Gastrointestinal parasites of cats in Brazil: frequency and zoonotic risk

Parasitas gastrointestinais em gatos no Brasil: frequência e risco zoonótico

Maria Fernanda Melo Monteiro Rafael Antonio Nascimento Ramos Andréa Maria Campos Calado Victor Fernando Santana Lima Ingrid Carla do Nascimento Ramos Rodrigo Ferreira Lima Tenório Maria Aparecida da Glória Faustino Leucio Câmara Alves About the authors

Abstract

Gastrointestinal helminths are considered to be the most common parasites affecting cats worldwide. Correct diagnosis of these parasites in animals living in urban areas is pivotal, especially considering the zoonotic potential of some species (e.g. Ancylostoma sp. and Toxocara sp.). In this study, a copromicroscopic survey was conducted using fecal samples (n = 173) from domestic cats living in the northeastern region of Brazil. Samples were examined through the FLOTAC technique and the overall results showed positivity of 65.31% (113/173) among the samples analyzed. Coinfections were observed in 46.01% (52/113) of the positive samples. The most common parasites detected were Ancylostoma sp., Toxocara cati, Strongyloides stercoralis, Trichuris sp., Dipylidium caninum and Cystoisospora sp. From an epidemiological point of view, these findings are important, especially considering that zoonotic parasites (e.g. Ancylostoma sp. and Toxocara sp.) were the nematodes most frequently diagnosed in this study. Therefore, the human population living in close contact with cats is at risk of infection caused by the zoonotic helminths of these animals. In addition, for the first time the FLOTAC has been used to diagnosing gastrointestinal parasites of cats in Brazil.

Keywords:
Copromicroscopic diagnosis; helminth; protozoa; felines; zoonosis; FLOTAC

Resumo

Helmintos gastrointestinais são considerados os mais frequentes parasitos que afetam gatos em todo o mundo. O correto diagnóstico desses parasitos, em animais que vivem em áreas urbanas, é crucial, especialmente quando considerado o potencial zoonótico de algumas espécies (ex. Ancylostoma sp. e Toxocara sp.). Neste estudo, uma pesquisa coproparasitológica foi realizada, utilizando-se amostras de fezes (n = 173) de gatos domésticos da região Nordeste do Brasil. As amostras foram examinadas através da técnica FLOTAC, e os resultados gerais mostraram uma positividade de 65,31% (113/173). Co-infecções foram observadas em 46,01% (52/113) das amostras positivas. Os parasitas mais comuns aqui detectados foram Ancylostoma sp., Toxocara cati, Strongyloides stercoralis, Trichuris sp., Dipylidium caninum e Cystoisospora sp. De um ponto de vista epidemiológico, esses resultados são importantes, especialmente considerando que os parasitos zoonóticos (ex. Ancylostoma sp. e Toxocara sp.) foram os mais frequentes nematódeos diagnosticados neste estudo. Portanto, a população humana, em estreito convívio com esses animais, apresenta risco de infecção por helmintos de caráter zoonótico. Além disso, pela primeira vez, a técnica de FLOTAC tem sido utilizada no diagnóstico de parasitos gastrointestinais em gatos no Brasil.

Palavras-chave:
Diagnóstico coproparasitológico; helmintos; protozoários; felinos; zoonoses; FLOTAC

Introduction

Recently, gastrointestinal helminths of cats have been deemed to be major problem within the veterinary clinical medicine of pets (FUNADA et al., 2007Funada MR, Pena HFJ, Soares RM, Amaku M, Gennari SM. Frequência de parasitos gastrintestinais em cães e gatos atendidos em hospital-escola veterinário da cidade de São Paulo. Arq Bras Med Vet Zootec 2007; 59(5): 1338-1340. http://dx.doi.org/10.1590/S0102-09352007000500038.
http://dx.doi.org/10.1590/S0102-09352007...
). A wide range of intestinal parasites (e.g. Ancylostoma sp., Toxocara cati, Trichuris sp. and Dipylidium caninum) has been reported in domestic cats worldwide (TRAVERSA, 2011Traversa D. Are we paying too much attention to cardio-pulmonary nematodes and neglecting old-fashioned worms like Trichuris vulpis?Parasit Vectors 2011; 4(1): 32. http://dx.doi.org/10.1186/1756-3305-4-32. PMid:21385441.
http://dx.doi.org/10.1186/1756-3305-4-32...
; WEI et al., 2014Wei YB, Yu ZH, Gao LL, Wu XY, Shi SJ, Yin LX, et al. infection in an infant: one case report. Dipylidium caninumZhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 2014; 26(3): 1. PMid:25345179.; RIBEIRO, 2015Ribeiro CM. Enfermidades parasitárias por protozoários em pequenos animais. Rio de Janeiro: Rubio; 2015. 64 p.). Nevertheless, the nematode species Ancylostoma sp. and Toxocara cati, which are the causative agents of cutaneous and visceral larva migrans, respectively, are undoubtedly the ones most frequently reported (REY, 2008Rey L. Parasitologia: parasitos e doenças parasitárias do homem nos trópicos ocidentais. 4th ed. Rio de Janeiro: Guanabara Koogan; 2008.; RODRÍGUEZ et al., 2006Rodríguez PF, Ripoll BED, Alberto EB, Sotelo JA. y Síndrome Larva Toxocara canisMigrans Visceralis.Rev Elec Vet REDVET 2006; 7(4): 1-42.).

