Gnathostomatidae nematode parasite of <i>Colomesus psittacus</i> (Osteichthyes, Tetraodontiformes) in the Ilha de Marajó, Brazilian Amazon

Pinheiro, Raul Henrique da Silva; Santana, Ricardo Luís Sousa; Melo, Francisco Tiago Vasconcelos; Santos, Jeannie Nascimento dos; Giese, Elane Guerreiro

doi:10.1590/S1984-29612017047

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Original Article • Rev. Bras. Parasitol. Vet. 26 (3) • Jul-Sep 2017 • https://doi.org/10.1590/S1984-29612017047 copy

Gnathostomatidae nematode parasite of Colomesus psittacus (Osteichthyes, Tetraodontiformes) in the Ilha de Marajó, Brazilian Amazon

Nematoide Gnathostomatidae parasito de Colomesus psittacus (Osteichthyes, Tetraodontiformes) na Ilha de Marajó, Amazônia Brasileira

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The genus Gnathostoma comprises 17 species, whose adult specimens are found in the stomach serosa of animals that consume raw fish; some species of the genus are zoonotic agents. The present study describes the presence of a nematode (Gnathostomatidae) parasitizing the digestive tract of Colomesus psittacus in the Ilha de Marajó in the eastern Brazilian Amazon. Thirty specimens of C. psittacus were collected in the municipality of Soure, Ilha de Marajó, state of Pará, Brazil, transported to the laboratory, necropsied and the helminths were collected and fixed. Of the 30 fish that were studied, 16.67% were parasitized with nematodes. The nematode larvae found encysted in the intestinal serosa have anterior region with two lips, each with a pair of papillae; a cephalic bulb armed with six rows of discontinuous spines; four cervical sacs; a claviform esophagus; cuticular striations along the body; a simple excretory pore; and a short tail ending in a mucron. These morphological structures are diagnostic characters of the genus Gnathostoma, whose adults parasitize the stomach of carnivorous mammals and, rarely, the stomach of fish. However, fish, amphibians, reptiles, and birds are intermediate hosts of the third-stage larvae (L3), and humans may act as accidental hosts.

