Avaliação morfométrica comparativa da hemossiderose hepática em pinguins-de-Magalhães (<i>Spheniscus magellanicus</i>) de vida livre infectados por diferentes subgêneros de <i>Plasmodium</i> spp.

Ewbank, Ana Carolina; Strefezzi, Ricardo de Francisco; Sacristán, Carlos; Kolesnikovas, Cristiane Kiyomi Miyaji; Martins, Aryse; Mayorga, Luis Felipe Silva Pereira; Vanstreels, Ralph Eric Thijl; Catão-Dias, José Luiz

doi:10.1590/S1984-296120180092

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Original Article • Rev. Bras. Parasitol. Vet. 28 (1) • Jan-Mar 2019 • https://doi.org/10.1590/S1984-296120180092 copiar

Avaliação morfométrica comparativa da hemossiderose hepática em pinguins-de-Magalhães (Spheniscus magellanicus) de vida livre infectados por diferentes subgêneros de Plasmodium spp.

Autoria SCIMAGO INSTITUTIONS RANKINGS

Resumo

Malária aviária é uma das mais relevantes doenças em pinguins cativos. Foram aplicadas técnicas morfométricas para avaliar a hemossiderose hepática em pinguins-de-Magalhães (Spheniscus magellanicus ) de vida livre em reabilitação negativos (n = 9) e naturalmente infectados por diferentes subgêneros de Plasmodium spp. (n = 24), quanto a: subgênero de Plasmodium (Haemamoeba , Huffia, Outras Linhagens, e Linhagens não identificadas), severidade das lesões histopatológicas causadas por Plasmodium e doenças concomitantes, faixa etária (plumagem juvenil ou adulta), sexo (macho, fêmea, indeterminado), condição corporal (emaciado, magro, bom, excelente, indisponível), muda, presença/ausência de óleo a admissão, suplementação de ferro, e centro de reabilitação. A porcentagem da área ocupada por hemossiderina foi denominada “Índice de Hemossiderose Hepática (IHH)”. Fêmeas Plasmodium -positivas apresentaram IHH significativamente mais elevado que machos, respectivamente, 17,53 ± 12,95% e 7,20 ± 4,25% (p = 0,041). Níveis mais elevados de congestão (p = 0,0182) e pneumonia (p = 0,0250) foram observados entre Linhagens não identificadas vs. Huffia. Possivelmente, a hemossiderose hepática observada nesse estudo seja multifatorial, resultado de processos patológicos causados por malária, muda, catabolismo de hemoglobina e mioglobina durante a migração, anemia, doenças concomitantes e suplementação de ferro, potencialmente intensificados por massa hepática reduzida. Estudos complementares são necessários para esclarecer os mecanismos de tais hipóteses.

Palavras-chave:
Malária aviária; ferro; hemosiderina; fígado; morfometria; pinguim

Rehabilitation Center	Iron supplementation	Administration Criteria	Diet
Rehabilitation Center	(Dose/Route/Frequency)	Administration Criteria	(whole fish-based)
CRAM ^a a CRAM = Centro de Recuperação de Animais Marinhos (Rio Grande do Sul state, Brazil).	Ferrodex ^d d Ferrodex® (Tortuga, Companhia Zootécnica Agrária, São Amaro, São Paulo, Brazil). → 0.2mg/kg/IM – single dose (until 2013)	Hematocrit < 35%	banded croaker
		Hematocrit < 35%	(Paralonchurus brasiliensis)
	Ferrodex → 0.2mg/kg/IM – single dose (from 2013 to the present)	Hematocrit < 30% until the parameter reaches the acceptable interval for the species ^f f Reference interval for the species ( SILVA-FILHO & RUOPPOLO, 2014 ).	stripped weakfish
			(Cynoscion guatucupa)
			acoupa weakfish
			(Cynoscion acoupa)
	Ferrodex → 0.2mg/kg/IM – single dose in association with Hemolitan pet ^e e Hemolitan pet (Indústria e Comércio de Produtos Veterinários Ltda., Louveira, São Paulo, Brazil). → 0.1mg/kg PO – q24h	Hematocrit < 35%until the parameter reaches the acceptable interval for the species ^f	Argentine croaker
			(Umbrina canosai)
	(from 2013 to the present)		whitemouth croaker
	(from 2013 to the present)		(Micropogonias furnieri)
R3 Animal ^b b R3 = Associação R3 Animal (Santa Catarina state, Brazil).	Ferrodex → 1ml/IM– single dose	Upon admission	Brazilian sardine
	Ferrodex → 1ml/IM– single dose	Upon admission	(Sardinella brasiliensis)
IPRAM ^c c IPRAM = Instituto de Pesquisa e Reabilitação de Animais Marinhos (Espírito Santo state, Brazil).	Hemolitan pet → 1ml/PO – q24h	Penguins treated as huddles. Medication administered upon admission and maintained for days to weeks, until the birds exhibited normal colored oral mucosae	Brazilian sardine
	Hemolitan pet → 1ml/PO – q24h		(Sardinella brasiliensis)

