Histopathology and microscopic morphology of protozoan and metazoan parasites of free ranging armadillos in Brazil

This study assessed microscopic morphology of protozoan and metazoan parasites, as well as parasite-associated histopathologic changes in five Brazilian free-ranging armadillos. Three armadillos had intra sarcolemmal cysts of Sarcocystis sp. in skeletal muscles without microscopic changes. One Dasypus novemcinctus was found parasitized with a nematode morphologically compatible with an oxyurid in the small intestine. One Dasypus sp. had neutrophilic enteritis associated with adult and larval stages of Strongyloides sp. and one D. novemcinctus had multiple embryonated eggs free in the lumen of the small intestine with mild neutrophilic enteritis. These findings represent a contribution for expanding our knowledge on parasitic diseases of armadillos.

Index term:
Histopathology; microscopic morphology; protozoan; metazoan; parasites; armadillos; Brazil; Dasypus novemcinctus; Sarcocystis sp.; Strongyloides sp.; parasitism

Authorship

Alexandre Arenales

Departamento de Clínica e Cirurgia Veterinária, Escola de Veterinária, Universidade Federal de Minas Gerais (UFMG), Campus Pampulha, Av. Pres. Antônio Carlos 6627, São Luiz, Belo Horizonte, MG 31270-901, Brazil.Universidade Federal de Minas GeraisBrazilBelo Horizonte, MG, BrazilDepartamento de Clínica e Cirurgia Veterinária, Escola de Veterinária, Universidade Federal de Minas Gerais (UFMG), Campus Pampulha, Av. Pres. Antônio Carlos 6627, São Luiz, Belo Horizonte, MG 31270-901, Brazil.

Estevam G.L. Hoppe

Departamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista “Júlio de Mesquita Filho” (Unesp), Via de Acesso Prof. Paulo Donato Castellane s/n, Vila Industrial, Jaboticabal, SP 14884-900, Brazil.Universidade Estadual PaulistaBrazilJaboticabal, SP, BrazilDepartamento de Patologia, Reprodução e Saúde Única, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista “Júlio de Mesquita Filho” (Unesp), Via de Acesso Prof. Paulo Donato Castellane s/n, Vila Industrial, Jaboticabal, SP 14884-900, Brazil.

Chris Gardiner

Veterinary Pathology Service, Joint Pathology Center, 606 Stephen Sitter Ave, Silver Spring, MD 20910, USA.Joint Pathology CenterUSASilver Spring, MD, USAVeterinary Pathology Service, Joint Pathology Center, 606 Stephen Sitter Ave, Silver Spring, MD 20910, USA.

Juliana P.S. Mol

Karin Werther

Renato L. Santos ^**Corresponding author: rsantos@vet.ufmg.br

http://orcid.org/0000-0002-4830-0470

*Corresponding author: rsantos@vet.ufmg.br

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (4)
Tables (1)

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Fig.1-3.
Armadillos with intrasarcolemmal Sarcocystis sp. cysts with two distinct morphologic appearance. (1) Dasypus novemcinctus, Animal 2. Tongue, skeletal muscle cells in transversal (mmT) and longitudinal (mmL) sections. Sarcolemma containing a Sarcocytis sp. cyst with thick and brush-like outer capsule (c) with large and low density bradyzoites (bz), and abundant matrix (mx). HE, obj.100x. (2) Dasypus sp., Animal 4. Esophagus; muscular esophageal layer (mm) with a cyst of Sarcocystis sp. (arrow); esophageal lumen (*), epithelium (e) and esophageal glands (gl). HE, obj.5x. Inset: higher magnification of a Sarcocytis sp. cyst. Notice a different morphological aspect when compared to Figure 1: thinner and smoother capsule (c), without brush appearance, smaller and higher density bradyzoites (bz) and fewer matrix (mx) amounts. HE, obj.40x. (3) Dasypus novemcinctus, Animal 5. Tongue. Epithelium (e) skeletal muscle cells in transversal (mmT) and longitudinal (mmL) sections and nerves (n); Sarcocytis sp. cyst (arrow) in the sarcolemma, with morphological features similar to Figure 2. HE, obj.5x.

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Fig.4-5.
Dasypus novemcinctus, Animal 5. Cross sections of an oxyurid nematode in the intestinal lumen, surrounded by debri and bacteria, measuring approximately 200µm in diameter, with a thick cuticle (ct), thin hypodermis (hp), lateral alae (a), platymyarian musculature (pm), characterized by large and separated muscle fibers, parallel to the cuticle; and an intestine (i) lined by columnar and uninuclear cells with prominent brush border (bb). (4) Two transversal sections of nematode surrounded by abundant cellular debris with scarce neutrophils. HE, obj.10x. (5) Transversal cut section of nematode in a different portion. HE, obj.20x.

