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Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd JOURNAL OF POULTRY SCIENCE AND TECHNOLOGY Journal homepage: www.jakraya.com/journal/jpst REVIEW ARTICLE Aspergillosis in Avian Species: A Review G.D. Leishangthem, N.D. Singh * , R.S. Brar and H.S. Banga Department of Veterinary Pathology, College of Veterinary Sciences, Guru Angad Veterinary and Animal Science University, Ludhiana-141004, Punjab, India. * Corresponding Author: N. D. Singh Email: [email protected] Received: 09/01/2015 Revised: 17/02/2015 Accepted: 19/02/2015 Abstract Aspergillosis is an infectious, non-contagious fungal disease of wild and domestic birds caused by fungus Aspergillus species. It is characterized by primary involvement of respiratory tract, formation of yellow cheesy plaques and hard nodular masses in the lungs and air sacs, though other organs may also be generally involved. This fungal disease is of economic importance being the main cause of mortality in the captive birds. Major causative factors are inhalation of overwhelming amount of spores in immunocompromised birds. The review presents the current knowledge on avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords: Aspergillosis, Aspergillus, Avian species, Pathology, Prevention and control. 1. Introduction Avian Aspergillosis is an infectious fungal disease of wild and domestic birds caused by fungus Aspergillus species. It is characterized by primary involvement of respiratory tract, formation of yellow cheesy plaques and hard nodular masses in the lungs and air sacs, though other organs may also be generally involved. The disease is non-contagious and usually occur either in epizootic (acute) or sporadic (chronic) form. Aspergillus species is a ubiquitous saprophytic mold with a worldwide distribution (Ben-Ami et al., 2010; McCormick et al., 2010). Aspergillosis is the most common opportunistic mycotic infection of respiratory tract in birds causing high morbidity and mortality (Tell, 2005) thus inducing a significant economic losses especially in poultry. Inhalation of A. fumigatus asexual spores (conidia) can cause a spectrum of clinical manifestations depending on the immunological status of the host (Ben-Ami et al., 2010; McCormick et al., 2010), besides anatomical and physiological factors also predisposed to such infection. 2. Etiology Among the avian pathogenic species of Aspergillus, Aspergillus fumigatus is the main cause of aspergillosis. Other species like A. flavus, A. nidulans, A. niger and A. terreus can also cause the disease but less frequently than A. fumigatus. Aspergillus belongs to the Kingdom: Fungi, Division: Ascomycota, Class: Eurotiomycetes, Order: Eurotiales, Family: Trichocomaceae. Genus Aspergillus was classified in 1729 by Micheli. The spore-bearing head is the first structure observed in a detailed study of the colony. The arrangement, shape, size and colour of such heads are characteristic of the species and to a lesser extent of the groups to which they belong (Table 1). 3. Transmission and Predisposing Factors All birds are susceptible to aspergillosis. It is reported in domestic birds like poultry, duck, and quails as well as in wild birds as shown in Table 2. Inhalation of conidia or spores from contaminated feed, fecal material, soil and contamination of egg in ovo, infect the developing embryo. Higher susceptibility of birds to aspergillosis may be attributed to anatomic and physiologic characteristics of the avian respiratory system. The small non-expanding lungs and nine air sacs constitute a primary nidus for infection because the air (or conidia) reaches the caudal air sacs before it pass through those part of the lungs in which the gas exchange takes place (Nardoni et al., 2006). Higher body temperature also allows quick fungal growth. Other factors include chronic stress, unsanitary conditions, overcrowding, malnutrition, vitamin deficiencies especially vitamin A and overuse of certain medications (corticosteroids) as well as respiratory irritants (disinfectant fumes and aerosol sprays). Birds that are otherwise ill or are very young or old are also susceptible to aspergillosis.
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Page 1: Aspergillosis in Avian Species: A Review · avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords:

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

JOURNAL OF POULTRY SCIENCE AND TECHNOLOGY Journal homepage: www.jakraya.com/journal/jpst

REVIEW ARTICLE

Aspergillosis in Avian Species: A Review G.D. Leishangthem, N.D. Singh*, R.S. Brar and H.S. Banga Department of Veterinary Pathology, College of Veterinary Sciences, Guru Angad Veterinary and Animal Science University, Ludhiana-141004, Punjab, India.

*Corresponding Author: N. D. Singh Email: [email protected] Received: 09/01/2015

Revised: 17/02/2015

Accepted: 19/02/2015

Abstract Aspergillosis is an infectious, non-contagious fungal disease of wild

and domestic birds caused by fungus Aspergillus species. It is characterized by primary involvement of respiratory tract, formation of yellow cheesy plaques and hard nodular masses in the lungs and air sacs, though other organs may also be generally involved. This fungal disease is of economic importance being the main cause of mortality in the captive birds. Major causative factors are inhalation of overwhelming amount of spores in immunocompromised birds. The review presents the current knowledge on avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords: Aspergillosis, Aspergillus, Avian species, Pathology, Prevention and control.

1. Introduction Avian Aspergillosis is an infectious fungal

disease of wild and domestic birds caused by fungus Aspergillus species. It is characterized by primary involvement of respiratory tract, formation of yellow cheesy plaques and hard nodular masses in the lungs and air sacs, though other organs may also be generally involved. The disease is non-contagious and usually occur either in epizootic (acute) or sporadic (chronic) form.

Aspergillus species is a ubiquitous saprophytic mold with a worldwide distribution (Ben-Ami et al., 2010; McCormick et al., 2010). Aspergillosis is the most common opportunistic mycotic infection of respiratory tract in birds causing high morbidity and mortality (Tell, 2005) thus inducing a significant economic losses especially in poultry. Inhalation of A. fumigatus asexual spores (conidia) can cause a spectrum of clinical manifestations depending on the immunological status of the host (Ben-Ami et al., 2010; McCormick et al., 2010), besides anatomical and physiological factors also predisposed to such infection. 2. Etiology

Among the avian pathogenic species of Aspergillus, Aspergillus fumigatus is the main cause of aspergillosis. Other species like A. flavus, A. nidulans, A. niger and A. terreus can also cause the disease but less frequently than A. fumigatus. Aspergillus belongs to the Kingdom: Fungi, Division: Ascomycota, Class:

Eurotiomycetes, Order: Eurotiales, Family: Trichocomaceae. Genus Aspergillus was classified in 1729 by Micheli. The spore-bearing head is the first structure observed in a detailed study of the colony. The arrangement, shape, size and colour of such heads are characteristic of the species and to a lesser extent of the groups to which they belong (Table 1). 3. Transmission and Predisposing Factors

All birds are susceptible to aspergillosis. It is reported in domestic birds like poultry, duck, and quails as well as in wild birds as shown in Table 2. Inhalation of conidia or spores from contaminated feed, fecal material, soil and contamination of egg in ovo, infect the developing embryo. Higher susceptibility of birds to aspergillosis may be attributed to anatomic and physiologic characteristics of the avian respiratory system. The small non-expanding lungs and nine air sacs constitute a primary nidus for infection because the air (or conidia) reaches the caudal air sacs before it pass through those part of the lungs in which the gas exchange takes place (Nardoni et al., 2006). Higher body temperature also allows quick fungal growth. Other factors include chronic stress, unsanitary conditions, overcrowding, malnutrition, vitamin deficiencies especially vitamin A and overuse of certain medications (corticosteroids) as well as respiratory irritants (disinfectant fumes and aerosol sprays). Birds that are otherwise ill or are very young or old are also susceptible to aspergillosis.

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Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

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Table 1: Summary of microscopic features and colour of colony of various Aspergillus species

4. Pathogenesis

Aspergillosis is caused by inhalation of overwhelming numbers of small, hydrophobic fungal spores (conidia) into the lungs (Oglesbee, 1997). During inhalation, spores initially enters the bird through the nares (two holes in the beak leading to respiratory system), trachea and to the primary bronchi (mesobronchi) which deliver the inhaled air to the posterior thoracic and abdominal air sacs. Thus the inhaled air reaches the posterior air sacs prior to contacting epithelial surfaces in the lungs (Nardoni et al., 2006). Air sacs are particularly prone to infection due to epithelial surface nearly devoid of a mucociliary transport mechanism and absence of macrophages (Brown et al., 1997). Conidia of small size (2-3 microns) enter and germinate in the lungs and air sacs (Fedde, 1998).