Detection of these parasites in cats is generally based on copromicroscopic methods. Among the main diagnostic techniques, those based on flotation, sedimentation and centrifuge-flotation have been widely used because they present low cost and are easily performed (OLIVEIRA-SEQUEIRA et al., 2002Oliveira-Sequeira TCG, Amarante AFT, Ferrari TB, Nunes LC. Prevalence of intestinal parasites in dogs from São Paulo State, Brazil. Vet Parasitol 2002; 103(1-2): 19-27. http://dx.doi.org/10.1016/S0304-4017(01)00575-1. PMid:11750997.
http://dx.doi.org/10.1016/S0304-4017(01)...
; FISHER, 2003Fisher M. Toxocara cati: an underestimated zoonotic agent. Trends Parasitol 2003; 19(4): 167-170. http://dx.doi.org/10.1016/S1471-4922(03)00027-8. PMid:12689646.
http://dx.doi.org/10.1016/S1471-4922(03)...
). However, these techniques present low sensitivity and it is believed that in many epidemiological surveys, the results have been underestimated. Recently, a reliable tool known as the FLOTAC technique has been used to diagnosing intestinal parasites of animals and humans (CRINGOLI et al., 2010Cringoli G, Rinaldi L, Maurelli MP, Utzinger J. FLOTAC: new multivalente techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 2010; 5(3): 503-515. http://dx.doi.org/10.1038/nprot.2009.235. PMid:20203667.
http://dx.doi.org/10.1038/nprot.2009.235...
; CRINGOLI et al., 2013Cringoli G, Rinaldi L, Albonico M, Bergquist R, Utzinger J. Geospatial (s) tools: integration of advanced epidemiological sampling and novel diagnostics. Geospat Health 2013; 7(2): 399-404. http://dx.doi.org/10.4081/gh.2013.97. PMid:23733301.
http://dx.doi.org/10.4081/gh.2013.97...
). It has been demonstrated that this diagnostic method presents high sensitivity for detecting eggs and/or oocysts of parasites in several species of animals (RINALDI et al., 2011Rinaldi L, Coles GC, Maurelli MP, Musella V, Cringoli G. Calibration and diagnostic accuracy of simple flotation, McMaster and FLOTAC for parasite egg counts in sheep. Vet Parasitol 2011; 177(3-4): 345-352. http://dx.doi.org/10.1016/j.vetpar.2010.12.010. PMid:21216533.
http://dx.doi.org/10.1016/j.vetpar.2010....
; LIMA et al., 2015Lima VFS, Cringoli G, Rinaldi L, Monteiro MFM, Calado AMC, Ramos RAN, et al. A comparison of mini-FLOTAC and FLOTAC with classic methods to diagnosing intestinal parasites of dogs from Brazil. Parasitol Res 2015; 114(9): 3529-3533. http://dx.doi.org/10.1007/s00436-015-4605-x. PMid:26122998.
http://dx.doi.org/10.1007/s00436-015-460...
).

Although correct diagnosis of these helminths in cats is pivotal for preventing spreading of the parasite and human infection, few studies have been conducted in Brazil, especially in urban areas. Therefore, the aim of this study was to detect the main gastrointestinal parasites affecting cats in an urban area in Brazil. In addition, the zoonotic risk presented by some nematode species (i.e. Ancylostoma sp. and Toxocara sp.) has been discussed.

