (Vitória do Xingu and Anapu) had sporadic cases of human VL according to the Notifiable Diseases Information System (SINAN, 2021) (i.e., the two municipalities accounted for five cases of VL between 2016 and 2019). Our results confirm infection by L. infantum in dogs from Pará state; moreover, indicate the presence of this parasite in remote areas occupied by communities of low socioeconomic status.

Similar to L. infantum, seroprevalence studies of T. gondii in dogs are especially important in a public health context. The frequency of antibodies in dogs indicates the level of environmental contamination by parasitic oocysts, thus indicating the risk of human exposure (Olbera et al. 2020). Toxoplasma gondii is one of the most studied parasites in dogs, and Brazil, including the Amazon biome, has broad serological assessments of this parasite. Seroprevalence in Brazilian dogs ranges from 3.1 to 91% (Dubey et al. 2012), and populations with no evidence of exposure are very rare, endorsing the generalist nature and wide geographical distribution of this parasite. The 47.1% seroprevalence detected in the present study is not surprising and corroborates previous studies that showed substantial rates of 69.8 and 52.0% seropositivity in the Amazon (Valadas et al. 2010; Minervino et al. 2012). These numbers indicate high levels of environmental contamination by T. gondii and, thus, an elevated risk for human infection by this pathogen.

The wide geographical distribution of animals seropositive to CDV, CPV, and T. gondii revealed that these pathogens were present in several localities of the surveyed region, and probably had a broad circulation in the animal population. Clusters of seropositive animals were detected for all the tested pathogens, indicating areas of elevated risk of exposure in the subpopulations of the animals sampled. This probably results from multiple factors that lead to higher transmission rates inside the areas comprised by the clusters. Additionally, cluster location differed among pathogens, probably reflecting epidemiological particularities. However, CDV and CPV clusters overlapped mostly between Altamira and Vitória do Xingu, which may be due to common epidemiological features of CDV and CPV, including dogs serving as the main reservoirs of these viruses and transmission through direct contact or contact with bodily fluids (Thompson et al. 2020). The spatial distribution of L. infantum was heterogeneous, with seropositive animals concentrated in the southern region. The origin of the geographical pattern of this disease is uncertain, but several factors are known to influence the prevalence of L. infantum in a particular region, such as the dispersion of sand flies (Oliveira et al. 2016) and dog density (Chamaillé et al. 2010). The detected areas of high risk of exposure can assist preventive interventions directed towards these pathogens and guide future research.

Since CDV is transmitted mainly through direct contact between animals, the association between exposure rates and land cover types is difficult to elucidate. Most studies on CDV risk factors have explored individual characteristics of animals, such as age, sex, and vaccination status, while the influence of the environment has been poorly assessed. The effect of environmental characteristics is likely related to the complex patterns of animal movements and contact rates. Areas with pastures likely provide open spaces that facilitate animal encounters through visual contact, thereby increasing CDV transmission rates. In contrast, water bodies (like rivers and lakes) are inappropriate for interactions among dogs.

The positive association of T. gondii with pasture areas was unexpected. Toxoplasma gondii oocysts are susceptible to ultraviolet radiation (Pinto-Ferreira et al. 2021), and open spaces such as pastures allow high penetration of sunlight on the ground surface, probably decreasing oocyst survival and infection rates in terrestrial animals. Pastures are resource-poor habitats for most animals, and dogs and wild carnivores that live close to pasture areas likely need to increase their home ranges. Dogs from rural areas can roam over long distances in search of mating opportunities, to hunt, form social groups, and mark territories. This may increase the risk of T. gondii exposure in a similar way that stray dogs have a greater chance of being seropositive than housed dogs (Liu et al. 2012). The negative association of T. gondii exposure with forest formations and floodplains were not expected. These areas are characterized by denser vegetation and higher humidity levels than pastures, benefiting oocyst survival. It is possible that the region we surveyed has a naturally low prevalence of T. gondii in the wild environment, and the detected high seroprevalence resulted from peridomicile exposure where domestic cats are more abundant.

