Avian Pathology

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Aspergillus infections in birds: a review

L. A. Beernaert , F. Pasmans , L. Van Waeyenberghe , F. Haesebrouck & A.

Martel

To cite this article: L. A. Beernaert , F. Pasmans , L. Van Waeyenberghe , F. Haesebrouck &

A. Martel (2010) Aspergillus infections in birds: a review, Avian Pathology, 39:5, 325-331, DOI:
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Avian Pathology (October 2010) 39(5), 325331

Aspergillus infections in birds: a review

L. A. Beernaert*, F. Pasmans, L. Van Waeyenberghe, F. Haesebrouck and A. Martel

Department of Pathology, Bacteriology and Poultry Diseases, Faculty of Veterinary Medicine, Ghent University,
Salisburylaan 133, 9820 Merelbeke, Belgium

Aspergillosis is an infectious, non-contagious fungal disease caused by species in the ubiquitous

opportunistic saprophytic genus Aspergillus, in particular Aspergillus fumigatus. This mycosis was described
many years ago, but continues to be a major cause of mortality in captive birds and, less frequently, in free-
living birds. Although aspergillosis is predominantly a disease of the respiratory tract, all organs can be
involved, leading to a variety of manifestations ranging from acute to chronic infections. It is believed that
impaired immunity and the inhalation of a considerable amount of spores are important causative factors.
The pathogenesis, early diagnostic methods and antifungal treatment schedules need to be further studied in
order to control this disease. The aim of the present review is to present the current knowledge on
aspergillosis with the main emphasis on A. fumigatus infections in captive and free-living birds rather than
domestic poultry. The review covers aetiology, epidemiology, pathogenesis, clinical signs and lesions,
diagnosis, treatment and prevention.

Aetiology
Aspergillosis is mostly caused by Aspergillus fumigatus
but Aspergillus flavus, Aspergillus niger, Aspergillus
glaucus, Aspergillus nidulans, and other Aspergillus
species or mixed infections can play a role in the disease
(Barton et al., 1992; Perelman & Kuttin, 1992; Joseph,
2000). The reason why A. fumigatus is the predominant
species of airborne fungal infections might be that the
spores are much smaller than the spores of other
Aspergillus species (Richard & Thurston, 1983).
Epidemiology
An increased concentration of spores in the environment
may predispose a bird to aspergillosis. A warm environ-
ment, humidity, poor ventilation (Phalen, 2000; Tell,
2005), poor sanitation (Oglesbee, 1997) and the long-
term storage of feed (Khosravi et al., 2008) may increase
the amount of spores in the air. Factors impairing the
bird’s immunity can also predispose to mycosis. Exam-
ples of this include the administration of tetracyclines
(Oglesbee, 1997) or long-term steroids (Verstappen &
Dorrestein, 2005), vaccination (Barton et al., 1992),
metabolic bone disease (Vanderheyden, 1993), an inade-
quate diet (Bauck et al., 1992; Dorrestein, 1992) result-
ing in hypovitaminosis A (McMillan & Petrak, 1989; De
Herdt, 1996), overcrowding (McMillan & Petrak, 1989),
shipping (Tsai et al., 1992), quarantine or capture of wild
birds (Abrams et al., 2001), starvation, thermal discom-
fort, migration (Young et al., 1998), inbreeding (Low
et al., 2005), circovirus infection (Soike et al., 1999) and
lymphoproliferative disorders (Kelly et al., 2004), tox-
icosis (Young et al., 1998; Carrasco et al., 2001; Jung
et al., 2009), traumatic injuries (Xavier, 2008) and
reproductive activity (Jones & Orosz, 2000).
Pathogenesis
Inhalation is considered the main infection route for A.
fumigatus in birds (Oglesbee, 1997), and because A.
fumigatus spores are too small to be trapped completely
in the nasal cavity or trachea, some are able to reach the
lungs and air sacs (Fedde, 1998). The air sacs are usually
the primary infection sites, since inhaled air reaches the
posterior thoracic and abdominal air sacs prior to
contacting epithelial surfaces in the lungs (Nardoni
et al., 2006). In the lung parenchyma, spores get
embedded in the atria and parts of the infundibula in
the parabronchus and are engulfed by (surface) phago-
cytic epithelial cells (Maina, 2002). When there are too
many spores or the bird has an impaired immune
response, the innate defence mechanisms do not succeed
in eliminating infection at the site of the air capillaries.
This may lead to the development of loosely attached
plaques, which may or may not become overgrown by
connective tissue of the host. These plaques or necrotic
debris in the respiratory tract can obstruct the trachea or
bronchi and/or fill up the air sacs (Oglesbee, 1997).
Occasionally, sporulation occurs in the lungs and air sacs
(Nardoni et al., 2006; Cacciuttolo et al., 2009). Hyphae
containing fruiting bodies can fill the lumen and may
penetrate the air sacs, causing serositis and superficial
necrosis in the adjacent organs (Tsai et al., 1992). Besides
direct extension of the infection through the air sac wall,
disseminated mycosis also occurs by haematogenous
spread. Hyphae, which are known to be tissue and
angio-invasive (Dahlhausen et al., 2004), as well as host
cells play a role in this spreading mechanism. Macro-
phages 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 &
Thurston, 1983).

