Parasitological diagnosis of fecal samples from domestic dogs from the municipality of Niterói, Rio de Janeiro, Brazil

[Diagnóstico parasitológico de amostras fecais de cães domésticos provenientes do município de Niterói, Rio de Janeiro, Brasil]

ABSTRACT

From 2015 to 2021 the prevalence of parasites was evaluated in fecal samples of dogs from the municipality of Niterói, RJ. The samples were examined at the Laboratory of Diagnostic Support in Parasitic Diseases (LADDP) of the Veterinary School at the Federal Fluminense University (UFF), using centrifugal flotation, sedimentation and mini-FLOTAC techniques. Of the 1,037 samples examined, 30.6% (318/1,037) showed positive results for some parasitic infections, of which 80.5% (256/318) were positive for only one species of parasite and 19.5% (62/318) for multiple infections. Parasitism by Ancylostoma caninum was the most prevalent, with 39% (124/318), followed by Giardia sp., 16% (51/318); Toxocara canis, 14.5% (46/318); Trichuris vulpis, 8.5% (27/318); Cystoisospora canis, 8.5% (27/318); Dipylidium caninum, 7.9% (25/318); and Cryptosporidium sp., 5.6% (18/318). The parasitological diagnosis of dogs in urban areas is the best choice to evaluate the efficacy of control measures adopted for parasitic infections, including those with zoonotic importance.

Keywords:
dog; feces; parasitosis; zoonosis

RESUMO

Durante o período de 2015 a 2021, foi avaliada a prevalência de endoparasitos em amostras fecais de cães provenientes do município de Niterói, RJ. As amostras foram analisadas no Laboratório de Apoio Diagnóstico em Doenças Parasitárias (LADDP) da Faculdade de Veterinária da Universidade Federal Fluminense (UFF), sendo usadas as técnicas de centrifugo-flutuação, sedimentação simples e mini-FLOTAC. Das 1.037 amostras analisadas, 30,6% (318/1.037) apresentaram resultados positivos para alguma infecção parasitária, sendo dessas 80,5% (256/318) positivas para apenas uma espécie de parasito e 19,5% (62/318) para infecções múltiplas. O parasitismo por Ancylostoma caninum foi o mais prevalente, com 39% (124/318), seguido por Giardia sp., 16% (51/318), Toxocara canis, 14,5% (46/318), Trichuris vulpis, 8,5% (27/318), Cystoisospora canis, 8,5% (27/318), Dipylidium caninum, 7,9% (25/318) e Cryptosporidium sp., 5,6% (18/318). O diagnóstico parasitológico de cães em áreas urbanas é a melhor alternativa para a avaliação da eficácia dos programas de controle de infecções parasitárias, incluindo aquelas com importância zoonótica.

Palavras-chave:
cão; fezes; parasitose; zoonose

INTRODUCTION

Infections caused by helminths and protozoa may result in relevant diseases in domestic animals that often might infect humans. Knowledge about parasitosis and the updated data survey on their epidemiology are essential for the adoption of proper preventive and curative measures.

The municipality of Niterói occupies a territorial area of 133,757km², with 515,317 inhabitants and a canine population estimated at 10% of the human population (IBGE, 2020). Because of technological advances and mainly to the improvement in preventive disease management, the lifespan of dogs has increased significantly. However, many preventive care measures, like treatment and prophylaxis of parasitic diseases, are not adequately performed. Consequently, parasitic infections may present worrying prevalence rates, including those with zoonotic importance (Serra et al., 2003; Brener et al., 2005; Katagiri and Oliveira-Sequeira, 2008; Barros et al. 2013; Ramos et al. 2015).

Non-invasive techniques can detect many species of gastrointestinal parasites that have the domestic dog as a host through the collection of fecal material and processing coproparasitological diagnosis (Matosinhos, 2012). The objective was to perform the diagnosis and determine the prevalence of gastrointestinal parasites in fecal samples obtained from domestic dogs treated in Niterói, RJ, during the period from 2016 to 2021.