Keywords:
Gnathostoma; parasitism; estuary; puffer fish

Character	*Third-stage larvae of Gnathostoma* spp.**
Character	Gnathostoma sp.	*G. binucleatum*	*G. turgidum*	*G. spinigerum*	*G. procyonis*	*G. lamothei*
Hosts—larvae	Colomesus psittacus	Oreochromis aureus	Lithobates zweifeli	Channa argus	Poecilia spp.	Poeciliopsis gracilis
Hosts—adults	-	Felis pardalis	Didelphis spp.	Felis tigris	Natrix rhombifera	Procyon lotor hernandezii
Type locality	Pará, Brazil	México	USA	Japan	Procyon l. lotor USA	México
Author	-	Almeyda-Artigas (1991)Almeyda-Artigas RJ. Hallazgo de Gnathostoma binucleatum n. sp. (Nematoda: Spirurida) en felinos silvestres y el papel de peces dulceacuícolas y oligohalinos como vectores de la Gnatostomiasis humana en la cuenca baja del Río Papaloapan, Oaxaca- Veracruz, México. An Inst Cienc del Mar y Limnol Univ Nac Autón Mex 1991; 18(2): 37-155.	Mosqueda-Cabrera et al. (2009)Mosqueda-Cabrera MA, Sanchez Miranda E, Calderon LC, Najera HEO. Finding advanced third-stage larvae of Gnathostoma turgidum Stossich, 1902 in Mexico from natural and experimental host and contributions to the life cycle description. Parasitol Res 2009; 104(5): 1219-1225. PMid:19130085. http://dx.doi.org/10.1007/s00436-008-1318-4. http://dx.doi.org/10.1007/s00436-008-131...	Miyazaki (1954)Miyazaki I. Studies on Gnathostoma occurring in Japan (Nematoda: Gnathostomatidae). II. Life history of Gnathostoma and morphological comparison of its larval forms. Kyushu Mem Med Sci 1954; 5(2): 123-139.	Ash (1960Ash LR. Life cycle studies on Gnathostoma procyonis Chandler, 1942, a nematode parasite of the raccoon. J Parasitol 1960; 46(5): 37., 1962Ash LR. Development of Gnathostoma procyonis Chandler, 1942, in the first and second intermediate hosts. J Parasitol 1962; 48(2): 298-305. PMid:13862797. http://dx.doi.org/10.2307/3275591. http://dx.doi.org/10.2307/3275591... )	Bertoni-Ruiz et al. (2005)Bertoni-Ruiz F, García-Prieto L, Osorio-Sarabia D, León-Règagnon V. A new species of Gnathostoma (Nematoda: Gnathostomatidae) in Procyon lotor hernandezii from Mexico. J Parasitol 2005; 91(5): 1143-1149. PMid:16419762. http://dx.doi.org/10.1645/GE-516R.1. http://dx.doi.org/10.1645/GE-516R.1...
Length (mm) ^* * Measurements in micrometers unless indicated. The parameter number of buds is given in amplitude;	12 (10-14)	4.3 (2.6-5.9)	1.67 (1.53-2)	5 (4.6-5.5)	5.2 (4.6-5.9)	4.48 (3.58-5.09)
Width	415 (333-480)	320 (310-320) ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;	140 (134.6-160.4)	366 (250-425) ^b b From Chai et al. (2015), based on measurements of 401 advanced third-stage larvae in Asian swamp eels (Monopterus albus) purchased from central Myanmar;	342 (283-382)	288.7 (236.6-318.2)
Cephalic bulb (L) ^ Abbreviations: L: length, W: width, Oe: esophagus;	313 (277-387)	120 (110-130) ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;	46.6 (36.7-65)	93 (75-115) ^b b From Chai et al. (2015), based on measurements of 401 advanced third-stage larvae in Asian swamp eels (Monopterus albus) purchased from central Myanmar;	180 ^e e From Ash (1962) based on measurements of 15 fully developed third-stage larvae collected from the muscles of Natrix rhombifera in Louisiana, USA.	84 (69.36-106.08)
Cephalic bulb (W) ^ Abbreviations: L: length, W: width, Oe: esophagus;	340 (293-386)	240 (230-250) ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;	110 (97.9-118.3)	221 (165-250) ^b b From Chai et al. (2015), based on measurements of 401 advanced third-stage larvae in Asian swamp eels (Monopterus albus) purchased from central Myanmar;	200 ^e e From Ash (1962) based on measurements of 15 fully developed third-stage larvae collected from the muscles of Natrix rhombifera in Louisiana, USA.	188 (167.28-216.24)
I row	35 (30-40)	39 (35-44)	30.8 (26-34)	44 (39-49)	32.70 (29-36)	339.33 (34-44)
II row	39 (36-42)	42 (38-47)	34 (29-38)	47 (42-54)	36.60 (32-40)	43.27 (38-47)
III row	40 (36-42)	45 (40-49)	36.7 (29-43)	50 (45-56)	41 (37-45)	44.20 (40-48)
IV row	37 (32-40)	48 (43-52)	39.6 (33-42)	52 (45-58)	45 (42-47)	47.33 (45-58)
V row	35 (30-38)	-	-	-	-	-
VI row	33 (26-38)	-	-	-	-	-
VI-I row	2	-	-	-	-	-
Rows in the body	-	271 (242-285)	188.6 (182-202)	244 (225-256) ^d d From Koga et al. (1994) based on measurements of eight advanced third-stage larvae from naturally infected eels, Fluta alba, from Thailand;	-	227 (137-258)
I Cervical sac (mm) ^* * Measurements in micrometers unless indicated. The parameter number of buds is given in amplitude;	1 (1.18-1.84)	0.7 (0.6-0.8) ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;			-	0.045-0.063
II Cervical sac (mm) ^* * Measurements in micrometers unless indicated. The parameter number of buds is given in amplitude;			0.350 (0.302-0.435)	0.574 (0.330-0.750) ^b b From Chai et al. (2015), based on measurements of 401 advanced third-stage larvae in Asian swamp eels (Monopterus albus) purchased from central Myanmar;
III Cervical sac (mm) ^* * Measurements in micrometers unless indicated. The parameter number of buds is given in amplitude;				0.43 ^c c From Jung et al. (2008) based on measurements of an advanced third-stage larva of G. spinigerum recovered from the muscle of a snakehead fish;
IV Cervical sac (mm) ^* * Measurements in micrometers unless indicated. The parameter number of buds is given in amplitude;
Deirid ^* ***** Location of deirid and excretory pore in relation to transverse rows of corporal spines;	-	14 ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;	11.7 (10-14)	14 (11-16) ^d d From Koga et al. (1994) based on measurements of eight advanced third-stage larvae from naturally infected eels, Fluta alba, from Thailand;	13.5 (11-16)	11.73 (10-14)
Excretory pore ^* ***** Location of deirid and excretory pore in relation to transverse rows of corporal spines;	-	30 ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;	19.7 (15-22)	25 (22-28) ^d d From Koga et al. (1994) based on measurements of eight advanced third-stage larvae from naturally infected eels, Fluta alba, from Thailand;	24.3 (19-27)	23.07 (20-29)
Nerve ring	260 (167-337)	-	-	-	-	-
Muscular oe. (L) ^ Abbreviations: L: length, W: width, Oe: esophagus;	313 (277-387)	1.22 (1.22-1.23) ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;	648 (579.4-722.2)	1,025 (0.630-1,220) ^b b From Chai et al. (2015), based on measurements of 401 advanced third-stage larvae in Asian swamp eels (Monopterus albus) purchased from central Myanmar; /800^c	1,200 (1,000-1,400)	970.8 (889.4-1,162.8)
Muscular oe. (W) ^ Abbreviations: L: length, W: width, Oe: esophagus;	340 (293-386)	200 (190-210) ^a a From García-Márquez et al. (2009), based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;	80.8 (69.4-85.7)	-	124 (109-142)	117 (97.9-134.6)
Tail	175 (100-216)	-	29.2 (24.4-40.8)	-	70 ^e e From Ash (1962) based on measurements of 15 fully developed third-stage larvae collected from the muscles of Natrix rhombifera in Louisiana, USA.	59.16 (36.72-75.44)
Reference	From this study	Almeyda-Artigas (1991)Almeyda-Artigas RJ. Hallazgo de Gnathostoma binucleatum n. sp. (Nematoda: Spirurida) en felinos silvestres y el papel de peces dulceacuícolas y oligohalinos como vectores de la Gnatostomiasis humana en la cuenca baja del Río Papaloapan, Oaxaca- Veracruz, México. An Inst Cienc del Mar y Limnol Univ Nac Autón Mex 1991; 18(2): 37-155.	Stossich (1902)Stossich M. Sopra alcuni nematodi della collezione elmintogica del Prof. Dott. Corrado Parona. Boll Mus Zool Anat Comp Genova 1902; 116: 1-16.	Miyazaki (1954)Miyazaki I. Studies on Gnathostoma occurring in Japan (Nematoda: Gnathostomatidae). II. Life history of Gnathostoma and morphological comparison of its larval forms. Kyushu Mem Med Sci 1954; 5(2): 123-139.	Chandler (1942)Chandler AC. The helminths of raccoons in east Texas. J Parasitol 1942; 28(4): 255-268. http://dx.doi.org/10.2307/3272963. http://dx.doi.org/10.2307/3272963...	Gaspar-Navarro et al. (2013)Gaspar-Navarro J, Almeyda-Artigas RJ, Sánchez-Miranda E, Carranza-Calderón L, Mosqueda-Cabrera MÁ. Description of advanced third-stage larvae of Gnathostoma lamothei Bertoni-Ruiz et al. 2005 (Nematoda: Gnathostomatidae) from experimental hosts and contributions to its life cycle. Parasitol Res 2013; 112(1): 169-175. PMid:23007726. http://dx.doi.org/10.1007/s00436-012-3122-4. http://dx.doi.org/10.1007/s00436-012-312...

