Gastrointestinal Parasites in Domestic Cats

With the domestication of animals, the contact between the latter and humans has intensified, favoring the occurrence of parasitic zoonoses (Brooker et al., 2004; Landmann et al., 2003; Katagiri et al., 2007; Thompson et al., 2008; Araújo et al., 2008). This is more evident in places where hygienic-sanitary conditions are poor (Ederli et al., 2008) and human or animal feces are present in the environment (Gatei et al., 2008; Smith et al., 2010; Sousa et al., 2010; Yoder et al., 2010).


Physiopathogenesis
Parasite migration and spoliation of larvae of A. braziliense and A. caninum lead to a disease named cutaneous larva migrans (CLM) (Hunter & Worth 1945;Hanslik et al.,, 1998;Kwon et al., 2003;Caumes et al., 2004).High levels of intestinal lesions and is mainly related to the number of worms present in the intestinal lumen, as well as to the age of animals (Rey, 2001;Fortes, 2004).

Biology
Except for D. caninum which needs fleas as intermediate host, parasites belonging to the genera Ancylostoma and Toxocara areoelomic cavity of these insects and, when ingested by a mammal biologically defined as host, the parasite is released in the small intestine, where it establishes (Rey, 2001;Fortes, 2004).

Clinical signs
The number of adult parasites in the animals is a determinant for the infection severity and the manifestation of clinical signs.Dermatitis, eczema, itch, hypersensitivity and anemia are some of the diverse clinical manifestations shown by animals parasitized by Ancylostoma (Rey, 2001;Fortes, 2004).
Human toxocariasis may be associated with the formation of pyogenic abscesses (Rayes & Lambertucci, 1999), asthma (Tonelli, 2005), and several forms of ocular, hepatic and renal disorders (Jacob et al., 1994).These clinical signs are similar to those observed in domestic cats, especially in pups (Fortes, 2004).

Diagnosis
Diagnosis must be based on the animal history, including detailed anamnesis with special attention to the clinical manifestations that may be easily confused with those of other diseases.Thus, skin biopsy can also be performed to detect Ancylostoma (Acha & Szyfres, 2003), as well as serological tests to detect anti-Toxocara antibodies (Marchioro et al., 2011).In addition, coproparasitological tests have been shown highly effective in detecting these parasites (Hoffmann, 1987;Coelho, 2009).
Different prevalence levels can be found for these parasites according to the adopted diagnosis technique.In our study, parasitological necropsy was the "gold standard" test, while the techniques of flotation in saturated sodium chloride solution of 1.182 density (Willis, 1921) and spontaneous sedimentation in water showed different sensitivity and specificity levels (Coelho et al., 2011a).

Zoonosis 418
This same difference was observed by our group in another study, in which fecal samples from 51 cats were analyzed, indicating the presence of eggs of Ancylostoma spp. in 96% samples according to the method of Willis and in 21.5% samples according to the technique of Faust.This study also indicated divergence between these techniques as to detection Toxocara eggs (43.1% by Willis and 9.8% by Faust) and D. caninum ovigerous capsules (19.6% by Willis and 5.8% by Faust (Coelho et al., 2009).
Thus, there is the need of associating different coproparasitological techniques in the laboratorial routine in order to increase the efficiency of the diagnosis of helminths and protozoa (Huber et al., 2004;Coelho et al., 2009).
Our group has worked to established an automated standard diagnosis method named Modified TF-Test ® , which allows 3D computer analysis of parasitic structures present in the feces of animals by means of image recombination, leading thus to an important diagnostic innovation concerning helminths and protozoa affecting pets.

Agents
Cryptosporidium spp.and Giardia spp.
On account of their low host selectivity, Cryptosporidium felis (Huber et al., 2007) and several other Cryptosporidium species have been described in cats, including Cryptosporidium parvum (Sargent et al., 1998) and Cryptosporidium muris (Pavlasek & Ryan, 2007).
In Australia, Palmer et al. (2008) used molecular analyses and verified that Giardia Assemblages F and D are present in the feces of domestic cats.This is important since infection by Giardia duodenalis assemblages are frequent in humans by assemblage B, while in pets assemblages C and D occur in dogs and assemblage F in cats (Monis & Thompson, 2003;Souza et al., 2007;Xiao & Fayer., 2008), there is also the possibility of cross infection by Giardia assemblages between animals and humans (Traub et al., 2004;Palmer et al., 2008;Feng & Xiao, 2011).
In our study, Giardia spp. was detected in 5.9% (3/51) fecal samples from domestic cats.Also in Brazil, Gennari et al. (1999) noted that 16.04% of 187 fecal samples from cats were positive for Giardia spp.In Australia, MacGlade et al. (2003) analyzed fecal samples from 40 cats and observed approximately 60% positivity prevalence for Giardia.
A similar occurrence was detected in Germany between 1999 and 2002, when fecal samples from 3164 cats were analyzed indicating that 51.6% had cysts of Giardia spp.(Barutzki & Schaper, 2003).