Aspergillus and Respiratory Epithelial Cells (REC) Interaction: After entry, the fungus comes in contact with the sticky mucus lining the respiratory tract and respiratory epithelial cells (REC). REC acts not only as a physical barrier but also an addition of the innate immune system. REC engulfed the conidia which are embedded in the atria and parts of the infundibula in the parabronchus (Maina, 2002). Féménia et al. (2009) evaluated that conidia of A. fumigatus and A. flavus inhibit human respiratory cell apoptosis. RECs internalized a portion of adherent conidia by endocytosis while some of the spores germinate externally forming hyphae which penetrates and damage the cells (Bellanger et al., 2009; Nardoni et al., 2006; Cacciuttolo et al., 2009). Invasion of hyphae, via spaces between and within the epithelium, cause cilia loss and cell detachment (Amitani and Kawanami, 2009) or the air sacs cause serosal

inflammation and superficial necrosis in the adjacent organs (Tsai et al., 1992).

Aspergillus and Endothelail Cells Interaction: Fungal conidia and hyphae interact differently with endothelial cells. Conidia were endocytosed by the endothelial cells. Disseminated mycosis occurs by haematogenous spread. Hyphae are tissue and angio invasive and have a unique capacity to survive and proliferate within the host (Dahlhausen et al., 2004). Hyphus interacts with endothelial cells lining of the blood vessels by passing from the abluminal to the luminal surface and cause endothelial cell injury (Kamai et al., 2009). Some of these hyphal fragments can break off and circulate in the bloodstream resulting in disseminated lesions, involving pneumatic bone, peritoneum, internal organs or the CNS (Redig, 1993).

Aspergillus and Macrophages Interaction: The avian respiratory system responds efficiently to invasion by pathogens with a rapid influx of heterophils and macrophages from the subepithelial compartment and pulmonary blood vessels (Nganpiep and Maina, 2002). Macrophages are the main by the phagocytic cells of the respiratory tract and phagocytosed conidia in an actin-dependent manner through the recognition of pathogen-associated molecular patterns by host cell pattern recognition receptors, PRRs (Toll Like Receptors, TLR2 and TLR4 (Netea et al., 2003; 2006) and the C-type lectin receptor dectin-1 (Gersuk et al., 2006). A proinflammatory response is generated characterized production of cytokines (Phadke and Mehrad, 2005) and chemokines (Morrison et al., 2003). Dectin-1 specifically binds to fungal carbohydrates (1, 3)- glucan, which results in phagocytosis, activation of macrophages and generation of proinflammatory responses (Gersuk et al., 2006; Hohl et al., 2005;

Species of Aspergillus

Characteristics of structures supporting asexual spores

Shape of vesicles Colour of the colony

A. clavatus A. flavus A. fumigatus

Long, smooth Colurless, round Short smooth, colourless, greenish

Clavate shape Round, radiate Round, columnar head

Blue-green Yellow-green Blue-green to gray

A. glaucus group A. nidulans A. niger

Variable length, smooth, colourless Short, smooth, brown Long, smooth, colourless or brown

Round, radiate to very loosely columnar head Round, small columnar head Round, radiate, globose and large head

Green with yellow areas Green, buff to yellow Black

A. terreus Short, smooth, colourless Round, compactly colourless head

Cinnamon to brown

A. versicolour

Long, smooth, colourless

Round, loosely, radiate head

White at the beginning turns to yellow, tan, pale green or pink

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Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

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Table 2: Aspergillosis in different avian species

Avian species Aspergillus sp Lesions References

Emu (Dromaius novaehollandiae) A. fumigatus

Pulmonary Aspergillosis Shukla et al., 2013; Eswaran et al., 2011

Emu Chicks Systemic aspergillosis Karunakaran et al., 2010 Pigeon(Columba livia) A. fumigatus Milliary aspergillosis

Systemic Aspergillosis Elmubarak and Fadlelmula, 1991 González-Acuña et al., 2007; Tokarzewski, 2007; Beernaert et al., 2008

A. terreus Disseminated aspergillosis Pal, 1992 Duck (Anas platyrhynchos) A. fumigatus Pulmonary aspergillosis Savage and Isa, 1951; Parker,

2011; Rao and Choudary, 1980

Brahmini duck (Tadoroma ferruginea, Pallus)

Sinha et al., 1978

Khaki Campbell ducks Bhattacharya, 2003

Mallard duck (Anas platyrhynchos)

Adrian et al., 1978; Pearson, 1969; Hille and Lindner, 1968; Whitford and Robinson, 1980

Common peafowl ( Pavo cristatus )

Aspergillus fumigatus

Respiratory aspergillosis Ainsworth and Rewell, 1948

Japanese quail (Coturnix coturnix japonica)

Aspergillus flavus Aspergillus fumigatus

Mycotic salpingitis Pneumonic aspergillosis Experimental aspergillosis Pulmonary Aspergillosis

Singh et al., 1994 Pandita et al., 1991 Chaudhari and Sadana, 1988; Gümüşsoy, 2004; Tell, 2010 Ghori and Edgar, 1973; Borah et al., 2010

Turkey ( Meleagris gallopavo)

A.flavus A. fumigatus

Mycotic pneumonia and pododermatitisArticular aspergillosis of hip joints

Stoute et al., 2010 Olias et al., 2010

Pulmonary Aspergillosis Kunkle and Sacco, 1998; Ghori and Edgar, 1973; Singh et al., 2009

Omphalitis Cortes et al., 2005 Acute aspergillosis Kunkle and Rimler, 1996 Aspergillosis in the brains Ozmen and Dorrestein (2004) Airsacculitis Richard et al., 1996

Davidson et al.,1985 Goliath Heron (Ardea goliath) Aspergillus sp Pulmonary aspergillosis Bonar et al., 2004 Vulture Bearded vulture (Gypaetos barbatus), Eurasian black vultures (Aegypius monachus Linnaeus) Himalayan Griffon Vulture (Gyps himalayensis)

A fumigatus

Pulmonary aspergillosis Angioinvasive pulmonary aspergillosis

Mihaylov et al., 2008; Jung et al., 2009 Barathidasan et al., 2013

Great horned owl (Bubo virginianus)

Aspergillus sp A niger

Pulmonary carcinoma Pulmonary aspergillosis

Rettenmund et al., 2010 Wobeser and Saunders, 1975

Herring Gulls (Larus a. argentatus L.), Seagulls (Larus cachinnans micaellis)

A fumigatus

Pulmonary and Disseminated aspergillosis

Beer 1963; Nardoni et al., 2006

Love bird (Agapornis roseicollis) Red-faced love bird (Agapornis pullaria)

A. fumigates, A. flavus

Pulmonary Apergillosis Mass in upper parts of both lungs

Corrasco et al., 1993 Ainsworth and Rewell, 1948

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Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

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Stitchbird or hihi (Nofiomystis cincta)

A. fumigatus

Lung and air sacs affected

Alley et al., 1999; Cork et al., 1999

Geese (Anser species) gosling

A. fumigatus Pulmonary and systemic aspergillosis

Beytut et al., 2004

Wild geese (Chloëphaga poliocephala)

Ullao et al., 1987

Canada geese (Branta Canadensis) Pink-footed Geese (Anser brachyrhynchus Baillon)

A.flavus A.fumigatus

Syringeal aspergillosis Pulmonary aspergillosis

Stroud and Duncan, 1982 Beer 1963

Geese (Anser species)

Aspergillus sp. Cerebal aspergillosis Palya and Balogh, 1971, 1972

King shag (Phalacocorax albivenier) Juvenile red-crowned crane (Grus japonensis)

A. flavus Pulmonary aspergilloma Hawkey et al, 1984; Stroud and Duncan, 1983

Pheasant Aspergillus species

Spinal Aspergillosis Bygrave, 1981; Barnett et al., 2011

Rhea (Rhea Americana) Aspergillus sp. Pulmonary aspergillosis Reissig et al, 2002; Copetti et al., 2004

Penguin Magellanic penguin (Spheniscus magellanicus, Gentoo penguin (Pygoscelis papua), Chinstrap penguin (Pygoscelis antarctica), King penguin (Aptenodytes patagonica), Little blue penguins (Eudyptula minor), Yellow-eyed penguins (Megadyptes antipodes), Rockhopper penguins (Eudyptes chrysocome), Adelie penguins (Pygoscelis adeliae), Peruvian penguin (Spheniscus humboldti), Black footed /Jackass Penguins (Spheniscus demersus)

A. flavus and A. niger

Tracheal and systemic forms of aspergillosis

Ainsworth and Rewell, 1949; Alvarez-Perez et al., 2010; Carrasco et al., 2001; Flach et al., 1990; Khan et al., 1977; Kittle et al., 2004; Obendorf and McColl, 1980; Graczyk and Cockrem,1995; Hocken, 2000; Nakeeb et al., 1981

Ostrich (Struthio camelus)

A. fumigatus A. niger and A. flavus

Pulmonary Aspergillosis Yokota et al., 2004; Perelman and Kuttin, 1992; Rousseaux and Dalziel, 1981