MATERIAL AND METHODS

This is a retrospective study, carried out through consultations to the LADD files of the Veterinary School of the Federal Fluminense University (UFF), using data concerning the period from October 2015 to December 2021 (certificate number on ethics committee: 4535081021). The samples were processed by the techniques of centrifugal flotation, simple sedimentation and mini-FLOTAC (Sloss et al. 1999; Barda et al. 2013). Besides, the study also analyzed the results of the coproparasitological tests, age profile and sex.

The results are expressed in prevalence ratio, using the terminology according to Busch et al. (1997). To compare species prevalence, mono- or polyinfections, sex and age profile, the Qui-square test was performed with a significance level of 95%. Data analyses were carried out with the Program BioEstat 5.3 (Ayres et al., 2007).

RESULTS

During the period from 2016 to 2021, 1,037 fecal samples of dogs from the municipality of Niterói were examined. Table 1 shows the prevalence data by species, emphasizing the highest prevalence of Ancylostoma caninum, followed by Giardia sp. and Toxocara canis. There is a significant difference between the prevalence rates of some species, especially A. caninum, which differed statistically from all others.

Table 1
Prevalence of parasites in fecal samples from dogs from the municipality of Niterói, RJ, during the period from 2016 to 2021

Species	No. of positive samples	Prevalence
Ancylostoma caninum	124ª	39.0%
Giardia sp.	51b	16.0%
Toxocara canis	46b	14.5%
Trichuris vulpis	27c	8.5%
Cystoisospora canis	27c	8.5%
Dipylidium caninum	25c	7.9%
Cryptosporidium sp.	18c	5.7%
Total	318	100.0%

• Note: Different letters in the rows indicate statistical difference (p<0.05).

Among positive animals, 54.1% (172/318) were female and 45.9% (146/318) were male, with no statistical difference (p=0.5110) between them. The number of youngsters corresponded to 24.8% (79/318) and adults to 75.2% (239/318), with a statistical difference between them (p=0.0023).

The prevalence of positive fecal samples was 30.6% (318/1,037), of which 80.5% (256/318) was for one species of parasite and 19.5% (62/318) for multiple parasites. Figs. 1 and 2 show the associations by age groups and sex regarding mono- and poly infections. There was a statistical difference between youngsters (p=0.01474) and adults (p<0.00001), as well as between males and females (p<0.00001 in both).

Figure 1
Prevalence of positive dogs for parasitic mono- and polyinfections, by age profile, in coproparasitological tests performed at the Laboratory of Diagnostic Support in Parasitic Diseases at UFF, during the period from 2016 to 2021.

Figure 2
Prevalence of dogs positive for parasitic mono- and polyinfections, by sex, in coproparasitological tests performed at the Laboratory for Diagnostic Support in Parasitic Diseases at UFF during the period from 2016 to 2021.

DISCUSSION

Gastrointestinal parasites are common in dogs and can occur at high prevalence rates in several regions of Brazil and other countries (Funada et al., 2007; Torrico et al., 2008; Gennari et al., 2016; Tamponi et al., 2020; Sobotyk et al., 2021).

According to Katagiri and Oliveira-Siqueira (2007) the last decades have been marked by intense technological progress and important social changes, with repercussions in both human and animal health. Unfortunately, zoonosis caused by intestinal parasites of dogs has not ceased to be a permanent public health problem in developing countries and is also a growing concern in developed countries.

In Niterói, RJ, Brener et al. (2005) and Barros et al. (2013) carried out studies on the prevalence of parasites in dogs and reported a prevalence of 33% (70/212) and 18.3% (44/240), respectively. In the present study, we found a prevalence of 30.6% (318/1,037), using an analysis period and a sample size larger than the previous authors. The prevalence found reveals that the rate of parasitism in dogs in the municipality of Niterói has not changed significantly in the last two decades, which is worrisome for the One Health approach.