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Fig.6-8.
Dasypus sp., Animal 3. Small intestine, adult female nematodes morphologically compatible with Strongyloides sp., measuring approximately 30µm in diameter. (6) Transversal section; intestine (i) and genital tracts (g) characterizing a female. HE, obj.40x. (7) Longitudinal section; nematode coiled (arrow) within the superficial mucosa with minimal neutrophilic (nph) inflammatory infiltrate in the lamina propria, characterizing a mild acute enteritis. HE, obj.20x. (8) Early stage eggs (arrows) on the superficial mucosa among cellular debris. HE, obj.10x.

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Fig.9.
Dasypus novemcinctus, Animal 1. Small intestine, lumen containing free embryonated eggs (arrow), which are multilobulated and contains multicellular structures, measuring approximately 20x10µm with scant neutrophils (nph) in the laminae propria. HE, obj.100x.

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Table 1.
Characterization of armadillos included in this study and microscopic changes associated with protozoan and metazoans

Fig.1-3. Armadillos with intrasarcolemmal Sarcocystis sp. cysts with two distinct morphologic appearance. (1) Dasypus novemcinctus, Animal 2. Tongue, skeletal muscle cells in transversal (mmT) and longitudinal (mmL) sections. Sarcolemma containing a Sarcocytis sp. cyst with thick and brush-like outer capsule (c) with large and low density bradyzoites (bz), and abundant matrix (mx). HE, obj.100x. (2) Dasypus sp., Animal 4. Esophagus; muscular esophageal layer (mm) with a cyst of Sarcocystis sp. (arrow); esophageal lumen (), epithelium (e) and esophageal glands (gl). HE, obj.5x. Inset: higher magnification of a Sarcocytis* sp. cyst. Notice a different morphological aspect when compared to Figure 1: thinner and smoother capsule (c), without brush appearance, smaller and higher density bradyzoites (bz) and fewer matrix (mx) amounts. HE, obj.40x. (3) Dasypus novemcinctus, Animal 5. Tongue. Epithelium (e) skeletal muscle cells in transversal (mmT) and longitudinal (mmL) sections and nerves (n); Sarcocytis sp. cyst (arrow) in the sarcolemma, with morphological features similar to Figure 2. HE, obj.5x.

Fig.4-5. Dasypus novemcinctus, Animal 5. Cross sections of an oxyurid nematode in the intestinal lumen, surrounded by debri and bacteria, measuring approximately 200µm in diameter, with a thick cuticle (ct), thin hypodermis (hp), lateral alae (a), platymyarian musculature (pm), characterized by large and separated muscle fibers, parallel to the cuticle; and an intestine (i) lined by columnar and uninuclear cells with prominent brush border (bb). (4) Two transversal sections of nematode surrounded by abundant cellular debris with scarce neutrophils. HE, obj.10x. (5) Transversal cut section of nematode in a different portion. HE, obj.20x.

Fig.6-8. Dasypus sp., Animal 3. Small intestine, adult female nematodes morphologically compatible with Strongyloides sp., measuring approximately 30µm in diameter. (6) Transversal section; intestine (i) and genital tracts (g) characterizing a female. HE, obj.40x. (7) Longitudinal section; nematode coiled (arrow) within the superficial mucosa with minimal neutrophilic (nph) inflammatory infiltrate in the lamina propria, characterizing a mild acute enteritis. HE, obj.20x. (8) Early stage eggs (arrows) on the superficial mucosa among cellular debris. HE, obj.10x.

Fig.9. Dasypus novemcinctus, Animal 1. Small intestine, lumen containing free embryonated eggs (arrow), which are multilobulated and contains multicellular structures, measuring approximately 20x10µm with scant neutrophils (nph) in the laminae propria. HE, obj.100x.

Table 1. Characterization of armadillos included in this study and microscopic changes associated with protozoan and metazoans

Animal	Host species	Sex	Age	Histopathology
1	Dasypus novemcinctus	M	Adult	Small intestine: lumenal embryonated eggs; no lesions associated
2	Dasypus novemcinctus	F	Adult	Tongue: intrasarcolemmal Sarcocystis sp. cysts (brush-like outer capsule); no lesions associated
3	Dasypus sp.*	F	Young	Small intestine: neutrophilic diffuse and mild enteritis with intralesional Strongyloides sp. (adults and larvae stages)
4	Dasypus sp.*	F	Adult	Esophagus and skeletal muscle: intrasarcolemmal Sarcocystis sp. cysts; no lesions associated
5	Dasypus novemcinctus	M	Adult	Duodenum: lumenal oxyurid nematode, tongue: intrasarcolemmal Sarcocystis sp. cysts; no lesions associated

* Species not identified; NR = not reported.

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Colégio Brasileiro de Patologia Animal - CBPA Pesquisa Veterinária Brasileira, Caixa Postal 74.591, 23890-000 Rio de Janeiro, RJ, Brasil, Tel./Fax: (55 21) 2682-1081 - Rio de Janeiro - RJ - Brazil
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Histopathology and microscopic morphology of protozoan and metazoan parasites of free ranging armadillos in Brazil

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[1] *Corresponding author: rsantos@vet.ufmg.br