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Brazilian Journal of Poultry Science

versão impressa ISSN 1516-635Xversão On-line ISSN 1806-9061

Rev. Bras. Cienc. Avic. vol.18 no.1 Campinas jan./mar. 2016

http://dx.doi.org/10.1590/18069061-2015-0122 

Articles

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

GS da SilvaI 

DM RomeraII 

LEC FonsecaIII 

MV MeirelesIV 

ILaboratório de Parasitologia Animal/Instituto Biológico - IB/APTA/SAA. Votuporanga, SP, Brazil

IIInstituto Agronômico de Campinas - IAC/APTA/SAA. Votuporanga, SP, Brazil

IIIDepartamento de Apoio, Produção e Saúde Animal/Faculdade de Medicina Veterinária/UNESP. Araçatuba, SP, Brazil

IVDepartamento de Clínica, Cirurgia e Reprodução Animal/Faculdade de Medicina Veterinária/UNESP. Araçatuba, SP, Brazil


Abstract

The Brazilian poultry industry is an outstanding national and international agribusiness sector. Among the Brazilian states, São Paulo is the largest producer of commercial eggs and the fourth largest producer and exporter of chicken meat. Alternatively, semi-intensive and/or organic poultry production have also obtained a significant share of the domestic market as a result of consumer demand. Helminths affect the performance of the birds, causing significant direct or indirect losses. The objective of the present study was to identify the main helminth species present in chickens reared in 17 municipalities of the state of São Paulo. In total, 359 adult birds were investigated. The birds were reared in different housing systems and were obtained from 69 farms in the selected regions. The birds were submitted to procedures for the detection and identification of helminth parasites, following international standards. 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 based on their morphological characteristics. The following helminth species were diagnosed in chickens reared in 17 municipalities of the state of São Paulo: nematodes (Ascaridia galli, Capillaria sp., Cheilospirura hamulosa, Heterakis gallinarum, Oxyspirura mansoni, and Strongyloides sp.), cestodes (Amoebotaenia cuneata, Choanotaenia infundibulum, Hymenolepis sp., Raillietina cesticillus, Raillietina echinobothrida, and Raillietina tetragona), and trematodes (Zygocotyle lunata and Postharmostomum commutatum).

Keywords: Helminths; cestodes; nematodes; trematodes; chicken

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).

Helminths, when present, affect poultry performance, causing significant direct or indirect losses (Reid& McDougald, 1997; Silva, 2009). São Paulo chicken farmers that use semi-intensive systems report that helminth control is one of the key obstacles to successful production.

Nematodes are an important group of bird parasites both in terms of the number of species and the damage caused (Ruff & Nortton, 1997). Out of the 25 families of nematodes, 13 infect birds: Strongyloididae, Trichuridae, Syngamidae, Trichostrongylidae, Subuluridae, Heterakidae, Ascarididae, Spiruridae, Thelaziidae, Gnathostomatidae, Physalopteridea, Acuariidae, and Dipetalonematidae.

Approximately 1400 species of cestodes that parasitize domestic and wild birds have been described. Three families (Davainidae, Dilepididae, and Hymenolepidae) and ten genera (Amoebotaenia, Choanotaenia, Davainea, Diorchis, Drepanidotaenia, Imparmargo, Metroliasthes, Raillietina, Hymenolepis, and Fimbriaria) were identified in a survey performed in the United States (Reid & McDougald, 1997).

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 Pakistan) have diagnosed an increasing prevalence of helminths, including Acuaria hamulosa, Amoebotaenia cuneata, Ascaridia galli, Cappilaria sp., Choanotaenia infundibulum, Cotugnia digonopora, Dispharinx spiralis, Heterakis spp., Heterakis gallinarum, Heterakis isolonche, Hymenolepsis cantaniana, Hymenolepsis carioca, Raillietina spp., Raillietina cesticillus, Raillietina echinobothrida, Raillietina magninumida, Raillietina tetragona, and Subulura suctoria .

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.