Case	Study group	Plasmodium lineage	IHH (%)	Malaria severity
1	Haemamoeba	P. cathemerium	0.4	Moderate pulmonary congestion
				Moderate granulocytic pneumonia
				Moderate-severe monocytic hepatitis
2	Haemamoeba	P. cathemerium	14.8	Moderate-severe pulmonary congestion
				Moderate to severe granulocytic pneumonia
				Mixed moderate-severe splenitis
				Mild-moderate monocytic hepatitis
3	Haemamoeba	P. cathemerium	1.1	Mild-moderate acute diffuse granulocytic pneumonia
				Parasitic pneumonia compatible with Schistosoma sp.
				Diffuse necrotic splenitis
				Splenic limphocytolysis, histiocytolysis and lymphoid hypoplasia
				Parasitic granulomatous hepatitis
				Diffuse renal degeneration
				Mild cerebellar congestion
				Mild necrotic focal myocarditis
				Mild monocytic diffuse myocarditis
4	Haemamoeba	P. cathemerium	18.3	Moderate pulmonary congestion
				Moderate granulocytic pneumonia
				Moderate-severe granulocytic splenitis
				Moderate mixed hepatitis
5	Haemamoeba	P. cathemerium	4.2	Moderate-severe pulmonary congestion
				Mild granulocytic pneumonia
				Moderate-severe mixed splenitis
				Moderate-severe monocytic hepatitis
6	Haemamoeba	P. cathemerium	5.8	Moderate pulmonary congestion
				Moderate granulocytic pneumonia
				Mild-moderate granulocytic splenitis
				Mild-moderate mixed hepatitis
7	Haemamoeba	P. tejerai	10.8	Moderate-severe pulmonary congestion
				Moderate granulocytic pneumonia
				Mild-moderate granulocytic splenitis
				Moderate monocytic hepatitis
				Hepatic ductal hyperplasia
8	Haemamoeba	P. tejerai	1.5	Moderate-severe pulmonary congestion
				Moderate mixed hepatitis
				Hepatic ductal hyperplasia
9	Haemamoeba	P. tejerai	38.2	Moderate pulmonary congestion
				Moderate granulocytic pneumonia
				Mild-moderate granulocytic splenitis
				Mild-moderate granulocytic hepatitis
				Hepatic ductal hyperplasia
10	Haemamoeba	P. tejerai	31.9	Moderate-severe pulmonary congestion
				Severe granulocytic pneumonia
				Mild-moderate mixed splenitis
				Moderate monocytic hepatitis
				Hepatic ductal hyperplasia
				Mild monocytic myocarditis
11	Haemamoeba	P. tejerai	9.4	Mild-moderate pulmonary congestion
				Mild-moderate granulocytic pneumonia Mild-moderate mixed splenitis
				Mild granulocytic myocarditis
12	Huffia	P. elongatum	22.8	Moderate pulmonary congestion
				Mild granulocytic pneumonia
				Moderate monocytic hepatitis
13	Huffia	P. elongatum	1.4	Mild-moderate congestion
				Acute granulocytic diffuse myocarditis
				Moderate cerebellar congestion
				Moderate diffuse acute granulocytic pneumonia
				Moderate coalescent multifocal histiocytosis, moderate lymphoid hypoplasia, lymphocytolisis, extramedullary erythropoiesis, mild-moderate mixed diffuse necrotic splenitis
				Mixed multifocal interstitial nephritis