Physiopathogenesis
The pathophysiological mechanism of cryptosporidiosis consists in its intraenterocytic stage.This enteroinfection causes atrophy, fusion of intestinal villi and inflammation, which result in absorptive surface loss and unbalanced nutrient transport.It is not clear yet whether the parasite interferes with the cell function but it seems capable of inducing or inhibiting cell apoptosis (Chen et al., 1998;Dagci et al., 2002;Buret et al., 2003;Leav et al., 2003).
Histopathological analyses have revealed that cryptosporidiosis may lead to minimal inflammatory infiltration and villus blunting, while changes are more pronounced in immunosuppressed individuals, including greater inflammatory changes, epithelial cell barrier rupture with more extensive and intense inflammatory cell infiltration.Massive parasite infection in the enterocytes stimulates local inflammatory reaction, increasing the levels of prostaglandins, several cytokines, especially interferon.These inflammatory mediators change solute transport in the intestinal epithelial cell, leading to osmotic diarrhea (Leav et al., 2003).
Diarrhea due to poor absorption results of the interaction between parasitic products such as proteinases, which rupture the epithelial barrier, and the immune/inflammatory responses of the host, favoring deficient absorption of electrolytes and nutrients, combined with the hypersecretion of chlorine and water (Argenzio et al., 1990;Huang & White, 2006), inducing intestinal abnormalities, especially due to the activation of CD8+ lymphocytes in the intraepithelial compartment, with increased cytotoxic activity (Chai et al., 1999;Buret, 2009).
Parasitic infection by Giardia intestinalis is most frequently reported all over the word.It causes several intestinal, nutritional and general development disorders (Botero-Garcés et al., 2009;Singh et al., 2009).
Although giardiasis is an auto-limiting disease, it manifests in individuals mainly by means of acute diarrhea; however, asymptomatic chronic infections may occur, leading to malabsorption of vitamin A, B12 (Springer et al., 1997) and anemia due to iron deficiency (Ertan et al., 2002).
In Colombia, Botero-Garcés et al. ( 2009) verified that 27.6% of the 2035 studied children were infected by G. intestinalis and part of them had significant body development deficit.

Biology
As to Cryptosporidium biology, sporulated oocysts are ingested by the host and, following exposure to the gastric juice and pancreatic enzymes, excystation occurs in the duodenum releasing four sporozoites.The latter are covered by microvilli located in a parasitophorous vacuole and start the asexual reproduction.In this event, they develop successive merogonies, releasing eight and four sporozoites, respectively (Fortes et al., 2004).
The four merozoites released from the second merogony originate the sexual stages, resulting in the genesis of microgametes and macrogametes, which unite to form the zygote.Sporulation occurs inside the oocyst, developing four sporozoites.In this event, oocysts of thin (capable of starting a new cycle inside the same host by means of retroinfection) and thick wall (highly resistant under environmental conditions and released in the feces) are formed.In healthy people, the infection generally remains in the gastrointestinal tract (TZIPORI & GRIFFTHS, 1998).
Considering the biological cycle of Giardia, we must highlight that in addition to producing trophozoites and cysts, this flagellate protozoan is capable of infecting a large number of domestic animals (Geurden et al., 2010), as well as men (Thompson & Monis, 2004); this microorganism is also highly evolved and with the capacity for recombination among their Assemblages (Cacciò & Sprong, 2010).

Clinical signs
In general, the clinical signs of parasitized animals consist in diarrhea (Fortes, 2004).Gastrointestinal disorders may manifest severely in immunosuppressed individuals (Assefa et al., 2009), while clinical manifestation variation, infection persistence and severity of symptoms are directly correlated to TCD4+ lymphocyte count (Gupta et al., 2008).

Diagnosis
The diagnosis of Cryptosporidium spp.and Giardia spp.must always be made by associating two or more techniques in order to increase the diagnosis efficacy (Mtambo et al., 1992;Huber et al., 2004;Coelho et al., 2009).
The intermittent release of Cryptosporidium oocysts requires that coproparasitological tests be repeated, including new sample collection, even after a negative result (Huber et al., 2002;Brook et al., 2008;Huber et al., 2005).