A. fumigatus

Severe disseminated aspergillosis

Khosravi et al., 2008

A.fumigatus Mycotic rhinitis Fitzgerald and Moisan, 1995

A.fumigatus, A. niger and A. flavus

Pulmonary Aspergillosis

Katz et al., 1996; Marks et al., 1994; Yokota et al., 2004; Perelman and Kuttin 1992

Poultry chicken (Gallus domesticus)

A. flavus A. fumigatus

Multisystemic Aspergillosis with Granulomas Systemic mycosis

Kim et al., 2011 Sawale et al., 2012

Pneumonic-encephalitic aspergillosis

Sawale et al., 2011

Pneumomycosis Islam et al., 2009

Mycotic tracheitis Corkish, 1982; Pal et al., 1990; Singh et al., 1993

Airsacculitis Spanamberg et al., 2013

Pulmonary aspergillosis Mukaratirwa, 2006 Disseminated mycosis Steinlage et al., 2003

Mycotic dermatitis Grewal and Brar, 1987

Concurrent aspergillosis and ascites

Zafra et al., 2008

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Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

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Luther et al., 2007; Kolls and Brown, 2005). Respiratory macrophages kill conidia that have swollen within the phagolysosome with reactive oxygen species (ROS) and phagolysosomal acidification (Ibrahim-Granet et al., 2003; Philippe et al., 2003).

Macrophages in the respiratory tract ingest spores and find their way through the interstitium into the blood and lymphatic stream and thus to other organs (Richard and Thurston, 1983). Macrophage infiltration and the formation of aggregates consisting of multinucleated macrophage giant cells may serve as a cellular defense against the spread of this disease to distant body organs. Van Waeyenberghe et al. (2009) and Qureshi et al. (2000) suggested that spores of A. fumigatus may escape killing by the avian respiratory macrophage. Large amounts of A. fumigatus conidia leads to intracellular germination and lysis of the phagocytic cells (Van Waeyenberghe et al., 2012). Aspergillus species produced a highly immunosuppressive mycotoxin (gliotoxin) which causes degeneration, oncosis and necrosis of the macrophages (Watanabe et al., 2004). Thus this may contribute to colonization of the respiratory tract.

Aspergillus and Immune Cells: Aspergillus fumigatus extract differentially regulates antigen-specific CD4+ and CD8+ T cell responses to promote host immunity (Tao et al., 2006).

Aspergillus Defences: Resting A. fumigatus conidia are resistant to macrophage killing by masking (1, 3)-glucan with hydrophobic rodlets protein and delaying macrophage activation. Melanin pigment in Aspergillus, serve a protective role against host defenses, specifically via scavenging ROS (Jacobson, 2000; Langfelder et al., 2003). Rodlets and superoxide dismutases (SODs) implicated in pathogenicity as scavengers of toxic ROS. Rodlets through the rod gene, rodA mutants, display increased susceptibility to alveolar macrophage killing (Paris et al., 2003). Rodletless conidia also induced a weak inflammatory response in a rat model of invasive aspergillosis (Shibuya et al., 1999). The eukaryotic SOD enzyme, Cu/Zn-SOD has been detected in the cell wall of conidia and hyphae (Hamilton et al., 1996). 5. Clinical Signs

Susceptible bird develops polymorphic clinical forms in relation to either localized or disseminated lesions. Aspergillosis occurs in acute and chronic form. Acute aspergillosis results from inhaling an overwhelming number of spores while chronic aspergillosis generally associates with immunosuppression (Vanderheyden, 1993). 5.1 Acute Form

The acute form usually develops less than a week. Young birds generally have a acute or peracute infection resulting in high morbidity and mortality. Clinical signs include difficult breathing, decrease or anorexia, polydypsia, cyanosis, foetid diarrhea and emaciation. Sometimes the birds may die suddenly without showing any clinical sign. Diagnosis is generally made through a post-mortem examination.

5.2 Chronic Form

The chronic form of aspergillosis may take weeks or months to develop. It is much more common in older birds. Clinical signs vary with the location of the infection. It includes inappetence, emaciation, dyspnea, gasping, increased thirst, fever, diarrhea and signs of nervous involvement (Jensen et al., 1997; Henrici, 1939). Green coloration in urates and hepatomegaly can be seen. Respiration may be noiseless and syrinx involvement leads to wheezing, rattling or clicking sound. Nares may become plugged or discharge with rhinitis (Tsai et al., 1992) along with malformation of the nostrils and beak (Bauck et al., 1992). Death occurs due to severe respiratory involvement. There may be opthalmitis and keratitis (periorbital and eyelid swelling with cheesy yellow exudates in the conjunctival sac) (Beckman et al., 1994; Hoppes et al., 2000) as well as necrotic granulomatous dermatitis (Abrams et al., 2001). Wing droop can be observed when pneumatic bones such as the humerus gets involved (Forbes, 1991). 6. Lesions

The primary location of lesions is the lungs and air sacs although other organs may be involved. Extensive involvement of the respiratory tract can occur before development of clinical signs. Lesions vary in size from pinhead or miller seed (milliary <1mm in diameter) white to yellowish granulomas up to the size of a pea. Roughly spherical granulomatous nodules (>2 cm) may also be observed in serosa and parenchyma of the other organs involved.

6.1 Respiratory System

In acute aspergillosis, lungs showed the most striking lesions which are characterized by marked congestion and often studded with milliary yellow nodules. Each nodule is surrounded by a dark infiltrated zone while the other part of the lung appears normal. Air sacs are usually thickened with small whitish-yellow plaque-like lesions. In peracute pneumonic form, there is complete congestion of lung and no formation of nodules. Chronic aspergillosis is characterized by typical granulomatous lesions. It includes of variable sized nodules or multiple plaques that may be disseminated throughout the air sacs and

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Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

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lungs (Fig 1). These lesions are especially observed in the periphery of the lungs and caudal thoracic and abdominal air sacs and may show sporulating fungal colonies. The serous membrane of the air-sacs is presented with yellowish-white plaque-like lesions or raised white nodules.

Trachea and bronchi may become blocked either by mucoid discharge or by the yellowish-white plaque-like lesions or raised white nodules. Nasal aspergillosis causes exudative rhinitis (Tsai et al., 1992). Malformation of the nostrils and beak were reported (Bauck et al., 1992). Mycotic tracheitis has been reported in chickens (Corkish, 1982) and domestic fowl (Singh et al., 1993). Fungal rhinosinusitis, with almost complete destruction of the premaxilla and deformation of the upper beak were reported by Mans et al. (2007).

6.2 Gastro-intestinal Tract

In turkeys, plaque-like lesions may occur in the mouth, gizzard and intestines (Lignires and Petit, 1898).

Fig 1: Yellowish dense nodules are observed in the air sac and lungs. There is also involvement of the rib bone beneath the lung

6.3 Liver, Kidney, Spleen, Heart, Brain, Ovary

Visceral organs were involved in aspergillosis with formation of nodular granulomatous lesions (Fig 2). Right ventricular dilatation or cor pulmonale due to pulmonary hypertension may occur with or without ascites in poultry (Julian and Goryo, 1990; Hofle et al., 2001). Abscesses in the cerebellum and cerebrum were reported (Raines et al., 1956; Jungherr and Gifford, 1944). It may occur with or without pulmonary and other lesions. In the cerebellum of broiler breeders and turkeys, circumscribed white to greyish areas were observed (Akan et al., 2002; Jensen et al., 1997). Granuloma formation was also seen in the brain and lungs of layer chicken (Kim et al., 2011). Nodular lesions have been reported in ovary (Emmel, 1929). Mycotic salphingitis associated with A. flavus was

reported in adult female Japanese quail. White to grayish nodules 2-5 mm in diameter was present on the serosal surface of the oviduct (Singh et al., 1994).

6.4 Skin

Mycotic pododermatitis along with pulmonary aspergillosis was reported in turkeys. In footpads, keratinized epidermal disruption, encrustations and acute inflammation were noted (Stoute et al., 2009). Epidermal cysts associated with A. fumigatus have been described in the comb of a silky bantam chicken (Suedmeyer et al., 2002). Mycotic dermatitis was also reported in domestic fowl (Grewal and Brar, 1987). 6.5 Eyes

Lesions were observed in the eyes of baby chicks (Hudson, 1947) and in turkeys (Moore, 1953). Mycotic keratitis has been reported. It leads to periorbital swelling, swollen and adhered eyelids with turbid discharge, cloudy cornea and cheesy yellow exudates within the conjunctival sac (Beckman et al., 1994; Hoppes et al., 2000). In a peregrine falcon-gyrfalcon hybrid, blepharitis and dermatitis involving the eyelids and the head were recorded (Abrams et al., 2001). Dyar et al. (1984) reported non ulcerative or mildly ulcerative keratitis in a turkey flock. Dalton and Ainsworth (2011) reported mycotic keratoconjunctivitis in 12-day-old red-legged partridges (Alectoris rufa).