Several factors may increase the incidence of L. infantum, including human-induced changes in environmental conditions that alter the vector (Lutzomyia spp.) habitat (Sevá et al. 2017). Floodplains and forest formations were risk factors for L. infantum exposure, suggesting that these habitats are suitable for the parasite vector. Forested areas were likely inhabited by wild animals that served as competent hosts for L. infantum, thus increasing the odds of exposure in this type of environment. Regarding floodplains, high humidity levels and organic matter in the soil may increase habitat suitability for sand fly larvae, and thus increase vector abundance, density, and feeding frequency in dogs. Previous studies have reported similar results, with increased densities of sand flies following the rainy seasons (França-Silva et al. 2005; Lara-Silva et al. 2015). However, in the norther region of this study, many seronegative dogs lived close to the Xingu River (Figure 2, between the BMHD and Senador José Porfírio). The low seroprevalence in this region - despite proximity to the river - is probably associated with pasture coverage in the animal buffer area, which was negatively correlated with positive results for L. infantum.

The small sample size of wild carnivores limits the discussion at the population level, as indicated by the wide range of the confidence intervals. Nonetheless, some useful pieces of information can be drawn from these results. First, the high prevalence rates for CDV and CPV indicate a high exposure level to these viruses that should cause concern. Second, CPV seropositivity was detected in five of the six carnivore species, suggesting exposure to this virus among diverse animal taxa. Finally, some of the sampled species, like bush dogs and kinkajous, are very difficult to access, and even results from a few animals may provide valuable epidemiological information.

Although the transmission chain for CDV and CPV could not be determined in the present study, domestic dogs are likely to be the origin of exposure among the studied carnivores, as discussed elsewhere (Woodroffe et al. 2004; Fiorello et al. 2006). CPV infection occurs mostly through contact with a contaminated environment, while CDV infection occurs more frequently through direct contact between infected and susceptible hosts (Fiorello et al. 2004). Therefore, the wild carnivores surveyed probably became exposed to CPV by sharing the same territories as dogs (in peridomestic or wild areas), while exposure to CDV presumably occurred during agonistic or social interactions with dogs. Transmission risk can be higher for dogs in poor body conditions (Fung et al. 2014) that roam freely in the environment (Hughes and Macdonald, 2013), conditions that were observed in most communities surveyed during sampling.

Studies on CDV and CPV in Brazilian Amazon wildlife are almost nonexistent. Serological evidence of infection has been described in wild carnivores from southeast and central-west Brazil (Nava et al. 2008; Curi et al. 2012; Furtado et al. 2013; Furtado et al. 2016), including seropositivity rates above 90% (Curi et al. 2012). Thus, wild populations may present high levels of exposure to these viruses in different Brazilian biomes. Additional investigations are required to assess the infection status and morbimortality by these pathogens in wildlife, including molecular diagnostic tests and comparisons with health parameters.

Broad assessments of VL in Brazilian wildlife, using serological and molecular tests (Humberg et al. 2012; Paiz et al. 2015), have demonstrated the diversity of species exposed to or infected by L. infantum and their possible role as reservoirs. However, most studies performed in the Amazon region have focused on detecting Leishmania species responsible for cutaneous leishmaniases (such as L. braziliensis Vianna, 1911 and L. amazonensis Lainson & Shaw, 1972), while investigations of VL in wildlife from this biome remain limited. The few records of L. infantum infection include a southern tamandua, Tamandua tetradactyla (Linnaeus, 1758) from Pará state, Brazil (Araújo et al. 2013), and two red howler monkeys, Alouatta seniculus (Linnaeus, 1766) from French Guiana (Medkour et al. 2019). A noteworthy study conducted in Marajó Island (Pará state, Brazil), detected a high prevalence of crab-eating foxes infected by L. infantum, but a low infectiousness rate for sandflies compared to domestic dogs, indicating that these foxes were not important sources of infection (Courtenay et al. 2002). These authors also suggested that foxes became infected in the peridomestic environment, where domestic dogs serve as the main reservoirs.

