Helminthic Parasites of Chickens ( Gallus Domesticus ) in Different Regions of São Paulo State , Brazil

I Laboratório de Parasitologia Animal/Instituto Biológico IB/APTA/SAA. Votuporanga, SP, Brazil II Instituto Agronômico de Campinas IAC/ APTA/SAA. Votuporanga, SP, Brazil III Departamento de Apoio, Produção e Saúde Animal/Faculdade de Medicina Veterinária/ UNESP. Araçatuba, SP, Brazil IV Departamento de Clínica, Cirurgia e Reprodução Animal/Faculdade de Medicina Veterinária/UNESP. Araçatuba, SP, Brazil


INTRODUCTION
The Brazilian poultry industry is an important national and international agribusiness sector.Among Brazilian states, São Paulo is the largest producer of commercial eggs and the fourth largest producer and exporter of chicken meat (UBA, 2014).According to the Brazilian Institute of Geography and Statistics (IBGE in Portuguese; Brasil, 2011), the Bastos and Amparo municipalities are the largest producers of commercial eggs and broilers, respectively.
However, alternative, semi-intensive and/or organic poultry production has conquered a significant share of the domestic market (Madeira et al., 2010) as a result of consumers' demand.These production systems are regulated in Brazil by the Ministry of Agriculture and Food Supply (Brasil, 1999).

Helminthic Parasites of Chickens (Gallus Domesticus) in Different Regions of São Paulo State, Brazil
report that helminth control is one of the key obstacles to successful production.
The class Trematoda includes 27 families, 125 genera, and approximately 500 species that are found in birds.Flukes are less host-specific than tapeworms, so wild birds often introduce infection in areas where domestic poultry is reared (Reid & McDougald, 1997).
Extensive studies on helminth parasites of poultry have been conducted, and new species have been described (Kolluri et al., 1985;Permin et al., 1999;Malhotra & Capoor, 1984;Dixit & Capoor, 1990).International studies examining poultry under different management conditions (Maqbool et al. (1998) in Pakistan; Permin et al. (1999) in Denmark; Hernández et al.(2002) in Cuba; Komba (2013) in Tanzania; Adang et al. (2014) in Nigeria; Alam et al.(2014) in Bangladesh and Butt et al. (2014)  In Brazil, Costa et al. (1986) conducted a literature review and described 50 species of helminthic parasites of chickens based on their occurrences in Brazilian states and territories.The literature review mentiones 29 parasites belonging to the class Nematoda, 12 belonging to the class Cestoda, eight belonging to the class Trematoda, and one belonging to the class Acanthocephala, with 19 nematode species, 10 cestode species, and two flukes present in poultry in São Paulo State.
During necropsy, the gastrointestinal organs of each chicken were separated, and their contents were collected to form a pool (five birds per farm) of each organ and was subsequently fixed in 70% ethanol.The remaining systems and organs were also assessed individually with respect to the helminthological study.
The evaluation of the small intestine employed the Mello-Campos method (Mello & Campos, 1974), which allows better recovery of cestode scolices attached to the intestinal mucosa.Stereomicroscopy was used to evaluate the collected materials, and light microscopy was used to identify the species according to their morphological characteristics (Yamaguthi, 1959;Schmidt, 1970;Reid &McDougald, 1987 andRuff &Norton, 1987).

RESULTS AND DISCUSSION
The results showed the presence of parasitic nematodes, cestodes, and trematodes in domestic chickens in the investigated regions of São Paulo (Tables 1 and 2).
Ascaridia galli and Heterakis gallinarum were the most frequently observed nematodes.Similar results were observed in São Paulo (Costa et al., 1986) and in a study performed in Rio de Janeiro (Gomes et al., 2009), where Ascaridia, Capillaria and Heterakis were the most commonly diagnosed nematodes in domestic chickens.Oxyspirura mansoni was found only in municipalities that belonged to the mesoregions of São José do Rio Preto and Presidente Prudente.Parasitism by Cheylospirura hamulosa was observed in only one chicken from the mesoregion of São José do Rio Preto, and Strongyloides sp. was observed in the municipality of Amparo.According to Costa et al. (1986), these species occur in São Paulo State and have been reported in the northern region of the state.Six cestode species were diagnosed (Amoebotaenia cuneata, Choanotaenia infundibulum, Hymenolepis sp., Raillietina cesticillus, Raillietina echinobothrida, and Raillietina tetragona -Figure 2).Out of these species, the occurrence of Hymenolepis sp. in São Paulo state had not been reported by Costa et al. (1986).The results showed the absence of parasitism by Davainea proglottina, one of the species considered most pathogenic for young chickens (Reid & McDougald, 1997); its occurrence was previously reported in São Paulo state (Costa et al., 1986).Choanotaenia infundibulum and Raillietina cesticillus were the most common cestodes.
Two species of trematodes were recovered from the cecum, Postharmostomum commutatum and Zygocotyle lunata (Figure 3), of chickens reared in the municipalities of Guatapará and Valentim Gentil, respectively.Postharmostomum commutatum was previously reported in Northern São Paulo State by Costa et al. (1986).Parasitological surveys at different locations and times are important for the epidemiological tracking of parasites because changes in animal husbandry due to advances in facilities, management, and preventive measures can lead to changes in the parasitic fauna of a particular location/region over time.Although most of the species diagnosed in the present study are consistent with those reported by Costa et al. (1996) with regard to their occurrence in São Paulo State, the number of species recovered was smaller than that compiled by those authors.However, this study detected the presence of Hymenolepis sp. and Zygocotyle lunata, which were not mentioned in the cited review.
Thus, further studies including additional municipalities and time periods are recommended for the constant tracking of the distribution of helminthic parasites in domestic poultry in São Paulo State and Brazil.