*To whom correspondence should be addressed. Tel:
32 474 43 86 62. E-mail: info@bijzonderehuisdieren.be
Received 17 November 2009
ISSN 0307-9457 (print)/ISSN 1465-3338 (online)/10/050325-07 # 2010 Houghton Trust Ltd
DOI: 10.1080/03079457.2010.506210
326 L. A. Beernaert et al.
The relevance of virulence factors in avian aspergillo-
sis is not well known, as research on this is minimal
(Peden & Rhoades, 1992; Richard et al., 1994, 1996).
Ongoing studies suggest that A. fumigatus conidia may
be able to resist killing by the avian respiratory macro-
phage (Van Waeyenberghe et al., 2009).
Two types of tissue reaction are recognized: the
granulomatous or deep nodular form, and the infiltra-
tive or superficial diffuse form. In the first type, neither
exudative inflammation nor vascular lesions in the
neighbouring tissues are seen. This type of encapsulated
reaction develops both in non-aerated and aerated
organs (Nardoni et al., 2006; Femenia et al., 2007;
Cacciuttolo et al., 2009). In the non-ridged, non-
encapsulated infiltrative type, the fungus frequently
invades blood vessels. In aerated organs such as the
lungs and the air sacs, the fungus may form aggregates of
radiating hyphae containing large numbers of conidio-
phores and conidia in the absence of a structured
granuloma formation (Nardoni et al., 2006; Cacciuttolo
et al., 2009). A mixed type composed of both tissue
reactions in the same tissue section is also possible (Tsai
et al., 1992; Atasever & Gümüssoy, 2004).
The popular assumption that the paucity of free avian
respiratory macrophages results in an inadequate or
incompetent avian respiratory immune system and is
therefore responsible for the high susceptibility of
birds to respiratory pathogens (Toth & Siegel, 1986)
lacks scientific foundation. Instead, the susceptibility of
birds to Aspergillus spp. may be attributed to differences
in anatomical, physiological and respiratory immune
system characteristics compared with mammals (Toth,
2000; Maina, 2002; Tell, 2005).
Clinical signs and lesions
Clinical manifestations depend on the infective dose, the
spore distribution, pre-existing diseases, and the immune
response of the host (Dahlhausen et al., 2004). Avian
aspergillosis is often classified as acute or chronic. Acute
aspergillosis is thought to be the result of inhaling an
overwhelming number of spores, while chronic aspergil-
losis is generally associated with immune suppression
(Vanderheyden, 1993).
Although aspergillosis is predominantly a disease of
the respiratory tract, any organ can be infected. Nasal
aspergillosis causes exudative rhinitis (Tsai et al., 1992),
possibly accompanied by malformation of the nostrils,
beak and cere (Bauck et al., 1992). Mycotic keratitis can
cause blepharospasm, photophobia, periorbital swelling,
turbid discharge, swollen and adhered eyelids, cloudy
cornea and cheesy yellow exudates within the conjuncti-
val sac (Beckman et al., 1994; Hoppes et al., 2000).
Neurological signs can be caused by Aspergillus spp.
(Jensen et al., 1997). Epidermal cysts associated with A.
fumigatus have been described in the comb of a silky
bantam chicken (Suedmeyer et al., 2002). Aspergillus
blepharitis and dermatitis involving the eyelids and the
head have been described in a peregrine falcongyrfalcon
hybrid (Falco peregrinus x Falco rusticolus) (Abrams
et al., 2001). Right ventricular dilatation (cor pulmonale)