Materials and Methods

Fecal samples (n=173) from domestic cats, aging from six months to eight years old, living in three different municipalities (Recife (n=154) 08°03'14” S and 34°52'52” W; Bezerros (n=7) 8°14’33” S and 35°47’7” W; and Limoeiro (n=12) 7°52’20” S and 35°26’23” W) in the state of Pernambuco were used in this study. All animals were domiciled cats, which had free access to the backyard (when present). In addition, all animals were ectoparasites (fleas and lice) free. All the samples were collected directly from the floor, put into plastic vials, identified and stored in isothermal boxes at 8 °C until laboratory processing, which occurred maximum six hours after collection. In order to avoid environmental contamination only the top of the fecal material was collected, while the material at the surface in contact with the floor was not taken into considered.

Samples were analyzed individually using the FLOTAC dual technique (CRINGOLI et al., 2010Cringoli G, Rinaldi L, Maurelli MP, Utzinger J. FLOTAC: new multivalente techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 2010; 5(3): 503-515. http://dx.doi.org/10.1038/nprot.2009.235. PMid:20203667.
http://dx.doi.org/10.1038/nprot.2009.235...
). FLOTAC was performed using two flotation solutions: saturated sodium chloride (1.200 s.g.) and zinc sulphate (1.350 s.g.). The method used here was performed in accordance with the instructions stated in the original description of the technique.

Results

Eggs and/or oocysts of gastrointestinal parasites were detected in 65.31% (113/173) of the samples analyzed. Helminth eggs (Ancylostoma sp., Toxocara cati, Strongyloides stercoralis and Trichuris sp., and ovigerous capsules of Dipylidium caninum) were detected in 100% (113/113) of the positive samples, whereas only in 25.6% (29/113) of the samples were observed oocysts of Cystoisospora sp.. It is important to highlight that Ancylostoma sp. and Toxocara cati, which are parasites with zoonotic potential, were the ones most frequently reported in this study, presenting positivity of 67.2% (76/113) and 40.7% (46/113), respectively (Table 1). Interestingly, all the samples were found to be negative for the presence of lungworm larvae.

Table 1
Absolute and relative frequencies of eggs of gastrointestinal parasites of cats detected through the FLOTAC technique.

Coinfections were detected in 46.01% (52/113) of the positive samples (Table 2), and double and triple coinfections were observed in 31.85% (36/113) and 13.27% (15/113) of the fecal samples. All eggs and oocysts were identified based on morphological features provided in Urquhart et al. (1991)Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW. Parasitologia veterinária. Rio de Janeiro: Guanabara Koogan; 1991. 306 p..

Table 2
Coinfections of gastrointestinal parasites of cats detected through the FLOTAC technique.

Discussion

This study assessed the frequency of gastrointestinal parasites in the feces of domestic cats living in urban areas in the northeastern region of Brazil. The overall frequency detected here (i.e. 65.31%) was higher than the levels previously reported in other studies, in which positivity of 53.8% (PEREIRA et al., 2012Pereira NV, Souza FS, Piranda EM, Cançado PHD, Lisbôa RS. Enteroparasitos encontrados em cães e gatos atendidos em duas clínicas veterinárias na cidade de Manaus, AM. Amazon Sci 2012; 1(1): 8-17.) and 43.91% (FERREIRA et al., 2013Ferreira FP, Dias RCF, Martins TA, Constantino C, Pasquali AKS, Vidotto O, et al. Frequência de parasitas gastrointestinais em cães e gatos do município de Londrina, PR, com enfoque em saúde pública. Semina: Cienc Agrar 2013; 34(6): 3851-3858.) was observed. Recently, a study conducted in the state of Mato Grosso detected gastrointestinal parasites in 67.12% of the cats on which postmortem examinations were conducted (RAMOS et al., 2013Ramos DGS, Scheremeta RGAC, Oliveira ACS, Sinkoc AL, Pacheco RC. Survey of helminth parasites of cats from the metropolitan area of Cuiabá, Mato Grosso, Brazil. Rev Bras Parasitol Vet 2013; 22(2): 201-206. http://dx.doi.org/10.1590/S1984-29612013000200040. PMid:23856737.
http://dx.doi.org/10.1590/S1984-29612013...
). Differences between the frequencies observed here might be related to several factors such as the animals’ ages, parasite load, sample conservation, environmental contamination and type of diagnostic test (VANDAMME & ELLIS, 2004Vandamme TF, Ellis KJ. Issues and challenges in developing ruminal drug delivery systems. Adv Drug Deliv Rev 2004; 56(10): 1415-1436. http://dx.doi.org/10.1016/j.addr.2004.02.011. PMid:15191790.
http://dx.doi.org/10.1016/j.addr.2004.02...
). In the present survey, helminth eggs were more frequently detected than were oocysts of protozoa. It has already been demonstrated that this is a common finding because helminth eggs are more easily detected in the environment, which may be an important source of infection for cats (COELHO et al., 2009Coelho WMD, Amarante AFT, Soutello RVG, Meireles MV, Bresciani KDS. Ocorrência de parasitos gastrintestinais em amostras fecais de felinos no município de Andradina, São Paulo. Rev Bras Parasitol Vet 2009; 18(2): 46-49. http://dx.doi.org/10.4322/rbpv.01802010. PMid:19602317.
http://dx.doi.org/10.4322/rbpv.01802010...
).

