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Helminthic Parasites of Chickens (Gallus Domesticus) in Different Regions of São Paulo State, 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, 2014União Brasileira de Avicultura. Relatório anual 2014. 2014. 55p. [cited 2015 Apr 24]. Available from: http://www.ubabef.com.br.
http://www.ubabef.com.br...
). According to the Brazilian Institute of Geography and Statistics (IBGE in Portuguese; Brasil, 2011IBGE - Instituto Brasileiro de Geografia e Estatística. Produção da pecuária municipal [cited 2015 abr 20]. 2011. v.39. Available from: http://www.ibge.gov.br/home/estatistica/economia/ppm/2011/default_pdf.shtm.
http://www.ibge.gov.br/home/estatistica/...
), 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., 2010Madeira LA, Sartori JR, Araujo PC, Pizzolante CC, Saldanha, ESPB., Pezzato AC. Avaliação do desempenho e do rendimento de carcaça de quatro linhagens de frangos de corte em dois sistemas de criação. Revista Brasileira de Zootecnia 2010;39(10):2214-2221.) as a result of consumers' demand. These production systems are regulated in Brazil by the Ministry of Agriculture and Food Supply (Brasil, 1999Brasil. Ministério da Agricultura e do Abastecimento. Ofício Circular DOI/DIPOA Nº007/99, de 19 de maio de 1999. Brasília, DF; 1999.).

Helminths, when present, affect poultry performance, causing significant direct or indirect losses (Reid& McDougald, 1997Reid WM, Mcdougald LR. Internal parasites. Cestodes and trematodes. In: Calnek BW, et al. Diseases of poultry. 10th ed. Ames: Iowa State University Press; 1997. p.850-864.; Silva, 2009Silva GS, Zoche AT. Endoparasitoses em aves de produção industrial In: Berchieri Júnior A, et al. ed. Doença das aves. 2ª ed. Campinas: FACTA; 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, 1997Ruff MD, Nortton RA. Internal parasites. Nematodes and acanthocephalans. In: Calnek BW, et al. Diseases of poultry. 10th ed. Ames: Iowa State University Press; 1997. p.815-850.). 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, 1997Reid WM, Mcdougald LR. Internal parasites. Cestodes and trematodes. In: Calnek BW, et al. Diseases of poultry. 10th ed. Ames: Iowa State University Press; 1997. p.850-864.).

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, 1997Reid WM, Mcdougald LR. Internal parasites. Cestodes and trematodes. In: Calnek BW, et al. Diseases of poultry. 10th ed. Ames: Iowa State University Press; 1997. p.850-864.).