Fig 2: Aspergillosis, Duck: Liver showing multiple

nodular lesions. 6.6 Bones and Joints

Involvement of ribs of broiler is observed as shown in Fig 3. Osteo-arthritis and granulomatous osteoarthritis of the hip joints with necrosis of the femur head was observed in turkey (Olias et al., 2010). Ribs of ostriches (Perelman and Kuttin, 1992) and sternum of broiler breeders with A. flavus (Martin et al., 2007) were reported.

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Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

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7. Histopathology Based on histopathological alterations,

aspergillosis is distinguished into a deep nodular and a superficial diffuse form (Cacciuttolo et al., 2009). A well-organised granulomatous reaction develops in non-aerated as well as aerated parenchyma. An outer thick fibrous layer encapsulated these organised granulomas (Beytut et al., 2004; Copetti et al., 2004). In the adjoining tissues neither exudative inflammation nor vascular lesions were observed in this form (Nardoni et al., 2006, Cacciuttolo et al., 2009).

Fig 3: Aspergillosis, Lung, Poultry: Photomicrograph

of Aspergillus granuloma structure showing necrotic area, inflammatory cells and fungal hyphae (Arrow). Grocott's methenamine silver, X10.

In superficial diffuse form, pyogranulomatous

reaction containing fungal elements predominates in air sacs and lungs and was non-encapsulated (Jensen, 1997). Pyogranuloma is characterized by a centre with variable amounts of septate, dichotomously branching hyphae containing large numbers of conidiophores and conidia. These hyphae were surrounded by a cliff of radially arranged macrophages, heterophils, foreign body giant cells and lymphocytes (Nardoni et al., 2006; Cacciuttolo et al., 2009). Multinucleated cells phagocytized fungal elements. Lymphocytes infiltrated along the margins of the granuloma. In case of severe inflammation, parabronchioles obscured with eosinophilic necrotic material containing degenerated heterophils, erythrocytes and exfoliated epithelial cells (Martin et al., 2007; Beytut, 2004). A mixed type of both tissue reactions in the same tissue section were also reported (Tsai et al., 1992; Atasever and Gu¨mu¨ssoy, 2004).

In case of angioinvasive pulmonary aspergillosis by A. fumigatus (Barathidasan et al., 2013), there was vascular invasion by fungal hyphae involving numerous small to large veins of lungs and air sacs. Both alveolar epithelium and the blood vessel wall were severely damaged by penetrating fungal

hyphae. Numerous vessels were thrombosed as a result of fungal hyphae invasion and intramural host reaction (Barathidasan et al., 2013). 8. Diagnosis

Antemortem diagnosis of aspergillosis can be very difficult since the signs of disease mimic those of many other illnesses, especially in the chronic form. Cases of aspergillosis in birds are often diagnosed based on postmortem findings of white caseous nodules in the lungs or air sacs of affected birds since clinical diagnosis is difficult (Beytut et al., 2004; Charlton et al., 2008). In case of exotic pet birds, cumulative diagnostic tests including biochemistry, haematology, radiography, laparoscopy or endoscopy (Jones and Orosz, 2000) may prove beneficial but these are not available in the poultry context.

8.1 Clinical History

A detailed history of the course of the illness and an accurate description of the diet and husbandry of the bird is required.

8.2 Necropsy Examination

Granulomatous nodules and /or cheesy plaques on the serosa and parenchyma of respiratory tracts as well as other organs are observed. But, definitive diagnosis is based on the isolation of Aspergillus species by culture or by the detection of the organism during histological examination (Kunkle, 2003). 8.3 Direct Microscopy (Wet Smear

Examination) Identification can also be made by preparing a

wet smear. For this, a nodule can be dissected out and crushed on a slide beneath a cover slip in a drop of 20% potassium hydroxide and lactophenol cotton blue. The lactophenol cotton blue stains the fungal hyphae. Wet mounts can also be prepared from sputum or nasal swabs in either 10% KOH and Calcofluor or Parker ink and/or Gram stain. 8.4 Histopathological Examinations

The tissue samples (lungs, trachea, pharynx and thoracic air sacs as well as other organs) fixed in 10% neutral buffered formalin are processed and embedded in paraffin blocks and stain with haematoxylin and eosin (HE) method. Aspergillus hyphae stained poorly in H and E stained sections. Differential stains such as Periodic acid-Schiff (PAS), Bauer's and Gridley's stains differentiate and easily identify the hyphae and mycelia. Special stains for fungus Grocott’s and Gomori Methanamine Silver stain should be employed to detect the presence of fungal hyphae (Fig 3-Arrows). 8.5 Culture

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For proper identification of the species, the pathogenic organism must be isolated by culturing it on differential media. Small pieces of lesions aseptically removed are placed onto plates or slants containing malt agar, Sabouraud's glucose agar or antibiotics and incubated at 37ºC for 24 hours. Species of Aspergillus can be identified by observing the characteristic conidial head and colony as shown in Table 2.

8.6 Immunohistochemistry

Immunohistochemistry with monoclonal or polyclonal antibodies can be used to identify A. fumigatus in lesions. 8.7 Serology

A number of serological test have been applied in the diagnosis of aspergillosis. It includes counter immunoelectrophoresis (CIE), agar gel immunodiffusion (AGI) and enzyme-linked immunosorbent assays (ELISA). However, they should never be used alone, and must be correlated with other clinical and diagnostic data (Redig et al., 1997; Cray et al., 2006; 2009). In acute cases, antibody titre is low and thus detection of circulating Aspergillus antigen in the serum (Cray et al., 2006) while in chronic cases in which antigen levels may be low, detection of antibodies (Jones and Orosz, 2000) may be useful. It should be noted that serological tests have not been validated in poultry and are not currently used in farms to investigate Aspergillosis outbreaks. França et al (2012) reported serologic testing for aspergillosis in commercial broiler chickens and turkeys.

8.8 Differential Diagnosis

Avian aspergillosis signs are nonspecific and depend on the system involved. Pulmonary aspergillosis is usually differentiated from other avian respiratory diseases by the granulomatous lesions at necropsy, but needs to be differentiated from other mycoses and mycobacteriosis. Aspergillosis should be differentiated from chlamydiophylosis, tuberculosis,

neoplasia, vitamin A deficiency, bacterial disease, candidiasis, ascitis, hepatomegaly and pneumonia. 9. Treatment

Treatment for aspergillosis is complicated and relies on the use of antifungal medication. The success of treatment depends upon the location and extent of the infection. However even the most potent drugs could not reach the fungal granulomas or the walled-off fungus by the inflammatory response. This disease has a poor prognosis in extensive infection in the tissues and using only systemic drugs. The best treatment results if the granulomatous lesions are debrided and a topic treatment in conjunction with a systemic therapy is given. The drugs used include itraconazole, fluconazole, clotrimazole, miconazole, ketoconazole and amphotericin B as shown in Table 3. 10. Prevention and Control

No vaccine against aspergillosis is available till date. Some autogenous vaccines have been applied but with little information about this vaccine. Although numerous antifungal protocols have been proposed to cure birds with aspergillosis, treatment of the disease in poultry farms is virtually impossible. Therefore, preventative measures should be practiced so that this disease does not become established in the flock. Since Aspergillus genus is an opportunistic pathogen, reduction of predisposing immunosuppressive factors such as malnutrition and stress should be encouraged. Standard of hygiene, nutrition and housing should be maintained. Mouldy litter or feed should be avoided. Feeders, waterers and incubators should be frequently cleaned and disinfected. Appropriate ventilation should be provided to maintain relative humidity so as to prevent wet litter. Environmental contamination should be control by sporadic or repeated antifungal treatment.

Spraying of fungistatic agents like nystatin, thiabendazole or copper sulphate (at 1 gram per 2 litre of water daily morning for 3 days) decreased fungal

Table 3: Summary of the antifungal drugs used in Aspergillosis

Anti-fungal drugs Dosage Route Amphotericin B

1 mg/kg for 20 minutes, 3 to 4 times a day for 10-14 days 1.5 mg/Kg TID for 3-5 days 1.35 mg/kg

Nebulization IV Topically

Clotrimazole

1% in 2 or 3 ml saline 1.5 hr/day for 4 to 6 weeks

Topical Nebulization

Fluconazole 15mg/kg twice a day for 7 days Orally Itraconazole 5mg-10 mg/kg twice a day for 7-21 days

or 10mg/kg once a day for 7-21 days Orally in feed

Ketoconazole 20 to 30mg/kg twice a day for 2 to 6 weeks Oral Miconazole 1% suspension in 2 or 3 ml saline for 1 week Topical

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contamination of litter. Itraconazole at 10mg/kg once a day for 10 days orally have been used as prophylactic measures in birds with high risk to develop aspergillosis. During outbreak, disease spread can be decreased by changing CuSO4 solution at a dose of 1 gram per 2 litre of water daily orally for 5 days instead of drinking water. Poultry breeder should disinfect eggs soon after being laid and gathered in order not to have problems for future new born chickens.