Treatment
To treat cryptosporidiosis, nitazoxanide, trimethoprim-sulfamethoxazole and pyrimethamine can be used with certain efficacy once there is no immunosuppression associated.The treatment of giardiasis has included metronidazole, nitazoxanide, furazolidone, quinacrine and paramomycin (Petri Jr., 2003).
This was confirmed in our study, in which 15.7% (11/70) cats were seroreactive for T. gondii, which occurred mainly in young animals (Coelho et al., 2011b).Association between sex and breed with occurrence of infection by T. gondii was not verified by Bresciani et al. (2007); Pinto et al. (2009) and Dalla Rosa et al. (2010).

Physiopathogenesis
Soon after the ingestion of environmental oocysts or tissue cysts, the parasite causes systemic infection, resulting in bradyzoite production (Dubey, 2010).It must be highlighted that toxoplasmosis manifests more severely in immunosuppressed individuals, especially those showing TCD4 lymphocyte count lower than 100 cells per mm 3 (Hoffmann et al., 2007).

Biology
As to T. gondii biology, it is important to emphasize that this parasite has zoonotic potential (Dubey, 2010), showing oocysts capable of contaminating the environment and remaining infective for long periods (Elmore et al., 2010).
The occurrence of these protozoan diseases has been correlated to management, environment (Modolo et al. 2008), livestock by-products (Hiramoto et al., 2001) and even dissemination through water (Jones & Dubey, 2010).
It is an opportunistic infection, common in immunosuppressed patients, being the most common cause of secondary infection of the central nervous system, causing the occurrence of severe encephalitis (Collazos, 2003;Pradhan et al., 2007).
Experimental infections in cats are often asymptomatic, few animals get sick and deaths rarely occur (Omata et al., 1990;Sato et al., 1993).However, Dubey et al. (1996) and Elmore et al. (2010) report the occurrence of some lesions in neonates.
Experimental infections in cats are frequently asymptomatic, a few animals become ill and deaths are rare (Omata et al., 1990;Sato et al., 1993).Abortion and neonatal mortality have been described for pregnant cats orally inoculated with T. gondii tissue cysts (Powell et al., 2001).
The cutaneous form of Leishmania (V.) braziliensis was described in two cats from Rio de Janeiro State, Brazil (Schubach et al., 2004), while Leishmania (L.) amazonensis was described in Mato Grosso do Sul State (Souza et al., 2005).Craig et al. (1986) detected the occurrence of L. mexicana in cats from Texas, USA.
Studies of animal epidemiology have evidenced several infection prevalence levels according to the employed method and the study site.In our study, the analyzed tissue samples were from 52 domestic cats with 5.76% positivity.Similarly, Rossi et al. (2007) detected 6.7% positivity for Leishmania spp.among 200 analyzed cats.

Physiopathogenesis
After parasite replication, there is formation of perivascular congestion, mononuclear and neutrophil inflammatory infiltrate (Schubach et al., 2004) with secondary bacterial (Coelho et al. 2010) and fungal infections (Ozon et al., 1998) at the lesion sites.Lesions may be localized or systemic, affecting different organs, and may be associated with FIV/ FeLV; in these cases, the most severe form of the disease occur (Pennisi et al. 2002;2004).

Biology
This heteroxenic protozoan has mammals as its definitive hosts and dipterans of the genera Lutzomyia and Phlebotomus as intermediate hosts and vectors (Fortes, 2004).As the dog is considered the main urban reservoir of this disease although there are frequent reports of this infection in cats, the role of felines in the biological cycle of this parasite is not well defined yet (Dantas-Torres et al. 2006).
However, xenodiagnosis studies carried out by Maroli et al. (2007) proved that sand flies are capable of acquiring the infection from naturally infected cats.

Clinical signs
Skin lesions are more frequent among felines.Infected animals may show vegetative lesions, dermatitis and ulcers (Coelho et al. 2010a); healthy animals may also carry this parasite (Coelho et al., 2010b), and in some cases the disseminated form may occur (Ozon et al., 1998).
Clinical tests in places where the disease is endemic have shown that some infected animals remain seronegative (Ferrer et al., 1999).The serological titer shown by the animal is not related to the presence of symptoms and their intensity (Lima et al., 2003).On the other hand, PCR sensitivity and specificity are very high and this technique can detect the DNA of parasites in patients that remain clinically healthy for many years (Ferrer et al., 1999).
In a previous study, our research group suggested that antibody production in response to Leishmania spp. in felines is very low, which led to no serological reactions by means of IFA and ELISA (Serrano et al., 2008).

Final considerations
The high occurrence of endoparasites observed among domestic and stray animals evidences the zoonotic potential of these helminth and protozoan diseases, suggesting greater concern about the therapeutic and prophylactic measures feasible to the feline population.