^*
Measurements in micrometers unless indicated. The parameter number of buds is given in amplitude;
^**
Abbreviations: L: length, W: width, Oe: esophagus;
^***
Location of deirid and excretory pore in relation to transverse rows of corporal spines;
^a
From García-Márquez et al. (2009)García-Márquez LJ, Lamothe-Argumedo R, Osorio-Sarabia D, García-Prieto L, León-Regagnon V. Morphological and molecular identification of Gnathostoma binucleatum (Nematoda: Gnathostomatidae) advanced third stage larvae (AdvL3) in the state of Colima, Mexico. Rev Mex Biodivers 2009; 80(3): 867-870., based on measurements of three AdvL3 of Gnathostoma found in the skeletal muscle of one specimen of Dormitator latifrons and five found in one specimen of Sciades guatemalensis; both fish specimens were from the Cuyutlán Lagoon;
^b
From Chai et al. (2015)Chai JY, Sohn WM, Na BK, Park JB, Jeoung HG, Hoang EH, et al. Larval Gnathostoma spinigerum detected in Asian swamp eels, Monopterus albus, purchased from a local market in Yangon, Myanmar. Korean J Parasitol 2015; 53(5): 619-625. PMid:26537042. http://dx.doi.org/10.3347/kjp.2015.53.5.619.
http://dx.doi.org/10.3347/kjp.2015.53.5.... , based on measurements of 401 advanced third-stage larvae in Asian swamp eels (Monopterus albus) purchased from central Myanmar;
^c
From Jung et al. (2008)Jung BK, Lee JJ, Pyo KH, Kim HJ, Jeong HG, Yoon CH, et al. Detection of Gnathostoma spinigerum third-stage larvae in snakeheads purchased from a central part of Myanmar. Korean J Parasitol 2008; 46(4): 285-288. PMid:19127338. http://dx.doi.org/10.3347/kjp.2008.46.4.285.
http://dx.doi.org/10.3347/kjp.2008.46.4.... based on measurements of an advanced third-stage larva of G. spinigerum recovered from the muscle of a snakehead fish;
^d
From Koga et al. (1994)Koga M, Akahane H, Ishii Y, Kojima S. External morphology of the advanced third-stage larvae of Gnathostoma spinigerum: A scanning electron microscopy. Kisechugaku Zasshi 1994; 43: 23-29. based on measurements of eight advanced third-stage larvae from naturally infected eels, Fluta alba, from Thailand;
^e
From Ash (1962)Ash LR. Development of Gnathostoma procyonis Chandler, 1942, in the first and second intermediate hosts. J Parasitol 1962; 48(2): 298-305. PMid:13862797. http://dx.doi.org/10.2307/3275591.
http://dx.doi.org/10.2307/3275591... based on measurements of 15 fully developed third-stage larvae collected from the muscles of Natrix rhombifera in Louisiana, USA.

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[1] *Corresponding author: Elane Guerreiro Giese. Laboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Av. Perimetral, 2501, Terra Firme, CEP 66077-830, Belém, PA, Brasil. e-mail: elane.giese@ufra.edu.br