First report of <i>Anisakis</i> sp. (Nematoda: Anisakidae) parasitizing Muscovy duck in Marajó Island, state of Pará, Brazil

Among the avian used for human consumption, the Muscovy duck is well adapted to various climatic conditions and its breeding is widespread due to its easy handling, and its meat is widely consumed and appreciated, especially in the cuisine of northern Brazil. The present study aimed to report and identify taxonomically the nematodes found in the esophagus of Muscovy ducks reared and marketed in the municipality of Soure, Marajó Island, state of Pará, Brazil, and discuss its zoonotic potential to human. The samples consisted of 30 specimens of Cairina moschata domestica analyzed. A total of 258 nematodes were recovered, which were strongly fixed in the esophageal mucosa of hosts. The morphological and morphometric characteristics were compatible with Anisakis third-stage larvae.

Keywords:
Amazon; esophagus; parasites; ducks; nematodes; Anisakis

Authorship

Elaine Lopes de Carvalho

Programa de Pós-graduação em Saúde e Produção Animal na Amazônia, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, BrasilUniversidade Federal Rural da AmazôniaBrasilBelém, PA, BrasilPrograma de Pós-graduação em Saúde e Produção Animal na Amazônia, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil

Laboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, BrasilUniversidade Federal Rural da AmazôniaBrasilBelém, PA, BrasilLaboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil

http://orcid.org/0000-0003-4177-9498

Ricardo Luis Sousa Santana

http://orcid.org/0000-0001-6219-1437

Evonnildo Costa Gonçalves

Laboratório de Tecnologia Biomolecular, Instituto de Ciências Biológicas, Universidade Federal do Pará - UFPA, Belém, PA, BrasilUniversidade Federal do ParáBrasilBelém, PA, BrasilLaboratório de Tecnologia Biomolecular, Instituto de Ciências Biológicas, Universidade Federal do Pará - UFPA, Belém, PA, Brasil

http://orcid.org/0000-0003-2221-1995

Raul Henrique da Silva Pinheiro

Programa de Pós-graduação em Sociedade, Natureza e Desenvolvimento, Instituto de Ciências e Tecnologia das Águas, Universidade Federal do Oeste do Pará – UFOPA, Santarém, PA, BrasilUniversidade Federal do Oeste do ParáBrasilSantarém, PA, BrasilPrograma de Pós-graduação em Sociedade, Natureza e Desenvolvimento, Instituto de Ciências e Tecnologia das Águas, Universidade Federal do Oeste do Pará – UFOPA, Santarém, PA, Brasil

http://orcid.org/0000-0003-3221-5017

Elane Guerreiro Giese ^**Corresponding author: Elane Guerreiro Giese. E-mail: elane.giese@ufra.edu.br

http://orcid.org/0000-0001-7833-1334

*Corresponding author: Elane Guerreiro Giese. E-mail: elane.giese@ufra.edu.br

SCIMAGO INSTITUTIONS RANKINGS

Figures

Figures (5)

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Figure 1
Collection locality of Cairina moschata domestica in municipality of Soure, Marajó Island, State of Pará, Brazil.

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Figure 2
Macroscopic observation of the esophagus of Cairina moschata domestica: (a) Presence of Anisakis sp. third-stage larvae in the early portion of the esophagus. Bar = 2 cm; (b) Esophageal opening in longitudinal section, with several Anisakis sp. third-stage larvae attached to the esophageal mucosa. Bar = 2 cm.

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Figure 3
Light microscopy of Anisakis sp. (L3 larvae) parasite of Cairina moschata domestica: (a) Lateral view of the cephalic region showing evidence a pointed tooth (pt), nerve ring (nr), esophagus (es) and ventricle (ve). Bar = 200 μm; (b) Detail of pointed tooth (pt), excretory pore (ep), nerve ring (nr) and cuticle with delicate transversal striations. Bar = 50 μm; (c) Posterior portion showing: intestine (in), rectum (r), rectal glands (*), anus (an) and the tail with mucron (mu). Bar = 50 μm.

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Figure 4
Photomicrography by scanning electron microscope of Anisakis sp. parasite of Cairina moschata domestica: (a) Dorso-lateral view of the cephalic region showing a pointed tooth (pt), deirid (de) and cuticle with delicate transversal striations. Bar = 50 μm; (b) Anterior end with three undeveloped lips (l) and four cephalic papillae, two on the dorsal lip (Arrowhead), oral opening oval (*). Bar = 20 μm; (c) Ventral view of excretory pore (ep) opening beneath the pointed tooth and cephalic papillae one on each ventro-lateral lip (Arrowhead). Bar = 20 μm. (d) Anus (an) and tail conical with mucron present (mu). Bar = 20 μm.