According to Dantas-Torres and Otranto (2014), Ancylostoma caninum is the most prevalent nematode in coproparasitological surveys of dogs in urban areas, and the data described here in agreement with the findings of those authors. Furthermore, according to Silva et al. (2021), Ancylostoma caninum is a parasite that determines significant clinical changes in dogs, causing dermatitis, hemorrhagic enteritis, anemia, pneumonia, and death. The third-stage larvae present in the soil can penetrate human skin, leading to cases of cutaneous larva migrants, also known as creeping eruption, which is an important zoonosis with an intense local inflammatory reaction.

The adult form of A. caninum lives in the small intestine of the host organism. Notwithstanding a predisposition for the infection of young dogs, Funada et al. (2007) and Ferreira et al. (2016) found a high prevalence of infected adult animals. Similarly, the results presented here show a higher prevalence of infected adults. This is relevant because most dogs that walk the streets and public squares in the municipality of Niterói are adult animals, and sometimes their owners often do not pick up their feces.

The lack of correct parasite control in companion animals and the absence or low effectiveness of population control programs for stray animals are significant factors in the maintenance and transmission of parasites and parasitic diseases in urban environments, including some of zoonotic importance. Serra et al. (2003), in a study carried out in the metropolitan region of Rio de Janeiro, found a prevalence of parasitism by Ancylostoma sp. of 43.5% among domestic and stray cats, bearing out the importance of this parasitosis in the study region.

Giardia sp. infection was the second most prevalent; however, it was not possible to distinguish the species, although G. duodenalis, also known as G. intestinalis or G. lamblia, is described with higher prevalence in coproparasitological tests in dogs (Lallo and Bondan, 2006). This parasite is restricted to the gastrointestinal tract and usually causes an asymptomatic infection, which helps to disseminate cysts in the environment and might contaminate humans and other animals. In humans, it compromises weight gain and is responsible for several extraintestinal and post-infectious complications, including post-infectious irritable bowel syndrome, chronic fatigue, growth deficiency, and cognitive impairment (Buret et al., 2015).

Dipylidium caninum infection is clinically characterized by digestive problems, such as diarrhea in dogs and, in some cases, problems for public health, mainly enteritis in children. It is more prevalent in abandoned animals due to the higher chance of ectoparasitim infestation, although it may also affect domiciled dogs (Quiroz, 1994; Urquhart, 2001).

Infections in young animals can result in nonspecific symptoms such as weight loss and digestive disorders. The increase in the number of adult specimens in the intestine may promote mucosal thickening and increased secretion with leukocyte infiltrate (Sánchez et al., 1999).

In relation to hosts, transmission is determined by several factors, such as eating habits, the life form of animals and certain human behaviors that allow dogs access to intermediate hosts (Sánchez et al., 1999).

There is great concern in Brazil about the occurrence of waterborne parasites, particularly Cryptosporidium and Giardia, found here with prevalence of 5.7% and 16%, respectively. This concern is expressed in Ordinance 518 of 2004 of the Ministry of Health, in the chapter on water quality standards, which recommends the absence of pathogens like enterovirus, Cryptosporidium and Giardia. The presence of these parasites in dogs suggests risk to the human population, and this fact should be considered in parasite control programs for dogs and humans in the municipality of Niterói.

Toxocariasis was the third most prevalent parasitosis in the dogs examined. It is caused by the nematode Toxocara spp., which can establish an erratic cycle, with migration of larvae through various tissues. This parasitosis in human hosts is known as Visceral Larva Migrans and represents a threat to the health of children and young companion animals, and therefore should be avoided and controlled. Contamination occurs after the ingestion of parasite eggs containing second-stage larvae that might be present in public areas frequented by infected dogs (Mirdha et al., 1998; Gilioli and Silva, 2000; Acha and Szyfres, 2003; Brandão et al., 2009).