In previous copromicroscopic surveys using different techniques, Ancylostoma sp. was the most prevalent gastrointestinal parasite (SCHUSTER et al., 2009Schuster RK, Thomas K, Sivakumar S, O’Donovan D. The parasite fauna of stray domestic cats (Felis catus) in Dubai, United Arab Emirates. Parasitol Res 2009; 105(1): 125-134. http://dx.doi.org/10.1007/s00436-009-1372-6. PMid:19238440.
http://dx.doi.org/10.1007/s00436-009-137...
; MILLÁN & CASANOVA, 2009Millán J, Casanova JC. High prevalence of helminth parasites in feral cats in Majorca Island (Spain). Parasitol Res 2009; 106(1): 183-188. http://dx.doi.org/10.1007/s00436-009-1647-y. PMid:19841943.
http://dx.doi.org/10.1007/s00436-009-164...
). In the present study, the high prevalence of infection due to this nematode was an expected finding, since it has been demonstrated that parasitism due to Ancylostoma sp. may occurs throughout the animal’s life (URQUHART et al., 1991Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW. Parasitologia veterinária. Rio de Janeiro: Guanabara Koogan; 1991. 306 p.). In fact, it is known that this nematode does not depend on the immunity acquired during the life of the animal (BOAG et al., 2003Boag PR, Parsons JC, Presidente PJ, Spithill TW, Sexton JL. Characterisation of humoral immune responses in dogs vaccinated with irradiated Ancylostoma caninum.Vet Immunol Immunopathol 2003; 92(1-2): 87-94. http://dx.doi.org/10.1016/S0165-2427(03)00006-0. PMid:12628766.
http://dx.doi.org/10.1016/S0165-2427(03)...
). Similarly, Toxocara sp. has been considered to be one of the most prevalent helminths in cats throughout the world, with prevalence rates ranging from 8% to 55.2% (ABU-MADI et al., 2008Abu-Madi MA, Pal P, Al-Thani A, Lewis JW. Descriptive epidemiology of intestinal helminth parasites from stray cat populations in Qatar. J Helminthol 2008; 82(1): 59-68. http://dx.doi.org/10.1017/S0022149X07870830. PMid:18199386.
http://dx.doi.org/10.1017/S0022149X07870...
; CALVETE et al., 1998Calvete C, Lucientes J, Castillo JA, Estrada R, Gracia MJ, Peribáñez MA, et al. Gastrointestinal helminth parasites in stray cats from the mid-Ebro Valley, Spain. Vet Parasitol 1998; 75(2-3): 235-240. http://dx.doi.org/10.1016/S0304-4017(97)00182-9. PMid:9637225.
http://dx.doi.org/10.1016/S0304-4017(97)...
). Although it is most common in young animals (up to six months of age), toxocarid species have been also diagnosed in adult felines (OGASSAWARA et al., 1986Ogassawara S, Benassi S, Larsson CE, Leme PTZ, Hagiwara MK. Prevalência de infecções helmínticas em gatos na cidade de São Paulo. Rev Fac Med Vet Zootec Univ São Paulo 1986; 23(2): 145-149. http://dx.doi.org/10.11606/issn.2318-3659.v23i2p145-149.
http://dx.doi.org/10.11606/issn.2318-365...
). It is important to highlight that both species reported above present great importance with regard to public health, because they are causative agents of cutaneous and visceral larva migrans in the human population.