Extensive studies on helminth parasites of poultry have been conducted, and new species have been described (Kolluri et al., 1985Kolluri SR, Lakshmi CV, Rao KH. Studies on cestodes of birds, with description of a new species of Raillietina (Raillietina). Revista Iberica de Parasitologia 1985;45(3):195-201.; Permin et al., 1999Permin A, Bisgaard M, Frandsen F, Pearman M, Kold J., Nansen, P. Prevalence of gastrointestinal helminths in different poultry production systems. British Poultry Science 1999;40(4):439-443.; Malhotra & Capoor, 1984Malhotra SK, Capoor, VN. A new cestode Raillietina (Skrjabinia) doggaddaensis n. sp. from Gallus gallus domesticus (L) from India. Korean Journal of Parasitology 1984;22(1):96-98.; Dixit & Capoor, 1990Dixit GR, Capoor VN. Studies on cestodes from a sub-humid region: a new dilepid from Coraciformes birds. Indian Journal of Parasitology 1990;14(2):179-182.). International studies examining poultry under different management conditions (Maqbool et al. (1998)Maqboo lA, Ahmad M, Raza A. Prevalence of helminth parasites of poultry under different management conditions. Journal of the Faculty of Veterinary Medicine,1998;53(1-2):102-103. in Pakistan; Permin et al. (1999)Permin A, Bisgaard M, Frandsen F, Pearman M, Kold J., Nansen, P. Prevalence of gastrointestinal helminths in different poultry production systems. British Poultry Science 1999;40(4):439-443. in Denmark; Hernández et al.(2002Hernández M, LarramendyR, Szczypel B. Incidencia de parásitos en aves de producción alternativa y recomendaciones para su control. Revista Cubana de Ciencia Avícola 2002;26:141-44.) in Cuba; Komba (2013Komba EVG, Mkupasi EM, Mwesiga GK, Mbyuzi AO, Busagwe Z, Mzula A, Lupindu AM, Nzalawahe J. Occurrence of helminths and coccidia in apparently healthy free range local chickens slaughtered at Morogoro live bird market. Tanzania Veterinary Journal 2013;28(2):55-61.) in Tanzania; Adang et al. (2014Adang KL, Asher R, Abba R. Gastro-intestinal helminths of domestic chickens Gallus gallus domestica and ducks Anas platyrhynchos slaughtered at Gombe mai market, Gombe State, Nigeria. Asian Journal of Poultry Science 2014;8(2):32-40.) in Nigeria; Alam et al.(2014Alam MN, Mostofa M, Khan MAHNA, Alim MA, Rahman AKMA Trisha AA. Prevalence of gastrointestinal helminth infections in indigenous chickens of selected areas of Barisal district, Bangladesh. Bangladesh Journal of Veterinary Medicine 2014;12(2):135-139.) in Bangladesh and Butt et al. (2014Butt Z, Shaikh AA, Memon SA, Mal B. Prevalence of Cestode parasites in the intestine of local chicken (Gallus Domesticus) from Hyderabad, Sindh, Pakistan. Journal of Entomology and Zoology Studies 2014;2(6):301-303.) 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. (1986Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.) 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., 2004D´Ávila S. Dias RJP, Bessa ECA, Rodrigues MLA. Exame parasitológico de fezes para o diagnóstico de helmintoses de galinhas (Gallus gallus Linnaeus, 1758) criadas em sistema semi-extensivo: avaliação das técnicas de sedimentação e de flutuação simples. Revista Brasileira de Parasitologia Veterinária 2004;13(Suppl):263. and Gomes et al., 2009Gomes FF, Machado HHS, Lemos LS, Almeida LG, Daher RF. Principais parasitos intestinais diagnosticados em galinhas domésticas criadas em regime extensivo na municipalidade de Campos dos Goytacazes, RJ. Ciência Animal Brasileira 2009;10(3):818-822.). In Northern Paraná State, Brazil, Vieira (2010Vieira FEG. Helmintofauna em frangos (Gallus gallus domesticus LINNAEUS, 1758) criados em sistema colonial/caipira na região norte do Estado do Paraná [mestrado]. 2010. Londrina (PR): Universidade Estadual de Londrina; 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. (1999Silva GS, Costa AJ, Soares VE, Meireles MV, Paulillo AC. Atividade anti-helmíntica do albendazole e do praziquantel em aves (Gallus gallus domesticus) naturalmente infectadas. ARS Veterinária 1999;15(Suppl):18-22.) 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, 2011IBGE - Instituto Brasileiro de Geografia e Estatística. Produção da pecuária municipal [cited 2015 abr 20]. 2011. v.39. Available from: http://www.ibge.gov.br/home/estatistica/economia/ppm/2011/default_pdf.shtm.
http://www.ibge.gov.br/home/estatistica/...
). 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, 2001Vich Topic GL21. Efficacy of anthelmintics: Specific recommendations for poultry. London: The European agency for the evaluation of medicinal products; 2001. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/10/WC500004587.pdf
http://www.ema.europa.eu/docs/en_GB/docu...
; Yazwinsk et al. , 2003Yazwinski TA, Chapman HD, Davis RB, Letonja T, Pote L, Maes L, et al. World Association for the Advancement of Veterinary Parasitology (WAAVP) guidelines for evaluating the effectiveness of anthelmintics in chickens and turkeys. Veterinary Parasitology 2003;116:159-73.).

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, 1974Mello EBF, Campos MS. Nova técnica de coleta de helmintos parasitos intestinais. Arquivo do Instituto Biológico de São Paulo 1974;41:201-206.), 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, 1970Schmidt GD. How to know the tapeworms. St Louis: WM. C. Brown Comp. Publishers; 1970.; Reid & McDougald, 1987Reid WM, Mcdougald LR. Internal parasites. Cestodes and trematodes. In: Calnek BW, et al. Diseases of poultry. 10th ed. Ames: Iowa State University Press; 1997. p.850-864. and Ruff & Norton, 1987Ruff MD, Nortton RA. Internal parasites. Nematodes and acanthocephalans. In: Calnek BW, et al. Diseases of poultry. 10th ed. Ames: Iowa State University Press; 1997. p.815-850.).

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).