11. Conclusions

In conclusion, aspergillosis is precipitated when the natural defenses and immunity of the bird is challenged by Aspergillus species. Since clinical diagnosis is difficult, avian aspergillosis is often diagnosed based on postmortem findings supported by microscopy, culture, immunohistochemical technique and molecular methods. Aspergillosis is preventable if proper intensive poultry farming with good husbandry practices like hygiene, food storage and preparation methods, cage location and avoiding stress factors and other conditions that could predispose a bird to the development of the disease.

References Abrams GA, Paul-Murphy J, Ramer JC, Murphy CJ (2001).

Aspergillus blepharitis and dermatitis in a peregrine falcon-gyrfalcon hybrid (Falco peregrinus x Falcorusticolus). Journal of Avian Medicine and Surgery, 15(2): 114-20.

Adrain WJ, Spraker TR and Davies RB (1978). Epornitics of aspergillosis in mallards (Anasplatyrhynchos) in north central Colorado. Journal of Wildlife Diseases, 14: 212-217.

Ainsworth GC and Rewell RE (1949). The incidence of aspergillosis in captive wild birds. Journal of Comparative Pathology and Therapeutics, 59: 213-224.

Akan M, Haziroğlu R, Ilhan Z, Sareyyüpoğlu B and Tunca R (2002). A case of aspergillosis in a broiler breeder flock. Avian Disease, 46(2): 497-501.

Alley MR, Castro I and Hunter JEB (1999). Aspergillosis in hihi (Notiomystis cincta) on Mokoia Island. New Zealand Veterinary Journal, 47: 88-91.

Alvarez-Perez S, Mateos A, Dominguez L, Martinez-Nevado E, Blanco JL and Garcia ME (2010). Polyclonal Aspergillus fumigatus infection in captive penguins. Veterinary Microbiology, 144(3-4): 444-449.

Amitani R and Kawanami R (2009). Interaction of Aspergillus with human respiratory mucosa: a study with organ culture model. Medical Mycology, 47(Suppl. 1): S127-S131.

Arné P, Thierry S, Wang D, Deville M, Le Loc’h G, Desoutter A, Féménia F, Nieguitsila A, Huang W, Chermette R and Guillot J (2011). Aspergillus fumigatus in Poultry. International Journal of Microbiology, Article ID 746356. Doi:10.1155/2011/746356. 14p.

Atasever A and Gümüşsoy KS (2004). Pathological, clinical and mycological findings in experimental aspergillosis infections of starlings. Journal of Veterinary Medicine A -Physiology, Pathology, Clinical Medicine, 51(1): 19-22.

Barathidasan R, Singh SD, Saini M, Sharma AK and Dhama K (2013). The first case of angioinvasive pulmonary aspergillosis in a Himalayan Griffon Vulture (Gyps himalayensis). Avian Biology Research, 6(4): 302-306.

Barnett J, Booth P, Arrow M, Garcia-Rueda C and Irvine RM (2011). Spinal aspergillosis in pheasants. Veterinary Record, 169(17): 449-450.

Bauck L (1994). Mycoses. In: Ritchie BW, Harrison GJ, Harrison LR, editors. Avian medicine: principles and application. Lake Worth: Wingers Publishing.

Bauck L, Hillyer A and Hoefer H (1992). Rhinitis: case reports. Proceedings of the Annual Conference of the Association of Avian Veterinarians New Orleans LA, USA, 134.

Beckman BJ, Howe CW, Trampel DW, DeBey MC, Richard JL and Niyo Y (1994). Aspergillus fumigatus keratitis with intraocular invasion in 15-day-old chicks. Avian Diseases, 38: 660-665.

Beer JV (1963). The incidence of Aspergillus fumigatus in the throats of wild geese and gulls. Sabouraudia, 2: 238-247.

Beernaert, L.A., Pasmans, F., Haesebrouck, F. and Martel, A. 2008. Modelling Aspergillus fumigatus infections in racing pigeons (Columba livia domestica). Avian Pathology 37(5): 545-549.

Bellanger AP, Millon L, Khoufache K, Rivollet D, Bieche I, Laurendeau I, Vidaud M, Botterel F and Bretagne S (2009). Aspergillus fumigatus germ tube growth and not conidia ingestion induces expression of inflammatory mediator genes in the human lung epithelial cell line A549. Journal of Medical Microbiology, 58: 174-179.

Ben-Ami R, Lewis RE and Kontoyiannis DP (2010). Enemy of the (immunosuppressed) state: an update on the pathogenesis of Aspergillus fumigatus infection. British Journal of Haematology, 150: 406-417.

Beytut E (2007). Immunohistochemical diagnosis of aspergillosis in adult turkeys. Turkish Journal of Veterinary and Animal Science, 31(2): 99-104.

Beytut E, Ozcan K and Erginsoy S (2004). Immunohistochemical detection of fungal elements in the tissues of goslings with pulmonary and systemic aspergillosis. Acta Veterinaria Hungarica, 52(1): 71-84.

Bhattacharya A (2003). Aspergillus fumigatus infection in Khaki Campbell ducks in an organized duck farm in Tripura. Indian Veterinary Journal, 80(11): 1178-1179.

Bonar CJ and Lewandowski AH (2004). Use of a liposomal formulation of amphotericin B for treating wound aspergillosis in a Goliath heron (Ardea goliath). Journal of Avian Medicine and Surgery, 18: 162-166.

Borah MK, Jangir BL, Raut SS, Gogo R and Sharma GD (2010). Aspergillosis in Japanese quail (Coturnix

Page 10: Aspergillosis in Avian Species: A Review · avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords:

Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

10

coturnix japonica). Indian Journal of Veterinary Pathology, 34(2): 203-204.

Brown RE, Brain JD and Wang N (1997). The avian respiratory system: a unique model for studies of respiratory toxicosis and for monitoring air quality, Environmental Health Perspectives, 105(2): 188-200.

Bygrave AC (1981). Leg paralysis in pheasant poults (Phasianus colchicus) due to spinal aspergillosis. Veterinary Record, 109(23): 516.

Cacciuttolo E, Rossi G, Nardoni S, Legrottaglie R and Mani P (2009). Anatomopathological aspects of avian aspergillosis. Veterinary Research Communication, 33: 521-527.

Carrasco L, Bautista MJ, de las Mulas JM and Jensen HE (1993). Application of enzyme-immunohistochemistry for the diagnosis of aspergillosis, candidiasis and zygomycosis in three lovebirds. Avian Diseases, 37: 923-927.

Carrasco L, Lima JS Jr., Halfen DC, Salguero FJ, Sanchez-Cordon P and Becker G (2001). Systemic Aspergillosis in an oiled Magallanic penguin (Spheniscus magellanicus). Journal of Veterinary Medicine-B, Infectious Diseases and Veterinary Public Health, 48: 551-554.

Charlton BR, Chin RP and Barnes HJ (2008). Fungal infections. In: Saif, Y.M., Fadly, A.M., Glisson, J.R., McDougald, L.R., Nolan, L.K. and Swayne, D.E. (eds), Diseases of poultry, 12th edn, chap.9, pp. 989-998. Blackwell Publishing, Iowa.

Chaudhari SK and Sadana JR (1988). Experimental aspergillosis in Japanese quails (Coturnix coturnix japonica). Clinical signs and haematological changes. Mycopathologia, 102(3): 179-184.

Copetti MV, Segabinazi SD, Flores ML, Alves SH and Santurio JM (2004). Pulmonary aspergillosis outbreak in Rhea americana in southern Brazil. Mycopathologia, 157(3): 269-271.

Cork SC, Alley MR, Johnstone AC and Stockldale PH (1999). Aspergillosis and other causes of mortality in the stitchbird in New Zealand. Journal of Wildlife Diseases, 35(3): 481-486.

Corkish JD (1982). Mycotic tracheitis in chickens. Avian Pathology, 11: 627-629.

Cortes PL, Shivaprasad HL, Kiupel M and Sentíes-Cué G (2005). Omphalitis associated with Aspergillus fumigatus in poults. Avian Disease, 49(2): 304-308.