Wild carnivores seropositive for L. infantum were not detected in this study, indicating low levels of exposure. However, an epidemiological bias due to the small sample size should be considered. Given the 15.4% seroprevalence detected in dogs, wildlife could possibly become exposed to L. infantum in the studied region. A larger number of specimens could provide more accurate data on VL seroprevalence in the Amazon wildlife.

The construction of hydroelectric dams has considerable negative impacts, such as deforestation of extensive areas, high mortality rates in wildlife, changes in the vegetation composition, and migration of traditional communities. These profound modifications succeeded the period of the study and probably increased the threat to wildlife and public health. Actions from diverse segments of the government and society are needed to mitigate the impacts of landscape modifications, hydroelectric dams, and the presence of domestic animals in this biodiversity hotspot.

CONCLUSIONS

This study represents one of the largest epidemiological surveys conducted on domestic dogs in the Brazilian Amazon. Exposure to CDV, CPV, T. gondii, and L. infantum was detected in dogs in the lower Xingu River basin. The high seroprevalence of CDV in dogs is concerning and highlights the risk of transmission to local wildlife. A wide spatial distribution of seropositive animals was observed for CDV, CPV, and T. gondii, whilst animals seropositive to L. infantum were concentrated near the Xingu River. Exposure to CDV and T. gondii was more frequent in areas of pasture, while exposure to L. infantum was positively associated with floodplains and forest formations. Clusters of seropositive animals were observed for all investigated pathogens, indicating specific areas with higher risk of exposure.

ACKNOWLEDGMENTS

We are thankful to Norte Energia S.A. and Biota Projetos e Consultoria Ambiental Ltda. for logistical support during field activities, and to all biologists who contributed in some way to this study.

