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Molecular detection, risk factors and public awareness of avian bornavirus among captive and non-captive birds in Peninsular Malaysia

Syamsiah Mohd Lutpi
Syamsiah Mohd Lutpi
, 
Jalila Abu
Jalila Abu
, 
Siti Suri Arshad
Siti Suri Arshad
 y 
Nor Yasmin Rahaman
Nor Yasmin Rahaman
   | 21 dic 2022
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Publicado en línea: 21 dic 2022
Páginas: 523 - 535
Recibido: 23 mar 2022
Aceptado: 26 oct 2022
DOI: https://doi.org/10.2478/jvetres-2022-0061
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© 2022 S.M. Lutpi et al. published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Fig. 1

Peninsular Malaysia sampling locations for waterfowl (A) and pet birds (B) where cloacal swabs or faeces were taken for molecular detection by RT-PCR
Peninsular Malaysia sampling locations for waterfowl (A) and pet birds (B) where cloacal swabs or faeces were taken for molecular detection by RT-PCR

Fig. 2

Agarose gel electrophoresis result in pet birds using avian bornavirus (ABV) M primers yielding an expected PCR product of 350 bp. Lane 1 – 50 bp DNA ladder; Lane 2 – negative control; Lane 3 – positive control; Lanes 4-6 – ABV-positive; Lanes 7 and 8 – ABV-negative
Agarose gel electrophoresis result in pet birds using avian bornavirus (ABV) M primers yielding an expected PCR product of 350 bp. Lane 1 – 50 bp DNA ladder; Lane 2 – negative control; Lane 3 – positive control; Lanes 4-6 – ABV-positive; Lanes 7 and 8 – ABV-negative

Fig. 3

Agarose gel electrophoresis result in waterfowl using avian bornavirus (ABV) M primers yielding an expected PCR product of 350 bp. Lane 1 – 50 bp DNA; Lane 2 – negative control; Lane 3 – positive control; Lanes 4-17 – ABV-negative
Agarose gel electrophoresis result in waterfowl using avian bornavirus (ABV) M primers yielding an expected PCR product of 350 bp. Lane 1 – 50 bp DNA; Lane 2 – negative control; Lane 3 – positive control; Lanes 4-17 – ABV-negative

Fig. 4

Phylogenetic tree using maximum likelihood tree building based on the partial M gene (350 bp). The tree was constructed based on reference sequences stored in the GenBank database. Sequences emphasised in the box were this study’s ABV-positive samples
Phylogenetic tree using maximum likelihood tree building based on the partial M gene (350 bp). The tree was constructed based on reference sequences stored in the GenBank database. Sequences emphasised in the box were this study’s ABV-positive samples

Knowledge of the participants about avian bornavirus (ABV) and proventricular dilatation disease (PDD)

Yes No I don’t know
ABV and PDD knowledge items n (%) n (%) n (%)
Had you ever heard about ABV before? 62 (39.2) 96 (60.8) 0 (0)
Had you ever heard about PDD before? 103 (65.2) 55 (34.8) 0 (0)
PDD is caused by ABV 56 (35.4) 0 (0) 102 (64.6)
It is a fatal disease that can affect mainly the neurological and digestive systems of the bird 82 (51.9) 0 (0) 76 (48.1)
Common species affected by ABV are domestic birds (e.g.: macaws, cockatoos, and cockatiels) and waterfowl (e.g.: ducks, swans, and geese) 68 (43) 4 (2.5) 86 (54.4)
The main signs and symptoms of birds affected by ABV are a reduced appetite, dilatation of the proventriculus, ventriculus or intestines, passage of undigested seeds in the faeces and seizures 56 (35.4) 2 (1.3) 100 (63.3)
ABV is intermittently shed in faeces and urates 36 (22.8) 4 (2.5) 118 (74.7)
ABV can be transmitted by healthy birds without the birds showing any clinical signs 46 (29.1) 0 (0) 112 (70.9)
ABV can be prevented by minimising stress through providing good nutrition and practising good husbandry 78 (49.4) 4 (2.5) 76 (48.1)

Practices of the participants with respect to avian bornavirus and proventricular dilatation disease

ABV and PDD practices Agree Disagree Not sure
n (%) n (%) n (%)
Provide good nutrition with an adequate amount of feed 148 (93.7) 0 (0) 10 (6.3)
Provide good husbandry and adequate ventilation 152 (96.2) 0 (0) 6 (3.8)
Wash hands between handlings of birds 150 (94.9) 0 (0) 8 (5.1)
Use a footbath or disinfect shoes when going from one place to another 138 (87.3) 2 (1.3) 18 (11.4)
Properly clean cages and dispose of bird faeces 154 (97.5) 0 (0) 4 (2.5)
Carry out regular health checks on birds 140 (88.6) 0 (0) 18 (11.4)
Quarantine or isolate if a bird shows signs inviting suspect of PDD 154 (97.5) 0 (0) 4 (2.5)
Quarantine and carry out a health check on a new bird 152 (96.2) 0 (0) 6 (3.8)
Seek veterinarian advice if bird is suspected of having PDD 150 (94.9) 2 (1.3) 6 (3.8)