Cray C, Watson T and Arheart KL (2009). Serosurvey and diagnostic application of antibody titers to Aspergillus in avian species. Avian Disease, 53(4):491-494.

Cray C, Watson T, Rodriguez M and Arheart K (2006). Assessment of aspergillosis diagnostics. In E. Bergman (Ed.). Proceedings of the 27th Annual Conference and Expo of the Association of Avian Veterinarians (p. 59). San Antonio, TX, USA.

Dahlhausen B, Abbott R and Van Overloop P (2004). Rapid detection of pathogenic Aspergillus species in avian samples by real-time PCR assay: a preliminary report. In E. Bergman (Ed.). Proceedings of the 25th Annual Conference and Expo of the Association of Avian Veterinarians (p. 37). New Orleans, LA, USA.

Dalton JR and Ainsworth H (2011). Mycotic keratoconjunctivitis in 12-day-old red-legged partridges (Alectoris rufa). Veterinary Record, 168(22): 590.

Davidson WR, Nettles VF, Couvillion CE and Howerth EW (1985). Diseases diagnosed in wild turkeys (Meleagris gallopavo) of the southeastern United States. Journal of Wild Disease. 21(4): 386-390.

Deak E, Arunmozhi S and Balajee SA (2010). Molecular methods for identification of Aspergillus species. In: Pasqualotto, A.C. (ed.), Aspergillosis: from diagnosis to prevention, pp. 75-86. Springer, London.

Dyar PM, Fletcher OJ and Page RK (1984). Aspergillosis in turkeys associated with use of contaminated litter. Avian Disease, 28(1): 250-255.

Elmubarak AK and Fadlelmula A (1991). Pathogenesis of Aspergillus fumigatus infection in pigeons in the Sudan. Revue d'élevage et de médecine vétérinaire des pays tropicaux, 44(1): 26-28.

Emmel MW (1929). Aspergillus fumigatus infection of the kidney. Journal of the American Veterinary Medical Association, 7: 369.

Eswaran MA, Sukumar K, Malmarugan S, Poomathi K and Rajeswar JJ (2011). Pulmonary Aspergillois in Emu (Dromaius novaehollandiae). Tamilnadu Journal Veterinary and Animal Sciences, 7(5): 254-255.

F´em´enia F, Huet D, Lair-Fulleringer S, Wagner MC, Sarfati J, Shingarova L, Guillot J, Boireau P, Chermette R and Berkova N (2009). Effects of conidia of various Aspergillus species on apoptosis of human pneumocytes and bronchial epithelial cells. Mycopathologia, 167(5): 249-262.

Fedde MR (1998). Relationship of structure and function of the avian respiratory system to disease susceptibility. Poultry Science, 77: 1130-1138.

Fitzgerald SD and Moisan PG (1995). Mycotic rhinitis in an ostrich. Avian Disease, 39(1): 194-196.

Flach EJ, Stevenson MF and Henderson GM (1990). Aspergillosis in gentoo penguins (Pygoscelis papua) at Edinburgh Zoo, 1964-1988. Veterinary Record, 126(4): 81-85.

Forbes NA (1991). Aspergillosis in raptors. Veterinary Record, 128 (11): 263.

França M, Cray C and Shivaprasad HL (2012). Serologic testing for aspergillosis in commercial broiler chickens and turkeys. Avian Disease, 56(1): 160-164.

Gersuk GM, Underhill DM, Zhu L and Marr KA (2006). Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. Journal of Immunology, 176: 3717-3724.

Ghori HM and Edgar SA (1973). Comparative susceptibility of chickens, turkeys and coturnix quail to aspergillosis. Poultry Science, 52: 2311-2315.

González-Acuña D, Silva GF, Moreno SL, Cerda LF, Donoso ES, Cabello CJ and López MJ (2007). Detection of some zoonotic agents in the domestic pigeon (Columba livia) in the city of Chillán, Chile. Revista Chilena de Infectología, 24(3): 199-203.

Graczyk TK and Cockrem JF (1995). Aspergillus spp. seropositivity in New Zealand penguins. Mycopathologia, 131(3): 179-184.

Grewal GS and Brar RS (1987). Mycotic dermatitis in domestic fowl. A case report. Mykosen, 30(9): 440-442.

Page 11: Aspergillosis in Avian Species: A Review · avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords:

Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

11

Gumussoy KS, Uyanik F, Atasever A and Cam Y (2004). Experimental Aspergillus fumigatus infection in quails and results of treatment with itraconazole. Journal of Veterinary Medicine B, 51: 34-38.

Hamilton AJ, Holdom MD and Jeavons L (1996). Expression of the Cu,Zn superoxide dismutase of Aspergillus fumigatus as determined by immunochemistry and immunoelectron microscopy. FEMS Immunolology and Medical Microbiology, 14: 95-102.

Hawkey CM, Pugsley SL and Knight JA (1984). Abnormal heterophils in a king shag with aspergillosis. Veterinary Record, 114: 322-324.

Henrici AT (1939). An endotoxin from Aspergillus fumigatus. Journal of Immunology, 36: 319-338.

Hille G and Lindner KE (1968). Spontaneous and experimental aflatoxicosis of ducks. Monatsh Veterinarmed, 23(18): 685-688.

Hocken AG (2000). Cause of death in blue penguins (Eudyptula m. minor) in North Otago, New Zealand. New Zealand Journal of Zoology, 27: 305-309.

Hofle U, Blanco JM, Rodriguez A and Vicente A (2001). Atypic aspergillosis-a new threat to the Iberian imperial eagle (Aquila adalberti)? In R. Korbel. Proceedings of the German Veterinary Medical Society, 6th European AAV-DVG Conference of the Association of Avian Veterinarians, 4th Scientific ECAMS Meeting of the European College of Avian Medicine and Surgery, 288. Munich, Germany.

Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, Feldmesser M and Pamer EG (2005). Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathogen, 1: e30.

Hoppes S, Gurfield N, Flammer K, Colitz C and Fisher P (2000). Mycotic keratitis in a blue-fronted Amazon parrot (Amazona aestiva). Journal of Avian Medicine and Surgery, 14: 185-189.

Hudson CB (1947). Aspergillus fumigatus infection in the eyes of baby chicks. Poultry Science, 26: 192-193.

Ibrahim-Granet O, Philippe B, Boleti H, Boisvieux-Ulrich E, Grenet D, Stern M and Latge JP (2003). Phagocytosis and intracellular fate of Aspergillus fumigatus conidia in alveolar macrophages. Infection and Immunity, 71: 891-903.

Islan MN, Rashid MH, Juli MSB, Rima UK and Khatun M (2009). Pneumomycosis in chickens: clinical, pathological and therapeutical investigation. International Journal of Sustainable Crop Production, 4: 16-21.

Jacobson ES (2000). Pathogenic roles for fungal melanins. Clinical Microbiology Reviews, 13: 708-717.

Jensen HE, Christensen JP, Bisgaard M and Nielsen OL (1997). Immunohistochemistry for the diagnosis of aspergillosis in turkey poults. Avian Pathology, 26(1): 5-18.

Jones MP, Orosz SE, Cox SK and Frazier DL (2000). Pharmacokinetic disposition of itraconazole in red-tailed hawks (Buteo jamaicensis). Journal of Avian Medicine and Surgery, 14(1): 15-22.

Julian RJ and Goryo M (1990). Pulmonary aspergillosis causing right ventricular failure and ascites in meat-type chickens. Avian Pathology, 19: 643-654.

Jung K, Kim Y, Lee H and Kim JT (2009). Aspergillus fumigatus infection in two wild Eurasian black vultures (Aegypius monachus Linnaeus) with carbofuran insecticide poisoning: a case report. Veterinary Journal, 179(2): 307-312.

Jungherr E and Gifford R (1944). Three hitherto unreported turkey diseases in Connecticut. Erysipelas - hexamitiasis - mycotic encephalomalacia. The Cornell Veterinarian, 34: 214-226.

Kamai Y, Lossinsky AS, Liu H, Sheppard DC and Filler SG (2009). Polarized response of endothelial cells to invasion by Aspergillus fumigatus. Cellular Microbiology, 11: 170-182.

Karunakaran S, Nair GK, Nair ND and Mini M (2010). Systemic Aspergillosis in Emu Chicks in an organised farm in Kerala. Veterinary World, 3(10): 453-455.

Katz ME, Love SC, Gill HS and Cheetham BF (1996). Development of a method for the identification, using the polymerase chain reaction, of Aspergillus fumigatus isolated from ostriches. Australian Veterinary Journal, 74(1): 50-54.