REFERENCES

• Araújo, V.A.L.; Boité, M.C.; Cupolillo, E.; Jansen, A.M.; Roque, A.L.R. 2013. Mixed infection in the anteater Tamandua tetradactyla (Mammalia: Pilosa) from Pará State, Brazil: Trypanosoma cruzi, T. rangeli and Leishmania infantum Parasitology, 140: 455-460.
• Blasio, A.; Irico, L.; Caruso, C.; Miceli, I.; Robetto, S.; Peletto, S.; et al 2019. Canine distemper virus as an emerging multihost pathogen in wild carnivores in northwest Italy. Journal of Wildlife Diseases, 55: 844-856.
• Brandão, E.M.V.; Xavier, S.C.C.; Rocha, F.L.; Lima, C.F.M.; Candeias, I.Z.; Lemos, F.G.; Azevedo, F.C.; Jansen, A.M.; Roque, A.L.R. 2020. Wild and domestic canids and their interactions in the transmission cycles of Trypanosoma cruzi and Leishmania spp. in an area of the Brazilian Cerrado. Pathogens, 9: 818. doi:10.3390/pathogens9100818.
  » https://doi.org/10.3390/pathogens9100818
• Bucafusco, D.; Argibay, H.; Diaz, L.; Vega, C.; Minatel, L.; Postma, G.C.; Rinas, M.; Bratanich, A. 2019. First characterization of a canine parvovirus causing fatal disease in coatis (Nasua nasua). Archives of Virology, 164: 3073-3079.
• Canning, G.; Camphor, H.; Schroder, B. 2019. Rabies outbreak in African Wild Dogs (Lycaon pictus) in the Tuli region, Botswana: Interventions and management mitigation recommendations. Journal for Nature Conservation, 48: 71-76.
• Chamaillé, L.; Tran, A.; Meunier, A.; Bourdoiseau, G.; Ready, P.; Dedet, J. 2010. Environmental risk mapping of canine leishmaniasis in France. Parasites & Vectors, 3: 1-8.
• Clifford, D.L.; Mazet, J.A.K.; Dubovi, E.J.; Garcelon, D.K.; Coonan, T.J.; Conrad, P.A.; Munson, L. 2006. Pathogen exposure in endangered island fox (Urocyon littoralis) populations: Implications for conservation management. Biological Conservation, 131: 230-243.
• Courtenay, O.; Quinnell, R.J.; Chalmers, W.S.K. 2001. Contact rates between wild and domestic canids: no evidence of parvovirus or caninedistemper virus in crab-eating foxes. Veterinary Microbiology, 81: 9-19.
• Courtenay, O.; Quinnell, R.J.; Garcez, L.M.; Dye, C. 2002. Low infectiousness of a wildlife host of Leishmania infantum: the crab-eating fox is not important for transmission. Parasitology, 125: 407-414.
• Curi, N.H.A.; Araújo, A.S.; Campos, F.S.; Lobato, Z.I.P.; Gennari, S.M.; Marvulo, M.F.V.; Silva, J.C.R.; Talamoni, S.A. 2010. Wild canids, domestic dogs and their pathogens in Southeast Brazil: Disease threats for canid conservation. Biodiversity and Conservation, 19: 3513-3524.
• Curi, N.H.A.; Coelho, C.M.; Malta, M.C.C.; Magni, E.M.V.; Sábato, M.A.L.; Araújo, A.S.; et al 2012. Pathogens of wild maned wolves (Chrysocyon brachyurus) in Brazil. Journal of Wildlife Diseases, 48: 1052-1056.
• Curi, N.H.A.; Massara, R.L.; Paschoal, A.M.O.; Soriano-Araújo, A.; Lobato, Z.I.P.; Demétrio, G.R.; Chiarello, A.G.; Passamani, M. 2016. Prevalence and risk factors for viral exposure in rural dogs around protected areas of the Atlantic Forest. BMC Veterinary Research, 12: 1-10.
• Dubey, J.P.; Lago, E.G.; Gennari, S.M.; Su, C.; Jones, J.L. 2012. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology, 139: 1375-1424.
• Fiorello, C.V.; Deem, S.L.; Gompper, M.E.; Dubovi, E.J. 2004. Seroprevalence of pathogens in domestic carnivores on the border of Madidi National Park, Bolivia. Animal Conservation, 7: 45-54.
• Fiorello, C.V.; Noss, A.J.; Deem, S.L. 2006. Demography, hunting ecology, and pathogen exposure of domestic dogs in the Isoso of Bolivia. Conservation Biology, 20: 762-771.