CONCLUSIONS

This study shows that Ancylostoma sp., Giardia sp., and Toxocara sp. were the most prevalent parasites in examined fecal samples from dogs from the municipality of Niterói. As these parasites entail a potential risk of zoonotic transmission, these results are epidemiologically relevant and contribute to updating data on endoparasitic infections in dogs in the study region. Therefore, the study reinforces the importance of regular parasitological testing for the accurate diagnosis and treatment of parasitosis in companion animals. Such measures can reduce the persistence and spread of parasitic diseases in dogs and humans.

REFERENCES

• ACHA, P.N.; SZYFRES, B. Zoonosis y enfermedades transmisibles comunes al hombre y a los animales. 3.ed. Washington, D.C.: Organización Panamericana de la Salud, 2003. 423p.
• AYRES, M.; AYRES Jr, M.; AYRES, D. L. et al. Bioestat 5.0 aplicações estatísticas nas áreas das ciências biológicas e médicas. Belém: IDSM, 2007.364p.
• BARDA, B.D.; RINALDI, L.; IANNIELLO, D. et al. Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field, PLoS Negl. Trop. Dis., v.7, e2344, 2013.
• BARROS, L.A.; SERRA, C.M.B.; MATTOS, D.G. et al. Estudo parasitológico de amostras fecais encontradas em calçadas no município de Niterói, RJ. Rev. Bras. Ciênc. Vet., v.20, p.20-22, 2013.
• BRANDÃO, M.L.; CHAME, M.; CORDEIRO, J.L.P. et al. Diversidade de helmintos intestinais em mamíferos silvestres e domésticos na Caatinga do Parque Nacional Serra da Capivara, Sudeste do Piauí, Brasil. Rev. Bras. Parasitol. Vet., v.18, suppl.1, p.19-28, 2009.
• BRENER, B.; MATTOS, D.P.B.G.; LISBOA, L. et al. Frequência de enteroparasitas em amostras fecais de cães e gatos dos municípios de Rio de Janeiro e Niterói. Rev. Bras. Ciênc. Vet., v.12, p.102-105, 2005.
• BURET, A.G.; AMAT, C.B.; MANKO, A. et al. Giardia duodenalis: new research developments in pathophysiology, pathogenesis, and virulence factors. Curr. Trop. Med. Rep., v.2, p.110-118, 2015.
• BUSH, A.O.; LAFFEREY, K. D.; LOTZ, J. M. et al. Parasitology meets ecology on its own terms: Margolis et al. Revisited. J. Parasitol., v.83, p. 575-583, 1997.
• DANTAS-TORRES, F.; OTRANTO, D. Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit. Vectors, v.7, p.1-25, 2014.
• FERREIRA, J.I.G.S.; PENA, H.F.J.; LABRUNA, M.B. et al. Occurrences of gastrointestinal parasites in fecal samples from domestic dogs in São Paulo, SP, Brazil. Rev. Bras. Parasitol., Vet., v.25, p.435-440, 2016.
• FUNADA, M.R.; PENA, H.F.J.; SOARES, R.M. et al. Frequência de parasitos gastrintestinais em cães e gatos atendidos em hospital-escola veterinário da cidade de São Paulo. Arq. Bras. Med. Vet. Zootec., v.59, p.1338-1340, 2007.
• GENNARI, S.M.; FERREIRA, J.I.G.S.; PENA, H.F.J. et al. Frequency of gastrointestinal parasites in cats seen at the University of São Paulo veterinary hospital, Brazil. Rev. Bras. Parasitol. Vet., v. 25, p. 423-428, 2016.
• GILIOLI, R.; SILVA, F.A. Frequência de parasitas e infecção por Salmonella em lobos guará, Chrysocyon brachyurus, mantidos em zoológicos no Estado de São Paulo. Arq. Bras. Med. Vet. Zootec., v.52, p.337-41, 2000.