Albeit less frequently, infections by other gastrointestinal helminths were detected in this study. For instance, eggs of Trichuris sp. were detected in 1.7% (2/113) of the samples analyzed, these data are similar to others previously reported (STALLIVIERE et al., 2009Stalliviere FM, Bellato V, Souza AP, Sartor AA, Moura AB, Rosa LD. Ectoparasitos e helmintos intestinais em Felis catus domesticus, da cidade de Lages, SC, Brasil e aspectos sócioeconômicos e culturais das famílias dos proprietários dos animais. Rev Bras Parasitol Vet 2009; 18(4): 26-31. http://dx.doi.org/10.4322/rbpv.01804005. PMid:20040205.
http://dx.doi.org/10.4322/rbpv.01804005...
; TESSEROLLI et al., 2005Tesserolli GL, Fayzano L, Agottani JVB. Ocorrência de parasitas gastrintestinais em fezes de cães e gatos, Curitiba – PR. Rev Acad 2005; 3(4): 31-34.). On the other hand, ovigerous capsule of D. caninum were detected only in 1% (1/113) of the positive samples, thus indicating a low parasite burden in cats and consequently low transmission between these animals. Moreover, Cystoisospora sp. was the only protozoon detected here. The prevalence of coccidian species in pets may vary widely depending on the technique used. It is important to note that the present study used the FLOTAC technique, which is a tool that presents high sensitivity in relation to the classical methods (LIMA et al., 2015Lima VFS, Cringoli G, Rinaldi L, Monteiro MFM, Calado AMC, Ramos RAN, et al. A comparison of mini-FLOTAC and FLOTAC with classic methods to diagnosing intestinal parasites of dogs from Brazil. Parasitol Res 2015; 114(9): 3529-3533. http://dx.doi.org/10.1007/s00436-015-4605-x. PMid:26122998.
http://dx.doi.org/10.1007/s00436-015-460...
). The high percentage of positivity (i.e. 25.6%; 29/113) detected here, probably occurred due to the high sensitivity presented by this technique for detecting eggs, larvae and/or oocysts.

Occurrences of coinfections are common findings and might result from environmental contamination (COELHO et al., 2009Coelho WMD, Amarante AFT, Soutello RVG, Meireles MV, Bresciani KDS. Ocorrência de parasitos gastrintestinais em amostras fecais de felinos no município de Andradina, São Paulo. Rev Bras Parasitol Vet 2009; 18(2): 46-49. http://dx.doi.org/10.4322/rbpv.01802010. PMid:19602317.
http://dx.doi.org/10.4322/rbpv.01802010...
; RAGOZO et al., 2002Ragozo AMA, Muradian V, Silva JCR, Caravieri R, Amajoner VR, Magnabosco C, et al. Ocorrência de parasitos gastrintestinais em fezes de gatos das cidades de São Paulo e Guarulhos. Braz J Vet Res Anim Sci 2002; 39(5): 244-246. http://dx.doi.org/10.1590/S1413-95962002000500005.
http://dx.doi.org/10.1590/S1413-95962002...
). Interestingly, to the best of the present authors’ knowledge, our study provides the first report in the scientific literature of simultaneous infection by Ancylostoma sp., T. cati and S. stercoralis.

In conclusion, our data indicate that gastrointestinal parasites have high prevalence among domestic cats living in the northeastern region of Brazil. From an epidemiological point of view, these findings are important, especially considering that zoonotic parasites (e.g. Ancylostoma sp. and Toxocara sp.) were the nematodes most frequently diagnosed in this study. Therefore, the human population living in close contact with cats is at risk of infection by the helminths of these animals. In addition, this is the first report of the use of the FLOTAC technique for diagnosing gastrointestinal parasites of cats in Brazil.