due to pulmonary hypertension, with or without ascites,
and congestion of the lungs caused by ventricular failure
occasionally occurs (Julian & Goryo, 1990; Höfle et al.,
2001). Birds suffering from aspergillosis do not always
show respiratory problems. The owner of a trained
raptor, for example, may rather observe that the bird’s
reactions are impaired. Unilateral drooping of the wing
(due to infection of the thoracic air sac, the clavicular air
sac or the proximal humerus) or repeated vomiting (due
to lesions in the anterior air sacs) is also seen (Forbes,
1991, 1992).
Diagnosis
The signs of aspergillosis are non-specific, making
diagnosis difficult (Dahlhausen et al., 2004). Moreover,
no single test provides certainty. Diagnosis usually relies
upon an accumulation of evidence from the history,
clinical presentation, haematology and biochemistry,
serology, radiographic changes, endoscopy and culture
of the fungus (Jones & Orosz, 2000).
The history of the bird can reveal a stressful event and/
or some underlying environmental factors and/or an
immunosuppressive condition or treatment (Jenkins,
1991). It may also reveal chronic debilitation, voice
change or exercise intolerance (Oglesbee, 1997).
The clinical signs depend on which form of aspergil-
losis the bird develops and which organs are involved
(Jones & Orosz, 2000). Hence, aspergillosis should be
included in the differential diagnosis of respiratory tract
and systemic diseases (Jenkins, 1991; Jones & Orosz,
2000).
Results of haematology and plasma biochemistry can
be considered indicative rather than diagnostic (Jones &
Orosz, 2000). Leukocytosis of 20,000 to more than
100,000 white blood cells per microlitre (Jenkins, 1991;
Oglesbee, 1997), heterophilia with a left shift (degenera-
tive shift), monocytosis and lymphopenia have been
described in aspergillosis cases (Forbes, 1992). In addi-
tion, non-regenerative anaemia, increased total protein
and globulin fraction can be observed (Vanderheyden,
1993; Reidarson & McBain, 1995; Jones & Orosz, 2000).
Acute infections often present an increase in b-globulins,
while chronic infections show an increase in b-globulin
and/or g-globulin fractions. However, immunosup-
pressed birds may have hypoproteinaemia (Ivey, 2000;
Cray et al., 2009a) and white blood cells may be in the
normal range (Flammer & Orosz, 2008). Overall,
changes in protein electrophoresis are non-specific, but
can be useful to estimate disease progression and the
response to therapy (Ivey, 2000; Cray et al., 2009a).
Serological tests have been developed to confirm an
early and more definite diagnosis of aspergillosis (Peden
& Rhoades, 1992). However, in the acute stage, antibody
production trails behind antigen exposure by 10 to 14
days (Brown & Redig, 1994); and if the bird is
immunosuppressed, the low antibody production results
in false negative results (Redig, 1994). In these cases,
detection of circulating Aspergillus antigen in the serum
may be more helpful (Cray et al., 2006). In chronic cases
in which antigen levels may be low, detection of
antibodies may be useful (Jones & Orosz, 2000). A
number of serological test methods have been applied in
birds, including counter-immunoelectrophoresis, agar gel
immunodiffusion and enzyme-linked immunosorbent
assays*but, in general, negative serological tests do
not rule out aspergillosis, and positive tests are only