• IBGE. Cidades e estados. Rio de Janeiro 2020. Available in: https://www.ibge.gov.br/cidades-e-estados/rj/niteroi.html Accessed in: 27 Jan. 2022.
  » https://www.ibge.gov.br/cidades-e-estados/rj/niteroi.html
• KATAGIRI, S.; OLIVEIRA-SEQUEIRA, T.C. Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in São Paulo State, Brazil. Zoonoses Public Health, v.55, p.406-413, 2008.
• KATAGIRI, S.; OLIVEIRA-SEQUEIRA, T.C. Zoonoses causadas por parasitas intestinais de cães e o problema do diagnóstico. Arq. Inst. Biol., v.74, p.175-184, 2007.
• LALLO, M.A.; BONDAN, E.F. Prevalência de Cryptosporidium sp. em cães de instituições da cidade de São Paulo. Rev. Saúde Pública, v.40, p.120-125, 2006.
• MATOSINHOS, F.C.L. Padronização de metodologia para detecção de ovos de helmintos em alface. 2012. 98f. Dissertação (Mestrado em Parasitologia) - Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG.
• MIRDHA, B.R.; SINGH, Y.G.; SAMANTRA, Y.J.C. et al. Trichuris vulpis infection in slum children. Indian J. Gastroenterol., v.17, p.154, 1998.
• QUIROZ, H.R. Cestodosis de perros y gatos. Parasitología y enfermedades parasitarias de los animales domésticos. 5.ed. México: Uteha Noriega editores, 1994. p.303-320.
• RAMOS, D.G.S.; ZOCCO, B.K.A.; TORRES, M.M. et al. Helmintofauna de cães errantes (Canis lupus familiaris) de Cuiabá, Centro-Oeste do Brasil. Semin. Ciênc. Agrár., v.36, p.889-894, 2015.
• SÁNCHEZ, A.C.; QUÍLEZ, J.; DEL CACHO, E. Cestodosis: teniosis, equinococosis, dipilidiosis, mesocestoidosis y difilobotriosis. In: CORDERO CAMPILLO, M.; ROJO, F.A.V.; MARTÍNEZ, A.R.F. Parasitología veterinaria. Madrid: Mc Graw Hill, 1999. p.626-635.
• SERRA, C.M.B.; UCHÔA, C.M.A.; COIMBRA, R.A. Exame parasitológico de fezes de gatos (Felis catus domesticus) domiciliados e errantes da Região Metropolitana do Rio de Janeiro, Brasil. Rev. Soc. Bras. Med. Trop., v.36, p.331-334, 2003.
• SILVA, R.C.; OLIVEIRA, P.A.; FARIAS, L.A. Particularidades do Ancylostoma caninum: revisão. Pubvet, v.15, p.143, 2021.
• SLOSS, M.W.; ZAJAC, A.M.; KEMP, R.L. Parasitologia clínica veterinária. 6.ed. São Paulo: Manole, 1999. 198p.
• SOBOTYK, C.; UPTON, K.E.; LEJEUNE, M. et al. Retrospective study of canine endoparasites diagnosed by fecal flotation methods analyzed across veterinary parasitology diagnostic laboratories, United States, 2018. Parasit. Vectors, v.14, p.439, 2021.
• TAMPONI, C.; KNOLL, S.; TOSCIRI, G. et al. Environmental contamination by dog feces in Touristic Areas of Italy: parasitological aspects and zoonotic hazards. Am. J. Trop. Med. Hyg., v.103, p.1143-1149, 2020.
• TORRICO, K.J.; SANTOS, K.R.; MARTINS, T. et al. Ocorrência de parasitas gastrintestinais em cães e gatos na rotina do laboratório de enfermidades parasitárias da FMVZ/UNESP - Botucatu, SP. Rev. Bras. Parasitol. Vet., v.17, p. 182-183, 2008.
• URQUHART, G.M.; ARMOUR, J.; DUCAN, J.L. et al. Parasitología veterinaria. 2.ed. Zaragoza, España: Acribia, 2001. p.150-153.

Publication Dates

• Publication in this collection
  10 Feb 2023
• Date of issue
  Jan-Feb 2023

History

• Received
  23 Mar 2022
• Accepted
  11 Nov 2022