Diagnostic criteria for Haemoproteus

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Diagnostic criteria

The diagnosis of Haemoproteus includes examination of stained blood smears to observed large, pigmented gametocytes in mature RBC which is characteristic to the parasite. The pigment may partially and sometime completely encircles the nucleus of the infected vertebrate host without displacing the nucleus. No merozoites are seen in the peripheral blood blood of the infected vertebrate host. The halter-shped gametocytes are present within erythrocytes slight displacement of nucleus of the infected host. In Haemoproteus infection, Schizonts are not present on peripheral blood smears of the infected host but multiple pigment granules which are refer to as hemozoin are present within the erythrocytes. There is presence of retractile yellow to brown color pigment granules.

Species identification is based only on the morphology of the gametocytes and their host cells (Atkinson, 1991). Drop of fresh blood from birds, for smear formation well demonstrates the presence of parasite in the blood (Merino et al., 1997). Accurate diagnosis

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depends on the experience of the microscopist (Morgan, 2000) . Early blood smears were used as a detection tool for blood parasites, may not detect parasites if their intensity is low (ValkiÅ«nas et al., 2008). PCR based detections are useful tools in determining the parasites and their lineages. Use of the genetic methods and sensitive polymerase chain reactions are very helpful in determining parasitemia (Parker PG, 2006). DNA extraction and the PCR are more sensitive techniques. The high degree of sensitivity is required in diagnosing those infections in which parasitemia is low. Diluted genomic DNA used as template in the Polymerase Chain Reaction assay for detecting Haemoproteus using a Nested PCR protocol (Waldenström et al., 2004). This methodology is most widely used for avian Haemosporidians. It accurately estimates the molecular diversity of specified gene and shows consistent results between morphological and molecular analysis. Following the standard procedures, positive amplicons are sequenced (Bensch et al., 2000).

Pathology

The pathogenicity of this parasite can vary depending upon the species of the parasite from altered physiology up to mortality (Donovan, 2008; Garvin et al., 2003; Marzal et al., 2005)

The livers and spleens from ten of the penguins exhibited varying degrees of multifocal, randomly scattered areas of necrosis and varying numbers of parasites were associated with these areas. Hepatomegaly and splenomegaly were noted in many of these ten cases. Necrosis and parasites were also observed in the cardiac muscle of four of the cases and in the lung tissue in one of the penguins (Cannell et al.; Donovan, 2008).

Infections with most Haemoproteus species appear to produce subclinical infections.

Post-mortem findings include enlargement of the spleen, liver and kidneys. These organs may appear chocolate-brown due to hemozoin deposition (Aiello, 2013). Cytologic imprints may reveal schizont-laden endothelial cells. Some species of Haemoproteus will also form large, cyst-like bodies within the skeletal muscles that resembling those seen with Sarcocystis species infections. Pigeons infected with Haemoproteus columbae may develop enlarged gizzards. Flocks of bobwhite quail (Colinus virginianus) may become infected with Haemoproteus lophortyx. Infected birds may suffer from reluctance to move, ruffled appearance, prostration and death. Other findings include parasitemia and anemia. Large megaloschizonts may be present in skeletal muscles, particularly those of the thighs and back. The average cumulative mortality for flocks experiencing outbreaks may be over 20% (Atkinson, 1961).

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Experimental infection of turkeys with Haemoproteus meleagridis resulted in lameness, diarrhea, depression, emaciation, anorexia and occasionally anemia (Griffiths, 1978). Muscovey ducks infected with Haemoproteus nettionis suffered lameness, dyspnea and sudden death. In other avian species, anemia and anorexia have been reported occasionally. Importantly, new records of Haemoproteus are discovered constantly and should still be monitored for effects on host condition (Clark et al., 2014a)

Host record (Avian hosts)