considered diagnostic when backed up by other evidence
(Peden & Rhoades, 1992; Brown & Redig, 1994; Redig,
1994; Redig et al., 1997; Le Loch et al., 2005; Arca-
Ruibal et al., 2006; Cray et al., 2006, 2009a,b).
Although radiographs may not be helpful, lateral and
ventrodorsal views can be taken in a bird suspected of
having aspergillosis. For those that are unlikely to
survive anaesthesia, standing or perching lateral views
as well as dorsoventral views are helpful (Jones & Orosz,
2000). The radiographic changes of pneumonia and
consolidating airsacculitis are non-specific (McMillan &
Petrak, 1989). Consistent with radiography, computed
tomography scans reveal the extent of lesions*but the
diagnosis of aspergillosis still requires identification by
biopsy, smear or culture (Phalen, 2000).
Endoscopy is invasive and requires anaesthesia, but it
allows the extent of the lesions to be seen as well as the
progress of infection during treatment (Redig, 1994;
Jones & Orosz, 2000). This technique enables evaluation
of the entire respiratory tract. Tracheal endoscopy is
useful for showing a single lesion, such as a thick white
discharge or plaque occluding the trachea or syrinx
(Jenkins, 1991; Marks et al., 1994; Redig, 1994). The
lower respiratory tract is best evaluated by laparoscopy
(Jones & Orosz, 2000). Endoscopy of the abdominal air
sac can show a diffuse cloudiness or white or yellow
plaques. In the event of sporulation, plaques are covered
with greengray pigmented mould. Samples for culture
and cytology should be taken directly with biopsy
forceps or via air sac lavage (Jenkins, 1991; Taylor,
1993; Oglesbee, 1997).
On necropsy, the yellow, green or white granuloma-
tous foci can be noted in chronic aspergillosis patients
(Jenkins, 1991; Vanderheyden, 1993). Acute aspergillosis
causes numerous miliary granulomatous foci (McMillan
& Petrak, 1989; Jenkins, 1991).
Definitive diagnosis requires demonstration of the
presence of the organism by cytology or histopathology
and its identification by culture (Dahlhausen et al.,
2004). It is important to mention that isolation of the
fungus alone does not confirm the infection because
Aspergillus organisms are ubiquitous and can be con-
taminants (Jensen et al., 1997; Flammer & Orosz, 2008).
However, an abundant culture from any organ should be
regarded as diagnostic. On the contrary, a negative
culture does not rule out aspergillosis (Redig, 1994;
Jensen et al., 1997).
Histopathological lesions can be suggestive, but be-
cause in vivo hyphae of hyaline filamentous fungi are
very similar and their in situ manifestations are not
pathognomonic, this technique does not allow fungal
species identification (Kaufman et al., 1997; Cray et al.,
2009a). Thus the aetiological diagnosis should ideally be
confirmed by immunohistochemistry, although few re-
ports on immunohistochemical techniques using mono-
clonal or polyclonal antibodies in birds with aspergillosis
are available (Carrasco et al., 1993; Jensen et al., 1997;
Beytut et al., 2004, Beytut, 2007).
A few reports of different polymerase chain reaction
assays (including real-time polymerase chain reactions)
tested on heparinized whole blood, tracheal washings,
air sac fluids, respiratory tract granulomas, or (biopsy)
tissue samples from birds support the value of this assay