An increasing occurrence of Ascaridia sp., Capillaria sp., Heterakis sp.,and Raillietina sp. was determined in poultry in Rio de Janeiro State, Brazil, (D'Avila et al., 2004 and Gomes et al., 2009). In Northern Paraná State, Brazil, Vieira (2010) described the occurrence of Ascaridia galli, Capillaria spp., Capillaria annatis, Capillaria annulata, Capillaria collaris, Capillaria contorta, Capillaria obsignata, Choanotaenia infundibulum, Dispharynx spiralis, Heterakis gallinarum, Hymenolepis carioca, Oxyspirura mansoni, Physaloptera truncata, Postharmostomum commutatum, Raillietina spp., Raillietina cesticillus, Raillietina echinobothrida, Raillietina tetragona, Strongyloides oswaldoi, Subulura brumpti, Syngamus trachea, Tropisurus americanus and Tropisurus fissispinus in birds. The helminths Ascaridia galli, Heterakis gallinarum, and Raillietina cesticillus showed a greater intensity of infection.

In a study evaluating antihelminthic drugs for poultry in Northwestern and Northeastern São Paulo State, Brazil, Silva et al. (1999) recorded the occurrence of the following species: Amoebotaenia cuneata, Davainea proglottina, Choanotaenia infundibulum, Hymenolepis cantaniana, Raillietina echinobothrida, R. cesticillus, and R. tetragona.

Literature describing helminthological surveys with domestic chickens (Gallus domesticus) in São Paulo State is scarce; the most important study, published in 1986 by Costa et al. , compiled the distribution of helminthic parasites of domestic animals in Brazil.

The objective of the present study was to determine the occurrence of the main helminth species present in domestic chickens (Gallus domesticus) reared in different municipalities of São Paulo State.

Material and Methods

The surveyed region included 17 municipalities (Amparo, Araçatuba, Bastos, Cedral, Fernandópolis, Guararapes, Guatapará, João Ramalho, Monte Alegre do Sul, Nhandeara, Panorama, Pereira Barreto, Presidente Prudente, Rancharia, Regente Feijó, Valentim Gentil and Votuporanga), according to divisions determined by the IBGE (Brazil, 2011). The municipalities included in the research represent 10 microregions (Andradina, Araçatuba, Amparo, Tupã, Presidente Prudente, Ribeirão Preto, São José do Rio Preto, Fernandópolis, Nhandeara, and Votuporanga) and, consequently, six mesoregions of São Paulo State.

In total, 359 adult chickens were investigated. The chickens were reared under different housing systems (extensive, intensive, and semi-intensive) and were obtained from 69 farms. The birds were submitted procedures for the detection and identification of helminthic parasites, following international criteria (Vich Topic GL21, 2001; Yazwinsk et al. , 2003).

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 and Ruff & 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).

Table 1 Helminths diagnosed in the regions of São Paulo State addressed in this study (17 municipalities/10 microregions/6 mesoregions).  

REGIONS N. BIRDS HELMINTHS
Mesoregions Microregions Municipalities Nematodes Cestodes Trematodes
Oxspirura mansoni Acuaria hamulosa Ascaridia galli Capillaria sp. Heterakis gallinarum Raillietina Postharmostomum commutatum Zygocotyle lunata
Strongyloides sp. Amoebotaenia cuneata Choanotaenia infundibulum Hymenolepis sp. cesticillus echinobothrida tetragona
Araçatuba Andradina Pereira Barreto 20 - - - - - - - + - + - - - -
Araçatuba Araçatuba 5 + - + + + - + + + + + + - -
Guararapes 5 - - - - + - + + + + - - - -
Campinas Amparo Amparo 20 + - + + + + + + + + + + - -
Monte Alegre do Sul 10 + - + - + - + - - + - - - -
Marilia Tupã Bastos 135 - - + - + - - + - + - - - -
Presidente Prudente Presidente Prudente Rancharia 10 - - - - - - - + - - - - - -
João Ramalho 10 - - - - - - - + - + - - - -
Regente Feijó 10 - - - - - - - + - - - - - -
Presidente Prudente 10 + - + - + - - + + - + + - -
Panorama 5 - - + + + - + + + + + + - -
Ribeirão Preto Ribeirão Preto Guatapará 50 - - + + + - + + + + + - + -
São José do Rio Preto S. J. Rio Preto Cedral 10 + - + + + - + + + + + + - -
Fernandópolis Fernandópolis 10 - - + + + - + + + - + + - -
Nhandeara Nhandeara 10 - - + + + - - - - - - + - -
Votuporanga Votuporanga 34 + + + + + - + + + + + - - -
Valentim Gentil 5 + - + - + - + + + - + + 4 - +