Haemoproteus sp

Avian Host

Scientific name of avian Host

H. anthi

Yellow wagtails

Motacilla flava

H. antigonis

Florida sandhill crane

Grus canadensis pratensis

H. balearicae

Black crowned crane

Balearica pavonina gibbericeps

H. balearicae

Florida sandhill crane

Grus canadensis pratensis

H. bambusicolae

Bamboo partridge

Bambusicola thoracica sonorivox

H. beckeri

Gray catbird

Dumetella carolinensis

H. belopolskyi (Parahaemoproteus)

Blackcaps

Sylvia atricapilla

H. bennetti

Greater yellownape

Picus flavinucha

H. borgesi

Red cockaded woodpecker

Picoides borealis

H. brachiatus

Saker falcon

Falco cherrug

H. bucerotis

Red billed hornbill

Tockus erythrorhynchus

H. canachites (Parahaemoproteus)

Ruffed Grouse

Bonasa umbellus

H. cathartic (Parahaemoproteus)

Turkey vulture

Cathartes aura

H. coatneyi (Parahaemoproteus)

Bananaquit

Coereba flaveola

H. coatneyi (Parahaemoproteus)

White-crowned sparrows

Zonotrichia leucophrys

H. columbae

Japanese black wood pigeons

Columba janthina

H. columbae

pigeon

Columba livia

H. columbae

Doves

Columbina talpacoti

H. columbae

Laughing dove

Stigmatopelia senegalensis

H. columbae

Eastern white-winged doves

Zenaida asiatica asiatica

H. columbae

Mourning doves

Zenaida macroura

H. cornuata

Coppersmith barbet

Megalaima haemacephala

H. crumenium

Wood stork

Mycteria americana

H. cyanomitrae (Parahaemoproteus)

Olive sunbird

Cyanomitra olivacea

H. danilewskyi (Parahaemoproteus)

Blue jays

Cyanocitta cristata

H. desseri (Parahaemoproteus)

Blossom headed parakeet

Psittacula roseata

H. dicruri

Fork tailed drongo

Dicrurus adsimilis

H. dicruri

Crested drongos

Dicrurus forficatus

H. elani

Cooper's hawk

Accipiter cooperii

H. elani

sharp shinned hawk

Accipiter striatus

H. enucleator

Kingfisher

Ispidina picta

H. (Parahaemoproteus) fringillae

Rufous-winged

Aimophila carpalis

H. (Parahaemoproteus) fringillae

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House finch

Carpodacus mexicanus

H. (Parahaemoproteus) fringillae

Hawfinch

Coccothraustes coccothraustes

H. (Parahaemoproteus) fringillae

Oriental magpie robin

Copsychus saularis

H. forresteri

Rufous-headed ground-roller

Atelornis crossleyi

H. fringillae (Parahaemoproteus)

Dark-eyed juncos

Junco hyemalis

H. fringillae (Parahaemoproteus)

American redstarts

Setophaga ruticilla

H. gabaldoni

Muscovy duck

Cairina moschata

H. garnhami (Parahaemoproteus)

Sparrows

Passer domesticus

Haemoproteus sp

Avian Host

Scientific name of avian Host

H. goodmani

Pitta-like ground-roller

Atelornis pittoides

H. greineri

Wood ducks

Aix sponsa

H. greineri

Common mergansers

Mergus merganser

H. handai

Lesser sulphur-crested cockatoo

Cacatua sulphurea

H. handai

Plum-headed parakeet

Psittacula cyanocephala

H. handai

Ring necked parakeet

Psittacula krameri manillensis

H. himalayanus

Rufous sibia

Heterophasia capistrata

H. ilanpapernai

Spotted wood owl

Strix seloputo

H. iwa

Brown Hawk-Owl

Ninox scutulata

H. iwa

Great frigatebirds

Fregata minor

H. janovyi

Whitebacked vulture

Gyps africanus

H. janovyi

Hooded vulture

Necrosyrtes monachus

H. janovyi

White-headed vulture

Trigonoceps occipitalis

H. janovyi

lappet faced vulture

Torgos tracheliotus

H. khani

Crested drongos

Dicrurus forficatus

