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Jacques Guillot, Guillaume Le Loc’h, Pascal Arné,Françoise Féménia, René Chermette
AvianAvianaspergillosisaspergillosis
UMR INRA, AFSSA, ENVA, UPVM 956, Biologie Moléculaire et Immunologie Parasitaires et Fongiques, Ecole Nationale Vétérinaire d’Alfort, 94704 Maisons-Alfort Cedex, France
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IntroductionIntroduction
Aspergillosis is considered as one of the most important infectious diseases in birds
• • early 1800s: first observationsearly 1800s: first observationsscaup duck, jay, bullfinch, bustard and several swansscaup duck, jay, bullfinch, bustard and several swans
• • 1898: first cases in turkey poults 1898: first cases in turkey poults (Lignières & Petit in France)(Lignières & Petit in France)
• • Since then, cases in a very wide range of avian species…Since then, cases in a very wide range of avian species…
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5 key questions…5 key questions…
Why are birds more susceptible than mammals ? Why are birds more susceptible than mammals ?
In which circumstances does aspergillosis occur in birds ? In which circumstances does aspergillosis occur in birds ?
Is it possible to make an early diagnosis in birds ? Is it possible to make an early diagnosis in birds ?
Is it possible to treat or prevent avian aspergillosis ? Is it possible to treat or prevent avian aspergillosis ?
What do the main clinical signs and lesions look like ? What do the main clinical signs and lesions look like ?
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Susceptibility of birdsSusceptibility of birds
Birds are much more susceptible to aspergillosis than mammalian species
• • Environmental contamination by Environmental contamination by AspergillusAspergillus spp. spp.
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Susceptibility of birdsSusceptibility of birds
• • Environmental contamination by Environmental contamination by AspergillusAspergillus spp. spp.• • Avian anatomy and physiologyAvian anatomy and physiology
40-43°C40-43°C
Birds are much more susceptible to aspergillosis than mammalian species
lungslungs / / air sacsair sacs
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Susceptibility of birdsSusceptibility of birds
• • Environmental contamination by Environmental contamination by AspergillusAspergillus spp. spp.• • Avian anatomy and physiologyAvian anatomy and physiology• • Avian immunologyAvian immunology
Lack of resident macrophages in airways and air sacs
Heterophils without peroxydation
Birds are much more susceptible to aspergillosis than mammalian species
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EpidemiologyEpidemiology
Aspergillus fumigatus / Aspergillus flavus, Aspergillus niger…
OvergrowthOvergrowth
Specific virulence factors ?Specific virulence factors ?
humidity, dampnesshumidity, dampnessdrying period …drying period …
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EpidemiologyEpidemiology
• • a 600 ma 600 m22 confinement building in the Center of France confinement building in the Center of France
• • a flock comprising 4500 turkeysa flock comprising 4500 turkeys females slaughtered at the age of 12 w and males at the age of 16 wfemales slaughtered at the age of 12 w and males at the age of 16 w
Genotyping of environmental Genotyping of environmental and clinical and clinical A. fumigatusA. fumigatus
isolatesisolates
(2 microsatellite markers)(2 microsatellite markers)Bart-Delabesse Bart-Delabesse et alet al. J. Clin. Microbiol. 1998. J. Clin. Microbiol. 1998
An epidemiological survey was conducted in France
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EpidemiologyEpidemiology
0255075
100125150
3 4 5 6 7 8 9 10 11 12 13 14 15 16
Aspergillus flavus Aspergillus fumigatus Other fungi
Lair-Fulleringer et al. Poultry Science 2006
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EpidemiologyEpidemiology
5 males5 males 5 females5 females
10 healthy chicks, 23 isolates,1 unique genotype
Lair-Fulleringer et al. J. Clin. Microbiol. 2003
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EpidemiologyEpidemiology
9 healthy turkeys, 55 isolates, 17 genotypes9 healthy turkeys, 55 isolates, 17 genotypes
Lair-Fulleringer et al. J. Clin. Microbiol. 2003
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EpidemiologyEpidemiology
2 carcass condemnations, 36 isolates, 2 genotypes
Lair-Fulleringer et al. J. Clin. Microbiol. 2003
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EpidemiologyEpidemiology
362 air samples, 134 isolates 53 genotypes
16 week-sampling periodLair-Fulleringer et al. Poultry Science 2006
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EpidemiologyEpidemiology
Aspergillus fumigatus / Aspergillus flavus, Aspergillus niger…
OvergrowthOvergrowthSpecific virulence factors ?Specific virulence factors ?