• França-Silva, J.C.; Barata, R.A.; Costa, R.T.; Monteiro, É.M.; Machado-Coelho, G.L.L.; Vieira, E.P.; et al 2005. Importance of Lutzomyia longipalpis in the dynamics of transmission of canine visceral leishmaniasis in the endemic area of Porteirinha Municipality, Minas Gerais, Brazil. Veterinary Parasitology, 131: 213-220.
• Fung, H.L.; Calzada, J.; Saldaña, A.; Santamaria, A.M.; Pineda, V.; Gonzalez, K.; Chaves, L.F.; Garner, B.; Gottdenker, N. 2014. Domestic dog health worsens with socio-economic deprivation of their home communities. Acta Tropica, 135: 67-74.
• Furtado, M.M.; Filho, J.D.R.; Scheffer, K.C.; Coelho, C.J.; Cruz, P.S.; Ikuta, C.Y.; et al 2013. Serosurvey for selected viral infections in free-ranging jaguars (Panthera onca) and domestic carnivores in Brazilian Cerrado, Pantanal, and Amazon. Journal of Wildlife Diseases, 49: 510-521.
• Furtado, M.M.; Hayashi, E.M.K.; Allendorf, S.D.; Coelho, C.J.; Jácomo, A.T.A.; Megid, J.; Filho, J.D.R; Silveira, L.; Tôrres, N.M.; Ferreira Neto, J.S. 2016. Exposure of free-ranging wild carnivores and domestic dogs to canine distemper virus and parvovirus in the Cerrado of Central Brazil. EcoHealth, 13: 549-557.
• Hughes, J.; Macdonald, D.W. 2013. A review of the interactions between free-roaming domestic dogs and wildlife. Biological Conservation, 157: 341-351.
• Humberg, R.M.P.; Oshiro, E.T.; Cruz, M.D.S.P.; Ribolla, P.E.M.; Alonso, D.P.; Ferreira, A.M.T.; Bonamigo, R.A.; Tasso, N.; Oliveira, A.G. 2012. Short report: Leishmania chagasi in opossums (Didelphis albiventris) in an urban area endemic for visceral leishmaniasis, Campo Grande, Mato Grosso do Sul, Brazil. American Journal of Tropical Medicine and Hygiene, 87: 470-472.
• Jesus, A.V.; Sevá, A.P.; Guedes, P.E.B.; Santos, K.C.; Harvey, T.V.; Oliveira, G.M.S.; Bitar, T.V.; Ferreira, F.; Albuquerque, G.R.; Carlos, R.S.A. 2023. Spatial distribution of off-host stages of Tunga penetrans in the soil within the home range of nine infected dogs in an endemic tourist area in Brazil. Tropical Medicine and Infectious Disease, 98: 1-13.
• Knobel, D.L.; Butler, J.R.A.; Lembo, T.; Critchlow, R.; Gompper, M.E. 2014. Dogs, disease, and wildlife. In: Gompper, M.E. (Ed.). Free-ranging dogs and wildlife conservation. Oxford University Press, New York, p.144-169.
• Kulldorff, M. 1997. A spatial scan statistic. Communications in Statistics - Theory and Methods, 26: 1481-1496.
• Kulldorff, M.; Nagarwalla, N. 1995. Spatial disease clusters: Detection and inference. Statistics in Medicine, 14: 799-810.
• Lara-Silva, F.O.; Michalsky, É.M.; Fortes-Dias, C.L.; Fiuza, V.O.P.; Pessanha, J.E.M.; Regina-Silva, S.; et al 2015. Epidemiological aspects of vector, parasite, and domestic reservoir in areas of recent transmission and no reported human cases of visceral leishmaniasis in Brazil. Acta Tropica, 148: 128-136.
• Liu, Y.; He, G.; Cheng, Z.; Qi, Y.; Liu, J.; Zhang, H.; Liu, G.; Shi, D.; Yang, D.; Wang, S.; Wang, Z. 2012. Seroprevalence of Toxoplasma gondii in dogs in Shandong, Henan, and Heilongjiang provinces, and in the Xinjiang Uygur Autonomous Region, People’s Republic of China. The Journal of Parasitology, 98: 211-212.
• MAPBIOMAS, 2022. ( (http://www.plataforma.brasil.mapbiomas.org ). Accessed on 16 Apr 2022.
  » http://www.plataforma.brasil.mapbiomas.org
• Mech, L.D.; Goyal, S.M.; Paul, W.J.; Newton, W.E. 2008. Demographic effects of canine parvovirus on a free-ranging wolf population over 30 Years. Journal of Wildlife Diseases, 44: 824-839.
• Medkour, H.; Davoust, B.; Levasseur, A.; Mediannikov, O. 2019. Molecular evidence of Leishmania infantum and Leishmania guyanensis in red howler monkey (Alouatta seniculus) from French Guiana. Vector-Borne and Zoonotic Diseases, 19: 896-900.