H. lanii (Parahaemoproteus)

Red backed shrike

Lanius collurio

H. lanii (Parahaemoproteus)

woodchat shrike

Lanius senator

H. lari

Caspian gulls

Larus cachinnans

H. lophortyx (Parahaemoproteus)

California quail

Callipepla californica

H. lophortyx (Parahaemoproteus)

Scaled quail

Callipepla squamata

H. lophortyx (Parahaemoproteus)

Bobwhite quail

Colinus virginianus

H. maccallumi

Mourning doves

Zenaida macroura

H. madagascariensis

hook billed vanga

Vanga curvirostris

H. majoris

Swainson's thrush

Catharus ustulatus

H. majoris

Blue tits

Cyanistes caeruleus

H. mansoni

Blue grouse

Dendragapus obscurus

H. mansoni

ptarmigan

Lagopus lagopus

H. meleagridis

Turkey

Meleagris gallopavo

H. multipigmentatus

Galapagos dove

Zenaida galapagoensis

H. motacillae

Yellow wagtails

Motacilla flava

H. nettionis (Parahaemoproteus)

Wood ducks

Aix sponsa

H. nettionis (Parahaemoproteus)

Blue-winged teals

Anas discors

H. nettionis (Parahaemoproteus)

Pekin duck

Anas platyrhynchos

H. nettionis (Parahaemoproteus)

Lesser scaups

Aythya affinis

H. nettionis (Parahaemoproteus)

Ring-necked ducks

Aythya collaris

H. nettionis (Parahaemoproteus)

Muscovey duck

Cairina moschata

H. nettionis (Parahaemoproteus)

Trumpeter swans

Cygnus buccinator

H. nisi

Cooper's hawk

Accipiter cooperii

H. nisi

Sharp shinned hawk

Accipiter striatus

H. noctuae

Snowy owls

Nyctea scandiaca

H. noctuae

spotted owl

Strix occidentalis

H. orioli

Golden oriole

Oriolus oriolus

H. oryzivorae

Oriental magpie robin

Copsychus saularis

H. oryzivorae

Indian silverbill

Lonchura malabarica

Haemoproteus sp

Avian Host

Scientific name of avian Host

H. oryzivorae

Tricoloured munia

Lonchura malacca ruboniger

H. oryzivorae

Scaly-breasted munia

Lonchura punctulata

H. oryzivorae

Baya weaver

Ploceus philippinus

H. oryzivorae

Jungle babbler

Turdoides striata

H. palumbus

Pigeon

Columba palumbus palumbus

H. pallidulus

Blackcap

Sylvia atricapilla

H. parabelopolskyi

Blackcap

Sylvia atricapilla

H. passeris

Israeli house sparrow

Passer domesticus biblicus

H. pasteris

pied myna

Sturnus contra

H. pastoris

Grey headed myna

Sturnus malabaricus

H. pastoris

Greater blue eared glossy starling

Lamprotornis chalybaeus

H. pastoris

Pied myna

Sturnus contra

H. payevskyi

Great reed warbler

Acrocephalus arundinaceus

H. payevskyi

marsh warbler

Acrocephalus palustris

H. piresi

Pigeon

Columba livia

H. plataleae

Glossy ibis

Plegadis falcinellus

H. pratosi

Ahanta francolin

Francolinus ahantensis

H. pratasi

Helmeted guineafowl

Numida meleagris

H. prognei

purple martin

Progne subis

H. psittaci

African grey parrot

Psittacus erithacus

H. raymundi

Eastern olive sunbird

Nectarinia olivacea

H. sacharovi

Eastern white-winged doves

Zenaida asiatica asiatica

H. sacharovi

Mourning doves

Zenaida macroura

H. sangunis

Red whiskered bulbul

Pycnonotus jocosus emeria

H. sanîosdiasï (Parahaemoproteus)

Chicken

Gallus gallus

H. silvaï

Guinea fowl

Numida meleagris mitrata

H. sylvae

Great reed warbler

Acrocephalus arundinaceus

H. syrnii

Tawny owl

Strix aluco

H. syrnii

spotted owl

Strix occidentalis

H. syrnii

European scops owl

Otus scops

H. telfordi

MacQueen's bustards

Chlamydotis macqueenii

H. telfordi

Rufous-crested bustards

