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Trematodes of free range reared guinea

fowls (Numida meleagris Linnaeus, 1758)
in the state of Rio de Janeiro, Brazil:
Morphology and pathology
Rodrigo C. Menezes, Dalton G. Mattos Jr, Delir Corrêêa Gomes, Rogéério
Tortelly, Luíís C. Muniz-Pereira & Roberto Magalhãães Pinto

Available online: 17 Jun 2010

To cite this article: Rodrigo C. Menezes, Dalton G. Mattos Jr, Delir Corrêêa Gomes, Rogéério Tortelly, Luíís
C. Muniz-Pereira & Roberto Magalhãães Pinto (2001): Trematodes of free range reared guinea fowls (Numida
meleagris Linnaeus, 1758) in the state of Rio de Janeiro, Brazil: Morphology and pathology, Avian Pathology,
30:3, 209-214

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 Avian Pathology ( 2001 ) 30, 209– 214

Trematodes of free range reared guinea fowls

( Numida meleagris Linnaeus, 1758) in the state of
Rio de Janeiro, Brazil: morphology and pathology

Rodrigo C. Menezes1 , Dalton G. Mattos Jr.1 , Rogério Tortelly2 ,

Lu´õ s C. Muniz-Pereira3 , Roberto Magalhães Pinto3 & Delir Corrêa Gomes3 *
1
Departamento de Patologia e Cl´õ nica Veterinária and 2 Departamento de Patologia, Faculdade de
Veterinária da Universidade Federal Fluminense, Rua Vital Brazil Filho, 64, 24.230–340, Niterói, RJ,
Brasil, and 3 Departamento de Helmintologia, Laborat ório de Helmintos Parasitos de Vertebrados,
Instituto Oswaldo Cruz, Av. Brasil 4361, 21.045– 900, Rio de Janeiro, Brasil
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An investigation on the digenetic trematodes parasitizing free range reared guinea fowls was conducted
in the state of Rio de Janeiro, Brazil, based on clinical examination, necropsies and histopathologica l
findings in 36 guinea fowls. Parasites, prevalence and intensity of infection were, respectively:
Paratanaisia bragai, 61.1% and 31 ( in each kidney); Athesmia heterolecithodes, 8.3% and 38;
Conspicuum conspicuum, 2.8% and 1. A. heterolecithodes was highly pathogenic to guinea fowls,
causing severe hepatic lesions. However, C. conspicuum and P. bragai were less pathogenic in the
considered intensities of infection. This is the first time that these parasite species have been reported
in Brazilian guinea fowls.

Introduction Brazil and concerning the prevalence, intensity of

Guinea fowls ( Numida meleagris) are indigenous in
West Africa and regarded as an important economic
resource in several African communities ( Ver-
cruysse et al., 1985 ). The species was introduced in
Brazil by Portuguese settlers and, presently, these
birds are reared in all regions, but mainly in
northeastern Brazil where they provide an alter-
native income to rearers. France and Russia are the
main markets for guinea fowl meat ( Fabichak,
1997 ).
The only reported Digenea parasitizing this host
in Brazil is Typhlocoelum cucumerinum Rudolphi,
1809 ( Freitas & Costa, 1969; Costa et al., 1986 ).
The present study is related to other digeneans,
namely Athesmia heterolecithode s ( Braun, 1899)
Looss, 1899, Conspicuum conspicuum ( Faria,
1912 ) Bhalerao, 1936 and Paratanaisia bragai
( Santos, 1934) Freitas, 1959, occurring in free
reared guinea fowls in the state of Rio de Janeiro,
parasitism and pathological findings due to the
infection.
Materials and Methods
Thirty-six guinea fowls from different rearers in the state of Rio de
Janeiro, Brazil, were examined, euthanized and necropsied according
to the technique of Zander et al. ( 1997 ) and to the Brazilian Code of
Ethics for Animals ( APA, 1989 ).
The recovered trematodes were fixed ( uncompressed ) in A.F.A.
( alcohol 70°GL, 93 ml; formaldehyde, 5 ml; acetic acid, 2 ml) and
quantified under a stereoscope microscope. Counting of kidney flukes
was performed in one kidney. The other was sent for histopathologica l
examination after identification of the parasitism. The trematodes were
stained with carmine-borax according to Ueno & Gonçalves ( 1994 ),
dehydrated in alcohol ( 70 to 100°GL), clarified in beechwood creosote,
preserved in Canada balsam and deposited in the Helminthologica l
Collection of the Oswaldo Cruz Institute ( CHIOC), numbers 34193
a–b, 34194 a–d, 34332 and 34333 a– b ( whole mounts). Fragments of
parasitized organs were removed and immediately fixed in formalin.
The material was then routinely processed for parafin embedding. Five
micrometer thick sections were stained with haematoxylin and eosin
( HE). Slides 34193 b, 34194 d and 34333 b refer to histological