References

  • Abu-Madi MA, Pal P, Al-Thani A, Lewis JW. Descriptive epidemiology of intestinal helminth parasites from stray cat populations in Qatar. J Helminthol 2008; 82(1): 59-68. http://dx.doi.org/10.1017/S0022149X07870830 PMid:18199386.
    » http://dx.doi.org/10.1017/S0022149X07870830
  • Boag PR, Parsons JC, Presidente PJ, Spithill TW, Sexton JL. Characterisation of humoral immune responses in dogs vaccinated with irradiated Ancylostoma caninum.Vet Immunol Immunopathol 2003; 92(1-2): 87-94. http://dx.doi.org/10.1016/S0165-2427(03)00006-0 PMid:12628766.
    » http://dx.doi.org/10.1016/S0165-2427(03)00006-0
  • Calvete C, Lucientes J, Castillo JA, Estrada R, Gracia MJ, Peribáñez MA, et al. Gastrointestinal helminth parasites in stray cats from the mid-Ebro Valley, Spain. Vet Parasitol 1998; 75(2-3): 235-240. http://dx.doi.org/10.1016/S0304-4017(97)00182-9 PMid:9637225.
    » http://dx.doi.org/10.1016/S0304-4017(97)00182-9
  • Coelho WMD, Amarante AFT, Soutello RVG, Meireles MV, Bresciani KDS. Ocorrência de parasitos gastrintestinais em amostras fecais de felinos no município de Andradina, São Paulo. Rev Bras Parasitol Vet 2009; 18(2): 46-49. http://dx.doi.org/10.4322/rbpv.01802010 PMid:19602317.
    » http://dx.doi.org/10.4322/rbpv.01802010
  • Cringoli G, Rinaldi L, Albonico M, Bergquist R, Utzinger J. Geospatial (s) tools: integration of advanced epidemiological sampling and novel diagnostics. Geospat Health 2013; 7(2): 399-404. http://dx.doi.org/10.4081/gh.2013.97 PMid:23733301.
    » http://dx.doi.org/10.4081/gh.2013.97
  • Cringoli G, Rinaldi L, Maurelli MP, Utzinger J. FLOTAC: new multivalente techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 2010; 5(3): 503-515. http://dx.doi.org/10.1038/nprot.2009.235 PMid:20203667.
    » http://dx.doi.org/10.1038/nprot.2009.235
  • Ferreira FP, Dias RCF, Martins TA, Constantino C, Pasquali AKS, Vidotto O, et al. Frequência de parasitas gastrointestinais em cães e gatos do município de Londrina, PR, com enfoque em saúde pública. Semina: Cienc Agrar 2013; 34(6): 3851-3858.
  • Fisher M. Toxocara cati: an underestimated zoonotic agent. Trends Parasitol 2003; 19(4): 167-170. http://dx.doi.org/10.1016/S1471-4922(03)00027-8 PMid:12689646.
    » http://dx.doi.org/10.1016/S1471-4922(03)00027-8
  • Funada MR, Pena HFJ, Soares RM, Amaku M, Gennari SM. Frequência de parasitos gastrintestinais em cães e gatos atendidos em hospital-escola veterinário da cidade de São Paulo. Arq Bras Med Vet Zootec 2007; 59(5): 1338-1340. http://dx.doi.org/10.1590/S0102-09352007000500038
    » http://dx.doi.org/10.1590/S0102-09352007000500038
  • Lima VFS, Cringoli G, Rinaldi L, Monteiro MFM, Calado AMC, Ramos RAN, et al. A comparison of mini-FLOTAC and FLOTAC with classic methods to diagnosing intestinal parasites of dogs from Brazil. Parasitol Res 2015; 114(9): 3529-3533. http://dx.doi.org/10.1007/s00436-015-4605-x PMid:26122998.
    » http://dx.doi.org/10.1007/s00436-015-4605-x
  • Millán J, Casanova JC. High prevalence of helminth parasites in feral cats in Majorca Island (Spain). Parasitol Res 2009; 106(1): 183-188. http://dx.doi.org/10.1007/s00436-009-1647-y PMid:19841943.
    » http://dx.doi.org/10.1007/s00436-009-1647-y
  • Ogassawara S, Benassi S, Larsson CE, Leme PTZ, Hagiwara MK. Prevalência de infecções helmínticas em gatos na cidade de São Paulo. Rev Fac Med Vet Zootec Univ São Paulo 1986; 23(2): 145-149. http://dx.doi.org/10.11606/issn.2318-3659.v23i2p145-149
    » http://dx.doi.org/10.11606/issn.2318-3659.v23i2p145-149
  • Oliveira-Sequeira TCG, Amarante AFT, Ferrari TB, Nunes LC. Prevalence of intestinal parasites in dogs from São Paulo State, Brazil. Vet Parasitol 2002; 103(1-2): 19-27. http://dx.doi.org/10.1016/S0304-4017(01)00575-1 PMid:11750997.