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Figure 5
Cycle proposal for occurrence of Anisakis sp. Cairina moschata domestica parasite on Marajó Island, state of Pará. (a) Adult nematodes reside in the stomach and intestines of aquatic mammals and eliminate non-embryonated eggs along with feces in the water; b-b1) Eggs in contact with water become embryos and develop into first-stage larva (L1), which hatch into a second-stage larva (L2) that actively swims; b2) Larvae are ingested by crustaceans (1st Intermediate Host), where they develop into third-stage larvae (L3) (infective stage); c) When fish ingested contaminated crustaceans, they become the second intermediate host (*), the L3 migrate to the muscle tissue in which they live; d) Piscivorous aquatic mammals may act as definitive hosts, starting the cycle again; d1) Humans may act as accidental hosts, being infected by eating raw or undercooked meat from infected fish; (d2) Muscovy ducks (paratenic host) are infected by ingesting the viscera of fish infected with L3, made available by fishermen when they are cleaning the fish for consumption. e) Humans may be infected by eating raw or undercooked meat from ducks accidentally infected with L3; e1) Aquatic and terrestrial mammals act as definitive hosts when they feed on these birds, which could be a hypothesis to maintain the Anisakis cycle on the island.

Figure 1 Collection locality of Cairina moschata domestica in municipality of Soure, Marajó Island, State of Pará, Brazil.

Figure 2 Macroscopic observation of the esophagus of Cairina moschata domestica: (a) Presence of Anisakis sp. third-stage larvae in the early portion of the esophagus. Bar = 2 cm; (b) Esophageal opening in longitudinal section, with several Anisakis sp. third-stage larvae attached to the esophageal mucosa. Bar = 2 cm.

Figure 3 Light microscopy of Anisakis sp. (L3 larvae) parasite of Cairina moschata domestica: (a) Lateral view of the cephalic region showing evidence a pointed tooth (pt), nerve ring (nr), esophagus (es) and ventricle (ve). Bar = 200 μm; (b) Detail of pointed tooth (pt), excretory pore (ep), nerve ring (nr) and cuticle with delicate transversal striations. Bar = 50 μm; (c) Posterior portion showing: intestine (in), rectum (r), rectal glands (*), anus (an) and the tail with mucron (mu). Bar = 50 μm.

Figure 4 Photomicrography by scanning electron microscope of Anisakis sp. parasite of Cairina moschata domestica: (a) Dorso-lateral view of the cephalic region showing a pointed tooth (pt), deirid (de) and cuticle with delicate transversal striations. Bar = 50 μm; (b) Anterior end with three undeveloped lips (l) and four cephalic papillae, two on the dorsal lip (Arrowhead), oral opening oval (*). Bar = 20 μm; (c) Ventral view of excretory pore (ep) opening beneath the pointed tooth and cephalic papillae one on each ventro-lateral lip (Arrowhead). Bar = 20 μm. (d) Anus (an) and tail conical with mucron present (mu). Bar = 20 μm.

Figure 5 Cycle proposal for occurrence of Anisakis sp. Cairina moschata domestica parasite on Marajó Island, state of Pará. (a) Adult nematodes reside in the stomach and intestines of aquatic mammals and eliminate non-embryonated eggs along with feces in the water; b-b1) Eggs in contact with water become embryos and develop into first-stage larva (L1), which hatch into a second-stage larva (L2) that actively swims; b2) Larvae are ingested by crustaceans (1st Intermediate Host), where they develop into third-stage larvae (L3) (infective stage); c) When fish ingested contaminated crustaceans, they become the second intermediate host (), the L3 migrate to the muscle tissue in which they live; d) Piscivorous aquatic mammals may act as definitive hosts, starting the cycle again; d1) Humans may act as accidental hosts, being infected by eating raw or undercooked meat from infected fish; (d2) Muscovy ducks (paratenic host) are infected by ingesting the viscera of fish infected with L3, made available by fishermen when they are cleaning the fish for consumption. e) Humans may be infected by eating raw or undercooked meat from ducks accidentally infected with L3; e1) Aquatic and terrestrial mammals act as definitive hosts when they feed on these birds, which could be a hypothesis to maintain the Anisakis* cycle on the island.

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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

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First report of <i>Anisakis</i> sp. (Nematoda: Anisakidae) parasitizing Muscovy duck in Marajó Island, state of Pará, Brazil

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[1] *Corresponding author: Elane Guerreiro Giese. E-mail: elane.giese@ufra.edu.br