* To whom correspondence should be addressed. E-mail: dcgomes@gene.dbbm.fiocruz.b r

Received 21 August 2000. Accepted 12 December 2000.
ISSN 0307-9457 ( print)/ISSN 1465-3338 ( online)/01/030209-0 6 © 2001 Taylor & Francis Ltd
DOI: 10.1080/03079450120054500
 210 R. C. Menezes et al.
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Figure 1. Athesmia heterolecithodes, total. Bar = 0.4 mm. Figure 2. Conspicuum conspicuum, total. Bar = 0.4 mm.

sections. Photomicrographs were obtained in a Zeiss Axiophot system
and in an Olympus BX 50 microscope. Measurements are in
millimeters, unless otherwise indicated. Classification of the trem-
atodes to the species level is in accordance with Travassos et al.
( 1969 ).
Results
Prevalence of parasitism with trematodes was of
63.8% in the 36 examined hosts. A. heterolecithode s
( Figure 1) in the bile ducts and gallbladder, C.
conspicuum ( Figure 2) in the gallbladder and P.
bragai ( Figure 3) in the renal collecting ducts and
ureters were recovered, and parasitized birds did not
present clinical signs. Data on prevalence, mean
intensity of infection and intensity of infection range
are presented in Table 1, and those on morphometrics
are presented in Table 2.
Parasites and associated gross and microscopic
lesions are as follows. First, for A. heteroleci-
thodes, gross lesions: congested liver with irregu-
lar surface, with several dark red spots, biliary

Table 1. Prevalence, mean intensity of infection, and range of the intensity of infection of trematodes parasitizing guinea fowls in the
State of Rio de Janeiro

Mean intensity of infection Range of the

intensity of
Trematodes Prevalence ( %) Necropsied Parasitized infection

P. bragai 61.1 18.68* 31* 1–142*

A. heterolecithodes 8.3 3.14 38 2– 90
C. conspicuum 2.8 0.03 1 1

* Values obtained from trematodes collected in one of the kidneys.

 Trematodes of guinea fowls in Brazil 211

debris were found in the bile ducts ( Figure 4). A

circular granulomatous reaction associated with
the necrotic eosinophilic residues was observed in
one of the livers.
Second, for C. conspicuum, gross lesions: liver
lobes enlarged, yellowish ( Figure 5); microscopic
lesions: vacuolar hepatic degenerative process.
Finally, for P. bragai, gross lesions: none;
microscopic lesions: chronic interstitial nephritis
and dilatation of the renal collecting ducts where
the trematodes were found. Sclerosis and a discrete
inflammatory reaction with the presence of hetero-
phils were observed around the collecting ducts
( Figure 6).

Discussion
In contrast to reports in other countries ( Hodasi,
1976; Haziev & Khan, 1991), the prevalence of
trematodes in Brazilian guinea fowls was high. The
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parasites referred to herein had not been found in

Figure 3. Paratanaisia bragai, total. Bar = 0.1 mm.
stasis in the bile ducts and gallbladder ( in two
birds ); microscopic lesions: cholangitis with thick-
ening and sclerosis of the bile ducts walls, dilata-
tion of the bile ducts with epithelial destruction,
biliary stasis, bile duct proliferation and presence
of multiple foci of chronic inflammation of the
hepatic parenchyma with heterophils together with
mononuclear cells. Trematode eggs and cellular
guinea fowls in Brazil. A. heterolecithode s and C.
conspicuum were reported in a domestic avian host
for the first time, although they occur in wild birds
and mammals ( Freitas, 1962; Travassos et al., 1969;
Thatcher, 1993). P. bragai, recovered from the
urinary tract of guinea fowls, was only previously
reported in kidneys of pigeons, turkeys, chickens
and the spot-winged wood quail in Brazil, Phil-
lipines and Puerto Rico ( Travassos et al., 1969;
Arnizaut et al., 1992; Thatcher, 1993).
The high prevalence of P. bragai in guinea fowls
reported herein was similar to that observed by
Silva et al. ( 1990 ), in pigeons from the same
locality.
Most of the measurements of A. heterolecithode s
were in agreement with those of Freitas ( 1962 ),
related to specimens from mammals recovered from
gallbladder of a raccoon ( Procyon cancrivorus ) and
liver of a monkey ( Chiroptes albinasa ), although