    » http://dx.doi.org/10.1016/S0304-4017(01)00575-1
  • Pereira NV, Souza FS, Piranda EM, Cançado PHD, Lisbôa RS. Enteroparasitos encontrados em cães e gatos atendidos em duas clínicas veterinárias na cidade de Manaus, AM. Amazon Sci 2012; 1(1): 8-17.
  • Ragozo AMA, Muradian V, Silva JCR, Caravieri R, Amajoner VR, Magnabosco C, et al. Ocorrência de parasitos gastrintestinais em fezes de gatos das cidades de São Paulo e Guarulhos. Braz J Vet Res Anim Sci 2002; 39(5): 244-246. http://dx.doi.org/10.1590/S1413-95962002000500005
    » http://dx.doi.org/10.1590/S1413-95962002000500005
  • Ramos DGS, Scheremeta RGAC, Oliveira ACS, Sinkoc AL, Pacheco RC. Survey of helminth parasites of cats from the metropolitan area of Cuiabá, Mato Grosso, Brazil. Rev Bras Parasitol Vet 2013; 22(2): 201-206. http://dx.doi.org/10.1590/S1984-29612013000200040 PMid:23856737.
    » http://dx.doi.org/10.1590/S1984-29612013000200040
  • Rey L. Parasitologia: parasitos e doenças parasitárias do homem nos trópicos ocidentais. 4th ed. Rio de Janeiro: Guanabara Koogan; 2008.
  • Ribeiro CM. Enfermidades parasitárias por protozoários em pequenos animais. Rio de Janeiro: Rubio; 2015. 64 p.
  • Rinaldi L, Coles GC, Maurelli MP, Musella V, Cringoli G. Calibration and diagnostic accuracy of simple flotation, McMaster and FLOTAC for parasite egg counts in sheep. Vet Parasitol 2011; 177(3-4): 345-352. http://dx.doi.org/10.1016/j.vetpar.2010.12.010 PMid:21216533.
    » http://dx.doi.org/10.1016/j.vetpar.2010.12.010
  • Rodríguez PF, Ripoll BED, Alberto EB, Sotelo JA. y Síndrome Larva Toxocara canisMigrans Visceralis.Rev Elec Vet REDVET 2006; 7(4): 1-42.
  • Schuster RK, Thomas K, Sivakumar S, O’Donovan D. The parasite fauna of stray domestic cats (Felis catus) in Dubai, United Arab Emirates. Parasitol Res 2009; 105(1): 125-134. http://dx.doi.org/10.1007/s00436-009-1372-6 PMid:19238440.
    » http://dx.doi.org/10.1007/s00436-009-1372-6
  • Stalliviere FM, Bellato V, Souza AP, Sartor AA, Moura AB, Rosa LD. Ectoparasitos e helmintos intestinais em Felis catus domesticus, da cidade de Lages, SC, Brasil e aspectos sócioeconômicos e culturais das famílias dos proprietários dos animais. Rev Bras Parasitol Vet 2009; 18(4): 26-31. http://dx.doi.org/10.4322/rbpv.01804005 PMid:20040205.
    » http://dx.doi.org/10.4322/rbpv.01804005
  • Tesserolli GL, Fayzano L, Agottani JVB. Ocorrência de parasitas gastrintestinais em fezes de cães e gatos, Curitiba – PR. Rev Acad 2005; 3(4): 31-34.
  • Traversa D. Are we paying too much attention to cardio-pulmonary nematodes and neglecting old-fashioned worms like Trichuris vulpis?Parasit Vectors 2011; 4(1): 32. http://dx.doi.org/10.1186/1756-3305-4-32 PMid:21385441.
    » http://dx.doi.org/10.1186/1756-3305-4-32
  • Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW. Parasitologia veterinária. Rio de Janeiro: Guanabara Koogan; 1991. 306 p.
  • Vandamme TF, Ellis KJ. Issues and challenges in developing ruminal drug delivery systems. Adv Drug Deliv Rev 2004; 56(10): 1415-1436. http://dx.doi.org/10.1016/j.addr.2004.02.011 PMid:15191790.
    » http://dx.doi.org/10.1016/j.addr.2004.02.011
  • Wei YB, Yu ZH, Gao LL, Wu XY, Shi SJ, Yin LX, et al. infection in an infant: one case report. Dipylidium caninumZhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 2014; 26(3): 1. PMid:25345179.

Publication Dates

  • Publication in this collection
    12 Apr 2016
  • Date of issue
    Apr-Jun 2016

History

  • Received
    02 Oct 2015
  • Accepted
    18 Nov 2015
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br