Khan ZU, Pal M, Paliwal DK and Damodaram VN (1977). Aspergillosis in imported penguins. Sabouraudia, 15: 43-45.

Khosravi AR, Shokri H, Ziglari T, Naeini AR, Mousavi Z and Hashemi H (2008). Outbreak of severe disseminated aspergillosis in a flock of ostrich (Struthio camelus). Mycoses, 51(6): 557-559.

Kim J, Kim J and Mo I (2011). Multisystemic Aspergillosis with Granulomas in Layer Chickens. Korean Journal of Poultry Science, 38(1): 45-50.

Kittle D (2004). Zoo without penguins after fatal 02 illness, 06/02/2003. Available at: http//www.potterparkzoo.org

Kolls JK and Brown GD (2005). The beta-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathogen, 1: e42.

Kunkle RA (2003). Aspergillosis: In Diseases of Poultry, Y. M. Saif, H. J. Barnes, J. R. Glisson et al., Eds., pp. 883–895, Iowa State University Press, Ames, Iowa, USA, 11th edition.

Kunkle RA and Rimler RB (1996). Pathology of acute aspergillosis in turkeys. Avian Disease, 40(4): 875-886.

Kunkle RA and Sacco RE (1998). Susceptibility of convalescent turkeys to pulmonary aspergillosis. Avian Disease, 42(4): 787-790.

Langfelder K, Streibel M, Jahn B, Haase G and Brakhage AA (2003). Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genetics and Biology, 38: 143-158.

Lignieres and Petit (1898). Péritonite aspergillaire des dindon. Rec Méd Vét, 75: 145-149.

Luther K, Torosantucci A, Brakhage AA, Heesemann J and Ebel F (2007). Phagocytosis of Aspergillus fumigatus conidia by murine macrophages involves recognition by the dectin-1 beta-glucan receptor and Toll-like receptor 2. Cellular Microbiology, 9: 368-381.

Maina JN (2002). Some recent advances on the study and understanding of the functional design of the avian lung: morphological and morphometric perspectives. Biological Reviews of the Cambridge Philosophical Society, 77: 97-152.

Page 12: Aspergillosis in Avian Species: A Review · avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords:

Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

12

Mans C and Guzman DS (2007). What is your diagnosis? Fungal rhinosinusitis, with almost complete destruction of the premaxilla and deformation of the upper beak. Journal of Avian Medicine and Surgery, 21(3): 235-238.

Marks SL, Stauber EH and Ernstrom SB (1994). Aspergillosis in an ostrich. Journal of the American Veterinary Medical Association, 204(5): 784-785.

Martin MP, Bouck KP, Helm J, Dykstra MJ, Wages DP and Barnes HJ (2007). Disseminated Aspergillus flavus infection in broiler breeder pullets. Avian Disease, 51(2): 626-631.

McCormick A, Loeffler J and Ebel F (2010). Aspergillus fumigatus: contours of an opportunistic human pathogen. Cellular Microbiology, 12: 1535-1543.

McDougle HC and Vaught W (1968). An epizootic of Aspergillosis in Canada Geese. Journal of Wildlife Management, 32: 415-417.

Mihaylov G, Petrov V, Marutsov P, Simeonov R and Simeonova G (2008). A case of aspergillosis in a bearded vulture (Gypaetos barbatus). Trakia Journal of Science, 6(1): 144-146.

Moore EN (1953). Aspergillus fumigatus as a cause of opthalmitis in turkeys. Poultry Science, 32: 796-799.

Morrison BE, Park SJ, Mooney JM and Mehrad B (2003). Chemokine- mediated recruitment of NK cells is a critical host defense mechanism in invasive aspergillosis. Journal of Clinical Investigation, 112: 1862-1870.

Mukaratirwa S (2006). Outbreak of disseminated zygomycosis and concomitant pulmonary aspergillosis in breeder layer cockerels. Journal of Veterinary Medicine, 53: 51-53.

Nganpiep L and Maina JN (2002). Composite cellular defence stratagem in the avian respiratory system: functional morphology of the free (surface) macrophages and specialized pulmonary epithelia. Journal of Anatomy, 200: 499-516.

Nakeeb SM, Babus B and Clifton Jr AY (1981). Aspergillosis in the Peruvian Penguin (Spheniscus humboldti). The Journal of Zoo Animal Medicine, 12(2): 51-54.

Nardoni S, Ceccherelli R, Rossi G and Mancianti F (2006). Aspergillosis in Larus cachinnans micaellis: survey of eight cases. Mycopathologia, 161(5): 317-321.

Netea MG, Ferwerda G, Van der Graaf CA, Van der Meer JW and Kullberg BJ (2006). Recognition of fungal pathogens by Toll-like receptors. Current Pharmaceutical Design, 12: 4195-4201.

Netea MG, Warris A, Van der Meer JW, Fenton MJ, Verver- Janssen TJ, Jacobs LE, Andresen T, Verweij PE and Kullberg BJ (2003). Aspergillus fumigatus evades immune recognition during germination through loss of Toll-like receptor-4-mediated signal transduction. Journal of Infectious Disease, 188: 320-326.

Obendorf DL and McColl K (1980). Mortality in little penguins (Eudyptula minor) along the coast of Victoria. Australia Journal of Wildlife Disease, 16: 251-259.

Oglesbee BL (1997). Mycotic Diseases. In: Altman, R.B., Clubb, S.L., Dorrestein, G.M., Quesenberry, K., editors. Avian medicine and surgery. Philadelphia: W.B. Saunders, 1997. Chapter pagination: 323-331.

Olias P, Hauck R, Windhaus H, van der Grinten E, Gruber AD and Hafez HM (2010). Articular aspergillosis of hip joints in turkeys. Avian Disease, 54(3): 1098-1101.

Ozmen O and Dorrestein MG (2004). Observations of aspergillosis in the brains of turkey poults using different histopathological staining techniques. Biotechnic and Histochemistry, 79(2): 95-99.

Pal M (1992). Disseminated Aspergillus terreus infection in a caged pigeon. Mycopathologia, 119(3): 137-139.

Pal M, Prajapati S and Gangopadhyay RM (1990). Aspergillus fumigatus as a cause of mycotic tracheitis in a chicken. Mycoses, 33(2): 70-72.

Palya V and Balogh T (1971). Brain aspergillosis in goose and poultry. Magyar Allatorvosok Lapja, 6: 307-310.

Palya V and Balogh T (1972). Cerebral aspergillosis in geese and turkeys. Veterinary Bulletin, 42: 1355.

Pandita A, Sadana JR and Asrani RK (1991). Studies on clinical signs and haematological alterations in pneumonic aspergillosis due to Aspergillus flavus in Japanese quail. Mycopathologia, 116(2): 119-123.

Paris S, Debeaupuis JP, Crameri R, Carey M, Charles F, Prevost MC, Schmitt C, Philippe B and Latge JP (2003). Conidial hydrophobins of Aspergillus fumigatus. Applied and Environmental Microbiology, 69: 1581-1588.

Parker CD (2011). Aspergillosis in gamebirds and ducks. Veterinary Record, 169(23): 613-614.

Pearson GL (1969). Aspergillosis in wintering mallards. Wildlife Disease, 5(4): 404-405.

Perelman, B. and Kuttin, E.S. 1992. Aspergillosis in ostriches Avian Pathology, 21:159-163.

Phadke AP and Mehrad B (2005). Cytokines in host defense against Aspergillus: recent advances. Medical Mycology, 43(Suppl. 1): S173-S176.

Philippe B, Ibrahim-Granet O, Prevost MC, Gougerot-Pocidalo MA, Sanchez Perez M, Van der Meeren A and Latge JP (2003). Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infection and Immunity, 71: 3034-3042.

Pollock C (2003). Fungal diseases of columbiformes and anseriformes. Veterinary Clinics of North America: Exotic Animal Practice, 6(2): 351-361.

Qureshi MA, Heggen CL and Hussain I (2000). Avian macrophage: effector functions in health and disease. Developmental and Comparative Immunology, 24: 103-119.

Raines TV, Kuzdas CD, Winkel FH and Johnson BS (1956). Encephalitic aspergillosis in turkeys - a case report. Journal of the American Veterinary Medical Association, 129: 435-436.

Rao MR and Choudary C (1980). Aspergillosis in ducks. Poultry Advisor, 13: 59-60.

Redig PT (1993). Avian aspergillosis. In Fowler, M E (ed): Zoo and Wild Animal Medicine: Current therapy 3. W B Saunders Inc. pp 178-181.

Redig PT, Orosz S and Cray C. (1997). The ELISA as a management guide for aspergillosis in raptors. M Doolen (Ed). Proceedings of the Annual Conference and Expo of the Association of Avian Veterinarians (p. 99). Reno, NV, USA.