• Megid, J.; Teixeira, C.R.; Amorin, R.L.; Cortez, A.; Heinemann, M.B.; Antunes, J.M.A.P.; et al 2010. First identification of canine distemper virus in hoary fox (Lycalopex vetulus): Pathologic aspects and virus phylogeny. Journal of Wildlife Diseases, 46: 303-305.
• Megid, J.; Teixeira, C.R.; Cortez, A.; Heinemman, M.B.; Antunes, J.M.A.P.; Fornazari, F.; Rassy, F.B.; Richtzenhain, L.J. 2013. Canine distemper virus infection in a lesser grison (Galictis cuja): First report and virus phylogeny. Pesquisa Veterinária Brasileira, 33: 247-250.
• Michelazzo, M.M.Z.; Oliveira, T.E.S.; Viana, N.E.; Moraes, W.; Cubas, Z.S.; Headley, S.A. 2020. Immunohistochemical evidence of canine morbillivirus (canine distemper) infection in coatis (Nasua nasua) from Southern Brazil. Transboundary and Emerging Diseases, 67: 178-184.
• Minervino, A.H.H.; Cassinelli, A.B.M.; Lima, J.T.R.; Soares, H.S.; Malheiros, A.F.; Marcili, A.; Gennari, S.M. 2012. Prevalence of anti-Neospora caninum and anti-Toxoplasma gondii antibodies in dogs from two different indigenous communities in the Brazilian amazon region. Journal of Parasitology, 98: 1276-1278.
• Mourya, D.T.; Yadav, P.D.; Mohandas, S.; Kadiwar, R.R.; Vala, M.K.; Saxena, A.K.; et al 2019. Canine distemper virus in Asiatic lions of Gujarat State, India. Emerging Infectious Diseases, 25: 2128-2130.
• Nava, A.F.D.; Cullen, L.; Sana, D.A.; Nardi, M.S.; Filho, J.D.R.; Lima, T.F.; Abreu, K.C.; Ferreira, F. 2008. First evidence of canine distemper in Brazilian free-ranging felids. EcoHealth, 5: 513-518.
• Olbera, A.V.G.; Fornazari, F.; Babboni, S.D.; Rossi, R.S.; Sevá, A.P.; Latosinski, G.S.; Silva, M.A.R.X.; Modolo, J.R.; Langoni, H. 2020. Cumulative incidence and spatial distribution of dogs exposed to Toxoplasma gondii Revista Brasileira de Parasitologia Veterinária, 29: 1-8.
• Oliveira, A.M.; Vieira, C.P.; Dibo, M.R.; Guirado, M.M.; Rodas, L.A.C.; Chiaravalloti-Neto, F. 2016. Dispersal of Lutzomyia longipalpis and expansion of canine and human visceral leishmaniasis in São Paulo State, Brazil. Acta Tropica, 164: 233-242.
• Paiz, L.M.; Fornazari, F.; Menozzi, B.D.; Oliveira, G.C.; Coiro, C.J.; Teixeira, C.R.; Silva, V.M.C.; Donalisio, M.R.; Langoni, H. 2015. Serological evidence of infection by Leishmania (Leishmania) infantum (Synonym: Leishmania (Leishmania) chagasi) in free-ranging wild mammals in a nonendemic region of the State of São Paulo, Brazil. Vector-Borne and Zoonotic Diseases, 15: 667-673.
• Pfeifer, D.; Robinson, T.; Stevenson, M.; Stevens, K.; Rogers, D.; Clemens, A. 2008. Spatial Analysis in Epidemiology 1^st ed. Oxford University Press, Oxford, 142p.
• Pinto-Ferreira, F.; Paschoal, A.T.P.; Pasquali, A.K.S.; Bernardes, J.C.; Caldart, E.T., Freire, R.L.; Mitsuka-Breganó, R.; Navarro, I.T. 2021. Techniques for inactivating Toxoplasma gondii oocysts: a systematic review. Brazilian Journal of Veterinary Parasitology, 30: e026420.
• Prager, K.C.; Mazet, J.A.K.; Munson, L.; Cleaveland, S.; Donnelly, C.A.; Dubovi, E.J.; et al 2012. The effect of protected areas on pathogen exposure in endangered African wild dog (Lycaon pictus) populations. Biological Conservation, 150: 15-22.
• Preece, N.D.; Abell, S.E.; Grogan, L.; Wayne, A.; Skerratt, L.F.; van Oosterzee, P.; et al 2017. A guide for ecologists: Detecting the role of disease in faunal declines and managing population recovery. Biological Conservation, 214: 136-146.
• Sevá, A.P.; Mao, L.; Galvis-Ovallos, F.; Lima, J.M.T.; Valle, D. 2017. Risk analysis and prediction of visceral leishmaniasis dispersion in São Paulo State, Brazil. PLOS Neglected Tropical Diseases, 11: e0005353.