				Moderate-severe multifocal necrotic hepatitis
				Extramedullary hepatic erythropoiesis
				Hepatic ductal hyperplasia
14	Huffia	P. elongatum	6.9	Mild cardiac congestion
				Mild acute diffuse myocarditis
				Mild to moderate cerebellar congestion
				Moderate mixed diffuse pneumonia
				Moderate pulmonary congestion
				Spleen tissue was not available for examination
				Diffuse renal degeneration
				Moderate-severe mixed coalescent multifocal necrotic periportal hepatitis and mild extramedullary erythropoiesis
15	Other lineages	P. nucleophilum	27.6	Mild pulmonary congestion
				Mild-moderate monocytic pneumonia
				Mild-moderate monocytic splenitis
				Moderate-severe mixed hepatitis
16	Other lineages	P. unalis	15	Moderate-severe pulmonary congestion
				Moderate-severe monocytic pneumonia
				Mild monocytic hepatitis
17	Other lineages	Plasmodium sp. E	6.2	Moderate pulmonary congestion
				Moderate granulocytic pneumonia
				Moderate granulocytic splenitis
				Mild monocytic hepatitis
				Hepatic ductal hyperplasia
18	Other lineages	Plasmodium sp. G	4.8	Moderate-severe pulmonary congestion
				Moderate granulocytic pneumonia
				Moderate granulocytic splenitis
				Moderate-severe monocytic hepatitis
19	Other lineages	Plasmodium sp. G	45.4	Moderate-severe pulmonary congestion
				Severe granulocytic pneumonia
				Mild granulocytic splenitis
				Mild-moderate granulocytic hepatitis
				Severe myocardial necrosis
20	Other lineages	Plasmodium sp. H	14.6	Moderate pulmonary congestion
				Moderate mixed pneumonia
				Moderate monocytic hepatitis
21	Unidentified lineages	Plasmodium sp.	10.7	Moderate-severe pulmonary congestion
				Moderate-severe monocytic pneumonia
				Moderate granulocytic splenitis
				Moderate-severe monocytic hepatitis
				Mild-moderate monocytic myocarditis
22	Unidentified lineages	Plasmodium sp.	12.8	Moderate-severe pulmonary congestion
				Moderate-severe granulocytic pneumonia
				Moderate-severe granulocytic splenitis
				Moderate granulocytic hepatitis
				Mild granulocytic hepatitis
23	Unidentified lineages	Plasmodium sp.	8.3	Severe pulmonary congestion
				Severe monocytic pneumonia
				Mild-moderate mixed splenitis
				Moderate monocytic hepatitis
				Mild granulocytic myocarditis
24	Unidentified lineages	Plasmodium sp.	13.8	Moderate-severe pulmonary congestion
				Moderate granulocytic pneumonia
				Mild-moderate monocytic hepatitis
				Hepatic ductal hyperplasia
25	Plasmodium - negative	Negative	0.9	-
26	Plasmodium - negative	Negative	18.1	-
27	Plasmodium - negative	Negative	11.6	-
28	Plasmodium - negative	Negative	2.9	-
29	Plasmodium - negative	Negative	0.9	-
30	Plasmodium - negative	Negative	5.6	-
31	Plasmodium - negative	Negative	13.4	-
32	Plasmodium - negative	Negative	6.5	-
33	Plasmodium - negative	Negative	12.5	-