Prevalence (%) of avian bornavirus in pet birds and waterfowl

Category Order Family Genus/species Common name No. of tested birds RT-PCR positive birds RT-PCR negative birds
Ara ararauna Blue and gold macaw 13 2 11
Psittacus erithacus African grey parrot 7 0 7
Psittacidae Amazona sp. Amazon parrot 3 1 2
Aratinga solstitialis Sun conure 10 0 10
Pyrrhura molinae Green-cheeked conure 30 4 26
Pionus menstruus Blue-headed pionus 1 0 1
Nymphicus hollandicus Cockatiel 12 1 11
Cacatua galerita Sulphur-crested cockatoo 14 0 14
Psittaciformes Cacatuidae Cacatua alba Umbrella cockatoo 1 0 1
Cacatua moluccensis Salmon-crested cockatoo 1 0 1
Probosciger aterrimus Black palm cockatoo 1 0 1
Chalcopsitta atra Black lory 1 0 1
Pet birds Melopsittacus undulatus Budgerigar 15 0 15
Psittaculidae Eclectus roratus Eclectus parrot 10 0 10
Trichoglossus moluccanus Rainbow lorikeet 9 1 8
Agapornis personatus Yellow-collared lovebird 10 0 10
Psittacula krameria Ring-necked parakeet 12 0 12
Taeniopygia guttata Zebra finch 24 0 24
Estrildidae Chloebia gouldiae Gouldian finch 3 0 3
Lonchura oryzivora Java finch 3 0 3
Passeriformes Fringillidae Serinus canaria f. domestica Domestic canary 9 0 9
Corvidae Copsychus saularis Oriental magpie-robin 4 0 4
Pycnonotidae Pycnonotus jocosus Red-whiskered bulbul 7 0 7
Sturnidae Acridotheres tristis Indian mynah 1 0 1
Total 201 9 (4.5%) 192
Anas platyrhynchos Pekin duck 72 0 72
Anas platyrhynchos Khaki Campbell 30 0 30
Anas platyrhynchos Domestic duck 17 0 17
Anatidae Cairina moschata Muscovy duck 2 0 2
Waterfowl Anseriformes Cygnus atratus Black swan 3 0 3
Alopochen aegyptiaca Egypt goose 8 0 8
Anser domesticus Domestic goose 9 0 9
Cygnus cygnus Whooper swan 2 0 2
Total 143 0 (0%) 143

Association between knowledge, attitude and practice scores

Variable Correlation coefficient P-value
Knowledge-attitude 50.058 0.000
Knowledge-practice 0.239 0.625
Attitude-practice 4.519 0.034

Socio-demographic characteristics of study population

n (/158) Percentage (%)
18-30 36 22.8
Age 31-40 41-50 98 20 62 12.7
51-60 4 2.5
Male 136 86.1
Gender Female 22 13.9
Malay 130 82.3
Chinese 16 10.1
Race Indian 10 6.3
Others 2 1.3
No formal education 0 0
Primary school 4 2.5
Education Secondary school Matriculation/foundation/college 44 28 27.8 17.7
University (bachelor, masters, doctorate) 74 46.8
Others 8 5.1
Characteristic Government 38 24.1
Occupation Private 64 40.5
Self-employed 44 27.8
Others 12 7.6
n (/62)
Veterinarian 16 25.8
Brochures, posters and other printed materials 0 0
Source of ABV information Internet, blog, website, social, media, Facebook 28 45.2
Family, friends, neighbours and colleagues 18 29
Others 0 0
n (103)
Veterinarian 19 18.4
Brochures, posters and other printed materials 0 0
Source of PDD information Internet, blog, website, social, media, Facebook 70 68
Family, friends, neighbours and colleagues 14 13.6
Others 0 0

Pet bird species and number of faeces samples collected in different locations from 2019 to 2021