• • SpeciesSpecies
• • Avian strainsAvian strains• • Individual susceptibility ?Individual susceptibility ?• • AgeAge• • SexSex
• • StressStress
• • Other micro-organismsOther micro-organisms
• • ToxicosisToxicosis
• • TherapeuticsTherapeutics
captive environmentcaptive environmenthandlinghandlingmigration…migration…
mycotoxins ?mycotoxins ?
corticosteroidscorticosteroids
turkeys, quails, turkeys, quails, raptors, penguins, raptors, penguins, parrots, waterfowlparrots, waterfowl
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Clinical signs and lesionsClinical signs and lesions
Different avian speciesDifferent epidemiological situations Many clinical signs
Acute aspergillosisAcute aspergillosis = inappetance, depression, polydipsia, polyuria, dyspnoea, cyanosis= sometimes, sudden death without any signs
Chronic aspergillosisChronic aspergillosis = signs are dependent on the area of invasion
change in voicerespiratory stridorexercice intoleranceataxia, torticollis, seizuresconjunctivitis, keratitisbeak malformation…
fatal evolution
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Clinical signs and lesionsClinical signs and lesions
ENVA
Kaminski et al.
air sacculitis
Aspergillosisof eggs
ENVA
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Clinical signs and lesionsClinical signs and lesions
Chute
pneumonia
meningo-encephalitis
Séguin
arthritis
Séguin
uveitis
Séguin
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DiagnosisDiagnosisFalcons, parrots, wild birds in zoological or rehabilitation centers
Clinical signsEpidemiologyRadiologyRadiologyEndoscopyEndoscopyHematologyHematology
SerologySerology
BiochemistryBiochemistryElectrophoresisElectrophoresis
Mycological cultureMycological culture
PCR ?PCR ?
Cytology, histologyCytology, histology
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DiagnosisDiagnosis
Clinical signsEpidemiologyRadiologyRadiologyEndoscopyEndoscopyHematologyHematology
SerologySerology
Juliet Joseph, Abu Dhabi Falcon Research Hospital
Falcons, parrots, wild birds in zoological or rehabilitation centers
BiochemistryBiochemistryElectrophoresisElectrophoresis
Mycological cultureMycological culture
PCR ?PCR ?
Cytology, histologyCytology, histology
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HematologyHematology
DiagnosisDiagnosis
Clinical signsEpidemiologyRadiologyRadiologyEndoscopyEndoscopy
SerologySerology
Falcons, parrots, wild birds in zoological or rehabilitation centers
BiochemistryBiochemistryElectrophoresisElectrophoresis
Mycological cultureMycological culture
PCR ?PCR ?
Cytology, histologyCytology, histology
a promising approach ?
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DiagnosisDiagnosis
SerologySerology
• • Immunologically, birds respond to Immunologically, birds respond to AspergillusAspergillus infection in infection in the same way as mammals and a type I response appears the same way as mammals and a type I response appears most beneficialmost beneficial
• • Birds also respond with specific antibody production Birds also respond with specific antibody production similar in its kinetics to mammalssimilar in its kinetics to mammals
• • Serological tests that may be used in birds include the Serological tests that may be used in birds include the detection of specific antibodies or fungal antigensdetection of specific antibodies or fungal antigens
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DiagnosisDiagnosis
SerologySerology detection of specific antibodies
False negative results False negative results some birds may not be able to mount an appropriate responsesome infection locations result in limited antigenic stimulation
Antibody titers not necessary correlated to clinical severityAntibody titers not necessary correlated to clinical severity
High prevalence of seropositivity in captive penguinsLow prevalence of seropositivity in wild birds
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DiagnosisDiagnosis
SerologySerology detection of galactomannan
• agglutination (Pastorex Aspergillus®)
• monoclonal sandwich ELISA (Platelia Aspergillus®)
• polyclonal sandwich ELISA
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DiagnosisDiagnosis
SerologySerology detection of galactomannan
Cray et al. ISHAM 2006 (poster P-0011)
839 serum samples (from suspected or confirmed cases)
Galactomannan in 50% of samples from penguinsin 25% of samples from other birds
Many chronic cases = negative for antibody but positive for galactomannanBut long term chronic cases = negative for both antigen and antibody !
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DiagnosisDiagnosis
SerologySerology detection of galactomannan
Arca-Ruiba et al. Vet. Rec. 2006
90 serum samples (from cases in falcons)182 control serum samples (from healthy falcons)
Galactomannan in 12% of samples from infected falconsin 5% of samples from healthy birds
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DiagnosisDiagnosis
SerologySerology detection of galactomannan
Le Loch’ et al. ISHAM 2006 (poster))
Platelia® Aspergillus
+ -
CIE+ 17 39 56
- 20 65 85
37 104 141
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DiagnosisDiagnosis
SerologySerology detection of galactomannan
Many false negative results Many false negative results variable release of GMvariable kinetics
according to avian species according to physiological status of each birdaccording to the level of immune complexing
Some false positive results Some false positive results circulating GM from other fungicross reactivity with bacterial components (food supplementation ?)
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SerologySerology
HematologyHematology
DiagnosisDiagnosis
Clinical signsEpidemiologyRadiologyRadiologyEndoscopyEndoscopy
Falcons, parrots, wild birds in zoological or rehabilitation centers
BiochemistryBiochemistryElectrophoresisElectrophoresis
Mycological cultureMycological culture
PCR ?PCR ?