Case	IHH (%)	Rehab center ^a a IPRAM = Instituto de Pesquisa e Reabilitação de Animais Marinhos (Espírito Santo state, Brazil); R3 = Associação R3 Animal (Santa Catarina state, Brazil); CRAM = Centro de Recuperação de Animais Marinhos (Rio Grande do Sul state, Brazil);	Age class ^b b J = Juvenile; A = adult;	Sex ^c c F = female; M = male; ND = not determined;	Body mass (g)	Body score	Ht ^d d N/A = Information not available.	Oil	Moult	Fe	Concurrent disease and/or significant lesion
1	0.4	IPRAM	J	F	1915	Thin	N/A	No	No	No	Aspergillosis
2	14.8	IPRAM	J	F	2290	Thin	N/A	No	No	No	Spleen hemorrhage and rupture
3	1.1	CRAM	J	M	N/A	N/A	N/A	No	No	N/A	-
4	18.3	R3	J	F	2560	Good	44%	No	Yes	No	Helminthiasis
5	4.2	R3	J	M	N/A	Good	40%	No	Yes	No	N/A
6	5.8	R3	J	M	3240	Good	N/A	No	Yes	No	Avipoxvirus
7	10.8	R3	J	M	2400	N/A	32%	No	No	Yes	N/A
8	1.5	R3	J	ND	2600	N/A	N/A	No	No	Yes	Disseminated intravascular clotting
9	38.2	R3	J	ND	3450	N/A	N/A	No	Yes	Yes	N/A
10	31.9	R3	A	F	3300	Good	N/A	No	No	No	Helminthiasis (small intestine)
11	9.4	R3	J	M	2100	Good	N/A	No	No	N/A	N/A
12	22.8	IPRAM	J	F	2260	Good	N/A	No	No	No	Biliary stasis, Unidentified cysts (myocardium)
13	1.4	CRAM	A	F	N/A	Good	N/A	No	No	N/A	-
14	6.9	CRAM	A	M	N/A	Good	N/A	No	No	N/A	-
15	27.6	CRAM	J	F	2802	Good	50%	Yes	No	N/A	Amyloidosis, helminthiasis (gastrointestinal, lungs, liver)
16	15	CRAM	J	F	2810	Good	40%	Yes	No	N/A	Aspergillosis, Amyloidosis
17	6.2	R3	A	F	3220	Good	N/A	No	No	No	-
18	4.8	R3	J	M	3060	Good	27%	No	Yes	No	Amyloidosis, helminths (air sacs)
19	45.4	R3	J	F	2700	Bad	19%	No	Yes	No	Aspergillosis, pancarditis
20	14.6	R3	A	M	3260	Good	N/A	No	Yes	No	Helminthiasis
21	10.7	CRAM	J	ND	3890	Good	36%	No	No	Yes	-
22	12.8	CRAM	J	F	2910	N/A	33%	No	No	N/A	Spleen hemorrhage and rupture
23	8.3	CRAM	J	ND	2645	Thin	53%	Yes	No	Yes	-
24	13.8	CRAM	A	F	2750	Thin	46%	Yes	No	Yes	-
25	0.9	IPRAM	J	F	1750	Cach ectic	N/A	Yes	No	Yes	-
26	18.1	IPRAM	J	F	1865	Thin	N/A	Yes	No	Yes	-
27	11.6	IPRAM	J	F	2015	Thin	N/A	Yes	No	Yes	-
28	2.9	IPRAM	J	F	2250	Thin	N/A	Yes	No	Yes	-
29	0.9	R3	J	ND	N/A	Good	N/A	Yes	No	Yes	-
30	5.6	R3	A	ND	N/A	Good	N/A	Yes	No	Yes	-
31	13.4	CRAM	J	M	2248	N/A	N/A	Yes	No	N/A	-
32	6.5	CRAM	J	M	2268	N/A	N/A	Yes	No	N/A	-
33	12.5	CRAM	J	M	3110	N/A	N/A	Yes	No	N/A	-

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E-mail: cbpv_rbpv.fcav@unesp.br

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[1] * Corresponding author: Ana Carolina Ewbank. Laboratório de Patologia Comparada de Animais Selvagens, Departamento de Patologia, Universidade de São Paulo – USP, Av. Orlando Marques de Paiva, 87, Butantã, CEP 05508-270, São Paulo, SP, Brasil. e-mail: carolewbank@yahoo.com.br