Table 2. Morphometrics obtained from trematodes collected in guinea fowls. All measurements in millimeters

Trematode species A. heterolecithodes C. conspicuum P. bragai

Body length 6.29–9.18 5.5 1.53–2.86

Body width ( greater) 0.51– 0.95 2.1 0.24–0.71
Oral sucker 0.21– 0.39 ´ 0.22– 0.34 0.43 ´ 0.49 0.11– 0.27 ´ 0.13– 0.27
Acetabulum 0.21– 0.35 ´ 0.22– 0.35 0.714 ´ 0.756 Not observed
Pharynx 0.084–0.126 ´ 0.070–0.112 0.18 ´ 0.20 0.04–0.08 ´ 0.06– 0.10
Oesophagus ( length) 0.13–0.42 0.27 Not measured
Cirrus pouch 0.21– 0.54 ´ 0.07– 0.13 0.48 ´ 0.18 Absent
Testes Anterior, 0.23–0.63 ´ 0.20– 0.54 Right, 0.32 ´ 0.28 Right, 0.14–0.28 ´ 0.10– 0.21
Posterior, 0.23–0.61 ´ 0.21– 0.53 Left, 0.34 ´ 0.28 Left, 0.10–0.31 ´ 0.08– 0.22
Ovary 0.27– 0.41 ´ 0.22– 0.43 0.41 ´ 0.48 0.10–0.28 ´ 0.14– 0.28
Seminal receptacle 0.112–0.25 ´ 0.14– 0.29 Not measured Not measured
Eggs 0.029–0.036 ´ 0.018–0.025 0.032 ´ 0.022 0.032–0.036 ´ 0.014–0.018
Vitellaria extension ( length) 1.20–2.21 1.6 Not measured
 212 R. C. Menezes et al.

Figure 4. Liver of a guinea fowl. Transversal section showing specimens of A. heterolecithodes in the interior of a dilated bile duct
with a partial epithelial destruction. Cholangitis with thickening and sclerosis of the bile duct walls can be observed. Bar = 0.03 mm
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( HE staining).

differences were observed in the width of the body,
diameter of the oral sucker, and size of the testes
and seminal receptacle.
Morphometrics of the specimen of C. con-
spicuum studied here were in accordance to the
results of Travassos et al. ( 1969 ), except for the size
of eggs.
Also, morphometrics of specimens of P. bragai
were in accordance with Santos ( 1934 ) and Trav-
assos et al. ( 1969 ). Nevertheless, the latter study
reported the presence of an acetabulum, which
was not observed either by the former author or in
the present investigation. Moreover, there was
reference to a scaled tegument but the tegumen-
tary spines detected in our study were not
mentioned.
Hepatic lesions due to the parasitism by A.
heterolecithodes in the hosts considered here were
severe. Kazacos et al. ( 1980), Kock & Duhamel
( 1982) and Quesenberry et al. ( 1986 ) reported
hepatic infection caused by Dicrocoellidae trem-
atodes in cockatoos in the USA. Gross lesions
were different from those presently observed;
nevertheless, microscopic findings were similar,
except for the presence of multifocal hepatic
necrosis, fibrosis of the hepatic parenchyma and
the great amount of necrotic debris in the bile
ducts.
Interestingly, the observed lesion suggesting a
hepatic lipidosis was not associated with the
presence of C. conspicuum in the gallbladder, since
two host specimens free of flukes presented the

Figure 5. Liver of a guinea fowl parasitized with C. conspicuum ( arrow) . The organ is enlarged and yellowish. Bar = 0.5 cm.