in diagnosing avian aspergillosis (Dahlhausen et al.,
Aspergillus infections in birds 327
2004; Cray et al., 2009a). However, further research is
necessary before such assays can be included in the
work-up of the avian practitioner.
Treatment
Treating avian aspergillosis is a challenge due to a
number of factors. These include the limited knowledge
on the pharmacokinetics of antifungal agents in different
bird species, the granulomatous inflammation that
makes it difficult for the drug to reach the target fungus,
the presence of concurrent disease and/or immunosup-
pression, and the late stage at which birds are usually
presented (McMillan & Petrak, 1989; Flammer, 1993;
Orosz & Frazier, 1995). The best way to overcome the
disease is topical therapy after removing the granuloma-
tous tracheal lesions by suction (Westerhof, 1995), and
this can be used in combination with an early, aggressive
systemic antifungal therapy. In most birds, however,
granulomatous lesions are difficult to remove because of
their location within the respiratory system and because
of the risk of surgical trauma and anaesthesia (Hernan-
dez-Divers, 2002). Hence, in most cases, only antifungal
therapy is applied. Topical therapy can be administered
by nebulization, nasal or air sac flushing, or surgical
irrigation of the abdominal cavities (Bauck et al., 1992;
Oglesbee, 1997; Abrams et al., 2001), while systemic
therapy can be administered intravenously and orally.
The role and prevalence of acquired resistance to
antifungal drugs as a potential contributing factor is
not well known. Since drug resistance has been increas-
ingly reported in human medicine (Snelders et al., 2008),
standardized susceptibility testing is also becoming
necessary in avian medicine. Literature regarding in vitro
susceptibilities of antifungal agents for avian A. fumigatus
strains in birds is scarce. The minimal inhibitory concen-
tration of thiabendazole, 5-fluorocytosine, fluconazole,
ketoconazole, caspofungin, amphotericin B, itraconazole
and voriconazole for a limited number of A. fumigatus
strains isolated from raptors has been determined using
non-standardized methods (Redig & Duke, 1985; Silva-
nose et al., 2006, 2009). Currently, a reference method is
available to test the antifungal susceptibility of filamen-
tous fungi (Clinical and Laboratory Standards Institute
document M38-A2), thus solving the lack of standardiza-
tion. Using this method, the in vitro susceptibility of 59
avian A. fumigatus strains against amphotericin B,
itraconazole and voriconazole has been determined.
Four isolates showed acquired resistance to both itraco-
nazole and voriconazole, a fact that may harbour
implications for the treatment (Beernaert et al., 2009c).
Specific drug properties, toxicity and dose regimens of
a number of antifungal drug classes commonly applied
in avian aspergillosis are summarized in Table 1.
Prevention
Protective immunity following vaccination is thought to
be useful in treating and preventing avian aspergillosis.
However, attempts to devise vaccination strategies
appear questionable in immunosuppressed animals that
would need passive immunization with immunoglobulins
(Schmidt, 2002). Nevertheless, a number of different
328 L. A. Beernaert et al.