Eupodotis ruficrista

H. telfordi

Great bustard

Otis tarda

H. tendeiroi

MacQueen's bustards

Chlamydotis macqueenii

H. tendeiroi

Rufous-crested bustards

Eupodotis ruficrista

H. tendeiroi

Great bustard

Otis tarda

H. tinnunculi

American kestrel

Falco sparverius

H. tinnunculi

Chimango caracara

Milvago chimango

H. turtur

Turtle dove

Streptopelia turtur

Haemoproteus sp

Avian Host

Scientific name of avian Host

H. vacuolatus (Parahaemoproteus)

Yellow whiskered greenbul

Andropadus latirostris

H. vangii

Hook billed vanga

Vanga curvirostris

H. velans (Parahaemoproteus)

Red-bellied woodpecker

Melanerpes carolinus

H. velans (Parahaemoproteus)

Red-cockaded woodpecker

Picoides borealis

H. zosteropsis

Oriental white eye

Zosterops palpebrosa palpebrosa

SOURCE; (Allendorf and Lundquist, 2003; Deviche et al., 2005; Mooney and Cleland, 2001; Navarro et al., 2004)

Vectors

species

vectors

H. balmorali

Culicoides impunctatus

H. belopolskyi

Culicoides impunctatus

H. columbae

Ornithomyia avicularia

H. columbae

Pseudolynchia canariensis

H. danilewskyi

Culicoides arboricola

H. danilewskyi

Culicoides edeni

H. danilewskyi

Culicoides knowltoni

H. dolniki

Culicoides impunctatus

H. fringillae

Culicoides impunctatus

H. lanii

Culicoides impunctatus

H. lophortyx

Culicoides bottimeri

H. lophortyx

Lynchia hirsuta

H. lophortyx

Stilbometopa impressa

H. metchinikovi

Chrysops callidus

H. nettionis

Culicoides downesi

H. sacharovi

Peseudolynchia maura

H. syrnii

Ornithomyia avicularia

H. tartakovskyi

Culicoides impunctatus

H. turtur

Pseudolynchia canariensis

Treatment

Little is known about effective treatment. Antimalarial drugs reduce the parasitemia but do not eliminate the parasite. Chloroquine, primaquine, quinacrine, and buparvaquone have been used in pigeons. Combinations of chloroquine and primaquine or chloroquine and mefloquine have been used to treat owls. Treatment is not recommended in asymptomatic birds. Measures to control invertebrate vectors, such as screening of aviaries, help prevent transmission and heavy infections.

MITOCHONDRIA

In the last decade, molecular biological tools have been de-veloped to study haemosporidian parasites of birds (Bensch etal., 2000; Ricklefs and Fallon, 2002; Beadell et al., 2004).DNA-based techniques render detection of haemosporidianseasier, especially at early stages of infections and during chronicinfections when parasitaemia is low and parasites can be over-looked in blood smears (Jarvi et al., 2003). Phylogenetic anal-yses based on parasite genomes have shown that the currentmorphologically based taxonomy may not always reflect ge-netic relationships. Considering genetic variation among indi-viduals within populations and species, molecular diversity isexpected to be greater than morphological diversity (Sehgaletal., 2006). However, Martinsen et al. (2006) concluded fromtheir study that morphological identification of haemosporidianswas fully supported by genetic data, with the exception of asingle species. On the other hand, Valkiu¯nas, Bensch et al.(2006) showed that polymerase chain reaction (PCR)-basedtechniques alone may even underestimate simultaneous infec-tions by haemosporidian parasites, so microscopy remains animportant tool for these kinds of investigation.