Cytology, histologyCytology, histology
Hardy et al. AAV proc. 2003Dahlahausen et al. AAV proc. 2004
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DiagnosisDiagnosis
Clinical signsEpidemiology
Turkeys, chickens, quails, ducks, ostriches…
HematologyHematology
RadiologyRadiologyEndoscopyEndoscopy
SerologySerology
BiochemistryBiochemistryElectrophoresisElectrophoresis
Mycological cultureMycological culture
NecropsyNecropsy
Cytology, histologyCytology, histology
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TreatmentTreatmentFalcons, parrots, wild birds in zoological or rehabilitation centers
Amphothericin BAmphothericin BFlucytosineFlucytosine
KetoconazoleKetoconazole
ItraconazoleItraconazole
TerbinafineTerbinafineVoriconazole (Langhofer, AAV proc. 2004)Voriconazole (Langhofer, AAV proc. 2004)
Radiography, endoscopy or serology for the follow up
+ Supportive therapy + Surgical debridement of the lesions
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TreatmentTreatment
No treatment !
Turkeys, chickens, quails, ducks, ostriches…
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PreventionPrevention
• Reduction of fungal contamination
• Chimioprevention ?
Vaccination with a heat-killed culture filtrate preparation has been reported Vaccination with a heat-killed culture filtrate preparation has been reported to reduce mortality in ducks and waterfowlto reduce mortality in ducks and waterfowl
• Reduction of stress
• Vaccination
Richard (1984) reduced mortalities by 50% in turkey poults vaccinated with Richard (1984) reduced mortalities by 50% in turkey poults vaccinated with germinated germinated A. fumigatusA. fumigatus conidia conidia
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ConclusionsConclusions
« Avian aspergillosis »« Avian aspergillosis » = not a single entity but a complex of several diseases… = not a single entity but a complex of several diseases…
• • importance of prophylactic procedures importance of prophylactic procedures
• • poor prognosispoor prognosis
• • need for specific avian models of aspergillosisneed for specific avian models of aspergillosis
• • variable epidemiological situationsvariable epidemiological situations
• • several diagnostic tools requiredseveral diagnostic tools required
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ReferencesReferencesCray, C., Rodriguez, M. & Watson, T. (2006) Aspergillus serodiagnostics in avian species. 16th Congress of the
International Society for Human and Animal Mycology (ISHAM), June 25-29th 2006, Paris (Poster).Harmon, B. (1998). Avian heterophils in inflammation and disease resistance. Poultry Science, 77, 972-977.Kearns, K.L. (2003). Avian aspergillosis. In: Recent advances in avian infectious diseases. Kearns KS, Loudis B
(Eds). Ithaca, International Information Service.Klika, E., Scheuermann, D.W., De Groodt-Lasseel, M.H.A., Bazantova, I. & Switka, A. (1996). Pulmonary macrophages
in birds (barn owl, Tyto tyto alba), domestic fowl (Gallus gallus domestica), quail (Coturnix coturnix) and pigeon (Columbia livia). Anatomy Record, 246, 87-97.
Kunkle, R.A. & Rimler, R.B. (1996). Pathology of acute aspergillosis in turkeys. Avian Diseases, 40, 875-886.Lair-Fulleringer, S., Guillot, J., Desterque, C., Seguin, D., Warin, S., Chermette, R. & Bretagne, S. 2003. Differentiation
of Aspergillus fumigatus isolates from breeding turkeys and their environment by genotyping with microsatellite markers. Journal of Clinical Microbiology, 41, 1798-1800.
Le Loc’h, G., Arné, P., Bougerol, C., Risi, E., Péricard, J.M., Quinton, J.F., Bretagne, S. & Guillot, J. (2006) Detection of circulating serum galactomannan for the diagnosis of avian aspergillosis. 16th Congress of the International Society for Human and Animal Mycology (ISHAM), June 25-29th 2006, Paris (Poster).
Morris, M.P. & Fletcher, O.J. (1988). Disease prevalence in Georgia turkey flocks in 1986. Avian Diseases, 32, 404-406.
Peden, W.M. & Rhoades, K.R. (1992). Pathogenicity differences of multiple isolates of Aspergillus fumigatus in turkeys. Avian Diseases, 36, 537-542.
Redig, P.T., Post, G.S., Concannon, T.M. & Dunette, J. (1986). Development of an ELISA for the detection of aspergillosis in avian species. Proceedings of the Association Avian Veterinarians, 165-178.
Redig, P.T. (1993). Avian aspergillosis. In: Fowler ME (Ed) Zoo and wild animals medicine. WB. Saunders Company, Philadelphia, 178-181.
Richard, J.L. (1997). Aspergillosis. In: Diseases of poultry. Calmek B.W. (Ed), Mosby-Wolfe, London, 351-365.Taylor, J.J. & Burroughs, E.J. (1973). Experimental avian aspergillosis. Mycopathologia Mycologia Applicata, 51, 131-
141.Tell, L.A. (2005). Aspergillosis in mammals and birds: impact in veterinary medicine. Medical Mycology, 43, S71-S73.