Date Location Pet bird species Age Management (group or individual/pair) Number of faeces samples collected
Ara ararauna (Blue and gold macaw) Juvenile Individual/pair 1
Aratinga solstitialis (Sun conure) Juvenile Individual/pair 1
27 November 2019 Serdang, Selangor
Chalcopsitta atra (Black lory) Adult Individual/pair 1
Pyrrhura molinae (Green-cheeked conure) Juvenile Individual/pair 1
Total 4
Taeniopygia guttata (Zebra finch) Adult Group 18
Chloebia gouldiae (Gouldian finch) Adult Individual/pair 1
Nymphicus hollandicus (Cockatiel) Juvenile Individual/pair 1
28 November 2019 Serdang, Selangor Nymphicus hollandicus (Cockatiel) Adult Group 7
Serinus canaria f. domestica (Domestic canary) Adult Individual/pair 8
Melopsittacus undulatus (Budgerigar) Adult Individual/pair 1
Copsychus saularis (Magpie-robin) Adult Individual/pair 4
Pycnonotus jocosus (Red-whiskered bulbul) Adult Group 4
Total 44
Pionus menstruus (Blue-headed pionus) Adult Individual/pair 1
Eclectus roratus (Eclectus parrot) Adult Individual/pair 1
Cacatua galerita (Sulphur crusted cockatoo) Adult Individual/pair 3
20 January 2020 Klang, Selangor
Taeniopygia guttata (Zebra finch) Adult Group 6
Lonchura oryzivora (Java finch) Adult Group 3
Chloebia gouldiae (Gouldian finch) Adult Group 2
Total 16
Nymphicus hollandicus (Cockatiel) Adult Group & indiv/pair 2
18 August 2020 Ampang, Selangor Melopsittacus undulatus (Budgerigar) Juvenile Group 6
Melopsittacus undulatus (Budgerigar) Adult Group & indiv/pair 8
Total 16
Cacatua galerita (Sulphur-crested cockatoo) Juvenile Individual/pair 2
Pyrrhura molinae (Green-cheeked conure) Adult Individual/pair 6
Aratinga solstitialis (Sun conure) Adult Individual/pair 1
12 September 2020 Seberang Prai, Pulau Pinang Trichoglossus moluccanus (Rainbow lorikeet) Adult Individual/pair 4
Eclectus roratus (Eclectus parrot) Juvenile Individual/pair 1
Agapornis personatus (Yellow-collared lovebird) Adult Group & indiv/pair 10
Psittacula krameria (Ring-necked parakeet) Adult Individual/pair 8
Total 32
Ara ararauna (Blue and gold macaw) Adult Individual/pair 7
Cacatua galerita (Sulphur-crested cockatoo) Adult Individual/pair 6
Cacatua alba (Umbrella cockatoo) Adult Individual/pair 1
Cacatua moluccensis (Salmon-crested cockatoo) Adult Individual/pair 1
Psittacus erithacus (African grey parrot) Adult Individual/pair 4
24 September 2020 Kuala Lumpur Amazona sp. (Amazon parrot) Adult Individual/pair 2
Aratinga solstitialis (Sun conure) Adult Group & indiv/pair 5
Aratinga solstitialis (Sun conure) Juvenile Group 1
Eclectus roratus (Eclectus parrot) Adult Individual/pair 4
Trichoglossus moluccanus (Rainbow lorikeet) Adult Individual/pair 1
Acridotheres tristis (Indian mynah) Adult Group 1
Pycnonotus jocosus (Red-whiskered bulbul) Adult Group 3
Total 36
28 September 2020 Ipoh, Perak Ara ararauna (Blue and gold macaw) Juvenile Individual/pair 1
Total 1
Pyrrhura molinae (Green-cheeked conure) Group & indiv/pair 16
Adult
Pyrrhura molinae (Green-cheeked conure) Individual/pair 7
Juvenile
Trichoglossus moluccanus (Rainbow lorikeet) Individual/pair 4
2 October 2020 Pasir Puteh, Kelantan Adult
Psittacus erithacus (African grey parrot) Individual/pair 2
Adult
Amazona sp. (Amazon parrot) Individual/pair 1
Adult
Psittacula krameria (Ring-neck parakeet) 2
Total 32
16 November 2020 Serdang, Selangor Ara ararauna (Blue and gold macaw) Adult Individual/pair 1
Ara ararauna (Blue and gold macaw) Juvenile Individual/pair 1
Total 2
Ara ararauna (Blue and gold macaw) Adult Individual/pair 1
Probosciger aterrimus (Black palm cockatoo) Adult Individual/pair 1
Cacatua galerita (Sulphur crested cockatoo) Adult Individual/pair 3
25 November 2020 Gombak, Selangor Psittacus erithacus (African grey parrot) Adult Individual/pair 1
Eclectus roratus (Eclectus parrot) Adult Individual/pair 3
Eclectus roratus (Eclectus parrot) Juvenile Individual/pair 1
Psittacula krameria (Ring-necked parakeet) Adult Individual/pair 2
Aratinga solstitialis (Sun conure) Adult Individual/pair 2
Total 14
Ara ararauna (Blue and gold macaw) Adult Individual/pair 1
9 March 2021 Rawang, Selangor Nymphicus hollandicus (Cockatiel) Adult Individual/pair 2
Serinus canaria f. domestica (Domestic canary) Adult Individual/pair 1
Total 4
All-location total 201