Table 2 Occurrence (%) of helminth species diagnosed in the regions of São Paulo State addressed in this study 

(17 municipalities/10 microregions/6 mesoregions).
HELMINTHS OCCURRENCE (%)
CLASS SPECIES MUNICIPALITIES (17*) MICRORREGIONS (10**) MESOREGIONS(6***)
NEMATODES Oxspirura mansoni 41 50 67
Acuaria hamulosa 6 10 17
Ascaridia galli 71 90 100
Capillaria sp. 59 80 83
Heterakis gallinarum 76 90 100
Strongyloidis sp. 6 10 17
CESTODES Amoebotaenia cuneata 59 70 83
Choanotaenia infundibulum 88 90 100
Hymenolepis sp. 59 70 83
Raillietina echinobothrida 53 70 83
cesticillus 65 80 100
tetragona 47 70 67
TREMATODES Zygocotyle lunata 6 10 17
Postharmostomum commutatum 6 10 17

*Municipalities: Amparo, Araçatuba, Bastos, Cedral, Fernandópolis, Guararapes, Guatapará, João Ramalho, Monte Alegre do Sul, Nhandeara, Panorama, Pereira Barreto, Presidente Prudente, Rancharia, Regente Feijó, Valentim Gentil, Votuporanga

**Microregions: Andradina, Araçatuba, Amparo, Tupã, Presidente Prudente, Ribeirão Preto, São José do Rio Preto, Fernandópolis, Nhandeara, Votuporanga

***Mesoregions: Araçatuba, Campinas, Marília, Presidente Prudente, Ribeirão Preto e São José do Rio Preto

Nematodes were found in the small intestine (Ascaridia galli, Capillaria spp., and Strongyloides sp. ), cecum (Heterakis gallinarum (Figure 1) and Capillaria sp. ), gizzard (Cheylospirura hamulosa) (Figure 1), crop (Capillaria sp.) and eye (Oxyspirura mansoni (Figure 1), which supports the results of Costa et al. (1986). 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.

Figure 1 Nematodes (Cheylospirura hamulosa, Heterakis gallinarum and Oxyspirura mansoni) present in chickens originating from state of São Paulo. 

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.

Figure 2 Cestodes (Amoebotaenia cuneata, Choanotaenia infundibulum, Raillietina echinobothrida, Raillietina cesticillus and Raillietina tetragona) present in chickens originating from state of São Paulo. 

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).

Figure 3 Trematodes (Postharmostomum commutatum and Zygocotyle lunata - stereomicroscopy) present in chickens originating from state of São Paulo. 

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.

Conclusions

The following helminth species were diagnosed in chickens reared in the regions sampled in the present study:

- nematodes: A. galli, Capillaria sp. , C. hamulosa, H. gallinarum, O. mansoni , and Strongyloides sp. ;

- cestodes: C. infundibulum, R. cesticillus, A. cuneata, Hymenolepis sp., R. echinobothrida , and R. tetragona ;

- trematodes: P. commutatum and Z. lunata .

Acknowledgements

The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the financial support (Proc. 2012/18929-3) and the technical support scholarships (Proc. 2013/03599-0 and Proc. 2014/04097-1), as well as the technicians at CATI and the researchers at APTA for their valuable contributions in contacting farmers to make birds available for sampling.

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Received: July 2015; Accepted: October 2015

Mail Address Corresponding author e-mail address Giane Serafim da Silva Caixa Postal 61 - Votuporanga - SP - Brazil - CEP 15500-970 Phone: +51(17)34222423 Ramal 207 Email:giane@biologico.sp.gov.br

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