• Silveira, F.T.; Carneiro, L.A.; Ramos, P.K.S.; Chagas, E.J.; Lima, L.V.R.; Campos, M.B.; Laurenti, M.D.; Gomes, C.M.C.; Corbett, C.E.P. 2012. A cross-sectional study on canine Leishmania (L.) infantum chagasi infection in Amazonian Brazil ratifies a higher prevalence of specific IgG-antibody response than delayed-type hypersensitivity in symptomatic and asymptomatic dogs. Parasitology Research, 111: 1513-1522.
• SINAN. 2021. Sistema de Informação de Agravos de Notificação. ( (http://www.portalsinan.saude.gov.br/dados-epidemiologicos-sinan ). Accessed on 15 Jun 2021.
  » http://www.portalsinan.saude.gov.br/dados-epidemiologicos-sinan
• Spera, C.G.; Lavorente, F.L.P.; Lorenzetti, E.; Marques, G.C; Freitas, L.A.; Martins, M.B.; Teixeira, C.R.; Alfieri, A.A.; Alfieri, A.F. 2021. First detection of canine parvovirus 2b DNA in a crab-eating fox pup (Cerdocyon thous, Linnaeus, 1766). Brazilian Journal of Microbiology, 52: 449-453.
• Spera, C.G.; Lorenzetti, E.; Lavorente, F.L.P.; Marques, G.C.; Bisca, J.M.; Teixeira, C.R.; Alfieri, A.A.; Alfieri, AF. 2020. Canine parvovirus 2b in fecal samples of asymptomatic free-living South American coatis (Nasua nasua, Linnaeus, 1766). Brazilian Journal of Microbiology, 51: 1399-1403.
• Thompson, R.; Adams, H.; Odoi, A.; Kennedy, M. 2020. Seroprevalence of viral and vector-borne bacterial pathogens in domestic dogs (Canis familiaris) in northern Botswana. PLoS ONE, 15: e0220593.
• Valadas, S.; Minervino, A.H.H.; Lima, V.M.F.; Soares, R.M.; Ortolani, E.L.; Gennari, S.M. 2010. Occurrence of antibodies anti-Neospora caninum, anti-Toxoplasma gondii, and anti-Leishmania chagasi in serum of dogs from Pará State, Amazon, Brazil. Parasitology Research, 107: 453-457.
• Viana, N.E.; Michelazzo, M.M.Z.; Oliveira, T.E.S.; Cubas, Z.S.; Moraes, W.; Headley, S.A. 2020. Immunohistochemical identification of antigens of canine distemper virus in neotropical felids from Southern Brazil. Transboundary and Emerging Diseases, 67: 149-153.
• Wheeler, D.C. 2007. A comparison of spatial clustering and cluster detection techniques for childhood leukemia incidence in Ohio, 1996-2003. International Journal of Health Geographics, 6: 13. doi:10.1186/1476-072X-6-13.
  » https://doi.org/10.1186/1476-072X-6-13
• Whiteman, C.W.; Matushima, E.R.; Confalonieri, U.E.C.; Palha, M.D.C.; Silva, A.S. L.; Monteiro, V.C. 2007. Human and domestic animal populations as a potential threat to wild carnivore conservation in a fragmented landscape from the Eastern Brazilian Amazon. Biological Conservation, 138: 290-296.
• Woodroffe, R.; Cleaveland, S.; Courtenay, O.; Laurenson, M.K.; Artois, M. 2004. Infectious Diseases. In: Macdonald, D.W.; Sillero-Zubiri, C.(Eds.) Biology and conservation of wild canids Oxford University Press, Oxford . p.123-142.
• Woodroffe, R.; Prager, K.C.; Munson, L.; Conrad, P.A.; Dubovi, E.J.; Mazet, J.A.K. 2012. Contact with domestic dogs increases pathogen exposure in endangered African wild dogs (Lycaon pictus). PLoS ONE, 7: e30099.

• CITE AS:

  Fornazari, F. et al. 2023. Exposure of dogs and wild carnivores to canine distemper virus, canine parvovirus, Leishmania infantum, and Toxoplasma gondii in the Xingu River basin, Brazilian Amazon: Prevalence, spatial distribution, and association with land cover types. Acta Amazonica 53: 325-335.

Data availability

The data that support the findings of this study are available, upon reasonable request, from the corresponding author (Felipe Fornazari).

Edited by

ASSOCIATE EDITOR:

Paulo E. Bobrowiec

Publication Dates

• Publication in this collection
  13 Nov 2023
• Date of issue
  Oct-Dec 2023

History

• Received
  07 May 2023
• Accepted
  27 July 2023