Page 13: Aspergillosis in Avian Species: A Review · avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords:

Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

13

Reissig EC, Uzal FA, Schettino A and Robles CA (2002). Pulmonary aspergillosis in a great rhea (Rhea americana). Avian Disease, 46(3): 754-756.

Rettenmund C, Sladky KK, Rodriguez D, Petersen M, Pinkerton ME and Rao D (2010). Pulmonary carcinoma in a great horned owl (Bubo virginianus). Journal of Zoo and Wildlife Medicine, 41(1): 77-82.

Richard JL and Thurston JR (1983). Rapid hematogenous dissemination of Aspergillus fumigatus and A. flavus spores in turkey poults following aerosol exposure. Avian Disease, 27(4): 1025-1033.

Richard JL, Dvorak TJ and Ross PF (1996). Natural occurrence of gliotoxin in turkeys infected with Aspergillus fumigatus, Fresenius. Mycopathologia, 134(3): 167-170.

Rousseaux CG and Dalziel JB (1981). Aspergillus pneumonia in an ostrich (Struthio camelus). Australian Veterinary Journal, 57(3): 151-152.

Savage A and Isa JM (1951). Aspergillosis in ducks. Canadian Journal of Comparative Medicine and Veterinary Science, 15(6): 146.

Sawale GK, Mane DV, Gupta SC, Srivastava PK, Rohi RR, Ingole KH, Bharkad GP and More BK (2011). Pneumoencephalitic aspergillosis in broiler breeder flock: Field investigation. Indian Journal of Veterinary Pathology, 35 (2): 221-222.

Sawale GK, Roshini S, Tirpude NV, Patil G, Satale SB, Yadav M, Mustare AK, Mhase AK, Wavhal S, Kadam DP, Patil SG and Moregaonkar SD (2012). Systemic mycosis in commercial broiler chicken flock. Indian Journal of Veterinary Pathology, 36(1): 57-59.

Shibuya K, Takaoka M, Uchida K, Wakayama M, Yamaguchi H, Takahashi K, Paris S, Latge JP and Naoe S (1999). Histopathology of experimental invasive pulmonary aspergillosis in rats: pathological comparison of pulmonary lesions induced by specific virulent factor deficient mutants. Microbial Pathogenesis, 27: 123-131.

Shukla S, Parihar S, Shrivastava N, Dar LM and Hussain SA (2013). Outbreak of Aspergillus fumigatus in an Organized Emu Farm in Indore, India. Journal of Advanced Veterinary Research, 3(1): 8-11.

Simpson VR and Euden PR (1991). Aspergillosis in parrots. Veterinary Record, 128(8): 191-192.

Singh H, Grewal GS and Singh N (1994). Mycotic salpingitis in a Japanese quail (Coturnix coturnix japonica). Avian Disease, 38(4): 910-913.

Singh N, Grewal GS, Brar RS, Singh B, Dhaliwal AS and Jand SK (1993). Outbreak of mycotic tracheitis in domestic fowl. Mycoses, 36(1-2): 65-67.

Singh S, Borah MK, Sharma DK, Joshi GD and Gogoi R (2009). Aspergillosis in turkey poults. Indian Journal of Veterinary Pathology, 33(2): 220-221.

Sinha BK, Sharma TS, Sinha PN and Jha GJ (1978). Aspergillosis in a Brahmini duck (Tadoroma ferruginea, Pallus)--a case report. Mykosen, 21(9): 307-311.

Spanamberg A, Machado G, Casagrande RA, Sales GM, Fraga CF, Corbellini LG, Driemeier D and Ferreiro L (2013). Aspergillus fumigatus from normal and conde-mned carcasses with airsacculitis in commercial

poultry. Pesquisa Veterinária Brasileira, 33(9): 1071-1075.

Steinlage SJT, Sander JE, Brown TP, Lobsinger CM, Thayer SG and Martinez A (2003). Disseminated mycosis in layer cockerels and pullets. Avian Disease, 47: 229-233.

Stoute ST, Bickford AA, Walker RL and Charlton BR (2009). Mycotic pododermatitis and mycotic pneumonia in commercial turkey poults in northern California. Journal of Veterinary Diagnostic Investigation, 21(4): 554-557.

Stroud RK and Duncan RM (1982). Occlusion of the syrinx as a manifestation of aspergillosis in Canada geese. Journal of the American Veterinary Medical Association, 181(11): 1389-1391.

Stroud RK and Duncan RM (1983). Aspergillosis in a red-crowned crane. Journal of the American Veterinary Medical Association, 183(11): 1297-1298.

Suedmeyer WK, Bermudez AJ and Fales WH (2002). Treatment of epidermal cysts associated with Aspergillus fumigatus and Alternaria species in a silky bantam chicken. Journal of Avian Medicine and Surgery, 16: 133-137.

Tao J, Segal BH, Eppolito C, Li Q, Dennis CG, Youn R and Shrikant PA (2006). Aspergillus fumigatus extract differentially regulates antigen-specific CD4+ and CD8+ T cell responses to promote host immunity. Journal of Leukocyte Biology, 80(3): 529-537.

Tell LA (2005). Aspergillosis in mammals and birds: impact on Veterinary medicine. Medical Mycology, 43 Suppl 1: S71-73.

Tell LA, Clemons KV, Kline Y, Woods L, Kass PH, Martinez M and Stevens DA (2010). Efficacy of voriconazole in Japanese quail (Coturnix japonica) experimentally infected with Aspergillus fumigatus. Medical Mycology, 48(2): 234-244.

Tokarzewski S, Zio´ łkowska G, Łopuszyn´ ski W and Nozdryn-Płotnick Z (2007). Aspergillus fumigatus infection in a pigeon flock. Bulletin of the Veterinary Institute in Pulawy, 51(4): 563-567.

Tsai SS, Park JH, Hirai K and Itakura C (1992). Aspergillosis and candidiasis in psittacine and passeriforme birds with particular reference to nasal lesions. Avian Pathology, 21: 699-709.

Ulloa J, Cubillos V, Montecinos MI and Alberdi A (1987). Aspergillosis in wild goose (Chloëphaga poliocephala Scl.,1857) in Chile. Journal of Veterinary Medicine-B, 34: 30-35.

Van Waeyenberghe L, Pasmans F, Beernaert LA, Haesebrouck F and Martel A (2009). Interaction of the avian macrophage with Aspergillus fumigatus: to let live or let die. In Martel, A. (Ed.). Proceedings of the 10th European Conference of the Association of Avian Veterinarians, 8th ECAMS Scientific Meeting of the Association of the European College of Avian Medicine and Surgery (p. 375). Antwerp, Belgium.

Van Waeyenberghe L, Pasmans F, D'Herde K, Ducatelle R, Favoreel H, Li SJ, Haesebrouck F and Martel A (2012). Germination of Aspergillus fumigatus inside avian respiratory macrophages is associated with cytotoxicity. Veterinary Research, 43(1): 32.

Page 14: Aspergillosis in Avian Species: A Review · avian aspergillosis, though in brief due to journal space limitations, from etiology, pathology, diagnosis to treatment and control. Keywords:

Leishangthem et al…Aspergillosis in Avian Species: A Review

Journal of Poultry Science and Technology | January-March, 2015 | Vol 3 | Issue 1 | Pages 01-14 © 2015 Jakraya Publications (P) Ltd

14

Vanderheyden N (1993). Aspergillosis in psittacine chicks. In Jackson, G. (Ed.). Proceedings of the Annual Conference of the Association of Avian Veterinarians (p. 207). Nashville, TN, USA.

Watanabe A, Kamei K, Sekine T, Higurashi H, Ochiai E, Hashimoto Y and Nishimura K (2004). Cytotoxic substances from Aspergillus fumigatus in oxygenated or poorly oxygenated environment. Mycopathologia, 158: 1-7.

Whitford HW and Robinson RM (1980). Aspergillosis in a wild mallard duck. Southwestern Veterinarian, 33(1): 11-12.

Wobeser G and Saunders JR (1975). Pulmonary oxalosis in association with Aspergillus niger infection in a Great Horned owl (Bubo virginianus). Avian Disease, 19(2): 388-392.

Yokota T, Shibahara T, Wada Y, Hiraki R, Ishikawa Y and Kadota K (2004). Aspergillus fumigatus infection in an ostrich (Struthio camelus). Journal of Veterinary Medical Science, 66(2): 201-204.

Zafra R, Pérez J, Pérez-Ecija RA, Borge C, Bustamante R, Carbonero A and Tarradas C (2008). Concurrent aspergillosis and ascites with high mortality in a farm of growing broiler chickens. Avian Disease, 52(4): 711-713.


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