Figure 6. Kidney of a guinea fowl. Transversal section showing specimens of P. bragai in the interior of very dilated renal collecting
ducts. Sclerosis and a discrete inflammatory reaction around the collecting ducts can be observed. Bar = 0.03 mm ( HE staining) .
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same lesions that, according to Rupley ( 1999 ), are
not of parasitic aetiology.
Guinea fowls harboring P. bragai, despite the
great size of the specimens, site of infection and
mean intensity of infection, did not present either
gross or severe microscopic lesions. Similar reports
were those of Santos ( 1934 ) with regard to kidneys
of pigeons and domestic chickens parasitized with
this helminth species. Conversely, we did not
observe either amorphous or crystalline material in
the collecting ducts or debris in the undilated ducts
of the cortical region.
Arnizaut et al. ( 1992 ) reported a severe outbreak
due to P. bragai in 43 out of 124 plain pigeons
maintained in captivity in Puerto Rico. The disease
induced loss of weight with an intermittent mucous
bloody diarrhoea, and enlarged and pale kidneys.
Microscopically, findings were an interstitial infil-
tration of heterophils and a few eosinophils in the
renal ducts, and several parasites in the collecting
ducts of the renal medulla. Clinical signs, gross
lesions and inflammatory cells in the renal ducts
were not associated with P. bragai in the present
investigation.
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 214 R. C. Menezes et al.
RÉSUMÉ
Trématodes des pintades élevées en plein air ( Numida meleagris
Linnaeus, 1758) dans l’état de Rio de Janeiro au Brésil:
Morphologie et Pathologie
Une enquête sur les trématodes digénétiques parasites des pintades
élevées en plein air a été conduite dans l’état de Rio de Janeiro, au
Brésil. Elle a concerné 36 pintades qui ont fait l’objet d’examens
cliniques, nécropsiques et histologiques. Les parasites, la prévalence et
l’intensité de l’infection ont été respectivement : Paratanaisia bragai,
61,1 % et 31 ( dans chaque rein) ; Athesmia heterolecithodes, 8,3% et 38
; Conspicuum conspicuu m, 2,8 % et 1. A. heterolecithodes a été très
pathogène pour les pintades entraˆõ nant des lésions hépatiques très
importantes. Cependant, C. conspicuu m et P. bragai ont été les moins
pathogènes en considérant l’intensité de l’infection. C’est la première
fois que ces espèces de parasites ont été observées chez les pintades
brésiliennes.
ZUSAMMENFASSUNG
Trematoden von extensiv aufgezogenen Perlhühnern ( Numida
meleagridis L., 1758 ) im Staat Rio de Janeiro, Brasilien:
Morphologie und Pathologie
Eine Untersuchung über die in extensiv aufgezogenen Perlhühnern
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parasitierenden digenetischen Trematoden wurde im Staat Rio de
Janeiro, Brasilien, durchgeführt und basierte auf der klinischen
Untersuchung, Sektionen und histopathologischen Befunden bei 36
Perlhühnern. Parasiten, Prävalenz und Infektionsst ärke waren, in dieser
Reihenfolge: Paratanaisia bragai, 61,1% und 31 ( in jeder Niere);
Athesmia heterolecithode s, 8,3% und 38; Conspicuum conspicuu m,
2,8% und 1. A. heterolecithode s war für Perlhühner hoch pathogen und
verursachte schwere Leberver änderungen. C. conspicuum und P.
bragai waren jedoch in den berücksichtigten Infektionsst ärken weniger
pathogen. Dies ist das erste Mal, dass über diese Parasitenspezies bei
brasilianischen Perlhühnern berichtet worden ist.
RESUMEN
Tremátodos de gallinas de Guinea cr´õ adas en extensivo ( Numida
meleagris Linnaeus, 1758) en el estado de R´õ o de Janeiro, Brasil:
morfolog´õ a y patolog´õ a
Se realizó una investigación sobre los tremátodos digenéticos que
gallinas de Guinea cr´õ adas en extensivo en el estado de R´õ o de Janeiro,
Brasil, en base al examen cl´õ nico, necropsia y hallazgos histopatológi-
cos en 36 gallinas de Guinea. Parásitos, prevalencia e intensidad de la
infecci ón fueron, respectivamente: Paratanaisia bragai, 61.1% y 31
( en cada riñón); Athesmia heterolecithode s, 8.3% y 38; Conspicuum
conspicuum , 2.8% y 1. A. heterolecithode s resultó ser altamente
patógeno para gallinas de Guinea, causándoles lesiones hepáticas
severas. C. conspicuu m y P. bragai fueron menos patogénos en las
intensidades de infección consideradas. Este es el primer reporte de
estas especies de parásitos en gallinas de Guinea brasileñas.