Prevalence of Avian Influenza in Live Bird Markets, Bird Gardens, and Zoos in Iran in 2015: A Cross-sectional Study

Document Type: Original Articles


1 Department of Poultry Viral Diseases, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

2 Department of Microbiology and Immunology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

3 Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

4 Department of Health and Management of Poultry Diseases, Iranian Veterinary Organization, Tehran, Iran

5 Animal Population Health Institute, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA


Avian Influenza (AI) H9N2 is endemic in Iran; therefore, it is necessary to estimate the disease prevalence among birds in live bird markets (LBMs) and assess the risk spread across the country. Accordingly, this study aimed to estimate the prevalence of AI subtypes in LBMs, bird gardens, and zoos during October and November 2015 in Iran and investigate the associated risk factors. Data related to independent variables for birds and premises were collected using a prepared questionnaire which included items about previously known potential risk factors associated with avian influenza infection. Serological testing was carried out to detect the antibodies against H5, H7, and H9. Regarding H5 and H7, the antigens H5N2 and H7N1 were used in this study. Positive samples on the first test were examined with the second antigens, namely H5N1 and H7N7. Moreover, sera with titers ≥4 (i.e. log2) were considered positive and premises with at least one positive bird were considered as positive units. In total, 87 premises were included in this cross-sectional study. Serum samples were examined utilizing hemagglutination inhibition, and RT-PCR was conducted on swab samples. Regarding the molecular test, the RNA was extracted using the High Pure Viral RNA Kit (Roche, Germany). In addition, real-time RT-PCR was conducted based on the described method. The seroprevalence rates of H9N2 were 83.9% and 31.8% at the premises and bird levels, respectively. Totally, 9.2% of pooled swab samples were positive for H9N2. However, all sera and swab samples were negative for H5 and H7. Hot and humid weather (OR=0.13, 95% CI 0.02 – 0.78) as well as bird-keeping condition (i.e., enclosed area) (OR=0.11, 95% CI 0.012 – 1.02) were protective factors for H9N2. High seroprevalence rate of H9 indicates that the disease is endemic in Iranian LBMs. Active surveillance must be carried out in LBMs, especially in the northern provinces of Iran. In addition, cleanliness and improved hygiene would be useful to prevent the spread of disease in LBMs.


Main Subjects

Article Title [French]

Prévalence de l'influenza Aviaire dans les Marchés, les Jardins d'Oiseaux Vivants et les Zoos Iraniens en 2015: une Analyse Transversale

Abstract [French]

L’influenza aviaire (IA) H9N2 est endémique en Iran; il est donc nécessaire d'estimer la prévalence de la maladie parmi les oiseaux sur les marchés d'oiseaux vivants (MOVs) et d'évaluer le risque réparti dans le pays. Dans ce but, cette étude visait à estimer la prévalence des sous-types d'IA dans les MOVs, les jardins d'oiseaux et les zoos iraniens en octobre et novembre 2015 ainsi qu’à étudier les facteurs de risque associés. Les données relatives aux variables indépendantes pour les oiseaux et les différents lieux concernés ont été collectées à l'aide d'un questionnaire comprenant des éléments sur les facteurs de risque potentiellement associés à l'infection par la grippe aviaire. Des tests sérologiques ont été effectués pour détecter les anticorps anti-H5, H7 et H9. En ce qui concerne H5 et H7, les antigènes H5N2 et H7N1 ont été utilisés dans cette étude. Les échantillons positifs du premier test ont été examinés avec les deuxièmes antigènes, à savoir H5N1 et H7N7. De plus, les sérums avec des titres ≥4 (c'est-à-dire log2) ont été considérés comme positifs et les lieux avec au moins un oiseau positif ont été considérés comme des unités positives. Au total, 87 locaux ont été inclus dans cette étude transversale. Les échantillons de sérum ont été examinés en utilisant l'inhibition de l'hémagglutination, et la RT-PCR a été réalisée par les échantillons sur écouvillon. En ce qui concerne le test moléculaire, l'ARN a été extrait à l'aide du Kit d'ARN Viral Très Pur (Roche, Allemagne). De plus, une RT-PCR en temps réel a été réalisée sur la base de la méthode décrite. Les taux de séroprévalence de H9N2 étaient respectivement de 83,9% et 31,8% aux niveaux des locaux et des oiseaux. Au total, 9,2% des échantillons collectés sur écouvillons étaient positifs pour H9N2. Cependant, tous les sérums et échantillons prélevés étaient négatifs pour H5 et H7. Le temps chaud et humide (OR = 0,13, IC 95%: 0,02 - 0,78) ainsi que les conditions d'élevage des oiseaux (c'est-à-dire, une zone fermée) (OR = 0,11, IC 95%, 0,012 - 1,02) étaient des facteurs de protection pour H9N2. Le taux élevé de séroprévalence de H9 indique que la maladie est endémique dans les LBM iraniens. Une surveillance active doit être effectuée dans les LBMs, en particulier dans les provinces du nord de l’Iran. De plus, la propreté et l'amélioration de l'hygiène seraient utiles pour prévenir la propagation de la maladie chez les LBMs.

Keywords [French]

  • Grippe Aviaire
  • Jardin d'oiseaux
  • Iran
  • Marché d'oiseaux vivants
  • Zoo (Parc zoologique)
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