Waterfowl species and number of swabs collected in different locations from 2019 to 2021

Date Location Waterfowl species Age Management (group or individual/pair) Number of swabs collected
2 February 2019 Kampar, Perak Anas platyrhynchos (Pekin duck) Adult Group 35
Bidor, Perak Anas platyrhynchos (Pekin duck) Adult Group 37
12 October 2019 Kuala Pilah, Negeri Sembilan Anas platyrhynchos (Khaki Campbell) Adult Group 30
Anas platyrhynchos (domestic duck) Adult Group 14
9 December 2020 Putrajaya Cairina moschata (Muscovy duck) Adult Group 2
Cygnus atratus (black swan) Adult Group 3
Alopochen aegyptiaca (Egypt goose) Adult Group 8
Anser anser domesticus (Domestic Adult Group 9
12 March 2021 Klang, Selangor goose) Cygus cygus (White swan) Adult Group 2
Anas platyrhynchos (Domestic duck) Adult Group 3
Total 143

Association between ABV-positivity and potential risk factors estimated by binary logistic regression

Total Prevalence of ABV (%) P-value Odd ratio 95% confidence interval
Category Pet birds Waterfowl 201 143 4.5 (9/201) 0 (0/143) 0.010 1.7 NA 1.591–1.914 NA
Psittacidae 46 10.6 (7/66) 0.844 0.7 0.075–6.471
Family Cacatuidae 11 1.5 (1/66) 1.3 0.067–23.259
Psittaculidae 9 1.5 (1/66) Ref Ref
Ara ararauna 13 3 (2/66) 0.867 0.7 0.053–8.960
Amazona sp. 3 1.5 (1/66) 0.3 0.010–5.985
Species Pyrrhura molinae 30 6.1 (4/66) 0.8 0.079–8.352
Factor Nymphicus hollandicus 11 1.5 (1/66) 1.3 0.067–23.259
Trichoglossus moluccanus 9 1.5 (1/66) Ref Ref
Age Adult Juvenile 177 24 3 (6/201) 1.5 (3/201) 0.043 4.1 Ref 0.947–17.499 Ref
East coast 32 3 (6/201) 0.000 0.1 0.012–0.388
Region North 33 0.5 (1/201) 0.5 0.042–5.432
Central 136 1 (2/201) Ref Ref
Management Group Individual/pair 75 126 2.5 (5/201) 2 (4/201) 0.247 0.5 Ref 0.119–1.766 Ref

Attitude of the participants toward ABV and PDD

ABV and PDD attitude criterion Yes No I don’t know
N (%) N (%) N(%)
Do you think PDD is a fatal bird disease? 90 (57) 4 (2.5) 64 (40.5)
Can PDD be prevented? 48 (30.4) 6 (3.8) 104 (65.8)
Do you believe that healthy birds may have ABV but not show any signs or symptoms? 72 (45.6) 2 (1.3) 84 (53.2)
Do you believe that healthy birds with ABV without showing clinical signs may infect other birds? 82 (51.9) 2 (1.3) 74 (46.8)
Should a bird suspected of PDD or having PDD-like symptoms be isolated or quarantined from others? 120 (75.9) 4 (2.5) 34 (21.5)
Will you seek the advice of a veterinarian if your bird has PDD-like symptoms? 126 (79.7) 12 (7.6) 20 (12.7)
Do you carry out regular health checks on your bird? 108 (68.4) 44 (27.8) 6 (3.8)
Should you carry out a health check on a new bird? 140 (88.6) 8 (5.1) 10 (6.3)

Comparison of Demographic characteristics and knowledge, attitude and practice scores

n (158) Knowledge score Attitude score Practicescore
P-value P-value P-value
18–30 36
31–40 98
Age 41–50 20 0.005 0.009 0.000
51–60 4
Male 136
Gender Female 22 0.273 0.766 0.243
Malay 130
Race Chinese 16 0.634 0.369 0.469
Indian 10
Characteristic Others 2
No formal education 0
Primary school 4
Education Secondary school 44 0.037 0.084 0.920
Matriculation/Foundation/College 28
University (Bachelors/Masters/Doctorate) 74
Other 8
Government 38
Private 64
Occupation Self-employed 44 0.322 0.529 0.000
Other 12
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