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

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. (1986Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.). Ascaridia galli and Heterakis gallinarum were the most frequently observed nematodes. Similar results were observed in São Paulo (Costa et al. , 1986Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.) and in a study performed in Rio de Janeiro (Gomes et al., 2009Gomes FF, Machado HHS, Lemos LS, Almeida LG, Daher RF. Principais parasitos intestinais diagnosticados em galinhas domésticas criadas em regime extensivo na municipalidade de Campos dos Goytacazes, RJ. Ciência Animal Brasileira 2009;10(3):818-822.), 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. (1986Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.), 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. (1986Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.). The results showed the absence of parasitism by Davainea proglottina, one of the species considered most pathogenic for young chickens (Reid & McDougald, 1997Reid WM, Mcdougald LR. Internal parasites. Cestodes and trematodes. In: Calnek BW, et al. Diseases of poultry. 10th ed. Ames: Iowa State University Press; 1997. p.850-864.); its occurrence was previously reported in São Paulo state (Costa et al. , 1986Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.). 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. (1986Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.).

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)Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579. 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.

References

  • Adang KL, Asher R, Abba R. Gastro-intestinal helminths of domestic chickens Gallus gallus domestica and ducks Anas platyrhynchos slaughtered at Gombe mai market, Gombe State, Nigeria. Asian Journal of Poultry Science 2014;8(2):32-40.
  • Alam MN, Mostofa M, Khan MAHNA, Alim MA, Rahman AKMA Trisha AA. Prevalence of gastrointestinal helminth infections in indigenous chickens of selected areas of Barisal district, Bangladesh. Bangladesh Journal of Veterinary Medicine 2014;12(2):135-139.
  • IBGE - Instituto Brasileiro de Geografia e Estatística. Produção da pecuária municipal [cited 2015 abr 20]. 2011. v.39. Available from: http://www.ibge.gov.br/home/estatistica/economia/ppm/2011/default_pdf.shtm
    » http://www.ibge.gov.br/home/estatistica/economia/ppm/2011/default_pdf.shtm
  • Brasil. Ministério da Agricultura e do Abastecimento. Ofício Circular DOI/DIPOA Nº007/99, de 19 de maio de 1999. Brasília, DF; 1999.
  • Butt Z, Shaikh AA, Memon SA, Mal B. Prevalence of Cestode parasites in the intestine of local chicken (Gallus Domesticus) from Hyderabad, Sindh, Pakistan. Journal of Entomology and Zoology Studies 2014;2(6):301-303.
  • Costa HMA, Leite ACR, Guimarães MP, Lima AS. Distribuição de helmintos parasitos de animais domésticos no Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 1986;38(4):465-579.
  • D´Ávila S. Dias RJP, Bessa ECA, Rodrigues MLA. Exame parasitológico de fezes para o diagnóstico de helmintoses de galinhas (Gallus gallus Linnaeus, 1758) criadas em sistema semi-extensivo: avaliação das técnicas de sedimentação e de flutuação simples. Revista Brasileira de Parasitologia Veterinária 2004;13(Suppl):263.
  • Dixit GR, Capoor VN. Studies on cestodes from a sub-humid region: a new dilepid from Coraciformes birds. Indian Journal of Parasitology 1990;14(2):179-182.
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  • Kolluri SR, Lakshmi CV, Rao KH. Studies on cestodes of birds, with description of a new species of Raillietina (Raillietina). Revista Iberica de Parasitologia 1985;45(3):195-201.
  • Komba EVG, Mkupasi EM, Mwesiga GK, Mbyuzi AO, Busagwe Z, Mzula A, Lupindu AM, Nzalawahe J. Occurrence of helminths and coccidia in apparently healthy free range local chickens slaughtered at Morogoro live bird market. Tanzania Veterinary Journal 2013;28(2):55-61.
  • Madeira LA, Sartori JR, Araujo PC, Pizzolante CC, Saldanha, ESPB., Pezzato AC. Avaliação do desempenho e do rendimento de carcaça de quatro linhagens de frangos de corte em dois sistemas de criação. Revista Brasileira de Zootecnia 2010;39(10):2214-2221.
  • Maqboo lA, Ahmad M, Raza A. Prevalence of helminth parasites of poultry under different management conditions. Journal of the Faculty of Veterinary Medicine,1998;53(1-2):102-103.
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    » http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/10/WC500004587.pdf
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Publication Dates

  • Publication in this collection
    Jan-Mar 2016

History

  • Received
    July 2015
  • Accepted
    Oct 2015
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