Table 1. Summary of the administration routes and doses of antifungal agents used for avian aspergillosis.

Antifungal agent Administration route Dose

Amphotericin B Intravenous 1.5 mg/kg qa8 h 3 to 5 days (Flammer, 1993; Joseph et al., 1994), 10 to 14 days (Jenkins, 1991)
Intratracheal 1.5 mg/kg q8 to 12 h (raptors) (Redig & Duke, 1985)
Nebulization 1 mg/kg q24 h 10 to 14 days (Jenkins, 1991), q12 h (raptors) (Joseph et al., 1994)
Into air sac 1 mg/ml 15 min 5 to 7 days every other week (Orosz & Frazier, 1995), q12 h (Joseph
et al., 1994)
Topical (wound) Dose not specified (Flammer, 1993)
1.35 mg/kg q24 h (liposomally encapsulated amphotericin B) (Bonar & Lewandowski, 2004)
Clotrimazole Topical Dose not specified (Flammer, 1993)
Nebulization 10 mg/ml polyethylene glycol for 30 to 45 min q24 h 3 days on/2 days off (1 to 4 months) (Joseph
et al., 1994; Orosz & Frazier, 1995)
Enilconazole Topical Dose not specified (Flammer, 1993)
Nebulization 0.1 ml/kg for 30 min q24 h 5 days on/2 days off (raptors) (Heatly et al., 2007)
Disinfection Environment: flush with solutions as recommended for use in poultry houses (Flammer, 1993)
Fluconazole Oral, intravenous 5 mg/kg q24 h 7 days (Bauck et al., 1992; Flammer, 1993)
15 mg/kg q12 h (psittacines) (Pericard, 2005)
Itraconazole Oral 5 to 15 mg/kg q12 h with food for 7 to 21 days (Bauck et al., 1992)
10 mg/kg q24 h 3 weeks (Verstappen & Dorrestein, 2005) (falcons) (Jones et al., 2000)
15 mg/kg per orally q12 h/q24 h (Abrams et al., 2001), 10 to 20 mg/kg q12 h/q24 h (Flammer,
1993)
5 mg/kg q24 h 30 days (African grey parrots) (Orosz & Frazier, 1995)
5 to 10 mg/kg q24 h (Amazon parrots) (Orosz et al., 1996), 6 mg/kg q12 h (pigeons) (Lumeij
et al., 1995)
Preventive: 10 mg/kg q24 h 10 days (Forbes, 1992), 20 mg/kg q24 h (Meredith, 1997), 15 to
25 mg/kg/day for 1 week (Xavier, 2008)
Ketoconazole Oral 10 to 30 mg/kg q12 h 21 days (resuspending in orange juice q5 days) (Bauck et al., 1992)
20 to 30 mg/kg q12 h (Flammer, 1993), 30 mg/kg q12 h 14 to 30 days (Orosz & Frazier, 1995)
Miconazole Topical q12 h (Flammer, 1993; Orosz & Frazier, 1995; Abrams et al., 2001; Suedmeyer et al., 2002)
Nebulization pH balanced solution, aqueous base, dilute in saline: 15 to 20 min q12 h (Orosz & Frazier, 1995)
Intratracheal 5 mg/kg, 10 mg/ml, q12 h (diluted to maximum 0.5 ml with saline) (Westerhof, 1995)
Terbinafine Oral 10 mg/kg q12 h to q24 h, 15 mg/kg q12 h (psittacines) (Flammer & Orosz, 2008)
Nebulization Can be combined with itraconazole (Flammer, 2006). Dose not mentioned
Voriconazole Oral 10 mg/kg q12 h (pigeon) (Beernaert et al., 2009a,b), q24 h (chickens) (Burhenne et al., 2008)
(African grey parrots) (Scope et al., 2007)
12 to 18 mg/kg q12 h (African grey parrots) (Flammer & Orosz, 2008)
12.5 mg/kg q12 h, 3 days loading dose, then q24 h (raptors) (Di Somma et al., 2007; Schmidt
et al., 2007)
40 mg/kg q24 h (quails) (Tell et al., 2009)
5-fluorocytosine Oral 50 to 100 mg/kg q12 h (Flammer, 1993)
60 to 250 mg/kg q12 h (cage birds); 40 mg/kg q6 to 8 h (raptors) (Jenkins, 1991)
150 to 250 mg/kg q12 h 21 days (Bauck et al., 1992)
120 mg/kg q12 h 3 weeks (Westerhof, 1995)
75 to 120 mg/kg q24 h (dose/4 q6 h) (Redig & Duke, 1985)
120 mg/kg q6 h (Joseph et al., 1994)

a
Every.

vaccination strategies have been attempted in birds using
different vaccine preparations, but with inconsistent
results (Richard et al., 1991; Bauck et al., 1992;
Meredith, 1997). Future knowledge regarding virulence
factors and the role of cellular immunity in avian
aspergillosis may contribute to newer and more effective
vaccination strategies.
The use of immune stimulants has been suggested
(Jenkins, 1991). Levamisole, a derivative of imidazothia-
zole, has been found to possess an immunostimulant
effect as an adjunct in the treatment of chronic infec-
tions. However, levamisole did not decrease aspergillosis-
associated lesions in turkeys (Perelman, 1993). In
humans, clinical improvement of aspergillosis has been
documented after the addition of interferon-g and
granulocytemacrophage colony-stimulating factor to
the antifungal treatment (Bandera et al., 2008). Whether
the favourable effect of interferon-g and granulocyte
macrophage colony-stimulating factor could also play a
role in future treatment protocols for avian aspergillosis
needs to be investigated.
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